Normal Polysomnographic Values for Children and Adolescents 1- 3
CAROLE L. MARCUS,4 KENNETH J. OMLlN, DANIEL J. BASINKI, SANDRA L. BAILEY, ADRIANA B. RACHAL, WALTER S. VON PECHMANN, THOMAS G. KEENS, and SALLY L. DAVIDSON WARD
Introduction
Polysomnography
is routinely performed to evaluate children and adolescents with sleep-disordered breathing. However, normal respiratory polysomnographic values for the pediatric age group have not yet been established. Although pediatric polysomnographic guidelines for diagnosing sleep-disordered breathing have been stated in the literature (1), few data are available regarding normal respiratory parameters during sleep in healthy children and adolescents. The use of adult criteria to evaluate children and adolescents with suspected sleep-disorderedbreathing may not be valid. The apnea index in asymptomatic adults increases with advancing age (2). Similarly, sleeping Sa02 values in normal adults tend to fall with increasing age (3). Thus, the normal respiratory pattern and gas-exchange values for healthy, asymptomatic children and adolescents are expected to differ from those of adults. Wetherefore performed polysomnography in 50 healthy children and adolescents in order to establish normal polysomnographic values. Methods Patient Selection Normal, healthy children and adolescents ranging in age from 1 to 18 yr were studied. Children were recruited from families of hospital employees. Children with significant medical problems requiring chronic medication or with a history of adenoidectomy, tonsillectomy, or other airway surgery were excluded. The height and weight were obtained for each child, and growth percentiles were obtained using standard growth charts (National Center for Health Statistics, adapted by Ross Laboratories, Columbus, OH). The body mass index (BMI) was defined as the weight in kilograms divided by the height in meters squared. Obese children and adolescents, defined as those with weights greater than 120070 of the ideal weight for height (4), were excluded.
SUMMARY Although polysomnography Is routinely performed to evaluate children and adolescents with sleep-disordered breathing, normal polysomnographic values for the pediatric age group have not yet been established. We therefore performed overnight polysomnography In 50 normal children and adolescents (mean age 9.7 ± 4.6 SO yr, range 1.1 to 17.4 yr). Of the children 56% were male. Chest wall motion, ECG, oronasat airflow, end-tidal PC02(PETC02), arterial oxygen saturation (Sa02), and electrooculogram were monitored. Children had 0.1 ± 0.5 (range 0 to 3.1) obstructive apneas per hour of total sleep time, with only 18% of children having any obstructive apneas. No child had obstructive apneas > 10 s In duration. Of the children 30% had central apneas ~ 10 s In duration, and one child had a central apnea associated with Sa02 < 90%. Peak PETC02 was 46 ± 4 mm Hg (range 38 to 53 mm Hg), and hypoventllatlon (PETC02 > 45 mm Hg) occurred for 7 ± 19% total sleep time (range 0 to 91%). The Sa02 nadir was 96 ± 2% (range 89 to 98%), with only one child desaturatlng below 90% in association with a central apnea. we conclude that polysomnographlc results In the pediatric age group differ from those in adults. Recommendations for normal polysomnographlc criteria are given. AM REV RESPIR DIS 1992; 146:1235-1239
Questionnaire A standard questionnaire regarding symptoms of obstructive sleep apnea syndrome, devised by Brouillette and colleagues (5), was administered to the parents of each child. Based on Brouillette's data, no subject with a questionnaire score < -1 would be expected to have obstructive sleep apnea syndrome, whereas a score between -1 and 3.5 is considered indeterminate and a score> 3.5 is considered highly predictive of obstructive sleep apnea syndrome. Children with questionnaire scores > -1 were excluded from study. Polysomnography Polysomnographic studies were performed overnight, in a quiet, dark room with an ambient temperature of 24 0 C. No sedation or sleep deprivation was used. Preadolescent children were accompanied by one parent throughout the night. During polysomnography, the following parameters were measured and recorded continuously on a Gould 16-channel strip-chart recorder (Gould, East Lake, OH): 1. Chest wall motion was measured by thoracic impedance or Respitrace (Ambulatory Monitoring, Inc., Ardsley, NY). 2. Heart rate was measured by electrocardiography (ECG). 3. Inspired and end-tidal POz and Pco, (PETeoz), sampled at the nose at a rate of 60 ml/min, were measured by mass spectrometry (medical gas analyzer; Perkin-Elmer, Wilton, CT). The mass spectrometer was calibrat-
ed against primary-grade gasses at the beginning and end of each study. End-tidal Po, was calibrated using 100% N, and room air, and end-tidal Pco, was calibrated using 100010 Ns and a 10% COz and 90% Os gas mixture. 4. Airflow was sampled at the mouth with a thermistor (Physitemp, Clifton, NJ). 5. Arterial oxygen saturation (Saoz) was measured by pulse oximetry (N 200 pulse oximeter; Nellcor, Haywood, CAl.
(Received in original form June 24, 1991 and in revised form February 3, 1992) 1 From the Division of Neonatology and Pediatric Pulmonology, Children's Hospital of Los Angeles, University of Southern California School of Medicine, Los Angeles, California. 2 Supported in part by Grant No. 1 ROI HD22696-01Al from the National Institute of Child Health and Human Development; the National Center for the Prevention of Sudden Infant Death Syndrome, Baltimore; the Greater Los Angeles and Washington State chapters of the National Sudden Infant Death Syndrome Alliance; the Los Angeles County, Orange County, Inland Empire, and Kern County chapters of the Guild for Infant Survival; the Junior Women's League of Orange County; and the Ruth and Vernon Taylor Foundation. 3 Correspondence and requests for reprints should be addressed to Carole L. Marcus, M.D., Johns Hopkins Hospital, Division of Pediatric Pulmonology, Park 316, 600 North Wolfe Street, Baltimore, MD 21205. 4 Recipient of a Children's Hospital of Los Angeles Fellowship Support Grant.
