Effect of Metformin on Survival Outcomes in Diabetic Patients With Triple Receptor-Negative Breast Cancer
Open accessAbstract
BACKGROUND: Recent observational studies have shown that metformin use in diabetic patients decreases both cancer incidence and mortality. Metformin use is also independently predictive of pathologic complete response. In the current study, the authors explored the association between metformin use and survival outcomes in patients with triple receptor-negative breast cancer (TNBC) who were receiving adjuvant chemotherapy. METHODS: The Breast Cancer Management System database of The University of Texas MD Anderson Cancer Center identified 1448 women who received adjuvant chemotherapy for TNBC between 1995 and 2007. Patients were categorized by diabetes status and metformin use. The Kaplan-Meier product-limit method was used to calculate distant metastasis-free survival (DMFS), recurrence-free survival (RFS), and overall survival (OS). Cox proportional hazards models were fit to determine the association between metformin use and survival outcomes. RESULTS: The study cohort was comprised of 63 diabetic patients receiving treatment with metformin, 67 diabetic patients not receiving metformin, and 1318 nondiabetic patients. Patients in the diabetic groups tended to be older (P = .005); more diabetic patients were postmenopausal (P = .0007), black (P = .0001), and obese (P < .0001). At a median follow-up of 62 months, there were no significant differences with regard to 5-year DMFS (P = .23), RFS (P = .38), and OS (P = .58) between the 3 groups. Compared with the metformin group, patients who did not receive metformin (hazard ratio [HR], 1.63; 95% confidence interval [95% CI], 0.87-3.06 [P = .13]) and nondiabetic patients (HR, 1.62; 95% CI, 0.97-2.71 [P = .06]) tended to have a higher risk of distant metastases. CONCLUSIONS: The findings of the current study suggest that metformin use during adjuvant chemotherapy does not significantly impact survival outcomes in diabetic patients with TNBC.
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A retrospective analysis of patients with T2DM and TNBC by Bayraktar et al. indicated that treatment with adjuvant metformin was not associated with a significantly improved survival.
“In contrast to the data from in vitro studies, a retrospective analysis of patients with T2DM and TNBC by Bayraktar et al. indicated that treatment with adjuvant metformin was not associated with a significantly improved survival and concluding the need for data from prospective Phase III randomized studies (252).”
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 [252]
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BackgroundAssociation Between Metformin Therapy and Mortality After Breast Cancer
Lega, I. C., Austin, P. C., Gruneir, A., Goodwin, P. J., Rochon, P. A., & Lipscombe, L. L. (2013) · Diabetes Care · doi:10.2337/dc12-2535 · Cited by 110 · see citing works
Xu, H., Chen, K., Jia, X., Tian, Y., Dai, Y., Li, D., Xie, J., Tao, M., & Mao, Y. (2015) · The Oncologist · doi:10.1634/theoncologist.2015-0096 · Cited by 110 · see citing works
Kim, H. J., Kwon, H., Lee, J. W., Kim, H. J., Lee, S. B., Park, H. S., Sohn, G., Lee, Y., Koh, B. S., Yu, J. H., et al. (2015) · Breast Cancer Research · doi:10.1186/s13058-015-0574-3 · Cited by 97 · see citing works
“[17] reported that metformin use during adjuvant chemotherapy does not significantly impact survival outcomes in diabetic patients with triple-negative breast cancer.”
BackgroundLin, H., Li, N., He, H., Ying, Y., Sunkara, S., Luo, L., Lv, N., Huang, D., & Luo, Z. (2015) · Molecular Pharmacology · doi:10.1124/mol.115.099549 · Cited by 95 · see citing works
Hadad, S. M., Coates, P. J., Jordan, L. B., Dowling, R. J. O., Chang, M. C., Done, S. J., Purdie, C. A., Goodwin, P. J., Stambolic, V., Moulder-Thompson, S. L., et al. (2015) · Breast Cancer Research and Treatment · doi:10.1007/s10549-015-3307-5 · Cited by 94 · see citing works
Hou, G., Zhang, S., Zhang, X., Wang, P., Hao, X., & Zhang, J. (2013) · Breast Cancer Research and Treatment · doi:10.1007/s10549-012-2404-y · Cited by 94 · see citing works
“In addition, although these patients with triple negative breast cancer and diabetes showed no significant differences in terms of 5-year distant metastasis rate, recurrence rate, and overall survival rate, the nonmetformin-treated subgroup, compared with the metformin-treated subgroup, showed a tendency (although not…”
ResultGAO, Z.-Y., Liu, Z., Bi, M., Zhang, J., Han, Z., Han, X., WANG, H.-Y., Sun, G., & Liu, H. (2016) · Experimental and Therapeutic Medicine · doi:10.3892/etm.2016.3143 · Cited by 91 · see citing works
“Moreover, a number of clinical studies have shown that the survival rate of cancer patients is improved by treatment with metformin (16-19).”
