Abstract
Summary
We recorded the results of areal bone mineral density (aBMD) and microarchitecture of the bone measured by trabecular bone score (TBS) in 416 glucocorticoid-treated men and women aged 40 years and older with or without fracture to 1104 controls. TBS better discriminated those with fracture compared to aBMD. These differences were the greatest in men.
Introduction
The aim of this study is to evaluate glucocorticoid (GC)-induced effects on areal bone mineral density (aBMD) and bone microarchitectural texture measured by trabecular bone score (TBS).
Methods
TBS and aBMD were evaluated at L1–L4 postero-anterior (PA) spine by dual X-ray absorptiometry (DXA) in 1520 men and women aged 40 years and over. Four hundred sixteen subjects who received GCs (≥5 mg/day, for ≥3 months) were matched with 1104 sex-, age-, and BMI-matched control subjects. Clinical data, osteoporotic fractures (OPF), and dietary habits were documented in the medical report.
Results
GC-treated patients were characterized by a significant decrease of TBS (1.267 vs. 1.298, p < 0.001) compared with control-matched subjects while no change in BMD was observed at any sites. These decreases were even more pronounced when fracture status was taken into account (1.222 vs. 1.298, p < 0.001). The odds ratio (OR) for TBS was 1.44 (1.095–1.89) for OPF, whereas no association was found for BMD at any sites (all p > 0.3). A similar effect on microarchitecture measured by TBS was seen by the presence of fracture as by the use of glucocorticoids. An influence on TBS by sex was also noted with a decrease in TBS of greater magnitude in men.
Conclusions
GC-treated individuals have a significant deterioration of bone microarchitectural texture as assessed by TBS which is more marked in those with OPF and in men. TBS seems to be more sensitive than aBMD for GC-related fracture detection and should be a good surrogate indicator of bone health in such secondary osteoporosis.
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References
Van Staa TP, Leufkens HG, Abenhaim L, Zhang B, Cooper C (2000) Use of oral corticosteroids and risk of fractures. J Bone Miner Res 15(6):1487–1494
Canalis E, Mazziotti G, Giustina A, Bilezikian JP (2007) Glucocorticoid-induced osteoporosis: pathophysiology and therapy. Osteoporos Int 18(10):1319–1328
Clowes JA, Peel N, Eastell R (2001) Glucocorticoid-induced osteoporosis. Curr Opin Rheumatol 13(4):326–332
Spreafico A, Frediani B, Francucci CM, Capperucci C, Chellini F, Galeazzi M (2008) Role of apoptosis in osteoporosis induced by glucocorticoids. J Endocrinol Investig 31(7):22–27
Weinstein RS, Wan C, Liu Q, Wang Y, Almeida M et al (2010) Endogenous glucocorticoids decrease skeletal angiogenesis, vascularity, hydration, and strength in aged mice. Aging Cell 9(2):147–161
Dalle Carbonare L, Arlot ME, Chavassieux PM, Roux JP et al (2001) Comparison of trabecular bone microarchitecture and remodeling in glucocorticoid-induced and postmenopausal osteoporosis. J Bone Miner Res 16(1):97–103
Manolagas SC, Weinstein RS (1999) New developments in the pathogenesis and treatment of steroid-induced osteoporosis. J Bone Miner Res 14(7):1061–1066
Reid IR, Heap SW (1990) Determinants of vertebral mineral density in patients receiving long-term glucocorticoid therapy. Arch Intern Med 150(12):2545–2548
Wetzsteon RJ, Shults J, Zemel BS, Gupta PU et al (2009) Divergent effects of glucocorticoids on cortical and trabecular compartment BMD in childhood nephrotic syndrome. J Bone Miner Res 24(3):503–513
Hall GM, Spector TD, Griffin AJ, Jawad AS et al (1993) The effect of rheumatoid arthritis and steroid therapy on bone density in postmenopausal women. Arthritis Rheum 36(11):1510–1516
Saario R, Sonninen P, Möttönen T, Viikari J, Toivanen A (1999) Bone mineral density of the lumbar spine in patients with advanced rheumatoid arthritis. Influence of functional capacity and corticosteroid use. Scand J Rheumatol 28(6):363–367
Kanis JA, Johansson H, Oden A, Johnell O, de Laet C et al (2004) A meta-analysis of prior corticosteroid use and fracture risk. J Bone Miner Res 19(6):893–899
Naganathan V, Jones G, Nash P, Nicholson G et al (2000) Vertebral fracture risk with long-term corticosteroid therapy: prevalence and relation to age, bone density, and corticosteroid use. Arch Intern Med 160(19):2917–2922
Rehman Q, Lang T, Modin G, Lane NE (2002) Quantitative computed tomography of the lumbar spine, not dual x-ray absorptiometry, is an independent predictor of prevalent vertebral fractures in postmenopausal women with osteopenia receiving long-term glucocorticoid and hormone-replacement therapy. Arthritis Rheum 46(5):1292–1297
Van Staa TP, Laan RF, Barton IP, Cohen S et al (2003) Bone density threshold and other predictors of vertebral fracture in patients receiving oral glucocorticoid therapy. Arthritis Rheum 48(11):3224–3229
