Risk of bone fractures associated with glucagon-like peptide-1 receptor agonists’ treatment: a meta-analysis of randomized controlled trials

Endocrine

Volumn 48, Issue 1, 2015, Pages 107-115

  Su, Bin ^a   Sheng, Hui ^a   Zhang, Manna ^a   Bu, Le ^a   Yang, Peng ^a   Li, Liang ^a   Li, Fei ^a   Sheng, Chunjun ^a   Han, Yuqi ^a   Qu, Shen ^a   Wang, Jiying ^a  

^a TONGJI UNIVERSITY   (China)

Author keywords

Bone fracture; Exenatide; Glucagon Like Peptide 1; Liraglutide

Indexed keywords

ANTIDIABETIC AGENT; EXENDIN 4; GLP1R PROTEIN, HUMAN; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCAGON RECEPTOR; LIRAGLUTIDE; PEPTIDE; VENOM;

AGONISTS; ANALOGS AND DERIVATIVES; COMPLICATION; DIABETES MELLITUS, TYPE 2; FRACTURES, BONE; HUMAN; META ANALYSIS; RANDOMIZED CONTROLLED TRIAL (TOPIC); RISK;

DIABETES MELLITUS, TYPE 2; FRACTURES, BONE; GLUCAGON-LIKE PEPTIDE 1; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; HUMANS; HYPOGLYCEMIC AGENTS; LIRAGLUTIDE; PEPTIDES; RANDOMIZED CONTROLLED TRIALS AS TOPIC; RECEPTORS, GLUCAGON; RISK; VENOMS;

EID: 84939877452     PISSN: 1355008X     EISSN: 15590100     Source Type: Journal    
DOI: 10.1007/s12020-014-0361-4     Document Type: Article

References (51)