Ferroni, P., Riondino, S., Buonomo, O., Palmirotta, R., Guadagni, F., & Roselli, M. (2015) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2015/183928 · Cited by 87 · see citing works
Metformin in obesity, cancer and aging: addressing controversies
Berstein, L. M. (2012) · Aging · doi:10.18632/aging.100455 · Cited by 85 · see citing works
“It should be noted that when cancer-related mortality, rather than cancer risk, is assessed in diabetics (once again, at ages mainly above 50), the belief that their survival is better in metformin-treated groups is not always confirmed for prostate and breast cancer [48, 49], although one study does suggest better su…”
BackgroundRETRACTED: Metformin and Breast Cancer: Where Are We Now?
Solís, M. C., Martı́n-Castillo, B., Menéndez, J. A., & Pernas, S. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23052705 · Cited by 85 · see citing works
RetractedAMP-activated protein kinase: a potential therapeutic target for triple-negative breast cancer
Cao, W., Li, J., Hao, Q., Vadgama, J. V., & Wu, Y. (2019) · Breast Cancer Research · doi:10.1186/s13058-019-1107-2 · Cited by 84 · see citing works
Leptin and Adiponectin: Emerging Therapeutic Targets in Breast Cancer
Surmacz, E. (2013) · Journal of Mammary Gland Biology and Neoplasia · doi:10.1007/s10911-013-9302-8 · Cited by 80 · see citing works
“non-metformin group, however, it did not improve survival in this population [152].”
BackgroundMetformin use and gynecological cancers: A novel treatment option emerging from drug repositioning
Gadducci, A., Biglia, N., Tana, R., Cosio, S., & Gallo, M. (2016) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2016.06.006 · Cited by 84 · see citing works
“treated with metformin, diabetic patients not treated with metformin, and non-diabetic patients (139) .”
BackgroundMetformin: The hidden chronicles of a magic drug
Mahmood, K., Naeem, M., & Rahimnajjad, N. A. (2012) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2012.10.011 · Cited by 79 · see citing works
“A current prospective cohort study suggests that metformin use during adjuvant chemotherapy does not significantly impact survival outcomes in diabetic patients with TNBC (Triple Negative Breast Cancer) [96].”
BackgroundMitochondrial remodeling in cancer metabolism and survival: Potential for new therapies
Barbosa, I. A., Machado, N. G., Skildum, A. J., Scott, P. M., & Oliveira, P. J. (2012) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2012.04.005 · Cited by 75 · see citing works
Xie, J., Ye, J., Cai, Z., Luo, Y., Zhu, X., Deng, Y., Feng, Y., Liang, Y., Liu, R., Han, Z., et al. (2020) · Cancer Research · doi:10.1158/0008-5472.can-19-2852 · Cited by 74 · see citing works
“Some studies also argued that metformin treatment does not have beneficial effect in patients with cancers (24, 25).”
BackgroundThe Pathophysiological Significance of Fibulin-3
Livingstone, I., Uversky, V. N., Furniss, D., & Wiberg, A. (2020) · Biomolecules · doi:10.3390/biom10091294 · Cited by 70 · see citing works
Chan, D. S. M., Vieira, R. D. C. P. A., Abar, L., Aune, D., Balducci, K., Cariolou, M., Greenwood, D. C., Markozannes, G., Nanu, N., Becerra‐Tomás, N., et al. (2022) · International Journal of Cancer · doi:10.1002/ijc.34322 · Cited by 71 · see citing works
“In addition, 119 publications were descriptively synthesized(139-257) and 156 publications were excluded.(258-413)”
BackgroundCancer stem cells, lymphangiogenesis, and lymphatic metastasis
Li, S., & Li, Q. (2014) · Cancer Letters · doi:10.1016/j.canlet.2014.12.013 · Cited by 67 · see citing works
Recent Advances in the Use of Metformin: Can Treating Diabetes Prevent Breast Cancer?
