{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,11,10]],"date-time":"2026-11-10T01:40:35Z","timestamp":1794274835756,"version":"4.9.0"},"reference-count":51,"publisher":"Oxford University Press (OUP)","issue":"12","license":[{"start":{"date-parts":[[2020,6,23]],"date-time":"2020-06-23T00:00:00Z","timestamp":1592870400000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by-nc\/4.0\/"}],"funder":[{"name":"Junior Scientific Masterclass","award":["16\u201322"],"award-info":[{"award-number":["16\u201322"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2020,12,2]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec><jats:title>Background and Aims<\/jats:title><jats:p>Multiple genetic and environmental factors are involved in the aetiology of inflammatory bowel disease [IBD] including Crohn\u2019s disease [CD] and ulcerative colitis [UC], but data on these exposome factors are difficult to identify. Several exposome factors such as smoking have been shown to be involved; as for other environmental factors, eg stress, results have been conflicting.<\/jats:p><\/jats:sec><jats:sec><jats:title>Methods<\/jats:title><jats:p>We performed a case-control study including 674 IBD patients of the 1000IBD cohort, frequency-matched based on sex and age with 1348 controls from the population-based Lifelines Cohort Study. Exposome data were obtained using the validated Groningen IBD Environmental Questionnaire [GIEQ], capturing exposome factors through different stages of life using 844 items, of which 454 were applicable to study the role of 93 exposome factors in disease aetiology. Logistic regression [LR] modelling with Bonferroni correction for multiple testing was applied to estimate the multivariable-adjusted effect of each exposome factor.<\/jats:p><\/jats:sec><jats:sec><jats:title>Results<\/jats:title><jats:p>For IBD, we identified four novel factors: stressful life events (CD odds ratio [OR] 2.61\/UC OR 2.92), high perceived stress [2.29\/2.67], alcohol use [0.40\/0.43], and bronchial hyper-reactivity [3.04\/2.36]. Four novel factors were associated with only CD: prenatal smoke exposure [1.89], having a bed partner [0.53], allergies [2.66], and cow\u2019s milk hypersensitivity [5.87]; and two solely with UC: carpet flooring [0.57] and neuroticism [1.32]. Nine factors were replicated.<\/jats:p><\/jats:sec><jats:sec><jats:title>Conclusions<\/jats:title><jats:p>In this study we identified 10 novel, and replicated nine previously reported, exposome factors associated with IBD. Identifying these factors is important for both understanding disease aetiology and future prevention strategies to decrease the development of IBD in genetically susceptible persons.<\/jats:p><\/jats:sec>","DOI":"10.1093\/ecco-jcc\/jjaa114","type":"journal-article","created":{"date-parts":[[2020,6,5]],"date-time":"2020-06-05T19:24:04Z","timestamp":1591385044000},"page":"1662-1671","source":"Crossref","is-referenced-by-count":44,"title":["Identification of Environmental Risk Factors Associated With the Development of Inflammatory Bowel Disease"],"prefix":"10.1093","volume":"14","author":[{"given":"Kimberley W J","family":"van der Sloot","sequence":"first","affiliation":[{"name":"Department of Gastroenterology and Hepatology, University of Groningen and University Medical Center Groningen, Groningen, The Netherlands"},{"name":"Department of Epidemiology, University of Groningen and University Medical Center Groningen, Groningen, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rinse K","family":"Weersma","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Hepatology, University of Groningen and University Medical Center Groningen, Groningen, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Behrooz Z","family":"Alizadeh","sequence":"additional","affiliation":[{"name":"Department of Epidemiology, University of Groningen and University Medical Center Groningen, Groningen, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gerard","family":"Dijkstra","sequence":"additional","affiliation":[{"name":"Department of Gastroenterology and Hepatology, University of Groningen and University Medical Center