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Amplitude-integrated electroencephalogram 1 h after birth in a preterm infant with cystic periventricular leukomalacia
Brain & Development 35 (2013) 75–78 www.elsevier.com/locate/braindev
Case report
Amplitude-integrated electroencephalogram 1 h after birth in a preterm infant with cystic periventricular leukomalacia Toru Kato a,⇑, Akihisa Okumura b, Fumio Hayakawa a, Takeshi Tsuji a, Seiji Hayashi a, Jun Natsume c b
a Department of Pediatrics, Okazaki City Hospital, Okazaki, Japan Department of Pediatrics and Adolescent Medicine, Juntendo University School of Medicine, Tokyo, Japan c Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya, Japan
Received 16 October 2011; received in revised form 24 November 2011; accepted 28 November 2011
Abstract We report a preterm infant, who showed abnormal amplitude-integrated electroencephalogram (aEEG) findings 1 h after birth and later developed cystic periventricular leukomalacia (PVL). The patient was a girl with a gestational age of 29 weeks. She was delivered by emergency cesarean section because of placental abruption and intrauterine co-twin demise. Artificial ventilation and administration of surfactant were needed to treat respiratory distress syndrome. Her cardiovascular condition was stable with artificial ventilation. Cranial ultrasonography showed extended cystic PVL after 11 days of age. aEEG 1 h after birth showed a consistently inactive pattern that resolved completely 28 h after birth. The neurophysiological findings of this patient suggest that aEEG findings during the very early period after birth provide significant information for predicting PVL. Ó 2011 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved. Keywords: Amplitude-integrated electroencephalogram; Periventricular leukomalacia; Prediction; Preterm infant; White matter injury
1. Introduction Brain injury in preterm infants has recently been understood as an encephalopathy of prematurity, which consists of periventricular leukomalacia (PVL), diffuse white matter injury, and other neuronal/axonal injuries [1]. These injuries cause cerebral palsy and cognitive/ behavioral/attentional deficits. We reported previously that a conventional electroencephalogram (EEG) is a powerful tool to assess brain damage, such as PVL, in preterm infants during the early neonatal period [2,3]. We also reported that earlier depression on a conven⇑ Corresponding author. Address: Department of Pediatrics, Okazaki City Hospital, 3-1 Goshoai, Koryuji-cho, Okazaki, Aichi 444-8553, Japan. Tel.: +81 564 21 8111; fax: +81 564 25 5531. E-mail address: [email protected] (T. Kato).
tional EEG results in a higher sensitivity for predicting PVL or cerebral palsy in preterm infants [3,4]. However, we could not examine conventional EEG within 3 h after birth because it was difficult to record without disturbing the management of cardiovascular and respiratory stabilization. Amplitude-integrated electroencephalogram (aEEG) is a simple and convenient tool for continuous brainfunction monitoring and is widely used in neonatal intensive care units. Although several studies have demonstrated the predictive value of aEEG for intraventricular hemorrhage or PVL within 12–48 h after birth in preterm infants [5–7], the clinical significance of aEEG within 3 h after birth in preterm infants has rarely been reported. We report a preterm infant, who showed abnormal aEEG findings 1 h after birth and later developed cystic PVL.
