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Original Research: Asthma |

Perception of Bronchoconstriction Following Methacholine and Eucapnic Voluntary Hyperpnea Challenges in Elite AthletesPerception of Bronchoconstriction in Athletes FREE TO VIEW

Simon Couillard, BSc; Valérie Bougault, PhD; Julie Turmel, PhD; Louis-Philippe Boulet, MD, FCCP
Author and Funding Information

From the Centre de Recherche de l’Institut universitaire de cardiologie et de pneumologie de Québec (Mr Couillard and Drs Turmel and Boulet), Québec City, QC, Canada; and Université du Droit et de la Santé (Dr Bougault), Faculté des Sciences du Sport et de l’Éducation physique, Ronchin, France.

Correspondence to: Louis-Philippe Boulet, MD, FCCP, Institut universitaire de cardiologie et de pneumologie de Québec, 2725 Chemin Sainte-Foy, Québec City, QC, G1V 4G5, Canada; e-mail: lpboulet@med.ulaval.ca


Funding/Support: This study was supported by local funds from Louis-Philippe Boulet.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;145(4):794-802. doi:10.1378/chest.13-1413
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Objective:  Self-reported respiratory symptoms are poor predictors of exercise-induced bronchoconstriction (EIB) in athletes. The objective of this study was to determine whether athletes have an inadequate perception of bronchoconstriction.

Methods:  One hundred thirty athletes and 32 nonathletes completed a standardized questionnaire and underwent eucapnic voluntary hyperpnea (EVH) and methacholine inhalation test. Perception scores were quoted on a modified Borg scale before each spirometry measurement for cough, breathlessness, chest tightness, and wheezing. Perception slope values were also obtained by plotting the variation of perception scores before and after the challenges against the fall in FEV1 expressed as a percentage of the initial value [(perception scores after − before)/FEV1].

Results:  Up to 76% of athletes and 68% of nonathletes had a perception score of ≤ 0.5 at 20% fall in FEV1 following methacholine. Athletes with EIB/airway hyperresponsiveness (AHR) had lower perception slopes to methacholine than nonathletes with asthma for breathlessness only (P = .02). Among athletes, those with EIB/AHR had a greater perception slope to EVH for breathlessness and wheezing (P = .02). Female athletes had a higher perception slope for breathlessness after EVH and cough after methacholine compared with men (P < .05). The age of athletes correlated significantly with the perception slope to EVH for each symptom (P < .05).

Conclusions:  Minimal differences in perception of bronchoconstriction-related symptoms between athletes and nonathletes were observed. Among athletes, the presence of EIB/AHR, older age, and female sex were associated with slightly higher perception scores.

Figures in this Article

The prevalence of airway hyperresponsiveness (AHR) to various stimuli has been shown to be high in endurance sports athletes.1 The use of self-reported symptoms to establish a diagnosis of exercise-induced bronchoconstriction (EIB), as assessed through questionnaires or reported to the physician, results in a high frequency of both false-positive and false-negative diagnoses in this population.2,3 Self-reported respiratory symptoms are not specific enough for the diagnosis of AHR or EIB in athletes.2 The reasons for this observation are still unclear, and whether athletes have an impaired perception of bronchoconstriction remains to be determined.

Perception of bronchoconstriction following bronchial provocation challenges has been studied in the general population and in subjects with asthma.410 It varies widely among individuals, and depending on the method used, 15% to 60% of adults with asthma can be defined as poor perceivers of bronchoconstriction.4,7,11 This point is important to consider because failure to perceive bronchoconstriction may lead to decreased therapeutic compliance12 and an increase in asthma morbidity and mortality.13,14

In the general population, the prevalence of asymptomatic AHR is < 15%.15 In elite athletes, we reported a significantly higher prevalence of asymptomatic AHR in swimmers (24%) than in winter sports athletes (7%).3 We suggested that swimmers may have a poor perception of bronchoconstriction, whereas winter sports athletes may have more symptoms triggered by cold air exposure, explaining their frequent complaints of exercise-induced cough.3 There are several possible explanations for the discrepancies in symptom perception in athletes. First, a protective effect of greater baseline lung function may be present in athletes, especially in swimmers who usually have supranormal FEV1,16 ranging from 111% to 170% predicted.1,3,17 Swimmers may not perceive a fall in FEV1 of 10% or 20% if they already have such high FEV1 values. Furthermore, the higher sputum eosinophil counts observed in the airways of swimmers with AHR and higher sputum neutrophil counts in athletes’ airways in general18 may also contribute to decreased respiratory symptom perception, as it has been observed in nonathlete subjects with asthma.9,19,20 The age of athletes may influence symptom perception because adolescent swimmers have a lower prevalence of AHR/EIB than young adult swimmers.3,21 Finally, sex may influence perception, thus, explaining the differences reported in asthma diagnosis and symptoms between women and men.22

