Association of metformin use with risk and prognosis of esophageal cancer in patients with diabetes: A systematic review and meta-analysis_Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Authors：

WU Yanming , WANG Yan , LI Jialong , SONG Wenpeng ,  CHE Guowei

Department of Thoracic Surgery, West China Hospital, Sichuan University, Chengdu, 610041, P. R. China;

Corresponding?author：

CHE Guowei, Email: cheguowei_hx@aliyun.com

Keywords：

Metformin; diabetes; esophageal cancer; disease risk; prognosis; systematic review/meta-analysis

DOI：

10.7507/1007-4848.202012001

Video：

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Abstract Full text Figures/Tables Video References Cited by

Objective To explore the relationship between metformin use and the risk and prognosis of esophageal cancer in patients with diabetes.Methods The PubMed, Web of Science, EMbase, VIP, WanFang and CNKI databases were searched by computer to identify relevant studies from inception to August 21, 2021. Newcastle-Ottawa scale (NOS) was used to evaluate research quality. The STATA 12.0 software was used to conduct the statistical analysis.Results A total of 14 studies involving 5 605 218 participants were included finally. NOS of all researches were≥6 points. The pooled results indicated that metformin use could decrease the risk of esophageal cancer in diabetics (OR=0.84, 95%CI 0.71-1.00, P=0.045), and could also prolong the overall survival of diabetics with esophageal cancer (HR=0.89, 95%CI 0.80-0.99, P=0.025).Conclusion Metformin use can not only decrease the risk of esophageal cancer in patients with diabetes, but also improve the prognosis of diabetics with esophageal cancer significantly. However, more prospective high-quality studies are still needed to verify the conclusion.

Citation： WU Yanming, WANG Yan, LI Jialong, SONG Wenpeng, CHE Guowei. Association of metformin use with risk and prognosis of esophageal cancer in patients with diabetes: A systematic review and meta-analysis. Chinese Journal of Clinical Thoracic and Cardiovascular Surgery, 2022, 29(2): 179-185. doi: 10.7507/1007-4848.202012001 Copy

