ISMJ

International SportMedJournal

Original research article

A workload equation for a bicycle ergometer is not sufficient to elicit exercise-induced bronchoconstriction in athletes

^1*Associate Professor Ugur Dal, MD, ²Mr A Taner Erdogan MSc, ³Mr Ilter Helvaci

¹Department of Physiology, Medical Faculty of Mersin University, Mersin, Turkey

²School of Physical Education and Sports, Mersin University, Mersin, Turkey

³Department of Biostatistics, Medical Faculty of Mersin University, Mersin, Turkey

*Corresponding author. Address at the end of text.

Abstract

Background: Elite athletes often experience exercise-induced bronchoconstriction (EIB). However, this generally occurs during long-duration, repetitive, high-intensity exercise in dry air. Respiratory symptoms and laboratory tests are not adequate to predict and to diagnose EIB in athletes. Establishing the level of exercise intensity necessary to induce bronchoconstriction is important in both athletes and sedentary subjects. Research question: The study attempted to evaluate the heart rate responses of seventeen male athletes and eighteen male sedentary subjects by using a target workload equation for a bicycle ergometer. Type of study: An experimental study, using human subjects, was designed. Methods: Seventeen volunteer male elite athletes and eighteen male sedentary subjects participated in the study. Subjects performed an exercise challenge test on an electromagnetically braked bicycle ergometer. The equation used to establish the target workload was in watts = 53.76 x measured forced expiratory volume in 1 s (FEV₁) - 11.07. Results: 88.2% of the athletes and 72.2% of the sedentary subjects reported at least one symptom of EIB. The difference between the percentage of maximal heart rate achieved in four minutes by athletes (81.4%) and sedentary subjects (86.3%) was statistically significant, but 5 of 18 sedentary subjects could not reach the target workload by the fourth minute. Only 1 of the 18 sedentary subjects demonstrated decrements greater than 10% in FEV₁.  Conclusion: This study demonstrated that a bicycle ergometer exercise challenge test using a workload equation is not suitable for EIB assessment for elite athletes because they cannot attain desired work intensity. It can be concluded that this equation may lead to a misdiagnosed or underdiagnosed athletic population. Keywords: bronchoprovocation, EIB, exercise, heart rate, intensity

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*Associate Professor Ugur Dal, MD

Dr Dal is a medical doctor and an Associate Professor in the Department of Physiology, University of Mersin, Mersin, Turkey. He is a lecturer at this university. He graduated from the Medical Faculty of Uludag University, Turkey. He has specialised in physiology. His main research interests are exercise physiology, resting energy expenditure and gait physiology.

Mr A Taner Erdogan, MSc

Erdogan received his BSc degree from Middle East Technical University, Ankara, Turkey and he studied exercise physiology at the Center for Exercise and Applied Human Physiology, Exercise Physiology Laboratories, University of New Mexico, Albuquerque, New Mexico, USA. He received a MSc degree from the School of Physical Education and Sports, Mersin University. He also studies exercise physiology at that School of Medicine Department of Physiology, Mersin University. His primary research interest is gait and exercise energy expenditure.

Mr Ilter Helvaci

Mr Ilter Helvaci is a research assistant and is a member of the Biostatistics Department, Mersin University, Turkey. His research interest is "Over- and under-diagnosis in early detection programs". He provides statistical consultancy in scientific articles. He also evaluates the results of the committee examinations held in Faculty of Medicine.

Introduction

Intense and prolonged physical exercise induces stress to the respiratory system because of hyperventilation ¹ that triggers an accumulation of inflammatory cells and mediator release triggering exercise-induced bronchoconstriction (EIB) ^2-4. EIB is an acute, transient airway narrowing that occurs during and after exercise ^5-7. When a subject is atopic or asthmatic, the risk of EIB is greater ^{8, 9}.

