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Sleep Medicine 12 (2011) 542–549

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Sleep Medicine
journal homepage: www.elsevier.com/locate/sleep

Original Article

Normative values of polysomnographic parameters in childhood


and adolescence: Quantitative sleep parameters
Sabine Scholle a,⇑, Uta Beyer b, Michael Bernhard c, Stephan Eichholz d, Thomas Erler e, Petra Graneß f,
Barbara Goldmann-Schnalke g, Katharina Heisch h, Frank Kirchhoff i, Karsten Klementz j, Gerhard Koch k,
Annmarie Kramer l, Christoph Schmidtlein m, Barbara Schneider n, Birgit Walther o, Alfred Wiater p,
Hans Christoph Scholle q
a
Zentrum für Schlaf- und Beatmungsmedizin, Robert-Koch-Krankenhaus Apolda GmbH, Apolda, Germany
b
O.v. Guericke-Universität, Klinik für Allgemeine Pädiatrie und Neonatologie, Magdeburg, Germany
c
Zentrum für Kinderheilkunde und Jugendmedizin, Universitätsklinikum Gießen und Marburg GmbH, Marburg, Germany
d
Städt. Krankenhaus, Dresden-Neustadt, Germany
e
Carl-Thiem-Klinikum Cottbus gGmbH, Cottbus, Germany
f
Neuropädiatrie/SPZ, Helios-Klinikum, Berlin Buch, Germany
g
Eichsfeld Klinikum gGmbH, Heiligenstadt, Germany
h
Klinik für Kinder- und Jugendmedizin, TU Dresden, Dresden, Germany
i
Schlaflabor, Abt. Neonatologie und Neonatologische Intensivmedizin, Klinikum Südstadt, Rostock, Germany
j
Zentrum für Kinder-und Jugendmedizin, Klinikum ‘‘E.v. Bergmann’’, Potsdam, Germany
k
AKH gGmbH, Kinderklinik, Hagen, Germany
l
Klinik für Kinder-u. Jugendmedizin Lindenhof, Sana Klinikum Berlin Lichtenberg, Berlin, Germany
m
Kinderklinik Dritter Orden, Passau, Germany
n
Kinderkrankenhaus St. Marien, Landshut, Germany
o
Kinderklinik, Kreiskrankenhaus Rendsburg, Germany
p
Kinderklinik, Krankenhaus Porz am Rhein gGmbH, Köln, Germany
q
FB Motorik, Pathophysiologie und Biomechanik der Klinik für Unfall-, Hand-und Wiederherstellungschirurgie, Universitätsklinikum Jena, Germany

a r t i c l e i n f o a b s t r a c t

Article history: Objective: To provide normative values for sleep macroarchitecture of healthy children aged 1–18 years
Received 19 July 2010 using the AASM sleep scoring criteria, assessing the effects of gender, age, and Tanner pubertal stage.
Received in revised form 1 October 2010 Methods: One-night polysomnography was performed at subjects’ habitual bedtimes in 16 laboratories
Accepted 12 November 2010
on 209 healthy German children.
Available online 20 May 2011
Results: Normal values of sleep macrostructure show significant age dependencies (p < 0.05). Increasing
with age: awakening index, R latency (RL), sleep efficiency (SE) (total sleep time (TST)/sleep period time
Keywords:
(SPT)) and SE (TST/time in bed), stage N2, mean sleep cycle duration, number of stage shifts. Decreasing
Polysomnography
Sleep
with age: TST, SPT, wake after sleep onset, stage N3, stage R, movement time (MT), number of sleep
Sleep stages cycles. The following sleep parameters show a dependency on Tanner stages as well as corresponding
Child age (p < 0.05):TST, SPT, awakening index, R latency, stage N2, stage N3, MT, number of sleep cycles, mean
Adolescent sleep cycle duration. No gender dependencies were found.
Development Conclusion: The given study, considering AASM rules, shows the development of sleep in normal children
Normative values ages 1–18. Subject selection criteria and other factors influencing sleep as well AASM guideline modifi-
cations including scoring arousals in N2 and scoring MT as a measure of sleep fragmentation are
discussed.
Ó 2011 Elsevier B.V. All rights reserved.

1. Introduction

In the literature normative data on the evolution of sleep archi-


tecture across childhood are limited (Table 1). The introduction of
the new AASM guidelines for scoring sleep in 2007 [1], including
⇑ Corresponding author. Address: Centre of Sleep Medicine, Robert-Koch-Hospi-
rules for scoring pediatric sleep, necessitates establishing new
tal Apolda GmbH, D-99510 Apolda, Jenaer Straße 66, Germany. Tel.: +49 3644
571711; fax: +49 3644 571601. normative values. As shown for children by Novelli et al. [2] and
E-mail address: sl@rkk-apolda.de (S. Scholle). Miano et al. [3] and for adults by Moser et al. [4], results of sleep

1389-9457/$ - see front matter Ó 2011 Elsevier B.V. All rights reserved.
doi:10.1016/j.sleep.2010.11.011
Table 1
Sleep characterizing parameters of pediatric normative literature. Data are presented as mean ± standard deviation or range. Sleep was staged in accordance with rules of Rechtschaffen and Kales (R&K) [5] or AASM [1].