1.	Landman GW, Kleefstra N, van Hateren KJ, et al. Metformin associated with lower cancer mortality in type 2 diabetes: ZODIAC-16. Diabetes Care, 2010, 33(2): 322-326.
2.	Hevroni G, Skwiersky S, Zhyvotovska A, et al. Metformin use and the risk of gastrointestinal malignancies in diabetic populations: A meta-analysis. Int J Clin Endocrinol Metab, 2020, 6(1): 035-41.
3.	Wang YB, Tan LM, Luo L, et al. Immortal time bias exaggerates the effect of metformin on the risk of gastric cancer: A meta-analysis. Pharmacol Res, 2021, 165: 105425.
4.	Chang MS, Hartman RI, Xue J, et al. Risk of skin cancer associated with metformin use: A meta-analysis of randomized controlled trials and observational studies. Cancer Prev Res (Phila), 2021, 14(1): 77-84.
5.	郭義. 二甲雙胍對糖尿病患者發生前列腺癌風險的meta分析. 大連醫科大學, 2019.
6.	胡悅, 金武勇, 孫超, 等. 二甲雙胍與結直腸腺瘤患病風險相關性的薈萃分析. 中華結直腸疾病電子雜志, 2019, 8(1): 58-62.
7.	周小蘭, 李陽. 二甲雙胍對2型糖尿病患者胃癌影響的研究進展. 公共衛生與預防醫學, 2021, 32(1): 90-95.
8.	Mekuria AN, Ayele Y, Tola A, et al. Monotherapy with metformin versus sulfonylureas and risk of cancer in type 2 diabetic patients: A systematic review and meta-analysis. J Diabetes Res, 2019, 2019: 7676909.
9.	Zhang J, Wu J, He Q, et al. The prognostic value of metformin for advanced non-small cell lung cancer: A systematic review and meta-analysis. Transl Lung Cancer Res, 2018, 7(3): 389-396.
10.	Tang GH, Satkunam M, Pond GR, et al. Association of metformin with breast cancer incidence and mortality in patients with type Ⅱ diabetes: A GRADE-assessed systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev, 2018, 27(6): 627-635.
11.	Cheng Y, Chen Y, Zhou C, et al. For colorectal cancer patients with type Ⅱ diabetes, could metformin improve the survival rate? A meta-analysis. Clin Res Hepatol Gastroenterol, 2020, 44(1): 73-81.
12.	Sarfstein R, Friedman Y, Attias-Geva Z, et al. Metformin downregulates the insulin/IGF-I signaling pathway and inhibits different uterine serous carcinoma (USC) cells proliferation and migration in p53-dependent or -independent manners. PLoS One, 2013, 8(4): e61537.
13.	譚志強, 何立, 江妍霞. 二甲雙胍抗糖尿病患者消化系統腫瘤分子機制的研究進展. 中國全科醫學, 2021, 24(21): 2744-8.
14.	于敬坤, 韓學超, 李明志, 等. 二甲雙胍對eca-109食管癌細胞遷移能力的影響及機制研究. 陜西醫學雜志, 2019, 48(2): 139-143,147.
15.	王繼霞, 張敏, 路平. 二甲雙胍的抗食管癌作用及機制. 醫學綜述, 2018, 24(21): 4214-4217,4223.
16.	Yang Y, Jin G, Liu H, et al. Metformin inhibits esophageal squamous cell carcinoma-induced angiogenesis by suppressing JAK/STAT3 signaling pathway. Oncotarget, 2017, 8(43): 74673-74687.
17.	王彥, 林琳, 戢艷麗, 等. 術前紅細胞分布寬度與食管癌患者預后關系的系統評價與Meta分析. 中國胸心血管外科臨床雜志, 2019, 26(12): 1247-1251.
18.	Wang Y, Zhou Y, Zhou K, et al. Prognostic value of pre-treatment red blood cell distribution width in lung cancer: A meta-analysis. Biomarkers, 2020, 25(3): 241-247.
19.	Wang Y, Wang Y, Li J, et al. Clinical significance of PIK3CA gene in non-small-cell lung cancer: A systematic review and meta-analysis. Biomed Res Int, 2020, 2020: 3608241.
20.	Wang Y, Li J, Chang S, et al. Risk and influencing factors for subsequent primary lung cancer after treatment of breast cancer: A systematic review and two meta-analyses based on four million cases. J Thorac Oncol, 2021, 16(11): 1893-1908.
21.	Cheng KC, Chen YL, Lai SW, et al. Risk of esophagus cancer in diabetes mellitus: A population-based case-control study in Taiwan. BMC Gastroenterol, 2012, 12: 177.
22.	Becker C, Meier CR, Jick SS, et al. Case-control analysis on metformin and cancer of the esophagus. Cancer Causes Control, 2013, 24(10): 1763-1770.
23.	Tsilidis KK, Capothanassi D, Allen NE, et al. Metformin does not affect cancer risk: A cohort study in the U. K. Clinical Practice Research Datalink analyzed like an intention-to-treat trial. Diabetes Care, 2014, 37(9): 2522-2532.
24.	關映紅. 二甲雙胍對合并2型糖尿病的食管癌患者預后的影響. 汕頭大學, 2014.
25.	He LR, Qiao W, Liao ZX, et al. Impact of comorbidities and use of common medications on cancer and non-cancer specific survival in esophageal carcinoma. BMC Cancer, 2015, 15: 1095.
26.	Spierings LE, Lagarde SM, van Oijen MG, et al. Metformin use during treatment of potentially curable esophageal cancer patients is not associated with better outcomes. Ann Surg Oncol, 2015, 22 Suppl 3: S766-771.
27.	Tseng CH. Metformin and esophageal cancer risk in Taiwanese patients with type 2 diabetes mellitus. Oncotarget, 2017, 8(12): 18802-18810.
28.	He HH, Fu JH, Hao ZX, et al. Impact of metformin on survival outcome of esophageal squamous cell carcinomas patients undergoing surgical resection: A multicenter retrospective study. J Thorac Dis, 2020, 12(3): 830-838.
29.	Oh TK, Song IA. Metformin use and the risk of cancer in patients with diabetes: A nationwide sample cohort study. Cancer Prev Res (Phila), 2020, 13(2): 195-202.
