REVIEW ARTICLE

Relation between maxillofacial form and respiratory

disorders in children

Tomonori IWASAKI and Youichi YAMASAKIDivision of Pediatric Dentistry, Field of Developmental Medicine, Health Research Course, Graduate School ofMedical and Dental Sciences, Kagoshima University, Kagoshima, Japan

Abstract

Obstructive sleep apnea syndrome (OSAS) in children is not rare and the importance of thisobstruction during childhood is increasingly recognized. Children with OSA often have excessivedaytime sleepiness, hyperactivity, attention deficit disorder, poor hearing, physical debilitation, andfailure to thrive. The first choice for treatment of childhood OSAS is adenotonsillectomy; however,OSAS treatment with rapid maxillary expansion (RME) has also been suggested. Therefore, wepresent summaries of the following RME studies about the relation between maxillofacial form andrespiratory disorders in children that showed the following: (i) RME improves nasal airway ventila-tion, suggesting that RME could contribute to treatment and prevention in children where OSAS iscaused by nasal obstruction; (ii) Children with nasal airway obstruction have low tongue posture,and tongue posture improves when nasal airway obstruction is improved by RME; (iii) RME enlargesthe pharyngeal airway. These effects of RME may contribute to treatment and prevention ofchildhood OSAS.

Key words: children, obstructive sleep apnea syndrome, rapid maxillary expansion, tongueposture.

INTRODUCTION

Respiratory disorders during growth can affect maxil-lofacial form,1–3 and abnormal maxillofacial form,in turn, can affect respiration.4,5 In addition, upperairway narrowing is implicated in the development ofobstructive sleep apnea (OSA).6 The importance of this

airway obstruction during childhood is increasinglyrecognized.6–8 Children with OSA often have excessivedaytime sleepiness, hyperactivity, attention deficit dis-order, poor hearing, physical debilitation, and failure tothrive.8 Accordingly, much attention has been paid tothe influence of maxillofacial form on respiratory func-tion during growth.9

We introduce studies on the: (i) the relation betweensleep disordered breathing (SDB) children and dentalarch morphology;10–12 (ii) the cephalometric evaluationof SDB children;13–17 (iii) the relation between maxillo-facial form and pharyngeal airway form;18 (iv) therelation between upper airway ventilation conditionand maxillofacial form;19 (v) the treatment of OSA chil-dren by rapid maxillary expansion (RME);20,21 and (vi)the influence of RME on the nasal airway ventilationcondition, tongue posture, and pharyngeal airwayform.22,23

Correspondence: Dr Tomonori Iwasaki, Field ofDevelopmental Medicine, Health Research Course,Graduate School of Medical and Dental Sciences,Kagoshima University, 8-35-1, SakuragaokaKagoshima-City, Kagoshima 890-8544, Japan. Email:yamame@dent.kagoshima-u.ac.jp

Disclosure: The authors report no commercial, proprietary,or financial interest in the products or companies describedin this article.

Accepted 12 November 2013.

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Sleep and Biological Rhythms 2014; 12: 2–11 doi:10.1111/sbr.12041

2 © 2013 The AuthorsSleep and Biological Rhythms © 2013 Japanese Society of Sleep Research

The relation between sleep disorderedbreathing children and dentalarch morphology

Dental arch morphology have been studied in connec-tion to different aspects of obstruction such as the influ-ence of habitual snoring and OSA.10,11

Lofstrand-Tidestrom et al.11 Showed several differ-ences between obstructed and non-symptomic children:the maxillary width was smaller when measured at theprimary canines, and at the first and second primarymolars, and lateral cross-bite that mandibular molaroccluded in the buccal side of the maxillary molar wasmore frequent among the obstructed children.

Hultcrantz et al.12 studied dental arch morphologywith sleep disordered breathing (SDB) from 4- to12-year-old children. The results showed that the dentalarch was narrower in the children snoring regularly at 4,6 and 12 years compared to not snoring children. Andcross-bites were more common among snoring childrenthan among non-snoring children, at 4 and 6, as well asat 12.

