PAULA ROBSON-ANSLEY1,2, GLYN HOWATSON1,3, JAMIE TALLENT1, KELLY MITCHESON1, IAN WALSHE1, CHRIS TOMS1, GEORGE DU TOIT4, MATT SMITH5, and LES ANSLEY1 1

School of Life Sciences, Northumbria University, Newcastle-upon-Tyne, UNITED KINGDOM; 2Department of Physiological Sciences, Stellenbosch University, Matieland, SOUTH AFRICA; 3Centre for Aquatic Research, University of Johannesburg, Johannesburg, SOUTH AFRICA; 4Medical Research Council and Asthma UK Centre in Allergic Mechanisms of Asthma, Division of Asthma, Allergy and Lung Biology, School of Medicine, King’s College London, Guy’s and St. Thomas’ National Health Service, Foundation Trust, London, UNITED KINGDOM; and 5National Pollen and Aerobiology Research Unit, University of Worcester, Worcester, UNITED KINGDOM

ABSTRACT ROBSON-ANSLEY, P., G. HOWATSON, J. TALLENT, K. MITCHESON, I. WALSHE, C. TOMS, G. DU TOIT, M. SMITH, and L. ANSLEY. Prevalence of Allergy and Upper Respiratory Tract Symptoms in Runners of the London Marathon. Med. Sci. Sports Exerc., Vol. 44, No. 6, pp. 999–1004, 2012. Background: The prevalence of self-reported upper respiratory tract (URT) symptoms in athletes has been traditionally associated with opportunistic infection during the temporal suppression of immune function after prolonged exercise. There is little evidence for this, and a competing noninfectious hypothesis has been proposed, whereby the exercise-induced immune system modulations favor the development of atopy and allergic disease, which manifests as URT symptoms. The aim of this study was to examine the association between allergy and URT symptoms in runners after an endurance running event. Methods: Two hundred eight runners from the 2010 London Marathon completed the validated Allergy Questionnaire for Athletes (AQUA) and had serum analyzed for total and specific immunoglobulin E response to common inhalant allergens. Participants who completed the marathon and nonrunning controls who lived in the same household were asked to complete a diary on URT symptoms. Results: Forty percent of runners had allergy as defined by both a positive AQUA and elevated specific immunoglobulin E. Forty-seven percent of runners experienced URT symptoms after the marathon. A positive AQUA was a significant predictor of postmarathon URT symptoms in runners. Only 19% of nonrunning controls reported symptoms. Conclusions: The prevalence of allergy in recreational marathon runners was similar to that in elite athletes and higher than that in the general population. There was a strong association between a positive AQUA and URT symptoms. The low proportion of households in which both runners and nonrunners were symptomatic suggests that the nature of symptoms may be allergic or inflammatory based rather than infectious. Allergy is a treatable condition, and its potential effect on performance and health may be avoided by accurate clinical diagnosis and management. Both athletes’ and coaches’ awareness of the potential implications of poorly managed allergy needs to be raised. Key Words: ALLERGIC RHINITIS, ATHLETES, EXERCISE-INDUCED ASTHMA, INHALANT ALLERGENS, UPPER RESPIRATORY TRACT INFECTION

A

necdotal evidence and scientific observation suggest that after exercise, there is an increase in the reported incidence, in athletes, of symptoms more commonly associated with infections of the upper respiratory airways. These reports are notably related to periods of heavy training as well as after a prolonged exercise bout (19,20,22). Temporary modulations in innate and adaptive immune system function have been proposed as the basis for the relation-

ship between susceptibility to infection and physical activity levels (19). However, a recent study that analyzed nasopharyngeal and throat swabs from athletes reporting symptoms of the upper respiratory tract (URT) (25) identified pathogens in only 30% of cases, with bacterial infections accounting for È5% of episodes. Indeed, where herpes group viruses and Epstein–Barr virus reactivation have been thought to be the cause of URT symptoms reported by elite athletes (23), antiherpes virus treatment was not effective in reducing the frequency of URT episodes and therefore suggests other noninfective causes for URT symptoms in athletes. This has lead to the development of the ‘‘noninfectious’’ hypothesis in which self-reported symptoms of infection are related to noninfective inflammatory factors (28). Many of the symptoms associated with URT infections, such as congestion and wheeze, are also common in allergy and airway inflammation. Because there is a greater prevalence of inhalant allergy in competitive athletes

