Sleep-related breathing disorders * 6Series editor: PM A Calverley

Obstructive sleep apnoea syndrome in infantsand children: established facts and unsettledissues

C Gaultier

The obstructive sleep apnoea (OSA) syndromewas first identified in infants and children byGuilleminault et al in 1976.' Since then, a

great deal has been learned about infancy andchildhood obstructive apnoea, although severalareas remain largely unexplored. Since the firstdescription of the OSA syndrome during in-fancy and childhood, we have learnt that theclinical symptoms ofan increased upper airwayresistive load during sleep are not always as-

sociated with complete airways obstructionduring sleep.2 Episodes of partial airways ob-struction without obstructive apnoea are fre-quently observed in infants and children,3 so

adult diagnostic criteria for the OSA syndromemay not identify infants and children withsleep-related increases in upper airway resistiveloads.34 As recommended by Carroll andLoughlin,4 we should consider that infancy andchildhood OSA syndrome is not a form of adultOSA but a separate syndrome with specificsymptoms, diagnostic criteria, and therapeuticrequirements.

Laboratory ofPhysiology, HospitalAntoine Beclere,Faculty of MedicineParis XI, 92141Clamart, FranceC Gaultier

PrevalenceWe still know little about the prevalence ofincreased respiratory resistive loads duringsleep in infants and children. Reliable data on

the incidence of the OSA syndrome duringinfancy and childhood are not available. Seriesofpatients withOSA published in the paediatricmedical literature suggest that the peak in-cidence is in the 2-5 year age group. This agegroup may be particularly susceptible to OSAbecause of the prominence of pharyngeallymphoid tissue during these years.5 In chil-dren, in contrast to adults, there is no clearmale predominance of OSA.4The prevalance of snoring in two large popu-

lations of children has been evaluated byquestionnaire.67 Between four and six years ofage the reported prevalence of snoring was

7-10%.7 In one of these studies children aged4-5 years were studied at home by overnightvideo recording and oximetry.7 The prevalenceof sleep and breathing disorders in this agegroup was estimated at 0O7%. Another ques-tionnaire based study in a wider age range (six

months to six years) estimated the prevalenceofOSA at 1 -6-3.4%.8 Large scale, well designedstudies assessing the prevalence of an increasedupper airway resistive load during sleep in in-fants and children are needed. A reasonablepriority would be to develop and validate aquestionnaire, use it in the general populationto detect high risk individuals, and subject theseto polysomnographic recordings.

Clinical symptomsA careful history of sleep-associated symptomsis the first step in detecting a sleep-relatedincrease in upper airway resistive loads in aninfant or child. However, more than a yearoften elapses between the onset of symptomsand diagnosis. This explains why severe com-plications such as cardiorespiratory failure aresometimes the presenting complaint.9

Clinical symptoms in children differ in sev-eral ways from those in adults. Excessivedaytime sleepiness, the typical presentingcomplaint in adults, is not frequent in children.4The two major symptoms are sleep-relatedbreathing difficulties and snoring."910 Parentssometimes report that during sleep their childstops breathing, sweats profusely, is restless,and assumes unusual positions in an attemptto relieve upper airways obstruction. Enuresishas been reported in children with the OSAsyndrome." Mouth breathing during wake-fulness is common when nasal obstruction issevere. Upper respiratory tract infections arefrequently reported in young children.9"0 Theseverity of the symptoms usually increases dur-ing these infections and decreases after re-covery. Behavioural disorders, includinghyperactivity, aggressiveness, and rebellious be-haviour, have been reported.91012 In school agechildren learning problems may occur." How-ever, it should not be concluded that a sleep-related increase in upper airway resistive loadsinvariably causes behavioural abnormalities.Psychological testing before and after treatmentcan be useful for determining the contributionof upper airway problems to behavioural ab-normalities.

Obesity has been reported in a large pro-

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portion of adults with OSA but has been foundin only a few of the patients in paediatricseries.4 The risk ofoccurrence of a sleep-relatedincrease in upper airway resistive loads is notclearly established in obese children. Howeveran abnormally high prevalence of OSA withoutclinical symptoms has been found in overweightinfants."4 In obese children both low and highpercentages of sleep-disordered breathing havebeen reported. 516 Silvestri et all6 recommendedthat obese children with a history of sleep-related breathing difficulties should be referredfor polysomnographic evaluation.

