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Metformin Associated With Lower Cancer Mortality in Type 2 Diabetes
Open accessAbstract
OBJECTIVE: Several studies have suggested an association between specific diabetes treatment and cancer mortality. We studied the association between metformin use and cancer mortality in a prospectively followed cohort. RESEARCH DESIGN AND METHODS: In 1998 and 1999, 1,353 patients with type 2 diabetes were enrolled in the Zwolle Outpatient Diabetes project Integrating Available Care (ZODIAC) study in the Netherlands. Vital status was assessed in January 2009. Cancer mortality rate was evaluated using standardized mortality ratios (SMRs), and the association between metformin use and cancer mortality was evaluated with a Cox proportional hazards model, taking possible confounders into account. RESULTS: Median follow-up time was 9.6 years, average age at baseline was 68 years, and average A1C was 7.5%. Of the patients, 570 died, of which 122 died of malignancies. The SMR for cancer mortality was 1.47 (95% CI 1.22–1.76). In patients taking metformin compared with patients not taking metformin at baseline, the adjusted hazard ratio (HR) for cancer mortality was 0.43 (95% CI 0.23–0.80), and the HR with every increase of 1 g of metformin was 0.58 (95% CI 0.36–0.93). CONCLUSIONS: In general, patients with type 2 diabetes are at increased risk for cancer mortality. In our group, metformin use was associated with lower cancer mortality compared with nonuse of metformin. Although the design cannot provide a conclusion about causality, our results suggest a protective effect of metformin on cancer mortality.
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“Several epidemiologic studies have shown that metformin use is associated with reduced cancer incidence and mortality (Landman et al., 2010; Lee et al., 2011; Libby et al., 2009; Monami et al., 2011; Tseng, 2012).”
From Metformin as a tool to target aging (2016) · cites this paper as Landman et al., 2010
In the citing paper
“The reduced risk of cancer and cancer mortality observed in these studies has been consistently in the range of 25% to 30% [135-139,145-147].”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“A prospective study (median follow-up time of 9.6 years) found that metformin use at baseline was associated with lower cancer-related mortality and that this association appeared to be dose dependent [138].”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“Metformin use is associated with lower cancer-related mortality.”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“Patients with type 2 diabetes who are prescribed metformin had a lower risk of cancer compared to patients who did not take it.”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“When compared to those on other treatments, metformin users had a lower risk of cancer. A dose-relationship has been reported [138,144,145].”
From Metformin: An Old But Still the Best Treatment for Type 2 Diabetes (2013) · cites this paper as [138]
In the citing paper
“Results of a growing number of observational human studies suggest that treatment with metformin (relative to other glucose-lowering therapies) is associated with reduced risk of cancer (89–93) or cancer mortality (94).”
From Diabetes and Cancer (2010) · cites this paper as [94]
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Metformin and reduced risk of cancer in diabetic patients
Evans, J. M. M., Donnelly, L. A., Emslie-Smith, A. M., Alessi, D. R., & Morris, A. D. (2005) · BMJ · doi:10.1136/bmj.38415.708634.f7 · Cited by 2,388
The influence of glucose-lowering therapies on cancer risk in type 2 diabetes
Currie, C. J., Poole, C. D., & Gale, E. A. M. (2009) · Diabetologia · doi:10.1007/s00125-009-1440-6 · Cited by 1,124
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
Bowker, S. L., Majumdar, S. R., Veugelers, P., & Johnson, J. A. (2006) · Diabetes Care · doi:10.2337/diacare.29.02.06.dc05-1558 · Cited by 933
Jiralerspong, S., Palla, S. L., Giordano, S. H., Meric-Bernstam, F., Liedtke, C., Barnett, C. M., Hsu, L., Hung, M.-C., Hortobagyi, G. N., & Gonzalez-Angulo, A. M. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2009.19.6410 · Cited by 880 · cited 1×
“For example, type 2 diabetic patients receiving neoadjuvant chemotherapy for breast cancer as well as metformin were more likely to have a complete remission than patients not receiving metformin (14).”
