European Journal of Applied Physiology

, Volume 113, Issue 3, pp 703–711 | Cite as

Distinctive bronchial inflammation status in athletes: basophils, a new player

  • Beatriz Sastre
  • Mar Fernández-Nieto
  • María Jesús Rodríguez-Nieto
  • Erica Aguado
  • Joaquín Sastre
  • Victoria del Pozo
Original Article


The aim of the study was to establish bronchial inflammation status and to measure eicosanoids in sputum obtained from active elite athletes. A total of 68 subjects were enrolled. Twelve were non-athletes and non-asthmatic (NAtNAs), 21 non-athlete asthmatics (NAtAs), 11 athlete non-asthmatics (AtNAs), and 24 athletes with asthma (AtAs) with positive indirect or direct bronchial challenges. Induced sputum was used to measure cells and eicosanoids. Sputum differential cell counts in all the subject groups revealed eosinophilia with the exception of NAtNAs control subjects. Athletes with and without diagnosed asthma showed a significant increase in bronchial epithelial cells and lymphocytes present in their sputum. Also, flow cytometry revealed that a significantly higher number of basophils were present in sputum from athletes (without and with asthma) when compared with non-athletes (without and with asthma). Asthmatic athletes and non-athletes showed a higher increase in LTC4 levels and PGE2 metabolites in sputum when compared with healthy controls. The present study identifies basophils as a new player present in athletes bronchial inflammation defining athlete status and not necessarily associated with exercise-induced bronchoconstriction.


Asthma Cellular inflammation Basophils Epithelial cells Eicosanoid mediators 



This study was supported by Universidad Europea de Madrid (Cátedra Real Madrid) and CIBER de Enfermedades Respiratorias (CIBERES), an initiative of Carlos III Institute of Health. The authors recognize Oliver Shaw for his revision and editing in English and Ignacio Mahillo for statistical support.


