Skip to main content
Top
Published in: BMC Pulmonary Medicine 1/2019

Open Access 01-12-2019 | Computed Tomography | Research article

Oxygen desaturation during the 6-min walk test as a risk for osteoporosis in non-cystic fibrosis bronchiectasis

Authors: Hung-Yu Huang, Te-Fang Sheng, Chang-Wei Lin, Ting-Wen Wang, Chun-Yu Lo, Fu-Tsai Chung, Lan-Yan Yang, Yu-Bin Pan, Chun-Hua Wang

Published in: BMC Pulmonary Medicine | Issue 1/2019

Login to get access

Abstract

Background

Osteoporosis is a common comorbidity in non-cystic fibrosis (non-CF) bronchiectasis patients. We determined whether desaturation during 6-min walk test (6MWT) can be a predictor for osteoporosis risk.

Methods

This was a retrospective cross-sectional study. Sixty-six non-CF bronchiectasis patients were enrolled. Lung function, walking distance, the lowest oxygen saturation (SpO2), the fall in SpO2 (ΔSpO2), and the distance–saturation product (DSP) were determined during the 6MWT. Desaturators (n = 45) were defined as those with ΔSpO2 > 10% or the lowest SpO2 < 88%. Bone mineral density (BMD) was determined through dual-energy X-ray absorptiometry. The severity of non-CF bronchiectasis was evaluated using high-resolution computed tomography.

Results

Osteoporosis was evident in more desaturators (82%) than non-desaturators (43%, p < 0.01). BMD at the level of the femoral neck was significantly lower in desaturators than in non-desaturators (− 3.6 ± 1.1 vs. − 2.4 ± 0.9, p < 0.01). BMD was correlated positively with the lowest SpO2 and negatively with ΔSpO2 and severe exacerbations. In multivariate linear regression analysis, desaturation during 6MWT was the most significant predictive factor for osteoporosis (95% confidence interval − 1.60 to − 0.26, p = 0.01). Other risk factors included old age, low body mass index and severe exacerbation.

