iBet uBet web content aggregator. Adding the entire web to your favor.
iBet uBet web content aggregator. Adding the entire web to your favor.



Link to original content: https://doi.org/10.1007/s10620-014-3350-9
Environmental Risk Factors for Inflammatory Bowel Diseases: A Review | Digestive Diseases and Sciences Skip to main content

Advertisement

Springer Nature Link
Log in

Environmental Risk Factors for Inflammatory Bowel Diseases: A Review

  • Review
  • Published:
Digestive Diseases and Sciences Aims and scope Submit manuscript

Abstract

Inflammatory bowel diseases comprising Crohn’s disease (CD) and ulcerative colitis (UC) are chronic immunologically mediated diseases. The key mechanism underlying the pathogenesis of these diseases is a dysregulated immune response to commensal flora in a genetically susceptible host. Thus intestinal microbial dysbiosis, host genetics, and the external environment all play an important role in the development of incident disease and in determining subsequent disease behavior and outcomes. There are several well-defined or putative environmental risk factors including cigarette smoking, appendectomy, diet, stress and depression, vitamin D as well as hormonal influence. The effect of some of the risk factors appears to differ between CD and UC suggesting that despite shared genetic and immunologic mechanisms, distinct pathways of pathogenesis exist. There is a growing body of literature identifying risk factors for incident disease. There is less rigorous literature defining triggers of relapse, and few controlled clinical trials examining if modification of such risk factors results in an improvement in patient outcomes. This is an area of considerable patient, physician, and scientific interest, and there is an important unmet need for rigorous studies of the external environment in disease pathogenesis and subsequent course.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Abraham C, Cho JH. Inflammatory bowel disease. N Engl J Med. 2009;361:2066–2078.

    CAS  PubMed Central  PubMed  Google Scholar 

  2. Cosnes J, Gower-Rousseau C, Seksik P, et al. Epidemiology and natural history of inflammatory bowel diseases. Gastroenterology. 2011;140:1785–1794.

    PubMed  Google Scholar 

  3. Bernstein CN, Loftus EV Jr, Ng SC, et al. Hospitalisations and surgery in Crohn’s disease. Gut. 2012;61:622–629.

    PubMed  Google Scholar 

  4. Khor B, Gardet A, Xavier RJ. Genetics and pathogenesis of inflammatory bowel disease. Nature. 2011;474:307–317.

    CAS  PubMed Central  PubMed  Google Scholar 

  5. Gevers D, Kugathasan S, Denson LA, et al. The treatment-naive microbiome in new-onset Crohn’s disease. Cell Host Microbe. 2014;15:382–392.

    CAS  PubMed  Google Scholar 

  6. Kostic AD, Xavier RJ, Gevers D. The microbiome in inflammatory bowel disease: current status and the future ahead. Gastroenterology. 2014;146:1489–1499.

    CAS  PubMed  Google Scholar 

  7. Morgan XC, Tickle TL, Sokol H, et al. Dysfunction of the intestinal microbiome in inflammatory bowel disease and treatment. Genome Biol. 2012;13:R79.

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Martin R, Chain F, Miquel S, et al. The commensal bacterium Faecalibacterium prausnitzii is protective in DNBS-induced chronic moderate and severe colitis models. Inflamm Bowel Dis. 2014;20:417–430.

    PubMed  Google Scholar 

  9. 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 USA. 2008;105:16731–16736.

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Darfeuille-Michaud A, Boudeau J, Bulois P, et al. High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology. 2004;127:412–421.

    PubMed  Google Scholar 

  11. Jostins L, Ripke S, Weersma RK, et al. Host-microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature. 2012;491:119–124.

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Molodecky NA, Soon IS, Rabi DM, et al. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 2012;142:46–54 e42; quiz e30.

  13. Thia KT, Loftus EV Jr, Sandborn WJ, et al. An update on the epidemiology of inflammatory bowel disease in Asia. Am J Gastroenterol. 2008;103:3167–3182.

