Sleep-Disordered Breathing and School Performance in Children

David Gozal, MD

ABSTRACT. Objective. To assess the impact of sleep-associated gas exchange abnormalities (SAGEA) onschool academic performance in children.

Design. Prospective study.Setting. Urban public elementary schools.Participants. Two hundred ninety-seven first-grade

children whose school performance was in the lowest10th percentile of their class ranking.

Methods. Children were screened for obstructivesleep apnea syndrome at home using a detailed parentalquestionnaire and a single night recording of pulse oxim-etry and transcutaneous partial pressure of carbon diox-ide. If SAGEA was diagnosed, parents were encouragedto seek medical intervention for SAGEA. School gradesof all participating children for the school year precedingand after the overnight study were obtained.

Results. SAGEA was identified in 54 children(18.1%). Of these, 24 underwent surgical tonsillectomyand adenoidectomy (TR), whereas in the remaining 30children, parents elected not to seek any therapeutic in-tervention (NT). Overall mean grades during the secondgrade increased from 2.43 6 0.17 (SEM) to 2.87 6 0.19 inTR, although no significant changes occurred in NT(2.44 6 0.13 to 2.46 6 0.15). Similarly, no academic im-provements occurred in children without SAGEA.

Conclusions. SAGEA is frequently present in poorlyperforming first-grade students in whom it adverselyaffects learning performance. The data suggest that asubset of children with behavioral and learning disabil-ities could have SAGEA and may benefit from prospec-tive medical evaluation and treatment. Pediatrics 1998;102:616–620; obstructive sleep apnea, hypoxia, sleepfragmentation, neurocognitive performance, hypercapnia.

ABBREVIATIONS. OSAS, obstructive sleep apnea syndrome; PS,primary snoring; SAGEA, sleep-associated gas exchange abnor-malities; Spo2, oxygen saturation by pulse oximetry; Tcco2, trans-cutaneous carbon dioxide tension; CO, children without SAGEAand without snoring; NT, no therapy; TR, children with SAGEAwho had surgical removal of hypertrophic adenoids and tonsils.

Sleep-disordered breathing is a relatively com-mon condition in otherwise healthy children.Although accurate figures on the prevalence of

obstructive sleep apnea syndrome (OSAS) in this agegroup are only now being actively sought, earlierestimates indicate that 1% to 2% of all children may

be affected.1,2 In contrast, up to 12% of children mayhave primary snoring (PS), ie, habitual snoring with-out alterations in sleep architecture, alveolar ventila-tion, and/or oxygenation.2–6 Because only a fractionof children with PS will have OSAS, and becauseclinical history and physical examination are usuallyinsufficient to establish the presence or severity ofOSAS, polysomnographic assessment is needed forthe definitive diagnosis of OSAS.7–9

In the vast majority of children with OSAS, surgi-cal removal of hypertrophic tonsillar and adenoidtissue will usually result in complete resolution ofOSAS. When OSAS is not recognized and is leftuntreated, significant morbidity such as failure tothrive,10–12 systemic hypertension,13 and pulmonaryhypertension with or without cor pulmonale14 maydevelop. However, the cognitive consequences ofdisrupted sleep architecture and hypoxemia as a re-sult of sleep-disordered breathing in children withOSAS are yet undefined in the pediatric popula-tion.15,16 A survey study of 782 children has recentlysuggested the association of daytime sleepiness, hy-peractivity, and aggressive behavior in children whosnored.2,5 Other studies reporting on smaller patientcohorts of patients with proven OSAS have also doc-umented parental reports of similar behavioral dis-turbances and their improvement after treatment ofOSAS.17–20 However, no prospective controlled stud-ies have yet examined whether OSAS indeed im-pinges on the academic performance of children.

