Abstract
Chronic rhinitis is often associated with sleep disturbance and daytime sleepiness. Disturbance in sleep impairs numerous metabolic processes and brain function. However, there is a paucity of data regarding the evaluation of nasal symptoms and sleep disturbance in chronic rhinitis, either allergic or non-allergic group. To evaluate the characteristic of sleep disturbance in allergic and non-allergic rhinitis in Dr. Cipto Mangunkusumo Hospital Jakarta, a cross sectional analytic descriptive study was performed. All recruited subjects were evaluated for total nasal symptom scores (TNSS) and nasal obstruction symptoms evaluation scores (NOSE). Sleep disorder was assessed using Epworth Sleepiness Scale (ESS), Pittsburg Sleep Quality Index (PSQI) questionnaires, and polysomnography (PSG). A total of 22 chronic rhinitis patients, with 11 allergic and 11 non-allergic rhinitis were evaluated. Most subjects with allergic rhinitis experienced daytime sleepiness and poor quality of sleep as well as non-allergic rhinitis, without significant differences in TNSS, NOSE, ESS, and PSQI scores. There was impairment in sleep architecture from PSG parameters in both groups, but the difference was not significant. However, RDI-REM (17.7 ± 14.5 vs. 14.7 ± 18.5) and RERA (2.2 ± 2.1 vs. 1.6 ± 1.7) parameters have a tendency to be higher in the allergic rhinitis compared to non-allergic rhinitis group. Sleep disturbance existed in chronic rhinitis, presented by excessive daytime sleepiness and impairment in sleep architecture, yet no significant difference shown in the severity of TNSS, NOSE, ESS, PSQI scores, and sleep architecture parameters between the allergic and non-allergic rhinitis.
Keywords: Allergic rhinitis, Non-allergic rhinitis, Nasal congestion, Daytime sleepiness, Polysomnography
Introduction
Allergic rhinitis (AR) is a chronic inflammatory nasal disease affecting 10–30% world population [1, 2]. Chronic rhinitis, divided into allergic and non-allergic, according to WHO ARIA is nasal inflammation characterized by rhinorrhea, nasal congestion, sneezing, and nasal itching [3].
Nasal congestion is a dominant and one of the most disturbing symptoms of both allergic and non-allergic rhinitis [1]. Edema of nasal mucosa and rhinorrhea lead to the increase of nasal resistance and congestion.
Rhinitis is associated with sleep disorders, daytime sleepiness, and chronic fatigue. In their study, Lunn and Craig proved that [4] nasal congestion is one of the risk factors of sleep disorder breathing (SDB). Nasal congestion is often worse at night and morning due to the overnight decline in serum cortisol. TNSS and NOSE are often used as subjective methods to evaluate nasal symptoms in chronic rhinitis patients.
Sleep is a crucial aspect of both physical and mental health, lack of sleep is associated with weakened immunity, poor wound healing, and to the development of chronic diseases. Sleep also improves procedural memory (skills and procedures) and declarative memory [5]. Non rapid eye movement (NREM) sleep affects the anabolic process and macromolecule RNA synthesis. More specifically, Rapid eye movement (REM) sleep, a deep restorative sleep that is heavily associated with allergies disorders. REM sleep affects the production of new junctions in the cortex of the brain and neuroendocrine system, therefore beneficial for memory consolidation [4, 5].
SDB is a spectrum of disorder, which encompasses apnea, hypopnea, and snoring episodes, all of which are associated with nasal congestion or obstruction. Snoring, upper airway resistance syndrome (UARS), obstructive sleep apnea (OSA) and obesity-hypoventilation syndrome are all spectrum of SDB. Obstructive sleep apnea (OSA) is associated with systemic hypertension, stroke and the incidence of cardiovascular disease [3, 4].
Sleep quality can be assessed with questionnaires which measure patient’s subjective symptoms such as the Epworth sleepiness scale (ESS) and Pittsburg Sleep Quality Index (PSQI). Laboratory based polysomnography can be used to measure sleep objectively and deemed as the gold standard method for objective sleep measurement [5, 6].
