Reduced risk of lung cancer with metformin therapy in diabetic patients: a systematic review and meta-analysis
Abstract
Emerging evidence from epidemiologic studies and basic science suggests an inverse association between metformin use and cancer risk in diabetic patients. However, the association with lung cancer is not consistent. We summarized the evidence currently available (2009-2013) and explored sources of heterogeneity. Metformin therapy was associated with significantly lower risks of cancers of the lung (4 studies; pooled relative risk = 0.71, 95% confidence interval (CI): 0.55, 0.95; P = 0.02) and respiratory system (6 studies; pooled relative risk = 0.85, 95% CI: 0.75, 0.96; P = 0.01). There was evidence of moderate heterogeneity (I(2) > 50%). The major sources of heterogeneity were smoking adjustment status and cancer site. The relative risk from studies that adjusted for smoking was 1.16-fold (95% CI: 1.00, 1.35) closer to the null than that from studies not adjusting for smoking. The relative risk of respiratory cancer was 1.23-fold (95% CI: 1.02, 1.49) closer to the null than that for lung cancer. In conclusion, metformin use appears to be associated with lower risks of lung and respiratory cancer in diabetic patients. However, caution regarding overestimation is needed, since adjustment for smoking attenuates the association.
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).”
This finding has subsequently been confirmed in several other studies.
“this finding has subsequently been confirmed in several other studies(7–10).”
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
Jemal, A., Bray, F., Ferlay, J., Ward, E., & Forman, D. (2011) · CA A Cancer Journal for Clinicians · doi:10.3322/caac.20107 · Cited by 54,708 · 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
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 · see citing works
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 · see citing works
Quantitative Synthesis in Systematic Reviews
Lau, J., Ioannidis, J. P. A., & Schmid, C. H. (1997) · Annals of Internal Medicine · doi:10.7326/0003-4819-127-9-199711010-00008 · Cited by 2,517 · see citing works
Chen, Y., Ebenstein, A. Y., Greenstone, M., & Li, H. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1300018110 · Cited by 1,819 · see citing works
Raaschou‐Nielsen, O., Andersen, Z. J., Beelen, R. M. J., Samoli, E., Stafoggia, M., Weinmayr, G., Hoffmann, B. H., Fischer, P. H., Nieuwenhuijsen, M. J., Brunekreef, B., et al. (2013) · The Lancet Oncology · doi:10.1016/s1470-2045(13)70279-1 · Cited by 1,584 · see citing works
Lee, I.-M., Cook, N. R., Gaziano, J. M., Gordon, D., Ridker, P. M., Manson, J. E., Hennekens, C. H., & Buring, J. E. (2005) · JAMA · doi:10.1001/jama.294.1.56 · Cited by 1,137 · see citing works
New Users of Metformin Are at Low Risk of Incident Cancer
Libby, G., Donnelly, L. A., Donnan, P. T., Alessi, D. R., Morris, A. D., & Evans, J. M. M. (2009) · Diabetes Care · doi:10.2337/dc08-2175 · Cited by 996 · see citing works
Metformin and Cancer Risk in Diabetic Patients: A Systematic Review and Meta-analysis
DeCensi, A., Puntoni, M., Goodwin, P., Cazzaniga, M., Gennari, A., Bonanni, B., & Gandini, S. (2010) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-10-0157 · Cited by 918 · see citing works
Goodman, G. E., Thornquist, M. D., Balmes, J. R., Cullen, M. R., Meyskens, F. L., Omenn, G. S., VALANIS, B. G., & Williams, J. H. (2004) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djh320 · Cited by 430 · see citing works
Metformin Prevents Tobacco Carcinogen–Induced Lung Tumorigenesis
Memmott, R. M., Mercado, J. R., Maier, C. R., Kawabata, S., Fox, S. D., & Dennis, P. A. (2010) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-10-0055 · Cited by 407 · see citing works
Reduced Risk of Colorectal Cancer With Metformin Therapy in Patients With Type 2 Diabetes
