Osteoporosis International

, Volume 24, Issue 11, pp 2789–2799 | Cite as

Additive association of vitamin D insufficiency and sarcopenia with low femoral bone mineral density in noninstitutionalized elderly population: the Korea National Health and Nutrition Examination Surveys 2009–2010

  • S.-G. Lee
  • Y.-h. Lee
  • K. J. Kim
  • W. Lee
  • O. H. Kwon
  • J.-H. KimEmail author
Original Article



Vitamin D insufficiency and sarcopenia are crucial risk factors for osteoporosis. In a study of noninstitutionalized elderly subjects, we investigated the simultaneous effect of vitamin D and sarcopenia on bone mineral density (BMD) and found that sarcopenia was associated with low BMD in the femur, especially in those with suboptimal vitamin D levels.


Although vitamin D insufficiency and sarcopenia are prevalent in the elderly population worldwide, their possible influence on BMD has not been determined. We aimed to investigate the different effect of vitamin D insufficiency and sarcopenia on BMD in the elderly Korean population.


Individuals aged 60 or older were selected from those who participated in the Fourth and Fifth Korea National Health and Nutrition Examination Surveys conducted in 2009 and 2010; 1,596 males and 1,886 females were analyzed. Appendicular skeletal muscle mass (ASM) and BMD were assessed by dual-energy X-ray absorptiometry; serum 25-hydroxyvitamin D [25(OH)D] and a panel of clinical and laboratory parameters were also measured.


The study population was divided into four groups according to their vitamin D and sarcopenic status. BMD in total femur and in the femoral neck but not the lumbar spine was markedly decreased in sarcopenic subjects with vitamin D insufficiency [25(OH)D < 20 ng/ml] comparing to other groups, regardless of gender. Multivariable linear regression models showed that BMD was significantly associated with ASM and high daily calcium intake as well as conventional risk factors such as age, body mass index (BMI), and history of fracture. Independent predictors for low femur BMD included sarcopenia, low daily calcium intake, low 25(OH)D levels, age, and BMI.


These data showed that an association between vitamin D insufficiency and low BMD was more prominent in elderly subjects with sarcopenia.


Bone mineral density Femoral bone Sarcopenia Vitamin D insufficiency 


Conflicts of interest


Supplementary material

198_2013_2378_MOESM1_ESM.docx (29 kb)
ESM 1 (DOCX 28.7 KB)
198_2013_2378_Fig3_ESM.jpg (44 kb)
Supplementary Fig. 1

T-score of the (A) femoral neck, (B) total femur, (C) total lumbar spine according to vitamin D level and sarcopenia status (JPEG 43 kb)

198_2013_2378_MOESM2_ESM.tif (637 kb)
High resolution image (TIFF 636 KB)
198_2013_2378_Fig4_ESM.jpg (44 kb)
Supplementary Fig. 2

Differences in bone mineral density of (A) femoral neck, (B) total femur, and (C) lumbar spine according to vitamin D level and sarcopenia status defined by ASM/Ht2 (JPEG 44 kb)

198_2013_2378_MOESM3_ESM.tif (689 kb)
High resolution image (TIFF 689 kb)


