ORIGINAL ARTICLE: The association between serum thyrotropin (TSH) levels and bone mineral density in healthy euthyroid men
Abstract
Summary: Objective Although osteoporosis is increasingly shown to occur in a considerable proportion of men, data on risk factors for male osteoporosis are limited. In this study, we investigated the association between serum thyrotropin (TSH) concentration and bone mineral density (BMD) in healthy euthyroid men. Design A cross‐sectional community (health promotion centre)‐based survey. Subjects and measurements For 1478 apparently healthy euthyroid men who participated in a routine health screening examination, we measured BMD at the lumbar spine and femoral neck using dual energy X‐ray absorptiometry and serum TSH concentrations using immunoluminometry. Results Lumbar spine BMD linearly increased with TSH level after adjustment for age, weight and height (P for trend = 0·002), and statistical significance persisted after additional adjustment for smoking and drinking habits (P for trend = 0·010). When serum alkaline phosphatase was added as a confounding variable, the relationship was still significant (P for trend = 0·016). Femoral neck BMD also tended to increase in higher TSH concentration after adjustment for age, weight and height (P for trend = 0·042), but this association disappeared after additional adjustment for smoking and drinking habits. The odds of lower BMD (i.e. osteopaenia and osteoporosis combined) were significantly increased in subjects with low‐normal TSH (i.e. 0·4–1·2 mU/l), when compared to high‐normal TSH (i.e. 3·1–5·0 mU/l), after adjustment for confounding factors (odds ratio = 1·45, 95% CI = 1·02–2·10). Conclusion These results suggest that a serum TSH concentration at the lower end of the reference range may be associated with low BMD in men.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Lower TSH levels and higher levels of FT4 within the population reference-range are associated with increased risk of developing osteoporosis and suffering subsequent fractures in post-menopausal women.
“Similar cross-sectional analyses have identified that lower TSH levels and higher levels of FT4 within the population reference-range are associated with increased risk of developing osteoporosis [70–73] and suffering subsequent fractures [71, 74] in post-menopausal women.”
From Age-related variation in thyroid function – a narrative review highlighting important implications for research and clinical practice (2023) · cites this paper as [72]
Cites
Hip fractures in the elderly: A world-wide projection
Cooper, C. C., Campion, G., & Melton, L. J. (1992) · Osteoporosis International · doi:10.1007/bf01623184 · Cited by 3,225 · see citing works
Mortality after all major types of osteoporotic fracture in men and women: an observational study
Nguyen, T. V., Schneider, D. L., Sambrook, P. N., & Eisman, J. A. (1999) · The Lancet · doi:10.1016/s0140-6736(98)09075-8 · Cited by 1,926 · see citing works
Khosla, S., Amin, S., & ORWOLL, E. S. (2008) · Endocrine Reviews · doi:10.1210/er.2008-0002 · Cited by 934 · see citing works
Pathogenesis of bone fragility in women and men
Seeman, E. (2002) · The Lancet · doi:10.1016/s0140-6736(02)08706-8 · Cited by 909 · see citing works
TSH Is a Negative Regulator of Skeletal Remodeling
Abe, E., Marians, R. C., Yu, W., Wu, X.-B., Ando, T., Li, Y., Iqbal, J., Eldeiry, L., Rajendren, G., Blair, H. C., et al. (2003) · Cell · doi:10.1016/s0092-8674(03)00771-2 · Cited by 691 · see citing works
Baskin, H. J., Cobin, R. H., Duick, D. S., Gharib, H., Guttler, R. B., Kaplan, M. M., Segal, R. L., Garber, J. R., Hamilton Jr, C. R., Handelsman, Y., et al. (2002) · Endocrine Practice · doi:10.4158/1934-2403-8.6.457 · Cited by 673 · see citing works
Parle, J. V., Maisonneuve, P., Sheppard, M. C., Boyle, P., & Franklyn, J. A. (2001) · The Lancet · doi:10.1016/s0140-6736(01)06067-6 · Cited by 669 · see citing works
Risk for fracture in women with low serum levels of thyroid-stimulating hormone
Bauer, D. C., Ettinger, B., Nevitt, M. C., Stone, K. L., & for the Study of Osteoporotic Fractures Research Group (2001) · Annals of Internal Medicine · doi:10.7326/0003-4819-134-7-200104030-00009 · Cited by 467 · see citing works
