(Chest. 2000;118:1460-1469.)
© 2000
American College of Chest Physicians
Aerobic Conditioning in Mild Asthma Decreases the Hyperpnea of Exercise and Improves Exercise and Ventilatory Capacity*
Teal S. Hallstrand, MD;
Peter W. Bates, MD, FCCP and
Robert B. Schoene, MD
*
From the Division of Pulmonary and Critical Care Medicine (Drs. Hallstrand and Schoene), University of Washington, Seattle, WA; and the Department of Medicine (Dr. Bates), Maine Medical Center, Portland, ME.
Correspondence to: Teal S. Hallstrand, MD, Division of Pulmonary and Critical Care Medicine, Department of Medicine, University of Washington, 1959 NE Pacific St, BB-1253 Health Sciences Center, Box 356522, Seattle, WA 98195-8673;e-mail: tealh{at}u.washington.edu
 |
Abstract
|
|---|
Study objective: To determine the effect of an aerobic
conditioning program on fitness, respiratory physiology, and resting
lung function in patients with mild asthma.
Design:
Prospective cohort study.
Setting: Outpatient
rehabilitation facility.
Methods: Five patients with
mild intermittent asthma and five normal control subjects completed a
10-week aerobic conditioning program. Pulmonary function studies and
noninvasive cardiopulmonary exercise tests were performed before and
after the conditioning program.
Results: After aerobic
conditioning, there were significant gains in maximum oxygen
consumption (
O2max; 22.73 mL/kg/min vs
25.29 mL/kg/min, p = 0.01, asthma; 22.94 mL/kg/min vs 27.85
mL/kg/min, p = 0.03, control) and anaerobic threshold (0.99 L/min vs
1.09 L/min, p = 0.03, asthma; 0.89 L/min vs 1.13 L/min, p = 0.01,
control) in both groups. Although FEV1 was unchanged, the
maximum voluntary ventilation (MVV) improved in the asthma group (96.0
L/min vs 108.2 L/min, p = 0.08, asthma; 134.0 L/min vs 131.2 L/min,
p = 0.35, control). During exercise, minute ventilation
(E) for each level of work was decreased in the
asthma group after conditioning, while little change occurred in the
control group (68.48 L/min vs 51.70 L/min at initial
O2max, p = 0.02, asthma; 65.82 L/min
vs 63.12 L/min at initial O2max,
p = 0.60, control). A significant decrease in the ventilatory
equivalent (E/oxygen consumption, 40.8 vs 30.4 at
O2max, p = 0.02, asthma; 37.2 vs 35.8
4 at O2max, p = 0.02,
control) and the dyspnea index (E/MVV) at submaximal
(0.44 vs 0.38, p = 0.05, asthma; 0.32 vs 0.38, p < 0.01, control)
and maximal exercise (0.72 vs 0.63, p = 0.03, asthma; 0.49 vs 0.62,
p = 0.02, control) occurred in the asthma group.
Conclusions: Exercise rehabilitation improves aerobic
fitness in both asthmatic and nonasthmatic participants of a 10-week
aerobic fitness program. Additional benefits of improved ventilatory
capacity and decreased hyperpnea of exercise occurred in patients with
mild asthma.
