Abstract
Summary
Association between lung function and bone metabolism remains controversial. We found that impaired lung function was associated with vertebral fractures and bone loss in Japanese postmenopausal women. While vertebral deformities would impair lung function, respiratory dysfunction might in turn increase fracture risk, suggesting a complex bidirectional interaction.
Introduction
Association between bone metabolism and pulmonary function in the general population is controversial. The aim of this study was to investigate relationship between lung and bone parameters in elderly postmenopausal women.
Methods
One hundred and six postmenopausal women (75.6 ± 8.0 years old) who underwent spirometric tests were examined for prevalent vertebral fractures, bone mineral density (BMD), bone metabolic markers, and other metabolic indices such as urinary pentosidine.
Results
Multivariable logistic regression analyses revealed that forced vital capacity (FVC) (OR = 0.063, 95% CI: 0.011–0.352, p = 0.002) and urinary pentosidine (OR = 1.067, 95% CI: 1.020–1.117, p = 0.005) were associated with the presence of vertebral fractures after adjustment for height loss, age, and BMD at femoral neck. Moreover, vital capacity (VC) or FVC as well as body mass index and age was among independent determinants of BMD after adjustment for height loss and the number and grade of vertebral fractures in forced multiple linear regression analysis (VC: β = 0.212, p = 0.021, FVC: β = 0.217, p = 0.031). Urinary pentosidine was negatively correlated with pulmonary function parameters such as FVC and forced expiratory volume in 1 s (FEV1.0), although these correlations appeared dependent on age.
Conclusions
Diminished FVC was associated with prevalent vertebral fractures and decreased BMD in Japanese postmenopausal women without apparent pulmonary diseases. Mechanism of such association between pulmonary function and bone status remains to be determined.
Similar content being viewed by others
References
Decramer M, Janssens W, Miravitlles M (2012) Chronic obstructive pulmonary disease. Lancet 379(9823):1341–1351. https://doi.org/10.1016/s0140-6736(11)60968-9
Graat-Verboom L, Wouters EF, Smeenk FW, van den Borne BE, Lunde R, Spruit MA (2009) Current status of research on osteoporosis in COPD: a systematic review. Eur Respir J 34(1):209–218. https://doi.org/10.1183/09031936.50130408
Lehouck A, Boonen S, Decramer M, Janssens W (2011) COPD, bone metabolism, and osteoporosis. Chest 139(3):648–657. https://doi.org/10.1378/chest.10-1427
Romme EA, Smeenk FW, Rutten EP, Wouters EF (2013) Osteoporosis in chronic obstructive pulmonary disease. Expert Rev Respir Med 7(4):397–410. https://doi.org/10.1586/17476348.2013.814402
Inoue D, Watanabe R, Okazaki R (2016) COPD and osteoporosis: links, risks, and treatment challenges. Int J Chron Obstruct Pulmon Dis 11:637–648. https://doi.org/10.2147/copd.s79638
Watanabe R, Tanaka T, Aita K, Hagiya M, Homma T, Yokosuka K, Yamakawa H, Yarita T, Tai N, Hirano J, Inoue D, Okazaki R (2015) Osteoporosis is highly prevalent in Japanese males with chronic obstructive pulmonary disease and is associated with deteriorated pulmonary function. J Bone Miner Metab 33(4):392–400. https://doi.org/10.1007/s00774-014-0605-7
Lombardi I Jr, Oliveira LM, Mayer AF, Jardim JR, Natour J (2005) Evaluation of pulmonary function and quality of life in women with osteoporosis. Osteoporos Int 16(10):1247–1253. https://doi.org/10.1007/s00198-005-1834-3
Leech JA, Dulberg C, Kellie S, Pattee L, Gay J (1990) Relationship of lung function to severity of osteoporosis in women. Am Rev Respir Dis 141(1):68–71. https://doi.org/10.1164/ajrccm/141.1.68
