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Breast cancer
Association of Insulin, Metformin, and Statin with Mortality in Breast Cancer Patients
Mihong Choi, Jiyeon Han, Bo Ram Yang, Myoung-jin Jang, Miso Kim, Dae-Won Lee, Tae-Yong Kim, Seock-Ah Im, Han-Byoel Lee, Hyeong-Gon Moon, Wonshik Han, Dong-Young Noh, Kyung-Hun Lee
Cancer Res Treat. 2021;53(1):65-76.   Published online September 23, 2020
DOI: https://doi.org/10.4143/crt.2020.430
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
This study investigated the association of insulin, metformin, and statin use with survival and whether the association was modified by the hormone receptor status of the tumor in patients with breast cancer.
Materials and Methods
We studied 7,452 patients who had undergone surgery for breast cancer at Seoul National University Hospital from 2008 to 2015 using the nationwide claims database. Exposure was defined as a recorded prescription of each drug within 12 months before the diagnosis of breast cancer.
Results
Patients with prior insulin or statin use were more likely to be older than 50 years at diagnosis and had a higher comorbidity index than those without it (p < 0.01 for both). The hazard ratio (HR) for death with insulin use was 5.7 (p < 0.01), and the effect was attenuated with both insulin and metformin exposure with an HR of 1.2 (p=0.60). In the subgroup analyses, a heightened risk of death with insulin was further prominent with an HR of 17.9 (p < 0.01) and was offset by co-administration of metformin with an HR of 1.3 (p=0.67) in patients with estrogen receptor (ER)–negative breast cancer. Statin use was associated with increased overall mortality only in patients with ER-positive breast cancer with HR for death of 1.5 (p=0.05).
Conclusion
Insulin or statin use before the diagnosis of breast cancer was associated with an increase in all-cause mortality. Subsequent analyses suggested that metformin or statin use may have been protective in patients with ER-negative disease, which warrants further studies.

Citations

Citations to this article as recorded by  
  • Repurposing of Metabolic Drugs Metformin and Simvastatin as an Emerging Class of Cancer Therapeutics
    Santosh Kumar Maurya, Smriti Chaudhri, Shashank Kumar, Sanjay Gupta
    Pharmaceutical Research.2025; 42(1): 49.     CrossRef
  • Are statins onco- suppressive agents for every type of tumor? A systematic review of literature
    Luca Filaferro, Fabiana Zaccarelli, Giovanni Francesco Niccolini, Andrea Colizza, Federica Zoccali, Michele Grasso, Massimo Fusconi
    Expert Review of Anticancer Therapy.2024; 24(6): 435.     CrossRef
  • Investigating the relationship between insulin use and all-cause mortality, breast cancer mortality, and recurrence risk in diabetic patients with breast cancer: A comprehensive systematic review and meta-analysis
    Marina V. Loktionova, Mahdi Mohammadian, Roya Choopani, Soleiman Kheiri, Abdollah Mohammadian-Hafshejani, Kathleen Bennett
    PLOS ONE.2024; 19(12): e0314565.     CrossRef
  • Impact of statin use on breast cancer recurrence and mortality before and after diagnosis: a systematic review and meta-analysis
    Xiaolin Jia, Ye Lu, Zili Xu, Qingqing Mu
    Frontiers in Oncology.2023;[Epub]     CrossRef
  • Effect of statins use on risk and prognosis of breast cancer: a meta-analysis
    Guodong Zhao, Yanjun Ji, Qing Ye, Xin Ye, Guanqun Wo, Xi Chen, Xinyi Shao, Jinhai Tang
    Anti-Cancer Drugs.2022; 33(1): e507.     CrossRef
  • Studying the Cytotoxic Activity of Newly Designed and Synthesized HDAC Inhibitors Derivatives of Pentanoyl Anilide‐5‐Biguanide
    Othman Makki Sagheer, Mohammed Hassan Mohammed, Jaafar S. Wadi, Zaid O. Ibraheem
    Macromolecular Symposia.2022;[Epub]     CrossRef
  • Metformin and Breast Cancer: Where Are We Now?