EIB is prevalent in elite athletes ¹⁰, with prevalence rates ranging from 10% to 50%; 90% of athletes with asthma may have EIB ^{6, 11}. The wide range is due to the nature of the sports performed (e.g., high-ventilation or low-ventilation sports), differences in test protocols used for bronchoprovocation, and the environmental conditions where the tests are done ¹¹. The various EIB testing protocols often demand different exercise intensities, which influences the results of EIB tests. Exercise intensity is an important parameter that must be monitored during EIB testing; and heart rate recording is the cheapest way to track exercise intensity. What is regarded as the first study that looked at the relationship between exercise intensity and EIB testing is the one conducted by Carlsen et al. ¹² which stated that the exercise used to provoke EIB should be of a high intensity ^12,13.

EIB is observed in healthy individuals, including children, as well as military recruits and elite athletes ^14-16. Because of this variability tests used for bronchoprovocation need to be adjusted for the specific groups. Since the American Thoracic Society’s (ATS) Guidelines for methacholine and exercise challenge testing-1999 is the only official statement ¹⁷ that describes the exercise challenge test using a bicycle ergometer - the ATS’ workload equation is used in this study. There are only a few studies that emphasise the importance of exercise intensity to induce bronchoconstriction in both athletes and sedentary subjects ^{12, 18}. The aim of this present study was to evaluate the intensity of the EIB test and heart rate response in athletes and sedentary subjects by using a target workload equation for a bicycle ergometer and to evaluate the relationship between EIB symptoms and EIB test results.

Materials and methods

Subjects

Seventeen male athletes and eighteen male sedentary subjects were recruited for the study. A local ethics committee approved the study. All participants gave written informed consent and filled out a questionnaire on their sex, age, asthmatic symptoms (shortness of breath, wheezing, excessive mucus formation, coughing) and use of any medication. The questionnaire was adopted from the European Community respiratory health survey and some exercise-specific questions were added ^{19, 20}. The subjects visited the laboratory on two different days. On the first day, a physical examination and skin prick test were performed, while on the second day, the EIB test was applied. The subjects refrained from coffee, tea, cigarettes, chocolate and exercise on the EIB test day. Three subjects (two athletes and one of the sedentary sujects) were withdrawn from the study because of respiratory infections in the preceding 6 weeks and recent infections. All EIB tests were performed between 14h00 and 16h00 by the same investigator.

Procedures

The study consisted of an exercise challenge as described in ATS’ guidelines for methacholine and exercise challenge testing ¹⁷. Standard spirometry evaluations were performed using a spirometer (Vmax Spectra 29C, Sensormedics, Yorba Linda, CA) prior to and immediately following, exercise. The spirometer was calibrated according to the manufacturer’s protocol using a 3L syringe before the EIB test every day. In addition, humidity and temperature were recorded.

Spirometry was done in accordance with The American Thoracic Society’s and European Respiratory Society’s (ERS) recommendations ²¹. Before each exercise challenge, baseline spirometry was performed. The best forced expiratory volume in 1 second (FEV₁) obtained from three trials was used for analysis and to determine the target workload. The exercise tests were performed in an air-conditioned room. An electromagnetically braked bicycle ergometer was used for the exercise challenge (Ergoline 800 Sensor Medics, Germany) and the subjects were not allowed to warm-up prior to the test. A target workload (TWR) to achieve the target ventilation was determined from an equation given in the ATS’) Guidelines for methacholine and exercise challenge testing-1999. The equation used to establish the target workload (TWR) was in watts = (53.76 x measured FEV₁) - 11.07). The workload was set to 60% of the target in the first minute, 75% in the second minute, 90% in the third minute, and 100% in the fourth minute. All subjects wore wireless heart rate monitors (Polar Electro; Oy, Finland) to verify exercise intensity. Heart rate was recorded prior to exercise, and at the end of each part of the workload. A valid test required the target exercise intensity to be sustained for at least 4mins. The test was terminated when the subject exercised at the target workload for 6mins. However, the subjects had the option to terminate the test at any time. FEV₁ was chosen as the parameter for evaluating the response to the challenges. The FEV₁ was measured at 5min intervals, starting from 0 to 30min after exercise. The lowest FEV₁ of the post-exercise measurement was used to determine the maximum decrease in FEV₁ as a percentage of baseline value. A positive response to the exercise bronchoprovocation test was defined as a 10% fall in FEV₁.

Maximum heart rate per minute was calculated as 220 minus the age of the participants. The percentage of maximum heart rate achieved was calculated from the following equation to evaluate the work intensity: (recorded heart rate at every minute / 220 - age) x 100.

