Workstation 2: Strategies in pulmonary rehabilitation for the severe COPD
patient
Breathing exercises to relieve dyspnea in severe COPD
Dr. Daniel Langer
KU Leuven Faculty of Kinesiology and Rehabilitation Sciences
Respiratory Rehabilitation and Respiratory Division, University Hospital Leuven, Belgium.
O&N I
Herestraat 49
BUS 706
3000 LEUVEN
BELGIUM
[email protected]
KEY MESSAGES
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Lung hyperinflation is closely associated with expiratory flow limitation and has major
clinical consequences for breathlessness and exercise intolerance in patients with COPD.
Dynamic hyperinflation (e.g. during exercise or exacerbations) critically limits tidal volume
expansion and negatively impacts the demand/capacity balance of the already compromised
respiratory muscles.
A growing disparity between increased central neural drive and the reduced respiratory
muscular/mechanical response due to hyperinflation contributes importantly to the perception
of respiratory discomfort and breathlessness during exertion.
Several non-pharmacological treatment options are available that can help to either 1) directly
reduce dynamic hyperinflation; 2) indirectly improve dynamic hyperinflation by reducing
ventilatory needs for a given level of exertion or 3) assist the overburdened respiratory
muscles to better cope with the increased loads and improve symptoms during exertion.
Several simple breathing strategies (e.g. pursed lips breathing, active expiration, and body
positioning techniques) that are sometimes used spontaneously may be taught to patients to
improve symptoms at rest and during exercise.
Subjective benefits in terms of dyspnea improvement during exertion need to be evaluated in
individual patients and weighed against the costs, risks, and time investment of the different
interventions.
SUMMARY
Introduction
Lung hyperinflation is highly prevalent in patients with chronic obstructive pulmonary disease
(COPD) and occurs across the continuum of the disease [1]. It is most pronounced in patients with
severe airflow obstruction. Important negative consequences of (dynamic) hyperinflation during
activities include:
1) limits on VT expansion resulting in early ventilatory mechanical limitation; [1-5]
2) increased elastic and threshold loading on the inspiratory muscles resulting in an increased work
and oxygen cost of breathing (reduced efficiency); [5-10]
3) functional inspiratory muscle weakening due to mechanical disadvantage (i.e. operating at shorter
lengths) and increased velocity of shortening (needed to create higher inspiratory flows);[5;7;11-13]
4) negative impact of increased inspiratory muscle work on leg blood flow and muscle fatigue;[14-17]
5) carbon dioxide (CO2) retention; [18] and
6) adverse effects on cardiac function and central hemodynamics.[19-22]
The growing disparity between increased central neural drive and the reduced respiratory
muscular/mechanical response due to hyperinflation contributes importantly to the perception of
respiratory discomfort during exertion.[23] The physiological rationale and efficacy of selected
breathing exercises aimed at improving symptoms caused by these alterations in breathing pattern will
be discussed below. Breathing exercises are mostly aimed at reducing symptoms of dyspnea during
exertion by assisting the overburdened respiratory muscles to better cope with the increased loads.
Breathing exercises
Deep and slow breathing
Training patients to transiently breathe slowly and deeply during exercise has been hypothesized to
decrease hyperinflation, work of breathing, and improve symptoms and exercise capacity. [24] Some
patients with severe airflow obstruction and lung hyperinflation spontaneously use pursed lip
breathing (PLB) to reduce expiratory flow and slow down respiratory rate and experience
improvements in dyspnea both at rest and during exercise.[25] Patients who do not adopt PLB
spontaneously show variable responses.[26] During PLB patients perform a moderately active
expiration through half-opened lips, thereby inducing expiratory mouth pressures of about
5cmH2O.[27] It has been shown that slowing down expiratory flow reduces the tendency of airways
to collapse and resulting air trapping.[28;29]. This is probably the reason why the technique seems to
be most effective in patients with severe loss of lung elastic recoil pressure and tracheobronchial
collapse. [26] Adopting PLB at rest reduces breathing frequency and increases VT, while V’E is
usually maintained or slightly reduced. [28] Reducing dead space and improving alveolar V’E in this
way probably explains improvements in gas exchange that are typically observed. [28;30] These
effects have also been observed when a slower and deeper breathing pattern was adopted without
using PLB.[31] In a recent small study (n=11) teaching patients with COPD yoga breathing resulted
in a slower, deeper pattern of breathing and improvements in oxygen saturation with no increases in
symptoms.[32] Effects of long term breathing retraining interventions on changes in spontaneous
ventilator pattern are still lacking. Data from Bianchi and colleagues obtained by using optoelectronic
plethysmography contribute to our understanding as to why not all patients with COPD obtain
symptom relief from PLB (and therefore probably not spontaneously use it).[33] They observed that
reductions in breathing frequency and increases in VT during PLB were achieved by either increasing
or decreasing EELV. The group that hyperinflated during PLB (n=19) did not perceive symptomatic
