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* Kosair Children’s Hospital Research Institute, and Division of Pediatric Sleep Medicine, Department of Pediatrics
Department of Psychological and Brain Sciences, University of Louisville, Louisville, Kentucky
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONAPPENDIX 1. The Sleep...REFERENCES |
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Methods. Parents of 5- to 7-year-old children in public schools were surveyed about their child’s sleeping habits using a validated questionnaire. The questionnaire also asked whether they believed their child to be hyperactive or have ADHD. Children with reported symptoms of ADHD and control children were randomly selected and invited to the Sleep Medicine Center for an overnight polysomnographic assessment and a battery of neurocognitive tests.
Results. The questionnaire response rate was 47.6% (n = 5728). Frequent and loud snoring was reported for 673 children (11.7%). Similarly, 418 (7.3%) children were reported to have hyperactivity/ADHD, 313 (76.5%) of which were boys. Eighty-three children with parentally reported symptoms of ADHD were invited for full evaluation at the Sleep Medicine Center together with 34 control children. After assessment with the Conners’ Parent Rating Scale, 44 children were designated as having "significant" symptoms of ADHD, 27 as "mild," and 39 designated as "none" (controls). Overnight polysomnography indicated that obstructive sleep apnea was present in 5% of those with significant ADHD symptoms, 26% of those with mild symptoms, and 5% of those with no symptoms. In the cohort, no sleep variable accounted for more than a negligible proportion of the variance in domains of neurobehavioral function.
Conclusions. An unusually high prevalence of snoring was identified among a group of children designated as showing mild symptoms of ADHD based on the Conners’ ADHD index identified from a community sample. However, whereas SDB is not more likely to occur among children with significant ADHD symptoms, it is significantly highly prevalent among children with mild hyperactive behaviors. Sleep studies further revealed that rapid eye movement disturbances are more likely to occur in children with significant symptoms, and they seem to impose significant but mild effects on daytime neurobehavioral functioning. We conclude that in children with significant symptoms of ADHD, the prevalence of SDB is not different from that of the general pediatric population and that rapid eye movement sleep in these children is disturbed and may contribute to the severity of their behavioral manifestations. Furthermore, SDB can lead to mild ADHD-like behaviors that can be readily misperceived and potentially delay the diagnosis and appropriate treatment.
Key Words: snoring • obstructive sleep apnea • periodic leg movement disorder of sleep • ADHD • cognitive function
Abbreviations: ADHD, attention-deficit/hyperactivity disorder • SDB, sleep-disordered breathing • OSA, obstructive sleep apnea • SPO2, oxygen saturation as measured by pulse oximetry • TST, total sleep time • AHI, apnea/hypopnea index • PLM, periodic limb movements • SD, standard deviation • DAS, Differential Ability Scales • OR, odds ratio • REM, rapid eye movement • DSM-IV, Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONAPPENDIX 1. The Sleep...REFERENCES |
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There is increasing evidence that snoring and sleep-disordered breathing (SDB) are associated with behavioral problems, in particular with hyperactivity and ADHD.9–13 Hyperactive and inattentive behavior has been reported in children with obstructive sleep apnea (OSA) syndrome14,15 and habitual snoring,16,17 and it has been further suggested that up to one third of all children with frequent, loud snoring or SDB will display significant hyperactivity and inattention.9 Improvement in the latter hyperactive and inattentive behaviors has been found in children who have undergone adenotonsillectomy for SDB.13 Conversely, children with ADHD seem to exhibit more sleep disturbances than normal children.18 However, most of the studies on sleep and ADHD have relied on parental reports of sleep disturbance, with only a few studies actually performing objective sleep assessments.19–22 The findings of most of the latter studies are difficult to interpret because of methodological problems such as small sample sizes, associated comorbidities, and the lack of adequate controls. Although improvement in behavior has been noted after treatment of SDB, few studies have specifically investigated the relationship between SDB and neurobehavioral function.
