Diseases of the Colon & Rectum

, Volume 41, Issue 11, pp 1435–1449 | Cite as

Clostridium difficile-associated diarrhea and colitis

Clinical manifestations, diagnosis, and treatment
  • Robert K. Cleary
Current Status


PURPOSE: This review examines the pathogenesis, clinical manifestations, diagnosis, and current medical and operative strategies in the treatment ofClostridium difficile diarrhea and colitis. Prevention and future avenues of research are also investigated. METHODS: A review of the literature was conducted with the use of MEDLINE. RESULTS:C. difficile is a gram-positive, spore-forming bacterium capable of causing toxigenic colitis in susceptible patients, usually those receiving antibiotics. Overgrowth of toxigenic strains may result in a spectrum of disease, including becoming an asymptomatic carrier, diarrhea, self-limited colitis, fulminant colitis, and toxic megacolon. Diagnosis requires a high index of suspicion and depends on clinical data, laboratory stool studies (enzyme-linked immunoabsorbent assay and cytotoxin test), and endoscopy in selected cases. Protocols for treatment of primary and relapsing infections are provided in algorithm format. Discontinuation of antibiotics may be enough to resolve symptoms. Medical management with oral metronidazole or vancomycin is the first-line therapy for those with symptomatic colitis. Teicoplanin,Saccharomyces spp. andLactobacillus spp., and intravenous IgG antitoxin are reserved for more recalcitrant cases. Refractory or relapsing infections may require vancomycin given orally or other newer modalities. Fulminant colitis and toxic megacolon warrant subtotal colectomy. Cost, in terms of extended hospital stay, medical and surgical management, and, in some cases, ward closure, is thought to be formidable. Review of perioperative antibiotic policies and analysis of hospital formularies may contribute to prevention and decreased costs. CONCLUSION:C. difficile diarrhea and colitis is a nosocomial infection that may result in significant morbidity, mortality, and medical costs. Standard laboratory studies and endoscopic evaluation assist in the diagnosis of clinically suspicious cases. Appropriate perioperative antibiotic dosing, narrowing the antibiotic spectrum when treating infections, and discontinuing antibiotics at appropriate intervals prevent toxic sequelae.

Key words

Clostridium difficile Antibiotic-associated colitis Pseudomembranous colitis nosocomial infection 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. 1.
    Bartlett JG, Chang TW, Gurwith M, Gorbach SL, Onderdonk AB. Antibiotic associated pseudomembranous colitis due to toxin-producing clostridia. N Engl J Med 1978;298:531–4.PubMedGoogle Scholar
  2. 2.
    Finney JM. Gastroenterostomy for cictratizing ulcer of the pylorus. Bull Johns Hopkins Hosp 1893;4:53–5.Google Scholar
  3. 3.
    Tedesco FJ, Stanley RJ, Alpers DH. Diagnostic features of clindamycin-associated pseudomembranous colins. N Engl J Med 1974;290:841–3.PubMedGoogle Scholar
  4. 4.
    Jobe BA, Grasley A, Deveney KE, Deveney CW, Sheppard BC. Clostridium difficile colitis: an increasing hospital-acquired illness. Am J Surg 1995;169:480–3.CrossRefPubMedGoogle Scholar
  5. 5.
    Altmeier WA, Hummel RP, Hill EO. Staphylococcal enterocolitis following antibiotic therapy. Ann Surg 1963;157:847–58.PubMedGoogle Scholar
  6. 6.
    Marr JJ, Sans MD, Tedesco FJ. Bacterial studies of clindamycin-associated colitis. Gastroenterology 1975;69:352–8.PubMedGoogle Scholar
  7. 7.
    Rolfe RD, Helebian S, Finegold SM. Bacterial interference between Clostridium difficile and normal fecal flora. J Infect Dis 1981;143:470–5.PubMedGoogle Scholar
  8. 8.
    Worden JP. Pharmacotherapy: Management of Clostridium difficile colitis. Curr Surg 1996;53:46–50.Google Scholar
  9. 9.
