Brief Communication
Defective Auditory Processing in a Child With Temporal Epileptic Focus
Journal of Child Neurology 2015, Vol. 30(4) 513-516 ª The Author(s) 2014 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0883073814532548 jcn.sagepub.com
Avinoam Shuper, MD1, Mordechai Medvedovsky, MD2, and Sara Kivity, MD1
Abstract A 9-year-old boy presented with intolerance to noise that was a trigger for violent temper tantrums that occasionally resembled complex partial seizures. The condition was also a cause for withdrawal from all activities and settings that could potentially be associated with noise. Both electroencephalography and magnetoencephalography clearly demonstrated a left temporal (T5) epileptic focus, although the child never had convulsive seizures. Genetic studies failed to reveal a GRIN2A mutation. We suggest that the hyperacusis in the reported child is another variation of the Landau-Kleffner spectrum. Keywords hyperacusis, temper tantrums, Landau-Kleffner, temporal epileptic focus Received March 23, 2014. Accepted for publication March 28, 2014.
The epilepsy-aphasia spectrum ranges from Landau-Kleffner syndrome and epileptic encephalopathy with continuous spike and wave during sleep in the most severe form to benign childhood epilepsy with centrotemporal spikes in the milder form.1 Language skills are commonly affected in these disorders. Landau-Kleffner syndrome in children is characterized by acquired aphasia and verbal auditory agnosia, with or without seizures, and with the appearance of predominantly temporal spikes or other epileptic activity in the electroencephalogram (EEG). Onset is usually between 3 and 10 years of age. The acquired aphasia in Landau-Kleffner syndrome is considered to be secondary to the epileptic activity that involves the cortical language network. The epileptic discharges are assumed to form the basis of language decline.2 Focal epileptiform activity, mainly temporal, can also be associated with speech, language, and cognitive dysfunction.3 GRIN2A mutations have been found in about 20% of cases of acquired epileptic aphasia, and related childhood focal epilepsies and encephalopathies were identified in cases of speech and language dysfunction. Those mutations were found to be significant in idiopathic focal epilepsy with rolandic spikes.4 This report describes a child who presented with behavioral disturbances associated with intolerance to noise and who exhibited a prominent left temporal epileptic focus. Informed consent to publish this report was obtained from the mother of this child.
Case Report A 9-year-old child from Russia presented to our neurology clinic because of severe behavioral disturbances. The major
complaint was severe and violent temper tantrums during which he hit and kicked everyone who was present. It took several hours to calm him down. He was born after a normal and uneventful pregnancy and delivery. He began having frequent attacks of vomiting at 7 months of age, for which he underwent a medical workup in Russia and was treated with various diets for suspected food intolerance. At around the age of 3 years, he exhibited difficulties in speech, which were treated with some success by an animal-derived cerebral cortical polypeptide (Cortexin, Geropharm, Russia). The brain magnetic resonance imaging (MRI) scan he had undergone in Russia was normal. The child had never had a true seizure. His mother reported that he had fine motor difficulties that eventually resolved. His speech development was slow: his vocabulary included only a few words at the age of 3 years, for which he was treated by a speech-language pathologist. He has always had difficulties in socializing with others and in adapting to any structured educational facility. His parents are university graduates. They
1
Department of Pediatric Neurology and Epilepsy Center, Schneider Children’s Medical Center of Israel, Petah Tiqva, Israel, affiliated to the Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel 2 Gonda Brain Research Center, Bar Ilan University, Israel Corresponding Author: Avinoam Shuper, MD, Department of Pediatric Neurology and Epilepsy Center, Schneider Children’s Medical Center of Israel, Petah Tiqva 49202, Israel. Email: [email protected]
Downloaded from jcn.sagepub.com at Purdue University on June 4, 2015
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Journal of Child Neurology 30(4)
Figure 1. Sleep electroencephalographic (EEG) recording showing left temporal (T5) epileptic focus.