benefits whereas patients who decreased their EELV (n=11) did (Figure 3). Reductions in EELV
were positively correlated with improvements in Borg Dyspnea scores (r=0.71, p<0.001) and with a
greater level of expiratory flow limitation (r=0.45, p<0.02).[33]
PLB during exercise has only been studied in few small studies, with mixed results in terms of
dyspnea reduction and improvements in exercise capacity. [25;34-36] Spahija et al. performed the
only study (n=8) that measured changes in EELV and respiratory muscle effort after PLB during
constant work bicycle exercise.[25] They found a strong correlation between changes in dyspnea
sensation during exercise and both changes in EELV (r2=0.82, p=0.002) and inspiratory muscle effort
(r2=0.84, p=0.001) occurring with PLB. Interestingly, while all patients reduced their breathing
frequency during PLB, only two out of eight subjects were able to reduce their EELV and to decrease
their inspiratory effort. These were also the only patients who perceived improvements in dyspnea
during exercise. Patients who increased their EELV during PLB experienced worsening of
symptoms.[25] Reductions in EELV with PLB again seemed to be related to levels of static
hyperinflation (more hyperinflated patients tended to improve more) but the sample size was too
small to demonstrate a statistically significant relation (r=0.54, p=0.17). Further research will be
needed to identify and select patients that might benefit from PLB during exercise.[26] It will further
be important to standardize the technique and to define the amount of training, instruction and
reinforcement needed to apply it successfully.[37;38]
Collins and colleagues used a computerized ventilation feedback intervention aimed at slowing
respiratory rate during exercise, in combination with an exercise training program.[39] They showed
surprising reductions in respiratory rate, ventilation and DH at isotime during a constant load cycling
task. These improvements were related to improvements in dyspnea during exercise. Feasibility and
persistence of the these positive effects in the absence of the feedback still need to be determined in
order to make this approach applicable for clinical practice.
Active expiration
In healthy subjects active expiration is not present during resting breathing and only occurs with
increased ventilation (e.g. physical activity).[40] In patients with COPD abdominal muscle activity is
often present during resting breathing and this occurs more often in patients with more severe airflow
obstruction.[41] Contraction of abdominal muscles increases abdominal pressure during active
expiration.[26] It has been hypothesized that, while this increase in abdominal pressure is unlikely to
facilitate lung emptying or contribute to lowering of end expiratory lung volume, it should result in
lengthening of the diaphragm, thereby optimizing its end-expiratory length tension characteristics.[42]
Diaphragm displacement and its contribution to tidal volume during resting breathing was shown not
to be different in COPD patients in comparison to healthy subjects.[43] Recently it was also
demonstrated that increased expiratory muscle activity in patients with COPD was accompanied by
preserved dynamic diaphragm function in comparison with healthy controls during exercise.[44] In
patients with very severe airflow obstruction and hyperinflation the contribution of the diaphragm
during exercise was reduced.[45]
It is not clear whether the spontaneously present activity of expiratory muscles should be further
stimulated in patients with COPD. Reybrouck et al. observed larger decreases in FRC and
improvements in pressure generating capacity of inspiratory muscles in patients performing active
expiration with electromyography feedback compared to patients who received instructions without
myofeedback.[46] Symptomatic benefits were unfortunately not assessed and no studies on the effects
of active expiration training during exercise have been performed so far. Casciari and colleagues
studied a range of breathing retraining strategies including PLB and active expiration techniques and
found additional improvements in exercise capacity in those patients that performed their rehab
program in combination with breathing retraining strategies.[34] The relative contribution of each of
the different components of the breathing retraining program to the observed benefits is however
unclear. Dodd et al. studied the effects of a belt strapped around the abdomen to improve length
tension characteristics of the diaphragm during exercise.[47] While this intervention resulted in
improved maximal transdiaphragmatic pressure generation it increased relative load on the diaphragm
and the diaphragmatic tension time index during exercise and decreased endurance time on the
bicycle in comparison with unstrapped exercise.
In summary, spontaneous activity of the abdominal muscles is, depending on the severity of
hyperinflation and expiratory flow limitation, often already present at rest in patients with COPD and
probably helps to preserve diaphragmatic function during rest and during exercise. Whether further
improvements in diaphragmatic function after stimulated active expiration can result in improvements
in dyspnea and exercise capacity needs to be studied.
Body Positioning Techniques
Forward leaning is (in analogy with active expiration) often spontaneously used by patients in an
attempt to decrease dyspnea, possibly by improving the length tension relationships of the diaphragm.
