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* Department of Medicine
Psychiatry
Pediatrics
|| Neurology, Boston University School of Medicine, Boston, Massachusetts
¶ Slone Epidemiology Center, Boston University School of Medicine, Boston, Massachusetts
# Department of Biostatistics, Boston University School of Public Health, Boston, Massachusetts
** Department of Pediatrics, Rush University, Chicago, Illinois
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ABSTRACT |
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 TOP ABSTRACT METHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Methods. A population-based, cross-sectional survey was conducted of a birth cohort of children who were born in eastern Massachusetts. Subjects were 3019 5-year-old children (1551 boys, 1468 girls) who were enrolled in the Infant Care Practices Study and whose mothers were contacted within 3 months of their child’s fifth birthday. A parent-completed questionnaire was used to ascertain the presence and intensity of snoring and other SDB symptoms and the presence of daytime sleepiness and problem behaviors. Parent-reported hyperactivity, inattention, and aggressiveness were each assessed by a single question that was validated against the Conners’ Parent Rating Scale. SDB was defined as frequent or loud snoring; trouble breathing or loud, noisy breathing during sleep; or witnessed sleep apnea.
Results. Parent-reported hyperactivity (19%) and inattention (18%) were common, with aggressiveness (12%) and daytime sleepiness (10%) reported somewhat less often. SDB symptoms were present in 744 (25%) children. Compared with children without snoring or other symptoms of SDB, children with SDB symptoms were significantly more likely to have parent-reported daytime sleepiness (odds ratio [OR]: 2.2; 95% confidence interval [CI]: 1.7–2.8) and problem behaviors, including hyperactivity (OR: 2.5; CI: 2.0–3.0), inattention (OR: 2.1; 95% CI: 1.7–2.6), and aggressiveness (OR: 2.1; 95% CI: 1.6–2.6). These associations remained significant after adjustment for sex, race/ethnicity, maternal education level, maternal marital status, household income, and respiratory health history.
Conclusions. SDB symptoms are common in 5-year-old children and are associated with an increased risk of daytime sleepiness and with problem behaviors suggestive of attention-deficit/hyperactivity disorder.
Key Words: snoring • sleep-disordered breathing • sleep apnea • behavior • hyperactivity
Abbreviations: SDB, sleep-disordered breathing • OSA, obstructive sleep apnea • ICPS, Infant Care Practices Study • FYFQ, Five-Year Follow-up Questionnaire • CPRS, Conners’ Parent Rating Scale • DSM-IV, Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition • OR, odds ratio • HI, Hyperactivity Index • PSQ, Pediatric Sleep Questionnaire
There is increasing recognition that obstructive sleep-disordered breathing (SDB), comprising snoring, obstructive sleep apnea/hypopnea, and obstructive hypoventilation, is a common and often unrecognized condition in children.1 Overt obstructive sleep apnea (OSA) has generally been estimated to affect 2% to 3% of children.2–4 Milder forms of SDB are common, however, with 10% to 36% of children age 3 to 6 years reported to snore habitually.2,5,6 Early case series variably identified sleepiness7 and hyperactive, aggressive, or rebellious behaviors8–10 in association with OSA in children, although potential referral bias impedes interpretation of these studies. Few data are available from population-based studies on the behavioral consequences of SDB in children. Although 2 studies from community-based2 or general pediatric clinic11 samples also suggest that SDB is associated with hyperactivity and other problem behaviors, these studies did not control for potentially important confounding factors. Asthma, atopic disorders, and adenotonsillar enlargement, a common correlate of recurrent upper respiratory infection, all have been associated with increased prevalence of SDB symptoms in children.5,10,12,13 As an association of these factors with inattention and hyperactivity has also been reported,14–16 confounding by these respiratory health variables may explain the apparent association of SDB with problem behaviors.
A true causal association of SDB with problem behaviors would be of great importance, however, given the high prevalence of both SDB symptoms and hyperactive or inattentive behaviors, which may have a significant adverse impact on school performance. Treatment of overt OSA in poorly performing first-grade students may improve subsequent academic performance.17 If milder forms of SDB are also associated with sleepiness and problem behaviors, then the identification and treatment of SDB in children before entry into elementary school may be of particular clinical and social benefit. In the present study, we extended the results of previous studies by assessing the relation of parent-reported sleepiness, hyperactivity, inattention, and aggressiveness to snoring and other symptoms of SDB in a large, population-based cohort of 5-year-old children, adjusting for a variety of sociodemographic and respiratory health variables.