To resolve some of these issues, we conducted this study to examine potential relationships between sleep measures and neurobehavioral function in a community cohort of 5- to 7-year-old children with reported symptoms of ADHD. Because we used both questionnaire data and polysomnography, we were in a unique position to compare both subjective and objective information in this group of children. Furthermore, we wished to determine the incidence of snoring and sleep problems in these children and assess the relationship with parental snoring and parental smoking.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONAPPENDIX 1. The Sleep...REFERENCES |
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Subject Selection
Returned questionnaires were scanned into a computerized database using Microsoft Access (Redmond, WA). Questionnaires of children whose parents believed that they were hyperactive (with or without a diagnosis of ADHD) were identified, and the parents were contacted without any preferential order and invited to the Sleep Medicine Center for an overnight polysomnographic assessment and a battery of neurobehavioral tests. Children were considered eligible as controls provided that they had no reports of hyperactivity and either did not snore or snored rarely. These questionnaires were identified, and parents were contacted in the same manner as the other children. Children were not contacted when the questionnaires reported other psychiatric diagnoses, any chronic medical conditions, or genetic or craniofacial syndromes. Children were retrospectively excluded when during the later phases of the study specific questioning would reveal the presence of any exclusionary criteria.
Measures
Polysomnographic Assessment
Parental informed consent and child assent, in the presence of a parent, were obtained. A standard overnight multichannel polysomnographic evaluation was performed at the Sleep Medicine Center of Kosair Children’s Hospital. Children were studied for up to 12 hours in a quiet, darkened room with an ambient temperature of 24°C in the company of 1 of their parents. No drugs were used to induce sleep. There was no adaptation night, and children were requested to be in bed with lights out occurring between 21:00 and 21:30 hours. All studies were terminated when the children woke up for the day or at approximately 7 AM if they were still sleeping, regardless of whether the studies were performed on a school night or a weekend. The following parameters were measured: chest and abdominal wall movement by respiratory impedance or inductance plethysmography; heart rate by electrocardiogram; and air flow by a sidestream end-tidal capnograph, which also provided breath-by-breath assessment of end-tidal carbon dioxide levels (BCI SC-300, Menomonee Falls, WI), and/or a thermistor. Arterial oxygen saturation was assessed by pulse oximetry (SPO2; Nellcor N 100; Nellcor Inc, Hayward, CA), with simultaneous recording of the pulse wave form. The bilateral electro-oculogram, 8 channels of electroencephalogram, chin and anterior tibial electromyograms, and analog output from a body position sensor (Braebon Medical Corporation, Ogdensburg, NY) were also monitored. All measures were digitized using a commercially available polysomnography system (Stellate Systems, Montreal, Canada). Tracheal sound was monitored with a microphone sensor (Sleepmate, Midlothian, VA), and a digital time-synchronized video recording was performed.
Sleep Variables
Sleep architecture was assessed by standard techniques.24 Arousals were defined as recommended by the American Sleep Disorders Association Task Force report25 and include respiratory-related (occurring immediately after an apnea, hypopnea, or snore), technician-induced, and spontaneous arousals. Arousals were expressed as the total number of arousals per hour of sleep time (arousal index). The apnea index was defined as the number of apneas per hour of total sleep time (TST). Hypopneas were defined as a decrease in nasal flow of 
50% with a corresponding decrease in SPO2 of 4% and/or arousal.26 The apnea/hypopnea index (AHI) was defined as the number of apneas and hypopneas per hour of TST. SPO2, together with SPO2 nadir, was determined. The mean and peak end-tidal carbon dioxide tension was determined. Central, obstructive, and mixed apneic events were counted. Obstructive apnea was defined as the absence of airflow with continued chest wall and abdominal movement for a duration of at least 2 breaths.26,27 Periodic limb movements (PLM) during sleep were scored when there were at least 4 movements of 0.5 to 5 seconds duration and between 5 and 90 seconds apart. A PLM index of 5 per hour of sleep is generally considered to be rare in normal children.28 For evaluating the number of children with objectively measured sleep disturbances, the number of children with a sleep efficiency 
70%, PLM index 10, AHI 5, or arousal index 20 was determined. The threshold values for these indices were selected as representing >3 standard deviations (SD) from normative values obtained in a large cohort of normal children and represent well-accepted criteria for the presence of disease.
