Pharmacologic therapy of diabetes and overall cancer risk and mortality: a meta-analysis of 265 studies
Open accessAbstract
Different anti-diabetic medications (ADMs) may modify cancer risk and mortality in patients with diabetes. We conducted a systematic review and meta-analysis to estimate the magnitude of association and quality of supporting evidence for each ADM. A total of 265 studies (44 cohort studies, 39 case-control studies, and 182 randomized controlled trials (RCT)) were identified, involving approximately 7.6 million and 137,540 patients with diabetes for observational studies and RCTs, respectively. The risk of bias overall was moderate. Meta-analysis demonstrated that the use of metformin or thiazolidinediones was associated with a lower risk of cancer incidence (RR = 0.86, 95% CI 0.83-0.90, I(2) = 88.61%; RR = 0.93, 95% CI 0.91-0.96, I(2) = 0.00% respectively). On the other hand, insulin, sulfonylureas and alpha glucosidase inhibitor use was associated with an increased risk of cancer incidence (RR = 1.21, 95% CI 1.08-1.36, I(2) = 96.31%; RR = 1.20, 95% CI 1.13-1.27, I(2) = 95.02%; RR = 1.10, 95% CI 1.05-1.15, I(2) = 0.00% respectively). Use of other types of ADMs was not significantly associated with cancer risk. This study indicates that some ADMs may modify the risk of cancer in individuals with diabetes. Knowledge of this risk may affect the choice of ADM in individuals concerned about cancer or at increased risk for cancer.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Metformin is now gaining attention as a potential anti-cancer agent.
“Originally introduced for the treatment of diabetes, metformin is now gaining attention as a potential anti-cancer agent (7–10) (Figure 1).”
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 [10]
This finding has subsequently been confirmed in several other studies.
“this finding has subsequently been confirmed in several other studies(7–10).”
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 [10]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Measuring inconsistency in meta-analyses
Higgins, J. P. T., Thompson, S. G., Deeks, J. J., & Altman, D. G. (2003) · BMJ · doi:10.1136/bmj.327.7414.557 · Cited by 63,139 · see citing works
Bias in meta-analysis detected by a simple, graphical test
Egger, M., Smith, G. D., Schneider, M., & Minder, C. (1997) · BMJ · doi:10.1136/bmj.315.7109.629 · Cited by 56,722 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA Statement.
(2009) · PubMed Central · Cited by 44,859 · see citing works
Meta-analysis in clinical trials
DerSimonian, R., & Laird, N. (1986) · Controlled Clinical Trials · doi:10.1016/0197-2456(86)90046-2 · Cited by 39,552 · see citing works
Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement
Moher, D., Liberati, A., Tetzlaff, J., Altman, D. G., & the PRISMA Group* (2009) · Annals of Internal Medicine · doi:10.7326/0003-4819-151-4-200908180-00135 · Cited by 37,554 · see citing works
The Cochrane Collaboration's tool for assessing risk of bias in randomised trials
Higgins, J. P. T., Altman, D. G., Gotzsche, P. C., Juni, P., Moher, D., Oxman, A. D., Savovic, J., Schulz, K. F., Weeks, L., Sterne, J. A. C., et al. (2011) · BMJ · doi:10.1136/bmj.d5928 · Cited by 33,817 · see citing works
Dermyshi, E., Wang, Y., Yan, C., Hong, W., Qiu, G., Gong, X., & Zhang, T. (2017) · Neonatology · doi:10.1159/000454668 · Cited by 24,577 · see citing works
(2014) · Medical Entomology and Zoology · Cited by 17,633 · see citing works
IDF Diabetes Atlas: Global estimates for the prevalence of diabetes for 2015 and 2040
Ogurtsova, K., Fernandes, J. D. D. R., Huang, Y., Linnenkamp, U., Guariguata, L., Cho, N. H., Cavan, D. A., Shaw, J. E., & Makaroff, L. (2017) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2017.03.024 · Cited by 6,977 · see citing works
Role of AMP-Activated Protein Kinase in Mechanism of Metformin Action
Zhou, G., Myers, R., Li, Y., Chen, Y., Shen, X., Fenyk-Melody, J., Wu, M., Ventre, J., Doebber, T., Fujii, N., et al. (2001) · Journal of Clinical Investigation · doi:10.1172/jci13505 · Cited by 5,652 · see citing works
IDF Diabetes Atlas: Global estimates of the prevalence of diabetes for 2011 and 2030
Whiting, D. R., Guariguata, L., Weil, C., & Shaw, J. E. (2011) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2011.10.029 · Cited by 3,994 · see citing works
Danaei, G., Finucane, M. M., Lu, Y., Singh, G. M., Cowan, M. J., Paciorek, C. J., Lin, J. K., Farzadfar, F., Khang, Y.-H., Stevens, G. A., et al. (2011) · The Lancet · doi:10.1016/s0140-6736(11)60679-x · Cited by 3,568 · see citing works
Diabetes and Cancer: A Consensus Report
Giovannucci, E. L., Harlan, D. M., Archer, M. C., Bergenstal, R. M., Gapstur, S. M., Habel, L. A., Pollak, M., Regensteiner, J. G., & Yee, D. (2010) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.20078 · Cited by 1,065 · see citing works
Bowker, S. L., Majumdar, S. R., Veugelers, P., & Johnson, J. A. (2006) · Diabetes Care · doi:10.2337/diacare.29.02.06.dc05-1558 · Cited by 933 · see citing works
