Anatomical Basis of Sleep-Related Breathing Abnormalities in Children with Nasal Obstruction

ORIGINAL ARTICLE Anatomical Basis of Sleep-Related Breathing Abnormalities in Children With Nasal Obstruction

Yehuda Finkelstein, MD; David Wexler, MD; Gilead Berger, MD; Ariela Nachmany, MA; Myra Shapiro-Feinberg, MD; Dov Ophir, MD

Objective: To define, in a group of children with nasal tified in patients prone to obstructive breathing pat- obstruction, the anatomical differences that differenti- terns: increased flexure of the cranial base and bony na- ate those with quiet, unobstructed nocturnal respira- sopharynx, opening of the gonial angle, shortened tion from those with obstructive sleep-related breathing mandibular length, dorsocaudal location of the hyoid, re- abnormalities (snoring and obstructive sleep apnea). duced posterior airway space, and increased velar thick- ness. Design: Case series. Conclusions: A number of anatomical abnormalities may Patients: Fifty-nine children aged 3 to 13 years (35 boys contribute to sleep-related abnormal breathing in oth- and 24 girls) with nasal obstruction and without tonsil- erwise normal children with nasal obstruction. Our re- lar hypertrophy, known craniofacial syndromes, or neu- sults suggest that symptomatic children show some of romuscular diseases were included in the study. the same skeletal and soft-tissue configurations that are found in adults with obstructive sleep apnea. While ad- Main Outcome Measures: Each patient was catego- enoidectomy is generally an effective treatment in chil- rized as to severity of nocturnal obstructive breathing dren with obstructive sleep-related breathing abnormali- symptoms. Angular and linear cephalometric measure- ties, the underlying craniofacial variances that remain after ments were used for assessment of craniofacial features. adenoidectomy may predispose these patients to rede- Clinical symptom scores were correlated with the cepha- velopment of obstructive breathing abnormalities in adult- lometric measurements. hood.

Results: Significant craniofacial abnormalities were iden- Arch Otolaryngol Head Neck Surg. 2000;126:593-600

ANIFESTATIONS of up- adenotonsillar hypertrophy. Children with per airway obstruc- adenoidal hypertrophy have nasal obstruction are common in tion with consequent chronic mouth children. An esti- breathing. However, some of these chil- mated 12% of children present with mouth breathing as an dren exhibit habitual snoring,1 and about isolated manifestation, while others de- M 2 1% suffer from obstructive sleep apnea. velop SRBAs of varying severity, from snor- Snoring and other sleep-related breathing to obstructive sleep-disordered breathing abnormalities (SRBAs) may be asso- ing. In most of these children, snoring and ciated with deleterious effects, including SRBAs are cured if the obstruction of the From the Palate Surgery Unit impaired daytime psychomotor perfor- nose is removed, usually by adenoidec- (Dr Finkelstein and mance, enuresis, hyperactivity, and poor tomy. In our experience and according to Ms Nachmany), Department of sleep quality.1,3,4 Several predisposing ana- reports in the literature, parents report that, Otolaryngology–Head and tomical and physiologic factors have been after surgical treatment, “they now have Neck Surgery (Drs Wexler, identified in children with SRBAs. These a different child” who is more alert and ac- Berger, and Ophir), and include localized sites of narrowing in the tive in all respects.5 Department of Radiology upper airways, neuromuscular disorders, It is not yet known why some chil- (Dr Shapiro-Feinberg), Meir and major craniofacial abnormalities, such dren with obstructive adenoid hypertro- Hospital, Sapir Medical Center, Kfar Saba; and the Sackler as Stickler syndrome, Crouzon syn- phy develop SRBAs while others with iden- School of Medicine, Tel-Aviv drome, Treacher Collins syndrome, and tical nasal obstruction remain otherwise University, Tel Aviv Pierre Robin syndrome. asymptomatic chronic mouth breathers. A (Drs Finkelstein, Berger, and The broadest subset of children with lack of correlation between adenoid size Ophir); Israel. SRBAs comprises those with obstructive and severity of apnea has also been docu-