    Mónica Cejuela, Begoña Martin-Castillo, Javier A. Menendez, Sonia Pernas
    International Journal of Molecular Sciences.2022; 23(5): 2705.     CrossRef
  • Cholesterol and Its Derivatives: Multifaceted Players in Breast Cancer Progression
    Giorgia Centonze, Dora Natalini, Alessio Piccolantonio, Vincenzo Salemme, Alessandro Morellato, Pietro Arina, Chiara Riganti, Paola Defilippi
    Frontiers in Oncology.2022;[Epub]     CrossRef
  • Synthesis of gamma biguanides butyric acid analogues as HDAC inhibitors and studying their cytotoxic activity
    Othman Makki Sagheer, Mohammed Hassan Mohammed, Zaid O. Ibraheem, Jaafar S. Wadi, Mustafa F. Tawfeeq
    Materials Today: Proceedings.2021; 47: 5983.     CrossRef
  • Statins: a repurposed drug to fight cancer
    Wen Jiang, Jin-Wei Hu, Xu-Ran He, Wei-Lin Jin, Xin-Yang He
    Journal of Experimental & Clinical Cancer Research.2021;[Epub]     CrossRef
  • Potential intrinsic subtype dependence on the association between metformin use and survival in surgically resected breast cancer: a Korean national population-based study
    Byoung Hyuck Kim, Moon-June Cho, Jeanny Kwon
    International Journal of Clinical Oncology.2021; 26(11): 2004.     CrossRef
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Diabetes Medication Use in Association with Survival among Patients of Breast, Colorectal, Lung, or Gastric Cancer
Michelle L. Baglia, Yong Cui, Tao Zheng, Gong Yang, Honglan Li, Mingrong You, Liling Xu, Harvey Murff, Yu-Tang Gao, Wei Zheng, Yong-Bing Xiang, Xiao-Ou Shu
Cancer Res Treat. 2019;51(2):538-546.   Published online July 2, 2018
DOI: https://doi.org/10.4143/crt.2017.591
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
Studies suggest that regular use of metformin may decrease cancer mortality. We investigated the association between diabetes medication use and cancer survival.
Materials and Methods
The current study includes 633 breast, 890 colorectal, 824 lung, and 543 gastric cancer cases identified from participants of two population-based cohort studies in Shanghai. Information on diabetes medication use was obtained by linking to electronic medical records. The associations between diabetes medication use (metformin, sulfonylureas, and insulin) and overall and cancer-specific survival were evaluated using time-dependent Cox proportional hazards models.
Results
After adjustment for clinical characteristics and treatment factors, use of metformin was associated with better overall survival among colorectal cancer patients (hazards ratio [HR], 0.55; 95% confidence interval [CI], 0.34 to 0.88) and for all four types of cancer combined (HR, 0.75; 95% CI, 0.57 to 0.98). Ever use of insulin was associated with worse survival for all cancer types combined (HR, 1.89; 95% CI, 1.57 to 2.29) and for the four cancer types individually. Similar associations were seen for diabetic patients. Sulfonylureas use was associated with worse overall survival for breast or gastric cancer (HR, 2.87; 95% CI, 1.22 to 6.80 and HR, 2.05; 95% CI, 1.09 to 3.84, respectively) among diabetic patients. Similar association patterns were observed between diabetes medication use and cancer-specific survival.
Conclusion
Metformin was associated with improved survival among colorectal cancer cases, while insulin use was associated with worse survival among patients of four major cancers. Further investigation on the topic is needed given the potential translational impact of these findings.

