The DOI matches its Crossref record; 41 of the 41 references it cites were found in a registry or an index.
Low Serum Thyrotropin Level and Duration of Suppression as a Predictor of Major Osteoporotic Fractures—The OPENTHYRO Register Cohort
Abstract
The relationship between thyrotoxicosis and osteoporotic fractures remains controversial, particularly in men. Register-based cohort study including all patients with a serum thyrotropin (TSH) measurement in the region of Funen 1996–2010. All TSH determinations were done in the same lab, which served all hospitals and General Practice (GP) practices in the region. Persons with raised TSH or a history of thyroid/pituitary disease or use of thyroid medications were excluded. The study population consisted of 222,138 (96%) persons with normal and 9217 (4%) with low TSH (<0.3 mIU/L). A single low TSH at baseline was associated with increased risk of hip fractures (adj HR 1.16, 95% CI 1.07–1.26, p < 0.001) but not major osteoporotic fractures (MOF, adj HR 1.06, 95% CI 0.99–1.12, p = 0.058) over a median follow-up of 7.5 years. When men were analyzed separately, results did not reach statistical significance. We found a significant association between duration of thyrotoxicosis and fracture. For each 6 months in which the mean TSH value was decreased (<0.3 mIU/L), hip fracture risk increased by a factor 1.07 (adj HR, 95% CI 1.04–1.10, p < 0.001) and MOF by 1.05 (adj HR, 95% CI 1.03–1.07, p < 0.001). Overt thyrotoxicosis was associated with an increased risk of hip fractures but not MOF. In euthyroid patients, the risk of fractures increased significantly with each SD unit of TSH decrease: Hip fracture (HR 1.45, 95% CI 1.22–1.71, p < 0.001) and MOF (HR 1.32, 95% CI 1.19–1.46, p < 0.001). In a population-based cohort, a single, first measurement of decreased TSH in patients without known thyroid disease was associated with an increased long-term risk of hip fracture, which remained significant in women but not in men after adjusting for confounders. Moreover, the risk of both hip fracture and MOF increased exponentially by the length of time during which TSH had remained low. © 2014 American Society for Bone and Mineral Research
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In the citing paper
“This large-scale study demonstrated a clear correlation between level of TSH, duration of low TSH and risk of osteoporotic fractures in relation to age and sex [30] .”
From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [30]
In the citing paper
“In a population-based cohort study, a single first measurement of decreased TSH was associated with an increased long-term risk of hip fractures in older women [30] .”
From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [30]
In the citing paper
“Differences in the degree of TSH suppression, causes of SHyper, patient age and duration of TSH suppression may influence the adverse consequences of Endo SHyper [3,5,30] .”
From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [30]
In the citing paper
“In fact, the effects of SHyper are likely influenced by the duration of the disease and associated risk factors for bone loss [30] .”
From The 2015 European Thyroid Association Guidelines on Diagnosis and Treatment of Endogenous Subclinical Hyperthyroidism (2015) · cites this paper as [30]
In the citing paper
“Variation in thyrotropin (TSH) levels within the normal reference range generally shows an inverse relationship with fracture risk so that low-normal TSH values are associated with modest increases in the risk of fractures.(13)(14)(15) and with decreases in BMD.(13,16)”
In the citing paper
“The impact of low TSH in this setting was very similar to that previously found by our group in patients with spontaneous hyperthyroidism using the same methodology (14)”
In the citing paper
“Risk increased with duration of SH, such that after a median follow-up of 7.5 years, 13.5% of subjects with a low TSH level had experienced at least one major osteoporotic fracture, compared to 6.9% of subjects with a normal TSH level (407).”
From 2016 American Thyroid Association Guidelines for Diagnosis and Management of Hyperthyroidism and Other Causes of Thyrotoxicosis (2016) · cites this paper as [407]
In the citing paper
“The most recent and by far the largest individual study to date (231,355 subjects) reported a hazard rate for all major osteoporotic fractures combined (hip, humerus, forearm, spine) of 1.13 [confidence intervals 1.014-1.26].”