    PubMed  Google Scholar 

  14. Birrenbach T, Bocker U. Inflammatory bowel disease and smoking: a review of epidemiology, pathophysiology, and therapeutic implications. Inflamm Bowel Dis. 2004;10:848–859.

    PubMed  Google Scholar 

  15. Cosnes J. Tobacco and IBD: relevance in the understanding of disease mechanisms and clinical practice. Best Pract Res Clin Gastroenterol. 2004;18:481–496.

    CAS  PubMed  Google Scholar 

  16. Cosnes J. What is the link between the use of tobacco and IBD? Inflamm Bowel Dis. 2008;14(Suppl 2):S14–S15.

    PubMed  Google Scholar 

  17. Cosnes J, Carbonnel F, Beaugerie L, et al. Effects of cigarette smoking on the long-term course of Crohn’s disease. Gastroenterology. 1996;110:424–431.

    CAS  PubMed  Google Scholar 

  18. Cosnes J, Carbonnel F, Carrat F, et al. Effects of current and former cigarette smoking on the clinical course of Crohn’s disease. Aliment Pharmacol Ther. 1999;13:1403–1411.

    CAS  PubMed  Google Scholar 

  19. Mahid SS, Minor KS, Soto RE, et al. Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clin Proc. 2006;81:1462–1471.

    PubMed  Google Scholar 

  20. Higuchi LM, Khalili H, Chan AT, et al. A prospective study of cigarette smoking and the risk of inflammatory bowel disease in women. Am J Gastroenterol. 2012;107:1399–1406.

    PubMed Central  PubMed  Google Scholar 

  21. Beaugerie L, Massot N, Carbonnel F, et al. Impact of cessation of smoking on the course of ulcerative colitis. Am J Gastroenterol. 2001;96:2113–2116.

    CAS  PubMed  Google Scholar 

  22. Persson PG, Hellers G, Ahlbom A. Use of oral moist snuff and inflammatory bowel disease. Int J Epidemiol. 1993;22:1101–1103.

    CAS  PubMed  Google Scholar 

  23. van der Heide F, Dijkstra A, Weersma RK, et al. Effects of active and passive smoking on disease course of Crohn’s disease and ulcerative colitis. Inflamm Bowel Dis. 2009;15:1199–1207.

    PubMed  Google Scholar 

  24. Bergeron V, Grondin V, Rajca S, et al. Current smoking differentially affects blood mononuclear cells from patients with Crohn’s disease and ulcerative colitis: relevance to its adverse role in the disease. Inflamm Bowel Dis. 2012;18:1101–1111.

    PubMed  Google Scholar 

  25. Andersson RE, Olaison G, Tysk C, et al. Appendectomy and protection against ulcerative colitis. N Engl J Med. 2001;344:808–814.

    CAS  PubMed  Google Scholar 

  26. Jackson HT, Mongodin EF, Davenport KP, et al. Culture-independent evaluation of the appendix and rectum microbiomes in children with and without appendicitis. PLoS One. 2014;9:e95414.

    PubMed Central  PubMed  Google Scholar 

  27. Swidsinski A, Dorffel Y, Loening-Baucke V, et al. Acute appendicitis is characterised by local invasion with Fusobacterium nucleatum/necrophorum. Gut. 2011;60:34–40.

    PubMed  Google Scholar 

  28. Zhong D, Brower-Sinning R, Firek B, et al. Acute appendicitis in children is associated with an abundance of bacteria from the phylum Fusobacteria. J Pediatr Surg. 2014;49:441–446.

    PubMed  Google Scholar 

  29. Hallas J, Gaist D, Vach W, et al. Appendicectomy has no beneficial effect on admission rates in patients with ulcerative colitis. Gut. 2004;53:351–354.

    CAS  PubMed Central  PubMed  Google Scholar 

  30. Okazaki K, Onodera H, Watanabe N, et al. A patient with improvement of ulcerative colitis after appendectomy. Gastroenterology. 2000;119:502–506.

    CAS  PubMed  Google Scholar 

  31. Radford-Smith GL, Edwards JE, Purdie DM, et al. Protective role of appendicectomy on onset and severity of ulcerative colitis and Crohn’s disease. Gut. 2002;51:808–813.