Citations

Citations to this article as recorded by  
  • Effect of Metformin Use on Survival and Recurrence Rate of Gastric Cancer After Gastrectomy in Diabetic Patients: A Systematic Review and Meta-analysis of Observational Studies
    Mansour Bahardoust, Safa Mousavi, Zahra Deylami Moezi, Mohsen Yarali, Ali Tayebi, Faranak Olamaeian, Adnan Tizmaghz
    Journal of Gastrointestinal Cancer.2024; 55(1): 65.     CrossRef
  • Antidiabetic Drugs in Breast Cancer Patients
    Wojciech Garczorz, Agnieszka Kosowska, Tomasz Francuz
    Cancers.2024; 16(2): 299.     CrossRef
  • Association of metformin and statin uses with the prognosis of colon cancer: a meta-analysis
    Yanyan Xu, Hao Che, Jiang Liu, Pingjiang Ye
    European Journal of Cancer Prevention.2024; 33(5): 414.     CrossRef
  • Metformin in combination with chemotherapy increases apoptosis in gastric cancer cells and counteracts senescence induced by chemotherapy
    Katia Vázquez‑Ibarra, Josefina Sánchez López, Tomás Pineda Razo, José Cruz Lozano, Brenda Ortiz‑Tamayo, Luis Palafox‑Mariscal, Rosa González Arreola, Juan González‑García, Pablo Ortiz-Lazareno
    Oncology Letters.2024;[Epub]     CrossRef
  • Investigating the relationship between insulin use and all-cause mortality, breast cancer mortality, and recurrence risk in diabetic patients with breast cancer: A comprehensive systematic review and meta-analysis
    Marina V. Loktionova, Mahdi Mohammadian, Roya Choopani, Soleiman Kheiri, Abdollah Mohammadian-Hafshejani, Kathleen Bennett
    PLOS ONE.2024; 19(12): e0314565.     CrossRef
  • A Mathematical Model of the Disruption of Glucose Homeostasis in Cancer Patients
    Noah Salentine, Jonathan Doria, Chinh Nguyen, Gabriella Pinter, Shizhen Emily Wang, Peter Hinow
    Bulletin of Mathematical Biology.2023;[Epub]     CrossRef
  • Effect of Metformin on the Prognosis of Gastric Cancer Patients with Type 2 Diabetes Mellitus: A Meta-Analysis Based on Retrospective Cohort Studies
    Lingna Li, Jianing Huang, Tongmin Huang, Jie Yao, Yeyuan Zhang, Meiling Chen, Haojie Shentu, Haiying Lou, Flavia Prodam
    International Journal of Endocrinology.2023; 2023: 1.     CrossRef
  • Shared Lifestyle-Related Risk Factors of Cardiovascular Disease and Cancer: Evidence for Joint Prevention
    Farzad Masoudkabir, Noushin Mohammadifard, Arya Mani, Andrew Ignaszewski, Margot K. Davis, Golnaz Vaseghi, Marjan Mansourian, Christopher Franco, Carolyn Gotay, Nizal Sarrafzadegan, Francesco Giallauria
    The Scientific World Journal.2023; 2023: 1.     CrossRef
  • Diabetes Mellitus and Gastric Cancer: Correlation and Potential Mechanisms
    Li Wang, Zhe Zhang, Eusebio Chiefari
    Journal of Diabetes Research.2023; 2023: 1.     CrossRef
  • Perspectives of metformin use in endometrial cancer and other gynaecological malignancies
    Bartłomiej Barczyński, Karolina Frąszczak, Jan Kotarski
    Journal of Drug Targeting.2022; 30(4): 359.     CrossRef
  • Type 2 Diabetes and all-cause mortality among Spanish women with breast cancer
    L. Fernández-Arce, N. Robles-Rodríguez, A. Fernández-Feito, A. Llaneza-Folgueras, A. I. Encinas-Muñiz, A. Lana
    Cancer Causes & Control.2022; 33(2): 271.     CrossRef
  • Diabetes and Colorectal Cancer Risk: Clinical and Therapeutic Implications
    Guan-Hua Yu, Shuo-Feng Li, Ran Wei, Zheng Jiang, Eusebio Chiefari
    Journal of Diabetes Research.2022; 2022: 1.     CrossRef
  • Systemic Evaluation of the Effect of Diabetes Mellitus on Breast Cancer in a Mouse Model
    Nana Wei, Jinmiao Lu, Zhibing Lin, Xiaoyu Wang, Mengmeng Cai, Shengyao Jiang, Xiaoyu Chen, Shilan Zhu, Dong Zhang, Li Cui
    Frontiers in Oncology.2022;[Epub]     CrossRef
  • The Association of Metformin, Other Antidiabetic Medications and Statins on the Prognosis of Rectal Cancer in Patients with Type 2 Diabetes: A Retrospective Cohort Study
    Sami Erkinantti, Ari Hautakoski, Reijo Sund, Martti Arffman, Elina Urpilainen, Ulla Puistola, Esa Läärä, Arja Jukkola, Peeter Karihtala