    Tabaqchali S, Jumaa P. Diagnosis and management of Clostridium difficile infection. BMJ 1995;310:1375–80.PubMedGoogle Scholar
  10. 10.
    Kelly CP, Pothoulakis C, LaMont JT. Clostridium difficile colitis. N Engl J Med 1992;330:257–62.CrossRefGoogle Scholar
  11. 11.
    Bradbury AW, Barrett S. Surgical aspects of Clostridium difficile colitis. Br J Surg 1997;84:150–9.CrossRefPubMedGoogle Scholar
  12. 12.
    Goodman LJ, Harris AA. Clostridium difficile: A review of recent advances in diagnosis, treatment, and prevention. J Nosoc Infect 1985;4:24–8.Google Scholar
  13. 13.
    Kabins SA, Spira TJ. Outbreak of clindamycin-associated colitis. Ann Intern Med 1975;83:830–1.PubMedGoogle Scholar
  14. 14.
    Bartlett JG. Clostridium difficile infection: pathophysiology and diagnosis. Semin Gastrointest Dis 1997;8:12–21.PubMedGoogle Scholar
  15. 15.
    Viscidi R, Willey S, Bartlett JG. Isolation rates and toxigenic potential of Clostridium difficile isolates from various patient populations. Gastroenterology 1981;81:5–9.PubMedGoogle Scholar
  16. 16.
    Larson HE, Barclay FE, Honour P, Hill ID. Epidemiology of Clostridium difficile in infants. J Infect Dis 1982;146:727–33.PubMedGoogle Scholar
  17. 17.
    Marts BC, Longo WE, Vernava AM III, Kennedy DJ, Daniel GL, Jones I. Patterns and prognosis ofClostridium difficile colitis. Dis Colon Rectum 1994;37:837–45.CrossRefPubMedGoogle Scholar
  18. 18.
    Wilcox MH. Cleaning up Clostridium difficile infection. Lancet 1996;348:767–8.CrossRefPubMedGoogle Scholar
  19. 19.
    Anand A, Bashey B, Mir T, Glatt AE. Epidemiology, clinical manifestations, and outcome of Clostridium difficile associated diarrhoea. Am J Gastroenterol 1994;89:519–23.PubMedGoogle Scholar
  20. 20.
    Keighley MR. Antibiotic-associated pseudomembranous colitis: pathogenesis and management. Drugs 1980;20:49–56.PubMedGoogle Scholar
  21. 21.
    Gerding DN, Olson MM, Peterson LR,et al. Clostridium difficile-associated diarrhea and colitis in adults: a prospective case-controlled epidemiologic study. Arch Intern Med 1986;146:95–100.CrossRefPubMedGoogle Scholar
  22. 22.
    Talbot RW, Walker RC, Beart RW Jr. Changing epidemiology, diagnosis, and treatment of Clostridium difficile toxin-associated colitis. Br J Surg 1986;73:3:457–60.PubMedGoogle Scholar
  23. 23.
    Medich DS, Lee KK, Simmons RL, Grubbs PE, Yang HC, Showalter DP. Laparotomy for fulminant pseudomembranous colitis. Arch Surg 1992;127:847–52.PubMedGoogle Scholar
  24. 24.
    McFarland LV, Mulligan ME, Kwok RY, Stamm WE. Nosocomial acquisition of Clostridium difficile infection. N Engl J Med 1989;320:204–10.PubMedGoogle Scholar
  25. 25.
    Fekety R. Guidelines for the diagnosis and management of Clostridium difficile-associated diarrhea and colitis. Am J Gastroenterol 1997;92:739–50.PubMedGoogle Scholar
  26. 26.
    Gerding DN. Is there a relationship between vancomycin-resistant enterococcal infection and Clostridium difficile infection? Clin Infect Dis 1997;25(Suppl 2):206–10.PubMedGoogle Scholar
  27. 27.
