Increased Circulating Osteoprotegerin Levels in Type 1 Diabetes Mellitus: A Systematic Review and Meta-analysis Based on Observational Studies

References

• Abd El Dayem SM, El-Shehaby AM, Abd El Gafar A, Fawzy A, Salama H. 2011. Bone density, body composition, and markers of bone remodeling in type 1 diabetic patients. Scand J Clin Lab Invest. 71:387–93.
   PubMed Web of Science ®Google Scholar
• Alexopoulou O, Jamart J, Devogelaer JP, Brichard S, de Nayer P, Buysschaert M. 2006. Bone density and markers of bone remodeling in type 1 male diabetic patients. Diabetes Metab. 32:453–58.
   PubMed Web of Science ®Google Scholar
• Atkinson MA, Roep BO, Posgai A, Wheeler DCS, Peakman M. 2019. The challenge of modulating beta-cell autoimmunity in type 1 diabetes. Lancet Diabetes Endocrinol. 7:52–64.
   PubMed Web of Science ®Google Scholar
• Benslimane-Ahmim Z, Heymann D, Dizier B, Lokajczyk A, Brion R, Laurendeau I, Bieche I, Smadja DM, Galy-Fauroux I, Colliec-Jouault S, et al. 2011. Osteoprotegerin, a new actor in vasculogenesis, stimulates endothelial colony-forming cells properties. J Thromb Haemost. 9:834–43.
   PubMed Web of Science ®Google Scholar
• Bucay N, Sarosi I, Dunstan CR, Morony S, Tarpley J, Capparelli C, Scully S, Tan HL, Xu W, Lacey DL, et al. 1998. Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 12:1260–68.
   PubMed Web of Science ®Google Scholar
• Carnevale V, Romagnoli E, D’Erasmo E. 2004. Skeletal involvement in patients with diabetes mellitus. Diabetes Metab Res Rev. 20:196–204.
   PubMed Web of Science ®Google Scholar
• Chen M, Hu X, Wu M, Yang J, Han R, Ma Y, Zhang X, Yuan Y, Liu R, Wang M, et al. 2019. Serum levels of OPG, RANKL, and RANKL/OPG ratio in patients with Ankylosing spondylitis: a systematic review and meta-analysis. Immunol Invest. 48:490–504.
   PubMed Web of Science ®Google Scholar
• Chrysis D, Efthymiadou A, Mermigka A, Kritikou D, Spiliotis BE. 2017. Osteoprotegerin, RANKL, ADMA, and fetuin-A serum levels in children with type I diabetes mellitus. Pediatr Diabetes. 18:277–82.
   PubMed Web of Science ®Google Scholar
• Cunha JS, Ferreira VM, Maquigussa E, Naves MA, Boim MA. 2014. Effects of high glucose and high insulin concentrations on osteoblast function in vitro. Cell Tissue Res. 358:249–56.
   PubMed Web of Science ®Google Scholar
• Elsamahy MH, Elhenawy YI, Nawar MM. 2015. Plasma osteoprotegerin concentrations in type 1 diabetic patients with albuminuria. J Diabetes Complications. 29:563–67.
   PubMed Web of Science ®Google Scholar
• Fekih O, Triki H, Triki S, Neffati F, Chouchane S, Guediche MN, Najjar MF. 2017. Osteoprotegerin as a marker of cardiovascular risk in children and adolescents with type 1 diabetes. Pediatr Diabetes. 18:230–36.
   PubMed Web of Science ®Google Scholar
• Galluzzi F, Stagi S, Salti R, Toni S, Piscitelli E, Simonini G, Falcini F, Chiarelli F. 2005. Osteoprotegerin serum levels in children with type 1 diabetes: a potential modulating role in bone status. Eur J endocrinol/Eur Fed Endocr Soc. 153:879–85.
   PubMed Web of Science ®Google Scholar
• Glass DA 2nd, Bialek P, Ahn JD, Starbuck M, Patel MS, Clevers H, Taketo MM, Long F, McMahon AP, Lang RA, et al. 2005. Canonical Wnt signaling in differentiated osteoblasts controls osteoclast differentiation. Dev Cell. 8:751–64.
   PubMed Web of Science ®Google Scholar
• Heap J, Murray MA, Miller SC, Jalili T, Moyer-Mileur LJ. 2004. Alterations in bone characteristics associated with glycemic control in adolescents with type 1 diabetes mellitus. J Pediatr. 144:56–62.
