Background: Drug induced sleep endoscopy (DISE) is hoped to identify reasons of failure of adenotonsillectomy (AT) in treating pediatric sleep disordered breathing (SDB). Maxillomandibular disproportion has been studied as another association which may explain alternative pathogenesis of SDB. We aimed to explore the relation between the size of the gonial angle and inclination of the epiglottis measured from cone beam CT (CBCT) and tongue base collapse based on DISE in children with SDB. Method: A retrospective chart review was conducted at a tertiary pediatric center. Children (6-17 years old) assessed at a multi-disciplinary Upper Airway Clinic, diagnosed with SDB and maxillo-mandibular disproportion (MMD), and who underwent DISE were eligible. Variables obtained from the electronic medical records of the clinic and prospective database included demographics, comorbidities, surgeries performed, investigations, DISE findings and CBCT findings. The gonial angle of subjects with and without tongue base collapse (TBC) on SNP were compared. Results: In total 29 patients (13 male, 8 female) age 6-17 (median= 9) were eligible for the study from January 2009 – July 2016. We included 11 subjects, and 10 comparators. The mean gonial angle of the TBC group was 139.3°± 7.6°, while that of the comparison group was 129.4°±3.5 (mean difference -9.937, 95% CI of -15.454 to - 4.421, P = 0.001, power of test 0.95). Additionally, the mean inclination of the epiglottis had a mild positive correlation (r=0.32, p<0.05) with the gonial angle, in the whole cohort. Conclusions: This pilot study suggests that TBC may be mediated by a wider gonial angle in children with SDB patients. The posterior tilt of the epiglottis on CBCT may be a surrogate sign of TBC. Keywords: Pediatric sleep disordered breathing, Maxillo-mandibular disproportion, Gonial angle, Adeno-tonsillectomy, Drug induced sleep endoscopy, Pharyngeal collapse Background apnea . Current evidence suggests a strong association The American Academy of Otolaryngology – Head and with multiple negative outcomes which include cardiovas- Neck Surgery defines Pediatric sleep disordered breath- cular, metabolic, behavioral and learning consequences, as ing (SDB) as difficulty in breathing during sleep, which well as increased rate of nocturnal enuresis [1–6]. The risk can range from habitual snoring to obstructive sleep factors for SDB include male sex, obesity, African American ethnicity, asthma, and allergies . Given the high prevalence of 4–11% [8, 9], and the negative * Correspondence: email@example.com Presented on the podium at the Annual meeting of the Canadian Society of associations, scrutiny of the pathogenesis of risk factors Otolaryngology Head & Neck Surgery, Saskatoon, Sask, June 2017. and effectiveness of treatment offered is of great University of Alberta, Edmonton, AB, Canada importance. Current guidelines consider adenotonsil- Division of Pediatric Surgery, Department of Surgery, Stollery Children’s Hospital, Edmonton, AB, Canada lectomy (AT) as the first line surgical solution for Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Anderson et al. Journal of Otolaryngology - Head and Neck Surgery (2018) 47:41 Page 2 of 6 pediatric SDB . However, as much as 20 to 40% on drug induced sleep endoscopy (DISE) or imaging of patients treated for SDB with AT fail to improve, [17, 18]. The pharynx may exhibit collapse upon in- resulting in a noteworthy volume who need further spiration in concentrically, lateral wall to lateral wall, treatment [11, 12]. or at thetonguebaselevel . The significance and Although prevalence estimates and the negative out- associations related to each type of collapse has nei- comes of pediatric SDB are well described within the lit- ther been studied nor determined to date. But the erature, there is a paucity of data regarding predictive proponents of DISE argue that its findings may pro- factors for failure of AT . Previously identified inde- vide an insight into the mechanisms of airway dys- pendent risk factors of failure include age, obesity, function for which there may be solutions other than chronic rhinitis, deviated nasal septum and tonsil size. traditional procedures. Therefore, we sought to conduct We expect other patient related variables which are yet an exploratory study to find a phenotypic marker (gonial to be accounted for, or researched, to play a role. In the angle) associated with SDB in which base of tongue late 1800’s Tomes was one of the first to described an collapse is found upon DISE. association with upper airway obstruction and morpho- logical facial changes due to adenoid hypertrophy which Methods he termed “adenoid facies” . Since then research has Study design supported this finding with changes in the nasal passage A retrospective chart review was conducted at the and gonial angle as a result of upper airway obstruction Stollery Children’s Hospital, Edmonton, Alberta, Canada [15, 16]. The gonial angle is that formed by the man- in order to explore the relationship between the gonial dibular plane and ramus, Fig. 1. A large gonial angle angle and pharyngeal collapse at the base of tongue in would indicate backwards (clockwise) rotation of the children with SDB. This study received IRB ethics ap- mandible