Thus, the present study aimed to assess the inci-dence of sleep-associated gas exchange abnormalities(SAGEA) in first-grade children with academic diffi-culties and to determine the impact of SAGEA onschool performance. The methodologic approachwas based on two major considerations. First, be-cause oxygen hemoglobin saturation values below95% are a rare occurrence in otherwise sleepinghealthy children, only pulse oximetry and transcuta-neous carbon dioxide measurements were per-formed instead of the more conventional albeit oner-ous polysomnograms. Second, recordings wereperformed in the children’s homes to minimize thepossibility of a first night effect.21–23

METHODSIn an initial stage, first-grade children attending regular public

schools and who were academically ranked in the lowest 10thpercentile of their class were identified. After institutional ap-proval, parental informed consent and child assent were obtained.An OSAS childhood questionnaire was filled by the parents withthe assistance of the investigator.8 The questionnaire was modifiedto assign numerical scores to each of the answers ranging from 0(never), 1 (rarely), 2 (occasionally), 3 (frequently) to 4 (almost

From the Constance S. Kaufman Pediatric Pulmonary Research Laboratory,Tulane University Comprehensive Sleep Disorders Center, Department ofPediatrics, Tulane University School of Medicine, New Orleans, Louisiana.Received for publication Jan 12, 1998; accepted Apr 17, 1998.Reprint requests to (D.G.) Section of Pediatric Pulmonology, Department ofPediatrics, SL-37, Tulane University School of Medicine, 1430 Tulane Ave,New Orleans, LA 70112.PEDIATRICS (ISSN 0031 4005). Copyright © 1998 by the American Acad-emy of Pediatrics.

616 PEDIATRICS Vol. 102 No. 3 September 1998

always). The questions asked in the questionnaire were as follows:1) Does the child stop breathing during sleep?; 2) Does the childstruggle to breathe while asleep?; 3) Do you ever shake your childto make him/her breathe again?; 4) Do your child’s lips ever turnblue or purple while asleep?; 5) Are you ever concerned aboutyour child’s breathing during sleep?; 6) How often does your childsnore?; 7) How loud is the snore? (mildly quiet, medium loud,loud, very loud, extremely loud); 8) How often does your childhave a sore throat?; 9) Does your child complain of morningheadaches?; 10) Is your child a daytime mouth breather?; 11) Isyour child sleepy during daytime?; 12) Does your child fall asleepat school?; 13) Does your child fall asleep while watching televi-sion?.

All children underwent an overnight recording of pulse oxim-etry (Spo2) and pulse signal (Nellcor N 200; Nellcor Inc, Hayward,CA) and transcutaneous carbon dioxide tension (Tcco2; Sensor-Medics Transcend Cutaneous Gas System; SensorMedics, YorbaLinda, CA) at home. The Tcco2 sensor was repositioned after 4hours recording after an internal calibration routine. Tcco2 valuesafter sensor repositioning were discarded if they were not within10 mm Hg of those preceding the location change. Analog signalswere digitally acquired onto a MacIntosh PowerBook computersystem at 60 Hz sampling frequency using MacLab Digital Acqui-sition Software (ADInstruments, Castle Hill, Australia). To mini-mize scoring of waking periods, parents were requested to docu-ment the time at which their child seemed to be asleep and anyobvious nighttime arousals. Subsequent off-line analysis was per-formed by a custom-designed program using Igor software(WaveMetrics, Lake Oswego, OR).

SAGEA was considered to be present if in addition to a ques-tionnaire score of $5, more than two oxygen desaturation epi-sodes per hour recording,24–26 and/or a sustained elevation ofTcco2 .8 mm Hg compared with waking values during initialelectrode positioning and lasting .60% of total recording timewere present.27 Oxyhemoglobin desaturation episodes were de-fined as periods of at least 6 seconds that were associated with.5% Spo2 reductions compared with the previous stable baselinevalues or Spo2 measurements ,90% in the presence of adequatepulse signal.28 When no significant alterations in oxyhemoglobinsaturation and Tcco2 were recorded in the presence of a cumula-tive questionnaire score of $5, PS was considered to be present.

Parents of all children fulfilling SAGEA criteria were alerted tothe likely presence of sleep-disordered breathing, were providedwith a written report of the overnight home study, and encour-aged to contact their pediatrician for further evaluation and sur-gical treatment. Three months and 1 year later, parents werecontacted by telephone, questioned whether their child had re-ceived any surgical therapy for SAGEA, and answered again to allthe questions pertaining to the aforementioned questionnaire.

