Comparative efficacy of anti-diabetic agents on nonalcoholic fatty liver disease in patients with type 2 diabetes mellitus: A systematic review and meta-analysis of randomized and non-randomized studies

Diabetes/Metabolism Research and Reviews

Volumn 32, Issue 2, 2016, Pages 200-216

  Tang, Wenjuan ^a   Xu, Qianyue ^a   Hong, Ting ^a   Tong, Guoyu ^a   Feng, Wenhuan ^a   Shen, Shanmei ^a   Bi, Yan ^a   Zhu, Dalong ^a  

^a THE AFFILIATED DRUM TOWER HOSPITAL OF NANJING UNIVERSITY MEDICAL SCHOOL   (China)

Author keywords

Anti diabetic agents; Meta analysis; Nonalcoholic fatty liver disease; Type 2 diabetes mellitus

Indexed keywords

2,4 THIAZOLIDINEDIONE DERIVATIVE; ANTIDIABETIC AGENT; DAPAGLIFLOZIN; GLUCAGON LIKE PEPTIDE 1 RECEPTOR AGONIST; INSULIN; METFORMIN; NATEGLINIDE; ORAL ANTIDIABETIC AGENT; SITAGLIPTIN;

ARTICLE; CLINICAL TRIAL (TOPIC); COMPARATIVE EFFECTIVENESS; DIABETIC PATIENT; DRUG EFFICACY; FAT CONTENT; HUMAN; LIVER HISTOLOGY; META ANALYSIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONALCOHOLIC FATTY LIVER; OBSERVATIONAL STUDY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL (TOPIC); SYSTEMATIC REVIEW; TREATMENT OUTCOME; COMPARATIVE STUDY; DIABETES MELLITUS, TYPE 2; NON-ALCOHOLIC FATTY LIVER DISEASE; PROGNOSIS;

CLINICAL TRIALS AS TOPIC; DIABETES MELLITUS, TYPE 2; HUMANS; HYPOGLYCEMIC AGENTS; NON-ALCOHOLIC FATTY LIVER DISEASE; PROGNOSIS;

EID: 84958168252     PISSN: 15207552     EISSN: 15207560     Source Type: Journal    
DOI: 10.1002/dmrr.2713     Document Type: Article

References (61)