0387-7604/$ - see front matter Ó 2011 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.braindev.2011.11.010
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T. Kato et al. / Brain & Development 35 (2013) 75–78
2. Case report The patient was an 1108-g girl born at 29 weeks of gestation. She was a monochorionic diamniotic twin. At 18 weeks of gestation, she was a recipient of stage 3 twin–twin transfusion syndrome, according to the criteria defined by Quintero et al. [8], and was treated with fetoscopic laser photocoagulation. After the therapy, the signs of twin–twin transfusion syndrome resolved completely. Because of placental abruption and intrauterine co-twin demise, she was delivered by emergency cesarean section in our hospital and was admitted to the neonatal intensive care unit. Her Apgar scores were 2 and 6 at 1 and 5 min, respectively. Venous blood gas analysis upon admission revealed a pH of 7.41, PCO2 at 32 mm Hg, and a base excess of 3.2 mmol/L. Her blood pressures were 47 and 30 mm Hg of systolic and diastolic, respectively. Ventilation was provided artificially, and surfactant was administered because of respiratory distress syndrome. Her cardiovascular condition was stable with artificial ventilation, and her neurological findings were normal. Clinical seizures were not observed. Cranial ultrasonography was performed daily during the first 2 weeks. Abnormal periventricular echogenicity was observed at 2 days of age, and multiple cysts more than 3 mm in diameter appeared at 11 days of age, extending into bilateral deep white matter (Fig. 1a). No other significant complications were observed during the neonatal period. Brain magnetic resonance imaging (MRI) was performed with a 1.5Tesla imager at term-equivalent age, which showed that bilateral cystic PVL extended into deep white matter (Fig. 1b and c). The patient developed spastic diplegia, and her psychomotor development was delayed moderately at 10 months of age. Parental informed consent was obtained for publication of this case report. The aEEG was recorded from 1 h after birth before administration of surfactant using a NicoletOne Monitor nICU (CareFusion, San Diego, CA, USA). A single channel (C3–C4) aEEG was obtained with surface Ag/ AgCl cup electrodes and displayed at 6 cm/h. The
impedance was <5 kO. The recording duration was 70 min. The aEEG consistently showed an inactive or flat pattern (Fig. 2a) according to the criteria defined by Hellstro¨m-Westas et al. [9]. A follow-up aEEG performed 28 h after birth with a recording duration of 70 min showed a discontinuous pattern (Fig. 2b) according to the same criteria, which is a normal finding in preterm infants. Mild cycling was observed. Electrical seizures were not seen. Sedative or antiepileptic drugs were not used. For the control, we also performed aEEG 1–3 h after birth using the same method in five infants in a consecutive period whose gestational age was between 26 and 32 weeks and who had no abnormalities on serial cranial ultrasonography and/or brain MRI during the neonatal period. In all five infants, the aEEG showed a discontinuous pattern. 3. Discussion The neurophysiological findings of this patient suggested that aEEG 1 h after birth in a preterm infant with later development of cystic PVL could show a severe abnormality, or this could resolve completely 28 h after birth. In this patient, the aEEG 1 h after birth showed a consistently inactive trace. During the recording, her cardiovascular condition was stable. The aEEG was started before administration of surfactant, and other agents affecting aEEG were not used. Therefore, severe depression of aEEG would be caused by fetal brain damage, probably due to placental abruption, and would predict later development of cystic PVL. All control infants without neuroimaging abnormalities showed a normal aEEG pattern. PVL and other diffuse white matter injury in preterm infants may be caused by multiple factors, and the precise mechanism of injury has not been fully elucidated. However, neurophysiological findings of this patient suggest that aEEG findings during the very early period, such as 1 h after birth, provide significant information for predicting PVL. Our previous
Fig. 1. Cranial ultrasonography and magnetic resonance imaging. (a) Cranial ultrasonography coronal section at 22 days of age shows multiple cysts in bilateral deep white matter (arrows). (b and c) Axial fluid-attenuated inversion recovery image (TR/TE = 8002/120 ms) at term-equivalent age shows multiple cysts in deep white matter (arrows).
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Fig. 2. Amplitude-integrated electroencephalogram (aEEG). (a) Upper row: aEEG 1 h after birth shows inactive pattern. Many artifacts were inserted (arrow). Lower row: raw waveform of electroencephalogram shows electrical inactivity. (b) Upper row: aEEG 28 h after birth shows discontinuous pattern. Lower row: raw waveform shows no significant abnormality.
