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Neurogenic Language Disorders in Children

Related Books Title: The Sciences of Aphasia: From Therapy to Theory Edited by: Was Papathanaslou & Ria De Bleser (eds) ISBN: 0080440738 Title: Speech-Language Pathology Author: Carl R. Schneiderman & Robert E. Potter ISBN: 0126278741 Title: Manifestations of Aphasia Symptoms in Different Languages Author: Michel Paradis (ed) ISBN: 0080436625 Title: Foundations of Stuttering Author: Marcel E. Wingate ISBN: 0127594515 Title: Clinical Phonetics & Phonology: Making Sense of Disordered Speech Author: Sara Howard & Barry Heselwood ISBN: 0123569184 Title: Concise Encyclopedia of Language Pathology Author: Franco Fabbro (ed) ISBN: 0080431518 Related Journals Journal of Fluency Disorders Editor: Richard Curlee Journal of Communication Disorders Editor: Theodore Glattke Journal of Neurolinguistics Editors: John Marshall & Michel Paradis Brain & Language Editor: Harry A. Whitaker

For further information on these titles, visit www.elsevier.com For free abstracts and sample copies of our journals, visit www.ScienceDirect.com

Neurogenic Language Disorders in Children EDITED BY

Franco Fabbro "E. Medea"Scientific Institute, University of I]dine

INTERNATIONAL ASSOCIATION OF LOGOPEDICS AND PHONIATRICS

2004

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© 2004 Elsevier Ltd. All rights reserved. This work is protected under copyright by Elsevier Ltd., and the following terms and conditions apply to its use: Photocopying Single photocopies of single chapters may be made for personal use as allowed by national copyright laws. Permission of the Publisher and payment of a fee is required for all other photocopying, including multiple or systematic copying, copying for advertising or promotional purposes, resale, and all forms of document delivery. Special rates are available for educational institutions that wish to make photocopies for non-profit educational classroom use. Permissions may be sought directly from Elsevier's Rights Department in Oxford, UK: phone (+44) 1865 843830, fax (+44) 1865 853333, e-mail: [email protected]. Requests may also be completed on-line via the Elsevier homepage (http://www.elsevier.com/locate/permissions). In the USA, users may clear permissions and make payments through the Copyright Clearance Center, Inc., 222 Rosewood Drive, Danvers, MA 01923, USA; phone: (+1) (978) 7508400, fax: (+1) (978) 7504744, and in the UK through the Copyright Licensing Agency Rapid Clearance Service (CLARCS), 90 Tottenham Court Road, London W1P 0LP, UK; phone: (+44) 20 7631 5555; fax: (+44) 20 7631 5500. Other countries may have a local reprographic rights agency for payments. Derivative Works Tables of contents may be reproduced for internal circulation, but permission of the Publisher is required for external resale or distribution of such material. Permission of the Publisher is required for all other derivative works, including compilations and translations. Electronic Storage or Usage Permission of the Publisher is required to store or use electronically any material contained in this work, including any chapter or part of a chapter. Except as outlined above, no part of this work may be reproduced, stored in a retrieval system or transmitted in any form or by any means, electronic, mechanical, photocopying, recording or otherwise, without prior written permission of the Publisher. Address permissions requests to: Elsevier's Rights Department, at the fax and e-mail addresses noted above. Notice No responsibility is assumed by the Publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. Because of rapid advances in the medical sciences, in particular, independent verification of diagnoses and drug dosages should be made.

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@ The paper used in this publication meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper). Printed in The Netherlands.

V

ACKNOWLEDGEMENTS This book collects the papers presented at the International Symposium of the IALP Aphasia Committee on Neurogenic Language Disorders in Children, held in Cividale del Friuli (Udine, Italy), on 9-10 May 2003. The Symposium was organized by Scientific Institute "E.Medea" of Association "la Nostra Famiglia", the Faculty of Education of the University of Udine, and IALP. Financial support was granted by Fondazione CRUP. The success of the meeting, in terms of scientific innovation and public participation, was also due to the work of Dr. Alessandro Tavano, Scientific Secretary to the Symposium, in dealing with both scientific and organizational issues. The administrative board and organizational secretariat of IRCCS "E.Medea" of San Vito al Tagliamento (Pordenone. Italy) and Pasian di Prato (Udine, Italy) provided invaluable assistance and deserve the utmost gratitude. Editorial assistance to this volume was provided by Dr. Alessandro Tavano and Dr. Barbara Alberti.

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vii

Contents 1

Neurogenic Language Disorders in Children: An Introduction. Franco Fabbro

1-7

2

Pathophysiological Basis of Aphasia and Verbal Outome in LandauKleffner Syndrome. Marie-Noelle Metz-Lutz and Steve Majerus

9-23

3

Acquired Language Disorders and Epilepsy: From Landau -Kleffner Syndrome to Autistic Regression. Roberto Tuchman

25-35

4

Persistent Subtle Language and Learning Deficits in a Child with Acquired Epileptiform Opercular Syndrome. Paola Cipriani, Anna M. Chilosi, Claudia Casalini, Lucia Pfanner, Annarita Ferrari, Daniela Brizzolara and Renzo Guerrini

37-48

5

Cerebral Language Lateralization and Early Linguistic In Children With Focal Brain Lesions. Anna M. Chilosi, Chiara Pecini, Paola Cipriani, Daniela Brizzolara, Paola Brovedani, Giovanni Ferretti, Lucia Pfanner and Giovanni Cioni

49-63

6

Language Disorders Associated With Paroxysmal Abnormalities During NREM Sleep After Very Early Brain Lesions. Franco Fabbro, Alessandro Tavano, Guido Cristofori and Renato Borgatti

65-85

7

Language and Phonological Awareness Abilities of Children treated for Posterior Fossa Tumor. Bruce E. Murdoch, Kimberley M. Docking, and Elizabeth C. Ward

87-126

8

Language Development in Children with Cerebellar Malformations. Renato Borgatti, Alessandro Tavano, Guido Cristofori and Franco Fabbro

127-145

viii 9

Contents Crossed Aphasia in Children. Peter Marien, Philippe Paquier, Sebastiaan Engelborghs and Peter P. De Deyn

147-180

10

Recognizable Spontaneous Language Characteristics in a Young Adult Twelve Years After She Became Aphasic as a Child. Philippe F. Paquier, Valerie R. van Maldeghem, Hugo R. van Dongen and Wouter L. Creten

181 -197

11

Recovery From Aphasia After Polytrauma in a Czech Child: What Is Lost and What Is Left. Helena Leheckovd

199-229

12

Persistent Acquired Childhood Aphasia. Isabel Pavao Martins

231-251

Introduction

1

1

NEUROGENIC LANGUAGE DISORDERS IN CHILDREN: AN INTRODUCTION Franco Fabbro "E. Medea" Scientific Institute, Polo del Friuli Venezia Giulia, Italy University ofUdine, Italy

INTRODUCTION Language disorders in children are one of the most frequent causes of difficulties in communication, social interaction, learning and academic achievement. It has been estimated that over 5% of children present with some kind of language disorders (Fabbro, 1999). Language disorders in children are distinguished into: 1) acquired language disorders; 2) language disorders due to pre-perinatal lesions; 3) developmental language disorders; 4) language disorders in genetic syndromes with mental retardation (Fabbro, 2000a).

ACQUIRED LANGUAGE DISORDERS IN CHILDREN Acquired language disorders in children can be distinguished into three main groups: acquired childhood aphasia, language disorders following posterior cranial fossa lesions (PCF) and acquired epileptiform aphasias. Acquired childhood aphasia Acquired childhood aphasia refers to language deficits following brain lesions after the age of acquisition of the first sentences, generally after the age of 2. The most common etiological causes include vascular lesions, trauma, tumors and infections involving the language dominant hemisphere {see Marien et al., this volume, for a review of the cases of "crossed

2

Neurogenic Language Disorders in Children

aphasia in children" or acquired childhood aphasia after right hemisphere lesions in righthanded children). Before the late 1970s it was believed that aphasia in children was characterized by "negative symptoms" such as mutism, dysarthria, reduction in sentence length and telegraphic speech. More recently, neurolinguistic tests, including systematic analyses of spontaneous and descriptive speech, and comprehensive language batteries have allowed researchers to evaluate the different aspects of language (for example, auditory, semantic and syntactic comprehension; syllable, word and sentence repetition; naming and sentence production). In children with acquired aphasia, these methods highlight positive symptoms such as logorrhea, paraphasia, perseverations and neologisms (see Leheckovd, Paquier et al., this volume). Moreover, these symptoms correlate with clinical aphasic profiles and lesion localizations similar to those of adults. Indeed, at least in their acute phase and lesional phase aphasic syndromes in children have been found similar to most of the aphasic syndromes in adults (cf. Van Hout, 2000). Recovery of acquired childhood aphasia remains one of the most debated issue still today. Before the early 1970s language recovery in childhood aphasia was believed to be rapid and complete (Lenneberg, 1967). Later studies have shown that, even if language seems to return to normal, non-linguistic abilities (such as working memory) are affected too. Therefore, irrespective of age and lesion etiology, children encounter educational difficulties. These findings stress the need for rehabilitation and educational/professional support in the chronic stages of childhood aphasia (see Pavao Martins, this volume). Language disorders following PCF lesions Almost 50% of brain tumors in children involve the cerebellum (medulloblastomas, cerebellar astrocytomas, ependymomas; cf. Becker and Jay, 1990), a structure localized in the posterior cranial fossa (PCF). In 10% of the children surgical removal of the tumor can cause a syndrome characterized by complete but transient loss of speech (transient cerebellar mutism), followed by dysarthria. This syndrome is frequent in patients aged 2-16 years. There have been reports of patients who became mute within 12 to 48 hours of surgery and the period of mutism lasted from 1.5 to 12 week after onset. Transient cerebellar mutism seems to be due to a diaschisis on the nervous structures of the brain stem which are responsible for verbal expression (cf. Pollak, 1997; Esposito et al., 1999). Recently, the cerebellum was also attributed an important role in the regulation of linguistic, cognitive and affective functions (cf. Fabbro, 2000b). Resection of cerebellar tumors both in childhood and adult age may cause a "Cognitive - Affective Syndrome" (Levisohn et al, 2000; Riva and Giorgi, 2000) characterized by expressive language deficits, verbal memory deficits (mainly after right hemisphere cerebellar lesions), deficits in the visuo-spatial functions (after left hemisphere cerebellar lesions) and deficits in affect regulation (after vermis damage) (see Murdoch et al., this volume). Deficits in the development of linguistic and cognitive functions were also described in patients with malformation lesions localized to the cerebellum (see Borgatti et al., this volume).

Introduction

3

Acquired Epileptiform Aphasias The main clinical syndrome of acquired epileptiform aphasias is acquired aphasia with convulsive disorder. It manifests in children, generally at 3-8 years of age. It was first described by Landau and Kleffner (1957); hence, its definition as Landau-Kleffner syndrome (LKS) (cf. Lebrun and Fabbro, 2002). It affects children with normal psychomotor and linguistic development. Language disruption may occur before or after seizures. At onset, the most frequent symptom is breakdown in language comprehension, whereas hearing and interpretation of non-linguistic sounds remain intact (word deafness). Following the breakdown in comprehension, expressive language and vocabulary decay progressively, too. Unlike other forms of acquired aphasia, in LKS verbal expression may be fluent with many semantic and verbal paraphasias, neologisms and jargon. There may be an almost full recovery after the first episode, even after a short period of time (days or weeks). In other cases, recovery may be very slow (months or years). Relapse is frequent and often the development of aphasia is fluctuating, with several aphasic episodes. The clinical picture stabilizes before the end of adolescence. Language recovery is sometimes very good, at other times it is defective, in which case subjects present with aphasic disorders throughout their lives (see Metz-Lutz and Majerus, this volume). Epileptic manifestations are heterogeneous (partial motor seizures, atypical absence, generalized tonic-clonic seizures) and their frequency is quite variable. Children with LKS often show a rather limited number of seizures which can be treated with anti-epileptic drugs. Seizures may disappear completely before the age of 15. In a review of the first cases described, Mantovani and Landau (1981) reported that, after more than 20 years, none of their patients still had seizures. On waking EEG paroxysmal abnormalities in children with LKS may vary: bilateral temporal or temporoparietal spikes, bilateral 1-3 Hz slow wave activity over the temporal regions, generalized sharp waves or slow wave discharges, and multifocal or unilateral spikes. The background rhythm of the EEG in waking state is normal. Generally, the epileptic focus is never stable, even if statistically it tends to be over the left temporal regions. An extremely significant feature which seems to be common to all children with LKS is an EEG with bilateral (focalized) paroxysmal abnormalities during non-REM sleep which is constantly associated with regression of language functions (cf. Fabbro and Zucca, 2000). Recently, many other clinical syndromes were associated to Landau-Kleffner Syndrome, and they include Acquired Epileptiform Opercular Syndrome (AEOS) (see Cipriani et al., this volume), the Continuous Spike-Waves during Slow Sleep (CSWS), the Benign Childhood Epilepsy with Centrotemporal Spikes (BECTS), and the Autistic Regression with an Epileptiform EEG. All of these clinical syndromes are associated with different degrees of cognitive disorders or mental retardation and language disorders (see Tuchman, this volume).

4

Neurogenic Language Disorders in Children

LANGUAGE DISORDERS DUE TO PRE-PERINATAL LESIONS The most frequent cause of prenatal lesion is cerebral palsy. The incidence of cerebral palsy of pre-perinatal origin is approximately 2 in 1000 births. Of these cerebral palsy cases approximately one-third have hemiplegia. The underlying unilateral hemispheric brain injury is supposed be due to a thrombotic, vasospasmic or embolic episode in the middle cerebral and/or the internal carotid artery. Between 30% and 40% of such hemiplegic cases develop a cerebral seizure disorder. As documented by many studies, the neuropsychological sequelae of early brain damage are relatively mild if compared with those of adults. Besides, contrary to the case of adults, not all cases of early brain damage show a clear-cut correlation of symptoms with characteristics of the lesion. The degree of preservation or recovery of language and other cognitive functions may be dependent on several factors such as time of injury, side of lesion, size of lesion; presence of epilepsy and role of anticonvulsant therapy. Numerous studies have been carried out to verify the effects of early left hemisphere damage (LHD) versus right hemisphere damage (RHD) on cognitive development, with particular attention to language development. Some studies show that, regardless of the affected hemisphere, linguistic functions tend to be preserved, while other studies reveal greater difficulties in children with left hemisphere damage in the acquisition of vocabulary and grammar (see Chilosi et al, this volume). Numerous reports demonstrate that seizures accompanying early brain injury are associated with poorer language and cognitive outcome (cf. Vargha-Khadem et al., 1992). The pathophysiological mechanism determining a deficit in cognitive and linguistic development in children with early hemisphere damage and epilepsy has not been clearly identified yet. Some authors have suggested that antiepileptic therapy may play an unfavorable role, while other authors have drawn the attention to some variables such as the presence of epileptiform abnormalities in NREM sleep, which associate these clinical pictures to Landau-Kleffner Syndrome (see Fabbro et al., this volume).

DEVELOPMENTAL LANGUAGE DISORDERS Developmental language disorders (DLDs) — also known as Specific Language Impairment (SLI) or Developmental Dysphasia — are language acquisition disorders manifesting in children with normal nonverbal intellectual development in the absence of hearing loss, frank neurological deficits, severe emotional disorders and environmental differences and deprivation. Children with specific language impairment show a very slow and laborious language development. They speak late as compared to peers and show comprehension and production disorders affecting more than one linguistic level (phonological, morphological, lexical, syntactic and semantic). Developmental language disorders are to be distinguished from acquired language disorders (acquired aphasia) affecting children with normal language development until their occurrence. The frequency of DLDs in children aged 5-6 years is surprisingly high, around 4% (Fletcher and Hall, 1993). Many classifications for

Introduction

5

developmental language disorders in children have been proposed, some of which are based on statistical criteria (e.g., the International Classification of Diseases, 10th Edition, ICD -10th, 1992), others on clinical data (Rapin, 1996). In the ICD-10th classification developmental language disorders are described in section F80 encompassing three syndromes: 1) Specific speech articulation disorders (F 80.0): children use sounds that are below the norm as compared to their mental age, whereas all other linguistic tasks are in the normal range; 2) Expressive language disorder (F80.1): the expressive spoken language ability of the children is markedly below the appropriate level for their mental age, and there may be an alteration in speech articulation; 3) Receptive language disorder (F80.2): the receptive ability of the children to understand spoken language is markedly below the appropriate level for their mental age and expressive language will also be markedly affected. Many studies have investigated the causes of DLDs (cf. Bishop, 1997; Leonard, 1999). At the pathophysiological level, some children are unable to discriminate language sounds at the normal speech speed (Merzenich et al, 1996), in others expressive language disorders are associated to developmental verbal dyspraxia (Shriberg et al., 1997) or to language acquisition deficits with a genetic origin (Gopnik, 2000). Several studies have shown that many children with DLDs present with paroxysmal abnormalities in non-REM sleep similar to those found in LandauKleffner Syndrome (Duvelleroy-Hommet et al, 1995). In particular, more than 50% of children with receptive language disorder (F80.2) have epileptiform abnormalities in NREM sleep (Picard et al, 1998; Fabbro et al, 2000). According to preliminary studies, an association of pharmacological treatment with valproic acid to speech therapy markedly improves language development in these children. Recently, Guerreiro et al. (2002) have made a relevant progress in understanding the causes of DLDs. They systematically studied the neuroimaging findings (MRI 2.0 T scanner) in a group of children with DLDs. All the children presented with pictures of polymicrogyria that were related to the degree of severity of dysphasia. Their findings suggest that developmental language disorders are associated to malformations of cortical development.

LANGUAGE DISORDERS RETARDATION

IN

GENETIC

SYNDROMES

WITH

MENTAL

An important line of research in modern clinical neurolinguistics is the study of language deficits in genetic syndromes with mental retardation. Recent studies have shown that some genetic syndromes such as Down Syndrome, Williams Syndrome, Fragile X Syndrome, Turner Syndrome, Prader-Willi Syndrome, etc., have deficits that are specific to each of them. For example, in Down Syndrome, the phonetic-phonological and the morphosyntactic levels are particularly affected, while in Williams Syndrome these levels are sufficiently spared, while the pragmatic level is impaired (cf. Rondal and Edwards, 1997). Language deficits peculiar to genetic syndromes are correlated with specific neurofunctional alterations that are typical of each of these pictures (cf. Tager-Flusberg, 1999).

6

Neurogenic Language Disorders in Children

CONCLUSION The different neurogenic language disorders described here and discussed in detail by the authors who contributed to this volume suggest that language disorders in children, both acquired and developmental, should be managed by an interdisciplinary approach. Each single disorder should also be studied keeping in mind the whole range of childhood language disorders.

REFERENCES Becker, L.E. and V. Jay (1990). Tumors of the central nervous system in children. In: Management of Childhood Brain Tumors (Deutsch M., ed.), pp. 5-51. Kluwer, Boston. Bishop, D. V. (1997). Uncommon Understanding. Development and Disorders of Language Comprehension in Children. Psychology Press, Hove. Duvelleroy-Hommet, C, C. Billard, B. Lucas, P. Gillet, M. A. Barthez, J. J. Santini, E. Degiovanni, F. Henry, B. De Toffol and A. Autret (1995). Sleep EEG and developmental dysphasia: Lack of consistent relationsip with paroxysmal EEG activity during sleep. Neuropediatrics, 26, 14-18. Esposito, A., G. Demeurisse, B. Alberti and F. Fabbro (1999). Complete mutism after midbrain periaqueductal gray lesion. NeuroReport, 10, 681-685. Fabbro, F. (1999). Concise Encyclopedia of Language Pathology. Pergamon, Oxford. Fabbro, F. (2000a). Languages Disorders in Children: An Introduction. Saggi, 26, 9-12. Fabbro, F. (2000b). Introduction to language and cerebellum. JNeuroling, 13, 83-94. Fabbro, F. and C. Zucca (2000). Acquired neuropsychological disorders in children with epilepsy. Saggi, 26, 23-29. Fabbro, F., C. Zucca, M. Molteni and R. Borgatti (2000). EEG abnormalities during slow sleep in children with developmental language disorders. Saggi, 25, 41-48. Fletcher, P. and D. Hall (1993). Specific Speech and Language Disorders in Children. Singular, San Diego. Gopnik, M. (2000). The investigation of genetic dysphasia. Saggi, 26, 31-40. Guerreiro, M. M., S. R. Hage, C. A. Guimaraes, D. V. Abramides, W. Fernandes, P. S. Pacheco, A. M. Piovesana, M. A. Montenegrol and F. Cendes (2002). Developmental language disorders associated with polymicrogyria. Neurology, 59, 245-250. International Statistical Classification of Diseases and Related Health Problems. Tenth Revision (1992). World Health Organization, Geneva. Landau, W. M. and F. R. Kleffner (1957). Syndrome of acquired aphasia with convulsive disorder in children. Neurology, 7, 523-530. Lebrun, Y. and F. Fabbro (2002). Language and Epilepsy. Whurr, London. Lenneberg, E. H. (1967). Biological Foundations of Language. John Wiley & Sons, New York.

Introduction

1

Leonard, L. B. (1998). Children with Specific Language Impairment. MIT Press, Cambridge. Levishon, L., A. Cronin-Golomb and J. D. Schmahmann (2000). Neuropsychological consequences of cerebellar tumor resection in children. Brain, 123, 1041-1050. Mantovani, J. F. and W. M. Landau (1980). Acquired aphasia with convulsive disorder: Course and prognosis. Neurology, 30, 524-529. Merzenich, M. M., W. M. Jenkins, P. Johnston, et al. (1996) Temporal processing deficits of language-learning impaired children ameliorating by training. Science, 271, 77-81. Picard, A., F. Cheliout Heraut, M. Bouskraoui, M. Lemoine, P. Lacert and J. Delattre (1998). Sleep EEG and developmental dysphasia. Dev Med Child Neurol, 40, 595-599. Pollack, I. F. (1997). Posterior fossa syndrome. Int RevNeurobiol, 41, 411-432. Rapin, I. (1996). Preschool Children with Inadequate Communication. Mac Keit Press, London. Riva, D. and C. Giorgi (2000). The Cerebellum contributes to higher functions during development. Brain, 123, 1051-1061. Rondal, J. A. and S. Edwards (1997). Language in Mental Retardation. Whurr, London. Shriberg, L. D., D. M. Aram and J. Kwiatkowski (1997). Developmental apraxia of speech. J Speech Hear Res, 40, 273-285. Tager-Flusberg, H. (1999). Neurodevelopmental Disorders. The MIT Press, Cambridge. Van Hout, A. (2000). An outline of acquired aphasia in children. Saggi, 26, 13-21. Vargha-Khadem, F., E. Isaacs, S. Van der Werf, S. Robb, J. Wilson (1992). Development of intelligence and memory in children with hemiplegic cerebral palsy. Brain, 115, 315329.

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Pathophysiology of Landau-Kleffner Syndrome

9

2

PATHOPHYSIOLOGICAL BASIS OF APHASIA AND VERBAL OUTCOME IN LANDAU-KLEFFNER SYNDROME Marie-Noelle Metz-Lutz Louis Pasteur University, France Steve Majerus University of Liege and Fonds National de la Recherche Scientifique, Belgium

Abstract Acquired childhood aphasia with epilepsy described by Landau and Kleffncr (LKS) in 1957, differs, by its clinical features and prognosis, from other types of aphasia in children due to brain structural lesions. Several critical features appear to influence consistently the prognosis of language disorder: the age at onset and the duration of language disorder associated with EEG abnormalities during wakefulness and sleep and the location of the epileptic focus. In order to elucidate the pathophysiological basis of epileptic aphasia and particularly of its poor outcome, we reexamine neuropsychological, electrophysiological and neuro-imaging data from the long-term follow-up study of several cases of Landau and Kleffner Syndrome (LKS). Our neuropsychological findings show that although the outcome of language abilities is variable, the common residual verbal disorders associate an impaired phonological short-term memory with a permanent one-ear extinction on dichotic listening tests contraleral to the temporal cortex previously affected by the epileptic focus. To check the hypothesis of a permanent dysfunction in the auditory system suggested by these findings, we studied auditory event-related potentials studies in order to localize the level of the dysfunction in auditory language processing and along the auditory pathways. Using H215O labeled positron emission tomography (PET), we compared the brain activation for immediate serial recall of lists of 4 words, contratsted to single word repetition in three recovered LKS patients and 14 healthy controls. Both ERP's and PET's findings suggest that the residual verbal impairments at the late outcome of LKS might indeed be related to persistent dysfunction in the temporal regions that were involved in the epileptic focus during the active phase.

Keywords: childhood epilepsy, Landau-Kleffner Syndrome, language, phonological shortterm memory, pathophysiology, brain imaging

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Neurogenic Language Disorders in Children

INTRODUCTION In 1957, Landau and Kleffner reported the cases of six children, instructed in a deaf institute of Saint Louis-Missouri, who developed aphasia in relation to convulsive disorder. They defined the syndrome as acquired childhood aphasia with convulsive disorder, called several years later Landau-Kleffner Syndrome (LKS). Following this seminal report, no new cases of acquired epileptic aphasia were described until 1968. From this date, an increasing number of reports were published providing deeper analysis of the aphasic symptoms, the electrophysiological features of epileptic discharges and the outcome of LKS. In 1992, William Landau's editorial in Annals of Neurology defined the label "Landau-Kleffner Syndrome" "an eponymic badge of ignorance" (Landau, 1992). Indeed, the still prevailing use of the generic label seems to imply that our knowledge about the aetiology, pathological physiology and therapy of the disease has made no significant progress during the 35-year history of this clinical phenomenon. Have we really made no advancements in the understanding of the pathophysiological basis of epileptic childhood aphasia or was Landau overly pessimistic in his appraisal of the scientific literature? In the present paper, we intend to provide a more optimistic review of the different studies aimed at understanding the relationship between the two main symptoms of this disease, i.e. epilepsy and aphasia. Firstly, we will summarize the main clinical and electrophysiological features of the syndrome and discuss their relationships with other agerelated epileptic conditions. From a set of recent metabolic and electrophysiological findings obtained both during the active phase and after recovery of LKS, we will set out a provisional pathophysiological account of epileptic aphasia and its residual verbal impairment.

CLINICAL FEATURES OF ACQUIRED EPILEPTIC APHASIA Beaumanoir (1992) reviewed about 200 cases described in 57 papers published between 1968 and 1990. In the following decade, no less than 145 papers were devoted to LKS adding 118 new clinical descriptions. This set of case reports provides a rather sound outline of the common clinical features of acquired epileptic aphasia. Epileptic disorders Despite its rarity - in a twenty-year cohort study of 440 epileptic children, Landau-Kleffner Syndrome represents less than 0.5 % (Kramer et al, 1998) - the syndrome comprises very typical features. It is characterised by a sudden onset between the age of 3 and 8 in children with otherwise usually normal neurocognitive development. In 70% of the cases, the onset is before age 6 and rarely occurs after the age of 8 (7%). Less than 13% of the cases may have had an impaired language development. Overt epileptic seizures are not present in all LKS children, only 72% of them present at least one seizure. One third experiences only one

Pathophysiology of Landau-Kleffner Syndrome

11

seizure, usually at the beginning of the disease. When present, seizures are of various types, but generalised or partial motor seizures are the most frequent. Whatever seizures are present, the EEG is always abnormal with repeated large-amplitude spikes followed by a large slow wave. During wake, these spike-wave discharges (SWDs) occurring on an almost normal background activity have a focal organisation (Figure 1). Usually the epileptic focus is unilateral. The observation of bilateral or multiple foci is not rare and raises the issue of secondary epileptic foci. Initially focal, the SWDs progressively spread to the whole hemisphere, but remain predominant over the temporal derivations.

Figure 1 — A Landau-Kleffner Syndrome typical EEG recorded during wakefulness showing paroxysmal spike-wave discharges (SWDs). The higher amplitude of SWDs over the left temporal electrodes (C3/T3; T3/O1) is indicative of the temporal focus of SWDs.

Figure 2 — LKS EEG recorded during sleep showing an aspect of continuous spike wave discharges during slow sleep (CSWSS).

12

Neurogenic Language Disorders in Children

During sleep, SWDs increase in frequency and spread to the contralateral hemisphere, leading to an aspect of continuous spike wave discharges during slow sleep (CSWSS) (Figure 2), which covers at least 80% of the sleep time. This sleep EEG profile, in the presence of nonlesional acquired childhood aphasia, may be considered as a hallmark for the diagnosis of LKS. Typical neuropsychological impairments Aphasia is the first symptom in 54% of LKS case reports. Verbal impairment begins with comprehension disorder and auditory agnosia in 85% of cases. Expressive disorders appear progressively and are characterised by vocabulary loss and speech reduction leading progressively to muteness. The severe deficits in auditory comprehension are the most common feature of LKS. Often LKS children are thought, at first, to be deaf, although audiometric investigations show normal hearing. Auditory disorders often appear like an auditory agnosia involving both verbal and non-verbal discrimination (Koeda & Kohno, 1992; Maquet et al, 1995). However, an in-depth evaluation of auditory discrimination evidences a dissociation between the discrimination of environmental sounds and phonological auditory discrimination, suggesting that the primary deficit of the receptive aphasia is an impairment of auditory phonological discrimination rather than a generalised auditory agnosia (Korkman et al, 1998; Metz-Lutz et al, 1999b). In most cases reported in the literature, expressive language impairments follow the onset of auditory comprehension deficits. Expressive disorders typically begin either with a progressive loss of vocabulary or phonological disturbances. In one recent case report, stuttering was the first symptom (Tutuncuoglu et al, 2002). Some authors have seen the expressive disorders of LKS as secondary to the impairment of phonological decoding. Expressive language disorders gradually increase and children become mute within several weeks. However, various patterns of expressive disorders have been described with agrammatism, echolalia, anomia or phonetic distortions (Paquier et al, 1992). In contrast to childhood aphasia due to focal lesions, paraphasia and neologisms are frequent aphasic symptoms observed before the complete loss of expressive language that may last several months, even years, if antiepileptic treatment is ineffective. Behavioural impairments with hyperactivity are mentioned in 78% of reported LKS cases. Landau and Kleffner already mentioned attention disorders and hyperactivity, which they viewed as a psychological reaction to impaired auditory comprehension. Preservation of nonverbal abilities is another common feature of LKS. This allows the use of gestures or lipreading as an alternative mode of communication. Figure 3 illustrates the typical performance profile on the different subtests of the Wechsler Intelligence Scale for Children Revised (WISC-R) showing very poor performances on the verbal subtests, particularly the digit span and vocabulary tests. The only disturbed nonverbal subtest is typically the coding test that requires attention capacities.

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Figure 3 — Typical performance profile on the Wechsler Intelligence Scale for Children Revised observed in LKS. The stars indicate the subtests which are the more systematically affected.

CLINICAL EVOLUTION Along the course of LKS, the degree of expressive impairments fluctuates. Periods of transient recovery are often observed after the introduction or change of anti-epileptic medication that successfully normalises the EEG, for several weeks or months ( Mantovani & Landau, 1980; Dugas et al, 1982; Marescaux et al, 1990). Several group studies emphasised the almost parallel fluctuation of aphasic disorders and EEG abnormalities and discussed the pharmacological sensitivity of both symptoms (Marescaux et al, 1990; Paquier et al, 1992; Robinson, Baird, Robinson, & Simonoff, 2001). They showed that medication active on the GABAergic receptors like Benzodiazepine (BDZ) favourably influences epileptic and aphasic symptoms, but most often only transiently. Conversely, medication typically active in focal epilepsy, particularly in temporal lobe epilepsy, like carbamazepine, usually worsens epilepsy, aphasia and behavioural disorders (Beaumanoir, 1992). Although their mode of action remains unknown, the corticosteroids have been shown to be useful after relapse of epilepsy and aphasia following an initial treatment by BDZ (Marescaux et al, 1990). According to the specific pattern of aphasic disorders involving primarily auditory comprehension, the use of a manual language has been proposed to prevent continuing problems with communication (Baynes et al, 1998; Perez et al, 2001). In this way, rehabilitation strategies involving signed language or cued speech have been shown to be adequate to bypass language deprivation during the active period of LKS. Indeed, the active

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period of epileptic aphasia ranging from 3 to 10 years overlaps the most critical period for the development of phonological and syntactic skills as well as for verbal learning.

LATE OUTCOME OF LKS While epileptic seizures and EEG abnormalities completely disappear at the age of 12 or 13 (Dugas et al, 1982; Mantovani & Landau, 1980; Paquier et al, 1992), recovery of receptive and productive language is variable. The verbal outcome seems to be poorer in LKS than in acquired childhood aphasia related to head injury. Moreover, in LKS outcome appears to be better for late-onset aphasic disorders, in contrast to childhood aphasia consecutive to an acquired brain lesion (Bishop, 1985; Beaumanoir, 1992; Kaga, 1999). Finally, poorer outcome appears to be related to the duration of epileptic aphasia (Metz-Lutz et al, 1999b; Robinson et al, 2001). Some children recover normal or near to normal written and oral language (Mantovani & Landau, 1980; Soprano et al, 1994; Robinson et al, 2001). However, most LKS patients show difficulties, affecting phonological aspects of language processing most severely (Zardini et al, 1995; Metz-Lutz et al, 1996; Metz-Lutz et al, 1999a). Chronic auditory agnosia has been described in the presence of the most unfavourable verbal outcome (Baynes et al, 1998; Sieratzki et al, 2001). Residual verbal impairments have been reported to involve both phonological and metaphonological judgments (Zardini et al, 1995; Notoya et al, 1991; Ege & Mouridsen, 1998; Vance et al, 1999), phonological verbal fluency (Metz-Lutz et al, 1999b) and articulatory aspects of speech production (Soprano et al, 1994). Several long-term follow-up studies showed a better outcome for naming and syntactic skills ( Zardini et al, 1995; Metz-Lutz et al, 1999b). One very consistent finding is a deficit in phonological short-term memory (STM) performance, even in patients showing relatively good language recovery (Soprano et al, 1994; Grote et al, 1999; Metz-Lutz et al, 1999b; Plaza et al, 2001; Robinson et al, 2001; Majerus et al, 2004). For example, Soprano et al. (1994) observed that the performances of LKS patients on auditory-verbal STM tasks were more severely impaired than their performances on other language processing tasks, several months after the onset of recovery from LKS. Similarly, Grote et al. (1999) and Robinson et al. (2001) showed that LKS patients with complete or nearly complete language recovery still presented deficits on tasks involving STM processing, such as verbatim sentence recall and serial recall of letter and digit sequences. More precisely, in a recent case study of 3 young adult patients who recovered from LKS 7-10 years ago, Majerus et al. (2004) observed selective deficits on tasks requiring short-term storage of phonological information. However, performance for short-term retention of lexico-semantic information was preserved. For example, the patients' scores for immediate

Pathophysiology of Landau-Kleffner Syndrome

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serial recall of nonword sequences and for a rhyme probe1 task were severely impaired in two patients, and more mildy impaired for the third patient, while performance on a category probe task2 was completely preserved in all three patients. Although two of the patients also presented with residual phonological processing deficits (as evidenced by impaired performance in speeded single nonword repetition and phonological awareness tasks), the severity of the phonological processing deficit was not related to the severity of their phonological STM impairment.

PATHOPHYSIOLOGICAL BASIS OF EPILEPTIC APHASIA A focal epileptic dysfunction in the temporal lobe As early as 1957, when the first LKS case report was published, a direct relationship between epilepsy and acquired aphasia was suggested. Indeed, on the basis of the EEG findings, Landau and Kleffner assumed "that persistent convulsive discharges in brain tissue largely concerned with linguistic communication result in the functional ablation of these areas for normal linguistic behavior". The almost parallel fluctuation of verbal impairments and epilepsy, more particularly with the EEG abnormalities observed in the follow-up studies, supported this assumption (Dugas et ah, 1982; Hirsch et ah, 1990; Paquier et ah, 1992; Lanzi et ah, 1994; Soprano et ah, 1994). As structural neuroimaging with computed tomography (CT) and magnetic resonance imaging (MRI) usually do not disclose structural brain lesions, several studies have looked at possible metabolic abnormalities common to LKS. Evidence from metabolic studies. Several studies using single photon emission computerised tomography (SPECT) have shown abnormal perfusion in the temporal lobe which correlates with the localisation of the epileptic focus (Mouridsen et ah, 1993; Harbord et ah, 1999). Similarly, positron emission tomography (PET) studies using 2-deoxy-2-[18F]fluoro-Dglucose (FDG) and carried out in approximately 29 LKS children consistently reported metabolic abnormalities in the temporal lobes; these abnormalities were either a unilateral or bilateral increase or decrease of glucose uptake (Maquet et ah, 1995; da Silva et ah, 1997). In one study, glucose consumption was investigated with 18FDG-PET at different times during the evolution of LKS in the same patients. This study showed that the metabolic changes appeared to be correlated with the epileptic activity, characterised by an hypermetabolic focus during the active phase of epileptic aphasia and a hypometabolic focus when EEG activity In a rhyme probe task, word lists of increasing length are presented auditorily. At the end of each list, a new word is presented and the participants are asked to determine whether this probe word rhymes with one of the words in the list. 2 The category probe task is very similar to the rhyme probe task but probes specifically STM retention for semantic information. Here, the patients are asked to determine whether the probe word presented at the end of the list belongs to the same semantic category as one of the words in the list.

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went back to normal (Maquet et al, 1995). Several improvements of PET data analyses, including the use of statistical parametric mapping (SPM), the comparison of each patient to a large control group and the co-registration of PET activity with a high resolution 3D-MRI scan of individual brains, have allowed a better definition of the spatial extent of the metabolic abnormalities. This has permitted to establish that, in the active period of epilepsy, the focus of hypermetabolism coincides with the topography of the predominant spike wave discharges recorded on waking and sleep EEG. Interestingly, these studies showed that the significantly higher glucose uptake only involved the associative but not the primary auditory cortex (Maquet et al., 1999). Neurophysiological evidences. Although the EEG recordings show both focal discharges and bilateral generalized spike-and-wave discharges, electrophysiological studies based on dipole mapping of spike discharge and magnetic source imaging provided arguments in favour of a focal source of epileptic discharges localised in the superior temporal gyms (Morrell, 1995). Using magneto-encephalographic recording (MEG) of SWD, Paetau et al. (1991) demonstrated that all spikes originated close to the auditory cortex, contaminating the ipsilateral auditory cortex and suppressing the contralateral auditory evoked potentials. Another study using auditory evoked magnetic field recordings (Paetau, 1994) in six children with LKS, suggested that the epileptiform activity may be produced by sound-responsive neurons in the non-primary auditory cortex within the middle and posterior perisylvian cortex. This set of findings is congruent with the suggestion that the apparently bilateral epileptic discharges of CSWSS are "driven" by a focal and unilateral source of primary epileptogenic activity in the superior temporal cortex. It also suggests that the bilateralisation of epileptic discharges and their generalisation during sleep makes the homotopic temporal cortex in the opposite hemisphere unavailable for auditory processing and more specifically for verbal processing. This might account for the main features of epileptic aphasia, i.e. the aphasic impairments that do not depend on the side of the temporal epileptic focus and the auditory agnosia observed in the active phase for about all LKS cases reported in the literature. An age-related focal epilepsy. The EEG pattern of SWDs and CSWSS is specific to agerelated idiopathic focal childhood epilepsy (IFCE). Indeed, SWDs are common to a wide range of so-called benign partial childhood epilepsies including rolandic epilepsy, the most frequent childhood epilepsy. SWDs and CSWSS are encountered in children aged 3-10 years and disappear in early adolescence, whatever the effectiveness of anti-epileptic treatment. Several studies showed that in IFCE, the epileptic foci are mainly located in the associative cortex whose maturation continues throughout childhood and adolescence. In LKS, the age of onset (70% before the age of 6) corresponds to the period of brain maturation that follows the peak of synaptogenesis in the associative temporal cortex. Considering the typical aspect of the epileptic discharges in LKS, it has been suggested that following a brief spike, the slow-wave component might be the manifestation of an

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inhibitory mechanism (Engel, 1995; 1996). Such a mechanism would not only prevent the occurrence of seizures dependent on the spike component but also inhibit the normal functioning of the cortical area involved in the generation of epileptic discharges. As the inhibitory component of the epileptic activity is predominant over the other EEG components, the epileptic aphasia would be the expression of an excess of inhibitory activity limited to a part of the temporal cortex. To account for this particular pattern of epileptic activity, Maquet et al. (1999) have hypothesised a focal alteration of the maturational processes leading to an imperfect neuronal wiring that induces an imbalance between inhibitory and excitatory drives generating epileptic discharges. According to this hypothesis, the large slow-wave component indicating a predominant inhibitory mechanism would result from a local excess of activity of the inhibitory interneurones within the epileptic focus. At the same time, the high density of synapses characteristic of this period of cortical maturation would facilitate the diffusion of SWDs leading to the aspect of CSWSS. The benefit of multiple subpial transection in LKS reinforced this hypothesis. Indeed, this particular surgical procedure consisting in the selective disruption of the intracortical horizontal fibers was used to mechanically interrupt the deleterious intracortical circuitry (Morrell et al, 1995). This method permitting the resumption of more normal synaptisation suppresses the focal epileptic activity and allows the recovery of the normal functioning of the temporal associative cortex.

PATHOPHYSIOLOGICAL BASIS OF VERBAL OUTCOME IN LKS The residual verbal impairments following LKS have been explained in different ways. Mantovani and Landau (1980) suggested that, like in the case of focal brain damage, the longterm effect of the epileptiform discharges on brain cells of a cortical area results in a functional hemispheric reorganisation with the shifting of language area in a cortical area spared by the epileptic activity. Bishop (1985) assumed that the loss of auditory verbal comprehension, during the active period of epileptic aphasia, deprives the child from the communicative verbal experience crucial for language development. Finally, Baynes et al. (1998) suggested that the nature of dysfunction and the outcome depend on the stage of language development at which LKS children experienced the disruption of auditory input. As regards the verbal outcome of epileptic aphasia, two points are at issue. Do the residual verbal disorders following LKS relate to some specific impairment in verbal processing? Indeed, a very consistent finding is a deficit in phonological short-term memory (STM) performance, even in patients showing relatively good language recovery as will be shown below ( Soprano et al, 1994; Grote et al, 1999; Metz-Lutz et al., 1999a, b; Plaza et al, 2001; Robinson et al, 2001; Majerus et al, 2003, 2004). The second point deals with the pathophysiological mechanisms underlying the residual verbal deficits. The data of PET studies performed at the recovery period of epileptic aphasia showing a focal hypometabolism in the temporal area initially involved in the epileptic focus suggest a persistent functional

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impairment of this cortical area. This persistent functional cortical impairment could also underlie the residual verbal deficits. Evidence for persistent dysfunction in the superior temporal cortex and its relationship to impaired phonological STM. One clinical finding consistently reported in all LKS follow-up studies including dichotic listening tasks is the one-ear dichotic listening extinction involving the ear contralateral to the temporal cortex affected by the epileptic discharges during the active phase of epilepsy (Metz-Lutz et al, 1997; Plaza et al, 2001). A similar one-ear dichotic extinction was described in patients who suffered structural lesion involving the temporal or parieto-temporal cortex and the geniculo-cortical pathway (Kimura, 1961; Damasio & Damasio, 1979). In LKS, this finding might be the expression of a permanent dysfunction in the temporal cortex. This assumption is supported by the findings of PET scan studies performed in the late recovery period in LKS patients, which disclosed a focal hypometabolism in the superior temporal region contralateral to the dichotic extinction (Maquet et al., 1999). In order to test this hypothesis, we used auditory evoked potentials (AEP) enabling us to check the whole auditory system along the auditory pathways to the temporal associative cortex in five children who had recovered from LKS and showed a right or left dichotic listening extinction. The five patients were compared to five control subjects matched for age and gender. This study showed normal and symmetrical early and middle latency auditory evoked potentials but significant alteration in the late Nib and N250 components with reduced amplitude over the temporal sites contralateral to the dichotic listening extinction (Wioland et al, 2001). The Nib and N250 components are known to arise from the temporal associative cortex. In a second study, we explored more specifically the integrity of temporal associative cortex and its relationship to the residual phonological STM deficits that characterise the late outcome of LKS, using PET imaging (Majerus et al, 2003). The three adult patients for which we had identified relatively specific phonological STM impairments (see above; Majerus et al, 2004) also participated in this second study. They were asked to repeat auditorily presented 4-word sequences (STM condition) or single words (control condition) while they underwent H2I5O-PET imaging. During the STM condition, we observed decreased activation in the bilateral posterior superior temporal gyms and adjacent perisylvian cortex in the two patients who presented the most severe phonological STM impairments. In the third patient whose phonological STM impairment was much milder, we observed increased activation in the right posterior superior temporal gyms during the STM condition. These data show that the posterior temporal cortex remains dysfunctional in the late outcome of LKS, relative to healthy controls, and is related to the persistent phonological STM impairment. Furthermore, we also observed a relationship between the regions that displayed abnormal glucose metabolism in the three patients during the active phase of the LKS (Maquet et al., 1995) and the recent brain activation pattern during the STM task. The first of the two

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patients with the most important phonological STM deficits had shown decreased glucose uptake in the left superior and middle temporal regions during the active phase of LKS as well as reduced glucose uptake bilaterally in superior temporal regions several months later. In the recent brain activation study, reduced activity in the right posterior superior temporal gyrus was observed. During the active phase the second patient had shown increased glucose metabolism in the right middle and superior temporal regions and decreased glucose metabolism in the left perisylvian cortex. In the recent study, diminished activity bilaterally in the posterior superior temporal cortex was observed. The third patient with milder phonological STM deficits had shown a very focal increase in glucose metabolism at the level of the right STG, which became hypometabolic several months later. In the recent study, increased activation in the right posterior as well as slightly reduced activity in the anterior part of the right midtemporal gyrus (although only at uncorrected P-levels) was observed. In sum, the results suggest that late outcome of LKS may indeed be characterised by a longlasting dysfunction of mainly posterior and superior temporal gyri and adjacent perisylvian areas which had also been dysfunctional during the active phase of epilepsy. Furthermore, this persistent dysfunction of superior temporal gyri appears to be related to the residual phonological STM impairments. DISCUSSION In this paper, we attempted to provide a provisional pathophysiological account of aphasic disorders and the late verbal outcome of LKS, a particular condition where acquired aphasia appears as the main clinical symptom of a focal epileptic activity. Most importantly, this epileptic activity has to be explained by a predominant inhibitory rather than by an excitatory mechanism. Indeed, the main symptoms of LKS as opposed to other childhood focal epilepsies are not sudden and brief episodes of behavioural changes in the form of seizures, but the rapidly progressive disappearance of initially normally developing language processing, appearing like an interictal disorder. Indeed, aphasic disorders are not transitory as would be the clinical expression of seizure. Furthermore, the propensity of SWDs to diffuse to the contralateral homologous region, probably due to the stage of maturation of the cortical tissue at which SWDs occur, prevents any possible compensation as long as the epilepsy is active. Thus, we think that the local excess of inhibitory mechanism can be viewed as a plausible pathophysiological account for both the "functional ablation" of verbal cortex and the inability to develop compensatory mechanisms during the active phase of epilepsy. This account suggests a more or less direct relationship between the (inhibitory) epileptic activity itself and the verbal impairment during the active phase. At outcome, a similar relationship is observed between residual phonological STM deficits and the persistent dysfunction of the superior temporal cortex that was involved in the epileptic focus during the active phase. However, this association between aphasia and epilepsy does not necessarily imply that aphasia and phonological STM deficits are exclusively and directly caused by the epileptic activity. Instead, we cannot exclude that the aphasic and epileptic symptoms during

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the active phase, as well as the residual verbal and STM impairments at later outcome, are both the result of a third variable. This third variable could represent the focal alteration of maturational processes of the cortex leading, in the case of LKS, to abnormal neuronal wiring in the superior temporal cortex, as suggested by Maquet et al. (1999). This abnormal wiring, in turn, will lead to epileptic activity within this area as well as to depressed language processing. The epileptic activity will then further aggravate the language impairments by further inhibiting functioning within the temporal cortex, via the inhibitory mechanisms discussed above. In addition, the absence of environmental verbal stimulation resulting from the severe receptive auditory-verbal impairments will also contribute to language decline. Although epileptic activity will disappear in adolescence, the wiring of superior temporal cortex may remain abnormal and thus language and STM processing will still be processed in a less efficient way. If the hypothesis of a focal alteration of the maturational processes is correct, it raises the issue of what determines this focal alteration and its more frequent localisation in the associative temporal cortex. This will be the challenge for future work on LKS. Whatever the pathophysiological considerations, one should keep in mind that during the active period of LKS, brain maturation is still in process. This maturation depends on both an internal genetically determined programme and external stimulation, notably perceptualmotor experience. Regarding verbal development, the experience of verbal input and interindividual verbal communication is especially determinant for further language development. This implies that the development of effective rehabilitation programmes, aiming at preventing and reducing the effect of deprivation of normal auditory feedback on phonological, syntactic, and lexical development, remains of utmost importance. ACKNOWLEDGEMENTS Steve Majerus is a Postdoctoral Researcher at the Fonds National de la Recherche Scientifique, Belgium.

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associated with Landau-Kleffner Syndrome: a long-term study of auditory disturbance. Auris Nasus Larynx, 18, 297-305. Paetau, R. (1994). Sounds triggers spikes in the Landau-Kleffner Syndrome. J Clin Neurophysiol, 11, 231 -241. Paetau, R., M. Kajola, M. Korkman, M. Hamalainen, M. L. Granstrom and H. Hari (1991). Landau-Kleffner Syndrome: epileptic activity in the auditory cortex. Neuroreport, 2, 201-204. Paquier, P. F., H. R. Van Dongen and C. B. Loonen (1992). The Landau-Kleffner Syndrome or "acquired aphasia with convulsive disorder". Long-term follow up of six children and a review of recent literature. Arch Neurol, 49, 354-359. Perez, E. R., V. Davidoff, A. C. Prelaz, B. Morel, F. Rickli, M. N. Metz-Lutz, P. Boyes Braem and T. Deonna (2001). Sign language in childhood epileptic aphasia (LandauKleffner Syndrome). Dev Med Child Neurol, 43, 739-744. Plaza, M., M. T. Rigoard, C. Chevriemuller, H. Cohen and A. Picard (2001). Short-term memory impairment and unilateral dichotic listening extinction in a child with Landau-Kleffner Syndrome: Auditory or phonological disorder? Brain Cogn, 46, 235240. Robinson, R. O., G. Baird, G. Robinson and E. Simonoff (2001). Landau-Kleffner Syndrome: course and correlates with outcome. Dev Med Child Neurol, 43, 243-247. Sieratzki, J. S., G. A. Calvert, M. Brammer, A. David and B. Woll (2001). Accessibility of spoken, written, and sign language in Landau-Kleffner Syndrome: a linguistic and functional MRI study. Epileptic Disord, 3, 79-89. Soprano, A. M., E. F. Garcia, R. Caraballo and N. Fejerman (1994). Acquired epileptic aphasia: neuropsychologic follow-up of 12 patients. Pediatr Neurol, 11, 230-235. Tutuncuoglu, S., G. Serdaroglu and B. Kadioglu (2002). Landau-Kleffner Syndrome beginning with stuttering: case report. J Child Neurol, 17, 785-788. Vance, M., S. Dry and S. Rosen (1999). Auditory processing deficits in a teenager with Landau-Kleffner Syndrome. Neurocase, 5, 545-554. Wioland, N., G. Rudolf and M. N. Metz-Lutz (2001). Electrophysiological evidence of persisting unilateral auditory cortex dysfunction in the late outcome of Landau and Kleffner Syndrome. Clin Neurophysiol, 112, 319-323. Zardini, G., B. Molterri, N. Nardocci, D. Sarti, G. Avanzini and T. Granata (1995). Linguistic development in a patient with Landau-kleffner Syndrome: A nine year follow-up. Neuropediatrics, 26, 19-25.

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ACQUIRED LANGUAGE DISORDERS AND EPILEPSY: FROM LANDAU-KLEFFNER SYNDROME TO AUTISTIC REGRESSION Roberto Tuchman Dan Marino Center and Miami Children's Hospital, Florida, USA

Abstract — The relationship of epilepsy, either clinical or subclinical, to the acquired aphasia or the loss of communicative intent that occurs in some children, most of whom are on the autistic spectrum, remains controversial and not understood. The report of loss of language in any child should raise concern and there are several clinical syndromes to consider when discussing the Acquired Epileptiform Aphasias (AEA). These include: Acquired aphasia with convulsive disorder or LandauKleffner Syndrome (LKS); Continuous Spike-Waves during Slow Sleep (CSWS) associated with Electrical Status Epilepticus during Slow-Wave Sleep (ESES); Benign Childhood Epilepsy with Centrotemporal Spikes (BECTS), and Autistic Regression with an Epileptiform EEG (AREE). The lack of strict criteria and the overlap of disorders with language loss associated with epilepsy or an epileptiform EEG have made classifying children who undergo a regression of their language in the context of either clinical or subclinical seizures a confusing and controversial undertaking. An important first step in our quest to understand the pathophysiology of the acquired epileptiform aphasias and to develop rational interventions is to rigorously define these syndromes at a clinical level. The purpose of this discussion is to review the nosology of acquired language disorders associated with epilepsy. Key words: language disorders, regression, epilepsy, autism, acquired aphasias, LandauKleffner Syndrome (LKS); Continuous Spike-Waves during Slow Sleep (CSWS), Electrical Status Epilepticus during Slow-Wave Sleep

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Neurogenic Language Disorders in Children

INTRODUCTION The classification of acquired language disorders in children and their relationship to epilepsy is a complex clinical problem. The lack of strict criteria and the overlap of disorders with language loss associated with epilepsy or an epileptiform EEG have made classifying children who undergo a regression of their language in the context of either clinical or subclinical seizures a confusing and controversial undertaking. The term I prefer to use for the above disorders is Acquired Epileptiform Aphasias, as opposed to Acquired Epileptic Aphasias, since epilepsy, defined as more than one unprovoked seizure, is not always present in this group of encephalopathies. The report of loss of language in any child should raise concern. Language regression was considered rare until recent reports have indicated that up to one-third of all children with autism regress in language or in communicative intent (Tuchman & Rapin, 1997). Although it is most often parental awareness of regression or stagnation of expressive language in their toddler or preschooler that brings the child to professional attention, it may be that there are premonitory signs. Some of these are the inability to coordinate attention and share the enjoyment of an event with a social partner. One important hallmark of social communication in early development is joint attention. Joint attention skills refer to the capacity of individuals to coordinate attention with a social partner vis-a-vis some object or event. This capacity, which is an essential precursor to verbal communication, begins to emerge by 6 months of age and takes on several different forms, each of which may be measured reliably in infants and young children. The social-communication disturbance of autism is exemplified by a striking failure to develop adequate joint attention skills or by the loss of these skills once developed. Research indicates that joint attention impairment is characteristic of autism. There is also evidence to suggest that joint attention may predict language, cognitive and social outcomes in children on the autistic spectrum, and that it may be an index of the neurodevelopmental components of the disorder. Consequently, joint attention has become an important dimension to consider in early diagnosis and treatment research in autism and related disorders. There are several clinical syndromes to consider when discussing the Acquired Epileptiform Aphasias (AEA). These include: Acquired aphasia with convulsive disorder or Landau-Kleffner Syndrome (LKS); Continuous Spike-Waves during Slow Sleep (CSWS) associated with Electrical Status Epilepticus during Slow-Wave Sleep (ESES); Benign Childhood Epilepsy with Centrotemporal Spikes (BECTS), and Autistic Regression with an Epileptiform EEG (AREE). All of these clinical syndromes are associated with different degrees of cognitive function or mental retardation (MR) and the language disorder most likely to be present in the majority of the acquired epileptiform aphasias is that of Verbal Auditory Agnosia (VAA). The purpose of this paper is to define, discuss and contrast this group of encephalopathies.

Acquired Epileptiform Aphasia

27

ACQUIRED APHASIA WITH CONVULSIVE DISORDER OR LANDAUKLEFFNER SYNDROME (LKS) Acquired epileptic aphasias have been used as an important model for expanding the concept of childhood epilepsy to include prolonged language, cognitive and behavioral disorders as primary epileptic manifestations (Deonna, 1991). The prototype of AEA is Landau-Kleffner syndrome. Landau-Kleffner syndrome is defined as an acquired aphasia in association with abnormal EEG demonstrating spikes, sharp waves or spike and wave discharges which are usually bilateral and occur predominantly over the temporal and parietal regions (Rapin, 1995a). The definition of LKS has been widely expanded and behavioral problems such as hyperkinesis, rage outbursts, aggressiveness, stereotypies and poor social communication skills in children with language regression and associated epilepsy or with an epileptiform EEG have been included under this eponym. Central to the original description of LKS in 1957 is language regression in association with an epileptiform EEG and either seizures or acquired aphasia are equally likely to be the first presenting complaint in this disorder (Landau & Kleffner, 1957). In LKS it is not the clinical epilepsy that is important in producing the language manifestations of LKS, but the "subclinical seizures" as indexed by epileptiform activity on the EEG as up to 25% of these patients may not have clinical seizures (Tuchman & Rapin, 2002). A rigorous definition of LKS should include only those children with primarily a regression in language and in whom the associated behavioral problems that occur are secondary to the language disorder and not due to a primary behavioral or cognitive regression (Tuchman, 1997). The primary language disorder in the majority of children with LKS is a severe receptive disorder amounting to verbal auditory agnosia (VAA) (Korkman et al., 1998; Klein et al. 2000). VAA is a receptive aphasia or dysphasia for acoustically, but not visually, presented language and arises from inadequate auditory or phonologic processing that engages activity in the primary or secondary auditory cortices and affecting output (expressive) language as well (Majerus et al, 2003). A central theme of any discussion of acquired epileptiform aphasia is the relationship of the abnormal electrical activity to the language disorder. The cortical areas responsible for VAA are the same regions where the centrotemporal epileptiform EEG activity characteristic of LKS and other AEA discussed below is found. Furthermore, VAA is associated with the highest rate of epilepsy, both among children with autistic spectrum disorders and those with developmental language disorders (Tuchman et al., 1991a). Age of symptoms may be important in differentiation of LKS from autistic regression with an epileptiform EGG (AREE) and possibly from other acquired epileptiform aphasias. The mean age of onset of the language regression in autistic spectrum disorders is 21 months and over 90% of children with autism who undergo a regression do so before age 3 years (Tuchman & Rapin, 1997). This is different from LKS where it is reported that mean age of onset is after age 4 years (Robinson et al, 2001). The prognosis in LKS for recovery of

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Neurogenic Language Disorders in Children

language and cognitive function is variable and in general not as good as it is for the seizures (Bishop, 1985; Mouridsen, 1995).

