e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 8 ( 2 0 1 4 ) 8 0 6 e8 1 0
Official Journal of the European Paediatric Neurology Society
Case study
Amplitude-integrated EEG revealed nonconvulsive status epilepticus in children with non-accidental head injury Ayuko Igarashi a,*, Akihisa Okumura a, Mitsutaka Komatsu a, Osamu Tomita a, Shinpei Abe a, Mitsuru Ikeno a, Masako Saito a, Tomoyuki Nakazawa b, Toshiaki Shimizu a a b
Department of Pediatrics, Juntendo University Faculty of Medicine, Japan Department of Pediatrics, Juntendo Urayasu Hospital, Japan
article info
abstract
Article history:
Objective: We describe the clinical course and amplitude-integrated EEG findings in three
Received 29 July 2013
children with non-accidental head injury and discuss on the importance of continuous aEEG
Received in revised form
monitoring in infants.
20 January 2014
Methods: NCSE was defined as a continuous 30-min seizure or briefer seizures occurring
Accepted 6 July 2014
consecutively comprising at least 30 min of any 1-h period. Non-accidental head injury was diagnosed on the basis of neuroimaging findings such as subdural hemorrhage. Antiepi-
Keywords:
leptic treatment was performed with continuous amplitude-integrated EEG monitoring.
Amplitude-integrated EEG
Results: The age of the patients ranged from 48 days to nine months. All of them had loss of
Nonconvulsive status epilepticus
consciousness and seizures on presentation. Nonconvulsive status epilepticus without
Saw-tooth pattern
clinical symptoms were recognized in all patients. Vigorous antiepileptic treatment against
Subclinical seizure
nonconvulsive status epilepticus was made in two patients, whereas nonconvulsive status
Non-accidental head injury
epilepticus disappeared within one hour without additional treatment in one.
Encephalopathic children
Conclusions: Our experience indicates that nonconvulsive status epilepticus were not uncommon in children with non-accidental head injury. Continuous amplitude-integrated EEG monitoring will be one of the useful methods in encephalopathic children in order to estimate seizure burden objectively and to treat seizures appropriately. © 2014 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
1.
Introduction
Nonconvulsive status epilepticus (NCSE) is a clinical diagnosis describing prolonged electrographic seizure activity resulting
in nonconvulsive clinical symptoms.1 The frequent occurrence of NCSE has been known in neonates and adults.2,3 Recent studies have shown that subclinical seizures and/or NCSE are not uncommon also in critically ill children.4,5 These
* Corresponding author. Department of Pediatrics, Juntendo University Faculty of Medicine, Hongo 2-1-1, Bunkyo-ku, Tokyo 113-8421, Japan. Tel.: þ81 3 3813 3111; fax: þ81 3 5800 1580. E-mail address: [email protected] (A. Igarashi). http://dx.doi.org/10.1016/j.ejpn.2014.07.003 1090-3798/© 2014 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 8 ( 2 0 1 4 ) 8 0 6 e8 1 0
studies indicate that continuous EEG monitoring is necessary for all encephalopathic children. Amplitude-integrated electroencephalography (aEEG) has been used to monitor brain function, particularly in neonates.2 Its display is time-compressed to allow an overview of long-term trends in cerebral activity. aEEG is useful in evaluating the severity of neonatal encephalopathy and detecting neonatal seizures, especially in those without clinical symptoms. We have also applied aEEG to brain function monitoring in older children. NCSE was commonly observed in children with some types of acute encephalopathy.6,7 aEEG was also useful for the continuous monitoring of repetitive seizures in children with epilepsy.8 We performed continuous aEEG monitoring in three infants with non-accidental head injury (NAHI). NCSE was observed in all of them. We describe the clinical course and aEEG findings of these patients and discuss on the importance of continuous aEEG monitoring in infants with NAHI.
2.
Case study
NCSE was defined as a continuous 30-min seizure or briefer seizures occurring consecutively comprising at least 30 min of any 1-h period.4,5 The recording and interpretation of aEEG
807
was made by general pediatricians under supervision of experienced pediatric neurologists in the Patients 1 and 2, and by experienced pediatric neurologists in the Patient 3. The diagnosis of seizures was made by experienced pediatric neurologists on the basis of raw-EEG findings at the part where the presence of seizures was suspected on aEEG.
2.1.
