• bronchial challenge;
  • exercise-induced asthma;
  • nitric oxide;
  • rhinitis


  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. References

To cite this article: Clearie KL, Vaidyanathan S, Williamson PA, Goudie A, Short P, Schembri S, Lipworth BJ. Effects of chlorine and exercise on the unified airway in adolescent elite Scottish swimmers.


Background:  Chlorine metabolites and high training load may produce exercise-induced bronchospasm (EIB) in elite swimmers. The aim of this study was to assess the combined effects of chlorine and exercise on the unified airway of adolescent elite swimmers.

Methods:  The Scottish Midlands District squad were assessed during an indoor pool session at the National Swimming Academy. Athletes trained at least 8 h per week. Subjects underwent tidal (TNO) and nasal (NNO) exhaled NO and peak nasal inspiratory flow (PNIF) pre and post a 2 h session. A physiological exercise challenge assessed EIB in n = 36 swimmers (>10% fall in forced expiratory volume in 1 s (FEV1)).

Results:  Combined and free chlorine levels (mg/l) were 1.66 and 0.3 respectively. n = 36 swimmers (mean age 13.3 years) were assessed: n = 8 (22%) had known asthma; n = 13 (36%) had a positive physiological challenge; 18 (50%) complained of symptoms suggestive of EIB. n = 10/28 (36%) who did not have asthma were found to have a positive exercise challenge. There was no significant association between reported exercise symptoms and positive exercise test. There was no significant change in TNO or NNO for pre vs postexposure, irrespective of asthma diagnosis or AHR. n = 15 (42%) swimmers complained of worsening nasal symptoms postexposure, but only n = 7 (14%) had a demonstrable fall in PNIF (mean 33 l/min). No significant association was found between PNIF and symptoms.

Conclusions:  Combined exposure to chlorine and exercise did not affect surrogate markers of inflammation in the unified airway. There was a high prevalence of undiagnosed EIB.

Elite swimmers have higher rates of rhinoconjunctivitis and exercise-induced bronchospasm (EIB) compared with any other groups of athletes (1, 2). Proposed mechanisms include a combination of chronic exposure to toxic chlorine metabolites, and high ventilatory rates leading to osmotic degranulation of mast cells and subsequent bronchoconstriction (3). In adult elite swimmers, significantly higher levels of airway inflammatory cells have been demonstrated compared with healthy controls. This reverts back to normal following long-term cessation of the sport (4). There is a paucity of data on the prevalence of rhinoconjunctivitis and exercise-induced bronchoconstriction in adolescent elite swimmers. This is of particular importance as rhinoconjunctivitis has been shown to be an independent risk factor for developing asthma (5). Indeed rhinitis and asthma are considered to be part of the same disease continuum, the ‘unified airway’ (6). We therefore conducted a pilot study to assess the combined effects of chlorine and exercise on the unified airway of adolescent elite swimmers, including estimating the prevalence of rhinoconjunctivitis and EIB.


  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. References

Participants and study design

The Scottish Midland District swimming squad (36 swimmers) were assessed during a 2 h training session. All swimmers underwent exhaled tidal (TNO) and nasal (NNO) nitric oxide measurement peak nasal inspiratory flow rate (PNIF), and forced expiratory volume in 1 s (FEV1) before and after swimming. A sport-specific exercise test was carried out during an intensive aerobic set. All swimmers completed a health questionnaire. Swimmers were asked to withhold anti-histamines, leukotriene receptor antagonists (LRTAs), nasal steroid sprays, and long acting β2-agonists (LABAs) for 1 week before the training session. Inhaled cortico-steroid inhalers could be taken as normal. Participants were asked to refrain from taking short acting β2-agonists (SABAs) 12 h before the session. This study was approved by the local ethics committee (REC ref: 09/S1402/6) and all participants gave written informed consent.


Nitric oxide (NO)

All participants underwent measurement of exhaled tidal nitric oxide (TNO) using a portable MINO (NIOX MINO® Airway Inflammation Monitor; Aerocrine AB, Solna, Sweden). A single reading was obtained in accordance with manufacturer’s guidelines. Nasal exhaled nitric oxide was measured using an adapted MINO device, as previously described (7).

Sport-specific field-based exercise challenge

The swimmers performed a sport-specific field-based exercise challenge following a low intensity warm up. Swimmers were required to maintain >80% maximum heart rate (220-age) for at least 8 min in order to optimally provoke EIB. Heart rate was measured objectively using pulse oximetry (M-pulse, Merlin Medical, Gwent, UK). FEV1 (forced expiratory volume in 1 s) was measured using a Piko-6® portable spirometer (Ferraris Respiratory, Hertford, UK). Heart rate and FEV1 were measured at baseline, immediately following challenge and at 5 and 10 min during recovery. A positive challenge was defined as a fall in FEV1 of ≥10%.

