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Metformin and Cancer Risk and Mortality: A Systematic Review and Meta-analysis Taking into Account Biases and Confounders
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Abstract
Previous meta-analyses have shown that the antidiabetic agent metformin is associated with reduced cancer incidence and mortality. However, this effect has not been consistently demonstrated in animal models and recent epidemiologic studies. We performed a meta-analysis with a focus on confounders and biases, including body mass index (BMI), study type, and time-related biases. We identified 71 articles published between January 1, 1966, and May 31, 2013, through Pubmed, ISI Web of Science (Science Citation Index Expanded), Embase, and the Cochrane library that were related to metformin and cancer incidence or mortality. Study characteristics and outcomes were abstracted for each study that met inclusion criteria. We included estimates from 47 independent studies and 65,540 cancer cases in patients with diabetes. Overall cancer incidence was reduced by 31% [summary relative risk (SRR), 0.69; 95% confidence interval (CI), 0.52–0.90], although between-study heterogeneity was considerable (I2 = 88%). Cancer mortality was reduced by 34% (SRR, 0.66; 95% CI, 0.54–0.81; I2 = 21%). BMI-adjusted studies and studies without time-related biases also showed significant reduction in cancer incidence (SRR, 0.82; 95% CI, 0.70–0.96 with I2 = 76% and SRR, 0.90; 95% CI, 0.89–0.91 with I2 = 56%, respectively), albeit with lesser magnitude (18% and 10% reduction, respectively). However, studies of cancer mortality and individual organ sites did not consistently show significant reductions across all types of analyses. Although these associations may not be causal, our results show that metformin may reduce cancer incidence and mortality in patients with diabetes However, the reduction seems to be of modest magnitude and not affecting all populations equally. Clinical trials are needed to determine if these observations apply to nondiabetic populations and to specific organ sites. Cancer Prev Res; 7(9); 867–85. ©2014 AACR.
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“long-term use of metformin in type 2 diabetes patients has been linked to a decline in tumor incidence and a reduced rate of cancer-related deaths.192–196”
From Drug repurposing for cancer therapy (2024) · cites this paper as [192]
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“a more thorough analysis that included more data and accounted for heterogeneous comparators showed that overall cancer incidence was reduced by 31% and cancer mortality by 34% (Gandini et al., 2014).”
From Metformin as a tool to target aging (2016) · cites this paper as Gandini et al., 2014
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“Furthermore, retrospective clinical studies have found that metformin use is associated with improved cancer outcomes, reductions in cancer incidence, and decreased cancer mortality (Evans et al., 2005; Franciosi et al., 2013; Gandini et al., 2014; Lee et al., 2012; Noto et al., 2012).”
From Targeting Metabolism for Cancer Therapy (2017) · cites this paper as Gandini et al., 2014
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“Extensive support for a protective effect of metformin against cancer has been provided by numerous, but not all studies (237, 238).”
From A Critical Review of the Evidence That Metformin Is a Putative Anti-Aging Drug That Enhances Healthspan and Extends Lifespan (2021) · cites this paper as [237]
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“In a meta-analysis(255), metformin-treated diabetic patients had a 31% reduction in the incidence of cancer and a 34% reduction in cancer mortality after adjusting for body mass index(255).”
From Metformin, the Aspirin of the 21st Century: Its Role in Gestational Diabetes Mellitus, Prevention of Preeclampsia and Cancer, and the Promotion of Longevity (2017) · cites this paper as [255]
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1 retracted
Metformin monotherapy for type 2 diabetes mellitus
Sáenz, A., Fernandez-Esteban, I., Mataix, A. L., Segura, M. A., Figuls, M. R. I., & Moher, D. (2005) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd002966.pub3 · Cited by 310
RetractedPreferred Reporting Items for Systematic Reviews and Meta-Analyses: the PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & for the PRISMA Group (2009) · BMJ · doi:10.1136/bmj.b2535 · Cited by 83,823
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859
Quantifying heterogeneity in a meta‐analysis
Higgins, J. P. T., & Thompson, S. G. (2002) · Statistics in Medicine · doi:10.1002/sim.1186 · Cited by 36,763
von Elm, E., Altman, D. G., Egger, M., Pocock, S. J., Gøtzsche, P. C., Vandenbroucke, J. P., & Initiative, F. T. S. (2007) · PLoS Medicine · doi:10.1371/journal.pmed.0040296 · Cited by 23,020
Meta-analysis of Observational Studies in Epidemiology<SUBTITLE>A Proposal for Reporting</SUBTITLE>
Stroup, D. F. (2000) · JAMA · doi:10.1001/jama.283.15.2008 · Cited by 20,623
Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement
Moher, D., Liberati, A., Tetzlaff, J., & Altman, D. G. (2009) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2009.06.005 · Cited by 19,575
Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin
(2002) · New England Journal of Medicine · doi:10.1056/nejmoa012512 · Cited by 19,011 · cited 2×
“Furthermore, metformin is the drug of choice in obese patients with diabetes because it reduces weight (3, 100), so its use is associated with obesity.”
