Published online December 1, 2005
PEDIATRICS Vol. 116 No. 6 December 2005, pp. 1374-1382 (doi:10.1542/peds.2004-1728)
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Functional Plasticity or Vulnerability After Early Brain Injury?

Vicki Anderson, PhD*,{ddagger},§, Cathy Catroppa, PhD*,{ddagger},§, Sue Morse, BAppSci{ddagger}, Flora Haritou, BAppSci{ddagger},§ and Jeffrey Rosenfeld, FRACS{ddagger}

* University of Melbourne, Melbourne, Australia
{ddagger} Royal Children’s Hospital, Melbourne, Australia
§ Murdoch Children’s Research Institute, Melbourne, Australia


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Context. Traumatic brain injury (TBI) is a common, acquired, childhood disability that may be used as a model to understand more completely the impact of early brain injury on both brain structure and day-to-day function. Contrary to previously held views of the "plasticity" of the young brain, recent research suggests that such early insults may have a profound impact on development. To date, these suggestions remain largely untested.

Objectives. To plot changes in cognitive abilities after childhood TBI over the 30 months after injury and to examine the impact of age at injury on cognitive outcomes.

Design. Prospective longitudinal study.

Setting. Royal Children’s Hospital, Victoria, Australia.

Main Outcome Measures. Global intellectual ability, verbal and nonverbal skills, attention, and processing speed.

Participants. A total of 122 children admitted to the hospital with a diagnosis of TBI were divided according to injury age, ie, young (age: 3–7 years) or old (age: 8–12 years), and injury severity (mild, moderate, or severe) and were evaluated acutely and at 12 and 30 months after injury. An additional sample of children injured before 3 years of age (n = 27) was compared with these groups with respect to global intellectual ability only.

Results. A clear relationship was documented between injury severity and cognitive performance. For children who sustained severe injury, younger age at injury was associated with minimal, if any, recovery after injury, but better outcomes were observed after severe TBI among older children. Age at injury was not predictive of outcomes for children with mild or moderate TBI, although infants (age: 0–2.11 years) with moderate TBI showed poorer outcomes than did older children with injury of similar severity.

Conclusions. Findings support a "double-hazard" model for severe and early brain insults and add to the ongoing debate regarding cerebral plasticity, suggesting that, contrary to traditional views, young children who sustain severe TBI in early childhood or moderate or severe TBI in infancy may be particularly vulnerable to significant residual cognitive impairment. From a clinical perspective, results indicate that long-term follow-up monitoring and management should be targeted to this high-risk group.

Key Words: traumatic brain injury • children • recovery

Abbreviations: TBI, traumatic brain injury • SES, socioeconomic status • GCS, Glasgow Coma Scale • CT, computed tomographic • VABS, Vineland Adaptive Behavior Scale • MDI, Mental Developmental Index • FSIQ, full-scale IQ • WISC-III, Wechsler Intelligence Scale for Children-III • WPPSI-R, Wechsler Preschool and Primary Intelligence Scale-Revised

Traumatic brain injury (TBI) is a major cause of death and disability worldwide. Among children, brain injury represents a common interruption of the course of normal development, occurring at an annual rate of 250 cases per 100000 children.1 Most of these injuries are mild and result in few, if any, long-term deficits. However, children who sustain severe insults demonstrate residual cognitive and functional impairments. Despite the commonly held view that young children’s brains are able to adapt to the impact of severe insults, clinical reports indicate that residual problems occur in a range of skills, including intellectual ability, attention, and memory.2 These deficits potentially interfere with development, reducing the child’s ability to acquire knowledge and skills and causing increasing gaps between the abilities of injured children and those of their peers. Secondary deficits in academic progress and social and emotional adjustment may also emerge.3,4