    CAS  PubMed Central  PubMed  Google Scholar 

  32. Zallot C, Quilliot D, Chevaux JB, et al. Dietary beliefs and behavior among inflammatory bowel disease patients. Inflamm Bowel Dis (2012).

  33. Cabre E, Domenech E. Impact of environmental and dietary factors on the course of inflammatory bowel disease. World J Gastroenterol. 2012;18:3814–3822.

    CAS  PubMed Central  PubMed  Google Scholar 

  34. Chapman-Kiddell CA, Davies PS, Gillen L, et al. Role of diet in the development of inflammatory bowel disease. Inflamm Bowel Dis. 2010;16:137–151.

    PubMed  Google Scholar 

  35. Hou JK, Abraham B, El-Serag H. Dietary intake and risk of developing inflammatory bowel disease: a systematic review of the literature. Am J Gastroenterol. 2011;106:563–573.

    CAS  PubMed  Google Scholar 

  36. Ananthakrishnan AN, Khalili H, Konijeti GG, et al. A prospective study of long-term intake of dietary fiber and risk of Crohn’s disease and ulcerative colitis. Gastroenterology. 2013;145:907–917.

    Google Scholar 

  37. Amre DK, D’Souza S, Morgan K, et al. Imbalances in dietary consumption of fatty acids, vegetables, and fruits are associated with risk for Crohn’s disease in children. Am J Gastroenterol. 2007;102:2016–2025.

    CAS  PubMed  Google Scholar 

  38. Roberts CL, Keita AV, Duncan SH, et al. Translocation of Crohn’s disease Escherichia coli across M-cells: contrasting effects of soluble plant fibres and emulsifiers. Gut. 2010;59:1331–1339.

    PubMed Central  PubMed  Google Scholar 

  39. Monteleone I, MacDonald TT, Pallone F, et al. The aryl hydrocarbon receptor in inflammatory bowel disease: linking the environment to disease pathogenesis. Curr Opin Gastroenterol. 2012;28:310–313.

    CAS  PubMed  Google Scholar 

  40. Kiss EA, Vonarbourg C, Kopfmann S, et al. Natural aryl hydrocarbon receptor ligands control organogenesis of intestinal lymphoid follicles. Science. 2011;334:1561–1565.

    CAS  PubMed  Google Scholar 

  41. Buonocore S, Ahern PP, Uhlig HH, et al. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature. 2010;464:1371–1375.

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Ananthakrishnan AN, Khalili H, Konijeti GG, et al. Long-term intake of dietary fat and risk of ulcerative colitis and Crohn’s disease. Gut. 2014;63:776–784.

    CAS  PubMed  Google Scholar 

  43. Jantchou P, Morois S, Clavel-Chapelon F, et al. Animal protein intake and risk of inflammatory bowel disease: The E3N prospective study. Am J Gastroenterol. 2010;105:2195–2201.

    CAS  PubMed  Google Scholar 

  44. Wu GD, Chen J, Hoffmann C, et al. Linking long-term dietary patterns with gut microbial enterotypes. Science. 2011;334:105–108.

    CAS  PubMed Central  PubMed  Google Scholar 

  45. Muegge BD, Kuczynski J, Knights D, et al. Diet drives convergence in gut microbiome functions across mammalian phylogeny and within humans. Science. 2011;332:970–974.

    CAS  PubMed Central  PubMed  Google Scholar 

  46. 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 USA. 2010;107:14691–14696.

    PubMed Central  PubMed  Google Scholar 

  47. David LA, Maurice CF, Carmody RN, et al. Diet rapidly and reproducibly alters the human gut microbiome. Nature. 2014;505:559–563.

    CAS  PubMed Central  PubMed  Google Scholar 

  48. Devkota S, Wang Y, Musch MW, et al. Dietary-fat-induced taurocholic acid promotes pathobiont expansion and colitis in Il10−/− mice. Nature. 2012;487:104–108.

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Huang EY, Leone VA, Devkota S, et al. Composition of dietary fat source shapes gut microbiota architecture and alters host inflammatory mediators in mouse adipose tissue. JPEN J Parenter Enteral Nutr. 2013;37:746–754.