Neurobehavioral Assessments
A battery of neurobehavioral tests was administered the morning after polysomnographic assessment. These tests comprised the Conners’ Parent Rating Scale,29 the Child Behavior Checklist,30 the Differential Ability Scales,31 and the NEPSY.32 For dividing the children into groups, the ADHD index of the Conners’ Parent Rating Scale was used. Children were classified as having significant ADHD symptoms when their scores were 2 SD above the mean (ie, 70). When scores were between 1 and 2 SD above the mean (ie, 61–69), children were assigned to the "mild" group, and children whose scores were 60 were included in the control group. Children who were reported as having ADHD or hyperactivity by their parents but scored 60 on the Conners’ Parent Rating Scale were included in the control group.
Behavioral Variables
The Conners’ Parent Rating Scale29 is used to identify behavioral problems in children. The 48-item version was used, which yields 7 factors: oppositional, cognitive problems/inattention, hyperactivity, anxious-shy, perfectionism, social problems, and psychosomatic, several summary indices, all with a mean score of 50 and an SD of 10. Although not a diagnostic tool for ADHD, the ADHD index of this rating scale is well validated and a score of 2 SD above the mean provides a recognized measure of children who are at risk for a diagnosis of ADHD.6,33
The Child Behavior Checklist30 is the most well-developed, empirically derived behavior rating scale available for assessing psychopathology and social competence in children.5 This questionnaire yields 8 factors: withdrawn, somatic complaints, anxious/depressed, social problems, thought problems, attention-hyperactive, delinquent behavior, and aggressive behavior with a mean T score of 50 and an SD of 10.
Neurocognitive Variables
The Differential Ability Scales (DAS)31 is a battery of cognitive tests designed to measure reasoning and conceptual ability. Individual DAS subtests are designed to measure separate and distinct areas of cognitive functioning and thus have high specificity. The ability score for a subtest is expressed as a T score with a mean of 50 and an SD of 10. The sum of the core subtest T scores is converted to a total standard score, with a mean of 100 and an SD of 15. The NEPSY,32 which abbreviates the word "NEuroPSYchology," is a relatively new neurobehavioral test battery and was designed to assess neurobiological development in 5 functional domains: attention/executive functions, language, sensorimotor functions, visuospatial processing, and memory and learning with a mean score of 100 and an SD of 15.
Data Analysis
Data are presented as means ± SD unless otherwise indicated. For questionnaire-derived responses, descriptive statistics and odds ratios (ORs) were calculated to assess relationships between snoring in children with snoring and smoking in their parents. Comparisons of the distribution of demographic and risk factors according to group membership (index or control) were made with unpaired t tests (continuous variables) with P values adjusted for unequal variances when appropriate or 
2 analyses (dichotomous outcomes). Analysis of variance was used for comparisons of polysomnographic and neurocognitive variables. Multiple regression and logistic regression were performed to evaluate potential relationships between sleep measures and neurobehavioral scores for the study groups. All P values reported are 2-tailed with statistical significance set at <.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONAPPENDIX 1. The Sleep...REFERENCES |
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When 1 of the parents snored, there was a mild albeit significant increase in the risk for the child to snore (Table 1). However, snoring by both parents did not further increase the risk of snoring by the child. When a parent smoked, an increased risk for snoring by the child was apparent (Table 1). Furthermore, a dose-dependent effect of passive smoking on snoring emerged, particularly if one assumes that children tend to spend more time with their mother during waking hours (Table 1).
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Subjective Sleep Assessment
Subjective sleep disturbances were frequently reported for the children classified as having symptoms of ADHD based on the Conners’ Parent Rating Scale (Table 2). With the use of the questionnaire variables "difficulty initiating sleep," "restless sleep," and "willingness to fall asleep" as an arbitrary measure of sleep disturbance, 77% of children with significant ADHD symptoms, 70% of children with mild ADHD symptoms, and 43% of control children were reported to have sleep disturbances (P = .003 significant versus control; P < .05 mild versus control).