Key Words: asthma • exercise-induced bronchospasm • rehabilitation
|
Introduction
|
|---|
The
physiologic effect of aerobic training in adults with asthma remains to
be clearly delineated. The notion that conditioning is beneficial in
asthmatics dates to
the mid-19th century.1
Aerobic conditioning improves
fitness and pulmonary symptoms in individuals with asthma. In children
with asthma, aerobic conditioning improves resting lung function,
dyspnea scores, and social development scores, and decreases
exercise-induced bronchospasm and peak expiratory flow
variability.2
3
4
5
In adults with asthma, conditioning
decreases exercise-induced bronchospasm and improves exercise
tolerance and quality of life.6
7
8
9
The fundamental basis of these effects of aerobic conditioning in
adults with asthma remains unclear. Improvement in peak expiratory flow
variability and decreased medication use in children suggests a decline
in airway inflammation; however, this has not been demonstrated
directly. Adults and children increase their exercise tolerance after
training without demonstrable changes in airflow
obstruction.8
9
10
11
12
13
Individuals with asthma are limited
during exercise by a low maximum voluntary ventilation (MVV) and a high
minute ventilation (E) for a particular
workload.6
14
15
The MVV is decreased in individuals with
asthma, either directly from fixed airflow obstruction or from
increased airway hyperresponsiveness that causes a decline in airway
conductance during the MVV maneuver.16
Ventilatory
efficiency is reduced, reflected by an increased E
for a particular workload.6
These factors are described
together in the dyspnea index (E/MVV). In mild to
moderate asthma, the dyspnea index is elevated, although not to the
degree that would conventionally define ventilatory
limitation.14
15
This increase in the degree of dyspnea
during aerobic activities may affect exercise tolerance and lead to
deconditioning.6
11
13
14
Despite these barriers, many
individuals with asthma take part in aerobic activities, even at the
highest levels of competition.17
To determine the effect of aerobic conditioning on exercise tolerance
and pulmonary physiology, we prospectively enrolled a group of patients
with mild asthma and a group of normal control subjects in a 10-week
conditioning program. We hypothesized that an aerobic exercise program
would have beneficial effects on exercise tolerance, fitness,
ventilatory efficiency, and lung function.
|
Materials and Methods
|
|---|
Subjects
A group of nine adult patients with mild intermittent asthma as
defined by the National Asthma Education and Prevention Program, Expert
Panel Report 218
were recruited for this study. The asthma
group was restricted to nonsmoking, sedentary individuals who required
only intermittent short-acting ß2-agonist
therapy in the 3 months preceding the study. Seven sedentary
individuals without a history of asthma were recruited for the control
group. Of these 16 individuals initially screened for the study, 6
individuals were excluded during the run-in period due to poor
compliance with the exercise regimen and were not included in the
study. Five individuals in each group entered the 10-week conditioning
program. The study protocol was approved by the human subjects review
committee of the Maine Medical Center.
Lung Function and Exercise Testing
Baseline lung function testing, including
FEV1 and MVV based on a 12-s trial, was performed
on a plethysmograph (model 6200; SensorMedics; Yorba Linda,
CA), according to American Thoracic Society
guidelines.19
Each participant underwent a
noninvasive, progressive exercise trial on a cycle ergometer
(Ergoline 800S; SensorMedics) to maximum oxygen consumption
(O2max). Individuals with
asthma were instructed not to use short-acting
ß2-agonists during the 4 h preceding the
test. The initial workload and rate of progression were selected, such
that each participant would reach
O2max after approximately 12
min. To standardize the stimulus for exercise-induced bronchospasm, the
participants continued to cycle at a power output of 60 W after the
maximum workload was achieved for a total of 15 min of exercise. After
completing the exercise trial, FEV1 was obtained
3, 6, 10, and 15 min after exercise.
Respiratory rate, tidal volume (VT), heart rate,
E, oxygen consumption
(O2), carbon dioxide
production (CO2), and
end-tidal carbon dioxide pressure
(PETCO2) were measured on a metabolic
cart (model 2900; SensorMedics). The anaerobic threshold was determined
by the V-slope method using the point of divergence of the slopes of
CO2 and
O2, expressed in terms of
O2.20
The
ventilatory equivalent was calculated by dividing E
by O2. The dyspnea index at
75% of maximum and at O2max
was calculated by dividing the E at each level of
O2 by the measured
MVV.14
15
Respiratory rate, VT,
E, CO2, and
Bohr dead space ratio (VD/VT) were determined
at 20% increments of O2max.
VD/VT was determined using the
PETCO2 substituted for
PaCO2 in the
VD/VT equation.20
Conditioning Program
Study participants were enrolled in an aerobic conditioning
program consisting of step aerobics three times a week for 10 weeks.
The fitness program was supervised by a physical therapist or an
exercise physiologist. Both the asthma and control groups exercised
together. Each participant learned to measure his or her heart rate at
the start of the conditioning program. During each session, heart rate
was monitored such that a target heart rate equal to that required for
70% O2max was achieved.
