Osteoporosis International

, Volume 25, Issue 5, pp 1571–1576 | Cite as

The relationship between pulmonary function and bone mineral density in healthy nonsmoking women: the Korean National Health and Nutrition Examination Survey (KNHANES) 2010

  • Y. K. Jeon
  • M. J. Shin
  • W. J. Kim
  • S. S. Kim
  • B. H. Kim
  • S. J. Kim
  • Y. K. Kim
  • Y. B. Shin
  • I. J. Kim
Original Article



The aim of this study was to examine the association between pulmonary function and bone mineral density (BMD) in subjects who had never smoked. Pulmonary function was associated with BMD in premenopausal, but not postmenopausal, women.


It has been reported that low bone mass is common in patients with pulmonary disorders such as chronic obstructive pulmonary disease. However, in healthy nonsmoking women, the relationship between bone mass and pulmonary function has yet to be clarified. The object of this study was to determine whether pulmonary function is related to BMD in healthy nonsmoking women based on menopausal status.


This study was a cross-sectional study based on data obtained from the Korean National Health and Nutrition Examination Survey (KNHANES), a nationwide representative survey conducted by the Korean Ministry of Health and Welfare in 2010. This study included 456 subjects who had never smoked and analyzed data concerning pulmonary function and BMD.


Functional vital capacity (FVC) and forced expiratory volume in 1 s (FEV1) were correlated with BMD at lumbar spine, femur neck (FN), and total hip in premenopausal women (p = 0.030, p = 0.003, p = 0.019, respectively, for FVC; p = 0.015, p = 0.006, p = 0.059, respectively, for FEV1). However, FVC and FEV1 were only correlated with BMD at FN in postmenopausal women (p = 0.003 for FVC; p = 0.006 for FEV1). Body mass index (BMI), FVC, and FEV1 were significantly related with BMD at FN, even after adjusting for age and other confounding factors (β = 0.334, p < 0.001; β = 0.145, p = 0.017; and β = 0.129, p = 0.037, respectively) in premenopausal women. However, only age and BMI were correlated with BMD at FN (β = −0.268, p = 0.001 and β = 0.384, p > 0.001) in postmenopausal women after adjusting for confounding factors.


Pulmonary function, including FVC and FEV1 are associated with BMD at FN in healthy nonsmoking premenopausal women but not in postmenopausal women.