Failure to thrive is a not unusual char-acteristic of infants with OSA.49 Investigationsto look for a sleep-related increase in upperairway resistive loads should be routinely per-formed as part of the evaluation of growthretarded infants and children and adequatetreatment of the upper airways obstructionresults in rapid catch-up growth.9 The mech-anisms of growth retardation are not well un-derstood but may include an increase in themetabolic rate during sleep. In a recent pre-liminary study oxygen consumption duringsleep decreased after treatment in children withOSA.'7 These data suggest that children gainweight after treatment because of a decrease inenergy expenditure and that before treatmentthe increase in the work of breathing duringsleep is responsible for an increase in the con-sumption of oxygen by respiratory muscles,leaving less oxygen available for growth.Alternatively and/or simultaneously, repeatedinterruption of sleep may intefere with the re-lease of growth hormone. One study showednormalisation of growth hormone releaseafter treatment of upper airways obstruction.'8

Cardiovascular complicationsThe syndrome combining hypoventilation, pul-monary hypertension, cor pulmonale, and pul-monary oedema was described in the middle ofthe 1960s in infants and children with chronicupper airways obstruction.'9 Sofer et al'0 de-scribed the haemodynamics of this syndromein a 22 month old child and suggested that thepulmonary oedema was secondary to both rightand left heart failure. In their patient pulmonaryarterial pressures returned to normal within 48hours ofsurgery. Acute cardiorespiratory failureseems to occur mainly in patients with long-standing neglected clinical symptoms. Upperrespiratory tract infection is usually the trig-gering event. Patients with an unrecognisedsleep-related increase in upper airway resistiveloads are still at risk of acute cardiorespiratoryfailure. Paediatricians should be aware of thispotential complication because it can result insudden death.""

Cardiovascular symptoms are common inadults with the OSA syndrome. It is thereforeof interest to review their frequency in infantsand children without cardiac failure. However,data on this issue are scant. Radiological and/or electrocardiographic evidence of right vent-ricular hypertrophy was reported in 55% of agroup of infants and children with OSA.'93" Incontrast, in a series of 92 children referred for

adenoidectomy and tonsillectomy Wilkinson etal found electrocardiographic evidence of rightventricular hypertrophy in only 3 3% of cases."Thus, available data do not provide an adequatebasis for estimating the prevalence of rightventricular dysfunction in infants and childrenwith complete and/or partial upper airwaysobstruction during sleep. Interestingly, low pre-treatment right ventricular ejection fraction val-ues have been shown to increase significantlyafter tonsillectomy.'4 Recently developed echo-cardiography techniques allow examination ofinterventricular septum behaviour duringsleep-related upper airways obstruction. In one11 year old child Guilleminault et al reporteda leftward shift of the septum, even duringheavy snoring.'5 In a preliminary study theseverity of clinical symptoms and/or poly-somnographic abnormalities was not relatedto the presence of echocardiographic ab-normalities.'6

Systemic hypertension is found in a largepercentage of adult patients with the OSA syn-drome.4 In a series of 50 cases diurnal systemichypertension was found in 10% of patients, allof whom were older than 10 years.'3 Morerecently, no abnormalities in systolic or diastolicarterial pressures were observed in 22 childrenaged 6 (0 4) years.'7 Non-invasive continuousblood pressure measurements were performedin two children whose fingers were big enoughto allow use of a cuff designed for adults andpulsus paradoxus was found in one.'5There are conflicting data with regard to

ECG abnormalities in children with the OSAsyndrome. A study carried out in the early1980s in a group of 50 children with OSAfound sinus arrests lasting from 2-5 to 9 secondsin 52% of cases, second degree atrioventricularblock in 28%, and paradoxical tachycardia in16%.'3 However, a more recent study in 12subjects aged eight months to 14 years withcomplete and/or partial airways obstructionduring sleep failed to find significant changes inheart rate during numerous episodes of severehypoxaemia.'8 No episodes of severe brady-cardia or cardiac arrhythmia were detected.These findings are of clinical relevance sinceambulatory ECG monitoring has been used inadults to screen for sinus brady-tachy-arrhythmia as a marker for OSA.'9 The datasuggest that this method would not detect allchildren with increased upper airway resistiveloads during sleep.

