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Published in: Current HIV/AIDS Reports 3/2013

01-09-2013 | Co-infections (MA Jacobson, Section Editor)

Clostridium Difficile Infection in Patients with HIV/AIDS

Authors: Paul J. Collini, Ed Kuijper, David H. Dockrell

Published in: Current HIV/AIDS Reports | Issue 3/2013

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Abstract

Clostridium difficile infection (CDI) affects significant numbers of hospitalized patients and is an increasing problem in the community. It is also among the most commonly isolated pathogens in HIV patients with diarrheal illness and is ≥2 fold more common in HIV-seropositive individuals. This association is stronger in those with low absolute CD4 T cell counts or meeting clinical criteria for an AIDS diagnosis, and was most pronounced before the wide availability of highly active antiretroviral therapy. The presentation and outcome of CDI in HIV appears similar to the general population. The increased risk can in part be attributed to increased hospitalization and antimicrobial use, but HIV related alterations in fecal microbiota, gut mucosal integrity, and humoral and cell mediated immunity are also likely to play a role. Here we review the evidence for these observations and the relevance of recent advances in the diagnosis and management of CDI for the HIV clinician.
Literature
1.
go back to reference Bartlett JG, Moon N, Chang TW, et al. Role of Clostridium difficile in antibiotic-associated pseudomembranous colitis. Gastroenterology. 1978;75(5):778–82.PubMed Bartlett JG, Moon N, Chang TW, et al. Role of Clostridium difficile in antibiotic-associated pseudomembranous colitis. Gastroenterology. 1978;75(5):778–82.PubMed
2.
go back to reference George RH, Symonds JM, Dimock F, et al. Identification of Clostridium difficile as a cause of pseudomembranous colitis. Br Med J. 1978;1(6114):695.PubMedCrossRef George RH, Symonds JM, Dimock F, et al. Identification of Clostridium difficile as a cause of pseudomembranous colitis. Br Med J. 1978;1(6114):695.PubMedCrossRef
3.
go back to reference Bauer MP, Notermans DW, van Benthem BH, et al. Clostridium difficile infection in Europe: a hospital-based survey. Lancet. 2011;377(9759):63–73.PubMedCrossRef Bauer MP, Notermans DW, van Benthem BH, et al. Clostridium difficile infection in Europe: a hospital-based survey. Lancet. 2011;377(9759):63–73.PubMedCrossRef
4.
go back to reference Lucado J, Gould C, Elixhauser A. Clostridium Difficile Infections (CDI) in Hospital Stays, 2009: Statistical Brief #124. 2012 Feb. Lucado J, Gould C, Elixhauser A. Clostridium Difficile Infections (CDI) in Hospital Stays, 2009: Statistical Brief #124. 2012 Feb.
5.
go back to reference Khanna S, Pardi DS, Aronson SL, et al. The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am J Gastroenterol. 2012;107(1):89–95.PubMedCrossRef Khanna S, Pardi DS, Aronson SL, et al. The epidemiology of community-acquired Clostridium difficile infection: a population-based study. Am J Gastroenterol. 2012;107(1):89–95.PubMedCrossRef
6.
go back to reference • Jones AM, Kuijper EJ, Wilcox MH. Clostridium difficile: a European perspective. J Infect. 2013;66(2):115–28. Recent review article of CDI epidemiology including epidemic strains. • Jones AM, Kuijper EJ, Wilcox MH. Clostridium difficile: a European perspective. J Infect. 2013;66(2):115–28. Recent review article of CDI epidemiology including epidemic strains.
7.
go back to reference Chang JY, Antonopoulos DA, Kalra A, et al. Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis. 2008;197(3):435–8.PubMedCrossRef Chang JY, Antonopoulos DA, Kalra A, et al. Decreased diversity of the fecal Microbiome in recurrent Clostridium difficile-associated diarrhea. J Infect Dis. 2008;197(3):435–8.PubMedCrossRef
8.
go back to reference Collini PJ, Bauer M, Kuijper E, et al. Clostridium difficile infection in HIV-seropositive individuals and transplant recipients. J Infect. 2012;64(2):131–47.PubMedCrossRef Collini PJ, Bauer M, Kuijper E, et al. Clostridium difficile infection in HIV-seropositive individuals and transplant recipients. J Infect. 2012;64(2):131–47.PubMedCrossRef
9.
go back to reference Dial S, Delaney JA, Barkun AN, et al. Use of gastric acid-suppressive agents and the risk of community-acquired Clostridium difficile-associated disease. JAMA. 2005;294(23):2989–95.PubMedCrossRef Dial S, Delaney JA, Barkun AN, et al. Use of gastric acid-suppressive agents and the risk of community-acquired Clostridium difficile-associated disease. JAMA. 2005;294(23):2989–95.PubMedCrossRef
10.
go back to reference Fujihashi K, Kiyono H. Mucosal immunosenescence: new developments and vaccines to control infectious diseases. Trends Immunol. 2009;30(7):334–43.PubMedCrossRef Fujihashi K, Kiyono H. Mucosal immunosenescence: new developments and vaccines to control infectious diseases. Trends Immunol. 2009;30(7):334–43.PubMedCrossRef
11.
go back to reference Hopkins MJ, Macfarlane GT. Changes in predominant bacterial populations in human faeces with age and with Clostridium difficile infection. J Med Microbiol. 2002;51(5):448–54.PubMed Hopkins MJ, Macfarlane GT. Changes in predominant bacterial populations in human faeces with age and with Clostridium difficile infection. J Med Microbiol. 2002;51(5):448–54.PubMed
12.
go back to reference Shulzhenko N, Morgun A, Hsiao W, et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat Med. 2011;17(12):1585–93.PubMedCrossRef Shulzhenko N, Morgun A, Hsiao W, et al. Crosstalk between B lymphocytes, microbiota and the intestinal epithelium governs immunity versus metabolism in the gut. Nat Med. 2011;17(12):1585–93.PubMedCrossRef
13.
