Original Contribution | Published:

Inflammatory Bowel Disease

Animal Protein Intake and Risk of Inflammatory Bowel Disease: The E3N Prospective Study

The American Journal of Gastroenterology volume 105, pages 21952201 (2010) | Download Citation

Abstract

OBJECTIVES:

Diet composition has long been suspected to contribute to inflammatory bowel disease (IBD), but has not been thoroughly assessed, and has been assessed only in retrospective studies that are prone to recall bias. The aim of the present study was to evaluate the role of dietary macronutrients in the etiology of IBD in a large prospective cohort.

METHODS:

The Etude Épidémiologique des femmes de la Mutuelle Générale de l’Education Nationale cohort consists of women living in France, aged 40–65 years, and free of major diseases at inclusion. A self-administered questionnaire was used to record dietary habits at baseline. Questionnaires on disease occurrence and lifestyle factors were completed every 24 months. IBDs were assessed in each questionnaire until June 2005, and subsequently validated using clinical and pathological criteria. We estimated the association between nutrients or foods and IBD using Cox proportional hazards models adjusted for energy intake.

RESULTS:

Among 67,581 participants (705,445 person-years, mean follow-up since completion of the baseline dietary questionnaire 10.4 years), we validated 77 incident IBD cases. High total protein intake, specifically animal protein, was associated with a significantly increased risk of IBD, (hazards ratio for the third vs. first tertile and 95% confidence interval being 3.31 and 1.41–7.77 (P trend=0.007), and 3.03 and 1.45–6.34 (P trend=0.005) for total and animal protein, respectively). Among sources of animal protein, high consumption of meat or fish but not of eggs or dairy products was associated with IBD risk.

CONCLUSIONS:

High protein intake is associated with an increased risk of incident IBD in French middle-aged women.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    . Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat Clin Pract Gastroenterol Hepatol 2006;3:390–407.

  2. 2.

    , . Inflammatory bowel disease: cause and immunobiology. Lancet 2007;369:1627–1640.

  3. 3.

    . The genetics and immunopathogenesis of inflammatory bowel disease. Nat Rev Immunol 2008;8:458–466.

  4. 4.

    Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 2007;447:661–678.

  5. 5.

    . Epidemiology of IBD during the twentieth century: an integrated view. Best Pract Res Clin Gastroenterol 2004;18:463–479.

  6. 6.

    , . The effects of migration on ulcerative colitis: a three-year prospective study among Europeans and first- and second-generation South Asians in Leicester (1991–1994). Am J Gastroenterol 1999;94:2918–2922.

  7. 7.

    , , et al. Incidence of inflammatory bowel disease is rising and abdominal tuberculosis is falling in Bangladeshis in East London, United Kingdom. Am J Gastroenterol 2004;99:1749–1755.

  8. 8.

    , , . Environmental risk factors in Crohn’s disease and ulcerative colitis (excluding tobacco and appendicectomy). Gastroenterol Clin Biol 2006;30:859–867.

  9. 9.

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

  10. 10.

    , , . Diet and inflammatory bowel disease: a case-control study. Epidemiology 1992;3:47–52.

  11. 11.

    , , et al. Pre-illness dietary factors in inflammatory bowel disease. Gut 1997;40:754–760.

  12. 12.

    , , et al. Dietary risk factors for inflammatory bowel disease: a multicenter case-control study in Japan. Inflamm Bowel Dis 2005;11:154–163.

  13. 13.

    . Environmental risk factors (excluding tobacco and microorganisms): a critical analysis of old and new hypotheses. Best Pract Res Clin Gastroenterol 2004;18:497–508.

  14. 14.

    , , et al. E3N, a French cohort study on cancer risk factors. Eur J Cancer Prev 1997;6:473–478.

  15. 15.

    , , et al. Relative validity and reproducibility of a French dietary history questionnaire. Int J Epidemiol 1997;26 (Suppl 1): S128–S136.

  16. 16.

    , , . Re: “Total energy intake: implications for epidemiologic analyses”. Am J Epidemiol 1986;124:157–9.

  17. 17.

    , . Introduction to stratified analysis. In: Rothman KJ, Greenland S (eds). Modern Epidemiology, 2nd edn. Lippincott-Raven: Philadelphia, PA, 1998, pp. 53–79.

