Metformin is associated with survival benefit in pancreatic cancer patients with diabetes: A systematic review and metaanalysis

Oncotarget

Volumn 8, Issue 15, 2017, Pages 25242-25250

  Zhou, Ping Ting ^a   Li, Bo ^b   Liu, Fu Rao ^a   Zhang, Mei Chao ^a   Wang, Qian ^a   Li, Yan Yan ^a   Xu, Ci ^a   Liu, Yuan Hua ^c   Yao, Yuan ^a   Li, Dong ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SECOND MILITARY MEDICAL UNIVERSITY   (China)

^c JIANGSU CANCER HOSPITAL   (China)

Author keywords

Diabetes; Metformin; Overall survival; Pancreatic cancer

Indexed keywords

METFORMIN; ANTIDIABETIC AGENT;

ARTICLE; ASIA; CANCER MORTALITY; CANCER PATIENT; CANCER SURVIVAL; CLINICAL TRIAL (TOPIC); DIABETES MELLITUS; DRUG EFFECT; DRUG EFFICACY; DRUG USE; EUROPE; HUMAN; META ANALYSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; OVERALL SURVIVAL; PANCREAS CANCER; RISK REDUCTION; SYSTEMATIC REVIEW; WESTERN HEMISPHERE; COMPLICATION; MORTALITY; PANCREAS TUMOR; PROPORTIONAL HAZARDS MODEL; PUBLISHING;

DIABETES MELLITUS, TYPE 2; HUMANS; HYPOGLYCEMIC AGENTS; METFORMIN; PANCREATIC NEOPLASMS; PROPORTIONAL HAZARDS MODELS; PUBLICATION BIAS;

EID: 85017541377     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.15692     Document Type: Article