Zhang, Z.-J., Zheng, Z., Kan, H., Song, Y., Cui, W., Zhao, G., & Kip, K. E. (2011) · Diabetes Care · doi:10.2337/dc11-0512 · Cited by 291 · see citing works
Self-citationStorozhuk, Y., Hopmans, S., Sanli, T., Barron, C. C., Tsiani, E., Cutz, J.-C., Pond, G. R., Wright, J. R., Singh, G., & Tsakiridis, T. K. (2013) · British Journal of Cancer · doi:10.1038/bjc.2013.187 · Cited by 272 · see citing works
Zhang, Z.-J., Zheng, Z., Shi, R., Su, Q., Jiang, Q., & Kip, K. E. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-1267 · Cited by 241 · see citing works
Self-citationLower Risk of Cancer in Patients on Metformin in Comparison With Those on Sulfonylurea Derivatives
Ruiter, R., Visser, L. E., van Herk‐Sukel, M. P. P., Coebergh, J. W. W., Haak, H. R., Geelhoed-Duijvestijn, P. H. L. M., Straus, S. M. J. M., Herings, R. M. C., & Stricker, B. H. C. (2011) · Diabetes Care · doi:10.2337/dc11-0857 · Cited by 232 · see citing works
Currie, C. J., Poole, C. D., Evans, M., Peters, J. R., & Morgan, C. L. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-3042 · Cited by 203 · see citing works
A genome-wide methylation study on obesity
Xu, X., Su, S., Barnes, V. A., Miguel, C. D., Pollock, J. S., Ownby, D. R., Shi, H., Zhu, H., Snieder, H., & Wang, X. (2013) · Epigenetics · doi:10.4161/epi.24506 · Cited by 191 · see citing works
Metformin attenuates the stimulatory effect of a high-energy diet on in vivo LLC1 carcinoma growth
Algire, C., Zakikhani, M., Blouin, M.-J., Shuai, J. H., & Pollak, M. (2008) · Endocrine Related Cancer · doi:10.1677/erc-08-0038 · Cited by 185 · see citing works
Cohort Study of Pioglitazone and Cancer Incidence in Patients With Diabetes
Ferrara, A. M., Lewis, J. D., Quesenberry, C. P., Peng, T., Strom, B. L., Eeden, S. K. V. D., Ehrlich, S. F., & Habel, L. A. (2011) · Diabetes Care · doi:10.2337/dc10-1067 · Cited by 182 · see citing works
The Influence of Type 2 Diabetes and Glucose-Lowering Therapies on Cancer Risk in the Taiwanese
Hsieh, M.-C., Lee, T.-C., Cheng, S.-M., Tu, S., Yen, M., & Tseng, C. (2012) · Experimental Diabetes Research · doi:10.1155/2012/413782 · Cited by 163 · see citing works
Zhang, Z., & Li, S. (2014) · Diabetes Obesity and Metabolism · doi:10.1111/dom.12267 · Cited by 149 · see citing works
Self-citationOral Insulin Secretagogues, Insulin, and Cancer Risk in Type 2 Diabetes Mellitus
Chang, C., Lin, J., Wu, L., Lai, M., & Chuang, L. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-1162 · Cited by 129 · see citing works
Metformin induces apoptosis of lung cancer cells through activating JNK/p38 MAPK pathway and GADD153
WU, N., GU, C., GU, H., Hu, H., Han, Y., & Li, Q. (2011) · Neoplasma · doi:10.4149/neo_2011_06_482 · Cited by 113 · see citing works
The effect of metformin and thiazolidinedione use on lung cancer in diabetics
Mazzone, P. J., Rai, H., Beukemann, M., Meng, X., Jain, A., & Sasidhar, M. (2012) · BMC Cancer · doi:10.1186/1471-2407-12-410 · Cited by 112 · see citing works
The Use of Metformin and the Incidence of Lung Cancer in Patients With Type 2 Diabetes
Smiechowski, B., Azoulay, L., Yin, H., Pollak, M., & Suissa, S. (2012) · Diabetes Care · doi:10.2337/dc12-0740 · Cited by 86 · see citing works
Lung Cancer Chemoprevention: A Randomized, Double-Blind Trial in Linxian, China
Kamangar, F., Qiao, Y., Yu, B., Sun, X., Abnet, C. C., Fan, J., Mark, S. D., Zhao, P., Dawsey, S. M., & Taylor, P. R. (2006) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-06-0316 · Cited by 60 · see citing works
Kelly, K. L., Kittelson, J. K., Franklin, W. A., Kennedy, T. C., Klein, C. E., Keith, R. L., Dempsey, E. C., Lewis, M. T., Jackson, M. K., Hirsch, F. R., et al. (2009) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-08-0136 · Cited by 31 · see citing works
Li, C., Zhao, G., Okoro, C. A., Wen, X., Ford, E. S., & Balluz, L. S. (2013) · Diabetes Care · doi:10.2337/dc12-1432 · Cited by 28 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