Sahra, I. B., Laurent, K., Loubat, A., Giorgetti-Peraldi, S., Colosetti, P., Auberger, P., Tanti, J. F., Le Marchand-Brustel, Y., & Bost, F. (2008) · Oncogene · doi:10.1038/sj.onc.1211024 · Cited by 861
Diabetes Mellitus as a Predictor of Cancer Mortality in a Large Cohort of US Adults
Coughlin, S. S., Calle, E. E., Teras, L. R., Petrelli, J. M., & Thun, M. J. (2004) · American Journal of Epidemiology · doi:10.1093/aje/kwh161 · Cited by 795
Hemkens, L. G., Grouven, U., Bender, R., Günster, C., Gutschmidt, S., Selke, G. W., & Sawicki, P. T. (2009) · Diabetologia · doi:10.1007/s00125-009-1418-4 · Cited by 607
Antidiabetic Therapies Affect Risk of Pancreatic Cancer
Li, D., Yeung, S. J., Hassan, M. M., Konopleva, M., & Abbruzzese, J. L. (2009) · Gastroenterology · doi:10.1053/j.gastro.2009.04.013 · Cited by 584
Prospective Study of Adult Onset Diabetes Mellitus (Type 2) and Risk of Colorectal Cancer in Women
Hu, F. B., Manson, J. E., Liu, S., Hunter, D. J., Colditz, G. A., Michels, K. B., Speizer, F. E., & Giovannucci, E. L. (1999) · JNCI Journal of the National Cancer Institute · doi:10.1093/jnci/91.6.542 · Cited by 420
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Items 201–300 of 503
More favorable progesterone receptor phenotype of breast cancer in diabetics treated with metformin
Berstein, L. M., Boyarkina, M. P., Tsyrlina, E. V., Turkevich, E. A., & Семиглазов, В. Ф. (2010) · Medical Oncology · doi:10.1007/s12032-010-9572-6 · Cited by 41
Design and Characterization of Metformin-Loaded Solid Lipid Nanoparticles for Colon Cancer
Ngwuluka, N. C., Kotak, D. J., & Devarajan, P. V. (2016) · AAPS PharmSciTech · doi:10.1208/s12249-016-0505-3 · Cited by 41
Wu, Y., Warner, J. L., Wang, L., Jiang, M., Xu, J., Chen, Q., Nian, H., Dai, Q., Du, X. L., Yang, P., et al. (2019) · JCO Clinical Cancer Informatics · doi:10.1200/cci.19.00001 · Cited by 44
Meta-Assessment of Metformin Absorption and Disposition Pharmacokinetics in Nine Species
Jeong, Y., & Jusko, W. J. (2021) · Pharmaceuticals · doi:10.3390/ph14060545 · Cited by 43
Type 2 Diabetes Mellitus and Cancer: Epidemiology, Physiopathology and Prevention
Rey‐Reñones, C., Baena-Díez, J. M., Aguilar‐Palacio, I., Miquel, C., & Grau, M. (2021) · Biomedicines · doi:10.3390/biomedicines9101429 · Cited by 43
Rieken, M., Xylinas, E. N., Kluth, L. A., Trinh, Q., Lee, R. K., Fajković, H., Novara, G., Margulis, V., Lotan, Y., Martínez‐Salamanca, J. I., et al. (2013) · European Journal of Surgical Oncology · doi:10.1016/j.ejso.2013.09.016 · Cited by 40
Axl receptor tyrosine kinase is up-regulated in metformin resistant prostate cancer cells
Bansal, N., Mishra, P. J., Stein, M. N., DiPaola, R. S., & Bertino, J. R. (2015) · Oncotarget · doi:10.18632/oncotarget.4148 · 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
Ambe, C. M., Mahipal, A., Fulp, J., Chen, L., & Malafa, M. P. (2016) · PLoS ONE · doi:10.1371/journal.pone.0151632 · Cited by 39
Molecular mechanisms underlining the role of metformin as a therapeutic agent in lung cancer
Hassanabad, A. F., & MacQueen, K. T. (2020) · Cellular Oncology · doi:10.1007/s13402-020-00570-0 · Cited by 40
Antitumor effect of metformin on cholangiocarcinoma: In vitro and in vivo studies