   PubMed Web of Science ®Google Scholar
• Higgins JP, Thompson SG. 2002. Quantifying heterogeneity in a meta-analysis. Stat Med. 21:1539–58.
   PubMed Web of Science ®Google Scholar
• Hygum K, Starup-Linde J, Harslof T, Vestergaard P, Langdahl BL. 2017. Mechanisms in endocrinology: diabetes mellitus, a state of low bone turnover - a systematic review and meta-analysis. Eur J Endocrinol. 176:R137–R157.
   PubMed Web of Science ®Google Scholar
• Lambrinoudaki I, Tsouvalas E, Vakaki M, Kaparos G, Stamatelopoulos K, Augoulea A, Pliatsika P, Alexandrou A, Creatsa M, Karavanaki K, et al. 2013. Osteoprotegerin, soluble receptor activator of nuclear factor- kappa B ligand, and subclinical atherosclerosis in children and adolescents with type 1 diabetes mellitus. Int J Endocrinol. 2013:102120.
   PubMed Web of Science ®Google Scholar
• Lange U, Dischereit G, Tarner I, Frommer K, Neumann E, Müller-Ladner U, Kürten B. 2016. The impact of serial radon and hyperthermia exposure in a therapeutic adit on pivotal cytokines of bone metabolism in rheumatoid arthritis and osteoarthritis. Clin Rheumatol. 35:2783–88.
   PubMed Web of Science ®Google Scholar
• Lappin DF, Eapen B, Robertson D, Young J, Hodge PJ. 2009. Markers of bone destruction and formation and periodontitis in type 1 diabetes mellitus. J Clin Periodontol. 36:634–41.
   PubMed Web of Science ®Google Scholar
• Liu LN, Mao YM, Zhao CN, Wang H, Yuan -F-F, Li X-M, Pan H-F. 2019. Circulating levels of osteoprotegerin, osteocalcin and osteopontin in patients with rheumatoid arthritis: a systematic review and meta-analysis. Immunol Invest. 48:107–20.
   PubMed Web of Science ®Google Scholar
• Liu Z, Jiang H, Dong K, Liu S, Zhou W, Zhang J, Meng L, Rausch-FAN X, Xu X. 2015. Different concentrations of glucose regulate proliferation and osteogenic differentiation of osteoblasts via the PI3 kinase/Akt pathway. Implant Dent. 24:83–91.
   PubMed Web of Science ®Google Scholar
• Malyankar UM, Scatena M, Suchland KL, Yun TJ, Clark EA, Giachelli CM. 2000. Osteoprotegerin is an alpha vbeta 3-induced, NF-kappa B-dependent survival factor for endothelial cells. J Biol Chem. 275:20959–62.
   PubMed Web of Science ®Google Scholar
• Mrozikiewicz-Rakowska B, Nehring P, Szymanski K, Sobczyk-Kopcioł A, Płoski R, Drygas W, Krzymień J, Acharya NA, Czupryniak L, Przybyłkowski A, et al. 2018. Selected RANKL/RANK/OPG system genetic variants in diabetic foot patients. J Diabetes Metab Disord. 17:287–96.
   PubMed Web of Science ®Google Scholar
• Neumann T, Lodes S, Kastner B, Franke S, Kiehntopf M, Lehmann T, Müller UA, Wolf G, Sämann A. 2016. Osteocalcin, adipokines and their associations with glucose metabolism in type 1 diabetes. Bone. 82:50–55.
   PubMed Web of Science ®Google Scholar
• Pambianco G, Costacou T, Ellis D, Becker DJ, Klein R, Orchard TJ. 2006. The 30-year natural history of type 1 diabetes complications: the Pittsburgh epidemiology of diabetes complications study experience. Diabetes. 55:1463–69.
   PubMed Web of Science ®Google Scholar
• Patterson CC, Gyurus E, Rosenbauer J, Cinek O, Neu A, Schober E, Parslow RC, Joner G, Svensson J, Castell C, et al. 2012. Trends in childhood type 1 diabetes incidence in Europe during 1989–2008: evidence of non-uniformity over time in rates of increase. Diabetologia. 55:2142–47.
