J Korean Med Sci.  2022 Feb;37(8):e66. 10.3346/jkms.2022.37.e66.

Relationships Between Pulmonary Function and Composite Indices of Femoral Neck Strength in Korean Men (KNHANES IV)

• KMID: 2526803
• DOI: http://doi.org/10.3346/jkms.2022.37.e66

Abstract

Background
Despite the close relationship between osteoporosis and chronic pulmonary diseases, few studies have evaluated relationships between pulmonary functions and bone quality. We investigated associations between pulmonary function test results and femoral neck strength indices (SIs) in Korean men.
Methods
This population-based, cross-sectional study was conducted using data from the Korea National Health and Nutrition Examination Survey IV on 936 men aged ≥ 19 years. Pulmonary functions (forced vital capacity [FVC] and forced expiratory volume in one second [FEV₁ ]) were measured using a dry rolling seal spirometer. Femoral neck SIs, relative to load, were calculated by hip dual-energy X-ray absorptiometry for compression strength index (CSI), bending strength index (BSI), and impact strength index (ISI).
Results
The 443 (47.3%) of the 936 men were current smokers. FVC, FVC percentage with respect to the expected normal value, FEV₁ , and FEV₁ percentage with respect to the expected normal value (FEV ₁ p) were positively associated with CSI and BSI after adjusting for confounders, including smoking history (β = 0.003–0.223, P = 0.005–0.036). FEV₁ and FEV₁ p were positively associated with ISI (β = 0.000–0.014, P = 0.010–0.025). Of components of femoral neck SIs, bone mineral density was correlated with FEV₁ and FEV₁ p (β = 0.001–0.037, P = 0.017–0.019). After adjusting for all confounders, all femoral neck SIs increased with FVC quintiles (P for trends = 0.001–0.012), and CSI and BSI increased with FEV₁ quintiles (Pfor trends = 0.034–0.043).
Conclusion
Reduced pulmonary function was correlated with reduced femoral neck strength, even after adjusting for smoking history in Korean men. Femoral neck SIs might be useful tools for evaluating bone health in men with reduced pulmonary function.

Keyword

Bone Quality; Composite Indices of Femoral Neck Strength; Osteoporosis; Pulmonary Function Test

Figure

• 

  Fig. 1 Femoral neck strengths by (A) FVC and (B) FEV1 quintiles. The multivariate model was adjusted for age, weight, height, 25-hydroxy vitamin D, calcium intake, phosphorus intake, physical activity, and drinking. Values are expressed as least-square means with 95% CI unless otherwise specified. P values for trends were generated by multiple linear regression analysis.FVC = forced vital capacity, FEV1 = forced expiratory volume in one second, CSI = compression strength index, BSI = bending strength index, ISI = impact strength index.a P < 0.05 vs. Q5 by post hoc analysis.

Reference

1. Okazaki R, Watanabe R, Inoue D. Osteoporosis associated with chronic obstructive pulmonary disease. J Bone Metab. 2016; 23(3):111–120. PMID: 27622174.

2. Graat-Verboom L, Wouters EF, Smeenk FW, van den Borne BE, Lunde R, Spruit MA. Current status of research on osteoporosis in COPD: a systematic review. Eur Respir J. 2009; 34(1):209–218. PMID: 19567604.

3. Kjensli A, Falch JA, Ryg M, Blenk T, Armbrecht G, Diep LM, et al. High prevalence of vertebral deformities in COPD patients: relationship to disease severity. Eur Respir J. 2009; 33(5):1018–1024. PMID: 19129288.

4. Graat-Verboom L, van den Borne BE, Smeenk FW, Spruit MA, Wouters EF. Osteoporosis in COPD outpatients based on bone mineral density and vertebral fractures. J Bone Miner Res. 2011; 26(3):561–568. PMID: 20878771.

5. Watanabe R, Tanaka T, Aita K, Hagiya M, Homma T, Yokosuka K, et al. Osteoporosis is highly prevalent in Japanese males with chronic obstructive pulmonary disease and is associated with deteriorated pulmonary function. J Bone Miner Metab. 2015; 33(4):392–400. PMID: 24996527.

6. Choi JW, Pai SH. Association between respiratory function and osteoporosis in pre- and postmenopausal women. Maturitas. 2004; 48(3):253–258. PMID: 15207891.

