Introduction
Allergic rhinitis (AR) is one of the most common diseases worldwide, affecting approximately 400 million people (Savouré et al., 2022; Nur Husna et al., 2022). AR affects quality of life, such as by impairing sleep quality, academic or occupational performance, and cognitive function (Brożek et al., 2017). AR involves inflammation of the nasal mucosa triggered by allergen-specific immunoglobulin E (IgE), which binds to IgE receptors on mast cells and basophils and releases chemical mediators, such as histamine, leukotrienes, and cytokines, which can cause AR symptoms to develop, including nasal congestion, itching, sneezing, and rhinorrhea (Wheatley & Togias, 2015). The severity of AR is associated with fractional exhaled nitric oxide (FeNO) levels. FeNO, a marker of airway inflammation, increases in inflammatory airway diseases like bronchial asthma, AR, and chronic rhinosinusitis (Takeno, Noda, & Hirakawa, 2012). Elevated FeNO in AR patients, especially those who are highly reactive, may indicate a higher risk of airway inflammation and asthma (Li YH et al., 2021). Exercise may decrease FeNO levels (Maroun et al., 1995; Gabriele et al., 2005). Terada et al. (2001) found that FeNO values significantly declined after exercise in patients with and without exercise-induced bronchoconstriction, as well as in healthy subjects.
Exercise has been linked to a variety of health advantages and is highly recommended for improving health, strengthening the immune system, and preventing or treating many diseases (Park et al., 2020). In addition, moderate- to vigorous-intensity acute exercise of <60 min can stimulate the continuous exchange of specific and physically active circulating immune cells (Nieman & Wentz, 2019). In fact, acute strenuous exercise has been shown to cause bronchoconstriction, asthma, and rhinitis in sensitive people. Runners and swimmers with AR have reported a decrease in peak nasal inspiratory flow (PNIF) levels and an increase in sneezing, nasal congestion, and itching after high-intensity exercise (Alves et al., 2010). Patients with AR who engage in vigorous exercise are associated with subjective and objective aggravation of AR symptoms (Park et al., 2020). However, previous studies have shown that single sessions of aerobic exercise decreased nasal blood flow (NBF) and nasal resistance and improved AR symptoms (Richerson & Seebohm, 1968; Serra-Batlles et al., 1994; Tongtako et al., 2012). Furthermore, aerobic exercise training also has improved the clinical symptoms of AR and cytokine profiles (Tongtako et al., 2018).
High-intensity interval exercise (HIIE) is a form of aerobic exercise characterized by repeated short cycles of intense effort followed by intervals of rest (Sawyer, Cavalheri, & Hill, 2020). The short intervals of high intensity aim to achieve 80%–95% of the maximum heart rate and alternate with rest periods of light exercise at 40%–50% of the maximum heart rate (Kravitz, 2015). HIIE takes less time than moderate continuous training exercise, helps improve the circulatory and respiratory systems and develop respiratory function, and increases the work of breathing, rate of ventilation, and blood flow to the muscles used in breathing, which has a positive effect in asthmatic subjects. Moreover, HIIE has been shown to improve the forced expiratory volume in 1 s in the acute phase and maximal oxygen consumption (VO2 max) in the chronic phase in patients with asthma (Ertürk et al., 2022).
However, to our knowledge, no studies have yet assessed the effect of HIIE on clinical symptoms in patients with AR. This study aimed to determine the acute effects of HIIE on AR symptoms, NBF, PNIF, and FeNO in patients with AR. Additionally, it sought to compare the effects of 1:1 HIIE and 1:2 HIIE on these parameters. We hypothesized that HIIE would positively affect AR patients and that the 1:1 and 1:2 HIIE protocols would have different impacts on AR symptoms, NBF, PNIF, and FeNO.
Methods
Study design and procedure
This study was approved by the Institutional Review Board of Chulalongkorn University (COA No. 180/65) and registered as a clinical trial with ClinicalTrials.gov (study # NCT05779046). All participants provided written informed consent before participation. The sample size was calculated using the G*Power program (version 3.1.9.2) with an alpha error of 0.05 and a power of 0.80. A minimum of eleven participants per group was required for this study.
Twelve patients with allergic rhinitis (AR), aged between 19 and 31 years (female/male ratio = 5/7), were recruited from Chulalongkorn University Health Service Center and Chulalongkorn Hospital and participated in this study. The participants had a clinical history of persistent rhinitis with characteristic symptoms (nasal congestion, sneezing, nasal itching, and runny nose) for more than 4 days per week and had a positive skin prick test (wheal diameter ≥ 3 mm) to house dust mites (Dermatophagoides pteronyssinus) (Greater Pharma Manufacturing Co. Ltd.). The participants also had a body mass index between 18.5 and 24.9 kg/m2. This study excluded participants with a history of smoking, asthma, chronic rhinosinusitis, hypertension, or cardiovascular disease. Participants were asked to abstain from all dietary supplements and to refrain from taking antihistamines, leukotriene receptor antagonists, and nasal steroids for 5 days, 1 week, and 2 weeks, respectively, before the start of the experiment.
