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Interpretation of the Polysomnogram in Children
Otolaryngol Clin N Am 40 (2007) 745–759
Interpretation of the Polysomnogram in Children Mary H. Wagner, MD*, Daniel M. Torrez, MD Department of Pediatrics, Division of Pediatric Pulmonary, University of Florida, 1600 SW Archer Road, Gainesville, FL 32610, USA
Polysomnography (PSG) is important in the evaluation of nocturnal events in children as well as adults. Events that can be evaluated include obstructive sleep apnea syndrome (OSAS), periodic leg movements (PLM), nocturnal seizures, parasomnias, and issues related to nocturnal gas exchange. This article discusses the use of PSG primarily in terms of respiratory events, leg movements, and gas exchange problems in children. PSG has been recommended to evaluate several conditions in children, including [1]
Differentiation of benign from pathologic snoring Disrupted sleep Excessive daytime sleepiness Unexplained failure to thrive Cor pulmonale Polycythemia Laryngomalacia in children when worsened with sleep Underlying disorders predisposing children to nocturnal hypoxemia or hypoventilation, such as bronchopulmonary dysplasia, cystic fibrosis, neuromuscular disorders (muscular dystrophy, spinal muscular atrophy, cerebral palsy, or congenital muscle diseases) Suspected alveolar hypoventilation Confirmation of clinical diagnosis of airway obstruction suggested by symptoms including apnea, paradoxical respirations, or increased work of breathing Documentation of severity of obstructed breathing to guide therapeutic intervention and identification of those at increased risk of postoperative complications * Corresponding author. E-mail address: [email protected] (M.H. Wagner). 0030-6665/07/$ - see front matter Ó 2007 Published by Elsevier Inc. doi:10.1016/j.otc.2007.04.004
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Titration of positive pressure for medical treatment of OSAS Follow-up evaluation of children who have persistent symptoms postintervention for OSAS Sleep disordered breathing (SDB) is a common cause of morbidity in childhood, with a spectrum ranging from benign snoring to complete airway obstruction. Benign or primary snoring is reported in 3% to 12% of the pediatric population, with OSAS affecting 1% to 3% [2]. Several authors have demonstrated that clinical history and physical examination are not accurate in the identification of children who have OSAS [3]. PSG is useful in documenting the presence of obstructive sleep apnea (OSA) events as well as their severity. PSG has been recommended as the test of choice to evaluate SDB by consensus of a panel of experts [4]. PSG has also shown to be useful in determining readiness for decannulation in children who have tracheostomy [5]. Performance of polysomnography in children PSG should be performed by a laboratory experienced in and comfortable with caring for children [1]. Technicians need to be experienced in dealing with children of various age levels and developmental status. Personnel should be certified in pediatric cardiopulmonary resuscitation. If a dedicated pediatric facility is not available, an area in the adult sleep laboratory should be designated for children. Children should be housed in an appropriate environment, with accommodations for a caregiver to sleep near the child. Caregiver availability to the child is important to minimize the child’s anxiety or fears about the study, as well as to provide any necessary care. The procedure should be explained to the child and the family by personnel skilled in the presentation of medical information. A crib should be available for small children. The person responsible for supervision of the pediatric sleep facility or functions should be a pediatrician with training and expertise in the area of sleep medicine. This person must assure that the PSG performance, scoring, and interpretation are appropriate for the age and condition of the child. The study timing should be set to mimic the child’s bedtime as closely as possible. Overnight studies are preferred because negative nap studies have been shown not to exclude the possibility of OSAS during a night study [6]. Studies should be performed without sedation in order to most accurately mimic the child’s normal sleep. Components of polysomnography in children Variables gathered during PSG in children are similar to those obtained in adults, with some additional information. Children may often demonstrate obstructive hypoventilation as a component of their OSAS, which
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may only be detected by increased carbon dioxide (CO2) levels [7]. Thus, PSG monitoring in children should include some method of determining CO2 levels, such as end tidal CO2 or transcutaneous CO2 [8]. The many channels of physiologic parameters and their purpose in the PSG are described in the following sections [1]. Sleep stages are determined using electroencephalogram (EEG), chin electromyogram (EMG), and electro-oculogram (EOG). EEG monitoring includes two central and two occipital leads with references to the opposite posterior auricular area. Additional EEG leads can be used to detect nocturnal events such as seizure activity. Three chin EMG leads are placed and used to detect skeletal muscle activity as required for the identification of rapid eye movement (REM) sleep. The chin EMG is also useful to detect swallowing and sucking during the study. Right and left EOG leads are used to detect eye movements essential to the identification of REM sleep. Respiratory effort is detected using chest and abdominal belts. Different styles of monitoring include strain gauges, chest wall impedance, inductance plethysmography, intercostal EMG, and pneumatic transducers [9]. These belts can assess qualitative respiratory effort, which is essential to distinguishing whether respiratory events are central or obstructive in origin. Air entry is assessed using a thermistor, nasal pressure, and a capnograph tracing. The thermistor detects airflow at the nose and mouth by detecting a temperature change in expired gas. Nasal pressure is an additional method of monitoring airflow by detecting pressure changes via a cannula placed in the nose. A recent study showed that the nasal pressure transducer is more sensitive in the detection of hypopnea, and suggested combining the use of both the thermistor and nasal pressure transducer for optimal detection of SDB in children [10]. During positive pressure titrations, flow is detected using measurements from the positive pressure device. Movements of extremities are monitored by EMG leads placed on the legs and sometimes on the arms. These movements are important in documenting PLM as well as movements that result from respiratory events. Position sensors can be used to document patient position. Digital video is also obtained. The video is useful in documenting patient position, movements, and unusual episodes such as parasomnias. Snoring is assessed by a snore microphone placed on the neck of the patient, by technician observation, and by audio recording. Gas exchange is assessed using monitoring for both oxygen and CO2. Oxygenation is monitored by pulse oximetry, using a comfortable sensor that can be left on the child for the duration of the study. It is essential that the pulse oximeter have a short sampling time (2 to 3 seconds) to avoid missing brief desaturations associated with events in children. The reliability of the pulse oximeter tracing is improved with recording of the pulse amplitude signal, allowing identification of desaturation events that are caused by poor probe function [11]. Ventilation is monitored in children by either end tidal (ET) CO2 or transcutaneous CO2 monitoring. The ET CO2 method is
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more responsive to rapid changes, whereas the transcutaneous method is not reflective of transient CO2 changes, and is most useful for a trend [8,12]. ET CO2 is monitored by a probe placed at the nose and mouth. ET CO2 generates a flow tracing that can also be used to monitor airflow. The sensor for the transcutaneous device must be changed every several hours to maintain accuracy. In patients with persistent gas exchange abnormalities, access to arterial blood gas measurement is useful in corroborating noninvasive monitoring of gas exchange. This can be useful in a patient who has alveolar hypoventilation, to accurately assess the extent of CO2 retention, or in a patient who has sickle cell disease with abnormal hemoglobin, in whom the pulse oximetry may not accurately reflect arterial oxygen level [13].