study using conventional EEG also supported this notion because earlier depression shows a higher sensitivity for predicting PVL or neurological outcome in preterm infants [3,4]. In this patient, the aEEG 28 h after birth recovered completely, suggesting that a later recording would have missed the brain injury. This might mean that it would be difficult to evaluate a mild voltage depression in the aEEG sensitively enough in preterm infants because EEG activity <2 Hz is greatly suppressed by special filtration to minimize artifacts, which is one of the main components for evaluating a depression on conventional EEG. A quantitative analysis of aEEG may provide a more precise evaluation. In conclusion, an aEEG 1 h after birth in a preterm infant who later developed cystic PVL could show a severe abnormality or it could resolve completely 28 h after birth. The neurophysiological findings of this
patient suggest that aEEG findings during the very early period after birth may provide significant information for predicting PVL. Further study with a larger number of patients will be needed to understand the significance of aEEG during the very early period after birth in preterm infants for predicting PVL or other encephalopathies of prematurity. References [1] Volpe JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 2009;8:110–24. [2] Watanabe K, Hayakawa F, Okumura A. Neonatal EEG: a powerful tool in the assessment of brain damage in preterm infants. Brain Dev 1999;21:361–72. [3] Kidokoro H, Okumura A, Hayakawa F, Kato T, Maruyama K, Kubota T, et al. Chronologic changes in neonatal EEG findings in periventricular leukomalacia. Pediatrics 2009;124:e468–75.
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T. Kato et al. / Brain & Development 35 (2013) 75–78
[4] Maruyama K, Okumura A, Hayakawa F, Kato T, Kuno K, Watanabe K. Prognostic value of EEG depression in preterm infants for later development of cerebral palsy. Neuropediatrics 2002;33:133–7. [5] Bowen JR, Paradisis M, Shah D. Decreased aEEG continuity and baseline variability in the first 48 hours of life associated with poor short-term outcome in neonates born before 29 weeks gestation. Pediatr Res 2010;67:538–44. [6] Hellstro¨m-Westas L, Klette H, Thorngren-Jerneck K, Rose´n I. Early prediction of outcome with aEEG in preterm infants with large intraventricular hemorrhages. Neuropediatrics 2001;32: 319–24.
[7] Kidokoro H, Kubota T, Hayashi N, Hayakawa M, Takemoto K, Kato Y, et al. Absent cyclicity on aEEG within the first 24 h is associated with brain damage in preterm infants. Neuropediatrics 2010;41:241–5. [8] Quintero RA, Morales WJ, Allen MH, Bornick PW, Johnson PK, Kruger M. Staging of twin–twin transfusion syndrome. J Perinatol 1999;19:550–5. [9] Hellstro¨m-Westas L, Rose´n I. Continuous brain-function monitoring: state of the art in clinical practice. Semin Fetal Neonatal Med 2006;11:503–11.
Case report
Amplitude-integrated electroencephalogram 1 h after birth in a preterm infant with cystic periventricular leukomalacia Toru Kato a,⇑, Akihisa Okumura b, Fumio Hayakawa a, Takeshi Tsuji a, Seiji Hayashi a, Jun Natsume c b
a Department of Pediatrics, Okazaki City Hospital, Okazaki, Japan Department of Pediatrics and Adolescent Medicine, Juntendo University School of Medicine, Tokyo, Japan c Department of Pediatrics, Nagoya University Graduate School of Medicine, Nagoya, Japan
Received 16 October 2011; received in revised form 24 November 2011; accepted 28 November 2011
Abstract We report a preterm infant, who showed abnormal amplitude-integrated electroencephalogram (aEEG) findings 1 h after birth and later developed cystic periventricular leukomalacia (PVL). The patient was a girl with a gestational age of 29 weeks. She was delivered by emergency cesarean section because of placental abruption and intrauterine co-twin demise. Artificial ventilation and administration of surfactant were needed to treat respiratory distress syndrome. Her cardiovascular condition was stable with artificial ventilation. Cranial ultrasonography showed extended cystic PVL after 11 days of age. aEEG 1 h after birth showed a consistently inactive pattern that resolved completely 28 h after birth. The neurophysiological findings of this patient suggest that aEEG findings during the very early period after birth provide significant information for predicting PVL. Ó 2011 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved. Keywords: Amplitude-integrated electroencephalogram; Periventricular leukomalacia; Prediction; Preterm infant; White matter injury
1. Introduction Brain injury in preterm infants has recently been understood as an encephalopathy of prematurity, which consists of periventricular leukomalacia (PVL), diffuse white matter injury, and other neuronal/axonal injuries [1]. These injuries cause cerebral palsy and cognitive/ behavioral/attentional deficits. We reported previously that a conventional electroencephalogram (EEG) is a powerful tool to assess brain damage, such as PVL, in preterm infants during the early neonatal period [2,3]. We also reported that earlier depression on a conven⇑ Corresponding author. Address: Department of Pediatrics, Okazaki City Hospital, 3-1 Goshoai, Koryuji-cho, Okazaki, Aichi 444-8553, Japan. Tel.: +81 564 21 8111; fax: +81 564 25 5531. E-mail address: [email protected] (T. Kato).
