0
We're unable to sign you in at this time. Please try again in a few minutes.
Retry
We were able to sign you in, but your subscription(s) could not be found. Please try again in a few minutes.
Retry
There may be a problem with your account. Please contact the AMA Service Center to resolve this issue.
Contact the AMA Service Center:
Telephone: 1 (800) 262-2350 or 1 (312) 670-7827  *   Email: subscriptions@jamanetwork.com
Error Message ......
Article |

Variation of Cognition and Achievement With Sleep-Disordered Breathing in Full-term and Preterm Children FREE

Judy L. Emancipator, MS; Amy Storfer-Isser, MS; H. Gerry Taylor, PhD; Carol L. Rosen, MD; H. L. Kirchner, PhD; Nathan L. Johnson, MS; Anne Marie Zambito, MPH; Susan Redline, MD, MPH
[+] Author Affiliations

Author Affiliations: Department of Pediatrics, Rainbow Babies and Children's Hospital, Case Western Reserve School of Medicine, Cleveland, Ohio.


Arch Pediatr Adolesc Med. 2006;160(2):203-210. doi:10.1001/archpedi.160.2.203.
Text Size: A A A
Published online

Objective  Pediatric sleep-disordered breathing (SDB) has a disproportionately high prevalence in children who were preterm infants (preterm children) and is associated with behavioral comorbidity. Exposure to intermittent hypoxemia and sleep disruption may contribute to cognitive impairment. We quantified the association of SDB with cognition and achievement and determined whether preterm children are at a differentially increased risk for SDB-related impairments.

Design  Cross-sectional analyses.

Setting  Urban community.

Participants  Eight hundred thirty-five children, aged 8 to 11 years.

Intervention(s)  None.

Main Outcome Measures  Scores on the Peabody Picture Vocabulary Test–Revised, Kaufman Assessment Battery for Children, and Continuous Performance Test.

Results  One hundred sixty-four children had SDB. In unadjusted analyses, children with SDB had poorer scores on almost all tests of cognition and achievement. Group differences were attenuated after adjusting for socioeconomic status; in these analyses, children with SDB scored lower on the Peabody Picture Vocabulary Test–Revised (mean ± SE score, 100.5 ± 1.4 vs 103.6 ± 0.7; P = .04), and the Kaufman Assessment Battery for Children riddles and triangles subscales. Associations were stronger in preterm than in full-term children. Of the sleep measures, snoring history was most strongly correlated with indices of cognition and achievement.

Conclusions  Although moderate group differences were observed for almost all cognitive measures, an attenuation of effects was observed once socioeconomic status was considered. The deficits in selective measures of academic abilities, language comprehension, and planning and organizational skills suggest a negative impact of SDB on achievement and cognition. Stronger associations in preterm children suggest the importance of screening for snoring, a good predictor of cognitive function in this population.

Sleep-disordered breathing (SDB), a common but underrecognized chronic health problem, is characterized by episodic periods of occlusion of the upper airway during sleep, often associated with oxygen desaturation, arousal, and impaired sleep quality. Symptoms include loud snoring, frequent awakenings, and excessive sleepiness. In adults, SDB is associated with a myriad of neurocognitive difficulties, including deficits in general intellectual function, attention, memory, and organizational abilities.13

Pediatric SDB may affect 2% to 4% of children, with a higher prevalence in certain subgroups, such as African American children and those who were preterm infants (preterm children).4 The health impact of childhood SDB, however, is not well understood. Because learning is incremental and a strong foundation is essential during childhood, it is important to evaluate the association of SDB with children's cognitive and academic skills. Previous research has been limited by small numbers of participants,5,6 a focus on children referred for clinical evaluation (in whom referral may have been stimulated by behavioral or cognitive concerns),5,6 nonstandardized assessments of cognition,7 exclusive reliance on parental observations of SDB symptoms,8 incomplete control for confounding factors,9 and inclusion of small numbers of children with objective evidence of sleep apnea.10

This study evaluates the performance of 835 children from a community-based sample on objective assessments of cognitive skills and academic achievement. We compared subgroups with and without SDB to address the following hypotheses: (1) SDB is associated with deficits in cognitive abilities and achievement; (2) preterm children, because of increased risk of neurodevelopmental disabilities related to early-life hypoxemia and ischemic injury, are at a differentially increased risk for SDB-related cognitive dysfunction; and (3) severity of overnight hypoxemia will be positively correlated with the extent of cognitive deficits.

STUDY POPULATION

Methods of recruitment to the Cleveland Children's Sleep and Health Study have been previously reported.4 In brief, the Cleveland Children's Sleep and Health Study is an urban community-based cohort of 907 children studied at 8 to 11 years of age. It was originally assembled as a stratified random sample of full-term and preterm children born at hospitals in the Cleveland, Ohio, area between January 1, 1988, and December 31, 1993. This cohort was designed to overrepresent African American and preterm children. Participants were excluded from analyses owing to inability to ascertain SDB status (n = 65) or missing cognitive function data (n = 7).

