{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,14]],"date-time":"2026-09-14T15:36:30Z","timestamp":1789400190788,"version":"build-2803163510"},"reference-count":37,"publisher":"Public Library of Science (PLoS)","issue":"11","license":[{"start":{"date-parts":[[2020,11,13]],"date-time":"2020-11-13T00:00:00Z","timestamp":1605225600000},"content-version":"vor","delay-in-days":0,"URL":"http:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Helmholz Association for Cancer Research Centers"}],"content-domain":{"domain":["www.plosmedicine.org"],"crossmark-restriction":false},"short-container-title":["PLoS Med"],"abstract":"<jats:sec id=\"sec001\"><jats:title>Background<\/jats:title><jats:p>Colorectal cancer (CRC) incidence is increasing among young adults below screening age, despite the effectiveness of screening in older populations. Individuals with diabetes mellitus are at increased risk of early-onset CRC. We aimed to determine how many years earlier than the general population patients with diabetes with\/without family history of CRC reach the threshold risk at which CRC screening is recommended to the general population.<\/jats:p><\/jats:sec><jats:sec id=\"sec002\"><jats:title>Methods and findings<\/jats:title><jats:p>A nationwide cohort study (follow-up:1964\u20132015) involving all Swedish residents born after 1931 and their parents was carried out using record linkage of Swedish Population Register, Cancer Registry, National Patient Register, and Multi-Generation Register. Of 12,614,256 individuals who were followed between 1964 and 2015 (51% men; age range at baseline 0\u2013107 years), 162,226 developed CRC, and 559,375 developed diabetes. Age-specific 10-year cumulative risk curves were used to draw conclusions about how many years earlier patients with diabetes reach the 10-year cumulative risks of CRC in 50-year-old men and women (most common age of first screening), which were 0.44% and 0.41%, respectively. Diabetic patients attained the screening level of CRC risk earlier than the general Swedish population. Men with diabetes reached 0.44% risk at age 45 (5 years earlier than the recommended age of screening). In women with diabetes, the risk advancement was 4 years. Risk was more pronounced for those with additional family history of CRC (12\u201321 years earlier depending on sex and benchmark starting age of screening). The study limitations include lack of detailed information on diabetes type, lifestyle factors, and colonoscopy data.<\/jats:p><\/jats:sec><jats:sec id=\"sec003\"><jats:title>Conclusions<\/jats:title><jats:p>Using high-quality registers, this study is, to our knowledge, the first one that provides novel evidence-based information for risk-adapted starting ages of CRC screening for patients with diabetes, who are at higher risk of early-onset CRC than the general population.<\/jats:p><\/jats:sec>","DOI":"10.1371\/journal.pmed.1003431","type":"journal-article","created":{"date-parts":[[2020,11,13]],"date-time":"2020-11-13T18:22:36Z","timestamp":1605291756000},"page":"e1003431","update-policy":"https:\/\/doi.org\/10.1371\/journal.pmed.corrections_policy","source":"Crossref","is-referenced-by-count":66,"title":["Risk of colorectal cancer in patients with diabetes mellitus: A Swedish nationwide cohort study"],"prefix":"10.1371","volume":"17","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-4021-134X","authenticated-orcid":true,"given":"Uzair","family":"Ali Khan","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mahdi","family":"Fallah","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8031-279X","authenticated-orcid":true,"given":"Kristina","family":"Sundquist","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7228-5015","authenticated-orcid":true,"given":"Jan","family":"Sundquist","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6129-1572","authenticated-orcid":true,"given":"Hermann","family":"Brenner","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-4919-6641","authenticated-orcid":true,"given":"Elham","family":"Kharazmi","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"340","published-online":{"date-parts":[[2020,11,13]]},"reference":[{"key":"pmed.1003431.ref001","article-title":"Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries","author":"F