Twenty-three elite athletes (age: 20 ± 4.5 yr, height: 173 ± 8.7 cm, weight: 67 ± 9.9 kg, 14 men and 9 women) identified as EIA positive were selected as subjects and provided written informed consent to participate in this study. Experimental procedures were approved by the Institutional Review Board of the Sport Science and Technology Division of the United States Olympic Committee (USOC). Six subjects were Olympians, 10 others had participated on World Championship Teams and the remaining 7 were top developmental athletes. Subject sports were: biathlon (6), cross-country skiing (6), Nordic combined (3), short-track speed skating (5), and kayaking (3). Fifteen subjects were from outdoor cold-weather sport, five from cold-weather indoor sport, and three from paddling sport. The athletes were selected from a larger pool of approximately 160 athletes who were evaluated for the presence of EIA by using a sport/environment specific “field” exercise challenge (race or race simulation) in a prior study. All subjects selected for this study demonstrated postexercise challenge decrements in pulmonary function consistent with EIA. Seven subjects had been previously diagnosed with EIA as children, but none were currently using oral or inhaled medication before exercise or competition. Before the field exercise challenge pulmonary function tests (PFT), each subject completed a questionnaire for four common symptoms of EIA: coughing, wheezing, excessive mucus formation, and chest tightness/trouble breathing. An additional gender and sport matched subpopulation of 23 athletes from the EIA screened athlete pool with normal postexercise challenge spirometry were randomly selected to establish references for PFT normal cold weather athletes.
Our study consisted of two series of EIA evaluations. The first involved a sport-specific exercise challenge of either actual competition or simulated competition (FBC). Time duration ranged from approximately 1 min 20 s for speed skaters to over 1 h for cross-country skiers. Subjects who demonstrated postexercise PFT decrements consistent with EIA from this evaluation were asked to perform a second exercise challenge in the laboratory (LBC; 21°C, 60% relative humidity). This involved treadmill running for 8 min at a speed and elevation that elicited approximately 95% of peak heart rate (an exercise challenge that closely mimicked competition level intensity). The rational for this intensity was based on competition specificity and the superior fitness level of this elite athlete population. In addition, verbal communication with symptomatic athletes indicated that symptoms did not occur at lower exercise intensities (e.g., <90% maximal heart rate).
Standard spirometry evaluations were performed preexercise and at 5, 10, and 15 min postexercise challenge using a calibrated computerized 10 L rolling dry-seal spirometer (Model 2130, Sensormedics, Yorba Linda, CA). Before each exercise challenge, baseline spirometry was performed by obtaining three consistent trials that involved the following procedure: 1) three normal tidal volume breaths; 2) maximal inhalation; 3) forced maximal exhalation; and 4) maximal inhalation. The best-of-three trials was used for analysis. The athletes performed preexercise baseline spirometry for FBC before any warm-up. After baseline spirometry was obtained, the athletes followed their usual warm-up schedule, completed their competition, and reported for postexercise pulmonary function tests (PFT). This procedure was the same for LBC except that no warm-up was done before the exercise challenge. Postexercise PFT were done at 5, 10, and 15 min post exercise challenge for both FBC and LBC. Pulmonary function decrements were determined by subtracting each postexercise value of FVC, FEV1, FEF25–75%, and PEF from best-of-three preexercise baseline values, dividing by baseline values and multiplying by 100. Decrements of greater than 10% in FEV1, and/or 15% in FEF25–75%, and/or 10% in PEF from baseline values were considered as positive indications of airway flow restriction. Nineteen of the 23 subjects demonstrated decrements in FEV1 greater than 10%. The remaining four subjects were FEV1 compromised by 8.7 ± 0.9% (outside of the −6.4% criteria established by our population of asymptomatics, see results), but values for FEF25–75% and PEF were consistent with EIA and exceeded the above established criteria, and were thus included in the study population.
Statistical comparisons between field and laboratory exercise challenge based spirometry were made by ANOVA. Pearson product moment correlations were used to evaluate relationships between pulmonary function deficits. For all statistical comparisons, the level of significance was set as P < 0.05.