Parameter Subjects Age Age TST (min) WASO (% SPT) Sleep REM Sleep NonREM 1 NonREM 2 SWS NonREM 3 NonREM 4 REM
(n) (years) (range) latency latency efficiency (% TST) (% TST) (% TST) (% TST) (% TST) (% TST)
(min) (min) (TST/SPT)

Acebo et al. [12] 13 boys 13.3 ± 2.1 9.7–16.7 R&K 515 ± 55 6.8 ± 6.0 20 ± 12 159 ± 50 89.4 ± 7.5 8.4 ± 3.7 43.7 ± 10.9 8.8 ± 4.2 20.7 ± 8.5 17.7 ± 3.7
22 girls 13.8 ± 1.8 10.2–16.8 R&K 510 ± 36 4.6 ± 4.9 21 ± 12 161 ± 77 91.6 ± 5.2 6.9 ± 3.4 50.0 ± 7.8 7.9 ± 4.0 17.9 ± 5.0 16.8 ± 3.7

S. Scholle et al. / Sleep Medicine 12 (2011) 542–549


Scholle et. al. [13] 37 5.9 ± 1.8 2.4–7.0 R&K 526.0 ± 63.5 3.4 ± 5.8 139.0 ± 73.2 94.0 ± 8.2 4.7 ± 7.1a 38.0 ± 10.2a 10.0 ± 5.1a 19.0 ± 6.0a 16 ± 10a
60 9.9 ± 2.2 7.0–13.0 R&K 495.5 ± 65.0 5.1 ± 10.1 157.0 ± 86.0 89.0 ± 13.5 7.0 ± 8.8a 39.0 ± 7.5a 8.4 ± 4.1a 20.0 ± 7.5a 17.0 ± 5.5a
34 14.7 ± 1.8 13.1–17.6 R&K 465 ± 53.0 4.8 ± 7.4 145.5 ± 98.0 94.0 ± 9.0 9.3 ± 9.2a 47.5 ± 9.0a 8.6 ± 4.0a 14.0 ± 6.4a 12.0 ± 8.1a
Li et al. [14] 62 11.2 ± 2.2 R&K 542.3 ± 13.5 26.2 ± 23.6 129.6 ± 55.4 82.5 ± 10.3 5.8 ± 2.8 51.0 ± 7.4 7.1 ± 3.38 17.5 ± 7.7 18.6 ± 4.0
Traeger et al. [15] 66 6.6 ± 1.9 2.5–9.4 R&K 460 ± 54 23 ± 20 89 ± 8 4±3 44 ± 10 32 ± 10 10 ± 6 22 ± 8 21 ± 6
Uliel et al. [7] 70 7.9 ± 4.4 1.0–15.0 R&K 388 ± 74 90.8 ± 6.5 1.4 ± 4.1 48.9 ± 9.7 25.2 ± 9.1 17.4 ± 5.7
Montgomery- 153 3.2–5.9 R&K 475.2 ± 42.0 9.4 ± 7.3 24.1 ± 25.6 90.0 ± 7.0 6.6 ± 4.8 41.6 ± 7.1 6.6 ± 2.6 21.6 ± 6.2 23.6 ± 4.8
Downs et al. [16] 388 6.0–8.6 R&K 471.6 ± 43.7 8.1 ± 7.1 23.0 ± 25.3 132.0 ± 57.7 89.3 ± 7.5 7.1 ± 5.5 46.1 ± 8.5 5.5 ± 2.9 18.5 ± 6.6 22.6 ± 5.2
Verhulst et al. [9] 60 11.7 ± 2.6 7.1–16.6 R&K 426 ± 48 45.6 ± 29.4 118.8 ± 49.9 80.5 ± 8.5 2.3 ± 2.0 42.5 ± 7.2 8.9 ± 4.1 23.1 ± 6.5 23.2 ± 4.9
Mason et al. [17] 98 1–10 R&K 116 (13–392) 89(44–99) 5 (1–11) 48 (32–61) 29 (18–47) 16 (8–30)
>10–18 R&K 137 (45–329) 89 (53–98) 5 (1–19) 56 (33–73) 20 (1–44) 19 (5–31)
Tapia et al. [6] 15 10.1 ± 0.9 Tanner 1 AASM 19.0 (0–42.0) 154.5 (60.5–267.0) 85.0 (71–94) 6.8 ± 3.7 48.2 ± 4.2 26.1 ± 4.9 18.9 ± 4.4
10 10.9 ± 0.9 Tanner 2 AASM 22.5 (3.5–76.0) 102.0 (53–325) 86.0 (74–95) 4.5 ± 2.3 49.7 ± 7.3 27.8 ± 7.8 17.4 ± 5.0
7 12.3 ± 1.3 Tanner 3 AASM 14.0 (5.0–33.5) 194.5 (133.5–329) 87.0 (66–92) 5.3 ± 2.9 52.3 ± 8.6 25.4 ± 8.4 17.0 ± 6.4
19 14.7 ± 1.8 Tanner 4 AASM 14.5 (1.0–83.5) 136.5 (69.0–392.0) 89.0 (43–97) 6.7 ± 4.0 56.6 ± 7.2 18.9 ± 7.3 17.7 ± 4.5
17 16.1 ± 1.8 Tanner 5 AASM 16.5 (2.5–72.0) 116.5 (44.5–287.0) 89 (56–98) 6.9 ± 5.6 59.7 ± 7.9 15.7 ± 6.0 17.8 ± 5.7
Novelli et al. [2] 45 8.5 ± 3.2 3.0–16.0 AASM 516.6 ± 55.4 12.5 ± 21.9 28.1 ± 26.6 111.5 ± 43.8 90.9 ± 7.8 9.6 ± 3.4 45.6 ± 4.5 23.5 ± 4.9 21.3 ± 4.1
R&K 517.1 ± 54.9 13.9 ± 22.4 29.0 ± 26.7 111.9 ± 44.0 90.9 ± 8.0 3.6 ± 3.0 50.8 ± 4.9 22.6 ± 5.0 23.1 ± 4.1
Miano et al. [3] 10 7.2 ± 2.8 AASM 416.0 ± 40.7 4.4 ± 4.3 22.3 ± 21.8 90.8 ± 5.3 8.2 ± 5.3a 32.3 ± 9.6a 37.0 ± 3.7a 19.6 ± 4.5a
R&K 413.3 ± 40.6 4.7 ± 4.6 22.3 ± 21.5 90.2 ± 5.2 3.6 ± 2.8a 37.1 ± 9.0a 34.2 ± 4.7a 20.6 ± 3.7a
a
Percentage of sleep period time in each stage.

