the influence of snoring mouth bmj open 2015 al ali

7232019 The Influence of Snoring Mouth BMJ Open 2015 Al Ali

httpslidepdfcomreaderfullthe-influence-of-snoring-mouth-bmj-open-2015-al-ali 110

The in 1047298 uence of snoring mouthbreathing and apnoea on facialmorphology in late childhood

a three-dimensional studyAla Al Ali1 Stephen Richmond1 Hashmat Popat1 Rebecca Playle1

Timothy Pickles1 Alexei I Zhurov1 David Marshall2 Paul L Rosin2

John Henderson3 Karen Bonuck4

To cite Al Ali A

Richmond S Popat H et al

The influence of snoring

mouth breathing and apnoea

on facial morphology in latechildhood

a three-dimensional study

BMJ Open 20155e009027

doi101136bmjopen-2015-

009027

Prepublication history for

this paper is available online

To view these files please

visit the journal online

(httpdxdoiorg101136

bmjopen-2015-009027 )

Received 10 June 2015Accepted 17 June 2015

1Applied Clinical Research amp

Public Health Dental School

Wales UK2School of Computer Science

amp Informatics CardiffUniversity Wales UK3Avon Longitudinal Study of

Parents and Children

University of Bristol Bristol

UK4Department of Family and

Social Medicine Albert

Einstein College of Medicine

Bronx New York USA

Correspondence to

Dr Ala Al Ali

alaaalalimohgovae

dralaa97hotmailcom

ABSTRACTObjective To explore the relationship between theprevalence of sleep disordered breathing (SDB) and

face shape morphology in a large cohort of 15-year-oldchildren

Design Observational longitudinal cohort study

Setting Avon Longitudinal Study of Parents andChildren (ALSPAC) South West of England

Participants Three-dimensional surface laser scanswere taken for 4784 white British children from the

ALSPAC during a follow-up clinic A total of 1724children with sleep disordered breathing (SDB) and1862 healthy children were identified via parentsrsquo

report of sleep disordered symptoms for their childrenWe excluded from the original cohort all childrenidentified as having congenital abnormalities

diagnoses associated with poor growth and children

with adenoidectomy andor tonsillectomy

Main outcome measures Parents in the ALSPACreported sleep disordered symptoms (snoring mouth

breathing and apnoea) for their children at 6 18 3042 57 69 and 81 months Average facial shells werecreated for children with and without SDB in order to

explore surface differences

Results Differences in facial measurements werefound between the children with and without SDBthroughout early childhood The mean differences

included an increase in face height in SDB children of03 mm (95 CI minus052 to minus005) a decrease inmandibular prominence of 09deg (95 CI minus130 to

minus042) in SDB children and a decrease in noseprominence and width of 012 mm (95 CI 000 to024) and 072 mm (95 CI minus010 to minus025)

respectively in SDB children The odds of childrenexhibiting symptoms of SDB increased significantlywith respect to increased face height and mandible

angle but reduced with increased nose width andprominence

Conclusions The combination of a long facereduced nose prominence and width and a

retrognathic mandible may be diagnostic facial featuresof SBD that may warrant a referral to specialists for theevaluation of other clinical symptoms of SDB

INTRODUCTION

Sleep-disordered breathing (SDB) including obstructive sleep apnoea (OSA) is highly prevalent in the general population Themost common symptoms are primary snoring mouth breathing and repetitiveperiods of cessation in breathing during sleep termed apnoeas or reductions in theamplitude of a breath known as hypopneas1

American Academy of Otolaryngology-Headand Neck Surgery (AAO-HNS) de1047297nes SDBas ldquoan abnormal respiratory pattern during sleep and includes snoring mouth breath-ing and pauses in breathing rdquo2

Strengths and limitations of this study

The strengths of this study are its large sample

size based on a population cohort of UK childrenthat is broadly representative of the general

population In addition the children were of thesame age (15 years) making comparisons stron-ger Furthermore the possible confounding

effect of obesity was ascertained Finally theimaging method used in the study is valid and

therefore the methods are transferrable to otherpopulation groups

A limitation of this study is that sleep disordered

breathing (SDB) data are based on parent-reportof SDB symptoms rather than a polysomnogram(PSG) which is considered the lsquogold standardrsquofor assessing SDB However the time expense

possible selection bias of those undergoing PSGand possible methodological changes over time

rendered it unfeasible for epidemiological pur-poses in a large longitudinal cohort studyHowever the five patterns of symptoms of SDB

defined in this study are correlated with the out-comes of polysomnogram examinations andwere found to be reliable

Al Ali A et al BMJ Open 20155e009027 doi101136bmjopen-2015-009027 1

Open Access Research

groupbmjcomon November 23 2015 - Published by httpbmjopenbmjcom Downloaded from



SDB is a subtle disorder of early childhood and may have serious consequences for long-term health espe-cially among children with macroglossia and retro-gnathia3 4 There have been few investigationsconcerning the prevalence of SDB in children Snoring has been reported in 10 of preschool children5ndash7 Theprevalence of parent-reported snoring is estimated to be75 for 2ndash18-year-olds8 while the prevalence of mouth

breathing in young children ranges from 3 to morethan 509ndash11 and the prevalence of OSA is reported torange from 07 to 4 among 2ndash18-year-olds12 13

The prevalence of SDB symptoms is reported by Bonuck et al 14 who conducted the 1047297rst study on thenatural history of snoring mouth breathing and apnoeain a population-based cohort across a key 6-year periodin the development of SDB symptoms The prevalenceof lsquo Alwaysrsquo snoring range=36ndash77 lsquohabitually rsquosnoring range=96ndash-212 the prevalence of apnoea(lsquo Alwaysrsquo) was 1ndash2 and lsquo Alwaysrsquo mouth breathing ranged from 21 to 7614

The current view is that adenotonsillar hypertrophy isthe major cause of SDB in otherwise healthy children15ndash

17

Adenotonsillar hypertrophy is associated with nasalobstruction resulting in breathing problems and leading to disturbed patterns of sleeping eating swallowing andspeaking18 Consequently the primar y therapy for chil-dren with SDB is adenotonsillectomy19

It is possible that obesity is a risk factor of SDBRudnick et al

20 reported that children with SDB whoundergo adenotonsillectomy are more likely to be obesethan children seen in a general paediatric clinic andthat African-American children w ho are obese are morelikely to have SDB Verhulst et al