Conclusions

Exertional desaturation during the 6MWT was a significant predictive factor for osteoporosis in Asian non-CF bronchiectasis patients. The 6MWT may be useful in identifying the osteoporotic phenotype of non-CF bronchiectasis and increasing clinician awareness to promote early intervention.
Literature
1.
go back to reference Shoemark A, Ozerovitch L, Wilson R. Aetiology in adult patients with bronchiectasis. Respir Med. 2007;101(6):1163–70.CrossRef Shoemark A, Ozerovitch L, Wilson R. Aetiology in adult patients with bronchiectasis. Respir Med. 2007;101(6):1163–70.CrossRef
2.
go back to reference Loebinger MR, Wells AU, Hansell DM, Chinyanganya N, Devaraj A, Meister M, et al. Mortality in bronchiectasis: a long-term study assessing the factors influencing survival. Eur Respir J. 2009;34(4):843–9.CrossRef Loebinger MR, Wells AU, Hansell DM, Chinyanganya N, Devaraj A, Meister M, et al. Mortality in bronchiectasis: a long-term study assessing the factors influencing survival. Eur Respir J. 2009;34(4):843–9.CrossRef
3.
go back to reference McDonnell MJ, Aliberti S, Goeminne PC, Restrepo MI, Finch S, Pesci A, et al. Comorbidities and the risk of mortality in patients with bronchiectasis: an international multicentre cohort study. Lancet Respir Med. 2016;4(12):969–79.CrossRef McDonnell MJ, Aliberti S, Goeminne PC, Restrepo MI, Finch S, Pesci A, et al. Comorbidities and the risk of mortality in patients with bronchiectasis: an international multicentre cohort study. Lancet Respir Med. 2016;4(12):969–79.CrossRef
4.
go back to reference Gale NS, Bolton CE, Duckers JM, Enright S, Cockcroft JR, Shale DJ. Systemic comorbidities in bronchiectasis. Chron Respir Dis. 2012;9(4):231–8.CrossRef Gale NS, Bolton CE, Duckers JM, Enright S, Cockcroft JR, Shale DJ. Systemic comorbidities in bronchiectasis. Chron Respir Dis. 2012;9(4):231–8.CrossRef
5.
go back to reference Diehl N, Johnson MM. Prevalence of osteopenia and osteoporosis in patients with noncystic fibrosis bronchiectasis. South Med J. 2016;109(12):779–83.CrossRef Diehl N, Johnson MM. Prevalence of osteopenia and osteoporosis in patients with noncystic fibrosis bronchiectasis. South Med J. 2016;109(12):779–83.CrossRef
6.
go back to reference NIH Consensus Development Panel on Osteoporosis Prevention D, Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA. 2001;285(6):785–95.CrossRef NIH Consensus Development Panel on Osteoporosis Prevention D, Therapy. Osteoporosis prevention, diagnosis, and therapy. JAMA. 2001;285(6):785–95.CrossRef
7.
go back to reference Lacativa PG, Farias ML. Osteoporosis and inflammation. Arq Bras Endocrinol Metabol. 2010;54(2):123–32.CrossRef Lacativa PG, Farias ML. Osteoporosis and inflammation. Arq Bras Endocrinol Metabol. 2010;54(2):123–32.CrossRef
8.
go back to reference Neri AS, Lori I, Taccetti G, Festini F, de Martino M, Masi L, et al. Alteration of bone mineral density in cystic fibrosis adults. Chest. 2006;130(6):1952–3.CrossRef Neri AS, Lori I, Taccetti G, Festini F, de Martino M, Masi L, et al. Alteration of bone mineral density in cystic fibrosis adults. Chest. 2006;130(6):1952–3.CrossRef
9.
go back to reference Tomiyama H, Okazaki R, Inoue D, Ochiai H, Shiina K, Takata Y, et al. Link between obstructive sleep apnea and increased bone resorption in men. Osteoporos Int. 2008;19(8):1185–92.CrossRef Tomiyama H, Okazaki R, Inoue D, Ochiai H, Shiina K, Takata Y, et al. Link between obstructive sleep apnea and increased bone resorption in men. Osteoporos Int. 2008;19(8):1185–92.CrossRef