The academic grades of each child enrolled in the study wereobtained from the school for the school year preceding and theschool year after the overnight recording. Teachers were notifiedabout their pupils’ participation in a study but were unaware ofthe purpose of the study. The usual grades range from 0 to 4. Agrade of 2 is the minimal passing grade, and grades in the 2.0 to2.5 range are considered as representative of poor academic per-formance.

AnalysisData are presented as means 6 standard deviation unless oth-

erwise indicated. Four groups were defined, namely, childrenwithout SAGEA and without snoring (CO), children with PS,children with SAGEA who received no therapy (NT), and childrenwith SAGEA who underwent surgical removal of hypertrophicadenoids and tonsils (TR). The severity of nocturnal hypoxemiawas expressed as the number of oxyhemoglobin desaturationevents per hour of recording and as the nadir Spo2. The degree ofnighttime hypoventilation was recorded both as the peak Tcco2,and as the percentage of total recording time spent with Tcco2 .45mm Hg. Numerical variables were compared by two-way analysisof variance and the Newman-Keuls multiple range test for multi-ple comparisons or using paired t tests as appropriate. A P value,.05 was set as statistically significant.

RESULTSA total of 358 families were initially contacted. Of

these, 297 first-grade children whose school perfor-

mance was in the lowest 10th percentile of their classranking underwent an overnight recording, and theremaining 61 children either declined to participatein the study (n 5 56) or the poor quality of theovernight recording did not allow for adequate in-terpretation of the study (n 5 5). The latter childrendid not differ in any identifiable way from thosechildren who were enrolled in the study. Childrenwere recruited from a total of 32 public schools thatare evenly distributed among the various city geo-graphical areas.

Based on the diagnostic criteria, 66 children fittedthe PS criteria (22.2%) and 54 children (18.1%) wereidentified as SAGEA. Of these, 24 underwent surgi-cal adenotonsillectomy with or without a course ofintranasal steroids (TR). In the remaining 30 chil-dren, parents elected not to seek any therapeuticintervention (NT). The frequency of positive re-sponses to each question in the questionnaire, as wellas mean desaturation and hypoventilation scores forthe four groups are shown in Tables 1 and 2. NT andTR had similar cumulative questionnaire scores (Fig1; P 5 NS), which were significantly higher whencompared with either PS (P , .01) or CO (P , .01).

Figure 2 shows the changes in academic scores inthe four study groups throughout the time period.Overall mean grades increased from 2.43 6 0.17(SEM) during the first grade to 2.87 6 0.19 during thesecond grade in the TR group (P , .001). In contrast,no significant changes occurred in NT (2.44 6 0.13 infirst grade to 2.46 6 0.15 in second grade; TR vs NT:P , .01), in PS (2.42 6 0.15 and 2.46 6 0.16; P , .01vs TR), or CO (2.41 6 0.11 to 2.47 6 0.13; P , .01 vsTR).

A follow-up questionnaire was administered bytelephone only to NT and TR children. The meancumulative scores were 10.4 6 2.6 in NT and 1.7 62.4 in TR (P , .001).

DISCUSSIONThis study shows that SAGEA is a frequent occur-

rence among first-grade children who demonstrateacademic difficulty. Furthermore, when therapeuticintervention in the form of adenotonsillectomy isperformed, subsequent school performance is signif-icantly improved, suggesting a causal relationshipbetween SAGEA and learning ability.