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6. Oximeter pulse waveform was recorded. 7. Transcutaneous P0 2and Pco, were measured using a heated (43 0 C) transcutaneous oxygen electrode (Transend'" cutaneous gas system; Sensorlvledics, Yorba Linda, CA). Trends of transcutaneous values were used to confirm PETc02 and Sao, values. 8. Electrooculograph (EOG) was recorded. Children were also monitored and recorded on videotape using an infrared video camera. The children were continuously observed by a technician trained in polysomnography. Observations ofthe child's sleep behavior and respiratory events were recorded directly on the strip-chart paper by the technician. The following parameters were evaluated: 1. Obstructive apneas were defined as the
presence of chest wall motion associated with the absence of airflow detection by both the end-tidal catheter at the nose and the thermistor at the mouth. The number and duration of obstructive apneas of any length were quantitated. The apnea index, defined here as the number of obstructive apneas of any length per hour 0 f sleep, was calculated for each subject. Because standardized methods for defining hypopneas in children have not been defined, we did not quantitate hypopneas. 2. Central apneas were defined as the absence of chest wall motion associated with absence of airflow detection by both the endtidal catheter at the nose and the thermistor at the mouth. The number of central apneas ~ 10 s was quantitated. Central apneas of any length that were associated with desaturation were quantitated separately. Central apneas occurring immediately following gross body movements were not quantitated. Central apneas occurring immediately after sighs were quantitated separately. 3. Mixed apneas were defined as apneas having both central and obstructive components, with the central component ~ 4 s duration or twice the respiratory cycle length for that subject and the obstructive component being of any length. The number and duration of mixed apneas were quantitated. 4. Periodic breathing was defined as three or more respiratory pauses of> 3 s duration with < 20 s of normal respiration between pauses (6). The length of the run of periodic breathing and the lowest arterial oxygen saturation associated with the periodic breathing were quantitated. 5. The lowestand highest Sao, and the number of desaturations > 4070 were quantitated. The total duration of desaturation (Sa0 2 < 90%) expressed as a percentage of total sleep time (TST) was quantitated. ASao2 was defined as the difference between the peak and nadir Sao, during sleep. Measurements associated with poor pulse tracings were discarded. 6. The lowest and highest PETC02 were quantitated. The total duration of time during which PETC02 was> 45 mm Hg and the total duration of time during which PETC02 was > 50 mm Hg, expressed as percentages
MARCUS, OMLlN, BASINKI, ET AL.
of TST, were quantitated. APETC02 was defined as the difference between the peak and nadir PETC02 during sleep. Transient (one to two breaths) increases in PETc 02 immediately following gross body movements were not quantitated because they were not representative of the subject's baseline ventilation and because the recording was occasionally obscured by motion artifact. An elevation in PETCO2 in the breath immediately following a sigh was not considered representative of the subject's baseline ventilation and was therefore quantitated separately. 7. Total sleep time was quantitated, and respiratory parameters were expressed as a percentage of TST. Sleep was based on behavioral observations and electrooculographic criteria. Respiratory parameters were not quantitated during periods of wakefulness.
Statistical Methods All data are expressed as mean ± standard deviation (SD) when appropriate. Recommendations for normal values were calculated from the mean plus twice the standard deviation when parameters followed a normal distribution. For data that were not normally distributed and were one tailed, we chose a normal range that included 97.5% of the subjects.
Results
A total of 50 children and adolescents were studied. Ages ranged from 1.1 to 17.4 yr, with a mean age of 9.7 ± 4.6 yr. The age distribution is shown in figure 1; 28 (56070) were male. Distribution by ethnic group was as follows: 25 (50%) children were non-Hispanic white, 13 (26%) wereHispanic, 5 (10070) wereblack, 4 (8%) were Asian, and 3 (6070) were Native American. Mean body mass index was 18.6 ± 3.2 (range 11.6to 26.3) kg/m', No child was obese. One child occasionally received nocturnal nasal desmopressin acetate (DDAVP) as treatment for enuresis. Three children were completing courses of antibiotics for otitis media at the time of study but were considered by their parents to be at the baseline level of health. Four children had a history consistent with symptoms of mild allergic rhinitis; none of these children were symptomatic or requiring treatment at the time of study. The mean score on the questionnaire was - 3.2 ± 0.1. All children had scores < -1. Duration of TST was 6.0 ± 1.6 h. A portion of a typical tracing, detailing the cardiorespiratory parameters, is shown (figure 2). Polysomnographic results are shown in table 1. Obstructive apneas were uncommon. A total of 9 (18%) children had one or more obstructive apneas (table 2). A total of six were male. No child had ob-
o
1
2 8 9 10 11 12 13 14 --'----"------~'---------.---------~-----
AGE (years)
Fig. 1. The number of SUbjectsstudied of each year of age are shown.
structive apneas > 10s in duration. There was no correlation between apnea index and age (r = -0.14, not significant [NS]) or apnea index and BMI (r = - 0.07, NS). Of the four children with histories of mild allergic rhinitis three had obstructive apneas. One child had an apnea index of 3.1. The child was asymptomatic and had a questionnaire score of - 3.83. However, she had an older sibling who was being treated for severe obstructive sleep apnea syndrome. In 15 (30070) children one to five central apneas ~ 10 s in duration occurred and were 10 to 18 s long. In addition, 1 child desaturated to 89070 during a 9-s central apnea. No other children desaturated below 90%. Saturation values during central apneas were not obtained for 1 child because of motion artifact. Children with central apneas ranged from 1.3 to 16.9 yr of age, and 56% were girls. Central apneas following sighs were quantitated separately. The mean longest central apnea following a sigh was 13 ± 6 s (range 5 to 26 s). No mixed apneas occurred in any children or adolescents. Periodic breathing occurred in 4 (8070) children and lasted for 0.4 to 5.7 min. Periodic breathing was associated with saturation values of 92 to 97%. Peak PETC02 was 46 ± 4 (range 38 to 53) mm Hg (table 1); 21 (42070) children had PETC02 > 45 mm Hg, and 3 children had PETC02 > 50 mm Hg (figure 3). PETC02was> 45 mm Hg for 6.9 ± 19.1070 (range 0 to 90.5%) of TST and> 50 mm Hg for 0.5 ± 4% (range 0 to 25070) TST (figure 4). There was no correlation between duration of hypoventilation and age (r = 0.16, NS). There was a significant but weak correlation between peak PETC02 and age (r = 0.28, p < 0.05). The highest end-tidal PETC02in the breath immediately after a sigh was 44 ± 4 (range 36 to 51) mm Hg. The Sao, nadir was 96 ± 2% (range 89 to 98070). Only 1 child desaturated to
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NORMAL POLYSOMNOGRAPHY IN CHILDREN
-r r~
No. of subjects
10'---:-:--=--':"::=~--------------------,
#
;r
125r50r
PI
Fig. 2. A detail of a portion of a typical polysomnogram. Sa02, arterial oxygen saturation; PETc02, end-tidal carbon dioxide tension.
1~
Sa0 2
J
o~,m.I~~UI~~
m
0
wav.Fofm~ Chest Wall Impedance
38 39
40
4,
42
43 44
45
46
47
48
49
50
5,
52
53
Peak peo 2 (mm Hg)
NasalThermlSlor~
Fig. 3. The number of subjects at each level of peak end-tidal carbon dioxide tension are shown. The data are normally distributed.