Begin the review It is helpful to preview the physician note/orders before the study to determine why the PSG is being performed. This will help ensure that the question being posed by the ordering physician will be appropriately addressed. For example, if a child is being studied to determine whether he/she can tolerate having his/her tracheostomy tube capped, it is important to make certain the child has the capping device, and that the technicians know that the tracheostomy is to be capped during the study. Before beginning review of the study, it is helpful to review any notes made by the technician during the course of the night. This alerts the physician to technical or patient issues encountered over the course of the study. These issues might include unusual events over the night, such as confusional arousals or artifactual desaturation related to patient compromise of the oximeter probe. In general, polysomnograms (PSGs) should be reviewed and scored by an experienced scoring technician before interpretation; however, all PSGs should be examined page by page by the reviewing professional for the most accurate interpretation of the nocturnal events. First, the biocalibration should be evaluated. This is a series of tests conducted by the technician at the beginning and end of the study to document the normal function of the various channels of information recorded. The biocalibration may be limited in children who are young, developmentally delayed, or uncooperative. The components of the biocalibration include having the patient look up, down, and to both sides in order to assess detection of eye movements by EOG, which facilitates scoring of REM sleep. The EEG is evaluated with eyes open and closed in order to identify alpha EEG waves, which aid in detection of wakefulness. The patient is asked to make a snoring type noise to check the snore channel, and the patient is asked to grit his/her teeth to detect bruxism. The patient moves both legs separately to assess the integrity of the leg EMGs. The patient is asked to hold his/her breath to detect cessation of chest wall movement, and the chest and abdomen belts are tested to make certain they move together with respiratory effort.
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Sleep stage analysis It is helpful to quickly review the patient’s sleep architecture by viewing the hypnogram (Fig. 1). A hypnogram is a summary of the different sleep stages achieved shown in graphic form. It is important to review the sleep architecture in terms of what is to be expected for the patient’s age. Timing and length of various sleep stages vary with patient age, and should be compared with age-expected norms. For example, although it is normal for infants to enter sleep through stage REM, entering sleep through stage REM may suggest an underlying sleep disorder such as narcolepsy in an older child or adolescent. Components of sleep architecture that should be assessed include: percentage of total sleep time (TST) spent in stage I/II, stage III/IV, stage REM, and wakefulness. These percentages should be compared with ageappropriate normals. Several authors have examined sleep architecture in normal children ages 1 to 15 years [14–18]. In these studies, stage I sleep occupied 4% to 7.7% of TST, and stage II occupied 36% to 49% of TST, with the combination of stage I and II in each study ranging from 41% to 53% of the TST. Slow wave sleep (combining stages III and IV) occupied 14% to 32% of the TST, whereas stage REM occupied 17.4% to 21.1% of the TST.
Fig. 1. This is a typical hypnogram showing time across the bottom axis. The left axis shows the different sleep stages. The horizontal bars indicate the time spent in the various sleep stages during the course of the PSG.
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Timing of sleep stages can be noted by review of the hypnogram. Children usually have a short period of stage I/II after sleep onset, and then enter stage III/IV (also known as delta or slow wave sleep). Stage III/IV sleep will predominate early in the night, with regular cycling between the stages I/II, stages III/IV, and REM. REM sleep will usually cycle every 60 to 120 minutes, with a wide range of timing between REM periods [14]. Sleep latency, the time after lights out until sleep is achieved, should also be noted. Sleep latency is generally less than 25 minutes [14,16]. It may be prolonged if the child has recently had a nap, and it may be shortened in certain sleep disorders. Sleep efficiency is a measurement of the amount of the total time in bed that the patient spends asleep, and should also be noted. It gives a picture of whether the patient has a disrupted sleep pattern. Sleep efficiency in children is usually greater than 89% [14–18]. REM latency, the time from onset of sleep to the first epoch of REM sleep, is also noted. REM latency can be prolonged if the first REM period is difficult to detect by the scoring technician. REM latency can be shortened in certain conditions, such as depression or narcolepsy. The presence and amount of REM sleep deserves careful attention. Length of time spent in REM is short earlier in the night, with lengthening of REM episodes as the night progresses [14]. During REM sleep, OSA may be worsened because of loss of muscle tone. Thus, to make certain the most severe extent of OSA is observed, patients should achieve REM sleep. REM sleep may be decreased if the patient has a disrupted sleep pattern, with arousals out of REM caused by obstructive events. This may cause the overall number of obstructive events to be lowered. EEG should be monitored for unusual complexes, such as nocturnal epileptiform discharges (Fig. 2). These may be noted in children who have a history of a seizure disorder as well as in those who do not have such a history. Whether these episodes are associated with clinical seizure activity or respiratory events should be noted. Technician observation and the video should be reviewed for evidence of clinical seizure activity in association with these EEG changes. Consideration may be given to a more thorough evaluation by a full sleep-deprived EEG if complexes are widespread during the recording. Arousal summary Arousals are scored by the scoring technician based on the appearance of the EEG tracing. An arousal is scored when there is an abrupt change in the EEG lasting 3 seconds, following at least 10 seconds of continuous sleep [19]. Arousals can be attributed to preceding events, including respiratory events, leg movements, snore events, or technician presence in the room, or may occur without an obvious trigger. Arousals are reported using the arousal index, which is the number of arousals divided by the hours of sleep. Normal values for arousal indices vary from laboratory to laboratory.
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Fig. 2. Shown here is an episode of spike and wave activity occurring out of stage II sleep. The tracing shows the EEG leads on the left axis with time on the bottom axis. A 10-second duration screen is shown, with each rectangle along the bottom axis representing 1 second.
Studies of normal children have found mean arousal indices of 8.8 to 9.5 [14,15,17]. Arousals attributed to respiratory events give a measure of sleep disruption caused by those respiratory events. It is also important to note that children may not arouse to respiratory events as easily as adults do [7].
Heart rate/rhythm The ECG should be reviewed for evidence of brady or tachy rhythms as well as abnormal ECG rhythms. Respiratory events may be associated with decrease in heart rate, with subsequent increase in heart rate after the event has resolved, or in association with arousals. Some patients will have evidence of premature ventricular or atrial contractions, which may or may not be related to respiratory events.
Snoring Determination of the presence or absence of snoring is important to note, particularly in comparison to what is observed in the home environment. If a child has loud snoring over the course of the night, typical to what parents describe at home, with few documented respiratory events, a diagnosis of
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primary snoring may be made. This may be reassuring to family members, in that the snoring they have noted at home is not associated with documented respiratory events or gas exchange abnormalities; however, there are reports in the literature that snoring without respiratory events has been associated with poor academic performance [20,21]. Leg movements The scoring technician will score leg movements that meet criteria for PLM. Criteria for PLM include leg movements noted in either or both legs that are at least one quarter of the amplitude noted during the biocalibration lasting from 0.5 to 5 seconds. Leg movements must be separated by at least 5 seconds, but not more than 90 seconds, and must occur in clusters of at least four to be considered PLM (Fig. 3). These leg movements should not be related to other events, such as respiratory events or arousals [22]. Leg movements should be carefully reviewed to make certain they meet criteria for PLM and are not related to subtle respiratory events. The total number of PLM that meet these criteria are determined, and the PLM index is calculated by dividing the total number of PLM by the number of hours of sleep. A PLM index of five or greater is considered abnormal [22,23].