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
Metformin attenuates lung fibrosis development via NOX4 suppression
Sato, N., Takasaka, N., Yoshida, M., Tsubouchi, K., Minagawa, S., Araya, J., Saito, N., Fujita, Y., Kurita, Y., Kobayashi, K., et al. (2016) · Respiratory Research · doi:10.1186/s12931-016-0420-x · Cited by 229 · see citing works
Targeting Cancer Metabolism: Dietary and Pharmacologic Interventions
Vernieri, C., Casola, S., Foiani, M., Pietrantonio, F., de Braud, F., & Longo, V. (2016) · Cancer Discovery · doi:10.1158/2159-8290.cd-16-0615 · Cited by 202 · see citing works
Metformin-treated cancer cells modulate macrophage polarization through AMPK-NF-κB signaling
Chiang, C., Chao, T., Su, Y., Hsu, C., Chien, C., Chiu, K., Shiah, S., Lee, C.-H., Liu, S.-Y., & Shieh, Y. (2017) · Oncotarget · doi:10.18632/oncotarget.14982 · Cited by 188 · see citing works
PolyMetformin combines carrier and anticancer activities for in vivo siRNA delivery
Zhao, Y. D., Wang, W., Guo, S., Wang, Y., Miao, L., Xiong, Y., & Huang, L. (2016) · Nature Communications · doi:10.1038/ncomms11822 · Cited by 171 · see citing works
Ding, L., Liang, G., Yao, Z., Zhang, J., Liu, R., Chen, H., Zhou, Y., Wu, H., Yang, B., & He, Q. (2015) · Oncotarget · doi:10.18632/oncotarget.5541 · Cited by 165 · 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
Kowall, B., Stang, A., Rathmann, W., & Kostev, K. (2015) · Pharmacoepidemiology and Drug Safety · doi:10.1002/pds.3823 · Cited by 98 · see citing works
Skinner, H. D., Hu, C., Tsakiridis, T. K., Santana-Dávila, R., Lü, B., Erasmus, J. J., Doemer, A., Videtic, G. M. M., Coster, J. R., Yang, A. X., et al. (2021) · JAMA Oncology · doi:10.1001/jamaoncol.2021.2318 · Cited by 99 · see citing works
Chemotherapy targeting cancer stem cells.
Liu, H., Lv, L. L., & Yang, K. (2015) · PubMed Central · Cited by 94 · see citing works
O’Brien, A. J., Villani, L. A., Broadfield, L. A., Houde, V. P., Galić, S., Blandino, G., Kemp, B. E., Tsakiridis, T. K., Muti, P. C., & Steinberg, G. R. (2015) · Biochemical Journal · doi:10.1042/bj20150122 · Cited by 89 · 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
Liu, X., Jiang, J., Yu, C., Wang, Y., Sun, Y., Tang, J., Chen, T., Bi, Y., Liu, Y., & Zhang, Z. (2019) · Cancer Epidemiology · doi:10.1016/j.canep.2019.05.011 · Cited by 87 · see citing works
Self-citationDiabetes induces fibrotic changes in the lung through the activation of TGF-β signaling pathways
Talakatta, G., Sarikhani, M., Muhamed, J., Dhanya, K., Somashekar, B. S., Mahesh, P. A., Sundaresan, N. R., & Veeranna, R. P. (2018) · Scientific Reports · doi:10.1038/s41598-018-30449-y · Cited by 83 · see citing works
Role of Metformin on Osteoblast Differentiation in Type 2 Diabetes
Jiating, L., Buyun, J., & Zhang, Y. (2019) · BioMed Research International · doi:10.1155/2019/9203934 · Cited by 76 · see citing works
Zhou, X., Xue, W., Ding, X., Li, L., Dou, M., Zhang, W., Lv, Z., Fan, Z., Zhao, J., & Wang, L. (2017) · Oncotarget · doi:10.18632/oncotarget.16973 · Cited by 75 · see citing works
Metformin in Lung Cancer: Review of in Vitro and in Vivo Animal Studies
Yousef, M., & Tsiani, E. (2017) · Cancers · doi:10.3390/cancers9050045 · Cited by 71 · see citing works
Rising Mortality Rate of Cervical Cancer in Younger Women in Urban China
Wei, M., Zhou, W., Bi, Y., Wang, H., Liu, Y., & Zhang, Z.-J. (2018) · Journal of General Internal Medicine · doi:10.1007/s11606-018-4732-z · Cited by 69 · see citing works
Self-citationGuo, L., Cui, J., Wang, H., Medina, R., Zhang, S., Zhang, X., Zhuang, Z., & Lin, Y. (2020) · Molecular Therapy — Oncolytics · doi:10.1016/j.omto.2020.11.004 · Cited by 63 · see citing works
Murff, H. J., Roumie, C. L., Greevy, R. A., Hackstadt, A. J., McGowan, L. D., Hung, A. M., Grijalva, C. G., & Griffin, M. R. (2018) · Cancer Causes & Control · doi:10.1007/s10552-018-1058-4 · Cited by 63 · see citing works