Bray","year":"2018","journal-title":"CA Cancer J Clin"},{"key":"pmed.1003431.ref002","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1177\/107327481502200219","article-title":"Cost Effectiveness of Colorectal Cancer Screening Strategies","volume":"22","author":"SS Patel","year":"2015","journal-title":"Cancer Control"},{"issue":"7","key":"pmed.1003431.ref003","doi-asserted-by":"crossref","first-page":"391","DOI":"10.1038\/s41575-018-0015-8","article-title":"Personalized screening for colorectal cancer","volume":"15","author":"EJ Kuipers","year":"2018","journal-title":"Nat Rev Gastroenterol Hepatol"},{"key":"pmed.1003431.ref004","first-page":"109","article-title":"Colorectal Cancer Incidence Patterns in the United States, 1974\u20132013","author":"RL Siegel","year":"2017","journal-title":"J Natl Cancer Inst"},{"key":"pmed.1003431.ref005","article-title":"Increasing incidence of colorectal cancer in young adults in Europe over the last 25 years","author":"FE Vuik","year":"2019","journal-title":"Gut"},{"issue":"7","key":"pmed.1003431.ref006","doi-asserted-by":"crossref","first-page":"511","DOI":"10.1016\/S2468-1253(19)30147-5","article-title":"Changes in colorectal cancer incidence in seven high-income countries: a population-based study","volume":"4","author":"M Araghi","year":"2019","journal-title":"Lancet Gastroenterol Hepatol"},{"issue":"4","key":"pmed.1003431.ref007","doi-asserted-by":"crossref","first-page":"950","DOI":"10.1053\/j.gastro.2018.08.019","article-title":"Potential Intended and Unintended Consequences of Recommending Initiation of Colorectal Cancer Screening at Age 45 Years","volume":"155","author":"PS Liang","year":"2018","journal-title":"Gastroenterology"},{"key":"pmed.1003431.ref008","doi-asserted-by":"crossref","first-page":"3632","DOI":"10.3748\/wjg.v23.i20.3632","article-title":"Colorectal cancer population screening programs worldwide in 2016: An update","volume":"23","author":"M Navarro","year":"2017","journal-title":"World J Gastroenterol"},{"issue":"2","key":"pmed.1003431.ref009","doi-asserted-by":"crossref","first-page":"109","DOI":"10.1002\/1878-0261.12417","article-title":"Early-onset colorectal cancer in young individuals","volume":"13","author":"G Mauri","year":"2019","journal-title":"Mol Oncol"},{"key":"pmed.1003431.ref010","article-title":"Personal History of Diabetes as Important as Family History of Colorectal Cancer for Risk of Colorectal Cancer: A Nationwide Cohort Study","author":"U Ali Khan","year":"2020","journal-title":"Am J Gastroenterol"},{"issue":"12","key":"pmed.1003431.ref011","doi-asserted-by":"crossref","first-page":"2837","DOI":"10.1002\/cncr.32815","article-title":"Familial risk of breast cancer by dynamic, accumulative, and static definitions of family history","volume":"126","author":"T Mukama","year":"2020","journal-title":"Cancer"},{"issue":"95","key":"pmed.1003431.ref012","first-page":"1","article-title":"Cancer registration: principles and methods","author":"PD Jensen OM","year":"1991","journal-title":"IARC Sci Publ"},{"issue":"1","key":"pmed.1003431.ref013","doi-asserted-by":"crossref","DOI":"10.1053\/j.gastro.2020.03.063","article-title":"Calculating the Starting Age for Screening in Relatives of Patients With Colorectal Cancer Based on Data From Large Nationwide Data Sets","volume":"159","author":"Y Tian","year":"2020","journal-title":"Gastroenterology"},{"key":"pmed.1003431.ref014","doi-asserted-by":"crossref","first-page":"207","DOI":"10.1016\/j.ejca.2019.10.011","article-title":"Risk-tailored starting age of breast cancer screening based on women's reproductive profile: A nationwide cohort study","volume":"124","author":"T Mukama","year":"2020","journal-title":"European journal