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Volume 13 No. 02
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Accepted Papers





Scientific Investigations

Dynamic Volume Computed Tomography Imaging of the Upper Airway in Obstructive Sleep Apnea

Robert J. Fleck, MD1; Stacey L. Ishman, MD, MPH2,3,4; Sally R. Shott, MD2,4; Ephraim J. Gutmark, PhD, DSc4,5; Keith B. McConnell, MS3; Mohamed Mahmoud, MD1,6; Goutham Mylavarapu, PhD3; Dhananjay R. Subramaniam, MS5; Rhonda Szczesniak, PhD3,7; Raouf S. Amin, MD3,8
1Division of Radiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH; 2Division of Pediatric Otolaryngology - Head and Neck Surgery, Cincinnati Children's Hospital Medical Center, Cincinnati, OH; 3Division of Pulmonary Medicine, Cincinnati Children's Hospital Medical Center, Cincinnati, OH; 4Department of Otolaryngology - Head and Neck Surgery, University of Cincinnati School of Medicine, Cincinnati, OH; 5Department of Aerospace Engineering and Engineering Mechanics, CEAS, University of Cincinnati, Cincinnati, OH; 6Department of Anesthesia, Cincinnati Children's Hospital Medical Center, Cincinnati, OH; 7Division of Biostatistics and Epidemiology, Cincinnati Children's Hospital Medical Center, Cincinnati, OH; 8Department of Pediatrics, University of Cincinnati School of Medicine, Cincinnati, OH

ABSTRACT

Study Objectives:

To describe a dynamic three-dimensional (3D) computed tomography (CT) technique for the upper airway and compare the required radiation dose to that used for common clinical studies of a similar anatomical area, such as for subjects undergoing routine clinical facial CT.

Methods:

Dynamic upper-airway CT was performed on eight subjects with persistent obstructive sleep apnea, four of whom were undergoing magnetic resonance imaging and an additional four subjects who had a contraindication to magnetic resonance imaging. This Health Insurance Portability and Accountability Act-compliant study was approved by our institutional review board, and informed consent was obtained. The control subjects (n = 41) for comparison of radiation dose were obtained from a retrospective review of the clinical picture-archiving computer system to identify 10 age-matched patients per age-based control group undergoing facial CT.

Results:

Dynamic 3D CT can be performed with an effective radiation dose of less than 0.38 mSv, a dose that is less than or comparable to that used for clinical facial CT. The resulting dataset is a uniquely complete, dynamic 3D volume of the upper airway through a full respiratory cycle that can be processed for clinical and modeling analyses.

Conclusions:

A dynamic 3D CT technique of the upper airway is described that can be performed with a clinically reasonable radiation dose and sets a benchmark for future use.

Citation:

Fleck RJ, Ishman SL, Shott SR, Gutmark EJ, McConnell KB, Mahmoud M, Mylavarapu G, Subramaniam DR, Szczesniak R, Amin RS. Dynamic volume computed tomography imaging of the upper airway in obstructive sleep apnea. J Clin Sleep Med. 2017;13(2):189–196.


INTRODUCTION

Obstructive sleep apnea (OSA) is a common disorder that manifests as repeated upper airway (UA) obstruction during sleep. Increasing prevalence of OSA in both pediatric and adult populations has been associated with increasing obesity and metabolic syndrome in the overall population.1,2 It is estimated that up to 5% of adults and 3% of all children in the United States are affected by OSA.1,3 In children, OSA is associated with excessive daytime sleepiness, hyperactivity, attention deficit disorder, failure to thrive, cardiometabolic problems, and neurocognitive deficits.4

As part of the evaluation of OSA, imaging of the UA in patients with OSA has traditionally been performed with magnetic resonance imaging (MRI), computed tomography (CT), and/or fluoroscopy during natural sleep, drug-induced sleep, or wakefulness to evaluate airway size, configuration, and dynamics. Commercially available MRI scanners produce static images that are used to identify UA soft-tissue targets amenable to surgical modification, such as enlarged adenoid or lingual tonsils, macroglossia, elongated soft palate, or enlarged turbinates.5 Additionally, current MRI scanners can provide detailed dynamic single-slice images of the airway during respirations that can be used to create a cine image of airway showing movement dynamics and pattern of collapse.6,7 Overall, MRI provides detailed information,6,810 but is limited to only single-slice cines. Although three-dimensional (3D) cine images obtained with compressed sensing techniques11,12 or multiple two-dimensional planes obtained simultaneously13 are available at advanced research sites, they are not yet available clinically.