Figure 2. Magnetoelectroencephalographic pattern showing a very large and prominent left midtemporal seizure activity.
are divorced and the child lives in Israel with his mother. There is no family history of seizures. The results of our physical and neurologic examination of the child were normal. Repeated challenging with various food products ruled out abnormal food reaction, and metabolic disorders were excluded by studies of blood chemistry and gases, measurements of the levels of ammonia, plasma amino acids, urine organic acids, carnitine and acylcarnitine, as well as by thyroid and adrenal function tests. The result of the chromosomal microarray analysis was normal, and testing for the GRIN2A mutation was negative (Dr Gaetan Lesca, France). A psychological examination revealed a very large vocabulary for his age, but his rates of performing tasks and thinking were very slow. He seemed to be depressive. His cognitive function was average, with higher function scored for verbal abilities. The possibility of autistic features was raised. The most prominent problem in his current behavior was hypersensitivity to
noise. Noises could make him lose control and violently attack those around him, after which it could take up to several hours to calm him down. This reaction severely limited his ability to be present in social, educational, and recreational settings. His initial EEG from Russia had revealed potential epileptic activity. The wakeful EEG performed in our clinic was normal, but a sleep recording clearly demonstrated a left temporal epileptic focus (Figure 1). He was started on valproic acid in a dose of 15 mg/kg alone and then in combination with risperidone 0.5 mg/d. Improvement was marked with this treatment such that he was able to visit Russia for several months, after which he returned to Israel and could attend a local school. One attack was witnessed in our clinic: the sudden ringing of a telephone led to an immediate change in mood and facial expression. He complained of headache, after which he demonstrated hyperexcitability, severe restlessness, and violent behavior, which gradually lessened over several minutes. He was referred to another EEG during which the ringing of a telephone was used in an attempt to trigger a seizure, but no seizure discharges were obtained by this maneuver. He then underwent magnetoencephalography. The recording was conducted by using a whole head system (Magnes 3600 WH) equipped with 248 magnetometers and 23 reference channels that record magnetic field changes distant from the head (environmental noise). Data recorded from these channels were used for further noise reduction during magnetoencephalography measurements. In addition, the data were cleaned online using a 1 to 200 Hz bandpass filter. The sampling rate was 678 Hz. The magnetoencephalography was recorded during both wakefulness and drowsiness in the evening close to the child’s usual bedtime. Epileptic activity in the form of frequent spike and wave complexes was recorded. The sources of this activity were localized in the left perisylvian area, that is, temporal, frontal and parietal opercula and insula (Figure 2). Exposure to loud noise led to immediate headache but did not affect the magnetoencephalography trace. At this stage, the valproic acid regime was changed to the sulthiame (Ospolot®, Desitin Arzneimittel GmbH) 200 mg/d. There was some improvement in behavior, but he still complained of headaches and was severely incapacitated by sudden and loud noises. There seem to be slow but persistent mental deterioration. The prominent temporal activity led to a presumptive diagnosis of the hyperacusis as resulting from inappropriate central processing of noise, a disturbance reported to be present in children with Landau-Kleffner syndrome.5
Discussion We describe a child with markedly exaggerated response to noise (hyperacusis) that could lead to loss of self-control and to violent behavior. The administration of valproic acid together with risperidone resulted in significant clinical improvement. A left temporal epileptic focus was found on a wakeful EEG. The differential diagnosis of this child is very interesting. He has hyperacusis, in which everyday sounds are perceived
Downloaded from jcn.sagepub.com at Purdue University on June 4, 2015
Shuper et al
515
