Cancer Incidence in a Population-Based Cohort of Patients Hospitalized With Diabetes Mellitus in Denmark
Abstract
BACKGROUND: Diabetes has been associated with an increased risk of several cancers, notably cancers of the pancreas, liver, endometrium, and kidney. Since most previous studies have involved a limited sample size or focused on specific cancer sites, we conducted a comprehensive assessment of the risk of cancer in a nationwide cohort of diabetics in Denmark. METHODS: Discharge records of 109581 individuals hospitalized with a diagnosis of diabetes from 1977 through 1989 were linked with national cancer registry records through 1993. Standardized incidence ratios (SIRs) were calculated for specific cancer sites. RESULTS: The SIRs for primary liver cancer were 4.0 (95% confidence interval [CI] = 3.5-4.6) in males and 2.1 (95% CI = 1.6-2.7) in females. These SIRs remained elevated with increasing years of follow-up and after exclusion of patients with reported risk factors (e.g., cirrhosis and hepatitis) or patients whose cancers were diagnosed at autopsy. Kidney cancer risk was also elevated, with SIRs of 1.4 (95% CI = 1.2-1.6) in males and 1.7 (95% CI = 1.4-1.9) in females. For both sexes combined, the SIR for pancreatic cancer was 2.1 (95% CI = 1.9-2.4), with a follow-up time of 1-4 years; this SIR declined to 1.3 (95% CI = 1.1-1.6) after 5-9 years of follow-up. Excess risks were also observed for biliary tract and endometrial cancers. The SIRs for kidney and endometrial cancers declined somewhat after exclusion of diabetics with reported obesity. CONCLUSIONS: Patients hospitalized with a diagnosis of diabetes appear to be at higher risk of developing cancers of the liver, biliary tract, pancreas, endometrium, and kidney. The elevated risks of endometrial and kidney cancers, however, may be confounded by obesity.
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Physical activity helps to prevent type 2 diabetes.
“Physical activity also helps to prevent type 2 diabetes, which has been associated with increased risk of cancers of the colon, pancreas, and possibly other sites.[115][116][117][118]”
Type 2 diabetes is associated with increased risk of cancers of the colon, pancreas, and possibly other sites.
“Physical activity also helps to prevent type 2 diabetes, which has been associated with increased risk of cancers of the colon, pancreas, and possibly other sites.[115][116][117][118]”
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ResultInfluentialDiabetes, metabolic syndrome, and breast cancer: a review of the current evidence
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“Conversely, results from studies in which the analysis was restricted to premenopausal women (20, 21, 30) or women of premenopausal age (26, 28) did not indicate an association between a history of diabetes and the risk of breast cancer, regardless of study design (overall summary OR 0.”
BackgroundResultInfluentialIs obesity an independent risk factor for hepatocellular carcinoma in cirrhosis?
Nair, S., Mason, A., Eason, J., Loss, G., & Perrillo, R. P. (2002) · Hepatology · doi:10.1053/jhep.2002.33713 · Cited by 348 · see citing works
The non-Hodgkin lymphomas: A review of the epidemiologic literature
Alexander, D. D., Mink, P. J., Adami, H., Chang, E. T., Cole, P. T., Mandel, J. S., & Trichopoulos, D. (2007) · International Journal of Cancer · doi:10.1002/ijc.22719 · Cited by 343 · see citing works
Byers, T., Nestle, M., McTiernan, A., Doyle, C., Currie-Williams, A., Gansler, T., & Thun, M. (2002) · CA: A Cancer Journal for Clinicians · doi:10.3322/canjclin.52.2.92 · Cited by 336 · see citing works
Eyre, H. J., Kahn, R., Robertson, R. M., Clark, N. G., Doyle, C., Gansler, T. S., Glynn, T., Hong, Y., Smith, R. A., Taubert, K. A., et al. (2004) · CA A Cancer Journal for Clinicians · doi:10.3322/canjclin.54.4.190 · Cited by 328 · see citing works
Diabetes mellitus and risk of prostate cancer: a meta-analysis
Bonovas, S., Filioussi, K., & Tsantes, A. (2004) · Diabetologia · doi:10.1007/s00125-004-1415-6 · Cited by 332 · see citing works
“Finally, we identified 25 studies examining the association between diabetes and prostate cancer [16, 17, 18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40].”
