Almost half of Crohn disease (CD) patients experience a dermatologic manifestation of the disease. A rare entity, metastatic CD (MCD) presents a diagnostic challenge without a high index of suspicion. Its etiology is not well defined; however, it appears to be an autoimmune response to gut antigens. Herein, we review the etiology/epidemiology, diagnostic criteria, and treatment for this uncommon condition.

Epidemiology and Clinical Characteristics of MCD

Metastatic CD was first described by Parks et al1 in 1965 and refers to a diverse collection of macroscopic dermatologic manifestations in tissue not contiguous with the gastrointestinal (GI) tract. To be classified as MCD, the tissue must demonstrate characteristic histopathologic findings, which invariably include noncaseating granulomas.

Crohn disease may affect any part of the GI tract from the mouth to anus, with a multitude of associated cutaneous manifestations having been described. The terminal ileum is the most commonly affected portion of the GI tract in CD, but the large intestine also may be involved in 55% to 80% of cases.² The incidence of non-MCD-associated anal lesions seems to correlate with intestinal involvement in that as few as 25% of patients with ileal-localized CD have anal lesions compared to nearly 80% of patients with large intestinal involvement.³

It has been estimated that 18% to 44% of patients with CD have some form of cutaneous manifestation,⁴ with MCD being a rare subcategory. As few as 100 cases have been described from 1965 to the present.⁵ The presence of MCD does not correlate well with severity of intestinal CD, and although a majority of MCD cases present after at least 6 months of GI symptoms,⁶ there are instances in which MCD presents without prior or existing evidence of intestinal CD.⁷

With regard to MCD, the term metastatic is sometimes supplanted in the literature by cutaneous to avoid any implication of cancer; however, due to a myriad of dermatologic manifestations, both terms can cause confusion. The categorization of the various types of cutaneous findings in CD is well summarized in a review by Palamaras et al8 with the following classifications: (1) granulomatous by direct extension (oral or perianal), (2) MCD lesions (genital and nongenital), (3) immune-related lesions, and (4) lesions from nutritional deficiencies. Of the cutaneous manifestations relating to CD, MCD is the least common cutaneous categorical manifestation and is further divided into subcategories of genital and nongenital lesions.⁸

The nongenital distribution of MCD is the more common variety in adults and particularly seems to affect the legs and plantar surfaces (38%), the trunk and abdomen (24%), and the face (15%).^5,9 These nongenital MCD manifestations are most commonly described as nodules, ulcerations, or erythematous to purple plaques, and less commonly described as abscesses, pustules, or papules.

The sequence of cutaneous symptoms of MCD relative to intestinal disease depends to some degree on patient age. In adults diagnosed with MCD, it has been noted that a GI flare is expected 2 months to 4 years after diagnosis; however, in children the subsequent GI flare has been noted to vary more widely from 9 months to 14 years following presentation of MCD.⁸ Furthermore, roughly 50% of children diagnosed with MCD present concomitantly with their first symptoms of a GI flare, whereas 70% of adults with MCD had been previously diagnosed with intestinal CD.⁸ In one review of 80 reported cases of MCD, 20% (16/80) had no symptoms of intestinal disease at the time of MCD diagnosis, and the majority of the asymptomatic cases were in children; interestingly, the majority of these same children were diagnosed with CD months to years later.⁹

Both the location and characteristics of cutaneous findings in MCD correlate with age.⁹ Metastatic CD has been identified in all age groups; however, lymphedema is more common in children/young adults, while nodules, ulceration, and fistulating disease are more often seen in adults.¹⁰ Affected children and adolescents with MCD range from 5 to 17 years of age, with a mean age at disease onset of 11.1 years and equal incidence in males and females.⁸ Adults with MCD range from 18 to 78 years of age, with a mean age at presentation of 38.4 years.^8,11

Concerning anatomic location of disease, adults with MCD most commonly have nodules with or without plaques on the arms and legs and less commonly in the genital area.⁸ In contrast, children with MCD are more prone to genital lesions, with up to 85% of cases including some degree of genital erythematous or nonerythematous swelling with or without induration.⁸ Genitourinary complications of CD as a broad category, however, are estimated to occur in only 5% to 20% of intestinal CD cases in both children and adults.¹²

There have been conflicting reports regarding gender predilection in MCD. Based on a review by Samitz et al¹³ of 200 cases of CD over an 18-year period, 22% of patients with CD were found to have cutaneous manifestations--presumably not MCD but rather perianal, perineal, vulvar fistulae, fissures, or abscesses--with a male to female preponderance of almost 2 to 1. A more recent review of the literature by Palamaras et al⁸ in 2008 reported that contiguous non-MCD affects adult females and children more often than adult males, with 63% adult cases being female. This review seems to be more congruent with other reports in the literature implicating that females are twice as commonly affected by MCD than males.^9,14

Pathophysiology

The etiology of MCD has not been well defined. One proposed mechanism of the distal tissue involvement of MCD is through passage of antigens to the skin with subsequent granulomatous response at the level of the dermis.¹⁰ Another proposed mechanism suggests antibody sensitization to gut antigens, possibly bacterial antigens, that then coincidentally cross-react with analogous skin antigens.^8,14 Burgdorf¹¹ supported this notion in a 1981 report in which it was suggested that the granulomatous reaction was related to deposition of immune complexes in the skin. Slater et al¹⁵ and Tatnall et al¹⁶ offered a variation of Burgdorf's notion, suggesting that it was sensitized T cells to circulating antigens that were the initiators of granuloma formation in the periphery.

An examination of MCD tissue in 1990 by Shum and Guenther¹⁷ under electron microscopy and immunofluorescence provided evidence against prior studies that purported to have identified immune complexes as the causative agents of MCD. In this study, the authors found no evidence of immune complexes in the dermis of MCD lesions. In addition, an attempt to react serum antibodies of a patient with MCD, which were postulated to have IgG, IgM, and IgA antibodies to specific gut antigens, yielded no response when reacted with the tongue, ileum, and colon tissue from a rat. As a culminant finding, the authors also noted MCD dermis tissue with granulomas without vasculitis, suggesting a T-cell mediated type IV hypersensitivity response with a secondary vasculitis from T-cell origin lymphokines and T-cell mediated monocyte activation.¹⁷

Research implicating other immunologic entities involved in the pathophysiology of CD such as β-2 integrin,¹⁸ CD14⁺ monocytes,¹⁹ and the role of the DNA repair gene MLH1 (mutL homolog 1)²⁰ have been considered but without a clearly definitive role in the manifestations of MCD.

The utility of metronidazole in the treatment of MCD has been suggested as evidence that certain bacteria in the gut may either serve as the causative antigen or may induce its formation²¹; however, the causative antigen has yet to be identified, and whether it travels distally to the skin or merely resembles a similar antigen normally present in the dermis has not yet been determined. Some research has used in situ polymerase chain reaction techniques to attempt to detect similar microbial pathogens in both the vasculature of active bowel lesions and in the skin, but to date, bacterial RNA noted to be present in the gut vasculature adjacent to CD lesions has not been detected in skin lesions.²²

Diagnosis

Physical Findings

Overall, it is estimated that roughly 56% of all MCD cases affect the external genitalia.²³ The classic appearance of MCD includes well-demarcated ulcerations in the areas of intertriginous skin folds with or without diffuse edema and tenderness to palpation.²³ Although MCD has been historically noted as having a predilection for moist skin folds, there are numerous case reports of MCD all over the body, including the face,^7,24-29 retroauricular areas,³⁰ arms and legs,^16,17,31-34 lower abdomen,^3,5 under the breasts,¹ perineum,³⁵ external genitalia,^1,9,36-40 and even the lungs⁴¹ and bladder.⁴²

As a dermatologic disease, MCD has been referred to as yet another great imitator, both on the macroscopic and microscopic levels.⁸ As such, more common causes of genital edema should be considered first and investigated based on the patient's history, physical examination, skin biopsy, lymphangiogram, ultrasound, and cystogram.⁴³ Ultrasonography and color Doppler sonography have been shown to be helpful in patients with genital involvement. This modality can evaluate not only the presence of normal testes but also intratesticular and scrotal wall fluid, especially when the physical examination reveals swelling that makes testicle palpation more difficult.⁶ Clinically, the correct diagnosis of MCD often is made through suspicion of inflammatory bowel disease based on classic symptoms and/or physical findings including abdominal pain, weight loss, bloody stool, diarrhea, perianal skin tags, and anal fissures or fistulas. Any of these GI findings should prompt an intestinal biopsy to rule out any histologic evidence of CD.

Metastatic CD affecting the vulva often presents with vulvar pain and pruritus and may clinically mimic a more benign disease such as balanitis plasmacellularis, also referred to as Zoon vulvitis.²³ Similar to MCD on any given body surface, there is dramatic variation in the macroscopic presentation of vulvar MCD, with physical examination findings ranging from bilateral diffuse, edematous, deeply macerated, red, ulcerated lesions over the vulva with lymphadenopathy to findings of bilateral vulvar pain with yellow drainage from the labia majora.²³ There have been cases of vulvar MCD that include exquisite vulvar pain but without structural abnormalities including normal uterus, cervix, adnexa, rectovaginal septum, and rectum. In these more nebulous cases of vulvar MCD, the diagnosis often is discovered incidentally when nonspecific diagnostic imaging suggests underlying CD.²³

Beyond the case-by-case variations on physical examination, the great difficulty in diagnosis, particularly in children, occurs in the absence of any GI symptoms and therefore no logical consideration of underlying CD. Consequently, there have been cases of children presenting with irritation of the vulva who were eventually diagnosed with MCD only after erroneous treatment of contact dermatitis, candidiasis, and even consideration of sexual abuse.³⁷ Because it is so rare and obscure among practicing clinicians, the diagnosis of MCD often is considered only after irritation or swelling of the external genitalia has not responded to standard therapies. If and when the diagnosis of MCD is considered in children, it has been suggested to screen patients for anorectal stricture, as case studies have found the condition to be relatively common in this subpopulation.⁴⁴

In the less common case of adults with genitourinary symptoms that suggest possible MCD, the differential diagnosis for penile or vaginal ulcers should include contact and irritant dermatitis, chronic infectious lesions (eg, hidradenitis suppurativa, actinomycosis, tuberculosis),⁴⁵ sexually transmitted ulcerative diseases (eg, chancroid, lymphogranuloma venereum, herpes genitalia, granuloma inguinale),⁴⁶ drug reactions, and even extramammary Paget disease.⁴⁷

Histologic Findings

Because MCD has so much macroscopic variation and can present anywhere on the surface of the body, formal diagnosis relies on microscopy. As an added measure of difficulty in diagnosis, one random biopsy of a suspicious segment of tissue may not contain the expected histologic findings; therefore, clinical suspicion may warrant a second biopsy.¹⁰ There have been reported cases of an adult patient without history of CD presenting with a lesion that resembled a more common pathology, such as a genital wart, and the correct diagnosis of MCD with pseudocondylomatous morphology was made only after intestinal manifestations prompted the clinician to consider such an unusual diagnosis.⁴⁸

From a histopathologic perspective, MCD is characterized by discrete, noncaseating, sarcoidlike granulomas with abundant multinucleated giant cells (Langhans giant cells) in the superficial dermis (papillary), deep dermis (reticular), and adipose tissue (Figure).^8,17 In the presence of concomitant intestinal disease, the granulomas of both the intestinal and dermal tissues should share the same microscopic characteristics.⁸ In addition, copious neutrophils and granulomas surrounding the microvasculature have been described,³⁴ as well as general lymphocyte and plasma cell infiltrate.⁴⁵ Some histologic samples have included collagen degeneration termed necrobiosis in the middle dermal layer as another variable finding in MCD.^14,34

On microscopy, it has been reported that use of Verhoeff-van Gieson staining may be helpful to highlight the presence of neutrophil obstruction within the dermal vasculature, particularly the arterial lumen, as well as to aid in highlighting swelling of the endothelium with fragmentation of the internal elastic lamina.¹⁷ Although not part of the routine diagnosis, electron microscopy of MCD tissue samples have confirmed hypertrophy of the endothelial cells composing the capillaries with resulting extravasation of fibrin, red blood cells, lymphocytes, and epithelioid histiocytes.¹⁷ Observation of tissue under direct immunofluorescence has been less helpful, as it has shown only nonspecific fibrinogen deposition within the dermis and dermal vessels.¹⁷

In an article on treatment of MCD, Escher et al⁴³ reinforced that the macroscopic findings of MCD are diverse, and the microscopic findings characteristic of MCD also can be mimicked by other etiologies such as sarcoidosis, tuberculosis, fungal infections, lymphogranuloma venereum, leishmaniasis, and connective tissue disorders.⁴³ As such, the workup to rule out infectious, anatomic, and autoimmune etiologies should be diverse. Often, the workup for MCD will include special stains such as Ziehl-Neelsen stain to rule out Mycobacterium tuberculosis and acid-fast bacilli and Fite stain to consider atypical mycobacteria. Other tests such as tissue culture, chest radiograph, tuberculin skin test (Mantoux test), IFN-γ release assay, or polarized light microscopy may rule out infectious etiologies.^9,49 Serologic testing might include VDRL test, Treponema pallidum hemagglutination assay, hepatitis B, hepatitis C, and human immunodeficiency virus.⁵

Crohn disease is characterized histologically by sarcoidlike noncaseating granulomas, and as such, it is important to differentiate MCD from sarcoidosis prior to histologic analysis. Sarcoidosis also can be considered much less likely with a normal chest radiograph and in the absence of increased serum calcium and angiotensin-converting enzyme levels.⁷ The differentiation of sarcoidosis from MCD on the microscopic scale is subtle but is sometimes facilitated in the presence of an ulcerated epidermis or lymphocytic/eosinophilic infiltrate and edema within the dermis, all suggestive of MCD.¹⁴

Metastatic CD also should be differentiated from erythema nodosum and pyoderma gangrenosum, which are among the most common cutaneous findings associated with CD.¹⁴ Pyoderma gangrenosum can be distinguished histologically by identifying copious neutrophilic infiltrate with pseudoepitheliomatous hyperplasia.⁵⁰

Treatment

Because MCD is relatively rare, there are no known randomized trials suggesting a particular medical or surgical treatment. In a review of perineal MCD from 2007, the 40-year-old recommendation by Moutain³ opting for surgical debridement versus medical management still resonates, particularly for perineal disease, as an effective measure in all but the mildest of presentations.⁵¹ However, recent case reports also suggest that the tumor necrosis factor α (TNF-α) inhibitors such as infliximab and adalimumab should be considered prior to surgery even with severe perineal MCD.⁵¹ Moreover, even if medical management with TNF-α inhibitors or some combination of immunosuppressants and antibiotics does not eradicate the disease, it often helps reduce the size of the ulcers prior to surgery.⁵² With a limited understanding of MCD, one might think that removal of the affected bowel would eliminate cutaneous disease, but it has been shown that this strategy is not effective.^53,54

The composition and location of the particular lesion affects the trajectory of treatment. For example, MCD manifesting as local ulcers and plaques has been described as responding well to topical and intralesional steroids.^10,55,56 In the case of penile swelling and/or phimosis, circumcision has been helpful to improve the patient's ability to void as well as to attain and maintain erection.¹⁰ In the case of scrotal swelling secondary to MCD, early treatment (ie, within 4 to 6 months) with oral steroids and/or metronidazole is likely beneficial to prevent refractory edematous organization of the tissue.⁵⁷

As a general rule, an effective treatment will include a combination of an immunosuppressant, antibiotic therapy, and sometimes surgery. The most commonly used immunosuppressant agents include topical or intralesional steroids, infliximab,^43,58 cyclosporine A,^59,60 dapsone, minocycline, thalidomide, methotrexate, mycophenolate mofetil, sulfasalazine, azathioprine, tacrolimus, and 6-mercaptopurine.⁴ Steroids have been the conventional treatment of extraintestinal manifestations of CD⁶¹; however, perineal CD has been poorly controlled with systemic steroids.⁶² If steroids are found not to be effective, sometimes agents such as dapsone or thalidomide are considered. One case report noted stabilization of MCD penile ulcers with oral thalidomide 300 mg once daily, oral minocycline 100 mg once daily, and topical tacrolimus 0.3% with benzocaine twice daily with continuation of prednisolone and methotrexate as parts of previously unsuccessful regimen.⁵²

Metronidazole is perhaps the most commonly used antibiotic, having been a component of many successful regimens.^4,63 For example, a 27-year-old patient with MCD presenting as a nonhealing ulcerative lesion in the subcoronal area of the penis and scrotum was treated successfully with a 6-month course of mesalamine, prednisone, and metronidazole.⁴⁵ Another case report of vulvar MCD reported initial success with intravenous methylprednisolone, ciprofloxacin, and metronidazole.²³ The primary limitation of metronidazole is that subsequent tapering of the dose seems to result in recurrence of disease.⁶⁴ Consequently, patients must remain on the antibiotic for an indeterminate course, with dosages ranging from 5 mg/kg daily in adolescents⁶⁵ to 1000 to 1500 mg daily in adults.⁶⁶

Of the various immunosuppressants available, infliximab has been listed in numerous reports as a successful agent in both the induction and maintenance of extraintestinal manifestations of CD including MCD.^67-71 Infliximab has been reported to be effective in the treatment of penile and scrotal edema secondary to MCD that did not respond to other immunosuppressants including oral prednisolone, azathioprine, and cyclosporine.⁴³ Infliximab may be a good option to help heal draining fistulas, particularly in combination with an antibiotic such as metronidazole and ciprofloxacin, which helps to prevent abscess formation during healing.⁷² The response to infliximab has been dramatic, with resolution of cutaneous lesions after just 6 weeks in some cases.⁷³ The dosing regimen of infliximab has been suggested at 5 mg/kg administered at 0, 2, and 6 weeks, with subsequent maintenance infusions every 10 weeks,⁷⁰ or at 0, 4, and 12 weeks, with subsequent infusions every 8 weeks.⁴³

Adalimumab may be considered as an alternative to infliximab and is potentially less allergenic as a fully humanized monoclonal antibody to TNF-α, which also has been used successfully to both induce and maintain remission of moderate to severe CD.^42,74,75 Proposed dosing of adalimumab includes a loading dose of 160 mg subcutaneously on day 1, followed by an 80-mg dose 2 weeks later and a 40-mg maintenance dose every other week indefinitely.⁴⁸ Of note, adalimumab has been noted in the literature to have many potential side effects, including one particular case in which severe headaches were attributed to its use.⁵⁹ As a consequence of the headaches, the patient was switched from adalimumab to cyclosporine and responded well with no subsequent flare-ups on follow-up.

In summary, treatment of MCD depends on cutaneous location, severity, physician experience with certain antibiotics or immunosuppressants, availability of medication, and patient disposition. It seems reasonable to attempt medical management with one or more medical regimens before committing to surgical intervention. Furthermore, even with debridement, curettage, skin graft, or other surgical strategy, the patient is likely to require some period of immunosuppression to provide long-lasting remission.

Conclusion

Patients with inflammatory bowel disease often develop dermatologic sequelae, with MCD being a rare but serious process. Patients may present with a wide array of physical concerns and symptoms, many resembling other disease processes. As such, education and a high index of suspicion are needed for proper diagnosis and treatment.

Almost half of Crohn disease (CD) patients experience a dermatologic manifestation of the disease. A rare entity, metastatic CD (MCD) presents a diagnostic challenge without a high index of suspicion. Its etiology is not well defined; however, it appears to be an autoimmune response to gut antigens. Herein, we review the etiology/epidemiology, diagnostic criteria, and treatment for this uncommon condition.

Epidemiology and Clinical Characteristics of MCD

Metastatic CD was first described by Parks et al1 in 1965 and refers to a diverse collection of macroscopic dermatologic manifestations in tissue not contiguous with the gastrointestinal (GI) tract. To be classified as MCD, the tissue must demonstrate characteristic histopathologic findings, which invariably include noncaseating granulomas.

Crohn disease may affect any part of the GI tract from the mouth to anus, with a multitude of associated cutaneous manifestations having been described. The terminal ileum is the most commonly affected portion of the GI tract in CD, but the large intestine also may be involved in 55% to 80% of cases.² The incidence of non-MCD-associated anal lesions seems to correlate with intestinal involvement in that as few as 25% of patients with ileal-localized CD have anal lesions compared to nearly 80% of patients with large intestinal involvement.³

It has been estimated that 18% to 44% of patients with CD have some form of cutaneous manifestation,⁴ with MCD being a rare subcategory. As few as 100 cases have been described from 1965 to the present.⁵ The presence of MCD does not correlate well with severity of intestinal CD, and although a majority of MCD cases present after at least 6 months of GI symptoms,⁶ there are instances in which MCD presents without prior or existing evidence of intestinal CD.⁷

With regard to MCD, the term metastatic is sometimes supplanted in the literature by cutaneous to avoid any implication of cancer; however, due to a myriad of dermatologic manifestations, both terms can cause confusion. The categorization of the various types of cutaneous findings in CD is well summarized in a review by Palamaras et al8 with the following classifications: (1) granulomatous by direct extension (oral or perianal), (2) MCD lesions (genital and nongenital), (3) immune-related lesions, and (4) lesions from nutritional deficiencies. Of the cutaneous manifestations relating to CD, MCD is the least common cutaneous categorical manifestation and is further divided into subcategories of genital and nongenital lesions.⁸

The nongenital distribution of MCD is the more common variety in adults and particularly seems to affect the legs and plantar surfaces (38%), the trunk and abdomen (24%), and the face (15%).^5,9 These nongenital MCD manifestations are most commonly described as nodules, ulcerations, or erythematous to purple plaques, and less commonly described as abscesses, pustules, or papules.

The sequence of cutaneous symptoms of MCD relative to intestinal disease depends to some degree on patient age. In adults diagnosed with MCD, it has been noted that a GI flare is expected 2 months to 4 years after diagnosis; however, in children the subsequent GI flare has been noted to vary more widely from 9 months to 14 years following presentation of MCD.⁸ Furthermore, roughly 50% of children diagnosed with MCD present concomitantly with their first symptoms of a GI flare, whereas 70% of adults with MCD had been previously diagnosed with intestinal CD.⁸ In one review of 80 reported cases of MCD, 20% (16/80) had no symptoms of intestinal disease at the time of MCD diagnosis, and the majority of the asymptomatic cases were in children; interestingly, the majority of these same children were diagnosed with CD months to years later.⁹

Both the location and characteristics of cutaneous findings in MCD correlate with age.⁹ Metastatic CD has been identified in all age groups; however, lymphedema is more common in children/young adults, while nodules, ulceration, and fistulating disease are more often seen in adults.¹⁰ Affected children and adolescents with MCD range from 5 to 17 years of age, with a mean age at disease onset of 11.1 years and equal incidence in males and females.⁸ Adults with MCD range from 18 to 78 years of age, with a mean age at presentation of 38.4 years.^8,11

Concerning anatomic location of disease, adults with MCD most commonly have nodules with or without plaques on the arms and legs and less commonly in the genital area.⁸ In contrast, children with MCD are more prone to genital lesions, with up to 85% of cases including some degree of genital erythematous or nonerythematous swelling with or without induration.⁸ Genitourinary complications of CD as a broad category, however, are estimated to occur in only 5% to 20% of intestinal CD cases in both children and adults.¹²

There have been conflicting reports regarding gender predilection in MCD. Based on a review by Samitz et al¹³ of 200 cases of CD over an 18-year period, 22% of patients with CD were found to have cutaneous manifestations--presumably not MCD but rather perianal, perineal, vulvar fistulae, fissures, or abscesses--with a male to female preponderance of almost 2 to 1. A more recent review of the literature by Palamaras et al⁸ in 2008 reported that contiguous non-MCD affects adult females and children more often than adult males, with 63% adult cases being female. This review seems to be more congruent with other reports in the literature implicating that females are twice as commonly affected by MCD than males.^9,14

Pathophysiology

The etiology of MCD has not been well defined. One proposed mechanism of the distal tissue involvement of MCD is through passage of antigens to the skin with subsequent granulomatous response at the level of the dermis.¹⁰ Another proposed mechanism suggests antibody sensitization to gut antigens, possibly bacterial antigens, that then coincidentally cross-react with analogous skin antigens.^8,14 Burgdorf¹¹ supported this notion in a 1981 report in which it was suggested that the granulomatous reaction was related to deposition of immune complexes in the skin. Slater et al¹⁵ and Tatnall et al¹⁶ offered a variation of Burgdorf's notion, suggesting that it was sensitized T cells to circulating antigens that were the initiators of granuloma formation in the periphery.

An examination of MCD tissue in 1990 by Shum and Guenther¹⁷ under electron microscopy and immunofluorescence provided evidence against prior studies that purported to have identified immune complexes as the causative agents of MCD. In this study, the authors found no evidence of immune complexes in the dermis of MCD lesions. In addition, an attempt to react serum antibodies of a patient with MCD, which were postulated to have IgG, IgM, and IgA antibodies to specific gut antigens, yielded no response when reacted with the tongue, ileum, and colon tissue from a rat. As a culminant finding, the authors also noted MCD dermis tissue with granulomas without vasculitis, suggesting a T-cell mediated type IV hypersensitivity response with a secondary vasculitis from T-cell origin lymphokines and T-cell mediated monocyte activation.¹⁷

Research implicating other immunologic entities involved in the pathophysiology of CD such as β-2 integrin,¹⁸ CD14⁺ monocytes,¹⁹ and the role of the DNA repair gene MLH1 (mutL homolog 1)²⁰ have been considered but without a clearly definitive role in the manifestations of MCD.

The utility of metronidazole in the treatment of MCD has been suggested as evidence that certain bacteria in the gut may either serve as the causative antigen or may induce its formation²¹; however, the causative antigen has yet to be identified, and whether it travels distally to the skin or merely resembles a similar antigen normally present in the dermis has not yet been determined. Some research has used in situ polymerase chain reaction techniques to attempt to detect similar microbial pathogens in both the vasculature of active bowel lesions and in the skin, but to date, bacterial RNA noted to be present in the gut vasculature adjacent to CD lesions has not been detected in skin lesions.²²

Diagnosis

Physical Findings

Overall, it is estimated that roughly 56% of all MCD cases affect the external genitalia.²³ The classic appearance of MCD includes well-demarcated ulcerations in the areas of intertriginous skin folds with or without diffuse edema and tenderness to palpation.²³ Although MCD has been historically noted as having a predilection for moist skin folds, there are numerous case reports of MCD all over the body, including the face,^7,24-29 retroauricular areas,³⁰ arms and legs,^16,17,31-34 lower abdomen,^3,5 under the breasts,¹ perineum,³⁵ external genitalia,^1,9,36-40 and even the lungs⁴¹ and bladder.⁴²

As a dermatologic disease, MCD has been referred to as yet another great imitator, both on the macroscopic and microscopic levels.⁸ As such, more common causes of genital edema should be considered first and investigated based on the patient's history, physical examination, skin biopsy, lymphangiogram, ultrasound, and cystogram.⁴³ Ultrasonography and color Doppler sonography have been shown to be helpful in patients with genital involvement. This modality can evaluate not only the presence of normal testes but also intratesticular and scrotal wall fluid, especially when the physical examination reveals swelling that makes testicle palpation more difficult.⁶ Clinically, the correct diagnosis of MCD often is made through suspicion of inflammatory bowel disease based on classic symptoms and/or physical findings including abdominal pain, weight loss, bloody stool, diarrhea, perianal skin tags, and anal fissures or fistulas. Any of these GI findings should prompt an intestinal biopsy to rule out any histologic evidence of CD.

Metastatic CD affecting the vulva often presents with vulvar pain and pruritus and may clinically mimic a more benign disease such as balanitis plasmacellularis, also referred to as Zoon vulvitis.²³ Similar to MCD on any given body surface, there is dramatic variation in the macroscopic presentation of vulvar MCD, with physical examination findings ranging from bilateral diffuse, edematous, deeply macerated, red, ulcerated lesions over the vulva with lymphadenopathy to findings of bilateral vulvar pain with yellow drainage from the labia majora.²³ There have been cases of vulvar MCD that include exquisite vulvar pain but without structural abnormalities including normal uterus, cervix, adnexa, rectovaginal septum, and rectum. In these more nebulous cases of vulvar MCD, the diagnosis often is discovered incidentally when nonspecific diagnostic imaging suggests underlying CD.²³

Beyond the case-by-case variations on physical examination, the great difficulty in diagnosis, particularly in children, occurs in the absence of any GI symptoms and therefore no logical consideration of underlying CD. Consequently, there have been cases of children presenting with irritation of the vulva who were eventually diagnosed with MCD only after erroneous treatment of contact dermatitis, candidiasis, and even consideration of sexual abuse.³⁷ Because it is so rare and obscure among practicing clinicians, the diagnosis of MCD often is considered only after irritation or swelling of the external genitalia has not responded to standard therapies. If and when the diagnosis of MCD is considered in children, it has been suggested to screen patients for anorectal stricture, as case studies have found the condition to be relatively common in this subpopulation.⁴⁴

In the less common case of adults with genitourinary symptoms that suggest possible MCD, the differential diagnosis for penile or vaginal ulcers should include contact and irritant dermatitis, chronic infectious lesions (eg, hidradenitis suppurativa, actinomycosis, tuberculosis),⁴⁵ sexually transmitted ulcerative diseases (eg, chancroid, lymphogranuloma venereum, herpes genitalia, granuloma inguinale),⁴⁶ drug reactions, and even extramammary Paget disease.⁴⁷

Histologic Findings

Because MCD has so much macroscopic variation and can present anywhere on the surface of the body, formal diagnosis relies on microscopy. As an added measure of difficulty in diagnosis, one random biopsy of a suspicious segment of tissue may not contain the expected histologic findings; therefore, clinical suspicion may warrant a second biopsy.¹⁰ There have been reported cases of an adult patient without history of CD presenting with a lesion that resembled a more common pathology, such as a genital wart, and the correct diagnosis of MCD with pseudocondylomatous morphology was made only after intestinal manifestations prompted the clinician to consider such an unusual diagnosis.⁴⁸

From a histopathologic perspective, MCD is characterized by discrete, noncaseating, sarcoidlike granulomas with abundant multinucleated giant cells (Langhans giant cells) in the superficial dermis (papillary), deep dermis (reticular), and adipose tissue (Figure).^8,17 In the presence of concomitant intestinal disease, the granulomas of both the intestinal and dermal tissues should share the same microscopic characteristics.⁸ In addition, copious neutrophils and granulomas surrounding the microvasculature have been described,³⁴ as well as general lymphocyte and plasma cell infiltrate.⁴⁵ Some histologic samples have included collagen degeneration termed necrobiosis in the middle dermal layer as another variable finding in MCD.^14,34

On microscopy, it has been reported that use of Verhoeff-van Gieson staining may be helpful to highlight the presence of neutrophil obstruction within the dermal vasculature, particularly the arterial lumen, as well as to aid in highlighting swelling of the endothelium with fragmentation of the internal elastic lamina.¹⁷ Although not part of the routine diagnosis, electron microscopy of MCD tissue samples have confirmed hypertrophy of the endothelial cells composing the capillaries with resulting extravasation of fibrin, red blood cells, lymphocytes, and epithelioid histiocytes.¹⁷ Observation of tissue under direct immunofluorescence has been less helpful, as it has shown only nonspecific fibrinogen deposition within the dermis and dermal vessels.¹⁷

In an article on treatment of MCD, Escher et al⁴³ reinforced that the macroscopic findings of MCD are diverse, and the microscopic findings characteristic of MCD also can be mimicked by other etiologies such as sarcoidosis, tuberculosis, fungal infections, lymphogranuloma venereum, leishmaniasis, and connective tissue disorders.⁴³ As such, the workup to rule out infectious, anatomic, and autoimmune etiologies should be diverse. Often, the workup for MCD will include special stains such as Ziehl-Neelsen stain to rule out Mycobacterium tuberculosis and acid-fast bacilli and Fite stain to consider atypical mycobacteria. Other tests such as tissue culture, chest radiograph, tuberculin skin test (Mantoux test), IFN-γ release assay, or polarized light microscopy may rule out infectious etiologies.^9,49 Serologic testing might include VDRL test, Treponema pallidum hemagglutination assay, hepatitis B, hepatitis C, and human immunodeficiency virus.⁵

Crohn disease is characterized histologically by sarcoidlike noncaseating granulomas, and as such, it is important to differentiate MCD from sarcoidosis prior to histologic analysis. Sarcoidosis also can be considered much less likely with a normal chest radiograph and in the absence of increased serum calcium and angiotensin-converting enzyme levels.⁷ The differentiation of sarcoidosis from MCD on the microscopic scale is subtle but is sometimes facilitated in the presence of an ulcerated epidermis or lymphocytic/eosinophilic infiltrate and edema within the dermis, all suggestive of MCD.¹⁴

Metastatic CD also should be differentiated from erythema nodosum and pyoderma gangrenosum, which are among the most common cutaneous findings associated with CD.¹⁴ Pyoderma gangrenosum can be distinguished histologically by identifying copious neutrophilic infiltrate with pseudoepitheliomatous hyperplasia.⁵⁰

Treatment

Because MCD is relatively rare, there are no known randomized trials suggesting a particular medical or surgical treatment. In a review of perineal MCD from 2007, the 40-year-old recommendation by Moutain³ opting for surgical debridement versus medical management still resonates, particularly for perineal disease, as an effective measure in all but the mildest of presentations.⁵¹ However, recent case reports also suggest that the tumor necrosis factor α (TNF-α) inhibitors such as infliximab and adalimumab should be considered prior to surgery even with severe perineal MCD.⁵¹ Moreover, even if medical management with TNF-α inhibitors or some combination of immunosuppressants and antibiotics does not eradicate the disease, it often helps reduce the size of the ulcers prior to surgery.⁵² With a limited understanding of MCD, one might think that removal of the affected bowel would eliminate cutaneous disease, but it has been shown that this strategy is not effective.^53,54

The composition and location of the particular lesion affects the trajectory of treatment. For example, MCD manifesting as local ulcers and plaques has been described as responding well to topical and intralesional steroids.^10,55,56 In the case of penile swelling and/or phimosis, circumcision has been helpful to improve the patient's ability to void as well as to attain and maintain erection.¹⁰ In the case of scrotal swelling secondary to MCD, early treatment (ie, within 4 to 6 months) with oral steroids and/or metronidazole is likely beneficial to prevent refractory edematous organization of the tissue.⁵⁷

As a general rule, an effective treatment will include a combination of an immunosuppressant, antibiotic therapy, and sometimes surgery. The most commonly used immunosuppressant agents include topical or intralesional steroids, infliximab,^43,58 cyclosporine A,^59,60 dapsone, minocycline, thalidomide, methotrexate, mycophenolate mofetil, sulfasalazine, azathioprine, tacrolimus, and 6-mercaptopurine.⁴ Steroids have been the conventional treatment of extraintestinal manifestations of CD⁶¹; however, perineal CD has been poorly controlled with systemic steroids.⁶² If steroids are found not to be effective, sometimes agents such as dapsone or thalidomide are considered. One case report noted stabilization of MCD penile ulcers with oral thalidomide 300 mg once daily, oral minocycline 100 mg once daily, and topical tacrolimus 0.3% with benzocaine twice daily with continuation of prednisolone and methotrexate as parts of previously unsuccessful regimen.⁵²

Metronidazole is perhaps the most commonly used antibiotic, having been a component of many successful regimens.^4,63 For example, a 27-year-old patient with MCD presenting as a nonhealing ulcerative lesion in the subcoronal area of the penis and scrotum was treated successfully with a 6-month course of mesalamine, prednisone, and metronidazole.⁴⁵ Another case report of vulvar MCD reported initial success with intravenous methylprednisolone, ciprofloxacin, and metronidazole.²³ The primary limitation of metronidazole is that subsequent tapering of the dose seems to result in recurrence of disease.⁶⁴ Consequently, patients must remain on the antibiotic for an indeterminate course, with dosages ranging from 5 mg/kg daily in adolescents⁶⁵ to 1000 to 1500 mg daily in adults.⁶⁶

Of the various immunosuppressants available, infliximab has been listed in numerous reports as a successful agent in both the induction and maintenance of extraintestinal manifestations of CD including MCD.^67-71 Infliximab has been reported to be effective in the treatment of penile and scrotal edema secondary to MCD that did not respond to other immunosuppressants including oral prednisolone, azathioprine, and cyclosporine.⁴³ Infliximab may be a good option to help heal draining fistulas, particularly in combination with an antibiotic such as metronidazole and ciprofloxacin, which helps to prevent abscess formation during healing.⁷² The response to infliximab has been dramatic, with resolution of cutaneous lesions after just 6 weeks in some cases.⁷³ The dosing regimen of infliximab has been suggested at 5 mg/kg administered at 0, 2, and 6 weeks, with subsequent maintenance infusions every 10 weeks,⁷⁰ or at 0, 4, and 12 weeks, with subsequent infusions every 8 weeks.⁴³

Adalimumab may be considered as an alternative to infliximab and is potentially less allergenic as a fully humanized monoclonal antibody to TNF-α, which also has been used successfully to both induce and maintain remission of moderate to severe CD.^42,74,75 Proposed dosing of adalimumab includes a loading dose of 160 mg subcutaneously on day 1, followed by an 80-mg dose 2 weeks later and a 40-mg maintenance dose every other week indefinitely.⁴⁸ Of note, adalimumab has been noted in the literature to have many potential side effects, including one particular case in which severe headaches were attributed to its use.⁵⁹ As a consequence of the headaches, the patient was switched from adalimumab to cyclosporine and responded well with no subsequent flare-ups on follow-up.

