Abstract
Introduction: Obstructive sleep apnoea (OSA) is characterized by repeated episodes of upper airway collapse. A review of literature shows limited and conflicting data regarding impact of upper pharyngeal collapse on severity of OSA and degree of sleepiness. Objective: To evaluate the association of the number of levels and degree of upper airway collapse and severity of OSA. Methods: This is a retrospective study including all patients with OSA over a two-year period. Data regarding neck circumference (NC), body mass index (BMI), nasopharyngolaryngoscopy with Muller’s manoeuvre, Epworth sleepiness scale (ESS) questionnaire and a full night polysomnography were collected. Correlation of the number of sites involved and degree of collapse at each site (velum, lateral pharyngeal wall- Level I, base of tongue – Level II and epiglottis – Level III) with BMI, NC, AHI and ESS were assessed. Results: Of the 144 patients, 98% had collapse at Level I. 80% of patients had multisegmental collapse with 30% having collapse at all three levels. The number of levels and the severity of collapse did not have a proportionate effect on the AHI and ESS and were not directly dependent on the BMI. However, changes in NC had a significant effect on the severity of collapse.Conclusion: Severity of OSA and degree of sleepiness were not directly dependent on the severity and the number of levels of collapse. Since majority of the patients had multi segmental collapse, the study highlights the importance of careful assessment of all levels to tailor management strategies for optimum patient management.
Keywords: Obstructive sleep apnoea, Sleepiness, Airway collapse, Nasopharyngolaryngoscopy
Introduction
Obstructive sleep apnoea (OSA) is characterized by repeated episodes of collapse of the upper airway causing symptoms of loud snoring, daytime sleepiness and sleep apnoea. Of the general population an estimated 1–4% is affected by OSA [1]. Associated excessive sleepiness has adverse effects on cognitive function, job performance and quality of life [2].
The most common anatomical sites of collapse in OSA are the velopharynx and lateral pharyngeal wall, base of tongue and epiglottis [3]. The dynamic nature of this collapsible upper pharyngeal airway is the main factor causing the repeated episodes of sleep apnoea seen in OSA. These potential sites of collapse can be assessed by various techniques like awake flexible nasopharyngolaryngoscopy with Muller’s manoeuvre, drug induced sleep endoscopy (DISE) [3] and dynamic sleep magnetic resonance imaging (MRI). The site and degree of dynamic obstruction at each level can vary quite significantly from partial to complete collapse at single or multiple levels. Accurate assessment of all the involved sites in the upper airway and the total severity of collapse in a patient is essential for deciding on appropriate treatment. Often the decision to consider CPAP, oral appliances and even the type and site of surgery is dependent on the site and degree of upper airway collapse.
Apnoea hypopnoea index (AHI) derived from a full night sleep study is the gold standard objective index to determine the severity of OSA. Epworth sleepiness scale (ESS) score provides a subjective measure regarding the degree of sleepiness in the patient [4]. However, a review of literature shows very scarce and conflicting data regarding the impact of upper pharyngeal collapse on the severity of OSA and degree of sleepiness. Bausamer et al. [5] and Belgu et al. [6] showed no meaningful relationship between AHI, ESS scores and upper airway collapse except at the base of tongue. On the other hand, Schwartz et al. showed significant correlation between AHI scores and collapse at the base of tongue and lateral pharyngeal walls [7]. We hypothesize that in addition to the number of levels, the cumulative degree of collapse also is a contributing factor. Therefore, the aim of the study was to assess the effect of number of levels and degree of collapse on the severity of OSA and subjective sleepiness. We also aimed at evaluating the impact of changes in body mass index (BMI) and neck circumference (NC) on the number of levels of upper airway collapse and severity of collapse at each level.
Materials and Methods
This was a retrospective study done in the department of Otorhinolaryngology in a tertiary hospital situated in South India over a two year period. All adult patients diagnosed to have OSA on a full night polysomnography were included in the study. Patients with acute or chronic infections, benign and malignant lesions of the upper aero digestive tract and those with predominant central apnoea on polysomnography were excluded from the study. Institutional review board approval was obtained prior to the commencement of the study.
The parameters which were collected included BMI, NC, AHI and ESS questionnaire scores. Only patients with ESS scores above 10 were considered to have significant sleepiness. All the patients had undergone an awake flexible nasopharyngolaryngoscopy with Muller’s manoeuvre in the outpatient clinic. The presence of collapse at three levels, the velum and lateral pharyngeal wall (Level 1), base of tongue (Level 2) and epiglottis (Level 3) were documented. The severity of collapse at each level was graded as Grade I - < 25% collapse, Grade II – 25–50% collapse, Grade III – 50–75% collapse and Grade IV - > 75% collapse.
