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ABSTRACT |
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ABSTRACT
INTRODUCTION
METHODS
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DISCUSSION
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Physiological responses to upper limb exercise have not been well documented in patients with cystic
fibrosis (CF). This is the first study to quantify ventilatory responses to supported incremental upper
limb exercise in this patient group. Twenty-four subjects with CF, with a wide range of pulmonary impairment, and ten normal control subjects were studied. Subjects performed pulmonary function
tests and incremental arm and leg exercise to peak work capacity on an arm crank and bicycle ergometer. All subjects performed less work with the arms than legs. At an equivalent oxygen consumption, ventilation was higher for arm work than leg work. This higher ventilation was achieved mainly
through a higher frequency of breathing. Only CF subjects with severe pulmonary impairment (FEV1 < 40% predicted, FEF25-75% < 20% predicted) had a reduced arm work capacity compared with control
subjects. At peak arm work, these subjects had a mean ventilation to maximum voluntary ventilation
ratio (
E/MVV) of 106% ± 25, while maximum heart rate was less than 80% predicted. Despite the
high ventilatory requirement for arm exercise, arm work capacity was well maintained in subjects
with CF until severe lung disease impaired the ability to further increase ventilation.
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INTRODUCTION |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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There is an increasing emphasis on maintenance of exercise capacity in patients with cystic fibrosis (CF). Reports have highlighted the beneficial effects from long-term regular exercise. Nixon and coworkers (1) demonstrated that exercise capacity was an independent determinant of prognosis in patients with CF, and in a recent abstract, Reisman and colleagues (2) reported that a 3-yr training program in subjects with CF resulted in a significantly lower rate of annual decline in forced vital capacity (FVC) and an improved sense of well-being. The lung transplantation literature also suggests that muscle deconditioning and atrophy that occurs before surgery may play an important role in the decreased exercise performance often seen after transplantation (3). This information supports the need to provide comprehensive training programs for people with CF. As the hand and upper limb are commonly used in everyday activities, upper limb exercise should be considered for inclusion in training programs. Precise documentation of upper limb exercise capacity in the CF group is therefore required.
To date, there is very little information on the physiological response to upper limb exercise in patients with CF. Knowledge of exercise response in patients with CF is derived almost entirely from studies of leg exercise (4). Only two previous studies have examined upper limb exercise in patients with CF. Keens and coworkers (8) demonstrated that upper limb training (canoeing) resulted in increased ventilatory muscle endurance while Strauss and coworkers (9) demonstrated increased upper body strength and a decrease in residual volume following six months of variable weight training. Neither of these studies have documented physiological responses to upper limb exercise in terms of exercise capacity, ventilatory response, or pattern of breathing.
The aim of the study was to quantify ventilatory responses to supported incremental arm exercise and to compare these to incremental leg exercise in adolescents and adults with CF. A group of patients with CF with a wide range of impairment in lung function was selected for study, and comparison was made with a group of healthy age-matched control subjects.
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METHODS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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Subjects
Twenty-four subjects with CF (18 males, six females) ranging in age from 17 to 44 yr (mean age ± SD, 26 ± 7.7), were recruited for the study. All subjects had a diagnosis of CF based on a positive sweat test result and clinical findings. In addition, 10 control subjects (five males, five females) ranging in age from 21 to 30 yr (mean ± SD = 24.6 ± 2.4) were recruited. Control subjects had no history of lung disease, and spirometry and lung volumes were within the normal range. None of the control subjects were involved in regular physical training. Informed consent was obtained from all subjects, and the study was approved by the Hospital Ethics Review Committee.