Table 1 lists self-reported symptoms that occurred during or after high exertion exercise. Twenty-one (91%) of 23 PFT+ athletes reported at least one symptom, whereas 11 (48%) of 23 PFT normal athletes reported at least one symptom (P < 0.05). Eighteen (78%) PFT+ athletes and 8 (35%) PFT-normal athletes reported two or more symptoms (P < 0.05). For the PFT+ athletes, a postrace cough/hack was the most prevalent symptom reported, followed by excess mucus, chest constriction, and wheezing and was significantly higher than other symptoms (P < 0.05). For PFT normal athletes, the post race cough/hack was the most reported symptom, followed by chest constriction, wheezing and excess mucus. The PFT positive group reported more than twice as many symptoms as the PFT normal group.
Table 2 provides baseline spirometry values for FBC, LBC, and for 23 PFT normal controls. As expected for this elite athlete population, mean values were above predicted values. No group or gender differences for any pulmonary function variables (as percent of predicted value) were noted. Four men and 4 women recorded baseline values below 100% predicted for at least one PFT variable (∼35% of the PFT+ population). Of those, two men and one woman (∼13% of the study population) had been previously diagnosed with asthma as children but did not use medication. PFT values for these eight were 102 ± 9.6, 101 ± 5.7, 96 ± 10.6, and 90 ± 15.4 for FVC, FEV1, FEF25–75%, and PEF, respectively.
Twenty-three gender and sport matched PFT normal controls who demonstrated no differences between pre- and post-FBC pulmonary function test values were used to determine a PFT reference range for an elite cold weather athlete population (Table 3). The mean maximal exercise induced change after FBC (in FVC, FEV1, FEF25–75%, and PEF) minus 2 SD was established as the lower limit reference range (Table 3). FEV1 and FEF25–75% lower limits determined with this group were less rigorous than the previously established cut-off criteria of 10–20% for FEV1 (1,2,4,7,27,36) and 15–25% for FEF25–75% (1,19).
Figure 1 shows post-FBC pulmonary functions of the study population grouped according to FBC exercise duration, <2 min (I), 6–7 min (II), and >25 min (III). No significant differences existed between groups for any pulmonary function at any time point.
Eighteen (78%) of the 23 post-FBC PFT positive subjects had normal spirometry post-LBC. Figure 2 depicts pulmonary function decrements from FBC and LBC for those 18 subjects. Significant differences between FBC and LBC pulmonary functions were apparent for all values (P < 0.05) except 10 and 15 min FVC and 15 min PEF. For FBC, 5 and 10 min FVC decrements were significantly greater than 15 min FVC (P < 0.05), whereas 10 min FEV1 and FEF 25–75% decrements were significantly greater than 15 min values (P < 0.05) but not different than those at 5 min. No differences were apparent between PEF decrements for FBC. For LBC, no differences between values at 5, 10, and 15 min postexercise were apparent for FVC, FEV1, or PEF, but 5 min was different than 10 and 15 min FEF25–75% post exercise values (P < 0.05).
Of the five FBC PFT positive athletes who demonstrated post LBC pulmonary decrements consistent with EIA positive criteria, no differences were evident between FBC and LBC values at any time point. No significant differences existed for postexercise challenge pulmonary decrements between time points for FVC, FEV1, FEF25–75%, or PEF (Fig. 3).
It is generally accepted that inhaling cold dry air at high ventilation rates causes EIA. Never the less, many authors (2,5,9,16,19,21,28) recommend that pulmonary function testing be performed in the laboratory environment using an exercise challenge with an intensity at or below lactate threshold (50% to 85% of maximal aerobic capacity) and a duration of 4–8 min. The rational for this intensity level is based on the assumption that catecholamine release at higher intensities may produce bronchodilation, resulting in false negative diagnoses. However, Warren et al. (36) states that withdrawal of vagal tone and not circulating catecholamines is responsible for bronchodilation during exercise. The recommended test duration is primarily based on studies done with asthmatic children (9) or a nonelite athletic population (2). These procedures may not apply to the elite athlete population.