of cancer (Oxford, England: 1990)"},{"issue":"1","key":"pmed.1003431.ref015","doi-asserted-by":"crossref","first-page":"68","DOI":"10.1001\/jamaoncol.2019.3876","article-title":"Risk-Adapted Starting Age of Screening for Relatives of Patients With Breast Cancer","volume":"6","author":"T Mukama","year":"2020","journal-title":"JAMA Oncol"},{"issue":"1","key":"pmed.1003431.ref016","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1007\/s10151-019-1926-2","article-title":"Colorectal cancer in inflammatory bowel disease: review of the evidence","volume":"23","author":"DS Keller","year":"2019","journal-title":"Tech Coloproctol"},{"key":"pmed.1003431.ref017","doi-asserted-by":"crossref","first-page":"6026","DOI":"10.3748\/wjg.v21.i19.6026","article-title":"Association of type 2 diabetes mellitus and the risk of colorectal cancer: A meta-analysis and systematic review","volume":"21","author":"SY Guraya","year":"2015","journal-title":"World J Gastroenterol"},{"issue":"22","key":"pmed.1003431.ref018","doi-asserted-by":"crossref","first-page":"1679","DOI":"10.1093\/jnci\/dji375","article-title":"Diabetes mellitus and risk of colorectal cancer: a meta-analysis","volume":"97","author":"SC Larsson","year":"2005","journal-title":"J Natl Cancer Inst"},{"issue":"3","key":"pmed.1003431.ref019","doi-asserted-by":"crossref","first-page":"495","DOI":"10.2337\/dc14-1175","article-title":"The risk of colorectal cancer in patients with type 2 diabetes: associations with treatment stage and obesity","volume":"38","author":"PJ Peeters","year":"2015","journal-title":"Diabetes Care"},{"key":"pmed.1003431.ref020","doi-asserted-by":"crossref","first-page":"v6","DOI":"10.1136\/gut.51.suppl_5.v6","article-title":"Surveillance guidelines after removal of colorectal adenomatous polyps","volume":"51","author":"WS Atkin","year":"2002","journal-title":"Gut"},{"issue":"1","key":"pmed.1003431.ref021","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1053\/j.gastro.2018.03.062","article-title":"Effectiveness of Colorectal Cancer Screening in Detecting Earlier-Stage Disease-A Nationwide Cohort Study in Denmark","volume":"155","author":"MB Larsen","year":"2018","journal-title":"Gastroenterology"},{"issue":"2","key":"pmed.1003431.ref022","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1136\/gutjnl-2016-312712","article-title":"Effectiveness of screening colonoscopy in reducing the risk of death from right and left colon cancer: a large community-based study","volume":"67","author":"CA Doubeni","year":"2018","journal-title":"Gut"},{"key":"pmed.1003431.ref023","doi-asserted-by":"crossref","first-page":"262","DOI":"10.1186\/s12916-015-0498-x","article-title":"Colorectal cancer screening: the time to act is now","volume":"13","author":"H Brenner","year":"2015","journal-title":"BMC Med"},{"key":"pmed.1003431.ref024","first-page":"1090198119835294","article-title":"Costs and Cost-Effectiveness of Targeted, Personalized Risk Information to Increase Appropriate Screening by First-Degree Relatives of People With Colorectal Cancer","author":"P Reeves","year":"2019","journal-title":"Health Educ Behav"},{"issue":"1","key":"pmed.1003431.ref025","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1001\/jamaoncol.2018.4280","article-title":"Association of Obesity With Risk of Early-Onset Colorectal Cancer Among Women","volume":"5","author":"PH Liu","year":"2019","journal-title":"JAMA Oncol"},{"key":"pmed.1003431.ref026","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1001\/jama.289.1.76","article-title":"Prevalence of obesity, diabetes, and obesity-related health risk factors, 2001","volume":"289","author":"AH Mokdad","year":"2003","journal-title":"JAMA"},{"key":"pmed.1003431.ref027","doi-asserted-by":"crossref","first-page":"544","DOI":"10.1002\/cncr.24760","article-title":"Annual report to the nation on the status of cancer, 1975\u20132006, featuring colorectal cancer trends and impact of interventions (risk factors, screening, and treatment) to reduce future