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Published in: Osteoporosis International 1/2016

01-01-2016 | Original Article

The utility of lumbar spine trabecular bone score and femoral neck bone mineral density for identifying asymptomatic vertebral fractures in well-compensated type 2 diabetic patients

Authors: V. V. Zhukouskaya, C. Ellen-Vainicher, A. Gaudio, F. Privitera, E. Cairoli, F. M. Ulivieri, S. Palmieri, V. Morelli, V. Grancini, E. Orsi, B. Masserini, A. M. Spada, C. E. Fiore, I. Chiodini

Published in: Osteoporosis International | Issue 1/2016

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Abstract

Summary

The objective of the study was to evaluate the usefulness of trabecular bone score (TBS) and bone mineral density (BMD) for identifying vertebral fractures (VFx) in well-compensated type 2 diabetic (T2D) patients. TBS and femoral neck BMD below certain cutoffs may be useful for identifying VFx in well-compensated T2D patients.

Introduction

In T2D, the prevalence of VFx is increased, especially in poorly compensated and complicated diabetic patients. The possibility of predicting the fracture risk in T2D patients by measuring BMD and TBS, an indirect parameter of bone quality, is under debate. Therefore, the objective was to evaluate the usefulness of TBS and BMD for identifying VFx in well-compensated T2D patients.

Methods

Ninety-nine T2D postmenopausal women in good metabolic control (glycosylated haemoglobin 6.8 ± 0.7 %) and 107 control subjects without T2D were evaluated. In all subjects, we evaluated the following: the BMD at the lumbar spine (LS) and the femoral neck (FN); the TBS by dual X-ray absorptiometry; and VFx by radiography. In T2D subjects, the presence of diabetic retinopathy, neuropathy, and nephropathy was evaluated.

Results

T2D subjects had increased VFx prevalence (34.3 %) as compared to controls (18.7 %) (p = 0.01). T2D subjects presented higher BMD (LS −0.8 ± 1.44, FN −1.06 ± 1.08), as compared to controls (LS −1.39 ± 1.28, p = 0.002; FN −1.45 ± 0.91, p = 0.006, respectively). TBS was not different between diabetics and controls. In fractured T2D patients, LS-BMD, FN-BMD, and TBS were reduced (−1.2 ± 1.44; −1.44 ± 1.04; 1.072 ± 0.15) and the prevalence of retinopathy (15.4 %) was increased than in nonfractured T2D subjects (−0.59 ± 1.4, p = 0.035; −0.87 ± 1.05, p = 0.005; 1.159 ± 0.15, p = 0.006; 1.8 %, p = 0.04, respectively). The combination of TBS ≤1.130 and FN-BMD less than −1.0 had the best diagnostic accuracy for detecting T2D fractured patients (SP 73.8 %, SN 63.6 %, NPV 78.9 %, PPV 56.8 %).