BRIEF SUMMARY

Current Knowledge/Study Rationale: Dynamic 3D CT produces a unique 3D dynamic dataset for evaluation of the upper airway for clinical or research use. Dynamic 3D CT can be performed with a radiation dose less than that of a static examination of the exact same anatomy imaged for a facial CT for common clinical indications.

Study Impact: Dynamic 3D CT is an alternative method capable of obtaining a uniquely dynamic 3D dataset for the evaluation of obstructive sleep apnea in patients with persistent, problematic sleep apnea and could be used to guide surgical treatment to result in better outcomes. The effective radiation dose for dynamic 3D CT is equal to or less than that of a facial CT, setting a benchmark for use of the technique.

CT of the UA and cine CT have also been described previously.8,14,15 However, with the advent of slip-ring and multi-detector CT technology, cine CT covering a wider anatomic area is now possible.16,17 Wide-detector scanners, with 256–320 detector rows, are sufficiently wide to image the UA from the nasal passages to the glottis during each rotation with high temporal resolution to stop motion and create a dynamic 3D dataset. For the current study, we modified and applied this method to the UA patients undergoing an imaging study during a sleep study for OSA aimed at creating a realistic model of UA dynamics. The purpose of this study was to describe a dynamic 3D CT technique for the UA, set a benchmark for radiation exposure requirements for this technique, and compare the radiation dose to that used for common clinical studies of an identical anatomical area (e.g., clinical facial CT).

METHODS

Subjects

This evaluation of the UA in OSA was approved by our institutional review board; informed consent was obtained for four subjects for prospective study and four additional subjects were retrospectively obtained from the clinical picture-archiving computer system. We performed a Health Information Portability and Accountability Act-compliant prospective study of dynamic 3D CT of the UA in four children with Down syndrome with OSA [subset of participants in the DYMOSA study (R01HL105206-01)] who were under drug-induced sleep for MRI evaluation between February 2013 and June 2013 (prospective subjects group). The four retrospective, clinical patients all had a contraindication to MRI (clinical subjects group), but did have dynamic 3D CT only between July 2012 and June 2013. Prior to imaging, all study subjects had undergone adenotonsillectomy and postoperative polysomnography to document persistent OSA (Table 1). The study subjects did not have concomitant pulmonary disease.

Polysomnography data for study subjects.

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Table 1

Polysomnography data for study subjects.

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The control subjects (n = 41) were obtained from a retrospective review of the picture-archiving computer system to identify age-matched patients undergoing facial CT between August 2012 to June 2013 for consideration of cranial facial surgery and trauma. The reason for using facial CT is twofold; first, facial CT has the same anatomical coverage as dynamic 3D CT and second, facial CT is often used for planning craniofacial surgery, which is sometimes a consideration in patients with OSA. The required information for calculating radiation dose and area of coverage were recorded. The control group was divided into subgroups based on age, and effective dose was calculated for comparison to individual age-matched study subjects.