Sahra, I. B., Laurent, K., Loubat, A., Giorgetti-Peraldi, S., Colosetti, P., Auberger, P., Tanti, J. F., Le Marchand-Brustel, Y., & Bost, F. (2008) · Oncogene · doi:10.1038/sj.onc.1211024 · Cited by 861 · see citing works
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 · see citing works
Metformin and the Risk of Cancer
Suissa, S., & Azoulay, L. (2012) · Diabetes Care · doi:10.2337/dc12-0788 · Cited by 532 · see citing works
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 · see citing works
The worldwide diabetes epidemic
Lam, D. W.-H., & LeRoith, D. (2012) · Current Opinion in Endocrinology Diabetes and Obesity · doi:10.1097/med.0b013e328350583a · Cited by 319 · see citing works
Singh, S., Singh, P. P., Singh, A. G., Murad, M. H., & Sánchez, W. (2013) · The American Journal of Gastroenterology · doi:10.1038/ajg.2013.5 · Cited by 318 · see citing works
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 273 · see citing works
Safety of dipeptidyl peptidase-4 inhibitors: a meta-analysis of randomized clinical trials
Monami, M., Dicembrini, I., Martelli, D., & Mannucci, E. (2011) · Current Medical Research and Opinion · doi:10.1185/03007995.2011.602964 · Cited by 217 · see citing works
Deng, L., Gui, Z., Zhao, L., Wang, J., & Shen, L. (2012) · Digestive Diseases and Sciences · doi:10.1007/s10620-012-2055-1 · Cited by 202 · see citing works
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 186 · see citing works
Stevens, R., Ali, R., Bankhead, C. R., Bethel, M. A., Cairns, B. J., Camisasca, R., Crowe, F. L., Farmer, A. A., Harrison, S., Hirst, J. A., et al. (2012) · Diabetologia · doi:10.1007/s00125-012-2653-7 · Cited by 183 · see citing works
Colmers-Gray, I. N., Bowker, S. L., Majumdar, S. R., & Johnson, J. A. (2012) · Canadian Medical Association Journal · doi:10.1503/cmaj.112102 · Cited by 156 · see citing works
Epidemiological aspects of neoplasms in diabetes
Nicolucci, A. (2010) · Acta Diabetologica · doi:10.1007/s00592-010-0187-3 · Cited by 152 · see citing works
Metformin and reduced risk of hepatocellular carcinoma in diabetic patients: a meta-analysis
Zhang, H., Gao, C., Fang, L., Zhao, H.-C., & Yao, S. (2012) · Scandinavian Journal of Gastroenterology · doi:10.3109/00365521.2012.719926 · Cited by 147 · see citing works
Pioglitazone and risk of bladder cancer: a meta‐analysis of controlled studies
Ferwana, M. S., Firwana, B., Hasan, R., Al-Mallah, M. H., Kim, S., Montori, V. M., & Murad, M. H. (2013) · Diabetic Medicine · doi:10.1111/dme.12144 · Cited by 146 · see citing works
Combined randomised controlled trial experience of malignancies in studies using insulin glargine
Home, P., & Lagarenne, P. (2009) · Diabetologia · doi:10.1007/s00125-009-1530-5 · Cited by 141 · see citing works
Singh, S., Singh, P. P., Singh, A. G., Murad, M. H., McWilliams, R. R., & Chari, S. T. (2013) · The American Journal of Gastroenterology · doi:10.1038/ajg.2013.7 · Cited by 124 · see citing works
Karlstad, Ø., Starup‐Linde, J., Vestergaard, P., Hjellvik, V., Bazelier, M. T., Schmidt, M. K., Andersen, M., Auvinen, A. P., Haukka, J. K., Furu, K., et al. (2013) · Current Drug Safety · doi:10.2174/15680266113136660067 · Cited by 119 · see citing works
Thiazolidinediones and cancer: results of a meta-analysis of randomized clinical trials
Monami, M., Dicembrini, I., & Mannucci, E. (2013) · Acta Diabetologica · doi:10.1007/s00592-013-0504-8 · Cited by 115 · see citing works
Singh, S., Singh, H., Singh, P. P., Murad, M. H., & Limburg, P. J. (2013) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-13-0429 · Cited by 98 · see citing works
Rosiglitazone and Risk of Cancer
Monami, M., Lamanna, C., Marchionni, N., & Mannucci, E. (2008) · Diabetes Care · doi:10.2337/dc07-2308 · Cited by 97 · see citing works
Colmers-Gray, I. N., Bowker, S. L., Tjosvold, L., & Johnson, J. A. (2012) · Diabetes & Metabolism · doi:10.1016/j.diabet.2012.08.011 · Cited by 86 · see citing works
Thiazolidinedione use and cancer incidence in type 2 diabetes: A systematic review and meta-analysis
Colmers, I. N., Bowker, S. L., & Johnson, J. A. (2012) · Diabetes & Metabolism · doi:10.1016/j.diabet.2012.06.003 · Cited by 81 · see citing works
Luan, N., Wu, L., Gong, T., Wang, Y.-L., Lin, B., & Wu, Q. (2014) · Cancer Causes & Control · doi:10.1007/s10552-014-0483-2 · Cited by 79 · see citing works
Mechanisms by which thiazolidinediones induce anti-cancer effects in cancers in digestive organs
Okumura, T. (2010) · Journal of Gastroenterology · doi:10.1007/s00535-010-0310-9 · Cited by 67 · see citing works
Wu, L., Jiang, Z., Li, C., & Shu, M. (2014) · International Journal of Cardiology · doi:10.1016/j.ijcard.2014.04.176 · Cited by 63 · see citing works
Gurney, K., MacConell, L., Brown, C. J., & Han, J. (2012) · Diabetes Metabolic Syndrome and Obesity · doi:10.2147/dmso.s28387 · Cited by 61 · see citing works
Insulin analogues and cancer risk: cause for concern orcause célèbre?