In summary, treatment of MCD depends on cutaneous location, severity, physician experience with certain antibiotics or immunosuppressants, availability of medication, and patient disposition. It seems reasonable to attempt medical management with one or more medical regimens before committing to surgical intervention. Furthermore, even with debridement, curettage, skin graft, or other surgical strategy, the patient is likely to require some period of immunosuppression to provide long-lasting remission.

Conclusion

Patients with inflammatory bowel disease often develop dermatologic sequelae, with MCD being a rare but serious process. Patients may present with a wide array of physical concerns and symptoms, many resembling other disease processes. As such, education and a high index of suspicion are needed for proper diagnosis and treatment.

Almost half of Crohn disease (CD) patients experience a dermatologic manifestation of the disease. A rare entity, metastatic CD (MCD) presents a diagnostic challenge without a high index of suspicion. Its etiology is not well defined; however, it appears to be an autoimmune response to gut antigens. Herein, we review the etiology/epidemiology, diagnostic criteria, and treatment for this uncommon condition.

Epidemiology and Clinical Characteristics of MCD

Metastatic CD was first described by Parks et al1 in 1965 and refers to a diverse collection of macroscopic dermatologic manifestations in tissue not contiguous with the gastrointestinal (GI) tract. To be classified as MCD, the tissue must demonstrate characteristic histopathologic findings, which invariably include noncaseating granulomas.

Crohn disease may affect any part of the GI tract from the mouth to anus, with a multitude of associated cutaneous manifestations having been described. The terminal ileum is the most commonly affected portion of the GI tract in CD, but the large intestine also may be involved in 55% to 80% of cases.² The incidence of non-MCD-associated anal lesions seems to correlate with intestinal involvement in that as few as 25% of patients with ileal-localized CD have anal lesions compared to nearly 80% of patients with large intestinal involvement.³

It has been estimated that 18% to 44% of patients with CD have some form of cutaneous manifestation,⁴ with MCD being a rare subcategory. As few as 100 cases have been described from 1965 to the present.⁵ The presence of MCD does not correlate well with severity of intestinal CD, and although a majority of MCD cases present after at least 6 months of GI symptoms,⁶ there are instances in which MCD presents without prior or existing evidence of intestinal CD.⁷

With regard to MCD, the term metastatic is sometimes supplanted in the literature by cutaneous to avoid any implication of cancer; however, due to a myriad of dermatologic manifestations, both terms can cause confusion. The categorization of the various types of cutaneous findings in CD is well summarized in a review by Palamaras et al8 with the following classifications: (1) granulomatous by direct extension (oral or perianal), (2) MCD lesions (genital and nongenital), (3) immune-related lesions, and (4) lesions from nutritional deficiencies. Of the cutaneous manifestations relating to CD, MCD is the least common cutaneous categorical manifestation and is further divided into subcategories of genital and nongenital lesions.⁸

The nongenital distribution of MCD is the more common variety in adults and particularly seems to affect the legs and plantar surfaces (38%), the trunk and abdomen (24%), and the face (15%).^5,9 These nongenital MCD manifestations are most commonly described as nodules, ulcerations, or erythematous to purple plaques, and less commonly described as abscesses, pustules, or papules.

The sequence of cutaneous symptoms of MCD relative to intestinal disease depends to some degree on patient age. In adults diagnosed with MCD, it has been noted that a GI flare is expected 2 months to 4 years after diagnosis; however, in children the subsequent GI flare has been noted to vary more widely from 9 months to 14 years following presentation of MCD.⁸ Furthermore, roughly 50% of children diagnosed with MCD present concomitantly with their first symptoms of a GI flare, whereas 70% of adults with MCD had been previously diagnosed with intestinal CD.⁸ In one review of 80 reported cases of MCD, 20% (16/80) had no symptoms of intestinal disease at the time of MCD diagnosis, and the majority of the asymptomatic cases were in children; interestingly, the majority of these same children were diagnosed with CD months to years later.⁹

Both the location and characteristics of cutaneous findings in MCD correlate with age.⁹ Metastatic CD has been identified in all age groups; however, lymphedema is more common in children/young adults, while nodules, ulceration, and fistulating disease are more often seen in adults.¹⁰ Affected children and adolescents with MCD range from 5 to 17 years of age, with a mean age at disease onset of 11.1 years and equal incidence in males and females.⁸ Adults with MCD range from 18 to 78 years of age, with a mean age at presentation of 38.4 years.^8,11

Concerning anatomic location of disease, adults with MCD most commonly have nodules with or without plaques on the arms and legs and less commonly in the genital area.⁸ In contrast, children with MCD are more prone to genital lesions, with up to 85% of cases including some degree of genital erythematous or nonerythematous swelling with or without induration.⁸ Genitourinary complications of CD as a broad category, however, are estimated to occur in only 5% to 20% of intestinal CD cases in both children and adults.¹²

There have been conflicting reports regarding gender predilection in MCD. Based on a review by Samitz et al¹³ of 200 cases of CD over an 18-year period, 22% of patients with CD were found to have cutaneous manifestations--presumably not MCD but rather perianal, perineal, vulvar fistulae, fissures, or abscesses--with a male to female preponderance of almost 2 to 1. A more recent review of the literature by Palamaras et al⁸ in 2008 reported that contiguous non-MCD affects adult females and children more often than adult males, with 63% adult cases being female. This review seems to be more congruent with other reports in the literature implicating that females are twice as commonly affected by MCD than males.^9,14

Pathophysiology

The etiology of MCD has not been well defined. One proposed mechanism of the distal tissue involvement of MCD is through passage of antigens to the skin with subsequent granulomatous response at the level of the dermis.¹⁰ Another proposed mechanism suggests antibody sensitization to gut antigens, possibly bacterial antigens, that then coincidentally cross-react with analogous skin antigens.^8,14 Burgdorf¹¹ supported this notion in a 1981 report in which it was suggested that the granulomatous reaction was related to deposition of immune complexes in the skin. Slater et al¹⁵ and Tatnall et al¹⁶ offered a variation of Burgdorf's notion, suggesting that it was sensitized T cells to circulating antigens that were the initiators of granuloma formation in the periphery.

An examination of MCD tissue in 1990 by Shum and Guenther¹⁷ under electron microscopy and immunofluorescence provided evidence against prior studies that purported to have identified immune complexes as the causative agents of MCD. In this study, the authors found no evidence of immune complexes in the dermis of MCD lesions. In addition, an attempt to react serum antibodies of a patient with MCD, which were postulated to have IgG, IgM, and IgA antibodies to specific gut antigens, yielded no response when reacted with the tongue, ileum, and colon tissue from a rat. As a culminant finding, the authors also noted MCD dermis tissue with granulomas without vasculitis, suggesting a T-cell mediated type IV hypersensitivity response with a secondary vasculitis from T-cell origin lymphokines and T-cell mediated monocyte activation.¹⁷

Research implicating other immunologic entities involved in the pathophysiology of CD such as β-2 integrin,¹⁸ CD14⁺ monocytes,¹⁹ and the role of the DNA repair gene MLH1 (mutL homolog 1)²⁰ have been considered but without a clearly definitive role in the manifestations of MCD.

The utility of metronidazole in the treatment of MCD has been suggested as evidence that certain bacteria in the gut may either serve as the causative antigen or may induce its formation²¹; however, the causative antigen has yet to be identified, and whether it travels distally to the skin or merely resembles a similar antigen normally present in the dermis has not yet been determined. Some research has used in situ polymerase chain reaction techniques to attempt to detect similar microbial pathogens in both the vasculature of active bowel lesions and in the skin, but to date, bacterial RNA noted to be present in the gut vasculature adjacent to CD lesions has not been detected in skin lesions.²²

Diagnosis

Physical Findings

Overall, it is estimated that roughly 56% of all MCD cases affect the external genitalia.²³ The classic appearance of MCD includes well-demarcated ulcerations in the areas of intertriginous skin folds with or without diffuse edema and tenderness to palpation.²³ Although MCD has been historically noted as having a predilection for moist skin folds, there are numerous case reports of MCD all over the body, including the face,^7,24-29 retroauricular areas,³⁰ arms and legs,^16,17,31-34 lower abdomen,^3,5 under the breasts,¹ perineum,³⁵ external genitalia,^1,9,36-40 and even the lungs⁴¹ and bladder.⁴²

As a dermatologic disease, MCD has been referred to as yet another great imitator, both on the macroscopic and microscopic levels.⁸ As such, more common causes of genital edema should be considered first and investigated based on the patient's history, physical examination, skin biopsy, lymphangiogram, ultrasound, and cystogram.⁴³ Ultrasonography and color Doppler sonography have been shown to be helpful in patients with genital involvement. This modality can evaluate not only the presence of normal testes but also intratesticular and scrotal wall fluid, especially when the physical examination reveals swelling that makes testicle palpation more difficult.⁶ Clinically, the correct diagnosis of MCD often is made through suspicion of inflammatory bowel disease based on classic symptoms and/or physical findings including abdominal pain, weight loss, bloody stool, diarrhea, perianal skin tags, and anal fissures or fistulas. Any of these GI findings should prompt an intestinal biopsy to rule out any histologic evidence of CD.

Metastatic CD affecting the vulva often presents with vulvar pain and pruritus and may clinically mimic a more benign disease such as balanitis plasmacellularis, also referred to as Zoon vulvitis.²³ Similar to MCD on any given body surface, there is dramatic variation in the macroscopic presentation of vulvar MCD, with physical examination findings ranging from bilateral diffuse, edematous, deeply macerated, red, ulcerated lesions over the vulva with lymphadenopathy to findings of bilateral vulvar pain with yellow drainage from the labia majora.²³ There have been cases of vulvar MCD that include exquisite vulvar pain but without structural abnormalities including normal uterus, cervix, adnexa, rectovaginal septum, and rectum. In these more nebulous cases of vulvar MCD, the diagnosis often is discovered incidentally when nonspecific diagnostic imaging suggests underlying CD.²³

Beyond the case-by-case variations on physical examination, the great difficulty in diagnosis, particularly in children, occurs in the absence of any GI symptoms and therefore no logical consideration of underlying CD. Consequently, there have been cases of children presenting with irritation of the vulva who were eventually diagnosed with MCD only after erroneous treatment of contact dermatitis, candidiasis, and even consideration of sexual abuse.³⁷ Because it is so rare and obscure among practicing clinicians, the diagnosis of MCD often is considered only after irritation or swelling of the external genitalia has not responded to standard therapies. If and when the diagnosis of MCD is considered in children, it has been suggested to screen patients for anorectal stricture, as case studies have found the condition to be relatively common in this subpopulation.⁴⁴

In the less common case of adults with genitourinary symptoms that suggest possible MCD, the differential diagnosis for penile or vaginal ulcers should include contact and irritant dermatitis, chronic infectious lesions (eg, hidradenitis suppurativa, actinomycosis, tuberculosis),⁴⁵ sexually transmitted ulcerative diseases (eg, chancroid, lymphogranuloma venereum, herpes genitalia, granuloma inguinale),⁴⁶ drug reactions, and even extramammary Paget disease.⁴⁷

Histologic Findings

Because MCD has so much macroscopic variation and can present anywhere on the surface of the body, formal diagnosis relies on microscopy. As an added measure of difficulty in diagnosis, one random biopsy of a suspicious segment of tissue may not contain the expected histologic findings; therefore, clinical suspicion may warrant a second biopsy.¹⁰ There have been reported cases of an adult patient without history of CD presenting with a lesion that resembled a more common pathology, such as a genital wart, and the correct diagnosis of MCD with pseudocondylomatous morphology was made only after intestinal manifestations prompted the clinician to consider such an unusual diagnosis.⁴⁸

From a histopathologic perspective, MCD is characterized by discrete, noncaseating, sarcoidlike granulomas with abundant multinucleated giant cells (Langhans giant cells) in the superficial dermis (papillary), deep dermis (reticular), and adipose tissue (Figure).^8,17 In the presence of concomitant intestinal disease, the granulomas of both the intestinal and dermal tissues should share the same microscopic characteristics.⁸ In addition, copious neutrophils and granulomas surrounding the microvasculature have been described,³⁴ as well as general lymphocyte and plasma cell infiltrate.⁴⁵ Some histologic samples have included collagen degeneration termed necrobiosis in the middle dermal layer as another variable finding in MCD.^14,34

On microscopy, it has been reported that use of Verhoeff-van Gieson staining may be helpful to highlight the presence of neutrophil obstruction within the dermal vasculature, particularly the arterial lumen, as well as to aid in highlighting swelling of the endothelium with fragmentation of the internal elastic lamina.¹⁷ Although not part of the routine diagnosis, electron microscopy of MCD tissue samples have confirmed hypertrophy of the endothelial cells composing the capillaries with resulting extravasation of fibrin, red blood cells, lymphocytes, and epithelioid histiocytes.¹⁷ Observation of tissue under direct immunofluorescence has been less helpful, as it has shown only nonspecific fibrinogen deposition within the dermis and dermal vessels.¹⁷

In an article on treatment of MCD, Escher et al⁴³ reinforced that the macroscopic findings of MCD are diverse, and the microscopic findings characteristic of MCD also can be mimicked by other etiologies such as sarcoidosis, tuberculosis, fungal infections, lymphogranuloma venereum, leishmaniasis, and connective tissue disorders.⁴³ As such, the workup to rule out infectious, anatomic, and autoimmune etiologies should be diverse. Often, the workup for MCD will include special stains such as Ziehl-Neelsen stain to rule out Mycobacterium tuberculosis and acid-fast bacilli and Fite stain to consider atypical mycobacteria. Other tests such as tissue culture, chest radiograph, tuberculin skin test (Mantoux test), IFN-γ release assay, or polarized light microscopy may rule out infectious etiologies.^9,49 Serologic testing might include VDRL test, Treponema pallidum hemagglutination assay, hepatitis B, hepatitis C, and human immunodeficiency virus.⁵

Crohn disease is characterized histologically by sarcoidlike noncaseating granulomas, and as such, it is important to differentiate MCD from sarcoidosis prior to histologic analysis. Sarcoidosis also can be considered much less likely with a normal chest radiograph and in the absence of increased serum calcium and angiotensin-converting enzyme levels.⁷ The differentiation of sarcoidosis from MCD on the microscopic scale is subtle but is sometimes facilitated in the presence of an ulcerated epidermis or lymphocytic/eosinophilic infiltrate and edema within the dermis, all suggestive of MCD.¹⁴

Metastatic CD also should be differentiated from erythema nodosum and pyoderma gangrenosum, which are among the most common cutaneous findings associated with CD.¹⁴ Pyoderma gangrenosum can be distinguished histologically by identifying copious neutrophilic infiltrate with pseudoepitheliomatous hyperplasia.⁵⁰

Treatment

Because MCD is relatively rare, there are no known randomized trials suggesting a particular medical or surgical treatment. In a review of perineal MCD from 2007, the 40-year-old recommendation by Moutain³ opting for surgical debridement versus medical management still resonates, particularly for perineal disease, as an effective measure in all but the mildest of presentations.⁵¹ However, recent case reports also suggest that the tumor necrosis factor α (TNF-α) inhibitors such as infliximab and adalimumab should be considered prior to surgery even with severe perineal MCD.⁵¹ Moreover, even if medical management with TNF-α inhibitors or some combination of immunosuppressants and antibiotics does not eradicate the disease, it often helps reduce the size of the ulcers prior to surgery.⁵² With a limited understanding of MCD, one might think that removal of the affected bowel would eliminate cutaneous disease, but it has been shown that this strategy is not effective.^53,54

The composition and location of the particular lesion affects the trajectory of treatment. For example, MCD manifesting as local ulcers and plaques has been described as responding well to topical and intralesional steroids.^10,55,56 In the case of penile swelling and/or phimosis, circumcision has been helpful to improve the patient's ability to void as well as to attain and maintain erection.¹⁰ In the case of scrotal swelling secondary to MCD, early treatment (ie, within 4 to 6 months) with oral steroids and/or metronidazole is likely beneficial to prevent refractory edematous organization of the tissue.⁵⁷

As a general rule, an effective treatment will include a combination of an immunosuppressant, antibiotic therapy, and sometimes surgery. The most commonly used immunosuppressant agents include topical or intralesional steroids, infliximab,^43,58 cyclosporine A,^59,60 dapsone, minocycline, thalidomide, methotrexate, mycophenolate mofetil, sulfasalazine, azathioprine, tacrolimus, and 6-mercaptopurine.⁴ Steroids have been the conventional treatment of extraintestinal manifestations of CD⁶¹; however, perineal CD has been poorly controlled with systemic steroids.⁶² If steroids are found not to be effective, sometimes agents such as dapsone or thalidomide are considered. One case report noted stabilization of MCD penile ulcers with oral thalidomide 300 mg once daily, oral minocycline 100 mg once daily, and topical tacrolimus 0.3% with benzocaine twice daily with continuation of prednisolone and methotrexate as parts of previously unsuccessful regimen.⁵²

Metronidazole is perhaps the most commonly used antibiotic, having been a component of many successful regimens.^4,63 For example, a 27-year-old patient with MCD presenting as a nonhealing ulcerative lesion in the subcoronal area of the penis and scrotum was treated successfully with a 6-month course of mesalamine, prednisone, and metronidazole.⁴⁵ Another case report of vulvar MCD reported initial success with intravenous methylprednisolone, ciprofloxacin, and metronidazole.²³ The primary limitation of metronidazole is that subsequent tapering of the dose seems to result in recurrence of disease.⁶⁴ Consequently, patients must remain on the antibiotic for an indeterminate course, with dosages ranging from 5 mg/kg daily in adolescents⁶⁵ to 1000 to 1500 mg daily in adults.⁶⁶

Of the various immunosuppressants available, infliximab has been listed in numerous reports as a successful agent in both the induction and maintenance of extraintestinal manifestations of CD including MCD.^67-71 Infliximab has been reported to be effective in the treatment of penile and scrotal edema secondary to MCD that did not respond to other immunosuppressants including oral prednisolone, azathioprine, and cyclosporine.⁴³ Infliximab may be a good option to help heal draining fistulas, particularly in combination with an antibiotic such as metronidazole and ciprofloxacin, which helps to prevent abscess formation during healing.⁷² The response to infliximab has been dramatic, with resolution of cutaneous lesions after just 6 weeks in some cases.⁷³ The dosing regimen of infliximab has been suggested at 5 mg/kg administered at 0, 2, and 6 weeks, with subsequent maintenance infusions every 10 weeks,⁷⁰ or at 0, 4, and 12 weeks, with subsequent infusions every 8 weeks.⁴³

Adalimumab may be considered as an alternative to infliximab and is potentially less allergenic as a fully humanized monoclonal antibody to TNF-α, which also has been used successfully to both induce and maintain remission of moderate to severe CD.^42,74,75 Proposed dosing of adalimumab includes a loading dose of 160 mg subcutaneously on day 1, followed by an 80-mg dose 2 weeks later and a 40-mg maintenance dose every other week indefinitely.⁴⁸ Of note, adalimumab has been noted in the literature to have many potential side effects, including one particular case in which severe headaches were attributed to its use.⁵⁹ As a consequence of the headaches, the patient was switched from adalimumab to cyclosporine and responded well with no subsequent flare-ups on follow-up.

In summary, treatment of MCD depends on cutaneous location, severity, physician experience with certain antibiotics or immunosuppressants, availability of medication, and patient disposition. It seems reasonable to attempt medical management with one or more medical regimens before committing to surgical intervention. Furthermore, even with debridement, curettage, skin graft, or other surgical strategy, the patient is likely to require some period of immunosuppression to provide long-lasting remission.

Conclusion

Patients with inflammatory bowel disease often develop dermatologic sequelae, with MCD being a rare but serious process. Patients may present with a wide array of physical concerns and symptoms, many resembling other disease processes. As such, education and a high index of suspicion are needed for proper diagnosis and treatment.

With more than 1,000 diseases for which genetic testing is available, and with the completion of the Human Genome Project, more patients are requesting genetic testing and more clinicians are utilizing such testing; it has become mainstream.¹ This increased utilization has resulted in increased cost as well, say Ruzzo and colleagues, who presented research on genetic testing costs and compliance with clinical best practices at the 2017 Annual Clinical and Scientific Meeting of the American College of Obstetricians and Gynecologists (ACOG).² But, according to previous research say Ruzzo and colleagues, these costs can be quelled by involving genetic counselors in the test-ordering process.

Just how much cost savings can be achieved? In their quality improvement project, the investigators found that 38.6% of 44 genetic tests reviewed were inappropriately ordered—either they were not indicated (21%), misordered for false reassurance (7%), or inadequately ordered (10.5%). If the tests were ordered as appropriately recommended, a cost savings of $20,912.58 would have been realized, according to the researchers.

Ruzzo and colleagues reviewed 114 charts over a 3-month period for adherence with published clinical practice guidelines. All of the charts were associated with a genetic test billing code for common tests ordered through LabCorp (for cystic fibrosis, BRCA mutation, factor V Leiden, prothrombin, alpha-thalassemia, hemochromatosis, and cell-free DNA).

The researchers concluded that genetic counselor review or involvement in genetic test ordering can decrease inappropriate spending and improve patient care. They pointed out that the 114 charts reviewed represent a fraction of genetic tests ordered at their institution, and further study should broaden the research scope to determine the full extent of the problem.

Ruzzo and colleagues were awarded first prize for their research as presented at ACOG.
 

Share your thoughts! Send your Letter to the Editor to [email protected]. Please include your name and the city and state in which you practice.

With more than 1,000 diseases for which genetic testing is available, and with the completion of the Human Genome Project, more patients are requesting genetic testing and more clinicians are utilizing such testing; it has become mainstream.¹ This increased utilization has resulted in increased cost as well, say Ruzzo and colleagues, who presented research on genetic testing costs and compliance with clinical best practices at the 2017 Annual Clinical and Scientific Meeting of the American College of Obstetricians and Gynecologists (ACOG).² But, according to previous research say Ruzzo and colleagues, these costs can be quelled by involving genetic counselors in the test-ordering process.

Just how much cost savings can be achieved? In their quality improvement project, the investigators found that 38.6% of 44 genetic tests reviewed were inappropriately ordered—either they were not indicated (21%), misordered for false reassurance (7%), or inadequately ordered (10.5%). If the tests were ordered as appropriately recommended, a cost savings of $20,912.58 would have been realized, according to the researchers.

Ruzzo and colleagues reviewed 114 charts over a 3-month period for adherence with published clinical practice guidelines. All of the charts were associated with a genetic test billing code for common tests ordered through LabCorp (for cystic fibrosis, BRCA mutation, factor V Leiden, prothrombin, alpha-thalassemia, hemochromatosis, and cell-free DNA).

The researchers concluded that genetic counselor review or involvement in genetic test ordering can decrease inappropriate spending and improve patient care. They pointed out that the 114 charts reviewed represent a fraction of genetic tests ordered at their institution, and further study should broaden the research scope to determine the full extent of the problem.

Ruzzo and colleagues were awarded first prize for their research as presented at ACOG.
 

Share your thoughts! Send your Letter to the Editor to [email protected]. Please include your name and the city and state in which you practice.

With more than 1,000 diseases for which genetic testing is available, and with the completion of the Human Genome Project, more patients are requesting genetic testing and more clinicians are utilizing such testing; it has become mainstream.¹ This increased utilization has resulted in increased cost as well, say Ruzzo and colleagues, who presented research on genetic testing costs and compliance with clinical best practices at the 2017 Annual Clinical and Scientific Meeting of the American College of Obstetricians and Gynecologists (ACOG).² But, according to previous research say Ruzzo and colleagues, these costs can be quelled by involving genetic counselors in the test-ordering process.

Just how much cost savings can be achieved? In their quality improvement project, the investigators found that 38.6% of 44 genetic tests reviewed were inappropriately ordered—either they were not indicated (21%), misordered for false reassurance (7%), or inadequately ordered (10.5%). If the tests were ordered as appropriately recommended, a cost savings of $20,912.58 would have been realized, according to the researchers.

Ruzzo and colleagues reviewed 114 charts over a 3-month period for adherence with published clinical practice guidelines. All of the charts were associated with a genetic test billing code for common tests ordered through LabCorp (for cystic fibrosis, BRCA mutation, factor V Leiden, prothrombin, alpha-thalassemia, hemochromatosis, and cell-free DNA).

The researchers concluded that genetic counselor review or involvement in genetic test ordering can decrease inappropriate spending and improve patient care. They pointed out that the 114 charts reviewed represent a fraction of genetic tests ordered at their institution, and further study should broaden the research scope to determine the full extent of the problem.

Ruzzo and colleagues were awarded first prize for their research as presented at ACOG.
 

Share your thoughts! Send your Letter to the Editor to [email protected]. Please include your name and the city and state in which you practice.

NEW ORLEANS – The integration of lifestyle, alternative, and conventional medicine into the care of patients with multiple sclerosis can be transformative for patients and clinicians alike, according to Allen C. Bowling, MD, PhD.

This approach not only emphasizes health and wellness of the whole person, it supports the clinician-patient relationship since neurologists serve as point persons for MS patients, Dr. Bowling said at the annual meeting of the Consortium of Multiple Sclerosis Centers. “It’s critical to not just think about MS the disease, but to think about the patient’s overall health, maintaining health,” he said. “That’s a big mind shift. I think sometimes people hear the term ‘integrative medicine’ and they start walking out of the room or think it’s getting ‘woo-woo,’ but there is a very evidence-based approach to integrative medicine. The core of it still is not familiar to a lot of physicians.”

Harness ‘built-in’ resources

Dr. Bowling, author of “Optimal Health With Multiple Sclerosis: A Guide to Integrating Lifestyle, Alternative, and Conventional Medicine” (New York: Demos Medical Publishing, 2014) and developer of a website devoted to integrative care and MS (www.neurologycare.net), said that some of best treatment approaches may be those that use the “built-in” resources of the human body and do not require any medications, supplements, devices, or technology. “The most effective and long-lasting changes in lifestyle may be those that are small and consistent,” he said. For example, when he first started applying integrative care principles to his practice more than 16 years ago, some patients told him that MS was “one of the best things that happened to them, and that it was a gift in that it helped them clean up their lifestyle.” In the summer of 2001, one such patient came to see Dr. Bowling and said, “Since my last appointment I’ve lost 20 pounds, bought a bike. I exercise four times weekly. My wife and I have changed our diet. This is real; I’m on it.”

“I said. ‘Very impressive. How did that happen? What motivated you?’ ”

“He said, ‘You did.’ This was like a turning point in his life.”

As of May 2017, this patient has maintained his healthy lifestyle changes.

Dr. Bowling told meeting attendees that early in his neurology career he didn’t always consider other ways he could impact MS patients beyond helping them determine the best disease-modifying treatment and/or assisting them in managing symptoms. Thinking to counsel them in areas such as a balanced diet, exercise, and emotional wellness “was a mind shift for me, and made me realize how narrow my focus was,” he said. “It transformed me to go back to thinking more about general medicine. I’m a detail-oriented guy, but I don’t think that’s in the best interests of our patients. I think we need to combine very disease-specific advice with very general advice. We’re at a very important place with our patients where we can potentially have a very significant impact with our recommendations about MS as well as other medical conditions and health maintenance.”

Take baby steps

Dr. Bowling recommended that clinicians take baby steps to incorporate aspects of integrated care, including use of brief, strong supportive statements; focusing on only one issue per visit; referring patients to information resources; and sharing or transferring responsibility/accountability with other providers. Excessive focus on one therapy – including unusual and unproven CAM therapies – may detract from, or be used to avoid, other valuable approaches. For example, some of Dr. Bowling’s patients may come in very enchanted with a particular dietary supplement yet their own diet is unhealthy. “I don’t scold them, but I say, ‘I don’t think this supplement’s going to hurt you but there’s much more evidence that we should shift the focus of your motivation and drive to dietary approaches.’ ”

Use leverage to tackle emotional health

In the area of emotional health, Dr. Bowling said that an MS diagnosis often serves as a springboard to help young patients develop emotional literacy so that they don’t develop high levels of stress and anxiety. “What I find are people on the verge of entering into depression or anxiety and not really knowing how to address those emotional issues or even to do basic identification and processing of emotions, and getting attached to mind-body approaches, which I think have a clear benefit, but for many patients it does not lead to emotional literacy,” he said. “I emphasize ‘I can’t be with you 24/7. That’s your piece of the equation.’ You can also help patients identify things that give them joy, meaning, and fun in life. That’s a motivator for a lot of them – to keep doing what they find joyful, meaningful, and fun.” Dr. Bowling said that this kind of approach brings “plain old common sense” to the clinician-patient relationship. “I think we all have lots of leverage with our patients, but there’s no cookbook or algorithm here; you need to start where patients are,” he said. “Our younger patients in particular are not really listening to their primary care doctor too much. They’re paying very close attention to what we’re talking about: disease-modifying therapies and symptomatic management.”

In Dr. Bowling’s clinical experience, men often struggle with emotional health and emotional literacy issues. “I have seen amazing transformations of men in their early 20s with very low emotional literacy, and working with them, sometimes with psychodynamic psychotherapy and other methods, sometimes just talking with friends and family – really encouraging them before there’s serious anxiety or depression.” One patient told him that MS “forced me to do a year of psychotherapy and some intensive introspection for a few years. This helped me and also my family.” He recommended that clinicians tread carefully when advising men about tobacco and alcohol use, and when advising women about weight management. “Be prepared; it’s a little different every time you bring those potential issues up,” he said.

Dr. Bowling added that MS often affects how patients view the aging process itself. “It can be a crash course in how to understand the body and best use it before people technically get to the aging years,” he said. “There’s also more acceptance of disability in people who are older.” In the setting of patients who experience disease flare-ups, they may ask you if there’s anything they can do from a lifestyle standpoint to make them go away. “Be primed for these teaching moments and opportunities where there’s a seed of motivation,” he advised.


Approach treats, prevents clinician burnout

Dr. Bowling described the integrative approach to treating MS patients as “an ever-changing skill set. There’s all this talk about neurologist burnout, which is very real. If you practice this way, this is a great treatment and preventive approach for clinician burnout because your patients check you out to see if you ‘walk the walk’ on advice you give them. My success with my patients in some of these areas is less than 50%. But when there’s a real change, it’s for the life of that person. That’s the most rewarding part of my career at this point.”

Dr. Bowling disclosed that he has received research, consulting, advising, and speaking fees from Acorda, Biogen, EMD Serono, Genentech, Genzyme, Sanofi-Aventis, Teva, the American Academy of Neurology, the CMSC, the Mandell Center for Multiple Sclerosis, and the National MS Society.

[email protected]

NEW ORLEANS – The integration of lifestyle, alternative, and conventional medicine into the care of patients with multiple sclerosis can be transformative for patients and clinicians alike, according to Allen C. Bowling, MD, PhD.

This approach not only emphasizes health and wellness of the whole person, it supports the clinician-patient relationship since neurologists serve as point persons for MS patients, Dr. Bowling said at the annual meeting of the Consortium of Multiple Sclerosis Centers. “It’s critical to not just think about MS the disease, but to think about the patient’s overall health, maintaining health,” he said. “That’s a big mind shift. I think sometimes people hear the term ‘integrative medicine’ and they start walking out of the room or think it’s getting ‘woo-woo,’ but there is a very evidence-based approach to integrative medicine. The core of it still is not familiar to a lot of physicians.”