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©2000 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 PATIENTS AND METHODS In addition, special attention was paid to malocclusion, mainly anterior open bites and overjet of the maxillary in- PATIENTS cisors. Lateral cephalometric radiographs were obtained for Fifty-nine healthy children ranging in age from 3 to 13 years all subjects. For 38 patients, the radiographs were taken (mean ± SD, 8.6±3.1 years) were included in this study. in an authorized laboratory. Standard technique was em- There were 35 boys and 24 girls. Forty-six patients se- ployed: The patients were instructed to fix their distant gaze lected had nasal obstruction caused by adenoid hypertro- on an imaginary horizon to reproduce their habitual oc- phy and 3 patients had obstructions caused by severe chronic clusion, with the lips together, and to allow the tongue to rhinitis with symptoms persisting at least 3 months. Ex- relax in the floor of the mouth. Exposures were taken with clusion criteria were tonsillar enlargement, personal or fam- the patient slowly exhaling through the nose. Exposures ily history of neuromuscular disorder or craniofacial syn- were optimized to demonstrate both the bony landmarks drome, and obesity. and the superimposed soft tissues. For the remaining 21 patients, the cephalometric measurements were made from METHODS lateral head radiographs. To allow correction for projec- tion enlargement of the linear measurements, these radio- The determination of obesity was made according to pe- graphs were made with a 10-mm round steel median cali- diatric growth charts. A thorough history was recorded for bration marker in place. The head was oriented in the each patient following a structured interview format ap- Frankfurt plane. plied in a consistent fashion. Each patient was accord- The cephalometric landmarks, angles, and linear mea- ingly classified as to level of obstructive symptom severity: surements are defined in Table 1 and shown in Figure 2. Grade Symptoms 0 Oral breathing with no snoring STATISTICAL ANALYSIS 1 Mild snoring or snoring only while sleeping on back Mean±SEM was calculated for each variable at each level 2 Habitual snoring in all positions of symptom severity. Correlation coefficients were deter- 3 Habitual snoring associated with a history of mild mined by the Pearson method for the associations be- to moderate apnea and/or restless sleep tween the cephalometric variables and symptom severity. 4 Habitual snoring associated with a The Pearson correlation method was also used to test the marked clinical presentation of apnea and restless sleep relationships of the craniofacial variables with age and the relationships of each craniofacial variable with the others. Ears, nose, and throat examination was performed with Analysis of variance was used to determine statistically sig- special attention to mouth breathing, daytime loud oral nificant differences of individual cephalometric variables breathing during wakefulness, adenoidal face (ie, long face), at each level of symptom severity. Between-sex differ- steep mandibular planes, and receding chin (Figure 1). ences were tested by independent t test.

mented.6 These discrepancies point to a lack of under- Cephalometric analysis has been used to character- standing of the substrates of SRBAs in children. ize skeletal and soft tissue relationships in adults with Two hypothetical mechanisms have been sug- SRBAs.9-14 Cephalometry can provide extensive data on gested to explain how nasal obstruction may induce the landmarks pertinent to the upper airways. However, SRBAs.7 According to the functional theory, upper air- correlative data between cephalometric parameters and way obstruction could lead to apneas via disturbed re- children with SRBA symptoms are sparse. Therefore, we flex mechanisms, possibly trigeminally or vagally medi- studied a series of children with chronic nasal obstruc- ated, that normally act to preserve airway patency in the tion without tonsillar hypertrophy, without any known presence of negative pressure in the upper airway.8 Con- craniofacial anomaly, and without hypotonia or neuro- tributing factors might be poor tone of the pharynx and muscular disease. tongue during sleep, leading to collapse of the orophar- Our hypothesis is that specific anatomical patterns ynx and obstruction. According to the mechanical theory, correlate with obstructive symptom severity in children with a direct mechanical effect—ie, with obstruction or with nasal obstructions. The present study was de- narrowing of the upper airway—the pressure gradient for signed to define the anatomical markers by craniofacial airflow increases and the pressures within the upper air- cephalometric evaluation of nonsyndromic young pa- way become more negative relative to the atmospheric tients who develop SRBAs in the presence of nasal ob- pressure. This could lead to a greater tendency toward struction. This is one component of our research pro- airway closure. gram on development of a general structural analytic We believe that airway stability during sleep is re- model of sleep-related upper airway obstruction. lated to structural parameters of the upper airways and that even the airflow-related soft tissue movements dur- RESULTS ing sleep are influenced by the underlying structural limits. We therefore decided to systematically study the skel- The summary of patient clinical data for each symptom etal and soft tissue relationships in children with nasal severity level is given in Table 2. A clear increase in like- obstruction in hopes of clarifying why some children with lihood of adenoid facies (Figure 1) and audible mouth nasal obstruction exhibit SRBAs while others do not. breathing during wakefulness is noted with higher lev-

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©2000 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 Figure 1. A 10-year-old girl with a typical adenoidal face (ie, long face, steep mandibular planes, receding chin, and the lips parted at rest, with a relatively short upper lip).