Skin prick test

A skin prick test was performed according to the EAACI recommendations ²² with the following allergens: house dust mite (Dermatophagoides pteronyssinus and Dermatophagoides, grass, alternaria, aspergillus mix, secale cereale, dog dander, cat dander, carpinus betulus, quercus robur, compositae). A positive test was defined as a weal of a minimum of 3mm in diameter to at least one of the allergens. The patient was considered to be atopic with at least one positive skin prick test.

Statistical analysis

Data were expressed as mean ± standard deviation (SD). Percentage values were also calculated for specific variables. For statistical comparisons, the level of significance was set as P< 0.05. Statistical analyses were done using the statistical software program SPSS 11.5 (SPSS Inc., Chicago, IL). To assess the normality of the parameters, a Shapiro Wilk test was used. For variables having normal distribution, a Student t-test was applied. A Mann Whitney U test was used for the variables that did not have normal distribution.

Results

As mentioned, seventeen volunteer male elite athletes and eighteen male medical school students selected as sedentary subjects participated in the study (Table 1). One of the sedentary subjects terminated the exercise in the fourth minute of the EIB test due to exhaustion and one exercise test was stopped in the 8^th min because the sedentary subject had vertigo that lasted 10 min, such that his post-exercise PFT tests could not be performed (these data are not included). Two sedentary subjects reported vertigo and nausea in the beginning of the exercise test that ended in a short time without any intervention.

Table 1: Demographic data of the groups

P>0.05

The mean baseline FEV₁ of athletes was significantly higher than sedentary subjects (P<0.05). The baseline FVC and FEV₁ were higher than predicted values in both groups. The mean and SD of baseline FVC was 109.2 ± 14.2 % of that predicted for the athletes and 104 ± 8.8 % of that predicted for the sedentary subjects (P>0.05). The difference between the mean baseline FEV₁ of the athletes (114.9 ± 12.7 % predicted) and sedentary subjects (103.3 ± 9.8 % predicted) were statistically significant (P<0.05).  Table 2 shows baseline lung function of subjects, environmental conditions, and other specific properties of the groups.

Table 2: Baseline lung functions of subjects, environmental conditions and specific properties of the groups

P<0.05

FEV₁ – forced expiratory volume in 1sec; FVC –forced vital capacity; PEF – peak expiratory flow

Three subjects were atopic (one athlete and two sedentary subjects) according to prick test results and they did not report any sign of EIB. Fifteen (88.2%) of the seventeen athletes reported at least one symptom. The most commonly reported respiratory symptom in athletes was a cough after exercise (64.7%). Thirteen (72.2%) of the eighteen sedentary subjects reported at least one symptom. The most commonly reported respiratory symptom in sedentary subjects was shortness of breath (33.3%). No statistically significant difference was found in the prevalence of reporting any respiratory symptom between athletes and sedentary subjects (P>0.05).

The EIB tests were analysed to determine the subjects’ heart rate in the fourth minute of the test and to evaluate the intensity of the exercise test (the mean heart rate for the exercise period after the 4^thmin). The difference between the percentage of maximal heart rate achieved in the fourth minute by athletes (81.4%, 161.8±10.0 bpm) and sedentary subjects (86.3 %,172.3±10.6 bpm) was statistically significant (P<0.05), but five (27.7%) of the eighteen sedentary subjects could not reach target workload calculated by using their FEV₁ in the fourth minute. Their workload decreased while they were riding to maintain the exercise test for at least 8 minutes ²³ ± the results of these tests are shown in Table 3. All athletes reached their target workload without any intervention.

Table 3: Exercise test results of subjects who could not reach target workload

FEV₁ – forced expiratory volume in 1sec; HR – heart rate

The average of the percentage of maximal heart rate achieved after the fourth minute of exercise (last 4-6 min) was 86.1% (171.1±8.1bpm) in the athletes and 88.5% (176.7±9.1bpm) in the sedentary subjects. The difference between the percentage of maximal heart rate achieved by athletes and sedentary subjects was not statistically significant (P>0.05) (see Figure 1).

