Abstract
Summary
We performed a meta-analysis to evaluate the femoral neck and lumbar spine bone mineral density (BMD) in adults with type 1 diabetes (T1D) compared with controls. Adults with T1D have modestly lower BMD at femoral neck and lumbar spine than adults without diabetes.
Introduction
Fracture risk is four to sixfold higher in adults with T1D. Since BMD is one of the major contributors for fracture risk, we performed a meta-analysis to evaluate differences in femoral neck and lumbar spine BMD between adults with T1D and controls.
Methods
MEDLINE, Ovid, and the Cochrane library and abstracts from various scientific meetings were searched. Studies reporting the femoral neck and/or lumbar spine BMD in adults (age > 20 years) with T1D in comparison with people without diabetes were selected. General linear mixed models were used to assess differences in BMD at femoral neck and lumbar spine between subjects with T1D and controls adjusting for age, sex, and dual x-ray absorptiometry (DXA) instruments.
Results
Sixteen studies met the inclusion criteria. The femoral neck BMD was modestly lower in adults with T1D compared to controls (−0.055 g/cm2; 95% CI: −0.065, −0.045). There were no differences in lumbar spine BMD between adults with T1D and controls (0.0062 g/cm2; 95% CI −0.04, 0.016). However, in a sensitivity analysis, lumbar spine BMD was modestly lower in adults with T1D compared to controls (−0.035 g/cm2; −0.049, −0.02). Studies using Lunar DXA instruments have reported higher lumbar spine and femoral neck BMD compared to studies using Hologic DXA instruments.
Conclusion
Femoral neck and lumbar spine BMD were modestly lower in adults with T1D compared to controls. However, this modest reduction in femoral neck and lumbar spine BMD cannot explain much higher observed fracture risk in adults with T1D.
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References
Pambianco G, Costacou T, Ellis D et al (2006) The 30-year natural history of type 1 diabetes complications: the Pittsburgh Epidemiology of diabetes complications study experience. Diabetes 55:1463–1469
Harding JL, Shaw JE, Peeters A et al (2014) Mortality trends among people with type 1 and type 2 diabetes in Australia: 1997–2010. Diabetes Care 37:2579–2586
Dhaon P, Shah VN (2014) Type 1 diabetes and osteoporosis: a review of literature. Indian J Endocrinol Metab 18:159–165
Shah VN, Shah CS, Snell-Bergeon JK (2015) Risk for fracture in type 1 diabetes: a meta-analysis and review of the literature. Diabet Med 32:1134–1142
Miao J, Brismar K, Nyrén O, Ugarph-Morawski A, Ye W (2005) Elevated hip fracture risk in type 1 diabetic patients: a population-based cohort study in Sweden. Diabetes Care 28:2850–2855
Hothersall EJ, Livingstone SJ, Looker HC et al (2014) Contemporary risk of hip fracture in type 1 and type 2 diabetes: a national registry study from Scotland. J Bone Miner Res 29:1054–1060
Weber DR, Haynes K, Leonard MB, Willi SM, Denburg MR (2015) Type 1 diabetes is associated with an increased risk of fracture across the life span: a population-based cohort study using the health improvement network (THIN). Diabetes Care 38:1913–1920
Rivadeneira F, Zillikens MC, De Laet CE, Hofman A, Uitterlinden AG, Beck TJ, Pols HA (2007) Femoral neck BMD is a strong predictor of hip fracture susceptibility in elderly men and women because it detects cortical bone instability: the Rotterdam study. J Bone Miner Res 22:1781–1790
Kanis JA, Johnell O, Oden A, Dawson A, De Laet C, Jonsson B (2001) Ten year probabilities of osteoporotic fractures according to BMD and diagnostic thresholds. Osteoporos Int 12:989–995
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. doi:10.1186/1472-6823-14-33
Liu EY, Wactawski-Wende J, Donahue RP, Dmochowski J, Hovey KM, Quattrin T (2003) Does low bone mineral density start in post-teenage years in women with type 1 diabetes? Diabetes Care 8:2365–2369
Strotmeyer ES, Cauley JA, Orchard TJ, Steenkiste AR, Dorman JS (2006) Middle-aged premenopausal women with type 1 diabetes have lower bone mineral density and calcaneal quantitative ultrasound than nondiabetic women. Diabetes Care 29:306–311
Hedström EM, Svensson O, Bergström U, Michno P (2010) Epidemiology of fractures in children and adolescents: increased incidence over the past decade: a population-based study from northern Sweden. Acta Orthop 81:148–153
Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes—a meta-analysis. Osteoporos Int 18:427–444
Pan H, Wu N, Yang T, He W (2014) Association between bone mineral density and type 1 diabetes mellitus: a meta-analysis of cross-sectional studies. Diabetes Metab Res Rev 7:531–542
Tothill P, Avenell A, Reid DM (1994) Precision and accuracy of measurements of whole-body bone mineral: comparisons between Hologic, Lunar and Norland dual-energy X-ray absorptiometers. Br J Radiol 67:1210–1217
Tothill P, Fenner JA, Reid DM (1995) Comparisons between three dual-energy X-ray absorptiometers used for measuring spine and femur. Br J Radiol 68:621–629
Fan B, Lu Y, Genant H, Fuerst T, Shepherd J (2010) Does standardized BMD still remove differences between Hologic and GE-Lunar state-of-the-art DXA systems? Osteoporos Int 21:1227–1236