els of sleep-related obstructive breathing. Thirty-one pa- toms, although the absolute difference was small, on the tients underwent adenoidectomy, and obstructive breath- order of a millimeter. Two derived measures, DTH/ ing was relieved in all patients. However, 3 patients had GnGo (ratio between the dorsal tongue height and GnGo) residual mild snoring after adenoidectomy. and MPH/GnGo (ratio between the distance from the man- Correlations between symptom severity and indi- dibular plane to the hyoid and GnGo), were positively vidual cephalometric measurements are given in Table 3. correlated with worsening of symptoms. Decreasing cranial base angles (BaSN [angle formed by Cross-correlation between cephalometric variables the intersection of lines drawn from the nasion to the sella demonstrated a number of statistically significant inter- and from the sella to the basion] and BaSPNS [angle relationships (Table 4). With increasing age, GnGo and formed by the line connecting the basion, sella, and pos- DTH were increased. With decreasing BaSN, there was terior nasal spine]) (compare Figure 3 with Figure 4) a tendency of BaSPNS and GnGo to decrease and of SNA were found to correlate with increasing levels of obstruc- and SNB to increase. With increasing GnGoH, there was tive symptoms. The BaSN was found to be 5.3° smaller a tendency of MPH and GnGo to increase (Figures 3 and in patients with severe obstructions than in asymptom- 4). With decreasing GnGo, there was a tendency of DTH atic patients, a statistically significant difference. Simi- and GnGoH to increase. larly, the BaSPNS was an average of 5° smaller in the se- The mean±SD age of the boys (7.8±3.0 years) was verely affected group, indicating nasopharyngeal significantly lower than that of the girls (10.1±2.6 years). narrowing. Increased gonial angle (ArGoGn) and hyoid The boys (127.7°±5.5°) had a more acute BaSN than the angle (GnGoH) were associated with higher symptom se- girls (130.4°±4.7°) and a more open ArGoGn verity scores (compare Figures 3 and 4). Protrusion of (132.9°±6.6°) than the girls (128.7°±6.3°). the maxilla (SNA [angle from the sella to the nasion to the subspinal point]) and mandible (SNB [angle from the COMMENT sella to the nasion to the supramental point]) did not correlate with patient symptom severity. In this study of children with SRBA, obstructive symp- The length of the mandibular plane (GnGo) and the toms were found to correlate with the following cranio- minimal posterior airway space (MPAS) were inversely facial (and velolinguopharyngeal) differences demon- correlated with symptom levels. Mean mandibular short- strated by cephalometry: skull base angles (BaSN and ening of 8.4 mm was found in the level-4 group com- BaSPNS), GnGo and ArGoGn, hyoid position as given pared with level 0. Decreasing MPAS was significantly by MPH and GnGoH, and MPAS at the level of the tongue correlated with increasing severity of obstruction; the pa- base. Some of these factors are directly interrelated, yet tients with the most severe obstructions exhibited a mean each individually contributes a component of potential MPAS less than 10 mm, in contrast to 14.2 mm for the upper airway compromise. These results are based on mul- asymptomatic group (Figures 3 and 4). Velar width tended tiple statistical correlations and cannot directly prove to be increased in patients with more pronounced symp- causal relationships. Individual statistically significant re-

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Abbreviation Definition Landmarks A Subspinal: the deepest point on the premaxillary outer contour between the anterior nasal spine and the central incisor Ar Posterior ramus plane: the intersection of a line along the posterior border of the mandible and the inferior border of the basilar occipital bone (basicranium) ANS Anterior nasal spine: the most anterior part of the nasal floor B Supramental: the deepest point on the outer contour of the mandible between the point of the chin and the incisor teeth Ba Basion: the midpoint of the anterior border of the foramen magnum Gn Gnathion: the most inferior point in the contour of the chin Go Gonion: the most posterior and inferior point on the convexity of the angle of the mandible H Hyoid: the most anterior-superior point on the body of the hyoid bone N Nasion: the sagittal junction of the frontal-nasal suture line PNS Posterior nasal spine: the most posterior part of the contour of the hard palate S Sella: the center of the hypophysial fossa (sella turcica) DT The highest point of the outline of the dorsum of the tongue Angles ArGoGn Angle formed by the line connecting the articulate, gonion, and gnathion BaSN Cranial base flexure: angle formed by the intersection of lines drawn from the nasion to the sella and from the sella to the basion BaSPNS Angle formed by the line connecting the basion, sella, and posterior nasal spine GnGoH Hyoid angle: angle formed by the line connecting the gnathion, gonion, and hyoid SNA Angle from the sella to the nasion to the subspinal point SNB Angle from the sella to the nasion to the supramental point ANB Angle from the subspinal point to the nasion to the supramental point BaN-ANSPNS Angle formed by the line connecting the nasion and basion (which we call the basal plan) and the line connecting the anterior nasal spine and the posterior nasal spine (which we call the palatal plan) BaN-GnGo Angle formed by the basal plan and the line connecting the gnathion and the gonion (which we call the mandibular plan) Linear Measurements MPAS Retrolingual posterior air space: the minimal distance (in millimeters) between the base of the tongue and the nearest point on the posterior pharyngeal wall MPH The distance between the mandibular plane and the hyoid GnGo The length of the mandibular plane Uw Maximal uvular width: the width of the uvula measured on cross-section at the widest point MPH/GnGo Relative hyoidal distance: the ratio between the hyoidal distance from the mandibular plane and the length of the mandibular plane DTH/GnGo Relative tongue height: the ratio between the tongue height and the length of the mandibular plane