Computed Tomography

All study subjects (both prospective and clinical) were anesthetized with dexmedetomidine and permitted to breathe spontaneously via the native airway using a protocol described previously.18 Depth of sedation was assessed using the University of Michigan Sedation Scale.19 After MRI was completed, the prospective subjects were transferred to the CT scanner and positioned with their head and neck in neutral position while anesthesia and adequate oxygenation were maintained. Patients with a contraindication to MRI (the clinical subjects) were transferred directly from induction to the CT scanner. All imaging was performed on a 320-slice volume CT scanner (Aquilion ONE, Toshiba, Otawara, Japan) and reconstructed using AIDR 3D with a FC18 reconstruction kernel.20 After scout views of the head and neck were obtained, the scan length was set to extend from the nasal air passages to the subglottic region, thus covering the entire nasal air passages, nasopharyngeal airway (NPA), retroglossal airway (RGA), and hypopharynx. The number of gantry rotations was determined by the respiratory interval in milliseconds (ms) divided by the gantry rotation speed (350-msec/rotation) such that the period of imaging covered one respiratory cycle. Because the respiratory cycle was relatively stable, the scan duration was calculated by dividing the minute respiratory rate into 60 sec. Therefore, if the respiratory rate was 24 breaths per minute, scanning was performed for 2.5 sec. The maximum z-axis coverage was 16 cm and could be decreased in 2-cm increments to fit each patient's requirements. Low-dose principles based on noise tolerance by radiologists were used when determining the dynamic 3D CT parameters.21 The tube voltage was determined as either 80-kVp or 100-kVp depending on each patient's age and size (cranial diameter). The cranial diameter was measured from the sagittal scout views as the distance from the soft tissues over the frontal bone to the soft tissues of the occiput. The tube current was based on the frontal occipital diameter obtained from the scout views and determined by the formula:

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The effective dose for all studies was calculated using the method of Deak and colleagues.22 For comparison of radiation doses, at least 10 age- and size-matched facial CT images were used as controls for each age group.

Image Reconstruction

The images were reconstructed from half-scans, which results in a number of images that are two times the number of gantry rotations. A half-scan is a reconstruction using 180° of the gantry rotation data. These dynamic temporal phases were reviewed at a workstation (Vital Images, Inc., Minnetonka, MN, USA) that allowed for simultaneous viewing of multiplanar and 3D reformats in static phases and as cine loops in multiple planes. The anterior-posterior (AP), transverse (Tx), and cross-sectional areas were measured at the narrowest section of the NPA and the RGA, above the epiglottis. Dynamic motion was defined by a greater than 50% reduction in the airway cross-sectional area, and collapse was defined by a greater than 80% reduction in cross-sectional area.23 The images also were assessed independently for quality on a four-point Likert-type scale (0-non diagnostic, 1-adequate, 2-good, and 3-excellent image quality) by two radiologists with 10 and 15 y of experience. Motion blurring was assessed on individual dynamics as either present or not present and expressed as a percentage of dynamic temporal phases in the CT study.

Airway Analysis

The NPA and RGA were measured transversely through the narrowest section when fully distended, and the same slice was measured throughout the respiratory cycle. The UA is a dynamic structure.8 To express this dynamic behavior, we introduce the term fractional collapse (FC), which yields a dimensionless fraction from 0 to 1.0 determined by the formula:

jcsm.13.2.189a-e2.jpg
where Dmax is the maximum dimension and Dmin is the minimum dimension.

FC is expressed as the degree of collapse in the Tx, AP, or cross-sectional area values. Collapse is defined as FC greater than 0.80, because it would greatly limit airflow from a fluid mechanics perspective, and dynamic motion is defined as FC greater than 0.50 based on observations in adults that the airway in patients with OSA is more dynamic than patients without OSA.8,24 Stable is defined as FC less than 0.50, which is an unproven, arbitrary limit.

Statistical Analysis

The radiation doses of the control groups were calculated in relation to an eight-number summary for comparison to the individual doses calculated for the study subjects. Values outside of the lower and upper quartiles or the 95% confidence intervals for the controls were reported. Demographic differences between the study subjects and the respective control group for each were examined by the Wilcoxon Mann-Whitney test, and Fisher exact test for continuous and categorical variables, respectively. Values of p < 0.05 were used to determine significance throughout the analysis.

