Sports Science (A+ work, No plagarism, Quality Work)

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Br J Sports Med 2012;46:407–412. doi:10.1136/bjsports-2011-090823 407

ABSTRACT Unfavourable effects on the respiratory and the cardio-

vascular systems from short-term and long-term

inhalation of air pollution are well documented. Exposure

to freshly generated mixed combustion emissions

such as those observed in proximity to roadways with

high volumes of traffi c and those from ice-resurfacing

equipment are of particular concern. This is because

there is a greater toxicity from freshly generated

whole exhaust than from its component parts. The

particles released from emissions are considered

to cause oxidative damage and infl ammation in the

airways and the vascular system, and may be related to

decreased exercise performance. However, few studies

have examined this aspect. Several papers describe

deleterious effects on health from chronic and acute air

pollution exposure. However, there has been no research

into the effects of long-term exposure to air pollution

on athletic performance and a paucity of studies that

describe the effects of acute exposure on exercise

performance. The current knowledge of exercising in the

high-pollution environment and the consequences that it

may have on athlete performance are reviewed.

Evidence supports unfavourable effects from short- term and long-term inhalation of air pollution to the respiratory and the cardiovascular systems.1–10 Combustion-related pollutants such as nitrogen and sulphur oxides, the ammonium ion, organic aerosols, particulate matter (PM) and ozone are of concern. Inhaled PM can be causal to oxidative stress-related airway and vascular injury. Although there is ample evidence of short-term and long-term exposure affecting the respiratory and the cardio- vascular systems, little data are available demon- strating the effects of air pollution inhalation on athlete performance.10–12 During athlete training and competition, lung deposition of emission- related pollutants is high because of the increased ventilation during exercise,13 14 and inhalation of emission pollutants has been shown to cause the release of infl ammatory mediators from airway cells.15 16 Furthermore, the asthmatic response is worsened by high emission pollution.17 This study describes combustion-related pollutants that are of concern to the athlete, examines adverse health effects of inhaling airborne pollution during exer- cise and presents current evidence that suggests that athletic performance is compromised by inha- lation of emission-related aerosols during exercise.

CATEGORIES OF PARTICULATE MATTER Exposure to freshly generated mixed combustion emissions such as those observed in proximity

to high volumes of traffi c is of particular concern since evidence supports a greater toxicity from the freshly generated whole exhaust than from its component parts.15 Further, PM toxicity has been shown to be related to particle surface area, num- ber count and particle charge.18

Airborne PM is categorised by aerodynamic diameter and includes the primary categories of coarse, fi ne and ultrafi ne particles. Particles larger than 10 μm are not considered harmful to airways since they are primarily fi ltered at the nasopha- ryngeal region. Coarse particles (PM10) include those between 2.5 and 10 μm in diameter, fi ne particles (PM2.5) are particles smaller than 2.5 μm in diameter and ultrafi ne particles include those less than 0.1 μm diameter.19 The establishment of a separate category for particles less than 2.5 μm is based on research demonstrating that these smaller particles are more toxic because of their deeper penetration within the airways of the lung. PM less than 1 μm in diameter (PM1) are recorded in many studies, primarily because of portable equipment limitations. This size range typically includes particles in the 0.05 to 1 μm in diameter and is a suitable representation of freshly gener- ated particles. Although ultrafi ne PM (PM0.1), are not yet recognised by the US Environmental Protection Agency (EPA), they are considered to be the most harmful.4 13 14 18 20 Ultrafi ne par- ticle concentrations are high in freshly generated exhaust and can penetrate deep within the lung, but rapidly decrease in number count over time by agglomeration and dispersion (fi gure 1).21

