- Email: [email protected]
Rolandic epilepsy: a challenge in terminology and classification
European Journal of Paediatric Neurology (2003) 7, 239–241
www.elsevier.com/locate/ejpn
ANNOTATION
Rolandic epilepsy: a challenge in terminology and classification Staffan Lundberg*, Orvar Eeg-Olofsson Department of Women’s and Children’s Health, Uppsala University, Uppsala, Sweden Received 2 June 2003; accepted 3 June 2003
KEYWORDS Epilepsy; Childhood; Rolandic; Terminology; Classification
Summary History and present definition of rolandic epilepsy (RE) is briefly presented. In the literature there has often been misconceptions in the description of the syndrome, and the affinity to related conditions and structural abnormalities with rolandic discharges is often unclear. This has resulted in confusion regarding the definition and delineation of RE. A spectrum of RE based on a maturational continuum is possible. Until more is known about the genetic background of RE, a simple classification is proposed: 1) RE ‘pure’ according to the original definition; 2) RE ‘plus’; 3) RE-related disorders; 4) Structural brain lesions with signs and symptoms as in RE. A summary of results from neuroimaging, neuropsychological and oromotor studies in RE ‘pure’ is presented. Accurate clinical assessment and EEG analysis is essential for a proper classification of RE. Q 2003 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
Rolandic epilepsy (RE) constitutes about 15% of all childhood epilepsies. The syndrome was not described and defined until in the 1950s. The EEG features were first reported by Y Gastaut in 1952, who called the discharges ‘prerolandique’,1 and Gibbs and Gibbs in the same year entitled them ‘mid-temporal’.2 The first accurate description of the electro-clinical syndrome was presented in 1958 by Nayrac and Beaussart,3 and this was followed by several other reports in the 1960s and 1970s. The name proposed by the Commission on Classification and Terminology of the International *Corresponding author. Tel.: þ 46-18-6119227; fax: þ46-186115853. E-mail address: [email protected]
League Against Epilepsy 1989, is ‘benign childhood epilepsy with centrotemporal spikes’ according to clinical and electroencephalographic features.4 The diagnosis is based on characteristic seizure manifestations, which are focal but may be secondarily generalized, rolandic seizures (RS), and typical EEG with sharp waves located in the centro-temporal (centro-parietal, fronto-central, centro-occipital) leads, rolandic discharges (RD). The syndrome occurs in mentally and neurologically normal children aged 3 –13 years.4 Thus, neither the clinical picture nor the EEG alone is enough to make the diagnosis. The prefix ‘benign’ is included in most synonyms of RE due to the excellent prognosis regarding the seizures, which always together with the EEG manifestations resolve before or at
1090-3798/03/$ - see front matter Q 2003 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/S1090-3798(03)00079-5
240
puberty. However, several studies during the last decade have shown previous overlooked cognitive deficits in these children, why the favorable prognosis has been challenged. Over the years, RE has unfortunately been diagnosed in children with RD without RS but with other paroxysmal manifestations, e.g. syncope, breath holding spells and vertigo, and in children with obvious behavioural disturbances. The RE diagnosis has also been put in children with RD and other seizure manifestations such as myoclonias, atonic seizures and absences, in addition to RS. It has also been reported in children with mental and motor deficits, in children less than 3 years, in children with outbreak of frequent seizures over a short period of time or focal status epilepticus, and in children with cerebral structural lesions including malformations.5 It can also appear very clear-cut initially and then move into other syndromes as atypical benign partial epilepsy (ABPE) or pseudoLennox syndrome (PLS), epilepsy with continuous spike-wave during slow sleep (CSWS), and LandauKleffner syndrome (LKS).6 Thus, the RE phenotype can appear in many different conditions. All what have been mentioned leads to confusion regarding the definition and delineation of the RE syndrome.6 Even the denomination ‘malignant rolandic-sylvian epilepsy’ has been used.7 The question is if there is a spectrum of RE pointing to a maturational continuum of disorders with different manifestations.8 It can also be argued that we deal with a spectrum of both idiopathic and symptomatic epilepsies with RD, i.e. different epileptic syndromes and epilepsies with structural abnormalities, with a common EEG pattern. These alternatives wipe out the ‘original RE’ as one entity. Until we know more about the genetics of the mentioned syndromes (up to now only the genetics of RD has been reported9), and different structural brain abnormalities with RD as a common EEG pattern, a simple classification to clean the conceptions could be proposed. 