Backgroundvon Elm, E., Altman, D. G., Egger, M., Pocock, S. J., Gøtzsche, P. C., & Vandenbroucke, J. P. (2008) · Journal of Clinical Epidemiology · doi:10.1016/j.jclinepi.2007.11.008 · Cited by 17,893
von Elm, E., Altman, D. G., Egger, M., Pocock, S. J., Gøtzsche, P. C., Vandenbroucke, J. P., & Initiative, F. T. S. (2007) · Annals of Internal Medicine · doi:10.7326/0003-4819-147-8-200710160-00010 · Cited by 17,796
Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. Adults
Calle, E. E., Rodriguez, C., Walker-Thurmond, K., & Thun, M. J. (2003) · New England Journal of Medicine · doi:10.1056/nejmoa021423 · Cited by 7,696
Diabetes Prevention Program Research Group (2009) · The Lancet · doi:10.1016/s0140-6736(09)61457-4 · Cited by 3,020
Glycemic durability of rosiglitazone, metformin, or glyburide monotherapy
Kahn, S. E., Haffner, S. M., Heise, M. A., Herman, W. H., Holman, R. R., Jones, N. P., Kravitz, B. G., Lachin, J. M., O'Neill, M. C., Zinman, B., et al. (2006) · New England Journal of Medicine · doi:10.1056/nejmoa066224 · Cited by 2,962
Giovannucci, E., Harlan, D. M., Archer, M. C., Bergenstal, R. M., Gapstur, S. M., Habel, L. A., Pollak, M., Regensteiner, J. G., & Yee, D. (2010) · Diabetes Care · doi:10.2337/dc10-0666 · Cited by 2,366
QUANTITATIVE METHODS IN THE REVIEW OF EPIDEMIOLOGIC LITERATURE1
GREENLAND, S. (1987) · Epidemiologic Reviews · doi:10.1093/oxfordjournals.epirev.a036298 · Cited by 1,644 · cited 1×
“We extracted fully adjusted risk estimates for ever use of metformin, alone or in combinationwithother antidiabetic treatments, compared with antidiabetic treatments other than metformin or no treatment, and we calculated the corresponding variance using the formula proposed by Greenland (20).”
MethodAdvanced methods in meta‐analysis: multivariate approach and meta‐regression
van Houwelingen, H. C., Arends, L. R., & Stijnen, T. (2002) · Statistics in Medicine · doi:10.1002/sim.1040 · Cited by 1,599
A comparison of methods to detect publication bias in meta‐analysis
Macaskill, P., Walter, S. D., & Irwig, L. (2001) · Statistics in Medicine · doi:10.1002/sim.698 · Cited by 1,286
The influence of glucose-lowering therapies on cancer risk in type 2 diabetes
Currie, C. J., Poole, C. D., & Gale, E. A. M. (2009) · Diabetologia · doi:10.1007/s00125-009-1440-6 · Cited by 1,124
Hirsch, H. A., Iliopoulos, D., Tsichlis, P. N., & Struhl, K. (2009) · Cancer Research · doi:10.1158/0008-5472.can-09-2994 · Cited by 1,115
Global guideline for type 2 diabetes
(2014) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2012.10.001 · Cited by 1,064
New Users of Metformin Are at Low Risk of Incident Cancer
Libby, G., Donnelly, L. A., Donnan, P. T., Alessi, D. R., Morris, A. D., & Evans, J. M. M. (2009) · Diabetes Care · doi:10.2337/dc08-2175 · Cited by 996
Metformin and Cancer Risk in Diabetic Patients: A Systematic Review and Meta-analysis
DeCensi, A., Puntoni, M., Goodwin, P., Cazzaniga, M., Gennari, A., Bonanni, B., & Gandini, S. (2010) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-10-0157 · Cited by 918
Self-citationAntidiabetic Therapies Affect Risk of Pancreatic Cancer
Li, D., Yeung, S. J., Hassan, M. M., Konopleva, M., & Abbruzzese, J. L. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.04.013 · Cited by 584
Cancer risk in diabetic patients treated with metformin: a systematic review and meta-analysis
Noto, H., Goto, A., Tsujimoto, T., & Noda, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033411 · Cited by 566