go back to reference • Cohen SH, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol. 2010;31(5):431–55. Infectious Disease Society of America (IDSA) guidelines for CDI diagnosis and management 2010.PubMedCrossRef • Cohen SH, Gerding DN, Johnson S, et al. Clinical practice guidelines for Clostridium difficile infection in adults: 2010 update by the society for healthcare epidemiology of America (SHEA) and the infectious diseases society of America (IDSA). Infect Control Hosp Epidemiol. 2010;31(5):431–55. Infectious Disease Society of America (IDSA) guidelines for CDI diagnosis and management 2010.PubMedCrossRef
14.
go back to reference Bauer MP, Kuijper EJ, van Dissel JT. European Society of Clinical Microbiology and Infectious Diseases (ESCMID): treatment guidance document for Clostridium difficile infection (CDI). Clin Microbiol Infect. 2009;15(12):1067–79.PubMedCrossRef Bauer MP, Kuijper EJ, van Dissel JT. European Society of Clinical Microbiology and Infectious Diseases (ESCMID): treatment guidance document for Clostridium difficile infection (CDI). Clin Microbiol Infect. 2009;15(12):1067–79.PubMedCrossRef
15.
go back to reference Kuijper EJ, Coignard B, Tull P. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect. 2006;12 Suppl 6:2–18.PubMedCrossRef Kuijper EJ, Coignard B, Tull P. Emergence of Clostridium difficile-associated disease in North America and Europe. Clin Microbiol Infect. 2006;12 Suppl 6:2–18.PubMedCrossRef
16.
go back to reference Crobach MJ, Dekkers OM, Wilcox MH, et al. European Society of Clinical Microbiology and Infectious Diseases (ESCMID): data review and recommendations for diagnosing Clostridium difficile-infection (CDI). Clin Microbiol Infect. 2009;15(12):1053–66.PubMedCrossRef Crobach MJ, Dekkers OM, Wilcox MH, et al. European Society of Clinical Microbiology and Infectious Diseases (ESCMID): data review and recommendations for diagnosing Clostridium difficile-infection (CDI). Clin Microbiol Infect. 2009;15(12):1053–66.PubMedCrossRef
18.
go back to reference Bartlett JG. Treatment of antibiotic-associated pseudomembranous colitis. Rev Infect Dis. 1984;6 Suppl 1:S235–41.PubMedCrossRef Bartlett JG. Treatment of antibiotic-associated pseudomembranous colitis. Rev Infect Dis. 1984;6 Suppl 1:S235–41.PubMedCrossRef
19.
go back to reference Bauer MP, Hensgens MP, Miller MA, et al. Renal failure and leukocytosis are predictors of a complicated course of Clostridium difficile infection if measured on day of diagnosis. Clin Infect Dis. 2012;55 Suppl 2:S149–53.PubMedCrossRef Bauer MP, Hensgens MP, Miller MA, et al. Renal failure and leukocytosis are predictors of a complicated course of Clostridium difficile infection if measured on day of diagnosis. Clin Infect Dis. 2012;55 Suppl 2:S149–53.PubMedCrossRef
20.
go back to reference Nelson RL, Kelsey P, Leeman H, et al. Antibiotic treatment for Clostridium difficile-associated diarrhea in adults. Cochrane Database Syst Rev. 2011;9:CD004610.PubMed Nelson RL, Kelsey P, Leeman H, et al. Antibiotic treatment for Clostridium difficile-associated diarrhea in adults. Cochrane Database Syst Rev. 2011;9:CD004610.PubMed
21.
go back to reference Neal MD, Alverdy JC, Hall DE, et al. Diverting loop ileostomy and colonic lavage: an alternative to total abdominal colectomy for the treatment of severe, complicated Clostridium difficile associated disease. Ann Surg. 2011;254(3):423–7. discussion 7–9.PubMedCrossRef Neal MD, Alverdy JC, Hall DE, et al. Diverting loop ileostomy and colonic lavage: an alternative to total abdominal colectomy for the treatment of severe, complicated Clostridium difficile associated disease. Ann Surg. 2011;254(3):423–7. discussion 7–9.PubMedCrossRef
22.
go back to reference Johnson S. Recurrent Clostridium difficile infection: a review of risk factors, treatments, and outcomes. J Infect. 2009;58(6):403–10.PubMedCrossRef Johnson S. Recurrent Clostridium difficile infection: a review of risk factors, treatments, and outcomes. J Infect. 2009;58(6):403–10.PubMedCrossRef
23.
go back to reference •• Louie TJ, Miller MA, Mullane KM, et al. Fidaxomicin versus vancomycin for Clostridium difficile infection. N Engl J Med. 2011;364(5):422–31. Randomized controlled trial demonstrating efficacy of new drug Fidaxomycin for first episode and recurrent CDI.PubMedCrossRef •• Louie TJ, Miller MA, Mullane KM, et al. Fidaxomicin versus vancomycin for Clostridium difficile infection. N Engl J Med. 2011;364(5):422–31. Randomized controlled trial demonstrating efficacy of new drug Fidaxomycin for first episode and recurrent CDI.PubMedCrossRef
24.
go back to reference Cornely OA, Miller MA, Louie TJ, et al. Treatment of first recurrence of Clostridium difficile infection: fidaxomicin versus vancomycin. Clin Infect Dis. 2012;55 Suppl 2:S154–61.PubMedCrossRef Cornely OA, Miller MA, Louie TJ, et al. Treatment of first recurrence of Clostridium difficile infection: fidaxomicin versus vancomycin. Clin Infect Dis. 2012;55 Suppl 2:S154–61.PubMedCrossRef
25.
