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Polysomnographic quantification of bioelectrical maturation in preterm and fullterm newborns at matched conceptional ages
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Electroencephalography and clinical Neurophysiology 102 (1997) 186-191
Polysomnographic quantification of bioelectrical maturation in preterm and fullterm newborns at matched conceptional ages Magda Lahorgue Nunes a'*, Jaderson Costa Da Costa a, Maria Valeriana Leme Moura-Ribeiro b ~Division of Neurology, Sao Lucas Hospital, PUCRS, av. lpiranga 6690, Room 322. 90610-000 Porto Alegre RS, Brazil bUniversity of Campinas, S6o Paulo, Brazil
Received 10 November 1995; revised version received 26 August 1996; accepted for publication: I September 1996
Abstract We analyzed the relationship between normal neonatal EEG features and gestational age and conceptional age, and evaluated the normal aspects of EEG maturation in preterm babies compared to term babies. We report 46 newborns, divided into two groups. Group I consisted of 11 newborns with gestational age between 30 and 32 weeks, followed with weekly polysomnograms until they reach 42 weeks' conceptional age. Group II (control) consisted of 35 newborns with gestational ages of 34 weeks (n = 5), 36 weeks (n = 10), 38 weeks (n = 10) and 40 weeks (n = 10) evaluated with one polysomnogram in their first 24-48 h of life. In each examination one 5 min epoch in REM and NREM sleep was analyzed to quantify the number of delta brushes, the presence of frontal and temporal sharp transients, the presence of delta frontal rhythmic activity, the grade of concordance between EEG patterns and sleep stages, the percent of interhemispheric synchrony and the duration of interburst interval. The age dependent variability of the EEG patterns was evaluated during the subsequent weeks with group comparisons at weeks 34, 36, 38 and 40. Our results show that the number of delta brushes and the duration of the interburst interval decrease as gestational and conceptional age increase. The percent of interhemispheric synchrony increases with gestational and conceptional age. The presence of frontal sharp transients and delta frontal rhythmic activity suggest that the newborn is fullterm. The presence of temporal sharp transients suggest a preterm newborn. The degree of concordance between behavioral sleep patterns and EEG was more helpful in recognizing sleep stages than in estimating gestational or conceptional age. Although the EEG patterns were comparable between the groups at the same age, analyses of the behavioral patterns of concordance in NREM sleep showed that newborns in Group I had a more immature behavior than newborns in Group II. Our results also suggest that extrauterine life of preterm babies does not seem to accelerate EEG maturation but may influence the acquisition of behavioral patterns during NREM sleep. © 1997 Elsevier Science Ireland Ltd. Keywords: Newborn; Preterm; Polysomnography; Neonatal EEG
1. Introduction The mechanisms responsible for intrauterine and extrauterine development of the central nervous system (CNS) are still a point of disagreement. The neonatal EEG is a non-invasive procedure used in the diagnosis of neurological diseases and prediction of outcome (Lombroso and Matsumiya, 1985; Scher and Barmada, 1987; Hahn et al., 1989; Nunes et al., 1992). The maturational changes in EEG patterns during sleep in preterm and fullterm newborns have been described by several authors (DreyfusBrisac et al., 1962; Monod et al., 1960; Samson-Dolfus * Corresponding author. Tel.: +55 51 3394936; fax: +55 51 2287770.
et al., 1984; Parrnelee et al., 1968; Goldie et al., 1971; Lombroso, 1979; Sarnat, 1984; Torres and Anderson, 1985; Nunes, 1994). Although studies have attempted to correlate EEG maturation patterns with gestational age (GA) and conceptional age (CA), the results remain controversial (Nolte and Haas, 1978; Eyre et al., 1988; Borsini et al., 1990; Duffy et al., 1990; Thornberg and Thiringer, 1990; Bell et al., 1991; Ferrari et al., 1992; Goto et al., 1992; Scher and Barmada, 1987; Scher et al., 1992; Biagioni et al., 1994; Nunes et al., 1994). The objectives of our study were to determine the relationship between normal neonatal EEG patterns and GA or CA, to contribute to the process of systematization of neonatal EEG and to evaluate normal aspects of EEG electrical maturation
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birth weight varying from 1180 to 1760 g. Clinical problems detected were jaundice (n = 7), mild respiratory distress syndrome ( n = 3 ) and transient tachypnea (n = 6). Six patients underwent cranial ultrasonography, all with normal results. The others did not present any symptoms of neurological disease. We were able to follow 9 newborns for 3 - 2 0 months; they all had normal neuropsychomotor development. Two newborns were lost to follow-up. Group II consisted of 35 low-risk newborns (25 female and 10 male babies) with GA of 34 weeks (n = 5), 36 weeks ( n = 1 0 ) , 38 weeks ( n = 1 0 ) or 40 weeks (n = 10), with Apgar scores of 8 - 1 0 at the fifth minute. Clinical problems, detected only in the group with GA of 34 weeks, were jaundice (n = 1), jitteriness (n = 1) and moderate respiratory distress (n = 1). In Group I concordance between physiological patterns of REM and NREM sleep varied in REM sleep from 4 to 5 points and in NREM from 1 to 5 points. In Group II in REM and NREM sleep the range was from 3 to 5 points.