Groningen, Groningen, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2020,6,23]]},"reference":[{"key":"2020120619083624200_CIT0001","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1038\/nrgastro.2015.34","article-title":"Epidemiology and risk factors for IBD","volume":"12","author":"Ananthakrishnan","year":"2015","journal-title":"Nat Rev Gastroenterol Hepatol"},{"key":"2020120619083624200_CIT0002","doi-asserted-by":"crossref","first-page":"1499","DOI":"10.1097\/MIB.0000000000001217","article-title":"Inflammatory bowel diseases: review of known environmental protective and risk factors involved","volume":"23","author":"van der Sloot","year":"2017","journal-title":"Inflamm Bowel Dis"},{"key":"2020120619083624200_CIT0003","doi-asserted-by":"crossref","first-page":"46","DOI":"10.1053\/j.gastro.2011.10.001","article-title":"Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review","volume":"142","author":"Molodecky","year":"2012","journal-title":"Gastroenterology"},{"key":"2020120619083624200_CIT0004","doi-asserted-by":"crossref","first-page":"267","DOI":"10.1038\/s41577-019-0156-1","article-title":"The Western lifestyle has lasting effects on metaflammation","volume":"19","author":"Christ","year":"2019","journal-title":"Nat Rev Immunol"},{"key":"2020120619083624200_CIT0005","doi-asserted-by":"crossref","first-page":"1462","DOI":"10.4065\/81.11.1462","article-title":"Smoking and inflammatory bowel disease: a meta-analysis","volume":"81","author":"Mahid","year":"2006","journal-title":"Mayo Clin Proc"},{"key":"2020120619083624200_CIT0006","doi-asserted-by":"crossref","first-page":"165","DOI":"10.3748\/wjg.14.165","article-title":"Hygiene hypothesis in inflammatory bowel disease: a critical review of the literature","volume":"14","author":"Koloski","year":"2008","journal-title":"World J Gastroenterol"},{"key":"2020120619083624200_CIT0007","doi-asserted-by":"crossref","first-page":"1775","DOI":"10.1111\/j.1572-0241.2008.01905.x","article-title":"Childhood hygiene is associated with the risk for inflammatory bowel disease: a population-based study","volume":"103","author":"Klement","year":"2008","journal-title":"Am J Gastroenterol"},{"key":"2020120619083624200_CIT0008","first-page":"607","article-title":"Environmental factors in a population-based inception cohort of inflammatory bowel disease patients in Europe\u2014An ECCO-EpiCom study for the EpiCom-group. J Crohns Colitis","author":"Burisch","year":"2014"},{"key":"2020120619083624200_CIT0009","doi-asserted-by":"crossref","first-page":"79","DOI":"10.1016\/j.crohns.2012.05.024","article-title":"Environmental factors and risk of developing paediatric inflammatory bowel disease\u2014A population-based study 2007\u20132009","volume":"7","author":"Jakobsen","year":"2013","journal-title":"J Crohns Colitis"},{"key":"2020120619083624200_CIT0010","doi-asserted-by":"crossref","first-page":"325","DOI":"10.1111\/j.1440-1746.2009.06140.x","article-title":"Population-based case-control study of inflammatory bowel disease risk factors","volume":"25","author":"Gearry","year":"2010","journal-title":"J Gastroenterol Hepatol"},{"key":"2020120619083624200_CIT0011","doi-asserted-by":"crossref","first-page":"1063","DOI":"10.1136\/gutjnl-2014-307410","article-title":"Environmental risk factors in inflammatory bowel disease: a population-based case-control study in Asia-Pacific","volume":"64","author":"Ng","year":"2015","journal-title":"Gut"},{"key":"2020120619083624200_CIT0012","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1186\/s12876-019-0938-8","article-title":"Correction to: The 1000IBD project: multi-omics data of 1000 inflammatory bowel disease patients; data release 1","volume":"19","author":"Imhann","year":"2019","journal-title":"BMC Gastroenterol"},{"key":"2020120619083624200_CIT0013","doi-asserted-by":"crossref","first-page":"238","DOI":"10.1007\/s00535-018-1501-z","article-title":"Development and validation of a web-based questionnaire to identify environmental risk factors for inflammatory bowel disease: the Groningen IBD Environmental Questionnaire [GIEQ]","volume":"54","author":"van der Sloot","year":"2019","journal-title":"J Gastroenterol"},{"key":"2020120619083624200_CIT0014","doi-asserted-by":"crossref","first-page":"1172","DOI":"10.1093\/ije\/dyu229","article-title":"Cohort