Respiratory Function Tests
Measurements of spirometry were performed with an autospirometer (AS6000 Autospirometer; Minato, Osaka, Japan) which was calibrated before each study. Lung volumes were determined by body plethysmography (Gould 2800; Gould Electronics, Dayton, OH). From three acceptable readings the total lung capacity (TLC) was calculated from the mean functional residual capacity (FRC) plus the mean inspiratory capacity (IC). Residual volume (RV) was calculated by subtracting the largest vital capacity (VC) from the TLC (10). Predicted normal values for spirometry were taken from Crapo and coworkers (11), and for lung volumes from Goldman and Becklake (12). Maximum voluntary ventilation (MVV) was calculated by multiplication of the FEV1 × 35 (13).
Maximum inspiratory mouth pressures at residual volume (RV) and maximum expiratory mouth pressures at total lung capacity (TLC) were measured using a hand-held pressure gauge reading zero to ± 250 cm H2O. The pressures achieved were used as an indicator of respiratory muscle strength. The value quoted was the best of three tests that were within ± 5 cm H2O of each other. Measurements were compared with predicted values reported by Wilson and coworkers (14). All respiratory measurements were taken after bronchodilators, if prescribed. Height and weight were measured and body mass index (BMI) (weight [kg]/height [m]2) was calculated for each subject.
Strength Measurements
Grip strength of the right and left hand was measured using a hand gripper. The best of three measurements was recorded. Normal values for grip strength were taken from Mathiowetz and coworkers (15).
Exercise Tests
All subjects performed an incremental arm and leg exercise test to peak work capacity using methodology previously described from our laboratory (16). An electrically braked bicycle ergometer (Seimens-Elema, Solina, Sweden) was modified for arm work. The bicycle ergometer was mounted on an adjustable table so that the crank shaft was in line with the gleno-humeral joint. The subjects sat in a straight-backed chair. The mouthpiece was adjusted so that the subjects sat fully upright during exercise. For leg exercise, subjects exercised on an electrically braked bicycle ergometer (Seimens-Elema, Solina, Sweden) using an incremental workload protocol as described by Jones (17). The height of the handlebars was adjusted so that the subjects sat fully upright during the test. The workload was increased each minute by a fixed amount (5 or 10 watts for arm exercise; 10 or 20 watts for leg exercise) that was chosen according to the severity of pulmonary disease.
Subjects breathed through a two-way valve (#2700; Hans Rudolph, Kansas City, MO). Inspired ventilation was measured using a dry gas meter (Vacumetrics, Ventura, CA). Mixed expired gases were continually sampled from a mixing chamber (4L chamber for FEV1 < 1.5 l; 8 l chamber for FEV1 > 1.5 l) and analyzed for oxygen (S3A; Applied Electrochemistry, Sunnyvale, CA) and carbon dioxide (Datex Normocap, Helsinki, Finland). End-tidal carbon dioxide was monitored at the subject's mouth (901-MK2; P.K. Morgan Ltd, Chatham, UK) throughout exercise. Heart rate and percent oxygen saturation (SaO2%) were obtained by a forehead probe attached to a pulse oximeter (N200; Nellcor, Hayward, CA). After 40 s of exercise at each workload subjects were asked to rate their breathlessness on a modified Borg dyspnea scale reading 0 ("nothing at all") to 10 ("maximal") (18).
Statistical Analysis
Regression lines were calculated using multiple data points from the subjects within each subgroup category. Testing for differences between slopes of regression lines was carried out according to the procedure outlined in Bland (19). Analysis of variance (ANOVA) with disease severity (mild, moderate, severe) and limb (arm, leg) were conducted on the relevant dependent variables. Disease severity was a between groups factor and limb was a repeated measures factor. Within the ANOVA framework, orthogonal planned comparisons were carried out to test for trends in the dependent variables across the CF subgroups as severity of lung disease increased, and also to test for any differences in trend between the limbs.
Further contrasts were carried out between the CF subgroups and the Control Group using an unpaired t test and the Bonferroni correction to control the Type 1 error rate. This procedure divides the Type 1 value by the number of contrasts performed on a measure. When the Bonferroni correction was applied a p < 0.025 was considered significant.