STUDY PROTOCOL

Children underwent assessment at 8 to 11 years of age during a home visit, when health information was ascertained with the use of a pediatric modification of a validated questionnaire.11 Trained research assistants (J.L.E. and A.M.Z.), blinded to the child's SDB status, administered the cognitive tests. On the night after the testing battery, children underwent an in-home sleep study. A small proportion (14%) of families and children were interviewed in a research setting rather than the home.

Institutional review boards at the participating hospitals approved the protocol. Written informed consent was obtained from the child's guardian, and assent was obtained from the child.

SDB ASSESSMENTS

Details on the methods for the assessing SDB have been reported.4 In brief, a 6-channel monitor recorded respiration (with rib cage and abdominal inductance plethysmography), heart rate, oxygen saturation level, and body position (SomnoStar PT-2; SensorMedics, Yorba Linda, Calif). Obstructive sleep apnea was defined as an obstructive apnea-hypopnea index (OAHI) of greater than or equal to 5 events per hour and/or an obstructive apnea index (OAI) of greater than or equal to 1 event per hour. The approach for quantifying obstructive sleep apnea has been validated by comparing the OAHI from the home study with a similar index from findings of 12-channel laboratory-based polysomnography in 55 children in whom the 2 tests were performed within 3 months (intraclass correlation coefficient, 0.85).4 Snoring was ascertained via a questionnaire that requested the parent to report the frequency of loud snoring by the child during the past month on a 5-point scale, ranging from never to always. Habitual snoring was defined as loud snoring during the past month, occurring at least 1 to 2 times per week. Children with obstructive sleep apnea and/or who were habitual snorers were categorized as having SDB, whereas children who were not habitual snorers and did not have obstructive sleep apnea were categorized as not having SDB. For exploratory analyses, children were also classified as nonsnorers vs snorers (ie, occurring rarely or more often per week, during the past month).

NEUROCOGNITIVE ASSESSMENTS

Cognitive skills and academic achievement were assessed with the Peabody Picture Vocabulary Test–Revised (PPVT-R),12 Kaufman Assessment Battery for Children (K-ABC),13 and Continuous Performance Test (CPT).14 To administer the PPVT-R, spoken words are presented in increasing order of difficulty, and the examinee is asked to point to 1 of 4 pictures that shows the meaning of the word. The test measures comprehension of spoken words but also requires the ability to selectively attend to the response choices. The K-ABC consists of 13 subscales and 5 composite scales assessing a range of mental processing abilities and written language and mathematics skills. The K-ABC mental processing composite consists of sequential and simultaneous global mental skills. Specific subscales require memory, eye-hand coordination, spatial skills, problem solving, and executive functions that include the abilities to attend to the task and plan and organize one's approach. The CPT is a 14-minute computerized test of sustained attention and response inhibition. This test requires the child to press a key whenever an x appears on the screen and not to press the key when nontarget stimuli are presented. Time to respond, correct and incorrect responses, and missed targets are recorded. Raw scores on the K-ABC and PPVT-R were converted to age-adjusted standard scores based on published normative values.13,14 Standard scores for the PPVT-R and K-ABC global measures have a mean of 100 and SD of 15, with higher scores reflecting better cognitive performance. Our primary outcome measures were standard scores from the PPVT-R, the K-ABC mental processing composite and achievement scales, the reaction time, and an index describing the child's ability to detect target stimuli while inhibiting responses to nontargets (response discrimination, D-prime) from the CPT.

STATISTICAL ANALYSIS

Analyses were designed to obtain an unbiased estimate of the association between SDB and each measure of cognitive performance. Covariates and potential confounders, including the child's age, sex, birth weight, and indices of socioeconomic status (SES), were selected on the basis of theory and empirical research. Socioeconomic status was assessed using data on caregiver education, caregiver marital status, and census tract median income. Median income from the 2000 census was obtained by matching the child's address to the corresponding census tract. To control for prematurity and birth weight, the following 4 mutually exclusive categories were created on the basis of a combination of preterm status and birth weight: premature with extremely low birth weight (<1000 g); premature with very low birth weight (1000-1499 g); premature with low birth weight (≥1500 g), and full-term with normal birth weight (≥2500 g).

Groups were compared using 2-sample t tests, Wilcoxon rank sum tests, and the Pearson χ2 test for normally distributed, skewed, and categorical data, respectively (SAS software, version 9.1; SAS Institute Inc, Cary, NC). Spearman correlations were used to assess the magnitude of the association between cognitive outcomes and sleep measures. Multiple linear regression was used to assess the relationship between SDB and each cognitive outcome, adjusting for potential confounders. Graphical techniques were used to assess the relationship between continuous covariates and cognitive outcomes. Models were fit without covariate adjustment (unadjusted); adjustment for age, sex, and birth weight category (partially adjusted); and adjustment for age, sex, birth weight category, caregiver education and marital status, and median income (fully adjusted). Unless otherwise indicated, data are expressed as mean ± SD.

