Skip to main content
Top
Published in: Lung 1/2017

01-02-2017

Impact of Non-Invasive Ventilation on Sympathetic Nerve Activity in Chronic Obstructive Pulmonary Disease

Authors: Helge Haarmann, Jan Folle, Xuan Phuc Nguyen, Peter Herrmann, Karsten Heusser, Gerd Hasenfuß, Stefan Andreas, Tobias Raupach

Published in: Lung | Issue 1/2017

Login to get access

Abstract

Purpose

Chronic obstructive pulmonary disease (COPD) is associated with elevated sympathetic nerve activity, which is probably linked to an increased cardiovascular risk, and may contribute to muscle dysfunction by heightened muscle vasoconstrictor drive. We hypothesized that resistive unloading of respiratory muscles by intermittent non-invasive ventilation (NIV) reduces sympathetic tone at rest and during subsequent handgrip exercise in patients with COPD.

Methods

Muscle sympathetic nerve activity (MSNA) in the peroneal nerve, heart rate, blood pressure, CO2, and SpO2 were continuously recorded in 5 COPD patients with intermittent NIV and 11 control COPD patients without NIV. Static and dynamic handgrip exercises were performed before and after NIV.

Results

At baseline, heart rate-adjusted MSNA (bursts/100 heart beats) did not differ between groups. NIV did not significantly affect MSNA levels at rest. However, during handgrip exercises directly following NIV, MSNA was lower than before, which was significant for dynamic handgrip (67.00 ± 3.70 vs. 62.13 ± 4.50 bursts/100 heart beats; p = 0.035 in paired t test). In contrast, MSNA (non-significantly) increased in the control group during repeated dynamic or static handgrip. During dynamic handgrip, tCO2 was lower after NIV than before (change by −5.04 ± 0.68 mmHg vs. −0.53 ± 0.64 in the control group; p = 0.021), while systolic and diastolic blood pressure did not change significantly.