30.	Lee MS, Hsu CC, Wahlqvist ML, et al. Type 2 diabetes increases and metformin reduces total, colorectal, liver and pancreatic cancer incidences in Taiwanese: A representative population prospective cohort study of 800, 000 individuals. BMC Cancer, 2011, 11: 20.
31.	Ruiter R, Visser LE, van Herk-Sukel MP, et al. Lower risk of cancer in patients on metformin in comparison with those on sulfonylurea derivatives: Results from a large population-based follow-up study. Diabetes Care, 2012, 35(1): 119-124.
32.	Murff HJ, Roumie CL, Greevy RA, et al. Metformin use and incidence cancer risk: Evidence for a selective protective effect against liver cancer. Cancer Causes Control, 2018, 29(9): 823-832.
33.	Wang QL, Santoni G, Ness-Jensen E, et al. Association between metformin use and risk of esophageal squamous cell carcinoma in a population-based cohort study. Am J Gastroenterol, 2020, 115(1): 73-78.
34.	Sung JJ, Ho JM, Lam AS, et al. Use of metformin and aspirin is associated with delayed cancer incidence. Cancer Epidemiol, 2020, 69: 101808.
35.	王丹. 艾塞那肽聯合二甲雙胍治療對2型糖尿病合并nafld患者胰島素抵抗、肝功能及炎癥反應的效應. 海南醫學院學報, 2017, 23(18): 2495-2498.
36.	Wu HD, Zhang JJ, Zhou BJ. The effect of metformin on esophageal cancer risk in patients with type 2 diabetes mellitus: A systematic review and meta-analysis. Clin Transl Oncol, 2021, 23(2): 275-282.
37.	劉哲銘. 二甲雙胍提高食管癌放療敏感性機制的研究. 南京: 南京大學, 2015.
38.	Xu Y, Lu S. Metformin inhibits esophagus cancer proliferation through upregulation of USP7. Cell Physiol Biochem, 2013, 32(5): 1178-1186.
39.	Hardie DG. AMP-activated/SNF1 protein kinases: Conserved guardians of cellular energy. Nat Rev Mol Cell Biol, 2007, 8(10): 774-785.
40.	Jeong KJ, Kim GW, Chung SH. AMP-activated protein kinase: An emerging target for ginseng. J Ginseng Res, 2014, 38(2): 83-88.
41.	Liu X, Chhipa RR, Pooya S, et al. Discrete mechanisms of mTOR and cell cycle regulation by AMPK agonists independent of AMPK. Proc Natl Acad Sci USA, 2014, 111(4): E435-444.
42.	Sepahi MA, Mehrabi S, Valizadeh R, et al. Nephroprotection and chemotherapy sensitivity impact of metformin during cisplatin therapy; an updated review. J Nephropathology, 2019, 8(4): e45.
43.	Saif MW, Rajagopal S, Caplain J, et al. A phaseⅠdelayed-start, randomized and pharmacodynamic study of metformin and chemotherapy in patients with solid tumors. Cancer Chemother Pharmacol, 2019, 84(6): 1323-1331.
44.	Shi YQ, Zhou XC, Du P, et al. Relationships are between metformin use and survival in pancreatic cancer patients concurrent with diabetes: A systematic review and meta-analysis. Medicine (Baltimore), 2020, 99(37): e21687.
45.	Ng CW, Jiang AA, Toh EMS, et al. Metformin and colorectal cancer: A systematic review, meta-analysis and meta-regression. Int J Colorectal Dis, 2020, 35(8): 1501-1512.
46.	Xiao K, Liu F, Liu J, et al. The effect of metformin on lung cancer risk and survival in patients with type 2 diabetes mellitus: A meta-analysis. J Clin Pharm Ther, 2020, 45(4): 783-792.
47.	Majidi A, Na R, Dixon-Suen S, et al. Common medications and survival in women with ovarian cancer: A systematic review and meta-analysis. Gynecol Oncol, 2020, 157(3): 678-685.
48.	Shuai Y, Li C, Zhou X. The effect of metformin on gastric cancer in patients with type 2 diabetes: A systematic review and meta-analysis. Clin Transl Oncol, 2020, 22(9): 1580-1590.
49.	Wang Y, Fu T, Liu Y, et al. The association between metformin and survival of head and neck cancer: A systematic review and meta-analysis of 7 retrospective cohort studies. Curr Pharm Des, 2020, 26(26): 3161-3170.
50.	Yang WT, Yang HJ, Zhou JG, et al. Relationship between metformin therapy and risk of colorectal cancer in patients with diabetes mellitus: A meta-analysis. Int J Colorectal Dis, 2020, 35(11): 2117-2131.
51.	Zhang K, Bai P, Dai H, et al. Metformin and risk of cancer among patients with type 2 diabetes mellitus: A systematic review and meta-analysis. Prim Care Diabetes, 2021, 15(1): 52-58.
52.	Wang Y, Liu X, Yan P, et al. Effect of metformin on the risk of prostate cancer in patients with type 2 diabetes by considering different confounding factors: A meta-analysis of observational studies. Eur J Cancer Prev, 2020, 29(1): 42-52.
53.	Wen Q, Zhao Z, Wen J, et al. The association between metformin therapy and risk of gynecological cancer in patients: Two meta-analyses. Eur J Obstet Gynecol Reprod Biol, 2019, 237: 33-41.
54.	Lu MZ, Li DY, Wang XF. Effect of metformin use on the risk and prognosis of ovarian cancer: An updated systematic review and meta-analysis. Panminerva Med, 2019. [Epub ahead of print].
55.	Feng Z, Zhou X, Liu N, et al. Metformin use and prostate cancer risk: A meta-analysis of cohort studies. Medicine (Baltimore), 2019, 98(12): e14955.