Injury severity is a well-established index of outcomes.5 Other predictors include type of injury, premorbid cognitive and learning abilities, family function, and access to rehabilitation.6,7 Age or developmental level at the time of injury may also influence outcomes. On the basis of the good outcomes observed for young children with focal cerebral pathologic conditions, proponents of brain plasticity models argue that young children sustain less-severe structural damage and fewer functional deficits from brain insults, compared with older children and adults.8–11 These findings are interpreted as evidence that brain physiologic features and structure are more modifiable early in life, with healthy tissue assuming functions of damaged tissue, resulting in minimal impairment. It is not clear that such principles apply when brain insults are generalized and there is little undamaged tissue to support functional reorganization.12,13 Among children who sustain generalized insults, structural factors may increase the likelihood of diffuse injury. Greater flexibility of the cranial bones of children may enhance the capacity of the skull to absorb traumatic forces, thereby reducing focal brain injury.14 A relatively larger head supported by a smaller neck among younger children increases the risk for diffuse injuries.15 Furthermore, because of their immaturity, frontal regions and myelinating fibers may be particularly vulnerable to the impact of injury.16,17 Functional domains documented commonly as deficient after TBI, such as information processing, memory, and executive function, implicate the involvement of these developing neural components.

An alternative interpretation18 argues that brain damage during childhood, especially early childhood, may disrupt development. There is some support for this suggestion, with reports that children experience more severe neurologic dysfunction and greater incidence of delayed brain pathologic conditions than do adults.19,20 From a cognitive perspective, early brain injury might be expected to result in cumulative deficits, because of the small repertoire of established skills available to young children and the likely difficulties of consolidating new skills and knowledge.21

Using a prospective longitudinal design, this study examined the relationship between injury severity, age at injury, and recovery. To our knowledge, no previous study has attempted this using such a wide age range and a follow-up period of >2 years. We predicted that (1) children who sustained early TBI (before 8 years of age) would achieve poorer outcomes than children with later injuries (after 8 years of age); (2) severe injury would be linked to greater impairment; and (3) interactions would be present between age at injury, injury severity, and time since injury, with few sequelae following mild TBI, regardless of age. For early moderate or severe injuries, where brain development was less complete, increasing deficits were expected with time since injury.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Participants
One hundred twenty-two children (85 male) with TBI participated in the study. Inclusion criteria were (1) age at injury of 3 years 0 months to 12 years 11 months; (2) documented evidence of TBI, including period of altered consciousness; (3) ability to complete cognitive evaluation; and (4) completion of acute, 12-month, and 30-month evaluations. Exclusion criteria were penetrating head injury, TBI as a result of child abuse, previous TBI, and preexisting physical, neurologic, psychiatric, or developmental disorder. During the recruitment period, 169 children were admitted to the hospital with a diagnosis of TBI. Twenty children did not meet recruitment criteria, due to preexisting developmental behavioral/neurologic problems (n = 11), previous TBI (n = 3), TBI attributable to abuse (n = 1), an inability to participate because of the severity of disability (n = 2), and incomplete data sets at acute evaluation (n = 3). Initial approaches were made to 149 children and families, with 27 declining to participate. Reasons for refusal included inconvenience (n = 7), distance (n = 8), and disinterest (n = 12). Comparison of the demographic and injury characteristics of participating and nonparticipating groups identified no group differences. Demographic characteristics of the sample are provided in Table 1.


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  		TABLE 1. Demographic Characteristics of the Sample According to Age at Injury and Injury Severity

 
Children were divided into groups on the basis of age at injury and injury severity, as follows: young TBI (n = 53), 3 year 0 months to 7 years 11 months at injury; old TBI (n = 69), 8 years 0 months to 12 years 11 months at injury. The age categorization was made on the basis of theoretical grounds and recent research supporting substantial changes in cerebral and cognitive development in infancy and before 8 years of age, with more gradual development from 8 to 12 years.17,20,21

A third group, the infant TBI group, conforming to the selection criteria described above, was used as a subset of the primary study and included children who had sustained their injuries before age 3 (birth to 2 years 11 months). This group was smaller (n = 27) and, because of developmental level, could not be assessed with the same intellectual measures as older children. However, we thought that the inclusion of this group provided important preliminary information regarding the impact of TBI and recovery patterns in the infant brain.

