Some general conclusions can be derived from inspecting the results of qualitative profile analyses. First, learning and memory impairments were most common among all subjects (both children and adults, left hemisphere and right hemisphere lesions). Second, impairments in academic skills were more common among the children than the adults. Third, receptive and expressive language impairments were more common in adults with left hemisphere lesions than in children with left hemisphere lesions. Fourth, visual-motor (visual-construction) impairments were more common in children with left hemisphere lesions than in adults with left hemisphere lesions. Notably, however, all children with these impairments were left handed. This raises the strong possibility that those children transitioned to being left handed after experiencing right hemiparesis, and poor performance on visual-construction tasks may thus reflect clumsiness in the use of the left hand. Fifth, attention impairments were more common in left hemisphere-lesioned adults than in left hemisphere-lesioned children, but in all these cases, the adults also had impairments in expressive language. The attention measure that was used, the Digit Span subtest of the Wechsler scales, requires oral expression of numbers and is confounded with expressive language ability. Last, and perhaps most importantly, there did not appear to be a consistent pattern of adults performing worse than children or vice-versa. There were nearly equal numbers of subject pairs in which the child member of the pair was impaired in more domains than the adult, the adult was impaired in more domains than the child, or the number of impaired domains was equal across both members of the pair. For example, among the left hemisphere pairs, there were five pairs in which the adult demonstrated more impairment, six pairs in which the child demonstrated more impairment, and two pairs in which the number of impaired domains was equal across both members of the pair. Among the right hemisphere pairs, there were four pairs in which the adult was impaired in more domains, six pairs in which the child was the impaired in more domains, and six pairs in which the number of impaired domains was equal across both members of the pair. Thus, the overall level of impairment judging by pair-by-pair qualitative profile analysis was not impressively different, but the pattern was somewhat different in terms of which domains of cognitive abilities were affected for children versus adults.
Turning now to the domain of Social Functioning, we examined the adult and child participants with the following analyses. We assessed differences among adult subjects and among child subjects with Kruskal-Wallis Nonparametric Tests. We assessed differences between matched pairs of adults and children with Wilcoxon Signed Rank Nonparametric Tests. The results are reported in Table 7.
In the adult participants, the development of impairments in various aspects of Social Functioning following stroke was strikingly different between left hemisphere- and right hemisphere-damaged subjects. Changes in the domains of Interpersonal Functioning and Clinician Rating were almost nonexistent in the left hemisphere-lesioned adults. By contrast, moderate to severe changes in all measured aspects of Social Functioning were nearly ubiquitous in the right hemisphere-lesioned adults. These differences between right and left hemisphere-lesioned subjects were statistically significant: Interpersonal Functioning (Kruskal-Wallis test χ2 = 15.08, df = 1, P < 0.0005), Clinician Rating (Kruskal-Wallis Test χ2 = 9.27, df = 1, P = 0.002). In the left hemisphere subjects, the only domain that changed in an appreciable number of subjects (7/13) was Employment Status, likely secondary to disability from acquired cognitive deficits (eg, aphasia). Nevertheless, subjects with right hemisphere lesions were significantly more impaired regarding Employment Status than their counterparts with left hemisphere lesions (Kruskal-Wallis test χ2 = 5.22, df = 1, P < 0.03).
The child participants with left versus right hemisphere lesions were not significantly different in any of the Social Functioning outcome variables, that is, Special Education Status, Interpersonal Functioning, and Clinician Rating (all P > 0.38).
Of greatest interest for the purposes of the current study is the comparison of adult and child participants, matched for lesion location and size. The Wilcoxon Signed Rank Test was used for these analyses. Social Function outcome was compared between the adult group (n = 29) and the child group (n = 29). The groups were not significantly different regarding Interpersonal Function or Clinician Rating. However, the adults had significantly greater impairment with regard to Employment Status compared with the children's corresponding Special Education Status (Z = −2.86, P = 0.004). The separate analyses comparing matched pairs of adults/children with left hemisphere lesions and then with right hemisphere lesions were more informative (see Table 7).
Left Hemisphere Lesion Social Function Outcome Analyses
There was no significant difference between the Employment Status of adults and the corresponding Special Education Status measure in children. However, children were more impaired than their adult left hemisphere matches with respect to Interpersonal Functioning (Z = −2.46, P = 0.014) and Clinician Rating (Z = −2.50, P = 0.013).
Right Hemisphere Lesion Social Function Outcome Analyses
Adults were significantly more impaired than their child right hemisphere matches with respect to Employment Status/Special Education Status (Z = −2.92, P = 0.004) and the Clinician Rating (Z = −1.99, P = 0.046). Adults tended to be more impaired than the children regarding Interpersonal Functioning (Z = −1.87, P = 0.061).