10.
go back to reference Wang TY, Lo YL, Chou PC, Chung FT, Lin SM, Lin TY, et al. Associated bone mineral density and obstructive sleep apnea in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2015;10:231–7.CrossRef Wang TY, Lo YL, Chou PC, Chung FT, Lin SM, Lin TY, et al. Associated bone mineral density and obstructive sleep apnea in chronic obstructive pulmonary disease. Int J Chron Obstruct Pulmon Dis. 2015;10:231–7.CrossRef
11.
go back to reference Waatevik M, Johannessen A, Gomez Real F, Aanerud M, Hardie JA, Bakke PS, et al. Oxygen desaturation in 6-min walk test is a risk factor for adverse outcomes in COPD. Eur Respir J. 2016;48(1):82–91.CrossRef Waatevik M, Johannessen A, Gomez Real F, Aanerud M, Hardie JA, Bakke PS, et al. Oxygen desaturation in 6-min walk test is a risk factor for adverse outcomes in COPD. Eur Respir J. 2016;48(1):82–91.CrossRef
12.
go back to reference Huang HY, Chou PC, Joa WC, Chen LF, Sheng TF, Lin HC, et al. Pulmonary rehabilitation coupled with negative pressure ventilation decreases decline in lung function, hospitalizations, and medical cost in COPD: a 5-year study. Medicine (Baltimore). 2016;95(41):e5119.CrossRef Huang HY, Chou PC, Joa WC, Chen LF, Sheng TF, Lin HC, et al. Pulmonary rehabilitation coupled with negative pressure ventilation decreases decline in lung function, hospitalizations, and medical cost in COPD: a 5-year study. Medicine (Baltimore). 2016;95(41):e5119.CrossRef
13.
go back to reference Hsieh MH, Fang YF, Chung FT, Lee CS, Chang YC, Liu YZ, et al. Distance-saturation product of the 6-minute walk test predicts mortality of patients with non-cystic fibrosis bronchiectasis. J Thorac Dis. 2017;9(9):3168–76.CrossRef Hsieh MH, Fang YF, Chung FT, Lee CS, Chang YC, Liu YZ, et al. Distance-saturation product of the 6-minute walk test predicts mortality of patients with non-cystic fibrosis bronchiectasis. J Thorac Dis. 2017;9(9):3168–76.CrossRef
14.
go back to reference Minai OA, Santacruz JF, Alster JM, Budev MM, McCarthy K. Impact of pulmonary hemodynamics on 6-min walk test in idiopathic pulmonary fibrosis. Respir Med. 2012;106(11):1613–21.CrossRef Minai OA, Santacruz JF, Alster JM, Budev MM, McCarthy K. Impact of pulmonary hemodynamics on 6-min walk test in idiopathic pulmonary fibrosis. Respir Med. 2012;106(11):1613–21.CrossRef
15.
go back to reference Maes C, Carmeliet G, Schipani E. Hypoxia-driven pathways in bone development, regeneration and disease. Nat Rev Rheumatol. 2012;8(6):358–66.CrossRef Maes C, Carmeliet G, Schipani E. Hypoxia-driven pathways in bone development, regeneration and disease. Nat Rev Rheumatol. 2012;8(6):358–66.CrossRef
16.
go back to reference Arnett TR, Gibbons DC, Utting JC, Orriss IR, Hoebertz A, Rosendaal M, et al. Hypoxia is a major stimulator of osteoclast formation and bone resorption. J Cell Physiol. 2003;196(1):2–8.CrossRef Arnett TR, Gibbons DC, Utting JC, Orriss IR, Hoebertz A, Rosendaal M, et al. Hypoxia is a major stimulator of osteoclast formation and bone resorption. J Cell Physiol. 2003;196(1):2–8.CrossRef
17.
go back to reference Fan L, Li J, Yu Z, Dang X, Wang K. The hypoxia-inducible factor pathway, prolyl hydroxylase domain protein inhibitors, and their roles in bone repair and regeneration. Biomed Res Int. 2014;2014:239356.PubMedPubMedCentral Fan L, Li J, Yu Z, Dang X, Wang K. The hypoxia-inducible factor pathway, prolyl hydroxylase domain protein inhibitors, and their roles in bone repair and regeneration. Biomed Res Int. 2014;2014:239356.PubMedPubMedCentral
18.