The main aim of the present study was to determine whether competing athletes have a reduced perception of bronchoconstriction following bronchial provocation challenges. Possible discrepancies in respiratory symptom perception were, therefore, studied according to EIB/AHR status, sports performed, resting spirometric values, self-reported symptoms on questionnaire, age, and sex.

Subjects

Data on athletes from different sports disciplines and on nonathletes who visited our research center between 2007 and 2011 were analyzed. Subjects had to be aged 14 to 35 years, nonsmokers, and free of any disease that may have interfered with the study. Athletes had to be active competitors, training at least 10 h/wk. Nonathletes taking part in physical activities > 6 h per week or regularly exposed to a chlorinated environment were excluded. Subjects regularly using inhaled corticosteroids were also excluded. Written informed consent was obtained from all subjects or their legal guardian before inclusion in their respective study. Respective study protocols and analyses (1243, 20088, 20141, 20159, 20160, 201366, 20471) were approved by our institutional ethics committee (FWA00003485).

Design

This cross-sectional retrospective analysis was based on data from previous and ongoing prospective studies performed at our research center. The design of the tests has been previously described.3 Only data from the baseline visit of subjects were considered. Physical examination was conducted, and a questionnaire on current health status and training was administered. Eucapnic voluntary hyperpnea (EVH) and methacholine inhalation test (MIT) were performed consecutively after recovery of expiratory flows within 10% of baseline. Test protocols were the same for all included studies, except nonathlete subjects with asthma had no EVH at the initial visit.

Baseline Spirometry

Spirometry was performed according to American Thoracic Society specifications.23 Predicted values were defined according to Knudson et al.24

EVH Challenge

The EVH challenge was performed according to the method described by Anderson and Brannan.25 The target ventilation was 30 times the baseline FEV1. FEV1 and perception scores were measured before and at 3, 5, 10, 15, 20, 25, and 30 min after EVH. A subject with ≥ 10% fall in FEV1 at two consecutive time points was considered to have EIB.

Methacholine Inhalation Test

AHR to methacholine was measured using the 2-min tidal breathing method by Crapo et al.23 After measurements of FEV1 and FVC, subjects inhaled 0.9% saline followed by doubling concentrations of methacholine, ranging from 0.03 to 128 mg/mL, to obtain a 20% decrease in FEV1. The response was expressed as the provocative concentration of methacholine causing a 20% fall in FEV1 (PC20) obtained from the log dose-response curve. AHR was defined as a PC20 < 16 mg/mL.

Perception of Bronchoconstriction

Cough, breathlessness, chest tightness, and wheezing were scored on a modified Borg scale (0-10).5,26 Perception scores were recorded before each FEV1 maneuver. The perception score on the Borg scale at 20% fall in FEV1 (PS20) during MIT was determined for each subject by interpolation of the two last perception scores.11 Linear regressions and subsequent slope values were also obtained by plotting the variation of perception scores before and after the challenge against the fall in FEV1, expressed as a percentage of the initial value [(perception score after − perception score before)/FEV1 fall] as previously described by Burdon et al5 and others.8,9,20 Slopes were obtained for each symptom following EVH and MIT. For the purpose of this analysis, the higher of the two reproducible measurements at 3 min following EVH was used to calculate the maximal fall in FEV1 and to evaluate symptom perception [Borg slope = (perception score after EVH at 3 min − perception score before EVH)/percentage of FEV1 fall at 3 min]. For MIT, perception score before is the score following the saline inhalation, perception score after is the score at the last methacholine dose, and FEV1 fall is considered at the last methacholine dose.

Questionnaire

A questionnaire regarding respiratory condition was administered.27 Athletes were dichotomized as ever-reporters and never-reporters on the basis of written and oral reports of symptoms during exercise or exposure to common allergens and tobacco smoke.