The most striking and perhaps most surprising conclusion from our study is the degree of similarity between chronic neuropsychological and social outcomes in children and adults with similarly located brain lesions due to unilateral stroke. Given the number of analyses that were conducted on the many different outcome measures, it is impressive that very few differences were found when comparing children versus adults as a whole, left hemisphere-lesioned children versus left hemisphere-lesioned adults, and right hemisphere-lesioned children versus right hemisphere-lesioned adults. The degree of similarity in chronic outcomes (ie, outcomes occurring on average 3 years after stroke for adults and 9 years after stroke for children) is, on balance, striking.
Despite this similarity, the quantitative statistical analyses suggest a few fairly consistent findings worth mentioning. First, children with left hemisphere lesions appeared to demonstrate difficulty with tasks requiring visual-motor integration (ie, visual construction or drawing of a complex figure). Initially, this finding might seem counterintuitive as one might expect that children with right hemisphere lesions would be more susceptible to problems with visual construction rather than children with left hemisphere lesions. This finding makes more sense when examined in the context of the fact that many of these children were left handed, suggesting that their poor scores on visual-motor tasks could reflect inefficiency in learning to use the left hand, a change in handedness that was probably initiated by right hemiparesis following left hemisphere damage.
Second, speech and language ratings appeared to be normal in children with chronic left hemisphere lesions but mildly abnormal in adults with chronic left hemisphere lesions. These differences were most apparent on measures of observed difficulty with word finding, fluency, presence of paraphasic errors, and comprehension of spoken information. In fact, no children were rated as abnormal on any of these dimensions, using the same criteria that were used to judge the speech and language abilities of the adults in this sample. This finding is consistent with research reviewed in the introductory text, demonstrating that damage to language-related neural structures in children inflicts less permanent speech and language impairment than similar damage in adults. However, support was garnered only on qualitative ratings of speech and language abilities and not on formal tests such as subtests from the Multilingual Aphasia Examination. In fact, average scores on the Token Test, Controlled Oral Word Association Test, and Sentence Repetition Test were not significantly better for the children with left hemisphere lesions than for adults with matched lesions. At issue here may be the sensitivity of the formal tests and even the qualitative speech/language assessments. For example, a more sensitive measure of narrative discourse in a subset of this child cohort elicited impairment especially in children with lesion acquisition before age 1.40
A third finding was that anterograde verbal memory scores were stronger for adults with right hemisphere lesions than for children with similar lesions. The same effect was not seen in left hemisphere-lesioned subjects. Overall, though, the mean score for right hemisphere-lesioned children was still within the average range and within 1 SD of the mean. This suggests that although adults performed slightly stronger than children with similar lesions in this domain, the children were not actually “impaired” in verbal memory. The explanation behind stronger performance in the right hemisphere adults compared with the right hemisphere children is unclear, and this finding warrants further investigation. One intriguing possibility is the so-called “crowding hypothesis,” which posits that early brain lesions lead to more cognitive functions being represented in the contralesional hemisphere, leading to a “crowding out” of some abilities. The nonlesioned hemisphere (in this case, the left hemisphere) carries the burden of serving the usual functions associated with that hemisphere (eg, verbal processing and verbal memory) but also acquires responsibility for subserving some cognitive functions of the injured hemisphere (eg, nonverbal memory), and thus some abilities end up compromised owing to this overburdening. A possibility is that in children with right hemisphere lesions, the burden of visual memory came to be subserved by the functioning left hemisphere and led to a decrease in the function usually served by the left mesiotemporal area, namely, verbal memory. This hypothesis warrants further investigation.
Fourth, the pattern of social function outcome was intriguing. In adults, there was a clear and potent effect of hemispheric side of damage. Adults with right hemisphere lesions fared significantly worse than adults with left hemisphere lesions in all domains of Social Function measured (Employment Status, Interpersonal Status, and Clinician Rating). This is consistent with previous studies and may be related, in part, to deficits in empathy and disruption in everyday decision making and emotional processing14,41,42 often associated with right-sided lesions. In contrast, the children with left versus right hemisphere lesions were not significantly different with respect to social function outcome. Both groups of children exhibited mild to moderate impairments, on average. This finding of the apparent absence of an effect of lesion laterality is consistent with the finding of a relative lack of laterality findings as well as the presence of mild to moderate impairment regarding neuropsychological functions in this cohort43 and others.23,24,44,45
This led to the interesting finding that children with right hemisphere lesions had significantly better social outcomes than adults with matched lesions. A finding of this nature suggests a process of plasticity buffering the children from more severe social outcome impairment. Further evidence of plasticity favoring children were analyses comparing the entire child cohort with the entire adult cohort, which found that outcome was significantly worse for adults regarding Employment Status/Special Education Status. However, if this is a function of plasticity, it is clear that the process of plasticity is domain selective. Children do not simply have better social outcomes than their lesion-matched adults. First, the child cohort and the adult cohort as a whole did not differ significantly in social outcomes other than Employment Status/Special Education Status. Second, children with left hemisphere lesions were significantly more impaired in their social function outcomes than adults with matched lesions. The latter finding may imply that plasticity processes involved recruitment of other brain areas-possibly in the right hemisphere-to subserve critical left hemisphere functions such as language and thereby compromised areas which are generally destined (in the absence of brain damage) to subserve a variety of social functions. This would be consistent with our finding that children with left hemisphere lesions had significantly better language function but significantly worse social outcomes than adults with matched lesions.