1. Ratziu V, Bellentani S, Cortez-Pinto H, Day C, Marchesini G. A position statement on NAFLD/NASH based on the EASL 2009 special conference. J Hepatol 2010; 53(2): 372-384.
2. Guariguata L, Whiting DR, Hambleton I, Beagley J, Linnenkamp U, Shaw JE. Global estimates of diabetes prevalence for 2013 and projections for 2035. Diabetes Res Clin Pract 2014; 103(2): 137-149.
3. Ortiz-Lopez C, Lomonaco R, Orsak B, et al. Prevalence of prediabetes and diabetes and metabolic profile of patients with nonalcoholic fatty liver disease (NAFLD). Diabetes Care 2012; 35(4): 873-878.
4. Targher G, Bertolini L, Rodella S, et al. Non-alcoholic fatty liver disease is independently associated with an increased prevalence of chronic kidney disease and proliferative/laser-treated retinopathy in type 2 diabetic patients. Diabetologia 2008; 51(3): 444-450.
5. Lizardi-Cervera J, Aguilar-Zapata D. Nonalcoholic fatty liver disease and its association with cardiovascular disease. Ann Hepatol 2009; 8(Suppl 1): S40-S43.
6. Xiao J, Guo R, Fung ML, Liong EC, Tipoe GL. Therapeutic approaches to non-alcoholic fatty liver disease: past achievements and future challenges. Hepatobiliary Pancreat Dis Int 2013; 12(2): 125-135.
7. Smith SR, De Jonge L, Volaufova J, Li Y, Xie H, Bray GA. Effect of pioglitazone on body composition and energy expenditure: a randomized controlled trial. Metabolism 2005; 54(1): 24-32.
8. Cusi K, Orsak B, Lomonaco R, Bril F. Extended treatment with pioglitazone improves liver histology in patients with prediabetes or type 2 diabetes mellitus and NASH. Hepatology 2013; 58(4 (SUPPL)): 248A.
9. Belfort R, Harrison SA, Brown K, et al. A placebo-controlled trial of pioglitazone in subjects with nonalcoholic steatohepatitis. N Engl J Med 2006; 355(22): 2297-2307.
10. Carey DG, Cowin GJ, Galloway GJ, et al. Effect of rosiglitazone on insulin sensitivity and body composition in type 2 diabetic patients [corrected]. Obes Res 2002; 10(10): 1008-1015.
11. Borra R, Lautamäki R, Parkkola R, et al. Inverse association between liver fat content and hepatic glucose uptake in patients with type 2 diabetes mellitus. Metab Clin Exp 2008; 57(10): 1445-1451.
12. Shah PK, Mudaliar S, Chang AR, et al. Effects of intensive insulin therapy alone and in combination with pioglitazone on body weight, composition, distribution and liver fat content in patients with type 2 diabetes. Diabetes Obes Metab 2011; 13(6): 505-510.
13. Zib I, Jacob AN, Lingvay I, et al. Effect of pioglitazone therapy on myocardial and hepatic steatosis in insulin-treated patients with type 2 diabetes. J Investig Med 2007; 55(5): 230-236.
14. Katoh S, Hata S, Matsushima M, et al. Troglitazone prevents the rise in visceral adiposity and improves fatty liver associated with sulfonylurea therapy - a randomized controlled trial. Metabolism 2001; 50(4): 414-417.
15. Sathyanarayana P, Jogi M, Muthupillai R, Krishnamurthy R, Samson SL, Bajaj M. Effects of combined exenatide and pioglitazone therapy on hepatic fat content in type 2 diabetes. Obesity (Silver Spring) 2011; 19(12): 2310-2315.
16. Jendle J, Nauck MA, Matthews DR, et al. Weight loss with liraglutide, a once-daily human glucagon-like peptide-1 analogue for type 2 diabetes treatment as monotherapy or added to metformin, is primarily as a result of a reduction in fat tissue. Diabetes Obes Metab 2009; 11(12): 1163-1172.
17. Jadad AR, Moore RA, Carroll D, et al. Assessing the quality of reports of randomized clinical trials: is blinding necessary? Control Clin Trials 1996; 17(1): 1-12.
18. Schulz KF, Chalmers I, Hayes RJ, Altman DG. Empirical evidence of bias. Dimensions of methodological quality associated with estimates of treatment effects in controlled trials. JAMA 1995; 273(5): 408-412.
19. Wells GA, Shea B, O'Connell D, Peterson J, Welch V, M L. The Newcastle-Ottawa Scale (NOS) for assessing the quality of non-randomized studies in meta-analysis. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
20. Hozo SP, Djulbegovic B, Hozo I. Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 2005; 5: 13.
21. Higgins JP, Thompson SG. Quantifying heterogeneity in a meta-analysis. Stat Med 2002; 21(11): 1539-1558.
