This study aimed to compare the bone mineral densities (BMDs) among male patients with latent autoimmune diabetes in adults (LADA), classical type 1 diabetes (T1DM), and type 2 diabetes (T2DM), and to examine the risk factors for developing low BMD in these patients.
Patients and methods
Between January 2017 and October 2020, a total of 57, 67, and 223 male patients with LADA, classical T1DM, and T2DM, respectively, were recruited from the endocrinology department of Shanghai Tenth People’s Hospital. Hormonal markers of bone metabolism, lipid profiles, uric acid, glycosylated hemoglobin A1c (HbA1c), and beta-cell function were measured using blood samples. BMD was measured at the lumbar spine, femoral neck, and right hip by dual-energy X-ray absorptiometry.
The mean BMD values from all three skeletal sites in male patients with LADA were comparable to those with classical T1DM but were much lower than those with T2DM. After adjusting for confounding factors, multiple linear regression analysis demonstrated that in all male patients with diabetes, body mass index (BMI), uric acid, and fasting C-peptide showed significant positive associations with BMD at all three skeletal sites; however, osteocalcin showed a negative association at all three sites.
Compared with male patients with T2DM, lower BMDs were observed in patients with LADA and T1DM. Low BMI, uric acid, C-peptide levels, and high osteocalcin levels are risk factors for developing low BMD in male patients with diabetes.
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Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2diabetes–a meta-analysis. Osteoporos Int 18:427–444
Kurra S, Fink DA, Siris ES (2014a) Osteoporosis-associated fracture and diabetes. Endocrinol Metab Clin N Am 43:233–243
Adil C, Aydın T, Taşpınar Ö, Kızıltan H, Eriş AH, Hocaoglu IT, Poşul S, Kepekci M, Denizli E, Güler M (2015) Bone mineral density evaluation of patients with type 2 diabetes mellitus. J Phys Ther Sci 27:179–182
Kurra S, Fink DA, Siris ES (2014b) Osteoporosis, Fractures, and Diabetes. Endocrinol Metab Clin N Am 43:233–243
Liu B, Xiang Y, Liu Z, Zhou Z (2019) Past, present and future of latent autoimmune diabetes in adults. Diabetes Metab Res Rev 18:e3205
Yohena S, Penas-Steinhardt A, Muller C, Faccinetti NI, Cerrone GE, Lovecchio S, Ridner E, Valdez S, Frechtel G (2019) Immunological and clinical characteristics of latent autoimmune diabetes in the elderly. Diabetes Metab Res Rev 35:e3137
Hu Y, Li X, Yan X, Huang G, Dai R, Zhou Z (2020) Bone mineral density spectrum in individuals with type 1 diabetes, latent autoimmune diabetes in adults, and type 2 diabetes. Diabetes Metab Res Rev. https://doi.org/10.1002/dmrr.3390
Napoli N, Strollo R, Defeudis G, Leto G, Moretti C, Zampetti S, D’Onofrio L, Campagna G, Palermo A, Greto V, Manfrini S, Hawa MI, Leslie RD, Pozzilli P, Buzzetti R, NIRAD (NIRAD 10) and Action LADA Study Group (2018) Serum sclerostin and bone turnover in latent autoimmune diabetes in adults. J Clin Endocrinol Metab 103(5):1921–1928
Hamilton EJ, Rakic V, Davis WA, Chubb SA, Kamber N, Prince RL, Davis TM (2009) Prevalence and predictors of osteopenia and osteoporosis in adults with type 1 diabetes. Diabetes Med 26:45–52
De Shields SC, Cunningham TD (2018) Comparison of osteoporosis in adults with type 1 and type 2 diabetes mellitus. J Endocrinol Invest 41:1051–1060
Hosszúfalusi N, Vatay A, Rajczy K, Prohászka Z, Pozsonyi E, Horváth L, Grosz A, Gerõ L, Madácsy L, Romics L, Karádi I, Füst G, Pánczél P (2003) Similar genetic features and different islet cell autoantibody pattern of latent autoimmune diabetes in adults (LADA) compared with adult-onset type 1 diabetes with rapid progression. Diabetes Care 26:452–457
Gielen E, Vanderschueren D, Callewaert F, Boonen S (2011) Osteoporosis in men. Best Pract Res Clin Endocrinol Metab 25:321–335
Huuskonen J, Kröger H, Arnala I, Alhava D (1999) Characteristics of male hip fracture patients. Ann Chir Gynaecol 88:48–53
Hadjidakis DJ, Raptis AE, SfakianakisM MA, Raptis SA (2006) Bone mineral density of both genders in type 1 diabetes according to bone composition. J Diabetes Complicat 20:302–307
Palermo A, D’Onofrio L, Buzzetti R, Manfrini S, Napoli N (2017) Pathophysiology of bone fragility in patients with diabetes. Calcif Tissue Int 100:122–132
Fourlanos S, Dotta F, Greenbaum CJ, Palmer JP, Rolandsson O, Colman PG, Harrison LC (2005) Latent autoimmune diabetesin adults (LADA) should be less latent. Diabetologia 48:2206–2212
