REVIEW URRENT C OPINION
Pediatric sleep studies: when and how often are they necessary? Norman R. Friedman
Purpose of review With the increased awareness of the morbidity associated with snoring, polysomnography (PSG) is becoming more prevalent. Many national organizations have recently published clinical guidelines to facilitate decision-making for children with disrupted breathing patterns. This review will discuss these clinical guidelines and describe the rationale behind them. It will also touch on the limitations of PSG. Recent findings The common theme for the clinical guidelines is that PSG is being underutilized. Not only is obstructive sleep apnea (OSA) associated with behavioral, cognitive, and cardiovascular morbidity, but primary snoring is also not always benign. The interpretation of the PSG is influenced by multiple variables: filter settings, sensors utilized, and how the respiratory events are tabulated. Summary To diagnose OSA, one requires overnight PSG. Multiple guidelines have been published to facilitate decision-making. Many questions remain unanswered and future research as well as PSG standardization will further clarify the role of PSG in the evaluation and treatment of disrupted breathing patterns in children. Keywords children, clinical guidelines, obstructive sleep apnea, polysomnography, snoring
INTRODUCTION The gold standard for diagnosing disrupted breathing patterns in children is overnight polysomnography (PSG) in a sleep facility [1 ,2]. Ambulatory sleep studies have not been accepted for children. PSG measures multiple variables: sleep architecture, gas exchange, respiratory events, snoring, limb movements, heart rate, and body position (Fig. 1). The outcome measures of PSG are listed below: &&
(1) (2) (3) (4) (5) (6) (7) (8) (9) (10) (11)
Sleep architecture Sleep efficiency Spontaneous arousal index Obstructive apnea/hypopnea index (OAHI) Central apnea/hypopnea index Respiratory disturbance index (RDI) Periodic breathing (% of total sleep time) Oxygen distribution Oxygen saturation nadir CO2 distribution Periodic limb movement index
Sleep-related breathing disorders (SRBDs) are a spectrum from primary snoring to upper airway resistance to obstructive hypoventilation and to
obstructive sleep apnea (OSA). To determine the type of SRBD, one needs overnight PSG. If one uses a clinical evaluation alone, the diagnosis is sleepdisordered breathing (SDB). OSA is diagnosed when SDB is accompanied by abnormal PSG with obstructive events [2]. Only PSG can distinguish primary snoring from OSA.
INDICATIONS Recently, there have been a variety of clinical guidelines released to facilitate decision-making of when PSG is indicated. The most common indication for requesting PSG is to evaluate for OSA. A comprehensive list of the respiratory indications for PSG in
Department of Otolaryngology, University of Colorado School of Medicine and Children’s Hospital Colorado, Aurora, Colorado, USA Correspondence to Norman R. Friedman, MD, DABSM, Department of Pediatric Otolaryngology, University of Colorado School of Medicine, Children’s Hospital Colorado, 13123 E 16th Avenue, B455, Aurora, CO 80045, USA. Tel: +1 303 777 4777; fax: +1 720 777 7345; e-mail: [email protected] Curr Opin Otolaryngol Head Neck Surg 2013, 21:557–566 DOI:10.1097/MOO.0b013e328365ba8d
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KEY POINTS To diagnose OSA, one requires overnight PSG. Surveys and clinical examination do not have high diagnostic test accuracy when compared with PSG. The severity of OSA does not always predict behavioral and neurocognitive outcomes. Primary snoring may not be benign. Variability exists in the acquisition of PSG. One needs to be aware of how the PSG is being performed because it will affect the final interpretation. Although PSG is considered the gold standard, it does have its limitations.
children according to the American Academy of Sleep Medicine (AASM) is presented in Table 1. The indications are divided into three groups: standard, guideline, and option. A ‘standard’ level of recommendation has high degree of clinical certainty with use of level 1 evidence or overwhelming level 2 evidence, whereas a ‘guideline’ has a moderate degree of clinical certainty. An ‘option’ has uncertain clinical use [3]. The American Academy of Pediatrics (AAP) states that if a child or adolescent snores on a regular basis and has either signs or symptoms suggestive of
sleep apnea (see clinical evaluation below), clinicians should ideally obtain PSG (recommendation), but may refer the patient to a sleep specialist or otolaryngologist for a more extensive evaluation (option). Following an adenotonsillectomy, the AAP asserts clinicians should reevaluate high-risk patients for persistent obstructive sleep apnea syndrome (OSAS): those who had significantly abnormal baseline PSG, have sequelae of OSAS, are obese, or remain symptomatic after treatment, with an objective test or refer such patients to a sleep specialist (recommendation) [1 ]. An accompanying technical report provides a comprehensive review of the SDB literature through 2011 [4 ]. As for Down syndrome, specific guidelines have also been published. Clinicians should discuss symptoms of SRBD at each well child visit and refer to a clinician with expertise in pediatric sleep disorders if symptoms are present. As there is a poor correlation between parent report and PSG results, all Down syndrome children should undergo PSG prior to 4 years of age even if they are asymptomatic [5]. Apart from Down syndrome children, a specific recommendation has been made for children with Prader-Willi syndrome. A consensus guideline from the Growth Hormone Research Society workshop established that PSG should be obtained prior to initiation of recombinant human growth hormone for Prader-Willi children. Severe OSA is considered an exclusion for starting therapy. Repeat PSG is &&
&&
EEG (brain)
EOG (Eyes) EMG (Muscles) EKG and heart rate Limb leads Snore microphone
Airflow
Effort Gas exchange (Oxygen & carbon dioxide)
FIGURE 1. A representative 30-s sample (epoch) of polysomnography. The EEG, electrooculogram (EOG), and electromyogram (EMG) allow for sleep stage scoring. 558
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Pediatric sleep studies Friedman Table 1. Respiratory indications for polysomnography in children according to the American Academy of Sleep Medicine I. Standard When the clinical assessment suggests the diagnosis of obstructive sleep apnea syndrome (OSAS) in children. If there are residual symptoms of OSAS for children with mild OSA preoperatively, postoperative PSG should be performed. Postoperative PSG is indicated to assess for residual OSAS in children with preoperative evidence for moderate-to-severe OSAS, obesity, craniofacial anomalies that obstruct the upper airway, and neurologic disorders (e.g., Down syndrome, Prader-Willi syndrome, and myelomeningocele). Initiation of positive airway pressure (PAP) in children with OSAS. II. Guideline When the clinical assessment suggests the diagnosis of congenital central alveolar hypoventilation syndrome or sleep-related hypoventilation due to neuromuscular disorders or chest wall deformities. When there is clinical evidence of a sleep-related breathing disorder in infants who have experienced an apparent life-threatening event. In children being considered for adenotonsillectomy to treat OSAS. In children on chronic PAP support to determine whether pressure requirements have changed as a result of the child’s growth and development, if symptoms recur while on PAP, or if additional or alternate treatment is instituted. III. Option After treatment with rapid maxillary expansion to assess for the level of residual disease and to determine whether additional treatment is necessary. OSAS treated with an oral appliance to assess response to treatment. For noninvasive positive pressure ventilation titration in children with other sleep-related breathing disorders. Children treated with mechanical ventilation may benefit from periodic evaluation with PSG to adjust ventilator settings. Children treated with tracheostomy for sleep-related breathing disorders as part of the evaluation prior to decannulation. In the following respiratory disorders, only if there is a clinical suspicion for an accompanying sleep-related breathing disorder: chronic asthma, cystic fibrosis, pulmonary hypertension, bronchopulmonary dysplasia, or chest wall abnormality such as kyphoscoliosis. PSG, polysomnography. Data from [3].