7. Jeon YK, Shin MJ, Kim WJ, Kim SS, Kim BH, Kim SJ, et al. The relationship between pulmonary function and bone mineral density in healthy nonsmoking women: the Korean National Health and Nutrition Examination Survey (KNHANES) 2010. Osteoporos Int. 2014; 25(5):1571–1576. PMID: 24577346.

8. Unnanuntana A, Rebolledo BJ, Khair MM, DiCarlo EF, Lane JM. Diseases affecting bone quality: beyond osteoporosis. Clin Orthop Relat Res. 2011; 469(8):2194–2206. PMID: 21107923.

9. Vestergaard P. Discrepancies in bone mineral density and fracture risk in patients with type 1 and type 2 diabetes--a meta-analysis. Osteoporos Int. 2007; 18(4):427–444. PMID: 17068657.

10. Johnell O, Kanis JA. An estimate of the worldwide prevalence and disability associated with osteoporotic fractures. Osteoporos Int. 2006; 17(12):1726–1733. PMID: 16983459.

11. Cawthon PM. Gender differences in osteoporosis and fractures. Clin Orthop Relat Res. 2011; 469(7):1900–1905. PMID: 21264553.

12. Rinonapoli G, Ruggiero C, Meccariello L, Bisaccia M, Ceccarini P, Caraffa A. Osteoporosis in men: a review of an underestimated bone condition. Int J Mol Sci. 2021; 22(4):2105. PMID: 33672656.

13. Center JR, Nguyen TV, Schneider D, Sambrook PN, Eisman JA. Mortality after all major types of osteoporotic fracture in men and women: an observational study. Lancet. 1999; 353(9156):878–882. PMID: 10093980.

14. Koh GC, Tai BC, Ang LW, Heng D, Yuan JM, Koh WP. All-cause and cause-specific mortality after hip fracture among Chinese women and men: the Singapore Chinese Health Study. Osteoporos Int. 2013; 24(7):1981–1989. PMID: 23224227.

15. Ahn SH, Park SM, Park SY, Yoo JI, Jung HS, Nho JH, et al. Osteoporosis and osteoporotic fracture fact sheet in Korea. J Bone Metab. 2020; 27(4):281–290. PMID: 33317231.

16. Karlamangla AS, Barrett-Connor E, Young J, Greendale GA. Hip fracture risk assessment using composite indices of femoral neck strength: the Rancho Bernardo study. Osteoporos Int. 2004; 15(1):62–70. PMID: 14605798.

17. Ahlborg HG, Nguyen ND, Nguyen TV, Center JR, Eisman JA. Contribution of hip strength indices to hip fracture risk in elderly men and women. J Bone Miner Res. 2005; 20(10):1820–1827. PMID: 16160739.

18. Korea Disease Control and Prevention Agency. The Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV). Cheongju, Korea: Korea Centers for Disease Control and Prevention;2008.

19. Kelly TL, Wilson KE, Heymsfield SB. Dual energy X-ray absorptiometry body composition reference values from NHANES. PLoS One. 2009; 4(9):e7038. PMID: 19753111.

20. Lee EY, Kim D, Kim KM, Kim KJ, Choi HS, Rhee Y, et al. Age-related bone mineral density patterns in Koreans (KNHANES IV). J Clin Endocrinol Metab. 2012; 97(9):3310–3318. PMID: 22701016.

21. Beck TJ, Looker AC, Ruff CB, Sievanen H, Wahner HW. Structural trends in the aging femoral neck and proximal shaft: analysis of the Third National Health and Nutrition Examination Survey dual-energy X-ray absorptiometry data. J Bone Miner Res. 2000; 15(12):2297–2304. PMID: 11127194.

22. Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, et al. Standardisation of spirometry. Eur Respir J. 2005; 26(2):319–338. PMID: 16055882.

23. Vrieze A, de Greef MH, Wijkstra PJ, Wempe JB. Low bone mineral density in COPD patients related to worse lung function, low weight and decreased fat-free mass. Osteoporos Int. 2007; 18(9):1197–1202. PMID: 17347789.

24. Dimai HP, Domej W, Leb G, Lau KH. 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. 2001; 16(11):2132–2141. PMID: 11697811.

25. Joo H, Park J, Lee SD, Oh YM. Comorbidities of chronic obstructive pulmonary disease in Koreans: a population-based study. J Korean Med Sci. 2012; 27(8):901–906. PMID: 22876057.

