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Predictors of COVID-19 Seropositivity Among Healthcare Workers: An Important Piece of an Incomplete Puzzle

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Predictors of COVID-19 Seropositivity Among Healthcare Workers: An Important Piece of an Incomplete Puzzle

SARS-CoV-2 seroprevalence studies of healthcare workers (HCWs) provide valuable insights into the excess risk of infection in this population and indirect evidence supporting the value of personal protective equipment (PPE) use. Seroprevalence estimates are composite measures of exposure risk and transmission mitigation both in the healthcare and community environments. The challenge of interpreting these studies arises from the diversity of HCW vocational roles and work settings in juxtaposition to heterogeneous community exposure risks. In this issue, two studies untangle some of these competing factors.

Investigators from Kashmir, India, assessed the relationship between seropositivity and specific HCW roles and work sites.1 They found a lower seroprevalence among HCWs at hospitals dedicated to COVID patients, relative to non-COVID hospitals. This seemingly paradoxical finding likely results from a combination of vigilant PPE adherence enforced through a buddy system, restrictive visitation policies, HCW residential dormitories reducing community exposure, and a spillover effect of careful in-hospital exposure avoidance practices on out-of-hospital behavior. A similar spillover effect has been hypothesized for low HCW seroprevalence relative to the surrounding community in California.2

In complement, researchers at a large New York City (NYC) hospital found higher overall HCW seropositivity rates compared with the community, though estimates were strikingly variable after detailed stratification by job function and location.3 The gradient of seroprevalence showed the highest risk among nurses and those in nonclinical, low-wage jobs (eg, patient transport, housekeeping), a finding also seen in another US study prior to adjustment for demographic and community factors.4 This finding highlights the association between socioeconomic status, structural community exposure risk factors such as multiple essential workers living within multigenerational households, and the challenges of sickness absenteeism. High seroprevalence among nurses and emergency department HCWs (who expeditiously evaluate many undifferentiated patients) may reflect both greater aggregate duration of exposure to infected patients and increased frequency of PPE donning and doffing, resulting in fatigue and diminished vigilance.5

A NYC-based study similarly showed high HCW seroprevalence, although no consistent associations with job function (albeit measured with less granularity) or community-based exposures were identified.6 Several studies comparing HCW to local community seropositivity rates have reached disparate conclusions.2,7 These contrasting data may result from variability in vigilance of PPE use, mask use in work rooms or during meals/breaktimes, sick leave policies driven by staffing demands, and neighborhood factors. In addition, selection biases and timing of blood sampling relative to viral transmission peaks (with differing degrees of temporal antibody waning) may contribute to the apparent discordance. In particular, comparative community-based samples vary greatly in their inclusion of asymptomatic patients, which can substantially affect such estimates by changing the denominator population.

We draw three conclusions: (1) Evidence for HCW exposure often tracks with community infection rates, suggesting that nonworkplace exposures are a dominant source of HCW seropositivity; (2) vigilant PPE use and assertively implemented protective measures unrelated to patient encounters can dramatically reduce infection risk, even among those with frequent exposures; and (3) HCW infection risk during future peaks can be effectively restrained with adequate resources and support, even in the presence of variants for which no effective vaccination or preventive pharmacotherapy exists. Given the divergent seroprevalence rates found in these studies after detailed stratification by job function and location, it is important for future studies to evaluate their relationship with infectious risk. Accurately quantifying the excess risks borne by HCWs may remain an elusive objective, but experiential knowledge offers numerous strategies worthy of proactive implementation to preserve HCW safety and well-being.

References

1. Khan M, Haq I, Qurieshi MA, et al. SARS-CoV-2 seroprevalence among healthcare workers by workplace exposure risk in Kashmir, India. J Hosp Med. 2021;16(5):274-281. https://doi.org/10.12788/jhm.3609
2. Brant-Zawadzki M, Fridman D, Robinson PA, et al. Prevalence and longevity of SARS-CoV-2 antibodies among health care workers. Open Forum Infect Dis. 2021;8(2):ofab015. https://doi.org/10.1093/ofid/ofab015
3. Purswani MU, Bucciarelli J, Tiburcio J. SARS-CoV-2 seroprevalence among healthcare workers by job function and work location in a New York inner-city hospital. J Hosp Med. 2021;16(5):274-281. https://doi.org/10.12788/jhm.3627
4. Jacob JT, Baker JM, Fridkin SK, et al. Risk factors associated with SARS-CoV-2 seropositivity among US health care personnel. JAMA Netw Open. 2021;4(3):e211283. https://doi.org/10.1001/jamanetworkopen.2021.1283
5. Ruhnke GW. COVID-19 diagnostic testing and the psychology of precautions fatigue. Cleve Clin J Med. 2020;88(1):19-21. https://doi.org/10.3949/ccjm.88a.20086
6. Venugopal U, Jilani N, Rabah S, et al. SARS-CoV-2 seroprevalence among health care workers in a New York City hospital: A cross-sectional analysis during the COVID-19 pandemic. Int J Infect Dis. 2021(1);102:63-69. https://doi.org/10.1016/j.ijid.2020.10.0367. Galanis P, Vraka I, Fragkou D, Bilali A, Kaitelidou D. Seroprevalence of SARS-CoV-2 antibodies and associated factors in healthcare workers: a systematic review and meta-analysis. J Hosp Infect. 2021;108:120-134. https://doi.org/10.1016/j.jhin.2020.11.008

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1Section of Hospital Medicine, Department of Medicine, University of Chicago, Chicago, Illinois; 2Division of Infectious Diseases, Hospital of the University of Pennsylvania, Philadelphia, Pennsylvania.

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SARS-CoV-2 seroprevalence studies of healthcare workers (HCWs) provide valuable insights into the excess risk of infection in this population and indirect evidence supporting the value of personal protective equipment (PPE) use. Seroprevalence estimates are composite measures of exposure risk and transmission mitigation both in the healthcare and community environments. The challenge of interpreting these studies arises from the diversity of HCW vocational roles and work settings in juxtaposition to heterogeneous community exposure risks. In this issue, two studies untangle some of these competing factors.

Investigators from Kashmir, India, assessed the relationship between seropositivity and specific HCW roles and work sites.1 They found a lower seroprevalence among HCWs at hospitals dedicated to COVID patients, relative to non-COVID hospitals. This seemingly paradoxical finding likely results from a combination of vigilant PPE adherence enforced through a buddy system, restrictive visitation policies, HCW residential dormitories reducing community exposure, and a spillover effect of careful in-hospital exposure avoidance practices on out-of-hospital behavior. A similar spillover effect has been hypothesized for low HCW seroprevalence relative to the surrounding community in California.2

In complement, researchers at a large New York City (NYC) hospital found higher overall HCW seropositivity rates compared with the community, though estimates were strikingly variable after detailed stratification by job function and location.3 The gradient of seroprevalence showed the highest risk among nurses and those in nonclinical, low-wage jobs (eg, patient transport, housekeeping), a finding also seen in another US study prior to adjustment for demographic and community factors.4 This finding highlights the association between socioeconomic status, structural community exposure risk factors such as multiple essential workers living within multigenerational households, and the challenges of sickness absenteeism. High seroprevalence among nurses and emergency department HCWs (who expeditiously evaluate many undifferentiated patients) may reflect both greater aggregate duration of exposure to infected patients and increased frequency of PPE donning and doffing, resulting in fatigue and diminished vigilance.5

A NYC-based study similarly showed high HCW seroprevalence, although no consistent associations with job function (albeit measured with less granularity) or community-based exposures were identified.6 Several studies comparing HCW to local community seropositivity rates have reached disparate conclusions.2,7 These contrasting data may result from variability in vigilance of PPE use, mask use in work rooms or during meals/breaktimes, sick leave policies driven by staffing demands, and neighborhood factors. In addition, selection biases and timing of blood sampling relative to viral transmission peaks (with differing degrees of temporal antibody waning) may contribute to the apparent discordance. In particular, comparative community-based samples vary greatly in their inclusion of asymptomatic patients, which can substantially affect such estimates by changing the denominator population.

We draw three conclusions: (1) Evidence for HCW exposure often tracks with community infection rates, suggesting that nonworkplace exposures are a dominant source of HCW seropositivity; (2) vigilant PPE use and assertively implemented protective measures unrelated to patient encounters can dramatically reduce infection risk, even among those with frequent exposures; and (3) HCW infection risk during future peaks can be effectively restrained with adequate resources and support, even in the presence of variants for which no effective vaccination or preventive pharmacotherapy exists. Given the divergent seroprevalence rates found in these studies after detailed stratification by job function and location, it is important for future studies to evaluate their relationship with infectious risk. Accurately quantifying the excess risks borne by HCWs may remain an elusive objective, but experiential knowledge offers numerous strategies worthy of proactive implementation to preserve HCW safety and well-being.

SARS-CoV-2 seroprevalence studies of healthcare workers (HCWs) provide valuable insights into the excess risk of infection in this population and indirect evidence supporting the value of personal protective equipment (PPE) use. Seroprevalence estimates are composite measures of exposure risk and transmission mitigation both in the healthcare and community environments. The challenge of interpreting these studies arises from the diversity of HCW vocational roles and work settings in juxtaposition to heterogeneous community exposure risks. In this issue, two studies untangle some of these competing factors.

Investigators from Kashmir, India, assessed the relationship between seropositivity and specific HCW roles and work sites.1 They found a lower seroprevalence among HCWs at hospitals dedicated to COVID patients, relative to non-COVID hospitals. This seemingly paradoxical finding likely results from a combination of vigilant PPE adherence enforced through a buddy system, restrictive visitation policies, HCW residential dormitories reducing community exposure, and a spillover effect of careful in-hospital exposure avoidance practices on out-of-hospital behavior. A similar spillover effect has been hypothesized for low HCW seroprevalence relative to the surrounding community in California.2

In complement, researchers at a large New York City (NYC) hospital found higher overall HCW seropositivity rates compared with the community, though estimates were strikingly variable after detailed stratification by job function and location.3 The gradient of seroprevalence showed the highest risk among nurses and those in nonclinical, low-wage jobs (eg, patient transport, housekeeping), a finding also seen in another US study prior to adjustment for demographic and community factors.4 This finding highlights the association between socioeconomic status, structural community exposure risk factors such as multiple essential workers living within multigenerational households, and the challenges of sickness absenteeism. High seroprevalence among nurses and emergency department HCWs (who expeditiously evaluate many undifferentiated patients) may reflect both greater aggregate duration of exposure to infected patients and increased frequency of PPE donning and doffing, resulting in fatigue and diminished vigilance.5

A NYC-based study similarly showed high HCW seroprevalence, although no consistent associations with job function (albeit measured with less granularity) or community-based exposures were identified.6 Several studies comparing HCW to local community seropositivity rates have reached disparate conclusions.2,7 These contrasting data may result from variability in vigilance of PPE use, mask use in work rooms or during meals/breaktimes, sick leave policies driven by staffing demands, and neighborhood factors. In addition, selection biases and timing of blood sampling relative to viral transmission peaks (with differing degrees of temporal antibody waning) may contribute to the apparent discordance. In particular, comparative community-based samples vary greatly in their inclusion of asymptomatic patients, which can substantially affect such estimates by changing the denominator population.

We draw three conclusions: (1) Evidence for HCW exposure often tracks with community infection rates, suggesting that nonworkplace exposures are a dominant source of HCW seropositivity; (2) vigilant PPE use and assertively implemented protective measures unrelated to patient encounters can dramatically reduce infection risk, even among those with frequent exposures; and (3) HCW infection risk during future peaks can be effectively restrained with adequate resources and support, even in the presence of variants for which no effective vaccination or preventive pharmacotherapy exists. Given the divergent seroprevalence rates found in these studies after detailed stratification by job function and location, it is important for future studies to evaluate their relationship with infectious risk. Accurately quantifying the excess risks borne by HCWs may remain an elusive objective, but experiential knowledge offers numerous strategies worthy of proactive implementation to preserve HCW safety and well-being.

References

1. Khan M, Haq I, Qurieshi MA, et al. SARS-CoV-2 seroprevalence among healthcare workers by workplace exposure risk in Kashmir, India. J Hosp Med. 2021;16(5):274-281. https://doi.org/10.12788/jhm.3609
2. Brant-Zawadzki M, Fridman D, Robinson PA, et al. Prevalence and longevity of SARS-CoV-2 antibodies among health care workers. Open Forum Infect Dis. 2021;8(2):ofab015. https://doi.org/10.1093/ofid/ofab015
3. Purswani MU, Bucciarelli J, Tiburcio J. SARS-CoV-2 seroprevalence among healthcare workers by job function and work location in a New York inner-city hospital. J Hosp Med. 2021;16(5):274-281. https://doi.org/10.12788/jhm.3627
4. Jacob JT, Baker JM, Fridkin SK, et al. Risk factors associated with SARS-CoV-2 seropositivity among US health care personnel. JAMA Netw Open. 2021;4(3):e211283. https://doi.org/10.1001/jamanetworkopen.2021.1283
5. Ruhnke GW. COVID-19 diagnostic testing and the psychology of precautions fatigue. Cleve Clin J Med. 2020;88(1):19-21. https://doi.org/10.3949/ccjm.88a.20086
6. Venugopal U, Jilani N, Rabah S, et al. SARS-CoV-2 seroprevalence among health care workers in a New York City hospital: A cross-sectional analysis during the COVID-19 pandemic. Int J Infect Dis. 2021(1);102:63-69. https://doi.org/10.1016/j.ijid.2020.10.0367. Galanis P, Vraka I, Fragkou D, Bilali A, Kaitelidou D. Seroprevalence of SARS-CoV-2 antibodies and associated factors in healthcare workers: a systematic review and meta-analysis. J Hosp Infect. 2021;108:120-134. https://doi.org/10.1016/j.jhin.2020.11.008

References

1. Khan M, Haq I, Qurieshi MA, et al. SARS-CoV-2 seroprevalence among healthcare workers by workplace exposure risk in Kashmir, India. J Hosp Med. 2021;16(5):274-281. https://doi.org/10.12788/jhm.3609
2. Brant-Zawadzki M, Fridman D, Robinson PA, et al. Prevalence and longevity of SARS-CoV-2 antibodies among health care workers. Open Forum Infect Dis. 2021;8(2):ofab015. https://doi.org/10.1093/ofid/ofab015
3. Purswani MU, Bucciarelli J, Tiburcio J. SARS-CoV-2 seroprevalence among healthcare workers by job function and work location in a New York inner-city hospital. J Hosp Med. 2021;16(5):274-281. https://doi.org/10.12788/jhm.3627
4. Jacob JT, Baker JM, Fridkin SK, et al. Risk factors associated with SARS-CoV-2 seropositivity among US health care personnel. JAMA Netw Open. 2021;4(3):e211283. https://doi.org/10.1001/jamanetworkopen.2021.1283
5. Ruhnke GW. COVID-19 diagnostic testing and the psychology of precautions fatigue. Cleve Clin J Med. 2020;88(1):19-21. https://doi.org/10.3949/ccjm.88a.20086
6. Venugopal U, Jilani N, Rabah S, et al. SARS-CoV-2 seroprevalence among health care workers in a New York City hospital: A cross-sectional analysis during the COVID-19 pandemic. Int J Infect Dis. 2021(1);102:63-69. https://doi.org/10.1016/j.ijid.2020.10.0367. Galanis P, Vraka I, Fragkou D, Bilali A, Kaitelidou D. Seroprevalence of SARS-CoV-2 antibodies and associated factors in healthcare workers: a systematic review and meta-analysis. J Hosp Infect. 2021;108:120-134. https://doi.org/10.1016/j.jhin.2020.11.008

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Bronchiolitis: Less Is More, but Different Is Better

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Bronchiolitis: Less Is More, but Different Is Better

Bronchiolitis, the most common cause of hospital admission for infants, is responsible for more than $500 million in direct medical costs in the United States yearly. Recent efforts have focused on what can be safely avoided when caring for patients with bronchiolitis (eg, continuous pulse oximetry, bronchodilator administration). While there remains substantial room for improvement in avoiding such low-value (or no-value) practices, the incremental improvements from these de-escalations will reach an asymptote over time. Further improvements in care and value must occur by doing things differently—not just simply doing less.

In this month’s Journal of Hospital Medicine, Ohlsen et al1 describe an intervention to decrease length of stay (LOS) for patients with bronchiolitis They employed an interrupted time series analysis to evaluate implementation of an observation unit and home oxygen therapy (OU-HOT) model of care and found that LOS dramatically decreased immediately following implementation. This reduction was maintained over 9 years. Use of home oxygen decreased over the study period, while LOS remained low, suggesting that the most important intervention was a structural one—the admission of patients to a unit dedicated to efficient discharge.

Observation units, staffed 24/7 with attending physicians, are well adapted to care for patients with illnesses like bronchiolitis, where hospitalization, though often needed, may be brief.2 These units are designed more like an emergency department than an inpatient unit, with protocolized care and the expectation of rapid turnover.

Multiple studies have shown that physician-related delays are a primary driver of delayed discharge from inpatient units. Such delays include delayed or variable clinical decision-making, inadequate communication of discharge criteria, and waiting to staff patients with an attending physician.3-5 Addressing these issues could allow inpatient units to function more like observation units for specific diagnoses. Standardization of care around specific diagnoses can make decision-making and discharge more efficient. In 2014, White et al4 showed that standardizing discharge criteria for specific diagnoses (including bronchiolitis) and embedding these criteria in admission order sets resulted in a significant decrease in LOS without affecting readmission rates or patient satisfaction.

To address the issues of attending availability, we may need to rethink rounding. The daily structure of inpatient rounding has not meaningfully changed since the 1950s. While there has been a push for increased morning discharges, this approach misses many patients whose illness course is evolving and who may be ready for discharge in the afternoon or evening.6 The current structure of morning rounds on medical teams is based on the need for resident education, supervision, and time available for attendings to complete administrative tasks and teaching in the afternoons. Structural change in patient care requires academic institutions to rethink what “being on service” actually means. Since LOS in these cases is brief, multiple days of clinical continuity may not be as beneficial as with other diagnoses. Further, there is no reason that daytime rounding teams are the only teams that can discharge patients. Telemedicine could also offer an opportunity for attending physicians to remotely determine whether a patient is discharge appropriate. Standardization of discharge criteria at admission could allow for trainees to discharge patients when they meet those criteria.

Perhaps we should begin to adapt our work structure to our patients’ needs, rather than the other way around. In pediatrics, we have already made traditional rounding more patient-focused through the practice of family-centered rounding. We should identify, as the authors have, ways to do things differently to make further improvements in care.

Ultimately, the success of this OU-HOT protocol demonstrates the power of structural interventions aimed at changing how we do things rather than just doing more (or less) of the same.

References

1. Ohlsen T, Knudson A, Korgenski EK, et al. Nine seasons of a bronchiolitis observation unit and home oxygen therapy protocol. J Hosp Med. 2021;16(5):261-267.
2. Plamann JM, Zedreck-Gonzalez J, Fennimore L. Creation of an adult observation unit: improving outcomes. J Nurs Care Qual. 2018;33(1):72-78. https://doi.org/10.1097/NCQ.0000000000000267
3. Zoucha J, Hull M, Keniston A, et al. Barriers to early hospital discharge: a cross-sectional study at five academic hospitals. J Hosp Med. 2018;13(12):816-822. https://doi.org/10.12788/jhm.3074
4. White CM, Statile AM, White DL, et al. Using quality improvement to optimise paediatric discharge efficiency. BMJ Qual Saf. 2014;23(5):428-436. https://doi.org/10.1136/bmjqs-2013-002556
5. Srivastava R, Stone BL, Patel R, et al. Delays in discharge in a tertiary care pediatric hospital. J Hosp Med. 2009;4(8):481-485. https://doi.org/10.1002/jhm.490
6. Gordon SA, Garber D, Taufique Z, et al. Improving on-time discharge in otolaryngology admissions. Otolaryngol Head Neck Surg. 2020;163(2):188-193. https://doi.org/10.1177/0194599819898910

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1Paul C Gaffney Division of Pediatric Hospital Medicine, Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania; 2Section of Hospital Medicine, Department of Medicine and Division of Pediatric Hospital Medicine, Department of Pediatrics, University of Minnesota Medical School, Minneapolis, Minnesota.

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1Paul C Gaffney Division of Pediatric Hospital Medicine, Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania; 2Section of Hospital Medicine, Department of Medicine and Division of Pediatric Hospital Medicine, Department of Pediatrics, University of Minnesota Medical School, Minneapolis, Minnesota.

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The authors have nothing to disclose.

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1Paul C Gaffney Division of Pediatric Hospital Medicine, Department of Pediatrics, University of Pittsburgh School of Medicine, Pittsburgh, Pennsylvania; 2Section of Hospital Medicine, Department of Medicine and Division of Pediatric Hospital Medicine, Department of Pediatrics, University of Minnesota Medical School, Minneapolis, Minnesota.

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Bronchiolitis, the most common cause of hospital admission for infants, is responsible for more than $500 million in direct medical costs in the United States yearly. Recent efforts have focused on what can be safely avoided when caring for patients with bronchiolitis (eg, continuous pulse oximetry, bronchodilator administration). While there remains substantial room for improvement in avoiding such low-value (or no-value) practices, the incremental improvements from these de-escalations will reach an asymptote over time. Further improvements in care and value must occur by doing things differently—not just simply doing less.

In this month’s Journal of Hospital Medicine, Ohlsen et al1 describe an intervention to decrease length of stay (LOS) for patients with bronchiolitis They employed an interrupted time series analysis to evaluate implementation of an observation unit and home oxygen therapy (OU-HOT) model of care and found that LOS dramatically decreased immediately following implementation. This reduction was maintained over 9 years. Use of home oxygen decreased over the study period, while LOS remained low, suggesting that the most important intervention was a structural one—the admission of patients to a unit dedicated to efficient discharge.

Observation units, staffed 24/7 with attending physicians, are well adapted to care for patients with illnesses like bronchiolitis, where hospitalization, though often needed, may be brief.2 These units are designed more like an emergency department than an inpatient unit, with protocolized care and the expectation of rapid turnover.

Multiple studies have shown that physician-related delays are a primary driver of delayed discharge from inpatient units. Such delays include delayed or variable clinical decision-making, inadequate communication of discharge criteria, and waiting to staff patients with an attending physician.3-5 Addressing these issues could allow inpatient units to function more like observation units for specific diagnoses. Standardization of care around specific diagnoses can make decision-making and discharge more efficient. In 2014, White et al4 showed that standardizing discharge criteria for specific diagnoses (including bronchiolitis) and embedding these criteria in admission order sets resulted in a significant decrease in LOS without affecting readmission rates or patient satisfaction.

To address the issues of attending availability, we may need to rethink rounding. The daily structure of inpatient rounding has not meaningfully changed since the 1950s. While there has been a push for increased morning discharges, this approach misses many patients whose illness course is evolving and who may be ready for discharge in the afternoon or evening.6 The current structure of morning rounds on medical teams is based on the need for resident education, supervision, and time available for attendings to complete administrative tasks and teaching in the afternoons. Structural change in patient care requires academic institutions to rethink what “being on service” actually means. Since LOS in these cases is brief, multiple days of clinical continuity may not be as beneficial as with other diagnoses. Further, there is no reason that daytime rounding teams are the only teams that can discharge patients. Telemedicine could also offer an opportunity for attending physicians to remotely determine whether a patient is discharge appropriate. Standardization of discharge criteria at admission could allow for trainees to discharge patients when they meet those criteria.

Perhaps we should begin to adapt our work structure to our patients’ needs, rather than the other way around. In pediatrics, we have already made traditional rounding more patient-focused through the practice of family-centered rounding. We should identify, as the authors have, ways to do things differently to make further improvements in care.

Ultimately, the success of this OU-HOT protocol demonstrates the power of structural interventions aimed at changing how we do things rather than just doing more (or less) of the same.

Bronchiolitis, the most common cause of hospital admission for infants, is responsible for more than $500 million in direct medical costs in the United States yearly. Recent efforts have focused on what can be safely avoided when caring for patients with bronchiolitis (eg, continuous pulse oximetry, bronchodilator administration). While there remains substantial room for improvement in avoiding such low-value (or no-value) practices, the incremental improvements from these de-escalations will reach an asymptote over time. Further improvements in care and value must occur by doing things differently—not just simply doing less.

In this month’s Journal of Hospital Medicine, Ohlsen et al1 describe an intervention to decrease length of stay (LOS) for patients with bronchiolitis They employed an interrupted time series analysis to evaluate implementation of an observation unit and home oxygen therapy (OU-HOT) model of care and found that LOS dramatically decreased immediately following implementation. This reduction was maintained over 9 years. Use of home oxygen decreased over the study period, while LOS remained low, suggesting that the most important intervention was a structural one—the admission of patients to a unit dedicated to efficient discharge.

Observation units, staffed 24/7 with attending physicians, are well adapted to care for patients with illnesses like bronchiolitis, where hospitalization, though often needed, may be brief.2 These units are designed more like an emergency department than an inpatient unit, with protocolized care and the expectation of rapid turnover.

Multiple studies have shown that physician-related delays are a primary driver of delayed discharge from inpatient units. Such delays include delayed or variable clinical decision-making, inadequate communication of discharge criteria, and waiting to staff patients with an attending physician.3-5 Addressing these issues could allow inpatient units to function more like observation units for specific diagnoses. Standardization of care around specific diagnoses can make decision-making and discharge more efficient. In 2014, White et al4 showed that standardizing discharge criteria for specific diagnoses (including bronchiolitis) and embedding these criteria in admission order sets resulted in a significant decrease in LOS without affecting readmission rates or patient satisfaction.

To address the issues of attending availability, we may need to rethink rounding. The daily structure of inpatient rounding has not meaningfully changed since the 1950s. While there has been a push for increased morning discharges, this approach misses many patients whose illness course is evolving and who may be ready for discharge in the afternoon or evening.6 The current structure of morning rounds on medical teams is based on the need for resident education, supervision, and time available for attendings to complete administrative tasks and teaching in the afternoons. Structural change in patient care requires academic institutions to rethink what “being on service” actually means. Since LOS in these cases is brief, multiple days of clinical continuity may not be as beneficial as with other diagnoses. Further, there is no reason that daytime rounding teams are the only teams that can discharge patients. Telemedicine could also offer an opportunity for attending physicians to remotely determine whether a patient is discharge appropriate. Standardization of discharge criteria at admission could allow for trainees to discharge patients when they meet those criteria.

Perhaps we should begin to adapt our work structure to our patients’ needs, rather than the other way around. In pediatrics, we have already made traditional rounding more patient-focused through the practice of family-centered rounding. We should identify, as the authors have, ways to do things differently to make further improvements in care.

Ultimately, the success of this OU-HOT protocol demonstrates the power of structural interventions aimed at changing how we do things rather than just doing more (or less) of the same.

References

1. Ohlsen T, Knudson A, Korgenski EK, et al. Nine seasons of a bronchiolitis observation unit and home oxygen therapy protocol. J Hosp Med. 2021;16(5):261-267.
2. Plamann JM, Zedreck-Gonzalez J, Fennimore L. Creation of an adult observation unit: improving outcomes. J Nurs Care Qual. 2018;33(1):72-78. https://doi.org/10.1097/NCQ.0000000000000267
3. Zoucha J, Hull M, Keniston A, et al. Barriers to early hospital discharge: a cross-sectional study at five academic hospitals. J Hosp Med. 2018;13(12):816-822. https://doi.org/10.12788/jhm.3074
4. White CM, Statile AM, White DL, et al. Using quality improvement to optimise paediatric discharge efficiency. BMJ Qual Saf. 2014;23(5):428-436. https://doi.org/10.1136/bmjqs-2013-002556
5. Srivastava R, Stone BL, Patel R, et al. Delays in discharge in a tertiary care pediatric hospital. J Hosp Med. 2009;4(8):481-485. https://doi.org/10.1002/jhm.490
6. Gordon SA, Garber D, Taufique Z, et al. Improving on-time discharge in otolaryngology admissions. Otolaryngol Head Neck Surg. 2020;163(2):188-193. https://doi.org/10.1177/0194599819898910

References

1. Ohlsen T, Knudson A, Korgenski EK, et al. Nine seasons of a bronchiolitis observation unit and home oxygen therapy protocol. J Hosp Med. 2021;16(5):261-267.
2. Plamann JM, Zedreck-Gonzalez J, Fennimore L. Creation of an adult observation unit: improving outcomes. J Nurs Care Qual. 2018;33(1):72-78. https://doi.org/10.1097/NCQ.0000000000000267
3. Zoucha J, Hull M, Keniston A, et al. Barriers to early hospital discharge: a cross-sectional study at five academic hospitals. J Hosp Med. 2018;13(12):816-822. https://doi.org/10.12788/jhm.3074
4. White CM, Statile AM, White DL, et al. Using quality improvement to optimise paediatric discharge efficiency. BMJ Qual Saf. 2014;23(5):428-436. https://doi.org/10.1136/bmjqs-2013-002556
5. Srivastava R, Stone BL, Patel R, et al. Delays in discharge in a tertiary care pediatric hospital. J Hosp Med. 2009;4(8):481-485. https://doi.org/10.1002/jhm.490
6. Gordon SA, Garber D, Taufique Z, et al. Improving on-time discharge in otolaryngology admissions. Otolaryngol Head Neck Surg. 2020;163(2):188-193. https://doi.org/10.1177/0194599819898910

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Le Petit Prince: Lessons From a Beloved Fable for Our Current Time

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”Good evening,“ said the little prince politely.

”Good evening,“ said the snake.

”What planet have I fallen on?“ asked the little prince.

”On the planet Earth, in Africa,“ replied the snake.

”Oh… Then there are no people on Earth?”

”This is the desert. There are no people in the desert. The Earth is big,“ said the snake.

The little prince sat down on a stone and looked up at the sky.

”I wonder,“ he said, “if the stars are lit up so that each of us can find his own star again. Look at my planet. It is right above us… But how far away is it?” 1

Le Petit Prince is one of the twentieth century’s most widely read fables.1 Written in 1943 by the French aviator and novelist Antoine de Saint-Exupéry, it tells the story of a young prince who inhabits a small planet in outer space with his muse, a fragile and dainty rose. The prince loves his rose and goes to great lengths to protect her, but her constant needs prove too much for him to bear. One day he decides to leave her and sets out on a journey across the universe. Along the way he stops at several different planets and interacts with their sole inhabitants, each of whom performs a bizarre and arguably pointless activity. The prince leaves each planet confused and despondent—for no place or person has proven more inspiring than his own planet or rose—until he arrives on Earth, where he meets a snake, a fox, and the novel’s unnamed narrator. Their company is a welcome relief for the travel-weary prince, who learns important lessons about love, friendship, and “matters of consequence.” Toward the novel’s end, the snake promises to deliver the little prince home if he allows himself to be bitten. The prince obliges in order to be with his rose, and he soon disappears. The story concludes with the narrator looking up at the stars, wondering if the prince is somewhere among them.

One interpretation of Le Petit Prince is that life is more beautiful when the things that give it meaning are recognized and cherished, but there is a heavy irony behind this theme. The story was published during one of the lowest points in the Second World War, when France was still in the grips of its German oppressors. Saint-Exupéry himself had fled to the United States years earlier and composed Le Petit Prince during a time of personal upheaval. In short, nothing about the context of the book’s birth seemed to inspire its rosy message.   

Now, almost 80 years after the first publication of Le Petit Prince, we find ourselves in a similarly jarring and unpredictable time. As calamitous global events unfold around us, it is difficult not to feel overwhelmed. For healthcare workers, the crush of patient care has made us feel vulnerable—first to a virus that might infect us and our loved ones, and second, to the overwhelming sense of despair when caring for patients who ultimately die despite our best efforts. Pandemics are a time of physical and social disruption, and while it has been 100 years since we experienced one like this, they are a repeated part of the history of life on our planet. What would the little prince see if he landed in our clinics, hospitals, nursing homes, testing centers, or vaccination facilities today? Would he observe patients saying good-bye to family members on tablets and cell phones because their loved ones are not allowed to visit in person? Would he see healthcare workers struggling to resuscitate dying patients in a crowded emergency department or intensive care unit? Would he see long lines of cars filled with people waiting for tests or vaccines? Would he see government officials and public health workers agonizing over decisions about steps that could reduce spread but impose economic hardship on many?

There has been much debate about whether Le Petit Prince is a children’s story or a message for adults disguised as a children’s fable. Perhaps the answer is that it is both, for many children’s stories were actually written for adults. Despite the fragility and delicacy of the book, there is clearly a haunting and deep irony inherent in what it is, in effect, a most savage critique of the world at war.

Two themes that emerge in the novel resonate widely now: isolation and death. Each character the little prince meets is alone, mirroring the long periods of social distancing we have experienced over the past year. And while death is never explicitly mentioned in the book, it seems to be lurking throughout, especially when the prince disappears from Earth after being bitten by the snake. Currently, we have almost become numb to the reported daily death counts—each one alone would have evoked outrage in more usual times. One might imagine that Saint-Exupéry wrote this fable in part to help people cope with the deaths of their loved ones.

And when you are comforted (time soothes all sorrows) you will be happy to have known me. You will always be my friend. You will want to laugh with me. And from time to time you will open your window, so, just for the pleasure of it ... And your friends will be astonished to see you laughing whilst gazing at the sky! And so you will say to them, “Yes, stars always make me laugh!”

Over the past year, both authors of this essay have seen people turn to Le Petit Prince to cope with death. One of us observed a daughter reading the book to her mother at her intensive care bedside on the day she died. The other received a copy as thanks from the wife of a young man who died after 18 months of punishing chemotherapy for sarcoma. Inside the cover was a picture of her husband and the inscription, “Please share this book with someone you love—it’s meant to be read out loud—and remember James.” And so I did, with my grandson Sebastian, who listened to the story with the imagination, wonder, and curiosity of a 6-year-old—he had many questions.

Perhaps the fable that has comforted our patients and their families during their time of despair can do the same for us. Like the prince, who returns to his rose after a difficult journey, we might find solace in the people and things that give our lives their deepest meaning. Thereafter, we might return, rejuvenated, to the clinics, emergency departments, and inpatient wards where our daily work must continue. While the scale of the problems around us makes it feel like any step we take towards preserving our hope will be moot, Le Petit Prince teaches us there is value in making the effort. And there is even a chance that we will find, to our surprise, and against our more cynical judgment, a small rose pushing itself up towards the light.  

Acknowledgments

The authors thank Rita Charon (Columbia University), Pam Hartzband (Harvard University), Raphael Rush (University of Toronto), and Emily Silverman (University of California San Francisco) for their comments on earlier versions of this essay. None were compensated. We thank Sebastian, James’ wife, and our other patient’s daughter for giving permission to include them in the story.

References

1. de Saint-Exupéry A. The Little Prince. Harcourt Brace; 1961.

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Dr Detsky reports that he will receive stocks in the future from Bindle Systems for serving on the company’s Scientific Advisory Board; receiving consulting fees from Telus for serving on the company’s Medical Advisory Committee for Pandemic Planning; and owning stock in Pfizer, Astra Zeneca, and Johnson & Johnson.

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Dr Detsky reports that he will receive stocks in the future from Bindle Systems for serving on the company’s Scientific Advisory Board; receiving consulting fees from Telus for serving on the company’s Medical Advisory Committee for Pandemic Planning; and owning stock in Pfizer, Astra Zeneca, and Johnson & Johnson.

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1Interdepartmental Division of Critical Care Medicine, University of Toronto, Toronto, Ontario, Canada; 2Institute for Health Policy, Management, and Evaluation, and Department of Medicine, University of Toronto; and Department of Medicine, Mount Sinai Hospital and University Health Network, Toronto, Ontario, Canada.

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Dr Detsky reports that he will receive stocks in the future from Bindle Systems for serving on the company’s Scientific Advisory Board; receiving consulting fees from Telus for serving on the company’s Medical Advisory Committee for Pandemic Planning; and owning stock in Pfizer, Astra Zeneca, and Johnson & Johnson.

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”Good evening,“ said the little prince politely.

”Good evening,“ said the snake.

”What planet have I fallen on?“ asked the little prince.

”On the planet Earth, in Africa,“ replied the snake.

”Oh… Then there are no people on Earth?”

”This is the desert. There are no people in the desert. The Earth is big,“ said the snake.

The little prince sat down on a stone and looked up at the sky.

”I wonder,“ he said, “if the stars are lit up so that each of us can find his own star again. Look at my planet. It is right above us… But how far away is it?” 1

Le Petit Prince is one of the twentieth century’s most widely read fables.1 Written in 1943 by the French aviator and novelist Antoine de Saint-Exupéry, it tells the story of a young prince who inhabits a small planet in outer space with his muse, a fragile and dainty rose. The prince loves his rose and goes to great lengths to protect her, but her constant needs prove too much for him to bear. One day he decides to leave her and sets out on a journey across the universe. Along the way he stops at several different planets and interacts with their sole inhabitants, each of whom performs a bizarre and arguably pointless activity. The prince leaves each planet confused and despondent—for no place or person has proven more inspiring than his own planet or rose—until he arrives on Earth, where he meets a snake, a fox, and the novel’s unnamed narrator. Their company is a welcome relief for the travel-weary prince, who learns important lessons about love, friendship, and “matters of consequence.” Toward the novel’s end, the snake promises to deliver the little prince home if he allows himself to be bitten. The prince obliges in order to be with his rose, and he soon disappears. The story concludes with the narrator looking up at the stars, wondering if the prince is somewhere among them.

One interpretation of Le Petit Prince is that life is more beautiful when the things that give it meaning are recognized and cherished, but there is a heavy irony behind this theme. The story was published during one of the lowest points in the Second World War, when France was still in the grips of its German oppressors. Saint-Exupéry himself had fled to the United States years earlier and composed Le Petit Prince during a time of personal upheaval. In short, nothing about the context of the book’s birth seemed to inspire its rosy message.   

Now, almost 80 years after the first publication of Le Petit Prince, we find ourselves in a similarly jarring and unpredictable time. As calamitous global events unfold around us, it is difficult not to feel overwhelmed. For healthcare workers, the crush of patient care has made us feel vulnerable—first to a virus that might infect us and our loved ones, and second, to the overwhelming sense of despair when caring for patients who ultimately die despite our best efforts. Pandemics are a time of physical and social disruption, and while it has been 100 years since we experienced one like this, they are a repeated part of the history of life on our planet. What would the little prince see if he landed in our clinics, hospitals, nursing homes, testing centers, or vaccination facilities today? Would he observe patients saying good-bye to family members on tablets and cell phones because their loved ones are not allowed to visit in person? Would he see healthcare workers struggling to resuscitate dying patients in a crowded emergency department or intensive care unit? Would he see long lines of cars filled with people waiting for tests or vaccines? Would he see government officials and public health workers agonizing over decisions about steps that could reduce spread but impose economic hardship on many?

There has been much debate about whether Le Petit Prince is a children’s story or a message for adults disguised as a children’s fable. Perhaps the answer is that it is both, for many children’s stories were actually written for adults. Despite the fragility and delicacy of the book, there is clearly a haunting and deep irony inherent in what it is, in effect, a most savage critique of the world at war.

Two themes that emerge in the novel resonate widely now: isolation and death. Each character the little prince meets is alone, mirroring the long periods of social distancing we have experienced over the past year. And while death is never explicitly mentioned in the book, it seems to be lurking throughout, especially when the prince disappears from Earth after being bitten by the snake. Currently, we have almost become numb to the reported daily death counts—each one alone would have evoked outrage in more usual times. One might imagine that Saint-Exupéry wrote this fable in part to help people cope with the deaths of their loved ones.

And when you are comforted (time soothes all sorrows) you will be happy to have known me. You will always be my friend. You will want to laugh with me. And from time to time you will open your window, so, just for the pleasure of it ... And your friends will be astonished to see you laughing whilst gazing at the sky! And so you will say to them, “Yes, stars always make me laugh!”

Over the past year, both authors of this essay have seen people turn to Le Petit Prince to cope with death. One of us observed a daughter reading the book to her mother at her intensive care bedside on the day she died. The other received a copy as thanks from the wife of a young man who died after 18 months of punishing chemotherapy for sarcoma. Inside the cover was a picture of her husband and the inscription, “Please share this book with someone you love—it’s meant to be read out loud—and remember James.” And so I did, with my grandson Sebastian, who listened to the story with the imagination, wonder, and curiosity of a 6-year-old—he had many questions.

Perhaps the fable that has comforted our patients and their families during their time of despair can do the same for us. Like the prince, who returns to his rose after a difficult journey, we might find solace in the people and things that give our lives their deepest meaning. Thereafter, we might return, rejuvenated, to the clinics, emergency departments, and inpatient wards where our daily work must continue. While the scale of the problems around us makes it feel like any step we take towards preserving our hope will be moot, Le Petit Prince teaches us there is value in making the effort. And there is even a chance that we will find, to our surprise, and against our more cynical judgment, a small rose pushing itself up towards the light.  

Acknowledgments

The authors thank Rita Charon (Columbia University), Pam Hartzband (Harvard University), Raphael Rush (University of Toronto), and Emily Silverman (University of California San Francisco) for their comments on earlier versions of this essay. None were compensated. We thank Sebastian, James’ wife, and our other patient’s daughter for giving permission to include them in the story.