Monzani, F., Di Bello, V., Caraccio, N., Bertini, A., Giorgi, D., Giusti, C., & Ferrannini, E. (2001) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.86.3.7291 · Cited by 308 · see citing works
The Thyrotropin Reference Range Should Remain Unchanged
Surks, M. I., Goswami, G., & Daniels, G. H. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-0170 · Cited by 287 · see citing works
Díez, J. J., & Iglesias, P. (2004) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2003-032061 · Cited by 281 · see citing works
The Effect of Thyroid Hormone on Skeletal Integrity
Greenspan, S. L., & Greenspan, F. S. (1999) · Annals of Internal Medicine · doi:10.7326/0003-4819-130-9-199905040-00016 · Cited by 249 · see citing works
Thyroid-Stimulating Hormone: Biosynthesis, Cell Biology, and Bioactivity
Magner, J. A. (1990) · Endocrine Reviews · doi:10.1210/edrv-11-2-354 · Cited by 179 · see citing works
Murphy, E., & Williams, G. R. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02053.x · Cited by 160 · see citing works
Michalopoulou, G., Alevizaki, M., Piperingos, G. D., Mitsibounas, D. N., Mantzos, E., Adamopoulos, P., & Koutras, D. A. (1998) · European Journal of Endocrinology · doi:10.1530/eje.0.1380141 · Cited by 156 · see citing works
The effect of smoking at different life stages on bone mineral density in elderly men and women
Kiel, D. P., Zhang, Y., Hannan, M. T., Anderson, J. J., Baron, J. A., & Felson, D. T. (1996) · Osteoporosis International · doi:10.1007/bf01622741 · Cited by 148 · see citing works
Sampath, T. K., Šimić, P., Sendak, R. A., Drača, N., Bowe, A. E., O'Brien, S., Schiavi, S. C., McPherson, J. M., & Vukičević, S. (2007) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.070302 · Cited by 143 · see citing works
Cigarette smoking and bone mineral density in the elderly.
Egger, P., Duggleby, S., Hobbs, R. F., Fall, C. H. D., & Cooper, C. C. (1996) · Journal of Epidemiology & Community Health · doi:10.1136/jech.50.1.47 · Cited by 136 · see citing works
Bone metabolism during anti‐thyroid drug treatment of endogenous subclinical hyperthyroidism
Mudde, A. H., Houben, A. J. H. M., & Kruseman, A. C. N. (1994) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1994.tb02571.x · Cited by 135 · see citing works
Morris, M. S. (2007) · Bone · doi:10.1016/j.bone.2006.12.001 · Cited by 129 · see citing works
Grimnes, G., Emaus, N., Joakimsen, R. M., Figenschau, Y., & Jorde, R. (2008) · Thyroid · doi:10.1089/thy.2008.0158 · Cited by 127 · see citing works
Amin, S., & Felson, D. T. (2001) · Rheumatic Disease Clinics of North America · doi:10.1016/s0889-857x(05)70186-1 · Cited by 123 · see citing works
Low normal TSH levels are associated with low bone mineral density in healthy postmenopausal women
Kim, D. J., Khang, Y. H., Koh, J., Shong, Y. K., & Kim, G. S. (2006) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2005.02422.x · Cited by 103 · see citing works
Self-citationLow Thyrotropin Levels Are Not Associated with Bone Loss in Older Women: A Prospective Study
Bauer, D. C., Nevitt, M. C., Ettinger, B. B., & Stone, K. L. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.9.4229 · Cited by 99 · see citing works
Gennari, L., & Bilezikian, J. P. (2007) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2007.03.008 · Cited by 98 · see citing works
Szulc, P., Montella, A., & Delmas, P. D. (2007) · Annals of the Rheumatic Diseases · doi:10.1136/ard.2007.077941 · Cited by 93 · see citing works
Bone mineral density in hyperthyroidism
Karga, H., Papapetrou, P. D., Korakovouni, A., Papandroulaki, F., Polymeris, A., & Pampouras, G. (2004) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2004.02110.x · Cited by 75 · see citing works
Bone and Calcium Metabolism in Subclinical Autoimmune Hyperthyroidism and Hypothyroidism
Kısakol, G., Kaya, A., Gönen, M. S., & Tunç, R. (2003) · Endocrine Journal · doi:10.1507/endocrj.50.657 · Cited by 67 · see citing works
Management of osteoporosis in men: an update and case example
Khan, A., Hodsman, A. B., Παπαϊωάννου, Α., Kendler, D. L., Brown, J. P., & Olszynski, W. P. (2007) · Canadian Medical Association Journal · doi:10.1503/cmaj.050816 · Cited by 41 · see citing works
