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Review Paper

Free Access

Skin Infections due to Bacteria in Solid Organ Transplant Recipients: A Review

Ilyas M. · Maganty N. · Ginsberg Z. · Sharma A.

Author affiliations

Department of Dermatology, Mayo Clinic Arizona, Scottsdale, AZ, USA

Corresponding Author

Nishita Maganty, MPH

Department of Dermatology, Mayo Clinic Arizona

13400 E. Shea Blvd.

Scottsdale, AZ 85259 (USA)

E-Mail nmaganty@email.arizona.edu

Related Articles for ""

Dermatology 2017;233:358–365

Abstract

Though there is an abundance of information on cutaneous malignancies in transplant recipients, cutaneous infections in solid organ transplant recipients (SOTRs) are underrepresented in the dermatological literature. Our paper provides a comprehensive review of bacterial cutaneous infections within the solid organ transplant population. Cutaneous bacterial infections may lead to significant morbidity and even mortality in this immunosuppressed population. Thus, it is to the benefit of both dermatologists and other transplant care providers to better understand and recognize the features of cutaneous bacterial infections in SOTRs. This paper can aid providers in promptly identifying, diagnosing, and treating bacterial skin infections. This review discusses the diagnosis and treatment of the following bacterial species: Staphylococcus, Streptococcus, Pseudomonas aeruginosa, Escherichia coli, Nocardia, Mycobacteria, and Bartonella henselae.

© 2018 S. Karger AG, Basel


Introduction

Due to their being on immunosuppressive medications, solid organ transplant recipients (SOTRs) are afflicted with a wide array of cutaneous diseases. Despite the abundant literature on cutaneous malignancies in SOTRs, information on the diagnosis and management of bacterial skin infections is underrepresented. Bacterial infections can present with a variety of symptoms and may cause significant morbidity in SOTRs (Table 1). Therefore, it is beneficial for transplant care providers to recognize the spectrum and management of bacterial cutaneous infections.

Table 1

Sources of bacterial skin infections and their cutaneous manifestations in SOTRs

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Materials and Methods

For further details, see the online supplementary material (see www.karger.com/doi/10.1159/000484405) (Fig. 1).

Fig. 1

Flowchart of the literature search.

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Infection Types and Treatment

Cutaneous Staphylococcal Infection

Prior to transplantation, Staphylococcus aureus colonizes the anterior nares of 67% of transplant candidates [1,2] compared to 50% of immunocompetent individuals [3]. In SOTRs, a majority of nasal carriers of S. aureus have methicillin-resistant S. aureus (MRSA), which if not properly eradicated can lead to bacteremia after transplantation. Folliculitis is an infection of the superficial hair follicle and the most prevalent cutaneous manifestation of S. aureus infection in the first 6 months following transplantation [4]. Hogewoning et al. [5] suggest that high-dose immunosuppression predisposes patients to folliculitis due to a diminished immune response. A study [6] found that folliculitis was significantly more prevalent in a group of Egyptian renal transplant recipients than an immunocompetent control group (10.3 vs. 1.7%, respectively). Euvrard et al. [7] found that 6.2% of pediatric SOTRs developed folliculitis. Methicillin-sensitive S. aureus (MSSA) folliculitis presents as follicular pustules and papules most commonly on the scalp and face [8]. MRSA folliculitis is more likely to occur on the trunk and scrotum when compared to MSSA [9]. Folliculitis is treated with topical antibiotics such as mupirocin or clindamycin and antibacterial washes [10]. If MSSA folliculitis is widespread, a 7- to 10-day course of oral dicloxacillin 500 mg q.i.d. or oral cephalexin 500 mg q.i.d. may be pursued [8]. If MRSA is cultured, a 7- to 14-day course of oral clindamycin 450 mg q.i.d. or oral doxycycline 100 mg b.i.d. can be used to resolve symptoms [9].