Cephalometric evaluation ofSDB children

Pharyngeal airway morphologies of SDB and OSA chil-dren have been studied by cephalometrically.13–15

Pirila-Parkkinen et al.15 reported that obstructivesleep apnea was associated with decreased pharyngealdiameters at the levels of the adenoids and tip of theuvula, an increased diameter at the level of the base ofthe tongue, a thicker soft palate, and anteriorly posi-tioned maxilla in relation to the cranial base.

Previous studies16,17,24 reported that children withsleep-disordered breathing have increased lower ante-rior face height, increased mandibular plane angle,retropositioned mandible, narrow maxilla, and smallerairway space.

Pirila-Parkkinen et al.15 showed the children withSDB were characterized by a longer (P = 0.018) andthicker (P = 0.002) soft palate, smaller airway diametersat multiple levels of the nasopharynx and oropharynx,larger oropharyngeal airway diameter at the level of thebase of the tongue (P = 0.011), and lower hyoid boneposition (P = 0.000) when compared with the non-obstructed controls. Therefore, OSA children deviatedsignificantly from the control children especially in theoropharyngeal variables.

Evaluation of pharyngeal airway form:Limitations of evaluation fromlateral cephalograms

Several articles have analyzed the morphology of theupper airway from lateral cephalograms.9,25 Neverthe-less, because the left-right length (width) of the upperairway is not visible, its volume and width cannot beestimated from lateral cephalograms alone. Accordingly,a systematic evaluation of the oropharyngeal airway inchildren with a Class III malocclusion (mandibular pro-trusion) was carried out using cone-beam computedtomography (CBCT) and 3-dimensional (3-D) imagereconstruction software.18 Volume, cross-sectional area,length, and width of the oropharyngeal airway in chil-dren with Class III malocclusion were measured andcompared to those of children with Class I malocclusion(normal maxillofacial form) (Fig. 1).

Figure 1 Measurements of the oropharyngeal airway.18 The width of oropharyngeal airway was measured at the narrowest partof the entire depth. Cross-sectional area (S), depth (D) and width (W).

Maxillofacial form and respiration

3© 2013 The AuthorsSleep and Biological Rhythms © 2013 Japanese Society of Sleep Research

The sample comprised 45 children (average age,8.6 ± 1.0 years) divided into two groups: 25 with ClassI and 20 with Class III malocclusions. The Class IIIgroup showed statistically larger oropharyngeal airwayarea and width compared with the Class I group(Table 1). Oropharyngeal airway depth was significantlycorrelated with only cross-sectional area in the Class Igroup. But depth was not significantly correlated withcross-sectional area or width in the Class III group(Table 2). These results show that the oropharyngealairway forms were different if maxillofacial forms weredifferent.

Evaluation of the upper airwayventilation condition: Limitationsof evaluation of from 3-D airwaymorphology alone

Morphometry (volume, cross-sectional area, depth,width) of a complex shape, such as the pharyngealairway, and evaluation of the ventilation condition of thewhole upper airway, including the nasal cavity, are both

difficult. Therefore, a 3-D model of the upper airway,including the nasal cavity was constructed, and fluid-mechanical simulation to evaluate the ventilation con-dition was used. This approach allowed us to investigatethe relation between maxillofacial form and the upperairway ventilation condition (Fig. 2).19

Forty subjects (7 to 11 years of age) with Class IImalocclusion (mandibular retrusion) participated andwere divided into two groups, dolichofacial andbrachyfacial, based on their mandibular plane anglesrelative to Frankfort horizontal (Fig. 3). CBCT imagessupplied the shape of the entire airway. Two measures ofrespiratory function, air velocity and pressure, weresimulated by using 3-dimensional images of the airway(Fig. 2). Pharyngeal airway size (Fig. 4) and fluid-mechanical simulation simulations were comparedbetween the two facial types.

