Early Human Development, 19 (1989) 183-190 Elsevier Scientific Publishers Ireland Ltd.

183

EHD 00964

Behavioral state distribution throughout 24-h video recordings in preterm infants at term with

good prognosis

Kenji Yokochi”, Yoshio Shiroiwa b, Kazuhisa Inukai’, Hideyuki Kite’ and Jiro OgawaC

‘Department of Pediatrics, Seirei-Mikatabara Hospital, 3453 Mikatabara, Hamamatsu, Shizuoka 433, bLaboratory of Child Psychology, Kinjo Gakuin University, 2282-2 Ohmori, Nagoya, Aichi 463 and PDepartment of Pediatrics, Seirei-Hamamatsu Hospital, 2-12-12 Sumiyoshi, Hamamatsu, Shizuoka 430.

Japan

Accepted for publication 10 November 1988

Summary

Behavioral state distribution in 19 preterm infants at term with good developmen- tal prognosis was studied by 24-h video recordings. The preterm infants of shor- test gestation had longer time awake and this was concentrated in the daytime. On classifying behavioral states by Prechtl’s criteria, the preterm infants had a smaller amount of state 1 than healthy term infants; but a similar amount of state 5 in awake time. Preterm infants were thought to have accelerated development in terms of diurnal sleep-awake rhythm, and decelerated development in terms of the content of sleep manifested by the amount of state 1.

preterm infants; behavioral state; sleep-awake rhythm.

Introduction

With recent advances in fetal and neonatal medicine, there is increasing interest in the neurobehavioral development of preterm infants. In general, neurological devel- opment in preterm infants has been considered to be parallel to postconceptional ages. This has been reported in sleep state [1,2], respiratory pattern [3], electroence-

Correspondence to: Kenji Yokochi.

0378-3782/89/$03.50 0 1989 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland

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phalogram [4], and other neurophysiological studies [5]. But some studies showed small difference in muscle tone [6--81 and some aspects of neurobehavior [6,7,9,10]. Postnatal development of behavioral states in preterm infants has also been reported to depend on postconceptional ages [ 1,2], or to be modified by postnatal ages when postconceptional ages are the same [l l-151. In the latter, preterm infants at term have been shown to have more quiet sleep [ 11,131, to have poorly organized or stabi- lized sleep [12,14], or to have more time awake [15] than term infants. These data have been obtained from the study during a limited time in a day. Development of circadian rhythm in preterm infants has not been fully clarified, except that a pre- vious study shows later acquisition in preterm than term infants [16]. The present study was undertaken to elucidate both development of circadian rhythm and of diurnal behavioral state distribution at term in preterm infants with good prognosis by 24-h video recordings.

Subjects and Methods

Nineteen preterm infants (6 males, 13 females) were studied. Clinical characteristics of the subjects are shown in Table I. They were followed-up beyond their third birthday and they had neither neurological nor developmental problems. Their intelligence quotients were all above 80 by Tanaka-Binet test. The infants were examined at the postconceptional age of 38-42 weeks, and their postnatal ages ranged from 3 to 13 weeks.

As controls, ten healthy term infants (5 males, 5 females) with uneventful preg- nancy and delivery were examined. Their gestational age was from 38 to 41 weeks, and their birth weight from 2670 to 3465 g. They were examined at the postnatal age of from 3 to 4 days.

All the preterm infants were admitted to the Neonatal Intensive Care Unit, Seirei- Hamamatsu Hospital within an hour of birth. This unit was maintained at approxi- mately 26OC and 50 f 5% relative humidity. The intensity of illumination ranged from 400 to 550 lx throughout the day. At the time of the examination no infants had received medical treatment other than routine nursing care mentioned below within 2 weeks of the examination. The heart and respiratory rates and body temper- ature were recorded every 3 h as were nappy changes and feeding. Fourteen of the infants were nursed in cots for more than a week before the examination. They were dressed and bedclothes were limited to the trunk so that limb movements could be observed. Five infants were nursed naked (except for nappies) in the incubator (Air Shields Isolette C-86) in which the temperature was 32OC, and humidity was 60%. The infants in cots were given 35-55 ml milk from bottles, and those in incubators 35-50 ml from nasogastric tubes. Ten healthy term infants also received routine nursery care in cots, where the room temperature, humidity and illumination were almost the same as those found in the Neonatal Intensive Care Unit. The infants were breast-fed every 3 h under the video camera.

The subjects were observed individually by a continuous video recording system throughout 24 h. This consisted of two video recorders (Victor HR-SlO) which were wired into the circuit so as to work alternately every 6 h. Whole body movements of the infants were recorded from upper camera (Hitachi VK-C750). Simultaneously,

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TABLE I

Clinical characteristics of preterm and term infants.