Comparing sleep phases we found higher scores in REM sleep. Comparing the two groups, we found similar scores in both groups in REM sleep. In NREM sleep we found higher scores in Group II at 38 and 40 weeks. There was a statistical difference between the two groups at 38 weeks (P = 0.008) and at 40 weeks (P = 0.02) using the MannWhitney test. The following EEG patterns showed differences between Group I and Group II: number of delta brushes, incidence of delta frontal rhythmic activity, temporal and frontal sharp transients, percentage of interhemispheric synchrony and maximum interburst interval (Table 1). The differences were not statistically significant.
3.2. Age-related changes Analyses of the age-related changes of these parameters during the subsequent weeks in Group II showed a negative correlation between number of delta brushes and GA
Table 1 Between-group differences without statistical significance EEG patterns
Group I (weeks)
Number of delta brushes (REM/NREM)
32 (57-16/54-11) 33 (34 -8/38-13) 34 (30-7/47-10) 35 (30-10/39--4) 36 (23-11/37-15) 37 (35-8/43-19) 38 (20--4/22-17) 39 (20-3/36-6) 40 (20-1/23-7) 41 (124)/27-5) 42 (134)/25-8) 32-42 32-42 34-42 32 (51-100%) 33 (62-88%) 34 (50-94%) 35 (65-88%) 36 (60-100%) 37 (70-83%) 38 (88-100%) 39 (90-100%) 40 (73-100%) 41 (100%) 42 (93-100%) 32 (53-12 S) 33 (30-10 S) 34 (24-8 S) 35 (30-11 S) 36 (25-3 S) 37 (26-8 S) 38 (10-5 S) 39 (10-3 S) 40 (8-2 S) 41 (4 S) 42 (5-3 S)
Temporal sharp transients Frontal sharp transients Delta frontal rhythmic activity Percentual of interhemispheric synchrony
Maximum interburst interval
Group II (weeks)
Statistical test
t test 34 (55-14/56-22) 36 (35-7/47-14) 38 (23-1/36-8) 40 (12-0/23-5)
34 36-40 36-38
Mann-Whitney Mann-Whitney Fischer t test
34 (55-82%) 36 (64-100%) 38 (83-100%) 40 (92-100%)
t test 34 (48-8 s) 36 (15-3 s) 38 (10-2 s) 40 (7-3 s)
The analyses of EEG patterns showed differences between the groups but they do not have statistical significance.
M.L. Nunes et al. /Electroencephalography and clinical Neurophysiology 102 (1997) 186-191
and behavioral features during sleep in preterm babies compared to fullterm babies. 2. Methods
2.1. Patient selection We report the data of 46 neurologically normal newborns from the Silo Lucas Hospital-PUCRS School of Medicine. The newborns were divided into two groups. Group I consisted of 11 preterm newborns with GA between 30 and 32 weeks, who were followed up with a weekly polysomnogram, until they reached 42 weeks CA. Group II (control) consisted of 35 newborns with GA of 34 weeks (n = 5), 36 weeks (n = 10), 38 weeks (n = 10) and 40 weeks (n = 10), submitted to one polysomnogram in their first 24-48 h of life. Newborns included in the study met the following criteria: admitted to NICU or Nursery of our hospital; 5 rain Apgar score greater than 7; gestational age calculated by the neonatologist using the Capurro method (Capurro et al., 1978); weight adequate for GA: no evidence of a CNS disorder; prenatal mother care during gestation. Newborns who developed CNS disorders during the study (n = 4) were not included in the final analysis. The research was approved by the Ethical Committee of Silo Lucas Hospital, and the parents gave informed consent.
2.2. Polysomnographic recordings The polysomnograms (PS) were performed on a 16 channel EEG and consisted of 11 channels of EEG, electro-oculogram, submental electromyogram, nasal and abdominal respiratory monitoring and electrocardiogram (Anders et al., 1971 ; Lombroso, 1993). Paper speed was 15 ram/s, and for the EEG we used the time constant of 0.3 s: sensitivity 10 /,V/mm and 70 Hz high linear frequency filter. The electrodes were placed based on the 10-20 system as modified for newborns (Anders et al., 1971; Da Costa, 1991; Lombroso, 1993). The montage Fpl-C3, C3-O1, Fpl-T3, T3-O1, Fp2-C4, C4-O2, Fp2-T4, T4-O2, C3-Cz and Cz-C4 was used for fullterm babies and FplC3, C3-P3, P3-O1, T3-T5, T5-O1, Fp2-C4, C4-P4, P4-O2, T4-T6, T6-O2 for preterm. The state of the newborn and all the movements during the exam were recorded on the exam by the technician. All studies were performed in the morning after the babies were fed, cleaned and dried. The babies were in the supine position and each exam lasted at least 50 min (or until a complete sleep cycle was recorded). The total number of delta brushes, frontal and temporal sharp transients, the presence of delta frontal rhythmic activity, concordance between behavioral sleep patterns and EEG, degree of interhemispheric synchrony and measurement of interburst interval were determined during one 5 rain epoch of REM and of NREM sleep (the most typical epochs in each PS were selected). These events were
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defined as follows: (a) Delta brushes: described by Lombroso (1979) as a spindle of varying frequencies (8-22 Hz) associated with a delta wave, were scored in one channel (C4-O2 or P402) during each exam in REM and NREM sleep. (b) Temporal sharp transients: we verified the presence/absence of isolated sharp waves in the temporal region during one 5 rain epoch of REM and NREM sleep (Hughes et al., 1987: Stockard-Pope et al., 1992). (c) Frontal sharp transients: biphasic negative-positive sharp waves, with maximum amplitude in the prefrontal regions and often followed by a slow wave (Monod et al., 1960; Arfel et al., 1977) were verified during one 5 rain epoch of REM and NREM sleep. (d) Delta frontal rhythmic activity (anterior slow dysrhythmia): bursts of polymorphic or monomorphic delta activity in the frontal areas that may follow frontal sharp transients (Stockard-Pope et al., 1992). (e) Concordance: as defined by Lombroso (1979) is the agreement between behavioral and physiological parameters of REM and NREM sleep. We scored one point for each 