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5) was present in 2 (5%) of 44 of children with significant symptoms, in 7 (26%) of 27 children with mild symptoms, and in 2 (5%) of 39 control children (P < .03 significant versus mild and P < .02 control versus mild). Analysis of variance revealed that rapid eye movement (REM) latency and proportion of REM sleep (%TST) were more likely to be affected in the significant symptoms group (P < .01 for REM latency and REM% for significant versus controls; P < .03 for REM latency and P < .02 for REM% for significant versus mild). The groups were not different for any other objective sleep measure.
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10, and none had any significant associated arousals. Furthermore, only 7 (16%) of those with significant symptoms, 4 (15%) of those with mild symptoms, and 5 (13%) controls had a PLM index of 5.
Nine (20%) of 44 children with significant symptoms had 1 or more of the objective sleep disturbances (sleep efficiency 70%, PLM index 10, AHI 5, or arousal index 20) compared with 13 (48%) of 27 children with mild symptoms and 6 (15%) of 39 control children (P < .03 significant versus mild; P < .01 mild versus controls). No subject in either group had >1 of the above sleep abnormalities.
Neurobehavioral Variables
The results of the neurocognitive test findings are shown in Table 4. As expected, the children with significant ADHD symptoms consistently performed worse on tasks related to language and memory skills, visuospatial tasks, and attention.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONAPPENDIX 1. The Sleep...REFERENCES |
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The overall response rate to the mailed questionnaires was good for a survey of the general population. Because no differences in the responses between those who responded to the initial mailing and those who completed the telephone questionnaires were found, we believe that the findings are valid for the cohort and essentially provides a very large community survey of sleep-associated snoring in a school district of US children. The prevalence of frequent snoring was similar to previous published studies in Europe that included a more restricted number of responders.2–4 It is interesting that we found that snoring by 1 of the parents increased the risk of snoring in the child. Our findings concur with those of Redline et al,34 who evaluated 399 children recruited from either 31 families in which a member was diagnosed with OSA or from 30 families without OSA. Indeed, these investigators found that a family history of OSA increased the risk for OSA in the offspring. However, they did not find increased risk for OSA in the presence of maternal smoking, after adjusting for other significant variables. This is in contrast with current findings, which suggest that the risk of nocturnal snoring is greatly increased not only when children are exposed to passive smoking but also as a function of the cigarette smoke exposure duration and intensity. Furthermore, in previous studies by Corbo et al and Forastiere et al,35,36 an increased risk of snoring in children exposed to passive smoking was indeed identified. Thus, this study has allowed for identification of both genetic and environmental risk factors for snoring during childhood in the United States.
Although we did not perform rigorous assessments for ADHD as stipulated by DSM-IV criteria, we were able to confirm the presence of abnormal levels of hyperactivity using a validated measure and did not solely rely on a positive answer by the parents to the questions, "Does your child have ADHD?" and is, "Is your child hyperactive?" From our initial recruitment, only half of the children whose parents reported hyperactivity behaviors actually fulfilled the score criteria of the Conners’ ADHD index scale.29 These findings further highlight potential biases introduced by the use of parental reports when assessing for behavioral disturbances in epidemiologic surveys. It should be acknowledged, however, that by using the Conners’ scale we were still unable to establish a formal diagnosis of ADHD based on DSM-IV criteria, and that is a limitation of the current study. Our survey also further expands on previous findings by Chervin et al16,17 and Owens et al11 that children with ADHD are at higher risk for snoring and other symptoms suggestive of SDB.