26. Leslie WD, Krieg MA, Hans D. Manitoba Bone Density Program. Clinical factors associated with trabecular bone score. J Clin Densitom. 2013; 16(3):374–379. PMID: 23452869.

27. Kulak CA, Borba VC, Jorgetti V, Dos Reis LM, Liu XS, Kimmel DB, et al. Skeletal microstructural abnormalities in postmenopausal women with chronic obstructive pulmonary disease. J Bone Miner Res. 2010; 25(9):1931–1940. PMID: 20564248.

28. Dennison EM, Dhanwal DK, Shaheen SO, Azagra R, Reading I, Jameson KA, et al. Is lung function associated with bone mineral density? Results from the Hertfordshire Cohort Study. Arch Osteoporos. 2013; 8:115. PMID: 23322029.

29. Zeng X, Liu D, Zhao X, Chao L, Li Y, Li H, et al. Association of bone mineral density with lung function in a Chinese general population: the Xinxiang rural cohort study. BMC Pulm Med. 2019; 19(1):239. PMID: 31818275.

30. Crabtree NJ, Kroger H, Martin A, Pols HA, Lorenc R, Nijs J, et al. Improving risk assessment: hip geometry, bone mineral distribution and bone strength in hip fracture cases and controls. The EPOS study. European Prospective Osteoporosis Study. Osteoporos Int. 2002; 13(1):48–54. PMID: 11883408.

31. Danielson ME, Beck TJ, Karlamangla AS, Greendale GA, Atkinson EJ, Lian Y, et al. A comparison of DXA and CT based methods for estimating the strength of the femoral neck in post-menopausal women. Osteoporos Int. 2013; 24(4):1379–1388. PMID: 22810918.

32. Ishii S, Cauley JA, Greendale GA, Crandall CJ, Danielson ME, Ouchi Y, et al. C-reactive protein, bone strength, and nine-year fracture risk: data from the Study of Women’s Health Across the Nation (SWAN). J Bone Miner Res. 2013; 28(7):1688–1698. PMID: 23456822.

33. Kim BJ, Ahn SH, Kim HM, Lee SH, Koh JM. Low skeletal muscle mass associates with low femoral neck strength, especially in older Korean women: the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV). Osteoporos Int. 2015; 26(2):737–747. PMID: 25391247.

34. Sarkar M, Bhardwaj R, Madabhavi I, Khatana J. Osteoporosis in chronic obstructive pulmonary disease. Clin Med Insights Circ Respir Pulm Med. 2015; 9:5–21. PMID: 25788838.

35. Sapey E, Ahmad A, Bayley D, Newbold P, Snell N, Rugman P, et al. Imbalances between interleukin-1 and tumor necrosis factor agonists and antagonists in stable COPD. J Clin Immunol. 2009; 29(4):508–516. PMID: 19291375.

36. Theoleyre S, Wittrant Y, Tat SK, Fortun Y, Redini F, Heymann D. The molecular triad OPG/RANK/RANKL: involvement in the orchestration of pathophysiological bone remodeling. Cytokine Growth Factor Rev. 2004; 15(6):457–475. PMID: 15561602.

37. Kneidinger N, Yildirim AÖ, Callegari J, Takenaka S, Stein MM, Dumitrascu R, et al. Activation of the WNT/β-catenin pathway attenuates experimental emphysema. Am J Respir Crit Care Med. 2011; 183(6):723–733. PMID: 20889911.

38. Arnett TR. Acidosis, hypoxia and bone. Arch Biochem Biophys. 2010; 503(1):103–109. PMID: 20655868.

39. Park JH, Park BH, Kim HK, Park TS, Baek HS. Hypoxia decreases Runx2/Cbfa1 expression in human osteoblast-like cells. Mol Cell Endocrinol. 2002; 192(1-2):197–203. PMID: 12088880.

40. Lau RY, Guo X. A review on current osteoporosis research: with special focus on disuse bone loss. J Osteoporos. 2011; 2011:293808. PMID: 21876833.

41. Lee SH, Kwon HY. Prevalence of osteoporosis in Korean patients with chronic obstructive pulmonary disease and their health-related quality of life according to the Korea National Health and Nutrition Examination Survey 2008-2011. J Bone Metab. 2017; 24(4):241–248. PMID: 29259964.