Abstract
Summary
Trabecular bone scores (TBS) have recently been developed as a diagnostic tool to assess bone texture. We studied thyroid status and TBS in a population-based cohort and demonstrated that high-normal thyroxine levels are associated with low TBS in healthy euthyroid postmenopausal women.
Introduction
Increased thyroid hormone levels affect bone mineral density (BMD) and, if untreated, increase the risk of fracture. However, the relationship between thyroid function and bone microarchitecture has not yet been established. Trabecular bone scores (TBS) are gray-level textural measurements of dual energy X-ray absorptiometry (DXA) images. The TBS has been proposed as an indirect index of bone microarchitecture. The goal of this study was to characterize the relationship between thyroid function and TBS in euthyroid men and postmenopausal euthyroid women.
Methods
A total of 1376 euthyroid subjects (648 postmenopausal women and 728 men) were recruited from a community-based cohort in Korea. Free thyroxine (fT4) levels, thyroid stimulating hormone (TSH) levels, BMD, and TBS were measured and compared.
Results
There was no significant relationship between either fT4 or TSH levels and BMD in men and women. Multiple linear regression analysis showed that high-normal fT4 levels were negatively correlated with TBS (β = −0.111; P = 0.002, after adjusting for both age and body mass index [BMI]) in postmenopausal women. In men, however, there was no significant correlation between fT4 levels and TBS. TSH levels were not significantly associated with TBS in either men or women.
Conclusion
Higher fT4 levels within the normal reference range are associated with deterioration of trabecular microarchitecture in healthy euthyroid postmenopausal women.
Similar content being viewed by others
References
Vestergaard P, Mosekilde L (2003) Hyperthyroidism, bone mineral, and fracture risk—a meta-analysis. Thyroid 13:585–593
Ross DS (1994) Hyperthyroidism, thyroid hormone therapy, and bone. Thyroid 4:319–326
Mosekilde L, Melsen F, Bagger JP, Myhre-Jensen O, Schwartz Sorensen N (1977) Bone changes in hyperthyroidism: interrelationships between bone morphometry, thyroid function and calcium-phosphorus metabolism. Acta Endocrinol (Copenh) 85:515–525
Eriksen EF, Mosekilde L, Melsen F (1985) Trabecular bone remodeling and bone balance in hyperthyroidism. Bone 6:421–428
Tauchmanova L, Nuzzo V, Del Puente A, Fonderico F, Esposito-Del Puente A, Padulla S, Rossi A, Bifulco G, Lupoli G, Lombardi G (2004) Reduced bone mass detected by bone quantitative ultrasonometry and DEXA in pre- and postmenopausal women with endogenous subclinical hyperthyroidism. Maturitas 48:299–306
Belaya ZE, Melnichenko GA, Rozhinskaya LY, Fadeev VV, Alekseeva TM, Dorofeeva OK, Sasonova NI, Kolesnikova GS (2007) Subclinical hyperthyroidism of variable etiology and its influence on bone in postmenopausal women. Hormones (Athens) 6:62–70
Lee WY, Oh KW, Rhee EJ et al (2006) Relationship between subclinical thyroid dysfunction and femoral neck bone mineral density in women. Arch Med Res 37:511–516
Galliford TM, Murphy E, Williams AJ, Bassett JH, Williams GR (2005) Effects of thyroid status on bone metabolism: a primary role for thyroid stimulating hormone or thyroid hormone? Minerva Endocrinol 30:237–246
Abe E, Marians RC, Yu W et al (2003) TSH is a negative regulator of skeletal remodeling. Cell 115:151–162
Sampath TK, Simic P, Sendak R, Draca N, Bowe AE, O’Brien S, Schiavi SC, McPherson JM, Vukicevic S (2007) Thyroid-stimulating hormone restores bone volume, microarchitecture, and strength in aged ovariectomized rats. J Bone Miner Res 22:849–859
Morris MS (2007) The association between serum thyroid-stimulating hormone in its reference range and bone status in postmenopausal American women. Bone 40:1128–1134
Kim DJ, Khang YH, Koh JM, Shong YK, Kim GS (2006) Low normal TSH levels are associated with low bone mineral density in healthy postmenopausal women. Clin Endocrinol (Oxf) 64:86–90
Murphy E, Gluer CC, Reid DM, Felsenberg D, Roux C, Eastell R, Williams GR (2010) Thyroid function within the upper normal range is associated with reduced bone mineral density and an increased risk of nonvertebral fractures in healthy euthyroid postmenopausal women. J Clin Endocrinol Metab 95:3173–3181
Brandi ML (2009) Microarchitecture, the key to bone quality. Rheumatology (Oxford) 48(Suppl 4):iv3–iv8
Bassett JH, O’Shea PJ, Sriskantharajah S et al (2007) Thyroid hormone excess rather than thyrotropin deficiency induces osteoporosis in hyperthyroidism. Mol Endocrinol 21:1095–1107