Statistical Analysis

Data are expressed as mean ± SD or percentage, according to the distribution of variables, to summarize clinical characteristics of patients. χ2 or Fisher exact tests were performed to assess baseline differences in individual nominal variables among groups. One-way analysis of variance was performed for continuous variables with heterogeneous variances. Testing whether the model could be reduced to a one-way analysis with the same variance across groups was rejected for almost all parameters. The univariate normality assumptions were verified with the Shapiro-Wilk test. For some variables (hours of training per week, PC20, maximal fall in FEV1 at EVH), values were log-transformed to stabilize variances. Reported P values are based on these transformations.

Zero inflation (excess zeros) occurred in symptoms because a high number of Borg slopes were null values. Rather than analyzing zero-inflated data that either focus only on the non-zero data or model the presence-absence data and the non-zero data separately, a generalized additive model was applied using a mixture of probability distribution that describe the data to be analyzed. The mixture distribution was defined to incorporate adjustments for excess zeros and to improve the fit of the model. The statistical model specified was a mixture of exponential distributions. Under the zero-inflated data, the structural zeros are assumed to follow a Bernouilli distribution with parameter π, denoting the probability of a zero, and the random observations > 0 are assumed to follow a Gaussian distribution with probability (-1 π). Additionally, a Tobit model was also performed with similar results.

The Tukey technique was performed for posteriori multiple comparisons. Pearson coefficients were used in the assessment of correlations. Results were considered significant at P ≤ .05. Analyses were conducted with SAS, version 9.1.3 (SAS Institute Inc) statistical software.

Subject Characteristics

Data from swimmers (51 swimmers, 10 synchronized swimmers), winter athletes (30 cross-country skiers, 11 speed skaters training outdoors, nine biathletes), other endurance sports athletes (10 triathletes, seven cyclists, two canoe-kayakers), and 32 nonathletes (15 with asthma) were obtained. Sixty-six athletes were considered to be positive for EIB, AHR, or both (EIB/AHR) on the basis of at least one positive challenge; the remaining 64 were considered healthy (negative EVH and MIT results). Subject characteristics are shown in Tables 1 and 2.

Table Graphic Jump Location
Table 1 —Subject Characteristics

Data are presented as mean ± SD, No. (%), or geometric mean (range) unless otherwise indicated. AHR = airway hyperresponsiveness; EIB = exercise-induced bronchoconstriction; EVH = eucapnic voluntary hyperpnea; NA = nonavailable; PC20 = provocative concentration of methacholine causing a 20% fall in FEV1; PDA = physician-diagnosed asthma.

a 

P < .05 vs athletes with EIB/AHR.

b 

P < .05 vs nonathletes with asthma.

c 

P < .05 vs healthy nonathletes.

Table Graphic Jump Location
Table 2 —Athlete Characteristics

Data are presented as No. (%), mean ± SD, or geometric mean (range) unless otherwise indicated. See Table 1 legend for expansion of abbreviations.

a 

P < .05 vs winter athletes.

b 

P < .05 vs swimmers.

c 

P < .05 vs other endurance sports athletes.

EVH data from 77 athletes and seven nonathletes were considered adequate25 and were included for analysis. In most cases, exclusion of EVH data resulted from suboptimal ventilation rates, except for nonathletes with asthma who did not perform this test. MIT data from 129 athletes and 32 nonathletes were considered valid and included for analysis.

Perception of Bronchoconstriction
Comparison Between Athletes and Nonathletes:

The MIT PS20 distribution in athletes and nonathletes is presented in Figures 1A and 1B, respectively. Forty-two percent to 76% of athletes and 56% to 68% of nonathletes had a PS20 ≤ 0.5 at MIT PC20.

Figure Jump LinkFigure 1. A and B, Distribution of the PS20 scores of four symptoms in athletes (A) and nonathletes (B). The number of subjects having a PS20 between the fixed intervals was counted. PS20 = perception score on the Borg scale at 20% fall in FEV1.Grahic Jump Location

Athletes with EIB/AHR had lower perception slopes at MIT than nonathletes with asthma for breathlessness only (0.05 ± 0.04 vs 0.03 ± 0.05, P = .02) (Fig 2). No difference was observed between perception slopes of healthy athletes and healthy nonathletes either at MIT or at EVH (Fig 3).

