Respiratory Research | |
Association of serum Clara cell protein CC16 with respiratory infections and immune response to respiratory pathogens in elite athletes | |
Marek L Kowalski1  Hubert Krysztofiak2  Joanna S Makowska1  Sylwia Moskwa1  Marzanna Jarzębska1  Janusz Jurczyk2  Marcin Kurowski1  | |
[1] Department of Immunology, Rheumatology and Allergy, Medical University of Łódź, ul. Pomorska 251, bud. C-5, Łódź 92-213, Poland;National Centre for Sports Medicine (COMS), Warsaw, Poland | |
关键词: Allergy; Asthma; Exercise training; Club cell protein; Clara cell protein; Respiratory viruses; | |
Others : 790329 DOI : 10.1186/1465-9921-15-45 |
|
received in 2013-05-10, accepted in 2014-03-07, 发布年份 2014 | |
【 摘 要 】
Background
Respiratory epithelium integrity impairment caused by intensive exercise may lead to exercise-induced bronchoconstriction. Clara cell protein (CC16) has anti-inflammatory properties and its serum level reflects changes in epithelium integrity and airway inflammation. This study aimed to investigate serum CC16 in elite athletes and to seek associations of CC16 with asthma or allergy, respiratory tract infections (RTIs) and immune response to respiratory pathogens.
Methods
The study was performed in 203 Olympic athletes. Control groups comprised 53 healthy subjects and 49 mild allergic asthmatics. Serum levels of CC16 and IgG against respiratory viruses and Mycoplasma pneumoniae were assessed. Allergy questionnaire for athletes was used to determine symptoms and exercise pattern. Current versions of ARIA and GINA guidelines were used when diagnosing allergic rhinitis and asthma, respectively.
Results
Asthma was diagnosed in 13.3% athletes, of whom 55.6% had concomitant allergic rhinitis. Allergic rhinitis without asthma was diagnosed in 14.8% of athletes. Mean CC16 concentration was significantly lower in athletes versus healthy controls and mild asthmatics. Athletes reporting frequent RTIs had significantly lower serum CC16 and the risk of frequent RTIs was more than 2-fold higher in athletes with low serum CC16 (defined as equal to or less than 4.99 ng/ml). Athletes had significantly higher anti-adenovirus IgG than healthy controls while only non-atopic athletes had anti-parainfluenza virus IgG significantly lower than controls. In all athletes weak correlation of serum CC16 and anti-parainfluenza virus IgG was present (R = 0.20, p < 0.01). In atopic athletes a weak positive correlations of CC16 with IgG specific for respiratory syncytial virus (R = 0.29, p = 0.009), parainfluenza virus (R = 0.31, p = 0.01) and adenovirus (R = 0.27, p = 0.02) were seen as well.
Conclusions
Regular high-load exercise is associated with decrease in serum CC16 levels. Athletes with decreased CC16 are more susceptible to respiratory infections. Atopy may be an additional factor modifying susceptibility to infections in subjects performing regular high-load exercise.
【 授权许可】
2014 Kurowski et al.; licensee BioMed Central Ltd.
【 预 览 】
Files | Size | Format | View |
---|---|---|---|
20140704234127675.pdf | 438KB | download | |
Figure 3. | 71KB | Image | download |
Figure 2. | 43KB | Image | download |
Figure 1. | 41KB | Image | download |
【 图 表 】
Figure 1.
Figure 2.
Figure 3.
【 参考文献 】
- [1]Helenius I, Rytilä P, Metso P, Haahtela T, Venge P, Tikkanen H: Respiratory symptoms, bronchial responsiveness, and cellular characteristics of induced sputum in elite swimmers. Allergy 1998, 53:346-352.
- [2]Helenius I, Tikkanen H, 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.
- [3]Carlsen K: Sports in extreme conditions: the impact of exercise in cold temperatures on asthma and bronchial hyper-responsiveness in athletes. Br J Sports Med 2012, 46:796-799.