  18. 18.

    AFSSA. Guidelines on protein: quality, intake, nutritional need and recommendations (accessed october 25, 2009, at ).

  19. 19.

    , , et al. Geographical variations of inflammatory bowel disease in France: a study based on national health insurance data. Inflamm Bowel Dis 2006;12:218–226.

  20. 20.

    , , et al. Incidence of inflammatory bowel disease in northern France (1988–1990). Gut 1994;35:1433–1438.

  21. 21.

    et al. Linoleic Acid, a dietary N-6 polyunsaturated fatty acid, and the aetiology of ulcerative colitis—a European prospective cohort study. Gut 2009;58:1606–1611.

  22. 22.

    , , et al. Reproducibility of a food-frequency questionnaire and stability of dietary habits determined from five annually repeated measurements. Eur J Clin Nut 1995;49:420–429.

  23. 23.

    , , et al. Epidemiologic analysis of Crohn disease in Japan: increased dietary intake of n-6 polyunsaturated fatty acids and animal protein relates to the increased incidence of Crohn disease in Japan. Am J Clin Nutr 1996;63:741–745.

  24. 24.

    . Protein consumption: which place for beef (Accessed october 25, 2009, at ).

  25. 25.

    . Animal source foods and human health during evolution. J Nutr 2003;133:3893S–3897S.

  26. 26.

    , , et al. A case-control study of drinking water and dairy products in Crohn's Disease; further investigation of the possible role of Mycobacterium avium paratuberculosis. Am J Epidemiol 2007;165:776–783.

  27. 27.

    , , et al. Influence of dietary factors on the clinical course of ulcerative colitis: a prospective cohort study. Gut 2004;53:1479–1484.

  28. 28.

    , , et al. Diet in the aetiology of ulcerative colitis: a European prospective cohort study. Digestion 2008;77:57–64.

  29. 29.

    , , . Protein degradation in the large intestine: relevance to colorectal cancer. Curr Issues Intest Microbiol 2000;1:51–58.

  30. 30.

    . Review article: nitric oxide from dysbiotic bacterial respiration of nitrate in the pathogenesis and as a target for therapy of ulcerative colitis. Alim Pharmacol Ther 2008;27:531–541.

  31. 31.

    , , et al. Influence of dietary protein supplements on the formation of bacterial metabolites in the colon. Gut 1997;41:70–76.

  32. 32.

    , , et al. Major dietary patterns are related to plasma concentrations of markers of inflammation and endothelial dysfunction. Am J Clin Nutr 2004;80:1029–1035.

Download references

Acknowledgements

The authors are indebted to all the women of the cohort for providing the data. They are grateful to the physicians and gastroenterologists for providing the clinical, endoscopy, and pathology reports, and also to Lyan Hoang, Marie Fangon, Maryvonne Niravong, and Celine Kernaleguen for their technical assistance and Ms Pamela Albert for English assistance.

Author information

Affiliations

  1. INSERM, UMRS 1018, Team 9, Centre for Research in Epidemiology and Population Health, Institut Gustave Roussy, Université Paris Sud, Villejuif Cedex, France

    • Prévost Jantchou
    • , Sophie Morois
    • , Françoise Clavel-Chapelon
    • , Marie-Christine Boutron-Ruault
    •  & Franck Carbonnel
  2. Service d’Hépatogastroentérologie, Centre Hospitalier Universitaire de Bicêtre, Assistance Publique-Hôpitaux de Paris, Université Paris Sud, Le Kremlin Bicêtre, France

    • Franck Carbonnel

Authors

  1. Search for Prévost Jantchou in:

  2. Search for Sophie Morois in:

  3. Search for Françoise Clavel-Chapelon in:

  4. Search for Marie-Christine Boutron-Ruault in:

  5. Search for Franck Carbonnel in:

Competing interests

Guarantor of the article: Franck Carbonnel, MD, PhD.