Profile: LifeLines, a three-generation cohort study and biobank","volume":"44","author":"Scholtens","year":"2015","journal-title":"Int J Epidemiol"},{"key":"2020120619083624200_CIT0015","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1016\/j.psychres.2016.04.004","article-title":"The Five-Factor Model personality traits in schizophrenia: A meta-analysis","volume":"240","author":"Ohi","year":"2016","journal-title":"Psychiatry Res"},{"key":"2020120619083624200_CIT0016","doi-asserted-by":"crossref","first-page":"743","DOI":"10.3748\/wjg.v17.i6.743","article-title":"Perinatal and early life risk factors for inflammatory bowel disease","volume":"17","author":"Roberts","year":"2011","journal-title":"World J Gastroenterol"},{"key":"2020120619083624200_CIT0017","doi-asserted-by":"crossref","first-page":"312","DOI":"10.1016\/j.fct.2019.04.059","article-title":"Smoking and DNA methylation: Correlation of methylation with smoking behavior and association with diseases and fetus development following prenatal exposure","volume":"129","author":"Fragou","year":"2019","journal-title":"Food Chem Toxicol"},{"key":"2020120619083624200_CIT0018","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1007\/s12519-019-00278-8","article-title":"Impact of maternal smoking on the infant gut microbiota and its association with child overweight: a scoping review","volume":"15","author":"McLean","year":"2019","journal-title":"World J Pediatr"},{"key":"2020120619083624200_CIT0019","first-page":"905","article-title":"European Crohn's and Colitis Organisation Topical Review on Environmental Factors in IBD","author":"Maaser","year":"2017;11","journal-title":"J Crohns Colitis"},{"key":"2020120619083624200_CIT0020","doi-asserted-by":"crossref","first-page":"542","DOI":"10.1097\/MIB.0b013e31828132f8","article-title":"Early life factors and risk of inflammatory bowel disease in adulthood","volume":"19","author":"Khalili","year":"2013","journal-title":"Inflamm Bowel Dis"},{"key":"2020120619083624200_CIT0021","doi-asserted-by":"crossref","first-page":"1342","DOI":"10.1093\/ajcn\/80.5.1342","article-title":"Breastfeeding and risk of inflammatory bowel disease: a systematic review with meta-analysis","volume":"80","author":"Klement","year":"2004","journal-title":"Am J Clin Nutr"},{"key":"2020120619083624200_CIT0022","first-page":"109","volume-title":"Smoking, breastfeeding, physical inactivity, contact with animals, and size of the family influence the risk of inflammatory bowel disease: A Slovak case-control study","author":"Hlavaty","year":"2013"},{"key":"2020120619083624200_CIT0023","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1016\/j.cgh.2015.02.045","article-title":"Inflammatory bowel disease environmental risk factors: a population-based case-control study of Middle Eastern migration to Australia","volume":"13","author":"Ko","year":"2015","journal-title":"Clin Gastroenterol Hepatol"},{"key":"2020120619083624200_CIT0024","doi-asserted-by":"crossref","first-page":"131","DOI":"10.1016\/j.crohns.2007.10.006","article-title":"Prevalence of inflammatory bowel disease in the Canton of Vaud [Switzerland]: A population-based cohort study","volume":"2","author":"Juillerat","year":"2008","journal-title":"J Crohns Colitis"},{"key":"2020120619083624200_CIT0025","doi-asserted-by":"crossref","first-page":"553","DOI":"10.1038\/ajg.2015.52","article-title":"Inflammatory bowel disease in immigrants to Canada and their children: a population-based cohort study","volume":"110","author":"Benchimol","year":"2015","journal-title":"Am J Gastroenterol"},{"key":"2020120619083624200_CIT0026","doi-asserted-by":"crossref","first-page":"2918","DOI":"10.1111\/j.1572-0241.1999.01438.x","article-title":"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]","volume":"94","author":"Carr","year":"1999","journal-title":"Am J Gastroenterol"},{"key":"2020120619083624200_CIT0027","doi-asserted-by":"crossref","first-page":"566","DOI":"10.1016\/j.crohns.2011.05.009","article-title":"Emigration to Western industrialised countries: A risk factor for developing inflammatory bowel disease","volume":"5","author":"Barreiro-de Acosta","year":"2011","journal-title":". Crohns