Short Communication

Yonago Acta medica 2016;59:89–91

Approximate Entropy of Respiratory Movements in Human Newborns during
Different Sleep States
Hiroo Tamaki,* Mazumi Miura,† Sachiko Nakamoto,* Takuya Horie,* Susumu Kanzaki,† Eiji Shimizu,‡
Takashi Amisaki§ and Naoto Burioka**Department of Pathobiological Science and Technology, School of Health Science, Tottori University Faculty of Medicine, Yonago 6838503, Japan, †Division of Pediatrics and Perinatology, Department of Multidisciplinary Internal Medicine, School of Medicine, Tottori
University Faculty of Medicine, Yonago 683-8503, Japan, ‡Division of Medical Oncology and Molecular Respirology, Department ofMultidisciplinary Internal Medicine, School of Medicine, Tottori University Faculty of Medicine, Yonago 683-8504, Japan and §Department of Biological Regulation, School of Health Science, Tottori University Faculty of Medicine, Yonago 683-8503, JapanABSTRACT
Previous studies have reported that the respiratory cycleof healthy newborns is more irregular during activesleep. This study aimed to apply non-linear analysis toexamine the irregularity of respiratory movement innewborns at different sleep states. The respiratory movement signals from an abdominal band during quiet andactive sleep were analyzed using approximate entropy(ApEn). The breathing interval of active sleep was significantly shorter than that of quiet sleep [1.30 (0.17) s
vs. 1.58 (0.11) s; (P < 0.03)]. The ApEn of respiratory
movements during active sleep were significantly larger
than that during quiet sleep [0.785 (0.135) s vs. 0.678(0.083) s; (P < 0.05)]. We found that the ApEn of respiratory movement in healthy newborns could detect irregularities in respiration during sleep.

SUBJECTS AND METHODS
We investigated eight healthy newborns within sevendays after birth [gestational age 39.6 (standard deviation: 1.7) weeks, range: 37.0–41.9]. EEG signals wererecorded (NicoletOne, IMI, Tokyo, Japan) from scalp
surface electrodes (F3, F4, C3, C4, O1 and O2 by theInternational 10–20 System). We categorized the state ofsleep-wake stage on the EEG records at 30-s intervals
using the criteria defined by the American Associationof Sleep Medicine.7 We measured the respiratory movements of newborns during active and quiet sleep using
an abdominal band (Quantum respiratory effort sensor;
Pro-Tech services, Murrysville, PA). We selected threedifferent 60-s artifact-free epochs of respiratory movements from each quiet or active sleep in newborns. The
protocol was approved by the local ethics committee inTottori University (# 2108). Written informed consent
was obtained from the mother of each newborn.
The signals from respiratory movements were digitized with A/D converter (PowerLab, ADInstruments,Tokyo, Japan) at sampling rate of 10 Hz (0.1 s). The
av- et al.
H. Tamaki
erage approximate entropy (ApEn) of three epochs of respiratory movement from each sleep stage was estimatedfor the eight newborns.
We computed the ApEn of time series from respiratory movement during each sleep stage. In mathematicalterms, ApEn was derived from the previously describedcorrelation integral Cm,i(r).4–6 As described by Pincus,6
the ApEn was computed as

Key words

active sleep; approximate entropy; newborn; quiet sleep; respiration
The respiratory pattern of healthy newborns was reportedly more irregular during active sleep than during quiet
sleep.1 Moreover, sleep apneas in neonates frequently
occur during active sleep.2 The analysis of breathing
patterns in neonatal sleep states have been based on respiratory rates and cycles.3 Recently, a new non-linear
analysis has been used to quantify biological signals,
such as human respiration and electroencephalogram(EEG).4, 5 In this study, we analyzed the respiratory pattern according to sleep states using approximate entropy6 to investigate the respiratory irregularity in healthy
newborns.

ApEn (N, m, r) = Φm(r) – Φm+1(r)Φm (r) = (N-(m-1))-1

N −( m −1)∑ log Cm,i(r)i =1-1ApEn (N, m, r) = (N−(m−1))

Corresponding author: Naoto Burioka, MD, PhD
burioka@med.tottori-u.ac.jp
Received 2015 November 25
Accepted 2015 December 17
Abbreviations: ApEn, approximate entropy; EEG, electroencephalogram; REM, rapid eye movement; SIDS, sudden infant death
syndromeN −( m −1)-1 N − m

i =1

i =1

∑ log Cm,i(r) – (N-m) ∑ log Cm+1,i(r)where m represented the vector length, r represented
the “filter factor”, and N represented the number ofdata points. The value of N for the ApEn computation
894