The sample was approximately 50% female and had a mean age of 9.5 ± 0.8 years (Table 1). By design, approximately half of the sample (45.9%) consisted of preterm infants, including 9.0% with extremely low birth weight (<1000 g). The median income from the census tract data was $46 000 per year, and the median poverty rate was 6.2%.

One hundred sixty-four children (19.6%) children were classified as having SDB. As reported previously,4 children with SDB were significantly more likely to be African American and to have been born prematurely. They also were more likely to live in a neighborhood with lower median income, live in a single parent household, and have a caregiver with a high school education or less. The 2 groups did not significantly differ with respect to age and sex. Tonsillectomy and/or adenoidectomy were reported more commonly among children with SDB compared with children without SDB.

Sleep characteristics of the sample are shown in Table 2. Overall, 21 children had an OAHI of 5 or greater, and 34 children had an OAI of 1 or greater. As expected, the percentage of sleep time at an oxygen desaturation level of less than 90% was higher among children with SDB. Approximately two thirds of parents reported that their child never snored, whereas 17.6% reported habitual snoring. Parents reported that their child slept 9.2 ± 0.9 hours on average, with no difference for children with and without SDB.

Table 3 shows the distribution of the unadjusted, partially adjusted, and fully adjusted PPVT-R and K-ABC scores. The unadjusted and partially adjusted (ie, not including indices of SES) results show that the SDB group scored significantly lower on the PPVT-R and K-ABC summary measures. The unadjusted analyses showed an average difference of 9 points for the PPVT-R and 5 points for the K-ABC summary scales, effect sizes that are moderate to large. There was a small attenuation of group differences once the effects of age, sex, and birth weight were considered (partially adjusted results). Further adjustment for SES, with consideration of caregiver education and marital status and median income (the latter explaining the largest proportion of variance in cognitive measures), resulted in considerable attenuation of SDB group differences. Although in fully adjusted analyses the SDB group tended to score lower on all tests and subtests, significantly lower scores were observed for the PPVT-R and the K-ABC riddles and triangles subscales only. Performance measured during the CPT showed a longer mean reaction time in children with SDB; however, this measure and response discrimination were not significantly associated with SDB after covariate adjustment. Excluding children who had had a tonsillectomy and/or adenoidectomy reduced statistical power slightly, but provided qualitatively similar results.

Table Graphic Jump LocationTable 3. Distribution of Cognition and Achievement Measures by SDB*

To address whether associations of SDB with cognitive and achievement skills may be stronger in a vulnerable group, analyses were repeated stratifying by preterm status, and the results for the preterm group are presented in Table 4. The fully adjusted models showed that preterm children with SDB performed significantly worse on the PPVT-R and the K-ABC achievement and simultaneous global scales and riddles and triangles subscales. In contrast, the differences in neurocognitive function between the full-term children with and without SDB did not achieve statistical significance after fully adjusting for covariates (data not shown).

Table Graphic Jump LocationTable 4. Distribution of Cognition and Achievement Measures in Preterm Children by SDB*

To explore which physiological stresses associated with SDB are most closely associated with neurocognitive deficits, the strength of the associations of overnight oxygen desaturation; frequencies of apnea and hypopnea and snoring; and sleep time with each cognitive outcome were assessed. The unadjusted and fully adjusted correlations show weak associations between cognitive outcomes and the oxygen saturation measures and OAHI and OAI variables, particularly after covariate adjustment (Table 5). Sleep time shows a modest, positive correlation with cognitive measures in unadjusted analyses only. Frequency of snoring has the strongest association with the cognitive outcomes, which are attenuated but remain statistically significant after covariate adjustment.

Table Graphic Jump LocationTable 5. Partial Spearman Correlations Relating Sleep Indices With Measures of Cognition and Achievement for the Analytic Sample*

Graphic techniques used to further assess the association between snoring frequency and cognitive performance showed that children who were reported to never snore in the preceding month had higher scores compared with snoring children, with no difference in those in whom snoring frequency was reported as rare compared with more frequent. Analyses that substituted snoring status as the primary predictor rather than SDB showed that the mean differences between groups were slightly greater compared with the main analysis in which SDB was the primary predictor (Table 6). In fully adjusted analyses, many of these group differences are statistically significant, with snorers demonstrating lower scores on the PPVT-R, K-ABC achievement global scale, and K-ABC subscales arithmetic (97.8 ± 0.9 vs 100.7 ± 0.7; P = .007), faces and places (100.8 ± 0.9 vs 103.2 ± 0.6; P = .01), reading/decoding (99.1 ± 0.8 vs 101.9 ± 0.6; P = .005), reading/understanding (100.8 ± 0.8 vs 103.0 ± 0.6; P = .02), and riddles and triangles (Table 6). Significant differences in the CPT measures were not observed. Results were essentially unchanged in analyses excluding children with an elevated OAHI or OAI.

