Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
European Journal of Nutrition
Published in: European Journal of Nutrition 1/2020

01-02-2020 | Ulcerative Colitis | Review

Dietary intake of fish, n-3 polyunsaturated fatty acids, and risk of inflammatory bowel disease: a systematic review and meta-analysis of observational studies

Authors: Hadis Mozaffari, Elnaz Daneshzad, Bagher Larijani, Nick Bellissimo, Leila Azadbakht

Published in: European Journal of Nutrition | Issue 1/2020

Login to get access

Abstract

Purpose

Fish consumption and dietary intake of n-3 polyunsaturated acids (PUFAs) may be associated with inflammatory bowel disease (IBD). We aimed to conduct a systematic review and summarize published articles on the association between fish consumption and dietary intake of n-3 PUFAs with the risk of IBD.

Methods

PubMed, Scopus, and Web of Science databases were used to conduct a comprehensive search and identify eligible literature published prior to January 2019. Fixed-effects model or random-effects models (DerSimonian–Laird method) were applied to pool the effect sizes. Cochrane Q test was used to trace the potential source of heterogeneity across studies.

Results

12 studies (5 prospective and 7 case–control) were included in the systematic review, which ten of them were eligible for inclusion in the meta-analysis. Studies were included a total sample size of 282610 participants which 2002 of them were cases of IBD [1061 Crohn’s disease (CD) and 937 ulcerative colitis (UC)]. A negative association was found between fish consumption and the incidence of CD (pooled effect size: 0.54, 95%CI: 0.31–0.96, P = 0.03). There was no relationship between total dietary n-3 PUFAs intake and IBD (pooled effect size: 1.17, 95%CI: 0.80–1.72, P = 0.41). A significant inverse association was observed between dietary long-chain n-3 PUFAs and the risk of UC (pooled effect size: 0.75, 95%CI: 0.57–0.98, P = 0.03). Moreover, no association was found between α-Linolenic acid (ALA) and IBD (pooled effect size: 1.17, 95%CI: 0.63–2.17, P = 0.62).

