Low normal TSH levels are associated with low bone mineral density in healthy postmenopausal women
Abstract
Summary: Objective Hyperthyroidism is accompanied by low bone mass. Because the reference range of TSH levels is defined statistically, some individuals with low normal TSH levels may have mild hyperthyroidism and reduced bone mass. We therefore determined whether serum TSH levels correlate with bone mineral density (BMD). Design A cross‐sectional hospital‐based survey. Participants Nine hundred and fifty‐nine healthy postmenopausal women. Measurements We measured BMD at the lumbar spine and femoral neck using dual energy X‐ray absorptiometry, and serum TSH concentrations using immunoluminometry. Results BMD at the lumbar spine and femoral neck increased with TSH level (P for trend < 0·001 at both sites). Even after adjustment for age, years since menopause and body mass index, subjects with low normal TSH levels (0·5–1·1 mU/l) had significantly lower BMDs at the lumbar spine (0·863 ± 0·009 g/cm 2vs 0·900 ± 0·009 g/cm 2, P = 0·004) and femoral neck (0·660 ± 0·006 g/cm 2vs 0·683 ± 0·006 g/cm 2, P = 0·006) than those with high normal TSH levels (2·8–5·0 mU/l), as well as a 2·2‐fold increased risk of osteoporosis (95% confidence interval: 1·2–4·0). Conclusion These results suggest that low normal TSH levels may not be physiological for postmenopausal women and, during treatment of hypothyroidism, may not be adequate for avoiding osteoporosis.
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Variation in thyroid status within the reference range in post-menopausal women is associated with altered bone mineral density and fracture risk.
“Population studies have also shown that variation in thyroid status within the reference range in post-menopausal women is associated with altered BMD and fracture risk.”
From Thyroid diseases and bone health (2018) · cites this paper as [43]
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 [73]
Cites
Long-term fracture prediction by bone mineral assessed at different skeletal sites
Melton, L. J., Atkinson, E. J., O’Fallon, W. M., Wahner, H. W., & Riggs, B. L. (1993) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.5650081010 · Cited by 860 · see citing works
Andersen, S., Pedersen, K. M., Bruun, N. H., & Laurberg, P. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.3.8165 · Cited by 686 · 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
Vestergaard, P., & Mosekilde, L. (2002) · Thyroid · doi:10.1089/105072502760043503 · Cited by 289 · 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
Biologic Variation is Important for Interpretation of Thyroid Function Tests
Andersen, S., Bruun, N. H., Pedersen, K. M., & Laurberg, P. (2003) · Thyroid · doi:10.1089/105072503770867237 · Cited by 241 · see citing works
Földes, J., Tarján, G., Szathmari, M., Varga, F., Krasznai, I., & Horvath, C. (1993) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1993.tb02403.x · Cited by 170 · see citing works
OSTEOPOROSIS AND FRACTURES FOLLOWING THYROTOXICOSIS
Fraser, S. A., Smith, D. A., Anderson, J., & Wilson, G. M. (1971) · The Lancet · doi:10.1016/s0140-6736(71)91383-3 · Cited by 159 · see citing works
Effect of Hyperthyroidism and Its Treatment on Bone Mineral Content
Toh, S. H. (1985) · Archives of Internal Medicine · doi:10.1001/archinte.1985.00360050147025 · Cited by 153 · see citing works
Changes in Parameters of Bone and Mineral Metabolism during Therapy for Hyperthyroidism
Pantazi, H., & Papapetrou, P. D. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.3.6457 · Cited by 140 · 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
Mazziotti, G., Sorvillo, F., Piscopo, M., Cioffi, M., Pilla, P., Biondi, B., Iorio, S., Giustina, A., Amato, G., & Carella, C. (2005) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.041126 · Cited by 126 · see citing works
Persistent Increase in Bone Turnover in Graves’ Patients with Subclinical Hyperthyroidism
Kumeda, Y., Inaba, M., Tahara, H., Kurioka, Y., Ishikawa, T., Morii, H., & Nishizawa, Y. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.85.11.6979 · Cited by 123 · see citing works
Hueston, W. J. (2001) · PubMed · Cited by 118 · see citing works
Peripheral bone density in women with untreated multinodular goitre
Mudde, A. H., Reijnders, F. J., & Kruseman, A. C. N. (1992) · Clinical Endocrinology · doi:10.1111/j.1365-2265.1992.tb02280.x · Cited by 73 · 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
Whose normal thyroid function is better—yours or mine?
