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Recent advances in basic science
Emerging role of environmental pollutants in inflammatory bowel disease risk, outcomes and underlying mechanisms
  1. Maria Manuela Estevinho1,2,
  2. Vishal Midya3,
  3. Shirley Cohen-Mekelburg4,5,
  4. Kristine Højgaard Allin6,7,
  5. Mathurin Fumery8,
  6. Salome S Pinho9,10,11,
  7. Jean-Frederic Colombel12,
  8. Manasi Agrawal6,12
  1. 1Department of Gastroenterology, Unidade Local de Saúde Gaia Espinho, Vila Nova de Gaia, Portugal
  2. 2Department of Biomedicine, Unit of Pharmacology and Therapeutics, Faculty of Medicine, University of Porto, Porto, Portugal
  3. 3Department of Environmental Medicine and Climate Science, Icahn School of Medicine at Mount Sinai, New York, New York, USA
  4. 4Division of Gastroenterology and Hepatology, University of Michigan Medicine, Ann Arbor, Michigan, USA
  5. 5VA Center for Clinical Management Research, VA Ann Arbor Health Care System, Ann Arbor, Michigan, USA
  6. 6Center for Molecular Prediction of Inflammatory Bowel Disease (PREDICT), Department of Clinical Medicine, Aalborg University, Copenhagen, Denmark
  7. 7Department of Gastroenterology and Hepatology, Aalborg University Hospital, Aalborg, Denmark
  8. 8Department of Gastroenterology, CHU Amiens and PériTox, UMR-I 01 INERIS, Picardie Jules Verne University, Amiens, France
  9. 9i3S, Institute for Research and Innovation in Health, Porto, Portugal
  10. 10ICBAS-School of Medicine and Biomedical Sciences, Porto, Portugal
  11. 11Faculty of Medicine, University of Porto, Porto, Portugal
  12. 12The Dr. Henry D. Janowitz Division of Gastroenterology, Icahn School of Medicine at Mount Sinai, New York, New York, USA
  1. Correspondence to Dr Manasi Agrawal, The Dr. Henry D. Janowitz Division of Gastroenterology, Icahn School of Medicine at Mount Sinai, New York, New York, USA; manasi.agrawal{at}mountsinai.org

Abstract

Epidemiological and translational data increasingly implicate environmental pollutants in inflammatory bowel disease (IBD). Indeed, the global incidence of IBD has been rising, particularly in developing countries, in parallel with the increased use of chemicals and synthetic materials in daily life and escalating pollution levels. Recent nationwide and ecological studies have reported associations between agricultural pesticides and IBD, particularly Crohn’s disease. Exposure to other chemical categories has also been linked with an increased risk of IBD. To synthesise available data and identify knowledge gaps, we conducted a systematic review of human studies that reported on the impact of environmental pollutants on IBD risk and outcomes. Furthermore, we summarised in vitro data and animal studies investigating mechanisms underlying these associations. The 32 included human studies corroborate that heavy and transition metals, except zinc, air pollutants, per- and polyfluorinated substances, and pesticides are associated with an increased risk of IBD, with exposure to air pollutants being associated with disease-related adverse outcomes as well. The narrative review of preclinical studies suggests several overlapping mechanisms underlying these associations, including increased intestinal permeability, systemic inflammation and dysbiosis. A consolidated understanding of the impact of environmental exposures on IBD risk and outcomes is key to the identification of potentially modifiable risk factors and to inform strategies towards prediction, prevention and mitigation of IBD.

  • CROHN'S DISEASE
  • ULCERATIVE COLITIS
  • EPIDEMIOLOGY
  • INFLAMMATION
  • INTESTINAL MICROBIOLOGY

https://doi.org/10.1136/gutjnl-2024-332523

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    Footnotes

    • X @ShirleyCoMekMD, @KristineAllin, @Matfum, @manasiagrawalmd

    • Correction notice This article has been corrected since it published Online First. The author's name, Salome S Pinho, has been updated.

    • Contributors All authors planned and formatted the review. MME conducted the literature search and data integration. MME, VM, SC-M and MA drafted the manuscript. MME, VM, SC-M, KHA, MF, SP, J-FC and MA conducted critical revision of the manuscript for important intellectual content. MA is responsible for the overall content as guarantor.

    • Funding MA is supported by the National Institute of Diabetes and Digestive and Kidney Diseases (K23DK129762-02), the International Organisation for the Study of Inflammatory Bowel Disease and the Crohn’s and Colitis Foundation Litwin IBD Pioneers Award. KHA is supported by the Danish National Research Foundation (DNRF148) and the Novo Nordisk Foundation (NNF23OC0086595).

    • Competing interests MF reports receiving lecture/consultant fees from Abbvie, Ferring, Tillots, MSD, Biogen, Amgen, Fresenius, Hospira, Sandoz, Pfizer, Bristol Myers Squibb, Celgene, Gilead, Boehringer, Eli Lilly, Nordic-Pharma, Arena, Galapagos, Janssen and Takeda. JFC reports receiving research grants from AbbVie, Janssen Pharmaceuticals and Takeda; receiving payment for lectures from AbbVie, Amgen, Allergan, Ferring Pharmaceuticals, Shire and Takeda; receiving consulting fees from AbbVie, Amgen, Arena Pharmaceuticals, Boehringer Ingelheim, Bristol Myers Squibb, Celgene Corporation, Eli Lilly, Ferring Pharmaceuticals, Galmed Research, Glaxo Smith Kline, Geneva, Iterative Scopes, Janssen Pharmaceuticals, Kaleido Biosciences, Landos, Otsuka, Pfizer, Prometheus, Sanofi, Takeda, TiGenix and hold stock options in Intestinal Biotech Development.MA reports consulting for Douglas Pharmaceutical.

    • Provenance and peer review Commissioned; externally peer reviewed.

    • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.