BackgroundInfluentialEpidemiology of Hepatocellular Carcinoma
El‐Serag, H. B. (2001) · Clinics in Liver Disease · doi:10.1016/s1089-3261(05)70155-0 · Cited by 327 · see citing works
van de Poll-Franse, L. V., Houterman, S., Janssen-Heijnen, M. L. G., Dercksen, M. W., Coebergh, J. W. W., & Haak, H. R. (2007) · International Journal of Cancer · doi:10.1002/ijc.22532 · Cited by 324 · see citing works
Diabetes and pancreatic cancer
Li, D. (2011) · Molecular Carcinogenesis · doi:10.1002/mc.20771 · Cited by 315 · see citing works
Endogenous Hormones and Ovarian Cancer: Epidemiology and Current Hypotheses
Lukanova, A., & Kaaks, R. (2005) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.98.14.1 · Cited by 314 · see citing works
“Type II diabetes, which is generally associated with a long history of insulin resistance and hyperinsulinemia before diagnosis and also for several years after diagnosis, also is not associated with an increased risk of ovarian cancer (179-181).”
BackgroundDiabetes mellitus and risk of hepatocellular carcinoma: a systematic review and meta‐analysis
Wang, P., Kang, D., Cao, W., Wang, Y., & Liu, Z. (2011) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.1291 · Cited by 309 · see citing works
Association of diabetes duration and diabetes treatment with the risk of hepatocellular carcinoma
Hassan, M. M., Curley, S. A., Li, D., Kaseb, A. O., Davila, M. L., Abdalla, E. K., Javle, M. M., Moghazy, D. M., Lozano, R. D., Abbruzzese, J. L., et al. (2010) · Cancer · doi:10.1002/cncr.24982 · Cited by 309 · see citing works
Diabetes mellitus and risk of bladder cancer: a meta-analysis
Larsson, S. C., Orsini, N., Brismar, K., & Wolk, A. (2006) · Diabetologia · doi:10.1007/s00125-006-0468-0 · Cited by 303 · see citing works
A Critical Analysis of the Clinical Use of Incretin-Based Therapies
Butler, P. C., Elashoff, M., Elashoff, R., & Gale, E. A. M. (2013) · Diabetes Care · doi:10.2337/dc12-2713 · Cited by 296 · see citing works
Donadon, V., Balbi, M., Mas, M. D., Casarin, P., & Zanette, G. (2010) · Liver International · doi:10.1111/j.1478-3231.2010.02223.x · Cited by 293 · see citing works
Therapy Insight: influence of type 2 diabetes on the development, treatment and outcomes of cancer
Richardson, L. C., & Pollack, L. A. (2005) · Nature Clinical Practice Oncology · doi:10.1038/ncponc0062 · Cited by 289 · see citing works
Contemporary Epidemiology of Renal Cell Cancer
Chow, W., & Devesa, S. S. (2008) · The Cancer Journal · doi:10.1097/ppo.0b013e3181867628 · Cited by 280 · see citing works
Self-citationZendehdel, K. (2003) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djg105 · Cited by 280 · see citing works
Evaluating All Potential Oral Complications of Diabetes Mellitus
Verhulst, M. J. L., Loos, B. G., Gerdes, V. E. A., & Teeuw, W. J. (2019) · Frontiers in Endocrinology · doi:10.3389/fendo.2019.00056 · Cited by 283 · see citing works
“They found that the incidence of “cancer of the mouth” was increased 2-fold in the diabetic population younger than 50 years (321).”
BackgroundFasting blood glucose and cancer risk in a cohort of more than 140,000 adults in Austria
Rapp, K., Schroeder, J. C., Klenk, J., Ulmer, H., Concin, H., Diem, G., Oberaigner, W., & Weiland, S. K. (2006) · Diabetologia · doi:10.1007/s00125-006-0207-6 · Cited by 271 · see citing works
“levels and gallbladder carcinoma and multiple myeloma are consistent with findings from a Danish record linkage study of incident cancers and hospitalisation for diabetes [1].”
