Published online September 1, 2006
PEDIATRICS Vol. 118 No. 3 September 2006, pp. e741-e746 (doi:10.1542/peds.2005-3046)
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ARTICLE

Chronic Snoring and Sleep in Children: A Demonstration of Sleep Disruption

M. Cecilia Lopes, MD and Christian Guilleminault, MD, BiolD

Stanford University Sleep Medicine Program, Stanford, California


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
OBJECTIVE. Chronic snoring that does not adhere to the criteria for a diagnosis of obstructive sleep apnea syndrome may be associated with learning and behavioral problems. We investigated the sleep structure of chronic snorers who had an apnea-hypopnea index of <1 event per hour and analyzed the cyclic alternating pattern.

METHODS. Fifteen successively seen chronic snorers (9.8 ± 4 years) with an apnea-hypopnea index of <1 and 15 aged-matched control subjects (10.3 ± 5 years) underwent an investigation of their sleep with the determination of non–apneic-hypopneic breathing abnormalities polysomnographic scoring using current criteria and analysis of the cyclic alternating pattern.

RESULTS. Chronic snorers have evidence of flow limitations and tachypnea during sleep even if they do not present with apneas, hypopneas, and decrease in oxygen saturations. They also present with abnormal cyclic alternating pattern rates and changes in phase A of cyclic alternating pattern compared with control subjects.

CONCLUSIONS. An apnea-hypopnea index value cannot be the sole determinant in evaluating sleep-disordered breathing in children. Children who have chronic snoring and do not respond to the criteria for obstructive sleep apnea syndrome can present with an abnormal sleep electroencephalogram as evidenced by a significant increase in cyclic alternating pattern rates, with a predominance of abnormalities in slow wave sleep.

Key Words: chronic snoring • cyclic-alternating-pattern • polysomnography • flow limitation • abnormal NREM sleep

Abbreviations: SDB—sleep-disordered breathing • EEG—electroencephalogram • CAP—cyclic alternating pattern • NREM—non–rapid eye movement • OSA—obstructive sleep apnea • REM—rapid eye movement • TST—total sleep time • SaO2—arterial oxygen saturation • AHI—apnea-hypopnea index • RDI—respiratory disturbance index • OSAS—obstructive sleep apnea syndrome

Because of the diversity and the ambiguity in its presentation of symptoms, sleep-disordered breathing (SDB) in children still is an ignored entity in clinical practice. Children, therefore, are often referred to specialty clinics on the basis of the prominent parental complaints: sleepwalkers are evaluated by neurologists, children with attention deficit and hyperactivity are evaluated by psychiatrists, and heavy snorers are evaluated by otorhinolaryngologists. On the basis of these clinicians' findings, some children thereafter will be sent to sleep clinics for evaluation of the sleep-related complaint. One of the reasons that SDB is not diagnosed in prepubertal children and teenagers may be that other behavioral symptoms and signs, besides obvious daytime sleepiness, often are the primary complaints. Another reason for the delay in the diagnosis and treatment of SDB may be that abnormal breathing patterns are not necessarily conspicuous when a polysomnography is performed. Sleep apneas may be more visually recognizable, but the "sleep hypopneas," depending on the definition used, may be a challenge to identify when the definition of such is not predicated solely on the degree of oxygen desaturation. Instead, SDB may encompass other parameters, such as a change in the nasal flow curve, termed a "flow limitation," or a recognition of abnormal breathing effort, namely the "esophageal pressure crescendo" (Pes crescendo), or "esophageal pressure continuous abnormal effort"1,2, that involve the use of specific sensors, such as a nasal cannula–pressure transducer or an esophageal catheter with a pressure transducer.1,3,4