  1. Aitken ML, Greene KE, Tonelli MR et al (2003) Analysis of sequential aliquots of hypertonic saline solution-induced sputum from clinically stable patients with cystic fibrosis. Chest 123:792–799PubMedCrossRefGoogle Scholar
  2. American Thoracic Society. Standards for the diagnosis and care of patients with chronic obstructive pulmonary disease (COPD) and asthma (1987) This official statement of the American Thoracic Society was adopted by the ATS Boards of Directors, November 1986. Am Rev Respir Dis 136:225–244Google Scholar
  3. Anderson SD, Daviskas E (2000) The mechanism of exercise-induced asthma is …. J Allergy Clin Immunol 106:453–459PubMedCrossRefGoogle Scholar
  4. Anderson SD, Argyros GJ, Magnussen H et al (2001) Provocation by eucapnic voluntary hyperpnoea to identify exercise induced bronchoconstriction. Br J Sports Med 35:344–347PubMedCrossRefGoogle Scholar
  5. Anderson SD, Brannan JD (2003) Methods for “indirect” challenge tests including exercise, eucapnic voluntary hyperpnea, and hypertonic aerosols. Clin Rev Allergy Immunol 24:27–54PubMedCrossRefGoogle Scholar
  6. Anderson SD, Kippelen P (2008) Airway injury as a mechanism for exercise-induced bronchoconstriction in elite athletes. J Allergy Clin Immunol 122:225–235PubMedCrossRefGoogle Scholar
  7. Anderson SD, Brannan JD (2011) Bronchial provocation testing: the future. Curr Opin Allergy Clin Immunol 11:46–52PubMedCrossRefGoogle Scholar
  8. Andregnette-Roscigno V, Fernández-Nieto M, García Del Potro M et al (2010) Methacholine is more sensitive than mannitol for evaluation of bronchial hyperresponsiveness in asthmatic children. J Allergy Clin Immunol 126:869–871PubMedCrossRefGoogle Scholar
  9. Bolger C, Tufvesson E, Anderson SD et al (2011) The effect of inspired air conditions on exercise-induced bronchoconstriction and urinary CC16 levels in athletes. J Appl Physiol 111:1059–1065PubMedCrossRefGoogle Scholar
  10. Boniface S, Koscher V, Mamessier E et al (2003) Assessment of T lymphocyte cytokine production in induced sputum from asthmatics: a flow cytometry study. Clin Exp Allergy 33:1238–1243PubMedCrossRefGoogle Scholar
  11. Bonsignore MR, Morici G, Vignola AM et al (2003) Increased airway inflammatory cells in endurance athletes: what do they mean? Clin Exp Allergy 33:14–21PubMedCrossRefGoogle Scholar
  12. Bougault V, Turmel J, St-Laurent J et al (2009) Asthma, airway inflammation and epithelial damage in swimmers and cold-air athletes. Eur Respir J 33:740–746PubMedCrossRefGoogle Scholar
  13. Bougault V, Turmel J, Boulet LP (2011) Airway hyperresponsiveness in elite swimmers: is it a transient phenomenon? J Allergy Clin Immunol 127:892–898PubMedCrossRefGoogle Scholar
  14. Carlsen KH, Kowalski ML (2008) Asthma, allergy, the athlete and the Olympics. Allergy 63:383–386PubMedCrossRefGoogle Scholar
  15. Carlsen KH, Anderson SD, Bjermer L et al (2008) European Respiratory Society; European Academy of Allergy and Clinical Immunology. Exercise-induced asthma, respiratory and allergic disorders in elite athletes: epidemiology, mechanisms and diagnosis: part I of the report from the Joint Task Force of the European Respiratory Society (ERS) and the European Academy of Allergy and Clinical Immunology (EAACI) in cooperation with GA2LEN. Allergy 63:387–403PubMedCrossRefGoogle Scholar
  16. Denzel A, Maus UA, Rodriguez Gomez M et al (2008) Basophils enhance immunological memory responses. Nat Immunol 9:733–742PubMedCrossRefGoogle Scholar
  17. Domínguez-Ortega J, León F, Martínez Alonso JC et al (2004) Fluorocytometric analysis of induced sputum cells in an asthmatic population. J Invest Allergol Clin Immunol 14:108–113Google Scholar
  18. Efthimiadis A, Spanevello A, Hamid Q et al (2002) Methods of sputum processing for cell counts, immunocytochemistry and in situ hybridisation. Eur Respir J 20:19s–23sCrossRefGoogle Scholar
  19. Fahy JV (2001) Remodeling of the airway epithelium in asthma. Am J Respir Crit Care Med 164:546–551Google Scholar
  20. Fernández-Nieto M, Sastre B, Sastre J et al (2009) Changes in sputum eicosanoids and inflammatory markers after inhalation challenges with occupational agents. Chest 136:1308–1315PubMedCrossRefGoogle Scholar
  21. Global strategy for asthma management and prevention (2002) Update from NHLB/WHO Workshop Report GINA, revised 2002, NIH Publication No. 02-3659Google Scholar
  22. Hallstrand TS, Moody MW, Wurfel MM et al (2005) Inflammatory basis of exercise induced bronchoconstriction. Am J Respir Crit Care Med 172:679–686PubMedCrossRefGoogle Scholar
  23. Hallstrand TS, Debley JS, Farin FM et al (2007) Role of MUC5AC in the pathogenesis of exercise-induced bronchoconstriction. J Allergy Clin Immunol 119:1092–1098PubMedCrossRefGoogle Scholar