Figure Jump LinkFigure 2. Comparison of Borg perception slopes following MIT between athletes and nonathletes. Bars represent mean ± SEM. *P < .05 vs athletes with EIB/AHR. #P < .05 vs healthy nonathletes. AHR = airway hyperresponsiveness; EIB = exercise-induced bronchoconstriction; MIT = methacholine inhalation test.Grahic Jump Location
Figure Jump LinkFigure 3. Comparison of Borg perception slopes following EVH between athletes and nonathletes. Bars represent mean ± SEM. *P < .05 vs athletes with EIB/AHR. EVH = eucapnic voluntary hyperpnea. See Figure 2 legend for expansion of other abbreviations.Grahic Jump Location
Comparison According to Responsiveness Status
Nonathletes—

After MIT, perception scores for wheezing (0.05 ± 0.05 vs 0 ± 0, P = .0005) and breathlessness (0.05 ± 0.04 vs 0.01 ± 0.03, P = .0068) were greater in nonathletes with asthma than in healthy nonathletes (Fig 2).

Athletes—

No significant difference was observed in perception slopes after MIT between healthy athletes and athletes with EIB/AHR (Fig 2). Perception slope values after EVH of athletes without asthma were lower than those of athletes with EIB/AHR for breathlessness (0.03 ± 0.12 vs 0.12 ± 0.29, P = .02) and wheezing (0.02 ± 0.13 vs 0.07 ± 0.31, P = .02) (Fig 3).

Comparison According to Sport:

After EVH, perception slope values for winter athletes were lower than those of other endurance sports athletes for breathlessness (0.03 ± 0.10 vs 0.22 ± 0.44, P = .02) and wheezing (0.01 ± 0.05 vs 0.24 ± 0.59, P = .02) (Fig 4). On MIT, swimmers had greater wheezing perception slope values than winter athletes (0.04 ± 0.07 vs 0.01 ± 0.02, P = .006) (Fig 5).

Figure Jump LinkFigure 4. Comparison of Borg perception slopes following EVH among different sports. Bars represent mean ± SEM. †P < .05 vs other endurance sports athletes. See Figure 3 legend for expansion of abbreviation.Grahic Jump Location
Figure Jump LinkFigure 5. Comparison of Borg perception slopes following MIT among different sports. Bars represent mean ± SEM. ‡P < .05 vs winter sports athletes. See Figure 2 legend for expansion of abbreviation.Grahic Jump Location
Comparison of Athletes Ever Reporting and Never Reporting Respiratory Symptoms:

After EVH only, never-reporters had lower perception slope values than ever-reporters for cough (0.01 ± 0.03 vs 0.20 ± 0.33, P = .005) and chest tightness (0.02 ± 0.07 vs 0.19 ± 0.35, P = .02).

The Role of Age:

After EVH, there were positive correlations between the age of athletes and slope values for cough (r = 0.25, P = .03), breathlessness (r = 0.36, P = .002), chest tightness (r = 0.27, P = .02), and wheezing (r = 0.36, P = .001).

The Role of Sex:

Perception slope values of female athletes (n = 65) were higher than those of male athletes (n = 65) for breathlessness after EVH (0.13 ± 0.30 vs 0.05 ± 0.16, P = .047) and cough after MIT (0.05 ± 0.06 vs 0.02 ± 0.09, P = .04).

The Role of Baseline Lung Function:

Correlations between baseline lung function (FEV1 and FVC % predicted) and perception slope values were performed according to the sport. Except for cough following MIT, which correlated positively with FEV1 (r = 0.28, P = .03) and FVC (r = 0.30, P = .02) values in swimmers, no significant correlation was observed between lung function and perception slopes.

Globally, the results show minimal differences in the perception of bronchoconstriction to MIT or EVH tests in athletes compared with nonathletes, suggesting that athletes’ symptom perception is not significantly altered. Among the few significant differences observed, the perception of breathlessness following MIT was lower in athletes with EIB/AHR than in nonathletes with asthma. Furthermore, in athletes, the EIB/AHR status and type of sport were associated with differences in breathlessness and wheezing perception after EVH. Of interest, the older the athletes were, the better they perceived symptoms after EVH. Additionally, female athletes had increased cough scores after MIT and breathlessness following EVH.