”Good evening,“ said the little prince politely.

”Good evening,“ said the snake.

”What planet have I fallen on?“ asked the little prince.

”On the planet Earth, in Africa,“ replied the snake.

”Oh… Then there are no people on Earth?”

”This is the desert. There are no people in the desert. The Earth is big,“ said the snake.

The little prince sat down on a stone and looked up at the sky.

”I wonder,“ he said, “if the stars are lit up so that each of us can find his own star again. Look at my planet. It is right above us… But how far away is it?” 1

Le Petit Prince is one of the twentieth century’s most widely read fables.1 Written in 1943 by the French aviator and novelist Antoine de Saint-Exupéry, it tells the story of a young prince who inhabits a small planet in outer space with his muse, a fragile and dainty rose. The prince loves his rose and goes to great lengths to protect her, but her constant needs prove too much for him to bear. One day he decides to leave her and sets out on a journey across the universe. Along the way he stops at several different planets and interacts with their sole inhabitants, each of whom performs a bizarre and arguably pointless activity. The prince leaves each planet confused and despondent—for no place or person has proven more inspiring than his own planet or rose—until he arrives on Earth, where he meets a snake, a fox, and the novel’s unnamed narrator. Their company is a welcome relief for the travel-weary prince, who learns important lessons about love, friendship, and “matters of consequence.” Toward the novel’s end, the snake promises to deliver the little prince home if he allows himself to be bitten. The prince obliges in order to be with his rose, and he soon disappears. The story concludes with the narrator looking up at the stars, wondering if the prince is somewhere among them.

One interpretation of Le Petit Prince is that life is more beautiful when the things that give it meaning are recognized and cherished, but there is a heavy irony behind this theme. The story was published during one of the lowest points in the Second World War, when France was still in the grips of its German oppressors. Saint-Exupéry himself had fled to the United States years earlier and composed Le Petit Prince during a time of personal upheaval. In short, nothing about the context of the book’s birth seemed to inspire its rosy message.   

Now, almost 80 years after the first publication of Le Petit Prince, we find ourselves in a similarly jarring and unpredictable time. As calamitous global events unfold around us, it is difficult not to feel overwhelmed. For healthcare workers, the crush of patient care has made us feel vulnerable—first to a virus that might infect us and our loved ones, and second, to the overwhelming sense of despair when caring for patients who ultimately die despite our best efforts. Pandemics are a time of physical and social disruption, and while it has been 100 years since we experienced one like this, they are a repeated part of the history of life on our planet. What would the little prince see if he landed in our clinics, hospitals, nursing homes, testing centers, or vaccination facilities today? Would he observe patients saying good-bye to family members on tablets and cell phones because their loved ones are not allowed to visit in person? Would he see healthcare workers struggling to resuscitate dying patients in a crowded emergency department or intensive care unit? Would he see long lines of cars filled with people waiting for tests or vaccines? Would he see government officials and public health workers agonizing over decisions about steps that could reduce spread but impose economic hardship on many?

There has been much debate about whether Le Petit Prince is a children’s story or a message for adults disguised as a children’s fable. Perhaps the answer is that it is both, for many children’s stories were actually written for adults. Despite the fragility and delicacy of the book, there is clearly a haunting and deep irony inherent in what it is, in effect, a most savage critique of the world at war.

Two themes that emerge in the novel resonate widely now: isolation and death. Each character the little prince meets is alone, mirroring the long periods of social distancing we have experienced over the past year. And while death is never explicitly mentioned in the book, it seems to be lurking throughout, especially when the prince disappears from Earth after being bitten by the snake. Currently, we have almost become numb to the reported daily death counts—each one alone would have evoked outrage in more usual times. One might imagine that Saint-Exupéry wrote this fable in part to help people cope with the deaths of their loved ones.

And when you are comforted (time soothes all sorrows) you will be happy to have known me. You will always be my friend. You will want to laugh with me. And from time to time you will open your window, so, just for the pleasure of it ... And your friends will be astonished to see you laughing whilst gazing at the sky! And so you will say to them, “Yes, stars always make me laugh!”

Over the past year, both authors of this essay have seen people turn to Le Petit Prince to cope with death. One of us observed a daughter reading the book to her mother at her intensive care bedside on the day she died. The other received a copy as thanks from the wife of a young man who died after 18 months of punishing chemotherapy for sarcoma. Inside the cover was a picture of her husband and the inscription, “Please share this book with someone you love—it’s meant to be read out loud—and remember James.” And so I did, with my grandson Sebastian, who listened to the story with the imagination, wonder, and curiosity of a 6-year-old—he had many questions.

Perhaps the fable that has comforted our patients and their families during their time of despair can do the same for us. Like the prince, who returns to his rose after a difficult journey, we might find solace in the people and things that give our lives their deepest meaning. Thereafter, we might return, rejuvenated, to the clinics, emergency departments, and inpatient wards where our daily work must continue. While the scale of the problems around us makes it feel like any step we take towards preserving our hope will be moot, Le Petit Prince teaches us there is value in making the effort. And there is even a chance that we will find, to our surprise, and against our more cynical judgment, a small rose pushing itself up towards the light.  

Acknowledgments

The authors thank Rita Charon (Columbia University), Pam Hartzband (Harvard University), Raphael Rush (University of Toronto), and Emily Silverman (University of California San Francisco) for their comments on earlier versions of this essay. None were compensated. We thank Sebastian, James’ wife, and our other patient’s daughter for giving permission to include them in the story.

References

1. de Saint-Exupéry A. The Little Prince. Harcourt Brace; 1961.

References

1. de Saint-Exupéry A. The Little Prince. Harcourt Brace; 1961.

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Respiratory Illness Presenteeism in Academic Medicine: A Conceivable COVID-19 Culture Change for the Better

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Respiratory Illness Presenteeism in Academic Medicine: A Conceivable COVID-19 Culture Change for the Better

An intern is rotating on a medical ward in January 2018. Influenza is prevalent and hospital admissions are increasing daily. Despite receiving her influenza vaccine in October 2017, she develops fevers and myalgias. Due to time constraints, she does not get tested for influenza. She instead decides to work while sick to avoid payback of shifts.

She is now a hematology/oncology fellow in December 2020. She and her colleagues experienced the harrowing first wave of the COVID-19 pandemic. Unfortunately, community prevalence and hospital admissions are again rising. She adheres to mandatory masking and eye protection at work. Two days after attending a procedural workshop with lunch provided, she develops headache, myalgias, and sore throat. She contacts her supervisor, calls out sick, and initiates home isolation due to a positive result on a COVID-19 test performed through occupational health services (OHS). No patients are affected, but multiple colleagues are required to quarantine and others are pulled to provide coverage.

PRESENTEEISM

Presenteeism, the act of attending work despite personal illness, can adversely affect individuals and organizations.1 In a healthcare setting, transmissible illnesses contribute to complications in patients and missed workdays for staff. Prior to the pandemic, the rate of presenteeism among physicians was as high as 90%.2 Such presenteeism may have contributed to medical errors and decreased work efficiency.3,4 At our hospital in the Bronx, New York, a high annual prevalence of seasonal influenza fueled influenza clusters among patients and trainees, leading to presenteeism.

Our prior work on influenza-related practices in academic medicine revealed that 54% of trainees and 26% of program directors self-reported influenza-like illness (ILI) presenteeism. Drivers included desire to display a strong work ethic, desire not to burden colleagues, concern about colleagues’ negative perceptions, and knowledge gaps in influenza transmission.5

INFLUENCE OF THE COVID-19 PANDEMIC ON PRESENTEEISM

The COVID-19 pandemic has profoundly affected staffing models, infection prevention protocols, use of shared spaces, educational conferences, visitation policies, and other habitual healthcare practices. The experience of post-graduate training during a pandemic has resulted in important mindset and practice changes that may decrease presenteeism. However, health systems need robust mechanisms to accommodate appropriate work absences due to illness. We hypothesize that ILI/COVID-like illness presenteeism will decrease significantly for the following reasons, which will have positive and negative impacts on the organization and individual.

Shift in Accountability and Rewards

Our 2018 study revealed that presenteeism was motivated by a desire not to burden colleagues with extra clinical duties and to display conscientiousness. Despite a back-up call system, house staff were concerned about colleagues’ negative perceptions. Accountability was perceived as fulfilling one’s assigned clinical duties rather than protecting others from illness.

More recently, staff have experienced personal or family illness with COVID-19 or witnessed its rapid spread through the healthcare system. Forty-two percent (103 of 245) of our internal medicine residents had work absences resulting in 875 total missed workdays between February 29 and May 22, 2020. At the peak of the pandemic’s first wave in the spring of 2020, 16% (38 of 245) were out sick.6 We hypothesize that this experience resulted in a modified sense of accountability to peers and patients which manifested as a desire not to expose them to illness. Staying home while ill is now positively reinforced by supervisors, and presenteeism is recognized as harmful rather than commendable. However, increased utilization of the back-up call system to meet patient care demands is a secondary consequence.

Consequences of Exposures

While trainees and program faculty acknowledged that presenteeism puts patients and coworkers at risk,5 there was insufficient individual or institutional motivation to prevent it or fear its consequences pre-pandemic. An individual infected with influenza A may spread illness to one or two others, and several outpatient influenza treatments exist. Also, current trainees did not experience the prior respiratory viral pandemic (2009 H1N1 influenza A) as healthcare workers (HCWs).

In contrast, SARS-CoV-2 is more transmissible, with one infection resulting in two to three additional cases.7 Hence, mandatory quarantine and isolation policies are more stringent than those for influenza. While reinfection with SARS-CoV-2 is rare,8 HCWs can be exposed and quarantined multiple times, which potentially impacts paid sick leave for HCWs and elective-time for house staff pursuing fellowships. COVID-19 among HCWs also impacts secondary contacts, resulting in missed work and school days and strain on families. Hospital resource utilization for contact tracing and testing postexposure is significant. Unlike influenza, there are currently no oral antiviral treatments for outpatient COVID-19, and illness has been linked to chronic disabling symptoms.9 Finally, absences due to illness or quarantine may disrupt education, training, and fulfillment of competencies and experiences necessary for advancement.

We predict that these potentially sweeping consequences will reduce presenteeism. An important aspect of health system pandemic planning must include adequate staffing to account for work absences due to illness or quarantine.

Access to Occupational Health Services

Previously, staff reported barriers to seeking care from OHS. Therefore, this step was skipped, and HCWs managed their own symptoms, tested and treated each other for influenza, and returned to work at an arbitrary interval, without coordination with OHS protocols. OHS processes have since greatly improved. Employees with a COVID-19 exposure or concerning symptoms call the OHS hotline, are referred for same-day testing, and are given specific instructions regarding home quarantine or isolation and return to work. Follow-up to confirm fitness for duty is provided. In September 2020, an electronic screening tool assessing COVID-19 symptoms, exposures, and high-risk travel was implemented at our institution. Associates must present their clearance at hospital entrances.

Protection From Vaccine

Survey results indicated that all house staff and program faculty received the annual influenza vaccine.5 In New York State, public health regulations ensure a high rate of annual influenza vaccination among HCWs.10 It is possible that house staff did not perceive that ILI symptoms were caused by influenza after vaccination, and that vaccinated colleagues were at lower risk of illness. The influenza vaccine also has a well-established safety record, contributing to good uptake among HCWs.

At the time of writing of this article, HCWs have been prioritized for COVID-19 vaccination. Studies are in progress pertaining to the degree of protection after one dose, incidence of new infections after first and second doses, and secondary transmissions from vaccinated individuals. Vaccination is likely to influence HCW behaviors as well as occupational health policies. We suggest that the impact of COVID-19 vaccination on subsequent HCW presenteeism be given precedence in future studies.

Consistent Messaging and Communication

Prior to the pandemic, regular communication to staff on transmissible disease outbreaks scarcely occurred. Likewise, recurring training on infection prevention and personal protective equipment (PPE) protocols did not occur, and hospital policies regarding personal illness were not emphasized. Harms of presenteeism were infrequently addressed outside of nosocomial outbreaks. The pandemic has positively impacted communication from hospital leadership. Infection control and occupational health guidelines are continually revised and disseminated. Program directors send regular COVID-19 updates to trainees. The infectious diseases program director serves as a graduate medical education liaison to hospital leadership. All staff are regularly updated on evolving policies and given resources to assist with personal illness. While many positive practice changes have occurred, a decrease in presenteeism may exhaust sick coverage and compromise patient care. We suggest that health systems create safer work environments and ensure adequate staffing to accommodate illnesses and quarantines.

STRATEGIES TO CREATE SAFER WORK ENVIRONMENTS

  • Conduct recurring staff PPE simulations spanning a range of communicable illnesses.
  • Ensure adequate PPE for surge conditions.
  • Implement occupancy limits for shared spaces, distanced seating, staggered mealtimes, plexiglass barriers, and portable air-filtration systems in rooms lacking windows.
  • Invest in large-scale, serial testing of asymptomatic HCWs to identify early cases and enact quarantines prior to excess exposures.

STRATEGIES TO ADDRESS STAFFING CONSTRAINTS IN ACADEMIC MEDICAL CENTERS

  • Adopt nonpunitive coverage systems, reducing presenteeism by removing expectations to “pay-back” colleagues later.
  • Establish a third-party notification system, reducing strain on house staff to find coverage. This will enable strategic use of the jeopardy pool by training program leadership.
  • Establish a backup coverage pool populated by hospitalists and third-year residents who have completed fellowship match. Ideally, health systems should be prepared to compensate physicians for extra shifts.
  • Engage nondeployed physician assistants or nurse practitioners to provide coverage for residents on a per diem basis.
  • At a federal level, funding for trainee workforce expansion can occur to ensure staffing redundancy. The appropriate number of trainees should be determined by program leadership, balancing surge needs with education and autonomy. Likewise, training extensions due to COVID-related absences or deployments away from research or electives should be federally funded.
  • Inpatient and community COVID-19 surges can result in large-scale furloughs of HCWs; hospital leadership should expediently implement public health recommendations allowing fully immunized HCWs to work after exposures while maximally adhering to infection prevention protocols.

The COVID-19 pandemic has profoundly impacted academic medicine. It is imperative to explore solutions to balance workplace safety, education, and training with staffing constraints and patient care needs. Resource investment and executive leadership support are required to achieve this balance.

References

1. Webster RK, Liu R, Karimullina K, Hall I, Amlôt R, Rubin GJ. A systematic review of infectious illness Presenteeism: prevalence, reasons and risk factors. BMC Public Health. 2019;19:799. https://doi.org/10.1186/s12889-019-7138-x
2. Bergström G, Bodin L, Hagberg J, Aronsson G, Josephson M. Sickness presenteeism today, sickness absenteeism tomorrow? A prospective study on sickness presenteeism and future sickness absenteeism. J Occup Environ Med. 2009;51(6):629-638. https://doi.org/10.1097/JOM.0b013e3181a8281b
3. Al Nuhait M, Al Harbi K, Al Jarboa A, et al. Sickness presenteeism among health care providers in an academic tertiary care center in Riyadh. J Infect Public Health. 2017;10(6):711-715. https://doi.org/10.1016/j.jiph.2016.09.019
4. Brborovic H, Brborovic O. Patient safety culture shapes presenteeism and absenteeism: a cross-sectional study among Croatian healthcare workers. Arh Hig Rada Toksikol. 2017;68(3):185-189. https://doi.org/10.1515/aiht-2017-68-2957
5. Cowman K, Mittal J, Weston G, et al. Understanding drivers of influenza-like illness presenteeism within training programs: a survey of trainees and their program directors. Am J Infect Control. 2019;47(8):895-901. https://doi.org/10.1016/j.ajic.2019.02.004
6. Merkin R, Kruger A, Bhardwaj G, Kajita GR, Shapiro L, Galen BT. Internal medicine resident work absence during the COVID-19 pandemic at a large academic medical center in New York City. J Grad Med Educ. 2020;12(6):682-685. https://doi.org/10.4300/JGME-D-20-00657.1
7. Petersen E, Koopmans M, Go U, et al. Comparing SARS-CoV-2 with SARS-CoV and influenza pandemics. Lancet Infect Dis. 2020;20(9):e238-244. https://doi.org/10.1016/S1473-3099(20)30484-9
8. Reinfection with COVID-19. Centers for Disease Control and Prevention. Updated October 27, 2020. Accessed March 31, 2021. https://www.cdc.gov/coronavirus/2019-ncov/your-health/reinfection.html
9. Rubin R. As their numbers grow, COVID-19 “long haulers” stump experts. JAMA. 2020;324(14):1381-1383. https://doi.org/10.1001/jama.2020.17709
10. Regulation for prevention of influenza transmission by healthcare and residential facility and agency personnel. New York State Department of Health. Revised March 2021. Accessed December 7, 2020. https://www.health.ny.gov/diseases/communicable/influenza/seasonal/providers/prevention_of_influenza_transmission/

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1Department of Medicine, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, NY; 2Department of Medicine, Division of Infectious Diseases, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, NY.

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1Department of Medicine, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, NY; 2Department of Medicine, Division of Infectious Diseases, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, NY.

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1Department of Medicine, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, NY; 2Department of Medicine, Division of Infectious Diseases, Montefiore Medical Center, Albert Einstein College of Medicine, Bronx, NY.

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Related Articles

An intern is rotating on a medical ward in January 2018. Influenza is prevalent and hospital admissions are increasing daily. Despite receiving her influenza vaccine in October 2017, she develops fevers and myalgias. Due to time constraints, she does not get tested for influenza. She instead decides to work while sick to avoid payback of shifts.

She is now a hematology/oncology fellow in December 2020. She and her colleagues experienced the harrowing first wave of the COVID-19 pandemic. Unfortunately, community prevalence and hospital admissions are again rising. She adheres to mandatory masking and eye protection at work. Two days after attending a procedural workshop with lunch provided, she develops headache, myalgias, and sore throat. She contacts her supervisor, calls out sick, and initiates home isolation due to a positive result on a COVID-19 test performed through occupational health services (OHS). No patients are affected, but multiple colleagues are required to quarantine and others are pulled to provide coverage.

PRESENTEEISM

Presenteeism, the act of attending work despite personal illness, can adversely affect individuals and organizations.1 In a healthcare setting, transmissible illnesses contribute to complications in patients and missed workdays for staff. Prior to the pandemic, the rate of presenteeism among physicians was as high as 90%.2 Such presenteeism may have contributed to medical errors and decreased work efficiency.3,4 At our hospital in the Bronx, New York, a high annual prevalence of seasonal influenza fueled influenza clusters among patients and trainees, leading to presenteeism.

Our prior work on influenza-related practices in academic medicine revealed that 54% of trainees and 26% of program directors self-reported influenza-like illness (ILI) presenteeism. Drivers included desire to display a strong work ethic, desire not to burden colleagues, concern about colleagues’ negative perceptions, and knowledge gaps in influenza transmission.5

INFLUENCE OF THE COVID-19 PANDEMIC ON PRESENTEEISM

The COVID-19 pandemic has profoundly affected staffing models, infection prevention protocols, use of shared spaces, educational conferences, visitation policies, and other habitual healthcare practices. The experience of post-graduate training during a pandemic has resulted in important mindset and practice changes that may decrease presenteeism. However, health systems need robust mechanisms to accommodate appropriate work absences due to illness. We hypothesize that ILI/COVID-like illness presenteeism will decrease significantly for the following reasons, which will have positive and negative impacts on the organization and individual.

Shift in Accountability and Rewards

Our 2018 study revealed that presenteeism was motivated by a desire not to burden colleagues with extra clinical duties and to display conscientiousness. Despite a back-up call system, house staff were concerned about colleagues’ negative perceptions. Accountability was perceived as fulfilling one’s assigned clinical duties rather than protecting others from illness.

More recently, staff have experienced personal or family illness with COVID-19 or witnessed its rapid spread through the healthcare system. Forty-two percent (103 of 245) of our internal medicine residents had work absences resulting in 875 total missed workdays between February 29 and May 22, 2020. At the peak of the pandemic’s first wave in the spring of 2020, 16% (38 of 245) were out sick.6 We hypothesize that this experience resulted in a modified sense of accountability to peers and patients which manifested as a desire not to expose them to illness. Staying home while ill is now positively reinforced by supervisors, and presenteeism is recognized as harmful rather than commendable. However, increased utilization of the back-up call system to meet patient care demands is a secondary consequence.

Consequences of Exposures

While trainees and program faculty acknowledged that presenteeism puts patients and coworkers at risk,5 there was insufficient individual or institutional motivation to prevent it or fear its consequences pre-pandemic. An individual infected with influenza A may spread illness to one or two others, and several outpatient influenza treatments exist. Also, current trainees did not experience the prior respiratory viral pandemic (2009 H1N1 influenza A) as healthcare workers (HCWs).

In contrast, SARS-CoV-2 is more transmissible, with one infection resulting in two to three additional cases.7 Hence, mandatory quarantine and isolation policies are more stringent than those for influenza. While reinfection with SARS-CoV-2 is rare,8 HCWs can be exposed and quarantined multiple times, which potentially impacts paid sick leave for HCWs and elective-time for house staff pursuing fellowships. COVID-19 among HCWs also impacts secondary contacts, resulting in missed work and school days and strain on families. Hospital resource utilization for contact tracing and testing postexposure is significant. Unlike influenza, there are currently no oral antiviral treatments for outpatient COVID-19, and illness has been linked to chronic disabling symptoms.9 Finally, absences due to illness or quarantine may disrupt education, training, and fulfillment of competencies and experiences necessary for advancement.

We predict that these potentially sweeping consequences will reduce presenteeism. An important aspect of health system pandemic planning must include adequate staffing to account for work absences due to illness or quarantine.

Access to Occupational Health Services

Previously, staff reported barriers to seeking care from OHS. Therefore, this step was skipped, and HCWs managed their own symptoms, tested and treated each other for influenza, and returned to work at an arbitrary interval, without coordination with OHS protocols. OHS processes have since greatly improved. Employees with a COVID-19 exposure or concerning symptoms call the OHS hotline, are referred for same-day testing, and are given specific instructions regarding home quarantine or isolation and return to work. Follow-up to confirm fitness for duty is provided. In September 2020, an electronic screening tool assessing COVID-19 symptoms, exposures, and high-risk travel was implemented at our institution. Associates must present their clearance at hospital entrances.

Protection From Vaccine

Survey results indicated that all house staff and program faculty received the annual influenza vaccine.5 In New York State, public health regulations ensure a high rate of annual influenza vaccination among HCWs.10 It is possible that house staff did not perceive that ILI symptoms were caused by influenza after vaccination, and that vaccinated colleagues were at lower risk of illness. The influenza vaccine also has a well-established safety record, contributing to good uptake among HCWs.

At the time of writing of this article, HCWs have been prioritized for COVID-19 vaccination. Studies are in progress pertaining to the degree of protection after one dose, incidence of new infections after first and second doses, and secondary transmissions from vaccinated individuals. Vaccination is likely to influence HCW behaviors as well as occupational health policies. We suggest that the impact of COVID-19 vaccination on subsequent HCW presenteeism be given precedence in future studies.

Consistent Messaging and Communication

Prior to the pandemic, regular communication to staff on transmissible disease outbreaks scarcely occurred. Likewise, recurring training on infection prevention and personal protective equipment (PPE) protocols did not occur, and hospital policies regarding personal illness were not emphasized. Harms of presenteeism were infrequently addressed outside of nosocomial outbreaks. The pandemic has positively impacted communication from hospital leadership. Infection control and occupational health guidelines are continually revised and disseminated. Program directors send regular COVID-19 updates to trainees. The infectious diseases program director serves as a graduate medical education liaison to hospital leadership. All staff are regularly updated on evolving policies and given resources to assist with personal illness. While many positive practice changes have occurred, a decrease in presenteeism may exhaust sick coverage and compromise patient care. We suggest that health systems create safer work environments and ensure adequate staffing to accommodate illnesses and quarantines.

STRATEGIES TO CREATE SAFER WORK ENVIRONMENTS

  • Conduct recurring staff PPE simulations spanning a range of communicable illnesses.
  • Ensure adequate PPE for surge conditions.
  • Implement occupancy limits for shared spaces, distanced seating, staggered mealtimes, plexiglass barriers, and portable air-filtration systems in rooms lacking windows.
  • Invest in large-scale, serial testing of asymptomatic HCWs to identify early cases and enact quarantines prior to excess exposures.

STRATEGIES TO ADDRESS STAFFING CONSTRAINTS IN ACADEMIC MEDICAL CENTERS

  • Adopt nonpunitive coverage systems, reducing presenteeism by removing expectations to “pay-back” colleagues later.
  • Establish a third-party notification system, reducing strain on house staff to find coverage. This will enable strategic use of the jeopardy pool by training program leadership.
  • Establish a backup coverage pool populated by hospitalists and third-year residents who have completed fellowship match. Ideally, health systems should be prepared to compensate physicians for extra shifts.
  • Engage nondeployed physician assistants or nurse practitioners to provide coverage for residents on a per diem basis.
  • At a federal level, funding for trainee workforce expansion can occur to ensure staffing redundancy. The appropriate number of trainees should be determined by program leadership, balancing surge needs with education and autonomy. Likewise, training extensions due to COVID-related absences or deployments away from research or electives should be federally funded.
  • Inpatient and community COVID-19 surges can result in large-scale furloughs of HCWs; hospital leadership should expediently implement public health recommendations allowing fully immunized HCWs to work after exposures while maximally adhering to infection prevention protocols.

The COVID-19 pandemic has profoundly impacted academic medicine. It is imperative to explore solutions to balance workplace safety, education, and training with staffing constraints and patient care needs. Resource investment and executive leadership support are required to achieve this balance.

An intern is rotating on a medical ward in January 2018. Influenza is prevalent and hospital admissions are increasing daily. Despite receiving her influenza vaccine in October 2017, she develops fevers and myalgias. Due to time constraints, she does not get tested for influenza. She instead decides to work while sick to avoid payback of shifts.

She is now a hematology/oncology fellow in December 2020. She and her colleagues experienced the harrowing first wave of the COVID-19 pandemic. Unfortunately, community prevalence and hospital admissions are again rising. She adheres to mandatory masking and eye protection at work. Two days after attending a procedural workshop with lunch provided, she develops headache, myalgias, and sore throat. She contacts her supervisor, calls out sick, and initiates home isolation due to a positive result on a COVID-19 test performed through occupational health services (OHS). No patients are affected, but multiple colleagues are required to quarantine and others are pulled to provide coverage.

PRESENTEEISM

Presenteeism, the act of attending work despite personal illness, can adversely affect individuals and organizations.1 In a healthcare setting, transmissible illnesses contribute to complications in patients and missed workdays for staff. Prior to the pandemic, the rate of presenteeism among physicians was as high as 90%.2 Such presenteeism may have contributed to medical errors and decreased work efficiency.3,4 At our hospital in the Bronx, New York, a high annual prevalence of seasonal influenza fueled influenza clusters among patients and trainees, leading to presenteeism.

Our prior work on influenza-related practices in academic medicine revealed that 54% of trainees and 26% of program directors self-reported influenza-like illness (ILI) presenteeism. Drivers included desire to display a strong work ethic, desire not to burden colleagues, concern about colleagues’ negative perceptions, and knowledge gaps in influenza transmission.5

INFLUENCE OF THE COVID-19 PANDEMIC ON PRESENTEEISM

The COVID-19 pandemic has profoundly affected staffing models, infection prevention protocols, use of shared spaces, educational conferences, visitation policies, and other habitual healthcare practices. The experience of post-graduate training during a pandemic has resulted in important mindset and practice changes that may decrease presenteeism. However, health systems need robust mechanisms to accommodate appropriate work absences due to illness. We hypothesize that ILI/COVID-like illness presenteeism will decrease significantly for the following reasons, which will have positive and negative impacts on the organization and individual.

Shift in Accountability and Rewards

Our 2018 study revealed that presenteeism was motivated by a desire not to burden colleagues with extra clinical duties and to display conscientiousness. Despite a back-up call system, house staff were concerned about colleagues’ negative perceptions. Accountability was perceived as fulfilling one’s assigned clinical duties rather than protecting others from illness.

More recently, staff have experienced personal or family illness with COVID-19 or witnessed its rapid spread through the healthcare system. Forty-two percent (103 of 245) of our internal medicine residents had work absences resulting in 875 total missed workdays between February 29 and May 22, 2020. At the peak of the pandemic’s first wave in the spring of 2020, 16% (38 of 245) were out sick.6 We hypothesize that this experience resulted in a modified sense of accountability to peers and patients which manifested as a desire not to expose them to illness. Staying home while ill is now positively reinforced by supervisors, and presenteeism is recognized as harmful rather than commendable. However, increased utilization of the back-up call system to meet patient care demands is a secondary consequence.

Consequences of Exposures

While trainees and program faculty acknowledged that presenteeism puts patients and coworkers at risk,5 there was insufficient individual or institutional motivation to prevent it or fear its consequences pre-pandemic. An individual infected with influenza A may spread illness to one or two others, and several outpatient influenza treatments exist. Also, current trainees did not experience the prior respiratory viral pandemic (2009 H1N1 influenza A) as healthcare workers (HCWs).

In contrast, SARS-CoV-2 is more transmissible, with one infection resulting in two to three additional cases.7 Hence, mandatory quarantine and isolation policies are more stringent than those for influenza. While reinfection with SARS-CoV-2 is rare,8 HCWs can be exposed and quarantined multiple times, which potentially impacts paid sick leave for HCWs and elective-time for house staff pursuing fellowships. COVID-19 among HCWs also impacts secondary contacts, resulting in missed work and school days and strain on families. Hospital resource utilization for contact tracing and testing postexposure is significant. Unlike influenza, there are currently no oral antiviral treatments for outpatient COVID-19, and illness has been linked to chronic disabling symptoms.9 Finally, absences due to illness or quarantine may disrupt education, training, and fulfillment of competencies and experiences necessary for advancement.

We predict that these potentially sweeping consequences will reduce presenteeism. An important aspect of health system pandemic planning must include adequate staffing to account for work absences due to illness or quarantine.

Access to Occupational Health Services

Previously, staff reported barriers to seeking care from OHS. Therefore, this step was skipped, and HCWs managed their own symptoms, tested and treated each other for influenza, and returned to work at an arbitrary interval, without coordination with OHS protocols. OHS processes have since greatly improved. Employees with a COVID-19 exposure or concerning symptoms call the OHS hotline, are referred for same-day testing, and are given specific instructions regarding home quarantine or isolation and return to work. Follow-up to confirm fitness for duty is provided. In September 2020, an electronic screening tool assessing COVID-19 symptoms, exposures, and high-risk travel was implemented at our institution. Associates must present their clearance at hospital entrances.

Protection From Vaccine

Survey results indicated that all house staff and program faculty received the annual influenza vaccine.5 In New York State, public health regulations ensure a high rate of annual influenza vaccination among HCWs.10 It is possible that house staff did not perceive that ILI symptoms were caused by influenza after vaccination, and that vaccinated colleagues were at lower risk of illness. The influenza vaccine also has a well-established safety record, contributing to good uptake among HCWs.

At the time of writing of this article, HCWs have been prioritized for COVID-19 vaccination. Studies are in progress pertaining to the degree of protection after one dose, incidence of new infections after first and second doses, and secondary transmissions from vaccinated individuals. Vaccination is likely to influence HCW behaviors as well as occupational health policies. We suggest that the impact of COVID-19 vaccination on subsequent HCW presenteeism be given precedence in future studies.

Consistent Messaging and Communication

Prior to the pandemic, regular communication to staff on transmissible disease outbreaks scarcely occurred. Likewise, recurring training on infection prevention and personal protective equipment (PPE) protocols did not occur, and hospital policies regarding personal illness were not emphasized. Harms of presenteeism were infrequently addressed outside of nosocomial outbreaks. The pandemic has positively impacted communication from hospital leadership. Infection control and occupational health guidelines are continually revised and disseminated. Program directors send regular COVID-19 updates to trainees. The infectious diseases program director serves as a graduate medical education liaison to hospital leadership. All staff are regularly updated on evolving policies and given resources to assist with personal illness. While many positive practice changes have occurred, a decrease in presenteeism may exhaust sick coverage and compromise patient care. We suggest that health systems create safer work environments and ensure adequate staffing to accommodate illnesses and quarantines.

STRATEGIES TO CREATE SAFER WORK ENVIRONMENTS

  • Conduct recurring staff PPE simulations spanning a range of communicable illnesses.
  • Ensure adequate PPE for surge conditions.
  • Implement occupancy limits for shared spaces, distanced seating, staggered mealtimes, plexiglass barriers, and portable air-filtration systems in rooms lacking windows.
  • Invest in large-scale, serial testing of asymptomatic HCWs to identify early cases and enact quarantines prior to excess exposures.

STRATEGIES TO ADDRESS STAFFING CONSTRAINTS IN ACADEMIC MEDICAL CENTERS

  • Adopt nonpunitive coverage systems, reducing presenteeism by removing expectations to “pay-back” colleagues later.
  • Establish a third-party notification system, reducing strain on house staff to find coverage. This will enable strategic use of the jeopardy pool by training program leadership.
  • Establish a backup coverage pool populated by hospitalists and third-year residents who have completed fellowship match. Ideally, health systems should be prepared to compensate physicians for extra shifts.
  • Engage nondeployed physician assistants or nurse practitioners to provide coverage for residents on a per diem basis.
  • At a federal level, funding for trainee workforce expansion can occur to ensure staffing redundancy. The appropriate number of trainees should be determined by program leadership, balancing surge needs with education and autonomy. Likewise, training extensions due to COVID-related absences or deployments away from research or electives should be federally funded.
  • Inpatient and community COVID-19 surges can result in large-scale furloughs of HCWs; hospital leadership should expediently implement public health recommendations allowing fully immunized HCWs to work after exposures while maximally adhering to infection prevention protocols.

The COVID-19 pandemic has profoundly impacted academic medicine. It is imperative to explore solutions to balance workplace safety, education, and training with staffing constraints and patient care needs. Resource investment and executive leadership support are required to achieve this balance.

References

1. Webster RK, Liu R, Karimullina K, Hall I, Amlôt R, Rubin GJ. A systematic review of infectious illness Presenteeism: prevalence, reasons and risk factors. BMC Public Health. 2019;19:799. https://doi.org/10.1186/s12889-019-7138-x
2. Bergström G, Bodin L, Hagberg J, Aronsson G, Josephson M. Sickness presenteeism today, sickness absenteeism tomorrow? A prospective study on sickness presenteeism and future sickness absenteeism. J Occup Environ Med. 2009;51(6):629-638. https://doi.org/10.1097/JOM.0b013e3181a8281b
3. Al Nuhait M, Al Harbi K, Al Jarboa A, et al. Sickness presenteeism among health care providers in an academic tertiary care center in Riyadh. J Infect Public Health. 2017;10(6):711-715. https://doi.org/10.1016/j.jiph.2016.09.019
4. Brborovic H, Brborovic O. Patient safety culture shapes presenteeism and absenteeism: a cross-sectional study among Croatian healthcare workers. Arh Hig Rada Toksikol. 2017;68(3):185-189. https://doi.org/10.1515/aiht-2017-68-2957
5. Cowman K, Mittal J, Weston G, et al. Understanding drivers of influenza-like illness presenteeism within training programs: a survey of trainees and their program directors. Am J Infect Control. 2019;47(8):895-901. https://doi.org/10.1016/j.ajic.2019.02.004
6. Merkin R, Kruger A, Bhardwaj G, Kajita GR, Shapiro L, Galen BT. Internal medicine resident work absence during the COVID-19 pandemic at a large academic medical center in New York City. J Grad Med Educ. 2020;12(6):682-685. https://doi.org/10.4300/JGME-D-20-00657.1
7. Petersen E, Koopmans M, Go U, et al. Comparing SARS-CoV-2 with SARS-CoV and influenza pandemics. Lancet Infect Dis. 2020;20(9):e238-244. https://doi.org/10.1016/S1473-3099(20)30484-9
8. Reinfection with COVID-19. Centers for Disease Control and Prevention. Updated October 27, 2020. Accessed March 31, 2021. https://www.cdc.gov/coronavirus/2019-ncov/your-health/reinfection.html
9. Rubin R. As their numbers grow, COVID-19 “long haulers” stump experts. JAMA. 2020;324(14):1381-1383. https://doi.org/10.1001/jama.2020.17709
10. Regulation for prevention of influenza transmission by healthcare and residential facility and agency personnel. New York State Department of Health. Revised March 2021. Accessed December 7, 2020. https://www.health.ny.gov/diseases/communicable/influenza/seasonal/providers/prevention_of_influenza_transmission/

References

1. Webster RK, Liu R, Karimullina K, Hall I, Amlôt R, Rubin GJ. A systematic review of infectious illness Presenteeism: prevalence, reasons and risk factors. BMC Public Health. 2019;19:799. https://doi.org/10.1186/s12889-019-7138-x
2. Bergström G, Bodin L, Hagberg J, Aronsson G, Josephson M. Sickness presenteeism today, sickness absenteeism tomorrow? A prospective study on sickness presenteeism and future sickness absenteeism. J Occup Environ Med. 2009;51(6):629-638. https://doi.org/10.1097/JOM.0b013e3181a8281b
3. Al Nuhait M, Al Harbi K, Al Jarboa A, et al. Sickness presenteeism among health care providers in an academic tertiary care center in Riyadh. J Infect Public Health. 2017;10(6):711-715. https://doi.org/10.1016/j.jiph.2016.09.019
4. Brborovic H, Brborovic O. Patient safety culture shapes presenteeism and absenteeism: a cross-sectional study among Croatian healthcare workers. Arh Hig Rada Toksikol. 2017;68(3):185-189. https://doi.org/10.1515/aiht-2017-68-2957
5. Cowman K, Mittal J, Weston G, et al. Understanding drivers of influenza-like illness presenteeism within training programs: a survey of trainees and their program directors. Am J Infect Control. 2019;47(8):895-901. https://doi.org/10.1016/j.ajic.2019.02.004
6. Merkin R, Kruger A, Bhardwaj G, Kajita GR, Shapiro L, Galen BT. Internal medicine resident work absence during the COVID-19 pandemic at a large academic medical center in New York City. J Grad Med Educ. 2020;12(6):682-685. https://doi.org/10.4300/JGME-D-20-00657.1
7. Petersen E, Koopmans M, Go U, et al. Comparing SARS-CoV-2 with SARS-CoV and influenza pandemics. Lancet Infect Dis. 2020;20(9):e238-244. https://doi.org/10.1016/S1473-3099(20)30484-9
8. Reinfection with COVID-19. Centers for Disease Control and Prevention. Updated October 27, 2020. Accessed March 31, 2021. https://www.cdc.gov/coronavirus/2019-ncov/your-health/reinfection.html
9. Rubin R. As their numbers grow, COVID-19 “long haulers” stump experts. JAMA. 2020;324(14):1381-1383. https://doi.org/10.1001/jama.2020.17709
10. Regulation for prevention of influenza transmission by healthcare and residential facility and agency personnel. New York State Department of Health. Revised March 2021. Accessed December 7, 2020. https://www.health.ny.gov/diseases/communicable/influenza/seasonal/providers/prevention_of_influenza_transmission/

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Still Burning

A celebratory mood pervaded the last week of service for my ward team at the end of the academic year. As the attending, it was just another day, but it was hard not to be caught up in the general feeling of a milestone flying past. Like most days in a hospital, this one passed in a rhythm of alternating mundanity and crisis. Late in the afternoon, one of the residents called me to a bedside for help. Imagining that my diagnostic skills were urgently required, I took the stairs. The problem, as it turned out, was not strictly medical.

I could hear the yelling before I cleared the locked entry doors to the ward. It doesn’t really matter what the yelling was about, just that there is often yelling and there is always very little I can do about the root cause of it. As I stepped into the middle of the conflagration, I remembered the story an intern told me about the night earlier in the month when it fell to her to wheel the same patient’s intoxicated parent down to the emergency department. After sleeping it off, the parent was diagnosed with an “allergic reaction” and given a prescription for diphenhydramine. We all knew the diagnosis was fantasy, and yet we all went along with it because there was simply no help available for the root cause of the problem. State social services was already involved, and we had a “safety” plan in place for discharge. As meager as that may have been, we had done the best we could to balance the risk with the available resources… or so we told ourselves.

As a nation, we have chosen not to provide much of a social safety net for our citizens who suffer from addiction and/or mental illness and, most importantly, for those who’ve just not had a leg up on the economic ladder. As a hospital-based clinician, I know that people in distress lose their cool and yell sometimes. Ironically, they may yell most loudly at people who sincerely want to help, simply because others do not engage them. Medical schools don’t teach us how to handle the yelling, though many would say it is part of the hidden curriculum. One thing that distinguishes many pediatricians like myself is a willingness to listen to the yelling, to engage with it, and to try to help. Not surprisingly, our reputation around the hospital is that we skew a bit naive.