Harness ‘built-in’ resources

Dr. Bowling, author of “Optimal Health With Multiple Sclerosis: A Guide to Integrating Lifestyle, Alternative, and Conventional Medicine” (New York: Demos Medical Publishing, 2014) and developer of a website devoted to integrative care and MS (www.neurologycare.net), said that some of best treatment approaches may be those that use the “built-in” resources of the human body and do not require any medications, supplements, devices, or technology. “The most effective and long-lasting changes in lifestyle may be those that are small and consistent,” he said. For example, when he first started applying integrative care principles to his practice more than 16 years ago, some patients told him that MS was “one of the best things that happened to them, and that it was a gift in that it helped them clean up their lifestyle.” In the summer of 2001, one such patient came to see Dr. Bowling and said, “Since my last appointment I’ve lost 20 pounds, bought a bike. I exercise four times weekly. My wife and I have changed our diet. This is real; I’m on it.”

“I said. ‘Very impressive. How did that happen? What motivated you?’ ”

“He said, ‘You did.’ This was like a turning point in his life.”

As of May 2017, this patient has maintained his healthy lifestyle changes.

Dr. Bowling told meeting attendees that early in his neurology career he didn’t always consider other ways he could impact MS patients beyond helping them determine the best disease-modifying treatment and/or assisting them in managing symptoms. Thinking to counsel them in areas such as a balanced diet, exercise, and emotional wellness “was a mind shift for me, and made me realize how narrow my focus was,” he said. “It transformed me to go back to thinking more about general medicine. I’m a detail-oriented guy, but I don’t think that’s in the best interests of our patients. I think we need to combine very disease-specific advice with very general advice. We’re at a very important place with our patients where we can potentially have a very significant impact with our recommendations about MS as well as other medical conditions and health maintenance.”

Take baby steps

Dr. Bowling recommended that clinicians take baby steps to incorporate aspects of integrated care, including use of brief, strong supportive statements; focusing on only one issue per visit; referring patients to information resources; and sharing or transferring responsibility/accountability with other providers. Excessive focus on one therapy – including unusual and unproven CAM therapies – may detract from, or be used to avoid, other valuable approaches. For example, some of Dr. Bowling’s patients may come in very enchanted with a particular dietary supplement yet their own diet is unhealthy. “I don’t scold them, but I say, ‘I don’t think this supplement’s going to hurt you but there’s much more evidence that we should shift the focus of your motivation and drive to dietary approaches.’ ”

Use leverage to tackle emotional health

In the area of emotional health, Dr. Bowling said that an MS diagnosis often serves as a springboard to help young patients develop emotional literacy so that they don’t develop high levels of stress and anxiety. “What I find are people on the verge of entering into depression or anxiety and not really knowing how to address those emotional issues or even to do basic identification and processing of emotions, and getting attached to mind-body approaches, which I think have a clear benefit, but for many patients it does not lead to emotional literacy,” he said. “I emphasize ‘I can’t be with you 24/7. That’s your piece of the equation.’ You can also help patients identify things that give them joy, meaning, and fun in life. That’s a motivator for a lot of them – to keep doing what they find joyful, meaningful, and fun.” Dr. Bowling said that this kind of approach brings “plain old common sense” to the clinician-patient relationship. “I think we all have lots of leverage with our patients, but there’s no cookbook or algorithm here; you need to start where patients are,” he said. “Our younger patients in particular are not really listening to their primary care doctor too much. They’re paying very close attention to what we’re talking about: disease-modifying therapies and symptomatic management.”

In Dr. Bowling’s clinical experience, men often struggle with emotional health and emotional literacy issues. “I have seen amazing transformations of men in their early 20s with very low emotional literacy, and working with them, sometimes with psychodynamic psychotherapy and other methods, sometimes just talking with friends and family – really encouraging them before there’s serious anxiety or depression.” One patient told him that MS “forced me to do a year of psychotherapy and some intensive introspection for a few years. This helped me and also my family.” He recommended that clinicians tread carefully when advising men about tobacco and alcohol use, and when advising women about weight management. “Be prepared; it’s a little different every time you bring those potential issues up,” he said.

Dr. Bowling added that MS often affects how patients view the aging process itself. “It can be a crash course in how to understand the body and best use it before people technically get to the aging years,” he said. “There’s also more acceptance of disability in people who are older.” In the setting of patients who experience disease flare-ups, they may ask you if there’s anything they can do from a lifestyle standpoint to make them go away. “Be primed for these teaching moments and opportunities where there’s a seed of motivation,” he advised.


Approach treats, prevents clinician burnout

Dr. Bowling described the integrative approach to treating MS patients as “an ever-changing skill set. There’s all this talk about neurologist burnout, which is very real. If you practice this way, this is a great treatment and preventive approach for clinician burnout because your patients check you out to see if you ‘walk the walk’ on advice you give them. My success with my patients in some of these areas is less than 50%. But when there’s a real change, it’s for the life of that person. That’s the most rewarding part of my career at this point.”

Dr. Bowling disclosed that he has received research, consulting, advising, and speaking fees from Acorda, Biogen, EMD Serono, Genentech, Genzyme, Sanofi-Aventis, Teva, the American Academy of Neurology, the CMSC, the Mandell Center for Multiple Sclerosis, and the National MS Society.

[email protected]

NEW ORLEANS – The integration of lifestyle, alternative, and conventional medicine into the care of patients with multiple sclerosis can be transformative for patients and clinicians alike, according to Allen C. Bowling, MD, PhD.

This approach not only emphasizes health and wellness of the whole person, it supports the clinician-patient relationship since neurologists serve as point persons for MS patients, Dr. Bowling said at the annual meeting of the Consortium of Multiple Sclerosis Centers. “It’s critical to not just think about MS the disease, but to think about the patient’s overall health, maintaining health,” he said. “That’s a big mind shift. I think sometimes people hear the term ‘integrative medicine’ and they start walking out of the room or think it’s getting ‘woo-woo,’ but there is a very evidence-based approach to integrative medicine. The core of it still is not familiar to a lot of physicians.”

Harness ‘built-in’ resources

Dr. Bowling, author of “Optimal Health With Multiple Sclerosis: A Guide to Integrating Lifestyle, Alternative, and Conventional Medicine” (New York: Demos Medical Publishing, 2014) and developer of a website devoted to integrative care and MS (www.neurologycare.net), said that some of best treatment approaches may be those that use the “built-in” resources of the human body and do not require any medications, supplements, devices, or technology. “The most effective and long-lasting changes in lifestyle may be those that are small and consistent,” he said. For example, when he first started applying integrative care principles to his practice more than 16 years ago, some patients told him that MS was “one of the best things that happened to them, and that it was a gift in that it helped them clean up their lifestyle.” In the summer of 2001, one such patient came to see Dr. Bowling and said, “Since my last appointment I’ve lost 20 pounds, bought a bike. I exercise four times weekly. My wife and I have changed our diet. This is real; I’m on it.”

“I said. ‘Very impressive. How did that happen? What motivated you?’ ”

“He said, ‘You did.’ This was like a turning point in his life.”

As of May 2017, this patient has maintained his healthy lifestyle changes.

Dr. Bowling told meeting attendees that early in his neurology career he didn’t always consider other ways he could impact MS patients beyond helping them determine the best disease-modifying treatment and/or assisting them in managing symptoms. Thinking to counsel them in areas such as a balanced diet, exercise, and emotional wellness “was a mind shift for me, and made me realize how narrow my focus was,” he said. “It transformed me to go back to thinking more about general medicine. I’m a detail-oriented guy, but I don’t think that’s in the best interests of our patients. I think we need to combine very disease-specific advice with very general advice. We’re at a very important place with our patients where we can potentially have a very significant impact with our recommendations about MS as well as other medical conditions and health maintenance.”

Take baby steps

Dr. Bowling recommended that clinicians take baby steps to incorporate aspects of integrated care, including use of brief, strong supportive statements; focusing on only one issue per visit; referring patients to information resources; and sharing or transferring responsibility/accountability with other providers. Excessive focus on one therapy – including unusual and unproven CAM therapies – may detract from, or be used to avoid, other valuable approaches. For example, some of Dr. Bowling’s patients may come in very enchanted with a particular dietary supplement yet their own diet is unhealthy. “I don’t scold them, but I say, ‘I don’t think this supplement’s going to hurt you but there’s much more evidence that we should shift the focus of your motivation and drive to dietary approaches.’ ”

Use leverage to tackle emotional health

In the area of emotional health, Dr. Bowling said that an MS diagnosis often serves as a springboard to help young patients develop emotional literacy so that they don’t develop high levels of stress and anxiety. “What I find are people on the verge of entering into depression or anxiety and not really knowing how to address those emotional issues or even to do basic identification and processing of emotions, and getting attached to mind-body approaches, which I think have a clear benefit, but for many patients it does not lead to emotional literacy,” he said. “I emphasize ‘I can’t be with you 24/7. That’s your piece of the equation.’ You can also help patients identify things that give them joy, meaning, and fun in life. That’s a motivator for a lot of them – to keep doing what they find joyful, meaningful, and fun.” Dr. Bowling said that this kind of approach brings “plain old common sense” to the clinician-patient relationship. “I think we all have lots of leverage with our patients, but there’s no cookbook or algorithm here; you need to start where patients are,” he said. “Our younger patients in particular are not really listening to their primary care doctor too much. They’re paying very close attention to what we’re talking about: disease-modifying therapies and symptomatic management.”

In Dr. Bowling’s clinical experience, men often struggle with emotional health and emotional literacy issues. “I have seen amazing transformations of men in their early 20s with very low emotional literacy, and working with them, sometimes with psychodynamic psychotherapy and other methods, sometimes just talking with friends and family – really encouraging them before there’s serious anxiety or depression.” One patient told him that MS “forced me to do a year of psychotherapy and some intensive introspection for a few years. This helped me and also my family.” He recommended that clinicians tread carefully when advising men about tobacco and alcohol use, and when advising women about weight management. “Be prepared; it’s a little different every time you bring those potential issues up,” he said.

Dr. Bowling added that MS often affects how patients view the aging process itself. “It can be a crash course in how to understand the body and best use it before people technically get to the aging years,” he said. “There’s also more acceptance of disability in people who are older.” In the setting of patients who experience disease flare-ups, they may ask you if there’s anything they can do from a lifestyle standpoint to make them go away. “Be primed for these teaching moments and opportunities where there’s a seed of motivation,” he advised.


Approach treats, prevents clinician burnout

Dr. Bowling described the integrative approach to treating MS patients as “an ever-changing skill set. There’s all this talk about neurologist burnout, which is very real. If you practice this way, this is a great treatment and preventive approach for clinician burnout because your patients check you out to see if you ‘walk the walk’ on advice you give them. My success with my patients in some of these areas is less than 50%. But when there’s a real change, it’s for the life of that person. That’s the most rewarding part of my career at this point.”

Dr. Bowling disclosed that he has received research, consulting, advising, and speaking fees from Acorda, Biogen, EMD Serono, Genentech, Genzyme, Sanofi-Aventis, Teva, the American Academy of Neurology, the CMSC, the Mandell Center for Multiple Sclerosis, and the National MS Society.

[email protected]

Several times a year, I’m privileged to step away from my role as chief medical officer of a health insurance company and return to a previous role I cherish – teaching.

This isn’t the clinical teaching that I used to do as a hospital medicine attending or palliative medicine consultant. These are mostly 4th-year medical students who have 90 minutes or so set aside during their primary care rotation to learn about “the business of medicine.”

I always begin by telling them that when I went to medical school, “I always intended to become a health insurance executive – NOT!” (If I get a few laughs, I know the time will fly by.) I share the history of my improbable career arc and how I wound up doing something I didn’t even know existed when I was their age. And, I still try to impart some pearls of wisdom in case they remember any of this discussion as they embark on their own personal and professional journeys, knowing that at this stage in their young careers, they will be almost totally immersed in their clinical training.

1. Do what you love

Sounds simple, but too many of us make the expedient choice, or the one expected of us. Work is hard enough without being able to find some joy and meaning every day in what you do. Every job has aspects that must be tolerated, but if you don’t find a greater purpose in practicing medicine, then find a way to get it back – or think about doing something else.

2. When opportunity knocks, be prepared to answer the door

For me, I enjoyed caring for patients one at a time, perhaps 15 or so during any particular day. Being a hospitalist is important and fulfilling work. But my experience as a hospitalist enabled me to recognize the “quality chasms” that existed in my hospital and across the “system,” namely lost opportunities to provide better end-of-life care and to better coordinate care within the hospital and across the care continuum. A new mission evolved for me: to do whatever I could to improve the safety, quality, and efficiency of the care we provided, and to make the hospital a better place to work. I taught myself the clinical skills to practice palliative medicine, and I attended courses that helped me prepare to become a service line medical director in hopes of starting a program at my hospital. I also took on the role of medical director of care management at my hospital, which in a sense allowed me to help take care of several hundred patients at a time – the beginning of my transition to population health.

3. Be a lifelong learner

When these opportunities arose, I was prepared for the challenges thanks to training opportunities I actively sought out, and thanks to the support of my mentors and my medical group to attend leadership training, such as SHM’s Leadership Academy. No matter what your role in your group or at your hospital, gaining these valuable skills outside of the usual medical training will help position you for new opportunities that can only help you create a more sustainable career. And although I never went back to school to earn another advanced degree such as an MBA or MHA, additional formal education is something to consider. You can never have too many tools in your toolkit.

4. Diversify!

It’s good advice from your financial adviser, and it’s good advice for your career. I’m not suggesting you take on a side job as a lawyer or a carpenter, but you might want to think about becoming an expert in a related field like perioperative medicine, primary palliative care, or postacute care. Or consider developing a niche as a sought-after leader for hospital-based committees, such as Quality or P&T. Or maybe consider clinical research, even if you’re not at an academic medical center. The point I’m making – and I know this may seem controversial – is that practicing medicine 100% of the time is probably no longer a sustainable plan for the entire 30- to 40-year span of your postgraduate career. Find an area that you can develop into protected, paid time apart from providing direct clinical care.

5. If you are thinking of changing jobs or even careers, run toward something – not away from something else

When I was first recruited to be a medical director at another health plan, I struggled mightily as to whether leaving full-time practice was an opportunity or a foolish, dead-end career move. Ultimately, I made my decision not to avoid night call or working every other weekend; I did it because I felt I had made a difference in the hospital where I had worked for 15 years and was ready to take on a new challenge by learning the business side of health care. It provided me the opportunity to positively impact the care of not just several hundred patients, but as many as two million! My current position now allows me to have even greater influence in pursuing my personal mission to improve the quality, safety, and affordability of health care.

6. Seek balance in life

Again, sounds trite, but think about it. Most health care professionals, especially physicians, have spent most of their adult lives focused on a single goal – and that often comes at a great cost, both financially and personally. (By the way, I say “seek” because at this point in my career, I doubt any of us ever really find balance.) The best you can hope for is to be wise enough to know that amongst all the balls we are juggling, there are a few that you just can’t let drop without possibly breaking without repair.

As I conclude my talks, I tell those young medical students to practice resiliency; the only constant is change. Remain inquisitive, open yourself to whatever life may bring and enjoy the ride. With a specialty as dynamic and diverse as hospital medicine, you never know where it will take you.
 

Dr. Epstein is executive vice president & chief medical officer at PreferredOne, and adjunct assistant professor of medicine at the University of Minnesota, Minneapolis. He also serves as Board Secretary of SHM.

Several times a year, I’m privileged to step away from my role as chief medical officer of a health insurance company and return to a previous role I cherish – teaching.

This isn’t the clinical teaching that I used to do as a hospital medicine attending or palliative medicine consultant. These are mostly 4th-year medical students who have 90 minutes or so set aside during their primary care rotation to learn about “the business of medicine.”

I always begin by telling them that when I went to medical school, “I always intended to become a health insurance executive – NOT!” (If I get a few laughs, I know the time will fly by.) I share the history of my improbable career arc and how I wound up doing something I didn’t even know existed when I was their age. And, I still try to impart some pearls of wisdom in case they remember any of this discussion as they embark on their own personal and professional journeys, knowing that at this stage in their young careers, they will be almost totally immersed in their clinical training.

1. Do what you love

Sounds simple, but too many of us make the expedient choice, or the one expected of us. Work is hard enough without being able to find some joy and meaning every day in what you do. Every job has aspects that must be tolerated, but if you don’t find a greater purpose in practicing medicine, then find a way to get it back – or think about doing something else.

2. When opportunity knocks, be prepared to answer the door

For me, I enjoyed caring for patients one at a time, perhaps 15 or so during any particular day. Being a hospitalist is important and fulfilling work. But my experience as a hospitalist enabled me to recognize the “quality chasms” that existed in my hospital and across the “system,” namely lost opportunities to provide better end-of-life care and to better coordinate care within the hospital and across the care continuum. A new mission evolved for me: to do whatever I could to improve the safety, quality, and efficiency of the care we provided, and to make the hospital a better place to work. I taught myself the clinical skills to practice palliative medicine, and I attended courses that helped me prepare to become a service line medical director in hopes of starting a program at my hospital. I also took on the role of medical director of care management at my hospital, which in a sense allowed me to help take care of several hundred patients at a time – the beginning of my transition to population health.

3. Be a lifelong learner

When these opportunities arose, I was prepared for the challenges thanks to training opportunities I actively sought out, and thanks to the support of my mentors and my medical group to attend leadership training, such as SHM’s Leadership Academy. No matter what your role in your group or at your hospital, gaining these valuable skills outside of the usual medical training will help position you for new opportunities that can only help you create a more sustainable career. And although I never went back to school to earn another advanced degree such as an MBA or MHA, additional formal education is something to consider. You can never have too many tools in your toolkit.

4. Diversify!

It’s good advice from your financial adviser, and it’s good advice for your career. I’m not suggesting you take on a side job as a lawyer or a carpenter, but you might want to think about becoming an expert in a related field like perioperative medicine, primary palliative care, or postacute care. Or consider developing a niche as a sought-after leader for hospital-based committees, such as Quality or P&T. Or maybe consider clinical research, even if you’re not at an academic medical center. The point I’m making – and I know this may seem controversial – is that practicing medicine 100% of the time is probably no longer a sustainable plan for the entire 30- to 40-year span of your postgraduate career. Find an area that you can develop into protected, paid time apart from providing direct clinical care.

5. If you are thinking of changing jobs or even careers, run toward something – not away from something else

When I was first recruited to be a medical director at another health plan, I struggled mightily as to whether leaving full-time practice was an opportunity or a foolish, dead-end career move. Ultimately, I made my decision not to avoid night call or working every other weekend; I did it because I felt I had made a difference in the hospital where I had worked for 15 years and was ready to take on a new challenge by learning the business side of health care. It provided me the opportunity to positively impact the care of not just several hundred patients, but as many as two million! My current position now allows me to have even greater influence in pursuing my personal mission to improve the quality, safety, and affordability of health care.

6. Seek balance in life

Again, sounds trite, but think about it. Most health care professionals, especially physicians, have spent most of their adult lives focused on a single goal – and that often comes at a great cost, both financially and personally. (By the way, I say “seek” because at this point in my career, I doubt any of us ever really find balance.) The best you can hope for is to be wise enough to know that amongst all the balls we are juggling, there are a few that you just can’t let drop without possibly breaking without repair.

As I conclude my talks, I tell those young medical students to practice resiliency; the only constant is change. Remain inquisitive, open yourself to whatever life may bring and enjoy the ride. With a specialty as dynamic and diverse as hospital medicine, you never know where it will take you.
 

Dr. Epstein is executive vice president & chief medical officer at PreferredOne, and adjunct assistant professor of medicine at the University of Minnesota, Minneapolis. He also serves as Board Secretary of SHM.

Several times a year, I’m privileged to step away from my role as chief medical officer of a health insurance company and return to a previous role I cherish – teaching.

This isn’t the clinical teaching that I used to do as a hospital medicine attending or palliative medicine consultant. These are mostly 4th-year medical students who have 90 minutes or so set aside during their primary care rotation to learn about “the business of medicine.”

I always begin by telling them that when I went to medical school, “I always intended to become a health insurance executive – NOT!” (If I get a few laughs, I know the time will fly by.) I share the history of my improbable career arc and how I wound up doing something I didn’t even know existed when I was their age. And, I still try to impart some pearls of wisdom in case they remember any of this discussion as they embark on their own personal and professional journeys, knowing that at this stage in their young careers, they will be almost totally immersed in their clinical training.

1. Do what you love

Sounds simple, but too many of us make the expedient choice, or the one expected of us. Work is hard enough without being able to find some joy and meaning every day in what you do. Every job has aspects that must be tolerated, but if you don’t find a greater purpose in practicing medicine, then find a way to get it back – or think about doing something else.

2. When opportunity knocks, be prepared to answer the door

For me, I enjoyed caring for patients one at a time, perhaps 15 or so during any particular day. Being a hospitalist is important and fulfilling work. But my experience as a hospitalist enabled me to recognize the “quality chasms” that existed in my hospital and across the “system,” namely lost opportunities to provide better end-of-life care and to better coordinate care within the hospital and across the care continuum. A new mission evolved for me: to do whatever I could to improve the safety, quality, and efficiency of the care we provided, and to make the hospital a better place to work. I taught myself the clinical skills to practice palliative medicine, and I attended courses that helped me prepare to become a service line medical director in hopes of starting a program at my hospital. I also took on the role of medical director of care management at my hospital, which in a sense allowed me to help take care of several hundred patients at a time – the beginning of my transition to population health.

3. Be a lifelong learner

When these opportunities arose, I was prepared for the challenges thanks to training opportunities I actively sought out, and thanks to the support of my mentors and my medical group to attend leadership training, such as SHM’s Leadership Academy. No matter what your role in your group or at your hospital, gaining these valuable skills outside of the usual medical training will help position you for new opportunities that can only help you create a more sustainable career. And although I never went back to school to earn another advanced degree such as an MBA or MHA, additional formal education is something to consider. You can never have too many tools in your toolkit.

4. Diversify!

It’s good advice from your financial adviser, and it’s good advice for your career. I’m not suggesting you take on a side job as a lawyer or a carpenter, but you might want to think about becoming an expert in a related field like perioperative medicine, primary palliative care, or postacute care. Or consider developing a niche as a sought-after leader for hospital-based committees, such as Quality or P&T. Or maybe consider clinical research, even if you’re not at an academic medical center. The point I’m making – and I know this may seem controversial – is that practicing medicine 100% of the time is probably no longer a sustainable plan for the entire 30- to 40-year span of your postgraduate career. Find an area that you can develop into protected, paid time apart from providing direct clinical care.

5. If you are thinking of changing jobs or even careers, run toward something – not away from something else

When I was first recruited to be a medical director at another health plan, I struggled mightily as to whether leaving full-time practice was an opportunity or a foolish, dead-end career move. Ultimately, I made my decision not to avoid night call or working every other weekend; I did it because I felt I had made a difference in the hospital where I had worked for 15 years and was ready to take on a new challenge by learning the business side of health care. It provided me the opportunity to positively impact the care of not just several hundred patients, but as many as two million! My current position now allows me to have even greater influence in pursuing my personal mission to improve the quality, safety, and affordability of health care.

6. Seek balance in life

Again, sounds trite, but think about it. Most health care professionals, especially physicians, have spent most of their adult lives focused on a single goal – and that often comes at a great cost, both financially and personally. (By the way, I say “seek” because at this point in my career, I doubt any of us ever really find balance.) The best you can hope for is to be wise enough to know that amongst all the balls we are juggling, there are a few that you just can’t let drop without possibly breaking without repair.

As I conclude my talks, I tell those young medical students to practice resiliency; the only constant is change. Remain inquisitive, open yourself to whatever life may bring and enjoy the ride. With a specialty as dynamic and diverse as hospital medicine, you never know where it will take you.
 

Dr. Epstein is executive vice president & chief medical officer at PreferredOne, and adjunct assistant professor of medicine at the University of Minnesota, Minneapolis. He also serves as Board Secretary of SHM.

In 2014, the United States spent $3 trillion on healthcare; hospitalization consumed 32% of these expenditures.¹ Today, Medicare patients account for over 50% of hospital days and over 30% of all hospital discharges in the United States.² Despite this staggering financial burden, hospitalization of older adults often results in poor patient outcomes.^3-6 The exponential growth of the hospitalist movement, from 350 hospitalists nationwide in 1995 to over 44,000 in 2014, has become the key strategy for providing care to hospitalized geriatric patients.^7-10 Most of these hospitalists have not received geriatric training.^11-15

There is growing evidence that a geriatric approach, emphasizing multidisciplinary management of the complex needs of older patients, leads to improved outcomes. Geriatric Evaluation and Management Units (GEMUs), such as Acute Care for Elderly (ACE) models, have demonstrated significant decreases in functional decline, institutionalization, and death in randomized controlled trials.^16,17 Multidisciplinary, nonunit based efforts, such as the mobile acute care of elderly (MACE), proactive consultation models (Sennour/Counsell), and the Hospital Elder Life Program (HELP), have demonstrated success in preventing adverse events and decreasing length of stay (LOS).^17-20

However, these models have not been systematically implemented due to challenges in generalizability and replicability in diverse settings. To address this concern, an alternative approach must be developed to widely “generalize” geriatric expertise throughout hospitals, regardless of their location, size, and resources. This initiative will require systematic integration of evidence-based decision support tools for the standardization of clinical management in hospitalized older adults.²¹

The 1998 Assessing Care of Vulnerable Elders (ACOVE) project developed a standardized tool to measure and evaluate the quality of care by using a comprehensive set of quality indicators (QIs) to improve the care of “vulnerable elders” (VEs) at a high risk for functional and cognitive decline and death.^22-24 The latest systematic review concludes that, although many studies have used ACOVE as an assessment tool of quality, there has been a dearth of studies investigating the ACOVE QIs as an intervention to improve patient care.²⁵

Our study investigated the role of ACOVE as an intervention by using the QIs as a standardized checklist in the acute care setting. We selected the 4 most commonly encountered QIs in the hospital setting, namely venous thrombosis prophylaxis (VTE), indwelling bladder catheter, mobilization, and delirium evaluation, in order to test the feasibility and impact of systematically implementing these ACOVE QIs as a therapeutic intervention for all hospitalized older adults.

This study (IRB #13-644B) was conducted using a prospective intervention with a nonequivalent control group design comprised of retrospective chart data from May 1, 2014, to June 30, 2015. Process and outcome variables were extracted from electronic medical records ([EMR], Sunrise Clinical Manager [SCM]) of 2,396 patients, with 530 patients in the intervention unit and 1,866 on the control units, at a large academic tertiary center operating in the greater New York metropolitan area. Our study investigated the role of ACOVE as an intervention to improve patient care by using selected QIs as a standardized checklist tool in the acute care setting. Of the original 30 hospital-specific QIs, our study focused on the care of older adults admitted to the medicine service.²⁶ We selected commonly encountered QIs, with the objective of testing the feasibility and impact of implementing the ACOVE QIs as an intervention to improve care of hospitalized older adults. This intervention consisted of applying the checklist tool, constructed with 4 selected ACOVE QIs and administered daily during interdisciplinary rounds, namely: 2 general “medical” indicators, VTE prophylaxis and indwelling bladder catheters, and 2 “geriatric”-focused indicators, mobilization and delirium evaluation.

Subject matter experts (hospitalists, geriatricians, researchers, administrators, and nurses) reviewed the ACOVE QIs and agreed upon the adaptation of the QIs from a quality measure assessment into a feasible and acceptable intervention checklist tool (Table 1). The checklist was reviewed during daily interdisciplinary rounds for all patients 75 years and older. While ACOVE defined vulnerable elders by using the Vulnerable Elder Screen (VES), we wanted to apply this intervention more broadly to all hospitalized older adults who are most at risk for poor outcomes.²⁷ Patients admitted to the intensive care unit, inpatient psychiatry, inpatient leukemia/lymphoma, and surgical services were excluded.

Daily interdisciplinary rounds are held on every one of the five 40-bed medical units; they last approximately 1 hour, and consist of a lead hospitalist, nurse manager, nurse practitioners, case managers, and the nursing staff. During interdisciplinary rounds, nurses present the case to the team members who then discuss the care plan. These 5 medical units did not differ in terms of patient characteristics or staffing patterns; the intervention unit was chosen simply for logistical reasons, in that the principal investigator (PI) had been assigned to this unit prior to study start-up.

Prior to the intervention, LS held an education session for staff on the intervention unit staff (who participated on interdisciplinary rounds) to explain the concept of the ACOVE QI initiative and describe the four QIs selected for the study. Three subsequent educational sessions were held during the first week of the intervention, with new incoming staff receiving a brief individual educational session. The staff demonstrated significant knowledge improvement after session completion (pre/post mean score 70.6% vs 90.0%; P < .0001).

The Clinical Information System for the Health System EMR, The Eclipsys SCM, has alerts with different levels of severity from “soft” (user must acknowledge a recommendation) to “hard” (requires an action in order to proceed).

To measure compliance of the quality indicators, we collected the following variables:

QI 1: VTE prophylaxis

Through SCM, we collected type of VTE prophylaxis ordered (pharmacologic and/or mechanical) as well as start and stop dates for all agents. International normalized ratio levels were checked for patients receiving warfarin. Days of compliance were calculated.

QI 2: Indwelling Bladder Catheters

SCM data were collected on catheter entry and discontinuation dates, the presence of an indication, and order renewal for bladder catheter at least every 3 days.

QI 3: Mobilization

Ambulation status prior to admission was extracted from nursing documentation completed on admission to the medical ward. Patients documented as bedfast were categorized as nonambulatory prior to admission. Nursing documentation of activity level and amount of feet ambulated per nursing shift were collected. In addition, hospital day of physical therapy (PT) order and hospital days with PT performed were charted. Compliance with QI 3 in patients documented as ambulatory prior to hospital admission was recorded as present if there was a PT order within 48 hours of admission.

QI 4: Delirium Evaluation

During daily rounds, the hospitalist (PI) questioned nurses about delirium evaluation, using the first feature of the Confusion Assessment Method (CAM) as well as the “single question in delirium,” namely, “Is there evidence of an acute change in mental status from the patient’s baseline?” and “Do you think [name of patient] has been more confused lately?”^28,29 Because EMR does not contain a specified field for delirium screening and documentation, and patients are not routinely included in rounds, documentation with QI 4 was recorded using the “key words” method as described in the work by Puelle et al.³⁰ To extract SCM key words, nursing documentation of the “cognitive/perceptual/neurological exam” section of the EMR on admission and on all subsequent documentation (once per shift) was retrieved to identify acute changes in mental status (eg, “altered mental status, delirium/delirious, alert and oriented X 3, confused/confusion, disoriented, lethargy/lethargic”).³⁰ In addition, nurses were asked to activate an SCM parameter, “Acute Confusion” SCM parameter, in the nursing documentation section, which includes potential risk factors for confusion.

In addition to QI compliance, we collected LOS, discharge disposition, and 30-day readmission data.

Generalized linear mixed models (GLMM) for binary clustered (ie, hierarchical) data were used to estimate compliance rates (ie, nurse adherence) for each group (intervention group or control group) in the postintervention period, along with their corresponding 95% confidence intervals. GLMM was used to account for the hierarchical structure of the data: nursing units within a hospital. In order to calculate the Charlson Comorbidity Index, we extracted past medical history from the EMR.³¹

Subjects (N = 2,396) were included in the comparison of the intervention group vs control group for each of the following 4 ACOVE QI compliance measures: DVT, mobilization, bladder catheter, and delirium.

Of the 2,396 patient admissions, 530 were in the intervention unit and 1,866 were in the control unit. In the intervention group, the average age was 84.65 years, 75.58% were white and 47.21% were married. There was no difference in patient demographics between groups (Table 2).

QI 1: VTE Prophylaxis

Compliance with VTE prophylaxis was met in 78.3% of the intervention subjects and 76.5% of the controls (P < .4371) (Table 3). Of note, the rate of VTE prophylaxis was 57% in the intervention vs 39% in the control group (P < .0056), in the 554 patients for whom compliance was not met. Mechanical prophylaxis was used in 35.6% of intervention subjects vs 30.6 in the control (P = .048). Patients who received no form of prophylaxis were 0.5% in the intervention and 3% in the control (P = .027).

QI 2: Indwelling Bladder Catheters

Out of 2,396 subjects, 406 had an indwelling bladder catheter (16.9%). Compliance with the catheter was met in 72.2% of the intervention group vs 54.4% in the control group (P = .1061). An indication for indwelling bladder catheters was documented in 100% of the subjects. The average number of catheter days was 5.16 in the intervention vs 5.88 in the control (P < .2284). There was statistical significance in catheter compliance in the longer stay (>15 days) subjects, decreasing to 23.32% in the control group while staying constant in the intervention group 71.5% (P = .0006).

QI 3: Mobilization

Of the 2,396 patients, 1,991 (83.1%) were reported as ambulatory prior to admission. In the intervention vs control group, 74 (14%) vs 297 (15.7%), respectively, were nonambulatory. Overall compliance with Q3 was 62.9% in the intervention vs 48.2% in the control (P < .0001). More specifically, the average time to PT order in the intervention group was 1.83 days vs 2.22 days in the control group (P < .0051) and the time to PT evaluation was 2.14 days vs 2.42 days, respectively (P < .0108). In the intervention group, 84 patients (15.8%) did not have a PT consult vs 511 (27%) in the control group (P < .0001). The average times per subject in which the nurses documented the approximate number of feet ambulated was 6.48 in the intervention group vs 0.11 in the control group.

QI 4: Delirium Evaluation

In terms of nursing documentation indicating the presence of an acute confusional state, the intervention group had 148 out of 530 nursing notes (27.9%) vs 405 out of 1,866 in the control group (21.7%; P = .0027). However, utilization of the “acute confusion” parameter with documentation of a risk factor did not differ between the groups (5.8% in the intervention group vs 5.6% in the control group, P < .94).

LOS, Discharge Disposition, and 30-Day Readmissions

LOS did not differ between intervention and control groups (6.37 days vs 6.27 days, respectively), with a median of 5 days (P = .877). Discharge disposition in the 2 groups included the following: home/home with services (71.32% vs 68.7%), skilled nursing facility/assisted living/long-term care (24.34 versus 25.83), inpatient hospice/home hospice (2.64 vs 2.25), and expired (1.13 vs 1.77; P < .3282). In addition, 30-day readmissions did not differ (21% vs 20%, respectively, P = .41).

Our goal was to explore an evidence-based, standardized approach to improve the care of hospitalized older adults. This approach leverages existing automated EMR alert functions with an additional level of decision support for VEs, integrated into daily multidisciplinary rounds. The use of a daily checklist-based tool offers a cost-effective and practical pathway to distribute the burden of compliance responsibility amongst team members.