Peak nasal inspiratory flow

Peak nasal inspiratory flow (PNIF) was measured using the In-Check® PNIF meter (Clement Clarke International Ltd, Harlow, UK). After horizontal positioning and restoration to zero, participants forcefully inhaled through their nose from residual volume to total lung capacity. The best of three measurements was taken.

Health questionnaire

A modified version of a questionnaire previously used in studies on elite athletes was used to assess the presence of exercise-induced symptoms (8). Symptoms of chlorine-induced rhinitis were assessed using a visual analogue scale. Atopy was defined as a history of intermittent rhinoconjunctivis (in accordance with current ARIA definitions) and/or a positive skin prick test or/IgE specific RAST test within the last 2 years.

Statistical analysis

spss version 15 (SPSS Inc., Chicago, IL, USA) was used to perform the statistical analysis. Non-Gaussian data were log transformed prior to analysis. Normalized data were assessed using paired t-tests. A P-value of less than 0.05 (two-tailed) was considered significant. As this was a pilot observational study, no formal power calculation was used.


  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. References

Combined and free chlorine levels on the day were 1.66 and 0.3 mg/l, respectively. Baseline characteristics are described in Table 1. Complete baseline data was available on 31/36 swimmers. Eight swimmers (22%) had known asthma. Eighteen (50%) had rhinitis according to the 2008 ARIA guidelines (11 = intermittent rhinitis, 7 = persistent rhinitis). There were no significant differences in TNO or NNO pre vs postexposure: mean (95% CI) for TNO 17.9 (13.5–23.5) ppb vs 17.0 (12.8–22.5) ppb (P = 0.12); NNO 47.5 (36.3–62.1) ppb vs 45.4 (34.0–60.6) ppb, respectively (= 0.71) (Table 2). Mean PNIF increased from 124.4 l/min (107.8–143.5) vs 136 l/min (121.3–152.5): (= 0.04). Baseline TNO readings in asthmatics and nonasthmatics were 35.7 (8.57) and 18.5 (3.01), respectively.

Table 1.   Lower airway outcomes
Study no.Age/sexKnown asthmaAsthma meds† FEV1% change FEV1Baseline TNO (ppb)Change in TNO (ppb)Symptoms suggestive of EIB
  1. †L = Leukotriene receptor antagonist, A = antihistamine, S = inhaled corticosteroid.

  2. ‡Maximal % change in FEV1 observed during exercise challenge.

 116/MN 6.28−29.022+1Y
 316/MN 5.57−2.311−2Y
 416/MY 5.27−23.317+1N
 715/FN 4.26−24.615−1N
 815/FN 4.27−7.355+17N
 913/FN 3.44−4.9NANAN
1118/MN 3.51−7.7NANAY
1215/MN 6.32−32.816+1N
1315/MN 4.56−11.690N
1415/FN 3.83−14.112−2N
1512/FN 3.08+7.5220N
1612/FN 2.70+21.9NANAY
1713/FN 3.26−5.232−11Y
1812/FN 3.86−14.213NAN
2011/MN 3.74−0.813+5Y
2114/FN 3.11+7.16−1Y
2212/FN 3.37−4.210−2N
2313/FN 3.44−17.217−5Y
2411/MN 2.85−5.658−23Y
2612/MN 2.50−0.86−1N
2711/MN 4.50−30.410−2Y
2812/MN 3.19−9.19+6Y
2912/MN 3.31−3.3120N
3012/MN 2.32−3.450N
3111/FN 2.64+1.513−2N
3211/FN 3.44−11.611−1Y
3411/FN 3.15−10.510−2N
3512/FN 2.88+1.024−2N
3611/FN 3.16−7.052−1N
Mean (SEM)13.3 (0.38) 17M : 18F8 (22%) 3.73 (0.17)−7.6 (1.96)22.28 (3.20)1.1 (1.10)18 (50%)
Table 2.   Upper airway outcomes and training
Study no.Known rhinitis†% fall PNIFChange in NNO (ppb)History of atopyDecrease in nasal visual analogue score postexposureTraining (h/week)Training (years)
  1. †I = intermittent, P = persistent, N = none.

Mean (SEM)I = 11(31%) P = 7(19%) N = 18(50%)+12.3 (4.88)−1.5 (5.85)14 (39%)15 (42%)10.2 (0.5)5.3 (0.5)

Thirteen out of thirty-six (36%) of swimmers had a positive exercise challenge. Ten out of thirteen (77%) of these were not previously known to asthmatic. Three of eight (38%) of asthmatic swimmers had a positive challenge. During the challenge swimmers achieved a mean (SEM) heart rate of 81.3% (1.5) maximum predicted.

Thirty-six percentage (13) had a positive exercise challenge. About 46% (6) of participants with a positive challenge were symptomatic, 54% (7) were asymptomatic. Forty-two percentage (15) swimmers complained of worsening nasal symptoms postswimming, but only 13% (2) had a demonstrable fall in PNIF (mean fall 33 l/min), 87% (13) had no change. Nine out of fifteen (60%) had a preexisting diagnosis of either intermittent or persistent rhinitis.