An evaluation of densitometric vertebral fracture assessment in men
Vallarta-Ast, N., Krueger, D. C., Wrase, C., Agrawal, S., & Binkley, N. (2007) · Osteoporosis International · doi:10.1007/s00198-007-0381-5 · Cited by 40 · see citing works
Mariotti, S. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2214 · Cited by 38 · see citing works
Engler, H., Oettli, R., & Riesen, W. F. (1999) · Clinica Chimica Acta · doi:10.1016/s0009-8981(99)00173-4 · Cited by 36 · see citing works
Szabolcs, I., Ploenes, C., Bernard, W., & Herrmann, J. (1990) · Hormone and Metabolic Research · doi:10.1055/s-2007-1004906 · Cited by 25 · see citing works
Cho, J. M., Kim, J. S., Kim, G. S., Kim, S., Shin, J. W., Moon, D. H., & Lee, H. K. (1999) · The Korean Journal of Nuclear Medicine · Cited by 20 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Role of Thyroid Hormones in Skeletal Development and Bone Maintenance
Bassett, J. H. D., & Williams, G. R. (2016) · Endocrine Reviews · doi:10.1210/er.2015-1106 · Cited by 540 · see citing works
A Review of the Clinical Consequences of Variation in Thyroid Function Within the Reference Range
Taylor, P. N., Razvi, S., Pearce, S. H., & Dayan, C. M. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-1315 · Cited by 274 · see citing works
Mazziotti, G., Frara, S., & Giustina, A. (2018) · Endocrine Reviews · doi:10.1210/er.2018-00005 · Cited by 181 · see citing works
Choi, Y. M., Kim, W. G., Kim, T. Y., Bae, S. J., Kim, H., Jang, E. K., Jeon, M. J., Han, J. M., Lee, S. H., Baek, J. H., et al. (2013) · Thyroid · doi:10.1089/thy.2013.0460 · Cited by 91 · see citing works
Self-citationMa, R., Morshed, S., Latif, R., Zaidi, M., & Davies, T. (2011) · Thyroid · doi:10.1089/thy.2010.0457 · Cited by 79 · see citing works
Taylor, P. N., Lansdown, A., Witczak, J., Khan, R., Rees, A., Dayan, C. M., & Okosieme, O. (2023) · Thyroid Research · doi:10.1186/s13044-023-00149-5 · Cited by 72 · see citing works
A prospective study of thyroid function, bone loss, and fractures in older men: The MrOS study
Waring, A. C., Harrison, S., Fink, H. A., Samuels, M. H., Cawthon, P. M., Zmuda, J. M., Orwoll, E. S., Bauer, D. C., & Study, F. T. O. F. I. M. (. (2013) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.1774 · Cited by 68 · see citing works
Garin, M. C., Arnold, A. M., Lee, J. S., Robbins, J., & Cappola, A. R. (2014) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2014-1051 · Cited by 65 · see citing works
Does thyroid function influence fracture risk? Prospective data from the HUNT2 study, Norway
Svare, A., Nilsen, T. I. L., Åsvold, B. O., Forsmo, S., Schei, B., Bjøro, T., & Langhammer, A. (2013) · European Journal of Endocrinology · doi:10.1530/eje-13-0546 · Cited by 52 · see citing works
Noh, H.-M., Park, Y. S., Lee, J., & Lee, W. (2015) · Osteoporosis International · doi:10.1007/s00198-014-2906-z · Cited by 47 · see citing works
Siru, R., Alfonso, H. S., Chubb, S. A. P., Golledge, J., Flicker, L. A., & Yeap, B. B. (2018) · Clinical Endocrinology · doi:10.1111/cen.13615 · Cited by 39 · see citing works
Bone health in children with long–term idiopathic subclinical hypothyroidism
Mase, R. D., Cerbone, M., Improda, N., Esposito, A., Capalbo, D., Mainolfi, C. G., Santamaria, F., Pignata, C., & Salerno, M. (2012) · The Italian Journal of Pediatrics/Italian journal of pediatrics · doi:10.1186/1824-7288-38-56 · Cited by 35 · see citing works
Should we treat mild subclinical/mild hyperthyroidism? Yes
Wiersinga, W. M. (2011) · European Journal of Internal Medicine · doi:10.1016/j.ejim.2011.03.008 · Cited by 27 · see citing works
Association of Serum TSH With Handgrip Strength in Community-Dwelling Euthyroid Elderly
Kim, B., Lee, S. H., Isales, C. M., Hamrick, M. W., Kwak, M. K., & Koh, J. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-01095 · Cited by 26 · see citing works
Self-citationGonzalez-Rodriguez, L. A., Felici-Giovanini, M. E., & Haddock, L. (2013) · PubMed · Cited by 26 · see citing works
Lee, K., Lim, S., Park, H. H., Woo, H., Chang, Y., Sung, E., Jung, H. S., Yun, K. E., Kim, C., Ryu, S., et al. (2019) · Osteoporosis International · doi:10.1007/s00198-019-05205-1 · Cited by 26 · see citing works
The impact of thyroid autoimmunity (TPOAb) on bone density and fracture risk in postmenopausal women