Pollak, M., & Russell-Jones, D. L. (2010) · International Journal of Clinical Practice · doi:10.1111/j.1742-1241.2010.02354.x · Cited by 45 · see citing works
Home, P. (2013) · Diabetes Care · doi:10.2337/dcs13-2002 · Cited by 44 · see citing works
Functional role of peroxisome‐proliferator‐activated receptor γ in hepatocellular carcinoma
Wu, C., Farrell, G. C., & Yu, J. Q. (2012) · Journal of Gastroenterology and Hepatology · doi:10.1111/j.1440-1746.2012.07213.x · Cited by 43 · see citing works
Parity and Pancreatic Cancer Risk: A Dose-Response Meta-Analysis of Epidemiologic Studies
Guan, H.-B., Wu, L., Wu, Q., Zhu, J., & Gong, T. (2014) · PLoS ONE · doi:10.1371/journal.pone.0092738 · Cited by 40 · see citing works
Review of current and emerging therapies in type 2 diabetes mellitus.
Mazzola, N. (2012) · PubMed · Cited by 40 · see citing works
Diabetes therapy and cancer risk
Vigneri, R. (2009) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2009.219 · Cited by 37 · see citing works
Insulin Glargine and Cancer Risk in Patients with Diabetes: A Meta-Analysis
Tang, X., Yang, L., He, Z., & Liu, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0051814 · Cited by 37 · see citing works
The Public Health Burden of Diabetes and the Reality of Limits
Vinicor, F. (1998) · Diabetes Care · doi:10.2337/diacare.21.3.c15 · Cited by 35 · see citing works
Wang, L., Cai, S., Teng, Z., Zhao, X., Chen, X., & Bai, X. (2013) · Diagnostic Pathology · doi:10.1186/1746-1596-8-180 · Cited by 31 · see citing works
Wu, L., Schaid, D. J., Sicotte, H., Wieben, E. D., Li, H., & Petersen, G. M. (2014) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2014-102697 · Cited by 24 · see citing works
Chen, Y., Chen, Q., Wang, Z., & Zhou, J. (2013) · PLoS ONE · doi:10.1371/journal.pone.0081594 · Cited by 20 · see citing works
Kuang, D., Chen, W., Song, Y.-Z., Yu, Y., Zhang, D., Wu, L., & Tang, J. (2014) · Asian Pacific Journal of Cancer Prevention · doi:10.7314/apjcp.2014.15.16.6855 · Cited by 19 · see citing works
Efficacy and safety of degludec insulin: a meta-analysis of randomised trials
Monami, M., & Mannucci, E. (2013) · Current Medical Research and Opinion · doi:10.1185/03007995.2013.772507 · Cited by 15 · see citing works
Wu, L., Rabe, K. G., & Petersen, G. M. (2015) · PLoS ONE · doi:10.1371/journal.pone.0117230 · Cited by 15 · see citing works
Insulin therapy and risk of colorectal cancer: an updated meta-analysis of epidemiological studies
Sun, A., Liu, R., & Sun, G. (2013) · Current Medical Research and Opinion · doi:10.1185/03007995.2013.858622 · Cited by 15 · see citing works
Wu, L., Goldstein, A. M., Yu, K. F., Yang, X. R., Rabe, K. G., Arslan, A. A., Canzian, F., Wolpin, B. M., Stolzenberg‐Solomon, R. Z., Amundadottir, L. T., et al. (2014) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-13-0627 · Cited by 15 · see citing works
Association between diabetes or antidiabetic therapy and lung cancer: A meta‐analysis
Wang, Z., Bao, C., Su, C., Xu, W., Luo, H., Chen, L., & Qi, X. (2013) · Journal of Diabetes Investigation · doi:10.1111/jdi.12112 · Cited by 12 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Blonde, L., Umpierrez, G. E., Reddy, S. S., McGill, J. B., Berga, S. L., Bush, M., Chandrasekaran, S., DeFronzo, R. A., Einhorn, D., Galindo, R. J., et al. (2022) · Endocrine Practice · doi:10.1016/j.eprac.2022.08.002 · Cited by 507 · see citing works
Sleire, L., Førde, H. E., Netland, I. A., Leiss, L., Skeie, B. S., & Enger, P. Ø. (2017) · Pharmacological Research · doi:10.1016/j.phrs.2017.07.013 · Cited by 329 · see citing works
Repurposing metformin for cancer treatment: current clinical studies
Chae, Y. K., Arya, A., Malecek, M., Shin, D. S., Carneiro, B. A., Chandra, S., Kaplan, J. B., Kalyan, A., Altman, J. K., Platanias, L. C., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.8194 · Cited by 325 · see citing works
Repurposing metformin for the prevention of cancer and cancer recurrence
Heckman‐Stoddard, B. M., DeCensi, A., Sahasrabuddhe, V. V., & Ford, L. G. (2017) · Diabetologia · doi:10.1007/s00125-017-4372-6 · Cited by 299 · see citing works
Metformin: Is it a drug for all reasons and diseases?