go back to reference Frey JL, Stonko DP, Faugere M-C, Riddle RC. Hypoxia-inducible factor-1α restricts the anabolic actions of parathyroid hormone. Bone Res. 2014;2:14005.CrossRef Frey JL, Stonko DP, Faugere M-C, Riddle RC. Hypoxia-inducible factor-1α restricts the anabolic actions of parathyroid hormone. Bone Res. 2014;2:14005.CrossRef
19.
go back to reference Kim SR, Kim DI, Kim SH, Lee H, Lee KS, Cho SH, et al. NLRP3 inflammasome activation by mitochondrial ROS in bronchial epithelial cells is required for allergic inflammation. Cell Death Dis. 2014;5:e1498.CrossRef Kim SR, Kim DI, Kim SH, Lee H, Lee KS, Cho SH, et al. NLRP3 inflammasome activation by mitochondrial ROS in bronchial epithelial cells is required for allergic inflammation. Cell Death Dis. 2014;5:e1498.CrossRef
20.
go back to reference Aliberti S, Lonni S, Dore S, McDonnell MJ, Goeminne PC, Dimakou K, et al. Clinical phenotypes in adult patients with bronchiectasis. Eur Respir J. 2016;47(4):1113–22.CrossRef Aliberti S, Lonni S, Dore S, McDonnell MJ, Goeminne PC, Dimakou K, et al. Clinical phenotypes in adult patients with bronchiectasis. Eur Respir J. 2016;47(4):1113–22.CrossRef
21.
go back to reference Ruscitti P, Cipriani P, Carubbi F, Liakouli V, Zazzeroni F, Di Benedetto P, et al. The role of IL-1β in the bone loss during rheumatic diseases. Mediat Inflamm. 2015;2015:782382.CrossRef Ruscitti P, Cipriani P, Carubbi F, Liakouli V, Zazzeroni F, Di Benedetto P, et al. The role of IL-1β in the bone loss during rheumatic diseases. Mediat Inflamm. 2015;2015:782382.CrossRef
22.
go back to reference O'Donnell AE, Barker AF, Ilowite JS, Fick RB. Treatment of idiopathic bronchiectasis with aerosolized recombinant human DNase I. Chest. 1998;113(5):1329–34.CrossRef O'Donnell AE, Barker AF, Ilowite JS, Fick RB. Treatment of idiopathic bronchiectasis with aerosolized recombinant human DNase I. Chest. 1998;113(5):1329–34.CrossRef
23.
go back to reference World Health Organization. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. World Health Organ Tech Rep Ser. 1994;843:1–129. World Health Organization. Assessment of fracture risk and its application to screening for postmenopausal osteoporosis. World Health Organ Tech Rep Ser. 1994;843:1–129.
24.
go back to reference Hans D, Downs RW Jr, Duboeuf F, Greenspan S, Jankowski LG, Kiebzak GM, et al. Skeletal sites for osteoporosis diagnosis: the 2005 ISCD official positions. J Clin Densitom. 2006;9(1):15–21.CrossRef Hans D, Downs RW Jr, Duboeuf F, Greenspan S, Jankowski LG, Kiebzak GM, et al. Skeletal sites for osteoporosis diagnosis: the 2005 ISCD official positions. J Clin Densitom. 2006;9(1):15–21.CrossRef
25.
go back to reference Hsieh MH, Chou PC, Chou CL, Ho SC, Joa WC, Chen LF, et al. Matrix metalloproteinase-1 polymorphism (−1607G) and disease severity in non-cystic fibrosis bronchiectasis in Taiwan. PLoS One. 2013;8(6):e66265.CrossRef Hsieh MH, Chou PC, Chou CL, Ho SC, Joa WC, Chen LF, et al. Matrix metalloproteinase-1 polymorphism (−1607G) and disease severity in non-cystic fibrosis bronchiectasis in Taiwan. PLoS One. 2013;8(6):e66265.CrossRef
26.
go back to reference Brooks D, Solway S, Gibbons WJ. ATS statement on six-minute walk test. Am J Respir Crit Care Med. 2003;167(9):1287.CrossRef Brooks D, Solway S, Gibbons WJ. ATS statement on six-minute walk test. Am J Respir Crit Care Med. 2003;167(9):1287.CrossRef
27.