5 behavioral parameters (eyes closed, presence or absence of phasic activity, presence or absence of affective components, isolated head or body movements and respiration pattern). A score of 5 points indicated concordance of the behavioral state with the physiological pattern. (f) Interhemispheric synchrony: the degree of synchrony of interhemispheric activity was measured during 5 consecutive minutes of NREM sleep (Lombroso, 1979). The percent of synchronic bursts was calculated. (g) Interburst interval: the maximum interval duration (defined as having no activity greater than 15 /xV in amplitude) between 2 bursts of activity during 5 consecutive minutes of NREM sleep was measured bilateraly. The age-related changes of these parameters were evaluated during the subsequent weeks and the groups were compared at 4 different times (34, 36, 38 and 40 weeks). Parametric and non-parametric statistical tests were used according to the type of variable (qualitative or quantitative). The data were analyzed statistically using Spearmans correlation and linear regression. Delta brushes. interhemispheric synchrony and maximum interburst interval were compared in matched weeks in both groups by the t test. The Mann-Whitney test was used to examine correlation of concordance, frontal and temporal sharp transients in both groups. The Fischer test examined the correlation of delta frontal rhythmic activity in both groups. 3. Results
3.1. Between-group differences Group I (G l)consisted of 7 female and 4 male white babies with Apgar scores of 7 or 8 at the fifth minute and
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Table Spearmans (r-values) correlation coeficient of the patterns analysed REM sleep
Delta brushes Concordance Interhemispheric synchrony Maximum interburst interval R/L
NREM sleep
Group I (n = 11)
Group II (n = 35)
Group I (n = 11)
Group II (n = 35)
--0.64 NT -0.06 NT -
-0.70 P < 0.001" 0.01 P = 0.946
-0.30 NT 0.28 NT 0.60 NT -0.8/-0.8 NT NT
-0.70 P < 0.001" 0.41 P = 0.013" 0.86 P < 0.001" -0.55/-0.62 P = 0.001*/P = 0.001" P = 0.004, *P = 0.008*
-
The analyses of the age-related changes of the parameters studied showed that delta brushes and maximum interburst interval decrease with increasing of GA or CA. Concordance in NREM sleep and degree of interhemispheric synchrony increase with the increase in GA or CA. NT, not tested; R/L, right/ left. *Statistically significant difference (P < 0.05).
or C A (P < 0.001) and maximum interburst interval (P = 0.001). A positive correlation was found between concordance in N R E M sleep and G A or CA (P = 0.013) and also in the degree of interhemispheric synchrony (P < 0.001) (Table 2). The linear regression coefficient to Group II showed a reduction of 4 delta brushes/week, an increase of 5.2% on interhemispheric synchrony/week and reduction of 3 s per week on the maximum interburst interval.
4. Discussion The possibility of a correlation between normal patterns of neonatal EEG and G A or CA has been explored by many authors with different approaches. Standardization of cerebral electrical maturation through EEG/PS can help not only with the evaluation of G A but also with the prediction of outcome. Conflicting results found by earlier authors may be due to the use of different methodologies and also to differences in the criteria used for selecting low-risk preterm newborns. Concordance between behavioral sleep patterns and E E G as described previously by Lombroso was determined by a very subjective evaluation. Our system of quantification of concordance has been shown to be more useful in the recognition of sleep stages (mainly REM sleep) than in the establishment of G A or CA. It has also shown that preterm babies when matched to fullterm babies with same C A have more immature behavioral sleep patterns. Duffy et al. (1990) has previously shown that preterm babies assessed by the Assessment of Preterm Infant's Behavior scale also had more immature behavior than matched controls. This suggests a negative environmental influence on the maturation of behavioral patterns. Our results for the analysis of delta brush activity were similar to the data obtained by Lombroso (1979) for babies examined at 3 2 - 3 6 weeks, and indicated that the number of delta brushes is a good quantitative feature for the deter-
mination of G A or C A because their number correlate to each specific G A or CA. W e found the degree of interhemispheric synchrony was similar to that seen by Lombroso (1979) for almost all ages, and correlated well with either G A or CA. As in the previous study developed by Hahn et al. (1989) and Biagioni et al. (1994) we found a negative correlation between maximum interburst interval and G A / CA. Although delta frontal rhythmic activity was first described by Dreyfus-Brisac (1962) as a feature of preterm newborns (around 36 weeks), we found this feature in preterm babies at less than 36 weeks and also in fulltenn (higher incidence). Our results showed that this activity when present suggests that the newborn is fullterm or near term, and as it can appear sporadically it is not a very good pattern to establish GA/CA. Frontal sharp transients as described by Monod et al. (1960) and later studied by Arfel et al. (1977), Scher et al. (1994b) and Nunes (1994), can appear in preterm babies but definitely had a higher incidence in fullterm babies. In our study, temporal sharp transients, previously studied by Hughes et al. (1987) and lately by Scher (Scher et al., 1992; Scher et al., 1994a; Scher et al., 1994b), were more evident in preterm babies, suggesting a relationship to prematurity. The relationship between EEG maturation, C A and the influence of extrauterine life on the development of the CNS is still a matter of disagreement. We can divide the findings obtained in previous studies into three groups. The first group consists of authors that stated that EEG maturation is a function of time from conception or C A and is independent of extrauterine environmental experiences (Dreyfus-Brisac et al., 1962; Parmelee et al., 1968; Goldie et al., 1971; Borsini et al., 1990; Ferrari et al., 1992). They related the differences found between preterm and term babies in their studies to C A and not to extrauterine experience. The second group consisted of authors that stated that extrauterine life of preterm babies accelerates the development of EEG patterns (Nolte and Haas (1978) and Sarnat (1984) in a review article). They both