Several technical aspects of this study merit someinitial comments. As mentioned in the introduction,it is important to emphasize that the use of SAGEAas an accurate and reliable indicator of OSAS inchildren as used in this study has only receivedpreliminary validation by other investigators,24,26 andcould introduce a potential diagnostic bias. Formalsleep studies on the children were not performed,and physiologic assessment was restricted to pulseoximetry and Tcco2 measurements. Thus, it is un-known whether sleep fragmentation because of mul-tiple arousals throughout the night was present ineither children with or without SAGEA. Further-more, because airflow was not measured, oxyhemo-globin desaturation episodes could have been theresult of respiratory events other than those relatedto upper airway obstruction. However, it should be

ARTICLES 617

stressed that hypoxemia is a highly unlikely occur-rence in otherwise healthy children,29 and it is there-fore believed that obstructive apnea events ac-counted for the vast majority if not the totality ofoxygen desaturations. Besides cost-related issues, an

additional reason for performing a more restrictedphysiologic study in the home environment ratherthan study all children in the sleep laboratory was tominimize the likelihood of a first night effect.21–23

However, even if such a first night effect was presentonly in children without SAGEA, it would not have

TABLE 1. Mean (6SD) Numerical Scores (Range, 0–4) in 177 CO, 66 PS, 30 NT, and 24 TR Children for Each Question and OverallCumulative Score

COn 5 177

PSn 5 66

NTn 5 30

TRn 5 24

Does the child stop breathing during sleep? 0.0 6 0.0* 0.20 6 0.44† 0.47 6 0.93*† 0.50 6 0.72*†Does the child struggle to breathe while asleep? 0.0 6 0.0* 0.12 6 0.33† 2.20 6 0.88*† 1.92 6 0.93*†Do you ever shake your child to make him/her breathe again? 0.0 6 0.0 0.0 6 0.0 0.0 6 0.0 0.03 6 0.18Do your child’s lips ever turn blue or purple while asleep? 0.0 6 0.0 0.0 6 0.0 0.06 6 0.25 0.04 6 0.20Are you ever concerned about your child’s breathing during sleep? 0.0 6 0.0* 0.24 6 0.43† 1.13 6 0.86*† 1.13 6 0.68*†How often does your child snore? 0.22 6 0.54*‡ 2.18 6 0.68‡ 2.40 6 1.00* 2.12 6 0.78*How loud is the snore? 0.15 6 0.47*‡ 1.74 6 0.85†‡ 1.27 6 0.64*† 1.92 6 0.78*†How often does your child have a sore throat? 0.60 6 0.65 0.76 6 0.68 1.20 6 0.61 1.63 6 0.88Does your child complain of morning headaches? 0.03 6 0.17* 0.11 6 0.36† 0.40 6 0.56*† 0.83 6 0.64*†Is your child a daytime mouth breather? 0.10 6 0.47*‡ 0.53 6 0.94†‡ 0.83 6 0.91*† 1.01 6 0.74*†Is your child sleepy during daytime? 0.0 6 0.0* 0.0 6 0.0† 0.63 6 0.72*† 0.75 6 0.79*†Does your child fall asleep at school? 0.01 6 0.07*‡ 0.39 6 0.63‡ 0.13 6 0.35*† 0.25 6 0.61*†Does your child fall asleep while watching television? 0.14 6 0.39* 0.30 6 0.60† 0.52 6 0.79*† 0.71 6 0.62*†Cumulative Score 1.25 6 1.29* 6.57 6 2.05† 11.43 6 2.34*† 12.52 6 2.35*†

Abbreviations: CO, children without SAGEA and without snoring; PS, primary snoring; NT, no therapy; TR, children with SAGEA whohad surgical removal of hypertrophic adenoids and tonsils.* CO vs NT or TR: P , .01.† PS vs NT or TR: P , .01.‡ CO vs PS: P , .01.

TABLE 2. Mean (6SD) Recording Duration, Oxyhemoglobin Desaturation, and Alveolar Hypoventilation Frequencies in 177 CO, 66PS, 30 NT, and 24 TR Children During an Overnight Home Recording

COn 5 177

PSn 5 66

NTn 5 30

TRn 5 24

Nadir Spo2 94.2 6 1.6* 93.6 6 1.8† 82.4 6 3.6*† 83.1 6 3.9*†Oxyhemoglobin desaturation (no./h) 0.0 6 0.0* 0.12 6 0.37† 4.7 6 2.4*† 4.9 6 2.6*†Peak Tcco2 47.4 6 2.4* 49.1 6 2.7† 54.9 6 3.8*† 54.6 6 4.1*†Alveolar hypoventilation (% recording time) 32.7 6 5.3* 45.8 6 5.7† 61.4 6 7.9*† 62.4 6 8.1*†Recording duration (minutes) 352.7 6 23.9 366.4 6 28.5 360.2 6 31.4 372.2 6 32.9