  24. Hallstrand TS, Henderson WR Jr (2009) Role of leukotrienes in exercise-induced bronchoconstriction. Curr Allergy Asthma Rep 9:18–25PubMedCrossRefGoogle Scholar
  25. Helenius IJ, Tikkanen HO, Sarna S et al (1998) Asthma and increased bronchial responsiveness in elite athletes: atopy and sport event as risk factors. J Allergy Clin Immunol 101:646–652PubMedCrossRefGoogle Scholar
  26. Helenius I, Haahtela T (2000) Allergy and asthma in elite summer sport athletes. J Allergy Clin Immunol 106:444–452PubMedCrossRefGoogle Scholar
  27. Hening NR, Aitken ML, Liu MC et al (2000) Effect of recombinant human platelet-activating factor-acetylhydrolase on allergen-induced asthmatic responses. Am J Respir Crit care Med 162:523–527Google Scholar
  28. Kanazawa H, Asai K, Hirata K et al (2002) Vascular involvement in exercise-induced airway narrowing in patients with bronchial asthma. Chest 122:166–170PubMedCrossRefGoogle Scholar
  29. Karasuyama H, Mukai K, Tsujimura Y et al (2009) Newly discovered roles for basophils: a neglected minority gains new respect. Nat Rev Immunol 9:9–13PubMedCrossRefGoogle Scholar
  30. Lumme A, Haahtela T, Öunap J et al (2003) Airway inflammation, bronchial hyperresponsiveness and asthma in elite ice hockey players. Eur Respir J 22:113–117PubMedCrossRefGoogle Scholar
  31. Lund TK, Pedersen L, Anderson SD (2009) Are asthma-like symptoms in elite athletes associated with classical features of asthma? Br J Sports Med 43:1131–1135PubMedCrossRefGoogle Scholar
  32. McFadden ER Jr (1990) Hypothesis: exercise-induced asthma as a vascular phenomenon. Lancet 335:880–883PubMedCrossRefGoogle Scholar
  33. MacFarlane AJ, Dworski R, Sheller JR et al (2000) Sputum cysteinyl leukotrienes increase 24 hours after allergen inhalation in atopic asthmatics. Am J Respir Crit Care Med 161:1553–1558PubMedGoogle Scholar
  34. Morici G, Bonsignore MR, Zangla D et al (2004) Airway cell composition at rest and after an all-out test in competitive rowers. Med Sci Sports Exerc 36:1723–1729PubMedCrossRefGoogle Scholar
  35. Pavord ID, Ward R, Woltmann G et al (1999) Induced sputum eicosanoid concentrations in asthma. Am J Respir Crit Care Med 160:1905–1909PubMedGoogle Scholar
  36. Pin I, Gibson PG, Kolendowicz R et al (1992) Use of induced sputum cell counts to investigate airway inflammation in asthma. Thorax 47:25–29PubMedCrossRefGoogle Scholar
  37. Pizzichini E, Pizzichini MM, Efthimiadis A et al (1996) Indices of airway inflammation in induced sputum: reproducibility and validity of cell and fluid-phase measurements. Am J Respir Crit Care Med 154:308–317PubMedGoogle Scholar
  38. Sacha JJ, Quinn JM (2011) The environment, the airway, and the athlete. Ann Allergy Asthma Immunol 106:81–88PubMedCrossRefGoogle Scholar
  39. Sastre B, Fernández-Nieto M, Mollá R et al (2008) Increased prostaglandin E2 levels in the airway of patients with eosinophilic bronchitis. Allergy 63:58–66PubMedCrossRefGoogle Scholar
  40. Sastre J, Fernandez-Nieto M, Novalbos A et al (2003) Need for monitoring nonspecific bronchial hyperresponsiveness before and after isocyanate inhalation challenge. Chest 123:1276–1279PubMedCrossRefGoogle Scholar
  41. Schroder JT (2011) Basophils: emerging roles in the pathogenesis of allergic disease. Immunol Rev 242:144–160CrossRefGoogle Scholar
  42. Sue-Chu M, Brannan JD, Anderson SD et al (2010) Airway hyperresponsiveness to methacholine, adenosine 5-monophosphate, mannitol, eucapnic voluntary hyperpnoea and field exercise challenge in elite cross-country skiers. Br J Sports Med 44:827–832PubMedCrossRefGoogle Scholar
  43. Thomas RA, Green RH, Brightling CE et al (2004) The influence of age on induced sputum differential cell counts in normal subjects. Chest 126:1811–1814PubMedCrossRefGoogle Scholar
  44. Verges S, Devouassoux G, Flore P et al (2005) Bronchial hyperresponsivness airway inflammation, and airway limitation in endurance athletes. Chest 127:1935–1941PubMedCrossRefGoogle Scholar
  45. Yoshikawa T, Shoji S, Fujii T et al (1998) Severity of exercise-induced bronchoconstriction is related to airway eosinophilic inflammation in patients with asthma. Eur Respir J 12:879–884PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • Beatriz Sastre
    • 1
    • 4
  • Mar Fernández-Nieto
    • 2
    • 4
  • María Jesús Rodríguez-Nieto
    • 3
    • 4
  • Erica Aguado
    • 2
    • 4
  • Joaquín Sastre
    • 2
    • 4
  • Victoria del Pozo
    • 1
    • 4
  1. 1.Immunology DepartmentIIS-Fundación Jiménez-DíazMadridSpain
  2. 2.Allergy DepartmentIIS-Fundación Jiménez-DíazMadridSpain
  3. 3.Pulmonology DepartmentIIS-Fundación Jiménez-DíazMadridSpain
  4. 4.CIBER de Enfermedades Respiratorias (CIBERES)MadridSpain

Personalised recommendations