Hatoum, D., & McGowan, E. M. (2015) · BioMed Research International · doi:10.1155/2015/548436 · Cited by 65 · see citing works
Metformin inhibits melanoma cell metastasis by suppressing the miR-5100/SPINK5/STAT3 axis
Suwei, D., Yanbin, X., Wang, J., Ma, X., Peng, Z., Jianping, K., Yunqing, W., & Li, Z. (2022) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-022-00353-5 · Cited by 64 · 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
“By contrast, one study showed that metformin did not affect survival of triple negative breast cancer patients (Bayraktar et al., 2012), and another report showed no survival benefits for breast cancer patients using metformin (Oppong et al., 2014).”
ResultBizjak, M., Malavašič, P., Dolinar, K., Pohar, J., Pirkmajer, S., & Pavlin, M. (2017) · Scientific Reports · doi:10.1038/s41598-017-01801-5 · Cited by 63 · see citing works
Metformin Decreases Circulating Androgen and Estrogen Levels in Nondiabetic Women With Breast Cancer
Campagnoli, C., Berrino, F., Venturelli, E., Abbà, C., Biglia, N., Brucato, T., Cogliati, P., Danese, S., Donadio, M., Zito, G., et al. (2013) · Clinical Breast Cancer · doi:10.1016/j.clbc.2013.08.012 · Cited by 59 · see citing works
Zhang, Y., Storr, S. J., Johnson, K., Green, A. R., Rakha, E. A., Ellis, I. O., Morgan, D. A. L., & Martin, S. G. (2014) · Oncotarget · doi:10.18632/oncotarget.2683 · Cited by 58 · see citing works
Metformin, an Old Drug, Brings a New Era to Cancer Therapy
He, H., Ke, R., Lin, H., Ying, Y., Liu, D., & Luo, Z. (2015) · The Cancer Journal · doi:10.1097/ppo.0000000000000103 · Cited by 55 · see citing works
Kawakita, E., Yang, F., Kumagai, A., Takagaki, Y., Kitada, M., Yoshitomi, Y., Ikeda, T., Nakamura, Y., Ishigaki, Y., Kanasaki, K., et al. (2020) · Molecular Cancer Research · doi:10.1158/1541-7786.mcr-20-0115 · Cited by 57 · see citing works
Drug repurposing—an emerging strategy in cancer therapeutics
Turabi, K. S., Deshmukh, A. J., Paul, S., Swami, D., Siddiqui, S., Kumar, U., Naikar, S., Devarajan, S., Basu, S., Paul, M. K., et al. (2022) · Naunyn-Schmiedeberg s Archives of Pharmacology · doi:10.1007/s00210-022-02263-x · Cited by 53 · see citing works
Molecular Pathways: Preclinical Models and Clinical Trials with Metformin in Breast Cancer
Thompson, A. M. (2014) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-13-0354 · Cited by 50 · see citing works
Prospective study of a diabetes risk reduction diet and the risk of breast cancer
Kang, J. H., Peng, C., Rhee, J. J., Farvid, M. S., Willett, W. C., Hu, F. B., ROSNER, B. A., Tamimi, R. M., & Eliassen, A. H. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa268 · Cited by 52 · see citing works
“This effect of metformin may operate through inhibition of the mTOR pathway (90); mTOR pathway deregulation is relatively prominent in TNBCs (91) and is associated with poor outcomes among TNBC patients (92, 93).”
The Effect of Metformin on Mortality Following Cancer among Patients with Diabetes
Lega, I. C., Shah, P. S., Margel, D., Beyene, J., Rochon, P. A., & Lipscombe, L. L. (2014) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-14-0327 · Cited by 50 · see citing works
The Antitumor Effect of Metformin Is Mediated by miR-26a in Breast Cancer
Cabello, P., Pineda, B., Tormo, E., Lluch, A. M., & Eroles, P. (2016) · International Journal of Molecular Sciences · doi:10.3390/ijms17081298 · Cited by 49 · see citing works
“However, although the beneficial effects of metformin on breast cancer patient survival rates has been described by several authors [32–34,43–46], little is known about the mechanism.”