    CAS  PubMed  Google Scholar 

  50. Cohen AB, Lee D, Long MD, et al. Dietary patterns and self-reported associations of diet with symptoms of inflammatory bowel disease. Dig Dis Sci. 2013;58:1322–1328.

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Cantorna MT, Mahon BD. D-hormone and the immune system. J Rheumatol Suppl. 2005;76:11–20.

    CAS  PubMed  Google Scholar 

  52. Cantorna MT, Mahon BD. Mounting evidence for vitamin D as an environmental factor affecting autoimmune disease prevalence. Exp Biol Med (Maywood). 2004;229:1136–1142.

    CAS  Google Scholar 

  53. Cantorna MT, Zhu Y, Froicu M, et al. Vitamin D status, 1,25-dihydroxyvitamin D3, and the immune system. Am J Clin Nutr. 2004;80:1717S–1720S.

    CAS  PubMed  Google Scholar 

  54. Khalili H, Huang ES, Ananthakrishnan AN, et al. Geographical variation and incidence of inflammatory bowel disease among US women. Gut. 2012.

  55. Ananthakrishnan AN, Khalili H, Higuchi LM, et al. Higher predicted vitamin d status is associated with reduced risk of Crohn’s disease. Gastroenterology. 2012;142:482–489.

    CAS  PubMed Central  PubMed  Google Scholar 

  56. Ananthakrishnan AN, Cagan A, Gainer VS, et al. Normalization of plasma 25-hydroxy vitamin D is associated with reduced risk of surgery in Crohn’s disease. Inflamm Bowel Dis. 2013;19:1921–1927.

    PubMed Central  PubMed  Google Scholar 

  57. Cantorna MT, Munsick C, Bemiss C, et al. 1,25-Dihydroxycholecalciferol prevents and ameliorates symptoms of experimental murine inflammatory bowel disease. J Nutr. 2000;130:2648–2652.

    CAS  PubMed  Google Scholar 

  58. Ananthakrishnan AN, Cagan A, Gainer VS, et al. Higher plasma vitamin D is associated with reduced risk of Clostridium difficile infection in patients with inflammatory bowel diseases. Aliment Pharmacol Ther. 2014;39:1136–1142.

    CAS  PubMed  Google Scholar 

  59. Ananthakrishnan AN, Cheng SC, Cai T, et al. Association between reduced plasma 25-hydroxy vitamin D and increased risk of cancer in patients with inflammatory bowel diseases. Clin Gastroenterol Hepatol. 2014;12:821–827.

    CAS  PubMed  Google Scholar 

  60. Jorgensen SP, Agnholt J, Glerup H, et al. Clinical trial: vitamin D3 treatment in Crohn’s disease—a randomized double-blind placebo-controlled study. Aliment Pharmacol Ther. 2010;32:377–383.

    CAS  PubMed  Google Scholar 

  61. Bernstein CN, Singh S, Graff LA, et al. A prospective population-based study of triggers of symptomatic flares in IBD. Am J Gastroenterol. 2010;105:1994–2002.

    PubMed  Google Scholar 

  62. Bitton A, Dobkin PL, Edwardes MD, et al. Predicting relapse in Crohn’s disease: a biopsychosocial model. Gut. 2008;57:1386–1392.

    CAS  PubMed  Google Scholar 

  63. Camara RJ, Schoepfer AM, Pittet V, et al. Mood and nonmood components of perceived stress and exacerbation of Crohn’s disease. Inflamm Bowel Dis. 2011;17:2358–2365.

    PubMed  Google Scholar 

  64. Goodhand JR, Wahed M, Mawdsley JE, et al. Mood disorders in inflammatory bowel disease: relation to diagnosis, disease activity, perceived stress, and other factors. Inflamm Bowel Dis. 2012;18:2301–2309.

    CAS  PubMed  Google Scholar 

  65. Lerebours E, Gower-Rousseau C, Merle V, et al. Stressful life events as a risk factor for inflammatory bowel disease onset: a population-based case-control study. Am J Gastroenterol. 2007;102:122–131.

