Pediatric Exercise Science, 1992, 4, 351 -359

Association of Exercise-Induced
Bronchospasm With Obesity
Ted A. Kaplan, Mary Helen Campbell-Shaw, and Gina Moccia
Exercise-induced bronchospasm (EIB) is present in many patients with
asthma or with a family history of atopy. A review was made of exercise
provocation testing performed on 37 children ages 5 to 17 years. Maximal
forced expiratory maneuvers were performed before and serially every
3 minutes after a 7-min runlwalk. A positive result was defined as a fall of
at least 15% in FEV, or PEFR or 25% in FEF,,,, at some point within
20 min postexercise. A total of 27 out of 37 patients in this select group had
positive tests (73%), with a mean fall in FEF,,, of 31.9%. Of these 27
children with EIB, 16 had a history of atopy, 23 had clinical symptoms of
EIB, and 21 were overweight. Of the 12 nonatopic children with EIB, 9 were
overweight, with a mean fall in FEF,,,, of 32.1%. These 9 came from a total
pool of 10 overweight, nonatopic children (90%). Being overweight was
associated with a high incidence of EIB independent of a history of atopic
disease.

Short-term, dynamic exercise can trigger bronchospasm by various mechanisms, including hyperventilation (1, 9, 14, 21). This phenomenon of exerciseinduced bronchospasm (EIB) can be symptomatic with wheezing, coughing, or
respiratory distress, or more insidiously, with chest pain (19), dyspnea, or easy
fatigability. Symptoms occur during or frequently soon after the exercise bout,
remit spontaneously within an hour or with bronchodilator treatment, and may
recur as a secondary response after a few hours (1, 9, 14).
Some of these symptoms that are less obviously of respiratory origin might
be confused with cardiac disease or simply poor cardiopulmonary fitness. One
way of clinically differentiating EIB from these and other possible etiologies is
the presence of a known risk factor for EIB in the patient's history. While some
studies have shown EIB to be present in about 3 to 10% of the general population
(5,22), studies have documented EIB in the majority of patients with asthma (18,
22).
Nonasthmatic patients with atopic disease (18,22), family history of atopic
disease (22), personal or family history of being a "wheezy infant" (lo), or cystic

The authors are with the Children's Sports and Exercise Medicine Center in South
Miami. Kaplan and Moccia are also with the Dept. of Pediatrics, Univ. of Miami School
of Medicine, Miami, FL. Request reprints from Dr. Kaplan, Children's Sports and Exercise
Medicine Ctr., 5975 Sunset Dr., Suite 101, S. Miami, FL 33143.

352 - Kaplan, Campbell-Shaw, and Moccia

fibrosis (25) all have intermediate risk for EIB (25 to 50%). These studies tested
for EIB by performing objective bronchospasm evaluation studies (8, 11,24) on
selected groups of children and adults. Challenges that can produce bronchospasm
in individuals with hyperreactive airways include exercise (5, 18, 22, 25), in the
laboratory or field setting, and methacholine (17). This type of approach can also
be used for diagnosing or evaluating treatment in patients with known or suspected
EIB (I, 21).
In the course of performing EIB evaluations on patients with the risk factors
or symptoms listed above, it became apparent that many of them also were
overweight. Interestingly, many of these patients presented with obesity as their
chief complaint; other factors associated with EIB surfaced in the course of the
medical history or were recalled after the EIB test result proved positive. Evaluation for EIB was subsequently done on all overweight patients. We then reviewed
the results of EIB testing in our laboratory to compare the rate of EIB in patients
with varying histories and presentations and evaluate the strength of this newly
observed association of EIB with obesity in atopic and nonatopic children.

Patients and Methods

The records of patients receiving exercise provocation spirometry testing between
August I989 and November 1991 were reviewed. Patients were referred or selfreferred for exercise related symptoms, evaluations of exercise performance, and/
or for prescription of therapeutic exercise programs. Testing was not attempted
on children less than 5 years of age. The results of patients with cystic fibrosis
were excluded from this review. Patients came with their parents for a complete
history and physical examination before testing. Any bronchodilator medications
that were used regularly or episodically were withheld on the day of testing. The
testing procedure was supervised by a physician after determining that the patients
were stable for testing, having no signs of wheezing, respiratory distress, or acute
illness.
Flow-volume loops were obtained by forced expiratory maneuvers after
demonstration and a few practice efforts and were analyzed by a pneumotachograph computerized spirometer (Multispiro, Medical Equipment Designs, Inc.,
Laguna Hills, CA). Among the parameters measured were forced vital capacity
(FVC), forced expiratory volume in the first second (FEV,), peak expiratory flow
rate (PEF), and forced expiratory flow between 25 and 75% of FVC (FEF,,,,).
The lowest possible number of preexercise efforts were requested to obtain at least
two consistent best performances as determined by reviewing the instantaneously
calculated results. A best test was chosen, based first on the test with the highest
FVC; however, if there was another test with an FVC insignificantly (less than
5%) lower but a significantly higher result in the other three primary variables,
it was instead chosen as the best.
The exercise tests were performed in an indoor, air-conditioned laboratory,
with temperature maintained between 23 and 26 "C and relative humidity between
60 and 70%. The exercise challenge was based on findings in the literature as to
the most effective mode, duration, and intensity of exercise (1, 8, 11). Patients
were fitted with a heart rate monitor/recorder (CIC Heartwatch, Computer Instruments Corp., Hempstead, NY). No warm-up was provided. The treadmill was set
at a 10% grade. Initial speed ranged from 2.5 to 4.0 mph depending on a subjective