1. M. Janghorbani, R.M. Van Dam, W.C. Willett, F.B. Hu, Systematic Review of Type 1 and Type 2 Diabetes Mellitus and Risk of Fracture. Am. J. Epidemiol. 166(5), 495–505 (2007). doi:10.1093/aje/kwm106
2. C. Hamann, S. Kirschner, K.-P. Gunther, L.C. Hofbauer, Bone, sweet bone—osteoporotic fractures in diabetes mellitus. Nat. Rev. Endocrinol. 8(5), 297–305 (2012)
3. L.C. Hofbauer, C.C. Brueck, S.K. Singh, H. Dobnig, Osteoporosis in patients with diabetes mellitus. J. Bone Miner. Res. 22(9), 1317–1328 (2007)
4. M. Monami, B. Cresci, A. Colombini, L. Pala, D. Balzi et al., Bone Fractures and Hypoglycemic Treatment in Type 2 Diabetic Patients A case-control study. Diabetes Care 31(2), 199–203 (2008)
5. P. Vestergaard, L. Rejnmark, L. Mosekilde, Relative fracture risk in patients with diabetes mellitus, and the impact of insulin and oral antidiabetic medication on relative fracture risk. Diabetologia 48(7), 1292–1299 (2005)
6. S.E. Kahn, S.M. Haffner, M.A. Heise, W.H. Herman, R.R. Holman et al., Glycemic durability of rosiglitazone, metformin, or glyburide monotherapy. N. Engl. J. Med. 355(23), 2427–2443 (2006)
7. C. Meier, M.E. Kraenzlin, M. Bodmer, S.S. Jick, H. Jick et al., Use of thiazolidinediones and fracture risk. Arch. Intern. Med. 168(8), 820–825 (2008). doi:10.1001/archinte.168.8.820
8. M. Monami, I. Dicembrini, A. Antenore, E. Mannucci, Dipeptidyl Peptidase-4 Inhibitors and Bone Fractures: a meta-analysis of randomized clinical trials. Diabetes Care 34(11), 2474–2476 (2011). doi:10.2337/dc11-1099
9. R.A. DeFronzo, R.E. Ratner, J. Han, D.D. Kim, M.S. Fineman et al., Effects of exenatide (exendin-4) on glycemic control and weight over 30 weeks in metformin-treated patients with type 2 diabetes. Diabetes Care 28(5), 1092–1100 (2005)
10. T. Vilsboll, M. Zdravkovic, T. Le-Thi, T. Krarup, O. Schmitz et al., Liraglutide, a long-acting human glucagon-like peptide-1 analog, given as monotherapy significantly improves glycemic control and lowers body weight without risk of hypoglycemia in patients with type 2 diabetes. Diabetes Care 30(6), 1608–1610 (2007). doi:10.2337/dc06-2593
11. T. Vilsboll, M. Christensen, A.E. Junker, F.K. Knop, L.L. Gluud, Effects of glucagon-like peptide-1 receptor agonists on weight loss: systematic review and meta-analyses of randomised controlled trials. BMJ 344, d7771 (2012)
12. B. Wang, J. Zhong, H. Lin, Z. Zhao, Z. Yan et al., Blood pressure-lowering effects of GLP-1 receptor agonists exenatide and liraglutide: a meta-analysis of clinical trials. Diabetes Obes. Metab. 15(8), 737–749 (2013). doi:10.1111/dom.12085
13. M. Monami, I. Dicembrini, C. Nardini, I. Fiordelli, E. Mannucci, Effects of glucagon-like peptide-1 receptor agonists on cardiovascular risk: a meta-analysis of randomized clinical trials. Diabetes Obes. Metab. 16(1), 38–47 (2013). doi:10.1111/dom.12175
14. B. Gallwitz, Extra-pancreatic effects of incretin-based therapies. Endocrine (2014). doi:10.1007/s12020-014-0223-0
15. S.K. Majumdar, S.E. Inzucchi, Investigational anti-hyperglycemic agents: the future of type 2 diabetes therapy? Endocrine 44(1), 47–58 (2013). doi:10.1007/s12020-013-9884-3
16. C.B. Giorda, E. Nada, B. Tartaglino, Pharmacokinetics, safety, and efficacy of DPP-4 inhibitors and GLP-1 receptor agonists in patients with type 2 diabetes mellitus and renal or hepatic impairment. A systematic review of the literature. Endocrine (2014). doi:10.1007/s12020-014-0179-0
17. N. Mikhail, Effects of incretin-based therapy in patients with heart failure and myocardial infarction. Endocrine (2014). doi:10.1007/s12020-014-0175-4
18. G. Mabilleau, A. Mieczkowska, D. Chappard, Use of glucagon-like peptide-1 receptor agonists and bone fractures: A meta-analysis of randomized clinical trials. J Diabetes 6(3), 260–266 (2014). doi:10.1111/1753-0407.12102
19. D. Moher, A. Liberati, J. Tetzlaff, D.G. Altman, Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339(jul21 1), b2535-b2535 (2009). doi:10.1136/bmj.b2535
20. A.R. Jadad, R.A. Moore, D. Carroll, C. Jenkinson, D.J.M. Reynolds et al., Assessing the quality of reports of randomized clinical trials: Is blinding necessary? Control Clin. Trials 17(1), 1–12 (1996). doi:10.1016/0197-2456(95)00134-4