21 reviewed the literature

on the prevalence anatomical correlates and treatment of SDB in obese children They concluded that obesechildren are at a higher risk of developing SDB andsuggest that in such children adiposity and upper airway factors such as adenotonsillar hypertrophy both moder-ated the severity of SDB In a direct response to thisreview Kohler and van den Heuvel22 argue ldquo We believehowever that the available studies do not support astraightforward association of overweight or obesity withincreased prevalence of SDB Rather the available dataare clearly equivocal mainly due to methodological dif-ferences between the previous studiesrdquo Kohler and van

den Heuvel examined other factors that may moderatethe relationship between overweight or obesity andprevalence of SDB in children particularly ethnicity andage In a more recent casendashcontrolled study Tripuraneniet al

23 conclude that the degree of obesity does not lin-early predict the severity of OSA in children howeverobese children may have worse symptoms of OSA (diag-nosed by polysomnography (PSG)) than normal-weight children

The concept that nasal obstruction and associatedmouth breathing affects craniofacial development andmorphology continues to be controversial24 A numberof craniofacial anomalies including maxillary and

mandibular retrognathia enlarged tongue soft palateadenotonsillar hypertrophy and an inferiorly positionedhyoid bone may be associated with decreased posteriorairway space and restriction of the upper air wa y promot-ing apnoeas and hypopnoeas during sleep25 Cessationof air1047298ow may develop during OSA because of anatomicobstruction of the upper airway related to obesity andexcessive tissue bulk in the pharynx1

Our previous studies on ALSPAC children with breath-ing disorders (atopy allergic rhinitis and asthma) show that the previously mentioned breathing disorders may have in1047298uenced face shape to varying degrees26 27

Atopic and allergic children had an increased total faceheight on an average of 06 mm when compared to con-trols whereas asthmatic children had a shorter mid-faceheight (04 mm) compared to a control group drawnfrom the same population

Linder-Aronson28 evaluated children who hadadenoid hyperplasia and concluded that nasal obstruc-tion may alter facial growth for which the term lsquolong or

adenoidal facersquo

was coined He found that children withlarge adenoids usually have longer and narrow faceslower tongue position anterior open bite narrow upper jaw and steep mandibles with a more backward positionLinder-Aronson et al

29 hypothesised that adenotonsillarhypertrophy in children induces mouth breathing dis-rupting the balance of labial lingual and cheek musclesresulting in facial anomalies Tomer and Harvold30 and Vickers31 suggest that nasal obstruction causes changesin muscular function conditioning dentofacial anomal-ies Children with enlarged tonsils may have a largeranterior total and lower facial height a more retro-gnathic mandible proclined upper incisors retroclined

lower incisors and a large overjet32 Other facial anomal-ies that may potentially be associated with SDB includeincreased anterior face height incompetent lip postureincreased mandibular plane angle and V-shaped maxil-lary arch33 Nasal obstruction associated with mouthbreathing may lead to a downward and backward rota-tion of the mandible associated with increased anteriorface height24 A recent systematic review andmeta-analysis comparing healthy controls versus children with OSA and primary snoring matched for gender34

provides limited statistical support for an associationbetween OSA and cephalometric measurements in chil-

dren aged 0ndash

18 years The meta-analysis used dataextracted from randomised controlled trials casendashcon-trols and cohort studies with relatively small aggregatedsamples The maximum sample sizes were n=87 cases with OSA and n=113 healthy controls Relative to thecontrols children with OSA and primary snoring werefound to exhibit (1) a signi1047297cantly increased mandibu-lar plane angle to the cranial base (ANB angle) and (2)a signi1047297cantly reduced upper airway sagittal width Anincreased ANB angle of less than 2o was howeverregarded as having marginal clinical signi1047297cance Thestudy concludes that ldquolarger well controlled trials arerequired to address the relationship of craniofacial

2 Al Ali A et al BMJ Open 20155e009027 doi101136bmjopen-2015-009027

Open Access




morphology to paediatric sleep-disordered breathing rdquoproviding a direction and rationale for the current study

PURPOSEThe purpose of this study is to determine the extent to which SDB (symptomised by snoring mouth breathing orOSA) is statistically related to face shape measurementsamong children in late childhood (15 years of age) Basedon the literature we hypothesise that the following faceshape measures might be predictors of the incidence andor patterns of severity of SDB (1) increased face height(2) smaller nose prominence (3) smaller mandibularprominence and (4) smaller maxillary prominence

METHODSSubjects and outcomesThe children who participated in this study wereCaucasian representatives of the UK population They were recruited from the Avon Longitudinal Study of

Parents and Children (ALSPAC) which is designed toexplore how the individualrsquos genotype is in1047298uenced by environmental factors impacting on health behaviourand development of children35 The initial ALSPACsample consisted of 14 541 pregnancies with an estimateddate of delivery between April 1991 and December 1992Oof the initial 14 541 pregnancies all but 69 had knownbirth outcome Of these 14 472 pregnancies 195 weretwins 3 were triplets and 1 was a quadruplet pregnancymeaning that there were 14 676 fetuses in the initial ALSPAC sample Of these 14 676 fetuses 14 062 were livebirths and 13 988 were alive at 1 year

SDB was assessed through parental reports of SDBrsquos

hallmark symptoms (snoring apnoea and mouth breath-ing) when each child was 6 18 30 42 57 69 and81 months of age Since objective sleep evaluation andpolysomnography data were not available the assess-ment of the incidence of SDB w as not fully diagnosticBased on Freeman and Bonuck 36 cluster analysis of SDBsymptoms 1047297 ve categories of SDB based on the severity of symptoms reported by the parents over time wereclassi1047297ed as follows Asymptomatic (healthy) Early snoring with peak symptoms at 6 months Early snoring with peak symptoms at 18 months

Late snoring and mouth breathing but remainedasymptomatic until 4 years old and

Severe and sustained symptoms of SDB throughout childhood

During 2006 and 2007 the cohort was re-called whenthe children were 15 years of age We excluded from theoriginal cohort all children identi1047297ed as having (1) con-genital abnormalities (2) diagnoses associated withpoor growth and (3) children with adenoidectomy andor tonsillectomy because we focused on cases of SDB not secondary to congenital or other medical com-plications The total sample size used in this study was3586 (1693 males and 1893 females)