Metformin and the Risk of Cancer
Suissa, S., & Azoulay, L. (2012) · Diabetes Care · doi:10.2337/dc12-0788 · Cited by 543
Metformin Associated With Lower Cancer Mortality in Type 2 Diabetes
Landman, G. W. D., Kleefstra, N., van Hateren, K. J. J., Groenier, K. H., Gans, R. O. B., & Bilo, H. J. G. (2010) · Diabetes Care · doi:10.2337/dc09-1380 · Cited by 502
Morris, P. G., Hudis, C. A., Giri, D. D., Morrow, M., Falcone, D. J., Zhou, X. K., Du, B., Brogi, E., Crawford, C. B., Kopelovich, L., et al. (2011) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-11-0110 · Cited by 473
Long-Term Metformin Use Is Associated With Decreased Risk of Breast Cancer
Bodmer, M., Meier, C., Krähenbühl, S., Jick, S. S., & Meier, C. R. (2010) · Diabetes Care · doi:10.2337/dc09-1791 · Cited by 466
Metformin Therapy and Risk of Cancer in Patients with Type 2 Diabetes: Systematic Review
Franciosi, M., Lucisano, G., Lapice, E., Strippoli, G. F. M., Pellegrini, F., & Nicolucci, A. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071583 · Cited by 428
Chen, H.-P., Shieh, J., Chang, C., Chen, T.-T., Lin, J., Wu, M., Lin, J.-H., & Wu, C. (2012) · Gut · doi:10.1136/gutjnl-2011-301708 · Cited by 399
Mortality After Incident Cancer in People With and Without Type 2 Diabetes
Currie, C. J., Poole, C., Jenkins‐Jones, S., Gale, E. A., Johnson, J. A., & Morgan, C. L. (2012) · Diabetes Care · doi:10.2337/dc11-1313 · Cited by 398
Lee, M.-S., Hsu, C.-C., Wahlqvist, M. L., Tsai, H.-N., Chang, Y.-H., & Huang, Y.-C. (2011) · BMC Cancer · doi:10.1186/1471-2407-11-20 · Cited by 380
Metformin reduces endogenous reactive oxygen species and associated DNA damage
Algire, C., Moiseeva, O., Deschênes-Simard, X., Amrein, L., Petruccelli, L., Birman, E., Viollet, B., Ferbeyre, G., & Pollak, M. N. (2012) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-11-0536 · Cited by 372
Insulin therapy and colorectal cancer risk among type 2 diabetes mellitus patients
Yang, Y., Hennessy, S., & Lewis, J. D. (2004) · Gastroenterology · doi:10.1053/j.gastro.2004.07.011 · Cited by 350
Lai, S., Chen, P., Liao, K.-F., Muo, C., Lin, C., & Sung, F.-C. (2011) · The American Journal of Gastroenterology · doi:10.1038/ajg.2011.384 · Cited by 311
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 308
Cardiovascular Outcomes in Trials of Oral Diabetes Medications: A Systematic Review
Selvin, E., Bolen, S., Yeh, H.-C., Wiley, C., Wilson, L. M., Marinopoulos, S. S., Feldman, L., Vassy, J., Wilson, R., Bass, E. B., et al. (2008) · Archives of Internal Medicine · doi:10.1001/archinte.168.19.2070 · Cited by 300
Anisimov, V. N., Berstein, L. M., Popovich, I. G., Zabezhinski, M. A., Egormin, P. A., Piskunova, T. S., Semenchenko, A. V., Tyndyk, M. L., Yurova, M. N., Kovalenko, I. G., et al. (2011) · Aging · doi:10.18632/aging.100273 · Cited by 285
Cancer Risk Associated with Use of Metformin and Sulfonylurea in Type 2 Diabetes: A Meta-Analysis
Soranna, D., Scotti, L., Zambon, A., Bosetti, C., Grassi, G. M., Catapano, A. L., Vecchia, C. L., Mancia, G., & Corrao, G. (2012) · The Oncologist · doi:10.1634/theoncologist.2011-0462 · Cited by 276
Wright, J. L., & Stanford, J. L. (2009) · Cancer Causes & Control · doi:10.1007/s10552-009-9407-y · Cited by 276
Schernthaner, G., Matthews, D. R., Charbonnel, B. H., Hanefeld, M., & Brunetti, P. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-030861 · Cited by 267
Dual Effect of Metformin on Breast Cancer Proliferation in a Randomized Presurgical Trial
