Asthma, Airway Inflammation and Epithelial Damage in Swimmers and Cold-Air Athletes
Open accessAbstract
Endurance athletes show an increased prevalence of airway hyperresponsiveness. The aim of the present study was to evaluate the long-term effects of training on airway responsiveness, inflammation and epithelial damage in swimmers and cold-air athletes. In total, 64 elite athletes (32 swimmers and 32 cold-air athletes), 32 mild asthmatic subjects and 32 healthy controls underwent allergy skin prick testing, methacholine challenge and induced sputum analysis. Overall, 69% of swimmers and 28% of cold-air athletes had airway hyperresponsiveness. Sputum neutrophil count correlated with the number of training hours per week in both swimmers and cold-air athletes. Eosinophil counts were higher in swimmers than in healthy subjects, although they were lower than in asthmatic subjects, and correlated with airway hyperresponsiveness in swimmers only. The eosinophil count in cold-air athletes was similar to that in healthy subjects. Bronchial epithelial cell count was not correlated with airway hyperresponsiveness but was significantly increased in swimmers, compared with healthy and asthmatic controls. In conclusion, the present authors observed significant airway inflammation only in competitive athletes with airway hyperresponsiveness. However, the majority of elite athletes showed evidence of bronchial epithelial damage that could possibly contribute to the development of airway hyperresponsiveness.
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In the lung, exposure to chlorination stressors has long been associated with a role in chronic inflammatory diseases of the respiratory system.
“In the lung, exposure to chlorination stressors has long been associated with a role in chronic inflammatory diseases of the respiratory system (137, 144–148).”
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Gomà, A., de Lluis, R., Roca-Ferrer, J., Lafuente, J., & Picado, C. (2017) · Environmental Research · doi:10.1016/j.envres.2016.10.030 · Cited by 23 · see citing works
Zhang, M., Deng, Y.-L., Liu, C., Lu, W., & Zeng, Q. (2023) · Chemosphere · doi:10.1016/j.chemosphere.2023.138808 · Cited by 23 · see citing works
Asthma Phenotypes and Endotypes: Implications for Personalised Therapy
Dean, K., & Niven, R. M. (2017) · BioDrugs · doi:10.1007/s40259-017-0242-5 · Cited by 22 · see citing works
Asthma prevalence in German Olympic athletes: A comparison of winter and summer sport disciplines
Selge, C., Thomas, S., Nowak, D., Radon, K., & Wolfarth, B. (2016) · Respiratory Medicine · doi:10.1016/j.rmed.2016.07.008 · Cited by 21 · see citing works
High incidence rate of asthma among elite endurance athletes: a prospective 4-year survey
Irewall, T., Söderström, L., Lindberg, A., & Stenfors, N. (2020) · Journal of Asthma · doi:10.1080/02770903.2020.1728769 · Cited by 20 · see citing works
“In aquatic sports, chlorine compounds in swimming pools may lead to increased airway inflammation and epithelial damage due to oxidative stress (9,10).”
BackgroundGoossens, J., Jonckheere, A., Seys, S., Dilissen, E., Decaesteker, T., Goossens, C., Peers, K. H. E., Vanbelle, V., Stappers, J., Aertgeerts, S., et al. (2023) · Thorax · doi:10.1136/thorax-2022-219651 · Cited by 20 · see citing works
Exercise-induced bronchoconstriction in the 21st century.
Anderson, S. D. (2011) · PubMed · Cited by 20 · see citing works
Bougault, V., & Boulet, L. (2012) · Expert Review of Respiratory Medicine · doi:10.1586/ers.12.51 · Cited by 20 · see citing works
Self-citationRole of sputum biomarkers in the management of asthma
Seys, S. (2016) · Current Opinion in Pulmonary Medicine · doi:10.1097/mcp.0000000000000345 · Cited by 20 · see citing works
Tarlo, S. M., & Malo, J. (2013) · Annals of the American Thoracic Society · doi:10.1513/annalsats.201305-119st · Cited by 20 · see citing works
Viglino, D., Maignan, M., Michalon, A., Turk, J., Buse, S. K., Blancher, M., Aufderheide, T. P., Belle, L., Savary, D., Ageron, F., et al. (2017) · Resuscitation · doi:10.1016/j.resuscitation.2017.07.030 · Cited by 19 · see citing works
Irritant-Induced Asthma and Reactive Airways Dysfunction Syndrome (RADS)
Brooks, S. M. (2014) · Journal of Allergy & Therapy · doi:10.4172/2155-6121.1000174 · Cited by 18 · see citing works
Rufo, J. C., Paciência, I., Silva, D., Martins, C., Madureira, J., Fernandes, E. D. O., Padrão, P., Moreira, P. A. M., Delgado, L., & Moreira, A. M. (2018) · PLoS ONE · doi:10.1371/journal.pone.0193848 · Cited by 17 · see citing works
Covariation amongst pool management, trichloramine exposure and asthma for swimmers in Norway
Nitter, T. B., & Svendsen, K. (2020) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2020.138070 · Cited by 18 · see citing works
Bernhardsen, G. P., Stang, J. S., Halvorsen, T., & Stensrud, T. (2022) · European Journal of Sport Science · doi:10.1080/17461391.2022.2113144 · Cited by 17 · see citing works
“In addition, sputum neutrophil counts are shown to correlate with training hours in both swimmers and cold air athletes (Bougault et al., 2009).”