There is a paucity of data regarding SDB and chronic rhinitis, among allergic & non-allergic rhinitis patients with daytime sleepiness. The aim of this study is to contribute supporting evidence, whether allergic and non-allergic rhinitis have different characteristic in nasal symptoms and sleep quality with the use of subjective measurement tools (questionnaires) and objective measurement (polysomnography).
Materials and Methods
This cross sectional analytical-descriptive study was conducted from March to August 2020 in the ORL-HNS outpatient clinic at Dr. Cipto Mangunkusumo Hospital. Ethical approval was granted by the Ethics Committee of the Faculty of Medicine, University of Indonesia with regards of the protection of human rights and welfare in medical research. Ethics approval number: KET-122/UN2.F1/ETIK/PPM.00.02/2020.
Subjects were recruited by consecutive sampling and consisted of male and female between 18 and 60 year old with chronic rhinitis symptoms and sleep disorder, who did not received intranasal steroid and oral anti-histamines within the last 1 month, and did not have history of psychiatric disorder. Subjects were given written consent and willing to participate. All subjects underwent ENT examination and nasal endoscopy to rule out nasal polyp, nasal or sinonasal tumor, septum deviation, chronic rhinosinusitis, adenoid hypertrophy, tonsil hypertrophy, macroglossia, and oropharyngeal tumour.
The nasal symptoms were evaluated using TNSS based on VAS and NOSE questionnaires. Sleep quality were subjectively assessed using Epworth Sleepiness Scale (ESS), and Pittsburg sleep quality index (PSQI).
Skin prick test was performed with 16 most common allergens produced by ALK-ABELLO to determine the allergic from the non-allergic rhinitis. Sleep parameters were objectively measured using polysomnography (PSG). Sleep architecture was assessed using NREM/REM and respiratory analysis was assessed using RDI-REM and RERA, based on earlier studies that showed REM, RDI-REM and RERA have been linked with allergic disorders. All subjects underwent polysomnography by SOMNOtouch Resp with Domino software.
All data documented from the examinations were put into electronic medical records. The results were analyzed using SPSS-20 program.
Results
A total of 22 patients with rhinitis symptoms and sleep disorder were included in this study. Based on the skin prick test, 11 patients were diagnosed with allergic rhinitis and 11 with non-allergic rhinitis. The mean age for the subjects were 32.0 ± 4.7 years old in the allergic rhinitis and 32.4 ± 5.6 years old in the non-allergic rhinitis. The BMI for the allergic and non-allergic rhinitis are 27.4 ± 1.9 and 27.2 ± 4.6 respectively.
The mean value for TNSS symptoms are displayed in Table 1. Symptom with the highest mean value was nasal congestion, scored 5.4 ± 1.2 in the allergic rhinitis group and 5.0 ± 1.3 in the non-allergic rhinitis group. The difference was not statistically significant using statistical analysis with Mann Whitney and unpaired T test.
Table 1.
Mean value of TNSS based on VAS symptoms in allergic and non-allergic rhinitis group (n = 22)
| TNSS questionnaire | Rhinitis allergy | Non-allergic rhinitis | p value |
|---|---|---|---|
| Nasal congestion | 5.4 ± 1.2 | 5.0 ± 1.3 | 0.414a |
| Rhinorrhea | 3.0 ± 2.2 | 2.8 ± 1.6 | 0.535b |
| Nasal itching | 1.5 ± 1.8 | 1.1 ± 1.7 | 0.578b |
| Sneezing | 3.3 ± 1.8 | 2.7 ± 2.2 | 0.607b |
aUnpaired T test
bMann Whitney
The comparison of allergic and non-allergic rhinitis based on the sleep disorder evaluation questionnaires (NOSE, ESS, and PSQI) are displayed in Table 2.
Table 2.