Colitis"},{"key":"2020120619083624200_CIT0028","doi-asserted-by":"crossref","first-page":"879","DOI":"10.1097\/MEG.0000000000000899","article-title":"Literature review","volume":"29","author":"Wardle","year":"2017","journal-title":"Eur J Gastroenterol Hepatol"},{"key":"2020120619083624200_CIT0029","doi-asserted-by":"crossref","first-page":"247","DOI":"10.2174\/156652408784533832","article-title":"The role of stress in the development and clinical course of inflammatory bowel disease: epidemiological evidence","volume":"8","author":"Maunder","year":"2008","journal-title":"Curr Mol Med"},{"key":"2020120619083624200_CIT0030","doi-asserted-by":"crossref","first-page":"122","DOI":"10.1111\/j.1572-0241.2006.00931.x","article-title":"Stressful life events as a risk factor for inflammatory bowel disease onset: A population-based case-control study","volume":"102","author":"Lerebours","year":"2007","journal-title":"Am J Gastroenterol"},{"key":"2020120619083624200_CIT0031","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1111\/j.1572-0241.2004.04155.x","article-title":"Psychological stress and inflammatory bowel disease: a follow-up study in parents who lost a child in Denmark","volume":"99","author":"Li","year":"2004","journal-title":"Am J Gastroenterol"},{"key":"2020120619083624200_CIT0032","first-page":"718","article-title":"Sleep and inflammatory bowel disease: exploring the relationship between sleep disturbances and inflammation","volume":"9","author":"Kinnucan","year":"2013","journal-title":"Gastroenterol Hepatol [N Y]"},{"key":"2020120619083624200_CIT0033","doi-asserted-by":"crossref","first-page":"1879","DOI":"10.1016\/j.cgh.2014.04.021","article-title":"Sleep duration affects risk for ulcerative colitis: a prospective cohort study","volume":"12","author":"Ananthakrishnan","year":"2014","journal-title":"Clin Gastroenterol Hepatol"},{"key":"2020120619083624200_CIT0034","doi-asserted-by":"crossref","first-page":"200","DOI":"10.1093\/sleep\/32.2.200","article-title":"Sleep duration and biomarkers of inflammation","volume":"32","author":"Patel","year":"2009","journal-title":"Sleep"},{"key":"2020120619083624200_CIT0035","doi-asserted-by":"crossref","first-page":"1425","DOI":"10.1016\/j.dld.2016.08.129","article-title":"Association between physical activity and inflammatory bowel disease risk: A meta-analysis","volume":"48","author":"Wang","year":"2016","journal-title":"Dig Liver Dis"},{"key":"2020120619083624200_CIT0036","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1038\/nature10758","article-title":"Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis","volume":"481","author":"He","year":"2012","journal-title":"Nature"},{"key":"2020120619083624200_CIT0037","doi-asserted-by":"crossref","first-page":"e0221961","DOI":"10.1371\/journal.pone.0221961","article-title":"Global smoking trends in inflammatory bowel disease: A systematic review of inception cohorts","volume":"14","author":"Thomas","year":"2019","journal-title":"PLoS One"},{"key":"2020120619083624200_CIT0038","doi-asserted-by":"crossref","first-page":"1304","DOI":"10.3748\/wjg.v16.i11.1304","article-title":"Alcohol, inflammation, and gut-liver-brain interactions in tissue damage and disease development","volume":"16","author":"Wang","year":"2010","journal-title":"World J Gastroenterol"},{"key":"2020120619083624200_CIT0039","doi-asserted-by":"crossref","first-page":"304","DOI":"10.1038\/s41430-017-0028-3","article-title":"Controversial role of alcohol consumption in the development of inflammatory bowel diseases","volume":"72","author":"Yang","year":"2018","journal-title":"Eur J Clin Nutr"},{"key":"2020120619083624200_CIT0040","doi-asserted-by":"crossref","first-page":"e9070","DOI":"10.1097\/MD.0000000000009070","article-title":"Beverage consumption and risk of ulcerative colitis: Systematic review and meta-analysis of epidemiological studies","volume":"96","author":"Nie","year":"2017","journal-title":"Medicine [Baltimore]"},{"key":"2020120619083624200_CIT0041","doi-asserted-by":"crossref","first-page":"512","DOI":"10.1038\/ejcn.2016.271","article-title":"No association of alcohol use and the risk of ulcerative colitis or Crohn\u2019s disease: data from a European