It is worth asking, though: Are pediatricians naive? Sure, we make funny faces. We clown. We baby-talk. Those things are largely true, but there are other true things about pediatricians. Chief among them is the fact that we come to know some of the worst things there are to know about human beings. Everybody knows people can be awful, but we know exactly how awful they are to defenseless children in precise detail. For instance, I’ve seen a 4-year-old who was repeatedly starved as a regular punishment. She was so hungry she ate her hair, which turned out to be lucky for her because it caused an intestinal blockage that led to the discovery of the abuse. I gave her an apple one day and she immediately hid it under her shirt. Where you see a scab on a child’s inner arm, I see a cigarette burn. I’ve resuscitated a baby whose parents dipped his pacifier in heroin to stop his crying—the remarkable part of the story being that it was heroin cooked in the hospital bathroom. And then there are the things that I cannot even bring myself to write down.

Carrying this knowledge hollows out a gap between pediatricians and the rest of the world. The divergence between our expectations of how a society should treat its children and the reality of our daily experience grinds away any naivete. The gap becomes a canyon for some of us. We live with the sense that nobody would believe the things we’ve seen, so we rarely talk about them. Years ago, I was testifying in a (for me) routine child-abuse case where this fact hit home. It is common for juries to disbelieve that a caregiver could do the things we allege. I say allege, but if you work as a pediatrician long enough, the space between allegation and fact narrows. It is simply pattern recognition to you—abuse happens so consistently that we accept it as a diagnostic category. The case in question was a submersion burn, which is an almost unmistakable pattern. The other piece of the story is that it happens to toddlers during toilet training as caregivers lose their self-control and punish children for soiling themselves. For me, simple pattern recognition; for the jury, simply unbelievable. We lost the case.

We are almost always losing the case as pediatricians. Spending on children makes up less than 10% of the federal budget, whereas spending on the elderly, including Social Security, Medicare, and the adult component of Medicaid, dominates that budget.1 Moreover, twice as many children as adults over age 65 are living in poverty in the United States. The Temporary Assistance for Needy Families program is often debated in this country and frequently criticized as wasteful. However, what is not debatable is that the allocated budget ($16.5 billion) hasn’t changed since 1996, resulting in a functional 40% decrease due to inflation.2 Life, for poor children, gets a little tougher every year.

After the resident and I wrapped up our day, we talked a little about how hard it is to witness some of the things you see in a children’s hospital. I could see the gap between her and the outside world widening right in front of me. In my weaker moments, I want to tell trainees like her to run while they can. I want to warn them that they don’t want to know so many of the things we’re going to teach them. I know how the story usually ends. I know that our country doesn’t promise children safety from social deprivation, hunger, or physical abuse. Instead, we’ve created the conditions for those things to occur at embarrassingly high rates, and we prosecute the unlucky after the fact. The children are simply collateral damage.

We stood at our patient’s bedside and tried to imagine a happy future. Even without his medical problems, he would likely need a major investment of resources in order to thrive. Where would those resources come from? I saw the hospital crib, metal bars on all sides and a thick plastic roof to prevent escape, as a metaphor. Later, I took the elevator down and overheard a snippet of conversation between two residents. One of them asked the other, “How do you know when you’ve burned out?” The other replied, “I don’t know, I guess when you’ve stopped burning.” Burnout is a hot topic in medicine, and some may assume the reasons are obvious: long hours and intellectually demanding work. In reality, those drivers may be less important than the repeated exposure to profound injustice inherent to the practice of medicine in our country.

As hospitalists, we address acute decompensation in our patients and send them back out into the world knowing there will soon be a next time. We also know that the next time might be preventable, if only … This cycle sometimes feels inexorable, but it can also prompt us to think about our obligation to work toward a more just society. We have to imagine a better future even as we struggle to believe it is on the way.

Most of our hospitals are trying to help. They have community-engagement programs, they purchase housing for homeless patients, they provide large amounts of uncompensated care and sometimes operate at a loss. Yet none of this addresses the root cause of the problem. Medicine, either in the form of an institution or a doctor, can’t replace a just society, but the truth of this fact does not mean we should not try.

Pediatrics has always been a field disposed toward advocacy. The origin of our largest professional organization in the United States was the intraprofessional conflict within the American Medical Association (AMA) over the Sheppard-Towner Act of 1921, one of this country’s first attempts to address the social determinants of health with legislation.3 The American Academy of Pediatrics was formed in 1930 after the AMA House of Delegates rebuked the Pediatric section for advocating for continuance of the act during the late 1920s.3 Perhaps what Pediatrics has to teach the rest of medicine is the necessity of making advocacy a part of our professional identity. And perhaps that’s the reason that so many pediatricians are still burning and not burned out.

References

1. Committee for a Responsible Federal Budget. Chartbook: budgeting for the next generation. October 11, 2018. Accessed February 2, 2021. http://www.crfb.org/papers/chartbook-budgeting-next-generation
2. Center on Budget and Policy Priorities. Policy basics: temporary assistance for needy families. Updated March 31, 2021. Accessed February 2, 2021. https://www.cbpp.org/research/family-income-support/temporary-assistance-for-needy-families
3. van Dyck PC. A history of child health equity legislation in the United States. Pediatrics. 2003;112(3 pt 2):727-730.

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A celebratory mood pervaded the last week of service for my ward team at the end of the academic year. As the attending, it was just another day, but it was hard not to be caught up in the general feeling of a milestone flying past. Like most days in a hospital, this one passed in a rhythm of alternating mundanity and crisis. Late in the afternoon, one of the residents called me to a bedside for help. Imagining that my diagnostic skills were urgently required, I took the stairs. The problem, as it turned out, was not strictly medical.

I could hear the yelling before I cleared the locked entry doors to the ward. It doesn’t really matter what the yelling was about, just that there is often yelling and there is always very little I can do about the root cause of it. As I stepped into the middle of the conflagration, I remembered the story an intern told me about the night earlier in the month when it fell to her to wheel the same patient’s intoxicated parent down to the emergency department. After sleeping it off, the parent was diagnosed with an “allergic reaction” and given a prescription for diphenhydramine. We all knew the diagnosis was fantasy, and yet we all went along with it because there was simply no help available for the root cause of the problem. State social services was already involved, and we had a “safety” plan in place for discharge. As meager as that may have been, we had done the best we could to balance the risk with the available resources… or so we told ourselves.

As a nation, we have chosen not to provide much of a social safety net for our citizens who suffer from addiction and/or mental illness and, most importantly, for those who’ve just not had a leg up on the economic ladder. As a hospital-based clinician, I know that people in distress lose their cool and yell sometimes. Ironically, they may yell most loudly at people who sincerely want to help, simply because others do not engage them. Medical schools don’t teach us how to handle the yelling, though many would say it is part of the hidden curriculum. One thing that distinguishes many pediatricians like myself is a willingness to listen to the yelling, to engage with it, and to try to help. Not surprisingly, our reputation around the hospital is that we skew a bit naive.

It is worth asking, though: Are pediatricians naive? Sure, we make funny faces. We clown. We baby-talk. Those things are largely true, but there are other true things about pediatricians. Chief among them is the fact that we come to know some of the worst things there are to know about human beings. Everybody knows people can be awful, but we know exactly how awful they are to defenseless children in precise detail. For instance, I’ve seen a 4-year-old who was repeatedly starved as a regular punishment. She was so hungry she ate her hair, which turned out to be lucky for her because it caused an intestinal blockage that led to the discovery of the abuse. I gave her an apple one day and she immediately hid it under her shirt. Where you see a scab on a child’s inner arm, I see a cigarette burn. I’ve resuscitated a baby whose parents dipped his pacifier in heroin to stop his crying—the remarkable part of the story being that it was heroin cooked in the hospital bathroom. And then there are the things that I cannot even bring myself to write down.

Carrying this knowledge hollows out a gap between pediatricians and the rest of the world. The divergence between our expectations of how a society should treat its children and the reality of our daily experience grinds away any naivete. The gap becomes a canyon for some of us. We live with the sense that nobody would believe the things we’ve seen, so we rarely talk about them. Years ago, I was testifying in a (for me) routine child-abuse case where this fact hit home. It is common for juries to disbelieve that a caregiver could do the things we allege. I say allege, but if you work as a pediatrician long enough, the space between allegation and fact narrows. It is simply pattern recognition to you—abuse happens so consistently that we accept it as a diagnostic category. The case in question was a submersion burn, which is an almost unmistakable pattern. The other piece of the story is that it happens to toddlers during toilet training as caregivers lose their self-control and punish children for soiling themselves. For me, simple pattern recognition; for the jury, simply unbelievable. We lost the case.

We are almost always losing the case as pediatricians. Spending on children makes up less than 10% of the federal budget, whereas spending on the elderly, including Social Security, Medicare, and the adult component of Medicaid, dominates that budget.1 Moreover, twice as many children as adults over age 65 are living in poverty in the United States. The Temporary Assistance for Needy Families program is often debated in this country and frequently criticized as wasteful. However, what is not debatable is that the allocated budget ($16.5 billion) hasn’t changed since 1996, resulting in a functional 40% decrease due to inflation.2 Life, for poor children, gets a little tougher every year.

After the resident and I wrapped up our day, we talked a little about how hard it is to witness some of the things you see in a children’s hospital. I could see the gap between her and the outside world widening right in front of me. In my weaker moments, I want to tell trainees like her to run while they can. I want to warn them that they don’t want to know so many of the things we’re going to teach them. I know how the story usually ends. I know that our country doesn’t promise children safety from social deprivation, hunger, or physical abuse. Instead, we’ve created the conditions for those things to occur at embarrassingly high rates, and we prosecute the unlucky after the fact. The children are simply collateral damage.

We stood at our patient’s bedside and tried to imagine a happy future. Even without his medical problems, he would likely need a major investment of resources in order to thrive. Where would those resources come from? I saw the hospital crib, metal bars on all sides and a thick plastic roof to prevent escape, as a metaphor. Later, I took the elevator down and overheard a snippet of conversation between two residents. One of them asked the other, “How do you know when you’ve burned out?” The other replied, “I don’t know, I guess when you’ve stopped burning.” Burnout is a hot topic in medicine, and some may assume the reasons are obvious: long hours and intellectually demanding work. In reality, those drivers may be less important than the repeated exposure to profound injustice inherent to the practice of medicine in our country.

As hospitalists, we address acute decompensation in our patients and send them back out into the world knowing there will soon be a next time. We also know that the next time might be preventable, if only … This cycle sometimes feels inexorable, but it can also prompt us to think about our obligation to work toward a more just society. We have to imagine a better future even as we struggle to believe it is on the way.

Most of our hospitals are trying to help. They have community-engagement programs, they purchase housing for homeless patients, they provide large amounts of uncompensated care and sometimes operate at a loss. Yet none of this addresses the root cause of the problem. Medicine, either in the form of an institution or a doctor, can’t replace a just society, but the truth of this fact does not mean we should not try.

Pediatrics has always been a field disposed toward advocacy. The origin of our largest professional organization in the United States was the intraprofessional conflict within the American Medical Association (AMA) over the Sheppard-Towner Act of 1921, one of this country’s first attempts to address the social determinants of health with legislation.3 The American Academy of Pediatrics was formed in 1930 after the AMA House of Delegates rebuked the Pediatric section for advocating for continuance of the act during the late 1920s.3 Perhaps what Pediatrics has to teach the rest of medicine is the necessity of making advocacy a part of our professional identity. And perhaps that’s the reason that so many pediatricians are still burning and not burned out.

A celebratory mood pervaded the last week of service for my ward team at the end of the academic year. As the attending, it was just another day, but it was hard not to be caught up in the general feeling of a milestone flying past. Like most days in a hospital, this one passed in a rhythm of alternating mundanity and crisis. Late in the afternoon, one of the residents called me to a bedside for help. Imagining that my diagnostic skills were urgently required, I took the stairs. The problem, as it turned out, was not strictly medical.

I could hear the yelling before I cleared the locked entry doors to the ward. It doesn’t really matter what the yelling was about, just that there is often yelling and there is always very little I can do about the root cause of it. As I stepped into the middle of the conflagration, I remembered the story an intern told me about the night earlier in the month when it fell to her to wheel the same patient’s intoxicated parent down to the emergency department. After sleeping it off, the parent was diagnosed with an “allergic reaction” and given a prescription for diphenhydramine. We all knew the diagnosis was fantasy, and yet we all went along with it because there was simply no help available for the root cause of the problem. State social services was already involved, and we had a “safety” plan in place for discharge. As meager as that may have been, we had done the best we could to balance the risk with the available resources… or so we told ourselves.

As a nation, we have chosen not to provide much of a social safety net for our citizens who suffer from addiction and/or mental illness and, most importantly, for those who’ve just not had a leg up on the economic ladder. As a hospital-based clinician, I know that people in distress lose their cool and yell sometimes. Ironically, they may yell most loudly at people who sincerely want to help, simply because others do not engage them. Medical schools don’t teach us how to handle the yelling, though many would say it is part of the hidden curriculum. One thing that distinguishes many pediatricians like myself is a willingness to listen to the yelling, to engage with it, and to try to help. Not surprisingly, our reputation around the hospital is that we skew a bit naive.

It is worth asking, though: Are pediatricians naive? Sure, we make funny faces. We clown. We baby-talk. Those things are largely true, but there are other true things about pediatricians. Chief among them is the fact that we come to know some of the worst things there are to know about human beings. Everybody knows people can be awful, but we know exactly how awful they are to defenseless children in precise detail. For instance, I’ve seen a 4-year-old who was repeatedly starved as a regular punishment. She was so hungry she ate her hair, which turned out to be lucky for her because it caused an intestinal blockage that led to the discovery of the abuse. I gave her an apple one day and she immediately hid it under her shirt. Where you see a scab on a child’s inner arm, I see a cigarette burn. I’ve resuscitated a baby whose parents dipped his pacifier in heroin to stop his crying—the remarkable part of the story being that it was heroin cooked in the hospital bathroom. And then there are the things that I cannot even bring myself to write down.

Carrying this knowledge hollows out a gap between pediatricians and the rest of the world. The divergence between our expectations of how a society should treat its children and the reality of our daily experience grinds away any naivete. The gap becomes a canyon for some of us. We live with the sense that nobody would believe the things we’ve seen, so we rarely talk about them. Years ago, I was testifying in a (for me) routine child-abuse case where this fact hit home. It is common for juries to disbelieve that a caregiver could do the things we allege. I say allege, but if you work as a pediatrician long enough, the space between allegation and fact narrows. It is simply pattern recognition to you—abuse happens so consistently that we accept it as a diagnostic category. The case in question was a submersion burn, which is an almost unmistakable pattern. The other piece of the story is that it happens to toddlers during toilet training as caregivers lose their self-control and punish children for soiling themselves. For me, simple pattern recognition; for the jury, simply unbelievable. We lost the case.

We are almost always losing the case as pediatricians. Spending on children makes up less than 10% of the federal budget, whereas spending on the elderly, including Social Security, Medicare, and the adult component of Medicaid, dominates that budget.1 Moreover, twice as many children as adults over age 65 are living in poverty in the United States. The Temporary Assistance for Needy Families program is often debated in this country and frequently criticized as wasteful. However, what is not debatable is that the allocated budget ($16.5 billion) hasn’t changed since 1996, resulting in a functional 40% decrease due to inflation.2 Life, for poor children, gets a little tougher every year.

After the resident and I wrapped up our day, we talked a little about how hard it is to witness some of the things you see in a children’s hospital. I could see the gap between her and the outside world widening right in front of me. In my weaker moments, I want to tell trainees like her to run while they can. I want to warn them that they don’t want to know so many of the things we’re going to teach them. I know how the story usually ends. I know that our country doesn’t promise children safety from social deprivation, hunger, or physical abuse. Instead, we’ve created the conditions for those things to occur at embarrassingly high rates, and we prosecute the unlucky after the fact. The children are simply collateral damage.

We stood at our patient’s bedside and tried to imagine a happy future. Even without his medical problems, he would likely need a major investment of resources in order to thrive. Where would those resources come from? I saw the hospital crib, metal bars on all sides and a thick plastic roof to prevent escape, as a metaphor. Later, I took the elevator down and overheard a snippet of conversation between two residents. One of them asked the other, “How do you know when you’ve burned out?” The other replied, “I don’t know, I guess when you’ve stopped burning.” Burnout is a hot topic in medicine, and some may assume the reasons are obvious: long hours and intellectually demanding work. In reality, those drivers may be less important than the repeated exposure to profound injustice inherent to the practice of medicine in our country.

As hospitalists, we address acute decompensation in our patients and send them back out into the world knowing there will soon be a next time. We also know that the next time might be preventable, if only … This cycle sometimes feels inexorable, but it can also prompt us to think about our obligation to work toward a more just society. We have to imagine a better future even as we struggle to believe it is on the way.

Most of our hospitals are trying to help. They have community-engagement programs, they purchase housing for homeless patients, they provide large amounts of uncompensated care and sometimes operate at a loss. Yet none of this addresses the root cause of the problem. Medicine, either in the form of an institution or a doctor, can’t replace a just society, but the truth of this fact does not mean we should not try.

Pediatrics has always been a field disposed toward advocacy. The origin of our largest professional organization in the United States was the intraprofessional conflict within the American Medical Association (AMA) over the Sheppard-Towner Act of 1921, one of this country’s first attempts to address the social determinants of health with legislation.3 The American Academy of Pediatrics was formed in 1930 after the AMA House of Delegates rebuked the Pediatric section for advocating for continuance of the act during the late 1920s.3 Perhaps what Pediatrics has to teach the rest of medicine is the necessity of making advocacy a part of our professional identity. And perhaps that’s the reason that so many pediatricians are still burning and not burned out.

References

1. Committee for a Responsible Federal Budget. Chartbook: budgeting for the next generation. October 11, 2018. Accessed February 2, 2021. http://www.crfb.org/papers/chartbook-budgeting-next-generation
2. Center on Budget and Policy Priorities. Policy basics: temporary assistance for needy families. Updated March 31, 2021. Accessed February 2, 2021. https://www.cbpp.org/research/family-income-support/temporary-assistance-for-needy-families
3. van Dyck PC. A history of child health equity legislation in the United States. Pediatrics. 2003;112(3 pt 2):727-730.

References

1. Committee for a Responsible Federal Budget. Chartbook: budgeting for the next generation. October 11, 2018. Accessed February 2, 2021. http://www.crfb.org/papers/chartbook-budgeting-next-generation
2. Center on Budget and Policy Priorities. Policy basics: temporary assistance for needy families. Updated March 31, 2021. Accessed February 2, 2021. https://www.cbpp.org/research/family-income-support/temporary-assistance-for-needy-families
3. van Dyck PC. A history of child health equity legislation in the United States. Pediatrics. 2003;112(3 pt 2):727-730.

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Ableism and Quality of Life During the Coronavirus Pandemic

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Ableism and Quality of Life During the Coronavirus Pandemic

Michael Hickson was a 46-year-old with a severe acquired disability whose COVID-19 course involved multisystem organ failure, a court-appointed guardian, hospice care, discontinued fluids and tube feeds, and eventual death. While some details have been released by the hospital,1 the recorded conversation between Mr. Hickson’s wife and a treating physician has been shared widely in disability communities.

Physician: “Right now, his quality of life—he doesn’t have much of one.”

Spouse: “What do you mean? Because he’s paralyzed with a brain injury, he doesn’t have a quality of life?”

Physician: “Correct.”

PHYSICIANS’ PERCEPTIONS OF PERSONS WITH DISABILITIES

As physiatrists—physicians for patients with disabilities—we heard those words with heavy hearts and sunken stomachs. We can only imagine the anger, fear, and betrayal felt by our patients and other people with disabilities. Or perhaps they feel vindicated, that the quiet sentiments were finally said out loud. The recording expresses what people with disabilities long suspected: physicians don’t always value the lives of persons with disabilities the way they value the nondisabled. Research confirms this.2-4 The privilege of the nondisabled is often expressed as “I would never want to live like that.” People make personal judgments about how they would feel in somebody else’s situation. The usually quiet sentiment, this time said aloud and recorded—“He doesn’t have much [quality of life]”—showed how physicians’ judgments and biases can have a grave impact on others, especially people with disabilities.

Stereotypes, assumptions, and biases about the quality of life of people with disabilities are pervasive throughout healthcare, resulting in the devaluation and disparate treatment of people with disabilities.5 Healthcare providers are not exempt from deficit-based perspectives about people with disabilities,6 and discrimination ensues when healthcare providers make critical decisions from these perspectives.5 Ableist biases are underrecognized among physicians, who often misperceive quality of life for people with disabilities as poor, and fail to recognize that medical judgments can be biased accordingly.5 Consequently, necessary care can be withheld or withdrawn inappropriately.5 An estimated 25% of adults in the United States self-report disability; furthermore, disability is highly correlated with age as well as socioeconomic disadvantages.7 There is also extensive evidence that, as a population, people with disabilities experience healthcare disparities.8 Bias against people with disabilities serves to both restrict and reduce access to healthcare.9

The consequences of the pandemic have disproportionally affected the Black community, in terms of both economic and disease burden. Mr. Hickson, a Black man with disabilities who contracted COVID-19, personifies the intersection of race and disability and demands our concern and attention as physicians. We must appreciate the intrinsic worth of all people and populations, and seek to understand and respect their capacity to be active agents in their own lives, making their own decisions about their quality of life. The lives of Black people have value, but movements such as Black Lives Matter have been needed to highlight this truth, and there still needs to be meaningful action beyond rhetoric. The lives of people with disabilities have value. Healthcare systems and providers similarly need to acknowledge and act in a way that honors the intrinsic worth of people with disabilities.

People with disabilities face long-standing systemic barriers to equitable healthcare,10 as do Black people. During the pandemic, widespread alarm was raised about individual and structural racism in medicine, just as numerous disability rights organizations raised concerns that ableism would lead to undertreatment during the COVID-19 crisis, worsening existing healthcare inequities. In response, the US Department of Health and Human Services Office for Civil Rights in Action released a bulletin that stated, “In this time of emergency, the laudable goal of providing care quickly and efficiently must be guided by the fundamental principles of fairness, equality, and compassion that animate our civil rights laws. This is particularly true with respect to the treatment of persons with disabilities during medical emergencies as they possess the same dignity and worth as everyone else.”11 Using the presence of disabilities to limit or deny a person’s access to health care constitutes a clear violation of nondiscrimination law.12 Hospitals and providers should not limit the care offered to people with disabilities because of their disabilities or utilize quality-of-life judgments when deciding whether or not to provide care.12 While the hospital where Michael Hickson died released a statement claiming that they did not consider his disability status as part of their treatment decision-making, the recorded words of the physician suggest otherwise.

The impact of our words and actions, and not the underlying intent, most affects patients’, families’, and communities’ trust in the institution of medicine, represented by individual providers. The hospital statement indicated “it was not medically possible to save [Mr. Hickson].”1 The phrase “not medically possible” ties Mr. Hickson’s case to one of futility; however, the recording was about quality of life, not futility. The National Council on Disability found that subjective quality-of-life assumptions influence medical futility decisions.5 While the intent of withdrawing care from Mr. Hickson may have been related to futility, the consequences of this decision are far-reaching as people with disabilities have reason to question whether someone else’s judgment about the quality and worth of their life will lead to loss of their life.

Emphasizing perceived quality of life in making treatment decisions, as was implied for Mr. Hickson, is not a rare event and is one that is likely more common when health systems are stressed. Despite having policies and procedures to follow, biases creep into treatment decisions. In Oregon, for example, multiple cases of disability discrimination during the pandemic were brought to the attention of the state Senate by Disability Rights Oregon.13,14

ADVOCATING FOR A DISABILITY INCLUSIVE COVID-19 RESPONSE

Physicians and healthcare leaders must consider the unique needs of the disability community through health equity efforts in the COVID-19 response. There must be universally accessible approaches when planning and implementing a COVID response to increase impact and ensure systems are reaching all underserved communities. For healthcare institutions and hospitals, disability equity must be emphasized in the development and implementation of COVID-19 policies. The exclusion of people with disabilities from decisions about people with disabilities is problematic. This systemic exclusion means that ableist beliefs and policies are often unchallenged.15 Including people with disabilities on committees creating crisis standards of care protocols or other policies that may purposefully or unintentionally discriminate against people with disabilities is an important step.16 Representation matters, and people with disabilities must be central in the development of all health equity strategies during a pandemic. Furthermore, when system-level decision algorithms exist that value the life of people with disabilities, clinician biases are minimized, leading to more equitable care.

Examples of strategies include accessible formats for essential COVID-19-related communications, such as American Sign Language, large print, or screen reading technology. We must acknowledge that necessary universal mask policies can generate communication barriers for people reading lips. Hospitals and clinics have rapidly expanded virtual care and telemedicine to improve access. This has enhanced access to care for many people with mobility disability, but can exacerbate disparities for those with vision, hearing, communication, or intellectual disability. To better manage this issue, tailored strategies, such as live closed captioning or digital patient navigators, can be implemented.

Additionally, a person with a disability has the legal right to be accompanied by a designated essential support person. Hospital visitor policies must become less restrictive or enable exceptions when a person with a disability requires their personal care attendant. When it comes to outcome data, it is important to highlight the need for better collection of disability data that can be used to identify inequities as well as monitor outcomes of treatment.

As previously acknowledged, people without disabilities tend to have negative attitudes (both implicit and explicit) toward people with disabilities. These attitudes are re-enforced by societal-level institutions, policies, and structures that marginalize people with disabilities.17 We call on all physicians and those working in healthcare to question their biases. When you consider quality of life in your decision-making, ask yourself, “whose life?” Recognize and honor the personal, social, and cultural contexts that affect how an individual experiences “quality of life.” Unless the answer to “whose life?” is your own or that of your incapacitated dependent, it is not your place to make “quality of life” judgments. You can and should describe potential outcomes at the physiological or activity level, but leave quality-of-life decisions where they belong—with the individual or their designated representative.

Social media activity in the disability community indicates that Mr. Hickson’s story is perceived, regardless of the provider’s and healthcare system’s intentions, to be yet another breach of trust by the medical system. It is not the burden of the oppressed and betrayed to repair a broken relationship. It is our obligation, as individual physicians and the greater medical institution, to provide care that demonstrates the value and worth of people with disabilities. An imperative step toward equitable care for people with disabilities is to recognize and address our ableist biases.

References

1. Anderson D. Statement on the death of Michael Hickson. St David’s HealthCare. July 2, 2020. Accessed July 6, 2020. https://stdavids.com/about/newsroom/statement-on-the-death-of-michael-hickson
2. Amundson R. Disability, ideology, and quality of life: a bias in biomedical ethics. In: Wasserman D, Bickenbach J, Wachbroit R, eds. Quality of Life and Human Difference: Genetic Testing, Health Care, and Disability. Cambridge University Press; 2005:101-124.
3. Dunn DS. Outsider privileges can lead to insider disadvantages: some psychosocial aspects of ableism. J Soc Issues. 2019;75(3):665-682. https://doi.org/10.1111/josi.12331
4. Kothari S. Clinical (mis)judgments of quality of life after disability. J Clin Ethics. 2004;15:300-307.
5. National Council on Disability. Medical futility and disability bias: part of the bioethics and disability series. November 19, 2019. Accessed March 31, 2021. https://www.ncd.gov/sites/default/files/NCD_Medical_Futility_Report_508.pdf
6. Iezzoni LI, Rao SR, Ressalam J, et al. Physicians’ perceptions of people with disability and their health care. Health Aff (Millwood). 2021;40(2):297-306. https://doi.org/10.1377/hlthaff.2020.01452
7. Okoro CA, Hollis ND, Cyrus AC, Griffin-Blake S. Prevalence of disabilities and health care access by disability status and type among adults - United States, 2016. MMWR Morb Mortal Wkly Rep. 2018;67(32):882-887. https://doi.org/10.15585/mmwr.mm6732a3
8. Meade MA, Mahmoudi E, Lee SY. The intersection of disability and healthcare disparities: a conceptual framework. Disabil Rehabil. 2015;37(7):632-641. https://doi.org/10.3109/09638288.2014.938176
9. Andrews EE, Ayers KB, Brown KS, Dunn DS, Pilarski CR. No body is expendable: medical rationing and disability justice during the COVID-19 pandemic. Am Psychol. Published online July 23, 2020. https://doi.org/10.1037/amp0000709
10. Savin K, Guidry-Grimes L. Confronting disability discrimination during the pandemic. The Hastings Center. April 2, 2020. Accessed March 31, 2021. https://www.thehastingscenter.org/confronting-disability-discrimination-during-the-pandemic/
11. Health and Human Services Office for Civil Rights in Action. Bulletin: civil rights, HIPAA, and the coronavirus disease 2019. March 28, 2020. Accessed March 31, 2021. https://www.hhs.gov/sites/default/files/ocr-bulletin-3-28-20.pdf
12. Preventing discrimination in the treatment of COVID-19 patients: the illegality of medical rationing on the basis of disability. Disability Rights Education & Defense Fund. March 25, 2020. Accessed March 31, 2021. https://dredf.org/wp-content/uploads/2020/03/DREDF-Policy-Statement-on-COVID-19-and-Medical-Rationing-3-25-2020.pdf
13. Oregon hospitals told not to withhold care because of a person’s disability. Transcript. Morning Edition. National Public Radio. December 21, 2020. Accessed March 31, 2021. https://www.npr.org/2020/12/21/948697808/oregon-hospitals-told-not-to-withhold-care-because-of-a-persons-disability
14. As hospitals fear being overwhelmed by COVID-19, do the disabled get the same access? Transcript. Morning Edition. National Public Radio. December 14, 2020. Accessed March 31, 2021. https://www.npr.org/2020/12/14/945056176/as-hospitals-fear-being-overwhelmed-by-covid-19-do-the-disabled-get-the-same-acc
15. Lund EM, Forber-Pratt AJ, Wilson C, Mona LR. The COVID-19 pandemic, stress, and trauma in the disability community: a call to action. Rehabil Psychol. 2020;65(4):313-322. https://doi.org/10.1037/rep0000368
16. Auriemma CL, Molinero AM, Houtrow AJ, Persad G, White DB, Halpern SD. Eliminating categorical exclusion criteria in crisis standards of care frameworks. Am J Bioeth. 2020;20(7):28-36. http://doi.org/10.1080/15265161.2020.1764141
17. Bogart KR, Dunn DS. Ableism special issue introduction. J Soc Issues. 2019;75(3):650-664. https://doi.org/10.1111/josi.12354

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1Department of Rehabilitation Medicine, University of Washington, Seattle, Washington; 2Department of Physical Medicine and Rehabilitation and Pediatrics, University of Pittsburgh; Pittsburgh, PA; 3Department of Physical Medicine and Rehabilitation; University of Texas Health Sciences Center at San Antonio; San Antonio, Texas.

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1Department of Rehabilitation Medicine, University of Washington, Seattle, Washington; 2Department of Physical Medicine and Rehabilitation and Pediatrics, University of Pittsburgh; Pittsburgh, PA; 3Department of Physical Medicine and Rehabilitation; University of Texas Health Sciences Center at San Antonio; San Antonio, Texas.

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Related Articles

Michael Hickson was a 46-year-old with a severe acquired disability whose COVID-19 course involved multisystem organ failure, a court-appointed guardian, hospice care, discontinued fluids and tube feeds, and eventual death. While some details have been released by the hospital,1 the recorded conversation between Mr. Hickson’s wife and a treating physician has been shared widely in disability communities.

Physician: “Right now, his quality of life—he doesn’t have much of one.”

Spouse: “What do you mean? Because he’s paralyzed with a brain injury, he doesn’t have a quality of life?”

Physician: “Correct.”

PHYSICIANS’ PERCEPTIONS OF PERSONS WITH DISABILITIES

As physiatrists—physicians for patients with disabilities—we heard those words with heavy hearts and sunken stomachs. We can only imagine the anger, fear, and betrayal felt by our patients and other people with disabilities. Or perhaps they feel vindicated, that the quiet sentiments were finally said out loud. The recording expresses what people with disabilities long suspected: physicians don’t always value the lives of persons with disabilities the way they value the nondisabled. Research confirms this.2-4 The privilege of the nondisabled is often expressed as “I would never want to live like that.” People make personal judgments about how they would feel in somebody else’s situation. The usually quiet sentiment, this time said aloud and recorded—“He doesn’t have much [quality of life]”—showed how physicians’ judgments and biases can have a grave impact on others, especially people with disabilities.

Stereotypes, assumptions, and biases about the quality of life of people with disabilities are pervasive throughout healthcare, resulting in the devaluation and disparate treatment of people with disabilities.5 Healthcare providers are not exempt from deficit-based perspectives about people with disabilities,6 and discrimination ensues when healthcare providers make critical decisions from these perspectives.5 Ableist biases are underrecognized among physicians, who often misperceive quality of life for people with disabilities as poor, and fail to recognize that medical judgments can be biased accordingly.5 Consequently, necessary care can be withheld or withdrawn inappropriately.5 An estimated 25% of adults in the United States self-report disability; furthermore, disability is highly correlated with age as well as socioeconomic disadvantages.7 There is also extensive evidence that, as a population, people with disabilities experience healthcare disparities.8 Bias against people with disabilities serves to both restrict and reduce access to healthcare.9

The consequences of the pandemic have disproportionally affected the Black community, in terms of both economic and disease burden. Mr. Hickson, a Black man with disabilities who contracted COVID-19, personifies the intersection of race and disability and demands our concern and attention as physicians. We must appreciate the intrinsic worth of all people and populations, and seek to understand and respect their capacity to be active agents in their own lives, making their own decisions about their quality of life. The lives of Black people have value, but movements such as Black Lives Matter have been needed to highlight this truth, and there still needs to be meaningful action beyond rhetoric. The lives of people with disabilities have value. Healthcare systems and providers similarly need to acknowledge and act in a way that honors the intrinsic worth of people with disabilities.

People with disabilities face long-standing systemic barriers to equitable healthcare,10 as do Black people. During the pandemic, widespread alarm was raised about individual and structural racism in medicine, just as numerous disability rights organizations raised concerns that ableism would lead to undertreatment during the COVID-19 crisis, worsening existing healthcare inequities. In response, the US Department of Health and Human Services Office for Civil Rights in Action released a bulletin that stated, “In this time of emergency, the laudable goal of providing care quickly and efficiently must be guided by the fundamental principles of fairness, equality, and compassion that animate our civil rights laws. This is particularly true with respect to the treatment of persons with disabilities during medical emergencies as they possess the same dignity and worth as everyone else.”11 Using the presence of disabilities to limit or deny a person’s access to health care constitutes a clear violation of nondiscrimination law.12 Hospitals and providers should not limit the care offered to people with disabilities because of their disabilities or utilize quality-of-life judgments when deciding whether or not to provide care.12 While the hospital where Michael Hickson died released a statement claiming that they did not consider his disability status as part of their treatment decision-making, the recorded words of the physician suggest otherwise.

The impact of our words and actions, and not the underlying intent, most affects patients’, families’, and communities’ trust in the institution of medicine, represented by individual providers. The hospital statement indicated “it was not medically possible to save [Mr. Hickson].”1 The phrase “not medically possible” ties Mr. Hickson’s case to one of futility; however, the recording was about quality of life, not futility. The National Council on Disability found that subjective quality-of-life assumptions influence medical futility decisions.5 While the intent of withdrawing care from Mr. Hickson may have been related to futility, the consequences of this decision are far-reaching as people with disabilities have reason to question whether someone else’s judgment about the quality and worth of their life will lead to loss of their life.

Emphasizing perceived quality of life in making treatment decisions, as was implied for Mr. Hickson, is not a rare event and is one that is likely more common when health systems are stressed. Despite having policies and procedures to follow, biases creep into treatment decisions. In Oregon, for example, multiple cases of disability discrimination during the pandemic were brought to the attention of the state Senate by Disability Rights Oregon.13,14

ADVOCATING FOR A DISABILITY INCLUSIVE COVID-19 RESPONSE

Physicians and healthcare leaders must consider the unique needs of the disability community through health equity efforts in the COVID-19 response. There must be universally accessible approaches when planning and implementing a COVID response to increase impact and ensure systems are reaching all underserved communities. For healthcare institutions and hospitals, disability equity must be emphasized in the development and implementation of COVID-19 policies. The exclusion of people with disabilities from decisions about people with disabilities is problematic. This systemic exclusion means that ableist beliefs and policies are often unchallenged.15 Including people with disabilities on committees creating crisis standards of care protocols or other policies that may purposefully or unintentionally discriminate against people with disabilities is an important step.16 Representation matters, and people with disabilities must be central in the development of all health equity strategies during a pandemic. Furthermore, when system-level decision algorithms exist that value the life of people with disabilities, clinician biases are minimized, leading to more equitable care.

Examples of strategies include accessible formats for essential COVID-19-related communications, such as American Sign Language, large print, or screen reading technology. We must acknowledge that necessary universal mask policies can generate communication barriers for people reading lips. Hospitals and clinics have rapidly expanded virtual care and telemedicine to improve access. This has enhanced access to care for many people with mobility disability, but can exacerbate disparities for those with vision, hearing, communication, or intellectual disability. To better manage this issue, tailored strategies, such as live closed captioning or digital patient navigators, can be implemented.

Additionally, a person with a disability has the legal right to be accompanied by a designated essential support person. Hospital visitor policies must become less restrictive or enable exceptions when a person with a disability requires their personal care attendant. When it comes to outcome data, it is important to highlight the need for better collection of disability data that can be used to identify inequities as well as monitor outcomes of treatment.

As previously acknowledged, people without disabilities tend to have negative attitudes (both implicit and explicit) toward people with disabilities. These attitudes are re-enforced by societal-level institutions, policies, and structures that marginalize people with disabilities.17 We call on all physicians and those working in healthcare to question their biases. When you consider quality of life in your decision-making, ask yourself, “whose life?” Recognize and honor the personal, social, and cultural contexts that affect how an individual experiences “quality of life.” Unless the answer to “whose life?” is your own or that of your incapacitated dependent, it is not your place to make “quality of life” judgments. You can and should describe potential outcomes at the physiological or activity level, but leave quality-of-life decisions where they belong—with the individual or their designated representative.

Social media activity in the disability community indicates that Mr. Hickson’s story is perceived, regardless of the provider’s and healthcare system’s intentions, to be yet another breach of trust by the medical system. It is not the burden of the oppressed and betrayed to repair a broken relationship. It is our obligation, as individual physicians and the greater medical institution, to provide care that demonstrates the value and worth of people with disabilities. An imperative step toward equitable care for people with disabilities is to recognize and address our ableist biases.

Michael Hickson was a 46-year-old with a severe acquired disability whose COVID-19 course involved multisystem organ failure, a court-appointed guardian, hospice care, discontinued fluids and tube feeds, and eventual death. While some details have been released by the hospital,1 the recorded conversation between Mr. Hickson’s wife and a treating physician has been shared widely in disability communities.

Physician: “Right now, his quality of life—he doesn’t have much of one.”

Spouse: “What do you mean? Because he’s paralyzed with a brain injury, he doesn’t have a quality of life?”

Physician: “Correct.”

PHYSICIANS’ PERCEPTIONS OF PERSONS WITH DISABILITIES

As physiatrists—physicians for patients with disabilities—we heard those words with heavy hearts and sunken stomachs. We can only imagine the anger, fear, and betrayal felt by our patients and other people with disabilities. Or perhaps they feel vindicated, that the quiet sentiments were finally said out loud. The recording expresses what people with disabilities long suspected: physicians don’t always value the lives of persons with disabilities the way they value the nondisabled. Research confirms this.2-4 The privilege of the nondisabled is often expressed as “I would never want to live like that.” People make personal judgments about how they would feel in somebody else’s situation. The usually quiet sentiment, this time said aloud and recorded—“He doesn’t have much [quality of life]”—showed how physicians’ judgments and biases can have a grave impact on others, especially people with disabilities.

Stereotypes, assumptions, and biases about the quality of life of people with disabilities are pervasive throughout healthcare, resulting in the devaluation and disparate treatment of people with disabilities.5 Healthcare providers are not exempt from deficit-based perspectives about people with disabilities,6 and discrimination ensues when healthcare providers make critical decisions from these perspectives.5 Ableist biases are underrecognized among physicians, who often misperceive quality of life for people with disabilities as poor, and fail to recognize that medical judgments can be biased accordingly.5 Consequently, necessary care can be withheld or withdrawn inappropriately.5 An estimated 25% of adults in the United States self-report disability; furthermore, disability is highly correlated with age as well as socioeconomic disadvantages.7 There is also extensive evidence that, as a population, people with disabilities experience healthcare disparities.8 Bias against people with disabilities serves to both restrict and reduce access to healthcare.9

The consequences of the pandemic have disproportionally affected the Black community, in terms of both economic and disease burden. Mr. Hickson, a Black man with disabilities who contracted COVID-19, personifies the intersection of race and disability and demands our concern and attention as physicians. We must appreciate the intrinsic worth of all people and populations, and seek to understand and respect their capacity to be active agents in their own lives, making their own decisions about their quality of life. The lives of Black people have value, but movements such as Black Lives Matter have been needed to highlight this truth, and there still needs to be meaningful action beyond rhetoric. The lives of people with disabilities have value. Healthcare systems and providers similarly need to acknowledge and act in a way that honors the intrinsic worth of people with disabilities.