BackgroundLiu, Z., Ren, L., Liu, C., Xia, T., Zha, X., & Wang, S. (2015) · PLoS ONE · doi:10.1371/journal.pone.0131207 · Cited by 50 · see citing works
Sui, X., Xu, Y., Yang, J., Fang, Y., Lou, H., Han, W., Zhang, M., Chen, W., Wang, K., Li, D., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0097781 · Cited by 49 · see citing works
“Metformin (1,1-dimethylbiguanide hydrochloride), a biguanide derivative which is widely used for treating diabetes mellitus, has been shown to exert potentially important anticancer effects [8,9], but others have not supported this view [10,11].”
BackgroundDiabetes, diabetes treatment and breast cancer prognosis
Luo, J., Virnig, B. A., HENDRYX, M. S., Wen, S., Chelebowski, R., Chen, C., Rohan, T. E., Tinker, L. F., Wactawski‐Wende, J., Lessin, L. S., et al. (2014) · Breast Cancer Research and Treatment · doi:10.1007/s10549-014-3146-9 · Cited by 49 · see citing works
“Three studies [16, 30, 40] found a significant inverse association between metformin therapy and allcause mortality, while three studies [4, 11, 20] did not.”
ResultThe effect of metformin on breast cancer outcomes in patients with type 2 diabetes
Oppong, B. A., Pharmer, L. A., Oskar, S., Eaton, A. A., Stempel, M. M., Patil, S. N., & King, T. A. (2014) · Cancer Medicine · doi:10.1002/cam4.259 · Cited by 47 · see citing works
“[29] analyzed women who received adjuvant chemotherapy for triple-negative BC.”
BackgroundCarbon Source and Myc Expression Influence the Antiproliferative Actions of Metformin
Javeshghani, S., Zakikhani, M., Austin, S., Bazile, M., Blouin, M., Topisirović, I., St‐Pierre, J., & Pollak, M. (2012) · Cancer Research · doi:10.1158/0008-5472.can-12-2907 · Cited by 47 · see citing works
“Some pharmacoepidemiologic studies have suggested that metformin may have antineoplastic activity (21-27) but others have not supported this view (28-31).”
BackgroundCai, H., Zhang, Y., Han, T. K., Everett, R. S., & Thakker, D. R. (2016) · International Journal of Cancer · doi:10.1002/ijc.29965 · Cited by 46 · see citing works
Use of Metformin and Survival of Diabetic Women with Breast Cancer
Peeters, P. J. H. L., Bazelier, M. T., Vestergaard, P., Leufkens, H. G. M., Schmidt, M. K., de Vries, F., & Bruin, M. L. D. (2013) · Current Drug Safety · doi:10.2174/15680266113136660069 · Cited by 46 · see citing works
Body mass index, diabetes, and triple-negative breast cancer prognosis
Tait, S. D., Pacheco, J. M., Gao, F., Bumb, C., Ellis, M. J., & Ma, C. X. (2014) · Breast Cancer Research and Treatment · doi:10.1007/s10549-014-3002-y · Cited by 46 · see citing works
“However, only one prior study has investigated the influence of diabetes on outcomes in TNBC [30] Since TNBC has limited treatment options, it is important to identify potential modifiable factors such as obesity and diabetes that could contribute to worse prognosis.”
BackgroundResultBaglia, M. L., Cui, Y., Zheng, T., Yang, G., Li, H., You, M., Xu, L., Murff, H. J., Gao, Y., Zheng, W., et al. (2018) · Cancer Research and Treatment · doi:10.4143/crt.2017.591 · Cited by 45 · see citing works
He, L., Lv, Y., Song, Y., & Zhang, B. (2019) · Cancer Management and Research · doi:10.2147/cmar.s213663 · Cited by 46 · see citing works
Vissers, P. A. J., Cardwell, C. R., van de Poll-Franse, L. V., Young, I. S., Pouwer, F., & Murray, L. (2015) · Breast Cancer Research and Treatment · doi:10.1007/s10549-015-3331-5 · Cited by 45 · see citing works
“These studies had several limitations such as small sample size[12,13,10], no”
BackgroundResultInfluentialObesity and cancer treatment efficacy: Existing challenges and opportunities
Ross‐Driscoll, K., Gogineni, K., Subhedar, P. D., Lin, J. Y., & McCullough, L. E. (2019) · Cancer · doi:10.1002/cncr.31976 · Cited by 45 · see citing works
Use of ACE Inhibitors and Angiotensin Receptor Blockers and Primary Breast Cancer Outcomes
Chae, Y. K., Brown, E. N., Lei, X. J., Melhem‐Bertrandt, A., Giordano, S. H., Litton, J. K., Hortobágyi, G. N., Gonzalez-Angulo, A. M., & Chávez‐MacGregor, M. (2013) · Journal of Cancer · doi:10.7150/jca.6888 · Cited by 44 · see citing works
“The type of ACEIs or ARBs and other medications that may affect pCR and relapse (beta-blocker, metformin) were also collected as we previously reported[24-27].”