543
544 S. Scholle et al. / Sleep Medicine 12 (2011) 542–549

classification according to the American Academy of Sleep Medi- To eliminate socio-geographic influences on sleep only German
cine criteria (AASM) [1] and Rechtschaffen and Kales criteria [5] children of Caucasian ancestery were included in our study. In 16
are significantly different. At the present time there are only stud- German sleep laboratories on the day of polysomnography all sub-
ies by Tapia et al. [6], Novelli et al. [2] and Miano et al. [3] consid- jects underwent a standard physical examination. Furthermore in
ering the new AASM rules for sleep classification in childhood. children from 8 years of age upwards Tanner stage was determined
However, these studies and earlier ones considering Rechtschaffen clinically by the responsible physician.
and Kales criteria [5] (Table 1) do not include the full age spectrum Two hundred nine subjects were grouped by gender (112 fe-
from toddlers to adolescents and so fail to show age dependencies males, 97 males), age, and Tanner stage.
of polysomnographic data with much precision. Some studies There were 8 groups: (1) mean: 1.4 years old (range:1.0–1.9)
ignore the evolution of sleep architecture during childhood and n = 22; (2) 3.0 years old (2.1–3.6) n = 23; (3) 5.0 years old
only generally assess childhood sleep over a very wide age range, (4.1–5.9) n = 25; (4) 8.1 years old (6.0–11.6), including Tanner 1
for example, 1.0–15.0 years of age [7] or 3.0–16.0 years of age n = 34; (5) 11.5 years old (9.4–13.4), Tanner 2 n = 33; (6) 12.8 years
[2]. Furthermore, the number of subjects included in previous old (9.5–16.1), Tanner 3 n = 23; (7) 15.2 years old (13.0–17.9),
studies was usually too small to provide significant statements. Tanner 4 n = 24 and (8) 16.9 years old (14.0–18.0), Tanner 5
Ohayon et al. [8] have shown age related trends in a meta-anal- n = 25. Because in the first years of life the development of sleep
ysis of quantitative sleep parameters in children from 5 years of is rapid, the age range was defined in group 1 rather narrowly
age upwards. Limitations of this analysis exist because the used (toddlers 12–23 months), followed by group 2 (toddlers
instrumentation varied study to study. Furthermore there were of- 2.1–3.6 years of age) and group 3 (preschool-age children
ten small sample sizes and inconsistency in controlling factors 4.1–5.9 years of age). The 4th group included school-age children
influencing sleep. 6.0–11.6 years of age, some of whom were preadolescents of
The present study considering the AASM rules [1] first shows Tanner 1 stage. Thereafter grouping was done corresponding to
the development of sleep in the full age range from 1 to 18 years Tanner stages 2–5.
in a statistically relevant number of normal subjects. The study
considers changes in dependence of age and maturation (Tanner 2.2. Polysomnography
stages). Age groups are narrowly defined for precision. Children’s
habitual bedtimes were maintained and, despite the number of The habitual sleep schedule of the children was considered. All
sleep labs involved, conditions such as subject selection criteria, recordings started at the child‘s usual bedtime and ended at the
instrumentation and measurement techniques, and sleep scoring usual time of getting up in the morning. School children were
were consistent. To exclude interscorer variability polysomnog- studied on days without school the next day.
raphies were scored by the same expert sleep researcher through- In 16 different sleep labs PSGs were performed according to
out the entire investigation. So it should be possible to show the the same standards. The examinations were conducted in accor-
dependency of sleep data on gender, age, and maturity in more de- dance with AASM rules for technical performance and scoring
tail than in previous studies. of sleep [1].
During nocturnal PSG the following parameters were recorded:
referential electroencephalograms (EEG) F4M1, F3M2, C4M1,
2. Method C3M2, O2M1, O1M2, submental surface electromyogram (EMG),
referential electrooculograms (E1M2–E1 is placed 1 cm below the
2.1. Subjects left outer canthus, and E2M2–E2 is placed 1 cm above the right
outer canthus), bipolar surface EMG from the right and left tibialis
In a prospective study polysomnographies were performed in anterior muscle, electrocardiogram (ECG), heart rate from ECG
16 sleep labs in Germany during a 2 year period (2008–2009). (R–R triggered), nasal pressure, rib cage and abdominal move-
Healthy subjects aged 1–18 years were recruited for research pur- ments, oxygen saturation, snoring, body position, digital video.
poses only by means of advertisements in hospitals, neighboring The RembrandtÒ PSG system (Embla Systems GmbH) as well as
nursery schools and other schools, and in families of hospital Alice 5Ò (Heinen + Löwenstein GmbH) were used. Behavior was
employees. Children and adolescents were investigated for one night. observed and recorded directly by a technician.
According to Verhulst et al. [9] exclusion criteria were snoring,
increased respiratory effort with intercostal, epigastric or jugular 2.3. Analysis of polysomnographic recordings
retractions, a history of adenoidectomy and/or tonsillectomy and/
or other airway surgery, craniofacial anomalies, current orthodon- The computer-aided evaluation of all parameters was checked
tic treatment, asthma, allergic rhinitis, irregular sleep habits, manually (30 s epochs for sleep staging). Sleep was staged in accor-
frequent night terrors, sleep walking, nocturnal enuresis after the dance with AASM rules adapted for age [11]. To exclude interscorer
5th year of age, neurologic abnormalities, chronic illness or requir- variability visual scoring of all PSGs was performed by the same
ing chronic medication, endocrine dysfunctions, medication at experienced observer for all the studies. The scorer of all the stud-
time of investigation, acute disease on the day of polysomnography ies was blinded to gender, age, and Tanner stage.
and the week before. The following sleep scoring data were included: total sleep
The body mass index of the subjects included was in the gender time (TST), defined as SPT minus WASO; sleep period time
and age-specific percentile range from 10th to less than 90th. On (SPT), defined as time of sleep onset to the end of sleep, including
the basis of a German reference population Kromeyer-Hauschild all sleep epochs and wakefulness after sleep onset; wakefulness
et al. [10] proposed using the 90th BMI percentile to define the after sleep onset (WASO), defined as time spent awake between
cutoff point for overweight status in German children and adoles- the sleep onset and the end of sleep; number of awakenings
cents; 5.1% of our children had a BMI between 89 and 85th percen- per hour SPT; sleep latency defined as time between turning off
tile, the cut off point to identify overweight status in the United the lights to the first epoch of any sleep; R latency, defined as
States. No subject was under sedation or was sleep-deprived. time between sleep onset to the first R epoch. Sleep efficiency
A written informed consent was obtained from the parents and was calculated as TST divided by SPT and TST divided by the time
children/adolescents. The local ethics committees approved the in bed. The percentage of TST in each sleep stage (NREM 1-N1,
study. NREM 2-N2, slow wave sleep, including NREM 3 and 4-N3, and
S. Scholle et al. / Sleep Medicine 12 (2011) 542–549 545