go back to reference Louie TJ, Cannon K, Byrne B, et al. Fidaxomicin preserves the intestinal microbiome during and after treatment of Clostridium difficile infection (CDI) and reduces both toxin reexpression and recurrence of CDI. Clin Infect Dis. 2012;55 Suppl 2:S132–42.PubMedCrossRef Louie TJ, Cannon K, Byrne B, et al. Fidaxomicin preserves the intestinal microbiome during and after treatment of Clostridium difficile infection (CDI) and reduces both toxin reexpression and recurrence of CDI. Clin Infect Dis. 2012;55 Suppl 2:S132–42.PubMedCrossRef
26.
go back to reference Goldstein EJ, Citron DM, Sears P, et al. Comparative susceptibilities to fidaxomicin (OPT-80) of isolates collected at baseline, recurrence, and failure from patients in two phase III trials of fidaxomicin against Clostridium difficile infection. Antimicrob Agents Chemother. 2011;55(11):5194–9.PubMedCrossRef Goldstein EJ, Citron DM, Sears P, et al. Comparative susceptibilities to fidaxomicin (OPT-80) of isolates collected at baseline, recurrence, and failure from patients in two phase III trials of fidaxomicin against Clostridium difficile infection. Antimicrob Agents Chemother. 2011;55(11):5194–9.PubMedCrossRef
27.
go back to reference Pillai A, Nelson R. Probiotics for treatment of Clostridium difficile-associated colitis in adults. Cochrane Database Syst Rev. 2008;1:CD004611.PubMed Pillai A, Nelson R. Probiotics for treatment of Clostridium difficile-associated colitis in adults. Cochrane Database Syst Rev. 2008;1:CD004611.PubMed
28.
go back to reference Pozzoni P, Riva A, Bellatorre AG, et al. Saccharomyces boulardii for the prevention of antibiotic-associated diarrhea in adult hospitalized patients: a single-center, randomized, double-blind, placebo-controlled trial. Am J Gastroenterol. 2012;107(6):922–31.PubMedCrossRef Pozzoni P, Riva A, Bellatorre AG, et al. Saccharomyces boulardii for the prevention of antibiotic-associated diarrhea in adult hospitalized patients: a single-center, randomized, double-blind, placebo-controlled trial. Am J Gastroenterol. 2012;107(6):922–31.PubMedCrossRef
29.
go back to reference Guo B, Harstall C, Louie T, et al. Systematic review: faecal transplantation for the treatment of Clostridium difficile-associated disease. Aliment Pharmacol Ther. 2012;35(8):865–75.PubMedCrossRef Guo B, Harstall C, Louie T, et al. Systematic review: faecal transplantation for the treatment of Clostridium difficile-associated disease. Aliment Pharmacol Ther. 2012;35(8):865–75.PubMedCrossRef
30.
go back to reference •• van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368(5):407–15. First randomized controlled trial of fecal microbiota transplantation demonstrating its efficacy for treating recurrent CDI.PubMedCrossRef •• van Nood E, Vrieze A, Nieuwdorp M, et al. Duodenal infusion of donor feces for recurrent Clostridium difficile. N Engl J Med. 2013;368(5):407–15. First randomized controlled trial of fecal microbiota transplantation demonstrating its efficacy for treating recurrent CDI.PubMedCrossRef
31.
go back to reference Postigo R, Kim JH. Colonoscopic versus nasogastric fecal transplantation for the treatment of Clostridium difficile infection: a review and pooled analysis. Infection. 2012;40(6):643–8.PubMedCrossRef Postigo R, Kim JH. Colonoscopic versus nasogastric fecal transplantation for the treatment of Clostridium difficile infection: a review and pooled analysis. Infection. 2012;40(6):643–8.PubMedCrossRef
33.
go back to reference ••Lowy I, Molrine DC, Leav BA, et al. Treatment with monoclonal antibodies against Clostridium difficile toxins. N Engl J Med. 2010;362(3):197–205. Randomized control trial demonstrating the efficacy of monoclonal antibodies against C. difficile toxins as an adjunct to antimicrobial agents for reducing recurrence.PubMedCrossRef ••Lowy I, Molrine DC, Leav BA, et al. Treatment with monoclonal antibodies against Clostridium difficile toxins. N Engl J Med. 2010;362(3):197–205. Randomized control trial demonstrating the efficacy of monoclonal antibodies against C. difficile toxins as an adjunct to antimicrobial agents for reducing recurrence.PubMedCrossRef
34.
go back to reference Mastroianni A, Coronado O, Nanetti A, et al. Nosocomial Clostridium difficile-associated diarrhea in patients with AIDS: a three-year survey and review. Clin Infect Dis. 1997;25 Suppl 2:S204–5.PubMedCrossRef Mastroianni A, Coronado O, Nanetti A, et al. Nosocomial Clostridium difficile-associated diarrhea in patients with AIDS: a three-year survey and review. Clin Infect Dis. 1997;25 Suppl 2:S204–5.PubMedCrossRef
35.
go back to reference Zulu I, Kelly P, Mwansa J, et al. Contrasting incidence of Clostridium difficile and other enteropathogens in AIDS patients in London and Lusaka. Trans R Soc Trop Med Hyg. 2000;94(2):167–8.PubMedCrossRef Zulu I, Kelly P, Mwansa J, et al. Contrasting incidence of Clostridium difficile and other enteropathogens in AIDS patients in London and Lusaka. Trans R Soc Trop Med Hyg. 2000;94(2):167–8.PubMedCrossRef
36.
