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Competitive swimmers with allergic asthma show a mixed type of airway inflammation

¹ Dept of Immunology, Faculty of Medicine, University of Porto, ² Immuno-allergology, Hospital of São João, and ⁴ FC Porto Swimming Section, Porto, Portugal. ³ Skin and Allergy Hospital, Helsinki University Central Hospital, Helsinki, Finland.

To the Editors:

Elite swimmers are at increased risk of asthma 1. This has been attributed to airway inflammation and increased airway responsiveness induced by high-intensity long-term exercise and repeated exposure to the chlorine-rich atmosphere in swimming pools during training and competition 2, 3. Recently, increased levels of leukotriene (LT)B₄ in exhaled breath condensate and normal exhaled nitric oxide fraction (F_eNO) levels have been reported in five elite swimmers, suggesting possible underlying neutrophilic airway inflammation 4. Previous analysis of induced sputum in nonasthmatic elite swimmers showed increased proportion of eosinophils and neutrophils compared with healthy controls 3.

We aimed to characterise the airway inflammation in competitive asthmatic swimmers. Athletes from the FC Porto main swimming team and 20 nonathlete asthmatics were recruited; participants gave informed consent. Subjects were classified by their asthma and training status as asthmatic swimmers (n = 6, two female, aged 17±2 yrs, competing 8±3 yrs, training 16±4 h·week^–1), asthmatics (n = 20, eight female, aged 14±3 yrs) and swimmers (n = 20, six female, aged 17±2 yrs, competing 8±3 yrs, training 17±3 h·week^–1).

All asthmatics and nine (45%) of the swimmers were atopic according to skin-prick test results. None smoked. During two visits to the clinic, 1 week apart, subjects’ sputum cell counts, F_eNO, lung volumes and airway responsiveness to methacholine (provocative dose causing a 20% fall in forced expiratory volume in one second (FEV₁); PD₂₀) were determined. Sputum cell counts were further compared with reference values from a group of healthy schoolchildren (n = 15, five female, aged 9±2 yrs, 40% atopic) 5.

Sputum was examined as described previously 3. Briefly, after induction using an inhalation of hypertonic saline, sputum was selected and treated with dithiothreitol (Sputolysin®; Calbiochem Corporation, San Diego, CA, USA). The suspension was centrifuged and the cell pellet was resuspended. Cytospins were prepared and stained using May-Grünwald/Giemsa. Differential cell counts were made by counting a minimum of 500 nonsquamous cells. F_eNO was measured by chemiluminescence (NIOX; Aerocrine, Stockholm, Sweden) and PD₂₀ methacholine was determined using the dosimeter method, according to recommendations 6, 7. ANOVA was used to detect differences between groups. Due to the skewed distribution, eosinophil counts and PD₂₀ methacholine comparisons were made after logarithmic transformation. In order to permit analysis in the log scale, a constant (0.01) was added to each value to eliminate 0 values. A p-value <0.05 was considered to be stastically significant.

Induced sputum samples of asthmatic swimmers showed increased numbers of eosinophils and neutrophils compared with both healthy subjects and asthmatic patients respectively, and lymphocytes compared with healthy subjects, although the numbers were approximately the same as in swimmers or asthmatic patients. Asthmatic swimmers had a similar magnitude of F_eNO but significantly more pronounced airway responsiveness than asthmatics (fig. 1).

View larger version (15K): [in this window] [in a new window]   Fig. 1— Per cent sputum a) eosinophils, c) neutrophils and e) lymphocytes and b) exhaled nitric oxide (FeNO) ppb, d) airway responsiveness provocative dose of methacholine causing a 20% fall in forced expiratory volume in one second (PD20 methacholine) and f) lung function (% predicted forced expiratory volume in one second (FEV1)) in competitive asthmatic swimmers (study subjects) compared with asthmatic subjects, competitive swimmers and healthy subjects (controls). Boxes represent mean and whiskers represent confidence intervals. #: p = 0.015; +: p = 0.002; ¶: p = 0.005; : p = 0.001; *: p<0.05; ***: p<0.001.