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showed precocious changes in the EEG of preterm babies in the post-term period, and stated that electrocerebral maturation may proceed at a slightly faster rate after delivery. The third group consisted of authors that observed differences between preterm babies when matched to fullterm at the same CA. Duffy et al. (1990) studied the effects of GA at birth on behavioral (Assessment of Preterm Infant's Behavior) and electrophysiological measures (brain electrical activity mapping) in healthy newborns. Their results showed that fullterm babies had significantly better behavioral function than preterms and also that EEG spectral and photic evoked responses were of significantly lower amplitude in the preterm group. Scher et al. (1992) studied healthy preterm and fullterm newborns at matched CA. Results showed that when preterm babies reached term, they had more immature sleep architecture and continuity patterns than fullterm babies, suggesting a delay in brain maturation in the preterm group. Scher et al. (1994c) also found a positive correlation between rapid eye movements and body movements in REM sleep and CA. They suggested that changes in phasic and continuity measures with increasing CA reflect maturation of specific neuronal processes of the CNS within a rudimentary sleep cycle of the preterm neonate. Our results suggest that EEG maturation is a function of CA and is not influenced by the external environmental experiences because the EEG patterns analyzed in our study did not show differences between preterm and fullterm babies when matched at the same CA. It is known that the increase in the percentage of NREM sleep is related to CA and is indicative of bioelectrical maturation. When we analyzed the concordance between behavioral and electrical patterns of sleep states we found no differences between Group I and Group II in REM sleep, which is an ontogenetically primitive state. However, when we considered NREM sleep, Group I showed more immature concordance between EEG and behavior than Group II. Preterm dysmaturity may reflect dissociation of sleep behaviors and EEG patterns. This suggests that the extrauterine life of preterm newborns may influence the acquisition of mature patterns of sleep. Considering the behavioral patterns of NREM sleep analyzed in this study we found that preterm babies when matched to fullterm babies at the same CA seem to have more immature behavioral state profiles. Three authors performed similar analyses, Duffy et al. (1990), Borsini et al. (1990) and Nolte and Haas (1978). The first group obtained similar results, the second found no behavioral differences between the groups and the last found no relation between EEG maturation and behavioral state profiles. Our results also suggest that extrauterine life of preterm babies does not seem to accelerate EEG maturation but influences the acquisition of behavioral patterns during NREM sleep.
Acknowledgements We acknowledge gratefully the discussions with Professor S.L. MoshE and the cooperation of the staff of our Neonatal Intensive Care Unit. We also wish to thank Dr. B. Bunch and Dr. A. Palmini for their helpful comments and editorial assistance.
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M.L. Nunes et al. /Electroencephalography and clinical Neurophysiology 102 (1997) 186-191 Lombroso, C.T. and Matsumiya, Y. Stability in waking-sleep in neonates as a predictor of long-term outcome. Pediatrics, 1985, 76: 52-63. Lombroso, C.T. Neonatal electroencephalography. In: E. Niedermayer and F. Lopes da Silva (Eds.). Electroencephalography, 3rd edn., Urban and Schwarzenberg, Baltimore, 1993, pp. 803-875. Monod, N., Dreyfus-Brisac., Ducas, P. and Mayer, M. L'EEG du nouveau-n6 ~i terme. ~tude comparative chez le nouveau-n6 en presentacion c6phalique et en presentacion de si6ge. Rev. Neurol., 1960, 102: 375-379. Nunes, M.L., Faraco, B.M., Nora, D.B., Lopes, D.K., Brunstein, M. and Sperb, J. Neuroradiology or neurophysiology: which method is the better approach to the diagnosis of neurologic diseases in the neonate? Pediatr. Neurol., 1992, 8:385 [abstract]. Nunes, M.L. Avaliaq~o da Evolu~fio da Atividade ElEtrica Cerebral em Rec6m-Nascidos Atrav6s da Polissonografia. Thesis, University of Campinas SP (UNICAMP), 1994. Nunes, M.L., Da Costa, J.C. and Ribeiro, M.V.M. Polysomnographic study of bioelectrical maturation in preterm and term newborns. Pediatr. Neurol., 1994, I 1:129-130 [abstract]. Nolte, R. and Haas, G. A polygraphic study of bioelectrical maturation in preterm infants. Dev. Med. Child Neurol., 1978, 20: 167-182. Parmelee, A.H. Jr., Schulte, F.J., Akiyama, Y., Wenner, W.H., Schultz, M.A. and Stem, E. Maturation of EEG activity during sleep in premature infants. Electroencephalogr. Clin. Neurophysiol., 1968, 24: 319-329. Samson-Dolfus, D., Forthome, J. and Capron, E. EEGs of the human infant during sleep and wakefulness during the first year of life. In: P. Kellaway, and I. Pettersen, I. (Eds). Neurological and Electroencephalographic Con-relative Studies in Infancy. Grunne and Stmtton, New York, 1984, 1-25.
