Neurological and MRI profiles of children with developmental language impairment
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1 Neurological and MRI profiles of children with developmental language impairment Doris Trauner* MD, Departments of Neurosciences and Pediatrics, University of California, San Diego School of Medicine; Beverly Wulfeck PhD, Department of Communication Disorders, San Diego State University, San Diego, CA; Paula Tallal PhD, Center for Molecular and Behavioral Neuroscience, Rutgers University, Newark, NJ; John Hesselink MD, Department of Radiology, University of California, San Diego School of Medicine, La Jolla, CA, USA. *Correspondence to first author at University of California, San Diego School of Medicine, 9500 Gilman Drive, La Jolla, CA , USA. Children with developmental language impairment (LI) are defined partly by the absence of other identifiable neurological diagnoses. Such children are generally considered to be neurologically normal, but no systematic studies of neurological function have been reported. We obtained detailed medical histories and conducted neurological examinations for 72 children aged 5 to 14 years with LI and 82 typically developing age-matched control children. All the children took a standardized test of language, and those who were at least 8 years old and were willing to have brain MRI scans (35 children with LI and 27 control children) had scans. Analysis of developmental milestones from the medical histories revealed that children with LI were not only significantly later in speaking, but also mildly but significantly delayed in motor milestones, particularly walking. On neurological examination, abnormalities were found in 70% of the children with LI and only 22% of the control children. The most common abnormalities in the LI group included obligatory synkinesis, fine motor impairments, and hyperreflexia. The children with LI with the most abnormal neurological findings had the lowest language scores. Finally, 12 of 35 children with LI had abnormalities on their MRI scan, while none of the 27 control children had abnormal scans. Abnormal findings included ventricular enlargement (in five), central volume loss (in three), and white matter abnormalities (in four). These findings suggest that developmental LI is not an isolated finding but is indicative of more widespread nervous system dysfunction. Children with LI may need more comprehensive intervention programs than language therapy alone, depending on their other areas of dysfunction. Early identification of such problems may allow for more successful remediation. Developmental disorders of language (language impairment; LI) are behaviorally defined conditions in which specific higher cortical functions in the brain are impaired (Tager-Flusberg and Cooper 2000). Children with this diagnosis are defined by a delay or abnormality in expressive and/or receptive language skills in the absence of global cognitive disability, autism, hearing loss, primary social or emotional problems, or severe environmental deprivation. For several decades, researchers have sought to understand why these children experience significant difficulties in language. Research has focused mainly on the languagespecific nature of the disorder. Initial studies of children with LI were motivated by models of LI and related these to deficits in the acquisition of language knowledge (Johnston and Kamhi 1984). More recently, studies have focused on a range of domains including pragmatics and/or social cognition (Rapin and Allen 1983, Johnston 1988, Leslie and Frith 1988), lexical semantics (Schwartz and Leonard 1985), and morphosyntax (Curtiss and Tallal 1991, Gopnik and Crago 1991, Leonard 1992). Some of these studies have shown that in younger children the performance of language in agematched controls is similar to that of the children with LI, suggesting that the language-learning system is essentially intact in LI and that delay rather than deviancy best characterizes LI in the early years. Studies have also shown that deficits of language, especially morphosyntax, extend well into the school years as children with LI face new challenges in learning and literacy (see Bird et al. 1995). Although past research has resulted in detailed characterizations of the language profiles of children with LI, little attention has been paid to their neurological status. Generally, it was assumed that they had no frank neurological impairment; however, few or no direct data were obtained to confirm normal neurodevelopment. A few reports have suggested evidence of neurological dysfunction in children with LI. Sheridan. (1973) reported an association of clumsiness with severe language delay. Johnston et al. (1981) identified an association between what are sometimes called soft neurological signs (rate of movements, left right identification, ability to perform rapid alternating movements of the fingers and hands) and children with LI. Tallal et al. (1989a), using information from the Achenbach Child Behavior Checklist (Achenbach and Edlebrock 1983), found that indicators of neurodevelopmental dysfunction were present in a group of children with LI. Gillberg and colleagues (Kadesjo and Gillberg 1998, Landgren et al. 1998), using a populationbased approach to the study of neurodevelopmental disorders, identified a cooccurrence of language problems