  1. 1.
    Rachner TD, Khosla S, Hofbauer LC (2011) Osteoporosis: now and the future. Lancet 377:1276–1287PubMedCrossRefGoogle Scholar
  2. 2.
    Choi HS, Oh HJ, Choi H, Choi WH, Kim JG, Kim KM, Kim KJ, Rhee Y, Lim SK (2011) Vitamin D insufficiency in Korea—a greater threat to younger generation: the Korea National Health and Nutrition Examination Survey (KNHANES) 2008. J Clin Endocrinol Metab 96:643–651PubMedCrossRefGoogle Scholar
  3. 3.
    McGreevy C, Williams D (2011) New insights about vitamin D and cardiovascular disease: a narrative review. Ann Intern Med 155:820–826PubMedCrossRefGoogle Scholar
  4. 4.
    Lim JS, Hwang JS, Lee JA, Kim DH, Park KD, Cheon GJ, Shin CH, Yang SW (2010) Bone mineral density according to age, bone age, and pubertal stages in Korean children and adolescents. J Clin Densitom 13:68–76PubMedCrossRefGoogle Scholar
  5. 5.
    Frisoli A, Chaves PH, Ingham SJ, Fried LP (2011) Severe osteopenia and osteoporosis, sarcopenia, and frailty status in community-dwelling older women: results from the Women's Health and Aging Study (WHAS) II. Bone 48:952–957PubMedCrossRefGoogle Scholar
  6. 6.
    Pongchaiyakul C, Nguyen ND, Nguyen TV (2004) Development and validation of a new clinical risk index for prediction of osteoporosis in Thai women. Chot Mai Het Thang Phaet 87:910–916PubMedGoogle Scholar
  7. 7.
    Duan Y, Beck TJ, Wang X, Seeman E (2003) Structural and biomechanical basis of sexual dimorphism in femoral neck fragility has its origins in growth and aging. J Bone Miner Res 18:1766–1774PubMedCrossRefGoogle Scholar
  8. 8.
    Pluijm SM, Visser M, Smit JH, Popp-Snijders C, Roos JC, Lips P (2001) Determinants of bone mineral density in older men and women: body composition as mediator. J Bone Miner Res 16:2142–2151PubMedCrossRefGoogle Scholar
  9. 9.
    Frost HM (1987) The mechanostat: a proposed pathogenic mechanism of osteoporoses and the bone mass effects of mechanical and nonmechanical agents. Bone Miner 2:73–85PubMedGoogle Scholar
  10. 10.
    Montagnani A, Gonnelli S, Alessandri M, Nuti R (2011) Osteoporosis and risk of fracture in patients with diabetes: an update. Aging Clin and Exp Res 23:84–90Google Scholar
  11. 11.
    Kim TN, Park MS, Lim KI, Yang SJ, Yoo HJ, Kang HJ, Song W, Seo JA, Kim SG, Kim NH, Baik SH, Choi DS, Choi KM (2011) Skeletal muscle mass to visceral fat area ratio is associated with metabolic syndrome and arterial stiffness: The Korean Sarcopenic Obesity Study (KSOS). Diabetes Res Clin Pract 93:285–291PubMedCrossRefGoogle Scholar
  12. 12.
    Lim S, Kim JH, Yoon JW, Kang SM, Choi SH, Park YJ, Kim KW, Lim JY, Park KS, Jang HC (2010) Sarcopenic obesity: prevalence and association with metabolic syndrome in the Korean Longitudinal Study on Health and Aging (KLoSHA). Diabetes Care 33:1652–1654PubMedCrossRefGoogle Scholar
  13. 13.
    Cruz-Jentoft AJ, Landi F, Topinkova E, Michel JP (2010) Understanding sarcopenia as a geriatric syndrome. Curr Opin Clin Nutr Metab Care 13:1–7PubMedCrossRefGoogle Scholar
  14. 14.
    Stephen WC, Janssen I (2009) Sarcopenic-obesity and cardiovascular disease risk in the elderly. J Nutr Health Aging 13:460–466PubMedCrossRefGoogle Scholar
  15. 15.
    Waugh EJ, Lam MA, Hawker GA, McGowan J, Papaioannou A, Cheung AM, Hodsman AB, Leslie WD, Siminoski K, Jamal SA (2009) Risk factors for low bone mass in healthy 40–60 year old women: a systematic review of the literature. Osteoporos Int 20:1–21PubMedCrossRefGoogle Scholar
  16. 16.
    Papaioannou A, Kennedy CC, Cranney A, Hawker G, Brown JP, Kaiser SM, Leslie WD, O'Brien CJ, Sawka AM, Khan A, Siminoski K, Tarulli G, Webster D, McGowan J, Adachi JD (2009) Risk factors for low BMD in healthy men age 50 years or older: a systematic review. Osteoporos Int 20:507–518PubMedCrossRefGoogle Scholar
  17. 17.
    Montero-Odasso M, Duque G (2005) Vitamin D in the aging musculoskeletal system: an authentic strength preserving hormone. Mol Aspects Med 26:203–219PubMedCrossRefGoogle Scholar
  18. 18.