Specific author contributions: Prévost Jantchou contributed to study design and implementation, data collection, design and implementation of the statistical analysis, interpretation of results, and drafting and review of the manuscript. Sophie Morois contributed to design and implementation of the statistical analysis, interpretation of results, and drafting and review of the manuscript. Marie-Christine Boutron-Ruault and Franck Carbonnel contributed to design and implementation of the study, data collection, design and implementation of the statistical analysis, interpretation of results, and drafting and review of the manuscript. Françoise Clavel-Chapelon contributed to enrollment and follow-up of patients, design and implementation of the study, and review of the manuscript. All authors have seen the final submitted manuscript and agree with its contents.

Financial support: P.J. has received an institutional research grant from UCB Pharma. S.M. is supported by a doctoral grant from the French Ministry of Research.

Potential competing interests: None.

Corresponding author

Correspondence to Franck Carbonnel.

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/ajg.2010.192

SUPPLEMENTARY MATERIAL is linked to the online version of the paper at http://www.nature.com/ajg

Further reading

  • The role of diet in the aetiopathogenesis of inflammatory bowel disease

    • Hamed Khalili
    • , Simon S. M. Chan
    • , Paul Lochhead
    • , Ashwin N. Ananthakrishnan
    • , Andrew R. Hart
    •  & Andrew T. Chan

    Nature Reviews Gastroenterology & Hepatology (2018)

  • Allergic and Immunologic Perspectives of Inflammatory Bowel Disease

    • Kofi Clarke
    •  & Jayakrishna Chintanaboina

    Clinical Reviews in Allergy & Immunology (2018)

  • Dietary practices and inflammatory bowel disease

    • Jimmy K. Limdi

    Indian Journal of Gastroenterology (2018)

  • Dramatic Increase in Incidence of Ulcerative Colitis and Crohn’s Disease (1988–2011): A Population-Based Study of French Adolescents