From 2016 American Thyroid Association Guidelines for Diagnosis and Management of Hyperthyroidism and Other Causes of Thyrotoxicosis (2016) · cites this paper as [407]
In the citing paper
“A number of population-based studies have reported that certain groups of subjects with SH have increased fracture rates, including all adults (407), postmenopausal women (408), men (409), or subjects who progress to overt hyperthyroidism over time (391).”
From 2016 American Thyroid Association Guidelines for Diagnosis and Management of Hyperthyroidism and Other Causes of Thyrotoxicosis (2016) · cites this paper as [407]
Citations
Cites
Coding algorithms for defining comorbidities in ICD-9-CM and ICD-10 administrative data
Quan, H., Sundararajan, V., Halfon, P., Fong, A., Burnand, B., Luthi, J.-C., Saunders, L. D., Beck, C. A., Feasby, T. E., & Ghali, W. A. (2005) · Medical Care · doi:10.1097/01.mlr.0000182534.19832.83 · Cited by 10,669
Incidence and Economic Burden of Osteoporosis-Related Fractures in the United States, 2005–2025
Burge, R., Dawson-Hughes, B., Solomon, D. H., Wong, J. B., King, A., & Tosteson, A. (2007) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.061113 · Cited by 4,026
The Danish National Hospital Register. A valuable source of data for modern health sciences.
Andersen, T. F., Madsen, M., Jørgensen, J. O. L., Mellemkjoer, L., & Olsen, J. H. (1999) · PubMed · Cited by 2,026
Excess mortality following hip fracture: a systematic epidemiological review
Abrahamsen, B., van Staa, T., Ariely, R., Olson, M., & Cooper, C. (2009) · Osteoporosis International · doi:10.1007/s00198-009-0920-3 · Cited by 1,079
Self-citationOsteoporosis in the European Union: a compendium of country-specific reports
IOF, T. E. R. P. O. T., Svedbom, A., Hernlund, E., Ivergård, M., Compston, J., Cooper, C. C., Stenmark, J., McCloskey, E. V., Jönsson, B., & Kanis, J. A. (2013) · Archives of Osteoporosis · doi:10.1007/s11657-013-0137-0 · Cited by 740
The Danish prescription registries.
Gaist, D., Sørensen, H. T., & Hallas, J. (1997) · PubMed · Cited by 570
Kannegaard, P. N., Mark, S., Eiken, P., & Abrahamsen, B. (2010) · Age and Ageing · doi:10.1093/ageing/afp221 · Cited by 534
Self-citationRisk 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
Effects of thyroid hormones on bone and mineral metabolism
Mosekilde, L., Eriksen, E. F., & Charles, P. (1990) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/s0889-8529(18)30338-4 · Cited by 423
Flynn, R. W., Bonellie, S. R., Jung, R. T., MacDonald, T. M., Morris, A. D., & Leese, G. P. (2010) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2009-1625 · Cited by 415
High-Trauma Fractures and Low Bone Mineral Density in Older Women and Men
Mackey, D. C. (2007) · JAMA · doi:10.1001/jama.298.20.2381 · Cited by 352
Hyperthyroidism, Bone Mineral, and Fracture Risk—A Meta-Analysis
Vestergaard, P., & Mosekilde, L. (2003) · Thyroid · doi:10.1089/105072503322238854 · Cited by 306
Ryg, J., Rejnmark, L., Overgaard, S., Brixen, K., & Vestergaard, P. (2009) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.090207 · Cited by 293
Vestergaard, P., & Mosekilde, L. (2002) · Thyroid · doi:10.1089/105072502760043503 · Cited by 289
Quality of life in patients with benign thyroid disorders. A review
Watt, T., Grøenvold, M., Rasmussen, Å. K., Bonnema, S. J., Hegedűs, L. D., Bjørner, J. B., & Feldt‐Rasmussen, U. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02124 · Cited by 234
Self-citationSTUDIES OF CALCIUM AND PHOSPHORUS METABOLISM
Aub, J. C., BAUER, W. H., Heath, C. W., & Ropes, M. W. (1929) · Journal of Clinical Investigation · doi:10.1172/jci100223 · Cited by 221
Jørgensen, N. R., Schwarz, P., Holme, I., Henriksen, B. M., Petersen, L. J., & Backer, V. (2006) · Respiratory Medicine · doi:10.1016/j.rmed.2006.03.029 · Cited by 219
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