    Biomolecules.2022; 12(9): 1301.     CrossRef
  • Metformin protects against diabetes-induced heart injury and dunning prostate cancer model
    BB Bayrak, P Koroglu, O Karabulut Bulan, R Yanardag
    Human & Experimental Toxicology.2021; 40(2): 297.     CrossRef
  • Pharmacological inhibition of tumor anabolism and host catabolism as a cancer therapy
    Alejandro Schcolnik-Cabrera, Alma Chavez-Blanco, Guadalupe Dominguez-Gomez, Mandy Juarez, Ariana Vargas-Castillo, Rafael Isaac Ponce-Toledo, Donna Lai, Sheng Hua, Armando R. Tovar, Nimbe Torres, Delia Perez-Montiel, Jose Diaz-Chavez, Alfonso Duenas-Gonzal
    Scientific Reports.2021;[Epub]     CrossRef
  • Repurposing metformin for the treatment of gastrointestinal cancer
    Ademar Dantas Cunha Júnior, Arinilda Campos Bragagnoli, Felipe Osório Costa, José Barreto Campello Carvalheira
    World Journal of Gastroenterology.2021; 27(17): 1883.     CrossRef
  • Improved prognosis in gastric adenocarcinoma among metformin users in a population-based study
    Jiaojiao Zheng, Giola Santoni, Shao-Hua Xie, Jesper Lagergren
    British Journal of Cancer.2021; 125(2): 277.     CrossRef
  • The Relationship between Diabetes Mellitus and Gastric Cancer and the Potential Benefits of Metformin: An Extensive Review of the Literature
    Chin-Hsiao Tseng
    Biomolecules.2021; 11(7): 1022.     CrossRef
  • Potential intrinsic subtype dependence on the association between metformin use and survival in surgically resected breast cancer: a Korean national population-based study
    Byoung Hyuck Kim, Moon-June Cho, Jeanny Kwon
    International Journal of Clinical Oncology.2021; 26(11): 2004.     CrossRef
  • Progress in understanding of relationship between diabetes and colorectal cancer
    Guan-Hua Yu, Zheng Jiang
    World Chinese Journal of Digestology.2021; 29(23): 1323.     CrossRef
  • The effect of metformin on gastric cancer in patients with type 2 diabetes: a systematic review and meta-analysis
    Y. Shuai, C. Li, X. Zhou
    Clinical and Translational Oncology.2020; 22(9): 1580.     CrossRef
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    Guntram Schernthaner, Gerit-Holger Schernthaner
    Diabetes Research and Clinical Practice.2020; 159: 107946.     CrossRef
  • Suppressive effects of metformin on colorectal adenoma incidence and malignant progression
    Min Deng, Siqin Lei, Dongdong Huang, Hui Wang, Shuli Xia, Enping Xu, Yihua Wu, Honghe Zhang
    Pathology - Research and Practice.2020; 216(2): 152775.     CrossRef
  • Preventative and Therapeutic Effects of Metformin in Gastric Cancer: A New Contribution of an Old Friend


    Jing Zhang, Liping Wen, Quan Zhou, Kuifeng He, Lisong Teng
    Cancer Management and Research.2020; Volume 12: 8545.     CrossRef
  • Does Roux-en-Y Construction Really Bring Benefit of Type 2 Diabetes Mellitus Remission After Gastrectomy in Patients with Gastric Cancer? A Systematic Review and Meta-Analysis
    Dong Peng, Yu-Xi Cheng, Wei Zhang
    Diabetes Therapy.2020; 11(12): 2863.     CrossRef
  • Prognosis of Patients with Colorectal Cancer with Diabetes According to Medication Adherence: A Population-Based Cohort Study
    Sunho Choe, Joonki Lee, Ji Won Park, Seung-Yong Jeong, Young Min Cho, Byung-Joo Park, Aesun Shin
    Cancer Epidemiology, Biomarkers & Prevention.2020; 29(6): 1120.     CrossRef
  • The combination of orlistat, lonidamine and 6‑diazo‑5‑oxo‑L‑norleucine induces a quiescent energetic phenotype and limits substrate flexibility in colon cancer cells
    Alejandro Schcolnik‑Cabrera, Alma Chavez‑Blanco, Guadalupe Dominguez‑Gomez, Mandy Juarez, Donna Lai, Sheng Hua, Armando Tovar, Jose Diaz‑Chavez, Alfonso Duenas‑Gonzalez
    Oncology Letters.2020; 20(3): 3053.     CrossRef
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    Junichi Kato, Yohei Shirakami, Masahito Shimizu