Table Graphic Jump LocationTable 6. Distribution of Cognition and Achievement Measures by Snoring History*

A major component of SDB morbidity is thought to relate to neuropsychological deficits, with concern that in children, SDB may result in long-term decrements in academic achievement.8 Although childhood SDB has been associated consistently with behavioral morbidity, including conduct problems and aggressiveness,1518 fewer data are available that address the association of childhood SDB and cognitive performance and achievement. This study extends previous research, addressing the association of a range of cognitive functions with SDB in a large, diverse pediatric population. The availability of several measures of SES allowed us to rigorously address potential environmental confounders. Inclusion of a large preterm group permitted assessment of low birth weight and prematurity as possible confounders while also providing an opportunity to explore differential susceptibility of a preterm population. These findings show (1) moderate to large SDB group differences for almost all cognitive measures (ie, effect sizes of 0.3-0.6), but evidence of considerable attenuation of group differences once SES (particularly neighborhood median income) was considered; (2) persistence of small to modest group differences for the PPVT-R and 2 K-ABC subscales (riddles and triangles) in adjusted analyses; (3) stronger associations of SDB with deficits in cognitive ability and academic achievement in preterm compared with full-term children; and (4) evidence that of all SDB measures (including oxygen saturation, the frequency of apneas and hypopneas, and sleep time), snoring history was most strongly associated with cognitive deficits.

Although large deficits in a broad range of neurocognitive tests were observed between SDB groups in unadjusted or partially adjusted analyses, differences were attenuated once SES was accounted for by adjusting for caregiver education and marital status and neighborhood income level. To our knowledge, this is the first time that an index of neighborhood poverty has been considered in relation to SDB. Because this measure may serve as a proxy for a wide variety of social and environmental risk factors that influence development, including quality of education and neighborhood structure, it may provide additional information over what is usually available from parent self-reported income. The findings suggest that some of the effects of childhood SDB in the literature may have been overestimated owing to incomplete consideration of confounding due to SES and premature birth or owing to other selection biases, eg, studying children at high risk for problems in behavior, cognition, and achievement.

Our findings of modest and selective cognitive deficits in children with SDB are consistent with results of previous research showing children with SDB to have poorer performances on a restricted range of neurocognitive assessments administered as part of larger test batteries.6,9,10,19,20 In several studies, deficits were greatest for language, spatial skills, attention, and organizational skills.10,21 In our study, the larger SDB group differences found for the PPVT-R than the K-ABC scores may reflect the relative sensitivity of the former test to accumulated verbal knowledge. This test also requires inhibition of impulsive responses—behaviors that are impaired in children with SDB.1618,21,22 Impairment of scores on the K-ABC riddles subscale, which requires the child to solve a verbal puzzle, is also consistent with limitations in verbal comprehension and the ability to be selective and to plan in responding to tasks. These deficits are similar to those suggested by weaknesses on the PPVT-R. The K-ABC triangles subscale scores were also impaired in children with SDB. The triangles subscale is the only timed test, and it requires children to plan and organize their responses in solving spatial puzzles, placing demands on multiple executive functions. These deficits are consistent with data from adult studies that show preferential deficits in planning and organizational skills and in efficiency of performance with SDB,13 and with evidence that adults with SDB have a relatively poorer performance on timed tests, including those that make demands on spatial abilities.23

The pattern of deficits observed suggests that children with SDB are vulnerable to weaknesses in attending selectively to tasks and planning their responses, and these weaknesses contribute over time to more pronounced deficits in accumulated knowledge and academic skills. The latter deficits are illustrated by the SDB group's reduced scores in verbal comprehension and the reductions in academic achievement observed among snorers. Although other investigators have shown deficits in learning, memory, and general intelligence,5,9,10 these latter studies included children referred for evaluation with high degrees of medical or psychological comorbidity5 or did not comprehensively address confounders such as SES and prematurity.5,9 Data from a subsample of children recruited from the Infant Practices Study10 showed reductions in both memory and general intelligence in 5-year-old children with SDB symptoms. However, the average scores for the SDB and non-SDB groups were both higher than normative data. These findings were based on parent-reported symptoms, without evidence that deficits were specific to the small number of children with breathing pauses.10

Although we posited that impairments in sustained attention may underlie deficits in other cognitive functions, we did not find evidence of these deficits when a standardized continuous performance task was used. This agrees with the findings of Beebe et al21 and Gottlieb et al,10 who also did not find significant attentional deficits in SDB when similar measures of visual attention were used. The CPT, originally designed as a tool for evaluating attention-deficit/hyperactivity disorder, may not be sufficiently sensitive in children with mild SDB, who are not overtly somnolent. Alternatively, computer-based vigilance tasks may be less discriminating in current cohorts of children who are now regularly exposed to computer-based video games compared with the older cohorts in whom such tests were originally developed.