References (58)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin. 2013; 63:11-30.
2. B. S, Smith G, Hurria A, Hortobagyi G, Buchholz T. Future of cancer incidence in the United States: burdens upon an aging, changing nation. Journal of clinical oncology. 2009; 27:2758-2765.
3. Schneider G, Siveke JT, Eckel F, Schmid RM. Pancreatic cancer: basic and clinical aspects. Gastroenterology. 2005; 128:1606-1625.
4. Li D, Xie K, Wolff R, Abbruzzese JL. Pancreatic cancer. Lancet. 2004; 363:1049-1057.
5. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin. 2012; 62:10-29.
6. Yeo CJ, Cameron JL, Sohn TA, Lillemoe KD, Pitt HA, Talamini MA, Hruban RH, Ord SE, Sauter PK, Coleman J, Zahurak ML, Grochow LB, Abrams RA. Six hundred fifty consecutive pancreaticoduodenectomies in the 1990s: pathology, complications, and outcomes. Annals of surgery. 1997; 226:248-257; discussion 257-260.
7. Nitecki SS, Sarr MG, Colby TV, van Heerden JA. Longterm survival after resection for ductal adenocarcinoma of the pancreas. Is it really improving? Annals of surgery. 1995; 221:59-66.
8. Maisonneuve P, Lowenfels AB. Epidemiology of pancreatic cancer: an update. Digestive diseases. 2010; 28:645-656.
9. Yuan C, Rubinson DA, Qian ZR, Wu C, Kraft P, Bao Y, Ogino S, Ng K, Clancy TE, Swanson RS, Gorman MJ, Brais LK, Li T, et al. Survival among patients with pancreatic cancer and long-standing or recent-onset diabetes mellitus. Journal of clinical oncology. 2015; 33:29-35.
10. Batabyal P, Vander Hoorn S, Christophi C, Nikfarjam M. Association of diabetes mellitus and pancreatic adenocarcinoma: a meta-analysis of 88 studies. Annals of surgical oncology. 2014; 21:2453-2462.
11. Li D, Yeung SC, Hassan MM, Konopleva M, Abbruzzese JL. Antidiabetic therapies affect risk of pancreatic cancer. Gastroenterology. 2009; 137:482-488.
12. Bodmer M, Meier C, Krahenbuhl S, Jick SS, Meier CR. Long-term metformin use is associated with decreased risk of breast cancer. Diabetes care. 2010; 33:1304-1308.
13. Tseng CH. Metformin reduces gastric cancer risk in patients with type 2 diabetes mellitus. Aging (Albany NY). 2016; 8:1636-1649. doi: 10.18632/aging.101019.
14. Bodmer M, Becker C, Meier C, Jick SS, Meier CR. Use of metformin and the risk of ovarian cancer: a case-control analysis. Gynecologic oncology. 2011; 123:200-204.
15. Yin M, Zhou J, Gorak EJ, Quddus F. Metformin is associated with survival benefit in cancer patients with concurrent type 2 diabetes: a systematic review and metaanalysis. The oncologist. 2013; 18:1248-1255.
16. Wang Z, Lai ST, Xie L, Zhao JD, Ma NY, Zhu J, Ren ZG, Jiang GL. Metformin is associated with reduced risk of pancreatic cancer in patients with type 2 diabetes mellitus: a systematic review and meta-analysis. Diabetes research and clinical practice. 2014; 106:19-26.
17. Amin S, Mhango G, Lin J, Aronson A, Wisnivesky J, Boffetta P, Lucas AL. Metformin Improves Survival in Patients with Pancreatic Ductal Adenocarcinoma and Pre-Existing Diabetes: A Propensity Score Analysis. The American journal of gastroenterology. 2016.
18. Chaiteerakij R, Petersen GM, Bamlet WR, Chaffee KG, Zhen DB, Burch PA, Leof ER, Roberts LR, Oberg AL. Metformin Use and Survival of Patients With Pancreatic Cancer: A Cautionary Lesson. Journal of clinical oncology. 2016; 34:1898-1904.
19. Ambe CM, Mahipal A, Fulp J, Chen L, Malafa MP. Effect of Metformin Use on Survival in Resectable Pancreatic Cancer: A Single-Institution Experience and Review of the Literature. PloS one. 2016; 11:e0151632.
20. Lee SH, Yoon SH, Lee HS, Chung MJ, Park JY, Park SW, Song SY, Chung JB, Bang S. Can metformin change the prognosis of pancreatic cancer? Retrospective study for pancreatic cancer patients with pre-existing diabetes mellitus type 2. Digestive and liver disease. 2016; 48:435-440.
21. Choi Y, Kim TY, Oh DY, Lee KH, Han SW, Im SA, Kim TY, Bang YJ. The Impact of Diabetes Mellitus and Metformin Treatment on Survival of Patients with Advanced Pancreatic Cancer Undergoing Chemotherapy. Cancer research and treatment. 2016; 48:171-179.