22. Gupta AK, Bray GA, Greenway FL, Martin CK, Johnson WD, Smith SR. Pioglitazone, but not metformin, reduces liver fat in type-2 diabetes mellitus independent of weight changes. J Diabetes Complications 2009; 24(5): 289-296.
23. Jonker JT, Wang Y, Haan WD, et al. Pioglitazone decreases plasma cholesteryl ester transfer protein mass, associated with a decrease in hepatic triglyceride content, in patients with type 2 diabetes. Diabetes Care 2010; 33(7): 1625-1628.
24. Tiikkainen M, Hakkinen AM, Korsheninnikova E, Nyman T, Makimattila S, Yki-Jarvinen H. Effects of rosiglitazone and metformin on liver fat content, hepatic insulin resistance, insulin clearance, and gene expression in adipose tissue in patients with type 2 diabetes. Diabetes 2004; 53(8): 2169-2176.
25. Omer Z, Cetinkalp S, Akyildiz M, et al. Efficacy of insulin-sensitizing agents in nonalcoholic fatty liver disease. Eur J Gastroenterol Hepatol 2010; 22(1): 18-23.
26. Maffioli P, Fogari E, D'Angelo A, Perrone T, Derosa G. Ultrasonography modifications of visceral and subcutaneous adipose tissue after pioglitazone or glibenclamide therapy combined with rosuvastatin in type 2 diabetic patients not well controlled by metformin. Eur J Gastroenterol Hepatol 2013; 25(9): 1113-1122.
27. Lingvay I, Roe ED, Duong J, Leonard D, Szczepaniak LS. Effect of insulin versus triple oral therapy on the progression of hepatic steatosis in type 2 diabetes. J Investig Med 2012; 60(7): 1059-1063.
28. Bolinder J, Ljunggren O, Kullberg J, et al. Effects of dapagliflozin on body weight, total fat mass, and regional adipose tissue distribution in patients with type 2 diabetes mellitus with inadequate glycemic control on metformin. J Clin Endocrinol Metab 2012; 97(3): 1020-1031.
29. Bi Y, Zhang B, Xu W, et al. Effects of exenatide, insulin, and pioglitazone on liver fat content and body fat distributions in drug-naive subjects with type 2 diabetes. Acta Diabetol 2014; 51(5): 865-873.
30. Morita Y, Ueno T, Sasaki N, et al. Nateglinide is useful for nonalcoholic steatohepatitis (NASH) patients with type 2 diabetes. Hepatogastroenterology 2005; 52(65): 1338-1343.
31. Mayerson AB, Hundal RS, Dufour S, et al. The effects of rosiglitazone on insulin sensitivity, lipolysis, and hepatic and skeletal muscle triglyceride content in patients with type 2 diabetes. Diabetes 2002; 51(3): 797-802.
32. Juurinen L, Kotronen A, Graner M, Yki-Jarvinen H. Rosiglitazone reduces liver fat and insulin requirements and improves hepatic insulin sensitivity and glycemic control in patients with type 2 diabetes requiring high insulin doses. J Clin Endocrinol Metab 2008; 93(1): 118-124.
33. Bajaj M, Suraamornkul S, Pratipanawatr T, et al. Pioglitazone reduces hepatic fat content and augments splanchnic glucose uptake in patients with type 2 diabetes. Diabetes 2003; 52(6): 1364-1370.
34. Bajaj M, Suraamornkul S, Piper P, et al. Decreased plasma adiponectin concentrations are closely related to hepatic fat content and hepatic insulin resistance in pioglitazone-treated type 2 diabetic patients. J Clin Endocrinol Metab 2004; 89(1): 200-206.
35. Bajaj M, Suraamornkul S, Hardies LJ, Pratipanawatr T, DeFronzo RA. Plasma resistin concentration, hepatic fat content, and hepatic and peripheral insulin resistance in pioglitazone-treated type II diabetic patients. Int J Obes Relat Metab Disord 2004; 28(6): 783-789.
36. Ravikumar B, Gerrard J, Dalla Man C, et al. Pioglitazone decreases fasting and postprandial endogenous glucose production in proportion to decrease in hepatic triglyceride content. Diabetes 2008; 57(9): 2288-2295.
37. Teranishi T, Ohara T, Maeda K, et al. Effects of pioglitazone and metformin on intracellular lipid content in liver and skeletal muscle of individuals with type 2 diabetes mellitus. Metab Clin Exp 2007; 56(10): 1418-1424.
38. Tushuizen ME, Bunck MC, Pouwels PJ, et al. Incretin mimetics as a novel therapeutic option for hepatic steatosis. Liver Int 2006; 26: 1015-1017.
39. Kenny PR, Brady DE, Torres DM, Ragozzino L, Chalasani N, Harrison SA. Exenatide in the treatment of diabetic patients with non-alcoholic steatohepatitis: a case series. Am J Gastroenterol 2010; 105(12): 2707-2709.
40. Suzuki D, Toyoda M, Kimura M, et al. Effects of liraglutide, a human glucagon-like peptide-1 analogue, on body weight, body fat area and body fat-related markers in patients with type 2 diabetes mellitus. Intern Med 2013; 52(10): 1029-1034.