Impetigo contagiosa, or nonbullous impetigo, is a skin infection associated with species of Staphylococcus or Streptococcus. Patients present with thin-walled vesicles and pustules that later rupture. The residual exudate leaves a classic golden crust [11]. In contrast to impetigo contagiosa, bullous impetigo is associated strictly with staphylococcal infection, particularly strains that produce exfoliative toxin A, which targets the protein desmoglein 1 [12]. Bullous impetigo presents with vesicles that rapidly progress to sharply demarcated, serous or yellow fluid-filled superficial bullae. These bullae easily denude and leave behind a crusted erosion. Hogewoning et al. [5] found that 6.7% of renal transplant recipients developed impetigo of some form. Topical antibiotics, such as mupirocin ointment applied 3 times a day for 5 days, is the preferred treatment for limited impetigo [13], but widespread disease is best managed with systemic antibiotics [14]. Oral dicloxacillin 500 mg q.i.d. or oral cephalexin 500 mg q.i.d. for 7 days are the recommended treatment options for extensive impetigo [15]. If impetigo is suspected to be caused by MRSA, a 14-day course of oral clindamycin 450 mg q.i.d. or oral doxycycline 100 mg b.i.d. should be used [9].

Ecthyma is an ulcerative cutaneous infection commonly seen on the shins or dorsal feet. It initially presents as a painless macule that becomes painful within 24 h and develops into a hemorrhagic vesicle. These vesicles then rupture, leaving behind ulceration with a central black necrotic eschar. The most common causes of ecthyma in SOTRs are staphylococcal and streptococcal species. Ecthyma is treated with systemic antibiotics including oral dicloxacillin 500 mg q.i.d. or oral cephalexin 500 mg q.i.d. for 7 days [15].

Staphylococcal species can also cause necrotizing fasciitis (NF). NF is a devastating cutaneous infection, especially so in the transplant population. NF spreads through the superficial fascia, subcutaneous fat, and deep fascia. It is most commonly seen in the extremities and abdominal wall [16]. NF is associated with a mortality rate between 25 and 30% and is diagnosed in 0.04 cases per 1,000 person-years within the general population [17]. Along with immunosuppression, other risk factors for NF include older age, diabetes, atherosclerosis, and drug or alcohol addiction [18]. Although commonly due to polymicrobial infection, staphylococcal species may be implicated [19]. Transplant recipients with NF are also much more likely to present with shock (50%) when compared to a control group (20.2%) [17]. Treatment of NF requires emergent surgical debridement along with broad-spectrum antimicrobial therapy with the addition of either intravenous vancomycin at 15-20 mg/kg/dose every 8- 12 h or intravenous daptomycin 4 mg/kg once daily to cover for MRSA [20]. In severe cases, amputation may need to be considered to prevent mortality [18,19].

S. aureus is capable of releasing epidermolytic toxins (ETA and ETB), which can cause a potentially fatal condition called staphylococcal scalded skin syndrome (SSSS) [21,22,23]. Clinically, SSSS develops as a scalantiform eruption with flaccid blister formation and a positive Nikolsky sign (Fig. 2a, b). It is seen particularly in the periorificial and flexural areas, although diffuse cutaneous involvement with large regions of epidermal shedding may be seen [24]. Other findings include fever, facial edema, fissures on the lips, and purulent conjunctivitis [25]. SSSS is normally seen in infants or young children and tends to self-resolve in these populations. However, in SOTRs, multisystem failure and electrolyte disturbance associated with SSSS can be potentially fatal [26]. The diagnosis is confirmed with biopsy or with a frozen section of a skin sample [26]. A Gram stain may be negative because the progression of the condition is due to toxin and not the presence of the bacteria itself [25]. Treatment is initiated with a parenteral penicillinase-resistant antistaphylococcal antibiotic such as intravenous flucloxacillin 500 mg per day, divided into 4 portions [27]. If the patient fails to improve following antistaphylococcal antibiotic therapy, MRSA should be considered as a possible source of infection and switching treatment to vancomycin may be considered [28]. Additionally, supportive skin care, intravenous fluids, and admission to the ICU or burn unit may be necessary depending on disease severity.

Fig. 2

a, b SSSS presenting with fragile bullae, desquamation, and a positive Nikolsky sign.

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In recent years, there has been increasing evidence of community-acquired MRSA skin infections affecting posttransplant patients [29,30,31]. In 1 study [30], 3 of 11 (27%) patients with skin or wound infection after lung transplantation were infected with MRSA. Four of 11 (36%) were infected with MSSA, showing that S. aureus alone was responsible for 63% of skin or wound infections in lung transplant recipients [30]. Community-acquired MRSA infections are generally susceptible to an array of broad-spectrum antibiotics when compared to hospital-acquired MRSA [30]. A large study [31] on liver transplant recipients found that nasal colonization by S. aureus was associated with an increased likelihood of MRSA infection, and patients who developed MRSA infection had twice the risk of death. These findings suggest that SOTRs should be evaluated and treated for nasal MRSA colonization, as this may lower mortality rates in transplant recipients [31,32]. Regardless of MRSA infection type, sensitivity testing must be conducted owing to potentially large differences in antibiotic resistance between MRSA strains [29].