21. M.J. Bradburn, J.J. Deeks, J.A. Berlin, A. Russell Localio, Much ado about nothing: a comparison of the performance of meta-analytical methods with rare events. Stat. Med. 26(1), 53–77 (2007). doi:10.1002/sim.2528
22. M. Egger, G.D. Smith, M. Schneider, C. Minder, Bias in meta-analysis detected by a simple, graphical test. BMJ 315(7109), 629–634 (1997)
23. C.B. Begg, M. Mazumdar, Operating characteristics of a rank correlation test for publication bias. Biometrics 50, 1088–1101 (1994)
24. M. Nauck, A. Frid, K. Hermansen, A.B. Thomsen, M. During et al., Long-term efficacy and safety comparison of liraglutide, glimepiride and placebo, all in combination with metformin in type 2 diabetes: 2-year results from the LEAD-2 study. Diabetes Obes. Metab. 15(3), 204–212 (2013). doi:10.1111/dom.12012
25. A. Garber, R.R. Henry, R. Ratner, P. Hale, C.T. Chang et al., Liraglutide, a once-daily human glucagon-like peptide 1 analogue, provides sustained improvements in glycaemic control and weight for 2 years as monotherapy compared with glimepiride in patients with type 2 diabetes. Diabetes Obes. Metab. 13(4), 348–356 (2011). doi:10.1111/j.1463-1326.2010.01356.x
26. J.B. Buse, J. Rosenstock, G. Sesti, W.E. Schmidt, E. Montanya et al., Liraglutide once a day versus exenatide twice a day for type 2 diabetes: a 26-week randomised, parallel-group, multinational, open-label trial (LEAD-6). Lancet 374(9683), 39–47 (2009). doi:10.1016/s0140-6736(09)60659-0
27. R. Pratley, M. Nauck, T. Bailey, E. Montanya, R. Cuddihy et al., One year of liraglutide treatment offers sustained and more effective glycaemic control and weight reduction compared with sitagliptin, both in combination with metformin, in patients with type 2 diabetes: a randomised, parallel-group, open-label trial. Int. J. Clin. Pract. 65(4), 397–407 (2011). doi:10.1111/j.1742-1241.2011.02656.x
28. M.E. Lean, R. Carraro, N. Finer, H. Hartvig, M.L. Lindegaard et al., Tolerability of nausea and vomiting and associations with weight loss in a randomized trial of liraglutide in obese, non-diabetic adults. Int J Obes (Lond) (2013). doi:10.1038/ijo.2013.149
29. B. Charbonnel, H. Steinberg, E. Eymard, L. Xu, P. Thakkar et al., Efficacy and safety over 26 weeks of an oral treatment strategy including sitagliptin compared with an injectable treatment strategy with liraglutide in patients with type 2 diabetes mellitus inadequately controlled on metformin: a randomised clinical trial. Diabetologia 56(7), 1503–1511 (2013). doi:10.1007/s00125-013-2905-1
30. J.B. Buse, M. Nauck, T. Forst, W.H.H. Sheu, S.K. Shenouda et al., Exenatide once weekly versus liraglutide once daily in patients with type 2 diabetes (DURATION-6): a randomised, open-label study. Lancet 381(9861), 117–124 (2013)
31. NCT00614120: Effect of Liraglutide or Glimepiride Added to Metformin on Blood Glucose Control in Subjects With Type 2 Diabetes. http://www.clinicaltrials.gov/show/NCT00614120. Accessed 02/01 2014
32. R.J. Heine, L.F. Van Gaal, D. Johns, M.J. Mihm, M.H. Widel et al., Exenatide versus insulin glargine in patients with suboptimally controlled type 2 diabetes: a randomized trial. Ann. Intern. Med. 143(8), 559–569 (2005)
33. M.A. Nauck, S. Duran, D. Kim, D. Johns, J. Northrup et al., A comparison of twice-daily exenatide and biphasic insulin aspart in patients with type 2 diabetes who were suboptimally controlled with sulfonylurea and metformin: a non-inferiority study. Diabetologia 50(2), 259–267 (2007). doi:10.1007/s00125-006-0510-2
34. A. Gill, B.J. Hoogwerf, J. Burger, S. Bruce, L. Macconell et al., Effect of exenatide on heart rate and blood pressure in subjects with type 2 diabetes mellitus: a double-blind, placebo-controlled, randomized pilot study. Cardiovasc Diabetol 9, 6 (2010). doi:10.1186/1475-2840-9-6
35. B. Gallwitz, M. Böhmer, T. Segiet, A. Mölle, K. Milek et al., Exenatide Twice Daily Versus Premixed Insulin Aspart 70/30 in Metformin-Treated Patients With Type 2 Diabetes: A randomized 26-week study on glycemic control and hypoglycemia. Diabetes Care 34(3), 604–606 (2011). doi:10.2337/dc10-1900
36. J.B. Buse, R.M. Bergenstal, L.C. Glass, C.R. Heilmann, M.S. Lewis et al., Use of twice-daily exenatide in Basal insulin-treated patients with type 2 diabetes: a randomized, controlled trial. Ann. Intern. Med. 154(2), 103–112 (2011). doi:10.7326/0003-4819-154-2-201101180-00300
