Abstract
Introduction
There is controversy over the effect that swimming in indoor pools can have on lung function and on bronchial inflammation parameters in asthma. The objective of this study was to observe the effect of recreational swimming in public indoor pools on changes in functional and inflammation parameters in patients with asthma.
Methodology
A prospective observational study, including asthmatics who were regular swimmers in indoor pools, and swimmers in the same pool without respiratory involvement. In both groups, baseline spirometry and measurement of fractional exhaled nitric oxide (FENO) were performed minutes before and after swimming. Additionally, the physicochemical parameters of the water were analyzed, including the disinfectant products used.
Results
Twenty five asthmatic swimmers (intermittent 53%; mild persistent 29.4%; moderate persistent 17.6%) and 50 healthy swimmers, mean age 40.8 ± 10.8 years, were included in the study. The mean immersion time was similar for both groups (asthma 31.9 ± 10, control 32.4 ± 12 min). The analysis of the water showed no differences in its composition or characteristics between the different pools. In asthmatics, FENO decreased significantly (28.7 ± 17.8 pre vs 23.7 ± 15.5 post, p < 0.001) after immersion, with no changes in the other functional parameters. In non-asthmatic subjects, increased vital capacity (p < 0.05) and volume expired in one second (p < 0.04) improved significantly after immersion, and FENO decreased (p < 0.01). No significant differences were found in functional or inflammation variables between the two groups after bathing.
Conclusion
In patients with intermittent and persistent asthma, no immediate functional or inflammatory alterations have been observed after bathing in legally regulated public swimming pools.
Keywords: Asthma, Pool, Swimming, Inflammation
Abstract
Introducción
Existe controversia sobre el efecto que la natación en piscinas cubiertas puede tener sobre la función pulmonar y los parámetros de inflamación bronquial en pacientes con asma bronquial. El objetivo de este estudio fue analizar el efecto de la natación recreativa en piscinas cubiertas públicas sobre los cambios en los parámetros funcionales y de inflamación en pacientes con asma bronquial.
Metodología
Estudio observacional prospectivo que incluyó a asmáticos que nadaban habitualmente en piscinas cubiertas y a nadadores en la misma piscina sin afectación respiratoria. En ambos grupos, se realizó una espirometría basal y la medición de la fracción de óxido nítrico exhalado (FENO) minutos antes y después de nadar. Además, se analizaron los parámetros fisicoquímicos del agua, incluyendo los productos desinfectantes utilizados.
Resultados
Se incluyeron en el estudio 25 nadadores asmáticos (asma intermitente 53%, asma persistente leve 29,4% y asma persistente moderada 17,6%) y 50 nadadores sanos, con una edad media de 40,8 ± 10,8 años. El tiempo medio de inmersión fue similar en ambos grupos (asma 31,9 ± 10, control 32,4 ± 12 minutos). El análisis del agua no mostró diferencias en su composición ni en sus características entre las diferentes piscinas. En los asmáticos, la FENO disminuyó significativamente (28,7 ± 17,8 antes frente a 23,7 ± 15,5 después, p < 0,001) tras la inmersión, sin cambios en los demás parámetros funcionales. En los sujetos no asmáticos, el aumento de la capacidad vital (p < 0,05) y el volumen espirado en un segundo (p < 0,04) mejoraron significativamente tras la inmersión, y la FENO disminuyó (p < 0,01). No se encontraron diferencias significativas en las variables funcionales ni inflamatorias entre los dos grupos tras el baño.
Conclusión
En pacientes con asma intermitente y persistente no se han observado alteraciones funcionales o inflamatorias inmediatas después del baño en piscinas públicas reguladas por la ley.
Palabras clave: Asma, Piscina, Natación, Inflamación
What is already known on this topic
The study was proposed due to the controversy over the effect of swimming in indoor pools on lung function and the doubt about the toxic effect of disinfectants, especially in asthmatic patients.