Address for correspondence: Paula Robson-Ansley, PhD, School of Life Sciences, Northumbria University, Newcastle-upon-Tyne NE1 8ST, United Kingdom; E-mail: [email protected]. Submitted for publication July 2011. Accepted for publication October 2011. 0195-9131/12/4406-0999/0 MEDICINE & SCIENCE IN SPORTS & EXERCISEÒ Copyright Ó 2012 by the American College of Sports Medicine DOI: 10.1249/MSS.0b013e318243253d

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Prevalence of Allergy and Upper Respiratory Tract Symptoms in Runners of the London Marathon

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TABLE 1. Environmental and pollen conditions on the London Marathon race day (April 25, 2010). Environmental Variable

Measure

Average temperature (-C) Maximum temperature (-C) Barometric pressure (hPa) Precipitation (mm) Pollen count (grains per cubic meter of air) Birch (Betula) Plane (Planatus) Willow (Salix) Ash (Fraxinus) Oak (Quercus) Grasses (Poaceae)

10 15 1019 0 356 519 11 10 2 0

than in their nonathletic counterparts (17), this may provide some explanation for the seemingly higher incidence of URT infection in athletes. Poorly managed allergic symptoms have the potential to impair an athlete’s performance (11,14,29). However, efficacious treatment and management strategies are readily available, but to implement these strategies, the allergy needs to be diagnosed in advance of competition or training season and in the context of the anticipated exposure to specific aeroallergens (9). With less than a year until the London 2012 Olympic Games, a focused approach to allergy diagnosis and management in inhalant-allergic athletes is essential to optimize their athletic performance. This is especially important because the Olympic Games are being held in August, which coincides with peak grass and weed season in London. In this study, we measured the prevalence of allergy in a large cohort of runners who competed in the 2010 London Marathon using the Allergy Questionnaire for Athletes (AQUA) (3) and specific immunoglobulin E (sIgE) response to a panel of common inhalant allergens. We also assessed the incidence of URT symptoms in the athletes for 2 wk after the run. We expected the prevalence of allergy in the marathon runners to be related to the incidence of self-reported URT symptoms after the race.

TABLE 2. Prevalence of sensitization to common allergens in runners (n = 201) partaking in the 2010 London Marathon. Common Name Dust mite Grass mix (sweet vernal, rye, Timothy, cultivated rye, velvet grass)

Timothy grass Common silver birch Tree pollen mix (box elder, common silver birch, hazel, oak, London plane) London plane Mold

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Latin Name

Panel Code

Prevalence (%)

Dermatophagoides pteronyssinus Anthoxanthum odoratum, Lolium perenne, Phleum pratense, Secale cereale, Holcus lanatus Phleum pratense Betula verrucosa Acer negundo, Betula verrucosa, Corylus avellana, Quercus alba, Platanus acerifolia Platanus acerifolia Alternaria alternata

d1

36.3

gx3

29.9

METHODS Recreational runners (n = 208) were recruited randomly during the 4-d registration exhibition before competing in the 2010 London Marathon (April 25, 2010). Participants were age 40.3 T 10.9 and 37.4 T 9.6 yr for males (n = 120) and females (n = 81), respectively, and had completed, on average, 7.6 h (range = 2–30 h) of training per week. Ethical approval for the study was gained through the local research ethics committee. Informed consent was obtained from all participating runners. The exclusion criterion for the study was an infection within the 2 wk preceding the registration. The AQUA was used to assess allergic symptoms. The AQUA has been validated as a reliable tool for assessing the prevalence of allergy in a group of athletes (3). The AQUA was derived from the European Community Respiratory Health Survey Questionnaire and adapted to the target population using open interviews with athletes, team physicians, and coaches. The AQUA was administered for validation to professional football players (n = 128) alongside allergy diagnosis using skin prick testing/sIgE determination and comprehensive allergy history. A total AQUA score of five or greater had the best predictive value for allergy (0.94) with a specificity of 97.1% and a sensitivity of 58.3%. In the current study, questions were weighted in accord with Bonini et al. (3); total AQUA scores of five or greater were used as the threshold for a positive questionnaire. Participants were also asked to report their average training volume (hIwkj1) in preparation for the marathon. Objective evidence of sensitization to common aeroallergens was obtained from sIgE determination (Phadia AB, Uppsala, Sweden) of a blood sample to a panel of common aeroallergens. The allergen panel was based on the most common airborne pollen on the day of the marathon (Table 1) and key inhalant allergens (Table 2). Sensitization was indicated when sIgE was 9 0.35 kUA per liter for any allergen. (Results are expressed in quantitative units, kUa/L, where one kUa/L corresponds to 2.4 mg of IgE per liter.) The threshold for a high total IgE was Q114 kU IgEILj1. We defined atopy as sensitization to at least one of the selected allergens, whereas a positive AQUA questionnaire, in addition to atopy, was considered as indicative of allergy. The term ‘‘allergic disease’’ refers to the reported presence of one or more of the conditions listed in Table 3 independent of the presence of sIgE antibodies.