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Samat, H.B. Anatomic and physiologic correlates of neurological development in prematurity. In: H.B. Sarnat (Ed.), Topics in Neonatal Neurology. Grunne and Stratton, New York, 1984, pp. 1-25. Scher, M.S. and Barmada, M.A. Estimation of gestational age by electrographic, clinical and anatomical criteria. Pediatr. Neurol., 1987, 3: 256-262. Scher, M.S., Steppe, D.A., Dahl, R.E., Astana, S. and Guthrie, R.D. Comparison of EEG sleep measures in healthy full-term and preterm infants at matched conceptional ages. Sleep, 1992, 15: 442448. Scher, M.S., Bova, J.M., Dokianakis, S.G. and Steppe, D.A. Positive temporal sharp waves on EEG recordings of healthy neonates: a benign pattern of dysmaturity in pre-term infants at post-conceptional term ages. Electroencephalogr. Clin. Neurophysiol., 1994a, 90: 173178. Scher, M.S., Bova, J.M., Dokianakis, S.G. and Steppe, D.A. Physiological significance of sharp wave transients on EEG recordings of healthy pre-term and full-term neonates. Electroencephalogr. Clin. Neurophysiol., 1994b, 90: 179-185. Scher, M.S. Steppe, D.A. Dokianakis, S.G. and Guthrie, R.D. Maturation of phasic and continuity measures during sleep in preterm neonates. Pediatr. Res., 1994, 36: 732-737. Stockard-Pope, J.E., Werner, S.S. and Bickford, R.G. Atlas of Neonatal Electroencephalography, 2nd edn. Raven Press, 1992. Thornberg, E. and Thiringer, K. Normal pattern of the cerebral function monitor trace in term and preterm neonates. Acta Paediatr. Scand., 1990, 79: 20-25. Torres, F. and Anderson, C. The normal EEG of the human newborn. J. Clin. Neurophysiol., 1985, 2: 89-103.
Electroencephalography and clinical Neurophysiology 102 (1997) 186-191
Polysomnographic quantification of bioelectrical maturation in preterm and fullterm newborns at matched conceptional ages Magda Lahorgue Nunes a'*, Jaderson Costa Da Costa a, Maria Valeriana Leme Moura-Ribeiro b ~Division of Neurology, Sao Lucas Hospital, PUCRS, av. lpiranga 6690, Room 322. 90610-000 Porto Alegre RS, Brazil bUniversity of Campinas, S6o Paulo, Brazil
Received 10 November 1995; revised version received 26 August 1996; accepted for publication: I September 1996
Abstract We analyzed the relationship between normal neonatal EEG features and gestational age and conceptional age, and evaluated the normal aspects of EEG maturation in preterm babies compared to term babies. We report 46 newborns, divided into two groups. Group I consisted of 11 newborns with gestational age between 30 and 32 weeks, followed with weekly polysomnograms until they reach 42 weeks' conceptional age. Group II (control) consisted of 35 newborns with gestational ages of 34 weeks (n = 5), 36 weeks (n = 10), 38 weeks (n = 10) and 40 weeks (n = 10) evaluated with one polysomnogram in their first 24-48 h of life. In each examination one 5 min epoch in REM and NREM sleep was analyzed to quantify the number of delta brushes, the presence of frontal and temporal sharp transients, the presence of delta frontal rhythmic activity, the grade of concordance between EEG patterns and sleep stages, the percent of interhemispheric synchrony and the duration of interburst interval. The age dependent variability of the EEG patterns was evaluated during the subsequent weeks with group comparisons at weeks 34, 36, 38 and 40. Our results show that the number of delta brushes and the duration of the interburst interval decrease as gestational and conceptional age increase. The percent of interhemispheric synchrony increases with gestational and conceptional age. The presence of frontal sharp transients and delta frontal rhythmic activity suggest that the newborn is fullterm. The presence of temporal sharp transients suggest a preterm newborn. The degree of concordance between behavioral sleep patterns and EEG was more helpful in recognizing sleep stages than in estimating gestational or conceptional age. Although the EEG patterns were comparable between the groups at the same age, analyses of the behavioral patterns of concordance in NREM sleep showed that newborns in Group I had a more immature behavior than newborns in Group II. Our results also suggest that extrauterine life of preterm babies does not seem to accelerate EEG maturation but may influence the acquisition of behavioral patterns during NREM sleep. © 1997 Elsevier Science Ireland Ltd. Keywords: Newborn; Preterm; Polysomnography; Neonatal EEG
1. Introduction The mechanisms responsible for intrauterine and extrauterine development of the central nervous system (CNS) are still a point of disagreement. The neonatal EEG is a non-invasive procedure used in the diagnosis of neurological diseases and prediction of outcome (Lombroso and Matsumiya, 1985; Scher and Barmada, 1987; Hahn et al., 1989; Nunes et al., 1992). The maturational changes in EEG patterns during sleep in preterm and fullterm newborns have been described by several authors (DreyfusBrisac et al., 1962; Monod et al., 1960; Samson-Dolfus * Corresponding author. Tel.: +55 51 3394936; fax: +55 51 2287770.