BackgroundResultInfluentialMallik, R., & Chowdhury, T. A. (2018) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2018.05.023 · Cited by 266 · see citing works
Risk of cancer in a large cohort of U.S. veterans with diabetes
Atchison, E. A., Gridley, G., Carreon, J. D., Leitzmann, M. F., & McGlynn, K. A. (2010) · International Journal of Cancer · doi:10.1002/ijc.25362 · Cited by 262 · see citing works
Self-citationPancreatogenic Diabetes: Special Considerations for Management
Cui, Y., & Andersen, D. K. (2011) · Pancreatology · doi:10.1159/000329188 · Cited by 255 · see citing works
Smedby, K. E. E., Baecklund, E., & Askling, J. (2006) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-06-0300 · Cited by 248 · see citing works
Non-alcoholic Steatohepatitis and Cancer
Bugianesi, E. (2007) · Clinics in Liver Disease · doi:10.1016/j.cld.2007.02.006 · Cited by 244 · see citing works
Stocks, T., Rapp, K., Bjørge, T., Manjer, J., Ulmer, H., Selmer, R. M., Lukanova, A., Johansen, D., Concin, H., Tretli, S., et al. (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000201 · Cited by 243 · see citing works
“Type 2 diabetes has consistently been related to an increased risk of cancer at many sites [1,31,32,33], and the findings in our and the Korean study suggest that also impaired fasting glucose levels, and to a lesser extent also glucose levels within the upper normal range are associated with an…”
Hyperglycemia, a Neglected Factor during Cancer Progression
Duan, W., Shen, X., Lei, J., Xu, Q., Yu, Y., Li, R., Wu, E., & Ma, Q. (2014) · BioMed Research International · doi:10.1155/2014/461917 · Cited by 239 · see citing works
“It has been recognized that diabetes plays a crucial role in the development of solid organ malignancies including liver [10, 11], pancreatic [10, 12], colorectal [10, 13], breast [14, 15], endometrial [16–18], and bladder cancers [19, 20].”
BackgroundHistory of allergies and autoimmune diseases and risk of brain tumors in adults
Brenner, A. V., Linet, M. S., Fine, H. A., Shapiro, W. R., Selker, R. G., Black, P. M., & Inskip, P. D. (2002) · International Journal of Cancer · doi:10.1002/ijc.10320 · Cited by 232 · see citing works
Self-citationAssociation Between Hyperglycemia and Survival in Patients With Newly Diagnosed Glioblastoma
Derr, R. L., Ye, X., Islas, M. U., Desideri, S., Saudek, C. D., & Grossman, S. A. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.19.1098 · Cited by 225 · see citing works
Metabolic syndrome and cancer risk
Russo, A. G., Autelitano, M., & Bisanti, L. (2007) · European Journal of Cancer · doi:10.1016/j.ejca.2007.11.005 · Cited by 224 · see citing works
The role of diabetes mellitus in the aetiology of renal cell cancer
Lindblad, P., Chow, W. H., Chan, J., Bergström, A., Wolk, A., Gridley, G., McLaughlin, J. K., Nyrén, O., & Adami, H. O. (1999) · Diabetologia · doi:10.1007/s001250051122 · Cited by 220 · see citing works
“Excess risks have also been reported in some cohort studies of patients with diabetes [17, 18], while others found no association [19±21].”
BackgroundSelf-citationJiang, Y., Ben, Q., Shen, H., Lu, W., Zhang, Y., & Zhu, J. (2011) · European Journal of Epidemiology · doi:10.1007/s10654-011-9617-y · Cited by 220 · see citing works
Hepatitis B Virus Infection and Intrahepatic Cholangiocarcinoma in Korea: A Case-Control Study
Lee, T. Y., Lee, S. S., Jung, S. W., Jeon, S. H., Yun, S.-C., Oh, H., Kwon, S., Lee, S. K., Seo, D. W., Kim, M., et al. (2008) · The American Journal of Gastroenterology · doi:10.1111/j.1572-0241.2008.01796.x · Cited by 217 · see citing works
“In agreement with previous findings (22, 27, 28), our results also suggest associations between heavy alcohol consumption and diabetes and risk of ICC.”
