Volume 123, Issue 2 , Pages 502-504, February 2009
The acute effect of swimming on airway inflammation in adolescent elite swimmers
Article Outline
To the Editor:
Elite athletes have been found to have airway inflammation, and endurance sport, in particular, has been suggested to cause inflammation. The number of studies on airway inflammation in elite athletes is limited. Most studies have focused on the long-term effect of elite sport, and only a few studies have examined the acute effect of exercise on airway inflammation. These few studies have mainly considered adult nonelite or elite athletes who have been involved in elite sport for many years and who already seem to have had significant inflammatory changes. It remains uncertain whether exercise increases existing airway inflammation or whether exercise can induce an acute inflammatory process in individuals without airway inflammation. In this study we aimed to evaluate the acute effect of a training session in an indoor swimming pool on airway inflammation in adolescent elite swimmers.
Participants were 21 adolescent elite swimmers (9 girls). The study was approved by the local ethics committee (journal no. KF 01 261528). All participants and their parents or guardians provided informed consent.
The study consisted of 2 visits. Visit 1 was performed at our department, where we performed sputum induction (baseline findings) and other tests as part of another study (skin prick tests to 10 aeroallergens, methacholine challenge, and the eucapnic voluntary hyperpnea test).1 At visit 2, the swimmers performed an early-morning training session of swimming at moderate intensity (approximately 45 minutes with an average heart rate of 162 beats/min) in the 8 indoor swimming pools normally used by the swimmers for training. The levels of free chlorine, combined chlorine, and pH were 0.60 to 1.04 mg/L, 0.18 to 0.35 mg/L, and 7.16 to 7.51, respectively. At visit 2, we performed sputum induction, fraction of exhaled nitric oxide (FeNO) measurement (NIOX MINO; Aerocrine, Stockholm, Sweden) at a flow of 50 mL/s, exhaled breath condensate (EBC) collection (RTube; Respiratory Research, Inc, Charlottesville, Va), and spirometry (EasyOne spirometer; Ndd Medical Technologies, Zurich, Switzerland). All tests at visit 2 were performed before the subjects entered the swimming pool area and were repeated 10 minutes after swimming, except for sputum induction, which was performed after swimming only. The pH measurements were done with a pH meter (Jenway pH meter 350; Dunmow, Essex, England) after deaeration with argon for 10 minutes. Sputum was induced and examined as described previously.1 Sputum samples were considered adequate if they contained less than 80% squamous cells. A blinded observer counted 400 nonsquamous cells.
Paired data were compared by using the paired t test or the Wilcoxon matched-pairs signed-rank test as appropriate. Differences in skewed data between the preswimming and postswimming measurements were assessed by using the Mann-Whitney test. P values of less than .05 were considered statistically significant.
Subject characteristics are shown in Table I. The swimmers had significantly higher baseline values of FEV1 and forced vital capacity than expected, and lung function values were unchanged after swimming (Table II). At baseline, 15 (71%) sputum samples met our criteria for being usable; 9 (43%) were usable after swimming, and only 5 sputum samples were usable at both visits. The sputum samples at baseline showed 37.3% neutrophils, 2.0% lymphocytes, and 0.5% eosinophils, and in the 9 sputum samples obtained after swimming, the corresponding numbers were 36.0%, 1.5%, and 0.0% (Table III). In a paired analysis there were no changes in differential cell counts in the 5 swimmers who managed to produce usable sputum samples at both visits. The median FeNO level was 12.0 ppb before swimming and increased insignificantly to 15.5 ppb after swimming (P = .07, Fig 1). We found no difference in preswimming and postswimming values of EBC pH (Table II), which has been suggested as a noninvasive marker of airway inflammation.
Table I. Subject characteristics
| Age (y) | 14.5 (1.0) |
| Physician-diagnosed asthma | 2 (10%) |
| Weekly exercise, recreational (h) | 3.9 (1.3) |
| Weekly training, elite (h) | 20.5 (5.6) |
| Duration of swimming in total (y) | 9.1 (2.9) |
| Duration of competitive swimming (y) | 2.6 (1.4) |
| Airway hyperresponsiveness | 6 (29%) |
| Atopy | 6 (29%) |
Table II. Lung function, FeNO, and EBC pH values
| Before swimming | After swimming | P value | |
|---|---|---|---|
| FEV1 (L) | 4.2 (3.1–5.4) | 4.3 (2.7–5.7) | NS |
| FEV1 (% predicted) | 115 (77–139) | 115 (62–144) | NS |
| FVC (L) | 4.8 (3.6–6.6) | 4.7 (3.2–7.8) | NS |
| FVC (% predicted) | 119 (77–139) | 120 (63–143) | NS |
| FEV1/FVC (% predicted) | 101 (84–110) | 101 (80–111) | NS |
| FeNO (ppb) | 12.0 (4–31) | 15.5 (5–47) | NS |
| EBC pH, deaerated | 8.05 (5.03–8.36) | 8.13 (6.82–8.51) | NS |
Table III. Induced sputum
| Before swimming | After swimming | P value | |
|---|---|---|---|
| Usable samples | 15 (71%) | 9 (43%) | NS |
| Squamous cells | 21.7 (0-79.0) | 14.9 (0-78.0) | NS |
| Eosinophils | 0.5 (0-3.0) | 0.0 (0-1.0) | NS |
| Lymphocytes | 2.0 (0-8.3) | 1.5 (0-5.0) | NS |
| Macrophages | 56.5 (10.6-96.8) | 49.0 (5.0-86.0) | NS |
| Neutrophils | 37.3 (0-81.7) | 36.0 (7.0-92.0) | NS |
| Columnar epithelial cells | 4.0 (0-13.3) | 2.3 (1.0-50.0) | NS |
Fig 1.