tional EEG results in a higher sensitivity for predicting PVL or cerebral palsy in preterm infants [3,4]. However, we could not examine conventional EEG within 3 h after birth because it was difficult to record without disturbing the management of cardiovascular and respiratory stabilization. Amplitude-integrated electroencephalogram (aEEG) is a simple and convenient tool for continuous brainfunction monitoring and is widely used in neonatal intensive care units. Although several studies have demonstrated the predictive value of aEEG for intraventricular hemorrhage or PVL within 12–48 h after birth in preterm infants [5–7], the clinical significance of aEEG within 3 h after birth in preterm infants has rarely been reported. We report a preterm infant, who showed abnormal aEEG findings 1 h after birth and later developed cystic PVL.
0387-7604/$ - see front matter Ó 2011 The Japanese Society of Child Neurology. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.braindev.2011.11.010
76
T. Kato et al. / Brain & Development 35 (2013) 75–78
2. Case report The patient was an 1108-g girl born at 29 weeks of gestation. She was a monochorionic diamniotic twin. At 18 weeks of gestation, she was a recipient of stage 3 twin–twin transfusion syndrome, according to the criteria defined by Quintero et al. [8], and was treated with fetoscopic laser photocoagulation. After the therapy, the signs of twin–twin transfusion syndrome resolved completely. Because of placental abruption and intrauterine co-twin demise, she was delivered by emergency cesarean section in our hospital and was admitted to the neonatal intensive care unit. Her Apgar scores were 2 and 6 at 1 and 5 min, respectively. Venous blood gas analysis upon admission revealed a pH of 7.41, PCO2 at 32 mm Hg, and a base excess of 3.2 mmol/L. Her blood pressures were 47 and 30 mm Hg of systolic and diastolic, respectively. Ventilation was provided artificially, and surfactant was administered because of respiratory distress syndrome. Her cardiovascular condition was stable with artificial ventilation, and her neurological findings were normal. Clinical seizures were not observed. Cranial ultrasonography was performed daily during the first 2 weeks. Abnormal periventricular echogenicity was observed at 2 days of age, and multiple cysts more than 3 mm in diameter appeared at 11 days of age, extending into bilateral deep white matter (Fig. 1a). No other significant complications were observed during the neonatal period. Brain magnetic resonance imaging (MRI) was performed with a 1.5Tesla imager at term-equivalent age, which showed that bilateral cystic PVL extended into deep white matter (Fig. 1b and c). The patient developed spastic diplegia, and her psychomotor development was delayed moderately at 10 months of age. Parental informed consent was obtained for publication of this case report. The aEEG was recorded from 1 h after birth before administration of surfactant using a NicoletOne Monitor nICU (CareFusion, San Diego, CA, USA). A single channel (C3–C4) aEEG was obtained with surface Ag/ AgCl cup electrodes and displayed at 6 cm/h. The
impedance was <5 kO. The recording duration was 70 min. The aEEG consistently showed an inactive or flat pattern (Fig. 2a) according to the criteria defined by Hellstro¨m-Westas et al. [9]. A follow-up aEEG performed 28 h after birth with a recording duration of 70 min showed a discontinuous pattern (Fig. 2b) according to the same criteria, which is a normal finding in preterm infants. Mild cycling was observed. Electrical seizures were not seen. Sedative or antiepileptic drugs were not used. For the control, we also performed aEEG 1–3 h after birth using the same method in five infants in a consecutive period whose gestational age was between 26 and 32 weeks and who had no abnormalities on serial cranial ultrasonography and/or brain MRI during the neonatal period. In all five infants, the aEEG showed a discontinuous pattern. 3. Discussion The neurophysiological findings of this patient suggested that aEEG 1 h after birth in a preterm infant with later development of cystic PVL could show a severe abnormality, or this could resolve completely 28 h after birth. In this patient, the aEEG 1 h after birth showed a consistently inactive trace. During the recording, her cardiovascular condition was stable. The aEEG was started before administration of surfactant, and other agents affecting aEEG were not used. Therefore, severe depression of aEEG would be caused by fetal brain damage, probably due to placental abruption, and would predict later development of cystic PVL. All control infants without neuroimaging abnormalities showed a normal aEEG pattern. PVL and other diffuse white matter injury in preterm infants may be caused by multiple factors, and the precise mechanism of injury has not been fully elucidated. However, neurophysiological findings of this patient suggest that aEEG findings during the very early period, such as 1 h after birth, provide significant information for predicting PVL. Our previous
Fig. 1. Cranial ultrasonography and magnetic resonance imaging. (a) Cranial ultrasonography coronal section at 22 days of age shows multiple cysts in bilateral deep white matter (arrows). (b and c) Axial fluid-attenuated inversion recovery image (TR/TE = 8002/120 ms) at term-equivalent age shows multiple cysts in deep white matter (arrows).
