Current Tropical Medicine Reports

, Volume 3, Issue 3, pp 94–101 | Cite as

Enteropathogen-Induced Microbiota Biofilm Disruptions and Post-Infectious Intestinal Inflammatory Disorders

  • Andre G. BuretEmail author
Protozoa (R Mejia, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Protozoa


Recent observations indicate that acute enteric infections may contribute to various intestinal and extra-intestinal disorders long after elimination of the inciting microorganism. The mechanisms remain unclear. This review discusses how alterations to the gut microbiota by enteropathogens during the acute stage of an infection may at least in part contribute to these presentations. After providing a critical discussion of the biology of the human intestinal microbiota, the review presents recent data that illustrate how enteropathogens may activate latent virulence genes in commensal bacteria, disrupt the microbiota biofilm phenotype, and promote the release of pathobionts from the commensal biofilm. Evidence suggests that, in turn, these planktonic pathobionts may spontaneously translocate across the mucus and the gut epithelium to trigger, at least in part, the pro-inflammatory events that lead to these long-term, post-infectious sequelae.


Campylobacter Diarrhea Giardia Inflammatory bowel disease Post-infectious intestinal inflammation Post-infectious irritable bowel syndrome 



Critical proofreading by Drs. Jean-Paul Motta and James Cotton is gratefully acknowledged.

Compliance with Ethical Standards

Conflict of Interest

Some of the findings discussed in this article have been generated through the financial support of the Natural Sciences and Engineering Research Council of Canada, Crohn’s and Colitis Canada, Alberta Innovates Health Solution, and the Canadian Institutes of Health Research. Lupin Pharmaceuticals, Inc., Baltimore, MD, facilitated this article by providing financial support.

Andre G. Buret declares no other conflict of interest.

Human and Animal Rights and Informed Consent

This article may contain studies with human or animal subjects performed by the author. The author verifies that all current Ethical Standards for the conductance of prospective research were followed.


