The Ventilatory Response to Arm Elevation of Patients With Chronic Obstructive Pulmonary Disease

The Ventilatory Response to Arm Elevation of Patients With Chronic Obstructive Pulmonary Disease* Thomas E. Dolmage, M.Sc.; Luigi Maestro , B.Sc .; Monica A. Avendano, M.D., F.C.C .P.; and RogerS. Goldstein, M.B., Ch.B., F.C.C.P. Although arm activity is poorly tolerated by patients with COPD, the ventilatory response to arm elevation alone is not well understood. We therefore studied the ventilatory response to arm elevation using a customized arm support sling to eliminate the effect of an increase in metabolic activity that might be attributable to independent arm elevation and used leg exercise to increase metabolic activity. During arm elevation at rest, there was a significant decrease in vital capacity (180 ml) and a small decrease in functional residual capacity (120 ml) as measured by body plethysmography. Minute ventilation was unchanged. When supported arm elevation (SAE) was compared with the control arm position (CAP), minute ventilation was unchanged although the pattern of breathing became more rapid and shallow (mean±SD, SAE vs CAP: f.= 17.9±5.3 vs 16.2±4.8 breaths·min-•; VT=533± 126 vs 579± 142 ml;

p<0.05). During steady-state leg exercise, the increase in Vo., Vco, and VE did not differ between SAE and CAP; however, both f. and VT changed toward a more rapid, shallow pattern of breathing (SAE vs CAP: f.= 24.3 ± 3.0 VS 22.8±3.5 breaths·min-•; VT=990±293 vs 1,081±309 ml; p<0.05). During unsupported arm elevation Vo., Vco., and VE, and f. were significantly greater than during the CAP. Approaches that train arm muscles and strategies that either support arm muscles or allow for frequent rests during upper arm activity may improve the endurance and the quality of life for COPD patients.

Arm activity is poorly tolerated by many patients

The influence of arm activity on ventilation will be determined by the arm and shoulder muscles that have attachments to the thoracic cage. Active shortening of these muscles during arm elevation may distort the thorax, especially if these muscles are also used as accessory muscles of ventilation. In healthy volunteers, Couser et al6 demonstrated that arm elevation at rest altered the diaphragmatic contribution to the generation of ventilatory pressures and Maestro et al7 have shown that arm elevation alters the breathing pattern during graded exercise at high workloads. Yet, information about the ventilatory response ofCOPD patients to arm elevation is limited. Furthermore, changes in the ventilatory response that occur solely due to changes in arm position are likely to be accentuated as the metabolic demand increases. Therefore, this study was designed to determine the ventilatory response of COPD patients to changes in arm position at rest and during leg exercise . A better understanding of arm position on the ventilatory response of COPD patients will help develop strategies that can alleviate some of the daily respiratory discomfort that such patients experience.

n_ with severe chronic obstructive pulmonary dis-

ease (COPD). 1-4 Celli et al2 showed that the time for which COPD patients could sustain elevated and unsupported arm exercise was half the time for which they could sustain leg exercise even though the total amount of work was lower during arm exercise. Although it is possible that arm activities are limited by weak shoulder and arm muscles, Ries et al5 did not observe improvements in the ability ofCOPD patients to complete activities of daily living such as dishwashing, shelving, and shopping after they had completed upper limb strength and endurance training. It is likely that the ability of patients with COPD to sustain arm exercise is determined not only by the strength and endurance of the arm muscles, but also by the influence of the arm position itself on ventilatory mechanics. The observations of Tangri and Woo!P of an altered breathing pattern during arm activity and the report by Celli et al2 of dyssynchronous breathing during arm but not leg exercise in patients with chronic airflow obstruction support the idea of a ventilatory component that limits arm activity in COPD patients.