1. RE ‘pure’ according to the original definition. 2. RE ‘plus’ including entities as benign partial epilepsy with affective symptoms10 and autosomal dominant rolandic epilepsy with speech dyspraxia.11 Also RE with some abnormal EEG patterns can be included here.12 3. RE-related disorders as ABPE/PLS, epilepsy with CSWS and LKS.6 4. Structural brain lesions with signs and symptoms as in RE. RE ‘pure’ has been studied from neuroimaging, neuropsychological and oromotor point of view by
S. Lundberg, O. Eeg-Olofsson
our group. A summary of the neuroimaging results show subcortical high signal intensities on T2 weighted images in the temporal and frontal lobes bilaterally in 28%, an asymmetry of the hippocampal size in 28%,13 and a neuronal metabolic imbalance in the hippocampal region measured by proton magnetic resonance spectroscopy.14 The RE children show deficits regarding auditory-verbal and executive tasks.15 Preliminary studies reveal oromotor difficulties and poor performance on dichotic listening test. Our results implies that other cerebral structures or neuronal pathways than merely the rolandic cortex, probably are involved in the pathophysiology of the syndrome. It has to be emphasized that accurate clinical assessments and EEG analyses, are essential for the definition of RE. This is also an absolute condition for further genetic studies in order to acquire more knowledge about RE and related conditions. If this is not achieved, the bewilderment concerning idiopathic partial epilepsies will remain. Prospective and longitudinal studies of children with typical RS with and without RD, and groups of children with typical RD and atypical seizures will hopefully collect more necessary information.
References 1. Gastaut Y. Un e ´le ´ment de ´routant de la se ´me ´iologie e ´lectroence ´phalographique: les points prerolandiques sans signification focale. Rev Neurol 1952;87:488—99. 2. Gibbs FA, Gibbs EL. Atlas of electroencephalography. Epilepsy. Reading, MA: Addison-Wesley; 1952. p. 214—90. 3. Nayrac P, Beaussart M. Les pointe-ondes pre ´rolandiques: Expression EEG tre `s particulie `re: Etude e ´lectroclinique de 21 cas. Rev Neurol 1958;99:201—6. 4. Proposal for revised classification of epilepsies and epileptic syndromes, Commission on classification and terminology of the International League against epilepsy. Epilepsia 1989; 30:389—99. 5. Gelisse P, Corda D, Raybaud C, et al. Abnormal neuroimaging in patients with benign epilepsy with centrotemporal spikes. Epilepsia 2003;44:372—8. 6. Stephani U. Spectrum of rolandic epilepsy. Agreements, disagreements and open questions. Proceedings of an International Workshop, September 10, 1999, Kiel, Germany. Epileptic Disord John Libbey Eurotext; 2000. 7. Otsubo H, Chitoku S, Ochi A, et al. Malignant rolandic-sylvian epilepsy in children: diagnosis, treatment, and outcomes. Neurology 2001;57:590—6. 8. Doose H, Baier WK. Benign partial epilepsy and related conditions: multifactorial pathogenesis with hereditary impairment of brain maturation. Eur J Pediatr 1989;149: 152—8. 9. Neubauer BA, Fiedler B, Himmelein B, et al. Centrotemporal spikes in families with rolandic epilepsy: linkage to chromosome 15q14. Neurology 1998;51:1608—12. 10. Dalla Bernardina B. Benign partial epilepsy with affective symptoms (benign psychomotor epilepsy). In: Roger J,
Rolandic epilepsy: a challenge in terminology and classification
editor. Epileptic syndromes in infancy, childhood and adolescence. London: John Libbey; 1992. p. 219—24. 11. Scheffer IE, Jones L, Pozzebon M, et al. Autosomal dominant rolandic epilepsy and speech dyspraxia: a new syndrome with anticipation. Ann Neurol 1995;38:633—42. 12. Massa R, de Saint-Martin A, Carcangiu R, et al. EEG criteria predictive of complicated evolution in idiopathic rolandic epilepsy. Neurology 2001;57:1071—9. 13. Lundberg S, Eeg-Olofsson O, Raininko R, Eeg-Olofsson KE. Hippocampal asymmetries and white matter abnormalities
241
on MRI in benign childhood epilepsy with centrotemporal spikes. Epilepsia 1999;40:1808—15. 14. Lundberg S, Weis J, Eeg-Olofsson O, Raininko R. Hippocampal region asymmetry assessed by 1H-MRS in rolandic epilepsy. Epilepsia 2003;44:205—10. 15. Croona C, Kihlgren M, Lundberg S, Eeg-Olofsson O, EegOlofsson KE. Neuropsychological findings in children with benign childhood epilepsy with centrotemporal spikes. Dev Med Child Neurol 1999;41:813—8.