Abbreviations: CO, children without SAGEA and without snoring; PS, primary snoring; NT, no therapy; TR, children with SAGEA whohad surgical removal of hypertrophic adenoids and tonsils; Spo2, oxygen saturation by pulse oximetry; Tcco2, transcutaneous carbondioxide tension.* CO vs NT or TR: P , .01.† PS vs NT or TR: P , .01.

Fig 1. Mean (6SD) overall cumulative questionnaire responsescore in 177 CO (no SAGEA), 66 PS (primary or habitual snoringwithout SAGEA), 30 NT (untreated SAGEA), and 24 TR (treatedSAGEA) children. Scores in NT and TR were significantly higherthan in PS (#, P , .01) or CO (*, P , .01). PS versus CO; P , .01.

Fig 2. Mean (6SEM) school grades in 177 CO (no SAGEA), 66 PS(primary or habitual snoring without SAGEA), 30 NT (untreatedSAGEA), and 24 TR (treated SAGEA) children during first andsecond grade. (*, preadenotonsillectomy versus postadenotonsil-lectomy; P , .001).

618 OBSTRUCTIVE SLEEP APNEA SYNDROME AND SCHOOL PERFORMANCE

detracted from the major finding of this study, ie,treatment of children with SAGEA is associated withsubsequent improvements in school performance.

Obviously, some children with the upper airwayresistance syndrome may have been included in thePS group because the duration of Tcco2 elevationsdid not exceed 60% of total recording time29 andhypoxemia was not present. These patients may ob-viously be at risk for disrupted sleep architecture.30

However, even if the traditional sleep laboratorymultichannel approach was used, these upper air-way resistance syndrome cases would have beenmissed and would not have been included in a groupcategory in which treatment was recommended.30 Ofnote, these children would have been equally ex-cluded from the TR and NT groups using the diag-nostic algorithm, such that the academic improve-ments observed in the TR group cannot beattributable to such considerations. Per definition,children with PS did not have frequent hypoxemicevents that are thought to be the major determinantfor OSAS-associated morbidity in adults.31 However,snoring and increased upper airway resistance mayelicit significant pulsus paradoxus and leftward shiftof the interventricular cardiac septum in PS childreneven in the absence of oxygen desaturation, as wellas marked changes in intrathoracic pressures sug-gesting that unless esophageal pressures are re-corded, the diagnostic category of PS may not be acompletely innocent condition.30,32,33 Notwithstand-ing these concerns, the prevalence of PS (22.2%) andthat of SAGEA (18.1%) in this study were relativelyhigh when compared with most of those reported inthe literature for the general pediatric population.2–6

However, a high prevalence of snoring in children,which was similar to that found in this study, wasrecently reported by Owen and colleagues.34 In ad-dition, OSAS was found in 16% of African-Americanchildren and 6% of white children in a recent surveyof the general pediatric population in the UnitedStates,35 thereby indicating that sleep-disorderedbreathing may have been underestimated in earlierstudies. Based on the responses to question number6 in the questionnaire (How often does your childsnore?), 120 of 297 children (40%) surveyed had apositive answer. Children with PS had similar scoreson question number 6 than those found in childrenwith SAGEA (Table 1), suggesting that the figuresindeed reflect the true prevalence of snoring in thisparticular pediatric population. It is also possiblethat because this study was primarily conductedduring the high pollen season, allergic manifesta-tions may have contributed to more frequently pos-itive responses by the parents.36

We deliberately selected a group of children expe-riencing academic difficulties during their first yearof school. Based on the assumption that SAGEA inchildren would be detrimental to academic perfor-mance, it was expected to detect any improvement inschool performance more readily in these childrenwhen compared with academically average orgreater than average children. Thus, it is possiblethat the high prevalence of snoring and SAGEA inthis cohort could reflect a clustering phenomenon

attributable to the effect of OSAS on academic per-formance. Indeed, all TR children improved theiracademic scores after adenotonsillectomy (Fig 2),such that only 2 of the 24 TR children remained in thelowest tenth percentile of their class after SAGEAtherapy. Such clustering had been previously notedby Weissbluth et al20 who studied a small group ofchildren selected for developmental, academic, orbehavioral problems.