Metformin: A Dual-Role Player in Cancer Treatment and Prevention
Galal, M. A., Al-Rimawi, M., Hajeer, A., Dahman, H., Alouch, S. S., & Aljada, A. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25074083 · Cited by 68 · see citing works
Metformin Use and Lung Cancer Risk in Diabetic Patients: A Systematic Review and Meta-Analysis
Long, Y., Liu, M., Huang, Y., Wu, K., Huang, X., Zhao, Y., He, W., & Zhang, R. (2019) · Disease Markers · doi:10.1155/2019/6230162 · Cited by 55 · see citing works
Metformin and lung cancer risk in patients with type 2 diabetes mellitus
Tseng, C. (2017) · Oncotarget · doi:10.18632/oncotarget.17066 · Cited by 53 · see citing works
Zhang, J., Zhang, Q., Li, Z.-Q., Zhou, J., & Du, J. (2019) · PubMed Central · Cited by 52 · see citing works
Self-citationArrieta, O. G., Varela‐Santoyo, E., Soto‐Pérez‐de‐Celis, E., Sánchez-Reyes, R., la Torre-Vallejo, M. D., Muñiz‐Hernández, S., & Cardona, A. F. (2016) · BMC Cancer · doi:10.1186/s12885-016-2658-6 · Cited by 51 · see citing works
Zhang, Z.-J., Yuan, J., Bi, Y., Wang, C., & Liu, Y. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2019.01.036 · Cited by 47 · see citing works
Self-citationCui, H., Wang, Y., Yang, S., He, G., Jiang, Z., Gang, X., & Wang, G. (2022) · Pharmacological Research · doi:10.1016/j.phrs.2022.106094 · Cited by 46 · see citing works
Role of p53 Family Proteins in Metformin Anti-Cancer Activities
Yi, Y., Zhang, W., Yi, J., & Xiao, Z. J. (2019) · Journal of Cancer · doi:10.7150/jca.30659 · Cited by 46 · see citing works
Wang, L., Yu, C., Liu, Y., Wang, J., Li, C., Wang, Q., Wang, P., Wu, S., & Zhang, Z. (2016) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph13111052 · Cited by 45 · see citing works
Self-citationMetformin for non-small cell lung cancer patients: Opportunities and pitfalls
Lévy, A., & Doyen, J. (2018) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2018.03.001 · Cited by 46 · see citing works
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 43 · see citing works
Subbiah, V., Coleman, N., Piha-Paul, S. A., Tsimberidou, A. M., Jankú, F., Rodon, J. A., Pant, S., Dumbrava, E. E. I., Fu, S., Hong, D. S., et al. (2023) · Cancer Research Communications · doi:10.1158/2767-9764.crc-22-0260 · Cited by 41 · see citing works
Liu, X., Yu, C., Wang, Y., Bi, Y., Liu, Y., & Zhang, Z. (2019) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph16010158 · Cited by 41 · see citing works
Self-citationMetformin with Everolimus and Octreotide in Pancreatic Neuroendocrine Tumor Patients with Diabetes
Pusceddu, S., Buzzoni, R., Vernieri, C., Concas, L., Marceglia, S. R. F., Giacomelli, L., Milione, M., Leuzzi, L., Femia, D., Formisano, B., et al. (2016) · Future Oncology · doi:10.2217/fon-2015-0077 · Cited by 38 · see citing works
Dickerman, B. A., García‐Albéniz, X., Logan, R. W., Denaxas, S., & Hernán, M. Á. (2023) · Epidemiology · doi:10.1097/ede.0000000000001626 · Cited by 34 · see citing works
The association between human papillomavirus infection and female lung cancer
Lin, F. C., Huang, J., Tsai, S. C., Nfor, O. N., Chou, M., Wu, M., Lee, C., Jan, C., & Liaw, Y. (2016) · Medicine · doi:10.1097/md.0000000000003856 · Cited by 33 · see citing works
He, Y., Tai, S., Deng, M., Fan, Z., Ping, F., He, L., Zhang, C., Huang, Y., Cheng, B., & Xia, J. (2019) · Cancer Medicine · doi:10.1002/cam4.2206 · Cited by 32 · see citing works
Wang, Y., Liu, X., Yan, P., Bi, Y., Liu, Y., & Zhang, Z.-J. (2019) · Diabetes & Metabolism · doi:10.1016/j.diabet.2019.04.006 · Cited by 33 · see citing works
Self-citationPharmacological Modulation of Lung Carcinogenesis in Smokers: Preclinical and Clinical Evidence
Flora, S. D., Ganchev, G., Iltcheva, M., Maestra, S. L., Micale, R. T., Steele, V. E., & Balansky, R. M. (2015) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2015.11.003 · Cited by 33 · see citing works
Metformin and pancreatic cancer survival: Real effect or immortal time bias?