    PubMed  Google Scholar 

  66. Levenstein S, Prantera C, Varvo V, et al. Stress and exacerbation in ulcerative colitis: a prospective study of patients enrolled in remission. Am J Gastroenterol. 2000;95:1213–1220.

    CAS  PubMed  Google Scholar 

  67. Levenstein S, Prantera C, Varvo V, et al. Psychological stress and disease activity in ulcerative colitis: a multidimensional cross-sectional study. Am J Gastroenterol. 1994;89:1219–1225.

    CAS  PubMed  Google Scholar 

  68. Li J, Norgard B, Precht DH, et al. Psychological stress and inflammatory bowel disease: a follow-up study in parents who lost a child in Denmark. Am J Gastroenterol. 2004;99:1129–1133.

    PubMed  Google Scholar 

  69. Maunder RG. Evidence that stress contributes to inflammatory bowel disease: evaluation, synthesis, and future directions. Inflamm Bowel Dis. 2005;11:600–608.

    PubMed  Google Scholar 

  70. Mawdsley JE, Rampton DS. Psychological stress in IBD: new insights into pathogenic and therapeutic implications. Gut. 2005;54:1481–1491.

    CAS  PubMed Central  PubMed  Google Scholar 

  71. Rampton DS. The influence of stress on the development and severity of immune-mediated diseases. J Rheumatol Suppl. 2011;88:43–47.

    PubMed  Google Scholar 

  72. Singh S, Graff LA, Bernstein CN. Do NSAIDs, antibiotics, infections, or stress trigger flares in IBD? Am J Gastroenterol. 2009;104:1298–1313; quiz 1314.

  73. Ananthakrishnan AN, Khalili H, Pan A, et al. Association between depressive symptoms and incidence of crohn’s disease and ulcerative colitis—results from the nurses’ health study. Clin Gastroenterol Hepatol. 2012;11:57–62.

    PubMed Central  PubMed  Google Scholar 

  74. Ananthakrishnan AN, Gainer VS, Perez RG, et al. Psychiatric co-morbidity is associated with increased risk of surgery in Crohn’s disease. Aliment Pharmacol Ther. 2013;37:445–454.

    CAS  PubMed Central  PubMed  Google Scholar 

  75. Ghia JE, Blennerhassett P, Deng Y, et al. Reactivation of inflammatory bowel disease in a mouse model of depression. Gastroenterology. 2009;136(2280–2288):e1–e4.

    PubMed  Google Scholar 

  76. Sun Y, Zhang M, Chen CC, et al. Stress-induced corticotropin-releasing hormone-mediated NLRP6 inflammasome inhibition and transmissible enteritis in mice. Gastroenterology. 2013;144:1478–1487, 1487 e1–8.

  77. Bailey MT, Dowd SE, Galley JD, et al. Exposure to a social stressor alters the structure of the intestinal microbiota: implications for stressor-induced immunomodulation. Brain Behav Immun. 2011;25:397–407.

    CAS  PubMed Central  PubMed  Google Scholar 

  78. Ananthakrishnan AN, Long MD, Martin CF, et al. Sleep disturbance and risk of active disease in patients with Crohn’s disease and ulcerative colitis. Clin Gastroenterol Hepatol. 2013;11:965–971.

    PubMed Central  PubMed  Google Scholar 

  79. Shaw SY, Blanchard JF, Bernstein CN. Association between the use of antibiotics in the first year of life and pediatric inflammatory bowel disease. Am J Gastroenterol. 2010;105:2687–2692.

    PubMed  Google Scholar 

  80. Shaw SY, Blanchard JF, Bernstein CN. Association between the use of antibiotics and new diagnoses of Crohn’s disease and ulcerative colitis. Am J Gastroenterol. 2011;106:2133–2142.

    PubMed  Google Scholar 

  81. Kronman MP, Zaoutis TE, Haynes K, et al. Antibiotic exposure and IBD development among children: a population-based cohort study. Pediatrics. 2012;130:e794–e803.