go back to reference Mathewson JJ, Salameh BM, DuPont HL, et al. HEp-2 cell-adherent Escherichia coli and intestinal secretory immune response to human immunodeficiency virus (HIV) in outpatients with HIV-associated diarrhea. Clin Diagn Lab Immunol. 1998;5(1):87–90.PubMed Mathewson JJ, Salameh BM, DuPont HL, et al. HEp-2 cell-adherent Escherichia coli and intestinal secretory immune response to human immunodeficiency virus (HIV) in outpatients with HIV-associated diarrhea. Clin Diagn Lab Immunol. 1998;5(1):87–90.PubMed
37.
go back to reference Anastasi JK, Capili B. HIV and diarrhea in the era of HAART: 1998 New York State hospitalizations. Am J Infect Control. 2000;28(3):262–6.PubMedCrossRef Anastasi JK, Capili B. HIV and diarrhea in the era of HAART: 1998 New York State hospitalizations. Am J Infect Control. 2000;28(3):262–6.PubMedCrossRef
38.
go back to reference Sanchez TH, Brooks JT, Sullivan PS, et al. Bacterial diarrhea in persons with HIV infection, United States, 1992–2002. Clin Infect Dis. 2005;41(11):1621–7.PubMedCrossRef Sanchez TH, Brooks JT, Sullivan PS, et al. Bacterial diarrhea in persons with HIV infection, United States, 1992–2002. Clin Infect Dis. 2005;41(11):1621–7.PubMedCrossRef
39.
go back to reference Pulvirenti J, Mehra T, Hafiz I, et al. Epidemiology and outcome of Clostridium difficile infection and diarrhea in HIV infected inpatients. Diagn Microbiol Infect Dis. 2002;44(4):325–30.PubMedCrossRef Pulvirenti J, Mehra T, Hafiz I, et al. Epidemiology and outcome of Clostridium difficile infection and diarrhea in HIV infected inpatients. Diagn Microbiol Infect Dis. 2002;44(4):325–30.PubMedCrossRef
40.
go back to reference Gordon MA, Kankwatira AM, Mwafulirwa G, et al. Invasive non-typhoid salmonellae establish systemic intracellular infection in HIV-infected adults: an emerging disease pathogenesis. Clin Infect Dis. 2010;50(7):953–62.PubMedCrossRef Gordon MA, Kankwatira AM, Mwafulirwa G, et al. Invasive non-typhoid salmonellae establish systemic intracellular infection in HIV-infected adults: an emerging disease pathogenesis. Clin Infect Dis. 2010;50(7):953–62.PubMedCrossRef
41.
go back to reference Larsen IK, Gradel KO, Helms M, et al. Non-typhoidal Salmonella and Campylobacter infections among HIV-positive patients in Denmark. Scand J Infect Dis. 2011;43(1):3–7.PubMedCrossRef Larsen IK, Gradel KO, Helms M, et al. Non-typhoidal Salmonella and Campylobacter infections among HIV-positive patients in Denmark. Scand J Infect Dis. 2011;43(1):3–7.PubMedCrossRef
42.
go back to reference Barbut F, Meynard JL, Guiguet M, et al. Clostridium difficile-associated diarrhea in HIV-infected patients: epidemiology and risk factors. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;16(3):176–81.PubMedCrossRef Barbut F, Meynard JL, Guiguet M, et al. Clostridium difficile-associated diarrhea in HIV-infected patients: epidemiology and risk factors. J Acquir Immune Defic Syndr Hum Retrovirol. 1997;16(3):176–81.PubMedCrossRef
43.
go back to reference Hutin Y, Molina JM, Casin I, et al. Risk factors for Clostridium difficile-associated diarrhoea in HIV-infected patients. AIDS. 1993;7(11):1441–7.PubMedCrossRef Hutin Y, Molina JM, Casin I, et al. Risk factors for Clostridium difficile-associated diarrhoea in HIV-infected patients. AIDS. 1993;7(11):1441–7.PubMedCrossRef
44.
go back to reference Tumbarello M, Tacconelli E, Leone F, et al. Clostridium difficile-associated diarrhoea in patients with human immunodeficiency virus infection: a case–control study. Eur J Gastroenterol Hepatol. 1995;7(3):259–63.PubMed Tumbarello M, Tacconelli E, Leone F, et al. Clostridium difficile-associated diarrhoea in patients with human immunodeficiency virus infection: a case–control study. Eur J Gastroenterol Hepatol. 1995;7(3):259–63.PubMed
45.
go back to reference Bouza E, Padilla B, Catalan P, et al. Diarrhea associated with Clostridium difficile: one-year experience in a general hospital. Rev Clin Esp. 1996;196(7):424–30.PubMed Bouza E, Padilla B, Catalan P, et al. Diarrhea associated with Clostridium difficile: one-year experience in a general hospital. Rev Clin Esp. 1996;196(7):424–30.PubMed
46.
go back to reference Dallal RM, Harbrecht BG, Boujoukas AJ, et al. Fulminant Clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg. 2002;235(3):363–72.PubMedCrossRef Dallal RM, Harbrecht BG, Boujoukas AJ, et al. Fulminant Clostridium difficile: an underappreciated and increasing cause of death and complications. Ann Surg. 2002;235(3):363–72.PubMedCrossRef
47.
go back to reference Mody LR, Smith SM, Dever LL. Clostridium difficile-associated diarrhea in a VA medical center: clustering of cases, association with antibiotic usage, and impact on HIV-infected patients. Infect Control Hosp Epidemiol. 2001;22(1):42–5.PubMedCrossRef Mody LR, Smith SM, Dever LL. Clostridium difficile-associated diarrhea in a VA medical center: clustering of cases, association with antibiotic usage, and impact on HIV-infected patients. Infect Control Hosp Epidemiol. 2001;22(1):42–5.PubMedCrossRef
48.
go back to reference Buchner AM, Sonnenberg A. Medical diagnoses and procedures associated with clostridium difficile colitis. Am J Gastroenterol. 2001;96(3):766–72.PubMedCrossRef Buchner AM, Sonnenberg A. Medical diagnoses and procedures associated with clostridium difficile colitis. Am J Gastroenterol. 2001;96(3):766–72.PubMedCrossRef
49.