    Riley TV, Cooper M, Bell B, Golledge CL. Community-acquired Clostridium difficile-associated diarrhea. Clin Infect Dis 1995;20(Suppl 2):263–5.PubMedGoogle Scholar
  28. 28.
    Gerding DN, Olson MM, Johnson S, Peterson LR, Lee JT Jr. Clostridium difficile diarrhea and colonization regimens after treatment with abdominal infection containing clindamycin or metronidazole. Am J Surg 1990;159:212–7.PubMedGoogle Scholar
  29. 29.
    Chen FC, Woods R. Pseudomembranous panenteritis and septicaemia in a patient with ulcerative colitis. Aust N Z J Surg 1996;66:565–7.PubMedGoogle Scholar
  30. 30.
    Trevisani F, Simoncini M, Alampi G, Bernardi M. Colitis associated to chemotherapy with 5-fluorouracil. Hepatogastroenterology 1997;44:710–2.PubMedGoogle Scholar
  31. 31.
    Yee J, Dixon CM, McLean AP, Meakins JL. Clostridium difficile disease in a department of surgery: the significance of prophylactic antibiotics. Arch Surg 1991;126:241–6.PubMedGoogle Scholar
  32. 32.
    Fekety R, Shah AB. Diagnosis and treatment of Clostridium difficile colitis. JAMA 1993;269:71–5.CrossRefPubMedGoogle Scholar
  33. 33.
    Settle CD. Clostridium difficile. Br J Hosp Med 1996;56:398–400.PubMedGoogle Scholar
  34. 34.
    Rosen L. Antibiotic-associated colitis. Perspect Colon Rectal Surg 1991;4:205–17.Google Scholar
  35. 35.
    Laughon BE, Viscidi RP, Gdovin SL, Yolken RH, Bartlett JG. Enzyme immunoassays for detection of Clostridium difficile toxins A and B in fecal specimens. J Infect Dis 1984;149:781–8.PubMedGoogle Scholar
  36. 36.
    Lipsett PA, Samantaray DK, Tam ML, Bartlett JG, Lillemoe KD. Pseudomembranous colitis; a surgical disease? Surgery 1994;116:491–6.PubMedGoogle Scholar
  37. 37.
    Pothoulakis C. Pathogenesis of Clostridium difficile-associated diarrhea. Eur J Gastroenterol Hepatol 1996;8:1041–47.PubMedGoogle Scholar
  38. 38.
    Trnka YM, Lamont JT. Clostridium difficile colitis. Adv Intern Med 1984;29:85–107.PubMedGoogle Scholar
  39. 39.
    Settle CD, Wilcox MH. Review article: antibiotic-induced Clostridium difficile infection. Aliment Pharmacol Ther 1996;10:835–41.CrossRefPubMedGoogle Scholar
  40. 40.
    Borriello SP, Ketley JM, Mitchell TJ,et al. Clostridium difficile-a spectrum of virulence and analysis of putative virulence determinants in the hamster model of antibiotic-associated colitis. J Med Microbiol 1987;24:53–64.PubMedGoogle Scholar
  41. 41.
    Seddon SV, Hemingway, I, Borriello SP. Hydrolytic enzyme production by Clostridium difficile and its relationship to toxin production and virulence in the hamster model. J Med Microbiol 1990;31:169–74.PubMedGoogle Scholar
  42. 42.
    Dailey DC, Kaiser A, Schloemer RH. Factors influencing the phagocytosis of Clostridium difficile by human polymorphonuclear leukocytes. Infect Immun 1987;55:1541–6.PubMedGoogle Scholar
  43. 43.
    Kelly CP, Becker S, Linevsky JK,et al. Neutrophil recruitment in Clostridium difficile toxin A enteritis in the rabbit. J Clin Invest 1994;93:1257–65.PubMedGoogle Scholar
  44. 44.
    Chatila W, Manthous CA. Clostridium difficile causing sepsis and an acute abdomen in critically ill patients. Crit Care Med 1995;23:1146–50.CrossRefPubMedGoogle Scholar
  45. 45.