indicated if there is worsening in a Prader-Willi child’s breathing status [6]. In regard to epilepsy and PSG, clinical guidelines have not been published. A recent retrospective study by Jain et al. [7] evaluated children with epilepsy and sleep disruption. There were 52 children who were diagnosed with OSA (OAHI >1 event/h) and 16 with primary snoring (no PSG evidence of OSA or hypoventilation). The odds ratio that a child with uncontrolled epilepsy would have OSA compared to primary snoring was 4.6. There were no significant differences based on age, BMI, epilepsy type, developmental state, and the number of antiepileptic drugs between the groups [7]. The study suggests that neurologists should screen for OSA, especially when uncontrolled epilepsy is present. The American Academy of Otolaryngology/ Head and Neck Surgery (AAO/HNS) has a more selective policy for obtaining PSG (Table 2). For action statement number 1, the rationale is to avoid unnecessary intervention in children with higher surgical risk and facilitate postoperative planning. For action statement number 2, the intent is to minimize the risk of either overtreating or undertreating. The AAO/HNS recommendations for postoperative monitoring were addressed in action
statement number 4, but were based only on observational studies [2]. Despite the lower quality of evidence, the academy decided to err on the side of caution. Needless to say, without preoperative PSG, one can only be compliant with the age requirement for action statement number 4. If one’s primary indication for performing PSG is for perioperative planning, one could limit the risks by admitting all children with SDB for observation, especially if comorbidities are present. In 2012, Friedman et al. [8 ] published an American Society of Pediatric Otolaryngology (ASPO) survey of the current practice patterns for SRBD. The survey was administered prior to the publication of the new AAO/HNS PSG guidelines. Only 4% of ASPO members referred an otherwise healthy 5-year-old child for PSG ‘most of the time’. Thirty one percent of the time, members ‘rarely to never’ requested preoperative PSG. The primary reason for requesting PSG in a healthy child was inconsistent history and physical examination. Although members were not routinely obtaining preoperative PSG for children with comorbidities, the threshold to admit these children for overnight observation was higher. Overnight observation was performed ‘most of the time’ for the following
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Pediatric otolaryngology Table 2. Indications for polysomnography according to the American Academy of Otolaryngology/Head and Neck Surgery Action statement no. 1 Before performing tonsillectomy, the clinician should refer children with SDB for PSG, if they exhibit any of the following: obesity, Down syndrome, craniofacial abnormalities, neuromuscular disorders, sickle cell disease, or mucopolysaccharidoses. Action statement no. 2 The clinician should advocate for PSG prior to tonsillectomy for SDB in children without any of the comorbidities listed in statement 1 for whom the need for surgery is uncertain or when there is discordance between tonsillar size on physical examination and the reported severity of SDB. Action statement no. 4 Clinicians should admit children with OSA documented in results of PSG for inpatient, overnight monitoring after tonsillectomy if they are younger than age 3 or have severe OSA (apnea/hypopnea index of 10 or more obstructive events/h, oxygen saturation nadir less than 80%, or both). OSA, obstructive sleep apnea; PSG, polysomnography; SDB, sleep-disordered breathing. Data from [2].
groups: Down syndrome (83%), age less than 3 years (83%), and obesity (70%). Dr Gozal, a pioneer in pediatric OSA, recently published his personal algorithm for the diagnosis and treatment of pediatric OSA that has some applicability for regions that have poor access to PSG [9]. Although the major indication for PSG is to identify OSA, there are nonrespiratory indications for obtaining PSG. In 2012, the AASM published practice parameters to help guide clinicians (Table 3) [10]. A Multiple Sleep Latency Test (MSLT) is daytime PSG that occurs at 2-h intervals following overnight PSG. It consists of five nap opportunities and is the primary test to evaluate narcolepsy. Kotagal et al. [11] published an accompanying evidence-based review for the nonrespiratory indications for PSG.
CLINICAL EVALUATION Clinical examination findings that should raise one’s suspicion of OSA are the following:
(1) Nighttime symptoms: frequent snoring (3 nights/week), labored breathing during sleep, gasps/snorting noises observed, episodes of apnea, secondary enuresis, sleeping in a seated position or with the neck hyperextended, and cyanosis (2) Daytime symptoms: headaches on awakening, daytime sleepiness, attention-deficit/hyperactivity disorder, and learning problems (3) Physical examination: underweight or overweight, tonsillar hypertrophy, adenoidal facies, micrognathia/retrognathia, high-arched palate, failure to thrive, or hypertension. According to the AAP, when these findings are present, clinicians should ideally request overnight PSG [1 ]. Unfortunately, there are no surveys that reliably predict the PSG findings, that is, clinical evaluation does not reliably detect OSA. Spruyt and Gozal [12] have proposed a set of questions to identify pediatric SDB. They identified an ordered set of six questions, &&
Table 3. Nonrespiratory indications for polysomnography I. Standard For children suspected of having periodic limb movement disorder (PLMD) for diagnosing PLMD. Nocturnal PSG should precede a Multiple Sleep Latency Test (MSLT). II. Guideline Children with frequent NREM parasomnias, epilepsy, or nocturnal enuresis if there is a suspicion for sleep-disordered breathing or PLMD. III. Option The MSLT, preceded by nocturnal PSG, is indicated in children suspected of having hypersomnia from causes other than narcolepsy to assess excessive sleepiness and to aid in differentiation from narcolepsy. The PSG using an expanded EEG montage is indicated in children to confirm the diagnosis of an atypical or potentially injurious parasomnia or differentiate a parasomnia from sleep-related epilepsy. In children suspected of having restless legs syndrome (RLS), who require supportive data for diagnosing RLS. NREM, nonrapid eye movement; PSG, polysomnography. Data from [10].
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FIGURE 2. A hypopnea that is scorable due to an arousal in the EEG pattern.
which were useful as a screening tool, but not to make a diagnosis of OSA. Clinical questions for a severity hierarchy for sleep-disordered breathing are as follows [12]: (1) Do you ever shake your child to make him/her breathe again when asleep?