* Percent maximum heart rate

** Significantly different between groups

Figure 1: The difference between the percent of maximal heart rate achieved by athletes and sedentary subjects respectively

The average of the percentage of maximal heart rate achieved from a complete exercise bout (8-10 min) was 80.8% (160.5 ± 8.2) in athletes and 83.9% (167.5 ± 8.8) in sedentary subjects. The difference between the percentage of maximal heart rate achieved by athletes and sedentary subjects was statistically significant (P<0.05) (see Figure 2).

Figure 2: Heart rate achieved during exercise test

The mean target workloads calculated by ATS’ workload equation for a bicycle ergometer were 250.29 ± 29.7 watts for the athletes and 225.83 ± 26.7 watts for the sedentary subjects. For this equation, actual FEV₁ was used ¹¹. The difference between target workloads for the athletes and the sedentary subjects was statistically significant (P<0.05) because the athletes’ baseline FEV₁ values were higher than those of the sedentary subjects. Only one of the eighteen sedentary subjects demonstrated a decrease greater than 10% in FEV₁. The mean fall in FEV₁ for the athletes and sedentary subjects was -0.23 ± 3.9% and -3.22 ± 3.7%, respectively.

Discussion

This study on exercise-induced bronchoconstriction demonstrates that the workload equation for a bicycle ergometer may not be sufficient for athletes to attain desired exercise intensity.

Exercise is the true stimulus that produces the symptoms and signs of EIB and has a high positive predictive value for identifying asthma ²⁴. In the EIB test, three variables must be strictly controlled for test standardisation, namely, intensity of physical exercise, temperature, and the humidity of the inhaled air ^{23, 25}. In laboratory-based EIB testing, temperature and humidity can be controlled by means of an air-conditioner; thus the intensity of physical exercise becomes the most important parameter of EIB testing. However, in field tests these variables cannot be controlled, making it difficult to standardise the tests ^{11, 25}, as well as the diagnosis when evaluating the treatment of EIB. It is important to use the same exercise intensity and environmental conditions to induce the EIB ¹¹. The environmental conditions in this study were acceptable for the EIB test (temperature ~ 20^oC and humidity ~ 35-36%). These values were also compatible with ATS and ERS recommendations ^{17, 26}.

Heart rate and the minute ventilation (VE) can be used as variables to detect exercise intensity in EIB testing. VE versus heart rate relationship can be described as a bi-linear or tri-linear response according to the intensity of exercise below or above the lactate threshold ²⁷. Using the heart rate to check exercise intensity has advantages in that the test is more common, affordable, and easily performed with a portable spirometer and heart rate monitor in every exercise laboratory. By contrast, Pohjantähti et al. ²⁸ used a heart rate monitor to check exercise intensity rather than the ventilation rate because, they claimed, the ventilation rate could not be reliably recorded during field exercises.

During EIB testing, workload intensity and increasing periods of the load can be easily modified using a bicycle ergometer. Anderson and Brannan ²³ reported that the ATS’ target workload could increase VE equivalent to 17– 21 times the FEV_1. This low ventilation rate could provide the rationale behind the low EIB incidence in elite athletes during test described in this study. Recently, during EIB testing, tests that induce VE better than other challenge tests have been favoured, such as a bronchial provocation test with eucapnic voluntary hyperpnoea (EVH). EVH induces ventilation rates equivalent to, or higher than, most forms of exercise ²⁹. A target VE of 30 times the FEV₁ is recommended in the EVH challenge test ^{11, 23, 30}, but the EVH test requires more equipment. Argyros et al. ³⁰ reported that EIB tests that induced a VE of 30 times the FEV1 for 6 minutes resulted in a greater fall in FEV₁ than in the other tests that produced lower VE rates, illustrating the importance of comparing the results obtained in this study with those from the EVH test. As stated throughout the literature, when the minute ventilation rate increased, the fall in FEV₁ would be greater than in the EIB test that caused lower VE rates.

During EIB testing studies conducted to evaluate the exercise intensity by using a bicycle ergometer, these authors stated that target heart rate was adjusted to an 80-85% maximum heart rate ^{31, 32}. This work intensity was lower than the commonly preferred work intensity for EIB testing ^{11, 12, 24, 28}. It was interesting that although the ATS’ guidelines were published in 2000, no interpretation of the bicycle ergometer workload equation’s exercise intensity could be found. This present study is likely to be the first one to analyse the ATS’ workload equation for a bicycle ergometer in athletes and sedentary subjects.