www.elsevier.com/locate/ejpn
ANNOTATION
Rolandic epilepsy: a challenge in terminology and classification Staffan Lundberg*, Orvar Eeg-Olofsson Department of Women’s and Children’s Health, Uppsala University, Uppsala, Sweden Received 2 June 2003; accepted 3 June 2003
KEYWORDS Epilepsy; Childhood; Rolandic; Terminology; Classification
Summary History and present definition of rolandic epilepsy (RE) is briefly presented. In the literature there has often been misconceptions in the description of the syndrome, and the affinity to related conditions and structural abnormalities with rolandic discharges is often unclear. This has resulted in confusion regarding the definition and delineation of RE. A spectrum of RE based on a maturational continuum is possible. Until more is known about the genetic background of RE, a simple classification is proposed: 1) RE ‘pure’ according to the original definition; 2) RE ‘plus’; 3) RE-related disorders; 4) Structural brain lesions with signs and symptoms as in RE. A summary of results from neuroimaging, neuropsychological and oromotor studies in RE ‘pure’ is presented. Accurate clinical assessment and EEG analysis is essential for a proper classification of RE. Q 2003 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved.
Rolandic epilepsy (RE) constitutes about 15% of all childhood epilepsies. The syndrome was not described and defined until in the 1950s. The EEG features were first reported by Y Gastaut in 1952, who called the discharges ‘prerolandique’,1 and Gibbs and Gibbs in the same year entitled them ‘mid-temporal’.2 The first accurate description of the electro-clinical syndrome was presented in 1958 by Nayrac and Beaussart,3 and this was followed by several other reports in the 1960s and 1970s. The name proposed by the Commission on Classification and Terminology of the International *Corresponding author. Tel.: þ 46-18-6119227; fax: þ46-186115853. E-mail address: [email protected]
League Against Epilepsy 1989, is ‘benign childhood epilepsy with centrotemporal spikes’ according to clinical and electroencephalographic features.4 The diagnosis is based on characteristic seizure manifestations, which are focal but may be secondarily generalized, rolandic seizures (RS), and typical EEG with sharp waves located in the centro-temporal (centro-parietal, fronto-central, centro-occipital) leads, rolandic discharges (RD). The syndrome occurs in mentally and neurologically normal children aged 3 –13 years.4 Thus, neither the clinical picture nor the EEG alone is enough to make the diagnosis. The prefix ‘benign’ is included in most synonyms of RE due to the excellent prognosis regarding the seizures, which always together with the EEG manifestations resolve before or at
1090-3798/03/$ - see front matter Q 2003 European Paediatric Neurology Society. Published by Elsevier Ltd. All rights reserved. doi:10.1016/S1090-3798(03)00079-5
240
puberty. However, several studies during the last decade have shown previous overlooked cognitive deficits in these children, why the favorable prognosis has been challenged. Over the years, RE has unfortunately been diagnosed in children with RD without RS but with other paroxysmal manifestations, e.g. syncope, breath holding spells and vertigo, and in children with obvious behavioural disturbances. The RE diagnosis has also been put in children with RD and other seizure manifestations such as myoclonias, atonic seizures and absences, in addition to RS. It has also been reported in children with mental and motor deficits, in children less than 3 years, in children with outbreak of frequent seizures over a short period of time or focal status epilepticus, and in children with cerebral structural lesions including malformations.5 It can also appear very clear-cut initially and then move into other syndromes as atypical benign partial epilepsy (ABPE) or pseudoLennox syndrome (PLS), epilepsy with continuous spike-wave during slow sleep (CSWS), and LandauKleffner syndrome (LKS).6 Thus, the RE phenotype can appear in many different conditions. All what have been mentioned leads to confusion regarding the definition and delineation of the RE syndrome.6 Even the denomination ‘malignant rolandic-sylvian epilepsy’ has been used.7 The question is if there is a spectrum of RE pointing to a maturational continuum of disorders with different manifestations.8 It can also be argued that we deal with a spectrum of both idiopathic and symptomatic epilepsies with RD, i.e. different epileptic syndromes and epilepsies with structural abnormalities, with a common EEG pattern. These alternatives wipe out the ‘original RE’ as one entity. Until we know more about the genetics of the mentioned syndromes (up to now only the genetics of RD has been reported9), and different structural brain abnormalities with RD as a common EEG pattern, a simple classification to clean the conceptions could be proposed. 