The laser scanning system consisted of two high-resolution cameras (Minolta VIVID 900 OpticalDigitizers) operating as a stereopair The system canacquire 307 200 (640times480) data points as thex-coordinates y-coordinates and z-coordinates of thesurface scanned with an average reported manufactur-ing accuracy of 01 mm (plusmn02 mm)37 A strict protocolfor capturing facial soft tissue morphology was applied

in this study Children sat on an adjustable stool and were asked to look at a Bristol red glass heart hung fromthe ceiling to simulate natural head posture (NHP)NHP was adopted because it has been shown to be clin-ically reproducible38ndash40 Children were also instructed toswallow hard and to keep their jaws relaxed just beforethe scans were taken If a patient moved between scansthe procedure was repeated The scanning took approxi-mately 8 s per child A locally developed algorithmimplemented as a macro in Rapidform software (INUSTechnology Inc Seoul South Korea) was used toprocess register and merge the left and right facial

scans of each individual

41

Prior to merging the scan-ning accuracy was checked At least 90 matching of the overlap area of facial halves with an errorle075 mm was deemed to be clinically acceptable Facialimages were normalised to natural head posture withthe origin set at mid-endocanthion point because this isthe most stable point with respect to the growth of theface42 The 21 soft tissue landmarks shown in 1047297gure 1 were manually ident i1047297ed on each facial shell using theRapidform software43 The precision of measuring thelandmarks was lt10 mm for both intraexaminer andinterexaminer assessments The 17 face shape variablescalculated from the landmarks are listed in table 1

Surface-based average faces were constructed separ-ately for those with SDB (1724) and healthy children(1862) In this study facial averaging was implementedusing a template face (randomly chosen from thesample) and by calculating point-wise mean coordinatesin the direction nearly perpendicular to all faces41 Theresulting average face was then used as a new templateand the averaging was repeated Three iterations wereperformed in order to get average faces with good accur-acy for children with SDB and healthy children41

The average face of children with SDB was compared with the average face of healthy children by superimpos-

ing them on the mid-endocanthion point using a best-1047297t registration41 44 Within each of the average faces thereis a variability in the anteroposterior vertical and trans- verse dimensions For this reason positive and negativechanges are produced between the different study groups Colour maps were used to illustrate this with atolerance level of 01 mm to highlight signi1047297cant topo-graphical facial differences

Statistical analysisThe statistical analysis was conducted using IBM SPSS V20 The steps undertaken were a χ

2 test was used toexamine the association of SDB status with gender


Open Access




Second an independent sample t test was used tocompare body mass index (BMI) in SDB status and ana-lysis of variance (ANOVA) was then used for SDBgroups Third factor analysis was used to reduce the 17facial angles and measurements into a smaller numberof facial dimensions Logistic regression was then usedto examine the relationship between the facial dimen-

sions and SDB status Finally SDB groups were plottedin box plots and tested for signi1047297cance using one way ANOVA

RESULTSDemographic summaryThe total sample consisted of 3586 children at age 15 of whom 528 were female The demographic summariesof the 1724 children with SDB symptoms and 1862asymptomatic children are summarised in table 2 The1047297 ve levels of SDB severity ranging from asymptomatic to

the persistent group were represented by 528 15699 162 and 53 of the total sample respectively

SDB was not signi1047297cantly associated with gender(χ2 p=0282) The proportion of boys and girls with SDB was 49 and 472 respectively BMI was associated withSDB (mean difference (95 CI) in BMI 028 (minus051 tominus006) p=0012) The SDB childrenrsquos BMI (2144) was

Figure 1 Facial soft tissue landmarks

Table 1 Variables operationalised from facial landmarks

(R=Right L=Left)

Variables Landmarks Units

Outer eyes distance exR-exL mm

Inner eyes distance enL-enR mm

Lower face height Is-pg mm

Mandible angle g-men-pg Degrees

Maxilla angle n-sn-pg DegreesMid-face height angle exR-pg-exL Degrees

Mid-face height Is-men mm

Mid-face height sn-men mm

Mid-face height n-sn mm

Nose prominence angle n-prn-sn Degrees

Nose prominence prn-sn mm

Nose width alL-alR mm

Philtrum angle prn-sn-Is Degrees

Total face height pg-n mm

Total face height pg-g mm

Total face height li-men mm

Total face height pg-men mm

Table 2 Demographic summary of the sample

Percentage (n)

or Mean (SD)Gender ( (n) Female) 528 (18933586)

BMI (kgmsup2) 214 (35)

SDB status

Asymptomatic 528 (1862)

Early snoring peak symptoms at

6 months

156 (599)


18 months

99 (354)

Late snoring and mouth breathing 162 (580)

Severe and sustained symptoms of

SDB

53 (191)

BMI body mass index SDB sleep disordered breathing


Open Access




higher than that in healthy children (2115) HoweverBMI did not differ within SDB groups (ANOVA p=0100)

Comparison of face shape dimensionsThe descriptive statistics (means SDs and 95 CI) forthe 17 face shape variables are presented in table 3Signi1047297cant mean differences in facial measurements inthose with SDB were an increased lower face height

(Is-pg) a decrease in nose prominence (prn-sn) adecrease in nose width (alL-alR) and an increase inmandible angle (g-men-pg) indicating a retrognathicmandible in those with SBD

Systematic relationships between lower face heightnose width and mandible angle (meanplusmn95 CI) withrespect to the 1047297 ve levels of SDB severity are illustratedin 1047297gures 2ndash4 Lower face height and mandible angle were consistently higher and nose width was consistently lower for those who experienced severe and sustainedsymptoms of SDB throughout childhood ANOVA resultsfor the lower face height mandible angle and nose

width are p=0006 0000 and 0004 respectively withregard to the 1047297 ve levels of SDB groups

Five dimensions of face shape variablesFactor solutions collectively explaining 79 of the vari-ance with consistently strong factor loadings gt05 wereused to classify the 17 face shape variables into 1047297 vedimensions (D1 to D5 table 4) D1 represented faceheight which explained 326 of the variance D2 repre-sented the distance between the eyes with nose width which explained 129 of the variance D3 representednose prominence with maxilla height (127 of the vari-ance) D4 was the maxilla angle and nose with philtrumangle (112 of the variance) and D5 was the mandibleangle (95 of the variance)