  1. 1.
    O’Ryan M, Prado V, Pickering LK. A millennium update on pediatric diarrheal illness in the developing world. Semin Pediatr Infect Dis. 2005;16:125–36.PubMedCrossRefGoogle Scholar
  2. 2.
    Riddle MS, Sanders JW, Putnam SD, et al. Incidence, etiology, and impact of diarrhea among long-term travelers (US military and similar populations): a systematic review. Am J Trop Med Hyg. 2006;74:891–900.PubMedGoogle Scholar
  3. 3.
    Letizia A, Riddle MS, Tribble D, et al. Effects of pre-deployment loperamide provision on use and travelers’ diarrhea outcomes among U.S. military personnel deployed to Turkey. Travel Med Infect Dis. 2014;12:360–3.PubMedCrossRefGoogle Scholar
  4. 4.
    Pavli A, Silvestros C, Patrinos S, et al. Pre-travel preparation practices among business travellers to tropical and subtropical destinations: results from the Athens International Airport Survey. Travel Med Infect Dis. 2014;12:364–9.PubMedCrossRefGoogle Scholar
  5. 5.
    Grady D. Gastrointestinal infection deaths more than doubled. New York Times; 2012. Available at: Accessed 8 Aug 2015.
  6. 6.
    Buret AG, Reti K. Acute enteric infections alter commensal microbiota: new mechanisms in post-infectious intestinal inflammatory disorders. In: Heidt PJ, Lang D, Riddle MS, et al, editors. Persisting Consequences of Intestinal Infections. Old Herborn University Monograph, OHUS; 2014. p. 87–106. ISBN: 3-923022-39-5.Google Scholar
  7. 7.
    Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the United States—major pathogens. Emerg Infect Dis. 2011;17:7–15.PubMedPubMedCentralCrossRefGoogle Scholar
  8. 8.
    Liu J, Kabir F, Manneh J, et al. Development and assessment of molecular diagnostic tests for 15 enteropathogens causing childhood diarrhoea: a multicentre study. Lancet Infect Dis. 2014;14:716–24.PubMedCrossRefGoogle Scholar
  9. 9.
    Payne DC, Vinjé J, Szilagyi PG, et al. Norovirus and medically attended gastroenteritis in U.S. children. N Engl J Med. 2013;368:1121–30.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Bartelt LA, Sartor RB. Advances in understanding Giardia: determinants and mechanisms of chronic sequelae. F1000Prime Rep. 2015;7:1–14.CrossRefGoogle Scholar
  11. 11.
    Rees JH, Soudain SE, Gregson NA, et al. Campylobacter jejuni infection and Guillain-Barré syndrome. N Engl J Med. 1995;333:1374–9.PubMedCrossRefGoogle Scholar
  12. 12.
    Thabane M, Kottachchi DT, Marshall JK. Systematic review and meta-analysis: the incidence and prognosis of post-infectious irritable bowel syndrome. Aliment Pharmacol Ther. 2007;26:535–44.PubMedCrossRefGoogle Scholar
  13. 13.
    Gradel KO, Nielsen HL, Schønheyder HC, et al. Increased short- and long-term risk of inflammatory bowel disease after Salmonella or Campylobacter gastroenteritis. Gastroenterology. 2009;137:495–501.PubMedCrossRefGoogle Scholar
  14. 14.
    García Rodríguez LA, Ruigómez A, Panés J. Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology. 2006;130:1588–94.PubMedCrossRefGoogle Scholar
  15. 15.
    Halliez MCM, Buret AG. Extra-intestinal and long term consequences of Giardia duodenalis infections. World J Gastroenterol. 2013;19:8974–85.PubMedPubMedCentralCrossRefGoogle Scholar
  16. 16.
    Network Investigators MAL-ED. The MAL-ED study: a multinational and multidisciplinary approach to understand the relationship between enteric pathogens, malnutrition, gut physiology, physical growth, cognitive development, and immune responses in infants and children up to 2 years of age in resource-poor environments. Clin Infect Dis. 2014;59:S193–206.CrossRefGoogle Scholar
  17. 17.
    Buret A, Amat C, Manko A, et al. Giardia duodenalis: new research developments in pathophysiology, pathogenesis, and virulence factors. Curr Trop Med Rep. 2015;2:110–8.CrossRefGoogle Scholar
  18. 18.
    Savioli L, Smith H, Thompson A. Giardia and Cryptosporidium join the ‘neglected diseases initiative’. Trends Parasitol. 2006;22:203–8.PubMedCrossRefGoogle Scholar
