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Subclinical thyroid dysfunction, bone mineral density, and osteoporosis in a middle-aged Korean population

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Abstract

Summary

Thyroid dysfunction is associated with the loss of bone density (osteoporosis). However, the connection between subclinical thyroid dysfunction and osteoporosis remains controversial. This study found no apparent association between subclinical hypothyroidism or subclinical hyperthyroidism and bone mineral density (BMD) in the lumbar spine and femur.

Introduction

The present study examined the relationship between subclinical thyroid dysfunction and BMD in healthy middle-aged adults.

Methods

A total of 25,510 healthy Koreans with normal free thyroxine levels were enrolled from January 2011 to December 2016, and 91% of subjects visited only once. The average age of the 15,761 women was 45, and the average age of the 9749 men was 48. Levels of thyroid-stimulating hormone (TSH) and BMD were recorded in all subjects. BMD was measured using dual-energy X-ray absorptiometry.

Results

No apparent association was found between subclinical thyroid dysfunction and BMD in the lumbar spine, femur-neck, and proximal femur sites compared with a euthyroid group. Age, body mass index (BMI), and postmenopausal status affected BMD in women, and only BMI affected BMD in men. Subclinical hypothyroidism was independently associated with a lower risk of osteoporosis (odds ratio 0.657, 95% confidence interval 0.464–0.930) in 4710 postmenopausal women.

Conclusions

No apparent association was found between subclinical hypothyroidism or subclinical hyperthyroidism defined on single TSH measurement and BMD at the lumbar spine and femur in a large cohort of middle-aged men and women. Subclinical hypothyroidism was independently associated with a lower risk of osteoporosis in postmenopausal women.

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References

  1. Wilson GR, Curry RW Jr (2005) Subclinical thyroid disease. Am Fam Physician 72:1517–1524

    PubMed  Google Scholar 

  2. Bahn Chair RS, Burch HB, Cooper DS, Garber JR, Greenlee MC, Klein I, Laurberg P, McDougall I, Montori VM, Rivkees SA, Ross DS, Sosa JA, Stan MN, American Thyroid Association, American Association of Clinical Endocrinologists (2011) Hyperthyroidism and other causes of thyrotoxicosis: management guidelines of the American Thyroid Association and American Association of Clinical Endocrinologists. Thyroid 21:593–646

    Article  Google Scholar 

  3. Garber JR, Cobin RH, Gharib H, Hennessey JV, Klein I, Mechanick JI, Pessah-Pollack R, Singer PA, Woeber KA, American Association Of Clinical Endocrinologists And American Thyroid Association Taskforce On Hypothyroidism In Adults (2012) Clinical practice guidelines for hypothyroidism in adults: cosponsored by the American Association of Clinical Endocrinologists and the American Thyroid Association. Thyroid 22:1200–1235

    Article  CAS  Google Scholar 

  4. Garmendia Madariaga A, Santos Palacios S, Guillén-Grima F, Galofré JC (2014) The incidence and prevalence of thyroid dysfunction in Europe: a meta-analysis. J Clin Endocrinol Metab 99:923–931

    Article  Google Scholar 

  5. Foldes J, Tarjan G, Szathmari M et al (1993) Bone mineral density in patients with endogenous subclinical hyperthyroidism: is this thyroid status a risk factor for osteoporosis? Clin Endocrinol 39:521–527

    Article  CAS  Google Scholar 

  6. Vestergaard P, Mosekilde L (2002) Fractures in patients with hyperthyroidism and hypothyroidism: a nationwide follow-up study in 16,249 patients. Thyroid 12:411–419

    Article  Google Scholar 

  7. Gogakos AI, Duncan Bassett JH, Williams GR (2010) Thyroid and bone. Arch Biochem Biophys 503:129–136

    Article  CAS  Google Scholar 

  8. Lee WY, Oh KW, Rhee EJ, Jung CH, Kim SW, Yun EJ, Tae HJ, Baek KH, Kang MI, Choi MG, Yoo HJ, Park SW (2006) Relationship between subclinical thyroid dysfunction and femoral neck bone mineral density in women. Arch Med Res 37:511–516

    Article  CAS  Google Scholar 

  9. Garin MC, Arnold AM, Lee JS, Robbins J, Cappola AR (2014) Subclinical thyroid dysfunction and hip fracture and bone mineral density in older adults: the cardiovascular health study. J Clin Endocrinol Metab 99:2657–2664