(Chest 1993; 104:1097-1100) CAP= control arm position; f.= frequency of breathing; SAE = supported arm elevation; Sa01 =oxygen saturation; U AE = unsupported arm elevation

METHODS *From West Park Hospital, Wellesley Hospital, and Mount Sinai Hospital, University ofToronto, Canada. This work is supported by the West Park Hospital Foundation, the Ontario Rehabilitation Technology Research and Development Consortium and the Respiratory Health Network of Centres of Excellence. Reprint requests: Dr. Goldstein, West FUrk Hospital, 82 Buttonwood Avenue , Toronto , Ontario, Canada M6M 2]5

Subjects Subjects with severe but stable COPD were recruited on an ongoing basis from the hospitals Respiratory Rehabilitation Program . Informed consent was obtained from those patients who volunteered for the study. Patients selected did not require supplemental oxygen at rest or during exercise. Each subject completed CHEST I 104 I 4 I OCTOBER, 1993

1097

standard measurements of pulmonary function.'~-'" Arterial blood gases were measured with the patient resting in the supine position and breathing room air.

Table 2-ln.fluence of Ann Position on Re/lting Pulmonary Function

Protocol Effects of Ann Position on Lung \blumes: Body plethysmography was used to determine the vital capacity (VC) and the functional residual capacity (FRC) of each subject with their arms either resting comfortably on their lap or in an elevated position. In the arms elevated position, the subject rested his clasped hands on top of his head so that his elbows were at shoulder level and at a slightly forward position from the coronal plane at approximately 70°. The order of arm position was randomized for each subject. Effect of Ann Position on lkntilation: The ventilatory response to arm elevation was studied at rest. Each subject sat in a firm straightbacked chair. During the control arm position (CAP), the subject's arms rested on the arms of the chair. During unsupported arm elevation (UAE), the subject raised his elbows to shoulder level, Hexed at the elbow to 90" with palms facing forward (ie, the surrender position). Supported arm elevation (SAE) was the same as UAE; however, the arms were supported by a customized sling. The customized sling served to fully counteract the effect of gravity on the elevated arms. Therefore, additional arm and shoulder muscle function was not used to maintain SAE. Minute ventilation (\'E), frequency of breathing (f..), tidal volume (VT), oxygen consumption fVoJ, carbon dioxide production fVcoJ, oxygen saturation (SaOJ, and heart rate were recorded with a metabolic cart (P.K. Morgan, England). Each arm position was held for 4 min. Four minutes was selected to ensure that a steady state had heen achieved. Data for each dependent variable were averaged over the fourth minute of each arm position. The subjects completed CAP and SAE in a randomized order after which UAE followed. This order was used after pilot studies showed that ventilatory re<.~>very following UAE sometimes required several minutes. Effect of Ann Position on lkntilation During Exercise: On a separate day, the ventilatory response to arm elevation was studied during leg exercise. The protocol and methods were the same as the protocol and methods used during rest (protocol 2) except that an electrically braked cycle ergometer (Rodby Electronic AB, Sweden) was modified so that the subject could perform leg exercise without the need li>r arm support. The order of arm position was the same as in protocol 2 (ie, UAE was always the last position). There was a rest of at least 5 min after each 4-min exercise period. In this way, the inRuence of different arm positions could be compared during exercise. The original seat and shaft were removed from the cycle ergometer and a chair identical to the one used previously to evaluate the resting position was placed behind the

Table !-Pulmonary Function of Subjects Studied During Each of the Three Protocols Protocol Age, yr Height, em Weight, kg FRC,L Predicted,% FEV,, L Predicted,% FVC, L FEV,IFVC,% Dco, ml·min - •·mm Hg - • Predicted , % PaCO,, mm Hg PaO,, mm Hg

1098

Arms elevated

Arms down

1 (n= 19), Mean SD

2 (n= 11), Mean SD

3 (n= 12), Mean SD

67 163 65 5.57 186 0.74 33 2.04 37 9.26 41 43 71

68 163 74 5.17 174 0.78

64 168 67 5.20 163 0.93 38 2.37 39 11.75 47 40 73

8 9 12 1.46 44 0.26 9 0.66 7 3.29 14 3 10

6 10 20 1.50 41 0.29 34 8 2.10 0.78 38 6 10.28 2.93 44 9 42 3 72 9

7 7 17 0.92 30 0.27 8 0.54 4 4.23 12 12

Vital capacity (L) Functional residual capacity (L) Residual volume (L) Total lung capacity (L) Inspiratory capacity (L)

Mean

SD

Mean

SD

2.62 5.61 4.75 7.38 1.70

0.66 1.46 1.48 1.67 0.45

2.44* 5.73 4.85 7.30 1.48*

0.63 1.40 1.41 1.58 0.36

*Significantly different from arms down position (p
The dependent variables VE, f,, VT, Vo,, and Vco, were analyzed using a two-tailed t test for pairwise comparisons with a Bonferroni correction. Means were reported as significantly different if the probability of the t score was less than 0.05 (p
Pulmonary function tests measured in each of the three protocols are summarized in Table 1. Results of the baseline pulmonary function tests among these groups were similar. The patients all had severe airflow obstruction as reflected by a mean FEV 1 of less than 1 Land a mean FEV/FVC ofless than 40 percent.