N N S S

BaN-GnGo Ba ANS Ar PNS BaAr PNS ANS

BaN-ANSPNS A A Uw DT DT

MPAS Go MP B Go B

Gn Gn H H

Figure 2. The cephalometric landmarks, angles (left), and linear measurements (right) used in the present study. MP indicates mandibular plane. See Table 1 for expansions of additional abbreviations and definitions.

sults are useful to the extent that they can be confirmed librium12 and do not change greatly from childhood to in subsequent studies and contribute to a coherent ana- adult form.15 Excessive flexure or relatively acute angu- tomical model of obstructed upper airway breathing. lation of the skull base refers to a decreased BaSN mea- Cranial base components (BaSN and BaSPNS) are surement. We found that nearly all the reduction of BaSN considered to be of primary importance in facial equi- in patients with severe obstructions was caused by re-

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Symptom Severity Level*

01234 No. of subjects 13 12 12 10 11 Age, y, mean ± SD (range) 8.9 ± 3.2 (3.5-12.5) 8.8 ± 3.6 (3-13.5) 8.8 ± 2.6 (3-12) 8.3 ± 3.0 (5-13) 8.3 ± 3.3 (3.5-13) Boys/girls, No. 7/6 8/4 6/6 8/2 7/4 Adenoidal facies, No. (%) 3 (23) 7 (58) 9 (75) 9 (90) 9 (82) Audible mouth breathing while awake, No. (%) 0 (0) 0 (0) 5 (42) 5 (50) 8 (73)

*See the “Patients and Methods” section for definitions of the symptom severity levels.

Table 3. Cephalometric Data*

Mean ± SEM Measurement by Symptom Severity Level† P ‡ Cephalometric Measure r 0123 40vs30vs4 BaSN −0.39 130.8 ± 1.1 131.8 ± 1.4 127.5 ± 1 127.4 ± 1.8 125.5 ± 1.8 NS .009 BaSPNS −0.39 58.9 ± 2.7 58.8 ± 1.0 56.7 ± 1.4 56.1 ± 1.6 53.9 ± 1.4 NS .004 ArGoGn 0.40 127.1 ± 1.4 130.7 ± 1.3 131.3 ± 1.8 132.8 ± 2.8 135.8 ± 1.9 .03 .001 GnGoH 0.45 23.2 ± 2.9 24.7 ± 2.4 31.9 ± 1.4 34.8 ± 3.4 34.8 ± 3.0 .003 .003 SNA −0.07 79.2 ± 1.4 77.8 ± 0.9 78.3 ± 0.9 78.8 ± 1.0 79.8 ± 0.8 NS NS SNB −0.05 75.0 ± 1.2 73.6 ± 0.8 73.7 ± 1.1 74.8 ± 0.8 73.8 ± 1.1 NS NS ANB −0.07 4.1 ± 0.6 4.2 ± 0.7 4.6 ± 0.8 4.1 ± 0.9 5.2 ± 0.9 NS NS BaN-ANSPNS 0.00 27.1 ± 1.0 26.2 ± 0.8 27.8 ± 0.9 25.2 ± 1.1 27.2 ± 1.0 NS NS BaN-GnGo 0.39 55.6 ± 1.5 57.8 ± 1.4 58.2 ± 2.3 58.6 ± 2.0 63.4 ± 1.8 NS .001 MPAS −0.48 14.2 ± 0.9 11.0 ± 0.6 10.5 ± 0.9 8.9 ± 1.1 9.8 ± 0.7 Ͻ.001 Ͻ.001 DTH −0.03 52.1 ± 2.9 50.6 ± 2.5 54.4 ± 2.1 49 ± 2.0 52.6 ± 2.1 NS NS GnGo −0.35 67.3 ± 2.2 65.2 ± 2.9 61.4 ± 1.7 60.2 ± 1.9 58.9 ± 1.5 .02 .007 MPH 0.37 12.2 ± 1.5 11.9 ± 1.5 15.7 ± 0.6 16.4 ± 1.7 16.8 ± 1.4 .03 .02 Velar width 0.31 6.6 ± 0.2 7.2 ± 0.2 7.7 ± 0.2 7.6 ± 0.2 7.3 ± 0.2 .005 .053 DTH/GnGo 0.37 0.77 ± 0.03 0.78 ± 0.03 0.89 ± 0.03 0.82 ± 0.04 0.90 ± 0.04 .045 .04 MPH/GnGo 0.44 0.19 ± 0.02 0.18 ± 0.02 0.26 ± 0.08 0.28 ± 0.03 0.28 ± 0.02 .009 .003