Cutaneous Streptococcal Infections

In SOTRs, streptococcal species are associated with causing a variety of skin infections, such as impetigo contagiosa [5], ecthyma, and NF [33]. Streptococcus pyogenes is the most common pathogen to cause monomicrobial NF [17], though Streptococcus pneumoniae has also caused disease in renal transplant recipients [34]. The management of these infections is similar whether infection is due to staphylococcal or streptococcal species.

Cutaneous Pseudomonal Infections

A severer variant, commonly regarded as a sign of underlying septicemia, is ecthyma gangrenosum (EG). The most common infection associated with EG is Pseudomonas aeruginosa[35]. EG lesions are described as gunmetal gray tense pustules that later evolve into round ulcerations with necrotic black eschars and surrounding erythema (Fig. 3) [35].

Fig. 3

Ecthyma gangrenosum presenting as a large ulceration with a black necrotic eschar. Reprinted with permission from Frey et al. [74]. Copyright 2014 by the Korean Society of Plastic and Reconstructive Surgeons.

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Nakai et al. [35] reported a case of EG without associated septicemia in a renal transplant recipient. Even without evidenced bacteremia, the patient showed progression of EG with numerous ulcerations and rapid spreading. This case was of particular interest given the presence of both P. aeruginosa and MRSA within the wound but the absence of both in the blood. It is imperative to make an early diagnosis and begin treatment promptly for suspected EG in the SOTRs [36]. Even without associated sepsis, immunosuppressed patients can rapidly develop life-threatening disease [35]. EG is treated using antipseudomonal monotherapy with intravenous ticarcillin-clavulanate 3.1 g/4 h (not currently available in the USA or Canada) or intravenous piperacillin-tazobactam 4.5 g/ 6 h [37]. Although controversial, dual therapy with an antipseudomonal penicillin and an aminoglycoside or other antipseudomonal is recommended in SOTRs [38].

In the renal transplant population, 1 study [39] found that the majority of NF infections (36.4%) were fungal, likely due to the iatrogenic immunosuppression. P. aeruginosa and Escherichia coli are other infectious causes linked with NF development in the renal transplant population [17]. There has also been a reported case of fatal NF due to carbapenem-resistant Acinetobacter baumannii in a transplant recipient [40].

Cutaneous Escherichia coli Infections

In SOTRs, 2 cases [39,41] of NF due to E. coli have been described. NF due to E. coli is managed with surgical debridement along with dual therapy with ciprofloxacin and imipenem for antimicrobial therapy [39].

Cutaneous Nocardial Infections

Nocardial infection in the immunocompromised host can lead to localized infection or hematogenous spread, causing disseminated nocardiosis. Localized infection can include ulcers, abscess formation, granulomas, soft tissue infection, and lymphocutaneous infection. In SOTRs, disseminated disease with organ involvement has been described [42]. Disseminated nocardiosis may present with pustules, abscesses, or subcutaneous nodules (Fig. 4) [43]. For diagnosis, both microbiological and histological testing on biopsy specimens should be performed with attempts to culture Nocardia. Depending on infection severity, the immunosuppressive regimen may need to be modified, and combination therapy with imipenem along with either trimethoprim-sulfamethoxazole, amikacin, or linezolid should be started [44]. A study [45] found that SOTRs with nocardiasis treated for a median duration of 56 days had a 1-year cure rate of 88%.

Fig. 4

Disseminated nocardiosis presenting as an indurated, erythematous plaque on the lower extremity. Reprinted with permission from Drone et al. [75]. Copyright 2014 by the Indian Dermatology Online Journal.

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Cutaneous Mycobacterial Infections

Cutaneous mycobacterial infection in SOTRs is most commonly due to nontuberculous mycobacteria (Mycobacterium marinum, M. haemophilum, M. fortuitum, M. chelonae, M. abscessus and M. ulcerans, or M. immunogenum), although 2 cases of hematogenous dissemination of M. tuberculosis leading to cutaneous tuberculosis have been described [46].