During each session, participants attempted to maintain their target
heart rate for at least 30 min. Participants with asthma were allowed
to use ß2-agonist therapy as needed during the
exercise program. During the fitness program, both groups were asked to
maintain a diary of medication use, daytime and nighttime asthma
symptoms, and cough.
At the conclusion of the exercise program, lung function and exercise
testing were repeated according to the baseline studies. The
postconditioning dyspnea index was calculated at 75% of maximum and at
O2max based on the measured
O2max in the postconditioning
exercise trial. Respiratory rate, VT, E,
CO2, and
VD/VT were recorded at 20, 40, 60, 80, and
100% of the pretraining O2max
during the postconditioning exercise trial.
Statistical Analysis
Spirometric values (FEV1, MVV, and decline
in FEV1 after exercise), before and after the
conditioning program, were compared using a paired t
test. The level of significance was based on a two-tailed distribution,
except in the case of MVV, in which a one-tailed critical value is
justified by prior studies.7
13
Comparison of physiologic
variables during exercise, before and after conditioning, were made
using paired t tests at each level of
O2.
|
Results
|
|---|
Participant Characteristics
The five participants in each group were similar in age, height,
weight, and gender (Table 1
). All patients in the asthma group reported a history of atopy, and
four patients reported a history of exercise-induced bronchospasm. The
participants in the asthma group used inhaled short-acting
ß2-agonists (eg, albuterol) on
average 2.8 times per week and reported episodic wheezing and
occasional cough.
Spirometry and Respiratory Symptoms
Baseline lung function in the asthma group was normal,
except for a reduction in the MVV. The asthma group demonstrated a
postexercise reduction in FEV1 of 6.1% (range, 0
to 18%; p < 0.01 vs control). After the 10-week conditioning
program, there was no change in FEV1,
FEV1/vital capacity ratio, or exercise-induced
bronchospasm in either group (Table 2
), although there was a trend toward improvement in the MVV in the
asthma group (Fig 1
). There was no significant change in bronchodilator use, daytime or
nocturnal asthma symptom scores, or cough after the conditioning
program.
Fitness
Both groups made significant gains in measures of fitness
after the 10-week conditioning program (Table 3
). Comparable gains in O2max
and anaerobic threshold were realized in the asthma and control groups
(Fig 2
,
3
).
Respiratory Physiology
At 75% of maximum and at maximum exercise, the dyspnea
index was elevated in the asthma group during the baseline exercise
trial (Table 3)
. After 10 weeks of conditioning, the dyspnea index was
significantly reduced at 75% of maximum and maximum exercise in the
asthma group, while the dyspnea index rose in the control group (Fig 4
,
5
). Prior to conditioning, the ventilatory equivalent for oxygen at
maximum exercise was elevated in the asthma group, compared to the
control group (Table 3)
. After the conditioning program, the
ventilatory equivalent at 75% of maximum and maximum exercise
decreased significantly in the asthma group, while only minor changes
occurred in the control group (Table 3)
.
The maximum values for work rate, E,
O2,
E/O2,
VT, respiratory rate, and VD/VT
before and after the conditioning program are presented in Table 3
.
During exercise, the E at each level of
O2 was reduced in the asthma
group after the conditioning program, while little change occurred in
the control group (Fig 6
). The VTs during exercise were similar for both trials in
the asthma and control groups. The respiratory rate at each level of
O2 was reduced in both groups
after the conditioning program, but the magnitude of this difference
was greater in the asthma group (Fig 7
). Measured CO2 was reduced for
each level of O2 in both
groups after the conditioning program; however, the magnitude of this
decrease was greater in the asthma group (Fig 8
). The VD/VT ratio declined during exercise in
both groups, and there was no difference between the groups. There was
a trend in the partial pressure of
PETCO2 toward an increase in the
asthma group after the conditioning program, while no change occurred
in the control group (Fig 9 ).
|
Discussion
|
|---|
This study demonstrates that exercise rehabilitation improves
aerobic fitness and decreases the hyperpnea of exercise in patients
with mild asthma. After 10 weeks of aerobic conditioning, patients with
asthma and a control group composed of nonasthmatic individuals
significantly increased their
O2max and increased their
anaerobic threshold. While baseline FEV1 remained
unchanged, the asthma group showed an increase in the MVV to within the
normal range. After the conditioning program, there was a decrease in
E for each level of work that occurred only in the
asthma group. There was a reduction in the respiratory rate and a rise
in the PETCO2 during exercise.