The pathophysiological basis for neurocognitive deficits occurring with SDB is thought to relate to exposure to intermittent hypoxemia and sleep disruption. Animal experiments have shown that intermittent hypoxemia produces apoptosis in the cerebral cortex and hippocampus,24 which correlates with spatial learning deficits.25 In humans, such exposures may disproportionately affect planning and organizational abilities (ie, executive functions), which are particularly dependent on the basal ganglia and frontal lobes, areas sensitive to intermittent hypoxemia. Accordingly, in several studies of adults, hypoxemia most closely predicted deficits in executive functions and psychomotor skills, whereas sleepiness predicted attentional deficits.1,26 One study showed no threshold effect for hypoxemia or the frequency of breathing pauses, suggesting that even mild SDB may have an adverse impact on neurocognitive function.3

We did not observe neurocognitive deficits to be linearly associated with frequency of breathing pauses or severity of overnight desaturation. This differs from the findings from a German study of children that showed that overnight oxygen nadir was associated with selective impairment in arithmetic scores.7 The clinical implications of this latter finding are unclear, because no other desaturation variable was associated with impairment in any academic measure, and because oxygen nadir may not provide a reliable estimate of overnight hypoxemia. In contrast, we found that reported snoring frequency was significantly correlated with cognitive and achievement scores. Even in fully adjusted analyses, significant associations were demonstrated between snoring and scores on the K-ABC achievement scale, 6 of the K-ABC subscales, and the PPVT-R. These findings are consistent with literature that has reported cognitive deficits in primary snorers27 and in children with symptoms of SDB who have few breathing pauses.10 The relatively small number of children with severe SDB might have limited our ability to detect dose-response relationships with indices of SDB severity. Nonetheless, these data suggest that snoring, especially assessed in general samples without high degrees of SDB severity, may provide a useful measure of chronic sleep disruption. Reported snoring at 8 to 11 years of age also may identify children who had experienced more severe SDB at earlier ages, including times of developmental susceptibility to adverse cognitive effects of hypoxemia. Although we were surprised that habitual snoring was not more strongly associated with cognitive deficits than any snoring in the preceding month, it is possible that parents of middle school children underestimate their children's snoring frequency. Regardless of the physiological basis for this observation, our data suggest that obtaining a snoring history may be useful for screening among children at risk for cognitive and achievement deficits.

A previous report from our group4 observed a 4-fold higher prevalence of SDB in preterm children, and our present study was designed to test whether this vulnerable group experiences disproportionate morbidity associated with SDB. Preterm children have a range of learning and cognitive deficits occurring in direct proportion to their immaturity,28,29 including deficits in language abilities, verbal learning, and spatial and organizational skills.28 Previous research in preterm children has not considered whether unrecognized SDB may account for such deficits. Conversely, previous studies of SDB have not considered prematurity as a contributor to SDB-associated comorbidity. Our analyses identify selective cognitive deficits attributable to SDB, even after adjusting for preterm status and birth weight. Furthermore, among children with predominantly mild SDB, SDB-associated comorbidity appears more pronounced in preterm than in full-term children. Although prospective studies are required, these results suggest that children with more limited cognitive reserve and/or who have had developmental or perinatal stresses may be especially vulnerable to mild SDB in childhood. These children may be less able to compensate for SDB-related cognitive deficits, possibly because of diminished plasticity of function after early brain insults.3032 Alternatively, a noncausal association between SDB and cognitive dysfunction in preterm children is plausible; ie, developmental and early life stresses could increase a predisposition to SDB by adversely influencing upper airway neuromuscular control and/or airway anatomy. In either case, because some research suggests beneficial effects on cognition with treatment of childhood SDB,15,33 there may be utility in efforts to more aggressively screen for snoring and SDB in premature children.

The strengths of our study include the large sample size with a wide range of SES and ethnicity and inclusion of sufficient numbers of preterm children to evaluate associations with birth weight and prematurity. The study used objective measures of neurocognitive function and nocturnal cardiorespiratory monitoring and contained robust measures of SES. Study weaknesses include the relatively low proportion of children with severe SDB, preventing a full evaluation of the extent to which marked hypoxemia or sleep disruption may contribute to cognitive deficits. Although validated measures for the OAHI were used that correlate excellently with full in-laboratory measures,4 the home sleep studies did not include direct measures of sleep stages or arousal, preventing evaluation of these factors.

Our analyses suggest that some of the reported cognitive and achievement deficits attributable to mild SDB in the literature may have been overestimated owing to confounding by SES and prematurity. However, our data on a large birth cohort are consistent with an association between mild SDB, including snoring, and selective deficits in verbal comprehension and executive functions, with effects relatively greater in preterm children, who may be particularly vulnerable to stresses associated with SDB. Furthermore, our data suggest the potential utility of snoring history as a screening tool, particularly in preterm children, who appear to be at increased risk for both SDB and SDB-associated cognitive deficits.

Correspondence: Susan Redline, MD, MPH, 11100 Euclid Ave, Department of Pediatrics, Case Western Reserve University School of Medicine, Cleveland, OH 44106-6003 (sxr15@case.edu).