- [4]Carlsen K-H, Kowalski ML: Asthma, allergy, the athlete and the Olympics. Allergy 2008, 63:383-386.
- [5]Walsh N, Gleeson M, Shephard R, Gleeson M, Woods J, Bishop N, Fleshner M, Green C, Pedersen BK, Hoffman-Goetz L, Rogers CJ, Northoff H, Abbasi A, Simon P: Position statement. Part one: immune function and exercise. Exerc Immunol Rev 2011, 17:6-63.
- [6]Bougault V, Turmel J, St-Laurent J, Bertrand M, Boulet LP: Asthma, airway inflammation and epithelial damage in swimmers and cold-air athletes. Eur Respir J 2009, 33:740-746.
- [7]Font-Ribera L, Kogevinas M, Zock J, Gómez F, Barreiro E, Nieuwenhuijsen M, Fernandez P, Lourencetti C, Pérez-Olabarría M, Bustamante M, Marcos R, Grimalt JO, Villanueva CM: Short-term changes in respiratory biomarkers after swimming in a chlorinated pool. Environ Health Perspect 2010, 118:1538-1544.
- [8]Shorter J, Nelson D, McManus J, Zahniser M, Sama S, Milton D: Clinical study of multiple breath biomarkers of asthma and COPD (NO, CO(2), CO and N(2)O) by infrared laser spectroscopy. J Breath Res 2011, 5:037108. doi:10.1088/1752-7155/5/3/
- [9]Braido F, Bagnasco D, Scichilone N, Santus P, Solidoro P, Di Marco F, Corsico A, Canonica GW: Biomarkers in obstructive respiratory diseases: an update. Panminerva Med 2012, 54:119-127.
- [10]Broeckaert F, Bernard A: Clara cell secretory protein (CC16): characteristics and perspectives as lung peripheral biomarker. Clin Exp Allergy 2000, 30:469-475.
- [11]LaKind J, Holgate S, Ownby D, Mansur A, Helms P, Pyatt D, Hays SM: A critical review of the use of Clara cell secretory protein (CC16) as a biomarker of acute or chronic pulmonary effects. Biomarkers 2007, 12:445-467.
- [12]Bolger C, Tufvesson E, Sue-Chu M, Devereux G, Ayres J, Bjermer L, Kippelen P: Hyperpnea-induced bronchoconstriction and urinary CC16 levels in athletes. Med Sci Sports Exerc 2011, 43:1207-1213.
- [13]Romberg K, Bjermer L, Tufvesson E: Exercise but not mannitol provocation increases urinary Clara cell protein (CC16) in elite swimmers. Resp Med 2011, 105:31-36.
- [14]Carbonnelle S, Francaux M, Doyle I, Dumont X, de Burbure C, Morel G, Michel O, Bernard A: Changes in serum pneumoproteins caused by short-term exposures to nitrogen trichloride in indoor chlorinated swimming-pools. Biomarkers 2002, 7:464-478.
- [15]Benson M, Fransson M, Martinsson T, Naluai A, Uddman R, Cardell L: Inverse relation between nasal fluid Clara cell protein 16 levels and symptoms and signs of rhinitis in allergen-challenged patients with intermittent allergic rhinitis. Allergy 2007, 62:178-183.
- [16]Shijubo N, Itoh Y, Yamaguchi T, Sugaya F, Hirasawa M, Yamada T, Kawai T, Abe S: Serum levels of Clara cell 10-kDa protein are decreased in patients with asthma. Lung 1999, 177:45-52.
- [17]Wang S, Rosenberger C, Bao Y, Stark J, Harrod K: Clara cell secretory protein modulates lung inflammatory and immune responses to respiratory syncytial virus infection. J Immunol 2003, 171:1051-1060.