Differences in perception slopes between athletes and nonathletes were < 0.5 points on the modified Borg scale for a 1% fall in FEV1 from baseline, and many athletes reported no symptoms after MIT. To our surprise, a high percentage of athletes and nonathletes reported no respiratory symptoms at 20% fall in FEV1 after MIT. Forty-two percent to 76% of athletes and 56% to 68% of nonathletes had a perception score of ≤ 0.5 at MIT PC20. This finding is somewhat different from what we previously observed, at least for breathlessness, wherein we showed a normal distribution of the PS20 after saline inhalation.11 The low level of symptom perception in the nonathletes with asthma may be due to the fact that these subjects, typically, had very mild asthma of shorter time duration compared with previous reports. For a majority of subjects, a lack of education on interpretation of asthma symptoms is possible and may have led to the low symptom perception scores.

The present results show that an EIB/AHR status in athletes is associated with increased breathlessness and wheezing perception after EVH, but no difference was observed after MIT. This finding is important because the stimulus of these two tests is different. This could indicate that local airway inflammation induced by EVH, which acts through inflammatory cell mediator release, may play a role in symptom perception. Kippelen et al28 and Bolger et al29 showed that epithelial damage and airway inflammatory mediators released by mast cells occur after an EVH challenge in athletes with or without EIB. In the present study, it is possible that the slight increases in wheezing and breathlessness perceptions were due to transient inflammatory mediator release induced by EVH rather than predominant smooth muscle contraction as during MIT. We can also hypothesize that neurogenic inflammation, which is insufficiently studied in athletes, may play a role in the increased symptom perception following EVH. Finally, in patients with asthma, it has been suggested that airway inflammation, either eosinophilic or neutrophilic, and epithelial shedding may blunt the perception of dyspnea.9,19,20

Previous studies3,27 suggested that the perception of bronchoconstriction may be reduced in swimmers and increased in winter athletes. Indeed, swimming, running, or cycling in a hot and humid environment is bronchoprotective in children and adults with asthma.3032 In contrast, winter athletes train in an environment with very low absolute water content and temperature, which can provide greater stimuli for bronchoconstriction or cough.33,34 The present study suggests that winter sports athletes perceive slightly less breathlessness and wheezing than other endurance sports athletes following EVH. The winter athletes in the present study always trained outdoors and, thus, are exposed to cold air, whereas other endurance sports athletes and swimmers train in indoor facilities. Because winter athletes inhale cold dry air at high ventilatory rates during prolonged periods, a 6-min EVH may not stimulate their airways as strongly as an outdoor training session, which could possibly explain why they showed a lower perception of breathlessness and wheezing. Knowledge regarding the specific modulation of chronic cold air hyperpnea on the perception of bronchoconstriction is lacking.

In the present study, the age of athletes correlated with all symptom perception scores following EVH. Potts35 suggested that older and more experienced athletes may better recognize exercise-induced symptoms as abnormal. Inadequate symptom report in athletes may be due to conditioning of inhaled air as previously suggested and to a dissociation between physiologic and nociceptive perception, as previously hypothesized.27,36 Mental representation of asthma symptoms37 may overlap with perception of intense exertion in athletes and be integrated as a normal side effect due to, for example, a strong chemical odor in the pool environment.35 To avoid asthmatic stigma and doping concerns by fellow athletes, some athletes may be poorly motivated to complain of respiratory symptoms. Additionally, there is a lack of education in athletes and coaches regarding the recognition of exercise-induced respiratory symptoms, high EIB/AHR prevalence in the athlete population, and the effects of asthma medication, which could contribute to inadequate symptom perception, especially in young athletes.

Female athletes had higher cough scores after MIT and greater breathlessness scores following EVH than male athletes. It is difficult to explain physiologically such results, and it may be a fortuitous finding. However, other authors have observed that the cough reflex is more sensitive in women than in men.38,39 Fujimura et al38 showed that the enhanced cough sensitivity in women was not due to age, weight, height, or pulmonary function, but they found that premenopausal women had a higher cough threshold than postmenopausal women, suggesting that cough sensitivity in women may be attributable to hormonal factors. The positive correlation between baseline lung function and cough perception scores following MIT in swimmers is difficult to explain.

Finally, slopes of perception scores obtained with EVH may be less precise than scores obtained with MIT because the falls in expiratory flows obtained after EVH were lower than those observed with MIT. For the latter, we aimed to get a 20% fall in FEV1 while using high doses of methacholine, if needed within the normal range of airway responsiveness, to obtain a PC20.