  19. 19.
    World Health Organization. Campylobacter. Fact sheet N°255. 2011. Available at: Accessed 7 Aug 2015.
  20. 20.
    Connor BA, Schwartz E. Typhoid and paratyphoid fever in travellers. Lancet Infect Dis. 2005;5:623–8.PubMedCrossRefGoogle Scholar
  21. 21.
    Evering T, Weiss LM. The immunology of parasite infections in immunocompromised hosts. Parasite Immunol. 2006;28:549–65.PubMedPubMedCentralGoogle Scholar
  22. 22.
    Solaymani-Mohammadi S, Singer SM. Giardia duodenalis: the double-edged sword of immune responses in giardiasis. Exp Parasitol. 2010;126:292–7.PubMedPubMedCentralCrossRefGoogle Scholar
  23. 23.
    Cotton JA, Beatty JK, Buret AG. Host parasite interactions and pathophysiology in Giardia infections. Int J Parasitol. 2011;41:925–33.PubMedCrossRefGoogle Scholar
  24. 24.
    von Allmen N, Christen S, Forster U, et al. Acute trichinellosis increases susceptibility to Giardia lamblia infection in the mouse model. Parasitology. 2006;133:139–49.CrossRefGoogle Scholar
  25. 25.
    Ankarklev J, Hestvik E, Lebbad M, et al. Common coinfections of Giardia intestinalis and Helicobacter pylori in non-symptomatic Ugandan children. PLoS Negl Trop Dis. 2012;6:e1780.PubMedPubMedCentralCrossRefGoogle Scholar
  26. 26.
    Bhavnani D, Goldstick JE, Cevallos W, et al. Synergistic effects between rotavirus and coinfecting pathogens on diarrheal disease: evidence from a community-based study in northwestern Ecuador. Am J Epidemiol. 2012;176:387–95.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Mahmoudi MR, Kazemi B, Mohammadiha A, et al. Detection of Cryptosporidium and Giardia (oo)cysts by IFA, PCR and LAMP in surface water from Rasht, Iran. Trans R Soc Trop Med Hyg. 2013;107:511–7.PubMedCrossRefGoogle Scholar
  28. 28.
    Mohamed AS, Levine M, Camp Jr JW, et al. Temporal patterns of human and canine Giardia infection in the United States: 2003–2009. Prev Vet Med. 2014;113:249–56.PubMedCrossRefGoogle Scholar
  29. 29.
    Mukherjee AK, Chowdhury P, Rajendran K, et al. Association between Giardia duodenalis and coinfection with other diarrhea-causing pathogens in India. Biomed Res Int. 2014;2014:786480.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Moore SR. Early childhood diarrhea and helminthiases associated with long-term linear growth faltering. Int J Epidemiol. 2001;30:1457–64.PubMedCrossRefGoogle Scholar
  31. 31.
    Jensen LA, Marlin JW, Dyck DD, et al. Prevalence of multi-gastrointestinal infections with helminth, protozoan and Campylobacter spp. in Guatemalan children. J Infect Dev Ctries. 2009;3:229–34.PubMedGoogle Scholar
  32. 32.
    Veenemans J, Schouten LRA, Ottenhof MJ, et al. Effect of preventive supplementation with zinc and other micronutrients on non-malarial morbidity in Tanzanian pre-school children: a randomized trial. PLoS One. 2012;7:e41630.PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Cotton J, Motta JP, Schenk LP, et al. Giardia duodenalis infection reduces granulocyte infiltration in an in vivo model of bacterial toxin-induced colitis and attenuates inflammation in human intestinal tissue. PLoS One. 2014;9:e109087.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol. 2003;3:733–44.PubMedCrossRefGoogle Scholar
  35. 35.
    Chen CC, Louie S, Shi HN. Concurrent infection with an intestinal helminth parasite impairs host resistance to enteric Citrobacter rodentium and enhances Citrobacter-induced colitis in mice. Infect Immun. 2005;73:5468–81.PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    Osborne LC, Monticelli LA, Nice TJ, et al. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science. 2014;345:578–82.PubMedPubMedCentralCrossRefGoogle Scholar
  37. 37.
    Cotton JA, Bhargava A, Ferraz JG, et al. Giardia duodenalis cathepsin B proteases degrade intestinal epithelial interleukin-8 and attenuate interleukin-8-induced neutrophil chemotaxis. Infect Immun. 2014;82:2772–87.PubMedPubMedCentralCrossRefGoogle Scholar