Finally, a recent study ofheart rate variabilityevaluated by power spectral analysis dem-onstrated a predominance of sympathetic ac-tivity throughout the night with surges duringperiods with apnoeas.30 This might indicate anincreased risk of systemic hypertension at anolder age in the event ofpersistent sleep-relatedbreathing disorders.

Methods of diagnosisA standardised questionnaire developed byBrouillette et al" has proved useful for sus-pected OSA in children aged one to 10 years.However, more recently Carroll et al reportedthat primary snoring cannot be differentiated

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from OSAby clinical history alone in children.32In a population of infants with an abnormalobstructive apnoea index Kahn et al foundthat a history of profuse sweating and noisybreathing during sleep in the absence of upperrespiratory infection was useful as an aid to thediagnosis of sleep-related obstructed breathingepisodes in infants.33 Thus, there is no con-sensus on whether or not an age-specific ques-tionnaire is an adequate tool for identifyinginfants and children with increased upper air-way resistive loads during sleep.

Polysomnographic examination remains thegold standard diagnostic investigation. How-ever, a full overnight polysomnographic studyis technically difficult and can be performedonly by trained personnel. Some laboratoriesstudy a daytime nap. One study compared napand overnight polysomnography recordings in40 children aged one month to 16-3 years,two thirds of whom received chloral hydratesedation for the nap polysomnography.34 Theresults showed that nap studies had a sensitivityof 74%, a specificity of 100%, a positive pre-dictive value of 100%, and a negative predictivevalue of 17% for the diagnosis of sleep-dis-ordered breathing. Thus, a negative nap studydoes not rule out the diagnosis and must becompleted by an overnight sleep study. Naturalsleep for a daytime polysomnographic study issometimes difficult to obtain. Sleep deprivationor sedation has been used to induce daytimesleep. However, sleep deprivation has beenshown to increase significantly the number ofobstructive respiratory events in healthy in-fants,35 and sedation by chloral hydrateis sometimes associated with a dramaticworsening of upper airways obstruction.3637Use ofhome monitoring using either a micro-

phone38 or video recording and oximetry3940has been suggested. However, none of thesetechniques has been validated against overnightpolysomnography in a large number of subjectswith different levels of severity of OSA. Morework is needed to verify the reliability of am-bulatory methods of diagnosis of sleep-relatedresistive load increases in infants and children.

Polysomnographic findingsThere are few data on the occurrence of ob-structive apnoea during overnight sleep in nor-mal infants and children. In infants older thansix weeks the index of obstructive apnoea epi-sodes lasting more than three seconds wasfound to be less than 1.4142 No episodes ofobstructive apnoea were detected in children43or in a small group of adolescents." However,in a more recent study of 50 children aged1-18 years there were 0-1 (0 5) (range 0-3.1)obstructive apnoeas lasting less than 10 secondsper hour of total sleep time.45 We clearly needmore normative data to improve our ability tointerpret polysomnographic data in paediatricpatients.

Polysomnographic recordings can be dividedinto two categories - those with and thosewithout obstructive apnoeas. When obstructiveapnoeas are found, their duration and rate ofoccurrence are usually greatest during REM

sleep. Associated with obstructive apnoeas,polygraphic recording shows laboured breath-ing during the ventilatory periods. Wide swingsin oesophageal pressure have been found dur-ing ventilatory periods.4647 Paradoxical inwardrib cage motion during inspiration has beenreported throughoutREM sleep periods in chil-dren and during non-REM sleep.48 Accessoryrespiratory muscles, including abdominalmuscles, are recruited during non-REM sleepwith snoring.49 Compared with non-REMsleep, REM sleep is associated with inhibitionof accessory respiratory muscle activity whichresults in an increase in the diaphragmatic workof breathing.

