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Air Quality and Temperature Effects on Exercise‐Induced Bronchoconstriction

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ABSTRACT

Exercise‐induced bronchoconstriction (EIB) is exaggerated constriction of the airways usually soon after cessation of exercise. This is most often a response to airway dehydration in the presence of airway inflammation in a person with a responsive bronchial smooth muscle. Severity is related to water content of inspired air and level of ventilation achieved and sustained. Repetitive hyperpnea of dry air during training is associated with airway inflammatory changes and remodeling. A response during exercise that is related to pollution or allergen is considered EIB. Ozone and particulate matter are the most widespread pollutants of concern for the exercising population; chronic exposure can lead to new‐onset asthma and EIB. Freshly generated emissions particulate matter less than 100 nm is most harmful. Evidence for acute and long‐term effects from exercise while inhaling high levels of ozone and/or particulate matter exists. Much evidence supports a relationship between development of airway disorders and exercise in the chlorinated pool. Swimmers typically do not respond in the pool; however, a large percentage responds to a dry air exercise challenge. Studies support oxidative stress mediated pathology for pollutants and a more severe acute response occurs in the asthmatic. Winter sport athletes and swimmers have a higher prevalence of EIB, asthma and airway remodeling than other athletes and the general population. Because of fossil fuel powered ice resurfacers in ice rinks, ice rink athletes have shown high rates of EIB and asthma. For the athlete training in the urban environment, training during low traffic hours and in low traffic areas is suggested. © 2015 American Physiological Society. Compr Physiol 5:579‐610, 2015.