What this study adds
Our study provides lung function analyzes after swimming in indoor pools in both the healthy population and asthmatic patients.
How this study might affect research, practice or policy
Our results do not show deterioration in lung function, as measured by respiratory and bronchial inflammation tests, when indoor pools meet health requirements.
Introduction
Swimming is associated with considerable cardiovascular and general health benefits at any age. For this reason, it is considered one of the most beneficial sports for the general population. From the respiratory point of view, the habitual practice of swimming has been associated with an improvement in lung function, and it has even been recommended in patients with chronic respiratory diseases, as long as the swimmer's conditions are optimal and the environment in which it is performed complies with suitable hygiene guidelines. However, in recent years, there has been speculation about the influence of certain physical and chemical agents in the water of indoor pools on the lungs of swimmers.1, 2
One of the most controversial triggers is swimming in heavily chlorinated pools as a risk factor for developing or worsening chronic respiratory diseases in children and adults. The warm temperature of indoor pools, the splashing and the lack of air renewal in the pools, causes some highly volatile products, such as disinfectants, to accumulate on the surface of the water and be inhaled by swimmers.
Notably, so far, the different data have given contrary messages about the impact on lung health in asthmatics after this exposure. On the one hand, in experimental animals, exposure of the respiratory tract to high concentrations (100–800 ppm) of chlorine-derived products triggers the appearance of an inflammatory infiltrate of the respiratory tract, increased nitric oxide and measured bronchial hyperreactivity by methacholine.3 On the other hand, experimental studies carried out in rats exposed to swimming pool disinfectant products4 do not show any substantial damage to the lung tissue, major alterations in the expression of cytokines, changes in the distribution of cells, or increased blood pressure associated with asthma. Consequently, the impact of non-competitive swimming on the respiratory system of swimmers continues to be an area of interest.5
The objective of the present study was to carry out a real-life assessment of exposure to non-competitive, recreational bathing for the purpose of keeping fit in public swimming pools, to objectify the variability of lung function before and after immersion in the water and compare it with swimmers without any lung involvement who go swimming in the same environmental conditions as the asthmatic population.
Methods
This is an observational study that evaluates the lung function of regular, asthmatic, non-competitive recreational swimmers in public pools. Cases of swimmers with asthma and those without respiratory diseases swimming for similar reasons were included consecutively, with a 1:2 ratio. The asthmatic swimmers were from a specialized bronchial asthma clinic and the non-asthmatic swimmers were volunteers from the same pools where the asthmatics swam. In both cases, they were regular users of indoor public swimming pools, of both sexes, and aged between 18 and 65 years old. Following previous studies,6 it was estimated that 25 asthmatic swimmers and 50 non-asthmatic swimmers would be needed.
The study was carried out at a total of five indoor public swimming pools attended by the asthmatics selected in the consultation. The functional data were collected on portable devices taken to the sports facilities, with the prior consent of the management staff at each of the pools which cooperated with the study. The healthcare staff responsible for the respiratory functional tests had a Diploma in Nursing from the Pulmonology service with previous experience in pulmonary function laboratories and traveled to the sports facilities to perform the functional tests on site. On the designated day, all the subjects underwent spirometry, and their fractional exhaled nitric oxide (FENO) was measured before and just after bathing. During spirometry, the forced vital capacity (FVC) was recorded, as well as the expired volume in one second (FEV1), and the relationship between the two.
The pools were covered, and had been subjected to exhaustive checks, including the registration and control of the water quality of each of the pools, in compliance with Royal Decree 485/2019 covering the Technical Regulations for Swimming Pool Sanitation in Andalusia. This protocol analyzes, among others, the disinfectants used, the characteristics of the water and the microbiological isolates, with biweekly and monthly analytical measurements being carried out in authorized Public Health laboratories. The technical-sanitary parameters of the pool water were provided by the health inspection service assigned to public pools, on the same day of the study. This data included:
-
1.
