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ARTICLE

Chronic Snoring and Sleep in Children:

A Demonstration of Sleep Disruption

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

Stanford University Sleep Medicine Program, Stanford, California

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

ABSTRACT

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 crite-ria 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.

www.pediatrics.org/cgi/doi/10.1542/ peds.2005-3046

doi:10.1542/peds.2005-3046

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).

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

Accepted for publication 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@ stanford.edu

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B

ECAUSE OF THE diversity and the ambiguity in its presentation of symptoms, sleep-disordered breath-ing (SDB) in children still is an ignored entity in clinical practice. Children, therefore, are often referred to spe-cialty 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 evalu-ated by otorhinolaryngologists. On the basis of these clinicians’ findings, some children thereafter will be sent to sleep clinics for evaluation of the sleep-related com-plaint. 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 recogniz-able, but the “sleep hypopneas,” depending on the def-inition 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 pres-sure crescendo” (Pes crescendo), or “esophageal prespres-sure

continuous abnormal effort”1,2, that involve the use of

specific sensors, such as a nasal cannula–pressure ducer or an esophageal catheter with a pressure trans-ducer.1,3,4

Because of these difficulties, some have preferred to look at “chronic snoring” as an abnormal breathing pat-tern 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

arous-al.5 The diurnal and nocturnal behavioral changes

strongly suggest that disruption of the normal sleep pro-cess 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

inves-tigated 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

(ⱖ3 seconds).12Normative data on small groups of

chil-dren of various ages have been published.8–10This report

delineates the analysis of sleep and breathing that is performed in children with daytime behavioral

symp-toms and marked nocturnal snoring in the absence of obstructive sleep apnea (OSA) during polysomnography.

METHODS

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 aris-ing in the mornaris-ing; phase delay schedules; behavioral symptoms that consisted of daytime chronic irritability with, at times, inappropriate aggressiveness; and difficul-ties in school that stemmed from inattention, hyperac-tivity, 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 un-dergo 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

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in-take, physical activity, and the presence of health prob-lems 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

fea-tures, tonsil size scales, Mallampatti scores,13,14nasal

ex-ternal 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 6:30PM. On the night of

the test and the next morning, the subjects also com-pleted questionnaires that evaluated their daytime activ-ities 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 electromy-elogram, electrocardiogram, a modified V2 lead, and position sensor. Respiration was monitored with nasal cannula pressure transducer, mouth thermistor, uncali-brated respiratory plethysmography, thoracic and ab-dominal bands, pulse oximeter, and neck microphone. Continuous video monitoring was used with the noctur-nal polysonogram. One parent also slept on the premises during the recording.

Data Analysis

Sleep stages were scored using the international

crite-ria.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

[␣] or ⬎16 Hz [␤]). In REM sleep, an increase in the

amplitude of the submental electromyelogram was des-ignated 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

de-tected 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 be-tween 2 phases A, 2 to 60 seconds in duration, corre-sponding 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␦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 predomi-nance of polyphasic bursts; and A3, in which at least 50% of the EEG activity is composed of low-amplitude

fast rhythms, such as K-␣ complexes, American

Acad-emy of Sleep Medicine arousals,17and 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 com-pared 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.

Ap-neas 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

can-nula curve. Tachypnea was defined as a switch to a

respiratory rateⱖ20 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 nonhy-popneic events (number of events with only flow limi-tations) were counted toward the calculation of the respiratory disturbance index (RDI) according to

Guil-leminault et al.20 The RDI included the AHI with the

addition of these breathing events. OSA syndrome (OSAS) was defined when clinical symptoms were

asso-ciated with an AHI ⬎1 event per hour of sleep. When

the AHI was⬍1, SaO2was⬎92%, and clinical symptoms

were present with the presence of an RDIⱖ1.5/hour, we

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Statistical Analysis

Central tendency measures were expressed as mean ⫾

SD. The Mann-WhitneyUtest 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 be-tween CAP parameters during NREM sleep stages. Cor-relations between sleep architecture parameters and CAP events, as well as between arousals and phase A subtypes of CAP, were evaluated by Spearman’s

corre-lation coefficient (rS). The level of significance for the

variance analyses and correlation tests was set atPⱕ.01.

All statistical analysis recommendations were conducted using SPSS statistical package version 11.5 (SPSS, Inc, Chicago, IL).

RESULTS

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 Ta-ble 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 polysom-nogram).

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 turbi-nates. 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

tur-binates, and 5 patients had enlarged tonsils13and

turbi-nates as well as a deviated septum; 7 patients had

Mal-lampatti 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.