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RESULTS |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
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Relationship between Lung Function and Arm and Leg Work Capacity
For subjects with CF there was a significant correlation between FEV1% predicted and peak arm work and between FEV1% predicted and peak leg work (Figure 1). The slopes of the regression between FEV1% predicted and peak work for arm and leg were significantly different (z = 3.06, p < 0.01), indicating that for the same FEV1% predicted, significantly more work was achieved during leg exercise than during arm exercise.
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Comparison of Control Subjects and All CF Subjects at Peak Exercise
Comparison of parameters of exercise response between control subjects and all CF subjects at peak arm and leg exercise
are presented in Table 1. For the control subjects, peak work
capacity and peak oxygen consumption during leg exercise
were within the normal range (104% and 107% predicted, respectively) (20). At peak leg exercise the control group was
able to achieve a significantly higher workload, oxygen consumption (O2), carbon dioxide production (CO2), respiratory exchange ratio (RER), minute ventilation (E) and tidal
volume (VT) than the CF group (p < 0.05 for all comparisons).
In contrast, at peak arm exercise only CO2, RER and VT
were significantly higher in the control group (p < 0.05). All
other measurements were not significantly different between the control group and the CF group. As the CF group represents subjects with a wide range of lung function, comparisons
between this group as a whole and the control group is less
meaningful, therefore all future comparisons are made with
the CF group divided into subgroups according to lung function.
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Subgroups
Subjects with CF were categorized according to the level of pulmonary impairment. Six subjects had mild pulmonary impairment with FEV1 > 80% predicted, FEF25-75% 70-80% predicted (Mild Group); 10 subjects had moderate pulmonary impairment FEV1 40-80% predicted, FEF25-75% 20-69% predicted (Moderate Group); and eight subjects had severe pulmonary impairment with FEV1 < 40% predicted, FEF25-75% < 20% predicted (Severe Group). In addition, there were 10 subjects in the control group (Control Group). Mean anthropometric data and resting lung function for each subgroup are presented in Table 2. Subjects in the Severe Group showed marked air trapping with a mean RV/TLC ratio of 58% (range 47-75%).
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Peak Exercise
Comparisons of workload, O2, E, Borg dyspnea score, E/
MVV ratio and heart rate (HR) at peak exercise for all subgroups are presented in Figure 2A-F, respectively.
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= ± SEM. Numbers in brackets in (A) and (B), respectively, represent the ratio of
peak arm work to peak leg work, and peak arm Overall, for both arm and leg exercise combined there
were significant linear declines in peak workload, O2 and E
with increasing disease severity in the subgroups with CF
(F(1,21) = 21.04, F(1,21) = 24.23, F(1,21) = 18.76, respectively, all
p < 0.001) (Figure 2A-C). At peak leg exercise measures of
workload, O2 and E were significantly higher than those
values recorded for peak arm exercise (F(1,21) = 88.21, F(1,21) = 19.18, F(1,21) = 22.44, respectively, all p < 0.001). Post hoc testing showed that while there were significant differences in
O2 and E between peak arm and leg exercise for the Mild
and Moderate Groups (all p < 0.025), there was no longer any
significant difference between these variables in the Severe
CF Group. In the Severe Group, at both peak arm and leg
work capacity, HR% predicted was significantly lower than
the Control Group (p < 0.001) and E/MVV ratio was significantly higher (p < 0.001). In all the relationships examined at
peak work capacity no quadratic trends were found.
When work rate (watts) and ventilation (L · min
1) were
expressed per kilogram (kg) of body weight to normalize
these measurements for different body sizes, the peak ventilation in relation to peak work capacity was significantly higher
for arm exercise than leg exercise in all subgroup categories
(Table 3). The ratio of peak ventilation to peak work capacity (Peak E/PeakWC) was significantly higher in the Severe
Group when compared with the Control Group for both arm
and leg exercise (unpaired Student's t test: p < 0.01 and p < 0.025, respectively) (Table 3).