    PubMed Central  PubMed  Google Scholar 

  82. Ananthakrishnan AN, Higuchi LM, Huang ES, et al. Aspirin, nonsteroidal anti-inflammatory drug use, and risk for crohn disease and ulcerative colitis: a cohort study. Ann Intern Med. 2012;156:350–359.

    PubMed Central  PubMed  Google Scholar 

  83. Khalili H, Higuchi LM, Ananthakrishnan AN, et al. Oral contraceptives, reproductive factors and risk of inflammatory bowel disease. Gut. 2013;62:1153–1159.

    CAS  PubMed Central  PubMed  Google Scholar 

  84. Khalili H, Higuchi LM, Ananthakrishnan AN, et al. Hormone therapy increases risk of ulcerative colitis but not crohn’s disease. Gastroenterology. 2012;143:1199–1206.

    CAS  PubMed Central  PubMed  Google Scholar 

  85. Ananthakrishnan AN, Issa M, Binion DG. Clostridium difficile and inflammatory bowel disease. Gastroenterol Clin North Am. 2009;38:711–728.

    PubMed  Google Scholar 

  86. Ananthakrishnan AN, McGinley EL, Binion DG. Excess hospitalisation burden associated with Clostridium difficile in patients with inflammatory bowel disease. Gut. 2008;57:205–210.

    CAS  PubMed  Google Scholar 

  87. Gradel KO, Nielsen HL, Schonheyder HC, et al. Increased short- and long-term risk of inflammatory bowel disease after salmonella or campylobacter gastroenteritis. Gastroenterology. 2009;137:495–501.

    PubMed  Google Scholar 

  88. Jess T, Simonsen J, Nielsen NM, et al. Enteric Salmonella or Campylobacter infections and the risk of inflammatory bowel disease. Gut. 2011;60:318–324.

    PubMed  Google Scholar 

  89. Garcia Rodriguez LA, Ruigomez A, Panes J. Acute gastroenteritis is followed by an increased risk of inflammatory bowel disease. Gastroenterology. 2006;130:1588–1594.

    PubMed  Google Scholar 

  90. Ananthakrishnan AN, McGinley EL, Binion DG, et al. Ambient air pollution correlates with hospitalizations for inflammatory bowel disease: an ecologic analysis. Inflamm Bowel Dis. 2011;17:1138–1145.

    PubMed  Google Scholar 

  91. Kaplan GG, Hubbard J, Korzenik J, et al. The inflammatory bowel diseases and ambient air pollution: a novel association. Am J Gastroenterol. 2010;105:2412–2419.

    CAS  PubMed Central  PubMed  Google Scholar 

  92. Khalili H, Ananthakrishnan AN, Konijeti GG, et al. Physical activity and risk of inflammatory bowel disease: prospective study from the Nurses’ Health Study cohorts. BMJ. 2013;347:f6633.

    PubMed Central  PubMed  Google Scholar 

  93. Lawrance IC, Murray K, Batman B, et al. Crohn’s disease and smoking: is it ever too late to quit? J Crohns Colitis. 2013;7:e665–e671.

    PubMed  Google Scholar 

  94. Nunes T, Etchevers MJ, Merino O, et al. High smoking cessation rate in Crohn’s disease patients after physician advice–the TABACROHN Study. J Crohns Colitis. 2013;7:202–207.

    PubMed  Google Scholar 

  95. Cosnes J, Beaugerie L, Carbonnel F, et al. Smoking cessation and the course of Crohn’s disease: an intervention study. Gastroenterology. 2001;120:1093–1099.

    CAS  PubMed  Google Scholar 

  96. Feagan BG, Sandborn WJ, Mittmann U, et al. Omega-3 free fatty acids for the maintenance of remission in Crohn disease: the EPIC Randomized Controlled Trials. JAMA. 2008;299:1690–1697.

    CAS  PubMed  Google Scholar 

  97. Cabre E, Manosa M, Gassull MA. Omega-3 fatty acids and inflammatory bowel diseases—a systematic review. Br J Nutr. 2012;107(Suppl 2):S240–S252.