Accepted for Publication: September 1, 2005.

Funding/Support: This study was supported by grants HL HL60957, K23 HL04426, M01 RR00080, RO1 NR02707, and RO1070916 from the National Institutes of Health, Bethesda, Md.

Naegele  BThouvard  VPepin  JL  et al.  Deficits of cognitive executive functions in patients with sleep apnea syndrome Sleep 1995;1843- 52
PubMed
Bedard  MAMontplaisir  JRicher  FRouleau  IMalo  J Obstructive sleep apnea: pathogenesis of neuropsychological deficits J Clin Exp Neuropsychol 1991;13950- 964
PubMed
Adams  NStrauss  MSchluchter  MRedline  S Relation of measures of sleep-disordered breathing to neuropsychological functioning Am J Respir Crit Care Med 2001;1631626- 1631
PubMed
Rosen  CLLarkin  EKKirchner  HL  et al.  Prevalence and risk factors for sleep-disordered breathing in 8- to 11-year-old children: association with race and prematurity J Pediatr 2003;142383- 389
PubMed
Rhodes  SKShimoda  KCWaid  LR  et al.  Neurocognitive deficits in morbidly obese children with obstructive sleep apnea J Pediatr 1995;127741- 744
PubMed
Beebe  DWGroesz  LWells  CNichols  AMcGee  K The neuropsychological effects of obstructive sleep apnea: a meta-analysis of norm-referenced and case-controlled data Sleep 2003;26298- 307
PubMed
Urschitz  MSWolff  JSokollik  C  et al.  Nocturnal arterial oxygen saturation and academic performance in a community sample of children Pediatrics 2005;115e204- e209
PubMed
Gozal  DPope  DW Snoring during early childhood and academic performance at ages thirteen to fourteen years Pediatrics 2001;1071394- 1399
PubMed
Kaemingk  KLPasvogel  AEGoodwin  JL  et al.  Learning in children and sleep disordered breathing: findings of the Tucson Children's Assessment of Sleep Apnea (tuCASA) prospective cohort study J Int Neuropsychol Soc 2003;91016- 1026
PubMed
Gottlieb  DJChase  CVezina  RM  et al.  Sleep-disordered breathing symptoms are associated with poorer cognitive function in 5-year-old children J Pediatr 2004;145458- 464
PubMed
Kump  KWhalen  CTishler  PV  et al.  Assessment of the validity and utility of a sleep-symptom questionnaire Am J Respir Crit Care Med 1994;150735- 741
PubMed
Umberger  FG Peabody Picture Vocabulary Test-Revised  Kansas City, Mo Test Corp America1985;
Merz  WR Kaufman Assessment Battery for Children  Kansas City, Mo Test Corp America1984;
Connors  CK Connor's Continuous Performance Test  North Tonawanda, NY Multi-Health System1995;
Ali  NJPitson  DStradling  JR Sleep disordered breathing: effects of adenotonsillectomy on behaviour and psychological functioning Eur J Pediatr 1996;15556- 62
PubMed
Chervin  RDArchbold  KHDillon  JE  et al.  Inattention, hyperactivity, and symptoms of sleep-disordered breathing Pediatrics 2002;109449- 456
PubMed
Gottlieb  DJVezina  RMChase  C  et al.  Symptoms of sleep-disordered breathing in 5-year-old children are associated with sleepiness and problem behaviors Pediatrics 2003;112870- 877
PubMed
Rosen  CLStorfer-Isser  ATaylor  HGKirchner  HLEmancipator  JLRedline  S Increased behavioral morbidity in school-aged children with sleep-disordered breathing Pediatrics 2004;1141640- 1648
PubMed
Beebe  DWGozal  D Obstructive sleep apnea and the prefrontal cortex: towards a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits J Sleep Res 2002;111- 16
PubMed
O’Brien  LMMervis  CBHolbrook  CR  et al.  Neurobehavioral correlates of sleep-disordered breathing in children J Sleep Res 2004;13165- 172
PubMed
Beebe  DWells  CJeffries  JChini  BKalra  MAmin  R Neuropsychological effects of pediatric obstructive sleep apnea J Int Neuropsychol Soc 2004;10962- 975
PubMed
Chervin  RDDillon  JEArchbold  KHRuzicka  DL Conduct problems and symptoms of sleep disorders in children J Am Acad Child Adolesc Psychiatry 2003;42201- 208
PubMed
Kim  HCYoung  TMatthews  CGWeber  SMWoodard  ARPalta  M Sleep-disordered breathing and neuropsychological deficits Am J Respir Crit Care Med 1997;1561813- 1819
PubMed
Gozal  ERow  BWSchurr  AGozal  D Developmental differences in cortical and hippocampal vulnerability to intermittent hypoxia in the rat Neurosci Lett 2001;305197- 201
PubMed
Gozal  DDaniel  JMDohanich  GP Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat J Neurosci 2001;212442- 2450
PubMed
Bedard  MAMontplaisir  JMalo  JRouleau  I Persistent neuropsychological deficits and vigilance impairments in sleep apnea syndrome after treatment with continuous positive airway pressure J Clin Exp Neuropsychol 1993;15330- 341
PubMed
O’Brien  LMMervis  CBHolbrook  CR  et al.  Neurobehavioral implications of habitual snoring in children Pediatrics 2004;11444- 49
PubMed
Bhutta  ATCleves  MACasey  PHCradock  MMAnand  KJ Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis JAMA 2002;288728- 737
PubMed
Taylor  HGMinich  NBangert  BFilipek  PAHack  M Long-term neuropsychological outcomes of very low birth weight: associations with early risks for periventricular brain insults J Int Neuropsychol Soc 2004;10987- 1004
PubMed
Kesler  SRMent  LRVohr  B  et al.  Volumetric analysis of regional cerebral development in preterm children Pediatr Neurol 2004;31318- 325
PubMed
Luciana  M Cognitive development in children born preterm: implications for theories of brain plasticity following early injury Dev Psychopathol 2003;151017- 1047
PubMed
McGauhey  PJStarfield  BAlexander  CEnsminger  ME Social environment and vulnerability of low birth weight children: a social-epidemiological perspective Pediatrics 1991;88943- 953
PubMed
Gozal  D Sleep-disordered breathing and school performance in children Pediatrics 1998;102616- 620
PubMed