PM from freshly generated exhaust emissions are likely to be the most toxic because they are high- est in number count and surface area and are in the particle size range of 50 to 100 nm (or about 1/1000 the diameter of a human hair) (fi gure 2). Fractional deposition of these 50 to 100 nm particles occurs in the alveolar region where exchange with the circulation may occur. Although coarse and fi ne particles are monitored by the EPA, most toxicol- ogy research has investigated ultrafi ne particles (PM0.1) and fi eld research has primarily measured PM1. An increased deposition fraction (fraction of inhaled particles remaining in the lungs after inha- lation) of PM during exercise has been identifi ed, with the largest deposition fraction noted for ultra- fi ne particles. For example, the fractional deposi- tion13 of PM0.1 is increased 4.5-fold during mild (38 l/min) exercise (fi gure 3).14 For PM2.5, it has been estimated that 9% is deposited in the lungs with 6% reaching the alveolar region.22 Exercise appears to increase the deleterious effects of PM inhalation by deposition, while damaged airway epithelium

Correspondence to Kenneth William Rundell, Pharmaxis Inc, Medical Affairs, One East Uwchlan Ave, Suite 405, Exton, Pennsylvania 19341, USA; [email protected]

Received 1 December 2011 Accepted 11 December 2011 Published Online First 20 January 2012

Effect of air pollution on athlete health and performance Kenneth William Rundell

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Br J Sports Med 2012;46:407–412. doi:10.1136/bjsports-2011-090823408

from mechanical stress of high ventilation may enhance par- ticle infi ltration to the circulatory system.

PM toxicology The precise toxicological mechanism(s) of inhaled PM has not been established; however, oxidative stress from exposure is likely involved. It is thought that inhalation of emission pollut- ants causes a release of infl ammatory mediators from airway cells that then enter the circulatory system, causing increased systemic oxidative stress. A decrease in lung antioxidants from in vitro carbon black exposure has been identifi ed and suggests that the epithelial lining fl uid-PM interface may represent an important initial PM detoxifying step.23 This could be critical to the exercising athlete as it is known that there is transient loss of airway surface liquid from high ventilation of dry air, mak- ing airway cells more vulnerable to effects of air pollutants. An acute twofold increase in lung antioxidants of rats exposed to diesel exhaust PM has been identifi ed,24 suggesting a protective role against PM-induced oxidative stress for lung antioxidants. As a consequence to exercise in high emission pollutants, a 44% decrease in total nitrate and a 40% increase in malondi- aldehyde in exhaled breath condensate were found, support- ing formation of the powerful oxidant, peroxynitrite9 from the reaction of nitric oxide (NO) and superoxide. Alternatively, NO reacts with glutathione in the lung to form a potent airway bronchodilator, S-nitrosoglutathione (GSNO).25–27

Studies have shown that reduced GSNO in the asthmatic airways could support increased leukotriene (LT) production, while high levels could inhibit LT production.28 Since a pre- dominantly LT-mediated bronchoconstriction after exercise in high PM has been shown,29 and marked glutathione depletion (to ~20% of pre-exposure levels)24 occurs in lung epithelial lin- ing fl uid after particle exposure, GSNO depletion may be, in part, responsible for PM-induced LT production.

If present in training and competition environments, freshly generated particles are of specifi c concern to athletes, and are likely to be related to the high prevalence of airway disease among certain athletic populations. The prevalence of exer- cise-induced bronchoconstriction (EIB), asthma and low rest- ing lung function is high for athletes who train and compete in a high PM-emission environments – far exceeding that of the non-athlete and the low-pollutant-exposed athlete. Pollutants from auto and truck emissions, high emissions from fossil-fu- el-powered ice-rink resurfacers and ski-waxing fumes all nega- tively affect the pulmonary and cardiovascular systems.

Potential consequences of inhaling pollutants during exer- cise include decreased lung function, increased exacerbations of asthma/EIB, decreased diffusion capacity, pulmonary hypertension, cardiovascular effects and decreased perfor- mance. McCreanor et al17 demonstrated the effect of a 2-h walk while breathing high-PM/high-ozone air compared with low-PM/low-ozone air on asthmatic airways. There was a concurrent signifi cant decrease in forced vital capacity (FVC) and forced expiratory volume in 1 s (FEV1) from the high-PM/ high-ozone exposure exercise, while lung function remained unchanged from walking in low-PM/low-ozone air (fi gure 4). An almost sixfold increase in sputum myeloperoxidase after the high-PM walk was also observed, suggesting neutrophilic infl ammation.