Conclusions

NIV reduces sympathetic activation during subsequent dynamic handgrip exercise and thereby may elicit positive effects on the cardiovascular system as well as on muscle function in patients with COPD.
Literature
1.
go back to reference Ottenheijm CA, Heunks LM, Dekhuijzen PN (2007) Diaphragm muscle fiber dysfunction in chronic obstructive pulmonary disease: toward a pathophysiological concept. Am J Respir Crit Care Med 175(12):1233–1240CrossRefPubMed Ottenheijm CA, Heunks LM, Dekhuijzen PN (2007) Diaphragm muscle fiber dysfunction in chronic obstructive pulmonary disease: toward a pathophysiological concept. Am J Respir Crit Care Med 175(12):1233–1240CrossRefPubMed
3.
go back to reference Laghi F, Tobin MJ (2003) Disorders of the respiratory muscles. Am J Respir Crit Care Med 168(1):10–48CrossRefPubMed Laghi F, Tobin MJ (2003) Disorders of the respiratory muscles. Am J Respir Crit Care Med 168(1):10–48CrossRefPubMed
4.
go back to reference Orozco-Levi M, Lloreta J, Minguella J, Serrano S, Broquetas JM, Gea J (2001) Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164(9):1734–1739CrossRefPubMed Orozco-Levi M, Lloreta J, Minguella J, Serrano S, Broquetas JM, Gea J (2001) Injury of the human diaphragm associated with exertion and chronic obstructive pulmonary disease. Am J Respir Crit Care Med 164(9):1734–1739CrossRefPubMed
5.
go back to reference Romer LM, Polkey MI (2008) Exercise-induced respiratory muscle fatigue: implications for performance. J Appl Physiol 104(3):879–888CrossRefPubMed Romer LM, Polkey MI (2008) Exercise-induced respiratory muscle fatigue: implications for performance. J Appl Physiol 104(3):879–888CrossRefPubMed
7.
go back to reference Piepoli M, Clark AL, Volterrani M, Adamopoulos S, Sleight P, Coats AJ (1996) Contribution of muscle afferents to the hemodynamic, autonomic, and ventilatory responses to exercise in patients with chronic heart failure: effects of physical training. Circulation 93(5):940–952CrossRefPubMed Piepoli M, Clark AL, Volterrani M, Adamopoulos S, Sleight P, Coats AJ (1996) Contribution of muscle afferents to the hemodynamic, autonomic, and ventilatory responses to exercise in patients with chronic heart failure: effects of physical training. Circulation 93(5):940–952CrossRefPubMed
8.
go back to reference Rodman JR, Henderson KS, Smith CA, Dempsey JA (2003) Cardiovascular effects of the respiratory muscle metaboreflexes in dogs: rest and exercise. J Appl Physiol 95(3):1159–1169CrossRefPubMed Rodman JR, Henderson KS, Smith CA, Dempsey JA (2003) Cardiovascular effects of the respiratory muscle metaboreflexes in dogs: rest and exercise. J Appl Physiol 95(3):1159–1169CrossRefPubMed
9.
go back to reference Seals DR, Victor RG (1991) Regulation of muscle sympathetic nerve activity during exercise in humans. Exerc Sport Sci Rev 19:313–349CrossRefPubMed Seals DR, Victor RG (1991) Regulation of muscle sympathetic nerve activity during exercise in humans. Exerc Sport Sci Rev 19:313–349CrossRefPubMed
10.
go back to reference Scott AC, Wensel R, Davos CH, Georgiadou P, Kemp M, Hooper J et al (2003) Skeletal muscle reflex in heart failure patients: role of hydrogen. Circulation 107(2):300–306CrossRefPubMed Scott AC, Wensel R, Davos CH, Georgiadou P, Kemp M, Hooper J et al (2003) Skeletal muscle reflex in heart failure patients: role of hydrogen. Circulation 107(2):300–306CrossRefPubMed
11.
go back to reference Andreas S, Haarmann H, Klarner S, Hasenfuss G, Raupach T (2014) Increased sympathetic nerve activity in COPD is associated with morbidity and mortality. Lung 192(2):235–241CrossRefPubMed Andreas S, Haarmann H, Klarner S, Hasenfuss G, Raupach T (2014) Increased sympathetic nerve activity in COPD is associated with morbidity and mortality. Lung 192(2):235–241CrossRefPubMed
12.