    McCarter MD, Abularrage C, Velasco FT, Davis JM, Daly JM. Diarrhea and Clostridium difficile-associated diarrhea on a surgical service. Arch Surg 1996;131:1333–7.PubMedGoogle Scholar
  46. 46.
    McNeeley SG, Jr, Anderson GD, Sibai BM. Clostridium difficile colitis associated with single dose cefazolin prophylaxis. Obstet Gynecol 1985;66:737–38.PubMedGoogle Scholar
  47. 47.
    Kreisel D, Savel TG, Silver AL, Cunningham JD. Surgical antibiotic prophylaxis and Clostridium difficile toxin positivity. Arch Surg 1995;130:989–93.PubMedGoogle Scholar
  48. 48.
    Tedesco FJ. Pseudomembranous colitis: pathogenesis and therapy. Med Clin North Am 1982;66:655–64.PubMedGoogle Scholar
  49. 49.
    Triadafilopoulos G, Hallstone AE. Acute abdomen as the first presentation of pseudomembranous colitis. Gastroenterology 1991;101:685–91.PubMedGoogle Scholar
  50. 50.
    Burke GW, Wilson ME, Mehrez IO. Absence of diarrhea in toxic megacolon complicating Clostridium difficile pseudomembranous colitis. Am J Gastroenterol 1988;83:304–7.PubMedGoogle Scholar
  51. 51.
    Biddle WL, Harms JL, Greenberger NJ, Miner PR Jr. Evaluation of antibiotic-associated diarrhea with a latex agglutination test and cell culture cytotoxicity assay for Clostridium difficile. Am J Gastroenterol 1989;84:379–82.PubMedGoogle Scholar
  52. 52.
    Gerding DN. Diagnosis of Clostridium-difficile-associated disease: patient selection and test perfection. Am J Med 1996;100:485–6.CrossRefPubMedGoogle Scholar
  53. 53.
    Arzese A, Trani G, Riul L, Botta GA. Rapid polymerase chain reaction method for specific detection of toxigenic Clostridium difficile. Eur J Clin Microbiol Infect Dis 1995;14:716–9.CrossRefPubMedGoogle Scholar
  54. 54.
    Bartlett JG. Clostridium difficile: clinical considerations. Rev Infect Dis 1990;12(Suppl 2)43–51.Google Scholar
  55. 55.
    Morris JB, Zollinger RM Jr, Stellato TA. Role of surgery in antibiotic-induced pseudomembranous enterocolitis. Am J Surg 1990;160:535–9.PubMedGoogle Scholar
  56. 56.
    Church JM, Fazio VW. A role for colonic stasis in the pathogenesis of disease related toClostridium difficile. Dis Colon Rectum 1986;29:804–9.PubMedGoogle Scholar
  57. 57.
    Seppala K, Hjelt L, Sipponen P. Colonoscopy in the diagnosis of antibiotic-associated colitis: a prospective study. Scand J Gastroenterol 1981;16:465–8.PubMedGoogle Scholar
  58. 58.
    Gerding DN, Brazier JS. Optimal methods for identifying Clostridium difficile infections. Clin Infect Dis 1993;16(Suppl 4):439–42.PubMedGoogle Scholar
  59. 59.
    Counihan TC, Roberts PL. Pseudomembranous colitis. Surg Clin North Am 1993;73:1063–74.PubMedGoogle Scholar
  60. 60.
    Dignan CR, Greenson JK. Can ischemic colitis be differentiated from C difficile colitis in biopsy specimens? Am J Surg Pathol 1997;21:706–10.CrossRefPubMedGoogle Scholar
  61. 61.
    Ros PR, Buetow PC, Pantograg-Brown L, Forsmark CE, Sobin LH. Pseudomembranous colitis. Radiology 1996;198:1–9.PubMedGoogle Scholar
  62. 62.
    Fishman EK, Kavuru M, Jones B,et al. Pseudomembranous colitis: CT evaluation of 26 cases. Radiology 1991;180:57–60.PubMedGoogle Scholar
  63. 63.