Exercise-Induced Bronchospasm - 353

estimate of the patient's exercise ability, and then was adjusted based on the heart
rate response and the patient's ease of adaptation to treadmill movement.
The patients were encouraged not to hold on to the handrails and to run as
much as possible; however, handrail holding was allowed and most patients
walked during most of the exercise challenge. The ultimate criteria for a successful
challenge was attainment of a heart rate of 170 bpm, which is approximately 85%
of the predicted maximal heart rate for this age group (using the formula 220 age). The treadmill speed was increased in a manner to reach this level of exercise
heart rate as soon as possible, preferably within 1-1/2 minutes. Speed was reduced
if exercise heart rate continued to climb steadily after attaining 170. The exercise
challenge lasted 7 minutes.
After the conclusion of the exercise challenge, the heart rate monitor was
removed and the patients rested until 2 minutes postexercise. Patients then began
postexercise spirometry, performing serial forced expiratory maneuvers every 3
minutes until 20 minutes postexercise. The worst postexercise test was selected
based on the test with the greatest drop in FEV, andlor FEF25.75
that was in greater
proportion than any fall in FVC. A positive result for EIB was defined as 215%
fall in FEV, or PEF or 225% fall in FEF,,,, at any point within 20 minutes after
exercise.
If any significant fall in pulmonary function or any symptoms were still
apparent at 20 minutes, two puffs (180 micrograms) of albuterol were administered by inhalation. Lung auscultation to subjectively evaluate air exchange was
performed preexercise and immediately postexercise; it was repeated if any
changes were found on spirometry. Although oxygen was available for any patient
who might have developed significant respiratory distress or significant wheezing,
it was never needed for those indications.
Patients were retrospectively assigned to any of the following categories
that applied to them based on a review of their records and the following criteria:
Asthma: by personal history of asthma, wheezing, or bronchodilator prescription (e.g., for bronchitis);
Atopy: by personal history of allergic rhinitis, food or drug allergy, or
urticaria;
Family history of atopic disease: any atopic disease (including asthma,
allergic rhinitis, or other atopic disease) in any first- or second-degree
relative (a standard family history section is present in all charts);
Symptoms of EIB: exercise related cough, chest pain, wheezing, exertional
dyspnea, or easy fatigability (a standard questionnaire for EIB symptoms
is present in all charts);
Obesity: at least 20% estimated body fat for boys, 30% for girls, as estimated
by skinfold measurements at the biceps, triceps, subscapular, and suprailiac
sites by the method of Durnin and Womersley (7). All patients in the obesity
group were also below the 10th percentiles (lower percentiles indicate
higher body fat) for age and sex in the more age-appropriate tables of
Johnston et al. (12, 13) for the sum of triceps and subscapular folds.
A t test was used to compare the mean fall in pulmonary function parameters
between best and worst tests for the different groups. The z statistic for comparing
proportions was used to compare the EIB incidence between various groups.

354 - Kaplan, Campbe!/-Shaw, and Moccia

Results
Table I lists the numbers of patients falling into each of the identified known risk
factors and the number in each category having a positive result on exercise
challenge. Each group is subdivided into those patients found to be obese and
those falling below the obesity cutoff used in this study. This breakdown is
reversed in the lower portion of Table 1, where all obese patients are considered,
and these children are further subdivided to demonstrate the presence or absence
of the known risk factors.
Many patients fell into more than one known risk factor category and/or
the obese category. Of the obese patients, 81% (21 of 26) tested positive for
EIB. This association is of equal or greater strength than with any other factor.
Removing patients with a history of asthma or any other atopic disease from the
obese group, a 90% incidence (9 of 10) of a positive exercise challenge was
found. Six of these 9 did have a family history of atopic disease, which was a
strong risk factor in the overall group (73%). The differences found between the
incidences of EIB in the obese nonatopic group (OB-NA) (90%) and all atopic
patients (AT) (15 of 22,68%), and between those in all obese patients (81%) and
all nonobese patients (64%), were not statistically significant.
Table 2 demonstrates the effectiveness of the symptom history at predicting
EIB. This was a reasonably sensitive method, with 70% (23 of 33) of the patients
who indicated any symptom of EIB having EIB. Overall, 89% of the patients had
at least one symptom, with a false positive rate of 29% (9 of 31). Of 17 patients
Table 1
Positive Exercise Challenge by Patient Categories
n