22. Hwang AL, Haynes K, Hwang WT, Yang YX. Metformin and survival in pancreatic cancer: a retrospective cohort study. Pancreas. 2013; 42:1054-1059.
23. Nakai Y, Isayama H, Sasaki T, Mizuno S, Sasahira N, Kogure H, Kawakubo K, Yamamoto N, Hirano K, Ijichi H, Tateishi K, Tada M, Koike K. Clinical outcomes of chemotherapy for diabetic and nondiabetic patients with pancreatic cancer: better prognosis with statin use in diabetic patients. Pancreas. 2013; 42:202-208.
24. Sadeghi N, Abbruzzese JL, Yeung SC, Hassan M, Li D. Metformin use is associated with better survival of diabetic patients with pancreatic cancer. Clinical cancer research. 2012; 18:2905-2912.
25. Currie CJ, Poole CD, Jenkins-Jones S, Gale EA, Johnson JA, Morgan CL. Mortality after incident cancer in people with and without type 2 diabetes: impact of metformin on survival. Diabetes care. 2012; 35:299-304.
26. Jo A, Kim Y, Kang S, Kim M, Ko M. The Effect Of Metformin Use And Mortality Among Those With Pancreatic Cancer And Type 2 Diabetes Mellitus: Findings From A Nationwide Population Retrospective Cohort Study. Value in health. 2015; 18:A439.
27. Reni M, Dugnani E, Cereda S, Belli C, Balzano G, Nicoletti R, Liberati D, Pasquale V, Scavini M, Maggiora P, Sordi V, Lampasona V, Ceraulo D, et al. (Ir)relevance of Metformin Treatment in Patients with Metastatic Pancreatic Cancer: An Open-Label, Randomized Phase II Trial. Clinical cancer research. 2016; 22:1076-1085.
28. Kordes S, Pollak MN, Zwinderman AH, Mathot RA, Weterman MJ, Beeker A, Punt CJ, Richel DJ, Wilmink JW. Metformin in patients with advanced pancreatic cancer: a double-blind, randomised, placebo-controlled phase 2 trial. The Lancet Oncology. 2015; 16:839-847.
29. Gullo L. Diabetes and the risk of pancreatic cancer. Annals of oncology. 1999; 10:79-81.
30. Pannala R, Leirness JB, Bamlet WR, Basu A, Petersen GM, Chari ST. Prevalence and clinical profile of pancreatic cancer-associated diabetes mellitus. Gastroenterology. 2008; 134:981-987.
31. Wang F, Herrington M, Larsson J, Permert J. The relationship between diabetes and pancreatic cancer. Molecular cancer. 2003; 2:4.
32. Huxley R, Ansary-Moghaddam A, Berrington de Gonzalez A, Barzi F, Woodward M. Type-II diabetes and pancreatic cancer: a meta-analysis of 36 studies. British journal of cancer. 2005; 92:2076-2083.
33. Senior K. Late-onset diabetes and the link with pancreatic cancer. The Lancet Oncology. 2005; 6:641.
34. Chari ST, Leibson CL, Rabe KG, Ransom J, de Andrade M, Petersen GM. Probability of pancreatic cancer following diabetes: a population-based study. Gastroenterology. 2005; 129:504-511.
35. Aung KL, Moore MJ. Metformin for pancreatic cancer. The Lancet Oncology. 2015; 16:748-749.
36. Ma SJ, Zheng YX, Zhou PC, Xiao YN, Tan HZ. Metformin use improves survival of diabetic liver cancer patients: systematic review and meta-analysis. Oncotarget. 2016; 7:66202-66211. doi: 10.18632/oncotarget.11033.
37. Wan G, Yu X, Chen P, Wang X, Pan D, Wang X, Li L, Cai X, Cao F. Metformin therapy associated with survival benefit in lung cancer patients with diabetes. Oncotarget. 2016; 7:35437-45. doi: 10.18632/oncotarget.8881.
38. Viollet B, Guigas B, Sanz Garcia N, Leclerc J, Foretz M, Andreelli F. Cellular and molecular mechanisms of metformin: an overview. Clin Sci (Lond). 2012; 122:253-270.
39. Picone P, Vilasi S, Librizzi F, Contardi M, Nuzzo D, Caruana L, Baldassano S, Amato A, Mule F, San Biagio PL, Giacomazza D, Di Carlo M. Biological and biophysics aspects of metformin-induced effects: cortex mitochondrial dysfunction and promotion of toxic amyloid pre-fibrillar aggregates. Aging (Albany NY). 2016; 8:1718-1734. doi: 10.18632/aging.101004.
40. Moiseeva O, Deschenes-Simard X, Pollak M, Ferbeyre G. Metformin, aging and cancer. Aging (Albany NY). 2013; 5:330-331. doi: 10.18632/aging.100556.