H. Tamaki et al.

is typically between 75 and 5000.6 ApEn measures thelogarithmic likelihood that close sets of patterns for mobservations remain close in the next incremental comparisons.6 It characterizes how different segments of signals with similar recent histories remain similar in thefuture. As ApEn decreases, the complexity of the signal
decreases and determinism is high.
In this study, the N was 600 (60 s); the set r was at 0.2
times the SD of the original data series; and m = 2 wasused.6 In order to facilitate interpretation of ApEn valuesof EEG signals, the ApEn of a time series of a sine wave
was estimated to be 0.0001 (N = 600), as an example ofa regular (linear) signal. The ApEn of a time series of
uniformly distributed random numbers was estimatedto be 1.538 (N = 600). We used the MatLab software(MathWorks, Natick, MA) to compute for the ApEn values.4, 5

Statistical analyses
The values of ApEn were presented as mean (SD). We
used Wilcoxon matched pairs signed-rank test to compare ApEn values and assess for any difference between
quiet and active sleep stages (Stat Flex; ViewFlex, Tokyo, Japan). Differences were considered to be statistically significant at P < 0.05.
RESULTS
Figure 1 shows an example of respiratory movements in
a newborn at a sampling rate of 10 Hz. In the eight newborns, the breathing interval of active sleep was significantly shorter than that of quiet sleep [1.30 (0.17) s vs. 1.58
(0.11) s; (P < 0.03)]. The ApEn of respiratory movement
was significantly higher during active sleep than during
quiet sleep [0.785 (0.135) vs. 0.678 (0.083); (P < 0.05)](Fig. 2).

A	 mV

0.8

0.78
0.76
0.74
0.72
0.7

B	
0.8

01020304050(s)601020304050(s)
60

mV

0.78
0.76
0.74
0.72
0.7

0Fig. 1. An example of respiratory movements in a newborn.
A: During quiet sleep. B: During active sleep.
Unit of the vertical axis is arbitrary.

90ApEn of respiration in newborns

ApEnin respiratory movement (Fig. 1B), because the respiratory irregularity is one of the features in active sleep ofnewborns. Although the breathing interval analysis uses
only some intervals in a time series, ApEn uses the total
data points. Moreover, entropy measurement can estimate the complex systems, including nonlinear deterministic and stochastic.4–6 In this point, ApEn measurement may be suitable to analyze biological signals. Nonlinear analysis of the ApEn of respiration may be usefulfor detecting the irregularity of respiration during sleep
in newborns, but further study is needed to validate andestimate its clinical usefulness.

P < 0.05

1.1
10.90.80.7The authors declare no conﬂict of interest.

0.60.50.4

REFERENCES

QS

1 Hathorn MK. The rate and depth of breathing in new-born
infants in different sleep states. J Physiol. 1974;243:101-13.
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2 Steinschneider A, Weinstein S. Sleep respiratory instability interm neonates under hyperthermic conditions: age, sex, typeof feeding, and rapid eye movements. Pediatr Res. 1983;17:3541. PMID: 6835713.
3 Finer NN, Abroms IF, Taeusch HW Jr. Ventilation and sleepstates in newborn infants. J Pediatr. 1976;89:100-8. PMID:
180273.
4 Burioka N, Cornélissen G, Halberg F, Kaplan DT, Suyama H,
Sako T, et al. Approximate entropy of human respiratory
movement during eye-closed waking and different sleep
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5 Burioka N, Cornélissen G, Maegaki Y, Halberg F, Kaplan DT,Miyata M, et al. Approximate entropy of the electroencephalogram in healthy awake subjects and absence epilepsy patients. Clin EEG Neurosci. 2005;36:188-93. PMID: 16128154.
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PMID: 11607165.
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ASFig. 2. ApEn of respiratory movements during quiet sleep andactive sleep in eight newborns. The values of ApEn during activesleep (AS) were significantly larger than that during quiet sleep(QS) (P < 0.05). ApEn, approximate entropy; AS, active sleep;
QS, quiet sleep.

DISCUSSION
This is the first study to report that the value of ApEn ofrespiratory movement in active sleep was significantly
larger than that of quiet sleep in healthy newborns,
which suggested that the state of respiration was more
irregular during active sleep than during quiet sleep. In
healthy adults, we have reported that ApEn from respiratory movement during rapid eye movement (REM) sleep
was significantly larger than that during sleep stage IV.4
REM sleep and non-REM sleep are equivalent to active
sleep and quiet sleep, respectively, in newborns.7 Changes in ApEn of respiratory movements during quiet sleep
and active sleep in newborns were similar to the changes
in non-REM sleep and REM sleep in adults.
One of the major problems during sleep in newborns is sudden infant death syndrome (SIDS), which
remains to be the important cause of infant deaths in Japan. It was reported that active sleep occupies more than
50% of the total sleep time in newborns.8 Sleep apneas
in the neonatal period frequently occur during active
sleep,2 and SIDS was found to happen in an abnormal
percentage of obstructive sleep apneas.8 We counted
the breathing interval in spite of the small amplitudes
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