World Health Organization (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. Report of a WHO Study Group. World Health Organ Tech Rep Ser 843:1–129
Pothuaud L, Carceller P, Hans D (2008) Correlations between grey-level variations in 2D projection images (TBS) and 3D microarchitecture: applications in the study of human trabecular bone microarchitecture. Bone 42:775–787
Bousson V, Bergot C, Sutter B, Levitz P, Cortet B, Scientific Committee of the Groupe de Recherche et d’Information sur les O (2012) Trabecular bone score (TBS): available knowledge, clinical relevance, and future prospects. Osteoporos Int 23:1489–1501
Silva BC, Bilezikian JP (2014) Trabecular bone score: perspectives of an imaging technology coming of age. Arq Bras Endocrinol Metabol 58:493–503
Shin CS, Choi HJ, Kim MJ et al (2010) Prevalence and risk factors of osteoporosis in Korea: a community-based cohort study with lumbar spine and hip bone mineral density. Bone 47:378–387
Dalle Carbonare L, Giannini S (2004) Bone microarchitecture as an important determinant of bone strength. J Endocrinol Investig 27:99–105
Boutroy S, Bouxsein ML, Munoz F, Delmas PD (2005) In vivo assessment of trabecular bone microarchitecture by high-resolution peripheral quantitative computed tomography. J Clin Endocrinol Metab 90:6508–6515
Krug R, Banerjee S, Han ET, Newitt DC, Link TM, Majumdar S (2005) Feasibility of in vivo structural analysis of high-resolution magnetic resonance images of the proximal femur. Osteoporos Int 16:1307–1314
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 14:302–312
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 26:2762–2769
Del Rio LM, Winzenrieth R, Cormier C, Di Gregorio S (2013) Is bone microarchitecture status of the lumbar spine assessed by TBS related to femoral neck fracture? A Spanish case-control study. Osteoporos Int 24:991–998
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 29:518–530
Romagnoli E, Cipriani C, Nofroni I et al (2013) “Trabecular Bone Score” (TBS): an indirect measure of bone micro-architecture in postmenopausal patients with primary hyperparathyroidism. Bone 53:154–159
Leslie WD, Aubry-Rozier B, Lamy O, Hans D, Manitoba Bone Density P (2013) TBS (trabecular bone score) and diabetes-related fracture risk. J Clin Endocrinol Metab 98:602–609
Leslie WD, Krieg MA, Hans D, Manitoba Bone Density P (2013) Clinical factors associated with trabecular bone score. J Clin Densitom 16:374–379
Eller-Vainicher C, Morelli V, Ulivieri FM et al (2012) Bone quality, as measured by trabecular bone score in patients with adrenal incidentalomas with and without subclinical hypercortisolism. J Bone Miner Res 27:2223–2230
Roef G, Lapauw B, Goemaere S, Zmierczak H, Fiers T, Kaufman JM, Taes Y (2011) Thyroid hormone status within the physiological range affects bone mass and density in healthy men at the age of peak bone mass. Eur J Endocrinol 164:1027–1034
van Rijn LE, Pop VJ, Williams GR (2014) Low bone mineral density is related to high physiological levels of free thyroxine in peri-menopausal women. Eur J Endocrinol 170:461–468
Papadimitriou A, Papadimitriou DT, Papadopoulou A, Nicolaidou P, Fretzayas A (2007) Low TSH levels are not associated with osteoporosis in childhood. Eur J Endocrinol 157:221–223
Leslie WD, Lix L, Morin S, Majumdar S, Hans D (2014) Difference in spine TBS between men and women: real or technical? Osteoporos Int 25:S25–S26
Leslie WD, Aubry-Rozier B, Lix LM, Morin SN, Majumdar SR, Hans D (2014) Spine bone texture assessed by trabecular bone score (TBS) predicts osteoporotic fractures in men: The Manitoba Bone Density Program. Bone 67:10–14
Acknowledgments
This work was supported by the Research Program funded by the Korea Centers for Disease Control and Prevention (funds 2011-E71008-00 and 2012-E71008-00) and also supported by a grant from the Korean Health Technology R&D Project, Ministry of Health & Welfare, Republic of Korea (HI12C1338). The funding source had no role in the collection of the data or in the decision to submit this manuscript for publication.
Conflicts of interest
None.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Hwangbo, Y., Kim, J.H., Kim, S.W. et al. High-normal free thyroxine levels are associated with low trabecular bone scores in euthyroid postmenopausal women. Osteoporos Int 27, 457–462 (2016). https://doi.org/10.1007/s00198-015-3270-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-015-3270-3