FeNO values before and after swimming.
We found that a training session of approximately 45 minutes at moderate intensity in an indoor chlorinated pool did not influence cellular composition of sputum, FeNO, EBC pH, or lung function in adolescent elite swimmers. Our results disagree with findings in nonasthmatic amateur adult runners, in whom FeNO and differential cell counts of neutrophils and macrophages in sputum have been shown to increase after running a marathon.2 Conversely, our findings are partly in line with studies on elite rowers and swimmers.3, 4
Whereas older elite swimmers with years of intense training have certain signs of airway inflammation, predominantly with neutrophils,5 the adolescent elite swimmers in the present study showed at baseline that they have not yet had major inflammatory airway changes, as evaluated based on FeNO results and cellular composition in sputum, nor did they have acute changes in response to a swimming training session of moderate intensity.1 Interestingly, findings by Belda et al6 suggest that the neutrophilic inflammation observed in elite swimmers relates to the duration of training, as well as AHR, and Boulet et al7 found that sputum neutrophils increase in hyperresponsive swimmers after a 1-hour training session, whereas no significant difference was observed in normoresponsive swimmers. We speculate that primarily athletes with signs of airway inflammation at baseline have significant acute changes in cellular composition in response to a training session of an intensity and length as seen in our study. However, we cannot rule out that a longer or more intense training session would have caused airway changes. Furthermore, the low number of usable sputum samples both before and after swimming limits the conclusions about changes in sputum composition. One explanation why only 9 sputum samples were usable after swimming could be that much of these materials are either coughed up or swallowed during swimming.
Not only endurance sports per se but also factors related to endurance sport are believed to be able to induce airway inflammation. In swimming chlorinated compounds are suggested as factors that cause airway inflammation and asthma not only in elite swimmers but also in the general population frequenting swimming pools.8, 9 It has been suggested that the increasing exposure to chlorine in swimming pools could be an important factor in the increase of asthma in developed countries, and the risk of having asthma culminates when children regularly attend chlorinated indoor pools before age 6 to 7 years.10 In contrast to this hypothesis, Carraro et al11 found that children regularly attending indoor swimming pools have no signs of eosinophilic airway inflammation. Our study supports the finding by Carraro and coworkers. Even though the swimmers in our study had been involved in competitive swimming for only a few years, most had done recreational swimming since early childhood, and still they had no sign of airway inflammation.
In conclusion, we found that a swimming training session in an indoor chlorinated swimming pool did not induce airway changes in adolescent elite swimmers with no signs of prior airway inflammation. More studies are needed to determine exactly what kind and how much exercise is needed to cause airway inflammation. Furthermore, the exact effect of environmental factors, such as chlorine-containing products, on the airways requires more attention.
We thank all of the swimmers, their clubs, the Danish Swimming Federation, and the pool attendants.
References
- . Airway responsiveness and inflammation in adolescent elite swimmers. J Allergy Clin Immunol. 2008;122:322–327
- Airway inflammation in nonasthmatic amateur runners. Am J Physiol Lung Cell Mol Physiol. 2001;281:L668–L676
- Airway cells after swimming outdoors or in the sea in nonasthmatic athletes. Med Sci Sports Exerc. 2003;35:1146–1152
- Airway cell composition at rest and after an all-out test in competitive rowers. Med Sci Sports Exerc. 2004;36:1723–1729
- . Respiratory symptoms, bronchial responsiveness, and cellular characteristics of induced sputum in elite swimmers. Allergy. 1998;53:346–352
- Airway inflammation in the elite athlete and type of sport. Br J Sports Med. 2008;42:244–249
- . Lower airway inflammatory responses to high-intensity training in athletes. Clin Invest Med. 2005;28:15–22
- Asthma and the elite athlete: summary of the International Olympic Committee's consensus conference, Lausanne, Switzerland, January 22-24, 2008. J Allergy Clin Immunol. 2008;122:254–260
- . Airway injury as a mechanism for exercise-induced bronchoconstriction in elite athletes. J Allergy Clin Immunol. 2008;122:225–237
- . Chlorinated pool attendance, atopy, and the risk of asthma during childhood. Environ Health Perspect. 2006;114:1567–1573
- Swimming pool attendance and exhaled nitric oxide in children. J Allergy Clin Immunol. 2006;118:958–960
Supported by research grants from Team Denmark; Anti-Doping Denmark; the Health Insurance Foundation; and the Academy of Muscle Biology, Exercise and Health Research. Polar Electro Denmark ApS (Denmark) provided the Polar FS3 devices and Flaemnuova (Italy) provided the Easyneb II devices.
Disclosure of potential conflict of interest: L. Pedersen has received financial support from the Academy of Muscle Biology, Exercise and Health Research, Anti-Doping Denmark, Team Denmark, the Health Insurance Foundation (Sygekassernes Helsefond), and Merck Sharpe & Dome. T. K. Lund has received financial support from Anti-Doping Denmark, Team Denmark, the Research Foundation of Bispebjerg Hospital, the Beckett Foundation, and Pharmaxis Ltd. P. J. Barnes has received research grants from GlaxoSmithKline, AstraZeneca, and Novartis. V. Backer has received financial support from Pharmaxis Ltd and the Danish Lung Foundation. The rest of the authors have declared that they have no conflict of interest.
PII: S0091-6749(08)02317-8
doi:10.1016/j.jaci.2008.11.039
© 2009 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.
Volume 123, Issue 2 , Pages 502-504, February 2009