ELECTRICAL STATUS EPILEPTICUS DURING SLEEP

(CSWS) AND BENIGN WITH VENTROTEMPORAL SPIKES (BECTS)

SPIKE-WAVES DURING SLOW SLEEP EPILEPSY

(ESES): CONTINUOUS CHILDHOOD

Electrical status epilepticus during slow wave sleep (ESES) is considered an EEG-defined syndrome characterized by nearly continuous (>85%) spike-and-slow-wave-complexes during non-REM sleep, but not during REM sleep or the awake state. The clinical syndrome that has been mostly associated with ESES is continuous spike-waves during slow sleep (CSWS) (Veggiotti et al, 1999). The majority of children with CSWS have normal development prior to the onset of ESES, but almost all deteriorate cognitively and behaviorally (increased aggressiveness, poor social contact, decreased attention span, and hyperactivity) during ESES (Roulet-Perez, 1993; Nieto-Barrera et al, 1997; Veggiotti et al, 2001). Language deterioration out of proportion to other abilities occurs in some cases. At a behavioral level the major difference between reported cases of LKS and CSWS is that children with CSWS show more diffuse cognitive and behavioral deterioration with dementia and behaviors consistent with autism than do children with LKS (Galanopoulou et al, 2000). Seizures are common in CSWS, but as in LKS not always present. LKS and CSWS syndromes may be on a continuum and as such some investigators have suggested that Landau-Kleffner may be too narrowly defined (Hirsch et al, 2000). Nevertheless, I would suggest that strictly defining these syndromes will be more productive in determining the relationship of acquired language regression to clinical and subclinical epilepsy. The electroencephalographic findings in LKS resemble the EEG findings in benign childhood epilepsy with centrotemporal spikes (BECTS) both in morphology and distribution and in both of these disorders the spikes are activated by sleep (Saint-Martin et al, 2001). At a clinical level these disorders are very different and in general children with BECTS do not have the associated clinically significant language or cognitive dysfunction found in LKS or in CSWS. However, recent work suggests that there is a subgroup of children with BECTS where the evolution of the spikes takes on a more atypical nature and the clinical evolution of these children is more similar to that of children with LKS or CSWS (Fejerman et al, 2000). There is also data suggesting that differences in morphology, topography, organization, and abundance of interictal abnormalities during sleep can differentiate BECTS from LKS early on and prior to the loss of language occurring in LKS (Massa et al, 2000). The outcome of some children with BECTS with atypical evolution of their spikes on EEG and with regression in language and behavior may be similar to those with LKS and CSWS (Yung et al, 2000). Recent work using magnetoencephalography has suggested that the location and possibly orientation of the spike might account for differences in clinical presentation of

Acquired Epileptiform Aphasia

29

disorders such as BECTS, LKS and AREE (Lewine et al, 1999; Sobel et al, 2000; Otsubo & Snead, 2001).

AUTISTIC REGRESSION WITH AN EPILEPTIFORM

EEG (AREE)

Autism is a life-long disorder with clinical symptoms that change with age and often improve with early intervention. Approximately one-third of parents report a regression of language, usually the loss of their toddler's first few words between 18 and 24 months, together with the appearance of autistic behaviors. Autistic regression, including regression in language may fluctuate for many months or even years and then improve, although rarely to complete recovery (Wilson et al, 2003). It is most often parental awareness of regression or stagnation of expressive language in their toddler or preschooler that brings the child to professional attention. Early on in development children with autism display a syndrome-specific inability to coordinate attention and share the enjoyment of an event with a social partner. Impairments in this domain may be assessed with measures of joint attention skills (Mundy et al, 1990). Since autistic regression occurs prior to age 2 years and as such may be associated with a the loss of only a few single words identifying loss of joint-attention skills may be a better early indicator of regression in children with autism. Autistic regression with or without an epileptiform EEG should be differentiated from children classified as having disintegrative disorder (DD) in whom language and behavioral regression is delayed and may occur as late as age 10 years (Rapin, 1995b). Children with disintegrative disorder, sometimes referred to as Heller's syndrome, are more likely to have epilepsy than children with autism (Burd et al, 1989). This group of children differs from children with LKS in the severity of their cognitive and behavioral manifestations and from the much more numerous children with typical autistic regression in two main ways: (1) the regression occurs later, usually between 3 and 6 years, prior to which development was entirely normal, in contrast to children with autism in whom the mean age at regression is 1824 months and earlier development already worrisome in some cases; and (2) the regression is even more profound and may leave these children frankly and permanently demented (Malhotra & Gupta, 1999; Dawson, 2000). The difference between disintegrative disorder and autism with regression is not crisp and what role epilepsy may play in the genesis of either or both is disputed. The relationship of epilepsy, either clinical or subclinical, to the acquired aphasia or the loss of communicative intent that occurs in autistic regression remains controversial and not understood. In a study of 314 children with autism and 237 children with language disorders examined by one child neurologist, parents of 32% of the autistic and 4.6% of the language disordered groups reported a regression (Tuchman et al, 1991a). Epilepsy (at least 2 unprovoked seizures) was correlated with motor and cognitive indices of the severity of the underlying brain dysfunction (Tuchman et al, 1991b). In an independent sample of 585 consecutive children with autistic spectrum disorders seen by another child neurologist,

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Neurogenic Language Disorders in Children

regression was stated to have occurred before age 2 years in 64% of cases and by age 3 years in 95% of cases (Tuchman & Rapin, 1997). Epilepsy was no more frequent (12%) in children who had regressed than in those without a history of regression (11%). An interesting but unexplained observation was that regression was significantly associated with an epileptiform EEG in the non-epileptic group, in that 14% of 155 non-epileptic children who had undergone a regression had an epileptiform EEG during sleep, as opposed to 6% of 364 children with neither regression nor epilepsy. There was no difference in the proportion of children with epilepsy or epileptiform EEGs who had regressed before or after 2 years of age. On the other hand, a recent multi-institutional study of 177 children with a history of language regression found that children with a history of regression prior to age 36 months were more likely to have autism than those who regressed after age 36 months, and that children with regression after age 36 months were more likely to have epilepsy than those with an earlier regression (Shinnar et at, 2001). Although all three studies found a mean age at regression between 21 to 22.8 months, mean age at referral to the specialist was uniformly over age 36 months. The studies just reviewed suggest that there are two groups of children who experience regression: somewhat older children who are more likely to have epilepsy but rarely experience a serious behavioral-autistic regression (the few who do are likely to suffer from the catastrophic disintegrative disorder phenotype), and a younger much larger group in whom epilepsy is less frequent but in whom language regression has a high probability of being associated with a serious behavioral/cognitive deterioration leading to autism. These studies also suggest that there may be neurophysiological markers of regression such as epileptiform discharges; however, their contribution to the autistic regression in this younger group is not known for two reasons: (1) a minority of children without clinical seizures undergo EEG recordings, let alone all night monitoring, and (2) the children are rarely seen at the time of the regression (the mean interval is measured in years, not months). The main cause for this long delay is that very early regression is regularly passed off because it is insidious and occurs so early in the course of language development. This early regression is not given the same importance as language regression in a fully verbal older child. This lack of early recognition may prevent early intensive intervention. Future studies will have to address this important concern.

MEDICAL AND SURGICAL MANAGEMENT OF CHILDREN WITH ACQUIRED EPILEPTIFORM APHASIAS Data regarding response to medication in well-defined subgroups of children with acquired epileptiform aphasias are very limited. The treatment strategies that have been reported for this group of children are those used for the management of children with LKS. Therapy in LKS has been the subject of numerous case reports or short series and the lack of wellcontrolled clinical trials has been frustrating to the clinician faced with a child with an acquired aphasia thought to be secondary to the clinical or subclinical epilepsy.

Acquired Epileptiform Aphasia

31

Anticonvulsants, especially valproate, ethosuximide and the benzodiazepines have been reported to improve the language of a limited numbers of children with LKS (Marescaux et al, 1990; Lerman et al, 1991). The use of ACTH, steroids, or immunoglobulins has also been the subject of several clinical reports which suggest improvements in language and behavior in children with LKS treated with these medications (Prasad et al, 1996; Lagae et al., 1998; Mikati et al, 1998; Tsuru et al, 2000). Several clinical reports of the use of Valproate in children with autism with or without clinical seizures but with epileptiform abnormalities on the EEG suggest an improvement in language and behavior in this group of children with AREE (Nass & Petrucha, 1990; Plioplys, 1994; Childs & Blair, 1997; Hollander et al, 2001; Holmes & Riviello, 2001). In a selected group of children with LKS surgical transection of epileptogenic frontotemporal cortex has been performed and reported to produce short-term improvement in language and behavior in perhaps half of the children (Morrell et al, 1995; Sawhney et al, 1995). Two studies of children with autistic regression and clinical seizures state that aggressive treatment of the seizures with epilepsy surgery was associated with positive outcomes (Neville et al, 1997; Nass et al., 1999). One study suggested that, in children with autism and intractable seizures, surgery may improve the seizures but not the autism (Szabo et al, 1999). The children in these case reports had intractable epilepsy and the epilepsy surgery was being done for the treatment of the seizures and not for the behavior or language dysfunction. A controversial study suggested that multiple subpial transections in children with autism spectrum disorders, a history of language regression, multifocal epileptiform EEGs, and possible minor clinical seizures (i.e. staring episodes, rapid eye blinking) without overt clinical seizures improved in language and behavior after surgery (Lewine et al, 1999). It is important to state that the role of surgery in children with LKS and especially in those with AREE is only recommended for the treatment of the seizures and not for the concomitant language or behavioral deficits.

CONCLUSION From a clinical perspective all children with stagnation or regression in communication skills should be promptly referred to a specialist that can evaluate them from a neurological perspective. It is extremely critical that speech and language intervention is promptly begun in all such children and that all forms of verbal and non-verbal communication systems are taught. An EEG with adequate sleep should be part of the work-up of any child with a history of language regression. Careful monitoring of the language progression should be carried out and in those children who do not progress after communication intervention is begun an overnight EEG with good amount of sleep recording should be obtained. If the EEG demonstrates epileptiform activity consideration should be given to the use of antiepileptic medications.

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Neurogenic Language Disorders in Children

An important first step in our quest to understand the pathophysiology of the acquired epileptiform aphasias and to develop rational interventions is to rigorously define these syndromes at a clinical level. Progress has been made in our understanding of the clinical differences and overlaps between Landau-Kleffner Syndrome and Autistic Regression with an Epileptiform EEG. In the process we have also gained a deeper understanding of the role of epilepsy, both clinical and subclinical, in all epileptic disorders in children with associated acquired aphasia. The use of newer imaging and EEG techniques such as magnetoencephalography is enhancing our ability to determine the role not only of the quantity of EEG discharges but also of the importance of understanding how the topography of the EEG may determine specific symptoms such as language regression. Clinical studies suggest that timing of the seizures or the development of EEG discharges may also help in the differentiation of the acquired epileptiform aphasias. Acquired epileptic aphasias associated with epilepsy or epileptiform abnormalities are not specific entities. The studies reviewed here suggest that they represent part of a spectrum disorder with a common pathophysiology with varying severity of clinical manifestations dependent on the location and quantity of the epileptiform activity. The differences in clinical symptoms and in their relationship to epilepsy or EEG changes in these disorders may, in selected cases, be due only to the time period in development when the seizures occur or to the site or the amount of cortical or subcortical epileptogenic dysfunction. However, the seizures and the EEG findings do not always correlate with the clinical picture and as such the EEG and the seizures may be only epiphenomena that provides for the identification of a diverse group of language-EEG-epileptic encephalopathies with diverse etiologies.

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Mouridsen, S. E. (1995). The Landau-Kleffner Syndrome: a review. Eur Child Adolesc Psychiatry, 4, 223-8. Mundy, P., M. Sigman and C. Kasari (1990). A longitudinal study of joint attention and language development in autistic children. J Autism Dev Disord, 20, 115-28. Nass, R. and D. Petrucha (1990). Acquired aphasia with convulsive disorder: a pervasive developmental disorder variant. J ChildNeurol, 5, 327-8. Nass, R., A. Gross, J. Wisoff and O. Devinsky (1999). Outcome of multiple subpial transections for autistic epileptiform regression. Pediatr Neurol, 21, 464-70. Neville, B. G., W. F. Harkness, J. H. Cross, H. C. Cass, V. C. Burch, J. A. Lees, et al. (1997). Surgical treatment of severe autistic regression in childhood epilepsy. Pediatr Neurol, 16, 137-40. Nieto-Barrera, M., F. Aguilar-Quero, E. Montes, R. Candau and P. Prieto (1997). Epileptic syndromes which show continuous spike and wake complexes during slow wave sleep. Rev Neurol, 25, 1045-51. Otsubo, H., Snead OC, 3rd. Magnetoencephalography and magnetic source imaging in children. J Child Neurol 2001;16(4):227-35. Plioplys, A. V. (1994). Autism: electroencephalogram

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improvement with valproic acid. Arch Pediatr Adolesc Med, 148, 220-2. Prasad, A. N., C. F. Stafstrom and G. L. Holmes (1996). Alternative epilepsy therapies: the ketogenic diet, immunoglobulins, and steroids. Epilepsia , 37, S81-95. Rapin, I. (1995a). Acquired aphasia in children. J Child Neurol, 10, 267-70. Rapin, I. (1995b). Autistic regression and disintegrative disorder: how important the role of epilepsy? Semin Pediatr Neurol, 2, 278-85. Robinson, R. O., G. Baird, G. Robinson and E. Simonoff (2001). Landau-Kleffner syndrome: course and correlates with outcome. Dev Med Child Neurol, 43, 243-7. Roulet-Perez E., V. Davidoff, P. A. Despland and T. Deonna (1993). Mental and behavioural deterioration of children with epilepsy and CSWS: acquired epileptic frontal syndrome. Dev Med Child Neurol, 35, 661-74. Saint-Martin, A. D., R. Carcangiu, A. Arzimanoglou, R. Massa, P. Thomas, J. Motte, et al. (2001). Semiology of typical and atypical Rolandic epilepsy: a video-EEG analysis. Epileptic Disord, 3, 173-82. Sawhney, I. M., I. J. Robertson, C. E. Polkey, C. D. Binnie and R. D. (1995). Multiple subpial transection: a review of 21 cases. J Neurol Neurosurg Psychiatry, 58, 344-9. Shinnar, S., I. Rapin, S. Arnold, R. F. Tuchman, L. Shulman, K. Ballaban-Gil, et al. (2001). Language regression in childhood. Pediatr Neurol, 24, 183-9. Sobel, D. F., M. Aung, H. Otsubo and M. C. Smith (2000). Magnetoencephalography in children with Landau-Kleffner syndrome and acquired epileptic aphasia. AJNR Am J Neuroradiol, 21, 301-7. Szabo, C. A., E. Wyllie, M. Dolske, L. D. Stanford, P. Kotagal and Y. G. Comair (1999). Epilepsy surgery in children with pervasive developmental disorder. Pediatr Neurol, 20, 349-53.

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Tsuru, T., M. Mori, M. Mizuguchi and M. Y. Momoi (2000). Effects of high-dose intravenous corticosteroid therapy in Landau-Kleffner syndrome. Pediatr Neurol, 22, 145-7. Tuchman, R. F. (1997). Acquired epileptiform aphasia. Semin Pediatr Neurol, 4, 93-101. Tuchman, R. F. and I. Rapin (1997). Regression in pervasive developmental disorders: seizures and epileptiform electroencephalogram correlates. Pediatrics, 99, 560-6. Tuchman, R. F. and I. Rapin (2002). Epilepsy in autism. Lancet Neurol, 1, 352-8. Tuchman, R. F., I. Rapin and S. Shinnar (1991a). Autistic and dysphasic children. I: Clinical characteristics. Pediatrics, 88, 1211-8. Tuchman, R. F., I. Rapin and S. Shinnar (1991b). Autistic and dysphasic children. II: Epilepsy. Pediatrics, 88,1219-25. Veggiotti, P., F. Beccaria, R. Guerrini, G. Capovilla and G. Lanzi (1999). Continuous spikeand-wave activity during slow-wave sleep: syndrome or EEG pattern? Epilepsia, 40, 1593-601. Veggiotti, P., S. Bova, E. Granocchio, G. Papalia, C. Termine and G. Lanzi (2001). Acquired epileptic frontal syndrome as long-term outcome in two children with CSWS. Neurophysiol Clin, 31, 387-97. Wilson, S., A. Djukic, S. Shinnar, C. Dharmani and I. Rapin (2003). Clinical characteristics of language regression in children. Dev Med Child Neurol, 45, 508-14. Yung, A. W., Y. D. Park, M. J. Cohen and T. N. Garrison (2000). Cognitive and behavioral problems in children with centrotemporal spikes. Pediatr Neurol, 23, 391-5.

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Persistent Language and Learning Deficits in AEOS

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PERSISTENT SUBTLE LANGUAGE AND LEARNING DEFICITS IN A CHILD WITH ACQUIRED EPILEPTIFORM OPERCULAR SYNDROME (AEOS) Paola Cipriani, Anna M. Chilosi,Claudia Casalini, Lucia Pfanner, Annarita Ferrari, Daniela Brizzolara and Renzo Guerrini "Stella Maris " Scientific Institute, Pisa, Italy University of Pisa, Italy

Abstract — Persistent linguistic deficits are sometimes observed after prolonged anarthric status epilepticus, even in the absence of structural abnormalities of the perisylvian cortex, leading some authors to interpret Acquired Epileptiform Opercular Syndrome (AEOS) as an expressive variant of Landau-Kleffner syndrome. The long-term outcome of children with AEOS is rarely reported, and no systematic neurolinguistic studies have been carried out with the aim of analysing the effects of abnormal articulatory experience on phonological coding in the course of language development. We report on a child who was followed at our department from age 5 years to age 8 years for a fluctuating clinical syndrome consisting of recurrent episodes of severe oral motor dysfunction, dysarthria and drooling paralleled with focal EEG abnormalities that fluctuated in phase with the clinical disorder. At follow-up, persistent subtle language and learning difficulties due to impaired phonological processing skills were observed, in spite of a good response to antiepileptic drugs, improved EEG, normal MRI and adequate nonverbal cognitive abilities. Keywords: Operculum syndrome, epilepsy, acquired speech and language dysfunction, phonological processing deficits.

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Neurogenic Language Disorders in Children

INTRODUCTION Opercular Syndrome (OS), also called Foix-Chavanny Marie Syndrome (FCMS) (Foix et al., 1926) results from a structural or functional abnormality in the opercular or perisylvian areas and is clinically manifested by anarthria/severe dysarthria and loss of voluntary muscular functions of the face and tongue as well as impaired mastication and swallowing. These symptoms result from a central disturbance of the volitional control of the facio-linguoglosso-pharingeal-masticatory muscles, with preserved automatic, involuntary and emotional innervation (automatic-voluntary dissociation). It has a variable etiology, which may be due to congenital or acquired bilateral damage of the perisylvian cortex (Christen et al, 2000; Salas-Puig et al, 2000; Gordon, 2002). Rarely does OS have an epileptic origin (Fejerman & Di Blasi, 1987; Roulet et al, 1989; Colamaria et al, 1991; Deonna et al, 1993; Shafrir & Prensky, 1995; De Saint-Martin et al, 1999; Galanopoulou et al, 2000; Shuper et al, 2000; Kramer et al, 2001; Tachikawa et al, 2001). In these cases, the underlying mechanisms are not fully understood as there is no clear link between the epileptic activity and the clinical manifestations. The term "Acquired Epileptiform Opercular Syndrome" (AEOS) was first used by Shafrir and Prensky in 1995 to describe a 5-year-old girl who developed recurrent prolonged episodes of suprabulbar palsy in association with continuous spike-and-wave activity during slow sleep. These authors interpreted the AEOS as an expressive variant of Landau-Kleffner syndrome (LKS). AEOS and LKS would represent neurological disorders, sharing similar pathophysiological mechanisms, in which long-standing electrical dysfunction of perisylvian neurons translates into bilateral neurological dysfunction. AEOS manifests with fluctuating signs of suprabulbar palsy resulting from a disruption of the connections between the cortical motor areas and the brainstem nuclei. The symptoms (identical to those attributed to bilateral structural abnormalities of the perisylvian cortex) show an intermittent course, with widely variable onset, duration and relapse. Persistent linguistic deficits are sometimes described (Deonna et al, 1993; De Saint-Martin et al, 1999; Kramer et al, 2001) after prolonged anarthric status epilepticus, but the long-term outcome of children with AEOS is rarely reported, and no systematic neurolinguistic studies have been carried out. We describe a longitudinal study of a child with functional, epilepsy-related oralmotor dysfunction who developed long-lasting oral and written language deficits.

CASE REPORT This Italian right-handed male child patient was born after an uneventful pregnancy, delivery and neonatal period and had a history of normal motor, cognitive and language development. At the age of 5 years and 3 months he had his first seizure while falling asleep with twitching of the right eyelid, corner of the mouth and right arm, lasting one minute, followed by an

Persistent Language and Learning Deficits in AEOS

39

inability to speak for about 10 minutes.The following day he was admitted to our Department: He was alert and fully conscious; the main clinical features included pharyngeal, lingual and masticatory motor deficits, drooling of saliva, and severely impaired speech initiation. A video EEG showed almost continuous, high-voltage, bilateral centro-temporal synchronous and asynchronous spikes and sharp and slow waves, more prominent on the left (Figure 1). The child was severely dysarthric but responsive and able to follow commands.

Figure 1 — EEG at admission: almost continuous, high-voltage, bilateral centro-temporal synchronous and asynchronous spikes and sharp and slow waves, more prominent on the left.

Figure 2 — EEG performed 3 minutes after an intravenous administration of diazepam (5mg): marked improvement in the EEG; a slow subcontinuous activity, 2-3 Hz, persisted on the left centro-parietal areas.

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Neurogenic Language Disorders in Children

Language testing, performed during the EEG recording, revealed a severe difficulty in naming familiar objects and pictures and an inability to reproduce simple oral gestures on imitation. Morphosyntactic comprehension as tested by TCGB, a multiple-choice test of receptive grammar, (Chilosi & Cipriani, 1995), was also impaired. Intravenous diazepam abated EEG discharges; a slow subcontinuous activity (2-3 Hz) persisted on the centro-parietal areas with concomitant clinical improvement (Figure 2). The child began to name objects and pictures and made some volitional orolingual movements on request (sticking out the tongue, clicking the tongue to imitate the sound of a horse galloping). Magnetic Resonance Imaging (MRI) was normal. Treatment with sodium valproate was started and no other acute episodes of oral motor dysfunction and speech arrest occurred. The child was followed at our clinic from the post-acute phase up to the age of 8 years and 7 months. Follow-up EEGs showed normal background activity and frequent sharpwave complexes, synchronous and asynchronous on both centro-temporo-parietal regions, dramatically enhanced during sleep. In spite of these severe abnormalities, no overt clinical symptoms or changes in speech fluency were demonstrated during the EEG recording. At 5 years and 9 months and 6 years and 4 months he suffered two right-sided focal motor seizures upon falling asleep. Various combinations of drugs (sodium valproate, clonazepam, hydrocortisone, ethosuximide) only produced transient improvement on EEG paralleled by improvement of language performance. Three years after the initial symptoms, the child was seizure-free under sodium valproate, but the EEG was persistently abnormal.

LANGUAGE AND NEUROPSYCHOLOGICAL FOLLOW-UP The child's neurological status, oromotor functions, language, speech and cognitive abilities were repeatedly evaluated from 5.3 up to 8.7 years of age. The first full language and cognitive assessment was performed a few days after the acute episode. Expressive language was grammatically correct but simplified, slow and nonfluent; on a picture naming test (Brizzolara et ai, 1994), global performance was within normal limits, but it was characterised by an excessively high latency of response and by an abnormally high number of anomias, as a consequence of word retrieval deficits. The child's language comprehension was within the norms for his age (Chilosi & Cipriani, 1995). Cognitive assessment revealed a mild deficit of nonverbal (Leiter International Performance Scale, LIPS) (Leiter, 1979) and visuo-motor integration abilities (VMI, Beery, 1997) and a severe impairment of verbal short-erm memory (Digit span) (Orsini et al., 1987) and phonological working memory (recall of lists of words in the auditory-visual modality). The child's subsequent course was relatively benign, though marked by some inconsistencies in cognitive and language functioning, parallel with improvements and

Persistent Language and Learning Deficits in AEOS

41

relapses of the electroclinical conditions. The main clinical features, as summarised in Table 1 and graphically represented in Figures 3-7 are as follows: fluctuating levels of performance on nonverbal tasks (visuo-motor integration skills and performance IQ) improvements and relapses of grammatical comprehension phonological processing deficits, manifested by an impaired performance on working memory and phonemic fluency tasks slow rate of articulation and mild oral dyspraxia word-retrieval difficulties with a variable preponderance of anomias and paraphasic speech manifesting as hesitations, circumlocutions, "conduites d'approche", and/or phonemic and semantic substitutions. Table 1 — Summary of clinical, neuropsychological and EEG data from 5.3 years to 6.4 years 5.3 (acute phase)

SPEECH AND LANGUAGE

5.5

5.7

++

++

5.11 +++

6.4

EEG abnormalities

++++

Partial motor seizures

Y

N

N

N

Y

Y

+++

++

+

+

+

++

+

+

Oral motor dysfunction

COGNITIVE SKILLS

5.3 (post acute phase) ++

Dysarthria Anomias Grammatical comprehension Phonemic fluency Semantic fluency Phonological Working memory Nonverbal IQ VMI (standard score) Digit span (percentile)

ft

ft +++

+++

+++

+++

impaired

normal

ft

+++

ft ++

+

ft

ft

+++

+++

normal

normal

++

ft normal

++ impaired

n.a. n.a.

impaired impaired

impaired impaired impaired impaired impaired borderline borderline borderline

n.a.

impaired

impaired borderline borderline impaired

n.a.

67

99

67

94

92

n.a.

72

85

77

79

83

n.a.

2°

2°

22°

9°

9°

Note: U = better; 0 = worse; Y= yes; N = no; n.a. = not available ++++ = very severe; +++ = severe; ++ = moderate; += mild

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Neurogenic Language Disorders in Children

Figure 3 — Neuropsychological follow-up: non verbal abilities: Performance IQ (PIQ) and Visuomotor integration skills (VMI Standard score).

Figure 4 — Neuropsychological follow-up: Grammatical Comprehension.

Figure 5 — Neuropsychological follow-up: Phonological Working Memory (auditory-visual modality).

Persistent Language and Learning Deficits in AEOS

43

Figure 6 — Neuropsychological follow-up: Verbal fluency.

Figure 1 — Neuropsychological follow-up: Lexical production (types of errors).

LONG-TERM OUTCOME When last seen, at the age of 8 years and 7 months (three years after the onset of the AEOS), the child was attending the 3rd grade of primary school. The EEG showed frequent sharp-wave complexes that were synchronous and asynchronous on both centro-temporo-parietal regions which became almost continuous during sleep, but the child was seizure-free. Upon examination, some residual signs of orofacial clumsiness and verbal dyspraxia were observed with a persistently very slow rate of speech and some prosodic alteration. Nonverbal cognitive abilities (PM47, Raven, 1956, 1984; Pruneti et al, 1996; VMI, Beery, 1997) and receptive vocabulary (Peabody Picture Vocabulary Test, PPVT, Dunn & Dunn, 1981; Stella et al, 2000) were within average range, whereas performance on morpho-syntactic comprehension, naming and phonological processing tasks was below the norms (Table 2). A

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Neurogenic Language Disorders in Children

formal assessment of literacy skills by means of standardized tests of reading and spelling (Martini, 1995; Sartori et al, 1995) revealed a severe learning disability. Reading performance was significantly impaired both for speed and accuracy. The child could read and write only disyllabic words, making use of a prevalent letter by letter strategy and manifested severe difficulties to find out the meaning of even single words. Writing to dictation was also severely impaired (Table 2).

Table 2 — Summary of residual deficits NON VERBAL ABILITIES VMI (standard score)

PM47 (percentile)

77

30°

LANGUAGE Expressive vocabulary Receptive grammar Naming test (z-score) TCGB (z-score) - ,4 102 -2.5 PHONOLOGICAL PROCESSINC Phonological Working Memory Verbal fluency (z-scores) (z-scores) Long words Phonemic Semantic Short words -2,2 -1,6 -0,9 -1,5 ACADEMIC SKILLS Writing Reading (z-scores) (single words) Speed Accuracy (z-scores) Short Letters Words Long Short words Long words -1,95 > -5 > -5 > -5 > -5 > -5 Receptive vocabulary PPVT (standard score)

DISCUSSION

This child sustained a severe functional, epilepsy-related disorder, with sudden onset of suprabulbar palsy and focal seizures. The course of epilepsy was rather favourable (despite persistent EEG abnormalities), but he was left with mild verbal dyspraxia, some expressive language difficulties and a severe disorder of reading and writing. Some other rare cases of AEOS with long-lasting high-level language deficits have occasionally been described in the literature. Deonna et al.'s case 2 (1993) was reported to have difficulty with written language (mainly severe dysorthography) and dysfluent speech. Patient 1 in the Kramer et al. 's series (2001) showed word-retrieving difficulties on a formal language test, whereas patient 3 (in the

Persistent Language and Learning Deficits in AEOS

45

same series) had poor reading skills. In the authors' opinion, the above symptoms should not be influenced by a sensorimotor deficit and represent a "higher function deficit" whose significance is unclear. In a recent review of the opercular epilepsies with oromotor dysfunction, Salas-Puig et al. (2000) pointed out that some children with perisylvian developmental disorders (bilateral opercular malformations) may present with a quite homogeneous language dysfunction that cannot be accounted for by a speech paretic disorder and by oral dyspraxia (as in the classic form of FCMS), but should imply involvement of language areas, though to a variable degree. At present, the pathophysiology of central processing disorders in AEOS rests on speculative grounds (Fejerman et al, 2000). We may hypothesise that the spreading of abnormal electrical brain activity to adjacent regions of the frontal cortex subserving phonologically-based linguistic processes would interfere with higher neurofunctional language mechanisms that sustain coding and rehearsal of phonological and lexical information. This hypothesis would also explain reading and writing difficulties, by assuming the presence of a central impairment in the acquisition of rapid and automatized rules for recoding oral language knowledge into its written form. From a neurolinguistic point of view, the relationship between AEOS and oral/verbal dyspraxia, has not been systematically addressed in the literature. This may be due, at least in part, to the following facts. First, in some papers on functional or structural Opercular Syndrome (OS), the terms dyspraxia and dysarthria have been used interchangeably, although the paretic origin of typical suprabulbar palsy is well recognised since Worster - Drought's (1974) influential work. In our patient, both paretic and praxic defects of the facio-lingualglosso-pharingeal muscles were variably present during different stages of the illness. Second, as described above, rare cases of AEOS with persisting subtle oral and written language deficits have been reported, but few explanatory hypotheses have been proposed. Third, the pathophysiology of acquired apraxia of speech in adults and of developmental apraxia of speech (DAS) in children is very controversial. The debate concerns both the nature of the disorder - in terms of a movement or a language disturbance (Robin, 1992) - and the specific brain site responsible for it. Some suggestions for speculating on the localization of DAS arise from different and sparse sources drawn from adult patients with acquired lesions and from children with both congenital and acquired speech disorders (Habib & Demonet, 1996; Vargha-Khadem et al, 1998; Van Mourik et al, 1997). However, an involvement of perirolandic cortex in the adjacency of the inferior motor strip (dedicated to the innervation of lips, tongue and glosso- pharyngeal muscles) and of the 'pars opercularis' of Broca's area has been advocated as the most likely candidate region by several authors (Alexander et al, 1990; Foundas et al, 1998). In addition, based on data from stroke patients with apraxia of speech, Dronkers (1996) identified the precentral gyrus of the insula as the brain region co-ordinating speech articulation. A functional impairment of these regions may result from epileptic activity involving them either primarily, or as a result of a spreading effect from contiguous areas. However, confirmation of this hypothesis would need sophisticated electrophysiological and neurofunctional studies, through two-dimensional topographical EEG mapping and coherence/spectrum analysis, and fMRI exploration of brain

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Neurogenic Language Disorders in Children

regions of interest. In conclusion, the long-lasting, praxic and language deficits in AEOS might be related as suggested for some permanent sequelae in Landau-Kleffner Syndrome (LKS) - to a disruption of normal synaptic connectivity in the perisylvian cortex during a sensitive stage of its development. Similarly to LKS, the effects of epileptogenic discharges on neuronal networks subserving language would 'activate and perpetuate synaptic arrangements that are functionally inappropriate' (Morrell et al, 1995).

REFERENCES Alexander, M. P., M. A. Naeser and C. Palumbo (1990), Broca's area aphasias: Aphasia after lesions including the frontal operculum. Neurology, 40, 353-362. Beery K.E. (1997) VMI. Developmental test of visual-motor integration, 4th Edition, Revised. Toronto: Modern Curriculum Press. Brizzolara, D., P. Cipriani, A. M. Chilosi and L. De Pasquale (1994). L'apprendimento del linguaggio scritto nei bambini con difficolta di acquisizione del linguaggio orale: continuita o discontinuity? In: Apprendimento e patologia neuropsichica nei primi anni di scuola. Modelli interpretativi della clinica (G. Masi and A. Martini, editors), pp. 124-135. Borla, Roma. Chilosi, A. and P. Cipriani (1995). Test di comprensione grammaticale per bambini (TCGB). Del Cerro, Tirrenia. Christen, H. J., F. Hanefeld, E. Kruse, S. Imhauser, J. P. Ernst and M. Finkenstaedt (2000). Foix-Chavany-Marie (anterior operculum) syndrome in childhood: a reappraisal of Worster-Drought syndrome. Dev Med Child Neurol, 42, 122-32. Colamaria, V., V. Sgro, R. Caraballo, M. Simeone, E. Zullini, E. Fontana, R. Zanetti, R. Grimau-Merino and B. Dalla Bernardina (1991). Status epilepticus in benign rolandic epilepsy manifesting as anterior operculum syndrome. Epilepsia, 32, 329-334. De Saint-Martin, A., C. Petiau, R. Massa, R. Maquet, C. Marescaux, E. Hirsch and M. N. Metz-Lutz (1999). Idiopathic rolandic epilepsy with "interictal" facial myoclonia and oromotor deficit: A longitudinal EEG and PET study. Epilepsia, 40, 614-620. Deonna, T. W., E. Roulet, D. Fontan and J. P. Marcoz (1993). Speech and oromotor deficits of epileptic origin in benign partial epilepsy of childhood with rolandic spikes (BPERS). Neuropediatrics, 24, 83-87. Dronkers, N. G. (1996). A new brain region for coordinating speech articulation. Nature, 384, 159-61. Dunn, L. and L. M. Dunn (1981). Peabody Picture Vocabulary Test - Revised. American Guidance Service, Circle Pines, MN. Fejerman, N. and M. Di Blasi (1987). Status epilepticus of benign partial epilepsies in children: report of two cases. Epilepsia, 28, 351-355.

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Fejerman, N., R. Caraballo, S. N. Tenembaum (2000). Atypical evolutions of benign localization-related epilepsies in children: Are they predictable? Epilepsia, 41, 380390. Foix, C, J. A. Chavany and J. Marie (1926). Diplegie facio-linguo-masticatrice d'origine cortico-sous-corticale sans paralysies des membres. Rev Neurol, 33, 214-219. Foundas, A. L., K. F. Eure, L. F. Luevano and D. R. Weinberger (1998). MRI asymmetries of Broca's area: The pars triangularis and pars opercularis. Brain Lang, 64, 282-296. Galanopoulou, A. S., A. Bojko, F. Lado and S. L. Moshe (2000). The spectrum of neuropsychiatric abnormalities associated with electrical status epilepticus in sleep. Brain Dev, 22, 279-295. Gordon, N. (2002) Worster-Drought and congenital bilateral perisylvian syndromes. Dev Med Child Neurol 44, 201-204. Habib, M., J.-F. Demonet (1996). Cognitive neuroanatomy of language: the contribution of functional neuroimaging, Aphasiology, 10, 217-234 Kramer, U., B. Ben-Zeev, S. Harel and S. Kivity (2001).Transient oromotor deficits in children with benign childhood epilepsy with central temporal spikes. Epilepsia, 42, 616-620. Leiter, R.G. (1979). Letter International Performance Scale. Stoelting Co, Chicago. Martini, A. (1995). Le difficolta di apprendimento della lingua scritta. Criteri di diagnosi e indirizzi di trattamento. Del Cerro, Tirrenia. Morrell, F., W. W. Whisler, M. C. Smith, J. H. Thomas, L. de Toledo-Morrell, S. J. C. PierreLouis, et al. (1995). Landau-Kleffner syndrome: Treatment with subpial intracortical transection. Brain, 118, 1529-1546. Orsini, A., D. Grossi, E. Capitani, M. Laiacona, C. Papagno and G. Vallar (1987). Verbal and spatial immediate memory span: normative data from 1355 adults and 1112 children. Ital J Neurol Sci, 8, 539-548. Pruned, C, A. Fenu, G. Freschi, S. Rota, D. Cocci, M. Marchionni, S. Rossi and G. Baracchini Muratorio (1996). Aggiornamento della standardizzazione italiana del test della Matrici Progressive Colorate di Raven (CPM). Bollettino di Psicologia Applicata, 217,51-57. Raven, J. C. (1956) Guide to using the Coloured Progressive Matrices, sets A, AB and B. London: H.K. Lewis. Italian version (1984): Progressivi matrici colore. Serie A, AB, B. Firenze: Organizzazioni Speciali. Robin, D. A. (1992). Developmental apraxia of speech. Am J Speech Lang Pathol, 1, 9-22. Roulet, E., T. Deonna and P. A. Despland (1989). Prolongued intermittent drooling and oromotor apraxia in benign chilhood epilepsy with centrotemporal spikes. Epilepsia, 30(5), 564-568. Salas-Puig, J., A. Perez-Jimenez, P. Thomas, I. E. Scheffer, B. Dalla Bemardina and R. Guerrini (2000). Opercular epilepsies with oromotor dysfunction. In: Epilepsy and Movement Disorders (R. Guerrini, J. Aicardi, F. Andermann and M. Hallet, editors), pp. 251-268. Cambridge University Press, Cambridge.

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Sartori, G., R. Job and P.E. Tressoldi (1995). Batteria per la valutazione della dislessia e delta disortografia evolutiva. Organizzazioni Speciali, Firenze. Shafrir, Y. and A. L. Prensky (1995). Acquired epileptiform opercular syndrome: a second case report, review of the literature, and comparison to the Landau-Kleffner syndrome. Epilepsia,36, 1050-1057. Shuper, A., B. Stahl and M. Mimouni (2000). Transient opercular syndrome: a manifestation of uncontrolled epileptic activity. Ada Neurol Scand, 101, 335-338. Stella, G., C. Pizzoli, P. E. Tressoldi (2000). Peabody. Test di Vocabolario Recettivo. Omega Edizioni, Torino. Tachikawa, E., H. Oguni, S. Shirakawa, M. Funatsuka, K. Hayashi and M. Osawa (2001). Acquired epileptiform opercular syndrome: a case report and results of single photon emission computed tomography and computer-assisted electroencephalographic analysis. Brain Dev, 23, 246-250. van Mourik, M., C. E. Catsman-Berrevoets, H. R. van Dongen and B.G.R. Neville (1997). Complex orofacial movements and the disappearance of cerebellar mutism: Report of five cases. Dev Med Child Neurol, 39, 686-690. Vargha-Kadem, F., K. Watkins, C. J. Price, J. Ashburner, K. J. Alcock, A. Connelly, et al. (1998) Neural basis of an inherited speech and language disorder. Proc Nat Acad Sci, 95, 12695-12700. Worster-Drought, C. (1974). Soprabulbar Paresis. Congenital suprabulbar paresis and its differential diagnosis, with special reference to acquired suprabulbar paresis. Dev Med Child Neurol, 16, 1-33.

Brain Language Lateralization and Focal Lesions

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5

CEREBRAL LANGUAGE LATERALIZATION AND EARLY LINGUISTIC DEVELOPMENT IN CHILDREN WITH FOCAL BRAIN LESIONS Anna M. Chilosi, Chiara Pecini, Paola Cipriani, Daniela Brizzolara, Paola Brovedani, Giovanni Ferretti, Lucia Pfanner and Giovanni Cioni "Stella Maris " Scientific Institute, Pisa, Italy

Abstract — We conducted a longitudinal study of 20 children with unilateral focal brain lesions and hemiplegia, 11 with left (LHD) and 9 with right hemisphere damage (RHD) to investigate the relationship between lesion characteristics, early linguistic development and hemisphere lateralization for language. Cerebral lateralization for language was measured by means of the Fused Dichotic Words Test. Two comprehensive assessments of language comprehension and production were performed at about 2 and 4 years of age. An early left side-specificity for language was revealed by the presence of lexical and grammatical delay in the majority of LHD children. In 90% of LHD children, plasticity and the potential for re-organization were documented by a shift in lateralization for language to the right hemisphere on the dichotic listening test. There was an association, irrespective of side, between the largest lesions, the most atypical hemispheric asymmetries (as expressed by laterality coefficients) and delay in grammatical development. Lesion type seemed to significantly affect hemispheric lateralisation and short-term language outcome, cortico-subcortical lesions being significantly associated with a greater degree of lateralization and language delay in comparison to periventricular white matter lesions. The presence of EEG abnormalities and/or seizures negatively affected language outcome. Keywords: language development, focal lesions, hemispheric lateralization, Fused Dichotic Words Test.

50

Neurogenic Language Disorders in Children

INTRODUCTION Several studies report that early brain lesions have relatively mild consequences on language development in comparison to lesions acquired later in adulthood, and do not necessarily show a clear-cut association to side, site or size of lesion (Vargha-Khadem el al, 1985; Vargha-Khadem et al, 1992; Muter et al., 1997; Reilly et al., 1998). These data have been interpreted in relation to the concepts of 'plasticity' and 'equipotentiality' of the immature brain: while plasticity refers to the compensatory mechanisms underlying lesion-induced neurofunctional and behavioural reorganisation, equipotentiality refers to the analogous capacity of the two hemispheres to sub-serve language functions after unilateral brain damage (Lenneberg, 1967). This theory has been challenged by several studies which support the existence of an early specialisation of the left hemisphere for language acquisition, although the differential effect of left and right lesions seems to depend on the specific stage of language development. In fact, Bates et al. (1997) found that in the period from 10 to 17 months of age, children with a right lesion were at a greater risk for delays in word comprehension and gesture production than children with left hemisphere damage (LHD), and in the period from 10 to 44 months children with a lesion involving the left temporal lobe showed significantly greater delay in expressive vocabulary and grammar (see also Thai et al., 1991; Vicari et al, 2000; Chilosi et al, 2001). However, the effect of a left temporal damage on grammar development was no longer detected past 5-6 years of age (Reilly et al, 1998). These data on the linguistic development of LHD children suggest that 'equipotentiality' and early 'left hemisphere specialisation' may represent the two poles of a continuum: the left hemisphere may be innately predisposed to language learning and processing, but this predisposition is sufficiently plastic for the non-dominant hemisphere to successfully acquire and mediate language in conditions such as early focal brain damage (Vicari et al, 2000; Chilosi etal, 2001; Satzefa/., 1990). More recently, the plasticity of the immature brain and the concept of equipotentiality of the two hemispheres was supported by new neuroimaging evidence which found a right hemisphere specialization for language after early damage to the left language areas (Miiller et al, 1999; Lazar et al, 2000). According to these studies, the reorganization for language in the right hemisphere involves regions which are mostly homotopic to the language areas in the left hemisphere of healthy right-handers, thus suggesting a 'near-equipotentiality' of the two hemispheres also at a topological level (Staudt et al, 2002). However, it is still too early to draw general conclusions from functional neuroimaging studies, as there are in fact two main methodological limitations: a) normative data from healthy children are still scarce, and b) most of the data are collected on patients with early-onset and severe epilepsy who are candidates for neurosurgery. The issue of how language reorganises after early focal damage has been traditionally addressed by behavioural techniques, such as the dichotic listening paradigm. The use of a behavioural paradigm allows for the study of larger samples of patients and is especially

Brain Language Lateralization and Focal Lesions

51

appropriate for investigating language lateralisation in very young children in comparison to neuroimaging methods. In the dichotic listening paradigm two competing verbal stimuli are presented simultaneously to the two ears. According to Kimura's structural model (Kimura, 1961, 1967), in this condition, controlateral auditory pathways occlude the ipsilateral pathways. This leads to a better processing of the stimuli presented to the right ear (REA, right ear advantage) as they have more direct and faster access to the language-dominant left hemisphere than the stimuli presented to the left ear, which are in fact assumed to access first the right hemisphere and then the left through the corpus callosum (for a review, see Bryden, 1981). Dichotic techniques were employed to investigate whether language reorganization after an early lesion occurs inter- or intrahemispherically in relation to the characteristics of the lesion (Brizzolara et al., 2002). The presence of epileptic activity is another factor that may in itself alter the pattern of lateralization. Piccirilli et al. (1988), using a verbal-manual dual task, found that in children with benign focal epilepsy with no documented lesion, a left unilateral epileptogenic focus was associated with a bilateral representation of language processing. Riva et al. (1993) compared the performance of epileptic children with unilateral foci and the presence or absence of CT documented lesions on a verbal-spatial tachistoscopic task and found that cerebral lateralisation was altered similarly in both groups. On the basis of these findings they suggested that epilepsy alone can change the pattern of lateralisation for verbal information processing. More recently, Isaacs et al. (1996) addressed the issue of the effect of seizure disorder on language lateralisation in hemiplegic children. On a dichotic listening task using digits, left lesioned children with a history of clinical seizures displayed a stronger LEA than left lesioned children without seizures, probably because of a more limited potential for language processing in the hemisphere where the epileptic focus was active. In a previous study conducted in our laboratory (Brizzolara et al., 2002), we investigated cerebral lateralization for language by means of the Fused Dichotic Words Test (Wexler & Halwes, 1985) in 26 hemiplegic children with congenital focal brain damage with the specific aim to investigate the relation between lesion characteristics (side, size and localisation) on MRI and the pattern of language lateralisation on the dichotic test. We found significant side and site effects at group level: while children with right lesions showed the expected right ear advantage (REA), in children with left hemisphere lesions there was a left ear advantage (LEA). An analysis of individual data, however, revealed that type of lesion (e.g., corticosubcortical versus periventricular) occurring at term or pre-term respectively, may be the primary factor responsible for inter- vs. intrahemispheric organisation of language after congenital brain lesions. Only when the left lesions involved cortico-subcortical regions encroaching the temporal lobe and occurred at term, language was reorganised in the right hemisphere; when lesions (whether left or right) involved only the periventricular white matter and occurred at pre-term, language was lateralised in the left hemisphere. However, the relationship between lesion localisation, re-organisation of language and functional effect on language development is still an open issue.

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Neurogenic Language Disorders in Children

On the basis of these considerations, the aim of the present study was twofold: a) to analyse the course of linguistic development in relation to different lesions characteristics; b) to investigate whether there is a relation between the degree of functional specialisation for language, expressed by LEA and REA values on the dichotic test, and the timing and trajectory of linguistic development. We addressed these issues by examining language development and reorganisation from the third to the fourth year of age in a sample of children with pre- or perinatal focal brain damage.

SUBJECTS Subjects were selected from a larger population of patients with congenital focal brain lesions referred to the Division of Child Neurology and Psychiatry of the University of Pisa on the basis of the following criteria: unilateral focal brain lesions, occurring pre- or peri-natally, documented on the basis of clinical records and MRI absence of diffuse or progressive lesions or brain malformations comprehensive longitudinal linguistic assessment with at least 2 evaluations between the age of about 2 and 4 years, with an interval between the two consecutive observations of at least 8 months absence of mental retardation (Developmental Quotient > 80) at the time of the first evaluation absence of treatment- resistant epilepsy at the two evaluation time points absence of auditory deficits and personality disorders. MRI assessment Brain MRI studies were performed under sedation using a 1.5 T system (GE, Signa Advantage); images were obtained in the axial, coronal and sagittal planes with sections of 5 mm. When multiple scans were available, the most recent one was considered. MRI findings were classified retrospectively by one of the authors (GC), blind to the results of linguistic and cognitive assessment, according to the most recent indications in the literature about neuroimaging findings in congenital hemiplegia (Tailairach & Tournoux, 1988; Barkovitch, 1995; Cioni et al, 1999). Results are reported in Table 2. Lesions were classified according to three different criteria: Side and site of lesion. Patients were assigned either to the "right" or "left" unilateral lesion group. Moreover, cerebral lobes involved in the lesion and the encroachment of language areas (frontal and temporal lobes) were recorded.

Brain Language Later•alization and Focal Lesions

53

Size of lesion. Lesion size was classified by a grading system adapted (with modifications) from Vargha-Khadem et al. (1985). It consists of a six-point scale, ranging from 0 to 5, providing an index of lateral ventricular dilatation and of the extension of encephaloclastic cysts; score 5 indicates the most severe abnormality. This scale is presented in papers previously published by the authors (Vicari et al, 2000; Chilosi et al, 2001). Type of lesion. Both the pathophysiological mechanisms of the lesion and its probable timing were taken into account. Two types of lesions were observed: 1) Periventricular white matter lesions (PV), likely due to parenchymal haemorrhages (results of venous infarction or of haemorrhagic periventricular leukomalacia) or to periventricular leukomalacia. These lesions usually occur either intra or extra utero (in case of preterm birth) in the last trimester of gestation. Unilateral encephaloclastic cysts, merged into a dilated ventricle, are often observed on MRI at older ages. In the other cases, lesions consist of symmetrical or asymmetrical periventricular gliosis. 2) Cortico-subcortical (C-SC-PV) lesions, due to an infarction of a main cerebral artery (generally main branch or cortical branch of middle artery), involving the cortex, the white matter below the cortex and often the periventricular white matter. Sometimes, the lesion concerns the deepest branches (exclusively or in association with other lesions) involving diencephalic structures. These lesions usually occur at around term age. Electrophysiological assessment EEGs were obtained for all patients, the majority of whom receiving repeated recordings. EEG tracings closest to the time of linguistic and psychological observations were analysed and results were classified according to the nature of the abnormality (diffuse, focal, paroxysmal), its frequency and the condition during which it occurred (wakefulness, sleep, other types of activation). Findings were scored as normal, mildly abnormal or severely abnormal. The occurrence of clinical seizures with onset beyond the neonatal period and excluding febrile convulsions were documented. Linguistic assessment Language evaluation was performed through a combination of indirect procedures (parental interview to collect information on productive vocabulary size) and direct observations to evaluate the level of expressive and receptive grammar. The latter were based on free-speech samples and on a test of Early Verbal Comprehension (Chilosi et al, 2003). Expressive vocabulary was tested by means of the Infant's and Toddler's MacArthur Communication Developmental Inventories (Italian version: // Primo Vocabolario del Bambino - PVB) (1995), for which normative data are available in the 8-30 months age range. Because many of the children in our focal lesion sample were delayed in language development, assignment of the Infant's or Toddler's form was based on language level rather

54

Neurogenic Language Disorders in Children

than on chronological age. The analyses presented here will focus on productive vocabulary from both forms and will be expressed by total number words and by a lexical quotient (LQ) corresponding to the ratio between lexical age (i.e., the age at which a particular score corresponds to the median in the normative sample) and chronological age. Expressive grammar was evaluated on the basis of language samples collected in our laboratory during a standardised play situation involving the child and his/her parents. Speech was transcribed independently by one of the authors (L.P.) and by a trained research assistant (inter-observer agreement reached 90%). The utterances were then coded according to the Child Language Exchange System (CHILDES) (Mac Whinney & Snow, 1985). For each child the level of grammatical development was scored on a six-level rating system (see Table 1) developed by Cipriani et al. (1993), ranging from Level 0 (pre-linguistic stage) to Level 5 (complex grammar). Verbal comprehension was investigated by an acting-out task that has been standardised on a sample of Italian children. It includes 20 simple verbal commands of increasing complexity that the child is required to act out with a set of toys or familiar objects. For each child, a z-score was obtained on the basis of normative data from 6 groups of normal children aged 16-36 months (Chilosi et al, 2003). Table 1 Levels of grammatical development Level

Expressive language

Level 0

Level 4

Babble, sounds, gestures and sporadic single word utterances (SW) Single-word utterances (SWU) start to be consistently produced Emergence of combinatorial speech, but SWU prevail Ungrammatical or telegraphic multiword utterances (MWU) Fully grammatical simple sentences

Level 5

Fully grammatical complex sentences

Level 1 Level 2 Level 3

Dichotic Listening paradigm The Fused Dichotic Words Listening Test (Wexler and Halwes, 1985) (consisting of pairs of rhyming words) was used since it has been shown to be a more valid measure of cerebral lateralisation than non-fused versions (Zatorre, 1989). Fifty-five high frequency two-syllable words were used (Marconi et al., 1994), 28 CVCV and 27 CVCCV. The stimuli were recorded in Digital Audio Tape mode in a noise-protected room and sampled by a digital SoundBlaster Hard-Disk-Recording for PC. Sampling cared that words forming the dichotic pair were synchronised for the beginning of the first consonant, for length and for some

Brain Language Lateralization and Focal Lesions

55

internal features (especially where the accent fell). Stimuli were presented by a specific program running on a PC. The experiment consisted in the dichotic presentation of 30 pairs of fused words: twenty-five pairs differed for the first consonant (e.g., cane-pane) and 5 pairs differed for the first vowel (e.g., luna-lana). Word pairs were presented twice to all subjects; in the second session the assignment of stimuli to ears was reversed. The order of presentation of the word pairs was fixed across subjects and varied across sessions. Overall, each subject heard 60 stimuli in each ear through headphones (Sony Professional MDR-V50). Children were instructed to repeat all the words they heard, after each presentation. The raw data were then converted to a laterality coefficient (Lambda) according to the procedure proposed by Bryden and Sprott (1981). It consists of the natural logarithm of the number of correct responses for the words heard by the right ear plus 1, divided by the number of correct responses for the words heard by the left ear plus 1 (Ln[(Right+l)/(Left +1)]). A positive value is indicative of REA, reflecting a left hemisphere superiority for language processing. Conversely, a negative value indicates a LEA, reflecting a right hemisphere superiority. Mean laterality coefficient values, obtained on a large sample of normal children aged 4-10 years, ranged from 0.32 to 0.54 and were stable across ages (Brizzolara et ah, 2000). In the present study the dichotic test was administered as soon as children were able to cooperate reliably, with mean chronological age of 5 years and 4 months. RESULTS Clinical and MRI characteristics According to the selection criteria, a total of 20 children (13 males and 7 females) participated in the study, 11 with LHD and 9 with RHD. Mean chronological age at the first evaluation time point (77) was 23.5 months (SD 3.0, range 16-29) for LHD children and 21.8 months (SD 5.1, range 17-32) for RHD children. At 77, mean age for LHD children was 38.3 months (SD 1.6, range 36-42) and 39.2 months (SD 3.6, range 35-44) for RHD children. The mean interval between 77 and T2 was 14.8 months for LHD children (range: 9-23) and 17.4 months for RHD children (range: 8-26). Neither age at the two time-points nor the T1-T2 interval significantly differed between the two groups (t-test). Table 2 shows the sample characteristics, time of brain injury (hypothesized on the basis of medical history and neuroradiological data), MRI findings, presence or absence of epilepsy, EEG findings and age at the two evaluation time points. Nineteen children had a documented hemiplegia of differing degree of severity. Four had epilepsy that was well controlled by mono- or polytherapy at the time of the study. Fourteen children had C-SC-PV lesions, 5 had PV lesions and only one child had a SC-PV lesion. The mean size of the lesions (grade) was 3.8, with a range between 1 and 5. Sixteen children had EEG abnormalities that were mildly abnormal in 10 and severely abnormal in 6. Four of the latter had clinical seizures at the time of the study, whereas two cases (cases 6 and 14) presented with epilepsy within two years from T2.

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Neurogenic Language Disorders in Children

Table 2 - Clinical and neuroradiological characteristics of the sample Case/

GA

Time of

Gender

(Wk)

lesion

MRI findings Site

1/M

42

term

Side L

Extention C,SC,

Age

Age

atTl

atT2

(mo)

(mo)

EEG

Epilepsy

findings

Lobes FTP

Size 4

23

37

N

MA

sc,

FTP

4

23

38

Y

SA

sc,

PTF

4

24

37

N

MA

sc,

PO

4

25

38

Y

SA

sc,

FTPO

5

24

39

Y

SA

sc,

TPO

4

16

39

Y

SA

sc,

PTF

4

23

36

N

MA

FP

3

24

38

N

N

sc,

TPF

5

24

42

N

MA

sc,

FTP

5

29

38

N

MA

PV 2/F

39

term

L

c, PV

3/M

38

term

L

c, PV

4/F

39

pre-term

L

c, PV

5/M

40

term

L

c, PV

6/M

38

term

L

c,

7/M

41

term

L

c,

PV PV 8/F

40

pre-term

L

PV

9/M

39

term

L

c, PV

10/M

42

term

L

c, PV

11/M

41

pre-term

L

PV

PF

5

24

40

N

N

12/M

38

pre-term

R

SC, ]PV

FPT

3

20

35

N

SA

13/F

34

pre-term

R

C

sc,

FPT

4

24

40

Y

MA

sc,

PFT

4

19

44

Y

SA

sc,

FTPO

5

17

32

N

MA

sc,

FTP

4

26

40

N

MA

PV 14/M

39

term

R

c, PV

15/M

40

term

R

c, PV

16/F

40

term

R

c, PV

17/M

40

pre-term

R

PV

FTP

1

22

42

N

N

18/F

40

pre-term

R

PV

PT

3

32

40

N

MA

19/M

39

term

R

c,

T

4

21

39

N

MA

P

1

15

41

N

N

sc,

PV 20/F

34

pre-term

R

PV

Note: GA = gestational age; Wk = weeks; Mo = months; R = right, L = left, C = Cortical; SC = subcortical; PV = Periventricular; F = Frontal; P = Parietal; T = Temporal; O = Occipital; N = Normal; MA = Mild abnormalities; SA = Severe abnormalities.

Brain Language Lateralization and Focal Lesions

57

A preliminary analysis was conducted to verify whether LHD and RHD groups differed for clinical and MRI characteristics: Lesion type: there was a slightly higher incidence of cortico- subcortical lesions in LHD than in RHD children but the difference was not significant (chi-square); Lesion size: LHD children showed a tendency to have larger lesions than RHD children, however this difference was not significant (chi-square); Lesion site: 18 children had a lesion encroaching temporal and/or frontal lobes, without significant differences between left and right lesions. EEG findings: EEG abnormalities were associated with lesion type, with a higher incidence of mild and severe abnormalities in C-SC-PV than in PV lesions (chi square = 11.7, p = 0.005); no significant associations were found with lesion side and size. Language development The mean number of words produced by the whole sample at Tl was 66.6 (SD = 102.7, range = 2-403). This corresponds to a mean age of 16.5 months and to a lexical quotient (LQ) of 78.7. At T2 the mean vocabulary raw score was 413 (SD = 218.9, range = 26 - 660; mean increase from Tl to T2 = 346.5 words) corresponding to a mean age of 29.8 months and an LQ of 77.9. The mean z-score for language comprehension at Tl was in the low average range (z = -0.9), but 70% of LHD and 37.5% of RHD children scored more than one standard deviation below the norm, showing a varying degree of delay. Table 3 shows the performance of LHD and RHD children on linguistic tests. Table 3 — Language performances of left (LHD) and right (RHD) damage children at Tl and T2 (means and standard deviations) Language assessment Vocabulary

LHD RHD

Tl T2 Tl T2

N words Mean sd 27.9 (26.7) 360.7 (192.6) 109.8 (137) 485.2 (244)

Lexical Quotient Mean sd 63 (25.7) 70.9 (15.8) 89.1 (19.1) 86.5 (17.5)

Expressive Grammar Level * 1 4 1.7 4.5

Language Comprehension Z score Mean sd -1.4 (0.8) -0.9 (0.9) -0.2 (1.1) 0.09 (0.5)

Note: * median value LHD = Left hemisphere damage; RHD = Right hemisphere damage; N words = number of words. At T2, language comprehension improved in both groups (mean z score = -0.36) with only 2 LHD children and 1 RHD child showing a persistent delay. The anova analysis revealed a significant effect of lesion side on LQ (F(l, 18) = 7.94, p < 0.01) and on verbal

58

Neurogenic Language Disorders in Children

comprehension (F(l,12) = 18.87, p < 0.001), with a lower performance in the LHD group versus the RHD group; the absence of a significant interaction between lesion side and time of evaluation indicated that this difference was stable from Tl to T2. The level of expressive grammar of the whole sample varied widely at Tl, ranging from a pre-linguistic to an early grammatical phase of development. However, while all LHD children were delayed and did not produce any word combination (level 0 or 1), only two children in the RHD group had not yet reached the level of combinatorial speech (chi square(l) = 8.14, p < 0.005). The disadvantage of LHD children was still present at T2, as 9 out of 11 showed a persistent delay in grammatical development in comparison to the 2 RHD children who maintained their delay (chi square (1) = 4.8, p < 0.05). To further analyze the effects of different variables on lexical and grammatical development, short-term language outcome at T2 was rated according to the following criteria: age-appropriate language outcome (LQ > 80; expressive grammar level >4) and delayed language outcome (LQ < 80, expressive grammar level <4). Significantly more LHD than RHD children showed a delay both in vocabulary (chi square(l) = 5.15, p < 0.05) and grammar (chi square(l) = 4.8, p < 0.05). Grammatical, but not lexical outcome, was also affected by lesion type and size: in children with PV lesions grammatical outcome was more frequently age-appropriate than in children with C-SC-PV lesions (chi square(l) = 6.7, p < 0.01); in children with lesion size greater than 3, grammatical outcome was more frequently delayed in comparison to children with smaller lesions (chi square(l) = 4.4, p < 0.05). A non-parametric correlation analysis (Spearman) between EEG findings (normal, mild and severe abnormalities) and linguistic measures produced a negative correlation with language comprehension (rho = -0.43, p < 0.05) and expressive grammar level (rho = -0.38, p <0.05)atT2butnotatTl. Hemispheric lateralization A t-test on Lambda values at the dichotic test revealed a significant difference between LHD and RHD groups (t(18) = -9.28, p < 0.001), with the former showing a left ear advantage and the latter a right ear advantage (Figure 1). A correlational analysis (Pearson) on the whole sample revealed that Lambda values significantly correlated with Tl and T2 LQs (Tl, r = 0.43, p < 0.05; T2, r = 0.43, p < 0.05) and language comprehension ( Tl, r = 0.44, p < 0.05; T2, r = 0.44, p < 0.05). Subjects were divided into two groups on the basis of Lambda coefficient values: normal and atypical (falling more than ± 2 SDs from the mean of the normative sample; Brizzolara et al., 2000). Atypical values were significantly associated with delayed grammatical outcome (chi square(l)= 7.5, p < 0.01). The Lambda absolute value, which reflects the magnitude of hemispheric lateralisation, varied according to lesion type, with C-SC-PV lesions showing a higher degree of lateralisation than PV lesions (t(18) = 2.3, p < 0.05). This result was confirmed by the analysis of the individual Lambda values: regardless of lesion side, 93% of the 14 children with C-SC-PV lesions had an atypical lateralisation, while only 34% of the

Brain Language Lateralization and Focal Lesions

59

children with a lesion confined to the periventricular white matter were in the atypical range. The Lambda absolute value also significantly correlated with lesion size (rho = 0.47, p < 0.05,) with larger lesions being associated with greater Lambda values. No significant correlations were found between EEG findings and Lambda values.