    CAS  PubMed  Google Scholar 

  98. Lee J, Allen R, Ashley S, et al. British Dietetic Association evidence-based guidelines for the dietary management of Crohn’s disease in adults. J Hum Nutr Diet 2013.

  99. Zachos M, Tondeur M, Griffiths AM. Enteral nutritional therapy for induction of remission in Crohn’s disease. Cochrane Database Syst Rev. 2007:CD000542.

  100. Suskind DL, Wahbeh G, Gregory N, et al. Nutritional therapy in pediatric Crohn disease: the specific carbohydrate diet. J Pediatr Gastroenterol Nutr. 2014;58:87–91.

    CAS  PubMed  Google Scholar 

  101. Wahed M, Corser M, Goodhand JR, et al. Does psychological counseling alter the natural history of inflammatory bowel disease? Inflamm Bowel Dis. 2010;16:664–669.

    PubMed  Google Scholar 

  102. Goodhand JR, Greig FI, Koodun Y, et al. Do antidepressants influence the disease course in inflammatory bowel disease? A retrospective case-matched observational study. Inflamm Bowel Dis. 2012;18:1232–1239.

    CAS  PubMed  Google Scholar 

  103. Boye B, Lundin KE, Jantschek G, et al. INSPIRE study: does stress management improve the course of inflammatory bowel disease and disease-specific quality of life in distressed patients with ulcerative colitis or Crohn’s disease? A randomized controlled trial. Inflamm Bowel Dis. 2011;17:1863–1873.

    PubMed  Google Scholar 

  104. Ananthakrishnan AN, Nguyen DD, Sauk J, et al. Genetic polymorphisms in metabolizing enzymes modifying the association between smoking and inflammatory bowel diseases. Inflamm Bowel Dis. 2014;20:783–789.

    PubMed  Google Scholar 

  105. Costea I, Mack DR, Lemaitre RN, et al. Interactions between the dietary polyunsaturated fatty acid ratio and genetic factors determine susceptibility to pediatric Crohn’s disease. Gastroenterology. 2014;146:929–931.

    CAS  PubMed  Google Scholar 

  106. Nagalingam NA, Lynch SV. Role of the microbiota in inflammatory bowel diseases. Inflamm Bowel Dis. 2012;18:968–984.

    PubMed  Google Scholar 

  107. Albenberg LG, Wu GD. Diet and the intestinal microbiome: associations, functions, and implications for health and disease. Gastroenterology. 2014.

  108. D’Argenio V, Precone V, Casaburi G, et al. An altered gut microbiome profile in a child affected by Crohn’s disease normalized after nutritional therapy. Am J Gastroenterol. 2013;108:851–852.

    PubMed Central  PubMed  Google Scholar 

  109. Benjamin JL, Hedin CR, Koutsoumpas A, et al. Smokers with active Crohn’s disease have a clinically relevant dysbiosis of the gastrointestinal microbiota. Inflamm Bowel Dis. 2012;18:1092–1100.

    PubMed  Google Scholar 

  110. Cadwell K, Patel KK, Maloney NS, et al. Virus-plus-susceptibility gene interaction determines Crohn’s disease gene Atg16L1 phenotypes in intestine. Cell. 2010;141:1135–1145.

    CAS  PubMed Central  PubMed  Google Scholar 

Download references

Acknowledgments

A.N.A is supported by funding from the US National Institutes of Health (K23 DK097142).

Conflict of interest

None.

Author information

Authors and Affiliations

  1. Division of Gastroenterology, Massachusetts General Hospital Crohn’s and Colitis Center and Harvard Medical School, 165 Cambridge Street, 9th Floor, Boston, MA, 02114, USA

    Ashwin N. Ananthakrishnan

Authors
  1. Ashwin N. Ananthakrishnan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Ashwin N. Ananthakrishnan.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ananthakrishnan, A.N. Environmental Risk Factors for Inflammatory Bowel Diseases: A Review. Dig Dis Sci 60, 290–298 (2015). https://doi.org/10.1007/s10620-014-3350-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10620-014-3350-9

Keywords

Search

Navigation