In this study, we examined the efficacy of sport/environment-specific field based exercise challenge of varying duration (but at maximal effort specific to the duration) compared to a standardized laboratory based exercise challenge for EIA diagnosis in elite cold weather athletes. “Field” evaluations were done in conjunction with actual competitions (e.g., U.S. Olympic Trials, World Cup competition) or mock competitions specific to each athlete’s sport. Laboratory evaluations were done at a specific duration (8 min) and intensity (≥95% of maximal heart rate) in controlled environmental conditions (22°C, 60% RH).
The findings of our study are critical to effective diagnosis of EIA in the elite cold weather athlete. We demonstrated that resting pulmonary functions of this PFT positive population are 10–20% above predicted normative values for the nonathlete and are not different from those of PFT normal elite cold weather athletes. We have established a lower limit reference range (MN –2 SD) for postexercise pulmonary function variables from a subpopulation of PFT normal elite cold weather athletes which we believe provides appropriate cut-off criteria for these athletes. Furthermore, these values agree with other reference ranges determined in elite runners (14). Moreover, we found that among this population, duration of the exercise perturbation (1.5 min to ∼1 h) is not as important as exercise intensity and environmental condition. We have clearly demonstrated that cold dry air and near maximal exercise intensity are critical components of the exercise challenge for EIA evaluation. Our data suggests that the laboratory environment, even at race pace intensity, does not provide appropriate conditions to assess cold weather athletes for EIA and will yield a high percentage of “false negatives” (>78%).
The questionnaire responses from the limited number of subjects (N = 46) in our study suggests that the majority of athletes who are PFT positive will report symptoms (91%); however, 48% of those athletes who have normal PFT will also report symptoms. This suggests that diagnosis based upon reported symptoms without pulmonary function testing may result in about one third of the symptom reporting population being treated unnecessarily. Other survey data on Nordic skiers (17) show that about 39% will report symptoms consistent with EIA. In the study by Rice et al. (25), intercollegiate athletes were referred for pulmonary function tests based on a reported medical history consistent with EIA. Among the 41 referred athletes in that study (25), 46% were positive for EIA based on a greater than 10% drop in FEV1. This number was substantially lower than we found in this study with elite cold weather athletes where 66% (21 of 32 subjects) of those who reported at least one symptom were PFT positive for EIA. This discrepancy was probably the result of differences in the exercise challenge. An alternative explanation would be an effect of the small “N ” in our study. More recently, we (26) examined a larger population of elite athletes (N = 158) and found that 61% of PFT positive and 45% of PFT normal athletes reported symptoms (cough, excess mucus, chest constriction, and wheezing).
Baseline pulmonary functions of elite athletes.
Normative resting pulmonary function data for the elite athlete population is limited. In a study of 58 elite Finnish runners, Helenius et al. (14) found FVC and FEV1 to approximate 100% predicted values, whereas PEF was 110% predicted. In our study, no difference in percent predicted baseline values was noted between FVC, FEV1, FEF25–75%, or PEF, and all criterion variables were between 109% and 123% of predicted, independent of gender or broncho-responsiveness. In support of this finding, Helenius et al. (13) examined 32 nonasthmatic Finnish runners and found no difference in preexercise FEV1 (expressed as percent predicted) between nonatopic and atopic subjects. Heir and Oseid (11) reported values for FVC, FEV1, FEF25%−75%, and PEF for male Norwegian cross-country skiers that were similar to our values. Baseline spirometry in our study, or in the above cited studies (11,13,14,20), was not sufficient to provide insight to the tendency for bronchial hyperreactivity.
“Normal range” postexercise pulmonary functions for elite athletes.