People with disabilities face long-standing systemic barriers to equitable healthcare,10 as do Black people. During the pandemic, widespread alarm was raised about individual and structural racism in medicine, just as numerous disability rights organizations raised concerns that ableism would lead to undertreatment during the COVID-19 crisis, worsening existing healthcare inequities. In response, the US Department of Health and Human Services Office for Civil Rights in Action released a bulletin that stated, “In this time of emergency, the laudable goal of providing care quickly and efficiently must be guided by the fundamental principles of fairness, equality, and compassion that animate our civil rights laws. This is particularly true with respect to the treatment of persons with disabilities during medical emergencies as they possess the same dignity and worth as everyone else.”11 Using the presence of disabilities to limit or deny a person’s access to health care constitutes a clear violation of nondiscrimination law.12 Hospitals and providers should not limit the care offered to people with disabilities because of their disabilities or utilize quality-of-life judgments when deciding whether or not to provide care.12 While the hospital where Michael Hickson died released a statement claiming that they did not consider his disability status as part of their treatment decision-making, the recorded words of the physician suggest otherwise.

The impact of our words and actions, and not the underlying intent, most affects patients’, families’, and communities’ trust in the institution of medicine, represented by individual providers. The hospital statement indicated “it was not medically possible to save [Mr. Hickson].”1 The phrase “not medically possible” ties Mr. Hickson’s case to one of futility; however, the recording was about quality of life, not futility. The National Council on Disability found that subjective quality-of-life assumptions influence medical futility decisions.5 While the intent of withdrawing care from Mr. Hickson may have been related to futility, the consequences of this decision are far-reaching as people with disabilities have reason to question whether someone else’s judgment about the quality and worth of their life will lead to loss of their life.

Emphasizing perceived quality of life in making treatment decisions, as was implied for Mr. Hickson, is not a rare event and is one that is likely more common when health systems are stressed. Despite having policies and procedures to follow, biases creep into treatment decisions. In Oregon, for example, multiple cases of disability discrimination during the pandemic were brought to the attention of the state Senate by Disability Rights Oregon.13,14

ADVOCATING FOR A DISABILITY INCLUSIVE COVID-19 RESPONSE

Physicians and healthcare leaders must consider the unique needs of the disability community through health equity efforts in the COVID-19 response. There must be universally accessible approaches when planning and implementing a COVID response to increase impact and ensure systems are reaching all underserved communities. For healthcare institutions and hospitals, disability equity must be emphasized in the development and implementation of COVID-19 policies. The exclusion of people with disabilities from decisions about people with disabilities is problematic. This systemic exclusion means that ableist beliefs and policies are often unchallenged.15 Including people with disabilities on committees creating crisis standards of care protocols or other policies that may purposefully or unintentionally discriminate against people with disabilities is an important step.16 Representation matters, and people with disabilities must be central in the development of all health equity strategies during a pandemic. Furthermore, when system-level decision algorithms exist that value the life of people with disabilities, clinician biases are minimized, leading to more equitable care.

Examples of strategies include accessible formats for essential COVID-19-related communications, such as American Sign Language, large print, or screen reading technology. We must acknowledge that necessary universal mask policies can generate communication barriers for people reading lips. Hospitals and clinics have rapidly expanded virtual care and telemedicine to improve access. This has enhanced access to care for many people with mobility disability, but can exacerbate disparities for those with vision, hearing, communication, or intellectual disability. To better manage this issue, tailored strategies, such as live closed captioning or digital patient navigators, can be implemented.

Additionally, a person with a disability has the legal right to be accompanied by a designated essential support person. Hospital visitor policies must become less restrictive or enable exceptions when a person with a disability requires their personal care attendant. When it comes to outcome data, it is important to highlight the need for better collection of disability data that can be used to identify inequities as well as monitor outcomes of treatment.

As previously acknowledged, people without disabilities tend to have negative attitudes (both implicit and explicit) toward people with disabilities. These attitudes are re-enforced by societal-level institutions, policies, and structures that marginalize people with disabilities.17 We call on all physicians and those working in healthcare to question their biases. When you consider quality of life in your decision-making, ask yourself, “whose life?” Recognize and honor the personal, social, and cultural contexts that affect how an individual experiences “quality of life.” Unless the answer to “whose life?” is your own or that of your incapacitated dependent, it is not your place to make “quality of life” judgments. You can and should describe potential outcomes at the physiological or activity level, but leave quality-of-life decisions where they belong—with the individual or their designated representative.

Social media activity in the disability community indicates that Mr. Hickson’s story is perceived, regardless of the provider’s and healthcare system’s intentions, to be yet another breach of trust by the medical system. It is not the burden of the oppressed and betrayed to repair a broken relationship. It is our obligation, as individual physicians and the greater medical institution, to provide care that demonstrates the value and worth of people with disabilities. An imperative step toward equitable care for people with disabilities is to recognize and address our ableist biases.

References

1. Anderson D. Statement on the death of Michael Hickson. St David’s HealthCare. July 2, 2020. Accessed July 6, 2020. https://stdavids.com/about/newsroom/statement-on-the-death-of-michael-hickson
2. Amundson R. Disability, ideology, and quality of life: a bias in biomedical ethics. In: Wasserman D, Bickenbach J, Wachbroit R, eds. Quality of Life and Human Difference: Genetic Testing, Health Care, and Disability. Cambridge University Press; 2005:101-124.
3. Dunn DS. Outsider privileges can lead to insider disadvantages: some psychosocial aspects of ableism. J Soc Issues. 2019;75(3):665-682. https://doi.org/10.1111/josi.12331
4. Kothari S. Clinical (mis)judgments of quality of life after disability. J Clin Ethics. 2004;15:300-307.
5. National Council on Disability. Medical futility and disability bias: part of the bioethics and disability series. November 19, 2019. Accessed March 31, 2021. https://www.ncd.gov/sites/default/files/NCD_Medical_Futility_Report_508.pdf
6. Iezzoni LI, Rao SR, Ressalam J, et al. Physicians’ perceptions of people with disability and their health care. Health Aff (Millwood). 2021;40(2):297-306. https://doi.org/10.1377/hlthaff.2020.01452
7. Okoro CA, Hollis ND, Cyrus AC, Griffin-Blake S. Prevalence of disabilities and health care access by disability status and type among adults - United States, 2016. MMWR Morb Mortal Wkly Rep. 2018;67(32):882-887. https://doi.org/10.15585/mmwr.mm6732a3
8. Meade MA, Mahmoudi E, Lee SY. The intersection of disability and healthcare disparities: a conceptual framework. Disabil Rehabil. 2015;37(7):632-641. https://doi.org/10.3109/09638288.2014.938176
9. Andrews EE, Ayers KB, Brown KS, Dunn DS, Pilarski CR. No body is expendable: medical rationing and disability justice during the COVID-19 pandemic. Am Psychol. Published online July 23, 2020. https://doi.org/10.1037/amp0000709
10. Savin K, Guidry-Grimes L. Confronting disability discrimination during the pandemic. The Hastings Center. April 2, 2020. Accessed March 31, 2021. https://www.thehastingscenter.org/confronting-disability-discrimination-during-the-pandemic/
11. Health and Human Services Office for Civil Rights in Action. Bulletin: civil rights, HIPAA, and the coronavirus disease 2019. March 28, 2020. Accessed March 31, 2021. https://www.hhs.gov/sites/default/files/ocr-bulletin-3-28-20.pdf
12. Preventing discrimination in the treatment of COVID-19 patients: the illegality of medical rationing on the basis of disability. Disability Rights Education & Defense Fund. March 25, 2020. Accessed March 31, 2021. https://dredf.org/wp-content/uploads/2020/03/DREDF-Policy-Statement-on-COVID-19-and-Medical-Rationing-3-25-2020.pdf
13. Oregon hospitals told not to withhold care because of a person’s disability. Transcript. Morning Edition. National Public Radio. December 21, 2020. Accessed March 31, 2021. https://www.npr.org/2020/12/21/948697808/oregon-hospitals-told-not-to-withhold-care-because-of-a-persons-disability
14. As hospitals fear being overwhelmed by COVID-19, do the disabled get the same access? Transcript. Morning Edition. National Public Radio. December 14, 2020. Accessed March 31, 2021. https://www.npr.org/2020/12/14/945056176/as-hospitals-fear-being-overwhelmed-by-covid-19-do-the-disabled-get-the-same-acc
15. Lund EM, Forber-Pratt AJ, Wilson C, Mona LR. The COVID-19 pandemic, stress, and trauma in the disability community: a call to action. Rehabil Psychol. 2020;65(4):313-322. https://doi.org/10.1037/rep0000368
16. Auriemma CL, Molinero AM, Houtrow AJ, Persad G, White DB, Halpern SD. Eliminating categorical exclusion criteria in crisis standards of care frameworks. Am J Bioeth. 2020;20(7):28-36. http://doi.org/10.1080/15265161.2020.1764141
17. Bogart KR, Dunn DS. Ableism special issue introduction. J Soc Issues. 2019;75(3):650-664. https://doi.org/10.1111/josi.12354

References

1. Anderson D. Statement on the death of Michael Hickson. St David’s HealthCare. July 2, 2020. Accessed July 6, 2020. https://stdavids.com/about/newsroom/statement-on-the-death-of-michael-hickson
2. Amundson R. Disability, ideology, and quality of life: a bias in biomedical ethics. In: Wasserman D, Bickenbach J, Wachbroit R, eds. Quality of Life and Human Difference: Genetic Testing, Health Care, and Disability. Cambridge University Press; 2005:101-124.
3. Dunn DS. Outsider privileges can lead to insider disadvantages: some psychosocial aspects of ableism. J Soc Issues. 2019;75(3):665-682. https://doi.org/10.1111/josi.12331
4. Kothari S. Clinical (mis)judgments of quality of life after disability. J Clin Ethics. 2004;15:300-307.
5. National Council on Disability. Medical futility and disability bias: part of the bioethics and disability series. November 19, 2019. Accessed March 31, 2021. https://www.ncd.gov/sites/default/files/NCD_Medical_Futility_Report_508.pdf
6. Iezzoni LI, Rao SR, Ressalam J, et al. Physicians’ perceptions of people with disability and their health care. Health Aff (Millwood). 2021;40(2):297-306. https://doi.org/10.1377/hlthaff.2020.01452
7. Okoro CA, Hollis ND, Cyrus AC, Griffin-Blake S. Prevalence of disabilities and health care access by disability status and type among adults - United States, 2016. MMWR Morb Mortal Wkly Rep. 2018;67(32):882-887. https://doi.org/10.15585/mmwr.mm6732a3
8. Meade MA, Mahmoudi E, Lee SY. The intersection of disability and healthcare disparities: a conceptual framework. Disabil Rehabil. 2015;37(7):632-641. https://doi.org/10.3109/09638288.2014.938176
9. Andrews EE, Ayers KB, Brown KS, Dunn DS, Pilarski CR. No body is expendable: medical rationing and disability justice during the COVID-19 pandemic. Am Psychol. Published online July 23, 2020. https://doi.org/10.1037/amp0000709
10. Savin K, Guidry-Grimes L. Confronting disability discrimination during the pandemic. The Hastings Center. April 2, 2020. Accessed March 31, 2021. https://www.thehastingscenter.org/confronting-disability-discrimination-during-the-pandemic/
11. Health and Human Services Office for Civil Rights in Action. Bulletin: civil rights, HIPAA, and the coronavirus disease 2019. March 28, 2020. Accessed March 31, 2021. https://www.hhs.gov/sites/default/files/ocr-bulletin-3-28-20.pdf
12. Preventing discrimination in the treatment of COVID-19 patients: the illegality of medical rationing on the basis of disability. Disability Rights Education & Defense Fund. March 25, 2020. Accessed March 31, 2021. https://dredf.org/wp-content/uploads/2020/03/DREDF-Policy-Statement-on-COVID-19-and-Medical-Rationing-3-25-2020.pdf
13. Oregon hospitals told not to withhold care because of a person’s disability. Transcript. Morning Edition. National Public Radio. December 21, 2020. Accessed March 31, 2021. https://www.npr.org/2020/12/21/948697808/oregon-hospitals-told-not-to-withhold-care-because-of-a-persons-disability
14. As hospitals fear being overwhelmed by COVID-19, do the disabled get the same access? Transcript. Morning Edition. National Public Radio. December 14, 2020. Accessed March 31, 2021. https://www.npr.org/2020/12/14/945056176/as-hospitals-fear-being-overwhelmed-by-covid-19-do-the-disabled-get-the-same-acc
15. Lund EM, Forber-Pratt AJ, Wilson C, Mona LR. The COVID-19 pandemic, stress, and trauma in the disability community: a call to action. Rehabil Psychol. 2020;65(4):313-322. https://doi.org/10.1037/rep0000368
16. Auriemma CL, Molinero AM, Houtrow AJ, Persad G, White DB, Halpern SD. Eliminating categorical exclusion criteria in crisis standards of care frameworks. Am J Bioeth. 2020;20(7):28-36. http://doi.org/10.1080/15265161.2020.1764141
17. Bogart KR, Dunn DS. Ableism special issue introduction. J Soc Issues. 2019;75(3):650-664. https://doi.org/10.1111/josi.12354

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The COVID-19 pandemic has put an extraordinary strain on US hospitals.1 In spring 2020, many hospitals had to quickly adapt to treat a surge of patients, and many more had to prepare for a potential surge. Creating reserve capacity meant halting outpatient care and elective surgeries, repurposing inpatient units, and increasing critical care staffing. Hospitals again face these difficult decisions, as COVID-19 resurges and variants of SARS-CoV-2 increasingly circulate, with large financial losses projected for 2021.2 Some large hospital systems may have the financial reserves to weather this storm, but the precarious situation facing others likely requires policy action.

Hospitals’ financial stress emanates from multiple quarters. First, revenue from elective inpatient procedures and outpatient care dropped dramatically, has not fully rebounded,3,4 and is not fully offset by revenue from COVID-19 care. Second, high unemployment may force up to 20% of commercially insured Americans into lower-reimbursing public insurance or the ranks of the uninsured, generating a projected $95 billion annual loss for hospitals.5 Third, under the current payment system, the costs of preparing for a pandemic are not directly reimbursed. Yet—whether or not they ultimately experienced a large COVID-19 caseload—hospitals’ surge preparation has involved purchasing vast quantities of protective personal equipment (PPE) and other supplies and equipment, hiring additional staff, building SARS-CoV-2 testing capacity, and expanding occupational health services. Many expenses persist as “the new normal”: admissions now require SARS-CoV-2 testing, additional staff and PPE, and often, a private room. Physical distancing requirements mean hospitals’ capacity—and thus, revenue—will remain reduced.

Private insurers, by and large, are not volunteering to cover these increased costs, and it is difficult for hospitals to pass them along. Payment terms in many contracts (eg, for Medicare) are not modifiable; even where they are, renegotiating takes time. To date, federal relief payments from the CARES Act do not fully reimburse COVID-19 losses—a particular problem for smaller and safety-net hospitals without large reserves.

This situation raises ethical concerns. For example, it is ethically relevant that COVID-19 resurgence and hospitalizations are linked to states’ decisions to reopen quickly to ease economic burdens on businesses and workers. One result has been to shift some of the pandemic’s economic burden to the healthcare sector. From a fairness perspective, there should be limits on the losses hospitals are forced to shoulder to maintain COVID-19 preparedness and services. Even if hospitals have reserves, spending them threatens funding for other essential activities, such as capital investment.

The current situation is also fraught with perverse incentives that could jeopardize safe care. With elective care remaining at risk of being reduced,6 pressure intensifies to deliver as many services as possible as quickly as possible, which may not align with patients’ best interests. Across hospitals that need to maximize volume to survive, a push to keep elective services open may emerge, even as COVID-19 prevalence may favor a shutdown. Hospitals with a heavy COVID-19 caseload may have greater difficulty reopening than competitors with lower caseloads, potentially impacting quality if patients seek elective care at lower-volume centers or in ways that disrupt continuity of care.

Ethical dilemmas are also raised by the delicate balancing of interests that hospitals have been engaging in among patient groups. How should they balance the needs of COVID-19 patients against potential harms to others who must delay care?

It is wrong to ask hospitals to make such choices when policy solutions are available. With the resurgence of COVID-19 must come a fresh, sustained program of federal financial relief for hospitals. While direct government support is the swiftest path, consideration should be given to the role of private insurers, which have benefited economically from the widespread deferment and forgoing of elective care. Voluntary or mandatory investments by insurers in helping hospitals survive the pandemic and weather the new normal are consonant with insurers’ commitment to providing their members access to high-quality healthcare.

The 200-page National Strategy document released by the Biden administration on January 21, 2021, promises some important assistance to hospitals.7 It includes plans to accelerate the production of PPE and other essential supplies using the Defense Production Act and other federal authorities, to rationalize nationwide distribution of these supplies and take steps to prevent price gouging, and to deploy federal personnel and assets to help surge critical-care personnel.

These steps, if fully funded and implemented, would bring welcome respite from some of the most vexing problems hospitals have encountered during COVID-19 surges. Yet, plans for direct financial relief for hospitals are strikingly absent from the National Strategy. Nor does the recently passed $1.9 trillion federal stimulus package provide dedicated funds for hospitals, though some funds earmarked for vaccine delivery may land at hospitals. These are consequential omissions in otherwise comprehensive, thoughtful pandemic response plans.

Future legislation should include an immediate revenue infusion to reimburse hospitals’ COVID-19 preparations and lost volume and a firm commitment of ongoing financial support for preparedness through the end of the pandemic at a level sufficient to offset COVID-19–related losses. Experience with the CARES Act also suggests specific lessons for statutory design: support for hospitals should be allocated based on actual COVID-19–related burden for preparation and care, unlike CARES Act grants that were allocated based on hospitals’ past revenue and Medicare billing. This resulted in some large payments to relatively well-off hospitals and scant support for others (eg, rural or safety-net hospitals) with substantial COVID-19–related losses, a misstep that should not be repeated.

Hospitals are an integral part of the nation’s public health system. In the context of a pandemic, they should not be forced to serve as a backstop for shortcomings in other parts of the system without assistance. They, and their mission during the pandemic, are too important to fail.

References

1. Khullar D, Bond AM, Schpero WL. COVID-19 and the financial health of US hospitals. JAMA. 2020;323(21):2127-2128. https://doi.org/10.1001/jama.2020.6269
2. Coleman-Lochner L. Hospitals plead for bailout in face of runaway pandemic bills. February 26, 2021. Accessed March 25, 2021. https://www.bloomberg.com/news/articles/2021-02-26/hospitals-plead-for-bailout-in-face-of-runaway-pandemic-bills
3. American Hospital Association. Hospitals and health systems continue to face unprecedented financial challenges due to COVID-19. June 2020. Accessed February 5. 2021. https://www.aha.org/system/files/media/file/2020/06/aha-covid19-financial-impact-report.pdf
4. Birkmeyer JD, Barnato A, Birkmeyer N, Bessler R, Skinner J. The impact of the COVID-19 pandemic on hospital admissions in the United States. Health Aff (Millwood). 2020;39(11):2010-2017. https://doi.org/10.1377/hlthaff.2020.00980
5. Teasdale B, Schulman KA. Are U.S. hospitals still “recession-proof”? N Engl J Med. 2020;383(13):e82. https://doi.org/10.1056/NEJMp2018846
6. Meredith JW, High KP, Freischlag JA. Preserving elective surgeries in the COVID-19 pandemic and the future. JAMA. 2020;324(17):1725-1726. https://doi.org/10.1001/jama.2020.19594
7. Biden JR. National strategy for the COVID-19 response and pandemic preparedness. Bloomberg. January 2021. Accessed February 8, 2021. https://www.whitehouse.gov/wp-content/uploads/2021/01/National-Strategy-for-the-COVID-19-Response-and-Pandemic-Preparedness.pdf

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1Armstrong Institute for Patient Safety and Quality, Johns Hopkins Medicine, Baltimore, Maryland; 2Department of Medicine, Johns Hopkins Medicine, Baltimore, Maryland; 3Stanford Law School, Stanford, California; 4Department of Medicine, Stanford University School of Medicine; Stanford, California; 5Freeman Spogli Institute for International Studies, Stanford, California.

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Dr. Kachalia serves in a systemwide role as senior vice president for patient safety and quality at Johns Hopkins Medicine.

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1Armstrong Institute for Patient Safety and Quality, Johns Hopkins Medicine, Baltimore, Maryland; 2Department of Medicine, Johns Hopkins Medicine, Baltimore, Maryland; 3Stanford Law School, Stanford, California; 4Department of Medicine, Stanford University School of Medicine; Stanford, California; 5Freeman Spogli Institute for International Studies, Stanford, California.

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Dr. Kachalia serves in a systemwide role as senior vice president for patient safety and quality at Johns Hopkins Medicine.

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1Armstrong Institute for Patient Safety and Quality, Johns Hopkins Medicine, Baltimore, Maryland; 2Department of Medicine, Johns Hopkins Medicine, Baltimore, Maryland; 3Stanford Law School, Stanford, California; 4Department of Medicine, Stanford University School of Medicine; Stanford, California; 5Freeman Spogli Institute for International Studies, Stanford, California.

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Dr. Kachalia serves in a systemwide role as senior vice president for patient safety and quality at Johns Hopkins Medicine.

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The COVID-19 pandemic has put an extraordinary strain on US hospitals.1 In spring 2020, many hospitals had to quickly adapt to treat a surge of patients, and many more had to prepare for a potential surge. Creating reserve capacity meant halting outpatient care and elective surgeries, repurposing inpatient units, and increasing critical care staffing. Hospitals again face these difficult decisions, as COVID-19 resurges and variants of SARS-CoV-2 increasingly circulate, with large financial losses projected for 2021.2 Some large hospital systems may have the financial reserves to weather this storm, but the precarious situation facing others likely requires policy action.

Hospitals’ financial stress emanates from multiple quarters. First, revenue from elective inpatient procedures and outpatient care dropped dramatically, has not fully rebounded,3,4 and is not fully offset by revenue from COVID-19 care. Second, high unemployment may force up to 20% of commercially insured Americans into lower-reimbursing public insurance or the ranks of the uninsured, generating a projected $95 billion annual loss for hospitals.5 Third, under the current payment system, the costs of preparing for a pandemic are not directly reimbursed. Yet—whether or not they ultimately experienced a large COVID-19 caseload—hospitals’ surge preparation has involved purchasing vast quantities of protective personal equipment (PPE) and other supplies and equipment, hiring additional staff, building SARS-CoV-2 testing capacity, and expanding occupational health services. Many expenses persist as “the new normal”: admissions now require SARS-CoV-2 testing, additional staff and PPE, and often, a private room. Physical distancing requirements mean hospitals’ capacity—and thus, revenue—will remain reduced.

Private insurers, by and large, are not volunteering to cover these increased costs, and it is difficult for hospitals to pass them along. Payment terms in many contracts (eg, for Medicare) are not modifiable; even where they are, renegotiating takes time. To date, federal relief payments from the CARES Act do not fully reimburse COVID-19 losses—a particular problem for smaller and safety-net hospitals without large reserves.

This situation raises ethical concerns. For example, it is ethically relevant that COVID-19 resurgence and hospitalizations are linked to states’ decisions to reopen quickly to ease economic burdens on businesses and workers. One result has been to shift some of the pandemic’s economic burden to the healthcare sector. From a fairness perspective, there should be limits on the losses hospitals are forced to shoulder to maintain COVID-19 preparedness and services. Even if hospitals have reserves, spending them threatens funding for other essential activities, such as capital investment.

The current situation is also fraught with perverse incentives that could jeopardize safe care. With elective care remaining at risk of being reduced,6 pressure intensifies to deliver as many services as possible as quickly as possible, which may not align with patients’ best interests. Across hospitals that need to maximize volume to survive, a push to keep elective services open may emerge, even as COVID-19 prevalence may favor a shutdown. Hospitals with a heavy COVID-19 caseload may have greater difficulty reopening than competitors with lower caseloads, potentially impacting quality if patients seek elective care at lower-volume centers or in ways that disrupt continuity of care.

Ethical dilemmas are also raised by the delicate balancing of interests that hospitals have been engaging in among patient groups. How should they balance the needs of COVID-19 patients against potential harms to others who must delay care?

It is wrong to ask hospitals to make such choices when policy solutions are available. With the resurgence of COVID-19 must come a fresh, sustained program of federal financial relief for hospitals. While direct government support is the swiftest path, consideration should be given to the role of private insurers, which have benefited economically from the widespread deferment and forgoing of elective care. Voluntary or mandatory investments by insurers in helping hospitals survive the pandemic and weather the new normal are consonant with insurers’ commitment to providing their members access to high-quality healthcare.

The 200-page National Strategy document released by the Biden administration on January 21, 2021, promises some important assistance to hospitals.7 It includes plans to accelerate the production of PPE and other essential supplies using the Defense Production Act and other federal authorities, to rationalize nationwide distribution of these supplies and take steps to prevent price gouging, and to deploy federal personnel and assets to help surge critical-care personnel.

These steps, if fully funded and implemented, would bring welcome respite from some of the most vexing problems hospitals have encountered during COVID-19 surges. Yet, plans for direct financial relief for hospitals are strikingly absent from the National Strategy. Nor does the recently passed $1.9 trillion federal stimulus package provide dedicated funds for hospitals, though some funds earmarked for vaccine delivery may land at hospitals. These are consequential omissions in otherwise comprehensive, thoughtful pandemic response plans.

Future legislation should include an immediate revenue infusion to reimburse hospitals’ COVID-19 preparations and lost volume and a firm commitment of ongoing financial support for preparedness through the end of the pandemic at a level sufficient to offset COVID-19–related losses. Experience with the CARES Act also suggests specific lessons for statutory design: support for hospitals should be allocated based on actual COVID-19–related burden for preparation and care, unlike CARES Act grants that were allocated based on hospitals’ past revenue and Medicare billing. This resulted in some large payments to relatively well-off hospitals and scant support for others (eg, rural or safety-net hospitals) with substantial COVID-19–related losses, a misstep that should not be repeated.

Hospitals are an integral part of the nation’s public health system. In the context of a pandemic, they should not be forced to serve as a backstop for shortcomings in other parts of the system without assistance. They, and their mission during the pandemic, are too important to fail.

The COVID-19 pandemic has put an extraordinary strain on US hospitals.1 In spring 2020, many hospitals had to quickly adapt to treat a surge of patients, and many more had to prepare for a potential surge. Creating reserve capacity meant halting outpatient care and elective surgeries, repurposing inpatient units, and increasing critical care staffing. Hospitals again face these difficult decisions, as COVID-19 resurges and variants of SARS-CoV-2 increasingly circulate, with large financial losses projected for 2021.2 Some large hospital systems may have the financial reserves to weather this storm, but the precarious situation facing others likely requires policy action.

Hospitals’ financial stress emanates from multiple quarters. First, revenue from elective inpatient procedures and outpatient care dropped dramatically, has not fully rebounded,3,4 and is not fully offset by revenue from COVID-19 care. Second, high unemployment may force up to 20% of commercially insured Americans into lower-reimbursing public insurance or the ranks of the uninsured, generating a projected $95 billion annual loss for hospitals.5 Third, under the current payment system, the costs of preparing for a pandemic are not directly reimbursed. Yet—whether or not they ultimately experienced a large COVID-19 caseload—hospitals’ surge preparation has involved purchasing vast quantities of protective personal equipment (PPE) and other supplies and equipment, hiring additional staff, building SARS-CoV-2 testing capacity, and expanding occupational health services. Many expenses persist as “the new normal”: admissions now require SARS-CoV-2 testing, additional staff and PPE, and often, a private room. Physical distancing requirements mean hospitals’ capacity—and thus, revenue—will remain reduced.

Private insurers, by and large, are not volunteering to cover these increased costs, and it is difficult for hospitals to pass them along. Payment terms in many contracts (eg, for Medicare) are not modifiable; even where they are, renegotiating takes time. To date, federal relief payments from the CARES Act do not fully reimburse COVID-19 losses—a particular problem for smaller and safety-net hospitals without large reserves.

This situation raises ethical concerns. For example, it is ethically relevant that COVID-19 resurgence and hospitalizations are linked to states’ decisions to reopen quickly to ease economic burdens on businesses and workers. One result has been to shift some of the pandemic’s economic burden to the healthcare sector. From a fairness perspective, there should be limits on the losses hospitals are forced to shoulder to maintain COVID-19 preparedness and services. Even if hospitals have reserves, spending them threatens funding for other essential activities, such as capital investment.

The current situation is also fraught with perverse incentives that could jeopardize safe care. With elective care remaining at risk of being reduced,6 pressure intensifies to deliver as many services as possible as quickly as possible, which may not align with patients’ best interests. Across hospitals that need to maximize volume to survive, a push to keep elective services open may emerge, even as COVID-19 prevalence may favor a shutdown. Hospitals with a heavy COVID-19 caseload may have greater difficulty reopening than competitors with lower caseloads, potentially impacting quality if patients seek elective care at lower-volume centers or in ways that disrupt continuity of care.

Ethical dilemmas are also raised by the delicate balancing of interests that hospitals have been engaging in among patient groups. How should they balance the needs of COVID-19 patients against potential harms to others who must delay care?

It is wrong to ask hospitals to make such choices when policy solutions are available. With the resurgence of COVID-19 must come a fresh, sustained program of federal financial relief for hospitals. While direct government support is the swiftest path, consideration should be given to the role of private insurers, which have benefited economically from the widespread deferment and forgoing of elective care. Voluntary or mandatory investments by insurers in helping hospitals survive the pandemic and weather the new normal are consonant with insurers’ commitment to providing their members access to high-quality healthcare.

The 200-page National Strategy document released by the Biden administration on January 21, 2021, promises some important assistance to hospitals.7 It includes plans to accelerate the production of PPE and other essential supplies using the Defense Production Act and other federal authorities, to rationalize nationwide distribution of these supplies and take steps to prevent price gouging, and to deploy federal personnel and assets to help surge critical-care personnel.

These steps, if fully funded and implemented, would bring welcome respite from some of the most vexing problems hospitals have encountered during COVID-19 surges. Yet, plans for direct financial relief for hospitals are strikingly absent from the National Strategy. Nor does the recently passed $1.9 trillion federal stimulus package provide dedicated funds for hospitals, though some funds earmarked for vaccine delivery may land at hospitals. These are consequential omissions in otherwise comprehensive, thoughtful pandemic response plans.

Future legislation should include an immediate revenue infusion to reimburse hospitals’ COVID-19 preparations and lost volume and a firm commitment of ongoing financial support for preparedness through the end of the pandemic at a level sufficient to offset COVID-19–related losses. Experience with the CARES Act also suggests specific lessons for statutory design: support for hospitals should be allocated based on actual COVID-19–related burden for preparation and care, unlike CARES Act grants that were allocated based on hospitals’ past revenue and Medicare billing. This resulted in some large payments to relatively well-off hospitals and scant support for others (eg, rural or safety-net hospitals) with substantial COVID-19–related losses, a misstep that should not be repeated.

Hospitals are an integral part of the nation’s public health system. In the context of a pandemic, they should not be forced to serve as a backstop for shortcomings in other parts of the system without assistance. They, and their mission during the pandemic, are too important to fail.

References

1. Khullar D, Bond AM, Schpero WL. COVID-19 and the financial health of US hospitals. JAMA. 2020;323(21):2127-2128. https://doi.org/10.1001/jama.2020.6269
2. Coleman-Lochner L. Hospitals plead for bailout in face of runaway pandemic bills. February 26, 2021. Accessed March 25, 2021. https://www.bloomberg.com/news/articles/2021-02-26/hospitals-plead-for-bailout-in-face-of-runaway-pandemic-bills
3. American Hospital Association. Hospitals and health systems continue to face unprecedented financial challenges due to COVID-19. June 2020. Accessed February 5. 2021. https://www.aha.org/system/files/media/file/2020/06/aha-covid19-financial-impact-report.pdf
4. Birkmeyer JD, Barnato A, Birkmeyer N, Bessler R, Skinner J. The impact of the COVID-19 pandemic on hospital admissions in the United States. Health Aff (Millwood). 2020;39(11):2010-2017. https://doi.org/10.1377/hlthaff.2020.00980
5. Teasdale B, Schulman KA. Are U.S. hospitals still “recession-proof”? N Engl J Med. 2020;383(13):e82. https://doi.org/10.1056/NEJMp2018846
6. Meredith JW, High KP, Freischlag JA. Preserving elective surgeries in the COVID-19 pandemic and the future. JAMA. 2020;324(17):1725-1726. https://doi.org/10.1001/jama.2020.19594
7. Biden JR. National strategy for the COVID-19 response and pandemic preparedness. Bloomberg. January 2021. Accessed February 8, 2021. https://www.whitehouse.gov/wp-content/uploads/2021/01/National-Strategy-for-the-COVID-19-Response-and-Pandemic-Preparedness.pdf

References

1. Khullar D, Bond AM, Schpero WL. COVID-19 and the financial health of US hospitals. JAMA. 2020;323(21):2127-2128. https://doi.org/10.1001/jama.2020.6269
2. Coleman-Lochner L. Hospitals plead for bailout in face of runaway pandemic bills. February 26, 2021. Accessed March 25, 2021. https://www.bloomberg.com/news/articles/2021-02-26/hospitals-plead-for-bailout-in-face-of-runaway-pandemic-bills
3. American Hospital Association. Hospitals and health systems continue to face unprecedented financial challenges due to COVID-19. June 2020. Accessed February 5. 2021. https://www.aha.org/system/files/media/file/2020/06/aha-covid19-financial-impact-report.pdf
4. Birkmeyer JD, Barnato A, Birkmeyer N, Bessler R, Skinner J. The impact of the COVID-19 pandemic on hospital admissions in the United States. Health Aff (Millwood). 2020;39(11):2010-2017. https://doi.org/10.1377/hlthaff.2020.00980
5. Teasdale B, Schulman KA. Are U.S. hospitals still “recession-proof”? N Engl J Med. 2020;383(13):e82. https://doi.org/10.1056/NEJMp2018846
6. Meredith JW, High KP, Freischlag JA. Preserving elective surgeries in the COVID-19 pandemic and the future. JAMA. 2020;324(17):1725-1726. https://doi.org/10.1001/jama.2020.19594
7. Biden JR. National strategy for the COVID-19 response and pandemic preparedness. Bloomberg. January 2021. Accessed February 8, 2021. https://www.whitehouse.gov/wp-content/uploads/2021/01/National-Strategy-for-the-COVID-19-Response-and-Pandemic-Preparedness.pdf

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A 19-year-old woman presented to the emergency department (ED) with a 14-day history of progressive fevers, night sweats, abdominal pain, nonbloody and nonbilious vomiting, diarrhea, cough, and myalgia. The fever occurred daily with no noted temporal pattern, and she had no significant weight loss. The abdominal pain was diffuse and exacerbated by eating. She experienced multiple sporadic episodes of vomiting and diarrhea daily. She denied any rash or arthralgia.

She had no known medical history and took no medications. Family history was negative for autoinflammatory and autoimmune conditions. She had emigrated from Kenya to the United States 28 days ago. Her immunization status was unknown.

This patient has prolonged fevers and evidence of multisystem involvement. The most likely etiologic categories are infectious, inflammatory, rheumatologic, and neoplastic. For febrile patients who have recently emigrated to or travelled outside of the United States, it is important to consider common infections, as well as those endemic to the nation of exposure, which in this case includes malaria, typhoid fever, tuberculosis, cholera, acute viral hepatitis, chikungunya fever, dengue fever, yellow fever, and rickettsial disease. All of these, other than tuberculosis, commonly present with fever, vomiting, diarrhea, and myalgia. She may also have bacterial pneumonia or influenza given her fever and cough, although the chronicity and persistence of symptoms would be atypical. Acute infectious gastroenteritis is a common cause of fever, vomiting, and diarrhea. Most cases resolve in 7 to 10 days, so the duration raises suspicion for a nonviral etiology or an immunocompromised state.

Inflammatory causes could include the first presentation of inflammatory bowel disease (IBD), particularly if the patient develops weight loss or eye, skin, or joint manifestations. The lack of rash or arthralgia makes rheumatologic conditions less likely. Prolonged fevers and night sweats could indicate malignancy such as intra-abdominal lymphoma, although infectious etiologies should be ruled out first.

Previously, on day 9 of symptoms, the patient presented to an ED at another institution. Laboratory evaluation at that time demonstrated an elevated aspartate aminotransferase (AST) level of 229 IU/L (reference, 0-40 IU/L) and alanine aminotransferase (ALT) level of 60 IU/L (reference, 0-32 IU/L) with normal alkaline phosphatase and bilirubin levels, proteinuria to 3+ (normal, negative/trace), ketonuria to 2+ (normal, negative), and hematuria to 2+ (normal, negative). Complete blood count and electrolytes were normal. Computed tomography (CT) scans of the chest, abdomen, and pelvis with intravenous contrast were normal and without evidence of organomegaly.

AST and ALT elevations often indicate hepatocellular damage, although the normal bilirubin levels suggest normal hepatic function. Because CT may miss extrahepatic biliary pathology, a right upper quadrant ultrasound should be obtained to better evaluate patency of the biliary system and hepatic echotexture. Coagulation studies and viral hepatitis serology should be obtained. The disproportionate elevation of AST versus ALT can suggest alcohol use or nonhepatic etiologies such as myositis. Acute viral hepatitis is less likely given there is only mild to moderate elevation in aminotransferase levels. However, the remaining infectious etiologies can have this level of elevation and should still be considered.

Enteritis and IBD are still considerations despite the normal CT results. Transient asymptomatic hematuria or proteinuria can be seen in multiple conditions, particularly proteinuria with febrile illnesses. Urine microscopy to evaluate for casts could indicate a glomerular origin of the hematuria. First morning urine protein-to-creatinine ratio would help quantify the degree of proteinuria. Serum creatinine level should be measured to determine whether there is any renal dysfunction.

While early imaging can be falsely negative, the unremarkable chest CT makes pneumonia and active pulmonary tuberculosis less likely.

Vital signs during this presentation were: temperature, 39.7 °C; heart rate, 126 beats per minute; blood pressure, 109/64 mm Hg; respiratory rate, 20 breaths per minute; and oxygen saturation, 98% on room air. She was ill-appearing, with diffuse abdominal tenderness without peritoneal signs. Other than her tachycardia, findings from her cardiopulmonary, neurologic, and skin exams were normal.

Laboratory testing revealed a white blood cell count of 4,300/µL (reference range, 4,500-13,000/µL), a hemoglobin level of 10.9 g/dL (reference range, 11.7-15.7 g/dL) with a mean corpuscular volume of 77 fL (reference range, 80-96 fL) and reticulocyte percentage of 0.5% (reference range, 0.5%-1.5%), and a platelet count of 59,000/µL (reference range, 135,000-466,000/µL). Her prothrombin time was 13.5 seconds (reference range, 9.6-11.6 seconds) with an international normalized ratio of 1.3 (reference range, 0.8-1.1), erythrocyte sedimentation rate of 46 mm/h (reference range, 0-20 mm/h), C-reactive protein level of 7.49 mg/dL (reference range, <0.3 mg/dL), and AST level of 194 units/L (reference range, 9-35 units/L). ALT, total and direct bilirubin, lipase, electrolytes, and creatinine levels were normal. An abdominal x-ray showed scattered air-fluid levels in a nonobstructed pattern.

Her mildly elevated prothrombin time and international normalized ratio suggest a coagulopathy involving either her extrinsic or common coagulation pathway, with disseminated intravascular coagulation (DIC) being most likely given her new thrombocytopenia and anemia. Hemolytic uremic syndrome and thrombotic thrombocytopenic purpura should be considered but would not cause coagulopathy. A peripheral smear to evaluate for schistocytes associated with microangiopathic hemolysis and serum fibrinogen to distinguish between DIC (low) and thrombocytopenic purpura or hemolytic uremic syndrome (normal or elevated) should be obtained. A thick and thin smear for malaria should also be performed.

Her new pancytopenia suggests bone marrow suppression or infiltration with or without a concomitant consumptive process such as sepsis with resulting DIC. Given her clinical picture, marrow infiltrative processes might include tuberculosis or malignancy, and marrow suppression may be caused by HIV or other viral infection. If she is found to have HIV, disseminated fungal or mycobacterial infections would become more likely. She now has an isolated elevated AST level, which could be secondary to hemolysis rather than hepatocyte damage. Findings from her abdominal exam are nonfocal; this is consistent with her x-ray findings, which reflect possible enteritis or colitis.

The most likely diagnosis currently is an infectious enteritis with resulting hematologic and hepatic abnormalities. Given her recent emigration from Kenya, typhoid fever and cholera are both possible, although cholera typically does not present with prolonged fever or severe abdominal pain. The severity and duration of her illness, and the abnormalities of her laboratory findings, warrant empiric therapy with ceftriaxone to treat possible severe Salmonella enterica infection while awaiting blood and stool cultures.

