273
Views
0
CrossRef citations to date
0
Altmetric
ORIGINAL RESEARCH

Liraglutide in Combination with Insulin Has a Superior Therapeutic Effect to Either Alone on Fracture Healing in Diabetic Rats

ORCID Icon, , , & ORCID Icon
Pages 1235-1245 | Received 11 Jan 2023, Accepted 10 Apr 2023, Published online: 29 Apr 2023

References

  • Shaw JE, Sicree RA, Zimmet PZ. Global estimates of the prevalence of diabetes for 2010 and 2030. Diabetes Res Clin Pract. 2010;87(1):4–14. doi:10.1016/j.diabres.2009.10.007
  • Sun HX, Lu N, Luo X, Zhao L, Liu JM. Liraglutide, the glucagon-like peptide-1 receptor agonist, has anabolic bone effects in diabetic Goto-Kakizaki rats. J Diabetes. 2015;7(4):584–588. doi:10.1111/1753-0407.12282
  • Gortler H, Rusyn J, Godbout C, Chahal J, Schemitsch EH, Nauth A. Diabetes and healing outcomes in lower extremity fractures: a systematic review. Injury. 2018;49(2):177–183. doi:10.1016/j.injury.2017.11.006
  • Claes L, Recknagel S, Ignatius A. Fracture healing under healthy and inflammatory conditions. Nat Rev Rheumatol. 2012;8(3):133–143. doi:10.1038/nrrheum.2012.1
  • Napoli N, Chandran M, Pierroz DD, et al. Mechanisms of diabetes mellitus-induced bone fragility. Nat Rev Endocrinol. 2017;13(4):208–219. doi:10.1038/nrendo.2016.153
  • Koromani F, Ghatan S, van Hoek M, et al. Type 2 diabetes mellitus and vertebral fracture risk. Curr Osteoporos Rep. 2021;19(1):50–57. doi:10.1007/s11914-020-00646-8
  • Loi F, Cordova LA, Pajarinen J, Lin TH, Yao Z, Goodman SB. Inflammation, fracture and bone repair. Bone. 2016;86:119–130. doi:10.1016/j.bone.2016.02.020
  • Kayal RA, Alblowi J, McKenzie E, et al. Diabetes causes the accelerated loss of cartilage during fracture repair which is reversed by insulin treatment. Bone. 2009;44(2):357–363. doi:10.1016/j.bone.2008.10.042
  • Paglia DN, Wey A, Breitbart EA, et al. Effects of local insulin delivery on subperiosteal angiogenesis and mineralized tissue formation during fracture healing. J Orthop Res. 2013;31(5):783–791. doi:10.1002/jor.22288
  • Gandhi A, Beam HA, O’Connor JP, Parsons JR, Lin SS. The effects of local insulin delivery on diabetic fracture healing. Bone. 2005;37(4):482–490. doi:10.1016/j.bone.2005.04.039
  • Nuche-Berenguer B, Moreno P, Esbrit P, et al. Effect of GLP-1 treatment on bone turnover in normal, type 2 diabetic, and insulin-resistant states. Calcif Tissue Int. 2009;84(6):453–461. doi:10.1007/s00223-009-9220-3
  • Su B, Sheng H, Zhang M, et al. Risk of bone fractures associated with glucagon-like peptide-1 receptor agonists’ treatment: a meta-analysis of randomized controlled trials. Endocrine. 2015;48(1):107–115. doi:10.1007/s12020-014-0361-4
  • Huang CF, Mao TY, Hwang SJ. The effects of switching from dipeptidyl peptidase-4 Inhibitors to Glucagon-Like Peptide-1 receptor agonists on bone mineral density in diabetic patients. Diabetes Metab Syndr Obes. 2023;16:31–36. doi:10.2147/dmso.S389964
  • Yang L, Yang J, Pan T, Zhong X. Liraglutide increases bone formation and inhibits bone resorption in rats with glucocorticoid-induced osteoporosis. J Endocrinol Invest. 2019;42(9):1125–1131. doi:10.1007/s40618-019-01034-5
  • Srinivasan K, Viswanad B, Asrat L, Kaul CL, Ramarao P. Combination of high-fat diet-fed and low-dose streptozotocin-treated rat: a model for type 2 diabetes and pharmacological screening. Pharmacol Res. 2005;52(4):313–320. doi:10.1016/j.phrs.2005.05.004
  • Cao X, Xu P, Oyola MG, et al. Estrogens stimulate serotonin neurons to inhibit binge-like eating in mice. J Clin Invest. 2014;124(10):4351–4362. doi:10.1172/JCI74726