et al., 1984; Parrnelee et al., 1968; Goldie et al., 1971; Lombroso, 1979; Sarnat, 1984; Torres and Anderson, 1985; Nunes, 1994). Although studies have attempted to correlate EEG maturation patterns with gestational age (GA) and conceptional age (CA), the results remain controversial (Nolte and Haas, 1978; Eyre et al., 1988; Borsini et al., 1990; Duffy et al., 1990; Thornberg and Thiringer, 1990; Bell et al., 1991; Ferrari et al., 1992; Goto et al., 1992; Scher and Barmada, 1987; Scher et al., 1992; Biagioni et al., 1994; Nunes et al., 1994). The objectives of our study were to determine the relationship between normal neonatal EEG patterns and GA or CA, to contribute to the process of systematization of neonatal EEG and to evaluate normal aspects of EEG electrical maturation
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birth weight varying from 1180 to 1760 g. Clinical problems detected were jaundice (n = 7), mild respiratory distress syndrome ( n = 3 ) and transient tachypnea (n = 6). Six patients underwent cranial ultrasonography, all with normal results. The others did not present any symptoms of neurological disease. We were able to follow 9 newborns for 3 - 2 0 months; they all had normal neuropsychomotor development. Two newborns were lost to follow-up. Group II consisted of 35 low-risk newborns (25 female and 10 male babies) with GA of 34 weeks (n = 5), 36 weeks ( n = 1 0 ) , 38 weeks ( n = 1 0 ) or 40 weeks (n = 10), with Apgar scores of 8 - 1 0 at the fifth minute. Clinical problems, detected only in the group with GA of 34 weeks, were jaundice (n = 1), jitteriness (n = 1) and moderate respiratory distress (n = 1). In Group I concordance between physiological patterns of REM and NREM sleep varied in REM sleep from 4 to 5 points and in NREM from 1 to 5 points. In Group II in REM and NREM sleep the range was from 3 to 5 points.
Comparing sleep phases we found higher scores in REM sleep. Comparing the two groups, we found similar scores in both groups in REM sleep. In NREM sleep we found higher scores in Group II at 38 and 40 weeks. There was a statistical difference between the two groups at 38 weeks (P = 0.008) and at 40 weeks (P = 0.02) using the MannWhitney test. The following EEG patterns showed differences between Group I and Group II: number of delta brushes, incidence of delta frontal rhythmic activity, temporal and frontal sharp transients, percentage of interhemispheric synchrony and maximum interburst interval (Table 1). The differences were not statistically significant.
3.2. Age-related changes Analyses of the age-related changes of these parameters during the subsequent weeks in Group II showed a negative correlation between number of delta brushes and GA
Table 1 Between-group differences without statistical significance EEG patterns
Group I (weeks)
Number of delta brushes (REM/NREM)
32 (57-16/54-11) 33 (34 -8/38-13) 34 (30-7/47-10) 35 (30-10/39--4) 36 (23-11/37-15) 37 (35-8/43-19) 38 (20--4/22-17) 39 (20-3/36-6) 40 (20-1/23-7) 41 (124)/27-5) 42 (134)/25-8) 32-42 32-42 34-42 32 (51-100%) 33 (62-88%) 34 (50-94%) 35 (65-88%) 36 (60-100%) 37 (70-83%) 38 (88-100%) 39 (90-100%) 40 (73-100%) 41 (100%) 42 (93-100%) 32 (53-12 S) 33 (30-10 S) 34 (24-8 S) 35 (30-11 S) 36 (25-3 S) 37 (26-8 S) 38 (10-5 S) 39 (10-3 S) 40 (8-2 S) 41 (4 S) 42 (5-3 S)
Temporal sharp transients Frontal sharp transients Delta frontal rhythmic activity Percentual of interhemispheric synchrony
Maximum interburst interval
Group II (weeks)
Statistical test
t test 34 (55-14/56-22) 36 (35-7/47-14) 38 (23-1/36-8) 40 (12-0/23-5)
34 36-40 36-38
Mann-Whitney Mann-Whitney Fischer t test
34 (55-82%) 36 (64-100%) 38 (83-100%) 40 (92-100%)
t test 34 (48-8 s) 36 (15-3 s) 38 (10-2 s) 40 (7-3 s)
The analyses of EEG patterns showed differences between the groups but they do not have statistical significance.
M.L. Nunes et al. /Electroencephalography and clinical Neurophysiology 102 (1997) 186-191
and behavioral features during sleep in preterm babies compared to fullterm babies. 2. Methods
2.1. Patient selection We report the data of 46 neurologically normal newborns from the Silo Lucas Hospital-PUCRS School of Medicine. The newborns were divided into two groups. Group I consisted of 11 preterm newborns with GA between 30 and 32 weeks, who were followed up with a weekly polysomnogram, until they reached 42 weeks CA. Group II (control) consisted of 35 newborns with GA of 34 weeks (n = 5), 36 weeks (n = 10), 38 weeks (n = 10) and 40 weeks (n = 10), submitted to one polysomnogram in their first 24-48 h of life. Newborns included in the study met the following criteria: admitted to NICU or Nursery of our hospital; 5 rain Apgar score greater than 7; gestational age calculated by the neonatologist using the Capurro method (Capurro et al., 1978); weight adequate for GA: no evidence of a CNS disorder; prenatal mother care during gestation. Newborns who developed CNS disorders during the study (n = 4) were not included in the final analysis. The research was approved by the Ethical Committee of Silo Lucas Hospital, and the parents gave informed consent.