  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. References

This study aimed to assess the combined effects of chlorine and exercise on the unified airway of adolescent elite swimmers. We found no significant change in either tidal (TNO) or nasal (NNO) nitric oxide following a 2 h training session, which included a high intensity anaerobic set. Using linear regression analysis, this change in NO was not influenced by asthma, presence of EIB or history of atopy. Furthermore, there was no correlation between upper and lower airway nitric oxide (r = 0.12, P = 0.81). We elected to use exhaled nitric oxide as it is noninvasive, reproducible and easy to perform at the poolside. Exhaled nitric oxide is an established surrogate in asthma, which correlates closely with airway inflammation (9). It is also used as a surrogate marker of inflammatory diseases in the upper airway (10), enabling us to examine effects on the unified airway. Additionally, TNO has been shown to rise in elite runners following a marathon (11). The absence of any acute rise in TNO was therefore unexpected. Whilst forced vital manoeuvres are known to ‘washout’ TNO from the airways (12), there are no reports of exercise or hyperventilation decreasing TNO. Indeed, our results did not show any reduction postswimming. It is also conceivable that the short duration of exposure was not sufficient to induce NO synthase, however, TNO has previously been shown to be elevated during an osmotic challenge suggesting that there is rapid induction of this enzyme (13). We did not assess whether a late phase response was present in either the upper and lower airway. This is supported by anecdotal reports from swimmers who frequently complain of nasal congestion and symptoms, 4–6 h after training.

The significant increase observed in PNIF postswimming may not represent an improvement in inflammation, but paradoxically may signify a ‘nasal douche effect’. Saline irrigation is known to significantly improve nasal congestion through a combination of improved mucociliary clearance and reduction of mucosal oedema (14). Eighteen (50%) of swimmers had a preexisting diagnosis of rhinitis, which is in line previously reported rates (15). Rhinitis did not necessarily predict worsening of nasal symptoms postswimming, however, large scale epidemiological studies are needed to investigate this issue further.

As part of this study we carried out a standardised field-based exercise challenge. Traditional field based testing in which athletes perform a challenge using their primary exercise, is usually limited by an inability to standardise both the cardiovascular workload and environmental conditions (16). We therefore decided to use a standardised protocol based on the ATS (1999) guidelines for exercise challenge, using an objective measure of heart rate monitoring. In the current study, swimmers achieved an average heart rate of 81.3% of maximum, which was maintained for an average of 8 min.

We found a high prevalence (36%) of EIB in our cohort of adolescent elite swimmers. This is a unique finding, as previous figures are biased towards adult swimmers (17). Indeed, 77% of our swimmers with a positive exercise challenge were not previously known to be asthmatic. Moreover, only 46% of swimmers who were exercise-positive reported symptoms suggestive of EIB. The diagnosis of EIB based on symptoms alone, is known to be highly inaccurate (18). This suggests that solely testing symptomatic athletes is grossly insufficient. At elite level small changes in physiological reserve could potentially translate into tangible improvements in performance. More importantly, adolescent swimmers with undiagnosed EIB may not reach their full potential, preventing them from progressing to compete at adult level. We therefore feel that universal screening of all elite swimmers for EIB and rhinoconjunctivitis and should be advocated.

We recognize some limitations in our study. It could be argued that the nonintensive exercise preceding the challenge may have induced a refractory period in some swimmers, which may have led to an underestimate of the true prevalence of EIB. However, previous studies have shown that low intensity warm-ups to not induce refractoriness prior to challenge (19). Four out of five asthmatic swimmers with a negative exercise challenge were on inhaled corticosteroids, which may explain the low incidence of EIB in this group. Ideally, these would have been stopped; however, this would have interfered excessively with training. As expected TNO was elevated at baseline in asthmatics, but not in nonasthmatic swimmers. This is in keeping with previous studies. It is possible that the swimmers in this cohort were too young to develop major airway inflammatory changes. A larger study in a cohort of older more experienced adolescent swimmers would help eliminate this as a confounding factor. Whilst this study does not allow us to differentiate between the relative contributions of exercise and chlorine on the airway we felt it was important to study swimmers in a ‘real life’ situation.


  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. References

In conclusion, we found that a 2 h training session, including a high intensity anaerobic set, in a chlorinated indoor pool did not affect surrogate markers of inflammation in the unified airway. There was a high prevalence of undiagnosed EIB, highlighting the importance of screening of all elite swimmers for asthma.


  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. References

This study funded from Departmental funds of the Asthma and Allergy Research Group.


  1. Top of page
  2. Abstract
  3. Methods
  4. Results
  5. Discussion
  6. Conclusions
  7. Acknowledgments
  8. References
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