Sensitization was indicated when sIgE was > 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 ≥114 kU IgE·L−1. 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.
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 −80°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.
Descriptive data are presented as mean ± 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 − 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 ≤ 0.05. All analyses were conducted on the GraphPad Prism 5.0d (GraphPad Software, Inc).
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 ± 4.66 h (n = 174), and the mean finishing time for the marathon was 5.07 ± 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 (≥5) AQUA questionnaire total 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 ± 8.1 and 6.1 ± 6.0, respectively (P < 0.0001); a positive AQUA was significantly predictive of atopy (LR+ = 1.6, P < 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 < 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 physician-diagnosed 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 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). Sixty-five 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 < 0.0001).
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 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 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 second-generation 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 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.
1. Alaranta A, Alaranta H, Heliovaara M, Alha P, Palmu P, Helenius I. Allergic rhinitis
and pharmacological management in elite athletes
. Med Sci Sports Exerc. 2005; 37 (5): 707–11.
2. Bermon S. Airway inflammation and upper respiratory tract infection
: is there a link? Exerc Immunol Rev. 2007; 13: 6–14.
3. Bonini M, Braido F, Baiardini I, et al.. AQUA: Allergy Questionnaire for Athletes
. Development and validation. Med Sci Sports Exerc. 2009; 41 (5): 1034–41.
4. Bousquet J, Khaltaev N, Cruz AA, et al.. Allergic Rhinitis
and its Impact on Asthma (ARIA) 2008 update (in collaboration with the World Health Organization, GA(2)LEN and AllerGen). Allergy. 2008; 63 (86 suppl): 8–160.
5. Bousquet J, Schunemann HJ, Zuberbier T, et al.. Development and implementation of guidelines in allergic rhinitis
—an ARIA–GA2LEN paper. Allergy. 2010; 65 (10): 1212–21.
6. British Aerobiology Federation. Airborne Pollens and Spores: A Guide to Trapping and Counting. 1st ed. 1995. p. 22–40.
7. Brozek JL, Bousquet J, Baena-Cagnani CE, et al.. Allergic Rhinitis
and its Impact on Asthma (ARIA) guidelines: 2010 revision. J Allergy Clin Immunol. 2010; 126 (3): 466–76.
8. Crystal-Peters J, Neslusan C, Crown WH, Torres A. Treating allergic rhinitis
in patients with comorbid asthma: the risk of asthma-related hospitalizations and emergency department visits. J Allergy Clin Immunol. 2002; 109 (1): 57–62.
9. Dijkstra HP, Robson-Ansley P. The prevalence and current opinion of treatment of allergic rhinitis
in elite athletes
. Curr Opin Allergy Clin Immunol. 2011; 11 (2): 103–8.
11. Hartgerink-Lutgens I, Vermeeren A, Vuurman E, Kremer B. Disturbed cognitive functions after nasal provocation in patients with seasonal allergic rhinitis
. Clin Exp Allergy. 2009; 39 (4): 500–8.
12. Helenius I, Haahtela T. Allergy and asthma in elite summer sport athletes
. J Allergy Clin Immunol. 2000; 106 (3): 444–52.
13. Helenius IJ, Tikkanen HO, 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 (5): 646–52.
14. Katelaris CH, Carrozzi FM, Burke TV. Allergic rhinoconjunctivitis in elite athletes
: optimal management for quality of life and performance. Sports Med. 2003; 33 (6): 401–6.
15. Katelaris CH, Carrozzi FM, Burke TV, Byth K. A springtime Olympics demands special consideration for allergic athletes
. J Allergy Clin Immunol. 2000; 106 (2): 260–6.
16. Lakier Smith L. Overtraining, excessive exercise, and altered immunity: is this a T helper-1 versus T helper-2 lymphocyte response? Sports Med. 2003; 33 (5): 347–64.
17. Lumme A, Haahtela T, Ounap J, et al.. Airway inflammation, bronchial hyperresponsiveness and asthma in elite ice hockey players. Eur Respir J. 2003; 22 (1): 113–7.
18. McFadden ER Jr, Pichurko BM, Bowman HF, et al.. Thermal mapping of the airways in humans. J Appl Physiol. 1985; 58 (2): 564–70.
19. Nieman DC. Exercise, upper respiratory tract infection
, and the immune system. Med Sci Sports Exerc. 1994; 26 (2): 128–39.
20. Nieman DC, Johanssen LM, Lee JW. Infectious episodes in runners before and after a roadrace. J Sports Med Phys Fitness. 1989; 29 (3): 289–96.
21. Nieman DC, Miller AR, Henson DA, et al.. Effect of high- versus moderate-intensity exercise on lymphocyte subpopulations and proliferative response. Int J Sports Med. 1994; 15 (4): 199–206.
22. Peters EM, Bateman ED. Ultramarathon running and upper respiratory tract infections. An epidemiological survey. S Afr Med J. 1983; 64 (15): 582–4.
23. Reid VL, Gleeson M, Williams N, Clancy RL. Clinical investigation of athletes
with persistent fatigue and/or recurrent infections. Br J Sports Med. 2004; 38 (1): 42–5.
24. Selgrade MK, Plopper CG, Gilmour MI, Conolly RB, Foos BS. Assessing the health effects and risks associated with children’s inhalation exposures—asthma and allergy. J Toxicol Environ Health A. 2008; 71 (3): 196–207.
25. Spence L, Brown WJ, Pyne DB, et al.. Incidence, etiology, and symptomatology of upper respiratory illness in elite athletes
. Med Sci Sports Exerc. 2007; 39 (4): 577–86.
26. Steensberg A, Toft AD, Bruunsgaard H, Sandmand M, Halkjaer-Kristensen J, Pedersen BK. Strenuous exercise decreases the percentage of type 1 T cells in the circulation. J Appl Physiol. 2001; 91 (4): 1708–12.
27. Sunyer J, Jarvis D, Pekkanen J, et al.. Geographic variations in the effect of atopy on asthma in the European Community Respiratory Health Study. J Allergy Clin Immunol. 2004; 114 (5): 1033–9.
28. Walsh NP, Gleeson M, Shephard RJ, et al.. Position statement. Part one: immune function and exercise. Exerc Immunol Rev. 2011; 17: 6–63.
29. Young T, Finn L, Kim H. Nasal obstruction as a risk factor for sleep-disordered breathing. The University of Wisconsin Sleep and Respiratory Research Group. J Allergy Clin Immunol. 1997; 99 (2): S757–62.
Keywords:©2012The American College of Sports Medicine
ALLERGIC RHINITIS; ATHLETES; EXERCISE-INDUCED ASTHMA; INHALANT ALLERGENS; UPPER RESPIRATORY TRACT INFECTION