go back to reference Saddi VR, Glatt AE. Clostridium difficile-associated diarrhea in patients with HIV: a 4-year survey. J Acquir Immune Defic Syndr. 2002;31(5):542–3.PubMedCrossRef Saddi VR, Glatt AE. Clostridium difficile-associated diarrhea in patients with HIV: a 4-year survey. J Acquir Immune Defic Syndr. 2002;31(5):542–3.PubMedCrossRef
50.
go back to reference Sherer R, Pulvirenti J, Stieglitz K, et al. Hospitalization in HIV in Chicago. J Int Assoc Physicians AIDS Care (Chic). 2002;1(1):26–33.CrossRef Sherer R, Pulvirenti J, Stieglitz K, et al. Hospitalization in HIV in Chicago. J Int Assoc Physicians AIDS Care (Chic). 2002;1(1):26–33.CrossRef
51.
go back to reference Palella Jr FJ, Chmiel JS, Moorman AC, et al. Durability and predictors of success of highly active antiretroviral therapy for ambulatory HIV-infected patients. AIDS. 2002;16(12):1617–26.CrossRef Palella Jr FJ, Chmiel JS, Moorman AC, et al. Durability and predictors of success of highly active antiretroviral therapy for ambulatory HIV-infected patients. AIDS. 2002;16(12):1617–26.CrossRef
52.
go back to reference Pavie J, Menotti J, Porcher R, et al. Prevalence of opportunistic intestinal parasitic infections among HIV-infected patients with low CD4 cells counts in France in the combination antiretroviral therapy era. Int J Infect Dis. 2012;16(9):e677–9.PubMedCrossRef Pavie J, Menotti J, Porcher R, et al. Prevalence of opportunistic intestinal parasitic infections among HIV-infected patients with low CD4 cells counts in France in the combination antiretroviral therapy era. Int J Infect Dis. 2012;16(9):e677–9.PubMedCrossRef
53.
go back to reference Samie A, Obi CL, Franasiak J, et al. PCR detection of Clostridium difficile triose phosphate isomerase (tpi), toxin A (tcdA), toxin B (tcdB), binary toxin (cdtA, cdtB), and tcdC genes in Vhembe District, South Africa. AmJTrop Med Hyg. 2008;78(4):577–85. Samie A, Obi CL, Franasiak J, et al. PCR detection of Clostridium difficile triose phosphate isomerase (tpi), toxin A (tcdA), toxin B (tcdB), binary toxin (cdtA, cdtB), and tcdC genes in Vhembe District, South Africa. AmJTrop Med Hyg. 2008;78(4):577–85.
54.
go back to reference Willingham FF, Ticona Chavez E, Taylor DN, et al. Diarrhea and Clostridium difficile infection in Latin American patients with AIDS. Working Group on AIDS in Peru. Clin Infect Dis. 1998;27(3):487–93.PubMedCrossRef Willingham FF, Ticona Chavez E, Taylor DN, et al. Diarrhea and Clostridium difficile infection in Latin American patients with AIDS. Working Group on AIDS in Peru. Clin Infect Dis. 1998;27(3):487–93.PubMedCrossRef
55.
go back to reference Onwueme K, Fadairo Y, Idoko L, et al. High prevalence of toxinogenic Clostridium difficile in Nigerian adult HIV patients. Trans R Soc Trop Med Hyg. 2011;105(11):667–9.PubMedCrossRef Onwueme K, Fadairo Y, Idoko L, et al. High prevalence of toxinogenic Clostridium difficile in Nigerian adult HIV patients. Trans R Soc Trop Med Hyg. 2011;105(11):667–9.PubMedCrossRef
56.
go back to reference Jha AK, Uppal B, Chadha S, et al. Clinical and Microbiological Profile of HIV/AIDS Cases with Diarrhea in North India. J Pathog. 2012;2012:971958.PubMed Jha AK, Uppal B, Chadha S, et al. Clinical and Microbiological Profile of HIV/AIDS Cases with Diarrhea in North India. J Pathog. 2012;2012:971958.PubMed
57.
go back to reference Cappell MS, Philogene C. Clostridium difficile infection is a treatable cause of diarrhea in patients with advanced human immunodeficiency virus infection: a study of seven consecutive patients admitted from 1986 to 1992 to a university teaching hospital. Am J Gastroenterol. 1993;88(6):891–7.PubMed Cappell MS, Philogene C. Clostridium difficile infection is a treatable cause of diarrhea in patients with advanced human immunodeficiency virus infection: a study of seven consecutive patients admitted from 1986 to 1992 to a university teaching hospital. Am J Gastroenterol. 1993;88(6):891–7.PubMed
58.
go back to reference Lu SS, Schwartz JM, Simon DM, et al. Clostridium difficile-associated diarrhea in patients with HIV positivity and AIDS: a prospective controlled study. Am J Gastroenterol. 1994;89(8):1226–9.PubMed Lu SS, Schwartz JM, Simon DM, et al. Clostridium difficile-associated diarrhea in patients with HIV positivity and AIDS: a prospective controlled study. Am J Gastroenterol. 1994;89(8):1226–9.PubMed
59.
go back to reference Zuckerman E, Kanel G, Ha C, et al. Low albumin gradient ascites complicating severe pseudomembranous colitis. Gastroenterology. 1997;112(3):991–4.PubMedCrossRef Zuckerman E, Kanel G, Ha C, et al. Low albumin gradient ascites complicating severe pseudomembranous colitis. Gastroenterology. 1997;112(3):991–4.PubMedCrossRef
60.