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Figure 1. Figure 1. The mean maximum percentage fall in FEV1 (±SEM) following bicycle exercise in relation to the concentration of water in the inspired air. Data taken, with permission, from Anderson et al. ().
Figure 2. Figure 2. Mean plus or minus SEM for the percentage fall in FEV1 in 8 asthmatic subjects who performed 4 minutes of exhausting cycling exercise while inspiring dry air at different temperatures. The mean values for expired temperature are given and demonstrate that abnormal cooling of the airways was unlikely to have occurred during exercise at the higher inspired temperatures. The data are from reference 111. The illustration is reproduced with permission from reference 12.
Figure 3. Figure 3. The change in FEV1 expressed as a percentage of the pre‐exercise value after exercise in children 20 to 24 h after 5 mg of montelukast. Reproduced, with permission, from Kemp et al. ().
Figure 4. Figure 4. Both airway cooling and mucosal dehydration occur in response to evaporative water loss from the airway surface. These events lead to exercise‐induced bronchoconstriction. Modified, with permission, from Anderson and Daviskas ().
Figure 5. Figure 5. The cumulative volume of periciliary fluid in relation to the number of generations of airways. The calculation was made on the basis of cumulative surface area of the airways assuming an exaggerated fluid depth of 10 microns (). This graph demonstrates that the volume of fluid available on the surface to humidify the inspired air is small. If the demand exceeds the rate of replacement, the osmolarity of the fluid will increase.
Figure 6. Figure 6. Epithelial cells and ion transport under basal conditions (A) and hyperosmotic stress during dry air hyperpnoea (B). Under basal conditions, Na+ ions are absorbed via an apical sodium channel, and Cl ions move paracellularly. Under basal conditions, water moves into the epithelial cells and submucosa due to the osmotic gradient created by the movement of these ions. During hyperpnoea, evaporative water loss reduces the periciliary fluid layer and increases the ion concentration, which creates an osmotic stimulus for water to move out of the epithelial cells. As a result, the epithelial cells shrink and this creates an osmotic stimulus for water to move from the submucosa. Hyperosmolarity of the epithelial cells and the submucosa is a possible stimulus for the release of nitric oxide (NO) and prostaglandins (PGs). These substances may contribute to the increase in the blood flow documented in humans breathing dry air. Reproduced, with permission, from Anderson and Daviskas ().
Figure 7. Figure 7. Cumulative loss of water predicted for each generation from the model of Daviskas () for a ventilation of 60 L/min at an inspired temperature of 26.7°C, and water content of 8.8 μL/L, a tidal volume of 2600 mL and a frequency of breathing of 23/min. The periciliary fluid layer volume is illustrated as the solid squares. The volume of water lost in 8 min exceeded the volume of periciliary fluid layer available in most generations. Reproduced, with permission, from Anderson et al. ().
Figure 8. Figure 8. Cumulative loss of water in relation to time predicted by the mathematical model of Daviskas et al. (). The horizontal lines intercept the axis at the volume of periciliary fluid assuming a depth of 5 or 10 microns and the epithelial cell fluid volume available assuming a depth of 50 microns from the trachea to the 12th generation. A net loss of 7.39 μL of fluid per liter of air is predicted to be lost after accounting for a predicted return under the inspired air conditions and ventilation. Adapted, with permission, from Anderson et al. ().
Figure 9. Figure 9. Mean percentage clearance (±SEM) of the whole right lung during isocapnic hyperventilation (ISH) with dry and warm humid air and nasal resting breathing (baseline) over the same time interval in asthmatic and healthy subjects. Inhalation of dry air caused a significant reduction (P < 0.002) in mucociliary clearance when compared with warm humid air and nasal breathing, both in asthmatic and healthy subjects. There was no difference between mucociliary clearance involving ISH with warm humid air and nasal breathing at rest. Adopted from Daviskas et al. (108), illustration reproduced from reference () with permission.
Figure 10. Figure 10. Cells involved in exercise‐induced bronchoconstriction. The epithelial cell layer is the source of prostaglandin E2 a bronchodilating prostaglandin. The levels are lower in asthmatics. The mast cells are the source of prostaglandin D2 and cysteinyl leukotrienes and eosinophils are also a source of cysteinyl leukotrienes. These bronchoconstricting mediators likely act directly on specific receptors on smooth muscle to cause contraction and airway narrowing. The sensory nerves may also be stimulated by these same mediators and contribute to airway narrowing. This has been demonstrated indirectly by the increase in leukotrienes being related to the increase in mucin (MUC5A) released from goblet cells and the release of neurokin A. The figure is modified, with permission, from the original by Hallstrand et al. ().