As we anticipated and similar to study findings in hospitalized medicine, geriatric trauma, and primary care, compliance with general care QIs was better than geriatric-focused QIs.^27,32 Wenger et al³³ demonstrated significant improvements with screening for falls and incontinence; however, screening for cognitive impairment did not improve in the outpatient setting by imbedding ACOVE QIs into routine physician practice.

Increased compliance with VTE prophylaxis and indwelling bladder catheters may be explained by national financial incentives for widespread implementation of EMR alert systems. Conversely, mobilization, delirium assessment, and management in hospitalized older adults don’t benefit from similar incentives.

VTE Prophylaxis

The American College of Chest Physicians (ACCP) supports the use of VTE prophylaxis, especially in hospitalized older adults with decreased mobility.³⁴ While greater adoption of EMR has already increased adherence, our intervention resulted in an even higher rate of compliance with the use of pharmacologic VTE prophylaxis.³⁵ In the future, validated scores for risk of thrombosis and bleeding may be integrated into our QI-based checklist.

Indwelling Bladder Catheters

The potential harms of catheters have been described for over 50 years, yet remain frequently used.^36,37 Previous studies have shown success in decreasing catheter days with computer-based and multidisciplinary protocols.^36-39

Our health system’s EMR has built-in “soft” and “hard” alerts for indwelling bladder catheters, so we did not expect intervention-associated changes in compliance.

Mobilization

Hospitalization in older adults frequently results in functional decline.^4,5,40 In response, the mobilization QI recommends an ambulation plan within 48 hours for those patients who were ambulatory prior to admission; it does not specifically define the components of the plan.²⁶ There are several multicomponent interventions that have demonstrated improvement in functional decline, yet they require skilled providers.^41,42 Our intervention implemented specific ambulation plan components: daily ambulation and documentation reminders and early PT evaluation.

While functional status measures have existed for decades, most are primarily geared to assess community-residing individuals and not designed to measure changes in function during hospitalization.^43,44 Furthermore, performance-based hospital measures are difficult to integrate into the daily nursing workflow as they are time consuming.^45,46 In practice, nurses routinely use free text to document functional status in the hospital setting, rendering comparative analysis problematic. Yet, we demonstrated that nurses were more engaged in reporting mobilization (increased documentation of ambulation distance and a decrease in time to PT). Future research should focus on the development of a standardized tool, integrated into the EMR, to accurately measure function in the acute care setting.

Delirium Evaluation

Delirium evaluation remains one of the most difficult clinical challenges for healthcare providers in hospitalized individuals, and our study reiterated these concerns. Previous research has consistently demonstrated that the diagnosis of delirium is missed by up to 75% of clinicians.^47,48 Indeed, our study, which exclusively examined nursing documentation of the delirium evaluation QI, found that both groups showed strikingly low compliance rates. This may have been due to the fact that we only evaluated nursing documentation of suspected or definite diagnosis of delirium and a documented attempt to attribute the altered mental state to a potential etiology.³¹ By utilizing the concept of “key words,” as developed by Puelle et al.³⁰, we were able to demonstrate a statistically significant improvement in nursing delirium documentation in the intervention group. This result should be interpreted with caution, as this approach is not validated. Furthermore, our operational definition of delirium compliance (ie, nurse documentation of delirium, requiring the launching of a separate parameter) may have been simply too cumbersome to readily integrate into the daily workflow. Future research should study the efficacy of a sensitive EMR-integrated screening tool that facilitates recognition, by all team members, of acute changes in cognition.

Although a number of QI improved for the intervention group, acute care utilization measures such as LOS, discharge disposition, and 30-day readmissions did not differ between groups. It may well be that improving quality for this very frail, vulnerable population may simply not result in decreased utilization. Our ability to further decrease LOS and readmission rates may be limited due to restriction of range in this complex patient population (eg, median LOS value of 5 days).

Limitations

Although our study had a large sample size, data were only collected from a single-center and thus require further exploration in different settings to ensure generalizability. In addition, QI observance was based on the medical record, which was problematic for some indicators, notably delirium identification. While prior literature highlights the difficulty in identifying delirium, especially during clinical practice without specialized training, our compliance was strikingly low.⁴⁷ While validated measures such as CAM may have been included as part of the assessment, there is currently no EMR documentation of such measures and therefore, these data could not be obtained.

In summary, our study demonstrates the successful integration of the established ACOVE QIs as an intervention, rather than as an assessment method, for improving care of hospitalized older patients. By utilizing a checklist-based tool at the bedside allows the multidisciplinary team to implement evidence-based practices with the ultimate goal of standardizing care, not only for VEs, but potentially for other high-risk populations with multimorbidity.⁴⁹ This innovative approach provides a much-needed direction to healthcare providers in the ever increasing stressful conditions of today’s acute care environment and for the ultimate benefit and safety of our older patients.

Disclosure

The authors declare no conflicts of interest. This study was supported by New York State Empire Clinical Research Investigators Program (ECRIP). The sponsor had no role in the conception, study design, data collection, data analysis, interpretation of data, manuscript preparation, or the decision to submit the manuscript for publication.

In 2014, the United States spent $3 trillion on healthcare; hospitalization consumed 32% of these expenditures.¹ Today, Medicare patients account for over 50% of hospital days and over 30% of all hospital discharges in the United States.² Despite this staggering financial burden, hospitalization of older adults often results in poor patient outcomes.^3-6 The exponential growth of the hospitalist movement, from 350 hospitalists nationwide in 1995 to over 44,000 in 2014, has become the key strategy for providing care to hospitalized geriatric patients.^7-10 Most of these hospitalists have not received geriatric training.^11-15

There is growing evidence that a geriatric approach, emphasizing multidisciplinary management of the complex needs of older patients, leads to improved outcomes. Geriatric Evaluation and Management Units (GEMUs), such as Acute Care for Elderly (ACE) models, have demonstrated significant decreases in functional decline, institutionalization, and death in randomized controlled trials.^16,17 Multidisciplinary, nonunit based efforts, such as the mobile acute care of elderly (MACE), proactive consultation models (Sennour/Counsell), and the Hospital Elder Life Program (HELP), have demonstrated success in preventing adverse events and decreasing length of stay (LOS).^17-20

However, these models have not been systematically implemented due to challenges in generalizability and replicability in diverse settings. To address this concern, an alternative approach must be developed to widely “generalize” geriatric expertise throughout hospitals, regardless of their location, size, and resources. This initiative will require systematic integration of evidence-based decision support tools for the standardization of clinical management in hospitalized older adults.²¹

The 1998 Assessing Care of Vulnerable Elders (ACOVE) project developed a standardized tool to measure and evaluate the quality of care by using a comprehensive set of quality indicators (QIs) to improve the care of “vulnerable elders” (VEs) at a high risk for functional and cognitive decline and death.^22-24 The latest systematic review concludes that, although many studies have used ACOVE as an assessment tool of quality, there has been a dearth of studies investigating the ACOVE QIs as an intervention to improve patient care.²⁵

Our study investigated the role of ACOVE as an intervention by using the QIs as a standardized checklist in the acute care setting. We selected the 4 most commonly encountered QIs in the hospital setting, namely venous thrombosis prophylaxis (VTE), indwelling bladder catheter, mobilization, and delirium evaluation, in order to test the feasibility and impact of systematically implementing these ACOVE QIs as a therapeutic intervention for all hospitalized older adults.

This study (IRB #13-644B) was conducted using a prospective intervention with a nonequivalent control group design comprised of retrospective chart data from May 1, 2014, to June 30, 2015. Process and outcome variables were extracted from electronic medical records ([EMR], Sunrise Clinical Manager [SCM]) of 2,396 patients, with 530 patients in the intervention unit and 1,866 on the control units, at a large academic tertiary center operating in the greater New York metropolitan area. Our study investigated the role of ACOVE as an intervention to improve patient care by using selected QIs as a standardized checklist tool in the acute care setting. Of the original 30 hospital-specific QIs, our study focused on the care of older adults admitted to the medicine service.²⁶ We selected commonly encountered QIs, with the objective of testing the feasibility and impact of implementing the ACOVE QIs as an intervention to improve care of hospitalized older adults. This intervention consisted of applying the checklist tool, constructed with 4 selected ACOVE QIs and administered daily during interdisciplinary rounds, namely: 2 general “medical” indicators, VTE prophylaxis and indwelling bladder catheters, and 2 “geriatric”-focused indicators, mobilization and delirium evaluation.

Subject matter experts (hospitalists, geriatricians, researchers, administrators, and nurses) reviewed the ACOVE QIs and agreed upon the adaptation of the QIs from a quality measure assessment into a feasible and acceptable intervention checklist tool (Table 1). The checklist was reviewed during daily interdisciplinary rounds for all patients 75 years and older. While ACOVE defined vulnerable elders by using the Vulnerable Elder Screen (VES), we wanted to apply this intervention more broadly to all hospitalized older adults who are most at risk for poor outcomes.²⁷ Patients admitted to the intensive care unit, inpatient psychiatry, inpatient leukemia/lymphoma, and surgical services were excluded.

Daily interdisciplinary rounds are held on every one of the five 40-bed medical units; they last approximately 1 hour, and consist of a lead hospitalist, nurse manager, nurse practitioners, case managers, and the nursing staff. During interdisciplinary rounds, nurses present the case to the team members who then discuss the care plan. These 5 medical units did not differ in terms of patient characteristics or staffing patterns; the intervention unit was chosen simply for logistical reasons, in that the principal investigator (PI) had been assigned to this unit prior to study start-up.

Prior to the intervention, LS held an education session for staff on the intervention unit staff (who participated on interdisciplinary rounds) to explain the concept of the ACOVE QI initiative and describe the four QIs selected for the study. Three subsequent educational sessions were held during the first week of the intervention, with new incoming staff receiving a brief individual educational session. The staff demonstrated significant knowledge improvement after session completion (pre/post mean score 70.6% vs 90.0%; P < .0001).

The Clinical Information System for the Health System EMR, The Eclipsys SCM, has alerts with different levels of severity from “soft” (user must acknowledge a recommendation) to “hard” (requires an action in order to proceed).

To measure compliance of the quality indicators, we collected the following variables:

QI 1: VTE prophylaxis

Through SCM, we collected type of VTE prophylaxis ordered (pharmacologic and/or mechanical) as well as start and stop dates for all agents. International normalized ratio levels were checked for patients receiving warfarin. Days of compliance were calculated.

QI 2: Indwelling Bladder Catheters

SCM data were collected on catheter entry and discontinuation dates, the presence of an indication, and order renewal for bladder catheter at least every 3 days.

QI 3: Mobilization

Ambulation status prior to admission was extracted from nursing documentation completed on admission to the medical ward. Patients documented as bedfast were categorized as nonambulatory prior to admission. Nursing documentation of activity level and amount of feet ambulated per nursing shift were collected. In addition, hospital day of physical therapy (PT) order and hospital days with PT performed were charted. Compliance with QI 3 in patients documented as ambulatory prior to hospital admission was recorded as present if there was a PT order within 48 hours of admission.

QI 4: Delirium Evaluation

During daily rounds, the hospitalist (PI) questioned nurses about delirium evaluation, using the first feature of the Confusion Assessment Method (CAM) as well as the “single question in delirium,” namely, “Is there evidence of an acute change in mental status from the patient’s baseline?” and “Do you think [name of patient] has been more confused lately?”^28,29 Because EMR does not contain a specified field for delirium screening and documentation, and patients are not routinely included in rounds, documentation with QI 4 was recorded using the “key words” method as described in the work by Puelle et al.³⁰ To extract SCM key words, nursing documentation of the “cognitive/perceptual/neurological exam” section of the EMR on admission and on all subsequent documentation (once per shift) was retrieved to identify acute changes in mental status (eg, “altered mental status, delirium/delirious, alert and oriented X 3, confused/confusion, disoriented, lethargy/lethargic”).³⁰ In addition, nurses were asked to activate an SCM parameter, “Acute Confusion” SCM parameter, in the nursing documentation section, which includes potential risk factors for confusion.

In addition to QI compliance, we collected LOS, discharge disposition, and 30-day readmission data.

Generalized linear mixed models (GLMM) for binary clustered (ie, hierarchical) data were used to estimate compliance rates (ie, nurse adherence) for each group (intervention group or control group) in the postintervention period, along with their corresponding 95% confidence intervals. GLMM was used to account for the hierarchical structure of the data: nursing units within a hospital. In order to calculate the Charlson Comorbidity Index, we extracted past medical history from the EMR.³¹

Subjects (N = 2,396) were included in the comparison of the intervention group vs control group for each of the following 4 ACOVE QI compliance measures: DVT, mobilization, bladder catheter, and delirium.

Of the 2,396 patient admissions, 530 were in the intervention unit and 1,866 were in the control unit. In the intervention group, the average age was 84.65 years, 75.58% were white and 47.21% were married. There was no difference in patient demographics between groups (Table 2).

QI 1: VTE Prophylaxis

Compliance with VTE prophylaxis was met in 78.3% of the intervention subjects and 76.5% of the controls (P < .4371) (Table 3). Of note, the rate of VTE prophylaxis was 57% in the intervention vs 39% in the control group (P < .0056), in the 554 patients for whom compliance was not met. Mechanical prophylaxis was used in 35.6% of intervention subjects vs 30.6 in the control (P = .048). Patients who received no form of prophylaxis were 0.5% in the intervention and 3% in the control (P = .027).

QI 2: Indwelling Bladder Catheters

Out of 2,396 subjects, 406 had an indwelling bladder catheter (16.9%). Compliance with the catheter was met in 72.2% of the intervention group vs 54.4% in the control group (P = .1061). An indication for indwelling bladder catheters was documented in 100% of the subjects. The average number of catheter days was 5.16 in the intervention vs 5.88 in the control (P < .2284). There was statistical significance in catheter compliance in the longer stay (>15 days) subjects, decreasing to 23.32% in the control group while staying constant in the intervention group 71.5% (P = .0006).

QI 3: Mobilization

Of the 2,396 patients, 1,991 (83.1%) were reported as ambulatory prior to admission. In the intervention vs control group, 74 (14%) vs 297 (15.7%), respectively, were nonambulatory. Overall compliance with Q3 was 62.9% in the intervention vs 48.2% in the control (P < .0001). More specifically, the average time to PT order in the intervention group was 1.83 days vs 2.22 days in the control group (P < .0051) and the time to PT evaluation was 2.14 days vs 2.42 days, respectively (P < .0108). In the intervention group, 84 patients (15.8%) did not have a PT consult vs 511 (27%) in the control group (P < .0001). The average times per subject in which the nurses documented the approximate number of feet ambulated was 6.48 in the intervention group vs 0.11 in the control group.

QI 4: Delirium Evaluation

In terms of nursing documentation indicating the presence of an acute confusional state, the intervention group had 148 out of 530 nursing notes (27.9%) vs 405 out of 1,866 in the control group (21.7%; P = .0027). However, utilization of the “acute confusion” parameter with documentation of a risk factor did not differ between the groups (5.8% in the intervention group vs 5.6% in the control group, P < .94).

LOS, Discharge Disposition, and 30-Day Readmissions

LOS did not differ between intervention and control groups (6.37 days vs 6.27 days, respectively), with a median of 5 days (P = .877). Discharge disposition in the 2 groups included the following: home/home with services (71.32% vs 68.7%), skilled nursing facility/assisted living/long-term care (24.34 versus 25.83), inpatient hospice/home hospice (2.64 vs 2.25), and expired (1.13 vs 1.77; P < .3282). In addition, 30-day readmissions did not differ (21% vs 20%, respectively, P = .41).

Our goal was to explore an evidence-based, standardized approach to improve the care of hospitalized older adults. This approach leverages existing automated EMR alert functions with an additional level of decision support for VEs, integrated into daily multidisciplinary rounds. The use of a daily checklist-based tool offers a cost-effective and practical pathway to distribute the burden of compliance responsibility amongst team members.

As we anticipated and similar to study findings in hospitalized medicine, geriatric trauma, and primary care, compliance with general care QIs was better than geriatric-focused QIs.^27,32 Wenger et al³³ demonstrated significant improvements with screening for falls and incontinence; however, screening for cognitive impairment did not improve in the outpatient setting by imbedding ACOVE QIs into routine physician practice.

Increased compliance with VTE prophylaxis and indwelling bladder catheters may be explained by national financial incentives for widespread implementation of EMR alert systems. Conversely, mobilization, delirium assessment, and management in hospitalized older adults don’t benefit from similar incentives.

VTE Prophylaxis

The American College of Chest Physicians (ACCP) supports the use of VTE prophylaxis, especially in hospitalized older adults with decreased mobility.³⁴ While greater adoption of EMR has already increased adherence, our intervention resulted in an even higher rate of compliance with the use of pharmacologic VTE prophylaxis.³⁵ In the future, validated scores for risk of thrombosis and bleeding may be integrated into our QI-based checklist.

Indwelling Bladder Catheters

The potential harms of catheters have been described for over 50 years, yet remain frequently used.^36,37 Previous studies have shown success in decreasing catheter days with computer-based and multidisciplinary protocols.^36-39

Our health system’s EMR has built-in “soft” and “hard” alerts for indwelling bladder catheters, so we did not expect intervention-associated changes in compliance.

Mobilization

Hospitalization in older adults frequently results in functional decline.^4,5,40 In response, the mobilization QI recommends an ambulation plan within 48 hours for those patients who were ambulatory prior to admission; it does not specifically define the components of the plan.²⁶ There are several multicomponent interventions that have demonstrated improvement in functional decline, yet they require skilled providers.^41,42 Our intervention implemented specific ambulation plan components: daily ambulation and documentation reminders and early PT evaluation.

While functional status measures have existed for decades, most are primarily geared to assess community-residing individuals and not designed to measure changes in function during hospitalization.^43,44 Furthermore, performance-based hospital measures are difficult to integrate into the daily nursing workflow as they are time consuming.^45,46 In practice, nurses routinely use free text to document functional status in the hospital setting, rendering comparative analysis problematic. Yet, we demonstrated that nurses were more engaged in reporting mobilization (increased documentation of ambulation distance and a decrease in time to PT). Future research should focus on the development of a standardized tool, integrated into the EMR, to accurately measure function in the acute care setting.

Delirium Evaluation

Delirium evaluation remains one of the most difficult clinical challenges for healthcare providers in hospitalized individuals, and our study reiterated these concerns. Previous research has consistently demonstrated that the diagnosis of delirium is missed by up to 75% of clinicians.^47,48 Indeed, our study, which exclusively examined nursing documentation of the delirium evaluation QI, found that both groups showed strikingly low compliance rates. This may have been due to the fact that we only evaluated nursing documentation of suspected or definite diagnosis of delirium and a documented attempt to attribute the altered mental state to a potential etiology.³¹ By utilizing the concept of “key words,” as developed by Puelle et al.³⁰, we were able to demonstrate a statistically significant improvement in nursing delirium documentation in the intervention group. This result should be interpreted with caution, as this approach is not validated. Furthermore, our operational definition of delirium compliance (ie, nurse documentation of delirium, requiring the launching of a separate parameter) may have been simply too cumbersome to readily integrate into the daily workflow. Future research should study the efficacy of a sensitive EMR-integrated screening tool that facilitates recognition, by all team members, of acute changes in cognition.

Although a number of QI improved for the intervention group, acute care utilization measures such as LOS, discharge disposition, and 30-day readmissions did not differ between groups. It may well be that improving quality for this very frail, vulnerable population may simply not result in decreased utilization. Our ability to further decrease LOS and readmission rates may be limited due to restriction of range in this complex patient population (eg, median LOS value of 5 days).

Limitations

Although our study had a large sample size, data were only collected from a single-center and thus require further exploration in different settings to ensure generalizability. In addition, QI observance was based on the medical record, which was problematic for some indicators, notably delirium identification. While prior literature highlights the difficulty in identifying delirium, especially during clinical practice without specialized training, our compliance was strikingly low.⁴⁷ While validated measures such as CAM may have been included as part of the assessment, there is currently no EMR documentation of such measures and therefore, these data could not be obtained.

In summary, our study demonstrates the successful integration of the established ACOVE QIs as an intervention, rather than as an assessment method, for improving care of hospitalized older patients. By utilizing a checklist-based tool at the bedside allows the multidisciplinary team to implement evidence-based practices with the ultimate goal of standardizing care, not only for VEs, but potentially for other high-risk populations with multimorbidity.⁴⁹ This innovative approach provides a much-needed direction to healthcare providers in the ever increasing stressful conditions of today’s acute care environment and for the ultimate benefit and safety of our older patients.

Disclosure

The authors declare no conflicts of interest. This study was supported by New York State Empire Clinical Research Investigators Program (ECRIP). The sponsor had no role in the conception, study design, data collection, data analysis, interpretation of data, manuscript preparation, or the decision to submit the manuscript for publication.

In 2014, the United States spent $3 trillion on healthcare; hospitalization consumed 32% of these expenditures.¹ Today, Medicare patients account for over 50% of hospital days and over 30% of all hospital discharges in the United States.² Despite this staggering financial burden, hospitalization of older adults often results in poor patient outcomes.^3-6 The exponential growth of the hospitalist movement, from 350 hospitalists nationwide in 1995 to over 44,000 in 2014, has become the key strategy for providing care to hospitalized geriatric patients.^7-10 Most of these hospitalists have not received geriatric training.^11-15

There is growing evidence that a geriatric approach, emphasizing multidisciplinary management of the complex needs of older patients, leads to improved outcomes. Geriatric Evaluation and Management Units (GEMUs), such as Acute Care for Elderly (ACE) models, have demonstrated significant decreases in functional decline, institutionalization, and death in randomized controlled trials.^16,17 Multidisciplinary, nonunit based efforts, such as the mobile acute care of elderly (MACE), proactive consultation models (Sennour/Counsell), and the Hospital Elder Life Program (HELP), have demonstrated success in preventing adverse events and decreasing length of stay (LOS).^17-20

However, these models have not been systematically implemented due to challenges in generalizability and replicability in diverse settings. To address this concern, an alternative approach must be developed to widely “generalize” geriatric expertise throughout hospitals, regardless of their location, size, and resources. This initiative will require systematic integration of evidence-based decision support tools for the standardization of clinical management in hospitalized older adults.²¹

The 1998 Assessing Care of Vulnerable Elders (ACOVE) project developed a standardized tool to measure and evaluate the quality of care by using a comprehensive set of quality indicators (QIs) to improve the care of “vulnerable elders” (VEs) at a high risk for functional and cognitive decline and death.^22-24 The latest systematic review concludes that, although many studies have used ACOVE as an assessment tool of quality, there has been a dearth of studies investigating the ACOVE QIs as an intervention to improve patient care.²⁵

Our study investigated the role of ACOVE as an intervention by using the QIs as a standardized checklist in the acute care setting. We selected the 4 most commonly encountered QIs in the hospital setting, namely venous thrombosis prophylaxis (VTE), indwelling bladder catheter, mobilization, and delirium evaluation, in order to test the feasibility and impact of systematically implementing these ACOVE QIs as a therapeutic intervention for all hospitalized older adults.

This study (IRB #13-644B) was conducted using a prospective intervention with a nonequivalent control group design comprised of retrospective chart data from May 1, 2014, to June 30, 2015. Process and outcome variables were extracted from electronic medical records ([EMR], Sunrise Clinical Manager [SCM]) of 2,396 patients, with 530 patients in the intervention unit and 1,866 on the control units, at a large academic tertiary center operating in the greater New York metropolitan area. Our study investigated the role of ACOVE as an intervention to improve patient care by using selected QIs as a standardized checklist tool in the acute care setting. Of the original 30 hospital-specific QIs, our study focused on the care of older adults admitted to the medicine service.²⁶ We selected commonly encountered QIs, with the objective of testing the feasibility and impact of implementing the ACOVE QIs as an intervention to improve care of hospitalized older adults. This intervention consisted of applying the checklist tool, constructed with 4 selected ACOVE QIs and administered daily during interdisciplinary rounds, namely: 2 general “medical” indicators, VTE prophylaxis and indwelling bladder catheters, and 2 “geriatric”-focused indicators, mobilization and delirium evaluation.

Subject matter experts (hospitalists, geriatricians, researchers, administrators, and nurses) reviewed the ACOVE QIs and agreed upon the adaptation of the QIs from a quality measure assessment into a feasible and acceptable intervention checklist tool (Table 1). The checklist was reviewed during daily interdisciplinary rounds for all patients 75 years and older. While ACOVE defined vulnerable elders by using the Vulnerable Elder Screen (VES), we wanted to apply this intervention more broadly to all hospitalized older adults who are most at risk for poor outcomes.²⁷ Patients admitted to the intensive care unit, inpatient psychiatry, inpatient leukemia/lymphoma, and surgical services were excluded.

Daily interdisciplinary rounds are held on every one of the five 40-bed medical units; they last approximately 1 hour, and consist of a lead hospitalist, nurse manager, nurse practitioners, case managers, and the nursing staff. During interdisciplinary rounds, nurses present the case to the team members who then discuss the care plan. These 5 medical units did not differ in terms of patient characteristics or staffing patterns; the intervention unit was chosen simply for logistical reasons, in that the principal investigator (PI) had been assigned to this unit prior to study start-up.

Prior to the intervention, LS held an education session for staff on the intervention unit staff (who participated on interdisciplinary rounds) to explain the concept of the ACOVE QI initiative and describe the four QIs selected for the study. Three subsequent educational sessions were held during the first week of the intervention, with new incoming staff receiving a brief individual educational session. The staff demonstrated significant knowledge improvement after session completion (pre/post mean score 70.6% vs 90.0%; P < .0001).

The Clinical Information System for the Health System EMR, The Eclipsys SCM, has alerts with different levels of severity from “soft” (user must acknowledge a recommendation) to “hard” (requires an action in order to proceed).

To measure compliance of the quality indicators, we collected the following variables:

QI 1: VTE prophylaxis

Through SCM, we collected type of VTE prophylaxis ordered (pharmacologic and/or mechanical) as well as start and stop dates for all agents. International normalized ratio levels were checked for patients receiving warfarin. Days of compliance were calculated.

QI 2: Indwelling Bladder Catheters

SCM data were collected on catheter entry and discontinuation dates, the presence of an indication, and order renewal for bladder catheter at least every 3 days.

QI 3: Mobilization

Ambulation status prior to admission was extracted from nursing documentation completed on admission to the medical ward. Patients documented as bedfast were categorized as nonambulatory prior to admission. Nursing documentation of activity level and amount of feet ambulated per nursing shift were collected. In addition, hospital day of physical therapy (PT) order and hospital days with PT performed were charted. Compliance with QI 3 in patients documented as ambulatory prior to hospital admission was recorded as present if there was a PT order within 48 hours of admission.

QI 4: Delirium Evaluation

During daily rounds, the hospitalist (PI) questioned nurses about delirium evaluation, using the first feature of the Confusion Assessment Method (CAM) as well as the “single question in delirium,” namely, “Is there evidence of an acute change in mental status from the patient’s baseline?” and “Do you think [name of patient] has been more confused lately?”^28,29 Because EMR does not contain a specified field for delirium screening and documentation, and patients are not routinely included in rounds, documentation with QI 4 was recorded using the “key words” method as described in the work by Puelle et al.³⁰ To extract SCM key words, nursing documentation of the “cognitive/perceptual/neurological exam” section of the EMR on admission and on all subsequent documentation (once per shift) was retrieved to identify acute changes in mental status (eg, “altered mental status, delirium/delirious, alert and oriented X 3, confused/confusion, disoriented, lethargy/lethargic”).³⁰ In addition, nurses were asked to activate an SCM parameter, “Acute Confusion” SCM parameter, in the nursing documentation section, which includes potential risk factors for confusion.

In addition to QI compliance, we collected LOS, discharge disposition, and 30-day readmission data.

Generalized linear mixed models (GLMM) for binary clustered (ie, hierarchical) data were used to estimate compliance rates (ie, nurse adherence) for each group (intervention group or control group) in the postintervention period, along with their corresponding 95% confidence intervals. GLMM was used to account for the hierarchical structure of the data: nursing units within a hospital. In order to calculate the Charlson Comorbidity Index, we extracted past medical history from the EMR.³¹

Subjects (N = 2,396) were included in the comparison of the intervention group vs control group for each of the following 4 ACOVE QI compliance measures: DVT, mobilization, bladder catheter, and delirium.

Of the 2,396 patient admissions, 530 were in the intervention unit and 1,866 were in the control unit. In the intervention group, the average age was 84.65 years, 75.58% were white and 47.21% were married. There was no difference in patient demographics between groups (Table 2).

QI 1: VTE Prophylaxis

Compliance with VTE prophylaxis was met in 78.3% of the intervention subjects and 76.5% of the controls (P < .4371) (Table 3). Of note, the rate of VTE prophylaxis was 57% in the intervention vs 39% in the control group (P < .0056), in the 554 patients for whom compliance was not met. Mechanical prophylaxis was used in 35.6% of intervention subjects vs 30.6 in the control (P = .048). Patients who received no form of prophylaxis were 0.5% in the intervention and 3% in the control (P = .027).

QI 2: Indwelling Bladder Catheters

Out of 2,396 subjects, 406 had an indwelling bladder catheter (16.9%). Compliance with the catheter was met in 72.2% of the intervention group vs 54.4% in the control group (P = .1061). An indication for indwelling bladder catheters was documented in 100% of the subjects. The average number of catheter days was 5.16 in the intervention vs 5.88 in the control (P < .2284). There was statistical significance in catheter compliance in the longer stay (>15 days) subjects, decreasing to 23.32% in the control group while staying constant in the intervention group 71.5% (P = .0006).

QI 3: Mobilization

Of the 2,396 patients, 1,991 (83.1%) were reported as ambulatory prior to admission. In the intervention vs control group, 74 (14%) vs 297 (15.7%), respectively, were nonambulatory. Overall compliance with Q3 was 62.9% in the intervention vs 48.2% in the control (P < .0001). More specifically, the average time to PT order in the intervention group was 1.83 days vs 2.22 days in the control group (P < .0051) and the time to PT evaluation was 2.14 days vs 2.42 days, respectively (P < .0108). In the intervention group, 84 patients (15.8%) did not have a PT consult vs 511 (27%) in the control group (P < .0001). The average times per subject in which the nurses documented the approximate number of feet ambulated was 6.48 in the intervention group vs 0.11 in the control group.

QI 4: Delirium Evaluation

In terms of nursing documentation indicating the presence of an acute confusional state, the intervention group had 148 out of 530 nursing notes (27.9%) vs 405 out of 1,866 in the control group (21.7%; P = .0027). However, utilization of the “acute confusion” parameter with documentation of a risk factor did not differ between the groups (5.8% in the intervention group vs 5.6% in the control group, P < .94).

LOS, Discharge Disposition, and 30-Day Readmissions

LOS did not differ between intervention and control groups (6.37 days vs 6.27 days, respectively), with a median of 5 days (P = .877). Discharge disposition in the 2 groups included the following: home/home with services (71.32% vs 68.7%), skilled nursing facility/assisted living/long-term care (24.34 versus 25.83), inpatient hospice/home hospice (2.64 vs 2.25), and expired (1.13 vs 1.77; P < .3282). In addition, 30-day readmissions did not differ (21% vs 20%, respectively, P = .41).

Our goal was to explore an evidence-based, standardized approach to improve the care of hospitalized older adults. This approach leverages existing automated EMR alert functions with an additional level of decision support for VEs, integrated into daily multidisciplinary rounds. The use of a daily checklist-based tool offers a cost-effective and practical pathway to distribute the burden of compliance responsibility amongst team members.

As we anticipated and similar to study findings in hospitalized medicine, geriatric trauma, and primary care, compliance with general care QIs was better than geriatric-focused QIs.^27,32 Wenger et al³³ demonstrated significant improvements with screening for falls and incontinence; however, screening for cognitive impairment did not improve in the outpatient setting by imbedding ACOVE QIs into routine physician practice.

Increased compliance with VTE prophylaxis and indwelling bladder catheters may be explained by national financial incentives for widespread implementation of EMR alert systems. Conversely, mobilization, delirium assessment, and management in hospitalized older adults don’t benefit from similar incentives.

VTE Prophylaxis

The American College of Chest Physicians (ACCP) supports the use of VTE prophylaxis, especially in hospitalized older adults with decreased mobility.³⁴ While greater adoption of EMR has already increased adherence, our intervention resulted in an even higher rate of compliance with the use of pharmacologic VTE prophylaxis.³⁵ In the future, validated scores for risk of thrombosis and bleeding may be integrated into our QI-based checklist.

Indwelling Bladder Catheters

The potential harms of catheters have been described for over 50 years, yet remain frequently used.^36,37 Previous studies have shown success in decreasing catheter days with computer-based and multidisciplinary protocols.^36-39

Our health system’s EMR has built-in “soft” and “hard” alerts for indwelling bladder catheters, so we did not expect intervention-associated changes in compliance.

Mobilization

Hospitalization in older adults frequently results in functional decline.^4,5,40 In response, the mobilization QI recommends an ambulation plan within 48 hours for those patients who were ambulatory prior to admission; it does not specifically define the components of the plan.²⁶ There are several multicomponent interventions that have demonstrated improvement in functional decline, yet they require skilled providers.^41,42 Our intervention implemented specific ambulation plan components: daily ambulation and documentation reminders and early PT evaluation.

While functional status measures have existed for decades, most are primarily geared to assess community-residing individuals and not designed to measure changes in function during hospitalization.^43,44 Furthermore, performance-based hospital measures are difficult to integrate into the daily nursing workflow as they are time consuming.^45,46 In practice, nurses routinely use free text to document functional status in the hospital setting, rendering comparative analysis problematic. Yet, we demonstrated that nurses were more engaged in reporting mobilization (increased documentation of ambulation distance and a decrease in time to PT). Future research should focus on the development of a standardized tool, integrated into the EMR, to accurately measure function in the acute care setting.

Delirium Evaluation

Delirium evaluation remains one of the most difficult clinical challenges for healthcare providers in hospitalized individuals, and our study reiterated these concerns. Previous research has consistently demonstrated that the diagnosis of delirium is missed by up to 75% of clinicians.^47,48 Indeed, our study, which exclusively examined nursing documentation of the delirium evaluation QI, found that both groups showed strikingly low compliance rates. This may have been due to the fact that we only evaluated nursing documentation of suspected or definite diagnosis of delirium and a documented attempt to attribute the altered mental state to a potential etiology.³¹ By utilizing the concept of “key words,” as developed by Puelle et al.³⁰, we were able to demonstrate a statistically significant improvement in nursing delirium documentation in the intervention group. This result should be interpreted with caution, as this approach is not validated. Furthermore, our operational definition of delirium compliance (ie, nurse documentation of delirium, requiring the launching of a separate parameter) may have been simply too cumbersome to readily integrate into the daily workflow. Future research should study the efficacy of a sensitive EMR-integrated screening tool that facilitates recognition, by all team members, of acute changes in cognition.