go back to reference Curtis BM, O’Keefe JH Jr. (2002) Autonomic tone as a cardiovascular risk factor: the dangers of chronic fight or flight. Mayo Clin Proc 77(1):45–54CrossRefPubMed Curtis BM, O’Keefe JH Jr. (2002) Autonomic tone as a cardiovascular risk factor: the dangers of chronic fight or flight. Mayo Clin Proc 77(1):45–54CrossRefPubMed
13.
go back to reference Andreas S, Anker SD, Scanlon PD, Somers VK (2005) Neurohumoral activation as a link to systemic manifestation of chronic lung disease. Chest 128:3618–3624CrossRefPubMed Andreas S, Anker SD, Scanlon PD, Somers VK (2005) Neurohumoral activation as a link to systemic manifestation of chronic lung disease. Chest 128:3618–3624CrossRefPubMed
14.
go back to reference Mohammed J, Meeus M, Derom E, Da Silva H, Calders P (2015) Evidence for autonomic function and its influencing factors in subjects with COPD: a systematic review. Respir Care. 60(12):1841–1851CrossRefPubMed Mohammed J, Meeus M, Derom E, Da Silva H, Calders P (2015) Evidence for autonomic function and its influencing factors in subjects with COPD: a systematic review. Respir Care. 60(12):1841–1851CrossRefPubMed
15.
go back to reference Rutten FH, Zuithoff NP, Hak E, Grobbee DE, Hoes AW (2010) Beta-blockers may reduce mortality and risk of exacerbations in patients with chronic obstructive pulmonary disease. Arch Intern Med 170(10):880–887CrossRefPubMed Rutten FH, Zuithoff NP, Hak E, Grobbee DE, Hoes AW (2010) Beta-blockers may reduce mortality and risk of exacerbations in patients with chronic obstructive pulmonary disease. Arch Intern Med 170(10):880–887CrossRefPubMed
16.
17.
go back to reference Shoemaker JK, Pandey P, Herr MD, Silber DH, Yang QX, Smith MB et al (1997) Augmented sympathetic tone alters muscle metabolism with exercise: lack of evidence for functional sympatholysis. J Appl Physiol (1985) 82(6):1932–1938 Shoemaker JK, Pandey P, Herr MD, Silber DH, Yang QX, Smith MB et al (1997) Augmented sympathetic tone alters muscle metabolism with exercise: lack of evidence for functional sympatholysis. J Appl Physiol (1985) 82(6):1932–1938
18.
go back to reference Borghi-Silva A, Oliveira CC, Carrascosa C, Maia J, Berton DC, Queiroga F Jr. et al (2008) Respiratory muscle unloading improves leg muscle oxygenation during exercise in patients with COPD. Thorax 63(10):910–915CrossRefPubMed Borghi-Silva A, Oliveira CC, Carrascosa C, Maia J, Berton DC, Queiroga F Jr. et al (2008) Respiratory muscle unloading improves leg muscle oxygenation during exercise in patients with COPD. Thorax 63(10):910–915CrossRefPubMed
19.
go back to reference Kolodziej MA, Jensen L, Rowe B, Sin D (2007) Systematic review of noninvasive positive pressure ventilation in severe stable COPD. Eur Respir J 30(2):293–306CrossRefPubMed Kolodziej MA, Jensen L, Rowe B, Sin D (2007) Systematic review of noninvasive positive pressure ventilation in severe stable COPD. Eur Respir J 30(2):293–306CrossRefPubMed
20.
go back to reference Kohnlein T, Windisch W, Kohler D, Drabik A, Geiseler J, Hartl S et al (2014) Non-invasive positive pressure ventilation for the treatment of severe stable chronic obstructive pulmonary disease: a prospective, multicentre, randomised, controlled clinical trial. Lancet Respir Med. 2(9):698–705CrossRefPubMed Kohnlein T, Windisch W, Kohler D, Drabik A, Geiseler J, Hartl S et al (2014) Non-invasive positive pressure ventilation for the treatment of severe stable chronic obstructive pulmonary disease: a prospective, multicentre, randomised, controlled clinical trial. Lancet Respir Med. 2(9):698–705CrossRefPubMed
21.
go back to reference Sin DD, Wong E, Mayers I, Lien DC, Feeny D, Cheung H et al (2007) Effects of nocturnal noninvasive mechanical ventilation on heart rate variability of patients with advanced COPD. Chest 131(1):156–163CrossRefPubMed Sin DD, Wong E, Mayers I, Lien DC, Feeny D, Cheung H et al (2007) Effects of nocturnal noninvasive mechanical ventilation on heart rate variability of patients with advanced COPD. Chest 131(1):156–163CrossRefPubMed