Patient 1
The patient was a 48-day-old boy. He had two seizures with loss of responsiveness, and right hemiconvulsion lasting for 2 min since the day before admission. He was the second child of non-consanguineous healthy parents. His perinatal and postnatal history was unremarkable. On admission, his consciousness was mildly reduced and his anterior fontanelle was bulging. Otherwise, neurological abnormalities were not found. No wound or subcutaneous hemorrhage was observed. Head CT showed high densities along with the left margin of falx cerebri and in the left occipital area (Fig. 1). Ophthalmological examination showed bilateral retinal hemorrhage. He was diagnosed as having shaken infant syndrome. Intensive treatment including artificial ventilation, fluid replacement, inotrope use was performed. Treatment for seizures was also performed under continuous single-channel aEEG monitoring using bifrontal
Fig. 1 e Patient 1. Top. Head CT on admission. High densities along with the left margin of falx cerebri and in the left occipital area were observed. Middle. Amplitude-integrated EEG on fourth day of illness. Saw-tooth pattern indicates nonconvulsive status epileptics (broken line). Although the dose of midazolam was increased to 0.4 mg/kg/h, nonconvulsive status epileptics persisted. Bottom. Amplitude-integrated EEG on fifth day of illness. Nonconvulsive status epileptics (broken line) persisted and seizures with clinical symptoms appeared sporadically (Sz). Seizures were suppressed after continuous infusion of thiopental.
808
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 8 ( 2 0 1 4 ) 8 0 6 e8 1 0
electrodes. Seizures with clinical symptoms disappear after intravenous phenobarbital and continuous midazolam, whereas aEEG demonstrated the presence of NCSE (Fig. 1). On the next day of admission, right hemiconvulsions were observed again. Continuous thiopental infusion was initiated and, thereafter, disappearance of NCSE or isolated seizures was confirmed on aEEG monitoring (Fig. 1). MRI one month after admission revealed cystic changes in the frontal, temporal and occipital areas of the left hemisphere. At 15 months of age, he could walk without support and speak a few words.
electrodes was started. He was treated with intravenous phenytoin and continuous midazolam infusion. Although both clinical and subclinical seizures were transiently suppressed (Fig. 2), he experienced clinical seizures followed by NCSE (Fig. 2). On the third day after admission, he was transferred to a tertiary medical center for intensive care. He was discharged on 24 days of illness without neurological symptoms. He was admitted to an infant home away from his parents. Information on his long-term outcome was not available.
2.2.
2.3.
Patient 2
The patient was a 4-month-old boy. He was admitted to our hospital because of repetitive seizures with staring and tonic posturing. He was the second child of non-consanguineous healthy parents. His perinatal and postnatal history was unremarkable. On admission, he was alert and vigorous. No abnormalities were noticed on physical and neurological examinations. No wound or subcutaneous hemorrhage was observed. Head MRI showed subdural hematoma and abnormal high intensities in right occipital area on diffusion-weighted images (Fig. 2). Laboratory examinations were unremarkable. Fundoscopy was not performed. Intravenous phenobarbital was administered, whereas seizures with convulsive movements persisted. Continuous monitoring with single-channel aEEG using bifrontal
Patient 3
The patient was a 9-month-old girl. She visited a local hospital because of fever and vomiting. On presentation, right femoral fracture, skull fracture, subdural hemorrhage, and retinal hemorrhage was recognized. She was diagnosed as having abusive head injury. She was born at home. Her gestational age was uncertain because her mother had no prenatal care. After admission, seizures characterized by loss of consciousness, right eye deviation, and right hemiconvulsion lasting for a few minutes were observed. Diazepam and midazolam were administered and seizures with clinical symptoms were suppressed. On the next day, she was transferred to our hospital for intensive care. Her consciousness was mildly reduced and bruises were seen on her neck and right thigh. MRI revealed subdural hematoma around bilateral occipital lobes and cerebellar hemispheres. She had clinical
Fig. 2 e Patient 2. Top. Head MRI on admission. Diffusion-weighted images (left and middle) showed high intensities in the subcortical white matter in the bilateral occipital areas. Subdural hematoma was seen on T2-weighted images (right). Middle. Amplitude-integrated EEG on second day of illness. Nonconvulsive status epileptics was suppressed after infusion of phenytoin. Bottom. Amplitude-integrated EEG on third day of illness. Sz indicates a clinical seizure and asterisks indicates a subclinical seizure. Both of them appeared sporadically.