1. RE ‘pure’ according to the original definition. 2. RE ‘plus’ including entities as benign partial epilepsy with affective symptoms10 and autosomal dominant rolandic epilepsy with speech dyspraxia.11 Also RE with some abnormal EEG patterns can be included here.12 3. RE-related disorders as ABPE/PLS, epilepsy with CSWS and LKS.6 4. Structural brain lesions with signs and symptoms as in RE. RE ‘pure’ has been studied from neuroimaging, neuropsychological and oromotor point of view by
S. Lundberg, O. Eeg-Olofsson
our group. A summary of the neuroimaging results show subcortical high signal intensities on T2 weighted images in the temporal and frontal lobes bilaterally in 28%, an asymmetry of the hippocampal size in 28%,13 and a neuronal metabolic imbalance in the hippocampal region measured by proton magnetic resonance spectroscopy.14 The RE children show deficits regarding auditory-verbal and executive tasks.15 Preliminary studies reveal oromotor difficulties and poor performance on dichotic listening test. Our results implies that other cerebral structures or neuronal pathways than merely the rolandic cortex, probably are involved in the pathophysiology of the syndrome. It has to be emphasized that accurate clinical assessments and EEG analyses, are essential for the definition of RE. This is also an absolute condition for further genetic studies in order to acquire more knowledge about RE and related conditions. If this is not achieved, the bewilderment concerning idiopathic partial epilepsies will remain. Prospective and longitudinal studies of children with typical RS with and without RD, and groups of children with typical RD and atypical seizures will hopefully collect more necessary information.
References 1. Gastaut Y. Un e ´le ´ment de ´routant de la se ´me ´iologie e ´lectroence ´phalographique: les points prerolandiques sans signification focale. Rev Neurol 1952;87:488—99. 2. Gibbs FA, Gibbs EL. Atlas of electroencephalography. Epilepsy. Reading, MA: Addison-Wesley; 1952. p. 214—90. 3. Nayrac P, Beaussart M. Les pointe-ondes pre ´rolandiques: Expression EEG tre `s particulie `re: Etude e ´lectroclinique de 21 cas. Rev Neurol 1958;99:201—6. 4. Proposal for revised classification of epilepsies and epileptic syndromes, Commission on classification and terminology of the International League against epilepsy. Epilepsia 1989; 30:389—99. 5. Gelisse P, Corda D, Raybaud C, et al. Abnormal neuroimaging in patients with benign epilepsy with centrotemporal spikes. Epilepsia 2003;44:372—8. 6. Stephani U. Spectrum of rolandic epilepsy. Agreements, disagreements and open questions. Proceedings of an International Workshop, September 10, 1999, Kiel, Germany. Epileptic Disord John Libbey Eurotext; 2000. 7. Otsubo H, Chitoku S, Ochi A, et al. Malignant rolandic-sylvian epilepsy in children: diagnosis, treatment, and outcomes. Neurology 2001;57:590—6. 8. Doose H, Baier WK. Benign partial epilepsy and related conditions: multifactorial pathogenesis with hereditary impairment of brain maturation. Eur J Pediatr 1989;149: 152—8. 9. Neubauer BA, Fiedler B, Himmelein B, et al. Centrotemporal spikes in families with rolandic epilepsy: linkage to chromosome 15q14. Neurology 1998;51:1608—12. 10. Dalla Bernardina B. Benign partial epilepsy with affective symptoms (benign psychomotor epilepsy). In: Roger J,
Rolandic epilepsy: a challenge in terminology and classification
editor. Epileptic syndromes in infancy, childhood and adolescence. London: John Libbey; 1992. p. 219—24. 11. Scheffer IE, Jones L, Pozzebon M, et al. Autosomal dominant rolandic epilepsy and speech dyspraxia: a new syndrome with anticipation. Ann Neurol 1995;38:633—42. 12. Massa R, de Saint-Martin A, Carcangiu R, et al. EEG criteria predictive of complicated evolution in idiopathic rolandic epilepsy. Neurology 2001;57:1071—9. 13. Lundberg S, Eeg-Olofsson O, Raininko R, Eeg-Olofsson KE. Hippocampal asymmetries and white matter abnormalities
241
on MRI in benign childhood epilepsy with centrotemporal spikes. Epilepsia 1999;40:1808—15. 14. Lundberg S, Weis J, Eeg-Olofsson O, Raininko R. Hippocampal region asymmetry assessed by 1H-MRS in rolandic epilepsy. Epilepsia 2003;44:205—10. 15. Croona C, Kihlgren M, Lundberg S, Eeg-Olofsson O, EegOlofsson KE. Neuropsychological findings in children with benign childhood epilepsy with centrotemporal spikes. Dev Med Child Neurol 1999;41:813—8.