Harrison RA, Siminoski K, Vethanayagam D, Majumdar SR (2007) Osteoporosis-related kyphosis and impairments in pulmonary function: a systematic review. J Bone Miner Res 22(3):447–457. https://doi.org/10.1359/jbmr.061202
Tanigawa N, Kariya S, Komemushi A, Nakatani M, Yagi R, Sawada S (2012) Added value of percutaneous vertebroplasty: effects on respiratory function. AJR Am J Roentgenol 198(1):W51–W54. https://doi.org/10.2214/ajr.11.6730
Lee JS, Kim KW, Ha KY (2011) The effect of vertebroplasty on pulmonary function in patients with osteoporotic compression fractures of the thoracic spine. J Spinal Disord Tech 24(2):E11–E15. https://doi.org/10.1097/BSD.0b013e3181dd812f
Dong R, Chen L, Gu Y, Han G, Yang H, Tang T, Xiaoqing C (2009) Improvement in respiratory function after vertebroplasty and kyphoplasty. Int Orthop 33(6):1689–1694. https://doi.org/10.1007/s00264-008-0680-2
Masala S, Magrini A, Taglieri A, Nano G, Chiaravalloti A, Calabria E, Di Trapano R, Pietroiusti A, Simonetti G (2014) Chronic obstructive pulmonary disease (COPD) patients with osteoporotic vertebral compression fractures (OVCFs): improvement of pulmonary function after percutaneous vertebroplasty (VTP). Eur Radiol 24(7):1577–1585. https://doi.org/10.1007/s00330-014-3165-2
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(9):710–715. https://doi.org/10.1007/s001980200097
Lekamwasam S, Trivedi DP, Khaw KT (2005) An association between respiratory function and hip bone mineral density in older men: a cross-sectional study. Osteoporos Int 16(2):204–207. https://doi.org/10.1007/s00198-004-1673-7
Morseth B, Melbye H, Waterloo S, Thomassen MR, Risberg MJ, Emaus N (2013) Cross-sectional associations between prevalent vertebral fracture and pulmonary function in the sixth Tromso study. BMC Geriatr 13(1):116. https://doi.org/10.1186/1471-2318-13-116
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(1–2):115. https://doi.org/10.1007/s11657-012-0115-y
Shiraki M, Kuroda T, Nakamura T, Fukunaga M, Hosoi T, Orimo H, Makino K (2006) The sample size required for intervention studies on fracture prevention can be decreased by using a bone resorption marker in the inclusion criteria: prospective study of a subset of the Nagano cohort, on behalf of the Adequate Treatment of Osteoporosis (A-TOP) Research Group. J Bone Miner Metab 24(3):219–225. https://doi.org/10.1007/s00774-005-0675-7
Shiraki M, Kuroda T, Tanaka S, Saito M, Fukunaga M, Nakamura T (2008) Nonenzymatic collagen cross-links induced by glycoxidation (pentosidine) predicts vertebral fractures. J Bone Miner Metab 26(1):93–100. https://doi.org/10.1007/s00774-007-0784-6
Shiraki M, Kuroda T, Shiraki Y, Tanaka S, Higuchi T, Saito M (2011) Urinary pentosidine and plasma homocysteine levels at baseline predict future fractures in osteoporosis patients under bisphosphonate treatment. J Bone Miner Metab 29(1):62–70. https://doi.org/10.1007/s00774-010-0191-2
Kuroda T, Tanaka S, Saito M, Shiraki Y, Shiraki M (2013) Plasma level of homocysteine associated with severe vertebral fracture in postmenopausal women. Calcif Tissue Int 93(3):269–275. https://doi.org/10.1007/s00223-013-9754-2
Genant HK, Wu CY, van Kuijk C, Nevitt MC (1993) Vertebral fracture assessment using a semiquantitative technique. J Bone Miner Res 8(9):1137–1148. https://doi.org/10.1002/jbmr.5650080915
Vester B, Rasmussen K (1991) High performance liquid chromatography method for rapid and accurate determination of homocysteine in plasma and serum. Eur J Clin Chem Clin Biochem 29(9):549–554
Tanaka S, Kuroda T, Saito M, Shiraki M (2011) Urinary pentosidine improves risk classification using fracture risk assessment tools for postmenopausal women. J Bone Miner Res 26(11):2778–2784. https://doi.org/10.1002/jbmr.467
