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Staphylococcal Enterocolitis: Forgotten but Not Gone?

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Abstract

Purpose

Staphylococcus aureus may cause antibiotic-associated diarrhea and enterocolitis, with or without preceding antibiotic use, in immunocompromised adults or infants, or individuals with predisposing conditions, but there is little appreciation of this condition clinically.

Clinical Disease

The main clinical feature that helps to differentiate staphylococcal enterocolitis (SEC) from Clostridium difficile-associated diarrhea is large-volume, cholera-like diarrhea in the former case. A predominance of gram-positive cocci in clusters on gram stain of stool or biopsy specimens and the isolation of S. aureus as the dominant or sole flora support the diagnosis.

Pathogenesis

The pathogenesis of SEC requires the interaction of staphylococcal enterotoxins, which function as superantigens, with interstitial epithelial lymphocytes and intestinal epithelial cells (IECs).

Management

Most SEC represents recent S. aureus acquisition, so that improved infection prevention practices can reduce disease recurrence. Management should include aggressive fluid management and repletion and oral vancomycin.

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References

  1. Felsen J, Wolarsky W. Epidemic diarrhea of the newborn. Arch Pediatr. 1942;59:495–512.

    Google Scholar 

  2. Kramer IRH. Fatal staphylococcal enteritis developing during streptomycin therapy by mouth. Lancet. 1948;2(6530):646–647.

    Article  CAS  PubMed  Google Scholar 

  3. Altemeier WA, Hummel RP, Hill EO. Staphylococcal enterocolitis following antibiotic therapy. Ann Surg. 1963;157:847–858.

    Article  CAS  PubMed  Google Scholar 

  4. Prohaska JV. Pseudomembranous enterocolitis; the experimental induction of the disease with Staphylococcus aureus and its enterotoxin. AMA Arch Surg. 1959;79:197–206.

    CAS  PubMed  Google Scholar 

  5. [No authors listed]. Antibiotics, staphylococcal enteritis and pseudomembranous enterocolitis. N Engl J Med. 1953;249:37–40.

    Google Scholar 

  6. Langley JM, LeBlanc JC, Hanakowski M, et al. The role of Clostridium difficile and viruses as causes of nosocomial diarrhea in children. Infect Control Hosp Epidemiol. 2002;23:660–664.

    Article  PubMed  Google Scholar 

  7. Cunha BA. Nosocomial diarrhea. Crit Care Clin. 1998;14:329–338.

    Article  CAS  PubMed  Google Scholar 

  8. College of American Pathologists. Microbiology Checklist, rev. 09/27/2007.

  9. Bauer TM, Lalvani A, Fehrenbach J, et al. Derivation and validation of guidelines for stool cultures for enteropathogenic bacteria other than Clostridium difficile in hospitalized adults. JAMA. 2001;285:313–319.

    Article  CAS  PubMed  Google Scholar 

  10. Gutman LT, Idriss ZH, Gehlbach S, et al. Neonatal staphylococcal enterocolitis: association with indwelling feeding catheters and S. aureus colonization. J Pediatr. 1976;88:836–839.

    Article  CAS  PubMed  Google Scholar 

  11. Christie CD, Lynch-Ballard E, Andiman WA. Staphylococcal enterocolitis revisited: cytotoxic properties of Staphylococcus aureus from a neonate with enterocolitis. Pediatr Infect Dis J. 1988;7:791–795.

    CAS  PubMed  Google Scholar 

  12. Masunaga K, Mazaki R, Endo A, et al. Colonic stenosis after severe methicillin-resistant Staphylococcus aureus enterocolitis in a newborn. Pediatr Infect Dis J. 1999;18:169–171.

    Article  CAS  PubMed  Google Scholar 

  13. Hinton NA, Taggart JG, Orr JH. The significance of the isolation of coagulase-positive staphylocci from stool. With special reference to the diagnosis of staphyloccocal enteritis. Am J Clin Pathol. 1960;53:505–510.

    Google Scholar 

  14. Baumgart S, Hall SE, Campos JM, et al. Sepsis with coagulase-negative staphylococci in critically ill newborns. Am J Dis Child. 1983;137(5):461–463.