TABLE 3. Prevalence of physician-diagnosed allergic diseases in runners (n = 201) partaking in the 2010 London Marathon. Allergic Condition g6 t3 tx8

28.9 15.9 15.4

t11 m6

8.0 1.5

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Prevalence (%)

Asthma Eczema Drugs allergy Rhinitis Food allergy Insect venom allergy Anaphylaxis Conjunctivitis Urticaria

24.8 8.0 7.0 3.4 1.5 1.0 0.5 0.4 0.0

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RESULTS Of the 208 volunteers, prerace AQUA and/or IgE was incomplete for seven athletes (3%); therefore, AQUA and atopy data are presented for 201 runners. One hundred seventy-one (85%) of these 201 participants finished the marathon. Fourteen athletes (7%) had reported current use of antihistamines (n = 13) and/or antibiotics (n = 5) and were excluded from the postrace symptom analysis. One hundred thirty-eight runners (69%) completed the postrace symptoms questionnaire, 117 (58%) of whom also provided symptoms data for another adult nonrunner member of their household. Study participants reported an average weekly training duration of 7.59 T 4.66 h (n = 174), and the mean finishing time for the marathon was 5.07 T 1.05 h (n = 171). The environmental conditions and pollen count on the day of the London Marathon are presented in Table 1. AQUA and atopy (n = 201). Sixty-six percent (132/201) of runners had a positive (Q5) AQUA questionnaire total

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score, and 49% (99/201) of runners displayed a positive sIgE response for one or more of the selected allergens. The prevalence of sensitization to common inhalant allergens is presented in Table 2. Forty percent (80/201) of athletes had a positive AQUA score and atopy. The mean AQUA scores for atopic and nonatopic runners were 12.5 T 8.1 and 6.1 T 6.0, respectively (P G 0.0001); a positive AQUA was significantly predictive of atopy (LR+ = 1.6, P G 0.0001) with a positive predictive value of 0.61 and a sensitivity and specificity of 81% and 49%, respectively. The AQUA questionnaire was also predictive of sensitivity to each individual allergen except mold (Alternaria alternata). However, 26% (52/201) of runners scored a positive AQUA with no objective evidence of atopy, although 12% (6/52) of these runners did have elevated total IgE suggesting a predisposition to sensitization. Fifty-five percent (110/201) of runners indicated either a physician-diagnosed allergic disease (Table 3) or self-reported allergic symptoms. However, 77% (85/110) of these athletes were not using any form of medication, a quarter of whom did not do so for fear of affecting performance. Allergic diseases were reported by 31% (23/75) of participants who had no detectable IgE antibodies to the atopy panel. Asthma and exercise-induced bronchoconstriction. Thirty-two percent (64/201) of athletes reported symptoms related to exercise-induced bronchoconstriction (EIB), i.e., shortness of breath, cough, and/or itching of the throat after exercise, and this was significantly predictive of asthma (LR+ = 3.9, P G 0.0001). Nineteen percent (12/64) of athletes with EIB were allergic (i.e., sensitized to one or more allergens and a positive AQUA) but did not have physiciandiagnosed asthma; 23% (15/64) had EIB symptoms during exercise but were neither atopic nor asthmatic. Only 30% (15/50) of runners with a diagnosis of asthma were using their medication. Seventeen percent (34/201) of athletes reported frequently experiencing URT infections. Athlete symptoms (n = 138). Of all the runners who completed the postrace questionnaire, 47% (65/138) complained of symptoms at some point in the 15 d after the

FIGURE 1—Prevalence and incidence of self-reported symptoms in runners (n = 138) during 15 d after a marathon. New incidences are topmost.