rates","volume":"116","author":"BK Edwards","year":"2010","journal-title":"Cancer"},{"issue":"1","key":"pmed.1003431.ref028","doi-asserted-by":"crossref","first-page":"133","DOI":"10.1158\/1055-9965.133.14.1","article-title":"Diabetes mellitus and subsite-specific colorectal cancer risks in the Iowa Women's Health Study","volume":"14","author":"PJ Limburg","year":"2005","journal-title":"Cancer Epidemiol Biomark Prev"},{"issue":"7","key":"pmed.1003431.ref029","doi-asserted-by":"crossref","first-page":"1805","DOI":"10.2337\/diacare.28.7.1805","article-title":"Diabetes and colorectal cancer incidence in the cohort of Swedish men","volume":"28","author":"SC Larsson","year":"2005","journal-title":"Diabetes Care"},{"key":"pmed.1003431.ref030","doi-asserted-by":"crossref","first-page":"980","DOI":"10.1007\/s00125-016-3884-9","article-title":"Cancer incidence in persons with type 1 diabetes: a five-country study of 9,000 cancers in type 1 diabetic individuals","volume":"59","author":"B Carstensen","year":"2016","journal-title":"Diabetologia"},{"key":"pmed.1003431.ref031","first-page":"l803","article-title":"Familial colorectal cancer risk in half siblings and siblings: nationwide cohort study","volume":"364","author":"Y Tian","year":"2019","journal-title":"BMJ (Clinical research ed)"},{"issue":"1","key":"pmed.1003431.ref032","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1002\/ijc.31043","article-title":"Status of implementation and organization of cancer screening in The European Union Member States\u2014Summary results from the second European screening report","volume":"142","author":"P Basu","year":"2018","journal-title":"Int J Cancer"},{"issue":"1","key":"pmed.1003431.ref033","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1177\/014572179001600112","article-title":"Adherence to diabetes regimens: empirical status and clinical applications","volume":"16","author":"SM Kurtz","year":"1990","journal-title":"Diabetes Educ"},{"key":"pmed.1003431.ref034","doi-asserted-by":"crossref","first-page":"k2452","DOI":"10.1136\/bmj.k2452","article-title":"Colorectal cancer: US guidelines urge screening from age 45 as incidence soars in younger adults","volume":"361","author":"O Dyer","year":"2018","journal-title":"BMJ (Clinical research ed)"},{"issue":"3","key":"pmed.1003431.ref035","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1016\/j.amjmed.2006.05.055","article-title":"Development of a risk score for colorectal cancer in men","volume":"120","author":"JA Driver","year":"2007","journal-title":"Am J Med"},{"key":"pmed.1003431.ref036","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1200\/JCO.2008.17.4797","article-title":"Colorectal cancer risk prediction tool for white men and women without known susceptibility","volume":"27","author":"AN Freedman","year":"2009","journal-title":"J Clin Oncol"},{"key":"pmed.1003431.ref037","doi-asserted-by":"crossref","first-page":"478","DOI":"10.1016\/j.cgh.2013.08.042","article-title":"Development and validation of a scoring system to identify individuals at high risk for advanced colorectal neoplasms who should undergo colonoscopy screening","volume":"12","author":"S Tao","year":"2014","journal-title":"Clin Gastroenterol Hepatol"}],"container-title":["PLOS Medicine"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pmed.1003431","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,28]],"date-time":"2022-11-28T01:04:32Z","timestamp":1669597472000},"score":1,"resource":{"primary":{"URL":"https:\/\/dx.plos.org\/10.1371\/journal.pmed.1003431"}},"subtitle":[],"editor":[{"given":"Aesun","family":"Shin","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"editor"}]}],"short-title":[],"issued":{"date-parts":[[2020,11,13]]},"references-count":37,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2020,11,13]]}},"URL":"https:\/\/doi.org\/10.1371\/journal.pmed.1003431","relation":{},"ISSN":["1549-1676"],"issn-type":[{"value":"1549-1676","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,11,13]]}}}