We formulated a scoring system to look at the cumulative effect of collapse at all three levels. For this a score of 1–4 was assigned to the corresponding grades of collapse at each level. The cumulative collapse score for each patient based on the sum of the degree of collapse at each of the three levels was thus determined with a maximum attainable cumulative score of 12.
Summary statistics was used for reporting demographic and clinical characteristics. All categorical variables reported using frequencies and percentages and continuous variables were expressed in terms of Mean (SD). Correlation between ESS, NC and AHI was done by Pearson correlation. t-test was used to compare ESS, NC and AHI when there were 2 groups. For more than 2 groups ANOVA was used. Differences was considered significant at p < 0.05. All the statistical analysis was performed using SPSS 25.0.
Results
A total of 144 patients were included in the study. The mean age was 42years (range 23–68) with a male to female ratio of 8: 1. There was a statistically significant difference in the neck circumference, AHI scores and BMI values between the two genders which was not seen with the ESS scores. 47% of the patients had various types of comorbidities in combination, the most common being hypertension (28%) followed by diabetes mellitus (10.34%), dyslipidemia (15.17%) and hypothyroidism (6.89%) in descending order.
Levels of Collapse
Among the sites of collapse, Level I was the most commonly involved site as seen in 97% of patients. Involvement of Level II was seen in 80% and Level III in 32% of patients. 80% (115) patients had collapse at multiple levels on endoscopy among whom 70 patients had collapse at two levels and 45 patients having collapse at all three levels. The scores for severity of collapse ranged from 0 to 12 with an average of 6.20 (SD = 2.44). 74% of the patients had a score ranging between 4 and 8. Patients having only a single level collapse had a collapse score of 3.17 (SD = 0.966) with an increase to 6.27 (SD = 1.54) and 8.20 (SD = 2.04) for those who had collapse at two and three levels respectively.
A) Level I (Retropalatal Collapse)
Of the 144 patients in the cohort, 98 (67.6%) patients had grade IV severity of collapse at level I, the mean score of the severity of collapse being 3.4 (SD = 1.02). Six (4.1%) patients had grade I collapse followed by 16 (11.6%) and 21(14.5%) having grade II and III collapse respectively (Table 1).
Table 1.
Distribution of patients based on the site and severity of collapse
| Sites of Collapse | N (%) |
|---|---|
|
Level I collapse – Total number < 25 collapse 25–50% collapse 50–75% collapse > 75% collapse Mean severity of collapse(SD) |
141 (97.2) 6 (4.1) 16 (11) 21 (14.5) 98 (67.6) 3.4(1.02) |
|
Level II collapse – Total number < 25 collapse 25–50% collapse 50–75% collapse > 75% collapse Mean severity of collapse(SD) |
117 (80.7) 18 (12.4) 27 (8.6) 37 (25.5) 35 (24.1) 2.2(1.44) |
|
Level III collapse – Total number < 25 collapse 25–50% collapse 50–75% collapse > 75% collapse Mean severity of collapse (SD) |
47 (32.4) 24(16.6) 13 (9) 6 (4.1) 4 (2.8) 0.57(1.01) |
B) Level II (Retrolingual Collapse)
Among the patients in the cohort, 117 patients (80.7%) had collapse at Level 2. The mean degree of collapse was 2.2(SD = 1.44) with many patients having grade III and IV severity of collapse (Table 1).
C) Level III (Epiglottic Collapse)
A total of 47 patients (32.4%) in the cohort showed an epiglottic collapse of which only 10 patients had a severe grade III and IV type of collapse. 13 patients had grade II, and 24 patients had grade I collapse respectively (Table 1).
Relationship of Levels and Severity of Collapse with AHI and ESS
Majority of the patients (87patients − 60.7%) had severe OSA whereas 24.8% (36 patients) were found to have moderate OSA and 14.5% (21 patients) with mild OSA. The cohort was equally distributed (71versus 73 patients) among those with and without significant sleepiness score (< 10 versus > 10).
Most of the patients had involvement of two levels with no statistically significant difference in the AHI and ESS with the number of levels involved. With regards to the severity of collapse, although there was an increasing trend with increases in AHI and ESS this was not statistically significant as shown in Table 2.