Conditioning improved the ventilatory efficiency in the asthma group,
reflected by a decrease in the ventilatory equivalent for oxygen and a
reduction in the dyspnea index at submaximal and maximal exercise.
These results show that in addition to improving fitness, aerobic
conditioning increases ventilatory capacity and decreases the hyperpnea
of exercise in patients with mild asthma.
Respiratory symptoms may cause asthmatics to avoid exercise, resulting
in aerobic fitness that is below that of their peers.6
13
Disease severity judged by FEV1 is not the
primary determinant of fitness in individuals with asthma, and aerobic
capacity can improve without a change in resting lung
function.11
21
Exercise tolerance is reduced primarily
from an increased sensation of dyspnea during
exercise.6
14
15
For a given workload, deconditioned
individuals with asthma maintain higher E than
similarly deconditioned control subjects without
asthma.6
22
The capacity to increase E
may also be diminished in individuals with asthma. The summation of
these physiologic parameters is described in the dyspnea index, which
is increased in individuals with asthma during exercise and likely
represents the primary barrier to aerobic activities in most
asthmatics.14
15
These data demonstrate that an aerobic
conditioning program improves the MVV and decreases the
E at a given workload, resulting in a decreased
dyspnea index and ventilatory equivalent after conditioning in patients
with mild asthma.
The capacity to increase E, as quantified by the
MVV, may be limited in individuals with asthma. The MVV may be
diminished as a direct consequence of airflow obstruction, but may be
further reduced due to airway hyperresponsiveness.16
The
MVV/FEV1 ratio is a reflection of increased
airway hyperresponsiveness, and the MVV maneuver causes a decrease in
airway conductance in individuals with asthma, but not normal
subjects.16
Aerobic conditioning improves the MVV in
patients with asthma,7
13
although the mechanism of this
improvement remains unclear. Increased respiratory muscle strength has
been cited as a possible mechanism for improvement in the MVV after
conditioning7
; however, this mechanism is not supported by
the present data, since a similarly deconditioned control group did not
show comparable gains in MVV. Improvement in the MVV could also reflect
subtle changes in lung function or airway reactivity not detected by
the FEV1 maneuver. In children, conditioning
reduces air trapping, placing the diaphragm in a more advantageous
position mechanically.4
Conditioning also decreases peak
expiratory flow variability, asthma symptom scores, and medication use
in children, suggesting a decrease in airway inflammation; however, it
is unclear how conditioning could affect airway
inflammation.3
5
6
10
In the present study, there was no
evidence of a change in disease activity, likely reflecting the mild
intermittent nature of the disease in our study population.
Individuals with asthma maintain a high E during
exercise.6
22
These data and previous studies demonstrate
that conditioning decreases E per level of work in
patients with asthma.6
9
22
Aerobic conditioning results
in a modest decrease in E in all subjects through an
improvement in anaerobic threshold; however, the magnitude of this
decrease is greater in individuals with asthma,6
and these
data show a reduction in E prior to the anaerobic
threshold. E was reduced by a decline in the
respiratory rate with maintenance of the preconditioning VT
and an increase in the PETCO2. No
change was noted in the VD/VT. These data
suggest that a blunted ventilatory response to exercise occurs in
response to conditioning in individuals with mild asthma. Reductions in
the ventilatory response to exercise have also been noted in
well-trained athletes, likely representing an adaptation to
conditioning.23
Further study is necessary to determine if
a change in central respiratory drive occurs in response to
conditioning.
E is an important determinant of the amount of
exercise-induced bronchospasm.24
The severity of
exercise-induced bronchospasm was similar in both trials, reflecting a
similar maximum E in both the preconditioning and
postconditioning trials. These data are consistent with the results of
other conditioning programs that show no change in the severity of
exercise-induced bronchospasm after a postconditioning maximal exercise
test in which the participants achieved a higher level of
work.25
26
27
The amount of exercise-induced bronchospasm
declines after conditioning if the amount of work is held constant in
the postconditioning exercise test due to the lower resultant
E.10
28
If the total
E is kept constant in the postconditioning trial, a
small improvement occurs in the amount of exercise-induced
bronchospasm.7
8
These data reinforce the importance that
a reduction in E and an improvement in ventilatory
efficiency play in the ability of patients with asthma to exercise
effectively.