Two factors could contribute to the neutrophilic airway inflammation in asthmatic competitive swimmers. First, endurance exercise associated hyperventilation and the inhalation of hypotonic aerosolised droplets from the pool surface during training may cause epithelial damage 1 and subsequent inflammation. Secondly, chronic low-grade exposure to chlorine derivatives may be related to the observed increased levels of exhaled LTB₄ in elite swimmers 4. This observation is also supported by the findings in children accidentally exposed to chlorine, with development of respiratory symptoms, lung function impairment and exhaled breath alterations, represented mainly by an increase in LTs and a decrease in F_eNO 8. If this is the case, new therapeutic approaches that, in addition to inhaled corticosteroids, would target the 5-lipoxygenase pathway could have a role attenuating the neutrophilic airway inflammation in swimmers with asthma.

In conclusion, asthma in allergic competitive swimmers is characterised by mixed type of eosinophilic and neutrophilic inflammation, which increase normal exhaled nitric oxide fraction and cause airway hyperresponsiveness. Daily exposure to aerosolised water droplets and chlorine derivatives probably contribute to the neutrophilic inflammation, which might respond poorly to standard asthma medication.

Support statement

A. Moreira holds a Grant from the Finnish Centre for International Mobility and a Fellowship Award from the European Academy of Allergy and Clinical Immunology.

Statement of interest

A statement of interest for this manuscript can be found at www.erj.ersjournals.com/misc/statements.shtml

ACKNOWLEDGEMENTS

The present authors would like to thank all subjects for their participation and the technical and administrative staff of FC Porto Swimming Section for logistical help. They would also like to thank S. Simões (Dept of Immunology, Faculty of Medicine, University of Porto, Porto, Portugal) for help with data collection and J. Fonseca (Biostatistics and Medical Informatics, Faculty of Medicine, University of Porto and Immuno-allergology, Hospital of São João, Porto, Portugal) for manuscript revision.

REFERENCES

1. Helenius I, Haahtela T. Allergy and asthma in elite summer sport athletes. J Allergy Clin Immunol 2000;106:444–452.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
2. Helenius IJ, Tikkanen HO, Sarna S, Haahtela T. Asthma and increased bronchial responsiveness in elite athletes: atopy and sport event as risk factors. J Allergy Clin Immunol 1998;101:646–652.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
3. Helenius IJ, Rytilä P, Metso T, Haahtela T, Venge P, Tikkanen HO. Respiratory symptoms, bronchial responsiveness, and cellular characteristics of induced sputum in elite swimmers. Allergy 1998;53:346–352.[Web of Science][Medline] [Order article via Infotrieve]
4. Piacentini GL, Rigotti E, Bodini A, Peroni D, Boner AL. Airway inflammation in elite swimmers. J Allergy Clin Immunol 2007;119:1559–1560.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
5. Rytilä P, Pelkonen AS, Metso T, Nikander K, Haahtela T, Turpeinen M. Induced sputum in children with newly diagnosed mild asthma: the effect of 6 months of treatment with budesonide or disodium cromoglycate. Allergy 2004;59:839–844.[CrossRef][Web of Science][Medline] [Order article via Infotrieve]
6. American Thoracic Society, European Respiratory Society. ATS/ERS recommendations for standardized procedures for the online and offline measurement of exhaled lower respiratory nitric oxide and nasal nitric oxide, 2005. Am J Respir Crit Care Med 2005;171:912–930.[Free Full Text]
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8. Bonetto G, Corradi M, Carraro S, et al. Longitudinal monitoring of lung injury in children after acute chlorine exposure in a swimming pool. Am J Respir Crit Care Med 2006;174:545–549.[Abstract/Free Full Text]

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