    Cleary RK, Grossmann R, Fernandez FB,et al. Metronidazole may inhibit intestinal colonization withClostridium difficile. Dis Colon Rectum 1998;41:464–7.CrossRefPubMedGoogle Scholar
  64. 64.
    Johnson S, Homann SR, Bettin KM,et al. Treatment of asymptomatic Clostridium difficile carriers (fecal excretors) with vancomycin or metronidazole: a randomized, placebo-controlled trial. Ann Intern Med 1992;117:297–302.PubMedGoogle Scholar
  65. 65.
    Pashby NL, Bolton RP, Sherriff RJ. Oral metronidazole in Clostridium difficile colitis. BMJ 1979;1:1605–6.PubMedGoogle Scholar
  66. 66.
    Fekety R, McFarland LV, Surawicz CM, Greenberg RN, Elmer GW, Mulligan ME. Recurrent Clostridium difficile diarrhea: characteristics of and risk factors for patients enrolled in a prospective, randomized, double-blinded trial. Clin Infect Dis 1997;24:324–33.PubMedGoogle Scholar
  67. 67.
    Schweitzer MA, Sweiss I, Silver DL, Stellato TA. The clinical spectrum of Clostridium difficile colitis in immunocompromised patients. Am Surg 1996;62:603–8.PubMedGoogle Scholar
  68. 68.
    Kleinfeld DI, Sharpe RJ, Donta ST. Parenteral therapy for antibiotic-associated pseudomembranous colitis [letter]. J Infect Dis 1988;157:389.PubMedGoogle Scholar
  69. 69.
    Freeman CD, Klutman NE, Lamp KC. Metronidazole: a therapeutic review and update. Drugs 1997;54:679–708.PubMedGoogle Scholar
  70. 70.
    Oliva SL, Guglielmo BJ, Jacobs R, Pons VG. Failure of intravenous vancomycin and intravenous metronidazole to prevent or treat antibiotic-associated pseudomembranous colitis. J Infect Dis 1989;159:1154–5.PubMedGoogle Scholar
  71. 71.
    Maggiolo F, Bianchi W, Ohnmeiss H. A new approach to the treatment of pseudomembranous colitis? J Infect Dis 1989;160:170–1.PubMedGoogle Scholar
  72. 72.
    Grundfest-Broniatowski S, Quader M, Alexander F, Walsh RM, Lavery I, Milsom J.Clostridium difficile colitis in the critically ill. Dis Colon Rectum 1996;39:619–23.CrossRefPubMedGoogle Scholar
  73. 73.
    Teasley DG, Gerding DN, Olson MM,et al. Prospective, randomized trial of metronidazoleversus vancomycin for Clostridium difficile-associated diarrhea and colitis. Lancet 1983;2:1043–6.CrossRefPubMedGoogle Scholar
  74. 74.
    Wenisch C, Parschalk B, Hasenhundl M, Hirschl AM, Graninger W. Comparison of vancomycin, teicoplanin, metronidazole, and fusidic acid for the treatment of Clostridium difficile-associated diarrhea. Clin Infect Dis 1996;22:813–8.PubMedGoogle Scholar
  75. 75.
    Fekety R, Silva J, Kauffman C, Buggy B, Deery HG. Treatment of antibiotic-associated Clostridium difficile colitis with oral vancomycin: comparison of two dosage regimens. Am J Med 1989;86:15–9.CrossRefGoogle Scholar
  76. 76.
    Wongwanich S, Kusum M, Phan-Urai R. Antibacterial activity of teicoplanin against Clostridium difficile. Southeast Asian J Trop Med Public Health 1996;27:606–9.PubMedGoogle Scholar
  77. 77.
    Bartlett JG. Clostridium difficile: History of its role as an enteric pathogen and the current state of knowledge about the organism. Clin Infect Dis 1994;18(Suppl 4):265–72.PubMedGoogle Scholar
  78. 78.