Table 2
Sleep architecture parameters in different age groups and different stages of maturation. Data are presented as mean ± standard deviation (bold fonts) and range (minimum and
maximum values).

Group 1 2 3 4 5 6 7 8
n 22 23 25 34 33 23 24 25
Male/female 12 m 10f 10 m 13f 12 m 13f 17 m 17f 13 m 20f 7 m 16f 12 m 12f 14 m 11f
Age (years) 1.4 ± 0.3 2.9 ± 0.5 5.1 ± 0.5 8.1 ± 1.4 11.5 ± 1.2 12.8 ± 1.6 15.2 ± 1.4 16.9 ± 0.9
Stage of maturation Tanner 1 Tanner 2 Tanner 3 Tanner 4 Tanner 5
Total sleep time (min) 488.7 ± 87.1 489.7 ± 92.2 541.7 ± 67.3 512.2 ± 61.7 478.6 ± 53.7 477.5 ± 68.0 481.5 ± 46.2 452.1 ± 80.2
Range 338.5–634.0 258.0–615.5 421.0–659.0 382.5–667.0 402.5–608.5 374.0–608.5 401.5–567.5 293.5–624.0
Sleep period time (min) 555.5 ± 78.7 529.8 ± 83.7 564.6 ± 64.7 540.5 ± 62.0 504.0 ± 49.4 511.8 ± 64.9 502.5 ± 45.2 476.5 ± 84.1
Range 367.0–680.5 273.0–630.0 437.0–674.0 388.5–681.0 434.0–612.5 395.0–643.5 423.5–591.5 319.5–640.5
Wake after sleep onset (% SPT) 12.1 ± 8.1 7.7 ± 7.3 4.1 ± 3.2 5.1 ± 5.2 5.2 ± 4.9 6.7 ± 5.9 4.2 ± 3.7 5.1 ± 3.0
Range 1.8–32.0 0.2–24.7 0.1–12.6 0.1–17.1 0.0–23.5 0.4–21.5 0.0–14.1 1.4–13.2
Awakening index (n/h SPT) 1.1 ± 0.5 1.1 ± 0.5 1.0 ± 0.4 1.1 ± 0.6 1.3 ± 0.8 1.3 ± 0.5 1.3 ± 0.7 1.8 ± 0.8
Range 0.4–2.2 0.3–2.2 0.2–2.1 0.0–2.7 0.1–3.3 0.3–2.1 0.3–3.4 0.7–3.4
Sleep latency (min) 24.4 ± 29.7 33.1 ± 25.9 32.0 ± 30.5 21.8 ± 23.5 20.4 ± 19.6 34.3 ± 33.8 22.0 ± 21.7 22.6 ± 29.8
Range 2.5–126.5 2.0–100.5 0.0–99.5 1,5–84.0 0.0–82.5 3.0–132.5 1.0–84.0 1.5–151.0
R latency (min) 83.9 ± 36.6 100.2 ± 38.3 140.0 ± 57.5 155.1 ± 44.1 161.8 ± 42.3 125.2 ± 40.3 138.2 ± 54.5 132.7 ± 36.4
Range 33.5–152.0 43.5–176.5 59.5–254.0 66.5–232.5 66.5–236.5 67.0–229.5 57.5–285.5 59.5–200.5
Sleep efficiency (TST/SPT) 87.9 ± 8.1 92.2 ± 7.3 95.9 ± 3.2 94.8 ± 5.2 94.9 ± 5.2 93.3 ± 6.0 95.8 ± 3.7 94.9 ± 3.0
Range 68.0–98.2 75.3–99.8 87.4–99.9 82.9–100.0 76.5–100.0 78.5–100.7 85.9–100.0 86.8–100.9
Sleep efficiency (TST/TIB) 83.5 ± 7.9 86.0 ± 9.0 90.0 ± 6.5 89.6 ± 6.4 89.8 ± 5.6 85.7 ± 7.6 90.7 ± 6.0 88.9 ± 6.9
Range 65.6–96.3 66.2–98.5 72.5–97.6 74.0–99.7 73.5–98.3 62.8–95.6 77.7–98.5 69.5–98.4
N1 (% TST) 7.0 ± 3.3 7.3 ± 2.9 6.4 ± 4.1 6.7 ± 2.8 6.9 ± 4.1 7.6 ± 4.0 7.9 ± 5.1 7.7 ± 3.1
Range 1.3–13.6 3.1–15.6 0.9–16.8 1.9–13.7 1.9–19.5 2.1–17.8 1.8–20.0 2.1–13.8
N2 (% TST) 31.1 ± 7.6 29.6 ± 6.2 36.5 ± 7.4 38.6 ± 6.8 42.6 ± 5.0 42.2 ± 8.3 45.6 ± 7.9 49.4 ± 7.0
Range 16.6–42.1 18.3–40.9 19.4–50.4 24.7–54.6 32.0–51.8 28.9–58.6 29.9–60.3 35.8–62.6
N3 (% TST) 34.9 ± 8.6 38.4 ± 8.3 32.9 ± 7.1 31.9 ± 6.7 28.9 ± 5.2 28.6 ± 7.5 25.5 ± 4.7 22.9 ± 7.3