Figure 1—Mean Lambda values in the LHD and RHD groups and in normal children

DISCUSSION In the present longitudinal study, we investigated the relationship between unilateral focal lesion characteristics, early linguistic development and hemispheric lateralisation for language. The main results consisted in an atypical degree of hemispheric lateralization of language in both left and right damaged children that was significantly associated with lexical and grammatical delay in the short-run. We also found an early left side-specificity for language, although a functional shift and reorganization of language in the right hemisphere occurred in most LHD children, due to the plasticity of the developing brain. Side-specificity was revealed by the presence of lexical and grammatical delay in the majority of LHD children. On the second evaluation, 8 LHD children were still lagging behind in the acquisition of vocabulary and 9 of them showed a delay in grammar, while only 2 RHD children presented with a delay in both vocabulary and grammar. Left hemisphere damage was also associated with an initial delay in verbal comprehension, while right injuries mostly appeared to be associated with a sparing of receptive skills, at least within the timewidow considered in the present study. Plasticity and the potential for reorganisation and recovery were documented by the pattern of lateralisation for language on the dichotic listening test. As expected, 90% of LHD children presented a shift for language processing to the right hemisphere, while RHD children showed a left hemisphere lateralisation. Apart from lesion side, the rate and mode of language development appeared to be influenced by other factors (alone or in combination) such as lesion size and type, and the presence of EEG abnormalities and/or seizures.

60

Neurogenic Language Disorders in Children

Lesion size was significantly correlated with grammatical outcome and with the degree of lateralisation, although there were no statistically significant differences between left and right-sided lesions. Moreover, there was an association, irrespective of side, between the largest lesions and the most atypical hemispheric asymmetries, confirming previous evidence obtained by our group (Brizzolara et al, 2002). Interestingly, atypical Lambda values were significantly associated with a delay in grammatical development. This association was present in all left damaged children who had an atypical Lambda, but only in 1 out of 5 RHD children with Lambda values in the atypical range. This may suggest that the right hemisphere, which takes over language after left cortico-subcortical lesions, cannot completely accomplish the task of learning grammar, at least at the stage when transition from primitive combinatorial speech to grammaticisation occurs in normal development. Lesion type was another variable that significantly affected hemisphere lateralization: CSC-PV lesions showed a greater degree of lateralisation than PV lesions, independently of the side of damage: 13 out of 14 patients with C-SC-PV lesions showed an atypical Lambda in comparison with only 1 out of 6 children with periventricular white matter lesions. Type of lesion also seemed to influence language outcome as the only two LHD children with an ageappropriate language development had a periventricular lesion. In two of our focal brain damaged children later onset of epilepsy was preceded by severe EEG abnormalities earlier in life. As outlined by several authors (Sussova et al, 1990; Claeys et al, 1983; Vargha-Khadem et al, 1992), electrical abnormalities in areas surrounding the lesion may limit the potential for neurofunctional substitution on the part of undamaged areas. In conclusion, our results suggest that, in spite of the side-specificity of brain circuitries dedicated to language, compensatory processes are at work from an early age, probably because of the activation of substitution mechanisms on the part of uncommitted areas of the right hemisphere, as revealed by the atypical lateralisation coefficients. The linguistic profile and the hemisphere lateralization for language in the LHD group could be interpreted as the consequence of re-allocation of language to alternative regions of the brain under the influence of different gradients of vulnerability and the asymmetrical maturation timing of the two hemispheres. According to the so-called 'maturation gradient hypothesis' proposed by Corballis and Morgan (1978), the more rapid rate of development of the left hemisphere would force a shift of verbal functions to homologous areas of the right hemisphere. However, our longitudinal study also demonstrates that neural reorganisation has some costs. In fact, the slow language development of our left-lesioned children suggests that reallocation of language functions in alternative regions of the brain and/or the emergence of substitution strategies for language is an extended process that goes on well beyond the normal age expectation. From a clinical perspective, it must be pointed out that the high degree of variability of developmental profiles in focal brain damaged children may make it impossible to predict the long-term outcome. Our data suggest that the risk of a negative short-term language outcome is represented, on the one hand, by the presence of a left cortico-subcortical hemispheric lesion, which is strongly associated with atypical cerebral lateralization, and on the other, by

Brain Language Lateralization and Focal Lesions

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severe EEG abnormalities and/or seizures which worsen language outcome both in left and right focal brain damage.

REFERENCES Barkovitch, A. J. (1995). Pediatric neuroimaging, 2nd Edition. Raven Press, New York. Bates, E., D. Thai, D. Trauner, J. Fenson, D. Aram, J. Eisele and R. Nass (1997). From first words to grammar in children with focal brain injury. Dev Neuropsychol, 13, 275-343. Brizzolara, D., P. Brovedani, G. Cioni, P. Cipriani, G. Ferretti and C. Pecini (2000). A comparison of two different dichotic tests for the assessment of language lateralization in children. Proceedings ofXXVll International Congress of Psychology. Stockholm, 23-28 July 2000, p.422. Brizzolara, D., C. Pecini, P. Brovedani, G. Ferretti, P. Cipriani and G. Cioni (2002). Timing and type of congenital brain lesion determine different patterns of language lateralization in hemiplegic children. Neuropsychologia, 40, 620-32. Bryden, M. P. and D. A. Sprott (1981). Statistical determination of degree of laterality. Neuropsychologia, 19, 571-81. Caselli, M. C. and P. Casadio (1995). // Primo Vocabolario del Bambino. Franco Angeli, Milano. Chilosi, A., P. Cipriani, B. Bertuccelli, L. Pfanner and G. Cioni (2001). Early cognitive and communication development in children with focal brain lesions. J Child Neurol, 16, 309-316. Chilosi A.M., Cipriani P., Pfanner L., Villani S. (2003). La valutazione della comprensione verbale nella prima infanzia: dati normativi e indici predittivi nei ritardi di acquisizione del linguaggio. Progetto di Ricerca CNR002D39-004. Technical report. Cioni, G., B. Sales, P. B. Paolicelli, E. Petacchi, M. F. Scusa and R. Canapicchi (1999). MRI and clinical characteristics of children with hemiplegic cerebral palsy. Neuropediatrics, 30, 249-255. Cipriani, P., A. M. Chilosi, P. Bottari and L. Pfanner (1993). L'acquisizione della morfosintassi in Italiano: Fasi e Processi. Unipress, Padova. Claeys, V., T. Deonna and R. Chrzanowski (1983). Congenital hemiparesis: the spectrum of lesions: A clinical and computerized tomographic study of 37 cases. Helv Paediatr Ada, 38, 439-455. Corballis, M. and M. Morgan (1978). On the biological basis of human laterality: Evidence for a matuartional left-right gradient. Behav Brain Sci, 1, 261-268. Isaacs, E., D. Christie, F. Vargha-Khadem and M. Mishkin (1996). Effects of hemispheric side of injury, age at injury, and presence of seizure disorder on functional ear and hand asymmetries in hemiplegic children. Neuropsychologia, 34, 127-37. Kimura, D. (1961). Cerebral dominance and the perception of verbal stimuli. Can J Psychol, 15, 166-71.

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Kimura, D. (1967). Functional asymmetry of the brain in dichotic listening. Cortex, 3, 163-78. Lazar, R. M., R. S. Marshall, J. Pile-Spellman, H. C. Duong, J. P. Mohr, W. L. Young, R. L. Solomon, G. M. Perera and R. L. DeLaPaz (2000). Interhemispheric transfer of language in patients with left frontal cerebral arteriovenous malformation. Neuropsychologia, 38, 1325-1332. Lenneberg, E. H. (1967). Biological foundations of language. Wiley, New York. Mac Whinney, B. and C. Snow (1985). The Child Language Data Exchange System. J Child Lang, 12,271-296. Marconi, L., M. Ott, E. Pesenti, D. Ratti and M. Tavella (1994). Lessico elementare: dati statistici suH'italiano scritto e letto dai bambini delle elementari. Zanichelli, Bologna. Miiller, R.-A., R. D. Rothermel, M. E. Behen, O. Muzik, P. K. Chakraborty and H. T. Chugani (1999). Language organization in patients with early and late left-hemisphere lesion: a PET study. Neuropsychologia, 37, 545-57. Muter, V., S. Taylor and F. Vargha-Khadem (1997). A longitudinal study of early intellectual development in hemiplegic children. Neuropsychologia, 35, 289-298. Piccirilli, M., P. D'Alessandro, C. Tiacci and A. Ferroni (1988). Language lateralization in children with benign partial epilepsy. Epilepsia, 29, 19-25. Reilly, J. S., E. Bates and V. A. Marchman (1998). Narrative discourse in children with early focal brain injury. Brain Lang, 61, 335-375. Riva, D., C. Pantaleoni, N. Milani and C. Giorgi (1993). Hemispheric specialization in children with unilateral epileptic focus, with and without computed tomographydemonstrated lesion. Epilepsia, 34, 69-73. Satz, P., E. Strauss and H. Whitaker (1990). The ontogeny of hemispheric specialisation: Some old hypotheses revisited. Brain Lang, 38, 596-614. Staudt, M., K. Lidzba, W. Grodd, D. Wildgruber, M. Erb and I. Krageloh-Mann (2002). Right-hemispheric organization of language following early left-sided brain lesions: functional MRI topography. Neuroimage, 16, 954-67. Sussova, J., Z. Seidl and J. Faber (1990). Hemiparetic forms of cerebral palsy in relation to epilepsy and mental retardation. Dev Med Child Neurol, 32, 792-795. Tailairach, J. and P. Tournoux (1988). A stereotactic coplanar atlas of the human brain. Thieme Med Pub, New York. Thai, D., V. Marchman, J. Stiles, D. Aram, D. Trauner, R. Nass and E. Bates (1991). Early lexical development in children with focal brain injury. Brain Lang, 40, 491-527. Vargha-Khadem, F., E. Isaacs, S. van der Werf, S. Robb and J. Wilson (1992). Development of intelligence and memory in children with hemiplegic cerebral palsy. Brain, 115, 315-329. Vargha-Khadem, F., A. O'Gorman and G. Watters (1985). Aphasia and handedness in relation to hemispheric side, age at injury and severity of cerebral lesion during childhood. Brain, 108, 677-96.

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Vicari, S., A. Albertoni, A. M. Chilosi, P. Cipriani, G. Cioni and E. Bates (2000). Plasticity and reorganization during language development in children with early brain injury. Cortex, 36, 31-36. Wexler, B. E. and T. Halwes (1985). Dichotic listening tests in studying brain-behavior relationships. Neuropsychologia, 23, 545-59. Zatorre, R. J. (1989). Perceptual asymmetry on the dichotic fused words test and cerebral speech lateralization determined by the carotid sodium amytal test. Neuropsychologia, 27, 1207-19.

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Language Disorders and EEG Abnormalities During NREM Sleep

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6

LANGUAGE DISORDERS ASSOCIATED WITH PAROXYSMAL ABNORMALITIES DURING NREM SLEEP AFTER VERY EARLY BRAIN LESIONS Franco Fabbro, Alessandro Tavano, Guido Cristofori and Renalo Borgalti "E.Medea " Scientific Institute, Polo del Friuli Venezia Giulia and Bosisio Parini (LC), Italy University of Udine, Italy

Abstract - We investigated the role of paroxysmal abnormalities in NREM sleep in children with early brain lesions and language disorders. The presence of epilepsy has been often associated to an unfavorable prognosis for cognitive and language development in children with early brain lesions. We assessed language development in six children with pre- or perinatal brain lesions and marked language disorders by focusing on the following variables: 1) site and side of lesion; 2) presence of epilepsy; 3) presence of paroxysmal abnormalities in NREM sleep; 4) presence of a clinical picture of epilepsy and language regression. Cases 1, 2 and 3 presented with many epileptic episodes. The remaining three cases showed language disorders in the absence of seizures and antiepileptic therapy. In all cases, we found a high percentage of epileptiform abnormalities in NREM sleep. Cases I, 2 and 3 present with a clinical picture of acquired aphasia associated to epilepsy in the presence of a neurological lesion (Landau-Kleffner Syndrome-Like). Results confirm the unfavorable prognosis of the association of early brain lesion, epilepsy and Landau-Kleffner Syndrome for linguistic and cognitive development. The association between language disorders and/or language regression in children with early brain lesions and paroxysmal abnormalities in NREM sleep is highlighted. Our study points out the need to constantly monitor the sleep EEG of children with an early brain injury, since the presence of a relevant paroxysmal activity in sleep - even in the absence of epilepsy - seems to be correlated to poor language development. Key words: early brain lesion, congenital aphasia, developmental dysphasia, NREM sleep, paroxysmal abnormalities, Landau-Kleffner Syndrome.

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Neurogenic Language Disorders in Children

INTRODUCTION The incidence of cerebral palsy of perinatal origin is approximately two in 1000 births. Of these cerebral palsy cases approximately one-third have hemiplegia. The hemispheric brain injury responsible for hemiplegia is believed to be due to a thrombotic, vasospasmic or embolic episode occurring in the middle cerebral and/or internal carotid artery territories. The etiology of the circulatory event is not yet well understood. It is believed to occur at some time between the end of the second trimester of pregnancy and the early postnatal period. Between 30% and 40% of such hemiplegic cases develop a cerebral seizure disorder (Brett, 1992). As documented by many studies, the neuropsychological sequelae of early brain damage are relatively mild if compared with those of adults. The degree of sparing or recovery of language and other cognitive functions seems to depend on several factors such as: 1) time of injury, 2) side of lesion, 3) size of lesion; 4) presence of epilepsy and/or role of anticonvulsant therapy. Time of injury. Often, in adults strokes in the left hemisphere do not only lead to hemiplegia but also to impairments in different aspects of language and/or other cognitive functions. Similarly, hemiplegia following right hemisphere strokes in adults is often accompanied by impairments in attentional, visuo-spatial and pragmatic functions (Cytowic, 1996). Contrary to adults, the language deficits observed in children with early left-hemisphere injury are far less pronounced than aphasic syndromes in adults (Lenneberg, 1967; Van Hout, 2000). Reports of childhood aphasia with favorable and expedient language recovery often mention the presence of lasting deficits in academic performance (e.g., reading and writing). These findings suggest the presence of residual deficits in language ability (Aram & Eisele, 1992). Numerous studies on the effects of early brain lesions have evidenced that the worst time for injury in the human brain is likely to be the third trimester of pregnancy. Side of lesion. Numerous studies have been carried out to verify the effects of early left hemisphere damage (LHD) versus right hemisphere damage (RHD) on language development. Vargha-Khadem et al. (1992) explored the effects of early brain lesions on the intellectual development of 82 children with hemiplegic cerebral palsy (42 with LHD and 40 with RHD) compared to a control group. If children with cerebral palsy and epilepsy (30 participants, 14 with LHD and 16 with RHD) were excluded, there were no differences in intellectual development between control children and children with cerebral palsy. Within this group, no significant differences were found in VIQ across control children (C-VIQ = 104.3), LHD children (L-VIQ= 101.3) and RHD children (R-VIQ= 103.4). In contrast, children with cerebral palsy (both the LHD and RHD groups) showed a similar, yet significantly lower, PIQ than control children (C-PIQ= 109.6; L-PIQ=98.6; R-PIQ= 97.9). Bates et al. (1999a) discussed the performances of 76 children - presented in previously published studies - with pre- or perinatal stroke (46 LHD and 30 RHD) tested between 3 and 14 years of age. Mean full-scale IQs were in the normal range. There were absolutely no

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differences between LHD and RHD children in full-scale, verbal or nonverbal IQ. The Italian sample (18 children with LHD and 15 RHD) received several language tests (Peabody Picture Vocabulary Test, Boston Naming Test, Token Test, Test of Receptive Grammar, Semantic Category Fluency Test). The brain-injured children performed significantly worse than normal controls on all language measures. However, no difference was found between LHD and RHD on any measure. Furthermore, when mental age was controlled for in analyses of covariance, the differences between brain-injured children and normal controls disappeared, except for a measure of lexical access (Boston Naming Test). In another study, Bates et al. (1999b) studied some characteristics of language production (word types, word tokens, mean length of utterance, grammatical complexity and word errors) based on samples of free speech, in a group of 38 brain-injured children (24 LHD and 14 RHD) aged 5-8 years, compared to 38 age- and gender-matched normal controls. There were no differences between LHD and RHD children on any measure. There were also very few differences between braininjured children (combining LHD and RHD) and controls. More recently, Chilosi et al. (2001) systematically investigated cognitive development and language abilities in a group of 18 children younger than 4 years with focal brain lesions (9 with LHD and 9 with RHD). Their findings differ from those of other recent studies (Bates et al. 1999a, b; Vicari et al, 2000) in that they suggest that children with LHD may have greater difficulties in vocabulary and grammar acquisition. However, the different results obtained by these studies may be attributed to age-related differences across samples. Size of lesion. According to Lashley's mass action effect (1929), large lesions are related to more severe cognitive deficits. However, several studies did not find a strong relationship between lesion size and language-cognitive outcome (Aram & Eisele 1992; Eisele & Aram 1994; Chilosi et al. 2001). Animal experiments suggest that small lesions have little effect because they are small; mid-size lesions are large enough to cause permanent behavioral impairments, but not large enough to enable the brain to re-organize. Compared to small or medium lesions, large lesions result in a better outcome because participants make a "fresh start" (Me, 1990). Presence of epilepsy. There have been reports which demonstrate that seizures accompanying early brain injury are associated with poorer language and cognitive outcome (Van Dongen & Loonen, 1977). Vargha-Khadem et al. (1992) showed that a history of seizures is the most important predictor of cognitive and language impairments in brain-injured children, regardless of side or size of injury or age of insult. In their study, children with cerebral palsy (LHD and RHD) and epilepsy presented with a significantly lower cognitive development than control children and children with cerebral palsy but without epilepsy. Cognitive impairment in children with cerebral palsy and epilepsy affected both verbal and performance skills. According to Chilosi et al. (2001) seizures are the single greatest risk factor for language and cognitive outcome in children with unilateral damage. Chilosi et al. (2001) suggested that the detrimental effect of epilepsy on the potential for recovery and

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development can be probably interpreted as the consequence of a more diffuse neurological dysfunction. In contrast, according to Vargha-Khadem et al. (1992) it is possible that anticonvulsant drug therapy administered to all the children with epilepsy rather than seizures per se may be responsible for these impairments. In the present study we looked at language development in six children with pre- perinatal brain lesions associated to important language deficits. We investigated the role of some classical neurological variables in language development: 1) site and side of the lesion and 2) presence of epilepsy. Further, we looked at the possible role of some factors whose relevance has not been sufficiently explored in the literature, namely 3) the presence of a "LandauKleffner Syndrome-Like" and 4) the presence of epileptiform abnormalities in non-REM (NREM) sleep.

METHODS Participants We selected six participants (three boys and three girls) who suffered an early brain damage before the end of their first year of life after a pregnancy without persistent problems. In all the participants lesions were localized to specific brain structures on the basis of neuroimaging procedures. Case 1 had suffered from bacterial meningitis with lesions localized to the caudate nuclei bilaterally. Case 2 showed a single unilateral focal ischemic lesion. Case 3 presented with a malformation syndrome affecting the cerebellum. The remaining three patients (Cases 4-6) had a single unilateral focal ischemic lesion (cf. Table 1). Neuropsychological assessment Patients were administered the following standard neuropsychological tests: Standard Progressive Matrices (Raven, 1954), WPPSI (Wechsler, 1973), WISC-R (Wechsler, 1986), Stanford- Binet, L-M (1968), Leitner-R (Roid & Miller, 2002), NEPSY battery (Korkman et al. 1998). Praxic abilities were evaluated by a standardized test for the evaluation of oro-facial praxis in children (Bearzotti & Fabbro, in press). Language assessment Parents of children aged 1-3 years received the Mac Arthur Questionnaire (Caselli & Casadio, 1990). Children aged 2-3 years were administered the Test del Primo Linguaggio battery (TPL, First Language Test) (Axia, 1995). Children aged 3-6 years received the Test di Valutazione del Linguaggio battery (TVL, Language Assessment Test) (Cianchetti & Fancello, 1996) or the Esame del Linguaggio dai 4 ai 12 anni battery (4-12, Language examination for children aged 4-12) (Fabbro, 1999). Children older than 12 years were

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administered the Italian adaptation of the Bilingual Aphasia Test (BAT, Paradis, 1987). A qualitative analysis of verbal expression was made according to Fabbro & Frau (2001). Table 1 — Participants' characteristics and clinical data. Case G HP

A

Lesion Site

1,MD F

LH

10

2, GM F

RH

10

Left caudate nucleus bilaterally Left upper parietal region

3, RP M RH 24 4, LS F

LH

7

5, LP M RH

4

6, GM M RH

3

Right cerebellar hemisphere Left fronto-temporal parietal Thalamus and deep white matter bilaterally Left frontal corticosubcortical region

VIQ PIQ FIQ

Convulsive episodes* 3rd day 8 years 7 years 9 years

79

76

75

70

91

77

54

81

66

7-12 years

92

89

90

6 years

106

-

100

2nd day

Therapy Valproate sodium Lamotrigine; valproate sodium; ACTH one cycle Carbamazepine Valproate sodium

No

Note: G= gender; HP =hand preference; A= age at most recent assessment; VIQ=verbal intelligence quotient; PIQ=performance intelligence quotient; FIQ= full-scale intelligence quotient; *= age at onset.

CASE HISTORIES Case 1 (MD) MD is a left-handed girl aged 10 years and four months. Pregnancy was uneventful and she was born at term (birth weight: 3.4 kg). On her third day of life she had meningitis owing to group B beta-hemolytic streptococcus complicated by a convulsive seizure (upper limb and mimic muscle spasms). She was under phenobarbital for a month. At 1 month of life, a brain CT scan revealed a linear ischemic lesion lateral to the frontal horn and the head of the left caudate nucleus. She achieved independent walking at 10 months of age and uttered her first words when she was 12 months old. At 5 years of age she started attending our residential kindergarten owing to emotional problems, attention difficulties and phonological deficits. On that occasion, a mild left hemiparesis was noted, mainly affecting the lower limb. A recent MRI scan evidenced the presence of lesions affecting the head of the caudate nucleus

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bilaterally (cf. Figure 1).

Figure 1 — MRI. Lesions affecting the head of the caudate nucleus bilaterally (gross areas of signal hyperintensity in T2). Possible outcome of inflammatory pathology. At 6 years of age she underwent a systematic neurological and neuropsychological evaluation. The EEG in wakefulness and NREM sleep showed a 8-9 Hz fundamental reactive rhythm with normal morphology. In light sleep conditions spike/slow wave sequences were found, recorded by bicentral derivations (cf. Figure 2).

Figure 2 — EEG. Diffusion of intraclinical paroxysmal abnormalities to both hemispheres in sleep stage 2 (ca. 50%). Paroxysmal abnormalities diffuse from the right hemisphere to the contralateral anterior regions.

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On several occasions, other left parietal paroxysmal abnormalities were found. Cognitive development was in the low normal range (VIQ= 78; PIQ= 73; FIQ= 73). On the 4 - 1 2 language battery (Fabbro, 1999) she performed 2 SDs below the norm on syntactic and grammatical comprehension tasks, naming, sentence repetition and semantic fluency. Speech was fragmentary and little contextual. On the neuropsychological evaluation with the NEPSY battery (Korkman el al. 1998), which allows an in-depth analysis of executive, sensorimotor, visuoperceptual and mnestic functions, she performed 1 SD below the mean on tests targeting attention and executive functions, and 2 SDs below the mean on tests targeting sensorimotor, visuo-spatial and memory functions. Neuropsychological rehabilitation and speech therapy were started. As her response to treatment was insufficient and paroxysmal anomalies in sleep persisted until she was 7 years old, she was started on valproate sodium (400 mg/day). Five months thereafter her EEG tracing had considerably improved. However, right focal temporal paroxysmal abnormalities were found. After a few months of therapy, her language abilities had improved. At the age of 8 years, when she received a new language assessment, her performance on grammatical comprehension and sentence repetition was still 2 SDs below the norm. Her expression was fragmented and characterized by pragmatic deficits. Her intellectual development was in the low normal range (VIQ = 79; PIQ = 76; FIQ = 75) (cf. Table 1).

Table 2 — EEG abnormalities and type of language deficits.

Case

Wa E

EEG

NREM sleep EEG

anguage Regression

Language deficits

Paroxysmal activity > 50% NREM sleep

One episode at 8 years of age

Receptive and expressive morphosyntax.

Two episodes at 7 and 9 years of age Between 7 and 12 years

Expressive morphosyntax, pragmatics. Transcortical motor aphasia.

No episodes

Receptive and expressive morphosyntax. Anomias.

1, MD

Normal

2, GM

Spike waves

3, RP

Spike-waves

4, LS

Spike-waves

Diffuse paroxysmal activity Diffuse paroxysmal . . , \ activity before 14 years Subcontinuous paroxysmal activity >

5, LP

Normal

Paroxysmal activity

No episodes

Verbal dyspraxia

6, GM

Normal

Paroxysmal activity

No episodes

Receptive and expressive morphosyntax.

At 8 years and 10 months she had a critical episode with loss of consciousness and right eye lateroversion, followed by an aggravation of language deficits. As her clinical picture which was typical of Landau-Kleffner Syndrome - with aphasic regression, seizures,

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paroxysmal EEG during NREM sleep - was associated to a documented neurological lesion, we defined it Landau-Kleffner Syndrome-Like. Ethosuximide was introduced to keep seizures under control. The sleep EEG still revealed focal paroxysmal abnormalities in the right frontal region, with mainly homolateral diffusion. Administration of the NEPSY battery showed a clear aggravation of memory skills compared to the previous evaluation (from 67% correct to 54%). On the language examination her language deficits had worsened. She performed 2 SDs below the norm on the following tasks: verbal discrimination, syntactic comprehension, grammatical comprehension, sentence repetition and semantic fluency (cf. Table 2). Case 2 (GM) GM is a right-handed girl aged 10 years and 8 months. Pregnancy was uneventful with normal delivery (low birth weight: 2.4 kg). At 10 days of life she suffered an episode of low platelet count, with bruises on her face, neck and trunk. At 1 year of life a left hemisyndrome was observed. This neurological picture was attributed to perinatal brain suffering. The child received kinesitherapy and speech therapy to improve her motor skills and pragmatic problems - poor relationships with adults and peers - as well as phonological and lexical deficits. At 4 years of age her IQ was in the normal range (WIPPSI: VIQ= 87; PIQ= 95; FIQ= 90). Her speech was little intelligible and she still had relational difficulties with adults. At 6 years and a half her intellectual development had improved (WISC-R: VIQ= 96; PIQ= 100; FIQ= 97). She showed semantic and grammatical comprehension deficits, phonological deficits, reading and writing disabilities. First episode ofLKS. At 7 years and a half she suffered two generalized tonic-clonic seizures. The EEG in wakefulness evidenced spike-wave paroxysmal activity in the fronto-temporal region bilaterally, mainly prevalent on the left. She received carbamazepine (300 mg/day). Progressively the child started to show language regression: her pragmatic problems aggravated and she had difficulties in establishing relationships with others, and avoided eye contact. Her speech was unintelligible. She uttered single words, with many anomias and perseverations. To communicate, she resorted to pointing or drawing. She read very slowly. On the WISC-R she showed increased difficulties (VIQ= 87; PIQ= 83; FIQ= 83). Her clinical picture, which was typical of Landau-Kleffner Syndrome - aphasic regression, seizures, paroxysmal EEG during NREM sleep - was associated to a documented neurological lesion. Thus, we defined it Landau-Kleffner Syndrome-Like. Slowly she showed a progressive language recovery. She was started on Lamotrigine (125 mg/day). At the age of 8.06 years she underwent another neurological examination. MRI imaging and CT scan evidenced an egg-like formation, 2.5 cm in diameter, in the left parietal region near the vertex and the midline (possible outcome of prenatal lesion) (see Figure 3).

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Figure 3 — MRI. Egg-like lesion due to an arachnoidal cyst possibly localized in the left upper parietal region, with likely areas of cortical dysplasia (coronal section, T2).

An EEG in wakefulness evidenced a symmetric and reactive 10 Hz background rhythm. On the frontal areas, isolated spikes and waves were noted, mainly prevalent on the left. Focal paroxysmal abnormalities were found (triphasic spikes followed by slow waves) in the right centro-temporal region throughout all sleep stages. Epileptiform abnormalities were repetitive and more numerous in NREM sleep (see Figure 4).

Figure 4 — EEG: Left centro-parietal paroxysmal slow focus in wakefulness and drowsiness, with immediate diffusion and generalization of paroxysms upon falling asleep.

Second episode of LKS. At the age of 9 years and a half seizures during sleep appeared again

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(eye opening, mouth clonic spasms, scialorrhea, clonic spasms of the lower limbs) with abrupt language regression. Her verbal comprehension was minimal and spontaneous speech was absent. Only upon request did she produce single words. An important regression in IQ was noted (WISC-R: VIQ= 70; PIQ= 91; FIQ= 77) (cf. Table 1). On the EEG in wakefulness the spike-slow wave complexes were more marked in the left anterior areas. This activity was not modified in sleep. ACTH therapy was started (Synacthen Depot 1, 1 via IM) with administration of 6 doses. Valproate sodium (600 mg/day) was introduced in the AE therapy. Progressively she showed language recovery. On the 4-12 language battery (Fabbro, 1999), she showed full recovery of sentence repetition and fluency. Verbal fluency, MLU and Type/Token Ratio of descriptive speech were age-appropriate. Omissions of free grammatical morphemes and phonemic paraphasias were still present (cf. The Bird Nest Story Picture Description Task; Paradis, 1987) (cf. Table 2). Case 3 (RP) RP is a right-handed young adult male aged 24 years. Pregnancy and labor were uneventful (birth weight: 3 kg). At 2 years he was examined by a neurologist owing to severe motor and linguistic deficits - independent walking was reached only at age 2 years when the child produced only few words. The neurological examination revealed cerebellar problems and the child was referred for outpatient rehabilitation. A CT scan evidenced a small poroencephalic area in the right cerebellar lobe, with signs of olivo-ponto-cerebellar atrophy. At 7 years he had seizures during sleep. Ictal episodes lasting about 1 minute were followed by a transient disorder of language expression. In the following years he continued to suffer from abrupt regression of language skills, receptive and expressive alike. Sometimes, these episodes were associated to seizures. As his clinical picture which was typical of Landau-Kleffner Syndrome - aphasic regression, seizures, paroxysmal EEG during NREM sleep - was associated to a documented neurological lesion, we defined it Landau-Kleffner Syndrome-Like. His IQ was in the normal range (Stanford - Binet Scale: IQ=93). The neurological examination revealed phonological and morphosyntactic deficits. His expression was characterized by many phonemic paraphasias and telegraphic style. The EEG in wakefulness showed paroxysmal activity characterized by bi- and triphasic spikes, followed by slow waves, in the left central and temporal regions. He was started on Carbamazepine (1 + l A cp/day). At 8 years the child started to attend primary school at our Rehabilitation Center. He was followed for epilepsy-related neurological problems and received speech therapy and neuropsychological therapy for 12 years. At the age of 10 years his IQ was in the low normal range (WISC-R: VIQ = 54; PIQ = 81; FIQ = 66) (cf. Table 1). Language was characterized by deficits that are typical of acquired aphasia in children, with many phonological, lexical access and morphosyntactic deficits. He showed clumsiness when performing fine distal movements, intentional tremor and asynergy bilaterally. At the age of 12 years he suffered from seizures in wakefulness, followed by transient aphasia. He also had many seizures in

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sleep. At the age of 14 years the AE therapy (Carbamazepine: 700 mg/day) was discontinued. He no longer had seizures. Until the age of 14 years he suffered from paroxysmal abnormalities mainly in the right centro-parietal region, which became accentuated in NREM sleep. They were also present in the contralateral hemisphere. Afterwards, the EEG normalized. Despite the fact that he no longer suffered from seizures and paroxysmal abnormalities, as shown by the EEG in sleep and wakefulness, his language was still pathological, with symptoms that are typical of transcortical motor aphasia (cf. Table 2). At the age of 24 years he received a detailed neuropsychological assessment and a language evaluation. On Raven's Standard Progressive Matrices his IQ was in the low normal range (Raven: IQ= 80). On the NEPSY his visuospatial skills were sufficiently developed, while he showed sensorimotor deficits (54% correct), attentional and executive deficits (79%) and memory deficits (88%). Language skills were assessed by the Italian version of the BAT (Paradis, 1987). The BAT comes with no normative values. However, to assess the extent of language deficits, we made reference to the values obtained from a control group, described in Fabbro et al. (2004). The morphological and syntactic language levels were most impaired (morphology = 39% of correct answers, <2SD below the mean; lexicon = 65%, <2SD), while the most severely compromised language tasks were propositional skills (48%, <2SD), lexical access (74%, <2SD) and comprehension (75%, <2SD). Case 4 (LS) LS is a left-handed girl aged 7 years and 3 months. A risk of miscarriage at the fourth month was evidenced. The child was born at term (birth weight: 2.85 kg). As she tended to always keep her head turned to the left, her mother consulted a neurologist.

Figure 5 — MRI. Large poroencephalic lesion affecting the temporal, parietal and frontal lobes, the thalamus and the basal ganglia (caudate nucleus, globus pallidus) of the left hemisphere (T2). The lesion affects over 40% of the left hemisphere, which is distinctly hypotrophic. Possible outcome of prenatal ischemia.

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A diagnosis of right hemiparesis, with more marked hypertonia of the lower limb (age: 5 months) was made. At the age of 6 months she started motor rehabilitation. The EEG in wakefulness at 18 months showed diphasic spikes - either isolated or in short sequences - over the left parieto-occipital derivations that tended neither to diffusion nor to generalization. At 6 years of age, an MRI evidenced an extended lesion to the left fronto-temporo-parietal lobe due to prenatal brain ischemia (cf. Figure 5). EEGs in wakefulness and Holter sleep were performed. The EEG in wakefulness was characterized by 9 Hz background activity. Paroxysmal discharges in the form of spikes and waves at 3 c/s were more diffuse in the anterior regions. Upon falling asleep and during sleep, subcontinuous paroxysmal activity at 2.5-3 c/s in the form of diffuse spike-wave complexes was evident (cf. Figure 6).

Figure 6— EEG: Intraclinical continuous paroxysmal activity (>75%) with 1-2 Hz spike-slow wave complexes in sleep stage 3 (CSWS).

Her IQ was in the normal range (WPPSI at age 5.06: VIQ= 92; PIQ= 89; FIQ= 90) (cf. Table 1). At the age of 6 she received a systematic neuropsychological and neurolinguistic assessment. On the neuropsychological evaluation by NEPSY (Korkman et al, 1998) she performed 1 or 2 SDs below the mean on all domains (attention, sensorimotor tasks, memory and learning, visuo-spatial tasks). The neurolinguistic assessment was made at 5 years and 11 months by the 4 -12 language battery (Fabbro, 1999). The child made significant errors on grammatical comprehension, word repetition and lexical fluency. Word comprehension was between 1 and 2 SDs below the norm. Her verbal expression was characterized by wordfinding difficulties, many morphosyntactic errors (substitution and addition of free inflectional morphemes and substitution of bound morphemes) and phonemic paraphasias. Once her neuropsychological and neurolinguistic deficits had been established, she received neuropsychological rehabilitation and speech therapy. In the evenings she also

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received valproate sodium which reduced her paroxysmal activity during sleep to a very small extent. She was also administered clobazam. After a few days the child showed short partial epileptic fits, which was unprecedented. The therapy was changed to control seizures (valproate sodium and ethosuximide). A language assessment was repeated at age 6 years and 8 months. A mild improvement in semantic comprehension, sentence repetition and semantic fluency was observed. A recent language assessment (7 years and 3 months) showed an improvement

in verb naming. The patient also mildly improved

in

grammatical

comprehension (up to 2 SDs below the mean). Semantic fluency was still between 1 and 2 SDs as in the previous assessment. In an analysis of descriptive speech, verbal fluency (words per minute) was between 1 and 2 SDs, while MLU and Type/Token Ratio were normal. Anomias were present. While these results may be indicative of some grammatical recovery, lexical difficulties still persist (cf. Table 2). Case 5 (LP) LP is a right-handed boy aged 4 years and 9 months. He was born at term after uneventful pregnancy (birth weight: 3.4 kg). At 4 months of age, he was diagnosed as having insufficient head control, axial hypotonia and rigidity of the upper and lower limbs. He started rehabilitation at 6 months of age. He reached independent sitting at 13 months of age, standing at 18 months, and walking at 21 months of age. At 4 years of age he underwent clinical and neuropsychological evaluations. The neurological examination revealed a dyskinetic tetraparesis, with greater impairment of the left side. Manipulative functions were limited because of dystonias. An MRI evidenced areas of signal alteration in the thalamus and the deep white matter bilaterally in the central, posterior and rolandic cortical-subcortical regions (cf. Figure 7), with lesions probably due to prenatal brain ischemia.

Figure 7— MRI. Lesions affecting the thalamus bilaterally and the periventricular white matter (area of signal hyperintensity in T2) probably due to a prenatal ischemic event.

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EEG scans in wakefulness and sleep were run at the age of 3 and 4 years. The EEG in wakefulness was characterized by unstable background activity. During sleep sharp waves were followed by slow medium-voltage waves over the left centro-temporal regions and asynchronous waves in the left central regions. During protracted sleep - up to NREM sleep stages 2 - a marked diffusion of epileptiform abnormalities was noted (cf. Figure 8). Paroxysmal abnormalities disappeared upon awakening. His IQ was in the normal range (Leiter-R, IQ= 106) (cf. Table 1). The child presented with scialorrhea and dyspraxia affecting the mouth, tongue and face (Bearzotti & Fabbro, in press). His verbal expression was dysarthric. Lexicon was limited to 10 words and CV+ CV strings. He could produce all vowels and semivowels, but only a few consonants (Iml, Ibl, Id/, Ik/). Word and sentence comprehension were normal (Cianchetti & Fancello, 1996). Naming was 1 SD below the norm, while sentence repetition was 2 SDs below the norm (cf. Table 2).

Figure 8 — EEG: Left focal spike activity. Spikes are more diffuse over the right hemisphere. A tendency was found to stage 2 paroxysmal synchronization. Case 6 (GM) GM is a right-handed boy aged 3 years and 4 months. Pregnancy was uneventful and he was born at term (birth weight: 3.5 kg). As fetal and neonatal suffering was observed, he was admitted to Intensive Care Unit. Twenty hours after birth he was taken to Nursery again. At 43 hours he suffered from clonic spasms affecting the right upper limb. The EEG tracing showed a marked depression in the left hemisphere, with convulsive activity starting from the left frontal lobe. He received phenobarbital (5 mg twice a day) for a month. AE therapy was thus discontinued and since then he no longer had seizures. Brain CT scan on his third day of life evidenced a cortico-subcortical vascular ischemic lesion in the left lateral frontal region. Another CT scan at age 1 month confirmed the extent of the ischemic lesion (cf. Figure 9). Motor and intellectual development was normal. He reached independent walking at 10

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months of age. When he was 3 years old, he was referred to our Center for a suspected expressive language disorder. The neurological examination was normal. His nonverbal IQ was in the normal range as assessed by Stanford - Binet Scale (cf. Table 1). A marked attention deficit was present, with hyperactive behavior. EEGs in wakefulness and sleep were performed at age 2 years and 10 months. The EEG in wakefulness evidenced a reactive 8.5 Hz fundamental rhythm. Paroxysmal discharges with large sharp spike-waves and atypical 4 Hz spikes-waves with maximal bicentral expression were present in the first sleep stages (stages 1 and 2). Reactivity was normal on awakening (Figure 10).

Figure 9 — CT Scan: cortico-subcortical lesion in the left rolandic and frontal area (4-6 cm in size) possibly due to an ischemic event.

Figure JO — EEG: Generalized paroxysmal discharges with 3.5-4 Hz spike-wave activity correlated to distal myoclonias in sleep stage 2 (<10%).

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Language examination showed a marked impairment in word comprehension (TPL Test, Axia, 1995) which was 2 SDs below the norm, and on word production (28 words, normal range > 300 words) on the Mac Arthur Scale (Caselli et al. 1990). He produced all the vowels but only some consonants (/p/, Pol, III, Id/, Ikl, Iml, In/, Its/) (cf. Table 2). DISCUSSION All the patients showed an early brain lesion localized in different brain structures (mainly cortical areas in cases 2, 4, 6; subcortical in cases 1 and 5 and cerebellar in case 3) and a severe language disorder. Many studies have shown that early brain lesions do not affect intellectual development and language acquisition in the absence of epilepsy (VarghaKhadem et al, 1992; Ballantyne & Trauner, 1999; Bates et al, 1999a,b). In our study three cases had seizures (cases 1-3), while the remaining cases showed defective language development without seizures. In all of them we found the presence of a high proportion of epileptiform abnormalities in NREM sleep. The first three cases did not only have epilepsy but showed a Landau-Kleffner SyndromeLike (LKS-L), that is a clinical picture of acquired aphasia associated to epilepsy in the presence of a neurological lesion. Acquired aphasia with convulsive disorder is an acquired language disorder associated with convulsive disorders and EEG abnormalities in children (Landau & Kleffner, 1957). Language disruption may occur before or after seizures. At onset the most frequent symptom is breakdown in language comprehension, while hearing and interpretation of non-linguistic sounds remain intact (word deafness). Following the breakdown in comprehension, expressive language and vocabulary decay progressively, too (Dugas et al, 1995). There may be (almost) full recovery following the first episode even after a short period of time (days or weeks). In other cases, recovery may be very slow (months or years) (cf. cases 1 and 2). Relapse is frequent and often the development of aphasia is fluctuating, with several aphasic episodes (cases 2 and 3). The clinical picture stabilizes before the end of adolescence with complete disappearance of seizures before the age of 15. Language recovery is sometimes very good, at other times defective. When defective, participants present with aphasic disorders for the rest of their lives (cf. case 3) (Mantovani & Landau, 1981). Despite the many studies and investigations carried out on LKS its cause is still unknown (Landau, 1992). Neuroradiological investigations have revealed that children with "classical" LKS do not exhibit quiescent or evolving cerebral lesions. An extremely significant feature which seems to be present in all children with LKS and which is revealed by the sleep EEG is a subcontinuous paroxysmal activity during NREM Sleep (ESES) (Tassinari et al, 1985a, Fabbro & Zucca, 2000). This bilateral (focalized) paroxysmal dysfunction during slow sleep is constantly associated with regression of language functions (Hirsh et al, 1990). Ravnik (1984) maintains there is an interdependence relationship between EEG abnormalities in sleep and verbal behavior. He documented recovery of verbal expression in a child with global aphasia and LKS immediately after intravenous injection of diazepam. The most frequent treatment is drug therapy.

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Phenobarbital, carbamazepine and phenytoin were either ineffective or even aggravative (cf. cases 1 and 3). Treatment with valproate sodium, ethosuximide, clobazam appeared to be partially or transiently effective, whereas the most encouraging results were obtained with corticosteroids (sleep-modifying drugs) (Marescaux et al, 1990). It has been observed that some cycles with cortisone (hydrocortisone) tend to reduce the frequency of seizures with paroxysmal abnormalities disappearing from tracings of both wake and sleep EEG. Often, an improvement in language functions (cf. case 2) is evident, which seems to be associated with a reduction or disappearance of paroxysmal abnormalities in sleep instead of seizures. Case 3 developed a language disorder, epilepsy and LKS-Like in the presence of a right cerebellar malformation lesion. The association between posterior fossa malformation and focal epilepsy has rarely been reported in the literature (Ducan el al, 1990; Parmeggiani et al, 1999), while the association between LKS and right cerebellar lesion has never been reported, at least to our knowledge. In contrast, the association between right cerebellar lesions and acquired or developmental language disorders has already been established (cf. Fabbro, 2000; Fabbro et al, 2000a). Cases 4, 5 and 6 presented a highly defective language development in the absence of epilepsy, though case 4 suffered from seizures from age 6 years onwards. In these cases too, paroxysmal abnormalities were present in NREM sleep. This pathological hallmark was also found in many children with severe Developmental Language Disorders (DLDs) — also known as Specific Language Impairment (SLI) or Developmental Dysphasia (cf. Bishop, 1997; Leonard, 1998). As early as the late 1960s it was reported that a large number of children with DLDs presented epileptiform EEG abnormalities without seizures (Forrest et al., 1967; Eisenson, 1968). These EEG abnormalities tended to be activated by drowsiness and sleep, at times occurring before the age of 3 and never after the age of 16 (Blom et al., 1972). Fois et al. (1968) discussed the issue of neuropsychological disorders following focal epileptic discharges in children without seizures. In some cases, they proposed an antiepileptic therapy. Often, this therapy reduced hyperactivity, improved the attention span and school performance, and eliminated vegetative and sleep disturbances. Maccario et al. (1972) described 7 children with a severe picture of DLD associated with epileptiform EEG abnormalities without convulsive seizures. The paroxysmal EEG abnormalities comprised sharp waves and spike-wave discharges in focal fashion, or bilateral synchronous bursts that were present in wakefulness and tended to intensify in slow wave sleep. The authors stressed the differences between this clinical picture and LKS. In their patients: 1) language impairment had been present from the start, and 2) no patient presented with clinical epilepsy. Echenne and co-workers made two EEG studies of children with DLD. In the former (Echenne et al, 1992) they studied 19 children with developmental dysphasia with no previous history of epileptic seizures. Each child received a diurnal prolonged EEG and a continuous overnight polygraph recording. Four children out of 19 presented paroxysmal EEG abnormalities (PA) in diurnal EEG and 17 children out of 19 presented PA in nocturnal EEG. These abnormalities clearly increased during NREM sleep. In a subsequent study, Echenne (1996) studied 76 children with developmental dysphasia without convulsive seizures. EEG paroxysmal abnormalities were found in 20% of the children with expressive

82

Neurogenic Language Disorders in Children

disorders and in 63.5% of children with comprehension difficulties. Picard et al. (1998) studied the diurnal and nocturnal EEGs of 52 children with DLD (40 boys and 12 girls), aged 4 to 11 years (mean age = 9 years). All children received a continuous overnight polygraph recording. In 46 out of 52 children with DLD the standard EEG in wakefulness was normal. In the control group, all children showed a standard EEG in the norm. In the nocturnal EEG paroxysmal activity during slow sleep was found in 50% of the participants with DLD. Recently, we followed 50 children with DLD classified according to ICD-10 criteria (Fabbro et al. 2000b). These children were administered: A) a standard EEG, and B) an EEG in afternoon sleep. Four children out of 50 (8%) presented with epileptiform abnormalities in the wake EEG. Twenty-eight children out of 50 (56%) presented with paroxysmal abnormalities in the EEG during afternoon sleep after partial deprivation of nocturnal sleep. According to Picard et al. (1998), paroxysmal abnormalities are responsible for developmental language disorders as interictal paroxysms occurring in epilepsy with rolandic paroxysms are responsible for transient cognitive problems, as suggested by Aarts et al. (1984) and Binnie (1993). Another explanation is provided by recent studies on memory and sleep. Slow sleep could be involved in structural modifications underlying long-term memory processes (such as protein synthesis, cf. Jones, 1998), which would be hampered by paroxysmal abnormalities. The presence of epileptiform abnormalities in NREM sleep is therefore a key clinical predictive factor of cognitive and/or linguistic delay in children with an early brain lesion. For this reason, it should be continuously monitored in these children. Paroxysmal abnormalities in NREM sleep in children with early brain lesions, children with LKS and children with developmental language disorders suggest the presence of common physiopathological mechanisms across the three clinical conditions. Recent studies with advanced neuroimaging techniques have shown that the majority of children with severe DLDs have malformative lesions of the cerebral cortex (polymicrogyria, PMG) and the parietal and perisylvian regions (Guerreiro et al., 2002). Furthermore, it is known that perisylvian PMG is frequently associated to epilepsy (Guerrini, 1999).

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Language Comprehension in Children. Psychology Press, Hove. Blom, S., J. Heijbel and P. G. Bergfors (1972). Benign epilepsy of children with centrotemporal EEG-foci. Prevalence and follow-up study of 40 patients. Epilepsia, 13, 609619. Brett, E. M. (1983). Pediatric Neurology. Churchill Livingstone, Edinburgh. Caselli M. C. and P. Casadio (1995). // primo vocabolario del bambino. Franco Angeli, Milano. Chilosi, A.M., P. Cipriani, B. Bertuccelli, L. Pfanner and G. Cioni (2001). Early Cognitive and Comunicative Development in Children with Focal Brain Lesions. J Child Neurol, 16,309-316. Cianchetti, C. and S. Fancello (1996). Test di valutazione del linguaggio. Erikson, Trento. Cytowic, R. E. (1996). The Neurological

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Fabbro, F. and G. Frau (2001). Manifestations of aphasia in Friulian. Journal of Neurolinguistics, 14, 255-279. Fabbro, F., and C. Zucca (2000). Acquired neuropsychological disorders in children with epilepsy. Saggi, 25, 23-29. Fabbro, F., R. Moretti and A. Bava (2000a). Language impairments in patients with cerebellar lesions. Journal of Neurolinguistics, 13, 173-88. Fabbro, F., C. Zucca, M. Molteni and R. Borgatti (2000b). EEG abnormalities during slow sleep in children with developmental language disorders. Saggi, 25, 41-8. Fabbro, F., A. Tavano, S. Corti, N. Bresolin, P. De Fabritiis and R. Borgatti (2004). Longterm neuropsychological deficits after cerebellar infarctions in two young adult twins. Neuropsychologia,42: 536-545. Fois, A., S. Borgheresi and E. Luti (1968). Clinical correlates of focal epileptic discharges in children without seizures. A study of 110 cases. Helvetica Pediatrica Acta, 23, 257265. Forrest, T., J. Eisenson and J. Stark (1967). EEG findings in 113 non verbal children. Electroencephalogr Clin Neurophysiol, 22, 291. Guerreiro, M. M., S. R. Hage, C. A. Guimaraes, D. V. Abramides, W. Fernandes, P. S. Pacheco, A. M. Piovesana, M. A. Montenegrol and F. Cendes (2002). Developmental language disorders associated with polymicrogyria. Neurology, 59, 245-250. Guerrini, R. (1999). Polymicrogyria and epilepsy. In: Abnormal cortical development and epilepsy (R. Spreafico, G. Avanzini and F. Andermann, eds.), pp. 191-201. J. Libbey & C, London. Hirsch, E., C. Marescaux, P. Maquet, M. N. Metz-Lutz, M. Kiesmann, E. Salmon, G. Franck and D. Kurtz (1990). Landau-Kleffner Syndrome: a clinical and EEG study of five cases. Epilepsia, 31, 756-767'. Jones, B. E. (1998). The neural basis of consciousness across the sleep-waking cycle. Adv Neurol, 77, 75-94. Me, E. (1990). An analysis of the correlation of lesion size, localization and behavioral effects in 283 published studies of cortical and subcortical lesions in old-world monkeys. Brain Research Review, 15, 181-213. Korkman, M, U. Kirk and S. Kemp (1998). NEPSY. A developmental Neuropsychological Assessment. The Psychological Corporation, San Antonio. Landau, W. M. (1992). Landau-Kleffner Syndrome: an eponymic badge of ignorance. Arch Neurol, 49,353. Landau, W.M. and F. R. Kleffner (1957). Syndrome of acquired aphasia with convulsive disorder in children. Neurology, 7, 523-530. Lashley, K. S. (1929). Brain Mechanisms and Intelligence. University of Chicago Press, Chicago. Lenneberg, E. H. (1967). Biological Foundations of Language. Wiley, New York. Leonard, L. B. (1998). Children with Specific Language Impairment. The MIT Press, Cambridge (MA).

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Maccario, M, S. J. Hefferen, S. J. Keblusek and K. A Lipinski KA (1982). Developmental dysphasia and electroencephalographic abnormalities. Dev Med Child NeuroL 24, 141155. Mantovani, J. F. and W. M. Landau (1980). Acquired aphasia with convulsive disorder: Course and prognosis. Neurology, 30, 524-529. Marescaux, C, E. Hirsch, S. Finck, P. Maquet, E. Schlumberger, F. Sellal, M. N. Metz-Lutz, Y. Alembik, E. Salmon and G. Franck (1990). Landau-Kleffner Syndrome: a pharmacological study of five cases. Epilepsia, 31. 768-777. Paradis, M. (1987). The Assessment of Bilingual Aphasia. LEA, Hillsdale (NJ). Parmeggiani, A.. A. Posar, M. C. Scaduto, S. Chiodo. M. Santucci and P. Giovanardi Rossi (1999). Posterior fossa malformations and epilepsy. J Child Neurol, 14, 113-117. Picard, A., F. Cheliout Heraut, M. Bouskraoui, M. Lemoine, P. Lacert and J. Delattre (1998). Sleep EEG and developmental dysphasia. Dev Med Child Neurol, 40, 595-599. Raven, J. C. (1954). Standard Progressive Matrices. The Psychological Corporation, New York. Ravnik, I. (1984). Un cas de syndrome de Landau-Kleffner: effet du Diazepam intraveineux. In: Les syndromes epiletiques de I 'enfant et de I'adolescent (J. Roger, C. Dravet, M. Bureau, F. E. Dreifuss, P. Wolf, eds.), pp. 196-7. John Libbey : London. Roid, G. H. and L. J. Miller (2002). Leitner International Performance Scale ~ R. Organizzazioni Speciali, Firenze. Tassinari, C. A., M. Bureau, C. Dravet, B. Dalla Bernardina and J. Roger (1985). Epilepsy with continous spikes and waves during slow sleep, otherwise described as ESES. In: Epileptic Syndromes in Infancy, Chilhood and Adolescence (J. Roger, C. Draver, M. Bureau, F. E. Dreifuss and P. Wolf P, eds.), pp. 194-204. John Libbey, London. Terman, L. M. and M. A. Merrill (1968). Scala di Intelligenza Stanford - Binet, forma L-M. Organizzazioni Speciali, Firenze. Tuchman, R. and I. Rapin (2002). Epilepsy in autism. Lancet. Neurology, 1, 352-358. Van Dongen, H. R. and M. C. B. Loonen (1977). Factors related to prognosis of acquired aphasia in children. Cortex; 13, 131-136. Van Hout, A. (2000). An Outline of Acquired Aphasia in Children. Saggi, 26, 13-21. Vargha-Khadem, F., E. Isaacs, S. Van der Werf, S. Robb and J. Wilson (1992). Development of intelligence and memory in children with hemiplegic cerebral palsy. Brain, 115, 315-329. Vicari, S., A. Albertoni, A. M. Chilosi, P. Cipriani, G. Cioni and E. Bates (2000). Plasticity and reorganization during language development in children with early brain injury. Cortex, 36, 31-46. Wechsler, D. (1973). WPPSI. Scala Wechsler a livello prescolare e di scuola elementare. Organizzazioni Speciali, Firenze. Wechsler, D. (1986). WISC-R. Scala di Intelligenza Wechsler per Bambini Riveduta. Organizzazioni Speciali, Firenze.

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Language in Children Treated for Posterior Fossa Tumor

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7

LANGUAGE AND PHONOLOGICAL AWARENESS ABILITIES OF CHILDREN TREATED FOR POSTERIOR FOSSA TUMOR Bruce, E. Murdoch, Kimberley M. Docking, and Elizabeth C. Ward The University of Queensland, Australia

Abstract — The general and high-level language and phonological awareness abilities of twelve children treated for posterior fossa tumor were examined in the context of recent theories implicating the cerebellum in language function, and treatment effects. At a group level, twelve children exhibited reduced performance in comparison to their individually matched peers on receptive and expressive general language measures. Across high-level language parameters, a group of ten of the twelve children with posterior fossa tumor demonstrated comparatively poor skills. At an individual case analysis level, three of twelve children demonstrated specific general language deficits, particularly in the areas of expressive language and syntax. However, three often children individually exhibited global impairments in high-level language, with an additional three demonstrating specific disturbances to problems solving, or lexical knowledge. Key contributing factors discussed included the impact of direct involvement of cerebellar structures, fourth ventricle location and associated hydrocephalus, tumor type, treatment effects, and young age at diagnosis. While all children with identified general language deficits also demonstrated severe global high-level impairments, findings indicated that high-level language disturbances may also occur in the presence of intact general language skills. Key words: posterior fossa, cerebellum, brain, tumor, children, language.