The high levels of PM1 observed at athletic fi elds and play- grounds in close proximity to major highways (fi gure 1) can affect pulmonary and vascular systems of healthy athletes. Only 30 min exposure to high-PM (>60 000 particles/cm3)/ high-ozone (106 to 300 ppb) ambient air during exercise

Figure 1 Sixty-two days of particle counts on an athletic fi eld within 50 m of a high-traffi c road. The x-axis is particle counts of particles <1 µm in diameter, those emitted from auto and truck emissions. Note that a rather rapid decay in number count is related to the distance from the source. Redrawn.21

Figure 2 Size distribution in number count of freshly generated emission particles. Note the largest number count is in the 50–60-nm size range.

Figure 3 Total particle deposition after 1-h rest and exercise while breathing 25 g/m3 ultrafi ne carbon black particulate matter. Redrawn.14

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20-min of exercise in freshly generated four-cycle exhaust (PM0.1>300 000 particles • cm

−3, CO<5 ppm).

ATHLETE PM EXPOSURE Ice-rink air is notoriously high in emission pollutants gener- ated from combustion-powered ice resurfacers.31 There have been numerous cases of NO2 and CO poisoning in ice rinks from ice-resurfacer exhaust emissions. Along with high NO2 and CO, high particle counts from fossil-fuelled ice resurfacers have been found.31 In one study, particle counts from rinks resurfaced with electric-powered resurfacers and those resur- faced with fossil-fuel-powered machines were compared.31 The particle counts in rinks using electric-powered resurfac- ers were not different to the particle counts of the proximal ambient air. Those rinks that were resurfaced by fossil-fuelled machines, however, had particle counts ~30 times greater than

causes a small but signifi cant decrease in lung function in non- asthmatics (fi gure 5).9

Inhalation of air pollution also has negative effects on the vascular system. Thirty minutes of exercise in high-PM air resulted in a basal vasoconstriction of the brachial artery, disrupted normal vascular endothelial function, decreased fl ow-mediated dilatation response and a 55% decrease in re oxygenation of the muscle microcirculation.8 Arteriole dila- tation was reported to be impaired after pulmonary exposure to particles and myeloperoxidase was found on adhering neu- trophils on the vascular endothelial wall.30 It was proposed that this may affect the infl uence of NO on vascular tone and that the decreased tissue perfusion of the microvascula- ture from particle inhalation may compromise muscle func- tion. Cutrufello et al10 noted an increase in pulmonary artery pressure as well as disrupted fl ow-mediated dilatation after

Figure 4 Lung function of asthmatic subjects during and after a 2-hour walk in either low or high freshly generated diesel emissions. Redrawn.17

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FEV1, with little change in the FEV1/FVC ratio, is characteristic of early asthma development.

For the Nordic and alpine skier, ski-waxing fumes from daily hot waxing provide a major contribution to exposure. Many of today’s ski waxes are fl uorinated and have been shown to have a negative effect on lung function.36 When applied to skis, a hot iron is used; termed ‘hot waxing’. Hot waxing results in ultrafi ne fl uorine particles being released into the air in concentrations 25-fold higher than prewaxing. Animal studies have shown that these fl uorine particles are quite toxic.37 Although exposure does not occur during exer- cise, it does occur on a daily basis beginning early in the skiers career, when lungs are susceptible to damage. This repeated exposure in combination with airway damage from high ven- tilation of cold dry air during competition and training may contribute to the airway dysfunction observed in Nordic ski- ers. Of course, the elite skier spends little time in the wax room, but young developing skiers do, since they wax their own skis until reaching the elite level. Consequently, there are many years of exposure to the developing lung on the path to becoming an elite-level skier.