TABLE 1 POLYSOMNOGRAPHIC VALUES*
No. of SUbjects
Mean ± SO Apnea index,t NIh Maximum PETC02, t mm Hg Minimum PETc02, mm Hg ~PETC02 t, mm Hg Duration of hypoventilation, (PETC02 > 45 mm Hg),t: % TST Maximum Sa02, % Minimum Sa02,t: % Desaturation > 4%/h TST,t: n ~Sa02,t %
Recommended Normal Values
Range
Children Classified Abnormal n (%)
0.1 46 38 7
± ± ± ±
0.5 4 3 3
0-3.1 38-53 28-44 2-11
" 13
1 (2) 0(0) NA 0
6.9 100 96 0.3
± ± ± ±
19.1 1 2 0.7
0-90.5 98-100 89-98 0-4.4
" 60% NA ~ 92 "1.4
3 (6) NA 2 (4) 1 (2)
"8
2 (4)
4±2
" 1 " 53 NA§
0-11
- The number of children classified as abnormal represents the number of children who would be judged to have an abnormality based on the recommended values. Apnea index is defined as the number N of obstructive apneas of any length per hour of sleep. t Recommended normal values based on mean :t: 2 SO when parameters follow a normal distribution. For data that are not normally distributed, the recommended normal values are based on inclusion of 97% of subjects tested for one-tailed distribution.
40~~=~----------------,
30
20
10
0 ..1
o
_
10
20
30
40
50
60
70
80
90
100
Duration of hypoventilation (pea 2 ) 45 mm Hg)
Fig. 4. The number of subjects at each duration of hypoventilation (end-tidal carbon dioxide tension> 45 mm Hg) are shown. Data not normally distributed, with a one-tailed configuration.
*
TABLE 2 CHARACTERISTICS OF SUBJECTS WITH OBSTRUCTIVE SLEEP APNEA (OSA)* Age (yr)
4.1t 4.2 4.6 6.3t: 12.6 13.0t: 14.5t: 16.9 16.9
n Sex
(OSAInight)
Apnea Index
Duration of Longest OSA (5)
F F M M M M M M F
12 1 2 1 1 2 1 2 1
3.1 0.2 0.3 0.2 0.2 0.3 0.3 0.3 0.2
10 6 10 5 5 3 6.5 4 5
- Characteristics of individual subjects with obstructive apneas are shown. Apnea index defined as number of obstructive apneas of any length per hour of sleep. t Sibling has obstructive sleep apnea syndrome. History of mild allergic rhinitis.
*
890/0 in association with a central apnea. No other child desaturated below 90%, and only 3 (60/0) children desaturated below 930/0. A total of 23 children had discrete episodes of desaturation >4070. The number of desaturations > 4%/h of sleep was 0.3 ± 0.7. The recommended normal values and the number of subjects who would be classified as abnormal based on these recommendations are shown in table 1. A total of 6 subjects had at least one ab-
normal parameter. Of these 6 subjects four had a single abnormal parameter. The fifth subject had a Sao, nadir < 92% and a dSao;z > 8070, and the sixth subject had a Sao, nadir < 92%, dSao;z > 8%, and more than 1.4desaturations >4%/h TST. Discussion
This study has defined normal polysomnographic values for children older than
infancy and for adolescents. Despite the increasing use of polysomnography in pediatrics, previous polysomnographic data in the pediatric age range have been scanty, From this study, it appears that adult polysomnographic criteria cannot be extrapolated to children and adolescents. Obstructive apneas occurred rarely in the children and adolescents in this study and werenever> 10s in duration. Therefore, this study has provided objective evidence for the statements by previous researchersthat obstructive apneas of any length are rare in children (7-9). This is in contrast to adults. In adults, the apnea index is commonly used to evaluate obstructive sleep apnea, with the apnea index defined as the number of obstructive apneas > 10 s in duration per hour of sleep (10). Obstructive apneas ~ 10 s in duration are not quantitated. The apnea index in asymptomatic adults increases with advancing age (2). Thus, some authorities consider an apnea index < 5 as normal for adults (11), whereas others consider an apnea index < 10 to be normal (12). In the present study, the apnea index (for apneas of any length) in children and adolescents was 0.1 ± 0.5. Clearly, therefore, adult criteria cannot be applied to children and
1238
adolescents. We recommend that more than one obstructive apnea of any length per hour of sleep be considered abnormal for the pediatric age group. However, the clinical significance of short apneas in children has not yet been ascertained. In this study, chest wall motion was measured by either thoracic impedance or respiratory inductive plethysmography. Impedance monitors do not directly detect chest wall motion. Although used frequently to monitor respiration, thoracic impedance monitors have been reported occasionally to detect cardiac artifact falsely as chest wall motion and therefore miss apneas (13). However, ECG artifact was not seen in any of the tracings in this study (figure 2). All subjects were continually observed by a trained polysomnography technician throughout the study, and videotapes were reviewedafter the study. There were no instances in which obstructive apneas were missed by monitoring but detected by direct observation. Central apneas occurred frequently in the normal children and adolescents studied. The central apneas demonstrated in our study were associated with desaturation below 90070 in only 1 child. Thus, although central apneas ~ 10 sin duration occur frequently in normal children, they rarely appear to cause physiologic impairment of gas exchange. Central apneas have been studied in detail in neonates and infants. Central apneas are considered pathologic in infants if they are >20 s in duration or are of shorter duration but are associated with cyanosis or bradycardia (6). However, central apneas ~ 20 s are of uncertain clinical significancein older children (14). Few studies have evaluated central apneas in children older than 1 yr. Carskadon and colleagues (15) studied 22 children aged 9 to 13yr. They showed that central apneas of more than 5 s in duration occurred frequently, with the longest recorded central apnea being 25 s in duration. Of all apneas in that study, 55070 occurred following movement. Tabachnik and coworkers (16)studied 9 adolescents and found that subjects had an average of 5.5 central apneas > 10 s in duration per night (range 0 to 22). The longest duration of a central apnea was 24 s. However, all non-rapid eye movement (non-REM) central apneas occurred in association with sighs or movement. We noted fewer central apneas in our study than in those cited. However,
MARCUS, OMLlN, BASINKI, ET AL.
