Digestive Diseases and Sciences

, Volume 58, Issue 11, pp 3242–3245 | Cite as

Pathogen-Specific Risk of Celiac Disease Following Bacterial Causes of Foodborne Illness: A Retrospective Cohort Study

  • Mark S. RiddleEmail author
  • Joseph A. Murray
  • Brooks D. Cash
  • Mark Pimentel
  • Chad K. Porter
Original Article



The US CDC recently estimated over 2 million foodborne illnesses annually are caused by 4 major enteropathogens: non-typhoid Salmonella spp., Campylobacter spp., Shigella spp., and Yersinia enterocolitica. While recent data suggest functional gastrointestinal disorders are associated with these infections, studies linking foodborne illness to celiac disease (CD) are limited. We utilized a US Department of Defense medical encounter database to evaluate the risk of CD following select foodborne infections.


We identified subjects with acute gastroenteritis between 1998 and 2009 attributed to Salmonella (nontyphoidal) spp., Shigella spp., Campylobacter spp., or Y. enterocolitica and matched each with up to 4 unexposed subjects. Exposed and unexposed subjects were followed for incident CD diagnosis for their entire military record duration (or a minimum of 1 year). Relative risks were calculated using modified Poisson regression to determine the relationship between pathogen-attributable gastroenteritis and CD while controlling for covariates.


A total of 1,753 pathogen-specific gastroenteritis cases (Campylobacter: 738; Salmonella: 624; Shigella: 376; Yersinia: 17) were identified and followed for a median of 3.8 years. The incidence (per 100,000 person-years) of CD was 0.05. We found a suggested risk of CD after Campylobacter, but not other foodborne infection etiologies.


These data support a previous study demonstrating increased risk of CD following Campylobacteriosis and highlight the need for additional research into how infections might trigger CD in susceptible individuals.


Epidemiology Cohort study Campylobacteriosis Celiac disease Foodborne illness 



The authors thank the staff at the Armed Forces Health Surveillance Center (Maryland) for their role in providing the data from the DoD Defense Medical Surveillance System.

Conflict of interest


Copyright statement

The views expressed in this article are those of the author and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, nor the US Government. This is a US Government work. There are no restrictions on its use. There were no financial conflicts of interests among any of the authors. Two of the authors are employees of the US Government and military service members. This work was prepared as part of official duties. Title 17 U.S.C. §105 provides that “Copyright protection under this title is not available for any work of the United States Government.” Title 17 U.S.C. §101 defines a US Government work as a work prepared by a military service member or employee of the US Government as part of that person’s official duties.

Human subjects review

The study protocol was approved by the Naval Medical Research Center Institutional Review Board in compliance with all applicable Federal regulations governing the protection of human subjects.


  1. 1.
    Scallan E, Griffin PM, Angulo FJ, Tauxe RV, Hoekstra RM. Foodborne illness acquired in the United States-unspecified agents. Emerg Infect Dis. 2011;17:16–22.PubMedCrossRefGoogle Scholar
  2. 2.
    Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis. 2011;17:7–15.PubMedGoogle Scholar
  3. 3.
    Tsang RS. The relationship of Campylobacter jejuni infection and the development of Guillain–Barre syndrome. Curr Opin Infect Dis. 2002;15:221–228.PubMedCrossRefGoogle Scholar
  4. 4.
    Hill Gaston JS, Lillicrap MS. Arthritis associated with enteric infection. Best Pract Res Clin Rheumatol. 2003;17:219–239.PubMedCrossRefGoogle Scholar
  5. 5.
    Verdu EF, Riddle MS. Chronic gastrointestinal consequences of acute infectious diarrhea: evolving concepts in epidemiology and pathogenesis. Am J Gastroenterol. 2012;107:981–989.PubMedCrossRefGoogle Scholar
  6. 6.
    Green PH, Cellier C. Celiac disease. N Engl J Med. 2007;357:1731–1743.PubMedCrossRefGoogle Scholar
  7. 7.
    Falth-Magnusson K, Franzen L, Jansson G, Laurin P, Stenhammar L. Infant feeding history shows distinct differences between Swedish celiac and reference children. Pediatr Allergy Immunol. 1996;7:1–5.PubMedCrossRefGoogle Scholar
  8. 8.
    Verdu EF, Mauro M, Bourgeois J, Armstrong D. Clinical onset of celiac disease after an episode of Campylobacter jejuni enteritis. Can J Gastroenterol. 2007;21:453–455.PubMedGoogle Scholar
  9. 9.
    Riddle MS, Murray JA, Porter CK. The incidence and risk of celiac disease in a healthy US adult population. Am J Gastroenterol. 2012;107:1248–1255.PubMedCrossRefGoogle Scholar
  10. 10.
    Rubertone MV, Brundage JF. The Defense Medical Surveillance System and the Department of Defense serum repository: glimpses of the future of public health surveillance. Am J Public Health. 2002;92:1900–1904.PubMedCrossRefGoogle Scholar
  11. 11.
    Zou G. A modified poisson regression approach to prospective studies with binary data. Am J Epidemiol. 2004;159:702–706.PubMedCrossRefGoogle Scholar
  12. 12.
    Chen ML, Ge Z, Fox JG, Schauer DB. Disruption of tight junctions and induction of proinflammatory cytokine responses in colonic epithelial cells by Campylobacter jejuni. Infect Immun. 2006;74:6581–6589.PubMedCrossRefGoogle Scholar
  13. 13.
    Kalischuk LD, Buret AG. A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease? Am J Physiol Gastrointest Liver Physiol. 2010;298:G1–G9.PubMedCrossRefGoogle Scholar
  14. 14.
    Kalischuk LD, Inglis GD, Buret AG. Campylobacter jejuni induces transcellular translocation of commensal bacteria via lipid rafts. Gut Pathog. 2009;1:2.PubMedCrossRefGoogle Scholar
  15. 15.
    Ternhag A, Torner A, Svensson A, Ekdahl K, Giesecke J. Short- and long-term effects of bacterial gastrointestinal infections. Emerg Infect Dis. 2008;14:143–148.PubMedCrossRefGoogle Scholar
  16. 16.
    Gradel KO, Nielsen HL, Schonheyder HC, Ejlertsen T, Kristensen B, Nielsen H. Increased short- and long-term risk of inflammatory bowel disease after salmonella or campylobacter gastroenteritis. Gastroenterology. 2009;137:495–501.PubMedCrossRefGoogle Scholar
  17. 17.
    Jabri B, Sollid LM. Tissue-mediated control of immunopathology in coeliac disease. Nat Rev Immunol. 2009;9:858–870.PubMedCrossRefGoogle Scholar
  18. 18.
    Jabri B, Kasarda DD, Green PH. Innate and adaptive immunity: the yin and yang of celiac disease. Immunol Rev. 2005;206:219–231.PubMedCrossRefGoogle Scholar
  19. 19.
    Natividad JM, Huang X, Slack E, et al. Host responses to intestinal microbial antigens in gluten-sensitive mice. PLoS One. 2009;4:e6472.PubMedCrossRefGoogle Scholar
  20. 20.
    Verdu EF, Huang X, Natividad J, et al. Gliadin-dependent neuromuscular and epithelial secretory responses in gluten-sensitive HLA-DQ8 transgenic mice. Am J Physiol Gastrointest Liver Physiol. 2008;294:G217–G225.PubMedCrossRefGoogle Scholar
  21. 21.
    Fasano A, Shea-Donohue T. Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat Clin Pract Gastroenterol Hepatol. 2005;2:416–422.PubMedCrossRefGoogle Scholar
  22. 22.
    DeMeo MT, Mutlu EA, Keshavarzian A, Tobin MC. Intestinal permeation and gastrointestinal disease. J Clin Gastroenterol. 2002;34:385–396.PubMedCrossRefGoogle Scholar
  23. 23.
    Chae SC, Yu JL, Oh GJ, et al. Identification of single nucleotide polymorphisms in the TNFRSF17 gene and their association with gastrointestinal disorders. Mol Cells. 2010;29:21–28.PubMedCrossRefGoogle Scholar
  24. 24.
    Landzberg BR, Connor BA. Persistent diarrhea in the returning traveler: think beyond persistent infection. Scand J Gastroenterol. 2005;40:112–114.PubMedCrossRefGoogle Scholar
  25. 25.
    Ginsburg PM, Bayless TM. How can IBD be distinguished from IBS? Inflamm Bowel Dis. 2008;14:S152–S154.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York (Outside the USA) 2013

Authors and Affiliations

  • Mark S. Riddle
    • 1
    Email author
  • Joseph A. Murray
    • 2
  • Brooks D. Cash
    • 3
  • Mark Pimentel
    • 4
  • Chad K. Porter
    • 1
  1. 1.Enteric Diseases Department, Infectious Disease DirectorateNaval Medical Research CenterSilver SpringUSA
  2. 2.Mayo ClinicRochesterUSA
  3. 3.Walter Reed National Military Medical CenterBethesdaUSA
  4. 4.Cedars-Sinai Medical CenterLos AngelesUSA

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