Airways Disorders and the Swimming Pool

Immunology and Allergy Clinics of North America

Volumn 33, Issue 3, 2013, Pages 395-408

  Bougault, Valérie ^a   Boulet, Louis Philippe ^b  

^a UNIV LILLE   (France)

^b LAVAL UNIVERSITY   (Canada)

Author keywords

Airways; Asthma; Chlorine; Exercise; Swimming

Indexed keywords

CHLORINE;

ASTHMA; BREATHING PATTERN; BRONCHOSPASM; CAUSAL ATTRIBUTION; CHLORINATION; DISEASE ASSOCIATION; DISINFECTION; ENVIRONMENTAL FACTOR; ENVIRONMENTAL TEMPERATURE; FORCED EXPIRATORY VOLUME; HUMAN; HUMIDITY; HYDROSTATIC PRESSURE; LUNG VENTILATION; PHYSICAL PERFORMANCE; PREVALENCE; PRIORITY JOURNAL; RESPIRATORY EPITHELIUM; RESPIRATORY TRACT ALLERGY; RESPIRATORY TRACT DISEASE; RESPIRATORY TRACT INFLAMMATION; RESPIRATORY TRACT INJURY; REVIEW; SWIMMING; SWIMMING POOL; WATER IMMERSION; WATER TREATMENT;

AIRWAYS; ASTHMA; CHLORINE; EXERCISE; SWIMMING;

ASTHMA, EXERCISE-INDUCED; BRONCHIAL HYPERREACTIVITY; CHILD; CHILD, PRESCHOOL; ENVIRONMENT; HUMANS; PREVALENCE; RESPIRATORY MUCOSA; RISK FACTORS; SWIMMING;

EID: 84880044640     PISSN: 08898561     EISSN: 15578607     Source Type: Journal    
DOI: 10.1016/j.iac.2013.02.008     Document Type: Review

References (93)