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Blood samples for total IgE and sIgE analysis were drawn from a superficial vein and collected in serum separation tubes (Becton, Dickinson, Oxford, United Kingdom). The sample was placed immediately inside a chilled chamber. All samples were frozen to j80-C within 12 h of collection. Samples were later analyzed for sIgEs as well as total IgE. URT symptoms were assessed from a questionnaire (22). Runners were required to complete a daily symptom questionnaire for 15 d after the race, reporting cough, watery eyes, a congested nose, sneezing, and nasal discharge. A runner was considered symptomatic if two or more of these symptoms were present for at least 2 d in a 3-d period. An identical questionnaire was used for the control member of the runners’ household. Pollen data for North London were obtained from the roof of the Environmental and Public Protection offices, in the Borough of Islington. The methodology used for collecting the pollen data at the London Marathon followed the standard method of the UK National Pollen Monitoring Network described by the British Aerobiology Federation (6). Pollen grains were identified to family or genus level, depending on type. Daily average concentrations of pollen are expressed as grains per cubic meter. Statistical analysis. Descriptive data are presented as mean T SD. A Fisher exact test (2  2) was used to examine the significance of association between test outcomes and conditions within the data and quantify the sensitivity, specificity, and likelihood ratio. The positive likelihood ratio (LR+) for predicting an outcome on the basis of a contingency table was calculated from the following formula: LR+ = sensitivity/(1 j specificity). LR+ is a measure of how many times more likely the outcome is when the test is positive. Differences between groups were assessed with an independent-samples t-test. The level of significance was accepted at P e 0.05. All analyses were conducted on the GraphPad Prism 5.0d (GraphPad Software, Inc).

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FIGURE 2—Prevalence of respiratory symptoms during the same 15-d period after the marathon in runners (n = 117) and nonrunners (n = 117) who live in the same household.

marathon (Fig. 1). Fifty-eight percent (48/81) of runners with allergy were symptomatic after the marathon (LR+ = 1.6, P = 0.07). A positive AQUA questionnaire was significantly predictive of self-reported postrace respiratory symptoms (LR+ = 1.5, P = 0.0008), whereas there was no association between atopy and symptoms (P = 0.733). Sixtyfive percent (17/26) of runners who responded positively to the AQUA question ‘‘Do you frequently suffer from URT infections or fever?’’ reported postrace URT symptoms (LR+ = 2.1, P = 0.05). Athlete versus nonathlete symptoms (n = 117). Of the 117 runners who also provided symptoms data for a nonrunner member of their household, 45% (53/117) reported symptoms, whereas only 19% (22/117) of the nonrunners displayed symptoms (Fig. 2). In only 12 households (23%) were symptoms reported by both runners and nonrunners. Being a runner significantly increased the risk of experiencing respiratory symptoms compared with nonrunners in the 2 wk after the marathon (LR+ = 1.8, sensitivity = 71% and specificity = 60%, P G 0.0001).

DISCUSSION The main finding of this study was that 40% of the runners in our study had allergy as defined by a positive AQUA questionnaire and objective evidence of sensitization. In addition, we found that almost half (47%) of the runners experienced URT symptoms after the marathon, and less than a fifth (19%) of nonrunners residing in the same household reported symptoms. Our data also showed that a positive AQUA questionnaire was a significant predictor of the development of URT symptoms in runners. Atopy was present in a high proportion of the marathon runners (almost one in two). This agrees with previous prevalence data from elite long-distance runners (49%) (13) but is higher than that reported for randomly selected adults in the United Kingdom (34%–44%) (27). A possible explanation for this difference in prevalence may be the effect of high volumes of physical exercise on T-helper cell polarization and the exercise-induced cytokine milieu. Immunological data suggest that chronic exercising training can