Category and subcategories

Asthma (fother allergies)

Allergic, nonasthmatic
Family history of atopy
All patients

+ EIB (%)

Obese
Not obese
Obese
Not obese
Obese
Not obese
Obese
Not obese
Asthma or atopy
Nonatopic
Atopic family history
No personal or family atopic history
EIB symptoms
= Total

Note. Patients with known atopic risk factors categorized by presence or absence of obesity.
tObese patients categorized for presence of known risk factors for EIB.
Total is not a sum of columns; refers to all obese patients.

Exercise-Induced Bronchospasm - 355

Table 2
EIB Symptoms and Positive Exercise Challenge Tests

+ ECT

Wheezing

Obese
Not obese
Obese
Not obese
Obese
Not obese
Obese
Not obese
Obese
Not obese
Obese
Not obese

Cough
Chest painltightness
Shortness of breathldyspnealeasily fatigued
Wheezing or cough
Any symptom

Note. + ECT = positive exercise challenge test.

Table 3
Maximum Postexercise Decreases in FEV,, PEF, and FEF25-75
in Patients Who Had Positive Exercise Challenges (M+ SD)

All atopic
Obese nonatopic

15
9

FEV,
(Liters)
(% fall)

PEF
(Usec)
(% fall)

-0.27 + 0.23
(-1 3.9 + 11.8%)
-0.43 + 0.28
(-1 2.4 + 13.5%)

-0.96 + 0.77
(-22.6 + 17.4%)
-1.77 + 1.32*
(-29.4 + 17.4%)

FEFz5-75
(Usec)
(% fall)

-0.66
(-33.7
-0.92
(-32.1

+ 0.36
+ 11.5%)
+ 0.47
+ 13.2%)

* p < 0.01 for PEF fall in obese nonatopic group vs. all atopic.

with cough or wheezing, only 10 (59%)were corroborated by a positive exercise

challenge test.
Table 3 gives the decreases (M SD) in the three analyzed pulmonary
function variables that reflect upon airway obstruction only for the patients with
positive exercise challenge tests, in order to demonstrate the degree of bronchial
reactivity. It can be seen that more impressive decreases came in the FEF,,,,
values than in the FEV, for both AT patients with EIB (n=15) and for OB-NA
patients with EIB (n=9). (These two groups are nonintersecting.) There was a
significantly greater (pc.01) mean fall in PEF in OB-NA with EIB than in AT
with EIB.

356

- Kaplan,

Campbell-Shaw, and Moccia

Discussion
The results of this study confirm the previous findings that a personal history of
asthma or other atopic disease, a family history of atopic disease, or a history
of wheezing, cough, chest pain, dyspnea, or easy fatigue with dynamic exercise
is frequently associated with EIB. It was also found that obesity, with or without
a personal history of atopic disease, also had an independent and strong association
with EIB. Not only was there a high incidence of EIB in OB-NA patients but the
degree of bronchial reactivity in that group was comparable (about 30% mean
fall in FEF2575) to that seen in atopic patients.
Only 10 of 28 cases of EIB would be discovered clinically by the patient
admitting to respiratory symptoms such as wheezing or cough. Only in the
minority of cases of a history of wheezing was EIB found on objective testing.
Whether the patients misinterpreted the sensation or meaning of wheezing or
whether the exercise challenge was not able to reproduce the conditions that
induced wheezing in those patients is not clear. While 23 of the 28 cases could
be diagnosed clinically by adding chest pain and exertional dyspnea and fatigue
to the history, these latter symptoms are not specific to the respiratory system and
would not always warrant the treatment that would be given for EIB (1, 21).
This is especially problematic for overweight children, for whom nonspecific
complaints and discomforts may lead to exercise avoidance (2, 4). The high
incidence of EIB found in all these situations argues for investigating for its
presence in patients presenting with its symptoms.
It has been recognized that chronic asthma causes some children to avoid
exercise and is sometimes associated with obesity (3,23). This is presumably due
to children with asthma developing uncomfortable symptoms such as dyspnea or
chest pain when attempting aerobic activities, and to some of them avoiding these
activities thereafter.
This study represents the first time that the association between bronchial
hyperreactivity after exercise in nonasthmatic children and obesity has been noted.
Our findings imply that EIB is more common than previously recognized, and
that its potential effects on enjoyment and performance of exercise is a predisposing factor toward a sedentary lifestyle contributing to the development or persistence of obesity. Obesity, by leading to a relative inefficiency in weight-bearing
activities such as running, and a relative hyperventilation during those activities,
could itself amplify any inherent bronchial reactivity. This might increase the
incidence of significant EIB and help perpetuate the obese state. Experimental
investigation of these hypotheses is lacking.
There are several limitations to this study. It is retrospective and examines
a nonrandom, unique, referral population. Although the tables presented make an
effort to sort out the various combinations of risk factors, this mixing of risk
factors handicaps an analysis of which factors are most prominent. The number
of patients with only one risk factor was too small for statistical analysis. The
exercise challenge and pulmonary testing procedures used in these patients are
highly sensitive for identifying bronchial reactivity. This makes our data difficult
to compare with studies in the literature (5, 10, 18, 22), which used only one to
five postexercise spirometry efforts, only looked at one pulmonary function
variable (such as PEF or FEV,), or did not monitor the exercise intensity of the
patients.