Fujimori, T., Kato, K., Fujihara, S., Iwama, H., Yamashita, T., Kobayashi, K., Kamada, H., Morishita, A., Kobara, H., Mori, H., et al. (2015) · Oncology Reports · doi:10.3892/or.2015.4284 · Cited by 41
Arwert, E. N., Mentink, R. A., Driskell, R. R., Hoste, E., Goldie, S. J., Quist, S., & Watt, F. M. (2011) · Oncogene · doi:10.1038/onc.2011.298 · Cited by 38
Lettieri‐Barbato, D., Vegliante, R., Desideri, E., & Ciriolo, M. R. (2014) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2014.02.003 · Cited by 39
Chen, M., Zhang, J., Hu, F., Liu, S., & Zhou, Z. (2015) · Diabetes/Metabolism Research and Reviews · doi:10.1002/dmrr.2761 · Cited by 37
Müssig, K., Staiger, H., Kantartzis, K., Fritsche, A., Kanz, L., & Häring, H. (2010) · Diabetic Medicine · doi:10.1111/j.1464-5491.2010.03132.x · Cited by 37
Diabetes treatments and cancer risk: the importance of considering aspects of drug exposure
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Cancer with Diabetes: Prevalence, Metabolic Control, and Survival in an Academic Oncology Practice
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Liu, Q., Xu, X., Zhou, Y., Liu, Y., Wu, X., Huang, Z., Liu, J., Huang, Z., Kong, G., Ding, J., et al. (2018) · Calcified Tissue International · doi:10.1007/s00223-018-0468-3 · Cited by 36
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Anwar, M. A., Kheir, W. A., Eid, S., Fares, J., Liu, X., Eid, A. H., & Eid, A. A. (2014) · Journal of Cancer · doi:10.7150/jca.9726 · Cited by 35
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
Li, H., Chen, X., Yu, Y., Wang, Z., Zuo, Y., Li, S., Yang, D., HU, S., XIANG, M., Xu, Z., et al. (2014) · Oncology Reports · doi:10.3892/or.2014.3485 · Cited by 35
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Steeves, M. A., Dorsey, F. C., & Cleveland, J. L. (2010) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2009.12.013 · Cited by 37
Soraya, H., Esfahanian, N., Shakiba, Y., Ghazi-Khansari, M., Nikbin, B., Hafezzadeh, H., Maleki‐Dizaji, N., & Garjani, A. (2012) · Europe PMC (PubMed Central) · Cited by 35
Metformin Associated With Lower Cancer Mortality in Type 2 Diabetes: ZODIAC-16
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Medairos, R. A., Clark, J., Holoubek, S. A., Kubasiak, J., Pithadia, R., Hamid, F., Chmielewski, G. W., Warren, W. H., Basu, S., Borgia, J. A., et al. (2016) · Journal of Thoracic and Cardiovascular Surgery · doi:10.1016/j.jtcvs.2016.03.094 · Cited by 34
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Haukka, J. K., NISKANEN, L. K., & Auvinen, A. P. (2017) · International Journal of Cancer · doi:10.1002/ijc.31016 · Cited by 33
Biondo, L. A., Batatinha, H., de Souza, C. O., Teixeira, A. A. D. S., Silveira, L. S., Alonso‐Vale, M. I. C., Oyama, L. M., Alves, M. J., Seelaender, M. C. L., & Neto, J. C. R. (2018) · Frontiers in Pharmacology · doi:10.3389/fphar.2018.00452 · Cited by 33
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Bo, S., Benso, A. S., Durazzo, M., & Ghigo, E. (2012) · Journal of Endocrinological Investigation · doi:10.1007/bf03345423 · Cited by 33
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Targosz‐Korecka, M., Malek-Zietek, K. E., Klóska, D., Rajfur, Z., Stępień, E. Ł., Grochot‐Przeczek, A., & Szymoński, M. (2020) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2020.129533 · Cited by 32