   PubMed Web of Science ®Google Scholar
• Rochette L, Meloux A, Rigal E, Zeller M, Malka G, Cottin Y, Vergely C. 2019. The role of osteoprotegerin in vascular calcification and bone metabolism: the basis for developing new therapeutics. Calcif Tissue Int. doi:10.1007/s00223-019-00573-6.
   PubMed Web of Science ®Google Scholar
• Shah VN, Carpenter RD, Ferguson VL, Schwartz AV. 2018. Bone health in type 1 diabetes. Curr Opin Endocrinol Diabetes Obes. 25:231–36.
   PubMedGoogle Scholar
• Shah VN, Shah CS, Snell-Bergeon JK. 2015. Type 1 diabetes and risk of fracture: meta-analysis and review of the literature. Diabet Med. 32:1134–42.
   PubMed Web of Science ®Google Scholar
• Siepi D, Marchesi S, Vaudo G, Lupattelli G, Bagaglia F, Pirro M, Brozzetti M, Roscini AR, Mannarino E. 2008. Preclinical vascular damage in white postmenopausal women: the relevance of osteoprotegerin. Metabolism. 57:321–25.
   PubMed Web of Science ®Google Scholar
• Singh DK, Winocour P, Summerhayes B, Viljoen A, Sivakumar G, Farrington K. 2010. Low serum osteoprotegerin levels in normoalbuminuric type 1 diabetes mellitus. Acta Diabetol. 47(Suppl 1):105–10.
   PubMed Web of Science ®Google Scholar
• Soedamah-Muthu SS, Fuller JH, Mulnier HE, Raleigh VS, Lawrenson RA, Colhoun HM. 2006. High risk of cardiovascular disease in patients with type 1 diabetes in the U.K.: a cohort study using the general practice research database. Diabetes Care. 29:798–804.
   PubMed Web of Science ®Google Scholar
• Thong EP, Herath M, Weber DR, Ranasinha S, Ebeling PR, Milat F, Teede H. 2018. Fracture risk in young and middle-aged adults with type 1 diabetes mellitus: A systematic review and meta-analysis. Clin Endocrinol (Oxf). 89:314–23.
   PubMed Web of Science ®Google Scholar
• Tsentidis C, Gourgiotis D, Kossiva L, Doulgeraki A, Marmarinos A, Galli-Tsinopoulou A, Karavanaki K. 2016. Higher levels of s-RANKL and osteoprotegerin in children and adolescents with type 1 diabetes mellitus may indicate increased osteoclast signaling and predisposition to lower bone mass: a multivariate cross-sectional analysis. Osteoporos Int. 27:1631–43.
   PubMed Web of Science ®Google Scholar
• Vistisen D, Andersen GS, Hansen CS, Hulman A, Henriksen JE, Bech-Nielsen H, Jørgensen ME. 2016. Prediction of first cardiovascular disease event in type 1 diabetes mellitus: the steno type 1 risk engine. Circulation. 133:1058–66.
   PubMed Web of Science ®Google Scholar
• Wajda J, Swiat M, Owczarek AJ, Holecki M, Duława J, Brzozowska A, Olszanecka-Glinianowicz M, Chudek J. 2019. Osteoprotegerin assessment improves prediction of mortality in stroke patients. J Stroke Cerebrovasc Dis. 28:1160–67.
   PubMed Web of Science ®Google Scholar
• Wan X, Wang W, Liu J, Tong T. 2014. Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol. 14:135.
   PubMed Web of Science ®Google Scholar
• Wang ST, Xu JM, Wang M, Chen FL, Ding G. 2013. Increased plasma osteoprotegerin concentrations in type 1 diabetes with albuminuria. Clin Nephrol. 79:192–98.
   PubMed Web of Science ®Google Scholar
• Wedrychowicz A, Stec M, Sztefko K, Starzyk JB. 2014. Associations between bone, fat tissue and metabolic control in children and adolescents with type 1 diabetes mellitus. Exp Clin Endocrinol Diabetes. 122:491–95.
   PubMed Web of Science ®Google Scholar
• Zobel EH, von Scholten BJ, Lajer M, Jorsal A, Tarnow L, Rasmussen LM, Holstein P, Parving -H-H, Hansen TW, Rossing P, et al. 2016. High osteoprotegerin is associated with development of foot ulcer in type 1 diabetes. J Diabetes Complications. 30:1603–08.
   PubMed Web of Science ®Google Scholar