Conclusions

TBS and FN-BMD below certain cutoffs may be useful for identifying VFx in well-compensated T2D patients.
Literature
1.
go back to reference Nicodemus KK, Folsom AR (2001) Iowa Women’s Health Study. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197PubMedCrossRef Nicodemus KK, Folsom AR (2001) Iowa Women’s Health Study. Type 1 and type 2 diabetes and incident hip fractures in postmenopausal women. Diabetes Care 24:1192–1197PubMedCrossRef
2.
go back to reference Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and 2 diabetes—a meta-analysis. Osteoporos Int 18:427–444PubMedCrossRef Vestergaard P (2007) Discrepancies in bone mineral density and fracture risk in patients with type 1 and 2 diabetes—a meta-analysis. Osteoporos Int 18:427–444PubMedCrossRef
3.
go back to reference Janghorbani M, Van Dam RM, Willett WC, Hu FB (2007) Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol 166:495–505PubMedCrossRef Janghorbani M, Van Dam RM, Willett WC, Hu FB (2007) Systematic review of type 1 and type 2 diabetes mellitus and risk of fracture. Am J Epidemiol 166:495–505PubMedCrossRef
4.
go back to reference Hofbauer LC, Brueck CC, Singh SK, Dobnig H (2007) Osteoporosis in patients with diabetes mellitus. J Bone Miner Res 22:1317–1328PubMedCrossRef Hofbauer LC, Brueck CC, Singh SK, Dobnig H (2007) Osteoporosis in patients with diabetes mellitus. J Bone Miner Res 22:1317–1328PubMedCrossRef
5.
go back to reference Vestergaard P, Rejnmark L, Mosekilde L (2009) Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcif Tissue Int 84:45–55PubMedCrossRef Vestergaard P, Rejnmark L, Mosekilde L (2009) Diabetes and its complications and their relationship with risk of fractures in type 1 and 2 diabetes. Calcif Tissue Int 84:45–55PubMedCrossRef
6.
go back to reference Hothersall EJ, Livingstone SJ, Looker HC, Ahmed SF, Cleland S, Leese GP, Lindsay RS, McKnight J, Pearson D, Philip S, Wild SH, Colhoun HM (2014) Contemporary risk of hip fracture in type 1 and type 2 diabetes: a national registry study from Scotland. J Bone Miner Res 29:1054–1060PubMedPubMedCentralCrossRef Hothersall EJ, Livingstone SJ, Looker HC, Ahmed SF, Cleland S, Leese GP, Lindsay RS, McKnight J, Pearson D, Philip S, Wild SH, Colhoun HM (2014) Contemporary risk of hip fracture in type 1 and type 2 diabetes: a national registry study from Scotland. J Bone Miner Res 29:1054–1060PubMedPubMedCentralCrossRef
7.
go back to reference Napoli N, Strotmeyer ES, Ensrud KE, Sellmeyer DE, Bauer DC, Hoffman AR, Dam TT, Barrett-Connor E, Palermo L, Orwoll ES, Cummings SR, Black DM, Schwartz AV (2014) Fracture risk in diabetic elderly men: the MrOS study. Diabetologia 57:2057–2065PubMedPubMedCentralCrossRef Napoli N, Strotmeyer ES, Ensrud KE, Sellmeyer DE, Bauer DC, Hoffman AR, Dam TT, Barrett-Connor E, Palermo L, Orwoll ES, Cummings SR, Black DM, Schwartz AV (2014) Fracture risk in diabetic elderly men: the MrOS study. Diabetologia 57:2057–2065PubMedPubMedCentralCrossRef
8.
go back to reference Schwartz AV, Vittinghoff E, Bauer DC, Hillier TA, Strotmeyer ES, Ensrud KE, Donaldson MG, Cauley JA, Harris TB, Koster A, Womack CR, Palermo L, Black DM (2011) Study of Osteoporotic Fractures (SOF) research group; Osteoporotic Fractures in Men (MrOS) research group; Health, Aging, and Body Composition (Health ABC) research group. Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA 305:2184–2192PubMedPubMedCentralCrossRef Schwartz AV, Vittinghoff E, Bauer DC, Hillier TA, Strotmeyer ES, Ensrud KE, Donaldson MG, Cauley JA, Harris TB, Koster A, Womack CR, Palermo L, Black DM (2011) Study of Osteoporotic Fractures (SOF) research group; Osteoporotic Fractures in Men (MrOS) research group; Health, Aging, and Body Composition (Health ABC) research group. Association of BMD and FRAX score with risk of fracture in older adults with type 2 diabetes. JAMA 305:2184–2192PubMedPubMedCentralCrossRef
9.
go back to reference Kanazawa I, Yamaguchi T, Yamamoto M, Yamauchi M, Yan S, Sugimoto T (2008) Combination of obesity with hyperglycemia is a risk factor for the presence of vertebral fractures in type 2 diabetic men. Calcif Tissue Int 83:324–331PubMedCrossRef Kanazawa I, Yamaguchi T, Yamamoto M, Yamauchi M, Yan S, Sugimoto T (2008) Combination of obesity with hyperglycemia is a risk factor for the presence of vertebral fractures in type 2 diabetic men. Calcif Tissue Int 83:324–331PubMedCrossRef