88

Neurogenic Language Disorders in Children

INTRODUCTION The posterior fossa accounts for just one-tenth of intracranial volume and yet it is this location that is responsible for over half of the brain tumors occurring in children (Cohen et al, 1982). Specific signs and symptoms relating to posterior fossa tumor often include signs of increased intracranial pressure due to obstruction of the cerebrospinal fluid pathways, or cerebellar signs which can include gait disturbances, nystagmus, dysarthria, dysmetria, and hypotonia (Heideman et al, 1993). Commonly occurring posterior fossa tumors include medulloblastomas, cerebellar astrocytomas, ependymomas, and choroid plexus papillomas (Becker & Jay, 1990). Studies by Hudson et al. (Hudson et al, 1989; Hudson & Murdoch, 1992a, b; Murdoch & Hudson-Tennent, 1994; Murdoch & Hudson, 1999a, c) constitute the most detailed reports of language disorders following posterior fossa tumor in children to date. Language abilities in the population of children with posterior fossa tumor were reported to range from above average language abilities to significant global language impairment, with specific areas of deficit noted to include expressive semantic and syntactic language, receptive language, and word-finding (Murdoch & Hudson-Tennent, 1994). Overall, this group of researchers reported that while not inevitable, language disorders do occur in children in the chronic stage following treatment for posterior fossa tumor, noting that no particular pattern of language impairment was considered characteristic, as all aspects of language were reported to be impacted in the population examined (Murdoch & Hudson, 1999a). In highlighting the heterogeneity of children with posterior fossa tumor examined across the studies reported due to the varying profiles, tumor types, and differing treatment approaches, several factors were proposed by Hudson et al. (1989) to have contributed to the resulting language disorders reported in this population. These factors included obstructive hydrocephalus, with the mass effect of the tumor impeding the flow of cerebrospinal fluid, dilating the ventricular system, compressing the cerebral cortex, and potentially contributing to tissue destruction and cortical compression (Murdoch & Hudson, 1999a). Other potential contributing factors noted by these authors included young age at diagnosis and/or treatment, tumor type, duration of pre-operative symptoms, extent of surgical excision, and insertion of ventriculoperitoneal shunts. The primary factor considered by these researchers, however, to have contributed to the presence of language deficits in children treated for posterior fossa tumor was treatment. One factor that was not considered by Hudson et al. (1989) was the potential for language deficits to occur as a direct result of cerebellar damage associated with posterior fossa tumor. While the significance of treatment effects on language function in children with posterior fossa is acknowledged, in light of the recently identified role of the cerebellum in cognitive and language functions, it is equally important to consider the direct effects of cerebellar damage. As these functions are only now beginning to be recognized, such recent contributions in the study of the cerebellum were unavailable for consideration in earlier studies of language function in children treated for posterior fossa tumor.

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89

Recent clinical and functional neuroimaging studies have provided evidence of the role of the cerebellum in modulating cognitive and language functions via its reciprocal connections with the cerebral cortex (Fabbro, 2000; Fabbro et al. 2000; Marien et al, 2000; Silveri & Misciagna, 2000; Marien et al, 2001; Silveri et al. 2001). Damage to the cerebellum, in particular the right cerebellar hemisphere and areas of the vermis, have been documented to impact nonmotor language function and result in impairments such as reduced verbal fluency, telegraphic speech, agrammatism, and word-finding difficulties (Riva, 1998, 2000; Schatz et al., 1998; Steinlin et al, 1999; Levisohn et al, 2000; Riva & Giorgi, 2000a, b; Scott et al, 2001). Considering the early language findings by Hudson et al. (Hudson et al, 1989; Hudson & Murdoch, 1992a, b; Murdoch & Hudson-Tennent, 1994; Murdoch & Hudson, 1999a) in light of this new understanding of the role of the cerebellum in language, the patterns of deficit reported may also have reflected direct damage to cerebellar function in addition to treatment effects. Disturbances to high-level language and cognition has also been observed in recent clinical studies relating to cerebellar damage (Riva, 2000: Riva & Giorgi. 2000a, b). As evidence outlining the cerebellar contribution to both language and cognition is now emerging, the direct effects on these areas of function are considered to be plausible, in addition to later developing processes which include high-level language (Levisohn et al, 2000). The potential for high-level language to be impacted following cerebellar involvement is supported by several authors. Riva and Giorgi (2000b) reported deficits such as reduced thinking flexibility and problem solving in children with cerebellar tumors. Other authors, however, noted disturbances to the processing of verbal intelligence, the ability to produce complex language structures, complex language tasks, and executive function and higherorder behaviour (Riva, 1998; Schatz et al, 1998; Levisohn et al, 2000; Riva & Giorgi, 2000a). Investigations into the presence of literacy and foundation pre-literacy difficulties in children treated for posterior fossa tumor to date have also been lacking and somewhat unclear. The reading and writing abilities of children with posterior fossa in a study by Hudson and Murdoch (1992a) were reported to be comparable to the control group performance as well as falling within the normal range on standardized assessment. Yet, at an individual level, two of the six participants experienced significant difficulty in these areas (Murdoch & Hudson-Tennent, 1994). Unfortunately, the specific underlying deficits and areas of difficulty experienced by these two participants were not outlined. Sands et al. (1998) included measures assessing the basic reading and spelling abilities of six children in their investigation of the neuropsychological functioning of children treated for brain tumor. These authors reported that mean performances were within the normal range on both tasks. Specifically, five of the six children demonstrated abilities within the high average to average range on the academic measure of reading, with the remaining child performing in the low average range. Reading and writing difficulties have also been documented as a component of acquired language disorders in children of varying aetiologies including brain tumor (Alajouanine & Lhermitte, 1965; Hecaen, 1976; Cooper & Flowers, 1987).

90

Neurogenic Language Disorders in Children The noted presence of reading and writing deficits in children with acquired language

deficits, combined with the young age at which treatment occurs for brain tumor, necessitates a focus on the impact of brain trauma (including to the posterior cranial fossa) on the development of pre-literacy skills that provide the foundation for literacy mastery. However, no study to date has investigated possible disturbances to the pre-literacy precursors that may result in reading and writing difficulties in children treated for posterior fossa tumor. This area of development, namely phonological awareness, clearly requires further attention. As relatively few studies to date have addressed language function in children treated for posterior fossa tumor (Hudson & Murdoch, 1992a, b; Murdoch & Hudson-Tennent, 1994) and the only contributing factors considered to impact were treatment effects, there is a need to extend this area of research in light of current theories. The importance of investigating high-level language abilities has been highlighted not only by recent evidence supporting the potential for high-level language disturbances to exist, but also the discrepancy between performance on general language tasks and high-level language tasks in populations of children treated for posterior fossa tumor (Murdoch & Hudson-Tennent, 1994). Additionally, while some reports of reading and writing difficulties have been previously documented in populations of children treated for posterior fossa tumor and studies of children with acquired language disorders resulting from varying aetiologies, the phonological awareness skills of this population, to date, have not been investigated. Therefore, the intent of the present paper is to examine general language, high-level language and pre-literacy skills in children following treatment for posterior fossa tumor, in the context of tumor types and their associated treatment effects, while also considering the impact of direct damage to the cerebellum on language functions.

METHODOLOGY Participants Twelve participants, nine male and three female, were included in the present study ranging in age from three years nine months to thirteen years six months (mean age = 9.76 years, standard deviation = 3.30 years), who had been diagnosed with a tumor in the posterior fossa and had completed treatment at least six months prior to involvement in the study. Biographical details of these twelve participants are summarized in Table 1. Twelve control participants individually matched for age and gender (mean age = 9.40 years, standard deviation = 3.33 years) were also included in the study. All control participants had no history of cancer, acquired brain injury, epileptic activity or seizures, or had a known history of speech/language difficulties. All twenty-four participants spoke English as their only language.

Language in Children Treated for Posterior Fossa Tumor

91

Table 1 — Biographical data of participants treated for posterior fossa tumor

Case/

AaA

AaD

TPT»

Gender 1/M

13.6

12.3

2/F

10.9

9.11

Tumor location 4thV

TM

Surgery

TRD

1.1

Tumor type MDB

R

—

0.6

EPD

RCH

s,

T

36Gy cranial 54Gy to PF 36Gy to spine 54Gy

R S, R

N-T

S

—

N-T

s

N-T

54Gy

—

s, c

NA

—

vincristine, CP, Mesna, G-CSF, HD methotrexate, cisplatin, carboplatin, etoposide

4"'V

s,

NA

45Gy to PF

4"'V Cerebellar vermis 4th V

R

NA T

13.3

10.1

2.0

MDB

Posterior to 41" V

4/M

10.11

2.6

8.5

CPP

5/M

7.9

7.3

0.6

JP AA

6/M

7.4

1.8

3.5

EPD

Roof of 4thV Inferior vermis, LCH 4"'V

7/F

6.11

2.11

3.9

EPD

8/M

13.0

5.4 11.1

1.7 1.2

AA JP AA

9/M

13.0

11.1

1.2

EPD

s s s,

S-T

R 11.0

6.6

4.1

JP AA

Il/F

3.9

2.5

0.8

EPD

3.1

12/M

5.11

5.4

0.7

AA

—

36Gy craniospinal 54Gy to PF —

3/M

10/M

CHEMO drugs —

Cerebellar midline, LH 4th V RCH, vermis, RC peduncle LC vermis, LCH

s

T

s, c #

T

s

S-T

—

50Gy + 5.4Gy to residual tumor

Note: "Age and time presented in years, months; LG = low-grade; 4th V = fourth ventricle; L = left; S = surgery, R = radiotherapy; C = Chemotherapy; NA = not available; - not applicable; Gy = grays; # = no treatment for recurrence at time of testing; AaA = Age at assessment; AaD = Age at diagnosis; TPT a = Time post-treatment; TM = Treatment; TRD = Total radiation dosage; T = Total; N-T = Near Total; S-T = Subtotal; RCH = Right cerebellar hemisphere; LCH = Left cerebellar hemisphere; LH = Left hemisphere; CP = cyclophosphamide; MDB = Medulloblastoma; EPD = Ependymoma; AA = Astrocytoma; CPP = Choroid plexus papilloma.

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Neurogenic Language Disorders in Children

Procedure All 24 participants underwent language testing in a quiet environment with limited distractions. In all cases, testing was conducted over a number of sessions to reduce the influences of fatigue. General Language Assessment Battery. The general language abilities of each of the twelve cases and their individually matched peers were assessed using three tests which reflect a measure of general language skills: either the Clinical Evaluation of Language Fundamentals - Third Edition (CELF-3) (Semel el al, 1995) or the Clinical Evaluation of Language Fundamentals - Preschool (CELF-Preschool) (Wiig el al, 1992), the Peabody Picture Vocabulary Test - Third Edition (PPVT-III) (Dunn & Dunn, 1997), and the Hundred Pictures Naming Test (HPNT) (Fisher & Glenister, 1992). High-level Language and Phonological Awareness Assessment Battery. The high-level language and phonological awareness abilities of a group of ten of the twelve participants treated for posterior fossa described above (excluding Cases 11 and 12) (mean age = 10.74 years, standard deviation = 2.57 years), and their matched peers (mean age = 10.36, standard deviation = 2.65) were administered a battery of standardized assessments designed to examine higher-level language function and pre-literacy ability. As Cases 11 and 12 did not meet the minimum age requirements of the high-level language and literacy assessments, these cases were not included in the present analysis. The assessment battery included: the Test of Problem Solving - Elementary (Revised) (TOPS-Elementary) (Zachman et al, 1994) or the Test of Problem Solving - Adolescent (TOPS-Adolescent) (Zachman et al., 1991), the Test of Word Knowledge (TOWK) (Wiig & Secord. 1992). the Test of Language Competence - Expanded (TLC-E) (Wiig & Secord, 1989), and the Queensland University Inventory of Literacy (QUIL) (Dodd el al, 1996). Again, the age of each participant treated for posterior fossa tumor and their individually matched peer determined the version or age group level that was completed for each of the high-level language assessments.

RESULTS Group Analysis

Non-parametric tests were adopted in the present analysis, due to an incongruity across some parameters relating to significance on a measure of homogeneity of variance (Levene's Test for Equality of Variance). The Mann-Whitney U was employed to determine the presence of statistically significant discrepancies across all parameters. These results are summarized respectively in Tables 2 and 3. Due to the multiplicity of subtests comprising the QUIL, a stringent alpha level of p<0.01 was applied for this assessment only (Shearer, 1982). For all other assessments, an alpha level of p<0.05 was adopted. The group of twelve children with

Language in Children '/'recitedfor Posterior Fossa Tumor

93

posterior fossa tumor performed significantly below an individually matched control group on the Receptive (p < 0.01), Expressive (p < 0.01) and Total Language (p< 0.01) component of both versions of the CELF assessments, and the Peabody Picture Vocabulary Test - Third Edition (p < 0.05). These results are summarized in Table 2. Table 2 — Posterior fossa tumor and control group analysis: Means (MX standard deviations (SD), and Mann Whitney U comparisons for the Clinical Evaluation of Language Fundamentals - Third Edition / Preschool (CELF-3/Prcschool), Peabody Picture Vocabulary Test - Third Edition (PPVT-III), and the Hundred Pictures Naming Test (HPNT) Parameter

Posterior fossa group (n = 12) M SD

Control group (n = 12) M SD

Mann-Whitney Asymp. Sig. V (2-tailed)

CELF-3/Preschool Receptive Language Score

107.17

12.66

121.25

11.43

27.5

0.010**

Expressive Language Score

98.42

17.23

117.08

12.39

24.5

0.006**

Total Language Score

102.67

15.26

119.75

11.92

24.0

0.006**

PPVT-III

102.25

12.05

114.17

9.33

32.0

0.021*

HPNT (Raw score /100)

91.58

12.31

97.91

2.66

40.5

0.066

Note: ** p < 0.01; *p < 0.05; Normative data for CELF-3/Preschool and PPVT = 100 ± 15; HPNT scores reported in raw value out of 100. Additionally, statistical measures applied to results of the high-level language abilities and phonological awareness skills revealed significantly reduced performance by the group often children treated for posterior fossa tumor on the TOPS, the Receptive (p<0.01), Expressive (p<0.05) and Total Composites (p<0.05) of the TOWK, and the Interpreting Intents (p<0.05), Expressing Intents (p<0.05), and Total component (p<0.05) of the TLC-E, when compared to an individually matched control group (see Table 3). Results yielded by the QUIL revealed no significant differences on any of the phonological awareness parameters (see Table 3). Individual analysis While group findings revealed significantly reduced performance across most general and all high-level language parameters, individual variation is a prominent feature of populations of children treated for posterior fossa tumor (Murdoch & Hudson-Tennent, 1994). Therefore, individual areas of strengths and weakness in the context of varying tumor types, associated

94

Neurogenic Language Disorders in Children

symptomatology, and treatment programs, may be masked by group level analysis. An examination of each case treated for posterior fossa tumor on an individual basis was, therefore, carried out to determine the presence of specific signs of language impairment in the context of tumor type, site, and treatments employed. Table 3 — Posterior fossa tumor and control group analysis: Means (M), standard deviations (SD), and Mann Whitney U comparisons for the Test of Problem Solving (TOPS), Test of Word Knowledge (TOWK), Test of Language Competence - Expanded (TLC-E), and Queensland University Inventory of Literacy (QUIL) Posterior fossa Control group group (n = 10) (n = 10) 88.80

15.35

109.70

5.25

MannWhitney U 12.0

Receptive Composite Expressive Composite Total Score

98.60 93.90 95.80

14.65 11.32 12.44

110.50 110.70 111.30

8.86 8.07 8.04

23.5 9.5 17.5

0.044* 0.002** 0.014*

TLC-E Interpreting Intents Expressing Intents Total Score

91.40 14.86 95.50 18.56 93.40 16.83

106.40 14.15 110.60 11.53 109.60 13.90

23.5 21.0 23.5

0.043* 0.027* 0.045*

QUIL Nonword spelling Nonword reading Syllable identification Syllable segmentation Spoken rhyme Visual Rhyme Spoonerisms Phoneme detection Phoneme segmentation Phoneme manipulation

12.70 11.20 11.00 10.10 9.30 7.80 11.70 10.60 11.70 10.30

14.30 11.50 10.80 11.20 8.80 8.33 11.60 9.90 11.20 10.80

36.5 47.0 48.5 35.5 48.5 39.5 42.5 45.0 41.5 29.0

0.300 0.816 0.905 0.205 0.906 0.648 0.553 0.702 0.513 0.936

TOPS

Asymp. Sig. (2-taiIed) 0.004**

TOWK

3.40 2.44 1.25 2.13 3.27 3.65 2.21 2.55 2.91 3.34

1.95 2.80 1.87 1.62 3.94 3.24 2.95 3.60 2.57 2.39

Note: ** = p<0.01; * = p<0.05; p significant at < 0.01 for QUIL subtests. An individual analysis of the general and high-level language, and phonological awareness abilities of each of the twelve participants treated for posterior fossa tumor will therefore follow. Performance was analyzed by comparing each standard score to the normative data for each assessment, where less than one standard deviation from the mean is considered to be below the normal range. Seven of the twelve cases (Cases 2, 3, 5, 6, 7, 9, and 11) were noted

Language in Children Treated for Posterior Fossa Tumor

95

to exhibit evidence of language deficits, while the remaining cases (Cases 1, 4, 8, 10, and 12) were found to function within normal limits. On the general language assessment battery, varying degrees of expressive language deficits were observed in the performance of Cases 6, 7, and 11, however a pattern of reduced performance in the area of syntax was also noted in the profile these three cases. Naming difficulties were only experienced by Case 11. However, on measures of high-level language and phonological awareness, three of these cases (Cases 6, 7, and 9) exhibited global deficits, with more specific areas of deficit in three children (Cases 2, 3, and 5). More specific phonological awareness difficulties were noted in five cases (Cases 3, 4, 6, 7, and 8). Specific details of Cases 2 - 9 and 11 are discussed below. Cases 1, 10, and 12 did not demonstrate reduced performance across all assessments of general and high-level language, as well as phonological awareness, and will therefore not be discussed in detail in the case analysis of this paper. Case 2. Following the diagnosis of a 2 cm low-grade ependymoma in the right cerebellum at the age of nine years eleven months, Case 2 underwent a treatment regimen of total surgical removal and an eight week course of radiotherapy (see Figure 1). At the age often years nine months, Case 2 participated in the current study. The MRI conducted six weeks prior to language testing revealed no evidence of recurrent tumor (see Figure 2). Case 2 demonstrated intact general language abilities according to the normative information provided for each of the assessments (see Table 4). In fact, performances on the Receptive, Expressive and Total Language components of the CELF-3, including the subtests, Word Classes and Sentences Assembly, were considered above the normal range. Receptive vocabulary skills measured by the PPVT-III were also noted to be above the normal range.

Figure 1 — Case 2 at diagnosis: T2 weighted coronal MRI scan demonstrating a 2 cm mass in anterior cerebellum, just to the right of the midline and adjacent to the right posterior aspect of the fourth ventricle.

96

Neurogenic Language Disorders in Children

Figure 2 — Case 2 at language testing (six months post treatment): Tl weighted coronal MRI scan revealing a small cystic areajust posterior to fourth ventricle in keeping with post-surgical change. No evidence of recurrent tumor following radiotherapy treatment. Table 4 — Individual general language assessment results (represented in standard scores) of Cases 1 - 5 treated for posterior fossa tumor on the Clinical Evaluation of Language Fundamentals - Third Edition (CELF-3), Peabody Picture Vocabulary Test - Third Edition (PPVT-III), and the Hundred Pictures Naming Test (HPNT) Tests

Case I

Case 2

Case 3

Case 4

CaseS

131 15 14

118 12 14

108 16 8

110 13 12

15A

13A

10A

10A

106 10 12 ll#

125 15 12

120 13 12

92 7 7

104 9 13

CELF-3 Receptive Language Concepts & Directions Word Classes Semantic Relationships1^ / Sentence Structure# Expressive Language Formulated Sentences Recalling Sentences Sentence AssemblyA / Word Structured Total Language

15A

15A

12A

10A

129

120

100

107

PPVT-III

120

116

111

100

HPNT (Raw score /100)

100

93

93

96

96 8 9 11# 101 107 95

Note: # = Level 1 subtest variation; A = Level 2 subtest variation; Standard scores in italics = normal range 85 - 115; Subtest standard score normal range = 7-13.

Language in Children Treated for Posterior Fossa Tumor

97

Table 5 — Individual high-level language and phonological awareness assessment results (represented in standard scores) of Cases 1 - 5 treated for posterior fossa tumor on the Test of Problem Solving (TOPS), Test of Word Knowledge (TOWK), Test of Language Competence - Expanded (TLC-E), and Queensland University Inventory- of Literacy (QUIL) Case 1 112

Case 2 78*

Case 3 96

Case 4 91

CaseS 78*

Receptive Composite Synonyms A / Word Opposites # Figurative Usage A / Receptive Vocabulary #

109 12A 11 A

109 11 A 12A

94 9A 9A

121 14A 13A

115 11# 14#

Expressive Composite Word Definitions Multiple Contexts A / Expressive

111 11 13A

100 10 10A

81* 4* 9A

97 9 10

100 9 11

Vocabulary # Total

111

105

86

109

108

Interpreting Intents Listening Comprehension: Making

135 15

91 8

100 12

94 8

109 13

Inferences Figurative Language Expressing Intents Ambiguous Sentences Oral Expression: Recreating Sentences'" /

17 112 15

9 97 12 7A

8 76* 9 3A*

10 94

1

100 8

11 A

nu

Speech Acts# Total QUIL

127

93

86

93

105

15 12 11 12 11 12 13 12 13 13

16 13 12 10 12 11

11 10 11 12 4*

12 11 13 13 11 5* 12 14 14 11

13 15 10 9 10 11 13 9

Tests TOPS TOWK

TLC-E

Nonword spelling Nonword reading Syllable identification Syllable segmentation Spoken rhyme Visual Rhyme Spoonerisms Phoneme detection Phoneme segmentation Phoneme manipulation Note: # = Level 1 subtest variation;

A

9

A

13 14 14 11

3* 13 8 12 13

10

14 11

= Level 2 subtest variation; * = below normal range (Standard

scores in italics: normal range 85 - 1 15; Subtest standard score normal range = 7-13);

The highest age range with respect to normative data on the HPNT comparable to Case 2's age often years nine months was seven years one month to nine years two months (with a

98

Neurogenic Language Disorders in Children

mean of seven years seven months). The mean accuracy score for this group of children (n=260) was 84.11, with a standard deviation of 9.85 (Fisher & Glenister, 1992). Therefore, while Case 2's raw accuracy score of 93 appears to be within the normal range for these lower age limits, it is impossible to speculate whether performance represents intact naming skills for this participant, or a mild deficit, at age ten years nine months. High-level language and phonological awareness assessments revealed performance on the TOPS that was considered below the normal range (see Table 5). All other performances across the remaining measures were considered within the normal range. Case 3. Case 3 was diagnosed at the age often years one month with a 3 cm medulloblastoma located in the posterior fossa immediately posterior to the fourth ventricle (see Figure 3). A six month history of increasing headaches associated with vomiting was also reported. A near total surgical removal was undertaken, followed by a four week course of radiotherapy, Craniospinal irradiation was administered to the whole brain and spinal axis at a dose of 36 Gy in twenty fractions, with the posterior boosted with the lateral oblique fields to a dose of 54 Gy in 30 fractions. No acute effects were noted.

Figure 3 — Case 3 at diagnosis: Sagittal MRI scan demonstrating a 3 cm medulloblastoma immediately posterior to the fourth ventricle. Two years following completion of treatment, at the age of thirteen years three months, Case 3 participated in the present study. A MRI scan of the brain carried out two weeks following language testing revealed stable appearance of the tumor with no evidence of tumor recurrence or metastases (see Figure 4). Case 3 demonstrated intact general language abilities across all assessments of general language including the CELF-3, PPVT-III and the HPNT (see Table 4).

Language in Children Treatedfor Posterior Fossa Tumor

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Reduced performance below the normal range, however, was noted on the Expressive Composite of the TOWK, and the expressive subtest Word Definitions, as well as the Expressing Intents section of the TLC-E and the expressive subtest Oral Expression: Recreating Sentences (see Table 5). It is noted that a reduced subtest score within each of these components would contribute to an overall reduction in the overall score for that component. Performance below the normal range was demonstrated on both the Spoken and Visual Rhyme subtests of the QUIL. Case 4. Case 4 was diagnosed with a choroid plexus papilloma in the roof of the fourth ventricle at the age of two years six months (see Figure 5). A history of increasing head tilting to the right, ataxia, vomiting after breakfast, and a one year history of irritability (with greater increase over the ten days prior to diagnosis) was also noted. Case 4 had associated chronic hydrocephalus. Treatment involved subtotal removal of the tumor, followed by shunt insertion ten days later. Cranial nerve dysfunction was observed subsequent to surgery, with residual bulbar palsy and a failure of return of the gag reflex. Neither radiotherapy or chemotherapy were administered. Case 4 has a history of ongoing speech pathology intervention from the time of tumor diagnosis until the present involvement in the current study. Management of severely impaired swallowing function has been extensive, in addition to a significant oral motor impairment and vocal fold impairment. General receptive and expressive language skills were also monitored over this protracted period of time.

Figure 4 — Case 3 at language testing (two years post treatment): Tl weighted sagittal MRI scan post surgery and radiotherapy treatment revealing stable appearances with no evidence of local tumor in the posterior fossa, or metastases.

100 Neurogenic Language Disorders in Children

Figure 5 — Case 4 at diagnosis: Coronal CT scan revealing a 2.8 x 2.6 cm choroid plexus pailloma in ihe midline of the posterior fossa. Surrounding oedema and associated hydrocephalus noted. Marked dilatation of lateral and third ventricles. Fourth ventricle displaced anterosuperiorly.

Clinical history reported that Case 4 presented with a mild expressive language delay initially post-surgery. Improvements in both comprehension and expressive language were noted over time, with some word finding skills also noted at age four years six months. Some delays in grammatical comprehension were also noted at this time. While at five years two months, expressive semantic skills were reportedly within normal limits Case 4 demonstrated mild deficits in expressive semantics and word retrieval skills during structured tasks at age six years. Expressive semantic difficulties were again noted six months later, in addition to significant difficulties in sentence formulation. A weakness in the area of sentence formulation was again noted at nine years five months. At the age often years eleven months, eight years five months following treatment, Case 4 underwent assessments for the present study. The most recent MRI available was performed six years and two months prior to language testing and revealed no evidence of recurrent tumor (see Figure 6). Performance across all subtests of the CELF-3, the PPVT-HI, and the HPNT, indicated intact general language abilities in the areas of receptive and expressive language, receptive vocabulary, and naming (see Table 4). High-level language and phonological awareness testing for the present study revealed intact high-level language abilities across all measures. A reduced score on the Visual Rhyme subtest of the QUIL, however, was evident (see Table 5).

Language in Children Treatedfor Posterior Fossa Tumor

101

Figure 6 — Case 4 six years two months prior to language testing (most recent MRI prior to testing): Post-surgical coronal CT scan indicating that the ventricular system remains dilated, despite no progression or evidence of recurrent tumor in the fourth ventricle. Case 5. Case 5 was diagnosed with a 4cm juvenile pilocytic astrocytoma arising from the inferior vermis and involving the left hemisphere (see Figure 7), and obstructive hydrocephalus, subsequent to a four month history of increasing intermittent headaches, nausea, and vomiting.

Figure 7 — Case 5 at diagnosis: Tl weighted sagittal MRI scan demonstrating a large complex cystic and solid mass lying within and expanding the fourth ventricle. There is cystic extension inferiorly through the foramina of Magendie into the Cisterna Magna, extending through the foramen magnum as far as the inferior margin of the Cl arch.

102 Neurogenic Language Disorders in Children

Figure 8 — Case 5 at language testing (six months post treatment): Post-surgical TI weighted coronal MR1 scan indicating persistent non-progressive residual tumor on left side of fourth ventricle and medial aspect of left cerebellar hemisphere.

A near total surgical resection was carried out leaving some residual tumor and associated oedema. Post-operatively, hydrocephalus was considered present as well as slight ataxia and left-sided weakness. A neuropsychological assessment revealed performance in the average range, with no difficulties evident before or after surgery. Some sequencing and divided attention difficulties were noted. Case 5 was also seen by the speech pathology department at the hospital post surgical intervention for motor speech difficulties due to a mild dysarthria. At this time, language abilities were considered intact. Case 5 was discharged from this service three months prior to involvement in the current study. Six months following completion of treatment, at the age of seven years nine months, Case 5 participated in the present study. A MRI of the brain carried out five days prior to language testing indicated unchanged residual tumor in the left side of the fourth ventricle and medial aspect of the left cerebellar hemisphere (see Figure 8). Performance on the CELF-3, PPVT-III, and HPNT indicated the presence of intact general language abilities according to the normative data for each of the assessments (see Table 4). Performance on high level language and phonological awareness tasks revealed abilities that were within the normal range across all assessments, except for reduced abilities noted on the TOPS (see Table 5). Case 6. Case 6 was diagnosed with a 4 x 4cm ependymoma located in the fourth ventricle at the age of one year eight months (see Figure 9). A two month history of headaches, vomiting, weight loss, irritability, tiredness and ataxia was reported. On examination Case 6 demonstrated ataxia with intention tremor, bilateral papilloedema and gross hydrocephalus. Case 6 underwent surgical resection, and over two weeks later required a shunt insertion for persisting hydrocephalus. Post-surgically, Case 6 was reportedly irritable and lethargic and

Language in Children Treated for Posterior Fossa Tumor

103

demonstrated bilateral sixth nerve palsy. The shunt was removed two months following insertion due to infection, and did not require replacement.

Figure 9 — Case 6 at diagnosis: Axial view MRI scan demonstrating a 4 x 4 cm ependymoma located within the fourth ventricle. Marked hydrocephalus also noted within the lateral ventricles.

Figure 10 — Case 6 at language testing (three years five months post treatment): Coronal view MRI scan revealing no evidence of recurrent tumor in the fourth ventricle post surgery and chemotherapy treatment. Chemotherapy treatment was commenced one month following resection. A personal protocol was administered over two years with each cycle fifty six days in length. The chemotherapeutic

drugs

vincristine,

cyclophosphamide,

Mesna,

G-CSF,

high-does

104 Neurogenic Language Disorders in Children

methotrexate, cisplatin, carboplatin, and etoposide were administered. Acute effects included progressive ototoxicity related to high-dose cisplatin. At the age of seven years four months (three years five months following completion of treatment), Case 6 participated in the present study. A MRI of the brain was carried out one week following language testing (see Figure 10). General language abilities were considered below the normal range on both the Expressive Language and Total Language components of the CELF-3, all of the expressive subtests (Word Structure, Formulated Sentences, and Recalling Sentences), and the receptive subtest, Sentence Structure (see Table 6). The Word Structure subtest assesses the expressive knowledge of word structures, whereas the Formulated Sentences subtest examines the formulation of simple, compound, and complex sentences (Semel et al, 1995). Recalling Sentences assesses recall and reproduction of sentence surface structure as a function of syntactic complexity (Semel et ai, 1995). The receptive subtest, Sentence Structure, assesses comprehension of structural rules at the sentence level. Performance on the Receptive Language component of the CELF-3 and both the PPVT-III and the HPNT were considered intact. High-level language and phonological awareness measures revealed reduced performance that was considered below the normal range on the TOPS, and the Expressive Composite and Total score of the TOWK (including the receptive subtest Receptive Vocabulary and the Expressive subtest Word Definitions) (see Table 7). It was also noted that performance on the Expressing Intents section (including both expressive subtests, Ambiguous Sentences and Oral Expression) and the Total score of the TLC-E were below the normal range. The QUIL subtests, Nonword Spelling, Nonword Reading, Visual Rhyme, Spoonerisms, Phoneme Detection, and Phoneme Manipulation were also considered reduced. Case 7. Case 7 was diagnosed with a 4 cm ependymoma in the fourth ventricle, which extended posteriorly between the cerebellar hemispheres and through the foramen magnum to the inferior border of the axis, including inferior extension along the brainstem. Obstructive hydrocephalus was also noted. A four day history of vomiting and mallena was reported prior to diagnosis at the age of two years eleven months. Treatment involved surgical resection as well as a five week course of radiotherapy, delivering a dose of 45 Gy to the posterior fossa in 25 fractions. A recurrence in the fourth ventricle at the age of five years four months was preceded by a two week history of headaches (see Figure 11). Treatment involved resection of the tumor, which was histologically classified an astrocytoma. A history of speech pathology intervention was noted over a period of several years following diagnosis for Case 7, continuing up to time of involvement in the present study. While therapy had focussed on Case 7's significant oral motor inefficiency, motor speech disturbances (with a noted right facial paralysis), and impaired swallowing abilities, no formal language assessment had been undertaken at the time of testing. Language testing for the present study was undertaken at the age of six years eleven months (three years nine months

Language in Children Treated for Posterior Fossa Tumor

105

following the initial treatment program consisting of surgery and radiotherapy treatment, and one year seven months following surgical treatment for tumor recurrence).

Figure 11 — Case 7 at diagnosis of recurrent tumor: Coronal MRI scan revealing recurring tumor in fourth ventricle. Table 6 — Individual general language assessment results (represented in standard scores) of Cases 6 - 10 treated for posterior fossa tumor on the Clinical Evaluation of Language Fundamentals - Third Edition (CELF-3), Peabody Picture Vocabulary Test - Third Edition (PPVT-III). and the Hundred Pictures Naming Test (HPNT) Tests CELF-3 Receptive Language Concepts & Directions Word Classes Semantic Relationships'^/ Sentence Structured

Case 6

Case 7

Case 8

Case 9

Case 10

88 10 8 6#*

90 8 7 10#

114 12 10 15A

118 11 9

110 10 13

61* 6* 4*

102 12 11 10A

106 10 8 13A

108 13 11 10A

110 108 97

110 90 98

109 110 98

Expressive Language Formulated Sentences Recalling Sentences Sentence AssemblyA / Word Structure#

4#*

82* 8 6* 7#

Total Language PPVT-III HPNT (Raw score / 100)

73* 89 94

85 84* 89

Note: # = Level 1 subtest variation; A = Level 2 subtest variation; Standard scores in italics = normal range 85 - 115; Subtest standard score normal range = 7-13.

106

Neurogenic Language Disorders in Children

Table 7 — Individual high-level language and phonological awareness assessment results (represented in standard scores) of Cases 6 - 1 0 treated for posterior fossa tumor on the Test of Problem Solving (TOPS), Test of Word Knowledge (TOWK), Test of Language Competence - Expanded (TLC-E), and Queensland University Inventory of Literacy (QUIL) Tests TOPS

Case 6 79*

Case 7 62*

Case 8 94

Case 9 88

Case 10 100

86 10#

81* 7# 6#*

91 10A 7A

83* 8A 6A*

4*

78* 4*

10A

8#

97 9 10A

88 6* 10A

97 12A 7A 106 11 11A

82*

78*

93

85

101

94 10

76* 7

97 1

65* 3*

94 8

8 73* 6* 5#*

5* 82* 6* 8#

12 100 8 12A

7 6* 6A*

10 118 12 14A

81*

76*

98

69*

106

5* 6* 1 1 9

11 9 9 9

16 12 11

16

8 3* 6* 6* 7 4*

3* 5* 10 11 12 5*

12 12 9 9 12 9 12 10 13 9

TOWK Receptive Composite Synonyms A / Word Opposites # Figurative Usage A / Receptive Vocabulary # Expressive Composite Word Definitions Multiple Contexts A / Expressive Vocabulary # Total TLC-E Interpreting Intents Listening Comprehension: Making Inferences Figurative Language Expressing Intents Ambiguous Sentences Oral Expression: Recreating Sentences'" / Speech Acts# Total QUIL Nonword spelling Nonword reading Syllable identification Syllable segmentation Spoken rhyme Visual Rhyme Spoonerisms Phoneme detection Phoneme segmentation Phoneme manipulation Note: # = Level 1 subtest variation;

A

5#* 81*

76*

6* 11 7 12 10 6* 13

12 11 12 11 12 13 12 11 13

= Level 2 subtest variation; * = below normal range (Standard

scores in italics: normal range 85 - 115; Subtest standard score normal range = 7-13)

A recent MRI of the brain was taken three months prior to language testing and indicated no evidence of recurrence or metastases (see Figure 12). Performance on both the Expressive Language component of the CELF-3, and the expressive subtest, Recalling Sentences, was

Language in Children Treatedfor Posterior Fossa Tumor

107

deemed below the normal range (see Table 6). The Recalling Sentences subtest of the CELF3 is responsible for assessing recall and reproduction of sentence surface structure as a function of syntactic complexity (Semel et al., 1995). All remaining subtests of the CELF-3, as well as the Receptive Language and Total components, were considered intact according to the normative data. Receptive vocabulary abilities as measured by the PPVT-III, were also below the normal range. Naming ability assessed by the HPNT, however, was considered within the normal limits for a child aged six years eleven months.

Figure 12 — Case 7 at language testing (one year seven months post treatment for recurrence): Tl weighted coronal MRI scan revealing evidence of right inferior vermian and cerebeilar tonsil resection via right posterior craniotomy. No locally recurrent soft tissue mass present. No positive mass effect. No tumor cyst in posterior fossa or at craniocervical junction. Also, no mass effect or enhancement above tentorium. Cerebral ventricles are decompressed. In an individual analysis of high-level language and phonological awareness tasks, performance revealed widespread difficulties across the expressive, receptive, and total language components of both the TOWK and the TLC-E, and most subtests (see Table 7). Both the Spoken and Visual Rhyme subtests of the QUIL were also noted to be below the normal range. Case 8. Case 8 was diagnosed with a 6 x 4 x 4 cm juvenile pilocytic astrocytoma in the cerebeilar vermis and hydrocephalus at the age of eleven years ten months (see Figure 13). A six to eight week history of morning nausea and vomiting, headaches, increased clumsiness, and blurred vision preceded diagnosis, with the most recent symptoms prior to diagnosis including unsteadiness on feet and papilloedema. A total resection and third ventriculostomy was carried out. Post-surgical complications included a right high-frequency hearing loss and a significant deterioration in the vision of the left eye. Additionally, increased intracranial

108 Neurogenic Language Disorders in Children pressure, headaches, and bitemporal hemianopia was noted post operatively, which was reported to resolve. Persisting difficulties included truncal ataxia, decreased coordination, right-sided hearing difficulties, left optic atrophy with secondary left visual diplopia.

Figure 13 — Case 8 at diagnosis: Sagittal view MRI scan demonstrating a 6 x 4 x 4 cm juvenile pilocytic astrocytoma in cerebellar vermis. Neuropsychological assessment was carried out both twelve weeks and eleven months following surgery. In the initial assessment following surgical treatment, it was reported that performance was considered in the average range of intellectual functional (verbal average to above average, nonverbal/visual in average range). It was reported that Case 8 generally performed within the normal range on all aspects of cognition and memory, although it was reportedly unknown whether his average performances in these areas represented a relative decline from previous functioning. No reported concerns in academic ability was noted prior to illness, with academic performance considered to be well above the average range (with particular strengths in English and Mathematics). Case 8 was reported to have not experienced any difficulty returning to school. The second neuropsychological evaluation eleven months post surgery also indicated performance in the average range of intellectual functioning, with most areas of performance considered consistent with the previous assessment, or slightly improved. However, certain areas of weakness were also reported with some areas of relative decline from the previous assessment. These included metal arithmetic reasoning abilities (although still in average range), and a relative weakness in speed of information processing (still in average range). At this time Case 8's mother also reported difficulties with concentration, motivation, organization, and task completion. At the age of thirteen years, Case 8 participated in the present study. Testing was carried out one year two months post treatment, and three months following the second neuropsychological testing session. Case 8 had been seen by the Speech Pathology team at the

Language in Children Treated for Posterior Fossa Tumor

109

hospital one year prior to testing for the current study, when language abilities were considered to be within normal limits. In the present study, general and high-level language, and phonological awareness parameters were considered to be well within the normal range (see Tables 6 and 7). Case 9. At the age of six years six months. Case 9 was diagnosed with a large ependymoma located in the fourth ventricle and extending out of the foramen of Magendie into the cisterna magna and partly extending into the cervical canal. Possible invasion of the right cerebellar hemisphere was also reported and obstructive hydrocephalus noted. An eleven month history of headaches, neck stiffness, and photophobia was reported prior to diagnosis. A partial surgical resection was carried out, followed by post-operative complications consisting of a right sixth nerve palsy with a vertical diplopia, and mildly impaired coordination. A six week course of radiotherapy was commenced one month following surgery. A dose of 50Gy was delivered in 25 fractions over 36 days using right and left posterior oblique fields with a smaller volume dose to the site of the residual tumor of a further 5.4 Gy in 3 fractions over 3 days. A ventriculoperitoneal shunt was inserted one month following completion of radiotherapy treatment due to increased intracranial pressure and a three week history of occasional headache, ataxia, cerebellar signs, nystagmus, and mild right facial nerve palsy. Involvement in the present study was carried out at the age of eleven years, four years and one month following treatment completion. Case 9 demonstrated intact general language abilities across all measures of receptive and expressive language, receptive vocabulary, naming (see Table 6). High-level language and phonological awareness assessments, however, revealed performance below the normal range on the Receptive Composite of the TOWK, the receptive subtest Figurative Usage (which may have contributed to an overall reduction in the overall receptive component), and the expressive subtest Word Definitions (see Table 7). More widespread difficulties were noted, however, across both the Expressing Intents and Interpreting Intents components of the TLC-E assessment, and most subtests. Performance on the QUIL, however, indicated abilities within the normal range. Case 11. Case 11 was diagnosed with an ependymoma of the fourth ventricle at the age of two years five months (see Figure 14). Surgical resection was carried and a shunt inserted. Postoperatively a left sixth nerve palsy was reported, as well as residual ataxia and mild rightsided hemiparesis. Two months later, chemotherapy treatment was commenced, with the drugs vincristine, cyclophosphamide, cisplatin, and etoposide employed. A language assessment carried out one month following commencement of chemotherapy noted delays in receptive and expressive language skills and speech skills. Case 11 was reported to perform at an eighteen to twenty-three month old level (at the age of two years eight months), and demonstrated a failure to understand verbs in context, spatial concepts, pronouns, quantity concepts, and recognize actions in pictures. Case 11 demonstrated a similar level of skill in the expressive language component in the use of pronouns, and naming objects and pictures, with an inability to use plural forms, verb + ing, and respond to what/where and yes/no

110 Neurogenic Language Disorders in Children questions. A follow-up assessment session seven months later at the age of three years three months, again reported delays in receptive and expressive language development. At this time, Case 11 was reportedly performing at a 24 to 29 month receptive language level, and failed to comprehend pronouns and descriptive concepts. At an expressive level, Case 11 was experiencing difficulty using verb + ing or possessives, and was only using three to four word sentences. It was also noted that Case 11 tended to substitute words within a related semantic category.

Figure 14 — Case 11 at diagnosis: Axial view MRI scan demonstrating an ependymoma in the fourth ventricle. At the age of three years nine months, Case 11 underwent general language testing for the present study. An MRI taken one month following language testing revealed evidence of recurrence of an ependymoma in the right cerebellar hemisphere, vermis, and right middle cerebellar peduncle (see Figure 15). While performance was considered to be within the normal range across most components of the CELF-Preschool, performance on the expressive subtest, Word Structure, was considered reduced at one standard deviation below the mean (see Table 8). The Word Structure subtest evaluates a child's knowledge and use of early acquired morphological rules and forms (Wiig & Secord, 1992). Although normative data is not available for children below the age of four years six months on the HPNT, it is considered that reduced naming abilities were evident for Case 11 with a score of 55, as the mean accuracy score for the nearest age range, the 4;6-4;ll age category (n=2), was 74.50. High-level language assessments were not conducted due to age requirements.

Language in Children Treatedfor Posterior Fossa Tumor

Ill

Figure 15 — Case 11 at language testing (eight months post treatment): Tl weighted coronal MR] scan revealing evidence of recurrence of ependymoma with a 2.2 cm enhancing mass in right cerebellar hemisphere, vermis, and right middle cerebellar peduncle. No associated hydrocephalus. Table 8 — General Language Assessments Results (represented in Standard Scores) of Case 11 & 12 with Posterior Fossa Tumor, on the Clinical Evaluation of Language Fundamentals - Preschool (CELF-Preschool), Peabody Picture Vocabulary Test - Third Edition (PPVT-HI), and the Hundred Pictures Naming Test (HPNT) Tests CELF-Preschool Receptive Language Linguistic Concepts Basic Concepts Sentence Structure

Case 11

Case 12

95 8 8 10

98 12 9 8

Expressive Language Recalling Sentences in Context Formulating Labels Word Structure

85 9 9 4*

100 11 8 11

Total Language

89

99

PPVT-III HPNT (Raw score /100)

87 55*

107 89

Note: Standard scores in italics = normal range 85 - 115; Subtest standard score normal range = 7-13.

112

Neurogenic Language Disorders in Children

DISCUSSION A group comparison between twelve children treated for posterior fossa tumor and their individually matched peers revealed significantly reduced performance on measures of general language in both receptive and expressive language, as well as at an overall language level indicated by the Total Language score. Receptive vocabulary skills on the PPVT-III were also noted to be significantly reduced compared to the control group. Naming abilities, however, were not considered significantly different. Reports of reduced receptive language (including receptive vocabulary) and expressive language in a group of children treated for posterior fossa tumor have been previously noted by Hudson, Murdoch and colleagues (Hudson & Murdoch, 1992a; Murdoch & Hudson-Tennent, 1994; Murdoch & Hudson, 1999a). Results of a group comparison between ten children treated for posterior fossa tumor and ten control participants matched for age and gender revealed significant differences across all measures of higher-level language in the areas of problem solving (TOPS), word and concept knowledge (TOWK), and abstract and complex linguistic structures (TLC-E). As mentioned previously, Hudson and Murdoch (1992a) and Murdoch and Hudson-Tennent (1994) are the only authors to date that have investigated the high-level language abilities of children treated for posterior fossa tumor. These researchers noted deficits in the ability to understand and manipulate complex and abstract language structures (Hudson & Murdoch, 1992a). Research evidence of high-level language and cognitive deficits in children with disturbances to the posterior fossa is supported by recent clinical and functional neuroimaging evidence implicating the cerebellum in these domains (Muller et al, 1998; Riva, 1998, 2000; Riva & Giorgi, 2000a, b). Results from the present study indicating reduced performance of high-level language abilities across areas involving problem solving, high-level semantic word and concept knowledge, and abstract and complex language structures in children treated for posterior fossa tumor may therefore be considered in the context of direct impact of a tumor in the cerebellum. Indeed, clinical findings relating to impaired higher language abilities following cerebellar disturbances, including tumor, have been previously documented. Riva and Giorgi (2000a) reported reduced thinking flexibility and problem solving in groups of children with left or right cerebellar involvement. Additionally, both Schatz et al. (1998) and Riva and Giorgi (2000a) reported deficits in verbal processing and complex language tasks in patients with cerebellar damage. A case study presented by Riva (1998) indicated a severely impaired ability to produce complex language structures following a viral inflammatory lesion in the cerebellum. Impairments in executive function and higher-order behaviour were also reported by Levisohn et al. (2000), in an examination of nineteen children who had undergone surgery for a cerebellar tumor in the absence of either radiotherapy or chemotherapy. Examination of twenty children treated for posterior fossa tumor at both group level and individual case level revealed patterns of individual variability were evident in reports by

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Hudson and colleagues (Hudson & Murdoch, 1992a; Murdoch & Hudson-Tennent, 1994). Such previously reported variability was also noted in the present study. Despite an overall reduction in performance as a group on both Receptive and Expressive Language components of the CELF-3 (and the Total Language score) and receptive vocabulary abilities on the PPVT-III, specific general language impairments were noted in just three of the twelve children with posterior fossa (Cases 6, 7. and 11). Across high-level language parameters, global reductions in group performance was demonstrated despite global high-level language impairments noted in just three of the ten participants (Cases 6, 7, and 9). Specific weaknesses in areas such as problem solving (Cases 2 and 5) and lexical knowledge (Case 3), however, were demonstrated by an additional three cases. Phonological awareness deficits ranging from mild to severe were noted in the profiles of five of the ten children examined (Cases 3, 4, 6, 7 and 8), despite being commensurate with their individually matched peers at a group level. It was noted that in the profiles of all three participants with identified general language performance (Cases 6, 7, and 11), that most of the demonstrated areas of difficulty were represented by expressive language deficits. In particular, Case 6, who exhibited difficulty across the greatest number of expressive tasks (all expressive language subtests of the CELF3, the Expressive Language Score, and Total Language Score), yielded the most reduced scores, such that performance on the Expressive Language component was more than two standard deviations below the mean. Murdoch and Hudson-Tennent (1994) also noted reduced performance by six children with posterior fossa tumor in expressive semantic and /or syntactic tasks. More recently, researchers investigating the presence of language disorders associated with cerebellar damage have also noted particular dysfunction in expressive language (Riva, 1998; Levisohn et al, 2000; Riva & Giorgi, 2000b). Syntax was also noted to be a predominant area of weakness represented by performance across subtests of the CELF-3/Preschool in all three cases with demonstrated general language deficits (Cases 6, 7, and 11). Difficulties specifically in the area of syntax are particularly prevalent across cerebellar clinical studies specifically investigating the role of the cerebellum in language and cognitive function (Silveri et al, 1994; Marien et al, 1996; Molinari et al, 1997; Schmahmann & Sherman, 1998; Gasparini et al, 1999; Fabbro et al, 2000; Marien et al, 2000; Riva & Giorgi 2000b; Silveri & Misciagna, 2000). In an examination of four patients with varying tumor types located in the cerebellum (including the right cerebellar hemisphere, the left cerebellar hemisphere, the vermis, and the superior vermis), Fabbro et al. (2000) recognised syntax as the most compromised language feature in all cases. In the context of an expressive aphasic syndrome, a patient with a history of ischemic infarction in the vascular territory of the right arteria cerebellaris superior was also noted by Marien et al. (2000; 1996) to have particularly impaired syntactic abilities at both a comprehension and expressive level, together with reduced verbal output, perseverations, word-finding difficulties, decreased speech rate, and lack of content words. Difficulties were also exhibited by seven children of the twenty children with posterior fossa tumor (Murdoch & Hudson-Tennent, 1994). Residual impaired syntactic abilities were also noted in the profile

114 Neurogenic Language Disorders in Children

of the only participant with a tumor (posterior fossa), in a group of brain injured children with acquired language disorders examined by Cooper and Flowers (1987). Although as a group, naming difficulties were not observed to be significantly reduced in comparison to an individually matched control group, at an individual level severe naming difficulties were observed in one participant (Case 11). Such a severe disturbance representing abilities that were two standard deviations below the normal range existed in the presence of generally intact skills, except for a specifically reduced subtest score in the area of expressive syntax. As previously mentioned, both Hudson and Murdoch (1992a) and Hudson-Tennent and Murdoch (1993) failed to find evidence of naming difficulties at a group level in their studies of children with posterior fossa tumor. However, in their individual examination of these same twenty children, Murdoch and Hudson-Tennent (1994) found that seven cases performed poorly on assessments measuring naming ability. Recent studies examining language disorders following cerebellar damage have also noted naming difficulties in these populations (Akshoomoff et al, 1992; Marien et al., 1996; Beldarrain et al., 1997; Schmahmann & Sherman, 1998; Gasparini et al., 1999; Marien et al., 2000; Riva & Giorgi, 2000a). In a study investigating the language and cognitive abilities of twenty-six children following removal of cerebellar tumor by Riva and Giorgi (2000b), a slight worsening in naming was noted to be associated with cerebellar damage to the hemispheres, regardless of laterality. The significant naming difficulties experienced by Case 11 in the present study may reflect the impact of a recurrent tumor at the time of testing on right cerebellar hemispheric function. Examination of the individual high-level language abilities of children treated for posterior fossa revealed that three of the ten participants (Cases 6, 7 and 9) demonstrated global deficits across most areas of high-level language. Of these participants, Cases 6 and 7 were noted to demonstrate difficulties in both general and high-level language. Furthermore, a pattern demonstrating particular expressive language weaknesses on high-level tasks followed a similar pattern in the general language profile of Case 6. While Case 7 demonstrated less severity of general language deficit than Case 6, with scattered mild-moderate difficulties in expressive syntax at a general level, Case 7 demonstrated the most severe global impairment in high-level language ability. In contrast to Cases 6 and 7, however, Case 9 demonstrated no general language deficits in general language ability despite quite widespread difficulties evident across assessments of high-level language in the present analysis. Therefore, it is significant that no evidence in the general language profile of this case indicated a need for either further assessment or signalled the severity of difficulties in this area of high-level language. In addition to the three patients with high-level language global deficits, three additional cases with no previous general language difficulties (Cases 2, 3, and 5) also demonstrated some specific disturbances to this level of language. Case 3 performed below the normal range on both the Expressive Composite of the TOWK and the Expressing Intents section of the TLC-E, with one expressive subtest below the normal range on each assessment (Word Definitions (TOWK) and Oral Expression: Recreating Speech Sentences (TLC-E)). It is

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suggested that as the scores for each of these two subtests were severely reduced, the overall expressive scores were adversely impacted by both subtests respectively. The Word Definitions subtest of the TOWK assesses the ability to provide definitions that include category membership and semantic features, whereas the Oral Expression subtest in Level 2 of the TLC-E addresses the ability to recreate intent-driven complex sentences that incorporate lexical items and respond to situational contexts. Both of these assessments involve the ability to retrieve and demonstrate the complexities of lexical knowledge and present this in context in a sentence form. Therefore, it is evident that Case 3 experienced specific difficulty in this area. In the present analysis, Cases 2 and 5 were the only two cases to demonstrate intact language in all areas except the specific area of problem solving. It was noted, however, that both Cases 2 and 5 shared a similar tumor location within the cerebellar hemispheres (right cerebellar hemisphere and the inferior vermis / left hemisphere respectively). As mentioned previously, Riva and Giorgi (2000a, b) reported that children with right or left hemispheric involvement exhibited reduced abilities in thinking flexibility and problem solving subsequent to an examination of the specific functions of both cerebellar hemispheres and the vermis in cognition, language, and executive functions of children who had undergone surgical removal of a tumor in these areas. As both Case 2 and 5 underwent total and near total tumor removal respectively in these critical areas, it is suggested that the observed disturbances to problem solving may be related to damage to the cerebellar structures. Other cases with disturbances to problem solving included Cases 6 and 7, who also experienced quite widespread impairment across most high-level language tasks, with tumor locations in the fourth ventricle. It must also be acknowledged that Case 8, who also had a tumor located in the vermis, did not experience problem solving difficulties in the present study. It was also noted that both Cases 2 and 5 participated in the present study at six months post treatment. Therefore, as has been suggested previously, while an impairment was evident in this specific area of problem solving only six months following treatment, the potential for these cases to develop more widespread difficulties in high-level language may exist due to evidence of neuropathological changes occurring from six months up to twenty years later, including radionecrosis, white matter density, intracerebral calcifications, cerebral atrophy, and ventricular and subarachnoid dilation (Arya et ai, 1986; Hoppe-Hirsch, 1993; Plowman, 1992). Variable findings in the present study demonstrating reduced general receptive and expressive language abilities as well as overall high-level language reductions at the group level, in addition to both global high-level language impairments and specific areas in either general or high-level language at an individual level, may be attributable to any one or a combination of varied factors that are present in the current group of children with posterior fossa tumor. These factors include tumor type, tumor location, treatment and/or combinations of treatments employed, treatment complications/effects, age at diagnosis/treatment, the cooccurrence of hydrocephalus, and other associated symptoms, and have been recognized to significantly impact general language ability in children with posterior fossa tumor,

116 Neurogenic Language Disorders in Children

particularly in children undergoing radiotherapy treatment (Murdoch & Hudson, 1999a, b). In fact, the variability in individual findings described is also not surprising given the inconsistency of factors between each case (Murdoch & Hudson, 1999c). It is suggested that all of the possible factors existing in the presentation and management of children with posterior fossa may play a part in contributing to the presence of language deficits. It is of interest that all five cases with a posterior fossa ependymoma (Cases 2, 6, 7, 9, and 11) presented with some form of language disturbance, accounting for all children with general language deficits and all cases with global high-level language impairment. Additionally, the ependymoma in four of the five children (Cases 6, 7, 9, and 11) had arisen in the fourth ventricle, a commonly reported location for this tumor type (Cohen el al, 1982; Gumbinas, 1983; van Eys, 1991; Plowman, 1992). Due to a characteristic presentation of the ependymoma as a space-occupying mass, the most common clinical findings are those resulting from increased intracranial pressure, including nausea, vomiting, headaches, and obstructive hydrocephalus (Wilson, 1975; Gumbinas, 1983; van Eys, 1991; Plowman, 1992; Heideman et al, 1993). Severe obstructive and persisting hydrocephalus was evident in all three cases with global high-level language impairment, with symptoms evident in all five children. Long-term and later developing effects resulting from hydrocephalus have been reported by several authors and included effects on cognition (Wilson, 1975; Danoff et al, 1982; McWhirter & Masel, 1987; Silverman & Thomas, 1990; van Eys, 1991). A study by Danoff el al. (1982) documented an increase in the incidence of intellectual impairment occurring in children treated for brain tumor who had presented with hydrocephalus compared to those who did not. Murdoch and Hudson-Tennent (1994) considered the presence of hydrocephalus to be associated with language disturbances in their twenty cases with posterior fossa tumor. The use of shunts to treat hydrocephalus in children with posterior fossa tumor (as in Cases 6 and 11) was also examined by these authors, although the influences of this treatment strategy on language function were considered unclear. Therefore, it is possible that the severe and persisting long-term nature of the hydrocephalus in at least three of the five cases due to an ependymoma in the fourth ventricle (Cases 6, 7. and 9) was a factor contributing to the widespread and more severe reduction in performance across all high-level language tasks observed, and the presence of increased intracranial pressure in the remaining two instances related to specific language disturbances in general. However, recent advances in the understanding of connections of the cerebellum to the language centres of the cerebral cortex may indicate the potential of a more direct impact by a tumor located in the posterior fossa. The site of the recurring tumor in Case 11 was noted to involve the right cerebellar hemisphere, the vermis, and the right cerebellar peduncle. As previously mentioned, it has been reported that critical areas of the cerebellum recently noted to be involved in language function include the right cerebellar hemisphere and the vermis (Oki et al, 1999; Riva, 2000; Riva & Giorgi, 2000a, b; Scott et al, 2001), and may account for the severely reduced naming difficulties in this case. As previously mentioned, naming and word finding difficulties have been commonly reported to be associated with disruptions to the cerebellum,

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1 17

particularly the right hemisphere and vermis (Akshoomoff et al. 1992; Marien et al, 1996; Beldarrain el al, 1997; Schmahmann & Sherman, 1998; Gasparini et al, 1999; Marien et al, 2000). Due to the potential for an ependymoma to be locally infiltrative with a tendency for dissemination via the cerebrospinal fluid (Cohen et al, 1982; Gumbinas. 1983; Segall et al, 1985; van Eys, 1991; Plowman, 1992; Tait et al, 1992; Heideman et al, 1993), together with its comparatively reduced prognostic favorability, treatment is often more aggressive for this type of tumor (e.g. higher dosages of radiotherapy or chemotherapy, more combinations of treatment techniques, more heroic attempts at surgical removal), as it is often recommended that adjuvant treatment is necessary in combination with surgical intervention in cases of ependymoma (Cohen et al, 1982). This is highlighted by the use of post-operative radiotherapy or chemotherapy in all five cases with ependymoma and some degree of language difficulties. While Cases 6 and 11 were treated with surgery followed by an intensive chemotherapeutic program, Cases 2, 7 and 9 underwent radiotherapy subsequent to surgical intervention. It is therefore also suggested that the intensive treatments employed may have also contributed to the profiles noted, as the effects of chemotherapy and radiotherapy on language and cognitive function have been well-documented (Cohen et al, 1982; Arya et al, 1986; Di Chiro et al, 1988; Hudson et al, 1989; Barrett & Donaldson, 1992; Heideman et al, 1993; Kun & Moulder, 1993; Murdoch et al, 1999) and explored in the present study. Therefore, the necessity of careful long-term monitoring of the high-level abilities of children treated with radiotherapy for posterior fossa tumor is highlighted. Case 3, who demonstrated specific high-level deficits, also received radiotherapy treatment following surgical intervention. Additionally, Case 3 was one of two cases in this analysis to have presented with a medulloblastoma, with the site identified as directly posterior to the fourth ventricle, and is only child with this tumor type to have been treated with radiotherapy following surgery. The other case with a medulloblastoma, Case 1, however, also received radiotherapy and did not experience any difficulties on both high-level or general language tasks. The presence of increased intracranial pressure in cases of medulloblastoma is considered a common finding due to compression of the fourth ventricle (Segall et al, 1985; Neidhardt el al, 1986; van Eys, 1991; Plowman, 1992; Heideman et al, 1993). While signs of increased intracranial pressure are reportedly seen early, these nonspecific findings may be intermittent and subtle. Therefore, the possibility of these symptoms being overlooked and the duration of symptoms occurring three or more months prior to diagnosis is within the realms of possibility (Heideman et al, 1993). It is suggested that the long-term presence of increased intracranial pressure evident in Case 3 prior to diagnosis may have been responsible for exerting prolonged effects on cerebellar function that contributed to disturbances to high-level language. Findings of long-term effects associated with prolonged increased intracranial pressure have been reported by several authors (Wilson, 1975; Danoff et al, 1982; McWhirter & Masel, 1987; Maria & Halpern, 1989; Silverman & Thomas, 1990; van Eys, 1991).