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 8 ( 2 0 1 4 ) 8 0 6 e8 1 0
seizures on day 3 of illness and continuous multiple-channel aEEG monitoring with 12 scalp electrodes was begun. Clinical seizures ceased spontaneously within a few minutes, whereas NCSE were seen on aEEG (Fig. 3). She was treated with continuous midazolam infusion, and then no clinical or electroencephalographic seizures were observed. She was discharged on the day 21 of illness with left hemiplegia. She was admitted to an infant home away from his parents. Information on her long-term outcome was not available.
3.
Discussion
We successfully monitored NCSE in three infants with NAHI using single-channel aEEG. In addition, application and interpretation of aEEG were relatively easy for untrained pediatricians. Our experience indicates that aEEG is useful for monitoring seizures even in older children and can apply to encephalopathic children of any origin. The most striking observation is NCSE seen in all patients, although the number of patients was small. Brief seizures with subtle clinical manifestations can be missed even when they are observed by caregivers or nurses. Moreover, some seizures can be subclinical without any clinical manifestations. Although it has been established that subclinical seizures are very frequent in neonates,2 recent studies using continuous EEG in pediatric intensive care units or emergency departments have shown the presence of NCSE in 7%e47% of
809
children with altered mental status of various etiologies.4,5,9e12 Deterioration of consciousness may be attributable to undetected NCSE in some critically ill children. Moreover, recent studies have shown that the outcome was considerably worse in patients presenting with NCSE than in those in whom convulsive status epilepticus was treated successfully.13 This highlights the importance of recognition of NCSE. Although the etiology of children with NCSE was different among the studies, central nervous system infection, hypoxic-ischemic encephalopathy and epilepsies were among common causes of NCSE in children. Head trauma was not a major cause of NCSE in previous studies, whereas Williams et al. reported that head trauma was at a higher risk of seizures.9 Hasbani et al. monitored twenty-one children with abusive head trauma, electrographic seizures occurred in 12 of 21 children (57%) and constituted electrographic status epilepticus in 8 of 12 children (67%).14 NCSE in children with NAHI has rarely been reported, and further studies are necessary in order to reveal the prevalence of NCSE in children with NAHI. Furthermore, the effect of NCSE to their outcome should be investigated, because recent studies have shown that NCSE is associated with mortality and worse short-term outcome.4 It is noteworthy that treatment was strengthened in all our infants after the recognition of NCSE. Although, at present, it is undetermined whether or not the attempt to control NCSE can alter the outcome of the patient, the recognition of NCSE will change treatment regimen.
Fig. 3 e Patient 3. Amplitude-integrated EEG on third day of illness. Saw-tooth pattern indicated nonconvulsive status epileptics (broken line) lasting for 40 min after a brief clinical seizure. Raw EEG at the vertical line showed rhythmic lowamplitude delta waves in the right centro-temporal area.
810
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 8 ( 2 0 1 4 ) 8 0 6 e8 1 0
Although continuous multi-channel conventional EEG (cEEG) is clearly superior to aEEG for a detailed diagnosis of NCSE,15 there are some difficulties to perform continuous cEEG monitoring in Japan. Trained pediatric neurologists or epileptologists are necessary to interpret cEEG accurately. Specialized technicians are also required to record highquality EEG for a long time. These conditions are hardly fulfilled in most hospitals in Japan. Therefore, aEEG will be useful as a surrogate device. Electrodes are easy to apply and maintain even for beginner because of a small number of electrodes. Recording of aEEG can be started immediately after admission without expert attendance. We consider that our study successfully showed the usefulness of aEEG for recognition of NCSE, although we must stress that final diagnosis of NSCE and making treatment decisions should be based on cEEG findings. It is also evident that there are several limitations of aEEG. aEEG is usually performed with a limited number of electrodes. In our patient, single-channel recording was applied with bifrontal electrodes, which is suitable for stable electrode placement due to no interference from hair. However, our previous studies on the rate of seizure detection among neonates demonstrated that only 40% of seizures were detected using bifrontal single-channel EEG.16 This clearly indicates that under-estimation of seizures may not be inevitable in single-channel aEEG monitoring. In order to detect seizures more sensitively, multi-channel recording is necessary. Laterality of seizure origin in case of focal seizures is difficult to determine by single-channel aEEG, because montage connecting the electrodes symmetrically placed in both hemispheres is usually applied. The number of the patients was small in this study, because our hospital does not have pediatric intensive care unit. In order to clarify the efficacy of aEEG monitoring, caseecontrol studies comparing aEEG and cEEG should be performed in the hospitals with large pediatric intensive care unit. Misinterpretation of aEEG findings can lead to over-estimation of seizures. There have been several studies on the accuracy of interpretation of aEEG.2,14 These studies imply that misinterpretation of artifact into ictal changes will not be uncommon. In our patients, recording and interpretation of aEEG was supervised by experienced pediatric neurologists in order to avoid misinterpretation. Education of doctors and nursing staffs and expert supervision will be essential to interpret aEEG findings accurately. In conclusion, subclinical seizures and/or NCSE were observed on continuous aEEG monitoring in all three infants with NAHI. Continuous aEEG monitoring should be performed in encephalopathic children in order to estimate seizure burden objectively and to treat seizures appropriately. aEEG will be one of useful methods for continuous EEG monitoring.