go back to reference Utting JC, Flanagan AM, Brandao-Burch A, Orriss IR, Arnett TR. Hypoxia stimulates osteoclast formation from human peripheral blood. Cell Biochem Funct. 2010;28(5):374–80.CrossRef Utting JC, Flanagan AM, Brandao-Burch A, Orriss IR, Arnett TR. Hypoxia stimulates osteoclast formation from human peripheral blood. Cell Biochem Funct. 2010;28(5):374–80.CrossRef
28.
go back to reference Halpern R, Becker L, Iqbal SU, Kazis LE, Macarios D, Badamgarav E. The association of adherence to osteoporosis therapies with fracture, all-cause medical costs, and all-cause hospitalizations: a retrospective claims analysis of female health plan enrollees with osteoporosis. J Manag Care Pharm. 2011;17(1):25–39.PubMed Halpern R, Becker L, Iqbal SU, Kazis LE, Macarios D, Badamgarav E. The association of adherence to osteoporosis therapies with fracture, all-cause medical costs, and all-cause hospitalizations: a retrospective claims analysis of female health plan enrollees with osteoporosis. J Manag Care Pharm. 2011;17(1):25–39.PubMed
29.
go back to reference Frick KK, Bushinsky DA. Chronic metabolic acidosis reversibly inhibits extracellular matrix gene expression in mouse osteoblasts. Am J Phys. 1998;275(5 Pt 2):F840–7. Frick KK, Bushinsky DA. Chronic metabolic acidosis reversibly inhibits extracellular matrix gene expression in mouse osteoblasts. Am J Phys. 1998;275(5 Pt 2):F840–7.
30.
go back to reference Arnett TR. Acidosis, hypoxia and bone. Arch Biochem Biophys. 2010;503(1):103–9.CrossRef Arnett TR. Acidosis, hypoxia and bone. Arch Biochem Biophys. 2010;503(1):103–9.CrossRef
31.
go back to reference Cole PJ. Inflammation: a two-edged sword--the model of bronchiectasis. Eur J Respir Dis Suppl. 1986;147:6–15.PubMed Cole PJ. Inflammation: a two-edged sword--the model of bronchiectasis. Eur J Respir Dis Suppl. 1986;147:6–15.PubMed
32.
go back to reference Martinez-Garcia MA, Soler-Cataluna JJ, Perpina-Tordera M, Roman-Sanchez P, Soriano J. Factors associated with lung function decline in adult patients with stable non-cystic fibrosis bronchiectasis. Chest. 2007;132(5):1565–72.CrossRef Martinez-Garcia MA, Soler-Cataluna JJ, Perpina-Tordera M, Roman-Sanchez P, Soriano J. Factors associated with lung function decline in adult patients with stable non-cystic fibrosis bronchiectasis. Chest. 2007;132(5):1565–72.CrossRef
33.
go back to reference Chalmers JD, Smith MP, McHugh BJ, Doherty C, Govan JR, Hill AT. Short- and long-term antibiotic treatment reduces airway and systemic inflammation in non-cystic fibrosis bronchiectasis. Am J Respir Crit Care Med. 2012;186(7):657–65.CrossRef Chalmers JD, Smith MP, McHugh BJ, Doherty C, Govan JR, Hill AT. Short- and long-term antibiotic treatment reduces airway and systemic inflammation in non-cystic fibrosis bronchiectasis. Am J Respir Crit Care Med. 2012;186(7):657–65.CrossRef
34.
go back to reference Saleh AD, Chalmers JD, De Soyza A, Fardon TC, Koustas SO, Scott J, et al. The heterogeneity of systemic inflammation in bronchiectasis. Respir Med. 2017;127:33–9.CrossRef Saleh AD, Chalmers JD, De Soyza A, Fardon TC, Koustas SO, Scott J, et al. The heterogeneity of systemic inflammation in bronchiectasis. Respir Med. 2017;127:33–9.CrossRef
35.
go back to reference Kwan TS, Padrines M, Théoleyre S, Heymann D, Fortun Y. IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev. 2004;15(1):49–60.CrossRef Kwan TS, Padrines M, Théoleyre S, Heymann D, Fortun Y. IL-6, RANKL, TNF-alpha/IL-1: interrelations in bone resorption pathophysiology. Cytokine Growth Factor Rev. 2004;15(1):49–60.CrossRef
36.