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Chinnaiyan, S. K., Mary, S. A., Kannan, P. R., Gopinath, A., & Madhan, B. (2019) · IET Nanobiotechnology · doi:10.1049/iet-nbt.2019.0007 · Cited by 31
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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
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Rysz, J., Franczyk, B., Ławiński, J., Olszewski, R., & Gluba-Brzózka, A. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21197246 · Cited by 31
Popovics, P., Frigo, D. E., Schally, A. V., & Rick, F. G. (2015) · Expert Opinion on Therapeutic Targets · doi:10.1517/14728222.2015.1005603 · Cited by 30
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
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Małyszko, J., Małyszko, M., Kozłowski, L., Kozlowska, K., & Małyszko, J. S. (2018) · Oncotarget · doi:10.18632/oncotarget.25024 · Cited by 29
Éthier, J., McGilchrist, M., Barton, A., Cloutier, A., Ćurčin, V., Delaney, B. C., & Burgun, A. (2017) · Learning Health Systems · doi:10.1002/lrh2.10037 · Cited by 28
The female breast and diabetes
Gouveri, E., Παπάνας, Ν., & Maltezos, E. S. (2011) · The Breast · doi:10.1016/j.breast.2011.02.019 · Cited by 28
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Kim, J. M., Park, J., Lee, J. H., Park, Y., Park, S. J., Cheon, J. H., Kim, W. H., & Kim, T. I. (2020) · Diseases of the Colon & Rectum · doi:10.1097/dcr.0000000000001624 · Cited by 27
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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
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Yokomichi, H., Nagai, A., Hirata, M., Kiyohara, Y., Muto, K., Ninomiya, T., Matsuda, K., Kamatani, Y., Tamakoshi, A., Kubo, M., et al. (2017) · Journal of Epidemiology · doi:10.1016/j.je.2016.12.012 · Cited by 26
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An, H., Wang, Y., Qin, C., Li, M., Maheshwari, A., & He, L. (2020) · Scientific Reports · doi:10.1038/s41598-020-67030-5 · Cited by 25
Parish, A. J., & Swindell, W. R. (2022) · Aging Cell · doi:10.1111/acel.13733 · Cited by 26
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Shi, R., Lin, J., Gong, Y., Yan, T., Shi, F., Yang, X., Liu, X., & Naren, D. (2015) · Anti-Cancer Drugs · doi:10.1097/cad.0000000000000266 · Cited by 25
Chiang, C., Chen, Y., Chiang, C., Chen, C.-Y., Chang, Y.-C., Wang, S., See, X. Y., Horng, C., Peng, C.-Y., Hsia, Y. P., et al. (2023) · Cancer Immunology Immunotherapy · doi:10.1007/s00262-022-03363-6 · Cited by 24
Xu, Q., Zhu, T., Yi, C., & Shen, Q. (2015) · Drug Development and Industrial Pharmacy · doi:10.3109/03639045.2015.1075028 · Cited by 24
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Advances in the management of diabetes: therapies for type 2 diabetes
Tsoutsouki, J., Wunna, W., Chowdhury, A., & Chowdhury, T. A. (2020) · Postgraduate Medical Journal · doi:10.1136/postgradmedj-2019-137404 · Cited by 24
Cheng, G., Zielonka, J., Hardy, M., Ouari, O., Chitambar, C. R., Dwinell, M. B., & Kalyanaraman, B. (2019) · Oncotarget · doi:10.18632/oncotarget.26943 · Cited by 24
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Tseng, Y. (2016) · The Anatolian Journal of Cardiology · doi:10.14744/anatoljcardiol.2016.18505 · Cited by 25
