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Drinking water quality and inflammatory bowel disease: a prospective cohort study

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Abstract

Environmental factors, such as drinking water and diets, play an important role in the development of inflammatory bowel disease (IBD). This study aimed to investigate the associations of metal elements and disinfectants in drinking water with the risk of inflammatory bowel disease (IBD) and to assess whether diet influences these associations. We conducted a prospective cohort study including 22,824 participants free from IBD from the Yinzhou cohort study in the 2016–2022 period with an average follow-up of 5.24 years. The metal and disinfectant concentrations were measured in local pipeline terminal tap water samples. Cox regression models adjusted for multi-level covariates were used to estimate adjusted hazard ratios (aHRs) and 95% confidence intervals (95% CIs). During an average follow-up period of 5.24 years, 46 cases of IBD were identified. For every 1 standard deviation (SD) increase in the concentration of manganese, mercury, selenium, sulfur tetraoxide (SO4), chlorine, and nitrate nitrogen (NO3_N) were associated with a higher risk of IBD with the HRs of 1.45 (95% CI: 1.14 to 1.84), 1.51 (95% CI: 1.24–1.82), 1.29 (95% CI: 1.03–1.61), 1.52 (95% CI: 1.26–1.83), 1.26 (95% CI: 1.18–1.34), and 1.66 (95% CI: 1.32–2.09), whereas zinc and fluorine were inversely associated with IBD with the HRs of 0.42 (95% CI: 0.24 to 0.73) and 0.68 (95% CI: 0.54–0.84), respectively. Stronger associations were observed in females, higher income groups, low education groups, former drinkers, and participants who never drink tea. Diets have a moderating effect on the associations of metal and nonmetal elements with the risk of IBD. We found significant associations between exposure to metals and disinfectants and IBD. Diets regulated the associations to some extent.

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References

  • Aamodt G, Bukholm G, Jahnsen J, Moum B, Vatn MH (2008) The association between water supply and inflammatory bowel disease based on a 1990–1993 cohort study in southeastern Norway. Am J Epidemiol 168(9):1065–1072

    Article  Google Scholar 

  • Abegunde AT, Muhammad BH, Bhatti O, Ali T (2016) Environmental risk factors for inflammatory bowel diseases: evidence based literature review. World J Gastroenterol 22(27):6296–6317

    Article  CAS  Google Scholar 

  • Abubakar I, Myhill DJ, Hart AR, Lake IR, Harvey I, Rhodes JM et al (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):776–783

    Article  Google Scholar 

  • Adegoke A, Salami A, Olaleye S (2017) Cadmium exacerbates acetic acid induced experimental colitis in rats. J Exp Biol 7(5):27

    Google Scholar 

  • Alatab S, Sepanlou SG, Ikuta K, Vahedi H, Bisignano C, Safiri S et al (2020) The global, regional, and national burden of inflammatory bowel disease in 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Gastroenterol Hepatol 5(1):17–30

    Article  Google Scholar 

  • Ananthakrishnan AN, Khalili H, Song M, Higuchi LM, Richter JM, Chan AT (2015) Zinc intake and risk of Crohn’s disease and ulcerative colitis: a prospective cohort study. Int J Epidemiol 44(6):1995–2005

    Article  Google Scholar 

  • Ananthakrishnan AN, Bernstein CN, Iliopoulos D, Macpherson A, Neurath MF, Ali RAR et al (2018) Environmental triggers in IBD: a review of progress and evidence. Nat Rev Gastroenterol Hepatol 15(1):39–49

    Article  Google Scholar 

  • Anka AU, Usman AB, Kaoje AN, Kabir RM, Bala A, KazemArki M (2022) Potential mechanisms of some selected heavy metals in the induction of inflammation and autoimmunity. Eur J Inflamm 20:1721727X221122719

    Article  CAS  Google Scholar 

  • Baron S, Turck D, Leplat C, Merle V, Gower-Rousseau C, Marti R et al (2005) Environmental risk factors in paediatric inflammatory bowel diseases: a population based case control study. Gut 54(3):357–363

    Article  CAS  Google Scholar 

  • Baumgart DC, Carding SR (2007) Inflammatory bowel disease: cause and immunobiology. Lancet 369(9573):1627–40

    Article  CAS  Google Scholar 

  • Burisch J, Pedersen N, Cukovic-Cavka S, Turk N, Kaimakliotis I, Duricova D, Bortlik M et al (2014) Environmental factors in a population-based inception cohort of inflammatory bowel disease patients in Europe—an ECCO-EpiCom study. J Crohns Colitis 8(7):607–616