Because of these difficulties, some have preferred to look at "chronic snoring" as an abnormal breathing pattern without trying to elucidate further the mechanisms that are inherent in the breathing per se. The associated changes in the sleep electroencephalogram (EEG) with these abnormal breathing patterns also may be difficult to recognize visually because, for example, an abnormal breath may not terminate with a clear visual EEG arousal.5 The diurnal and nocturnal behavioral changes strongly suggest that disruption of the normal sleep process is an important element in the impairment of healthy children. In performing a computerized analysis on the basis of a new algorithm, Chervin et al6,7 investigated the abnormalities of sleep that are associated with SDB and reported the presence of more significant sleep disruption than previously was thought. The cyclic alternating pattern (CAP)8–11 is a visual scoring pattern that allows for an analysis of the EEG in non–rapid eye movement (NREM) sleep as opposed to the usual sleep staging method and the recognition of the American Sleep Disorders Association's guidelines for EEG arousals (≥3 seconds).12 Normative data on small groups of children of various ages have been published.8–10 This report delineates the analysis of sleep and breathing that is performed in children with daytime behavioral symptoms and marked nocturnal snoring in the absence of obstructive sleep apnea (OSA) during polysomnography.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Criteria for Inclusion
Children who were involved in the study were between 6 and 17 years of age and had confirmed history of the presence of nocturnal snoring, and their parents signed an informed consent for the study approved by the Institutional Review Board. These children were seen for a panoply of complaints: chronic sleepwalking; disrupted nocturnal sleep; symptoms of tiredness; difficulty in arising in the morning; phase delay schedules; behavioral symptoms that consisted of daytime chronic irritability with, at times, inappropriate aggressiveness; and difficulties in school that stemmed from inattention, hyperactivity, and/or poor school performances. To be included in the analysis, the children must have undergone a nocturnal polysomnogram that revealed an absence of OSA and an oxygen desaturation <92%.

The criteria for exclusion were the presence of a psychiatric, neurologic, or medical disorder; intake of medication on a long-term basis or for the past 15 days, excepting oral contraceptives; and presence of an acute illness, menses, or pregnancy. All prospectively seen children who met the above criteria during a 4-month period were included in this study.

Control subjects, who were matched for age (±1 year compared with index case patients) and gender, were recruited from the community and were asked to undergo similar clinical evaluations as the symptomatic children and obtain polysomnographies. Criteria to be recruited as a control subject were response to a request placed in university and local newspapers; absence of complaints, whether these be sleep related (eg, snoring) or not; absence of chronic or acute health problems, including seasonal allergies and chronic orthodontic treatment; and absence of drug intake excepting oral contraceptives. Similar to the symptomatic children, an evaluation also could not be performed at the time of menses, except during a 15-day window that started 3 days after the termination of menstruation, if present. The subjects and parents had to sign consents, the former being recruited to serve as control subjects for various research protocols. Only the polysomnographies of the matching subjects were submitted to the specific analyses presented here. Subjects received a form of compensation for their overall participation, more often gift certificates than a direct monetary compensation.

Evaluation
All subjects who had parental help were asked to complete the pediatric sleep questionnaire and 1 week of sleep diaries, indicating the time in and out of bed, nocturnal sleep events, daytime naps, time of food intake, physical activity, and the presence of health problems or complaints.

Reports of health problems were obtained from the subjects' pediatricians and, each individual had a clinical evaluation that involved clinical evaluation with a child neurologist; psychiatrist; ear, nose, and throat specialist; and orthodontic specialist. Various data and features were calculated and analyzed: BMI, craniofacial features, tonsil size scales, Mallampatti scores,13,14 nasal external valves via digital photographs, size of inferior nasal turbinates (rated on a 3-point subjective scale by the same evaluator), narrowness of the hard palate and mandible, overjet (calculated in millimeters), and an orthodontic class. All subjects had polysomnographies that adhered to the same protocols.