It is important to monitor the heart rate when detecting workload intensity during EIB testing. Carlsen et al. ¹² performed a study that used two different exercise loads (85% and 95% of maximal heart rate) to examine the effect of workloads during EIB testing. At the 85% load, nine out of twenty children had falls greater than 10% in FEV₁ and at the 95% load, all children had a fall greater than 10% in FEV₁. This study indicated that strict standardisation of the exercise test was necessary when using the high-intensity protocol.

In these authors’ study, the achieved heart rate in the fourth minute was 81.4% of the predicted maximum in athletes and 86.3% of the predicted maximum in sedentary subjects. The average of the percentage of maximal heart rate achieved in the last four to six minutes of exercise was 86.1% in athletes and 88.5% in sedentary subjects. These data show that the target workload was low for athletes but reasonable for sedentary subjects. Anderson ²⁴ reported that exercise requires six to eight minutes of vigorous exercise at 85��% of maximal heart rate to elicit bronchoconstriction, while this range could be low for elite athletes in laboratory settings. Rundell and Slee ¹¹ recommended 95% of peak heart rate for an elite athlete population. The findings in this study confirmed that the workload intensity should be higher for elite athletes as mentioned in those previous studies. During the EIB testing study conducted by Pedersen et al. ¹³, swimmers reached an average of 99% of their predicted maximal heart rate and reported that if a higher exercise intensity was used the number of positive tests would have been greater. Thus if the intensity in this study’s protocol was increased, there may have been more positive EIB tests, but this study’s aim was to investigate the ATS protocol.

The diagnosis of EIB is important in targeting athletes who would benefit most from effective preventative measures¹⁰. This study’s findings suggest that the ATS’ workload equation for EIB testing using a bicycle ergometer may result in a misdiagnosis or underdiagnosis of EIB in athletes. Although fifteen (88.2%) of seventeen athletes and thirteen (72.2%) of eighteen sedentary subjects reported at least one respiratory symptom, only one sedentary subject’s EIB test was positive. Self-reported symptoms of EIB have created an important basis for diagnosis, but symptoms of EIB, or laboratory tests alone, are sufficient for the diagnosis of EIB ^{9, 33}. This study’s exercise protocol was not sufficiently intense to elicit EIB in athletes. A diagnosis of EIB cannot be eliminated by this EIB test’s results.

In this study, five (27.7%) of the sedentary subjects did not reach the target workload and their loads were reduced to maintain the exercise test for at least eight minutes. However, all the athletes in the study attained their target workload in the fourth minute. This intervention may explain the cause of reduced heart rate in the fourth minute and the remaining four minutes of the exercise test in the sedentary subjects. The sedentary subjects’ mean exercise time in this study was 1.33 h/week. Since sedentary subjects had a low weekly exercise time, beginning an EIB testing with a heavy load and without a warm-up period was difficult for them. A treadmill could be used for subjects who cannot reach the target workload using a bicycle.

A limitation in this study was that the target ventilation could not be evaluated by the spirometer because of technical problems (i.e. lack of equipment). A study that analyses both heart rate and target ventilation using a bicycle ergometer would be more convenient. These authors attempted to repeat the test using higher intensities but were unsuccessful because an additional test day would have interrupted the athletes’ training programme. The rationale behind using a bicycle ergometer for the EIB test was that it was the only ergometer equipment available in these authors’ laboratory.

Conclusion

The results from this study suggest that a laboratory-based exercise challenge test, using a workload equation for EIB testing using a bicycle ergometer, is not appropriate for the assessment of EIB in elite athletes because they cannot attain desired work intensity. This workload equation may lead to misdiagnosis or underdiagnosis of EIB in athletes.

Address for correspondence:

Associate Professor Ugur Dal, Department of Physiology, Medical Faculty of Mersin University, Mersin, Turkey

Tel.: +90 324 3412815-1026, Fax: +90 324 341 24 00

Email: drugurdal@gmail.com

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