  • Wen B, Zhao L, Zhao H, Wang X. Liraglutide exerts a bone-protective effect in ovariectomized rats with streptozotocin-induced diabetes by inhibiting osteoclastogenesis. Exp Ther Med. 2018;15(6):5077–5083. doi:10.3892/etm.2018.6043
  • Bonnarens F, Einhorn TA. Production of a standard closed fracture in laboratory animal bone. J Orthop Res. 1984;2(1):97–101. doi:10.1002/jor.1100020115
  • Cao GL, Tian FM, Liu GY, et al. Strontium ranelate combined with insulin is as beneficial as insulin alone in treatment of fracture healing in ovariectomized diabetic rats. Med Sci Monit. 2018;24:6525–6536. doi:10.12659/MSM.911573
  • Liu GY, Cao GL, Tian FM, et al. Parathyroid hormone (1-34) promotes fracture healing in ovariectomized rats with type 2 diabetes mellitus. Osteoporos Int. 2017;28(10):3043–3053. doi:10.1007/s00198-017-4148-3
  • Schmidmaier G, Wildemann B, Cromme F, Kandziora F, Haas NP, Raschke M. Bone morphogenetic protein-2 coating of titanium implants increases biomechanical strength and accelerates bone remodeling in fracture treatment: a biomechanical and histological study in rats. Bone. 2002;30(6):816–822. doi:10.1016/s8756-3282(02)00740-8
  • Miao D, Scutt A. Recruitment, augmentation and apoptosis of rat osteoclasts in 1,25-(OH)2D3 response to short-term treatment with 1,25-dihydroxyvitamin D3 in vivo. BMC Musculoskelet Disord. 2002;3:16. doi:10.1186/1471-2474-3-16
  • Shifeng L, Hong X, Xue Y, et al. Ac-SDKP increases alpha-TAT 1 and promotes the apoptosis in lung fibroblasts and epithelial cells double-stimulated with TGF-beta1 and silica. Toxicol Appl Pharmacol. 2019;369:17–29. doi:10.1016/j.taap.2019.02.015
  • Komori T. Functions of osteocalcin in bone, pancreas, testis, and muscle. Int J Mol Sci. 2020;21:20. doi:10.3390/ijms21207513
  • Depalle B, McGilvery CM, Nobakhti S, Aldegaither N, Shefelbine SJ, Porter AE. Osteopontin regulates type I collagen fibril formation in bone tissue. Acta Bio. 2021;120:194–202. doi:10.1016/j.actbio.2020.04.040
  • Duan P, Bonewald LF. The role of the wnt/beta-catenin signaling pathway in formation and maintenance of bone and teeth. Int J Biochem Cell Biol. 2016;77:23–29. doi:10.1016/j.biocel.2016.05.015
  • Jiao H, Xiao E, Graves DT. Diabetes and Its Effect on Bone and Fracture Healing. Curr Osteoporos Rep. 2015;13(5):327–335. doi:10.1007/s11914-015-0286-8
  • Bai XC, Lu D, Bai J, et al. Oxidative stress inhibits osteoblastic differentiation of bone cells by ERK and NF-kappaB. Biochem Biophys Res Commun. 2004;314(1):197–207. doi:10.1016/j.bbrc.2003.12.073
  • Figeac F, Tencerova M, Ali D, et al. Impaired bone fracture healing in type 2 diabetes is caused by defective functions of skeletal progenitor cells. Stem Cells. 2022;40(2):149–164. doi:10.1093/stmcls/sxab011
  • Gonzalez Y, Herrera MT, Soldevila G, et al. High glucose concentrations induce TNF-α production through the down-regulation of CD33 in primary human monocytes. BMC Immunol. 2012;13:19. doi:10.1186/1471-2172-13-19
  • Picke AK, Gordaliza Alaguero I, Campbell GM, et al. Bone defect regeneration and cortical bone parameters of type 2 diabetic rats are improved by insulin therapy. Bone. 2016;82:108–115. doi:10.1016/j.bone.2015.06.001
  • Creecy A, Uppuganti S, Merkel AR, et al. Changes in the fracture resistance of bone with the progression of type 2 diabetes in the ZDSD rat. Calcif Tissue Int. 2016;99(3):289–301. doi:10.1007/s00223-016-0149-z
  • Eom YS, Gwon AR, Kwak KM, et al. Protective effects of vildagliptin against pioglitazone-induced bone loss in type 2 diabetic rats. PLoS One. 2016;11(12):e0168569. doi:10.1371/journal.pone.0168569