The patient was admitted to the hospital and her symptoms continued. Results of serum HIV 1 and 2 polymerase chain reactions, herpes simplex virus 1 and 2 polymerase chain reactions, three malaria smears, human T-lymphotropic virus serologies, Toxoplasma serology, Bartonella serology, a stool culture, and multiple large volume blood cultures were negative. Serologic testing for hepatitis A, B, and C, Epstein-Barr virus, cytomegalovirus, and dengue virus were negative for acute infection. Results of an interferon-gamma release assay were indeterminate; results of purified protein derivative (PPD) and Candida antigen control testing were both negative. Ceruloplasmin and α1-antitrypsin levels were normal. An abdominal ultrasound showed central intrahepatic biliary duct dilatation, splenomegaly, and sluggish portal venous flow.

While central intrahepatic biliary ductal dilation could be caused by an obstructive lesion, none were seen on CT or ultrasound. Her normal alkaline phosphatase and bilirbuin levels also suggest functional patency of the biliary system. The thrombocytopenia, splenomegaly, and sluggish portal venous flow suggest possible portal hypertension, though no cirrhotic changes were noted on the ultrasound or abdominal CT. Her negative PPD and Candida antigen control results may suggest underlying immune dysregulation or suppression, though anergy could be secondary to sepsis.

Given her negative initial infectious evaluation, other etiologies such as atypical infections, rheumatologic disorders, and malignancies warrant consideration. She has no murmur; however, subacute bacterial endocarditis with a fastidious organism is possible, which could be investigated with a transthoracic echocardiogram. Other tests to consider include blood cultures for fungi and atypical mycobacterial species, and serology for Coxiella burnetii, chikungunya virus, and yellow fever. Rheumatologic conditions such as systemic lupus erythematosus, hemophagocytic lymphohistiocytosis (HLH), or adult Still’s disease should be considered. Complement levels and an antinuclear antibody panel, including those for dsDNA and Smith antigen, should be performed to evaluate for systemic lupus erythematosus. Serum ferritin, fibrinogen, and triglyceride levels should be measured to evaluate for HLH. Hematologic malignancy is also a consideration, particularly given her pancytopenia. Multicentric Castleman disease can cause prolonged fevers, pancytopenia, and elevated inflammatory markers, but is less likely without lymphadenopathy. A peripheral blood smear should be sent, and a bone marrow biopsy may be needed.

Empiric ciprofloxacin was initiated; however, the patient continued to have fevers up to 39.9 °C, abdominal pain, and myalgia. Ferritin level was over 3,000 ng/mL (reference range, 8-255 ng/mL), and a soluble interleukin-2 (IL-2) receptor level was 1,188 units/mL (reference range, 45-1,105 units/mL). Triglycerides were normal.

The elevated ferritin and soluble IL-2 levels raise concern for HLH. Hyperferritinemia is relatively nonspecific because extremely elevated ferritin can be seen with other conditions, such as renal failure, hepatocellular injury, infection, rheumatologic conditions, and hematologic malignancy. Soluble IL-2 receptor elevation is more specific for HLH than ferritin or triglycerides, but alone does not make the diagnosis because it can be elevated in other rheumatologic disorders and malignancy. The HLH-2004 criteria are commonly used and require either molecular diagnostic testing or meeting at least five out of eight clinical and lab criteria to make the diagnosis. Our patient currently meets three criteria (fever, splenomegaly, and elevated ferritin). Elevated soluble IL-2 is part of the HLH-2004 criteria, but her level of elevation does not meet the required threshold (≥2,400 units/mL). Her cytopenias have also not quite met the HLH-2004 thresholds (two of the following three: hemoglobin <9 g/dL, platelets <100,000/µL, and/or absolute neutrophil count <1,000/µL). Elevated aminotransferase levels and DIC are not part of the HLH-2004 criteria but are often seen with HLH.

Evaluation for an underlying infectious, rheumatologic, or malignant trigger should continue as previously discussed. If this patient does have HLH, it is most likely secondary to an infection, autoimmune disease, or malignancy rather than genetic HLH. HLH has a high mortality rate, but before beginning treatment with immunosuppressive agents, a peripheral smear and a bone marrow biopsy should be performed to evaluate for hematologic malignancy or signs of hemophagocytosis.

Empiric ciprofloxacin covers most bacterial etiologies of diarrhea, including those previously mentioned such as cholera and most strains of S enterica. Her symptoms and laboratory findings (including cytopenias, elevated aminotransferases, and coagulopathy) could suggest enteric fever due to S enterica serovar Typhi, which is endemic in Kenya. Results of blood and stool cultures, though negative, are relatively insensitive for this organism, particularly this far into the illness course. A bone marrow biopsy may also help with diagnosis of occult typhoid fever because marrow culture can be more sensitive than blood or stool culture.

A bone marrow aspiration revealed hemophagocytic histiocytes, no malignant cells, and negative bacterial (including anaerobic), fungal, and acid-fast bacilli cultures. Considering the high mortality rate of untreated HLH/macrophage activation syndrome (MAS), empiric glucocorticoid administration was considered. However, this was withheld due to concern for ongoing undetected infection given her persistent fever and systemic symptoms.

There should still be high suspicion for HLH. Further evaluation for other laboratory manifestations of HLH such as fibrinogen and natural killer cell activity should be considered, as well as repeating her complete blood count to see if her cytopenias have progressed. Her marrow shows no evidence of hematologic malignancy, so other triggers of possible HLH should be sought out by continuing the workup. Consulting specialists from rheumatology and infectious disease may help clarify possible underlying diagnoses and the best management plan. If she continues to have organ damage or clinically worsens, it may be prudent to empirically broaden her antibiotic coverage and begin antifungal agents while starting glucocorticoid therapy for suspected HLH.

A stool molecular screen from admission was returned positive for S enterica serovar Typhi. Ciprofloxacin was discontinued and ceftriaxone was started out of concern for antibiotic resistance. On hospital day 14, the patient’s brother presented to the ED with fever. His blood and stool cultures were positive for S enterica serovar Typhi with intermediate sensitivity to ciprofloxacin and sensitivity to ceftriaxone. With continued treatment with ceftriaxone, the patient improved significantly. Following discharge, she remained afebrile and asymptomatic. During outpatient follow up, a repeat PPD was positive and she was diagnosed with and treated for latent tuberculosis.

COMMENTARY

The evaluation of a patient who has recently emigrated from a foreign nation requires a broad differential diagnosis and a keen awareness of the clinical conditions present in the patient’s country of origin. This often involves knowledge of diseases infrequently encountered in daily practice, as well as awareness of the nuances of rare presentations and possible complications. When the presentation is not classic for a relevant infectious disease and clinical conditions from other diagnostic classes are considered, the evaluation and management of the patient is particularly challenging.

Typhoid fever is a severe systemic illness caused by the organism S enterica serovar Typhi. The organism is ingested, penetrates the small intestinal epithelium, enters the lymphoid tissue, and disseminates via the lymphatic and hematogenous routes. Onset of symptoms typically occurs 5 to 21 days after ingestion of contaminated food or water. Clinical features include fever, chills, relative bradycardia (pulse-temperature dissociation), abdominal pain, rose spots (salmon-colored macules) on the trunk and abdomen, and hepatosplenomegaly. Diarrhea is not a typical symptom of patients with typhoid fever, which can lead to a delayed or missed diagnosis. Life-threatening complications can be seen, including gastrointestinal bleeding, intestinal perforation, and meningitis.1 Typhoid fever is most prevalent in impoverished areas with poor access to sanitation. Regions with the highest incidence include south-central Asia, southeast Asia, and southern Africa.2-4 Approximately 200 to 300 cases are reported in the United States each year.5

Classically, the diagnosis is made by means of clinical symptoms and a positive culture from a sterile site. A recent study of 529 patients found that 61% had positive blood cultures and 96% had positive bone marrow cultures.6 Our patient’s diagnosis was significantly delayed by multiple negative cultures and failure to improve on first-line antibiotics, which initially suggested that the S enterica serovar Typhi stool molecular screen likely represented carriage caused by colonization. Chronic S enterica serovar Typhi carriage is defined as excretion of the organism in stool or urine 1 year or longer after acute infection. Rates of carriage range from 1% to 6%, and up to 25% of carriers have no history of typhoid fever.1,7,8 Carriage is more common in females and in those with biliary tract abnormalities.9,10

Once a presumptive diagnosis is made, antibiotic choice remains a challenge. Resistance to fluoroquinolones, the preferred drug for multidrug-resistant typhoid fever, is growing but remains rare, at approximately 5%.11,12 Ceftriaxone and azithromycin have been used successfully in areas with high resistance.13 Given the patient’s slow response to therapy even after transitioning from ciprofloxacin to ceftriaxone, her brother’s presentation and obtaining the antibiotic sensitivities for his organism were critical to confirming that our diagnosis and management decisions were correct.

One strongly considered diagnosis was HLH/MAS. MAS is an aggressive syndrome of excessive inflammation and tissue destruction caused by inappropriate immune system activation. It belongs to a group of histiocytic disorders collectively known as HLH. Aside from primary (genetic) forms, secondary forms exist that can be triggered by malignancy, infection, or rheumatologic disorders. In infection-associated HLH/MAS, viral infections are a common trigger, with Epstein-Barr virus being the most common. Association with bacterial infections, including tuberculosis and typhoid fever, has also been reported.14 Prompt therapy, often with immunosuppressive agents such as glucocorticoids, is essential for survival because there is a reported mortality rate of up to 50% when untreated.15 When infection-induced HLH/MAS occurs, treatment of the underlying infection is critical.14,15 The greatest barrier to a favorable outcome from HLH/MAS is often a delay in diagnosis because the rarity of this disease, the variable clinical presentation, and the lack of specificity of the clinical and laboratory findings make a conclusive diagnosis challenging.

In the presented case, diagnostic uncertainty challenged the decision to administer systemic glucocorticoids. Glucocorticoids conferred a risk of harm for multiple diagnoses that remained on the differential, including malignancy and infection. Her diagnostic evaluation made malignancy less likely, but because testing was unable to rule out tuberculosis as either the underlying cause or coinfection, the team opted to defer initiating glucocorticoids and instead closely monitor for a worsening inflammatory response. Following appropriate treatment of her systemic infection, her PPD was repeated and became positive. The negative PPD and Candida control obtained during her hospitalization were, therefore, likely caused by anergy in the setting of overwhelming systemic illness. Initiation of glucocorticoids prematurely in this case could have led to further harm because immunosuppression may have led to reactivation of latent tuberculosis or exacerbation of illness from an alternative but then undiagnosed infection.

The patient’s ultimate unifying diagnosis was typhoid fever; however, there are mixed expert opinions as to whether the systemic immune activation was significant enough to merit the diagnosis of infection-induced secondary HLH/MAS. Despite the high morbidity and mortality that can accompany HLH/MAS, it has been reported that a significant proportion of cases of secondary HLH/MAS can be managed effectively with treatment of the underlying etiology; this may have been the case for our patient.14,15 The clinicians in this case were caught between diagnoses, unable to safely reach either one—much like a baseball player stranded between bases. Fortunately for this patient, the diagnosis ultimately emerged after a careful and thorough workup, assisted by the more straightforward diagnosis of her brother with the same disease.

KEY TEACHING POINTS

  • Salmonella enterica serovar Typhi has a high false-negative rate in blood and stool cultures; therefore, clinical suspicion should remain high in the setting of a high pre-test probability.
  • Fluoroquinolones are traditionally first-line therapy for typhoid fever, but the use of ceftriaxone and azithromycin is increasing because of rising fluoroquinolone resistance.
  • Hemophagocytic lymphohistiocytosis/macrophage activation syndrome is characterized by excessive inflammation and tissue destruction caused by inappropriate immune system activation. This syndrome can be fatal without appropriate immunosuppressive therapy; however, glucocorticoid administration must be pursued with caution when infection and malignancy are on the differential diagnosis.
References

1. Parry CM, Hien TT, Dougan G, et al. Typhoid fever. N Engl J Med. 2002;347(22):1770-1782. https://doi.org/10.1056/nejmra020201
2. Crump JA, Luby SP, Mintz ED. The global burden of typhoid fever. Bull World Health Organ. 2004;82(5):346-353.
3. Buckle GC, Walker CL, Black RE. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J Glob Health. 2012;2(1):010401. https://doi.org/10.7189/jogh.02.010401
4. Mogasale V, Maskery B, Ochiai RL, et al. Burden of typhoid fever in low-income and middle-income countries: a systematic, literature-based update with risk-factor adjustment. Lancet Glob Health. 2014;2(10):e570-e580. https://doi.org/10.1016/s2214-109x(14)70301-8
5. Lynch MF, Blanton EM, Bulens S, et al. Typhoid fever in the United States, 1999-2006. JAMA. 2009;302(8):859-865. https://doi.org/10.1001/jama.2009.1229
6. Mogasale V, Ramani E, Mogasale VV, Park J. What proportion of Salmonella typhi cases are detected by blood culture? a systematic literature review. Ann Clin Microbiol Antimicrob. 2016;15(1):32. https://doi.org/10.1186/s12941-016-0147-z
7. Merselis JG Jr, Kaye D, Connolly CS, Hook EW. Quantitative bacteriology of the Typhoid carrier state. Am J Trop Med Hyg. 1964;13:425-429. https://doi.org/10.4269/ajtmh.1964.13.425
8. Lanata CF, Levine MM, Ristori C, et al. Vi serology in detection of chronic Salmonella typhi carriers in an endemic area. Lancet. 1983;2(8347):441-443. https://doi.org/10.1016/s0140-6736(83)90401-4
9. Lai CW, Chan RC, Cheng AF, Sung JY, Leung JW. Common bile duct stones: a cause of chronic salmonellosis. Am J Gastroenterol. 1992;87(9):1198-1199.
10. Hofmann E, Chianale J, Rollán A, Pereira J, Ferrecio C, Sotomayor V. Blood group antigen secretion and gallstone disease in the Salmonella typhi chronic carrier state. J Infect Dis. 1993;167(4):993-994. https://doi.org/10.1093/infdis/167.4.993
11. Steel AD, Hay Burgess DC, Diaz Z, Carey ME, Zaidi AKM. Challenges and opportunities for typhoid fever control: a call for coordinated action. Clin Infect Dis. 2016;62 (Suppl 1):S4-S8. https://doi.org/10.1093/cid/civ976
12. Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, et al. Genomic signature of multidrug resistant Salmonella enterica serovar Typhi isolates related to a massive outbreak in Zambia between 2010 and 2012. J Clin Microbiol. 2015;53(1):262-272. https://doi.org/10.1128/jcm.02026-14
13. Crump JA, Sjölund-Karlsson M, Gordon MA, Parry CM. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of Salmonella infections. Clin Microbiol Rev. 2015;28(4):901-936. https://doi.org/10.1128/cmr.00002-15
14. Rouphael NG, Talati NJ, Vaughan C, Cunningham K, Moreira R, Gould C. Infections associated with haemophagocytic syndrome. Lancet Infect Dis. 2007;7(12):814-822. https://doi.org/10.1016/s1473-3099(07)70290-6
15. Fisman DN. Hemophagocytic syndromes and infection. Emerg Infect Dis. 2000;6(6):601-608. https://doi.org/10.3201/eid0606.000608

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1Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; 2Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio; 3Division of Hospital Medicine, Children’s Hospital of Los Angeles, Los Angeles, California; 4Department of Pediatrics, Keck School of Medicine, University of Southern California, Los Angeles, California; 5Department of Medicine, University of California, San Francisco, California; 6Medical Service, San Francisco VA Medical Center, San Francisco, California; 7Division of Infectious Diseases, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; 8Division of Rheumatology, Children’s Hospital of Philadelphia, Philadelphia, Pennsylvania; 9Department of Pediatrics, Perelman School of Medicine, University of Pennsylvania, Philadelphia, Pennsylvania.

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A 19-year-old woman presented to the emergency department (ED) with a 14-day history of progressive fevers, night sweats, abdominal pain, nonbloody and nonbilious vomiting, diarrhea, cough, and myalgia. The fever occurred daily with no noted temporal pattern, and she had no significant weight loss. The abdominal pain was diffuse and exacerbated by eating. She experienced multiple sporadic episodes of vomiting and diarrhea daily. She denied any rash or arthralgia.

She had no known medical history and took no medications. Family history was negative for autoinflammatory and autoimmune conditions. She had emigrated from Kenya to the United States 28 days ago. Her immunization status was unknown.

This patient has prolonged fevers and evidence of multisystem involvement. The most likely etiologic categories are infectious, inflammatory, rheumatologic, and neoplastic. For febrile patients who have recently emigrated to or travelled outside of the United States, it is important to consider common infections, as well as those endemic to the nation of exposure, which in this case includes malaria, typhoid fever, tuberculosis, cholera, acute viral hepatitis, chikungunya fever, dengue fever, yellow fever, and rickettsial disease. All of these, other than tuberculosis, commonly present with fever, vomiting, diarrhea, and myalgia. She may also have bacterial pneumonia or influenza given her fever and cough, although the chronicity and persistence of symptoms would be atypical. Acute infectious gastroenteritis is a common cause of fever, vomiting, and diarrhea. Most cases resolve in 7 to 10 days, so the duration raises suspicion for a nonviral etiology or an immunocompromised state.

Inflammatory causes could include the first presentation of inflammatory bowel disease (IBD), particularly if the patient develops weight loss or eye, skin, or joint manifestations. The lack of rash or arthralgia makes rheumatologic conditions less likely. Prolonged fevers and night sweats could indicate malignancy such as intra-abdominal lymphoma, although infectious etiologies should be ruled out first.

Previously, on day 9 of symptoms, the patient presented to an ED at another institution. Laboratory evaluation at that time demonstrated an elevated aspartate aminotransferase (AST) level of 229 IU/L (reference, 0-40 IU/L) and alanine aminotransferase (ALT) level of 60 IU/L (reference, 0-32 IU/L) with normal alkaline phosphatase and bilirubin levels, proteinuria to 3+ (normal, negative/trace), ketonuria to 2+ (normal, negative), and hematuria to 2+ (normal, negative). Complete blood count and electrolytes were normal. Computed tomography (CT) scans of the chest, abdomen, and pelvis with intravenous contrast were normal and without evidence of organomegaly.

AST and ALT elevations often indicate hepatocellular damage, although the normal bilirubin levels suggest normal hepatic function. Because CT may miss extrahepatic biliary pathology, a right upper quadrant ultrasound should be obtained to better evaluate patency of the biliary system and hepatic echotexture. Coagulation studies and viral hepatitis serology should be obtained. The disproportionate elevation of AST versus ALT can suggest alcohol use or nonhepatic etiologies such as myositis. Acute viral hepatitis is less likely given there is only mild to moderate elevation in aminotransferase levels. However, the remaining infectious etiologies can have this level of elevation and should still be considered.

Enteritis and IBD are still considerations despite the normal CT results. Transient asymptomatic hematuria or proteinuria can be seen in multiple conditions, particularly proteinuria with febrile illnesses. Urine microscopy to evaluate for casts could indicate a glomerular origin of the hematuria. First morning urine protein-to-creatinine ratio would help quantify the degree of proteinuria. Serum creatinine level should be measured to determine whether there is any renal dysfunction.

While early imaging can be falsely negative, the unremarkable chest CT makes pneumonia and active pulmonary tuberculosis less likely.

Vital signs during this presentation were: temperature, 39.7 °C; heart rate, 126 beats per minute; blood pressure, 109/64 mm Hg; respiratory rate, 20 breaths per minute; and oxygen saturation, 98% on room air. She was ill-appearing, with diffuse abdominal tenderness without peritoneal signs. Other than her tachycardia, findings from her cardiopulmonary, neurologic, and skin exams were normal.

Laboratory testing revealed a white blood cell count of 4,300/µL (reference range, 4,500-13,000/µL), a hemoglobin level of 10.9 g/dL (reference range, 11.7-15.7 g/dL) with a mean corpuscular volume of 77 fL (reference range, 80-96 fL) and reticulocyte percentage of 0.5% (reference range, 0.5%-1.5%), and a platelet count of 59,000/µL (reference range, 135,000-466,000/µL). Her prothrombin time was 13.5 seconds (reference range, 9.6-11.6 seconds) with an international normalized ratio of 1.3 (reference range, 0.8-1.1), erythrocyte sedimentation rate of 46 mm/h (reference range, 0-20 mm/h), C-reactive protein level of 7.49 mg/dL (reference range, <0.3 mg/dL), and AST level of 194 units/L (reference range, 9-35 units/L). ALT, total and direct bilirubin, lipase, electrolytes, and creatinine levels were normal. An abdominal x-ray showed scattered air-fluid levels in a nonobstructed pattern.

Her mildly elevated prothrombin time and international normalized ratio suggest a coagulopathy involving either her extrinsic or common coagulation pathway, with disseminated intravascular coagulation (DIC) being most likely given her new thrombocytopenia and anemia. Hemolytic uremic syndrome and thrombotic thrombocytopenic purpura should be considered but would not cause coagulopathy. A peripheral smear to evaluate for schistocytes associated with microangiopathic hemolysis and serum fibrinogen to distinguish between DIC (low) and thrombocytopenic purpura or hemolytic uremic syndrome (normal or elevated) should be obtained. A thick and thin smear for malaria should also be performed.

Her new pancytopenia suggests bone marrow suppression or infiltration with or without a concomitant consumptive process such as sepsis with resulting DIC. Given her clinical picture, marrow infiltrative processes might include tuberculosis or malignancy, and marrow suppression may be caused by HIV or other viral infection. If she is found to have HIV, disseminated fungal or mycobacterial infections would become more likely. She now has an isolated elevated AST level, which could be secondary to hemolysis rather than hepatocyte damage. Findings from her abdominal exam are nonfocal; this is consistent with her x-ray findings, which reflect possible enteritis or colitis.

The most likely diagnosis currently is an infectious enteritis with resulting hematologic and hepatic abnormalities. Given her recent emigration from Kenya, typhoid fever and cholera are both possible, although cholera typically does not present with prolonged fever or severe abdominal pain. The severity and duration of her illness, and the abnormalities of her laboratory findings, warrant empiric therapy with ceftriaxone to treat possible severe Salmonella enterica infection while awaiting blood and stool cultures.

The patient was admitted to the hospital and her symptoms continued. Results of serum HIV 1 and 2 polymerase chain reactions, herpes simplex virus 1 and 2 polymerase chain reactions, three malaria smears, human T-lymphotropic virus serologies, Toxoplasma serology, Bartonella serology, a stool culture, and multiple large volume blood cultures were negative. Serologic testing for hepatitis A, B, and C, Epstein-Barr virus, cytomegalovirus, and dengue virus were negative for acute infection. Results of an interferon-gamma release assay were indeterminate; results of purified protein derivative (PPD) and Candida antigen control testing were both negative. Ceruloplasmin and α1-antitrypsin levels were normal. An abdominal ultrasound showed central intrahepatic biliary duct dilatation, splenomegaly, and sluggish portal venous flow.

While central intrahepatic biliary ductal dilation could be caused by an obstructive lesion, none were seen on CT or ultrasound. Her normal alkaline phosphatase and bilirbuin levels also suggest functional patency of the biliary system. The thrombocytopenia, splenomegaly, and sluggish portal venous flow suggest possible portal hypertension, though no cirrhotic changes were noted on the ultrasound or abdominal CT. Her negative PPD and Candida antigen control results may suggest underlying immune dysregulation or suppression, though anergy could be secondary to sepsis.

Given her negative initial infectious evaluation, other etiologies such as atypical infections, rheumatologic disorders, and malignancies warrant consideration. She has no murmur; however, subacute bacterial endocarditis with a fastidious organism is possible, which could be investigated with a transthoracic echocardiogram. Other tests to consider include blood cultures for fungi and atypical mycobacterial species, and serology for Coxiella burnetii, chikungunya virus, and yellow fever. Rheumatologic conditions such as systemic lupus erythematosus, hemophagocytic lymphohistiocytosis (HLH), or adult Still’s disease should be considered. Complement levels and an antinuclear antibody panel, including those for dsDNA and Smith antigen, should be performed to evaluate for systemic lupus erythematosus. Serum ferritin, fibrinogen, and triglyceride levels should be measured to evaluate for HLH. Hematologic malignancy is also a consideration, particularly given her pancytopenia. Multicentric Castleman disease can cause prolonged fevers, pancytopenia, and elevated inflammatory markers, but is less likely without lymphadenopathy. A peripheral blood smear should be sent, and a bone marrow biopsy may be needed.

Empiric ciprofloxacin was initiated; however, the patient continued to have fevers up to 39.9 °C, abdominal pain, and myalgia. Ferritin level was over 3,000 ng/mL (reference range, 8-255 ng/mL), and a soluble interleukin-2 (IL-2) receptor level was 1,188 units/mL (reference range, 45-1,105 units/mL). Triglycerides were normal.

The elevated ferritin and soluble IL-2 levels raise concern for HLH. Hyperferritinemia is relatively nonspecific because extremely elevated ferritin can be seen with other conditions, such as renal failure, hepatocellular injury, infection, rheumatologic conditions, and hematologic malignancy. Soluble IL-2 receptor elevation is more specific for HLH than ferritin or triglycerides, but alone does not make the diagnosis because it can be elevated in other rheumatologic disorders and malignancy. The HLH-2004 criteria are commonly used and require either molecular diagnostic testing or meeting at least five out of eight clinical and lab criteria to make the diagnosis. Our patient currently meets three criteria (fever, splenomegaly, and elevated ferritin). Elevated soluble IL-2 is part of the HLH-2004 criteria, but her level of elevation does not meet the required threshold (≥2,400 units/mL). Her cytopenias have also not quite met the HLH-2004 thresholds (two of the following three: hemoglobin <9 g/dL, platelets <100,000/µL, and/or absolute neutrophil count <1,000/µL). Elevated aminotransferase levels and DIC are not part of the HLH-2004 criteria but are often seen with HLH.

Evaluation for an underlying infectious, rheumatologic, or malignant trigger should continue as previously discussed. If this patient does have HLH, it is most likely secondary to an infection, autoimmune disease, or malignancy rather than genetic HLH. HLH has a high mortality rate, but before beginning treatment with immunosuppressive agents, a peripheral smear and a bone marrow biopsy should be performed to evaluate for hematologic malignancy or signs of hemophagocytosis.

Empiric ciprofloxacin covers most bacterial etiologies of diarrhea, including those previously mentioned such as cholera and most strains of S enterica. Her symptoms and laboratory findings (including cytopenias, elevated aminotransferases, and coagulopathy) could suggest enteric fever due to S enterica serovar Typhi, which is endemic in Kenya. Results of blood and stool cultures, though negative, are relatively insensitive for this organism, particularly this far into the illness course. A bone marrow biopsy may also help with diagnosis of occult typhoid fever because marrow culture can be more sensitive than blood or stool culture.

A bone marrow aspiration revealed hemophagocytic histiocytes, no malignant cells, and negative bacterial (including anaerobic), fungal, and acid-fast bacilli cultures. Considering the high mortality rate of untreated HLH/macrophage activation syndrome (MAS), empiric glucocorticoid administration was considered. However, this was withheld due to concern for ongoing undetected infection given her persistent fever and systemic symptoms.

There should still be high suspicion for HLH. Further evaluation for other laboratory manifestations of HLH such as fibrinogen and natural killer cell activity should be considered, as well as repeating her complete blood count to see if her cytopenias have progressed. Her marrow shows no evidence of hematologic malignancy, so other triggers of possible HLH should be sought out by continuing the workup. Consulting specialists from rheumatology and infectious disease may help clarify possible underlying diagnoses and the best management plan. If she continues to have organ damage or clinically worsens, it may be prudent to empirically broaden her antibiotic coverage and begin antifungal agents while starting glucocorticoid therapy for suspected HLH.

A stool molecular screen from admission was returned positive for S enterica serovar Typhi. Ciprofloxacin was discontinued and ceftriaxone was started out of concern for antibiotic resistance. On hospital day 14, the patient’s brother presented to the ED with fever. His blood and stool cultures were positive for S enterica serovar Typhi with intermediate sensitivity to ciprofloxacin and sensitivity to ceftriaxone. With continued treatment with ceftriaxone, the patient improved significantly. Following discharge, she remained afebrile and asymptomatic. During outpatient follow up, a repeat PPD was positive and she was diagnosed with and treated for latent tuberculosis.

COMMENTARY

The evaluation of a patient who has recently emigrated from a foreign nation requires a broad differential diagnosis and a keen awareness of the clinical conditions present in the patient’s country of origin. This often involves knowledge of diseases infrequently encountered in daily practice, as well as awareness of the nuances of rare presentations and possible complications. When the presentation is not classic for a relevant infectious disease and clinical conditions from other diagnostic classes are considered, the evaluation and management of the patient is particularly challenging.

Typhoid fever is a severe systemic illness caused by the organism S enterica serovar Typhi. The organism is ingested, penetrates the small intestinal epithelium, enters the lymphoid tissue, and disseminates via the lymphatic and hematogenous routes. Onset of symptoms typically occurs 5 to 21 days after ingestion of contaminated food or water. Clinical features include fever, chills, relative bradycardia (pulse-temperature dissociation), abdominal pain, rose spots (salmon-colored macules) on the trunk and abdomen, and hepatosplenomegaly. Diarrhea is not a typical symptom of patients with typhoid fever, which can lead to a delayed or missed diagnosis. Life-threatening complications can be seen, including gastrointestinal bleeding, intestinal perforation, and meningitis.1 Typhoid fever is most prevalent in impoverished areas with poor access to sanitation. Regions with the highest incidence include south-central Asia, southeast Asia, and southern Africa.2-4 Approximately 200 to 300 cases are reported in the United States each year.5

Classically, the diagnosis is made by means of clinical symptoms and a positive culture from a sterile site. A recent study of 529 patients found that 61% had positive blood cultures and 96% had positive bone marrow cultures.6 Our patient’s diagnosis was significantly delayed by multiple negative cultures and failure to improve on first-line antibiotics, which initially suggested that the S enterica serovar Typhi stool molecular screen likely represented carriage caused by colonization. Chronic S enterica serovar Typhi carriage is defined as excretion of the organism in stool or urine 1 year or longer after acute infection. Rates of carriage range from 1% to 6%, and up to 25% of carriers have no history of typhoid fever.1,7,8 Carriage is more common in females and in those with biliary tract abnormalities.9,10

Once a presumptive diagnosis is made, antibiotic choice remains a challenge. Resistance to fluoroquinolones, the preferred drug for multidrug-resistant typhoid fever, is growing but remains rare, at approximately 5%.11,12 Ceftriaxone and azithromycin have been used successfully in areas with high resistance.13 Given the patient’s slow response to therapy even after transitioning from ciprofloxacin to ceftriaxone, her brother’s presentation and obtaining the antibiotic sensitivities for his organism were critical to confirming that our diagnosis and management decisions were correct.

One strongly considered diagnosis was HLH/MAS. MAS is an aggressive syndrome of excessive inflammation and tissue destruction caused by inappropriate immune system activation. It belongs to a group of histiocytic disorders collectively known as HLH. Aside from primary (genetic) forms, secondary forms exist that can be triggered by malignancy, infection, or rheumatologic disorders. In infection-associated HLH/MAS, viral infections are a common trigger, with Epstein-Barr virus being the most common. Association with bacterial infections, including tuberculosis and typhoid fever, has also been reported.14 Prompt therapy, often with immunosuppressive agents such as glucocorticoids, is essential for survival because there is a reported mortality rate of up to 50% when untreated.15 When infection-induced HLH/MAS occurs, treatment of the underlying infection is critical.14,15 The greatest barrier to a favorable outcome from HLH/MAS is often a delay in diagnosis because the rarity of this disease, the variable clinical presentation, and the lack of specificity of the clinical and laboratory findings make a conclusive diagnosis challenging.

In the presented case, diagnostic uncertainty challenged the decision to administer systemic glucocorticoids. Glucocorticoids conferred a risk of harm for multiple diagnoses that remained on the differential, including malignancy and infection. Her diagnostic evaluation made malignancy less likely, but because testing was unable to rule out tuberculosis as either the underlying cause or coinfection, the team opted to defer initiating glucocorticoids and instead closely monitor for a worsening inflammatory response. Following appropriate treatment of her systemic infection, her PPD was repeated and became positive. The negative PPD and Candida control obtained during her hospitalization were, therefore, likely caused by anergy in the setting of overwhelming systemic illness. Initiation of glucocorticoids prematurely in this case could have led to further harm because immunosuppression may have led to reactivation of latent tuberculosis or exacerbation of illness from an alternative but then undiagnosed infection.

The patient’s ultimate unifying diagnosis was typhoid fever; however, there are mixed expert opinions as to whether the systemic immune activation was significant enough to merit the diagnosis of infection-induced secondary HLH/MAS. Despite the high morbidity and mortality that can accompany HLH/MAS, it has been reported that a significant proportion of cases of secondary HLH/MAS can be managed effectively with treatment of the underlying etiology; this may have been the case for our patient.14,15 The clinicians in this case were caught between diagnoses, unable to safely reach either one—much like a baseball player stranded between bases. Fortunately for this patient, the diagnosis ultimately emerged after a careful and thorough workup, assisted by the more straightforward diagnosis of her brother with the same disease.

KEY TEACHING POINTS

  • Salmonella enterica serovar Typhi has a high false-negative rate in blood and stool cultures; therefore, clinical suspicion should remain high in the setting of a high pre-test probability.
  • Fluoroquinolones are traditionally first-line therapy for typhoid fever, but the use of ceftriaxone and azithromycin is increasing because of rising fluoroquinolone resistance.
  • Hemophagocytic lymphohistiocytosis/macrophage activation syndrome is characterized by excessive inflammation and tissue destruction caused by inappropriate immune system activation. This syndrome can be fatal without appropriate immunosuppressive therapy; however, glucocorticoid administration must be pursued with caution when infection and malignancy are on the differential diagnosis.

A 19-year-old woman presented to the emergency department (ED) with a 14-day history of progressive fevers, night sweats, abdominal pain, nonbloody and nonbilious vomiting, diarrhea, cough, and myalgia. The fever occurred daily with no noted temporal pattern, and she had no significant weight loss. The abdominal pain was diffuse and exacerbated by eating. She experienced multiple sporadic episodes of vomiting and diarrhea daily. She denied any rash or arthralgia.

She had no known medical history and took no medications. Family history was negative for autoinflammatory and autoimmune conditions. She had emigrated from Kenya to the United States 28 days ago. Her immunization status was unknown.

This patient has prolonged fevers and evidence of multisystem involvement. The most likely etiologic categories are infectious, inflammatory, rheumatologic, and neoplastic. For febrile patients who have recently emigrated to or travelled outside of the United States, it is important to consider common infections, as well as those endemic to the nation of exposure, which in this case includes malaria, typhoid fever, tuberculosis, cholera, acute viral hepatitis, chikungunya fever, dengue fever, yellow fever, and rickettsial disease. All of these, other than tuberculosis, commonly present with fever, vomiting, diarrhea, and myalgia. She may also have bacterial pneumonia or influenza given her fever and cough, although the chronicity and persistence of symptoms would be atypical. Acute infectious gastroenteritis is a common cause of fever, vomiting, and diarrhea. Most cases resolve in 7 to 10 days, so the duration raises suspicion for a nonviral etiology or an immunocompromised state.

Inflammatory causes could include the first presentation of inflammatory bowel disease (IBD), particularly if the patient develops weight loss or eye, skin, or joint manifestations. The lack of rash or arthralgia makes rheumatologic conditions less likely. Prolonged fevers and night sweats could indicate malignancy such as intra-abdominal lymphoma, although infectious etiologies should be ruled out first.

Previously, on day 9 of symptoms, the patient presented to an ED at another institution. Laboratory evaluation at that time demonstrated an elevated aspartate aminotransferase (AST) level of 229 IU/L (reference, 0-40 IU/L) and alanine aminotransferase (ALT) level of 60 IU/L (reference, 0-32 IU/L) with normal alkaline phosphatase and bilirubin levels, proteinuria to 3+ (normal, negative/trace), ketonuria to 2+ (normal, negative), and hematuria to 2+ (normal, negative). Complete blood count and electrolytes were normal. Computed tomography (CT) scans of the chest, abdomen, and pelvis with intravenous contrast were normal and without evidence of organomegaly.

AST and ALT elevations often indicate hepatocellular damage, although the normal bilirubin levels suggest normal hepatic function. Because CT may miss extrahepatic biliary pathology, a right upper quadrant ultrasound should be obtained to better evaluate patency of the biliary system and hepatic echotexture. Coagulation studies and viral hepatitis serology should be obtained. The disproportionate elevation of AST versus ALT can suggest alcohol use or nonhepatic etiologies such as myositis. Acute viral hepatitis is less likely given there is only mild to moderate elevation in aminotransferase levels. However, the remaining infectious etiologies can have this level of elevation and should still be considered.

Enteritis and IBD are still considerations despite the normal CT results. Transient asymptomatic hematuria or proteinuria can be seen in multiple conditions, particularly proteinuria with febrile illnesses. Urine microscopy to evaluate for casts could indicate a glomerular origin of the hematuria. First morning urine protein-to-creatinine ratio would help quantify the degree of proteinuria. Serum creatinine level should be measured to determine whether there is any renal dysfunction.

While early imaging can be falsely negative, the unremarkable chest CT makes pneumonia and active pulmonary tuberculosis less likely.

Vital signs during this presentation were: temperature, 39.7 °C; heart rate, 126 beats per minute; blood pressure, 109/64 mm Hg; respiratory rate, 20 breaths per minute; and oxygen saturation, 98% on room air. She was ill-appearing, with diffuse abdominal tenderness without peritoneal signs. Other than her tachycardia, findings from her cardiopulmonary, neurologic, and skin exams were normal.

Laboratory testing revealed a white blood cell count of 4,300/µL (reference range, 4,500-13,000/µL), a hemoglobin level of 10.9 g/dL (reference range, 11.7-15.7 g/dL) with a mean corpuscular volume of 77 fL (reference range, 80-96 fL) and reticulocyte percentage of 0.5% (reference range, 0.5%-1.5%), and a platelet count of 59,000/µL (reference range, 135,000-466,000/µL). Her prothrombin time was 13.5 seconds (reference range, 9.6-11.6 seconds) with an international normalized ratio of 1.3 (reference range, 0.8-1.1), erythrocyte sedimentation rate of 46 mm/h (reference range, 0-20 mm/h), C-reactive protein level of 7.49 mg/dL (reference range, <0.3 mg/dL), and AST level of 194 units/L (reference range, 9-35 units/L). ALT, total and direct bilirubin, lipase, electrolytes, and creatinine levels were normal. An abdominal x-ray showed scattered air-fluid levels in a nonobstructed pattern.

Her mildly elevated prothrombin time and international normalized ratio suggest a coagulopathy involving either her extrinsic or common coagulation pathway, with disseminated intravascular coagulation (DIC) being most likely given her new thrombocytopenia and anemia. Hemolytic uremic syndrome and thrombotic thrombocytopenic purpura should be considered but would not cause coagulopathy. A peripheral smear to evaluate for schistocytes associated with microangiopathic hemolysis and serum fibrinogen to distinguish between DIC (low) and thrombocytopenic purpura or hemolytic uremic syndrome (normal or elevated) should be obtained. A thick and thin smear for malaria should also be performed.

Her new pancytopenia suggests bone marrow suppression or infiltration with or without a concomitant consumptive process such as sepsis with resulting DIC. Given her clinical picture, marrow infiltrative processes might include tuberculosis or malignancy, and marrow suppression may be caused by HIV or other viral infection. If she is found to have HIV, disseminated fungal or mycobacterial infections would become more likely. She now has an isolated elevated AST level, which could be secondary to hemolysis rather than hepatocyte damage. Findings from her abdominal exam are nonfocal; this is consistent with her x-ray findings, which reflect possible enteritis or colitis.

The most likely diagnosis currently is an infectious enteritis with resulting hematologic and hepatic abnormalities. Given her recent emigration from Kenya, typhoid fever and cholera are both possible, although cholera typically does not present with prolonged fever or severe abdominal pain. The severity and duration of her illness, and the abnormalities of her laboratory findings, warrant empiric therapy with ceftriaxone to treat possible severe Salmonella enterica infection while awaiting blood and stool cultures.

The patient was admitted to the hospital and her symptoms continued. Results of serum HIV 1 and 2 polymerase chain reactions, herpes simplex virus 1 and 2 polymerase chain reactions, three malaria smears, human T-lymphotropic virus serologies, Toxoplasma serology, Bartonella serology, a stool culture, and multiple large volume blood cultures were negative. Serologic testing for hepatitis A, B, and C, Epstein-Barr virus, cytomegalovirus, and dengue virus were negative for acute infection. Results of an interferon-gamma release assay were indeterminate; results of purified protein derivative (PPD) and Candida antigen control testing were both negative. Ceruloplasmin and α1-antitrypsin levels were normal. An abdominal ultrasound showed central intrahepatic biliary duct dilatation, splenomegaly, and sluggish portal venous flow.

While central intrahepatic biliary ductal dilation could be caused by an obstructive lesion, none were seen on CT or ultrasound. Her normal alkaline phosphatase and bilirbuin levels also suggest functional patency of the biliary system. The thrombocytopenia, splenomegaly, and sluggish portal venous flow suggest possible portal hypertension, though no cirrhotic changes were noted on the ultrasound or abdominal CT. Her negative PPD and Candida antigen control results may suggest underlying immune dysregulation or suppression, though anergy could be secondary to sepsis.