    CAS  PubMed  Google Scholar 

  15. Noel GJ, Edelson PJ. Staphylococcus epidermidis bacteremia in neonates: Further observations and the occurrence of focal infection. Pediatrics. 1984;74:832–837.

    CAS  PubMed  Google Scholar 

  16. Gruskay JA, Abbasi S, Anday E, et al. Staphylococcus epidermidis-associated enterocolitis. J Pediatr. 1986;109:520–524.

    Article  CAS  PubMed  Google Scholar 

  17. Sáenz de Pipaón Marcos M, Rodríguez Delgado J, Martínez Biarge M, et al. Low mortality in necrotizing enterocolitis associated with coagulase-negative Staphylococcus infection. Pediatr Surg Int. 2008;24:831–835.

    Article  PubMed  Google Scholar 

  18. Mollitt DL, Tepas JJ, Talbert JL. The role of coagulase-negative Staphylococcus in neonatal necrotizing enterocolitis. J Pediatr Surg. 1988;23:60–63.

    Article  CAS  PubMed  Google Scholar 

  19. Mintz AC, Applebaum H. Focal gastrointestinal perforations not associated with necrotizing enterocolitis in very low birth weight neonates. J Pediatr Surg. 1993;28:857–860.

    Article  CAS  PubMed  Google Scholar 

  20. Coates EW, Karlowicz MG, Croitoru DP, et al. Distinctive distribution of pathogens associated with peritonitis in neonates with focal intestinal perforation compared with necrotizing enterocolitis. Pediatrics. 2005;116:e241–e246.

    Article  PubMed  Google Scholar 

  21. Scheifele DW, Bjornson GL, Dyer RA, et al. Delta-like toxin produced by coagulase-negative staphylococci is associated with neonatal necrotizing enterocolitis. Infect Immun. 1987;55:2268–2273.

    CAS  PubMed  Google Scholar 

  22. Overturf GD, Sherman MP, Scheifele DW, et al. Neonatal necrotizing enterocolitis associated with delta toxin-producing methicillin-resistant Staphylococcus aureus. Pediatr Infect Dis J. 1990;9:88–91.

    Article  CAS  PubMed  Google Scholar 

  23. Gemmel CG, Thelestam M. Toxigenicity of clinical isolates of coagulase negative staphylococci towards various animal cells. Acta Pathol Microbiol Scand B. 1981;89:417–421.

    Google Scholar 

  24. Boyce JM, Havill NL. Nosocomial antibiotic-associated diarrhea associated with enterotoxin-producing strains of methicillin-resistant Staphylococcus aureus. Am J Gastroenterol. 2005;100:1828–1834.

    Article  PubMed  Google Scholar 

  25. Rhee KY, Soave R, Maltz C. Methicillin-resistant Staphylococcus aureus as a cause of antibiotic-associated diarrhea. J Clin Gastroenterol. 2004;38:299–300.

    Article  PubMed  Google Scholar 

  26. Batts DH, Silva J, Fekety R. Staphylococcus enterocolitis. In: Fekety R, Nelson JD, Grassi C, eds. Current chemotherapy and infectious diseases, vol. 11. Washington, DC: American Society for Microbiology; 1980:944.

    Google Scholar 

  27. Gruber WC, Pietsch JB. Toxic shock syndrome associated with Staphylococcus aureus enterocolitis. Pediatr Infect Dis J. 1988;7:71–72.

    Article  CAS  PubMed  Google Scholar 

  28. Gravet A, Rondeau M, Harf-Monteil C, et al. Predominant Staphylococcus aureus isolated from antibiotic-associated diarrhea is clinically relevant and produces enterotoxin A and the bicomponent toxin LukE-lukD. J Clin Microbiol. 1999;37:4012–4019.

    CAS  PubMed  Google Scholar 

  29. Yoshida D, Fukunari H, Hojo I, et al. Enterocolitis due to methicillin-resistant Staphylococcus aureus—report of two cases. Bull Tokyo Med Dent Univ. 1992;39:31–34.

    CAS  PubMed  Google Scholar 

  30. Takeuchi K, Tsuzuki Y, Ando T, et al. Clinical studies of enteritis caused by methicillin-resistant Staphylococcus aureus. Eur J Surg. 2001;167:293–296.