causing the tongue/tongue base to be situated proval (Pro00067134). Eligible children were those inferiorly-posteriorly and potentially cause pharyngeal assessed at the multidisciplinary Upper Airway Clinic for airway obstruction. Furthermore, it can cause the devel- a combination of persistent symptoms of SDB and opment of anterior open bite thus promoting or enab- maxillo-mandibular disproportion (MMD) from January ling mouth breathing. Whereas retrognathia indicates a 2009 till July 2016. Disciplines involved in this clinic are small jaw regardless of its angle relative to the horizontal Pediatric Orthodontics, Pulmonary medicine, and plane. They are separate entities, possibly can occur Otolaryngology- Head and Neck Surgery. together or independently. The inclusion criteria comprised ages 6–17 years old, On the other hand, there are two patterns of Pediatric Sleep Questionnaire (PSQ) score over 33 , pharyngeal compromise that may occur in SDB, namely features of MMD requiring radiologic assessment by pharyngeal obstruction or collapse, and can be identified cone beam computerized tomography (CBCT), and hav- ing undergone DISE (and being eligible for operative treatment). All patients were scanned with the same CBCT machine in the seated-natural head position, asked to rest their tongues at the anterior teeth, and the total scan time was 4.8 s. The study group were those who exhibited tongue base collapse (TBC) on DISE, whereas the comparison group did not. We excluded children who had a history of maxillo-facial trauma or surgery, congenital craniofacial abnormalities or syn- dromes, and those who had incomplete data (including those with an incomplete view of the epiglottis or man- dible on CBCT). Variables were collected from electronic medical re- cords, the electronic repository of CBCT, surgical data- base of the otolaryngologist and video documentation of the performed DISE. These included demographics, diagnoses, procedures performed, McGill score for over- night sleep oximetry , gonial angle measurement, in- clination of the epiglottis on CBCT, type of pharyngeal Fig. 1 Lateral 3D image reconstructed from CBCT showing the gonial collapse on DISE, and surgery performed. angle; formed by the mandibular plane (solid line) and ramus plane DISE was conducted using a uniform technique and (dotted line) reported in a structured format that was previously Anderson et al. Journal of Otolaryngology - Head and Neck Surgery (2018) 47:41 Page 3 of 6 validated. The patients were kept spontaneously breath- The assessor of the gonial angle and the epiglottic in- ing throughout the assessment in the operating room, clination was unaware of the type of collapse in the using Remifentanyl 2–2.5 mcg/ml and infusion rates of pharynx. The subjects were recruited from a database Propofol varying from 200 to 350 mcg/kg/min titrated which was intended for use in another project. for response to stimulation . DISE was always con- ducted under the same anesthetic where the surgery Outcome measures planned will take place. The primary outcome measure was the difference be- tween means of gonial angles of study and comparison groups. The secondary outcome measure was the correl- Measures ation between epiglottic inclination and gonial angle. A certified maxillo-facial radiologist conducted two one-on-one training sessions for a senior medical stu- Statistical analysis dent on preforming the CBCT measurements. The med- Basic descriptive statistics were conducted to obtain the ical student measured the angle of the mandible (gonial mean and standard deviation of the angle of mandible angle) and inclination of the epiglottis. Prior to perform- and the inclination of the epiglottis. An independent ing the actual measurements, an intra and inter-rater as- sample T-test was used to assess the statistical variance sessment on a sample (n = 10) of patients, not included between the study and comparison gonial angles. in this pilot, demonstrated 0.95 agreement (Cohen’s Pearson r correlation analysis and r statistics were con- kappa) between the student and the expert. ducted between the angle of mandible and inclination of Prior to any measurement, the CBCT volume was ad- the epiglottis. All analyses were conducted and com- justed such that the Frankfort plane (eye-ear plane) and pleted using SPSS 23. interorbital line were parallel to the horizontal plane, and any right-left rotations were corrected. The gonial Results angle, as conventionally described, was that between the In total 29 eligible patients, 18 male and 11 female ages intersection of the ramus and the mandibular lines 6–12 (median = 9) were identified (Fig. 1). Eighteen of (Fig. 1). The inclination of the epiglottis was whom met the inclusion criteria as study group, and 11 measured as the angle at the intersection between the as the comparator group (Table 1) and Fig. 3. Seven pa- horizontal plane and a line drawn through long axis tients out of the study group and one out of the com- of the epiglottis (Fig. 2). The latter was chosen based parator group were excluded, Fig. 2. As a result, we on an observation by the multidisciplinary group of a included 11 (seven males) valid subjects and 10 (six were possible association between large gonial angle and