Relief of dyspnea is often experienced by patients in the forward leaning position.[48-51] The
presence of hyperinflation and paradoxical abdominal movements have been shown to be related to
relief of dyspnea in this position.[49] Forward leaning is associated with a significant reduction in in
electromyographic activity of scalene and sternocleidomastoid muscles, an increase in pressure
generating capacity of inspiratory muscles and diaphragm efficiency (Figure 4),[49;50] and
significant improvements in thoracoabdominal movements.[49-51] In addition, forward leaning with
arm support allows accessory muscles (pectoralis minor and major) to significantly contribute to rib
cage elevation.[26] Use of a rollator while ambulating allows forward leaning with arm support,
decreases dyspnea, and increases exercise capacity.[52;53[
Diaphragmatic breathing
Several studies have described an increase in rib cage contribution to chest wall motion and/or
asynchrony between rib cage and abdominal motion in patients with COPD that correlates with
airflow obstruction and hyperinflation of the rib cage.[54-56] During diaphragmatic breathing patients
are instructed to move the abdominal wall predominantly during inspiration and to reduce upper rib
cage motion.[26] This aims to:
1) improve chest wall motion and the distribution of ventilation;
2) decrease the contribution of rib cage muscles to and the energy cost of breathing; and
3) to improve dyspnea and exercise performance.[26]
It has been consistently shown that patients with COPD are able to voluntarily change their breathing
pattern to more abdominal movement and less thoracic excursion during diaphragmatic breathing.[5759] Diaphragmatic breathing however often results in more asynchronous breathing movements and
has not been shown to improve breathing pattern and ventilation distribution.[57-60] In most patients
mechanical efficiency of breathing decreased whereas work and oxygen cost of breathing increased
resulting in worsening of dyspnea.[57;60;61] In summary, there is no evidence from controlled
studies to support the use of diaphragmatic breathing in hyperinflated patients with COPD.
Inspiratory muscle training (IMT)
Strengthening inspiratory muscles by specific training programs has been applied frequently in
patients with COPD to alleviate dyspnea symptoms and improve exercise capacity.[62;63] The
rationale for IMT is to compensate for the negative consequences of acute-on-chronic hyperinflation
(e.g. exercise, exacerbations) on the demand/capacity imbalance of the already compromised
respiratory muscles in COPD.[13;62-64] IMT has been shown to improve inspiratory muscle function
(pressure generating capacity and endurance) and to reduce dyspnea and improve exercise capacity
when applied as a stand-alone intervention with controlled training loads.[62] The intervention seems
to be most effective in patients with compromised inspiratory muscle function (Figure).[62] Effects
on dyspnea symptoms and exercise capacity when combining it with an exercise training intervention
are however still not conclusive.[62;65;66] In this context it should however be noted that additional
effects of other interventions exerting acute physiological effects during exercise testing (e.g heliox,
or oxygen supplementation, and assisted ventilation techniques) were difficult to establish when
combining them with an exercise training program.[67;68] Larger studies will be needed to show
additional effects of interventions that are combined with exercise training since the latter is by itself
already a very effective intervention.68 Significant enhancement in the velocity of inspiratory muscle
shortening during resistive breathing tasks, and increases in the size of type II muscle fibres following
IMT have been previously observed in patients with COPD.[69;70] These improvements might be of
clinical relevance to patients with respiratory muscle weakness secondary, in part, to lung
hyperinflation since improved muscle performance characteristics may improve dynamic function
during exercise. Similar to non-invasive ventilator support, IMT is not likely to directly affect
hyperinflation at rest or the increase in EELV during exercise. Improvements in dyspnea during
exercise in response to IMT and NIV are probably mostly related to adjustments in the
demand/capacity imbalance in the setting of high inspiratory muscle work and functional weakening
induced by DH.[62;63;71;72] The direct effects of IMT on operating lung volumes during exercise
have so far only been investigated in a single study.[73] Petrovic and colleagues showed that IMT
could reduce the rate of DH but, unfortunately, did not provide data on inspiratory muscle work and
neuromechanical dissociation during exercise.[73] Detailed measurements of inspiratory muscle
function during exercise in response to inspiratory muscle training have however not been performed
so far. The additional effects of IMT on exercise performance seem to be related to the presence of
inspiratory muscle weakness.[62] Positive effects were only observed in studies with cautious control
of training intensity (i.e. training loads of more than 30% Pi,max)[74] and careful patient selection.
Patients with impaired inspiratory muscle strength, a ventilatory limitation to exercise with dyspnea as
the main factor limiting exercise seem to have more potential to benefit.
Conclusions
Strong evidence supports the use of exercise training to reduce symptoms, increase exercise capacity
and improve quality of life in patients with COPD. Properly conducted exercise training has been
shown to reduce ventilatory needs and dynamic hyperinflation during exercise at a given workrate.