    Article  CAS  Google Scholar 

  10. Yang R, Yao L, Fang Y, Sun J, Guo T, Yang K, Tian L (2018) The relationship between subclinical thyroid dysfunction and the risk of fracture or low bone mineral density: a systematic review and meta-analysis of cohort studies. J Bone Miner Metab 36:209–220

    Article  Google Scholar 

  11. Vadiveloo T, Donnan PT, Cochrane L, Leese GP (2011) The thyroid epidemiology, audit, and research study (TEARS): morbidity in patients with endogenous subclinical hyperthyroidism. J Clin Endocrinol Metab 96:1344–1351

    Article  CAS  Google Scholar 

  12. Svare A, Nilsen TI, Asvold BO, Forsmo S, Schei B, Bjøro T, Langhammer A (2013) Does thyroid function influence fracture risk? Prospective data from the HUNT2 study, Norway. Eur J Endocrinol 169:845–852

    Article  CAS  Google Scholar 

  13. Kim M, Kim TY, Kim SH, Lee Y, Park SY, Kim HD, Kwon H, Choi YM, Jang EK, Jeon MJ, Kim WG, Shong YK, Kim WB (2015) Reference interval for thyrotropin in a ultrasonography screened Korean population. Korean J Intern Med 30:335–344

    Article  CAS  Google Scholar 

  14. Park SY, Kim HI, Oh HK et al (2018) Age- and gender-specific reference intervals of TSH and free T4 in an iodine-replete area: Data from Korean National Health and Nutrition Examination Survey IV (2013-2015). PLoS One 13:e0190738

    Article  Google Scholar 

  15. Chang Y, Kim BK, Yun KE, Cho J, Zhang Y, Rampal S, Zhao D, Jung HS, Choi Y, Ahn J, Lima JA, Shin H, Guallar E, Ryu S (2014) Metabolically-healthy obesity and coronary artery calcification. J Am Coll Cardiol 63:2679–2686

    Article  Google Scholar 

  16. Kim MK, Lee WY, Kang JH et al (2014) 2014 clinical practice guidelines for overweight and obesity in Korea. Endocrinol Metab (Seoul) 29:405–409

    Article  Google Scholar 

  17. Kanis JA (1994) Assessment of fracture risk and its application to screening for postmenopausal osteoporosis: synopsis of a WHO report. WHO Study Group. Osteoporos Int 4:368–381

    Article  CAS  Google Scholar 

  18. Lewiecki EM, Gordon CM, Baim S, Leonard MB, Bishop NJ, Bianchi ML, Kalkwarf HJ, Langman CB, Plotkin H, Rauch F, Zemel BS, Binkley N, Bilezikian JP, Kendler DL, Hans DB, Silverman S (2008) International Society for Clinical Densitometry 2007 Adult and Pediatric Official Positions. Bone 43:1115–1121

    Article  Google Scholar 

  19. Kim TH, Joung JY, Kang M et al (2015) A modest protective effect of thyrotropin against bone loss is associated with plasma triiodothyronine levels. PLoS One 10:e0145292

    Article  Google Scholar 

  20. Blum MR, Bauer DC, Collet TH, Fink HA, Cappola AR, da Costa BR, Wirth CD, Peeters RP, Åsvold BO, den Elzen W, Luben RN, Imaizumi M, Bremner AP, Gogakos A, Eastell R, Kearney PM, Strotmeyer ES, Wallace ER, Hoff M, Ceresini G, Rivadeneira F, Uitterlinden AG, Stott DJ, Westendorp RG, Khaw KT, Langhammer A, Ferrucci L, Gussekloo J, Williams GR, Walsh JP, Jüni P, Aujesky D, Rodondi N, Thyroid Studies Collaboration (2015) Subclinical thyroid dysfunction and fracture risk: a meta-analysis. JAMA 313:2055–2065

    Article  Google Scholar 

  21. Wartofsky L (2014) Subclinical hyperthyroidism and fracture risk in women. J Clin Endocrinol Metab 99:2654–2656

    Article  CAS  Google Scholar 

  22. Kim DJ, Khang YH, Koh JM et al (2006) Low normal TSH levels are associated with low bone mineral density in healthy postmenopausal women. Clin Endocrinol 64:86–90