Effect of Ann Position on Pulrrwnary Function The results of arm elevation on static lung volumes are shown in Table 2. During arm elevation there was Table 3-ln.fluence of Ann Position on Re/lting Ventilation Control Mean SD Tidal volume, ml Frequency, breaths· min - 1 Ventilation, L·min - • Oxygen consumption, L·min -• Carbon dioxide production, L·min - •

579

142

Supported Mean SD 533*

126

Unsupported Mean SD 694*

197

16.2

4.8

17.9*

5.3

17.5*

5.0

9.0

2.5

9.2

2.4

11.9*

2.9

227

50

230

49

308*

60

195

46

193

42

263*

58

*Significantly different from control position (p
a small but significant decrease (180 ml) in VC. A small increase (120 ml) in FRC was not statistically significant. There was no relationship between the baseline FRC and either the change in VC or FRC with arm elevation. Effect of Ann Position on Ventilation at Rest

Table 3 shows the influence of arm position on resting ventilation. During SAE there was no change in Vo2 , Vco2 , or VE when compared with the control arm position. However, the fh was significantly greater during SAE and the VT was significantly less during SAE when compared with the control position. In contrast, during UAE the Vo2 , Vco2 , VE, fh and VT were significantly greater than in the control position. Effect of Ann Position on Ventilation During Exercise

Table 4 shows the influence of changing arm position during steady-state submaximal leg exercise. When metabolic demand was increased with leg exercise, there was no difference in the Vo 2 , Vco2 , and VE when SAE was compared with the control position. The fh was significantly greater and the VT was significantly less when SAE was compared with the control position. However, during leg exercise and UAE, the Vo2 , Vco 2 , VE, and fh were significantly greater than the control position. The subjects reported significantly greater shortness of breath (heavy) during UAE when compared with the shortness of breath (moderate) in the SAE and control positions (Table 4). DISCUSSION

Altered ventilatory responses have been observed during arm elevation in healthy volunteers and in subjects with CO PO. 1-4·6 •7 The extent to which these altered ventilatory responses are due to an increase in Table 4 -Influence of Ann Position on Ventilation During Exercise Control SO Mean lidal volume, ml Frequency, hreaths·

1,081

309

Supported SO Mean 990*

293

Unsupported SO Mean 999

318

22.8

3.5

24.3*

3.0

26.6*

4.7

24.4

7.1

24.0

7.6

26.1*

7.9

min - 1

Ventilation, L·min · • Oxygen consumption, L·min · • Carhon dioxide production, L·min ·• Shortness ofhreath

735

187

713

203

774*

219

681

202

681

226

736*

218

3. 1

2.0

2.9

1.4

*Significantly different from control position (p<0.05).