    Gastrointestinal Disorders.2019; 1(2): 273.     CrossRef
  • Use of Antihypertensive Medications and Survival Rates for Breast, Colorectal, Lung, or Stomach Cancer
    Yong Cui, Wanqing Wen, Tao Zheng, Honglan Li, Yu-Tang Gao, Hui Cai, Mingrong You, Jing Gao, Gong Yang, Wei Zheng, Yong-Bing Xiang, Xiao-Ou Shu
    American Journal of Epidemiology.2019; 188(8): 1512.     CrossRef
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    Jinhui Liu, Li Yang
    Oncology Letters.2019;[Epub]     CrossRef
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    Audrius Dulskas, Ausvydas Patasius, Donata Linkeviciute-Ulinskiene, Lina Zabuliene, Giedre Smailyte
    Aging.2019; 11(17): 7197.     CrossRef
  • 10,742 View
  • 266 Download
  • 38 Web of Science
  • 32 Crossref
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High-Dose Metformin Plus Temozolomide Shows Increased Anti-tumor Effects in Glioblastoma In Vitro and In Vivo Compared with Monotherapy
Jung Eun Lee, Ji Hee Lim, Yong Kil Hong, Seung Ho Yang
Cancer Res Treat. 2018;50(4):1331-1342.   Published online January 10, 2018
DOI: https://doi.org/10.4143/crt.2017.466
AbstractAbstract PDFSupplementary MaterialPubReaderePub
Purpose
The purpose of the study is to investigate the efficacy of combined treatment with temozolomide (TMZ) and metformin for glioblastoma (GBM) in vitro and in vivo.
Materials and Methods
We investigated the efficacy of combined treatment with TMZ and metformin using cell viability and apoptosis assays. A GBM orthotopic mice model was established by inoculation of 5×105 U87 cells and treatedwith metformin, TMZ, and the combination for 4weeks. Western blotting and immunofluorescence of tumor specimens were analyzed to investigate AMP-activated protein kinase (AMPK) and AKT pathway.
Results
The combination of TMZ and metformin showed higher cytotoxicity than single agents in U87, U251, and A172 cell lines. A combination of high-dose metformin and TMZ showed the highest apoptotic activity. The combination of TMZ and metformin enhanced AMPK phosphorylation and inhibited mammalian target of rapamycin phosphorylation, AKT phosphorylation, and p53 expression. The median survival of each group was 43.6, 55.2, 53.2, 65.2, and 71.3 days for control, metformin treatment (2 mg/25 g/day or 10 mg/25 g/day), TMZ treatment (15 mg/kg/day), combination treatment with low-dose metformin and TMZ, and combination treatment with high-dose metformin and TMZ, respectively. Expression of fatty acid synthase (FASN) was significantly decreased in tumor specimens treated with metformin and TMZ.
Conclusion
The combination of metformin and TMZ was superior to monotherapy using metformin or TMZ in terms of cell viability in vitro and survival in vivo. The combination of high-dose metformin and TMZ inhibited FASN expression in an orthotopic model. Inhibition of FASN might be a potential therapeutic target of GBM.

Citations

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    Marcio Yuri Ferreira, Eloísa Bittencurt Thomaz de Assis, Savio Batista, Lucca B. Palavani, Gabriel Verly, Eduardo Mendes Corrêa, Lucas Pari Mitre, Jessica Sales de Oliveira, Raphael Bertani, Daniel Antunes Moreno, Allan Dias Polverini
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    Shankargouda Patil
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    Neslisah Barlak, Fatma Sanli, Ozel Capik, Elanur Tuysuz, Elanur Aydın Karatas, Hasan Turkez, Omer Faruk Karatas
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Effects and Mechanisms of Metformin on the Proliferation of Esophageal Cancer Cells In Vitro and In Vivo
Jian-Cai Tang, Rui An, Yi-Qing Jiang, Jian Yang
Cancer Res Treat. 2017;49(3):778-789.   Published online November 11, 2016
DOI: https://doi.org/10.4143/crt.2015.485
AbstractAbstract PDFPubReaderePub
Purpose
The purpose of this study was to observe the effects of metformin on human esophageal cancer cell and to investigate its possible mechanisms.