as being unbearable, strong, or painful and which can by itself be associated with psychological disturbances. Hyperacusis is described in Williams syndrome, and sensory overresponsiveness and psychopathology were described in familial impairments, but our patient did not exhibit other key characteristics of those conditions.6 Another potential diagnosis was reflex epilepsy, in which noise7 or telephone ringing8 can trigger seizures, but repeated attempts to elicit a convulsive seizure by both sound sources failed to achieve any changes in his EEG recordings. The findings on his magnetoencephalography led us to consider the potential diagnosis of acquired epileptiform opercular syndrome, but our patient never had overt convulsive seizures or oral motor dysfunction.9 There is a diagnostic possibility of ictal vomiting, taking into consideration his past history of recurrent vomiting episodes together with the inability to exclude that they had been a true seizure manifestation.10,11 However, vomiting was no longer a predominant feature of his behavior when he was evaluated in our neurology clinic. After ruling out those alternatives, we concluded that the most appropriate diagnosis was an epilepsy–aphasia spectrum disorder12,13 leading to abnormal central auditory processing manifesting clinically as hyperacusis. The magnetoencephalography pattern supports this connection.14 A defective auditory processing is a well-recognized feature of Landau-Kleffner syndrome.15 Selassie et al3 reported dysfunction of auditory perception in noise in more than half of their study participants who had focal epileptiform activity. It is possible that the presence of temporal epileptic focus may be related to a large spectrum of auditory- or languageassociated disorders. We had earlier noted a relation between selective mutism and temporal foci.16 There is an increasing amount of data to support the notion that language dysfunction can be related to a spectrum of disorders which encompass the involvement of the temporal lobe(s) as a source of abnormal EEGs17 and which are probably part of an expanding ‘‘spectrum’’ of Landau-Kleffner syndrome. Selassie et al3 concluded that focal epileptiform activity can be associated not only by language dysfunction but also by auditory dysfunction, oralmotor dysfunction, and stuttering. In addition to variations on EEGs, the clinical manifestations may include autism, attention deficit hyperactivity disorder, learning disability, mental retardation and others, and the affected children do not necessarily seize. GRIN2A mutations are found in a part but not in most of these children.4 Lesca et al18 showed an overrepresentation of cell adhesion genes in Landau-Kleffner syndrome and autistic spectrum disorders, and suggested that there is a potential mechanism to explain the clinical link between the two. We suggest that the hyperacusis in the reported child represents an abnormality in the central processing of noise, and that abnormal central processing of noise may be considered a heretofore undescribed part of the Landau-Kleffner syndrome spectrum. Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The authors received no financial support for the research, authorship, and/or publication of this article.
Ethical Approval Being a case report, the need for the Hospital Helsinki Board was waived. The publication of the manuscript was fully approved by the child’s mother who also read the manuscript.
References 1. Deonna T, Rouket-Perez E. Early-onset acquired epileptic aphasia (Landau-Kleffner syndrome, LKS) and regressive autistic disorders with epileptic EEG abnormalities: the continuing debate. Brain Dev. 2010;32:746-752. 2. Datta AN, Oser N, Ramelli GP, et al. BECTS evolving to Landau-Kleffner syndrome and back by subsequent recovery: a longitudinal language reorganization case study using fMRI, source EEG and psychological testing. Epilepsy Behav. 2013; 27:107-114. 3. Selassie GR-H, Hedstrom A, Viggedal G, et al. Speech, language and cognitive dysfunction in children with focal epileptiform activity: a follow-up study. Epilepsy Behav. 2010;18: 267-275. 4. Lesca G, Rudolf G, Bruneau N, et al. GRIN2A mutations in acquired epileptic aphasia and related childhood focal epilepsies and encephalopathies with speech and language dysfunction. Nat Genet. 2013;45:1061-1066. 5. Fandino M, Connoly M, Usher L, Palm S, Kozak FK. LandauKleffner syndrome: a rare auditory processing disorder. Series of cases and review of the literature. Int J Pediatr Otorhinolaryngol. 2011;75:33-38. 6. Zarchi O, Attias J, Gothelf D. Auditory and visual processing in Williams syndrome. Isr J Psychiatry Relat Sci. 2010;47: 125-131. 