1. Bar-Yishay E., Gur I., Inbar O., et al. Difference between swimming and running as stimuli for exercise-induced asthma. Eur J Appl Physiol 1982, 48:387-397.
2. Bar-Or O., Inbar O. Swimming and asthma. Sports Med 1992, 16:397-405.
3. Piacentini G.L., Baraldi E. Pro: swimming in chlorinated pools and risk of asthma: we can now carry on sending our children to swimming pools!. Am J Respir Crit Care Med 2011, 183:569-570.
4. Bernard A., Voisin C., Sardella A. Con: respiratory risks associated with chlorinated swimming pools: a complex pattern of exposure and effects. Am J Respir Crit Care Med 2011, 183:570-572.
5. Bernard A., Nickmilder M., Voicin C., et al. Impact of chlorinated swimming pool attendance on the respiratory health of adolescents. Pediatrics 2009, 124:1110-1118.
6. Carbonnelle S., Francaux M., Doyle I., et al. Changes in serum pneumoproteins caused by short-term exposures to nitrogen trichloride in indoor chlorinated swimming pools. Biomarkers 2002, 7:464-478.
7. Voisin C., Sardella A., Marcucci F., et al. Infant swimming in chlorinated pools and the risks of bronchiolitis, asthma and allergy. Eur Respir J 2010, 36:41-47.
8. Bernard A., Nickmilder M., Voisin C. Outdoor swimming pools and the risks of asthma and allergies during adolescence. Eur Respir J 2008, 32:979-988.
9. Bernard A., Carbonnelle S., Dumont X., et al. Infant swimming practice, pulmonary epithelium integrity, and the risk of allergic and respiratory diseases later in childhood. Pediatrics 2007, 119:1095-1103.
10. Chaumont A., Voisin C., Sardella A., et al. Interactions between domestic water hardness, infant swimming and atopy in the development of childhood eczema. Environ Res 2012, 116:52-57.
11. Langdeau J.B., Turcotte H., Bowie D.M., et al. Airway hyperresponsiveness in elite athletes. Am J Respir Crit Care Med 2000, 161:1479-1484.
12. Zwick H., Popp W., Budik G., et al. Increased sensitization to aeroallergens in competitive swimmers. Lung 1990, 168:111-115.
13. Potts J.E. Adverse respiratory health effects of competitive swimming: the prevalence of symptoms; illness, and bronchial responsiveness to methacholine and exercise 1994, [dissertation], University of British Columbia, Vancouver (British Columbia).
14. Helenius I.J., Rytilä P., Metso T., et al. Respiratory symptoms, bronchial responsiveness, and cellular characteristics of induced sputum in elite swimmers. Allergy 1998, 53:346-352.
15. Bougault V., Turmel J., Boulet L.P. Bronchial challenges and respiratory symptoms in elite swimmers and winter sport athletes: airway hyperresponsiveness in asthma: its measurement and clinical significance. Chest 2010, 138:31S-37S.
16. Massin N., Bohadana A.B., Wild P., et al. Respiratory symptoms and bronchial responsiveness in lifeguards exposed to nitrogen trichloride in indoor swimming pools. Occup Environ Med 1998, 55:258-263.
17. Jacobs J.H., Spaan S., van Rooy G.B., et al. Exposure to trichloramine and respiratory symptoms in indoor swimming pool workers. Eur Respir J 2007, 29:690-698.
18. Nemery B., Hoet P.H., Nowak D. Indoor swimming pools, water chlorination and respiratory health. Eur Respir J 2002, 19:790-793.
19. Thickett K.M., McCoach J.S., Gerber J.M., et al. Occupational asthma caused by chloramines in indoor swimming-pool air. Eur Respir J 2002, 19:827-832.
20. Nordberg G.F., Lundstrom N.G., Forsberg B., et al. Lung function in volunteers before and after exposure to trichloramine in indoor pool environments and asthma in a cohort of pool workers. BMJ Open 2012, 2(5). pii:e000973.
21. Fantuzzi G., Righi E., Predieri G., et al. Airborne trichloramine (NCl(3)) levels and self-reported health symptoms in indoor swimming pool workers: dose-response relationships. JExpo Sci Environ Epidemiol 2012, 10.1038/jes.2012.56.
22. McFadden E.R., Gilbert I.A. Exercise-induced asthma. NEngl J Med 1994, 330:1362-1367.
23. Fitch K., Morton A.R. Specificity of exercise in exercise-induced asthma. Br Med J 1971, 4:577-581.
24. Ram F.S., Robinson S.M., Black P.N., et al. Physical training for asthma. Cochrane Database Syst Rev 2005, (4). CD001116.
25. Inbar O., Dotan R., Dlin R.A., et al. Breathing dry or humid air and exercise-induced asthma during swimming. Eur J Appl Physiol 1980, 44:43-50.
26. Gilbert I.A., Regnard J., Lenner K.A., et al. Intrathoracic airstream temperatures during acute expansions of thoracic blood volume. Clin Sci 1991, 81:655-661.
27. Donnelly P.M. Exercise-induced asthma: the protective role of CO2 during swimming. Lancet 1991, 337:179-180.
28. Bar-Or O., Neuman I., Dotan R. Effects of dry and humid climates on exercise-induced asthma in children and preadolescents. JAllergy Clin Immunol 1977, 60:163-168.
29. Anderson S.D., Daviskas E. The mechanisms of exercise-induced asthma is. ... JAllergy Clin Immunol 2000, 106:453-459.
30. Drobnic F., Freixa A., Casan P., et al. Assessment of chlorine exposure in swimmers during training. Med Sci Sports Exerc 1996, 28:271-274.