BackgroundFunction of the Airway Epithelium in Asthma
Hallstrand, T. S., Woodruff, P. G., Holgate, S. T., & Knight, D. A. (2012) · Journal of Allergy · doi:10.1155/2012/160586 · Cited by 17 · see citing works
“[159] M.”
BackgroundAQUA© as predictor of allergy in elite marathon runners
Teixeira, R. N., Mendes, F. A. R., Martins, M. A., Mickleborough, T. D., & Carvalho, C. R. F. (2014) · World Allergy Organization Journal · doi:10.1186/1939-4551-7-7 · Cited by 17 · see citing works
“For instance, there are many environmental conditions that are sport specific and can induce adverse effects on the respiratory system, such as pollen exposure in athletes who train outdoors, cold air in winter athletes [21,22], fine particles in ice rinks [23] and chlorine exposure in swimmers [24].”
Sperm morphology normalcy is inversely correlated to cycling kilometers in elite triathletes
Vaamonde, D., Silva‐Grigoletto, M. E. D., Manso, J. M. G., Cunha‐Filho, J. S., & Vaamonde-Lemos, R. (2009) · Redalyc (Universidad Autónoma del Estado de México) · Cited by 17 · see citing works
Price, O. J., & Hull, J. H. (2014) · Clinical Pulmonary Medicine · doi:10.1097/cpm.0000000000000030 · Cited by 17 · see citing works
Demange, V., Wild, P. P., Zmirou‐Navier, D., Tossa, P., Bohadana, A., Barbaud, A. M., & Paris, C. (2010) · BMC Pulmonary Medicine · doi:10.1186/1471-2466-10-37 · Cited by 16 · see citing works
“According to literature, eosinophil numbers in induced sputum is more often used than the same count in nasal lavage fluid and was not significantly associated with BHR in 32 healthy controls used in a comparative study of airway inflammation and epithelial damage in swimmers and cold-air athletes[29].”
Airways Disorders and the Swimming Pool
Bougault, V., & Boulet, L. (2013) · Immunology and Allergy Clinics of North America · doi:10.1016/j.iac.2013.02.008 · Cited by 16 · see citing works
Self-citationBronchial Nitric Oxide Flux and Alveolar Nitric Oxide Concentration After Exposure to Hyperoxia
Caspersen, C., Stensrud, T., & Thorsen, E. (2011) · Aviation Space and Environmental Medicine · doi:10.3357/asem.2995.2011 · Cited by 15 · see citing works
Effect of competitive swimming on airway inflammation: A 3‐yr longitudinal study
Couto, M., Andrade, P., Pereira, M., Araújo, J. R., Moreira, P. A. M., Delgado, L., & Moreira, A. M. (2014) · Pediatric Allergy and Immunology · doi:10.1111/pai.12172 · Cited by 15 · see citing works
Reproducibility of the bronchoconstrictive response to eucapnic voluntary hyperpnoea
Williams, N. C., Johnson, M. A., Hunter, K. A., & Sharpe, G. R. (2015) · Respiratory Medicine · doi:10.1016/j.rmed.2015.08.006 · Cited by 15 · see citing works
Airway dysfunction in elite swimmers: prevalence, impact, and challenges
Lomax, M. (2016) · Open Access Journal of Sports Medicine · doi:10.2147/oajsm.s88339 · Cited by 15 · see citing works
Asthma and exercise-induced respiratory symptoms in the athlete
Boulet, L., Turmel, J., & Côté, A. (2016) · Current Opinion in Pulmonary Medicine · doi:10.1097/mcp.0000000000000339 · Cited by 15 · see citing works
Self-citationEucapnic voluntary hyperpnoea and exercise-induced vocal cord dysfunction
Turmel, J., Gagnon, S., Bernier, M., & Boulet, L. (2015) · BMJ Open Sport & Exercise Medicine · doi:10.1136/bmjsem-2015-000065 · Cited by 14 · see citing works
Self-citationExercise and Sinonasal Disease
Steelant, B., Hox, V., Hellings, P. W., Bullens, D. M. A., & Seys, S. (2018) · Immunology and Allergy Clinics of North America · doi:10.1016/j.iac.2018.01.014 · Cited by 14 · see citing works
Systemic and airway oxidative stress in competitive swimmers