The pressure of the dolichofacial type (147.70 Pa)was significantly higher than that of the brachyfacialtype (80.55 Pa), and the velocity the dolichofacial type(13.46 m/s) was higher than that of the brachyfacialtype (9.63 m/s), However, evaluation of the airway formdetected a significant difference only in the cross-sectional area of the nasopharyngeal airway. In otherwords, the fluid-mechanical simulation system devel-oped in this study could identify functional sites ofupper airway obstruction that were not apparent frommorphologic studies (Figs 5,6). This suggests that thissystem might be helpful in the identification of airwayobstruction sites in OSAS treatment.

Rapid maxillary expansion in childrenwith OSAS

Pirelli20 showed positive effects of RME in 31 children.The mean age was 8.7 with a mean pre-treatment AHIof 12.2. Immediately following expansion (meanexpansion was 4.2 mm) 29 of the 31 patients had anAHI <5. At follow-up (6–12 months post-expansion),all patients were brought into the normal range (AHI<1). 29 of the 31 patients had an AHI <RME removalfollowing expansion allowing the tongue greaterroom.

Villa et al.21 reported on RME in children with OSASby evaluating objective subject data over a 36-monthfollow-up period. The AHI decreased and the clinicalsymptoms had resolved by the end of the treatment.Twenty-four months after the end of the treatment, nosignificant changes in the AHI and other variables wereobserved.

Table 1 Mean measurements of the upper airway18

Class I group Class III group

P

(n = 25) (n = 20)

Mean SD Mean SD

Oropharyngeal airwayCSA (mm2) 119.18 48.09 168.56 54.40 0.002**Depth (mm) 10.68 2.52 13.58 3.16 0.001**Width (mm) 14.97 3.98 18.40 4.47 0.021*

*Statistically significant at P < 0.05; **statistically significant at P <0.01. CSA, cross-sectional area.

Table 2 Correlations among the oropharyngeal airwaymeasurements of Class I and Class III groups. Probabilities inparenthesis18

Depth Width

Class I group CSA 0.471 (0.018)* 0.570 (0.003)**(n = 25) Depth – –0.234 (0.261)Class III group CSA 0.219 (0.355) 0.536 (0.015)*(n = 20) Depth – –0.406 (0.076)

*Statistically significant at P < 0.05; **statistically significant at P <0.01. CSA, cross-sectional area.

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4 © 2013 The AuthorsSleep and Biological Rhythms © 2013 Japanese Society of Sleep Research

100.050.00.0

Pressure (Pa)

a dcbFigure 2 Fluid-mechanical simulation analysis of the upper airway.19 (a) Cone-beam computed tomography (CBCT) used inthis study; (b) extracted upper airway image; (c) fluid-mechanical simulation; (d) evaluation of upper airway ventilation.

FMA > 35° FMA < 25°

Figure 3 Lateral cephalogram imagesreconstructed from cone-beam com-puted tomography (CBCT) data ofa dolichofacial child (left) and abrachyfacial child (right).19 FMA isthe Frankfort mandibular plane angle.

CSA

a

D

b

CSA

D FH plane

A B

Figure 4 Measurement of cross-sections in the nasopharyngeal airway and the oropharyngeal airway.19 (a) nasopharyngealairway cross-section is defined as a horizontal plane at the airway’s narrowest part in the reconstructed lateral cephalometricimage; (b) oropharyngeal airway cross-section is defined as the horizontal plane through the mid-point of bilateral gonion. CSAis cross-sectional area; D is depth.

Maxillofacial form and respiration

5© 2013 The AuthorsSleep and Biological Rhythms © 2013 Japanese Society of Sleep Research

The influence of rapid maxillaryexpansion on the upper airwayventilation condition, tongue posture,and pharyngeal airway form -possiblecontribution to OSAS treatmentand prevention

Nasal airway ventilation condition

Rapid maxillary expansion (RME) expands the maxillarybone about 5–8 mm laterally. It has been suggested thatthis expansion improves nasal airway ventilation.However, evaluation of the ventilation condition of the

nasal airway by conventional rhinomanometry is diffi-cult because the condition of the adenoids, palatinetonsil, and soft palate all affect the results. However, thefluid-mechanical simulation technique can evaluate pre-cisely how RME changes the nasal airway ventilationcondition by extracting and evaluating the nasal cavityalone (Fig. 7).