31. Bundgaard A., Schmidt A., Ingemann Hansen T., et al. Exercise-induced asthma after swimming and bicycle exercise. Eur J Respir Dis 1982, 63:245-248.
32. Withers R.T., Hamdorf P.A. Effect of immersion on lung capacities and volumes: implications for the densitometric estimation of relative body fat. JSports Sci 1989, 7:21-30.
33. Park K.S., Choi J.K., Park Y.S. Cardiovascular regulation during water immersion. Appl Human Sci 1999, 18:233-241.
34. Inbar O., Naiss S., Neuman E., et al. The effect of body posture on exercise- and hyperventilation- induced asthma. Chest 1991, 100:1229-1234.
35. Emtner M., Herala M., Stalenheim G. High intensity physical training in adults with asthma. Chest 1996, 109:323-330.
36. Fitch K.D., Morton A.R., Blansky B.A. Effects of swimming training on children with asthma. Arch Dis Child 1976, 51:190-194.
37. Varray A., Mercier J.G., Préfaut C.G. Individualized training reduces excessive hyperventilation in asthmatics. Int J Rehabil Res 1995, 18:297-312.
38. Weisgerber M.C., Guill M., Weisgerber J.M., et al. Benefits of swimming in asthma: effect of a session of swimming lessons on symptoms and PFTs with review of the literature. JAsthma 2003, 40:453-464.
39. Weisgerber M., Webber K., Meurer J., et al. Moderate and vigorous exercise programs in children with asthma: safety, parental satisfaction, and asthma outcomes. Pediatr Pulmonol 2008, 43:1175-1182.
40. Wardell C.P., Isbister C. Aswimming program for children with asthma. Does it improve their quality of life?. Med J Aust 2000, 173:647-648.
41. Matsumoto I., Araki H., Tsuda K., et al. Effects of swimming training on aerobic capacity and exercise-induced bronchoconstriction in children with bronchial asthma. Thorax 1999, 54:196-201.
42. Wicher I.B., Ribeiro M.A., Marmo D.B., et al. Effects of swimming on spirometric parameters and bronchial hyperresponsiveness in children and adolescents with moderate persistent atopic asthma. JPediatr (Rio J) 2010, 86:384-390.
43. Chandratilleke M.G., Carson K.V., Picot J., et al. Physical training for asthma. Cochrane Database Syst Rev 2012, (5). CD001116.
44. Sturani C., Sturani A., Tosi I. Parasympathetic activity assessed by diving-reflex and by airway response to methacholine in bronchial asthma and rhinitis. Respiration 1985, 48:321-328.
45. Kallenbach J.M., Webster T., Dowdeswell R., et al. Reflex heart rate control in asthma. Evidence of parasympathetic overactivity. Chest 1985, 85:644-648.
46. Penny P.T. Swimming pool wheezing. Br Med J (Clin Res Ed) 1983, 287:461-462.
47. Mustchin C.P., Pickering C.A. "Coughing water": bronchial hyperreactivity induced by swimming in a chlorinated pool. Thorax 1979, 34:682-683.
48. Stav D., Stav M. Asthma and whirlpool baths. NEngl J Med 2005, 353:1635-1636.
49. World Health Organization International programme on chemical safety, environmental health criteria 216: disinfectants and disinfectant by-products 2000, WHO, Geneva (Switzerland).
50. Keuten M.G., Schets F.M., Schijven J.F., et al. Definition and quantification of initial anthropogenic pollutant release in swimming pools. Water Res 2012, 46:3682-3692.
51. Varraso R., Massin N., Hery M., et al. Not only training but also exposure to chlorinated compounds generates response to oxidative stimuli in swimmers. Toxicol Ind Health 2002, 18:269-278.
52. Bernard A. Chlorination products: emerging links with allergic diseases. Curr Med Chem 2007, 14:1689-1699.
53. Agabiti N., Ancona C., Forastiere F., et al. Short term respiratory effects of acute exposure to chlorine due to a swimming pool accident. Occup Environ Med 2001, 58:399-404.
54. Lemiere C., Malo J.L., Boutet M. Reactive airways dysfunction syndrome due to chlorine: sequential bronchial biopsies and functional assessment. Eur Respir J 1997, 10:241-244.
55. Parimon T., Kanne J.P., Pierson D.J. Acute inhalation injury with evidence of diffuse bronchiolitis following chlorine gas exposure at a swimming-pool. Respir Care 2004, 49:291-294.
56. Deschamps D., Soler P., Rosenberg N., et al. Persistent asthma after inhalation of a mixture of sodium hypochlorite and hypochloric acid. Chest 1994, 105:1895-1896.
57. Martinez T.T., Long C. Explosion risk from swimming pool chlorinators and review of chlorine toxicity. JToxicol Clin Toxicol 1995, 33:349-354.
58. 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.
59. Ploysongsang Y., Beach B.C., DiLisio R.E. Pulmonary function changes after acute inhalation of chlorine gas. South Med J 1982, 75:23-26.
60. D'Alessandro A., Kuschner W., Wong H., et al. Exaggerated responses to chlorine inhalation among persons with non-specific airway hyperreactivity. Chest 1996, 109:331-337.
61. Cotter A., Ryan C.A. The pool chlorine hypothesis and asthma among boys. Ir Med J 2009, 102:79-82.
62. Kohlhammer Y., Döring A., Schäfer T., et al. Swimming pool attendance and hay fever rates later in life. Allergy 2006, 61:1305-1309.
63. Font-Ribera L., Kogevinas M., Zock J.P., et al. Swimming pool attendance and risk of asthma and allergic symptoms in children. Eur Respir J 2009, 34:1304-1310.
