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Behavioral state distribution throughout 24-h video recordings in preterm infants at term with good prognosis
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 developmental prognosis was studied by 24-h video recordings. The preterm infants of shortest 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 development in preterm infants has been considered to be parallel to postconceptional ages. This has been reported in sleep state [1,2], respiratory pattern [3], electroenceCorrespondence to: Kenji Yokochi. 0378-3782/89/$03.50 0 1989 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland
184
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 stabilized 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 previous 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 pregnancy 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, SeireiHamamatsu Hospital within an hour of birth. This unit was maintained at approximately 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 temperature 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,
185 TABLE I Clinical characteristics of preterm and term infants. I. Pretem infants Gestational age at birth (weeks)
No.
Birth weight (g)
No.
-28 29-32 33-
2 9 8
-999 1000-1499 1500-1999 2000Range 930-2050
2 6 10 1
Range 27-36
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 39 40 41 42
4 4 6 3 2
3-4 5-8 9-12 13-14
4 6 7 2
II. Term infants: Birth weight 2670-3465 g; postnatal age at examination 3-4 days Gestational age at birth (weeks)
No.
38 39 40 41
3 3 3 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 throughout 24 h according to the criteria by Prechtl [17], with some modification. Our classified 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
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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 compared with that of the healthy term infants. Total sleep time in a day was not significantly different in each group. But the preterm infants whose postnatal ages were 0
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Fig. 2. Sleep-awake rhythm of preterm infants at term.
187
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Fig. 3. Sleep-awake rhythm of healthy term infants. 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 different 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 (%)
5
12.7 +
27.5 + 10.5
2
53.0 f 11.1
*P<
6.7 +
I
0.01,Rest.
7.9 + 3.3
7.6
3+4
1
Healthy term infants (%)
3.9
40.2 f 12.8 (awake)
24.6 •t- 6.3
32.5 & 5.8 (awake)
51.9 f 6.8 60.3 + 14.2 (sleep)
*
15.6 f 4.2
67.5 _, 5.8 (sleep)
0 . t
. .
.
.
; ? ?
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TERM
5 POSTNATAL
.
. .
10 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 extrauterine 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 discrepancy 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, 1l-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 difference in their neonatal complications or environments. Some of our subjects may have had more serious neonatal complications cured by modern intensive care than
189
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 abnormalities 125-281. Such studies have not been done for preterm infants; further comparable 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. References
8 9
10
11 12 13 14
15 16 17