    Korea Centers for Disease Control and Prevention, Ministry of Health and Welfare, South Korea. Korea National Health and Nutrition Examination Survey (KNHANES). Accessed 20 Dec 2012
  19. 19.
    Lim S, Shin H, Song JH, Kwak SH, Kang SM, Won Yoon J, Choi SH, Cho SI, Park KS, Lee HK, Jang HC, Koh KK (2011) Increasing prevalence of metabolic syndrome in Korea: the Korean National Health and Nutrition Examination Survey for 1998–2007. Diabetes Care 34:1323–1328PubMedCrossRefGoogle Scholar
  20. 20.
    Organization WH (1994) WHO Technical Report Series No. 843: assessment of fracture risk and its application to screening for postmenopausal osteoporosis. WHO, GenevaGoogle Scholar
  21. 21.
    Janssen I, Heymsfield SB, Ross R (2002) Low relative skeletal muscle mass (sarcopenia) in older persons is associated with functional impairment and physical disability. J Am Geriatr Soc 50:889–896PubMedCrossRefGoogle Scholar
  22. 22.
    Lee YH, Bang H, Kim HC, Kim HM, Park SW, Kim DJ (2012) A simple screening score for diabetes for the Korean population: development, validation, and comparison with other scores. Diabetes Care 35:1723–1730PubMedCrossRefGoogle Scholar
  23. 23.
    Hwang YC, Ahn HY, Jeong IK, Ahn KJ, Chung HY (2013) Optimal serum concentration of 25-hydroxyvitamin D for bone health in older Korean adults. Calcif Tissue Int 92:68–74PubMedCrossRefGoogle Scholar
  24. 24.
    Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412–419PubMedCrossRefGoogle Scholar
  25. 25.
    World Health Organization Western Pacific Region IAftSoO (2000) The Asia-Pacific perspective: redefining obesity and its treatment. Health Communications Australia, Sydney, pp 15–21Google Scholar
  26. 26.
    MacLaughlin J, Holick MF (1985) Aging decreases the capacity of human skin to produce vitamin D3. J Clin Invest 76:1536–1538PubMedCrossRefGoogle Scholar
  27. 27.
    Morley JE, Argiles JM, Evans WJ, Bhasin S, Cella D, Deutz NE, Doehner W, Fearon KC, Ferrucci L, Hellerstein MK, Kalantar-Zadeh K, Lochs H, MacDonald N, Mulligan K, Muscaritoli M, Ponikowski P, Posthauer ME, Rossi Fanelli F, Schambelan M, Schols AM, Schuster MW, Anker SD (2010) Nutritional recommendations for the management of sarcopenia. J Am Med Dir Assoc 11:391–396PubMedCrossRefGoogle Scholar
  28. 28.
    Bischoff-Ferrari HA, Dawson-Hughes B, Willett WC, Staehelin HB, Bazemore MG, Zee RY, Wong JB (2004) Effect of vitamin D on falls: a meta-analysis. JAMA 291:1999–2006PubMedCrossRefGoogle Scholar
  29. 29.
    Saquib N, von Muhlen D, Garland CF, Barrett-Connor E (2006) Serum 25-hydroxyvitamin D, parathyroid hormone, and bone mineral density in men: the Rancho Bernardo study. Osteoporos Int 17:1734–1741PubMedCrossRefGoogle Scholar
  30. 30.
    von Muhlen DG, Greendale GA, Garland CF, Wan L, Barrett-Connor E (2005) Vitamin D, parathyroid hormone levels and bone mineral density in community-dwelling older women: the Rancho Bernardo Study. Osteoporos Int 16:1721–1726CrossRefGoogle Scholar
  31. 31.
    Walsh MC, Hunter GR, Livingstone MB (2006) Sarcopenia in premenopausal and postmenopausal women with osteopenia, osteoporosis and normal bone mineral density. Osteoporos Int 17:61–67PubMedCrossRefGoogle Scholar
  32. 32.
    Kim MK, Baek KH, Song KH, Il Kang M, Park CY, Lee WY, Oh KW (2011) Vitamin D deficiency is associated with sarcopenia in older Koreans, regardless of obesity: the Fourth Korea National Health and Nutrition Examination Surveys (KNHANES IV) 2009. J Clin Endocrinol Metab 96:3250–3256PubMedCrossRefGoogle Scholar
  33. 33.
    Sowers M, Crutchfield M, Bandekar R, Randolph JF, Shapiro B, Schork MA, Jannausch M (1998) Bone mineral density and its change in pre-and perimenopausal white women: the Michigan Bone Health Study. J of Bone and Mineral Res 13:1134–1140CrossRefGoogle Scholar
  34. 34.
    Liu-Ambrose T, Kravetsky L, Bailey D, Sherar L, Mundt C, Baxter-Jones A, Khan KM, McKay HA (2006) Change in lean body mass is a major determinant of change in areal bone mineral density of the proximal femur: a 12-year observational study. Calcif Tissue Int 79:145–151PubMedCrossRefGoogle Scholar