  38. 38.
    Kamada N, Chen GY, Inohara N, et al. Control of pathogens and pathobionts by the gut microbiota. Nat Immunol. 2013;14:685–90.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Faith JJ, Guruge JL, Charbonneau M, et al. The long-term stability of the human gut microbiota. Science. 2013;341:1237439.PubMedPubMedCentralCrossRefGoogle Scholar
  40. 40.
    Dominianni C, Sinha R, Goedert JJ, et al. Sex, body mass index, and dietary fiber intake influence the human gut microbiome. PLoS One. 2015;10(4):e0124599.PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Thompson JA, Oliveira RA, Djukovic A, et al. Manipulation of the quorum sensing signal AI-2 affects the antibiotic-treated gut microbiota. Cell Rep. 2015;10:1861–71.PubMedCrossRefGoogle Scholar
  42. 42.
    Franzosa EA, Hunag K, Meadow JF, et al. Identifying personal microbiomes using metagenomic codes. Proc Natl Acad Sci U S A. 2015;112:E2930–8.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Magnusson KR, Hauck L, Jeffrey BM, et al. Relationship between diet-related changes in the gut microbiome and cognitive flexibility. Neuroscience. 2015;300:128–40.PubMedCrossRefGoogle Scholar
  44. 44.
    Nobel YR, Cox LM, Kirigin FK, et al. Metabolic and metagenomic outcomes from early-life pulsed antibiotic treatment. Nat Commun. 2015;6:7486.PubMedPubMedCentralCrossRefGoogle Scholar
  45. 45.
    Collins SM, Surette M, Bercik P. The interplay between the intestinal microbiota and the brain. Nat Rev Microbiol. 2012;10:735–42.PubMedCrossRefGoogle Scholar
  46. 46.
    Carding S, Verbeke K, Vipond DT, et al. Dysbiosis of the gut microbiota in disease. Microb Ecol Health Dis. 2015;26:26191.PubMedGoogle Scholar
  47. 47.
    Gao Z, Guo B, Gao R, et al. Microbiota dysbiosis is associated with colorectal cancer. Front Microbiol. 2015;6:20.PubMedPubMedCentralGoogle Scholar
  48. 48.
    Ijssennagger N, Belzer C, Hooiveld GJ, et al. Gut microbiota facilitates dietary heme-induced epithelial hyperproliferation by opening the mucus barrier in colon. Proc Natl Acad Sci U S A. 2015;112:10038–43.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    De Weerth C, Funetes S, Puylaert P, et al. Intestinal microbiota of infants with colic: development and specific signatures. Pediatrics. 2013;131:e550–8.PubMedCrossRefGoogle Scholar
  50. 50.
    Lepage P, LeClerc MC, Joossens M, et al. Metagenomic insight into our gut’s microbiome. Gut. 2013;62:146–58.PubMedCrossRefGoogle Scholar
  51. 51.
    de Vos WM. Microbial biofilms and the human intestinal microbiome. NPJ Biofilms Microbiomes. 2015;1:15005.CrossRefGoogle Scholar
  52. 52.
    Motta JP, Flannigan KL, Agbor TA, et al. Hydrogen sulfide protects from colitis and restores intestinal microbiota biofilm and mucus production. Inflamm Bowel Dis. 2015;21:1006–17.PubMedCrossRefGoogle Scholar
  53. 53.
    Hity M, Burke C, Pedro H, et al. Disordered microbial communities in asthmatic airways. PLoS One. 2010;5:e8578.CrossRefGoogle Scholar
  54. 54.
    Scher JU, Abramson SB. The microbiome and rheumatoid arthritis. Nat Rev Rheumatol. 2011;7:569–78.PubMedPubMedCentralGoogle Scholar
  55. 55.
    Kelly CR, Kahn S, Kashyap P, et al. Update on fecal microbiota transplantation 2015: indications, methodologies, mechanisms, and outlook. Gastroenterology. 2015;149:223–37.PubMedPubMedCentralCrossRefGoogle Scholar
  56. 56.
    Zoetendal EG, Rajilic-Stojanovic M, de Vos WM. High-throughput diversity and functionality analysis of the gastrointestinal tract microbiota. Gut. 2008;57:1605–15.PubMedCrossRefGoogle Scholar
  57. 57.
    Dethlefsen L, Relman DA. Incomplete recovery and individualized responses of the human distal gut microbiota to repeated antibiotic perturbation. Proc Natl Acad Sci U S A. 2011;108 Suppl 1:4554–61.PubMedCrossRefGoogle Scholar
  58. 58.
    Forsythe P, Kunze WA. Voices from within: gut microbes and the CNS. Cell Mol Life Sci. 2013;70:55–69.PubMedCrossRefGoogle Scholar