One potential limitation of this study is that it was a retrospective analysis of existing data. It was initially conducted in a prospective cohort of subjects volunteering to take part in a research program on the prevalence of EIB/AHR in athletes. Nevertheless, in this database, respiratory symptoms were always recorded on a standardized scale and measured at the same time as the challenge-induced bronchoconstriction, and we believe that it is of scientific and clinical interest in this specific population.

In summary, this study is, to our knowledge, the first to investigate symptom perception following bronchial provocative challenges in competitive athletes. It shows only slight differences of perception of bronchoconstriction-related symptoms between athletes and nonathletes. The presence of EIB/AHR, female sex, and previous report of respiratory symptoms in questionnaires, however, were factors associated with higher perception scores for bronchoconstriction-induced symptoms in athletes.

Future research should evaluate athletes’ subjective awareness, understanding, and attitudes toward respiratory symptoms during training based on objective measurements of associated physiologic changes. Educational programs on the recognition of abnormal respiratory symptoms in athletes could help athletes to optimize their health and training. Peak expiratory flow measurements before and after exercise could help athletes with asthma to determine which symptoms are associated with a reduced airway caliber and, therefore, lead to a better interpretation of asthma symptoms.40

Author contributions: Dr Boulet had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Mr Couillard: contributed to the data collection, analysis, and interpretation and preparation of the manuscript.

Dr Bougault: contributed to the study conception, performance of tests, study coordination, and writing and review of the manuscript.

Dr Turmel: contributed to the study conception, performance of tests, and writing and review of the manuscript.

Dr Boulet: contributed to the development of the initial questions and protocol, medical examinations of all subjects, and review and approval of the manuscript.

Financial/nonfinancial disclosures: The authors have reported to CHEST the following conflicts of interest: Dr Boulet has served on advisory boards for GlaxoSmithKline plc and Novartis Corp and received honoraria for lectures from AstraZeneca, GlaxoSmithKline plc, Merck Sharp & Dohme Corp, and Novartis Corp; sponsorship for investigator-generated research from AstraZeneca, GlaxoSmithKline plc, Merck Canada Inc, and Schering AG; sponsorship for participation in multicenter studies from Altair Engineering, Inc; Amgen Inc; Asmacure Ltée; AstraZeneca; Boehringer Ingelheim GmbH; Genentech, Inc; GlaxoSmithKline plc; Novartis Corp; Ono Pharmaceutical Co, Ltd; Pharmaxis Ltd; Schering AG; and Wyeth Pharmaceuticals Inc; support for the production of educational materials from AstraZeneca, GlaxoSmithKline plc, Merck Canada Inc, Boehringer Ingelheim GmbH, and Novartis Corp; governmental funding as an adviser for the Quebec National Health Institute; organizational funding as chair of the Global Initiative for Asthma (GINA) Guidelines Dissemination and Implementation Committee; and funding as Laval University Chair on Knowledge Transfer, Prevention and Education in Respiratory and Cardiovascular Health. Mr Couillard and Drs Bougault and Turmel have reported that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Role of sponsors: The sponsor had no role in the design of the study, the collection and analysis of the data, or the preparation of the manuscript.

Other contributions: The authors thank Helene Turcotte, MSc, for technical assistance; Serge Simard, MSc, for statistical analyses; and Marie-Eve Boulay, MSc, and Philippe Prince, MSc, for review of the manuscript.

AHR

airway hyperresponsiveness

EIB

exercise-induced bronchoconstriction

EVH

eucapnic voluntary hyperpnea

MIT

methacholine inhalation test

PC20

provocative concentration of methacholine causing a 20% fall in FEV1

PS20

perception score on the Borg scale at 20% fall in FEV1

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Borg GAV. Psychophysical bases of perceived exertion. Med Sci Sports Exerc. 1982;14(5):377-381. [CrossRef]
 
Turcotte H, Langdeau JB, Thibault G, Boulet LP. Prevalence of respiratory symptoms in an athlete population. Respir Med. 2003;97(8):955-963. [CrossRef]
 
Kippelen P, Larsson J, Anderson SD, Brannan JD, Dahlén B, Dahlén SE. Effect of sodium cromoglycate on mast cell mediators during hyperpnea in athletes. Med Sci Sports Exerc. 2010;42(10):1853-1860. [CrossRef]
 
Bolger C, Tufvesson E, Sue-Chu M, et al. Hyperpnea-induced bronchoconstriction and urinary CC16 levels in athletes. Med Sci Sports Exerc. 2011;43(7):1207-1213. [CrossRef]
 