Conflict of interest None declared.
Acknowledgments We thank all doctors and nursing staffs who treated and cared these children and supported our study.
references
1. Walker M, Cross H, Smith S, et al. Nonconvulsive status epilepticus: epilepsy research foundation workshop reports. Epileptic Disord 2005;7:253e96. € m-Westas L, Rose n I. Continuous brain-function 2. Hellstro monitoring: state of the art in clinical practice. Semin Fetal Neonatal Med 2006;11:503e11. 3. Sutter R, Kaplan PW. Electroencephalographic criteria for nonconvulsive status epilepticus: synopsis and comprehensive survey. Epilepsia 2012;53(Suppl. 3):1e51. 4. Topjian AA, Gutierrez-Colina AM, Sanchez SM, et al. Electrographic status epilepticus is associated with mortality and worse short-term outcome in critically ill children. Crit Care Med 2013;41:215e23. 5. Greiner HM, Holland K, Leach JL, et al. Nonconvulsive status epilepticus: the encephalopathic pediatric patient. Pediatrics 2012;129:748e55. 6. Okumura A, Komatsu M, Abe S, et al. Amplitude-integrated electroencephalography in patients with acute encephalopathy with refractory, repetitive partial seizures. Brain Dev 2011;33:77e82. 7. Komatsu M, Okumura A, Matsui K, et al. Clustered subclinical seizures in a patient with acute encephalopathy with biphasic seizures and late reduced diffusion. Brain Dev 2010;32:472e6. 8. Okumura A, Komatsu M, Kitamura T, et al. Usefulness of single-channel amplitude-integrated electroencephalography for continuous seizure monitoring in infancy: a case report. Brain Dev 2009;31:766e70. 9. Williams K, Jarrar R, Buchhalter J. Continuous video-EEG monitoring in pediatric intensive care units. Epilepsia 2011;52:1130e6. 10. McCoy B, Sharma R, Ochi A, et al. Predictors of nonconvulsive seizures among critically ill children. Epilepsia 2011;52:1973e8. 11. Abend NS, Gutierrez-Colina AM, Topjian AA, et al. Nonconvulsive seizures are common in critically ill children. Neurology 2011;76:1071e7. 12. Hyllienmark L, Amark P. Continuous EEG monitoring in a paediatric intensive care unit. Eur J Paediatr Neurol 2007;11:70e5. 13. Korff CM, Nordli Jr DR. Diagnosis and management of nonconvulsive status epilepticus in children. Nat Clin Pract Neurol 2007;3:505e16. 14. Hasbani DM, Topjian AA, Friess SH, et al. Nonconvulsive electrographic seizures are common in children with abusive head trauma. Pediatr Drit Care Med 2013;14:709e15. 15. Shellhaas RA, Soaita AI, Clancy RR. Sensitivity of amplitudeintegrated electroencephalography for neonatal seizure detection. Pediatrics 2007;120:770e7. 16. Kidokoro H, Kubota T, Hayakawa M, Kato Y, Okumura A. Neonatal seizure identification on reduced channel EEG. Arch Dis Child Fetal Neonatal Ed 2013;98:359e61.