*See Table 1 for expansions of abbreviations and definitions. †See the “Patients and Methods” section for definitions of the symptom severity levels. ‡One-way analysis of variance post hoc comparisons.

duction of the BaSPNS, which defines the bony limits of sures of maxillary and mandibular protrusion. Future the nasopharyngeal space. Bacon et al12 noted a similar studies need to determine the compensation factor, which reduction of BaSPNS in adults with obstructive sleep will be derived from BaSN, needed to establish norms for apnea. They found that the reduction in BaSPNS was SNA and SNB. associated with decreased sagittal facial length, which The MPAS is another important measurement in they interpreted as facial and pharyngeal “compres- the evaluation of patients with SRBA. In adults, uvulo- sion.” Thus, it appears that acute angulation of the skull palatopharyngoplasty failure has been shown to corre- base is associated with posterior displacement of the late with MPAS less than 1 cm.17,18 In our study of chil- facial skeleton and shortening of the anteroposterior dren, decrease in MPAS from a norm of 14 mm was dimensions of the pharynx.12,16 In addition, excessive associated with increased clinical symptoms. The most cranial base flexure may play a role in the development symptomatic children had an MPAS as low as 7 mm. We of SRBA; the decreased operating length of the pharyn- found that MPAS had a statistically significant correla- geal dilator muscles compromises their efficiency.13 tion with ArGoGn and GnGo. In the children with a It is well documented that adenoidectomy is effec- more obtuse ArGoGn and a shorter GnGo, the symp- tive is relieving snoring in children because it relieves toms tended to be more pronounced. Since the genio- nasopharyngeal obstruction. Therefore, it is interesting glossus muscle has its origin at the internal surface of to note that 3 of our young patients who had some re- the anterior mandible, both shortening of the GnGo and sidual snoring after adenoidectomy all had excessive cra- an increase in the ArGoGn result in relative retrodis- nial base flexure (117°, 119°, and 119.5°) and reduction placement of the tongue. Furthermore, these mandibu- of the BaSPNS (45°, 50°, and 45°). These findings sug- lar changes result in reduced protrusor mechanical effi- gest that excessive flexure of the cranial base is a risk fac- ciency of the genioglossus muscle,19,20 which could tor for incomplete clinical response to adenoidectomy. contribute to posterior airway obstruction, as the muscle We found no significant correlation between SNA tone is diminished during sleep. or SNB and patient symptom severity scores. This is likely Nasal obstruction induces mouth breathing, a char- due to interdependence between BaSN and these mea- acteristic of so-called adenoidal facies. Mouth breathing

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° 135° 77 79° 61°

Ar Ba PNS

DT A

119° Go TB

19° MP MPAS B H

Figure 3. Left, Cephalometric roentgenogram of a 15-year-old girl who underwent adenoidectomy at age 3 years and suffered from nasal obstruction because of severe rhinitis without snoring. All the craniofacial features are within the normal range. Note that the tongue is normally positioned and the velum rests on it. The facial morphologic characteristics are normal, and the lips are well balanced and competent at rest. She has a class I profile. Right, Cephalometric tracing and analysis. The reference contours, points, and lines used in the study are shown. Arrow indicates the competent lips. MP indicates mandibular plane; TB, tongue base. See Table 1 for expansions of additional abbreviations and definitions.