Golshan M, Crapo RO, Amra B, Jensen RL, Golshan R (2007) Arm span as an independent predictor of pulmonary function parameters: validation and reference values. Respirology 12(3):361–366. https://doi.org/10.1111/j.1440-1843.2007.01070.x
Pothirat C, Chaiwong W, Phetsuk N (2015) Impact of direct substitution of arm span length for current standing height in elderly COPD. Int J Chron Obstruct Pulmon Dis 10:1173–1178. https://doi.org/10.2147/COPD.S84225
Quanjer PH, Capderou A, Mazicioglu MM, Aggarwal AN, Banik SD, Popovic S, Tayie FA, Golshan M, Ip MS, Zelter M (2014) All-age relationship between arm span and height in different ethnic groups. Eur Respir J 44(4):905–912. https://doi.org/10.1183/09031936.00054014
Capderou A, Berkani M, Becquemin MH, Zelter M (2011) Reconsidering the arm span-height relationship in patients referred for spirometry. Eur Respir J 37(1):157–163. https://doi.org/10.1183/09031936.00199209
Kjensli A, Ryg M, Falch JA, Armbrecht G, Diep LM, Eriksen EF, Ellingsen I (2010) Does body height reduction influence interpretation of lung function in COPD patients? Eur Respir J 36(3):540–548. https://doi.org/10.1183/09031936.00148609
Briot K, Legrand E, Pouchain D, Monnier S, Roux C (2010) Accuracy of patient-reported height loss and risk factors for height loss among postmenopausal women. CMAJ 182(6):558–562. https://doi.org/10.1503/cmaj.090710
Masunari N, Fujiwara S, Nakata Y, Nakashima E, Nakamura T (2007) Historical height loss, vertebral deformity, and health-related quality of life in Hiroshima cohort study. Osteoporos Int 18(11):1493–1499. https://doi.org/10.1007/s00198-007-0392-2
Siminoski K, Warshawski RS, Jen H, Lee K (2006) The accuracy of historical height loss for the detection of vertebral fractures in postmenopausal women. Osteoporos Int 17(2):290–296. https://doi.org/10.1007/s00198-005-2017-y
Vogt TM, Ross PD, Palermo L, Musliner T, Genant HK, Black D, Thompson DE (2000) Vertebral fracture prevalence among women screened for the Fracture Intervention Trial and a simple clinical tool to screen for undiagnosed vertebral fractures. Fracture Intervention Trial Research Group. Mayo Clin Proc 75(9):888–896. https://doi.org/10.4065/75.9.888
Tamaki J, Iki M, Kadowaki E, Sato Y, Kagamimori S, Kagawa Y, Yoneshima H (2009) Arm span increases predictive value of models for prevalent vertebral deformities: the Japanese Population-based Osteoporosis (JPOS) Study. Maturitas 64(4):241–245. https://doi.org/10.1016/j.maturitas.2009.09.005
Saito M, Marumo K (2010) Collagen cross-links as a determinant of bone quality: a possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 21(2):195–214. https://doi.org/10.1007/s00198-009-1066-z
Yang J, Hu X, Zhang Q, Cao H, Wang J, Liu B (2012) Homocysteine level and risk of fracture: a meta-analysis and systematic review. Bone 51(3):376–382. https://doi.org/10.1016/j.bone.2012.05.024
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(5):1571–1576. https://doi.org/10.1007/s00198-014-2627-3
Acknowledgments
We would like to thank Yoshie Fujita and Kanako Yamagishi (measurement of respiratory function) for their technical assistance.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
The protocol was approved by the Ethics Committee at the Research Institute and Practice for Involutional Diseases, and we obtained comprehensive written informed consent from all subjects.
Conflicts of interest
None.
Rights and permissions
About this article
Cite this article
Watanabe, R., Shiraki, M., Saito, M. et al. Restrictive pulmonary dysfunction is associated with vertebral fractures and bone loss in elderly postmenopausal women. Osteoporos Int 29, 625–633 (2018). https://doi.org/10.1007/s00198-017-4337-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00198-017-4337-0