An expanded inquiry into parental perception of sleep quality in hyperactive children revealed that 77% of the children with significant ADHD symptoms were considered to have a significant sleep problem by their parents. These findings confirm multiple earlier studies,10–12 all of which found an increased prevalence of parent-reported sleep disturbances in hyperactive children. However, objective sleep disorders were identified in only 20% of these children in this community cohort, clearly a substantially lower frequency than the frequency derived from parental reports. This is of particular importance, given that the majority of studies reporting sleep disturbances in children with ADHD are based on parental perception rather than on objective assessments. Nevertheless, although children with significant ADHD symptoms are at higher risk for objective REM sleep disturbances compared with normal children, the prevalence of OSA in this cohort does not seem to differ from the prevalence in the general population.9,34,37 However, among children with mild ADHD symptoms, an unusually high frequency of OSA was found. Thus, our findings suggest that although OSA can induce statistically significant yet mild behavioral effects, it does not seem to mimic more severe ADHD symptoms as assessed by the Conners’ Parent Rating Scale. Therefore, in a child who presents with parental complaints of hyperactivity and who does not meet the diagnostic criteria of ADHD after undergoing a thorough evaluation as recently recommended by the American Academy of Pediatrics,33 a careful sleep history should be taken, and if snoring is present, then an overnight polysomnographic evaluation should be performed.
The mechanism(s) by which OSA may contribute to hyperactivity remains unknown. It is possible that both the sleep fragmentation and episodic hypoxia that characterize OSA will lead to alterations in the neurochemical substrate of the prefrontal cortex and resultant executive dysfunction.38 Notwithstanding these considerations, sleep disturbances are frequently reported by parents of children with ADHD even when snoring is excluded.11 On the basis of the available literature, the comorbidity of OSA and ADHD could be shared by a substantial number of hyperactive children, and, in fact, it has been suggested that up to 25% of children with a diagnosis of ADHD may actually have OSA.16 However, our data suggest that children with mild hyperactive behaviors rather than children who are at risk for a diagnosis of ADHD are at higher risk for OSA. In addition, the overlap between ADHD/hyperactivity may be less prominent than previously estimated when medication status and psychiatric comorbidity are accounted for in the multivariate analysis.39
Sleep fragmentation and consequent daytime sleepiness are another possible theoretical explanation for the potential relationships between disturbed sleep and ADHD. Evidence of increased sleepiness, measured by multiple sleep latency tests, was reported by Lecendreux et al40 in 30 children with ADHD who otherwise had no significant polysomnographic alterations. Therefore, these investigators surmised that ADHD may be accompanied by an intrinsic deficit in daytime alertness.
Restless sleep is frequently reported by parents of children with ADHD.20,41 When accompanied by arousals, frequent limb movements could induce sleep fragmentation and daytime sleepiness. PLM disorder of sleep has been described in children with ADHD,42 and treatment of this condition often leads to substantial behavioral improvements.42–45 Chervin et al46 further reported a dose-dependent association between hyperactivity, measured by the Conners’ Parent Rating Scale, and PLM index, a finding that we were unable to replicate in our study (see below). Similarly, Konofal et al47 reported higher levels of nocturnal limb activity in 30 unmedicated children with ADHD when compared with 19 controls. However, no disruption of sleep continuity could be identified, so the implications of such findings remain unclear.
Our findings do not support the concept that PLM during sleep are more frequent in hyperactive children.46 However, our population was taken from a community sample, and not from a highly selected clinical population referred for sleep problems. In the present study, we postulate that PLM disorder may occur in a select group of children with more severe ADHD symptoms and may in fact represent a distinct categorical subset of ADHD.
A reduction in proportion of REM sleep and increased REM latencies were found in our children with significant symptoms of ADHD, based on the Conners’ Parent Rating Scale. The exact implications of these findings are unclear, although both hyperactivity and neurocognitive measures associated with executive function were weakly but significantly correlated with REM sleep disturbance, suggesting that delayed REM onset and/or decreased REM percentage may impose a small but significant adverse effect on daytime functioning. These findings are not surprising when one considers some of the putative functions ascribed to REM sleep. In recent years, it has become apparent that REM sleep may play an important role in memory consolidation of a learned task.48 Memory for declarative or explicit types of tasks seems not to be affected by REM sleep loss, whereas memory and learning of cognitive procedural or implicit types of material such as visuospatial tasks is impaired. Visuospatial functions exhibited negative correlations with REM sleep measures in our cohort, suggesting that potential interventions aiming at improving REM sleep in these children may be accompanied by favorable changes in some of their neurobehavioral functions.