Guilleminault et al were the first to pointout in 1982 that some children with clinicalsymptoms do not have obstructive apnoeasduring sleep.2 However, these children havesignificantly increased respiratory resistiveloads during sleep and wide swings in oeso-phageal pressure. Their breathing is mostlaboured during REM sleep. Recently, Rosenet al3 documented partial airways obstructionduring sleep in a group of 20 patients agedeight months to 16 years; 80% of their patientshad sustained partial airways obstruction char-acterised by cyclic decreases in Sao2, hyper-carbia, laboured paradoxical respiratory efforts,and snoring. Such episodes of partial air-ways obstruction are described as obstructivehypopnoeas in adult patients.50 However, thereis no consensus among laboratories on thedefinition of obstructive hypopnoea. Studiesare needed to determine the clinical usefulnessof oesophageal pressure measurements duringsleep in symptomatic infants or children withno obstructive apnoeas on polysomnographicrecordings. However, data on the normal rangeof oesophageal pressure swings during sleep inchildren are scant. The lowest negative oeso-phageal pressures have been reported to rangefrom -8 to -20 cm H20 in two groups ofhealthy children aged 2-14 years.247

Early studies in children with the OSA syn-drome found abnormalities in the sleep patternwith a decrease in the duration of slow wavesleep.'3 These findings were not borne out byrecent investigations in which the sleep patternwas normal.5' Differences in the severity andduration of the disease may at least partiallyexplain these discrepancies.

Different categories of arousal have beencharacterised, such as behavioural arousal,EEG arousal, and movement arousal.52 How-ever, several laboratories are still working onthe development of standardised criteria forarousal detection in infants and children. Fewreports have documented the occurrence ofarousal at the end of sleep-related obstructiveevents in infants or children. In a study ofpreterm infants with apnoeas, behaviouralarousal occurred more frequently after ob-structive apnoeas than after central apnoeas,53but no attempt was made to characterise EEGarousal. An important study in infants withincreased upper airway resistive load duringsleep found an abnormal number of EEGarousals compared with age matched controlinfants.54 Interestingly, EEG arousals occurred

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at the nadirs of the oesophageal pressure re-

cording. In a group of prepubertal childrenwith OSA the end of non-REM sleep apnoea

was marked by EEG arousal in 12% of eventsand by movement arousal in the remainingevents.49 During REM sleep only movementarousals occurred.49 Another study reported a

similar low rate of occurrence of EEG arousalin children and adults.55 The fact that EEGand behavioural arousals are uncommon inchildren may be related to the less frequentoccurrence of excessive daytime sleepiness inchildren than in adults.4 However, more ex-

tensive multicentre studies using standardisedcriteria for arousal detection and assessment ofdaytime behavioural disturbances are neededin different age groups of infants and childrenwith increased upper airway resistive loads.

PathophysiologyThe pathophysiology ofincreased upper airwayresistive load in infants and children is not fullyunderstood. Several factors may place infantsand children at risk for developing the OSAsyndrome. The leading cause of sleep-relatedincreases in upper airway resistive load in thepaediatric population is the prominence oflymphoid tissues.9"0 However, the severity ofOSA is not always proportional to the sizeof the tonsils and adenoids.5657 This suggestsinvolvement of other risk factors such as ab-normal ventilatory drive and/or mechanical andanatomical abnormalities of the upper airways.Few studies have evaluated ventilatory drive

in children with OSA. One early study foundthat some children had low hypercapnic ventil-atory responses when awake several years afteradenotonsillectomy.58 However, Marcus et alrecently reported normal hypercapnic ventil-atory responses when awake in children withtonsilloadenoidal hypertrophy.59 The ventil-atory response to chemical stimuli during sleephas not been studied. It can be speculatedthat the sleep-related decrease in ventilatoryresponses to chemical stimuli may differ be-tween healthy children and children withchronic upper airways obstruction. On theother hand, children with OSA appear to havenormal central control of the upper airwaymuscles during sleep. Continuous upper airwaymuscle activity was found during airway ob-struction, and this muscle activity increasedwith the degree of hypercapnia and hyp-oxaemia.60 Furthermore, a decrease in genio-glossus muscle activity at the onset of ob-structive apnoeas has been found in adults6'but not in children.62 In children, obstructiveapnoeas may, rather, be the result of a suddenincrease in upper airways resistance. Fibro-scopic6" and fluoroscopic64 studies in childrenwith enlarged tonsils have shown that in-spiratory movements of the tonsils and pharyn-

geal walls tend to narrow the upper airwaysand occasionally lead to occlusion. A narrow