The time in bed and lights out was based on sleep logs that were obtained before testing. All subjects had been in the sleep laboratory before testing and were aware of the polysomnographic routine. Subjects were asked to arrive at the sleep laboratory at 6:30 PM. On the night of the test and the next morning, the subjects also completed questionnaires that evaluated their daytime activities and the perception of their nocturnal sleep the next morning.15

On the selected night, the following variables were monitored for analyses: EEG, C3/A2, C4/A1, Fp1/A2, O1/A2, 2 electro-occulograms, chin and leg electromyelogram, electrocardiogram, a modified V2 lead, and position sensor. Respiration was monitored with nasal cannula pressure transducer, mouth thermistor, uncalibrated respiratory plethysmography, thoracic and abdominal bands, pulse oximeter, and neck microphone. Continuous video monitoring was used with the nocturnal polysonogram. One parent also slept on the premises during the recording.

Data Analysis
Sleep stages were scored using the international criteria.16 The analyzed sleep parameters were sleep-onset latency, defined as 3 consecutive epochs of stage 1; total sleep time (TST); sleep efficiency (TST/total recording time); NREM and REM sleep stages and percentages of TST; and short EEG arousals, adhering to the American Sleep Disorders Association arousal definition17,18 (an abrupt EEG shift toward fast activity, such as 8–13 Hz [{alpha}] or >16 Hz [ß]). In REM sleep, an increase in the amplitude of the submental electromyelogram was designated to score an arousal event. A minimum interval of 10 seconds of continuous sleep was needed to score each event, an arousal index being derived from these tabulations. Wake after sleep onset was scored with the inclusion of short EEG arousals.

The CAP was scored following the guidelines set forth by the international atlas.7 CAP parameters were detected visually according to the CAP Consensus Report,7 CAP cycles were defined as the sum of A and B phases, and a CAP sequence consisted of at least 2 consecutive CAP cycles. CAP phase A is defined as periodic EEG activity during NREM sleep and considered an activation phase, lasting 2 to 60 seconds; it includes high-voltage slow waves (synchronization) or low-voltage fast waves (desynchronization). CAP phase B is the interval between 2 phases A, 2 to 60 seconds in duration, corresponding to the stage-related background activity. The CAP parameters that were studied in NREM sleep were CAP rate (time occupied by CAP sequences over total NREM sleep, expressed in percentages), CAP time (the number and the duration of CAP cycles), CAP phase A events, CAP phase B events, the number of cycles per CAP sequence, and the duration of CAP sequences in seconds. Phase A has been divided into 3 subtypes: A1 with a predominance of synchronized EEG activity and <20% of desynchronization, such as {delta} bursts, K complex sequences, vertex waves, and polyphasic bursts (of slow and fast rhythms); A2, scored in the presence of 20% to 50% of desynchronized EEG activity, with predominance of polyphasic bursts; and A3, in which at least 50% of the EEG activity is composed of low-amplitude fast rhythms, such as K-{alpha} complexes, American Academy of Sleep Medicine arousals,17 and polyphasic bursts. The number of each phase A subtype was calculated to obtain the percentages of phase A1, A2, or A3 per hour of NREM sleep.

The respiratory parameters were defined according to American Academy of Sleep Medicine.19 Hypopneas were defined as a 30% reduction in nasal airflow compared with a previous normal breathing pattern for a duration of 10 seconds or more and a drop of arterial oxygen saturation (SaO2) >3% or an EEG arousal. Apneas were defined as a cessation of airflow for at least 10 seconds; the apnea-hypopnea index (AHI; number of apneas and hypopneas per hour of sleep) is calculated from these 2 values. The respiratory event–related arousals and the presence of "flow limitations" also were identified. A flow limitation was defined as a decrease in nasal flow to <30% of the previous normal nasal cannula curve. Tachypnea was defined as a switch to a respiratory rate ≥20 breaths/min during one 30-second epoch of sleep, this being scored along with the presence of snoring as indicated by a microphone. The number of epochs that revealed these 2 parameters of tachypnea and snoring was obtained. The nonapneic and nonhypopneic events (number of events with only flow limitations) were counted toward the calculation of the respiratory disturbance index (RDI) according to Guilleminault et al.20 The RDI included the AHI with the addition of these breathing events. OSA syndrome (OSAS) was defined when clinical symptoms were associated with an AHI >1 event per hour of sleep. When the AHI was <1, SaO2 was >92%, and clinical symptoms were present with the presence of an RDI ≥1.5/hour, we considered that patients had a SDB and not OSAS.