10.
go back to reference Oei L, Zillikens MC, Dehghan A, Buitendijk GHS, Castaño-Betancourt MC, Estrada K, Stolk L, Oei EHG, Van Meurs JBJ, Janssen JAMJL, Hofman A, van Leeuwen JPTM, Witteman JCM, Pols HAP, Uitterlinden AG, Klaver CCW, Franco OH, Rivadeneira F (2013) High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control. Diabetes Care 36(6):1619–1628PubMedPubMedCentralCrossRef Oei L, Zillikens MC, Dehghan A, Buitendijk GHS, Castaño-Betancourt MC, Estrada K, Stolk L, Oei EHG, Van Meurs JBJ, Janssen JAMJL, Hofman A, van Leeuwen JPTM, Witteman JCM, Pols HAP, Uitterlinden AG, Klaver CCW, Franco OH, Rivadeneira F (2013) High bone mineral density and fracture risk in type 2 diabetes as skeletal complications of inadequate glucose control. Diabetes Care 36(6):1619–1628PubMedPubMedCentralCrossRef
11.
go back to reference Viégas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F (2011) Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. J Diabetes Complicat 25:216–221PubMedCrossRef Viégas M, Costa C, Lopes A, Griz L, Medeiro MA, Bandeira F (2011) Prevalence of osteoporosis and vertebral fractures in postmenopausal women with type 2 diabetes mellitus and their relationship with duration of the disease and chronic complications. J Diabetes Complicat 25:216–221PubMedCrossRef
12.
go back to reference Kim JH, Jung MH, Lee JM, Son HS, Cha BY, Chang SA (2012) Diabetic peripheral neuropathy is highly associated with nontraumatic fractures in Korean patients with type 2 diabetes mellitus. Clin Endocrinol (Oxf) 77:51–55CrossRef Kim JH, Jung MH, Lee JM, Son HS, Cha BY, Chang SA (2012) Diabetic peripheral neuropathy is highly associated with nontraumatic fractures in Korean patients with type 2 diabetes mellitus. Clin Endocrinol (Oxf) 77:51–55CrossRef
13.
go back to reference Muñoz-Torres M, Reyes-García R, García-Martin A, Jiménez-Moleón JJ, Gonzalez-Ramírez AR, Lara-Villoslada MJ, Moreno PR (2013) Ischemic heart disease is associated with vertebral fractures in patients with type 2 diabetes mellitus. J Diabetes Investig 4:310–315PubMedPubMedCentralCrossRef Muñoz-Torres M, Reyes-García R, García-Martin A, Jiménez-Moleón JJ, Gonzalez-Ramírez AR, Lara-Villoslada MJ, Moreno PR (2013) Ischemic heart disease is associated with vertebral fractures in patients with type 2 diabetes mellitus. J Diabetes Investig 4:310–315PubMedPubMedCentralCrossRef
14.
go back to reference Kanis JA, McCloskey EV, Johansson H, Cooper C, Rizzoli R, Reginster JY, Scientific Advisory Board of the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO) and the Committee of Scientific Advisors of the International Osteoporosis Foundation (IOF) (2013) European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 24(1):23–57PubMedPubMedCentralCrossRef Kanis JA, McCloskey EV, Johansson H, Cooper C, Rizzoli R, Reginster JY, Scientific Advisory Board of the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO) and the Committee of Scientific Advisors of the International Osteoporosis Foundation (IOF) (2013) European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 24(1):23–57PubMedPubMedCentralCrossRef
15.
go back to reference Carnevale V, Morano S, Fontana A, Annese MA, Fallarino M, Filardi T, Copetti M, Pellegrini F, Romagnoli E, Eller-Vainicher C, Zhukouskaya VV, Chiodini I, D'Amico G (2014) Assessment of fracture risk by the FRAX algorithm in men and women with and without type 2 diabetes mellitus: a cross-sectional study. Diabetes Metab Res Rev 30:313–322PubMedCrossRef Carnevale V, Morano S, Fontana A, Annese MA, Fallarino M, Filardi T, Copetti M, Pellegrini F, Romagnoli E, Eller-Vainicher C, Zhukouskaya VV, Chiodini I, D'Amico G (2014) Assessment of fracture risk by the FRAX algorithm in men and women with and without type 2 diabetes mellitus: a cross-sectional study. Diabetes Metab Res Rev 30:313–322PubMedCrossRef
16.