Physicochemical variables of the pool water: color and odor, foam characteristics, turbidity (measured in UNF: Nephelometric Turbidity Units), conductivity at 20 °C, pH, free residual chlorine concentration, combined chlorine levels, bromine concentration total and ozone.
-
2.
Levels of isocyanuric acid, polymer derivatives of biguanide, ammonia, nitrates, oxidizability to permanganate, levels of aluminum, iron, copper.
-
3.
Microbiological variables of the water: aerobic bacteria, total and fecal coliforms, fetal streptococci, sulfite-reducing clostridia, algae, arthropod larvae, salmonella, Staphylococcus aureus and Pseudomonas aeruginosa, among others.
The study followed the recommendations of the Declaration of Helsinki, promulgated by the World Medical Association for studies involving human beings. The swimmers signed an informed consent form to agree to participate in the study, and the study was approved by the Research Ethics Committee. All patient database records generated were confidential and treated in accordance with Organic Law 3/2018, of December 5, on the Protection of Personal Data.
Statistical analysis
The statistical analysis was performed using the Statistical Package for Social Sciences (IBM Corporation, Armok, New York) version 22.0. The level of statistical significance was set at 0.05. Descriptive statistics were performed on the study variables, using absolute and relative frequencies in the case of qualitative variables. The quantitative variables were checked to see whether they followed a normal distribution through mean and standard deviation and range (minimum and maximum). To analyze the association between the qualitative variables, the Chi-square test or Fisher's exact statistic was used, and we used the Pearson correlation coefficient or Spearman's Rho to analyze the association between the quantitative variables. To analyze the qualitative variables with the quantitative variables together to see if they were dichotomous, we performed the T-Student for independent measurements or the U-Mann–Whitney, as appropriate. For multiple comparisons, post-hoc tests or the corresponding non-parametric tests (Mann–Whitney U) were performed, applying the Bonferroni correction.
Results
Twenty-five asthmatic patients and 50 swimmers without lung disease were included. The data on the subjects are summarized in Table 1. The immersion time for recreational, non-competitive swimming was similar for both groups. The severity of asthma patients was 53% intermittent asthma, 29.4% mild persistent asthma, and 17.6% moderate persistent asthma.
Table 1.
Descriptive analysis of the two groups of patients: control group (CG) and asthmatic group (AG).
| Control group (CG) n = 50 |
Asthmatic group (AG) n = 25 |
|
|---|---|---|
| Sex (male, female) | 52%, 48% | 36%, 64% |
| Age (years) | 40.8 (18–59) | 42.38 (22–62) |
| Smoking | ||
| Never | 50% | 60% |
| Ex-smokers | 44% | 24% |
| Smokers | 6% | 12% |
| Time spent in the water (min) | 32.4 ± 12 | 31.9 ± 10 |
The characteristics of the pool water are summarized in Table 2. The average disinfectant concentration was 1.4 mg/L. These disinfectants were in most cases sodium or calcium hypochlorite, and in all cases were within the normal range of disinfection levels established by law. The water temperature remained constant, in most of the measurements, at around 29 °C, while the relative humidity of the air in the pools was 43.3%. The presence of pathological microorganisms was not observed in the microbiological analysis of the water.
Table 2.
Analysis of the main characteristics of the swimming pool water.
| Minimum value | Middle value | Maximum value | |
|---|---|---|---|
| pH | 7.17 | 7.2 | 7.5 |
| Free chlorine (mg/L) | 0.4 | 0.7 | 1.8 |
| Total chlorine (mg/L) | 0.9 | 1.4 | 2.3 |
| Turbidity (UNF)a | 0.3 | 0.4 | 0.4 |
| Glass water temperature (°C) | 26 | 29 | 30 |
| Relative humidity (%) | 35 | 43.3 | 50 |
| CO2 (ppm) | 471 | 489.1 | 492 |
UNF: Nephelometric Turbidity Units.