Range 20.8–51.9 25.2–58.0 23.1–46.9 15.2–51.6 17.0–40.1 17.3–48.0 16.9–37.4 9.3–39.8
R (% TST) 25.6 ± 4.0 23.2 ± 4.8 22.6 ± 3.8 21.1 ± 3.7 20.3 ± 4.5 20.3 ± 5.1 19.4 ± 3.9 19.0 ± 5.4
Range 16.3–33.6 12.8–32.2 15.0–29.6 12.0–28.4 11.2–30.0 10.0–28.4 13.7–30.7 10.3–28.3
Movement time (% TST) 1.5 ± 0.6 1.5 ± 0.8 1.6 ± 0.6 1.6 ± 0.7 1.4 ± 0.6 1.3 ± 0.5 1.6 ± 0.6 0.9 ± 0.5
Range 0.5–2.5 0.4–3.1 0.5–2.7 0.4–3.0 0.4–2.6 0.4–2.6 0.6–2.7 0.1–2.3
Movement time index (n/h TST) 1.7 ± 0.6 1.7 ± 1.0 1.8 ± 0.7 1.8 ± 0.7 1.5 ± 0.6 1.5 ± 0.6 1.8 ± 0.7 1.1 ± 0.6
Range 0.6–2.9 0.5–3.7 0.6–3.0 0.4–3.2 0.4–3.1 0.4–2.8 0.7–3.0 0.1–2.8
Number of stage shifts (n/h SPT) 8.5 ± 3.0 8.5 ± 1.5 9.3 ± 1.7 9.8 ± 1.6 9.7 ± 2.0 9.4 ± 1.8 10.7 ± 3.1 11.1 ± 1.9
Range 4.9–11.0 6.2–11.5 7.0–12.9 7.1–12.6 5.9–13.5 7.0–14.2 5.5–18.1 8.3–14.9
Sleep cycles (n/SPT) 7.5 ± 1.4 6.9 ± 1.3 6.6 ± 1.1 5.9 ± 0.9 5.3 ± 0.7 5.1 ± 0.9 5.1 ± 0.8 4.9 ± 1.0
Range 5.0–10.0 4.0–9.0 4.0–9.0 3.0–7.0 4.0–7.0 4.0–7.0 4.0–7.0 3.0–7.0
Mean sleep cycle duration (min) 64.7 ± 7.3 68.9 ± 7.2 79.2 ± 7.9 81.6 ± 8.3 82.5 ± 9.8 87.0 ± 11.9 88.9 ± 12.7 91.4 ± 10.9
Range 50.5–81.0 54.9–87.4 58.8–94.1 62.5–101.4 56.1–100.8 66.5–105.5 65.5–117.5 73.5–118.2

Table 3
Results of statistical analysis of different sleep architecture parameters. Normality of distribution (p > 0.05) and statistical significant correlations of sex, group and age to different
sleep parameters (p < 0.05) are marked by bold faced type. n = 209, age range 1–18 years of age. Age dependency (ad): + increasing with increasing age, decreasing with
increasing age.

Kolmogorov- Smirnov t-Test One-way ANOVA Linear regression ad


normality test sex differences group dependency age dependency
Group 0.022 0.908 x 0.000
Age (months) 0.020 0.909 0.000 x
Gender 0.000 x 0.595 0.908
TST (h) 0.180 0.391 0.001 0.005
SPT (h) 0.415 0.580 0.000 0.000
WASO (% SPT) 0.000 0.671 0.000 0.001
Awakening index (n/h SPT) 0.004 0.115 0.001 0.000 +
Sleep latency (min) 0.000 0.175 0.096 0.339
R latency (min) 0.672 0.401 0.000 0.000 +
Sleep efficiency (TST/SPT) 0.000 0.592 0.000 0.001 +
Sleep efficiency (TST/TIB) 0.069 0.679 0.001 0.022 +
N1 (% TST) 0.051 0.421 0.614 0.287
N2 (% TST) 0.631 0.606 0.000 0.000 +
N3 (% TST) 0.368 0.651 0.000 0.000
R (% TST) 0.982 0.611 0.000 0.000
MT (% TST) 0.206 0.406 0.012 0.015
MT index (n/hTST) 0.108 0.358 0.016 0.015
Sleep cycles (n/SPT) 0.000 0.528 0.000 0.000
Mean sleep cycle duration (min) 0.748 0.739 0.000 0.000 +
Number of stage shifts (n/h SPT) 0.677 0.078 0.005 0.000 +