it is difficult to compare our results with the other studies. Our study population was younger than the other populations. In addition, different parameters were used to assesscentral apneas in the different studies. We did not quantitate central apneas following movement in our study because these occurred very frequentlyand probably represent a normal phenomenon. In addition, motion artifact occasionally obscured a portion of the recording. Based on the present study, we recommend that central apneas in the pediatric age group be considered abnormal if they are associated with desaturation below 90%, irrespective of the length of the apnea. Normal end-tidal carbon dioxide tension values during sleep have not been established for children and adolescents. Conventionally, PETc02 > 45 mm Hg has been considered abnormal (1). Because children with the obstructive sleep apnea syndrome frequently have persistent hypopneas with hypoventilation rather than clear-cut obstructive apneas (1, 8), it is important to define normal sleeping values for PETC 0 2 for the pediatric age group. In this study, PETC02 was frequently > 45 mm Hg and was occasionally> 50 mm Hg. The duration of total sleep time during which PETC02 was > 45 mm Hg, although usually short, was as much as two-thirds of TST in some normal subjects. The duration of sleep time with PETC02 > 45 mm Hg correlated only weakly with age. Based on these results, we recommend that a peak PETC0 2 > 53 rom Hg, or PETC02 > 45 mm Hg for more than 60070 of TST, be considered abnormal in the pediatric age group. In this study, only one subject desaturated below 90070. There was no difference in Sao, between boys and girls. It was previously suggested that a sleeping Sao, < 90070 be considered abnormal for children (1) and adults. Block and colleagues (17)showed that 13of 17normal men desaturated during sleep, with a mean ~Sao2 of 11 %. In the same study, no women desaturated. Catterall and coworkers (3) demonstrated a mean sleeping Sao, nadir of 91 to 92070 in healthy adult men and women, with a tendency for Sao, to fall with increasing age in both sexes. Previous studies in adolescents demonstrated sleeping Sao, nadirs of 96.1 ± 0.6 and 96.6 ± 1.5070, with ~Saoz 2.2 ± 1.2070 (16, 18).Our study confirms these findings and extends them to preadolescents. On the basis of this study,
we recommend that Sao, values < 92070 be considered abnormal for both males and females in the pediatric age group. Because the respiratory system in infants differs from that in older children and infants have been studied extensively by others (9), we chose not to include infants < 1 yr of age in this study. The results of this study therefore cannot be extrapolated to infants. The TST during the study period was reduced (19,20). This was probably a result of the unfamiliar environment of the sleep laboratory. No bias in the timing of the recordings was discerned. Because sleep was staged byEOG and behavioral criteria alone, it is possible that some quiet drowsiness was misinterpreted as sleep, and vice versa. The clinical significance of the abnormal values defined in this study has yet to be determined. Although all study subjects were asymptomatic, six of the children in this study had an abnormal value. In all cases, only a single parameter, or permutations of a single parameter (Sao.), fell in the abnormal range. Thus, patients with abnormal polysomnograms may not necessarily require treatment, and clinical judgment is required. In summary, this study has defined normal polysomnographic values for children (older than infancy) and adolescents. Further studies to determine sleep state-specific normal values may be desirable. Criteria for diagnosing sleepdisordered breathing in adults should not be applied to children and adolescents because they may result in underdiagnosis in the pediatric age group. Acknowledgment The writers thank Michael W. Stabile, M.S., R.P.F.T., Amma B. Amihyia, M.Sc., and Kate T. Tannenbaum, B.S., C.P.F.T. for technical assistance; Linda S. Chan, Ph.D. for statistical assistance; and the children and their parents for their enthusiastic participation in this study.
References 1. Brouillette RT, Weese-Mayer DE, Hunt CEo Disorders of breathing during sleep in the pediatric population. Semin Respir Med 1988; 9:594-606. 2. Berry nrs, Webb WB, Block AI. Sleep apnea syndrome. A critical review of the apnea index as a diagnostic criterion. Chest 1984; 86:529-31. 3. Catterall JR, Calverley PMA, Shapiro CM, Flenley DC, Douglas NJ. Breathing and oxygenation during sleep are similar in normal men and normal women. Am Rev Respir Dis 1985; 132:86-8. 4. Kleinman RE. Obesity. In: Rudolph A, ed. Pediatrics. Norwalk, CT: Appleton & Lange, 1987; 206.
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NORMAL POLYSOMNOGRAPHY IN CHILDREN
5. Brouillette R, Hanson D, David R, et al. A diagnostic approach to suspected obstructive sleep apnea in children. J Pediatr 1984; 105:10-4. 6. American Academy of Pediatrics Task Force on Prolonged Apnea. Prolonged apnea. Pediatrics 1978; 61:651-2. 7. Guilleminault C. Obstructive sleep apnea and its treatment in children: areas of agreement and controversy. Pediatr Pulmonol 1987; 3:429-36. 8. Rosen CL, D'Andrea G, Haddad G. Adult criteria for obstructive sleep apnea do not identify serious airway obstruction in children (abstract). Am Rev Respir Dis 1991; 143:A388. 9. Gaultier C. Respiratory adaption during sleep from the neonatal period to adolescence. In: Guilleminault C, ed. Sleep and its disorders in children. New York: Raven Press, 1987; 67-97. 10. American Thoracic Society. Indications and standards for cardiopulmonary sleep studies. Am Rev Respir Dis 1989; 139:559-68.
11. Guilleminault C, van den Hoed J, Mitler MM. Clinical overview of the sleep apnea syndromes. In: Guilleminault C, Dement WC, eds. Sleep apnea syndromes. New York:Alan R Liss, 1978;1-12. 12. Schmidt-Nowara WW, Jennum P. Epidemiology of sleep apnea. In: Guilleminault C, Partinen M, eds. Obstructive sleepapnea syndrome. New York: Raven Press, 1990; 1-8. 13. Brouillette RT, Morrow S, Weese-Mayer DE, Hunt CEo Comparison of respiratory inductive plethysmography and thoracic impedance for apnea monitoring. J Pediatr 1987; 111:377-83. 14. Weese-Mayer DE, Morrow AS, Conway LP, Brouillette RT,Silvestri JM. Assessing clinical significance of apnea exceeding fifteen seconds with event recording. J Pediatr 1990; 117:568-74. 15. Carskadon MA, Harvey K, Dement WC, Guilleminault C, Simmons FB, Anders TF. Respiration during sleep in children. West J Med 1978; 128:477-81.
16. Tabachnik E, Muller NL, Bryan AC, Levison H. Changes in ventilation and chest wall mechanicsduring sleepin normal adolescents. J Appl Physiol 1981; 51:557-64. 17. Block AJ, Boysen PG, Wynne JW, Hunt LA. Sleep apnea, hypopnea and oxygen desaturation in normal subjects. NEngl J Med 1979;300:513-7. 18. Chipps BE, Mak H, Schuberth KC, Talamo JH, Menkes HA, Scherr MS. Nocturnal oxygen saturation in normal and asthmatic children. Pediatrics 1980, 65:1157-60. 19. Carskadon MA, Keenan S, Dement WC. Nighttime sleep and daytime sleep tendency in preadolescents. In: Guilleminault C, ed. Sleep and its disorders in children. New York: Raven Press, 1987; 43-52. 20. Carskadon MA, HarveyK, Dement WC. Sleep loss in young adolescents. Sleep 1981; 4:299-312.
