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Digestive Diseases and Sciences

, Volume 55, Issue 5, pp 1200–1207 | Cite as

Staphylococcal Enterocolitis: Forgotten but Not Gone?

  • Zheng Lin
  • Donald P. Kotler
  • Patrick M. Schlievert
  • Emilia Mia Sordillo
Review

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.

Keywords

Staphylococcus aureus Enterocolitis Infectious diarrhea Toxic shock Superantigen 

References

  1. 1.
    Felsen J, Wolarsky W. Epidemic diarrhea of the newborn. Arch Pediatr. 1942;59:495–512.Google Scholar
  2. 2.
    Kramer IRH. Fatal staphylococcal enteritis developing during streptomycin therapy by mouth. Lancet. 1948;2(6530):646–647.CrossRefPubMedGoogle Scholar
  3. 3.
    Altemeier WA, Hummel RP, Hill EO. Staphylococcal enterocolitis following antibiotic therapy. Ann Surg. 1963;157:847–858.CrossRefPubMedGoogle Scholar
  4. 4.
    Prohaska JV. Pseudomembranous enterocolitis; the experimental induction of the disease with Staphylococcus aureus and its enterotoxin. AMA Arch Surg. 1959;79:197–206.PubMedGoogle Scholar
  5. 5.
    [No authors listed]. Antibiotics, staphylococcal enteritis and pseudomembranous enterocolitis. N Engl J Med. 1953;249:37–40.Google Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. 7.
    Cunha BA. Nosocomial diarrhea. Crit Care Clin. 1998;14:329–338.CrossRefPubMedGoogle Scholar
  8. 8.
    College of American Pathologists. Microbiology Checklist, rev. 09/27/2007.Google Scholar
  9. 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.CrossRefPubMedGoogle Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. 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.PubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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. 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.PubMedGoogle Scholar
  15. 15.
    Noel GJ, Edelson PJ. Staphylococcus epidermidis bacteremia in neonates: Further observations and the occurrence of focal infection. Pediatrics. 1984;74:832–837.PubMedGoogle Scholar
  16. 16.
    Gruskay JA, Abbasi S, Anday E, et al. Staphylococcus epidermidis-associated enterocolitis. J Pediatr. 1986;109:520–524.CrossRefPubMedGoogle Scholar
  17. 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.CrossRefPubMedGoogle Scholar
  18. 18.
    Mollitt DL, Tepas JJ, Talbert JL. The role of coagulase-negative Staphylococcus in neonatal necrotizing enterocolitis. J Pediatr Surg. 1988;23:60–63.CrossRefPubMedGoogle Scholar
  19. 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.CrossRefPubMedGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.PubMedGoogle Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. 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. 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.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefPubMedGoogle Scholar
  26. 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. 27.
    Gruber WC, Pietsch JB. Toxic shock syndrome associated with Staphylococcus aureus enterocolitis. Pediatr Infect Dis J. 1988;7:71–72.PubMedCrossRefGoogle Scholar
  28. 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.PubMedGoogle Scholar
  29. 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.PubMedGoogle Scholar
  30. 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.CrossRefPubMedGoogle Scholar
  31. 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.PubMedGoogle Scholar
  32. 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.CrossRefPubMedGoogle Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. 35.
    Taylor M, Ajayi F, Almond M. Enterocolitis caused by methicillin-resistant Staphylococcus aureus. Lancet. 1993;342(8874):804.CrossRefPubMedGoogle Scholar
  36. 36.
    Schiller B, Chiorazzi N, Farber BF. Methicillin-resistant staphylococcal enterocolitis. Am J Med. 1998;105:164–166.CrossRefPubMedGoogle Scholar
  37. 37.
    Flemming K, Ackermann G. Prevalence of enterotoxin producing Staphylococcus aureus in stools of patients with nosocomial diarrhea. Infection. 2007;35:356–358.CrossRefPubMedGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.CrossRefPubMedGoogle Scholar
  42. 42.
    Kelly CP, Pothoulakis C, LaMont JT. Clostridium difficile colitis. N Engl J Med. 1994;330:257–262.CrossRefPubMedGoogle Scholar
  43. 43.