Stevenson‐Hoare, J. O., Leonenko, G., & Escott‐Price, V. (2023) · BMC Public Health · doi:10.1186/s12889-023-15764-y · Cited by 25
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
Bilušić, M., Toney, N. J., Donahue, R. N., Wróblewski, S., Zibelman, M. R., Ghatalia, P., Ross, E. A., Karzai, F. H., Madan, R. A., Dahut, W. L., et al. (2022) · Prostate Cancer and Prostatic Diseases · doi:10.1038/s41391-022-00492-y · Cited by 24
Metts, J. L., Trucco, M. M., Weiser, D. A., Thompson, P., Sandler, E. S., Smith, T., Crimella, J., Sansil, S. S., Thapa, R., Fridley, B. L., et al. (2022) · Cancer Medicine · doi:10.1002/cam4.5297 · Cited by 23
Potential biomarker of metformin action
He, L., Meng, S., Germain‐Lee, E. L., Radovick, S., & Wondisford, F. E. (2014) · Journal of Endocrinology · doi:10.1530/joe-14-0084 · Cited by 23
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Nakayama, A., Ninomiya, I., Harada, S., Tsukada, T., Okamoto, K., Nakanuma, S., Sakai, S., Makino, I., Kinoshita, J., Hayashi, H., et al. (2016) · International Journal of Oncology · doi:10.3892/ijo.2016.3676 · Cited by 23
He, X., Yao, M., Zhu, M., Liang, D.-L., Guo, W., Yang, Y., Zhao, R., Ren, T., Ao, X., Wang, W., et al. (2018) · Stem Cell Research & Therapy · doi:10.1186/s13287-018-1057-0 · Cited by 23
Su, Y., Chen, T., Hsu, C., Chiu, W.-T., Lin, Y., & Chi, C. (2019) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-02526 · Cited by 23
Targeting Cancer Stem Cells with Defined Compounds and Drugs
Naujokata, C., & Laufer, S. (2013) · Journal of cancer research updates · doi:10.6000/1929-2279.2013.02.01.7 · Cited by 23
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Sun, J., Zhao, M., Jia, P., Lily, W., Wu, Y., Carissa, I., Zhou, Y., Bowton, E., Roden, D. M., Denny, J. C., et al. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004202 · Cited by 24
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Dworacki, G., Urazayev, O., Bekmukhambetov, Y., Iskakova, S., Frycz, B. A., Jagodziński, P. P., & Dworacka, M. (2015) · Immunology · doi:10.1111/imm.12522 · Cited by 23
The use of real-world data in drug repurposing
Park, K. (2021) · Translational and Clinical Pharmacology · doi:10.12793/tcp.2021.29.e18 · Cited by 22
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Hyroššová, P., Milošević, M., Škoda, J., Vachtenheim, J., Jr., Rohlena, J., & Rohlenová, K. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2022.1046630 · Cited by 23
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Rietman, E. A., Friesen, D. E., Hahnfeldt, P., Gatenby, R. A., Hlatky, L., & Tuszyński, J. A. (2013) · Theoretical Biology and Medical Modelling · doi:10.1186/1742-4682-10-39 · Cited by 22
Metformin Use in Relation With Survival Outcomes of Patients With Renal Cell Carcinoma
Cheng, J. J. S., Li, H., Tan, H. S., Tan, P. H., Ng, L. G., Ng, Q. S., Toh, C., Kanesvaran, R., & Tan, M. (2015) · Clinical Genitourinary Cancer · doi:10.1016/j.clgc.2015.12.012 · Cited by 22
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Frouws, M. A., Mulder, B. G. S., Bastiaannet, E., Zanders, M. M. J., van Herk‐Sukel, M. P. P., de Leede, E. M., Bonsing, B. A., Mieog, J. S. D., van de Velde, C. J. �., & Liefers, G. (2017) · Medicine · doi:10.1097/md.0000000000006229 · Cited by 22