Official Journal of the European Paediatric Neurology Society
Case study
Amplitude-integrated EEG revealed nonconvulsive status epilepticus in children with non-accidental head injury Ayuko Igarashi a,*, Akihisa Okumura a, Mitsutaka Komatsu a, Osamu Tomita a, Shinpei Abe a, Mitsuru Ikeno a, Masako Saito a, Tomoyuki Nakazawa b, Toshiaki Shimizu a a b
Department of Pediatrics, Juntendo University Faculty of Medicine, Japan Department of Pediatrics, Juntendo Urayasu Hospital, Japan
article info
abstract
Article history:
Objective: We describe the clinical course and amplitude-integrated EEG findings in three
Received 29 July 2013
children with non-accidental head injury and discuss on the importance of continuous aEEG
Received in revised form
monitoring in infants.
20 January 2014
Methods: NCSE was defined as a continuous 30-min seizure or briefer seizures occurring
Accepted 6 July 2014
consecutively comprising at least 30 min of any 1-h period. Non-accidental head injury was diagnosed on the basis of neuroimaging findings such as subdural hemorrhage. Antiepi-
Keywords:
leptic treatment was performed with continuous amplitude-integrated EEG monitoring.
Amplitude-integrated EEG
Results: The age of the patients ranged from 48 days to nine months. All of them had loss of
Nonconvulsive status epilepticus
consciousness and seizures on presentation. Nonconvulsive status epilepticus without
Saw-tooth pattern
clinical symptoms were recognized in all patients. Vigorous antiepileptic treatment against
Subclinical seizure
nonconvulsive status epilepticus was made in two patients, whereas nonconvulsive status
Non-accidental head injury
epilepticus disappeared within one hour without additional treatment in one.
Encephalopathic children
Conclusions: Our experience indicates that nonconvulsive status epilepticus were not uncommon in children with non-accidental head injury. Continuous amplitude-integrated EEG monitoring will be one of the useful methods in encephalopathic children in order to estimate seizure burden objectively and to treat seizures appropriately. © 2014 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
1.
Introduction
Nonconvulsive status epilepticus (NCSE) is a clinical diagnosis describing prolonged electrographic seizure activity resulting
in nonconvulsive clinical symptoms.1 The frequent occurrence of NCSE has been known in neonates and adults.2,3 Recent studies have shown that subclinical seizures and/or NCSE are not uncommon also in critically ill children.4,5 These
* Corresponding author. Department of Pediatrics, Juntendo University Faculty of Medicine, Hongo 2-1-1, Bunkyo-ku, Tokyo 113-8421, Japan. Tel.: þ81 3 3813 3111; fax: þ81 3 5800 1580. E-mail address: [email protected] (A. Igarashi). http://dx.doi.org/10.1016/j.ejpn.2014.07.003 1090-3798/© 2014 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 8 ( 2 0 1 4 ) 8 0 6 e8 1 0
studies indicate that continuous EEG monitoring is necessary for all encephalopathic children. Amplitude-integrated electroencephalography (aEEG) has been used to monitor brain function, particularly in neonates.2 Its display is time-compressed to allow an overview of long-term trends in cerebral activity. aEEG is useful in evaluating the severity of neonatal encephalopathy and detecting neonatal seizures, especially in those without clinical symptoms. We have also applied aEEG to brain function monitoring in older children. NCSE was commonly observed in children with some types of acute encephalopathy.6,7 aEEG was also useful for the continuous monitoring of repetitive seizures in children with epilepsy.8 We performed continuous aEEG monitoring in three infants with non-accidental head injury (NAHI). NCSE was observed in all of them. We describe the clinical course and aEEG findings of these patients and discuss on the importance of continuous aEEG monitoring in infants with NAHI.
2.
Case study
NCSE was defined as a continuous 30-min seizure or briefer seizures occurring consecutively comprising at least 30 min of any 1-h period.4,5 The recording and interpretation of aEEG
807
was made by general pediatricians under supervision of experienced pediatric neurologists in the Patients 1 and 2, and by experienced pediatric neurologists in the Patient 3. The diagnosis of seizures was made by experienced pediatric neurologists on the basis of raw-EEG findings at the part where the presence of seizures was suspected on aEEG.
2.1.