    • Silvia Ghione
    • , Hélène Sarter
    • , Mathurin Fumery
    • , Laura Armengol-Debeir
    • , Guillaume Savoye
    • , Delphine Ley
    • , Claire Spyckerelle
    • , Benjamin Pariente
    • , Laurent Peyrin-Biroulet
    • , Dominique Turck
    • , Corinne Gower-Rousseau
    • , Andre J M
    • , Antonietti M
    • , Aouakli A
    • , Armand A
    • , Aroichane I
    • , Assi F
    • , Aubet J P
    • , Auxenfants E
    • , Ayafi-Ramelot F
    • , Bankovski D
    • , Barbry B
    • , Bardoux N
    • , Baron P
    • , Baudet A
    • , Bazin B
    • , Bebahani A
    • , Becqwort J P
    • , Benet V
    • , Benali H
    • , Benguigui C
    • , Ben Soussan E
    • , Bental A
    • , Berkelmans I
    • , Bernet J
    • , Bernou K
    • , Bernou-Dron C
    • , Bertot P
    • , Bertiaux-Vandaële N
    • , Bertrand V
    • , Billoud E
    • , Biron N
    • , Bismuth B
    • , Bleuet M
    • , Blondel F
    • , Blondin V
    • , Bohon P
    • , Boniface E
    • , Bonnière P
    • , Bonvarlet E
    • , Bonvarlet P
    • , Boruchowicz A
    • , Bostvironnois R
    • , Boualit M
    • , Bouche B
    • , Boudaillez C
    • , Bourgeaux C
    • , Bourgeois M
    • , Bourguet A
    • , Bourienne A
    • , Branche J
    • , Bray G
    • , Brazier F
    • , Breban P
    • , Brihier H
    • , Brung-Lefebvre V
    • , Bulois P
    • , Burgiere P
    • , Butel J
    • , Canva J Y
    • , Canva-Delcambre V
    • , Capron J P
    • , Cardot F
    • , Carpentier P
    • , Cartier E
    • , Cassar J F
    • , Cassagnou M
    • , Castex J F
    • , Catala P
    • , Cattan S
    • , Catteau S
    • , Caujolle B
    • , Cayron G
    • , Chandelier C
    • , Chantre M
    • , Charles J
    • , Charneau T
    • , Chavance-Thelu M
    • , Chirita D
    • , Choteau A
    • , Claerbout J F
    • , Clergue P Y
    • , Coevoet H
    • , Cohen G
    • , Collet R
    • , Colombel J F
    • , Coopman S
    • , Corvisart J
    • , Cortot A
    • , Couttenier F
    • , Crinquette J F
    • , Crombe V
    • , Dadamessi I
    • , Dapvril V
    • , Davion T
    • , Dautreme S
    • , Debas J
    • , Degrave N
    • , Dehont F
    • , Delatre C
    • , Delcenserie R
    • , Delette O
    • , Delgrange T
    • , Delhoustal L
    • , Delmotte J S
    • , Demmane S
    • , Deregnaucourt G
    • , Descombes P
    • , Desechalliers J P
    • , Desmet P
    • , Desreumaux P
    • , Desseaux G
    • , Desurmont P
    • , Devienne A
    • , Devouge E
    • , Devred M
    • , Devroux A
    • , Dewailly A
    • , Dharancy S
    • , Di Fiore A
    • , Djeddi D
    • , Djedir R
    • , Dreher-Duwat M L
    • , Dubois R
    • , Dubuque C
    • , Ducatillon P
    • , Duclay J
    • , Ducrocq B
    • , Ducrot F
    • , Ducrotte P
    • , Dufilho A
    • , Duhamel C
    • , Dujardin D
    • , Dumant-Forest C
    • , Dupas J L
    • , Dupont F
    • , Duranton Y
    • , Duriez A
    • , El Achkar K
    • , El Farisi M
    • , Elie C
    • , Elie-Legrand M C
    • , Elkhaki A
    • , Eoche M
    • , Evrard D
    • , Evrard J P
    • , Fatome A
    • , Filoche B
    • , Finet L
    • , Flahaut M
    • , Flamme C
    • , Foissey D
    • , Fournier P
    • , Foutrein- Comes M C
    • , Foutrein P
    • , Fremond D
    • , Frere T
    • , Fumery M
    • , Gallet P
    • , Gamblin C
    • , Ganga-Zandzou P S
    • , Gérard R
    • , Geslin G
    • , Gheyssens Y
    • , Ghossini N
    • , Ghrib S
    • , Gilbert T
    • , Gillet B
    • , Godard D
    • , Godard P
    • , Godchaux J M
    • , Godchaux R
    • , Goegebeur G
    • , Goria O
    • , Gottrand F
    • , Gower P
    • , Grandmaison B
    • , Groux M
    • , Guedon C
    • , Guillard J F
    • , Guillem L
    • , Guillemot F
    • , Guimber D
    • , Haddouche B
    • , Hakim S
    • , Hanon D
    • , Hautefeuille V
    • , Heckestweiller P
    • , Hecquet G
    • , Hedde J P
    • , Hellal H
    • , Henneresse P E
    • , Heyman B
    • , Heraud M
    • , Herve S
    • , Hochain P
    • , Houssin-Bailly L
    • , Houcke P
    • , Huguenin B
    • , Iobagiu S
    • , Ivanovic A
    • , Iwanicki-Caron I