7. Ferlazzo E, Zifkin BG, Andermann E, Andermann F. Cortical triggers in generalized reflex seizures and epilepsies. Brain. 2005;128:700-710. 8. Michelucci R, Mecarelli O, Bovo G, et al. A de-novo LGI1 mutation causing idiopathic partial epilepsy with telephone-induced seizures. Neurology. 2007;68:2150-2151. 9. Shafrir Y, Prensky AL. Acquired epileptiform opercular syndrome: a second case report, review of the literature and comparison to the Landau-Kleffner syndrome. Epilepsia. 1995;36: 1050-1057. 10. Schindler K, Wieser HG. Ictal vomiting in a left hemisphere language dominant patient with left-sided temporal lobe epilepsy. Epilepsy Behav. 2006;8:323-327. 11. Shuper A, Goldberg-Stern H. Ictus emeticus (ictal vomiting). Pediatr Neurol. 2004;31:283-286. 12. Tsai M-H, Vears DF, Turner SJ, et al. Clinical genetic study of the epilepsy-aphasia spectrum. Epilepsia. 2013;54:280-287. 13. Carvill GM, Regan B, Yendle SC, et al. GRIN2A mutations cause epilepsy-aphasia spectrum disorders. Nat Genet. 2013; 45:1073-1076. 14. Lewine JD, Andrews R, Chez M, et al. Magnetoencephalographic patterns of epileptiform activity in children with
Downloaded from jcn.sagepub.com at Purdue University on June 4, 2015
516
Journal of Child Neurology 30(4)
regressive autism spectrum disorders. Pediatrics. 1999;104: 405-418. 15. Rapin I, Mattis S, Rowan AJ, Golden GG. Verbal auditory agnosia in children. Dev Med Child Neurol. 1977;19:192-207. 16. Politi K, Kivity S, Goldberg-Stern H, et al. Mutism and abnormal EEG tracings. J Child Neurol. 2011;26:1377-1382.
17. Wheless JW, Simos PG, Butler IJ. Language dysfunction in epileptic conditions. Semin Pediatr Neurol. 2002;9:218-228. 18. Lesca G, Rudolf G, Labalme A, et al. Epileptic encephalopathies of the Landau-Kleffner and continuous spike and waves during slow-wave sleep types: genomic dissection makes the link with autism. Epilepsia. 2012;53:1526-1538.
Downloaded from jcn.sagepub.com at Purdue University on June 4, 2015
Defective Auditory Processing in a Child With Temporal Epileptic Focus
Journal of Child Neurology 2015, Vol. 30(4) 513-516 ª The Author(s) 2014 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0883073814532548 jcn.sagepub.com
Avinoam Shuper, MD1, Mordechai Medvedovsky, MD2, and Sara Kivity, MD1
Abstract A 9-year-old boy presented with intolerance to noise that was a trigger for violent temper tantrums that occasionally resembled complex partial seizures. The condition was also a cause for withdrawal from all activities and settings that could potentially be associated with noise. Both electroencephalography and magnetoencephalography clearly demonstrated a left temporal (T5) epileptic focus, although the child never had convulsive seizures. Genetic studies failed to reveal a GRIN2A mutation. We suggest that the hyperacusis in the reported child is another variation of the Landau-Kleffner spectrum. Keywords hyperacusis, temper tantrums, Landau-Kleffner, temporal epileptic focus Received March 23, 2014. Accepted for publication March 28, 2014.
The epilepsy-aphasia spectrum ranges from Landau-Kleffner syndrome and epileptic encephalopathy with continuous spike and wave during sleep in the most severe form to benign childhood epilepsy with centrotemporal spikes in the milder form.1 Language skills are commonly affected in these disorders. Landau-Kleffner syndrome in children is characterized by acquired aphasia and verbal auditory agnosia, with or without seizures, and with the appearance of predominantly temporal spikes or other epileptic activity in the electroencephalogram (EEG). Onset is usually between 3 and 10 years of age. The acquired aphasia in Landau-Kleffner syndrome is considered to be secondary to the epileptic activity that involves the cortical language network. The epileptic discharges are assumed to form the basis of language decline.2 Focal epileptiform activity, mainly temporal, can also be associated with speech, language, and cognitive dysfunction.3 GRIN2A mutations have been found in about 20% of cases of acquired epileptic aphasia, and related childhood focal epilepsies and encephalopathies were identified in cases of speech and language dysfunction. Those mutations were found to be significant in idiopathic focal epilepsy with rolandic spikes.4 This report describes a child who presented with behavioral disturbances associated with intolerance to noise and who exhibited a prominent left temporal epileptic focus. Informed consent to publish this report was obtained from the mother of this child.