Bone mineral density Osteoporosis Respiratory function Smoking 



Bone mineral density


Body mass index




25-Hydroxy vitamin D


Functional vital capacity


Forced expiratory volume in 1 s


Forced expiratory volume in 6 s


Forced expiratory flow rate of 25–75 %


Peak expiratory flow rate


Grant support


Conflicts of interest

The authors declare no conflicts of interest


  1. 1.
    Elkin SL, Fairney A, Burnett S, Kemp M, Kyd P, Burgess J, Compston JE, Hodson ME (2001) Vertebral deformities and low bone mineral density in adults with cystic fibrosis: a cross-sectional study. Osteoporos Int 12:366–372PubMedCrossRefGoogle Scholar
  2. 2.
    Graat-Verboom L, Spruit MA, van den Borne BE, Smeenk FW, Martens EJ, Lunde R, Wouters EF, Network CIRO (2009) Correlates of osteoporosis in chronic obstructive pulmonary disease: an underestimated systemic component. Respir Med 103:1143–1151PubMedCrossRefGoogle Scholar
  3. 3.
    Jorgensen NR, Schwarz P, Holme I, Henriksen BM, Petersen LJ, Backer V (2007) The prevalence of osteoporosis in patients with chronic obstructive pulmonary disease: a cross sectional study. Respir Med 101:177–185PubMedCrossRefGoogle Scholar
  4. 4.
    Ferguson GT, Calverley PM, Anderson JA, Jenkins CR, Jones PW, Willits LR, Yates JC, Vestbo J, Celli B (2009) Prevalence and progression of osteoporosis in patients with COPD: results from the towards a revolution in COPD health study. Chest 136:1456–1465PubMedCrossRefGoogle Scholar
  5. 5.
    Sin DD, Man JP, Man SF (2003) The risk of osteoporosis in Caucasian men and women with obstructive airways disease. Am J Med 114:10–14PubMedCrossRefGoogle Scholar
  6. 6.
    Incalzi RA, Caradonna P, Ranieri P, Basso S, Fuso L, Pagano F, Ciappi G, Pistelli R (2000) Correlates of osteoporosis in chronic obstructive pulmonary disease. Respir Med 94:1079–1084PubMedCrossRefGoogle Scholar
  7. 7.
    Dimai HP, Domej W, Leb G, Lau KH (2001) Bone loss in patients with untreated chronic obstructive pulmonary disease is mediated by an increase in bone resorption associated with hypercapnia. J Bone Miner Res 16:2132–2141PubMedCrossRefGoogle Scholar
  8. 8.
    Iqbal F, Michaelson J, Thaler L, Rubin J, Roman J, Nanes MS (1999) Declining bone mass in men with chronic pulmonary disease: contribution of glucocorticoid treatment, body mass index, and gonadal function. Chest 116:1616–1624PubMedCrossRefGoogle Scholar
  9. 9.
    Lekamwasam S, Trivedi DP, Khaw KT (2002) An association between respiratory function and bone mineral density in women from the general community: a cross sectional study. Osteoporos Int 13:710–715PubMedCrossRefGoogle Scholar
  10. 10.
    Choi JW, Pai SH (2004) Association between respiratory function and osteoporosis in pre- and postmenopausal women. Maturitas 48:253–258PubMedCrossRefGoogle Scholar
  11. 11.
    Dennison EM, Dhanwal DK, Shaheen SO, Azagra R, Reading I, Jameson KA, Sayer AA, Cooper C (2013) Is lung function associated with bone mineral density? Results from the Hertfordshire Cohort Study. Arch Osteoporos 8:115, 012–0115-yPubMedCentralPubMedCrossRefGoogle Scholar
  12. 12.
    Niewoehner DE, Kleinerman J, Rice DB (1974) Pathologic changes in the peripheral airways of young cigarette smokers. N Engl J Med 291:755–758PubMedCrossRefGoogle Scholar
  13. 13.
    Xu X, Weiss ST, Rijcken B, Schouten JP (1994) Smoking, changes in smoking habits, and rate of decline in FEV1: new insight into gender differences. Eur Respir J 7:1056–1061PubMedCrossRefGoogle Scholar
  14. 14.
    Law MR, Hackshaw AK (1997) A meta-analysis of cigarette smoking, bone mineral density and risk of hip fracture: recognition of a major effect. BMJ 315:841–846PubMedCentralPubMedCrossRefGoogle Scholar
  15. 15.
    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
  16. 16.
    Soen S, Fukunaga M, Sugimoto T, Sone T, Fujiwara S, Endo N, Gorai I, Shiraki M, Hagino H, Hosoi T, Ohta H, Yoneda T, Tomomitsu T, Japanese Society for Bone and Mineral Research and Japan Osteoporosis Society Joint Review Committee for the Revision of the Diagnostic Criteria for Primary Osteoporosis (2013) Diagnostic criteria for primary osteoporosis: year 2012 revision. J Bone Miner Metab 31:247–257PubMedCrossRefGoogle Scholar