Cutaneous manifestations of mycobacterial infections range from macular erythema to nonhealing ulcers, although erythematous nodules and papules are the most common presentations [46]. In kidney transplant recipients, cutaneous nontuberculous mycobacteria may present with painless, violaceous nodules that can ulcerate and manifest with a sporotrichoid appearance [45].

Hematogenous spread of mycobacterial infection could present as nodules or abscesses. Disseminated disease in transplant recipients is most commonly caused by M. chelonae, presenting with multiple red subcutaneous nodules or abscesses [47]. Additional nontuberculous mycobacteria associated with disseminated infection include M. kansasii, M. haemophilum, M. fortuitum, and others [48]. Other presentations include lupus vulgaris, which presents with small, sharply defined red papules with gelatinous consistency, or acute miliary tuberculosis, which presents with millet-sized red papules that may progress into ulcers and abscesses. Presentations with subcutaneous abscesses, cellulitis, erysipelas, or pseudotumors have also been described [46,49,50].

There are cases of M. leprae causing lepromatous leprosy in SOTRs [51,52,53]. Infection with M. leprae in the SOTR population presents with a variety of cutaneous manifestations (Fig. 5). Currently, there are 16 reported cases of lepromatous leprosy in SOTRs. One case [52] in a heart transplant recipient described the presence of a migratory papular red rash over the upper torso along with violaceous papules on the hands. A report on a renal transplant recipient describes development of a hypoesthetic, hypopigmented patch with thickening and tenderness of an adjacent nerve [51]. Another case describes a renal transplant recipient with erythematous papules and nodules over the face and earlobes, scars on the knee, and purulent discharge and impetiginous crust over the hands and feet [54]. Leprosy infections can range from milder tuberculoid to severe lepromatous infections. Immunosuppression in SOTRs is thought to contribute to disease severity as it reduces T-cell function [53]. All reported cases of lepromatous leprosy in SOTRs occurred in endemic areas or in patients originally from endemic regions [51,52,53,55,56,57]. Currently, there are limited data on the effect of leprosy infection on allograft function or on the association between immunosuppression and leprosy infection.

Fig. 5

Tuberculoid leprosy presenting as an annular, anesthetic plaque on the forearm. Reprinted with permission from Thakkar and Patel [76].

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When mycobacterial infection is being considered, a tissue specimen should be cultured for species identification and sensitivity. Polymerase chain reaction (PCR) may be used for mycobacterial identification owing to the 12-week period needed to culture mycobacterial species. In the past, PCR only allowed for the differentiation between nontuberculous and tuberculous mycobacteria; However, recent advancements in PCR techniques allow clinicians to distinguish between nontuberculous mycobacterial species [58,59,60,61].

Treatment of cutaneous mycobacterial infection depends on the species and sensitivity data. Limited M. marinum may be managed with monotherapy using either clarithromycin, doxycycline, minocycline, or trimethoprim-sulfamethoxazole for 3 months. Severe M. marinum skin infection is managed using combination therapy with rifampin and ethambutol [47]. M. ulcerans is managed with rifampin and streptomycin treatment for 8 weeks along with surgical intervention [47]. Guidelines for treating nontuberculous mycobacteria are not clearly defined; hence, infectious disease consultation is advised in transplant recipients who develop mycobacterial infection. For primary prevention, transplant recipients should avoid fish tank water and fresh fish because exposure to these agents is a risk factor for infection with M. marinum and other nontuberculous mycobacterial species [49]. Acupuncture is associated with nontuberculous mycobacterial infections, and SOTRs should be appropriately cautioned [46,62,63].

Cutaneous Bartonella henselae Infections

Bacillary angiomatosis (BA) is a vasculoproliferative disorder caused by Bartonella species [64]. The most common bacterium associated with BA in SOTRs is B. henselae[64]. The classic presentation is with smooth, domed red or violaceous lesions that resemble hemangiomas. Lesions can be solitary or widespread and scattered, normally on the face and extremities. Development of cellulitis or of a large flesh-colored indurated mass is also a possible presentation. These lesions are very vascular and bleed with minor trauma. Additional findings include fever, lymphadenopathy, and vascular nodules within organs [64]. Exposure to the bacterium is most commonly through cats. About 25% of cases of BA in SOTRs were in the pediatric or adolescent population, despite only 3-4% of transplant recipients being in this age range [65,66,67,68,69]. BA can be associated with some devastating consequences. There have been documented occurrences of hemophagocytic syndrome and renal graft rejection, both due to BA in renal transplant recipients [65,70].