  35. 35.
    Schoffl I, Kemmler W, Kladny B, Vonstengel S, Kalender WA, Engelke K (2008) In healthy elderly postmenopausal women variations in BMD and BMC at various skeletal sites are associated with differences in weight and lean body mass rather than by variations in habitual physical activity, strength or VO2max. J Musculoskelet Neuronal Interact 8:363–374PubMedGoogle Scholar
  36. 36.
    Binkley N (2012) Vitamin D and osteoporosis-related fracture. Arch Biochem Biophys 523:115–122PubMedCrossRefGoogle Scholar
  37. 37.
    Muraki S, Yamamoto S, Ishibashi H, Horiuchi T, Hosoi T, Orimo H, Nakamura K (2004) Impact of degenerative spinal diseases on bone mineral density of the lumbar spine in elderly women. Osteoporos Int 15:724–728PubMedCrossRefGoogle Scholar
  38. 38.
    von der Recke P, Hansen MA, Overgaard K, Christiansen C (1996) The impact of degenerative conditions in the spine on bone mineral density and fracture risk prediction. Osteoporos Int 6:43–49PubMedCrossRefGoogle Scholar
  39. 39.
    Drinka PJ, DeSmet AA, Bauwens SF, Rogot A (1992) The effect of overlying calcification on lumbar bone densitometry. Calcif Tissue Int 50:507–510PubMedCrossRefGoogle Scholar
  40. 40.
    Reid IR, Evans MC, Ames R, Wattie DJ (1991) The influence of osteophytes and aortic calcification on spinal mineral density in postmenopausal women. J Clin Endocrinol Metab 72:1372–1374PubMedCrossRefGoogle Scholar
  41. 41.
    Orwoll ES, Oviatt SK, Mann T (1990) The impact of osteophytic and vascular calcifications on vertebral mineral density measurements in men. J Clin Endocrinol Metab 70:1202–1207PubMedCrossRefGoogle Scholar
  42. 42.
    Cummings SR, Bates D, Black DM (2002) Clinical use of bone densitometry: scientific review. JAMA 288:1889–1897PubMedCrossRefGoogle Scholar
  43. 43.
    Cummings SR, Black DM, Nevitt MC, Browner W, Cauley J, Ensrud K, Genant HK, Palermo L, Scott J, Vogt TM (1993) Bone density at various sites for prediction of hip fractures. The Study of Osteoporotic Fractures Research Group. Lancet 341:72–75PubMedCrossRefGoogle Scholar
  44. 44.
    Avenell A, Gillespie WJ, Gillespie LD, O'Connell D (2009) Vitamin D and vitamin D analogues for preventing fractures associated with involutional and post-menopausal osteoporosis. Cochrane Database Syst Rev:CD000227Google Scholar
  45. 45.
    Cui LH, Shin MH, Kweon SS, Park KS, Lee YH, Chung EK, Nam HS, Choi JS (2007) Relative contribution of body composition to bone mineral density at different sites in men and women of South Korea. J Bone Miner Metab 25:165–171PubMedCrossRefGoogle Scholar
  46. 46.
    Petit MA, Beck TJ, Lin HM, Bentley C, Legro RS, Lloyd T (2004) Femoral bone structural geometry adapts to mechanical loading and is influenced by sex steroids: the Penn State Young Women’s Health Study. Bone 35:750–759PubMedCrossRefGoogle Scholar
  47. 47.
    Genaro PS, Pereira GA, Pinheiro MM, Szejnfeld VL, Martini LA (2010) Influence of body composition on bone mass in postmenopausal osteoporotic women. Arch Gerontol Geriatr 51:295–298PubMedCrossRefGoogle Scholar
  48. 48.
    Lips P, Bouillon R, van Schoor NM, Vanderschueren D, Verschueren S, Kuchuk N, Milisen K, Boonen S (2010) Reducing fracture risk with calcium and vitamin D. Clin Endocrinol (Oxf) 73:277–285CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2013

Authors and Affiliations

  • S.-G. Lee
    • 1
    • 2
    • 3
  • Y.-h. Lee
    • 3
    • 4
  • K. J. Kim
    • 4
    • 5
  • W. Lee
    • 2
  • O. H. Kwon
    • 2
  • J.-H. Kim
    • 2
    Email author
  1. 1.Department of Laboratory MedicineArmed Forces Capital HospitalSeongnamSouth Korea
  2. 2.Department of Laboratory MedicineYonsei University College of MedicineSeoulSouth Korea
  3. 3.Graduate SchoolYonsei University College of MedicineSeoulSouth Korea
  4. 4.Department of Internal MedicineYonsei University College of MedicineSeoulSouth Korea
  5. 5.Severance Executive Healthcare ClinicYonsei University Health SystemSeoulSouth Korea

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