  17. 17.
    Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J, ATS/ERS Task Force (2005) Standardisation of spirometry. Eur Respir J 26:319–338PubMedCrossRefGoogle Scholar
  18. 18.
    Jones G, Scott FS (1999) A cross-sectional study of smoking and bone mineral density in premenopausal parous women: effect of body mass index, breastfeeding, and sports participation. J Bone Miner Res 14:1628–1633PubMedCrossRefGoogle Scholar
  19. 19.
    Mazess RB, Barden HS (1991) Bone density in premenopausal women: effects of age, dietary intake, physical activity, smoking, and birth-control pills. Am J Clin Nutr 53:132–142PubMedGoogle Scholar
  20. 20.
    Krall EA, Dawson-Hughes B (1991) Smoking and bone loss among postmenopausal women. J Bone Miner Res 6:331–338PubMedCrossRefGoogle Scholar
  21. 21.
    Paganini-Hill A, Chao A, Ross RK, Henderson BE (1991) Exercise and other factors in the prevention of hip fracture: the leisure world study. Epidemiology 2:16–25PubMedCrossRefGoogle Scholar
  22. 22.
    Krall EA, Dawson-Hughes B (1999) Smoking increases bone loss and decreases intestinal calcium absorption. J Bone Miner Res 14:215–220PubMedCrossRefGoogle Scholar
  23. 23.
    Brot C, Jorgensen NR, Sorensen OH (1999) The influence of smoking on vitamin D status and calcium metabolism. Eur J Clin Nutr 53:920–926PubMedCrossRefGoogle Scholar
  24. 24.
    Barbieri RL, Gochberg J, Ryan KJ (1986) Nicotine, cotinine, and anabasine inhibit aromatase in human trophoblast in vitro. J Clin Invest 77:1727–1733PubMedCentralPubMedCrossRefGoogle Scholar
  25. 25.
    Duthie GG, Arthur JR, James WP (1991) Effects of smoking and vitamin E on blood antioxidant status. Am J Clin Nutr 53:1061S–1063SPubMedGoogle Scholar
  26. 26.
    Fang MA, Frost PJ, Iida-Klein A, Hahn TJ (1991) Effects of nicotine on cellular function in UMR 106-01 osteoblast-like cells. Bone 12:283–286PubMedCrossRefGoogle Scholar
  27. 27.
    Ramp WK, Lenz LG, Galvin RJ (1991) Nicotine inhibits collagen synthesis and alkaline phosphatase activity, but stimulates DNA synthesis in osteoblast-like cells. Proc Soc Exp Biol Med 197:36–43PubMedCrossRefGoogle Scholar
  28. 28.
    Nystad W, Samuelsen SO, Nafstad P, Langhammer A (2006) Association between level of physical activity and lung function among Norwegian men and women: the hunt study. Int J Tuberc Lung Dis 10:1399–1405PubMedGoogle Scholar
  29. 29.
    Berntsen S, Wisloff T, Nafstad P, Nystad W (2008) Lung function increases with increasing level of physical activity in school children. Pediatr Exerc Sci 20:402–410PubMedGoogle Scholar
  30. 30.
    Welten DC, Kemper HC, Post GB, Van Mechelen W, Twisk J, Lips P, Teule GJ (1994) Weight-bearing activity during youth is a more important factor for peak bone mass than calcium intake. J Bone Miner Res 9:1089–1096PubMedCrossRefGoogle Scholar
  31. 31.
    Muir JM, Ye C, Bhandari M, Adachi JD, Thabane L (2013) The effect of regular physical activity on bone mineral density in post-menopausal women aged 75 and over: a retrospective analysis from the Canadian multicentre osteoporosis study. BMC Musculoskeletal Disorder 14:253CrossRefGoogle Scholar

Copyright information

© International Osteoporosis Foundation and National Osteoporosis Foundation 2014

Authors and Affiliations

  • Y. K. Jeon
    • 1
    • 5
  • M. J. Shin
    • 2
    • 5
  • W. J. Kim
    • 1
    • 5
  • S. S. Kim
    • 1
    • 5
  • B. H. Kim
    • 1
    • 5
  • S. J. Kim
    • 3
    • 5
  • Y. K. Kim
    • 4
  • Y. B. Shin
    • 2
    • 5
  • I. J. Kim
    • 1
    • 5
  1. 1.Division of Endocrinology, Department of Internal MedicinePusan National University School of MedicineBusanKorea
  2. 2.Department of Rehabilitation Medicine, Pusan National University HospitalPusan National University School of MedicineBusanKorea
  3. 3.Department of Nuclear MedicinePusan National University School of MedicineBusanKorea
  4. 4.Kim Yong Ki Internal Medicine ClinicBusanKorea
  5. 5.Medical Research InstitutePusan National UniversityBusanKorea

Personalised recommendations