REM-R) and movement time (MT) and MT index (n/h TST) was 2.4. Statistical analysis
measured. The number of stage shifts (n/h SPT), number of sleep
cycles (n/SPT), and mean sleep cycle duration were also SPSS version 11.5.1, 2001 (SPSS, Inc., Chicago, IL, USA) was used
computed. for statistical analysis.
546 S. Scholle et al. / Sleep Medicine 12 (2011) 542–549

600 Differences between age groups were tested by oneway


ANOVA; post hoc analysis was performed with Bonferroni-test.
500 The dependency of parameters on age was tested by linear regres-
SL sion. In groups 4–8 (n = 139) we compared Tanner stages and
400 WASO corresponding age in months in relation to sleep parameters by
[min]

300 MT Pearson correlation test.


N1 A probability value (p) of less than 0.05 was considered
200 N2 significant.
N3
100
REM
3. Results
0
s s s
ld ld ld r1 r2 r3 r4 r5 Two hundred nine subjects were grouped by gender (112
a r-o ar-o ar-o nne n ne nne nne nne females, 97 males), age and Tanner stage. Age and sex distribution
ye ye ye Ta Ta Ta Ta Ta
1 3 5 is shown in Table 2. All subjects were German Caucasians.
2- 4- s
ld Sleep architecture parameters according to age and Tanner
a r-o stage are shown in Table 2.
ye
-12 All sleep characterizing parameters beside WASO, awakening
6 index, SL, SE (TST/SPT) and number of sleep cycles are normally
Fig. 1. Age related trends from 1st year of age to 18th year of age of SL, WASO, MT, distributed (p > 0.05) (Table 3).
N1, N2, N3 and R in minutes. There were no differences in the parameters dependent on sex
(p < 0.05) (Table 3).
There was an age dependency of most sleep architecture
To determine the normality of distribution the Kolmogorov– parameters (p < 0.05) (Table 3, Figs. 1–3). Only SL and N1 were
Smirnov test was applied. The most quantitative sleep parameters not age dependent. With increasing age awakening index, RL, SE
demonstrated normal distributions (p > 0.05). Therefore values are (TST/SPT as well TST/TIB), N2, mean cycle duration and number
generally displayed as mean + standard deviation (SD). Further- of stage shifts increased (p < 0.05). The following parameters
more, parametric statistic tests were preferred. decreased with increasing age: TST, SPT, WASO, N3, R, MT, MT
Data were analysed based solely on gender, again based on index, number of sleep cycles (p < 0.05).
group, on age, and on Tanner staging. Sleep architecture according to Tanner stage and corresponding
Differences between males and females were investigated by age is shown in Table 4. There is a significant correlation (p < 0.05)
t-test. between Tanner stages and TST, SPT, awakening index, RL, N2, N3,

60 60

50 50

40 40
N2 [% TST]
N1 [% TST]

30 30

20 20

10 10

0 0
0 25 50 75 100 125 150 175 200 225 0 25 50 75 100 125 150 175 200 225
age [months] age [months]
Y = 6.641 + .004 * X; R^2 = .006 Y = 29.007 + .093 * X; R^2 = .417

60 60

50 50

40 40
N3 [% TST]

R [% TST]

30 30

20 20

10 10

0 0
0 25 50 75 100 125 150 175 200 225 0 25 50 75 100 125 150 175 200 225
age [months] age [months]
Y = 37.997 - .066 * X; R^2 = .264 Y = 24.733 - .03 * X; R^2 = .161

Fig. 2. Evolution of N1, N2, N3 and R in the range from 1 to 18 years of age: Results of the linear regression analysis.
S. Scholle et al. / Sleep Medicine 12 (2011) 542–549 547

120 11

110 10
sleep cycle duration [min]
100 9

sleep cycles [n]


8
90
7
80
6
70
5
60 4
50 3
40 2
0 25 50 75 100 125 150 175 200 225 0 25 50 75 100 125 150 175 200 225
age [months] age [months]
Y = 66.815 + .123 * X; R^2 = .386 Y = 7.379 - .013 * X; R^2 = .392

Fig. 3. Evolution of sleep cycle duration and the number of sleep cycles in the age range 1–18 years. Results of the linear regression analysis.