Severity groups were established, as follows: (1) mild TBI, Glasgow Coma Scale (GCS) score22 at admission of 13 to 15, no abnormality on computed tomographic (CT)/MRI scans, and no neurologic deficits; (2) moderate TBI, GCS score at admission of 9 to 12 and mass lesion and/or evidence of specific injury on CT/MRI scans; (3) severe TBI, GCS score at admission of 3 to 8 and mass lesion or evidence of pathologic condition on CT/MRI scans. Injury characteristics are presented in Tables 1 and 2.


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  		TABLE 2. Injury and Medical Characteristics of the Sample According to Age at Injury and Injury Severity

 
GCS scores (at admission) and neurologic status were recorded by the admitting medical officer, with a standardized protocol. After admission, standardized, half-hourly, neurosurgical observations were recorded by experienced nursing staff members. These gradually increased to every 4 hours, with recordings continuing until the child regained consciousness. CT/MRI scans were reported by a pediatric neuroradiologist and a neurosurgeon who were blinded to the injury status of the participants.

According to requirements of the Royal Children’s Hospital Human Ethics Committee, information packs describing the study were provided to families during their child’s hospital admission. Participants were children who met inclusion criteria and for whom signed consent forms were obtained. After families gave consent, demographic questionnaires and the Vineland Adaptive Behavior Scale (VABS)23 were completed by parents, on the basis of preinjury functioning. Children were evaluated after acute neurologic dysfunction/posttraumatic amnesia resolved (time 1, 0–3 months after injury). Review evaluations were conducted 12 months (time 2) and 30 months (time 3) after injury.

Measures
Injury and Demographic Variables
Children’s medical and developmental histories, parental education and occupation, and family configuration were documented. During hospitalization, GCS scores, length of coma, neurologic abnormalities, and surgical interventions were recorded. Environmental factors (socioeconomic status [SES] and family function) were also assessed, given the previously reported relevance of such variables to recovery after TBI. SES was coded with the Scale of Occupational Prestige reported by Daniel,24 which rates parental occupations on a 7-point scale, with high scores representing low SES. Family factors were measured (at all time points) with the Family Function Questionnaire,25 which includes 3 scales, ie, intimacy, conflict, and parenting style.

Preinjury Abilities
The VABS23 was completed by parents on the basis of children’s preinjury functioning. Four measures were derived, ie, communication, daily living skills, socialization, and total adaptive behavior score (mean: 100; SD: 15).

Postinjury Abilities
For the young and old TBI groups, the Wechsler Preschool and Primary Intelligence Scale-Revised (WPPSI-R)26 or the Wechsler Intelligence Scale for Children-III (WISC-III)27 was administered, depending on the age of the child (WPPSI-R for those <6.5 years of age and WISC-III for those ≥6.5 years of age). Verbal IQ, performance IQ, full-scale IQ (FSIQ) (mean: 100; SD: 15), and index scores (mean: 10; SD: 3) were calculated. Index scores (verbal comprehension, perceptual organization, freedom from distractibility, and processing speed) were derived from subtests of the WISC-III and WPPSI-R and included in the analyses to facilitate examination of attention and processing skills, which are commonly identified as deficient after TBI.

For children in the infant TBI group, the Bayley Scales of Infant Development28 were administered. A Mental Developmental Index (MDI) was derived from this measure, reflecting global intellectual ability. The MDI has psychometric properties similar to those of the Wechsler scales, as described above (mean: 100; SD: 15).

Funding for this study was provided by the National Health and Medical Research Council of Australia and the Royal Children’s Hospital Research Institute. These agencies played no role in any aspect of performance of the study, interpretation of findings, or publication of results.

Statistical Methods
All analyses were performed with the SPSS statistical package (version 11.0.0; SPSS, Chicago, IL). Infant, young, and old TBI groups were initially compared with respect to demographic, preinjury, psychosocial, and injury-related variables, to identify group differences that might influence postinjury function. Group differences in age at injury and SES were analyzed with 1-way analysis of variance. For categorical variables such as gender and family structure, group differences were assessed with the Pearson {chi}2 test. Repeated-measures analysis of variance (full factorial model: age x severity x time) was conducted with IQ scores and indices, to investigate the effects of age at injury and injury severity over the 30 months after injury. Residuals were assessed for each repeated-measures analysis of variance, and models provided good fits in all instances. Given the small cell sizes and overall sample size, as well as the exploratory nature of the study, we chose to err on the side of generosity when determining levels for statistical significance, with a cutoff value of P = .05.

