Snoring and stertor are associated with more sleep disturbance than apneas and hypopneas in pediatric SDB

Sleep-disordered breathing (SDB) in children typically presents as a history of snoring, disturbed sleep, and enlarged adenoids/tonsils. An array of daytime symptoms, including attention difficulties and hyperactivity are common [1]. Supervised polysomnography (PSG) is the recommended diagnostic test in clinical practice [2]; however, it is widely recognized that PSG-derived indices do not adequately characterize childhood SDB [3]. While standard PSG metrics report apneas and hypopneas, they do not measure periods of partial upper airway obstruction (UAO) such as snoring that are characteristic of pediatric SDB. Many PSG systems do use snore sensors but the recommended recording parameters [4] only permit capture of a small bandwidth of snore sounds [5‐7]. Flow limitation is another sign of UAO seen on PSG but it is not routinely quantified as it is difficult to do so. Additionally, body movements, a robust indicator of sleep disruption intrinsic to actigraphy, are not scored as arousal events in PSG unless there is a concurrent EEG activation [4].

The Sonomat is a non-contact mat system, recently validated against PSG in children for measurement of PSG metrics such as total sleep time (TST) and the apnea/hypopnea index (AHI) [7] with sensitivity and specificity of 86% and 96% respectively at a threshold of 5 events per hour. This system also allows accurate measurement of snoring and stertor [6, 7] which are pathognomonic physical signs of partial UAO and may be associated with sleep disruption [8].

The purpose of this study was to use the Sonomat in the homes of a large group of children with symptoms of SDB and to compare the sleep disturbance (movement arousal) associated with snoring and stertor to that caused by apneas and hypopneas. A secondary aim was to evaluate the unsupervised use of this system when administered by parents/caregivers.

This study was undertaken through the David Read Laboratory (University of Sydney, NSW, Australia) with the protocol approved by the University of Sydney Human Research Ethics Committee (HREC Ref: 10–2007/10229). Parents/caregivers of children (< 18 years) with suspected SDB were invited to participate and provided written informed consent if agreeable. Children provided assent when able.

There were 213 technically successful recordings (92%) from 231 children. The 18 failures comprised no recording in three (17%), < 4 h of interpretable data in seven (39%), and < 4 h lying on the Sonomat in eight (44%); all in this latter group left the bed after several hours of sleep and did not return. Six of the seven children (86%) who were on the Sonomat for ≥ 4 h, but whose recordings contained < 4 h of interpretable data, were ≤ 5 years old. However, although children ≤ 5 years of age predominated in this group of poor-quality recordings, they were only a small proportion (5%) of the 129 children in this age group.

The cohort was aged 5.2 years (3.7, 8.5) range 0.8–17.7, 120 (56%) were male, with BMI z-score = 0.46 (− 0.35, 1.7) (n = 154 with height/weight information). Two-thirds of children (n = 141) were ≤ 6 years (Fig. 2).

There were 116,605 min recorded (range 284 to 733) with uninterpretable signals for 10,841 min (9% of TRT) leaving 105,764 min (91% of TRT) available for analysis (range 240 to 710). Uninterpretable signals included poor-quality signals (max = 382 min) and time out of bed (max = 250 min). There were 145 children (68%) with ≥ 1 episode of poor signal quality and 59 (28%) left their bed on ≥ 1 occasion. Detailed time and movement data are shown in Table 1.

While it has long been recognized that childhood SDB is characterized by “prolonged partial upper airway obstruction” [9], objective measurement has proven elusive. Various methods have attempted to compensate for the limitations of AHI metrics [3], but their invasive [10] or complex [11] nature has precluded widespread acceptance in clinical practice. Quantitative measurement of snoring and stertor with the Sonomat system provides a practical way of assessing partial UAO, in addition to identifying discrete apnea/hypopnea events. The failure rate in an unsupervised environment was very low, confirming that the Sonomat is practical and easy to use with children in the home.

A small proportion of children, not unexpectedly, left their bed and did not return (possibly to sleep in their parent’s bed). Those whose studies failed due to poor signal quality tended to be younger (≤ 5 years). It is possible that their small size allowed them to lie between the four sensors for long periods although one study was failed due to the presence of a cooling fan masking signals from all sensors. Despite children ≤ 5 years of age predominating in the studies deemed to have failed due to poor-quality signals, they were only a small proportion of all children aged 5 years or younger. Additionally, although we show that the duration of poor-quality signal is greater in younger age groups, the duration of good quality recordings remains at > 7 h (Table 3). Therefore, a younger age does not contraindicate Sonomat use. In our experience, younger children are ideally suited for Sonomat use as they are often the most distressed during polysomnography.

Our results in this large group extends previous work in which the method was validated against PSG [7] and confirms that obstructed breathing predominates as an indicator of pediatric SDB. Quantification of obstructed breathing identified 98% of OSA children with only 2 children crossing one, but not both obstructed breathing thresholds (Fig. 3). Thus, the absence of obstructed breathing could be used to discount the presence of OSA. Most importantly, OSA and non-OSA children were frequently indistinguishable regarding the frequency and duration of obstructed breathing and many symptomatic children did not have OSA or obstructed breathing.

A major new finding is that runs of snoring and stertor are linked to most movement arousals resulting in a level of sleep disruption that is an order of magnitude greater than that associated with apneas/hypopneas alone. The current standard metrics generated from routine PSG, focusing on apneas and hypopneas, underestimate the nature and extent of partial UAO in children and its major role in sleep disruption.