2.2. Polysomnographic recordings The polysomnograms (PS) were performed on a 16 channel EEG and consisted of 11 channels of EEG, electro-oculogram, submental electromyogram, nasal and abdominal respiratory monitoring and electrocardiogram (Anders et al., 1971 ; Lombroso, 1993). Paper speed was 15 ram/s, and for the EEG we used the time constant of 0.3 s: sensitivity 10 /,V/mm and 70 Hz high linear frequency filter. The electrodes were placed based on the 10-20 system as modified for newborns (Anders et al., 1971; Da Costa, 1991; Lombroso, 1993). The montage Fpl-C3, C3-O1, Fpl-T3, T3-O1, Fp2-C4, C4-O2, Fp2-T4, T4-O2, C3-Cz and Cz-C4 was used for fullterm babies and FplC3, C3-P3, P3-O1, T3-T5, T5-O1, Fp2-C4, C4-P4, P4-O2, T4-T6, T6-O2 for preterm. The state of the newborn and all the movements during the exam were recorded on the exam by the technician. All studies were performed in the morning after the babies were fed, cleaned and dried. The babies were in the supine position and each exam lasted at least 50 min (or until a complete sleep cycle was recorded). The total number of delta brushes, frontal and temporal sharp transients, the presence of delta frontal rhythmic activity, concordance between behavioral sleep patterns and EEG, degree of interhemispheric synchrony and measurement of interburst interval were determined during one 5 rain epoch of REM and of NREM sleep (the most typical epochs in each PS were selected). These events were
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defined as follows: (a) Delta brushes: described by Lombroso (1979) as a spindle of varying frequencies (8-22 Hz) associated with a delta wave, were scored in one channel (C4-O2 or P402) during each exam in REM and NREM sleep. (b) Temporal sharp transients: we verified the presence/absence of isolated sharp waves in the temporal region during one 5 rain epoch of REM and NREM sleep (Hughes et al., 1987: Stockard-Pope et al., 1992). (c) Frontal sharp transients: biphasic negative-positive sharp waves, with maximum amplitude in the prefrontal regions and often followed by a slow wave (Monod et al., 1960; Arfel et al., 1977) were verified during one 5 rain epoch of REM and NREM sleep. (d) Delta frontal rhythmic activity (anterior slow dysrhythmia): bursts of polymorphic or monomorphic delta activity in the frontal areas that may follow frontal sharp transients (Stockard-Pope et al., 1992). (e) Concordance: as defined by Lombroso (1979) is the agreement between behavioral and physiological parameters of REM and NREM sleep. We scored one point for each 5 behavioral parameters (eyes closed, presence or absence of phasic activity, presence or absence of affective components, isolated head or body movements and respiration pattern). A score of 5 points indicated concordance of the behavioral state with the physiological pattern. (f) Interhemispheric synchrony: the degree of synchrony of interhemispheric activity was measured during 5 consecutive minutes of NREM sleep (Lombroso, 1979). The percent of synchronic bursts was calculated. (g) Interburst interval: the maximum interval duration (defined as having no activity greater than 15 /xV in amplitude) between 2 bursts of activity during 5 consecutive minutes of NREM sleep was measured bilateraly. The age-related changes of these parameters were evaluated during the subsequent weeks and the groups were compared at 4 different times (34, 36, 38 and 40 weeks). Parametric and non-parametric statistical tests were used according to the type of variable (qualitative or quantitative). The data were analyzed statistically using Spearmans correlation and linear regression. Delta brushes. interhemispheric synchrony and maximum interburst interval were compared in matched weeks in both groups by the t test. The Mann-Whitney test was used to examine correlation of concordance, frontal and temporal sharp transients in both groups. The Fischer test examined the correlation of delta frontal rhythmic activity in both groups. 3. Results
3.1. Between-group differences Group I (G l)consisted of 7 female and 4 male white babies with Apgar scores of 7 or 8 at the fifth minute and
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Table Spearmans (r-values) correlation coeficient of the patterns analysed REM sleep
Delta brushes Concordance Interhemispheric synchrony Maximum interburst interval R/L
NREM sleep
Group I (n = 11)
Group II (n = 35)
Group I (n = 11)
Group II (n = 35)
--0.64 NT -0.06 NT -
-0.70 P < 0.001" 0.01 P = 0.946
-0.30 NT 0.28 NT 0.60 NT -0.8/-0.8 NT NT
-0.70 P < 0.001" 0.41 P = 0.013" 0.86 P < 0.001" -0.55/-0.62 P = 0.001*/P = 0.001" P = 0.004, *P = 0.008*
-
The analyses of the age-related changes of the parameters studied showed that delta brushes and maximum interburst interval decrease with increasing of GA or CA. Concordance in NREM sleep and degree of interhemispheric synchrony increase with the increase in GA or CA. NT, not tested; R/L, right/ left. *Statistically significant difference (P < 0.05).
or C A (P < 0.001) and maximum interburst interval (P = 0.001). A positive correlation was found between concordance in N R E M sleep and G A or CA (P = 0.013) and also in the degree of interhemispheric synchrony (P < 0.001) (Table 2). The linear regression coefficient to Group II showed a reduction of 4 delta brushes/week, an increase of 5.2% on interhemispheric synchrony/week and reduction of 3 s per week on the maximum interburst interval.