Participants were first screened by a physician to evaluate disease symptoms and ensure the discontinuation of certain medications required for the study. Following this initial screening, the researcher conducted a secondary screening based on the study’s inclusion and exclusion criteria. Once participants met these criteria, appointments were scheduled for testing and data collection.
This study was a randomized crossover trial using computer-generated simple random sampling to investigate the acute effect of 1:1 HIIE and 1:2 HIIE on respiratory function and rhinitis symptoms in patients with AR. The participants were randomly assigned to either 1:1 HIIE followed by 1:2 HIIE or 1:2 HIIE followed by 1:1 HIIE by exercising 1 week apart. Assessment of rhinitis symptoms, NBF, PNIF, pulmonary functions, respiratory muscle strength, and FeNO were performed before and after 0, 15, 30, 45, and 60 min after exercise for each exercise program.
The physiological characteristics of the participants are presented in Table 1. There were 15 participants in the research; 3 participants dropped out of the study because of scheduling difficulties. There were 12 participants in the research collection (7 males, 5 females) (Figure 1). The participants were randomly assigned to exercise using one of the two HIIE protocols.
Table 1
Physiological characteristics in patients with allergic rhinitis.
| PHYSIOLOGICAL CHARACTERISTICS | S.D. | |
|---|---|---|
| Age (years) | 23.08 | 3.68 |
| Weight (kg) | 62.2 | 10.2 |
| BMI (kg/m2) | 21.88 | 2.12 |
| Resting heart rate (beat/min) | 81.33 | 11.23 |
| Systolic blood pressure (mmHg) | 112.25 | 7.53 |
| Diastolic blood pressure (mmHg) | 64.08 | 7.79 |
[i] BMI = Body Mass Index.
Figure 1
CONSORT flow diagram of participant allocation and analysis.
Skin prick test
A metal lancet with a singular tip is gently inserted into the allergen extract droplet and maintained in contact with the skin for a duration of no less than 1 second. As a negative control, normal saline solution is employed. The outcomes are examined between 15 to 20 minutes subsequent to the application.
Exercise Protocol
In this study, the participants performed HIIE programs involving walking/running on a treadmill for approximately 40 min. Two different exercise protocols were used, each preceded by a 10-min warm-up at low intensity: a 1:1 HIIE (high intensity for 1 min at 85%–90% of the maximum heart rate alternating with low intensity at 50%–55% of the maximum heart rate for 1 min); and a 1:2 HIIE (high intensity for 1 min at 85%–90% of the maximum heart rate alternating with low intensity at 50%–55% of the maximum heart rate for 2 min). Heart rate was continuously monitored by the researcher using a Polar H10 chest strap heart rate monitor to ensure participants maintained the prescribed intensity levels. During high-intensity intervals, participants walked or ran at a treadmill speed of 8.51 ± 0.27 mph, while during low-intensity intervals, they walked or ran at 2.10 ± 0.15 mph with no incline. The Rate of Perceived Exertion (RPE) was recorded at 14.81 ± 0.78 for high intensity and 10.29 ± 0.63 for low intensity. The second of the two protocols was performed 1 week after the first day (Figure 2). Both training programs are structured to require the same amount of energy expenditure.
Figure 2
1:1 and 1:2 High intensity interval exercise protocol.
Physiological Characteristics
After a 10-min rest period, a digital sphygmomanometer (GE Dinamap CARESCAPE, V100, USA.) was used to measure blood pressure and heart rate were measured. Dual-energy x-ray absorptiometry (USA) was also used to measure body weight and percentage body fat.
Rhinitis Symptom Scores
The Total Nasal Symptom Score questionnaire was used to assess nasal symptoms (Chanta et al., 2022). Before and after each exercise session, the participants were asked to rate the severity of persistent AR symptoms, including nasal congestion, itching, sneezing, and rhinorrhea. The score ranged from 0 to 3 points (0 = none, 1 = mild, 2 = moderate, 3 = severe).
NBF
Laser Doppler flowmetry (DRT4, Moor Instruments, UK) was used to measure the NBF. Before the test, each subject rested for 1 hour in a separate room. During the test, the participants were instructed to breathe normally and not to speak, cough, or move. A lateral endoscopic probe with a flexible 1.34-mm-diameter flexible nylon sheath was placed on the front of the nose. The NBF measurements were performed before, 0, 15, 30, 45, and 60 min after each exercise program.