We did not find gender-by-age-group differences of sleep


Table 4
Results of Pearson correlation test (r) considering Tanner stages and corresponding parameters as reported by Montgomery-Downs et al. [16] for sleep
age in months in relation to sleep parameters. n = 139. The p < 0.05 is considered efficiency, WASO, % NREM 3 in 3–5-year-olds and % NREM 1 in 6–
statistically significant. Statistically significant correlations are marked by bold faced 7-year-olds (Table 1). Also Traeger et al. [15] did not describe dif-
type. ferences of sleep parameters based on gender.
Tanner 1–5 Age (months) As Ohayon et al. [8] outlined, changes in sleep patterns across
r p r p
childhood and adolescence are related not only to chronological
age but also to maturation stage. So we consider in the present
Group x x 0.902 0.000
Age (months) 0.902 0.000 x x
study the chronological age, and in adolescents the physiologic
Gender 0.073 0.395 0.103 0.227 age characterized by Tanner stages as well. It is interesting that
TST (h) 0.271 0.001 0.234 0.006 in the current study significant correlations of Tanner stages to
SPT (h) 0.297 0.000 0.259 0.002 sleep parameters are also reflected in significant correlations of
WASO (% SPT) 0.024 0.778 0.027 0.749
age to the same parameters (Table 4). Tapia et al. [6] prefer the
Awakening index (n/h SPT) 0.252 0.003 0.253 0.003
Sleep latency (min) 0.022 0.802 0.022 0.794 Tanner staging of adolescents to describe the development of sleep
R latency (min) 0.241 0.004 0.198 0.020 related data. As shown by our analyses the relation of Tanner
Sleep efficiency (TST/SPT) 0.018 0.838 0.020 0.819 stages and age in adolescence gives comparable results.
Sleep efficiency (TST/TIB) 0.016 0.854 0.013 0.881 The present study includes only single-night polysomnograph-
N1 (% TST) 0.100 0.245 0.089 0.300
N2 (% TST) 0.446 0.000 0.446 0.000
ies. Clinical diagnosis of children typically only involves one night
N3 (% TST) 0.435 0.000 0.418 0.000 of PSG recording [18], especially in searching for sleep related
R (% TST) 0.141 0.098 0.163 0.057 breathing disorders. This procedure neglects the first night effect
MT (% TST) 0.266 0.002 0.247 0.003 characterized in children with a night-to-night-variability in sleep
MT index (n/h TST) 0.229 0.007 0.210 0.013
parameters [8,9,14]. As shown in our own results [13], in the sec-
Sleep cycles (n/SPT) 0.348 0.000 0.351 0.000
Mean sleep cycle duration (min) 0.315 0.000 0.316 0.000 ond night the sleep efficiency is higher corresponding to less
Number of stage shifts (n/h SPT) 0.215 0.215 0.247 0.247 WASO, the proportion of N1 is lower, and proportion of R is higher.
The RL is comparable in the first and second night. First night effect
should to be considered if the normative data of the present study
are assessed.
MT, MT index, number of sleep cycles and mean sleep cycle
duration. We did not find correlations with Tanner stage for WASO, Performance of PSG in children should ideally consider the
child‘s habitual bedtime. As Ohayon et al. [8] outlined, the timing
SL, SE (TST/SPT and TST/TIB), N1, R or in the number of stage shifts.
Comparing results from subjects aged 6–18 years with the same of recording influences age-related changes of several sleep param-
subjects according to Tanner staging, the same correlations were eters. With advancing age, there is a typical pattern of sleep struc-
shown (Table 4). ture with a high density of slow wave sleep in the first half of the
night and more light sleep and R sleep thereafter. A too late
beginning or a too short duration of the polysomnography will
4. Discussion show portions of sleep states not representative of the full time
of sleep, making it impossible to evaluate the normal sleep dura-
Until now, limited polysomnographic normative data have been tion, sleep efficiency, sleep latency, number of sleep cycles and
available for children (Table 1) [2,3,6,7,9,12–17]. Also, most studies so on. For example TST in the study of Uliel et al. [7] is very short
include too wide of an age spectrum and the number of subjects in comparison with other studies (Table 1) and our study. This
was usually too small to give precise, significant statements. This influences the portion of N1 that is shorter than in other studies.
study aimed to describe age-related changes in the macrostructure Most previous studies do not even include information about the
of normal sleep during childhood and adolescence regarding AASM beginning or the end of polysomnography. In the given study the
guidelines in performing and scoring polysomnographies. Further- habitual rhythm of sleep in different age groups was considered
more, the effect of gender and stage of maturation in adolescence in performing the polysomnography. School-aged children were
(Tanner stage) on sleep should be shown. The present study for investigated on days without school the next day, so school sched-
the first time shows the development of sleep in the age range ules do not influence the results of the study. The relatively long
from 1 to 18 years in a statistically relevant number of normal TST in our study could explain the relatively high portion of stage
subjects. R comparable with studies of Montgomery-Downs et al. [16],
548 S. Scholle et al. / Sleep Medicine 12 (2011) 542–549