N S

69° 131° 76° 53°

Ar Ba PNS

DT 135°

Go MP 34°

TB B MPAS H Gn

Figure 4. Left, Cephalometric roentgenogram of the girl shown in Figure 1, showing a posteriorly and inferiorly displaced tongue base and an acute cranial base combined with a dorsocaudal position of the hyoid. Note the anterior open bite, large overjet, steep mandibular plane, large gonial angle, overjet, and high, ogival hard palate. She has a class II profile: a normally positioned maxilla and a retropositioned mandible. Her lips are parted at rest, with the upper lip incompetent or nonfunctional. Right, Cephalometric tracing and analysis. Black arrows indicate shallow palatal arch and narrow mandibular arch. MP indicates mandibular plane; TB, tongue base. See Table 1 for expansions of additional abbreviations and definitions.

is associated with dorsocaudal rotation of the mandible Inferoposterior (dorsocaudal) placement of the hy- about the temporomandibular joint. This mandibular oid bone has repeatedly been shown to correlate with repositioning in turn brings the origin of the genioglos- SRBA in both children23 and adults.9,13,14,17,18,24 In addi- sus muscle into a more posterior and inferior position, tion, in our study, MPH/GnGo and GnGoH were in- with direct narrowing of the MPAS. Also, genioglossus creased in patients with more severe obstructive symp- protrusor mechanical efficacy may be reduced, as seen toms. The overall effects of dorsocaudal hyoid placement with an excessive ArGoGn or a shortened GnGo. These include narrowing of the MPAS and decreased mechani- factors may explain the increased upper airway col- cal efficiency of the genioglossus muscle protrusor ac- lapsibility documented by Meurice et al21 in mouth tion. One reason children with SRBA are often found to breathers. In other words, mouth breathing itself creates sleep with extended-head postures14,25 may be to bring a propensity for pharyngeal airway narrowing and about elevation of the hyoid so as to relieve retrolingual increased collapsibility. Thus, nasal obstruction of an airway obstruction. acute or chronic nature can induce snoring and There is a descent in hyoid position during life. A increases in apnea-hypopnea severity.22 significant relationship was reported between age and the

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Age BaSN BaSPNS ArGoGn GnGoH SNA SNB ANB BaN-ANSPNS MPAS DTH GnGo MPH BaSN NS BaSPNS NS Ͻ.001 ArGoGn NS NS NS GnGoH .045 NS NS .047 SNA NS .001 NS NS NS SNB NS Ͻ.001 NS NS NS Ͻ.001 ANB NS NS NS NS NS .07 NS BaN- NS NS NS NS NS NS NS NS ANSPNS MPAS .049 NS .04 NS NS NS NS NS NS DTH Ͻ.001 NS NS NS NS NS NS NS NS NS GnGo Ͻ.001 Ͻ.001 NS NS .02 NS NS NS NS Ͻ.001 Ͻ.001 MPH .01 NS NS NS .001 NS .049 NS NS NS .002 NS Uw .005 NS .046 NS NS NS NS NS NS .002 NS NS NS

*See Table 1 for expansions of abbreviations and definitions.

