Introduction
Rhinitis in athletes has frequently been studied in combination with asthma. Reported prevalence varies widely, ranging from 27 to 74 per cent.Reference Bougault, Turmel and Boulet 1 – Reference Surda, Walker, Putala and Siarnik 3 The impact of exercise on the paracrine and secretory functions of nasal mucosa is less well established. Moreover, repeated exposure to allergens and irritants such as those encountered in the exercise environment may cause changes leading to mucosal damage. The phenomenon of exercise-induced rhinorrhoea – ‘runner's nose’ – was described in 1979.Reference Saketkhoo, Kaplan and Sackner 4 Nearly 20 years elapsed before the technology was available to accurately analyse nasal secretions, and, by proxy, the secretory function of nasal mucosa.
The aetiology and nature of the nasal changes induced by exercise depends on several factors. The acute effects of exercise on the nose have been well delineated: vasoconstriction of the capacitance vessels results in a measurable increase in nasal volume.Reference Dallimore and Eccles 5 In aerobic exercise, nasal minute ventilation increases absolutely, but proportionately contributes less than at rest, as the low resistance oral airway is used preferentially.Reference Niinimaa, Cole, Mintz and Shephard 6 Many of the environments and endeavours in which athletes are immersed can potentially harm nasal mucosa. For example, an exercise that takes place in cold air (skiers, snowboarders, ice hockey) or in chlorinated water (swimmers, divers, water polo) subjects the nasal mucosa to local irritants. Aerobic exercise that takes place outdoors may result in inhalation of above-average volumes of aeroallergens, nitrous oxide or pollution because of the increased minute ventilation required to sustain activity.Reference Bonini, Bonini, Bousquet, Brusasco, Canonica and Carlsen 7 – Reference Walker, Surda, Rossiter and Little 9
The induction of nasal symptoms in swimmers is also determined by age and the hours spent in a swimming pool. When swimming up to 30 hours per week, swimmers inhale a large amount of air floating just above the water that is disinfected with either chlorine gas or hypochlorite liquid, and therefore elite athletes may be more affected than others.Reference Bernard, Nickmilder, Voisin and Sardella 10 However, there is a lack of evidence directly comparing the elite athlete to the recreational counterpart. As stated previously, age may be crucial factor, and children are more susceptible to chronic changes: a Belgian schoolchildren study showed that early swimming in chlorinated pools can cause permanent alterations of lower airway epithelium, predisposing them to allergic diseases.Reference Bernard, Nickmilder, Voisin and Sardella 10
This systematic review aimed to examine the effect of exercise on the nasal mucosa in elite athletes.
Materials and methods
We sought to investigate nasal changes associated with exercise in athletes. The inclusion criteria were: studies that evaluated human participants aged at least 12 years, presented in articles that included an abstract, and which were published in the English language between January 1980 and October 2015. We defined an elite athlete as a person who trains more than 6 hours per week. We classified sports into three categories which represent their different environments: land, water and cold air.
Our review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (‘PRISMA’) guidelines for reporting. A medical information specialist (JL) performed a systematic search of Medline (Ovid), Embase (Ovid) and the non-Medline subset of PubMed, from inception to 8th March 2016, to identify studies on rhinitis in athletes. Both controlled vocabulary (including Medical Subject Heading terms) and words in titles, abstracts and author keywords were searched. We excluded studies indexed with animals, but not indexed with humans, conference abstracts and case reports, and studies with ‘trauma’ or ‘concussion’ in the title. The search consisted of two concepts: athletes (including all kinds of athletic sports, swimming and high-intensity training) and rhinitis (including synonyms for rhinitis, symptoms, underlying mechanisms of rhinitis and tests for rhinitis). We cross-checked the reference lists and the citing articles of the identified relevant papers, and adapted the search in case of additional relevant studies. The bibliographic records retrieved were imported and de-duplicated using Endnote. The entire Medline search is shown in Appendix 1.
Studies meeting the inclusion criteria were assessed in terms of quality using the Preferred Reporting Items for Systematic Reviews and Meta-Analysis and the Assessing the Methodological Quality of Systematic Reviews (‘AMSTAR’) checklist as guidelines. The studies that did not discuss the subject of interest were excluded. No minimum was set on the number of study participants.