International Committee for Standards in Bone Measurement Standardization of proximal femur bone mineral density (BMD) measurements by DXA (1997) Bone 21:369–370
Moher D, Liberati A, Tetzlaff J, Altman DG, PRISMA Group (2009) Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151:264–269
Davies JH, Evans BA, Gregory JW (2005) Bone mass acquisition in healthy children. Arch Dis Child 90:373–378
Slade JM, Coe LM, Meyer RA, McCabe LR (2012) Human bone marrow adiposity is linked with serum lipid levels not T1-diabetes. J Diabetes Complicat 26:1–9
Neumann T, Sämann A, Lodes S, Kästner B, Franke S, Kiehntopf M, Hemmelmann C, Lehmann T, Müller UA, Hein G, Wolf G (2011) Glycaemic control is positively associated with prevalent fractures but not with bone mineral density in patients with Type 1 diabetes. Diabet Med 28:872–875
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. Diabet Med 26:45–52
Miazgowski T, Pynka S, Noworyta-Zietara M, Krzyzanowska-Swiniarska B, Pikul R (2007) Bone mineral density and hip structural analysis in type 1 diabetic men. Eur J Endocrinol 156:123–127
Ingberg CM, Palmér M, Aman J, Arvidsson B, Schvarcz E, Berne C (2004) Body composition and bone mineral density in long-standing type 1 diabetes. J Intern Med 255:392–398
Tuominen JT, Impivaara O, Puukka P, Rönnemaa T (1999) Bone mineral density in patients with type 1 and type 2 diabetes. Diabetes Care 22:1196–1200
Miazgowski T, Czekalski S (1998) A 2-year follow-up study on bone mineral density and markers of bone turnover in patients with long-standing insulin-dependent diabetes mellitus. Osteoporos Int 8:399–403
Hampson G, Evans C, Petitt RJ, Evans WD, Woodhead SJ, Peters JR, Ralston SH (1998) Bone mineral density, collagen type 1 alpha 1 genotypes and bone turnover in premenopausal women with diabetes mellitus. Diabetologia 41:1314–1320
Lunt H, Florkowski CM, Cundy T, Kendall D, Brown LJ, Elliot JR, Wells JE, Turner JG (1998) A population-based study of bone mineral density in women with longstanding type 1 (insulin dependent) diabetes. Diabetes Res Clin Pract 40:31–38
Rachoń D, Myśliwska J, Suchecka-Rachoń K, Semetkowska-Jurkiewicz B, Zorena K, Łysiak-Szydłowska W (2003) Serum interleukin-6 levels and bone mineral density at the femoral neck in post-menopausal women with Type 1 diabetes. Diabet Med 20:475–480
Rakic V, Davis WA, Chubb SA, Islam FM, Prince RL, Davis TM (2006) Bone mineral density and its determinants in diabetes: the Fremantle Diabetes Study. Diabetologia 49:863–871
Botushanov N, Yaneva M, Orbetzova M, Botushanova A (2014) Bone mineral density in bulgarian patients with type 1 diabetes mellitus. J Osteopor Phys Act 2:1. doi:10.4172/2329-9509.1000113
Gallacher SJ, Fenner JA, Fisher BM, Quin JD, Fraser WD, Logue FC, Cowan RA, Boyle IT, MacCuish AC (1993) An evaluation of bone density and turnover in premenopausal women with type 1 diabetes mellitus. Diabet Med 10:129–133
Shuster JJ, Jones LS, Salmon DA (2007) Fixed vs random effects meta-analysis in rare event studies: the rosiglitazone link with myocardial infarction and cardiac death. Stat Med 26:4375–4385
Kenward MG, Roger JH (1997) Small sample inference for fixed effects from restricted maximum likelihood. Biometrics 53:983–997
Farlay D, Armas LA Gineyts E, Akhter MP, Recker RR, Boivin G (2016) Nonenzymatic glycation and degree of mineralization are higher in bone from fractured patients with type 1 diabetes mellitus. J Bone Miner Res 31:190–195
The Diabetes Control and Complications Trial Research Group (1993) The effect of intensive treatment of diabetes on the development and progression of long-term complications in insulin-dependent diabetes mellitus. N Engl J Med 329:977–986
Nathan DM, Zinman B, Cleary PA et al (2009) Diabetes control and complications trial/epidemiology of diabetes interventions and complications (DCCT/EDIC) research group. Modern-day clinical course of type 1 diabetes mellitus after 30 years duration: the diabetes control and complications trial/epidemiology of diabetes interventions and complications and Pittsburgh epidemiology of diabetes complications experience (1983–2005). Arch Intern Med 169:1307–1316
Shanbhogue VV, Hansen S, Frost M, Jørgensen NR, Hermann AP, Henriksen JE, Brixen K (2015) Bone geometry, volumetric density, microarchitecture, and estimated bone strength assessed by HR-pQCT in adult patients with type 1 diabetes mellitus. J Bone Miner Res 30:2188–2199
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We acknowledge the help of Anne Caulfield for the critical review of the manuscript.
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Supplementary Table 1
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Supplemental Figure 1
Funnel Plot for assessment of publication bias for femoral neck BMD (JPEG 77 kb)
Supplemental Figure 2
Funnel Plot for assessment of publication bias for lumbar spine BMD (JPEG 76 kb)
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Shah, V.N., Harrall, K.K., Shah, C.S. et al. Bone mineral density at femoral neck and lumbar spine in adults with type 1 diabetes: a meta-analysis and review of the literature. Osteoporos Int 28, 2601–2610 (2017). https://doi.org/10.1007/s00198-017-4097-x
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DOI: https://doi.org/10.1007/s00198-017-4097-x