Fig. 3. This tracing shows a series of four periodic leg movements occurring over a time span of 2.5 minutes. The PLM are apparent as deflections in the two leg channels. LAT refers to left anterior tibialis and RAT refers to right anterior tibialis. These leg movements are not associated with respiratory events or arousals.
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Respiratory events Several definitions are important for the classification of respiratory events. The term ‘‘apnea’’ refers to an event with no flow. Apneas are scored for events with a decrease in flow by 75% or greater from the baseline flow observed before the event. If any portion of an event fits this definition, the event can be scored as an apnea. Hypopnea refers to a decrease in flow by 30% to 50% from the usual baseline. Apneas and hypopneas can be further classified as being central, obstructive, or mixed in nature. Obstructive events are those caused by a decrease in flow associated with persistent, sometimes increased respiratory effort noted in the chest and abdominal belts. Obstructive apneas are scored when a decrease of 75% or greater is detected in the airflow or nasal pressure channels associated with continued respiratory effort (Fig. 4) [24]. Whereas in adults there is a 10-second minimum event length noted, in children the events must be two respiratory cycles [25]. Thus, in an infant breathing at 60 times per minute, a significant event can be as brief as 2 seconds. An obstructive hypopnea is scored when a decrease in the flow channel of 30% to 50% is noted with persistent respiratory effort (Fig. 5) [1,25]. In order for an obstructive hypopnea to be scored, there must be some consequence to the event, including a 3% to 4% drop in oxygen saturation, a leg movement, or an EEG arousal.
Fig. 4. This figure demonstrates two episodes of obstructive apnea shown by cessation of flow in the nasal pressure and airflow channels with continued respiratory effort. The events result in oxygen desaturation as low as 80%.
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Fig. 5. An episode of obstructive hypopnea is shown here, depicting two epochs or 1 minute of a PSG. The event is marked by a decrease in the nasal pressure and airflow with continued respiratory effort. The hypopnea results in a drop in oxygen saturation to 94% and an EEG arousal.
The contour of the nasal pressure tracing is often flattened, indicating flow limitation with respiratory effort during obstructive hypopneas [26]. Central events are those caused by an absence or severe decrease in respiratory effort, as measured by chest or abdominal belts. Central apneas (Fig. 6) are scored when there is an absence of respiratory effort associated with a 70% or greater decrease in the airflow or nasal pressure. During central apneas, there may be small deflections noted in the chest tracing corresponding to cardioblastic artifact from chest wall movement associated with cardiac activity. Central hypopneas (Fig. 7) are events with decreased respiratory effort associated with a 30% to 50% decrease in the airflow or nasal pressure channels and desaturation or EEG arousal. The contour of the nasal pressure tracing will be rounded during central hypopneas, compared with the flattened contour noted with obstructive hypopneas [26]. It is important to be certain that central hypopneas are not confused with obstructive hypopneas. Obstructive hypopneas may appear to be associated with an apparent decrease in respiratory effort caused by work against an obstructed upper airway [26]. Central events are more likely to be noted during REM sleep, particularly in patients who have underlying disorders such as Prader-Willi syndrome or Arnold-Chiari malformation. Mixed
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Fig. 6. This tracing demonstrates a central apnea lasting 11.5 seconds, resulting in a drop in oxygen saturation to 91% and an EEG arousal. During this event there is cessation of airflow with lack of respiratory effort.
respiratory events are those with a central and obstructive component. Usually, these events begin with the central component, then progress to an obstructed component with the resumption of respiratory effort. After all events are reviewed and scored, several indices can be calculated. These include apnea index (AI) and apnea-hypopnea index (AHI) which are calculated for the entire sleep period, for non-REM (NREM) and REM sleep. The term ‘‘index’’ refers to the number of events divided by the number of hours of sleep. This calculation allows the comparison of PSGs of various lengths. The AI is determined using only apneas; the AHI includes apneas and hypopneas. Studies of normal children suggest that any obstruction is abnormal, and that normal values for children are different from those for adults. Several authors have investigated PSG findings in normal children [14,15,17]. There is general agreement that AI and AHI are less than 1 in normal children. Katz and Marcus [2] have suggested the following values for classification of respiratory events in children:
AHI AHI AHI AHI
less than 1 ¼ normal 1 through 4 ¼ mild OSA 5 through 10 ¼ moderate OSA greater than 10 ¼ severe OSA
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Fig. 7. This tracing demonstrates a 2-minute window in REM sleep with two episodes of central hypopnea. These events are marked by a decrease of at least 30% in the airflow channel, with a concomitant decrease in respiratory effort in the chest and abdomen channels. These events result in significant oxygen desaturation as low as 78% and increase in ETCO2 to 53 torr.
They also propose grading of disease severity by gas exchange parameters. The AHI should be considered in the context of the patient’s presentation. Children who have complications of OSAS or underlying medical problems may require intervention for mild OSA in order to prevent worsening of their medical disorder or worsened complications. For example, children who have pulmonary hypertension might require aggressive intervention, despite mild OSA, to prevent worsening of their pulmonary hypertension. Gas exchange Gas exchange should be reviewed carefully for the entire tracing. The pulse oximetry tracing should be reviewed for desaturation, with careful attention to whether the desaturation is associated with a respiratory event, arousal, or leg movement. Desaturations might be caused by respiratory events of any duration. The actual desaturation will occur 1 to several seconds after the respiratory event. If the respiratory event is prolonged, the desaturation may begin before the event has terminated. Desaturations unassociated with respiratory events should be reviewed for accuracy in
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terms of whether the pulse oximeter is tracing accurately, or whether the pulse oximetry probe has been compromised by patient position. It is important to note the baseline oxygen saturation before study onset. Patients who have low saturation at baseline may be at risk for desaturation with sleep onset, worsening with respiratory events. Those who have persistent oxygen desaturation without respiratory events potentially require further investigation for underlying lung disease, hypoventilation, or abnormal hemoglobin (ie, sickle cell disease). Hypoventilation can be evaluated by noting the CO2 associated with episodes of oxygen desaturation. In general, oxygen saturation should be greater than 92% in normal studies [14,15,17,18,27]. Children on oxygen supplementation should have their flow rate recorded at the beginning of the study, with monitoring of response to changes in the oxygen flow rate over the course of the study. CO2 tracing should be reviewed as well. Baseline CO2 level before sleep onset should be noted. Normal children can be expected to have a 5 to 7 torr rise in CO2 with sleep onset [27]. Children may have a pattern of obstructive hypoventilation with OSAS, resulting in increases in CO2 without significant oxygen desaturation. Abnormal levels of CO2 vary, with Marcus and colleagues [27] reporting greater than 10% of TST being spent with CO2 greater than 50 torr as abnormal, and Montgomery-Downs and colleagues [14] reporting that in normal children, 2.8 11.3 of the TST was spent with a CO2 greater than or equal to 50 torr. Marcus and colleagues [27] also report CO2 levels of greater than 53 torr as being abnormal. Uliel and colleagues [18] found less time spent with CO2 greater than 45 torr in their study of normal children, suggesting that ET CO2 greater than 45 torr for greater than 10% of the TST, or any CO2 greater than 50 torr, is abnormal. It is important to recognize potential issues associated with ETCO2 monitoring. Sampling tubing can become obstructed with nasal secretions or moisture, and may become displaced. Other factors that affect the accuracy of the ETCO2 readings include mouth breathing, airway obstruction, supplemental oxygen delivery at the other nostril, and cyanotic heart disease [28–30]. It is important to know the values obtained in your individual sleep laboratory, and compare values during the study with the baseline values. CO2 trends may be more helpful, with consideration given to obtaining a blood gas for high values to determine the accuracy of noninvasive measurements.