MPH during childhood,26 from childhood to adult- taining nasal breathing during childhood is important for hood,26-28 and during adult life.14,28 While in children the preventing alterations of the facial skeleton that reduce hyoid position is related to the development of the lin- upper airway stability during sleep. Nasal obstruction of guomandibular complex, in adults, the dorsocaudal shift- long duration must be avoided throughout the growing ing of the hyoid is probably accentuated by increased body process. Persistent nasal obstruction should be cor- weight.14 Those young patients with SRBA and a dorso- rected surgically early in life, even if, in most cases, the caudally located hyoid, even if cured by adenoidec- original cause will be resolved spontaneously.38 tomy, certainly may be at higher risk to develop SRBA in their adult life as body weight increases. CONCLUSIONS Children are usually respond well to adenoidectomy, in contrast to adults, in whom relief from nasal ob- This cephalometric study of children with nasal obstruc- struction is markedly less successful in curing SRBA. We tion found several structural parameters that correlated believe that SRBA develops as a result of posterior tongue with the severity of the obstructive symptoms. The cepha- displacement during mouth breathing. Accordingly, ad- lometric findings indicate that regional sites of airway nar- enoidectomy is effective in relieving SRBA because the rowing, as well as mechanically disadvantageous con- children revert to nasal breathing with the mouth closed. figurations of the mandible and hyoid, appear to In contrast, adults may exhibit SRBA despite patent na- contribute to sleep-related upper airway collapse. For- sal airway; this appears to be a consequence of cranio- tunately, relief of nasal obstruction by adenoidectomy is facial maturation, including increased nasomaxillary highly effective in improving obstructed breathing in chil- 26-28 height, decreased ArGoGn, and hyoid descent. These dren. Nevertheless, cephalometric analysis reveals cra- changes correspond to vertical elongation of the phar- niofacial patterns that may predispose the patient to a sub- 27,28 ynx and increased tongue height, both of which im- optimal surgical result or redevelopment of SRBA in ply a more unstable mechanical arrangement of the tongue adulthood. Cephalometric analysis may identify a sub- 14,23,25,28 and velopharynx, independent of nasal or naso- set of patients who are at risk for continued obstruction. pharyngeal obstruction. Children exhibit relatively ob- Future studies are needed to clarify whether early sur- lique orientation of the pharynx and a superiorly placed gical intervention for chronic mouth breathing can re- hyoid, which enhance airway stability at the level of the verse some craniofacial substrates of SRBA. tongue. These advantages disappear during transforma- tion toward the adult craniofacial form. Accepted for publication December 22, 1999. Untreated chronic mouth breathing in children might We thank Nava Yellin, MA, for statistical analysis of lead to unfavorable developmental changes in the cra- the data. niofacial complex that predispose the individual to SRBA 29-37 Corresponding author: Yehuda Finkelstein, MD, Pal- in adulthood. Adverse developmental effects of chronic ate Surgery Unit, Department of Otolaryngology–Head and mouth breathing include increased height of the naso- Neck Surgery, Meir Hospital, Sapir Medical Center, Kfar maxillary complex, obtuse ArGoGn, and secondary dor- Saba 44281, Israel (e-mail: [email protected]). socaudal shifting of the hyoid, as has been shown in hu- mans36 and experimentally in monkeys.34,35 This means that children who are chronic mouth breathers develop REFERENCES secondary changes in craniofacial morphologic characteristics that predispose them to adulthood obstructive 1. Ali NJ, Pitson D, Stradling JR. Natural history of snoring and related behaviour sleep apnea.37 Thus, as Guilleminault38 concluded, main- problems between the ages of 4 and 7 years. Arch Dis Child. 1994;71:74-76.