I. Pretem infants

Gestational age at birth (weeks) No. Birth weight (g) No.

-28 2 -999 2 29-32 9 1000-1499 6 33- 8 1500-1999 10

2000- 1 Range 27-36 Range 930-2050

Neonatal complications Respiratory problems

Respiratory distress syndrome and apnea of prematurity Persistent fetal circulation Wet lung and apnea of prematurity

Hyperbilirubinemia treated by phototherapy Bacterial infection

Postconceptional age at examination (weeks)

No. Postnatal age at examination (weeks)

No.

38 4 3-4 4 39 4 5-8 6 40 6 9-12 7 41 3 13-14 2 42 2

II. Term infants: Birth weight 2670-3465 g; postnatal age at examination 3-4 days

Gestational age at birth (weeks) No.

38 3 39 3 40 3 41 1

heart and respiratory rates were registered on a neonatal monitor (Model HRI 4-25 and Model RI 71-25, Air Shields Inc.), and the date and time of the observation (within l/l00 s) were recorded on the videotape. A microphone was placed inside the incubator to record the vocalization of the subjects.

The present study had the ethical approval of the hospital and only infants whose parents had given informed consent were chosen as subjects.

The recorded video tapes were played back (National NV-D2000) at a speed nine times faster than normal. Behavioral state was determined on each infant through- out 24 h according to the criteria by Prechtl [17], with some modification. Our clas- sified states were as follows. State 1, eyes closed, regular respiration, no movements; state 2, eyes closed, irregular respiration, no gross movements; state 3 + 4, eyes open, no crying; state 5, eyes open or closed, crying. The state was classified every minute, and the state transition was defined when a new state lasted longer than 3

186

24 I 1 1 1

12 u All 1 ’ ’ ’ I ’ ’ I ’ ’ ’ 1 J

3;4 1 1 I I I 1

n u & ’ I 11 I I I I , I I I

1 2 3 4 5 G 7 8 9 10 11 IL

Fig. 1. An example of diurnal behavioral states distribution. Male preterm infant (case no. 1 in Fig. 2) is illustrated at the postnatal age of 13 weeks. His gestational age was 27 weeks, and birth weight lo90 g. V, milk feeding.

min. States 1 and 2 were regarded as sleep, and states 3 + 4 and 5 as awake. For these criteria, the bottle or breast feeding periods were included in state 3 + 4. The state determinations were made independently by two observers (K.Y. and Y .S.) and there was a 92% rate of agreement.

Results

An example of diurnal state distribution is shown in Fig. 1. Diurnal sleep-awake rhythm for the preterm infants at term and for the healthy term infants are shown in Figs. 2 and 3, respectively. The term infants had cyclic sleep lasting l-2 h, equally distributed in a day. In contrast, the preterm infants at term (cases 1,2, 3, 5,7 and 9 in Fig. 2) had longer periods awake during the daytime, with an inverse correlation to their gestational age, as their postnatal ages were the longer.

In Table II, the state distribution of the preterm infants at term in a day is com- pared with that of the healthy term infants. Total sleep time in a day was not signifi- cantly different in each group. But the preterm infants whose postnatal ages were

0 6 12 18 24 I 4 ” ,I II I 8, I j I , ” ( I I, 1 (13) . *- B--F__ _ 2 (13) - - . ___ - _-_- ____.. ___. . . 3 (11) --* - - --__- _-_- 4(11)_ -_- - -. - - _ _- 5 (11) - -- -.--. -- _. -. 6 (jj) __-_--- __. - __ _ --._-

11) - _. - - - _ - -- - __- -..--

1(-J) m-m-.. --. _- -- - -- --.. _-

9) . ..- -. - _ _ __ -_._.___-_- _-.-. _--

8) - _ _- _ -- - __ -. .

_-.--_ ;; .

- -- _ __ .: . _

_- _- __.I__. ..__ -

6)-_ _. ._ -__- -- __.- - -_.__-

2; 1 _-_ ‘-1, . _ -_ _- .-.--_ . . . . - - . . .

__. -__ ._ _-

q) _ . . _ _ _ - _. . . . _

3”; .- .- - -.-. _. - _ - .

3) . - _:-.:. _: _.- _I, _ - _-_I_ .:_ _I-._ ( ): POSTNATAL WEEKS

-AWAKE

Fig. 2. Sleep-awake rhythm of preterm infants at term.