22.
go back to reference Skyba P, Joppa P, Orolin M, Tkacova R (2007) Blood pressure and heart rate variability response to noninvasive ventilation in patients with exacerbations of chronic obstructive pulmonary disease. Physiol Res 56(5):527–533PubMed Skyba P, Joppa P, Orolin M, Tkacova R (2007) Blood pressure and heart rate variability response to noninvasive ventilation in patients with exacerbations of chronic obstructive pulmonary disease. Physiol Res 56(5):527–533PubMed
23.
go back to reference Borghi-Silva A, Reis MS, Mendes RG, Pantoni CB, Simoes RP, Martins LE et al (2008) Noninvasive ventilation acutely modifies heart rate variability in chronic obstructive pulmonary disease patients. Respir Med 102(8):1117–1123CrossRefPubMed Borghi-Silva A, Reis MS, Mendes RG, Pantoni CB, Simoes RP, Martins LE et al (2008) Noninvasive ventilation acutely modifies heart rate variability in chronic obstructive pulmonary disease patients. Respir Med 102(8):1117–1123CrossRefPubMed
24.
go back to reference Windisch W, Walterspacher S, Siemon K, Geiseler J, Sitter H, German Society for P (2010) Guidelines for non-invasive and invasive mechanical ventilation for treatment of chronic respiratory failure. Published by the German Society for Pneumology (DGP). Pneumologie. 64(10):640–652CrossRefPubMed Windisch W, Walterspacher S, Siemon K, Geiseler J, Sitter H, German Society for P (2010) Guidelines for non-invasive and invasive mechanical ventilation for treatment of chronic respiratory failure. Published by the German Society for Pneumology (DGP). Pneumologie. 64(10):640–652CrossRefPubMed
25.
go back to reference Notarius CF, Atchison DJ, Floras JS (2001) Impact of heart failure and exercise capacity on sympathetic response to handgrip exercise. Am J Physiol Heart Circ Physiol 280(3):H969–H976PubMed Notarius CF, Atchison DJ, Floras JS (2001) Impact of heart failure and exercise capacity on sympathetic response to handgrip exercise. Am J Physiol Heart Circ Physiol 280(3):H969–H976PubMed
26.
go back to reference Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A et al (2005) Standardisation of spirometry. Eur Respir J 26(2):319–338CrossRefPubMed Miller MR, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A et al (2005) Standardisation of spirometry. Eur Respir J 26(2):319–338CrossRefPubMed
27.
go back to reference (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Eur Heart J 17(3):354–81 (1996) Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Eur Heart J 17(3):354–81
28.
go back to reference Raupach T, Bahr F, Herrmann P, Luethje L, Heusser K, Hasenfuss G et al (2008) Slow breathing reduces sympathoexcitation in COPD. Eur Respir J 32(2):387–392CrossRefPubMed Raupach T, Bahr F, Herrmann P, Luethje L, Heusser K, Hasenfuss G et al (2008) Slow breathing reduces sympathoexcitation in COPD. Eur Respir J 32(2):387–392CrossRefPubMed
30.
go back to reference Wallin BG, Esler M, Dorward P, Eisenhofer G, Ferrier C, Westerman R et al (1992) Simultaneous measurements of cardiac noradrenaline spillover and sympathetic outflow to skeletal muscle in humans. J Physiol Lond. 453:45–58CrossRefPubMedPubMedCentral Wallin BG, Esler M, Dorward P, Eisenhofer G, Ferrier C, Westerman R et al (1992) Simultaneous measurements of cardiac noradrenaline spillover and sympathetic outflow to skeletal muscle in humans. J Physiol Lond. 453:45–58CrossRefPubMedPubMedCentral
31.
go back to reference Haarmann H, Folle J, Nguyen XP, Herrmann P, Heusser K, Hasenfuß G, Andreas S, Raupach T (2016) Sympathetic activation is associated with exercise limitation in COPD. COPD. 13(5):589–594CrossRefPubMed Haarmann H, Folle J, Nguyen XP, Herrmann P, Heusser K, Hasenfuß G, Andreas S, Raupach T (2016) Sympathetic activation is associated with exercise limitation in COPD. COPD. 13(5):589–594CrossRefPubMed