CAROLE L. MARCUS,4 KENNETH J. OMLlN, DANIEL J. BASINKI, SANDRA L. BAILEY, ADRIANA B. RACHAL, WALTER S. VON PECHMANN, THOMAS G. KEENS, and SALLY L. DAVIDSON WARD
Introduction
Polysomnography
is routinely performed to evaluate children and adolescents with sleep-disordered breathing. However, normal respiratory polysomnographic values for the pediatric age group have not yet been established. Although pediatric polysomnographic guidelines for diagnosing sleep-disordered breathing have been stated in the literature (1), few data are available regarding normal respiratory parameters during sleep in healthy children and adolescents. The use of adult criteria to evaluate children and adolescents with suspected sleep-disorderedbreathing may not be valid. The apnea index in asymptomatic adults increases with advancing age (2). Similarly, sleeping Sa02 values in normal adults tend to fall with increasing age (3). Thus, the normal respiratory pattern and gas-exchange values for healthy, asymptomatic children and adolescents are expected to differ from those of adults. Wetherefore performed polysomnography in 50 healthy children and adolescents in order to establish normal polysomnographic values. Methods Patient Selection Normal, healthy children and adolescents ranging in age from 1 to 18 yr were studied. Children were recruited from families of hospital employees. Children with significant medical problems requiring chronic medication or with a history of adenoidectomy, tonsillectomy, or other airway surgery were excluded. The height and weight were obtained for each child, and growth percentiles were obtained using standard growth charts (National Center for Health Statistics, adapted by Ross Laboratories, Columbus, OH). The body mass index (BMI) was defined as the weight in kilograms divided by the height in meters squared. Obese children and adolescents, defined as those with weights greater than 120070 of the ideal weight for height (4), were excluded.
SUMMARY Although polysomnography Is routinely performed to evaluate children and adolescents with sleep-disordered breathing, normal polysomnographic values for the pediatric age group have not yet been established. We therefore performed overnight polysomnography In 50 normal children and adolescents (mean age 9.7 ± 4.6 SO yr, range 1.1 to 17.4 yr). Of the children 56% were male. Chest wall motion, ECG, oronasat airflow, end-tidal PC02(PETC02), arterial oxygen saturation (Sa02), and electrooculogram were monitored. Children had 0.1 ± 0.5 (range 0 to 3.1) obstructive apneas per hour of total sleep time, with only 18% of children having any obstructive apneas. No child had obstructive apneas > 10 s In duration. Of the children 30% had central apneas ~ 10 s In duration, and one child had a central apnea associated with Sa02 < 90%. Peak PETC02 was 46 ± 4 mm Hg (range 38 to 53 mm Hg), and hypoventllatlon (PETC02 > 45 mm Hg) occurred for 7 ± 19% total sleep time (range 0 to 91%). The Sa02 nadir was 96 ± 2% (range 89 to 98%), with only one child desaturatlng below 90% in association with a central apnea. we conclude that polysomnographlc results In the pediatric age group differ from those in adults. Recommendations for normal polysomnographlc criteria are given. AM REV RESPIR DIS 1992; 146:1235-1239
Questionnaire A standard questionnaire regarding symptoms of obstructive sleep apnea syndrome, devised by Brouillette and colleagues (5), was administered to the parents of each child. Based on Brouillette's data, no subject with a questionnaire score < -1 would be expected to have obstructive sleep apnea syndrome, whereas a score between -1 and 3.5 is considered indeterminate and a score> 3.5 is considered highly predictive of obstructive sleep apnea syndrome. Children with questionnaire scores > -1 were excluded from study. Polysomnography Polysomnographic studies were performed overnight, in a quiet, dark room with an ambient temperature of 24 0 C. No sedation or sleep deprivation was used. Preadolescent children were accompanied by one parent throughout the night. During polysomnography, the following parameters were measured and recorded continuously on a Gould 16-channel strip-chart recorder (Gould, East Lake, OH): 1. Chest wall motion was measured by thoracic impedance or Respitrace (Ambulatory Monitoring, Inc., Ardsley, NY). 2. Heart rate was measured by electrocardiography (ECG). 3. Inspired and end-tidal POz and Pco, (PETeoz), sampled at the nose at a rate of 60 ml/min, were measured by mass spectrometry (medical gas analyzer; Perkin-Elmer, Wilton, CT). The mass spectrometer was calibrat-
ed against primary-grade gasses at the beginning and end of each study. End-tidal Po, was calibrated using 100% N, and room air, and end-tidal Pco, was calibrated using 100010 Ns and a 10% COz and 90% Os gas mixture. 4. Airflow was sampled at the mouth with a thermistor (Physitemp, Clifton, NJ). 5. Arterial oxygen saturation (Saoz) was measured by pulse oximetry (N 200 pulse oximeter; Nellcor, Haywood, CAl.
(Received in original form June 24, 1991 and in revised form February 3, 1992) 1 From the Division of Neonatology and Pediatric Pulmonology, Children's Hospital of Los Angeles, University of Southern California School of Medicine, Los Angeles, California. 2 Supported in part by Grant No. 1 ROI HD22696-01Al from the National Institute of Child Health and Human Development; the National Center for the Prevention of Sudden Infant Death Syndrome, Baltimore; the Greater Los Angeles and Washington State chapters of the National Sudden Infant Death Syndrome Alliance; the Los Angeles County, Orange County, Inland Empire, and Kern County chapters of the Guild for Infant Survival; the Junior Women's League of Orange County; and the Ruth and Vernon Taylor Foundation. 3 Correspondence and requests for reprints should be addressed to Carole L. Marcus, M.D., Johns Hopkins Hospital, Division of Pediatric Pulmonology, Park 316, 600 North Wolfe Street, Baltimore, MD 21205. 4 Recipient of a Children's Hospital of Los Angeles Fellowship Support Grant.