Several interventions might be useful adjuncts to exercise in primarily ventilatory limited and
hyperinflated patients who experience severe breathlessness during activities. Breathing exercises
might be applied on a trial and error basis taking into account perceived subjective benefits in terms of
symptom reduction. Even though the evidence base for most breathing exercises (except for
inspiratory muscle training) is small application of these techniques might be worthwhile (except for
diaphragmatic breathing) since even modest benefits, when achieved with simple, non-invasive, and
inexpensive interventions such as PLB, active expiration and body positioning might be of value to
patients. With all these interventions careful patient selection, proper and repeated instruction, control
of techniques, and repeated assessments of perceived benefits in terms of symptom improvements is
necessary. The transfer effects of controlled breathing exercises from resting to exercise conditions
are not well established and further research should be performed in this area.
FIGURES
Figure 1. Changes in volumes of the chest wall (∆VCW) with pursed lip breathing (PLB) in
comparison with normal breathing at rest (QB). Closed symbols indicate end-expiratory volume; open
symbols indicate end-inspiratory volume. Bars are means ± SEM.
Adapted from: Bianchi R, et al. Chest Wall Kinematics and Breathlessness During Pursed-Lip
Breathing in Patients With COPD. Chest. 2004; 125:459–465.
Figure 2. Mean data for 4 subjects with COPD in supine, standing, erect sitting, and forward leaning
position. ∆Edi = inspiratory phasic change in diaphragmatic electromyograph; ∆Pdi = inspiratory
phasic change in transdiaphragmatic pressure. The ratio ∆Pdi%/∆Edi% is an index of the efficiency of
the diaphragm.
From: Druz WS and Sharp JT. Electrical and Mechanical Activity of the Diaphragm Accompanying
Body Position in Severe Chronic Obstructive Pulmonary Disease. Am Rev Resp Dis 1982; 125:275280.
REFERENCES
1. O'Donnell, D. E., J. A. Guenette, F. Maltais, and K. A. Webb. 2012. Decline of resting
inspiratory capacity in COPD: the impact on breathing pattern, dyspnea, and ventilatory capacity
during exercise. Chest 141:753-762.
2. Guenette, J. A., K. A. Webb, and D. E. O'Donnell. 2012. Does dynamic hyperinflation contribute
to dyspnoea during exercise in patients with COPD? Eur.Respir J 40:322-329.
3. Laveneziana, P., K. A. Webb, J. Ora, K. Wadell, and D. E. O'Donnell. 2011. Evolution of
dyspnea during exercise in chronic obstructive pulmonary disease: impact of critical volume
constraints. Am.J Respir Crit Care Med. 184:1367-1373.
4. O'Donnell, D. E., S. M. Revill, and K. A. Webb. 2001. Dynamic hyperinflation and exercise
intolerance in chronic obstructive pulmonary disease. Am.J Respir Crit Care Med. 164:770-777.
5. O'Donnell, D. E., A. L. Hamilton, and K. A. Webb. 2006. Sensory-mechanical relationships
during high-intensity, constant-work-rate exercise in COPD. J.Appl.Physiol 101:1025-1035.
6. Loring, S. H., M. Garcia-Jacques, and A. Malhotra. 2009. Pulmonary characteristics in COPD
and mechanisms of increased work of breathing. J.Appl.Physiol 107:309-314.
7. O'Donnell, D. E., J. C. Bertley, L. K. Chau, and K. A. Webb. 1997. Qualitative aspects of
exertional breathlessness in chronic airflow limitation: pathophysiologic mechanisms.
Am.J.Respir.Crit Care Med 155:109-115.
8. Pride, N. B. and P. T. Macklem 1986. Lung Mechanics in Disease. In A. P. Fishman, editor
Handbook of Physiology, Section 3: The Respiratory System, Mechanics of Breathing, Part 2
American Physiological Society, Bethesda, MD. 659-692.
9. Roussos, C. and E. J. M. Campbell 1986. Respiratory Muscle Energetics. In A. P. Fishman,
editor Handbook of Physiology, Section 3: The Respiratory System, Mechanics of Breathing,
Part 2 American Physiological Society, Bethesda, MD. 481-509.
10. Whipp, B. J. and R. L. Pardy 1986. Breathing during exercise. In A. P. Fishman, editor
Handbook of Physiology, Section 3: The Respiratory System, Mechanics of Breathing, Part 2
American Physiological Society, Bethesda, MD. 605-629.
11. De Troyer A. and T. A. Wilson. 2009. Effect of acute inflation on the mechanics of the
inspiratory muscles. J.Appl.Physiol 107:315-323.