Definitive EIA has been defined most frequently as a >10% postexercise fall in FEV1 or PEF (2,5,31,32). Others have suggested that a 15–20% postexercise reduction in FEV1 or PEF is appropriate (4,27). Further recommendations include decrements in FEF25–75% ranging from 15% to 25% to be representative of EIA (1,19). More recently a normal range for pulmonary functions has been established for elite runners by defining the lower limit of normal bronchial flow rate for symptom-free nonatopic runners as mean maximal exercise induced change in FEV1 and PEF minus 2 SD (13,14,33). Postexercise reductions in FEV1 and/or PEF of 6.5% and 17% (or greater), respectively, were considered abnormal (13,14,33). We have extended this concept to include a reference range for FVC, FEV1, FEF25–75%, and PEF for cold weather athletes. The lower limit (mean postexercise change from baseline spirometry minus 2 SD) for FEV1 of −6.4% in our PFT normal control group is in agreement with values for elite runners (13,14,33), but the PEF lower limit in our study was less than that defined by Tikkanen et al. (−12% vs –17%) (33). Still, these lower limit PEF values are greater than recommended cut-off criteria of 10% (2,8,27) and are probably a consequence of the effort dependency of PEF. In another study (35) (N = 87 nonasthmatic athletes) we found lower limit reference ranges for FEV1 and PEF to be −7.1% and 18.1%, respectively.
By using the lower limit for FEV1 (−6.4% postexercise decrement) defined by our control group, an additional four athletes would be considered probable for EIA from the laboratory exercise-challenge. This is still only 39% of those identified positive for definitive EIA (>10% decrement in FEV1) from the field based exercise-challenge. If the control group defined lower limit for PEF (−12%) was used in addition to FEV1 to evaluate the efficacy of LBC, the reliability improves to 57% of FBC identified EIA positive athletes. Of the 18 athletes PFT positive post-FBC who were PFT normal post-LBC, all were above the control group established lower limit of −13.5% for FEF25–75% post-LBC.
Field versus laboratory exercise challenge.
The remarkable differences in postexercise pulmonary functions between FBC and LBC provide strong evidence for the efficacy of a field based cold weather exercise challenge for EIA diagnosis. Control of the exercise challenge and ambient conditions (except for speed skaters) during FBC was limited, since testing was done according to the race or athlete’s training schedule. Baseline spirometry was done before any warm-up or prolonged exposure to cold air. However, after baseline spirometry was completed, the athlete assumed his/her usual prerace strategy, including a warm-up. Several authors (6,15,19,21,29) have suggested a “refractory period” whereby a warm-up before exercise decreases postexercise bronchoconstriction. However, this data may not apply to our elite athlete subject pool. Using FBC for broncho-provocation and allowing for a warm-up period of the athletes’ choice, we have reported EIA incidence consistent with others that evaluated cold weather athletes (17,20,24,38). These included, cross-country skiers using a methacholine challenge (33%) (17) and figure skaters using an on-ice high intensity protocol (30%−35%) (20,24). Therefore, our data does not support the existence of a refractory period that significantly attenuates broncho-responsiveness for elite cold weather athletes. This finding is in agreement with Beck et al. (3) who found no evidence of a refractory period during interval type exercise by EIA patients. Moreover, the LBC did not allow for a warm-up period, yet only 5 of 23 PFT positive athletes (post-FBC) were positive post-LBC.
Several studies (4,10,22,23,30) have examined bronchial responsiveness to temperature and humidity. Our study is the first to provide strong evidence that among elite winter athletes, cold dry ambient air and near maximal exercise effort are key to diagnosing bronchospasm while exercise duration is not important. Exercise intensity during FBC and LBC was at or near race pace for our subjects, whereas exercise duration during FBC ranged from 1.5 min to over 60 min and was held constant during LBC (8 min). FBC data (cf., Fig. 1) demonstrates that exercise challenge duration per se is unimportant in provoking broncho-responsiveness, implying that intensity (high ventilation rates and not total ventilation during the exercise) and ambient conditions determine the occurrence of bronchospasm. No difference in pulmonary response relative to FBC duration was found. We did not examine a control FBC group where intensity was manipulated, but verbal communication with our elite athlete subjects indicated that the onset of symptoms was coincident with cold ambient temperatures coupled with high intensity (above 90% maximum heart rate) exercise. Even in cold ambient temperatures, the athletes stated that they were typically asymptomatic unless exercise intensity was at or near race pace. The primary difference between FBC and LBC tests was ambient air temperature and humidity.