Conclusions

Findings showed a negative association between fish consumption and the risk of CD. Moreover, there was a significant inverse association between dietary long-chain n-3 PUFAs and the risk of UC.
Appendix
Available only for authorised users
Literature
1.
Molodecky NA, Soon S, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW (2012) Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142(1):46–54.e42CrossRefPubMed
2.
Cho JH (2008) The genetics and immunopathogenesis of inflammatory bowel disease. Nat Rev Immunol 8(6):458PubMedCrossRef
3.
Jantchou P, Monnet E, Carbonnel F (2006) Environmental risk factors in Crohn’s disease and ulcerative colitis (excluding tobacco and appendicectomy). Gastroenterol Clin Biol 30(6–7):859–867PubMedCrossRef
4.
5.
Lee D, Albenberg L, Compher C, Baldassano R, Piccoli D, Lewis JD, Wu GD (2015) Diet in the pathogenesis and treatment of inflammatory Bowelá diseases. Gastroenterology 148(6):1087–1106PubMedCrossRef
6.
Cashman KD, Shanahan F (2003) Is nutrition an aetiological factor for inflammatory bowel disease? Eur J Gastroenterol Hepatol 15(6):607–613PubMedCrossRef
7.
Boeing H, Bechthold A, Bub A, Ellinger S, Haller D, Kroke A, Leschik-Bonnet E, Müller MJ, Oberritter H, Schulze M (2012) Critical review: vegetables and fruit in the prevention of chronic diseases. Eur J Nutr 51(6):637–663PubMedPubMedCentralCrossRef
8.
Mouli VP, Ananthakrishnan AN (2014) vitamin D and inflammatory bowel diseases. Aliment Pharmacol Ther 39(2):125–136PubMedCrossRef
9.
Oldenburg B, Koningsberger J, Van Berge Henegouwen G, Van Asbeck B, Marx J (2001) Iron and inflammatory bowel disease. Aliment Pharmacol Ther 15(4):429–438PubMedCrossRef
10.
Mori TA, Beilin LJ (2004) Omega-3 fatty acids and inflammation. Curr Atheroscler Rep 6(6):461–467PubMedCrossRef
11.
Abubakar I, Myhill DJ, Hart AR, Lake IR, Harvey I, Rhodes JM, Robinson R, Lobo AJ, Probert CS, Hunter PR (2007) 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 165(7):776–783PubMedCrossRef
12.
Ananthakrishnan AN, Khalili H, Konijeti GG, Higuchi LM, de Silva P, Fuchs CS, Willett WC, Richter JM, Chan AT (2014) Long-term intake of dietary fat and risk of ulcerative colitis and Crohn’s disease. Gut 63(5):776–784PubMedCrossRef
13.
Ananthakrishnan AN, Khalili H, Song M, Higuchi LM, Richter JM, Nimptsch K, Wu K, Chan AT (2015) High school diet and risk of Crohn’s disease and ulcerative colitis. Inflamm Bowel Dis 21(10):2311–2319PubMed
14.
Chan S, Luben R, Olsen A, Tjonneland A, Kaaks R, Lindgren S, Grip O, Bergmann M, Boeing H, Hallmans G (2014) Association between high dietary intake of the n – 3 polyunsaturated fatty acid docosahexaenoic acid and reduced risk of Crohn’s disease. Aliment Pharmacol Ther 39(8):834–842PubMedPubMedCentralCrossRef
15.
Investigators IiES (2009) Linoleic acid, a dietary n-6 polyunsaturated fatty acid, and the aetiology of ulcerative colitis: a nested case–control study within a European prospective cohort study. Gut 58(12):1606–1611CrossRef
16.
Jantchou P, Morois S, Clavel-Chapelon F, Boutron-Ruault M-C, Carbonnel F (2010) Animal protein intake and risk of inflammatory bowel disease: the E3N prospective study. Am J Gastroenterol 105(10):2195PubMedCrossRef
17.
Maconi G, Ardizzone S, Cucino C, Bezzio C, Russo AG, Porro GB (2010) Pre-illness changes in dietary habits and diet as a risk factor for inflammatory bowel disease: a case-control study. World J Gastroenterol WJG 16(34):4297PubMedCrossRef
18.
Pugazhendhi S, Sahu MK, Subramanian V, Pulimood A, Ramakrishna BS (2011) Environmental factors associated with Crohn’s disease in India. Indian J Gastroenterol 30(6):264–269PubMedCrossRef
19.
Rashvand S, Somi MH, Rashidkhani B, Hekmatdoost A (2015) Dietary protein intakes and risk of ulcerative colitis. Med J Islam Repub Iran 29:253PubMedPubMedCentral
20.
Rashvand S, Somi MH, Rashidkhani B, Hekmatdoost A (2015) Dietary fatty acid intakes are related to the risk of ulcerative colitis: a case–control study. Int J Colorectal Dis 30(9):1255–1260PubMedCrossRef
21.
22.