(2) Does your child stop breathing during sleep? (3) Does your child struggle to breathe while asleep? (4) Are you ever concerned about your child’s breathing during sleep? (5) How loud is the snore?0: mildly quiet; 1: medium loud; 2: loud; 3: very loud; 4: extremely loud. (6) How often does your child snore?
FIGURE 3. A hypopnea that is scorable due to a 3% oxygen desaturation without EEG recording. 1068-9508 ß 2013 Wolters Kluwer Health | Lippincott Williams & Wilkins
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FIGURE 4. An obstructive apnea without an oxygen desaturation.
(a)
FIGURE 5. (a) Epoch of sleep with flow thermistor only. (b) Epoch of sleep with nasal pressure and flow thermistor. The nasal pressure allows identification of the hypopnea. 562
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(b)
FIGURE 5. (Continued ).
The negative predictive value was 93%, but the positive predictive value was only 35% [12]. Goldstein et al. [13] have validated a 15-item clinical assessment score (CAS). The positive predictive value for their CAS to predict an AHI more than 2 was 82%, whereas the negative predictive value was 53%. A meta-analysis of the literature prior to August 2011 did not identify any combination of history or physical examination findings that was satisfactory in predicting pediatric OSA [14].
of the study was typical in terms of breathing and sleep. This information is useful for the referring clinician when a parent disagrees with the study’s findings. Of note, a study of 257 healthy children between the ages of 3 and 12 years from Melbourne, Australia, did demonstrate a seasonal variability in OSA. The mean seasonal OAHI was significantly higher in winter and spring compared with fall and summer [15]. The decision to obtain postoperative PSG has been addressed by clinical guidelines [1 ,3]. However, treatment outcome studies for OSA after an adenotonsillectomy are sparse. A large multicenter retrospective analysis of factors that were associated with an elevated postoperative AHI, in order of influence, were as follows: age more than 7 years; elevated BMI percentile for age; presence of asthma; and more severe OSA preoperatively, AHI more than &&
TIMING As to when a sleep study should be performed, a child may not be acutely ill At least for children, there is little night-to-night variability. Our laboratory specifically asks the parents through a morning after questionnaire whether they felt that the night
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10 events an hour. Ninety percent of the children were under 13 years of age and 50% were obese [16]. The data from the Childhood Adenotonsillectomy Trial (CHAT) are starting to appear in the literature. CHAT was a multicenter single-blind, randomized, controlled trial at seven academic sleep centers for children between ages 5 and 9 years. Adenotonsillectomy was less likely to result in normalization of PSG findings for African–Americans, children with AHI more than 4.7 preoperatively, and obese children [17 ]. These studies imply that children undergoing adenotonsillectomy for OSA who are older, African–American, obese, asthmatic, or with a more elevated AHI should have postoperative PSG. &&
OTHER TESTS A systematic review of alternative tests to diagnose OSA did not identify strong evidence to support replacing PSG [18]. Their review did identify a study from 2009 that analyzed urinary proteins and had excellent diagnostic test accuracy [19]. Unfortunately, other than a comment in a review article, further evidence to support this analysis has not been published. The article did describe other novel tests that are under investigation to facilitate the diagnosis of OSA [20]. Another option was limited PSG or cardiorespiratory study [18]. Limited PSG does not include EEG, eye leads, or chin tone. Unless EEG recordings are used, one will not be able to
identify all types of hypopneas (Fig. 2). Limited PSG may underestimate the OAHI. Figure 3 is an example of a scorable hypopnea without EEG recordings due to a 3% oxygen desaturation. The McGill group has been pioneer in investigating the role of overnight oximetry in detecting OSA. They have shown that overnight oximetry has a high positive predictive value to detect moderateto-severe OSA. However, a negative study does not exclude OSA. One can have obstructive respiratory events without oxygen desaturations (Fig. 4). A recent study demonstrated excellent night-to-night consistency using nocturnal pulse oximetry [21].
CONTRARIAN VIEW A contrarian view recommends against the routine use of PSG. One should only request a test if the results are going to influence management decisions. Many clinicians view AHI as the primary outcome measure for PSG. Historically, the severity of OSA has not always been predictive of morbidity. Children with primary snoring have been diagnosed with daytime sleepiness, behavioral problems, hypertension, and cognitive delays. Jackman et al. [22] demonstrated that children not only with OSA but also those with primary snoring were identified with behavioral issues. If future research continues to demonstrate that primary snoring is no longer benign, one of the major indications for PSG will become moot.
(a)
(b)
FIGURE 6. (a) Normal CO2 value with a good waveform. (b) Low CO2 value that may be an underestimate as the waveform is peaked. 564
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Limitations of polysomnography Even if the OAHI severity could reliably predict behavioral and neurocognitive morbidity, technical factors can influence PSG outcomes. Chervin et al. [23] demonstrated that esophageal pressure monitoring was more reliable in predicting morbidity and treatment outcomes than the AHI index. Neither esophageal monitoring nor AHI had a robust ability to predict baseline morbidity or treatment outcomes [23]. Few centers use esophageal pressure monitoring. During PSG acquisition, filter and sensor selection may alter the respiratory indices. A nasal pressure cannula is a quantitative sensor and can detect more subtle respiratory events. Without a functional nasal pressure cannula, the severity of OSA may be underestimated (Fig. 5a and b). A disadvantage of the nasal pressure
sensor is that it does not measure oral airflow, which is why more than one flow sensor should be used for PSG acquisitions. Carbon dioxide (CO2) sensors are also important for detecting disrupted breathing patterns for children. Many children, rather than having discrete respiratory events, have prolonged periods of partial obstruction, which are detected by CO2 monitoring. For end-tidal CO2 monitoring, an accurate number depends upon a high-quality signal with a square waveform. One could have a normal end-tidal CO2 distribution, but if the signal is ‘peaked’, the CO2 value is erroneously low (Fig. 6a and b) [24]. PSG outcomes may also be affected by the scoring criteria and terminology of the individual sleep laboratory. Some laboratories provide separate indices for central and obstructive respiratory
FIGURE 7. Example of flow limitation with flattening of the nasal pressure. 1068-9508 ß 2013 Wolters Kluwer Health | Lippincott Williams & Wilkins
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events, whereas others lump all the respiratory events together as an AHI. Apart from apneas and hypopneas, there is a more subtle respiratory event known as a respiratory effort-related arousal (RERA). A RERA is scored when there is a drop in airflow (flow limitation) that does not meet the definition of a hypopnea, but an arousal occurs. The standard definition of an RDI includes all apneas, hypopneas, and RERAS. To detect flow limitation, the appropriate filter settings must be selected (Fig. 7) [24].