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lead to a polarization of T-helper lymphocytes toward the Th2 phenotype (16,26), which could predispose athletes to allergic disease and greater frequency of reported URT symptoms such as allergic rhinitis. Peters and Bateman (22) also observed a twofold increase in reported URT symptoms in runners compared with nonrunners. These symptoms have traditionally been attributed to infection resulting from acute suppression of the immune function (19). It seems that excessive exercise can transiently suppress markers of immune function (21), but to date, there is no evidence to support the progression from low-level immune function suppression to infection (28) . Moreover, the time course of symptoms and the absence of pathogens in the sputum of more than two-thirds of runners reporting URT symptoms (25) lend support to the noninfectious hypothesis (2). Significantly, symptoms were concurrent in only 23% of households in which runners and nonrunners both reported symptoms. This provides further evidence that in a significant proportion of instances where URT symptoms are reported, the pathology is unlikely to be an infectious agent. We found a strong association between both a positive AQUA questionnaire and positive sIgE and the incidence of postrace URT symptoms in runners, indicating that a high proportion of these symptoms might be related to allergy rather than infection. Overall, our data are in agreement with previous research (23) that suggests only one-third of URT symptoms are attributable to infection and the remaining two-thirds are caused by allergy and/or inflammation. Marathon runners have extensive exposure to many outdoor inhalant allergens during the pollen season. The London Marathon usually takes place before many herbaceous plants have started flowering (15) and tree pollen is a most dominant outdoor allergen, although the amount and type of tree pollen recorded on the day of the London Marathon varies annually (Fig. 3). The shifting of breathing during exercise from nose to combined mouth and nasal breathing results in a greater deposition of airborne allergens and unconditioned

FIGURE 3—Daily average pollen counts for birch (Betula) and plane (Planatus) recorded on the day of the London Marathon during the last decade (2000–2010).

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allergy-related incidents, which could affect subsequent athletic performance. In consideration of the London 2012 Olympic Games, it would be prudent for all elite athletes to be screened for atopy and allergy to prevalent inhalant allergens for the season and time of year, e.g., grass pollen, which peaks in June and July but can be present in the air to mid-August, and weeds such as Artemisia that flower in late summer. This advice is particularly sage considering the planned planting of 10,000 trees in the run up to the Olympics for London (10). In conclusion, the prevalence of allergy in recreational athletes performing high volumes of training is higher than that in the general population but similar to that reported for elite athletes. The incidence of URT symptoms is higher in runners than nonrunners of the London Marathon, and the strong association between a positive allergy questionnaire and URT symptoms in addition to the low proportion of households in which both runners and nonrunners were symptomatic suggests that the pathology of symptoms may be allergic rather than infectious in nature. On the basis of these results, we recommend that, even at the level of recreational participation, individuals undertaking endurance exercise should be educated in the health implications of unmanaged allergy and screened for allergic predisposition using a validated questionnaire and/or a validated objective allergy test (e.g., skin prick testing and/or sIgE blood tests) for inhalant allergens. There are no conflicts of interest for any author. No funding was received for this work (from the National Institutes of Health, Wellcome Trust, or any others). The authors thank the Environmental and Public Protection offices, Islington, for use of the pollen data and Phadia, Sweden, for their provision of consumables for total IgE and sIgE tests. The results of the present study do not constitute endorsement by the American College of Sports Medicine.

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air to the lower airways (18). It has been previously proposed that athletes who are repeatedly and excessively exposed to outdoor inhalant allergens may develop symptoms of asthma (12). Our data indicate that 32% of marathon runners had symptoms of EIB, which was predictive of physician-diagnosed asthma (LR+ = 3.9). Of particular concern are the 19% of athletes reporting symptoms of EIB who were allergic but not asthmatic because they may be at significant risk of developing asthma in the future if their EIB and allergy remain untreated (4,5). It was also worrying to note that fewer than half of the runners who had an asthma diagnosis were using medication to control their condition. In general, the use of pharmacological treatment for allergy and asthma by runners with diagnosed allergic disease was extremely low (23%), with a large proportion of athletes not taking medication. This is due to perceived performance effects and/or concerns of falling foul of World Anti-Doping Association–banned substance list. The risk of untreated allergy and asthma on long-term health is considerable (7,24) and is associated with a higher risk of hospitalization in persons with asthma with untreated allergic rhinitis (8). Perhaps surprising at first glance is that a greater proportion of elite athletes report regular use of allergy medications (50% of Finnish elite athletes) (1); however, this is most likely due to improved clinical provision and education of athletes at that level of participation. Recommendations for allergy treatment in athletes are the same as in nonathletes. Intranasal corticosteroids are the management drug of choice in conjunction with secondgeneration antihistamines (severity dependent) and, where practicable, allergen avoidance (9). Immunotherapy should also be considered as a potential therapy for pollen-allergic individuals. Diagnosis and the development and implementation of an early management plan for allergic conditions in athletes are essential to prevent any adverse

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