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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 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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“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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“Number 5,085 5,115 5,037 5,077 3,805 3,748 3,780 3,773 Age (y)* 33 (22, 56) 38 (25, 57) 41 (26, 58) 43 (26, 59) 27 (20, 53) 39 (21, 57) 45 (22, 59) 48 (25, 61) Plasma glucose (mg/dL)* 115 (83, 175) 123 (87, 185) 129 (90, 194) 136 (95, 205) 111 (82, 170) 118 (85, 180) 122 (87, 188) 134 (92, 196)”
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A cohort study of antihypertensive treatments and risk of renal cell cancer
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“Finally, diabetes has been associated with an increased prevalence of certain cancers, such as endometrial, liver, biliary, pancreatic and renal [63], due to an enhanced propensity for neovascularization of these tumours in diabetic patients.”
Insulin Resistance: Any Role in the Changing Epidemiology of Thyroid Cancer?
Malaguarnera, R., Vella, V., Nicolosi, M. L., & Belfiore, A. (2017) · Frontiers in Endocrinology · doi:10.3389/fendo.2017.00314 · Cited by 68
“Despite of a high heterogeneity among studies, the observation that the risk is increased among diabetic women, but not among men, has been always confirmed (37, 46, 233).”
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BackgroundResultInfluentialDiabetes and Risk of Renal Cell Carcinoma
Habib, S. L., Prihoda, T. J., Luna, M., & Werner, S. A. (2012) · Journal of Cancer · doi:10.7150/jca.3718 · Cited by 61
“Epidemiologic studies have shown that patients with type 1 and type 2 diabetes mellitus (DM) are at higher risk than the general population for developing certain malignancies including kidney, liver, biliary tract, pancreas and colon [1-6].”
BackgroundThe biological and pharmacological connections between diabetes and various types of cancer
Wang, X., & Ding, S. (2021) · Pathology - Research and Practice · doi:10.1016/j.prp.2021.153641 · Cited by 60
Evert, M., Calvisi, D. F., Evert, K., Murtas, V. D., Gasparetti, G., Mattu, S., Destefanis, G., Ladu, S., Zimmermann, A., Delogu, S., et al. (2012) · Hepatology · doi:10.1002/hep.25600 · Cited by 61
“Accordingly, recent investigations indicate that T2DM people are at a significantly higher risk to develop liver cancer than normoglycemic people.(1,10-13) Furthermore, although highly debated, recent studies suggest that treatment with insulin analogs, such as insulin glargine, increases the incidence of various tumo…”
BackgroundChao, L.-T., Wu, C. F., Sung, F.-Y., Lin, C., Liu, C., Huang, C.-J., Tsai, K., & Yu, M. (2011) · Carcinogenesis · doi:10.1093/carcin/bgr058 · Cited by 60
Reduced risk of prostate cancer among patients with diabetes mellitus
Weiderpass, E., Ye, W., Vainio, H., Kaaks, R., & Adami, H. (2002) · International Journal of Cancer · doi:10.1002/ijc.10685 · Cited by 60
Association between Liver Cirrhosis and Diabetes Mellitus: A Review on Hepatic Outcomes
Coman, L. I., Coman, O. A., Bădărău, I. A., Păunescu, H., & Ciocîrlan, M. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10020262 · Cited by 59
Czyżyk, A., & Szczepanik, Z. (2000) · European Journal of Internal Medicine · doi:10.1016/s0953-6205(00)00106-0 · Cited by 59
“Similarly, a retrospective or over 50 years of age when they entered the cohort study ̈ study in Zurich during the years 1971–1988 showed that [11].”
BackgroundInfluentialInsulin and IGFs in renal cancer risk and progression
Solarek, W., Czarnecka, A. M., Escudier, B. J., Bielecka, Z. F., Lian, F., & Szczylik, C. A. (2015) · Endocrine Related Cancer · doi:10.1530/erc-15-0135 · Cited by 59
Diabetes Mellitus and Risk of Bladder Cancer: A Meta-Analysis of Cohort Studies
Xu, X., Wu, J., Mao, Y., Zhu, Y., Hu, Z., Xu, X., Lin, Y., Chen, H., Zheng, X., Qin, J., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0058079 · Cited by 58
Lee, J. E., Giovannucci, E. L., Smith‐Warner, S. A., Spiegelman, D. L., Willett, W. C., & Curhan, G. C. (2006) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-05-0889 · Cited by 58
“Individuals with type 2 diabetes, which results from reduced insulin sensitivity (69), may be more likely to develop renal cell cancer (12, 13).”