Škrgat, S., Marčun, R., Kern, I., Šilar, M., Šelb, J., Fležar, M., & Korošec, P. (2018) · Respiratory Medicine · doi:10.1016/j.rmed.2018.03.005 · Cited by 14 · see citing works
The Effect of Different Training Loads on the Lung Health of Competitive Youth Swimmers
Davies, R., Parent, É., Steinback, C. D., & Kennedy, M. D. (2018) · International journal of exercise science · doi:10.70252/wqbr8294 · Cited by 14 · see citing works
“Airway inflammation can be determined through induced sputum analysis (12), however an innovative and potentially less invasive technique is measuring Fractional Exhaled Nitric Oxide (FeNO), which may also be used as a surrogate for AHR (2).”
BackgroundExhaled nitric oxide indicates poorly athlete's asthma
Voutilainen, M., Malmberg, L. P., Vasankari, T. J., & Haahtela, T. (2013) · The Clinical Respiratory Journal · doi:10.1111/crj.12014 · Cited by 14 · see citing works
“A mixed type of eosinophilic and neutrophilic airway inflammation seems to affect elite athletes (10, 11, 28), with concomitant evidence of bronchial epithelial damage (29).”
BackgroundSpecial considerations for adolescent athletic and asthmatic patients
Wolfarth, B., & Wuestenfeld, J. C. (2013) · Open Access Journal of Sports Medicine · doi:10.2147/oajsm.s23438 · Cited by 13 · see citing works
“Mechanisms of exercised-induced bronchoconstriction The mild hyperventilation during exercise and the inhalation of cold, dry air are thought to be important triggers for EIB.(32) These findings are leading to the development of different etiological theories.”
InfluentialAsthma, airway inflammation and epithelial damage in elite athletes
Carlsen, K.-H. (2009) · European Respiratory Journal · doi:10.1183/09031936.00011909 · Cited by 13 · see citing works
Exercise in Cold Air and Hydrogen Peroxide Release in Exhaled Breath Condensate
Marek, E., Volke, J., Mückenhoff, K., Platen, P., & Marek, W. (2012) · Advances in experimental medicine and biology · doi:10.1007/978-94-007-4549-0_22 · Cited by 12 · see citing works
Couto, M., Santos, P., Silva, D., Delgado, L., & Moreira, A. M. (2015) · Pediatric Allergy and Immunology · doi:10.1111/pai.12426 · Cited by 12 · see citing works
“Bronchial epithelial cells are released in higher amounts into sputum (epithelial shedding) of cold air athletes and swimmers (28), a result also found in our study.”
BackgroundResultEffects of steroid therapy on inflammatory cell subtypes in asthma
Boulet, L. (2010) · Thorax · doi:10.1136/thx.2009.131391 · Cited by 12 · see citing works
Self-citationBoskabady, M., Esmaeilizadeh, M., & Boskabady, M. (2014) · Toxicology and industrial health · doi:10.1177/0748233712454465 · Cited by 12 · see citing works
“…hyperresponsiveness (Agabiti et al., 2001; Das and Blanc, 1993; Nemery, 1996; Pedersen et al., 2008; Zwick et al., 1990) Airway hyperresponsiveness, airway inflammation, and destruction of airway mucosa have also been reported in swimmers (Bougault et al., 2009a, 2009b; Helenius et al., 1998).”
BackgroundStang, J. S., Couto, M., Carlsen, K.-H., & Stensrud, T. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2014-094053 · Cited by 11 · see citing works
RetractedGraff, P., Fredrikson, M. G., Jönsson, P., & Flodin, U. (2011) · International Archives of Occupational and Environmental Health · doi:10.1007/s00420-011-0671-2 · Cited by 11 · see citing works
“Interestingly, outside working life, athletes such as swimmers who are exposed to chlorine and cross-country skiers inhaling cold air are observed as having an increased incidence for asthma (Bougault et al. 2009).”