Figure 11. Figure 11. Density of mast cells, within airway epithelium, among subjects stratified by disease status (A) and by TH2 subgroup (B). Lines represent median values and boxes represent interquartile ranges. A, Asthmatic; H, Healthy. *P =0.011, Kruskal‐Wallis test. Reproduced, with permission, from Dougherty et al. ().
Figure 12. Figure 12. Mast cell mediator concentration increases in sputum of asthmatics with EIB in response to dry air. Values for histamine, tryptase, and cysteinyl leukotrienes at baseline and post exercise. Data adapted, with permission, from Hallstrand et al. ().
Figure 13. Figure 13. (A and C) The percentage change in FEV1 from baseline and (B and D) maximum change in 9 alpha 11 beta PGF2 in response to 6 min eucapnic voluntary hyperpnea of dry air (A and B) in the presence of placebo (closed circles) and after sodium cromoglycate (inverted triangles) in 11 subjects with >10% fall in FEV1 and (C and D) 4.5 h after placebo (closed circles) and 1500 μg of beclomethasone (squares) in eight subjects with asthma. Based on original data, with permission, from Kippelen et al. ().
Figure 14. Figure 14. Arachidonic acid pathway leading to the production of bronchodilating (PGE2) and bronchoconstricting (PGD2) and leukotrienes C4, D4 and E4. Adapted, with permission, from Wikimedia Commons.
Figure 15. Figure 15. Ground level Ozone is produced from the photochemical reaction between fossil fuel combustion emission volatile organic hydrocarbons and NO2 with oxygen. Ozone is significantly related to ambient temperature (R = 0.61; P < 0.05). Redrawn, with permission, from data from reference .
Figure 16. Figure 16. The highest particle number count from freshly generated emissions is in the 30 to 100 nm aerodynamic diameter particle size range. Adapted, with permission, from unpublished data.
Figure 17. Figure 17. Particle size relationship to the cross section of a human hair: Note most of the freshly generated emissions particles are in the ultrafine and smaller size range.
Figure 18. Figure 18. The relationship between particle mass and number count: note the smaller particles have high number counts but minimal mass. Redrawn, with permission, from data from reference .
Figure 19. Figure 19. Rate of PM1 decay from 62‐day mean values at 12 university soccer field measurement sites in relation to distance from a high traffic interstate highway (R = −0.999; values are presented as mean ± SE). Figure inset shows a three‐dimensional blanket graph of 62‐day PM1 mean measurements at the university soccer field. Redrawn, with permission, from data from reference .
Figure 20. Figure 20. Total lung deposition of particles of approximately 30 nm in diameter at rest and during exercise. Drawn, with permission, from data from reference .
Figure 21. Figure 21. The rate of PM1 decay for one rink when the ventilation system was at (A) low operational capacity and (B) peak operational capacity during two back‐to‐back ice hockey games. W, 1, 2, and 3 depicts warm‐up and between period ice resurfacing. Slopes of PM1 decay were significantly different between conditions (P < 0.05). Redrawn, with permission, from data from reference .
Figure 22. Figure 22. Baseline values for (A) FVC and FEV1 and (B) FEF25−75. Measurements after a transition to a training site where PM1 concentrations were high from fossil‐fueled ice resurfacers show significant declines in FEV1 and FEF25−75 (P < 0.05). Redrawn, with permission, from data from reference .
Figure 23. Figure 23. Reductions up to 6.1% in FEV1 and 5.4% in FVC after 2 h walking in high Ozone/PM1 were significantly larger than after walking for 2 h in low ozone/PM1 (P = 0.04 and P = 0.01) with P < 0.005 at some time points. Note the difference in response between mild and moderate asthmatics. Redrawn, with permission, from data from reference .
Figure 24. Figure 24. MDA concentration in exhaled breath condensate doubled after high PM1 exercise (P = 0.06), but not after low PM1 exercise, suggesting increased lipid peroxidation from high PM1 exposure exercise. Redrawn, with permission, from data from reference .
Figure 25. Figure 25. Falls in FEV1 at 5, 10, and 15 min after high‐intensity cycle ergometry in high and low PM1 after placebo (PL) or montelukast (ML) ingestion. Note the significant protection by ML during high PM1 exposure exercise (P < 0.05). Redrawn, with permission, from data from reference .
Figure 26. Figure 26. Possible mechanisms involved in the combined effects of exercise and chlorine by‐products exposure in swimmers.