Bonanni, B., Puntoni, M., Cazzaniga, M., Pruneri, G., Serrano, D., Guerrieri‐Gonzaga, A., Gennari, A., Trabacca, M. S., Galimberti, V. E., Veronesi, P., et al. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2011.39.3769 · Cited by 246
Self-citationInsulin-Lowering Effects of Metformin in Women with Early Breast Cancer
Goodwin, P. J., Pritchard, K. I., Ennis, M., Clemons, M. J., Graham, M., & Fantus, I. G. (2008) · Clinical Breast Cancer · doi:10.3816/cbc.2008.n.060 · Cited by 234
Lower Risk of Cancer in Patients on Metformin in Comparison With Those on Sulfonylurea Derivatives
Ruiter, R., Visser, L. E., van Herk‐Sukel, M. P. P., Coebergh, J. W. W., Haak, H. R., Geelhoed-Duijvestijn, P. H. L. M., Straus, S. M. J. M., Herings, R. M. C., & Stricker, B. H. C. (2011) · Diabetes Care · doi:10.2337/dc11-0857 · Cited by 232
Hanefeld, M., Brunetti, P., Schernthaner, G. H., Matthews, D. R., Charbonnel, B. H., & on behalf of the QUARTET Study Group (2004) · Diabetes Care · doi:10.2337/diacare.27.1.141 · Cited by 230
Diabetes, Metformin, and Breast Cancer in Postmenopausal Women
Chlebowski, R. T., McTiernan, A., Wactawski‐Wende, J., Manson, J. E., Aragaki, A. K., Rohan, T. E., Ipp, E., Kaklamani, V., Vitolins, M. Z., Wallace, R. B., et al. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2011.39.7505 · Cited by 218
The effects of metformin on the survival of colorectal cancer patients with diabetes mellitus
Lee, J. H., Kim, T. I., Jeon, S. M., Hong, S. P., Cheon, J. H., & Kim, W. H. (2011) · International Journal of Cancer · doi:10.1002/ijc.26421 · Cited by 206
He, X., Esteva, F. J., Ensor, J., Hortobágyi, G. N., Lee, M., & Yeung, S. J. (2011) · Annals of Oncology · doi:10.1093/annonc/mdr534 · Cited by 206
Currie, C. J., Poole, C. D., Evans, M., Peters, J. R., & Morgan, C. L. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3042 · Cited by 203
Sulphonylureas and cancer: a case-control study
Monami, M., Lamanna, C., Balzi, D., Marchionni, N., & Mannucci, E. (2009) · Acta Diabetologica · doi:10.1007/s00592-008-0083-2 · Cited by 194
Thakkar, B., Aronis, K. N., Vamvini, M. T., Shields, K. S., & Mantzoros, C. S. (2013) · Metabolism · doi:10.1016/j.metabol.2013.01.014 · Cited by 188
Spratt, D. E., Zhang, C., Zumsteg, Z. S., Pei, X., Zhang, Z., & Zeléfsky, M. J. (2012) · European Urology · doi:10.1016/j.eururo.2012.12.004 · Cited by 184
Cohort Study of Pioglitazone and Cancer Incidence in Patients With Diabetes
Ferrara, A. M., Lewis, J. D., Quesenberry, C. P., Peng, T., Strom, B. L., Eeden, S. K. V. D., Ehrlich, S. F., & Habel, L. A. (2011) · Diabetes Care · doi:10.2337/dc10-1067 · Cited by 184
Hosono, K., Endo, H., Takahashi, H., Sugiyama, M., Uchiyama, T., Suzuki, K., Nozaki, Y., Yoneda, K., Fujita, K., Yoneda, M., et al. (2010) · Molecular Carcinogenesis · doi:10.1002/mc.20637 · Cited by 181
Home, P. D., Kahn, S. E., Jones, N. P., Noronha, D., Beck‐Nielsen, H., & Viberti, G. C. (2010) · Diabetologia · doi:10.1007/s00125-010-1804-y · Cited by 176
Bowker, S. L., Majumdar, S. R., Veugelers, P. J., & Johnson, J. A. (2006) · Diabetes Care · doi:10.2337/dc06-0997 · Cited by 175
Impact of Metformin on the Prognosis of Cirrhosis Induced by Viral Hepatitis C in Diabetic Patients
Nkontchou, G., Cosson, E., Aout, M., Mahmoudi, A., Bourcier, V., Charif, I., Ganne‐Carrié, N., Grando–Lemaire, V., Vicaut, É., Trinchet, J., et al. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-2415 · Cited by 167