Wei, M., Liu, Y., Bi, Y., & Zhang, Z. (2019) · International Journal of Cancer · doi:10.1002/ijc.32254 · Cited by 33 · see citing works
Self-citationDu, L., Wang, M., Kang, Y., Li, B., Guo, M., Cheng, Z., & Bi, C. (2017) · Oncotarget · doi:10.18632/oncotarget.14688 · Cited by 32 · see citing works
Kok, V. C., Chen, Y., Chien, C.-H., Horng, J., & Tsai, J. (2015) · Therapeutics and Clinical Risk Management · doi:10.2147/tcrm.s91513 · Cited by 32 · see citing works
Fixed-Dose Combinations of Pioglitazone and Metformin for Lung Cancer Prevention
Seabloom, D. E., Galbraith, A. R., Haynes, A. M., Antonides, J. D., Wuertz, B. R. K., Miller, W. A., Miller, K. A., Steele, V. E., Miller, M. S., Clapper, M. L., et al. (2017) · Cancer Prevention Research · doi:10.1158/1940-6207.capr-16-0232 · Cited by 30 · see citing works
A Phase Ib Clinical Trial of Metformin and Chloroquine in Patients with IDH1-Mutated Solid Tumors
Khurshed, M., Molenaar, R. J., Linde, M. E. V., Mathôt, R. A. A., Struys, E. A., van Wezel, T., Noorden, C. J. F. V., Klümpen, H., Bovée, J. V. M. G., & Wilmink, J. W. (2021) · Cancers · doi:10.3390/cancers13102474 · Cited by 30 · see citing works
Metformin enhances radiation response of ECa109 cells through activation of ATM and AMPK
Feng, T., Li, L., Ling, S., Fan, N., Fang, M., Zhang, H., Fang, X. H., Lan, W., Hou, Z., Meng, Q.-C., et al. (2014) · Biomedicine & Pharmacotherapy · doi:10.1016/j.biopha.2014.11.021 · Cited by 30 · see citing works
Advances in metformin‑based metabolic therapy for non‑small cell lung cancer (Review)
Chen, N., Zhou, Y.-S., Wang, L.-C., & Huang, J. (2022) · Oncology Reports · doi:10.3892/or.2022.8266 · Cited by 29 · see citing works
Translational geroscience: From invertebrate models to companion animal and human interventions
Lee, M. B., & Kaeberlein, M. R. (2018) · Translational Medicine of Aging · doi:10.1016/j.tma.2018.08.002 · Cited by 27 · see citing works
Assessing the Current State of Lung Cancer Chemoprevention: A Comprehensive Overview
Ashraf-Uz-Zaman, M., Bhalerao, A., Mikelis, C. M., Cucullo, L., & German, N. (2020) · Cancers · doi:10.3390/cancers12051265 · Cited by 27 · see citing works
Rising Mortality Rate of Cervical Cancer in Younger Women in Urban China
Chen, T., Wei, M., Liu, Y., Wang, H., Zhou, W., Bi, Y., & Zhang, Z. (2019) · Journal of General Internal Medicine · doi:10.1007/s11606-019-05174-5 · Cited by 25 · see citing works
Self-citationMetformin use and lung cancer survival: a population-based study in Norway
Brandão, S. L. B., Støer, N. C., Weiderpass, E., Damhuis, R. A. M., Johannesen, T. B., Botteri, E., & Strand, T. (2020) · British Journal of Cancer · doi:10.1038/s41416-020-01186-9 · Cited by 24 · see citing works
Luo, X., Chen, X., Wang, L., Yang, B., & Cai, S. (2021) · Frontiers in Pharmacology · doi:10.3389/fphar.2021.639016 · Cited by 24 · see citing works
Zhang, Q., Kong, J., Dong, S., Xu, W., & Sun, W. (2017) · Cancer Cell International · doi:10.1186/s12935-017-0418-6 · Cited by 23 · see citing works
Self-citationMoradinazar, 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
Sugiyama, Y., Shudo, T., Hosokawa, S., Watanabe, A., Nakano, M., & Kakizuka, A. (2019) · Genes to Cells · doi:10.1111/gtc.12712 · Cited by 21 · see citing works
Shi, R., Mei, Z., Zhang, Z., & Zhu, Z. (2019) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2019.06.027 · Cited by 21 · see citing works