12. Decramer, M. 1989. Effects of hyperinflation on the respiratory muscles. Eur.Respir J. 2:299302.
13. LeBlanc, P., D. M. Bowie, E. Summers, N. L. Jones, and K. J. Killian. 1986. Breathlessness and
exercise in patients with cardiorespiratory disease. Am.Rev Respir Dis. 133:21-25.
14. Amann, M., M. S. Regan, M. Kobitary, M. W. Eldridge, U. Boutellier, D. F. Pegelow, and J. A.
Dempsey. 2010. Impact of pulmonary system limitations on locomotor muscle fatigue in patients
with COPD. Am.J Physiol Regul.Integr.Comp Physiol 299:R314-R324.
15. Borghi-Silva, A., C. C. Oliveira, C. Carrascosa, J. Maia, D. C. Berton, F. Queiroga, Jr., E. M.
Ferreira, D. R. Almeida, L. E. Nery, and J. A. Neder. 2008. Respiratory muscle unloading
improves leg muscle oxygenation during exercise in patients with COPD. Thorax 63:910-915.
16. Chiappa, G. R., F. Queiroga, Jr., E. Meda, L. F. Ferreira, F. Diefenthaeler, M. Nunes, M. A. Vaz,
M. C. Machado, L. E. Nery, and J. A. Neder. 2009. Heliox improves oxygen delivery and
utilization during dynamic exercise in patients with chronic obstructive pulmonary disease. Am.J
Respir Crit Care Med 179:1004-1010.
17. Chiappa, G. R., P. J. Vieira, D. Umpierre, A. P. Correa, D. C. Berton, J. P. Ribeiro, and J. A.
Neder. 2013. Inspiratory resistance decreases limb blood flow in COPD patients with heart
failure. Eur.Respir J.
18. O'Donnell, D. E., C. D'Arsigny, M. Fitzpatrick, and K. A. Webb. 2002. Exercise hypercapnia in
advanced chronic obstructive pulmonary disease: the role of lung hyperinflation. Am.J.Respir
Crit Care Med 166:663-668.
19. Chiappa, G. R., A. Borghi-Silva, L. F. Ferreira, C. Carrascosa, C. C. Oliveira, J. Maia, A. C.
Gimenes, F. Queiroga, Jr., D. Berton, E. M. Ferreira, et al. 2008. Kinetics of muscle
deoxygenation are accelerated at the onset of heavy-intensity exercise in patients with COPD:
relationship to central cardiovascular dynamics. J Appl.Physiol 104:1341-1350.
20. Montes de, O. M., J. Rassulo, and B. R. Celli. 1996. Respiratory muscle and cardiopulmonary
function during exercise in very severe COPD. Am.J.Respir Crit Care Med 154:1284-1289.
21. Vassaux, C., L. Torre-Bouscoulet, S. Zeineldine, F. Cortopassi, H. Paz-Diaz, B. R. Celli, and V.
M. Pinto-Plata. 2008. Effects of hyperinflation on the oxygen pulse as a marker of cardiac
performance in COPD. Eur.Respir J 32:1275-1282.
22. Watz, H., B. Waschki, T. Meyer, G. Kretschmar, A. Kirsten, M. Claussen, and H. Magnussen.
2010. Decreasing cardiac chamber sizes and associated heart dysfunction in COPD: role of
hyperinflation. Chest 138:32-38.
23. McKenzie, D. K., J. E. Butler, and S. C. Gandevia. 2009. Respiratory muscle function and
activation in chronic obstructive pulmonary disease. J Appl.Physiol 107:621-629.
24. Macklem, P. T. 2010. Therapeutic implications of the pathophysiology of COPD. Eur.Respir J
35:676-680.
25. Spahija, J., M. Marchie, H. Ghezzo, and A. Grassino. 2010. Factors discriminating spontaneous
pursed-lips breathing use in patients with COPD. COPD. 7:254-261.
26. Gosselink, R. 2003. Controlled breathing and dyspnea in patients with chronic obstructive
pulmonary disease (COPD). J.Rehabil.Res.Dev. 40:25-33.
27. van der Schans, C. P., W. de Jong, E. Kort, P. J. Wijkstra, G. H. Koeter, D. S. Postma, and Th.
W. van der Mark. 1995. Mouth pressures during pursed lip breathing. Physiother Theory Pract
11:29-34.
28. Tiep, B. L., M. Burns, D. Kao, R. Madison, and J. Herrera. 1986. Pursed lips breathing training
using ear oximetry. Chest 90:218-221.
29. Schmidt, R. W., K. Wasserman, and G. A. Lillington. 1964. The effect of flow and oral pressure
on the mechanics of breathing in patients with asthma and emphysema. Am.Rev.Respir.Dis.
90:564-571.
30. Mueller, R. E., T. L. Petty, and G. F. Filley. 1970. Ventilation and arterial blood gas changes
induced by pursed lips breathing. J.Appl.Physiol 28:784-789.