All patients were snorers, but, per definition, did not show the polysomnographic criteria for OSAS. They

pre-sented 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

SaO2of 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 re-cordings.

TABLE 1 Complaints Associated With Chronic Snoring

Patients Controls

Complaints

Snoring 15 1

Difficulty sleeping 2 0

Sleepwalking 3 0

Difficulty waking up 4 0

Sleep-phase delay 2 0

School difficulties 7 1

Hyperactivity 4 0

Irritability 3 0

Inattention 2 0

Daytime fatigue 6 0

Association of symptoms

School difficulties with inattention/ hyperactivity/aggressiveness

5 0

School difficulties with inattention/ hyperactivity

3 0

School difficulties with daytime fatigue 2 0

School difficulties, waking-up difficulties, daytime fatigue

1 0

Waking-up difficulties, sleep-phase delay 2 0

Waking-up difficulties, daytime fatigue 1 0

Daytime fatigue, sleep difficulties 2 0

TABLE 2 Anatomic Findings Involving the Upper Airway Anatomic Scales

Results

Patients Controls

Tonsil scale

Tonsil1 1 6

Tonsil2 7 8

Tonsil3 6 1

Tonsil4 1 0

Mallampati scale

M.1 4 8

M.2 4 7

M.3 5 0

M.4 2 0

Nasal inferior turbinates

N1 1 11

N2 4 2

N3 11 2

Narrow hard palate 6 0

Deviated septum 6 1

Retroposition mandible 5 1

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Sleep Parameters

TST was not significantly longer in normal control sub-jects, 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).

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

sig-nificant, but the group sizes were small (Table 4). 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 com-plaints 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

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

Disor-ders22 for OSA determination in children is applied. It

was reported previously that snoring can be associated

with impairments in school performance23–26 and

para-somnias, such as chronic sleepwalking in children.27,28It

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.29Using a computerized analysis and a

sophis-ticated algorithm, Chervin et al7showed 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 def-inition 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 pat-terns. 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 anatomi-cally different from the control subjects: they exhibited

not only larger tonsil sizes13 but also narrow hard

pal-ates. They also had increased scores in the Mallampatti

scale,14 indicative of a more dolichocephalic facial

skel-eton with an usually narrow upper airway and enlarged inferior nasal turbinates. We, as well as others, previ-ously reported that appropriate surgical treatments help to eliminate the reported symptoms, the snoring and the

nonapneic/nonhypopneic events.7,23,30

CONCLUSIONS

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

TABLE 3 Sleep Parameters

Snorers (n⫽15)

Controls (n⫽15)

SL, min 9.5 (1.6) 12.1 (2.2)

TST, min 435.6 (26) 471.5 (46)

WASO, min 20.2 (7.7) 19.8 (6.9)

SE, % 95.6 95.8

S1, min 9.5 (6.1) 17.8 (11.2)

S2, min 251.9 (21) 262.8 (26)

S3, min 17.0 (4) 15.1 (3.8)

S4, min 61.0 (12) 77.1 (19)

REM, min 96.9 (8.4) 99.0 (9)

Arousal index in NREM 7.8 (3.0) 4.7 (2.1)

SL indicates sleep latency; WASO, wake after sleep onset; SE, sleep efficiency; S, stage. Arousal index: number of arousal per hour of NREM sleep. None of the variables were significantly significant despite a trend toward longer TST in control subjects. The numbers in parentheses are SDs.

TABLE 4 CAP Parameters in NREM Sleep

Snorers (n⫽15) Controls (n⫽15)

CAP rate, % 65.2⫾6.6a 52.8 (8.6)

CAP time, min 214 (41.1)a 195.7 (17.9)

CAP cycles 374 (101)a 297 (54)

Duration of cycles, s 28 (2) 27 (3)

Phase A 8 (1) 9 (1.5)

Phase B 20 (2) 18 (3)

Phase A indices

A1, % 73.5 (12.8) 85.1 (9.8)

A2, % 18.5 (5.3)a 13.0 (6.3)

A3, % 8.5 (2.4)a 5.3 (2.8)

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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.

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DOI: 10.1542/peds.2005-3046

2006;118;e741

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M. Cecilia Lopes and Christian Guilleminault

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

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M. Cecilia Lopes and Christian Guilleminault

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

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Figure

TABLE 1Complaints Associated With Chronic Snoring
TABLE 4CAP Parameters in NREM Sleep

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