Patient 1
The patient was a 48-day-old boy. He had two seizures with loss of responsiveness, and right hemiconvulsion lasting for 2 min since the day before admission. He was the second child of non-consanguineous healthy parents. His perinatal and postnatal history was unremarkable. On admission, his consciousness was mildly reduced and his anterior fontanelle was bulging. Otherwise, neurological abnormalities were not found. No wound or subcutaneous hemorrhage was observed. Head CT showed high densities along with the left margin of falx cerebri and in the left occipital area (Fig. 1). Ophthalmological examination showed bilateral retinal hemorrhage. He was diagnosed as having shaken infant syndrome. Intensive treatment including artificial ventilation, fluid replacement, inotrope use was performed. Treatment for seizures was also performed under continuous single-channel aEEG monitoring using bifrontal
Fig. 1 e Patient 1. Top. Head CT on admission. High densities along with the left margin of falx cerebri and in the left occipital area were observed. Middle. Amplitude-integrated EEG on fourth day of illness. Saw-tooth pattern indicates nonconvulsive status epileptics (broken line). Although the dose of midazolam was increased to 0.4 mg/kg/h, nonconvulsive status epileptics persisted. Bottom. Amplitude-integrated EEG on fifth day of illness. Nonconvulsive status epileptics (broken line) persisted and seizures with clinical symptoms appeared sporadically (Sz). Seizures were suppressed after continuous infusion of thiopental.
808
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 8 ( 2 0 1 4 ) 8 0 6 e8 1 0
electrodes. Seizures with clinical symptoms disappear after intravenous phenobarbital and continuous midazolam, whereas aEEG demonstrated the presence of NCSE (Fig. 1). On the next day of admission, right hemiconvulsions were observed again. Continuous thiopental infusion was initiated and, thereafter, disappearance of NCSE or isolated seizures was confirmed on aEEG monitoring (Fig. 1). MRI one month after admission revealed cystic changes in the frontal, temporal and occipital areas of the left hemisphere. At 15 months of age, he could walk without support and speak a few words.
electrodes was started. He was treated with intravenous phenytoin and continuous midazolam infusion. Although both clinical and subclinical seizures were transiently suppressed (Fig. 2), he experienced clinical seizures followed by NCSE (Fig. 2). On the third day after admission, he was transferred to a tertiary medical center for intensive care. He was discharged on 24 days of illness without neurological symptoms. He was admitted to an infant home away from his parents. Information on his long-term outcome was not available.
2.2.
2.3.
Patient 2
The patient was a 4-month-old boy. He was admitted to our hospital because of repetitive seizures with staring and tonic posturing. He was the second child of non-consanguineous healthy parents. His perinatal and postnatal history was unremarkable. On admission, he was alert and vigorous. No abnormalities were noticed on physical and neurological examinations. No wound or subcutaneous hemorrhage was observed. Head MRI showed subdural hematoma and abnormal high intensities in right occipital area on diffusion-weighted images (Fig. 2). Laboratory examinations were unremarkable. Fundoscopy was not performed. Intravenous phenobarbital was administered, whereas seizures with convulsive movements persisted. Continuous monitoring with single-channel aEEG using bifrontal
Patient 3
The patient was a 9-month-old girl. She visited a local hospital because of fever and vomiting. On presentation, right femoral fracture, skull fracture, subdural hemorrhage, and retinal hemorrhage was recognized. She was diagnosed as having abusive head injury. She was born at home. Her gestational age was uncertain because her mother had no prenatal care. After admission, seizures characterized by loss of consciousness, right eye deviation, and right hemiconvulsion lasting for a few minutes were observed. Diazepam and midazolam were administered and seizures with clinical symptoms were suppressed. On the next day, she was transferred to our hospital for intensive care. Her consciousness was mildly reduced and bruises were seen on her neck and right thigh. MRI revealed subdural hematoma around bilateral occipital lobes and cerebellar hemispheres. She had clinical
Fig. 2 e Patient 2. Top. Head MRI on admission. Diffusion-weighted images (left and middle) showed high intensities in the subcortical white matter in the bilateral occipital areas. Subdural hematoma was seen on T2-weighted images (right). Middle. Amplitude-integrated EEG on second day of illness. Nonconvulsive status epileptics was suppressed after infusion of phenytoin. Bottom. Amplitude-integrated EEG on third day of illness. Sz indicates a clinical seizure and asterisks indicates a subclinical seizure. Both of them appeared sporadically.