37. B. Gallwitz, J. Guzman, F. Dotta, B. Guerci, R. Simo et al., Exenatide twice daily versus glimepiride for prevention of glycaemic deterioration in patients with type 2 diabetes with metformin failure (EUREXA): an open-label, randomised controlled trial. Lancet 379(9833), 2270–2278 (2012). doi:10.1016/s0140-6736(12)60479-6
38. N. Inagaki, Y. Atsumi, T. Oura, H. Saito, T. Imaoka, Efficacy and safety profile of exenatide once weekly compared with insulin once daily in Japanese patients with type 2 diabetes treated with oral antidiabetes drug(s): results from a 26-week, randomized, open-label, parallel-group, multicenter, noninferiority study. Clin Ther 34(9), 1892–1908 e1891 (2012). doi:10.1016/j.clinthera.2012.07.007
39. NCT00960661: A Trial Comparing Two Therapies: Basal Insulin/Glargine, Exenatide and Metformin Therapy (BET) or Basal Insulin/Glargine, Bolus Insulin Lispro and Metformin Therapy (BBT) in Subjects With Type 2 Diabetes http://www.clinicaltrials.gov/ct2/show/NCT00960661. Accessed 02/01 2014
40. C. Yamada, Y. Yamada, K. Tsukiyama, K. Yamada, N. Udagawa et al., The Murine Glucagon-Like Peptide-1 Receptor Is Essential for Control of Bone Resorption. Endocrinology 149(2), 574–579 (2008). doi:10.1210/en.2007-1292
41. B. Nuche-Berenguer, P. Moreno, S. Portal-Nuñez, S. Dapía, P. Esbrit, et al., Exendin-4 exerts osteogenic actions in insulin-resistant and type 2 diabetic states. Regul Pept 159(1–3), 61–66 (2010). doi:http://dx.doi.org/10.1016/j.regpep.2009.06.010
42. G. Mabilleau, A. Mieczkowska, N. Irwin, P.R. Flatt, D. Chappard, Optimal bone mechanical and material properties require a functional glucagon-like peptide-1 receptor. J. Endocrinol. 219(1), 59–68 (2013). doi:10.1530/joe-13-0146
43. M. Monami, N. Marchionni, E. Mannucci, Glucagon-like peptide-1 receptor agonists in type 2 diabetes: a meta-analysis of randomized clinical trials. Eur. J. Endocrinol. 160(6), 909–917 (2009). doi:10.1530/eje-09-0101
44. M.J. Jespersen, F.K. Knop, M. Christensen, GLP-1 agonists for type 2 diabetes: pharmacokinetic and toxicological considerations. Expert. Opin. Drug. Met. 9(1), 17–29 (2013). doi:10.1517/17425255.2013.731394
45. Y.M. Cui, X.H. Guo, D.M. Zhang, L.S. Tham, C.C. Tang et al., Pharmacokinetics, safety, and tolerability of single- and multiple-dose exenatide once weekly in Chinese patients with type 2 diabetes mellitus. J Diabetes 5(2), 127–135 (2013). doi:10.1111/1753-0407.12020
46. M. Malm-Erjefält, I. Bjørnsdottir, J. Vanggaard, H. Helleberg, U. Larsen et al., Metabolism and excretion of the once-daily human glucagon-like peptide-1 analog liraglutide in healthy male subjects and its in vitro degradation by dipeptidyl peptidase iv and neutral endopeptidase. Drug Metab. Dispos. 38(11), 1944–1953 (2010). doi:10.1124/dmd.110.034066
47. J.B. Buse, A. Garber, J. Rosenstock, W.E. Schmidt, J.H. Brett et al., Liraglutide treatment is associated with a low frequency and magnitude of antibody formation with no apparent impact on glycemic response or increased frequency of adverse events: results from the Liraglutide Effect and Action in Diabetes (LEAD) trials. J. Clin. Endocrinol. Metab. 96(6), 1695–1702 (2011). doi:10.1210/jc.2010-2822
48. J.A. Langlois, M.E. Mussolino, M. Visser, A.C. Looker, T. Harris et al., Weight loss from maximum body weight among middle-aged and older white women and the risk of hip fracture: the NHANES I epidemiologic follow-up study. Osteoporos. Int. 12(9), 763–768 (2001). doi:10.1007/s001980170053
49. L. Oei, M.C. Zillikens, A. Dehghan, G.H.S. Buitendijk, M.C. Castaño-Betancourt et al., High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control: the Rotterdam Study. Diabetes Care 36(6), 1619–1628 (2013). doi:10.2337/dc12-1188
50. S.S. Johnston, C. Conner, M. Aagren, K. Ruiz, J. Bouchard, Association between hypoglycaemic events and fall-related fractures in Medicare-covered patients with type 2 diabetes. Diabetes Obes. Metab. 14(7), 634–643 (2012). doi:10.1111/j.1463-1326.2012.01583.x
51. A. Montagnani, S. Gonnelli, Antidiabetic therapy effects on bone metabolism and fracture risk. Diabetes Obes. Metab. 15(9), 784–791 (2013). doi:10.1111/dom.12077