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METHODS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Questionnaire Data
Descriptive data (eg, maternal age, race, ethnicity, educational status) were collected by interview at the time of enrollment into the ICPS. The FYFQ asked the child’s height, weight, frequency of upper respiratory and ear infections, history of tympanostomy and adenotonsillectomy and about the presence of SDB symptoms, daytime sleepiness, wheezing, asthma, respiratory allergy, and problem behaviors. Five questions were used to assess the presence of SDB: "On average, how often does your child snore?" "How loud is your child’s snoring?" "When sleeping, does your child have trouble breathing, or struggle to breathe?" "Have you ever seen your child stop breathing when he/she was asleep?" "When sleeping, does your child have ‘‘heavy,’ loud, or noisy breathing?" Three questions were used to identify the presence of problem behaviors. Hyperactivity was defined as a positive response to the question, "Would you say that your child is often restless, overly active, or someone who can’t sit still?" Inattention was defined as a positive response to the question, "Would you say that your child often seems not to listen when spoken to directly?" Aggressiveness was defined as a positive response to the question, "Does your child tend to be more aggressive or rebellious than other children his/her age?" A single question was used to assess sleepiness, with excessive sleepiness defined as a response of 1 or more days per week to the question, "Is your child overly sleepy during the daytime?" The Conners’ Parent Rating Scale, Revised (CPRS)19 was also completed for a subset of 219 children, 131 who were participants in an ongoing laboratory-based study of pediatric sleep apnea and 88 who were mailed the CPRS after declining to participate in the laboratory-based protocol. These data were used to validate the FYFQ questions regarding problem behaviors.
Analysis
All analyses were performed using SPSS software (SPSS, Inc, Chicago, IL). Descriptive statistics of the subject characteristics are presented. The FYFQ items regarding hyperactivity, inattention, and aggressiveness were validated against the CPRS using the Mann-Whitney U test to compare scores on the relevant CPRS scales and Fisher exact test to compare the percentage with scores 
65, between subjects with positive versus negative responses on each screening question. Bivariate and multivariate logistic regression analyses were used to assess the relation of SDB symptoms to daytime sleepiness and problem behaviors. The multivariate models adjusted for potential confounders including sociodemographic variables (sex, race/ethnicity, maternal education level, marital status, and household income) and respiratory illness history (frequency of upper respiratory and ear infections, tympanostomy tube placement or adenotonsillectomy, diagnosis of asthma, wheezing in the past 12 months, or respiratory allergy). The primary analyses included all subjects, and additional sex-specific analyses were conducted.
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RESULTS |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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.001 for each comparison; for aggressiveness screening question, P < .025 for each comparison). Detailed comparisons for the 3 DSM-IV ADHD indices are shown in Table 2. In contrast, scores on the Anxious-Shy, Perfectionism, Social Problems, Psychosomatic, and Emotional Lability scales did not differ significantly between children with positive versus negative responses to any of the 3 FYFQ problem behavior questions. Children with positive responses to the hyperactivity, inattention, or aggressiveness questions on the FYFQ were also much more likely to have abnormally high scores, defined as a t score 65, on the DSM-IV Inattentive, Hyperactive-Impulsive, and Total indices than were children with negative responses to the screening questions (Table 2).
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3 nights/wk, "loud" or "very loud" snoring, loud or noisy breathing during sleep, witnessed apneas, or trouble breathing during sleep 1 or more nights per week.
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Although the prevalence of SDB symptoms in nonrespondents cannot be determined, we explored the potential impact of nonrespondents on the observed prevalence of SDB symptoms by comparing symptom prevalence between those who responded to the mailed questionnaire (56% of respondents) and those who responded only after telephone contact (44% of respondents). For each of the 5 symptoms of SDB, the prevalence was slightly higher in the latter group: 13% versus 11% with frequent snoring; 19% versus 15% with loud, noisy breathing during sleep; and 28% versus 22% with any of the 5 SDB symptoms.