Case Report A 9-year-old child from Russia presented to our neurology clinic because of severe behavioral disturbances. The major
complaint was severe and violent temper tantrums during which he hit and kicked everyone who was present. It took several hours to calm him down. He was born after a normal and uneventful pregnancy and delivery. He began having frequent attacks of vomiting at 7 months of age, for which he underwent a medical workup in Russia and was treated with various diets for suspected food intolerance. At around the age of 3 years, he exhibited difficulties in speech, which were treated with some success by an animal-derived cerebral cortical polypeptide (Cortexin, Geropharm, Russia). The brain magnetic resonance imaging (MRI) scan he had undergone in Russia was normal. The child had never had a true seizure. His mother reported that he had fine motor difficulties that eventually resolved. His speech development was slow: his vocabulary included only a few words at the age of 3 years, for which he was treated by a speech-language pathologist. He has always had difficulties in socializing with others and in adapting to any structured educational facility. His parents are university graduates. They
1
Department of Pediatric Neurology and Epilepsy Center, Schneider Children’s Medical Center of Israel, Petah Tiqva, Israel, affiliated to the Sackler Faculty of Medicine, Tel Aviv University, Tel Aviv, Israel 2 Gonda Brain Research Center, Bar Ilan University, Israel Corresponding Author: Avinoam Shuper, MD, Department of Pediatric Neurology and Epilepsy Center, Schneider Children’s Medical Center of Israel, Petah Tiqva 49202, Israel. Email: [email protected]
Downloaded from jcn.sagepub.com at Purdue University on June 4, 2015
514
Journal of Child Neurology 30(4)
Figure 1. Sleep electroencephalographic (EEG) recording showing left temporal (T5) epileptic focus.
Figure 2. Magnetoelectroencephalographic pattern showing a very large and prominent left midtemporal seizure activity.
are divorced and the child lives in Israel with his mother. There is no family history of seizures. The results of our physical and neurologic examination of the child were normal. Repeated challenging with various food products ruled out abnormal food reaction, and metabolic disorders were excluded by studies of blood chemistry and gases, measurements of the levels of ammonia, plasma amino acids, urine organic acids, carnitine and acylcarnitine, as well as by thyroid and adrenal function tests. The result of the chromosomal microarray analysis was normal, and testing for the GRIN2A mutation was negative (Dr Gaetan Lesca, France). A psychological examination revealed a very large vocabulary for his age, but his rates of performing tasks and thinking were very slow. He seemed to be depressive. His cognitive function was average, with higher function scored for verbal abilities. The possibility of autistic features was raised. The most prominent problem in his current behavior was hypersensitivity to
noise. Noises could make him lose control and violently attack those around him, after which it could take up to several hours to calm him down. This reaction severely limited his ability to be present in social, educational, and recreational settings. His initial EEG from Russia had revealed potential epileptic activity. The wakeful EEG performed in our clinic was normal, but a sleep recording clearly demonstrated a left temporal epileptic focus (Figure 1). He was started on valproic acid in a dose of 15 mg/kg alone and then in combination with risperidone 0.5 mg/d. Improvement was marked with this treatment such that he was able to visit Russia for several months, after which he returned to Israel and could attend a local school. One attack was witnessed in our clinic: the sudden ringing of a telephone led to an immediate change in mood and facial expression. He complained of headache, after which he demonstrated hyperexcitability, severe restlessness, and violent behavior, which gradually lessened over several minutes. He was referred to another EEG during which the ringing of a telephone was used in an attempt to trigger a seizure, but no seizure discharges were obtained by this maneuver. He then underwent magnetoencephalography. The recording was conducted by using a whole head system (Magnes 3600 WH) equipped with 248 magnetometers and 23 reference channels that record magnetic field changes distant from the head (environmental noise). Data recorded from these channels were used for further noise reduction during magnetoencephalography measurements. In addition, the data were cleaned online using a 1 to 200 Hz bandpass filter. The sampling rate was 678 Hz. The magnetoencephalography was recorded during both wakefulness