BA may have an exceedingly similar presentation to that of Kaposi's sarcoma or pyogenic granuloma. A consequence of this similarity is the potential delay in diagnosis and subsequent treatment. A diagnosis can be made with electron microscopy showing clumped and solitary rods within the intercellular space. An alternative is using the Warthin-Starry stain, but this test may be difficult to interpret [64]. Bartonella species are difficult to identify in culture, and a negative result should not rule out disease [71]. Antibiotic therapy with doxycycline 100 mg b.i.d. for 3 months is recommended for BA in HIV patients [71]. Both ciprofloxacin and doxycycline have been used to resolve BA in SOTRs [72,73].

Conclusion

SOTRs may present with a wide variety of cutaneous findings. Sources of skin pathology in SOTRs include infection, drug toxicity, and malignancy. Bacterial skin infections can vary in presentation, severity, and prognosis. In order to best reduce disease-associated morbidity and mortality, SOTR care providers must promptly identify, diagnose, and treat bacterial skin infections.

Key Message

A comprehensive review of bacterial cutaneous infections in the solid organ transplant population is presented.

Disclosure Statement

The authors have no conflicts of interest to disclose.


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  60. Springer B, Stockman L, Teschner K, Roberts GD, Bottger EC: Two-laboratory collaborative study on identification of mycobacteria: molecular versus phenotypic methods. J Clin Microbiol 1996;34:296-303.
  61. Shrestha NK, Tuohy MJ, Hall GS, Reischl U, Gordon SM, Procop GW: Detection and differentiation of Mycobacterium tuberculosis and nontuberculous mycobacterial isolates by real-time PCR. J Clin Microbiol 2003;41:5121-5126.
  62. Woo PC, Li JH, Tang W, Yuen K: Acupuncture mycobacteriosis. N Engl J Med 2001;345:842-843.
  63. Tang P, Walsh S, Murray C, Alterman C, Varia M, Broukhanski G, Chedore P, DeKoven J, Assaad D, Gold WL, Ghazarian D, Finkelstein M, Pritchard M, Yaffe B, Jamieson F, Henry B, Phillips E: Outbreak of acupuncture-associated cutaneous Mycobacterium abscessus infections. J Cutan Med Surg 2006;10:166-169.
  64. Moulin C, Kanitakis J, Ranchin B, Chauvet C, Gillet Y, Morelon E, Euvrard S: Cutaneous bacillary angiomatosis in renal transplant recipients: report of three new cases and literature review. Transpl Infect Dis 2012;14:403-409.
  65. Apalsch AM, Nour B, Jaffe R: Systemic cat-scratch disease in a pediatric liver transplant recipient and review of the literature. Pediatr Infect Dis J 1993;12:769-774.
  66. Dharnidharka VR, Richard GA, Neiberger RE, Fennell RS 3rd: Cat scratch disease and acute rejection after pediatric renal transplantation. Pediatr Transplant 2002;6:327-331.
  67. Rheault MN, van Burik JA, Mauer M, Ingulli E, Ferrieri P, Jessurun J, Chavers BM: Cat-scratch disease relapse in a kidney transplant recipient. Pediatr Transplant 2007;11:105-109.
  68. Juskevicius R, Vnencak-Jones C: Pathologic quiz case: a 17-year-old renal transplant patient with persistent fever, pancytopenia, and axillary lymphadenopathy. Bacillary angiomatosis of the lymph node in the renal transplant recipient. Arch Pathol Lab Med 2004;128:e12-e14.
  69. Scolfaro C, Mignone F, Gennari F, Alfarano A, Veltri A, Romagnoli R, Salizzoni M: Possible donor-recipient bartonellosis transmission in a pediatric liver transplant. Transpl Infect Dis 2008;10:431-433.
  70. Karras A, Thervet E, Legendre C; Groupe Cooperatif de transplantation d'Ile de France: Hemophagocytic syndrome in renal transplant recipients: report of 17 cases and review of literature. Transplantation 2004;77:238-243.
  71. Rolain JM, Brouqui P, Koehler JE, Maguina C, Dolan MJ, Raoult D: Recommendations for treatment of human infections caused by Bartonella species. Antimicrob Agents Chemother 2004;48:1921-1933.
  72. Patel SJ, Petrarca R, Shah SM, Zimmer-Galler I, Janjua KA, Do DV, Nguyen QD: Atypical Bartonella henselae chorioretinitis in an immunocompromised patient. Ocul Immunol Inflamm 2008;16:45-49.
  73. Nadimi AE, Cheng K, Radfar A: Bacillary angiomatosis from Bartonella quintana in a cardiac transplant patient. J Am Acad Dermatol 2016;74:AB150.
  74. Frey JD, Latkowski J-AM, Louie E, Chiu ES: Diagnosis and management of ecthyma gangrenosum in chronic renal failure patient. Arch Plastic Surg 2014;41:299.
  75. Drone ER, McCrory AL, Lane N, Fiala K: Disseminated nocardiosis in a patient on infliximab and methylprednisolone for treatment-resistant Sweet's syndrome. Indian Dermatol Online J 2014;5:300.
  76. Thakkar S, Patel SV: Clinical profile of leprosy patients: a prospective study. Indian J Dermatol 2014;59:160.

