Comparing upper airway awake exploration, drug-induced sleep endoscopy and natural sleep—a systematic review

Introduction

Background

Traditionally, the assessment of obstructive sleep apnea (OSA) patients has relied on cervicofacial profiling and awake upper airway (UA) exploration. However, this approach merely allows the observation of static anatomical traits, failing to provide insights into the dynamic behavior of these structures when the UA muscle tone diminishes during sleep. Some authors even contend that only the evaluation of palatine tonsils is reliable in awake UA exploration (1). Many physical traits observed in OSA patients, such as retrognathia, highly arched palates, palatine tonsil hypertrophy, septal deviations, and inferior turbinate hypertrophy, are also present in otherwise healthy individuals without snoring or OSA (2). Additionally, imaging studies using computer tomography (CT) scans and magnetic resonance have revealed disparities in obstructed areas between awake and sleeping OSA patients (3).

Rationale and knowledge gap

To replicate the collapse observed during sleep, various maneuvers, such as the Müller maneuver (MM) and simulated snoring, have been proposed to transform static exploration into a dynamic one. Numerous studies have compared dynamic awake exploration with UA sleep endoscopy, yielding conflicting results (4-12). Although the ideal exploration would occur during natural sleep, it is impractical in daily practice. This limitation was addressed in 1991 when Croft and Pringle first introduced sleep nasendoscopy, now known as drug-induced sleep endoscopy (DISE) (13). DISE offers the opportunity to assess the UA in a pharmacologically induced state simulating natural sleep. The key question is whether this pharmacologically induced sleep state can replicate natural sleep and if conducting endoscopy during this induced sleep state provides additional information compared to awake exploration.

Objective

The objective of this paper is to systematically review the literature comparing DISE with natural sleep, particularly focusing on UA collapse, and to analyze which aspects of awake exploration might correlate with the UA collapse observed in DISE. We present this article in accordance with the PRISMA reporting checklist (available at https://joma.amegroups.com/article/view/10.21037/joma-23-36/rc).

Methods

Data search

Two authors (P.M.R.d.A. & S.M.Q.) independently conducted a search in PubMed/MEDLINE, Cochrane Database, Google Scholar, and Scopus/Embase in December 2023. Table 1 outlines the search strategies for each database. Additionally, a manual search of the references in selected articles was performed.

Eligibility criteria

This review considered studies conducted in adults with OSA. Papers published in languages other than English or those without available full text were excluded. The search was restricted to studies involving human subjects, and single case reports were excluded.

Results

A total of 877 publications were identified. After removing duplicates, reviewing titles and abstracts, and applying inclusion and exclusion criteria to the full text, 22 articles were selected. An additional 14 articles were added after a manual review of references, resulting in the inclusion of 36 studies in this systematic review. Figure 1 depicts the flowchart of the procedure, and a summary of the included studies is provided in Table 2.

Figure 1 Selection of articles included in the systematic review comparing drug-induced sleep endoscopy with natural sleep and awake exploration.

DISE vs. natural sleep

Fifteen studies compared natural sleep with sleep under different drugs, analyzing various parameters of collapse and respiration (14-28). All studies were prospective cohort studies. Table 3 presents the different parameters studied and their similarities or differences between natural sleep and DISE. Notably, Ordones et al. compared target-controlled infusion (TCI)-propofol DISE vs. zolpidem-induced sleep (25). Another article suggested that zolpidem, with its short half-life and minimal impact on UA collapsibility, could be comparable to natural sleep (41).

DISE vs. awake exploration

Twenty-one articles attempted to compare awake exploration and DISE, with results being non-uniform and sometimes contradictory. Among these studies, 14 were prospective cohort studies (4,6-9,11,12,29,30,32,34,35,38,39), five were retrospective cohort studies (31,33,36,37,40), and two were retrospective case series (5,10). Table 4 outlines the aspects of awake exploration (both static and dynamic) positively or negatively correlated with DISE collapse.

Discussion

DISE vs. natural sleep

The studies comparing natural sleep with sedation using propofol or midazolam conclude that the UA collapse observed in those situations is similar and therefore DISE represents natural sleep (14,19,21,25,26). There were no differences in the pattern or the degree of collapse at any UA level (25,26), although one study demonstrated a slightly higher degree of obstruction with midazolam (26). This finding might be related to the longer duration of DISE compared to natural sleep (≥20 vs. <20 minutes respectively). Abdullah et al. reported that midazolam did not cause deeper muscle relaxation compared to natural sleep (14). Propofol administered with a TCI pump also conferred muscle relaxation similar to natural sleep (21). Nevertheless, propofol has a central inhibitory effect on the respiratory muscles and, if administered in higher doses, produces a relaxation of the genioglossus muscle that increases the UA collapsibility (19,42,43). Therefore, it is of the utmost importance to monitor the depth of the sedation and try to avoid propofol in bolus.

