Abstract
Smoking induces bone loss; however, data on the relationship between smoking history and bone mineral density (BMD) are lacking. Age and pulmonary function can affect BMD. We investigated the relationships among pack-years (PYs) of smoking, pulmonary function, and BMD in middle-aged Korean men (50–64 years old). This cross-sectional study used data from the Korean National Health and Nutrition Examination Survey, 2008–2011. All participants underwent BMD measurements using dual energy X-ray absorptiometry and pulmonary function tests using standardized spirometry. In total, 388 never-smokers and 1088 ever-smokers were analyzed. The number of PYs of smoking was negatively correlated with total hip BMD (r = −0.088; P = 0.004) after adjusting for age, height, and weight. Ever-smokers were classified into 3 groups according to PYs of smoking. The highest tertile (n = 482) exhibited significantly lower total hip bone mass than the lowest tertile (n = 214) after adjusting for confounding factors (age, height, weight, forced expiratory volume in 1 s (FEV1), alcohol consumption, physical activity, and vitamin D levels) that could affect bone metabolism (P = 0.003). In conclusion, smoking for >30 PYs was significantly associated with low hip BMD after adjusting for pulmonary function in middle-aged Korean men. Long-term smoking may be a risk factor for bone loss in middle-aged men independent of age, height, weight, and pulmonary function.
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References
Park EJ, Joo IW, Jang MJ, Kim YT, Oh K, Oh HJ (2014) Prevalence of osteoporosis in the Korean population based on Korea National Health and Nutrition Examination Survey (KNHANES), 2008–2011. Yonsei Med J 55:1049–1057
Shin CS, Choi HJ, Kim MJ, Kim JT, Yu SH, Koo BK, Cho HY, Cho SW, Kim SW, Park YJ, Jang HC, Kim SY, Cho NH (2010) Prevalence and risk factors of osteoporosis in Korea: a community-based cohort study with lumbar spine and hip bone mineral density. Bone 47:378–387
Wright NC, Looker AC, Saag KG, Curtis JR, Delzell ES, Randall S, Dawson-Hughes B (2014) The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res 29:2520–2526
Olszynski WP, Davison KS, Adachi JD, Brown JP, Cummings SR, Hanley DA, Harris SP, Hodsman AB, Kendler D, McClung MR, Miller PD, Yuen CK (2004) Osteoporosis in men: epidemiology, diagnosis, prevention, and treatment. Clin Ther 26:15–28
Amin S, Felson DT (2001) Osteoporosis in men. Rheum Dis Clin North Am 27:19–47
Roy D, O’neill T, Finn J, Lunt M, Silman A et al (2003) Determinants of incident vertebral fracture in men and women: results from the European Prospective Osteoporosis Study (EPOS). Osteoporos Int 14:19–26
Ward KD, Klesges RC (2001) A meta-analysis of the effects of cigarette smoking on bone mineral density. Calcif Tissue Int 68:259–270
Lorentzon M, Mellstrom D, Haug E, Ohlsson C (2007) Smoking is associated with lower bone mineral density and reduced cortical thickness in young men. J Clin Endocrinol Metab 92:497–503
Kiel DP, Zhang Y, Hannan MT, Anderson JJ, Baron JA, Felson DT (1996) The effect of smoking at different life stages on bone mineral density in elderly men and women. Osteoporos Int 6:240–248
Egger P, Duggleby S, Hobbs R, Fall C, Cooper C (1996) Cigarette smoking and bone mineral density in the elderly. J Epidemiol Community Health 50:47–50
Jaramillo JD, Wilson C, Stinson DJ, Lynch DA, Bowler RP et al (2015) Reduced bone density and vertebral fractures in smokers. Men and COPD patients at increased risk. Ann Am Thorac Soc 12:648–656
Jones G, Nguyen T, Sambrook P, Kelly PJ, Eisman JA (1994) Progressive loss of bone in the femoral neck in elderly people: longitudinal findings from the Dubbo osteoporosis epidemiology study. BMJ 309:691–695
Cawthon PM, Ewing SK, McCulloch CE, Ensrud KE, Cauley JA, Cummings SR, Orwoll ES (2009) Loss of hip BMD in older men: the osteoporotic fractures in men (MrOS) study. J Bone Miner Res 24:1728–1735
Johansson C, Black D, Johnell O, Oden A, Mellström D (1998) Bone mineral density is a predictor of survival. Calcif Tissue Int 63:190–196
Johansson H, Oden A, Johnell O, Jonsson B, De Laet C, Oglesby A, McCloskey EV, Kayan K, Jalava T, Kanis JA (2004) Optimization of BMD measurements to identify high risk groups for treatment—a test analysis. J Bone Miner Res 19:906–913
Burchfiel CM, Marcus EB, Curb JD, MacLean CJ, Vollmer WM, Johnson LR, Fong K-O, Rodriguez BL, Masaki KH, Buist AS (1995) Effects of smoking and smoking cessation on longitudinal decline in pulmonary function. Am J Respir Crit Care Med 151:1778–1785
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 12:366–372