Rapid maxillary expansion evaluated changes of thenasal airway ventilation condition.22 Twenty-three sub-jects (nine boys, 14 girls; mean ages, 9.74 ± 1.29 yearsbefore RME and 10.87 ± 1.18 years after RME) whorequired RME as part of their orthodontic treatment hadCBCT images taken before and after RME. The data were

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b Figure 5 Airway images of a brachyfacial child, representing a normal ventilation condition.19 (a) Morphological airwayimages (right lateral, front, and superior views) extracted from a cone-beam computed tomography (CBCT) image; (b)Fluid-mechanical simulation analysis of the same airway in the sagittal plane (left: is the pressure analysis, right is the velocityanalysis). In (a), no stenosis was found in either the pharynx or bilateral nasal cavity. In (b), both the maximal pressure andvelocity were relatively low, and no abrupt change of pressure or velocity was detected.

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Figure 6 Airway images of a dolichofacial child, representing obstruction at both the nasopharynx and nasal cavity.19 (a)Morphological airway images (right lateral, front, and superior views) extracted from a cone-beam computed tomography(CBCT) image; (b) Fluid-mechanical simulation analysis of the same airway in the sagittal plane (left: is the pressure analysis,right is the velocity analysis). In (a) stenosis by the hypertrophied adenoid and complete perforation of the right nasal cavitywere found (yellow arrow). In (b), because the pressure decreases abruptly around the adenoids, and the velocity was so high,the existence of an obstruction can be diagnosed (yellow arrow). Similar findings are present at the left nasal cavity. This couldnot be determined from the morphology alone (red arrow).

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6 © 2013 The AuthorsSleep and Biological Rhythms © 2013 Japanese Society of Sleep Research

used to reconstruct the 3-dimensional shape of the nasalcavity. Two measures of nasal airflow function (pressureand velocity) were simulated using fluid-mechanicalsimulation.

The pressure after RME (80.55 Pa) was significantlylower than before RME (147.70 Pa), and the velocityafter RME (9.63 m/s) was slower than before RME(13.46 m/s) (Fig. 8). RME was shown to improve thenasal airway ventilation condition. These results suggest

the possibility that, in children in whom OSAS is causedby nasal obstruction, RME could contribute to its treat-ment and prevention.

Tongue posture

The mechanism is uncertain, but low tongue posture isoften detected in OSAS. Therefore, we evaluated therelation between the nasal airway ventilation condition

adenoid

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a b c dsoft palate

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Figure 7 Steps in the evaluation of nasal cavity ventilation by fluid-mechanical simulation:22 (a) The cone-beam computedtomography (CBCT) instrument; (b) Extraction of the nasal cavity data; (c) Volume rendering and numerical simulation; (d)Evaluation of the nasal cavity ventilation condition.

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Figure 8 Example of change in the ventilation condition after rapid maxillary expansion (RME) in a selected patient (a: beforeRME, b: after RME):22 (a) Stenosis of the nasal cavity can be seen but the presence of an obstruction cannot be determined fromthe 3D form (yellow arrow). Nevertheless, fluid-mechanical simulation shows that the maximal pressure and maximumvelocity were both high (red arrow), indicating an obstruction. (b) The 3D form indicates improvement of the stenosis, but itcannot determine whether the obstruction was reduced (yellow arrow). On the other hand, fluid-mechanical simulation showsthat both pressure and velocity decreased (blue arrow), and the obstruction was reduced.

Maxillofacial form and respiration

7© 2013 The AuthorsSleep and Biological Rhythms © 2013 Japanese Society of Sleep Research

and tongue posture.23 In addition, we concurrentlyevaluated the influence of RME on tongue posture.