41. Cuthbertson DJ, Irwin A, Gardner CJ, et al. Improved glycaemia correlates with liver fat reduction in obese, type 2 diabetes, patients given glucagon-like peptide-1 (GLP-1) receptor agonists. PLoS One 2012; 7(12e50117).
42. Yilmaz Y, Yonal O, Deyneli O, Celikel CA, Kalayci C, Duman DG. Effects of sitagliptin in diabetic patients with nonalcoholic steatohepatitis. Acta Gastroenterol Belg 2012; 75(2): 240-244.
43. Juurinen L, Tiikkainen M, Hakkinen AM, Hakkarainen A, Yki-Jarvinen H. Effects of insulin therapy on liver fat content and hepatic insulin sensitivity in patients with type 2 diabetes. Am J Physiol Endocrinol Metab 2007; 292(3): E829-E835.
44. Lingvay I, Raskin P, Szczepaniak LS. Effect of insulin-metformin combination on hepatic steatosis in patients with type 2 diabetes. J Diabetes Complications 2007; 21(3): 137-142.
45. Yamauchi T, Kamon J, Minokoshi Y, et al. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase. Nat Med 2002; 8(11): 1288-1295.
46. Ding X, Saxena NK, Lin S, Gupta NA, Anania FA. Exendin-4, a glucagon-like protein-1 (GLP-1) receptor agonist, reverses hepatic steatosis in ob/ob mice. Hepatology 2006; 43(1): 173-181.
47. Xu F, Li Z, Zheng X, et al. SIRT1 mediates the effect of GLP-1 receptor agonist exenatide on ameliorating hepatic steatosis. Diabetes 2014; 63(11): 3637-3646.
48. Ben-Shlomo S, Zvibel I, Shnell M, et al. Glucagon-like peptide-1 reduces hepatic lipogenesis via activation of AMP-activated protein kinase. J Hepatol 2011; 54(6): 1214-1223.
49. Fukuhara T, Hyogo H, Ochi H, et al. Efficacy and safety of sitagliptin for the treatment of nonalcoholic fatty liver disease with type 2 diabetes mellitus. Hepatogastroenterology 2014; 61(130): 323-328.
50. Ohki T, Isogawa A, Iwamoto M, et al. The effectiveness of liraglutide in nonalcoholic fatty liver disease patients with type 2 diabetes mellitus compared to sitagliptin and pioglitazone. ScientificWorldJournal 2012; 2012: 496453.
51. He L, Sabet A, Djedjos S, et al. Metformin and insulin suppress hepatic gluconeogenesis through phosphorylation of CREB binding protein. Cell 2009; 137(4): 635-646.
52. Haukeland JW, Konopski Z, Eggesbo HB, et al. Metformin in patients with non-alcoholic fatty liver disease: a randomized, controlled trial. Scand J Gastroenterol 2009; 44(7): 853-860.
53. Byrne CD, Olufadi R, Bruce KD, Cagampang FR, Ahmed MH. Metabolic disturbances in non-alcoholic fatty liver disease. Clin Sci (Lond) 2009; 116(7): 539-564.
54. Musso G, Cassader M, Rosina F, Gambino R. Impact of current treatments on liver disease, glucose metabolism and cardiovascular risk in non-alcoholic fatty liver disease (NAFLD): a systematic review and meta-analysis of randomised trials. Diabetologia 2012; 55(4): 885-904.
55. Petersen KF, Dufour S, Befroy D, Lehrke M, Hendler RE, Shulman GI. Reversal of nonalcoholic hepatic steatosis, hepatic insulin resistance, and hyperglycemia by moderate weight reduction in patients with type 2 diabetes. Diabetes 2005; 54(3): 603-608.
56. Lim EL, Hollingsworth KG, Aribisala BS, Chen MJ, Mathers JC, Taylor R. Reversal of type 2 diabetes: normalisation of beta cell function in association with decreased pancreas and liver triacylglycerol. Diabetologia 2011; 54(10): 2506-2514.
57. Chatrath H, Vuppalanchi R, Chalasani N. Dyslipidemia in patients with nonalcoholic fatty liver disease. Semin Liver Dis 2012; 32(1): 22-29.
58. Choi CS, Savage DB, Kulkarni A, et al. Suppression of diacylglycerol acyltransferase-2 (DGAT2), but not DGAT1, with antisense oligonucleotides reverses diet-induced hepatic steatosis and insulin resistance. J Biol Chem 2007; 282(31): 22678-22688.
59. Yu XX, Murray SF, Pandey SK, et al. Antisense oligonucleotide reduction of DGAT2 expression improves hepatic steatosis and hyperlipidemia in obese mice. Hepatology 2005; 42(2): 362-371.
60. Porepa L, Ray JG, Sanchez-Romeu P, Booth GL. Newly diagnosed diabetes mellitus as a risk factor for serious liver disease. CMAJ 2010; 182(11): E526-E531.
61. Cali AM, De Oliveira AM, Kim H, et al. Glucose dysregulation and hepatic steatosis in obese adolescents: is there a link? Hepatology 2009; 49(6): 1896-1903.