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 8 ( 2 0 1 4 ) 8 0 6 e8 1 0
seizures on day 3 of illness and continuous multiple-channel aEEG monitoring with 12 scalp electrodes was begun. Clinical seizures ceased spontaneously within a few minutes, whereas NCSE were seen on aEEG (Fig. 3). She was treated with continuous midazolam infusion, and then no clinical or electroencephalographic seizures were observed. She was discharged on the day 21 of illness with left hemiplegia. She was admitted to an infant home away from his parents. Information on her long-term outcome was not available.
3.
Discussion
We successfully monitored NCSE in three infants with NAHI using single-channel aEEG. In addition, application and interpretation of aEEG were relatively easy for untrained pediatricians. Our experience indicates that aEEG is useful for monitoring seizures even in older children and can apply to encephalopathic children of any origin. The most striking observation is NCSE seen in all patients, although the number of patients was small. Brief seizures with subtle clinical manifestations can be missed even when they are observed by caregivers or nurses. Moreover, some seizures can be subclinical without any clinical manifestations. Although it has been established that subclinical seizures are very frequent in neonates,2 recent studies using continuous EEG in pediatric intensive care units or emergency departments have shown the presence of NCSE in 7%e47% of
809
children with altered mental status of various etiologies.4,5,9e12 Deterioration of consciousness may be attributable to undetected NCSE in some critically ill children. Moreover, recent studies have shown that the outcome was considerably worse in patients presenting with NCSE than in those in whom convulsive status epilepticus was treated successfully.13 This highlights the importance of recognition of NCSE. Although the etiology of children with NCSE was different among the studies, central nervous system infection, hypoxic-ischemic encephalopathy and epilepsies were among common causes of NCSE in children. Head trauma was not a major cause of NCSE in previous studies, whereas Williams et al. reported that head trauma was at a higher risk of seizures.9 Hasbani et al. monitored twenty-one children with abusive head trauma, electrographic seizures occurred in 12 of 21 children (57%) and constituted electrographic status epilepticus in 8 of 12 children (67%).14 NCSE in children with NAHI has rarely been reported, and further studies are necessary in order to reveal the prevalence of NCSE in children with NAHI. Furthermore, the effect of NCSE to their outcome should be investigated, because recent studies have shown that NCSE is associated with mortality and worse short-term outcome.4 It is noteworthy that treatment was strengthened in all our infants after the recognition of NCSE. Although, at present, it is undetermined whether or not the attempt to control NCSE can alter the outcome of the patient, the recognition of NCSE will change treatment regimen.
Fig. 3 e Patient 3. Amplitude-integrated EEG on third day of illness. Saw-tooth pattern indicated nonconvulsive status epileptics (broken line) lasting for 40 min after a brief clinical seizure. Raw EEG at the vertical line showed rhythmic lowamplitude delta waves in the right centro-temporal area.
810
e u r o p e a n j o u r n a l o f p a e d i a t r i c n e u r o l o g y 1 8 ( 2 0 1 4 ) 8 0 6 e8 1 0
Although continuous multi-channel conventional EEG (cEEG) is clearly superior to aEEG for a detailed diagnosis of NCSE,15 there are some difficulties to perform continuous cEEG monitoring in Japan. Trained pediatric neurologists or epileptologists are necessary to interpret cEEG accurately. Specialized technicians are also required to record highquality EEG for a long time. These conditions are hardly fulfilled in most hospitals in Japan. Therefore, aEEG will be useful as a surrogate device. Electrodes are easy to apply and maintain even for beginner because of a small number of electrodes. Recording of aEEG can be started immediately after admission without expert attendance. We consider that our study successfully showed the usefulness of aEEG for recognition of NCSE, although we must stress that final diagnosis of NSCE and making treatment decisions should be based on cEEG findings. It is also evident that there are several limitations of aEEG. aEEG is usually performed with a limited number of electrodes. In our patient, single-channel recording was applied with bifrontal electrodes, which is suitable for stable electrode placement due to no interference from hair. However, our previous studies on the rate of seizure detection among neonates demonstrated that only 40% of seizures were detected using bifrontal single-channel EEG.16 This clearly indicates that under-estimation of seizures may not be inevitable in single-channel aEEG monitoring. In order to detect seizures more sensitively, multi-channel recording is necessary. Laterality of seizure origin in case of focal seizures is difficult to determine by single-channel aEEG, because montage connecting the electrodes symmetrically placed in both hemispheres is usually applied. The number of the patients was small in this study, because our hospital does not have pediatric intensive care unit. In order to clarify the efficacy of aEEG monitoring, caseecontrol studies comparing aEEG and cEEG should be performed in the hospitals with large pediatric intensive care unit. Misinterpretation of aEEG findings can lead to over-estimation of seizures. There have been several studies on the accuracy of interpretation of aEEG.2,14 These studies imply that misinterpretation of artifact into ictal changes will not be uncommon. In our patients, recording and interpretation of aEEG was supervised by experienced pediatric neurologists in order to avoid misinterpretation. Education of doctors and nursing staffs and expert supervision will be essential to interpret aEEG findings accurately. In conclusion, subclinical seizures and/or NCSE were observed on continuous aEEG monitoring in all three infants with NAHI. Continuous aEEG monitoring should be performed in encephalopathic children in order to estimate seizure burden objectively and to treat seizures appropriately. aEEG will be one of useful methods for continuous EEG monitoring.