go back to reference Beaugerie L, Ngo Y, Goujard F, et al. Etiology and management of toxic megacolon in patients with human immunodeficiency virus infection. Gastroenterology. 1994;107(3):858–63.PubMedCrossRef Beaugerie L, Ngo Y, Goujard F, et al. Etiology and management of toxic megacolon in patients with human immunodeficiency virus infection. Gastroenterology. 1994;107(3):858–63.PubMedCrossRef
61.
go back to reference DeMarais PL, Gertzen J, Weinstein RA. Nosocomial infections in human immunodeficiency virus-infected patients in a long-term-care setting. Clin Infect Dis. 1997;25(5):1230–2.PubMedCrossRef DeMarais PL, Gertzen J, Weinstein RA. Nosocomial infections in human immunodeficiency virus-infected patients in a long-term-care setting. Clin Infect Dis. 1997;25(5):1230–2.PubMedCrossRef
62.
go back to reference Olofinlade O, Chiang C. Cytomegalovirus infection as a cause of pseudomembrane colitis: a report of four cases. J Clin Gastroenterol. 2001;32(1):82–4.PubMedCrossRef Olofinlade O, Chiang C. Cytomegalovirus infection as a cause of pseudomembrane colitis: a report of four cases. J Clin Gastroenterol. 2001;32(1):82–4.PubMedCrossRef
63.
go back to reference Younus F, Steigbigel RT. Images in clinical medicine. Nodular Clostridium difficile colitis. N Engl J Med. 2004;350(10):e9.PubMedCrossRef Younus F, Steigbigel RT. Images in clinical medicine. Nodular Clostridium difficile colitis. N Engl J Med. 2004;350(10):e9.PubMedCrossRef
64.
go back to reference Cozart JC, Kalangi SS, Clench MH, et al. Clostridium difficile diarrhea in patients with AIDS versus non-AIDS controls. Methods of treatment and clinical response to treatment. J Clin Gastroenterol. 1993;16(3):192–4.PubMedCrossRef Cozart JC, Kalangi SS, Clench MH, et al. Clostridium difficile diarrhea in patients with AIDS versus non-AIDS controls. Methods of treatment and clinical response to treatment. J Clin Gastroenterol. 1993;16(3):192–4.PubMedCrossRef
65.
go back to reference Pepin J, Valiquette L, Gagnon S, et al. Outcomes of Clostridium difficile-associated disease treated with metronidazole or vancomycin before and after the emergence of NAP1/027. Am J Gastroenterol. 2007;102(12):2781–8.PubMedCrossRef Pepin J, Valiquette L, Gagnon S, et al. Outcomes of Clostridium difficile-associated disease treated with metronidazole or vancomycin before and after the emergence of NAP1/027. Am J Gastroenterol. 2007;102(12):2781–8.PubMedCrossRef
66.
go back to reference Alonso R, Gros S, Pelaez T, et al. Molecular analysis of relapse vs re-infection in HIV-positive patients suffering from recurrent Clostridium difficile associated diarrhoea. J Hosp Infect. 2001;48(2):86–92.PubMedCrossRef Alonso R, Gros S, Pelaez T, et al. Molecular analysis of relapse vs re-infection in HIV-positive patients suffering from recurrent Clostridium difficile associated diarrhoea. J Hosp Infect. 2001;48(2):86–92.PubMedCrossRef
67.
go back to reference Ricciardi R, Rothenberger DA, Madoff RD, et al. Increasing prevalence and severity of Clostridium difficile colitis in hospitalized patients in the United States. Arch Surg. 2007;142(7):624–31. discussion 31.PubMedCrossRef Ricciardi R, Rothenberger DA, Madoff RD, et al. Increasing prevalence and severity of Clostridium difficile colitis in hospitalized patients in the United States. Arch Surg. 2007;142(7):624–31. discussion 31.PubMedCrossRef
68.
go back to reference • Saxena D, Li Y, Yang L, et al. Human microbiome and HIV/AIDS. Curr HIV/AIDS Rep. 2012;9(1):44–51. Review article summarizing what is known about the effect of HIV on the microbiome.PubMedCrossRef • Saxena D, Li Y, Yang L, et al. Human microbiome and HIV/AIDS. Curr HIV/AIDS Rep. 2012;9(1):44–51. Review article summarizing what is known about the effect of HIV on the microbiome.PubMedCrossRef
69.
go back to reference Qiao X, He B, Chiu A, et al. Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat Immunol. 2006;7(3):302–10.PubMedCrossRef Qiao X, He B, Chiu A, et al. Human immunodeficiency virus 1 Nef suppresses CD40-dependent immunoglobulin class switching in bystander B cells. Nat Immunol. 2006;7(3):302–10.PubMedCrossRef
70.
go back to reference Sullivan A, Edlund C, Nord CE. Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect Dis. 2001;1(2):101–14.PubMedCrossRef Sullivan A, Edlund C, Nord CE. Effect of antimicrobial agents on the ecological balance of human microflora. Lancet Infect Dis. 2001;1(2):101–14.PubMedCrossRef
71.
go back to reference Tvede M, Rask-Madsen J. Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients. Lancet. 1989;1(8648):1156–60.PubMedCrossRef Tvede M, Rask-Madsen J. Bacteriotherapy for chronic relapsing Clostridium difficile diarrhoea in six patients. Lancet. 1989;1(8648):1156–60.PubMedCrossRef
72.
go back to reference Gori A, Tincati C, Rizzardini G, et al. Early impairment of gut function and gut flora supporting a role for alteration of gastrointestinal mucosa in human immunodeficiency virus pathogenesis. J Clin Microbiol. 2008;46(2):757–8.PubMedCrossRef Gori A, Tincati C, Rizzardini G, et al. Early impairment of gut function and gut flora supporting a role for alteration of gastrointestinal mucosa in human immunodeficiency virus pathogenesis. J Clin Microbiol. 2008;46(2):757–8.PubMedCrossRef
73.