Sakamoto N, Kono S, Wakai K, Fukuda Y, Satomi M, Shimoyama T, Inaba Y, Miyake Y, Sasaki S, Okamoto K (2005) Dietary risk factors for inflammatory bowel disease A multicenter case–control Study in Japan. Inflamm Bowel Dis 11(2):154–163PubMedCrossRef
23.
Turner D, Shah PS, Steinhart AH, Zlotkin S, Griffiths AM (2011) Maintenance of remission in inflammatory bowel disease using omega-3 fatty acids (fish oil): a systematic review and meta-analyses. Inflamm Bowel Dis 17(1):336–345PubMedCrossRef
24.
Moher D, Liberati A, Tetzlaff J, Altman DG (2010) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Int J Surg 8(5):336–341PubMedCrossRef
25.
Wells G, Shea B, O’connell D, Peterson J, Welch V, Losos M, Tugwell P (2016) The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Ottawa (ON): Ottawa Hospital Research Institute, 2009. (Available in March)
26.
Mozaffari H, Djafarian K, Mofrad M, Shab-Bidar S (2018) Dietary fat, saturated fatty acid, and monounsaturated fatty acid intakes and risk of bone fracture: a systematic review and meta-analysis of observational studies. Osteoporos Int 2018:1–13
27.
Higgins JP, Green S (2011) Cochrane handbook for systematic reviews of interventions, vol 4. Wiley, Hoboken
28.
Egger M, Smith GD, Schneider M, Minder C (1997) Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109):629–634PubMedPubMedCentral
29.
Marlow G, Ellett S, Ferguson IR, Zhu S, Karunasinghe N, Jesuthasan AC, Han DY, Fraser AG, Ferguson LR (2013) Transcriptomics to study the effect of a Mediterranean-inspired diet on inflammation in Crohn’s disease patients. Hum Genomics 7(1):24PubMedPubMedCentralCrossRef
30.
Amre DK, D’souza S, Morgan K, Seidman G, Lambrette P, Grimard G, Israel D, Mack D, Ghadirian P, Deslandres C (2007) Imbalances in dietary consumption of fatty acids, vegetables, and fruits are associated with risk for Crohn’s disease in children. Am J Gastroenterol 102(9):2016PubMedCrossRef
31.
D’souza S, Levy E, Mack D, Israel D, Lambrette P, Ghadirian P, Deslandres C, Morgan K, Seidman EG, Amre DK (2007) Dietary patterns and risk for Crohn’s disease in children. Inflamm Bowel Dis 14(3):367–373CrossRef
32.
Tasson L, Canova C, Vettorato MG, Savarino E, Zanotti R (2017) Influence of diet on the course of inflammatory bowel disease. Dig Dis Sci 62(8):2087–2094PubMedCrossRef
33.
Andersen V, Olsen A, Carbonnel F, Tjønneland A, Vogel U (2012) Diet and risk of inflammatory bowel disease. Dig Dis Sci 44(3):185–194
34.
Gentschew L, Ferguson LR (2012) Role of nutrition and microbiota in susceptibility to inflammatory bowel diseases. Mol Nutr Food Res 56(4):524–535PubMedCrossRef
35.
Benno Y, Suzuki K, Suzuki K, Narisawa K, Bruce WR, Mitsuoka T (1986) Comparison of the fecal microflora in rural Japanese and urban Canadians. Microbiol Immunol 30(6):521–532PubMedCrossRef
36.
Benno Y, Endo K, Miyoshi H, Okuda T, Koishi H, Mitsuoka T (1989) Effect of rice fiber on human fecal microflora. Microbiol Immunol 33(5):435–440PubMedCrossRef
37.
Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH (2001) A frameshift mutation in NOD2 associated with susceptibility to Crohn’s disease. Nature 411(6837):603PubMedCrossRef
38.
Hisamatsu T, Suzuki M, Reinecker H-C, Nadeau WJ, McCormick BA, Podolsky DK (2003) CARD15/NOD2 functions as an antibacterial factor in human intestinal epithelial cells. Gastroenterology 124(4):993–1000PubMedCrossRef
39.
Flores A, Burstein E, Cipher DJ, Feagins LA (2015) Obesity in inflammatory bowel disease: a marker of less severe disease. Dig Dis Sci 60(8):2436–2445PubMedCrossRef
40.
Aljada A, Mohanty P, Ghanim H, Abdo T, Tripathy D, Chaudhuri A, Dandona P (2004) Increase in intranuclear nuclear factor κB and decrease in inhibitor κB in mononuclear cells after a mixed meal: evidence for a proinflammatory effect. Am J Clin Nutr 79(4):682–690PubMedCrossRef
41.
Chapman-Kiddell CA, Davies PS, Gillen L, Radford-Smith GL (2010) Role of diet in the development of inflammatory bowel disease. Inflamm Bowel Dis 16(1):137–151PubMedCrossRef
42.