    Article  CAS  PubMed  Google Scholar 

  31. Morita H, Tani M, Adachi H, et al. Methicillin-resistant Staphylococcus aureus (MRSA) enteritis associated with prophylactic cephalosporin administration and hypochlorhydria, after subtotal gastrectomy. Am J Gastroenterol. 1991;86:791–792.

    CAS  PubMed  Google Scholar 

  32. McPherson S, Ellis R, Fawzi H, et al. Postoperative methicillin-resistant Staphylococcus aureus enteritis following hysterectomy: a case report and review of the literature. Eur J Gastroenterol Hepatol. 2005;17:1225–1227.

    Article  PubMed  Google Scholar 

  33. Chubachi A, Hashimoto K, Miura AB. Successful treatment of methicillin-resistant Staphylococcus aureus (MRSA) enterocolitis in a neutropenic patient following cytotoxic chemotherapy. Am J Hematol. 1993;43:327.

    Article  CAS  PubMed  Google Scholar 

  34. Kotler DP, Sandkovsky U, Schlievert PM, et al. Toxic shock-like syndrome associated with staphylococcal enterocolitis in an HIV-infected man. Clin Infect Dis. 2007;44:e121–e123.

    Article  PubMed  Google Scholar 

  35. Taylor M, Ajayi F, Almond M. Enterocolitis caused by methicillin-resistant Staphylococcus aureus. Lancet. 1993;342(8874):804.

    Article  CAS  PubMed  Google Scholar 

  36. Schiller B, Chiorazzi N, Farber BF. Methicillin-resistant staphylococcal enterocolitis. Am J Med. 1998;105:164–166.

    Article  CAS  PubMed  Google Scholar 

  37. Flemming K, Ackermann G. Prevalence of enterotoxin producing Staphylococcus aureus in stools of patients with nosocomial diarrhea. Infection. 2007;35:356–358.

    Article  CAS  PubMed  Google Scholar 

  38. Asha NJ, Tompkins D, Wilcox MH. Comparative analysis of prevalence, risk factors, and molecular epidemiology of antibiotic-associated diarrhea due to Clostridium difficile, Clostridium perfringens, and Staphylococcus aureus. J Clin Microbiol. 2006;44:2785–2791.

    Article  CAS  PubMed  Google Scholar 

  39. Froberg MK, Palavecino E, Dykoski R, et al. Staphylococcus aureus and Clostridium difficile cause distinct pseudomembranous intestinal diseases. Clin Infect Dis. 2004;39:747–750.

    Article  PubMed  Google Scholar 

  40. Agwu A, Brady KM, Ross T, et al. Cholera-like diarrhea and shock associated with community-acquired methicillin-resistant Staphylococcus aureus (USA400 clone) pneumonia. Pediatr Infect Dis J. 2007;26:271–273.

    Article  PubMed  Google Scholar 

  41. Lieverse RJ, van Hooft J, Fedder G, et al. Necrotizing enterocolitis in a married couple due to a staphylococcal toxin. Eur J Gastroenterol Hepatol. 2001;13:595–597.

    Article  CAS  PubMed  Google Scholar 

  42. Kelly CP, Pothoulakis C, LaMont JT. Clostridium difficile colitis. N Engl J Med. 1994;330:257–262.

    Article  CAS  PubMed  Google Scholar 

  43. McCormick JK, Yarwood JM, Schlievert PM. Toxic shock syndrome and bacterial superantigens: An update. Ann Rev Microbiol. 2001;55:77–104.

    Article  CAS  Google Scholar 

  44. MacDonald KL, Osterholm MT, Hedberg CW, et al. Toxic shock syndrome. A newly recognized complication of influenza and influenzalike illness. JAMA. 1987;257:1053–1058.

    Article  CAS  PubMed  Google Scholar 

  45. Bohach GA, Fast DJ, Nelson RD, et al. Staphylococcal and streptococcal pyrogenic toxins involved in toxic shock syndrome and related illnesses. Crit Rev Microbiol. 1990;17:251–272.

    Article  CAS  PubMed  Google Scholar 

  46. Han SJ, Jung PM, Kim H, et al. Multiple intestinal ulcerations and perforations secondary to methicillin-resistant Staphylococcus aureus enteritis in infants. J Pediatr Surg. 1999;34:381–386.