CONCLUSION PSG is a useful test and is the gold standard to diagnose OSA, but does have its limitations. If a child has disrupted breathing patterns at night and PSG has not been performed, one should use the diagnosis of SDB. Without PSG, one cannot diagnose OSA. As research continues on the disrupted breathing patterns in children, the evidence will mandate revisions of the current clinical guidelines. Acknowledgements The author would like to thank Amanda Ruiz for her help in putting together this study. Conflicts of interest The author has no conflicts of interest and there are no sources of funding.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Marcus CL, Brooks LJ, Draper KA, et al. Diagnosis and management of childhood obstructive sleep apnea syndrome. Pediatrics 2012; 130:576– 584. doi: 10.1542/peds.2012-1671. Revised clinical practice guideline published by the AAP to provide recommendations for the diagnosis and management of the OSA syndrome, specifically for primary care clinicians. 2. Roland PS, Rosenfeld RM, Brooks LJ, et al. Clinical practice guideline: polysomnography for sleep-disordered breathing prior to tonsillectomy in children. Otolaryngol Head Neck Surg 2011; 145 (1 Suppl):S1–S15. doi:10.1177/0194599811409837. 3. Aurora RN, Zak RS, Karippot A, et al., American Academy of Sleep Medicine. Practice parameters for the respiratory indications for polysomnography in children. Sleep 2011; 34:379–388. 4. Marcus CL, Brooks LJ, Draper KA, et al. Diagnosis and management of && childhood obstructive sleep apnea syndrome. Pediatrics 2012; 130:e714– e755. doi: 10.1542/peds.2012-1672. A comprehensive literature review that accompanies the AAP clinical practice guideline. &&
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5. Bull MJ. Clinical report: health supervision for children with Down syndrome. Pediatrics 2011; 128:393–406. 6. Deal CL, Tony M, Ho¨ybye C, et al., 2011 Growth Hormone in Prader-Willi Syndrome Clinical Care Guidelines Workshop Participants. Growth Hormone Research Society workshop summary: consensus guidelines for recombinant human growth hormone therapy in Prader-Willi syndrome. J Clin Endocrinol Metab 2013; 98:E1072–E1087. doi: 10.1210/jc.2012-3888. 7. Jain SV, Horn PS, Simakajornboon N, Glauser TA. Obstructive sleep apnea and primary snoring in children with epilepsy. J Child Neurol 2013; 28:77–82. doi: 10.1177/0883073812440326. 8. Friedman NR, Perkins JN, McNair B, Mitchell RB. Current practice patterns for & sleep-disordered breathing in children. Laryngoscope 2013; 123:1055– 1058. doi: 10.1002/lary.23709. An internet-based survey to pediatric otolaryngologists to determine how they manage children with SDB. 9. Kaditis A, Kheirandish-Gozal L, Gozal D. Algorithm for the diagnosis and treatment of pediatric OSA: a proposal of two pediatric sleep centers. Sleep Med 2012; 13:217–227. doi: 10.1016/j.sleep.2011.09.009. 10. Aurora RN, Lamm CI, Zak RS, et al. Practice parameters for the nonrespiratory indications for polysomnography and multiple sleep latency testing for children. Sleep 2012; 35:1467–1473. doi: 10.5665/sleep.2190. 11. Kotagal S, Nichols CD, Grigg-Damberger MM, et al. Nonrespiratory indications for polysomnography and related procedures in children: an evidencebased review. Sleep 2012; 35:1451–1466. doi: 10.5665/sleep.2188. 12. Spruyt K, Gozal D. Screening of pediatric sleep-disordered breathing: a proposed unbiased discriminative set of questions using clinical severity scales. Chest 2012; 142:1508–1515. doi: 10.1378/chest.11-3164. 13. Goldstein NA, Stefanov DG, Graw-Panzer KD, et al. Validation of a clinical assessment score for pediatric sleep-disordered breathing. Laryngoscope 2012; 122:2096–2104. doi: 10.1002/lary.23455. 14. Certal V, Catumbela E, Winck JC, et al. Clinical assessment of pediatric obstructive sleep apnea: a systematic review and meta-analysis. Laryngoscope 2012; 122:2105–2114. doi: 10.1002/lary.23465. 15. Walter LM, Nisbet LC, Nixon GM, et al. Seasonal variability in paediatric obstructive sleep apnoea. Arch Dis Child 2013; 98:208–210. doi: 10.1136/ archdischild-2012-302599. 16. Bhattacharjee R, Kheirandish-Gozal L, Spruyt K, et al. Adenotonsillectomy outcomes in treatment of obstructive sleep apnea in children: a multicenter retrospective study. Am J Respir Crit Care Med 2010; 182:676–683. doi: 10.1164/rccm.200912-1930OC. 17. Marcus CL, Moore RH, Rosen CL, et al., Childhood Adenotonsillectomy Trial && (CHAT). A randomized trial of adenotonsillectomy for childhood sleep apnea. N Engl J Med 2013; 368:2366–2376. doi: 10.1056/NEJMoa1215881. A randomized controlled trial of children with OSA but normal oxygenation that compared early adenotonsillectomy to watchful waiting to determine whether earlier treatment would have better neuropsychological outcomes. 18. Brockmann PE, Schaefer C, Poets S, et al. Diagnosis of obstructive sleep apnea in children: a systematic review. Sleep Med Rev 2013; 17:331–340. 19. Gozal D, Jortani S, Snow AB, et al. Two-dimensional differential in-gel electrophoresis proteomic approaches reveal urine candidate biomarkers in pediatric obstructive sleep apnea. Am J Respir Crit Care Med 2009; 180:1253–1261. doi: 10.1164/rccm.200905-0765OC. 20. Gozal D. Serum, urine, and breath-related biomarkers in the diagnosis of obstructive sleep apnea in children: is it for real? Curr Opin Pulm Med 2012; 18:561–567. doi: 10.1097/MCP.0b013e328358be2d. 21. Pavone M, Cutrera R, Verrillo E, et al. Night-to-night consistency of at-home nocturnal pulse oximetry testing for obstructive sleep apnea in children. Pediatr Pulmonol 2013; 48:754–760. doi: 10.1002/ppul.22685. 22. Jackman AR, Biggs SN, Walter LM, et al. Sleep-disordered breathing in preschool children is associated with behavioral, but not cognitive, impairments. Sleep Med 2012; 13:621–631. doi: 10.1016/j.sleep.2012.01.013. 23. Chervin RD, Ruzicka DL, Hoban TF, et al. Esophageal pressures, polysomnography, and neurobehavioral outcomes of adenotonsillectomy in children. Chest 2012; 142:101–110. doi: 10.1378/chest.11-2456. 24. Berry RB, Budhiraja R, Gottlieb DJ, et al., American Academy of Sleep Medicine. Rules for scoring respiratory events in sleep: update of the 2007 AASM Manual for the Scoring of Sleep and Associated Events. Deliberations of the Sleep Apnea Definitions Task Force of the American Academy of Sleep Medicine. J Clin Sleep Med 2012; 8:597–619. doi: 10.5664/jcsm.2172.