Materials and Methods
Cell viability was detected by using a Cell Counting Kit-8, while cell cycle and apoptosis were assessed by flow cytometry and western blot was used to measure the expression of the related proteins. RNAi was used to knockout pyruvate kinase muscle isozyme 2 (PKM2). An Eca109 tumor model was established to evaluate the antitumor effect in vivo. Immunohistochemistry was determined based on the expression of PKM2 and Bim in tumor tissues. Tunnel was used to assess tumor cell apoptosis.
Results
Esophageal cancer cells viability was reduced after metformin treatment. The cell cycle was arrested in the G0/G1 phase, apoptosis was induced, caspase 3 was activated, caspase 9 was downregulated, and the pro-apoptotic protein Bim increased. Further study revealed that metformin could suppress the expression of insulin-like growth factor 1 receptor and its downstream proteins, phosphoinositide 3-kinase (PI3K), protein kinase B (AKT/PKB), phosphorylation of AKT (pAKT), mammalian target of rapamycin (mTOR), p70S6K, and PKM2. Insulin-like growth factor 1 partly reversed metfromin-induced apoptosis and attenuated the repression effect of metfomin to PI3K, pAKT, and PKM2. Knockout PKM2 resulted in the activation of caspase 3, down-regulation of caspase 9, and increased expression of Bim. In the Eca109 xenograft model, metformin significantly reduced tumor growth. Furthermore, we found that metformin treatment increased the rate of apoptosis, down-regulation of PKM2, and up-regulation of Bim in tumor tissues.
Conclusion
Metformin restrained esophageal cancer cell proliferation partly by suppressing the PI3K/AKT/mTOR pathway.

Citations

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Association between Metformin Use and Survival in Nonmetastatic Rectal Cancer Treated with a Curative Resection: A Nationwide Population Study
Young-Jun Ki, Hyo Jeong Kim, Mi-Sook Kim, Chan Mi Park, Min Jung Ko, Young Seok Seo, Sun Mi Moon, Jin A Choi
Cancer Res Treat. 2017;49(1):29-36.   Published online July 4, 2016
DOI: https://doi.org/10.4143/crt.2016.128
AbstractAbstract PDFPubReaderePub
Purpose
Metformin is associated with an anticancer effect. However, the effects of metformin in rectal cancer are controversial. This study investigated the impact of metformin on the survival of patients with diabetes mellitus and nonmetastatic rectal cancer who underwent curative surgery.
Materials and Methods
The database was provided by the Korea Center Cancer Registry and National Health Insurance Service of the Republic of Korea. A cohort of patients with newly diagnosed rectal cancer between 2005 and 2011 was identified. Drug exposure was defined as receiving the oral hypoglycemic agent for at least 90 days over the period from 6 months before the initial diagnosis of rectal cancer to the last follow-up.
Results
A total of 4,503 patients were prescribed oral hypoglycemic agents and classified as the diabetic group, of which 3,694 patients received metformin for at least 90 days. Unadjusted analyses showed a significantly higher overall survival (hazard ratio, 0.596; 95% confidence interval, 0.506 to 0.702) and rectal cancer-specific survival (hazard ratio, 0.621; 95% confidence interval, 0.507 to 0.760) in the metformin group than in the nonmetformin group. The adjusted overall survival (hazard ratio, 0.631; 95% confidence interval, 0.527 to 0.755) and cancer-specific survival (hazard ratio, 0.598; 95% confidence interval, 0.479 to 0.746) in the group with a medication possession ratio of 80% or greater was significantly higher than in the group with a medication possession ratio of less than 80%.
Conclusion
Metformin use is associated with overall and cancer-specific survival in diabetic patients with a nonmetastatic rectal cancer treated with a curative resection.

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