Association of SDB and facial dimensionsSince SDB status was associated with BMI logistic regres-sion was used to examine the relationships between thefacial dimensions and SDB status adjusted for BMI A binary logistic regression model was constructed (theresults are presented in table 5) using the principalcomponent scores for the 1047297 ve dimensions extracted by factor analysis as the predictor variables Four dimen-

sions were signi1047297cantly associated with SDB The odds of the children exhibiting symptoms of SBD increased sig-ni1047297cantly with respect to D5mdashmandible angle (OR 11195 CI 104 to 119) and D1mdashface height (OR 10995 CI 102 to 116) In contrast an increase in D 2mdashdis-tance between the eyes with nose width (OR 090 95CI 084 to 097) and an increase in D3mdashnose promin-ence with mid-face height (OR 093 95 CI 086 to099) was associated with reduced odds of SDB Thedimensions D4mdashmaxilla angle nose with philtrumangle was not signi1047297cantly associated with SDB Anincrease in the BMI was associated with increased odds

of SDB (OR 103 95 CI 101 to 105)

Superimposition of average facesSuperimposed surface-based average faces of SDB andhealthy children are presented in 1047297gure 5 while thecolour maps in 1047297gure 6 show morphological differencesbetween the groups As the 1047297gures illustrate healthy children tended to have slightly bigger noses moreprominent mandibles cheeks and foreheads when com-pared to SDB children

DISCUSSIONPrevious analyses of the variability in facial anomaliesassociated with the development of SDB among children

Table 3 Descriptive statistics for face shapes

Non-SDB SDB

Dimension M SD M SD Δ M CI

1 Total face height (pg-men) 9350 563 9375 556 025 (minus061 to 011)

Total face height (pg-g) 11346 612 11380 610 033 (minus073 to 006)

Total face height (pg-n) 10146 617 10185 622 039 (minus080 to 001)

Lower face height (Is-pg) 3654 352 3683 360 028 (minus052 to minus005)

Total face height (li-men) 7473 469 7497 474 024 (minus055 to 006)

Mid-face height (Is-men) 6169 400 6166 396 003 (minus023 to 029)Mid-face angle (exR-pg-exL) 4967 260 4941 268 026 (minus008 to 043)

2 Outer eyes distance (exR-exL) 8768 391 8733 411 034 (minus008 to 060)

Inner eyes distance (enL-enR) 3431 286 3416 291 014 (minus004 to 033)

Nose width (alL-alR) 3364 270 3350 272 072 (minus010 to minus025)

3 Nose prominence (prn-sn) 1979 187 1966 187 012 (000 to 024)

Mid-face height (n-sn) 5234 382 5234 384 000 (minus024 to 025)

Mid-face height (sn-men) 4830 349 4811 341 018 (minus003 to 041)

4 Maxilla angle (n-sn-pg) 16245 569 16232 563 013 (minus023 to 050)

Philtrum angle (prn-sn-Is) 12712 878 12735 885 022 (minus080 to 035)

Nose angle (n-prn-sn) 10056 457 10088 476 031 (minus062 to minus001)

5 Mandible angle(g-men-pg) 13342 672 13429 660 086 (minus130 to minus042)

SDB sleep disordered breathing


Open Access




(aged 0ndash18 years) provide inconsistent and con1047298icting

results Consequently the concept that nasal obstructionand associated mouth breathing in1047298uence craniofacialdevelopment and morpholog y and are related to SDBin children is controversial24 Misleading conclusionsmay have been drawn in previous studies because thesample sizes were too small providing insuf 1047297cient statis-tical power and the cases with SDB and the asymptom-atic controls were not necessarily equivalent with respect to their demographic and other attributes (eg equalproportions of cases and controls by gender age obesity and clinical history) If the study groups were not demo-graphically equivalent then the differences between the

face shape variables could potentially be confounded by factors other than SDB In accordance with the designof an effective study45 we used a large sample size (1693males and 1893 females) all of whom were the same age(15 years) in order to provide suf 1047297cient statistical power

interpreted effect sizes in addition to p values ensuredthat the SDB and healthy children were demographically equivalent and controlled for confounding variables

Figure 2 Meanplusmn95 CI of lower face height (Is-pg) and 5

levels of sleep disordered breathing severity

Figure 3 Meanplusmn95 CI of nose width (alL-alR) and 5 levels

of sleep disordered breathing severity

Figure 4 Meanplusmn95 CI of mandible angle (g-men-pg) and 5

levels of sleep disordered breathing (SDB) severity In each

figure 1=asymptomatic healthy 2=children with early snoring

peak symptoms at 6 months 3=children with early snoring

peak symptoms at 18 months 4=children with late snoringand mouth breathing but who remained asymptomatic until

4 years 5=children with severe and sustained symptoms of

SDB throughout childhood

Table 4 Face shape dimensions extracted by factor

analysis

Percentage ofvariance explained

Per cent Cumulative

Factor 1 326 326

Total face height (pg-men)

Total face height (pg-g)

Total face height (pg-n)

Lower face height (Is-pg)

Total face height (li-men)

Mid-face height (Is-men)

Mid-face height angle

(exR-pg-exL)

Factor 2 129 456

Outer eyes distance (exR-exL)Inner eyes distance (enL-enR)

Nose width (alL-alR)

Factor3 127 583

Nose prominence (prn-sn)

Mid-face height (n-sn)

Mid-face height (sn-men)

Factor 4 112 695

Maxilla angle (n-sn-pg)

Philtrum angle (prn-sn-Is)

Nose angle (n-prn-sn)

Factor 5 95 79

Mandible angle (g-men-pg)


Open Access




(BMI and gender) Furthermore none of the childrenin this study had their tonsils andor adenoids removed while the possible confounding effect of obesity wasascertained