in approximately two-thirds of children who had deficits in attention, motor control, and perception (DAMP). The nature of the language problems was not sufficiently clear to determine whether these children would meet the criteria of most researchers for specific LI. Several studies have investigated the association between toe-walking and language disorders. Accardo and Whitman (1989) found that approximately one-third of children referred for possible developmental disorders walked on their toes. Language delays were associated with toe-walking in their study, and there was a direct correlation between the severity of the LI and the likelihood of toe-walking. Shulman et al. (1997) approached the question of toe-walking and LI by evaluating a group of young children (under 7 years of 470 Developmental Medicine & Child Neurology 2000, 42:
2 age) referred to an orthopedic clinic for idiopathic toewalking. A strong association between toe-walking and the presence of language delays was found. Their population of children also had a high incidence of gross motor, fine motor, and/or visual motor delays. These studies thus contribute to the information on the association of soft neurological signs with LI in young children. Tuchman et al. (1991) reported on neurological findings in 236 preschool-age children with LI. Using specific criteria for designation of abnormal sensorimotor examinations, they found that 10% of the children with dysphasia had abnormal sensorimotor findings. The most common such finding was hypotonia, found in 5%. Other hard motor abnormalities included spastic diplegia in 3%; hemiparesis in 2%; and ataxia in 1%. Neuroimaging studies of children with LI are rare. In one study of 20 children with LI and 12 control children, there was no evidence of gross structural abnormalities in either group (Jernigan et al. 1991). However, quantitative morphometric analyses of MRIs in LI did identify some differences, including a smaller volume of the left posterior perisylvian region in the children with LI than in the control children. Another quantitative MRI study in boys with specific LI (Plante et al. 1991) identified atypical asymmetries in perisylvian volumes (either right = left or right > left) in six of eight individuals with LI and only two of eight control children, suggesting that the normal course of brain development may be altered in conditions associated with specific LI. A single case report of a child with LI who had bilateral changes in the caudate nuclei (Tallal et al. 1994) suggests that further studies of brain structure in this group might be warranted. If brain development is aberrant in LI, we would predict that the changes must be bilateral or multifocal, based on studies of children with unilateral brain damage. In contrast to the persistent language deficits that are found even in school-age children with LI, studies of narratives in similarly aged children who had suffered early unilateral brain injury (from strokes or bleeds) reveal performance within the normal range on measures of grammar and sentence structure (Reilly et al. 1998). These findings have led us and others (Bates 1997) to begin exploring factors that might explain why children with LI have poorer language performance than children with frank neurological lesions. A better understanding of the neurological status of children with LI can not only inform our models of LI but also contribute more broadly to our understanding of neurodevelopment and brain plasticity. As part of a large, interdisciplinary research project on language and learning in children, we conducted neurological evaluations of school-age children with LI and age-matched control children. MRI scans of the brain were performed on a subset of children in each group, and neurological and MRI findings were compared with language scores to determine whether neurological abnormalities aside from the LI were a consistent part of LI. Method PARTICIPANTS Seventy-two school-age children with LI (25 girls and 47 boys; age range 5 to 14 years) and 82 age-matched control children (47 girls and 35 boys) participated in the study. A diagnosis of LI was based on the presence of receptive and/or expressive language scores greater than 1.5 standard deviations below the mean on the Clinical Evaluation of Language Fundamentals Revised (CELF-R) or similar test; normal nonverbal IQ; and the absence of hearing loss, primary social or emotional problems, environmental deprivation, autism, or other specific neurological diagnoses. Control children were typically developing children who had normal IQs and normal language scores on standardized tests. They were not specifically matched to the children with LI. Informed consent was obtained for each participant before testing, in accordance with Institutional Review Board procedures. Children were recruited from a variety of sources. Potential participants with LI were recruited from contacts with speech pathologists, resource teachers, psychologists, pediatric neurologists, pediatricians, and advertisements in parents magazines and local newspapers. Control children were recruited from local schools, physicians offices, and through advertisements in newspapers and parents magazines. Once the children were referred to the study, they underwent screening testing with language and intelligence measures to determine whether they