For each subject, the actual airway dimensions (AP, Tx, and cross-sectional area) for both the RGA and NPA were plotted over time. A smoothing curve with a cubic B-spline basis function25 was applied to each measure to obtain an overall indication of the longitudinal course of the airway opening, closing, and reopening during the respiratory cycle.

RESULTS

The first clinical study (Subject 5) was performed prior to the prospective group, and the additional clinical studies (Subjects 6, 7, and 8) were performed after the prospective patients were enrolled and imaged. The radiation doses for Subjects 1 (first prospective) and 5 (first clinical) were substantially more than the doses for the remaining six subjects (Table 2). This was due to subsequent modification of the dynamic 3D CT parameters to minimize the dose while maintaining adequate quality.

Comparison of study subjects with age- and size-matched control subjects.

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Table 2

Comparison of study subjects with age- and size-matched control subjects.

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All studies were of diagnostic quality, and the airway was reformatted for viewing as both a multiplanar image (Figure 1) and a 3D-surface-rendered cine movie (Video 1 in the supplemental material) using a commercially available automated segmentation tool (Vital Images, Inc.). The demographic characteristics of each study subject are summarized in Table 3. There were no significant differences in any of the measured demographic parameters between the study subjects and the age-matched control groups (n = 41) used for determining radiation dose. However, because of incomplete height and weight data for the control group, the cranial AP and Tx diameters of each of the control age groups are reported in Table 4. The cranial AP and Tx diameters of the study subjects are included in Table 3. Most of the subjects had smaller AP and Tx cranial diameters than the corresponding age-matched control group. The effective dose for each of these groups is reported in Table 4.

Volume-rendered surface display of air-filled structures and face in Subject 3, a 3-y-old boy with obstructive sleep apnea and Down syndrome.

(A) Fully distended airway during expiration; retroglossal airway widely patent (arrowhead), nasopharyngeal airway widely patent (small arrow), soft palate outlined by air in the oral cavity (long arrow). (B) Airway collapse during inspiration; hypopharyngeal and retroglossal collapse (arrowheads), nasopharyngeal airway widely patent (small arrow), soft palate outlined by air in the oral cavity (long arrow), oral cavity cut off from the airway. The facial surface is in the image to show the location of the nose (N) and mouth (M).

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Figure 1

Volume-rendered surface display of air-filled structures and face in Subject 3, a 3-y-old boy with obstructive sleep apnea and Down syndrome.

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Demographics for obstructive sleep apnea study subjects.

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Table 3

Demographics for obstructive sleep apnea study subjects.

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Effective dose and cranial diameter for control groups.

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Table 4

Effective dose and cranial diameter for control groups.

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Dynamic 3D CT studies were performed with a radiation dose that is within the range of radiation exposure used for facial CT, as shown by the effective dose calculated for each subject (Table 2). Multiphase, dynamic CT scans of the UA for all eight of the study subjects were performed at an effective dose equal to or lower than that for a standard facial CT. In fact, four of the eight were at a dose below the fifth percentile for the facial CT controls. Blurring due to motion was present in two subjects from the prospective group (Subjects 2 and 3), but only visible on lung window. Reconstruction and measurements were not affected because the true surface was evident, utilizing full width at half-maximum measurement and display techniques established for CT.26 However, 61% of Subject 1 images and 86% of Subject 4 images showed no blurring. In all cases, image quality was judged by both readers as excellent.

The measures of the NPA and RGA are summarized in Tables 5 and 6, respectively, and include the FC. We found that the motion of the airway was strongly dynamic. Three patterns of airway motion were noted: stable (FC < 0.50), dynamic motion (FC > 0.50), and collapse (FC > 0.80). FC is used to express the degree of collapse in the Tx, AP, or cross-sectional area values. It was possible to identify different dynamic behavior of the airway (see Tables 5 and 6), such as the complete multilevel collapse observed in Subjects 1 and 4, the stable non-collapsing airway observed in Subject 2, or the dynamic but noncollapsing airway observed in Subject 3 (Video 1). Airway dynamics of the NPA and RGA of all eight study subjects are summarized in Table 7.