Dandona P, Aljada A, Bandyopadhyay A (2004) Inflammation: the link between insulin resistance, obesity and diabetes. Trends Immunol 25(1):4–7CrossRefPubMed
43.
44.
Miller LG, Goldstein G, Murphy M, Ginns LC (1982) Reversible alterations in immunoregulatory T cells in smoking: analysis by monoclonal antibodies and flow cytometry. Chest 82(5):526–529PubMedCrossRef
45.
46.
Thomas GA, Rhodes J, Green JT, Richardson C (2000) Role of smoking in inflammatory bowel disease: implications for therapy. Postgrad Med J 76(895):273–279PubMedPubMedCentralCrossRef
47.
Prytz H, Benoni C, Tagesson C (1989) Does smoking tighten the gut? Scand J Gastroenterol 24(9):1084–1088PubMedCrossRef
48.
John S, Luben R, Shrestha SS, Welch A, Khaw K-T, Hart AR (2010) Dietary n-3 polyunsaturated fatty acids and the aetiology of ulcerative colitis: a UK prospective cohort study. Eur J Gastroenterol Hepatol 22(5):602–606PubMedCrossRef
49.
Hekmatdoost A, Wu X, Morampudi V, Innis SM, Jacobson K (2013) Dietary oils modify the host immune response and colonic tissue damage following Citrobacter rodentium infection in mice. Am J Physiol Gastrointest Liver Physiol 304(10):G917–G928PubMedCrossRef
50.
Hekmatdoost A, Mirshafiey A, Feizabadi MM, Djazayeri A (2009) Polyunsaturated fatty acids, microflora and colitis. Ann Nutr Metabol 55(4):325–325CrossRef
51.
Hekmatdoost A, Feizabadi MM, Djazayery A, Mirshafiey A, Eshraghian MR, Yeganeh SM, Sedaghat R, Jacobson K (2008) The effect of dietary oils on cecal microflora in experimental colitis in mice. Indian J Gastroenterol 27(5):186–189PubMed
52.
Nieto N, Torres MI, Ríos A, Gil A (2002) Dietary polyunsaturated fatty acids improve histological and biochemical alterations in rats with experimental ulcerative colitis. J Nutr 132(1):11–19PubMedCrossRef
53.
Uchiyama K, Nakamura M, Odahara S, Koido S, Katahira K, Shiraishi H, Ohkusa T, Fujise K, Tajiri H (2010) N-3 polyunsaturated fatty acid diet therapy for patients with inflammatory bowel disease. Inflamm Bowel Dis 16(10):1696–1707PubMedCrossRef
54.
Collie-Duguid E, Wahle K (1996) Inhibitory effect of fish oil N-3 polyunsaturated fatty acids on the expression of endothelial cell adhesion molecules. Biochem Biophys Res Commun 220(3):969–974PubMedCrossRef
55.
Shores DR, Binion DG, Freeman BA, Baker PR (2010) New insights into the role of fatty acids in the pathogenesis and resolution of inflammatory bowel disease. Inflamm Bowel Dis 17(10):2192–2204PubMedCrossRef
56.
Esteve-Comas M, Nunez M, Fernández-Bañares F, Abad-Lacruz A, Gil A, Cabre E, Gonzalez-Huix F, Bertran X, Gassull M (1993) Abnormal plasma polyunsaturated fatty acid pattern in non-active inflammatory bowel disease. Gut 34(10):1370–1373PubMedPubMedCentralCrossRef
57.
Kawakami Y, Okada H, Murakami Y, Kawakami T, Ueda Y, Kunii D, Sakamoto Y, Shiratori Y, Okita M (2007) Dietary intake, neutrophil fatty acid profile, serum antioxidant vitamins and oxygen radical absorbance capacity in patients with ulcerative colitis. J Nutr Sci Vitaminol 53(2):153–159PubMedCrossRef
58.
Nishida T, Miwa H, Shigematsu A, Yamamoto M, Iida M, Fujishima M (1987) Increased arachidonic acid composition of phospholipids in colonic mucosa from patients with active ulcerative colitis. Gut 28(8):1002–1007PubMedPubMedCentralCrossRef
59.
Marion-Letellier R, Savoye G, Beck PL, Panaccione R, Ghosh S (2013) Polyunsaturated fatty acids in inflammatory bowel diseases: a reappraisal of effects and therapeutic approaches. Inflamm Bowel Dis 19(3):650–661PubMedCrossRef
60.
Weatherill AR, Lee JY, Zhao L, Lemay DG, Youn HS, Hwang DH (2005) Saturated and polyunsaturated fatty acids reciprocally modulate dendritic cell functions mediated through TLR4. J Immunol 174(9):5390–5397PubMedCrossRef
61.
Novak TE, Babcock TA, Jho DH, Helton WS, Espat NJ (2003) NF-κB inhibition by ω-3 fatty acids modulates LPS-stimulated macrophage TNF-α transcription. Am J Physiol Lung Cell Mol Physiol 284(1):L84–L89PubMedCrossRef
62.
Hughes R, Magee E, Bingham S (2000) Protein degradation in the large intestine: relevance to colorectal cancer. Curr Issues Intestinal Microbiol 1(2):51–58