  59. 59.
    Hopkins MJ, Sharp R, Macfarlane GT. Variation in human intestinal microbiota with age. Dig Liver Dis. 2002;34 Suppl 2:S12–8.PubMedCrossRefGoogle Scholar
  60. 60.
    Tap J, Mondot S, Levenez F, et al. Towards the human intestinal phylogenetic core. Environ Microbiol. 2009;11:2574–84.PubMedCrossRefGoogle Scholar
  61. 61.
    Frank DN, St Amand AL, Feldman RA, et al. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A. 2007;104:13780–5.PubMedPubMedCentralCrossRefGoogle Scholar
  62. 62.
    Macfarlane GT, Gibson GR, Cumming JH. Comparison of fermentation reactions in different regions of the human colon. J Appl Bacteriol. 1992;72:57–64.PubMedGoogle Scholar
  63. 63.
    Macfarlane S, Macfarlane G. Bacterial colonization of surfaces in the large intestine. In: Gibson G, Roberfroid M, editors. Colonic Microflora, Nutrition and Health. London: Chapman and Hall; 1999. p. 71–87.CrossRefGoogle Scholar
  64. 64.
    Ganesh BP, Klopfleisch R, Loh G, et al. Commensal Akkermansia muciniphila exacerbates gut inflammation in Salmonella typhimurium-infected gnotobiotic mice. PLoS One. 2013;8:e74963.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Jakobsson HE, Rodríguez-Piñeiro AM, Schütte A, et al. The composition of the gut microbiota shapes the colon mucus barrier. EMBO Rep. 2015;16:164–77.PubMedCrossRefGoogle Scholar
  66. 66.
    Swidsinsky A, Loering-Bauke V, Herber A. Mucosal flora in Crohn’s disease and ulcerative colitis – an overview. J Physiol Pharmacol. 2009;60 Suppl 6:61–71.Google Scholar
  67. 67.
    Darfeuille-Michaud A, Neut C, Barnich N, et al. Presence of adherent Escherichia coli strains in ileal mucosa of patients with Crohn’s disease. Gastroenterology. 1998;115:1405–13.PubMedCrossRefGoogle Scholar
  68. 68.
    Chassaing B, Koren O, Goodrich JK, et al. Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature. 2015;519:92–6.PubMedPubMedCentralCrossRefGoogle Scholar
  69. 69.
    De Filippo C, Cavalieri D, Di Paola M, et al. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci U S A. 2010;107:14691–6.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Xavier RJ, Podolsky DK. Unravelling the pathogenesis of inflammatory bowel disease. Nature. 2007;448:427–34.PubMedCrossRefGoogle Scholar
  71. 71.
    Kalischuk LD, Buret AG. A role for Campylobacter jejuni-induced enteritis in inflammatory bowel disease? Am J Physiol Gastrointest Liver Physiol. 2009;298:G1–9.PubMedCrossRefGoogle Scholar
  72. 72.
    Chassaing B, Darfeuille-Michaud A. The commensal microbiota and enteropathogens in the pathogenesis of inflammatory bowel diseases. Gastroenterology. 2011;140:1720–8.PubMedCrossRefGoogle Scholar
  73. 73.
    Sokol H, Pigneur B, Watterlot L, et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci U S A. 2008;105:16731–6.PubMedPubMedCentralCrossRefGoogle Scholar
  74. 74.
    Quévrain E, Maubert MA, Michon C, et al. Identification of an anti-inflammatory protein from Faecalibacterium prausnitzii, a commensal bacterium deficient in Crohn’s disease. Gut. 2015. doi: 10.1136/gutjnl-2014-307649 [Epub ahead of print].Google Scholar
  75. 75.
    Nelson AM, Walk ST, Taube S, et al. Disruption of the human gut microbiota following norovirus infection. PLoS One. 2012;7:e48224.PubMedPubMedCentralCrossRefGoogle Scholar
  76. 76.
    Lupp C, Robertson ML, Wickham ME, et al. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe. 2007;2:119–29.PubMedCrossRefGoogle Scholar
  77. 77.
    Stecher B, Robbiani R, Walker AW, et al. Salmonella enterica serovar typhimurium exploits inflammation to compete with the intestinal microbiota. PLoS Biol. 2007;5:2177–89.PubMedCrossRefGoogle Scholar
  78. 78.