31. Paul, G., F. Eldridge, J. Mitchell, and T. Fiene. 1966. Some effects of slowing respiration rate in
chronic emphysema and bronchitis. J.Appl.Physiol 21:877-882.
32. Pomidori, L., F. Campigotto, T. M. Amatya, L. Bernardi, and A. Cogo. 2009. Efficacy and
tolerability of yoga breathing in patients with chronic obstructive pulmonary disease: a pilot
study. J Cardiopulm.Rehabil.Prev. 29:133-137.
33. Bianchi, R., F. Gigliotti, I. Romagnoli, B. Lanini, C. Castellani, B. Binazzi, L. Stendardi, M.
Grazzini, and G. Scano. 2007. Patterns of chest wall kinematics during volitional pursed-lip
breathing in COPD at rest. Respir.Med. 101:1412-1418.
34. Casciari, R. J., R. D. Fairshter, A. Harrison, J. T. Morrison, C. Blackburn, and A. F. Wilson.
1981. Effects of breathing retraining in patients with chronic obstructive pulmonary disease.
Chest 79:393-398.
35. Garrod, R., K. Dallimore, J. Cook, V. Davies, and K. Quade. 2005. An evaluation of the acute
impact of pursed lips breathing on walking distance in nonspontaneous pursed lips breathing
chronic obstructive pulmonary disease patients. Chron.Respir Dis. 2:67-72.
36. Nield, M. A., G. W. Soo Hoo, J. M. Roper, and S. Santiago. 2007. Efficacy of pursed-lips
breathing: a breathing pattern retraining strategy for dyspnea reduction. J
Cardiopulm.Rehabil.Prev. 27:237-244.
37. Garrod, R. and T. Mathieson. 2013. Pursed lips breathing: are we closer to understanding who
might benefit? Chron.Respir Dis. 10:3-4.
38. Tiep, B. L. 2007. Pursed lips breathing-easing does it. J.Cardiopulm.Rehabil.Prev. 27:245-246.
39. Collins, E. G., W. E. Langbein, L. Fehr, S. O'Connell, C. Jelinek, E. Hagarty, L. Edwards, D.
Reda, M. J. Tobin, and F. Laghi. 2008. Can ventilation-feedback training augment exercise
tolerance in patients with chronic obstructive pulmonary disease? Am.J Respir Crit Care Med.
177:844-852.
40. DeTroyer, A. 1983. Cournand lecture: Mechanical action of the abdominal muscles.
Bull.Eur.Physiopathol.Respir. 19:575-581.
41. Ninane, V., F. Rypens, J. C. Yernault, and T. A. De. 1992. Abdominal muscle use during
breathing in patients with chronic airflow obstruction. Am.Rev.Respir.Dis. 146:16-21.
42. Dodd, D. S., T. Brancatisano, and L. A. Engel. 1984. Chest wall mechanics during exercise in
patients with severe chronic air-flow obstruction. Am.Rev.Respir.Dis. 129:33-38.
43. Gorman, R. B., D. K. McKenzie, N. B. Pride, J. F. Tolman, and S. C. Gandevia. 2002.
Diaphragm length during tidal breathing in patients with chronic obstructive pulmonary disease.
Am J Respir Crit Care Med 166:1461-1469.
44. Laveneziana, P., K. A. Webb, K. Wadell, J. A. Neder, and D. E. O'donnell. 2014. Does
expiratory muscle activity influence dynamic hyperinflation and exertional dyspnea in COPD?
Respir.Physiol Neurobiol. 199:24-33.
45. Montes de Oca, M., J. Rassulo, and B. R. Celli. 1996. Respiratory muscle and cardiopulmonary
function during exercise in very severe COPD. Am.J.Respir Crit Care Med 154:1284-1289.
46. Reybrouck, T., A. Wertelaers, P. Bertrand, and M. Demedts. 1987. Myofeedback Training of the
Respiratory Muscles in Patients With Chronic Obstructive Pulmonary Disease. Journal of
Cardiopulmonary Rehabilitation and Prevention 7.
47. Dodd, D. S., T. P. Brancatisano, and L. A. Engel. 1985. Effect of abdominal strapping on chest
wall mechanics during exercise in patients with severe chronic air-flow obstruction.
Am.Rev.Respir.Dis. 131:816-821.
48. Barach, A. L. 1974. Chronic obstructive lung disease: postural relief of dyspnea.
Arch.Phys.Med.Rehabil. 55:494-504.
49. Sharp, J. T., W. S. Drutz, T. Moisan, J. Foster, and W. Machnach. 1980. Postural relief of
dyspnea in severe chronic obstructive pulmonary disease. Am.Rev.Respir.Dis. 122:201-211.
