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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]”
In the citing paper
“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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Antonelli, A. (2014) · World Journal of Diabetes · doi:10.4239/wjd.v5.i5.586 · Cited by 113
A rodent model of NASH with cirrhosis, oval cell proliferation and hepatocellular carcinoma
de Lima, V. M. R., de Oliveira, C. P. M. S., Alves, V. A. F., Chammas, M. C., Oliveira, E. P., Stefano, J. T., de Mello, E. S., Cerri, G. G., Carrilho, F. J., & Caldwell, S. H. (2008) · Journal of Hepatology · doi:10.1016/j.jhep.2008.07.024 · Cited by 107
“Because obesity and diabetes are both risk factors for HCC [7–12], it is suspected that steatosis may play a prominent role in HCC development in both NAFLD and other forms of chronic liver disease due to the associated presence of oxidative stress and inflammation.”
BackgroundLindkvist, B., Johansen, D., Stocks, T., Concin, H., Bjørge, T., Almquist, M., Häggström, C., Engeland, A., Hallmans, G., Nagel, G., et al. (2014) · BMC Cancer · doi:10.1186/1471-2407-14-103 · Cited by 105
“men with diabetes [12,48], fatal esophageal cancer [13] or fatal esophageal cancer among men [11]).”
Lin, Y., Tamakoshi, A., Kawamura, T., Inaba, Y., Kikuchi, S., Motohashi, Y., Kurosawa, M., Ohno, Y., & JACC Study Group (2002) · International Journal of Cancer · doi:10.1002/ijc.10402 · Cited by 105
The Value of Risk-Factor (“Black-Box”) Epidemiology
Greenland, S., Gago-Domínguez, M., & Castelao, J. E. (2004) · Epidemiology · doi:10.1097/01.ede.0000134867.12896.23 · Cited by 101
Diabetes Mellitus and Risk of Thyroid Cancer: A Meta-Analysis
Yeo, Y., Ma, S.-H., Hwang, Y., Horn‐Ross, P. L., Hsing, A. W., Lee, K.-E., Park, Y. J., Park, D.-J., Yoo, K., & Park, S. S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098135 · Cited by 107
“All summary ORs/RRs (95% CIs) were calculated by the random-effect model We excluded three studies using the risk estimates with SIRs ([14] and [32]) and the different definition of diabetes ([33] was included with IFG and IGT and [34] used quintile of glucose level) Publication bias by Egger and Begg test (p,0.”
BackgroundMethodResultInfluentialBalkau, B., Kahn, H. S., Courbon, D., Eschwège, É., & Ducimetière, P. (2001) · Diabetes Care · doi:10.2337/diacare.24.5.843 · Cited by 101
Diabetes mellitus and breast cancer: a retrospective population-based cohort study
Lipscombe, L. L., Goodwin, P. J., Zinman, B., McLaughlin, J. R., & Hux, J. E. (2006) · Breast Cancer Research and Treatment · doi:10.1007/s10549-006-9172-5 · Cited by 100
“Prior studies have included both pre- and post-menopausal women, and some studies found that breast cancer risk was limited to older or postmenopausal subjects with diabetes [29, 32, 33].”
BackgroundResultType 1 diabetes mellitus and risk of cancer: a meta-analysis of observational studies
Sona, M. F., Myung, S., Park, K., & Galsuren, J. (2018) · Japanese Journal of Clinical Oncology · doi:10.1093/jjco/hyy047 · Cited by 101
Diabetes and the Risk of Lung Cancer
Hall, G. C., Roberts, C. M., Boulis, M., Mo, J., & MacRae, K. D. (2005) · Diabetes Care · doi:10.2337/diacare.28.3.590 · Cited by 99
Morita, T., Tabata, S., Mineshita, M., Mizoue, T., Moore, M. A., & Kono, S. (2005) · PubMed · Cited by 99
Diabetes mellitus and incidence and mortality of kidney cancer: A meta-analysis
Bao, C., Yang, X., Xu, W., Luo, H., Xu, Z., Su, C., & Qi, X. (2013) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2013.01.004 · Cited by 98
“, 2007) and 5 cohort studies reported SIR/SMR (Hemminki et al., 2010; Kessler, 1970; Swerdlow et al., 2005; Verlato, Zoppini, Bonora, & Muggeo, 2003; Wideroff et al., 1997) (See Appendix tables 1, 2 and 3).”