The possible effects of obesity may be a confounding

factor leading to con1047298icting observations in previousstudies However our 1047297ndings support Verhulst et al 21

who concluded that obese children are at a higher risk of developing SDB

Using factor analysis we established that 17 variablesmeasured by use of a three-dimensional facial scancould be reduced to 1047297 ve dimensions of face shape Weestablished consistent outcomes using binary logisticregression to conclude that among children with SDBrelative to healthy children the mandible was retro-gnathic the face height dimensions were signi1047297cantly higher and the nose prominence and nose width dimen-

sions were consistently lower The mandible among theSDB children was found to be signi1047297cantly less promin-ent and in a posterior position relative to the maxillasupporting previous evidence that the prevalence of ret-rognathic mandible in mouth breathing children ishigher than in nasal breathing children46 Increasedtotal and lower face height has previously been reported

among children with SDB18 47ndash49 Nasal obstruction asso-ciated with mouth breathing is assumed to lead to adownward and backward rotation of the mandible andto an increase in anterior face height24ndash26 29 This is con-sistent with our 1047297ndings that face height measurements were higher in SDB children when compared to healthy asymptomatic children We also found that the noseprominence dimension was lower in children with SDB

relative to asymptomatic children This is consistent withthe 1047297ndings of Zettergren-Wijk et al 48 who reported that the nose was less pronounced in a small sample of chil-dren (10 boys and 7 girls) with OSA when compared with controls It is suggested that nose prominencecould re1047298ect a comparatively short anterior cranial baseIn contrast we found no statistical evidence to deter-mine a signi1047297cant difference between SDB and healthy asymptomatic children with respect to maxillary prog-nathism consistent with the 1047297ndings of Zettergren-Wijk et al 48 Overall correlations between SDB severity andfacial morphology were indicated in t his study which

supports the 1047297

ndings of Wenzel et al

50

who reported amore retrognathic mandible in association with increas-ing severity of breathing disorders

The limitation of this study is that SDB was assessedthrough parental reports of SDBrsquos hallmark symptoms(snoring apnoea and mouth breathing) Although PSGis considered the lsquogold standardrsquo for assessing SDB thetime expense possible selection bias of those undergo-ing PSG and possible methodological changes over timerendered it unfeasible for epidemiological purposes in alarge longitudinal cohort study on the other hand the1047297 ve patterns of symptoms of SDB de1047297ned in this study were assumed to be reliable because the y are correlated

with the outcomes of PSG examination36 51

CONCLUSIONConsistent evidence was provided using binary logisticregression and three-dimensional average face superim-position to con1047297rm the hypothesis that SDB (snoring

Table 5 Binary logistic regression model using five face

shape dimensions

Predictor OR p Value 95 CI

D1 face height 109 0011 102 116

D2 eyes distance with nose

width

090 0005 084 097

D3 nose prominence with

mid-face height

093 0028 086 099

D4 maxilla angle nose with

philtrum angle

105 0162 098 112

D5 mandible angle 111 0001 104 119

BMI 103 0003 101 105

BMI body mass index

Figure 5 Superimposition of

average facial shells of sleep

disordered breathing and healthy

children


Open Access




apnoea and mouth breathing) among a cohort of 15-year-old children was associated with (1) an increasein face height (2) a decrease in nose prominence (3) adecrease in nose width and (4) a retrognathic man-dible There was however no statistical evidence todetermine if the prevalence and severity of SDB wasassociated with an increase or decrease in the angle of the maxilla However evidence was found to indicate anassociation between increased BMI and the prevalence

of SDB symptomsSince SDB has serious consequences for long-term

health and quality of life early diagnosis of SDB is essen-tial Healthcare professionals can play an important rolein the early diagnosis of SDB recognising distinct facialmorphologies of long face reduced nose prominenceand a retrognathic mandible and referring these chil-dren to specialists for further assessment of SDB clinicalsymptoms

Twitter Follow David Marshall at marshalldavid32

Acknowledgements The authors are extremely grateful to all the individuals

who took part in this study the midwives for their help in recruiting them

and the whole ALSPAC team which includes interviewers computer andlaboratory technicians clerical workers research scientists volunteers

managers receptionists and nurses

Contributors AAA SR and HP designed the study in association with JH and

KB The individuals with sleep disorder breathing (SDB) were identified by JH

and SDB trajectories were determined by KB The three-dimensional facial

data was acquired processed and reviewed by AAA AIZ SR and HP with

support from DM and PLR AAA wrote the manuscript and performed the

statistical analyses with RP and TP All the authors contributed to the writing

critical appraisal and revision of the manuscript

Funding This publication is the work of the authors and AAA will serve as

guarantor for the contents of this paper The UK Medical Research Council

the Wellcome Trust (grant ref 092731) and the University of Bristol provided

core support for the Avon Longitudinal Study of Parents and their Children

The collection of the face data was funded by ALSPAC and Cardiff University

AAArsquos 3-year PhD programme was funded by the Ministry of Higher

Education and Scientific Research in the United Arab Emirates (UAE)

Competing interests None declared

Patient consent Obtained

Ethics approval Ethical approval for the study was obtained from the ALSPAC

Law and Ethics Committee and the Local Research Ethics Committee

Provenance and peer review Not commissioned externally peer reviewed

Data sharing statement The ALSPAC policy on data sharing is available on

the website httpwwwbristolacukalspac To discuss access to ALSPAC

data please contact the ALSPAC executive team on alspac-execbristolacuk

No additional data available

Open Access This is an Open Access article distributed in accordance with

the terms of the Creative Commons Attribution (CC BY 40) license which

permits others to distribute remix adapt and build upon this work for

commercial use provided the original work is properly cited See http

creativecommonsorglicensesby40

REFERENCES1 Panossian L Daley J Sleep-disordered breathing Continuum

(Minneap Minn) 20131986ndash1032 Roland PS Rosenfeld RM Brooks LJ et al Clinical practice

guideline polysomnography for sleep-disordered breathing prior totonsillectomy in children Otolaryngol Head Neck Surg 2011145S1ndash15

3 Defabjanis P Impact of nasal airway obstruction on dentofacialdevelopment and sleep disturbances in children preliminary notesJ Clin Pediatr Dent 20032795ndash100

4 Gregg JM Zedalis D Howard CW et al Surgical alternatives for treatment of obstructive sleep apnoea review and case series Ann R Australas Coll Dent Surg 200015181ndash4

5 Ali NJ Pitson DJ Stradling JR Snoring sleep disturbance andbehaviour in 4ndash5year olds Arch Dis Child 199368360ndash6

6 Ali NJ Pitson D Stradling JR Natural history of snoring and relatedbehaviour problems between the ages of 4 and 7years Arch Dis Child 19947174ndash6

7 Teculescu DB Caillier I Perrin P et al Snoring in French preschoolchildren Pediatr Pulmonol 199213239ndash44

8 Lumeng JC Chervin RD Epidemiology of pediatric obstructive sleepapnea Proc Am Thorac Soc 20085242ndash52

Figure 6 Colour maps and histogram plots to assess facial differences between children with and without sleep disordered

breathing (SDB) The pink areas represent no difference in the SDB and non-SDB children (0 mm) The blue areas represent

less prominent chin and nose in SDB children (01ndash

06 mm) while the deeper blue represents greater facial retrusion in the SDBgroups The red areas are those prominent features in the SDB face