ResultAdvances in diagnosis, treatment and palliation of pancreatic carcinoma: 1990-2010
Sharma, C. (2011) · World Journal of Gastroenterology · doi:10.3748/wjg.v17.i7.867 · Cited by 214 · see citing works
S3-Leitlinie zum exokrinen Pankreaskarzinom
Seufferlein, T. T. W., Porzner, M., Becker, T., Budach, V., Ceyhan, G. O., Esposito, I., Fietkau, R., Follmann, M., Frieß, H., Galle, P. R., et al. (2013) · Zeitschrift für Gastroenterologie · doi:10.1055/s-0033-1356220 · Cited by 213 · see citing works
Castillo, J. J., Mull, N. K., Reagan, J. L., Nemr, S., & Mitri, J. (2012) · Blood · doi:10.1182/blood-2011-06-362830 · Cited by 212 · see citing works
Risk Factors for Renal Cell Cancer: The Multiethnic Cohort
Setiawan, V. W., Stram, D. O., Nomura, A. M. Y., Kolonel, L. N., & Henderson, B. E. (2007) · American Journal of Epidemiology · doi:10.1093/aje/kwm170 · Cited by 211 · see citing works
“Diabetes has been shown to increase risk (20, 21), but whether the association is truly causal or confounded by obesity is unclear (4, 20).”
BackgroundThe impact of obesity and diabetes mellitus on the risk of hepatocellular carcinoma
Polesel, J., Zucchetto, A., Montella, M., Maso, L. D., Crispo, A., Vecchia, C. L., Serraino, D., Franceschi, S., & Talamini, R. (2008) · Annals of Oncology · doi:10.1093/annonc/mdn565 · Cited by 210 · see citing works
The relationship between diabetes and pancreatic cancer.
Wang, F., Herrington, M. K., Larsson, J., & Permert, J. (2003) · Molecular Cancer · doi:10.1186/1476-4598-2-4 · Cited by 198 · see citing works
Liver Disease in Patients With Diabetes Mellitus
Harrison, S. A. (2005) · Journal of Clinical Gastroenterology · doi:10.1097/01.mcg.0000190774.91875.d2 · Cited by 197 · see citing works
Welzel, T. M., Mellemkjaer, L., Gloria, G., Sakoda, L. C., Hsing, A. W., Ghormli, L. E., Olsen, J. H., & McGlynn, K. A. (2007) · International Journal of Cancer · doi:10.1002/ijc.22283 · Cited by 195 · see citing works
Self-citationPancreatic cancer in type 1 and young-onset diabetes: systematic review and meta-analysis
Stevens, R., Roddam, A. W., & Beral, V. (2007) · British Journal of Cancer · doi:10.1038/sj.bjc.6603571 · Cited by 194 · see citing works
“…three cohort and six case–control studies that reported pancreatic cancer by diabetes subtype (O’Mara et al, 1985; Bueno De Mesquita et al, 1992; Ekoe et al, 1992; Gullo et al, 1994; La Vecchia et al, 1994; Wideroff et al, 1997; Silverman et al, 1999; Zendehdel et al, 2003; Swerdlow et al, 2005).”
Ohkuma, T., Peters, S. A. E., & Woodward, M. (2018) · Diabetologia · doi:10.1007/s00125-018-4664-5 · Cited by 188 · see citing works
Cancer incidence and mortality in patients with insulin-treated diabetes: a UK cohort study
Swerdlow, A. J., Laing, S. P., Qiao, Z., Slater, S. D., Burden, A. C., Botha, J. L., Waugh, N. R., Morris, A. D., Gatling, W., Gale, E. A. M., et al. (2005) · British Journal of Cancer · doi:10.1038/sj.bjc.6602611 · Cited by 190 · see citing works
“…et al , 1976; Ragozzino et al , 1982; Green and Jensen, 1985; O’Mara et al , 1985; Adami et al , 1991; La Vecchia et al , 1994; Hjalgrim et al , 1997; Wideroff et al , 1997; Verlato et al , 2003), but interpretation is uncertain because of potential confounding by obesity and alcohol consumption.”
InfluentialMcGlynn, K. A., Tarone, R. E., & El‐Serag, H. B. (2006) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-05-0811 · Cited by 190 · see citing works
“A Danish cohort study reported an association between diabetes and PLC in Denmark (38).”
BackgroundMarkers of insulin resistance and colorectal cancer mortality.