A critical review and meta-analysis of the association between overt hyperthyroidism and mortality
Brandt, F., Green, A., Hegedüs, L., & Brix, T. H. (2011) · European Journal of Endocrinology · doi:10.1530/eje-11-0299 · Cited by 170
Self-citationFaber, Jensen, Petersen, Nygaard, Hegedüs, & Siersbæk‐Nielsen (1998) · Clinical Endocrinology · doi:10.1046/j.1365-2265.1998.00427.x · Cited by 156
Levothyroxine dose and risk of fractures in older adults: nested case-control study
Turner, M. R., Camacho, X., Fischer, H. D., Austin, P. C., Anderson, G. M., Rochon, P. A., & Lipscombe, L. L. (2011) · BMJ · doi:10.1136/bmj.d2238 · Cited by 152
Mosekilde, L., & Melsen, F. (1978) · Acta Medica Scandinavica · doi:10.1111/j.0954-6820.1978.tb08406.x · Cited by 148
Morbidity before and after the diagnosis of hyperthyroidism: a nationwide register-based study
Brandt, F., Thvilum, M., Almind, D., Christensen, K., Green, A., Hegedüs, L., & Brix, T. H. (2013) · PLoS ONE · doi:10.1371/journal.pone.0066711 · Cited by 142
Self-citationBorgström, F., Lekander, I., Ivergård, M., Ström, O., Svedbom, A., Alekna, V., Bianchi, M. L., Clark, P., Díaz Curiel, M., Dimai, H. P., et al. (2013) · Osteoporosis International · doi:10.1007/s00198-012-2240-2 · Cited by 141
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
Effects of serum TSH and FT4 levels and the TSHR‐Asp727Glu polymorphism on bone: the Rotterdam Study
van der Deure, W. M., Uitterlinden, A. G., Albert Hofman, D., Rivadeneira, F., Pols, H. A. P., Peeters, R. P., & Visser, T. J. (2007) · Clinical Endocrinology · doi:10.1111/j.1365-2265.2007.03016.x · Cited by 132
Morris, M. S. (2007) · Bone · doi:10.1016/j.bone.2006.12.001 · Cited by 129
Hyperthyroidism and psychiatric morbidity: evidence from a Danish nationwide register study
Brandt, F., Thvilum, M., Almind, D., Christensen, K., Green, A., Hegedüs, L., & Brix, T. H. (2014) · European Journal of Endocrinology · doi:10.1530/eje-13-0708 · Cited by 111
Self-citationLow 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
Epidemiology of Osteoporosis and Fracture in Men
Kanis, J. А., Johnell, O., Odén, A., Laet, C. E. D. H. D., & Mellström, D. (2004) · Calcified Tissue International · doi:10.1007/s00223-004-0287-6 · Cited by 102
Proton Pump Inhibitor Use and the Antifracture Efficacy of Alendronate
Abrahamsen, B., Eiken, P., & Eastell, R. (2011) · Archives of Internal Medicine · doi:10.1001/archinternmed.2011.20 · Cited by 96
Self-citationBrandt, F., Almind, D., Christensen, K., Green, A., Brix, T. H., & Hegedüs, L. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2268 · Cited by 83
Self-citationMetabolic and Clinical Consequences of Hyperthyroidism on Bone Density
Gorka, J., Taylor‐Gjevre, R. M., & Arnason, T. (2013) · International Journal of Endocrinology · doi:10.1155/2013/638727 · Cited by 83
From relative risk to absolute fracture risk calculation: The FRAX algorithm
McCloskey, E. V., Johansson, H., Odén, A., & Kanis, J. А. (2009) · Current Osteoporosis Reports · doi:10.1007/s11914-009-0013-4 · Cited by 79
Hundrup, Y. A., Høidrup, S., Obel, E. B., & Rasmussen, N. K. (2004) · Scandinavian Journal of Public Health · doi:10.1080/14034940310017490 · Cited by 76
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
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
Risk of femoral shaft and subtrochanteric fractures among users of bisphosphonates and raloxifene
Vestergaard, P., Schwartz, F., Rejnmark, L., & Mosekilde, L. (2011) · Osteoporosis International · doi:10.1007/s00198-010-1512-y · Cited by 62
Langdahl, B. L., Loft, A. G., Eriksen, E. F., Mosekilde, L., & Charles, P. (1996) · PubMed · doi:10.1089/thy.1996.6.161 · Cited by 55
Langdahl, B. L., Loft, A. G., Eriksen, E. F., Mosekilde, L., & Charles, P. (1996) · PubMed · doi:10.1089/thy.1996.6.169 · Cited by 37
Irreversible Perforations in Vertebral Trabeculae?