The high prevalence of snoring and SAGEA in thiscohort could be hypothetically explained if relativelyless stringent diagnostic criteria were used than gen-erally used by most centers. For example, it is nowwell accepted that the diagnostic criteria used inadults are inadequate when applied to children.37,38

However, brief oxygen desaturations of .4% occur-ring at a rate of #3 events/hour may occur in somenormal children19 while desaturation episodes to,90% are rare and their frequency decreases withage.26,39 Furthermore, increasing the stringency of theoxygen desaturation criteria to .8% instead of .5%decreases, would have disqualified only 1 child fromthe TR group and 2 children in the NT group, andassigned them to the PS group. Therefore, additionalstudies examining the prevalence of SAGEA and PSin children without low school grades will be re-quired to confirm the postulated cohort selectionclustering found in this study.

Although widely cited as a major complication ofOSAS, developmental and behavioral disturbancesin children with OSAS have been mostly inferredfrom case studies.2,5,17–20 In an initial attempt to estab-lish a causal relationship between OSAS and neuro-cognitive function, Rhodes and colleagues40 have re-cently reported inverse correlations betweenmemory and learning performance and the apnea/hypopnea index in 14 morbidly obese children.However, these investigators did not have a controlgroup, and no intervention-related outcomes weredescribed. Therefore, the current report provides thefirst randomized prospective interventional study onthe effects of OSAS on learning. It should be stressedat this point that school grades provide only a veryrudimentary assessment of cognitive, behavioral,and learning capabilities, and that more elaboratetools will be needed in future studies. However,because teachers were unaware of the results of theovernight study, grade scoring of each child enrolledin the study was a truly unbiased process. Further-more, allocation to either NT or TR groups was theresult of a parental decision based on the same rec-ommendation to seek therapeutic intervention. Thus,the investigators had no involvement in the random-ization process to TR and NT groups. A follow-uphome study was not performed in TR and NT chil-dren. However, a significant reduction in the ques-tionnaire score occurred only the TR group, suggest-ing that adenotonsillectomy indeed resolved SAGEAin these children whereas no such improvementsoccurred in the NT group. In addition, such changesin questionnaire scores do not support a learningeffect introduced by readministration of the samequestionnaire. The findings are in close agreementwith the recent recommendations of an expert panel

ARTICLES 619

that does not advocate a follow-up polysomno-graphic study for the majority of children with SA-GEA after undergoing adenotonsillectomy.7,35 Thesignificant improvement in school performance inthe TR group demonstrates that some component ofthe learning difficulties exhibited by these children isattributable to sleep-disordered breathing. It remainsunclear whether earlier diagnosis and interventionwill further ameliorate one or more aspects of neu-rocognitive function.

CONCLUSIONIn summary, it was demonstrated that there was

an unusually high prevalence of snoring and noctur-nal gas exchange abnormalities in a cohort of chil-dren who were academically poor achievers. Whensuccessful therapeutic intervention was adminis-tered to those children in whom SAGEA waspresent, significant improvements in school gradesoccurred. It is therefore recommended that sleep-related symptoms should be actively sought in chil-dren with developmental or learning problems, andthat referral for evaluation of sleep-disorderedbreathing should occur early rather than late.

ACKNOWLEDGMENTSPartial support was received from the National Institute of

Health (Grant HD-01072), the Maternal and Child Health Bureau(Grant MCJ-229163), and the American Lung Association (GrantCI-002-N).

I wish to thank all the students who provided technical assis-tance with the overnight studies, and all the school teachers,parents, and children for their patience and cooperation.

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620 OBSTRUCTIVE SLEEP APNEA SYNDROME AND SCHOOL PERFORMANCE