Inbar O, Dotan R, Dlin RA, Neuman I, Bar-Or O. Breathing dry or humid air and exercise-induced asthma during swimming. Eur J Appl Physiol Occup Physiol. 1980;44(1):43-50. [CrossRef]
 
Strauss RH, McFadden ER Jr, Ingram RH Jr, Deal EC Jr, Jaeger JJ. Influence of heat and humidity on the airway obstruction induced by exercise in asthma. J Clin Invest. 1978;61(2):433-440. [CrossRef]
 
Anderson SD, Silverman M, Walker SR. Metabolic and ventilatory changes in asthmatic patients during and after exercise. Thorax. 1972;27(6):718-725. [CrossRef]
 
Weiler JM, Ryan EJ III. Asthma in United States Olympic athletes who participated in the 1998 Olympic winter games. J Allergy Clin Immunol. 2000;106(2):267-271. [CrossRef]
 
Turmel J, Bougault V, Boulet LP. Seasonal variations of cough reflex sensitivity in elite athletes training in cold air environment. Cough. 2012;8(1):2-8. [CrossRef]
 
Potts JE. Adverse Respiratory Health Effects of Competitive Swimming: The Prevalence of Symptoms, Illness, and Bronchial Hyper-responsiveness to Methacholine and Exercise[dissertation]. Vancouver, BC, Canada: University of British Columbia; 1994.
 
Catellier P, Turcotte H, Deschesnes F, Boulet LP. Changes in lung volumes and poor perception of bronchoconstriction-induced respiratory symptoms. Ann Allergy Asthma Immunol. 1998;81(4):315-321. [CrossRef]
 
Janssens T, Verleden G, De Peuter S, Van Diest I, Van den Bergh O. Inaccurate perception of asthma symptoms: a cognitive-affective framework and implications for asthma treatment. Clin Psychol Rev. 2009;29(4):317-327. [CrossRef]
 
Fujimura M, Kasahara K, Kamio Y, Naruse M, Hashimoto T, Matsuda T. Female gender as a determinant of cough threshold to inhaled capsaicin. Eur Respir J. 1996;9(8):1624-1626. [CrossRef]
 
Dicpinigaitis PV, Rauf K. The influence of gender on cough reflex sensitivity. Chest. 1998;113(5):1319-1321. [CrossRef]
 
Feldman JM, Kutner H, Matte L, et al. Prediction of peak flow values followed by feedback improves perception of lung function and adherence to inhaled corticosteroids in children with asthma. Thorax. 2012;67(12):1040-1045. [CrossRef]
 

Figures

Figure Jump LinkFigure 1. A and B, Distribution of the PS20 scores of four symptoms in athletes (A) and nonathletes (B). The number of subjects having a PS20 between the fixed intervals was counted. PS20 = perception score on the Borg scale at 20% fall in FEV1.Grahic Jump Location
Figure Jump LinkFigure 2. Comparison of Borg perception slopes following MIT between athletes and nonathletes. Bars represent mean ± SEM. *P < .05 vs athletes with EIB/AHR. #P < .05 vs healthy nonathletes. AHR = airway hyperresponsiveness; EIB = exercise-induced bronchoconstriction; MIT = methacholine inhalation test.Grahic Jump Location
Figure Jump LinkFigure 3. Comparison of Borg perception slopes following EVH between athletes and nonathletes. Bars represent mean ± SEM. *P < .05 vs athletes with EIB/AHR. EVH = eucapnic voluntary hyperpnea. See Figure 2 legend for expansion of other abbreviations.Grahic Jump Location
Figure Jump LinkFigure 4. Comparison of Borg perception slopes following EVH among different sports. Bars represent mean ± SEM. †P < .05 vs other endurance sports athletes. See Figure 3 legend for expansion of abbreviation.Grahic Jump Location
Figure Jump LinkFigure 5. Comparison of Borg perception slopes following MIT among different sports. Bars represent mean ± SEM. ‡P < .05 vs winter sports athletes. See Figure 2 legend for expansion of abbreviation.Grahic Jump Location

Tables

Table Graphic Jump Location
Table 1 —Subject Characteristics

Data are presented as mean ± SD, No. (%), or geometric mean (range) unless otherwise indicated. AHR = airway hyperresponsiveness; EIB = exercise-induced bronchoconstriction; EVH = eucapnic voluntary hyperpnea; NA = nonavailable; PC20 = provocative concentration of methacholine causing a 20% fall in FEV1; PDA = physician-diagnosed asthma.

a 

P < .05 vs athletes with EIB/AHR.

b 

P < .05 vs nonathletes with asthma.

c 

P < .05 vs healthy nonathletes.