ResultLin, 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 43 · see citing works
Chen, L., Chubak, J., Boudreau, D. M., Barlow, W. E., Weiss, N. S., & Li, C. I. (2017) · Cancer Research · doi:10.1158/0008-5472.can-17-0687 · Cited by 43 · see citing works
Banerjee, A., Birts, C. N., Darley, M., Parker, R., Mirnezami, A. H., West, J. J., Cutress, R., Beers, S. A., Rose-Zerilli, M. J. J., & Blaydes, J. P. (2018) · Carcinogenesis · doi:10.1093/carcin/bgy174 · Cited by 42 · see citing works
Impact of Statin Use on Outcomes in Triple Negative Breast Cancer
Shaitelman, S., Stauder, M., Allen, P., Reddy, S., Lakoski, S., Atkinson, B., Reddy, J., Amaya, D., Guerra, W., Ueno, N., et al. (2017) · Journal of Cancer · doi:10.7150/jca.18743 · Cited by 40 · see citing works
“Efforts have been made to identify existing, relatively low cost and low toxicity medications that can be repurposed for their anti-cancer effects in TNBC [4, 5].”
BackgroundChoi, H. S., Ko, G. H., Jin, H., Kang, K. M., Ha, I. B., Jeong, H., Song, H., Kim, H. J., & Jeong, B. K. (2021) · Molecules · doi:10.3390/molecules26175118 · Cited by 41 · see citing works
“In the field of oncology, with the advent of metformin, immunotherapy, and alpha-lipoic acid, interest is increasing in drug repurposing of nonanticancer drugs to anticancer drugs [9,10].”
BackgroundRepositioning metformin in cancer: genetics, drug targets, and new ways of delivery
Aldea, M. D., Craciun, L., Tomuleasa, C., Berindan‐Neagoe, I., Kacsó, G., Florian, I. Ş., & Crivii, C. B. (2014) · Tumor Biology · doi:10.1007/s13277-014-1676-8 · Cited by 40 · see citing works
“hepatocellular carcinoma) [5–9], breast [10, 11], prostate [12], ovarian [13, 14], or even lung cancer [15].”
Barakat, H. E., Hussein, R. R. S., Elberry, A. A., Zaki, M. A., & Ramadan, M. E. (2022) · Scientific Reports · doi:10.1038/s41598-022-11138-3 · Cited by 41 · see citing works
Hiding in plain view: the potential for commonly used drugs to reduce breast cancer mortality
Holmes, M. D., & Chen, W. Y. (2012) · Breast Cancer Research · doi:10.1186/bcr3336 · Cited by 40 · see citing works
Phase 1 Study of Erlotinib and Metformin in Metastatic Triple-Negative Breast Cancer
Fenn, K. M., Maurer, M., Lee, S. M., Crew, K. D., Trivedi, M. S., Accordino, M. K., Hershman, D. L., & Kalinsky, K. M. (2019) · Clinical Breast Cancer · doi:10.1016/j.clbc.2019.08.004 · Cited by 38 · see citing works
“Increased bilirubin 1 (33) --1 (20) ---”
Associations between diabetes medication use and risk of second breast cancer events and mortality
Calip, G. S., Yu, O., Hoskins, K. F., & Boudreau, D. M. (2015) · Cancer Causes & Control · doi:10.1007/s10552-015-0599-z · Cited by 37 · see citing works
“Other studies reported a beneficial effect of metformin in BC survivors including reduced BC-specific mortality in HER2? women [41] and reduced risk of distant metastases in triple receptor-negative BC [38].”
Hakimi, A. A., Chen, L., Kim, P. H., Sjoberg, D. D., Glickman, L., Walker, M. R., & Russo, P. (2013) · Canadian Urological Association Journal · doi:10.5489/cuaj.1447 · Cited by 35 · see citing works
Metformin: A Rising Star to Fight the Epithelial Mesenchymal Transition in Oncology
Barrière, G., Tartary, M., & Rigaud, M. (2013) · Anti-Cancer Agents in Medicinal Chemistry · doi:10.2174/1871520611313020018 · Cited by 35 · see citing works
“However they indicated a trend toward a decrease in the risk of developing distant metastases in diabetic patients receiving metformin [71].”