    Article  CAS  Google Scholar 

  23. Ding B, Zhang Y, Li Q, Hu Y, Tao XJ, Liu BL, Ma JH, Li DM (2016) Low thyroid stimulating hormone levels are associated with low bone mineral density in femoral neck in elderly women. Arch Med Res 47:310–314

    Article  Google Scholar 

  24. 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

    Article  CAS  Google Scholar 

  25. Kim BJ, Lee SH, Bae SJ, Kim HK, Choe JW, Kim HY, Koh JM, Kim GS (2010) The association between serum thyrotropin (TSH) levels and bone mineral density in healthy euthyroid men. Clin Endocrinol 73:396–403

    Article  CAS  Google Scholar 

  26. Murphy E, Gluer CC, Reid DM et al (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

    Article  CAS  Google Scholar 

  27. Saler T, Ahbab S, Saglam ZA et al (2014) Endogenous subclinical hyperthyroidism may not lead to bone loss in premenopausal women. Hippokratia 18:240–244

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Abrahamsen B, Jorgensen HL, Laulund AS et al (2014) Low serum thyrotropin level and duration of suppression as a predictor of major osteoporotic fractures-the OPENTHYRO register cohort. J Bone Miner Res 29:2040–2050

    Article  CAS  Google Scholar 

  29. Abrahamsen B, Jorgensen HL, Laulund AS et al (2015) The excess risk of major osteoporotic fractures in hypothyroidism is driven by cumulative hyperthyroid as opposed to hypothyroid time: an observational register-based time-resolved cohort analysis. J Bone Miner Res 30:898–905

    Article  CAS  Google Scholar 

  30. Schneider C, Feller M, Bauer DC et al. (2018) Initial evaluation of thyroid dysfunction—are simultaneous TSH and fT4 tests necessary? PLoS One 13:e0196631

  31. Kim WG, Kim WB, Woo G et al (2017) Thyroid stimulating hormone reference range and prevalence of thyroid dysfunction in the Korean population: Korea National Health and Nutrition Examination Survey 2013 to 2015. Endocrinol Metab 32:106–114

    Article  Google Scholar 

  32. Biondi B (2012) Natural history, diagnosis and management of subclinical thyroid dysfunction. Best Pract Res Clin Endocrinol Metab 26:431–446

    Article  CAS  Google Scholar 

  33. Cheserek MJ, Wu GR, Ntazinda A, Shi YH, Shen LY, le GW (2015) Association between thyroid hormones, lipids and oxidative stress markers in subclinical hypothyroidism. J Med Biochem 34:323–331

    Article  CAS  Google Scholar 

  34. Erdogan M, Kosenli A, Ganidagli S et al (2012) Characteristics of anemia in subclinical and overt hypothyroid patients. Endocr J 59:213–220

    Article  CAS  Google Scholar 

  35. Sengul E, Cetinarslan B, Tarkun I et al (2004) Homocysteine concentrations in subclinical hypothyroidism. Endocr Res 30:351–359

    Article  Google Scholar 

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Acknowledgments

We would like to thank the staff of the Kangbuk Samsung Cohort Study for their hard work, dedication and continuing support.

Funding

This work was supported by a National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (No. 2017R1D1A1B03036425).

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Authors and Affiliations

  1. Department of Laboratory Medicine, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Korea

    K. Lee, S. Lim, H. Park, H.Y. Woo & M.J. Kwon

  2. Center for Cohort Studies, Total Healthcare Center, Kangbuk Samsung Hospital, Sungkyunkwan University School of Medicine, Seoul, Korea

    Y. Chang, E. Sung, H.S. Jung, K.E. Yun, C.W. Kim, S. Ryu & M.J. Kwon

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  1. K. Lee
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  2. S. Lim
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  3. H. Park
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  11. M.J. Kwon
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Correspondence to M.J. Kwon.

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Lee, K., Lim, S., Park, H. et al. Subclinical thyroid dysfunction, bone mineral density, and osteoporosis in a middle-aged Korean population. Osteoporos Int 31, 547–555 (2020). https://doi.org/10.1007/s00198-019-05205-1

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  • DOI: https://doi.org/10.1007/s00198-019-05205-1

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