1. Landman GW, Kleefstra N, van Hateren KJ, et al. Metformin associated with lower cancer mortality in type 2 diabetes: ZODIAC-16. Diabetes Care, 2010, 33(2): 322-326.
2. Hevroni G, Skwiersky S, Zhyvotovska A, et al. Metformin use and the risk of gastrointestinal malignancies in diabetic populations: A meta-analysis. Int J Clin Endocrinol Metab, 2020, 6(1): 035-41.
3. Wang YB, Tan LM, Luo L, et al. Immortal time bias exaggerates the effect of metformin on the risk of gastric cancer: A meta-analysis. Pharmacol Res, 2021, 165: 105425.
4. Chang MS, Hartman RI, Xue J, et al. Risk of skin cancer associated with metformin use: A meta-analysis of randomized controlled trials and observational studies. Cancer Prev Res (Phila), 2021, 14(1): 77-84.
5. 郭義. 二甲雙胍對糖尿病患者發生前列腺癌風險的meta分析. 大連醫科大學, 2019.
6. 胡悅, 金武勇, 孫超, 等. 二甲雙胍與結直腸腺瘤患病風險相關性的薈萃分析. 中華結直腸疾病電子雜志, 2019, 8(1): 58-62.
7. 周小蘭, 李陽. 二甲雙胍對2型糖尿病患者胃癌影響的研究進展. 公共衛生與預防醫學, 2021, 32(1): 90-95.
8. Mekuria AN, Ayele Y, Tola A, et al. Monotherapy with metformin versus sulfonylureas and risk of cancer in type 2 diabetic patients: A systematic review and meta-analysis. J Diabetes Res, 2019, 2019: 7676909.
9. Zhang J, Wu J, He Q, et al. The prognostic value of metformin for advanced non-small cell lung cancer: A systematic review and meta-analysis. Transl Lung Cancer Res, 2018, 7(3): 389-396.
10. Tang GH, Satkunam M, Pond GR, et al. Association of metformin with breast cancer incidence and mortality in patients with type Ⅱ diabetes: A GRADE-assessed systematic review and meta-analysis. Cancer Epidemiol Biomarkers Prev, 2018, 27(6): 627-635.
11. Cheng Y, Chen Y, Zhou C, et al. For colorectal cancer patients with type Ⅱ diabetes, could metformin improve the survival rate? A meta-analysis. Clin Res Hepatol Gastroenterol, 2020, 44(1): 73-81.
12. Sarfstein R, Friedman Y, Attias-Geva Z, et al. Metformin downregulates the insulin/IGF-I signaling pathway and inhibits different uterine serous carcinoma (USC) cells proliferation and migration in p53-dependent or -independent manners. PLoS One, 2013, 8(4): e61537.
13. 譚志強, 何立, 江妍霞. 二甲雙胍抗糖尿病患者消化系統腫瘤分子機制的研究進展. 中國全科醫學, 2021, 24(21): 2744-8.
14. 于敬坤, 韓學超, 李明志, 等. 二甲雙胍對eca-109食管癌細胞遷移能力的影響及機制研究. 陜西醫學雜志, 2019, 48(2): 139-143,147.
15. 王繼霞, 張敏, 路平. 二甲雙胍的抗食管癌作用及機制. 醫學綜述, 2018, 24(21): 4214-4217,4223.
16. Yang Y, Jin G, Liu H, et al. Metformin inhibits esophageal squamous cell carcinoma-induced angiogenesis by suppressing JAK/STAT3 signaling pathway. Oncotarget, 2017, 8(43): 74673-74687.
17. 王彥, 林琳, 戢艷麗, 等. 術前紅細胞分布寬度與食管癌患者預后關系的系統評價與Meta分析. 中國胸心血管外科臨床雜志, 2019, 26(12): 1247-1251.
18. Wang Y, Zhou Y, Zhou K, et al. Prognostic value of pre-treatment red blood cell distribution width in lung cancer: A meta-analysis. Biomarkers, 2020, 25(3): 241-247.
19. Wang Y, Wang Y, Li J, et al. Clinical significance of PIK3CA gene in non-small-cell lung cancer: A systematic review and meta-analysis. Biomed Res Int, 2020, 2020: 3608241.
20. Wang Y, Li J, Chang S, et al. Risk and influencing factors for subsequent primary lung cancer after treatment of breast cancer: A systematic review and two meta-analyses based on four million cases. J Thorac Oncol, 2021, 16(11): 1893-1908.