50. O'Neill, S. and D. S. McCarthy. 1983. Postural relief of dyspnoea in severe chronic airflow
limitation: relationship to respiratory muscle strength. Thorax 38:595-600.
51. Delgado, H. R., S. R. Braun, J. B. Skatrud, W. G. Reddan, and D. F. Pegelow. 1982. Chest wall
and abdominal motion during exercise in patients with chronic obstructive pulmonary disease.
Am.Rev.Respir.Dis. 126:200-205.
52. Solway, S., D. Brooks, L. Lau, and R. Goldstein. 2002. The short-term effect of a rollator on
functional exercise capacity among individuals with severe COPD. Chest 122:56-65.
53. Probst, V. S., T. Troosters, I. Coosemans, M. A. Spruit, F. O. Pitta, M. Decramer, and R.
Gosselink. 2004. Mechanisms of improvement in exercise capacity using a rollator in patients
with COPD. Chest 126:1102-1107.
54. Martinez, F. J., J. I. Couser, and B. R. Celli. 1990. Factors influencing ventilatory muscle
recruitment in patients with chronic airflow obstruction. Am.Rev Respir Dis. 142:276-282.
55. Sharp, J. T., J. Danon, W. S. Druz, N. B. Goldberg, H. Fishman, and W. Machnach. 1974.
Respiratory muscle function in patients with chronic obstructive pulmonary disease: its
relationship to disability and to respiratory therapy. Am.Rev.Respir.Dis. 110:154-168.
56. Sharp, J. T., N. B. Goldberg, W. S. Druz, H. C. Fishman, and J. Danon. 1977. Thoracoabdominal
motion in chronic obstructive pulmonary disease. Am.Rev.Respir.Dis. 115:47-56.
57. Gosselink, R. A., R. C. Wagenaar, H. Rijswijk, A. J. Sargeant, and M. L. Decramer. 1995.
Diaphragmatic breathing reduces efficiency of breathing in patients with chronic obstructive
pulmonary disease. Am.J.Respir.Crit Care Med. 151:1136-1142.
58. Grimby, G., H. Oxhoj, and B. Bake. 1975. Effects of abdominal breathing on distribution of
ventilation in obstructive lung disease. Clin.Sci.Mol.Med. 48:193-199.
59. Sackner, M. A., H. F. Gonzalez, G. Jenouri, and M. Rodriguez. 1984. Effects of abdominal and
thoracic breathing on breathing pattern components in normal subjects and in patients with
chronic obstructive pulmonary disease. Am.Rev.Respir.Dis. 130:584-587.
60. Willeput, R., J. P. Vachaudez, D. Lenders, A. Nys, T. Knoops, and R. Sergysels. 1983.
Thoracoabdominal motion during chest physiotherapy in patients affected by chronic obstructive
lung disease. Respiration 44:204-214.
61. Vitacca, M., E. Clini, L. Bianchi, and N. Ambrosino. 1998. Acute effects of deep diaphragmatic
breathing in COPD patients with chronic respiratory insufficiency. Eur.Respir.J. 11:408-415.
62. Gosselink, R., J. De Vos, S. P. van den Heuvel, J. Segers, M. Decramer, and G. Kwakkel. 2011.
Impact of inspiratory muscle training in patients with COPD: what is the evidence? Eur Respir J
37:416-425.
63. Spruit, M. A., S. J. Singh, C. Garvey, R. ZuWallack, L. Nici, C. Rochester, K. Hill, A. E.
Holland, S. C. Lareau, W. D. Man, et al. 2013. An official American Thoracic Society/European
Respiratory Society statement: key concepts and advances in pulmonary rehabilitation. Am J
Respir Crit Care Med 188:e13-e64.
64. LeBlanc, P., E. Summers, M. D. Inman, N. L. Jones, E. J. Campbell, and K. J. Killian. 1988.
Inspiratory muscles during exercise: a problem of supply and demand. J Appl.Physiol 64:24822489.
65. Ambrosino, N. 2011. The case for inspiratory muscle training in COPD. Eur Respir J 37:233235.
66. Polkey, M. I., J. Moxham, and M. Green. 2011. The case against inspiratory muscle training in
COPD. Eur Respir J 37:236-237.
67. Ambrosino, N. and S. Strambi. 2004. New strategies to improve exercise tolerance in chronic
obstructive pulmonary disease. Eur.Respir J. 24:313-322.
68. Puhan, M. A., H. J. Schunemann, M. Frey, and L. M. Bachmann. 2004. Value of supplemental
interventions to enhance the effectiveness of physical exercise during respiratory rehabilitation in
COPD patients. A systematic review. Respir.Res. 5:25.