and drowsiness in the evening close to the child’s usual bedtime. Epileptic activity in the form of frequent spike and wave complexes was recorded. The sources of this activity were localized in the left perisylvian area, that is, temporal, frontal and parietal opercula and insula (Figure 2). Exposure to loud noise led to immediate headache but did not affect the magnetoencephalography trace. At this stage, the valproic acid regime was changed to the sulthiame (Ospolot®, Desitin Arzneimittel GmbH) 200 mg/d. There was some improvement in behavior, but he still complained of headaches and was severely incapacitated by sudden and loud noises. There seem to be slow but persistent mental deterioration. The prominent temporal activity led to a presumptive diagnosis of the hyperacusis as resulting from inappropriate central processing of noise, a disturbance reported to be present in children with Landau-Kleffner syndrome.5
Discussion We describe a child with markedly exaggerated response to noise (hyperacusis) that could lead to loss of self-control and to violent behavior. The administration of valproic acid together with risperidone resulted in significant clinical improvement. A left temporal epileptic focus was found on a wakeful EEG. The differential diagnosis of this child is very interesting. He has hyperacusis, in which everyday sounds are perceived
Downloaded from jcn.sagepub.com at Purdue University on June 4, 2015
Shuper et al
515
as being unbearable, strong, or painful and which can by itself be associated with psychological disturbances. Hyperacusis is described in Williams syndrome, and sensory overresponsiveness and psychopathology were described in familial impairments, but our patient did not exhibit other key characteristics of those conditions.6 Another potential diagnosis was reflex epilepsy, in which noise7 or telephone ringing8 can trigger seizures, but repeated attempts to elicit a convulsive seizure by both sound sources failed to achieve any changes in his EEG recordings. The findings on his magnetoencephalography led us to consider the potential diagnosis of acquired epileptiform opercular syndrome, but our patient never had overt convulsive seizures or oral motor dysfunction.9 There is a diagnostic possibility of ictal vomiting, taking into consideration his past history of recurrent vomiting episodes together with the inability to exclude that they had been a true seizure manifestation.10,11 However, vomiting was no longer a predominant feature of his behavior when he was evaluated in our neurology clinic. After ruling out those alternatives, we concluded that the most appropriate diagnosis was an epilepsy–aphasia spectrum disorder12,13 leading to abnormal central auditory processing manifesting clinically as hyperacusis. The magnetoencephalography pattern supports this connection.14 A defective auditory processing is a well-recognized feature of Landau-Kleffner syndrome.15 Selassie et al3 reported dysfunction of auditory perception in noise in more than half of their study participants who had focal epileptiform activity. It is possible that the presence of temporal epileptic focus may be related to a large spectrum of auditory- or languageassociated disorders. We had earlier noted a relation between selective mutism and temporal foci.16 There is an increasing amount of data to support the notion that language dysfunction can be related to a spectrum of disorders which encompass the involvement of the temporal lobe(s) as a source of abnormal EEGs17 and which are probably part of an expanding ‘‘spectrum’’ of Landau-Kleffner syndrome. Selassie et al3 concluded that focal epileptiform activity can be associated not only by language dysfunction but also by auditory dysfunction, oralmotor dysfunction, and stuttering. In addition to variations on EEGs, the clinical manifestations may include autism, attention deficit hyperactivity disorder, learning disability, mental retardation and others, and the affected children do not necessarily seize. GRIN2A mutations are found in a part but not in most of these children.4 Lesca et al18 showed an overrepresentation of cell adhesion genes in Landau-Kleffner syndrome and autistic spectrum disorders, and suggested that there is a potential mechanism to explain the clinical link between the two. We suggest that the hyperacusis in the reported child represents an abnormality in the central processing of noise, and that abnormal central processing of noise may be considered a heretofore undescribed part of the Landau-Kleffner syndrome spectrum. Declaration of Conflicting Interests The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding The authors received no financial support for the research, authorship, and/or publication of this article.