Triggle, C. R., Mohammed, I., Bshesh, K., Marei, I., Ye, K., Ding, H., MacDonald, R. S., Hollenberg, M. D., & Hill, M. A. (2022) · Metabolism · doi:10.1016/j.metabol.2022.155223 · Cited by 282 · see citing works
Romero, R., Erez, O., Hüttemann, M., Maymon, E., Panaitescu, B., Conde-Agudelo, A., Pacora, P., Yoon, B. H., & Grossman, L. I. (2017) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2017.06.003 · Cited by 253 · see citing works
Cancer, obesity, diabetes, and antidiabetic drugs: is the fog clearing?
Klil-Drori, A. J., Azoulay, L., & Pollak, M. (2016) · Nature Reviews Clinical Oncology · doi:10.1038/nrclinonc.2016.120 · Cited by 207 · see citing works
Diabetes and Cancer: Cancer Should Be Screened in Routine Diabetes Assessment
Suh, S., & Kim, K. (2019) · Diabetes & Metabolism Journal · doi:10.4093/dmj.2019.0177 · Cited by 185 · see citing works
From obesity to diabetes and cancer: epidemiological links and role of therapies
García‐Jiménez, C., Gutiérrez‐Salmerón, M. T., Chocarro‐Calvo, A., García-Martínez, J. M., Castaño, Á., & la Vieja, A. D. (2016) · British Journal of Cancer · doi:10.1038/bjc.2016.37 · Cited by 173 · see citing works
González, N., Prieto, I., del Puerto‐Nevado, L., Portal‐Núñez, S., Ardura, J. A., Cortón, M., Fernández‐Fernández, B., Aguilera, Ó., Gómez‐Guerrero, C., Mas, S., et al. (2017) · Oncotarget · doi:10.18632/oncotarget.14472 · Cited by 169 · see citing works
The Relationship Between Diabetes Mellitus and Cancers and Its Underlying Mechanisms
Zhu, B., & Qu, S. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.800995 · Cited by 173 · see citing works
Metformin Prevents Cisplatin-Induced Cognitive Impairment and Brain Damage in Mice
Zhou, W., Kavelaars, A., & Heijnen, C. J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151890 · Cited by 167 · see citing works
Drug-repositioning opportunities for cancer therapy: novel molecular targets for known compounds
Würth, R., Thellung, S., Bajetto, A., Mazzanti, M., Florio, T., & Barbieri, F. (2015) · Drug Discovery Today · doi:10.1016/j.drudis.2015.09.017 · Cited by 145 · see citing works
Diabetes and cancer: Pathophysiological fundamentals of a ‘dangerous affair’
Cignarelli, A., Genchi, V. A., Caruso, I., Natalicchio, A., Perrini, S., Laviola, L., & Giorgino, F. (2018) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2018.04.002 · Cited by 146 · see citing works
Insights into the Link Between Obesity and Cancer
Ackerman, S. E., Blackburn, O. A., Marchildon, F., & Cohen, P. (2017) · Current Obesity Reports · doi:10.1007/s13679-017-0263-x · Cited by 115 · see citing works
Parity and endometrial cancer risk: a meta-analysis of epidemiological studies
Wu, Q., Li, Y., Tu, C., Zhu, J., Qian, K., Feng, T., Li, C., Wu, L., & Ma, X. (2015) · Scientific Reports · doi:10.1038/srep14243 · Cited by 108 · see citing works
Repurposing old drugs to fight multidrug resistant cancers
Dinić, J., Efferth, T., García‐Sosa, A. T., Grahovac, J., Padrón, J. M., Pajeva, I. K., Rizzolio, F., Saponara, S., Spengler, G., & Tsakovska, I. (2020) · Drug Resistance Updates · doi:10.1016/j.drup.2020.100713 · Cited by 100 · see citing works
Diabesity and antidiabetic drugs
Pappachan, J. M., Fernandez, C. J., & Chacko, E. C. (2018) · Molecular Aspects of Medicine · doi:10.1016/j.mam.2018.10.004 · Cited by 99 · see citing works
Diabetes Mellitus and the Colon
Piper, M. S., & Saad, R. J. (2017) · Current Treatment Options in Gastroenterology · doi:10.1007/s11938-017-0151-1 · Cited by 98 · see citing works
How Comorbidities Shape Cancer Biology and Survival
Panigrahi, G., & Ambs, S. (2021) · Trends in cancer · doi:10.1016/j.trecan.2020.12.010 · Cited by 88 · see citing works
Is metformin poised for a second career as an antimicrobial?
Malik, F. R., Mehdi, S. F., Ali, H., Patel, P., Basharat, A., Kumar, A., Ashok, F., Stein, J., Brima, W., Malhotra, P., et al. (2017) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2975 · Cited by 87 · see citing works
Turbitt, W. J., Demark‐Wahnefried, W., Peterson, C. M., & Norian, L. A. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01402 · Cited by 84 · see citing works
Diabetes and cancer, common threads and missing links
Hua, F., Yu, J., & Hu, Z. (2016) · Cancer Letters · doi:10.1016/j.canlet.2016.02.006 · Cited by 79 · see citing works
Metformin for cancer and aging prevention: is it a time to make the long story short?