    Abraham C, Medzhitov R. Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology. 2011;140:1729–37.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    O’Hara JR, Feener TD, Fischer CD, et al. Campylobacter jejuni disrupts protective Toll-like receptor 9 signaling in colonic epithelial cells and increases the severity of dextran sulfate sodium-induced colitis in mice. Infect Immun. 2012;80:1563–71.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    McCormick BA, Nusrat A, Parkos CA, et al. Unmasking of intestinal epithelial lateral membrane beta1 integrin consequent to transepithelial neutrophil migration in vitro facilitates inv-mediated invasion by Yersinia pseudotuberculosis. Infect Immun. 1997;65:1414–21.PubMedPubMedCentralGoogle Scholar
  81. 81.
    Medzhitov R. Toll-like receptors and innate immunity. Nat Rev Immunol. 2001;1:135–45.PubMedCrossRefGoogle Scholar
  82. 82.
    Muza-Moons MM, Koutsouris A, Hecht G. Disruption of cell polarity by enteropathogenic Escherichia coli enables basolateral membrane proteins to migrate apically and to potentiate physiological consequences. Infect Immun. 2003;71:7069–78.PubMedPubMedCentralCrossRefGoogle Scholar
  83. 83.
    O’Hara JR, Buret AG. Mechanisms of intestinal tight junctional disruption during infection. Front Biosci. 2008;13:7008–21.PubMedGoogle Scholar
  84. 84.
    Kalischuk LD, Inglis GD, Buret AG. Strain-dependent induction of epithelial cell oncosis by Campylobacter jejuni is correlated with invasion ability and is independent of cytolethal distending toxin. Microbiology. 2007;153:2952–63.PubMedPubMedCentralCrossRefGoogle Scholar
  85. 85.
    Lamb-Rosteski JM, Kalischuk LD, Inglis GD, et al. Epidermal growth factor inhibits Campylobacter jejuni-induced claudin-4 disruption, loss of epithelial barrier function, and Escherichia coli translocation. Infect Immun. 2008;76:3390–8.PubMedPubMedCentralCrossRefGoogle Scholar
  86. 86.
    Kalischuk LD, Inglis GD, Buret AG. Campylobacter jejuni induces transcellular translocation of commensal bacteria via lipid rafts. Gut Pathog. 2009;1:2.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Kalischuk LD, Leggett F, Inglis GD. Campylobacter jejuni induces transcytosis of commensal bacteria across the intestinal epithelium through M-like cells. Gut Pathog. 2010;2:14.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Knoop KA, McDonald KG, Kulkarni DH, et al. Antibiotics promote inflammation through the translocation of native commensal colonic bacteria. Gut. 2015. doi: 10.1136/gutjnl-2014-309059 [Epub ahead of print].PubMedGoogle Scholar
  89. 89.
    Nazli A, Yang PC, Jury J, et al. Epithelia under metabolic stress perceive commensal bacteria as a threat. Am J Pathol. 2004;164:947–57.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Clark E, Hoare C, Tanianis-Hughes J, et al. Interferon gamma induces translocation of commensal Escherichia coli across gut epithelial cells via a lipid raft-mediated process. Gastroenterology. 2005;128:1258–67.PubMedCrossRefGoogle Scholar
  91. 91.
    Söderholm JD, Streutker C, Yang PC, et al. Increased epithelial uptake of protein antigens in the ileum of Crohn’s disease mediated by tumour necrosis factor alpha. Gut. 2004;53:1817–24.PubMedPubMedCentralCrossRefGoogle Scholar
  92. 92.
    Swidsinski A, Weber J, Loening-Baucke V, et al. Spatial organization and composition of the mucosal flora in patients with inflammatory bowel disease. J Clin Microbiol. 2005;43:3380–9.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Kamada N, Kim YG, Sham HP, et al. Regulated virulence controls the ability of a pathogen to compete with the gut microbiota. Science. 2012;336:1325–9.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Chen TL, Chen S, Wu HW, et al. Persistent gut barrier damage and commensal bacterial influx following eradication of Giardia infection in mice. Gut Pathog. 2013;5:26.PubMedPubMedCentralCrossRefGoogle Scholar
  95. 95.
    Halliez M, Motta JP, Feener T, et al. Giardia duodenalis induces bacterial translocation and causes post-infectious visceral hypersensitity. Am J Physiol. (Gastrointestinal and Liver Physiol.) 2016;310(8):G574–85.Google Scholar
  96. 96.