Exercise rehabilitation in patients with mild intermittent asthma
improves aerobic fitness and ventilatory efficiency. Aerobic
conditioning is well tolerated and leads to fitness gains similar to
those in nonasthmatic individuals. An improvement in ventilatory
capacity and a decrease in the hyperpnea of exercise that was present
prior to conditioning in asthmatics occurred after aerobic conditioning
in patients with asthma, but not in normal control subjects. We
conclude that physical training results in beneficial adaptations that
allow individuals with mild asthma to participate comfortably in
aerobic activities. Further study is necessary to determine the
underlying basis of these adaptations.
|
Acknowledgements
|
|---|
The authors thank Clifford Hoover and John Rojecki
for their assistance with cardiopulmonary exercise testing and
pulmonary function studies. We greatly appreciate the thoughtful
comments of Drs. Joshua O. Bendit and H. Thomas Robertson during the
preparation of this article.
|
Footnotes
|
|---|
Abbreviations: MVV = maximum voluntary ventilation;
PETCO2 = end-tidal carbon dioxide pressure;
CO2 = carbon dioxide production;
VD/VT = Bohr dead space ratio;
E = minute ventilation;
O2 = oxygen consumption;
O2max = maximum oxygen consumption;
VT = tidal volume
Funding provided by the Maine Medical Center Research
Committee.
Received for publication December 30, 1999.
Accepted for publication May 31, 2000.
|
References
|
|---|
-
Salter, HH (1882) On asthma: its pathology and treatment. 1st American ed. ,163-164 Wood New York, NY.
-
Engstrom, I, Fallstrom, K, Karlberg, E, et al (1991) Psychological and respiratory physiological effects of a physical exercise programme on boys with severe asthma. Acta Paediatr Scand 80,1058-1065[ISI][Medline]
-
Huang, SW, Veiga, R, Sila, U, et al (1989) The effect of swimming in asthmatic children-participants in a swimming program in the city of Baltimore. J Asthma 26,117-121[ISI][Medline]
-
Ramazanoglu, YM, Kraemer, R (1985) Cardiorespiratory response to physical conditioning in children with bronchial asthma. Pediatr Pulmonol 1,272-277[Medline]
-
Szentagothai, K, Gyene, I, Szocska, M, et al (1987) Physical exercise program for children with bronchial asthma. Pediatr Pulmonol 3,166-172[ISI][Medline]
-
Robinson, DM, Egglestone, DM, Hill, PM, et al (1992) Effects of a physical conditioning programme on asthmatic patients. N Z Med J 105,253-256[ISI][Medline]
-
Haas, F, Pasierski, S, Levine, N, et al (1987) Effect of aerobic training on forced expiratory airflow in exercising asthmatic humans. J Appl Physiol 63,1230-1235[Abstract/Free Full Text]
-
Freeman, W, Nute, MG, Williams, C (1989) The effect of endurance running training on asthmatic adults. Br J Sports Med 23,115-122[Abstract]
-
Cochrane, LM, Clark, CJ (1990) Benefits and problems of a physical training programme for asthmatic patients. Thorax 45,345-351[Abstract]
-
Emtner, M, Herala, M, Stalenheim, G (1996) High-intensity physical training in adults with asthma: a 10-week rehabilitation program. Chest 109,323-330[Abstract/Free Full Text]
-
Ludwick, SK, Jones, JW, Jones, TK, et al (1986) Normalization of cardiopulmonary endurance in severely asthmatic children after bicycle ergometry therapy. J Pediatr 109,446-451[CrossRef][ISI][Medline]
-
Nickerson, BG, Bautista, DB, Namey, MA, et al (1983) Distance running improves fitness in asthmatic children without pulmonary complications or changes in exercise-induced bronchospasm. Pediatrics 71,147-152[Abstract/Free Full Text]