Conflict of interest None declared.
Acknowledgments We thank all doctors and nursing staffs who treated and cared these children and supported our study.
references
1. Walker M, Cross H, Smith S, et al. Nonconvulsive status epilepticus: epilepsy research foundation workshop reports. Epileptic Disord 2005;7:253e96. € m-Westas L, Rose n I. Continuous brain-function 2. Hellstro monitoring: state of the art in clinical practice. Semin Fetal Neonatal Med 2006;11:503e11. 3. Sutter R, Kaplan PW. Electroencephalographic criteria for nonconvulsive status epilepticus: synopsis and comprehensive survey. Epilepsia 2012;53(Suppl. 3):1e51. 4. Topjian AA, Gutierrez-Colina AM, Sanchez SM, et al. Electrographic status epilepticus is associated with mortality and worse short-term outcome in critically ill children. Crit Care Med 2013;41:215e23. 5. Greiner HM, Holland K, Leach JL, et al. Nonconvulsive status epilepticus: the encephalopathic pediatric patient. Pediatrics 2012;129:748e55. 6. Okumura A, Komatsu M, Abe S, et al. Amplitude-integrated electroencephalography in patients with acute encephalopathy with refractory, repetitive partial seizures. Brain Dev 2011;33:77e82. 7. Komatsu M, Okumura A, Matsui K, et al. Clustered subclinical seizures in a patient with acute encephalopathy with biphasic seizures and late reduced diffusion. Brain Dev 2010;32:472e6. 8. Okumura A, Komatsu M, Kitamura T, et al. Usefulness of single-channel amplitude-integrated electroencephalography for continuous seizure monitoring in infancy: a case report. Brain Dev 2009;31:766e70. 9. Williams K, Jarrar R, Buchhalter J. Continuous video-EEG monitoring in pediatric intensive care units. Epilepsia 2011;52:1130e6. 10. McCoy B, Sharma R, Ochi A, et al. Predictors of nonconvulsive seizures among critically ill children. Epilepsia 2011;52:1973e8. 11. Abend NS, Gutierrez-Colina AM, Topjian AA, et al. Nonconvulsive seizures are common in critically ill children. Neurology 2011;76:1071e7. 12. Hyllienmark L, Amark P. Continuous EEG monitoring in a paediatric intensive care unit. Eur J Paediatr Neurol 2007;11:70e5. 13. Korff CM, Nordli Jr DR. Diagnosis and management of nonconvulsive status epilepticus in children. Nat Clin Pract Neurol 2007;3:505e16. 14. Hasbani DM, Topjian AA, Friess SH, et al. Nonconvulsive electrographic seizures are common in children with abusive head trauma. Pediatr Drit Care Med 2013;14:709e15. 15. Shellhaas RA, Soaita AI, Clancy RR. Sensitivity of amplitudeintegrated electroencephalography for neonatal seizure detection. Pediatrics 2007;120:770e7. 16. Kidokoro H, Kubota T, Hayakawa M, Kato Y, Okumura A. Neonatal seizure identification on reduced channel EEG. Arch Dis Child Fetal Neonatal Ed 2013;98:359e61.