go back to reference Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T (2007) Bone mineral density is not sensitive enough to assess the risk of vertebral fractures in type 2 diabetic women. Calcif Tissue Int 80:353–358PubMedCrossRef Yamamoto M, Yamaguchi T, Yamauchi M, Kaji H, Sugimoto T (2007) Bone mineral density is not sensitive enough to assess the risk of vertebral fractures in type 2 diabetic women. Calcif Tissue Int 80:353–358PubMedCrossRef
17.
go back to reference Yamamoto M, Yamaguchi T (2009) Diabetic patients have increased risk of vertebral fractures indipendent of BMD or diabetic complications. J Bone Miner Res 24:702–709PubMedCrossRef Yamamoto M, Yamaguchi T (2009) Diabetic patients have increased risk of vertebral fractures indipendent of BMD or diabetic complications. J Bone Miner Res 24:702–709PubMedCrossRef
18.
go back to reference Manavalan JS, Cremers S, Dempster DW, Zhou H, Dworakowski E, Kode A, Kousteni S, Rubin MR (2012) Circulating osteogenic precursor cells in type 2 diabetes mellitus. J Clin Endocrinol Metab 97:3240–3250PubMedPubMedCentralCrossRef Manavalan JS, Cremers S, Dempster DW, Zhou H, Dworakowski E, Kode A, Kousteni S, Rubin MR (2012) Circulating osteogenic precursor cells in type 2 diabetes mellitus. J Clin Endocrinol Metab 97:3240–3250PubMedPubMedCentralCrossRef
19.
go back to reference Bousson V, Bergot C, Sutter B, Levitz P, Cortet B, the Scientific Committee of the GRIO (Groupe de Recherche et d'Information sur les Ostéoporoses) (2012) Trabecular bone score (TBS): available knowledge, clinical relevance, and future prospects. Osteoporos Int 23:1489–1501PubMedCrossRef Bousson V, Bergot C, Sutter B, Levitz P, Cortet B, the Scientific Committee of the GRIO (Groupe de Recherche et d'Information sur les Ostéoporoses) (2012) Trabecular bone score (TBS): available knowledge, clinical relevance, and future prospects. Osteoporos Int 23:1489–1501PubMedCrossRef
20.
go back to reference Ulivieri FM, Silva BC, Sardanelli F, Hans D, Bilezikian JP, Caudarella R (2014) Utility of the trabecular bone score (TBS) in secondary osteoporosis. Endocrine 47:435–448PubMedCrossRef Ulivieri FM, Silva BC, Sardanelli F, Hans D, Bilezikian JP, Caudarella R (2014) Utility of the trabecular bone score (TBS) in secondary osteoporosis. Endocrine 47:435–448PubMedCrossRef
21.
go back to reference Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the dxa image. J Bone Miner Res 29:518–530PubMedCrossRef Silva BC, Leslie WD, Resch H, Lamy O, Lesnyak O, Binkley N, McCloskey EV, Kanis JA, Bilezikian JP (2014) Trabecular bone score: a noninvasive analytical method based upon the dxa image. J Bone Miner Res 29:518–530PubMedCrossRef
22.
go back to reference Leslie WD, Aubry-Rozier B, Lamy O, Hans D (2013) Manitoba Bone Density Program. TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98:602–609PubMedCrossRef Leslie WD, Aubry-Rozier B, Lamy O, Hans D (2013) Manitoba Bone Density Program. TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98:602–609PubMedCrossRef
23.
go back to reference Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM (2014) Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int 25:1969–1973PubMedCrossRef Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM (2014) Bone quality assessment in type 2 diabetes mellitus. Osteoporos Int 25:1969–1973PubMedCrossRef
24.
go back to reference Varenna M, Binelli L, Zucchi F, Ghiringhelli D, Sinigaglia L (2001) Unbalanced diet to lower serum cholesterol level is a risk factor for postmenopausal osteoporosis and distal forearm fracture. Osteoporos Int 12:296–301PubMedCrossRef Varenna M, Binelli L, Zucchi F, Ghiringhelli D, Sinigaglia L (2001) Unbalanced diet to lower serum cholesterol level is a risk factor for postmenopausal osteoporosis and distal forearm fracture. Osteoporos Int 12:296–301PubMedCrossRef
25.
go back to reference Eller-Vainicher C, Morelli V, Ulivieri FM, Palmieri S, Zhukouskaya VV, Cairoli E, Pino R, Naccarato A, Scillitani A, Beck-Peccoz P, Chiodini I (2012) Bone quality, as measured by Trabecular Bone Score, in patients with adrenal incidentalomas with and without subclinical hypercortisolism. J Bone Miner Res 27:2223–2230PubMedCrossRef Eller-Vainicher C, Morelli V, Ulivieri FM, Palmieri S, Zhukouskaya VV, Cairoli E, Pino R, Naccarato A, Scillitani A, Beck-Peccoz P, Chiodini I (2012) Bone quality, as measured by Trabecular Bone Score, in patients with adrenal incidentalomas with and without subclinical hypercortisolism. J Bone Miner Res 27:2223–2230PubMedCrossRef