Although a number of QI improved for the intervention group, acute care utilization measures such as LOS, discharge disposition, and 30-day readmissions did not differ between groups. It may well be that improving quality for this very frail, vulnerable population may simply not result in decreased utilization. Our ability to further decrease LOS and readmission rates may be limited due to restriction of range in this complex patient population (eg, median LOS value of 5 days).

Limitations

Although our study had a large sample size, data were only collected from a single-center and thus require further exploration in different settings to ensure generalizability. In addition, QI observance was based on the medical record, which was problematic for some indicators, notably delirium identification. While prior literature highlights the difficulty in identifying delirium, especially during clinical practice without specialized training, our compliance was strikingly low.⁴⁷ While validated measures such as CAM may have been included as part of the assessment, there is currently no EMR documentation of such measures and therefore, these data could not be obtained.

In summary, our study demonstrates the successful integration of the established ACOVE QIs as an intervention, rather than as an assessment method, for improving care of hospitalized older patients. By utilizing a checklist-based tool at the bedside allows the multidisciplinary team to implement evidence-based practices with the ultimate goal of standardizing care, not only for VEs, but potentially for other high-risk populations with multimorbidity.⁴⁹ This innovative approach provides a much-needed direction to healthcare providers in the ever increasing stressful conditions of today’s acute care environment and for the ultimate benefit and safety of our older patients.

Disclosure

The authors declare no conflicts of interest. This study was supported by New York State Empire Clinical Research Investigators Program (ECRIP). The sponsor had no role in the conception, study design, data collection, data analysis, interpretation of data, manuscript preparation, or the decision to submit the manuscript for publication.

Fever in hospitalized patients is a nonspecific finding with many potential causes. Blood cultures (BC) are commonly obtained prior to commencing parenteral antibiotics in febrile patients. However, as many as 35% to 50% of positive BCs represent a contamination with organisms inoculated from the skin into culture bottles at the time of sample collection.^1-3 Such results represent false-positive BCs that can lead to unnecessary investigations and treatment.

Recently, Coburn et al. reviewed the severity of chills (graded on an ordinal scale) as the most useful predictor of true bacteremia (positive likelihood ratio [LR], 4.7; 95% confidence interval [CI], 3.0–7.2),^4-6 and the lack of the systemic inflammatory response syndrome (SIRS) criteria as the best negative indicator of true bacteremia with a negative LR of 0.09 (95% CI, 0.03-0.3).^6,7 We have also previously reported normal food consumption as a negative indicator of true bacteremia, with a 98.3% negative predictive value.⁸ Henderson’s Basic Principles of Nursing Care emphasizes the importance of evaluating whether a patient can eat and drink adequately,⁹ and the evaluation of a patient’s food consumption is a routine nursing staff practice, which is treated as vital sign in Japan, in contrast to nursing practices in the United States.

However, these data were the result of a single-center retrospective study using the nursing staff’s assessment of food consumption, and they cannot be generalized to larger patient populations. Therefore, the aim of this prospective, multicenter study was to measure the accuracy of food consumption and shaking chills as predictive factors for true bacteremia.

Study Design

This was a prospective multicenter observational study (UMIN ID: R000013768) involving 3 hospitals in Tokyo, Japan, that enrolled consecutive patients who had BCs obtained. This study was approved by the ethical committee at Juntendo University Nerima Hospital and each of the participating centers, and the study was conducted in accordance with the Declaration of Helsinki 1971, as revised in 1983. We evaluated 2,792 consecutive hospitalized patients (mean age, 68.9 ± 17.1 years; 55.3% men) who had BCs obtained between April 2013 and August 2014, inclusive. The indication for BC acquisition was at the discretion of the treating physician. The study protocol and the indication for BCs are described in detail elsewhere.⁸ We excluded patients with anorexia-inducing conditions such as gastrointestinal disease, including gastrointestinal bleeding, enterocolitis, gastric ulceration, peritonitis, appendicitis, cholangitis, pancreatitis, diverticulitis, and ischemic colitis. We also excluded patients receiving chemotherapy for malignancy. In this study, true bacteremia was defined as identical organisms isolated from 2 sets of blood cultures (a set refers to one aerobic bottle and one anaerobic bottle). Moreover, even if only one set of blood cultures was acquired, when the identified pathogen could account for the clinical presentation, we also defined this as true bacteremia. Briefly, contaminants were defined as organisms common to skin flora, including Bacillus species, coagulase-negative Staphylococcus, Corynebacterium species, and Micrococcus species, without isolation of an identical organism with the same antibiotic susceptibilities from another potentially infected site in a patient with incompatible clinical features and no risk factors for infection with the isolated organism. Single BCs that were positive for organisms that were unlikely to explain the patient’s symptoms were also considered as contaminants. Patients with contaminated BCs were excluded from the analyses.

Structure of Reliability Study Procedures

Nurses in the 3 different hospitals performed daily independent food consumption ratings during each patient’s stay. Interrater reliability assessments were conducted in the morning or afternoon, and none of the raters had access to the other nurses’ scores at any time. The study nurses performed simultaneous ratings during these assessments (one interacted with and rated the patient while the other observed and rated the same patient).

Prediction Variables of True Bacteremia


1. Food consumption. Assessment of food consumption has been previously described in detail.⁸ Briefly, we characterized the patients’ oral intake based on the meal taken immediately prior to the BCs. For example, if a fever developed at 2 pm, lunch consumption was evaluated. If a fever developed at 2 am, dinner consumption was evaluated. We categorized the patients into 3 groups: low food consumption (<50% consumed), moderate food consumption (>50% to <80% consumed), and high food consumption (>80% consumed). To simplify our prediction rule, we subsequently divided food consumption into just 2 groups: high food consumption, referred to as the “normal food consumption group,” and the combination of low and moderate food consumption, referred to as the “poor food consumption group.”

2. Chills. As done previously, the physician evaluated the patient for a history of chills at the time of BCs and classified the patients into 1 of 4 grades^4,5: “no chills,” the absence of any chills; “mild chills,” feeling cold, equivalent to needing an outer jacket; “moderate chills,” feeling very cold, equivalent to needing a thick blanket; and “shaking chills,” feeling extremely cold with rigors and generalized bodily shaking, even under a thick blanket. To distinguish between those patients who had shaking chills and those who did not, we divided the patients into 2 groups: the “shaking chills group” and the combination of none, mild, and moderate chills, referred to as the “negative shaking chills group.”

3. Other predictive variables. We considered the following additional predictive variables: age, gender, axillary body temperature (BT), heart rate (HR), systolic blood pressure (SBP), respiratory rate (RR), white blood cell count (WBC), and serum C-reactive protein level (CRP). These predictive variables were obtained immediately prior to the BCs. We defined SIRS based on standard criteria (HR >90 beats/m, RR >20/m, BT <36°C or >38°C, and a WBC <4 × 10³ WBC/μL or >12 × 10³ WBC/μL). Patients were subcategorized by age into 2 groups (≤69 years and >70 years). CRP levels were dichotomized as >10.0 mg/dL or ≤10.0 mg/dL. We reviewed the patients’ charts to determine whether they had received antibiotics. In the case of walk-in patients, we interviewed the patients regarding whether they had visited a clinic; if they had, they were questioned as to whether any antibiotic therapy had been prescribed.

Statistical Analysis

Continuous variables are presented as the mean with the associated standard deviation (SD). All potential variables predictive of true bacteremia are shown in Table 1. The variables were dichotomized by clinically meaningful thresholds and used as potential risk-adjusted variables. We calculated the sensitivity and specificity and positive and negative predictive value for each criterion. Multiple logistic regression analysis was used to select components that were significantly associated with true bacteremia (the level of statistical significance determined with maximum likelihood methods was set at P < .05). To visualize and quantify other aspects in the prediction of true bacteremia, a recursive partitioning analysis (RPA) was used to make a decision tree model for true bacteremia. This nonparametric regression method produces a classification tree following a series of nonsequential top-down binary splits. The tree-building process starts by considering a set of predictive variables and selects the variable that produces 2 subsets of participants with the greatest purity. Two factors are considered when splitting a node into its daughter nodes: the goodness of the split and the amount of impurity in the daughter nodes. The splitting process is repeated until further partitioning is no longer possible and the terminal nodes have been reached. Details on this method are discussed in Monte Carlo Calibration of Distributions of Partition Statistics (www.jmp.com).

Probability was considered significant at a value of P < .05. All statistical tests were 2-tailed. Statistical analyses were conducted by a physician (KI) and an independent statistician (JM) with the use of the SPSS^® v.16.0 software package (SPSS Inc., Chicago, IL) and JMP^® version 8.0.2 (SAS Institute, Cary, NC).

Patients Characteristics

Two thousand seven hundred and ninety-two patients met the inclusion criteria for our study, from which 849 were excluded (see Figure 1 for flow diagram). Among the remaining 1,943 patients, there were 317 patients with positive BCs, of which 221 patients (69.7%) were considered to have true-positive BCs and 96 (30.3%) were considered to have contaminated BCs. After excluding these 96 patients, 221 patients with true bacteremia (true bacteremic group) were compared with 1,626 nonbacteremic patients (nonbacteremic group; Figure 1). The baseline characteristics of the subjects are shown in Table 1. The mean BT was 38.4 ± 1.2°C in the true bacteremic group and 37.9 ± 1.0°C in the nonbacteremic group. The mean serum CRP level was 11.6 ± 9.6 mg/dL in the true bacteremic group and 7.3 ± 6.9 mg/dL in the nonbacteremic group. In the true bacteremic group, there were 6 afebrile patients, and 27 patients without leukocytosis. The pathogens identified from the true-positive BCs were Escherichia coli (n = 59, 26.7%), including extended-spectrum beta-lactamase producing species, Staphylococcus aureus (n = 36, 16.3%), including methicillin-resistant Staphylococcus aureus, and Klebsiella pneumoniae (n = 22, 10.0%; Supplemental Table 1).

The underlying clinical diagnoses in the true bacteremic group included urinary tract infection (UTI), pneumonia, abscess, catheter-related bloodstream infection (CRBSI), cellulitis, osteomyelitis, infective endocarditis (IE), chorioamnionitis, iatrogenic infection at hemodialysis puncture sites, bacterial meningitis, septic arthritis, and infection of unknown cause (Supplemental Table 2).

Interrater Reliability Testing of Food Consumption

Patients were evaluated during their hospital stays. The interrater reliability of the evaluation of food consumption was very high across all participating hospitals (Supplemental Table 3). To assess the reliability of the evaluations of food consumption, patients (separate from this main study) were selected randomly and evaluated independently by 2 nurses in 3 different hospitals. The kappa scores of agreement between the nurses at the 3 different hospitals were 0.83 (95% CI, 0.63-0.88), 0.90 (95% CI, 0.80-0.99), and 0.80 (95% CI, 0.67-0.99), respectively. The interrater reliability of food consumption evaluation by the nurses was very high at all participating hospitals.

Food Consumption

The low, moderate, and high food consumption groups consisted of 964 (52.1%), 306 (16.6%), and 577 (31.2%) patients, respectively (Table 1). Of these, 174 (18.0%), 33 (10.8%), and 14 (2.4%) patients, respectively, had true bacteremia. The presence of poor food consumption had a sensitivity of 93.7% (95% CI, 89.4%-97.9%), specificity of 34.6% (95% CI, 33.0%-36.2%), and a positive LR of 1.43 (95% CI, 1.37-1.50) for predicting true bacteremia. Conversely, the absence of poor food consumption (ie, normal food consumption) had a negative LR of 0.18 (95% CI, 0.17-0.19).

Chills

The no, mild, moderate, and shaking chills groups consisted of 1,514 (82.0%), 148 (8.0%), 53 (2.9%), and 132 (7.1%) patients, respectively (Table 1). Of these, 136 (9.0%), 25 (16.9%), 8 (15.1%), and 52 (39.4%) patients, respectively, had true bacteremia. The presence of shaking chills had a sensitivity of 23.5% (95% CI, 22.5%-24.6%), a specificity of 95.1% (95% CI, 90.7%-99.4%), and a positive LR of 4.78 (95% CI, 4.56–5.00) for predicting true bacteremia. Conversely, the absence of shaking chills had a negative LR of 0.80 (95% CI, 0.77-0.84).

Prediction Model for True Bacteremia

The components identified as significantly related to true bacteremia by multiple logistic regression analysis are indicated in Table 2. The significant predictors of true bacteremia were shaking chills (odds ratio [OR], 5.6; 95% CI, 3.6-8.6; P < .01), SBP <90 mmHg (OR, 3.1; 95% CI, 1.6-5.7; P < 01), CRP levels >10.0 mg/dL (OR, 2.2; 95% CI, 1.6-3.1; P < .01), BT <36°C or >38°C (OR, 1.8; 95% CI, 1.3-2.6; P < .01), WBC <4 × 10³/μL or >12 × 10³/μL (OR, 1.6; 95% CI, 1.2-2.3; P = .003), HR >90 bpm (OR, 1.5; 95% CI, 1.1-2.1; P = .021), and female (OR, 1.4; 95% CI, 1.0-1.9; P = .036). An RPA to create an ideal prediction model for patients with true bacteremia or nonbacteremia is shown in Figure 2. The original group consisted of 1,847 patients, including 221 patients with true bacteremia. The pretest probability of true bacteremia was 2.4% (14/577) for those with normal food consumption (Group 1) and 2.4% (13/552) for those with both normal food consumption and the absence of shaking chills (Group 2). Conversely, the pretest probability of true bacteremia was 16.3% (207/1270) for those with poor food consumption and 47.7% (51/107) for those with both poor food consumption and shaking chills. The patients with true bacteremia with normal food consumption and without shaking chills consisted of 4 cases of CRBSI and UTI, 2 cases of osteomyelitis, 1 case of IE, 1 case of chorioamnionitis, and 1 case for which the focus was unknown (Supplemental Table 4).

In this observational study, we evaluated if a simple algorithm using food consumption and shaking chills was useful for assessing whether a patient had true bacteremia. A 2-item screening checklist (nursing assessment of food consumption and shaking chills) had excellent statistical properties as a brief screening instrument for true bacteremia.

We have prospectively validated that food consumption, as assessed by nurses, is a reliable predictor of true bacteremia.⁸ A previous single-center retrospective study showed similar findings, but these could not be generalized across all institutions because of the limited nature of the study. In this multicenter study, we used 2 statistical methods to reduce selection bias. First, we performed a kappa analysis across the hospitals to evaluate the interrater reliability of the evaluation of food consumption. Second, we used an RPA (Figure 2), also known as a decision tree model. RPA is a step-by-step process by which a decision tree is constructed by either splitting or not splitting each node on the tree into 2 daughter nodes.¹⁰ By using this method, we successfully generated an ideal approach to predict true bacteremia using food consumption and shaking chills. After adjusting for food consumption and shaking chills, groups 1 to 2 had sequentially decreasing diagnoses of true bacteremia, varying from 221 patients to only 13 patients.

Appetite is influenced by many factors that are integrated by the brain, most importantly within the hypothalamus. Signals that impinge on the hypothalamic center include neural afferents, hormones, cytokines, and metabolites.¹¹ These factors elicit “sickness behavior,” which includes a decrease in food-motivated behavior.¹² Furthermore, exposure to pathogenic bacteria increases serotonin, which has been shown to decrease metabolism in amphid neurons by transcriptional and post-transcriptional mechanisms.¹³ Therefore, nonbacteremic patients retain their appetites. Shaking chills are a well-known predictor of true bacteremia.^4,5 Several cytokines, including tumor necrosis factor-alpha and interleukins 6 and 10, may be related to shaking chills.¹⁴ Coburn et al. reviewed that shaking chills appear to be useful for identifying true bacteremia (positive LR, 4.7; 95% CI, 3.0-7.2),^5,6 similar to our study. In our study, the pretest probability of true bacteremia was the same whether shaking chills was included or not (ie, 2.4% for normal food consumption and 2.4% for normal food consumption plus absence of shaking chills). This would seem to imply that the assessment of shaking chills does not appear to add anything over food assessment alone when trying to rule out bacteremia. Rather, shaking chills seem more important for ruling in bacteremia rather than ruling it out. Moreover, the recent retrospective study revealed that age >60 years (OR = 2.75, 95% CI, 1.23-6.48, P = .015), female sex (OR = 2.21, 95% CI, 1.07- 4.67, P = .038), heart rate >90 bpm (OR = 5.18, 95% CI, 2.25-12.48, P < .001) and neutrophil percentage >80% (OR = 3.61, 95% CI, 1.71- 8.00, P = .001) were independent risk factors for true bacteremia.¹⁵ Conversely, the lack of the SIRS criteria was reported as the best negative indicator of true bacteremia with a negative LR of 0.09 (95% CI, 0.03-0.3).^6,7 However, the evaluation of SIRS criteria requires the acquisition of laboratory data. To our knowledge, no previous prospective studies have evaluated food consumption in terms of a risk prediction for true bacteremia. This extremely simple model can enable a physician to make a rapid bedside estimation of the risk of true bacteremia.

The strengths of this study include its relatively large sample size, multicenter design, uniformity of data collection across sites, and completeness of data collection from study participants. All of these factors allowed for a robust analysis.

However, there are several limitations of this study. First, the physicians or nurses asked the patients about the presence of shaking chills when they obtained the BCs. It may be difficult for patients, especially elderly patients, to provide this information promptly and accurately. Some patients did not call the nurse when they had shaking chills, and the chills were not witnessed by a healthcare provider. However, we used a more specific definition for shaking chills: a feeling of being extremely cold with rigors and generalized bodily shaking, even under a thick blanket. Second, this algorithm is not applicable to patients with immunosuppressed states because none of the hospitals involved in this study perform bone marrow or organ transplantation. Third, although we included patients with dementia in our cohort, we did not specifically evaluate performance of the algorithm in patients with this medical condition. It is possible that the algorithm would not perform well in this subset of patients owing to their unreliable appetite and food intake. Fourth, some medications may affect appetite, leading to reduced food consumption. Although we have not considered the details of medications in this study, we found that the pretest probability of true bacteremia was low for those patients with normal food consumption regardless of whether the medication affected their appetites or not. However, the question of whether medications truly affect patients’ appetites concurrently with bacteremia would need to be specifically addressed in a future study.

CONCLUSION

In conclusion, we have established a simple algorithm to identify patients with suspected true bacteremia who require the acquisition of blood cultures. This extremely simple model can enable physicians to make a rapid bedside estimation of the risk of true bacteremia.

Acknowledgment

The authors thank Drs. H. Honda and S. Saint, and Ms. A. Okada for their helpful discussions with regard to this study; Ms. M. Takigawa for the collection of data; and Ms. T. Oguri for providing infectious disease consultation on the pathogenicity of the identified organisms.

Disclosure

This work was supported by JSPS KAKENHI Grant Number 15K19294 (to TK) and 20590840 (to KI) from the Japan Society for the Promotion of Science. The authors report no potential conflicts of interest relevant to this article.

Fever in hospitalized patients is a nonspecific finding with many potential causes. Blood cultures (BC) are commonly obtained prior to commencing parenteral antibiotics in febrile patients. However, as many as 35% to 50% of positive BCs represent a contamination with organisms inoculated from the skin into culture bottles at the time of sample collection.^1-3 Such results represent false-positive BCs that can lead to unnecessary investigations and treatment.

Recently, Coburn et al. reviewed the severity of chills (graded on an ordinal scale) as the most useful predictor of true bacteremia (positive likelihood ratio [LR], 4.7; 95% confidence interval [CI], 3.0–7.2),^4-6 and the lack of the systemic inflammatory response syndrome (SIRS) criteria as the best negative indicator of true bacteremia with a negative LR of 0.09 (95% CI, 0.03-0.3).^6,7 We have also previously reported normal food consumption as a negative indicator of true bacteremia, with a 98.3% negative predictive value.⁸ Henderson’s Basic Principles of Nursing Care emphasizes the importance of evaluating whether a patient can eat and drink adequately,⁹ and the evaluation of a patient’s food consumption is a routine nursing staff practice, which is treated as vital sign in Japan, in contrast to nursing practices in the United States.

However, these data were the result of a single-center retrospective study using the nursing staff’s assessment of food consumption, and they cannot be generalized to larger patient populations. Therefore, the aim of this prospective, multicenter study was to measure the accuracy of food consumption and shaking chills as predictive factors for true bacteremia.

Study Design

This was a prospective multicenter observational study (UMIN ID: R000013768) involving 3 hospitals in Tokyo, Japan, that enrolled consecutive patients who had BCs obtained. This study was approved by the ethical committee at Juntendo University Nerima Hospital and each of the participating centers, and the study was conducted in accordance with the Declaration of Helsinki 1971, as revised in 1983. We evaluated 2,792 consecutive hospitalized patients (mean age, 68.9 ± 17.1 years; 55.3% men) who had BCs obtained between April 2013 and August 2014, inclusive. The indication for BC acquisition was at the discretion of the treating physician. The study protocol and the indication for BCs are described in detail elsewhere.⁸ We excluded patients with anorexia-inducing conditions such as gastrointestinal disease, including gastrointestinal bleeding, enterocolitis, gastric ulceration, peritonitis, appendicitis, cholangitis, pancreatitis, diverticulitis, and ischemic colitis. We also excluded patients receiving chemotherapy for malignancy. In this study, true bacteremia was defined as identical organisms isolated from 2 sets of blood cultures (a set refers to one aerobic bottle and one anaerobic bottle). Moreover, even if only one set of blood cultures was acquired, when the identified pathogen could account for the clinical presentation, we also defined this as true bacteremia. Briefly, contaminants were defined as organisms common to skin flora, including Bacillus species, coagulase-negative Staphylococcus, Corynebacterium species, and Micrococcus species, without isolation of an identical organism with the same antibiotic susceptibilities from another potentially infected site in a patient with incompatible clinical features and no risk factors for infection with the isolated organism. Single BCs that were positive for organisms that were unlikely to explain the patient’s symptoms were also considered as contaminants. Patients with contaminated BCs were excluded from the analyses.

Structure of Reliability Study Procedures

Nurses in the 3 different hospitals performed daily independent food consumption ratings during each patient’s stay. Interrater reliability assessments were conducted in the morning or afternoon, and none of the raters had access to the other nurses’ scores at any time. The study nurses performed simultaneous ratings during these assessments (one interacted with and rated the patient while the other observed and rated the same patient).

Prediction Variables of True Bacteremia


1. Food consumption. Assessment of food consumption has been previously described in detail.⁸ Briefly, we characterized the patients’ oral intake based on the meal taken immediately prior to the BCs. For example, if a fever developed at 2 pm, lunch consumption was evaluated. If a fever developed at 2 am, dinner consumption was evaluated. We categorized the patients into 3 groups: low food consumption (<50% consumed), moderate food consumption (>50% to <80% consumed), and high food consumption (>80% consumed). To simplify our prediction rule, we subsequently divided food consumption into just 2 groups: high food consumption, referred to as the “normal food consumption group,” and the combination of low and moderate food consumption, referred to as the “poor food consumption group.”

2. Chills. As done previously, the physician evaluated the patient for a history of chills at the time of BCs and classified the patients into 1 of 4 grades^4,5: “no chills,” the absence of any chills; “mild chills,” feeling cold, equivalent to needing an outer jacket; “moderate chills,” feeling very cold, equivalent to needing a thick blanket; and “shaking chills,” feeling extremely cold with rigors and generalized bodily shaking, even under a thick blanket. To distinguish between those patients who had shaking chills and those who did not, we divided the patients into 2 groups: the “shaking chills group” and the combination of none, mild, and moderate chills, referred to as the “negative shaking chills group.”

3. Other predictive variables. We considered the following additional predictive variables: age, gender, axillary body temperature (BT), heart rate (HR), systolic blood pressure (SBP), respiratory rate (RR), white blood cell count (WBC), and serum C-reactive protein level (CRP). These predictive variables were obtained immediately prior to the BCs. We defined SIRS based on standard criteria (HR >90 beats/m, RR >20/m, BT <36°C or >38°C, and a WBC <4 × 10³ WBC/μL or >12 × 10³ WBC/μL). Patients were subcategorized by age into 2 groups (≤69 years and >70 years). CRP levels were dichotomized as >10.0 mg/dL or ≤10.0 mg/dL. We reviewed the patients’ charts to determine whether they had received antibiotics. In the case of walk-in patients, we interviewed the patients regarding whether they had visited a clinic; if they had, they were questioned as to whether any antibiotic therapy had been prescribed.

Statistical Analysis

Continuous variables are presented as the mean with the associated standard deviation (SD). All potential variables predictive of true bacteremia are shown in Table 1. The variables were dichotomized by clinically meaningful thresholds and used as potential risk-adjusted variables. We calculated the sensitivity and specificity and positive and negative predictive value for each criterion. Multiple logistic regression analysis was used to select components that were significantly associated with true bacteremia (the level of statistical significance determined with maximum likelihood methods was set at P < .05). To visualize and quantify other aspects in the prediction of true bacteremia, a recursive partitioning analysis (RPA) was used to make a decision tree model for true bacteremia. This nonparametric regression method produces a classification tree following a series of nonsequential top-down binary splits. The tree-building process starts by considering a set of predictive variables and selects the variable that produces 2 subsets of participants with the greatest purity. Two factors are considered when splitting a node into its daughter nodes: the goodness of the split and the amount of impurity in the daughter nodes. The splitting process is repeated until further partitioning is no longer possible and the terminal nodes have been reached. Details on this method are discussed in Monte Carlo Calibration of Distributions of Partition Statistics (www.jmp.com).

Probability was considered significant at a value of P < .05. All statistical tests were 2-tailed. Statistical analyses were conducted by a physician (KI) and an independent statistician (JM) with the use of the SPSS^® v.16.0 software package (SPSS Inc., Chicago, IL) and JMP^® version 8.0.2 (SAS Institute, Cary, NC).

Patients Characteristics

Two thousand seven hundred and ninety-two patients met the inclusion criteria for our study, from which 849 were excluded (see Figure 1 for flow diagram). Among the remaining 1,943 patients, there were 317 patients with positive BCs, of which 221 patients (69.7%) were considered to have true-positive BCs and 96 (30.3%) were considered to have contaminated BCs. After excluding these 96 patients, 221 patients with true bacteremia (true bacteremic group) were compared with 1,626 nonbacteremic patients (nonbacteremic group; Figure 1). The baseline characteristics of the subjects are shown in Table 1. The mean BT was 38.4 ± 1.2°C in the true bacteremic group and 37.9 ± 1.0°C in the nonbacteremic group. The mean serum CRP level was 11.6 ± 9.6 mg/dL in the true bacteremic group and 7.3 ± 6.9 mg/dL in the nonbacteremic group. In the true bacteremic group, there were 6 afebrile patients, and 27 patients without leukocytosis. The pathogens identified from the true-positive BCs were Escherichia coli (n = 59, 26.7%), including extended-spectrum beta-lactamase producing species, Staphylococcus aureus (n = 36, 16.3%), including methicillin-resistant Staphylococcus aureus, and Klebsiella pneumoniae (n = 22, 10.0%; Supplemental Table 1).

The underlying clinical diagnoses in the true bacteremic group included urinary tract infection (UTI), pneumonia, abscess, catheter-related bloodstream infection (CRBSI), cellulitis, osteomyelitis, infective endocarditis (IE), chorioamnionitis, iatrogenic infection at hemodialysis puncture sites, bacterial meningitis, septic arthritis, and infection of unknown cause (Supplemental Table 2).

Interrater Reliability Testing of Food Consumption

Patients were evaluated during their hospital stays. The interrater reliability of the evaluation of food consumption was very high across all participating hospitals (Supplemental Table 3). To assess the reliability of the evaluations of food consumption, patients (separate from this main study) were selected randomly and evaluated independently by 2 nurses in 3 different hospitals. The kappa scores of agreement between the nurses at the 3 different hospitals were 0.83 (95% CI, 0.63-0.88), 0.90 (95% CI, 0.80-0.99), and 0.80 (95% CI, 0.67-0.99), respectively. The interrater reliability of food consumption evaluation by the nurses was very high at all participating hospitals.

Food Consumption

The low, moderate, and high food consumption groups consisted of 964 (52.1%), 306 (16.6%), and 577 (31.2%) patients, respectively (Table 1). Of these, 174 (18.0%), 33 (10.8%), and 14 (2.4%) patients, respectively, had true bacteremia. The presence of poor food consumption had a sensitivity of 93.7% (95% CI, 89.4%-97.9%), specificity of 34.6% (95% CI, 33.0%-36.2%), and a positive LR of 1.43 (95% CI, 1.37-1.50) for predicting true bacteremia. Conversely, the absence of poor food consumption (ie, normal food consumption) had a negative LR of 0.18 (95% CI, 0.17-0.19).

Chills

The no, mild, moderate, and shaking chills groups consisted of 1,514 (82.0%), 148 (8.0%), 53 (2.9%), and 132 (7.1%) patients, respectively (Table 1). Of these, 136 (9.0%), 25 (16.9%), 8 (15.1%), and 52 (39.4%) patients, respectively, had true bacteremia. The presence of shaking chills had a sensitivity of 23.5% (95% CI, 22.5%-24.6%), a specificity of 95.1% (95% CI, 90.7%-99.4%), and a positive LR of 4.78 (95% CI, 4.56–5.00) for predicting true bacteremia. Conversely, the absence of shaking chills had a negative LR of 0.80 (95% CI, 0.77-0.84).

Prediction Model for True Bacteremia

The components identified as significantly related to true bacteremia by multiple logistic regression analysis are indicated in Table 2. The significant predictors of true bacteremia were shaking chills (odds ratio [OR], 5.6; 95% CI, 3.6-8.6; P < .01), SBP <90 mmHg (OR, 3.1; 95% CI, 1.6-5.7; P < 01), CRP levels >10.0 mg/dL (OR, 2.2; 95% CI, 1.6-3.1; P < .01), BT <36°C or >38°C (OR, 1.8; 95% CI, 1.3-2.6; P < .01), WBC <4 × 10³/μL or >12 × 10³/μL (OR, 1.6; 95% CI, 1.2-2.3; P = .003), HR >90 bpm (OR, 1.5; 95% CI, 1.1-2.1; P = .021), and female (OR, 1.4; 95% CI, 1.0-1.9; P = .036). An RPA to create an ideal prediction model for patients with true bacteremia or nonbacteremia is shown in Figure 2. The original group consisted of 1,847 patients, including 221 patients with true bacteremia. The pretest probability of true bacteremia was 2.4% (14/577) for those with normal food consumption (Group 1) and 2.4% (13/552) for those with both normal food consumption and the absence of shaking chills (Group 2). Conversely, the pretest probability of true bacteremia was 16.3% (207/1270) for those with poor food consumption and 47.7% (51/107) for those with both poor food consumption and shaking chills. The patients with true bacteremia with normal food consumption and without shaking chills consisted of 4 cases of CRBSI and UTI, 2 cases of osteomyelitis, 1 case of IE, 1 case of chorioamnionitis, and 1 case for which the focus was unknown (Supplemental Table 4).

In this observational study, we evaluated if a simple algorithm using food consumption and shaking chills was useful for assessing whether a patient had true bacteremia. A 2-item screening checklist (nursing assessment of food consumption and shaking chills) had excellent statistical properties as a brief screening instrument for true bacteremia.

We have prospectively validated that food consumption, as assessed by nurses, is a reliable predictor of true bacteremia.⁸ A previous single-center retrospective study showed similar findings, but these could not be generalized across all institutions because of the limited nature of the study. In this multicenter study, we used 2 statistical methods to reduce selection bias. First, we performed a kappa analysis across the hospitals to evaluate the interrater reliability of the evaluation of food consumption. Second, we used an RPA (Figure 2), also known as a decision tree model. RPA is a step-by-step process by which a decision tree is constructed by either splitting or not splitting each node on the tree into 2 daughter nodes.¹⁰ By using this method, we successfully generated an ideal approach to predict true bacteremia using food consumption and shaking chills. After adjusting for food consumption and shaking chills, groups 1 to 2 had sequentially decreasing diagnoses of true bacteremia, varying from 221 patients to only 13 patients.

Appetite is influenced by many factors that are integrated by the brain, most importantly within the hypothalamus. Signals that impinge on the hypothalamic center include neural afferents, hormones, cytokines, and metabolites.¹¹ These factors elicit “sickness behavior,” which includes a decrease in food-motivated behavior.¹² Furthermore, exposure to pathogenic bacteria increases serotonin, which has been shown to decrease metabolism in amphid neurons by transcriptional and post-transcriptional mechanisms.¹³ Therefore, nonbacteremic patients retain their appetites. Shaking chills are a well-known predictor of true bacteremia.^4,5 Several cytokines, including tumor necrosis factor-alpha and interleukins 6 and 10, may be related to shaking chills.¹⁴ Coburn et al. reviewed that shaking chills appear to be useful for identifying true bacteremia (positive LR, 4.7; 95% CI, 3.0-7.2),^5,6 similar to our study. In our study, the pretest probability of true bacteremia was the same whether shaking chills was included or not (ie, 2.4% for normal food consumption and 2.4% for normal food consumption plus absence of shaking chills). This would seem to imply that the assessment of shaking chills does not appear to add anything over food assessment alone when trying to rule out bacteremia. Rather, shaking chills seem more important for ruling in bacteremia rather than ruling it out. Moreover, the recent retrospective study revealed that age >60 years (OR = 2.75, 95% CI, 1.23-6.48, P = .015), female sex (OR = 2.21, 95% CI, 1.07- 4.67, P = .038), heart rate >90 bpm (OR = 5.18, 95% CI, 2.25-12.48, P < .001) and neutrophil percentage >80% (OR = 3.61, 95% CI, 1.71- 8.00, P = .001) were independent risk factors for true bacteremia.¹⁵ Conversely, the lack of the SIRS criteria was reported as the best negative indicator of true bacteremia with a negative LR of 0.09 (95% CI, 0.03-0.3).^6,7 However, the evaluation of SIRS criteria requires the acquisition of laboratory data. To our knowledge, no previous prospective studies have evaluated food consumption in terms of a risk prediction for true bacteremia. This extremely simple model can enable a physician to make a rapid bedside estimation of the risk of true bacteremia.