Polovina, S. P., Miljić, D., Zivojinović, S., Milic, N. M., Micić, D., & Popović-Brkić, V. (2017) · HORMONES · doi:10.14310/horm.2002.1719 · Cited by 25 · see citing works
Clozapine protects bone mineral density in female patients with schizophrenia
Lin, C., Huang, K.-H., Chang, Y., Huang, Y., Hsu, W.-C., Lin, C.-Y., Chou, F. H., Tsai, G. E., & Lane, H. (2011) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145711001507 · Cited by 22 · see citing works
Pituitary-bone connection in skeletal regulation
Zaidi, M., Sun, L., Liu, P., Davies, T. F., New, M. I., Zallone, A. Z., & Yuen, T. (2016) · Hormone Molecular Biology and Clinical Investigation · doi:10.1515/hmbci-2016-0015 · Cited by 21 · see citing works
Association between Sensitivity to Thyroid Hormone Indices and Bone Mineral Density in US Males
Chen, S., Huang, W., Zhou, G., Sun, X., Jin, J., & Li, Z. (2022) · International Journal of Endocrinology · doi:10.1155/2022/2205616 · Cited by 20 · see citing works
Long-term Use of Clozapine is Protective for Bone Density in Patients with Schizophrenia
Lin, C., Lin, C.-Y., Wang, H.-S., & Lane, H. (2019) · Scientific Reports · doi:10.1038/s41598-019-40691-7 · Cited by 18 · see citing works
Thyroid-Stimulating Hormone Is Significantly Associated with Bone Health Status in Men
Chin, K., Ima-Nirwana, S., Mohamed, I. N., Aminuddin, A., Johari, M. H., & Ngah, W. Z. W. (2013) · International Journal of Medical Sciences · doi:10.7150/ijms.5870 · Cited by 16 · see citing works
Yang, L., Wang, H., Guo, J., Zheng, G., Wei, D., & Zhang, T. (2020) · Endocrine Metabolic & Immune Disorders - Drug Targets · doi:10.2174/1871530320666200810144506 · Cited by 16 · see citing works
Cho, S. W., Bae, J. H., Noh, G. W., Kim, Y. A., Moon, M. K., Park, K. U., Song, J., Yi, K. H., Park, D. J., Chung, J., et al. (2015) · PLoS ONE · doi:10.1371/journal.pone.0144599 · Cited by 15 · see citing works
Approach to the Patient With a Suppressed TSH
Praw, S. S., & Brent, G. A. (2022) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/clinem/dgac635 · Cited by 13 · see citing works
The Association of Thyroid Function With Bone Density During Childhood
Veldscholte, K., Barjaktarovic, M., Trajanoska, K., Jaddoe, V. W. V., Visser, T. J., de Rijke, Y. B., Peeters, R. P., Rivadeneira, F., & Korevaar, T. I. M. (2018) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2018-00294 · Cited by 12 · see citing works
Krieg, E. F. (2018) · Journal of Trace Elements in Medicine and Biology · doi:10.1016/j.jtemb.2018.10.010 · Cited by 11 · see citing works
Barbosa, A. P., Mascarenhas, M. R., Silva, C. F., Távora, I., Bicho, M., do Carmo, I., & de Oliveira, A. G. (2015) · European Journal of Endocrinology · doi:10.1530/eje-14-0602 · Cited by 8 · see citing works
Thyroid Disorders and Bone Mineral Homeostasis
Feigerlová, E., Klein, M., Angelousi, A. G., Groza, L., Leheup, B., & Weryh, G. (2012) · InTech eBooks · doi:10.5772/46207 · Cited by 5 · see citing works
Jia, H., Qu, W., Cai, X.-T., Li, M., Qian, Y., Jiang, Z., & Zhang, Z. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2023.1286947 · Cited by 4 · see citing works
Barbosa, A. P., Mascarenhas, M. R., Bicho, M., Janeiro, J., & Oliveira, A. G. (2017) · Osteoporosis and Sarcopenia · doi:10.1016/j.afos.2017.08.099 · Cited by 3 · see citing works
The risk between thyrotropin suppression and bone mineral density in differentiated thyroid cancer
Zou, Y., Li, B., Wang, X., Mao, J., & Zhang, Y. (2022) · Medicine · doi:10.1097/md.0000000000031991 · Cited by 3 · see citing works
Lessons from the Bone Chapter of the Malaysian Aging Men Study
Chin, K., Ngah, W. W., & Ima-Nirwana, S. (2016) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph13060531 · Cited by 3 · see citing works
Pituitary Hormone-Driven Mechanism for Skeletal Loss
Yuen, T., Sun, L., Abu‐Amer, W., Liu, P., Davies, T. F., Blair, H. C., New, M. I., Zallone, A. Z., & Zaidi, M. (2017) · Molecular and integrative toxicology · doi:10.1007/978-3-319-56192-9_10 · Cited by 2 · see citing works
Dickson, G. M. (2011) · Journal of Men s Health · doi:10.1016/j.jomh.2011.01.002 · Cited by 2 · see citing works
Variation in 'normal' thyroid function—effect on bone health?