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Fig. 2. Amplitude-integrated electroencephalogram (aEEG). (a) Upper row: aEEG 1 h after birth shows inactive pattern. Many artifacts were inserted (arrow). Lower row: raw waveform of electroencephalogram shows electrical inactivity. (b) Upper row: aEEG 28 h after birth shows discontinuous pattern. Lower row: raw waveform shows no significant abnormality.
study using conventional EEG also supported this notion because earlier depression shows a higher sensitivity for predicting PVL or neurological outcome in preterm infants [3,4]. In this patient, the aEEG 28 h after birth recovered completely, suggesting that a later recording would have missed the brain injury. This might mean that it would be difficult to evaluate a mild voltage depression in the aEEG sensitively enough in preterm infants because EEG activity <2 Hz is greatly suppressed by special filtration to minimize artifacts, which is one of the main components for evaluating a depression on conventional EEG. A quantitative analysis of aEEG may provide a more precise evaluation. In conclusion, an aEEG 1 h after birth in a preterm infant who later developed cystic PVL could show a severe abnormality or it could resolve completely 28 h after birth. The neurophysiological findings of this
patient suggest that aEEG findings during the very early period after birth may provide significant information for predicting PVL. Further study with a larger number of patients will be needed to understand the significance of aEEG during the very early period after birth in preterm infants for predicting PVL or other encephalopathies of prematurity. References [1] Volpe JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 2009;8:110–24. [2] Watanabe K, Hayakawa F, Okumura A. Neonatal EEG: a powerful tool in the assessment of brain damage in preterm infants. Brain Dev 1999;21:361–72. [3] Kidokoro H, Okumura A, Hayakawa F, Kato T, Maruyama K, Kubota T, et al. Chronologic changes in neonatal EEG findings in periventricular leukomalacia. Pediatrics 2009;124:e468–75.
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T. Kato et al. / Brain & Development 35 (2013) 75–78
[4] Maruyama K, Okumura A, Hayakawa F, Kato T, Kuno K, Watanabe K. Prognostic value of EEG depression in preterm infants for later development of cerebral palsy. Neuropediatrics 2002;33:133–7. [5] Bowen JR, Paradisis M, Shah D. Decreased aEEG continuity and baseline variability in the first 48 hours of life associated with poor short-term outcome in neonates born before 29 weeks gestation. Pediatr Res 2010;67:538–44. [6] Hellstro¨m-Westas L, Klette H, Thorngren-Jerneck K, Rose´n I. Early prediction of outcome with aEEG in preterm infants with large intraventricular hemorrhages. Neuropediatrics 2001;32: 319–24.
[7] Kidokoro H, Kubota T, Hayashi N, Hayakawa M, Takemoto K, Kato Y, et al. Absent cyclicity on aEEG within the first 24 h is associated with brain damage in preterm infants. Neuropediatrics 2010;41:241–5. [8] Quintero RA, Morales WJ, Allen MH, Bornick PW, Johnson PK, Kruger M. Staging of twin–twin transfusion syndrome. J Perinatol 1999;19:550–5. [9] Hellstro¨m-Westas L, Rose´n I. Continuous brain-function monitoring: state of the art in clinical practice. Semin Fetal Neonatal Med 2006;11:503–11.