The strengths of this study include its relatively large sample size, multicenter design, uniformity of data collection across sites, and completeness of data collection from study participants. All of these factors allowed for a robust analysis.

However, there are several limitations of this study. First, the physicians or nurses asked the patients about the presence of shaking chills when they obtained the BCs. It may be difficult for patients, especially elderly patients, to provide this information promptly and accurately. Some patients did not call the nurse when they had shaking chills, and the chills were not witnessed by a healthcare provider. However, we used a more specific definition for shaking chills: a feeling of being extremely cold with rigors and generalized bodily shaking, even under a thick blanket. Second, this algorithm is not applicable to patients with immunosuppressed states because none of the hospitals involved in this study perform bone marrow or organ transplantation. Third, although we included patients with dementia in our cohort, we did not specifically evaluate performance of the algorithm in patients with this medical condition. It is possible that the algorithm would not perform well in this subset of patients owing to their unreliable appetite and food intake. Fourth, some medications may affect appetite, leading to reduced food consumption. Although we have not considered the details of medications in this study, we found that the pretest probability of true bacteremia was low for those patients with normal food consumption regardless of whether the medication affected their appetites or not. However, the question of whether medications truly affect patients’ appetites concurrently with bacteremia would need to be specifically addressed in a future study.

CONCLUSION

In conclusion, we have established a simple algorithm to identify patients with suspected true bacteremia who require the acquisition of blood cultures. This extremely simple model can enable physicians to make a rapid bedside estimation of the risk of true bacteremia.

Acknowledgment

The authors thank Drs. H. Honda and S. Saint, and Ms. A. Okada for their helpful discussions with regard to this study; Ms. M. Takigawa for the collection of data; and Ms. T. Oguri for providing infectious disease consultation on the pathogenicity of the identified organisms.

Disclosure

This work was supported by JSPS KAKENHI Grant Number 15K19294 (to TK) and 20590840 (to KI) from the Japan Society for the Promotion of Science. The authors report no potential conflicts of interest relevant to this article.

Fever in hospitalized patients is a nonspecific finding with many potential causes. Blood cultures (BC) are commonly obtained prior to commencing parenteral antibiotics in febrile patients. However, as many as 35% to 50% of positive BCs represent a contamination with organisms inoculated from the skin into culture bottles at the time of sample collection.^1-3 Such results represent false-positive BCs that can lead to unnecessary investigations and treatment.

Recently, Coburn et al. reviewed the severity of chills (graded on an ordinal scale) as the most useful predictor of true bacteremia (positive likelihood ratio [LR], 4.7; 95% confidence interval [CI], 3.0–7.2),^4-6 and the lack of the systemic inflammatory response syndrome (SIRS) criteria as the best negative indicator of true bacteremia with a negative LR of 0.09 (95% CI, 0.03-0.3).^6,7 We have also previously reported normal food consumption as a negative indicator of true bacteremia, with a 98.3% negative predictive value.⁸ Henderson’s Basic Principles of Nursing Care emphasizes the importance of evaluating whether a patient can eat and drink adequately,⁹ and the evaluation of a patient’s food consumption is a routine nursing staff practice, which is treated as vital sign in Japan, in contrast to nursing practices in the United States.

However, these data were the result of a single-center retrospective study using the nursing staff’s assessment of food consumption, and they cannot be generalized to larger patient populations. Therefore, the aim of this prospective, multicenter study was to measure the accuracy of food consumption and shaking chills as predictive factors for true bacteremia.

Study Design

This was a prospective multicenter observational study (UMIN ID: R000013768) involving 3 hospitals in Tokyo, Japan, that enrolled consecutive patients who had BCs obtained. This study was approved by the ethical committee at Juntendo University Nerima Hospital and each of the participating centers, and the study was conducted in accordance with the Declaration of Helsinki 1971, as revised in 1983. We evaluated 2,792 consecutive hospitalized patients (mean age, 68.9 ± 17.1 years; 55.3% men) who had BCs obtained between April 2013 and August 2014, inclusive. The indication for BC acquisition was at the discretion of the treating physician. The study protocol and the indication for BCs are described in detail elsewhere.⁸ We excluded patients with anorexia-inducing conditions such as gastrointestinal disease, including gastrointestinal bleeding, enterocolitis, gastric ulceration, peritonitis, appendicitis, cholangitis, pancreatitis, diverticulitis, and ischemic colitis. We also excluded patients receiving chemotherapy for malignancy. In this study, true bacteremia was defined as identical organisms isolated from 2 sets of blood cultures (a set refers to one aerobic bottle and one anaerobic bottle). Moreover, even if only one set of blood cultures was acquired, when the identified pathogen could account for the clinical presentation, we also defined this as true bacteremia. Briefly, contaminants were defined as organisms common to skin flora, including Bacillus species, coagulase-negative Staphylococcus, Corynebacterium species, and Micrococcus species, without isolation of an identical organism with the same antibiotic susceptibilities from another potentially infected site in a patient with incompatible clinical features and no risk factors for infection with the isolated organism. Single BCs that were positive for organisms that were unlikely to explain the patient’s symptoms were also considered as contaminants. Patients with contaminated BCs were excluded from the analyses.

Structure of Reliability Study Procedures

Nurses in the 3 different hospitals performed daily independent food consumption ratings during each patient’s stay. Interrater reliability assessments were conducted in the morning or afternoon, and none of the raters had access to the other nurses’ scores at any time. The study nurses performed simultaneous ratings during these assessments (one interacted with and rated the patient while the other observed and rated the same patient).

Prediction Variables of True Bacteremia


1. Food consumption. Assessment of food consumption has been previously described in detail.⁸ Briefly, we characterized the patients’ oral intake based on the meal taken immediately prior to the BCs. For example, if a fever developed at 2 pm, lunch consumption was evaluated. If a fever developed at 2 am, dinner consumption was evaluated. We categorized the patients into 3 groups: low food consumption (<50% consumed), moderate food consumption (>50% to <80% consumed), and high food consumption (>80% consumed). To simplify our prediction rule, we subsequently divided food consumption into just 2 groups: high food consumption, referred to as the “normal food consumption group,” and the combination of low and moderate food consumption, referred to as the “poor food consumption group.”

2. Chills. As done previously, the physician evaluated the patient for a history of chills at the time of BCs and classified the patients into 1 of 4 grades^4,5: “no chills,” the absence of any chills; “mild chills,” feeling cold, equivalent to needing an outer jacket; “moderate chills,” feeling very cold, equivalent to needing a thick blanket; and “shaking chills,” feeling extremely cold with rigors and generalized bodily shaking, even under a thick blanket. To distinguish between those patients who had shaking chills and those who did not, we divided the patients into 2 groups: the “shaking chills group” and the combination of none, mild, and moderate chills, referred to as the “negative shaking chills group.”

3. Other predictive variables. We considered the following additional predictive variables: age, gender, axillary body temperature (BT), heart rate (HR), systolic blood pressure (SBP), respiratory rate (RR), white blood cell count (WBC), and serum C-reactive protein level (CRP). These predictive variables were obtained immediately prior to the BCs. We defined SIRS based on standard criteria (HR >90 beats/m, RR >20/m, BT <36°C or >38°C, and a WBC <4 × 10³ WBC/μL or >12 × 10³ WBC/μL). Patients were subcategorized by age into 2 groups (≤69 years and >70 years). CRP levels were dichotomized as >10.0 mg/dL or ≤10.0 mg/dL. We reviewed the patients’ charts to determine whether they had received antibiotics. In the case of walk-in patients, we interviewed the patients regarding whether they had visited a clinic; if they had, they were questioned as to whether any antibiotic therapy had been prescribed.

Statistical Analysis

Continuous variables are presented as the mean with the associated standard deviation (SD). All potential variables predictive of true bacteremia are shown in Table 1. The variables were dichotomized by clinically meaningful thresholds and used as potential risk-adjusted variables. We calculated the sensitivity and specificity and positive and negative predictive value for each criterion. Multiple logistic regression analysis was used to select components that were significantly associated with true bacteremia (the level of statistical significance determined with maximum likelihood methods was set at P < .05). To visualize and quantify other aspects in the prediction of true bacteremia, a recursive partitioning analysis (RPA) was used to make a decision tree model for true bacteremia. This nonparametric regression method produces a classification tree following a series of nonsequential top-down binary splits. The tree-building process starts by considering a set of predictive variables and selects the variable that produces 2 subsets of participants with the greatest purity. Two factors are considered when splitting a node into its daughter nodes: the goodness of the split and the amount of impurity in the daughter nodes. The splitting process is repeated until further partitioning is no longer possible and the terminal nodes have been reached. Details on this method are discussed in Monte Carlo Calibration of Distributions of Partition Statistics (www.jmp.com).

Probability was considered significant at a value of P < .05. All statistical tests were 2-tailed. Statistical analyses were conducted by a physician (KI) and an independent statistician (JM) with the use of the SPSS^® v.16.0 software package (SPSS Inc., Chicago, IL) and JMP^® version 8.0.2 (SAS Institute, Cary, NC).

Patients Characteristics

Two thousand seven hundred and ninety-two patients met the inclusion criteria for our study, from which 849 were excluded (see Figure 1 for flow diagram). Among the remaining 1,943 patients, there were 317 patients with positive BCs, of which 221 patients (69.7%) were considered to have true-positive BCs and 96 (30.3%) were considered to have contaminated BCs. After excluding these 96 patients, 221 patients with true bacteremia (true bacteremic group) were compared with 1,626 nonbacteremic patients (nonbacteremic group; Figure 1). The baseline characteristics of the subjects are shown in Table 1. The mean BT was 38.4 ± 1.2°C in the true bacteremic group and 37.9 ± 1.0°C in the nonbacteremic group. The mean serum CRP level was 11.6 ± 9.6 mg/dL in the true bacteremic group and 7.3 ± 6.9 mg/dL in the nonbacteremic group. In the true bacteremic group, there were 6 afebrile patients, and 27 patients without leukocytosis. The pathogens identified from the true-positive BCs were Escherichia coli (n = 59, 26.7%), including extended-spectrum beta-lactamase producing species, Staphylococcus aureus (n = 36, 16.3%), including methicillin-resistant Staphylococcus aureus, and Klebsiella pneumoniae (n = 22, 10.0%; Supplemental Table 1).

The underlying clinical diagnoses in the true bacteremic group included urinary tract infection (UTI), pneumonia, abscess, catheter-related bloodstream infection (CRBSI), cellulitis, osteomyelitis, infective endocarditis (IE), chorioamnionitis, iatrogenic infection at hemodialysis puncture sites, bacterial meningitis, septic arthritis, and infection of unknown cause (Supplemental Table 2).

Interrater Reliability Testing of Food Consumption

Patients were evaluated during their hospital stays. The interrater reliability of the evaluation of food consumption was very high across all participating hospitals (Supplemental Table 3). To assess the reliability of the evaluations of food consumption, patients (separate from this main study) were selected randomly and evaluated independently by 2 nurses in 3 different hospitals. The kappa scores of agreement between the nurses at the 3 different hospitals were 0.83 (95% CI, 0.63-0.88), 0.90 (95% CI, 0.80-0.99), and 0.80 (95% CI, 0.67-0.99), respectively. The interrater reliability of food consumption evaluation by the nurses was very high at all participating hospitals.

Food Consumption

The low, moderate, and high food consumption groups consisted of 964 (52.1%), 306 (16.6%), and 577 (31.2%) patients, respectively (Table 1). Of these, 174 (18.0%), 33 (10.8%), and 14 (2.4%) patients, respectively, had true bacteremia. The presence of poor food consumption had a sensitivity of 93.7% (95% CI, 89.4%-97.9%), specificity of 34.6% (95% CI, 33.0%-36.2%), and a positive LR of 1.43 (95% CI, 1.37-1.50) for predicting true bacteremia. Conversely, the absence of poor food consumption (ie, normal food consumption) had a negative LR of 0.18 (95% CI, 0.17-0.19).

Chills

The no, mild, moderate, and shaking chills groups consisted of 1,514 (82.0%), 148 (8.0%), 53 (2.9%), and 132 (7.1%) patients, respectively (Table 1). Of these, 136 (9.0%), 25 (16.9%), 8 (15.1%), and 52 (39.4%) patients, respectively, had true bacteremia. The presence of shaking chills had a sensitivity of 23.5% (95% CI, 22.5%-24.6%), a specificity of 95.1% (95% CI, 90.7%-99.4%), and a positive LR of 4.78 (95% CI, 4.56–5.00) for predicting true bacteremia. Conversely, the absence of shaking chills had a negative LR of 0.80 (95% CI, 0.77-0.84).

Prediction Model for True Bacteremia

The components identified as significantly related to true bacteremia by multiple logistic regression analysis are indicated in Table 2. The significant predictors of true bacteremia were shaking chills (odds ratio [OR], 5.6; 95% CI, 3.6-8.6; P < .01), SBP <90 mmHg (OR, 3.1; 95% CI, 1.6-5.7; P < 01), CRP levels >10.0 mg/dL (OR, 2.2; 95% CI, 1.6-3.1; P < .01), BT <36°C or >38°C (OR, 1.8; 95% CI, 1.3-2.6; P < .01), WBC <4 × 10³/μL or >12 × 10³/μL (OR, 1.6; 95% CI, 1.2-2.3; P = .003), HR >90 bpm (OR, 1.5; 95% CI, 1.1-2.1; P = .021), and female (OR, 1.4; 95% CI, 1.0-1.9; P = .036). An RPA to create an ideal prediction model for patients with true bacteremia or nonbacteremia is shown in Figure 2. The original group consisted of 1,847 patients, including 221 patients with true bacteremia. The pretest probability of true bacteremia was 2.4% (14/577) for those with normal food consumption (Group 1) and 2.4% (13/552) for those with both normal food consumption and the absence of shaking chills (Group 2). Conversely, the pretest probability of true bacteremia was 16.3% (207/1270) for those with poor food consumption and 47.7% (51/107) for those with both poor food consumption and shaking chills. The patients with true bacteremia with normal food consumption and without shaking chills consisted of 4 cases of CRBSI and UTI, 2 cases of osteomyelitis, 1 case of IE, 1 case of chorioamnionitis, and 1 case for which the focus was unknown (Supplemental Table 4).

In this observational study, we evaluated if a simple algorithm using food consumption and shaking chills was useful for assessing whether a patient had true bacteremia. A 2-item screening checklist (nursing assessment of food consumption and shaking chills) had excellent statistical properties as a brief screening instrument for true bacteremia.

We have prospectively validated that food consumption, as assessed by nurses, is a reliable predictor of true bacteremia.⁸ A previous single-center retrospective study showed similar findings, but these could not be generalized across all institutions because of the limited nature of the study. In this multicenter study, we used 2 statistical methods to reduce selection bias. First, we performed a kappa analysis across the hospitals to evaluate the interrater reliability of the evaluation of food consumption. Second, we used an RPA (Figure 2), also known as a decision tree model. RPA is a step-by-step process by which a decision tree is constructed by either splitting or not splitting each node on the tree into 2 daughter nodes.¹⁰ By using this method, we successfully generated an ideal approach to predict true bacteremia using food consumption and shaking chills. After adjusting for food consumption and shaking chills, groups 1 to 2 had sequentially decreasing diagnoses of true bacteremia, varying from 221 patients to only 13 patients.

Appetite is influenced by many factors that are integrated by the brain, most importantly within the hypothalamus. Signals that impinge on the hypothalamic center include neural afferents, hormones, cytokines, and metabolites.¹¹ These factors elicit “sickness behavior,” which includes a decrease in food-motivated behavior.¹² Furthermore, exposure to pathogenic bacteria increases serotonin, which has been shown to decrease metabolism in amphid neurons by transcriptional and post-transcriptional mechanisms.¹³ Therefore, nonbacteremic patients retain their appetites. Shaking chills are a well-known predictor of true bacteremia.^4,5 Several cytokines, including tumor necrosis factor-alpha and interleukins 6 and 10, may be related to shaking chills.¹⁴ Coburn et al. reviewed that shaking chills appear to be useful for identifying true bacteremia (positive LR, 4.7; 95% CI, 3.0-7.2),^5,6 similar to our study. In our study, the pretest probability of true bacteremia was the same whether shaking chills was included or not (ie, 2.4% for normal food consumption and 2.4% for normal food consumption plus absence of shaking chills). This would seem to imply that the assessment of shaking chills does not appear to add anything over food assessment alone when trying to rule out bacteremia. Rather, shaking chills seem more important for ruling in bacteremia rather than ruling it out. Moreover, the recent retrospective study revealed that age >60 years (OR = 2.75, 95% CI, 1.23-6.48, P = .015), female sex (OR = 2.21, 95% CI, 1.07- 4.67, P = .038), heart rate >90 bpm (OR = 5.18, 95% CI, 2.25-12.48, P < .001) and neutrophil percentage >80% (OR = 3.61, 95% CI, 1.71- 8.00, P = .001) were independent risk factors for true bacteremia.¹⁵ Conversely, the lack of the SIRS criteria was reported as the best negative indicator of true bacteremia with a negative LR of 0.09 (95% CI, 0.03-0.3).^6,7 However, the evaluation of SIRS criteria requires the acquisition of laboratory data. To our knowledge, no previous prospective studies have evaluated food consumption in terms of a risk prediction for true bacteremia. This extremely simple model can enable a physician to make a rapid bedside estimation of the risk of true bacteremia.

The strengths of this study include its relatively large sample size, multicenter design, uniformity of data collection across sites, and completeness of data collection from study participants. All of these factors allowed for a robust analysis.

However, there are several limitations of this study. First, the physicians or nurses asked the patients about the presence of shaking chills when they obtained the BCs. It may be difficult for patients, especially elderly patients, to provide this information promptly and accurately. Some patients did not call the nurse when they had shaking chills, and the chills were not witnessed by a healthcare provider. However, we used a more specific definition for shaking chills: a feeling of being extremely cold with rigors and generalized bodily shaking, even under a thick blanket. Second, this algorithm is not applicable to patients with immunosuppressed states because none of the hospitals involved in this study perform bone marrow or organ transplantation. Third, although we included patients with dementia in our cohort, we did not specifically evaluate performance of the algorithm in patients with this medical condition. It is possible that the algorithm would not perform well in this subset of patients owing to their unreliable appetite and food intake. Fourth, some medications may affect appetite, leading to reduced food consumption. Although we have not considered the details of medications in this study, we found that the pretest probability of true bacteremia was low for those patients with normal food consumption regardless of whether the medication affected their appetites or not. However, the question of whether medications truly affect patients’ appetites concurrently with bacteremia would need to be specifically addressed in a future study.

CONCLUSION

In conclusion, we have established a simple algorithm to identify patients with suspected true bacteremia who require the acquisition of blood cultures. This extremely simple model can enable physicians to make a rapid bedside estimation of the risk of true bacteremia.

Acknowledgment

The authors thank Drs. H. Honda and S. Saint, and Ms. A. Okada for their helpful discussions with regard to this study; Ms. M. Takigawa for the collection of data; and Ms. T. Oguri for providing infectious disease consultation on the pathogenicity of the identified organisms.

Disclosure

This work was supported by JSPS KAKENHI Grant Number 15K19294 (to TK) and 20590840 (to KI) from the Japan Society for the Promotion of Science. The authors report no potential conflicts of interest relevant to this article.

Implantable cardioverter-defibrillators (ICDs) offer lifesaving therapies to many patients and have been implanted in hundreds of thousands of patients.¹ The population of patients with ICDs is growing rapidly, and the national ICD Registry reports over 12,000 devices are implanted monthly.² This population includes patients with congenital heart disease, ischemic cardiomyopathy, and idiopathic arrhythmias. If these patients experience ventricular tachycardia or fibrillation, an ICD attempts to restore sinus rhythm and prevent death. While a shock from an ICD may be lifesaving, it can be a traumatic and startling experience for the patient and perhaps distressful for families to witness.^3,4

Although ICDs are intended to save lives, they do not slow the progress of the patient’s underlying cardiac and noncardiac comorbidities. All these patients will eventually die, whether from their cardiac disease or another condition. The literature includes many anecdotes about patients shocked multiple times by their defibrillator while actively dying.⁴ These situations could be prevented with preemptive ICD deactivation. (ICDs can function not only as cardioverters and defibrillators, as implied by their name, but also as pacemakers. “Deactivation” as used in this paper refers only to disabling the tachycardia therapies. No distinction was made between defibrillation with a shock and anti-tachycardia pacing.) Therefore, research on ICD deactivation has emphasized patients who are acutely terminally ill, while less emphasis has been placed on patients who are not actively dying.^4–8

Patients may, for a variety of reasons, request a do-not-resuscitate/do-not-intubate (DNR/DNI) order as their code status. However, it is not necessarily clear what a DNR/DNI order implies for ICD management. One survey of attending physicians found that 19% of respondents felt a DNR/DNI order was equivalent to requesting ICD deactivation.⁹ On the other hand, patients are split on whether they would want their device deactivated while in hospice or even at the very end of life.⁶ Heart Rhythm Society (HRS) guidelines favor a nuanced approach to ICD deactivation in DNR/DNI patients that emphasizes the individual patient’s comorbidities and goals.¹⁰ A patient’s individual circumstances might justify a choice to be DNR/DNI without deactivating the ICD. Decision-making in these circumstances requires a careful conversation between the patient and clinician. It is important to identify barriers that might prevent optimal shared decision-making.

Clinicians have been surveyed on ICD management at the end of life, but these studies have generally focused on attending physicians.^5,9,11 However, physician trainees (ie, residents and fellows) as well as advanced practice providers (ie, physician assistants and nurse practitioners) are responsible for much of the clinical care provided to hospitalized patients. In particular, they are often the clinicians to discuss code status with patients. Different specialties (eg, cardiology, general medicine, and geriatrics) manage different sets of patients, which might affect clinicians’ opinions on ICD management. We therefore designed a survey to assess clinician attitudes and beliefs regarding ICD deactivation, including in non-terminally ill patients, and to evaluate for differences according to training level and specialty.

Case-based and Likert-scale questions were considered for this survey, with the latter being chosen for ease of completion by respondents. An online survey tool (SurveyMonkey; San Mateo, CA) was used for data collection; no identifying data were collected. E-mail invitations to participate were sent to a combination of mailing lists and individual addresses for residents, fellows, advanced practice providers, and attending physicians in general internal medicine, cardiology, electrophysiology, and geriatrics. The survey remained open for 2.5 weeks. It was conducted 5 months into the academic year, thus trainees were well-established in their current roles. Two $25 gift cards were offered to respondents who entered their e-mail into a drawing; responses were not tied to e-mail addresses. Approval for the study was obtained from the University of Michigan Institutional Review Board.

The survey posed 12 questions assessing general attitudes about ICDs as well as individual beliefs and behaviors relating to ICD deactivation. Answers were on a Likert scale of 1 to 5 with 1 representing “strongly disagree” and 5 representing “strongly agree.” A score of 3 indicated “unsure or neutral.” The first 3 questions appeared together on the first page and were prefaced with “Please respond to the following statements about ICD shocks.” The next 9 were likewise grouped on the next page and were prefaced with “Please respond to the following statements about ICD deactivation.” All 12 questions are shown in Figures 1 and 2. Respondents could easily return to previous questions and change their answers. The survey ended with a third page showing 3 multiple choice demographic questions. The demographic questions were about clinical role (first-, second-, third-, or fourth-year resident, fellow, advanced practice provider, and attending), specialty, and number of ICD deactivations the respondent had been directly involved in (0, 1 to 5, 5 to 10, and more than 10). Specialty options were internal medicine resident, inpatient general medicine, outpatient general medicine, cardiology, electrophysiology, and geriatrics.

Likert scale answers of “agree” or “strongly agree” were grouped together as an affirmative response, while all other answers were grouped together as a nonaffirmative response. For analysis, residents were grouped together and their responses compared with attending physicians as a group. Additional analysis was done comparing attending physicians stratified by clinical specialty. Given the small number of responses from attending electrophysiologists, they were grouped with attending cardiologists for analysis. Due to the limited number of fellows and advanced practice providers who responded, further evaluation of these groups was not performed. Finally, the number of ICD deactivations respondents had been involved in was stratified by training level. All comparisons were performed using the two-tailed Pearson’s chi-squared test.

A total of 170 responses were collected from 508 individuals on the e-mail lists. Two responses were from registered nurses who were not part of the intended study sample and 7 responses were incomplete, having only answered the first 3 questions. These 9 responses were excluded from further analysis, yielding an overall response rate of 32%. The demographics of the remaining 161 respondents are shown in Table 1. Figure 1 shows overall responses to each question.

When comparing residents to attending physicians, there were no statistically significant between-differences except on questions 5 and 6. Specifically, residents were less comfortable than attending physicians discussing ICD deactivation and did so with less regularity (P < .001 and P = .018, respectively; Figure 2). Comfort levels improved markedly with experience: 29.2% of interns expressed comfort asking about ICD deactivation as compared with 60.7% of third- and-fourth year residents and 78.8% of attending physicians. Furthermore, comfort level seemed to parallel the regularity with which respondents asked about ICD deactivation: 4.2% of interns routinely asked about ICD deactivation as compared with 21.4% of third- and fourth-year residents and 34.8% of attending physicians.

Overall, our major findings were (1) residents, who provide much of the clinical care in a teaching hospital, are remarkably uncomfortable discussing ICD deactivation, (2) general internists and residents ask about ICD deactivation infrequently compared to geriatricians and cardiologists, and (3) about one fifth of our respondents believe ICD deactivation is automatically part of a DNR/DNI order.

Although the majority of respondents did not routinely address ICD deactivation in conjunction with code status, there was significant variability among subgroups. For example, 83.3% of geriatricians routinely discussed ICD deactivation as part of code status compared with only 4% of first-year residents and 10.5% of inpatient general internists. This finding is interesting because 90.7% of all respondents believed that discussions of code status should address preferences on ICD deactivation. This apparent discrepancy could be explained by the relatively small number of patients admitted to the hospital who have both an ICD and a request to be DNR/DNI. Residents and inpatient general internists see a very broad spectrum of patients; ICD deactivation is frequently irrelevant in the cases these physicians manage. The subset of patients seen in consultation by cardiologists and geriatricians, by contrast, is expected to include a larger proportion of patients with ICDs. Therefore, discussing ICD deactivation will be more relevant to their daily practice. Fear of alienating patients was not a reason for our findings, as our respondents did not express concern that recommending ICD deactivation would harm the patient-clinician relationship.

There are several possible reasons that residents, particularly interns, are uncomfortable discussing ICD deactivation. A lack of exposure to ICD deactivation is probably a key contributor. Over half of interns had never been involved in any ICD deactivations. Residents and hospitalists may also feel as if they are overstepping their boundaries to discuss deactivating ICD therapies. Their feelings may not be misplaced, as one survey of ICD patients found that over 75% thought responsibility for discussing ICD deactivation, at least at the end of life, rests with cardiologists or electrophysiologists.⁶

The HRS guidelines call for individualized decisions regarding ICD deactivation, even if a patient is DNR/DNI. However, our respondents frequently felt a standardized approach was indicated, with 21% believing that a DNR/DNI order included ICD deactivation. Additionally, 28% agreed that even non-terminally ill DNR/DNI patients should have their device deactivated. This is relevant because it is the role of clinicians to engage in shared decision-making with their patients. If the clinician holds the fixed belief that a DNR/DNI order, regardless of the precise clinical scenario, should include ICD deactivation, they may pressure a patient to have their device deactivated even if it could still benefit them.

In 2009, Kelley et al published results of a survey on ICD deactivation at the end of life.⁹ They contacted 4,876 attending physicians in cardiology, electrophysiology, geriatrics, and general medicine, receiving 558 responses. The survey included Likert-scale questions assessing attitudes and knowledge about ICD functionality. Demographic information was also collected, including how many patients in their practice had ICDs and how often they had previously discussed ICD deactivation.

There are some interesting comparisons between Kelley et al’s findings and ours, although we included trainees and the precise wording of questions was different. The specific questions used by Kelley et al to ask whether ICD shocks were painful or distressing and to ask if ICD deactivation is part of a DNR order were: “The shock from an ICD is very painful for most patients.” “The shock of an ICD at the end of life is distressing to a patient and their loved ones.” “A DNR order is equivalent to deactivation of an ICD.”

Only 47% of general internists in the Kelley et al survey thought that ICD shocks were painful, compared with 83% of electrophysiologists. In addition, 65% of general internists and 85% of electrophysiologists viewed shocks at the end of life to be distressing to patients and families. By contrast, our respondents were nearly unanimous in believing shocks to be painful and distressing. This discrepancy may be due to the growing prevalence of ICDs over the past several years as well as the growing body of literature on unnecessary shocks at the end of life. In line with our study, 19% of their respondents believed a DNR order was equivalent to ICD deactivation.⁹

Taken together, our findings indicate that additional education for clinicians of all levels could be helpful. Didactic lessons cannot replace experience, and it is important for residents to be exposed to discussions of ICD deactivation. However, lessons about ICD therapies and practical examples of how to broach the topic of deactivation could be beneficial, especially for interns whose responsibility includes discussions of code status. Within the context of an internal medicine residency, the fundamentals of ICD functionality could be covered during rotations on cardiology or palliative care services. Additionally, the recommendations of the HRS for device management can be covered in didactic sessions. Similar opportunities could be built into continuing medical education for practicing physicians and the training of advanced practice providers.

There are limitations to this survey, most notably the fact that it was restricted to a single academic medical center, the patient population and practices of which may not be generalizable to medical practice at large. Selection bias is also a distinct possibility given the 32% overall response rate; those who responded may feel more strongly about the survey topic. Our study subgroups may have interpreted questions differently because of their particular area of clinical practice. The small sample size also precluded an effective analysis of fellows and advanced practice practitioners due to lack of power. A major strength of this survey was the inclusion of a large number of residents upon whom the majority of inpatient contact rests. Future work could include expanding the survey to multiple medical centers, which would enhance generalizability and improve the ability to recruit sufficient fellows and advanced practice providers.

In summary, we conducted a single-center survey of residents, fellows, advanced practice providers, and attending physicians on their attitudes and beliefs about ICD deactivation in DNR/DNI patients. Residents are particularly uncomfortable discussing ICD deactivation with patients, which is an important finding because of their crucial role in providing patient care. Additionally, residents and hospitalists do not broach the topic of deactivation regularly, especially when compared to geriatricians and cardiologists. Despite HRS guidelines to the contrary, a fifth of our respondents believed that DNR/DNI orders include ICD deactivation. Overall, ICD deactivation in DNR/DNI patients is a topic that needs further attention in clinical education so that patients receive care that respects their individual wishes.

Disclosure

Nothing to report.

Implantable cardioverter-defibrillators (ICDs) offer lifesaving therapies to many patients and have been implanted in hundreds of thousands of patients.¹ The population of patients with ICDs is growing rapidly, and the national ICD Registry reports over 12,000 devices are implanted monthly.² This population includes patients with congenital heart disease, ischemic cardiomyopathy, and idiopathic arrhythmias. If these patients experience ventricular tachycardia or fibrillation, an ICD attempts to restore sinus rhythm and prevent death. While a shock from an ICD may be lifesaving, it can be a traumatic and startling experience for the patient and perhaps distressful for families to witness.^3,4

Although ICDs are intended to save lives, they do not slow the progress of the patient’s underlying cardiac and noncardiac comorbidities. All these patients will eventually die, whether from their cardiac disease or another condition. The literature includes many anecdotes about patients shocked multiple times by their defibrillator while actively dying.⁴ These situations could be prevented with preemptive ICD deactivation. (ICDs can function not only as cardioverters and defibrillators, as implied by their name, but also as pacemakers. “Deactivation” as used in this paper refers only to disabling the tachycardia therapies. No distinction was made between defibrillation with a shock and anti-tachycardia pacing.) Therefore, research on ICD deactivation has emphasized patients who are acutely terminally ill, while less emphasis has been placed on patients who are not actively dying.^4–8

Patients may, for a variety of reasons, request a do-not-resuscitate/do-not-intubate (DNR/DNI) order as their code status. However, it is not necessarily clear what a DNR/DNI order implies for ICD management. One survey of attending physicians found that 19% of respondents felt a DNR/DNI order was equivalent to requesting ICD deactivation.⁹ On the other hand, patients are split on whether they would want their device deactivated while in hospice or even at the very end of life.⁶ Heart Rhythm Society (HRS) guidelines favor a nuanced approach to ICD deactivation in DNR/DNI patients that emphasizes the individual patient’s comorbidities and goals.¹⁰ A patient’s individual circumstances might justify a choice to be DNR/DNI without deactivating the ICD. Decision-making in these circumstances requires a careful conversation between the patient and clinician. It is important to identify barriers that might prevent optimal shared decision-making.

Clinicians have been surveyed on ICD management at the end of life, but these studies have generally focused on attending physicians.^5,9,11 However, physician trainees (ie, residents and fellows) as well as advanced practice providers (ie, physician assistants and nurse practitioners) are responsible for much of the clinical care provided to hospitalized patients. In particular, they are often the clinicians to discuss code status with patients. Different specialties (eg, cardiology, general medicine, and geriatrics) manage different sets of patients, which might affect clinicians’ opinions on ICD management. We therefore designed a survey to assess clinician attitudes and beliefs regarding ICD deactivation, including in non-terminally ill patients, and to evaluate for differences according to training level and specialty.

Case-based and Likert-scale questions were considered for this survey, with the latter being chosen for ease of completion by respondents. An online survey tool (SurveyMonkey; San Mateo, CA) was used for data collection; no identifying data were collected. E-mail invitations to participate were sent to a combination of mailing lists and individual addresses for residents, fellows, advanced practice providers, and attending physicians in general internal medicine, cardiology, electrophysiology, and geriatrics. The survey remained open for 2.5 weeks. It was conducted 5 months into the academic year, thus trainees were well-established in their current roles. Two $25 gift cards were offered to respondents who entered their e-mail into a drawing; responses were not tied to e-mail addresses. Approval for the study was obtained from the University of Michigan Institutional Review Board.