Anisimov, V. N. (2015) · Oncotarget · doi:10.18632/oncotarget.6347 · Cited by 77 · see citing works
Medical Management of Diabesity: Do We Have Realistic Targets?
Pappachan, J. M., & Viswanath, A. (2017) · Current Diabetes Reports · doi:10.1007/s11892-017-0828-9 · Cited by 69 · see citing works
Metformin inhibits ovarian cancer via decreasing H3K27 trimethylation
Tang, G., Guo, J., Zhu, Y., Huang, Z., Liu, T., Cai, J., Yu, L., & Wang, Z. (2018) · International Journal of Oncology · doi:10.3892/ijo.2018.4343 · Cited by 65 · see citing works
Ma, W., Chen, J., Meng, Y., Yang, J., Cui, Q., & Zhou, Y. (2018) · Frontiers in Microbiology · doi:10.3389/fmicb.2018.01336 · Cited by 63 · see citing works
Statin use and breast cancer survival and risk: a systematic review and meta-analysis
Wu, Q., Tu, C., Li, Y., Zhu, J., Qian, K., Li, W., & Wu, L. (2015) · Oncotarget · doi:10.18632/oncotarget.5557 · Cited by 65 · see citing works
Repurposing old drugs in oncology: Opportunities with clinical and regulatory challenges ahead
Shah, R. R., & Stonier, P. (2018) · Journal of Clinical Pharmacy and Therapeutics · doi:10.1111/jcpt.12759 · Cited by 65 · see citing works
Metformin-induced anticancer activities: recent insights
Safe, S. H., Nair, V., & Karki, K. (2017) · Biological Chemistry · doi:10.1515/hsz-2017-0271 · Cited by 61 · see citing works
The 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 · see citing works
Repurposing old drugs to chemoprevention: the case of metformin
Heckman‐Stoddard, B. M., Gandini, S., Puntoni, M., Dunn, B. K., DeCensi, A., & Szabo, E. M. (2015) · Seminars in Oncology · doi:10.1053/j.seminoncol.2015.09.009 · Cited by 58 · see citing works
Caloric restriction - A promising anti-cancer approach: From molecular mechanisms to clinical trials
Kopeina, G. S., Senichkin, V. V., & Zhivotovsky, B. (2016) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2016.11.002 · Cited by 57 · see citing works
Bronczek, G. A., Vettorazzi, J. F., Soares, G. M., Kurauti, M. A., dos Santos, C., Bonfim, M. F., Carneiro, E. M., Balbo, S. L., Boschero, A. C., & Júnior, J. M. C. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00561 · Cited by 57 · see citing works
Zhang, Y., Kong, W., & Jiang, J. (2017) · Science China Life Sciences · doi:10.1007/s11427-017-9047-4 · Cited by 58 · see citing works
Gong, J., Kelekar, G., Shen, J., Shen, J., Kaur, S., & Mita, M. M. (2016) · Targeted Oncology · doi:10.1007/s11523-016-0423-z · Cited by 55 · see citing works
Lee, D. Y., Yu, J. H., Park, S. H., Han, K., Kim, N. H., Yoo, H. J., Choi, K. M., Baik, S. H., Kim, N. H., & Seo, J. A. (2018) · Scientific Reports · doi:10.1038/s41598-018-27965-2 · Cited by 48 · see citing works
Diabetes, Antidiabetic Medications and Cancer Risk in Type 2 Diabetes: Focus on SGLT-2 Inhibitors
Dąbrowski, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22041680 · Cited by 47 · see citing works
Associations between Diabetes Mellitus and Selected Cancers
Pliszka, M., & Szablewski, L. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25137476 · Cited by 52 · see citing works
Association of diabetes mellitus with thyroid cancer risk
Li, H., & Qian, J. (2017) · Medicine · doi:10.1097/md.0000000000008230 · Cited by 47 · see citing works
Dankner, R. S., Agay, N., Olmer, L., Murad, H., Keinan‐Boker, L., Balicer, R. D., & Freedman, L. S. (2019) · American Journal of Epidemiology · doi:10.1093/aje/kwz157 · Cited by 46 · see citing works
Survival of Colorectal Cancer Patients With Diabetes Mellitus: A Meta-Analysis
Petrelli, F., Ghidini, M., Rausa, E., Ghidini, A., Cabiddu, M., Borgonovo, K., Ghilardi, M., Parati, M. C., Pietrantonio, F., Sganzerla, P., et al. (2020) · Canadian Journal of Diabetes · doi:10.1016/j.jcjd.2020.06.009 · Cited by 46 · see citing works
Drug repositioning in drug discovery of T2DM and repositioning potential of antidiabetic agents
Zhu, S., Bai, Q., Li, L., & Xu, T. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.05.057 · Cited by 42 · see citing works
Chen, Y., Mushashi, F., Son, S., Bhatti, P., Dummer, T., & Murphy, R. A. (2023) · Scientific Reports · doi:10.1038/s41598-023-38431-z · Cited by 41 · see citing works
Parity and thyroid cancer risk: a meta‐analysis of epidemiological studies