-
Orenstein, DM, Reed, ME, Grogan, FT, Jr, et al (1985) Exercise conditioning in children with asthma. J Pediatr 106,556-560[CrossRef][ISI][Medline]
-
Clark, CJ, Cochrane, LM (1988) Assessment of work performance in asthma for determination of cardiorespiratory fitness and training capacity. Thorax 43,745-749[Abstract]
-
Clark, CJ (1992) The role of physical training in asthma. Chest 101,293S-298S[Abstract/Free Full Text]
-
Fairshter, RD, Carilli, A, Soriano, A, et al (1989) The MVV/FEV1 ratio in normal and asthmatic subjects. Chest 95,76-81[Abstract/Free Full Text]
-
Voy RO. The U.S. Olympic Committee experience with exercise-induced bronchospasm, 1984. Med Sci Sports Exerc 1986; 18:328–330
-
National Asthma Education and Prevention Program. Expert panel report 2: guidelines for the diagnosis and management of asthma. Bethesda, MD: National Institutes of Health, April 1997; Publication No. 97–4051A
-
Standardization of spirometry, 1994 update: American Thoracic Society. Am J Respir Crit Care Med 1995; 152:1107–1136
-
Wasserman, K, Hansen, JE, Sue, DY, et al (1994) Principles of exercise testing and interpretation 2nd ed. ,457 Lea and Febiger Malvern, PA.
-
Garfinkel, SK, Kesten, S, Chapman, KR, et al (1992) Physiologic and nonphysiologic determinants of aerobic fitness in mild to moderate asthma. Am Rev Respir Dis 145,741-745[ISI][Medline]
-
Varray, AL, Mercier, JG, Terral, CM, et al (1991) Individualized aerobic and high intensity training for asthmatic children in an exercise readaptation program: is training always helpful for better adaptation to exercise? Chest 99,579-586[Abstract/Free Full Text]
-
Martin, BJ, Sparks, KE, Zwillich, CW, et al (1979) Low exercise ventilation in endurance athletes. Med Sci Sports 11,181-185[ISI][Medline]
-
Deal, EC, Jr, McFadden, ER, Jr, Ingram, RH, Jr, et al (1979) Hyperpnea and heat flux: initial reaction sequence in exercise-induced asthma. J Appl Physiol 46,476-483[Free Full Text]
-
Bundgaard, A, Ingemann-Hansen, T, Schmidt, A, et al (1982) Effect of physical training on peak oxygen consumption rate and exercise-induced asthma in adult asthmatics. Scand J Clin Lab Invest 42,9-13[ISI][Medline]
-
Fitch, KD, Morton, AR, Blanksby, BA (1976) Effects of swimming training on children with asthma. Arch Dis Child 51,190-194[Abstract]
-
Fitch, KD, Blitvich, JD, Morton, AR (1986) The effect of running training on exercise-induced asthma. Ann Allergy 57,90-94[ISI][Medline]
-
Arborelius, M, Jr, Svenonius, E (1984) Decrease of exercise-induced asthma after physical training. Eur J Respir Dis Suppl 136,25-31[Medline]
This article has been cited by other articles:
|
|
|
|
 
E.N. Kosmas, J. Milic-Emili, A. Polychronaki, I. Dimitroulis, S. Retsou, M. Gaga, A. Koutsoukou, Ch. Roussos, and N.G. Koulouris
Exercise-induced flow limitation, dynamic hyperinflation and exercise capacity in patients with bronchial asthma
Eur. Respir. J.,
September 1, 2004;
24(3):
378 - 384.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
A. Pastva, K. Estell, T. R. Schoeb, T. P. Atkinson, and L. M. Schwiebert
Aerobic Exercise Attenuates Airway Inflammatory Responses in a Mouse Model of Atopic Asthma
J. Immunol.,
April 1, 2004;
172(7):
4520 - 4526.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
C. J. Worsnop
Asthma and Physical Activity
Chest,
August 1, 2003;
124(2):
421 - 422.
[Full Text]
[PDF]
|
|
|
TOP
Abstract
Introduction
) and after (
) 10
weeks of aerobic conditioning in patients with mild intermittent asthma
and in normal control subjects.