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Pediatric sleep studies: when and how often are they necessary? Norman R. Friedman
Purpose of review With the increased awareness of the morbidity associated with snoring, polysomnography (PSG) is becoming more prevalent. Many national organizations have recently published clinical guidelines to facilitate decision-making for children with disrupted breathing patterns. This review will discuss these clinical guidelines and describe the rationale behind them. It will also touch on the limitations of PSG. Recent findings The common theme for the clinical guidelines is that PSG is being underutilized. Not only is obstructive sleep apnea (OSA) associated with behavioral, cognitive, and cardiovascular morbidity, but primary snoring is also not always benign. The interpretation of the PSG is influenced by multiple variables: filter settings, sensors utilized, and how the respiratory events are tabulated. Summary To diagnose OSA, one requires overnight PSG. Multiple guidelines have been published to facilitate decision-making. Many questions remain unanswered and future research as well as PSG standardization will further clarify the role of PSG in the evaluation and treatment of disrupted breathing patterns in children. Keywords children, clinical guidelines, obstructive sleep apnea, polysomnography, snoring
INTRODUCTION The gold standard for diagnosing disrupted breathing patterns in children is overnight polysomnography (PSG) in a sleep facility [1 ,2]. Ambulatory sleep studies have not been accepted for children. PSG measures multiple variables: sleep architecture, gas exchange, respiratory events, snoring, limb movements, heart rate, and body position (Fig. 1). The outcome measures of PSG are listed below: &&
(1) (2) (3) (4) (5) (6) (7) (8) (9) (10) (11)
Sleep architecture Sleep efficiency Spontaneous arousal index Obstructive apnea/hypopnea index (OAHI) Central apnea/hypopnea index Respiratory disturbance index (RDI) Periodic breathing (% of total sleep time) Oxygen distribution Oxygen saturation nadir CO2 distribution Periodic limb movement index
Sleep-related breathing disorders (SRBDs) are a spectrum from primary snoring to upper airway resistance to obstructive hypoventilation and to
obstructive sleep apnea (OSA). To determine the type of SRBD, one needs overnight PSG. If one uses a clinical evaluation alone, the diagnosis is sleepdisordered breathing (SDB). OSA is diagnosed when SDB is accompanied by abnormal PSG with obstructive events [2]. Only PSG can distinguish primary snoring from OSA.
INDICATIONS Recently, there have been a variety of clinical guidelines released to facilitate decision-making of when PSG is indicated. The most common indication for requesting PSG is to evaluate for OSA. A comprehensive list of the respiratory indications for PSG in
Department of Otolaryngology, University of Colorado School of Medicine and Children’s Hospital Colorado, Aurora, Colorado, USA Correspondence to Norman R. Friedman, MD, DABSM, Department of Pediatric Otolaryngology, University of Colorado School of Medicine, Children’s Hospital Colorado, 13123 E 16th Avenue, B455, Aurora, CO 80045, USA. Tel: +1 303 777 4777; fax: +1 720 777 7345; e-mail: [email protected] Curr Opin Otolaryngol Head Neck Surg 2013, 21:557–566 DOI:10.1097/MOO.0b013e328365ba8d
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KEY POINTS To diagnose OSA, one requires overnight PSG. Surveys and clinical examination do not have high diagnostic test accuracy when compared with PSG. The severity of OSA does not always predict behavioral and neurocognitive outcomes. Primary snoring may not be benign. Variability exists in the acquisition of PSG. One needs to be aware of how the PSG is being performed because it will affect the final interpretation. Although PSG is considered the gold standard, it does have its limitations.
children according to the American Academy of Sleep Medicine (AASM) is presented in Table 1. The indications are divided into three groups: standard, guideline, and option. A ‘standard’ level of recommendation has high degree of clinical certainty with use of level 1 evidence or overwhelming level 2 evidence, whereas a ‘guideline’ has a moderate degree of clinical certainty. An ‘option’ has uncertain clinical use [3]. The American Academy of Pediatrics (AAP) states that if a child or adolescent snores on a regular basis and has either signs or symptoms suggestive of
sleep apnea (see clinical evaluation below), clinicians should ideally obtain PSG (recommendation), but may refer the patient to a sleep specialist or otolaryngologist for a more extensive evaluation (option). Following an adenotonsillectomy, the AAP asserts clinicians should reevaluate high-risk patients for persistent obstructive sleep apnea syndrome (OSAS): those who had significantly abnormal baseline PSG, have sequelae of OSAS, are obese, or remain symptomatic after treatment, with an objective test or refer such patients to a sleep specialist (recommendation) [1 ]. An accompanying technical report provides a comprehensive review of the SDB literature through 2011 [4 ]. As for Down syndrome, specific guidelines have also been published. Clinicians should discuss symptoms of SRBD at each well child visit and refer to a clinician with expertise in pediatric sleep disorders if symptoms are present. As there is a poor correlation between parent report and PSG results, all Down syndrome children should undergo PSG prior to 4 years of age even if they are asymptomatic [5]. Apart from Down syndrome children, a specific recommendation has been made for children with Prader-Willi syndrome. A consensus guideline from the Growth Hormone Research Society workshop established that PSG should be obtained prior to initiation of recombinant human growth hormone for Prader-Willi children. Severe OSA is considered an exclusion for starting therapy. Repeat PSG is &&
&&
EEG (brain)
EOG (Eyes) EMG (Muscles) EKG and heart rate Limb leads Snore microphone
Airflow
Effort Gas exchange (Oxygen & carbon dioxide)
FIGURE 1. A representative 30-s sample (epoch) of polysomnography. The EEG, electrooculogram (EOG), and electromyogram (EMG) allow for sleep stage scoring. 558
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Pediatric sleep studies Friedman Table 1. Respiratory indications for polysomnography in children according to the American Academy of Sleep Medicine I. Standard When the clinical assessment suggests the diagnosis of obstructive sleep apnea syndrome (OSAS) in children. If there are residual symptoms of OSAS for children with mild OSA preoperatively, postoperative PSG should be performed. Postoperative PSG is indicated to assess for residual OSAS in children with preoperative evidence for moderate-to-severe OSAS, obesity, craniofacial anomalies that obstruct the upper airway, and neurologic disorders (e.g., Down syndrome, Prader-Willi syndrome, and myelomeningocele). Initiation of positive airway pressure (PAP) in children with OSAS. II. Guideline When the clinical assessment suggests the diagnosis of congenital central alveolar hypoventilation syndrome or sleep-related hypoventilation due to neuromuscular disorders or chest wall deformities. When there is clinical evidence of a sleep-related breathing disorder in infants who have experienced an apparent life-threatening event. In children being considered for adenotonsillectomy to treat OSAS. In children on chronic PAP support to determine whether pressure requirements have changed as a result of the child’s growth and development, if symptoms recur while on PAP, or if additional or alternate treatment is instituted. III. Option After treatment with rapid maxillary expansion to assess for the level of residual disease and to determine whether additional treatment is necessary. OSAS treated with an oral appliance to assess response to treatment. For noninvasive positive pressure ventilation titration in children with other sleep-related breathing disorders. Children treated with mechanical ventilation may benefit from periodic evaluation with PSG to adjust ventilator settings. Children treated with tracheostomy for sleep-related breathing disorders as part of the evaluation prior to decannulation. In the following respiratory disorders, only if there is a clinical suspicion for an accompanying sleep-related breathing disorder: chronic asthma, cystic fibrosis, pulmonary hypertension, bronchopulmonary dysplasia, or chest wall abnormality such as kyphoscoliosis. PSG, polysomnography. Data from [3].