The Influence of Type 2 Diabetes and Glucose-Lowering Therapies on Cancer Risk in the Taiwanese
Hsieh, M.-C., Lee, T.-C., Cheng, S.-M., Tu, S., Yen, M., & Tseng, C. (2012) · Experimental Diabetes Research · doi:10.1155/2012/413782 · Cited by 166
Metformin for Obesity in Children and Adolescents: A Systematic Review
Park, M. H., Kinra, S., Ward, K. J., White, B., & Viner, R. (2009) · Diabetes Care · doi:10.2337/dc09-0258 · Cited by 165
Tan, B., Yao, W., Ge, J., Peng, X., Du, X., Zhang, R., Yao, B., Xie, K., Li, L., Dong, H., et al. (2011) · Cancer · doi:10.1002/cncr.26151 · Cited by 161
Stevens, R. J., Ali, R., Bankhead, C. R., Bethel, M. A., Cairns, B. J., Camisasca, R. P., Crowe, F. L., Farmer, A. J., Harrison, S., Hirst, J. A., et al. (2012) · Diabetologia · doi:10.1007/s00125-012-2653-7 · Cited by 161
Liao, K., Lai, S., Li, C., & Chen, W. (2011) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2011.06938.x · Cited by 158
Williams‐Herman, D., JOHNSON, J. R., Teng, R., Golm, G. T., Kaufman, K. D., Goldstein, B. J., & Amatruda, J. M. (2010) · Diabetes Obesity and Metabolism · doi:10.1111/j.1463-1326.2010.01204.x · Cited by 154
Metformin Prevents Liver Tumorigenesis by Inhibiting Pathways Driving Hepatic Lipogenesis
Bhalla, K., Hwang, B. J., Dewi, R. E., Twaddel, W., Goloubeva, O. G., Wong, K., Saxena, N. K., Biswal, S. S., & Girnun, G. D. (2012) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-11-0228 · Cited by 152
Chaiteerakij, R., Yang, J. D., Harmsen, W. S., Slettedahl, S. W., Mettler, T. A., Fredericksen, Z. S., Kim, W. R., Gores, G. J., Roberts, R. O., Olson, J. E., et al. (2012) · Hepatology · doi:10.1002/hep.26092 · Cited by 150
Bosco, J. L. F., Antonsen, S., Sørensen, H. T., Pedersen, L. H., & Lash, T. L. (2011) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-10-0817 · Cited by 148
Antidiabetic therapy and increased risk of hepatocellular carcinoma in chronic liver disease
Donadon, V., Balbi, M., Ghersetti, M., Grazioli, S., Perciaccante, A., Valentina, G. D., Gardenal, R., Mas, M. D., Casarin, P., Zanette, G., et al. (2009) · World Journal of Gastroenterology · doi:10.3748/wjg.15.2506 · Cited by 145
Vitale-Cross, L. A., Molinolo, A., Martín, D., Younis, R. H., Maruyama, T., Patel, V., Chen, W., Schneider, A., & Gutkind, J. S. (2012) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-11-0502 · Cited by 145
Diabetes and risk of bladder cancer: a study using the National Health Insurance database in Taiwan
Tseng, C. (2011) · Diabetologia · doi:10.1007/s00125-011-2171-z · Cited by 139
Use of Antidiabetic Agents and the Risk of Pancreatic Cancer: A Case–Control Analysis
Bodmer, M., Becker, C., Meier, C., Jick, S. S., & Meier, C. R. (2012) · The American Journal of Gastroenterology · doi:10.1038/ajg.2011.483 · Cited by 139
Lai, S., Liao, K., Chen, P., Tsai, P., Hsieh, D. P. H., & Chen, C. (2011) · Clinical Lung Cancer · doi:10.1016/j.cllc.2011.10.002 · Cited by 138
Metformin and the Incidence of Prostate Cancer in Patients with Type 2 Diabetes
Azoulay, L., Dell’Aniello, S., Gagnon, B., Pollak, M., & Suissa, S. (2011) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-10-0940 · Cited by 133
Diabetes, metformin use, and colon cancer: a population-based cohort study in Taiwan
Tseng, C. (2012) · European Journal of Endocrinology · doi:10.1530/eje-12-0369 · Cited by 132
van Staa, T. P., Patel, D., Gallagher, A. M., & Bruin, M. L. D. (2011) · Diabetologia · doi:10.1007/s00125-011-2390-3 · Cited by 121