go back to reference Fontova R, Gutiérrez C, Vendrell J, Broch M, Vendrell I, Simón I, et al. Bone mineral mass is associated with interleukin 1 receptor autoantigen and TNF-alpha gene polymorphisms in post-menopausal Mediterranean women. J Endocrinol Investig. 2002;25(8):684–90.CrossRef Fontova R, Gutiérrez C, Vendrell J, Broch M, Vendrell I, Simón I, et al. Bone mineral mass is associated with interleukin 1 receptor autoantigen and TNF-alpha gene polymorphisms in post-menopausal Mediterranean women. J Endocrinol Investig. 2002;25(8):684–90.CrossRef
37.
go back to reference Vogelmeier CF, Criner GJ, Martinez FJ, Anzueto A, Barnes PJ, Bourbeau J, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive lung disease 2017 report. GOLD executive summary. Am J Respir Crit Care Med. 2017;195(5):557–82.CrossRef Vogelmeier CF, Criner GJ, Martinez FJ, Anzueto A, Barnes PJ, Bourbeau J, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive lung disease 2017 report. GOLD executive summary. Am J Respir Crit Care Med. 2017;195(5):557–82.CrossRef
38.
go back to reference Fitzpatrick SF, Tambuwala MM, Bruning U, Schaible B, Scholz CC, Byrne A, et al. An intact canonical NF-kappaB pathway is required for inflammatory gene expression in response to hypoxia. J Immunol. 2011;186(2):1091–6.CrossRef Fitzpatrick SF, Tambuwala MM, Bruning U, Schaible B, Scholz CC, Byrne A, et al. An intact canonical NF-kappaB pathway is required for inflammatory gene expression in response to hypoxia. J Immunol. 2011;186(2):1091–6.CrossRef
39.
go back to reference Abo-Leyah H, Chalmers JD. New therapies for the prevention and treatment of exacerbations of bronchiectasis. Curr Opin Pulm Med. 2017;23(3):218–24.CrossRef Abo-Leyah H, Chalmers JD. New therapies for the prevention and treatment of exacerbations of bronchiectasis. Curr Opin Pulm Med. 2017;23(3):218–24.CrossRef
40.
go back to reference van Staa TP, Leufkens HG, Abenhaim L, Zhang B, Cooper C. Oral corticosteroids and fracture risk: relationship to daily and cumulative doses. Rheumatology (Oxford). 2000;39(12):1383–9.CrossRef van Staa TP, Leufkens HG, Abenhaim L, Zhang B, Cooper C. Oral corticosteroids and fracture risk: relationship to daily and cumulative doses. Rheumatology (Oxford). 2000;39(12):1383–9.CrossRef
41.
go back to reference Lasserson T, Holt K, Greenstone M. Oral steroids for bronchiectasis (stable and acute exacerbations). Cochrane Database Syst Rev. 2001;4:CD002162. Lasserson T, Holt K, Greenstone M. Oral steroids for bronchiectasis (stable and acute exacerbations). Cochrane Database Syst Rev. 2001;4:CD002162.
42.
go back to reference Andrianopoulos V, Wouters EF, Pinto-Plata VM, Vanfleteren LE, Bakke PS, Franssen FM, et al. Prognostic value of variables derived from the six-minute walk test in patients with COPD: results from the ECLIPSE study. Respir Med. 2015;109(9):1138–46.CrossRef Andrianopoulos V, Wouters EF, Pinto-Plata VM, Vanfleteren LE, Bakke PS, Franssen FM, et al. Prognostic value of variables derived from the six-minute walk test in patients with COPD: results from the ECLIPSE study. Respir Med. 2015;109(9):1138–46.CrossRef
Metadata
Title
Oxygen desaturation during the 6-min walk test as a risk for osteoporosis in non-cystic fibrosis bronchiectasis
Authors
Hung-Yu Huang
Te-Fang Sheng
Chang-Wei Lin
Ting-Wen Wang
Chun-Yu Lo
Fu-Tsai Chung
Lan-Yan Yang
Yu-Bin Pan
Chun-Hua Wang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Pulmonary Medicine / Issue 1/2019
Electronic ISSN: 1471-2466
DOI
https://doi.org/10.1186/s12890-019-0794-x

Other articles of this Issue 1/2019

BMC Pulmonary Medicine 1/2019 Go to the issue