Author Contacts

Nishita Maganty, MPH

Department of Dermatology, Mayo Clinic Arizona

13400 E. Shea Blvd.

Scottsdale, AZ 85259 (USA)

E-Mail nmaganty@email.arizona.edu


Article / Publication Details

First-Page Preview
Abstract of Review Paper

Received: July 02, 2017
Accepted: October 14, 2017
Published online: January 10, 2018
Issue release date: February 2018

Number of Print Pages: 8
Number of Figures: 5
Number of Tables: 1

ISSN: 1018-8665 (Print)
eISSN: 1421-9832 (Online)

For additional information: https://www.karger.com/DRM


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  64. Moulin C, Kanitakis J, Ranchin B, Chauvet C, Gillet Y, Morelon E, Euvrard S: Cutaneous bacillary angiomatosis in renal transplant recipients: report of three new cases and literature review. Transpl Infect Dis 2012;14:403-409.
  65. Apalsch AM, Nour B, Jaffe R: Systemic cat-scratch disease in a pediatric liver transplant recipient and review of the literature. Pediatr Infect Dis J 1993;12:769-774.
  66. Dharnidharka VR, Richard GA, Neiberger RE, Fennell RS 3rd: Cat scratch disease and acute rejection after pediatric renal transplantation. Pediatr Transplant 2002;6:327-331.
  67. Rheault MN, van Burik JA, Mauer M, Ingulli E, Ferrieri P, Jessurun J, Chavers BM: Cat-scratch disease relapse in a kidney transplant recipient. Pediatr Transplant 2007;11:105-109.
  68. Juskevicius R, Vnencak-Jones C: Pathologic quiz case: a 17-year-old renal transplant patient with persistent fever, pancytopenia, and axillary lymphadenopathy. Bacillary angiomatosis of the lymph node in the renal transplant recipient. Arch Pathol Lab Med 2004;128:e12-e14.
  69. Scolfaro C, Mignone F, Gennari F, Alfarano A, Veltri A, Romagnoli R, Salizzoni M: Possible donor-recipient bartonellosis transmission in a pediatric liver transplant. Transpl Infect Dis 2008;10:431-433.
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  72. Patel SJ, Petrarca R, Shah SM, Zimmer-Galler I, Janjua KA, Do DV, Nguyen QD: Atypical Bartonella henselae chorioretinitis in an immunocompromised patient. Ocul Immunol Inflamm 2008;16:45-49.
  73. Nadimi AE, Cheng K, Radfar A: Bacillary angiomatosis from Bartonella quintana in a cardiac transplant patient. J Am Acad Dermatol 2016;74:AB150.
  74. Frey JD, Latkowski J-AM, Louie E, Chiu ES: Diagnosis and management of ecthyma gangrenosum in chronic renal failure patient. Arch Plastic Surg 2014;41:299.
  75. Drone ER, McCrory AL, Lane N, Fiala K: Disseminated nocardiosis in a patient on infliximab and methylprednisolone for treatment-resistant Sweet's syndrome. Indian Dermatol Online J 2014;5:300.
  76. Thakkar S, Patel SV: Clinical profile of leprosy patients: a prospective study. Indian J Dermatol 2014;59:160.