Some studies used the critical closing pressure (Pcrit) in order to compare natural sleep and DISE. For instance, Genta et al. concluded that the Pcrit during natural sleep was equal to the one during DISE (19). However, Maddison et al. observed a higher Pcrit with propofol, although both were linearly correlated (24). This increased collapsibility was likely induced by the depth of sedation. The authors reported reaching bispectral index (BIS) levels lower than 50, whereas the recommended sedation depth in the European position paper for DISE ranges from 80 to 60 (44). It is noted that deeper sedation leads to increased UA collapsibility (45,46).

Civelek et al. did not find differences in the titration pressure of continuous positive airway pressure (CPAP) obtained during conventional polysomnography (PSG) or DISE, reinforcing that both explorations show similar results regarding UA collapse (18).

It is also crucial to determine whether snoring under sedation is comparable to snoring occurring during natural sleep. Despite the administration of high doses of propofol using a TCI pump, Berry et al. demonstrated that snoring in control subjects could not be induced. However, it could be triggered in habitual snorers and patients with OSA (17,27). Koo et al. did not observe differences in the frequency or intensity of snoring (23). Agrawal et al. found a correlation between snoring during DISE and natural sleep, but noted it to be more frequent during DISE (15). Jones et al. reported that the intensity of snoring was higher with propofol compared to natural sleep (22).

These differences might be caused by the different tools used to explore snoring (intensity, frequencies, different microphones between the different studies), more studies are needed in this regard.

No studies comparing dexmedetomidine with natural sleep were found in our review of the literature. Nevertheless, it has shown minimal effect in the UA collapse (42). Moreover, the studies that compare propofol and dexmedetomidine UA collapse in the same patients showed similar patterns and degree of collapse with both (47,48).

Concerning respiratory parameters, the majority of the studies did not find differences between natural sleep and sleep induced with different drugs. No distinction was found in minimum (min) O₂ saturation (sat) values with propofol compared to natural sleep (16,20). Similarly, there were no variations in min O₂ sat or apnea/hypopnea index (AHI) between midazolam-induced sleep and natural sleep (16,19).

Sadaoka et al. compared diazepam to natural sleep, and found no differences in AHI, oxygen desaturation index (ODI), min O₂ sat or mean O₂ sat (28). Only Rabelo et al. found a statistically lower min O₂ sat with propofol, however this was not clinically relevant (85.04% vs. 88.64%, P<0.01). Moreover, the mean O₂ sat and the AHI were not statistically different (27).

UA exploration with no fiberscope vs. DISE

Several authors have discovered that the Friedman tongue position (FTP) is associated with retrolingual collapse in DISE (5,39), while others have reported a correlation between a higher FTP and velum collapse rather than retrolingual collapse (33). However, these findings were not corroborated by den Herder et al., Zerpa Zerpa et al., or Aktas et al., who did not identify any relationship between retrolingual collapse and FTP grade, or as it was originally referred to, the modified Mallampati index (MMI) (10,29,32).

FTP and MMI are suggested to assess the space between the soft palate and the tongue base (49,50). The higher the grade, the smaller the retrolingual or retropalatal space. However, these classifications exhibit significant inter-rater variability, making them unreliable (51).

Harvey et al. demonstrated that patients with a higher FTP were found to have less space in the entire UA, not just in the retrolingual area (52). A high FTP grade was associated with multilevel collapse by several authors (4,36,37). Additionally, Zhao et al. suggested that a high FTP grade may be linked to concentric palatal collapse (40). Patients with a grade IV FTP had an odds ratio (OR) of 4.4 for experiencing a complete circumferential collapse (CCC) after adjusting for age, sex, body mass index (BMI), and tonsil grade. The author explained this phenomenon by the increase in the magnitude of tongue drop, resulting in pharyngeal occupation, antero-posterior central compression, and posterior movement of the lateral margins of the soft palate, constituting a circumferential constriction (40).

Lin et al. assessed various UA parameters and found no relationship between FTP and retrolingual collapse; instead, they reported a correlation between the oropharyngeal collapse observed in DISE and higher tonsil grades (37).

These studies present conflicting results, likely attributed to the diverse anatomical characteristics of the sampled populations and the severity of the disease. Moreover, it is crucial to recognize that the UA collapse is not solely governed by anatomical features. Other factors such as loop gain, muscle responsiveness, and arousal threshold play a significant role, as demonstrated by Eckert et al., underscoring the necessity of observing the UA in a state similar to natural sleep to discern the pattern and areas of collapse (53).