Banse, X., Devogelaer, J., Delloye, C., Lafosse, A., Holmyard, D., & Grynpas, M. D. (2003) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.2003.18.7.1247 · Cited by 18
Research works printed but not linked: 1
- McCloskey, 2009, From relative risk to absolute fracture risk calculation: the FRAX algorithm, CurrOsteoporosRep., 7, 77
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“A number of population-based studies have reported that certain groups of subjects with SH have increased fracture rates, including all adults (407), postmenopausal women (408), men (409), or subjects who progress to overt hyperthyroidism over time (391).”
BackgroundGharib, H., Papini, E., Garber, J. R., Duick, D. S., Harrell, R. M., Hegedűs, L. D., Paschke, R., Valcavi, R., & Vitti, P. (2016) · Endocrine Practice · doi:10.4158/ep161208.gl · Cited by 1,285
Self-citationRole 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
MANAGEMENT OF ENDOCRINE DISEASE: Secondary osteoporosis: pathophysiology and management
Mirza, F., & CANALIS, E. M. (2015) · European Journal of Endocrinology · doi:10.1530/eje-15-0118 · Cited by 343
Biondi, B., Bartalena, L., Cooper, D. S., Hegedüs, L., Laurberg, P., & Kahaly, G. J. (2015) · European Thyroid Journal · doi:10.1159/000438750 · Cited by 323
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Metadata
- Authors
- Abrahamsen, B., Jørgensen, H. L., Laulund, A. S., Nybo, M., Brix, T. H., & Hegedüs, L.
- Affiliations
- University of Southern Denmark (DK)
- Bispebjerg Hospital (DK)
- Odense University Hospital (DK)
- Department of Endocrinology and MetabolismOdense University HospitalOdenseDenmark
- Corresponding author
- Abrahamsen, Bo
- Venue
- Journal of Bone and Mineral Research
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-04-09
- Volume
- 29
- Issue
- 9
- Pages
- 2040-2050
- ISSN
- 0884-0431 (ISSN-L)
- 1523-4681
- OpenAlex
- W1712440049
- Cited by
- 112
- References
- 41
- Citations by year
- 2026: 4 · 2025: 2 · 2024: 7 · 2023: 6 · 2022: 14 · 2021: 11 · 2020: 10 · 2019: 14 · 2018: 13 · 2017: 10 · 2016: 8 · 2015: 10 · 2014: 3
- FWCI
- 10.70
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
- Locations
- Journal of Bone and Mineral Research (publishedVersion)
- PubMed (publishedVersion)
- University of Southern Denmark Research Portal (University of Southern Denmark) (submittedVersion)
- Funders
- Amgen
- Eli Lilly and Company
- 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 › Surgery › Thyroid and Parathyroid Surgery
- Keywords
- TSH suppression, thyrotoxicosis, osteoporotic fractures, hip fracture, major osteoporotic fracture, overt hypothyroidism, fracture risk prediction, Funen, thyroid function tests, euthyroid patients, pituitary disorders, thyroid medication
- MeSH terms
- Adolescent, Adult, Aged, Denmark, Dose-Response Relationship, Drug, Female, Hospitals, Humans, Male, Middle Aged, Reference Values, Registries, Thyrotoxicosis, Thyrotropin, Cohort Studies, Incidence, Proportional Hazards Models, Survival Analysis, Young Adult, General Practice, Osteoporotic Fractures
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