Schorlemmer S, Ignatius A, Claes L, Augat P (2005) Inhibition of cortical and cancellous bone formation in glucocorticoid-treated OVX sheep. Bone 37(4):491–496
Chappard D, Legrand E, Basle MF, Fromont P et al (1996) Altered trabecular architecture induced by corticosteroids: a bone histomorphometric study. J Bone Miner Res 11(5):676–685
LoCascio V, Ballanti P, Milani S, Bertoldo F et al (1998) A histomorphometric long-term longitudinal study of trabecular bone loss in glucocorticoid-treated patients: prednisone versus deflazacort. Calcif Tissue Int 62(3):199–204
Manolides AS, Cullen DM, Akhter MP (2010) Effects of glucocorticoid treatment on bone strength. J Bone Miner Metab 28(5):532–539
Winzenrieth R, Michelet F, Hans D (2013) 3D microarchitecture correlations with 2D projection image grey level variations assessed by TBS using high resolution CT acquisitions: effects of resolution and noise. J Clin Densitom 16(3):287–296
Hans D, Barthe N, Boutroy S, Pothuaud L, Winzenrieth R, Krieg MA (2011) Correlations between trabecular bone score, measured using anteroposterior dual-energy X-ray absorptiometry acquisition, and 3-dimensional parameters of bone microarchitecture: an experimental study on human cadaver vertebrae. J Clin Densitom 14(3):302–312
Romagnoli E, Cipriani C, Nofroni I, Castro C, Angelozzi M, Scarpiello A, Pepe J, Diacinti D, Piemonte S, Carnevale V, Minisola S (2013) “Trabecular bone score” (TBS): an indirect measure of bone micro-architecture in postmenopausal patients with primary hyperparathyroidism. Bone 53(1):154–159
Eller-Vainicher C, Filopanti M, Palmieri S, Ulivieri FM, Morelli V, Zhukouskaya V, Cairoli E, Pino R, Naccarato A, Verga U, Scillitani A, Beck-Peccoz P, Chiodini I (2013) Bone quality, as measured by trabecular bone score (TBS) in patients with primary hyperparathyroidism. Eur J Endocrinol 169(2):155–162
Bréban S, Briot K, Kolta S, Paternotte S, Ghazi M, Fechtenbaum J, Roux C (2012) Identification of rheumatoid arthritis patients with vertebral fractures using bone mineral density and trabecular bone score. J Clin Densitom 15(3):260–266
Dhaliwal R, Cibula D, Ghosh C, Weinstock RS, Moses AM (2014) Bone quality assessment in type diabetes mellitus. Osteoporos Int 25(7):1969–1973
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(2):602–609
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(10):2223–2230
Dempster DW (1983) Bone histomorphometry in glucocorticoid-induced osteoporosis. J Clin Densitom 4(2):137–141
Angeli A, Guglielmi G, Dovio A, Capelli G et al (2006) High prevalence of asymptomatic vertebral fractures in post-menopausal women receiving chronic glucocorticoid therapy: a cross-sectional outpatient study. BONE 39(2):253–259
Habib GS, Haj S (2005) Bone mineral density in patients with early rheumatoid arthritis treated with corticosteroids. Clin Rheumatol 24(2):129–133
Hansen M, Floresco A, Stoltenberg M, Podenphant J et al (1996) Bone loss in rheumatoid arthritis. Influence of disease activity, duration of the disease, functional capacity and corticosteroid treatment. Scand J Rheumatol 25:367–376
Felder M, Ruegsegger P (1991) Bone loss in patients with rheumatoid arthritis—effect of steroids measured by low dose quantitative computed tomography. Rheumatol Int 1:41–44
van Everdingen AA, van Reesema DRS, Jacobs JW, Bijlsma JW (2003) Low-dose glucocorticoids in early rheumatoid arthritis: discordant effects on bone mineral density and fractures? Clin Exp Rheumatol 21(2):155–160
Kaji H, Yamauchi M, Chihara K, Sugimoto T (2006) The threshold of bone mineral density for vertebral fracture in female patients with glucocorticoid-induced osteoporosis. Endocr J 53(1):27–34
Angeli A, Capelli G, deFeo D, Giustina A et al (2003) Age-related prevalence of vertebral deformities in post-menopausal women treated or untreated with glucocorticoids: a comparison between two national studies. J Clin Densitom 18(S2):360
Graeff C, Marin F, Petto H, Kayser O, Reisinger A, Peña J, Zysset P, Glüer CC (2013) High resolution quantitative computed tomography-based assessment of trabecular microstructure and strength estimates by finite-element analysis of the spine, but not DXA, reflects vertebral fracture status in men with glucocorticoid-induced osteoporosis. Bone 52:568–577
Reid IR, France JT, Pybus J, Ibbertson HK (1985) Low plasma testosterone levels in glucocorticoid-treated male asthmatics. Br Med J 291:574
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):2762–2769
Conflicts of interest
Renaud Winzenrieth is a senior scientist at Med-Imaps.
Edward Leib has no conflict of interest.
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Leib, E.S., Winzenrieth, R. Bone status in glucocorticoid-treated men and women. Osteoporos Int 27, 39–48 (2016). https://doi.org/10.1007/s00198-015-3211-1
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DOI: https://doi.org/10.1007/s00198-015-3211-1