Summary PSG in children represents an important and useful tool in the evaluation of the multitude of sleep-related conditions, including OSAS, PLM disorder, and those with an underlying predisposition toward gas exchange aberrancies. To obtain the most useful information, sleep studies in this unique population should be performed in laboratories with staff experienced in
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working with children of all ages and stages of development, in a setting sensitive to both child and caregiver. In performing pediatric PSG, physicians should keep in mind PSG can be successfully performed in children. Pediatric PSG should be performed in a laboratory experienced in and comfortable with the care of children. Recognize that PSG in children includes measurement of carbon dioxide levels to detect obstructive or central hypoventilation. Criteria for scoring and interpretation of PSG in children differ from those for adults.
References [1] Standards and indications for cardiopulmonary sleep studies in children. Am J Respir Crit Care Med 1996;153:866–78. [2] Katz ES, Marcus CL. Diagnosis of obstructive sleep apnea syndrome in infants and children. In: Sheldon SH, Ferber R, Kryger MH, editors. Principles and practice of pediatric sleep medicine. USA: Elsevier Saunders; 2005. p. 197–210. [3] Brietzke SE, Katz ES, Roberson DW. Can history and physical examination reliably diagnose pediatric obstructive sleep apnea/hypopnea syndrome? A systematic review of the literature. Otolaryngol Head Neck Surg 2004;131(6):827–32. [4] American Academy of pediatrics, Section on Pediatric Pulmonology, Subcommittee on Obstructive Sleep Apnea. Clinical practice guideline: diagnosis and management of childhood obstructive sleep apnea syndrome. Pediatrics 2002;109:704–12. [5] Tunkel DE, McColley SA, Baroody FM, et al. Polysomnography in the evaluation of readiness for decannulation in children. Arch Otolaryngol Head Neck Surg 1996;122(7):721–4. [6] Marcus CL, Keens TG, Ward SL. Comparison of nap and overnight polysomnography in children. Pediatr Pulmonol 1992;13:16–21. [7] Rosen CL, D’Andrea L, Haddad GG. Adult criteria for obstructive sleep apnea do not identify children with serious obstruction. Am Rev Respir Dis 1992;146:1231–4. [8] Morielli A, Desjardins D, Brouillette RT. Transcutaneous and end-tidal carbon dioxide pressures should be measured during pediatric polysomnography. Am Rev Respir Dis 1993; 148:1599–604. [9] Krishna J, Sans-Capdevila O, Gozal D. Sleep studies: which technologies? Paediatr Respir Rev 2006;7(Suppl 1):S202–5. [10] Budhiraja R, Goodwin JL, Parthasarathy S, et al. Comparison of nasal pressure transducer and thermistor for detection of respiratory events during polysomnography in children. Sleep 2005;28(9):1117–21. [11] Lafontaine V, Ducharme FM, Brouillette RT. Can we rely on pulse oximetry desaturation events? [abstract] Am Rev Respir Dis 1994;149:69A. [12] Hansen TN, Tooley WH. Skin surface carbon dioxide tension in sick infants. Pediatrics 1979; 64:942–5. [13] Craft JA, Alessandrini E, Kenney LB, et al. Comparison of oxygenation measurements in pediatric patients during sickle cell crises. J Pediatr 1994;124:93–5. [14] Montgomery-Downs HE, O’Brien LM, Gulliver TE, et al. Polysomnographic characteristics in normal preschool and early school-aged children. Pediatrics 2006;117:741–53. [15] Wong TK, Galster P, Lau TS, et al. Reliability of scoring arousals in normal children and children with obstructive sleep apnea syndrome. Sleep 2004;27:1139–45.
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[16] Coble PA, Kupfer DJ, Taska LS, et al. EEG sleep or normal health children. Part I: findings using standard measurement methods. Sleep 1984;7:289–303. [17] Traeger N, Schultz B, Pollock AN, et al. Polysomnographic values in children 2–9 years old: additional data and review of the literature. Pediatr Pulmonol 2005;40:22–30. [18] Uliel S, Tauman R, Greenfeld M, et al. Normal polysomnographic respiratory values in children and adolescents. Chest 2004;125:872–8. [19] American Sleep Disorders AssociationdThe Atlas Task Force. EEG arousals: scoring rules and examples. Sleep 1992;15:174–84. [20] Gozal D, Pope DW. Snoring during early childhood and academic performance at ages thirteen to fourteen years. Pediatrics 2001;107(6):1394–9. [21] Urschitz MS, Guenther A, Eggebrecht E, et al. Snoring, intermittent hypoxia and academic performance in primary school children. Am J Respir Crit Care Med 2003;168(4):464–8. [22] American Academy of Sleep Medicine. International classification of sleep disorders. 2nd edition. Diagnostic and coding manual. Westchester (IL): American Academy of Sleep Medicine; 2005. p. 182–6. [23] Picchietti DL, Walters AS. Moderate to severe periodic limb movement disorder in childhood and adolescence. Sleep 1999;22(3):297–300. [24] Phillips B, Kryger MH. Management of obstructive sleep apnea-hypopnea syndrome: overview. In: Kryger MH, Roth T, Dement WC, editors. Principles and practice of sleep medicine. 4th edition. USA: Elsevier Saunders; 2005. p. 1111–3. [25] Kheirandish-Gozal L. Practical aspects of scoring sleep in children. Paediatr Respir Rev 2006;7(S1):S50–4. [26] Berry RB. Monitoring respiration during sleep. In: Sleep medicine pearls. 2nd edition. Philadelphia: Hanley and Belfus, Inc.; 2003. p. 84–5. [27] Marcus CL, Omlin KJ, Basinki DJ, et al. Normal polysomnographic values for children and adolescents. Am Rev Respir Dis 1992;146:1235–9. [28] Tobias JD, Meyer DJ. Noninvasive monitoring of carbon dioxide during respiratory failure in toddlers and infants: end-tidal versus transcutaneous carbon dioxide. Anesth Analg 1997; 85:55–8. [29] Friesen RH, Alswang M. End-tidal pCO2 monitoring via nasal cannulae in pediatric patients: accuracy and sources of error. J Clin Monit 1996;12:155–9. [30] Fukuda K, Ichinohe T, Kaneko Y. Is measurement of end-tidal CO2 through a nasal cannula reliable? Anesth Prog 1997;44:23–6.