Comparison of sleep disorder evaluation allergic rhinitis and non-allergic rhinitis (n = 22)
| Questionnaires | Allergic rhinitis (n = 11) | Non-allergic rhinitis (n = 11) | p value | RR (CI 95%) |
|---|---|---|---|---|
| NOSE | ||||
| Mild (5–25) | 8 | 8 | References | |
| Moderate (30–50) | 1 | 3 | 0.392 | 2.0 (0.3–11.7) |
| Severe (55–75) | 1 | 0 | 0.5 (0.3–0.8) | |
| Extreme (≥ 80) | 1 | 0 | 0.5(0.3–0.8) | |
| ESS | ||||
| 5–9 | 3 | 5 | 0.659 | 0.7 (0.2–1.8) |
| > 10 | 8 | 6 | ||
| PSQI | ||||
| Good (< 5) | 3 | 1 | 0.586 | 1.7 (0.8–3.6) |
| Poor (≥ 5) | 8 | 10 | ||
Analyzed using Chi square test
In the NOSE questionnaire, mild nasal congestion was found in the majority of subjects (8 out of 11) in both allergic and non-allergic rhinitis. For the ESS questionnaire, 3 out of 11 subjects in the allergic rhinitis group and 5 out of 11 of the non-allergic rhinitis showed ESS score of 5–9, while 8 out of 11 and 6 out of 11 have ESS score > 10. Based on the PSQI questionnaire, 8 out of 11 subjects in the allergic rhinitis group and 10 out 11 subjects in the non-allergic rhinitis had poor quality of sleep.
The mean value of polysomnography (PSG) between the allergic and non-allergic rhinitis group is shown in Table 3. Normality test showed that all data have normal distribution. Our study showed an increase in percent total time of light sleep, 69.2% and 64.3% in allergic and non-allergic group respectively. For deep sleep, the percent total time was not disturbed, approximately 20%. There was a reduced sleep latency, less than 5 min in both groups. For REM stage, there was a decrease in total percent time as low as 10.9% and 9.5% in allergic and non-allergic rhinitis.
Table 3.
The parameters of PSG in allergic and non-allergic rhinitis group (n = 22)
| PSG parameter | Mean value ± SD | p value | |
|---|---|---|---|
| Allergic rhinitis n = 11 | Non-allergic rhinitis n = 11 | ||
| Sleep architecture | |||
| REM | |||
| Light sleep | 10.3 ± 4.6 | 9.5 ± 4.2 | 0.577 |
| Sleep latency | 69.2 ± 8.1 | 64.3 ± 6.8 | 0.082 |
| Deep sleep | 4.1 ± 4.5 | 3.9 ± 3.2 | 0.974 |
| 20.5 ± 5.6 | 26.2 ± 7.3 | 0.053 | |
| Respiratory analysis | |||
| RDI REM | 17.7 ± 14.5 | 14.7 ± 18.5 | 0.224 |
| RERA | 2.2 ± 2.1 | 1.6 ± 1.7 | 0.469 |
Analyzed using Mann Whitney Test
Discussion
In this study, symptoms with the highest mean value was nasal congestion (VAS > 5), indicated uncontrolled rhinitis, but there was no difference in allergic and non-allergic rhinitis group. This finding is similar to a study done by Bacahu et al. [7] where nasal congestion was present in 59% patients with allergic rhinitis. In a similar study done by Tamasauskiene et al. [8] there was also no differences found regarding the TNSS symptoms in allergic and non-allergic rhinitis. According to Braido et al. [9], patient’s adaptive ability is not based on the severity of the disease, in other words, patient’s perspective on allergic rhinitis does not correlate with the persistency and severity of rhinitis. This offer a possible explanation that the diagnosis of allergic rhinitis is often under diagnosed despite patients having severe symptoms.
The NOSE scoring system is a valid, reliable, and responsive instrument used to measure the degree of nasal congestion and have been used widely in many literatures [10]. However, there are some limitation regarding the use of NOSE, such as the implication of nasal trauma, nasal deformities, septal deviation, and history of allergic rhinitis, which is an independent predictor of high NOSE scores [10, 11].
From the sleepiness screening tools (ESS and PSQI), majority of chronic rhinitis subjects showed disturbance in sleep, represented with excessive daytime sleepiness (ESS score > 10) and poor quality of sleep (PSQI.