met the criteria. This was true for both children with LI and control children. If they had been tested for other reasons (e.g. academic placement) within a year of the referral, we used the scores from the outside testing rather than retesting the children. Twenty-seven of the control children and 35 of the children with LI had MRI brain scans. These children were not chosen for any specific reason except age and willingness to undergo an MRI scan: as sedation was not used, only children older than 8 years were asked to participate. Because most of the children who were scanned were enrolled in the early years of the study, not all children 8 years and older received MRI scans. Scans were performed at the University of California, San Diego Medical Center MRI unit using a GE 1.5-tesla unit. All scans were interpreted by a neuroradiologist (JH) who was unaware of the child s language or neurological status. MEASURES A standard medical/developmental history questionnaire was completed by a parent or guardian for each child. This included questions relating to the mother s pregnancy, the child s delivery, motor and language milestones, medications, treatment interventions, other illnesses, and family history. Parents were encouraged, but not required, to use baby books and other records for information when these were available. Each child was given a neurological examination by an experienced clinical pediatric neurologist. A standard examination, modified from that of Rapin (personal communication), was completed for all study participants. Gross, fine, and oromotor skills, muscle tone and strength, reflexes, cerebellar functions, sensory functions, and gait were examined and scored as normal (0), mildly abnormal (1), or moderately to severely abnormal (2) for age. These included tests for soft neurological signs, e.g. synkinesis or mirror movements of the hands, clumsiness, inability to hop or skip, and other non-focal findings. The same scoring system was used for all study participants. The CELF-R (Semel 1987) was administered to each child. This comprehensive language battery is designed to identify individuals aged between 6 and 21 years. Norms, including Neurological and MRI Abnormalities in Language Impairment Doris Trauner et al. 471
3 standard scores, centile ranks, and age-equivalents, are available for each subtest. A Receptive Language score can be obtained using the subtests Linguistic Concepts, Sentence Structure, Oral Directions, Word Classes, and Semantic Relationships. An Expressive Language score can be obtained using the subtests Word Structure, Formulated Sentences, Recalling Sentences, and Sentence Assembly. Supplementary language areas may be assessed using the subtests Listening to Paragraphs, and Word Associations. STATISTICAL ANALYSES Independent t tests were used to compare the LI and control groups on motor and language milestones and language scores. The Wilcoxon signed rank test was used to assess the differences in neurological findings between LI and control groups. Results FAMILY HISTORY On the medical history questionnaire, parents of 54% (39 of 72) of the children with LI reported a positive family history of speech or language problems, specific learning disabilities, and/or attention-deficit disorder. Only 18% (15 of 82) of the control children reported a positive family history of the same conditions (χ 2 =9.24; p<0.001). MILESTONES As expected, the group with LI was much slower than the control children in developing expressive language, as evidenced by their significantly later acquisition of first word use and word combinations (Table I). However, there was also a mild but statistically significant delay in acquisition of motor skills, especially for walking, in the LI group than in the control children (Table I). RELATION BETWEEN CELF-R SCORES AND NEUROLOGICAL FINDINGS There were no significant differences in CELF-R Expressive, Receptive, or Total Language scores between the LI group with normal (Expressive 65.3 [SD 9.4], Receptive 72.9 [10.5], Total 67.8 [8.9]) and those with mildly abnormal neurological examinations (Expressive 63.8 [9.1], Receptive 73.4 [12.1], Total 66.6 [9.6]). However, Expressive and Total Language scores were significantly lower in children with LI who had moderately abnormal neurological findings (Expressive 56.7 [6.8], p=0.03; Receptive 68.3 [10.2]; Total 60.4 [7.1], p=0.05) than in those with normal examinations (Fig. 1). MRI FINDINGS Twelve (34%) of the 35 children with LI had abnormalities noted on MRI scans. None of the 27 control children was deemed to have abnormal scans (three control children had a single, small, punctate hyperintensity in the white matter, but the neuroradiologist did not consider this significant). Types of abnormalities found on MRI scans are listed in Table III. In almost all children, the observed abnormalities were in the white matter (see Figs 2 and 3 for examples). MRI AND NEUROLOGICAL FINDINGS Ten of the 12 children with abnormal MRI scans also had abnormal neurological examinations. Eight of these 10 were rated as moderately abnormal, and two were rated as mildly abnormal. Seventeen of the 23 children with LI with normal MRI scans also had abnormal neurological examinations. Twelve of these 17 children had moderately abnormal findings and five had mildly abnormal findings on neurological examination. Thus, there did