32.
go back to reference Valipour A, Schneider F, Kossler W, Saliba S, Burghuber OC (2005) Heart rate variability and spontaneous baroreflex sequences in supine healthy volunteers subjected to nasal positive airway pressure. J Appl Physiol (1985) 99(6):2137–2143 Valipour A, Schneider F, Kossler W, Saliba S, Burghuber OC (2005) Heart rate variability and spontaneous baroreflex sequences in supine healthy volunteers subjected to nasal positive airway pressure. J Appl Physiol (1985) 99(6):2137–2143
33.
go back to reference Lukacsovits J, Carlucci A, Hill N, Ceriana P, Pisani L, Schreiber A et al (2012) Physiological changes during low- and high-intensity noninvasive ventilation. Eur Respir J 39(4):869–875CrossRefPubMed Lukacsovits J, Carlucci A, Hill N, Ceriana P, Pisani L, Schreiber A et al (2012) Physiological changes during low- and high-intensity noninvasive ventilation. Eur Respir J 39(4):869–875CrossRefPubMed
34.
go back to reference Heindl S, Dodt C, Krahwinkel M, Hasenfuss G, Andreas S (2001) Short term effect of continuous positive airway pressure on muscle sympathetic nerve activity in patients with chronic heart failure. Heart 85(2):185–190CrossRefPubMedPubMedCentral Heindl S, Dodt C, Krahwinkel M, Hasenfuss G, Andreas S (2001) Short term effect of continuous positive airway pressure on muscle sympathetic nerve activity in patients with chronic heart failure. Heart 85(2):185–190CrossRefPubMedPubMedCentral
35.
go back to reference Clarenbach CF, Sievi NA, Brock M, Schneiter D, Weder W, Kohler M (2015) Lung volume reduction surgery and improvement of endothelial function and blood pressure in patients with chronic obstructive pulmonary disease. A randomized controlled trial. Am J Respir Crit Care Med 192(3):307–314CrossRefPubMed Clarenbach CF, Sievi NA, Brock M, Schneiter D, Weder W, Kohler M (2015) Lung volume reduction surgery and improvement of endothelial function and blood pressure in patients with chronic obstructive pulmonary disease. A randomized controlled trial. Am J Respir Crit Care Med 192(3):307–314CrossRefPubMed
36.
go back to reference Somers VK, Mark AL, Zavala DC, Abboud FM (1989) Contrasting effects of hypoxia and hypercapnia on ventilation and sympathetic activity in humans. J Appl Physiol (1985) 67(5):2101–2106 Somers VK, Mark AL, Zavala DC, Abboud FM (1989) Contrasting effects of hypoxia and hypercapnia on ventilation and sympathetic activity in humans. J Appl Physiol (1985) 67(5):2101–2106
37.
go back to reference Garrod R, Mikelsons C, Paul EA, Wedzicha JA (2000) Randomized controlled trial of domiciliary noninvasive positive pressure ventilation and physical training in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 162(4 Pt 1):1335–1341CrossRefPubMed Garrod R, Mikelsons C, Paul EA, Wedzicha JA (2000) Randomized controlled trial of domiciliary noninvasive positive pressure ventilation and physical training in severe chronic obstructive pulmonary disease. Am J Respir Crit Care Med 162(4 Pt 1):1335–1341CrossRefPubMed
38.
go back to reference Anker SD, Coats AJ (1999) Cardiac cachexia: a syndrome with impaired survival and immune and neuroendocrine activation. Chest 115(3):836–847CrossRefPubMed Anker SD, Coats AJ (1999) Cardiac cachexia: a syndrome with impaired survival and immune and neuroendocrine activation. Chest 115(3):836–847CrossRefPubMed
Metadata
Title
Impact of Non-Invasive Ventilation on Sympathetic Nerve Activity in Chronic Obstructive Pulmonary Disease
Authors
Helge Haarmann
Jan Folle
Xuan Phuc Nguyen
Peter Herrmann
Karsten Heusser
Gerd Hasenfuß
Stefan Andreas
Tobias Raupach
Publication date
01-02-2017
Publisher
Springer US
Published in
Lung / Issue 1/2017
Print ISSN: 0341-2040
Electronic ISSN: 1432-1750
DOI
https://doi.org/10.1007/s00408-016-9965-1

Other articles of this Issue 1/2017

Lung 1/2017 Go to the issue