    Gerbaba TK, Gupta P, Rioux K, et al. Giardia duodenalis-induced alterations of commensal bacteria kill Caenorhabditis elegans: a new model to study microbial-microbial interactions in the gut. Am J Physiol Gastrointest Liver Physiol. 2015;308:G550–61.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Pham TA, Clare S, Goulding D, et al. Epithelial IL-22RA1-mediated fucosylation promotes intestinal colonization resistance to an opportunistic pathogen. Cell Host Microbe. 2014;16:504–16.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Goto Y, Obata T, Kunisawa J, et al. Innate lymphoid cells regulate intestinal epithelial cell glycosylation. Science. 2014;345:1254009.PubMedPubMedCentralCrossRefGoogle Scholar
  99. 99.
    Pickard JM, Maurice CF, Kinnebrew MA, et al. Rapid fucosylation of intestinal epithelium sustains host-commensal symbiosis in sickness. Nature. 2014;514:638–41.PubMedPubMedCentralCrossRefGoogle Scholar
  100. 100.
    DuPont AW, DuPont HL. The intestinal microbiota and chronic disorders of the gut. Nat Rev Gastoenterol Hepatol. 2011;8:523–31.CrossRefGoogle Scholar
  101. 101.
    Probert HM, Gibson GR. Bacterial biofilms in the human gastrointestinal tract. Curr Issues Intest Microbiol. 2002;3:23–7.PubMedGoogle Scholar
  102. 102.
    Pruteanu M, Hyland NP, Clarke DJ, et al. Degradation of the extracellular matrix components by bacterial-derived metalloproteases: implications for inflammatory bowel diseases. Inflamm Bowel Dis. 2010;17:1189–200.PubMedCrossRefGoogle Scholar
  103. 103.
    Spiller R, Campbell E. Post-infectious irritable bowel syndrome. Curr Opin Gastroenterol. 2006;22:13–7.PubMedCrossRefGoogle Scholar
  104. 104.
    Hanevik K, Dizdar V, Langeland N, et al. Development of functional gastrointestinal disorders after Giardia lamblia infection. BMC Gastroenterol. 2009;9:27.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Marshall JK, Thabane M, Garg AX, et al. Eight year prognosis of postinfectious irritable bowel syndrome following waterborne bacterial dysentery. Gut. 2010;59:605–11.PubMedCrossRefGoogle Scholar
  106. 106.
    Wensaas KA, Langeland N, Hanevik K, et al. Irritable bowel syndrome and chronic fatigue 3 years after acute giardiasis: historic cohort study. Gut. 2012;61:214–9.PubMedCrossRefGoogle Scholar
  107. 107.
    Cremon C, Stanghellini V, Pallotti F, et al. Salmonella gastroenteritis during childhood is a risk factor for irritable bowel syndrome in adulthood. Gastroenterology. 2014;147:69–103.PubMedCrossRefGoogle Scholar
  108. 108.
    Ceri H, Olson ME, Stremick C, et al. The Calgary Biofilm Device: a new technology for the rapid determination of antibiotic susceptibility of bacterial biofilms. J Clin Microbiol. 1999;37:1771–6.PubMedPubMedCentralGoogle Scholar
  109. 109.
    Sproule-Willoughby KM, Stanton MM, Rioux KP, et al. In vitro anaerobic biofilms of human colonic microbiota. J Microbiol Methods. 2010;83:296–301.PubMedCrossRefGoogle Scholar
  110. 110.
    Beatty J, Akierman S, Rioux K, et al. Gut microbiota biofilm disruptions by Giardia: pathology in human enterocytes and germ-free mice. FASEB J 2013;27 [abstract 131.1].Google Scholar
  111. 111.
    Buret AG, Akierman S, Feener T, et al. Campylobacter jejuni or Giardia duodenalis-mediated disruptions of human intestinal microbiota biofilms: novel mechanisms producing post-infectious intestinal inflammatory disorders. Gastroenterology. 2013;144:S–309 [abstract Sa1802].CrossRefGoogle Scholar
  112. 112.
    Reti KL, Tymensen LD, Davis Sp, et al. Campylobacter jejuni increases flagellar expression and adhesion of non-invasive Escherichia coli: effects on enterocytic TLR4 and CXCL8 expression. Infect Immun. 2015;83(12):4571–4581.Google Scholar

Copyright information

© Springer International Publishing AG 2016

Authors and Affiliations

  1. 1.Department of Biological SciencesInflammation Research Network and Host-Parasite Interaction NSERC-CREATE Program, University of CalgaryAlbertaCanada

Personalised recommendations