    Article  CAS  PubMed  Google Scholar 

  47. Lundeen SJ, Otterson MF, Binion DG, et al. Clostridium difficile enteritis: An early postoperative complication in inflammatory bowel disease patients after colectomy. J Gastrointest Surg. 2007;11(2):138–142.

    Article  PubMed  Google Scholar 

  48. Price AB, Davies DR. Pseudomembranous colitis. J Clin Pathol. 1977;30:1–12.

    Article  CAS  PubMed  Google Scholar 

  49. Okii K, Hiyama E, Takesue Y, et al. Molecular epidemiology of enteritis-causing methicillin-resistant Staphylococcus aureus. J Hosp Infect. 2006;62(1):37–43.

    Article  CAS  PubMed  Google Scholar 

  50. Lindsay JA, Ruzin A, Ross HF, et al. The gene for toxic shock toxin is carried by a family of mobile pathogenicity islands in Staphylococcus aureus. Mol Microbiol. 1998;29:527–543.

    Article  CAS  PubMed  Google Scholar 

  51. Yarwood JM, Schlievert PM. Quorum sensing in Staphylococcus infections. J Clin Invest. 2003;112:1620–1625.

    CAS  PubMed  Google Scholar 

  52. Dinges MM, Orwin PM, Schlievert PM. Exotoxins of Staphylococcus aureus. Clin Microbiol Rev. 2000;13:16–34.

    Article  CAS  PubMed  Google Scholar 

  53. Beery JT, Taylor SL, Schlunz LR, et al. Effects of staphylococcal enterotoxin A on the rat gastrointestinal tract. Infect Immun. 1984;44:234–240.

    CAS  PubMed  Google Scholar 

  54. Hu DL, Suga S, Omoe K, et al. Staphylococcal enterotoxin A modulates intracellular Ca2+ signal pathway in human intestinal epithelial cells. FEBS Lett. 2005;579:4407–4412.

    Article  CAS  PubMed  Google Scholar 

  55. Lionetti P, Spencer J, Breese EJ, et al. Activation of mucosal V beta 3+ T cells and tissue damage in human small intestine by the bacterial superantigen, Staphylococcus aureus enterotoxin B. Eur J Immunol. 1993;23:664–668.

    Article  CAS  PubMed  Google Scholar 

  56. McKay DM, Singh PK. Superantigen activation of immune cells evokes epithelial (T84) transport and barrier abnormalities via IFN-gamma and TNF alpha: Inhibition of increased permeability, but not diminished secretory responses by TGF-beta2. J Immunol. 1997;159:2382–2390.

    CAS  PubMed  Google Scholar 

  57. Li H, Llera A, Malchiodi EL, et al. The structural basis of T cell activation by superantigens. Annu Rev Immunol. 1999;17:435–466.

    Article  CAS  PubMed  Google Scholar 

  58. Li H, Llera A, Tsuchiya D, et al. Three-dimensional structure of the complex between a T cell receptor beta chain and the superantigen staphylococcal enterotoxin B. Immunity. 1998;9:807–816.

    Article  CAS  PubMed  Google Scholar 

  59. Li Y, Li H, Dimasi N, et al. Crystal structure of a superantigen bound to the high-affinity, zinc-dependent site on MHC class II. Immunity. 2001;14:93–104.

    Article  CAS  PubMed  Google Scholar 

  60. Malchiodi EL, Eisenstein E, Fields BA, et al. Superantigen binding to a T cell receptor beta chain of known three-dimensional structure. J Exp Med. 1995;182:1833–1845.

    Article  CAS  PubMed  Google Scholar 

  61. Marrack P, Kappler J. The staphylococcal enterotoxins and their relatives. Science. 1990;248:705–711.

    Article  CAS  PubMed  Google Scholar 

  62. Kotzin BL, Leung DY, Kappler J, et al. Superantigens and their potential role in human disease. Adv Immunol. 1993;54:99–166.

    Article  CAS  PubMed  Google Scholar 

  63. Benjamin MA, Lu J, Donnelly G, et al. Changes in murine jejunal morphology evoked by the bacterial superantigen Staphylococcus aureus enterotoxin B are mediated by CD4+ T cells. Infect Immun. 1998;66:2193–2199.