BackgroundGuo, J., Liu, C., Pan, J., & Yang, J. (2022) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2022.109866 · Cited by 57
Khan, A. E., Gallo, V., Linseisen, J., Kaaks, R., Rohrmann, S., Raaschou‐Nielsen, O., Tjønneland, A. M., Johnsen, H. E., Overvad, K., Bergmann, M. M., et al. (2008) · Haematologica · doi:10.3324/haematol.12297 · Cited by 61
Vavallo, A., Simone, S., Lucarelli, G. T., Rutigliano, M., Galleggiante, V., Grandaliano, G., Gesualdo, L., Campagna, M., Cariello, M., Ranieri, E., et al. (2014) · Medicine · doi:10.1097/md.0000000000000183 · Cited by 57
Glucose intolerance and adenomas of the sigmoid colon in Japanese men (Japan)
Kono, S., Honjo, S., Todoroki, I., Nishiwaki, M., Hamada, H., Nishikawa, H., Koga, H., Ogawa, S., & Nakagawa, K. (1998) · Cancer Causes & Control · doi:10.1023/a:1008879920140 · Cited by 57
Type 2 Diabetes Mellitus and Risk of Non-Hodgkin Lymphoma: A Systematic Review and Meta-Analysis
Chao, C., & Page, J. H. (2008) · American Journal of Epidemiology · doi:10.1093/aje/kwn160 · Cited by 56
Rotbain, E. C., Niemann, C. U., Rostgaard, K., da Cunha‐Bang, C., Hjalgrim, H., & Frederiksen, H. (2021) · Leukemia · doi:10.1038/s41375-021-01156-x · Cited by 55
Gordon-Dseagu, V., Shelton, N. J., & Mindell, J. S. (2012) · International Journal of Cancer · doi:10.1002/ijc.27703 · Cited by 57
“A Danish cohort study found mixed results depending on cancer site.(25) Among those defined as having type-1 diabetes (hospitalised for diabetes within the study period before the age of 50), the SIR for all cancers was 1.”
ResultHarris, D. R., Barts, A. D., Connors, J. M., Dahl, M., Elliott, T., Kong, J. M., Keane, T. J., Thompson, D. M., Stafford, S. G., Ur, E., et al. (2013) · Current Oncology · doi:10.3747/co.20.1499 · Cited by 54
Impact of diabetes mellitus on outcome of HCC
Amarapurkar, D. N., Patel, N. D., & Kamani, P. M. (2008) · Annals of Hepatology · doi:10.1016/s1665-2681(19)31871-x · Cited by 53
“by 2- to 4-fold, even after adjusting for other predisposing factors.(5,9-29) In presence of viral hepatitis and alcohol intake, DM increases risk for HCC by 10-fold.”
BackgroundWashio, M., Mori, M., Khan, M., Sakauchi, F., Watanabe, Y., Ozasa, K., Hayashi, K., Miki, T., Nakao, M., Mikami, K., et al. (2007) · International Journal of Urology · doi:10.1111/j.1442-2042.2007.01744.x · Cited by 52
Zhang, F., Yang, Y., Skrip, L., Hu, D., Wang, Y., Wong, C., Qiu, J., & Lei, H. (2012) · Acta Diabetologica · doi:10.1007/s00592-012-0439-5 · Cited by 52
“The results of 2 case–control studies [18, 19] and 4 cohort studies [52, 53, 55, 56] were adjusted for age only; results of 2 cohort studies [11, 23] did not adjust for any potential confounders; whereas the remaining studies included adjustment for several conventional risk factors, including age, body mass index, ra…”
BackgroundHidaka, A., Sasazuki, S., Goto, A., Sawada, N., Shimazu, T., Yamaji, T., Iwasaki, M., Inoue, M., Noda, M., Tajiri, H., et al. (2014) · International Journal of Cancer · doi:10.1002/ijc.29098 · Cited by 52
Charles, M.-A. A., Fontbonne, A., Thibult, N., Claude, J., Warnet, J., Rosselin, G., Ducimetière, P., & Eschwège, É. (2001) · American Journal of Epidemiology · doi:10.1093/aje/153.3.292 · Cited by 52
Diabetes and risk of subsequent gastric cancer: a population-based cohort study in Taiwan
Chen, Y., Cheng, K. F., Lai, S., Tsai, I., Lin, C.-C., Sung, F., Lin, C., & Chen, P. (2012) · Gastric Cancer · doi:10.1007/s10120-012-0197-7 · Cited by 51
“However, the association between diabetes and risk of gastric cancer is inconclusive [7, 8, 11, 12, 16], and the association may vary among ethnic groups [12].”
BackgroundResultInfluentialCancer Risk in Type 2 Diabetes Mellitus: Metabolic Links and Therapeutic Considerations
Sun, G. E. C., & Kashyap, S. R. (2011) · Journal of Nutrition and Metabolism · doi:10.1155/2011/708183 · Cited by 51
“Some studies showed an increased risk of breast malignancy in individuals with diabetes [8–11, 14–16, 18], whereas others did not [36–39].”
BackgroundTung, H., Wang, J., Tseng, P., Hung, C., Kee, K., Chen, C., Chang, K., Lee, C., Changchien, C., Chen, Y.-D., et al. (2010) · The American Journal of Gastroenterology · doi:10.1038/ajg.2009.711 · Cited by 51
Diabetes mellitus increases the risk of early gastric cancer development
Sekikawa, A. M., Fukui, H., Maruo, T., Tsumura, T., Okabe, Y., & Osaki, Y. (2014) · European Journal of Cancer · doi:10.1016/j.ejca.2014.05.020 · Cited by 51
“Increasing evidence indicates that patients with DM have a higher risk of not only cardiovascular disease, but also cancer in various organs [9–12].”
Background
Metadata
- 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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