Figure 1. The mean maximum percentage fall in FEV1 (±SEM) following bicycle exercise in relation to the concentration of water in the inspired air. Data taken, with permission, from Anderson et al. ().


Figure 2. Mean plus or minus SEM for the percentage fall in FEV1 in 8 asthmatic subjects who performed 4 minutes of exhausting cycling exercise while inspiring dry air at different temperatures. The mean values for expired temperature are given and demonstrate that abnormal cooling of the airways was unlikely to have occurred during exercise at the higher inspired temperatures. The data are from reference 111. The illustration is reproduced with permission from reference 12.


Figure 3. The change in FEV1 expressed as a percentage of the pre‐exercise value after exercise in children 20 to 24 h after 5 mg of montelukast. Reproduced, with permission, from Kemp et al. ().


Figure 4. Both airway cooling and mucosal dehydration occur in response to evaporative water loss from the airway surface. These events lead to exercise‐induced bronchoconstriction. Modified, with permission, from Anderson and Daviskas ().


Figure 5. The cumulative volume of periciliary fluid in relation to the number of generations of airways. The calculation was made on the basis of cumulative surface area of the airways assuming an exaggerated fluid depth of 10 microns (). This graph demonstrates that the volume of fluid available on the surface to humidify the inspired air is small. If the demand exceeds the rate of replacement, the osmolarity of the fluid will increase.


Figure 6. Epithelial cells and ion transport under basal conditions (A) and hyperosmotic stress during dry air hyperpnoea (B). Under basal conditions, Na+ ions are absorbed via an apical sodium channel, and Cl ions move paracellularly. Under basal conditions, water moves into the epithelial cells and submucosa due to the osmotic gradient created by the movement of these ions. During hyperpnoea, evaporative water loss reduces the periciliary fluid layer and increases the ion concentration, which creates an osmotic stimulus for water to move out of the epithelial cells. As a result, the epithelial cells shrink and this creates an osmotic stimulus for water to move from the submucosa. Hyperosmolarity of the epithelial cells and the submucosa is a possible stimulus for the release of nitric oxide (NO) and prostaglandins (PGs). These substances may contribute to the increase in the blood flow documented in humans breathing dry air. Reproduced, with permission, from Anderson and Daviskas ().


Figure 7. Cumulative loss of water predicted for each generation from the model of Daviskas () for a ventilation of 60 L/min at an inspired temperature of 26.7°C, and water content of 8.8 μL/L, a tidal volume of 2600 mL and a frequency of breathing of 23/min. The periciliary fluid layer volume is illustrated as the solid squares. The volume of water lost in 8 min exceeded the volume of periciliary fluid layer available in most generations. Reproduced, with permission, from Anderson et al. ().


Figure 8. Cumulative loss of water in relation to time predicted by the mathematical model of Daviskas et al. (). The horizontal lines intercept the axis at the volume of periciliary fluid assuming a depth of 5 or 10 microns and the epithelial cell fluid volume available assuming a depth of 50 microns from the trachea to the 12th generation. A net loss of 7.39 μL of fluid per liter of air is predicted to be lost after accounting for a predicted return under the inspired air conditions and ventilation. Adapted, with permission, from Anderson et al. ().


Figure 9. Mean percentage clearance (±SEM) of the whole right lung during isocapnic hyperventilation (ISH) with dry and warm humid air and nasal resting breathing (baseline) over the same time interval in asthmatic and healthy subjects. Inhalation of dry air caused a significant reduction (P < 0.002) in mucociliary clearance when compared with warm humid air and nasal breathing, both in asthmatic and healthy subjects. There was no difference between mucociliary clearance involving ISH with warm humid air and nasal breathing at rest. Adopted from Daviskas et al. (108), illustration reproduced from reference () with permission.


Figure 10. Cells involved in exercise‐induced bronchoconstriction. The epithelial cell layer is the source of prostaglandin E2 a bronchodilating prostaglandin. The levels are lower in asthmatics. The mast cells are the source of prostaglandin D2 and cysteinyl leukotrienes and eosinophils are also a source of cysteinyl leukotrienes. These bronchoconstricting mediators likely act directly on specific receptors on smooth muscle to cause contraction and airway narrowing. The sensory nerves may also be stimulated by these same mediators and contribute to airway narrowing. This has been demonstrated indirectly by the increase in leukotrienes being related to the increase in mucin (MUC5A) released from goblet cells and the release of neurokin A. The figure is modified, with permission, from the original by Hallstrand et al. ().


Figure 11. Density of mast cells, within airway epithelium, among subjects stratified by disease status (A) and by TH2 subgroup (B). Lines represent median values and boxes represent interquartile ranges. A, Asthmatic; H, Healthy. *P =0.011, Kruskal‐Wallis test. Reproduced, with permission, from Dougherty et al. ().


Figure 12. Mast cell mediator concentration increases in sputum of asthmatics with EIB in response to dry air. Values for histamine, tryptase, and cysteinyl leukotrienes at baseline and post exercise. Data adapted, with permission, from Hallstrand et al. ().