    CAS  PubMed  Google Scholar 

  64. McKay DM, Benjamin MA, Lu J. CD4+ T cells mediate superantigen-induced abnormalities in murine jejunal ion transport. Am J Physiol. 1998;275:G29–G38.

    CAS  PubMed  Google Scholar 

  65. Marrack P, Blackman M, Kushnir E, et al. The toxicity of staphylococcal enterotoxin B in mice is mediated by T cells. J Exp Med. 1990;171:455–464.

    Article  CAS  PubMed  Google Scholar 

  66. Hamad AR, Marrack P, Kappler JW. Transcytosis of staphylococcal superantigen toxins. J Exp Med. 1997;185:1447–1454.

    Article  CAS  PubMed  Google Scholar 

  67. Stiles BG, Garza AR, Ulrich RG, et al. Mucosal vaccination with recombinantly attenuated staphylococcal enterotoxin B and protection in a murine model. Infect Immun. 2001;69:2031–2036.

    Article  CAS  PubMed  Google Scholar 

  68. Langley R, Wines B, Willoughby N, et al. The staphylococcal superantigen-like protein 7 binds IgA and complement C5 and inhibits IgA-Fc alpha RI binding and serum killing of bacteria. J Immunol. 2005;174:2926–2933.

    CAS  PubMed  Google Scholar 

  69. Lundqvist C, Baranov V, Hammarström S, et al. Intra-epithelial lymphocytes. Evidence for regional specialization and extrathymic T cell maturation in the human gut epithelium. Int Immunol. 1995;7:1473–1487.

    Article  CAS  PubMed  Google Scholar 

  70. Roberts AI, Blumberg RS, Christ AD, et al. Staphylococcal enterotoxin B induces potent cytotoxic activity by intraepithelial lymphocytes. Immunology. 2000;101:185–190.

    Article  CAS  PubMed  Google Scholar 

  71. Mayumi T, Takezawa J, Takahashi H, et al. IL-15 is elevated in the patients of postoperative enterocolitis. Cytokine. 1999;11:888–893.

    Article  CAS  PubMed  Google Scholar 

  72. Miller C, Ragheb JA, Schwartz RH. Anergy and cytokine-mediated suppression as distinct superantigen-induced tolerance mechanisms in vivo. J Exp Med. 1999;190:53–64.

    Article  CAS  PubMed  Google Scholar 

  73. Stone SP, Beric V, Quick A, et al. The effect of an enhanced infection-control policy on the incidence of Clostridium difficile infection and methicillin-resistant Staphyloccocus aureus colonization in acute elderly medical patients. Age Ageing. 1998;27:561–568.

    Article  CAS  PubMed  Google Scholar 

  74. Henderson DK. Managing methicillin-resistant staphylococci: A paradigm for preventing nosocomial transmission of resistant organisms. Am J Infect Control. 2006;34:S46–S54.

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Division of Gastroenterology, Department of Medicine, St. Luke’s-Roosevelt Hospital Center, New York, NY, USA

    Zheng Lin

  2. Division of Gastroenterology, Department of Medicine, S&R 12, St. Luke’s-Roosevelt Hospital Center, Columbia University College of Physicians and Surgeons, 1111 Amsterdam Avenue, New York, NY, 10025, USA

    Donald P. Kotler

  3. University of Minnesota School of Medicine, Minneapolis, MN, USA

    Patrick M. Schlievert

  4. Division of Infectious Diseases, Department of Medicine, St. Luke’s-Roosevelt Hospital Center, Columbia University College of Physicians and Surgeons, New York, NY, USA

    Emilia Mia Sordillo

  5. Department of Pathology, St. Luke’s-Roosevelt Hospital Center, Columbia University College of Physicians and Surgeons, New York, NY, USA

    Emilia Mia Sordillo

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  1. Zheng Lin
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  2. Donald P. Kotler
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  3. Patrick M. Schlievert
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  4. Emilia Mia Sordillo
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Correspondence to Donald P. Kotler.

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Lin, Z., Kotler, D.P., Schlievert, P.M. et al. Staphylococcal Enterocolitis: Forgotten but Not Gone?. Dig Dis Sci 55, 1200–1207 (2010). https://doi.org/10.1007/s10620-009-0886-1

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  • DOI: https://doi.org/10.1007/s10620-009-0886-1

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