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6. Oximeter pulse waveform was recorded. 7. Transcutaneous P0 2and Pco, were measured using a heated (43 0 C) transcutaneous oxygen electrode (Transend'" cutaneous gas system; Sensorlvledics, Yorba Linda, CA). Trends of transcutaneous values were used to confirm PETc02 and Sao, values. 8. Electrooculograph (EOG) was recorded. Children were also monitored and recorded on videotape using an infrared video camera. The children were continuously observed by a technician trained in polysomnography. Observations ofthe child's sleep behavior and respiratory events were recorded directly on the strip-chart paper by the technician. The following parameters were evaluated: 1. Obstructive apneas were defined as the
presence of chest wall motion associated with the absence of airflow detection by both the end-tidal catheter at the nose and the thermistor at the mouth. The number and duration of obstructive apneas of any length were quantitated. The apnea index, defined here as the number of obstructive apneas of any length per hour 0 f sleep, was calculated for each subject. Because standardized methods for defining hypopneas in children have not been defined, we did not quantitate hypopneas. 2. Central apneas were defined as the absence of chest wall motion associated with absence of airflow detection by both the endtidal catheter at the nose and the thermistor at the mouth. The number of central apneas ~ 10 s was quantitated. Central apneas of any length that were associated with desaturation were quantitated separately. Central apneas occurring immediately following gross body movements were not quantitated. Central apneas occurring immediately after sighs were quantitated separately. 3. Mixed apneas were defined as apneas having both central and obstructive components, with the central component ~ 4 s duration or twice the respiratory cycle length for that subject and the obstructive component being of any length. The number and duration of mixed apneas were quantitated. 4. Periodic breathing was defined as three or more respiratory pauses of> 3 s duration with < 20 s of normal respiration between pauses (6). The length of the run of periodic breathing and the lowest arterial oxygen saturation associated with the periodic breathing were quantitated. 5. The lowestand highest Sao, and the number of desaturations > 4070 were quantitated. The total duration of desaturation (Sa0 2 < 90%) expressed as a percentage of total sleep time (TST) was quantitated. ASao2 was defined as the difference between the peak and nadir Sao, during sleep. Measurements associated with poor pulse tracings were discarded. 6. The lowest and highest PETC02 were quantitated. The total duration of time during which PETC02 was> 45 mm Hg and the total duration of time during which PETC02 was > 50 mm Hg, expressed as percentages
MARCUS, OMLlN, BASINKI, ET AL.
of TST, were quantitated. APETC02 was defined as the difference between the peak and nadir PETC02 during sleep. Transient (one to two breaths) increases in PETc 02 immediately following gross body movements were not quantitated because they were not representative of the subject's baseline ventilation and because the recording was occasionally obscured by motion artifact. An elevation in PETCO2 in the breath immediately following a sigh was not considered representative of the subject's baseline ventilation and was therefore quantitated separately. 7. Total sleep time was quantitated, and respiratory parameters were expressed as a percentage of TST. Sleep was based on behavioral observations and electrooculographic criteria. Respiratory parameters were not quantitated during periods of wakefulness.
Statistical Methods All data are expressed as mean ± standard deviation (SD) when appropriate. Recommendations for normal values were calculated from the mean plus twice the standard deviation when parameters followed a normal distribution. For data that were not normally distributed and were one tailed, we chose a normal range that included 97.5% of the subjects.
Results
A total of 50 children and adolescents were studied. Ages ranged from 1.1 to 17.4 yr, with a mean age of 9.7 ± 4.6 yr. The age distribution is shown in figure 1; 28 (56070) were male. Distribution by ethnic group was as follows: 25 (50%) children were non-Hispanic white, 13 (26%) wereHispanic, 5 (10070) wereblack, 4 (8%) were Asian, and 3 (6070) were Native American. Mean body mass index was 18.6 ± 3.2 (range 11.6to 26.3) kg/m', No child was obese. One child occasionally received nocturnal nasal desmopressin acetate (DDAVP) as treatment for enuresis. Three children were completing courses of antibiotics for otitis media at the time of study but were considered by their parents to be at the baseline level of health. Four children had a history consistent with symptoms of mild allergic rhinitis; none of these children were symptomatic or requiring treatment at the time of study. The mean score on the questionnaire was - 3.2 ± 0.1. All children had scores < -1. Duration of TST was 6.0 ± 1.6 h. A portion of a typical tracing, detailing the cardiorespiratory parameters, is shown (figure 2). Polysomnographic results are shown in table 1. Obstructive apneas were uncommon. A total of 9 (18%) children had one or more obstructive apneas (table 2). A total of six were male. No child had ob-
o
1
2 8 9 10 11 12 13 14 --'----"------~'---------.---------~-----
AGE (years)
Fig. 1. The number of SUbjectsstudied of each year of age are shown.
structive apneas > 10s in duration. There was no correlation between apnea index and age (r = -0.14, not significant [NS]) or apnea index and BMI (r = - 0.07, NS). Of the four children with histories of mild allergic rhinitis three had obstructive apneas. One child had an apnea index of 3.1. The child was asymptomatic and had a questionnaire score of - 3.83. However, she had an older sibling who was being treated for severe obstructive sleep apnea syndrome. In 15 (30070) children one to five central apneas ~ 10 s in duration occurred and were 10 to 18 s long. In addition, 1 child desaturated to 89070 during a 9-s central apnea. No other children desaturated below 90%. Saturation values during central apneas were not obtained for 1 child because of motion artifact. Children with central apneas ranged from 1.3 to 16.9 yr of age, and 56% were girls. Central apneas following sighs were quantitated separately. The mean longest central apnea following a sigh was 13 ± 6 s (range 5 to 26 s). No mixed apneas occurred in any children or adolescents. Periodic breathing occurred in 4 (8070) children and lasted for 0.4 to 5.7 min. Periodic breathing was associated with saturation values of 92 to 97%. Peak PETC02 was 46 ± 4 (range 38 to 53) mm Hg (table 1); 21 (42070) children had PETC02 > 45 mm Hg, and 3 children had PETC02 > 50 mm Hg (figure 3). PETC02was> 45 mm Hg for 6.9 ± 19.1070 (range 0 to 90.5%) of TST and> 50 mm Hg for 0.5 ± 4% (range 0 to 25070) TST (figure 4). There was no correlation between duration of hypoventilation and age (r = 0.16, NS). There was a significant but weak correlation between peak PETC02 and age (r = 0.28, p < 0.05). The highest end-tidal PETC02in the breath immediately after a sigh was 44 ± 4 (range 36 to 51) mm Hg. The Sao, nadir was 96 ± 2% (range 89 to 98070). Only 1 child desaturated to
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NORMAL POLYSOMNOGRAPHY IN CHILDREN
-r r~
No. of subjects
10'---:-:--=--':"::=~--------------------,
#
;r
125r50r
PI
Fig. 2. A detail of a portion of a typical polysomnogram. Sa02, arterial oxygen saturation; PETc02, end-tidal carbon dioxide tension.
1~
Sa0 2
J
o~,m.I~~UI~~
m
0
wav.Fofm~ Chest Wall Impedance
38 39
40
4,
42
43 44
45
46
47
48
49
50
5,
52
53
Peak peo 2 (mm Hg)
NasalThermlSlor~
Fig. 3. The number of subjects at each level of peak end-tidal carbon dioxide tension are shown. The data are normally distributed.