118 Neurogenic Language Disorders in Children

It was noted in the present study that all three cases with demonstrated language impairment (Cases 6, 7, and 11), two of who also exhibited global high-level language impairment, were initially diagnosed and subsequently treated under the age of three years. Although a recurrent tumor had been noted at the time of testing for Case 11, treatment had not yet been carried out and is therefore exempt from the present consideration of treatment effects. Therefore, it is suggested that the factor of very young age in these three cases may have led to the occurrence of the general language deficits observed, due to reports that effects of treatment, particularly radiotherapy, are more serious in very young children (van Eys, 1991). Young age at tumor diagnosis has been noted by several authors to be directly linked to impaired neuropsychological functioning and intellectual dysfunction (Alajouanine & Lhermitte, 1965; Mulhern et al, 1992; Broadbent et al, 1981; Dennis el al., 1996). In a retrospective study by Sue el al. (1990), examining twenty children who had been diagnosed with a brain tumor under the age of three, eighteen cases were noted to have exhibited adverse sequelae. Impaired cognitive function was reported in 85% of the children examined, neurological sequelae in 65%, and central endocrinopathies in 70%. All three cases diagnosed under the age of three years in the present study were also treated with surgical intervention prior to radiotherapy or chemotherapy. While age at surgical treatment was not considered a strong predictor of IQ performance in a study by Kao el al. (1994), some associated declines in intellectual function were noted. Surgery was also noted by Sue et al (1990) to be a possible cause of the late effects observed in their study of children under three years of age. In contrast, however, Levisohn et al. (2000) reported that younger children treated with surgery were less likely to exhibit neuropsychological deficits (demonstrated in 33 % of children under age seven compared to 80% of children aged over seven years). Therefore, it is possible other factors such as radiotherapy or chemotherapy following surgery may have been a contributing factor in the deficits observed in these participants than the surgery itself. Such a suggestion receives some support in the present study by an absence of a general language impairment in Case 4, who was diagnosed and subsequently treated under the age of three years for a posterior fossa choroid plexus papilloma with surgery only. However, it must be noted that ongoing speech pathology intervention from the time of diagnosis until involvement in the present study included monitoring of general language abilities, with some mild difficulty in expressive semantics and sentence formulation noted two years prior to involvement in the present study. The most prevalent information regarding the adverse impact of young age on cognitive, neuropsychological, and language function, however, is related to the use of radiotherapy (Danoff et al, 1982; Duffner et al., 1983; Silverman et al, 1984; van Eys, 1991; Barrett & Donaldson, 1992; Plowman, 1992; Tait et al, 1992; Heideman et al, 1993; Hoppe-Hirsch, 1993; Kun & Moulder, 1993;). Case 7 was treated by radiotherapy subsequent to surgery and exhibited the most severe language deficits out of all twelve subjects examined in the present study. It is acknowledged that prior to involvement in the present study Case 7 had been treated for both an initial tumor and a subsequent recurrence. Initial treatment involved surgery followed by radiotherapy, with surgical removal of the recurred tumor. Therefore, not

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only did this case undergo radiotherapy for treatment of posterior fossa tumor with its known associated language effects, Case 7 also underwent surgical intervention twice. While repeat craniotomy was noted by Kao et al, 1994 to be strongly associated with declines in IQ scores, and may explain similar findings related to language in Case 7, a case described by Murdoch and Hudson-Tennent (1994) who also underwent two craniotomies (second to remove residual tumor five weeks following initial surgery), did not display evidence of general language difficulties. Packer et al. (1986) indicated that the immature brain is more susceptible to the effects of radiation due to axonal growth, dendriatic arborization and synaptogenesis occurring in the early years of life. In fact according to Sue el al. (1990) irradiation was clearly responsible for intellectual sequelae in seven of the twenty children treated for brain tumors under the age of three in their study. These authors concluded that the high rate of intellectual impairment was consistent with the concept that radiotherapy is very hazardous before the age of three. Considering the disruption to higher functions of intelligence documented in children, it could be reasonably expected that the adverse impact on the language abilities of the children in the present study noted to be under age three years at the time of diagnosis were related to age. It is noteworthy, however, that Cases 2, 3, and 9, also underwent radiotherapy as part of their treatment program and while did not exhibit general language difficulties, all demonstrated disturbances of varying degrees to high-level language abilities (Danoff et al, 1982; Duffner et al, 1983; Silverman et al, 1984; van Eys, 1991; Barrett & Donaldson, 1992; Plowman, 1992; Tait et al, 1992; Heideman et al, 1993; Hoppe-Hirsch, 1993; Kun & Moulder, 1993). Irrespective of age, however, both cases (Cases 6 and 11) treated with chemotherapy following surgery exhibited language disturbances. While the effects across areas of language varied from specific difficulties to widespread impairment, the degree of these disturbances were noted to be consistently severe in both cases. Adverse effects on brain structure, cognition, and language function have been reported in populations of children treated with chemotherapy irrespective of age (Murdoch el al, 1999). Effects resulting from chemotherapy treatment have been considered to be able to be examined more definitively when examined in populations of children treated for acute lymphoblastic leukaemia. It is suggested that as chemotherapy is often used in isolation, or with minimal radiation dosages, findings may be more clearly attributed to chemotherapy than in populations of children with brain tumor (Murdoch et al, 1999). The phonological awareness abilities of children treated for posterior fossa tumor were also explored in the present analysis. Despite previous reports indicating deficits in the overlying literacy manifestations of reading and writing in populations of children with brain trauma, inclusive of tumor (Hecaen, 1976; Cooper & Flowers, 1987; Van Dongen et al, 1995), no significant differences were evident between the present group of children treated for posterior fossa tumor and their individually matched peers with respect to phonological awareness skills. These results relate to the findings of Hudson and Murdoch (1992a), who found no significant differences between a group of six children treated for posterior fossa tumor and a control group, on measures of both reading and writing.

120 Neurogenic Language Disorders in Children At an individual level, however, some deficits were noted in the children treated for posterior fossa tumor. Similar to the presentation of widespread difficulties in high-level language, Case 6 also demonstrated extensive difficulties in phonological awareness. Severe deficits were demonstrated in both the Visual Rhyme and Phoneme Manipulation subtests. Other areas of weakness included Nonword Spelling and Nonword Reading, Spoonerisms, and Phoneme Detection. Cases 3, 4, and 7, however, presented with more specific areas of weakness, as all three cases demonstrated difficulties specifically in the area of rhyme, as assessed by the Spoken and Visual Rhyme subtests. In fact, reduced performance in the area of rhyme was the only area of difficulty observed across all assessments inclusive of general and high-level language and phonological awareness in the profile of Case 4. It was also noted that while Case 6 did experience many difficulties in the area of literacy, the most severe impairment observed was evident on the Visual Rhyme subtest. On the basis of this preliminary pattern, it is suggested that rhyme may present as an area of weakness in the phonological awareness skills of children treated for posterior fossa tumor, and warrants further investigation in this population. Particular difficulty in the Phoneme Manipulation subtest by two cases was also noted. Case 6 and 7 were observed to perform poorly on this subtest Case 8, however, experienced difficulty in the area of segmentation, with reduced performance on both the Syllable Segmentation and Phoneme Segmentation subtests. It is possible that due to an absence of any other difficulties across all measures of general and high-level language assessments and other literacy subtests, Case 8 may have experienced difficulty

understanding the

requirements of the tasks involving segmentation. It is suggested that as phonological awareness skills are recognised to provide the foundation for the development of literacy abilities such as reading, spelling, and writing (e.g. Kahmi & Catts, 1991; MacDonald & Cornwall, 1995; Stackhouse & Wells, 1997), these findings highlight the potential for reduced phonological awareness skills to lead to possible impaired abilities in these areas. As few previous studies have specifically investigated the contributing factors that may result in impaired pre-literacy or literacy skills in these populations, it is suggested from the present study that location, as well as associated factors such as hydrocephalus or post surgical management, may also impact on the development phonological awareness skills. The impact of location is supported by an examination of fiftyfive children with dyslexia and their matched control participants by Fawcett el al. (1996), in which cerebellar impairment was considered to be associated with dyslexia. However, it must also be considered that periods of hospitalization in this population also occur and may somewhat result from disturbances to schooling and therefore, the manifestation of these types of disturbances. More indepth investigations, however, are required to further clarify patterns of deficits and the contribution of specific tumor location on this skill.

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CONCLUSION The present study confirmed the presence of both general and high-level language deficits at a group level in the performance of children treated for posterior fossa tumor. At an individual level three children demonstrated evidence of specific general language deficit, largely in the area of expressive language and syntax. Global high-level language deficits were noted in three of ten participants, as well as more specific and subtle areas of high-level language impairment (expressive semantic and lexical knowledge and problems solving) noted in three additional cases. Contributing factors noted included direct involvement of tumor location on cerebellar connections involved in language function, fourth ventricle tumor location and the indirect impact of hydrocephalus, tumor type, young age at diagnosis / treatment, and treatment effects such as those associated with radiotherapy or chemotherapy. It was highlighted that children with no initial observed general language difficulties in the acute phase post management be monitored long-term. The present analysis also highlighted the importance of investigating high-level language abilities in this population in the presence of intact general language, due to observed high-level language abilities in children who did not present with any evidence of general language deficits. Individual deficits identified in 50% of the group children highlights the need for further analysis of both the pre-literacy awareness and later literacy abilities of children treated for posterior fossa tumor.

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124 Neurogenic Language Disorders in Children McWhirter, W. R. and J. P. Masel (1987). Paediatric Oncology: An Illustrated Introduction. Williams & Wilkins and Associates Pty Limited, Sydney. Molinari, M , M. G. Leggio and M. C. Silveri (1997). Verbal fluency and agrammatism. Int Rev Neurobiol, 41, 325-339. Mulhern, R. K., J. Hancock, D. Fairclough, and L. Kun (1992). Neuropscyhological status of children treated for brain tumors: a critical review and integrative analysis. Med Pediatr Oncol, 20, 181 -191. Muller, R., H. T. Chugani, O. Muzik, and T. J. Mangner (1998). Brain organization of motor and language functions following hemispherectomy: a [ l5 O]-water positron emission tomography study. Child Neurol, 13, 16-22. Murdoch, B. E. and L. J. Hudson (1999a). Language disorders in children treated for brain tumors. In: Communication Disorders in Childhood Cancer (B. E. Murdoch, ed.), pp. 55-75. Whurr Publishers, London. Murdoch, B. E. and L. J. Hudson (1999b). Language recovery following treatment for paediatric brain tumors. In: Communication Disorders in Childhood Cancer (B. E. Murdoch, ed.), pp. 76-88. Whurr Publishers, London. Murdoch, B. E. and L. J. Hudson (1999c). Variability in patterns of language impairment in children following treatment for posterior fossa tumor. In: Communication

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Sue, E., C. Kalifa, R. Brauner, J. L. Habrand, M. J. Terrier-Lacombe, G. Vassal, et al. (1990). Brain tumors under the age of three. The price of survival: a retrospective study of 20 long-term survivors. Ada Neurochir, 106, 93-98. Tait, D. M., C. C. Bailey, and M. M. Cameron (1992). Tumors of the central nervous system. In: Cancer in Children: Clinical Management (P. A. Voute, A. Barrett & J. Lemerle, eds.), Third Revised Ed., pp. 184-206. Berlin: Springer-Verlag. van Eys, J. (1991). Malignant tumors of the central nervous system. In: Clinical Pediatric Oncology (D. J. Fernbach & T. J. Vietti, eds.), Fourth Ed., pp. 409-426. Mosby - Year Book, Inc., St.Louis. Van ongen, H. R., M. C. B. Loonen, and K. J. VanDongen (1985). Anatomical basis for acquired fluent aphasia in children. Ann Neurol, 17, 306-309. Wiig, E. H. and M. Secord (1989). Test of Language Competence - Expanded Edition. The Psychological Corporation: San Antonio. Wiig, E. H. and M. Secord (1992). Test of Word Knowledge. The Psychological Corporation, San Antonio. Wiig, E. H., W. A. Secord and E. Semel (1992). Clinical Evaluation of Language Fundamentals - Preschool. The Psychological Corporation, San Antonio. Wilson, C. B. (1975). Diagnosis and surgical treatment of childhood brain tumors. Cancer, 35, 950-956. Zachman, L., M. Barrett, R. Huisingh, J. Orman and C. Blagden (1991). Test of Problem Solving - Adolescent. LinguiSystems, East Moline. Zachman, L., R. Huisingh, M. Barrett, J. Orman, and C. LoGiudice (1994). Test of Problem Solving - Elementary, Revised. LinguiSystems, East Moline.

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8

LANGUAGE DEVELOPMENT IN CHILDREN WITH CEREBELLAR MALFORMATIONS Renato Borgatti, Alessandro Tavano, Guido Cristofori and Franco Fabbro "E.Medea " Scientific Institute, Polo del Friuli Venezia Giulia and Bosisio Parini (LC), Italy University ofUdine, Italy

Abstract We investigated language development in three participants with cerebellar malformations. The extent of the lesions varies from near total absence of the cerebellum to hypoplasia of one cerebellar hemisphere. The effect of cerebellar malformations on language development is not yet known. Acquired focal cerebellar lesions in adults may determine mild expressive language deficits, which tend to regress rather rapidly over time. However, subtle deficits may persist. We show that malformations localized to one or both cerebellar hemispheres and to the vermis may result in permanent receptive and expressive language deficits. The degree of impairment varies from subtle deficits (e.g., right cerebellar hypoplasia) to severe disorders of language and communication (autistic-like behavior associated to vermal hypoplasia). However, we document that near total absence of the cerebellum does not prevent general cognitive functioning and language acquisition to a sufficient extent. Considerations about the plasticity of the human brain suggest that cortical and subcortical mechanisms may compensate for the cerebellar contribution to language to a considerable extent. Key words: cerebellum, cerebellar malformations, cerebellar aplasia, language development

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INTRODUCTION Over the last 20 years, besides being attributed a major role in mediating motor functions (Dow & Moruzzi, 1958), the cerebellum has been consistently involved in the modulation of non-motor functions (Leiner et al, 1986; Leiner et al, 1991; Schmahmann, 1991; Fiez, 1996; Fabbro, 2000). Recently, Schmahmann and Sherman (1998) identified a "Cerebellar Cognitive Affective Syndrome" in a group of adult patients with acquired cerebellar lesions. This syndrome is characterized by: 1) impairment of executive functions; 2) impaired spatial cognition; 3) affect change; and 4) expressive linguistic deficits. Investigations involving children with acquired cerebellar lesions showed a similar pattern of deficits (Levinsohn et al, 2000; Riva & Giorgi, 2000). Levinsohn et al. (2000) studied 19 children who underwent excision of cerebellar tumor. Results showed that younger children were the least likely to show deficits in language, cognition or affect. Similarly, Riva and Giorgi (2000) studied 26 children who underwent surgery for cerebellar hemisphere or vermal tumor. Vermal lesions determined two different outcomes: 1) postsurgical mutism, which evolved into speech or expressive language disorders similar to agrammatism; 2) disturbances of social and communicative skills, ranging from irritability to autistic-like behavior. Excision of tumors confined to the cerebellar hemispheres led to selective language deficits. Children with right cerebellar tumors presented with disturbances of auditory sequential memory and language disorders, particularly on the expressive side, as is reflected by low MLU scores (mean length of utterance), an index of expressive grammar (cf. the Methods section). Children with left cerebellar tumors showed a marked impairment in lexical access but on tasks tapping comprehension and expressive skills. They also showed a less marked decrease in executive functions than children with right cerebellar tumors. In a review of studies on acquired cerebellar hemisphere lesion and subsequent language disturbances in adults, Marien et al. (2001) argued for language lateralization in the right cerebellar hemisphere pointing out an involvement of the right cerebellar hemisphere in: 1) verbal working memory; 2) articulatory planning; 3) semantic and phonological word retrieval; 4) syntactic processing. Some neuroimaging data seem to support this proposal. Patterns of cerebellar and cortical (notably Broca's area and Supplementary Motor Area, SMA) activation have been documented in healthy participants performing a word association task, namely producing appropriate verbs for given nouns (Petersen et al, 1989; Petersen & Fiez, 1993; Desmond & Fiez, 1998). At the neuroanatomical level, the cerebellum has extensive input and output connections to the frontal and prefrontal cortices (so-called 'Frontal lobe system'). Input connections run from association areas in the frontal, temporal and parietal lobes through the pontine nuclei and the red nucleus - inferior olive system (Leiner et al, 1993). Output connections to the frontal and prefrontal cortices (Broca's area, SMA) run through the thalamus, in particular the ventrolateral, ventral-anterior and centromedian nuclei (Leiner et al, 1993). Cerebrocerebellar connections are organized in a crossed pattern, whereby the right cerebellar hemisphere is connected to the left cerebral hemisphere,

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and the left cerebellar hemisphere is connected to the right cerebral hemisphere. Based on these considerations, some researchers have mentioned the phenomenon of 'crossed cerebello-cerebral diaschisis' to explain the development of expressive agrammatic and expressive-receptive syndromes following right cerebellar hemisphere damage (Fabbro et al, 2000a; Marien et al, 1996; Molinari et al. 1997; Silveri et al, 1994). An important issue is that the extent of expressive agrammatic symptoms following acquired cerebellar vascular lesions tends to regress rapidly over time (Marien et al., 2000; Silveri et al., 1998). The phenomenon of 'crossed cerebello-cerebral diaschisis' is a temporary functional deactivation of frontal lobe areas subsequent to damage to contralateral cerebellar hemisphere. As neurofunctional activation becomes normal, language deficits rapidly regress in severity and extent. Another important issue is that language deficits following cerebellar damage are sometimes difficult to detect through administration of formal language tests. They can become manifest at a qualitative analysis of spontaneous or descriptive speech (Fabbro et al., 2004). Zettin et al. (1997) described the case of a 46-year-old highly educated right-handed patient who developed severe expressive agrammatism (omission of function words) after a hemorrhagic stroke involving the right cerebellar hemisphere. However, such deficit was manifest only in spontaneous speech and the patient is reported to have fully recovered language three months post-onset. Besides rapidity in regression over time and limitations in deficit extent, this finding outlines a third important issue, that is the possible persistency of residual linguistic difficulties. Unlike the patient studied by Zettin et al. (1997), the patients studied by Fabbro et al. (2004) showed minor linguistic deficits that were still detectable many years after insult. The patients were aware of such difficulties and their impairing effect on daily activities and working abilities, hi conclusion, although subtle and transient, language disorders following acquired focal or large cerebellar lesions point to some involvement of the cerebellum in language processing (Fabbro, 2000). The effects of cerebellar aplasia or hypoplasia on higher order cognitive functions are yet to be investigated. As for language, two main issues may be raised. First, there are no available data about the influence of cerebellar malformations on language acquisition. Malformation-associated cerebellar lesions are likely to induce a consistent reorganization of cerebello-cortical connections. Notably, the cerebellum seems to partly sustain the acquisition and processing of procedural aspects of language such as phonological and morphosyntactic rules (Molinari et al, 1997b; Ullman, 2001). Therefore, malfonnative lesions may delay or disrupt normal language acquisition patterns. Second, it is not known whether malformations affecting single cerebellar structures have differential effects on language acquisition. In the case of near total absence of the cerebellum - indeed, a very rare event - the few case studies reported in the literature (Stewart, 1956; Sener & Jinkins, 1993; Gardner et al., 2001) documented that initially patients show a very marked delay in development but slowly and steadily recover motor, affective and cognitive functions. However, these studies lack detailed information on language development and language skills in adult age. Linguistic and communicative outcomes of other types of cerebellar malformations show great variability

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depending, for example, on the extent of vermian involvement. A more important involvement of the vermis seems to be linked to severe pervasive impairments in social and communication skills (autism or autistic-like behavior), although mainly neuropsychological and linguistic deficits have been described (Gilberg & Coleman, 1992; Courchesne, 1997). In this study we discuss the general development and, in particular, language development in three patients with cerebellar malformations, ranging in localization and extent from near total absence of the cerebellum to a large malformative lesion limited to the right cerebellar hemisphere. Our aim is to provide some preliminary answers to the following three questions: 1) Is the cerebellum involved in language acquisition? 2) What is the effect of malformative lesions on language acquisition and language development in adult age? 3) What are the characteristics of language deficits associated to cerebellar malformations?

METHODS Participants Three participants were selected from a pool of 20 patients (15 adults, 5 children) who were referred to the "E. Medea" Scientific Institute in Bosisio Parini (Lecco - Italy) over a 13-year period (1991-2003). The pool of 20 patients was selected among a total number of 156 participants with cerebellar lesions of different etiology. Exclusion criteria were: 1) suspected perinatal cerebellar lesion; 2) degenerative cerebellar disease; 3) diagnosis of Joubert syndrome; 4) diagnosis of Dandy-Walker syndrome; 5) diagnosis of Chiari syndrome Type I and II; 6) a clinical history of seizures. The pool of 20 participants then underwent extensive clinical, neuroradiological and neuropsychological investigations as part of a current study aiming at verifying whether a Cognitive Affective Syndrome is also associated to malformative cerebellar lesions apart from acquired cerebellar lesions (see Schmahmann & Sherman, 1998). Three male patients were selected for the present study: Case 1, aged 32.01, right-handed, presents with near total absence of the cerebellum; Case 2, aged 10.03, right-handed, presents with mild vermian hypoplasia and mega cisterna magna; Case 3, aged 21.10, left-handed, shows severe hypoplasia of the right hemisphere. Clinical, radiological and neuropsychological assessments Patients were administered a standard neurological examination based on the "International Cooperative Ataxia Rating Scale" (Trouillas et al, 1996). They also received an EEG and MRI scanning (0.5 or 1.5 Tesla, Tl, T2-weighted spin-echo sequences and protonic density, along axial and coronal sections of 1.3 mm). Images were analyzed according to the Atlas by Schmahmann et al. (1999) by one neuroradiologist blind to the patients' identity and clinical

Language Development and Cerebellar Malformations 131 history. In each case the malformation was classified into one of the following categories according to Altman et al. (1992): Type I: Complete cerebellar agenesis (case 1); Type III: Hypoplasia involving the vermis and both hemispheres (case 2); Type IV: Malformation involving cerebellar hemispheres (one or both) (case 3). Neuropsychological assessment included the following tests: IQ: Wechsler Adult Intelligence Scale (WAIS, Weschler, 1974), Wechsler Adult Intelligence Scale-Revised (WAIS-R) (Weschler, 1997); Wechsler Intelligence Scale for Children-Revised (WISC-R) (Wechler 1986); Wechsler Preschool and Primary Scale of Intelligence (WPPSI) (Weschler, 1973); Griffiths Scale (Griffths, 1986), Stanford-Binet Intelligence Scale, L-M form (Terman & Merrill, 1968). Visuospatial functions:

Test of Visual-Perceptual Skills (non-motor) (Gardner, 1996);

Line Orientation Judgment (Benton & Benton, 1983); Temporal Orientation Test (Spinnler & Tognoni, 1987); Rey Complex Figure "A" (Rey, 1967); Constructive Apraxia Test (Spinnler & Tognoni, 1987); Developmental Test of Visual Motor Integration Test (VMI) (Beery & Buktenica, 2000). Executive functions: (Planning and Control): Wisconsin Card Sorting Test (Heaton et al, 2000); Tower of London Test (Shallice, 1982). Memory: Wide Range Assessment of Memory and Learning (WRAML) (Adams & Sheslow, 1990); Rey Complex Figure "B" (Rey, 1967); Corsi Span (Corsi, 1972); Digit span (Spinnler & Tognoni, 1987); Word span, forward (Spinnler & Tognoni, 1987); Long-term Memory Test (Spinnler & Tognoni, 1987). Language assessment was organized as follows. Case 2 was administered the Esame del Linguaggio dai 4 ai 12 anni, a standardized language battery for children aged 4-12 (Fabbro, 1999), which includes tests of comprehension, repetition, production and articulation. Comprehension: Auditory and Verbal Discrimination tests (Bearzotti, Lilli & Fabbro, in press); British Picture Vocabulary Scale (De Agostini et al., 1998); Token test (short-version, 21 items) (Vender et al, 1981; De Agostini et al, 1998); Test di Comprensione Grammaticale per Bambini (TCGB), a test of grammatical comprehension in children (Chilosi & Cipriani, 1995); Repetition: Word and non-word repetition (De Agostini et al,

1998); Sentence

repetition (Ferrari et al, 1981; Vender et al, 1981); Production: Naming (De Agostini et al, 1998); Semantic Fluency (De Agostini et al, 1998); a picture description task, the Bird Nest Story (Paradis, 1987). Case 1 and 3 were administered the Bilingual Aphasia Test, Part B (Paradis 1987, 1999). The BAT, Part B consists of 32 subtests (427 items) and allows an indepth investigation of linguistic levels and linguistic skills. This test comes with no normative values for the Italian population. We thus compared the performances of Cases 1 and 3 to the values obtained for a control group of 19 participants (12 males, 7 females) with high educational level (equivalent to MSc or A level degree), mean age 35.6 (age range 31-42), described in detail in Fabbro et al. (2004). Reading: Prove di lettura MT (Cornoldi & Colpo 1981), age-appropriate reading tasks standardized for an Italian school-age sample.

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CASE 1, NEAR TOTAL ABSENCE OF THE CEREBELLUM Clinical data Case 1 is a 32 year old right-handed male who, despite near total absence of the cerebellum, presents with mild mental retardation and a harmonious profile as far as cognitive functions are concerned. An MRl at the age of 31 evidenced near total absence of the cerebellum with only a tiny cerebellar remnant and flat ventral pons (cf. Figures 1 and 2).

Figure 1 — MRl: Near total absence of the cerebellum with only a tiny cerebellar remnant positioned superiorly within the posterior fossa. Loss of prominence of the ventral pons is also evident (coronal section, Tl- weighted).

Figure 2 — MRl: Same lesion (sagittal section, Tl- weighted).

Language Development and Cerebellar Malformations 133

Standard neurological examination based on the "International Cooperative Ataxia Rating Scale" (Trouillas et al, 1996) yielded a score of 29/100, evidencing cerebellar ataxia (Postural and gait disturbances = 8/34; Limb ataxia = 16/52; Speech = 3/8; Oculomotor disorders = 2/6). Development Case 1 presents with no familiar history of neurologic or psychiatric diseases. He was born from first-degree cousins, pregnancy and delivery were normal. Weight at birth was 2550gr. The participant's motor and cognitive development soon appeared to be profoundly compromised. However, he presented with slow but steady progress in all functional domains up to almost adequate levels. Motor skills were severely impaired during the first years of life due to a marked hypotony. He did not achieve sitting until after the age of 2; as a child, he dragged himself along and achieved crawling at 5 years of age. He achieved standing and walking if sustained when he was 10. Independent walking was reached at the age of 22. His motor skills developed further and at the time of testing a neurological examination detected only a marked ataxia when walking, a mild dysmetria and intentional tremors (cf. neurological assessment above). He was first seen at our Institute when he was 4.06 years old. At that time he showed an autistic-like behavior, he did not actively search for other people, spending time on his own and being engaged in stereotyped and repetitive activities. If cared for, he did not reject attention. Up to age of 8-10 years his personality was extremely fragile and emotionally passive: socialization was hardly possible. During adolescence his social skills improved and he started actively interacting with parents and other significant adults. At present, affect and behavior are normal, without psychopathological signs. Language development was also markedly impaired. He uttered his first words after age 2 years. Until age 7 years he produced only one-word sentences. He was able to correctly pronounce all single phonemes of the Italian language but articulation of words was still effortful and often incorrect. At age 12 years he was able to produce a simple sentence (Subject - Predicate - Complement), short and contextually linked but sufficient for communication with peers. He had learnt to read and write in capital letters with many spelling errors. Language skills steadily progressed over time up to complete functionality. Regarding quality of life, since he was 5 years of age he has been attending a special school at our Rehabilitation Institute where he lived during the school year. Teachers reported that his performances significantly improved if someone helped him to plan the task and reinforced his attention steadily. He needed constant stimulation as he seemed unable to initiate a requested or desired action on his own. When he was 17 he entered a family residence of our Institute in the framework of a rehabilitation program centered on learning of

134 Neurogenic Language Disorders in Children basic self-sufficiency skills, and he still lives there today. He is completely independent in his personal life, being able to perform a simple work activity (assembling electronic components), knows the value of money and is able to shop. He also has personal interests in music and movies, and keeps himself informed by reading music and film magazines. He is able to use a video recorder and a mobile phone to call and send text messages to his family and friends. He is also able to travel independently by bus from the community where he lives (in a valley in Lombardy, Northern Italy) to a near-by city (Bergamo, Northern Italy), where he stops for lunch and shops for the friends he will be visiting. Neuropsychological assessment at age 32.01 Intelligence Quotient (IQ). Administration of the WAIS (Weschler, 1974) evidenced a mild mental retardation with a harmonious profile: VIQ = 72, PIQ= 67, FIQ= 68. The patient showed more marked impairments on the following subtests: Arithmetics (standardized score= 3), Coding (standardized score = 3), Similarities (standardized score = 4), and Picture Arrangement (standardized score = 4). Visuospatial functions.

On the Rey Complex Figure "A" Test the participant scored

comparably to children with a mental age of 6.06 years (Copy) and 7.06 years (Memory), showing a marked impairment in appreciating the organizing structure of the figure (Schmahmann & Sherman, 1998). Corsi Test yielded a mildly deficient result (<1 SD; raw score= 4; Mean = 5.11 for the 40-49 age group, SD= 1.1). No signs of constructive apraxia were found (raw score = 1 3 ; Mean = 13.2 for the 40-49 age group, SD = 1,48). Executive functions. The Tower of London Test score disclosed a marked impairment in attention (<2 SD; raw score= 8.62; equivalent score = 0 for the age group of 40 years). However, on the Wisconsin Card Sorting Test he did not show any impairment in executive functions (Total errors = 18%, Mean and standard deviation = 24.32 ±15.11; Total categories completed = 6, Mean and standard deviation = 5±1.6). Memory. On the Verbal Span Test the patient scored within normal limits (raw score = 4; Mean = 4.75 for the 40-49 age group, SD = 0.86); however, administration of the Long-term Memory Test (Spinnler & Tognoni, 1987) highlighted a markedly defective performance (<1 SD; raw score= 8.5; Mean = 13.32 for the 40-49 age group, SD= 2.65). Procedural memory as measured on the Star Test was unimpaired. Language. Voice was hypophonic, scanned, nasalized (non-occluding velum). The phonological and phonetic deficits and the irregular patterns of articulatory breakdown suggest a diagnosis of ataxic dysarthria. Spontaneous speech is characterized by phonologic and phonetic problems to a greater extent than descriptive speech (ciamo instead of siamo, "we are"; /zi/ instead of the Italian affermative particle /si/). The patient was administered the Italian adaptation of the Bilingual Aphasia Test, part B (Paradis 1987, 1999). Results show a marked impairment of syntax (72% correct) and semantics (85%), with subtler deficits of lexicon (93%), morphology (95%) and phonology

Language Development and Cerebellar Malformations 135 (96%). With regard to language skills, results show a marked impairment in writing (60% correct), comprehension (78%), sentence construction (86%), reading (89%), with a somewhat milder impairment of lexical access (92%). A closer investigation of his performance on the BAT subtests shows marked deficits in Mental Arithmetic (13% correct), Sentence dictation (20%), Auditory comprehension of a short story (40%), Reading Comprehension of sentences (50%), Syntactic comprehension (70%), Antonyms (80%). Reading. Administration of the MT reading tests evidenced a score average for a 5lh grade as far as correctness, rapidity and comprehension are concerned. The analysis of a sample of descriptive speech (The Bird Nest Story; Paradis, 1987) showed numerous morphosyntactic errors (omissions of function words, substitution of bound grammatical morphemes) and semantic paraphasias. In addition, the patient was not able to appreciate the "gist" of the story. In conclusion, the patient seems to have acquired language to a considerable extent and is able to use it for everyday activities. However, he presents with marked permanent impairments of receptive and expressive language and of speech, with more accentuated comprehension difficulties, probably due to syntactic processing deficits. CASE 2, DIFFUSE VERMIAN HYPOPLASIA Clinical data Case 2 is a 10 year old right-handed boy. He presents with moderate mental retardation, with a harmonious profile. An MRJ revealed Mega Cisterna Magna with diffuse vermian hypoplasia. Cerebellar hemispheres are near to normal (cf. Figure 3). The patient was diagnosed as having a Type III malformation, according to Altman et al. (1992).

Figure 3 — MRI: Mega Cisterna Magna with diffuse vermian hypoplasia. Cerebellar hemispheres are nearly normal (coronal section, Tl- weighted).

136 Neurogenic Language Disorders in Children

Development The patient was referred to our Institute when he was 9.01 for severe language delay and reduced social and affective skills. Neuromotor development was slightly retarded. He reached independent walking when he was 16 months of age. Development of affective, cognitive and linguistic skills was markedly impaired. He had been living in an Englishspeaking country until he was 4 years old and was thus exposed to both English and Italian (parent's language) input. A marked communicative and linguistic delay was reported by operators at the English-speaking kindergarten. He uttered his first words in Italian when he was 5 years of age. Language production improved over time, but the patient soon showed autistic-like behaviors. Clinical and neuropsychological assessment at age 9 Clinical assessment. A neurological examination evidenced mild hypotonia, hypodiadococinesis, and mildly deficient fine and gross motor skills. Karyotype was normal and a diagnosis of Fragile X syndrome was excluded. The EEG showed epileptiform abnormalities (SW) over the central-posterior regions, bilaterally, mainly on the right side, and over the anterior regions in NREM sleep (cf. Figure 4). On the psychomotor evaluation he showed a severe delay as he could not complete the proposed tasks.

Figure 4 — Epileptiform abnormalities (SW) over the central-posterior regions, bilaterally, mainly on the right side, and over the anterior regions during NREM sleep.

Language Development and Cerebellar Malformations 137

IQ. On the Stanford-Bmet Scale the patients obtained a full-scale IQ score of 50, comparable to a mental age of 4.06. Language. Articulation showed some phonological problems (phonemic simplifications). His descriptive speech (Birds' Nest Story; Paradis, 1987) was characterized by numerous morphosyntactic errors (omissions of free grammatical morphemes), anomic errors, phonemic paraphasias. Fluency (words per minute) was markedly reduced (= 21.3, < 2 SD) as was MLU = 3 (<2SD). The patient substituted the description of one story character for another, demonstrating an impaired ability at understanding the story structure. Spontaneous speech revealed inappropriate language switching episodes (from Italian to English in interaction with a non English-speaking Italian operator), tangential answers and perseverations (Fabbro et al., 2000b). Grammatical structure was more preserved, with few omissions of free grammatical morphemes. However, answers were often in the form of a list, thereby limiting the extent of possible morphosyntatic errors. Clinical and neuropsychological assessment at age 10 At the age of 10 Case 2 received a complete clinical reassessment. The neurological examination confirmed mild hypotonia, adiadococinesis, and mildly deficient fine and gross motor skills. The psychomotor evaluation confirmed a severe delay as the child could not complete the proposed, age-appropriate, tasks. IQ. On the WISC-R (Weschler, 1986) he obtained the following scores: VIQ = 51; PIQ = 49; FIQ = 49, which confirm the moderate retardation evidenced on the first evaluation. Language. Language scores on formal tests showed a change in profile, with word and non-word repetition within normal limits and a decrease in semantic comprehension and action naming. Scores were <2 SD on the following tests: syntactic comprehension (Token Test), grammatical comprehension (TCGB), sentence repetition, object naming, action naming, semantic fluency. Semantic comprehension was <1 SD. Language articulation showed only mild inaccuracies. His descriptive speech (Birds' Nest Story) was characterized by poor narrative skills and omission of bound grammatical morphemes. The patient delivered an empty story, perseverating on just one aspect (whether one character falls or not) and applying it to all figures inappropriately. Neologisms and inappropriate list-like object descriptions (IT: "Un'auto ha tre targhe", ENG: "A car has three number plates") were present in his spontaneous speech. In conclusion, Case 2 presents with a moderate retardation, with language and affect/relational skills being the most severely impaired functional areas. Remarkably, on continuous and regular language therapy, the patient showed a regression in language competence, while peripheral linguistic components such as articulation improved (as evidenced by testing word and nonword repetition in the second assessment).

13 8 Neurogenic Language Disorders in Children CASE 3, SEVERE HYPOPLASIA OF THE RIGHT CEREBELLAR HEMISPHERE Clinical data Case 3 is a highly educated 21 year-old left-handed male who, despite severe hypoplasia of the right cerebellar hemisphere, presents with normal cognitive development. He was referred to our Institute following a sudden onset of two hyperventilation crises associated with postural tremors to the right forearm and diurnal drowsiness (onset of postural tremor to the right forearm at 15 years of age). An MRi (Spin Echo) evidenced a severe hypoplasia of the right cerebellar hemisphere (which is practically absent) (cf. Figure 5). Case 3 has been classified as showing a Type IV category malformation, which includes all types of malformations limited to one or both cerebellar hemispheres.

Figure 5 — Severe hypoplasia of the right cerebellar hemisphere. Axial MRI shows near total absence of the right cerebellar hemisphere with an asymmetric IV ventricle which is more enlarged to the right side (coronal section, T2- weighted). Development His parents reported some difficulties in acquiring reading and writing skills. One episode of sudden and transient partial loss of consciousness at the age of 14 years was reported, followed by headache. Language development was reported to be normal, with some initial difficulties in acquisition of reading and writing skills. The patient is left-handed and tends not to actively use the right hand also in tasks requiring bi-manual coordination. The neurological examination revealed the following cerebellar signs: appearance of distal kinetic tremor in the right upper limb under emotional stress conditions, tendency to move left when walking

with

eyes

closed,

tremor

and

right

dysmetria

in

finger

to

nose

test,

Language Development and Cerebellar Malformations 139

hypodiadococinesis. At present Case 3 attends University classes with good results. He also practices various types of sports. Neuropsychological assessment IQ. On the WAIS-R, the patient shows a harmonious profile (VIQ=107, PIQ=100, FIQ=105), with a marked difficulty in performing the figure reconstruction task. Visuospatial functions. On the Rey Complex Figure "A" Test the participant scored comparably to a mental age of 6.00 years (Copy), 5.00 years (Memory immediate), 4.06 years (Memory delayed), showing a marked impairment in appreciating the organizing structure of the figure. On the Corsi Test he performed within the norm (Span = 6). No signs of constructive apraxia were noted (raw score = 14; Mean = 13.2 for the 40-49 age group, SD = 1.48). Executive functions. The Wisconsin Card Sorting Test did not evidence any impairment in executive functions (Total errors = 19%, Mean and standard deviation = 24.32±15.11; Total categories completed = 6, Mean and standard deviation = 5±1.6). Memory. Mnestic functions were not impaired as assessed by the Verbal Span Test (raw score = 5; Mean = 4.75 for the 40-49 age group, SD = 0.86); he performed in the normal range on the Long-term memory test (raw score = 12.7; Mean = 13.32 for the 40-49 age group, SD = 2.65). Language. The patient was administered the Italian adaptation of the Bilingual Aphasia Test (Paradis 1987, 1999). He showed a moderate impairment in semantics (83% correct), mainly pertaining to lexical knowledge (antonyms, synonyms). With regard to language skills, he had subtle deficits in reading (95% correct) and comprehension (97% correct). A closer look at his performance on the BAT shows that the patient had difficulties with reading comprehension of a short story (50% correct), listening comprehension of a short story (80%), synonyms (80%) and repetition of sentences (86%). The analysis of a sample of descriptive speech (Bird Nest Story; Paradis, 1987) reveals fluent speech and grammatically well articulated discourse (MLU = 14.2; subordinate clauses = 6), a higher than normal type/token ratio (0.69), some morphosyntactic errors (2 omissions of function words) and 2 instances of word-finding difficulty. In addition, the patient was not able to appreciate the "gist" of the story. Voice was normal. Spontaneous speech manifested extremely rare morphosyntactic difficulties (in a sample of 100 utterances, 2 substitutions of bound grammatical morphemes: IT "Sono tornata (FEM) a Milano", ENG "I went back to Milan", instead of IT "Sono tomato (MASC) a Milano". In conclusion, the patient seems to have very subtle language difficulties, which become more manifest in tasks tapping descriptive and spontaneous speech or lexical search and decision (such as choice of a synonym). The higher than normal type/token ratio is indicative of a conscious control over speech production.

140 Neurogenic Language Disorders in Children

DISCUSSION In this study we set out to study language development in three subjects with different types (localization and extent) of congenital cerebeliar malformations. We also presented preliminary data on the characteristics of language disorders (e.g., receptive vs. expressive) in congenital cerebeliar malformations as distinct from acquired cerebeliar lesions. Our findings show that two out of three cases (Cases 1 and 2) have a marked language delay. Case 1 presented with a continuous although remarkably unusual language development, with language acquisition phenomena occurring also at an adult age. In addition, Case 2 presented with an episode of language regression in the presence of EEG epileptiform discharge. Case 3 presented with no language delay, although at present very subtle language deficits may be detected. The different outcome between Cases 1 and 2 and Case 3 may be correlated to lesion localization and extent. In Case 1 permanent deficits, more marked on the receptive side (syntactic comprehension), are evident. The patient also presents with ataxic dysarthria, phonological and phonetic deficits, and a scanned voice. Case 2 shows a marked language delay, especially evident on syntactic and grammatical comprehension tasks. He presents with language regression and EEG paroxysmal abnormalities during NREM sleep, in the presence of a documented neurological lesion and thus shows remarkable similarities with the cases described by Fabbro et al. (cf. this volume). In Case 3 only very subtle language deficits could be detected, mainly on semantic comprehension tasks (e.g., synonym comprehension; cf. Fabbro et al, 2004). Therefore, the study of language development in the three cases of cerebellar malformations that we have presented suggests that the cerebellum is involved in language acquisition. However, the effect of malformative lesions on language acquisition and language development in adult age seems to vary according to lesion extent and localization. Near total absence of the cerebellum does not seem to prevent a considerable degree of language development, up to full communicative functionality, although the acquisition of morphosyntax remains incomplete. The event of near total absence of the cerebellum is very rare. Recently, Gardner et al. (2001) described three new cases and reviewed the relevant literature which included only five other cases (Sener & Jinkins, 1993; Sener et al, 1995; Van Hoof & Wilmink, 1996; Velioglu et al, 1998). The authors identified a syndrome termed "Near-total absence of cerebellum with flat ventral pons and relatively mild clinical affection". The same diagnosis has been made for our Case 1. However, Case 1 is remarkable in that the MRI shows a very limited cerebeliar residue (possibly of the vermis) compared to the cases described by Gardner et al. (2001). Nonetheless, like in Gardner's cases, cognition and behavior are rather mildly affected in contrast with the extent of the anatomical defect. A general feature of the "Near-total absence of cerebellum" syndrome seems to be that initially patients show a very marked delay in development but slowly and steadily recover motor, affective and cognitive functions. Recovery may occur very late in life, compared to normal developmental milestones. In Case 1, plasticity factors may act on the remaining normal

Language Development and Cerebellar Malformations 141

cerebellar tissue and on a process of "cerebellization" of supratentorial regions (Macchi & Bentivoglio, 1987). Malformations involving the vermis do not seem to prevent language acquisition but profoundly disrupt communication (up to autistic-like behavior) and therefore markedly delay language acquisition. Malformations limited to the right cerebellar hemisphere may not impair language acquisition. This may be due to two main reasons: 1) language may not be lateralized in the cerebellum, and thus it can be sustained by either remaining cerebellar hemisphere, 2) language may be lateralized to the right cerebellar hemisphere, as proposed by Marien et al. (1996), but plasticity factors may induce transfer of language functions to the contralateral cerebellar hemisphere. Language deficits associated to cerebellar malformations show important similarities and differences with language deficits associated to cerebellar lesions. Both congenital and acquired cerebellar lesions can show a great improvement of language impairment over time, although cerebellar malformations involving the vermis show a specific language acquisition delay and require constant speech therapy, while linguistic symptoms following acquired cerebellar lesions usually regress spontaneously and rapidly to a considerable extent (but see Fabbro et al., 2004; for a discussion on the persistency of residual deficits). Both congenital and acquired cerebellar lesions may induce deficits in language comprehension and expression. However, congenital cerebellar malformations involving the vermis seem to induce more marked and permanent language disorders, especially in language comprehension. This can be explained if one considers that the cerebellum seems to be involved in procedural language acquisition, in particular in the acquisition of phonology and syntax (see Ullman, 2001). A malformative lesion may impair procedural learning of language and require long-term, effortful explicit training for language to be acquired, as in Case 1. On the contrary, acquired cerebellar lesions seem to induce mild language expression deficits. In conclusion, though our data do not allow us to take a definite stance on the type (neuromodulation vs. processing) of cerebellar contribution to language, it seems likely that normal language acquisition is crucially supported by full functionality of the cerebellum.

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Schmahmann J. D. & J. C. Sherman (1998). The cerebellar cognitive affective syndrome. Brain, 121, 561-579. Sener, R. N. and J. R. Jinkins (1993). Subtotal agenesis of the cerebellum in an adult. MRI demonstration. Neuroradiology, 35, 286-287. Sener, R. N. (1995). Cerebellar agenesis versus vanishing cerebellum in Chiari II malformation. Comput Med Imaging Graph 19, 491-494. Shallice, T. (1982). Specific impairments of planning. Philosophical Transactions of the Royal Society of London, 298, 199-209. Silveri, M. C, A. M. Di Betta, V. filippini, M. G. Leggio and M. Molinari (1998). Verbal short-term store-reharsal system and the cerebellum. Evidence from a patients with a right cerebellar lesion. Brain, 121, 2175-2187. Silveri, M. C, M. G. Leggio and M. Molinari (1994). The cerebellum contributes to linguistics production: a case of agrammatic speech following a right cerebellar lesion. Neurology, 44, 2047-2050. Spinnler, H. and G. Tognoni (1987). Standardizzazione e Taratura Italiana di test Neuropsicologici. The Italian Journal of Neurological Sciences, 6, supplement 8. Stewart, R.M. (1956). Cerebellar agenesis. J. Men Sci, 102, 67-77. Terman, L. M. and M. A. Merrill (1968). Scala di Intelligenza Stanford - Binet, forma L-M. Organizzazioni Speciali, Firenze. Trouillas P., T. Takayanagi, M. Hallett, R. D. Currier, S. H. Subramony, K. Wessel, et al. (1997) International Cooperative Ataxia Rating Scale for pharmacological assessment of the cerebellar syndrome. The Ataxia Neuropharmacology Committee of the World Federation of Neurology. JNeurol Sci, 145(2), 205-11. Ullman, M. T. (2001). The neural basis of lexicon and grammar in first and second language: the declarative/procedural model. Bilingualism: Language and Cognition, 4, 105-122. Van Hoof, S. C. and J. T. Wilmink (1996). Cerebellar agenesis. J. Beige Radiol, 79, 282. Velioglu, S. K., K. Kuzelyli and M Zzmenoglu (1998). Cerebellar agenesis: a case report with clinical MR imaging finding and a review of the literature. Eur. J. Neurol, 5, 503-506. Vender, C, D. A. Anghini, S. Cumer Bruno, R. Borgia and G. Zardini (1979). Contributo allo studio del Token Test in eta evolutiva. Neuropsichiatria Infantile, 215, 436-439. Vender, C, R. Borgia, S. Cumer Bruno, P. Freo and G. Zardini (1981). Un test di ripetizione di frasi. Analisi delle perfomances di bambini normali. Neuropsichiatria infantile, 243, 819-831. Zettin, M., S. F. Cappa, A. D'Amico, R. Rago, C. Perino, D. Perani and F. Fazio (1997). Agrammatic speech production after a right cerebellar haemorrage. Neurocase, 3, 375380. Weschler, D. (1974). WAIS. Scala di Intelligenza Weschler per Adulti. Organizzazioni Speciali, Firenze Weschler, D. (1973). WPPSI. Scala Weschler a livello prescolare e di scuola elementare. Organizzazioni Speciali, Firenze.

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9

CROSSED APHASIA IN CHILDREN Peter Marien General Hospital Middelheim, Belgium

University of Antwerp and Free University of Brussels,

Philippe Paquier University Hospital Erasme, University of Antwerp and Free University of Brussels, Belgium Sebastiaan Engelborghs and Peter P. De Deyn General Hospital Middelheim, University of Antwerp, Belgium

Abstract - In 1899, Byrom Bramwell (1899) introduced the concept of crossed aphasia (CA) as an exception to the prevailing insight of an inherent association between cerebral dominance for language and hand preference (so-called Broca's dogma). He defined as such the phenomenon of aphasia caused by brain damage ipsilateral to the dominant hand (i.e. aphasia resulting from a lesion to the left hemisphere in sinistrals and aphasia following a lesion to the right hemisphere in dextrals). Rather striking in the development of this concept is the absence of any reference to the understanding of acquired childhood aphasia (ACA) in which aphasia after a right hemisphere lesion was considered a frequent phenomenon. However, following erosion of Bramwell's positions and a decay of the feasibility of so-called Broca's dogma, a confluence of concepts was established between CA, aphasia in sinistrals and ACA seven decades later. The first part of this chapter reviews the history of the genesis, development and collusion of concepts in these atypical populations. The second part addresses CA in children in more detail. In contrast to the estimated low incidence in dextral adults (among 1%), CA in children is generally considered a common finding. Reviewing the literature from 1975 onwards, we only found five children (2.7%) in a corpus of 180 dextrals with aphasia following a right hemisphere lesion (Marien et al, 2001c). A critical analysis rendered three of the reported cases ambiguous for a CAD diagnosis and hence not suitable to draw conclusions. The neurobehavioural characteristics of the two representative childhood CAD cases are discussed and compared with adult CAD and ACA. Keywords: Crossed aphasia, acquired childhood aphasia, language dominance

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PART I: DEVELOPMENT AND CONFLUENCE OF CONCEPTS - FORMATION OF CONCEPTS The standard view on acquired childhood aphasia (ACA) In 1868, Cotard for the first time systematically studied the phenomenon of ACA. In his elaborated monograph entitled 'Etude sur l'atrophie cerebrale' he reported the post-mortem findings of seven left hemisphere lesioned adults with right hemiplegia and normal neurocognitive development since early childhood. Cotard (1868) stated that language in these patients had developed in the right hemisphere, and that, in general, functions of the lesioned hemisphere are taken over by the intact one, if damage is sustained at a young age. As a consequence, he postulated that aphasic disorders do not occur in children. Clarus (1874), however, disputed this position and concluded from an analysis of 50 published cases that: 1) aphasia in children is not rare, 2) prognosis is not invariably benign but depends in part on both etiology and extent of the lesion, and 3) the right hemisphere can take over language functions when the left hemisphere is damaged. Given the relatively large proportion of left hemiplegic aphasic children Sach and Peterson (1890) advanced the view that during the first years of life both hemispheres are equally equipped for the development of language and that during the expansion of language functions, the role of the right hemisphere progressively decreases in favour of the left one. This view was later to be designated by Basser (1962) and Lenneberg (1967) as the hypothesis of 'hemispheric equipotentiality and progressive lateralization of language development'. Freud (1897) seconded this position with the observation that aphasia in children, entirely unlike aphasia in adults, occurs relatively frequently after right hemisphere lesions. In spite of an ongoing controversy surrounding the theme, Bernhardt (1885) defined acquired childhood aphasia (ACA) on five characteristics: 1) ACA is not rare, 2) ACA is predominantly of the nonfluent (expressive, motor) type, 3) ACA entails a benign prognosis, 4) ACA lasts only a short time, and 5) ACA is entirely compensated for by the expansion of language functions in the right hemisphere. Towards the end of the 19th century, this definition became generally accepted, giving rise to a 'standard doctrine' which would last more than 70 years. Crossed aphasia: a new concept in adult aphasia During the last decades of the 19th century, so-called Broca's doctrine assigned left hemisphere dominance for language to dextrals and right hemisphere dominance for language to sinistrals. This 'dogma' established a strict anatomo-functional connection -much stricter indeed than Broca himself had implied in his seminal 1865 paper- between motor control of the dominant hand and control over language functions. However, in the same period, a number of observations casted doubt on such a clear-cut view. The counter-evidence brought

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forth by the early, often anecdotical case-reports was not very strong. Hughlings Jackson (1880), for instance, described aphasia with left hemiplegia in a sailor who, though lefthanded, was obliged to consistently use the right hand for mending the sails (a large share of his work), and hence was, at least in part, a dextral. A few years later, Oppenheim (1889) observed aphasia associated with anatomopathologically verified right hemisphere lesions (a solitary tuberculoma and a subcortical sarcoma) in two right-handed patients, one of whom, however, had become left-handed following injury to the right hand at the age of 17 years. Before the turn of the century, more convincing evidence against the model of cerebral dominance for language and handedness was provided by Bramwell (1899). He described a 36-year-old left-handed man who developed persistent nonfluent aphasia and a right sensorimotor deficit following a left hemisphere stroke. Bramwell introduced the term crossed aphasia (CA) to denote, in a broad sense, any aphasic syndrome resulting from a cerebral lesion 'ipsilateral' to the dominant hand. He particularly emphasized the exceptional character of this observation because of the persistent aphasia and noted that in most CA cases, the language symptoms are temporary. In agreement with his predecessors, Broca and Hughlings Jackson, Bramwell attributed what he considered the inherently transient character of CA to the compensatory role of the non-dominant hemisphere. In contrast to temporary manifestations of CA, which he assumed to occur in both left- and right-handers, Bramwell postulated that CA characterized by persistent language disturbances is extremely rare and limited to the sinistral population. Although several reports of dextral aphasics with anatomopathologically verified lesions of the right hemisphere had already been described (e.g. Farge, 1877; Oppenheim, 1890; Preobrashenski, 1893; Moltschanow, 1897), Bramwell stated explicitly that he knew of no pure cases of CA in dextrals (CAD). Indeed, Bramwell believed that crossed aphasia was always a transient condition in dextrals who: (1) had not suffered brain damage during early development, (2) were born to dextral parents and (3) had learned to write with the right hand. To explain the exceptional observations of 'pure' right-handers in whom acute damage to the anatomical language region of the left hemisphere induced no aphasia (negative cases), he proposed that language dominance of the lesioned left hemisphere was immediately taken over by the language centres of the right hemisphere. Notably absent in the formation of the concept of CA is any reference to the understanding of ACA, which, at the turn of the 19th century, had arrived at a consensus within a standard doctrine. This is striking given the fact that ACA was also considered: 1) to result frequently from cerebral lesions ipsilateral to the dominant hand, and 2) to occur frequently as a transient phenomenon due to the compensatory role of the non-lesioned hemisphere. The fact that, within ACA, the right hemisphere was deemed central for both the genesis of language as well as the recovery from aphasia makes its absence from the development of the CA concept all the more conspicuous.

150

Neurogenic Language Disorders in Children

EVOLUTION OF CONCEPTS IN THE 2OTH CENTURY Acquired Childhood Aphasia (ACA)1: 1900-1978 Neglected early evidence against semiological uniformity. During the first decades of the 20th century, a few reports (e.g. Potzl, 1926; Wagner & Mayer, 1933; Brunner & Stengel, 1932; De Girardier & Jeannin, 1939) documented a range of fluent (sensory) language deficits in children, questioning the classical views on the predominantly motor character of ACA (Bernhardt, 1885). Although these few scattered counter-examples constituted a striking deviation from the homogeneous semiological picture portrayed by the standard doctrine, they did not succeed in modifying the standard doctrine. The aphasiogenic and compensatory role of the right hemisphere. Several authors, including Taylor (1905) and Sachs & Hausmann (1926) subscribed to the notion that ACA frequently occurs in association with lesions of the right hemisphere. By contrast, Smithies' review (1907) of the literature did not confirm the purported role of the right hemisphere in ACA but he unfortunately did not pursue this finding. Marie (1922) again emphasized the absence of aphasia in children with right hemiplegia at a young age and, in accord with the findings of Cotard (1868) and Jendrassik & Marie (1885), focused attention on the transient character of ACA. Convinced that the anatomical centres are bilaterally and symmetrically represented at birth, Marie (1922) posited that the language centres are not innate, but that they develop self-sufficiently in each individual. Much like Broca (1865) before him, Marie (1922) attributed left hemisphere superiority in this process to the anatomical fact that the left hemisphere maturates faster than the right one. In a similar sense, Mingazzini (1925) supported the views of Sachs & Peterson (1890) claiming that, during development the role of the right hemisphere in language progressively decreases. Recovery reconsidered. The prevalent optimism regarding favourable recovery from ACA was not shared by Potzl (1926), Ford & Schaffer (1927), Minkowski (1930), and Brunner & Stengel (1932), among others. They stated that prognosis for recovery is markedly worse for sensory than for motor aphasia. Minkowski (1930), moreover, pointed out that residual language symptoms undermine neurocognitive and social development. Guttmann (1942) for the first time highlighted ACA as a multifaceted disorder. He analyzed research data of 30 patients between two and 14 years of age with primarily unilateral brain damage caused by different etiologies (traumas, tumors, abscesses, and thromboses). Sixteen of the patients exhibited aphasia. With respect to incidence, Guttmann (1942) found that aphasia following left hemisphere lesions is not at all infrequent in children

Crossed Aphasia in Children 151 (14/16 cases); in fact, prevalence was comparable to that of acquired aphasia in adults. Regarding semiology, he noted that irrespectively of the localization of the lesion, all children under 10 years of age exhibited reduced spontaneous speech, ranging from mutism to dysarthria and telegraphic style during recovery. In addition to expressive (nonfluent) language symptoms, children with posterior lesions also presented sensory (fluent) deficits, which, as in adults, could take the form of logorrhea. Although the data did not permit rigorous deductions due to the variability of etiology and follow-up, Guttmann (1942) concluded

that:

1)

a

combination

of

expressive

(nonfluent/motor)

and

receptive

(fluent/sensory) aphasia entails a less favourable prognosis than purely expressive aphasia, 2) recovery from expressive aphasia occurs notably faster and 3) prognosis for recovery is reserved if the aphasic symptoms are still present after four weeks. Following Guttmann (1942), the view of AC A as a transient infliction slowly changed. The exclusively motor character and the unequivocally successful recovery, however, remained indubitable even during the 1950s (Branco-Lefevre, 1950; Critchley, 1950; De Ajuriaguerra, 1958; Subirana, 1960) and the influence of these notions was felt well into the 1980s (Denckla, 1979). hi a study of 102 cases with acquired infantile hemiplegia, Basser (1962) discerned 30 patients whose cerebral lesion (15 in the left and 15 in the right hemisphere) occurred during language development. A lesion in the left hemisphere gave rise to aphasia in 13 of the children, while in seven of the children aphasia was due to a lesion in the right hemisphere. According to Basser (1962), duration of aphasia did not depend on the severity of the hemiplegia, but rather on the age of onset. A better outcome was attributed when the lesion was sustained before the age of two years. In 1965, Alajouanine & Lhermitte studied 32 children between 6 and 15 years of age with an aphasiogenic lesion of traumatic, vascular or tumoral origin in the left hemisphere. They found semiological differences between the children under and over 10 years of age. In the group of children younger than 10 years the aphasia was predominantly characterized by: 1) severely reduced verbal expression, 2) distorted articulation and phonetic disintegration, 3) impaired auditory-verbal comprehension, 4) severe spelling impairments and 5) lack of paraphasias. Aphasia in children older than 10 years consisted mostly of: 1) a markedly lower frequency of articulation distortions, 2) an increased incidence of paraphasias, which even took the form of jargon speech in some children, 3) impaired reading comprehension and 4) disturbed spelling. With respect to recovery, Alajouanine & Lhermitte (1965) observed complete recovery of language functions in 75% of the population sampled, although none of the children made normal academic progress consequent to learning difficulties. Lenneberg (1967), in turn, reformulated classical insights into AC A and posited that, when the lesion is limited to one hemisphere and sustained before the age of 9 years, complete remission of aphasia will ensue. One year later, Collignon et al. (1968) confirmed a negative 1 The Landau-Kieffher syndrome (Landau and Kleffner, 1957) is not reviewed here because of its special position within acquired childhood aphasia. For critical reviews, we refer to the contributions by Gordon (1990), Deonna (1991), Paquier, Van Dongen & Loonen (1992) and Marien et al. (1993).