Prevalence of Sleepiness and Problem Behaviors
Daytime sleepiness was reported to occur at least occasionally in 38% of children, but excessive daytime sleepiness, defined as sleepiness occurring at least once per week, was reported in only 10% of children (Table 4). Hyperactivity was reported in 19% of children and inattention in 18%. Although the presence of hyperactivity and inattention was strongly associated (OR: 9.9; P < .001), of the 805 children with a positive response to either of these questions, only 292 (36%) had a positive response to both questions. Only 12% of children were reported to be more aggressive or rebellious than other children their age. Although the prevalence of daytime sleepiness did not differ significantly between boys and girls, hyperactivity, inattention, and aggressiveness were reported 25% to 55% more often in boys than in girls (Table 4).
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2 analysis for each comparison; Table 5). A similar trend was observed for witnessed apneas, although perhaps as a result of the low frequency of this symptom, the association was significant only for hyperactivity (P < .001). A dose-response effect on sleepiness and problem behaviors was observed for both snoring frequency and snoring loudness. Multivariate logistic regression analyses were conducted to assess the association of SDB symptoms with sleepiness and problem behaviors and to adjust for potential confounders including sociodemographic variables and respiratory illness history. SDB was strongly associated with each behavioral measure, with unadjusted ORs >2.0 for the association of the composite SDB variable with each behavior (Table 6). After adjustment for sociodemographic variables, the ORs were only trivially reduced from their unadjusted values, suggesting little confounding by these variables. There was an additional slight reduction in the ORs after adjustment for respiratory health variables (Table 6). When separate models were constructed for boys and girls, the association of SDB symptoms with behavioral measures was similar across the sexes (excessive daytime sleepiness, adjusted ORs 1.8 and 2.4 for boys and girls, respectively; hyperactivity, 2.3 and 1.4; inattention, 1.7 and 1.9; aggressiveness, 1.8 and 1.8). Although the association of SDB symptoms with hyperactivity was somewhat stronger in boys, a sex-SDB interaction term entered in the logistic regression model was not statistically significant (P = .07). The association of SDB symptoms with problem behaviors was also assessed excluding occasionally snoring children from the referent group. When compared with children who were reported never to snore, those with SDB symptoms had unadjusted ORs for sleepiness, hyperactivity, inattention, and aggressiveness that were 2.4, 3.2, 2.4, and 2.2, respectively, falling slightly with adjustment for sociodemographic and respiratory health variables to 2.2, 2.3, 2.0, and 1.9.
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DISCUSSION |
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TOPABSTRACTMETHODSRESULTSDISCUSSIONCONCLUSIONSREFERENCES |
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Several previous studies have assessed the relation of parent-reported SDB symptoms to behavior problems. Weissbluth et al20 used a questionnaire survey of 2076 children to identify 71 with behavioral or academic problems. Compared with a control group without such problems, these children had significantly more reported snoring and difficulty breathing at night, an association that was strongest for children with academic problems or symptoms of attention-deficit/hyperactivity disorder. In a questionnaire survey of the parents of 782 children aged 4 to 5 years, Ali et al2 found that the unadjusted prevalence of daytime sleepiness and hyperactivity increased with frequency of snoring. The Conners’ Child Behavior Scale was completed by the parents of a subgroup of 34 children with symptoms most suggestive of OSA and 52 low-risk control subjects. After adjustment for age and social class, median scores on the Hyperactivity, Inattention, and Aggression scales were at least twice as high in the high-risk group as in the low-risk group, although there was a substantially lower participation rate among high-risk (51%) versus low-risk (78%) children, raising concern of recruitment bias.2 Recently, Chervin et al11 evaluated 866 children who were aged 2 to 14 years and recruited from general pediatrics clinics using a sleep symptom questionnaire and the Hyperactivity Index (HI) of the CPRS. A t score >60 on the HI was seen in 22% of habitually snoring children but in only 12% of nonsnoring children, with an OR for elevated HI score of 2.2 after adjustment for age and sex. In that study, the association of snoring with elevated HI was seen primarily in boys younger than 8 years.