Data collection
All abstracts and full-text articles were reviewed by two researchers (PS and AW); only case–control and cohort study designs were included (case reports, case series, other non-cohort study designs and non-systematic reviews were excluded).
Information obtained from each article included authors, year of publication, number of participants, number of participants per category (land, water, cold air), study design, outcomes and nasal changes associated with exercise in athletes. For each study, the following variables were recorded: changes in objective airway measurements, changes in smell and/or mucociliary clearance, and mucosal changes. Findings were tabulated and descriptively analysed, listing outcomes measured.
Results
A systematic review of titles, abstracts and full-text publications was performed, as described in Figure 1. Of the 373 identified unique articles, a total of 8 studies satisfied the criteria for this review.Reference Bougault, Turmel and Boulet 1 , Reference Clearie, Williamson, Vaidyanathan, Short, Goudie and Burns 11 – Reference Muns 17 The characteristics are described in Tables I–III. Demographic details and efforts to control confounding variables were incompletely reported. Three cohort and five case–control studies were included. The final group contained six studies examining changes in objective airway measurements, three that evaluated changes in smell and mucociliary clearance, and five that investigated mucosal changes.
Fig. 1 Flow chart of data extraction and analysis.
Table I Objective airway measurement changes
H = hours; PNIF = peak nasal inspiratory flowmetry; min = minutes
Table II Smell and mucociliary clearance changes
H = hours
Table III Mucosal changes
H = hours; NO = nitric oxide; min = minutes
In the eight studies included in this review, changes in objective measurements were reported in: mucociliary transport time, peak nasal inspiratory flowmetry, acoustic rhinometry, nasal cytology and ciliary beat frequency (Tables I–III). Several authors studied the objective changes in nasal patency assessed by peak nasal inspiratory flowmetry. There was no statistical difference in measurements before and after the exercise, or in comparison with healthy controls.Reference Bougault, Turmel and Boulet 1 , Reference Clearie, Williamson, Vaidyanathan, Short, Goudie and Burns 11 – Reference Ottaviano, Staffieri, Stritoni, Ermolao, Coles and Zaccaria 13 However, acoustic rhinometry showed a decreased cross-sectional area in one study in response to acute exercise in skiers, compared to swimmers, runners and boxers.Reference Passali, Damiani, Passali, Passali and Bellussi 14 Unfortunately, that study did not include a healthy control group for comparison.
Mucociliary clearance was judged by three articles as impaired, based on mucociliary transport time, with normalisation to baseline over several days after the race.Reference Ottaviano, Staffieri, Stritoni, Ermolao, Coles and Zaccaria 13 , Reference Muns, Singer, Wolf and Rubinstein 15 , Reference Passali 18
Two studies found increased neutrophil levels after exercise in swimmers and runners.Reference Gelardi, Ventura, Fiorella, Fiorella, Russo and Candreva 16 , Reference Muns 17 Furthermore, Muns also reported that the capacity of phagocytes to ingest Escherichia coli was significantly suppressed immediately after the race.Reference Muns 17 These findings seem to be reversible. The cellular changes in swimmers described by Gelardi et al. improved 1 month after the use of a nose clip, and the acute post-race changes in runners (neutrophil count and phagocytic activity) normalised 3 days after the running race.Reference Gelardi, Ventura, Fiorella, Fiorella, Russo and Candreva 16
Two studies examined changes in nasal nitric oxide in swimmers before and after exercise.Reference Clearie, Williamson, Vaidyanathan, Short, Goudie and Burns 11 , Reference Alves, Martins, Delgado, Fonseca and Moreira 12 The measurements showed no significant difference.
Discussion
This is the first systematic review to explore the effect of rhinitis on the nasal airway.
Main results summary
This systematic review of the literature identified eight studies that fulfilled the inclusion criteria. Nasal mucosa changes triggered by sport activity can be reflected in predominant neutrophilic infiltration, with reduced phagocytic activity, deterioration of olfaction, reduced ciliary beat frequency and prolonged mucociliary transport time.Reference Ottaviano, Staffieri, Stritoni, Ermolao, Coles and Zaccaria 13 , Reference Passali, Damiani, Passali, Passali and Bellussi 14 , Reference Gelardi, Ventura, Fiorella, Fiorella, Russo and Candreva 16 , Reference Muns 17 These changes can be chronic or acutely related to a strenuous training exercise, and depend on the different sport activity and environment.