males) valid comparators. In the comparison group, four posterior tilt of the epiglottis, which may affect air- patients exhibited lateral and six circumferential flow into the laryngeal inlet. pharyngeal collapse upon SNP. The median age for the study group was 9 years (range = 6–12) and 7 (range 6–13). for the comparison group. Comorbidities and types of surgeries are summa- rized in Table 1. AT was the most common surgery per- formed followed by adenoidectomy. There was no difference between the parameters of the sleep oximetry between the two groups (Table 2). The mean gonial angle of the study group were 139.3° ± 7.6° (95% CI 134.8–143.8), as opposed to 129.4° ± 3.5° (95% CI 127.2–131.6) in the comparison group which were significantly different (p < 0.01). The mean difference is − 9.937 (95% CI of − 15.454 to − 4.421, P = 0.001). The effect size is 1.675 and is large. Since the study group values were not normally distrib- uted, Mann Whitney test was also run and the difference between the medians was still significant. However, the mean difference between the epiglottic inclination in the study (123.0° ± 4.6°) and the comparison groups Fig. 2 Sagittal CBCT image showing the inclination of epiglottis; the (121.45° ± 6.94°) was 1.932 (95% CI -3.389 to 7.252, P = angle formed by the long axis of epiglottis (dotted line) relative to the 0.457), which was not significant, but the test was short horizontal plane (solid line) of the recommended power of 0.8 (0.05). Anderson et al. Journal of Otolaryngology - Head and Neck Surgery (2018) 47:41 Page 4 of 6 Fig. 3 Recruitment of patients for inclusion and account for exclusions Analysis of our secondary outcome showed that within Our exploratory study demonstrated that the children the whole cohort, inclination of the epiglottis had a mild with SDB and MMD who exhibited TBC has a larger positive correlation (r = 0.32, p < 0.05) between gonial mean gonial angle (139.3° ± =7.6°), than their counter- angle and inclination of the epiglottis. parts who exhibit different types of collapse (129.4° ± 3.5°), and more than the reported mean values of gonial angle for this age group in the literature Discussion (133.96° ± =7.6°) . A mild positive correlation (r = Current recommended first line surgical treatment for 0.32, p < 0.05) was also found between the size of the SDB is AT . However, given the significant pro- gonial angle and the inclination or posterior tilt of the portion of patients who fail to receive benefit from epiglottis. This suggests that downward growth of the such treatment, evidence providing insight into pre- mandible might be associated with that particular type dictors of the pathophysiology of patients SDB could of pharyngeal tongue collapse. reduce unnecessary and ineffective surgical proce- This is the first study to investigate how dynamic dures. Gonial angle, was chosen based on the clinical endoscopic findings during chemically induced sleep can observation of the interdisciplinary airway team relate to static 3D imaging (CBCT) in children with during the six years’ experience in the clinical and SDB. There is a surging interest into the role of imaging radiographic assessment of children with MMD and in assessing SDB in children and specifically in ortho- Snoring/Sleep Disordered Breathing. dontic and maxillofacial literature . In the adult lit- erature, a systematic review was conducted to assess the Table 1 Comparison between means of gonial angle of the study most important anatomical characteristics of the upper and comparison group. 95CI: 95% confidence interval airway related to the pathogenesis of obstructive sleep Parameter Subjects (n of 11) Comparison (n of 10) Male: female 7:4 6:4 Table 2 Sleep oximetry parameters Age in years (median & range) 9 (6–12) 7 (5–12) Parameter Subjects Comparison Comorbidities McGill Oximetry Score Chronic rhinitis 4 5 1 3 (27%) 0 (0%) Obesity 0 1 2 5 (46%) 7 (70%) Asthma 1 2 3 3 (27%) 3 (30%) Surgeries performed 4 0 (0%) 0 (0%) Adenotonsillectomy 6 5 Mean Desaturation Index ± SD 6.4 ± 4.6 7.2 ± 5.5 Tonsillectomy 1 2 Mean Sa02 Saturation ± SD 96.1 ± 2.2 95.7 ± 3.1 Adenoidectomy 4 3 Mean Sa02 Nadir ± SD 86.2 ± 5.4 83.8 ± 6.5 Anderson et al. Journal of Otolaryngology - Head and Neck Surgery (2018) 47:41 Page 5 of 6 apnea by analyzing the three-dimensional parameters different between SDB and normal patients (mean of (using different imaging modalities) of the airway col- 36.0° range of 34.0°– 41.5° versus a mean of 30.5° and umn. The minimum cross-sectional area was the only range of 27.0°–33.0°, p < 0.05). This study correlated one that was reduced consistently in obstructive sleep cephalometric, two-dimensional measures with a dy- apnea (OSA) patients. The majority of the studies were namic assessment of pharyngeal collapse, along the same of fair quality and quite heterogenous precluding a lines of the current work. meta-analysis . Another systematic review, this time Further epidemiological and biological studies are war- in the pediatric literature , indicated that multiple ranted to confirm this association and to provide further cepahlometric measures of children diagnosed with insight into biological mechanisms for purported associ- MMD are statistically different between those who were ation. The