Open Access




9 Felcar JM Bueno IR Massan AC et al Prevalence of mouthbreathing in children from an elementary school Cien Saude Colet 201015437ndash44

10 Huang X Wang H Jiang JX et al The epidemiology of sleep andits disorder in Chinese children aged 0ndash5years Biol Rhythm Res 200940399ndash411

11 Abreu RR Rocha RL Lamounier JA et al Prevalence of mouthbreathing among children J Pediatr (Rio J) 200884467ndash70

12 Lofstrand-Tidestrom B Thilander B Ahlqvist-Rastad J et al Breathing obstruction in relation to craniofacial and dental archmorphology in 4-year-old children Eur J Orthod 199921323ndash32

13 Gislason T Benediktsdottir B Snoring apneic episodes and nocturnalhypoxemia among children 6months to 6years old An epidemiologicstudy of lower limit of prevalence Chest 1995107963ndash6

14 Bonuck KA Chervin RD Cole TJ et al Prevalence and persistenceof sleep disordered breathing symptoms in young children a 6-year population-based cohort study Sleep 201134875ndash84

15 Benninger M Walner D Obstructive sleep-disordered breathing inchildren Clin Cornerstone 20079(Suppl 1)S6ndash12

16 Li HY Lee LA Sleep-disordered breathing in children Chang Gung Med J 200932247ndash57

17 Marcus CL Pathophysiology of childhood obstructive sleep apneacurrent concepts Respir Physiol 2000119143ndash54

18 Kawashima S Peltomaki T Sakata H et al Craniofacial morphologyin preschool children with sleep-related breathing disorder andhypertrophy of tonsils Acta Paediatr 20029171ndash7

19 Friedman NR Perkins JN McNair B et al Current practice patternsfor sleep-disordered breathing in children Laryngoscope 20131231055ndash8

20 Rudnick EF Walsh JS Hampton MC et al Prevalence and ethnicityof sleep-disordered breathing and obesity in children Otolaryngol Head Neck Surg 2007137878ndash82

21 Verhulst SL Van Gaal L De Backer W et al The prevalenceanatomical correlates and treatment of sleep-disordered breathing inobese children and adolescents Sleep Med Rev 200812339ndash46

22 Kohler MJ van den Heuvel CJ Is there a clear link betweenoverweightobesity and sleep disordered breathing in childrenSleep Med Rev 200812347ndash61 discussion 63ndash4

23 Tripuraneni M Paruthi S Armbrecht ES et al Obstructive sleepapnea in children Laryngoscope 20131231289ndash93

24 Harari D Redlich M Miri S et al The effect of mouth breathingversus nasal breathing on dentofacial and craniofacial developmentin orthodontic patients Laryngoscope 20101202089ndash93

25 Cakirer B Hans MG Graham G et al The relationship betweencraniofacial morphology and obstructive sleep apnea in whitesand in African-Americans Am J Respir Crit Care Med

2001163947ndash

5026 Al Ali A Richmond S Popat H et al A three-dimensional analysis ofthe effect of atopy on face shape Eur J Orthod 201436506ndash11

27 Al Ali A Richmond S Popat H et al The influence of asthmaon face shape a three-dimensional study Eur J Orthod 201436373ndash80

28 Linder-Aronson S Effects of adenoidectomy on dentition andnasopharynx Am J Orthod 1974651ndash15

29 Linder-Aronson S Woodside DG Hellsing E et al Normalization ofincisor position after adenoidectomy Am J Orthod Dentofacial Orthop 1993103412ndash27

30 Tomer BS Harvold EP Primate experiments on mandibular growthdirection Am J Orthod 198282114ndash19

31 Vickers PD Respiratory obstruction and its role in long facesyndrome Northwest Dent 19987719ndash22

32 Behlfelt K Enlarged tonsils and the effect of tonsillectomyCharacteristics of the dentition and facial skeleton posture of thehead hyoid bone and tongue mode of breathing Swed Dent J Suppl 1990721ndash35

33 Schlenker WL Jennings BD Jeiroudi MT et al The effects ofchronic absence of active nasal respiration on the growth of theskull a pilot study Am J Orthod Dentofacial Orthop 2000117706ndash13

34 Katyal V Pamula Y Martin AJ et al Craniofacial and upper airwaymorphology in pediatric sleep-disordered breathing systematicreview and meta-analysis Am J Orthod Dentofacial Orthop

201314320ndash

30 e335 Golding J Pembrey M Jones R ALSPAC-the Avon LongitudinalStudy of Parents and Children I study methodology Paediatr Perinat Epidemiol 20011574ndash87

36 Freeman K Bonuck K Snoring mouth-breathing and apneatrajectories in a population-based cohort followed from infancy to 81months a cluster analysis Int J Pediatr Otorhinolaryngol 201276122ndash30

37 Kau CH Zhurov A Knox J et al Validation of a portablethree-dimensional laser scanner for field studies European Craniofacial Congress 200341ndash5

38 Solow B Tallgren A Natural head position in standing subjectsActa Odontol Scand 197129591ndash607

39 Chiu CS Clark RK Reproducibility of natural head position J Dent 199119130ndash1

40 Lundstrom A Lundstrom F Lebret LM et al Natural head positionand natural head orientation basic considerations in cephalometricanalysis and research Eur J Orthod 199517111ndash20

41 Kau CH Richmond S Three-dimensional imaging for orthodontics and maxillofacial surgery London Wiley-Blackwellm 2010

42 Toma AM Zhurov A Playle R et al Reproducibility of facial softtissue landmarks on 3D laser-scanned facial images Orthod Craniofac Res 20091233ndash42

43 Toma AM Zhurov AI Playle R et al The assessment of facialvariation in 4747 British school children Eur J Orthod 201234655ndash64

44 Zhurov AI Richmond S Kau CH et al Averaging facial imagesIn Kau CH Richmond S ed Three-dimensional imaging for orthodontics and maxillofacial surgery London Wiley-Blackwell2010126ndash44

45 Machin D Cambell MJ Design of studies for medical research New York John Wiley 2005

46 Lessa FC Enoki C Feres MF et al Breathing mode influence incraniofacial development Braz J Otorhinolaryngol 200571156ndash60