Figures

Tables

Table Graphic Jump LocationTable 3. Distribution of Cognition and Achievement Measures by SDB*
Table Graphic Jump LocationTable 4. Distribution of Cognition and Achievement Measures in Preterm Children by SDB*
Table Graphic Jump LocationTable 5. Partial Spearman Correlations Relating Sleep Indices With Measures of Cognition and Achievement for the Analytic Sample*
Table Graphic Jump LocationTable 6. Distribution of Cognition and Achievement Measures by Snoring History*

References

Naegele  BThouvard  VPepin  JL  et al.  Deficits of cognitive executive functions in patients with sleep apnea syndrome Sleep 1995;1843- 52
PubMed
Bedard  MAMontplaisir  JRicher  FRouleau  IMalo  J Obstructive sleep apnea: pathogenesis of neuropsychological deficits J Clin Exp Neuropsychol 1991;13950- 964
PubMed
Adams  NStrauss  MSchluchter  MRedline  S Relation of measures of sleep-disordered breathing to neuropsychological functioning Am J Respir Crit Care Med 2001;1631626- 1631
PubMed
Rosen  CLLarkin  EKKirchner  HL  et al.  Prevalence and risk factors for sleep-disordered breathing in 8- to 11-year-old children: association with race and prematurity J Pediatr 2003;142383- 389
PubMed
Rhodes  SKShimoda  KCWaid  LR  et al.  Neurocognitive deficits in morbidly obese children with obstructive sleep apnea J Pediatr 1995;127741- 744
PubMed
Beebe  DWGroesz  LWells  CNichols  AMcGee  K The neuropsychological effects of obstructive sleep apnea: a meta-analysis of norm-referenced and case-controlled data Sleep 2003;26298- 307
PubMed
Urschitz  MSWolff  JSokollik  C  et al.  Nocturnal arterial oxygen saturation and academic performance in a community sample of children Pediatrics 2005;115e204- e209
PubMed
Gozal  DPope  DW Snoring during early childhood and academic performance at ages thirteen to fourteen years Pediatrics 2001;1071394- 1399
PubMed
Kaemingk  KLPasvogel  AEGoodwin  JL  et al.  Learning in children and sleep disordered breathing: findings of the Tucson Children's Assessment of Sleep Apnea (tuCASA) prospective cohort study J Int Neuropsychol Soc 2003;91016- 1026
PubMed
Gottlieb  DJChase  CVezina  RM  et al.  Sleep-disordered breathing symptoms are associated with poorer cognitive function in 5-year-old children J Pediatr 2004;145458- 464
PubMed
Kump  KWhalen  CTishler  PV  et al.  Assessment of the validity and utility of a sleep-symptom questionnaire Am J Respir Crit Care Med 1994;150735- 741
PubMed
Umberger  FG Peabody Picture Vocabulary Test-Revised  Kansas City, Mo Test Corp America1985;
Merz  WR Kaufman Assessment Battery for Children  Kansas City, Mo Test Corp America1984;
Connors  CK Connor's Continuous Performance Test  North Tonawanda, NY Multi-Health System1995;
Ali  NJPitson  DStradling  JR Sleep disordered breathing: effects of adenotonsillectomy on behaviour and psychological functioning Eur J Pediatr 1996;15556- 62
PubMed
Chervin  RDArchbold  KHDillon  JE  et al.  Inattention, hyperactivity, and symptoms of sleep-disordered breathing Pediatrics 2002;109449- 456
PubMed
Gottlieb  DJVezina  RMChase  C  et al.  Symptoms of sleep-disordered breathing in 5-year-old children are associated with sleepiness and problem behaviors Pediatrics 2003;112870- 877
PubMed
Rosen  CLStorfer-Isser  ATaylor  HGKirchner  HLEmancipator  JLRedline  S Increased behavioral morbidity in school-aged children with sleep-disordered breathing Pediatrics 2004;1141640- 1648
PubMed
Beebe  DWGozal  D Obstructive sleep apnea and the prefrontal cortex: towards a comprehensive model linking nocturnal upper airway obstruction to daytime cognitive and behavioral deficits J Sleep Res 2002;111- 16
PubMed
O’Brien  LMMervis  CBHolbrook  CR  et al.  Neurobehavioral correlates of sleep-disordered breathing in children J Sleep Res 2004;13165- 172
PubMed
Beebe  DWells  CJeffries  JChini  BKalra  MAmin  R Neuropsychological effects of pediatric obstructive sleep apnea J Int Neuropsychol Soc 2004;10962- 975