concept of measuring a dynamic soft tissue asymptomatic and those with primary snoring and/or structure in a static cone beam CT is far from accurate. SDB. However, given the modest differences demon- However, we attempted to standardize patient posture strated, the clinical significance was deemed question- and use small scan time thus reducing chances of mo- able. Alsufyani et al.  in a review of the literature tion or multiple breathing cycles. We are aware of our indicated that several modalities had been used to per- small sample size, and the lack of polysomnographic form three-dimensional analysis and measurements of data which prevents us from making any generalizable the airway of SDB patients before and after treatment, conclusions to the larger population, nor establishing a including magnetic resonance imaging, multi-detector dose response relation. However, given this is an ex- computed tomography and CBCT. The group commen- ploratory study, and the first to investigate the correl- ted that aside from the well known inherent advantages ation between gonial angle, the static inclination of the and disadvantages of each modality (expense, radiation epiglottis and dynamic TBC in children with SDB, find- exposure, physics inadequacies) the authors highlighted ings are valuable for hypothesis generation for future the challenges remaining with respect to image acquisi- larger scale studies. tion, three-dimensional reconstruction and analysis. Thus far nearly all the work concentrates on static mea- Conclusions sures (be them two dimensional of volume related) and The preliminary observation indicates that tongue base how they relate to cross sectional polysomnographic pa- collapse is associated with a large gonial angle, which rameters and their changes after various treatment lines. provides a hypothesis for a phenotypic marker that could Some of this work is in support of our observation. explain persistence of SDB after traditional AT. For example, Finkelstein et al. , in 2000 studied a group of children with nasal obstruction and counter- Abbreviations CBCT: Cone beam computed tomography; DISE: Drug induced sleep endoscopy; parts without, all of whom did not have tonsillar en- MMD: Maxillo-mandibular disproportion; OSA: Obstructive sleep apnea; largement and were otherwise healthy. They explored PSQ: Pediatric Sleep Questionnaire; SDB: Sleep disordered breathing; the relation between cephalometric measures and the se- SNP: Sleep nasopharyngoscopy; TA: Adenotonsillectomy; TBC: Tongue base collapse verity of their symptoms (5 grade severity ranging from none to nasal obstruction with universally observed Availability of data and materials snoring and obstructive symptoms during sleep – but no The datasets during and/or analyzed during the current study available from objective or validated sleep parameters). An increased the corresponding author on reasonable request. gonial angle was associated with increased symptoms Authors’ contributions which was statistically significant, and interestingly SM, NA and HE were responsible for the inception, planning / protocol, ERB within the values which we reported and more than application, data collection, analysis, writing and revision. MG and AI were those reported for normative values, although including responsible for the data collection, analysis and revision. All authors read and approved the final manuscript. wider age group than ours. In another clinical study by Iwasaki and coinvestigator , after treating 28 subjects Ethics approval and consent to participate with rapid maxillary expansion, a significant increase in This study received IRB ethics approval (Pro00067134). pharyngeal airway volume was demonstrated which they related to improvement in tongue position. Consent for publication Appropriate consent obtained. However, the study that may lend support to our work was done by Watanabe and colleagues . In a study of Competing interests the impact of body habitus and craniofacial parameters The authors declare that they have no competing interests. on pharyngeal closing pressures, SDB adult patients were found to have receded mandibles, with longer faces Publisher’sNote and downward mandibular growth. The angle reflecting Springer Nature remains neutral with regard to jurisdictional claims in the development of the mandible was significantly published maps and institutional affiliations. Anderson et al. Journal of Otolaryngology - Head and Neck Surgery (2018) 47:41 Page 6 of 6 Author details J Otolaryngol Head Neck Surg. 2017;46(1):37. [cited 29 Nov 2017]. Available Department of Dentistry, Faculty of Medicine and Dentistry, University of from: http://www.ncbi.nlm.nih.gov/pubmed/28476166 Alberta, Edmonton, Canada. Department of Oral Medicine and Diagnostic 14. Tomes CS. The bearing of the development of the jaws on irregularities. Sciences, College of Dentistry, King Saud University Division of Dent Cosm. 1873;115:292–6. Otolaryngology-Head and Neck Surgery Department of Surgery, Riyadh, 15. Linder-Aronson S, Woodside DG, Lundström A. Mandibular growth direction 3 4 Saudi Arabia. University of Alberta, Edmonton, AB, Canada. Division of following adenoidectomy. 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Published: Jun 4, 2018