Interpretation of the Polysomnogram in Children Mary H. Wagner, MD*, Daniel M. Torrez, MD Department of Pediatrics, Division of Pediatric Pulmonary, University of Florida, 1600 SW Archer Road, Gainesville, FL 32610, USA
Polysomnography (PSG) is important in the evaluation of nocturnal events in children as well as adults. Events that can be evaluated include obstructive sleep apnea syndrome (OSAS), periodic leg movements (PLM), nocturnal seizures, parasomnias, and issues related to nocturnal gas exchange. This article discusses the use of PSG primarily in terms of respiratory events, leg movements, and gas exchange problems in children. PSG has been recommended to evaluate several conditions in children, including [1]
Differentiation of benign from pathologic snoring Disrupted sleep Excessive daytime sleepiness Unexplained failure to thrive Cor pulmonale Polycythemia Laryngomalacia in children when worsened with sleep Underlying disorders predisposing children to nocturnal hypoxemia or hypoventilation, such as bronchopulmonary dysplasia, cystic fibrosis, neuromuscular disorders (muscular dystrophy, spinal muscular atrophy, cerebral palsy, or congenital muscle diseases) Suspected alveolar hypoventilation Confirmation of clinical diagnosis of airway obstruction suggested by symptoms including apnea, paradoxical respirations, or increased work of breathing Documentation of severity of obstructed breathing to guide therapeutic intervention and identification of those at increased risk of postoperative complications * Corresponding author. E-mail address: [email protected] (M.H. Wagner). 0030-6665/07/$ - see front matter Ó 2007 Published by Elsevier Inc. doi:10.1016/j.otc.2007.04.004
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Titration of positive pressure for medical treatment of OSAS Follow-up evaluation of children who have persistent symptoms postintervention for OSAS Sleep disordered breathing (SDB) is a common cause of morbidity in childhood, with a spectrum ranging from benign snoring to complete airway obstruction. Benign or primary snoring is reported in 3% to 12% of the pediatric population, with OSAS affecting 1% to 3% [2]. Several authors have demonstrated that clinical history and physical examination are not accurate in the identification of children who have OSAS [3]. PSG is useful in documenting the presence of obstructive sleep apnea (OSA) events as well as their severity. PSG has been recommended as the test of choice to evaluate SDB by consensus of a panel of experts [4]. PSG has also shown to be useful in determining readiness for decannulation in children who have tracheostomy [5]. Performance of polysomnography in children PSG should be performed by a laboratory experienced in and comfortable with caring for children [1]. Technicians need to be experienced in dealing with children of various age levels and developmental status. Personnel should be certified in pediatric cardiopulmonary resuscitation. If a dedicated pediatric facility is not available, an area in the adult sleep laboratory should be designated for children. Children should be housed in an appropriate environment, with accommodations for a caregiver to sleep near the child. Caregiver availability to the child is important to minimize the child’s anxiety or fears about the study, as well as to provide any necessary care. The procedure should be explained to the child and the family by personnel skilled in the presentation of medical information. A crib should be available for small children. The person responsible for supervision of the pediatric sleep facility or functions should be a pediatrician with training and expertise in the area of sleep medicine. This person must assure that the PSG performance, scoring, and interpretation are appropriate for the age and condition of the child. The study timing should be set to mimic the child’s bedtime as closely as possible. Overnight studies are preferred because negative nap studies have been shown not to exclude the possibility of OSAS during a night study [6]. Studies should be performed without sedation in order to most accurately mimic the child’s normal sleep. Components of polysomnography in children Variables gathered during PSG in children are similar to those obtained in adults, with some additional information. Children may often demonstrate obstructive hypoventilation as a component of their OSAS, which
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may only be detected by increased carbon dioxide (CO2) levels [7]. Thus, PSG monitoring in children should include some method of determining CO2 levels, such as end tidal CO2 or transcutaneous CO2 [8]. The many channels of physiologic parameters and their purpose in the PSG are described in the following sections [1]. Sleep stages are determined using electroencephalogram (EEG), chin electromyogram (EMG), and electro-oculogram (EOG). EEG monitoring includes two central and two occipital leads with references to the opposite posterior auricular area. Additional EEG leads can be used to detect nocturnal events such as seizure activity. Three chin EMG leads are placed and used to detect skeletal muscle activity as required for the identification of rapid eye movement (REM) sleep. The chin EMG is also useful to detect swallowing and sucking during the study. Right and left EOG leads are used to detect eye movements essential to the identification of REM sleep. Respiratory effort is detected using chest and abdominal belts. Different styles of monitoring include strain gauges, chest wall impedance, inductance plethysmography, intercostal EMG, and pneumatic transducers [9]. These belts can assess qualitative respiratory effort, which is essential to distinguishing whether respiratory events are central or obstructive in origin. Air entry is assessed using a thermistor, nasal pressure, and a capnograph tracing. The thermistor detects airflow at the nose and mouth by detecting a temperature change in expired gas. Nasal pressure is an additional method of monitoring airflow by detecting pressure changes via a cannula placed in the nose. A recent study showed that the nasal pressure transducer is more sensitive in the detection of hypopnea, and suggested combining the use of both the thermistor and nasal pressure transducer for optimal detection of SDB in children [10]. During positive pressure titrations, flow is detected using measurements from the positive pressure device. Movements of extremities are monitored by EMG leads placed on the legs and sometimes on the arms. These movements are important in documenting PLM as well as movements that result from respiratory events. Position sensors can be used to document patient position. Digital video is also obtained. The video is useful in documenting patient position, movements, and unusual episodes such as parasomnias. Snoring is assessed by a snore microphone placed on the neck of the patient, by technician observation, and by audio recording. Gas exchange is assessed using monitoring for both oxygen and CO2. Oxygenation is monitored by pulse oximetry, using a comfortable sensor that can be left on the child for the duration of the study. It is essential that the pulse oximeter have a short sampling time (2 to 3 seconds) to avoid missing brief desaturations associated with events in children. The reliability of the pulse oximeter tracing is improved with recording of the pulse amplitude signal, allowing identification of desaturation events that are caused by poor probe function [11]. Ventilation is monitored in children by either end tidal (ET) CO2 or transcutaneous CO2 monitoring. The ET CO2 method is
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more responsive to rapid changes, whereas the transcutaneous method is not reflective of transient CO2 changes, and is most useful for a trend [8,12]. ET CO2 is monitored by a probe placed at the nose and mouth. ET CO2 generates a flow tracing that can also be used to monitor airflow. The sensor for the transcutaneous device must be changed every several hours to maintain accuracy. In patients with persistent gas exchange abnormalities, access to arterial blood gas measurement is useful in corroborating noninvasive monitoring of gas exchange. This can be useful in a patient who has alveolar hypoventilation, to accurately assess the extent of CO2 retention, or in a patient who has sickle cell disease with abnormal hemoglobin, in whom the pulse oximetry may not accurately reflect arterial oxygen level [13].