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0 6 12 IS 24 /III/ /I/I I,,,,,, ,I/,,

1 - - -_ - - _ . 2 .-- __- _ - __I r _ 3 -_ -- - __ ._ _... - u

_I -__I--: --- - - - -.-

5 _- 6 - . __I. _--‘--._._ _

7 -.-.-. - - - --_ __ -_ _-._. 8 I ---- _ _ __-

9 -- - _ _ _ .-__-_ - __

10 ----- - _. . __ - - _ _- -

- AWAKE

Fig. 3. Sleep-awake rhythm of healthy term infants.

1, , , , , , , , ,

TERM 5 10 POSTNATAL WEEKS

Fig. 4. Total sleep time of preterm infants at term. The preterm infants whose postnatal ages are the longer have the smaller amount of total sleep time (a correlation coefficient r = - 0.72, F test, P < 0.01). t, mean value + standard deviation in the term infants.

the longer, had the smaller amount of total sleep time (a correlation coefficient r = - 0.72, F test, P < 0.01, Fig. 4). Duration of state 1 was significantly shorter in the

preterm infants than in the term ones (F test, P < 0.01, Table II). Duration of state 1 in the preterm infants was not related to their postnatal ages (Fig. 5). Some preterm infants with good prognosis had a remarkably small amount of state 1. Eight infants had state 1 for less than 5% of a day, or than 10% of total sleep time. Total awake time and duration of state 5 in the preterm infants at term were not significantly dif- ferent from those in the healthy term infants (Table II). But, the preterm infants with the shorter gestational ages had the longer total awake time, as shown in Fig. 4. They had longer duration of state 5 in a day, but not in total awake time (Fig. 6).

Discussion

Postnatal development of circadian rhythm in our preterm infants with good developmental prognosis shows some different characteristics from that found in healthy term infants. Sleep/waking pattern, seemingly organized by a 4-h prandial

TABLE II

State distribution of preterm infants at term and healthy term infants (percent of each state in a day, mean value f standard deviation).

State Preterm infants at term (%) Healthy term infants (%)

5

3+4

2

1

12.7 + 7.6 7.9 + 3.3 40.2 f 12.8 32.5 & 5.8

27.5 + 10.5 (awake) 24.6 •t- 6.3 (awake)

53.0 f 11.1 51.9 f 6.8 60.3 + 14.2 67.5 _, 5.8

6.7 + 3.9 (sleep) 15.6 f 4.2 (sleep) I *

*P< 0.01, Rest.

t . .

. . . ; ?? ? ? ? ?

? ?

0

I ,I I,,,,,,,,

.

. . . .

.

TERM 5 10 POSTNATAL WEEKS

Fig. 5. State 1 of preterm infants at term. t, mean value + standard deviation in the term infants.

Fig. 6. State 5 of preterm infants at term. j’, mean value + standard deviation in the term infants.

cycle, has been reported to change into a diurnal pattern between 1 and 3 months of age in term infants [ 18,191. Our preterm infants spent much of their early extrauter- ine life in an artificial situation, where it is bright all day long. Nevertheless, preterm infants are known to acquire prolonged awakening during the daytime at earlier postconceptional ages than term infants by our study. This occurred between 2 and 3 months of postnatal age in preterm infants, likewise in term infants. Consequently, the development of diurnal sleep-awake rhythm in preterm infants is thought not to depend on postconceptional ages but on postnatal ages.

As to content of sleep, our preterm infants at term have a smaller amount of state 1 that may be equivalent to quiet sleep than term infants. They are thought to lag in the development of quiet sleep with advance in postconceptional ages [ 1,2]. Preterm infants at term have been reported to have an amount of quiet sleep close to [1,2], or more than that of term infants [11,13]; this differs from our results. This discrep- ancy possibly resulted from the difference of the criteria used in determining states or from the difference of the subjects. Firstly, the states being judged as quiet or indeterminate sleep by other criteria may classify into state 2 by Prechtl’s criteria, laying stress on regularity of respiration [17]. But, this discrepancy cannot be explained by the difference of the criteria, because the state distribution in the term infants determined by the same criteria is similar to that of previous reports [1,2, 1 l-151. Sleep state organization in preterm infants cannot be investigated by our methods. Secondly, the subjects in our study may have different behavioral state development from the premature infants previously reported, because of the differ- ence in their neonatal complications or environments. Some of our subjects may have had more serious neonatal complications cured by modern intensive care than

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previously reported infants [ 1,2,11,13]. Knowledge about the factors modifying neonatal behavioral development has been limited almost entirely to that of term infants [20-281 and to a small number of infants with developmental abnormali- ties 125-281. Such studies have not been done for preterm infants; further compara- ble study is required to clarify neonatal complications or environmental factors modifying postnatal development of behavioral states.

In conclusion, preterm infants have accelerated neonatal development in terms of diurnal sleep-awake rhythm, and decelerated development in terms of the content of sleep manifested by the amount of state 1.

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