TABLE 1 POLYSOMNOGRAPHIC VALUES*
No. of SUbjects
Mean ± SO Apnea index,t NIh Maximum PETC02, t mm Hg Minimum PETc02, mm Hg ~PETC02 t, mm Hg Duration of hypoventilation, (PETC02 > 45 mm Hg),t: % TST Maximum Sa02, % Minimum Sa02,t: % Desaturation > 4%/h TST,t: n ~Sa02,t %
Recommended Normal Values
Range
Children Classified Abnormal n (%)
0.1 46 38 7
± ± ± ±
0.5 4 3 3
0-3.1 38-53 28-44 2-11
" 13
1 (2) 0(0) NA 0
6.9 100 96 0.3
± ± ± ±
19.1 1 2 0.7
0-90.5 98-100 89-98 0-4.4
" 60% NA ~ 92 "1.4
3 (6) NA 2 (4) 1 (2)
"8
2 (4)
4±2
" 1 " 53 NA§
0-11
- The number of children classified as abnormal represents the number of children who would be judged to have an abnormality based on the recommended values. Apnea index is defined as the number N of obstructive apneas of any length per hour of sleep. t Recommended normal values based on mean :t: 2 SO when parameters follow a normal distribution. For data that are not normally distributed, the recommended normal values are based on inclusion of 97% of subjects tested for one-tailed distribution.
40~~=~----------------,
30
20
10
0 ..1
o
_
10
20
30
40
50
60
70
80
90
100
Duration of hypoventilation (pea 2 ) 45 mm Hg)
Fig. 4. The number of subjects at each duration of hypoventilation (end-tidal carbon dioxide tension> 45 mm Hg) are shown. Data not normally distributed, with a one-tailed configuration.
*
TABLE 2 CHARACTERISTICS OF SUBJECTS WITH OBSTRUCTIVE SLEEP APNEA (OSA)* Age (yr)
4.1t 4.2 4.6 6.3t: 12.6 13.0t: 14.5t: 16.9 16.9
n Sex
(OSAInight)
Apnea Index
Duration of Longest OSA (5)
F F M M M M M M F
12 1 2 1 1 2 1 2 1
3.1 0.2 0.3 0.2 0.2 0.3 0.3 0.3 0.2
10 6 10 5 5 3 6.5 4 5
- Characteristics of individual subjects with obstructive apneas are shown. Apnea index defined as number of obstructive apneas of any length per hour of sleep. t Sibling has obstructive sleep apnea syndrome. History of mild allergic rhinitis.
*
890/0 in association with a central apnea. No other child desaturated below 90%, and only 3 (60/0) children desaturated below 930/0. A total of 23 children had discrete episodes of desaturation >4070. The number of desaturations > 4%/h of sleep was 0.3 ± 0.7. The recommended normal values and the number of subjects who would be classified as abnormal based on these recommendations are shown in table 1. A total of 6 subjects had at least one ab-
normal parameter. Of these 6 subjects four had a single abnormal parameter. The fifth subject had a Sao, nadir < 92% and a dSao;z > 8070, and the sixth subject had a Sao, nadir < 92%, dSao;z > 8%, and more than 1.4desaturations >4%/h TST. Discussion
This study has defined normal polysomnographic values for children older than
infancy and for adolescents. Despite the increasing use of polysomnography in pediatrics, previous polysomnographic data in the pediatric age range have been scanty, From this study, it appears that adult polysomnographic criteria cannot be extrapolated to children and adolescents. Obstructive apneas occurred rarely in the children and adolescents in this study and werenever> 10s in duration. Therefore, this study has provided objective evidence for the statements by previous researchersthat obstructive apneas of any length are rare in children (7-9). This is in contrast to adults. In adults, the apnea index is commonly used to evaluate obstructive sleep apnea, with the apnea index defined as the number of obstructive apneas > 10 s in duration per hour of sleep (10). Obstructive apneas ~ 10 s in duration are not quantitated. The apnea index in asymptomatic adults increases with advancing age (2). Thus, some authorities consider an apnea index < 5 as normal for adults (11), whereas others consider an apnea index < 10 to be normal (12). In the present study, the apnea index (for apneas of any length) in children and adolescents was 0.1 ± 0.5. Clearly, therefore, adult criteria cannot be applied to children and
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adolescents. We recommend that more than one obstructive apnea of any length per hour of sleep be considered abnormal for the pediatric age group. However, the clinical significance of short apneas in children has not yet been ascertained. In this study, chest wall motion was measured by either thoracic impedance or respiratory inductive plethysmography. Impedance monitors do not directly detect chest wall motion. Although used frequently to monitor respiration, thoracic impedance monitors have been reported occasionally to detect cardiac artifact falsely as chest wall motion and therefore miss apneas (13). However, ECG artifact was not seen in any of the tracings in this study (figure 2). All subjects were continually observed by a trained polysomnography technician throughout the study, and videotapes were reviewedafter the study. There were no instances in which obstructive apneas were missed by monitoring but detected by direct observation. Central apneas occurred frequently in the normal children and adolescents studied. The central apneas demonstrated in our study were associated with desaturation below 90070 in only 1 child. Thus, although central apneas ~ 10 sin duration occur frequently in normal children, they rarely appear to cause physiologic impairment of gas exchange. Central apneas have been studied in detail in neonates and infants. Central apneas are considered pathologic in infants if they are >20 s in duration or are of shorter duration but are associated with cyanosis or bradycardia (6). However, central apneas ~ 20 s are of uncertain clinical significancein older children (14). Few studies have evaluated central apneas in children older than 1 yr. Carskadon and colleagues (15) studied 22 children aged 9 to 13yr. They showed that central apneas of more than 5 s in duration occurred frequently, with the longest recorded central apnea being 25 s in duration. Of all apneas in that study, 55070 occurred following movement. Tabachnik and coworkers (16)studied 9 adolescents and found that subjects had an average of 5.5 central apneas > 10 s in duration per night (range 0 to 22). The longest duration of a central apnea was 24 s. However, all non-rapid eye movement (non-REM) central apneas occurred in association with sighs or movement. We noted fewer central apneas in our study than in those cited. However,
MARCUS, OMLlN, BASINKI, ET AL.