21. Cheng KC, Chen YL, Lai SW, et al. Risk of esophagus cancer in diabetes mellitus: A population-based case-control study in Taiwan. BMC Gastroenterol, 2012, 12: 177.
22. Becker C, Meier CR, Jick SS, et al. Case-control analysis on metformin and cancer of the esophagus. Cancer Causes Control, 2013, 24(10): 1763-1770.
23. Tsilidis KK, Capothanassi D, Allen NE, et al. Metformin does not affect cancer risk: A cohort study in the U. K. Clinical Practice Research Datalink analyzed like an intention-to-treat trial. Diabetes Care, 2014, 37(9): 2522-2532.
24. 關映紅. 二甲雙胍對合并2型糖尿病的食管癌患者預后的影響. 汕頭大學, 2014.
25. He LR, Qiao W, Liao ZX, et al. Impact of comorbidities and use of common medications on cancer and non-cancer specific survival in esophageal carcinoma. BMC Cancer, 2015, 15: 1095.
26. Spierings LE, Lagarde SM, van Oijen MG, et al. Metformin use during treatment of potentially curable esophageal cancer patients is not associated with better outcomes. Ann Surg Oncol, 2015, 22 Suppl 3: S766-771.
27. Tseng CH. Metformin and esophageal cancer risk in Taiwanese patients with type 2 diabetes mellitus. Oncotarget, 2017, 8(12): 18802-18810.
28. He HH, Fu JH, Hao ZX, et al. Impact of metformin on survival outcome of esophageal squamous cell carcinomas patients undergoing surgical resection: A multicenter retrospective study. J Thorac Dis, 2020, 12(3): 830-838.
29. Oh TK, Song IA. Metformin use and the risk of cancer in patients with diabetes: A nationwide sample cohort study. Cancer Prev Res (Phila), 2020, 13(2): 195-202.
30. Lee MS, Hsu CC, Wahlqvist ML, et al. Type 2 diabetes increases and metformin reduces total, colorectal, liver and pancreatic cancer incidences in Taiwanese: A representative population prospective cohort study of 800, 000 individuals. BMC Cancer, 2011, 11: 20.
31. Ruiter R, Visser LE, van Herk-Sukel MP, et al. Lower risk of cancer in patients on metformin in comparison with those on sulfonylurea derivatives: Results from a large population-based follow-up study. Diabetes Care, 2012, 35(1): 119-124.
32. Murff HJ, Roumie CL, Greevy RA, et al. Metformin use and incidence cancer risk: Evidence for a selective protective effect against liver cancer. Cancer Causes Control, 2018, 29(9): 823-832.
33. Wang QL, Santoni G, Ness-Jensen E, et al. Association between metformin use and risk of esophageal squamous cell carcinoma in a population-based cohort study. Am J Gastroenterol, 2020, 115(1): 73-78.
34. Sung JJ, Ho JM, Lam AS, et al. Use of metformin and aspirin is associated with delayed cancer incidence. Cancer Epidemiol, 2020, 69: 101808.
35. 王丹. 艾塞那肽聯合二甲雙胍治療對2型糖尿病合并nafld患者胰島素抵抗、肝功能及炎癥反應的效應. 海南醫學院學報, 2017, 23(18): 2495-2498.
36. Wu HD, Zhang JJ, Zhou BJ. The effect of metformin on esophageal cancer risk in patients with type 2 diabetes mellitus: A systematic review and meta-analysis. Clin Transl Oncol, 2021, 23(2): 275-282.
37. 劉哲銘. 二甲雙胍提高食管癌放療敏感性機制的研究. 南京: 南京大學, 2015.
38. Xu Y, Lu S. Metformin inhibits esophagus cancer proliferation through upregulation of USP7. Cell Physiol Biochem, 2013, 32(5): 1178-1186.
39. Hardie DG. AMP-activated/SNF1 protein kinases: Conserved guardians of cellular energy. Nat Rev Mol Cell Biol, 2007, 8(10): 774-785.
40. Jeong KJ, Kim GW, Chung SH. AMP-activated protein kinase: An emerging target for ginseng. J Ginseng Res, 2014, 38(2): 83-88.