69. Ramirez-Sarmiento, A., M. Orozco-Levi, R. Guell, E. Barreiro, N. Hernandez, S. Mota, M.
Sangenis, J. M. Broquetas, P. Casan, and J. Gea. 2002. Inspiratory muscle training in patients
with chronic obstructive pulmonary disease: structural adaptation and physiologic outcomes.
Am.J.Respir Crit Care Med 166:1491-1497.
70. Villafranca, C., G. Borzone, A. Leiva, and C. Lisboa. 1998. Effect of inspiratory muscle training
with an intermediate load on inspiratory power output in COPD. Eur.Respir J. 11:28-33.
71. Maltais, F., H. Reissmann, and S. B. Gottfried. 1995. Pressure support reduces inspiratory effort
and dyspnea during exercise in chronic airflow obstruction. Am.J.Respir Crit Care Med
151:1027-1033.
72. O'Donnell, D. E., R. Sanii, G. Giesbrecht, and M. Younes. 1988. Effect of continuous positive
airway pressure on respiratory sensation in patients with chronic obstructive pulmonary disease
during submaximal exercise. Am.Rev.Respir Dis. 138:1185-1191.
73. Petrovic, M., M. Reiter, H. Zipko, W. Pohl, and T. Wanke. 2012. Effects of inspiratory muscle
training on dynamic hyperinflation in patients with COPD. Int.J Chron.Obstruct.Pulmon.Dis.
7:797-805.
74. Smith, K., D. Cook, G. H. Guyatt, J. Madhavan, and A. D. Oxman. 1992. Respiratory muscle
training in chronic airflow limitation: a meta-analysis. Am.Rev.Respir.Dis. 145:533-539.
SUGGESTED READING
1. O'Donnell DE, Guenette JA, Maltais F, Webb KA. Decline of resting inspiratory capacity in
COPD: the impact on breathing pattern, dyspnea, and ventilatory capacity during exercise. Chest
2012;141:753-762.
Results of this study illustrate how the progressive increase in resting hyperinflation as the
disease advances has major implications for dyspnea and exercise limitation in COPD.
2. Loring SH, Garcia-Jacques M, Malhotra A. Pulmonary characteristics in COPD and mechanisms
of increased work of breathing. J Appl Physiol 2009;107:309-314.
This paper summarizes the mechanisms of increased work of breathing in COPD, as caused by
increases in resistive and elastic loading, using pressure-volume plots popularized by E.J.M.
Campbell.
3. Parshall MB, Schwartzstein RM, Adams L, et al. An official American Thoracic Society
statement: update on the mechanisms, assessment, and management of dyspnea. Am J Respir
Crit Care Med 2012;185:435-452.
This statement provides an update on the mechanisms, assessment, and management of dyspnea
and illustrates how imbalances in demand-to-capacity ratios caused by hyperinflation relate to
the intensity and quality of dyspnea in COPD.
4. Spruit MA, Singh SJ, Garvey C, et al. An official American Thoracic Society/European
Respiratory Society statement: key concepts and advances in pulmonary rehabilitation. Am J
Respir Crit Care Med 2013;188:e13-e64.
This statement summarizes the rehabilitative treatment options available for improving dynamic
hyperinflation, dyspnea, exercise capacity, and quality of life in patients with COPD.
5. van 't Hul A, et al. Acute effects of inspiratory pressure support during exercise in patients with
COPD. Eur Respir J. 2004 Jan;23(1):34-40.
This paper describes a method of IPS that can be used to improve exercise endurance in patients
with COPD. The authors have subsequently also applied this method during a pulmonary
rehabilitation program.
6. Spahija J, et al. Effects of imposed pursed-lips breathing on respiratory mechanics and dyspnea
at rest and during exercise in COPD. Chest. 2005;128(2):640-50.
The only study to date that evaluated respiratory effort, dynamic hyperinflation, and dyspnea
responses to pursed lips breathing during a constant work rate cycle exercise test.
7. Laveneziana, P., K. A. Webb, K. Wadell, J. A. Neder, and D. E. O'Donnell.. Does expiratory
muscle activity influence dynamic hyperinflation and exertional dyspnea in COPD?
Respir.Physiol Neurobiol. 2014; 199:24-33.
This paper describes the evaluation of expiratory muscle activity during exercise in patients with
COPD. It was concluded that dynamic diaphragmatic function was not different in health and in
COPD throughout exercise.
8. Druz WS and Sharp JT. Electrical and Mechanical Activity of the Diaphragm Accompanying
Body Position in Severe Chronic Obstructive Pulmonary Disease. Am Rev Resp Dis 1982;
125:275-280.
This classic study illustrates that diaphragm efficiency is better and related to reduced dyspnea
in the forward leaning position in comparison with erect sitting and standing in severely
hyperinflated patients with severe expiratory flow limitation.