152

Neurogenic Language Disorders in Children

prognosis for recovery after bilateral lesions, hi agreement with the findings of Alajouanine & Lhermitte (1965) and Collignon et al. (1968), the contributions by Riese & Collison (1964) as well as Aicardi et al. (1969) further weakened the case for widespread complete recovery from ACA. In contrast to Lenneberg's conclusions (1967), which indicated that ACA after the age of 10 years leaves undisputable traces, Hecaen (1976) found excellent recovery in three patients who had acquired aphasia at the age of 14 years. In accord with Collignon et al. (1968), Hecaen (1976) indicated that extent and bilateral cerebral damage are the most important variables in the recovery process. Van Dongen & Loonen (1977) investigated recovery of ACA with a follow-up of three years in a group of 15 right-handed children between 4 and 14 years of age. Eight children, seven of which with a traumatic etiology, recovered while the four children with vascular aphasia barely recovered at all. In addition to the impact of etiology, the authors also found a correlation between recovery and type of aphasia, and identified severity of impaired comprehension as a crucial factor. Brown & Hecaen (1976) summarized the predominant insights into ACA in the mid1970s as follows: 1) the initial phase of ACA is characterized by mutism or agrammatism and is followed by anomia and nonfluent phonemic paraphasias, 2) a distorted articulation appears in a context of a nonfluent or borderline fluent output, 3) fluent phonemic paraphasias (conduction aphasia) are uncommon, 4) logorrhea and semantic or neologistic jargon do not arise, 5) impaired comprehension is found in one-third of patients, 6) recovery is manifestly superior compared to acquired aphasia in adults, and 7) at a young age, there is an approximately equal chance to develop aphasia following damage to either hemisphere. Crossed aphasia in sinistrals and dextrals: 1900-1970 In the course of seven decades, Bramwell's positions (1899) on CA were shown to be untenable and the initial concept of CA completely eroded. Firstly, it became clear that permanent aphasia following a hemispheric lesion ipsilateral to the dominant hand is not limited to sinistrals, but is also occasionally observed in dextrals. In further contrast with Bramwell's views (1899), consensus arose regarding the fact that CA in sinistrals is not the exception, but the rule. The conceptual turning point in classical thinking about CA was due to the insights derived from systematic investigation of sinistral aphasics during the 1950s and 1960s rather than to the increasing number of observations of crossed aphasia in dextrals (CAD), which were often reduced to artifacts and impelled to accommodate the prevalent view of an intrinsic connection between cerebral dominance for language and hand preference (so-called Broca's doctrine). Explanations such as hidden sinistrality (e.g. Joffroy, 1903), absence of a decussation of the pyramidal tract (e.g. Souques, 1910), familial left-handedness inducing a genetic predisposition for right hemisphere dominance for language (e.g. Kennedy, 1916), bilateral language representation linked to gradations in manual preference (e.g. Rothschild,

Crossed Aphasia in Children 153

1931) or consequent to developmental complications (e.g. Stone, 1934), undetected damage of the left hemisphere (e.g. Scollo, 1926) and the presumed linguistic role of phylogenetically older subcortical structures in which language functions were assumed not to be lateralized (e.g. Ardin-Delteil et al, 1923) did not put so-called Broca's doctrine fundamentally into question. The relation between hand preference and hemispheric dominance for language was investigated by Conrad (1949) in a study of sinistral war victims inflicted with traumatic brain injury. He concluded that: 1) aphasia occurs more frequently in sinistrals than in dextrals, 2) the chance of recovery is greater in sinistrals than in dextrals, and 3) in contrast to the accepted view, aphasia in the majority of cases is not caused by lesions of the right hemisphere, but by lesions of the left hemisphere. Despite considerable differences in the proportion and incidence of cases, these findings were corroborated by numerous studies (Goodglas & Quadfasel, 1954; Bingley, 1958; Penfield & Roberts, 1959; Hecaen & De Ajuriaguerra, 1963, Hecaen & Sauguet, 1971; Newcombe & Ratcliff, 1971; Satz, 1980; Annett, 1985). Although only a very limited number of these studies systematically paid attention to the semiological characteristics, they also gave rise to the long-standing view that, irrespective of the lateralization of the lesion, aphasia in sinistrals significantly differs from uncrossed aphasia in dextrals. In comparison to uncrossed aphasia in dextrals a more uniform semiological syndrome was advanced for aphasia in sinistrals, typically characterized by: 1) markedly less severe language disturbances, 2) a significantly lower incidence of comprehension deficits, 3) a higher incidence of expressive language disturbances and 4) a much better, often complete recovery (Luria, 1947; Goodglass & Quadfasel, 1954; Subirana, 1958, 1969; Hecaen & De Ajuriaguerra, 1963). The implication that CA in sinistrals is the rule rather than the exception led to the disuse of the term in the sinistral population and became synonym of crossed aphasia in dextrals (CAD). In addition, the change of insights in the anatomoclinical configurations of aphasia in sinistrals and the decay of the feasibility of the doctrine established the basis for the development of other types of explanations for CAD in the 1970s. In accord with the view that left hemisphere language dominance reflects the end-point of a successful maturation process which ensues progressively from an initially bilateral representation of language functions, the hypothesis was made that bilateral language representations in CAD reflect a disrupted maturation. This view resulted from a confluence of concepts stemming from acquired aphasia in three atypical populations: children, sinistrals and anomalous dextrals.

A CONFLUENCE OF CONCEPTS In their contribution on the relation between cerebral dominance for language and hand preference, Anastasopoulos & Kokkoni (1962) incorporated the ideas from AC A and made them central to their discourse regarding the gradual differences of cerebral lateralization of

154 Neurogenic Language Disorders in Children

language and hand preference. In agreement with the hypotheses of hemispheric equipotentiality and progressive maturation of language dominance, they posited that complete unilateral representation of language and hand preference are the end product of optimal development, which ensues progressively from an initially bilateral cerebral potential for giving rise to manifold brain functions. At the basis of the lateralization process they posited a dynamic mechanism of inhibiting influences exerted on the contralateral homologous brain area by the hemisphere that is becoming dominant. Based on this assumption, they subsequently claimed that language capacity and hand preference will be represented within one and the same hemisphere only if the process of cerebral lateralization develops fully into unilaterality. According to the authors, variants of a separate development of both functions would arise as soon as complete unilateral cerebral dominance becomes unattainable. Anastasopoulos & Kokkoni (1962) explicitly related the conclusions from comparative studies of left- and right-handed aphasics carried out in the 1950s to language representation in children: 'Various authors (...) who studied aphasia in left-handers state that these individuals, in contrast to right-handers, are more frequently made aphasic irrespective of the side of the lesion, and that the occurring aphasia is on the whole less severe and less persistent. These characteristics are attributed to a significant participation of both hemispheres in language in left-handers, the same as in children ' (p. 14) They also attributed the parallels between the pattern of recovery from ACA and aphasia in sinistrals to the adoption of the language functions by the non-lesioned, active language centres of the contralateral hemisphere. Despite gradual differences in the extent of cerebral dominance, Anastasopoulos & Kokkoni (1962) deemed unlikely the possibility of a complete separation in the representation of language and hand preference. Influenced by this view that variants of a dissociated lateralization of hand preference and language reflect developmental irregularities, Brown & Hecaen (1976) and Brown & Wilson (1973) achieved a quasi complete symbiosis between ACA, aphasia in sinistrals, and CAD. They acknowledged two phases within ACA, namely 1) mutism, or agrammatism at an early infantile age and 2) anomia with nonfluent phonemic paraphasias at a later infantile age, and found these phases prominently represented as distinct phenomena in CAD and aphasia in sinistrals, respectively. The temporal substrate of these mutual commonalities led them to conclude that these three special forms of aphasia are situated in a continuum of gradual development from bilateral to unilateral left hemisphere dominance for language. As such, they proclaimed ACA, aphasia in left-handers, and CAD to be representative of an immature lateralization process.

Crossed Aphasia in Children 155 Concurring with the model of a disrupted maturation process from initial bilateral to unilateral left hemisphere language dominance, they posited that CAD reflects various forms of bilateral language representation. Following these contributions, the semiological uniform type of CAD was systematically reproduced in many additional observations. In the 1970s, the uniform pattern of these observations rapidly led to a so-called standard doctrine for CAD. In accord with the classical conception of ACA, nonfluent characteristics were ascribed to prototypical CAD irrespective of the location of the lesion. Agrammatism, mutism at onset, relatively preserved word retrieval, and variability in repetition and comprehension were propagated in numerous publications, while the possibility of jargon was formally excluded. The swiftness and extent of recovery were found to be superior compared to the classical types of uncrossed aphasia. As in ACA, a comparable dissociation in CAD was frequently observed between superior oral and inferior written language (Table 1).

Table 1 — Overview of characteristics of acquired aphasia in children, aphasia in smistrals and CAD during the seventies

Nonfluent symptoms Mutism Agrammatism Distorted articulation Phonemic paraphasias Disturbed verbal fluency Fluent symptoms Verbal paraphasias Fluent phonemic paraphasias Logorrhea Semantic j agon Neologistic jargon Disturbed comprehension Anomia Disturbed repetition Oral better than written Recovery Lesion site

Acquired Childhood aphasia

Aphasia in sinistrals

CAD

+

rare

+

+

+

+

+

+

+

+

+

+

+

rare rare

rare rare

-

rare rare rare

-

-

-

+

-

-

-

-

rare

rare

+

+

+

+

rare variable rare

+

?

+

good bilateral/LH/RH

good if expressive bilateral/LH/RH

good

Legend: + = present; - = absent; LH = left hemisphere; RH = right hemisphere

RH

156

Neurogenic Language Disorders in Children

EROSION OF STANDARD DOCTRINES Despite several contestations of the classical ideas expressed in the standard doctrine on AC A, a new era on the conceptual development only followed Woods & Teuber's (1978) landmark review paper entitled 'On changing patterns of childhood aphasia'. In radical contrast to the standard opinion, they demonstrated that: 1) crossed aphasia does not occur more frequently in children than in adults, 2) the extent of recovery does not clearly correlate with age at onset and 3) exceptions exist regarding the predominance of nonfluent aphasia characteristics. A sizable number of reports following this study systematically demonstrated the heterogeneous character of ACA (for a review, see Paquier & Van Dongen, 1996; 1998). Moreover, the remarkable conformity with acquired aphasia in adults provided a direct impetus for a radical break with the leading views on the neurobiological mechanisms of language acquisition such as the hemispheric equipotentiality and progressive lateralization hypotheses, which had held sway for more than a century. The untenability of the postulate that during the initial process of normal language acquisition both hemispheres are equally actively involved was furthermore supported by an increasing number of neuroanatomical, neurophysiological and neuroradiological studies which contend an innate predisposition of the left hemisphere for language acquisition. The view of aphasiologic uniformity and rapid recovery was also contended in CAD under the cumulative evidence of reports illustrating a broad spectrum of aphasic manifestations. In the first place, numerous CAD patients with receptive (fluent) aphasia were described and neuroradiologically documented. These reports established that, as a consequence of the methodological limitations inherent to the predominantly clinical approach in the pre-neuroradiological period, fluent types of CAD have been heavily underrepresented throughout the conceptual evolution of CAD. Carr et al. (1981) also expanded the evidence against a homogeneous nonfluent CAD syndrome reporting similar distribution figures of respectively 72% and 27% for the nonfluent-fluent dichotomy in both standard forms of aphasia and CAD. Secondly, several CAD patients were described with language profiles that did not at all or not significantly improve during follow-up (see Coppens & Hungerford, 1998; Marien et al, 2004). Thirdly, in opposition to the frequently reported dissociation between superior oral and inferior written language, reversed patterns in which oral language is more prominently affected than written language have been reported as well (see Marien et al, 2004).

PART 2: CROSSED APHASIA IN CHILDREN - SELECTION OF CASES Irrespectively of etiology we selected from the literature all right-handed patients with aphasia following a right hemisphere lesion. 1975 was chosen as a starting-point for this selection since Faglia, Rottoli and Vignolo (1990) showed that all fully acceptable CAD cases were published after this date. From this corpus of 170 cases, enriched with 10 personal

Crossed Aphasia in Children 157 observations (Marien et al, 2001b; Paghera et al, 2003), all childhood cases were selected. This resulted in a total number of five cases (2.7%). The first case was described by Assal & Deonna (1977) with a close follow-up of almost four years. Twelve years later, Assal (1987) reinvestigated this patient. The other patients were reported by Martins et al. (1987), Burd et al, (1990), Martins et al. (1995) and Marien et al. (2001a). Schematic case presentations such as the one in the sample of Hecaen (1976) and Woods & Teuber (1978) (case 18) were considered to be too concise to allow any further analysis and were not withheld in the present review. Demographic, clinical and neuroradiological data of these cases are summarized in Appendices 1 and 2. To allow for a comparison between cases -and hence theoretical deductions- all case descriptions were critically evaluated in terms of their reliability for a CAD diagnosis according to the revised criteria developed by Marien et al. (2004). A diagnosis of possible CAD was made whenever the three following criteria were met: 1) clearcut evidence of aphasia, 2) evidence of natural (i.e. not shifted) right-handedness as documented by a formal test, and 3) evidence of lesions strictly confined to the right hemisphere, leaving the left hemisphere structurally intact. Patients not complying with these three criteria were considered unreliable CAD. Two additional criteria were required to justify the diagnosis of reliable CAD: 4) absence of familial left-handedness or ambidexterity, and 5) no history of early brain damage and/or seizures in childhood. In the reliable CAD cases, anatomo-clinical correlations were judged to be reliable only if language was formally assessed during the lesion phase. The following were not considered to be exclusion criteria for CAD: 1) illiteracy and schooling, 2) bi- or multi-lingualism, 3) use of a tonal language, and 4) use of an ideographic script. As shown in the algorithm for childhood CAD (Figure 1), three cases did not meet the mandatory criteria: Assal & Deonna (1977), Assal (1987), Martins et al. (1987) and Martins et al. (1995). Assal & Deonna (1977) and Assal (1987) reported a five-year-old boy who sustained an extensive cortico-subcortical fronto-parietotemporal infarction secondary to a complete obstruction of the right internal carotid artery. After a ten-day period of mutism and severe auditory-verbal comprehension deficits, the aphasic syndrome evolved within three years to a nonfluent, adynamic and agrammatic output disorder with marked sequelae in the subsequent acquisition of reading and writing. A residual adynamic output syndrome associated with semantic naming defects and insufficient reading and writing capacities persisted 12 years after the onset of neurological symptoms. A two-year delay in schooling reflected learning disabilities which particularly consisted of memory disturbances and calculation defects. Twelve years post-onset, the neurological condition was characterized by a paralysis of the left arm. Unfortunately, neither the initial description, nor the follow-up report after 12 years mention any formal measures to assess the patient's hand preference. Despite thorough descriptions on the linguistic, neurocognitive and neurological level, absence of a standardized test to assess handedness casts doubt on the diagnosis of acquired CAD in this case. Both cases reported by Martins et al. (1987; 1995) were also classified as unreliable cases (cf. Figure 1). Martins et al. (1987) reported a 15 yearold-boy with an initially fluent aphasic syndrome that aggravated and evolved to a nonfluent

158 Neurogenic Language Disorders in Children

aphasia in association with the fatal course of a right posterior oligodendroglioma. Irrespective of surgical treatment and irradiation, the tumor progressed, invaded more anterior brain regions and caused the patient's death four months after onset of the neurological symptoms. Along the progression of actual right hemisphere destruction, a considerable mass effect of the infiltrative right hemisphere lesion on the left hemisphere was demonstrated on computerized tomography (CT) images. Though in this patient a close correlation between the aphasic symptoms and right hemisphere damage might be considered likely, distant intra- and interhemispheric mass effects as well as functional compensation mechanisms inherent to this type of pathology blurr the circumscription of the exact impact of the lesion on the clinical syndrome. Because of a possible impact on the left hemisphere, a CAD diagnosis is generally rejected when, as in this case, the underlying cause is an infiltrative or space-occupying brain lesion. In the second case reported by Martins et al. (1995), a penetrating gunshot trauma caused destruction of right frontal brain tissue in a 13-year-old right-handed boy. Only five days after this event the boy developed repeated complex partial and focal motor seizures as the first neurological symptoms. Analogous to Todd's paresis, a motor aphasia developed along a left-sided weakness following the epileptic fits. On admission, a CT scan of the brain disclosed a right frontal abscess and a midline shift with some mass effect on the left hemisphere. Martins et al. (1995) claimed that the clinical course ruled out any dysfunction of the left hemisphere arguing that the aphasia: 1) coincided with the development of the right hemispheric abscess, 2) transiently aggravated in association with the left-sided motor seizures indicating that the epileptic activity originated in the motor cortex of the right hemisphere, and 3) followed the course of treatment of the abscess. However, viewing this patient as an unambiguous CAD can be challenged for various reasons. Firstly, penetrating brain injuries cause more diffuse brain damage especially when complicated by concomitant brain tissue infections. In this respect, it should be noted that the highest CAD frequencies have been reported in association with trauma - up to 18% in the Mohr et al.'s study (1980). The extreme values reported in these populations (Ludwig, 1939; Mohr et al., 1980) underscore the importance to control for etiology when a CAD diagnosis is considered. The fact that no aphasic symptoms were encountered at the time of actual brain destruction but only in association with the genesis and course of the frontal abscess makes it equally plausible that the brain was more diffusely affected. Secondly, it is not appropriate to infer definite conclusions with respect to cerebral language representation on the basis of epileptic phenomena, since even in focal epilepsies bilateral cerebral dysfunction cannot be excluded conclusively. Thirdly, the child presented with a history of developmental language disturbances. Until the age of four the boy was said to produce only unintelligible sounds and to communicate by means of pointing and gesturing. In marked contrast to his extremely limited expressive language capacities, auditory-verbal comprehension was considered within the normal ranges. Speech therapy, which was initiated from the age of three years onwards and which was continued for four subsequent years, apparently yielded a favourable outcome. At the age of seven the boy entered the first grade of a normal school but displayed learning

Crossed Aphasia in Ch ildren

15 9

disabilities. He had to repeat the second and fourth grade twice, and difficulties in learning to read and write as well as difficuties with the acquisition of a foreign language were reported. An increasing amount of evidence has corroborated the hypothesis that, in cases of developmental language disorders, alterations in the typical pattern of cerebral dominance for language may take place. Lou et al. (1984), for instance, showed that confrontational naming tasks performed in children with developmental aphasia fail to disclose the expected blood perfusion levels in the left perisylvian region, while Jernigan et al. (1991) as well as Plante et al. (1991) documented absence of normal anatomical brain asymmetries on magnetic resonance imaging (MRI). Given the assumption that in Martins et al.'s (1995) patient, the aphasia solely originated from focal destruction of right frontal brain tissue, the history of a developmental language disorder might be considered the reflection of an early pathological condition in which the failure of the left hemisphere to acquire expressive language functions might have led to a shift in cerebral dominance for language. The Martins et al.'s (1995) case can therefore alternatively be considered an exponent of a subgroup of patients with pathologically induced atypical cerebral dominance and anomalous intrahemispheric specialization for language. The case highlights the importance to distinguish patients with developmental disturbances from patients with a normal cognitive development in discussions on functional brain organization.

Figure 1 - Reproduced from Marien et al. (2001a; 2004)

160 Neurogenic Language Disorders in Children

The cases reported by Burd et al. (1990) and Marien et al. (2001a) fulfilled the criteria for definite CAD. Burd et al. (1990) assessed handedness in a four-year-old boy who had become aphasic after an infarct in the right middle cerebral artery territory by parental report using the Edinburgh Inventory (Oldfield, 1971). The integrity of the left hemisphere was confirmed on CT, which disclosed a large cortico-subcortical fronto-parietal and posterior parietal hypodens lesion of the right hemisphere. A vascular cause was clearly established and the aphasic as well as neurocognitive symptoms were thoroughly documented during a three year follow-up period. Though the child had no personal history of developmental disabilities, his familial history was positive for dyslexia and seizures on the maternal side and for dyslexia and dysorthographia on the paternal side. Besides these problems, attentional and concentration disturbances were reported in the extended family. The patient's subsequent learning impairments for reading, his further language development, his attention and concentration problems might either constitute the sequelae of the acquired brain lesion - in which context the family history may have been coincidental - or might form the expression of a genetic predisposition for learning disabilities. Marien et al. (2001a) reported a 13-year-old strongly right-handed girl who developed aphasic symptoms following a right cortico-subcortical temporo-parietal haemorrhage. Repeat CT and MRI of the brain confirmed the structural integrity of the left hemisphere. Handedness was assessed by means of the Edinburgh Inventory (Oldfield, 1971) which yielded a laterality quotient of +100. Medical history, growth and developmental milestones were normal. She was born at term after normal gestation and labour and there had been no perinatal or postnatal problems. Her scholastic achievements had always been above average and there was no familial history of (neuro)developmental disorder or learning disability. No familial strain of left-handedness was found after careful inquiry. During a longitudinal follow-up of ten years the aphasic manifestations were described on a temporal basis in agreement with the three epoch timeframes for models of aphasia (Mazzocchi & Vignolo, 1979; Basso et al., 1985; Alexander, 1989). To avoid remote functional effects of the hemorrhagic lesion, generally accounting for the instability of aphasic profiles during the first two or three weeks post-onset (acute phase), extensive language examinations were performed in the lesion phase. During this phase, which might last up to four months, the purest and most robust anatomo-clinical correlations are found (Alexander, 1989). To capture various effects of recovery and functional brain reorganization, a third extensive neurolinguistic examination was performed during the late phase, ten years after onset of neurological symptoms. Neurocognitive investigations using standardized test batteries were performed on a similar temporal basis.

Acquired childhood CAD characteristics Only the definite CAD cases reported by Burd et al. (1990) and Marien et al. (2001a) constitute a sufficiently reliable source of information to allow comparison between cases and

Crossed Aphasia in Children 161 theoretical deductions. Though this small number of patients does not allow general conclusions, potentially relevant tendencies might nevertheless already be suggested with respect to aphasic semiology and lesion-behavior relationships (Marien et al., 2001a). Aphasia symptoms. As displayed in Table 2, aphasic symptoms were listed according to a three epoch time-frame model encompassing acute, lesion and late phase findings (Mazzocchi & Vignolo, 1979). To present the semiological characteristics in more detail, we added to this model symptom descriptions 'at early onset' and at an 'end stage' after follow-up. At onset, both cases invariably presented with a similar aphasic syndrome consisting of mutism and marked auditory-verbal comprehension disturbances. Within the acute phase, they partly recovered the ability to comprehend and they also started to speak again. Within a fortnight the syndrome evolved to a severe adynamic output disorder combined with still prominent auditory-verbal comprehension defects. Both patients subsequently developed a variety of symptoms on distinct linguistic levels within the acute phase. The patient described by Burd et al. (1990) showed severe anomia and prosodic disturbances after an eight-day period of mutism. The restricted verbal output of the patient described by Marien et al. (2001a) was contaminated by phonematic paraphasias and dysarthria. The cardinal feature of the dysarthria was

a hypertonic,

effortful

articulation.

During the

lesion phase,

auditory-verbal

comprehension of daily conversations improved to functional levels for both patients. Apart from adynamia, they showed prosodic deficits (bradylalia) and anomic disturbances. The anomia in Burd et al.'s (1990) patient had improved but confrontational colour naming remained moderately impaired. As part of an adynamic output syndrome, word-retrieval disturbances in the patient reported by Marien et al. (2001a) were restricted to self-generated speech. In this patient, repetition normalized during the lesion phase but reading and writing remained deficient due to (morpho)syntactic errors. The patient described by Burd et al. (1990) had not yet initiated the process of written language acquisition at the moment of brain injury. During the late phase, commencing around three months post-onset, the most important changes in the limited sample of childhood CAD patients seem to consist of a remission of verbal-auditory comprehension defects. In the patients reported by Burd et al. (1990) and Marien et al. (2001a), the adynamic features resolved within respectively nine and four months. In Burd et al.'s (1990) patient, a mild dysarthria and resolution of prosody were reported as late phase findings, nine months after onset. Dysarthric features were no longer mentioned at the end of the follow-up, 27 months post-onset. As developmental outcome cannot be anticipated after this restricted follow-up period, we interpreted the findings reported in Burd et al. (1990) as late-phase phenomena. Defective comprehension of grammatical morphemes, insufficient sentence repetition and insufficient oral vocabulary characterized the language profile of this seven-year-old boy in this period. In contrast to this observation, the longitudinal follow-up of 10 years of the patient reported by Marien et al. (2001a) disclosed residual anomia in confrontational naming tasks.

162 Neurogenic Language Disorders in Children Table 2 — Summary of speech and language symptoms in two childhood CAD cases represented in a time-frame model

Authors

Acute Phase Onset 21 days B M B M

Lesion Phase >21 days B

M

Symptoms Comprehesion defects Mutism Adynamia Agrammatism Repetition defects Naming defects Phonemic Paraphasias Reading disturbances Writing disturbances Prosodic disturbances Dysarthria

+ +

+ +

+

Late Phase > 3 months 10 yrs B M M 9m

27m

+

0

sem

-

gm

0

-

-

-

-

-

-

+

+

0

+

-

-

-

0

0

0

+

0

0

0

0

0

+

-

+

+

-

+

0

+

+

+

+

0

+

0

-

0

0

0 0

0

0

0

+

0

0

0

0

0

0

+

0

0

0

+

0

+

+

-

-

0

0

+

0

+

+

0

0

+ 0

Legend: B = Burd; M = Marien; + = applicable; - = not applicable; 0 = no data available; y = years; m = months; sem = semantics; gm = grammatical morphemes Cognitive and behavioural symptoms. In the acute phase no thorough neurocognitive assessments were performed in either of the two children under consideration (Table 3). Neurocognitive assessments performed by Burd et al. (1990) during the lesion phase disclosed a drawing apraxia, calculation problems and memory disturbances. During this phase, the patient of Marien et al. (2001a) also displayed calculation deficiencies secondary to a distorted visuo-spatial processing, right-left orientation problems and a triad of gnostic disturbances consisting of an autotopagnosia, finger agnosia and astereognosis. In the late phase, the gnostic and spatial disturbances persisted in this patient and were complicated by concentration defects, constructional

difficulties

and minor learning disabilities

for

mathematics and foreign language learning. The patient reported by Burd et al. (1990) showed learning disabilities, concentration difficulties and neglect phenomena during the late phase. A slight, though not significant discrepancy between verbal (VIQ = 85) and performance (PIQ = 92) intelligence levels was reported by Burd et al. (1990) after 27 months of follow-up. Contrary to these findings, Marien et al. (2001a) reported a more pronounced dissociation between the VIQ and PIQ in their patient three months post-onset. The WISC revealed a normal global intelligence quotient of 100 with a discrepancy of 14 points between the verbal (92) and performance intelligence level (106). After 10 years the IQ levels had homogenized.

Crossed Aphasia in Children 163 Both patients under consideration also developed social and psychological problems. The patient of Burd et al. (1990) displayed enuresis and elective mutism at school. The patient of Marien et al. (2001a) withdrew from social contacts and developed feelings of inferiority and depressive stigmata secondary to physical incapacities. Table 3 — Summary of lesion and late phase cognitive symptoms of two childhood CAD cases Lesion Phase >21 days B M

LatelPhase lOyrs

> 3 months B

M

M

+

+

Authors 9m

27m

Cognitive Domains Apraxia bucco-labio-lingual ideomotor ideational constructive Agnosia visual tactile fingers autotopagnosia Neglect visuo-spatial motor R/L orientation Calculation Learning Memory Concentration Behavior Intelligence Global IQ Verbal IQ Performance IQ

-

-

-

-

-

-

+

+

-

-

+

-

+

+

-

+

+

-

+

+

+

-

+

+

-

+

-

+

+ + +

+

+

97

+ + +

+

+ +

+ +

93*

100

99

85

106

100

109

92

98

Legend: B = Burd; M = Marien; + = applicable; - = not applicable; y = years; m = months; blank = no data available; * personally derived intelligence levels from available scaled scores using the Flemish and Dutch Wisc-R norms.

164

Neurogenic Language Disorders in Children

Anatomoclinical correlations. On the basis of the anatomoclinical characteristics both cases were divided into mirror image and anomalous, according to Henderson's (1983) and Alexander et al.'s

criteria (1989). These authors denoted cases with lesion-aphasia

relationships comparable to those following an analogous lesion in the left hemisphere as mirror-image and cases with an unexpected lesion-aphasia profile as anomalous. In Burd et al.'s (1990) patient, large cortico-subcortical damage to fronto-parietal and posterior parietal structures initially caused a severe aphasic disorder with equal involvement of expressive and receptive abilities. Since the lesion-aphasia profile does not match standard lesion-symptom configurations this patient represents the first example of the 'anomalous' CAD in the ACA literature. In the light of the anatomical structures involved and the severity of the aphasic syndrome at onset, the rapid evolution within 27 months to an only discrete syndrome of insufficient linguistic performances on the level of grammatical morpheme comprehension, oral vocabulary and sentence imitation represents a finding beyond the late phase expectations for standard aphasia. In contrast to this case, the anatomoclinical findings reported by Marien et al. (2001a) are not within plausible expectations. The posteriorly located, high parietal lesion which extended subcortically to the crus posterior of the internal capsule induced an adynamic aphasic syndrome complicated by agrammatism. Two distinct dominant hemisphere areas are most typically discerned as the anatomical substrate for this type of aphasia: the area situated anterior and/or superior to Broca's area and the territory supplied by the anterior cerebral artery. As evidenced by repeated neuroimaging, neither of these areas had sustained damage. Destruction of the posterior limb of the internal capsule could also not be held responsible for the adynamic language phenomena (Marien et al., 2001).

Since

the

lesion-aphasia

profile

does not

match

standard

lesion-symptom

configurations, within the restricted group of childhood cases this patient represents the first example of the 'anomalous' CAD variant.

Acquired childhood CAD compared Acquired childhood CAD versus classical ACA. In contrast to the statement in the updated standard doctrine on ACA (Brown & Hecaen, 1976), age at onset in the small sample of childhood CAD patients does not seem to be a significant parameter for aphasia typology. In this respect, mutism not only occurred in the youngest CAD patient described by Burd et al. (1990) but also in the patient reported by Marien et al. (2001a) who was 13 years of age at the onset of neurological symptoms. Agrammatic features were not encountered in Burd et al.'s (1990) four-year-old patient but were present in the patient reported by Marien et al. (2001a). Articulatory defects were found in both cases in the context of predominantly nonfluent aphasia. Though inherently fluent aphasic characteristics such as logorrhoea, semantic or neologistic jargon did not occur in the limited corpus of childhood CAD patients, comprehension disturbances might possibly represent a more prominent feature than the onethird ratio mentioned in the doctrine for patients with standard ACA. In agreement with the

Crossed Aphasia in Children 165 standard doctrine, and similar to adult forms of aphasia, no association between logorrhoea and comprehension defects was found. In the restricted childhood CAD group, mutism was found as an early acute phase phenomenon irrespective of lesion location. No such correlation seems to hold currently for the comprehension disturbances which occurred within the expectations of standard anatomoclinical correlations. Dysarthric speech characteristics, prosodic abnormalities and difficulties in written language represent childhood CAD phenomena that are not dealt with in the standard thinking about ACA. Acquired childhood CAD versus adult CAD. Our limited sample of childhood CAD cases seems to share a number of anatomoclinical similitudes with adult CAD. In the childhood CAD group, the lesion-symptom profiles of the lesion phase follow the distinction made in adult CAD between anomalous - mirror image cases (Marien et ai, 2004). In the light of the conceptual evolution of both ACA and adult CAD, it further seems plausible to expect that the heterogeneity of symptoms of adult CAD will also be reproduced in future descriptions of childhood CAD. Apart from a variety of expressive and receptive aphasic manifestations, the limited group of reported patients seems to indicate that prognosis for complete recovery is not univocally favourable when poor academic performance and subsequent scholastic difficulties are also taken into consideration. Acquired childhood CAD and language lateralization A wide variety of explanations has been proposed for CAD such as absence of decussation of cortico-spinal tracts (Souques, 1910), a familial strain of sinistrality (Ardin-Delteil et ai, 1923), involvement of phylogenetically older subcortical structures (Habib et ah, 1983), a simultaneously acquired invisible small left hemisphere lesion (Castro-Caldas et al., 1986), inhibitory metabolic repercussions of the right hemisphere lesion on left hemisphere functioning (Schweiger, 1987) and natural variation in functional brain organization due to the presence or absence of a single gene (Alexander & Annett, 1996). To these, Brown and colleagues (1973; 1976) added the hypothesis that CAD is the result of incomplete lateralization of language functions in the left hemisphere during maturation. This hypothesis implies that during normal maturation a gradual shift takes place from initially bilateral to unilateral left hemisphere dominance for language. The concept of innate equipotentiality of both cerebral hemispheres for language at birth and the subsequent process of progressive lateralization of language functions was firmly established when Lenneberg (1967) claimed on the basis of a high incidence of CA in children2 and the transient nature of symptoms in ACA- that there exists a critical age (nine to ten years of age) below which language functions are not yet clearly lateralized. This view was called into question and was fundamentally contested. Hecaen (1976) proposed to lower the critical age referring to Kxashen's (1973)

R i i c c p r ( 1 Q l ^ ^ nKtdinP'/^ nrt ini--ii-J*»ti <-»*=> f i n i i r p ' r\f A A"/,

166 Neurogenic Language Disorders in Children observation that Basser's (1962) study contained no CAD patients with right hemisphere damage sustained after the age of five. In their population of 65 brain-damaged children Woods & Teuber (1978) found a marked disparity between the aphasiogenic power of left (15/34) and right (4/31) hemisphere lesions. Following the fact that these findings sharply contrasted with the prevailing insights of hemispheric equipotentiality for language, they extensively reviewed the literature on AC A and noticed a dramatic change of the incidence of childhood CAD over time. While one-third of the patients in the studies published before the 1930s were claimed to be CAD representatives, only a proportion of 5% was found in the studies undertaken after 1940. Woods & Teuber (1978) held undetected bilateral cerebral involvement before the introduction of antibiotics and mass immunization programs in the earlier studies responsible for the higher incidence. Similarly, Satz & Bullard-Bates (1981) concluded from a review based on ACA cases reported since 1940 that: 1) irrespective of age, the risk of ACA is substantially greater after left than right hemisphere damage, 2) CAD in children is rare after three to five years of age (or perhaps even earlier), and 3) CA is more commonly observed in sinistral children regardless of age. Carter et al. (1982) critically analyzed the data of five ACA studies (Basser, 1962; Shillito, 1964; Isler, 1971; Hecaen, 1977; Woods & Teuber, 1978) applying exclusionary rules and advanced statistical methods for estimating the distribution of language organization. Data were moreover seperately analyzed according to the critical age boundary of five years of age as postulated by Krashen (1973) and Hecaen (1976). For the age group from six to 15 years consisting of 107 non-lefthanded children, Carter et al. (1982) obtained a figure of 97% left-hemispheric language dominance with a standard deviation of six percent. When the Basser's (1962) study was included in the analysis of the data of the 64 younger children, figures diminished to 69% and 31%, respectively for the proportion of children with left-sided and bilateral language representation. The estimated proportion of bilateral language representation dropped from 31% to 16%, while the proportion of left-sided language representation increased from 69% to 84% when the Basser (1962) study was not taken into consideration. Carter et al. (1982) additionally stated that, when all cases with trauma and undetermined handedness were excluded from the four remaining studies, only four patients with a right-hemiphere lesion remained. In none of these children the lesion caused aphasia. Considering the developmental maturation hypothesis, Carter et al. (1982) concluded from their results that language distribution for older right-handed children is nearly identical to that for right-handed adults. They further stated that, even when the hypothesis is adjusted with the modification that righthanded children below the age of five years have speech organization distributions similar to those of sinistrals, the developmental maturation hypothesis remains incorrect since the estimated figure of 3 1 % for bilateral language representation in this group is not compatible with the 70% figure for left-handed adults. In a less stringent analysis retaining only the children with undetermined hand preference, the authors obtained similar adjusted proportions of aphasia following left and right hemisphere lesions to those reported for adults, resulting in estimated figures for left and right hemisphere language dominance of 0.94 and 0.06,

Crossed Aphasia in Children

167

respectively. On the basis of these findings, Carter et al. (1982) rejected the developmental maturation hypothesis and adopted the 'developmental invariance position'. This hypothesis advocates that 1) lateralized cerebral specialization for language is innate, 2) the cerebral organization of language in children is similar to that of adults, and 3) it does not change with time. The second founding factor of the equipotentiality theory concerns the speed and extent of recovery which were reported to be faster and better in children than in adults. Though there is general agreement about the fact that functional recovery from comparable aphasic lesions decreases with age, the variety of different interrelated variables determining the outcome acts as a confounding factor. Among others, type of language disorder (expressive versus receptive or combinations of both), etiology (e.g. trauma versus vascular lesions), extent of the lesion, duration of post-traumatic coma, motor symptoms, and electroencephalographic characteristics have all been granted important prognostic variables. Neuroanatomical, neurophysiological and neurobehavioural studies have also discredited the developmental maturation hypothesis with explicit evidence. Apart from right-left asymmetries on the gross morphological level, interhemispheric histological differences of cytoarchitectonically defined regions have been reported in the adult, neonatal and even fetal brain (e.g. Geschwind & Levitsky, 1968; Teszner et al., 1972; Galaburda et al., 1978; Falzi et al., 1982; Eidelberg & Galaburda 1984). These biological differences favour the view of a genetic predisposition of particular brain regions to develop specific functions. On a functional-anatomical level, interhemispheric differences in the processing of speech and nonspeech signals, which were demonstrated in the neonate brain using dichotic listening procedures (e.g. Bertoncini et al, 1989) and auditory event-related potentials (e.g. Molfese et al. 1988), also contributed to the hypothesis that lateralized specialization for language is already present at the onset of language acquisition. Our analysis of children with CAD also suggests that the equipotential and progressive maturation hypothesis is not tenable. In the CAD patient with brain damage sustained around the age of five years (Burd et al, 1990), residual language disturbances contend the notion of a complete interhemispheric language reorganization. Furthermore, Marien et al.'s, (2001a) findings of severe language symptoms encountered in a 13-year-old patient are inconsistent with the notion that maturation of cerebral dominance for language should be accomplished around puberty. On the other hand, the low incidence of CAD in children indirectly corroborates the view that lateralized cerebral dominance for language represents an innate neurobiological condition. CONCLUSIONS From a historical perspective, striking similarities have characterized the conceptual development and evolution of ACA and CAD. On the common basis of a presumed incomplete language lateralization process, overt application and even transposition of the concepts of the standard doctrine on ACA to the clinically comparable CAD profiles led in the

168 Neurogenic Language Disorders in Children

1970s to a confluence of both aphasic conditions. Similar to the conceptual development of AC A, a wide range of counterexamples provided strong evidence against the 'standard doctrine on CAD' and modified the concept of a uniform syndrome that, irrespectively of lesion location, would consist of nonfluent, agrammatic and often transient language symptoms with a frequent dissociation between superior oral and inferior written language. No symptom constellations have so far been reported that distinguish CAD from the rich spectrum of standard aphasic syndromes following damage to the left hemisphere. From the restricted case study of five children documented in the literature since 1975, only two (Burd et al, 1990; Marien et al, 2001a) could be reliably assigned an unambiguous diagnosis of childhood CAD. The other cases (Assal & Deonna, 1977; Assal, 1987; Martins et al, 1987; 1995), however, underscore the importance to stringently control for handedness, etiology and neurodevelopmental factors when CAD is considered and its impact on functional brain organization discussed. Supporting evidence exists in favour of developmental language disturbances as an influencial variable in the functional organization of the brain. We therefore proposed to form distinct groups of childhood CAD based on developmental characteristics (Marien et al, 2001a). Patients in whom a partial or complete right hemisphere dominance for language is suspected in the absence of prior developmental language anomalies belong to a group of 'primary CAD cases'. Patients with developmental language disturbances belong to a group of 'secondary CAD cases'. In this group, the presence of developmental language disturbances might reflect a maturation dysfunction of the language-dominant hemisphere that likely accounts for the supposed selective or complete shift of cerebral dominance for language to the right hemisphere. The common aphasic pattern of the limited number of convincing childhood CAD representatives consists of an initially severe expressive and receptive language syndrome characterized by speechlessness and severe auditory-verbal comprehension defects. In its further course, this syndrome seems to evolve rapidly to a predominantly adynamic output disorder that may be of long duration. A variety of residual semantic deficits might be expected as (final) outcome variables after longitudinal follow-up. Agrammatic features, repetition disturbances, phonematic paraphasias, (subsequent) reading and writing disorders, prosodic disturbances and dysarthric features occurred. None of these symptoms persisted after longitudinal follow-up. A variety of neurocognitive symptoms seems to characterize the cognitive profiles of the representative cases. Visuo-constructive disturbances of apraxic or perceptual origin occurred in both patients at different epochs. Calculation disturbances represented relatively early reported lesion-phase phenomena and, along with learning disabilities, memory disturbances and concentration defects, they constituted a major (complicating) factor during recovery. Autotopagnostic disturbances occurred in one patient as well. Although the distribution of the IQ profile might remain asymmetrical, intelligence levels normalized. Psychogenic socio-behavioural problems were also encountered. Alterations in social contact and secondary depressive symptoms constituted major reactive phenomena.

Crossed Aphasia in Children 169 On the anatomoclinical level, several tentative conclusions may be proposed. In the first place, acquired CAD in the selected patients is irrespective of lesion localization characterized at onset by a uniform nonfluent aphasic syndrome. The subsequent differential evolution of predominantly nonfluent aphasic symptoms towards a variety of symptom complexes in the late phase is a rather unexpected finding. Although this evolution emphasizes the importance of temporal factors in the description of neurological language phenomena, it might additionally reflect the anomalous patterns of inter- and intrahemispheric

language

organization inherent to this group of exceptional patients. From the limited number of observations, the childhood CAD characteristics so far identified differ in a number of aspects from the concepts expressed in the standard doctrine on ACA. Aphasic typology in childhood CAD seems to be unaffected by age at onset and comprehension disturbances seem to represent at least initially a much more prominent feature than the one to three ratio mentioned in the standard doctrine for patients with standard ACA. The concept of a complete interhemispheric language re-organization after early cerebral damage is also contended by the aphasic sequelae reported in the CAD children. Taken together with the extremely low incidence of CAD in children, these considerations corroborate the view that lateralized cerebral dominance for language represents an innate neurobiological condition. There is a need for carefully controlled clinical research on larger groups of cases with childhood CAD to improve the insights in the pathophysiological mechanisms of anomalous cerebral language organization in the child. At an elementary level, future clinical studies might, for instance, be directed to the question whether the semiological heterogeneity in adult CAD is also present in childhood CAD and whether the anatomoclinical correlations can be further divided into distinct patterns such as the "mirror image - anomalous case' dichotomy.

APPENDIX I Case summaries of acquired childhood aphasia associated with right hemisphere lesions: Clinical and neurolinguistic data. [Abbreviations: y: years; m: months; M: male; F: Female; AVM: arteriovenous malformation] ASSAL & DEONNA (1977) Age/Gender: 5y 9m / M Etiology: Infarction Aphasic symptoms: Type and course During 10 days: mutism, minimal comprehension after heavy prompting; day 14: some words while singing; during the following weeks: monophasic output; after

lm: sporadic

170

Neurogenic Language Disorders in Children

comprehension errors in semi-complex instructions; after 2m: first comprehensible words; the following months: agrammatic output, poor vocabulary; after 6.5m: unaltered comprehension, spontaneous speech limited to interjections, phonemic distortions in responses, disturbed repetition, long delay in naming; after 3v 10m; normal comprehension, reduced spontaneous speech (<7 words), phonemic distortions, agrammatic errors, repetition disturbances for words (>4 syllables), slow syllabic reading with phonemic errors, insufficient writing. 12v post-onset: sparse and fragmented spontaneous speech, semantic naming errors, insufficient verbal fluency, slow reading, inverted spelling, bad orthography (normal verbal comprehension, repetition, no word deformations). Lesion site localization Arteriography on day 2: complete obstruction of the right internal carotid artery CT after 12 years: right fronto-parieto-temporal lesion involving the 3rd frontal, the 1st temporal convolution & the supramarginal gyrus, the anterior limb of the internal capsule, the anterior & middle parts of the caudate nucleus & the putamen, atypical frontal asymmetry (left anterior region more developed than the right). MARTINS ETAL. (1987) Age/Gender: 15 / M Etiology: Oligodendroglioma, partially resected, irradiation therapy 14 days post-surgery Aphasic symptoms: Type and course lm before admission: word-finding difficulties; admission: fluent anomic speech with rare literal and verbal paraphasias, impaired sentence repetition, impaired Token Test, limited word reading, partial comprehension of simple texts, agraphia; 7 days post-surgery: unchanged picture and agrammatism; 14 days post-surgery: worsened aphasia, change to nonfluent output; 40 days post-surgery: further language deterioration, only sparse isolated word production, severe anomia, paraphasias, mild dysarthria, agraphia, alexia. Lesion site localization CT on admission: right temporo-parieto-occipital tumor; CT 14 days post-surgery: no evidence for a regrowth of the tumor or a hematoma; CT 40 days post-surgery: anterior extension with tumor growth in the basal ganglia, the internal capsule and the frontal white matter. BVRDETAL. (1990) Age/Gender: 4y 10m / M Etiology: Infarction Aphasic symptoms: Type and course For 8 days after admission: speechlessness; at day 8: single word utterances, severe anomia, speech initiation defects; within a few days: correct completion of one-step commands, more

Crossed Aphasia in Children 171 fluent output, repetition of 3 numbers and words, impaired naming and prosody; after 3m (age 5y1m): functional

comprehension of conversations, fluent spontaneous speech, short

sentences, mild dysarthria, impaired colour naming; after 9m (age 5y7m): normal sentence length, sentence repetition most impaired, selective naming difficulties, no prosodic defects; after 27m (age 7ylm): insufficient

comprehension of grammatical morphemes, oral

vocabulary and sentence imitation. Lesion site localization CT on admission: large right cortico-subcortical fronto-parietal and posterior parietal lesion. MARTINS ETAL. (1995) Age/Gender: 13/M Etiology: Gunshot injury & infection Aphasic symptoms: Type and course Developmental

language

disturbances:

unintelligible

speech

until

age

4,

gestural

communication, normal comprehension; between age 3-7 good recovery with speech therapy, difficulties in foreign language learning and written language acquisition. Day 3 of admission: impaired comprehension at simple levels, loss of verbal initiative, nonfluent speech, isolated words, multiple pauses, word-finding difficulties, perseverations, verbal paraphasias, normal word repetition. On day 10: mixed transcortical aphasia with impaired comprehension, nonfluent low verbal output of isolated words or telegraphic sentences (normal articulation, prosody, automatic speech, repetition of sounds and sentences), rare verbal paraphasias, moderately impaired naming with semantic paraphasias and perseverations, disturbed reading comprehension, spelling errors, disturbed written syntax, paragraphias, perseverations and neologisms; at 3 weeks: speech deterioration; till 10 days post-surgery: total speech loss; at 2.5m: recovery of comprehension. Lesion site localization

CT on admission: right frontal abscess. MARIEN ETAL. (2001) Age/Gender: 1 3 / F Etiology: Hemorrhage, AVM resection on day 73 Aphasic symptoms: Type and course On admission: non-responsive; at day 2: global aphasia; during the following 3 weeks: nonfluent

output,

adynamia, phonemic paraphasias, hypertonic

dysarthria,

disturbed

comprehension; at day 25: full-blown receptive and expressive agrammatism, disturbed semantic knowledge, bradylalia, hypertonic articulation, agrammatic reading and writing errors; at day 83 (10 days post-operatively): receptive agrammatism, bradylalic and

172 Neurogenic Language Disorders in Children

dysprosodic output, agrammatic written output; after 10 y: discrete residual anomia on the BNT visual confrontation naming test. Lesion site localization CT on admission: right temporo-parieto-occipital lesion. Arteriography: hemorrhagic dislocation of the middle cerebral artery branches, small parietal AV malformation. MRI after 10 years: extensive lesion extending from the crus posterior of the internal capsule to high parietal and encroaching from the precentral sulcus upon the focally dilatated right lateral ventricle with marked atrophy of the posterior part of the corpus callosum. APPENDIX 2 Case summaries of acquired childhood aphasia associated with right hemisphere lesions: Clinical, neurocognitive and neurological data. [Abbreviations: y: years; m: months; M: male; F: Female; IQ: intelligence quotient; VIQ: verbal IQ; PIQ: performal IQ] ASSAL & DEONNA (1977) Age/Gender: 5y 9m / M Neurocognitive & neurobehavioural symptoms: Type & course Onset: coma, left hemiparesis, eye deviation to the right; after lm: independent walking, paralysis of left arm (normal sensation & visual fields); after 12y: unchanged neurological tableau. MARTINS ETAL. (1987) Age/Gender: 15 / M Neurocognitive & neurobehavioural symptoms: Type & course Admission: visuo-spatial defects, left-sided neglect (normal bucco-facial, limb and drawing praxis); 40 days post-surgery: mildly impaired constructional praxis (no visual neglect). 1 month before admission: progressive loss of vision, headaches, word-finding difficulties; I week before admission: left-sided paresis; admission: bilateral papiloedema, left hemianopia, left hemiplegia and hypoesthesia; died 3m later. BURD ETAL. (1990) Age/Gender: 4y 10m / M Neurocognitive & neurobehavioural symptoms: Type & course After 3m (age 5ylm): difficulties drawing simple shapes, insufficient visual motor ntegration, deficient preschool mathematics level, impaired attention and short-term memory, elective

Crossed Aphasia in Children 173

mutism; after 9 months (age 5y7m): Stanford-Binet IQ = 97, concentration difficulties, moderate problems on visual discrimination and visual closure tests (no gnostic or apractic deficits); after 27m (age 7ylm): delay in schooling, special education for learning disabled children, persisting concentration and memory problems, spatial distortions in clock drawing, average IQ, motor neglect left hand. Clinical and neurological findings Sudden onset of left hemiplegia; on admission: left hemiparesis affecting the arm more than the leg, confusion; after 9m (age 5y7m): minimal left hand weakness (no sensory loss or hemianopia); after 27m (age 7ylm): residual left hemiparesis affecting the arm more than the leg. MARTINS ETAL. (1995) Age/Gender: 13/M Neurocognitive & neurobehavioural symptoms: Type & course Developmental language problems: repeated grades 2 & 4 at school; day 10 of admission: acquired acalculia, mild left neglect (no spatial dysgraphia or dyscalculia); at 2.5m: remission of visual neglect, onset behavioural disturbances with attentional deficits, impulsive, desinhibited behaviour: at 6 m: desinhibited, provocative behaviour made a return to school impossible, WISC VIQ = 75, PIQ = 105, GIQ = 89. Clinical and neurological findings Admission 5 days after a gunshot injury: complex partial seizures, focal motor seizures, postictal aphasia, left hemiparesis; at 3 weeks: deterioration of speech and drowsiness (surgical drainage of the abscess); at 2.5m: fully recovered hemiparesis. MARIEN ETAL. (2001) Age/Gender: 13/F Neurocognitive & neurobehavioural symptoms: Type & course Day 27: unilateral astereognosis, fmgeragnosia, autotopagnosia, afferent dysgraphia and spatial dyscalculia, right-left disorientation; day 85: amelioration of visuo-spatial disturbances, unchanged gnostic defects, WISC-R VIQ = 106, PIQ = 92; at lOy normalized IQ profile, poor concentration, poor visuo-constructional abilities Clinical and neurological findings On admission: sub-coma, left hemiplegia; post-surgery (after 73d & 10y) improvement to mild residual left-sided sensory-motor hemisyndrome; lOv post-onset: normal.

174

Neurogenic Language Disorders in Children

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Crossed Aphasia in Children 175

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Crossed Aphasia in Children 111 Humphrey, M. and O. Zangwill (1952). Dysphasia in left-handed patients with unilateral brain lesions. JAWP, 15, 184-193. Isler, W. (1971. Acute

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180 Neurogenic Language Disorders in Children Taylor, J. (1905). Paralysis and other diseases of the nervous system in childhood and early life. J & A Churchill, London. Teszner, D., A. Tzavaras, J. Gruner and H. Hecaen (1972). L'assymetrie droit-gauche du planum temporale: a propos de l'etude anatomique de 100 cerveaux. Rev Neurol, 179, 444-448. Van Dongen, H. R. and M. C. B. Loonen (1977). Factors related to prognosis of acquired aphasia in children. Cortex, 13, 131-136. Wada, J. and T. Rasmussen (1960). Intracarotid injection of sodium amytal for the lateralization of cerebral speech dominance: Experimental and clinical observations. Neurosurgery, 17, 266-282. Wagner, W. and K. Mayer (1933). Psychologische Untersuchung an der Sprachstorung einer Zwolfjahrigen (Psychopathologische Studie zur Frage der Grundfunktionsstorungen). Monatsschr Psychiatr Neurol, 87, 108-55. Wallenberg, A. (1886). Ein Beitrag zur Lehre von den cerebralen Kinderlahmungen. Arch Kinderheilkd, 24, 384-439. Woods, B. T. and L. Teuber (1978). Changing patterns of childhood aphasia. Ann Neurol, 3, 273-280.

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RECOGNIZABLE SPONTANEOUS LANGUAGE CHARACTERISTICS IN A YOUNG ADULT TWELVE YEARS AFTER SHE BECAME APHASIC AS A CHILD Philippe F. Paquier Department of Neurology, University Hospital Erasme ULB; Department of Linguistics, Free University of Brussels (VUB-ULB); Department of ENT-surgery, School of Medicine, University of Antwerp, Belgium. Valerie R. van Maldeghem Speech and Hearing Rehabilitation Center, University of Ghent, Belgium. Hugo R. van Dongen Department of Child Neurology, Children's University Hospital Sophia-Rotterdam, The Netherlands. and Wouter L. Creten Department of Physics, Research Group on Biomedical Physics, University of Antwerp, Belgium.

Abstract — We report on a patient who developed fluent aphasia when she was 9. Spontaneous language characteristics were analyzed in the acute phase, and 1014 and 12 years post-onset to determine why her aphasia was still instantly recognizable in adulthood by the way she talked. Videoand audiotaped recordings were rated according to several psycholinguistic variables, among which mean length of utterance (MLU). Pragmatic aspects of communication such as presupposition and topic-maintenance were also assessed. Evaluations in the acute phase and at follow-up did not show any significant difference between MLU measurements. The patient produced long utterances and spoke fluently. A number of language characteristics were present to a varying degree both in the acute phase and at follow-up: semantic verbal paraphasias (including superordinate substitutions), passe-partout words, circumlocutions, conduites d'approche, dyssyntaxis, false starts, inappropriate

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use of anaphors, and empty speech. At follow-up, a quantitative improvement of the patient's verbal output was observed. The follow-up did not reveal any new language features or anomalies. The patient's verbal output was still recognizable at 12-year follow-up because of a combination of factors: (a) persisting anaphoric difficulties which, along with lack of cohesion, explicit information and accuracy, resulted in inadequate pragmatic interaction and disjointed and fragmented discourse; (b) the presence of comparable paralinguistic aspects of communication (such as intelligibility, voice quality, prosody, and rate of speaking) in the acute phase of aphasia and at follow-up; and (c) the presence of mild but lasting word-finding difficulties with similar strategic adaptations at follow-up. Although MLU measurements did not differ significantly between assessments in the acute phase and at followup, they did not add much value to the characterization - hence, the recognition - of the patient's verbal output. Keywords: acquired aphasia, children, tumor, recovery

INTRODUCTION Long-term follow-up studies of children with early (i.e., before 6 months of age) left-sided focal brain injury are numerous and tend to demonstrate that, if they do not develop epilepsy, these children usually acquire language skills that are within the normal range, that is, they are not aphasic (e.g., Woods and Carey, 1979; Bates et al, 1997, 2001; Nass, 1997; Reilly et al, 1998; Bates, 1999a, b). In contrast, children with acquired aphasia - i.e., a childhood language disorder resulting from a cerebral lesion sustained after onset of language acquisition - have a less favorable prognosis than children with early brain lesions (Paquier and Van Dongen, 1996, 1998). Most longitudinal follow-up studies, which mainly focus on school-aged children, emphasize the deleterious effects of acquired childhood aphasia (ACA) on school achievement even in children who clinically recovered from aphasia (e.g., Alajouanine and Lhermitte, 1965; Hecaen, 1983; Cooper and Flowers, 1987; Cranberg et al, 1987; Klein et al, 1992; Martins and Ferro, 1992; Pitchford et al, 1997; Pitchford, 2000). However, little is known about the long-term outcome of ACA in adult age, with the likely exception of language outcome associated with Landau-Kleffner syndrome, i.e., acquired epileptic aphasia (Mantovani and Landau, 1980; Deonna et al, 1989; Van Dongen et al, 1989). Woods and Teuber (1978) reported on a patient who at the age of 5 acquired jargon aphasia as a result of stroke. The patient was seen again when he was 21. At follow-up he was not clinically aphasic. Nevertheless, he displayed some difficulties in reading aloud, in naming to category and from definition, in spelling, and in comprehending spelled words. He performed normally on the Token Test. Watamori et al. (1990) described the long-term outcome of linguistic and nonlinguistic functions in three adults with ACA. This study revealed that, despite the early restoration of functional communication ability, language recovery was not complete, and syntactic processing difficulties, limitation of lexicalsemantic abilities, as well as written language processing difficulties were still present in adulthood. When compared to controls matched for lexical-semantic ability, all three patients showed poorer performance on spontaneous speech measures such as production of complex syntactic structures and efficiency of production. Their case histories suggested that the influence of residual linguistic impairments was not restricted to academic achievement but also had an effect on the subjects' personalities and social development. Watamori et al's

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(1990) findings also revealed that child-onset aphasics used similar strategies for functional compensation as seen in recovered adult aphasics. We had the opportunity of assessing a previously reported girl with ACA (Paquier and Van Dongen, 1991, case 2) both in the acute phase (at the age of 9 years 3 months) and at 12year follow-up. Remarkably, after all these years, the patient could still blindly be recognized as aphasic just by the way she expressed herself, even by naive listeners who never met her and who only had the opportunity of listening to recordings of her spontaneous language. This study was thus geared to analyze the patient's spontaneous verbal output in the acute phase and 10/4 and 12 years post-onset, to determine why she was still instantly recognizable in adulthood. Several linguistic and nonlinguistic variables as well as pragmatic aspects of communication were evaluated.