Vrieze A, De Greef M, Wijkstra PJ, Wempe JB (2007) Low bone mineral density in COPD patients related to worse lung function, low weight and decreased fat-free mass. Osteoporos Int 18:1197–1202
Watanabe R, Tanaka T, Aita K, Hagiya M, Homma T, Yokosuka K, Yamakawa H, Yarita T, Tai N, Hirano J, Inoue D, Okazaki R (2014) Osteoporosis is highly prevalent in Japanese males with chronic obstructive pulmonary disease and is associated with deteriorated pulmonary function. J Bone Miner Metab:1–9
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 94:1079–1084
Moayyeri A, Bingham SA, Luben RN, Wareham NJ, Khaw KT (2009) Respiratory function as a marker of bone health and fracture risk in an older population. J Bone Miner Res 24:956–963
Korea Centers for Disease Control and Prevention Ministry of Health and Welfare, South Korea Korea National Health and Nutrition Examination Survey (KNHANES) (2011). https://knhanescdcgokr/knhanes/indexdo. Accessed 18 November 2015
Jöström M, Ainsworth B, Bauman A, Bull F, Craig C, Sallls J (2005) Guidelines for Data Processing and Analysis of the International Physical Activity Questionnaire (IPAQ)—short and long forms. IPAQ core group 2005
Vogel JM, Davis JW, Nomura A, Wasnich RD, Ross PD (1997) The effects of smoking on bone mass and the rates of bone loss among elderly Japanese–American men. J Bone Miner Res 12:1495–1501
Leslie WD, Lix LM, Tsang JF, Caetano PA (2007) Single-site vs multisite bone density measurement for fracture prediction. Arch Intern Med 167:1641–1647
Nguyen TV, Kelly PJ, Sambrook PN, Gilbert C, Pocock NA, Eisman JA (1994) Lifestyle factors and bone density in the elderly: implications for osteoporosis prevention. J Bone Miner Res 9:1339–1346
Hopper JL, Seeman E (1994) The bone density of female twins discordant for tobacco use. N Engl J Med 330:387–392
Rudäng R, Darelid A, Nilsson M, Nilsson S, Mellström D, Ohlsson C, Lorentzon M (2012) Smoking is associated with impaired bone mass development in young adult men: a 5-year longitudinal study. J Bone Miner Res 27:2189–2197
Martin RB (2002) Size, structure and gender: lessons about fracture risk. J Musculoskelet Neuronal Interact 2:209–211
Kapoor D, Jones TH (2005) Smoking and hormones in health and endocrine disorders. Eur J Endocrinol 152:491–499
Mody N, Parhami F, Sarafian TA, Demer LL (2001) Oxidative stress modulates osteoblastic differentiation of vascular and bone cells. Free Radic Biol Med 31:509–519
Bernhard D, Moser C, Backovic A, Wick G (2007) Cigarette smoke–an aging accelerator? Exp Gerontol 42:160–165
Järup L, Alfvén T (2004) Low level cadmium exposure, renal and bone effects-the OSCAR study. Biometals 17:505–509
Ionescu AA, Schoon E (2003) Osteoporosis in chronic obstructive pulmonary disease. Eur Respir J Suppl 46:64s–75s
Myong JP, Kim HR, Choi SE, Koo JW (2013) Dose-related effect of urinary cotinine levels on bone mineral density among Korean females. Osteoporos Int 24:1339–1346
Walker LM, Preston MR, Magnay JL, Thomas PB, El Haj AJ (2001) Nicotinic regulation of c-fos and osteopontin expression in human-derived osteoblast-like cells and human trabecular bone organ culture. Bone 28:603–608
Lekamwasam S, Trivedi D, Khaw KT (2002) An association between respiratory function and bone mineral density in women from the general community: a cross sectional study. Osteoporos Int 13:710–715
Lekamwasam S, Trivedi D, Khaw KT (2005) An association between respiratory function and hip bone mineral density in older men: a cross-sectional study. Osteoporos Int 16:204–207
Silva DR, Coelho AC, Dumke A, Valentini JD, de Nunes JN, Stefani CL, da Silva Mendes LF, Knorst MM (2011) Osteoporosis prevalence and associated factors in patients with COPD: a cross-sectional study. Respir Care 56:961–968
Jeon YK, Shin MJ, Kim WJ, Kim SS, Kim BH, Kim SJ, Kim YK, Shin YB, Kim IJ (2014) 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 25:1571–1576
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 8:1–6
Lee K (2015) Is FEV1 an indicator of low bone mineral density in adults? The Fifth Korea National Health and Nutrition Examination Survey. J Bone Miner Metab 33:335–341
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KNHANES was conducted after the ethical approval by the Institutional Review Board of the Korea Center for Disease Control and Prevention (Approval Number 2008-04EXP-01-C, 2009-01CON-03-2C, 2010-02CON-21-C, 2011-02CON-06C).
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Lee, J.H., Hong, A.R., Kim, J.H. et al. Amount of smoking, pulmonary function, and bone mineral density in middle-aged Korean men: KNHANES 2008–2011. J Bone Miner Metab 36, 95–102 (2018). https://doi.org/10.1007/s00774-017-0811-1
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DOI: https://doi.org/10.1007/s00774-017-0811-1