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Coexisting Cytomegalovirus Infection in Immunocompetent Patients with Clostridium Difficile Colitis Khee-Siang Chan A, Wen-Ying Lee B,C, Wen-Liang Yu A,D,*

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Coexisting Cytomegalovirus Infection in Immunocompetent Patients with Clostridium Difficile Colitis Khee-Siang Chan A, Wen-Ying Lee B,C, Wen-Liang Yu A,D,* View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Journal of Microbiology, Immunology and Infection (2016) 49, 829e836 Available online at www.sciencedirect.com ScienceDirect journal homepage: www.e-jmii.com REVIEW ARTICLE Coexisting cytomegalovirus infection in immunocompetent patients with Clostridium difficile colitis Khee-Siang Chan a, Wen-Ying Lee b,c, Wen-Liang Yu a,d,* a Department of Intensive Care Medicine, Chi Mei Medical Center, Tainan City, Taiwan b Department of Pathology, Chi Mei Medical Center, Tainan City, Taiwan c Department of Pathology, Taipei Medical University, Taipei City, Taiwan d Department of Medicine, Taipei Medical University, Taipei City, Taiwan Received 30 June 2015; received in revised form 31 October 2015; accepted 14 December 2015 Available online 12 January 2016 KEYWORDS Abstract Cytomegalovirus (CMV) colitis usually occurs in immunocompromised patients with Clostridium difficile; human immunodeficiency virus infection, organ transplantation, and malignancy receiving C. difficile infection; chemotherapy or ulcerative colitis receiving immunosuppressive agents. However, CMV colitis colitis; is increasingly recognized in immunocompetent hosts. Notably, CMV colitis coexisting with cytomegalovirus; Clostridium difficile infection (CDI) in apparently healthy individuals has been published in immunocompetent recent years, which could result in high morbidity and mortality. CMV colitis is a rare but possible differential diagnosis in immunocompetent patients with abdominal pain, watery, or especially bloody diarrhea, which could be refractory to standard treatment for CDI. As a characteristic of CDI, however, pseudomembranous colitis may be only caused by CMV infec- tion. Real-time CMV-polymerase chain reaction (PCR) for blood and stool samples may be a useful and noninvasive diagnostic strategy to identify CMV infection when treatment of CDI eventually fails to show significant benefits. Quantitative CMV-PCR in mucosal biopsies may in- crease the diagnostic yield of traditional histopathology. CMV colitis is potentially life- threatening if severe complications occur, such as sepsis secondary to colitis, massive colo- rectal bleeding, toxic megacolon, and colonic perforation, so that may necessitate pre- emptive antiviral treatment for those who are positive for CMV-PCR in blood and/or stool sam- ples while pending histological diagnosis. Copyright ª 2016, Taiwan Society of Microbiology. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by- nc-nd/4.0/). * Corresponding author. Department of Medical Research, Chi Mei Medical Center, Number 901, Zhonghua Road, Yongkang District, 710 Tainan City, Taiwan. E-mail address: [email protected] (W.-L. Yu). http://dx.doi.org/10.1016/j.jmii.2015.12.007 1684-1182/Copyright ª 2016, Taiwan Society of Microbiology. Published by Elsevier Taiwan LLC. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 830 K.-S. Chan et al. Background The biopsy-proven diagnosis was made for eight patients. Other probable cases were diagnosed based on clinical Cytomegalovirus (CMV) is a highly prevalent and globally symptoms with detection of blood CMV DNA plus either colonoscopic findings or detection of CMV DNA in stool distributed virus. CMV infection in healthy adults is usually 28 asymptomatic or causes a mildly infectious mononucleosis- samples. Traditionally, CMV colitis was easily neglected and underdiagnosed in ICU patients with chronic critical like syndrome. CMV then usually becomes dormant until 23,27,28 reactivation in patients with severely immunocompromised illness, particularly with chronic renal failure. status, who may potentially develop invasive CMV disease with a wide range of manifestations, most commonly Epidemiology of C. difficile colitis colorectal infection with hemorrhagic ulceration. Two coexistent entitiesdCMV colitis and Clostridium difficile colitisdhave usually been reported among immunocom- Diseases caused by C. difficile range from mild diarrhea to promised patients, who have human immunodeficiency potentially life-threatening pseudomembranous colitis. CDIs occur primarily in hospitalized patients with risk fac- virus infection, organ transplantation, hematologic malig- 29 nancy, solitary organ cancer, or inflammatory bowel disease tors such as concomitant or recent use of antibiotics. The receiving immunosuppressive agents.1e9 For example, colonization rate of C. difficile in adult hospitalized pa- 8 tients shows geographic variation, ranging from 4.4% to Florescu