Mucociliary transport time was found to be prolonged in swimmers, which can be attributed to chlorine irritation.Reference Ottaviano, Staffieri, Stritoni, Ermolao, Coles and Zaccaria 13 , Reference Passali, Damiani, Passali, Passali and Bellussi 14 Deterioration of mucociliary transport and reduced ciliary beat frequency can also be observed in runners after a 20 km race. Nasal lavage examination findings obtained immediately after a competition showed an increased number of neutrophils with reduced phagocytic activity.Reference Muns, Singer, Wolf and Rubinstein 15 , Reference Muns 17
Acute nasal mucosa changes induced by strenuous exercise in runners recovered to the baseline level within 3 days after the competition. In elite swimmers, a decrease in neutrophilic infiltration and improvement of clinical symptoms were described after 2 weeks of training cessation or 30 days after the use of a nasal clip.Reference Gelardi, Ventura, Fiorella, Fiorella, Russo and Candreva 16
Several authors studied changes in nasal patency using peak nasal inspiratory flowmetry before and after exercise. Interestingly, there was no significant difference observed.Reference Clearie, Williamson, Vaidyanathan, Short, Goudie and Burns 11 – Reference Ottaviano, Staffieri, Stritoni, Ermolao, Coles and Zaccaria 13 , Reference Gelardi, Ventura, Fiorella, Fiorella, Russo and Candreva 16
Quality of evidence
The overall quality of evidence in the papers investigating nasal changes associated with exercise was low to moderate. The main reason why the screened articles did not meet the inclusion criteria was poor reporting of methods, such as unclear participant age and numbers of training hours per week.
Limitations
One of the major aims of the review was to distinguish between the physiological and pathological responses to exercise. Confounding was reduced in five studies that included a healthy control group. All studies were limited to a relatively small sample size.
Comparison with other reviews
No specific review articles of nasal changes associated with exercise in athletes were identified (in the peer-reviewed journals). Many of the available reviews were part of a case–control or cohort study. Methodology and search strategy were often not discussed.
Implications for clinical practice
The magnitude of rhinitis and associated nasal changes in athletes may be greater than it seems. The number of registered swimmers, who seem to be the most affected, exceeds 100 000 in Australia, 19 and the USA Swimming national governing body counts 404 448 members. 20 The observed cytology changes in swimmers and runners may impair the defence barrier of the upper respiratory tract and contribute to the increased susceptibility to upper respiratory tract infection.Reference Muns 17
This review demonstrated that most of the nasal changes return to a baseline level after a few weeks of training cessation. However, there is emerging evidence that chronic exposure, as seen in swimmers, can cause permanent alterations of lower airway epithelium, predisposing the individuals to asthma and allergic diseases.Reference Bernard, Nickmilder, Voisin and Sardella 10 The presence of rhinitic symptoms in elite athletes is common. A lack of recognition may lead to under-treatment of this condition.
Implications for research
All articles examining the changes in objective airway measurements occurring shortly after a training session showed no improvement. This finding might be biased by a physiological improvement of the nasal efficiency during exercise because of an increase in nasal sympathetic tone, causing constriction of nasal blood vessels through α-adrenergic receptor stimulation. However, repeated exposure to allergens and irritants, such as those encountered in the exercise environment, may cause changes, leading to mucosal damage and subsequently to mucosal oedema. Therefore, future research is needed to objectively evaluate a reduction in the nasal airway in the evening or during daytime activities.Reference Gelardi, Ventura, Fiorella, Fiorella, Russo and Candreva 16 , Reference Bernard, Nickmilder and Dumont 21
Furthermore, there is a well-described negative impact of rhinitis on quality of life in the general population, which in athletes might affect training and performance. This systematic search suggests that studies examining the association between rhinitis, performance and quality of life are lacking.
Conclusion
There is no evidence in the existing literature to indicate a reduction in nasal airway induced by exercise. Olfaction and mucociliary transport time are affected in swimmers, which are likely to be associated with chlorine irritation, and which resolve with cessation of the training. Short-term strenuous exercise may trigger changes in cytology and prolonged mucociliary transport time, which also resolves quickly with rest. For the purposes of future research, it is important to reliably differentiate between physiological changes in the nasal airway during exercise and abnormal changes induced by the sporting event or environment.
Appendix 1. Entire medline search