The survey posed 12 questions assessing general attitudes about ICDs as well as individual beliefs and behaviors relating to ICD deactivation. Answers were on a Likert scale of 1 to 5 with 1 representing “strongly disagree” and 5 representing “strongly agree.” A score of 3 indicated “unsure or neutral.” The first 3 questions appeared together on the first page and were prefaced with “Please respond to the following statements about ICD shocks.” The next 9 were likewise grouped on the next page and were prefaced with “Please respond to the following statements about ICD deactivation.” All 12 questions are shown in Figures 1 and 2. Respondents could easily return to previous questions and change their answers. The survey ended with a third page showing 3 multiple choice demographic questions. The demographic questions were about clinical role (first-, second-, third-, or fourth-year resident, fellow, advanced practice provider, and attending), specialty, and number of ICD deactivations the respondent had been directly involved in (0, 1 to 5, 5 to 10, and more than 10). Specialty options were internal medicine resident, inpatient general medicine, outpatient general medicine, cardiology, electrophysiology, and geriatrics.

Likert scale answers of “agree” or “strongly agree” were grouped together as an affirmative response, while all other answers were grouped together as a nonaffirmative response. For analysis, residents were grouped together and their responses compared with attending physicians as a group. Additional analysis was done comparing attending physicians stratified by clinical specialty. Given the small number of responses from attending electrophysiologists, they were grouped with attending cardiologists for analysis. Due to the limited number of fellows and advanced practice providers who responded, further evaluation of these groups was not performed. Finally, the number of ICD deactivations respondents had been involved in was stratified by training level. All comparisons were performed using the two-tailed Pearson’s chi-squared test.

A total of 170 responses were collected from 508 individuals on the e-mail lists. Two responses were from registered nurses who were not part of the intended study sample and 7 responses were incomplete, having only answered the first 3 questions. These 9 responses were excluded from further analysis, yielding an overall response rate of 32%. The demographics of the remaining 161 respondents are shown in Table 1. Figure 1 shows overall responses to each question.

When comparing residents to attending physicians, there were no statistically significant between-differences except on questions 5 and 6. Specifically, residents were less comfortable than attending physicians discussing ICD deactivation and did so with less regularity (P < .001 and P = .018, respectively; Figure 2). Comfort levels improved markedly with experience: 29.2% of interns expressed comfort asking about ICD deactivation as compared with 60.7% of third- and-fourth year residents and 78.8% of attending physicians. Furthermore, comfort level seemed to parallel the regularity with which respondents asked about ICD deactivation: 4.2% of interns routinely asked about ICD deactivation as compared with 21.4% of third- and fourth-year residents and 34.8% of attending physicians.

Overall, our major findings were (1) residents, who provide much of the clinical care in a teaching hospital, are remarkably uncomfortable discussing ICD deactivation, (2) general internists and residents ask about ICD deactivation infrequently compared to geriatricians and cardiologists, and (3) about one fifth of our respondents believe ICD deactivation is automatically part of a DNR/DNI order.

Although the majority of respondents did not routinely address ICD deactivation in conjunction with code status, there was significant variability among subgroups. For example, 83.3% of geriatricians routinely discussed ICD deactivation as part of code status compared with only 4% of first-year residents and 10.5% of inpatient general internists. This finding is interesting because 90.7% of all respondents believed that discussions of code status should address preferences on ICD deactivation. This apparent discrepancy could be explained by the relatively small number of patients admitted to the hospital who have both an ICD and a request to be DNR/DNI. Residents and inpatient general internists see a very broad spectrum of patients; ICD deactivation is frequently irrelevant in the cases these physicians manage. The subset of patients seen in consultation by cardiologists and geriatricians, by contrast, is expected to include a larger proportion of patients with ICDs. Therefore, discussing ICD deactivation will be more relevant to their daily practice. Fear of alienating patients was not a reason for our findings, as our respondents did not express concern that recommending ICD deactivation would harm the patient-clinician relationship.

There are several possible reasons that residents, particularly interns, are uncomfortable discussing ICD deactivation. A lack of exposure to ICD deactivation is probably a key contributor. Over half of interns had never been involved in any ICD deactivations. Residents and hospitalists may also feel as if they are overstepping their boundaries to discuss deactivating ICD therapies. Their feelings may not be misplaced, as one survey of ICD patients found that over 75% thought responsibility for discussing ICD deactivation, at least at the end of life, rests with cardiologists or electrophysiologists.⁶

The HRS guidelines call for individualized decisions regarding ICD deactivation, even if a patient is DNR/DNI. However, our respondents frequently felt a standardized approach was indicated, with 21% believing that a DNR/DNI order included ICD deactivation. Additionally, 28% agreed that even non-terminally ill DNR/DNI patients should have their device deactivated. This is relevant because it is the role of clinicians to engage in shared decision-making with their patients. If the clinician holds the fixed belief that a DNR/DNI order, regardless of the precise clinical scenario, should include ICD deactivation, they may pressure a patient to have their device deactivated even if it could still benefit them.

In 2009, Kelley et al published results of a survey on ICD deactivation at the end of life.⁹ They contacted 4,876 attending physicians in cardiology, electrophysiology, geriatrics, and general medicine, receiving 558 responses. The survey included Likert-scale questions assessing attitudes and knowledge about ICD functionality. Demographic information was also collected, including how many patients in their practice had ICDs and how often they had previously discussed ICD deactivation.

There are some interesting comparisons between Kelley et al’s findings and ours, although we included trainees and the precise wording of questions was different. The specific questions used by Kelley et al to ask whether ICD shocks were painful or distressing and to ask if ICD deactivation is part of a DNR order were: “The shock from an ICD is very painful for most patients.” “The shock of an ICD at the end of life is distressing to a patient and their loved ones.” “A DNR order is equivalent to deactivation of an ICD.”

Only 47% of general internists in the Kelley et al survey thought that ICD shocks were painful, compared with 83% of electrophysiologists. In addition, 65% of general internists and 85% of electrophysiologists viewed shocks at the end of life to be distressing to patients and families. By contrast, our respondents were nearly unanimous in believing shocks to be painful and distressing. This discrepancy may be due to the growing prevalence of ICDs over the past several years as well as the growing body of literature on unnecessary shocks at the end of life. In line with our study, 19% of their respondents believed a DNR order was equivalent to ICD deactivation.⁹

Taken together, our findings indicate that additional education for clinicians of all levels could be helpful. Didactic lessons cannot replace experience, and it is important for residents to be exposed to discussions of ICD deactivation. However, lessons about ICD therapies and practical examples of how to broach the topic of deactivation could be beneficial, especially for interns whose responsibility includes discussions of code status. Within the context of an internal medicine residency, the fundamentals of ICD functionality could be covered during rotations on cardiology or palliative care services. Additionally, the recommendations of the HRS for device management can be covered in didactic sessions. Similar opportunities could be built into continuing medical education for practicing physicians and the training of advanced practice providers.

There are limitations to this survey, most notably the fact that it was restricted to a single academic medical center, the patient population and practices of which may not be generalizable to medical practice at large. Selection bias is also a distinct possibility given the 32% overall response rate; those who responded may feel more strongly about the survey topic. Our study subgroups may have interpreted questions differently because of their particular area of clinical practice. The small sample size also precluded an effective analysis of fellows and advanced practice practitioners due to lack of power. A major strength of this survey was the inclusion of a large number of residents upon whom the majority of inpatient contact rests. Future work could include expanding the survey to multiple medical centers, which would enhance generalizability and improve the ability to recruit sufficient fellows and advanced practice providers.

In summary, we conducted a single-center survey of residents, fellows, advanced practice providers, and attending physicians on their attitudes and beliefs about ICD deactivation in DNR/DNI patients. Residents are particularly uncomfortable discussing ICD deactivation with patients, which is an important finding because of their crucial role in providing patient care. Additionally, residents and hospitalists do not broach the topic of deactivation regularly, especially when compared to geriatricians and cardiologists. Despite HRS guidelines to the contrary, a fifth of our respondents believed that DNR/DNI orders include ICD deactivation. Overall, ICD deactivation in DNR/DNI patients is a topic that needs further attention in clinical education so that patients receive care that respects their individual wishes.

Disclosure

Nothing to report.

Implantable cardioverter-defibrillators (ICDs) offer lifesaving therapies to many patients and have been implanted in hundreds of thousands of patients.¹ The population of patients with ICDs is growing rapidly, and the national ICD Registry reports over 12,000 devices are implanted monthly.² This population includes patients with congenital heart disease, ischemic cardiomyopathy, and idiopathic arrhythmias. If these patients experience ventricular tachycardia or fibrillation, an ICD attempts to restore sinus rhythm and prevent death. While a shock from an ICD may be lifesaving, it can be a traumatic and startling experience for the patient and perhaps distressful for families to witness.^3,4

Although ICDs are intended to save lives, they do not slow the progress of the patient’s underlying cardiac and noncardiac comorbidities. All these patients will eventually die, whether from their cardiac disease or another condition. The literature includes many anecdotes about patients shocked multiple times by their defibrillator while actively dying.⁴ These situations could be prevented with preemptive ICD deactivation. (ICDs can function not only as cardioverters and defibrillators, as implied by their name, but also as pacemakers. “Deactivation” as used in this paper refers only to disabling the tachycardia therapies. No distinction was made between defibrillation with a shock and anti-tachycardia pacing.) Therefore, research on ICD deactivation has emphasized patients who are acutely terminally ill, while less emphasis has been placed on patients who are not actively dying.^4–8

Patients may, for a variety of reasons, request a do-not-resuscitate/do-not-intubate (DNR/DNI) order as their code status. However, it is not necessarily clear what a DNR/DNI order implies for ICD management. One survey of attending physicians found that 19% of respondents felt a DNR/DNI order was equivalent to requesting ICD deactivation.⁹ On the other hand, patients are split on whether they would want their device deactivated while in hospice or even at the very end of life.⁶ Heart Rhythm Society (HRS) guidelines favor a nuanced approach to ICD deactivation in DNR/DNI patients that emphasizes the individual patient’s comorbidities and goals.¹⁰ A patient’s individual circumstances might justify a choice to be DNR/DNI without deactivating the ICD. Decision-making in these circumstances requires a careful conversation between the patient and clinician. It is important to identify barriers that might prevent optimal shared decision-making.

Clinicians have been surveyed on ICD management at the end of life, but these studies have generally focused on attending physicians.^5,9,11 However, physician trainees (ie, residents and fellows) as well as advanced practice providers (ie, physician assistants and nurse practitioners) are responsible for much of the clinical care provided to hospitalized patients. In particular, they are often the clinicians to discuss code status with patients. Different specialties (eg, cardiology, general medicine, and geriatrics) manage different sets of patients, which might affect clinicians’ opinions on ICD management. We therefore designed a survey to assess clinician attitudes and beliefs regarding ICD deactivation, including in non-terminally ill patients, and to evaluate for differences according to training level and specialty.

Case-based and Likert-scale questions were considered for this survey, with the latter being chosen for ease of completion by respondents. An online survey tool (SurveyMonkey; San Mateo, CA) was used for data collection; no identifying data were collected. E-mail invitations to participate were sent to a combination of mailing lists and individual addresses for residents, fellows, advanced practice providers, and attending physicians in general internal medicine, cardiology, electrophysiology, and geriatrics. The survey remained open for 2.5 weeks. It was conducted 5 months into the academic year, thus trainees were well-established in their current roles. Two $25 gift cards were offered to respondents who entered their e-mail into a drawing; responses were not tied to e-mail addresses. Approval for the study was obtained from the University of Michigan Institutional Review Board.

The survey posed 12 questions assessing general attitudes about ICDs as well as individual beliefs and behaviors relating to ICD deactivation. Answers were on a Likert scale of 1 to 5 with 1 representing “strongly disagree” and 5 representing “strongly agree.” A score of 3 indicated “unsure or neutral.” The first 3 questions appeared together on the first page and were prefaced with “Please respond to the following statements about ICD shocks.” The next 9 were likewise grouped on the next page and were prefaced with “Please respond to the following statements about ICD deactivation.” All 12 questions are shown in Figures 1 and 2. Respondents could easily return to previous questions and change their answers. The survey ended with a third page showing 3 multiple choice demographic questions. The demographic questions were about clinical role (first-, second-, third-, or fourth-year resident, fellow, advanced practice provider, and attending), specialty, and number of ICD deactivations the respondent had been directly involved in (0, 1 to 5, 5 to 10, and more than 10). Specialty options were internal medicine resident, inpatient general medicine, outpatient general medicine, cardiology, electrophysiology, and geriatrics.

Likert scale answers of “agree” or “strongly agree” were grouped together as an affirmative response, while all other answers were grouped together as a nonaffirmative response. For analysis, residents were grouped together and their responses compared with attending physicians as a group. Additional analysis was done comparing attending physicians stratified by clinical specialty. Given the small number of responses from attending electrophysiologists, they were grouped with attending cardiologists for analysis. Due to the limited number of fellows and advanced practice providers who responded, further evaluation of these groups was not performed. Finally, the number of ICD deactivations respondents had been involved in was stratified by training level. All comparisons were performed using the two-tailed Pearson’s chi-squared test.

A total of 170 responses were collected from 508 individuals on the e-mail lists. Two responses were from registered nurses who were not part of the intended study sample and 7 responses were incomplete, having only answered the first 3 questions. These 9 responses were excluded from further analysis, yielding an overall response rate of 32%. The demographics of the remaining 161 respondents are shown in Table 1. Figure 1 shows overall responses to each question.

When comparing residents to attending physicians, there were no statistically significant between-differences except on questions 5 and 6. Specifically, residents were less comfortable than attending physicians discussing ICD deactivation and did so with less regularity (P < .001 and P = .018, respectively; Figure 2). Comfort levels improved markedly with experience: 29.2% of interns expressed comfort asking about ICD deactivation as compared with 60.7% of third- and-fourth year residents and 78.8% of attending physicians. Furthermore, comfort level seemed to parallel the regularity with which respondents asked about ICD deactivation: 4.2% of interns routinely asked about ICD deactivation as compared with 21.4% of third- and fourth-year residents and 34.8% of attending physicians.

Overall, our major findings were (1) residents, who provide much of the clinical care in a teaching hospital, are remarkably uncomfortable discussing ICD deactivation, (2) general internists and residents ask about ICD deactivation infrequently compared to geriatricians and cardiologists, and (3) about one fifth of our respondents believe ICD deactivation is automatically part of a DNR/DNI order.

Although the majority of respondents did not routinely address ICD deactivation in conjunction with code status, there was significant variability among subgroups. For example, 83.3% of geriatricians routinely discussed ICD deactivation as part of code status compared with only 4% of first-year residents and 10.5% of inpatient general internists. This finding is interesting because 90.7% of all respondents believed that discussions of code status should address preferences on ICD deactivation. This apparent discrepancy could be explained by the relatively small number of patients admitted to the hospital who have both an ICD and a request to be DNR/DNI. Residents and inpatient general internists see a very broad spectrum of patients; ICD deactivation is frequently irrelevant in the cases these physicians manage. The subset of patients seen in consultation by cardiologists and geriatricians, by contrast, is expected to include a larger proportion of patients with ICDs. Therefore, discussing ICD deactivation will be more relevant to their daily practice. Fear of alienating patients was not a reason for our findings, as our respondents did not express concern that recommending ICD deactivation would harm the patient-clinician relationship.

There are several possible reasons that residents, particularly interns, are uncomfortable discussing ICD deactivation. A lack of exposure to ICD deactivation is probably a key contributor. Over half of interns had never been involved in any ICD deactivations. Residents and hospitalists may also feel as if they are overstepping their boundaries to discuss deactivating ICD therapies. Their feelings may not be misplaced, as one survey of ICD patients found that over 75% thought responsibility for discussing ICD deactivation, at least at the end of life, rests with cardiologists or electrophysiologists.⁶

The HRS guidelines call for individualized decisions regarding ICD deactivation, even if a patient is DNR/DNI. However, our respondents frequently felt a standardized approach was indicated, with 21% believing that a DNR/DNI order included ICD deactivation. Additionally, 28% agreed that even non-terminally ill DNR/DNI patients should have their device deactivated. This is relevant because it is the role of clinicians to engage in shared decision-making with their patients. If the clinician holds the fixed belief that a DNR/DNI order, regardless of the precise clinical scenario, should include ICD deactivation, they may pressure a patient to have their device deactivated even if it could still benefit them.

In 2009, Kelley et al published results of a survey on ICD deactivation at the end of life.⁹ They contacted 4,876 attending physicians in cardiology, electrophysiology, geriatrics, and general medicine, receiving 558 responses. The survey included Likert-scale questions assessing attitudes and knowledge about ICD functionality. Demographic information was also collected, including how many patients in their practice had ICDs and how often they had previously discussed ICD deactivation.

There are some interesting comparisons between Kelley et al’s findings and ours, although we included trainees and the precise wording of questions was different. The specific questions used by Kelley et al to ask whether ICD shocks were painful or distressing and to ask if ICD deactivation is part of a DNR order were: “The shock from an ICD is very painful for most patients.” “The shock of an ICD at the end of life is distressing to a patient and their loved ones.” “A DNR order is equivalent to deactivation of an ICD.”

Only 47% of general internists in the Kelley et al survey thought that ICD shocks were painful, compared with 83% of electrophysiologists. In addition, 65% of general internists and 85% of electrophysiologists viewed shocks at the end of life to be distressing to patients and families. By contrast, our respondents were nearly unanimous in believing shocks to be painful and distressing. This discrepancy may be due to the growing prevalence of ICDs over the past several years as well as the growing body of literature on unnecessary shocks at the end of life. In line with our study, 19% of their respondents believed a DNR order was equivalent to ICD deactivation.⁹

Taken together, our findings indicate that additional education for clinicians of all levels could be helpful. Didactic lessons cannot replace experience, and it is important for residents to be exposed to discussions of ICD deactivation. However, lessons about ICD therapies and practical examples of how to broach the topic of deactivation could be beneficial, especially for interns whose responsibility includes discussions of code status. Within the context of an internal medicine residency, the fundamentals of ICD functionality could be covered during rotations on cardiology or palliative care services. Additionally, the recommendations of the HRS for device management can be covered in didactic sessions. Similar opportunities could be built into continuing medical education for practicing physicians and the training of advanced practice providers.

There are limitations to this survey, most notably the fact that it was restricted to a single academic medical center, the patient population and practices of which may not be generalizable to medical practice at large. Selection bias is also a distinct possibility given the 32% overall response rate; those who responded may feel more strongly about the survey topic. Our study subgroups may have interpreted questions differently because of their particular area of clinical practice. The small sample size also precluded an effective analysis of fellows and advanced practice practitioners due to lack of power. A major strength of this survey was the inclusion of a large number of residents upon whom the majority of inpatient contact rests. Future work could include expanding the survey to multiple medical centers, which would enhance generalizability and improve the ability to recruit sufficient fellows and advanced practice providers.

In summary, we conducted a single-center survey of residents, fellows, advanced practice providers, and attending physicians on their attitudes and beliefs about ICD deactivation in DNR/DNI patients. Residents are particularly uncomfortable discussing ICD deactivation with patients, which is an important finding because of their crucial role in providing patient care. Additionally, residents and hospitalists do not broach the topic of deactivation regularly, especially when compared to geriatricians and cardiologists. Despite HRS guidelines to the contrary, a fifth of our respondents believed that DNR/DNI orders include ICD deactivation. Overall, ICD deactivation in DNR/DNI patients is a topic that needs further attention in clinical education so that patients receive care that respects their individual wishes.

Disclosure

Nothing to report.

Nearly 70% of bariatric surgery patients received postoperative imaging, with more than one-third receiving CT imaging. This high level of screening resulted in symptom-related findings in only 23% of cases, and may be excessive, according to researchers who studied nearly 600 adults who underwent bariatric surgery.

As the volume of bariatric surgery has increased, so has the role of postoperative imaging, wrote Dana Haddad, MD, and her colleagues at Harlem Hospital Center, New York.

“However, there is a lack of well-defined postoperative imaging guidelines,” they said. “Detrimental aspects of postoperative imaging include the potential for false-positive findings leading to further and often unnecessary investigations, radiation exposure, and additional cost,” they added.

copyright picsfive/Fotolia.com

Nearly 70% of bariatric surgery patients received postoperative imaging, with more than one-third receiving CT imaging. This high level of screening resulted in symptom-related findings in only 23% of cases, and may be excessive, according to researchers who studied nearly 600 adults who underwent bariatric surgery.

As the volume of bariatric surgery has increased, so has the role of postoperative imaging, wrote Dana Haddad, MD, and her colleagues at Harlem Hospital Center, New York.

“However, there is a lack of well-defined postoperative imaging guidelines,” they said. “Detrimental aspects of postoperative imaging include the potential for false-positive findings leading to further and often unnecessary investigations, radiation exposure, and additional cost,” they added.

copyright picsfive/Fotolia.com

Nearly 70% of bariatric surgery patients received postoperative imaging, with more than one-third receiving CT imaging. This high level of screening resulted in symptom-related findings in only 23% of cases, and may be excessive, according to researchers who studied nearly 600 adults who underwent bariatric surgery.

As the volume of bariatric surgery has increased, so has the role of postoperative imaging, wrote Dana Haddad, MD, and her colleagues at Harlem Hospital Center, New York.

“However, there is a lack of well-defined postoperative imaging guidelines,” they said. “Detrimental aspects of postoperative imaging include the potential for false-positive findings leading to further and often unnecessary investigations, radiation exposure, and additional cost,” they added.

copyright picsfive/Fotolia.com

In recent years, the American Board of Internal Medicine (ABIM) Foundation’s Choosing Wisely™ campaign has advanced the dialogue on cost-consciousness by identifying potential examples of overuse in clinical practice.¹ Eliminating low-value care can decrease costs, improve quality, and potentially decrease patient harm.² In fact, there is growing consensus among health leaders and educators on the need for a physician workforce that is conscious of high-value care.^3,4 The Institute of Medicine has issued a call-to-action for graduate medical education (GME) to emphasize value-based care,⁵ and the Accreditation Council for Graduate Medical Education has outlined expectations that residents receive formal and experiential training on overuse as a part of its Clinical Learning Environment Review.⁶

However, recent reports highlight a lack of emphasis on value-based care in medical education.⁷ For example, few residency program directors believe that residents are prepared to incorporate value and cost into their medical decisions.⁸ In 2012, only 15% of medicine residencies reported having formal curricula addressing value, although many were developing one.⁸ Of the curricula reported, most were didactic in nature and did not include an assessment component.⁸

Experiential learning through simulation is one promising method to teach clinicians-in-training to practice value-based care. Simulation-based training promotes situational awareness (defined as being cognizant of one’s working environment), a concept that is crucial for recognizing both low-value and unsafe care.^9,10 Simulated training exercises are often included in GME orientation “boot-camps,” which have typically addressed safety.¹¹ The incorporation of value into existing GME boot-camp exercises could provide a promising model for the addition of value-based training to GME.

At the University of Chicago, we had successfully implemented the “Room of Horrors,” a simulation for entering interns to promote the detection of patient safety hazards.¹¹ Here, we describe a modification to this simulation to embed low-value hazards in addition to traditional patient safety hazards. The aim of this study is to assess the entering interns’ recognition of low-value care and their ability to recognize unsafe care in a simulation designed to promote situational awareness.

Setting and Participants

The simulation was conducted during GME orientation at a large, urban academic medical institution. One hundred and twenty-five entering postgraduate year one (PGY1) interns participated in the simulation, which was a required component of a multiday orientation “boot-camp” experience. All eligible interns participated in the simulation, representing 13 specialty programs and 60 medical schools. Interns entering into pathology were excluded because of infrequent patient contact. Participating interns were divided into 7 specialty groups for analysis in order to preserve the anonymity of interns in smaller residency programs (surgical subspecialties combined with general surgery, medicine-pediatrics grouped with internal medicine). The University of Chicago Institutional Review Board deemed this study exempt from review.

Program Description

A simulation of an inpatient hospital room, known as the “Room of Horrors,” was constructed in collaboration with the University of Chicago Simulation Center and adapted from a previous version of the exercise.¹¹ The simulation consisted of a mock door chart highlighting the patient had been admitted for diarrhea (Clostridium difficile positive) following a recent hospitalization for pneumonia. A clinical scenario was constructed by using a patient mannequin and an accompanying door chart that listed information on the patient’s hospital course, allergies, and medications. In addition to the 8 patient safety hazards utilized in the prior version, our team selected 4 low-value hazards to be included in the simulation.

The 8 safety hazards have been detailed in a prior study and were previously selected from Medicare’s Hospital-Acquired Conditions (HAC) Reduction Program and Agency for Healthcare Research and Quality (AHRQ) Patient Safety Indicators.^11-13 Each of the hazards was represented either physically in the simulation room and/or was indicated on the patient’s chart. For example, the latex allergy hazard was represented by latex gloves at the bedside despite an allergy indicated on the patient’s chart and wristband. A complete list of the 8 safety hazards and their representations in the simulation is shown in Table 1.

The Choosing Wisely™ lists were reviewed to identify low-value hazards for addition to the simulation.¹⁴ Our team selected 3 low-value hazards from the Society of Hospital Medicine (SHM) list,¹⁵ including (1) arbitrary blood transfusion despite the patient’s stable hemoglobin level of 8.0 g/dL and absence of cardiac symptoms,¹⁶ (2) addition of a proton pump inhibitor (PPI) for stress ulcer prophylaxis in a patient without high risk for gastrointestinal (GI) complications who was not on a PPI prior to admission, and (3) placement of a urinary catheter without medical indication. We had originally selected continuous telemetry monitoring as a fourth hazard from the SHM list, but were unable to operationalize, as it was difficult to simulate continuous telemetry on a mannequin. Because many inpatients are older than 65 years, we reviewed the American Geriatrics Society list¹⁷ and selected our fourth low-value hazard: (4) unnecessary use of physical restraints to manage behavioral symptoms in a hospitalized patient with delirium. Several of these hazards were also quality and safety priorities at our institution, including the overuse of urinary catheters, physical restraints, and blood transfusions. All 4 low-value hazards were referenced in the patient’s door chart, and 3 were also physically represented in the room via presence of a hanging unit of blood, Foley catheter, and upper-arm restraints (Table 1). See Appendix for a photograph of the simulation setup.

Each intern was allowed 10 minutes inside the simulation room. During this time, they were instructed to read the 1-page door chart, inspect the simulation room, and write down as many potential low-value and safety hazards as they could identify on a free-response form (see Appendix). Upon exiting the room, they were allotted 5 additional minutes to complete their free-response answers and provide written feedback on the simulation. The simulation was conducted in 3 simulated hospital rooms over the course of 2 days, and the correct answers were provided via e-mail after all interns had completed the exercise.

To assess prior training and safety knowledge, interns were asked to complete a 3-question preassessment on a ScanTron^TM (Tustin, CA) form. The preassessment asked interns whether they had received training on hospital safety during medical school (yes, no, or unsure), if they were satisfied with the hospital safety training they received during medical school (strongly disagree to strongly agree on a Likert scale), and if they were confident in their ability to identify potential hazards in a hospital setting (strongly disagree to strongly agree). Interns were also given the opportunity to provide feedback on the simulation experience on the ScanTron^TM (Tustin, CA) form.

One month after participating in the simulation, interns were asked to complete an online follow-up survey on MedHub^TM (Ann Arbor, MI), which included 2 Likert-scale questions (strongly disagree to strongly agree) assessing the simulation’s impact on their experience mitigating hospital hazards during the first month of internship.

Data Analysis

Interns’ free-response answers were manually coded, and descriptive statistics were used to summarize the mean percent correct for each hazard. A paired t test was used to compare intern identification of low-value vs safety hazards. T tests were used to compare hazard identification for interns entering highly procedural-intensive specialties (ie, surgical specialties, emergency medicine, anesthesia, obstetrics/gynecology) and those entering less procedural-intensive specialties (ie, internal medicine, pediatrics, psychiatry), as well as among those graduating from “Top 30” medical schools (based on US News & World Report Medical School Rankings¹⁸) and our own institution. One-way analysis of variance (ANOVA) calculations were used to test for differences in hazard identification based on interns’ prior hospital safety training, with interns who rated their satisfaction with prior training or confidence in identifying hazards as a “4” or a “5” considered “satisfied” and “confident,” respectively. Responses to the MedHub^TM (Ann Arbor, MI) survey were dichotomized with “strongly agree” and “agree” considered positive responses. Statistical significance was defined at P < .05. All data analysis was conducted using Stata 14^TM software (College Station, TX).

Intern Characteristics

One hundred twenty-five entering PGY1 interns participated in the simulation, representing 60 medical schools and 7 different specialty groups (Table 2). Thirty-five percent (44/125) were graduates from “Top 30” medical schools, and 8.8% (11/125) graduated from our own institution. Seventy-four percent (89/121) had received prior hospital safety training during medical school, and 62.9% (56/89) were satisfied with their training. A majority of interns (64.2%, 79/123) felt confident in their ability to identify potential hazards in a hospital setting, although confidence was much higher among those with prior safety training (71.9%, 64/89) compared to those without prior training or who were unsure about their training (40.6%, 13/32; P = .09, t test).

Identification of Hazards

The mean percentage of hazards correctly identified by interns during the simulation was 50.4% (standard deviation [SD] 11.8%), with a normal distribution (Figure 1). Interns identified a significantly lower percentage of low-value hazards than safety hazards in the simulation (mean 19.2% [SD 18.6%] vs 66.0% [SD 16.0%], respectively; P < .001, paired t test). Interns also identified significantly more room-based errors than chart-based errors (mean 58.6% [SD 13.4%] vs 9.6% [SD 19.8%], respectively; P < .001, paired t test). The 3 most commonly identified hazards were unavailability of hand hygiene (120/125, 96.0%), presence of latex gloves despite the patient’s allergy (111/125, 88.8%), and fall risk due to the lowered bed rail (107/125, 85.6%). More than half of interns identified the incorrect name on the patient’s wristband and IV bag (91/125, 72.8%), a lack of isolation precautions (90/125, 72.0%), administration of penicillin despite the patient’s allergy (67/125, 53.6%), and unnecessary restraints (64/125, 51.2%). Less than half of interns identified the wrong medication being administered (50/125, 40.0%), unnecessary Foley catheter (25/125, 20.0%), and absence of venous thromboembolism (VTE) prophylaxis (24/125, 19.2%). Few interns identified the unnecessary blood transfusion (7/125, 5.6%), and no one identified the unnecessary stress ulcer prophylaxis (0/125, 0.0%; Figure 2).

Predictors of Hazard Identification

Interns who self-reported as confident in their ability to identify hazards were not any more likely to correctly identify hazards than those who were not confident (50.9% overall hazard identification vs 49.6%, respectively; P = .56, t test). Interns entering into less procedural-intensive specialties identified significantly more safety hazards than those entering highly procedural-intensive specialties (mean 69.1% [SD 16.9%] vs 61.8% [SD 13.7%], respectively; P = .01, t test). However, there was no statistically significant difference in their identification of low-value hazards (mean 19.8% [SD 18.3%] for less procedural-intensive vs 18.4% [SD 19.1%] for highly procedural-intensive; P = .68, t test). There was no statistically significant difference in hazard identification among graduates of “Top 30” medical schools or graduates of our own institution. Prior hospital safety training had no significant impact on interns’ ability to identify safety or low-value hazards. Overall, interns who were satisfied with their prior training identified a mean of 51.8% of hazards present (SD 11.8%), interns who were not satisfied with their prior training identified 51.5% (SD 12.7%), interns with no prior training identified 48.7% (SD 11.7%), and interns who were unsure about their prior training identified 47.4% (SD 11.5%) [F(3,117) = .79; P = .51, ANOVA]. There was also no significant association between prior training and the identification of any one of the 12 specific hazards (chi-square tests, all P values > .1).

Intern Feedback and Follow-Up Survey

Debriefing revealed that most interns passively assumed the patient’s chart was correct and did not think they should question the patient’s current care regimen. For example, many interns commented that they did not think to consider the patient’s blood transfusion as unnecessary, even though they were aware of the recommended hemoglobin cutoffs for stable patients.

Interns also provided formal feedback on the simulation through open-ended comments on their ScanTron^TM (Tustin, CA) form. For example, one intern wrote that they would “inherently approach every patient room ‘looking’ for safety issues, probably directly because of this exercise.” Another commented that the simulation was “more difficult than I expected, but very necessary to facilitate discussion and learning.” One intern wrote that “I wish I had done this earlier in my career.”

Ninety-six percent of participating interns (120/125) completed an online follow-up survey 1 month after beginning internship. In the survey, 68.9% (82/119) of interns indicated they were more aware of how to identify potential hazards facing hospitalized patients as a result of the simulation. Furthermore, 52.1% (62/119) of interns had taken action during internship to reduce a potential hazard that was present in the simulation.

While many GME orientations include simulation and safety training, this study is the first of its kind to incorporate low-value care from Choosing Wisely™ recommendations into simulated training. It is concerning that interns identified significantly fewer low-value hazards than safety hazards in the simulation. In some cases, no interns identified the low-value hazard. For example, while almost all interns identified the hand hygiene hazard, not one could identify the unnecessary stress ulcer prophylaxis. Furthermore, interns who self-reported as confident in their ability to identify hazards did not perform any better in the simulation. Interns entering less procedural-intensive specialties identified more safety hazards overall.

The simulation was well received by interns. Many commented that the experience was engaging, challenging, and effective in cultivating situational awareness towards low-value care. Our follow-up survey demonstrated the majority of interns reported taking action during their first month of internship to reduce a hazard included in the simulation. Most interns also reported a greater awareness of how to identify hospital hazards as a result of the simulation. These findings suggest that a brief simulation-based experience has the potential to create a lasting retention of situational awareness and behavior change.

It is worth exploring why interns identified significantly fewer low-value hazards than safety hazards in the simulation. One hypothesis is that interns were less attuned to low-value hazards, which may reflect a lacking emphasis on value-based care in undergraduate medical education (UME). It is especially concerning that so few interns identified the catheter-associated urinary tract infection (CAUTI) risk, as interns are primarily responsible for recognizing and removing an unnecessary catheter. Although the risks of low-value care should be apparent to most trainees, the process of recognizing and deliberately stopping or avoiding low-value care can be challenging for young clinicians.¹⁹ To promote value-based thinking among entering residents, UME programs should teach students to question the utility of the interventions their patients are receiving. One promising framework for doing so is the Subjective, Objective, Assessment, Plan- (SOAP)-V, in which a V for “Value” is added to the traditional SOAP note.²⁰ SOAP-V notes serve as a cognitive forcing function that requires students to pause and assess the value and cost-consciousness of their patients’ care.²⁰

The results from the “Room of Horrors” simulation can also guide health leaders and educators in identifying institutional areas of focus towards providing high-value and safe care. For example, at the University of Chicago we launched an initiative to improve the inappropriate use of urinary catheters after learning that few of our incoming interns recognized this during the simulation. Institutions could use this model to raise awareness of initiatives and redirect resources from areas that trainees perform well in (eg, hand hygiene) to areas that need improvement (eg, recognition of low-value care). Given the simulation’s low cost and minimal material requirements, it could be easily integrated into existing training programs with the support of an institution’s simulation center.