Parmelee, A.H., Wenner, W.H., Akiyama, Y., Schultz, M. and Stern, E. (1967): Sleep states in premature infants. Dev. Med. Child Neurol., 9,70-77. Stem, E., Parmelee, A.H. and Harris, M.A. (1973): Sleep state periodicity in premature and term infants. Dev. Psychobiol., 6,357-365. Parmlee, A.H., Stern, E. and Harris, M.A. (1972): Maturation of respiration in prematures and young infants. Neuropaediatrics, 3,294-304. Parmelee, A.H. Jr., Schulte, F.J., Akiyama, Y., Wenner, W.H., Schulz, M.A. and Stern, E. (1968): Maturation of EEG activity during sleep in premature infants. Electroencephalogr. Clin. Neurophysiol., 24,319-329. Parmelee, A.H. (1975): Neurophysiological and behavioral organization of premature infants in the first months of life. Biol. Psychiatr., 10,501-511. Howard, J., Parmelee, A.H., Kopp, C.B. and Littman, B. (1976): A neurologic comparison of preterm and full-term infants at term conceptional age. J. Pediatr., 88.995-1002. Palmer, PG., Dubowitz, L.M.S., Verghote, M. and Dubowitz, V. (1982): Neurological and neurobehavioural differences between preterm infants at term and full-term newborn infants. Neuropediatrics, 13, 183-189. Forslund, M. and Bjerre, I. (1983): Neurological assessment of preterm infants at term conceptional age in comparison with normal full-term infants. Early Hum. Dev., 8, 195-208. Kurtzberg, D., Vaughan, H.G. Jr., Daum, C., Grellong, B.A., Albin, S. and Rotkin, L. (1979): Neurobehavioral performance of low-birthweight infants at 40 weeks conceptional age: comparison with normal fullterm infants. Dev. Med. Child Neurol., 21.590-607. Pahrdetto, R., Mansi, G., Rinaldi, P., De Luca, T., Corchia, C., De Curtis, M. and Andolfi, M. (1982): Behaviour of preterm newborns reaching term without any serious disorder. Early Hum. Dev., 6,357-363. Stern, E., Parmelee, A.H., Akiyama, Y., Schulz, M.A. and Wenner, W.H. (1969): Sleep cycle characteristics in infants. Pediatrics, 43,65-70. Dreyfus-Brisac, C. (1970): Ontogenesis of sleep in human prematures after 32 weeks of conceptional age. Dev. Psychobiol., 3,91--121. Booth, C.L., Leonard, H.L. and Thoman, E.B. (1980): Sleep states and behavior patterns in preterm and full term infants. Neuropediatrics, 11,354-364. Watt, J.E. and Strongman, K.T. (1985): The organization and stability of sleep states in fullterm, preterm, and small-for-gestational age infants: a comparative study. Dev. Psychobiol., 18, 151162. Davis, D.H. and Thoman, E.B. (1987): Behavioral states of premature infants: implications for neural and behavioral development. Dev. Psychobiol., 20,25-38. Hellbriigge, T. (1960): The development of circadian rhythms in infants. Cold Spring Harbor Symp. Quant. Bio., 25,311-323. Prechtl, H.F.R. (1974): The behavioral states of the newborn infant (a review). Brain Res., 76, 185 -212.
190 18
Kleitman, N. and Engelmann, T.G. (1953): Sleep characteristics in infants. J. Appl. Physiol., 6,269 -282. 19 Meier-Koll, A., Hall, U., Kott, G. and Meier-Koll, V. (1978): A biological oscillator system and the development of sleep-waking behavior during early infancy. Chronobiologia, 5,425-440. 20 Hashimoto, T., Hiura, K., Endo, S., Fukuda, K., Mori, A., Tayama, M. and Miyao, M. (1983): Postural effects on behavioral states of newborn infants. A sleep polygraphic study. Brain Dev., 5, 286-291. 21 Prechtl, H.F.R., Weinmann, H. and Akiyama, Y. (1969): Organization of physiological parameters in normal and neurologically abnormal infants. Neuropaediatrie, 1, 101-129. 22 Dreyfus-Brisac, C. and Monod, N. (1970): Sleeping behaviour in abnormal newborn infants. Neuropaediatrie, 1, 354-366. 23 Prechtl, H.F.R., Theorell, K. and Blair, A.W. (1973): Behavioral state cycle in abnormal infants. Dev. Med. ChildNeurol., 15,606-615. 24 Theorell, K., Prechtl, H.F.R. and Vos, J.E. (1974): A polygraphic study of normal and abnormal newborninfants. Neuropaediatrie, 5,279-317. 25 Monod, N. and Guidasci, S. (1976): Sleep and brain malformation in the neonatal period. Neuropaediatrie, 7,229-249. 26 Watanabe, K., Miyazaki, S., Hara, K. and Hakamada, S. (1980): Behavioral state cycles, background EEGs and prognosis of newborns with perinatal hypoxia. Electroencephalogr. Clin. Neurophysiol., 49,618-625. 27 Thoman, E.B., Denenberg, V.H., Sieve], J., Zeidner, L.P. and Becker, P. (1981): State organization in neonates: developmental inconsistency indicates risk for developmental dysfunction. Neuropediatrics, 12,45-54. 28 Lombroso, CT. and Matsumiya, Y., (1985): Stability in waking-sleep states in neonates as a predictor of long-term neurologic outcome. Pediatrics, 76,52-63.