Zhu, J., Zhu, X. D., Tu, C., Li, Y., Qian, K., Jiang, C. S., Feng, T., Li, C., Liu, G. J., & Wu, L. (2015) · Cancer Medicine · doi:10.1002/cam4.604 · Cited by 41 · see citing works
Repurposing metformin for the treatment of gastrointestinal cancer
Júnior, A. D. D. C., Bragagnoli, A. S. C., Costa, F. O., & Carvalheira, J. B. C. (2021) · World Journal of Gastroenterology · doi:10.3748/wjg.v27.i17.1883 · Cited by 42 · see citing works
Comorbidity of patients with noncommunicable diseases in general practice. Eurasian guidelines
Drapkina, O. M., Васильевна, К. А., Калинина, А. М., Avdeev, S. N., Викторович, А. М., Алексеева, Л. И., Almazova, I. I., Andreenko, Е. Y., Antipushina, D. N., Balanova, Y. А., et al. (2024) · CARDIOVASCULAR THERAPY AND PREVENTION · doi:10.15829/1728-8800-2024-3996 · Cited by 49 · see citing works
Metformin beyond type 2 diabetes: Emerging and potential new indications
Petrie, J. R. (2024) · Diabetes Obesity and Metabolism · doi:10.1111/dom.15756 · Cited by 47 · see citing works
Obesity, diabetes, and cancer: epidemiology, pathophysiology, and potential interventions
Mesquita, L. D. A., Wayerbacher, L. F., Schwartsmann, G., & Gerchman, F. (2023) · Archives of Endocrinology and Metabolism · doi:10.20945/2359-3997000000647 · Cited by 41 · see citing works
Yarmolinsky, J., Bouras, E., Constantinescu, A., Burrows, K., Bull, C. J., Vincent, E. E., Martin, R. M., Dimopoulou, O., Lewis, S. J., Moreno, V. R., et al. (2023) · Diabetologia · doi:10.1007/s00125-023-05925-4 · Cited by 38 · see citing works
Brown, J. C., Carson, T. L., Thompson, H. J., & Agurs‐Collins, T. (2021) · Obesity · doi:10.1002/oby.23161 · Cited by 37 · see citing works
Diabetes mellitus and endometrial carcinoma: Risk factors and etiological links
Wang, Y., Zeng, X., Tan, J., Xu, Y., & Yi, C. (2022) · Medicine · doi:10.1097/md.0000000000030299 · Cited by 37 · see citing works
Zhao, Y., Wang, Y., Lou, H.-Y., & Shan, L. (2017) · Oncotarget · doi:10.18632/oncotarget.17515 · Cited by 34 · see citing works
Lam, G. T., Jeong, Y. S., Kim, S., & Ahn, S. (2017) · Cancer Science · doi:10.1111/cas.13482 · Cited by 34 · see citing works
Arnason, T., & Harkness, T. A. A. (2015) · Cancers · doi:10.3390/cancers7040877 · Cited by 33 · see citing works
Júnior, A. D. D. C., Pericole, F. V., & Carvalheira, J. B. C. (2018) · Clinics · doi:10.6061/clinics/2018/e412s · Cited by 31 · see citing works
Li, P., Zhang, C., Gao, P., Chen, X., Ma, B., Yu, D., Song, Y., & Wang, Z. (2017) · Oncology Letters · doi:10.3892/ol.2017.7370 · Cited by 32 · see citing works
Wu, L., & Zhu, J. (2015) · Human Reproduction · doi:10.1093/humrep/dev160 · Cited by 31 · see citing works
Chovsepian, A., Prokopchuk, O., Petrova, G., Gjini, T., Kuzi, H., Heisz, S., Janssen, K., Martignoni, M. E., Friess, H., Hauner, H., et al. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101729 · Cited by 30 · see citing works
Use of Antihyperglycemic Drugs and Risk of Cancer in Patients with Diabetes
Søndergaard, C. S., Esquivel, P. N., Dalamaga, Μ., & Magkos, F. (2022) · Current Oncology Reports · doi:10.1007/s11912-022-01344-7 · Cited by 30 · see citing works
The Role of AMPK/mTOR Modulators in the Therapy of Acute Myeloid Leukemia
Višnjić, D., Dembitz, V., & Lalić, H. (2018) · Current Medicinal Chemistry · doi:10.2174/0929867325666180117105522 · Cited by 28 · see citing works
Yi, X., Zhu, J., Zhu, X. M., Liu, G. J., & Wu, L. (2015) · Clinical Nutrition · doi:10.1016/j.clnu.2015.12.005 · Cited by 28 · see citing works
Association of Genomic Instability with HbA1c levels and Medication in Diabetic Patients
Grindel, A., Brath, H., Nersesyan, A. K., Knasmüller, S., & Wagner, K. (2017) · Scientific Reports · doi:10.1038/srep41985 · Cited by 28 · see citing works
Urpilainen, E., Marttila, M. M., Hautakoski, A., Arffman, M., Sund, R., Ilanne‐Parikka, P., Arima, R., Kangaskokko, J., Puistola, U., Läärä, E., et al. (2018) · BJOG An International Journal of Obstetrics & Gynaecology · doi:10.1111/1471-0528.15151 · Cited by 27 · see citing works
Metformin and health outcomes: An umbrella review of systematic reviews with meta‐analyses
Li, X., Celotto, S., Pizzol, D., Gašević, D., Ji, M., Barnini, T., Solmi, M., Stubbs, B., Smith, L., Sánchez, G. F. L., et al. (2021) · European Journal of Clinical Investigation · doi:10.1111/eci.13536 · Cited by 27 · see citing works