Table 2.
Relationship of Levels and severity of collapse with AHI and ESS
| Parameter | Number of levels involved | Severity of collapse | ||
|---|---|---|---|---|
|
AHI Mild (5–15) Moderate (15–30) Severe (> 30) |
2.10 (0.83) 2.11 (0.70) 2.09 (0.72) |
p value:0.99 |
5.48 (2.71) 6.08 (2.47) 6.43 (2.09) |
p value:0.26 |
|
ESS < 10 > 10 |
2.06 (0.74) 2.12 (0.70) |
p value:0.94 |
5.87 (2.29) 6.53 (2.57) |
p value:0.34 |
AHI – Apnoea hypopnoea index; ESS – Epworth sleepiness scale
A) Partial Versus Complete Collapse at each Level
The patients were sub analyzed as those who had partial (< 75%) versus complete (> 75%) collapse at all three levels. There was no statistically significant difference in AHI and ESS between the two groups. (Table 3).
Table 3.
Correlation of AHI and ESS in patients with partial and complete collapse
| Level | Degree of collapse | AHI Mean(SD) |
ESS Mean(SD) |
||
|---|---|---|---|---|---|
| I | < 75% | 36.49(22.71) | p = 0.056 | 10.35(5.31) | p = 0.593 |
| > 75% | 44.68(24.24) | 10.90(5.91) | |||
| II | < 75% | 40.91(24.40) | p = 0.311 | 10.28(5.81) | p = 0.104 |
| > 75% | 45.65(22.61) | 12.09(5.22) | |||
| III | < 75% | 41.85(23.94) | p = 0.530 | 10.62(5.74) | p = 0.211 |
| > 75% | 49.53(28.24) | 14.25(3.50) | |||
AHI – Apnoea hypopnoea index; ESS – Epworth sleepiness scale
B) Single Level Versus Multilevel Collapse
On analysis of patients with multilevel and single level collapse, we found that there was no statistically significant difference between these two groups with changes in the AHI and ESS as shown in Table 4.
Table 4.
Correlation of AHI and ESS among patients with single and multilevel obstruction
| Single level Mean (SD) |
Multilevel Mean (SD) |
p value | |
|---|---|---|---|
| AHI | 36.65 (22.98) | 43.43 (24.15) | 0.175 |
| ESS | 10.86 (5.81) | 10.68 (5.72) | 0.882 |
AHI – Apnoea hypopnoea index; ESS – Epworth sleepiness scale
Relationship of BMI and NC with Levels of Collapse
84% of the patients had a BMI of more than 25 kg/m2 with 54.5% and 29.7% of the patients falling in the overweight (BMI 25–29.9 kg/m2) and obese (BMI > 30 kg/m2) category respectively. 124 (86%) patients had a NC less than 43 cm. There was a statistically significant increase in the severity of collapse in the upper airway with increase in NC (p = 0.001). However, a similar correlation was not seen with the different BMI groups.
Discussion
The prime reason for the symptoms in OSA is collapse of the upper pharyngeal wall causing repeated arousals and disruption of the sleep architecture. Our study showed that though 97% of the patients had a collapse at Level I with a higher degree of collapsibility at the retropalatal level (3.2), 80% of patients had multi segmental collapse with milder degrees of collapse at the retrolingual (2.2) and epiglottic level (0.57) too. This was similar to that seen in the literature where the velopharynx was the most vulnerable site of collapse and often, multiple sites of collapse are seen [8]. Irrespective of the number of levels involved (single versus multilevel) and the severity of collapse (partial versus complete), our study showed that though a rising trend was seen between patients with partial and complete collapse, there was no statistically significant change with both the AHI and ESS scores. Moreover, only NC and not BMI showed a statistically significant correlation with the severity of collapse.
The cross sectional diameter of the pharyngeal wall during wakefulness is much smaller in OSA patients with increase in thickness of the lateral pharyngeal muscular wall when compared to normal controls which makes these patients more at risk of a high degree of collapsibility [9]. The surface tension across the mucosal surfaces of the upper airway is also increased in patients with OSA which gets accentuated with oral breathing causing increased closing pressures [10]. Therefore, an increasing collapsible nature of the upper airway can predispose to increasing severity of OSA and degree of sleepiness. However, the literature does not distinctly reveal what is the impact of upper pharyngeal collapsibility both on the AHI and ESS scores. Also recognizing the levels of obstruction and its severity plays a pivotal role in surgical decision making and counselling regarding management options.