Both child behavior and the presence of SDB may be influenced by a variety of social and health factors, raising concern that the observed association of SDB symptoms with problem behaviors could reflect confounding by such factors. The present study has the advantage of a considerably larger sample size and more detailed covariate data than previous studies. We were particularly concerned that asthma and respiratory allergies, previously identified as risk factors for SDB in children,5,13 or frequent respiratory infections, which might cause SDB through adenotonsillar enlargement, could also have an adverse impact on child behavior. Indeed, we observed significant associations of both SDB symptoms and problem behaviors with all sociodemographic and respiratory health variables included in the multivariate analyses, including sex, race/ethnicity, household income, maternal education level and marital status, frequency of upper respiratory and ear infections, a diagnosis of asthma, the presence of wheezing and respiratory allergies, and history of tympanostomy or adenotonsillectomy. The persistence of the association of SDB symptoms with problem behaviors after adjustment for these sociodemographic and respiratory health variables, however, indicates that confounding by these factors does not explain the observed association.
The magnitude of the association of SDB symptoms with hyperactivity in this study is similar to that reported by Chervin et al11 for the association of habitual snoring with elevated HI. Although we also observed a somewhat stronger association in boys than in girls (adjusted OR: 2.3 vs 1.4), the effect in girls remained of borderline statistical significance, and the difference in OR between boys and girls was not statistically significant (P = .07). Whether this reflects true modification by sex of the effect of SDB on symptoms of hyperactivity is uncertain, although the consistency across studies and the known higher prevalence of hyperactive behavior in boys are consistent with this interpretation. However, we observed no such effect of sex on the association of SDB symptoms with parent-reported inattention or aggressiveness, despite the higher prevalence of these behaviors in boys. Sleepiness is a cardinal feature of OSA syndrome in adults and is associated with snoring independent of the presence of OSA.21,22 Although sleepiness is generally considered a less common manifestation of OSA in children,1 we found that children with SDB symptoms were twice as likely as those without to have parent-reported daytime sleepiness, an association somewhat stronger than that reported by Ali et al2 for habitual snoring.
In the present study, we relied on parental report of sleepiness and problem behaviors. Although we did not use standardized measures of behavior, the construct validity of our questionnaire items was tested against the CPRS, a widely used standardized instrument for assessment of child behavior. Each of our behavior questions was found to be strongly associated with standardized measures of inattention and hyperactivity obtained from the CPRS. In contrast, our screening questions were not associated with other CPRS scales that were not expected to reflect inattention or hyperactivity, eg, Perfectionism, Social Problems, Psychosomatic, and Emotional Lability. Thus, the screening questions seem to be valid measures of the behavioral domains of interest. Furthermore, the specificity of the questions for hyperactive or inattentive behavior suggests that the association was not attributable to response bias, in which certain parents are likely to endorse a high level of abnormality for any symptom. This also increases our confidence that response bias is not the cause of the observed association of problem behaviors with SDB symptoms in the main analysis. Although the parental report of daytime sleepiness was not similarly validated, the question that we used to assess daytime sleepiness, "Is your child overly sleepy during the daytime?" is similar to the question, "Does your child have a problem with sleepiness during the day?" which is included in the Pediatric Sleep Questionnaire (PSQ) developed by Chervin et al.23 Factor analysis revealed that question to be 1 of only 2 items in the PSQ loading on the factor "sleepiness."23
Our diagnostic criteria for SDB similarly used parental report of symptoms consistent with obstructive breathing during sleep. For our primary analysis, we used an a priori composite SDB variable that incorporated 5 questionnaire items regarding snoring frequency and loudness, the presence of loud or noisy breathing during sleep, witnessed nocturnal apneas, or trouble breathing during sleep. Although this questionnaire has not been validated in relation to objective measures of SDB, the questions are similar to those used in previously validated questionnaires. Responses of "frequent" or "constant" to questions of whether their child snored, had difficulty breathing during sleep, or stopped breathing during sleep were the 3 items that best discriminated children with OSA from age- and sex-matched control subjects drawn from general pediatric clinics on the questionnaire developed by Brouillette et al.7 All 5 sleep symptom questions in the FYFQ are very similar to questions in Chervin’s PSQ that weight on the factor "breathing," and all were retained in the questionnaire as independent predictors of the presence of polysomnographically defined SBD.23
Studies from France,5 England,2 and Italy6 provide data on snoring frequency of children whose ages were within the range of 3 to 6 years. Although these studies did not use a uniform questionnaire instrument, snoring "often" or "most nights" was reported in 10% to 12% of the French and English children, strikingly similar to our own 12% prevalence of snoring 3 nights/wk.2,5 An additional 26% of the English children were reported to snore often apart from colds, whereas 36% of the Italian children were reported to have frequent or habitual snoring.2,6 Although snoring frequency is the symptom most often used to identify children with SDB, the report of snoring is likely to be dependent on multiple factors influencing the perception of SDB symptoms. Our data, for example, suggest cultural differences in the way sleep-related respiratory noise is labeled: among children with SDB symptoms, non-Hispanic white parents were less likely to report that their children snore and more likely to report loud, noisy breathing during sleep than were black, Hispanic, or Asian parents.