4. Discussion The possibility of a correlation between normal patterns of neonatal EEG and G A or CA has been explored by many authors with different approaches. Standardization of cerebral electrical maturation through EEG/PS can help not only with the evaluation of G A but also with the prediction of outcome. Conflicting results found by earlier authors may be due to the use of different methodologies and also to differences in the criteria used for selecting low-risk preterm newborns. Concordance between behavioral sleep patterns and E E G as described previously by Lombroso was determined by a very subjective evaluation. Our system of quantification of concordance has been shown to be more useful in the recognition of sleep stages (mainly REM sleep) than in the establishment of G A or CA. It has also shown that preterm babies when matched to fullterm babies with same C A have more immature behavioral sleep patterns. Duffy et al. (1990) has previously shown that preterm babies assessed by the Assessment of Preterm Infant's Behavior scale also had more immature behavior than matched controls. This suggests a negative environmental influence on the maturation of behavioral patterns. Our results for the analysis of delta brush activity were similar to the data obtained by Lombroso (1979) for babies examined at 3 2 - 3 6 weeks, and indicated that the number of delta brushes is a good quantitative feature for the deter-
mination of G A or C A because their number correlate to each specific G A or CA. W e found the degree of interhemispheric synchrony was similar to that seen by Lombroso (1979) for almost all ages, and correlated well with either G A or CA. As in the previous study developed by Hahn et al. (1989) and Biagioni et al. (1994) we found a negative correlation between maximum interburst interval and G A / CA. Although delta frontal rhythmic activity was first described by Dreyfus-Brisac (1962) as a feature of preterm newborns (around 36 weeks), we found this feature in preterm babies at less than 36 weeks and also in fulltenn (higher incidence). Our results showed that this activity when present suggests that the newborn is fullterm or near term, and as it can appear sporadically it is not a very good pattern to establish GA/CA. Frontal sharp transients as described by Monod et al. (1960) and later studied by Arfel et al. (1977), Scher et al. (1994b) and Nunes (1994), can appear in preterm babies but definitely had a higher incidence in fullterm babies. In our study, temporal sharp transients, previously studied by Hughes et al. (1987) and lately by Scher (Scher et al., 1992; Scher et al., 1994a; Scher et al., 1994b), were more evident in preterm babies, suggesting a relationship to prematurity. The relationship between EEG maturation, C A and the influence of extrauterine life on the development of the CNS is still a matter of disagreement. We can divide the findings obtained in previous studies into three groups. The first group consists of authors that stated that EEG maturation is a function of time from conception or C A and is independent of extrauterine environmental experiences (Dreyfus-Brisac et al., 1962; Parmelee et al., 1968; Goldie et al., 1971; Borsini et al., 1990; Ferrari et al., 1992). They related the differences found between preterm and term babies in their studies to C A and not to extrauterine experience. The second group consisted of authors that stated that extrauterine life of preterm babies accelerates the development of EEG patterns (Nolte and Haas (1978) and Sarnat (1984) in a review article). They both
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showed precocious changes in the EEG of preterm babies in the post-term period, and stated that electrocerebral maturation may proceed at a slightly faster rate after delivery. The third group consisted of authors that observed differences between preterm babies when matched to fullterm at the same CA. Duffy et al. (1990) studied the effects of GA at birth on behavioral (Assessment of Preterm Infant's Behavior) and electrophysiological measures (brain electrical activity mapping) in healthy newborns. Their results showed that fullterm babies had significantly better behavioral function than preterms and also that EEG spectral and photic evoked responses were of significantly lower amplitude in the preterm group. Scher et al. (1992) studied healthy preterm and fullterm newborns at matched CA. Results showed that when preterm babies reached term, they had more immature sleep architecture and continuity patterns than fullterm babies, suggesting a delay in brain maturation in the preterm group. Scher et al. (1994c) also found a positive correlation between rapid eye movements and body movements in REM sleep and CA. They suggested that changes in phasic and continuity measures with increasing CA reflect maturation of specific neuronal processes of the CNS within a rudimentary sleep cycle of the preterm neonate. Our results suggest that EEG maturation is a function of CA and is not influenced by the external environmental experiences because the EEG patterns analyzed in our study did not show differences between preterm and fullterm babies when matched at the same CA. It is known that the increase in the percentage of NREM sleep is related to CA and is indicative of bioelectrical maturation. When we analyzed the concordance between behavioral and electrical patterns of sleep states we found no differences between Group I and Group II in REM sleep, which is an ontogenetically primitive state. However, when we considered NREM sleep, Group I showed more immature concordance between EEG and behavior than Group II. Preterm dysmaturity may reflect dissociation of sleep behaviors and EEG patterns. This suggests that the extrauterine life of preterm newborns may influence the acquisition of mature patterns of sleep. Considering the behavioral patterns of NREM sleep analyzed in this study we found that preterm babies when matched to fullterm babies at the same CA seem to have more immature behavioral state profiles. Three authors performed similar analyses, Duffy et al. (1990), Borsini et al. (1990) and Nolte and Haas (1978). The first group obtained similar results, the second found no behavioral differences between the groups and the last found no relation between EEG maturation and behavioral state profiles. Our results also suggest that extrauterine life of preterm babies does not seem to accelerate EEG maturation but influences the acquisition of behavioral patterns during NREM sleep.
Acknowledgements We acknowledge gratefully the discussions with Professor S.L. MoshE and the cooperation of the staff of our Neonatal Intensive Care Unit. We also wish to thank Dr. B. Bunch and Dr. A. Palmini for their helpful comments and editorial assistance.
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