Given her negative initial infectious evaluation, other etiologies such as atypical infections, rheumatologic disorders, and malignancies warrant consideration. She has no murmur; however, subacute bacterial endocarditis with a fastidious organism is possible, which could be investigated with a transthoracic echocardiogram. Other tests to consider include blood cultures for fungi and atypical mycobacterial species, and serology for Coxiella burnetii, chikungunya virus, and yellow fever. Rheumatologic conditions such as systemic lupus erythematosus, hemophagocytic lymphohistiocytosis (HLH), or adult Still’s disease should be considered. Complement levels and an antinuclear antibody panel, including those for dsDNA and Smith antigen, should be performed to evaluate for systemic lupus erythematosus. Serum ferritin, fibrinogen, and triglyceride levels should be measured to evaluate for HLH. Hematologic malignancy is also a consideration, particularly given her pancytopenia. Multicentric Castleman disease can cause prolonged fevers, pancytopenia, and elevated inflammatory markers, but is less likely without lymphadenopathy. A peripheral blood smear should be sent, and a bone marrow biopsy may be needed.

Empiric ciprofloxacin was initiated; however, the patient continued to have fevers up to 39.9 °C, abdominal pain, and myalgia. Ferritin level was over 3,000 ng/mL (reference range, 8-255 ng/mL), and a soluble interleukin-2 (IL-2) receptor level was 1,188 units/mL (reference range, 45-1,105 units/mL). Triglycerides were normal.

The elevated ferritin and soluble IL-2 levels raise concern for HLH. Hyperferritinemia is relatively nonspecific because extremely elevated ferritin can be seen with other conditions, such as renal failure, hepatocellular injury, infection, rheumatologic conditions, and hematologic malignancy. Soluble IL-2 receptor elevation is more specific for HLH than ferritin or triglycerides, but alone does not make the diagnosis because it can be elevated in other rheumatologic disorders and malignancy. The HLH-2004 criteria are commonly used and require either molecular diagnostic testing or meeting at least five out of eight clinical and lab criteria to make the diagnosis. Our patient currently meets three criteria (fever, splenomegaly, and elevated ferritin). Elevated soluble IL-2 is part of the HLH-2004 criteria, but her level of elevation does not meet the required threshold (≥2,400 units/mL). Her cytopenias have also not quite met the HLH-2004 thresholds (two of the following three: hemoglobin <9 g/dL, platelets <100,000/µL, and/or absolute neutrophil count <1,000/µL). Elevated aminotransferase levels and DIC are not part of the HLH-2004 criteria but are often seen with HLH.

Evaluation for an underlying infectious, rheumatologic, or malignant trigger should continue as previously discussed. If this patient does have HLH, it is most likely secondary to an infection, autoimmune disease, or malignancy rather than genetic HLH. HLH has a high mortality rate, but before beginning treatment with immunosuppressive agents, a peripheral smear and a bone marrow biopsy should be performed to evaluate for hematologic malignancy or signs of hemophagocytosis.

Empiric ciprofloxacin covers most bacterial etiologies of diarrhea, including those previously mentioned such as cholera and most strains of S enterica. Her symptoms and laboratory findings (including cytopenias, elevated aminotransferases, and coagulopathy) could suggest enteric fever due to S enterica serovar Typhi, which is endemic in Kenya. Results of blood and stool cultures, though negative, are relatively insensitive for this organism, particularly this far into the illness course. A bone marrow biopsy may also help with diagnosis of occult typhoid fever because marrow culture can be more sensitive than blood or stool culture.

A bone marrow aspiration revealed hemophagocytic histiocytes, no malignant cells, and negative bacterial (including anaerobic), fungal, and acid-fast bacilli cultures. Considering the high mortality rate of untreated HLH/macrophage activation syndrome (MAS), empiric glucocorticoid administration was considered. However, this was withheld due to concern for ongoing undetected infection given her persistent fever and systemic symptoms.

There should still be high suspicion for HLH. Further evaluation for other laboratory manifestations of HLH such as fibrinogen and natural killer cell activity should be considered, as well as repeating her complete blood count to see if her cytopenias have progressed. Her marrow shows no evidence of hematologic malignancy, so other triggers of possible HLH should be sought out by continuing the workup. Consulting specialists from rheumatology and infectious disease may help clarify possible underlying diagnoses and the best management plan. If she continues to have organ damage or clinically worsens, it may be prudent to empirically broaden her antibiotic coverage and begin antifungal agents while starting glucocorticoid therapy for suspected HLH.

A stool molecular screen from admission was returned positive for S enterica serovar Typhi. Ciprofloxacin was discontinued and ceftriaxone was started out of concern for antibiotic resistance. On hospital day 14, the patient’s brother presented to the ED with fever. His blood and stool cultures were positive for S enterica serovar Typhi with intermediate sensitivity to ciprofloxacin and sensitivity to ceftriaxone. With continued treatment with ceftriaxone, the patient improved significantly. Following discharge, she remained afebrile and asymptomatic. During outpatient follow up, a repeat PPD was positive and she was diagnosed with and treated for latent tuberculosis.

COMMENTARY

The evaluation of a patient who has recently emigrated from a foreign nation requires a broad differential diagnosis and a keen awareness of the clinical conditions present in the patient’s country of origin. This often involves knowledge of diseases infrequently encountered in daily practice, as well as awareness of the nuances of rare presentations and possible complications. When the presentation is not classic for a relevant infectious disease and clinical conditions from other diagnostic classes are considered, the evaluation and management of the patient is particularly challenging.

Typhoid fever is a severe systemic illness caused by the organism S enterica serovar Typhi. The organism is ingested, penetrates the small intestinal epithelium, enters the lymphoid tissue, and disseminates via the lymphatic and hematogenous routes. Onset of symptoms typically occurs 5 to 21 days after ingestion of contaminated food or water. Clinical features include fever, chills, relative bradycardia (pulse-temperature dissociation), abdominal pain, rose spots (salmon-colored macules) on the trunk and abdomen, and hepatosplenomegaly. Diarrhea is not a typical symptom of patients with typhoid fever, which can lead to a delayed or missed diagnosis. Life-threatening complications can be seen, including gastrointestinal bleeding, intestinal perforation, and meningitis.1 Typhoid fever is most prevalent in impoverished areas with poor access to sanitation. Regions with the highest incidence include south-central Asia, southeast Asia, and southern Africa.2-4 Approximately 200 to 300 cases are reported in the United States each year.5

Classically, the diagnosis is made by means of clinical symptoms and a positive culture from a sterile site. A recent study of 529 patients found that 61% had positive blood cultures and 96% had positive bone marrow cultures.6 Our patient’s diagnosis was significantly delayed by multiple negative cultures and failure to improve on first-line antibiotics, which initially suggested that the S enterica serovar Typhi stool molecular screen likely represented carriage caused by colonization. Chronic S enterica serovar Typhi carriage is defined as excretion of the organism in stool or urine 1 year or longer after acute infection. Rates of carriage range from 1% to 6%, and up to 25% of carriers have no history of typhoid fever.1,7,8 Carriage is more common in females and in those with biliary tract abnormalities.9,10

Once a presumptive diagnosis is made, antibiotic choice remains a challenge. Resistance to fluoroquinolones, the preferred drug for multidrug-resistant typhoid fever, is growing but remains rare, at approximately 5%.11,12 Ceftriaxone and azithromycin have been used successfully in areas with high resistance.13 Given the patient’s slow response to therapy even after transitioning from ciprofloxacin to ceftriaxone, her brother’s presentation and obtaining the antibiotic sensitivities for his organism were critical to confirming that our diagnosis and management decisions were correct.

One strongly considered diagnosis was HLH/MAS. MAS is an aggressive syndrome of excessive inflammation and tissue destruction caused by inappropriate immune system activation. It belongs to a group of histiocytic disorders collectively known as HLH. Aside from primary (genetic) forms, secondary forms exist that can be triggered by malignancy, infection, or rheumatologic disorders. In infection-associated HLH/MAS, viral infections are a common trigger, with Epstein-Barr virus being the most common. Association with bacterial infections, including tuberculosis and typhoid fever, has also been reported.14 Prompt therapy, often with immunosuppressive agents such as glucocorticoids, is essential for survival because there is a reported mortality rate of up to 50% when untreated.15 When infection-induced HLH/MAS occurs, treatment of the underlying infection is critical.14,15 The greatest barrier to a favorable outcome from HLH/MAS is often a delay in diagnosis because the rarity of this disease, the variable clinical presentation, and the lack of specificity of the clinical and laboratory findings make a conclusive diagnosis challenging.

In the presented case, diagnostic uncertainty challenged the decision to administer systemic glucocorticoids. Glucocorticoids conferred a risk of harm for multiple diagnoses that remained on the differential, including malignancy and infection. Her diagnostic evaluation made malignancy less likely, but because testing was unable to rule out tuberculosis as either the underlying cause or coinfection, the team opted to defer initiating glucocorticoids and instead closely monitor for a worsening inflammatory response. Following appropriate treatment of her systemic infection, her PPD was repeated and became positive. The negative PPD and Candida control obtained during her hospitalization were, therefore, likely caused by anergy in the setting of overwhelming systemic illness. Initiation of glucocorticoids prematurely in this case could have led to further harm because immunosuppression may have led to reactivation of latent tuberculosis or exacerbation of illness from an alternative but then undiagnosed infection.

The patient’s ultimate unifying diagnosis was typhoid fever; however, there are mixed expert opinions as to whether the systemic immune activation was significant enough to merit the diagnosis of infection-induced secondary HLH/MAS. Despite the high morbidity and mortality that can accompany HLH/MAS, it has been reported that a significant proportion of cases of secondary HLH/MAS can be managed effectively with treatment of the underlying etiology; this may have been the case for our patient.14,15 The clinicians in this case were caught between diagnoses, unable to safely reach either one—much like a baseball player stranded between bases. Fortunately for this patient, the diagnosis ultimately emerged after a careful and thorough workup, assisted by the more straightforward diagnosis of her brother with the same disease.

KEY TEACHING POINTS

  • Salmonella enterica serovar Typhi has a high false-negative rate in blood and stool cultures; therefore, clinical suspicion should remain high in the setting of a high pre-test probability.
  • Fluoroquinolones are traditionally first-line therapy for typhoid fever, but the use of ceftriaxone and azithromycin is increasing because of rising fluoroquinolone resistance.
  • Hemophagocytic lymphohistiocytosis/macrophage activation syndrome is characterized by excessive inflammation and tissue destruction caused by inappropriate immune system activation. This syndrome can be fatal without appropriate immunosuppressive therapy; however, glucocorticoid administration must be pursued with caution when infection and malignancy are on the differential diagnosis.
References

1. Parry CM, Hien TT, Dougan G, et al. Typhoid fever. N Engl J Med. 2002;347(22):1770-1782. https://doi.org/10.1056/nejmra020201
2. Crump JA, Luby SP, Mintz ED. The global burden of typhoid fever. Bull World Health Organ. 2004;82(5):346-353.
3. Buckle GC, Walker CL, Black RE. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J Glob Health. 2012;2(1):010401. https://doi.org/10.7189/jogh.02.010401
4. Mogasale V, Maskery B, Ochiai RL, et al. Burden of typhoid fever in low-income and middle-income countries: a systematic, literature-based update with risk-factor adjustment. Lancet Glob Health. 2014;2(10):e570-e580. https://doi.org/10.1016/s2214-109x(14)70301-8
5. Lynch MF, Blanton EM, Bulens S, et al. Typhoid fever in the United States, 1999-2006. JAMA. 2009;302(8):859-865. https://doi.org/10.1001/jama.2009.1229
6. Mogasale V, Ramani E, Mogasale VV, Park J. What proportion of Salmonella typhi cases are detected by blood culture? a systematic literature review. Ann Clin Microbiol Antimicrob. 2016;15(1):32. https://doi.org/10.1186/s12941-016-0147-z
7. Merselis JG Jr, Kaye D, Connolly CS, Hook EW. Quantitative bacteriology of the Typhoid carrier state. Am J Trop Med Hyg. 1964;13:425-429. https://doi.org/10.4269/ajtmh.1964.13.425
8. Lanata CF, Levine MM, Ristori C, et al. Vi serology in detection of chronic Salmonella typhi carriers in an endemic area. Lancet. 1983;2(8347):441-443. https://doi.org/10.1016/s0140-6736(83)90401-4
9. Lai CW, Chan RC, Cheng AF, Sung JY, Leung JW. Common bile duct stones: a cause of chronic salmonellosis. Am J Gastroenterol. 1992;87(9):1198-1199.
10. Hofmann E, Chianale J, Rollán A, Pereira J, Ferrecio C, Sotomayor V. Blood group antigen secretion and gallstone disease in the Salmonella typhi chronic carrier state. J Infect Dis. 1993;167(4):993-994. https://doi.org/10.1093/infdis/167.4.993
11. Steel AD, Hay Burgess DC, Diaz Z, Carey ME, Zaidi AKM. Challenges and opportunities for typhoid fever control: a call for coordinated action. Clin Infect Dis. 2016;62 (Suppl 1):S4-S8. https://doi.org/10.1093/cid/civ976
12. Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, et al. Genomic signature of multidrug resistant Salmonella enterica serovar Typhi isolates related to a massive outbreak in Zambia between 2010 and 2012. J Clin Microbiol. 2015;53(1):262-272. https://doi.org/10.1128/jcm.02026-14
13. Crump JA, Sjölund-Karlsson M, Gordon MA, Parry CM. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of Salmonella infections. Clin Microbiol Rev. 2015;28(4):901-936. https://doi.org/10.1128/cmr.00002-15
14. Rouphael NG, Talati NJ, Vaughan C, Cunningham K, Moreira R, Gould C. Infections associated with haemophagocytic syndrome. Lancet Infect Dis. 2007;7(12):814-822. https://doi.org/10.1016/s1473-3099(07)70290-6
15. Fisman DN. Hemophagocytic syndromes and infection. Emerg Infect Dis. 2000;6(6):601-608. https://doi.org/10.3201/eid0606.000608

References

1. Parry CM, Hien TT, Dougan G, et al. Typhoid fever. N Engl J Med. 2002;347(22):1770-1782. https://doi.org/10.1056/nejmra020201
2. Crump JA, Luby SP, Mintz ED. The global burden of typhoid fever. Bull World Health Organ. 2004;82(5):346-353.
3. Buckle GC, Walker CL, Black RE. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J Glob Health. 2012;2(1):010401. https://doi.org/10.7189/jogh.02.010401
4. Mogasale V, Maskery B, Ochiai RL, et al. Burden of typhoid fever in low-income and middle-income countries: a systematic, literature-based update with risk-factor adjustment. Lancet Glob Health. 2014;2(10):e570-e580. https://doi.org/10.1016/s2214-109x(14)70301-8
5. Lynch MF, Blanton EM, Bulens S, et al. Typhoid fever in the United States, 1999-2006. JAMA. 2009;302(8):859-865. https://doi.org/10.1001/jama.2009.1229
6. Mogasale V, Ramani E, Mogasale VV, Park J. What proportion of Salmonella typhi cases are detected by blood culture? a systematic literature review. Ann Clin Microbiol Antimicrob. 2016;15(1):32. https://doi.org/10.1186/s12941-016-0147-z
7. Merselis JG Jr, Kaye D, Connolly CS, Hook EW. Quantitative bacteriology of the Typhoid carrier state. Am J Trop Med Hyg. 1964;13:425-429. https://doi.org/10.4269/ajtmh.1964.13.425
8. Lanata CF, Levine MM, Ristori C, et al. Vi serology in detection of chronic Salmonella typhi carriers in an endemic area. Lancet. 1983;2(8347):441-443. https://doi.org/10.1016/s0140-6736(83)90401-4
9. Lai CW, Chan RC, Cheng AF, Sung JY, Leung JW. Common bile duct stones: a cause of chronic salmonellosis. Am J Gastroenterol. 1992;87(9):1198-1199.
10. Hofmann E, Chianale J, Rollán A, Pereira J, Ferrecio C, Sotomayor V. Blood group antigen secretion and gallstone disease in the Salmonella typhi chronic carrier state. J Infect Dis. 1993;167(4):993-994. https://doi.org/10.1093/infdis/167.4.993
11. Steel AD, Hay Burgess DC, Diaz Z, Carey ME, Zaidi AKM. Challenges and opportunities for typhoid fever control: a call for coordinated action. Clin Infect Dis. 2016;62 (Suppl 1):S4-S8. https://doi.org/10.1093/cid/civ976
12. Hendriksen RS, Leekitcharoenphon P, Lukjancenko O, et al. Genomic signature of multidrug resistant Salmonella enterica serovar Typhi isolates related to a massive outbreak in Zambia between 2010 and 2012. J Clin Microbiol. 2015;53(1):262-272. https://doi.org/10.1128/jcm.02026-14
13. Crump JA, Sjölund-Karlsson M, Gordon MA, Parry CM. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of Salmonella infections. Clin Microbiol Rev. 2015;28(4):901-936. https://doi.org/10.1128/cmr.00002-15
14. Rouphael NG, Talati NJ, Vaughan C, Cunningham K, Moreira R, Gould C. Infections associated with haemophagocytic syndrome. Lancet Infect Dis. 2007;7(12):814-822. https://doi.org/10.1016/s1473-3099(07)70290-6
15. Fisman DN. Hemophagocytic syndromes and infection. Emerg Infect Dis. 2000;6(6):601-608. https://doi.org/10.3201/eid0606.000608

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Clinical Progress Note: Vascular Access Appropriateness Guidance for Pediatric Hospitalists

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Clinical Progress Note: Vascular Access Appropriateness Guidance for Pediatric Hospitalists

Hospitalized pediatric patients often require vascular access for necessary therapies, such as antibiotics. However, vascular access devices (VADs) are also associated with harm, ranging from insertion complications to life-threatening bloodstream infections or thrombosis.1 Pediatric hospitalists often guide VAD placement. There is a paucity of evidence to guide VAD selection based on the relative benefits and risks.2 The Michigan Appropriateness Guide for Intravenous Catheters in Pediatrics (miniMAGIC)2 offers the first set of standards. Like its adult predecessor guideline (MAGIC) published in 2015, it provides guidance on appropriate VAD selection based on current evidence and expertise from a multidisciplinary panel.2 The guideline informs device selection, device characteristics, and insertion technique for the pediatric population (term neonates to adolescents) and across a wide range of clinical indications.2 This review highlights key recommendations for pediatric hospitalists to help their decision-making.

METHODS USED IN PREPARING THE GUIDELINE

miniMAGIC was developed using the RAND/UCLA Appropriateness Method, a method proven to reduce inappropriate (ie, overused or underused) healthcare interventions.3 It combines rigorous evidence review with multidisciplinary expert opinion on real-world clinical scenarios to provide recommendations about an intervention’s appropriateness.3 This is particularly useful for clinical scenarios that lack high-quality evidence to guide decision-making. The RAND/UCLA method deems an intervention appropriate if the benefits outweigh the risks by a wide enough margin that proceeding is worthwhile, and it does not take cost into account.2 The method design consists of five phases: (1) defining the scope and key terms, (2) reviewing and synthesizing the literature, (3) selecting an expert panel, (4) developing case scenarios, and (5) conducting two rounds of appropriateness ratings by the expert panel for each clinical scenario.3 The guideline’s scope included term neonates (aged 0-30 days), infants (aged 31 days-1 year), children (aged 1-12 years), and adolescents (aged 12-18 years). Infants receiving care in the neonatal intensive care unit or special care nursery were excluded. Other specialized populations addressed based on setting or diagnosis were general hospitalized patients and patients with congenital cardiac disease, critical illness, oncologic and hematologic conditions, and long-term VAD-dependent conditions.3

A total of 133 studies or clinical practice guidelines (CPGs) met the eligibility criteria for the systematic review.4 Although the systematic review was conducted per the RAND/UCLA method using two independent reviewers who evaluated the methodologic quality, transparency, and relevancy of each article, there was no formal assessment of evidence quality. The recommendations were based primarily on observational studies and CPGs because there were few randomized controlled trials or systematic reviews on VAD selection for pediatric patients in the literature. Pediatric evidence was limited for certain scenarios or populations (eg, term neonates, midline catheters, difficult venous access, long-term VAD), so adult and/or neonatal evidence was included when applicable.

The panel included 14 pediatric clinical experts from cardiology, vascular access, critical care, hematology/oncology, emergency medicine, general surgery, hospital medicine, anesthesia, interventional radiology, pharmacology, and infectious diseases. The panel also included nonvoting panel members such as the panel facilitators, a methodologist, and a patient representative.

RESULTS OF THE CLINICAL REVIEW

We review four common clinical scenarios encountered by pediatric hospitalists and summarize key recommendations (Table).

Key Recommendations for Pediatric Hospital Medicine

Peripherally Inserted Central Catheter

Patients may require peripherally inserted central catheters (PICCs) to facilitate a longer duration of intravenous (IV) therapy, such as delivery of antibiotics, or frequent blood draws. The need for prolonged vascular access is decreasing, as studies show many infections in children previously treated with prolonged IV antibiotics can be safely and equally effectively managed with early transition to oral therapy.5-8 These studies highlight the higher rate of complications and risks associated with PICCs, including thrombosis, infection, and mechanical issues, as well as the added healthcare utilization needed to evaluate and manage the complications. PICC-associated complication rates also increase with duration.4

However, there are some clinical scenarios that still warrant prolonged therapy and/or access; PICC recommendations are summarized in the Appendix Figure. The miniMAGIC panel deemed PICC lines appropriate for any nonperipheral therapy of any length. For peripherally compatible therapy, the panel rated PICC placement as inappropriate for therapy lasting less than 8 days, regardless of patient age. PICC placement in infants, children, and adolescents was rated appropriate for therapy with a duration exceeding 14 days, but the panel was uncertain about therapy expected to last between 8 and 14 days. Recognizing the additional challenges with maintaining peripheral IV catheter access in neonates, PICCs were deemed appropriate for neonates needing peripheral therapy lasting longer than 7 days.

The panel rated PICC placement appropriate for frequent blood draws (defined as more than one time per day) for more than 7 days in neonates or infants and more than 14 days in children and adolescents. But regardless of patient age, the PICC caliber must be at least 3F.

The miniMAGIC panel found that a single lumen is appropriate in most cases, highlighting that multilumen catheters increase the risk for infection, occlusion, and venous thrombosis.4 Multilumen catheters were rated as inappropriate in the case of reserving a lumen for blood products and blood sampling. When reserving a lumen for lipids and parenteral nutrition (PN), the panel was uncertain given the lack of evidence regarding the risks/benefits of the complications associated with the infusions themselves versus those of the device. Regardless, collaboration with a pharmacist and vascular access specialist is recommended to aid in choosing the most appropriate device characteristics.

Midline Catheters

Midline catheters are inserted in a peripheral vein, but the catheter tip terminates in the proximal extremity. Compared with peripheral IV catheters, midline catheters last longer and have lower rates of phlebitis. In addition, midline catheter placement does not require sedation or fluoroscopy and has lower rates of infection compared with PICC lines.9 Although there is good evidence in adults, and multiple panelists reported success in using midline catheters in various age groups, the evidence for their safe and efficacious use in pediatrics is limited, particularly for infants. Midline catheters were rated as appropriate for peripheral therapy lasting less than 8 days in neonates and less than 15 days in children and adolescents. Use in infants was deemed uncertain based on lack of published evidence. Midline catheters were also rated as appropriate for frequent blood draws of less than 8 days in neonates and less than 15 days in adolescents, but uncertain for children and infants.

Difficult Access and Insertion Procedure

The panel rated three or more attempts for peripheral IV catheter insertion by a single clinician as inappropriate and recommended early escalation to a more experienced inserter after 0 to 2 attempts by a single provider. The goal is to preserve insertion sites and reduce patient discomfort. If a patient loses access when only 1 day of therapy remains, the provider should transition to oral or intramuscular therapy when appropriate, particularly if there are no advanced insertion staff available or after two or more attempts at re-insertion are unsuccessful. There is high-quality evidence that supports vessel visualization (primarily ultrasound) with peripheral IV catheter and PICC placement.2 In the case of two or more unsuccessful attempts at peripheral IV catheter placement by an advanced inserter using technology assistance (ultrasound), PICC placement is considered appropriate by the panel to avoid delays in treatment and limit patient discomfort associated with repeat attempts.

Long-term Vascular Access

Children with medical complexity or chronic illness may require long-term (>2 months) or very-long-term (>1 year) vascular access. Common themes for VAD selection in this heterogeneous population include a focus on vessel preservation and complication prevention.2 The panel strongly recommended that clinicians partner with the patient and caregivers in the decision-making process. Shared decision-making is necessary to meet both the short-term and evolving needs of the of the patient and family. The panel also believed the frequency of hospitalization should not be used as a criterion for VAD selection since acute hospitalization is an unreliable proxy for disease severity in pediatric chronic disease conditions.2 Rather, the infusate characteristics and length/intermittency of therapy should be primary influencers of VAD selection. In general, the panel rated cuffed tunneled central VADs (CVADs) as appropriate for all age groups for long-term PN, long-term continuous infusions, and long-term intermittent therapies. For continuous non-PN infusions, appropriate ratings were given to PICCs for infants and children and total implanted venous devices (TIVDs) in children and adolescents. For intermittent (but at least daily) access, TIVDs and PICC lines were both rated as appropriate for children and adolescents but uncertain for neonates and infants. Peripheral devices were deemed inappropriate for all long-term complex therapies. For children and adolescents needing intermittent, regular peripheral treatments (eg, steroids or antibiotics), peripheral IVs and TIVDs were rated appropriate for short duration (<7 days) therapies. PICCs and midlines for this indication were uncertain because of the lack of evidence. For medium-duration intermittent therapies (8-14 days), PICCs, tunneled cuffed CVADs, and TIVDs were rated as appropriate. A recently released mobile application can help guide the clinician through many varied clinical scenarios and indications.10

LIMITATIONS AND GAPS

The guideline recommendations were more often reliant on clinical practice guidelines and expert panel opinion given the lack of high-quality pediatric evidence for most scenarios. The panel members were from the United States and Australia, so the recommendations may not be generalizable to care systems in other countries. Although the panel included experts from many specialties that care for patient populations needing VADs, not all subspecialty populations were considered, particularly those with long-term vascular access–dependent conditions who may be commonly hospitalized. Scenarios with disagreement or uncertainty highlight gaps in need of future study (eg, midline catheter use and device selection for blood draws).

CONCLUSIONS AND APPLICATION

miniMAGIC is the first appropriateness guideline to help standardize the safe use of VADs in children. Although some gaps remain, the authors intend it to be a living document that will need revisions as new evidence is published. A mobile health application facilitates use of the recommendations, providing quick, point-of-care decision support based on clinical features.10 Pediatric hospitalists should collaborate with their institutions to examine their current VAD use in hospitalized children and identify opportunities for practice change and standardization. Use of these recommendations may help hospitalists improve the care of hospitalized children by decreasing unnecessary PICC placement and better partner with patients and caregivers to limit discomfort surrounding VAD placement.

Files
References

1. Ullman AJ, Marsh N, Mihala G, Cooke M, Rickard CM. Complications of central venous access devices: a systematic review. Pediatrics. 2015;136(5):e1331-e1344. https://doi.org/10.1542/peds.2015-1507
2. Ullman AJ, Bernstein SJ, Brown E, et al. The Michigan appropriateness guide for intravenous catheters in pediatrics: miniMAGIC. Pediatrics. 2020;145(Suppl 3):S269-S284. https://doi.org/10.1542/peds.2019-3474I
3. Ullman AJ, Chopra V, Brown E, et al. Developing appropriateness criteria for pediatric vascular access. Pediatrics. 2020;145(Suppl 3):S233-S242. https://doi.org/10.1542/peds.2019-3474G
4. Paterson RS, Chopra V, Brown E, et al. Selection and insertion of vascular access devices in pediatrics: a systematic review. Pediatrics. 2020;145(Suppl 3):S243-S268. https://doi.org/10.1542/peds.2019-3474H
5. Keren R, Shah SS, Srivastava R, et al. Comparative effectiveness of intravenous vs oral antibiotics for postdischarge treatment of acute osteomeyelitis in children. JAMA Pediatr. 2015;169(2):120-128. https://doi.org/10.1001/jamapediatrics.2014.2822
6. Shah SS, Srivastava R, Wu S, et al. Intravenous versus oral antibiotics for postdischarge treatment of complicated pneumonia. Pediatrics. 2016;138(6):e20161692. https://doi.org/10.1542/peds.2016-1692
7. Rangel SJ, Anderson BR, Srivastava R, et al. Intravenous versus oral antibiotics for the prevention of treatment failure in children with complicated appendicitis: has the abandonment of peripherally inserted catheters been justified? Ann Surg. 2017;266(2):361-368. https://doi.org/10.1097/SLA.0000000000001923
8. Desai S, Aronson PL, Shabanova V, et al. Parenteral antibiotic therapy duration in young infants with bacteremic urinary tract infections. Pediatrics. 2019;144(3):e20183844. https://doi.org/10.1542/peds.2018-3844
9. Anderson J, Greenwell A, Louderback J, Polivka BJ, Herron Behr J. Comparison of outcomes of extended dwell/midline peripheral intravenous catheters and peripherally inserted central catheters in children. J Assoc Vasc Access. 2016;21(3):158-164. https://doi.org/10.1016/j.java.2016.03.007
10. miniMAGIC: the Michigan Appropriateness Guide for Intravenous Catheters in Pediatrics app. Version 1.0.0. Alliance for Vascular Access Teaching and Research.
11. Shaughnessy EE, Morton K, Shah SS. Vascular access in hospitalized children. Pediatrics. 2020;145(Suppl 3):S298-S299. https://doi.org/10.1542/peds.2019-3474P

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1Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio; 2Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; 3Division of Inpatient Medicine, Department of Pediatrics, University of Utah and Intermountain Primary Children’s Hospital, Salt Lake City, Utah; 4Intermountain Healthcare Delivery Institute, Murray, Utah.

Disclosures
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1Department of Pediatrics, University of Cincinnati College of Medicine, Cincinnati, Ohio; 2Division of Hospital Medicine, Cincinnati Children’s Hospital Medical Center, Cincinnati, Ohio; 3Division of Inpatient Medicine, Department of Pediatrics, University of Utah and Intermountain Primary Children’s Hospital, Salt Lake City, Utah; 4Intermountain Healthcare Delivery Institute, Murray, Utah.

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Related Articles

Hospitalized pediatric patients often require vascular access for necessary therapies, such as antibiotics. However, vascular access devices (VADs) are also associated with harm, ranging from insertion complications to life-threatening bloodstream infections or thrombosis.1 Pediatric hospitalists often guide VAD placement. There is a paucity of evidence to guide VAD selection based on the relative benefits and risks.2 The Michigan Appropriateness Guide for Intravenous Catheters in Pediatrics (miniMAGIC)2 offers the first set of standards. Like its adult predecessor guideline (MAGIC) published in 2015, it provides guidance on appropriate VAD selection based on current evidence and expertise from a multidisciplinary panel.2 The guideline informs device selection, device characteristics, and insertion technique for the pediatric population (term neonates to adolescents) and across a wide range of clinical indications.2 This review highlights key recommendations for pediatric hospitalists to help their decision-making.

METHODS USED IN PREPARING THE GUIDELINE

miniMAGIC was developed using the RAND/UCLA Appropriateness Method, a method proven to reduce inappropriate (ie, overused or underused) healthcare interventions.3 It combines rigorous evidence review with multidisciplinary expert opinion on real-world clinical scenarios to provide recommendations about an intervention’s appropriateness.3 This is particularly useful for clinical scenarios that lack high-quality evidence to guide decision-making. The RAND/UCLA method deems an intervention appropriate if the benefits outweigh the risks by a wide enough margin that proceeding is worthwhile, and it does not take cost into account.2 The method design consists of five phases: (1) defining the scope and key terms, (2) reviewing and synthesizing the literature, (3) selecting an expert panel, (4) developing case scenarios, and (5) conducting two rounds of appropriateness ratings by the expert panel for each clinical scenario.3 The guideline’s scope included term neonates (aged 0-30 days), infants (aged 31 days-1 year), children (aged 1-12 years), and adolescents (aged 12-18 years). Infants receiving care in the neonatal intensive care unit or special care nursery were excluded. Other specialized populations addressed based on setting or diagnosis were general hospitalized patients and patients with congenital cardiac disease, critical illness, oncologic and hematologic conditions, and long-term VAD-dependent conditions.3

A total of 133 studies or clinical practice guidelines (CPGs) met the eligibility criteria for the systematic review.4 Although the systematic review was conducted per the RAND/UCLA method using two independent reviewers who evaluated the methodologic quality, transparency, and relevancy of each article, there was no formal assessment of evidence quality. The recommendations were based primarily on observational studies and CPGs because there were few randomized controlled trials or systematic reviews on VAD selection for pediatric patients in the literature. Pediatric evidence was limited for certain scenarios or populations (eg, term neonates, midline catheters, difficult venous access, long-term VAD), so adult and/or neonatal evidence was included when applicable.

The panel included 14 pediatric clinical experts from cardiology, vascular access, critical care, hematology/oncology, emergency medicine, general surgery, hospital medicine, anesthesia, interventional radiology, pharmacology, and infectious diseases. The panel also included nonvoting panel members such as the panel facilitators, a methodologist, and a patient representative.

RESULTS OF THE CLINICAL REVIEW

We review four common clinical scenarios encountered by pediatric hospitalists and summarize key recommendations (Table).

Key Recommendations for Pediatric Hospital Medicine

Peripherally Inserted Central Catheter

Patients may require peripherally inserted central catheters (PICCs) to facilitate a longer duration of intravenous (IV) therapy, such as delivery of antibiotics, or frequent blood draws. The need for prolonged vascular access is decreasing, as studies show many infections in children previously treated with prolonged IV antibiotics can be safely and equally effectively managed with early transition to oral therapy.5-8 These studies highlight the higher rate of complications and risks associated with PICCs, including thrombosis, infection, and mechanical issues, as well as the added healthcare utilization needed to evaluate and manage the complications. PICC-associated complication rates also increase with duration.4

However, there are some clinical scenarios that still warrant prolonged therapy and/or access; PICC recommendations are summarized in the Appendix Figure. The miniMAGIC panel deemed PICC lines appropriate for any nonperipheral therapy of any length. For peripherally compatible therapy, the panel rated PICC placement as inappropriate for therapy lasting less than 8 days, regardless of patient age. PICC placement in infants, children, and adolescents was rated appropriate for therapy with a duration exceeding 14 days, but the panel was uncertain about therapy expected to last between 8 and 14 days. Recognizing the additional challenges with maintaining peripheral IV catheter access in neonates, PICCs were deemed appropriate for neonates needing peripheral therapy lasting longer than 7 days.

The panel rated PICC placement appropriate for frequent blood draws (defined as more than one time per day) for more than 7 days in neonates or infants and more than 14 days in children and adolescents. But regardless of patient age, the PICC caliber must be at least 3F.

The miniMAGIC panel found that a single lumen is appropriate in most cases, highlighting that multilumen catheters increase the risk for infection, occlusion, and venous thrombosis.4 Multilumen catheters were rated as inappropriate in the case of reserving a lumen for blood products and blood sampling. When reserving a lumen for lipids and parenteral nutrition (PN), the panel was uncertain given the lack of evidence regarding the risks/benefits of the complications associated with the infusions themselves versus those of the device. Regardless, collaboration with a pharmacist and vascular access specialist is recommended to aid in choosing the most appropriate device characteristics.

Midline Catheters

Midline catheters are inserted in a peripheral vein, but the catheter tip terminates in the proximal extremity. Compared with peripheral IV catheters, midline catheters last longer and have lower rates of phlebitis. In addition, midline catheter placement does not require sedation or fluoroscopy and has lower rates of infection compared with PICC lines.9 Although there is good evidence in adults, and multiple panelists reported success in using midline catheters in various age groups, the evidence for their safe and efficacious use in pediatrics is limited, particularly for infants. Midline catheters were rated as appropriate for peripheral therapy lasting less than 8 days in neonates and less than 15 days in children and adolescents. Use in infants was deemed uncertain based on lack of published evidence. Midline catheters were also rated as appropriate for frequent blood draws of less than 8 days in neonates and less than 15 days in adolescents, but uncertain for children and infants.

Difficult Access and Insertion Procedure

The panel rated three or more attempts for peripheral IV catheter insertion by a single clinician as inappropriate and recommended early escalation to a more experienced inserter after 0 to 2 attempts by a single provider. The goal is to preserve insertion sites and reduce patient discomfort. If a patient loses access when only 1 day of therapy remains, the provider should transition to oral or intramuscular therapy when appropriate, particularly if there are no advanced insertion staff available or after two or more attempts at re-insertion are unsuccessful. There is high-quality evidence that supports vessel visualization (primarily ultrasound) with peripheral IV catheter and PICC placement.2 In the case of two or more unsuccessful attempts at peripheral IV catheter placement by an advanced inserter using technology assistance (ultrasound), PICC placement is considered appropriate by the panel to avoid delays in treatment and limit patient discomfort associated with repeat attempts.

Long-term Vascular Access

Children with medical complexity or chronic illness may require long-term (>2 months) or very-long-term (>1 year) vascular access. Common themes for VAD selection in this heterogeneous population include a focus on vessel preservation and complication prevention.2 The panel strongly recommended that clinicians partner with the patient and caregivers in the decision-making process. Shared decision-making is necessary to meet both the short-term and evolving needs of the of the patient and family. The panel also believed the frequency of hospitalization should not be used as a criterion for VAD selection since acute hospitalization is an unreliable proxy for disease severity in pediatric chronic disease conditions.2 Rather, the infusate characteristics and length/intermittency of therapy should be primary influencers of VAD selection. In general, the panel rated cuffed tunneled central VADs (CVADs) as appropriate for all age groups for long-term PN, long-term continuous infusions, and long-term intermittent therapies. For continuous non-PN infusions, appropriate ratings were given to PICCs for infants and children and total implanted venous devices (TIVDs) in children and adolescents. For intermittent (but at least daily) access, TIVDs and PICC lines were both rated as appropriate for children and adolescents but uncertain for neonates and infants. Peripheral devices were deemed inappropriate for all long-term complex therapies. For children and adolescents needing intermittent, regular peripheral treatments (eg, steroids or antibiotics), peripheral IVs and TIVDs were rated appropriate for short duration (<7 days) therapies. PICCs and midlines for this indication were uncertain because of the lack of evidence. For medium-duration intermittent therapies (8-14 days), PICCs, tunneled cuffed CVADs, and TIVDs were rated as appropriate. A recently released mobile application can help guide the clinician through many varied clinical scenarios and indications.10

LIMITATIONS AND GAPS

The guideline recommendations were more often reliant on clinical practice guidelines and expert panel opinion given the lack of high-quality pediatric evidence for most scenarios. The panel members were from the United States and Australia, so the recommendations may not be generalizable to care systems in other countries. Although the panel included experts from many specialties that care for patient populations needing VADs, not all subspecialty populations were considered, particularly those with long-term vascular access–dependent conditions who may be commonly hospitalized. Scenarios with disagreement or uncertainty highlight gaps in need of future study (eg, midline catheter use and device selection for blood draws).

CONCLUSIONS AND APPLICATION

miniMAGIC is the first appropriateness guideline to help standardize the safe use of VADs in children. Although some gaps remain, the authors intend it to be a living document that will need revisions as new evidence is published. A mobile health application facilitates use of the recommendations, providing quick, point-of-care decision support based on clinical features.10 Pediatric hospitalists should collaborate with their institutions to examine their current VAD use in hospitalized children and identify opportunities for practice change and standardization. Use of these recommendations may help hospitalists improve the care of hospitalized children by decreasing unnecessary PICC placement and better partner with patients and caregivers to limit discomfort surrounding VAD placement.

Hospitalized pediatric patients often require vascular access for necessary therapies, such as antibiotics. However, vascular access devices (VADs) are also associated with harm, ranging from insertion complications to life-threatening bloodstream infections or thrombosis.1 Pediatric hospitalists often guide VAD placement. There is a paucity of evidence to guide VAD selection based on the relative benefits and risks.2 The Michigan Appropriateness Guide for Intravenous Catheters in Pediatrics (miniMAGIC)2 offers the first set of standards. Like its adult predecessor guideline (MAGIC) published in 2015, it provides guidance on appropriate VAD selection based on current evidence and expertise from a multidisciplinary panel.2 The guideline informs device selection, device characteristics, and insertion technique for the pediatric population (term neonates to adolescents) and across a wide range of clinical indications.2 This review highlights key recommendations for pediatric hospitalists to help their decision-making.