PNIF
A PNIF meter (Clement Clark International, model IN-CHECK ORAL, UK) was attached to an anesthesia mask to measure the PNIF. During the process, the participants covered their mouth and nose with a mask that was turned onto a plastic cylinder through which air was passed during inspiration. The participants then forcefully inhaled through their noses while keeping their lips firmly closed. The airflow was controlled by a diaphragm inside the cylinder, and the highest peak flow was measured on a scale between 30–370 L/min. The test participants covered their mouth and nose with a mask and forcefully inhaled through their noses while keeping their lips closed. Both before and after activity, PNIF was measured.
FeNO
FeNO Monitor (BedFont, UK) was used to measure the FeNO. The participants inhaled deeply for 2 to 3 seconds before exhaling slowly, which normally took 10 seconds.
Statistical Analysis
The statistical program SPSS version 28 for Windows was used to evaluate the data (IBM SPSS Statistics for Windows, IBM Corp., Armonk, NY, USA). The Shapiro–Wilk test was used to determine if the data were normally distributed. Two-way analysis of variance was used to determine the significant differences in NBF, PNIF, and FeNO before and at 0, 15, 30, 45, and 60 min after exercise for each exercise program. The data were presented as the mean and standard deviation. The Friedman test was used to examine the rhinitis symptoms scores. Differences were considered significant at p < 0.05.
Results
NBF and PNIF
After 1:2 HIIE, NBF was significantly lower at 0, 15, 30, 45, and 60 minutes post-exercise (p < .05) compared to the pre-exercise. Conversely, PNIF was significantly higher at 0, 15, 30, 45, and 60 minutes post-exercise (p < .05) compared to the pre-exercise. Following 1:1 HIIE, PNIF was significantly lower only at 0 minute post-exercise (140 ± 9.05, p < .001) compared to the pre-exercise (p < .05). Additionally, there was a significant difference in NBF at 0 minute post-exercise between 1:2 HIIE and 1:1 HIIE (p < .05) (Figure 3).
Figure 3
The comparison of NBF (A.) and PNIF (B.) between pre- and post-exercise at 0, 15, 30, 45, and 60 minutes and between each protocols.
Data are presented as mean ± SD. * p < 0.05 vs. pre-test., † p < 0.05 vs. 1:1 HIIE.
Rhinitis Symptom Scores
After 1:2 HIIE, Rhinitis symptom scores include nasal congestion, itching, sneezing, rhinorrhea symptoms, and total rhinitis symptoms cores were significantly lower post exercise at 0, 15, 30, 45, and 60 minutes than the pre-exercise (p < .05). In addition, there was a significant difference in itching, sneezing, and total rhinitis symptoms scores at 0, 15, 30, 45, and 60 min after 1:1 HIIE than the pre-exercise (p < .05). After 1:1 HIIE, showed significantly decreases in nasal congestion at 0 min and rhinorrhea at 45 and 60 min when compared with pre-exercise (p < .05). However, the total rhinitis symptom scores at 0 min and rhinorrhea scores at 0 and 15 min were significantly lower and different after 1:2 HIIE than after 1:1 HIIE (p < .05) (Figure 4).
Figure 4
The comparison of nasal congestion (A), itching (B), sneezing (C), rhinorrhea (D), and total rhinitis symptoms (E) between pre- and post-exercise at 0, 15, 30, 45, and 60 minutes and between each protocols.
Data are presented as mean ± SD. * p < 0.05 vs. pre-exercise., † p < 0.05 vs. 1:1 HIIE.
FeNO
FeNO was significantly lower after 1:2 HIIE than after the pre-exercise at baseline (p < .05), but there was no significant difference in FeNO between the after 1:1 HIIE value and the after pre-exercise (Figure 5).
Figure 5
The comparison of FeNO between pre- and post-exercise at 0, 15, 30, 45, and 60 minutes and between each protocols.
Data are presented as mean ± SD. * p < 0.05 vs. pre-exercise.
Discussion
The key findings of this study indicate that HIIE, which involves short bursts of very high effort, can be an effective alternative form of exercise for patients with AR. The HIIE protocol improved clinical AR symptoms. Both 1:2 HIIE and 1:1 HIIE reduced PNIF and rhinitis symptoms, but only 1:2 HIIE had beneficial effects on the rhinorrhea symptoms, NBF, and FeNO in patients with AR.