Medical questionnaires/interviews do not provide accurate information concerning the prevalence or severity of EIA. Likewise, a laboratory exercise challenge at room temperature and 50% relative humidity is not appropriate for assessment of EIA in elite cold weather athletes and it will likely result in false negative evaluations. Our results suggest that broncho-responsiveness is strongly related to high ventilation rates (not total ventilation during exercise) in cold-dry air, and time duration of the exercise challenge seems to be unimportant. The lower limit reference range established from our PFT normal control group implies that among elite cold weather athletes, previously recommended cut-off criteria for establishing EIA diagnosis may be too stringent. In conclusion, to appropriately diagnose EIB in elite cold weather athletes, we suggest a sport/environment specific field based exercise challenge using postexercise decrement lower limits of −8.3% for FVC, −6.5% for FEV1, −13.5% for FEF25–75%, and −12% for PEF.
This study was supported by the United States Olympic Committee.
The views, opinions, and findings contained in this report are those of the authors and should not be construed as an official United States Olympic Committee position.
The authors would like to express gratitude to the athletes participating in this study.
1. American Thoracic Society. Lung function testing: selection of reference values and interpretive strategies. Am. Rev. Respir. Dis. 144:1202–1218, 1991.
2. Anderson, S. D., N. M. Connolly, and S. Godfrey. Comparison of bronchoconstriction induced by cycling and running. Thorax 26:396–401, 1971.
3. Beck, K. C., K. P. Offord, and P. D. Scanlon. Bronchoconstriction occurring during exercise in asthmatic subjects. Am. J. Respir. Crit. Care Med. 149:352–375, 1994.
4. Deal, E. C., E. R. McFadden, Jr., R. H. Ingram, F. J. Breslin, and J. J. Jaeger. Airway responsiveness to cold air and hyperpnea in normal subjects and in those with hay fever and asthma. Am. Rev. Respir. Dis. 121:621–628, 1980.
5. Eggleston, P. A., R. R. Rosenthal, S. A. Anderson, et al. Guidelines for the methodology of exercise challenge testing of asthmatics. J. Allergy Clin. Immunol. 64:642–645, 1979.
6. Eggleston, P. A. Pathophysiology of exercise-induced asthma. Med. Sci. Sports Exerc. 18 (3):318–321, 1986.
7. Folinsbee, L. J. Does NO2
exposure increase airway responsiveness? Toxicol. Indust. Health 8:273–283, 1992.
8. Giesbrecht, G. G., and M. Younes. Exercise- and cold-induced asthma. Can. J. Appl. Physiol. 20:300–314, 1995.
9. Godfrey, S., M. Silverman, and S. D. Anderson. The use of the treadmill for assessing exercise-induced asthma and the effect of varying the severity and duration of exercise. Pediatrics 56:893–898, 1975.
10. Haas, F., N. Levin, S. Pasierski, M. Bishop, and K. Axen. Reduced hyperpnea-induced bronchospasm following repeated cold air challenge. J. Appl. Physiol. 61:210–214, 1986.
11. Heir, T., and S. Oseid. Self-reported asthma and exercise-induced asthma symptoms in high-level competitive cross-country skiers. Scand. J. Med. Sci. Sports 4:128–133, 1994.
12. Heir, T. Longitudinal variations in bronchial responsiveness in cross-country skiers and control subjects. Scand. J. Med. Sci. Sports 4:134–139, 1994.
13. Helenius, I. J., H. O. Tikkanen, and T. Haahtela. Exercise-induced bronchospasm at low temperature in elite runners. Thorax 51:628–629, 1996.
14. Helenius, I. J., H. O. Tikkanen, and T. Haahtela. Occurrence of exercise-induced bronchospasm in elite runners: dependence on atopy and exposure to cold air and pollen. Br. J. Sports Med. 32:125–129, 1998.
15. Katz, R. M. Prevention with and without the use of medications for exercise-induced asthma. Med. Sci. Sports Exerc. 18:331–333, 1986.
16. Konig, P. Exercise challenge: indications and techniques. Allergy Proc. 10:345–348, 1989.
17. Larsson, L., P. Hemmingsson, and G. Boethius. Self-reported obstructive airway symptoms are common in young cross-country skiers. Scand. J. Med. Sci. Sports. 4:124–127, 1994.
18. Lee, K., Y. Yanagisawa, J. D. Spengler, and S. Nakai. Carbon monoxide and nitrogen dioxide exposures in indoor ice skating rinks. J. Sports Sci. 12:279–283, 1994.