indicated if there is worsening in a Prader-Willi child’s breathing status [6]. In regard to epilepsy and PSG, clinical guidelines have not been published. A recent retrospective study by Jain et al. [7] evaluated children with epilepsy and sleep disruption. There were 52 children who were diagnosed with OSA (OAHI >1 event/h) and 16 with primary snoring (no PSG evidence of OSA or hypoventilation). The odds ratio that a child with uncontrolled epilepsy would have OSA compared to primary snoring was 4.6. There were no significant differences based on age, BMI, epilepsy type, developmental state, and the number of antiepileptic drugs between the groups [7]. The study suggests that neurologists should screen for OSA, especially when uncontrolled epilepsy is present. The American Academy of Otolaryngology/ Head and Neck Surgery (AAO/HNS) has a more selective policy for obtaining PSG (Table 2). For action statement number 1, the rationale is to avoid unnecessary intervention in children with higher surgical risk and facilitate postoperative planning. For action statement number 2, the intent is to minimize the risk of either overtreating or undertreating. The AAO/HNS recommendations for postoperative monitoring were addressed in action
statement number 4, but were based only on observational studies [2]. Despite the lower quality of evidence, the academy decided to err on the side of caution. Needless to say, without preoperative PSG, one can only be compliant with the age requirement for action statement number 4. If one’s primary indication for performing PSG is for perioperative planning, one could limit the risks by admitting all children with SDB for observation, especially if comorbidities are present. In 2012, Friedman et al. [8 ] published an American Society of Pediatric Otolaryngology (ASPO) survey of the current practice patterns for SRBD. The survey was administered prior to the publication of the new AAO/HNS PSG guidelines. Only 4% of ASPO members referred an otherwise healthy 5-year-old child for PSG ‘most of the time’. Thirty one percent of the time, members ‘rarely to never’ requested preoperative PSG. The primary reason for requesting PSG in a healthy child was inconsistent history and physical examination. Although members were not routinely obtaining preoperative PSG for children with comorbidities, the threshold to admit these children for overnight observation was higher. Overnight observation was performed ‘most of the time’ for the following
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Pediatric otolaryngology Table 2. Indications for polysomnography according to the American Academy of Otolaryngology/Head and Neck Surgery Action statement no. 1 Before performing tonsillectomy, the clinician should refer children with SDB for PSG, if they exhibit any of the following: obesity, Down syndrome, craniofacial abnormalities, neuromuscular disorders, sickle cell disease, or mucopolysaccharidoses. Action statement no. 2 The clinician should advocate for PSG prior to tonsillectomy for SDB in children without any of the comorbidities listed in statement 1 for whom the need for surgery is uncertain or when there is discordance between tonsillar size on physical examination and the reported severity of SDB. Action statement no. 4 Clinicians should admit children with OSA documented in results of PSG for inpatient, overnight monitoring after tonsillectomy if they are younger than age 3 or have severe OSA (apnea/hypopnea index of 10 or more obstructive events/h, oxygen saturation nadir less than 80%, or both). OSA, obstructive sleep apnea; PSG, polysomnography; SDB, sleep-disordered breathing. Data from [2].
groups: Down syndrome (83%), age less than 3 years (83%), and obesity (70%). Dr Gozal, a pioneer in pediatric OSA, recently published his personal algorithm for the diagnosis and treatment of pediatric OSA that has some applicability for regions that have poor access to PSG [9]. Although the major indication for PSG is to identify OSA, there are nonrespiratory indications for obtaining PSG. In 2012, the AASM published practice parameters to help guide clinicians (Table 3) [10]. A Multiple Sleep Latency Test (MSLT) is daytime PSG that occurs at 2-h intervals following overnight PSG. It consists of five nap opportunities and is the primary test to evaluate narcolepsy. Kotagal et al. [11] published an accompanying evidence-based review for the nonrespiratory indications for PSG.
CLINICAL EVALUATION Clinical examination findings that should raise one’s suspicion of OSA are the following:
(1) Nighttime symptoms: frequent snoring (3 nights/week), labored breathing during sleep, gasps/snorting noises observed, episodes of apnea, secondary enuresis, sleeping in a seated position or with the neck hyperextended, and cyanosis (2) Daytime symptoms: headaches on awakening, daytime sleepiness, attention-deficit/hyperactivity disorder, and learning problems (3) Physical examination: underweight or overweight, tonsillar hypertrophy, adenoidal facies, micrognathia/retrognathia, high-arched palate, failure to thrive, or hypertension. According to the AAP, when these findings are present, clinicians should ideally request overnight PSG [1 ]. Unfortunately, there are no surveys that reliably predict the PSG findings, that is, clinical evaluation does not reliably detect OSA. Spruyt and Gozal [12] have proposed a set of questions to identify pediatric SDB. They identified an ordered set of six questions, &&
Table 3. Nonrespiratory indications for polysomnography I. Standard For children suspected of having periodic limb movement disorder (PLMD) for diagnosing PLMD. Nocturnal PSG should precede a Multiple Sleep Latency Test (MSLT). II. Guideline Children with frequent NREM parasomnias, epilepsy, or nocturnal enuresis if there is a suspicion for sleep-disordered breathing or PLMD. III. Option The MSLT, preceded by nocturnal PSG, is indicated in children suspected of having hypersomnia from causes other than narcolepsy to assess excessive sleepiness and to aid in differentiation from narcolepsy. The PSG using an expanded EEG montage is indicated in children to confirm the diagnosis of an atypical or potentially injurious parasomnia or differentiate a parasomnia from sleep-related epilepsy. In children suspected of having restless legs syndrome (RLS), who require supportive data for diagnosing RLS. NREM, nonrapid eye movement; PSG, polysomnography. Data from [10].
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FIGURE 2. A hypopnea that is scorable due to an arousal in the EEG pattern.
which were useful as a screening tool, but not to make a diagnosis of OSA. Clinical questions for a severity hierarchy for sleep-disordered breathing are as follows [12]: (1) Do you ever shake your child to make him/her breathe again when asleep?
(2) Does your child stop breathing during sleep? (3) Does your child struggle to breathe while asleep? (4) Are you ever concerned about your child’s breathing during sleep? (5) How loud is the snore?0: mildly quiet; 1: medium loud; 2: loud; 3: very loud; 4: extremely loud. (6) How often does your child snore?