Dayan, C. M., Saravanan, P., & Bayly, G. (2002) · The Lancet · doi:10.1016/s0140-6736(02)09602-2 · Cited by 61 · see citing works
Effect of hyperthyroidism and its treatment on bone mineral content
Toh, S. H. (1985) · Archives of Internal Medicine · doi:10.1001/archinte.145.5.883 · Cited by 40 · 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
Estradiol and tamoxifen interactions with thyroid hormone in the ovariectomized-thyroidectomized rat
DiPippo, V. A., Lindsay, R., & Powers, C. A. (1995) · Endocrinology · doi:10.1210/endo.136.3.7867556 · Cited by 35 · see citing works
Krakauer, J. C. (1992) · Archives of Internal Medicine · doi:10.1001/archinte.152.2.360 · Cited by 29 · see citing works
The significance of clinical euthyroidism on reference range for thyroid hormones
Kvetny, J. (2003) · European Journal of Internal Medicine · doi:10.1016/s0953-6205(03)00101-8 · Cited by 12 · see citing works
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
Thyroid diseases and bone health
Williams, G. R., & Bassett, J. H. D. (2018) · Journal of Endocrinological Investigation · doi:10.1007/s40618-017-0753-4 · Cited by 276 · 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
Murphy, E., Glüer, C. C., Reid, D. M., Felsenberg, D., Roux, C., Eastell, R., & Williams, G. R. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-2630 · Cited by 180 · see citing works
The skeletal consequences of thyrotoxicosis
Nicholls, J. J., Brassill, M. J., Williams, G. R., & Bassett, J. H. D. (2012) · Journal of Endocrinology · doi:10.1530/joe-12-0059 · Cited by 138 · 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
Mazziotti, G., Porcelli, T., Patelli, I., Vescovi, P. P., & Giustina, A. (2010) · Bone · doi:10.1016/j.bone.2009.10.031 · Cited by 113 · see citing works
Abrahamsen, B., Jørgensen, H. L., Laulund, A. S., Nybo, M., Brix, T. H., & Hegedüs, L. (2014) · Journal of Bone and Mineral Research · doi:10.1002/jbmr.2244 · Cited by 112 · 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
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
Boeving, A., Paz-Filho, G., Radominski, R. B., Graf, H., & de Carvalho, G. A. (2011) · Thyroid · doi:10.1089/thy.2010.0315 · Cited by 58 · see citing works
Yang, L.-B., Jiang, D.-Q., Qi, W.-B., Zhang, T., Feng, Y.-L., Gao, L., & Zhao, J. (2012) · European Journal of Endocrinology · doi:10.1530/eje-12-0015 · Cited by 56 · see citing works
Roef, G., Lapauw, B., Goemaere, S., Zmierczak, H., Fiers, T., Kaufman, J.-M., & Taes, Y. (2011) · European Journal of Endocrinology · doi:10.1530/eje-10-1113 · Cited by 54 · 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
Kim, B., Lee, S. H., Bae, S. J., Kim, H. K., Choe, J. W., Kim, H. Y., Koh, J., & Kim, G. S. (2010) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2010.03818.x · Cited by 43 · see citing works
Self-citationBone circuitry and interorgan skeletal crosstalk
Zaidi, M., Kim, S.-M., Mathew, M., Korkmaz, F., Sultana, F., Miyashita, S., Gumerova, A. A., Frolinger, T., Moldavski, O., Barak, O., et al. (2023) · eLife · doi:10.7554/elife.83142 · Cited by 45 · see citing works
Hwangbo, Y., Kim, J. H., Kim, S. W., Park, Y. J., Park, D. J., Kim, S. Y., Shin, C. S., & Cho, N. H. (2016) · Osteoporosis International · doi:10.1007/s00198-015-3270-3 · Cited by 34 · see citing works
- Authors
- Kim, D. J., Khang, Y. H., Koh, J., Shong, Y. K., & Kim, G. S.
- Affiliations
- Asan Medical Center (KR)
- Corresponding author
- Kim, Ghi Su
- Venue
- Clinical Endocrinology
- Publisher
- Wiley
- Published
- 2005-12-13
- Volume
- 64
- Issue
- 1
- Pages
- 86-90
- ISSN
- 0300-0664 (ISSN-L)
- 1365-2265
- OpenAlex
- W2093677271
- Cited by
- 103
- References
- 23
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 5 · 2023: 9 · 2022: 5 · 2021: 3 · 2020: 4 · 2019: 6 · 2018: 4 · 2017: 3 · 2016: 6 · 2015: 4 · 2014: 6 · 2013: 3 · 2012: 8
- FWCI
- 4.50
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Clinical Endocrinology (publishedVersion)
- PubMed (publishedVersion)
- Seoul National University Open Repository (Seoul National University) (submittedVersion)
- 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 › Menopause: Health Impacts and Treatments
- Keywords
- thyroid-stimulating hormone, bone mineral density, osteoporosis, postmenopausal women, hypothyroidism treatment, lumbar spine, femoral neck, bone loss
- MeSH terms
- Aged, Cross-Sectional Studies, Female, Femur Neck, Humans, Lumbar Vertebrae, Middle Aged, Reference Values, Regression Analysis, Testosterone, Thyrotropin, Time Factors, Bone Density, Body Mass Index, Postmenopause
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