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At peak arm work capacity, only the Severe Group had a frequency of breathing that was significantly higher than the Control Group (p < 0.01). In all other groups, for both arm and leg exercise, frequency of breathing was not significantly different from the Control Group. The tidal volume in the Severe Group at peak arm and leg work capacity was significantly lower than the Control Group (p < 0.001 for both).
The fall in SaO2% at peak work capacity for arm and leg exercise with increasing disease severity did not reach significance (F(1,21) = 4.09, p = 0.056), and no significant difference was found in the fall in SaO2% at peak work capacity between arm and leg exercise. The mean fall in SaO2% in the Severe Group was 4.0% at peak arm exercise and 3.3% at peak leg exercise. Four subjects in the Severe Group had a fall in SaO2% of greater than, or equal to 5% at peak arm exercise, while only three subjects in this group had similar falls at peak leg exercise.
Relationship between O2 and Ventilation
Within each subgroup of lung disease severity in patients with
CF and also in the Control Group, O2 and E measured during progressive arm and leg exercise were strongly correlated
(all r values > 0.91, all p < 0.001). When the slopes of the relationship for arm and leg exercise were compared for the Control Group and the Severe CF Group, the ventilation required
for arm exercise at an equivalent O2 was significantly higher
than that required for leg exercise (all z > 3.2, p < 0.01).
The higher ventilation for arm exercise compared with leg
exercise in the Severe and Control Groups (Figure 3A) was
largely due to a higher frequency of breathing at an equivalent
O2 (Figure 3B) with tidal volume not being significantly different (Figure 3C).
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Relationship between Oxygen Consumption and Workload
There was a significant correlation between O2, and workload for arm exercise and for leg exercise in all subgroups (all r values > 0.92, all p < 0.001). When the slopes of the relationships were compared, the O2 required for arm exercise was
significantly higher than leg exercise at an equivalent workload for all subgroups (p < 0.01). Figure 4 shows the relationship for the Severe Group and the Control Group.
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Dyspnea
The relationship between O2 and dyspnea throughout exercise was available in 20 of the twenty-four subjects with CF
(seven in the Severe Group and six in each of the Moderate
and Mild Groups), and in the ten subjects in the Control
Group. Within each subgroup, there was a significant relationship between O2 and the Borg dyspnea score during both
progressive arm and progressive leg exercise (p < 0.001). In
Figure 5A it is apparent that for a given O2, the highest dyspnea score occurs for arm exercise in the Severe Group. However, there was no significant difference between the slopes
for arm or leg exercise between groups.
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The Borg dyspnea score at peak arm and leg work capacity is presented in Figure 5B. The dyspnea score at peak arm work was significantly less than at peak leg work in the Control Group (F(1,9) = 17.3, p < 0.001) and did not quite reach significance in the Mild Group (F(1,5) = 9.22, p < 0.02). Mean Borg dyspnea scores at peak arm work, in all the CF subgroups, were not significantly different from the Control Group. This was also the case at peak leg exercise.
PImax, PEmax and Grip Strength
PImax was within normal limits (14) except for two subjects in the Severe Group who had PImax less than 48% predicted. PEmax was within normal range for all subjects. Hand grip strength was normal in all but one subject in the Severe Group. There were significant, but not strong, correlations between grip strength and PImax (r = 0.42, p < 0.05); grip strength and PEmax (r = 0.37, p < 0.05); between BMI and PImax (r = 0.37, p < 0.05); and BMI and PEmax (r = 0.50, p < 0.0l). There was no significant relationship between BMI and grip strength.