METHODS USED IN PREPARING THE GUIDELINE

miniMAGIC was developed using the RAND/UCLA Appropriateness Method, a method proven to reduce inappropriate (ie, overused or underused) healthcare interventions.3 It combines rigorous evidence review with multidisciplinary expert opinion on real-world clinical scenarios to provide recommendations about an intervention’s appropriateness.3 This is particularly useful for clinical scenarios that lack high-quality evidence to guide decision-making. The RAND/UCLA method deems an intervention appropriate if the benefits outweigh the risks by a wide enough margin that proceeding is worthwhile, and it does not take cost into account.2 The method design consists of five phases: (1) defining the scope and key terms, (2) reviewing and synthesizing the literature, (3) selecting an expert panel, (4) developing case scenarios, and (5) conducting two rounds of appropriateness ratings by the expert panel for each clinical scenario.3 The guideline’s scope included term neonates (aged 0-30 days), infants (aged 31 days-1 year), children (aged 1-12 years), and adolescents (aged 12-18 years). Infants receiving care in the neonatal intensive care unit or special care nursery were excluded. Other specialized populations addressed based on setting or diagnosis were general hospitalized patients and patients with congenital cardiac disease, critical illness, oncologic and hematologic conditions, and long-term VAD-dependent conditions.3

A total of 133 studies or clinical practice guidelines (CPGs) met the eligibility criteria for the systematic review.4 Although the systematic review was conducted per the RAND/UCLA method using two independent reviewers who evaluated the methodologic quality, transparency, and relevancy of each article, there was no formal assessment of evidence quality. The recommendations were based primarily on observational studies and CPGs because there were few randomized controlled trials or systematic reviews on VAD selection for pediatric patients in the literature. Pediatric evidence was limited for certain scenarios or populations (eg, term neonates, midline catheters, difficult venous access, long-term VAD), so adult and/or neonatal evidence was included when applicable.

The panel included 14 pediatric clinical experts from cardiology, vascular access, critical care, hematology/oncology, emergency medicine, general surgery, hospital medicine, anesthesia, interventional radiology, pharmacology, and infectious diseases. The panel also included nonvoting panel members such as the panel facilitators, a methodologist, and a patient representative.

RESULTS OF THE CLINICAL REVIEW

We review four common clinical scenarios encountered by pediatric hospitalists and summarize key recommendations (Table).

Key Recommendations for Pediatric Hospital Medicine

Peripherally Inserted Central Catheter

Patients may require peripherally inserted central catheters (PICCs) to facilitate a longer duration of intravenous (IV) therapy, such as delivery of antibiotics, or frequent blood draws. The need for prolonged vascular access is decreasing, as studies show many infections in children previously treated with prolonged IV antibiotics can be safely and equally effectively managed with early transition to oral therapy.5-8 These studies highlight the higher rate of complications and risks associated with PICCs, including thrombosis, infection, and mechanical issues, as well as the added healthcare utilization needed to evaluate and manage the complications. PICC-associated complication rates also increase with duration.4

However, there are some clinical scenarios that still warrant prolonged therapy and/or access; PICC recommendations are summarized in the Appendix Figure. The miniMAGIC panel deemed PICC lines appropriate for any nonperipheral therapy of any length. For peripherally compatible therapy, the panel rated PICC placement as inappropriate for therapy lasting less than 8 days, regardless of patient age. PICC placement in infants, children, and adolescents was rated appropriate for therapy with a duration exceeding 14 days, but the panel was uncertain about therapy expected to last between 8 and 14 days. Recognizing the additional challenges with maintaining peripheral IV catheter access in neonates, PICCs were deemed appropriate for neonates needing peripheral therapy lasting longer than 7 days.

The panel rated PICC placement appropriate for frequent blood draws (defined as more than one time per day) for more than 7 days in neonates or infants and more than 14 days in children and adolescents. But regardless of patient age, the PICC caliber must be at least 3F.

The miniMAGIC panel found that a single lumen is appropriate in most cases, highlighting that multilumen catheters increase the risk for infection, occlusion, and venous thrombosis.4 Multilumen catheters were rated as inappropriate in the case of reserving a lumen for blood products and blood sampling. When reserving a lumen for lipids and parenteral nutrition (PN), the panel was uncertain given the lack of evidence regarding the risks/benefits of the complications associated with the infusions themselves versus those of the device. Regardless, collaboration with a pharmacist and vascular access specialist is recommended to aid in choosing the most appropriate device characteristics.

Midline Catheters

Midline catheters are inserted in a peripheral vein, but the catheter tip terminates in the proximal extremity. Compared with peripheral IV catheters, midline catheters last longer and have lower rates of phlebitis. In addition, midline catheter placement does not require sedation or fluoroscopy and has lower rates of infection compared with PICC lines.9 Although there is good evidence in adults, and multiple panelists reported success in using midline catheters in various age groups, the evidence for their safe and efficacious use in pediatrics is limited, particularly for infants. Midline catheters were rated as appropriate for peripheral therapy lasting less than 8 days in neonates and less than 15 days in children and adolescents. Use in infants was deemed uncertain based on lack of published evidence. Midline catheters were also rated as appropriate for frequent blood draws of less than 8 days in neonates and less than 15 days in adolescents, but uncertain for children and infants.

Difficult Access and Insertion Procedure

The panel rated three or more attempts for peripheral IV catheter insertion by a single clinician as inappropriate and recommended early escalation to a more experienced inserter after 0 to 2 attempts by a single provider. The goal is to preserve insertion sites and reduce patient discomfort. If a patient loses access when only 1 day of therapy remains, the provider should transition to oral or intramuscular therapy when appropriate, particularly if there are no advanced insertion staff available or after two or more attempts at re-insertion are unsuccessful. There is high-quality evidence that supports vessel visualization (primarily ultrasound) with peripheral IV catheter and PICC placement.2 In the case of two or more unsuccessful attempts at peripheral IV catheter placement by an advanced inserter using technology assistance (ultrasound), PICC placement is considered appropriate by the panel to avoid delays in treatment and limit patient discomfort associated with repeat attempts.

Long-term Vascular Access

Children with medical complexity or chronic illness may require long-term (>2 months) or very-long-term (>1 year) vascular access. Common themes for VAD selection in this heterogeneous population include a focus on vessel preservation and complication prevention.2 The panel strongly recommended that clinicians partner with the patient and caregivers in the decision-making process. Shared decision-making is necessary to meet both the short-term and evolving needs of the of the patient and family. The panel also believed the frequency of hospitalization should not be used as a criterion for VAD selection since acute hospitalization is an unreliable proxy for disease severity in pediatric chronic disease conditions.2 Rather, the infusate characteristics and length/intermittency of therapy should be primary influencers of VAD selection. In general, the panel rated cuffed tunneled central VADs (CVADs) as appropriate for all age groups for long-term PN, long-term continuous infusions, and long-term intermittent therapies. For continuous non-PN infusions, appropriate ratings were given to PICCs for infants and children and total implanted venous devices (TIVDs) in children and adolescents. For intermittent (but at least daily) access, TIVDs and PICC lines were both rated as appropriate for children and adolescents but uncertain for neonates and infants. Peripheral devices were deemed inappropriate for all long-term complex therapies. For children and adolescents needing intermittent, regular peripheral treatments (eg, steroids or antibiotics), peripheral IVs and TIVDs were rated appropriate for short duration (<7 days) therapies. PICCs and midlines for this indication were uncertain because of the lack of evidence. For medium-duration intermittent therapies (8-14 days), PICCs, tunneled cuffed CVADs, and TIVDs were rated as appropriate. A recently released mobile application can help guide the clinician through many varied clinical scenarios and indications.10

LIMITATIONS AND GAPS

The guideline recommendations were more often reliant on clinical practice guidelines and expert panel opinion given the lack of high-quality pediatric evidence for most scenarios. The panel members were from the United States and Australia, so the recommendations may not be generalizable to care systems in other countries. Although the panel included experts from many specialties that care for patient populations needing VADs, not all subspecialty populations were considered, particularly those with long-term vascular access–dependent conditions who may be commonly hospitalized. Scenarios with disagreement or uncertainty highlight gaps in need of future study (eg, midline catheter use and device selection for blood draws).

CONCLUSIONS AND APPLICATION

miniMAGIC is the first appropriateness guideline to help standardize the safe use of VADs in children. Although some gaps remain, the authors intend it to be a living document that will need revisions as new evidence is published. A mobile health application facilitates use of the recommendations, providing quick, point-of-care decision support based on clinical features.10 Pediatric hospitalists should collaborate with their institutions to examine their current VAD use in hospitalized children and identify opportunities for practice change and standardization. Use of these recommendations may help hospitalists improve the care of hospitalized children by decreasing unnecessary PICC placement and better partner with patients and caregivers to limit discomfort surrounding VAD placement.

References

1. Ullman AJ, Marsh N, Mihala G, Cooke M, Rickard CM. Complications of central venous access devices: a systematic review. Pediatrics. 2015;136(5):e1331-e1344. https://doi.org/10.1542/peds.2015-1507
2. Ullman AJ, Bernstein SJ, Brown E, et al. The Michigan appropriateness guide for intravenous catheters in pediatrics: miniMAGIC. Pediatrics. 2020;145(Suppl 3):S269-S284. https://doi.org/10.1542/peds.2019-3474I
3. Ullman AJ, Chopra V, Brown E, et al. Developing appropriateness criteria for pediatric vascular access. Pediatrics. 2020;145(Suppl 3):S233-S242. https://doi.org/10.1542/peds.2019-3474G
4. Paterson RS, Chopra V, Brown E, et al. Selection and insertion of vascular access devices in pediatrics: a systematic review. Pediatrics. 2020;145(Suppl 3):S243-S268. https://doi.org/10.1542/peds.2019-3474H
5. Keren R, Shah SS, Srivastava R, et al. Comparative effectiveness of intravenous vs oral antibiotics for postdischarge treatment of acute osteomeyelitis in children. JAMA Pediatr. 2015;169(2):120-128. https://doi.org/10.1001/jamapediatrics.2014.2822
6. Shah SS, Srivastava R, Wu S, et al. Intravenous versus oral antibiotics for postdischarge treatment of complicated pneumonia. Pediatrics. 2016;138(6):e20161692. https://doi.org/10.1542/peds.2016-1692
7. Rangel SJ, Anderson BR, Srivastava R, et al. Intravenous versus oral antibiotics for the prevention of treatment failure in children with complicated appendicitis: has the abandonment of peripherally inserted catheters been justified? Ann Surg. 2017;266(2):361-368. https://doi.org/10.1097/SLA.0000000000001923
8. Desai S, Aronson PL, Shabanova V, et al. Parenteral antibiotic therapy duration in young infants with bacteremic urinary tract infections. Pediatrics. 2019;144(3):e20183844. https://doi.org/10.1542/peds.2018-3844
9. Anderson J, Greenwell A, Louderback J, Polivka BJ, Herron Behr J. Comparison of outcomes of extended dwell/midline peripheral intravenous catheters and peripherally inserted central catheters in children. J Assoc Vasc Access. 2016;21(3):158-164. https://doi.org/10.1016/j.java.2016.03.007
10. miniMAGIC: the Michigan Appropriateness Guide for Intravenous Catheters in Pediatrics app. Version 1.0.0. Alliance for Vascular Access Teaching and Research.
11. Shaughnessy EE, Morton K, Shah SS. Vascular access in hospitalized children. Pediatrics. 2020;145(Suppl 3):S298-S299. https://doi.org/10.1542/peds.2019-3474P

References

1. Ullman AJ, Marsh N, Mihala G, Cooke M, Rickard CM. Complications of central venous access devices: a systematic review. Pediatrics. 2015;136(5):e1331-e1344. https://doi.org/10.1542/peds.2015-1507
2. Ullman AJ, Bernstein SJ, Brown E, et al. The Michigan appropriateness guide for intravenous catheters in pediatrics: miniMAGIC. Pediatrics. 2020;145(Suppl 3):S269-S284. https://doi.org/10.1542/peds.2019-3474I
3. Ullman AJ, Chopra V, Brown E, et al. Developing appropriateness criteria for pediatric vascular access. Pediatrics. 2020;145(Suppl 3):S233-S242. https://doi.org/10.1542/peds.2019-3474G
4. Paterson RS, Chopra V, Brown E, et al. Selection and insertion of vascular access devices in pediatrics: a systematic review. Pediatrics. 2020;145(Suppl 3):S243-S268. https://doi.org/10.1542/peds.2019-3474H
5. Keren R, Shah SS, Srivastava R, et al. Comparative effectiveness of intravenous vs oral antibiotics for postdischarge treatment of acute osteomeyelitis in children. JAMA Pediatr. 2015;169(2):120-128. https://doi.org/10.1001/jamapediatrics.2014.2822
6. Shah SS, Srivastava R, Wu S, et al. Intravenous versus oral antibiotics for postdischarge treatment of complicated pneumonia. Pediatrics. 2016;138(6):e20161692. https://doi.org/10.1542/peds.2016-1692
7. Rangel SJ, Anderson BR, Srivastava R, et al. Intravenous versus oral antibiotics for the prevention of treatment failure in children with complicated appendicitis: has the abandonment of peripherally inserted catheters been justified? Ann Surg. 2017;266(2):361-368. https://doi.org/10.1097/SLA.0000000000001923
8. Desai S, Aronson PL, Shabanova V, et al. Parenteral antibiotic therapy duration in young infants with bacteremic urinary tract infections. Pediatrics. 2019;144(3):e20183844. https://doi.org/10.1542/peds.2018-3844
9. Anderson J, Greenwell A, Louderback J, Polivka BJ, Herron Behr J. Comparison of outcomes of extended dwell/midline peripheral intravenous catheters and peripherally inserted central catheters in children. J Assoc Vasc Access. 2016;21(3):158-164. https://doi.org/10.1016/j.java.2016.03.007
10. miniMAGIC: the Michigan Appropriateness Guide for Intravenous Catheters in Pediatrics app. Version 1.0.0. Alliance for Vascular Access Teaching and Research.
11. Shaughnessy EE, Morton K, Shah SS. Vascular access in hospitalized children. Pediatrics. 2020;145(Suppl 3):S298-S299. https://doi.org/10.1542/peds.2019-3474P

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SARS-CoV-2 Seroprevalence Among Healthcare Workers by Job Function and Work Location in a New York Inner-City Hospital

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SARS-CoV-2 Seroprevalence Among Healthcare Workers by Job Function and Work Location in a New York Inner-City Hospital

SARS-CoV-2 has infected 141 million people worldwide and 31 million people in the United States as of April 20, 2021.1,2 The influx of hospital admissions and deaths has severely strained healthcare systems worldwide and placed healthcare workers (HCWs) at increased risk for acquiring COVID-19.3-5

Several studies have described the impact of COVID-19 on this heterogeneous group of HCWs. Shields et al reported a seroprevalence of 24.4% in HCWs at University Hospitals Birmingham (UK), with the highest rate, 34.5%, in housekeeping staff.6 Steensels et al reported a lower prevalence of 6.4% at a tertiary care center in Belgium, and showed no increased risk for HCWs when directly involved in clinical care.7 The authors attributed this to adequate use of personal protective equipment (PPE). Other studies have reported seroprevalences ranging from 1.6% to 18%.8-11 In the New York City (NYC) metro area, Jeremias et al reported a seroprevalence of 9.8% in HCWs and found no difference by job title or work location,12 whereas Moscola et al reported a seroprevalence of 13.7% and demonstrated a 3% increased risk for those working in service or maintenance.13 Antibody tests were conducted between March and April 2020 in all but two of these studies; testing in these two studies was performed between April 13 and June 23, 2020, with one reporting a seroprevalence of 6%11 and the other, 13.7%.13

NYC became the earliest pandemic epicenter in the United States following untracked transmission from ongoing circulation of SARS-CoV-2 in Europe.14 As a result, the COVID-19 surge in NYC commenced in March and largely subsided by the end of May 2020. Most HCW data reported to date do not reflect the situation at the end of the surge, and may underestimate true seroprevalence. We describe SARS-CoV-2 seroprevalence in HCWs in a large inner-city hospital in NYC, with antibody testing conducted from May 18 to June 26, 2020, at the subsidence of the surge. To further our understanding of occupational risk among different groups of HCWs, we examined associations of seroprevalence with HCWs’ job function and work location.

METHODS

This was a cross-sectional seroprevalence study conducted in the BronxCare Health System located in South and Central Bronx, an area that experienced one of the highest incidences of SARS-CoV-2 infections within NYC’s five boroughs.

HCWs were offered voluntary testing for serum antibodies to SARS-CoV-2 between May 18 and June 26, 2020. Testing occurred in the institution’s auditorium, a central and easily accessible location. Weekly emails were sent to all employees and department heads during the testing period, offering antibody testing and providing location and testing time information. The Elecsys Anti-SARS-CoV-2 (Roche) assay measuring total qualitative antibodies was used; the assay has a reported sensitivity of 97.1% 14 days after a positive SARS-CoV-2 RNA polymerase chain reaction (PCR) test result and a specificity of 100%.15

Demographic and work-related information was abstracted from electronic medical records, including all comorbid conditions that affected 30 or more HCWs. Pulmonary diagnoses, including asthma and chronic obstructive pulmonary disease, were grouped as chronic lung disease, and cardiovascular diseases, including hypertension, as chronic heart disease. Personal identifiers and data were delinked upon completion of data abstraction. The study was approved by the hospital’s institutional review board.

Job Function and Work Location

HCWs were grouped by job function as follows: physicians; nurses (including physician assistants and nurse practitioners); allied HCW I (medical assistants, patient care, and electrocardiogram, radiology, and ear, nose and throat technicians); allied HCW II (social workers, dieticians and nutritionists, registration clerks and unit associates, physical and occupational therapists); nonclinical staff (patient transporters, housekeeping staff, and security staff); pharmacists; engineering; and administrative staff. Respiratory therapists were considered as a separate group as their work placed them at high risk for respiratory diseases.

Work locations were as follows: clinics (including dental, outpatient, and satellite clinics), emergency departments (ED), inpatient units (including floors and intensive care units [ICU]), radiology suite, laboratory and pharmacy, and offices.

Statistical Analysis

Descriptive statistics were calculated using χ2 analyses. All demographic variables were tested against serology status (positive/negative). A binary logistic regression analysis was used to calculate odds ratios (ORs). Eight separate univariate unadjusted ORs were calculated by running each predictor variable against serology status (dependent variable), which included the six categorical variables—race, ethnicity, age, sex, body mass index (BMI), and prior SARS-CoV-2 PCR results—and the two main predictors—job function and work location. To obtain adjusted ORs, two final separate multivariable logistic regression analyses were executed including the six covariates listed. Due to high collinearity between job function and work location (χ2 = 3030.13, df = 35 [6 levels of work location – 1]*[8 levels of job function – 1]; P < .001), we included only one of the main predictors in each model. The regressions were specified such that the reference groups for the work location and job function variables were office work and administration, respectively. This choice was made based on the fact that their nonclinical functions do not confer an exposure risk in excess of that experienced by typical community populations. Sensitivity analyses were performed on the subset of HCWs whose address zip codes indicated residence within NYC to exclude the effect of different community seroprevalences in areas outside of NYC. The 95% CI for seroprevalence of antibodies within tested HCWs was estimated using the Clopper-Pearson binomial method.

RESULTS

Among all HCWs in the institution (N = 4,807), 2,749 (57.2%) underwent voluntary testing. Of those who underwent testing, 831 were positive for antibodies to SARS-CoV-2 (Figure 1), a seroprevalence of 30.2% (95% CI, 29%-32%). Among the age groups, the 45-to-64−year group had the highest seropositivity at 33% (400/1203), and those ≥75 years of age, the lowest at 16.7% (2/12) (P < .009).

Flow Diagram Showing Voluntary Testing Uptake and Results for Qualitative SARS-CoV-2 Antibody Testing
Data on race was available for 38.7% (1,064/2,749) of HCWs (Table); seropositivity was highest for Blacks (259/664, 39%) and lowest for Whites (36/163, 22.1%; P < .001). Certain comorbid conditions were associated with seropositivity (P = .001).
Healthcare Workers’ Demographic, Comorbid, and Work Characteristics by SARS-CoV-2 Antibody Status

Among all tested HCWs, 70.1% (1,928/2,749) resided in NYC. SARS-CoV-2 seroprevalence in this subset was 32% (616/1,928) (Figure 1). Demographic and comorbid conditions in HCWs who lived in NYC were similar to those of the whole group (Appendix Table 1).

HCWs who underwent voluntary antibody testing (Appendix Table 2) had a higher percentage of persons in the 45-to-64−year age group (43.8% vs 40.9%) and a lower percentage of persons in the 65-to-74−year age group (3.3% vs 5.3%) compared with the group of HCWs that did not undergo testing (P < .001). Gender, race, ethnicity, comorbid conditions, SARS-CoV-2 PCR testing, and work locations were not different between groups. The tested group had higher proportions of clinicians (physicians, nurses, allied HCWs I and II) than the untested nonparticipant group (P = .014).

SARS-CoV-2 PCR Tests on HCWs

More than one-third (34.1%; 938/2,749) of HCWs had a documented nasopharyngeal PCR test between March 23 and June 26, 2020 (Table). Of all PCRs performed, 262 were positive, giving an overall PCR positivity rate of 27.9%. Positivity was 51.4% in March and 36.6% in April. The reasons for PCR testing were not available, but likely represent a combination of exposure-related testing among asymptomatic individuals and diagnostic testing of symptomatic HCWs. In contrast, serology testing was indicative of prior infection and yielded a cumulative seroprevalence at the end of the surge. Findings were similar among HCWs residing in NYC (Appendix Table 1).

Work Location and Job Function

Among all HCWs (Table, Figure 2), there were differences in seropositivity by work location (P = .001). The largest number of HCWs worked in inpatient units (1,348/2,749, 49%), and the second largest in offices (554/2,749, 20%). The highest seropositivity rate was in the EDs, at 36.4% (64/176), followed by radiology suites, at 32.7% (17/52); the seropositivity rate in office locations was 25.8% (143/554). Among HCWs residing in NYC (Appendix Table 1, Appendix Figure 1), the rank order according to proportion seropositive by work location was similar to that of the whole group (P = .004), except that the second highest seropositivity rate was in the inpatient units (33.9% [323/953]). In the group of HCWs residing in NYC, office locations had a seropositivity of 27.4% (102/372). The seropositivity rates for both groups working in office locations were slightly higher than the 22% community seroprevalence in NYC reported for the same period.16

 Proportions Seropositive for SARS-CoV-2 Among All Tested Healthcare Workers by Job Function and Work Location

Among all HCWs, there were differences in seropositivity by job function (P = .001). The greatest proportion of HCWs were allied HCW II (23% [631/2,749]), followed by nurses (22.2% [611/2,749]) and physicians (21.3% [585/2,749] ). Seropositivity was highest for nonclinical staff (44.0% [51/116]), followed by nurses (37.5% [229/611]) and allied clinical HCW I and II (34.5% [143/414] and 32.0% [202/631], respectively). It was lowest for administrative staff (20.9% [42/201]) and pharmacists (11.1% [5/45]). Among HCWs residing in NYC, the rank order according to proportion seropositive by location was similar to that of the whole group. Administrative staff seropositivity was 18.3% (20/109). Administrative staff seropositivity for both groups was marginally lower than the 22% community seroprevalence in NYC for the same period.16

Odds Ratios for SARS-CoV-2 Seropositivity

For all HCWs, in unadjusted models (Appendix Table 3), age 45 to 64 years and Black race were associated with increased odds of being seropositive (1.26; 95% CI, 1.07-1.49 and 2.26; 95% CI, 1.51-3.37, respectively). Increased odds were seen for HCWs working in the ED (1.64; 95% CI, 1.14-2.36) and inpatient units (1.35; 95% CI, 1.08-1.69), and decreased odds were seen for those working in the laboratory and pharmacy (0.47; 95% CI, 0.26-0.86). Increased odds for seropositivity were found for nurses (2.27; 95% CI, 1.56-3.31), allied HCW I (2.00; 95% CI, 1.34-2.97), allied HCW II (1.78; 95% CI, 1.22-2.60), and nonclinical staff (2.97; 95% CI,1.80-4.90).

After adjusting for all covariates, HCWs who were Black remained at increased odds for being seropositive in the two final models (adjusted OR, 2.29; 95% CI, 1.38-3.81 and adjusted OR, 2.94; 95% CI, 1.78-4.85), as did those who had a BMI >30 kg/m2, with an adjusted OR of 1.36 (95% CI, 1.05-1.77) in one of the final models (Appendix Table 3). None of the other comorbid conditions had increased ORs. Those who worked in the ED and inpatient units also remained at increased odds after adjusting for covariates (2.27; 95% CI, 1.53-3.37 and 1.48; 95% CI, 1.14-1.92, respectively; Figure 3). Other job functions that had increased odds for seropositivity were nurses (2.54; 95% CI, 1.64-3.94), allied HCW I (1.83; 95% CI, 1.15-2.89) and II (1.70; 95% CI, 1.10-2.63), and nonclinical staff (2.51; 95% CI, 1.42-4.43).

Association of Job Function and Work Location With Seropositivity Among All Tested Healthcare Workers

Having a positive PCR for SAR-CoV-2 on nasopharyngeal swabs was strongly associated with seropositivity (OR, 47.26; 95% CI, 29.30-76.23 and OR, 44.79; 95% CI, 27.87-72.00) in the two multivariate-adjusted models. These findings were confirmed when the analyses were performed on HCWs who resided in NYC (Appendix Table 4 and Appendix Figure 2).

DISCUSSION

In a large inner-city New York hospital, we report a cumulative SARS-CoV-2 seroprevalence of 30.2% in HCWs at the end of the first surge of SARS-CoV-2 infections in NYC. We identified the highest seropositivity rates for nonclinical staff and nurses, followed by allied HCWs, with the odds of being seropositive ranging from 1.7 to 2.5. The work locations with the highest seroprevalences were the ED and inpatient units, with 2.3-fold and 1.5-fold increased odds of seropositivity, respectively.

Serosurveillance studies have reported the trajectory of community prevalence in NYC over the first wave. A 6.3% prevalence was reported in samples collected between March 23 and April 1, 2020.17 In a study by Rosenberg et al18 with testing performed from April 9 through April 28, 2020, prevalence increased to 22.7%. Serosurveillance data from the NYC Department of Health show prevalence ranging from 20.1% to 23.3% (average 22%) during the study period.16 Compared to the estimated seroprevalence of 9.3% in the United States,19 these rates established NYC as an early epicenter for the COVID-19 pandemic, with our institution’s HCW seroprevalence considerably higher than NYC community serosurveillance rates, 2.2 times higher than reported in the earlier HCW study in the greater NYC area,13 and higher than the 27% rate during May 2020 recently reported in another NYC hospital.20

Data from studies of hospital transmission and effects of mitigation measures, such as a universal masking policy for HCWs and patients, clearly demonstrate the high effectiveness of these measures in reducing hospital transmissions.21,22 This suggests HCW seroprevalence in institutions with well-implemented infection control and universal masking policies may not be a consequence of workplace exposures, but rather may be reflective of community rates.23 Our institution’s response commenced February 3, 2020, with implementation of social distancing, a universal masking policy, transmission-based precautions, and use of fitted N95 masks. Mid-March, elective surgeries were canceled, and inpatient visitation suspended. During the surge, these measures were widely and consistently implemented for all categories of HCWs throughout the work environment, based on emerging guidelines from the Centers for Disease Control and Prevention (CDC) and NYC Department of Health. Our overall observed HCW seroprevalence, well above that of the community, with differences in categories of job function and work locations, is therefore an important finding. Our sample of 2,749 HCWs lived in NYC and its surrounding suburbs and nearby states. There is heterogeneity in community seroprevalence between areas outside of NYC and NYC (an epicenter) itself. We therefore analyzed our data in the subset with NYC zip codes, confirming a similar overall prevalence and increased odds of seropositivity in nurses, allied HCWs, and nonclinical staff.

Physicians and administrative and office staff had seropositivity rates of 18.1%, 20.9%, and 25.8%, respectively, consistent with community rates and illustrating the effectiveness of PPE in the hospital setting. Since PPE use was part of a universal policy applied to all HCWs in our institution, other possible reasons may explain the differences we found. We speculate that the close working relationship nurses have with their patients resulted in a longer duration and higher frequency of daily interactions, increasing the risk for transmission and causing breakthrough infections.24,25 This increased risk is reflected in a study in which 28% of hospitalized patients were nurses and 9% certified nursing assistants.26

The CDC recently redefined close contact with someone with COVID-19 as a cumulative total of >15 minutes over 24 hours.25 Thus, several multiple short periods of exposure can increase risk for infection with SARS-CoV-2; such exposure is characteristic of the job function of nurses, nursing staff, and nonclinical staff. Further, housekeeping, transportation, and security officers are all nonclinical staff with significant and multiple exposures to COVID-19 patients during the surge, and for security officers, to continuous public traffic in and out of the hospital. SARS-CoV-2 spreads by virus shedding in large droplets and aerosols, with droplet nuclei <5 microns in size efficiently dispersed in air, an important additional mode of transmission.27-30 Airborne transmission coupled with virus shedding in asymptomatic and presymptomatic persons, which has been shown to cause secondary attack rates of up to 32%, are other factors that likely contributed to the increased seroprevalence in this group.31 Our observation is consistent with the Birmingham study, which reported the highest rate in housekeeping staff, with a prevalence of 34.5%, compared to 44% in this study.6 Similar reasons for high seropositivity rates apply to the two groups of allied HCWs (eg, medical assistants and patient care technicians, social workers, nutritionists and therapists), whose job functions place them in intermittent but significant proximity with inpatients and outpatients.

Consistent with public health data showing that minorities are disproportionately affected by this disease, we found that Black HCWs were three times more likely to be seropositive.32 However, an unexpected observation was the association between obesity and SARS-CoV-2 seropositivity. A possible explanation for this association may be inability to achieve optimal fit testing for N95 masks, thereby increasing the risk of exposure to droplet nuclei. This is important given that obesity is associated with poorer outcomes from COVID-19.

During the height of the first wave in NYC, EDs and inpatient units handled a large volume of COVID-19 patients with high PCR positivity rates (peak of 51% in March in our hospital). It was not unexpected that we observed increased odds of seropositivity in these work locations. As ICUs were at capacity, inpatient units cared for critically ill patients they would not normally have. HCWs in these locations coped with an increased workload, increased demand on PPE supplies, and work fatigue, which contributed to increased risk for hospital-acquired SARS-CoV-2 infections.

Reporting seroprevalence at a single institution was a limitation of the study. Approximately 57% of the hospital’s total HCW population was tested for antibodies. It is possible their risk profile influenced their decision to volunteer for testing when it became available, introducing selection bias. A comparison between tested and untested HCWs showed similarity in all demographic measures, including nasopharyngeal PCR testing, except for age. We did not have information on symptoms that would prompt PCR testing. HCWs who underwent voluntary testing were younger compared to those who did not undergo testing. Current NYC serosurveillance data showed higher seropositivity in the 45-to-64–year age group (27.8%-28.6%) compared to the 65-to-74–year age group (24.3%), which suggests that the tested group may overestimate seroprevalence among HCWs relative to a randomly selected sample.33 Similarly, there were more nurses, allied HCWs, physicians, and administrative staff in the tested group, with the former two having higher SARS-CoV-2 seropositivity compared to community prevalence, which could also overestimate seroprevalence. Our large sample size provided us with the power to detect differences within several different job functions and work locations, a strength of this study. It was not possible to differentiate community- from hospital-acquired infection in our HCWs, a limitation in many observational HCW seroprevalence studies. However, when we analyzed data restricted only to HCWs in NYC, to reduce the effect of differing community prevalences outside the city, our results were unchanged. Since it is possible that nonclinical HCWs are of a lower socioeconomic status compared to others (nurses and allied HCWs), we cannot exclude the possibility that higher SARS-CoV-2 seroprevalence associated with lower status explains, partly or completely, the increased odds of seropositivity we observed.34 Due to the high proportion of missing data for race (61.3%), we advise caution in interpreting our finding that the odds of seropositivity were three times higher for Black race, even though consistent with prior literature.34 Healthcare organizations have similar job function and work location categories incorporated in their infrastructure, suggesting that our observations may be generalizable to other hospitals in the United States.

CONCLUSION

These findings show that during the first surge in NYC, with its increased burden of disease, hospitalizations, morbidity, and mortality, seroprevalences varied based on job function and work location within this institution. Nurses were at highest risk for SARS-CoV-2 infection, as were those who worked in the ED. In preparation for subsequent waves of SARS-CoV-2 and other highly contagious respiratory infections, major medical centers need to enhance efforts aimed at protecting HCWs, with particular attention to these groups. This study also strongly supports the recent CDC guideline prioritizing HCWs to receive COVID-19 mRNA and adenovirus vector vaccines that have obtained emergency use authorization by the US Food and Drug Administration.35

Acknowledgments

The authors thank all the residents, nurses, and staff of the Department of Family Medicine for their contribution to this work.

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18. Rosenberg ES, Tesoriero JM, Rosenthal EM, et al. Cumulative incidence and diagnosis of SARS-CoV-2 infection in New York. Ann Epidemiol. Aug 2020;48:23-29 e4. https://doi.org/10.1016/j.annepidem.2020.06.004
19. Anand S, Montez-Rath M, Han J, et al. Prevalence of SARS-CoV-2 antibodies in a large nationwide sample of patients on dialysis in the USA: a cross-sectional study. Lancet. 2020;396(10259):1335-1344. https://doi.org/10.1016/S0140-6736(20)32009-2
20. Venugopal U, Jilani N, Rabah S, et al. SARS-CoV-2 seroprevalence among health care workers in a New York City hospital: a cross-sectional analysis during the COVID-19 pandemic. Int J Infect Dis. 2020;102:63-69. https://doi.org/10.1016/j.ijid.2020.10.036
21. Samaranayake LP, Fakhruddin KS, Ngo HC, Chang JWW, Panduwawala C. The effectiveness and efficacy of respiratory protective equipment (RPE) in dentistry and other health care settings: a systematic review. Acta Odontol Scand. 2020;78(8):626-639. https://doi.org/10.1080/00016357.2020.1810769
22. Seidelman JL, Lewis SS, Advani SD, et al. Universal masking is an effective strategy to flatten the severe acute respiratory coronavirus virus 2 (SARS-CoV-2) healthcare worker epidemiologic curve. Infect Control Hosp Epidemiol. 2020;41(12):1466-1467. https://doi.org/10.1017/ice.2020.313
23. Richterman A, Meyerowitz EA, Cevik M. Hospital-acquired SARS-CoV-2 infection: lessons for public health. JAMA. Published online November 13, 2020. https://doi.org/10.1001/jama.2020.21399
24. Degesys NF, Wang RC, Kwan E, Fahimi J, Noble JA, Raven MC. Correlation between n95 extended use and reuse and fit failure in an emergency department. JAMA. 2020;324(1):94-96. https://doi.org/10.1001/jama.2020.9843
25. Pringle JC, Leikauskas J, Ransom-Kelley S, et al. COVID-19 in a correctional facility employee following multiple brief exposures to persons with COVID-19 - Vermont, July-August 2020. MMWR Morb Mortal Wkly Rep. 2020;69(43):1569-1570. https://doi.org/10.15585/mmwr.mm6943e1
26. Kambhampati AK, O’Halloran AC, Whitaker M, et al. COVID-19-associated hospitalizations among health care personnel - COVID-NET, 13 states, March 1-May 31, 2020. MMWR Morb Mortal Wkly Rep. 2020;69(43):1576-1583. https://doi.org/10.15585/mmwr.mm6943e3
27. Zhang R, Li Y, Zhang AL, Wang Y, Molina MJ. Identifying airborne transmission as the dominant route for the spread of COVID-19. Proc Natl Acad Sci U S A. 2020;117(26):14857-14863. https://doi.org/10.1073/pnas.2009637117
28. Setti L, Passarini F, De Gennaro G, et al. Airborne transmission route of COVID-19: why 2 meters/6 feet of inter-personal distance could not be enough. Int J Environ Res Public Health. 2020;17(8):2932. https://doi.org/doi:10.3390/ijerph17082932
29. Klompas M, Baker MA, Rhee C. Airborne transmission of SARS-CoV-2: theoretical considerations and available evidence. JAMA. 2020;324(5):441-442. https://doi.org/10.1001/jama.2020.12458
30. Bourouiba L. Turbulent gas clouds and respiratory pathogen emissions: potential implications for reducing transmission of COVID-19. JAMA. 2020;323(18):1837-1838. https://doi.org/10.1001/jama.2020.4756
31. Qiu X, Nergiz A, Maraolo A, Bogoch I, Low N, Cevik M. The role of asymptomatic and pre-symptomatic infection in SARS-CoV-2 transmission – a living systematic review. Clin Mibrobiol Infect. 2021;20:S1198-743X(21)00038-0. Published online January 20, 2021. https://doi.org/10.1016/j.cmi.2021.01.011
32. Price-Haywood EG, Burton J, Fort D, Seoane L. Hospitalization and mortality among black patients and white patients with Covid-19. N Engl J Med. 2020;382(26):2534-2543. https://doi.org/doi:10.1056/NEJMsa2011686
33. New York City Department of Health. Covid-19: Data. Antibody testing by group - age. Accessed March 5, 2021. https://www1.nyc.gov/site/doh/covid/covid-19-data-totals.page#antibody
34. Patel JA, Nielsen FBH, Badiani AA, et al. Poverty, inequality and COVID-19: the forgotten vulnerable. Public Health. 2020;183:110-111. https://doi.org/10.1016/j.puhe.2020.05.006
35. Polack FP, Thomas SJ, Kitchin N, et al. Safety and efficacy of the BNT162b2 mRNA Covid-19 vaccine. N Engl J Med. 2020;383(27):2603-2615. https://doi.org/10.1056/NEJMoa2034577

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Disclosures
Dr Purswani receives research grant support, unrelated to this work, from the National Institute of Child Health and Human Development as the clinical site principal investigator for the International Maternal Pediatric and Adolescent Clinical Trials Group (IMPAACT) and the Pediatric HIV/AIDS Cohort Study (PHACS). The other authors have nothing to disclose.

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Disclosures
Dr Purswani receives research grant support, unrelated to this work, from the National Institute of Child Health and Human Development as the clinical site principal investigator for the International Maternal Pediatric and Adolescent Clinical Trials Group (IMPAACT) and the Pediatric HIV/AIDS Cohort Study (PHACS). The other authors have nothing to disclose.

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Disclosures
Dr Purswani receives research grant support, unrelated to this work, from the National Institute of Child Health and Human Development as the clinical site principal investigator for the International Maternal Pediatric and Adolescent Clinical Trials Group (IMPAACT) and the Pediatric HIV/AIDS Cohort Study (PHACS). The other authors have nothing to disclose.

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SARS-CoV-2 has infected 141 million people worldwide and 31 million people in the United States as of April 20, 2021.1,2 The influx of hospital admissions and deaths has severely strained healthcare systems worldwide and placed healthcare workers (HCWs) at increased risk for acquiring COVID-19.3-5

Several studies have described the impact of COVID-19 on this heterogeneous group of HCWs. Shields et al reported a seroprevalence of 24.4% in HCWs at University Hospitals Birmingham (UK), with the highest rate, 34.5%, in housekeeping staff.6 Steensels et al reported a lower prevalence of 6.4% at a tertiary care center in Belgium, and showed no increased risk for HCWs when directly involved in clinical care.7 The authors attributed this to adequate use of personal protective equipment (PPE). Other studies have reported seroprevalences ranging from 1.6% to 18%.8-11 In the New York City (NYC) metro area, Jeremias et al reported a seroprevalence of 9.8% in HCWs and found no difference by job title or work location,12 whereas Moscola et al reported a seroprevalence of 13.7% and demonstrated a 3% increased risk for those working in service or maintenance.13 Antibody tests were conducted between March and April 2020 in all but two of these studies; testing in these two studies was performed between April 13 and June 23, 2020, with one reporting a seroprevalence of 6%11 and the other, 13.7%.13

NYC became the earliest pandemic epicenter in the United States following untracked transmission from ongoing circulation of SARS-CoV-2 in Europe.14 As a result, the COVID-19 surge in NYC commenced in March and largely subsided by the end of May 2020. Most HCW data reported to date do not reflect the situation at the end of the surge, and may underestimate true seroprevalence. We describe SARS-CoV-2 seroprevalence in HCWs in a large inner-city hospital in NYC, with antibody testing conducted from May 18 to June 26, 2020, at the subsidence of the surge. To further our understanding of occupational risk among different groups of HCWs, we examined associations of seroprevalence with HCWs’ job function and work location.

METHODS

This was a cross-sectional seroprevalence study conducted in the BronxCare Health System located in South and Central Bronx, an area that experienced one of the highest incidences of SARS-CoV-2 infections within NYC’s five boroughs.

HCWs were offered voluntary testing for serum antibodies to SARS-CoV-2 between May 18 and June 26, 2020. Testing occurred in the institution’s auditorium, a central and easily accessible location. Weekly emails were sent to all employees and department heads during the testing period, offering antibody testing and providing location and testing time information. The Elecsys Anti-SARS-CoV-2 (Roche) assay measuring total qualitative antibodies was used; the assay has a reported sensitivity of 97.1% 14 days after a positive SARS-CoV-2 RNA polymerase chain reaction (PCR) test result and a specificity of 100%.15

Demographic and work-related information was abstracted from electronic medical records, including all comorbid conditions that affected 30 or more HCWs. Pulmonary diagnoses, including asthma and chronic obstructive pulmonary disease, were grouped as chronic lung disease, and cardiovascular diseases, including hypertension, as chronic heart disease. Personal identifiers and data were delinked upon completion of data abstraction. The study was approved by the hospital’s institutional review board.