Statistical Analysis
Central tendency measures were expressed as mean ± SD. The Mann-Whitney U test for independent samples was used to assess gender differences between SDB and control groups, with a significance level of P < .05. One-way analysis of variance, followed by the Tukey test with Bonferroni adjustment, was used to describe the differences between CAP parameters during NREM sleep stages, and 2-way analysis of variance, followed by the Tukey test, was used to detect gender differences between CAP parameters during NREM sleep stages. Correlations between sleep architecture parameters and CAP events, as well as between arousals and phase A subtypes of CAP, were evaluated by Spearman's correlation coefficient (rS). The level of significance for the variance analyses and correlation tests was set at P ≤ .01. All statistical analysis recommendations were conducted using SPSS statistical package version 11.5 (SPSS, Inc, Chicago, IL).


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
There were 10 boys and 5 girls in the study (mean age: 9.8 ± 4 years; range: 6–16 years). All were of normal weight with a BMI between 14 and 19 kg/m2.21 Data with regard to parental complaints are presented in Table 1. Half of the sample had parents who reported that their children had school difficulties, and 11 of the 15 reported sleep-related problems. The control group had 9 boys and 6 girls (mean age: 10.3 ± 5 years; range: 6 to 16 year; nonsignificant). The AHI was 0.6 ± 0.3, the RDI was 1.1 ± 0.5, and none was a chronic snorer (1 child had intermittent snoring as evidenced by the polysomnogram).


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  		TABLE 1 Complaints Associated With Chronic Snoring

 
The clinical evaluation of patients was abnormal only when otorhinolaryngologic and orthodontic findings were tabulated. Table 2 presents the results of abnormal scores for the patients and control subjects. As can be seen, a large proportion had abnormally enlarged turbinates. There was a combination of associated changes in both the soft tissues and the facial, skeletal framework. Six patients had both enlarged tonsils and enlarged turbinates, and 5 patients had enlarged tonsils13 and turbinates as well as a deviated septum; 7 patients had Mallampatti scales scores >214 and a narrow, high-arched, hard palate; 4 patients had a retropositioning of their mandibles and an overjet >3 mm. The group, composed of 7 patients with a long face and an elongated lower one third of the anterior face, included those with enlarged turbinates and 3 patients with a Mallampatti scale score >2. Control subjects, as seen in Table 2, rarely had abnormal features, excepting 1 subject with a deviated septum and enlarged inferior turbinates.


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  		TABLE 2 Anatomic Findings Involving the Upper Airway

 
All patients were snorers, but, per definition, did not show the polysomnographic criteria for OSAS. They presented with an apnea index of 0, AHI <1 (0.7 ± 0.2), but a mean RDI of 7.2 ± 1.2/hour with the mean lowest SaO2 of hemoglobin of 96.1 ± 2.4%. The RDI was based on the presence of several successive minutes of snoring (sometimes lasting 45–60 minutes during the night) and the presence of a change of the flow curve at the nasal cannula pressure transducer, defined as a flattening of the curve, but never a drop in the amplitude of the curve by >5% of the amplitude obtained in the same stage without snoring and never adhering to the criteria in defining a hypopnea. In the control group, the AHI was 0.6 ± 0.3, the RDI was 1.1 ± 0.5 (P = .01 compared with snorers), and none was noted to snore during the recordings.

Sleep Parameters
TST was not significantly longer in normal control subjects, but, if there were a slight increase in the total number of arousals in the SDB patients, then this was far from significant (n = 40 vs 44). Wake after sleep onset was very similar in both groups, as was sleep using the usual sleep analysis criteria (Table 3).