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DISCUSSION |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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This study is the first to document responses to incremental arm exercise in patients with cystic fibrosis. The major findings of the study were that all subjects performed less work with arm exercise than leg exercise and that at an equivalent oxygen consumption during incremental exercise, ventilation was higher for arm work than leg work. This higher ventilation was achieved mainly through a higher frequency of breathing. In addition, at peak exercise, when work rate and ventilation were expressed per kilogram of body weight to normalize for different body sizes, the peak ventilation in relation to peak work capacity was significantly higher for arm than leg exercise. These findings indicate a relatively greater ventilatory requirement during arm exercise. Interestingly, despite this, only CF subjects with severe pulmonary impairment had reduced arm work capacity compared to control subjects.
There was a significant relationship between lung function and peak arm work in patients with CF which has not previously been described. Compared with leg exercise, the peak workloads achieved at an equivalent FEV1% predicted for peak arm exercise were significantly less. This most likely reflects the smaller muscle mass involved in arm exercise compared with leg exercise. Shephard and colleagues (21) have shown a significant correlation between muscle volume and peak work rate.
Although there are previous studies which have defined
the physiological response to arm ergometry in normal subjects (22), there are none which include sufficient numbers
in different age ranges to provide age-related predicted values
for maximal oxygen consumption or maximal power output.
Thus results from our CF subjects were compared with those
of our normal control subgroup. The control male subjects in
our group had a similar physiological response to progressive
arm exercise in terms of O2 peak and Wpeak as has previously been reported in males of a similar age (24). The females in our group had lower values than those reported by
Washburn and coworkers (25) of a group of females of a similar age. However, the group of females that these researchers
studied were active physical education students whereas our
subjects were sedentary and perhaps more representative of
the general population.
All subjects (control and CF) performed less work, as measured by peak workload, with arms than with legs. It has previously been reported in normal male subjects that peak arm
work is approximately 50% of peak leg work and that peak
arm O2 is approximately 66% of peak leg O2 (22, 23, 26).
Our data from control subjects supports this with peak arm
O2 being 64% of peak leg O2 (Figure 2).
When compared with control subjects, only those subjects with severe lung disease due to CF had a reduced capacity to perform arm exercise, while those with mild and moderate lung disease had an exercise response similar to control subjects. This well maintained arm exercise capacity in all but the Severe Group may be influenced by the lack of habitual rhythmic arm exercise performed by the Control Group resulting in relatively untrained arm muscles for this activity and therefore less difference between the groups studied. The response to progressive leg exercise in the subjects with CF was similar to that reported by Cropp and coworkers (5). There was a progressive decline in peak leg work with increasing disease severity but only subjects with severe lung impairment had a peak work capacity significantly lower than the Control Group.
Interestingly, in the Severe Group there was no significant
difference in peak O2 and peak ventilation between arm and
leg exercise. This suggests that a level of exercise was reached
beyond which the O2 could not be increased. The limitation
in O2 peak was probably due to an inability to increase ventilation to meet increasing exercise demands since at peak exercise in the Severe Group, ventilation was the same for arm and
leg exercise. This differed from the results observed in other
groups where ventilation at peak leg exercise exceeded that at
peak arm exercise. In addition, in the Severe Group the mean
E/MVV ratio was 109% at peak arm work and 110% at peak
leg work (similar to that previously reported for leg exercise
[4]), indicating that there was a limitation to ventilation in the
CF group with severe airways obstruction which provided a
major constraint to further exercise. This data, combined with
the peak HR in the Severe Group being less than 80% predicted suggests that there was a major ventilatory, rather than
a cardiac, constraint to continued exercise.
The demands on the respiratory system differ between arm
and leg exercise. When work rates and ventilation were normalized for body weight (Table 3), peak ventilation was significantly higher for arm than leg exercise in all subgroups. This
was also true at common submaximal O2 where ventilation
was higher for arm than leg exercise (Figure 3). Thus, arm exercise provides a relatively greater stimulus to ventilation than
leg exercise. It has previously been documented in normal
subjects that lactic acid production is higher at an equivalent
workload for arm exercise than leg exercise (27) and may explain the higher ventilation seen during incremental arm exercise. Ventilation during arm cranking may also have been
stimulated by a higher sympathetic drive which Bevegard and
coworkers (28) cited as a possible reason for the observed
higher ventilation, HR, and blood pressure observed for a
given O2 during arm exercise compared to leg exercise in
normal subjects.