et al reviewed nine patients who developed C. 30 difficile and CMV colitis; among them, eight patients were 23.2%. The hypervirulent C. difficile strains such as the epidemic clone (027/NAP1/BI) has partly contributed to immunocompromised: four transplant recipients, two 31 oncology patients, one patient with advanced acquired change the CDI epidemiology to worldwide dissemination. immunodeficiency syndrome, and one on an immunosup- In particular, elderly patients in surgical wards and ICUs are at significant risk of developing CDI.32 After 2006, a 47% pressive regimen for severe ulcerative colitis. Besides, CMV 33 colitis can mimic or present as pseudomembranous colitis in increase in the rate of CDI was noted in the USA. In a immunocompromised patients.10e14 cohort of hospitalized older adults in Michigan, impaired functional status was an independent risk factor for severe CMV gastrointestinal disease rarely occurs in immuno- 34 competent patients and could resolve completely without CDI. In one study in Korea between January 2007 and July the use of antiviral drugs, if the immunity is obtained.15 In 2012, 55% of colitis in elderly people in long-term care fa- addition, CMV colitis is increasingly recognized in appar- cilities was caused by CDI, whereas nonspecific colitis was most common (63%) in elderly people in local commu- ently immunocompetent patients in some immunomodu- 35 lating conditions, such as elderly, pregnancy, chronic renal nities. Diagnosis of CDI is based on the identification of C. failure, coronary artery disease, ischemic heart disease, difficile toxins A and B in diarrheal stool. First-line antibi- otics for CDI treatment are metronidazole and vancomy- congestive heart failure, diabetes mellitus, steroid use, 36 blood transfusion, and prolonged stay in the intensive care cin. Fidaxomicin, a macrolide antibiotic, has been shown 15e28 to be significantly effective in treating CDI compared with units (ICUs). However, CMV colitis in these patients has 37 often been neglected by clinical physicians.28 Therefore, vancomycin. For recurrence and relapse of CDI, rifaximin and tigecycline have yielded some positive outcomes this review article will mainly focus on English literature of 38 CMV colitis coexisting, following, or followed by C. difficile against C. difficile. Fecal microbiota transplant is an alternative therapy for CDI that is effective and promising colitis among previously healthy or apparently immuno- 39 competent adult patients. We will also review those cases in multiple CDI recurrences. of CMV colitis presenting as a sole cause of pseudomem- branous colitis without C. difficile infection (CDI). Coexisting CMV and C. difficile colitis Epidemiology of CMV colitis in A history of cytomegalovirus infection has been recognized immunocompetent patients as one of the significant risk factors for C. difficile coloni- zation.30,40 Adult patients colonized with toxigenic C. One systemic review identified only 91 immunocompetent difficile were prone to the subsequent development of C. patients with gastrointestinal CMV infections for the period difficile-associated diarrhea.30 Critically ill patients and of 1950e2007.25 Another literature review from 1980 to elderly patients are at an increased risk of developing 2003 identified 44 immunocompetent patients with CMV diarrheal illness like CDI and CMV colitis. Literature of colitis. Among them, spontaneous remission occurred in coexisting CMV and C. difficile colitis have been reported in 31.8%, mostly individuals <55 years old.21 In Korea, 51 immunocompetent patients, mostly in the years after 2010 immunocompetent patients with CMV colitis, including 11 (Table 1), implying that effective alerts are increasing to ICU patients and 17.6% with spontaneous remission, were current physicians. Presenting symptoms of both diseases diagnosed at a tertiary care university hospital between included fever, diarrhea, gastrointestinal bleeding, and January 1995 and February 2014.23 In specific hospital ICU abdominal pain, with predominance of severe watery units, CMV colitis was diagnosed in 14 previously immuno- diarrhea for CD, and bloody stool and occasional massive competent ICU patients at a teaching hospital in Brazil from bleeding for CMV colitis. Both may cause toxic megacolon January 2000 to March 2013.27 While in Taiwan, with and bowel perforation, leading to a poor prognosis.51 intention to diagnosis, CMV colitis was detected in 18 ICU However, we propose that the clinical features of colitis patients at a teaching hospital from January 2011 through caused by both etiologies could vary with the following June 2013.28 Among them, three patients had malignancy. scenarios (Table 1). Cytomegalovirus and Clostridium difficile colitis 831 Table 1 The clinical features of cytomegalovirus colitis coexisting, following, or mimicking Clostridium
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