Our study showed that irrespective of the number of levels involved and the severity of collapse there was no statistically significant change in both the AHI and ESS scores. This was discordant with a few relevant articles in the literature. Schwartz et al. showed significant correlation between the severity of OSA and collapse at base of tongue and lateral pharyngeal wall [7]. Similarly, Belgu et al. showed a significant correlation between AHI and collapse at tongue base [6]. A plausible explanation for the lack of a linear relationship between upper airway collapsibility and AHI in our study could be the influence of other static obstructions in the sinonasal region which could also apply a negative pressure on the pharyngeal walls in the sleep state affecting the overall airflow [11]. Since the overall tone of the upper airway musculature is reduced, even minor changes in the upper airway diameter can have profound consequences on the severity of OSA [12].
On comparison between groups of patients with partial and complete collapse at each level, although there was a rising trend with AHI and ESS, these changes were not statistically significant. Also, when comparing patients with multilevel versus single level collapse there was no significant correlation with AHI and ESS. To the best of our knowledge, this finding has not been shown before in the literature indicating that the severity of OSA and sleepiness can vary and shows no relationship whether the obstruction is multilevel or single level type of collapse.
One of our hypothesis was that an increase in the BMI and NC can predispose to increased collapse of the upper airway. However, our study showed that only NC showed a statistically significant correlation with the severity of collapse. This is in contrary to that shown in literature where an increase in BMI has a direct correlation with upper airway collapsibility [13]. Kum et al. showed a significant association between BMI and NC with lateral collapse at the retropalatal and retrolingual areas [14]. OSA in the Asian population is often not associated with obesity and therefore NC rather than BMI tends to be a more effective marker of OSA explaining the greater correlation of upper airway collapse with NC in our study [15, 16].
Although retropalatal collapse is most frequently encountered with a high degree of severity in our study, majority of the patients had multilevel obstruction. However, since there is no significant correlation between the number of levels and severity of collapse with the AHI and ESS, there could be other factors contributing to the severity of OSA. Proper assessment of all the levels of collapse is therefore important to bring about a reduction in total score rather than targeting only one particular level. It was also noted that the average degree of collapsibility was much higher at the retropalatal level (3.2) compared to the retrolingual (2.2) and the epiglottic level (0.57). This signifies that although other sites in the upper airway are also commonly involved, it is often to a lesser degree which can at times remain inconspicuous and left untreated. Often this is a single major cause of failure after OSA surgery leading to residual collapse and persistence of symptoms [17]. The importance of multilevel surgery either as a single or staged procedure with no added risk is therefore highly recommended [18].
Along with targeted surgery, options like CPAP, adequate counselling regarding lifestyle changes and oropharyngeal exercises may also be beneficial [19]. Since the number of levels involved and the severity of collapse are not dependent on the BMI but rather on the NC, emphasis on increasing the tone of the neck muscles can play a very important role in reducing the severity of upper airway collapse.
The limitations of our study is that it was retrospective in nature and therefore inter observer variability in the assessment of the severity of collapse needs to be considered. Collapse of airway was assessed using awake flexible endoscopy and Mullers manoeuvre rather than DISE. Although a number of techniques are available for the assessment of the levels and severity of upper pharyngeal collapse, the need for a standard cost-effective method is important. A flexible nasopharyngolaryngoscopy can be easily performed in the outpatient clinic and is often done as part of routine evaluation in a patient with OSA. Studies have shown high levels of concordance between endoscopy done in the awake status versus drug induced sleep endoscopy especially at the level of the velum and lateral pharyngeal walls [20, 21].
The total scoring system used in this study is a newly devised one. A further prospective study looking into the above parameters will give a better insight regarding association between the levels and severity of pharyngeal collapse and the severity of OSA and sleepiness.
Our study highlights that the severity of OSA and degree of sleepiness were not directly dependent on the severity and the number of levels of collapse. Rather than BMI, NC had a significant effect on the severity of collapse rationalizing the importance of oropharyngeal exercises. Since majority of the patients had multi segmental collapse, careful assessment of all levels to tailor management strategies is required for optimum patient management.
Funding
This study received no funding.
Declarations
Conflict of Interest
The authors declare no conflict of interest.
Ethical Approval
All procedures performed in this study were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. Institutional review board approval was obtained prior to the commencement of the retrospective study.
Informed Consent
Since this is a retrospective study using existing data, informed consent was not required.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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