Cervical perimeter was found to be associated with CCC in the palate, as reported by Van de Perck et al. (9), supporting the correlation of BMI and CCC as identified by Ravesloot and de Vries (54).

Static fiberscopy vs. DISE

In the absence of consensus on how to evaluate the UA spaces and volumes by fiberscopy, Van de Perck et al. proposed a new method for awake nasopharyngoscopy. It is based on anatomical features and found compatibility with DISE collapse patterns measured by Kendall’s tau correlation coefficient (τ) (9). The palate is assessed by means of three distinct shapes: (I) the “oval shape”, (II) the “C-shape”, and (III) the “dumbbell shape”. Crowding of the oropharynx corresponds to large palatine tonsils or pronounced pharyngeal pillars relative to the UA dimensions. The tongue base position is assessed according to the visibility of the vallecula: (I) completely visible, (II) partially visible, (III) not visible, and (IV) compression of the epiglottis/contact with the posterior pharyngeal wall/posteriorly located tongue. The shape of the epiglottis is described as normal (slightly concave curvature), flat, or curved (including omega-shape). Four endoscopic features during tidal breathing were significantly correlated with DISE: (I) the position of the soft palate with complete palatal collapse [τ=0.29, 95% confidence interval (CI): 0.07–0.49; P=0.007]; (II) crowding of the oropharynx with oropharyngeal collapse (τ=0.32, 95% CI: 0.04–0.56; P=0.026); (III) a posteriorly located tongue base with complete tongue base collapse (τ=0.32, 95% CI: 0.04–0.60; P=0.046); and (IV) the modified Cormack-Lehane scale with epiglottic collapse (τ=0.45, 95% CI: 0.30–0.58; P<0.001) (9).

The Modified Cormack-Lehane scale was recently adapted for nasopharyngoscopy approach by Torre et al. The aim of this adaptation was to improve the assessment of the patterns of hypopharyngeal airway visualization seen during awake flexible laryngoscopy among patients with OSA (55). Indeed, this new classification method for the retropharyngeal-epiglottic aerospace (RPEA) demonstrated correlation with hypopharyngeal collapse during DISE (9).

Other authors, Joy et al. for instance, used Fujita classification to compare awake static endoscopic exploration with DISE findings. These authors obtained a high sensibility but very low specificity on awake endoscopic exploration for palatal collapse, and a low sensibility (40%) for hypopharyngeal collapse (35).

Another independent element evaluated was the Friedman lingual tonsil hypertrophy (LTH) grade, but no correlation with retrolingual collapse during DISE was found (9). Similarly, neither did the shape of the epiglottis correlate with epiglottic collapse (9).

Pérez-Martín et al. compared retrolingual obstruction in DISE, assessed with VOTE (velum, oropharynx, tongue base and epiglottis) and NOHL (nose, oropharynx, hypopharynx and larynx) classifications, with the one observed in awake endoscopy using Friedman staging and LTH. LTH and Friedman stage on awake exploration were mild predictors of collapse at retrolingual level, showing significant correlation to sleep induced endoscopy in cases with severe retrolingual collapse (12). The lack of uniformity, both in describing anatomical features while awake and in DISE classifications makes it difficult to achieve conclusions in this topic.

Dynamic fiberscopy with maneuvers vs. DISE

MM was first introduced by Sher et al. in 1985 to predict surgical success of uvulopalatopharyngoplasty (UPPP) (56). The patient makes an inspiratory effort while the mouth and the nose are closed, creating a negative pharyngeal pressure that would mimic the UA collapse observed during sleep. Nevertheless, there is no clear evidence that this maneuver is able to reproduce this collapse (57,58), and it is also believed that this collapse is dependent of the inspiratory effort of the patient (59).

Campanini et al. (31) showed that the collapses during the MM and DISE were not equivalent, specifically at the level of the hypopharynx, where there was 59% of disagreement regarding grade and 49% disagreement when morphology was considered. At the oropharynx, they observed a 32% disagreement in terms of the grade of collapse and a 24% of disagreement on its morphology. These findings are consistent with the ones of Bindi et al., who obtained similar results on their prospective study comparing awake exploration with MM and DISE using NOHL classification. Thus, observing differences at the hypopharynx, where MM underestimates the severity of the collapse detecting less than 50% of the obstructions observed in DISE (41.8% vs. 88.3% hypopharyngeal collapse, P=0.000) (11). Fernández-Julián et al. also found fair correlation for velum/tonsil (k=0.41–0.60) and poor (k=0.01–0.20) for tongue-base, lateral pharyngeal wall, and epiglottis (4). Aktas et al. support these findings given that in their study 30% of patients who were identified as having only upper-airway obstruction according to Muller’s maneuver had only obstruction of the lower airway involving the tongue base, epiglottis, or hypopharynx, without upper-airway obstruction (29).