64. Ferrari M., Schenk K., Mantovani W., et al. Attendance at chlorinated indoor pools and risk of asthma in adult recreational swimmers. JSci Med Sport 2011, 14:184-189.
65. Jacobs J.H., Fuertes E., Krop E.J., et al. Swimming Pool attendance and respiratory symptoms and allergies among Dutch children. Occup Environ Med 2012, 69:823-830.
66. Schoefer Y., Zutavern A., Brockow I., et al. Health risks of early swimming pool attendance. Int J Hyg Environ Health 2008, 211:367-373.
67. Font-Ribera L., Villanueva C.M., Nieuwenhuijsen M.J., et al. Swimming pool attendance, asthma, allergies, and lung function in the Avon Longitudinal Study of Parents and Children cohort. Am J Respir Crit Care Med 2011, 183:582-588.
68. Gelardi M., Ventura M.T., Fiorella R., et al. Allergic and non-allergic rhinitis in swimmers: clinical and cytological aspects. Br J Sports Med 2012, 46:54-58.
69. Bougault V., Turmel J., Boulet L.P. Effect of intense swimming training on rhinitis in high-level competitive swimmers. Clin Exp Allergy 2010, 40:1238-1246.
70. Levesque B., Duchesne J.F., Gingras S., et al. The determinants of prevalence of health complaints among young competitive swimmers. Int Arch Occup Environ Health 2006, 80:32-39.
71. Castricum A., Holzer K., Brukner P., et al. The role of the bronchial provocation challenge tests in the diagnosis of exercise-induced bronchoconstriction in elite swimmers. Br J Sports Med 2010, 44:736-740.
72. Boulet L.P. Asymptomatic airway hyperresponsiveness: a curiosity or an opportunity to prevent asthma?. Am J Respir Crit Care Med 2003, 167:371-378.
73. Tschumperlin D.J., Drazen J.M. Chronic effects of mechanical force on airways. Annu Rev Physiol 2006, 68:563-583.
74. Bougault V., Morissette M., Murray N., et al. Oxidative stress in swimmers' airways. Eur Respir J 2010, 36(Suppl 54):5582. [abstract].
75. Bougault V., Turmel J., St Laurent J., et al. Asthma, airway inflammation and epithelial damage in swimmers and cold-air athletes. Eur Respir J 2009, 33:740-746.
76. Bougault V., Loubaki L., Joubert P., et al. Airway remodeling and inflammation in competitive swimmers with and without airway hyperresponsiveness. JAllergy Clin Immunol 2012, 129:351-358.
77. Karjalainen E.M., Laitinen A., Sue-Chu M., et al. Evidence of airway inflammation and remodeling in ski athletes with and without bronchial hyperresponsiveness to methacholine. Am J Respir Crit Care Med 2000, 161:2086-2091.
78. Nanson C.J., Burgess J.L., Robin M., et al. Exercise alters serum pneumoprotein concentrations. Respir Physiol 2001, 127:259-265.
79. Deitmer T., Scheffler R. Nasal physiology in swimmers and swimmers' sinusitis. Acta Otolaryngol 1990, 110:286-291.
80. Ondolo C., Aversa S., Passali F., et al. Nasal and lung function in competitive swimmers. Acta Otorhinolaryngol Ital 2009, 29:137-143.
81. Clearie K.L., Vaidyanathan S., Williamson P.A., et al. Effects of chlorine and exercise on the unified airway in adolescent elite Scottish swimmers. Allergy 2010, 65:269-273.
82. Fitch K.D. An overview of asthma and airway hyper-responsiveness in Olympic athletes. Br J Sports Med 2012, 46:413-416.
83. Simon-Rigaud M.L., Eechout C., Bourdin H., et al. Hyperréactivité bronchique et natation. Influence de l'entraînement en atmosphère chlorée. Sci Sports 1997, 12:142-147.
84. Bougault V., Turmel J., Boulet L.P. Airway hyperresponsiveness in elite swimmers: Is it a transient phenomenon?. JAllergy Clin Immunol 2011, 127:892-898.
85. Helenius I.J., Rytila P., Sarna S., et al. Effect of continuing or finishing high-level sports on airway inflammation, bronchial hyperresponsiveness, and asthma. JAllergy Clin Immunol 2002, 109:962-968.
86. Anderson S.D., Kippelen P. Assessment and prevention of exercise-induced bronchoconstriction. Br J Sports Med 2012, 46:391-396.
87. Bonini S., Bonini M., Bousquet J., et al. Rhinitis and asthma in athletes: an ARIA document in collaboration with GA2LEN. Allergy 2006, 61:681-692.
88. Bougault V., Boulet L.P. Airway dysfunction in swimmers. Br J Sports Med 2012, 46:402-406.
89. Lourencetti C., Grimalt J.O., Marco E., et al. Trihalomethanes in chlorine and bromine disinfected swimming pools: air-water distributions and human exposure. Environ Int 2012, 15:59-67.
90. Lee J., Jun M.J., Lee M.H., et al. Production of various disinfection byproducts in indoor swimming pool waters treated with different disinfection methods. Int J Hyg Environ Health 2010, 213:465-474.
91. Wyatt T.D., Wilson T.S. Abacteriological investigation of two leisure centre swimming pools disinfected with ozone. JHyg (Lond) 1979, 82:425-441.
92. Weng S., Li J., Blatchley E.R. Effects of UV 254 irradiation on residual chlorine and DBPs in chlorination of model organic-N precursors in swimming pools. Water Res 2012, 46:2674-2682.
93. Landeen L.K., Yahya M.T., Gerba C.P. Efficacy of copper and silver ions and reduced levels of free chlorine in inactivation of legionella pneumophila. Appl Environ Microbiol 1989, 55:3040-3050.