Rathmann, W., & Kostev, K. (2017) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2017.01.012 · Cited by 34 · see citing works
“Furthermore, a clinic-based observational study found that breast cancer patients with diabetes who did not takemetformin and patients without diabetes tended to have a higher risk of distant metastases (Bayraktar et al., 2012).”
BackgroundImpact of metformin on metastases in patients with breast cancer and type 2 diabetes
Jacob, L., Kostev, K., Rathmann, W., & Kalder, M. (2016) · Journal of Diabetes and its Complications · doi:10.1016/j.jdiacomp.2016.04.003 · Cited by 34 · see citing works
“71) tended to have a higher risk of distant metastases, respectively (Bayraktar et al., 2012).”
BackgroundInfluentialMetformin use improves the survival of diabetic combined small-cell lung cancer patients
Kong, F., Gao, F., Liu, H., Chen, L., Zheng, R., Yu, J., Li, X., Liu, G., & Jia, Y. (2015) · Tumor Biology · doi:10.1007/s13277-015-3549-1 · Cited by 33 · see citing works
Metformin and breast and gynecological cancer risk among women with diabetes
Soffer, D., Shi, J. M., Chung, J., Schottinger, J. E., Wallner, L. P., Chlebowski, R. T., Lentz, S. E., & Haque, R. (2015) · BMJ Open Diabetes Research & Care · doi:10.1136/bmjdrc-2014-000049 · Cited by 33 · see citing works
Xiao, Y.-T., Zhang, S., Hou, G., Zhang, X., Hao, X., & Zhang, J. (2013) · Tumor Biology · doi:10.1007/s13277-013-1270-5 · Cited by 32 · see citing works
“In addition, although there was no significant difference in 5-year distant metastasis, recurrence rate and overall survival among breast cancer patients (triple negative) with diabetes, the risk of distant metastasis was higher in the non-metformin group and the nondiabetic group than in the metformin group [6].”
BackgroundXue, L., Chen, F., Yue, F., Camacho, L., Kothapalli, S., Wei, G., Huang, S., Mo, Q., Ma, F., Li, Y., et al. (2020) · Breast Cancer Research and Treatment · doi:10.1007/s10549-020-05927-5 · Cited by 30 · see citing works
Prognosis of small cell lung cancer patients with diabetes treated with metformin
Xu, T., Liang, G., Yang, L., & Zhang, F. (2015) · Clinical & Translational Oncology · doi:10.1007/s12094-015-1311-1 · Cited by 30 · see citing works
Metformin: A candidate for the treatment of gynecological tumors based on drug repositioning
Irie, H., Banno, K., Yanokura, M., Iida, M., Adachi, M., Nakamura, K., Umene, K., Nogami, Y., Masuda, K., Kobayashi, Y., et al. (2016) · Oncology Letters · doi:10.3892/ol.2016.4075 · Cited by 29 · see citing works
Patorno, E., Garry, E. M., Patrick, A. R., Schneeweiß, S., Gillet, V. G., Zorina, O., Bartels, D. B., & Seeger, J. D. (2015) · Drug Safety · doi:10.1007/s40264-015-0280-1 · Cited by 29 · see citing works
“This scenario may confer increased mortality risk and could lead to bias in the setting of studies evaluating mortality risk in patients with pre-existing cancer with or without diabetes [7, 25, 26, 86].”
Wu, J. W., Boudreau, D. M., Park, Y., Simonds, N. I., & Freedman, A. N. (2014) · Expert Opinion on Drug Safety · doi:10.1517/14740338.2014.926887 · Cited by 27 · see citing works
“2 Current literature Seventeen articles on diabetes medications and cancer recurrence and/or cancer-specific mortality were identified, where almost all studies focused on metformin (Table 1) [32-48].”
BackgroundLee, K. N., Torres, M. A., Troeschel, A. N., He, J., Gogineni, K., & McCullough, L. E. (2020) · PLoS ONE · doi:10.1371/journal.pone.0232581 · Cited by 27 · see citing works
Can metformin improve ‘the tomorrow’ of patients treated for oesophageal cancer?