41. Gui DY, Sullivan LB, Luengo A, Hosios AM, Bush LN, Gitego N, Davidson SM, Freinkman E, Thomas CJ, Vander Heiden MG. Environment Dictates Dependence on Mitochondrial Complex I for NAD+ and Aspartate Production and Determines Cancer Cell Sensitivity to Metformin. Cell Metab. 2016; 24:716-727.
42. Liu X, Romero IL, Litchfield LM, Lengyel E, Locasale JW. Metformin Targets Central Carbon Metabolism and Reveals Mitochondrial Requirements in Human Cancers. Cell Metab. 2016; 24:728-739.
43. Hardie DG. AMP-activated protein kinase: a cellular energy sensor with a key role in metabolic disorders and in cancer. Biochem Soc Trans. 2011; 39:1-13.
44. Zhou G, Myers R, Li Y, Chen Y, Shen X, Fenyk-Melody J, Wu M, Ventre J, Doebber T, Fujii N, Musi N, Hirshman MF, Goodyear LJ, Moller DE. Role of AMP-activated protein kinase in mechanism of metformin action. The Journal of clinical investigation. 2001; 108:1167-1174.
45. Ben Sahra I, Laurent K, Loubat A, Giorgetti-Peraldi S, Colosetti P, Auberger P, Tanti JF, Le Marchand-Brustel Y, Bost F. The antidiabetic drug metformin exerts an antitumoral effect in vitro and in vivo through a decrease of cyclin D1 level. Oncogene. 2008; 27:3576-3586.
46. Blandino G, Valerio M, Cioce M, Mori F, Casadei L, Pulito C, Sacconi A, Biagioni F, Cortese G, Galanti S, Manetti C, Citro G, Muti P, Strano S. Metformin elicits anticancer effects through the sequential modulation of DICER and c-MYC. Nature communications. 2012; 3:865.
47. Anisimov VN. Metformin and rapamycin are master-keys for understanding the relationship between cell senescent, aging and cancer. Aging (Albany NY). 2013; 5:337-338. doi: 10.18632/aging.100561.
48. Wu L, Zhou B, Oshiro-Rapley N, Li M, Paulo JA, Webster CM, Mou F, Kacergis MC, Talkowski ME, Carr CE, Gygi SP, Zheng B, Soukas AA. An Ancient, Unified Mechanism for Metformin Growth Inhibition in C. elegans and Cancer. Cell. 2016; 167:1705-1718 e1713.
49. Cifarelli V, Lashinger LM, Devlin KL, Dunlap SM, Huang J, Kaaks R, Pollak MN, Hursting SD. Metformin and Rapamycin Reduce Pancreatic Cancer Growth in Obese Prediabetic Mice by Distinct MicroRNA-Regulated Mechanisms. Diabetes. 2015; 64:1632-1642.
50. Jiralerspong S, Palla SL, Giordano SH, Meric-Bernstam F, Liedtke C, Barnett CM, Hsu L, Hung MC, Hortobagyi GN, Gonzalez-Angulo AM. Metformin and pathologic complete responses to neoadjuvant chemotherapy in diabetic patients with breast cancer. Journal of clinical oncology. 2009; 27:3297-3302.
51. Koo YX, Tan DS, Tan IB, Tai DW, Ha T, Ong WS, Quek R, Tao M, Lim ST. Effect of concomitant statin, metformin, or aspirin on rituximab treatment for diffuse large B-cell lymphoma. Leukemia & lymphoma. 2011; 52:1509-1516.
52. Kumar S, Meuter A, Thapa P, Langstraat C, Giri S, Chien J, Rattan R, Cliby W, Shridhar V. Metformin intake is associated with better survival in ovarian cancer: a casecontrol study. Cancer. 2013; 119:555-562.
53. Nagi DK, Yudkin JS. Effects of metformin on insulin resistance, risk factors for cardiovascular disease, and plasminogen activator inhibitor in NIDDM subjects. A study of two ethnic groups. Diabetes care. 1993; 16:621-629.
54. Wells GASB OCD, Peterson J, Welch V, Losos M, Tugwell P. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses. Available from: http://www/ohrica/programs/clinical_epidemiology/oxfordhtm. cited 5 May 2012.
55. Woods BS, Hawkins N, Scott DA. Network meta-analysis on the log-hazard scale, combining count and hazard ratio statistics accounting for multi-arm trials: a tutorial. BMC medical research methodology. 2010; 10:54.
56. Kanwal F, White D. 'Systematic Reviews and Metaanalyses' in Clinical Gastroenterology and Hepatology. Clinical gastroenterology and hepatology. 2012; 10:1184-1186.
57. Begg CB, Mazumdar M. Operating characteristics of a rank correlation test for publication bias. Biometrics. 1994; 50:1088-1101.
58. Egger M, Davey Smith G, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. Bmj. 1997; 315:629-634.