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 developmental prognosis was studied by 24-h video recordings. The preterm infants of shortest 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 development in preterm infants has been considered to be parallel to postconceptional ages. This has been reported in sleep state [1,2], respiratory pattern [3], electroenceCorrespondence to: Kenji Yokochi. 0378-3782/89/$03.50 0 1989 Elsevier Scientific Publishers Ireland Ltd. Published and Printed in Ireland
184
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 stabilized 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 previous 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 pregnancy 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, SeireiHamamatsu Hospital within an hour of birth. This unit was maintained at approximately 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 temperature 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,
185 TABLE I Clinical characteristics of preterm and term infants. I. Pretem infants Gestational age at birth (weeks)
No.
Birth weight (g)
No.
-28 29-32 33-
2 9 8
-999 1000-1499 1500-1999 2000Range 930-2050
2 6 10 1
Range 27-36
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 39 40 41 42
4 4 6 3 2
3-4 5-8 9-12 13-14
4 6 7 2
II. Term infants: Birth weight 2670-3465 g; postnatal age at examination 3-4 days Gestational age at birth (weeks)
No.
38 39 40 41
3 3 3 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 throughout 24 h according to the criteria by Prechtl [17], with some modification. Our classified 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 All
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1
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1
&
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1
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3
4
’
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J
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I
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I
I
I
I
,
5
G
7
8
9
n I
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 compared with that of the healthy term infants. Total sleep time in a day was not significantly different in each group. But the preterm infants whose postnatal ages were 0
I
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Fig. 2. Sleep-awake rhythm of preterm infants at term.
187
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,
10 WEEKS
Fig. 3. Sleep-awake rhythm of healthy term infants. 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 different 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 (%)
5
12.7 +
27.5 + 10.5
2
53.0 f 11.1
*P<
6.7 +
I
0.01,Rest.
7.9 + 3.3
7.6
3+4
1
Healthy term infants (%)
3.9
40.2 f 12.8 (awake)
24.6 •t- 6.3
32.5 & 5.8 (awake)
51.9 f 6.8 60.3 + 14.2 (sleep)
*
15.6 f 4.2
67.5 _, 5.8 (sleep)
0 . t
. .
.
.
; ? ?
?? ? ?
? ?
I
,I
. . .
I,,,,,,,,
TERM
5 POSTNATAL
.
. .
10 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 extrauterine 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 discrepancy 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, 1l-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 difference in their neonatal complications or environments. Some of our subjects may have had more serious neonatal complications cured by modern intensive care than
189
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 abnormalities 125-281. Such studies have not been done for preterm infants; further comparable 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. References
8 9
10
11 12 13 14
15 16 17