4.4*

2.0

the metabolic demand that results from arm elevation alone remains unclear. When the arms are elevated, some muscles such as the pectorals will expand the rib cage by passive stretching, whereas others, such as serratus anterior will do so by active contraction. When expanded, the rib cage will shorten the neck accessory muscles. It is conceivable that if shortened, these muscles may be less effective as force generators and thereby their contribution to inspiratory volume could be diminished. However, at least one report of a study of contractile characteristics and operating lengths of the neck inspiratory muscles in dogs has suggested that the neck muscles appear to maintain their force-generating potential regardless of the lung volume. 13 It is still possible, however, even when force generation is maintained, that the muscles, by being shorter, are less able to contribute to a volume change. The mechanical consequences of simple arm elevation are evident when static lung volumes are measured with a body plethysmograph. As the arms are raised, we observed a loss of vital capacity (Table 2). We also observed small changes in FRC. These changes were of the same magnitude (120-ml increase with arm elevation) as those observed by Martinez et al4 in subjects with COPD even though there were slight differences between the two study protocols. Martinez measured lung volumes with the arms elevated anteriorly to the level of the shoulders at a 90° angle as compared with our subjects who sat with their arms clasped together resting lightly on top of their heads. Martinez et al4 also investigated the influence of UAE on ventilation in 21 subjects with COPD. They observed increases in Vo2 , Vco2 , and VE within 30 s of arm elevation. The increase in VE was associated with an increase in the VT and the fb. These changes were accompanied by ventilatory muscle group partitioning suggesting an increase in diaphragmatic recruitment as well as an increase in the contribution of the muscles of expiration. We also found an increase in VE when the arms were elevated, which was associated with an increase in the VT and the fb. The consequences of arm elevation are broadly similar between the two studies. We observed an increase in ventilation of 2. 9 Umin and Martinez et al reported an increase of 2.3 Umin. Such differences may re8ect error variance between experiments or the slight differences in the position of the arms. We did observe greater changes in both Vo2 and Vco2 than those observed by Martinez et al. This may relate to differences in the protocol for data collection (2 min of arm elevation by Martinez et al vs 4 min in our protocol). During UAE, the in8uence of position alone on ventilation may be obscured by the alterations in ventilation caused by the increase in metabolic activity of the active arm muscles that maintain this position. CHEST I 104 I 4 I OCTOBER, 1993

1099

We therefi>re supported the arms to eliminate the additional work of active arm elevation. In this way we were able to measure the changes in pattern of breathing at levels of ventilation that were similar irrespective of whether the arms were elevated (Table 3). Criner and CeiiP studied 11 patients with COPD in whom unsupported arm exercise was compared with supported arm exercise. They concluded that the observed alteration in breathing pattern during unsupported arm exercise was associated with a shift away from the rib cage muscles to the diaphragm and the expiratory muscles. Again, although the arms were supported by the arm ergometer, the influence of arm position alone could not be isolated from the contribution of the active arm muscles to the increase in metabolism. By choosing to increase metabolic rate with leg exercise, we were able to isolate the influence of arm position using a customized arm support sling. Moreover, any possible influence that rhythmic limb movement might have had on ventilation was consistent for each arm position. Leg exercise alone resulted in au additional Vo 2 and Vco 2 of508 and 486 ml·min - 1, respectively (Table 4). This was associated with an increase in VE. A further increase in VE was observed during U AE. This was associated with a further increase in ~,. However, when the arms were supported during exercise and VE during exercise was similar to that of the control position (24.0 L·min - I and 24.4 L·min - I, respectively), a more rapid, shallow pattern of breathing was still observed. From previous studies 14 in which gastric and esophageal pressures have been measured in patients with COPD, it has been proposed that with increasing disease severity, there is a shift in ventilatory muscle recruitment from the diaphragm to the rib cage. It has also been suggested that the degree of dyspnea experienced by the COPD patients may relate in part to this shift in ventilatory muscle recruitment. Furthermore, in order to meet the increased ventilatory demands of exercise, patients with COPD increase their expiratory flow by increasing their end-expiratory lung volume even at the expense of working against a greater elastic load. Clearly if the arms are elevated, the contribution of the muscles of the thoracic cage to respiration will be opposed by the contribution of the same muscles to arm elevation and to the maintenance of posture. When exercise involves arm elevation, shortened and therefore less effective accessory muscles plus a passively stretched thoracic cage will not necessarily result in mechanics beneficial to meeting the increased ventilatory demands. The rapid, shallow pattern of breathing adopted likely contributes to the semation of dyspnea. Training programs that increase the strength and

1100

endurance of upper and lower limb muscles have reduced dyspnea and improved the quality of life of patients with COPD. 15 •16 Additional exercises that specifically train muscles required for both arm elevation and ventilation should be incorporated into these programs. Furthermore, these programs should be coupled with strategies that either support the arms during activity or allow frequent rests during which the arms are lowered. Incorporating specific training and strategies for arm elevation activities may result in a reduction in dyspnea and an increase in the quality oflife of patients with COPD greater than that achieved by general fitness programs alone. ACKNOWLEDGMENT: The authors wish to acknowledge the assistance of D. Mills in the preparation of this manuscript.

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Ventilatory Response to Arm Elevation in COPD Patients (Do/mage et al)