not appear to be any greater likelihood of neurological abnormalities if the child had an abnormal MRI scan than if the scan was normal. NEUROLOGICAL FINDINGS A significantly higher percentage of children with LI than of control children had abnormal neurological examinations. Only 29.6% of the children with LI had normal neurological examinations, compared with 78% of the control children (χ 2 =36.8, p<0.001). One-third of children with LI had mildly abnormal exams and 42.3% had moderately abnormal exams, compared with 19.5% and 2% of control children, respectively (χ 2 =13.1, p<0.001). Types of abnormalities are listed in Table II. The most common abnormal findings were obligatory synkinesis (42%), fine motor impairments (35%), and hyperreflexia (14%). Table I: Age at which developmental milestones (assessed from parental report) were reached by children with language impairment (LI) and by control children CELF-R standard score Normal Mildly abnormal Moderately abnormal Milestone Age (mo) t value p Children Control with LI children Mean (SD) Mean (SD) Sat unsupported 6.4 (1.7) 5.8 (1.5) ns Walked unassisted 13.0 (2.7) 11.8 (2.8) First words spoken 22.7 (11) 10.3 (3.1) <0.001 Used sentences 36.5 (13) 17.1 (5.2) < Expressive Receptive Total Figure 1: CELF-R standard scores for Total, Receptive and Expressive Language scales in children with LI with normal, mildly abnormal, or moderately to severely abnormal (moderately abnormal) neurological examinations. Standard score normative means are 100 (SD 15). 472 Developmental Medicine & Child Neurology 2000, 42:
4 FAMILY HISTORY AND MRI ABNORMALITIES Six of the 23 children with LI with normal MRI scans had a positive family history of language, learning, or attentional disorders in parent(s) or siblings. Four of the 12 children with LI with abnormal scans had a positive family history for one or more of these disorders. These differences were not significant. Discussion This study showed that neurological and brain morphological abnormalities were quite common in a large group of Table II: Types of abnormalities on neurological examination of children with language impairment (LI) and control children Abnormality Children Control p with LI children n (%) n (%) Obligatory synkinesis 30 (42) 6 (7) Fine motor impairment 25 (35) 4 (5) Hyperreflexia 10 (14) 3 (4) Oromotor apraxia 9 (13) 1 (1) Gross motor impairment 8 (11) 5 (6) ns Sensory deficit 7 (10) Hypotonia 4 (6) 3 (4) ns Muscle weakness 2 (3) 1 (1) ns Ataxia 1 (1) 0 ns Tremor 1 (1) 1 (1) ns Microcephaly 1 (1) 0 ns school-age children with developmental LI compared with typically developing children. Furthermore, the severity of the neurological abnormalities directly correlated with the severity of the language deficit as indicated by the scores on the CELF-R. In addition, the high incidence of abnormalities (in 12 of 35 children) on MRI scan in the group with LI suggests structural as well as functional involvement of the nervous system. These findings expand on previous reports suggesting neurodevelopmental dysfunction in children with LI, and provide profiles of the types of abnormalities that might be associated with LI. The neurological and MRI findings also support the hypothesis that developmental language disorders are not isolated entities, but are associated with other evidence of brain dysfunction. A similar conclusion can be drawn from the work of Gillberg and colleagues (Gillberg 1998, Kadesjo and Gillberg 1998, Landgren et al. 1998), who have conducted Table III: Types of abnormalities seen on MRI scans in children with developmental language impairment (n=12) Abnormality Nr of children Right ventricular enlargement 3 Left ventricular enlargement 1 Central volume loss 3 Band of hyperintensity in white matter 1 Multiple areas of white matter hyperintensity 2 Periventricular encephalomalacia 1 Asymmetry of occipital lobes left > right 1 Figure 2: MRI scan of 9-year-old girl with developmental language impairment (LI). Note asymmetry of lateral ventricles (left slightly larger than right). Figure 3: MRI scan of 12-year-old boy with developmental language impairment (LI). Note punctate hyperintensities in white matter, most prominent on the right. Neurological and MRI Abnormalities in Language Impairment Doris Trauner et al. 473
5 epidemiological studies of children in Sweden, and identified a 6% incidence of DAMP in school-age children (Kadesjo and Gillberg 1998). Two-thirds of the children with DAMP were said to have language problems (Landgren et al. 1998). These studies suggest a continuum of language, learning, and sensorimotor deficits, or that such multiple deficits may be common to any neurodevelopmental disorder. However, in our study, the primary (and often sole) problem for which the children with LI were referred was a language disorder, indicating that these children were not merely selected from a more global developmentally impaired group, but that their overriding clinically relevant deficit was in language. The structural differences found on MRI scans in almost one-third of the children with LI are of interest because they all show cortical and/or subcortical white matter abnormalities. Thus, the structural changes may suggest a common mechanism for developmental LI, i.e. some disruption in the normal development of primarily subcortical white matter pathways, perhaps resulting in an