PATIENT AND METHODS Patient At the age of 9 years and 3 months, this right-handed, Dutch-speaking girl was admitted because of lasting complaints of headache, nausea, and fatigue. Her psychomotor and language development had been normal, and she was attending normal primary school. Upon admission, the girl was conscious and well-oriented. No aphasic signs were present. A clinical neurological examination revealed papilledema, a right homonymous hemianopia, and a right-sided hypoesthesia. An electroencephalogram showed left temporal focal abnormalities. A space-occupying neoplastic lesion in the left temporoparietal area was revealed by CT scan and confirmed by cerebral angiography. The tumor - a ganglioneuroma as revealed by the neuropathological examination - was partially resected fifteen days after admission. After surgery the patient developed grand-mal seizures and, later on, right-sided focal insults. She was aphasic and slightly hemiparetic. Her general conditions improved steadily, and she was discharged one month after admission. However, she still had epilepsy, and presented with a persisting right homonymous hemianopia. At follow-up, two years post-onset the girl demonstrated mild aphasic disturbances which increased during and after epileptic seizures, thus resulting in a transitory exacerbation of aphasia, with different clinical manifestations, including speech arrests, depending on the location of the epileptic focus. Nine years post-onset, the patient was started on chemotherapy because of increasing vision problems. They were believed to be due to residual tumor growth, as later revealed by MRI. One year later she was irradiated as vision further deteriorated despite chemotherapy. Since then her sight has remained stable, and the recurring epileptic insults which used to produce a transient aggravation of her language impairment disappeared. The patient has been seizure-free ever since but she is still under anti-epileptic therapy because she fears new fits. Immediately after the post-operative time, the girl presented with fluent aphasia which in the early phase was predominantly characterized by logorrheic utterances, mild auditory comprehension and repetition difficulties, and by lasting word-finding difficulties with conduites d'approche1. She was spontaneous and cheerful during the post-operative assessments, as well as lO'A and 12 years post-onset. Her spontaneity was never affected by 1 For detailed information regarding the patient's neurological and aphasiological condition in the acute phase and 2 years post-onset, see Paquier and Van Dongen (1991).

184 Neurogenic Language disorders in Children

the language disorder. Nevertheless, she could not resume normal education after discharge from hospital, and went to a school for visually disabled children. The teachers reported learning and memory difficulties which eventually resulted in poor academic achievements. Despite these difficulties she succeeded in completing secondary school, and she is currently working in a day nursery. Twelve years post-onset, the patient complained of impaired vision, memory difficulties, and attentional problems. She did not openly mention the presence of language difficulties, although she was presenting with a residual anomic aphasia. Her spontaneous language was fluent and sporadically empty, with some verbal paraphasias and circumlocutions. Word-finding difficulties, however, were most conspicuous during object naming tasks. Repetition of spoken language was only mildly disturbed by mnestic difficulties which resulted in occasional word omissions or word order errors in longer sentences. The hemianopia had remained unchanged. Language sample. Spontaneous language was elicited in a free interview situation by means of standard open-ended questions concerning the patient's interests (holidays, school or professional activities, pets, etc.). The interviewer's task was to prompt the patient or to initiate conversation. This was the conversational discourse. In addition, samples of narrative discourse were obtained by asking the patient to tell the well-known Little Red Riding Hood's tale. Both the conversational and the narrative discourse were video- or audiotaped. Three language samples were obtained: sample LI (229 utterances; 19 min 27 sec) was a videotaped recording made in the acute phase (approximately 6 days after surgery), samples L2 (177 utterances; 14 min 23 sec) and L3 (114 utterances; 12 min 36 sec) were audiotaped recordings at lO'A and 12 years, respectively. The patient was alert and co-operative during the recordings. Transcription. The recordings of the conversational and narrative discourses were orthographically transcribed by one of the examiners (VVM) according to the TOAST procedure (Taal-Onderzoek via Analyse van Spontane Taal - Language Assessment through Analysis of Spontaneous Language) (Moerman-Coetsier and Van Besien, 1987). Neologisms and unintelligible productions were transcribed using the International Phonetic Alphabet. One week later, the language samples were completely re-listened to and, where necessary, corrections were made to the first transcripts. Another week later, if necessary, final adaptations were made after listening again to transcripts. Then, the patient's and interviewer's turns were segmented into utterances, an utterance being considered as "a unity of expression that utters a thought, a feeling, an intention, etc." (Moerman-Coetsier and Van Besien, 1987, p. 45). Criteria for segmentation were changes in intonation and the occurrence of pauses, as determined by the TOAST procedure.

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Reliability of transcription. An independent and naive judge, who by reason of her profession was familiar with orthographic transcription, was asked to transcribe five minutes of spontaneous language selected at random from each of the three language samples. Interjudge agreement was then determined by comparing her transcripts with the corresponding three original transcripts, and calculated according to a frequency ratio in which the number of similarly transcribed items was divided by the total number of transcribed items and multiplied by 100. The mean inter-judge percent agreement was 9 1 % (94% for LI, 91% for L2, and 88% for L3). These percentages are relatively high, which indicates a fair inter-judge agreement. Analysis of spontaneous language. Mean length of utterance (MLU) was rated according to the TOAST procedure. As the easiest way to measure MLU, the MLU length expressed in words (MLUW) was considered (Beheydt, 1983). MLUW and MLU of the three longest utterances expressed in words (MLU3) were calculated according to Wagenaar et al.'s (1975) psycholinguistic analysis of spontaneous language in adult aphasics2. We also calculated the length expressed in morphemes (MLUm) as several studies indicate that MLUm can be considered a measure of morphosyntactic development, the length of the utterances also depending on the acquisition level of morphology, at least in young children (Brown, 1973; Bloom and Lahey, 1978; Moerman-Coetsier and Van Besien, 1987). There is a high correlation between MLU m and MLUW, especially in younger children (Moerman-Coetsier and Van Besien, 1987). Other variables of study included the presence of neologisms, circumlocutions, conduites d'approche, dyssyntaxis, hedging, false starts, and anaphors. hi line with Kerschensteiner et al. (1972), we also rated a number of variables relevant for the analysis of adult spontaneous aphasic language, which have subsequently been rated in children with ACA too (Van Dongen et al, 2001): rate of speaking, prosody, effort, articulation, perseveration, word choice (such as passe-partout words), pauses, verbal paraphasias, and literal paraphasias (for a description, see the Appendix). Application of TOAST procedure to language samples. The work samples used to compute MLU were defined following the TOAST procedure. According to the assessment manual, first a sample consisting of at least 110 usable patient's utterances - 55 coming from conversational discourse and 55 from narrative discourse - has to be selected from the complete language samples. Then, the sample is reduced to 100 usable utterances (2 x 50, viz. the 6th up to the 55 th utterance included) by omitting the first five utterances from each discourse (because utterances tend to be shorter at the beginning of verbal interaction). As our recordings did not allow us to apply this procedure literally, we changed it as follows: three work samples were chosen to contain the same number of usable utterances as those present in the smallest language sample (in our case, 101 usable utterances in L3) with a minimum of 100 utterances. Consequently, MLU was calculated as follows: MLU m = 2 morphemes / 101 MLUW = S w o r d s / 1 0 1 MLU3 = Z words of 3 longest utterances / 3 2 Although direct comparisons between data collected in aphasic adults and children with this method are not possible for methodological reasons, we would like to point out that the computation of MLUW is identical in TOAST and Wagenaar et a/.'s (1975) study.

186 Neurogenic Language disorders in Children The remaining (non-TOAST) variables were rated on the complete language samples.

RESULTS To ascertain the representativeness of the work samples and, thus, the validity of the MLU analysis we checked the distribution of the utterance lengths throughout the work samples according to the TOAST procedure. Language samples that are representative of the patient's overall verbal output, indeed, show a normal distribution of utterance lengths (MoermanCoetsier and Van Besien, 1987). Kolmogorov-Smirnov test results showed that utterance lengths are normally distributed throughout the three language samples (p > 0.10) (Figure 1); a reliable interpretation of MLU is thus possible. Table 1 displays the different MLU values for the three work samples. Table 2 shows the non-TOAST spontaneous language characteristics for the three language samples. A Bartlett's test for homogeneity of variances did not find any significant difference in standard deviations of MLU m across the three work samples (B = 0.27; d.f. = 2; p > 0.05). A one-way analysis of variance (ANOVA) indicated that there was no significant difference across the three MLUm (VR = 2.86; d.f. = 2,300; p > 0.05) (Table 1). MLUW remained stable across the three work samples, whereas MLU3 slightly increased (Table 1).

Table I — MLU values computed for the three work samples MLU In morphemes (MLUm) In words (MLUW) MLUwof the 3 longest utterances (MLU3) SDofMLU,,,

LI 9.6 8 16 4.7

L2 11.0 9 19 4.8

L3 9.6 8 18 4.6

Note: MLU = mean length of utterance; L = language sample; SD = standard deviation Regarding the remaining (non-TOAST) language characteristics, Table 2 shows that paraphasias were observed at onset of aphasia but they decreased dramatically in the course of follow-up. Twelve years post-onset only two semantic paraphasias were noted. Neologisms were not observed in the acute phase or at follow-up. In the acute phase, passe-partout words mainly concerned the class of verbs and, to a lesser degree, that of substantives; 12 years later they were sporadically recorded as empty substantives. Circumlocutions and conduites d'approche only made up a small proportion of all utterances in the acute phase and at followup. However, the percentage of false starts against the total number of utterances was markedly more important both in the acute phase and 12 years post-onset. In the acute phase and at follow-up, the patient experienced mild syntactic difficulties which sporadically manifested themselves as dyssyntaxis characterized by a wrong word sequence within sentences, concord errors between subject and verb form, a wrong article use, a wrong verb tense use, erroneous application of the double negation rule, and confusions between substantives and nominal forms.

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The rate of speaking increased from 108 words per minute in the acute phase to 129 and 121 words per minute lO'A and 12 years post-onset. Based on a perceptual analysis of speech characteristics, no anomalies of prosody, effort, articulation, and pauses were observed in the acute phase or at follow-up.

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Neurogenic Language disorders in Children

Figure I - Distribution of utterance lengths expressed in morphemes.

In the acute phase literal and verbal perseverations were observed, as well as a small number of word group perseverations. At follow-up 12 years post-onset, perseverations had almost completely disappeared (except for one verbal perseveration).

Table 2 — Non-TOAST spontaneous language characteristics rated throughout the three language samples (percentages are calculated against total number of utterances)

Speech and language variables

LI

L2

L3

Verbal paraphasias:

Morphemic

0.9%

—

—

Semantic

1.3% 1.3%

2.8%

1.8%

—

—

Unrelated Total Literal paraphasias Neologisms

3.5%

2.8%

1.8%

2.6%

—

—

—

—

—

Circumlocutions

3.1%

—

1.8%

Conduites d'approche

1.7%

—

0.9%

Dyssyntaxis

+

+

+

Hedging

+

+

—

15.7%

9.0%

10.5%

Erroneous use

2.6%

4.5%

3.5%

Indefinite

4.8%

2.8%

2.6%

Omission

2.2%

0.9%

Total

9.6%

1.1% 8.4%

108

129

121

False starts Anaphors:

Rate of speaking (wpm)

7.0%

Prosody

N

N

N

Effort

—

—

—

Articulation Perseverations:

Word choice:

N

N

N

Literal

5.2%

0.6%

—

Verbal

3.1%

3.4%

0.9%

Word group

0.9%

0.6%

—

Total

9.2%

4.6% +

0.9%

+

Empty Cliches Passe-partout words

Pauses

+

—

—

—

8.7%

—

1.8%

N

N

N

Aphasic spontaneous speech at 12-year follow-up

189

Note: L = language sample; wpm = words per minute; N = normal; + = present; — = absent Finally, especially in the acute phase but also at follow-up the patient experienced difficulties with anaphors (Table 2). Anaphoric difficulties were classified as indefinite anaphors (anaphors without a referent), erroneous use of anaphors, and omission of anaphors. During the acute phase, indefinite anaphors occurred more often than omissions and erroneous uses of anaphors (Table 2). At follow-up, the number of indefinite anaphors and anaphoric omissions decreased, while erroneous use of anaphors slightly increased. To summarize, evaluations in the acute phase and at follow-up did not show any significant difference across MLUm. The patient used long utterances and spoke fluently. The analysis further revealed the presence of a varying number of language characteristics both in the acute phase and at follow-up, including semantic verbal paraphasias (including superordinate substitutions), passe-partout words, circumlocutions, conduites d'approche, dyssyntaxis, false starts, inappropriate use of anaphors, and empty speech. At follow-up, a quantitative improvement in the patient's verbal output was observed but no new language features or anomalies.

DISCUSSION Methods for the analysis of spontaneous language in aphasic subjects are scarce in the Dutchspeaking area, especially with regard to a pediatric population (Evy Visch-Brink, personal communication). Moreover, no methods have been developed which allow similar analyses and reliable comparisons of spontaneous language in both child and adult aphasic populations. With these practical constraints and the unavailability of comparable norms in mind, we chose the TOAST procedure (Moerman-Coetsier and Van Besien, 1987) to analyze aspects of our Dutch-speaking patient's language that were related to utterance length, as a number of linguistic variables assessed by TOAST (e.g., MLU) are universally recognized in language research (Wagenaar et ai, 1975; Vermeulen et al, 1989; Eisenberg et ai, 2001; Bol, 2003). However, a major methodological limitation due to this choice is the impossibility to judge the normality or abnormality of our patient's performance levels on the assessed TOAST variables, as norms corresponding to her chronological age are not available. Taking these restrictions into account, we considered the TOAST analysis as true intellectual exercise aimed at collecting potentially interesting information that might add value to the analysis of the other linguistic and non-linguistic variables. Our patient's MLUm in the acute phase (9.55) is exceeding the mean MLU m of the oldest norm group, i.e., 48-54 months (mean 5.25, s.d. 0.58), thus preventing any firm interpretation as to the normality of her MLU m . It can only be stated that her MLU m in the acute phase is comparable to that at follow-up, which might suggest that her expressive morphosyntactic ability did not significantly change since onset of aphasia. Whether this invariability reflects an acquired aphasic morphosyntactic disorder persisting in the long-term or a normal morphosyntactic acquisition level already present in the acute stage is perhaps less a matter of speculation than it may appear at first sight. Indeed, one may assume that the comparable MLUm values indicate an age-adequate acquisition level of morphology already present at onset of aphasia for at least three reasons: (a) unlike the early stages of language acquisition

190 Neurogenic Language disorders in Children

during which any morphosyntactic progress causes utterance lengthening, an increase in structural complexity may cause no change in utterance length in later acquisition stages (Feyereisen et al., 1991); (b) the active development of syntax and morphology is generally complete between the age of VA and 814 (Gillis and Schaerlaekens, 2000), whereas our patient became aphasic beyond that period; and (c) the overall clinical course of our patient's aphasic language disorder evolved quite favorably over the years, making the existence of a specific, chronic, and stable deficit of morphosyntaxis since onset of aphasia most unlikely. When considering the other language variables of study, we observed that word-finding difficulties were prominent in the acute phase, and more subtle at follow-up. At both times they appeared to be the cause of false starts, repetitions, conduites d'approche (the active search for the right word), circumlocutions, verbal and literal paraphasias, and passe-partout words. Semantic verbal paraphasias also occurred at follow-up. The use of circumlocutions, being object or function descriptions of words, delayed the transfer of information. Wordfinding difficulties also gave rise to semantically empty spontaneous language. At follow-up, sporadic passages of empty speech were caused by the use of vague or generic substantives, passe-partout words (e.g., thing, thingummy, stuff), and all-purpose verbs (e.g., to do) as substitutes for information-loaded words. The use of circumlocutions and passe-partout words might not only be the mere manifestation of word-finding difficulties, but also an adaptive strategy to compensate for these difficulties. Interestingly enough, both in the acute phase and at follow-up the patient gave evidence of metalinguistic awareness, as she often self-corrected verbal paraphasias even before pronouncing the word completely, or interrupted her utterances to re-edit them (so-called false starts). The use of hedges also reflected the patient's metalinguistic awareness, as in doing so she admitted not being sure about certain statements of hers. It is clear that the patient was not anosognosic. Especially in the acute phase but also at follow-up, at times the patient's message was hardly intelligible owing to the lack of explicit and accurate information. For instance, she frequently used pronouns without antecedents instead of substantives. The lack of accuracy was also evident in the disordered cohesion between co-referring words. There is cohesion between sentences when two words (e.g., a pronoun and its antecedent) co-refer to the same entity. The most frequently studied types of cohesion are pronominal and lexical co-reference. Lexical co-reference occurs when the definite article 'the' precedes a noun to signal that this noun refers to a previously mentioned entity (Davis et al, 1997). Pronominal co-reference occurs when a pronoun such as a personal or possessive pronoun refers to an antecedent. It appears that the patient only had difficulties with pronominal co-reference. In the acute phase, incomplete cohesion resulted from the use of indefinite anaphors (the information referred to by the anaphors was not always provided by the patient), whereas other anaphors were omitted or erroneously used. Again, at follow-up we observed this inadequate use of anaphors, which resulted in an inappropriate pragmatic interaction as the global meaning of the patient's message could not sufficiently be inferred from the context. Anaphoric errors and omissions of relevant information often resulted in a disjointed and fragmented discourse. A few pragmatic aspects of her communicative behavior were also manifest at follow-up. The patient behaved as if she assumed the listener had sufficient foreknowledge to understand the message (presupposition), and omitted significant parts of the information. She did not always succeeded in conveying the content and purpose of her message. A relation between this pragmatic aspect of communication and her anaphoric difficulties seems plausible.

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191

The paralinguistic aspects of the patient's utterances (the so-called suprasegmental characteristics of language: intelligibility, loudness, voice quality, prosody, fluency, and rate of speaking) were always adequate, both in the acute stage and at follow-up. From a video recording made in the acute stage we were able to analyze the nonverbal aspects of the patient's communication such as posture, gestures, eye contact, and facial expressions. All these facets were adequate, and they still were 12 years post-onset. Both in the acute phase and at follow-up, the patient was aware of the social rules of conversation as she adequately waited for her turn without interrupting the interlocutor. When she did not understand a question, she asked for clarification. After having discussed our patient's aphasiological features in the acute stage and at follow-up, we would like to address some methodological issues that are of importance in a clinical setting. The lack of significant difference in MLU values between the first assessment and follow-ups raises some questions about the clinical utility of this measure in aphasiological practice. Indeed, MLU did not differ significantly between both assessment times, although our patient showed an indisputable clinical recovery, even if she still presented with some residual anomic aphasia in the long term. Consequently, it is questionable whether MLU measures are capable of objectivizing such a favorable evolution. Wagenaar et al. (1975) demonstrated that MLU measures are helpful in differentiating nonfluent from fluent adult aphasics, nonfluent patients producing utterances shorter than 6.25 words and fluent patients having utterances longer than 7.33 words. In other words, fluent aphasics are capable of producing utterances, the length of which equals that of normal speakers, even if their sentences are semantically empty and morphosyntactically inadequate. Consequently, it is not surprising that within the group of fluent aphasics, MLU measurements performed at two different points in time in the same patient do not show significant differences despite a significant recovery, as these measurements are not indicative of the intrinsic characteristics of semantic adequacy or morphosyntactic complexity and exactness. MLU measures are not able to capture positive signs such as paraphasias and dyssyntaxis. As a matter of fact, any improvement in structural complexity or semantic adequacy may cause no change in utterance length at all once the early stages of language acquisition are completed (Feyereisen et al, 1991). Consequently, MLU measures reflect nothing but utterance length, which is known to be normal in fluent aphasics (Benson and Ardila, 1996). Regarding our patient, similar MLU values in the acute stage and 12 years later only reveal that the mean length of her utterances remained comparable but they are not indicative of the nature of the underlying defective linguistic mechanisms or the qualitative improvements in content. As a consequence, it seems that in our patient MLU measurements would only have contributed to the characterization of her aphasic deficit if a change in utterance length (i.e., a quantitative change) would have occurred between the two assessments. The clinical utility of MLU measurements in aphasic patients who are fluent from the very beginning of their aphasia appears, thus, to be quite limited.

CONCLUSION Our patient presented with a fluent type of aphasia since the onset of her language problems (Paquier and Van Dongen, 1991). In a psycholinguistic study on spontaneous language in adult aphasics, Wagenaar et al. (1975) concluded that patients can be classified as fluent or nonfluent on the basis of two variables, viz. MLU and rate of speaking. They found that fluent

192

Neurogenic Language disorders in Children

patients had utterances longer than 7.33 words and that they uttered more than 540 words in 6 minutes (90 wpm). Although their analysis does not apply to a pediatric population of aphasic subjects, and, consequently, does not allow reliable comparisons between adults and children, we would yet like to remark that already in the acute phase of aphasia (and, later on, during follow-up assessments) our patient's performance levels on MLUW and speech rate exceeded both cut-off values proposed by Wagenaar et al. (1975). No anomalies of prosody, effort, articulation, and pauses were observed. Positive signs (Van Hout et al, 1985) such as dyssyntaxis and paraphasias were noted at the onset of aphasia. The patient's verbal output features, which are specific to fluent aphasia, were confirmed in a recent study on conversational speech fluency in the acute phase of ACA (Van Dongen et al, 2001). The patient's clinical recovery is indisputable, yet not complete. Twelve years post-onset she presented with residual anomic aphasia which was most evident during naming tasks. In our opinion, the patient's verbal output was still recognizable as aphasic 12 years postonset because of a combination of factors. As most salient feature we would suggest the anaphoric difficulties and the lack of explicit information and semantic accuracy which, along with a disturbed cohesion between discourse elements, led to an inadequate pragmatic interaction and a disjointed and fragmented discourse. In addition, paralinguistic aspects of the patient's verbal output such as intelligibility, voice quality, prosody, and rate of speaking did not differ subjectively across the three recorded language samples. Also, the patient still displayed word-finding difficulties with similar strategic adaptations at follow-up. As MLU measures are not capable of capturing any relevant changes in morphosyntactic complexity and exactness or in semantic adequacy, we do not feel that the similar MLU values in the acute stage and 12 years later add much value to the recognition of our patient's verbal output, except perhaps that they demonstrated that her utterances did not substantially increase or decrease in length over time. As a consequence, we believe that our findings shed but a subdued light on the clinical utility of MLU measures in aphasiological practice, at least in fluent aphasic subjects. Finally, the present study confirms that subtle but lasting language difficulties can persist as long-term outcome of ACA. In cases of tumor-related etiology, the course and outcome of aphasia usually parallel the growth of the tumor, except when aphasia is caused by acute bleeding or sudden cystic enlargement (Van Hout, 1990). Surgical resection of the tumor can cause aphasia in a previously non-aphasic subject, and post-surgical epileptic disorders can impair the recovery process by causing transient aggravations of the language impairment.

ACKNOWLEDGEMENTS The authors are indebted to John van Borsel, PhD, Speech and Hearing Rehabilitation Center, University of Ghent, for co-supervising the second author's MA dissertation (Van Maldeghem, 1999; Van Maldeghem et al, 2001).

APPENDIX Description of the variables used in the analysis of spontaneous language samples (MonradKxohn, 1947; Benson, 1967; Kerschensteiner et al., 1972; Benson and Ardila, 1996).

Aphasic spontaneous speech at 12-year follow-up

193

Anaphors

A word that has an antecedent occurring before or after the word to which it refers. Words that can be used as anaphors are definite articles, relative pronouns, and possessive pronouns. Aphasics often use anaphors for which there is no referent (indefinite anaphors). For instance, a patient may say "I saw it" but the key referent ('book', 'car', 'accident', etc) has not been mentioned; in this example, 'it' is an indefinite anaphor. Articulation The attributes of articulation and phonation which are necessary to produce readily intelligible word speech patterns. Circumlocution A substitution of object description or instrumental function for a word. Cliche An accepted and stereotyped utterance which is little specific and carries different meanings, and can thus be used in different situations. Cliches are used as fillers, and as such they are redundant and empty. Conduite d 'approche A patient's repeated and conscious attempts to correct an erroneous utterance and to pronounce a word correctly. Dysssyntaxis Grammatical deviation characterized by a verbal output that violates the normative rales of morphosyntactic convention. Dyssyntaxis may result from: (a) erroneous selection of grammatical elements; (b) overuse of grammatical elements (particularly connectors) associated with a decrease of nouns; and (c) lack of defining limits in the sentences, correlated with an excessive verbal output. Effort Two patterns are recognized, one with marked difficulty in starting to speak, and a second in which the patient readily begins a word or a short phrase but becomes tied up and labored in attempting to continue, hi the former group, the evidence of effort is often dramatic with facial grimacing, puffing of the chest, and body movements. Empty speech A fluent verbal output that conveys very little explicit information because of the lack of information-loaded words as opposed to the use of a number of relational words, vague and generic adjectives and adverbs. False start Evidence of metalinguistic awareness, characterized by a patient's interruptions, alterations or adjustments of his/her production in order to re-edit it. Hedging

194 Neurogenic Language disorders in Children An expression of uncertainty (derived from the verb 'to hedge') such as: "I think", "I guess", "according to me", etc. The difference between a 'hedge' and a 'cliche' is that the latter does not necessarily carry a connotation of uncertainty. Literal (or phonological) paraphasia An incorrectly produced word caused by omissions, additions, displacements, or substitutions of phonemes within the desired word (e.g., 'nitroben' for "nitrogen", 'porlity' for "policy"). Neologism A meaningless phonological form resulting from the combination of appropriate and reproducible phonemes carrying no meaning in the speaker's vocabulary. The listener is not able to identify the target word. Passe-partout word Vague or generic, all-purpose word. Pauses The hesitations occurring within a phrase; pauses are not the intervals in the flow of speech which interrupt phrases. Pauses may be due to: great effort to produce words resulting in breaks preceding and following phonation; articulation difficulties as the patient struggles to pronounce or goes back to correct improperly produced syllables; paraphasic substitutions as the patient attempts to correct or decides to continue despite the error; word-finding difficulties as the patient finds he is unable to produce the word necessary to continue. Perseveration The needless repetition of a phoneme, syllable, word or even a short phrase. Prosody Correct placing of stress upon syllables and words within the sentence (including prolongations); natural rhythm, pauses and rate of speaking; natural shifting of pitch from syllable to syllable and from word to word, some being pronounced on a higher note, some on a lower note, varying from sentence to sentence (gradual or abrupt rising and falling of the pitch). Rate of speaking The number of words uttered in one minute (wpm); the normal rate being more than 90 wpm. Verbal paraphasia The erroneous use of a word belonging to an inventory of the language in place of another word that also belongs to one of the language inventories. Morphemic verbal paraphasias refer to inadequate words that have been assembled by using morphemes belonging to the language inventory (e.g., "winterly"). Semantic verbal paraphasias designate aphasic transformations in which the desired and the substituted words are close in meaning (e.g., fork-knife). Morphological verbal paraphasias are transformations in which the substituting word and the substituted word are similar in form but not in meaning (e.g., house-mouse). Unrelated verbal paraphasias are word substitutions that, in the given context, are neither phonologically nor

Aphasic spontaneous speech at 12-year follow-up

195

semantically related to the word that seems to be required (e.g., "It costs a fortune to fly first carbuncle"). Word choice The division into predominantly substantive word use (classic telegraphic speech or one-word sentences, i.e. the use of nouns but also action verbs and significant modifiers expressing an entire idea) or predominantly relational word use (empty speech, i.e. the use of many relational words, adjectives, adverbs carrying very little information because of the lack of specific substantive words). The use of many relational words, cliches and empty speech has been shown to be peculiar of fluent aphasia.

REFERENCES Alajouanine, T. and F. Lhermitte (1965). Acquired aphasia in children. Brain, 88, 653-662. Bates, E. (1999a). Plasticity, localization, and language development. In: The Changing Nervous System: Neurobehavioral Consequences of Early Brain Disorders (S.H. Broman and J. M. Fletcher, eds.), pp. 214-253. Oxford University Press, New York. Bates, E. (1999b). Language and the infant brain. JComm Disord, 32, 195-205. Bates, E., J. Reilly, B. Wulfeck, N. Dronkers, M. Opie, J. Fenson, S. Kriz, R. Jeffries, L. Miller and K. Herbst (2001). Differential effects of unilateral lesions on language production in children and adults. Brain Lang, 79, 223-265. Bates, E., D. Thai, D. Trauner, J. Fenson, D. Aram, J. Eisele and R. Nass (1997). From first words to grammar in children with focal brain injury. Dev Neuropsychol, 13, 275-343. Beheydt, L. (1983). Kindertaalonderzoek: Een Methodologisch Handboek. Cabay, Louvainla-Neuve. Benson, D. F. (1967). Fluency in aphasia: correlation with radioactive scan localization. Cortex, 3, 373-394. Benson, D. F. and A. Ardila (1996). Aphasia: A Clinical Perspective. Oxford University Press, New York. Bloom, L. and M. Lahey (1978). Language Development and Language Disorders. Wiley, New York. Bol, G. W. (2003). MLU-matching and the production of morphosyntax in Dutch children with specific language impairment. In: Language Competence across Populations: Toward a Definition of Specific Language Impairment (Y. Levy and J. Schaeffer, eds.), pp. 259-271. Lawrence Erlbaum Associates, Mahwah. Brown, R. (1973). A First Language. Harvard University Press, Cambridge. Cooper, J.A. and C. R. Flowers (1987). Children with a history of acquired aphasia: residual language and academic impairments. J Speech Hear Disord, 52, 251-262. Cranberg, L. D., C. M. Filley, E. J. Hart and M. P. Alexander (1987). Acquired aphasia in childhood: clinical and CT investigations. Neurology, 37, 1165-1172. Davis, G. A., Th. M. O'Neil-Pirozzi and M. Coon (1997). Referential cohesion and logical coherence of narration after right hemisphere stroke. Brain Lang, 56, 183-210. Deonna, T., C. Peter and A. L. Ziegler (1989). Adult follow-up of the acquired aphasiaepilepsy syndrome in childhood: report of seven cases. Neuropediatrics, 20, 132-138. Eisenberg, S.L., T. Fersko and C. Lundgren (2001). The use of MLU for identifying language impairment in preschool children: a review. Am J Speech Lang Pathol, 10, 323-342.

196 Neurogenic Language disorders in Children Feyereisen, P., A. Pillon and M. P. De Partz (1991). On the measures of fluency in the assessment of spontaneous speech production by aphasic subjects. Aphasiology, 5, 121. Gilles, S. and A. M. Schaerlaekens (2000). Kindertaalverwerving: Een Handboek voor het Nederlands. Nijhoff, Groningen. Hecaen, H. (1983). Acquired aphasia in children: revisited. Neuropsychologia, 21, 581-587. Kerschensteiner, M., K. Poeck and E. Brunner (1972). The fluency-non fluency dimension in the classification of aphasic speech. Cortex, 8, 233-247. Klein, S.K., D. Masur, K. Farber, S. Shinnar and I. Rapin (1992). Fluent aphasia in children: definition and natural history. J Child Neurol, 7, 50-59. Mantovani, J. F. and W. M. Landau (1980). Acquired aphasia with convulsive disorder: course and prognosis. Neurology, 30, 524-529. Martins, I. P. and J. Ferro (1992). Recovery of acquired aphasia in children. Aphasiology, 6, 431-438. Moerman-Coetsier, L. and F. Van Besien, (1987). Toast - TaalOnderzoek via Analyse van Spontane Taal. Acco, Amersfoort/Leuven. Monrad-Krohn, G. H. (1947). Dysprosody or altered melody of language. Brain, 70, 405-415. Nass, R. (1997). Language development in children with congenital strokes. Semin Pediatr Neurol, 4, 109-116. Paquier, P. and H. R. Van Dongen (1991). Two contrasting cases of fluent aphasia in children. Aphasiology, 5, 235-245. Paquier, P. and H. R. Van Dongen (1996). Review of research on the clinical presentation of acquired childhood aphasia. Acta Neurol Scand, 93, 428-436. Paquier, P. and H. R. Van Dongen (1998). Is acquired childhood aphasia atypical? In: Aphasia in Atypical Populations (P. Coppens, Y. Lebrun and A. Basso, eds.), pp. 67115). Lawrence Erlbaum Associates, Mahwah. Pitchford, N. J. (2000). Spoken language correlates of reading impairments acquired in childhood. Brain Lang, 72, 129-149. Pitchford, N. J., E. Funnell, A. W. Ellis, S. H. Green and S. Chapman (1997). Recovery of spoken language processing in a 6-year-old child following a left hemisphere stroke: a longitudinal study. Aphasiology, 11, 83-102. Reilly, J. S., E. A. Bates and V. A. Marchman (1998). Narrative discourse in children with early focal brain injury. Brain Lang, 61, 335-375. Van Dongen, H. R., J. Meulstee, M. Blauw-Van Mourik and F. Van Harskamp (1989). Landau-Kleffner syndrome: a case study with a 14-year follow-up. Eur Neurol, 29, 109-114. Van Dongen, H. R., P. Paquier, W. L. Creten, J. Van Borsel and C. Catsman-Berrevoets (2001). Clinical evaluation of conversational speech fluency in the acute phase of acquired childhood aphasia: does a fluency/nonfluency dichotomy exist? J Child Neurol, 16, 345-351. Van Hout, A. (1990). Acquired Aphasia in Childhood. Its Impact on the Conception of Functional Maturation of the Brain and its Implication for Pediatric Neuropsychology. Unpublished doctoral thesis. Catholic University of Louvain (UCL): School of Medicine. Van Hout, A., P. Evrard and G. Lyon. (1985). On the positive semiology of acquired aphasia in children. Dev Med Child Neurol, 27, 231-241.

Aphasic spontaneous speech at 12-year follow-up Van Maideghem, V. (1999). Spontane Taalanalyse bij Verworven Kinderafasie na Resectie van een Temporo-Parietale Tumor: een Gevalsstudie met een 12 Jaar Follow-up. Unpublished master's dissertation. University of Ghent: School of Medicine. Van Maldeghem, V., P. Paquier, H. R. Van Dongen and J. Van Borsel (2001). Analyse van de spontane taal bij verworven kinderafasie: een gevalsstudie met een 12 jaar follow-up. Stem-, Spraak- en Taalpathologie, 10, 49-70. Vermeulen, J., R. Bastiaanse and B. Van Wageningen (1989). Spontaneous speech in aphasia: a correlational study. Brain Lang, 36, 252-274. Wagenaar, E., C. Snow and R. Prins. (1975). Spontaneous speech of aphasic patients: a psycholinguistic analysis. Brain Lang, 2, 281-303. Watamori, T. S., S. Sasanuma and S. Ueda. (1990). Recovery and plasticity in child-onset aphasics: ultimate outcome at adulthood. Aphasiology, 4, 9-30. Woods, B. T. and S. Carey (1979). Language deficits after apparent clinical recovery from childhood aphasia. Ann Neurol, 6, 405-409. Woods, B.T. and H. L. Teuber (1978). Changing patterns of childhood aphasia. Ann Neurol, 3, 273-280.

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Long-term language recovery in an aphasic Czech child

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11

RECOVERY FROM APHASIA AFTER POLYTRAUMA IN A CZECH CHILD: WHAT I S LOST AND WHAT IS LEFT Helena Leheckovd University of Helsinki, Finland

Abstract—A case study is presented of a Czech-speaking child with acquired aphasia. The patient (a right-handed female) was 11 years old when she sustained multiple severe injuries in a car accident. Long-lasting intensive care began when she was in a state of traumatic shock accompanied by multiple organic failures. There was an extensive craniocerebral contusion. Most of the lesions were situated in both frontal regions, with left prevalence and a bilateral subdural haematoma. In the beginning, the patient was in a deep comatose state. When she showed signs of regaining consciousness, many neurological deficits manifested: hemiparesis on the right side, cerebellar symptomatology, severe psychosyndrome and global aphasia. The peripheral traumatic lesions were compensated for after 3-4 months, which was followed by a slow amelioration of cerebral functions. The aim of this study is to describe the aphasic symptoms in the child during her re-acquisition of language and to compare them with the aphasic symptoms in Czech adults. The conclusion is that the aphasic symptoms of the child are identical to those of comparable cases of adult aphasia and to aphasic symptoms in Czech in general. What is lost, 3'A years after the accident, is fluent reading and writing, smooth access to the whole lexicon and sensitivity to some grammatical features, especially those with a formal character only. What is re-achieved after an almost hopeless state is the ability to use language for communication and reflection. While two years post-onset the comparable adult patient reached a stage after which her language skills no longer improved, this child continued to develop her linguistic abilities. Key words: child aphasia, Czech aphasic symptoms, long-term recovery

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Neurogenic Language Disorders in Children

CASE DESCRIPTION Aphasia is always manifested in a certain impairment of the morphosyntactic structure. All aphasic patients, independently of the type of impairment, make mistakes in grammar. Generally speaking, grammatical problems in language production are mainly reflected in: (1) omission of grammatical morphemes; and (2) substitution of incorrect grammatical morphemes for correct ones. In inflecting languages only free grammatical morphemes are omitted. Bound morphemes are substituted because word stems cannot stand as separate items. Czech is a strongly inflecting language with a great number of different grammatical forms for each inflected word. Grammatical relations in Czech are mostly expressed by bound morphemes. The typical structure of inflected words consists of a stem and an ending, neither of which exist as separate words. In Leheckova (2001) I have described the typical manifestations of agrammatism in Czech adults: (a) omission of some grammatical words (mainly prepositions, auxiliaries and pronouns); (b) concentration of errors in some grammatical categories (especially case, tense and person); (c) overuse of certain forms of grammatical categories (masculine gender, singular number, nominative case, 3rd person, present tense, indicative mood, active voice and imperfective aspect). In this paper I present a detailed description of a longitudinal study of a Czech child with acquired aphasia. The patterns of aphasia in childhood have been believed not to be exactly the same as those in adulthood. The aim of this paper is to describe the aphasic symptoms in a child during her re-acquisition of language and to compare them with aphasic symptoms in adults. The results may shed some light not only on child aphasia but also on the functioning of language in general.

Diagnosis The patient (born 1988, right-handed, female) was 11 years old when she sustained multiple severe injuries in a car accident. The long-lasting intensive care began during the severe traumatic shock state and was accompanied by multiple organic failures. First, it was necessary to compensate for the exudative pulmonary contusion with traumatic hepatic and lienal lesions and to stabilize multiple osseous fractures: clavicular, scapular and pelvic. In addition, the patient had an extensive craniocerebral contusion. The largest of the lesions was situated in both frontal regions, with prevalence on the left side and a bilateral subdural haematoma. During her prolonged intensive care, an infectious endocarditis appeared, requiring protracted treatment with different antibiotics. A hemorrhagic gastrointestinal ulcer also developed. Both subdural haematomas were treated by repeated surgical evacuation.

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Three months after she sustained the injury, computer tomography showed post-contusion and post-ischemic changes in her left frontal, temporal and parietal lobes, significant supratentorial brain atrophy with a dilated ventricular system -the 3rd ventricule was 10 mm wide. Subdural collection occurred on both sides with the character of a chronical haematoma that was 11 mm thick. For three months after the accident, the patient remained in a deep coma which was followed by an apallic state. The peripheral traumatic lesions were compensated for after 3-4 months, followed by a slow amelioration of her cerebral functions. When the child exhibited signs of regaining consciousness, about four months post-onset, more local neurological deficits manifested. Central spastic quadriparesis changed into a hemiparesis on the right side, and the patient was diagnosed with cerebellar symptomatology and severe psychosyndrome. The initial global aphasia developed into a mixed aphasia with a predominant expressive component (Broca's aphasia). The clinical neurological amelioration was accompanied by the amelioration of diffuse EEG abnormalities and improved evoked potentials. After six months of intensive care, the patient could be transferred to the Institute of Rehabilitation for physiotherapy and logopaedic training. Two months of these procedures markedly ameliorated the symptoms. Computerized tomography conducted six months post-onset revealed that the subdural collection had receded on both sides. Thus, only smaller residual changes could be observed frontally on both sides. Post-contusion and post-ischemic changes remained in the frontal, temporal and parietal regions. The signs of supratentorial brain atrophy, located mainly in the left hemisphere, had not changed. The neurological report stated that the patient had a central right-sided hemiparesis, tremor and apraxia. The patient was cooperative, though motorically and mentally apparently slow. Rehabilitation1 Six months after her accident, the patient was admitted to the Institute of Rehabilitation. She was in a wheelchair, accompanied by her mother. She was insecure and frightened in her new environment. Her articulatory organs showed no pathology, her sight and hearing were normal. Her voice was high and clear, and she breathed calmly. She had difficulties coordinating her articulatory movements. The patient communicated only by gestures and mimics in answers to yes-no-questions. She understood basic instructions and tended to show objects and pictures correctly even though her achievement was restricted by her apraxia. On the other hand, she was confused by instructions containing more complicated grammatical structures (constructions containing prepositions, prefixes, etc.):

1

In this section I shall present an overview of medical reports made by neurologists, phoniatrists and speech therapists during the three years after the accident.

202 (1)

(2)

Neurogenic Language Disorders in Children Dej papir na knihu.

'Put the paper on the book.'

Dejpapir do knihy.

'Put the paper in the book.'

Dej papir pfed knihu.

'Put the paper in front of the book.'

Vyndej papir z knihy.

'Take the paper out of the book.'

Lezi kniha na stole?

'Does the book lie on the table?'

Nelezi kniha pod stolem ?

'Doesn't the book lie under the table?'

Nelezi kniha vedle stolu?

'Doesn't the book lie beside the table?'

The patient had problems in establishing logico-grammatical relations such as the opposition between 'first - last', 'big - small', and 'biggest - smallest'. She made mistakes in recognizing colours. Furthermore, she was unable to repeat and used the perseverance mama instead. She could not name objects. She read globally, put inscriptions to pictures but used only short simple words. She made mistakes eventually and corrected herself occasionally. She was unable to read letters or nonsense words. She made mistakes in recognizing numbers and she was more certain of the 100-1000 scale than in smaller numbers. She had apraxia. She began speech therapy by doing phonic exercises during which she produced all vowels (la/, /i/, /u/\ with some difficulties lo/, /e/). Later, they were combined with consonants in syllables (pa - ba - ma, pi - bi - mi, etc.), reduplicated syllables (jo-jo, je-je, pi-pi, etc.) and simple words (bdba, ndna, pipd, pes, pas). Short sentences were then introduced: (3)

Mimi hajd.

'Baby sleeps.'

Tata void.

'Daddy calls.'

Her repetition gradually improved. The most difficult phonemes proved to be Iv/, /f/, /// and M. Six weeks after having started intensive speech therapy the patient could repeat short sentences, especially when divided into syllables. She named spontaneously about 20 familiar pictures. She recognized some letters in the alphabet but was uncertain about them. She could count to 10. Speech production improved, although it was not fluent. She provided mostly one-word answers to questions and rarely used a simple sentence. Her speech was very slow, her intonation flat and she expressed herself with no emotional charge. She had hypomimia. Her understanding of grammatical structures, e.g. (1) or (2), improved but was far from perfect. At one year and three months post-onset, all symptoms of Gerstmann's syndrome were still present (i.e. amnestic aphasia, alexia, agraphia, acalculia, agnosia of fingers and problems with left — right orientation). Whereas spontaneous drawing was impossible for her, copying was preserved. Her spontaneous speech was slow and laborious with apparent word-finding

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difficulties. Understanding of speech was relatively good as far as global information was concerned. However, isolated information (without context) caused problems. At one and a half years post-onset Gerstmann's syndrome was still observable but had improved. She had much better left - right orientation and finger gnosia with only a slight uncertainty. Her drawing had improved substantially, both in copying and as spontaneous activity. Her spontaneous speech was still marked by word-finding difficulties, but to a lesser degree. Acalculia and alexia persisted. Three years after the accident the character of aphasia is reported to have changed both qualitatively and quantitatively: from global through Broca's to amnestic aphasia. Finger agnosia had disappeared. Her drawing further developed both as to form and content. Moreover, her spontaneous speech improved considerably. Latencies caused by word-finding difficulties almost disappeared. The patient needed a longer time for reading, remembering and reproducing a text. Understanding of logico-grammatical structures still caused problems but they were smaller than before. School attendance Before the injury, the patient was an excellent pupil in the 6th form of a primary school. She resumed school attendance one year after the accident, although she still could neither read nor write. She had hemiparesis on the right-hand side and her psychomotor performance was slower. However, her intellectual capacity (in the sense of finding connections and solutions) was reported to be undisturbed. As a result, it was recommended that she not be transferred to a special school but be kept in her previous class, even though she could not fully participate in the schoolwork. Three and a half years post-onset, the patient is attending the last form of compulsory primary school. She is not marked and follows an individual plan. Her family faces the serious problem of her further education.

APHASIC SYMPTOMS 2 IN SPONTANEOUS SPEECH Six months post-onset The patient produced no spontaneous speech except for perseverance on two words: mama ('Mom') and ne ('no'). After six weeks of intensive therapy, she used simple sentences such as: (4)

Jajsem DN.

'I am DN.'

Jdjedu na hole.

'I ride a bike.'

Jd mam pannu.

'I have a doll.'

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Neurogenic Language Disorders in Children

Her spontaneous speech was not fluent. Two and a half years post-onset 1 examined the patient two and a half years after the polytrauma. While organic and motor problems had mostly disappeared by that time, the patient's linguistic functions were not fully restored. I recorded the spontaneous speech of the patient during a long visit at home. I asked her about her illness, school, friends and hobbies. I also asked her to retell the Red Riding Hood story and the content of a film she had seen. The patient cooperated eagerly and spoke fluently. Subjectively she did not feel she had any problems in understanding or expressing herself: (5)

Dfivjsemjako

nevedela, co mam fikat, a co patri k sobe, ale ted' toje normalni.

'Earlier I did not know what to say and what belongs together but now it is normal.' It is only the linguistic analysis that revealed an impairment of language. The material consists of about one hour's recording. There were 3256 words in 543 clauses, 14% of which were ungrammatical. Of all errors, 80% can be classified as omissions and 20% as substitutions. It is not always easy to draw the line between omissions and substitutions, as the same error can be classified as both (for explanation, cf. Leheckova 2001). The criterion that I have applied was the system of Czech language (i.e. in nouns with a zero ending in nominative, I classified a missing ending in another case as substitution by nominative, not an omission of a case ending, because it was analogical to errors in nouns that do have an ending in nominative). The speech of the patient was rather fluent, with normal melody and intonation, without articulatory difficulties. As long as the conversation was confined to small talk with a quick exchange of questions and answers, no abnormalities were observable. Furthermore, the patient understood all questions and re-used many words from the question in her answer: (6)

Hralajsi nejakou hru? 'Did you play any game?' Hrdla. Basket a ... tenis. 'I played. Basketball and ... tennis.'

(7)

Jakou hudbu rdda poslouchds? 'Which music do you like to listen to?'

2

In what follows I shall present my own results obtained from testing the patient.

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205

No takposlouchdm rdda takovou moderni... 'Well, I like to listen to a kind of modern ...' However, longer answers revealed substantial word-finding difficulties and the use of fillers and empty words. (8)

To mi kamarddka nahrdla, to kamardd nekde sehnal, takze to ... takze tyhlety takhle. 'My friend recorded it, my friend found it somewhere, thus that... thus these so.'

(9)

To ted' vsechno mdme asi moderni... to takze takovyhle... jd nevim tfeba ndky skupiny... tfeba ndky kluci... 'Thus now we have everything modern ... so thus such ... I don't know let's say some groups... let's say some boys ...'

(10)

Vsakse fikd, ze muzikajako leci, takjd to to... 'They say that music heals, so I that that...'

The patient encountered difficulties with questions that demanded more complicated formulations and words that were not originally in the question. The speech rate decreased, the syntactic structure of the utterances was disrupted and content words were missing: (11)

Ctes si knizky? 'Do you read books?' Jo, to si ctu. Jdjsem ted' zacala, ted' sem dfiv necetla, ndky holky mi tfeba pucily vo ndkejch... jd nevim, tarn bylo tfeba... tarn bylo vo ndky ... z knihovny jsem tfeba si pucovala, tak tarn je ndky pro nds uz tak ... sem si tfeba cetla .. no ale zatim... to je hrozny. 'Yes, I do read. I have started now, now I have not read earlier, some girls lent me for example about some... I don't know, there was for example ... there was about some ... in the library I borrowed, so there is some for us already so ... I read for example ... well but still... that is terrible.'

When the subject of the question was unexpected, the patient reacted with semantically almost empty utterances. Interestingly enough, the syntactic structure was preserved but content words were missing: (12)

Mohla bys mi vypravovat Cervenou Karkulku? 'Could you tell me Red Riding Hood?'

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Neurogenic Language Disorders in Children No jo, Cervend Karkulka, to jo, ale vyprdvet, to rnoc teda... to nevim, co tarn bylo a co tarn nebylo ... tfeba von si dycky ...no ... co fikd ...ale tfeba co si vymyslim ...moznd bysem si vzpomnela, ale ted' vubec takovyhle pohddky nebo tak...to ted' vubec... 'Oh yes, Red Riding Hood, oh yes, but to tell, well that ... I don't know, what was there and what wasn't there ... for example he always ... well ... what he says ... but maybe what I make out... maybe I would remember, but now such stories or so ... well now completely ...' When the question was more personal and familiar, the patient did much better:

(13)

Vzpomnela by sis vubec na nejakou pohddku nebo pfibeh, kterej se ti libil? Melas rdda pohddky, kdyzjsi by la mala? 'Could you remember any story that you liked? Did you like fairy tales when you were little?' Jo, tak jo. Jd nevim, deda mi vzdycky rikal nejlepsi. To von mel jako pro sebe, o ndkym drakovi, ze byli ctyri nohy, teda ... jd nevim, jak mne to deda rikal... asi tak by la asi takovd nejlepsipohddka, co deda vzdycky... 'Well, yes. I don't know, Grandfather always told the best ones. He had it out of himself, about a dragon, that there were four legs, actually ... I don't know how grandfather told it... about that was about the best story, what grandfather always ...'

Table 1 — Omissions in spontaneous speech. Omitted item

Number of errors 17 11 3 5 8 2 3

Percent of all errors 28% 18% 5% 8% 13% 3% 5%

Content words

Finite verb in pres Finite verb in past Infinitive Past participle Predicative adjective Noun after preposition Adverbial

Content / Grammatical words

Pro/noun in object

9

15%

Grammatical words

Preposition Modal verb before inf.

2 1

3% 2%

Long-term language recovery in an aphasic Czech child Total (omitted items)

Number of errors 49 9 3

Content words Content/grammatical words Grammatical words

207

Percent of all errors 80% 15% 5%

Omissions. Relatively few grammatical errors were found in the material. The patient even used grammatical items that are most difficult for children, i.e. comparative/superlative, or the conditional. The syntactic structure was mostly preserved, even though some arguments were missing. As expected, only free morphemes were omitted. Surprisingly, the omissions affected mostly content words (49 errors, i.e. 80% of omissions), not grammatical words. There were only 3 examples of missing purely grammatical items, while in 9 cases, the missing word could be a pronoun as well as a noun. Substitutions. Errors caused by substitution were rarer than those caused by omission. Few lexical substitutions occurred: (14)

pisnicka ('song') instead of pismenko ('letter')

(15)

drak ma styri nohy ('dragon has four legs') instead of hlavy ('heads')

(16)

tak dve nebo tak ('about two or so') instead oinekolik ('several')

Table 2 — Substitutions in spontaneous speech Category Gender Number Case

Other Total (uncorrected errors)

Replacing item Replaced item IN[umber of errors 1 FEM MASC 1 NEUTR FEM 3 PL SG 1 SG PL 2 ACC NOM 1 NOM INSTR GEN 1 NOM INSTR 1 GEN 2 PREP PREP 13

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Neurogenic Language Disorders in Children

Self-corrected errors:

Category

Replacing item

Number

Replaced item

PL

SG

Total (self-corrected errors)

Number of cases 1 1

Grammatical substitutions affected mainly bound morphemes. There were only two substitutions of free morphemes (prepositions), otherwise one grammatical ending was replaced by another ending belonging to the same category. The number of substitutions is too small to draw any definitive conclusion. Nevertheless, the replacing forms are mostly those that I have defined as best preserved in Czech adult aphasics: i.e. masculine gender, singular number, nominative case, 3 rd person, present tense, indicative mood, active voice and the imperfective aspect (for the hierarchy of replacing forms, cf. Leheckova, 2001). Neologisms. There were 10 neologisms in the recording: 4 were nonsense-words both lexically and structurally, while 6 were non-existing words with correct grammatical endings: (17)

tak me tak docela pobuzdili (instead of povzbudili) 'thus they rather supported me1 - 3rd PERS PL PAST

(18)

dycky me tak ndk pozdrej (instead ofpodrzej) 'they always somehow keep me' - 3rd PERS PL PRES

(19)

voni sou ted' v kutdku (instead of e.g. v prvdku) 'they are now in (e.g. first form)' - LOC SG

(20)

ale snazilajsem se to vsechno narazit (instead of e.g. nahradit) 'I tried to replace that all' - INF

(21)

nejtezsijsou tydlety prirodnice (instead of e.g. prdce) 'the most difficult are these subjects' - NOM PL FEM

The patient overused some words expressing uncertainty (jd nevim 'I don't know', tfeba 'for example', moznd 'maybe', etc.). Three and a half years post-onset A year after the first recording, I again recorded the patient's responses to the same questions. During the second session, she produced 1981 words which were divided into 342 clauses. Of

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209

these, 6% were erroneous. Most of her errors were omissions (62%). As before, she omitted mainly content words, especially verbs. In the second recording, she only omitted 2 grammatical words. The substitutions again concentrated in the category of case (75%). While in the previous testing the patient substituted mostly nominative case for other cases, during the second testing she replaced cases without a clear preference (genitive for dative, instrumental for genitive, dative for accusative, genitive for locative, nominative for accusative etc.). There was only one neologism in the material, which was used with the proper verbal ending. The grammaticality of the spontaneous speech improved quantitatively while qualitatively showed roughly the same tendencies as a year ago. Table 3 — Errors in spontaneous speech at 2 14 and 3 Vi years post-onset 2!4 years post-onset Ungrammatical clauses Errors caused by omission Errors caused by substitution Number of neologisms

3/4 years post-onset

14% 80% 20% 10

6% 62% 38% 1

GRAMMATICAL TESTS Two and a half years post-onset Two and a half years post-onset the spontaneous speech of the patient seemed to be only mildly impaired. However, grammatical tests revealed a more serious deficit. There were two grammatical issues that I tested with the patient: prepositions and prefixes. The reason for this choice is based on my experience with aphasics on the one hand and language learners on the other. Even patients with mild impairments as well as foreigners speaking Czech have problems both with prepositions and prefixes. Prepositions. The use of prepositions in Czech is influenced by two factors: either by their own (mostly spatial) meaning as in (22), or by the government (mostly of the verb), as in (23): (22)

(23)

Zahradaje za domem.

'The garden is behind the house.1

Knihaje na stole.

'The book is on the table.'

Dekuji ti za dopis.

'Thank you for the letter.'

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Neurogenic Language Disorders in Children Odpovez na otdzku.

'Answer the question.'

The patient was administered a test consisting of written sentences in which the preposition was missing and the noun was given in its nominative form. (24)

Moji rodice bydli 'My parents live

(Praha). (Prague).'

Test 1 is comprised of 34 sentences with missing prepositions having their own lexical meaning. It took the patient 25 minutes to fill in the gaps. There were two wrong prepositions substituted for the correct ones and one preposition was omitted. Thus, 9% of the sentences were erroneous. Test 2 consisted of 33 sentences with missing prepositions having grammatical meaning only. The test took the patient 25 minutes to accomplish. One preposition was replaced by a wrong one and three prepositions were omitted. Thus, 12% of sentences were erroneous. It seems to be easier to omit and even substitute prepositions that have only a grammatical function. Some of the errors were caused by choosing a wrong, but in another context possible, government: (25)

Rodice poslali doktora. 'The parents sent the doctor.' instead of Rodice poslali pro doktora. 'The parents sent for the doctor.'

However, it would be possible to say: Rodice poslali telegram. 'The parents sent a wire.' (26)

Vybral si bohatou nabidku. 'He chose a rich offer.' instead of Vybral si z bohate nabidky. 'He chose from a rich offer.'

However, it would be possible to say: Vybral si bohatou nevestu. 'He chose a rich bride.'

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The patient did not have many prepositional errors in her spontaneous speech (two prepositions omitted, two substituted for by another preposition). The grammatical test revealed a more serious problem in this category, especially with prepositions without lexical meaning. Prefixes. Czech verb can be modified by different prefixes. Prefixes have a purely grammatical function, i.e. they form the perfective aspect from imperfective: (27)

Psal dopis. Napsal dopis.

'He was writing a letter.' 'He has written a letter.'

Prefixes can also modify the meaning of the verb: (28)

Dopsal dopis . Rozepsal dopis. Pfepsal dopis. Podepsal dopis.

'He finished writing a letter.' 'He started to write a letter.' 'He wrote the letter again.' 'He signed a letter.'

The patient was administered three tests with missing prefixes. Test 3 consisted of 20 sentences with verbs that demanded unmotivated grammatical prefixes: (29)

Je tfeba to poradne ... .pldnovat. 'It must be well planned.' Je tfeba to pofddne napldnovat.

(30)

Tatinek se rdno zapomnel... holit. 'Daddy forgot to shave himself in the morning.' Tatinek se rdno zapomnel oholit.

The patient completed the test in seven minutes with one error only (omission of prefix). Test 4 had the same structure but the missing prefixes had their own meaning, that of direction: (31)

Na pfisti zastdvce musite vystoupit. Dobehl do cilejako prvni.

'You must get off on the next stop.' 'He ran into the goal as the first.'

The patient usually used the same prefix as the preposition in the sentence. This is often correct:

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(32)

Auto zajelo za roh. 'The car disappeared.'

Sometimes the following is possible, though not as a first option: (33)

Dojeli jsme vytahem do pfizemi. 'We descended to the ground floor by elevator.' instead of Sjelijsme vytahem do pfizemi.

Sometimes it is wrong: (34)

Dopsaljsem se do sesitu. 'I wrote my name in the notebook.' instead of Zapsaljsem se do sesitu.

The patient needed 25 minutes for this test and made 8 mistakes: three omissions and five substitutions. That means that 40% of the responses were incorrect. Test 5 consisted of 20 sentences with missing prefixes in a more abstract, mostly idiomatic meaning: (35)

Maji pofad obsazeno, nemuzu se tarn dovolat. 'The phone is busy, I cannot get through.' Ktere noviny mate pfedplacene? 'Which newspaper do you subscribe to?'

The patient completed this task in 20 minutes with five errors (two omissions and three substitutions), thus 25% of the responses were incorrect. In her spontaneous speech the patient made no errors in prefixes but did not use many prefixes (only 19). Grammatical tests revealed the uncertainty of the patient as far as prefixes were concerned. I expected that the biggest problem would be caused by purely grammatical prefixes that cannot be chosen on the basis of their meaning. However, they were almost always used correctly. The most difficult proved to be the use of prefixes with directional meaning. In choosing them, both their meaning and the structure of the sentence must be taken into account. The use of prefixes in idioms was better because the expressions concerned are very frequent in everyday use.

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Three and a half years post-onset One year later I administered the grammatical tests again to the patient. She was asked both to fill in missing grammatical items and to judge the grammaticality of the test sentences. Compared to the previous testing, she was much quicker and self-assured in her responses. However, the error rate in the grammatical categories in question was still much higher than in her spontaneous speech generally, hi contrast to the previous testing, the differences in test scores diminished.

Table 4 — Errors on grammatical tests

Test No. 1 2 3 4 5

Grammatical features tested Prepositions with lexical meaning Prepositions with grammatical meaning Grammatical prefixes Directional / spatial prefixes Idiomatic prefixes

2'A years post-onset Error Time rate 9% 25 min 12% 25 min 5% 40% 25%

7 min 25 min 20 min

3/2 years post-onset Error Time rate 21% 8 min 27% 12 min

11% 26% 15%

4 min 15 min 10 min

As the patient was doing well enough and was cooperative, I could test other grammatical issues as well. I used similar tasks as those proposed in Paradis (1989). The patient had no problems with determining thematic roles (both for nouns and pronouns) as long as there was the canonic word order (SVO). (36)

Divka strka chlapce.' 'The girl (NOM) pushes the boy (ACC).' Divka ho strka. 'The girl (NOM) pushes him (ACC).'