Nasopharyngeal airway measurements and fractional collapse for prospective subjects.

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Table 5

Nasopharyngeal airway measurements and fractional collapse for prospective subjects.

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Retroglossal airway measurements and fractional collapse for prospective subjects.

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Table 6

Retroglossal airway measurements and fractional collapse for prospective subjects.

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Summary of dynamics of the nasopharyngeal and retroglossal airways for prospective subjects.

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Table 7

Summary of dynamics of the nasopharyngeal and retroglossal airways for prospective subjects.

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The three patterns of airway motion (stable, dynamic motion, and collapse) are illustrated in Figure 2. Each graph summarizes the cross-sectional area of the NPA and RGA over the time of the dynamic 3D CT. The data were smoothed with a spline function. Subject 2 (Figure 2A) had a NPA that was relatively stable and RGA with intermittent collapse. Subject 3 (Figure 2B) had a paradoxical movement of the NPA and RGA relationship due to occlusion of the retro-palatal airway during expiration.27 Subject 4 (Figure 2C) had a very dynamic concomitant collapse of both the NPA and RGA.

Fractional collapse of the NPA and the RGA over a respiratory cycle.

NPA = nasopharygeal airway (represented by the solid blue line), RGA = retroglossal airway (represented by the dashed yellow line). The respiratory cycle was repeated three times to show the pattern repetition, but it was only imaged once. (A) Subject 2, with a relatively stable NPA, but very dynamic collapse of the RGA. (B) Subject 3, with a relatively dynamic NPA with fractional collapse of 0.55 and a very dynamic collapse of the RGA (see also Video 1 in the supplemental material). (C) Subject 4, with a very dynamic collapse of both the NPA and RGA.

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Figure 2

Fractional collapse of the NPA and the RGA over a respiratory cycle.

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DISCUSSION

The primary purpose of this report is to describe a dynamic 3D CT technique that can be used to evaluate the entire UA, including the dynamic movement in patients with OSA, and establish the effective radiation dose comparable to that used for control subjects undergoing standard CT studies. We think that having a benchmark radiation dose and a description of the technique is important for clinical and research communities treating OSA. We demonstrate the feasibility of acquiring high-quality dynamic images of the UA by CT at relatively low radiation dose. Furthermore, the image resolution was sufficient to delineate the UA contour and quantify the dynamic profile of the UA.

In this study, four subjects (the prospective subjects) were undergoing a clinically indicated sleep MRI for OSA as described by Donnelly7; cine MRI is the primary imaging modality for evaluation of children with persistent OSA at our institution. However, some patients cannot undergo cine sleep MRI because of artifact caused by metal-containing oral appliances or implanted devices (e.g., pacemakers) that are not magnetic resonance compatible.7 In this study, we included an additional four patients who were scanned by dynamic 3D CT only because of contraindications for magnetic resonance (the clinical subjects). Dynamic 3D CT of the UA is a viable alternative to cine sleep MRI and has several advantages; (1) the examination is brief, (2) spatial resolution is better than MRI, (3) temporal resolution is better at 175 msec per dynamic temporal phase, (4) data are much easier to segment, (5) bony structures are amenable to automated segmentation for 3D images and cephalometric measurement, and most importantly, (6) a dynamic 3D dataset can be obtained of the entire UA simultaneously with isotropic resolution for later reconstruction and analysis. This last aspect is something that is not currently available with clinical MRI.

Other advantages for dynamic 3D CT of the UA exist. The CT scanner is quiet compared to a magnetic resonance scanner so that imaging can be performed during natural sleep without arousing the patient. However, MRI has been used during natural sleep in many settings13 and magnetic resonance scanners are becoming equipped with novel “silent modes” of scanning that are substantially quieter.28 The acquisition of a 3D dataset of the UA, inclusive of the nasal air passages, can be used for computational fluid dynamics modeling of air flow in the UA2931 and ultimately modeling of fluid structure interaction, which is a method of combining computational fluid dynamics scans and interactions with the surrounding structures to predict the movement of the airway during breathing. The goal of such a model would be to predict change in airway dynamics based on an intervention, such as a surgical procedure. Ultimately, this could lead to new and better procedures to remedy OSA.