inefficiency in processing information from a variety of modalities. If this is so, the phenotype would differ from that of white matter damage seen in other conditions, such as periventricular leukomalacia (PVL). Studies have consistently documented impaired performance of children with PVL on visual motor (Skranes et al. 1998), visual perceptual (Olsaen et al. 1998), and visual-learning (Schatz et al. 1997) tasks, with spared language functions. The location of the white matter abnormalities may dictate which functions are most likely to be impaired. Etiological factors may also play a role in the differential effects of white matter insults on cognitive outcome. Multiple etiologies (e.g. genetic factors, toxins, hypoxia) may lead to subcortical dysfunction in children with LI. However, extensive reviews of the medical histories failed to identify consistent evidence for toxins or other environmental factors. The role of genetic influences was difficult to assess in this population, because information about relatives with similar disorders was retrospective and often incomplete. We did, however, find a much higher incidence of a positive family history of language, learning, and attention disorders in the LI group than in the control group (54% versus 18%), suggesting that genetic factors may influence language development. Studies from several other investigators have strongly implicated genetic factors as a cause for developmental LI (e.g. Neils and Aram 1986, Tallal et al. 1989b, Tomblin 1989, Plante 1996). The large cohort of twins included in the studies of Bishop and colleagues (Dale et al. 1998, Bishop et al. 1999) suggests a strong hereditary factor in specific LI. Recently, a large family was described in whom approximately half of both males and females in the family were said to have a specific impairment in grammar, such that they were unable to generate certain syntactic rules (e.g. for tense, number, or sex) (Gopnik and Crago 1991). These authors postulated the existence of grammar genes based on studies of this large kinship. Vharga-Khadem et al. (1995), studying members of this same family, identified more widespread deficits, including severe articulation defects, general intellectual impairments, linguistic problems, and oromotor dyspraxia. Recent genetic work by Fisher et al. (1998) has identified a locus on chromosome 7 (designated SPCH1) in the affected family members. The function of this gene has yet to be determined. Based on the results of the present study, suggesting that LI is not an isolated neurological deficit, as well as the findings of Vharga- Khadem and colleagues, it might be more reasonable to postulate the existence of genes that affect white matter development and/or function, rather than specific grammar genes, in the pathogenesis of language disorders. One limitation of the present study is the absence of information on electroencephalographic (EEG) abnormalities in LI and control children. A high incidence of paroxysmal abnormalities has been reported on EEG studies of children with developmental LI (Picard et al. 1998). Tuchman et al. (1991) found a high incidence (8%) of epilepsy in children with LI, although EEG findings were not reported. Although none of our children with LI had clinically documented seizures, we cannot rule out the possibility that the language deficit, neurological findings, or MRI changes might be related to subclinical epileptiform activity. Although there were differences in the sex distribution between the two groups (more boys than girls in the LI group), it is unlikely that the sex difference was responsible for the abnormalities found on neurological examination in the LI group. Gross and fine motor impairments, hyperreflexia, and apraxia, for example, are not reported to be more common in normally developing boys than girls. In summary, children with LI have dysfunctional nervous systems, and this is manifested in several ways, including abnormal motor and coordination skills, abnormal MRI scans, and perhaps with other non-linguistic cognitive abnormalities. children with LI are not neurologically homogeneous. The condition may be associated with various neurological and MRI findings in different children. This may reflect a spectrum of the same disorder, or multiple etiologies with the final common pathway resulting in significant LI. Our findings suggest that a multifaceted intervention approach to children with LI may be indicated. This would include not only speech and language therapy, but also perhaps occupational or sensory integration therapy and adaptive physical education programs. Early recognition of language and other neurological impairments will permit intervention when the developing nervous system has potential to reorganize. Accepted for publication 6th November Acknowledgements This research was supported partly by NIH-NINDS Grant PSO NS22343 and MH-NIDCD R29 DC We would like to thank the families who participated in this study and the research staff at the UCSD Project in Cognitive and Neural Development/Language Research Center. References Accardo P, Whitman B. (1989) Toe-walking: a marker for language disorders in the developmentally disabled. Clinical Pediatrics 28: Achenbach T, Edlebrock C. (1983) Manual for the Child Behavior Checklist and Revised Child Behavior Profile. 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