ESS score in the allergic rhinitis was also found to be higher compared to the non-allergic rhinitis group. These findings might be explained by higher nasal congestion in the allergic rhinitis group, as demonstrated by a study done by Hiraki et al. [12] which stated that nasal congestion corelates with excessive daytime sleepiness and high ESS scores, meaning that allergic rhinitis could cause SDB due to nasal congestion and the role of pro-inflammatory mediators, that includes histamine, leukotriene, cytokines, chemotactic factors, and enzymes.
In this study, there were no difference in the mean value of PSQI in allergic and non-allergic groups. These findings are in contrast to a meta-analysis by Liu et al. [13], showed that between four studies that compared PSQI score between allergic rhinitis group and control group, the allergic rhinitis group have higher PSQI score, sleep disorder scores, and sleep latency scores compared to their counterparts. Several mechanism have been proposed to these findings, including the overproduction of proinflammatory cytokines that directly induced fatigue, rhinitis symptoms and the pathophysiology of rhinitis that indirectly affects sleep quality, histamine effect on sleep–wake cycle, as well as the effect of autonomic dysfunction on sleep quality [14].
Our study showed an increase in percent total time of light sleep, that were 69.2% in allergic and 64.3% in non-allergic group. In sleep study, sleep is comprised into 5 stages: wake, N1, N2, N3, and REM. In sleep, N1 and N2 stage are regarded as “light sleep”, the lightest stage of sleep and begins as greater than half of the alpha waves are replaced with low-amplitude mixed-frequency (LAMF) activity. The tone of respiratory skeletal muscle is still maintained and breathing progressed at a stable rate. N1 stage typically last from 1 to 5 min, consisting of around 5% of the total cycle, while N2 stage is around 50% of total cycle [15]. The deep sleep or N3, is known to be characterized with delta waves, and is set apart by the presence of a slower frequency and have greater amplitude waves. In this stage, the person have lower chance to be awaken from sleep than any other stages. As we age, people tend to have less time in this slow, delta wave sleep and more time in the light sleep stage [15]. N3 sleep is depicted to have the highest arousal threshold, nevertheless, when a person is woken up in this stage, the person will eventually experience a “mental fogginess”, or better known as sleep inertia, in which they will have impaired mental performance for a brief 1/2-h until 1 h. In N3 sleep, our body exalts in cells and tissues growth, muscle and bone growth and build stronger immunity [15]. Our study found that the percent total time of deep sleep was not disturbed, approximately 20%.
Sleep latency, one of the most important parameters in sleep study, is the duration of time when the patient is trying to fall asleep, until the time patient actually falls asleep. Sleep latency is measured by EEG and behavioural parameters changes consistent with sleep. Normal mean sleep latency is between 10 and 20 min [15]. Our study found reduced sleep latency, less than 5 min in both groups, which is considered as diagnostic characteristic of daytime sleepiness. However, similar to Liu et al. [13], we did not find any differences on sleep onset latency between allergic and non-allergic rhinitis.
In contrast, this study clinically found a decrease in total percent time of REM stage as low as 10.9% and 9.5% in allergic and non-allergic rhinitis. REM is a type of sleep that is characterized by low-voltage and various frequency brain wave activity unsynchronized, muscle atonia, and bursts of rapid eye movements. REM sleep in OSA has been associated with increased events of obstructive episodes and prolonged oxyhaemoglobin desaturation, as the respiratory muscles are atonic in REM sleep. REM sleep should contribute to 25% of total sleep time [15].
Proposed mechanisms for allergic rhinitis include higher serum proallergic cytokines (IL-1β, IL-4, and IL-10), and found to be associated with increased latency to the onset of REM sleep and shorter duration of REM sleep. This suggests that the allergic group may be more inclined to have drowsiness and excessive daytime sleepiness than the non-allergic group. In a study done by Liu et al. [13] allergic rhinitis group identified with increased sleep quality scores, sleep disturbance scores, and sleep latency scores on the PSQI. Allergic rhinitis group was also found to be linked with a greater chance of sleep disorders, including insomnia, nocturnal enuresis, restless sleep, SDB, OSA, and snoring.