Self-citationThe Diverse Roles of Adiponectin in Non-Small-Cell Lung Cancer: Current Data and Future Perspectives
Boura, P., Loukides, S., Grapsa, D., Achimastos, A. D., & Syrigos, K. (2015) · Future Oncology · doi:10.2217/fon.15.96 · Cited by 20 · see citing works
Zhang, J., Wu, J., He, Q., Liang, W., & He, J. (2018) · Translational Lung Cancer Research · doi:10.21037/tlcr.2018.03.14 · Cited by 20 · see citing works
Liu, X., Bi, Y., Wang, H., Meng, R., Zhou, W., Zhang, G., Yu, C., & Zhang, Z.-J. (2018) · Public Health · doi:10.1016/j.puhe.2018.08.007 · Cited by 18 · see citing works
Self-citationEvaluation of the pharmacokinetics of metformin and acarbose in the common marmoset
Fernández, E., Ross, C. N., Liang, H., Javors, M. A., Tardif, S. D., & Salmon, A. B. (2019) · Pathobiology of Aging & Age-related Diseases · doi:10.1080/20010001.2019.1657756 · Cited by 18 · see citing works
A phase Ib study of everolimus combined with metformin for patients with advanced cancer
Molenaar, R. J., van de Venne, T., Weterman, M. J., Mathôt, R. A. A., Klümpen, H., Richel, D. J., & Wilmink, J. W. (2017) · Investigational New Drugs · doi:10.1007/s10637-017-0478-4 · Cited by 17 · see citing works
Yang, H., Peng, Y., Ni, H., Li, Y., Shi, Y., Ding, W., & Fan, J. (2015) · PLoS ONE · doi:10.1371/journal.pone.0130953 · Cited by 16 · see citing works
Zhang, J., Hang, C., Jiang, T., Yi, S., Shao, W., Li, W., & Lin, D. (2020) · Frontiers in Oncology · doi:10.3389/fonc.2020.570516 · Cited by 16 · see citing works
Obesity-specific improvement of lung cancer outcomes and immunotherapy efficacy with metformin
Smith, R. J., Zollo, R. A., Kalvapudi, S., Vedire, Y., Pachimatla, A. G., Petrucci, C. M., Shaller, G., Washington, D., Vethanayagam, R. R., Sass, S. N., et al. (2024) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/djae295 · Cited by 15 · see citing works
Synergistic effect of metformin and EGFR-TKI in the treatment of non-small cell lung cancer
Wang, H., Yang, X. L., Sun, Y., Li, Y., Dong, Y., Shan, D., & Yu, Z. (2020) · Translational Cancer Research · doi:10.21037/tcr.2019.11.09 · Cited by 11 · see citing works
Yang, T., Wang, H., Zhou, Q., Huang, W., Zhang, J., Yu, Y., & Sun, T. (2023) · ACS Applied Nano Materials · doi:10.1021/acsanm.3c00140 · Cited by 12 · see citing works
Metformin and thyroid carcinoma incidence and prognosis: A systematic review and meta-analysis
Wang, Z., Luo, J., Zhang, Y., Xun, P., & Chen, Z. (2022) · PLoS ONE · doi:10.1371/journal.pone.0271038 · Cited by 12 · see citing works
Singh, S. V., Carlo, F. D., Ibrahim, M. A., Penfornis, P., Mouton, A. J., Tripathi, S., Agarwal, A. K., Eastham, L. L., Pasco, D. S., Balachandran, P., et al. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24097741 · Cited by 11 · see citing works
Zhang, H., Yang, Y. S., Lee, S., Park, S., Nam, C. M., & Jee, S. H. (2022) · International Journal of Colorectal Disease · doi:10.1007/s00384-022-04212-9 · Cited by 10 · see citing works
Will metformin use lead to a decreased risk of thyroid cancer? A systematic review and meta-analyses
Li, H., Chen, Y., Hu, L., Yang, W., Gao, Z., Liu, M., Tao, H., & Li, J. (2023) · European Journal of Medical Research · doi:10.1186/s40001-023-01287-0 · Cited by 10 · see citing works