When the word order changed into OVS, which is quite possible in Czech, she assigned the role of the agent to the first noun, although it was in accusative: (37)

Chlapce strka divka. 'The boy (ACC) pushes the girl (NOM).' It is the girl who pushes the boy.

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The patient also got confused by negation: (38)

Chlapce divka nestrkd. 'The boy (ACC) the girl (NOM) not push.' The boy is not pushed by the girl.

She could not construct simple sentences from given words in basic forms: (39)

zeleny / list / videt 'green / a leaf/ to see'

Her reading was laborious and slow, she obviously did not understand what she was reading. When asked about less frequent words, she did not know their meaning. Moreover, she was unable to find synonyms and antonyms to isolated words but she was doing much better with words in context or with whole sentences. Another problem she encountered was that she could not divide the text written without punctuation into sentences. Recent grammatical tests show that the patient's linguistic performance is far from being perfect. The main difficulty seems to concentrate in her syntactic (structural) organization of language, both in production and perception.

WRITING AND DRAWING The patient suffered from a complete agraphia after the accident. Six months later, she tried to use her left hand for writing block letters. She found that could not make a cross, a circle or connect two points. She was also unable to sign her name. After six weeks of intensive therapy she switched back to the right hand, although her left hand was still more dexterous. She could now spontaneously produce the following block letters: D, T, A, E, I, M. She could draw a cross and a circle, which reflected her improvement. Two months later, she was able to draw simplified pictures of her house and of a human being. At this point, she could write her name, but she was not able to write spontaneously any other word. On the other hand, she could copy writing. One year and three months post-onset, the patient began to use block letters and simple pictures spontaneously: (40)

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(41)

One and a half years post-onset she still could not manage handwriting but her drawing was improving.

Two years post-onset, the patient could write the names of the weekdays with only slight errors {uteri instead of utery). In this instance, both forms would be pronounced in the same way but an orthographic rule dictates that the word should be written utery. According to this rule letter r cannot be followed by i/i but only by y/y and this is already mastered by nine-year-old children. (44)

utery stfeda ctvrtek pdtek sobota nedele

'Tuesday' 'Wednesday' Thursday1 'Friday' 'Saturday' 'Sunday'

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She wrote spontaneously the following sentence: (45)

Cesta z Podebrad do Prahy byla ndrocna. 'The journey from P. to Prague was difficult.' Pronounced as [cesta s pod'ebrat do prahi bila na:rocna:]

This sentence resembles a phonetic transcription, in that it reflects more or less the phonetic value of the spoken form but neglects all rules of orthography which had been well known to the patient before the accident. In fact, she did not even start the sentence with a capital letter or end it with a period. Her drawing continued to develop: (46)

Two years post-onset the patient used a computer to type spontaneously a longer text (94 words) about Christmas. This text is surprisingly consistent and contains no major lexical or grammatical mistakes. On the other hand, it completely neglects orthographic rules and reflects only the phonetic representation. It is worth noting that at that time, the patient could not have delivered a coherent speech of this type orally. This text starts with a capital letter but contains no punctuation except for one period in an inappropriate place. She uses capitals for the kinship terms 'Mum, Dad, Grandmother, Grandfather', which is incorrect in Czech, but she does not begin the sentence with a capital letter. There are many misspellings, usually reflecting what is pronounced instead of what should be written. Often two words are merged into one. The phonetically motivated mistakes were:

Long-term language recovery in an aphasic Czech child

(47)

217

gdis instead of kdyz pronounced as [gdis] 'when' du instead ofjdu pronounced [du] 'I go' pride instead ofpfijde pronounced [pfi:de] 'it comes' druhi instead ofdruhy pronounced [druhi:] 'second' g Dedovi instead of A; dedovi pronounced [gd'edovi] 'to Grandfather' nejraci instead of nejradsi pronounced [nejraci] 'I like most'

The phonetically unmotivated mistakes were: (48)

chamilie insead offamilie 'family' kukuju instead ofkupuju 'I buy'; repeated in the next sentence: koukim instead koupim 'I shall buy' Vdvdnoce instead of Vdnoce 'Christmas' (reduplication)

Two years and four months post-onset, the patient made the same errors in listing weekdays as four months earlier.

Two years and seven months post-onset, the patient handwrote a text about her summer holiday (111 words): (50)

This text is divided into sentences, although punctuation is often incorrect. For example, commas are mostly missing, periods are used in illogical places and are not followed by capital letters, and conjunctions do not correspond to the logical structure of the text: (51)

Kdyz jsme pfijeli takjsme nevefili vlastnim ocim ale potom jsme to pfezili. ale koupili jsme si dve deky 'When we came we did not believe our eyes but then we coped, but we bought two blankets'

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Her lexicon and grammar do not exhibit major mistakes. Her orthography has improved dramatically, as there is only one misspelling: (52)

podkala instead of potkala pronounced [potkala] 'I met'

Three years post-onset, the patient's handwriting improved slightly but she still occasionally forgot letters. The patient preferred to write on a computer. She wrote spontaneously an introspective text of 488 words. This text is divided into long sentences starting with a capital letter and ending with a period. However, clauses within sentences are not divided by obligatory punctuation so that 60 commas or periods are missing. Otherwise the patient made only four grammatical mistakes: — one missing relative pronoun: (53)

a ptaljak mu to slusi 'and he asked how he looked' instead of a ptal se, jak mu to slusi

— one missing subordinate conjunction 'that': (54)

byla st'astna jsme si psali kazdy den 'she was happy that we wrote every day' instead of byla st'astna, zejsme si psali kazdy den

— one missing object of a transitive verb: (55)

ale nebudu psatprotoze si mislim 'but I shall not write it because I think' instead of ale nebudu to psdt, protoze si myslim

— one substituted preposition: (56)

s autobusu instead of k autobusu 'to the bus'

There were 21 misspellings, which were mainly the incorrect representations of the phoneme HI. In Czech I'll can be written either as i or y, depending on the morphophonological

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219

context. The patient would certainly not have made similar mistakes before the accident as she had been taught the correct orthography at school by the age of 11 and she had been an excellent pupil. Examples of the letter i used instead oiy are: (57)

druchi instead of druhy 'another' pizamo instead oipyzamo 'pyjamas' holky zarlili instead oiholky zdrlily 'girls were jealous' mislim instead otmyslim 'I think' (2 errors)

The use of the letter >> instead of/: (5 8) lavycce instead of lavicce 'a bench' libym instead of libim 'I like' stavyl instead oistavil 'he stopped' vydet instead of videt 'to see' (3 errors) nevym instead of nevim 'I don't know1 The letter ch (in Czech ch is taken for one letter representing the voiceless /h/) instead ofh: (59) druchi instead of druhy 'another' pomdchat instead ofpomdhat 'to help' dloucho instead of dlouho 'long' The letter ch instead of/? (60) douchdm instead of doufdm 'I hope' The letter z instead off: (61) zikat instead offikat 'to say' (6 errors) Her drawing again improved: (62)

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The patient's spontaneous writing seemed to adjust to spontaneous speech, with regard to both the orthography of single words and the text structure. She has made a tremendous development in re-achieving her writing skills but text subdivision into structured concatenation of clauses and correct spelling remained out of reach. When I asked the patient whether she remembered the orthographic rules that she had learned at school, she answered affirmatively. Nevertheless, she completely neglects these in her writing, even when she is copying texts (cf. zeleny - zeleni 'green', videt - vydet 'to see') (63)

zeleny / list / videt and especially in spontaneous writing (commas missing, an impossible combination of f+y): (64)

Jirka zjistil, ze ho boli zuby, tak se rozhodl, ze pujde k lekafi. 'Jirka found out that he has tooth-ache, thus he decided to go to the dentist.'

COMPARISON WITH AN ADULT CASE In what follows I shall compare the language production of the child with that of an adult who was, just like the child, classified two and a half years post-onset as having amnestic aphasia with about the same severity of language impairment, i.e. she was able to accomplish the same linguistic tasks with roughly the same error rate. My aim is to capture the type of their errors3. The patient (born 1945, female, right-handed, computer maintenance person) suffered a haemorrhage in the left parietal region with a right-sided hemiparesis and mixed aphasia in February 1997. The haematoma was aspirated. Angiography revealed a residual arteriovenous malformation (AVM), which was irradiated by a Gamma Knife in April 1998. Eight months 3

As a linguist based in Finland, I am not in permanent touch with Czech aphasic patients. Their choice and diagnosis (including the determination of the type of aphasia) are made by speech pathologists and neurologists with whom I have been co-operating. I concentrate on the linguistic analysis of the material.

Long-term language recovery in an aphasic Czech child

221

post-onset, the patient began speech therapy. An amelioration of the hemiparesis and aphasia was observed during the rehabilitation. I examined the patient two and a half years post-onset. She was diagnosed as having residual hemiparesis on the right side, agraphia, alexia and amnestic aphasia. Her sight and hearing, as well as orientation as to time and space, were normal. The patient still could not write with her right hand. She used her left hand to compensate, but only for a short time before she got tired. She had difficulties with reading, especially long words. She had special problems with letters v and /, and she could not differentiate letters a and e. Her spontaneous speech was relatively fluent, though slow. The impairment of grammatical structure was mild. The patient often noticed that she had made a mistake and tried desperately to correct herself. When she did not succeed, she expressed her dissatisfaction: (65)

Mohl bych vets prosit ... laskavost? Ale neco tarn chybi, ne? Jajsempak takovd nest'astnd. 'Could I ask you for (omitted PREP) something? But something is missing there, isn't it?

I am so unhappy then.' The patient had occasional word-finding difficulties, especially with members of the following automated sequences: (66)

bylo to pondeli, utery, ne, stfeda 'it was Monday, Tuesday, no, Wednesday'

(67)

chci deset, patndct, ne, dvacet deka 'I want ten, fifteen, no, twenty decagrammes'

Spontaneous speech I met the patient in one session, and our conversation was recorded. I inquired about her illness, her work and her hobbies. The analysed material consists of 824 clauses containing 4126 words. The average number of words per clause (5) is rather high, because repetitions were counted as separate words. Of the total 824 clauses, 89 were erroneous, i.e. 11% of clauses were ungrammatical. Among the errors, 71% were classified as omissions and 29% were substitutions. Omissions. It is interesting to note that in both cases, most of the omissions are such that the omitted element is a content word, not a grammatical one. Furthermore, most of the omissions affect finite verbs (46% for the child and 45% for the adult). Curiously enough, no

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auxiliaries were missing, while infinitives and participles after auxiliaries were omitted in several cases. (68)

no, takjsem ..., kdyz jsem nemohla vubec ...-, takjsemji

ukdzala tohleto

'well, so I have ..., when I couldn't at all..., so I showed it to her' There were as many cases of omitted prepositions before nouns as omitted nouns after prepositions: (69)

takjsem furt chodila do ..., kdyz topfislo 'so I used to go to ... (omitted NOUN) when it occured'

(70)

kdyz ...- ty operace

seprobudim

'when ... (omitted PREP) the operation I wake up' Table 5 — Transcribed material of the child and the adult (2V2 years post-onset) The adult

The child Words Clauses Ungrammatical clauses Errors: Omissions Substitutions

3256

4126

543

824

76

14%

94

11%

61

80%

67

71%

15

20%

27

29%

Table 6 — Comparison of omissions between the child and the adult patients Omitted items

Finite verb in PRES Finite verb in PAST Finite verb in FUT Infinitive Past participle Predicative adjective Noun after PREPOSITION Adverbial Pro/noun in OBJECT Pro/noun in SUBJECT Preposition Modal verb before INFINITIVE

The child Number ]Percent of all of errors errors

The adult

Number of errors

Percent of all errors

17

28%

22

33%

11

18%

7

10%

1

1%

5%

9

13%

5

8%

7

10%

8

13%

6

9%

2

3%

3

5%

6

9%

3

3

5%

9

15%

2

3%

1

2%

3

5%

3

5%

Long-term language recovery in an aphasic Czech child

Total (omitted items)

The child

Content words Content/Grammatical words Grammatical words

Number of errors 49 9 3

223

Th e adult

Percent of all errors 80% 15% 5%

Number of errors 55 9 3

Percent of all errors 82% 13% 5%

Substitutions. Interestingly enough, the self-corrected errors do not correspond to the substitution hierarchy presented in Leheckova (2001), whereas the uncorrected errors do follow the suggested hierarchical pattern. The majority of the substitution errors were existing forms of the same category, and as to the order of substitution, they showed the same tendency as described in Leheckova (2001). The number of errors was nevertheless too small to make generalizations concerning the distribution among different forms.

Table 7 — Comparison of substitutions between the child and the adult patients

Category

Replacing item

Replaced item

Gender

MASC FEM SG PL NOM NOM NOM NOM GEN 3SG 1SG PRES IND

FEM NEUTR PL SG ACC INSTR GEN LOC INSTR 1SG 2SG PAST COND

PREP INDEF. PRON.

PREP FINITE VERB

Number Case

Person Tense Moorf Other

Total (uncorrected errors)

The child

The adult

Number of errors 1 1 3 1 2 1 1

Number of errors 2 2 2 2 4

1 2 1 4 1 2 13

4 24

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Neurogenic Language Disorders in Children

Self-corrected errors:

Category

Replacing item

Gender NEUTR Number PL Person 2SG Other INF Total (self-corrected errors)

Replaced item

The child Number of errors

MASC SG 1SG PAST PART

The adult Number of errors 1

1

1

1 1 3

Neologisms. The adult patient did not use neologisms. When she could not find the correct word, she used indefinite pronouns or adverbs instead (which sometimes occurs even in normal spontaneous speech): (71)

tak to me tak tohleto 'so it me so like this'

(72)

no tak tohleto tak, todleto tadyhle 'well so this so, this here'

The adult patient seemed to have greater word-finding difficulties than the child, although the latter used neologisms that appeared to be correct grammatically in analogical situations. Grammatical tests The most significant grammatical problem in the spontaneous speech of the adult patient seems to be the use of a preposition with a noun phrase. The adult patient omitted either a preposition or a noun, or put the noun in a wrong case (nominative singular). The material contained 68 occurrences of the PREPOSITION + NOUN combination, out of which 46 were correct and 22 incorrect. This error rate (32%) is much higher than in other categories (median 11%). It is also noteworthy that during the following sessions, the patient did not make any preposition errors in grammatical tests that were administered in the written form (cf. 2.2.). She succeeded in achieving 100% accuracy, although she displayed hesitation. (73)

Vesnice byla za - na - ee -po zemetreseni uplne znicena. 'The village was behind - on - ee- completely destroyed after the earthquake.'

The adult patient made many preposition errors in spontaneous speech but none in grammatical tests. The child, on the contrary, made few errors in prepositions in spontaneous

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225

speech but many on tests. As for prefixes, the adult had neither errors in her spontaneous speech nor on the grammatical tests two years post-onset, while the child continued to make mistakes (median error rate 17%) even three and a half years, after her injury. Writing and reading The writing samples of the child and adult could not be compared due to the adult patient's lasting right hemiparesis. Both patients reported difficulties in reading. The child expressed these sentiments: (74)

To je hrozny, jd vzdycky kdyz si to pfectu, ale moc tomu nerozumim, tak si to musim vod zacdtku vsechno, takze to je delsi doba... Nekdy tfeba... kdyz j'a ctu a nekdo na me promluvi, tak to musim cist uplneznova, a toje... 'That is awful, I always when I have read it, but I do not understand it very much, thus I have to ... from the beginning everything, thus it is a longer time ... Sometimes maybe ... when I am reading and somebody speaks to me, so I have to reread it from the very beginning again, and that is ...'

The adult: (75)

Mne se ted' stdvd to, ze viibec, jako ted'... nevim, co ctu i co je to na ... ee ... za pismenko, tfeba a musim to odlozit, ze chci taky cist, jo. Nahlas mne to nejde, to se nejak zarazim a nemuzu, tak abych vedela, co ctu, zejo, no takjenom tohle. ' It happens to me that I at all, as now ... do not know what I read and what is on ... ee ... which letter, maybe I have to put it down, that I want to read too, yes. I cannot read aloud, I get somehow stuck and cannot, so that I know what I am reading, all right, so thus only this.'

APHASIA IN CHILDHOOD AND IN ADULTHOOD Acquired childhood aphasia is a relatively rare syndrome and its clinical description has changed substantially over the last 15 years (Van Hout, 2000). The patterns of aphasia in childhood had been reported not to be exactly like those of adulthood. The similarity of all aphasias in children suggested that language abilities might be more diffusely organized for them, at least within the language areas, than in adults. Obler (2000) states that there are no reports of fluent aphasias in children. Even when the localization of the lesion would suggest a Wernicke's aphasia, the child will produce slow, laborious speech with reduced syntactic

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Neurogenic Language Disorders in Children

complexity, if not outright agrammatism. Most recently, however, neurological studies have observed that aphasic syndromes in children are somewhat similar to adult aphasic syndromes. Van Hout (2000) maintains that all aphasic subtypes described in adults also apply to children. Prognosis is less favourable than what was originally thought, both in terms of language sequelae and academic failure (Pavao Martins, 1991; Van Hout, 1992). Lenneberg (1967) studied children with unilateral brain injury to analyse its effects on language and concluded that the two hemispheres are initially equally able to control language. This is known as the equipotentiality hypothesis. He maintained that in the age group consisting of 3-10 year-olds aphasic symptoms tend to be fully recovered (except in reading and/or writing). At that age, there is evidence of both hemispheres' involvement in language and it is thus possible to re-establish language in the right hemisphere if the left is damaged. In the age-group of 11-14 year-olds, some aphasia symptoms are not reversible, particularly after traumatic lesions. Lateralization is formally established already at this age and it is usually irreversible. More recent studies have shown that the right hemisphere is not entirely able to take over language functions, even in childhood. The language of children who had had left-brain damage looked normal on the surface as they participated in daily conversation. However, grammatical tests revealed below-normal performance (Dennis & Kohn, 1975). Aram (1988) analysed the spontaneous speech of aphasic children and concluded that lefthemisphere-damaged children had more difficulty with simple and complex sentences than normal controls. Both left- and right-hemisphere-damaged children showed persistent difficulty in naming objects. Children with a left-sided injury answered questions more slowly but more accurately than children with a right-sided injury. Aram found no effect of age at the time of brain injury in any of her analyses. Murdoch (1990) points out that although the rate of spontaneous recovery in children following closed head injury is often described as excellent, persistent long-term language disorders have been reported. Especially naming difficulties in children with acquired aphasia are more common than first thought. Written language disorders are often more severe than oral language impairment, and expressive disorders more frequent than the receptive disorders of written language. The present case of child aphasia in Czech confirms these findings. On the one hand, the patient recovered remarkably well from a serious polytrauma and from being in a comatose state for four months. After a global aphasia, she progressed into a mild amnestic aphasia and re-achieved most of the linguistic functions, except for fluent writing and reading. On the other hand, a linguistic analysis uncovers grammatical and lexical problems that do not necessarily appear in everyday conversation but which nevertheless restrict the patient's language. Van Hout (2000) points out that, although aphasic symptoms in children have been found to be similar to those of adults, children may show atypical symptoms. Their frequency might provide an explanation for some of the discrepancies found between classic and new

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227

symptom descriptions in childhood aphasia. Some of these symptoms consist in a dissociation between the different fluency parameters, or in general hypospontaneity. Hypospontaneity was not manifested in the present case of a Czech child. Compared to an analogous case of adult aphasia, the child's spontaneous speech appeared to be more normal. The child neither noticed nor corrected her errors, whereas the adult patient was very upset about her mistakes. While the adult compensated for her word-finding difficulties using a very slow speech rate and long pauses while she searched for words from the same lexical field, the child replaced the missing lexemes either by neologisms that have the formal characteristics of the target word, or by indefinite expressions. In other respects, the linguistic deficit of the child corresponds both quantitatively and qualitatively to the comparable adult case. Moreover, the type of linguistic errors made by the child is in accordance with the manifestation of aphasic symptoms in Czech adults in general. My synoptic study of the spontaneous speech of Czech aphasics (cf. Leheckova, 2001) showed that: a. the morpho-syntactic structure of language production is impaired for all patients; b. grammatical errors result from both omissions and substitutions; c. free grammatical morphemes are only omitted, not substituted; d. bound grammatical morphemes are only substituted, not omitted; e. morpho-syntactic errors caused by substitutions are more frequent than those caused by omissions of grammatical morphemes; f. grammatical words are omitted less than content words; g. in substitutions, the replacing forms are existing grammatical morphemes, mainly belonging to the same grammatical category (e.g. one case ending substituting for another); h. the richer a category is in forms, the more it is liable to errors; i. there is a clear hierarchical order in the substitution of some grammatical forms for others. Both the child and the adult patient differ from the general tendency in (e) only. This difference may be caused by their type of aphasia (i.e. amnestic) because the general tendencies were investigated mainly in Broca's aphasics.

CONCLUSION To answer the question in the title: What is lost three and a half years after the accident is fluent writing and reading, smooth access to the whole lexicon and sensitivity to some more complicated grammatical features, especially to those with a formal, not semantic character. What is re-achieved after an almost hopeless state is the ability to use language for communication and reflection. The child's aphasia is basically manifested in the same way as the adult's aphasia with one exception: while the adult patient two years post-onset reached a

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stage after which her language skills no longer improved, the child has continued to develop her linguistic abilities.

ACKNOWLEDGEMENTS I am grateful to Dr. Eva Skodova and Dr. Jitka Stejskalova for allowing me to work with their patients and providing me with their documentation.

REFERENCES: Aram, D. M., B.L. Ekelman and S.A. Whitaker (1986). Spoken syntax in children with acquired unilateral hemisphere lesions. Brain Lang, 27, 75-100. Aram, D. M. (1988). Language sequelae of unilateral brain lesions in children. In: Language communication and the brain (F. Plum, ed.), pp. Raven Press, New York. Bishop, V. M. and L. B. Leonard. (2000). Speech and language impairments in children: causes, characteristics, intervention and outcome. Psychology Press, Hove. Dennis, M. and B. Kohn (1975). Comprehension of syntax in infantile hemiplegics after cerebral hemidecortication: Left hemisphere superiority. Brain Lang, 2, 472-482. Eisenson, J. (1972). Aphasia in children. Harper and Row, New York. Grodzinsky, Y., L.P. Shapiro and D. Swinney (2000). Language and the brain: representation and processing. Academic Press, San Diego. Jakobson, R. (1968). Child language, aphasia and phonological universals. Mouton, The Hague. Joanette, Y. and H. H. Brownell (1990). Discourse ability and brain damage: theoretical and empirical perspectives. Springer, New York. Leheckova, H. (1988). Linguistic theories and the interpretation of agrammatism. Clin Linguist Phon, 2, 271-289. Leheckova, H. (1997). Jazyk, komunikace a fecove poruchy. In: Afdzie (P. Kulistak, H. Leheckova, M. Mimrova and J. Nebudova, eds.) pp. 125-175. Triton, Praha. Leheckova, H. (2001). Manifestation of Aphasic Symptoms in Czech. Journal of Neurolinguistics, 14, 179-208. Lenneberg, E.H. (1967). Biological foundations of language. John Wiley and Sons, New York. Murdoch, B. E. (1990). Acquired neurological speech/language disorders in childhood. Taylor and Francis, London. Obler, L. K. and K. Gjerlow (1999). Language and the brain. Cambridge University Press, Cambridge.

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Paradis, M. (1989). Bilingual aphasia test. Czech version. Lawrence Erlbaum Associates, Inc., New Jersey. Pavao Martins, I., A. Castro-Caldas, H.R. Van Dongen, A. Van Hout (1991). Acquired Aphasia in Children. Martinus Nijhoff Publishers, Dordrecht. Van Hout, A. (1992). Acquired aphasias in children. In: Handbook in Neuropsychology (F. Boiler and J. Grafman, eds.), Volume 7, pp. 139-161. Elsevier, Amsterdam. Van Hout, A. (2000). An outline of acquired aphasia in children. Saggi CD&D, 26, 13-21.

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Persistent Acquired Childhood Aphasia

231

12

PERSISTENT ACQUIRED CHILDHOOD APHASIA Isabel Pavao Martins Universidade de Lisboa, Portugal

Abstract — It is recognized that acquired childhood aphasia has a favourable prognosis, but the longterm outcome of chronic cases is not known. Eleven patients are described (mean age = 17.5 years, + 5.2), who remained chronically aphasic for 2 or more years following a non-progressive brain lesion sustained in childhood (mean age at onset = 9.5 years). These patients belong to a series of 50 children with aphasia followed for an average of 6.9 years after lesion onset. Factors associated with persistent aphasia were traumatic or infectious etiology, poor verbal comprehension at onset, epilepsy and lesions involving the classical language areas of the left hemisphere. Six patients had mild forms of anomic aphasia, and the majority continued to improve their language test scores, changing their aphasic profile on consecutive evaluations and showing that recovery continues in the chronic period. In adult age these patients had educational, social and professional problems. Children who recovered were compared with a control group consisting of their healthy siblings of identical age. Recovered aphasics had significantly lower scores on short-term and working memory tests and also had educational difficulties. Our findings stress the need for rehabilitation and educational/professional support in the chronic stages of childhood aphasia.

Key words: acquired aphasia in children, recovery, prognosis, chronic aphasia in children.

232 Neurogenic Language Disorders in Children

INTRODUCTION Language is a well lateralized and localized function in the adult brain, and the study of acquired aphasia in children allows us to understand the development of its cerebral organization with time and cognitive development. In the last two decades, systematic studies of acquired aphasia in children have dismissed traditional beliefs about this disorder showing that: a) crossed aphasia is rare in children and, therefore, in normal circumstances language develops in the left hemisphere from the outset (Martins, 1997; Marien et al, 2001); b) all types of aphasia may affect children, namely fluent aphasia, jargon aphasia and disturbances of oral comprehension (Van Hout, 1986; Klein et al, 1992; Paquier et al, 1996; Van Dongen et al, 2001); c) positive aphasic symptoms may occur such as paraphasias, circumlocutions, conduites d'approche, preserverations, etc. (Van Hout et al, 1985); and d) anatomo-clinical correlations are identical to those found in adults, suggesting a modular developmental organization (Van Dongen et al, 1985; Cranberg et al, 1987; Martins & Ferro, 1992; Martins & Ferro, 1993; Nass et al, 1998; Van Dongen et al, 2001). The last evidence, however, is based on few studies. The most striking differences between child and adult acquired aphasia concern the high frequency of mutism and nonfluent types of speech in children (Basso & Scarpa, 1990; Van Hout, 1991; Martins, 1997), and prognosis, which is more favourable in young children. Although evidence of good recovery has been reported in a number of studies (Cranberg et al, 1987; Satz & Bullard-Bates, 1981; Loonen & Van Dongen, 1990; Martins & Ferro, 1992b), only few reports address the long-term outcome in these children. Some authors described subtle language sequelae and learning disabilities after apparent clinical recovery of acquired aphasia (Woods & Carey, 1979; Riva & Cazzaniga, 1986; Cooper & Flowers, 1987; Cranberg et al, 1987; Eisele & Aram, 1993), but only a few reported chronic aphasia. Watamori et al. (1990) described in detail three patients with acquired aphasia followed up into adult life. Three other studies (Cooper & Flowers, 1987; Basso & Scarpa, 1990; Lees, 1997) reported cases of permanent language sequelae of variable types and degrees, 2 or more years after acquired aphasia. These series includes patients with Landau-Kleffner syndrome, which is not a good model to study recovery as its underlying pathology may be progressive or fluctuating and thus interfere with the usual recovery mechanisms. The purpose of this report is to describe the long-tem outcome in adulthood of patients who suffered aphasia during childhood, focusing on those that did not recover. METHOD Population Children included in this study are part of a series of 120 children with acquired brain lesions referred to our Centre since 1979.

Persistent Acquired Childhood Aphasia

233

Inclusion criteria for the present study were: 1) lesion onset after some language development (minimum age was 18 months) and before 15 years of age; 2) documented diagnosis of acquired aphasia (with language testing) during the acute or chronic stage; 3) brain lesions due to non-progressive pathology; vascular, traumatic and infectious etiologies were included, but not patients with a diagnosis of tumor or Landau-Kleffner syndrome; 4) follow-up time longer than two years for children that did not recover. Procedure Clinical data concerning lesion onset, etiology, epilepsy, biographical, educational and social information were obtained from medical records and through an interview with parents. Children were assessed by a test battery including: 1) the Lisbon Aphasia battery (CastroCaldas, 1979) comprising an analysis of spontaneous speech features such as fluency, syntax, prosody, anomia, paraphasias and dysarthria; and tests of visual object naming, auditory comprehension and word and sentence repetition; 2) the aphasia severity rating scale from the Boston Diagnosis Aphasia Examination (Goodglass & Kaplan, 1983); 3) fluency grades from the Western Aphasia Battery (Kertesz, 1979); 4) a short version of the Token Test (De Renzi & Vignolo, 1962; Benton, 1969); 5) WAIS or WISC forward and backward digit span (Wechsler, 1949, 1970). Children younger than 6 years were also assessed by the Reynell Developmental Language Scales (Reynell, 1977). Children who recovered from aphasia and were more than 10 years of age, were also tested by a more extensive battery including the WAIS/WISC (Wechsler, 1949, 1970) and the Wechsler Memory Scale (Wechsler, 1969), among other tests, and are now being compared with the'ir healthy brothers or sisters in an on-going case-control study. Lesion localization was determined either by Computerized Tomography (CT) or brain Magnetic Resonance Imaging (MRI) and judged by two independent observers who were asked to verify the presence or absence of lesions in selected brain areas of the left hemisphere, according to brain maps (Matsui & Hirano, 1978; Damasio, 1995). Areas of interest included the classical language areas of the left hemisphere (Broca and Wernicke's areas), insula, superior temporal cortex (Brodmann areas 41, 42), supramargynal gyrus and angular gyrus (Brodmann areas 40 and 39). Extension of lesion in Wernicke's area was scored according to a 5-point scale: grade 0 = no lesion; 1 = lesion involving less than 25% of this area; 2 = 25-50% of Wernicke's area was damaged; 3 = 50-75% of area was involved; and 4 = more than 75% of the area was damaged. Since this study began before imaging studies were systematically performed, the number of imaging exams is lower than the number of children included. In the remaining cases, lesion side and localization were determined by clinical evaluation, angiography or surgery. Only CT and MRI data were analysed. Socio-economic status of patients who reached adult age (or their controls) was classified in 4 points, according to their occupation (or their spouses', if married): 1 - Unskilled manual

234 Neurogenic Language Disorders in Children

labour; 2 - Skilled manual work, 3 - Clerk or technical work and small trade, 4 Professionals, large trade or land owners. Operational criteria used to define recovery were the following: a) normal speech (concerning fluency, syntax, prosody, effort and articulation); b) normal performance on the four cardinal tests of the Lisbon battery (naming, repetition, fluency and auditory comprehension) or on both Reynell subscales; c) maximum score on the aphasia severity rating scale and, d) normal (age-adjusted) performance on the Token Test. A neurological examination was also performed to quantify motor impairment at the time of language assessment.

RESULTS Fifty children (27 girls and 23 boys) had sustained aphasia due to a static brain lesion. Their age at lesion onset was, on average, 8.7 (+3.9) years. Thirteen patients were preschoolers and 37 attended school, their school grade being on average 4.05 (+2.6) years. Lesion etiology was varied: vascular in 19 cases, traumatic in 23 and infectious in 8 cases. The lesion was localized unilaterally to the left hemisphere in 40 cases, bilateral in 6 and localized to the right hemisphere in 4 patients (including one left-handed child). Thirty-four (34) patients received the first neuropsychological evaluation in the first month, six (6) during the first six months and ten (10) after the 6th month. Children were re-evaluated and followed for variable periods of time, ranging from 6 months to 27 years (6.9 years on average): 39 (78%) patients recovered from aphasia, while 11 (22%) did not. Forty-two patients had imaging exams (CT scan in 30 cases and MRI in 12). Only left hemisphere lesions were compared between the two outcome groups. Prognostic factors. Children who recovered were not significantly different from those that did not recover in terms of (Tables 1 and 2) age at aphasia onset (8.4 years for those who recovered versus 9.5 years for those who remained aphasic [t = - 0.80, p=0.42, n.s.]), gender (X2= 0.41, p= n.s.), mean follow-up time (6.8 and 7.5 years, respectively [t=-.27, p= n.s.]), age at last evaluation (14.9 and 16.8 years, [t=-.82, p= n.s.]), school grade of school attenders (4.04 and 4.11 years, respectively [t=-.75, p= n.s.]), knowledge of reading and writing (preschoolers and first graders versus those mastering reading and writing [x2= 0.78, p= n.s.]), mutism during the acute period (yes or no [x2=-00, p= n.s]), or speech fluency at onset (fluent or nonfluent [x2 = 1.8, p=n.s.]). Lesion side (left, right or bilateral) was not different in the two outcome groups (x 2= 0.13, p= n.s.) neither was the occurrence of hemiparesis (x = .47, p= n.s.), change of handedness (yes or no [x =.36, p= n.s]), or convulsions during the acute stage (yes or no [x2=3.4, p= n.s.]).

Persistent Acquired Childhood Aphasia

235

Table 1 — Recovery from aphasia Aphasia Handedness recovery N R

Sex

L A M

Mean age Lesion side Follow-up Age at last at onset Left Right Bilat time evaluation mean (sd) F (yrs) (years) mean (sd) yrs

Yes

39 35

2

2

17 22

8.4(3.8)

31

3

5

6.8(7.5)

14.9(7.5)

No

11 11

0

0

6

5

9.5(4.2)

9

1

1

7.5(4.5)

16.8(4.4)

X2=41 p=n.s.

t=-.8O p=n.s.

t=- .27 p=n.s.

t=-.82 p=n.s.

X2=.13 p=n.s.

Note: R = right, L = left; A = hand preference undefined; M = male; F = female

Factors associated with persistent aphasia included impaired verbal auditory comprehension (simple verbal commands) in the acute stage (%2= 6.88, p=.008) and infectious or traumatic etiology, compared to stroke (x2=13.3, p=.001). Patients who later developed epilepsy (x =6.20, p=.01) had a worse outcome. Two children developed intractable epilepsy, being candidates for surgery: one boy was in the chronic aphasia group, while the other (with a left latero-temporal vascular malformation) was in the recovered group. Speech therapy was inversely related to outcome (x2=21.18, p<.000) since the majority of children who recovered were never referred to speech therapy, while chronic aphasics were. Thirty-four patients with demonstrable left hemisphere (unilateral left or bilateral) lesions were studied by imaging. There was a high agreement between two independent observers in terms of presence or absence of lesions in areas of interest of the left hemisphere (Cohen's kappa coefficient= 0.88). Lesions of the classical left language areas were associated with a poor outcome, that is damage to Broca's area (cortical and/or subcortical [x 2= 3.85, p=. 04]), superior temporal cortex (auditory cortex, BA 41,42 [x 2= 13.46, p= .0002]), Wernicke's area (cortical and or subcortical [x2= 14.24, p= .0002]), and the insula (y}= 15.9, p= .0001) (Table 3). In contrast, lesions involving the prefrontal or the parietal cortex (BA 39 and 40), and subcortical lesions (basal ganglia and subcortical white matter fiber tracts) were not associated with a worse outcome. The extension of lesion into Wernicke's area was associated with the outcome, being worse when lesions were more extensive [x = 29.9, p< .0000](see Table 3). Cases that did not recover. Eleven children (6 boys and 5 girls) (Table 4) remained chronically aphasic for 2 or more years after the lesion onset. Mean follow-up time was 7.5 (+ 4.5) years, ranging from 2 to 15 years. Six children had severe head injuries with depressed fractures, and five had infectious diseases of the CNS (cerebral malaria in one case, herpes encephalitis in three and tuberculous meningitis in one). All but two children (pre-schoolers)

236 Neurogenic Language Disorders in Children were attending school at the time of injury. Four children had persistent motor weakness mostly involving the right hand, and became left-handed. All eleven children walked independently at the last examination. Table 2 — Recovery from aphasia - Prognostic factors N Recove red Urn-eco1*/ered N=39 N=ll Etiology stroke 0 19 19 head trauma 6 X2=13.2 23 17 infection 8 3 5 p= .001 Mutism* yes 28 23 X2=.OO 5 no 11 9 p=n.s. 2 Speech fluency* 1 nonfluent 21 20 x2=1.80 fluent 16 8 p=n.s. 8 Auditory comprehension* normal 23 23 X2=6.88 0 poor 11 8 3 p=.008 Token Test score* normal X2=2.35 0 5 5 poor p=n.s. 33 22 11 Hemiparesis* 8 X2=0.47 yes 40 32 no p=n.s. 10 7 3 School grade at lesion onset Preschooler +lst grader X2=0.78 20 16 4 More than one year p=n.s. 7 30 23 Speech Therapy X2=21.18 yes 17 7 10 0 p< .0000 no 28 28 Chronic epilepsy X2=6.2 2 yes 3 1 5 no p=.O13 41 36 1 Results of the evaluation performed during the acute period

Persistent Acquired Childhood Aphasia

237

Table 3 — Recovery from aphasia - Damaged areas Area of interest Left hemisphere Prerolandic

Lesion ]Recovered Not recovered X2= 1.04

n.s.

Broca (cortical/ /subcortical) Insula

3.85

0.04

Temporal cortex (areas 41, 42) Wernicke's area (cortical/subcortical) Parietal cortex (BA 39, 40) Caudate nucleus Lenticular nucleus internal capsule

yes no yes no yes no yes no yes no yes no yes no yes no

8 20 3 24 3 24 4 23 6 21 11 16 4 23 10 17

3 3 3 4 6 1 6 1 7 0 5 2 1 6 1 6

p=

15.9 0.0001 13.46 0.0002 14.24 0.0002 2.1

n.s.

0.00

n.s.

1.31

n.s.

Extent of lesion in Wernicke's area No lesion Lesion < 25% Lesion 25-50% Lesion 50-75% Lesion>75%

21 5 1 0 0

0 0 2 2 3

29.92 0.0000

Nine patients were studied by imaging (MRI in four, CT scan in five cases). One child (patient 10) had an extensive contusion of the right temporal lobe (including both the hippocampus and the neocortex) and no visible lesions of the left hemisphere on MRI. However, and due to its traumatic etiology, this case cannot be considered a crossed aphasia case since traumatic lesions may be unapparent on imaging. All other patients had left hemisphere lesions involving the temporal cortex (areas 41 and 42), Wernicke's area and additional lesions of the insula and Broca's area in some cases. In 6 patients BA 39 and 40 were also damaged (Table 5).

238 Neurogenic Language Disorders in Children Table 4 — Chronic Aphasics: clinical data and follow-up N Sex

Age at Etiology Chronic Change in Epilepsy 1esion onse:t Hemiparesis laterality* 1 M yes(hand) 8.2 Cerebral malaria yes(L) yes 2 M 8.6 no Herpes encephalitis no yes** 3 F 13.7 no Herpes encephalitis no no 4 M 14 no no Herpes encephalitis no Tuberculous 11 5 F meningitis yes(hand) yes(L) no HT + 6 M 12 no Parietal DF no no HT+DF+ 7 F 6.7 FTP contusion no no no HT+ DF+TP 8 M 15.4 yes(hand) contusion yes(L) no HT+DF+ 9 F 1.5 no no T contusion no Closed HT+ 10 F 5.7 RT contusion no no no HT+DF+ 11 M 7.7 yes (hand) yes(L) FP contusion no N Ileturn to Special Repeated Final Follow-up Final age school education grade grade (years) (years) 1 11 1 yes yes yes 19 2 20 9 12 yes yes 8 5 18 3 yes 3 no 4 7 3.3 17 no 5 2 12.6 yes 5 yes yes 4 8 20 no 6 1 22 7 15 yes yes yes 4 4 8 20 no 2 7.7 8.9 9 no yes no 6 12 17 yes 10 yes yes 11 10.2 9 2.3 yes yes yes

Note: *present handedness in brackets; ** intractable epilepsy, requiring surgery Evolution of chronic aphasia. Although these eleven patients remained aphasic two or more years after lesion onset, their aphasic profile, aphasia severity and taxonomic diagnosis continued to change in the chronic period (Table 6). For instance, patient 6 changed from Broca's to conduction aphasia (improving fluency) more than 5 years after lesion onset.

Persistent Acquired Childhood Aphasia

239

Another patient (case 9) evolved from transcortical sensory aphasia to anomic aphasia more than three years after onset and patient 7 was still improving after more than ten years. Her diagnosis evolved from conduction aphasia to anomic aphasia. Table 5 - Unrecovered patients-lesion localization in the left hemisphere

Imaging lesionPre-ro Exam

N

Temporal Wernicke's area Lesion

side landicBrocalnsula Cortex cortex

1 CT/MRI 2 CT/MRI

L L

3

CT

L

4

CT

L

5 CT/MRI Bilat

+ -

+ -

-

(BA 22)

BA 41,42 B/W + -

+

-

+

+

+

+

+

+

+

+

+

+

+

+

4 +

+

+

+

3

+

+

+

2

-

+

+

4

+

+

CT

L

+

+

+

+

+

+

8

no

L

9

no

L .

.

+

+

+

+

+

L

+

+ 4 -

7

R

4

+

+

2

-

CT

+

+

+

+

11

3

+

L

10* CT/MRI

gyrus marginal

+

CT

+

+ -

6

+

supra

W Sc Wernicke (BA 39) (BA40)

-

+ +

Ext.

angular

. +

0

CT=Computerized Tomography; MRI-Magnetic Resonance Imaging R=right hemisphere*, L=left hemisphere, Bilat=bilateral BA=Brodmann area; + lesion involving that area; -no lesion Changes were observed in all aspects of language abilities, namely visual naming, word repetition, auditory comprehension of simple verbal commands and speech fluency scales often switching from non-fluent to fluent types of speech (Table 7). On the last evaluation, most children (6/11) had mild forms of anomic aphasia. Language scores declined in only one patient. This was related to the development of an intractable epilepsy requiring surgery. School achievement. Although these children had mild aphasic syndromes, three of them never returned to school. Five of them attended special education classes. All but one (the younger child at lesion onset) repeated grades and eventually left school (Table 4). Socio-professional achievement. By the time the last evaluation was performed, 9 patients had reached adult age (> 18 years of age) (Table 8). Four were unemployed, often after trying several jobs. Two patients (cases 6 and 7) specifically mentioned that they were unable to keep their jobs because of their inability to maintain a conversation with clients (while working as a salesman in a shop and helping in a hairdressers', respectively). Patient 6 was now working on a voluntary basis (being unpaid) in a garage, helping to load and unload materials. Others complained of reading or writing difficulties

as their main handicap for

240 Neurogenic Language Disorders in Children work. Only three subjects were still studying (in two cases, special education classes). Although four had a paresis of the right upper limb, involving the hand, none of them mentioned it as a cause for their professional or school difficulties. Compared to their parents, these young adults had a lower socio-economic status. Most had brothers or sisters who were still studying. Only one patient was economically independent, all others depended upon their parents or spouses. Table 6 — Chronic aphasic patients - Type and Severity of Aphasia: changes at follow-up

N

First

1-6

month

months

1 2 4

W

3 1

Ts

4

5

4 4

Ts

W Ts

Time Post-onset 6-12 1-3

5-10

4-5

>10

years years years months years 1 B 2 Tm 2 Tm 0 G 0 G 1 Tm 5 A 5 Ts 5 A 5 A 2

Ts

4

A

4

A

4

A

1

B

1

B

4

A

4

A

6

5

B

5

B

5

C

7

4

C

4

C

4

A

5

A

5

8 1

G

9 10 11 0 Mutism 0

G

4

Tm

2

G

1

G

1

G

3

Ts

4

A

4

A

4

A

4

Tm

Note: T= transcortical aphasia; Tm = Transcortical motor aphasia; Ts = Transcortical sensory aphasia; G = global aphasia; A = anomic aphasia; C = conduction aphasia; B = Broca's aphasia; W = Wemicke's aphasia. Numbers represent severity of aphasia by the Boston Diagnosis Aphasia Examination (Maximum =5)

Persistent Acquired Childhood Aphasia

241

Two patients developed epilepsy. In one case (patient 2) it was a chronic intractable epilepsy requiring surgery (left anterior temporal lobectomy) which did not lead to any consistent improvement. Another patient (patient 1) developed epilepsy when he was 17 years old but easily controlled it with sodium valproate. Family life. Only the three female patients in this adult group got married and had children. Since they did not work, they were economically dependent on their husbands or parents. All the male patients continued to live with their parents, were economically dependent and did not establish new stable emotional relationships. Table 7 — Performances of chronic aphasics on Naming, Word Repetition, Verbal Comprehension, Speech Fluency (changes at follow-up) Naming Performance 1 to 6 6-12 1 to 3 4 to 5 5 to 10 >10yrs months months years years years 1 7 0 0 3 6 2 0 11 12 11 14 13 3 0 11 3 9 4 0 9 10 14 5 0 0 6 15 15 15 7 13 13 13 8 0 0 0 9 12 13 10 10 10 15 13 16 11 0 14 8 Maximum score = 16 Word Repetition Test 1 month 1 to 6 6-12 1 to 3 4 to 5 5tol0 >10yrs months months years years years 1 28 30 21 0 0 2 20 30 30 30 30 30 28 3 30 30 30 4 11 30 29 30 5 0 15 6 27 26 25 24 26 7 22 0 2 8 0 9 29 30 30 10 30 30 30 30 11 0 15 28 1 month

Maximum score = 30

242 Neurogenic Language Disorders in Children

N

1 month

1 2

5

3

1

4

Ve rbal comiprehensiian 1 to 4 to 5 3 1 to 6, 6-12 5 tolO nnonths month,s years years years 7 6 7 8 7 8 7.5 8 6.5

5

3.5

7

7.5

8

8

8

>10 yrs 6 8

7 8

6

8

8

8

7

7.5

8

8

6 5.5 8

8

8

8

3.5

2

9 8

10 11

3

5

8 8

8

Maximum score = 8

N

1 2 3 4 5 6 7 8 9 10 11

Speech fluency lto 4 to 5 3 5 1 tof> 6-12 tolO rnonths months years years years Mutism NFO NFO NF3 NF4 FL 3 FL5 FL5 FL5 FL4 FL 3 FL3 FL3 FL3 FL4 F14 FL4 FL3 NF3 NF3 NF5 NF5 FL4 FL4 NF 0 NF1 NF1 FL4 FL4 NF5 NF5 FL5 NF3 NF5 NFO

1 month

>10 yrs NF4 FL5

FL4 FL4 FL4 FL5

NF= non fluent; FL= Fluent. Figures represent fluency grades (from the Western Aphasia Battery ranging from 0 to 5 in either scale, fluent and nonfluent) at different follow-up times. Note: Numbers represent raw scores obtained at different follow-up times.

Recovered Cases. Thirty-nine children (17 boys and 22 girls) recovered from aphasia. The majority (19 cases) had vascular lesions, but there were also traumatic (17) and infectious cases (3). At the time of the last evaluation their age was, on average, 14.9 years (+ 7.5).

Persistent Acquired Childhood Aphasia

243

To understand their cognitive and educational achievement, those children were compared with their healthy siblings of identical age in a case-control study: 16.8 years (+ 5.5) in patients and 16.6 years (+4.5) in controls. Table 8 — Chronic aphasics - Evaluation in adult age ( age > 18 years)

Pt N

folio hand w-up ed time ness

19

11

L

RHemi paresis

Yes

Job or Occupation special education gardening

2*

20

12

R

no

Yes

3

18

5

R

no

yes

4

18

3.3

R

no

yes

yes

1

Age

motor defect

Independent Walking

5

23**

13

R

R Upper limb paresis

6

20

8

R

no

7

22

15

R

no

8

20

5

L

R Upper limb paresis R Upper limb paresis

SES economic pati pare dependen cy ent nts

1

yes

unemployed

3

yes

student unskilled work

4

yes

2

no

lives with mother lives with mother married one child lives with parents

1

yes

married one child

1

yes

unemployed voluntary manual job unpaid

1

3

yes

yes

unemployed

1

2

yes

lives with an aunt married pregnant lives with husband

yes

unemployed

yes

lives with parents

yes

lives with parents

special education

18** Pt= patient, L=left, R right; Figures represent socio-economic status, estimated from jobs or from spouses' occupation *intractable epilepsy, submitted to epilepsy surgery ** information obtained at present from clinical records and by telephone interview 11

10

L

Family Life

yes

3

244 Neurogenic Language Disorders in Children An analysis of the first eleven patient-control pairs has shown that: a) There are no significant differences between the two groups concerning verbal IQ (patients: VIQ = 96.2, controls: VIQ= 106.2 [paired t test = -1.4, p = n.s.]), performance IQ (patients: PIQ = 100.8, controls: PIQ = 111.3 [paired t = -0.6, p = n.s.]) or full scale IQ (patients: FIQ= 97.6, controls: FIQ=109.4 [paired t = -1.4, p = n.s.]) neither on Wechsler verbal episodic memory subtests, logic memory (patients = 9.3, controls = 11.8 [paired t= -.91, p= n.s.]), word pair associates (patients = 16.3, controls = 17.9 [paired t= -1.6, p=n.s.]) or visual memory (patients = 12.0, controls = 14.3 [paired t= -.91, p= n.s.]), although controls had higher average scores on all tests. b) Ex-aphasics have significantly lower scores in forward and backward digit span (patients' average = 8.2, controls' average =12.5 [paired t= -6.14, pO.OOO, df =9]). c) Although patients had a poor school achievement, they did not differ significantly from controls in grade repetitions (average number of grade repetitions of patients was 1.5 versus 1.0 of controls) (excluding the year of illness or missing school because of illness) or final school grade. DISCUSSION Focal brain lesions in childhood are associated with a favourable prognosis for language recover}' and subsequent development, as demonstrated in several longitudinal studies of children with congenital or perinatal lesions of the left cerebral hemisphere (Eisele & Aram, 1993; Bates et al, 1999; Vargha-Khadem et al, 1994; Trauner et al, 2001), acquired aphasia (Cranberg et al, 1987; Loonen et al, 1990; Satz , 1981; Martins & Ferro, 1992b), and also by the follow-up of patients with left hemispherectomy (Dennis & Whitaker, 1976; Ogden, 1988; Vargha-Kadhem et al, 1991; Devlin et al, 2003). These studies have shown that patients with left hemisphere damage have a nearly normal development of language, although a finegrain analysis of their linguistic abilities may reveal subtle defects. This indicates a remarkable plasticity of the developing brain for functional re-organization as well as language resilience after brain lesions. The present study suggests that plasticity declines after language acquisition. While almost 80% of children recovered - a higher percentage than the one reported in adult patients - this outcome is worse than when lesions occur before language acquisition, where clinical aphasia is unusual. Of 50 children who developed aphasia between the ages of 1.5 and 15 years, 11 (22%) remained chronically aphasic after a long follow-up. However, age was not a significant factor for prognosis in this particular group. Indeed, it was found that lesionrelated variables (site and nature, late epilepsy) but not subject-related variables (age, gender, grade of education) were the main factors responsible for the outcome. This corroborates results from a previous research on a smaller sample of patients (Martins & Ferro, 1992b) and studies of adult aphasia (Basso, 1992) suggesting that individual variables cannot compensate for the degree and type of structural damage. This study also showed that albeit mild, child or

Persistent Acquired Childhood Aphasia

245

adolescent chronic aphasia has an impact on the educational, socio-professional and family life, just as would be expected in adults. Regarding recovery, there are two main differences between these findings and findings related to adult aphasics. First, unlike adults, the overall recovery was better in children and, secondly, children improved in the chronic period. In different series of stroke patients, recovery rates of adult aphasia vary between 40 and 50% (Kertesz, 2002). In the present study, all vascular cases recovered completely, even when lesions were localized bilaterally. The same advantage for children compared to adults was found by Bates et al. (2001) in a direct comparison of language abilities in patients with left hemisphere lesions sustained in the perinatal period or during adulthood. However, besides the brain plasticity hypothesis, other factors may account for a better recovery, namely the specific topography and pathogenesis of stroke in young children (Ganesan et al, 2003). Regarding the other two etiologies, traumatic aphasia in general has a better prognosis than stroke (Basso, 1992), but the outcome of head injury and CNS infections depends upon multiple factors (type and severity of injury, infectious agent, etc.), and differences between children and adults are more disputable (Basso & Scarpa, 1990). Another difference between child and adult aphasics, was the timing of recovery. Curves of aphasia recovery in adults (again, mostly stroke patients) have shown that the greatest improvement is seen in the first 3 months (especially in the first three weeks) (Hartman, 1981). There may be some recovery during the first year (Basso, 1992), but afterwards there are no significant changes, and functional decline has occasionally been reported (Hanson, 1989). Although children who recovered did so during the first year, in our group of chronic aphasics improvement of different language abilities was found not only after the first year, but also 5 or more years after lesion onset, causing changes in the aphasic profile and taxonomic diagnosis. Unusual patterns of recovery and long periods of aphasia improvement in children have also been described by other authors (Watamori et al., 1990; Ogden, 1988; Ikeda et al, 1993). It is difficult to attribute these changes to simple developmental progression as some of these patients were already in the adult age. The long follow-up period of children may explain some of this advantage, since adults are not usually followed for so long. Recovery mechanisms are different during the acute and chronic stages of brain damage. During the first weeks after stroke, for instance, functional improvement is associated with reversal of diachisis and ischemic penumbra, and better perfusion after volume reabsorption (Ferro et al, 1999). During the chronic period, on the other hand, recovery depends upon four basic forms of neuroplasticity (Grafman & Litvan, 1999), some of which have been demonstrated in children with left hemisphere lesions. These mechanisms are: 1) Language transfer to the homologous areas of the right hemisphere following cortical lesions in childhood (especially associated with epilepsy) which explains recovery after left hemispherectomy. This has been demonstrated by fMRI (Hertz-Pannier et al, 2002; Staudt et al, 2002), electrical stimulation (Duchowny, 1996) and Wada testing (Miller et al, 2003). 2)

246 Neurogenic Language Disorders in Children

Map expansion, i.e. the use of neighbouring areas to perform the same function. This was shown for language recovery (De Vos et al, 1995) and might be facilitated in childhood because normal children activate more extensive neuronal networks than adults, while performing verbal tasks (Gaillard et al, 2000), thus, naturally using "neighbouring" areas. 3) Compensatory masquerade. This mechanism has been suggested by Stiles-Davis et al. (1988) in children with right hemisphere damage who, although fully recovered, had difficulty performing non-canonical drawing tasks, which suggested a rigid pattern of performance. 4) Cross-modal reassignment, which is more often observed after congenital sensory deprivation. The lack of recovery in our 11 patients compared to those that recovered suggests that lesions may have hampered some of these possible recovery mechanisms. Infectious and traumatic lesions may cause bilateral hemispheric damage, even if not visible on imaging exams. This could interfere with homologous area transfer. The extensive, or cumulative, destruction of the left hemisphere language areas may have impaired map expansion. There are some indications that the left temporal cortex may be particularly vulnerable to persistent functional impairment. Left temporal lobe lesions have been associated with a worse outcome even in congenital lesions. According to Bates et al. (1999), "this pattern is more evident during the early stages of language acquisition". In our patients, the lesion extension in Wernicke's area was a negative factor as was a poor verbal comprehension in the acute stage, a symptom of left temporal involvement. This area may be of particular importance either because of its aptitude to handle "perceptual detail" (Bates et al, 1999) or because it is one of the first areas to commit to language, as demonstrated by fMRI in infants (Elman et al, 1996). This early commitment and eventual automatization of function, may enhance its innate cytoarchitectonic aptitude to process speech sounds, reduce its representation and make it difficult to transfer this function to neighbouring areas. However, the continuing recovery of function in the chronic period, observed in these patients, suggests that plasticity phenomena, possible behavioural compensation or compensatory masquerade, are still taking place many years after injury, at least in the child and adolescent brain. They may be sensitive to rehabilitation mesures. Differences between congenital left hemisphere lesions and the cases just described suggest that language acquisition may impair functional re-organization. These differences support the theory of computational nativism [60] in the sense that the progressive commitment of an area to a function may transform a small computational difference into a major bias for functional processing to the point of no return. The observed language impairment was sufficient to cause educational and socioprofessional handicaps. It is well-known that adult aphasia is associated with poor professional and social adjustment, poor quality of life, depression and social impairment. In this respect, these children were not different from adult aphasics, although their aphasic syndrome was relatively mild as were their motor impairments, and only one had refractory epilepsy. Children failed or left school. In adult age, they were economically dependent and

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247

most of them did not live on their own nor had a family. This stresses the specific educational needs of these patients. However, it is important to note that behavioural difficulties are common not only to children with trauma but also after stroke (Blom et al, 2003), independently of aphasia, and this may have an additional impact on the outcome that was not specifically sought. Although this is a very small sample, it is striking that women had an advantage concerning family life compared to men, which may be related to the traditional gender effect on social roles. These women were not impaired in social or family life but, as they were unemployed, they were just as handicapped as men. Men are expected to support the family, economically. However, we acknowledge that we need more information from the control group to understand this data. Children who recovered from aphasia might also have specific educational and professional needs. Compared with the control group, they had lower scores on measures of IQ and long-term verbal memory and visual memory. These differences reached statistical significance on the phonological/working memory tests, which may underlie some of their school difficulties often described as sequelae of acquired aphasia. Although these are preliminary data, they stress the educational needs of recovered patients.

CONCLUSION The prognosis of acquired childhood aphasia secondary to static brain lesions is generally favourable, with a higher rate of recovery than in adults. Yet, language recovery is less complete than that reported after congenital lesions, suggesting a reduced plasticity during the first years of life. In a subset of patients, recovery is partial, even after long periods of followup. Impaired verbal comprehension of simple verbal commands and lesion etiology and localization are prognostic indicators. Although chronic aphasics tend to have mild forms of aphasia and their linguistic abilities may continue to improve in the chronic stage, persistent aphasia has a negative impact on their educational, social and professional life.

ACKOWLEDGMENTS The author is indebted to Professor Jose Ferro, MD, for his help in the analysis of the imaging exams and wishes to thank Drs. Alexandra Reis and Susana Rodrigues who participated in the evaluation of controls.

248 Neurogenic Language Disorders in Children

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INDEX acquired aphasias 26, 27-8, 182-3 acquired aphasia in children 232-3 acquired childhood aphasia 148, 150-2, 160-7 acquired speech and language dysfunction 40-3 autism 29-30 brain imaging 15-16 brain 112-20 cerebellar aplasia 129-30 cerebellar malformations 128-9 cerebellum 88-90, 128 child aphasia 200, 225-6 childhood epilepsy 10-11,15,16 children 112-20, 182-3 chronic aphasia in children 238–4 congenital aphasia 68-9 Continuous Spike-Waves during Slow Sleep (CSWS) 26, 28-9 crossed aphasia 148-9, 152-3, 156-60 Czech aphasic symptoms 203-9 development dysphasia

80

early brain lesion 66-8 Electrical Status Epilepticus during Slow-Wave Sleep 26, 28-9 epilepsy 28-9,43–4

focal lesions 53-4 Fused Dichotic Words Test hemispheric lateralization

54-5 58-9

Landau-Kleffner Syndrome (LKS) 10, 13-15, 17-18, 27-8, 72, 74, 80-1 language development 57-8, 133–4, 136, 137, 138 language disorders 26 language dominance 165-7 language 13, 104 long-term recovery 203-20 NREM sleep

70, 75, 78, 80, 82

Operculum syndrome

38

paroxysmal abnormalities 71, 73, 82 pathophysiology 15-19 phonological processing deficits 44 phonological short-term memory 14-15 po sterior fo s sa 88-90 prognosis 234-5 recovery 191, 235-7, 242-4, 245-6 regression 29-30 tumor

112-20,192

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