ATHLETE PERFORMANCE AND PM Inhalation of high levels of combustion-derived PM during exercise has been shown to result in reduced exercise perfor- mance during short-term maximal-intensity cycle ergometry.10 12 A single 6-min exercise bout in high PM failed to reduce exercise performance; however, a second 6-min of exercise in high PM 3 days after the fi rst resulted in decreased exercise performance. This observation supports a delayed infl am- matory effect from the initial exercise.12 In a separate study, decreased work accumulation was observed in a high-inten- sity 6-min cycle ergometer ride that immediately followed a 20-min high-PM exposure ride at 60% of estimated maxi- mal heart rate,10 suggesting that a rapid response can occur within a single 20-min exposure. In this study, low-PM (L) and high-PM groups (H) were randomised, but L and H pairs were exercised 1 day apart, to evaluate 24-h effect of exposure. Unlike the previous study,12 these results showed decreases in performance in both high-PM rides. This was thought to occur because the 20-min prework accumulation ride allowed time for a systemic infl ammatory response to occur, whereas the earlier study12 did not incorporate that pretime trial 20-min ride. The performance decreases from exercise in high emis- sion-generated PM air observed in those studies were about 5%12 and 3%, respectively (fi gure 7).10 The implications of these studies to the athlete competing in a high-air-pollution environment suggest that even a 20-min warm-up in high air pollution will have an impact on subsequent performance. Further, only one 6-min bout of exercise in high pollution may have a carryover effect that will decrease the performance in exercise 3 days later.

Blunted fl ow-mediated dilatation from exercise in freshly generated four-cycle emission aerosols has been observed ( fi gure 8A).10 12 Signifi cant increases in pulmonary artery pres- sure after high-pollution exercise were also noted (fi gure 8B).10 Vascular function was correlated with exercise performance and accounted for as much as 24.4% of the decline in exercise performance. The <5% performance decrements are quite sig- nifi cant to the competing athlete. For example, all but the last place fi nisher in the 3000-m steeplechase at the 2008 Olympics were separated by less than 5%. These studies provide evi- dence that high-PM conditions are likely to affect athletic

Figure 6 Measurements of PM1 at 10 ice rinks demonstrate signifi cant increases in particulate matter (PM1) after rinks were resurfaced by fossil-fuelled machines. Rinks using electric-powered machines showed no increase in PM1. Redrawn.

6

Figure 5 Signifi cant change in lung function (forced expiratory volume in 1 s (FEV1) and FEF25–75) of non-asthmatic subjects after 30-min of high-particulate matter (PM1) exercise was identifi ed. No change in lung function was noted from low-PM1 exposure exercise (p=0.0005 for FEV1 and p=0.002 for FEF25–75). Redrawn.

9

proximal ambient air (fi gure 6). As a result of this study, the Vancouver 2010 Olympic Games used electric-powered ice resurfacers to ensure acceptable air quality at all 2010 Olympic ice rinks.

Recent papers examining ice-rink air quality31 and the relationship to EIB have associated the high prevalence of airway dysfunction in skating athletes to inhalation of PM1.

6

7 The 20% to 43% prevalence of EIB reported in fi gure skat- ers, hockey players and short-track-speed skaters32–34 is much higher than the estimated 10% asthma prevalence in the US and the reported prevalence for summer Olympic Games, ath- letes.35 Repeated ventilation of cold/dry air during sport train- ing and competition, combined with high levels of PM1, may enhance the expression of or directly cause EIB and airway damage. Long-term exposure can have signifi cant effects on resting airway function.6 7 Signifi cant decrease in FVC, FEV1 and FEF25–75 over a 3-year period of daily training in an ice rink with high PM1 from fossil-fuelled resurfacers in female hockey players has been identifi ed.6 The decline in FVC and

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CONCLUSION Acute exposure to mixed exhaust aerosols during exercise can cause decreases in lung and vascular function in healthy and asthmatic subjects. Chronic exposure to mixed exhaust aerosols during exercise may result in decreased lung function and may promote vascular dysfunction, which appear to be related to increased airway and systemic oxidative stress. The physiological effects of high-intensity exercise in high levels of mixed exhaust aerosols support the observed compromised performance.

Competing interests None.

Provenance and peer review Commissioned; internally peer reviewed

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