go back to reference Ellis CL, Ma ZM, Mann SK, et al. Molecular characterization of stool microbiota in HIV-infected subjects by panbacterial and order-level 16S ribosomal DNA (rDNA) quantification and correlations with immune activation. J Acquir Immune Defic Syndr. 2011;57(5):363–70.PubMedCrossRef Ellis CL, Ma ZM, Mann SK, et al. Molecular characterization of stool microbiota in HIV-infected subjects by panbacterial and order-level 16S ribosomal DNA (rDNA) quantification and correlations with immune activation. J Acquir Immune Defic Syndr. 2011;57(5):363–70.PubMedCrossRef
75.
go back to reference Mainardi JL, Lacassin F, Guilloy Y, et al. Low rate of Clostridium difficile colonization in ambulatory and hospitalized HIV-infected patients in a hospital unit: a prospective survey. J Infect. 1998;37(2):108–11.PubMedCrossRef Mainardi JL, Lacassin F, Guilloy Y, et al. Low rate of Clostridium difficile colonization in ambulatory and hospitalized HIV-infected patients in a hospital unit: a prospective survey. J Infect. 1998;37(2):108–11.PubMedCrossRef
76.
go back to reference Hutin Y, Casin I, Lesprit P, et al. Prevalence of and risk factors for Clostridium difficile colonization at admission to an infectious diseases ward. Clin Infect Dis. 1997;24(5):920–4.PubMedCrossRef Hutin Y, Casin I, Lesprit P, et al. Prevalence of and risk factors for Clostridium difficile colonization at admission to an infectious diseases ward. Clin Infect Dis. 1997;24(5):920–4.PubMedCrossRef
77.
go back to reference Poxton IR, McCoubrey J, Blair G. The pathogenicity of Clostridium difficile. Clin Microbiol Infect. 2001;7(8):421–7.PubMedCrossRef Poxton IR, McCoubrey J, Blair G. The pathogenicity of Clostridium difficile. Clin Microbiol Infect. 2001;7(8):421–7.PubMedCrossRef
78.
go back to reference Epple HJ, Zeitz M. HIV infection and the intestinal mucosal barrier. Ann N Y Acad Sci. 2012;1258:19–24.PubMedCrossRef Epple HJ, Zeitz M. HIV infection and the intestinal mucosal barrier. Ann N Y Acad Sci. 2012;1258:19–24.PubMedCrossRef
79.
go back to reference Varin A, Manna SK, Quivy V, et al. Exogenous Nef protein activates NF-kappa B, AP-1, and c-Jun N-terminal kinase and stimulates HIV transcription in promonocytic cells. Role in AIDS pathogenesis. J Biol Chem. 2003;278(4):2219–27.PubMedCrossRef Varin A, Manna SK, Quivy V, et al. Exogenous Nef protein activates NF-kappa B, AP-1, and c-Jun N-terminal kinase and stimulates HIV transcription in promonocytic cells. Role in AIDS pathogenesis. J Biol Chem. 2003;278(4):2219–27.PubMedCrossRef
80.
go back to reference Vilhardt F, Plastre O, Sawada M, et al. The HIV-1 Nef protein and phagocyte NADPH oxidase activation. J Biol Chem. 2002;277(44):42136–43.PubMedCrossRef Vilhardt F, Plastre O, Sawada M, et al. The HIV-1 Nef protein and phagocyte NADPH oxidase activation. J Biol Chem. 2002;277(44):42136–43.PubMedCrossRef
81.
go back to reference Viscidi R, Laughon BE, Yolken R, et al. Serum antibody response to toxins A and B of Clostridium difficile. J Infect Dis. 1983;148(1):93–100.PubMedCrossRef Viscidi R, Laughon BE, Yolken R, et al. Serum antibody response to toxins A and B of Clostridium difficile. J Infect Dis. 1983;148(1):93–100.PubMedCrossRef
82.
go back to reference Kyne L, Warny M, Qamar A, et al. Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N Engl J Med. 2000;342(6):390–7.PubMedCrossRef Kyne L, Warny M, Qamar A, et al. Asymptomatic carriage of Clostridium difficile and serum levels of IgG antibody against toxin A. N Engl J Med. 2000;342(6):390–7.PubMedCrossRef
83.
go back to reference Moir S, Malaspina A, Ogwaro KM, et al. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc Natl Acad Sci USA. 2001;98(18):10362–7.PubMedCrossRef Moir S, Malaspina A, Ogwaro KM, et al. HIV-1 induces phenotypic and functional perturbations of B cells in chronically infected individuals. Proc Natl Acad Sci USA. 2001;98(18):10362–7.PubMedCrossRef
84.
go back to reference Ryan A, Lynch M, Smith SM, et al. A Role for TLR4 in Clostridium difficile Infection and the Recognition of Surface Layer Proteins. PLoS Pathog. 2011;7(6):e1002076.PubMedCrossRef Ryan A, Lynch M, Smith SM, et al. A Role for TLR4 in Clostridium difficile Infection and the Recognition of Surface Layer Proteins. PLoS Pathog. 2011;7(6):e1002076.PubMedCrossRef
85.
go back to reference Modi N, Gulati N, Solomon K, et al. Differential binding and internalization of Clostridium difficile toxin A by human peripheral blood monocytes, neutrophils and lymphocytes. Scand J Immunol. 2011;74(3):264–71. Modi N, Gulati N, Solomon K, et al. Differential binding and internalization of Clostridium difficile toxin A by human peripheral blood monocytes, neutrophils and lymphocytes. Scand J Immunol. 2011;74(3):264–71.