BackgroundExercise and the Immune System
Gomes, E. C., & Florida-James, G. (2013) · Springer eBooks · doi:10.1007/978-3-7091-1890-0_6 · Cited by 2 · see citing works
Prevalence of Asthma among Norwegian Elite Athletes
Melsom, H. S., Randa, A., Hisdal, J., Stang, J. S., & Stensrud, T. (2022) · Translational Sports Medicine · doi:10.1155/2022/3887471 · Cited by 10 · see citing works
“Airway hyperresponsiveness was found in 69% of the swimmers and 28% of the cold air athletes [26].”
BackgroundBeyond bronchodilation: Illuminating the performance benefits of inhaled beta2‐agonists in sports
Hostrup, M., & Jessen, S. (2024) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.14567 · Cited by 10 · see citing works
Diagnosis of Exercise-induced Bronchoconstriction in Swimmers: Context Matters
Leahy, M. G., Peters, C. M., Geary, C. M., Koehle, M. S., McKenzie, D. C., Brotherhood, J. S., & Sheel, A. W. (2020) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000002335 · Cited by 11 · see citing works
Vollsæter, M., Stensrud, T., Maat, R. C., Halvorsen, T., Røksund, O. D., Sandnes, A., & Clemm, H. H. (2022) · Frontiers in Pediatrics · doi:10.3389/fped.2021.800073 · Cited by 10 · see citing works
“These findings are related to the time spent exercising in harsh conditions, and also to the timing of the testing, whether this is in close relation to a period of intensive training or competition (25).”
BackgroundSachs‐Olsen, C., Berntsen, S., Carlsen, K. L., Anderssen, S. A., Mowinckel, P., & Carlsen, K. (2012) · The Clinical Respiratory Journal · doi:10.1111/j.1752-699x.2012.00283.x · Cited by 10 · see citing works
“Presently, the most probable explanation for this phenomenon is bronchial epithelial damage with resulting airway inflammation (4), possibly combined with increased parasympathetic activity (5), inflicted by the increased ventilation because of regularly repeated intensive exercise (6).”
BackgroundThe Role of Airway Inflammation and Bronchial Hyperresponsiveness in Athlete’s Asthma
Stang, J. S., Sikkeland, L. I. B., Tufvesson, E., Holm, A. M., Stensrud, T., & Carlsen, K. (2017) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000001478 · Cited by 10 · see citing works
“Although swimmers and cold air endurance athletes do have increased BHR when compared with healthy nonathletes (6,7), there is no difference when comparing to asthmatic individuals (7).”
BackgroundResultInfluentialExhaled nitric oxide concentration upon acute exposure to moderate altitude
Caspersen, C., Stang, J. S., Thorsen, E., & Stensrud, T. (2012) · Scandinavian Journal of Medicine and Science in Sports · doi:10.1111/sms.12018 · Cited by 9 · see citing works
- Authors
- Bougault, V., Turmel, J., St-Laurent, J., Bertrand, M., & Boulet, L.-P.
- Affiliations
- Institut universitaire de cardiologie et de pneumologie de Québec (CA)
- Venue
- European Respiratory Journal
- Publisher
- European Respiratory Society (ERS)
- Published
- 2009-01-07
- Volume
- 33
- Issue
- 4
- Pages
- 740-746
- ISSN
- 0903-1936 (ISSN-L)
- 1399-3003
- OpenAlex
- W2158216179
- Cited by
- 170
- References
- 34
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 8 · 2023: 4 · 2022: 8 · 2021: 6 · 2020: 6 · 2019: 2 · 2018: 12 · 2017: 8 · 2016: 13 · 2015: 10 · 2014: 11 · 2013: 19 · 2012: 19
- FWCI
- 11.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- European Respiratory Journal (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Topics
- Health Sciences › Medicine › Physiology › Asthma and respiratory diseases
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Occupational exposure and asthma
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Respiratory and Cough-Related Research
- Keywords
- airway hyperresponsiveness, asthma, airway inflammation, swimmers, endurance athletes, training, sputum neutrophils, eosinophils, methacholine challenge, induced sputum, bronchial epithelial cells
- MeSH terms
- Adolescent, Adult, Analysis of Variance, Asthma, Bronchial Provocation Tests, Cold Temperature, Female, Humans, Inflammation, Male, Physical Fitness, Regression Analysis, Seasons, Skin Tests, Sports, Sputum, Swimming, Case-Control Studies, Bronchial Hyperreactivity
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