The effect of metformin and thiazolidinedione use on lung cancer in diabetics
Mazzone, P. J., Rai, H., Beukemann, M., Meng, X., Jain, A., & Sasidhar, M. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-410 · Cited by 112
Metformin and Cancer Occurrence in Insulin-Treated Type 2 Diabetic Patients
Monami, M., Colombi, C., Balzi, D., Dicembrini, I., Giannini, S., Melani, C., Vitale, V., Romano, D., Barchielli, A., Marchionni, N., et al. (2010) · Diabetes Care · doi:10.2337/dc10-1287 · Cited by 110
for the DIGAMI 2 Investigators, Mellbin, L., Malmberg, K., Norhammar, A., Wedel, H., & Rydén, L. (2011) · Diabetologia · doi:10.1007/s00125-011-2084-x · Cited by 107
Antidiabetic Medication and Prostate Cancer Risk: A Population-based Case-Control Study
Murtola, T. J., Tammela, T. L. J., Lahtela, J. T., & Auvinen, A. P. (2008) · American Journal of Epidemiology · doi:10.1093/aje/kwn190 · Cited by 104
Diabetes and Cancer—An AACE/ACE Consensus Statement
Handelsman, Y., LeRoith, D., Bloomgarden, Z. T., Dagogo-Jack, S. E., EINHORN, D. F., Garber, A. J., Grunberger, G., Harrell, R. M., Gagel, R. F., Lebovitz, H. E., et al. (2013) · Endocrine Practice · doi:10.4158/ep13248.cs · Cited by 100
Bodmer, M., Becker, C., Meier, C., Jick, S. S., & Meier, C. R. (2012) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-11-0992-t · Cited by 99
Further Exploration of the Relationship Between Insulin Glargine and Incident Cancer
Morden, N. E., Liu, S. K., Smith, J., MacKenzie, T. A., Skinner, J., & Korc, M. (2011) · Diabetes Care · doi:10.2337/dc11-0699 · Cited by 94
Morgan, C. L., Poole, C., Evans, M., Barnett, A. H., Jenkins‐Jones, S., & Currie, C. J. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3034 · Cited by 90
Baur, D. M., Klotsche, J., Hamnvik, O. R., Sievers, C., Pieper, L., Wïttchen, H., Stalla, G. K., Schmid, R. M., Kales, S. N., & Mantzoros, C. S. (2010) · Metabolism · doi:10.1016/j.metabol.2010.09.012 · Cited by 90
Use of sulphonylurea and cancer in type 2 diabetes—The Hong Kong Diabetes Registry
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Metadata
- Authors
- Gandini, S., Puntoni, M., Heckman-Stoddard, B. M., Dunn, B. K., Ford, L., DeCensi, A., & Szabo, E.
- Affiliations
- European Institute of Oncology (IT)
- Ente Ospedaliero Ospedali Galliera (IT)
- 3Breast and Gynecologic Cancer Research Group, Division of Cancer Prevention, National Cancer Institute, Bethesda, Maryland.
- National Institutes of Health (US)
- National Cancer Institute (US)
- Corresponding author
- Szabo, Eva
- Venue
- Cancer Prevention Research
- Published
- 2014-09-01
- Volume
- 7
- Issue
- 9
- Pages
- 867-885
- ISSN
- 1940-6207 (ISSN-L)
- 1940-6215
- PMC
- PMC4154969
- OpenAlex
- W1976655891
- Cited by
- 457
- References
- 115
- Citations by year
- 2026: 18 · 2025: 29 · 2024: 34 · 2023: 37 · 2022: 47 · 2021: 43 · 2020: 40 · 2019: 43 · 2018: 43 · 2017: 41 · 2016: 43 · 2015: 28 · 2014: 10
- FWCI
- 3.83
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Cancer Prevention Research (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (Z99 CA999999)
- 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 › Public Health, Environmental and Occupational Health › Nutritional Studies and Diet
- Keywords
- metformin, cancer incidence, cancer mortality, diabetes mellitus, body mass index, confounding, antidiabetic drugs, chemoprevention
- MeSH terms
- Diabetes Mellitus, Type 2, Humans, Hypoglycemic Agents, Metformin, Neoplasms, Risk
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