Wang, Y., Sun, Y., Tang, J., Zhou, W., Liu, X., Bi, Y., & Zhang, Z.-J. (2018) · Annals of Epidemiology · doi:10.1016/j.annepidem.2018.11.010 · Cited by 10 · see citing works
Self-citationMetformina: más allá del control glucémico
de Colombia, U. N., Morantes-Caballero, J. A., Londoño-Zapata, G. A., de Colombia, U. N., Rivera, M. R., de Colombia, U. N., Pinilla-Roa, A. E., & de Colombia, U. N. (2017) · Revista Médicas UIS · doi:10.18273/revmed.v30n1-2017005 · Cited by 9 · see citing works
Yue, N., Jia, F., Du, X., & Mei, Z. (2020) · International Journal of Surgery · doi:10.1016/j.ijsu.2020.02.041 · Cited by 7 · see citing works
Bosco, C. (2015) · ecancermedicalscience · doi:10.3332/ecancer.2015.555 · Cited by 8 · see citing works
Wang, Z., Li, J., Wang, L., Liu, Y., Wang, W., Chen, J., Liang, H., Chen, Y. Q., & Zhu, S. (2024) · Cellular & Molecular Biology Letters · doi:10.1186/s11658-024-00535-3 · Cited by 7 · see citing works
Zhang, Z.-J. (2019) · Journal of General Internal Medicine · doi:10.1007/s11606-019-04982-z · Cited by 7 · see citing works
Self-citationWang, Y., Hu, J., Sun, Y. L., Song, B., Zhang, Y., Lu, Y., & Ma, H. (2022) · Evidence-based Complementary and Alternative Medicine · doi:10.1155/2022/5983959 · Cited by 7 · see citing works
RetractedCancer Prevention Strategies for Women
Tergas, A. I., & Wright, J. D. (2019) · Obstetrics and Gynecology · doi:10.1097/aog.0000000000003304 · Cited by 7 · see citing works
Wei, M., Liu, Y., Wang, C., Yu, C., Li, D., Zhou, W., & Zhang, Z.-J. (2016) · Acta Diabetologica · doi:10.1007/s00592-016-0948-8 · Cited by 7 · see citing works
Self-citationWei, M., Liu, Y., Wang, C., Yu, C., Li, D., Zhou, W., & Zhang, Z.-J. (2016) · Acta Diabetologica · doi:10.1007/s00592-016-0933-2 · Cited by 7 · see citing works
Self-citationThe Interplay Between Cardiovascular Disease and Lung Cancer
Katić, L., Choi, J. W., Saravia, S. D., Silverman, A., Nagourney, A., Torelli, V. A., Gupta, S., Glavan, M., Gulati, A., Khurana, S., et al. (2024) · Cureus · doi:10.7759/cureus.62953 · Cited by 6 · see citing works
Wang, Y., Fu, T., Liu, Y., Yang, G., Yu, C., & Zhang, Z.-J. (2020) · Current Pharmaceutical Design · doi:10.2174/1381612826666200218095310 · Cited by 6 · see citing works
Self-citationWang, Y., Liu, X., Yan, P., Bi, Y., Liu, Y., & Zhang, Z.-J. (2019) · Current Pharmaceutical Design · doi:10.2174/1381612825666190716113126 · Cited by 6 · see citing works
Self-citationSchmedt, N., Azoulay, L., & Hense, S. (2014) · American Journal of Epidemiology · doi:10.1093/aje/kwu311 · Cited by 6 · see citing works
Phenformin Induces Caspase-dependent Apoptosis of FaDu Head and Neck Squamous Cell Carcinoma Cells
Seo, Y., Kim, T. H., Lim, H., Oh, J.-S., You, J., Lee, G., Yu, S., Kim, D. K., KIM, H.-J., KIM, C. S., et al. (2019) · Anticancer Research · doi:10.21873/anticanres.13496 · Cited by 5 · see citing works
Hense, H. W., & Geier, A. (2014) · American Journal of Epidemiology · doi:10.1093/aje/kwu296 · Cited by 5 · see citing works
Zhang, Z.-J. (2014) · American Journal of Epidemiology · doi:10.1093/aje/kwu297 · Cited by 5 · see citing works
Self-citationA doxycycline-loaded microfiber of poly-metformin/PCL for eradicating melanoma stem cells
Zarei, B., Akrami, M., Rezaei, N., Mahdavi, M. R., Kamankesh, M., Haririan, I., Asadi, M., & Nigjeh, M. N. (2024) · International Journal of Pharmaceutics · doi:10.1016/j.ijpharm.2024.124358 · Cited by 4 · see citing works