41. Liu X, Chhipa RR, Pooya S, et al. Discrete mechanisms of mTOR and cell cycle regulation by AMPK agonists independent of AMPK. Proc Natl Acad Sci USA, 2014, 111(4): E435-444.
42. Sepahi MA, Mehrabi S, Valizadeh R, et al. Nephroprotection and chemotherapy sensitivity impact of metformin during cisplatin therapy; an updated review. J Nephropathology, 2019, 8(4): e45.
43. Saif MW, Rajagopal S, Caplain J, et al. A phaseⅠdelayed-start, randomized and pharmacodynamic study of metformin and chemotherapy in patients with solid tumors. Cancer Chemother Pharmacol, 2019, 84(6): 1323-1331.
44. Shi YQ, Zhou XC, Du P, et al. Relationships are between metformin use and survival in pancreatic cancer patients concurrent with diabetes: A systematic review and meta-analysis. Medicine (Baltimore), 2020, 99(37): e21687.
45. Ng CW, Jiang AA, Toh EMS, et al. Metformin and colorectal cancer: A systematic review, meta-analysis and meta-regression. Int J Colorectal Dis, 2020, 35(8): 1501-1512.
46. Xiao K, Liu F, Liu J, et al. The effect of metformin on lung cancer risk and survival in patients with type 2 diabetes mellitus: A meta-analysis. J Clin Pharm Ther, 2020, 45(4): 783-792.
47. Majidi A, Na R, Dixon-Suen S, et al. Common medications and survival in women with ovarian cancer: A systematic review and meta-analysis. Gynecol Oncol, 2020, 157(3): 678-685.
48. Shuai Y, Li C, Zhou X. The effect of metformin on gastric cancer in patients with type 2 diabetes: A systematic review and meta-analysis. Clin Transl Oncol, 2020, 22(9): 1580-1590.
49. Wang Y, Fu T, Liu Y, et al. The association between metformin and survival of head and neck cancer: A systematic review and meta-analysis of 7 retrospective cohort studies. Curr Pharm Des, 2020, 26(26): 3161-3170.
50. Yang WT, Yang HJ, Zhou JG, et al. Relationship between metformin therapy and risk of colorectal cancer in patients with diabetes mellitus: A meta-analysis. Int J Colorectal Dis, 2020, 35(11): 2117-2131.
51. Zhang K, Bai P, Dai H, et al. Metformin and risk of cancer among patients with type 2 diabetes mellitus: A systematic review and meta-analysis. Prim Care Diabetes, 2021, 15(1): 52-58.
52. Wang Y, Liu X, Yan P, et al. Effect of metformin on the risk of prostate cancer in patients with type 2 diabetes by considering different confounding factors: A meta-analysis of observational studies. Eur J Cancer Prev, 2020, 29(1): 42-52.
53. Wen Q, Zhao Z, Wen J, et al. The association between metformin therapy and risk of gynecological cancer in patients: Two meta-analyses. Eur J Obstet Gynecol Reprod Biol, 2019, 237: 33-41.
54. Lu MZ, Li DY, Wang XF. Effect of metformin use on the risk and prognosis of ovarian cancer: An updated systematic review and meta-analysis. Panminerva Med, 2019. [Epub ahead of print].
55. Feng Z, Zhou X, Liu N, et al. Metformin use and prostate cancer risk: A meta-analysis of cohort studies. Medicine (Baltimore), 2019, 98(12): e14955.

Chinese Journal of Clinical Thoracic and Cardiovascular Surgery

Association of metformin use with risk and prognosis of esophageal cancer in patients with diabetes: A systematic review and meta-analysis

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