This study’s limitations include its conduction at single-institution, although the participants represented graduates of 60 different institutions. Furthermore, while the 12 hazards included in the simulation represent patient safety and value initiatives from a wide array of medical societies, they were not intended to be comprehensive and were not tailored to specific specialties. The simulation included only 4 low-value hazards, and future iterations of this exercise should aim to include an equal number of safety and low-value hazards. Furthermore, the evaluation of interns’ prior hospital safety training relied on self-reporting, and the specific context and content of each interns’ training was not examined. Finally, at this point we are unable to provide objective longitudinal data assessing the simulation’s impact on clinical practice and patient outcomes. Subsequent work will assess the sustained impact of the simulation by correlating with institutional data on measurable occurrences of low-value care.

In conclusion, interns identified significantly fewer low-value hazards than safety hazards in an inpatient simulation designed to promote situational awareness. Our results suggest that interns are on the lookout for errors of omission (eg, absence of hand hygiene, absence of isolation precautions) but are often blinded to errors of commission, such that when patients are started on therapies there is an assumption that the therapies are correct and necessary (eg, blood transfusions, stress ulcer prophylaxis). These findings suggest poor awareness of low-value care among incoming interns and highlight the need for additional training in both UME and GME to place a greater emphasis on preventing low-value care.

Disclosure

Dr. Arora is a member of the American Board of Medicine Board of Directors and has received grant funding from ABIM Foundation via Costs of Care for the Teaching Value Choosing Wisely™ Challenge. Dr. Farnan, Dr. Arora, and Ms. Hirsch receive grant funds from Accreditation Council of Graduate Medical Education as part of the Pursuing Excellence Initiative. Dr. Arora and Dr. Farnan also receive grant funds from the American Medical Association Accelerating Change in Medical Education initiative. Kathleen Wiest and Lukas Matern were funded through matching funds of the Pritzker Summer Research Program for NIA T35AG029795.

In recent years, the American Board of Internal Medicine (ABIM) Foundation’s Choosing Wisely™ campaign has advanced the dialogue on cost-consciousness by identifying potential examples of overuse in clinical practice.¹ Eliminating low-value care can decrease costs, improve quality, and potentially decrease patient harm.² In fact, there is growing consensus among health leaders and educators on the need for a physician workforce that is conscious of high-value care.^3,4 The Institute of Medicine has issued a call-to-action for graduate medical education (GME) to emphasize value-based care,⁵ and the Accreditation Council for Graduate Medical Education has outlined expectations that residents receive formal and experiential training on overuse as a part of its Clinical Learning Environment Review.⁶

However, recent reports highlight a lack of emphasis on value-based care in medical education.⁷ For example, few residency program directors believe that residents are prepared to incorporate value and cost into their medical decisions.⁸ In 2012, only 15% of medicine residencies reported having formal curricula addressing value, although many were developing one.⁸ Of the curricula reported, most were didactic in nature and did not include an assessment component.⁸

Experiential learning through simulation is one promising method to teach clinicians-in-training to practice value-based care. Simulation-based training promotes situational awareness (defined as being cognizant of one’s working environment), a concept that is crucial for recognizing both low-value and unsafe care.^9,10 Simulated training exercises are often included in GME orientation “boot-camps,” which have typically addressed safety.¹¹ The incorporation of value into existing GME boot-camp exercises could provide a promising model for the addition of value-based training to GME.

At the University of Chicago, we had successfully implemented the “Room of Horrors,” a simulation for entering interns to promote the detection of patient safety hazards.¹¹ Here, we describe a modification to this simulation to embed low-value hazards in addition to traditional patient safety hazards. The aim of this study is to assess the entering interns’ recognition of low-value care and their ability to recognize unsafe care in a simulation designed to promote situational awareness.

Setting and Participants

The simulation was conducted during GME orientation at a large, urban academic medical institution. One hundred and twenty-five entering postgraduate year one (PGY1) interns participated in the simulation, which was a required component of a multiday orientation “boot-camp” experience. All eligible interns participated in the simulation, representing 13 specialty programs and 60 medical schools. Interns entering into pathology were excluded because of infrequent patient contact. Participating interns were divided into 7 specialty groups for analysis in order to preserve the anonymity of interns in smaller residency programs (surgical subspecialties combined with general surgery, medicine-pediatrics grouped with internal medicine). The University of Chicago Institutional Review Board deemed this study exempt from review.

Program Description

A simulation of an inpatient hospital room, known as the “Room of Horrors,” was constructed in collaboration with the University of Chicago Simulation Center and adapted from a previous version of the exercise.¹¹ The simulation consisted of a mock door chart highlighting the patient had been admitted for diarrhea (Clostridium difficile positive) following a recent hospitalization for pneumonia. A clinical scenario was constructed by using a patient mannequin and an accompanying door chart that listed information on the patient’s hospital course, allergies, and medications. In addition to the 8 patient safety hazards utilized in the prior version, our team selected 4 low-value hazards to be included in the simulation.

The 8 safety hazards have been detailed in a prior study and were previously selected from Medicare’s Hospital-Acquired Conditions (HAC) Reduction Program and Agency for Healthcare Research and Quality (AHRQ) Patient Safety Indicators.^11-13 Each of the hazards was represented either physically in the simulation room and/or was indicated on the patient’s chart. For example, the latex allergy hazard was represented by latex gloves at the bedside despite an allergy indicated on the patient’s chart and wristband. A complete list of the 8 safety hazards and their representations in the simulation is shown in Table 1.

The Choosing Wisely™ lists were reviewed to identify low-value hazards for addition to the simulation.¹⁴ Our team selected 3 low-value hazards from the Society of Hospital Medicine (SHM) list,¹⁵ including (1) arbitrary blood transfusion despite the patient’s stable hemoglobin level of 8.0 g/dL and absence of cardiac symptoms,¹⁶ (2) addition of a proton pump inhibitor (PPI) for stress ulcer prophylaxis in a patient without high risk for gastrointestinal (GI) complications who was not on a PPI prior to admission, and (3) placement of a urinary catheter without medical indication. We had originally selected continuous telemetry monitoring as a fourth hazard from the SHM list, but were unable to operationalize, as it was difficult to simulate continuous telemetry on a mannequin. Because many inpatients are older than 65 years, we reviewed the American Geriatrics Society list¹⁷ and selected our fourth low-value hazard: (4) unnecessary use of physical restraints to manage behavioral symptoms in a hospitalized patient with delirium. Several of these hazards were also quality and safety priorities at our institution, including the overuse of urinary catheters, physical restraints, and blood transfusions. All 4 low-value hazards were referenced in the patient’s door chart, and 3 were also physically represented in the room via presence of a hanging unit of blood, Foley catheter, and upper-arm restraints (Table 1). See Appendix for a photograph of the simulation setup.

Each intern was allowed 10 minutes inside the simulation room. During this time, they were instructed to read the 1-page door chart, inspect the simulation room, and write down as many potential low-value and safety hazards as they could identify on a free-response form (see Appendix). Upon exiting the room, they were allotted 5 additional minutes to complete their free-response answers and provide written feedback on the simulation. The simulation was conducted in 3 simulated hospital rooms over the course of 2 days, and the correct answers were provided via e-mail after all interns had completed the exercise.

To assess prior training and safety knowledge, interns were asked to complete a 3-question preassessment on a ScanTron^TM (Tustin, CA) form. The preassessment asked interns whether they had received training on hospital safety during medical school (yes, no, or unsure), if they were satisfied with the hospital safety training they received during medical school (strongly disagree to strongly agree on a Likert scale), and if they were confident in their ability to identify potential hazards in a hospital setting (strongly disagree to strongly agree). Interns were also given the opportunity to provide feedback on the simulation experience on the ScanTron^TM (Tustin, CA) form.

One month after participating in the simulation, interns were asked to complete an online follow-up survey on MedHub^TM (Ann Arbor, MI), which included 2 Likert-scale questions (strongly disagree to strongly agree) assessing the simulation’s impact on their experience mitigating hospital hazards during the first month of internship.

Data Analysis

Interns’ free-response answers were manually coded, and descriptive statistics were used to summarize the mean percent correct for each hazard. A paired t test was used to compare intern identification of low-value vs safety hazards. T tests were used to compare hazard identification for interns entering highly procedural-intensive specialties (ie, surgical specialties, emergency medicine, anesthesia, obstetrics/gynecology) and those entering less procedural-intensive specialties (ie, internal medicine, pediatrics, psychiatry), as well as among those graduating from “Top 30” medical schools (based on US News & World Report Medical School Rankings¹⁸) and our own institution. One-way analysis of variance (ANOVA) calculations were used to test for differences in hazard identification based on interns’ prior hospital safety training, with interns who rated their satisfaction with prior training or confidence in identifying hazards as a “4” or a “5” considered “satisfied” and “confident,” respectively. Responses to the MedHub^TM (Ann Arbor, MI) survey were dichotomized with “strongly agree” and “agree” considered positive responses. Statistical significance was defined at P < .05. All data analysis was conducted using Stata 14^TM software (College Station, TX).

Intern Characteristics

One hundred twenty-five entering PGY1 interns participated in the simulation, representing 60 medical schools and 7 different specialty groups (Table 2). Thirty-five percent (44/125) were graduates from “Top 30” medical schools, and 8.8% (11/125) graduated from our own institution. Seventy-four percent (89/121) had received prior hospital safety training during medical school, and 62.9% (56/89) were satisfied with their training. A majority of interns (64.2%, 79/123) felt confident in their ability to identify potential hazards in a hospital setting, although confidence was much higher among those with prior safety training (71.9%, 64/89) compared to those without prior training or who were unsure about their training (40.6%, 13/32; P = .09, t test).

Identification of Hazards

The mean percentage of hazards correctly identified by interns during the simulation was 50.4% (standard deviation [SD] 11.8%), with a normal distribution (Figure 1). Interns identified a significantly lower percentage of low-value hazards than safety hazards in the simulation (mean 19.2% [SD 18.6%] vs 66.0% [SD 16.0%], respectively; P < .001, paired t test). Interns also identified significantly more room-based errors than chart-based errors (mean 58.6% [SD 13.4%] vs 9.6% [SD 19.8%], respectively; P < .001, paired t test). The 3 most commonly identified hazards were unavailability of hand hygiene (120/125, 96.0%), presence of latex gloves despite the patient’s allergy (111/125, 88.8%), and fall risk due to the lowered bed rail (107/125, 85.6%). More than half of interns identified the incorrect name on the patient’s wristband and IV bag (91/125, 72.8%), a lack of isolation precautions (90/125, 72.0%), administration of penicillin despite the patient’s allergy (67/125, 53.6%), and unnecessary restraints (64/125, 51.2%). Less than half of interns identified the wrong medication being administered (50/125, 40.0%), unnecessary Foley catheter (25/125, 20.0%), and absence of venous thromboembolism (VTE) prophylaxis (24/125, 19.2%). Few interns identified the unnecessary blood transfusion (7/125, 5.6%), and no one identified the unnecessary stress ulcer prophylaxis (0/125, 0.0%; Figure 2).

Predictors of Hazard Identification

Interns who self-reported as confident in their ability to identify hazards were not any more likely to correctly identify hazards than those who were not confident (50.9% overall hazard identification vs 49.6%, respectively; P = .56, t test). Interns entering into less procedural-intensive specialties identified significantly more safety hazards than those entering highly procedural-intensive specialties (mean 69.1% [SD 16.9%] vs 61.8% [SD 13.7%], respectively; P = .01, t test). However, there was no statistically significant difference in their identification of low-value hazards (mean 19.8% [SD 18.3%] for less procedural-intensive vs 18.4% [SD 19.1%] for highly procedural-intensive; P = .68, t test). There was no statistically significant difference in hazard identification among graduates of “Top 30” medical schools or graduates of our own institution. Prior hospital safety training had no significant impact on interns’ ability to identify safety or low-value hazards. Overall, interns who were satisfied with their prior training identified a mean of 51.8% of hazards present (SD 11.8%), interns who were not satisfied with their prior training identified 51.5% (SD 12.7%), interns with no prior training identified 48.7% (SD 11.7%), and interns who were unsure about their prior training identified 47.4% (SD 11.5%) [F(3,117) = .79; P = .51, ANOVA]. There was also no significant association between prior training and the identification of any one of the 12 specific hazards (chi-square tests, all P values > .1).

Intern Feedback and Follow-Up Survey

Debriefing revealed that most interns passively assumed the patient’s chart was correct and did not think they should question the patient’s current care regimen. For example, many interns commented that they did not think to consider the patient’s blood transfusion as unnecessary, even though they were aware of the recommended hemoglobin cutoffs for stable patients.

Interns also provided formal feedback on the simulation through open-ended comments on their ScanTron^TM (Tustin, CA) form. For example, one intern wrote that they would “inherently approach every patient room ‘looking’ for safety issues, probably directly because of this exercise.” Another commented that the simulation was “more difficult than I expected, but very necessary to facilitate discussion and learning.” One intern wrote that “I wish I had done this earlier in my career.”

Ninety-six percent of participating interns (120/125) completed an online follow-up survey 1 month after beginning internship. In the survey, 68.9% (82/119) of interns indicated they were more aware of how to identify potential hazards facing hospitalized patients as a result of the simulation. Furthermore, 52.1% (62/119) of interns had taken action during internship to reduce a potential hazard that was present in the simulation.

While many GME orientations include simulation and safety training, this study is the first of its kind to incorporate low-value care from Choosing Wisely™ recommendations into simulated training. It is concerning that interns identified significantly fewer low-value hazards than safety hazards in the simulation. In some cases, no interns identified the low-value hazard. For example, while almost all interns identified the hand hygiene hazard, not one could identify the unnecessary stress ulcer prophylaxis. Furthermore, interns who self-reported as confident in their ability to identify hazards did not perform any better in the simulation. Interns entering less procedural-intensive specialties identified more safety hazards overall.

The simulation was well received by interns. Many commented that the experience was engaging, challenging, and effective in cultivating situational awareness towards low-value care. Our follow-up survey demonstrated the majority of interns reported taking action during their first month of internship to reduce a hazard included in the simulation. Most interns also reported a greater awareness of how to identify hospital hazards as a result of the simulation. These findings suggest that a brief simulation-based experience has the potential to create a lasting retention of situational awareness and behavior change.

It is worth exploring why interns identified significantly fewer low-value hazards than safety hazards in the simulation. One hypothesis is that interns were less attuned to low-value hazards, which may reflect a lacking emphasis on value-based care in undergraduate medical education (UME). It is especially concerning that so few interns identified the catheter-associated urinary tract infection (CAUTI) risk, as interns are primarily responsible for recognizing and removing an unnecessary catheter. Although the risks of low-value care should be apparent to most trainees, the process of recognizing and deliberately stopping or avoiding low-value care can be challenging for young clinicians.¹⁹ To promote value-based thinking among entering residents, UME programs should teach students to question the utility of the interventions their patients are receiving. One promising framework for doing so is the Subjective, Objective, Assessment, Plan- (SOAP)-V, in which a V for “Value” is added to the traditional SOAP note.²⁰ SOAP-V notes serve as a cognitive forcing function that requires students to pause and assess the value and cost-consciousness of their patients’ care.²⁰

The results from the “Room of Horrors” simulation can also guide health leaders and educators in identifying institutional areas of focus towards providing high-value and safe care. For example, at the University of Chicago we launched an initiative to improve the inappropriate use of urinary catheters after learning that few of our incoming interns recognized this during the simulation. Institutions could use this model to raise awareness of initiatives and redirect resources from areas that trainees perform well in (eg, hand hygiene) to areas that need improvement (eg, recognition of low-value care). Given the simulation’s low cost and minimal material requirements, it could be easily integrated into existing training programs with the support of an institution’s simulation center.

This study’s limitations include its conduction at single-institution, although the participants represented graduates of 60 different institutions. Furthermore, while the 12 hazards included in the simulation represent patient safety and value initiatives from a wide array of medical societies, they were not intended to be comprehensive and were not tailored to specific specialties. The simulation included only 4 low-value hazards, and future iterations of this exercise should aim to include an equal number of safety and low-value hazards. Furthermore, the evaluation of interns’ prior hospital safety training relied on self-reporting, and the specific context and content of each interns’ training was not examined. Finally, at this point we are unable to provide objective longitudinal data assessing the simulation’s impact on clinical practice and patient outcomes. Subsequent work will assess the sustained impact of the simulation by correlating with institutional data on measurable occurrences of low-value care.

In conclusion, interns identified significantly fewer low-value hazards than safety hazards in an inpatient simulation designed to promote situational awareness. Our results suggest that interns are on the lookout for errors of omission (eg, absence of hand hygiene, absence of isolation precautions) but are often blinded to errors of commission, such that when patients are started on therapies there is an assumption that the therapies are correct and necessary (eg, blood transfusions, stress ulcer prophylaxis). These findings suggest poor awareness of low-value care among incoming interns and highlight the need for additional training in both UME and GME to place a greater emphasis on preventing low-value care.

Disclosure

Dr. Arora is a member of the American Board of Medicine Board of Directors and has received grant funding from ABIM Foundation via Costs of Care for the Teaching Value Choosing Wisely™ Challenge. Dr. Farnan, Dr. Arora, and Ms. Hirsch receive grant funds from Accreditation Council of Graduate Medical Education as part of the Pursuing Excellence Initiative. Dr. Arora and Dr. Farnan also receive grant funds from the American Medical Association Accelerating Change in Medical Education initiative. Kathleen Wiest and Lukas Matern were funded through matching funds of the Pritzker Summer Research Program for NIA T35AG029795.

In recent years, the American Board of Internal Medicine (ABIM) Foundation’s Choosing Wisely™ campaign has advanced the dialogue on cost-consciousness by identifying potential examples of overuse in clinical practice.¹ Eliminating low-value care can decrease costs, improve quality, and potentially decrease patient harm.² In fact, there is growing consensus among health leaders and educators on the need for a physician workforce that is conscious of high-value care.^3,4 The Institute of Medicine has issued a call-to-action for graduate medical education (GME) to emphasize value-based care,⁵ and the Accreditation Council for Graduate Medical Education has outlined expectations that residents receive formal and experiential training on overuse as a part of its Clinical Learning Environment Review.⁶

However, recent reports highlight a lack of emphasis on value-based care in medical education.⁷ For example, few residency program directors believe that residents are prepared to incorporate value and cost into their medical decisions.⁸ In 2012, only 15% of medicine residencies reported having formal curricula addressing value, although many were developing one.⁸ Of the curricula reported, most were didactic in nature and did not include an assessment component.⁸

Experiential learning through simulation is one promising method to teach clinicians-in-training to practice value-based care. Simulation-based training promotes situational awareness (defined as being cognizant of one’s working environment), a concept that is crucial for recognizing both low-value and unsafe care.^9,10 Simulated training exercises are often included in GME orientation “boot-camps,” which have typically addressed safety.¹¹ The incorporation of value into existing GME boot-camp exercises could provide a promising model for the addition of value-based training to GME.

At the University of Chicago, we had successfully implemented the “Room of Horrors,” a simulation for entering interns to promote the detection of patient safety hazards.¹¹ Here, we describe a modification to this simulation to embed low-value hazards in addition to traditional patient safety hazards. The aim of this study is to assess the entering interns’ recognition of low-value care and their ability to recognize unsafe care in a simulation designed to promote situational awareness.

Setting and Participants

The simulation was conducted during GME orientation at a large, urban academic medical institution. One hundred and twenty-five entering postgraduate year one (PGY1) interns participated in the simulation, which was a required component of a multiday orientation “boot-camp” experience. All eligible interns participated in the simulation, representing 13 specialty programs and 60 medical schools. Interns entering into pathology were excluded because of infrequent patient contact. Participating interns were divided into 7 specialty groups for analysis in order to preserve the anonymity of interns in smaller residency programs (surgical subspecialties combined with general surgery, medicine-pediatrics grouped with internal medicine). The University of Chicago Institutional Review Board deemed this study exempt from review.

Program Description

A simulation of an inpatient hospital room, known as the “Room of Horrors,” was constructed in collaboration with the University of Chicago Simulation Center and adapted from a previous version of the exercise.¹¹ The simulation consisted of a mock door chart highlighting the patient had been admitted for diarrhea (Clostridium difficile positive) following a recent hospitalization for pneumonia. A clinical scenario was constructed by using a patient mannequin and an accompanying door chart that listed information on the patient’s hospital course, allergies, and medications. In addition to the 8 patient safety hazards utilized in the prior version, our team selected 4 low-value hazards to be included in the simulation.

The 8 safety hazards have been detailed in a prior study and were previously selected from Medicare’s Hospital-Acquired Conditions (HAC) Reduction Program and Agency for Healthcare Research and Quality (AHRQ) Patient Safety Indicators.^11-13 Each of the hazards was represented either physically in the simulation room and/or was indicated on the patient’s chart. For example, the latex allergy hazard was represented by latex gloves at the bedside despite an allergy indicated on the patient’s chart and wristband. A complete list of the 8 safety hazards and their representations in the simulation is shown in Table 1.

The Choosing Wisely™ lists were reviewed to identify low-value hazards for addition to the simulation.¹⁴ Our team selected 3 low-value hazards from the Society of Hospital Medicine (SHM) list,¹⁵ including (1) arbitrary blood transfusion despite the patient’s stable hemoglobin level of 8.0 g/dL and absence of cardiac symptoms,¹⁶ (2) addition of a proton pump inhibitor (PPI) for stress ulcer prophylaxis in a patient without high risk for gastrointestinal (GI) complications who was not on a PPI prior to admission, and (3) placement of a urinary catheter without medical indication. We had originally selected continuous telemetry monitoring as a fourth hazard from the SHM list, but were unable to operationalize, as it was difficult to simulate continuous telemetry on a mannequin. Because many inpatients are older than 65 years, we reviewed the American Geriatrics Society list¹⁷ and selected our fourth low-value hazard: (4) unnecessary use of physical restraints to manage behavioral symptoms in a hospitalized patient with delirium. Several of these hazards were also quality and safety priorities at our institution, including the overuse of urinary catheters, physical restraints, and blood transfusions. All 4 low-value hazards were referenced in the patient’s door chart, and 3 were also physically represented in the room via presence of a hanging unit of blood, Foley catheter, and upper-arm restraints (Table 1). See Appendix for a photograph of the simulation setup.

Each intern was allowed 10 minutes inside the simulation room. During this time, they were instructed to read the 1-page door chart, inspect the simulation room, and write down as many potential low-value and safety hazards as they could identify on a free-response form (see Appendix). Upon exiting the room, they were allotted 5 additional minutes to complete their free-response answers and provide written feedback on the simulation. The simulation was conducted in 3 simulated hospital rooms over the course of 2 days, and the correct answers were provided via e-mail after all interns had completed the exercise.

To assess prior training and safety knowledge, interns were asked to complete a 3-question preassessment on a ScanTron^TM (Tustin, CA) form. The preassessment asked interns whether they had received training on hospital safety during medical school (yes, no, or unsure), if they were satisfied with the hospital safety training they received during medical school (strongly disagree to strongly agree on a Likert scale), and if they were confident in their ability to identify potential hazards in a hospital setting (strongly disagree to strongly agree). Interns were also given the opportunity to provide feedback on the simulation experience on the ScanTron^TM (Tustin, CA) form.

One month after participating in the simulation, interns were asked to complete an online follow-up survey on MedHub^TM (Ann Arbor, MI), which included 2 Likert-scale questions (strongly disagree to strongly agree) assessing the simulation’s impact on their experience mitigating hospital hazards during the first month of internship.

Data Analysis

Interns’ free-response answers were manually coded, and descriptive statistics were used to summarize the mean percent correct for each hazard. A paired t test was used to compare intern identification of low-value vs safety hazards. T tests were used to compare hazard identification for interns entering highly procedural-intensive specialties (ie, surgical specialties, emergency medicine, anesthesia, obstetrics/gynecology) and those entering less procedural-intensive specialties (ie, internal medicine, pediatrics, psychiatry), as well as among those graduating from “Top 30” medical schools (based on US News & World Report Medical School Rankings¹⁸) and our own institution. One-way analysis of variance (ANOVA) calculations were used to test for differences in hazard identification based on interns’ prior hospital safety training, with interns who rated their satisfaction with prior training or confidence in identifying hazards as a “4” or a “5” considered “satisfied” and “confident,” respectively. Responses to the MedHub^TM (Ann Arbor, MI) survey were dichotomized with “strongly agree” and “agree” considered positive responses. Statistical significance was defined at P < .05. All data analysis was conducted using Stata 14^TM software (College Station, TX).

Intern Characteristics

One hundred twenty-five entering PGY1 interns participated in the simulation, representing 60 medical schools and 7 different specialty groups (Table 2). Thirty-five percent (44/125) were graduates from “Top 30” medical schools, and 8.8% (11/125) graduated from our own institution. Seventy-four percent (89/121) had received prior hospital safety training during medical school, and 62.9% (56/89) were satisfied with their training. A majority of interns (64.2%, 79/123) felt confident in their ability to identify potential hazards in a hospital setting, although confidence was much higher among those with prior safety training (71.9%, 64/89) compared to those without prior training or who were unsure about their training (40.6%, 13/32; P = .09, t test).

Identification of Hazards

The mean percentage of hazards correctly identified by interns during the simulation was 50.4% (standard deviation [SD] 11.8%), with a normal distribution (Figure 1). Interns identified a significantly lower percentage of low-value hazards than safety hazards in the simulation (mean 19.2% [SD 18.6%] vs 66.0% [SD 16.0%], respectively; P < .001, paired t test). Interns also identified significantly more room-based errors than chart-based errors (mean 58.6% [SD 13.4%] vs 9.6% [SD 19.8%], respectively; P < .001, paired t test). The 3 most commonly identified hazards were unavailability of hand hygiene (120/125, 96.0%), presence of latex gloves despite the patient’s allergy (111/125, 88.8%), and fall risk due to the lowered bed rail (107/125, 85.6%). More than half of interns identified the incorrect name on the patient’s wristband and IV bag (91/125, 72.8%), a lack of isolation precautions (90/125, 72.0%), administration of penicillin despite the patient’s allergy (67/125, 53.6%), and unnecessary restraints (64/125, 51.2%). Less than half of interns identified the wrong medication being administered (50/125, 40.0%), unnecessary Foley catheter (25/125, 20.0%), and absence of venous thromboembolism (VTE) prophylaxis (24/125, 19.2%). Few interns identified the unnecessary blood transfusion (7/125, 5.6%), and no one identified the unnecessary stress ulcer prophylaxis (0/125, 0.0%; Figure 2).

Predictors of Hazard Identification

Interns who self-reported as confident in their ability to identify hazards were not any more likely to correctly identify hazards than those who were not confident (50.9% overall hazard identification vs 49.6%, respectively; P = .56, t test). Interns entering into less procedural-intensive specialties identified significantly more safety hazards than those entering highly procedural-intensive specialties (mean 69.1% [SD 16.9%] vs 61.8% [SD 13.7%], respectively; P = .01, t test). However, there was no statistically significant difference in their identification of low-value hazards (mean 19.8% [SD 18.3%] for less procedural-intensive vs 18.4% [SD 19.1%] for highly procedural-intensive; P = .68, t test). There was no statistically significant difference in hazard identification among graduates of “Top 30” medical schools or graduates of our own institution. Prior hospital safety training had no significant impact on interns’ ability to identify safety or low-value hazards. Overall, interns who were satisfied with their prior training identified a mean of 51.8% of hazards present (SD 11.8%), interns who were not satisfied with their prior training identified 51.5% (SD 12.7%), interns with no prior training identified 48.7% (SD 11.7%), and interns who were unsure about their prior training identified 47.4% (SD 11.5%) [F(3,117) = .79; P = .51, ANOVA]. There was also no significant association between prior training and the identification of any one of the 12 specific hazards (chi-square tests, all P values > .1).

Intern Feedback and Follow-Up Survey

Debriefing revealed that most interns passively assumed the patient’s chart was correct and did not think they should question the patient’s current care regimen. For example, many interns commented that they did not think to consider the patient’s blood transfusion as unnecessary, even though they were aware of the recommended hemoglobin cutoffs for stable patients.

Interns also provided formal feedback on the simulation through open-ended comments on their ScanTron^TM (Tustin, CA) form. For example, one intern wrote that they would “inherently approach every patient room ‘looking’ for safety issues, probably directly because of this exercise.” Another commented that the simulation was “more difficult than I expected, but very necessary to facilitate discussion and learning.” One intern wrote that “I wish I had done this earlier in my career.”

Ninety-six percent of participating interns (120/125) completed an online follow-up survey 1 month after beginning internship. In the survey, 68.9% (82/119) of interns indicated they were more aware of how to identify potential hazards facing hospitalized patients as a result of the simulation. Furthermore, 52.1% (62/119) of interns had taken action during internship to reduce a potential hazard that was present in the simulation.

While many GME orientations include simulation and safety training, this study is the first of its kind to incorporate low-value care from Choosing Wisely™ recommendations into simulated training. It is concerning that interns identified significantly fewer low-value hazards than safety hazards in the simulation. In some cases, no interns identified the low-value hazard. For example, while almost all interns identified the hand hygiene hazard, not one could identify the unnecessary stress ulcer prophylaxis. Furthermore, interns who self-reported as confident in their ability to identify hazards did not perform any better in the simulation. Interns entering less procedural-intensive specialties identified more safety hazards overall.

The simulation was well received by interns. Many commented that the experience was engaging, challenging, and effective in cultivating situational awareness towards low-value care. Our follow-up survey demonstrated the majority of interns reported taking action during their first month of internship to reduce a hazard included in the simulation. Most interns also reported a greater awareness of how to identify hospital hazards as a result of the simulation. These findings suggest that a brief simulation-based experience has the potential to create a lasting retention of situational awareness and behavior change.

It is worth exploring why interns identified significantly fewer low-value hazards than safety hazards in the simulation. One hypothesis is that interns were less attuned to low-value hazards, which may reflect a lacking emphasis on value-based care in undergraduate medical education (UME). It is especially concerning that so few interns identified the catheter-associated urinary tract infection (CAUTI) risk, as interns are primarily responsible for recognizing and removing an unnecessary catheter. Although the risks of low-value care should be apparent to most trainees, the process of recognizing and deliberately stopping or avoiding low-value care can be challenging for young clinicians.¹⁹ To promote value-based thinking among entering residents, UME programs should teach students to question the utility of the interventions their patients are receiving. One promising framework for doing so is the Subjective, Objective, Assessment, Plan- (SOAP)-V, in which a V for “Value” is added to the traditional SOAP note.²⁰ SOAP-V notes serve as a cognitive forcing function that requires students to pause and assess the value and cost-consciousness of their patients’ care.²⁰

The results from the “Room of Horrors” simulation can also guide health leaders and educators in identifying institutional areas of focus towards providing high-value and safe care. For example, at the University of Chicago we launched an initiative to improve the inappropriate use of urinary catheters after learning that few of our incoming interns recognized this during the simulation. Institutions could use this model to raise awareness of initiatives and redirect resources from areas that trainees perform well in (eg, hand hygiene) to areas that need improvement (eg, recognition of low-value care). Given the simulation’s low cost and minimal material requirements, it could be easily integrated into existing training programs with the support of an institution’s simulation center.

This study’s limitations include its conduction at single-institution, although the participants represented graduates of 60 different institutions. Furthermore, while the 12 hazards included in the simulation represent patient safety and value initiatives from a wide array of medical societies, they were not intended to be comprehensive and were not tailored to specific specialties. The simulation included only 4 low-value hazards, and future iterations of this exercise should aim to include an equal number of safety and low-value hazards. Furthermore, the evaluation of interns’ prior hospital safety training relied on self-reporting, and the specific context and content of each interns’ training was not examined. Finally, at this point we are unable to provide objective longitudinal data assessing the simulation’s impact on clinical practice and patient outcomes. Subsequent work will assess the sustained impact of the simulation by correlating with institutional data on measurable occurrences of low-value care.

In conclusion, interns identified significantly fewer low-value hazards than safety hazards in an inpatient simulation designed to promote situational awareness. Our results suggest that interns are on the lookout for errors of omission (eg, absence of hand hygiene, absence of isolation precautions) but are often blinded to errors of commission, such that when patients are started on therapies there is an assumption that the therapies are correct and necessary (eg, blood transfusions, stress ulcer prophylaxis). These findings suggest poor awareness of low-value care among incoming interns and highlight the need for additional training in both UME and GME to place a greater emphasis on preventing low-value care.

Disclosure

Dr. Arora is a member of the American Board of Medicine Board of Directors and has received grant funding from ABIM Foundation via Costs of Care for the Teaching Value Choosing Wisely™ Challenge. Dr. Farnan, Dr. Arora, and Ms. Hirsch receive grant funds from Accreditation Council of Graduate Medical Education as part of the Pursuing Excellence Initiative. Dr. Arora and Dr. Farnan also receive grant funds from the American Medical Association Accelerating Change in Medical Education initiative. Kathleen Wiest and Lukas Matern were funded through matching funds of the Pritzker Summer Research Program for NIA T35AG029795.

Inherited mutations in a single gene may contribute to a severe form of atopic dermatitis (AD), a study of eight patients showed.

Investigators from the National Institute of Allergy and Infectious Diseases (NIAID) and elsewhere identified eight individuals with severe AD from four unrelated families. All of the patients had a mutation in the CARD11 gene, which is part of the nuclear factor–kappa B (NF-kB) pathway.

Courtesy National Institute of Allergy and Infectious Diseases

Inherited mutations in a single gene may contribute to a severe form of atopic dermatitis (AD), a study of eight patients showed.

Investigators from the National Institute of Allergy and Infectious Diseases (NIAID) and elsewhere identified eight individuals with severe AD from four unrelated families. All of the patients had a mutation in the CARD11 gene, which is part of the nuclear factor–kappa B (NF-kB) pathway.

Courtesy National Institute of Allergy and Infectious Diseases

Inherited mutations in a single gene may contribute to a severe form of atopic dermatitis (AD), a study of eight patients showed.

Investigators from the National Institute of Allergy and Infectious Diseases (NIAID) and elsewhere identified eight individuals with severe AD from four unrelated families. All of the patients had a mutation in the CARD11 gene, which is part of the nuclear factor–kappa B (NF-kB) pathway.

Courtesy National Institute of Allergy and Infectious Diseases