Begin the review It is helpful to preview the physician note/orders before the study to determine why the PSG is being performed. This will help ensure that the question being posed by the ordering physician will be appropriately addressed. For example, if a child is being studied to determine whether he/she can tolerate having his/her tracheostomy tube capped, it is important to make certain the child has the capping device, and that the technicians know that the tracheostomy is to be capped during the study. Before beginning review of the study, it is helpful to review any notes made by the technician during the course of the night. This alerts the physician to technical or patient issues encountered over the course of the study. These issues might include unusual events over the night, such as confusional arousals or artifactual desaturation related to patient compromise of the oximeter probe. In general, polysomnograms (PSGs) should be reviewed and scored by an experienced scoring technician before interpretation; however, all PSGs should be examined page by page by the reviewing professional for the most accurate interpretation of the nocturnal events. First, the biocalibration should be evaluated. This is a series of tests conducted by the technician at the beginning and end of the study to document the normal function of the various channels of information recorded. The biocalibration may be limited in children who are young, developmentally delayed, or uncooperative. The components of the biocalibration include having the patient look up, down, and to both sides in order to assess detection of eye movements by EOG, which facilitates scoring of REM sleep. The EEG is evaluated with eyes open and closed in order to identify alpha EEG waves, which aid in detection of wakefulness. The patient is asked to make a snoring type noise to check the snore channel, and the patient is asked to grit his/her teeth to detect bruxism. The patient moves both legs separately to assess the integrity of the leg EMGs. The patient is asked to hold his/her breath to detect cessation of chest wall movement, and the chest and abdomen belts are tested to make certain they move together with respiratory effort.
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Sleep stage analysis It is helpful to quickly review the patient’s sleep architecture by viewing the hypnogram (Fig. 1). A hypnogram is a summary of the different sleep stages achieved shown in graphic form. It is important to review the sleep architecture in terms of what is to be expected for the patient’s age. Timing and length of various sleep stages vary with patient age, and should be compared with age-expected norms. For example, although it is normal for infants to enter sleep through stage REM, entering sleep through stage REM may suggest an underlying sleep disorder such as narcolepsy in an older child or adolescent. Components of sleep architecture that should be assessed include: percentage of total sleep time (TST) spent in stage I/II, stage III/IV, stage REM, and wakefulness. These percentages should be compared with ageappropriate normals. Several authors have examined sleep architecture in normal children ages 1 to 15 years [14–18]. In these studies, stage I sleep occupied 4% to 7.7% of TST, and stage II occupied 36% to 49% of TST, with the combination of stage I and II in each study ranging from 41% to 53% of the TST. Slow wave sleep (combining stages III and IV) occupied 14% to 32% of the TST, whereas stage REM occupied 17.4% to 21.1% of the TST.
Fig. 1. This is a typical hypnogram showing time across the bottom axis. The left axis shows the different sleep stages. The horizontal bars indicate the time spent in the various sleep stages during the course of the PSG.
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Timing of sleep stages can be noted by review of the hypnogram. Children usually have a short period of stage I/II after sleep onset, and then enter stage III/IV (also known as delta or slow wave sleep). Stage III/IV sleep will predominate early in the night, with regular cycling between the stages I/II, stages III/IV, and REM. REM sleep will usually cycle every 60 to 120 minutes, with a wide range of timing between REM periods [14]. Sleep latency, the time after lights out until sleep is achieved, should also be noted. Sleep latency is generally less than 25 minutes [14,16]. It may be prolonged if the child has recently had a nap, and it may be shortened in certain sleep disorders. Sleep efficiency is a measurement of the amount of the total time in bed that the patient spends asleep, and should also be noted. It gives a picture of whether the patient has a disrupted sleep pattern. Sleep efficiency in children is usually greater than 89% [14–18]. REM latency, the time from onset of sleep to the first epoch of REM sleep, is also noted. REM latency can be prolonged if the first REM period is difficult to detect by the scoring technician. REM latency can be shortened in certain conditions, such as depression or narcolepsy. The presence and amount of REM sleep deserves careful attention. Length of time spent in REM is short earlier in the night, with lengthening of REM episodes as the night progresses [14]. During REM sleep, OSA may be worsened because of loss of muscle tone. Thus, to make certain the most severe extent of OSA is observed, patients should achieve REM sleep. REM sleep may be decreased if the patient has a disrupted sleep pattern, with arousals out of REM caused by obstructive events. This may cause the overall number of obstructive events to be lowered. EEG should be monitored for unusual complexes, such as nocturnal epileptiform discharges (Fig. 2). These may be noted in children who have a history of a seizure disorder as well as in those who do not have such a history. Whether these episodes are associated with clinical seizure activity or respiratory events should be noted. Technician observation and the video should be reviewed for evidence of clinical seizure activity in association with these EEG changes. Consideration may be given to a more thorough evaluation by a full sleep-deprived EEG if complexes are widespread during the recording. Arousal summary Arousals are scored by the scoring technician based on the appearance of the EEG tracing. An arousal is scored when there is an abrupt change in the EEG lasting 3 seconds, following at least 10 seconds of continuous sleep [19]. Arousals can be attributed to preceding events, including respiratory events, leg movements, snore events, or technician presence in the room, or may occur without an obvious trigger. Arousals are reported using the arousal index, which is the number of arousals divided by the hours of sleep. Normal values for arousal indices vary from laboratory to laboratory.
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Fig. 2. Shown here is an episode of spike and wave activity occurring out of stage II sleep. The tracing shows the EEG leads on the left axis with time on the bottom axis. A 10-second duration screen is shown, with each rectangle along the bottom axis representing 1 second.
Studies of normal children have found mean arousal indices of 8.8 to 9.5 [14,15,17]. Arousals attributed to respiratory events give a measure of sleep disruption caused by those respiratory events. It is also important to note that children may not arouse to respiratory events as easily as adults do [7].
Heart rate/rhythm The ECG should be reviewed for evidence of brady or tachy rhythms as well as abnormal ECG rhythms. Respiratory events may be associated with decrease in heart rate, with subsequent increase in heart rate after the event has resolved, or in association with arousals. Some patients will have evidence of premature ventricular or atrial contractions, which may or may not be related to respiratory events.
Snoring Determination of the presence or absence of snoring is important to note, particularly in comparison to what is observed in the home environment. If a child has loud snoring over the course of the night, typical to what parents describe at home, with few documented respiratory events, a diagnosis of
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primary snoring may be made. This may be reassuring to family members, in that the snoring they have noted at home is not associated with documented respiratory events or gas exchange abnormalities; however, there are reports in the literature that snoring without respiratory events has been associated with poor academic performance [20,21]. Leg movements The scoring technician will score leg movements that meet criteria for PLM. Criteria for PLM include leg movements noted in either or both legs that are at least one quarter of the amplitude noted during the biocalibration lasting from 0.5 to 5 seconds. Leg movements must be separated by at least 5 seconds, but not more than 90 seconds, and must occur in clusters of at least four to be considered PLM (Fig. 3). These leg movements should not be related to other events, such as respiratory events or arousals [22]. Leg movements should be carefully reviewed to make certain they meet criteria for PLM and are not related to subtle respiratory events. The total number of PLM that meet these criteria are determined, and the PLM index is calculated by dividing the total number of PLM by the number of hours of sleep. A PLM index of five or greater is considered abnormal [22,23].