Regarding retrolingual obstruction, awake exploration with MM did not exhibit a significant correlation with DISE in the studies conducted by Pérez-Martín et al., Wang et al., Zerpa Zerpa et al., and Soares et al. (10,12,39). Zerpa Zerpa et al. also found no correlation between awake exploration with MM and DISE concerning retropalatal obstruction (10). Ibrahim et al. reported differences in the grade of collapse at the retropalatal, oropharyngeal, and hypopharyngeal regions, as well as the morphology of the collapse between retropalatal and oropharyngeal areas when comparing awake endoscopic exploration with MM and DISE (34).

Cavaliere et al. used the VOTE classification to compare awake endoscopic exploration with MM versus DISE, reporting differences mostly on the severity of the obstruction at the palate and the tongue, but not at the oropharynx. These authors did not observe differences on the morphology of the collapse for any of the areas analyzed (7). Van de Perck et al. who only found correlation at the oropharynx (r=0.33, P=0.003), but not at other sites of collapse (9).

Rabelo et al. employed Fujita classification, which the authors favored for its simplicity over VOTE or NOHL, to compare awake endoscopic exploration with MM. The study revealed no agreement in the Fujita classification assigned to patients between awake and DISE (Kappa=−0.03) (38).

Lovato et al. introduced the simulated snoring maneuver, placing the endoscope through the nose and the mouth. The agreement with DISE was higher when the endoscope was introduced through the nose in all the levels, hypopharynx included (6). Reproducing snore with the endoscope through the mouth was effective in observing oropharyngeal collapse but failed to reproduce the remaining UA collapses. The agreement between the MM and DISE was also reported in this paper obtaining a moderate agreement just for the oropharyngeal collapse, and no agreement for the remaining collapses. Hence, the simulated snoring maneuver involving the passage of the endoscope through the nose could serve as a viable surrogate to replicate the collapse observed in DISE. However, further evidence is required to establish its efficacy with certainty (6).

Recently, Askar et al. conducted a comparison between MM performed in the supine position and DISE to replicate conditions similar to natural sleep. The authors reported that supine MM accurately predicts the type of collapse in the velum or hypopharynx (lateral, anteroposterior, or concentric) (8). Unfortunately, this conclusion was based on the similar proportion of observed collapses, without employing statistical tests such as Cohen’s Kappa or Kendall’s Tau to assess the equivalence of collapses in both situations. It should be noted that despite the comparable proportions of collapse, the observations of collapse in DISE and MM may differ as they could have been conducted on different patients. Additionally, the authors noted a higher proportion of collapse in the hypopharynx during DISE compared to supine MM. These findings align with the argument made by other authors who assert that hypopharyngeal collapse is underestimated with supine MM, even though oropharyngeal collapse is not (9,30,47).

Concerning epiglottic collapse, it can only be observed during DISE and is not likely to be suspected during awake exploration unless there is an anatomical malformation (7,31,60).

In summary, the consensus among most studies is that dynamic awake exploration underestimates the grade of collapse in the UA. This underestimation is attributed to the physiological muscle hypotonia occurring during sleep, which is more pronounced in patients with OSA.

Limitations

The studies included that performed nasal snoring endoscopy (NSE) had relatively small sample sizes, suggesting the possibility that results might differ with larger sample sizes. A recent systematic review of NSE papers indicated that the soft palate was the most frequently reported site of UA collapse during natural sleep endoscopy, followed by the tongue base, lateral walls, and epiglottis, aligning with previous findings during DISE (61). However, further research is needed in this area. It is conceivable that new tools based on flow appearance or sound analysis could provide a reliable understanding of events during natural sleep without requiring NSE or DISE.

The impact of body position on UA collapse is crucial, particularly in positional patients. However, this review did not delve into this aspect extensively, as many centers perform DISE only in the supine position, and information on other body positions was lacking.

Additionally, there is a gap in the literature regarding publications that compare UA findings while awake with airway evaluation during natural sleep. Despite the prevailing view that DISE represents natural sleep, particularly non-rapid eye movement (REM) sleep, there is a dearth of information concerning REM sleep-related collapse.

Conclusions

The gathered evidence supports the utilization of DISE as an exploration method similar to natural sleep. Awake exploration, whether static or dynamic, lacks good agreement with the types of collapse observed in DISE for many patients. Consequently, up to the present time, no exploration method surpasses DISE in effectively observing the UA collapse in patients with OSA, particularly those in need of alternative treatments to standard positive pressure therapies.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://joma.amegroups.com/article/view/10.21037/joma-23-36/rc

Peer Review File: Available at https://joma.amegroups.com/article/view/10.21037/joma-23-36/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://joma.amegroups.com/article/view/10.21037/joma-23-36/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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