86.
go back to reference Mahida YR, Galvin A, Makh S, et al. Effect of Clostridium difficile toxin A on human colonic lamina propria cells: early loss of macrophages followed by T-cell apoptosis. Infect Immun. 1998;66(11):5462–9.PubMed Mahida YR, Galvin A, Makh S, et al. Effect of Clostridium difficile toxin A on human colonic lamina propria cells: early loss of macrophages followed by T-cell apoptosis. Infect Immun. 1998;66(11):5462–9.PubMed
87.
go back to reference Dockrell DH. The multiple roles of Fas ligand in the pathogenesis of infectious diseases. Clin Microbiol Infect. 2003;9(8):766–79.PubMedCrossRef Dockrell DH. The multiple roles of Fas ligand in the pathogenesis of infectious diseases. Clin Microbiol Infect. 2003;9(8):766–79.PubMedCrossRef
88.
go back to reference Hensgens MP, Goorhuis A, Dekkers OM, et al. Time interval of increased risk for Clostridium difficile infection after exposure to antibiotics. J Antimicrob Chemother. 2012;67(3):742–8.PubMedCrossRef Hensgens MP, Goorhuis A, Dekkers OM, et al. Time interval of increased risk for Clostridium difficile infection after exposure to antibiotics. J Antimicrob Chemother. 2012;67(3):742–8.PubMedCrossRef
89.
go back to reference Dockrell DH, Edwards S, Fisher M, et al. Evolving controversies and challenges in the management of opportunistic infections in HIV-seropositive individuals. J Infect. 2011;63(3):177–86.PubMedCrossRef Dockrell DH, Edwards S, Fisher M, et al. Evolving controversies and challenges in the management of opportunistic infections in HIV-seropositive individuals. J Infect. 2011;63(3):177–86.PubMedCrossRef
90.
go back to reference Spencer RC. The role of antimicrobial agents in the aetiology of Clostridium difficile-associated disease. J Antimicrob Chemother. 1998;41(Suppl C):21–7.PubMedCrossRef Spencer RC. The role of antimicrobial agents in the aetiology of Clostridium difficile-associated disease. J Antimicrob Chemother. 1998;41(Suppl C):21–7.PubMedCrossRef
91.
go back to reference Reiss P. HIV, co-morbidity and ageing. J Int AIDS Soc. 2012;15 Suppl 4:18073. Reiss P. HIV, co-morbidity and ageing. J Int AIDS Soc. 2012;15 Suppl 4:18073.
92.
go back to reference Terhes G, Urban E, Soki J, et al. Community-acquired Clostridium difficile diarrhea caused by binary toxin, toxin A, and toxin B gene-positive isolates in Hungary. J Clin Microbiol. 2004;42(9):4316–8.PubMedCrossRef Terhes G, Urban E, Soki J, et al. Community-acquired Clostridium difficile diarrhea caused by binary toxin, toxin A, and toxin B gene-positive isolates in Hungary. J Clin Microbiol. 2004;42(9):4316–8.PubMedCrossRef
94.
go back to reference Bakken JS, Borody T, Brandt LJ, et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol. 2011;9(12):1044–9.PubMedCrossRef Bakken JS, Borody T, Brandt LJ, et al. Treating Clostridium difficile infection with fecal microbiota transplantation. Clin Gastroenterol Hepatol. 2011;9(12):1044–9.PubMedCrossRef
95.
go back to reference Zainah H, Silverman A. Fecal bacteriotherapy: a case report in an immunosuppressed patient with ulcerative colitis and recurrent clostridium difficile infection. Case Rep Infect Dis. 2012;2012:810943.PubMed Zainah H, Silverman A. Fecal bacteriotherapy: a case report in an immunosuppressed patient with ulcerative colitis and recurrent clostridium difficile infection. Case Rep Infect Dis. 2012;2012:810943.PubMed
96.
go back to reference Neemann K, Eichele DD, Smith PW, et al. Fecal microbiota transplantation for fulminant Clostridium difficile infection in an allogeneic stem cell transplant patient. Transpl Infect Dis. 2012;14(6):E161–5.PubMedCrossRef Neemann K, Eichele DD, Smith PW, et al. Fecal microbiota transplantation for fulminant Clostridium difficile infection in an allogeneic stem cell transplant patient. Transpl Infect Dis. 2012;14(6):E161–5.PubMedCrossRef
97.
go back to reference Hoffmann C, Schmid H, Muller M, et al. Improved outcome with rituximab in patients with HIV-associated multicentric Castleman disease. Blood. 2011;118(13):3499–503.PubMedCrossRef Hoffmann C, Schmid H, Muller M, et al. Improved outcome with rituximab in patients with HIV-associated multicentric Castleman disease. Blood. 2011;118(13):3499–503.PubMedCrossRef
98.
go back to reference Foglia G, Shah S, Luxemburger C, et al. Clostridium difficile: development of a novel candidate vaccine. Vaccine. 2012;30(29):4307–9.PubMedCrossRef Foglia G, Shah S, Luxemburger C, et al. Clostridium difficile: development of a novel candidate vaccine. Vaccine. 2012;30(29):4307–9.PubMedCrossRef
99.
go back to reference Geretti AM, Brook G, Cameron C, et al. British HIV Association guidelines for immunization of HIV-infected adults 2008. HIV Med. 2008;9(10):795–848.PubMedCrossRef Geretti AM, Brook G, Cameron C, et al. British HIV Association guidelines for immunization of HIV-infected adults 2008. HIV Med. 2008;9(10):795–848.PubMedCrossRef
Metadata
Title
Clostridium Difficile Infection in Patients with HIV/AIDS
Authors
Paul J. Collini
Ed Kuijper
David H. Dockrell
Publication date
01-09-2013
Publisher
Springer US
Published in
Current HIV/AIDS Reports / Issue 3/2013
Print ISSN: 1548-3568
Electronic ISSN: 1548-3576
DOI
https://doi.org/10.1007/s11904-013-0162-z

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