Fig. 3. This tracing shows a series of four periodic leg movements occurring over a time span of 2.5 minutes. The PLM are apparent as deflections in the two leg channels. LAT refers to left anterior tibialis and RAT refers to right anterior tibialis. These leg movements are not associated with respiratory events or arousals.
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Respiratory events Several definitions are important for the classification of respiratory events. The term ‘‘apnea’’ refers to an event with no flow. Apneas are scored for events with a decrease in flow by 75% or greater from the baseline flow observed before the event. If any portion of an event fits this definition, the event can be scored as an apnea. Hypopnea refers to a decrease in flow by 30% to 50% from the usual baseline. Apneas and hypopneas can be further classified as being central, obstructive, or mixed in nature. Obstructive events are those caused by a decrease in flow associated with persistent, sometimes increased respiratory effort noted in the chest and abdominal belts. Obstructive apneas are scored when a decrease of 75% or greater is detected in the airflow or nasal pressure channels associated with continued respiratory effort (Fig. 4) [24]. Whereas in adults there is a 10-second minimum event length noted, in children the events must be two respiratory cycles [25]. Thus, in an infant breathing at 60 times per minute, a significant event can be as brief as 2 seconds. An obstructive hypopnea is scored when a decrease in the flow channel of 30% to 50% is noted with persistent respiratory effort (Fig. 5) [1,25]. In order for an obstructive hypopnea to be scored, there must be some consequence to the event, including a 3% to 4% drop in oxygen saturation, a leg movement, or an EEG arousal.
Fig. 4. This figure demonstrates two episodes of obstructive apnea shown by cessation of flow in the nasal pressure and airflow channels with continued respiratory effort. The events result in oxygen desaturation as low as 80%.
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Fig. 5. An episode of obstructive hypopnea is shown here, depicting two epochs or 1 minute of a PSG. The event is marked by a decrease in the nasal pressure and airflow with continued respiratory effort. The hypopnea results in a drop in oxygen saturation to 94% and an EEG arousal.
The contour of the nasal pressure tracing is often flattened, indicating flow limitation with respiratory effort during obstructive hypopneas [26]. Central events are those caused by an absence or severe decrease in respiratory effort, as measured by chest or abdominal belts. Central apneas (Fig. 6) are scored when there is an absence of respiratory effort associated with a 70% or greater decrease in the airflow or nasal pressure. During central apneas, there may be small deflections noted in the chest tracing corresponding to cardioblastic artifact from chest wall movement associated with cardiac activity. Central hypopneas (Fig. 7) are events with decreased respiratory effort associated with a 30% to 50% decrease in the airflow or nasal pressure channels and desaturation or EEG arousal. The contour of the nasal pressure tracing will be rounded during central hypopneas, compared with the flattened contour noted with obstructive hypopneas [26]. It is important to be certain that central hypopneas are not confused with obstructive hypopneas. Obstructive hypopneas may appear to be associated with an apparent decrease in respiratory effort caused by work against an obstructed upper airway [26]. Central events are more likely to be noted during REM sleep, particularly in patients who have underlying disorders such as Prader-Willi syndrome or Arnold-Chiari malformation. Mixed
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Fig. 6. This tracing demonstrates a central apnea lasting 11.5 seconds, resulting in a drop in oxygen saturation to 91% and an EEG arousal. During this event there is cessation of airflow with lack of respiratory effort.
respiratory events are those with a central and obstructive component. Usually, these events begin with the central component, then progress to an obstructed component with the resumption of respiratory effort. After all events are reviewed and scored, several indices can be calculated. These include apnea index (AI) and apnea-hypopnea index (AHI) which are calculated for the entire sleep period, for non-REM (NREM) and REM sleep. The term ‘‘index’’ refers to the number of events divided by the number of hours of sleep. This calculation allows the comparison of PSGs of various lengths. The AI is determined using only apneas; the AHI includes apneas and hypopneas. Studies of normal children suggest that any obstruction is abnormal, and that normal values for children are different from those for adults. Several authors have investigated PSG findings in normal children [14,15,17]. There is general agreement that AI and AHI are less than 1 in normal children. Katz and Marcus [2] have suggested the following values for classification of respiratory events in children:
AHI AHI AHI AHI
less than 1 ¼ normal 1 through 4 ¼ mild OSA 5 through 10 ¼ moderate OSA greater than 10 ¼ severe OSA
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Fig. 7. This tracing demonstrates a 2-minute window in REM sleep with two episodes of central hypopnea. These events are marked by a decrease of at least 30% in the airflow channel, with a concomitant decrease in respiratory effort in the chest and abdomen channels. These events result in significant oxygen desaturation as low as 78% and increase in ETCO2 to 53 torr.
They also propose grading of disease severity by gas exchange parameters. The AHI should be considered in the context of the patient’s presentation. Children who have complications of OSAS or underlying medical problems may require intervention for mild OSA in order to prevent worsening of their medical disorder or worsened complications. For example, children who have pulmonary hypertension might require aggressive intervention, despite mild OSA, to prevent worsening of their pulmonary hypertension. Gas exchange Gas exchange should be reviewed carefully for the entire tracing. The pulse oximetry tracing should be reviewed for desaturation, with careful attention to whether the desaturation is associated with a respiratory event, arousal, or leg movement. Desaturations might be caused by respiratory events of any duration. The actual desaturation will occur 1 to several seconds after the respiratory event. If the respiratory event is prolonged, the desaturation may begin before the event has terminated. Desaturations unassociated with respiratory events should be reviewed for accuracy in
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terms of whether the pulse oximeter is tracing accurately, or whether the pulse oximetry probe has been compromised by patient position. It is important to note the baseline oxygen saturation before study onset. Patients who have low saturation at baseline may be at risk for desaturation with sleep onset, worsening with respiratory events. Those who have persistent oxygen desaturation without respiratory events potentially require further investigation for underlying lung disease, hypoventilation, or abnormal hemoglobin (ie, sickle cell disease). Hypoventilation can be evaluated by noting the CO2 associated with episodes of oxygen desaturation. In general, oxygen saturation should be greater than 92% in normal studies [14,15,17,18,27]. Children on oxygen supplementation should have their flow rate recorded at the beginning of the study, with monitoring of response to changes in the oxygen flow rate over the course of the study. CO2 tracing should be reviewed as well. Baseline CO2 level before sleep onset should be noted. Normal children can be expected to have a 5 to 7 torr rise in CO2 with sleep onset [27]. Children may have a pattern of obstructive hypoventilation with OSAS, resulting in increases in CO2 without significant oxygen desaturation. Abnormal levels of CO2 vary, with Marcus and colleagues [27] reporting greater than 10% of TST being spent with CO2 greater than 50 torr as abnormal, and Montgomery-Downs and colleagues [14] reporting that in normal children, 2.8 11.3 of the TST was spent with a CO2 greater than or equal to 50 torr. Marcus and colleagues [27] also report CO2 levels of greater than 53 torr as being abnormal. Uliel and colleagues [18] found less time spent with CO2 greater than 45 torr in their study of normal children, suggesting that ET CO2 greater than 45 torr for greater than 10% of the TST, or any CO2 greater than 50 torr, is abnormal. It is important to recognize potential issues associated with ETCO2 monitoring. Sampling tubing can become obstructed with nasal secretions or moisture, and may become displaced. Other factors that affect the accuracy of the ETCO2 readings include mouth breathing, airway obstruction, supplemental oxygen delivery at the other nostril, and cyanotic heart disease [28–30]. It is important to know the values obtained in your individual sleep laboratory, and compare values during the study with the baseline values. CO2 trends may be more helpful, with consideration given to obtaining a blood gas for high values to determine the accuracy of noninvasive measurements.