The finding that obstructed breathing runs are frequently terminated by movement may help to explain why some robust measures of SDB outcome do not have a simple relationship with the AHI. The most notable is that SDB of any severity, including “simple” snoring, is associated with elevated blood pressure [12]. Our data support the idea that obstructed breathing, not just AHI-linked events, is a major pathophysiological pathway in pediatric SDB. We suggest that the further step of providing an accurate measurement of obstructed breathing, as a complementary measurement to AHI metrics, will further clarify links to cardiovascular and other outcomes.

Our analyses show that snore and stertor runs are brief and, as they are also separated by short intervals, tend to occur in clusters. Without an electroencephalogram (EEG), we cannot confirm that the episodes of normal breathing between obstructed breathing runs occur during wake/arousal or sleep; however, they would undoubtedly have a fragmentary effect on sleep and/or sleep processes. Even in the absence of a MA, a change from abnormal to normal breathing strongly indicates that some form of activation has occurred within the airway. Work investigating respiratory effort-related arousal events [13] would support this.

These data may also provide an explanation for anomalies in the landmark CHAT study [14, 15]. The first anomaly was a lack of correlation between the AHI and clinical measures of severity from the pediatric sleep questionnaire (PSQ). Secondly, the AHI did not predict the response to surgery, whereas the PSQ did. At face value, these results question the utility of PSG. Our findings, that large numbers of obstructed breathing runs are associated with sleep disruption, could explain this as partial UAO was not quantified in the CHAT study.

Our results also align with recent prospective work identifying adverse impacts of childhood SDB in cognitive and behavioral domains. Hunter et al. [16] found an association between SDB and cognitive dysfunction that was particularly marked in moderate/severe OSA. In contrast, separate analysis in the same cohort [17] found that behavioral dysfunction was most prominent in the mildest SDB (habitually snoring children without OSA). Furthermore, abnormalities in the behavioral domain were less marked as SDB severity increased. In these two analyses, the history of snoring (assessed by questionnaire) was included with the AHI as the independent variable. More recently, the same data was re-analyzed with snoring and OSA assessed as separate variables [18]. It emerged that the frequency of snoring (parentally reported weekly frequency, not to be confused with frequencies contained within snoring sounds) was better correlated with behavioral dysfunction than was the AHI. Additionally, while behavioral abnormalities were less marked as the AHI increased, abnormalities in cognitive measures were worse. Notably, these relationships were apparent despite snoring “frequency” being assessed only by parental reports. The findings are consistent with the interpretation that sleep fragmentation induced by runs of snoring/stertor may have the greatest impact on behavior, whereas changes in blood gases associated with apneas/hypopneas may have a more pronounced effect on cognition.

The two dominant pathophysiological pathways in SDB, sleep fragmentation and blood gas changes, both entrain a variety of different and overlapping downstream effects. Blood gas changes induce major reflex responses (hypertension and arousal) as well as more direct adaptive and maladaptive cellular changes [19]. Arousal and sleep fragmentation induces sympathetic activation (which may contribute to hypertension) and impacts on sleep-dependent brain function [20]. It is not surprising that SDB can produce arousal without significant blood gas changes. There is substantial data implicating that a major pathway to arousal from sleep are upper airway reflexes induced by vibratory stimuli [21]. We suggest that obstructed breathing is a sensitive and specific indicator of pediatric SDB that will show strong correlations with a different spectrum of objective outcomes than does the MOAHI alone [22].

Negative intrathoracic and increased intracranial pressures may be another set of important pathophysiological pathways in SDB; both are known to be influenced by UAO [23]. The longer the duration that abnormal pressures are present may be important and the total duration of UAO may be a useful measurement to indicate this. The total duration of UAO is not typically measured in PSG but we show that obstructed breathing occurs for 60 times longer than do obstructive apneas/hypopneas in this group of symptomatic children (Table 5). Prolonged partial obstruction is a key mechanism of elevated carbon dioxide levels, and in turn, a driver of cerebrospinal fluid pressures and sympathetic outflow. Future work examining the relationship between time spent in obstructed breathing and various outcomes is clearly warranted.

These subjects were typical of a clinical group of children referred to an otolaryngologist needing assessment for adenotonsillectomy. All had a range of symptoms indicative of SDB, for which the primary care physician thought assessment was required and is representative of the ~ 90% of children who undergo adenotonsillectomy without PSG evaluation [24, 25]. We incidentally found nocturnal asthma in one child. Although some snoring was present, the major component of this child’s disordered breathing during sleep consisted of wheeze. This exemplifies work showing that parents are unreliable in both determining the severity of OSA [26] and in identifying wheeze [27] and has important clinical implications.

Limitations include the lack of an EEG to identify sleep and arousal. However, previous work confirmed a close relationship between Qd and EEG-defined sleep as well as accurate calculation of MOAHI [7] and the use of body movement is a robust indicator of sleep disturbance [28]. Adding oximetry to the Sonomat system provides a more complete evaluation of SDB but requires attachment to the body; we have experienced problems using this additional channel, particularly in the home. Transcutaneous carbon dioxide measurement has the same physical constraints although it may be a better indicator of the downstream effects of obstructed breathing [29].

The Sonomat is a reliable method for quantifying and characterizing the extent and disruptive nature of partial UAO in children in the home environment as well as measuring the standard metrics of SDB. Our previous work has been extended in this study by linking runs of snoring and stertor with sleep fragmentation to an extent that is an order of magnitude greater than that caused by apnea/hypopnea events. Thus, many children classified as “simple” snorers without OSA may have numerous runs of snoring and/or stertor that fragment sleep. These findings may help to explain apparent anomalies between the downstream effects of SDB and measurements obtained using standard PSG. Finally, many children who would progress to surgery on clinical indicators, without objective measurement of SDB, may have minimal partial obstruction and no obstructive respiratory events.