airway is an additional risk factor. A relationshiphas been reported between the size of the pos-terior airway and the severity of the OSAsyndrome.5765 A recent study evaluated themechanical properties of the pharynx in chil-

dren with OSA.66 Closing pressure is increasedin children with OSA compared with agematched subjects with primary snoring; similarfindings have been reported in adults.67 In-terestingly, closing pressure was lower in chil-dren than in adults with snoring, suggestingdifferences in upper airways collapsibilitybetween children and adults. Further in-vestigations are needed to document changesin the mechnical properties ofthe upper airwaysin healthy children. Currently, data are avail-able only in healthy infants.68 Little attentionhas been paid to the functional and anatomicalconsequences of chronic obstruction on thegrowth of the upper airways. Experiments inrhesus monkeys have demonstrated inter-actions between abnormal nasal breathingand abnormal growth of the mandible startingat birth.69 These environmental factors mayexplain why residual symptoms are sometimesseen after tonsillectomy70 and why symptomscan recur after puberty.7" Finally, a racial pre-disposition for OSA due to hypertrophy ofthe lymphoid tissues has been suggested, sinceyoung black subjects have more lymphoid tis-sue than young white subjects.72Of the craniofacial abnormalities that have

been found to be responsible for sleep-relatedupper airways obstruction, the Pierre Robinsyndrome has been extensively studied.73 Usingflexible fibreoptic endoscopy Sher et al showedthat obstruction of the airways is due not onlyto glossoptosis but also to many other ab-normalities.74 In infants with micrognathia thepharyngeal airway closing pressure during nasalocclusion trials was correlated with genio-glossus muscle activity, suggesting that thismuscle contributes to pharyngeal airway pat-ency in micrognathic infants.75Endoscopic observations in children with the

OSA syndrome due to other craniofacial an-omalies such as Crouzon syndrome, Treacher-Collins syndrome, and other disorders haveshown that the mechanism of airway collapseis variable.76 The midfacial and mandibularhypoplasia and glossoptosis seen in Down'ssyndrome increase the risk of OSA. Un-diagnosed OSA may contribute to the un-explained pulmonary hypertension seen insome of these children.77

Other disorders associated with an increasedrisk of OSA in children include sickle cell an-aemia,78 brainstem disorders such as Arnold-Chiari malformation79 and myelomeningo-cele,7980 achondroplasia,8' neuromuscular dis-orders,82 and Prader Willi syndrome.83 In infantslaryngomalacia can be responsible forsevere OSA.84

Familial factorsA familial basis for the OSA syndrome is sug-gested by reports of families with several affec-ted members.8485 One recent pilot studyshowed an increased frequency of sleep-dis-ordered breathing in relatives of non-obeseadult patients with sleep apnoea/hyponoea syn-drome.86 Preliminary data on the prevalence ofsnoring in the parents of children who snore

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have been reported.87 Ventilatory control dys-function and craniofacial morphology ab-normalities have a familial basis85 and may berisk factors for OSA in adults. Guilleminaultet al reported five families in which severalmembers, covering three generations, had OSAassociated with a small upper airway.88 Thus,there is evidence that familial factors influencethe risk of developing an increase in upperairway resistive loads. Adult physicians andpaediatricians should look for symptoms ofsleep-disordered breathing in the relatives oftheir patients.

OSA and sudden infant death syndrome(SIDS)It is unclear whether the risk factors for SIDSand OSA operate similarly, but there is someevidence that SIDS and OSA aggregate withinthe same families. Guilleminault et al88 observedclinical symptoms ofOSA and abnormal num-bers of obstructive apnoeas among the parentsor grandparents of SIDS or near-miss SIDScases in five families. The risk was apparentlyrelated to the presence of a small posteriorairway, which was found in several family mem-bers including children. Infants with near-missSIDS were followed up and found to developOSA during childhood.8990 These are the firstpatients who have been studied during thedevelopment of OSA. More recently the samegroup found sleep-related increases in upperairways resistance in infants with a family his-tory of SIDS, apparent life-threatening events,and parental sleep-related breathing dis-orders.54 These infants may be at the highestend ofthe spectrum of at risk infants. However,these findings are in agreement with those ofa Belgian case control study that found a sig-nificant increase in the rate of occurrence ofobstructive events in infants who later died ofSIDS compared with control infants.9' In twoongoing studies of the familial aggregation ofOSA, families with both OSA in adults andSIDS ornear-miss SIDS have been identified.85 92All these data suggest that there is a subset offamilies at risk for both disorders. From aclinical point of view, paediatricians and adultphysicians should look for familial histories ofboth disorders and should recommend a carefulinvestigation in at risk infants.