Yang W, Liu J, Shan Z, Tian H, Zhou Z, Ji Q (2014) Acarbose compared with metformin as initial therapy in patients with newly diagnosed type 2 diabetes: an open-label, non-inferiority randomised trial. Lancet Diabetes Endocrinol 2:46–55
Kanis JA, Melton LJ 3rd, Christiansen C, Johnston CC, Khaltaev N (1994) The diagnosis of osteoporosis. J Bone Miner Res 9:1137–1141
Leidig-Bruckner G, Grobholz S, Bruckner T, Scheidt-Nave C, Nawroth P, Schneider JG (2014) Prevalence and determinants of osteoporosis in patients with type 1 and type 2 diabetes mellitus. BMC Endocr Disord 14:33
Cree M, Soskolne CL, Belseck E, Hornig J, McElhaney JE, Brant R, Suarez-Almazor M (2000) Mortality and institutionalization following hip fracture. J Am Geriatr Soc 48:283–288
Chen HL, Deng LL, Li JF (2013) Prevalence of osteoporosis and its associated factors among older men with type 2 diabetes. Int J Endocrinol 2013:285729
Zhou Z, Xiang Y, Ji L, Jia W, Ning G, Huang G, Yang L, Lin J, Liu Z, Hagopian WA, Leslie RD, LADA China Study Group (2013) Frequency, immunogenetics, and clinical characteristics of latent autoimmune diabetes in China (LADA China study): nation-wide, multicenter, clinic-based cross-sectional study. Diabetes 62:543–550
Lu J, Hou X, Zhang L, Hu C, Zhou J, Pang C, Pan X, Bao Y, Jia W (2015) Associations between clinical characteristics and chronic complications in latent autoimmune diabetes in adults and type 2 diabetes. Diabetes Metab Res Rev 31:411–420
Pánczél P, Hosszúfalusi N, Bornemisza B, Hudes M, Flegal KM, Crawford PB (2001) Latent autoimmune diabetes in adults (LADA): part of the clinical spectrum of type-1 diabetes mellitus of autoimmune origin. Orv Hetil 142:2571–2578
Wang MC, Bachrach LK, Van Loan M, Yamwong S, Ratanachaiwong W, Sritara P (2005) The relative contributions of lean tissue mass and fat mass to bone density in young women. Bone 37:4744–4781
Barrera G, Bunout D, Gattás V, de la Maza MP, Leiva L, Hirsch S (2004) A high body mass index protects against femoral neck osteoporosis in healthy elderly subjects. Nutrition 20:769–771
Ahn SH, Lee SH, Kim BJ, Lim KH, Bae SJ, Kim EH, Kim HK, Choe JW, Koh JM, Kim GS (2013) Higher serum uric acid is associated with higher bone mass, lower bone turnover, and lower prevalence of vertebral fracture in healthy postmenopausal women. Osteoporos Int 24:2961–2970
Wu ZQ, Zhang Y, Xie E, Song WJ, Yang RX, Yan CJ, Zhang BF, Xu HG (2016) High uric acid (UA) negatively affects serumtartrate-resistant acid phosphatase 5b (TRACP 5b) immunoassay. PLoS ONE 11e:0147554
Li HZ, Chen Z, Hou CL, Tang YX, Wang F, Fu QG (2015) Uric acid promotes osteogenic differentiation and inhibits adipogenic differentiation of human bone mesenchymal stem cells. J Biochem Mol Toxicol 29:382–387
Reid IR, Evans MC, Cooper GJ, Ames RW, Stapleton J (1993) Circulating insulin levels are related to bone density in normal postmenopausal women. Am J Physiol 265:E655-659
Stolk RP, van Daele PL, Pols HA, Burger H, Hofman A, Birkenhäger JC, Lamberts SW, Grobbee D (1996) Hyperinsulinemia and bone mineral density in an elderly population: the Rotterdam study. Bone 18:545–549
Barrett-Connor E, Kritz-Silverstein D (1996) Does hyperinsulinemia preserve bone? Diabetes Care 19:1388–1392
Zhou Y, Li Y, Zhang D, Wang J, Yang H (2010) Prevalence and predictors of osteopenia and osteoporosis in postmenopausal Chinese women with type 2 diabetes. Diabetes Res Clin Pract 90:261–269
This study was supported by grants from the National Key R&D Program of China (No. 2018YFC1314100) and the National Nature Science Foundation (No. 81601269 and No.81700752).
Conflict of interest
The authors have no conflicts of interest.
All procedures performed in our study involving human participants were in accordance with the ethical standards of the institutional human subjects review board of the shanghai Tenth people’s hospital and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study.
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Zhang, M., Sheng, C., You, H. et al. Comparing the bone mineral density among male patients with latent autoimmune diabetes and classical type 1 and type 2 diabetes, and exploring risk factors for osteoporosis. J Endocrinol Invest (2021). https://doi.org/10.1007/s40618-020-01472-6
- Latent autoimmune diabetes in adults
- Classical type 1 diabetes
- Type 2 diabetes
- Bone mineral density