The inflammatory and functional changes before and after bathing are summarized in Table 3 and Fig. 1. After immersion in the asthmatic group, FENO levels significantly decreased.
Table 3.
Functional and inflammatory parameters before and after swimming.
| Control group (CG) (n = 50) |
Asthmatic group (n = 25) |
p valuea | |||||
|---|---|---|---|---|---|---|---|
| Before bathing | After bathing | p value* | Before bathing | After bathing | p value* | ||
| FVC (%) | 105.82 (13.91) | 110 (13.98) | <0.05 | 109 (13.62) | 109 (12.74) | – | 0.06 |
| FEV1 (%) | 103.54 (13.93) | 104.08 (13.52) | <0.04 | 96 (17.36) | 99.39 (17.29) | – | 0.08 |
| FEV1/FVC (%) | 82.18 (5.59) | 82.56 (5.68) | – | 77 (12.36) | 80.47 (14.36) | – | 0.99 |
| FeNO (ppb) | 22.74 (14.40) | 20.1 (14.01) | <0.01 | 28.7 (17.85) | 23.7 (15.56) | <0.001 | 0.1 |
Values expressed as mean (standard deviation). FVC: forced vital capacity; FEV1: expired volume in one second; FENO: fractional exhaled nitric oxide.
p value between groups after bathing.
p value between before and after bathing within each group.
Fig. 1.
Lung function and bronchial inflammation in swimmers before and after swimming. FVC, FEV1 and FEV1/FVC expressed in % and FeNO (fractional exhaled nitric oxide) in ppb (particles per billion).
After bathing, while the other parameters did not change. In the non-asthmatic group, we found differences in respiratory functional parameters. After immersion in water, the functional values improved significantly, and there was also a decrease in FENO values.
No differences were found in the parameters of bronchial function and immediate variation of FeNO in relation to the physical and chemical data of the pool water collected at the time of inclusion, in either of the two study groups (data not shown).
Discussion
Our data shows no deterioration in lung function in a sample of asthmatic users of indoor public swimming pools after swimming, during approximately half an hour of non-competitive exercise. Meanwhile, in swimmers without any previous respiratory pathology, we observed an immediate improvement in certain respiratory functional parameters after swimming. These findings suggest that there is no negative impact on healthy or asthmatic users of certain substances used for conditioning and disinfecting the swimming pools. Likewise, the decrease in inflammation values (FENO) in both groups points to the very low immediate inflammatory impact that certain water products could cause in the airways of swimmers.
Traditionally, there has been a considerable degree of controversy over the effect that swimming in indoor pools could have on lung function and inflammation parameters. Some authors have shown an increase in bronchial hyperreactivity and inflammation, especially due to the effect of water chlorination and the exercise itself.7 As a result, the controversy over the risk of developing asthma from using swimming pools has been reactivated on several occasions. Previous studies, such as that by Bernard et al.8 carried out in school children, have compared the prevalence of asthma and bronchial hyperreactivity due to exercise and the time spent swimming. These authors found a strong positive correlation between the prevalence of asthma and the time spent swimming, with this effect being greater in young children.
The authors conclude that the chlorine products that children inhale when swimming damage the bronchial epithelium, increase bronchial permeability and lead to allergic sensitization and the development of asthma, particularly in young children and those with a family history of asthma. However, the methodology of this publication was strongly criticized by Armstrong et al.,6 who argued that the article does not demonstrate a clear association between use of swimming pools and the risk of asthma.