    Article  CAS  Google Scholar 

  • El-Tawil AM (2012) Zinc supplementation tightens leaky gut in Crohn’s disease. Inflamm Bowel Dis 18(2):E399

    Article  CAS  Google Scholar 

  • Engwa GA, Ferdinand PU, Nwalo FN, Unachukwu MN (2019) Mechanism and health effects of heavy metal toxicity in humans. In: Karcioglu O, Arslan B (eds) Poisoning in the modern world-new tricks for an old dog?, vol 10. Intechopen, London, pp 70–90

  • Forbes JD, Van Domselaar G, Sargent M, Green C, Springthorpe S, Krause DO, Bernstein CN (2016) Microbiome profiling of drinking water in relation to incidence of inflammatory bowel disease. Can J Microbiol 62(9):781–793

    Article  CAS  Google Scholar 

  • Galvez J, Rodríguez-Cabezas ME, Zarzuelo A (2005) Effects of dietary fiber on inflammatory bowel disease. Mol Nutr Food Res 49(6):601–608

    Article  Google Scholar 

  • Hansen TS, Jess T, Vind I, Elkjaer M, Nielsen MF, Gamborg M, Munkholm P (2011) Environmental factors in inflammatory bowel disease: a case-control study based on a Danish inception cohort. J Crohns Colitis 5(6):577–584

    Article  Google Scholar 

  • Harischandra DS, Ghaisas S, Zenitsky G, Jin H, Kanthasamy A, Anantharam V, Kanthasamy AG (2019) Manganese-induced neurotoxicity: new insights into the triad of protein misfolding, mitochondrial impairment, and neuroinflammation. Front Neurosci 13:654

    Article  Google Scholar 

  • Hu D, Ren J, Wang G, Gu G, Liu S, Wu X et al (2014) Geographic mapping of Crohn’s disease and its relation to affluence in Jiangsu province, an eastern coastal province of china. Gastroenterol Res Pract 2014:590467

    Article  Google Scholar 

  • Jädert C, Petersson J, Massena S, Ahl D, Grapensparr L, Holm L et al (2012) Decreased leukocyte recruitment by inorganic nitrate and nitrite in microvascular inflammation and NSAID-induced intestinal injury. Free Radical Biol Med 52(3):683–692

    Article  Google Scholar 

  • Jairath V, Feagan BG (2020) Global burden of inflammatory bowel disease. Lancet Gastroenterol Hepatol 5(1):2–3

    Article  Google Scholar 

  • Jantchou P, Morois S, Clavel-Chapelon F, Boutron-Ruault MC, Carbonnel F (2010) Animal protein intake and risk of inflammatory bowel disease: the E3N prospective study. Am J Gastroenterol 105(10):2195–2201

    Article  CAS  Google Scholar 

  • Jin Y, Wu S, Zeng Z, Fu Z (2017) Effects of environmental pollutants on gut microbiota. Environ Pollut 222:1–9

    Article  CAS  Google Scholar 

  • Jostins L, Ripke S, Weersma RK, Duerr RH, McGovern DP, Hui KY et al (2012) Host–microbe interactions have shaped the genetic architecture of inflammatory bowel disease. Nature 491(7422):119–124

    Article  CAS  Google Scholar 

  • Jowett SL, Seal CJ, Pearce MS, Phillips E, Gregory W, Barton JR, Welfare MR (2004) Influence of dietary factors on the clinical course of ulcerative colitis: a prospective cohort study. Gut 53(10):1479–1484

    Article  CAS  Google Scholar 

  • Kaplan GG, Windsor JW (2021) The four epidemiological stages in the global evolution of inflammatory bowel disease. Nat Rev Gastroenterol Hepatol 18(1):56–66

    Article  Google Scholar 

  • Klement E, Lysy J, Hoshen M, Avitan M, Goldin E, Israeli E (2008) Childhood hygiene is associated with the risk for inflammatory bowel disease: a population-based study. Am J Gastroenterol 103(7):1775–1782

    Article  Google Scholar 

  • Kudva AK, Shay AE, Prabhu KS (2015) Selenium and inflammatory bowel disease. Am J Physiol Gastrointest Liver Physiol 309(2):G71–G77

    Article  CAS  Google Scholar 

  • Kushkevych I, Leščanová O, Dordević D, Jančíková S, Hošek J, Vítězová M et al (2019) The sulfate-reducing microbial communities and meta-analysis of their occurrence during diseases of small–large intestine axis. J Clin Med 8(10):1656