26.
go back to reference Genant HK, Wu CY, van Knijk C, Nevitt M (1993) Vertebral fracture assessment using a semi-quantitative technique. J Bone Miner Res 8:1137–1148PubMedCrossRef Genant HK, Wu CY, van Knijk C, Nevitt M (1993) Vertebral fracture assessment using a semi-quantitative technique. J Bone Miner Res 8:1137–1148PubMedCrossRef
28.
go back to reference Schwartz AV, Ewing SK, Porzig AM, McCulloch CE, Resnick HE, Hillier TA, Ensrud KE, Black DM, Nevitt MC, Cummings SR, Sellmeyer DE (2013) Diabetes and change in bone mineral density at the hip, calcaneus, spine, and radius in older women. Front Endocrinol (Lausanne) 4:62PubMedCentral Schwartz AV, Ewing SK, Porzig AM, McCulloch CE, Resnick HE, Hillier TA, Ensrud KE, Black DM, Nevitt MC, Cummings SR, Sellmeyer DE (2013) Diabetes and change in bone mineral density at the hip, calcaneus, spine, and radius in older women. Front Endocrinol (Lausanne) 4:62PubMedCentral
29.
go back to reference Bates DW, Black DM, Cummings SR (2002) Clinical use of bone densitometry: clinical applications. JAMA 288:1898–1900PubMedCrossRef Bates DW, Black DM, Cummings SR (2002) Clinical use of bone densitometry: clinical applications. JAMA 288:1898–1900PubMedCrossRef
30.
go back to reference Eller-Vainicher C, Filopanti M, Palmieri S, Ulivieri FM, Morelli V, Zhukouskaya VV, Cairoli E, Pino R, Naccarato A, Verga U, Scillitani A, Beck-Peccoz P, Chiodini I (2013) Bone quality, as measured by trabecular bone score, in patients with primary hyperparathyroidism. Eur J Endocrinol 169:155–162PubMedCrossRef Eller-Vainicher C, Filopanti M, Palmieri S, Ulivieri FM, Morelli V, Zhukouskaya VV, Cairoli E, Pino R, Naccarato A, Verga U, Scillitani A, Beck-Peccoz P, Chiodini I (2013) Bone quality, as measured by trabecular bone score, in patients with primary hyperparathyroidism. Eur J Endocrinol 169:155–162PubMedCrossRef
31.
go back to reference Rabier B, Héraud A, Grand-Lenoir C, Winzenrieth R, Hans D (2010) A multicentre, retrospective case-control study assessing the role of trabecular bone score (TBS) in menopausal Caucasian women with low areal bone mineral density (BMDa): Analysing the odds of vertebral fracture. Bone 46(1):176–181PubMedCrossRef Rabier B, Héraud A, Grand-Lenoir C, Winzenrieth R, Hans D (2010) A multicentre, retrospective case-control study assessing the role of trabecular bone score (TBS) in menopausal Caucasian women with low areal bone mineral density (BMDa): Analysing the odds of vertebral fracture. Bone 46(1):176–181PubMedCrossRef
32.
go back to reference Winzenrieth R, Dufour R, Pothuaud L, Hans D (2010) A retrospective case-control study assessing the role of trabecular bone score in postmenopausal Caucasian women with osteopenia: analyzing the odds of vertebral fracture. Calcif Tissue Int 86(2):104–109PubMedCrossRef Winzenrieth R, Dufour R, Pothuaud L, Hans D (2010) A retrospective case-control study assessing the role of trabecular bone score in postmenopausal Caucasian women with osteopenia: analyzing the odds of vertebral fracture. Calcif Tissue Int 86(2):104–109PubMedCrossRef
33.
go back to reference Hans D, Goertzen AL, Krieg MA, Leslie WD (2011) Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res 26(11):2762–2769PubMedCrossRef Hans D, Goertzen AL, Krieg MA, Leslie WD (2011) Bone microarchitecture assessed by TBS predicts osteoporotic fractures independent of bone density: the Manitoba study. J Bone Miner Res 26(11):2762–2769PubMedCrossRef
Metadata
Title
The utility of lumbar spine trabecular bone score and femoral neck bone mineral density for identifying asymptomatic vertebral fractures in well-compensated type 2 diabetic patients
Authors
V. V. Zhukouskaya
C. Ellen-Vainicher
A. Gaudio
F. Privitera
E. Cairoli
F. M. Ulivieri
S. Palmieri
V. Morelli
V. Grancini
E. Orsi
B. Masserini
A. M. Spada
C. E. Fiore
I. Chiodini
Publication date
01-01-2016
Publisher
Springer London
Published in
Osteoporosis International / Issue 1/2016
Print ISSN: 0937-941X
Electronic ISSN: 1433-2965
DOI
https://doi.org/10.1007/s00198-015-3212-0

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