Twenty-eight treatment subjects (mean age 9.96 ± 1.21years) who required RME treatment had CBCT imagestaken before and after RME. Twenty control subjects (meanage 9.68 ± 1.02 years) received orthodontic treatmentwithout RME. Nasal airway ventilation was analyzed byfluid-mechanical simulation, and the size of the intraoralairway (the space between the tongue and palate) wasmeasured as an indicator of low tongue position (Fig. 9).

Intraoral airway volume decreased significantly in theRME group from 1212.9 ± 1370.9 mm3 before RME to

279.7 ± 472.0 mm3 after RME (Table 3). Nasal airwayventilation was significantly correlated with intraoralairway volume (Figs 10,11).

In children with nasal obstruction, RME not onlyreduces nasal obstruction but also raises tongue posture(Table 4). This study showed that children with nasalairway obstruction had a lower tongue posture, and thetongue had a higher position when nasal airwayobstruction was improved by RME. These resultssuggest both the mechanism for OSAS in children withlow tongue posture as well as the possibility of usingRME for effective treatment.

Table 3 Statistical comparison of effect of rapid maxillary expansion (RME) on intraoral airway volume23

RME (n = 28) Control (n = 20) Group differences

Mean SD Mean SD P

Before RME (mm3) 1212.9 1370.9 415.1 803.1 0.024After RME (mm3) 279.7 472 570.2 1031.4 0.251Treatment change (mm3) –933.3 1308.8* 155.1 1096.7 0.004

*Significant changes between before and after RME (P < 0.05).

Figure 9 Estimate of low tongue posture in a selected patient.23 (a) Cephalometric image (left, lateral view; right, posterior-anterior view); (b) 3D views of the intraoral airway (right lateral, superior, and front views).

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8 © 2013 The AuthorsSleep and Biological Rhythms © 2013 Japanese Society of Sleep Research

Pharyngeal airway

Because obstruction can occur in the pharyngeal airway,OSAS can also occur. Procedures that enlarge the phar-yngeal airway may effectively treat OSAS. Therefore the

effect of RME on pharyneal airway enlargement wasexamined.23

Pharyngeal airway volumes were measured in 28treatment subjects (mean age 9.96 ± 1.21 years) whorequired RME treatment. CBCT images were taken

b a

Figure 10 Improvement of lowtongue posture after rapid maxillaryexpansion (RME) (frontal view) in aselected patient:23 (a) before RMEtongue posture is low (red arrow); (b)after RME tongue posture hasimproved (blue arrow).

a b

Figure 11 Enlargement of the phar-yngeal airway after rapid maxillaryexpansion (RME) in a selectedpatient.23 (a) Before RME, tongueposture is low (white arrow) and thepharyngeal airway is narrow; (b) AfterRME, tongue posture has improved(white arrow) and the pharyngealairway has enlarged (black arrow).

Table 4 Comparisons of rapid maxillary expansion (RME) treatment changes among three groups (Ventilation group,Improvement group, and Non-improvement group)23

Ventilation Improvement Non-improvementGroup differences(n = 8) (n = 13) (n = 7)

Mean SD Mean SD Mean SD P Post hoc†

Maximum Pressure (Pa)Before RME‡ 46.27 26.51 140.97 71.43 220.05 57.92 <0.001 1,2After RME§ 36.98 24.39 68.49 18.56 203.15 66.63 <0.001 2,3Treatment change¶ –9.29 30.81 –76.50 73.14 –50.03 47.53 0.025

Maximum velocity (m/s)Before RME‡ 7.39 3.87 13.38 2.72 19.25 7.84 0.005 1,2After RME§ 6.18 3.36 9.53 4.16 19.36 5.32 0.001 2,3Treatment change¶ –1.21 5.36 –4.08 5.03 –2.11 5.72 0.461

Intraoral airway (mm3)Before RME 114.8 212.5 1638.8 1507.9 1677.0 1266.6 0.021 1After RME 0.0 0.0 123.1 197.0 890.1 576.9 <0.001 2,3Treatment change –114.8 212.5 –1515.8 1481.2* –786.9 1270.4 0.049 1

*Significant change between before and after RME (P < 0.05). †Significant group differences based on Bonferroni test P < 0.05: 1, ventilationvs. improvement; 2, ventilation vs. non-improvement; 3, improvement vs. non-improvement. ‡ventilation (n = 8), improvement (n = 10),non-improvement (n = 4). §ventilation (n = 8), improvement (n = 13), non-improvement (n = 6). ¶ventilation (n = 8), improvement (n = 10),non-improvement (n = 4).