Medication use and survival in diabetic patients with kidney cancer: A population-based cohort study
Nayan, M., Macdonald, E. M., Juurlink, D. N., Austin, P. C., Finelli, A., Kulkarni, G. S., & Hamilton, R. J. (2016) · Pharmacological Research · doi:10.1016/j.phrs.2016.09.027 · Cited by 21
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Wang, T., Ning, G., & Bloomgarden, Z. T. (2013) · Journal of Diabetes · doi:10.1111/1753-0407.12057 · Cited by 21
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Morrison, M. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-1-4614-5441-0_18 · Cited by 21
Ma, Y., Zhu, Q., Liang, J., Li, Y., Li, M., Zhang, Y., Wang, X., Zeng, Y., & Jiao, Y. (2020) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-020-0203-1 · Cited by 21
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Vecchia, C. L. (2011) · Metabolism · doi:10.1016/j.metabol.2011.03.011 · Cited by 20
Wang, F., Xu, J., LIU, H., Liu, Z., & XIA, F. (2016) · Molecular Medicine Reports · doi:10.3892/mmr.2016.5143 · Cited by 20
Wang, F., Ding, X., Wang, T., Shan, Z., Wang, J., Wu, S., Chi, Y., Zhang, Y., Lv, Z., Wang, L., et al. (2017) · PLoS ONE · doi:10.1371/journal.pone.0174276 · Cited by 20
Zheng, K. C., Chen, S., & Hu, X. (2022) · Current Cancer Drug Targets · doi:10.2174/1568009622666220330194149 · Cited by 20
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Lee, S., Hong, S. K., Kwak, C. H., Kim, H. H., & Lee, S. E. (2012) · Japanese Journal of Clinical Oncology · doi:10.1093/jjco/hys018 · Cited by 20
Metadata
- Authors
- Landman, G. W. D., Kleefstra, N., van Hateren, K. J. J., Groenier, K. H., Gans, R. O. B., & Bilo, H. J. G.
- Affiliations
- Isala (NL)
- Diabetes Centre, Isala Clinics, Zwolle, the Netherlands;
- University Medical Center Groningen (NL)
- Corresponding author
- Landman, Gijs W.D.
- Venue
- Diabetes Care
- Publisher
- American Diabetes Association
- Published
- 2009-11-16
- Volume
- 33
- Issue
- 2
- Pages
- 322-326
- ISSN
- 0149-5992 (ISSN-L)
- 1935-5548
- PMC
- PMC2809274
- OpenAlex
- W2058725063
- Cited by
- 502
- References
- 20
- Citations by year
- 2026: 5 · 2025: 7 · 2024: 11 · 2023: 17 · 2022: 28 · 2021: 24 · 2020: 31 · 2019: 23 · 2018: 28 · 2017: 30 · 2016: 25 · 2015: 39 · 2014: 41 · 2013: 54 · 2012: 48
- FWCI
- 18.64
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by-nc-nd
- Locations
- Diabetes Care (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, other-oa)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Metabolism, Diabetes, and Cancer
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Diabetes Treatment and Management
- Health Sciences › Medicine › Oncology › Pancreatic and Hepatic Oncology Research
- Keywords
- metformin, cancer mortality, type 2 diabetes, diabetes drugs, cancer risk, standardized mortality ratio
- MeSH terms
- Aged, Blood Pressure, Diabetes Mellitus, Type 2, Diabetic Angiopathies, Female, Glycated Hemoglobin, Humans, Hypertension, Hypoglycemic Agents, Insulin, Male, Metformin, Middle Aged, Neoplasms, Netherlands, Prospective Studies, Risk Factors, Smoking, Cohort Studies, Body Mass Index
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