Parmelee, A.H., Wenner, W.H., Akiyama, Y., Schultz, M. and Stern, E. (1967): Sleep states in premature infants. Dev. Med. Child Neurol., 9,70-77. Stem, E., Parmelee, A.H. and Harris, M.A. (1973): Sleep state periodicity in premature and term infants. Dev. Psychobiol., 6,357-365. Parmlee, A.H., Stern, E. and Harris, M.A. (1972): Maturation of respiration in prematures and young infants. Neuropaediatrics, 3,294-304. Parmelee, A.H. Jr., Schulte, F.J., Akiyama, Y., Wenner, W.H., Schulz, M.A. and Stern, E. (1968): Maturation of EEG activity during sleep in premature infants. Electroencephalogr. Clin. Neurophysiol., 24,319-329. Parmelee, A.H. (1975): Neurophysiological and behavioral organization of premature infants in the first months of life. Biol. Psychiatr., 10,501-511. Howard, J., Parmelee, A.H., Kopp, C.B. and Littman, B. (1976): A neurologic comparison of preterm and full-term infants at term conceptional age. J. Pediatr., 88.995-1002. Palmer, PG., Dubowitz, L.M.S., Verghote, M. and Dubowitz, V. (1982): Neurological and neurobehavioural differences between preterm infants at term and full-term newborn infants. Neuropediatrics, 13, 183-189. Forslund, M. and Bjerre, I. (1983): Neurological assessment of preterm infants at term conceptional age in comparison with normal full-term infants. Early Hum. Dev., 8, 195-208. Kurtzberg, D., Vaughan, H.G. Jr., Daum, C., Grellong, B.A., Albin, S. and Rotkin, L. (1979): Neurobehavioral performance of low-birthweight infants at 40 weeks conceptional age: comparison with normal fullterm infants. Dev. Med. Child Neurol., 21.590-607. Pahrdetto, R., Mansi, G., Rinaldi, P., De Luca, T., Corchia, C., De Curtis, M. and Andolfi, M. (1982): Behaviour of preterm newborns reaching term without any serious disorder. Early Hum. Dev., 6,357-363. Stern, E., Parmelee, A.H., Akiyama, Y., Schulz, M.A. and Wenner, W.H. (1969): Sleep cycle characteristics in infants. Pediatrics, 43,65-70. Dreyfus-Brisac, C. (1970): Ontogenesis of sleep in human prematures after 32 weeks of conceptional age. Dev. Psychobiol., 3,91--121. Booth, C.L., Leonard, H.L. and Thoman, E.B. (1980): Sleep states and behavior patterns in preterm and full term infants. Neuropediatrics, 11,354-364. Watt, J.E. and Strongman, K.T. (1985): The organization and stability of sleep states in fullterm, preterm, and small-for-gestational age infants: a comparative study. Dev. Psychobiol., 18, 151162. Davis, D.H. and Thoman, E.B. (1987): Behavioral states of premature infants: implications for neural and behavioral development. Dev. Psychobiol., 20,25-38. Hellbriigge, T. (1960): The development of circadian rhythms in infants. Cold Spring Harbor Symp. Quant. Bio., 25,311-323. Prechtl, H.F.R. (1974): The behavioral states of the newborn infant (a review). Brain Res., 76, 185 -212.
190 18
Kleitman, N. and Engelmann, T.G. (1953): Sleep characteristics in infants. J. Appl. Physiol., 6,269 -282. 19 Meier-Koll, A., Hall, U., Kott, G. and Meier-Koll, V. (1978): A biological oscillator system and the development of sleep-waking behavior during early infancy. Chronobiologia, 5,425-440. 20 Hashimoto, T., Hiura, K., Endo, S., Fukuda, K., Mori, A., Tayama, M. and Miyao, M. (1983): Postural effects on behavioral states of newborn infants. A sleep polygraphic study. Brain Dev., 5, 286-291. 21 Prechtl, H.F.R., Weinmann, H. and Akiyama, Y. (1969): Organization of physiological parameters in normal and neurologically abnormal infants. Neuropaediatrie, 1, 101-129. 22 Dreyfus-Brisac, C. and Monod, N. (1970): Sleeping behaviour in abnormal newborn infants. Neuropaediatrie, 1, 354-366. 23 Prechtl, H.F.R., Theorell, K. and Blair, A.W. (1973): Behavioral state cycle in abnormal infants. Dev. Med. ChildNeurol., 15,606-615. 24 Theorell, K., Prechtl, H.F.R. and Vos, J.E. (1974): A polygraphic study of normal and abnormal newborninfants. Neuropaediatrie, 5,279-317. 25 Monod, N. and Guidasci, S. (1976): Sleep and brain malformation in the neonatal period. Neuropaediatrie, 7,229-249. 26 Watanabe, K., Miyazaki, S., Hara, K. and Hakamada, S. (1980): Behavioral state cycles, background EEGs and prognosis of newborns with perinatal hypoxia. Electroencephalogr. Clin. Neurophysiol., 49,618-625. 27 Thoman, E.B., Denenberg, V.H., Sieve], J., Zeidner, L.P. and Becker, P. (1981): State organization in neonates: developmental inconsistency indicates risk for developmental dysfunction. Neuropediatrics, 12,45-54. 28 Lombroso, CT. and Matsumiya, Y., (1985): Stability in waking-sleep states in neonates as a predictor of long-term neurologic outcome. Pediatrics, 76,52-63.