Voorde, L. V. D., Janssen, L., Larue, R. T. H. M., Houben, R. M. A., Buijsen, J., Sosef, M. N., Vanneste, B. G. L., Schraepen, M.-C., Berbée, M., & Lambin, P. (2015) · European Journal of Surgical Oncology · doi:10.1016/j.ejso.2015.05.012 · Cited by 26 · see citing works
Diabetes, Metformin, and Breast Cancer: Lilac Time?
Goodwin, P. J., Thompson, A. M., & Stambolic, V. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2012.42.3319 · Cited by 26 · see citing works
Unexploited Antineoplastic Effects of Commercially Available Anti-Diabetic Drugs
Papanagnou, P., Stivarou, T., & Tsironi, M. (2016) · Pharmaceuticals · doi:10.3390/ph9020024 · Cited by 25 · see citing works
“Still, metformin manages to lower the risk for the occurrence of distal metastases [138].”
BackgroundMetformin and survival in diabetic patients with breast cancer
El-Benhawy, S. A., & Elsheredy, H. (2014) · Journal of the Egyptian Public Health Association · doi:10.1097/01.epx.0000456620.00173.c0 · Cited by 25 · see citing works
Prognostic value of metformin for non-small cell lung cancer patients with diabetes
Xu, T., Li, D., He, Y., Zhang, F.-L., Qiao, M., & Chen, Y. (2018) · World Journal of Surgical Oncology · doi:10.1186/s12957-018-1362-1 · Cited by 25 · see citing works
“Moreover, some clinical and experimental studies confirmed that metformin had the anti-tumor effect and could prolong the survival time of patients who had been diagnosed of diabetes mellitus accompanied by hepatocellular carcinoma or prostate cancer in a long term [10, 12, 13].”
BackgroundObesity–cancer axis crosstalk: Molecular insights and therapeutic approaches
Rakib, A., Mamun, M. A. A., Mandal, M., Sinha, P., & Singh, U. P. (2025) · Acta Pharmaceutica Sinica B · doi:10.1016/j.apsb.2025.04.029 · Cited by 24 · see citing works
“However, metformin shows limited or no potential benefits in randomized clinical trials when used as an adjuvant therapy 193,194 .”
Mitochondrial determinants of chemoresistance
Bokil, A. A., & Sancho, P. (2019) · Cancer Drug Resistance · doi:10.20517/cdr.2019.46 · Cited by 23 · see citing works
Yoshida, J., Ishikawa, T., Endo, Y., Matsumura, S., Ota, T., Mizushima, K., Hirai, Y., Oka, K., Okayama, T., Sakamoto, N., et al. (2020) · Oncology Reports · doi:10.3892/or.2020.7595 · Cited by 26 · see citing works
- Authors
- Bayraktar, S., Hernadez‐Aya, L. F., Lei, X., Meric‐Bernstam, F., Litton, J. K., Hsu, L., Hortobagyi, G. N., & Gonzalez‐Angulo, A. M.
- Affiliations
- The University of Texas MD Anderson Cancer Center (US)
- Venue
- Cancer
- Publisher
- Wiley
- Published
- 2011-07-28
- Volume
- 118
- Issue
- 5
- Pages
- 1202-1211
- ISSN
- 0008-543X (ISSN-L)
- 1097-0142
- PMC
- PMC3207034
- OpenAlex
- W2078767636
- Cited by
- 176
- References
- 57
- Citations by year
- 2026: 2 · 2025: 5 · 2024: 2 · 2023: 4 · 2022: 11 · 2021: 15 · 2020: 19 · 2019: 8 · 2018: 5 · 2017: 15 · 2016: 10 · 2015: 23 · 2014: 18 · 2013: 20 · 2012: 18
- FWCI
- 7.39
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Cancer (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (5k23ca121994-03)
- National Cancer Institute (P50CA116199, 1K23CA121994-01), K23-CA121994)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Breast Cancer Treatment Studies
- Health Sciences › Medicine › Oncology › Cancer Risks and Factors
- Keywords
- metformin, diabetes mellitus, adjuvant chemotherapy, distant metastasis-free survival, recurrence-free survival, overall survival, survival outcomes
- MeSH terms
- Adult, Aged, Aged, 80 and over, Breast Neoplasms, Carcinoma, Diabetes Mellitus, Type 2, Female, Humans, Hypoglycemic Agents, Metformin, Middle Aged, Retrospective Studies, Survival Analysis, Case-Control Studies, Treatment Outcome, Receptors, Cytoplasmic and Nuclear, Young Adult
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 ›
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