Figure 13. (A and C) The percentage change in FEV1 from baseline and (B and D) maximum change in 9 alpha 11 beta PGF2 in response to 6 min eucapnic voluntary hyperpnea of dry air (A and B) in the presence of placebo (closed circles) and after sodium cromoglycate (inverted triangles) in 11 subjects with >10% fall in FEV1 and (C and D) 4.5 h after placebo (closed circles) and 1500 μg of beclomethasone (squares) in eight subjects with asthma. Based on original data, with permission, from Kippelen et al. ().


Figure 14. Arachidonic acid pathway leading to the production of bronchodilating (PGE2) and bronchoconstricting (PGD2) and leukotrienes C4, D4 and E4. Adapted, with permission, from Wikimedia Commons.


Figure 15. Ground level Ozone is produced from the photochemical reaction between fossil fuel combustion emission volatile organic hydrocarbons and NO2 with oxygen. Ozone is significantly related to ambient temperature (R = 0.61; P < 0.05). Redrawn, with permission, from data from reference .


Figure 16. The highest particle number count from freshly generated emissions is in the 30 to 100 nm aerodynamic diameter particle size range. Adapted, with permission, from unpublished data.


Figure 17. Particle size relationship to the cross section of a human hair: Note most of the freshly generated emissions particles are in the ultrafine and smaller size range.


Figure 18. The relationship between particle mass and number count: note the smaller particles have high number counts but minimal mass. Redrawn, with permission, from data from reference .


Figure 19. Rate of PM1 decay from 62‐day mean values at 12 university soccer field measurement sites in relation to distance from a high traffic interstate highway (R = −0.999; values are presented as mean ± SE). Figure inset shows a three‐dimensional blanket graph of 62‐day PM1 mean measurements at the university soccer field. Redrawn, with permission, from data from reference .


Figure 20. Total lung deposition of particles of approximately 30 nm in diameter at rest and during exercise. Drawn, with permission, from data from reference .


Figure 21. The rate of PM1 decay for one rink when the ventilation system was at (A) low operational capacity and (B) peak operational capacity during two back‐to‐back ice hockey games. W, 1, 2, and 3 depicts warm‐up and between period ice resurfacing. Slopes of PM1 decay were significantly different between conditions (P < 0.05). Redrawn, with permission, from data from reference .


Figure 22. Baseline values for (A) FVC and FEV1 and (B) FEF25−75. Measurements after a transition to a training site where PM1 concentrations were high from fossil‐fueled ice resurfacers show significant declines in FEV1 and FEF25−75 (P < 0.05). Redrawn, with permission, from data from reference .


Figure 23. Reductions up to 6.1% in FEV1 and 5.4% in FVC after 2 h walking in high Ozone/PM1 were significantly larger than after walking for 2 h in low ozone/PM1 (P = 0.04 and P = 0.01) with P < 0.005 at some time points. Note the difference in response between mild and moderate asthmatics. Redrawn, with permission, from data from reference .


Figure 24. MDA concentration in exhaled breath condensate doubled after high PM1 exercise (P = 0.06), but not after low PM1 exercise, suggesting increased lipid peroxidation from high PM1 exposure exercise. Redrawn, with permission, from data from reference .


Figure 25. Falls in FEV1 at 5, 10, and 15 min after high‐intensity cycle ergometry in high and low PM1 after placebo (PL) or montelukast (ML) ingestion. Note the significant protection by ML during high PM1 exposure exercise (P < 0.05). Redrawn, with permission, from data from reference .


Figure 26. Possible mechanisms involved in the combined effects of exercise and chlorine by‐products exposure in swimmers.
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Kenneth W. Rundell, Sandra D. Anderson, Malcolm Sue‐Chu, Valerie Bougault, Louis‐Philippe Boulet. Air Quality and Temperature Effects on Exercise‐Induced Bronchoconstriction. Compr Physiol 2015, 5: 579-610. doi: 10.1002/cphy.c130013