PubMed
Chervin  RDDillon  JEArchbold  KHRuzicka  DL Conduct problems and symptoms of sleep disorders in children J Am Acad Child Adolesc Psychiatry 2003;42201- 208
PubMed
Kim  HCYoung  TMatthews  CGWeber  SMWoodard  ARPalta  M Sleep-disordered breathing and neuropsychological deficits Am J Respir Crit Care Med 1997;1561813- 1819
PubMed
Gozal  ERow  BWSchurr  AGozal  D Developmental differences in cortical and hippocampal vulnerability to intermittent hypoxia in the rat Neurosci Lett 2001;305197- 201
PubMed
Gozal  DDaniel  JMDohanich  GP Behavioral and anatomical correlates of chronic episodic hypoxia during sleep in the rat J Neurosci 2001;212442- 2450
PubMed
Bedard  MAMontplaisir  JMalo  JRouleau  I Persistent neuropsychological deficits and vigilance impairments in sleep apnea syndrome after treatment with continuous positive airway pressure J Clin Exp Neuropsychol 1993;15330- 341
PubMed
O’Brien  LMMervis  CBHolbrook  CR  et al.  Neurobehavioral implications of habitual snoring in children Pediatrics 2004;11444- 49
PubMed
Bhutta  ATCleves  MACasey  PHCradock  MMAnand  KJ Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis JAMA 2002;288728- 737
PubMed
Taylor  HGMinich  NBangert  BFilipek  PAHack  M Long-term neuropsychological outcomes of very low birth weight: associations with early risks for periventricular brain insults J Int Neuropsychol Soc 2004;10987- 1004
PubMed
Kesler  SRMent  LRVohr  B  et al.  Volumetric analysis of regional cerebral development in preterm children Pediatr Neurol 2004;31318- 325
PubMed
Luciana  M Cognitive development in children born preterm: implications for theories of brain plasticity following early injury Dev Psychopathol 2003;151017- 1047
PubMed
McGauhey  PJStarfield  BAlexander  CEnsminger  ME Social environment and vulnerability of low birth weight children: a social-epidemiological perspective Pediatrics 1991;88943- 953
PubMed
Gozal  D Sleep-disordered breathing and school performance in children Pediatrics 1998;102616- 620
PubMed

Correspondence

CME
Meets CME requirements for:
Browse CME for all U.S. States
Accreditation Information
The American Medical Association is accredited by the Accreditation Council for Continuing Medical Education to provide continuing medical education for physicians. The AMA designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 CreditTM per course. Physicians should claim only the credit commensurate with the extent of their participation in the activity. Physicians who complete the CME course and score at least 80% correct on the quiz are eligible for AMA PRA Category 1 CreditTM.
Note: You must get at least of the answers correct to pass this quiz.
You have not filled in all the answers to complete this quiz
The following questions were not answered:
Sorry, you have unsuccessfully completed this CME quiz with a score of
The following questions were not answered correctly:
Commitment to Change (optional):
Indicate what change(s) you will implement in your practice, if any, based on this CME course.
Your quiz results:
The filled radio buttons indicate your responses. The preferred responses are highlighted
For CME Course: A Proposed Model for Initial Assessment and Management of Acute Heart Failure Syndromes
Indicate what changes(s) you will implement in your practice, if any, based on this CME course.
NOTE:
Citing articles are presented as examples only. In non-demo SCM6 implementation, integration with CrossRef’s "Cited By" API will populate this tab (http://www.crossref.org/citedby.html).
Submit a Comment

Multimedia

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging & repositioning the boxes below.

Articles Related By Topic
Related Topics
PubMed Articles
Obstructive sleep apnea syndrome. Eur J Intern Med 2012;23(7):586-93.
JAMAevidence.com

The Rational Clinical Examination
Assessing Cognition

The Rational Clinical Examination
Relationship Between Cognition and Incapacity