Analyses were also conducted with Family Function Questionnaire results and gender as covariates, to examine the impact of demographic and environmental factors on outcomes. Results showed that these variables did not have significant effects on neurobehavioral measures. Therefore, these analyses are not reported in more detail.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
As illustrated in Table 1, no group differences were found among the infant, young, and old TBI groups with respect to gender, SES, or family structure before injury, indicating no preexisting psychosocial differences. As illustrated in Table 2, severity groups, but not age groups, showed significant differences with respect to GCS scores at 24 hours [F(2115) = 32.43; P = .002]. Infants with moderate or severe injuries were more likely to suffer loss of consciousness, with 77.7% having a period of coma of >1 hour. In contrast, less than one half of the children in the older groups recorded a similar period of coma. Although the proportions of children with moderate or severe TBI and abnormal radiologic and neurologic results were similar across age groups, infants with moderate or severe injuries exhibited edema, extradural or subdural bleeding, or focal pathologic conditions less frequently. Data presented in Table 2 show that children with severe injuries were more likely to demonstrate multiple areas of cerebral pathology, with frontal and subcortical pathology being identified most commonly. Children injured at 3 to 7 years of age were more likely to suffer subcortical damage (infants: 0%; young: 21.2%; old: 7.2%), but the 3 groups had similar rates of generalized pathology (infants: 7.4%; young: 8.5%; old: 10.1%). Most children in each group sustained TBI as a result of a fall or motor vehicle accident. Mild or moderate injuries were more likely to be associated with falls, whereas severe TBI was commonly attributable to motor vehicle accidents (Table 2). Preinjury levels of functioning showed no significant group differences with respect to total scores or the domains of communication, daily living skills, and socialization. These results are presented in Table 3.


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  		TABLE 3. Preinjury Adaptive Functioning for Young and Old TBI Groups

 
Global intellectual quotients (FSIQ/MDI) across the 3 age groups (infant, young, and old), severity levels (mild, moderate, and severe injury), and time points (acute, 12 months, and 30 months) are presented in Fig 1. Repeated-measures analysis of variance (age group x severity x time) identified a significant main effect for severity [F(2,133) = 4.9; P = .009] but not for age group [F(2,133) = 1.2; P = .30] or time [F(1,133) = 0.9; P = .8] and significant interactions for time x severity [F(2,133) = 4.2; P = .02], time x age group [F(2,133) = 7.0; P = .001], and time x severity x age group [F(4,133) = 4.2; P = .003]. These results, illustrated in Fig 1, indicate that all groups in the young and old age ranges recorded higher FSIQ scores at time 2 than time 1, suggesting evidence of some recovery in the 12 months after TBI. With the exception of the 2 severe TBI groups, performances remained relatively stable from time 2 to time 3. In contrast, results for the 2 severe TBI groups suggested divergence of outcomes from time 2 to time 3, with the old/severe TBI group displaying continued improvement and the young/severe TBI group demonstrating a similar decrease in performance. A dose-response relationship between injury severity and outcomes was demonstrated clearly.


Figure 1
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  		Fig 1. Recovery of global intellectual skills over 30 months after TBI for children sustaining TBI from birth to 12 years. Mod indicates moderate.