    McCormick JK, Yarwood JM, Schlievert PM. Toxic shock syndrome and bacterial superantigens: An update. Ann Rev Microbiol. 2001;55:77–104.CrossRefGoogle Scholar
  44. 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.CrossRefPubMedGoogle Scholar
  45. 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.CrossRefPubMedGoogle Scholar
  46. 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.CrossRefPubMedGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. 48.
    Price AB, Davies DR. Pseudomembranous colitis. J Clin Pathol. 1977;30:1–12.CrossRefPubMedGoogle Scholar
  49. 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.CrossRefPubMedGoogle Scholar
  50. 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.CrossRefPubMedGoogle Scholar
  51. 51.
    Yarwood JM, Schlievert PM. Quorum sensing in Staphylococcus infections. J Clin Invest. 2003;112:1620–1625.PubMedGoogle Scholar
  52. 52.
    Dinges MM, Orwin PM, Schlievert PM. Exotoxins of Staphylococcus aureus. Clin Microbiol Rev. 2000;13:16–34.CrossRefPubMedGoogle Scholar
  53. 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.PubMedGoogle Scholar
  54. 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.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefPubMedGoogle Scholar
  56. 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.PubMedGoogle Scholar
  57. 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.CrossRefPubMedGoogle Scholar
  58. 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.CrossRefPubMedGoogle Scholar
  59. 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.CrossRefPubMedGoogle Scholar
  60. 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.CrossRefPubMedGoogle Scholar
  61. 61.
    Marrack P, Kappler J. The staphylococcal enterotoxins and their relatives. Science. 1990;248:705–711.CrossRefPubMedGoogle Scholar
  62. 62.
    Kotzin BL, Leung DY, Kappler J, et al. Superantigens and their potential role in human disease. Adv Immunol. 1993;54:99–166.CrossRefPubMedGoogle Scholar
  63. 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.PubMedGoogle Scholar
  64. 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.PubMedGoogle Scholar
  65. 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.CrossRefPubMedGoogle Scholar
  66. 66.
    Hamad AR, Marrack P, Kappler JW. Transcytosis of staphylococcal superantigen toxins. J Exp Med. 1997;185:1447–1454.CrossRefPubMedGoogle Scholar
  67. 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.CrossRefPubMedGoogle Scholar
  68. 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.PubMedGoogle Scholar
  69. 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.CrossRefPubMedGoogle Scholar
  70. 70.
    Roberts AI, Blumberg RS, Christ AD, et al. Staphylococcal enterotoxin B induces potent cytotoxic activity by intraepithelial lymphocytes. Immunology. 2000;101:185–190.CrossRefPubMedGoogle Scholar
  71. 71.
    Mayumi T, Takezawa J, Takahashi H, et al. IL-15 is elevated in the patients of postoperative enterocolitis. Cytokine. 1999;11:888–893.CrossRefPubMedGoogle Scholar
  72. 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.CrossRefPubMedGoogle Scholar
  73. 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.CrossRefPubMedGoogle Scholar
  74. 74.
    Henderson DK. Managing methicillin-resistant staphylococci: A paradigm for preventing nosocomial transmission of resistant organisms. Am J Infect Control. 2006;34:S46–S54.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Zheng Lin
    • 1
  • Donald P. Kotler
    • 2
  • Patrick M. Schlievert
    • 3
  • Emilia Mia Sordillo
    • 4
    • 5
  1. 1.Division of Gastroenterology, Department of MedicineSt. Luke’s-Roosevelt Hospital CenterNew YorkUSA
  2. 2.Division of Gastroenterology, Department of Medicine, S&R 12St. Luke’s-Roosevelt Hospital Center, Columbia University College of Physicians and SurgeonsNew YorkUSA
  3. 3.University of Minnesota School of MedicineMinneapolisUSA
  4. 4.Division of Infectious Diseases, Department of MedicineSt. Luke’s-Roosevelt Hospital Center, Columbia University College of Physicians and SurgeonsNew YorkUSA
  5. 5.Department of PathologySt. Luke’s-Roosevelt Hospital Center, Columbia University College of Physicians and SurgeonsNew YorkUSA

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