Cooper, M. S. (2010) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2010.132 · Cited by 1 · see citing works
Аналіз впливу субклінічного гіпертиреозу на параметри кісткового метаболізму
Pankiv, І. V. (2016) · INTERNATIONAL JOURNAL OF ENDOCRINOLOGY (Ukraine) · doi:10.22141/2224-0721.2.74.2016.70946 · Cited by 1 · see citing works
Chen, J., Hu, L., Li, N., Deng, W., Xu, X., Wang, L., Zhao, K., Lu, S., Liu, X., Cheng, X., et al. (2024) · Nutrition & Metabolism · doi:10.1186/s12986-024-00841-9 · Cited by 1 · see citing works
Perte osseuse et ostéoporose au cours des traitements des dysthyroïdies
Weryha, G., Dassa, Y., Weryha, B., Fiorani, L., & Klein, M. (2011) · Revue du Rhumatisme Monographies · doi:10.1016/j.monrhu.2011.02.002
Rising prevalence of Osteopenia in young and middle aged Men in South Mumbai-An Alarming Situation
Bala, S. S., & Chhabria, P. (2017) · Madridge Journal of Behavioral & Social Sciences · doi:10.18689/mjbss-1000105
Thyroid hormone, thyroid medication, and the skeleton
Freudenthal, B., Watts, L., Bassett, J. H. D., & Williams, G. R. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-813073-5.00046-0
Thyroid Disorders and Bone Disease
Watts, L. M., Freudenthal, B., Bassett, J. H. D., & Williams, G. R. (2022) · doi:10.1093/med/9780198870197.003.0089
- Authors
- Kim, B., Lee, S. H., Bae, S. J., Kim, H. K., Choe, J. W., Kim, H. Y., Koh, J., & Kim, G. S.
- Affiliations
- Asan Medical Center (KR)
- Corresponding author
- Koh, Jung‐Min
- Venue
- Clinical Endocrinology
- Publisher
- Wiley
- Published
- 2010-08-17
- Volume
- 73
- Issue
- 3
- Pages
- 396-403
- ISSN
- 0300-0664 (ISSN-L)
- 1365-2265
- OpenAlex
- W1600732834
- Cited by
- 43
- References
- 34
- Citations by year
- 2024: 1 · 2023: 3 · 2022: 4 · 2020: 2 · 2019: 2 · 2018: 5 · 2017: 4 · 2016: 4 · 2015: 2 · 2014: 2 · 2013: 5 · 2012: 3
- FWCI
- 4.49
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Clinical Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Thyroid Disorders and Treatments
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Hormonal and reproductive studies
- Keywords
- thyroid-stimulating hormone, bone mineral density, male osteoporosis, osteopenia, lumbar spine, femoral neck, alkaline phosphatase, smoking, alcohol consumption
- MeSH terms
- Adult, Aged, Aged, 80 and over, Alkaline Phosphatase, Analysis of Variance, Bone Diseases, Metabolic, Cross-Sectional Studies, Femur Neck, Humans, Lumbar Vertebrae, Male, Middle Aged, Osteoporosis, Reference Values, Thyrotropin, Thyroxine, Absorptiometry, Photon, Bone Density, Linear Models, Odds Ratio, Young Adult
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