Use of dynamic 3D CT of the UA does have disadvantages, the most obvious of which is exposure to ionizing radiation. However, we have demonstrated that this type of study can be performed with a radiation dose comparable to that used during routine indications for imaging the same anatomic area of the body. Facial CT and this type of dynamic upper airway CT both contain the facial bones and glottis in all cases and therefore is directly comparable. In light of the serious repercussions of recurrent OSA and its effects on the patient's heart, vascular and metabolic systems, and mental status,1,2 we would argue that dynamic 3D CT utilizes a reasonable radiation dose that is comparable to that used for anatomic imaging obtained to guide surgical treatment when MRI cannot be employed.5 Initially, the radiation dose for Subject 5, the first subject on whom this technique was used, and Subject 1, the first prospective subject, was extrapolated from experience in lowering the radiation dose in abdomen and chest studies and converted to a formula based on AP cranial diameter.21,32 However, because the goal was to extract information about the airway soft-tissue interface and bony structure, we pushed the dose lower for the remaining subjects. Image quality was favorably received and all cases were easily viewed and reconstructed using automatic segmentation at a commercially available workstation. Our current technique is similar to that described in the Methods section, but we now are using fixed voltage (kVp) and electric current (mA) as depicted in Table 8.

Scan settings for Toshiba Aquilion ONE (Toshiba, Otawara, Japan) scanner.

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Table 8

Scan settings for Toshiba Aquilion ONE (Toshiba, Otawara, Japan) scanner.

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Limitations of this report include the small number of study subjects enrolled and no direct comparison to the MRI findings. Also, inspiration and expiration were tracked, but were not measured at the time of CT. Airflow and mask pressure were measured in the induction room, which is something we plan to do in future research studies. Additionally, the generalizability of the information presented here is limited to wide detector-array CT scanners. Performance of dynamic imaging on other multidetector CT scanners is technically possible, but the extent of z-axis coverage would be limited by the number of detectors and their configuration, and radiation exposure and temporal resolution may differ between vendors. As well, the number of gantry rotations and scanning parameters would be different based on gantry rotation speed.

In summary, dynamic 3D CT of the UA provides a unique 3D dataset with high spatial and temporal resolution of the dynamic motion of the entire UA simultaneously, which can provide important information about the dynamic patterns of collapse in OSA. The ease of rendering the bony structures and soft-tissue structure into multiplanar and 3D displays of the airway motion is invaluable for identifying structures that contribute to airway collapse to aid surgical planning. Additionally, these airway data can be segmented into a model that utilizes both computational fluid dynamics and fluid structure interaction modeling for virtual surgical planning.

Dynamic 3D CT of the upper airway can be performed with a radiation dose less than that of a facial CT and provides a unique 3D dataset with high spatial and temporal resolution depicting dynamic motion of the entire upper airway simultaneously, which can provide important information about dynamic patterns of collapse in OSA.

DISCLOSURE STATEMENT

This was not an industry supported study. This study was supported by National Institutes of Health grant (RO1HL105206-01). The authors have indicated no financial conflicts of interest.

ABBREVIATIONS

3D

three-dimensional

AP

anteriorposterior

CT

computed tomography

Dmax

diameter maximum

Dmin

diameter minimum

FC

fractional collapse

kVp

kilovoltage potential

mA

milliampere

MRI

magnetic resonance imaging

ms

millisecond

mSv

millisievert

NPA

nasopharyngeal airway

OSA

obstructive sleep apnea

RGA

retroglossal airway

Tx

transverse

UA

upper airway

ACKNOWLEDGMENTS

The authors are grateful to J. Denise Wetzel, CCHMC Medical Writer, for critical review of the manuscript.

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Supplemental Material

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