The Severe Group required a significantly higher ventilation throughout arm and leg exercise than the Control Group. Godfrey and Meams (4) demonstrated that CF subjects with severe lung disease have increased dead space ventilation which would require higher levels of ventilation to maintain adequate gas exchange. The higher frequency of breathing seen during arm exercise would result in even greater dead space ventilation.
The higher oxygen consumption at an equivalent workload for arm exercise compared to leg exercise is consistent with a lower mechanical efficiency for arm than leg exercise reported by Bevegard and coworkers (28) and Bergh and colleagues (29). The smaller muscle mass of the arms (28) and additional work required to stabilize the torso during arm exercise may contribute to this. Alternatively, the difference in efficiency between arm and leg exercise may have been due to lack of upper body restraint during arm exercise, as some researchers (22) have found that if the upper body is restrained, efficiency between arm and leg exercise is not significantly different.
Studies reporting the pattern of breathing in normal subjects and patients with moderate chronic obstructive lung disease during arm and leg ergometry have produced variable results. Davies and Sargeant (22) reported in a group of normal
subjects that the higher ventilation required for arm exercise
at an equivalent O2 was almost entirely due to an increase in
respiratory rate whereas Bevegard and associates (28) found
that the higher ventilation with arm exercise was achieved by
increases in both respiratory rate and tidal volume. In the
studies of patients with moderate chronic airflow limitation,
Owens and colleagues (30) demonstrated no significant differences between arm and leg ergometry in values for respiratory
rate and tidal volume at maximal and submaximal exercise. In
contrast, our results demonstrate that the higher ventilation
for arm exercise in CF subgroups was largely due to a higher
respiratory rate.
This study highlights that subjects with CF with severe lung
disease experience marked dyspnea for a given level of exercise. This was especially true for arm exercise. Our subjects
with severe lung disease had a significantly higher minute ventilation at an equivalent O2 than control subjects and a correspondingly higher dyspnea score. This is in agreement with
work by Wilson and Jones (31) who demonstrated a significant relationship between dyspnea and minute ventilation in
normal subjects. Although our subjects with severe lung disease had higher dyspnea scores than the Control Group at the
same relative O2, at peak work capacity the dyspnea scores
for the Severe Group were similar for arm and leg exercise
and lower than the Control Group. This suggests that dyspnea
was not the overriding sensation at the termination of exercise
in those CF subjects with severe lung disease. It is possible
that in these subjects other factors such as peripheral muscle
deconditioning may affect exercise performance. It has recently been demonstrated in subjects with chronic obstructive pulmonary disease (FEV1 = 43 ± 19% predicted) that peripheral muscle weakness contributed to exercise limitation (32).
Alternatively, subjects with long-term chronic lung disease
like those with CF may become desensitized to dyspnea.
In summary, arm exercise required a significantly higher ventilation than leg exercise in both control subjects and subjects with severe lung disease due to CF. Subjects with mild and moderate lung disease due to CF had well-preserved arm exercise capacity while those with severe lung disease had reduced arm exercise capacity. This reduction was most likely due to a limitation in ventilatory capacity.
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Footnotes |
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Correspondence and request for reprints should be addressed to Assoc. Prof. P. T. P. Bye, Department of Respiratory Medicine, Level 10, Page Chest Pavilion, Royal Prince Alfred Hospital, Missenden Road, Camperdown, 2050, NSW, Australia.
(Received in original form February 11, 1997 and in revised form June 9, 1997).
Acknowledgments: The authors wish to acknowledge the helpful comments and suggestions of Professor Neil Pride and the assistance of Nathan Brown in the preparation of the figures.
Supported by NH&MRC Biomedical Scholarship.
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References |
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES
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