Impact of Fasting Plasma Glucose Levels on Gastric Cancer Incidence in a General Japanese Population
Yamagata, H., Kiyohara, Y., Nakamura, S., Kubo, M., Tanizaki, Y., Matsumoto, T., Tanaka, K., Kato, I., Shirota, T., & Iida, M. (2005) · Diabetes Care · doi:10.2337/diacare.28.4.789 · Cited by 94
“Several recent studies have shown associations between diabetes and cancer in the pancreas (8,9), liver (8,10), and large bowel (11,12).”
BackgroundBody mass index and risk of multiple myeloma: A meta‐analysis
Larsson, S. C., & Wolk, A. (2007) · International Journal of Cancer · doi:10.1002/ijc.22968 · Cited by 96
“disease onset, has been related to an increased risk of multiple myeloma in men(28,29) and women.(30) Moreover, a recent case–control study found a statistically significant 3.”
Backgroundfor the Prostate, L., Leitzmann, M. F., Ahn, J., Albanes, D., Hsing, A. W., Schatzkin, A. G., Chang, S.-C., Huang, W., Weiss, J. M., Danforth, K. N., et al. (2008) · Cancer Causes & Control · doi:10.1007/s10552-008-9198-6 · Cited by 97
“screening [16, 31, 32, 65-70] found no association between diabetes and prostate cancer.”
BackgroundThomson, C. A., Stopeck, A. T., Bea, J. W., Cussler, E., Nardi, E., Frey, G., & Thompson, P. A. (2010) · Nutrition and Cancer · doi:10.1080/01635581.2010.513803 · Cited by 94
Associations of diabetes mellitus with site-specific cancer mortality in the Asia-Pacific region
Lam, E. K. K., Batty, G. D., Huxley, R., Martiniuk, A. L. C., Barzi, F., Lam, T., Lawes, C. M. M., Giles, G. G., Welborn, T. A., Ueshima, H., et al. (2010) · Annals of Oncology · doi:10.1093/annonc/mdq405 · Cited by 93
Raff, E., Kakati, D., Bloomer, J. R., Shoreibah, M., Rasheed, K., & Singal, A. K. (2015) · Journal of Clinical and Translational Hepatology · doi:10.14218/jcth.2015.00001 · Cited by 96
The epidemiology of bladder and kidney cancer
Scélo, G., & Brennan, P. (2007) · Nature Clinical Practice Urology · doi:10.1038/ncpuro0760 · Cited by 93
Chen, H.-F., Chen, P., & Li, C. (2010) · Hepatology · doi:10.1002/hep.23641 · Cited by 93
“In our study, the risk estimates of diabetic women and diabetic men were similar to the findings of Wideroff et al.(8) Further age stratifications revealed that only those subjects aged 45-64 years had significant increased risks compared with the agematched and sex-matched control group in both sexes, but its signifi…”
ResultZhu, Z., Wang, X., Shen, Z., Lu, Y., Zhong, S., & Chen, X. (2013) · BMC Cancer · doi:10.1186/1471-2407-13-310 · Cited by 93
“Additional file 3: Table S3.”
BackgroundKoh, W.-P., Wang, R., Jin, A., Yu, M. C., & Yuan, J.-M. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.25 · Cited by 92
“…2006), Korea (Jee et al, 2005), the US (Coughlin et al, 2004; El-Serag et al, 2004; Atchison et al, 2011) and European countries (Adami et al, 1996; Wideroff et al, 1997; Batty et al, 2004; Ogunleye et al, 2009; Zhou et al, 2010) have recorded a statistically significant increased incidence of HCC…”
BackgroundBurger, H., Nooter, K., Boersma, A. W. M., van Wingerden, K. E., Looijenga, L. H. J., Jochemsen, A. G., & Stoter, G. (1999) · International Journal of Cancer · doi:10.1002/(sici)1097-0215(19990517)81:4 · Cited by 89
Impaired glucose metabolism and diabetes and the risk of breast, endometrial, and ovarian cancer
Lambe, M. P., Wigertz, A., Garmo, H., Walldius, G., Jungner, I., & Hammar, N. (2011) · Cancer Causes & Control · doi:10.1007/s10552-011-9794-8 · Cited by 96
“found no association [12-15].”
ResultExamining the relationship between diet-induced acidosis and cancer
Robey, I. (2012) · Nutrition & Metabolism · doi:10.1186/1743-7075-9-72 · Cited by 93
“Epidemiology studies have shown a positive correlation between circulating insulin levels and increased risk and pathogenesis of colorectal and pancreatic cancers [71-76], cancers of the endometrium [77], kidney cancer [78] and breast cancer [79,80].”
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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