Zunica, E. R. M., Yang, S., Coulter, A. A., White, C. L., Kirwan, J. P., & Gilmore, L. A. (2021) · Nutrients · doi:10.3390/nu13092923 · Cited by 26 · see citing works
Shao, H., Zhao, L., Chen, F., Zeng, S., Liu, S., & Li, J. (2015) · Medical Science Monitor · doi:10.12659/msm.895362 · Cited by 25 · see citing works
Dankner, R. S., & Roth, J. (2019) · Diabetic Medicine · doi:10.1111/dme.14179 · Cited by 24 · see citing works
Bland, A. R., Shrestha, N., Bower, R. L., Rosengren, R. J., & Ashton, J. C. (2020) · Biochemical Pharmacology · doi:10.1016/j.bcp.2020.114345 · Cited by 23 · see citing works
Arima, R., Marttila, M., Hautakoski, A., Arffman, M., Sund, R., Ilanne‐Parikka, P., Kangaskokko, J., Läärä, E., Puistola, U., & Hinkula, M. (2017) · Gynecologic Oncology · doi:10.1016/j.ygyno.2017.06.011 · Cited by 23 · see citing works
No association between metformin use and survival in patients with pancreatic cancer
Frouws, M. A., Mulder, B. G. S., Bastiaannet, E., Zanders, M. M. J., van Herk‐Sukel, M. P. P., de Leede, E. M., Bonsing, B. A., Mieog, J. S. D., van de Velde, C. J. �., & Liefers, G. (2017) · Medicine · doi:10.1097/md.0000000000006229 · Cited by 22 · see citing works
Moradinazar, M., Najafi, F., Rajati, F., Sarokhani, D., & Bavandpour, M. (2023) · International Journal of Preventive Medicine · doi:10.4103/ijpvm.ijpvm_62_21 · Cited by 23 · see citing works
Zaccardi, F., Davies, M. J., & Khunti, K. (2020) · Diabetes Obesity and Metabolism · doi:10.1111/dom.13929 · Cited by 22 · see citing works
Alhourani, A. H., Tidwell, T., Bokil, A. A., Røsland, G. V., Tronstad, K. J., Søreide, K., & Hagland, H. R. (2021) · Scientific Reports · doi:10.1038/s41598-021-89861-6 · Cited by 21 · see citing works
Cancer Prevention: Lessons Learned and Future Directions
Dunn, B. K., & Kramer, B. S. (2016) · Trends in cancer · doi:10.1016/j.trecan.2016.11.003 · Cited by 20 · see citing works
Cardiovascular Risk in Cancer Survivors
Agmon, I. N., & Iakobishvili, Z. (2018) · Current Treatment Options in Cardiovascular Medicine · doi:10.1007/s11936-018-0645-8 · Cited by 20 · see citing works
Repurposing Drugs for Acute Myeloid Leukemia: A Worthy Cause or a Futile Pursuit?
Wojcicki, A. V., Kadapakkam, M., Frymoyer, A. R., Lacayo, N. J., Chae, H.-D., & Sakamoto, K. M. (2020) · Cancers · doi:10.3390/cancers12020441 · Cited by 20 · see citing works
Mitochondrial DNA Copy Number: Linking Diabetes and Cancer
Memon, A. A., Vats, S., Sundquist, J., Li, Y., & Sundquist, K. (2022) · Antioxidants and Redox Signaling · doi:10.1089/ars.2022.0100 · Cited by 19 · see citing works
Sciannimanico, S. M., Grimaldi, F., Vescini, F., Pergola, G. D., Iacoviello, M., Licchelli, B., Guastamacchia, E., Giagulli, V. A., & Triggiani, V. (2019) · Endocrine Metabolic & Immune Disorders - Drug Targets · doi:10.2174/1871530319666190507125847 · Cited by 20 · see citing works
Li, C., Kuang, J., Zhao, Y., Sun, H., & Guan, H. (2020) · Endocrine · doi:10.1007/s12020-020-02291-8 · Cited by 19 · see citing works
Stidsen, J. V., Nielsen, J. S., Henriksen, J. E., Friborg, S. G., Thomsen, R. W., Olesen, T. B., Olsen, M. H., & Beck‐Nielsen, H. (2017) · BMJ Open · doi:10.1136/bmjopen-2017-017493 · Cited by 18 · see citing works
Screening of GPCR drugs for repurposing in breast cancer
Abdulkareem, N. M., Bhat, R. R., Powell, R. T., Chikermane, S. G., Yande, S., Trinh, L., Abdelnasser, H. Y., Tabassum, M., Ruiz, A., Sobieski, M. M., et al. (2022) · Frontiers in Pharmacology · doi:10.3389/fphar.2022.1049640 · Cited by 18 · see citing works
Phyotochemical candidates repurposing for cancer therapy and their molecular mechanisms
Jung, J. H., Hwang, J., Kim, J., Sim, D. Y., Im, E., Park, J. E., Park, W. Y., Shim, B., Kim, B., & Kim, S. (2019) · Seminars in Cancer Biology · doi:10.1016/j.semcancer.2019.12.009 · Cited by 18 · see citing works
An Observational Study on Breast Cancer Survival and Lifestyle Related Risk Factors
Kreklau, A., Nel, I., Kasimir‐Bauer, S., Kimmig, R., Frackenpohl, A., & Aktas, B. (2021) · In Vivo · doi:10.21873/invivo.12344 · Cited by 17 · see citing works
Early-Phase Interventional Trials in Oral Cancer Prevention
McCarthy, C., Fedele, S., Ottensmeier, C. H. H., & Shaw, R. (2021) · Cancers · doi:10.3390/cancers13153845 · Cited by 17 · see citing works
Impact of diabetes on the increased risk of hepatic cancer: An updated review of biological aspects
Das, B. K., & Gadad, P. C. (2021) · Diabetes Epidemiology and Management · doi:10.1016/j.deman.2021.100025 · Cited by 15 · see citing works
Ghiasi, B., Sarokhani, D., Najafi, F., Motedayen, M., & Dehkordi, A. H. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666190215123759 · Cited by 15 · see citing works
Schwartz, S. S., Grant, S. F. A., & Herman, M. E. (2019) · Postgraduate Medicine · doi:10.1080/00325481.2019.1657358 · Cited by 15 · see citing works
Mesquita, L. A., Spiazzi, B. F., Piccoli, G. F., Nogara, D. A., da Natividade, G. R., Garbin, H. I., Wayerbacher, L. F., Wiercinski, V. M., Baggio, V. A., Zingano, C. P., et al. (2024) · Diabetes Obesity and Metabolism · doi:10.1111/dom.15509 · Cited by 17 · see citing works
Treatment Effects in Randomized and Nonrandomized Studies of Pharmacological Interventions
Salcher‐Konrad, M., Nguyen, M., Savović, J., Higgins, J. P. T., & Naci, H. (2024) · JAMA Network Open · doi:10.1001/jamanetworkopen.2024.36230 · Cited by 14 · see citing works
Kim, D. B., Lee, K., Lee, J. M., Ko, S., Han, K., & Park, Y. G. (2020) · Journal of Gastroenterology and Hepatology · doi:10.1111/jgh.15152 · Cited by 13 · see citing works
Shah, R. R. (2016) · Drug Safety · doi:10.1007/s40264-016-0485-y · Cited by 13 · see citing works
Drug repositioning in thyroid cancer treatment: the intriguing case of anti-diabetic drugs
Greco, A., Coperchini, F., Croce, L., Magri, F., Teliti, M., & Rotondi, M. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1303844 · Cited by 12 · see citing works
Wong, C. K. H., Man, K. K. C., Chan, E. W., Wu, T., Tse, E. T. Y., Wong, I. C. K., & Lam, C. L. K. (2020) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2020-001346 · Cited by 12 · see citing works
Arima, R., Marttila, M., Hautakoski, A., Arffman, M., Sund, R., Ilanne‐Parikka, P., Kangaskokko, J., Urpilainen, E., Läärä, E., Hinkula, M., et al. (2018) · Anticancer Research · doi:10.21873/anticanres.12710 · Cited by 11 · see citing works
Thiazolidinedione Use in Individuals With Type 2 Diabetes and Chronic Obstructive Pulmonary Disease
Yen, F., Wei, J. C., Yang, Y., Hsu, C., & Hwu, C. (2021) · Frontiers in Medicine · doi:10.3389/fmed.2021.729518 · Cited by 10 · see citing works
Obesity: Molecular Mechanisms, Epidemiology, Complications and Pharmacotherapy
Jaberi, S. A., Cohen, A., Saeed, Z., Ojha, S. K., Singh, J., & Adeghate, E. A. (2021) · Advances in biochemistry in health and disease · doi:10.1007/978-3-030-84763-0_13 · Cited by 10 · see citing works
AWRK6, a Novel GLP-1 Receptor Agonist, Attenuates Diabetes by Stimulating Insulin Secretion
Wang, Q., Zhao, C., Jin, L., Zhang, H., Miao, Q., Liu, H., & Zhang, D. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19103053 · Cited by 9 · see citing works
Sani, D. H., Munna, A. N., Alam, M. J., Salim, M., & Alam, M. J. (2020) · Current Nutrition & Food Science · doi:10.2174/1573401316999200728183434 · Cited by 9 · see citing works
Fan, H., Shikun, B. A. I., Guan, X., Wen, M. A., Fu, Y., Zhang, X., Lili, D. E. N. G., & Tian, J. (2021) · Minerva Endocrinology · doi:10.23736/s2724-6507.21.03289-2 · Cited by 9 · see citing works
- Authors
- Wu, L., Zhu, J., Prokop, L. J., & Murad, M. H.
- Affiliations
- Mayo Clinic (US)
- University of Minnesota (US)
- Corresponding author
- Wu, Lang
- Venue
- Scientific Reports
- Published
- 2015-06-15
- Volume
- 5
- Issue
- 1
- Pages
- 10147-10147
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC4467243
- OpenAlex
- W2262375108
- Cited by
- 144
- References
- 58
- Citations by year
- 2026: 3 · 2025: 3 · 2024: 12 · 2023: 10 · 2022: 15 · 2021: 17 · 2020: 11 · 2019: 15 · 2018: 13 · 2017: 24 · 2016: 10 · 2015: 11
- FWCI
- 1.88
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- Mayo Clinic
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
- Health Sciences › Medicine › Oncology › Cancer Risks and Factors
- Keywords
- diabetes mellitus, antidiabetic drugs, cancer risk, cancer mortality, metformin, thiazolidinediones, insulin, sulfonylureas, alpha-glucosidase inhibitors, drug safety, cancer incidence
- MeSH terms
- Diabetes Mellitus, Type 2, Humans, Hypoglycemic Agents, Insulin, Metformin, Neoplasms, Risk, Sulfonylurea Compounds, Odds Ratio, Randomized Controlled Trials as Topic, Thiazolidinediones, Glycoside Hydrolase Inhibitors
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