  • Lee NK, Sowa H, Hinoi E, et al. Endocrine regulation of energy metabolism by the skeleton. Cell. 2007;130(3):456–469. doi:10.1016/j.cell.2007.05.047
  • Komori T. Regulation of osteoblast differentiation by transcription factors. J Cell Biochem. 2006;99(5):1233–1239. doi:10.1002/jcb.20958
  • Julien A, Perrin S, Duchamp de Lageneste O, et al. FGFR3 in periosteal cells drives cartilage-to-bone transformation in bone repair. Stem Cell Rep. 2020;15(4):955–967. doi:10.1016/j.stemcr.2020.08.005
  • Kayal RA, Siqueira M, Alblowi J, et al. TNF-alpha mediates diabetes-enhanced chondrocyte apoptosis during fracture healing and stimulates chondrocyte apoptosis through FOXO1. J Bone Miner Res. 2010;25(7):1604–1615. doi:10.1016/j.stemcr.2020.08.005
  • Wong SA, Hu DP, Slocum J, et al. Chondrocyte-to-osteoblast transformation in mandibular fracture repair. J Orthop Res. 2021;39(8):1622–1632. doi:10.1002/jor.24904
  • Shi P, Hou A, Li C, et al. Continuous subcutaneous insulin infusion ameliorates bone structures and mechanical properties in type 2 diabetic rats by regulating bone remodeling. Bone. 2021;153:116101. doi:10.1016/j.bone.2021.116101
  • Hou K, Lin C, Wu B, et al. Exogenetic insulin increased bone mineral density in middle-aged male patients with type 2 diabetes mellitus. Pak J Pharm Sci. 2015;28(6 Suppl):2227–2230.
  • de Waard EAC, Driessen JHM, de Jong JJA, et al. The association between insulin use and volumetric bone mineral density, bone micro-architecture and bone strength of the distal radius in patients with type 2 diabetes - The Maastricht study. Bone. 2017;101:156–161. doi:10.1016/j.bone.2017.05.004
  • Hou CJ, Liu JL, Li X, Bi LJ. Insulin promotes bone formation in augmented maxillary sinus in diabetic rabbits. Int J Oral Maxillofac Surg. 2012;41(3):400–407. doi:10.1016/j.ijom.2011.10.004
  • Gilbert MP, Marre M, Holst JJ, et al. Comparison of the long-term effects of liraglutide and glimepiride monotherapy on bone mineral density in patients with type 2 diabetes. Endocr Pract. 2016;22(4):406–411. doi:10.4158/EP15758.OR
  • Lu N, Sun H, Yu J, et al. Glucagon-like peptide-1 receptor agonist Liraglutide has anabolic bone effects in ovariectomized rats without diabetes. PLoS One. 2015;10(7):e0132744. doi:10.1371/journal.pone.0132744
  • Ma X, Meng J, Jia M, et al. Exendin-4, a glucagon-like peptide-1 receptor agonist, prevents osteopenia by promoting bone formation and suppressing bone resorption in aged ovariectomized rats. J Bone Miner Res. 2013;28(7):1641–1652. doi:10.1002/jbmr.1898
  • Sassenrath K, Phillips BB, Stone RH. Evaluation of GLP-1 receptor agonists in combination with multiple daily insulin injections for type 2 diabetes. J Pharm Pract. 2022;35(6):979–990. doi:10.1177/08971900211010678
  • Hou HW, Xue P, Wang Y, Li YK. Liraglutide regulates proliferation, differentiation, and apoptosis of preosteoblasts through a signaling network of Notch/Wnt/Hedgehog signaling pathways. Eur Rev Med Pharmacol Sci. 2020;24(23):12408–12422. doi:10.26355/eurrev_202012_24037
  • Harris K, Nealy KL. The clinical use of a fixed-dose combination of insulin degludec and liraglutide (Xultophy 100/3.6) for the treatment of type 2 diabetes. Ann Pharmacother. 2018;52(1):69–77. doi:10.1177/1060028017726348
  • Wysham CH, Campos C, Kruger D. Safety and Efficacy of Insulin Degludec/Liraglutide (IDegLira) and Insulin Glargine U100/Lixisenatide (iGlarLixi), two novel co-formulations of a basal insulin and a glucagon-like peptide-1 receptor agonist, in patients with diabetes not adequately controlled on oral antidiabetic medications. Clin Diabetes. 2018;36(2):149–159. doi:10.2337/cd17-0064