Results from the qualitative pair-by-pair profile analysis also lead to some general conclusions. First, academic skill impairments were more likely to be seen in children than their adult counterparts. This finding is consistent with those of Pitchford11 that suggest that lesions acquired in childhood before literacy acquisition detrimentally affected the development of reading skills, both in children who suffered general declines in verbal processing (Verbal IQ relative to Performance IQ) and in children who merely showed a deficit in basic phonics skills without poor Verbal IQ. Together these results suggest the possibility that children with unilateral strokes who have not yet fully developed academic skills might be more prone to problems in this area than adults with unilateral strokes in whom these skills were already firmly established. However, it is important to note that even though there seems to be greater vulnerability to poor academic skill development in children with strokes as compared with adults with similar strokes, the majority of children in both the left hemisphere and the right hemisphere groups did not show impairment in this area. Additionally, in several cases in which the child member of the pair demonstrated an academic skill impairment, the adult was not administered the relevant academic skill test, and thus we have missing data that further dilutes the salience of this difference.
Another conclusion from the pair-by-pair profile analysis is that learning and memory impairments appeared to be the most commonly demonstrated weaknesses, for both children and their adult counterparts with both the left hemisphere-lesioned group and the right hemisphere-lesioned group. This finding was not necessarily anticipated based on the extant literature but is not all that surprising, given the prevalence of learning and memory impairments encountered in clinical practice with stroke patients. Several cognitive abilities are paramount in successful performance on a learning and memory task, including attention to the task at hand, organization of the to-be-learned information, adequate rehearsal and encoding, consolidation, and retrieval. Damage to brain structures affecting any of these abilities could impair or at least hinder performance on the final outcome measure: delayed spontaneous recall of an orally presented word list. Therefore, it is possible that the frequency of learning and memory impairments demonstrated by our sample is expected, given that this type of task is very sensitive to any type of brain dysfunction in general, as there are so many prerequisite cognitive abilities required for successful performance. Likewise, the finding from qualitative analyses that more left hemisphere-lesioned adults showed attention impairments than left hemisphere-lesioned children also could be due to the fact that several abilities are paramount to successful completion of the particular attention measure that was used, the Digit Span subtest from the Wechsler scales. This is strengthened by the fact that all adults with impairments in this domain also had impairments in expressive language.
Additional conclusions from the qualitative profile analyses echo those garnered from the quantitative analyses: Some aspects of speech and language abilities were more fully recovered in children with left hemisphere lesions than in their adult counterparts with similar lesions, and second, more children with left hemisphere lesions experienced visual-motor impairments than adults with similar lesions.
Last, the overall degree of impairment, as reflected in the number of impaired cognitive domains, was not consistently greater for children or adults. There appeared to be almost equal numbers of pairs in which the adult seemed more impaired than the child with a similar lesion and vice versa, or both members of the pair were impaired along the same number of cognitive domains. These findings echo the larger conclusion from this study that was somewhat surprising, given the literature on neural plasticity. That is to say, we did not find compelling evidence of striking differences between the degree and patterns of recovery in chronic neuropsychological functioning in children and adults with very similar brain lesions.
The fact that our subjects were matched based on brain lesion location and size is a novel approach to studying this question and helps refute the argument that the reason the children were not found to be more fully recovered was because of some systematic bias in the amount and nature of neuroanatomical damage between the children and the adults who were studied. Our lesion-matching approach to this issue is certainly one of the main strengths of this study, and we hope other authors will attempt to replicate and extend our findings using this scientifically rigorous approach. Another strength of our study is the fact that we examined chronic outcome data, and these findings have some clinical relevance for what practitioners are able to tell their patients to expect “in the long run.” Pediatric neuropsychologists probably get this question from parents of their patients more often than any other question (ie, “What will my child be like in 5-10 years, and will this problem ever recover?”). This type of chronic outcome data is often lacking in stroke research, and child samples are especially challenging to follow over long intervals for obvious reasons.