- [18]GINA Report, Global Strategy for Asthma Management and Prevention. 2011. Updated 2011. http://www.ginasthma.org/uploads/users/files/GINA_Report2011_May4.pdf webcite [accessed 23 June 2012]
- [19]Bousquet J, Schünemann H, Samolinski B, Demoly P, Baena-Cagnani C, Bachert C, Bonini S, Boulet LP, Bousquet PJ, Brozek JL, Canonica GW, Casale TB, Cruz AA, Fokkens WJ, Fonseca JA, van Wijk RG, Grouse L, Haahtela T, Khaltaev N, Kuna P, Lockey RF, Lodrup Carlsen KC, Mullol J, Naclerio R, O'Hehir RE, Ohta K, Palkonen S, Papadopoulos NG, Passalacqua G, Pawankar R: Allergic Rhinitis and its Impact on Asthma (ARIA): achievements in 10 years and future needs. J Allergy Clin Immunol 2012, 130:1049-1062.
- [20]Bonini M, Braido F, Baiardini I, Del Giacco S, Gramiccioni C, Manara M, Tagliapietra G, Scardigno A, Sargentini V, Brozzi M, Rasi G, Bonini S: AQUA: Allergy Questionnaire for Athletes. Development and validation. Med Sci Sports Exerc 2009, 41:1034-1041.
- [21]Miller M, Hankinson J, Brusasco V, Burgos F, Casaburi R, Coates A, Crapo R, Enright P, van der Grinten CP, Gustafsson P, Jensen R, Johnson DC, MacIntyre N, McKay R, Navajas D, Pedersen OF, Pellegrino R, Viegi G, Wanger J, ATS/ERS Task Force: Standardisation of spirometry. Eur Respir J 2005, 26:319-338.
- [22]Bernard A, Carbonnelle S, Dumont X, Nickmilder M: Infant swimming practice, pulmonary epiuthelium integrity, and the risk of allergic and respiratory diseases later in childhood. Pediatrics 2007, 119:1095-1103.
- [23]Lagerkvist B, Bernard A, Blomberg A, Bergstrom E, Forsberg B, Holmstrom K, Karp K, Lundstrom NG, Segerstedt B, Svensson M, Nordberg G: Pulmonary epithelial integrity in children: relationship to ambient ozone exposure and swimming pool attendance. Environ Health Perspect 2004, 112:1768-1771.
- [24]Carbonnelle S, Bernard A, Doyle I, Grutters J, Francaux M: Fractional exhaled NO and serum pneumoproteins after swimming in a chlorinated pool. Med Sci Sports Exerc 2008, 40:1472-1476.
- [25]Fernández-Luna Á, Gallardo L, Plaza-Carmona M, García-Unanue J, Sánchez-Sánchez J, Felipe J, Burillo P, Ara I: Respiratory function and changes in lung epithelium biomarkers after a short-training intervention in chlorinated vs. ozone indoor pools. PLoS One 2013, 8:e68447.
- [26]Braido F, Riccio A, Guerra L, Gamalero C, Zolezzi A, Tarantini F, De Giovanni B, Folli C, Descalzi D, Canonica GW: Clara cell 16 protein in COPD sputum: a marker of small airways damage? Resp Med 2007, 101:2119-2124.
- [27]Jacobs J, Fuertes E, Krop E, Spithoven J, Tromp P, Heederik D: Swimming pool attendance and respiratory symptoms and allergies among Dutch children. Occup Environ Med 2012, 69:823-830.
- [28]Broeckaert F, Clippe A, Knoops B, Hermans C, Bernard A: Clara Cell Secretory Protein (CC16): features as a peripheral lung biomarker. Ann N Y Acad Sci 2000, 923:68-77.
- [29]Sengler C, Heinzmann A, Jerkic S, Haider A, Sommerfeld C, Niggemann B, Lau S, Forster J, Schuster A, Kamin W, Bauer C, Laing I, LeSouef P, Wahn U, Deichmann K, Nickel R: Clara cell protein 16 (CC16) gene polymorphism influences the degree of airway responsiveness in asthmatic children. J Allergy Clin Immunol 2003, 111:515-519.