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CONCLUSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONAPPENDIX 1. The Sleep...REFERENCES |
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APPENDIX 1. The Sleep Questionnaire |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONAPPENDIX 1. The Sleep...REFERENCES |
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Name
Address
Telephone number
Date of birth
Gender
Ethnicity
Father’s demographic information
Profession:
Highest level graduated from:
JHS HS COL GRAD
Snore: YES NO
Smoke: YES NO
Adenoids or tonsils removed: YES NO
Mother’s demographic information
Profession:
Highest level graduated from: JHS HS COL GRAD
Snore: YES NO
Smoke: YES NO
Adenoids or tonsils removed: YES NO
Pregnancy: Normal Abnormal
Pregnancy: Full-term Preterm
Child
Medical problems:
Medications:
Allergies:
Birth weight
Adenoids or tonsils removed: YES NO
Vision problems: YES NO
Hearing problems: YES NO
Poor appetite: YES NO
Poor growth: YES NO
Ear infections: YES NO
Asthma: YES NO
Frequent colds/flus: YES NO
Constant runny nose: YES NO
Does child sleep alone, share with 1, share with 2, share with 3, share with >3
Do any of his/her siblings snore? YES NO
Does your child have ADHD (also called hyperkinetic/attention deficit)? YES NO
Is your child hyperactive? YES NO
Is your child on any ADHD medication? YES NO; Which one:
How long does your child sleep at night?
At what time does your child go to bed?
At what time does your child wake up?
The following questions can be answered by "never," "rarely," "occasionally, "frequently," or "almost always":
Have you seen or heard your child having nightmares that he/she does not remember the next day?
Has he/she expressed fear of sleeping in the dark?
Is your child easy to wake up in the morning?
Does your child go to bed willingly?
Is he/she a restless sleeper?
Have you seen your child smiling during sleep?
Does he/she wake up at night?
Have you heard your child talking during his/her sleep?
Have you observed him/her sleepwalking?
While asleep, does he/she ever sit up in bed?
Does he/she grind his/her teeth during sleep?
Have you heard your child laugh during sleep?
Has your child told you about having a frightening dream?
Have you observed repetitive actions such as rocking or head banging during sleep?
Does he/she have problems with bed wetting?
Have you observed your child having a nightmare during which he/she appeared extremely afraid or terrified?
Have you looked in on your child and discovered he/she was crying while asleep?
Has he/she told you about having a pleasant dream?
Does your child complain about difficulties going to sleep?
Does your child get up to go to the bathroom during the night?
Does your child stop breathing during sleep?
Does your child struggle to breathe while asleep?
Does your child fall asleep easily?
Do you ever shake your child to make him/her breathe again when asleep?
Do your child’s lips ever turn blue or purple while asleep?
Are you ever concerned about your child’s breathing during sleep?
How often does your child snore?
How loud is the snore? (the responses to this question are "mildly quiet," "medium loud," "loud," "very loud," and "extremely loud")
How often does your child have a sore throat?
Does your child complain of morning headaches?
Is your child a daytime mouth breather?
Is your child sleepy during the daytime?
Does your child fall asleep at school?
Does your child fall asleep while watching television?
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ACKNOWLEDGMENTS |
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We thank the parents and children for cooperation. We are particularly grateful to Dr Robert J. Rodovsky and Richard Spayd from the Jefferson County Public School System for assistance in this project.
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FOOTNOTES |
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Reprint requests to (D.G.) Kosair Children’s Hospital Research Institute, University of Louisville School of Medicine, 571 S Preston St, Ste 321, Louisville, KY 40202. E-mail: david.gozal{at}louisville.edu
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONCONCLUSIONAPPENDIX 1. The Sleep...REFERENCES |
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