 
The results for the infant TBI group suggest a somewhat different pattern. Preinjury adaptive behavior skills in this age group were comparable to those recorded for older age groups across severity levels (Table 3). In contrast to the older groups, however, the impact of injury severity was not apparent at acute assessment for the moderate and severe TBI groups, which demonstrated mean global intellectual quotients within the average range at this time point. To illustrate this, preinjury versus acute performance decrements for moderate and severe TBI groups were substantially smaller for infants than for older children (infant/moderate TBI: –0.05 points; infant/severe TBI: –5.4 points; young/moderate TBI: –16.7 points; young/severe TBI: –26.2 points; old/moderate TBI: –11.5 points; old/severe TBI: –11.9 points). This better recovery was not sustained, however, and infants with both moderate and severe TBI showed substantive decreases in performance from acute assessments to 30 months after TBI (moderate: –13.0 points; severe: –6.4 points). Older age groups showed no such decrements. In contrast, the infant/mild TBI group (n = 4) had a decrease of 11.4 points between preinjury (VABS) and acute (FSIQ/MDI) assessments, which was twice as great as that demonstrated by older children with mild injuries. Despite this early deterioration, the infant/mild TBI group showed the steepest trajectory from acute to 30-month assessments (infant/mild: 6.3 points; young/mild: 0.4 points; old/mild: –4.0 points), at which time they performed similarly to the other mild TBI groups.

The remainder of analyses were restricted to the young and old TBI groups, because measures used for the infant group were not able to differentiate specific cognitive domains. As illustrated in Fig 2A, verbal skills (verbal IQ) were also affected significantly by injury severity [F(2,114) = 6.17; P = .003], with a severity x age x time interaction also being detected [F(4,114) = 3.63; P = .008]. More severe injury was associated with poorer performance in the verbal domain. In the first 12 months after injury, greatest improvement was evident for the young/mild TBI group (5.2 points), with similar progress for the old/severe TBI group (4.5 points). All other groups showed relatively flat trajectories for verbal skills during that time. The only improvement noted from 12 to 30 months was for the old/severe TBI group, which demonstrated ongoing score increases throughout the follow-up period. Other groups showed small reductions in verbal scores, with no evidence of ongoing recovery. Because these scores are age-standardized, these findings suggest a lack of expected development for these groups.


Figure 2
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  		Fig 2. Trajectories for verbal IQ (A) and performance IQ (B) over 30 months after TBI.

 
For nonverbal abilities measured as performance IQ (Fig 2B), significant main effects for severity [F(2,116) = 11.42; P < .0001] and time [F(1,116) = 24.17; P < .0001) were identified. Again, more severe injury was related to poorer performance, and all except 1 group (young/mild TBI group) demonstrated some evidence of recovery (above developmental expectations) in the postacute stage, with improvement in scores from time 1 to time 2. A number of significant interactions were detected, ie, time x severity [F(4,116) = 4.20; P = .003], time x age [F(1,116) = 5.72; P = .004], and time x severity x age [F(4,116) = 3.16; P = .02]. Trajectories for moderate injuries were similar, regardless of age at injury; however, younger injury was related to poorer development in the 30 months after injury for mild and severe TBI with this measure.

Results from domain-specific index scores were also examined (Tables 4 and 5), to investigate performance in the areas of working memory/attentional capacity (freedom from distractibility) and speed of response (processing speed). No main effects or interactions were evident for the freedom from distractibility factor, with group means falling consistently within the normal range. Severity effects were significant for all other indices [processing speed: F(2,110) = 15.38; P < .0001; verbal comprehension: F(2,110) = 6.64; P = .002; perceptual organization: F(2,118) = 8.66; P < .001], with more severe injury being linked consistently with poorest results.


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  		TABLE 4. Index Scores Across Injury Severity and Age at Injury Groups

 

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  		TABLE 5. Wechsler IQ Scores Across Injury Severity and Age at Injury Groups

 
Increases in index scores from acute to 30-month assessments were evident for processing speed [F(2,110) = 7.18; P = .001] and perceptual organization [F(11,110) = 20.79; P < .0001], which suggests that most improvement after injury occurred in nonverbal skills and response speed, whereas verbal skills and attention remained stable. A time x severity interaction was found for perceptual organization: [F(4,110) = 5.38; P = .001], with greatest improvement for children with more severe injuries. There were no age at injury effects for index scores, but time x age effects emerged for the nonverbal indices [perceptual organization: F(2,110) = 6.74; P = .001; processing speed: F(2,110) = 4.47; P < .05], with younger age at injury being associated with less improvement in these indices. Finally, time x age x severity interactions were present for verbal comprehension [F(4,110) = 3.52; P = .01] and perceptual organization [F(2,110) = 2.56; P = .04].