AR causes inflammation of the nasal mucosa, resulting in sneezing, itching, rhinorrhea, and congestion. The mechanism of nasal symptoms development is more complex. Some symptoms, such as rhinorrhea, can be caused by the direct effects of allergic response products on nasal end organs, whereas typical rhinitis symptoms can be caused by neurological mechanisms (Sarin et al., 2006). The present study showed that nasal congestion, sneezing, itching, and total rhinitis symptoms were significantly lower after exercise for both HIIE protocols (1:1 and 1:2 HIIE) than after the pretest. These changes may be caused by sympathetic-induced nasal vasoconstriction, which decreases venous sinusoid volume (Valero et al., 2005). Furthermore, because the nasal mucosa has both resistance and capacitance blood vessels (Howarth et al., 2005), the improvement is most likely related to reduced nasal congestion by decreasing blood flow and increasing sinus emptying in the capacitance vessels after performing both acute HIIE protocols (Ramey, Bailen, & Lockey, 2006). Similar to other studies report that nasal resistance has been shown to decrease with exercise (Serra-Batlles et al., 1994; Tongtako et al., 2012). However, a few studies have found that high-intensity exercise caused an increase in rhinitis symptoms (Bonini et al., 2006; Alves et al., 2010). The present study show that the rhinorrhea symptoms after exercise at 0 and 15 min were significantly lower and significantly different after 1:2 HIIE than after 1:1 HIIE. This may be because 1:2 HIIE has a longer rest period, but 1:1 HIIE has the same rest period as high intensity, so a runny nose is less likely to decrease.
Changes in the blood circulation of the nasal cavity may be responsible. Laser Doppler blood flow measurement is a noninvasive method for precise measurement of mucosal perfusion, which is commonly used in the study of nasal mucosal pathophysiology (Lee et al., 2002). In the present study, patients with AR had lower NBF after 1:2 HIIE. The reduction in NBF by HIIE appears to cause vasoconstriction in both the external and internal parts of the nasal mucosa (Ohki et al., 1987), leading to a reduction in nasal resistance and congestion. In addition, our study showed a higher PNIF after both programs. The PNIF rate has been shown to relate well to subjective measures of nasal congestion (Agnihotri, & McGrath, 28). Moreover, Tongtako et al. found that NBF decreased and PNIF increased after a single bout of exhaustive and moderate exercise related to decreased rhinitis symptoms in patients with AR (Tongtako et al., 2012).
In our study, FeNO was significantly higher after 1:2 HIIE than at baseline. Research has shown that FeNO is frequently involved in allergic inflammatory processes. Increased production of inducible NO synthase has been found to be involved in the development of allergic inflammation in the upper and lower airways as well as in AR comorbidity (Kalpaklioglu, & Kalkan, 2012). The overall decrease in FeNO following HIIE can be explained by a change in NO dynamics caused by a ventilation impact. Exercise increases the ability of NO to diffuse and decreases NO concentrations in the airway wall. The lower NO, which has been related to greater NO loss in breathed air, has been interpreted as a washout of tissue NO reserves (Shin et al., 2003; Evjenth et al., 2015). Some studies have reported that acute exercise is associated with a reduction in exhaled NO levels (Shin et al., 2003; Petsky et al., 2013). However, Scollo et al. (2000) found no difference in FeNO values following a treadmill exercise challenge.
There are some limitations should be noted. First, the sample size may be considered small, with an unequal distribution of males and females—7 males and 5 females—which could impact the results. Consequently, our findings should be interpreted with caution. Additionally, there were uncontrollable variables such as air quality and atmospheric dust on the days participants were tested, as well as stress and emotional factors that could trigger disease symptoms. Furthermore, we did not include a moderate-intensity continuous exercise protocol, which could have provided more information on the acute effects of HIIE compared to continuous exercise. Therefore, future studies with larger, more balanced samples and varied exercise protocols are needed to better understand the effects of exercise on rhinitis symptoms.
Conclusion
This study showed that both HIIE protocols improved the symptoms of AR, including nasal congestion, sneezing, itching, rhinorrhea, and total rhinitis symptoms. However, NBF decreased only after performing the 1:2 HIIE protocol and reduced rhinorrhea symptoms more than the 1:1 HIIE. Overall, the 1:2 HIIE protocol significantly improved AR symptoms and is suitable for patients with AR.
Data Accessibility Statement
The data supporting the findings of the current study are available from the corresponding author on reasonable request.
Acknowledgements
We are indebted to all volunteers. We would like to thank Supranee Buranapraditkun, Ph.D. for cytokines analysis. This study was supported by Exercise Physiology in Special Population Research Unit, and Faculty of Sports Science Fund, Chulalongkorn University.
Competing Interests
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Author Contributions
B.P. designed and performed the experiments, data collection, analyzed the data, and drafted the manuscript. J.K. designed the experiments, contributed to sample preparation, aided in interpreting the results. T.D.M. designed the experiments and reviewed the manuscript. W.T. conceptualized and designed the study, assisted with the implemented of the intervention, interpreting the results, discussion and conclusion, and revised/reviewed the manuscript. All authors have read and approved the manuscript and gave consent to publish it.