Ethical Approval Being a case report, the need for the Hospital Helsinki Board was waived. The publication of the manuscript was fully approved by the child’s mother who also read the manuscript.
References 1. Deonna T, Rouket-Perez E. Early-onset acquired epileptic aphasia (Landau-Kleffner syndrome, LKS) and regressive autistic disorders with epileptic EEG abnormalities: the continuing debate. Brain Dev. 2010;32:746-752. 2. Datta AN, Oser N, Ramelli GP, et al. BECTS evolving to Landau-Kleffner syndrome and back by subsequent recovery: a longitudinal language reorganization case study using fMRI, source EEG and psychological testing. Epilepsy Behav. 2013; 27:107-114. 3. Selassie GR-H, Hedstrom A, Viggedal G, et al. Speech, language and cognitive dysfunction in children with focal epileptiform activity: a follow-up study. Epilepsy Behav. 2010;18: 267-275. 4. Lesca G, Rudolf G, Bruneau N, et al. GRIN2A mutations in acquired epileptic aphasia and related childhood focal epilepsies and encephalopathies with speech and language dysfunction. Nat Genet. 2013;45:1061-1066. 5. Fandino M, Connoly M, Usher L, Palm S, Kozak FK. LandauKleffner syndrome: a rare auditory processing disorder. Series of cases and review of the literature. Int J Pediatr Otorhinolaryngol. 2011;75:33-38. 6. Zarchi O, Attias J, Gothelf D. Auditory and visual processing in Williams syndrome. Isr J Psychiatry Relat Sci. 2010;47: 125-131. 7. Ferlazzo E, Zifkin BG, Andermann E, Andermann F. Cortical triggers in generalized reflex seizures and epilepsies. Brain. 2005;128:700-710. 8. Michelucci R, Mecarelli O, Bovo G, et al. A de-novo LGI1 mutation causing idiopathic partial epilepsy with telephone-induced seizures. Neurology. 2007;68:2150-2151. 9. Shafrir Y, Prensky AL. Acquired epileptiform opercular syndrome: a second case report, review of the literature and comparison to the Landau-Kleffner syndrome. Epilepsia. 1995;36: 1050-1057. 10. Schindler K, Wieser HG. Ictal vomiting in a left hemisphere language dominant patient with left-sided temporal lobe epilepsy. Epilepsy Behav. 2006;8:323-327. 11. Shuper A, Goldberg-Stern H. Ictus emeticus (ictal vomiting). Pediatr Neurol. 2004;31:283-286. 12. Tsai M-H, Vears DF, Turner SJ, et al. Clinical genetic study of the epilepsy-aphasia spectrum. Epilepsia. 2013;54:280-287. 13. Carvill GM, Regan B, Yendle SC, et al. GRIN2A mutations cause epilepsy-aphasia spectrum disorders. Nat Genet. 2013; 45:1073-1076. 14. Lewine JD, Andrews R, Chez M, et al. Magnetoencephalographic patterns of epileptiform activity in children with
Downloaded from jcn.sagepub.com at Purdue University on June 4, 2015
516
Journal of Child Neurology 30(4)
regressive autism spectrum disorders. Pediatrics. 1999;104: 405-418. 15. Rapin I, Mattis S, Rowan AJ, Golden GG. Verbal auditory agnosia in children. Dev Med Child Neurol. 1977;19:192-207. 16. Politi K, Kivity S, Goldberg-Stern H, et al. Mutism and abnormal EEG tracings. J Child Neurol. 2011;26:1377-1382.
17. Wheless JW, Simos PG, Butler IJ. Language dysfunction in epileptic conditions. Semin Pediatr Neurol. 2002;9:218-228. 18. Lesca G, Rudolf G, Labalme A, et al. Epileptic encephalopathies of the Landau-Kleffner and continuous spike and waves during slow-wave sleep types: genomic dissection makes the link with autism. Epilepsia. 2012;53:1526-1538.
Downloaded from jcn.sagepub.com at Purdue University on June 4, 2015