it is difficult to compare our results with the other studies. Our study population was younger than the other populations. In addition, different parameters were used to assesscentral apneas in the different studies. We did not quantitate central apneas following movement in our study because these occurred very frequentlyand probably represent a normal phenomenon. In addition, motion artifact occasionally obscured a portion of the recording. Based on the present study, we recommend that central apneas in the pediatric age group be considered abnormal if they are associated with desaturation below 90%, irrespective of the length of the apnea. Normal end-tidal carbon dioxide tension values during sleep have not been established for children and adolescents. Conventionally, PETc02 > 45 mm Hg has been considered abnormal (1). Because children with the obstructive sleep apnea syndrome frequently have persistent hypopneas with hypoventilation rather than clear-cut obstructive apneas (1, 8), it is important to define normal sleeping values for PETC 0 2 for the pediatric age group. In this study, PETC02 was frequently > 45 mm Hg and was occasionally> 50 mm Hg. The duration of total sleep time during which PETC02 was > 45 mm Hg, although usually short, was as much as two-thirds of TST in some normal subjects. The duration of sleep time with PETC02 > 45 mm Hg correlated only weakly with age. Based on these results, we recommend that a peak PETC0 2 > 53 rom Hg, or PETC02 > 45 mm Hg for more than 60070 of TST, be considered abnormal in the pediatric age group. In this study, only one subject desaturated below 90070. There was no difference in Sao, between boys and girls. It was previously suggested that a sleeping Sao, < 90070 be considered abnormal for children (1) and adults. Block and colleagues (17)showed that 13of 17normal men desaturated during sleep, with a mean ~Sao2 of 11 %. In the same study, no women desaturated. Catterall and coworkers (3) demonstrated a mean sleeping Sao, nadir of 91 to 92070 in healthy adult men and women, with a tendency for Sao, to fall with increasing age in both sexes. Previous studies in adolescents demonstrated sleeping Sao, nadirs of 96.1 ± 0.6 and 96.6 ± 1.5070, with ~Saoz 2.2 ± 1.2070 (16, 18).Our study confirms these findings and extends them to preadolescents. On the basis of this study,
we recommend that Sao, values < 92070 be considered abnormal for both males and females in the pediatric age group. Because the respiratory system in infants differs from that in older children and infants have been studied extensively by others (9), we chose not to include infants < 1 yr of age in this study. The results of this study therefore cannot be extrapolated to infants. The TST during the study period was reduced (19,20). This was probably a result of the unfamiliar environment of the sleep laboratory. No bias in the timing of the recordings was discerned. Because sleep was staged byEOG and behavioral criteria alone, it is possible that some quiet drowsiness was misinterpreted as sleep, and vice versa. The clinical significance of the abnormal values defined in this study has yet to be determined. Although all study subjects were asymptomatic, six of the children in this study had an abnormal value. In all cases, only a single parameter, or permutations of a single parameter (Sao.), fell in the abnormal range. Thus, patients with abnormal polysomnograms may not necessarily require treatment, and clinical judgment is required. In summary, this study has defined normal polysomnographic values for children (older than infancy) and adolescents. Further studies to determine sleep state-specific normal values may be desirable. Criteria for diagnosing sleepdisordered breathing in adults should not be applied to children and adolescents because they may result in underdiagnosis in the pediatric age group. Acknowledgment The writers thank Michael W. Stabile, M.S., R.P.F.T., Amma B. Amihyia, M.Sc., and Kate T. Tannenbaum, B.S., C.P.F.T. for technical assistance; Linda S. Chan, Ph.D. for statistical assistance; and the children and their parents for their enthusiastic participation in this study.
References 1. Brouillette RT, Weese-Mayer DE, Hunt CEo Disorders of breathing during sleep in the pediatric population. Semin Respir Med 1988; 9:594-606. 2. Berry nrs, Webb WB, Block AI. Sleep apnea syndrome. A critical review of the apnea index as a diagnostic criterion. Chest 1984; 86:529-31. 3. Catterall JR, Calverley PMA, Shapiro CM, Flenley DC, Douglas NJ. Breathing and oxygenation during sleep are similar in normal men and normal women. Am Rev Respir Dis 1985; 132:86-8. 4. Kleinman RE. Obesity. In: Rudolph A, ed. Pediatrics. Norwalk, CT: Appleton & Lange, 1987; 206.
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NORMAL POLYSOMNOGRAPHY IN CHILDREN
5. Brouillette R, Hanson D, David R, et al. A diagnostic approach to suspected obstructive sleep apnea in children. J Pediatr 1984; 105:10-4. 6. American Academy of Pediatrics Task Force on Prolonged Apnea. Prolonged apnea. Pediatrics 1978; 61:651-2. 7. Guilleminault C. Obstructive sleep apnea and its treatment in children: areas of agreement and controversy. Pediatr Pulmonol 1987; 3:429-36. 8. Rosen CL, D'Andrea G, Haddad G. Adult criteria for obstructive sleep apnea do not identify serious airway obstruction in children (abstract). Am Rev Respir Dis 1991; 143:A388. 9. Gaultier C. Respiratory adaption during sleep from the neonatal period to adolescence. In: Guilleminault C, ed. Sleep and its disorders in children. New York: Raven Press, 1987; 67-97. 10. American Thoracic Society. Indications and standards for cardiopulmonary sleep studies. Am Rev Respir Dis 1989; 139:559-68.
11. Guilleminault C, van den Hoed J, Mitler MM. Clinical overview of the sleep apnea syndromes. In: Guilleminault C, Dement WC, eds. Sleep apnea syndromes. New York:Alan R Liss, 1978;1-12. 12. Schmidt-Nowara WW, Jennum P. Epidemiology of sleep apnea. In: Guilleminault C, Partinen M, eds. Obstructive sleepapnea syndrome. New York: Raven Press, 1990; 1-8. 13. Brouillette RT, Morrow S, Weese-Mayer DE, Hunt CEo Comparison of respiratory inductive plethysmography and thoracic impedance for apnea monitoring. J Pediatr 1987; 111:377-83. 14. Weese-Mayer DE, Morrow AS, Conway LP, Brouillette RT,Silvestri JM. Assessing clinical significance of apnea exceeding fifteen seconds with event recording. J Pediatr 1990; 117:568-74. 15. Carskadon MA, Harvey K, Dement WC, Guilleminault C, Simmons FB, Anders TF. Respiration during sleep in children. West J Med 1978; 128:477-81.
16. Tabachnik E, Muller NL, Bryan AC, Levison H. Changes in ventilation and chest wall mechanicsduring sleepin normal adolescents. J Appl Physiol 1981; 51:557-64. 17. Block AJ, Boysen PG, Wynne JW, Hunt LA. Sleep apnea, hypopnea and oxygen desaturation in normal subjects. NEngl J Med 1979;300:513-7. 18. Chipps BE, Mak H, Schuberth KC, Talamo JH, Menkes HA, Scherr MS. Nocturnal oxygen saturation in normal and asthmatic children. Pediatrics 1980, 65:1157-60. 19. Carskadon MA, Keenan S, Dement WC. Nighttime sleep and daytime sleep tendency in preadolescents. In: Guilleminault C, ed. Sleep and its disorders in children. New York: Raven Press, 1987; 43-52. 20. Carskadon MA, HarveyK, Dement WC. Sleep loss in young adolescents. Sleep 1981; 4:299-312.