Exercise-Induced Bronchospasm

- 357

A nonobese nonatopic control group would have been ideal but was not
available in the population reviewed for this study. Instead of demonstrating a
significantly higher incidence of EIB in nonatopic obese versus nonatopic nonobese subjects, we were able in the present study to demonstrate no significant
difference between the incidence of EIB in atopic patients, expected to be high,
and nonatopic patients who were obese, whose rate of EIB would be expected to
be low.
Despite these drawbacks, several factors tend to validate the methods used.
The time course of postexercise response is consistent with the pattern for EIB
in prior studies (1, 6). The high incidences of EIB reported for most groups in
this study may seem unlikely. However, preliminary evidence from our work
with patients with cystic fibrosis (15), and with normal controls (16) using the
same procedures employed in this study, indicates that a much lower incidence
of positive exercise challenges will be found with the same methodology in lower
risk populations. The incidence of EIB in all groups with these methods is still
higher than that found for control populations using less sensitive procedures
(5, 22). Interestingly, Weiler et al. (24) found a 25-50% incidence of hyperresponsiveness to methacholine challenge in various groups of nonasthmatic
college athletes. Their work and our findings suggest that bronchial hyperreactivity may be much more common than would be expected if only sought in
people with known risk factors.
Methacholine challenge was not used to confirm any of the exercise challenge results. Kilvoog (17) has demonstrated a high correlation between exercise
and methacholine challenge in known asthmatics, with methacholine challenge
being a somewhat more sensitive procedure.
Our preliminary data comparing normal controls to nonasthmatic overweight children has indicated that there may be a relationship between the amount
of small airway bronchial reactivity, as measured by change in FEF,,,,, and
amount of obesity, as measured by triceps skinfold thickness (16). Probably due
to the heterogeneity of the population in the present study, a much lower and
nonsignificant correlation was found between these variables in this study.
The frequent association between EIB and obesity should increase the index
of suspicion for EIB in the "unfit" overweight child. While both poor physical
fitness and EIB can be mitigated by participation in an appropriate physical fitness
program (1,20), EIB alone can be rapidly treated by preexercise prophylaxis such
as medications, warm-up, or sprints, or it can be minimized by choice of activity
and avoiding cold, dry, or polluted air (I). Being self-limited and easily treated,
EIB, once diagnosed, can be dealt with to remove one impediment to using
exercise in the treatment of obesity (3). The data available do not clarify whether
the bronchial hyperreactivity found in these patients is a result of being overweight
or is due to other factors, or whether these patients were overweight in part
because of bronchial hyperreactivity since birth or acquired early in life. The
mechanisms of EIB in nonasthmatic children and the implications on physical
performance need further investigation.

References
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Authors' Note
Preliminary findings were presented at the Southern Society of Pediatric Research
meeting in New Orleans, January 3 1, 1991. Abstracts from this meeting are published in
Clinical Research, Vol. 38, No. 4, December 1990.

1992 NASPEM Meeting Site Changed

The 1992 meeting of the North American Society of Pediatric Exercise
Medicine, October 30 to November 1, 1992, will now be held at the
Miami Beach Ocean Resort. For more information, please contact
Giannina Yehle at 1-800-62 CHILD or Dr. Ted Kaplan at 3051547-3994.