    Article  CAS  Google Scholar 

  • Kushkevych I, Castro Sangrador J, Dordević D, Rozehnalová M, Černý M, Fafula R, Vítězová M, Rittmann SKR (2020) Evaluation of physiological parameters of intestinal sulfate-reducing bacteria isolated from patients suffering from IBD and healthy people. J Clin Med 9(6):1920

  • Lahiri A, Abraham C (2014) Activation of pattern recognition receptors up-regulates metallothioneins, thereby increasing intracellular accumulation of zinc, autophagy, and bacterial clearance by macrophages. Gastroenterology 147(4):835–846

    Article  CAS  Google Scholar 

  • Lakatos PL (2009) Environmental factors affecting inflammatory bowel disease: have we made progress? Dig Dis 27(3):215–225

    Article  Google Scholar 

  • Lerner A (2007) Aluminum is a potential environmental factor for Crohn’s disease induction: extended hypothesis. Ann N Y Acad Sci 1107:329–345

    Article  CAS  Google Scholar 

  • Li XF, Mitch WA (2018) Drinking water disinfection byproducts (DBPs) and human health effects: multidisciplinary challenges and opportunities. Environ Sci Technol 52(4):1681–1689

    Article  CAS  Google Scholar 

  • Li T, Yu Z, Xu L, Wu Y, Yu L, Yang Z (2022) Residential greenness, air pollution, and incident ischemic heart disease: a prospective cohort study in China. Sci Total Environ 838:155881

    Article  CAS  Google Scholar 

  • Mahid SS, Minor KS, Soto RE, Hornung CA, Galandiuk S (2006) Smoking and inflammatory bowel disease: a meta-analysis. Mayo Clin Proc 81(11):1462–1471

    Article  Google Scholar 

  • Ng SC, Shi HY, Hamidi N, Underwood FE, Tang W, Benchimol EI et al (2017) Worldwide incidence and prevalence of inflammatory bowel disease in the 21st century: a systematic review of population-based studies. Lancet 390(10114):2769–2778

    Article  Google Scholar 

  • Oudkerk Pool M, Bouma G, Visser JJ, Kolkman JJ, Tran DD, Meuwissen SG, Peña AS (1995) Serum nitrate levels in ulcerative colitis and Crohn’s disease. Scand J Gastroenterol 30(8):784–788

    Article  CAS  Google Scholar 

  • Ozenne B, Sørensen AL, Scheike T, Torp-Pedersen C, Gerds TA (2017) riskRegression: predicting the risk of an event using Cox regression models. R Journal 9(2):440–460

    Article  Google Scholar 

  • Park J, Cheon JH (2021) Incidence and prevalence of inflammatory bowel disease across Asia. Yonsei Med J 62(2):99–108

    Article  Google Scholar 

  • Perl DP, Fogarty U, Harpaz N, Sachar DB (2004) Bacterial-metal interactions: the potential role of aluminum and other trace elements in the etiology of Crohn’s disease. Inflamm Bowel Dis 10(6):881–883

    Article  Google Scholar 

  • Piovani D, Danese S, Peyrin-Biroulet L, Bonovas S (2020) Inflammatory bowel disease: estimates from the global burden of disease 2017 study. Aliment Pharmacol Ther 51(2):261–270

    Article  Google Scholar 

  • Piovani D, Danese S, Peyrin-Biroulet L, Nikolopoulos GK, Lytras T, Bonovas S (2019) Environmental risk factors for inflammatory bowel diseases: an umbrella review of meta-analyses. Gastroenterology 157(3):647–659. e4

  • Ramos GP, Papadakis KA (2019) Mechanisms of disease: inflammatory bowel diseases. Mayo Clin Proc 94(1):155–165

    Article  CAS  Google Scholar 

  • Rice KM, Walker EM Jr, Wu M, Gillette C, Blough ER (2014) Environmental mercury and its toxic effects. J Prev Med Public Health 47(2):74–83

    Article  Google Scholar 

  • Rose DJ, DeMeo MT, Keshavarzian A, Hamaker BR (2007) Influence of dietary fiber on inflammatory bowel disease and colon cancer: importance of fermentation pattern. Nutr Rev 65(2):51–62

    Article  Google Scholar 

  • Singh P, Mogra P, Bano H, Sankhla V, Deora K, Barolia S, Javeria S (2012) Protective and preventive effects of curcumin against cadmium chloride induced gastrointestinal toxicity in Swiss albino mice. World J Sci Technol 2(12):10–17