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©2000 American Medical Association. All rights reserved. Downloaded From: https://jamanetwork.com/ on 10/02/2021 2. Gislason T, Benediktsdottir B. Snoring, apneic episodes, and nocturnal hypox- way collapsibility in normal sleeping subjects. Am J Respir Crit Care Med. 1996; emia among children 6 months to 6 years old: an epidemiologic study of lower 153:255-259. limit of prevalence. Chest. 1995;107:963-966. 22. Suratt PM, Turner BL, Wilhoit SC. Effect of intranasal obstruction on breathing 3. Ali NJ, Pitson D, Stradling SR. Snoring, sleep disturbance and behavior in 4-5 during sleep. Chest. 1986;90:324-329. year olds. Arch Dis Child. 1993;68:360-366. 23. Glander K, Cisneros GJ. Comparison of the craniofacial characteristics of two 4. Gozal D. Sleep-disordered breathing and school performance in children. Pedi- syndromes associated with the Pierre Robin sequence. Cleft Palate Craniofac J. atrics. 1998:102:616-620. 1992;29:210-219. 5. Ahlqvist-Rastad J, Hultcrantz E, Svanholm H. Children with tonsillar obstruc- 24. Hochban W, Brandenburg U. Morphology of the viscerocranium in obstructive tion: indications for and efficacy of tonsillectomy. Acta Paediatr Scand. 1988; sleep apnoea syndrome: cephalometric evaluation of 400 patients. J Craniomax- 77:831-835. illofac Surg. 1994;22:205-213. 6. Grundfast KM, Wittich DJ. Adenotonsillar hypertrophy and airway obstruction. 25. Winnberg A, Pancherz H, Westesson PL. Head posture and hyomandibular func- Laryngoscope. 1982;92:650-656. tion in man: a synchronized electromyographic and videofluoroscopic study of the 7. Leach J, Olson J, Hermann J, Manning S. Polysomnographic and clinical find- open-close-clench cycle. Am J Orthod Dentofacial Orthop. 1988;94:393-404. ings in children with obstructive sleep apnea. Arch Otolaryngol Head Neck Surg. 26. Subtelny JD. A cephalometric study of the growth of the soft palate. Plast Re- 1992;118:741-744. constr Surg. 1957;19:49-62. 8. Mathew OP, Abu-Osba YK, Thach BT. Influence of upper airway pressure changes 27. Siegal-Sadewitz VL, Shprintzen RJ. Changes in velopharyngeal valving with age. on genioglossus muscle respiratory activity. J Appl Physiol. 1982;52:438-444. Int J Pediatr Otolaryngol. 1986;11:171-182. 9. Jamieson A, Guilleminault C, Partinen M, Quera Salva MP. Obstructive sleep ap- 28. Tallgren A, Solow B. Hyoid bone position, facial morphology and head posture neic patients have craniomandibular abnormalities. Sleep. 1986;9:469-477. in adults. Eur J Orthod. 1987;9:1-8. 10. Strelzow VV, Blank RHI, Basile A, et al. Cephalometric airway analysis in ob- 29. Cheng MC, Enlow DH, Papsidero M, Broadbent BH Jr, Oyen O, Sabat M. Devel- structive sleep apnea syndrome. Laryngoscope. 1988;98:1149-1158. opmental effects of impaired breathing in the face of the growing child. Angle 11. DeBerry-Borowiecki B, Kukwa AA, Blanks RHI. Cephalometric analysis for diag- Orthod. 1988;58:309-320. nosis and treatment of obstructive sleep apnea. Laryngoscope. 1988;98:226- 30. Linder-Aronson S. Adenoids: their effect on mode of breathing and nasal airflow 234. and their relationship to characteristics of the facial skeleton and the dentition: a 12. Bacon WH, Krieger J, Turlot JC, Stierle JL. Craniofacial characteristics in pa- biometric, rhino-manometric and cephalometro-radiographic study on children tients with obstructive sleep apnea syndrome. Cleft Palate J. 1988;25:374-378. with and without adenoids. Acta Otolaryngol Suppl (Stockh). 1970;265:1-132. 13. Maltais F, Series F, Carrier G, Cormier Y. Cephalometric measurements in snor- 31. Linder-Aronson S. Effects of adenoidectomy on dentition and nasopharynx. Am ers, non-snorers and sleep-apnea patients. Thorax. 1991;46:419-423. J Orthod. 1974;65:1-15. 14. Tsuchiya M, Lowe AA, Pae EK, Fleetham JA. Obstructive sleep apnea subtypes 32. Cohen AM, Orth D, Vic PS. A serial growth study of the tongue and intermaxil- by cluster analysis. Am J Orthod Dentofacial Orthop. 1992;101:533-542. lary space. Angle Orthod. 1976;46:332-336. 15. Engman LT, Spriestersbach DC, Moll KL. Cranial base angle and nasopharyn- 33. Miller AJ, Vargervik K. Neuromuscular adaptation in experimentally induced oral res- geal depth. Cleft Palate J. 1965;2:32-39. piration in the rhesus monkey (Macaca mulata). Arch Oral Biol. 1980;25:579-589. 16. Harris EF. Size and form of the cranial base in isolated cleft lip and palate. Cleft 34. Miller AJ, Vargervik K, Chierici G. Sequential neuromuscular changes in rhesus Palate Craniofac J. 1993;30:170-174. monkeys during the initial adaptation to oral respiration. Am J Orthod. 1982;81: 17. DeBerry-Borowiecki B, Kukwa AA, Blanks RHI. Indications for palatoplasty. Arch 99-107. Otolaryngol. 1985;111:659-663. 35. Tomer BS, Harvold EP. Primate experiments on mandibular growth direction. 18. Riley R, Guilleminault C, Powell N, Simmons FB. Palatopharyngoplasty failure, Am J Orthod. 1982;82:115-119. cephalometric roentgenograms, and obstructive sleep apnea. Otolaryngol Head 36. Woodside DG, Linder-Aronson S, Lundstrom A, McWilliam J. Mandibular and Neck Surg. 1985;93:240-244. maxillary growth after change mode of breathing. Am J Orthod Dentofacial Or- 19. Kuna S, Remmers JE. Neural and anatomic factors related to upper airway oc- thop. 1991;100:1-18. clusion during sleep. Med Clin North Am. 1985;69:1221-1242. 37. Guilleminault C, Stoohs R, Kim Y, Chervin R. Black J, Clerk A. Upper airway sleep- 20. Brown IG, Bradley TD, Phillipson EA, et al. Pharyngeal compliance in snoring disordered breathing in women. Ann Intern Med. 1995;122:493-501. subjects with and without obstructive sleep apnea. Am Rev Respir Dis. 1985; 38. Guilleminault C. In discussion of: Johns FR, Strollo PJ Jr, Buckley M, Con- 132:211-215. stantino J. The influence of craniofacial structure on obstructive sleep apnea in 21. Meurice JC, Marc I, Carrier G, Series F. Effects of mouth opening on upper air- young adults. J Oral Maxillofac Surg. 1998;56:596-603.

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