The most recent studies carried out in the adult population have been mainly conducted with swimming pool workers, who show slight increases in FENO after their working shift,6 while other studies, most recently in young athletes who swim, were limited to recording symptoms of rhinitis and not lung function itself. The study which most resembles ours is the one carried out in a sample of over 1000 swimmers, in which spirometry tests showed airway obstruction in 15 swimmers, which represented 12% of a group of 130 competitive swimmers. In this study, the spirometry tests were not compared with functional tests taken before entering the water and the diagnosis of asthma was based on asking the swimmer, without any of the prior consultation we carried out in our study.9
The strength of our study, unlike previous articles dealing with competitive or elite swimmers, is the fact that it focuses on swimming for recreational or leisure purposes, which is the most frequent type of swimming regularly done by swimmers. Competitive athletes, unlike the patients in this study, achieve high lung flows, which means that their respiratory tracts are more exposed to irritating elements such as the cold, and that they breathe in large quantities of air which contains the chlorine-derived products used to disinfect the pool, which remain on the surface of the water. In this context, previous publications, such as that by Helenius et al.,10 reported that 36–79% of elite swimmers suffer bronchial hyperreactivity, as measured with methacholine or histamine, and the risk is greater in atopic swimmers. Eosinophilic inflammation can also be demonstrated in elite athletes, which correlates with the severity of bronchial hyperresponsiveness, as measured by methacholine or exercise tests. However, in the adult population, research studies similar to the sample in our analysis are scarce, since the population studied in most publications consists of children and adolescents.11 Likewise, there are few studies that evaluate lung involvement in relation to the aquatic parameters analyzed in our research.12
Our work also has certain limitations: the study does not include severe asthmatics because we did not find any patients from this group who practiced swimming. Volatile by-products were not taken into account because these parameters are not analyzed in the official records, but normal CO2 levels confirmed good ventilation in all pools. The time spent in the water is limited; we do not know if increasing the immersion time in the water with prolonged exposure can lead to greater deterioration of lung function.
On the other hand, the drop in FENO as an indicative variable of lung inflammation may be due to the hyperventilation that occurs physiologically after carrying out any form of physical exercise. Similarly, the improvement in parameters such as FVC is associated with the improvement in respiratory capacity just after completing any kind of sports activity, due to the physiological mechanisms associated with physical exercise, although we do not know how long this lasts, since no spirometric control tests were taken after the subjects had left the pool area, mainly due to technical difficulties.
Our analysis is consistent with the latest systematic reviews and meta-analyses on the effectiveness of recreational swimming on lung function and asthma control in children with asthma,13 in which swimming was found to have favorable effects on FEV1 and the FVC. Consequently, our results agree with previous studies that demonstrate the positive impact of swimming compared to other sports activities, as demonstrated by previous publications that show statistically higher values of FVC, FEV1 and FEV1/FVC in swimmers when compared with players of land sports such as soccer14 or running.15 This points to the need for future research on the benefit of swimming in patients with respiratory pathologies other than asthma. In conclusion, the results obtained in our study allow us, on the one hand, to rule out a deterioration in immediate lung function in asthmatic swimmers and healthy non-professional swimmers and, on the other, to objectify the beneficial effect of swimming in healthy subjects, in line with the classic recommendations of the beneficial effects of carrying out this sport. Therefore, swimming in public indoor pools subject to health controls does not seem to cause any immediate worsening of lung capacity in intermittent and persistent asthmatic patients and appears to significantly improve lung function parameters in healthy subjects.
Informed consent
All participants were informed and signed an informed consent form before their inclusion.
Funding
This study was funded by Neumosur.
Authors’ contributions
MARF: Methodology and Project administration. CGM: Methodology and Resources. FJAG: Methodology and Supervision. MARF, JFMG and FJAG: Recruited patients.
All authors agree to have their names added to the paper. All named authors meet the International Committee of Medical Journal Editors (ICMJE) criteria for authorship of this article, take responsibility for the integrity of the work as a whole, and have given their approval for this version to be published.
Artificial intelligence involvement
No artificial intelligence tools were used in the preparation of this manuscript.
Ethical considerations
The study was approved by the ethics committee before its commencement and all participants were informed and signed an informed consent form before their inclusion.
Conflicts of interest
The authors declare no conflicts of interest.
Acknowledgments
We would like to thank the volunteer swimmers who agreed to participate in this study and to the staff of the sports facilities where the study was carried out.
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