63.
Roediger W (2008) Nitric oxide from dysbiotic bacterial respiration of nitrate in the pathogenesis and as a target for therapy of ulcerative colitis. Aliment Pharmacol Ther 27(7):531–541PubMedCrossRef
64.
Weylandt KH, Chiu C-Y, Gomolka B, Waechter SF, Wiedenmann B (2012) Omega-3 fatty acids and their lipid mediators: towards an understanding of resolvin and protectin formation. Prostaglandins Other Lipid Mediat 97(3–4):73–82PubMedCrossRef
65.
Depner CM, Philbrick KA, Jump DB (2013) Docosahexaenoic acid attenuates hepatic inflammation, oxidative stress, and fibrosis without decreasing hepatosteatosis in a Ldlr–/– mouse model of western diet-induced nonalcoholic steatohepatitis1–3. J Nutr 143(3):315–323PubMedPubMedCentralCrossRef
66.
Goldman D, Pickett W, Goetzl E (1983) Human neutrophil chemotactic and degranulating activities of leukotriene B5 (LTB5) derived from eicosapentaenoic acid. Biochem Biophys Res Commun 117(1):282–288PubMedCrossRef
67.
Rodríguez-Lagunas MJ, Ferrer R, Moreno JJ (2013) Effect of eicosapentaenoic acid-derived prostaglandin E3 on intestinal epithelial barrier function. Prostaglandins Leukot Essent Fatty Acids 88(5):339–345PubMedCrossRef
68.
Patterson E, Wall R, Fitzgerald G, Ross R, Stanton C (2012) Health implications of high dietary omega-6 polyunsaturated fatty acids. J Nutr Metabol 2012:539426CrossRef
69.
Turner D, Steinhart AH, Griffiths AM (2007) Omega 3 fatty acids (fish oil) for maintenance of remission in ulcerative colitis. Cochrane Database of Syst Rev 18(3):CD006443
70.
Scaioli E, Liverani E, Belluzzi A (2017) The imbalance between n-6/n-3 polyunsaturated fatty acids and inflammatory bowel disease: a comprehensive review and future therapeutic perspectives. Int J Mol Sci 18(12):2619PubMedCentralCrossRef
71.
Blasbalg TL, Hibbeln JR, Ramsden CE, Majchrzak SF, Rawlings RR (2011) Changes in consumption of omega-3 and omega-6 fatty acids in the United States during the 20th century. Am J Clin Nutr 93(5):950–962PubMedPubMedCentralCrossRef
72.
Meyer BJ, Mann NJ, Lewis JL, Milligan GC, Sinclair AJ, Howe PR (2003) Dietary intakes and food sources of omega-6 and omega-3 polyunsaturated fatty acids. Lipids 38(4):391–398PubMedCrossRef
Metadata
Title
Dietary intake of fish, n-3 polyunsaturated fatty acids, and risk of inflammatory bowel disease: a systematic review and meta-analysis of observational studies
Authors
Hadis Mozaffari
Elnaz Daneshzad
Bagher Larijani
Nick Bellissimo
Leila Azadbakht
Publication date
01-02-2020
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Nutrition / Issue 1/2020
Print ISSN: 1436-6207
Electronic ISSN: 1436-6215
DOI
https://doi.org/10.1007/s00394-019-01901-0

Other articles of this Issue 1/2020

European Journal of Nutrition 1/2020 Go to the issue

Original Contribution

Effect of Vitamin A status during pregnancy on maternal anemia and newborn birth weight: results from a cohort study in the Western Brazilian Amazon

Correction

Correction to: Evaluation of the efficacy of Lactobacillus plantarum HEAL9 and Lactobacillus paracasei 8700:2 on aspects of common cold infections in children attending day care: a randomised, double-blind, placebo-controlled clinical study

Original Contribution

Intakes of long-chain omega-3 polyunsaturated fatty acids and non-fried fish in relation to incidence of chronic kidney disease in young adults: a 25-year follow-up

Original Contribution

Evaluation of the efficacy of Lactobacillus plantarum HEAL9 and Lactobacillus paracasei 8700:2 on aspects of common cold infections in children attending day care: a randomised, double-blind, placebo-controlled clinical study

Original Contribution

Effects of a polysaccharide-rich extract derived from Irish-sourced Laminaria digitata on the composition and metabolic activity of the human gut microbiota using an in vitro colonic model

Original Contribution

Chocolate and risk of chronic disease: a systematic review and dose-response meta-analysis
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits