The DOI matches its Crossref record; 113 of the 115 references it cites were found in a registry or an index.
Metformin and Cancer Risk and Mortality: A Systematic Review and Meta-analysis Taking into Account Biases and Confounders
Open accessPublished version of a preprint
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.
Overview
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
Verification
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?
The source backs part of the claim, not all of it — or backs it for a different population, condition or comparison.
In the citing paper
“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]
Experimental — accuracy not yet measuredThe cited source says what the claim attributes to it.
In the citing paper
“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
In the citing paper
“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
In the citing paper
“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]
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
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
Cited by
Sorted by citations
Items 101–200 of 457
Rao, M., Gao, C., Guo, M., Law, B. Y. K., & Xu, Y. (2018) · Cancer Management and Research · doi:10.2147/cmar.s174535 · Cited by 54
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 56
Davies, G. F., Lobanova, L., Dawicki, W., Groot, G., Gordon, J., Bowen, M., Harkness, T. A. A., & Arnason, T. (2017) · PLoS ONE · doi:10.1371/journal.pone.0187191 · Cited by 53
Metformin and cancer in type 2 diabetes: a systematic review and comprehensive bias evaluation
Farmer, R. E., Ford, D., Forbes, H. J., Chaturvedi, N., Kaplan, R. S., Smeeth, L. L., & Bhaskaran, K. (2016) · International Journal of Epidemiology · doi:10.1093/ije/dyw275 · Cited by 53
Saito, A., Kitayama, J., Horie, H., Koinuma, K., Ohzawa, H., Yamaguchi, H., Kawahira, H., Mimura, T., Lefor, A. K., & Sata, N. (2020) · Cancer Science · doi:10.1111/cas.14615 · Cited by 53
Type 2 Diabetes in Neuroendocrine Tumors: Are Biguanides and Statins Part of the Solution?
Herrera-Martínez, A. D., Pedraza‐Arévalo, S., L‐López, F., Gahete, M. D., Gálvez-Moreno, M. Á., Castano, J. P., & Luque, R. M. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-01455 · Cited by 52
Cancer Therapy-Induced Cardiotoxicity—A Metabolic Perspective on Pathogenesis, Diagnosis and Therapy
Choksey, A., & Timm, K. N. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms23010441 · Cited by 76
Metformin and cancer: Between the bioenergetic disturbances and the antifolate activity
Jara, J. A., & López‐Muñoz, R. (2015) · Pharmacological Research · doi:10.1016/j.phrs.2015.06.014 · Cited by 50
Cancer incidence among Finnish people with type 2 diabetes during 1989–2014
Saarela, K., Tuomilehto, J., Sund, R., Keskimäki, I., Hartikainen, S. A., & Pukkala, . (2018) · European Journal of Epidemiology · doi:10.1007/s10654-018-0438-0 · Cited by 50
Metformin Benefits: Another Example for Alternative Energy Substrate Mechanism?
Giaccari, A., Solini, A., Frontoni, S., & Prato, S. D. (2021) · Diabetes Care · doi:10.2337/dc20-1964 · Cited by 54
Fontvieille, E., Viallon, V., Recalde, M., Córdova, R., Jansana, A., Peruchet‐Noray, L., Lennon, H., Heath, A. K., Aune, D., Christakoudi, S., et al. (2023) · BMC Medicine · doi:10.1186/s12916-023-03114-z · Cited by 55
Nie, Z., Zhu, H., & Gu, M. (2016) · Pharmaceutical Biology · doi:10.1080/13880209.2016.1176057 · Cited by 49
Insulin/IGF Axis in Breast Cancer: Clinical Evidence and Translational Insights
Biello, F., Platini, F., D’Avanzo, F., Cattrini, C., Mennitto, A., Genestroni, S., Martini, V., Marzullo, P., Aimaretti, G., & Gennari, A. (2021) · Biomolecules · doi:10.3390/biom11010125 · Cited by 52
p21cip1/waf1 Coordinates Autophagy, Proliferation and Apoptosis in Response to Metabolic Stress
Manu, K. A., Cao, P. H. A., Chai, T. F., Casey, P. J., & Wang, M. (2019) · Cancers · doi:10.3390/cancers11081112 · Cited by 47
Riera, C. E., & Dillin, A. G. (2015) · Nature Medicine · doi:10.1038/nm.4005 · Cited by 48
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
Metformin Use and Lung Cancer Risk in Patients with Diabetes
Sakoda, L. C., Ferrara, A. M., Achacoso, N. S., Peng, T., Ehrlich, S. F., Quesenberry, C. P., & Habel, L. A. (2015) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-14-0291 · Cited by 44
Diabetes, Diabetes Treatment, and Risk of Thyroid Cancer
Luo, J., Phillips, L. S., Liu, S., Wactawski‐Wende, J., & Margolis, K. L. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2015-3901 · Cited by 44
Mitochondria-targeted metformins: anti-tumour and redox signalling mechanisms
Kalyanaraman, B., Cheng, G., Hardy, M., Ouari, O., Sikora, A., Zielonka, J., & Dwinell, M. B. (2017) · Interface Focus · doi:10.1098/rsfs.2016.0109 · Cited by 44
Barbieri, F., Würth, R., Pattarozzi, A., Verduci, I., Mazzola, C., Cattaneo, M. G., Tonelli, M., Solari, A., Bajetto, A., Daga, A., et al. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00899 · Cited by 46
Brown, J. C., Zhang, S., Ligibel, J. A., Irwin, M. L., Jones, L. W., Campbell, N., Pollak, M., Sorrentino, A., Cartmel, B., Harrigan, M., et al. (2020) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-20-0188 · Cited by 45
The Influence of Metformin on IGF-1 Levels in Humans: A Systematic Review and Meta-Analysis
Yang, X., Kord-Varkaneh, H., Talaei, S., Clark, C. C. T., Zanghelini, F., Tan, S. C., Zarezadeh, M., Mousavi, S. M., Rahmani, J., & Zhang, Y. (2020) · Pharmacological Research · doi:10.1016/j.phrs.2019.104588 · Cited by 43
Expanding the therapeutic spectrum of metformin: from diabetes to cancer
Coperchini, F., Leporati, P., Rotondi, M., & Chiovato, L. (2015) · Journal of Endocrinological Investigation · doi:10.1007/s40618-015-0370-z · Cited by 43
Lin, J., Gill, A. A., Zahm, S. H., Carter, C. A., Shriver, C. D., Nations, J. A., Anderson, W. F., McGlynn, K. A., & Zhu, K. (2017) · International Journal of Cancer · doi:10.1002/ijc.30724 · Cited by 44
European Code against Cancer 4th Edition: Medical exposures, including hormone therapy, and cancer
Friis, S., Kesminiene, A., Espina, C., Auvinen, A. P., Straíf, K., & Schüz, J. (2015) · Cancer Epidemiology · doi:10.1016/j.canep.2015.08.003 · Cited by 45
Changing patterns of sexually transmitted infections in India.
Sharma, V., & Khandpur, S. (2004) · PubMed · Cited by 42
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
Metformin inhibits cell cycle progression of B-cell chronic lymphocytic leukemia cells
Bruno, S., Ledda, B., Tenca, C., Ravera, S., Orengo, A. M., Mazzarello, A. N., Pesenti, E., Casciaro, S., Racchi, O., Ghiotto, F., et al. (2015) · Oncotarget · doi:10.18632/oncotarget.4168 · Cited by 42
Self-citationLennon, F. E., Cianci, G. C., Kanteti, R., Riehm, J., Arif, Q., Poroyko, V. A., Lupovitch, E., Vigneswaran, W. T., Husain, A. N., Chen, P., et al. (2016) · Scientific Reports · doi:10.1038/srep24578 · Cited by 41
Mayer, M., Klotz, L. H., & Venkateswaran, V. (2016) · The Journal of Urology · doi:10.1016/j.juro.2016.10.069 · Cited by 41
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
Rotondi, M., Coperchini, F., Pignatti, P., Magri, F., & Chiovato, L. (2015) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-3045 · Cited by 40
Metabolomics profiling of metformin-mediated metabolic reprogramming bypassing AMPKα
Yan, M., Qi, H., Xia, T., Zhao, X., Wang, W., Wang, Z., Lu, C., Ning, Z., Chen, H., Li, T., et al. (2018) · Metabolism · doi:10.1016/j.metabol.2018.11.010 · Cited by 40
Singh, A., Gu, J. J., Zhang, Q., Torka, P., Sundaram, S., Mavis, C. K., & Hernandez‐Ilizaliturri, F. J. (2020) · Cancer & Metabolism · doi:10.1186/s40170-020-00213-w · Cited by 40
Hirose, S., Matsumoto, K., Tatemichi, M., Tsuruya, K., Anzai, K., Arase, Y., Shiraishi, K., Suzuki, M., Ieda, S., & Kagawa, T. (2020) · PLoS ONE · doi:10.1371/journal.pone.0241770 · Cited by 40
Rani, R., Hajam, Y. A., Kumar, R., Bhat, R. A., Rai, S., & Rather, M. A. (2021) · Phytomedicine Plus · doi:10.1016/j.phyplu.2021.100161 · Cited by 45
Gorica, E., Mohammed, S. A., Ambrosini, S., Calderone, V., Costantino, S., & Paneni, F. (2022) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2022.923014 · Cited by 39
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 42
Repurposing metabolic regulators: antidiabetic drugs as anticancer agents
Dhas, Y., Biswas, N., Divyalakshmi, M. R., Jones, L., & Ashili, S. (2024) · Molecular Biomedicine · doi:10.1186/s43556-024-00204-z · Cited by 45
Metformin: A promising drug for human cancers (Review)
Wu, H., Huang, D., Zhou, H., Sima, X., Wu, Z., Sun, Y., Wang, L., Ruan, Y., Wu, Q., Wu, F., et al. (2022) · Oncology Letters · doi:10.3892/ol.2022.13325 · Cited by 38
Taming expectations of metformin as a treatment to extend healthspan
Konopka, A. R., & Miller, B. F. (2019) · GeroScience · doi:10.1007/s11357-019-00057-3 · Cited by 42
Epidemiology and Inherited Predisposition for Sporadic Pancreatic Adenocarcinoma
Stolzenberg‐Solomon, R. Z., & Amundadottir, L. T. (2015) · Hematology/Oncology Clinics of North America · doi:10.1016/j.hoc.2015.04.009 · Cited by 37
New drugs are not enough‑drug repositioning in oncology: An update
Armando, R., Mengual G�mez, D., & Gomez, D. (2020) · International Journal of Oncology · doi:10.3892/ijo.2020.4966 · Cited by 90
Kim, K., Choi, S., & Park, S. M. (2018) · European Journal of Cancer · doi:10.1016/j.ejca.2018.07.008 · Cited by 36
Han, K. C.-Z., Fyles, A., Shek, T. L. T., Croke, J. M., Dhani, N. C., D'Souza, D. P., Lee, T., Chaudary, N., Bruce, J. P., Pintilie, M., et al. (2022) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-22-1665 · Cited by 36
Metformin Use and Risk of Prostate Cancer: Results from the REDUCE Study
Feng, T., Sun, X., Howard, L. E., Vidal, A. C., Freedland, A. R., Moreira, D. M., Castro‐Santamaria, R., Andriole, G. L., & Freedland, S. J. (2015) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-15-0141 · Cited by 37
Colon neoplasia in patients with type 2 diabetes on metformin: A meta-analysis
Rokkas, T., & Portincasa, P. (2016) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2016.05.027 · Cited by 34
Soo, S. K., Rudich, P. D., Traa, A., Harris-Gauthier, N., Shields, H. J., & Raamsdonk, J. M. V. (2020) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2020.111297 · Cited by 37
Targeting breast cancer and their stem cell population through AMPK activation: novel insights
Uprety, B., & Abrahamse, H. (2022) · Cells · doi:10.3390/cells11030576 · Cited by 33
A Retrospective Study on the Role of Diabetes and Metformin in Colorectal Cancer Disease Survival
Ramjeesingh, R., Orr, C., Bricks, C. S., Hopman, W. M., & Hammad, N. (2016) · Current Oncology · doi:10.3747/co.23.2809 · Cited by 34
Bhaw‐Luximon, A., & Jhurry, D. (2016) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-016-2178-4 · Cited by 34
Serrano, D., Bonanni, B., & Brown, K. (2019) · Molecular Oncology · doi:10.1002/1878-0261.12461 · Cited by 34
Barbieri, F., Verduci, I., Carlini, V., Zona, G., Pagano, A., Mazzanti, M., & Florio, T. (2019) · Frontiers in Oncology · doi:10.3389/fonc.2019.00135 · Cited by 34
Shikuma, C. M., Chew, G. M., Kohorn, L. B., Souza, S. A., Chow, D. C., SahBandar, I. N., Park, E. Y., Hanks, N., Gangcuangco, L. M. A., Gerschenson, M., et al. (2019) · AIDS Research and Human Retroviruses · doi:10.1089/aid.2019.0078 · Cited by 33
Association Between Lifestyle Changes, Mammographic Breast Density, and Breast Cancer
Lester, S. P., Kaur, A. S., & Vegunta, S. (2022) · The Oncologist · doi:10.1093/oncolo/oyac084 · Cited by 34
Age-related diseases, therapies and gut microbiome: A new frontier for healthy aging
Barone, M., D’Amico, F., Rampelli, S., Brigidi, P., & Turroni, S. (2022) · Mechanisms of Ageing and Development · doi:10.1016/j.mad.2022.111711 · Cited by 34
MATE2 Expression Is Associated With Cancer Cell Response to Metformin
Chowdhury, S., Yung, E., Pintilie, M., Muaddi, H., Chaib, S., Yeung, M., Fusciello, M., Sykes, J., Pitcher, B., Hagenkort, A., et al. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165214 · Cited by 33
High efficacy of intravesical treatment of metformin on bladder cancer in preclinical model
Peng, M., Su, Q., Zeng, Q., Li, L., Liu, Z., Xue, L., Cheng, Y., Huang, Y., Tao, T., Lv, H., et al. (2016) · Oncotarget · doi:10.18632/oncotarget.6933 · Cited by 33
Júnior, A. D. D. C., Pericole, F. V., & Carvalheira, J. B. C. (2018) · Clinics · doi:10.6061/clinics/2018/e412s · Cited by 32
Jacobi, O., Landman, Y., Reinhorn, D. J., Icht, O., Sternschuss, M., Rotem, O., Finkel, I., Allen, A. M., Dudnik, E., Goldstein, D. A., et al. (2021) · Oncology · doi:10.1159/000516671 · Cited by 34
Metformin reduces glycometabolism of papillary thyroid carcinoma in vitro and in vivo
Shen, C., Wei, W., Qiu, Z., Song, H.-J., Zhang, X., Sun, Z., & Luo, Q. (2016) · Journal of Molecular Endocrinology · doi:10.1530/jme-16-0134 · Cited by 32
de Jong, R. G., Burden, A. M., de Kort, S., van Herk‐Sukel, M. P. P., Vissers, P. A. J., Janssen, P. K. C., Haak, H. R., Masclee, A., de Vries, F., & Janssen-Heijnen, M. L. G. (2017) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-16-0277 · Cited by 36
Crawley, D., Chamberlain, F., Garmo, H., Rudman, S. M., Zethelius, B., Holmberg, L., Adolfsson, J., Stattin, P. E., Carroll, P., & Hemelrijck, M. V. (2018) · ecancermedicalscience · doi:10.3332/ecancer.2018.802 · Cited by 32
Mechanisms of ageing: growth hormone, dietary restriction, and metformin
Khan, J., Pernicova, I., Nisar, K., & Korbonits, M. (2023) · The Lancet Diabetes & Endocrinology · doi:10.1016/s2213-8587(23)00001-3 · Cited by 34
Metformin: From diabetes to cancer to prolongation of life
Sirtori, C. R., Castiglione, S., & Pavanello, C. (2024) · Pharmacological Research · doi:10.1016/j.phrs.2024.107367 · Cited by 38
Serrano, D., Lazzeroni, M., & Bonanni, B. (2014) · Molecular Oncology · doi:10.1016/j.molonc.2014.12.006 · Cited by 31
DeCensi, A., Puntoni, M., Guerrieri‐Gonzaga, A., Cazzaniga, M., Serrano, D., Lazzeroni, M., Vingiani, A., Gentilini, O., Petrera, M., Viale, G., et al. (2015) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-15-0048 · Cited by 31
Self-citationWhy does obesity promote cancer? Epidemiology, biology, and open questions
Mazzarella, L. (2015) · ecancermedicalscience · doi:10.3332/ecancer.2015.554 · Cited by 31
Minimizing Membrane Arachidonic Acid Content as a Strategy for Controlling Cancer: A Review
McCarty, M. F., & DiNicolantonio, J. J. (2018) · Nutrition and Cancer · doi:10.1080/01635581.2018.1470657 · Cited by 31
Wang, Y., Liu, X., Yan, P., Tang, J., Chen, T., Sun, Y., Zhou, W., Bi, Y., & Zhang, Z.-J. (2019) · European Journal of Cancer Prevention · doi:10.1097/cej.0000000000000514 · Cited by 32
Effects of Metformin on the virus/host cell crosstalk in human papillomavirus‐positive cancer cells
Hoppe‐Seyler, K., Herrmann, A. L., Däschle, A., Kuhn, B. J., Strobel, T. D., Lohrey, C., Bulkescher, J., Krijgsveld, J., & Hoppe‐Seyler, F. (2021) · International Journal of Cancer · doi:10.1002/ijc.33594 · Cited by 31
Action Mechanism of Metformin and Its Application in Hematological Malignancy Treatments: A Review
Zhang, Y., Zhou, F., Guan, J., Zhou, L., & Chen, B. (2023) · Biomolecules · doi:10.3390/biom13020250 · Cited by 38
Suissa, S., Dell’Aniello, S., & Renoux, C. (2023) · Epidemiology · doi:10.1097/ede.0000000000001628 · Cited by 35
Tan, M. H., Alquraini, H., Mizokami‐Stout, K., & MacEachern, M. (2016) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2016.06.008 · Cited by 33
Vicentini, M., Ballotari, P., Rossi, P. G., Venturelli, F., Sacchettini, C., Greci, M., Mangone, L., Pezzarossi, A., & Manicardi, V. (2018) · Diabetes Research and Clinical Practice · doi:10.1016/j.diabres.2018.04.036 · Cited by 30
Synergistic anti-tumor effects of liraglutide with metformin on pancreatic cancer cells
Lu, R., Yang, J., Wei, R., Ke, J., Tian, Q., Yu, F., Liu, J., Zhang, J., & Hong, T. (2018) · PLoS ONE · doi:10.1371/journal.pone.0198938 · Cited by 30
Recent Advances in the Development of Fatty Acid Synthase Inhibitors as Anticancer Agents
Singh, S., Karthikeyan, C., & Moorthy, N. S. H. N. (2020) · Mini-Reviews in Medicinal Chemistry · doi:10.2174/1389557520666200811100845 · Cited by 30
Risk-reducing medications for primary breast cancer: a network meta-analysis
D, S. M. M., Goodwin, A., & Pasquali, S. (2019) · Cochrane Database of Systematic Reviews · doi:10.1002/14651858.cd012191.pub2 · Cited by 31
Bahardoust, M., Mousavi, S., Moezi, Z. D., Yarali, M., Tayebi, A., Olamaeian, F., & Tizmaghz, A. (2023) · Journal of Gastrointestinal Cancer · doi:10.1007/s12029-023-00955-y · Cited by 30
Anti-Aging Effect of Metformin: A Molecular and Therapeutical Perspective
Torres, W., Nava, M., Galbán, N., Gómez, Y., Morillo, V., Rojas, M., Cano, C., Chacín, M., D’Marco, L., Herazo-Beltrán, Y., et al. (2020) · Current Pharmaceutical Design · doi:10.2174/1381612826666200716161610 · Cited by 28
Metal Complex Formation and Anticancer Activity of Cu(I) and Cu(II) Complexes with Metformin
Abdelrahman, S., Alghrably, M., Campagna, M., Hauser, C. A. E., Jaremko, M., & Lachowicz, J. I. (2021) · Molecules · doi:10.3390/molecules26164730 · Cited by 29
Caparrotti, F., O’Sullivan, B., Bratman, S. V., Ringash, J. G., Lu, L., Bayley, A., Cho, J., Giuliani, M., Hope, A. J., Kim, J., et al. (2016) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2016.11.044 · Cited by 28
Exercise-Pharmacology Interactions: Metformin, Statins, and Healthspan
Miller, B. F., & Thyfault, J. P. (2020) · Physiology · doi:10.1152/physiol.00013.2020 · Cited by 30
Recycling the Purpose of Old Drugs to Treat Ovarian Cancer
Nunes, M., Abreu, M. H., Bartosch, C., & Ricardo, S. A. V. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21207768 · Cited by 29
Mao, D., Lau, E. S. H., Wu, H., Yang, A., Shi, M., Fan, B., Tam, C. H. T., Chow, E., Kong, A. P. S., Ronald, C. W., et al. (2021) · The Lancet Regional Health - Western Pacific · doi:10.1016/j.lanwpc.2021.100315 · Cited by 31
Controversial association between polycystic ovary syndrome and breast cancer
Carvalho, M. J., Subtil, S., Rodrigues, Â. R., Oliveira, J., & Figueiredo-Dias, M. (2019) · European Journal of Obstetrics & Gynecology and Reproductive Biology · doi:10.1016/j.ejogrb.2019.10.011 · Cited by 28
The therapeutic potential of metformin in gastric cancer
Courtois, S., Lehours, P., & Bessède, E. (2019) · Gastric Cancer · doi:10.1007/s10120-019-00952-w · Cited by 26
Targeting Myotonic Dystrophy Type 1 with Metformin
García-Puga, M., Saenz‐Antoñanzas, A., Matheu, A., & de Munaín, A. L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052901 · Cited by 26
Teh, J. T., Zhu, W., Newgard, C. B., Casey, P. J., & Wang, M. (2019) · Molecular Cancer Therapeutics · doi:10.1158/1535-7163.mct-18-0766 · Cited by 27
Diabetes and Cancer: A Twisted Bond
Stan, M. C., & Paul, D. (2024) · Oncology Reviews · doi:10.3389/or.2024.1354549 · Cited by 30
Gennari, A., Foca, F., Zamarchi, R., Rocca, A., Amadori, D., DeCensi, A., Bologna, A., Cavanna, L., Gianni, L., Scaltriti, L., et al. (2020) · Breast Cancer Research and Treatment · doi:10.1007/s10549-020-05596-4 · Cited by 27
Self-citationMetformin Use and the Risk of Cancer in Patients with Diabetes: A Nationwide Sample Cohort Study
Oh, T. K., & Song, I. (2019) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-19-0427 · Cited by 26
Chen, C. B., Eskin, M., Eurich, D. T., Majumdar, S. R., & Johnson, J. A. (2018) · BMC Cancer · doi:10.1186/s12885-017-3934-9 · Cited by 26
Wang, Y., Maurer, M. J., Larson, M. C., Allmer, C., Feldman, A. L., Bennani, N. N., Thompson, C. A., Porrata, L. F., Habermann, T. M., Witzig, T. E., et al. (2019) · British Journal of Haematology · doi:10.1111/bjh.15997 · Cited by 24
Takaki, A., Kawano, S., Uchida, D., Takahara, M., Hiraoka, S., & Okada, H. (2019) · Cancers · doi:10.3390/cancers11020213 · Cited by 24
Targeting the pH Paradigm at the Bedside: A Practical Approach
Koltai, T. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21239221 · Cited by 24
Huynh, T. Y. L., Ościłowska, I., Sáiz, J., Nizioł, M., Baszanowska, W., Barbas, C., & Palka, J. A. (2021) · Biomolecules · doi:10.3390/biom11121888 · Cited by 23
Antihypertensive agents and the risk of breast cancer in women aged 55 years and older
Chang, C., Chiang, C., Yen, C., Wu, L., Lin, J., & Lai, M. (2016) · Journal of Hypertension · doi:10.1097/hjh.0000000000000813 · Cited by 24
Tang, B., Li, X., Wang, Y., Sjölander, A., Johnell, K., Thambisetty, M., Ferrucci, L., Reynolds, C. A., Finkel, D., Jylhävä, J., et al. (2023) · GeroScience · doi:10.1007/s11357-023-00784-8 · Cited by 25
Kim, B., Han, S., Lee, H., Park, C. H., Chung, Y. M., Shin, K., Lee, H. G., & Ye, S. (2014) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2014.11.054 · Cited by 24
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
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