FIGURE 3. A hypopnea that is scorable due to a 3% oxygen desaturation without EEG recording. 1068-9508 ß 2013 Wolters Kluwer Health | Lippincott Williams & Wilkins
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FIGURE 4. An obstructive apnea without an oxygen desaturation.
(a)
FIGURE 5. (a) Epoch of sleep with flow thermistor only. (b) Epoch of sleep with nasal pressure and flow thermistor. The nasal pressure allows identification of the hypopnea. 562
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(b)
FIGURE 5. (Continued ).
The negative predictive value was 93%, but the positive predictive value was only 35% [12]. Goldstein et al. [13] have validated a 15-item clinical assessment score (CAS). The positive predictive value for their CAS to predict an AHI more than 2 was 82%, whereas the negative predictive value was 53%. A meta-analysis of the literature prior to August 2011 did not identify any combination of history or physical examination findings that was satisfactory in predicting pediatric OSA [14].
of the study was typical in terms of breathing and sleep. This information is useful for the referring clinician when a parent disagrees with the study’s findings. Of note, a study of 257 healthy children between the ages of 3 and 12 years from Melbourne, Australia, did demonstrate a seasonal variability in OSA. The mean seasonal OAHI was significantly higher in winter and spring compared with fall and summer [15]. The decision to obtain postoperative PSG has been addressed by clinical guidelines [1 ,3]. However, treatment outcome studies for OSA after an adenotonsillectomy are sparse. A large multicenter retrospective analysis of factors that were associated with an elevated postoperative AHI, in order of influence, were as follows: age more than 7 years; elevated BMI percentile for age; presence of asthma; and more severe OSA preoperatively, AHI more than &&
TIMING As to when a sleep study should be performed, a child may not be acutely ill At least for children, there is little night-to-night variability. Our laboratory specifically asks the parents through a morning after questionnaire whether they felt that the night
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10 events an hour. Ninety percent of the children were under 13 years of age and 50% were obese [16]. The data from the Childhood Adenotonsillectomy Trial (CHAT) are starting to appear in the literature. CHAT was a multicenter single-blind, randomized, controlled trial at seven academic sleep centers for children between ages 5 and 9 years. Adenotonsillectomy was less likely to result in normalization of PSG findings for African–Americans, children with AHI more than 4.7 preoperatively, and obese children [17 ]. These studies imply that children undergoing adenotonsillectomy for OSA who are older, African–American, obese, asthmatic, or with a more elevated AHI should have postoperative PSG. &&
OTHER TESTS A systematic review of alternative tests to diagnose OSA did not identify strong evidence to support replacing PSG [18]. Their review did identify a study from 2009 that analyzed urinary proteins and had excellent diagnostic test accuracy [19]. Unfortunately, other than a comment in a review article, further evidence to support this analysis has not been published. The article did describe other novel tests that are under investigation to facilitate the diagnosis of OSA [20]. Another option was limited PSG or cardiorespiratory study [18]. Limited PSG does not include EEG, eye leads, or chin tone. Unless EEG recordings are used, one will not be able to
identify all types of hypopneas (Fig. 2). Limited PSG may underestimate the OAHI. Figure 3 is an example of a scorable hypopnea without EEG recordings due to a 3% oxygen desaturation. The McGill group has been pioneer in investigating the role of overnight oximetry in detecting OSA. They have shown that overnight oximetry has a high positive predictive value to detect moderateto-severe OSA. However, a negative study does not exclude OSA. One can have obstructive respiratory events without oxygen desaturations (Fig. 4). A recent study demonstrated excellent night-to-night consistency using nocturnal pulse oximetry [21].
CONTRARIAN VIEW A contrarian view recommends against the routine use of PSG. One should only request a test if the results are going to influence management decisions. Many clinicians view AHI as the primary outcome measure for PSG. Historically, the severity of OSA has not always been predictive of morbidity. Children with primary snoring have been diagnosed with daytime sleepiness, behavioral problems, hypertension, and cognitive delays. Jackman et al. [22] demonstrated that children not only with OSA but also those with primary snoring were identified with behavioral issues. If future research continues to demonstrate that primary snoring is no longer benign, one of the major indications for PSG will become moot.
(a)
(b)
FIGURE 6. (a) Normal CO2 value with a good waveform. (b) Low CO2 value that may be an underestimate as the waveform is peaked. 564
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Limitations of polysomnography Even if the OAHI severity could reliably predict behavioral and neurocognitive morbidity, technical factors can influence PSG outcomes. Chervin et al. [23] demonstrated that esophageal pressure monitoring was more reliable in predicting morbidity and treatment outcomes than the AHI index. Neither esophageal monitoring nor AHI had a robust ability to predict baseline morbidity or treatment outcomes [23]. Few centers use esophageal pressure monitoring. During PSG acquisition, filter and sensor selection may alter the respiratory indices. A nasal pressure cannula is a quantitative sensor and can detect more subtle respiratory events. Without a functional nasal pressure cannula, the severity of OSA may be underestimated (Fig. 5a and b). A disadvantage of the nasal pressure
sensor is that it does not measure oral airflow, which is why more than one flow sensor should be used for PSG acquisitions. Carbon dioxide (CO2) sensors are also important for detecting disrupted breathing patterns for children. Many children, rather than having discrete respiratory events, have prolonged periods of partial obstruction, which are detected by CO2 monitoring. For end-tidal CO2 monitoring, an accurate number depends upon a high-quality signal with a square waveform. One could have a normal end-tidal CO2 distribution, but if the signal is ‘peaked’, the CO2 value is erroneously low (Fig. 6a and b) [24]. PSG outcomes may also be affected by the scoring criteria and terminology of the individual sleep laboratory. Some laboratories provide separate indices for central and obstructive respiratory
FIGURE 7. Example of flow limitation with flattening of the nasal pressure. 1068-9508 ß 2013 Wolters Kluwer Health | Lippincott Williams & Wilkins
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events, whereas others lump all the respiratory events together as an AHI. Apart from apneas and hypopneas, there is a more subtle respiratory event known as a respiratory effort-related arousal (RERA). A RERA is scored when there is a drop in airflow (flow limitation) that does not meet the definition of a hypopnea, but an arousal occurs. The standard definition of an RDI includes all apneas, hypopneas, and RERAS. To detect flow limitation, the appropriate filter settings must be selected (Fig. 7) [24].
CONCLUSION PSG is a useful test and is the gold standard to diagnose OSA, but does have its limitations. If a child has disrupted breathing patterns at night and PSG has not been performed, one should use the diagnosis of SDB. Without PSG, one cannot diagnose OSA. As research continues on the disrupted breathing patterns in children, the evidence will mandate revisions of the current clinical guidelines. Acknowledgements The author would like to thank Amanda Ruiz for her help in putting together this study. Conflicts of interest The author has no conflicts of interest and there are no sources of funding.