    Job ML, Jacobs NF Jr. Drug-induced Clostridium difficile-associated disease. Drug Saf 1997;17:37–46.PubMedGoogle Scholar
  79. 79.
    Young GP, Ward PB, Bayley N,et al. Antibiotic-associated colitis due to Clostridium difficile: doubleblind comparison of vancomycin with bacitracin. Gastroenterology 1985;89:1038–45.PubMedGoogle Scholar
  80. 80.
    Salcedo J, Keates S, Pothoulakis C,et al. Intravenous immunoglobulin therapy for severe Clostridium difficile colitis. Gut 1997;41:366–70.PubMedGoogle Scholar
  81. 81.
    Hassett J, Meyers S, McFarland L, Mulligan ME. Recurrent Clostridium difficile infection in a patient with selective IgG1 deficiency treated with intravenous immune globulin and Saccharomyces boulardii. Clin Infect Dis 1995;20(Suppl 2):266–8.Google Scholar
  82. 82.
    Van Ness MM, Cattau EL Jr. Fulminant colitis complicating antibiotic-associated pseudomembranous colitis: case report and review of the clinical manifestations and treatment. Am J Gastroenterol 1987;82:374–7.PubMedGoogle Scholar
  83. 83.
    Tsutaoka B, Hansen J, Johnson D, Holodniy M. Antibiotic-associated pseudomembranous enteritis due to Clostridium difficile. Clin Infect Dis 1994;18:982–4.PubMedGoogle Scholar
  84. 84.
    Shortland JR, Spencer RC, Williams JL. Pseudomembranous colitis associated with changes in an ileal conduit. J Clin Pathol 1983;36:1184–7.PubMedGoogle Scholar
  85. 85.
    Testore GP, Nardi F, Babudieri S, Giuliano M, DiRosa R, Panichi G. Isolation of Clostridium difficile from human jejunum: identification of a reservoir for disease? J Clin Pathol 1986;39:861–2.PubMedGoogle Scholar
  86. 86.
    Schwan A, Sjolin S, Trottestam U, Aronsson B. Relapsing Clostridium difficile enterocolitis cured by rectal infusion of normal feces. Scand J Infect Dis 1984;16:211–5.PubMedGoogle Scholar
  87. 87.
    McFarland LV, Surawicz CM, Greenberg RN,et al. Prevention of beta-lactam-associated diarrhea by Saccharomyces boulardii compared with placebo. Am J Gastroenterol 1995;90:439–48.PubMedGoogle Scholar
  88. 88.
    Biller JA, Katz AJ, Flores AF, Buie TM, Gorbach SL. Treatment of recurrent Clostridium difficile colitis with Lactobacillus GG. J Pediatr Gastroenterol Nutr 1995;21:224–6.PubMedGoogle Scholar
  89. 89.
    Seal D, Borriello SP, Barclay F, Welch A, Piper M, Bonnycastle M. Treatment of relapsing Clostridium difficile diarrhoea by administration of a non-toxigenic strain. Eur J Clin Microbiol Infect Dis 1987;6:51–3.CrossRefGoogle Scholar
  90. 90.
    Boland GW, Lee MJ, Cats AM, Gaa JA, Saini S, Mueller PR. Antibiotic-induced diarrhea: specificity of abdominal CT for the diagnosis of Clostridium difficile disease. Radiology 1994;191:103–6.PubMedGoogle Scholar
  91. 91.
    Holmes NJ. Clostridium difficile colitis. Curr Surg 1996;53:16–9.Google Scholar
  92. 92.
    Rubin MS, Bodenstein LE, Kent KC. SevereClostridium difficile colitis. Dis Colon Rectum 1995;38:350–4.CrossRefPubMedGoogle Scholar
  93. 93.
    Trudel JL, Deschenes M, Mayrand S, Barkun AN. Toxic megacolon complicating pseudomembranous enterocolitis. Dis Colon Rectum 1995;38:1033–8.CrossRefPubMedGoogle Scholar
  94. 94.