Moreover, reliance on snoring frequency alone fails to identify a large proportion of children with SDB symptoms. In the present study, only half of children who were identified as having SDB symptoms using our composite measure were reported to snore 3 nights per week, yet each of the 5 SDB symptoms showed a strong association with problem behaviors (Table 5). Thus, although the 25% prevalence of SDB symptoms in the present study seems high, it is probably a more accurate representation of the prevalence of potentially important SDB symptoms than is the commonly cited 10% to 12% prevalence of habitual snoring. Although snoring frequency alone identified only half of the children with SDB symptoms in the present study, 91% of children with SDB symptoms could be identified by 2 of these items: the presence of snoring 3 nights/wk or the presence of loud, noisy breathing during sleep.
It is generally accepted that the adverse consequences of SDB are attributable to the effects of OSA, leading to the recommendation that children with symptoms of SDB undergo polysomnography to distinguish OSA from primary snoring (ie, snoring without OSA) to determine the need for therapeutic intervention.1,24,25 In a group of first-grade children with OSA and poor school performance, adenotonsillectomy did lead to improvement in school performance.17 It is unlikely, however, that the strong association of SDB symptoms with sleepiness and problem behaviors identified in this or previous epidemiologic studies is driven by the estimated 2% of children with overt OSA. Indeed, when standardized tests of inattention and hyperactivity were administered to small groups of children who underwent tonsillectomy for OSA or primary snoring, both groups had higher scores than a control group, and both groups showed improvement 3 to 6 months postoperatively, whereas the control group had no reduction in inattention or hyperactivity scores.26 The magnitude of improvement in the primary snoring group was approximately half that of the overt OSA group. It has recently been reported that in children, there is little night-to-night variability in polysomnography and that among 30 children who were studied on 2 separate nights there was no difference between nights in the classification of children as having OSA versus primary snoring.27 It therefore is likely that SDB symptoms are associated with problem behaviors independent of the presence of overt OSA.
Although the ICPS cohort was recruited as a population-based birth cohort, the children in the study sample are more likely to be non-Hispanic white from families with higher income and educational level than either the general population or the total ICPS cohort. This may reflect a more frequent change of residence among those with lower income and educational level, increasing their likelihood of loss to follow-up. Although this may limit generalizability of the study and may have led to a lower prevalence of SDB symptoms in the study sample than in the source population, it should not have an impact on the internal validity of the study. Moreover, the number of minority subjects included in this study approaches the total sample size of previous studies of this topic, and race and ethnicity did not confound the observed associations. The narrow age range of the children, all within several months of their fifth birthday, is both a strength and a limitation of this study. As the manifestations of SDB vary with age, the findings may not apply to children of other ages. Conversely, restriction to a narrow age range improves the ability to identify the behavioral effects at that age. Although the identification of hyperactivity and inattention may be imprecise in 5-year-olds, for whom a short attention span may be considered normal, this makes the observed association even more striking.
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CONCLUSIONS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Reprint requests to (D.J.G.) Pulmonary Center, Boston University School of Medicine, 715 Albany St, R-304, Boston, MA 02118-2394. E-mail: dgottlieb{at}lung.bumc.bu.edu
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REFERENCES |
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