Prospective cohort study [EPIC]","volume":"71","author":"Bergmann","year":"2017","journal-title":"Eur J Clin Nutr"},{"key":"2020120619083624200_CIT0042","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1007\/s40264-015-0372-y","article-title":"Risk of inflammatory bowel disease with oral contraceptives and menopausal hormone therapy: current evidence and future directions","volume":"39","author":"Khalili","year":"2016","journal-title":"Drug Saf"},{"key":"2020120619083624200_CIT0043","doi-asserted-by":"crossref","first-page":"2394","DOI":"10.1111\/j.1572-0241.2008.02064.x","article-title":"The risk of oral contraceptives in the etiology of inflammatory bowel disease: a meta-analysis","volume":"103","author":"Cornish","year":"2008","journal-title":"Am J Gastroenterol"},{"key":"2020120619083624200_CIT0044","doi-asserted-by":"crossref","first-page":"1614","DOI":"10.1038\/ajg.2016.464","article-title":"Oral contraceptive use and risk of ulcerative colitis progression: a nationwide study","volume":"111","author":"Khalili","year":"2016","journal-title":"Am J Gastroenterol"},{"key":"2020120619083624200_CIT0045","doi-asserted-by":"crossref","first-page":"171","DOI":"10.1111\/j.1572-0241.2000.01680.x","article-title":"Appendectomy and the development of ulcerative colitis: results of a metaanalysis of published case-control studies","volume":"95","author":"Koutroubakis","year":"2000","journal-title":"Am J Gastroenterol"},{"key":"2020120619083624200_CIT0046","doi-asserted-by":"crossref","first-page":"2925","DOI":"10.1111\/j.1572-0241.2008.02118.x","article-title":"The risk of developing Crohn\u2019s disease after an appendectomy: a meta-analysis","volume":"103","author":"Kaplan","year":"2008","journal-title":"Am J Gastroenterol"},{"key":"2020120619083624200_CIT0047","doi-asserted-by":"crossref","first-page":"36","DOI":"10.1067\/msy.2001.115362","article-title":"Appendectomy and subsequent risk of inflammatory bowel diseases","volume":"130","author":"Frisch","year":"2001","journal-title":"Surgery"},{"key":"2020120619083624200_CIT0048","volume-title":"Control of Immune Pathology by Regulatory T Cells","author":"Powrie","year":"2008"},{"key":"2020120619083624200_CIT0049","doi-asserted-by":"crossref","first-page":"1085","DOI":"10.1111\/jgh.13273","article-title":"Tonsillectomy and the risk of inflammatory bowel disease: A systematic review and meta-analysis","volume":"31","author":"Sun","year":"2016","journal-title":"J Gastroenterol Hepatol"},{"key":"2020120619083624200_CIT0050","doi-asserted-by":"crossref","first-page":"256","DOI":"10.1097\/EDE.0000000000000946","article-title":"Increased risk of inflammatory bowel disease in families with tonsillectomy: A Danish National Cohort Study","volume":"30","author":"Bager","year":"2019","journal-title":"Epidemiology"},{"key":"2020120619083624200_CIT0051","first-page":"282","article-title":"Prevalence of allergic diseases in children with inflammatory bowel disease","volume":"36","author":"Wasielewska","year":"2019","journal-title":"Postepy Dermatol Alergol"}],"container-title":["Journal of Crohn's and Colitis"],"original-title":[],"language":"en","link":[{"URL":"http:\/\/academic.oup.com\/ecco-jcc\/advance-article-pdf\/doi\/10.1093\/ecco-jcc\/jjaa114\/33558134\/jjaa114.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/ecco-jcc\/article-pdf\/14\/12\/1662\/34665099\/jjaa114.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"http:\/\/academic.oup.com\/ecco-jcc\/article-pdf\/14\/12\/1662\/34665099\/jjaa114.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,3,18]],"date-time":"2021-03-18T23:11:28Z","timestamp":1616109088000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/ecco-jcc\/article\/14\/12\/1662\/5861037"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,6,23]]},"references-count":51,"journal-issue":{"issue":"12","published-online":{"date-parts":[[2020,6,23]]},"published-print":{"date-parts":[[2020,12,2]]}},"URL":"https:\/\/doi.org\/10.1093\/ecco-jcc\/jjaa114","relation":{},"ISSN":["1873-9946","1876-4479"],"issn-type":[{"value":"1873-9946","type":"print"},{"value":"1876-4479","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2020,12,1]]},"published":{"date-parts":[[2020,6,23]]}}}