Jonušas, J., Patašius, A., Drevinskaitė, M., Ladukas, A., Linkevičiūtė-Ulinskienė, D., Zabulienė, L., & Smailytė, G. (2024) · Medicina · doi:10.3390/medicina60081275 · Cited by 3 · see citing works
Effects of Hypoglycemic Agents on Pulmonary Diseases: A Comprehensive Narrative Review
Yang, Y., Wang, K., & CHEN, S. (2025) · Journal of Inflammation Research · doi:10.2147/jir.s556790 · Cited by 4 · see citing works
Associations of aspirin, statins and metformin with lung cancer risk and related mortality
Frille, A., Costantini, A., & Sreter, K. B. (2021) · Breathe · doi:10.1183/20734735.0325-2020 · Cited by 3 · see citing works
Zhang, Z.-J. (2014) · American Journal of Epidemiology · doi:10.1093/aje/kwu314 · Cited by 3 · see citing works
Self-citationLu, Z., Bi, J., Zheng, C., Cui, L., Xia, H., Wan, X., & Chen, Y. H. (2026) · Molecular Therapy · doi:10.1016/j.ymthe.2026.01.032 · Cited by 2 · see citing works
Gheorghiu, A., Brunborg, C., Johannesen, T. B., Helseth, E., Zwart, J., & Wiedmann, M. K. H. (2024) · Frontiers in Oncology · doi:10.3389/fonc.2024.1428142 · Cited by 2 · see citing works
Insulin, Other Hypoglycemic Drugs, and Glucagon
Escaño, A. K. (2015) · Side effects of drugs annual · doi:10.1016/bs.seda.2015.05.006 · Cited by 2 · see citing works
Emerging Link between Diabetes and Cancer
Noto, H., Goto, A., Tsujimoto, T., & Noda, M. (2015) · Journal of General and Family Medicine · doi:10.14442/jgfm.16.3_170 · Cited by 2 · see citing works
Boura, P., Grapsa, D., Loukides, S., Angelidou, M., Tsakanika, K., Syrigos, N. K., & Gkiozos, I. (2017) · Lung Cancer Management · doi:10.2217/lmt-2016-0018 · Cited by 2 · see citing works
Metformin – the old drug with new therapeutic possibilities
Oleksa, P., Jasiński, K., Żuraw, D., Sobczyk, M., Żybowska, M., Rzewuska, A., Haczkur-Pawłowska, K., & Więsyk, P. J. (2024) · Polish Journal of Public Health · doi:10.12923/2083-4829/2024-0011 · Cited by 1 · see citing works
Zhang, X., Liu, J., Zhao, Z., Jiang, J., & Geng, G. (2025) · PLoS ONE · doi:10.1371/journal.pone.0329277 · Cited by 1 · see citing works
Hiroki, S., Fukasawa, T., Honda, M., & Kawakami, K. (2026) · Pharmacoepidemiology and Drug Safety · doi:10.1002/pds.70429 · Cited by 1 · see citing works
- Authors
- Zhang, Z.-J., Bi, Y., Li, S., Zhang, Q., Zhao, G., Guo, Y., & Song, Q.
- Affiliations
- Wuhan University (CN)
- Wuhan Donghu University (CN)
- Corresponding author
- Zhang, Zhi-Jiang
- Venue
- American Journal of Epidemiology
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-06-10
- Volume
- 180
- Issue
- 1
- Pages
- 11-14
- ISSN
- 0002-9262 (ISSN-L)
- 1476-6256
- OpenAlex
- W3145105062
- Cited by
- 120
- References
- 28
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 14 · 2023: 9 · 2022: 6 · 2021: 7 · 2020: 8 · 2019: 19 · 2018: 11 · 2017: 14 · 2016: 9 · 2015: 12 · 2014: 5
- FWCI
- 1.26
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Epidemiology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer, Hypoxia, and Metabolism
- Health Sciences › Medicine › Oncology › Cancer Risks and Factors
- Keywords
- metformin, lung cancer, respiratory cancer, diabetes mellitus, cancer risk, smoking adjustment, heterogeneity
- MeSH terms
- Diabetes Mellitus, Type 2, Humans, Hypoglycemic Agents, Lung Neoplasms, Metformin, Risk, Risk Factors, Smoking
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