Job Function and Work Location

HCWs were grouped by job function as follows: physicians; nurses (including physician assistants and nurse practitioners); allied HCW I (medical assistants, patient care, and electrocardiogram, radiology, and ear, nose and throat technicians); allied HCW II (social workers, dieticians and nutritionists, registration clerks and unit associates, physical and occupational therapists); nonclinical staff (patient transporters, housekeeping staff, and security staff); pharmacists; engineering; and administrative staff. Respiratory therapists were considered as a separate group as their work placed them at high risk for respiratory diseases.

Work locations were as follows: clinics (including dental, outpatient, and satellite clinics), emergency departments (ED), inpatient units (including floors and intensive care units [ICU]), radiology suite, laboratory and pharmacy, and offices.

Statistical Analysis

Descriptive statistics were calculated using χ2 analyses. All demographic variables were tested against serology status (positive/negative). A binary logistic regression analysis was used to calculate odds ratios (ORs). Eight separate univariate unadjusted ORs were calculated by running each predictor variable against serology status (dependent variable), which included the six categorical variables—race, ethnicity, age, sex, body mass index (BMI), and prior SARS-CoV-2 PCR results—and the two main predictors—job function and work location. To obtain adjusted ORs, two final separate multivariable logistic regression analyses were executed including the six covariates listed. Due to high collinearity between job function and work location (χ2 = 3030.13, df = 35 [6 levels of work location – 1]*[8 levels of job function – 1]; P < .001), we included only one of the main predictors in each model. The regressions were specified such that the reference groups for the work location and job function variables were office work and administration, respectively. This choice was made based on the fact that their nonclinical functions do not confer an exposure risk in excess of that experienced by typical community populations. Sensitivity analyses were performed on the subset of HCWs whose address zip codes indicated residence within NYC to exclude the effect of different community seroprevalences in areas outside of NYC. The 95% CI for seroprevalence of antibodies within tested HCWs was estimated using the Clopper-Pearson binomial method.

RESULTS

Among all HCWs in the institution (N = 4,807), 2,749 (57.2%) underwent voluntary testing. Of those who underwent testing, 831 were positive for antibodies to SARS-CoV-2 (Figure 1), a seroprevalence of 30.2% (95% CI, 29%-32%). Among the age groups, the 45-to-64−year group had the highest seropositivity at 33% (400/1203), and those ≥75 years of age, the lowest at 16.7% (2/12) (P < .009).

Flow Diagram Showing Voluntary Testing Uptake and Results for Qualitative SARS-CoV-2 Antibody Testing
Data on race was available for 38.7% (1,064/2,749) of HCWs (Table); seropositivity was highest for Blacks (259/664, 39%) and lowest for Whites (36/163, 22.1%; P < .001). Certain comorbid conditions were associated with seropositivity (P = .001).
Healthcare Workers’ Demographic, Comorbid, and Work Characteristics by SARS-CoV-2 Antibody Status

Among all tested HCWs, 70.1% (1,928/2,749) resided in NYC. SARS-CoV-2 seroprevalence in this subset was 32% (616/1,928) (Figure 1). Demographic and comorbid conditions in HCWs who lived in NYC were similar to those of the whole group (Appendix Table 1).

HCWs who underwent voluntary antibody testing (Appendix Table 2) had a higher percentage of persons in the 45-to-64−year age group (43.8% vs 40.9%) and a lower percentage of persons in the 65-to-74−year age group (3.3% vs 5.3%) compared with the group of HCWs that did not undergo testing (P < .001). Gender, race, ethnicity, comorbid conditions, SARS-CoV-2 PCR testing, and work locations were not different between groups. The tested group had higher proportions of clinicians (physicians, nurses, allied HCWs I and II) than the untested nonparticipant group (P = .014).

SARS-CoV-2 PCR Tests on HCWs

More than one-third (34.1%; 938/2,749) of HCWs had a documented nasopharyngeal PCR test between March 23 and June 26, 2020 (Table). Of all PCRs performed, 262 were positive, giving an overall PCR positivity rate of 27.9%. Positivity was 51.4% in March and 36.6% in April. The reasons for PCR testing were not available, but likely represent a combination of exposure-related testing among asymptomatic individuals and diagnostic testing of symptomatic HCWs. In contrast, serology testing was indicative of prior infection and yielded a cumulative seroprevalence at the end of the surge. Findings were similar among HCWs residing in NYC (Appendix Table 1).

Work Location and Job Function

Among all HCWs (Table, Figure 2), there were differences in seropositivity by work location (P = .001). The largest number of HCWs worked in inpatient units (1,348/2,749, 49%), and the second largest in offices (554/2,749, 20%). The highest seropositivity rate was in the EDs, at 36.4% (64/176), followed by radiology suites, at 32.7% (17/52); the seropositivity rate in office locations was 25.8% (143/554). Among HCWs residing in NYC (Appendix Table 1, Appendix Figure 1), the rank order according to proportion seropositive by work location was similar to that of the whole group (P = .004), except that the second highest seropositivity rate was in the inpatient units (33.9% [323/953]). In the group of HCWs residing in NYC, office locations had a seropositivity of 27.4% (102/372). The seropositivity rates for both groups working in office locations were slightly higher than the 22% community seroprevalence in NYC reported for the same period.16

 Proportions Seropositive for SARS-CoV-2 Among All Tested Healthcare Workers by Job Function and Work Location

Among all HCWs, there were differences in seropositivity by job function (P = .001). The greatest proportion of HCWs were allied HCW II (23% [631/2,749]), followed by nurses (22.2% [611/2,749]) and physicians (21.3% [585/2,749] ). Seropositivity was highest for nonclinical staff (44.0% [51/116]), followed by nurses (37.5% [229/611]) and allied clinical HCW I and II (34.5% [143/414] and 32.0% [202/631], respectively). It was lowest for administrative staff (20.9% [42/201]) and pharmacists (11.1% [5/45]). Among HCWs residing in NYC, the rank order according to proportion seropositive by location was similar to that of the whole group. Administrative staff seropositivity was 18.3% (20/109). Administrative staff seropositivity for both groups was marginally lower than the 22% community seroprevalence in NYC for the same period.16

Odds Ratios for SARS-CoV-2 Seropositivity

For all HCWs, in unadjusted models (Appendix Table 3), age 45 to 64 years and Black race were associated with increased odds of being seropositive (1.26; 95% CI, 1.07-1.49 and 2.26; 95% CI, 1.51-3.37, respectively). Increased odds were seen for HCWs working in the ED (1.64; 95% CI, 1.14-2.36) and inpatient units (1.35; 95% CI, 1.08-1.69), and decreased odds were seen for those working in the laboratory and pharmacy (0.47; 95% CI, 0.26-0.86). Increased odds for seropositivity were found for nurses (2.27; 95% CI, 1.56-3.31), allied HCW I (2.00; 95% CI, 1.34-2.97), allied HCW II (1.78; 95% CI, 1.22-2.60), and nonclinical staff (2.97; 95% CI,1.80-4.90).

After adjusting for all covariates, HCWs who were Black remained at increased odds for being seropositive in the two final models (adjusted OR, 2.29; 95% CI, 1.38-3.81 and adjusted OR, 2.94; 95% CI, 1.78-4.85), as did those who had a BMI >30 kg/m2, with an adjusted OR of 1.36 (95% CI, 1.05-1.77) in one of the final models (Appendix Table 3). None of the other comorbid conditions had increased ORs. Those who worked in the ED and inpatient units also remained at increased odds after adjusting for covariates (2.27; 95% CI, 1.53-3.37 and 1.48; 95% CI, 1.14-1.92, respectively; Figure 3). Other job functions that had increased odds for seropositivity were nurses (2.54; 95% CI, 1.64-3.94), allied HCW I (1.83; 95% CI, 1.15-2.89) and II (1.70; 95% CI, 1.10-2.63), and nonclinical staff (2.51; 95% CI, 1.42-4.43).

Association of Job Function and Work Location With Seropositivity Among All Tested Healthcare Workers

Having a positive PCR for SAR-CoV-2 on nasopharyngeal swabs was strongly associated with seropositivity (OR, 47.26; 95% CI, 29.30-76.23 and OR, 44.79; 95% CI, 27.87-72.00) in the two multivariate-adjusted models. These findings were confirmed when the analyses were performed on HCWs who resided in NYC (Appendix Table 4 and Appendix Figure 2).

DISCUSSION

In a large inner-city New York hospital, we report a cumulative SARS-CoV-2 seroprevalence of 30.2% in HCWs at the end of the first surge of SARS-CoV-2 infections in NYC. We identified the highest seropositivity rates for nonclinical staff and nurses, followed by allied HCWs, with the odds of being seropositive ranging from 1.7 to 2.5. The work locations with the highest seroprevalences were the ED and inpatient units, with 2.3-fold and 1.5-fold increased odds of seropositivity, respectively.

Serosurveillance studies have reported the trajectory of community prevalence in NYC over the first wave. A 6.3% prevalence was reported in samples collected between March 23 and April 1, 2020.17 In a study by Rosenberg et al18 with testing performed from April 9 through April 28, 2020, prevalence increased to 22.7%. Serosurveillance data from the NYC Department of Health show prevalence ranging from 20.1% to 23.3% (average 22%) during the study period.16 Compared to the estimated seroprevalence of 9.3% in the United States,19 these rates established NYC as an early epicenter for the COVID-19 pandemic, with our institution’s HCW seroprevalence considerably higher than NYC community serosurveillance rates, 2.2 times higher than reported in the earlier HCW study in the greater NYC area,13 and higher than the 27% rate during May 2020 recently reported in another NYC hospital.20

Data from studies of hospital transmission and effects of mitigation measures, such as a universal masking policy for HCWs and patients, clearly demonstrate the high effectiveness of these measures in reducing hospital transmissions.21,22 This suggests HCW seroprevalence in institutions with well-implemented infection control and universal masking policies may not be a consequence of workplace exposures, but rather may be reflective of community rates.23 Our institution’s response commenced February 3, 2020, with implementation of social distancing, a universal masking policy, transmission-based precautions, and use of fitted N95 masks. Mid-March, elective surgeries were canceled, and inpatient visitation suspended. During the surge, these measures were widely and consistently implemented for all categories of HCWs throughout the work environment, based on emerging guidelines from the Centers for Disease Control and Prevention (CDC) and NYC Department of Health. Our overall observed HCW seroprevalence, well above that of the community, with differences in categories of job function and work locations, is therefore an important finding. Our sample of 2,749 HCWs lived in NYC and its surrounding suburbs and nearby states. There is heterogeneity in community seroprevalence between areas outside of NYC and NYC (an epicenter) itself. We therefore analyzed our data in the subset with NYC zip codes, confirming a similar overall prevalence and increased odds of seropositivity in nurses, allied HCWs, and nonclinical staff.

Physicians and administrative and office staff had seropositivity rates of 18.1%, 20.9%, and 25.8%, respectively, consistent with community rates and illustrating the effectiveness of PPE in the hospital setting. Since PPE use was part of a universal policy applied to all HCWs in our institution, other possible reasons may explain the differences we found. We speculate that the close working relationship nurses have with their patients resulted in a longer duration and higher frequency of daily interactions, increasing the risk for transmission and causing breakthrough infections.24,25 This increased risk is reflected in a study in which 28% of hospitalized patients were nurses and 9% certified nursing assistants.26

The CDC recently redefined close contact with someone with COVID-19 as a cumulative total of >15 minutes over 24 hours.25 Thus, several multiple short periods of exposure can increase risk for infection with SARS-CoV-2; such exposure is characteristic of the job function of nurses, nursing staff, and nonclinical staff. Further, housekeeping, transportation, and security officers are all nonclinical staff with significant and multiple exposures to COVID-19 patients during the surge, and for security officers, to continuous public traffic in and out of the hospital. SARS-CoV-2 spreads by virus shedding in large droplets and aerosols, with droplet nuclei <5 microns in size efficiently dispersed in air, an important additional mode of transmission.27-30 Airborne transmission coupled with virus shedding in asymptomatic and presymptomatic persons, which has been shown to cause secondary attack rates of up to 32%, are other factors that likely contributed to the increased seroprevalence in this group.31 Our observation is consistent with the Birmingham study, which reported the highest rate in housekeeping staff, with a prevalence of 34.5%, compared to 44% in this study.6 Similar reasons for high seropositivity rates apply to the two groups of allied HCWs (eg, medical assistants and patient care technicians, social workers, nutritionists and therapists), whose job functions place them in intermittent but significant proximity with inpatients and outpatients.

Consistent with public health data showing that minorities are disproportionately affected by this disease, we found that Black HCWs were three times more likely to be seropositive.32 However, an unexpected observation was the association between obesity and SARS-CoV-2 seropositivity. A possible explanation for this association may be inability to achieve optimal fit testing for N95 masks, thereby increasing the risk of exposure to droplet nuclei. This is important given that obesity is associated with poorer outcomes from COVID-19.

During the height of the first wave in NYC, EDs and inpatient units handled a large volume of COVID-19 patients with high PCR positivity rates (peak of 51% in March in our hospital). It was not unexpected that we observed increased odds of seropositivity in these work locations. As ICUs were at capacity, inpatient units cared for critically ill patients they would not normally have. HCWs in these locations coped with an increased workload, increased demand on PPE supplies, and work fatigue, which contributed to increased risk for hospital-acquired SARS-CoV-2 infections.

Reporting seroprevalence at a single institution was a limitation of the study. Approximately 57% of the hospital’s total HCW population was tested for antibodies. It is possible their risk profile influenced their decision to volunteer for testing when it became available, introducing selection bias. A comparison between tested and untested HCWs showed similarity in all demographic measures, including nasopharyngeal PCR testing, except for age. We did not have information on symptoms that would prompt PCR testing. HCWs who underwent voluntary testing were younger compared to those who did not undergo testing. Current NYC serosurveillance data showed higher seropositivity in the 45-to-64–year age group (27.8%-28.6%) compared to the 65-to-74–year age group (24.3%), which suggests that the tested group may overestimate seroprevalence among HCWs relative to a randomly selected sample.33 Similarly, there were more nurses, allied HCWs, physicians, and administrative staff in the tested group, with the former two having higher SARS-CoV-2 seropositivity compared to community prevalence, which could also overestimate seroprevalence. Our large sample size provided us with the power to detect differences within several different job functions and work locations, a strength of this study. It was not possible to differentiate community- from hospital-acquired infection in our HCWs, a limitation in many observational HCW seroprevalence studies. However, when we analyzed data restricted only to HCWs in NYC, to reduce the effect of differing community prevalences outside the city, our results were unchanged. Since it is possible that nonclinical HCWs are of a lower socioeconomic status compared to others (nurses and allied HCWs), we cannot exclude the possibility that higher SARS-CoV-2 seroprevalence associated with lower status explains, partly or completely, the increased odds of seropositivity we observed.34 Due to the high proportion of missing data for race (61.3%), we advise caution in interpreting our finding that the odds of seropositivity were three times higher for Black race, even though consistent with prior literature.34 Healthcare organizations have similar job function and work location categories incorporated in their infrastructure, suggesting that our observations may be generalizable to other hospitals in the United States.

CONCLUSION

These findings show that during the first surge in NYC, with its increased burden of disease, hospitalizations, morbidity, and mortality, seroprevalences varied based on job function and work location within this institution. Nurses were at highest risk for SARS-CoV-2 infection, as were those who worked in the ED. In preparation for subsequent waves of SARS-CoV-2 and other highly contagious respiratory infections, major medical centers need to enhance efforts aimed at protecting HCWs, with particular attention to these groups. This study also strongly supports the recent CDC guideline prioritizing HCWs to receive COVID-19 mRNA and adenovirus vector vaccines that have obtained emergency use authorization by the US Food and Drug Administration.35

Acknowledgments

The authors thank all the residents, nurses, and staff of the Department of Family Medicine for their contribution to this work.

SARS-CoV-2 has infected 141 million people worldwide and 31 million people in the United States as of April 20, 2021.1,2 The influx of hospital admissions and deaths has severely strained healthcare systems worldwide and placed healthcare workers (HCWs) at increased risk for acquiring COVID-19.3-5

Several studies have described the impact of COVID-19 on this heterogeneous group of HCWs. Shields et al reported a seroprevalence of 24.4% in HCWs at University Hospitals Birmingham (UK), with the highest rate, 34.5%, in housekeeping staff.6 Steensels et al reported a lower prevalence of 6.4% at a tertiary care center in Belgium, and showed no increased risk for HCWs when directly involved in clinical care.7 The authors attributed this to adequate use of personal protective equipment (PPE). Other studies have reported seroprevalences ranging from 1.6% to 18%.8-11 In the New York City (NYC) metro area, Jeremias et al reported a seroprevalence of 9.8% in HCWs and found no difference by job title or work location,12 whereas Moscola et al reported a seroprevalence of 13.7% and demonstrated a 3% increased risk for those working in service or maintenance.13 Antibody tests were conducted between March and April 2020 in all but two of these studies; testing in these two studies was performed between April 13 and June 23, 2020, with one reporting a seroprevalence of 6%11 and the other, 13.7%.13

NYC became the earliest pandemic epicenter in the United States following untracked transmission from ongoing circulation of SARS-CoV-2 in Europe.14 As a result, the COVID-19 surge in NYC commenced in March and largely subsided by the end of May 2020. Most HCW data reported to date do not reflect the situation at the end of the surge, and may underestimate true seroprevalence. We describe SARS-CoV-2 seroprevalence in HCWs in a large inner-city hospital in NYC, with antibody testing conducted from May 18 to June 26, 2020, at the subsidence of the surge. To further our understanding of occupational risk among different groups of HCWs, we examined associations of seroprevalence with HCWs’ job function and work location.

METHODS

This was a cross-sectional seroprevalence study conducted in the BronxCare Health System located in South and Central Bronx, an area that experienced one of the highest incidences of SARS-CoV-2 infections within NYC’s five boroughs.

HCWs were offered voluntary testing for serum antibodies to SARS-CoV-2 between May 18 and June 26, 2020. Testing occurred in the institution’s auditorium, a central and easily accessible location. Weekly emails were sent to all employees and department heads during the testing period, offering antibody testing and providing location and testing time information. The Elecsys Anti-SARS-CoV-2 (Roche) assay measuring total qualitative antibodies was used; the assay has a reported sensitivity of 97.1% 14 days after a positive SARS-CoV-2 RNA polymerase chain reaction (PCR) test result and a specificity of 100%.15

Demographic and work-related information was abstracted from electronic medical records, including all comorbid conditions that affected 30 or more HCWs. Pulmonary diagnoses, including asthma and chronic obstructive pulmonary disease, were grouped as chronic lung disease, and cardiovascular diseases, including hypertension, as chronic heart disease. Personal identifiers and data were delinked upon completion of data abstraction. The study was approved by the hospital’s institutional review board.

Job Function and Work Location

HCWs were grouped by job function as follows: physicians; nurses (including physician assistants and nurse practitioners); allied HCW I (medical assistants, patient care, and electrocardiogram, radiology, and ear, nose and throat technicians); allied HCW II (social workers, dieticians and nutritionists, registration clerks and unit associates, physical and occupational therapists); nonclinical staff (patient transporters, housekeeping staff, and security staff); pharmacists; engineering; and administrative staff. Respiratory therapists were considered as a separate group as their work placed them at high risk for respiratory diseases.

Work locations were as follows: clinics (including dental, outpatient, and satellite clinics), emergency departments (ED), inpatient units (including floors and intensive care units [ICU]), radiology suite, laboratory and pharmacy, and offices.

Statistical Analysis

Descriptive statistics were calculated using χ2 analyses. All demographic variables were tested against serology status (positive/negative). A binary logistic regression analysis was used to calculate odds ratios (ORs). Eight separate univariate unadjusted ORs were calculated by running each predictor variable against serology status (dependent variable), which included the six categorical variables—race, ethnicity, age, sex, body mass index (BMI), and prior SARS-CoV-2 PCR results—and the two main predictors—job function and work location. To obtain adjusted ORs, two final separate multivariable logistic regression analyses were executed including the six covariates listed. Due to high collinearity between job function and work location (χ2 = 3030.13, df = 35 [6 levels of work location – 1]*[8 levels of job function – 1]; P < .001), we included only one of the main predictors in each model. The regressions were specified such that the reference groups for the work location and job function variables were office work and administration, respectively. This choice was made based on the fact that their nonclinical functions do not confer an exposure risk in excess of that experienced by typical community populations. Sensitivity analyses were performed on the subset of HCWs whose address zip codes indicated residence within NYC to exclude the effect of different community seroprevalences in areas outside of NYC. The 95% CI for seroprevalence of antibodies within tested HCWs was estimated using the Clopper-Pearson binomial method.

RESULTS

Among all HCWs in the institution (N = 4,807), 2,749 (57.2%) underwent voluntary testing. Of those who underwent testing, 831 were positive for antibodies to SARS-CoV-2 (Figure 1), a seroprevalence of 30.2% (95% CI, 29%-32%). Among the age groups, the 45-to-64−year group had the highest seropositivity at 33% (400/1203), and those ≥75 years of age, the lowest at 16.7% (2/12) (P < .009).

Flow Diagram Showing Voluntary Testing Uptake and Results for Qualitative SARS-CoV-2 Antibody Testing
Data on race was available for 38.7% (1,064/2,749) of HCWs (Table); seropositivity was highest for Blacks (259/664, 39%) and lowest for Whites (36/163, 22.1%; P < .001). Certain comorbid conditions were associated with seropositivity (P = .001).
Healthcare Workers’ Demographic, Comorbid, and Work Characteristics by SARS-CoV-2 Antibody Status

Among all tested HCWs, 70.1% (1,928/2,749) resided in NYC. SARS-CoV-2 seroprevalence in this subset was 32% (616/1,928) (Figure 1). Demographic and comorbid conditions in HCWs who lived in NYC were similar to those of the whole group (Appendix Table 1).

HCWs who underwent voluntary antibody testing (Appendix Table 2) had a higher percentage of persons in the 45-to-64−year age group (43.8% vs 40.9%) and a lower percentage of persons in the 65-to-74−year age group (3.3% vs 5.3%) compared with the group of HCWs that did not undergo testing (P < .001). Gender, race, ethnicity, comorbid conditions, SARS-CoV-2 PCR testing, and work locations were not different between groups. The tested group had higher proportions of clinicians (physicians, nurses, allied HCWs I and II) than the untested nonparticipant group (P = .014).

SARS-CoV-2 PCR Tests on HCWs

More than one-third (34.1%; 938/2,749) of HCWs had a documented nasopharyngeal PCR test between March 23 and June 26, 2020 (Table). Of all PCRs performed, 262 were positive, giving an overall PCR positivity rate of 27.9%. Positivity was 51.4% in March and 36.6% in April. The reasons for PCR testing were not available, but likely represent a combination of exposure-related testing among asymptomatic individuals and diagnostic testing of symptomatic HCWs. In contrast, serology testing was indicative of prior infection and yielded a cumulative seroprevalence at the end of the surge. Findings were similar among HCWs residing in NYC (Appendix Table 1).

Work Location and Job Function

Among all HCWs (Table, Figure 2), there were differences in seropositivity by work location (P = .001). The largest number of HCWs worked in inpatient units (1,348/2,749, 49%), and the second largest in offices (554/2,749, 20%). The highest seropositivity rate was in the EDs, at 36.4% (64/176), followed by radiology suites, at 32.7% (17/52); the seropositivity rate in office locations was 25.8% (143/554). Among HCWs residing in NYC (Appendix Table 1, Appendix Figure 1), the rank order according to proportion seropositive by work location was similar to that of the whole group (P = .004), except that the second highest seropositivity rate was in the inpatient units (33.9% [323/953]). In the group of HCWs residing in NYC, office locations had a seropositivity of 27.4% (102/372). The seropositivity rates for both groups working in office locations were slightly higher than the 22% community seroprevalence in NYC reported for the same period.16

 Proportions Seropositive for SARS-CoV-2 Among All Tested Healthcare Workers by Job Function and Work Location

Among all HCWs, there were differences in seropositivity by job function (P = .001). The greatest proportion of HCWs were allied HCW II (23% [631/2,749]), followed by nurses (22.2% [611/2,749]) and physicians (21.3% [585/2,749] ). Seropositivity was highest for nonclinical staff (44.0% [51/116]), followed by nurses (37.5% [229/611]) and allied clinical HCW I and II (34.5% [143/414] and 32.0% [202/631], respectively). It was lowest for administrative staff (20.9% [42/201]) and pharmacists (11.1% [5/45]). Among HCWs residing in NYC, the rank order according to proportion seropositive by location was similar to that of the whole group. Administrative staff seropositivity was 18.3% (20/109). Administrative staff seropositivity for both groups was marginally lower than the 22% community seroprevalence in NYC for the same period.16

Odds Ratios for SARS-CoV-2 Seropositivity

For all HCWs, in unadjusted models (Appendix Table 3), age 45 to 64 years and Black race were associated with increased odds of being seropositive (1.26; 95% CI, 1.07-1.49 and 2.26; 95% CI, 1.51-3.37, respectively). Increased odds were seen for HCWs working in the ED (1.64; 95% CI, 1.14-2.36) and inpatient units (1.35; 95% CI, 1.08-1.69), and decreased odds were seen for those working in the laboratory and pharmacy (0.47; 95% CI, 0.26-0.86). Increased odds for seropositivity were found for nurses (2.27; 95% CI, 1.56-3.31), allied HCW I (2.00; 95% CI, 1.34-2.97), allied HCW II (1.78; 95% CI, 1.22-2.60), and nonclinical staff (2.97; 95% CI,1.80-4.90).

After adjusting for all covariates, HCWs who were Black remained at increased odds for being seropositive in the two final models (adjusted OR, 2.29; 95% CI, 1.38-3.81 and adjusted OR, 2.94; 95% CI, 1.78-4.85), as did those who had a BMI >30 kg/m2, with an adjusted OR of 1.36 (95% CI, 1.05-1.77) in one of the final models (Appendix Table 3). None of the other comorbid conditions had increased ORs. Those who worked in the ED and inpatient units also remained at increased odds after adjusting for covariates (2.27; 95% CI, 1.53-3.37 and 1.48; 95% CI, 1.14-1.92, respectively; Figure 3). Other job functions that had increased odds for seropositivity were nurses (2.54; 95% CI, 1.64-3.94), allied HCW I (1.83; 95% CI, 1.15-2.89) and II (1.70; 95% CI, 1.10-2.63), and nonclinical staff (2.51; 95% CI, 1.42-4.43).

Association of Job Function and Work Location With Seropositivity Among All Tested Healthcare Workers

Having a positive PCR for SAR-CoV-2 on nasopharyngeal swabs was strongly associated with seropositivity (OR, 47.26; 95% CI, 29.30-76.23 and OR, 44.79; 95% CI, 27.87-72.00) in the two multivariate-adjusted models. These findings were confirmed when the analyses were performed on HCWs who resided in NYC (Appendix Table 4 and Appendix Figure 2).

DISCUSSION

In a large inner-city New York hospital, we report a cumulative SARS-CoV-2 seroprevalence of 30.2% in HCWs at the end of the first surge of SARS-CoV-2 infections in NYC. We identified the highest seropositivity rates for nonclinical staff and nurses, followed by allied HCWs, with the odds of being seropositive ranging from 1.7 to 2.5. The work locations with the highest seroprevalences were the ED and inpatient units, with 2.3-fold and 1.5-fold increased odds of seropositivity, respectively.

Serosurveillance studies have reported the trajectory of community prevalence in NYC over the first wave. A 6.3% prevalence was reported in samples collected between March 23 and April 1, 2020.17 In a study by Rosenberg et al18 with testing performed from April 9 through April 28, 2020, prevalence increased to 22.7%. Serosurveillance data from the NYC Department of Health show prevalence ranging from 20.1% to 23.3% (average 22%) during the study period.16 Compared to the estimated seroprevalence of 9.3% in the United States,19 these rates established NYC as an early epicenter for the COVID-19 pandemic, with our institution’s HCW seroprevalence considerably higher than NYC community serosurveillance rates, 2.2 times higher than reported in the earlier HCW study in the greater NYC area,13 and higher than the 27% rate during May 2020 recently reported in another NYC hospital.20

Data from studies of hospital transmission and effects of mitigation measures, such as a universal masking policy for HCWs and patients, clearly demonstrate the high effectiveness of these measures in reducing hospital transmissions.21,22 This suggests HCW seroprevalence in institutions with well-implemented infection control and universal masking policies may not be a consequence of workplace exposures, but rather may be reflective of community rates.23 Our institution’s response commenced February 3, 2020, with implementation of social distancing, a universal masking policy, transmission-based precautions, and use of fitted N95 masks. Mid-March, elective surgeries were canceled, and inpatient visitation suspended. During the surge, these measures were widely and consistently implemented for all categories of HCWs throughout the work environment, based on emerging guidelines from the Centers for Disease Control and Prevention (CDC) and NYC Department of Health. Our overall observed HCW seroprevalence, well above that of the community, with differences in categories of job function and work locations, is therefore an important finding. Our sample of 2,749 HCWs lived in NYC and its surrounding suburbs and nearby states. There is heterogeneity in community seroprevalence between areas outside of NYC and NYC (an epicenter) itself. We therefore analyzed our data in the subset with NYC zip codes, confirming a similar overall prevalence and increased odds of seropositivity in nurses, allied HCWs, and nonclinical staff.

Physicians and administrative and office staff had seropositivity rates of 18.1%, 20.9%, and 25.8%, respectively, consistent with community rates and illustrating the effectiveness of PPE in the hospital setting. Since PPE use was part of a universal policy applied to all HCWs in our institution, other possible reasons may explain the differences we found. We speculate that the close working relationship nurses have with their patients resulted in a longer duration and higher frequency of daily interactions, increasing the risk for transmission and causing breakthrough infections.24,25 This increased risk is reflected in a study in which 28% of hospitalized patients were nurses and 9% certified nursing assistants.26

The CDC recently redefined close contact with someone with COVID-19 as a cumulative total of >15 minutes over 24 hours.25 Thus, several multiple short periods of exposure can increase risk for infection with SARS-CoV-2; such exposure is characteristic of the job function of nurses, nursing staff, and nonclinical staff. Further, housekeeping, transportation, and security officers are all nonclinical staff with significant and multiple exposures to COVID-19 patients during the surge, and for security officers, to continuous public traffic in and out of the hospital. SARS-CoV-2 spreads by virus shedding in large droplets and aerosols, with droplet nuclei <5 microns in size efficiently dispersed in air, an important additional mode of transmission.27-30 Airborne transmission coupled with virus shedding in asymptomatic and presymptomatic persons, which has been shown to cause secondary attack rates of up to 32%, are other factors that likely contributed to the increased seroprevalence in this group.31 Our observation is consistent with the Birmingham study, which reported the highest rate in housekeeping staff, with a prevalence of 34.5%, compared to 44% in this study.6 Similar reasons for high seropositivity rates apply to the two groups of allied HCWs (eg, medical assistants and patient care technicians, social workers, nutritionists and therapists), whose job functions place them in intermittent but significant proximity with inpatients and outpatients.

Consistent with public health data showing that minorities are disproportionately affected by this disease, we found that Black HCWs were three times more likely to be seropositive.32 However, an unexpected observation was the association between obesity and SARS-CoV-2 seropositivity. A possible explanation for this association may be inability to achieve optimal fit testing for N95 masks, thereby increasing the risk of exposure to droplet nuclei. This is important given that obesity is associated with poorer outcomes from COVID-19.

During the height of the first wave in NYC, EDs and inpatient units handled a large volume of COVID-19 patients with high PCR positivity rates (peak of 51% in March in our hospital). It was not unexpected that we observed increased odds of seropositivity in these work locations. As ICUs were at capacity, inpatient units cared for critically ill patients they would not normally have. HCWs in these locations coped with an increased workload, increased demand on PPE supplies, and work fatigue, which contributed to increased risk for hospital-acquired SARS-CoV-2 infections.

Reporting seroprevalence at a single institution was a limitation of the study. Approximately 57% of the hospital’s total HCW population was tested for antibodies. It is possible their risk profile influenced their decision to volunteer for testing when it became available, introducing selection bias. A comparison between tested and untested HCWs showed similarity in all demographic measures, including nasopharyngeal PCR testing, except for age. We did not have information on symptoms that would prompt PCR testing. HCWs who underwent voluntary testing were younger compared to those who did not undergo testing. Current NYC serosurveillance data showed higher seropositivity in the 45-to-64–year age group (27.8%-28.6%) compared to the 65-to-74–year age group (24.3%), which suggests that the tested group may overestimate seroprevalence among HCWs relative to a randomly selected sample.33 Similarly, there were more nurses, allied HCWs, physicians, and administrative staff in the tested group, with the former two having higher SARS-CoV-2 seropositivity compared to community prevalence, which could also overestimate seroprevalence. Our large sample size provided us with the power to detect differences within several different job functions and work locations, a strength of this study. It was not possible to differentiate community- from hospital-acquired infection in our HCWs, a limitation in many observational HCW seroprevalence studies. However, when we analyzed data restricted only to HCWs in NYC, to reduce the effect of differing community prevalences outside the city, our results were unchanged. Since it is possible that nonclinical HCWs are of a lower socioeconomic status compared to others (nurses and allied HCWs), we cannot exclude the possibility that higher SARS-CoV-2 seroprevalence associated with lower status explains, partly or completely, the increased odds of seropositivity we observed.34 Due to the high proportion of missing data for race (61.3%), we advise caution in interpreting our finding that the odds of seropositivity were three times higher for Black race, even though consistent with prior literature.34 Healthcare organizations have similar job function and work location categories incorporated in their infrastructure, suggesting that our observations may be generalizable to other hospitals in the United States.

CONCLUSION

These findings show that during the first surge in NYC, with its increased burden of disease, hospitalizations, morbidity, and mortality, seroprevalences varied based on job function and work location within this institution. Nurses were at highest risk for SARS-CoV-2 infection, as were those who worked in the ED. In preparation for subsequent waves of SARS-CoV-2 and other highly contagious respiratory infections, major medical centers need to enhance efforts aimed at protecting HCWs, with particular attention to these groups. This study also strongly supports the recent CDC guideline prioritizing HCWs to receive COVID-19 mRNA and adenovirus vector vaccines that have obtained emergency use authorization by the US Food and Drug Administration.35

Acknowledgments

The authors thank all the residents, nurses, and staff of the Department of Family Medicine for their contribution to this work.

References

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8. Stubblefield WB, Talbot HK, Feldstein L, et al. Seroprevalence of SARS-CoV-2 Among frontline healthcare personnel during the first month of caring for COVID-19 patients - Nashville, Tennessee. Clin Infect Dis. 2020. https://doi.org/10.1093/cid/ciaa936
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12. Jeremias A, Nguyen J, Levine J, et al. Prevalence of SARS-CoV-2 infection among health care workers in a tertiary community hospital. JAMA Intern Med. 2020 Aug 11:e204214. https://doi.org/10.1001/jamainternmed.2020.4214
13. Moscola J, Sembajwe G, Jarrett M, et al. Prevalence of SARS-CoV-2 antibodies in health care personnel in the New York City area. JAMA. 2020;324(9):893-895. https://doi.org/10.1001/jama.2020.14765
14. Gonzalez-Reiche AS, Hernandez MM, Sullivan MJ, et al. Introductions and early spread of SARS-CoV-2 in the New York City area. Science. 2020;369(6501):297-301. https://doi.org/10.1126/science.abc1917
15. Lau CS, Hoo SF, Yew SF, et al. Evaluation of the Roche Elecsys Anti-SARS-CoV-2 assay. Preprint. Posted online June 29, 2020. Accessed November 8, 2020. https://www.medrxiv.org/content/10.1101/2020.06.28.20142232v1 https://doi.org/10.1101/2020.06.28.20142232
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References

1. Liu YC, Kuo RL, Shih SR. COVID-19: The first documented coronavirus pandemic in history. Biomed J. 2020;43(4):328-333. https://doi.org/10.1016/j.bj.2020.04.007
2. World Health Organization. WHO coronavirus disease (COVID-19) dashboard. Accessed April 12, 2021. https://covid19.who.int
3. Nguyen LH, Drew DA, Graham MS, et al. Risk of COVID-19 among front-line health-care workers and the general community: a prospective cohort study. Lancet Public Health. 2020;5(9):e475-e483. https://doi.org/10.1016/S2468-2667(20)30164-X
4. Gupta S, Federman DG. Hospital preparedness for COVID-19 pandemic: experience from department of medicine at Veterans Affairs Connecticut Healthcare System. Postgrad Med. 2020:1-6. https://doi.org/10.1080/00325481.2020.1761668
5. Woolley K, Smith R, Arumugam S. Personal protective equipment (PPE) guidelines, adaptations and lessons during the COVID-19 pandemic. Ethics Med Public Health. 2020;14:100546. https://doi.org/10.1016/j.jemep.2020.100546
6. Shields A, Faustini SE, Perez-Toledo M, et al. SARS-CoV-2 seroprevalence and asymptomatic viral carriage in healthcare workers: a cross-sectional study. Thorax. 2020;75(12):1089-1094. https://doi.org/10.1136/thoraxjnl-2020-215414
7. Steensels D, Oris E, Coninx L, et al. Hospital-wide SARS-CoV-2 antibody screening in 3056 staff in a tertiary center in Belgium. JAMA. 2020;324(2):195-197. https://doi.org/10.1001/jama.2020.11160
8. Stubblefield WB, Talbot HK, Feldstein L, et al. Seroprevalence of SARS-CoV-2 Among frontline healthcare personnel during the first month of caring for COVID-19 patients - Nashville, Tennessee. Clin Infect Dis. 2020. https://doi.org/10.1093/cid/ciaa936
9. Korth J, Wilde B, Dolff S, et al. SARS-CoV-2-specific antibody detection in healthcare workers in Germany with direct contact to COVID-19 patients. J Clin Virol. 2020;128:104437. https://doi.org/10.1016/j.jcv.2020.104437
10. Keeley AJ, Evans C, Colton H, et al. Roll-out of SARS-CoV-2 testing for healthcare workers at a large NHS Foundation Trust in the United Kingdom, March 2020. Euro Surveill. 2020;25(14). https://doi.org/10.2807/1560-7917.ES.2020.25.14.2000433
11. Self WH, Tenforde MW, Stubblefield WB, et al. Seroprevalence of SARS-CoV-2 among frontline health care personnel in a multistate hospital network - 13 academic medical centers, April-June 2020. MMWR Morb Mortal Wkly Rep. 2020;69(35):1221-1226. https://doi.org/10.15585/mmwr.mm6935e2
12. Jeremias A, Nguyen J, Levine J, et al. Prevalence of SARS-CoV-2 infection among health care workers in a tertiary community hospital. JAMA Intern Med. 2020 Aug 11:e204214. https://doi.org/10.1001/jamainternmed.2020.4214
13. Moscola J, Sembajwe G, Jarrett M, et al. Prevalence of SARS-CoV-2 antibodies in health care personnel in the New York City area. JAMA. 2020;324(9):893-895. https://doi.org/10.1001/jama.2020.14765
14. Gonzalez-Reiche AS, Hernandez MM, Sullivan MJ, et al. Introductions and early spread of SARS-CoV-2 in the New York City area. Science. 2020;369(6501):297-301. https://doi.org/10.1126/science.abc1917
15. Lau CS, Hoo SF, Yew SF, et al. Evaluation of the Roche Elecsys Anti-SARS-CoV-2 assay. Preprint. Posted online June 29, 2020. Accessed November 8, 2020. https://www.medrxiv.org/content/10.1101/2020.06.28.20142232v1 https://doi.org/10.1101/2020.06.28.20142232
16. New York City Department of Health. Covid-19: data. long-term trends. Antibody testing. Accessed March 5, 2021. https://www1.nyc.gov/site/doh/covid/covid-19-data-trends.page#antibody
17. Havers FP, Reed C, Lim T, et al. Seroprevalence of antibodies to SARS-CoV-2 in 10 sites in the United States, March 23-May 12, 2020. JAMA Intern Med. Published online July 21, 2020. https://doi.org/10.1001/jamainternmed.2020.4130
18. Rosenberg ES, Tesoriero JM, Rosenthal EM, et al. Cumulative incidence and diagnosis of SARS-CoV-2 infection in New York. Ann Epidemiol. Aug 2020;48:23-29 e4. https://doi.org/10.1016/j.annepidem.2020.06.004
19. Anand S, Montez-Rath M, Han J, et al. Prevalence of SARS-CoV-2 antibodies in a large nationwide sample of patients on dialysis in the USA: a cross-sectional study. Lancet. 2020;396(10259):1335-1344. https://doi.org/10.1016/S0140-6736(20)32009-2
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Journal of Hospital Medicine 16(5)
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Journal of Hospital Medicine 16(5)
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282-289. Published Online First April 20, 2021
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282-289. Published Online First April 20, 2021
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SARS-CoV-2 Seroprevalence Among Healthcare Workers by Job Function and Work Location in a New York Inner-City Hospital
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Murli U Purswani, MD; Email: [email protected]; Telephone: 718-960-1010. Twitter: @purswani_murli.
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