47 Pirila-Parkkinen K Lopponen H Nieminen P et al Cephalometric

evaluation of children with nocturnal sleep-disordered breathingEur J Orthod 201032662ndash7148 Zettergren-Wijk L Forsberg CM Linder-Aronson S Changes in

dentofacial morphology after adeno-tonsillectomy in young childrenwith obstructive sleep apnoeamdasha 5-year follow-up study Eur J Orthod 200628319ndash26

49 Finkelstein Y Wexler D Berger G et al Anatomical basis ofsleep-related breathing abnormalities in children with nasalobstruction Arch Otolaryngol Head Neck Surg 2000126593ndash600

50 Wenzel A Hojensgaard E Henriksen JM Craniofacial morphologyand head posture in children with asthma and perennial rhinitisEur J Orthod 1985783ndash92

51 Chervin RD Weatherly RA Garetz SL et al Pediatric sleepquestionnaire prediction of sleep apnea and outcomesArch Otolaryngol Head Neck Surg 2007133216ndash22


Open Access




childhood a three-dimensional studyand apnoea on facial morphology in lateThe influence of snoring mouth breathing

and Karen BonuckPickles Alexei I Zhurov David Marshall Paul L Rosin John HendersonAla Al Ali Stephen Richmond Hashmat Popat Rebecca Playle Timothy

doi 101136bmjopen-2015-009027

2015 5BMJ Open

httpbmjopenbmjcomcontent59e009027Updated information and services can be found at

These include

References BIBLhttpbmjopenbmjcomcontent59e009027

This article cites 47 articles 12 of which you can access for free at

Open Access

httpcreativecommonsorglicensesby40 use provided the original work is properly cited Seeothers to distribute remix adapt and build upon this work for commercialthe Creative Commons Attribution (CC BY 40) license which permits

This is an Open Access article distributed in accordance with the terms of

serviceEmail alerting

box at the top right corner of the online articleReceive free email alerts when new articles cite this article Sign up in the

CollectionsTopic Articles on similar topics can be found in the following collections

(217)Respiratory medicine (333)Research methods

(71)Radiology and imaging

(347)Paediatrics (27)Dentistry and oral medicine

Notes

httpgroupbmjcomgrouprights-licensingpermissionsTo request permissions go to

httpjournalsbmjcomcgireprintformTo order reprints go to

httpgroupbmjcomsubscribeTo subscribe to BMJ go to




SDB is a subtle disorder of early childhood and may have serious consequences for long-term health espe-cially among children with macroglossia and retro-gnathia3 4 There have been few investigationsconcerning the prevalence of SDB in children Snoring has been reported in 10 of preschool children5ndash7 Theprevalence of parent-reported snoring is estimated to be75 for 2ndash18-year-olds8 while the prevalence of mouth

breathing in young children ranges from 3 to morethan 509ndash11 and the prevalence of OSA is reported torange from 07 to 4 among 2ndash18-year-olds12 13

The prevalence of SDB symptoms is reported by Bonuck et al 14 who conducted the 1047297rst study on thenatural history of snoring mouth breathing and apnoeain a population-based cohort across a key 6-year periodin the development of SDB symptoms The prevalenceof lsquo Alwaysrsquo snoring range=36ndash77 lsquohabitually rsquosnoring range=96ndash-212 the prevalence of apnoea(lsquo Alwaysrsquo) was 1ndash2 and lsquo Alwaysrsquo mouth breathing ranged from 21 to 7614

The current view is that adenotonsillar hypertrophy isthe major cause of SDB in otherwise healthy children15ndash

17

Adenotonsillar hypertrophy is associated with nasalobstruction resulting in breathing problems and leading to disturbed patterns of sleeping eating swallowing andspeaking18 Consequently the primar y therapy for chil-dren with SDB is adenotonsillectomy19

It is possible that obesity is a risk factor of SDBRudnick et al

20 reported that children with SDB whoundergo adenotonsillectomy are more likely to be obesethan children seen in a general paediatric clinic andthat African-American children w ho are obese are morelikely to have SDB Verhulst et al

21 reviewed the literature

on the prevalence anatomical correlates and treatment of SDB in obese children They concluded that obesechildren are at a higher risk of developing SDB andsuggest that in such children adiposity and upper airway factors such as adenotonsillar hypertrophy both moder-ated the severity of SDB In a direct response to thisreview Kohler and van den Heuvel22 argue ldquo We believehowever that the available studies do not support astraightforward association of overweight or obesity withincreased prevalence of SDB Rather the available dataare clearly equivocal mainly due to methodological dif-ferences between the previous studiesrdquo Kohler and van

den Heuvel examined other factors that may moderatethe relationship between overweight or obesity andprevalence of SDB in children particularly ethnicity andage In a more recent casendashcontrolled study Tripuraneniet al

23 conclude that the degree of obesity does not lin-early predict the severity of OSA in children howeverobese children may have worse symptoms of OSA (diag-nosed by polysomnography (PSG)) than normal-weight children

The concept that nasal obstruction and associatedmouth breathing affects craniofacial development andmorphology continues to be controversial24 A numberof craniofacial anomalies including maxillary and

mandibular retrognathia enlarged tongue soft palateadenotonsillar hypertrophy and an inferiorly positionedhyoid bone may be associated with decreased posteriorairway space and restriction of the upper air wa y promot-ing apnoeas and hypopnoeas during sleep25 Cessationof air1047298ow may develop during OSA because of anatomicobstruction of the upper airway related to obesity andexcessive tissue bulk in the pharynx1

Our previous studies on ALSPAC children with breath-ing disorders (atopy allergic rhinitis and asthma) show that the previously mentioned breathing disorders may have in1047298uenced face shape to varying degrees26 27

Atopic and allergic children had an increased total faceheight on an average of 06 mm when compared to con-trols whereas asthmatic children had a shorter mid-faceheight (04 mm) compared to a control group drawnfrom the same population

Linder-Aronson28 evaluated children who hadadenoid hyperplasia and concluded that nasal obstruc-tion may alter facial growth for which the term lsquolong or

adenoidal facersquo

was coined He found that children withlarge adenoids usually have longer and narrow faceslower tongue position anterior open bite narrow upper jaw and steep mandibles with a more backward positionLinder-Aronson et al