Some weaknesses in this study that we would have liked to have addressed include that we had more missing data for the adults, particularly on tests of academic skills and executive abilities, than we did for the children. Given the fact that we were using retrospective data, we had little remedy for this problem. Certainly, a longitudinal design might be a more effective approach to dealing with this issue in future research. Additionally, we had only one measure of attention and concentration, the Digit Span subtest of the Wechsler scales, which is potentially confounded with language abilities. Ideally, we would have used other measures as well (such as Trail Making Test A) without the same language requirements. Other such measures were not used consistently enough in testing our subjects to make meaningful comparisons between and within groups. Last, although we attempted to match brain lesions as closely as possible and used two clinical anatomic methods to optimize the quality of the matches (expert judgments and lesion code cross-checking), complemented by statistical methods (correlation of extent of lesions was 0.694 and nonsignificant difference on paired nonparametric analyses), there was not perfect consistency in every pair. Given the infinite variability of the human brain, attempting “perfect” matches between any two injured brains is a lofty but probably unattainable goal. Future researchers may wish to expand and refine our method to attempt even more rigorous matching procedures, possibly incorporating lesion location and lesion volume.
Research on age at onset of childhood brain lesions and cognitive outcomes could potentially clarify the issue of neural plasticity if consistent relationships were documented between age at onset and outcomes, such as was initiated in the animal work conducted by Hubel and Weisel6 documenting “critical periods” of neural development. Unfortunately, the relevant adult data in the extant literature do not serve to clarify the issue much because the findings are mixed. Some studies have found no significant influence of age at onset of childhood lesions,46,47 and some have found a U-shaped IQ distribution (children with congenital and late lesions having higher IQ scores than children with middle childhood lesions).23,24,48 Taking into account both age at onset and side of lesion, Hogan et al22 presented data from an ongoing project that suggest that early lesions (acquired before age 5) do not lead to a dissociation between Verbal and Performance IQ based on hemispheric location. Lesions acquired after age 5 begin to show lateralization, with the relative preservation of Verbal IQ in right hemisphere cases and lower Verbal and Performance IQ in left hemisphere cases. Aram,9 in a review of studies examining age at lesion onset as a predictor of subsequent cognitive impairment, concluded that there is not a strong relationship between the age at which children's lesions are acquired and performance on cognitive tasks. Rather, there appears to be a modest relationship suggesting that lesions acquired very early (eg, before the age of 1) lead to poorer outcome than childhood lesions acquired later.
Our research did not address the issue of age at onset except in a very general manner, such that children and adults were separate groups for quantitative and qualitative statistical analysis. Further research on this topic might explore this issue by examining age at onset within each group as an independent variable, either as a continuous variable or a categorical variable (eg, “early” lesions defined as acquired at younger than 1 year versus “middle” and “late” childhood lesions). Because of our somewhat small sample sizes, we did not approach our data in this manner as we would have significantly lost statistical power by further dividing our child and adult subjects into smaller groups.
Another possibly pertinent issue that was not specifically addressed in our research is whether lesion location as divided into “cortical-only” or “subcortical-only” categories leads to the finding of differential neuropsychological effects. Relevant data from Aram and Ekelman16,49 suggest that children with subcortical-only lesions (as opposed to cortical-only lesions) tend to be more impaired, with left hemisphere subcortical-lesioned children having lower Verbal IQ scores (relative to Performance IQ) and right hemisphere-lesioned children having lower Performance IQ scores (relative to Verbal IQ). Review of these studies and others led Aram9 to conclude that children with left hemisphere lesions confined to subcortical structures show persistent and severe deficits in academic skills acquisition. In contrast, Hogan et al22 reviewed evidence to raise the possibility that cortical damage was more detrimental than subcortical damage, although when size of lesion was taken into account, this effect became questionable. Again, our limited sample sizes prevented further analysis along these lines, as many of our subjects had both cortical and subcortical involvement and thus subgroups of “cortical-only” and “subcortical-only” subjects would have been quite small.
In conclusion, the most interesting and compelling overall finding from this research is the degree of similarity between outcomes of adults and children with carefully matched brain lesions who are studied years after lesion onset. Although there is some evidence of adult plasticity in the existing literature, this was a somewhat unexpected finding, given that much of the previous work in the area suggested that children might show more resiliency after brain damage than adults with similar brain damage. Our approach of lesion matching based on location and size is a novel one that was used to further illuminate this issue and highlights the similarity in plasticity between immature and mature nervous systems. We hope the method will provide fodder for future research and debate in this exciting arena.
We acknowledge the support of Katherine Mathews for assistance with selection of the child subjects, Facundo Manes for child lesion identification, Gregory Cooper, Liana Apostolova, and Hanna Damasio for assistance in lesion matching, Peter Fox and Jack Lancaster for child volumetric measurements, Amy Lansing for database management, and Damien Ihrig for child data collection.
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Keywords:© 2005 Lippincott Williams & Wilkins, Inc.
brain injury; unilateral stroke; neural plasticity; social functioning; pediatric stroke; adult stroke.