Summary PSG in children represents an important and useful tool in the evaluation of the multitude of sleep-related conditions, including OSAS, PLM disorder, and those with an underlying predisposition toward gas exchange aberrancies. To obtain the most useful information, sleep studies in this unique population should be performed in laboratories with staff experienced in
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working with children of all ages and stages of development, in a setting sensitive to both child and caregiver. In performing pediatric PSG, physicians should keep in mind PSG can be successfully performed in children. Pediatric PSG should be performed in a laboratory experienced in and comfortable with the care of children. Recognize that PSG in children includes measurement of carbon dioxide levels to detect obstructive or central hypoventilation. Criteria for scoring and interpretation of PSG in children differ from those for adults.
References [1] Standards and indications for cardiopulmonary sleep studies in children. Am J Respir Crit Care Med 1996;153:866–78. [2] Katz ES, Marcus CL. Diagnosis of obstructive sleep apnea syndrome in infants and children. In: Sheldon SH, Ferber R, Kryger MH, editors. Principles and practice of pediatric sleep medicine. USA: Elsevier Saunders; 2005. p. 197–210. [3] Brietzke SE, Katz ES, Roberson DW. Can history and physical examination reliably diagnose pediatric obstructive sleep apnea/hypopnea syndrome? A systematic review of the literature. Otolaryngol Head Neck Surg 2004;131(6):827–32. [4] American Academy of pediatrics, Section on Pediatric Pulmonology, Subcommittee on Obstructive Sleep Apnea. Clinical practice guideline: diagnosis and management of childhood obstructive sleep apnea syndrome. Pediatrics 2002;109:704–12. [5] Tunkel DE, McColley SA, Baroody FM, et al. Polysomnography in the evaluation of readiness for decannulation in children. Arch Otolaryngol Head Neck Surg 1996;122(7):721–4. [6] Marcus CL, Keens TG, Ward SL. Comparison of nap and overnight polysomnography in children. Pediatr Pulmonol 1992;13:16–21. [7] Rosen CL, D’Andrea L, Haddad GG. Adult criteria for obstructive sleep apnea do not identify children with serious obstruction. Am Rev Respir Dis 1992;146:1231–4. [8] Morielli A, Desjardins D, Brouillette RT. Transcutaneous and end-tidal carbon dioxide pressures should be measured during pediatric polysomnography. Am Rev Respir Dis 1993; 148:1599–604. [9] Krishna J, Sans-Capdevila O, Gozal D. Sleep studies: which technologies? Paediatr Respir Rev 2006;7(Suppl 1):S202–5. [10] Budhiraja R, Goodwin JL, Parthasarathy S, et al. Comparison of nasal pressure transducer and thermistor for detection of respiratory events during polysomnography in children. Sleep 2005;28(9):1117–21. [11] Lafontaine V, Ducharme FM, Brouillette RT. Can we rely on pulse oximetry desaturation events? [abstract] Am Rev Respir Dis 1994;149:69A. [12] Hansen TN, Tooley WH. Skin surface carbon dioxide tension in sick infants. Pediatrics 1979; 64:942–5. [13] Craft JA, Alessandrini E, Kenney LB, et al. Comparison of oxygenation measurements in pediatric patients during sickle cell crises. J Pediatr 1994;124:93–5. [14] Montgomery-Downs HE, O’Brien LM, Gulliver TE, et al. Polysomnographic characteristics in normal preschool and early school-aged children. Pediatrics 2006;117:741–53. [15] Wong TK, Galster P, Lau TS, et al. Reliability of scoring arousals in normal children and children with obstructive sleep apnea syndrome. Sleep 2004;27:1139–45.
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[16] Coble PA, Kupfer DJ, Taska LS, et al. EEG sleep or normal health children. Part I: findings using standard measurement methods. Sleep 1984;7:289–303. [17] Traeger N, Schultz B, Pollock AN, et al. Polysomnographic values in children 2–9 years old: additional data and review of the literature. Pediatr Pulmonol 2005;40:22–30. [18] Uliel S, Tauman R, Greenfeld M, et al. Normal polysomnographic respiratory values in children and adolescents. Chest 2004;125:872–8. [19] American Sleep Disorders AssociationdThe Atlas Task Force. EEG arousals: scoring rules and examples. Sleep 1992;15:174–84. [20] Gozal D, Pope DW. Snoring during early childhood and academic performance at ages thirteen to fourteen years. Pediatrics 2001;107(6):1394–9. [21] Urschitz MS, Guenther A, Eggebrecht E, et al. Snoring, intermittent hypoxia and academic performance in primary school children. Am J Respir Crit Care Med 2003;168(4):464–8. [22] American Academy of Sleep Medicine. International classification of sleep disorders. 2nd edition. Diagnostic and coding manual. Westchester (IL): American Academy of Sleep Medicine; 2005. p. 182–6. [23] Picchietti DL, Walters AS. Moderate to severe periodic limb movement disorder in childhood and adolescence. Sleep 1999;22(3):297–300. [24] Phillips B, Kryger MH. Management of obstructive sleep apnea-hypopnea syndrome: overview. In: Kryger MH, Roth T, Dement WC, editors. Principles and practice of sleep medicine. 4th edition. USA: Elsevier Saunders; 2005. p. 1111–3. [25] Kheirandish-Gozal L. Practical aspects of scoring sleep in children. Paediatr Respir Rev 2006;7(S1):S50–4. [26] Berry RB. Monitoring respiration during sleep. In: Sleep medicine pearls. 2nd edition. Philadelphia: Hanley and Belfus, Inc.; 2003. p. 84–5. [27] Marcus CL, Omlin KJ, Basinki DJ, et al. Normal polysomnographic values for children and adolescents. Am Rev Respir Dis 1992;146:1235–9. [28] Tobias JD, Meyer DJ. Noninvasive monitoring of carbon dioxide during respiratory failure in toddlers and infants: end-tidal versus transcutaneous carbon dioxide. Anesth Analg 1997; 85:55–8. [29] Friesen RH, Alswang M. End-tidal pCO2 monitoring via nasal cannulae in pediatric patients: accuracy and sources of error. J Clin Monit 1996;12:155–9. [30] Fukuda K, Ichinohe T, Kaneko Y. Is measurement of end-tidal CO2 through a nasal cannula reliable? Anesth Prog 1997;44:23–6.