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  		TABLE 3 Sleep Parameters

 
CAP Analysis
Patients presented with a significant increase in the CAP rate compared with control subjects (65.2% ± 6.6% vs 52.8% ± 8.6%; P < .01) and a significant increase in CAP during slow wave sleep (94.3% ± 1.6% vs 83.4% ± 2.6%; P < .01). The phase A2s also were increased in the patient group (P < .01), and the phase A1s were decreased, the latter not being statistically significant (P > .01). The differences between genders were not significant, but the group sizes were small (Table 4).


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  		TABLE 4 CAP Parameters in NREM Sleep

 
No direct correlation was found between the presence of CAP phases A1, A2, and A3 and the termination of flow limitation, but the presence of more frequent CAP, particularly with A2 and A3 phases, was seen in NREM sleep in epochs with snoring. When behavioral complaints were grouped (school difficulties, hyperactivity, inattention, aggressiveness, and irritability), a positive correlation (Spearman correlation coefficient) was found with an increase in the CAP rate (rS = 0.82; P < .01).


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
None of our patients would be considered as having OSA by the current scoring standards, even when the new criteria of the International Classification of Sleep Disorders22 for OSA determination in children is applied. It was reported previously that snoring can be associated with impairments in school performance23–26 and parasomnias, such as chronic sleepwalking in children.27,28 It also was shown that adenotonsillectomy may improve the childrens' behavioral complaints.27 In our current study, the polysomnographies reveal the presence of an abnormal sleep structure when using the CAP scoring system, suggesting significant NREM sleep disruption. There is a trend toward shorter TSTs but otherwise no significant differences in the sleep scoring as already reported.29 Using a computerized analysis and a sophisticated algorithm, Chervin et al7 showed that a change in the sleep EEG of children can be detected each time that an increased respiratory effort occurs during hypopnea and apnea, the changes that are markedly evident before the visual detection of an EEG arousal. Our findings are compatible with those of the mentioned study. The definition of hypopnea is arbitrary because it requires a change in oxygen saturation or a visual EEG arousal for it to be recognized as such. Our study suggests that what we define as nonapneic and nonhypopneic respiratory events, seen in association with snoring, are associated with clinical complaints and abnormal NREM sleep patterns. It also shows that the amount of disruption is not negligible and occurs during the different NREM sleep periods. The analysis of CAP is reliant on NREM sleep, and we cannot make any statements as far as REM sleep is concerned. In the latter, we are obligated to use the traditional scoring analysis, which did not reveal an increase in short EEG arousals compared with control subjects. The patients in this study presented anatomically different from the control subjects: they exhibited not only larger tonsil sizes13 but also narrow hard palates. They also had increased scores in the Mallampatti scale,14 indicative of a more dolichocephalic facial skeleton with an usually narrow upper airway and enlarged inferior nasal turbinates. We, as well as others, previously reported that appropriate surgical treatments help to eliminate the reported symptoms, the snoring and the nonapneic/nonhypopneic events.7,23,30


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Children who have chronic snoring and do not meet the criteria for OSAS present an abnormal sleep EEG with significant increase in CAP rate, with a predominance of abnormalities in slow wave sleep. The sleep instability demonstrated with the CAP scoring system can explain the detrimental effects that are associated with chronic nonapneic snoring on the sleep EEG. A better analysis of sleep disruption should be attempted when investigating the potential detrimental effects of chronic snoring.


   ACKNOWLEDGMENTS
 
Dr Lopes was supported by an educational grant from Sanofi-Aventis during her postdoctoral fellowship.

We thank Dr P. Navab for editing the manuscript.


   FOOTNOTES
 
Accepted Feb 6, 2006.

Address correspondence to Christian Guilleminault, MD, BiolD, Stanford University Sleep Disorders Clinic, 401 Quarry Rd, Suite 3301, Stanford, CA 94305. E-mail: cguil{at}stanford.edu

The authors have indicated they have no financial relationships relevant to this article to disclose.

Dr Lopes verbally presented this work at the annual meeting of the Associated Professional Sleep Societies; June 18–23, 2005; Denver, CO (Pediatric Young Investigator Award).


   REFERENCES
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 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2006 by the American Academy of Pediatrics



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