19. Mahler, D. A. Exercise-induced asthma. Med. Sci. Sports Exerc. 25:554–561, 1993.
20. Mannix, E. T., M. O. Farber, P. Palange, P. Galassetti, and F. Manfredi. Exercise-induced asthma in figure skaters. Chest 109:312–315, 1996.
21. McKenzie, D. C., S. L. McLuckie, and D. R. Stirling. The protective effects of continuous and interval exercise in athletes with exercise-induced asthma. Med. Sci. Sports Exerc. 26:951–956, 1994.
22. McLaughlin, F. J., and A. J. Dozor. Cold air inhalation challenge in the diagnosis of asthma in children. Pediatrics 72:503–509, 1983.
23. Noviski, N., E. Bar-Yishay, I. Gur, and S. Godfrey. Exercise intensity determines and climatic conditions modify the severity of exercise-induced asthma. Am. Rev. Respir. Dis. 136:592–594, 1987.
24. Provost-Craig, M. A., K. S. Arbour, D. C. Sestilli, J. J. Chabalko, and E. Ekinol. The incidence of exercise-induced bronchospasm in competitive figure skaters. J. Asthma 33:67–71, 1996.
25. Rice, S. G., C. W. Bierman, G. G. Shapiro, C. T. Furukawa, and W. E. Pierson. Identification of exercise-induced asthma among intercollegiate athletes. Ann. Allergy. 55:790–793, 1985.
26. Rundell, K. W., J. Im, R. L. Wilber, and H. R. Schmitz. Self-reported symptoms and exercise-induced asthma in the elite athlete. Med. Sci. Sports Exerc.
27. Rupp, N. T., M. F. Guill, and D. S. Brudno. Unrecognized exercise-induced bronchospasm in adolescent athletes. Am. J. Dis. Child. 146:941–944, 1992.
28. Rupp, N. T. Diagnosis and management of exercise-induced asthma. Phys. Sports Med. 24:77–87, 1996.
29. Schoeffel, R. E., S. D. Anderson, and R. E. C. Altounyan. Bronchial hyperreactivity in response to inhalation of ultrasonically nebulized solutions of distilled water and saline. Br. Med. J. 283:1285–1287, 1981.
30. Strauss, R. H., E. R. McFadden Jr, R. H. Ingram, and J. J. Jaeger. Enhancement of exercise-induced asthma by cold air. N. Engl. J. Med. 297:743–747, 1977.
31. Sterk, R. H., L. M. Fabbri, P. H. Quanjer, et al. Airway responsiveness. Standardized challenge testing with pharmacological, physical and sensitizing stimuli in adults. Eur. Respir. J. 6(Suppl. 16):53–83, 1993.
32. Tan, R. A., and S. L. Spector. Exercise-induced asthma. Sports Med. 25:1–6. 1998.
33. Tikkanen, H. O., I. Helenius, and T. Haahtela. Pulmonary functions of healthy elite runners in winter and pollen-season out door running test. Med. Sci. Sports Exerc. 28:(Suppl.)S90, 1996.
34. Tikkanen, H. O., and J. E. Peltonen. Asthma–cross-country skiing. Med. Sci. Sports Exerc. 31:(Suppl.)S99, 1999.
35. Voy, R. O. The U. S. Olympic Committee experience with exercise-induced bronchospasm, 1984. Med. Sci. Sports Exerc. 18:328–330, 1984.
36. Warren, J. B., S. J. Jennings, and T. J. H. Clark. Effect of adrenergic and vagal blockade on the normal human airway response to exercise. Clin. Sci. 66:79–85, 1984.
37. Weiler, J. M., T. Layton, and M. Hunt. Asthma in United States: Olympic athletes who participated in the 1996 summer games. J. Allergy Clin. Immunol. 102:722–726, 1998.
38. Wilber, R. L., K. W. Rundell, L. Szmedra, D. M. Jenkinson, J. Im, and S. D. Drake. Incidence of exercise-induced bronchospasm in Olympic winter sport athletes. Med. Sci. Sports Exerc
. (in press).