    Google Scholar 

  • Stochel-Gaudyn A, Fyderek K, Kościelniak P (2019) Serum trace elements profile in the pediatric inflammatory bowel disease progress evaluation. J Trace Elem Med Biol 55:121–126

    Article  CAS  Google Scholar 

  • Vaghari-Tabari M, Jafari-Gharabaghlou D, Sadeghsoltani F, Hassanpour P, Qujeq D, Rashtchizadeh N, Ghorbanihaghjo A (2021) Zinc and selenium in inflammatory bowel disease: trace elements with key roles? Biol Trace Elem Res 199(9):3190–3204

    Article  CAS  Google Scholar 

  • Vojdani A, Pangborn JB, Vojdani E, Cooper EL (2003) Infections, toxic chemicals and dietary peptides binding to lymphocyte receptors and tissue enzymes are major instigators of autoimmunity in autism. Int J Immunopathol Pharmacol 16(3):189–199

    Article  CAS  Google Scholar 

  • Wang W, Green M, Choi JE, Gijón M, Kennedy PD, Johnson JK et al (2019) CD8+ T cells regulate tumour ferroptosis during cancer immunotherapy. Nature 569(7755):270–274

    Article  CAS  Google Scholar 

  • Yamamoto T, Nakahigashi M, Saniabadi AR (2009) Review article: diet and inflammatory bowel disease–epidemiology and treatment. Aliment Pharmacol Ther 30(2):99–112

    Article  CAS  Google Scholar 

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Acknowledgements

We would like to thank all co-authors. We would also like to extend our thanks to the Yinzhou cohort survey team for providing data and the training in using the dataset.

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Authors and Affiliations

  1. Department of Global Health, School of Public Health, Peking University, 38 Xue Yuan Road, Haidian District, Beijing, 100191, China

    Shuduo Zhou, Xuejie Dong, Zhisheng Liang, Ming Xu, Zhi-Jie Zheng & Zhenyu Zhang

  2. Institute for Global Health and Development, Peking University, Beijing, China

    Shuduo Zhou, Xuejie Dong, Ming Xu, Zhi-Jie Zheng & Zhenyu Zhang

  3. The Center for Disease Control and Prevention of Yinzhou District, Ningbo, Zhejiang, China

    Pengfei Chai

  4. Department of Epidemiology and Biostatistics, Zhejiang University School of Public Health, Hangzhou, 310058, China

    Zongming Yang, Jianbing Wang & Kun Chen

  5. Department of Gastroenterology, Peking University First Hospital, Beijing, 100034, China

    Junxia Li & Guigen Teng

  6. School of Public Health, Capital Medical University, Beijing, 100069, China

    Shengzhi Sun

  7. Department of Epidemiology and Biostatistics, and National Clinical Research Center for Child Health of the Children’s Hospital, Zhejiang University School of Medicine, Hangzhou, 310058, China

    Jianbing Wang

  8. Department of Epidemiology and Biostatistics, and Cancer Institute of the Second Affiliated Hospital, Zhejiang University School of Medicine, Hangzhou, 310058, China

    Kun Chen

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  1. Shuduo Zhou
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Contributions

Shuduo Zhou, Zhenyu Zhang, and Kun Chen: drafting the manuscript, study design, data analysis, and interpretation. Shuduo Zhou, Pengfei Chai, Zhenyu Zhang, Shengzhi Sun, Ming Xu, and Jianbing Wang: study concept and design, and critical revision of the article for important intellectual content. Junxia Li, Guigen Teng, Xuejie Dong, Zhisheng Liang, and Zongming Yang: critical revision of the article for important intellectual content. All authors gave final approval of the version to be published.

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Correspondence to Zhenyu Zhang.

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Written informed consent from participants was obtained before they completed the questionnaires. All methods were carried out in accordance with relevant guidelines and regulations of Declaration of Helsinki.

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Highlights

• We found significant associations between exposure to metals and disinfectants and inflammatory bowel disease (IBD).

• Stronger associations were observed in females, higher income groups, and low education groups.

• Diets have a moderating effect on the associations of metal and nonmetal elements with the risk of IBD.

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Zhou, S., Chai, P., Dong, X. et al. Drinking water quality and inflammatory bowel disease: a prospective cohort study. Environ Sci Pollut Res 30, 71171–71183 (2023). https://doi.org/10.1007/s11356-023-27460-w

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