TreatmentThe optimal treatment strategies for paediatricOSA are still the focus of intensive research,taking into account not only obstructiveapnoeas but also sleep-related increases inupper airways resistive load. Treatment shouldbe considered only after objective testing todetermine the severity of the syndrome andafter otorhinolaryngological and maxillofacialstudies. The pretreatment examination shouldinclude radiological evaluation,9394 cephalo-metric measurements,95 fluoroscopic andfibroscopic studies,63 6496 computed tomo-graphic scanning and magnetic resonanceimaging.70 The respective indications of theseprocedures are not yet standardised in infants

and children. Further investigations and multi-centre studies are needed to clarify their clinicalusefulness for elucidating the pathophysiologyofOSA and for determining the best treatmentstrategy.

Tonsillectomy and adenoidectomy have beenthe most commonly recommended treatments.However, associated problems such as an ab-normally long soft palate, retroposition of themandible, or soft tissue infiltration behind thebase ofthe tongue must receive attention. Suchproblems may lead to residual symptoms aftertonsillectomy. Long term monitoring is re-quired in infants and children treated for sleep-related upper airway symptoms. Follow upevaluations should include a physical ex-amination, detailed questionnaires, andpolysomnographic recordings if necessary.Symptoms sometimes recur after puberty, espe-cially in boys.7' The usefulness of orthodontictreatment in children with mandibular ab-normalities after tonsillectomy is still underinvestigation.

In 1986 Guilleminault suggested that nasalcontinuous positive airway pressure (CPAP)could be used as an alternative to tracheostomyin young patients with OSA due to craniofacialabnormalities.97 The preliminary findings of amulticentre study conducted in North Americaand France have recently been reported.9899The patients were obese or had craniofacialabnormalities or residual problems after ton-sillectomy.1'0 The mean level of positive pres-sure used was lower than in adults with OSA.However, pressure requirements changed withgrowth, suggesting that CPAP requirementsshould be routinely re-evaluated at regular in-tervals. In general, the level of pressure was setto maintain the Sao2 above 95%. However,further investigations are needed to establishthe best criteria for selecting the optimal pres-sure. In infants with sleep-related increases inupper airway resistance Guilleminault re-commended that the level of nasal pressureshould be selected to maintain the oesophagealpressure no lower than -8 cm H20 duringsleep.54 Commercial masks for infants are avail-able, but in patients with craniofacial ab-normalities custom-made masks may benecessary. Finally, the BiPAP system may beuseful in some cases. Further studies are neededto determine the specific indications of bothCPAP and the BiPAP system.

In patients with craniofacial abnormalitiestreatment with CPAP enables the patient towait until optimal surgery can be performedand avoids the use of a tracheostomy in youngpatients. Close follow up is mandatory. Inpatients with the Pierre Robin syndrome somestudies have found that clinical and poly-somnographic abnormalities persisted duringchildhood and adolescence.9610' Finally,laryngomalacia can be treated successfully byepiglottoplasty.84

SummaryThe presence of increased upper airway res-istive loads during sleep can now be diagnosedby paediatricians. However, diagnostic criteria

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need to be further clarified to allow accurateidentification of episodes of partial airway ob-struction. New technological advances can beexpected to help to determine the clinical use-

fulness of ambulatory testing during sleep andthus to establish the indications for poly-somnographic investigations in the laboratory.A thorough investigation of the anatomical ab-normalities that contribute to airways ob-struction is essential for selecting the mostappropriate therapy. However, the order inwhich these investigations should be performedremains unclear. The diagnostic tools, in-cluding questionnaires and sleep testing, andmethods aimed at investigating patho-physiological mechanisms should be stand-ardised for multicentre studies. Familial factorsshould be taken into acount. The best strategyfor preventing the complications of the OSAsyndrome is to identify the disorder as earlyas possible. This requires close cooperationbetween adult physicians and paediatricianscalled upon to evaluate sleep-related disorders.

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