Table Graphic Jump Location
Table 2 —Athlete Characteristics

Data are presented as No. (%), mean ± SD, or geometric mean (range) unless otherwise indicated. See Table 1 legend for expansion of abbreviations.

a 

P < .05 vs winter athletes.

b 

P < .05 vs swimmers.

c 

P < .05 vs other endurance sports athletes.

References

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Anderson SD, Brannan JD. Methods for “indirect” challenge tests including exercise, eucapnic voluntary hyperpnea, and hypertonic aerosols. Clin Rev Allergy Immunol. 2003;24(1):27-54. [CrossRef]
 
Borg GAV. Psychophysical bases of perceived exertion. Med Sci Sports Exerc. 1982;14(5):377-381. [CrossRef]
 
Turcotte H, Langdeau JB, Thibault G, Boulet LP. Prevalence of respiratory symptoms in an athlete population. Respir Med. 2003;97(8):955-963. [CrossRef]
 
Kippelen P, Larsson J, Anderson SD, Brannan JD, Dahlén B, Dahlén SE. Effect of sodium cromoglycate on mast cell mediators during hyperpnea in athletes. Med Sci Sports Exerc. 2010;42(10):1853-1860. [CrossRef]
 
Bolger C, Tufvesson E, Sue-Chu M, et al. Hyperpnea-induced bronchoconstriction and urinary CC16 levels in athletes. Med Sci Sports Exerc. 2011;43(7):1207-1213. [CrossRef]
 
Inbar O, Dotan R, Dlin RA, Neuman I, Bar-Or O. Breathing dry or humid air and exercise-induced asthma during swimming. Eur J Appl Physiol Occup Physiol. 1980;44(1):43-50. [CrossRef]
 
Strauss RH, McFadden ER Jr, Ingram RH Jr, Deal EC Jr, Jaeger JJ. Influence of heat and humidity on the airway obstruction induced by exercise in asthma. J Clin Invest. 1978;61(2):433-440. [CrossRef]
 
Anderson SD, Silverman M, Walker SR. Metabolic and ventilatory changes in asthmatic patients during and after exercise. Thorax. 1972;27(6):718-725. [CrossRef]
 
Weiler JM, Ryan EJ III. Asthma in United States Olympic athletes who participated in the 1998 Olympic winter games. J Allergy Clin Immunol. 2000;106(2):267-271. [CrossRef]
 
Turmel J, Bougault V, Boulet LP. Seasonal variations of cough reflex sensitivity in elite athletes training in cold air environment. Cough. 2012;8(1):2-8. [CrossRef]
 
Potts JE. Adverse Respiratory Health Effects of Competitive Swimming: The Prevalence of Symptoms, Illness, and Bronchial Hyper-responsiveness to Methacholine and Exercise[dissertation]. Vancouver, BC, Canada: University of British Columbia; 1994.
 
Catellier P, Turcotte H, Deschesnes F, Boulet LP. Changes in lung volumes and poor perception of bronchoconstriction-induced respiratory symptoms. Ann Allergy Asthma Immunol. 1998;81(4):315-321. [CrossRef]
 
Janssens T, Verleden G, De Peuter S, Van Diest I, Van den Bergh O. Inaccurate perception of asthma symptoms: a cognitive-affective framework and implications for asthma treatment. Clin Psychol Rev. 2009;29(4):317-327. [CrossRef]
 
Fujimura M, Kasahara K, Kamio Y, Naruse M, Hashimoto T, Matsuda T. Female gender as a determinant of cough threshold to inhaled capsaicin. Eur Respir J. 1996;9(8):1624-1626. [CrossRef]
 
Dicpinigaitis PV, Rauf K. The influence of gender on cough reflex sensitivity. Chest. 1998;113(5):1319-1321. [CrossRef]
 
Feldman JM, Kutner H, Matte L, et al. Prediction of peak flow values followed by feedback improves perception of lung function and adherence to inhaled corticosteroids in children with asthma. Thorax. 2012;67(12):1040-1045. [CrossRef]
 
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