29 hypothesised that adenotonsillarhypertrophy in children induces mouth breathing dis-rupting the balance of labial lingual and cheek musclesresulting in facial anomalies Tomer and Harvold30 and Vickers31 suggest that nasal obstruction causes changesin muscular function conditioning dentofacial anomal-ies Children with enlarged tonsils may have a largeranterior total and lower facial height a more retro-gnathic mandible proclined upper incisors retroclined

lower incisors and a large overjet32 Other facial anomal-ies that may potentially be associated with SDB includeincreased anterior face height incompetent lip postureincreased mandibular plane angle and V-shaped maxil-lary arch33 Nasal obstruction associated with mouthbreathing may lead to a downward and backward rota-tion of the mandible associated with increased anteriorface height24 A recent systematic review andmeta-analysis comparing healthy controls versus children with OSA and primary snoring matched for gender34

provides limited statistical support for an associationbetween OSA and cephalometric measurements in chil-

dren aged 0ndash

18 years The meta-analysis used dataextracted from randomised controlled trials casendashcon-trols and cohort studies with relatively small aggregatedsamples The maximum sample sizes were n=87 cases with OSA and n=113 healthy controls Relative to thecontrols children with OSA and primary snoring werefound to exhibit (1) a signi1047297cantly increased mandibu-lar plane angle to the cranial base (ANB angle) and (2)a signi1047297cantly reduced upper airway sagittal width Anincreased ANB angle of less than 2o was howeverregarded as having marginal clinical signi1047297cance Thestudy concludes that ldquolarger well controlled trials arerequired to address the relationship of craniofacial


Open Access
















41








Open Access











(R=Right L=Left)



















Percentage (n)



SDB status



6 months

156 (599)


18 months

99 (354)



SDB

53 (191)



Open Access












of SDB (OR 103 95 CI 101 to 105)




Non-SDB SDB




















Open Access




















analysis


Per cent Cumulative

Factor 1 326 326








(exR-pg-exL)

Factor 2 129 456



Factor3 127 583




Factor 4 112 695




Factor 5 95 79



Open Access














50






shape dimensions


D1 face height 109 0011 102 116


width

090 0005 084 097


mid-face height

093 0028 086 099


philtrum angle

105 0162 098 112


BMI 103 0003 101 105

BMI body mass index




children


Open Access






















































Open Access





















2001163947ndash










201314320ndash




















Open Access






doi 101136bmjopen-2015-009027

2015 5BMJ Open


These include



Open Access









Notes



















41








Open Access











(R=Right L=Left)



















Percentage (n)



SDB status



6 months

156 (599)


18 months

99 (354)



SDB

53 (191)



Open Access












of SDB (OR 103 95 CI 101 to 105)




Non-SDB SDB




















Open Access




















analysis


Per cent Cumulative

Factor 1 326 326








(exR-pg-exL)

Factor 2 129 456



Factor3 127 583




Factor 4 112 695




Factor 5 95 79



Open Access














50






shape dimensions


D1 face height 109 0011 102 116


width

090 0005 084 097


mid-face height

093 0028 086 099


philtrum angle

105 0162 098 112


BMI 103 0003 101 105

BMI body mass index




children


Open Access






















































Open Access





















2001163947ndash










201314320ndash




















Open Access






doi 101136bmjopen-2015-009027

2015 5BMJ Open


These include



Open Access









Notes














(R=Right L=Left)



















Percentage (n)



SDB status



6 months

156 (599)


18 months

99 (354)



SDB

53 (191)



Open Access












of SDB (OR 103 95 CI 101 to 105)




Non-SDB SDB




















Open Access




















analysis


Per cent Cumulative

Factor 1 326 326








(exR-pg-exL)

Factor 2 129 456



Factor3 127 583




Factor 4 112 695




Factor 5 95 79



Open Access














50






shape dimensions


D1 face height 109 0011 102 116


width

090 0005 084 097


mid-face height

093 0028 086 099


philtrum angle

105 0162 098 112


BMI 103 0003 101 105

BMI body mass index




children


Open Access






















































Open Access





















2001163947ndash










201314320ndash




















Open Access






doi 101136bmjopen-2015-009027

2015 5BMJ Open


These include



Open Access









Notes















of SDB (OR 103 95 CI 101 to 105)




Non-SDB SDB




















Open Access




















analysis


Per cent Cumulative

Factor 1 326 326








(exR-pg-exL)

Factor 2 129 456



Factor3 127 583




Factor 4 112 695




Factor 5 95 79



Open Access














50






shape dimensions


D1 face height 109 0011 102 116


width

090 0005 084 097


mid-face height

093 0028 086 099


philtrum angle

105 0162 098 112


BMI 103 0003 101 105

BMI body mass index




children


Open Access






















































Open Access





















2001163947ndash










201314320ndash




















Open Access






doi 101136bmjopen-2015-009027

2015 5BMJ Open


These include



Open Access









Notes























analysis


Per cent Cumulative

Factor 1 326 326








(exR-pg-exL)

Factor 2 129 456



Factor3 127 583




Factor 4 112 695




Factor 5 95 79



Open Access














50






shape dimensions


D1 face height 109 0011 102 116


width

090 0005 084 097


mid-face height

093 0028 086 099


philtrum angle

105 0162 098 112


BMI 103 0003 101 105

BMI body mass index




children


Open Access






















































Open Access





















2001163947ndash










201314320ndash




















Open Access






doi 101136bmjopen-2015-009027

2015 5BMJ Open


These include



Open Access









Notes

















50






shape dimensions


D1 face height 109 0011 102 116


width

090 0005 084 097


mid-face height

093 0028 086 099


philtrum angle

105 0162 098 112


BMI 103 0003 101 105

BMI body mass index




children


Open Access






















































Open Access





















2001163947ndash










201314320ndash




















Open Access






doi 101136bmjopen-2015-009027

2015 5BMJ Open


These include



Open Access









Notes

























































Open Access





















2001163947ndash










201314320ndash




















Open Access






doi 101136bmjopen-2015-009027

2015 5BMJ Open


These include



Open Access









Notes
























2001163947ndash










201314320ndash




















Open Access






doi 101136bmjopen-2015-009027

2015 5BMJ Open


These include



Open Access









Notes









doi 101136bmjopen-2015-009027

2015 5BMJ Open


These include



Open Access









Notes





the influence of snoring mouth bmj open 2015 al ali

Documents