Verhulst et al. [9], and Novelli et al. [2]. These authors show a sim- of stage, the gross body movement is considered less than an arou-
ilarly high proportion of stage R; Novelli et al. [2] also considered sal. Reflecting these points in the current study we score arousals
subjects habitual bedtime. as specific patterns in different sleep stages [23] and ignore the
Sleep structure changes with age. A meta-analysis of quantitative new rule of AASM to change N2–N1 if there is an arousal. The per-
sleep parameters by Ohayon et al. [8] showed an increase of SWS, a centage of N1 and the number of stage shifts should be higher if
decrease of N2 and an increase of R as well as a decrease of RL in the rule is considered, especially if there are a lot of arousals as
children from age 5 to adolescence. SL, SE, and percentage of N1 were shown by Novelli et al. [2] and Miano et al. [3]. But as outlined
not significantly age related from childhood to adolescence. by Novelli et al. [2] in normal children there is a low incidence of
In accordance with these results, in our study we can show a cortical arousals; therefore the different approaches of AASM and
strong age dependency of all quantitative sleep parameters except the presented study give nearly the same results.
N1 and SL (p < 0.05) (Table 3, Figs. 1–3). WASO showed a signifi- Rechtschaffen and Kales [5] introduced the term ‘‘movement
cant decrease across the age groups, as was also shown by time (MT)’’ to account for epochs that are mostly obscured by
Montgomery-Downs et al. [16] for 3- to 7-year-old children. movement artifacts. The AASM scoring rules [1] proposed to score
There is an increase of stage N2 with age at the expense of N3 this epoch as the same stage as the epoch that follows it. But in
(Figs. 1 and 2). This is in concordance with studies of Montgom- childhood scoring of MT gives some additional information: for
ery-Downs et al. [16], Tapia et al. [6] and Jenni et al. [19]. Also example, children with sleep disturbed breathing have restless
McLaughlin, Crabtree and Williams [20] described a decrease in sleep with more gross body movements [24] and, for children with
slow-wave sleep and increase in stage 2 from childhood through attention-deficit/hyperactivity disorder, movement time is also en-
adolescence. hanced [25–27]. There is a direct correlation between such distur-
We can show an age dependent decrease of stage R from age 1 bances of sleep and clinical outcomes. Furthermore the scoring of
to 18 (p < 0.05) (Tables 2 and 3). In contrast, Ohayon et al. [8] MT explains an enhanced heart rate in these epochs. That is why
described a modest increase of R sleep with age. As in our results we scored movement time as admitted by Rechtschaffen and Kales
(Table 4) Tapia et al. [6] could not show age differences of R during [5]. In the present study we can show that in normal children the
adolescence. portion of MT decreases with maturation (p < 0.05) (Tables 2 and 3)
Sleep is a dynamic process and consists of periodic alternation and is unimportant with nearly 1% TST (Table 2). In our opinion, an
of sleep states. Sleep proceeds in cycles of R and N; the order is nor- enhanced MT is an important indication of disturbed sleep. Some-
mally N1 ? N2 ? N3 ? N2 ? R. Independence of age length of N- times there is more than one epoch (2–3 epochs) in succession
R-cycles is changing. For the first time, this study demonstrated with movement artifacts and without awakening. Therefore we
that for the age range 1–18 years, cycle duration is shorter in the also scored the MT index (n/h TST).
youngest children (64.7 ± 7.3 min) and is comparable in adoles- Results of previous studies regarding normal values of sleep
cents (91.4 ± 10.9 min/Tanner 5) to the cycle length of adults. architecture in sleep are not directly comparable with our results.
Accordingly the number of N-R-cycles decreases with age Differences in criteria and methodology for selecting participants,
(p < 0.05) (Tables 2 and 3, Fig. 3). grouping ages, polysomnography technique, or in scoring of sleep
The first sleep cycle in older children (age group 3 and upward) pattern according to the rules of Rechtschaffen and Kales [5] or
is mostly incomplete, which is interpreted as an abortive R-part the AASM rules [1], and in interpretating these rules, limits
[21]. Therefore in this age RL is longer than the mean N-R-cycle comparison, for example, in comparing this investigation with
length shown in this study (Table 2). the Tapia study [6]. Both studies considered AASM rules and
RL values reflect sleep cycle changes during development. investigated the influence of Tanner stages on sleep parameters,
Montgomery-Downs et al. [12] showed an increasing RL in normal but the Tapia study included African American, Caucasian and a
children aged 3–7 years. This is concordant with our results dem- few Asian and Hispanic children; we only studied German chil-
onstrating a significant correlation between age and RL in the dren of Caucasian ethnicity. The cut off of the body mass index
range from 1 to 18 years of age (p < 0.05). Also Mason et al. [17] re- was the 95th percentile by Tapia et al. [6], in our study the
ported that pediatric RL is shortest during infancy and longer in la- 90th percentile. In the Tapia study we did not find any informa-
ter childhood and adolescence, and in children RL is longer than tion on the beginning or ending times of polysomnography and
values typically reported for adults (90 ± 30 min). This is in agree- whether the recordings were made during school days or non-
ment with our results (Table 2). Mason et al. [17] found an inverse school days or whether they were a first-night study or not. So
correlation between age and RL in the age group 10–18 years. They for instance, in the Tapia study SL is shorter, RL is different, SE
discuss that the decrease in RL across Tanner stages reflects age re- (TST/TIB) is comparable, TST-portion of stage N1 is shorter, stage
lated changes that continue through adulthood. In our study we N2 is longer, stage N3 is shorter and stage R is shorter in compar-
also find differences in the RL across the different puberty stages ison to our results. These differences may be more a result of
(p < 0.05) (Table 4). study design differences than conflicting results demonstrating
Rules of sleep stage scoring must consider some special features the necessity to consider the same rules for technical perfor-
in childhood in comparison with adults [11]. Maturation is re- mance of polysomnography and interpretation of polysomno-
flected in the changing organization of parameters commonly used graphic patterns. AASM guidelines are helpful in this way, but
to define the states. This is especially important in scoring N2 char- there are several points that have to be regarded including racial
acterized by sleep spindles and K-complexes [22]. differences and age typical sleep schedule, as well as other factors
AASM-rules [1] proposed to change stage N2–N1 if there is an that may influence sleep.
arousal. The increase of N1 and stage shifts corresponding to the In our opinion a discussion of some aspects of the AASM pedi-
occurrence of arousals should be representative of sleep disruption atric rules is indeed important. First discussion is needed regarding
by arousal [2,3]. Questions arise: Why is there not the same rule for the rule to change N2 to N1 if there is an arousal, second the signif-
N3 and R to change the stage to N1 if there is an arousal? And what icance of movements in relation to sleep disturbances in childhood.
about arousals in N1? Furthermore, the rule is in conflict with the Scoring of movement time as defined by Rechtschaffen and Kales
rule ‘‘major body movements are to be scored as the same stage as [5] as a measure of sleep fragmentation should be included in
the epoch that follows it, if there is no alpha rhythm or stage W be- childhood polysomnography.
fore or after the epoch’’ [1]. A gross body movement can be inter- Third we agree with Novelli et al. [2] that the unification of
preted as an arousal-dependent phenomenon. If there is no change stages 3 and 4 might be criticized because many physiologic and
S. Scholle et al. / Sleep Medicine 12 (2011) 542–549 549

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