Trevisan, M., Liu, J., Muti, P. C., Misciagna, G., Menotti, A., & Fucci, F. (2001) · PubMed · Cited by 189 · see citing works
Type 2 diabetes and hepatocellular carcinoma
Lai, M., Hsieh, M., Chiu, Y., & Chen, T. H. (2006) · Hepatology · doi:10.1002/hep.21208 · Cited by 187 · see citing works
Association of Diabetes Mellitus and Pancreatic Adenocarcinoma: A Meta-Analysis of 88 Studies
Batabyal, P., Hoorn, S. V., Christophi, C., & Nikfarjam, M. (2014) · Annals of Surgical Oncology · doi:10.1245/s10434-014-3625-6 · Cited by 186 · see citing works
Diabetes and Risk of Prostate Cancer in a Prospective Cohort of US Men
Rodriguez, C. (2005) · American Journal of Epidemiology · doi:10.1093/aje/kwh334 · Cited by 185 · see citing works
on behalf of the Diabetes and Cancer Research Consortium, Carstensen, B., Read, S. H., Friis, S., Sund, R., Keskimäki, I., Svensson, A.-M., Ljung, R., Wild, S. H., Kerssens, J. J., et al. (2016) · Diabetologia · doi:10.1007/s00125-016-3884-9 · Cited by 180 · see citing works
“Although this definition of type 1 diabetes is not strictly comparable with ours, the result is consistent with our findings [19].”
ResultDiabetes mellitus and incidence of kidney cancer: a meta-analysis of cohort studies
Larsson, S. C., & Wolk, A. (2011) · Diabetologia · doi:10.1007/s00125-011-2051-6 · Cited by 182 · see citing works
“The outcome was renal cell carcinoma in three studies [20, 23, 25], and total or unspecified kidney cancer in six studies [18, 21, 22, 24, 26, 27].”
BackgroundMethodInfluentialNonalcoholic Fatty Liver Disease, Diabetes, Obesity, and Hepatocellular Carcinoma
Noureddin, M., & Rinella, M. E. (2015) · Clinics in Liver Disease · doi:10.1016/j.cld.2015.01.012 · Cited by 181 · see citing works
Salomao, M. A., Remotti, H. E., VAUGHAN, R. D., Siegel, A. B., Lefkowitch, J. H., & Moreira, R. K. (2011) · Human Pathology · doi:10.1016/j.humpath.2011.07.005 · Cited by 180 · see citing works
“First, although mounting evidence that a significant association between HCC and NAFLD/metabolic syndrome exists [5-12,25,26,28-33], the”
BackgroundAnothaisintawee, T., Wiratkapun, C., Lerdsitthichai, P., Kasamesup, V., Wongwaisayawan, S., Srinakarin, J., Hirunpat, S., Woodtichartpreecha, P., Boonlikit, S., Teerawattananon, Y., et al. (2013) · Asia Pacific Journal of Public Health · doi:10.1177/1010539513488795 · Cited by 179 · see citing works
- Authors
- Wideroff, L., Gridley, G., Chow, W. H., Linet, M., Mellemkjaer, L., Olsen, J. H., Keehn, S., & Borch-Johnsen, K.
- Affiliations
- National Institutes of Health (US)
- National Cancer Institute (US)
- Danish Cancer Society (DK)
- Information Management Services (US)
- University of Copenhagen (DK)
- Corresponding author
- Wideroff, L.
- ORCID
- Olsen, J. H.
- Venue
- JNCI Journal of the National Cancer Institute
- Publisher
- Oxford University Press (OUP)
- Published
- 1997-09-17
- Volume
- 89
- Issue
- 18
- Pages
- 1360-1365
- ISSN
- 0027-8874 (ISSN-L)
- 1460-2105
- OpenAlex
- W2122576167
- Cited by
- 627
- References
- 42
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 9 · 2023: 13 · 2022: 14 · 2021: 16 · 2020: 8 · 2019: 19 · 2018: 12 · 2017: 20 · 2016: 20 · 2015: 28 · 2014: 38 · 2013: 43 · 2012: 42
- FWCI
- 2.26
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- JNCI Journal of the National Cancer Institute (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Oncology › Cancer Risks and Factors
- Health Sciences › Medicine › Oncology › Global Cancer Incidence and Screening
- Keywords
- diabetes mellitus, cancer incidence, liver cancer, pancreatic cancer, kidney cancer, endometrial cancer, biliary tract cancer, obesity, standardized incidence ratio, diabetes and cancer association
- MeSH terms
- Denmark, Female, Hospitalization, Humans, Male, Medical Record Linkage, Middle Aged, Neoplasms, Registries, Risk, Cohort Studies, Incidence, Age Distribution, Sex Distribution, Diabetes Complications
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