However, our study showed no difference between allergic and non-allergic groups. The predicted mechanism that underlies this study in chronic rhinitis is, despite clear difference in pathophysiology, both in allergic rhinitis and non-allergic rhinitis, the increased nasal resistance results in negative pressure of the pharynx, adding factor for upper airway collapse during sleep as the patient is lying in a supine position [16]. Moreover, a chronic eosinophilic inflammation that modifies to the activation of neuronal reflex, such as nasopulmonary reflex that will lead to alveolar hypoventilation [13].
In a study done by Zheng et al. [16], both allergic rhinitis and non-allergic rhinitis are associated with the occurrence of OSA, even though no difference found in the PSG parameters which comprised of stage 1 sleep time, stage 2 sleep time, REM, total sleep time, apnea–hypopnea index, oxygen desaturation index and sleep efficiency.
This study found presence of RDI REM and RERA in both groups. In respiratory analysis, RERA is defined by a respiratory parameter that shows arousal associated with a respiratory event and an increase effort for breathing. A greater effort for breathing ensues subsequently as a response to the increase of upper respiratory tract resistance, which is one of the factor in the pathophysiology of SDB [15].
In this study, respiratory analysis parameters have a tendency to be higher in the allergic rhinitis group compared to the non-allergic rhinitis group, RDI-REM (17.7 ± 14.5 vs. 14.7 ± 18.5) and RERA (2.2 ± 2.1 vs. 1.6 ± 1.7). Earlier studies have concluded that nasal congestion in AR is a primary contributor to the increase in the number of apneic episodes, RERAs, that are microarousals that cause disturbance in sleep [17, 18]. This study hypothesized that inflammation situationally paralyzed upper airway structures, thus would preferentially narrow air passages during REM due to REM stage–specific skeletal muscle atonia. As demonstrated by Kimura et al. [19], an increase in nasal resistance has a direct association with the nasal cycle occurring primarily around REM sleep, and never occurs during non-REM (NREM) sleep.
In another study by Huseni et al. [20] in 145 children with OSA alone and OSA with rhinitis, rhinitis is not associated with more severe OSA and children with rhinitis have more REM-related upper airway obstruction independently of confounding factors. These findings are in general agreement with prior data reported in adults.
Limitation
We realized, our limited sample size was our study limitation. With a larger sample size, we might obtained a higher statistical power among the results. Therefore, further investigation with a larger sample size was needed to see the applicability of our result in the community.
Conclusion
Our study found that sleep disturbance existed in chronic rhinitis, presented by the excessive daytime sleepiness and the impairment in sleep architecture. However, this study showed no differences in the severity of nasal symptoms, sleepiness/sleep quality, and PSG parameters between the allergic rhinitis and the non-allergic rhinitis groups. Different type of inflammation did not give different degree of disturbance. Further studies with larger sample is needed to achieve more reliable results.
Author Contributions
All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by NI, RSW, NLP, and IR. The first draft of the manuscript was written by NI and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. Conceptualization: NI, RSW, NLP, and IR. Methodology: NI, RSW, NLP, and IR. Formal analysis and investigation: NI, NLP, and IR. Writing—original draft preparation: NI, IR. Writing—review and editing: NI, RSW, NLP, and IR. Supervision: NI.
Funding
This study was funded by PUTI QI Universitas Indonesia Agreement letter NKB-1324/UN2.RST/HKP.05.00/2020. Addendum letter NKB-3933/UN2.RST/HKP.05.00/2020. Record of transfer BA-345/UN2.RST/PPM.00.03.01/2021.
Declarations
Conflict of interests
The authors have no relevant financial or non-financial interests to disclose.
Consent to Participate
Informed consent was obtained from all individual participants included in the study.
Consent to Publish
Patients signed informed consent regarding publishing their data.
Ethical Approval
This study was performed in line with the principles of the Declaration of Helsinki. Approval was granted by the Ethics Committee of the Faculty of Medicine, University of Indonesia with regards of the protection of human rights and welfare in medical research. Ethics approval number: KET-122/UN2.F1/ETIK/PPM.00.02/2020.
Footnotes
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