    Drapkin MS, Worthington MG, Chang TW, Razvi SA. Clostridium difficile colitis mimicking acute peritonitis. Arch Surg 1985;120:1321–2.PubMedGoogle Scholar
  95. 95.
    Reihner E, Hellers G, Lindqvist L, Veress B. Pseudomembranous colitis presenting as an acute abdomen. Eur J Surg 1996;162:579–81.PubMedGoogle Scholar
  96. 96.
    Yee HF Jr, Brown RS Jr, Ostroff JW. Fatal Clostridium difficile enteritis after total abdominal colectomy. J Clin Gastroenterol 1996;22:45–7.CrossRefPubMedGoogle Scholar
  97. 97.
    Surawicz C. Clostridium difficile colitis: optimizing a cost-effective approach. Am J Gastroenterol 1996;91:1662–3.PubMedGoogle Scholar
  98. 98.
    Starr JM, Rogers TR, Impallomeni M. Hospital-acquired Clostridium difficile diarrhea and herd immunity. Lancet 1997;349:426–8.CrossRefPubMedGoogle Scholar
  99. 99.
    Manian FA, Meyer L. CDAD rates [letter;comment]. Infect Control Hosp Epidemiol 1995;16:63–5.Google Scholar
  100. 100.
    Kaatz GW, Gitlin SD, Schaberg DR,et al. Acquisition of Clostridium difficile from the hospital environment. Am J Epidemiol 1988;127:1289–94.PubMedGoogle Scholar
  101. 101.
    Silva J Jr, Iezzi C. Clostridium difficile as a nosocomial pathogen. J Hosp Infect 1988;11(Suppl A):378–85.CrossRefPubMedGoogle Scholar
  102. 102.
    Cartmill TD, Panigrahi H, Worsley, MA,et al. Management and control of a large outbreak of diarrhea due to Clostridium difficile. J Hosp Infect 1994;27:1–15.CrossRefPubMedGoogle Scholar
  103. 103.
    Katz DA, Bates DW, Rittenberg E,et al. Predicting Clostridium difficile stool cytotoxin results in hospitalized patients with diarrhea. J Gen Intern Med 1997;12:57–62.CrossRefPubMedGoogle Scholar
  104. 104.
    Larson E, Bobo L, Bennett R,et al. Lack of care giver hand contamination with endemic bacterial pathogens in a nursing home. Am J Infect Control 1992;20:11–5.CrossRefPubMedGoogle Scholar
  105. 105.
    Dodson AP, Borriello SP. Clostridium difficile infection of the gut. J Clin Pathol 1996;49:529–32.PubMedGoogle Scholar
  106. 106.
    Ho M, Yang D, Wyle FA, Mulligan ME. Increased incidence of Clostridium difficile-associated diarrhea following decreased restriction of antibiotic use. Clin Infect Dis 1996;23(Suppl 1):102–6.Google Scholar
  107. 107.
    Naaber P, Lehto E, Salminen S, Mikelsaar M. Inhibition of adhesion of Clostridium difficile to caco-2 cells. FEMS Immunol Med Microbiol 1996;14:205–9.CrossRefPubMedGoogle Scholar
  108. 108.
    Bartlett JG. Management of Clostridium difficile infection and other antibiotic-associated diarrheas. Eur J Gastroenterol Hepatol 1996;8:1054–61.PubMedGoogle Scholar
  109. 109.
    Kelly CP. Immune response to Clostridium difficile infection. Eur J Gastroenterol Hepatol 1996;8:1048–53.PubMedGoogle Scholar
  110. 110.
    Starr JM, Rogers TR, Impallomeni M. Hospital-acquired Clostridium difficile diarrhoea. Lancet 1997;349:1176–7.Google Scholar

Copyright information

© The American Society of Colon and Rectal Surgeons 1998

Authors and Affiliations

  • Robert K. Cleary
    • 1
  1. 1.St. Joseph Mercy HospitalAnn Arbor

Personalised recommendations