    • , Janicki E
    • , Jarry M
    • , Jeu J
    • , Joly J P
    • , Jonas C
    • , Katherin F
    • , Kerleveo A
    • , Khachfe A
    • , Kiriakos A
    • , Kiriakos J
    • , Klein O
    • , Kohut M
    • , Kornhauser R
    • , Koutsomanis D
    • , Laberenne J E
    • , Laffineur G
    • , Lagarde M
    • , Lannoy P
    • , Lapchin J
    • , Lapprand M
    • , Laude D
    • , Leblanc R
    • , Lecieux P
    • , Leclerc N
    • , Le Couteulx C
    • , Ledent J
    • , Lefebvre J
    • , Lefiliatre P
    • , Legrand C
    • , Le Grix A
    • , Lelong P
    • , Leluyer B
    • , Lenaerts C
    • , Lepileur L
    • , Leplat A
    • , Lepoutre-Dujardin E
    • , Leroi H
    • , Leroy M Y
    • , Lesage J P
    • , Lesage X
    • , Lesage J
    • , Lescanne-Darchis I
    • , Lescut J
    • , Lescut D
    • , Leurent B
    • , Levy P
    • , Lhermie M
    • , Lion A
    • , Lisambert B
    • , Loire F
    • , Louf S
    • , Louvet A
    • , Luciani M
    • , Lucidarme D
    • , Lugand J
    • , Macaigne O
    • , Maetz D
    • , Maillard D
    • , Mancheron H
    • , Manolache O
    • , Marks-Brunel A B
    • , Marti R
    • , Martin F
    • , Martin G
    • , Marzloff E
    • , Mathurin P
    • , Mauillon J
    • , Maunoury V
    • , Maupas J L
    • , Mesnard B
    • , Metayer P
    • , Methari L
    • , Meurisse B
    • , Meurisse F
    • , Michaud L
    • , Mirmaran X
    • , Modaine P
    • , Monthe A
    • , Morel L
    • , Mortier P E
    • , Moulin E
    • , Mouterde O
    • , Mudry J
    • , Nachury M
    • , N'Guyen Khac E
    • , Notteghem B
    • , Ollevier V
    • , Ostyn A
    • , Ouraghi A
    • , Ouvry D
    • , Paillot B
    • , Panien-Claudot N
    • , Paoletti C
    • , Papazian A
    • , Parent B
    • , Pariente B
    • , Paris J C
    • , Patrier P
    • , Paupart L
    • , Pauwels B
    • , Pauwels M
    • , Petit R
    • , Piat M
    • , Piotte S
    • , Plane C
    • , Plouvier B
    • , Pollet E
    • , Pommelet P
    • , Pop D
    • , Pordes C
    • , Pouchain G
    • , Prades P
    • , Prevost A
    • , Prevost J C
    • , Quesnel B
    • , Queuniet A M
    • , Quinton J F
    • , Rabache A
    • , Rabelle P
    • , Raclot G
    • , Ratajczyk S
    • , Rault D
    • , Razemon V
    • , Reix N
    • , Revillon M
    • , Richez C
    • , Robinson P
    • , Rodriguez J
    • , Roger J
    • , Roux J M
    • , Rudelli A
    • , Saber A
    • , Savoye G
    • , Schlosseberg P
    • , Segrestin M
    • , Seguy D
    • , Serin M
    • , Seryer A
    • , Sevenet F
    • , Shekh N
    • , Silvie J
    • , Simon V
    • , Spyckerelle C
    • , Talbodec N
    • , Techy A
    • , Thelu J L
    • , Thevenin A
    • , Thiebault H
    • , Thomas J
    • , Thorel J M
    • , Tielman G
    • , Tode M
    • , Toisin J
    • , Tonnel J
    • , Touchais J Y
    • , Touze Y
    • , Tranvouez J L
    • , Triplet C
    • , Turck D
    • , Uhlen S
    • , Vaillant E
    • , Valmage C
    • , Vanco D
    • , Vandamme H
    • , Vanderbecq E
    • , Vander Eecken E
    • , Vandermolen P
    • , Vandevenne P
    • , Vandeville L
    • , Vandewalle A
    • , Vandewalle C
    • , Vaneslander P
    • , Vanhoove J P
    • , Vanrenterghem A
    • , Varlet P
    • , Vasies I
    • , Verbiese G
    • , Vernier-Massouille G
    • , Vermelle P
    • , Verne C
    • , Vezilier-Cocq P
    • , Vigneron B
    • , Vincendet M
    • , Viot J
    • , Voiment Y M
    • , Wacrenier A
    • , Waeghemaecker L
    • , Wallez J Y
    • , Wantiez M
    • , Wartel F
    • , Weber J
    • , Willocquet J L
    • , Wizla N
    • , Wolschies E
    • , Zalar A
    • , Zaouri B
    • , Zellweger A
    •  & Ziade C

    The American Journal of Gastroenterology (2018)

  • Influence of diet on the gut microbiome and implications for human health

    • Rasnik K. Singh
    • , Hsin-Wen Chang
    • , Di Yan
    • , Kristina M. Lee
    • , Derya Ucmak
    • , Kirsten Wong
    • , Michael Abrouk
    • , Benjamin Farahnik
    • , Mio Nakamura
    • , Tian Hao Zhu
    • , Tina Bhutani
    •  & Wilson Liao

    Journal of Translational Medicine (2017)