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9© 2013 The AuthorsSleep and Biological Rhythms © 2013 Japanese Society of Sleep Research

before and after RME and also in 20 control subjects(mean age 9.68 ± 1.02 years) who received orthodontictreatment without RME (Fig. 12).

The change in pharyngeal airway volume in the RMEtreatment group (3015.4 mm3) was significantly greaterthan that of the control group (1226.3 mm3) (Table 5)(Fig. 11). These results indicate that pharyngeal airwayenlargement occurs with RME, a clinical result thatmight contribute to improvement of OSAS symptoms.

The ventilation condition of the upper airway wasevaluated using fluid-mechanical simulation andobtained the following results.

There is a relation between the ventilation conditionof the upper airway and maxillofacial form duringgrowth. Fluid-mechanical simulation can identify pos-sible airway obstruction sites that are not detectable bymorphological studies. RME leads to an improvement ofthe nasal airway ventilation condition, improvement oftongue posture, and pharyngeal airway enlargement.

The identification of the airway obstruction site maybe enhanced by using fluid-mechanical simulation inchildren with OSAS. We also believe that nasal cavityventilation improvement, tongue posture improvement,and pharyngeal airway enlargement by RME will help

improve symptoms of childhood OSAS. RME mayalso reduce the future OSAS risk during growth in chil-dren without apparent OSAS symptoms. Upper airwayobstruction is associated with development of a longface,which we consider to increase the risk of future OSAS.However, in cases where the maxilla is wide enough thatmaxillary expansion is not needed, RME is not indicatedand should not be used to treat OSAS.

One limitation of our studies was that the studysamples consisted of orthodontic cases rather thanOSAS cases. A study using OSAS cases will be requiredto confirm our conclusions. Furthermore, fluid-mechanical simulation produces estimates of airflowvelocities and pressures, not real physiological data.Studies are needed to confirm how well estimates fromfluid-mechanical simulation correspond to actualphysiological measurements.

ACKNOWLEDGMENTS

This work was supported by KAKENHI from JapanSociety for the Promotion of Science (No. 18791563,19390532, 19592357, 19592360, 22390392,22592292, 22792061) and Comprehensive promotion

Palate

a

1

2

Tongue

b

Nasal airway

IAv PAv

Figure 12 Measurement of airwayvolumes.23 (a) Planes for the axialsection of the airway: 1. Palatal plane(PL plane); 2. EB plane (plane parallelto PL plane passing through base ofepiglottis). (b) Each part of airway:PAv. Pharyngeal airway volume,between PL plane and EB plane; IAv.intraoral airway volume, betweenpalate and tongue.

Table 5 Statistical comparison of effect of rapid maxillary expansion (RME) on pharyngeal airway volume23

RME (n = 28) Control (n = 20) Group differences

Mean SD Mean SD P

Before RME (mm3) 6370.7 2291.7 6489.3 1946.2 0.851After RME (mm3) 9386.1 2440.6 7715.6 2151.1 0.018Treatment change (mm3) 3015.4 1297.6* 1226.3 1782.5* <0.001

*Significant changes between T1 and T2 (P < 0.05).

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10 © 2013 The AuthorsSleep and Biological Rhythms © 2013 Japanese Society of Sleep Research

study from the Japanese Association for Dental Science(fiscal year 2012). We thank Professor GaylordThrockmorton, PhD for reviewing this paper for Englishusage.

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