REFERENCES AND RECOMMENDED READING Papers of particular interest, published within the annual period of review, have been highlighted as: & of special interest && of outstanding interest 1. Marcus CL, Brooks LJ, Draper KA, et al. Diagnosis and management of childhood obstructive sleep apnea syndrome. Pediatrics 2012; 130:576– 584. doi: 10.1542/peds.2012-1671. Revised clinical practice guideline published by the AAP to provide recommendations for the diagnosis and management of the OSA syndrome, specifically for primary care clinicians. 2. Roland PS, Rosenfeld RM, Brooks LJ, et al. Clinical practice guideline: polysomnography for sleep-disordered breathing prior to tonsillectomy in children. Otolaryngol Head Neck Surg 2011; 145 (1 Suppl):S1–S15. doi:10.1177/0194599811409837. 3. Aurora RN, Zak RS, Karippot A, et al., American Academy of Sleep Medicine. Practice parameters for the respiratory indications for polysomnography in children. Sleep 2011; 34:379–388. 4. Marcus CL, Brooks LJ, Draper KA, et al. Diagnosis and management of && childhood obstructive sleep apnea syndrome. Pediatrics 2012; 130:e714– e755. doi: 10.1542/peds.2012-1672. A comprehensive literature review that accompanies the AAP clinical practice guideline. &&
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5. Bull MJ. Clinical report: health supervision for children with Down syndrome. Pediatrics 2011; 128:393–406. 6. Deal CL, Tony M, Ho¨ybye C, et al., 2011 Growth Hormone in Prader-Willi Syndrome Clinical Care Guidelines Workshop Participants. Growth Hormone Research Society workshop summary: consensus guidelines for recombinant human growth hormone therapy in Prader-Willi syndrome. J Clin Endocrinol Metab 2013; 98:E1072–E1087. doi: 10.1210/jc.2012-3888. 7. Jain SV, Horn PS, Simakajornboon N, Glauser TA. Obstructive sleep apnea and primary snoring in children with epilepsy. J Child Neurol 2013; 28:77–82. doi: 10.1177/0883073812440326. 8. Friedman NR, Perkins JN, McNair B, Mitchell RB. Current practice patterns for & sleep-disordered breathing in children. Laryngoscope 2013; 123:1055– 1058. doi: 10.1002/lary.23709. An internet-based survey to pediatric otolaryngologists to determine how they manage children with SDB. 9. Kaditis A, Kheirandish-Gozal L, Gozal D. Algorithm for the diagnosis and treatment of pediatric OSA: a proposal of two pediatric sleep centers. Sleep Med 2012; 13:217–227. doi: 10.1016/j.sleep.2011.09.009. 10. Aurora RN, Lamm CI, Zak RS, et al. Practice parameters for the nonrespiratory indications for polysomnography and multiple sleep latency testing for children. Sleep 2012; 35:1467–1473. doi: 10.5665/sleep.2190. 11. Kotagal S, Nichols CD, Grigg-Damberger MM, et al. Nonrespiratory indications for polysomnography and related procedures in children: an evidencebased review. Sleep 2012; 35:1451–1466. doi: 10.5665/sleep.2188. 12. Spruyt K, Gozal D. Screening of pediatric sleep-disordered breathing: a proposed unbiased discriminative set of questions using clinical severity scales. Chest 2012; 142:1508–1515. doi: 10.1378/chest.11-3164. 13. Goldstein NA, Stefanov DG, Graw-Panzer KD, et al. Validation of a clinical assessment score for pediatric sleep-disordered breathing. Laryngoscope 2012; 122:2096–2104. doi: 10.1002/lary.23455. 14. Certal V, Catumbela E, Winck JC, et al. Clinical assessment of pediatric obstructive sleep apnea: a systematic review and meta-analysis. Laryngoscope 2012; 122:2105–2114. doi: 10.1002/lary.23465. 15. Walter LM, Nisbet LC, Nixon GM, et al. Seasonal variability in paediatric obstructive sleep apnoea. Arch Dis Child 2013; 98:208–210. doi: 10.1136/ archdischild-2012-302599. 16. Bhattacharjee R, Kheirandish-Gozal L, Spruyt K, et al. Adenotonsillectomy outcomes in treatment of obstructive sleep apnea in children: a multicenter retrospective study. Am J Respir Crit Care Med 2010; 182:676–683. doi: 10.1164/rccm.200912-1930OC. 17. Marcus CL, Moore RH, Rosen CL, et al., Childhood Adenotonsillectomy Trial && (CHAT). A randomized trial of adenotonsillectomy for childhood sleep apnea. N Engl J Med 2013; 368:2366–2376. doi: 10.1056/NEJMoa1215881. A randomized controlled trial of children with OSA but normal oxygenation that compared early adenotonsillectomy to watchful waiting to determine whether earlier treatment would have better neuropsychological outcomes. 18. Brockmann PE, Schaefer C, Poets S, et al. Diagnosis of obstructive sleep apnea in children: a systematic review. Sleep Med Rev 2013; 17:331–340. 19. Gozal D, Jortani S, Snow AB, et al. Two-dimensional differential in-gel electrophoresis proteomic approaches reveal urine candidate biomarkers in pediatric obstructive sleep apnea. Am J Respir Crit Care Med 2009; 180:1253–1261. doi: 10.1164/rccm.200905-0765OC. 20. Gozal D. Serum, urine, and breath-related biomarkers in the diagnosis of obstructive sleep apnea in children: is it for real? Curr Opin Pulm Med 2012; 18:561–567. doi: 10.1097/MCP.0b013e328358be2d. 21. Pavone M, Cutrera R, Verrillo E, et al. Night-to-night consistency of at-home nocturnal pulse oximetry testing for obstructive sleep apnea in children. Pediatr Pulmonol 2013; 48:754–760. doi: 10.1002/ppul.22685. 22. Jackman AR, Biggs SN, Walter LM, et al. Sleep-disordered breathing in preschool children is associated with behavioral, but not cognitive, impairments. Sleep Med 2012; 13:621–631. doi: 10.1016/j.sleep.2012.01.013. 23. Chervin RD, Ruzicka DL, Hoban TF, et al. Esophageal pressures, polysomnography, and neurobehavioral outcomes of adenotonsillectomy in children. Chest 2012; 142:101–110. doi: 10.1378/chest.11-2456. 24. Berry RB, Budhiraja R, Gottlieb DJ, et al., American Academy of Sleep Medicine. Rules for scoring respiratory events in sleep: update of the 2007 AASM Manual for the Scoring of Sleep and Associated Events. Deliberations of the Sleep Apnea Definitions Task Force of the American Academy of Sleep Medicine. J Clin Sleep Med 2012; 8:597–619. doi: 10.5664/jcsm.2172.
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