As illustrated in Table 4, mild and moderate TBI groups functioned within the average range (mean score: 10 ± 3) at each time point for verbal comprehension, perceptual organization, and processing speed. In contrast, mean scores for the severe TBI groups were more deviant, with processing speed scores being >1 SD below expectations at that stage. Even at 30 months, few index scores were within the average range for the severe TBI group.


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Several factors influence long-term outcomes after childhood TBI. Severity of insult is a critical predictor of outcomes in the acute postinjury period. With time after injury, other factors begin to play roles, and different recovery trajectories have been documented, depending on interactions between severity, age at injury, and time since injury. Improvements in general intellectual ability during the first 12 months after injury were observed for children with an injury age of ≥3 years, consistent with previous research.4,13,21,29 From 12 to 30 months after TBI, recovery trajectories began to diverge. Children with mild or moderate injuries sustained at ≥3 years of age displayed gradual improvements in abilities, regardless of age at injury. Within the severe TBI group, extremes of performance were observed. Children with later injuries showed the best recovery of all groups, and those who sustained early insults demonstrated the least recovery.

Although these findings are specific to TBI, they may also be applied to other childhood conditions in which diffuse brain injury is present (eg, infections or toxicities).2,12,30 Overall, results do not support plasticity models, which are based on results from animal studies or cases of focal brain pathologic conditions,10,11 as a universal template for all early brain injury. These results cannot be attributed simply to the impact of typical confounders associated with TBI (for example, social and family factors and preexisting conditions), because these factors did not differ significantly across age and severity groups.

Recovery From Mild or Moderate TBI After 3 Years of Age
Postinjury IQ trajectories were similar for children who sustained mild or moderate TBI, for both young and old groups. For children who sustained mild TBI after 3 years of age, mean intellectual abilities were within the average range (range: 102.7–104.3), which suggests that brain insults had minimal effects on overall levels of function. Scores achieved by children with moderate TBI sustained after 3 years of age were marginally lower (range: 94.3–98.2) but also fell within the average range. Children who sustained mild or moderate TBI showed small gains during the first 12 months after injury, which suggests some recovery of cognitive function, above gains expected in normal development, during the months immediately after injury. From 12 to 30 months, however, these trajectories were stable.

Outcomes of Severe TBI After 3 Years of Age
Severe TBI after 3 years of age was associated with low average intellectual function (mean FSIQ: acute, 82.7; 12 months, 89.2; 30 months, 89.8), with performances being associated with age at injury. Children who sustained severe TBI later in childhood (8–12 years) showed pleasing (clinically significant, ie, >0.5 SD) increments in performance in the initial 12 months after injury (FSIQ: +8.9 points) but less improvement from 12 to 30 months (+2.3 points). Postinjury IQ trajectories were steeper in the late/severe TBI group than in any other group and were similar to those described for adult populations.27 In contrast, children who sustained severe TBI between 3 and 7 years of age showed flatter recovery curves (FSIQ: +1.1 points from acute to 30-month assessments), which indicated minimal improvement.

Global Intellectual Outcomes After Infant TBI
Preliminary results for children who sustained their injuries in infancy suggest a somewhat different pattern of postinjury performance, although these findings must be interpreted in the context of small sample size and the use of a different measure of global intellectual ability (Bayley’s MDI). Mild injury sustained before 3 years of age was associated with continued improvements, greater than those expected for normal development. In contrast, those with moderate or severe TBI recorded continuing significant decreases (>0.67 SD) in global intellectual ability from acute assessments to 12 to 30 months after injury (moderate: –13.5 points; severe: –12.2 points). These results require replication but do suggest that TBI in infancy (ie, <3 of age) may be more detrimental to ongoing development than is the case for preschool- and school-aged children. Such findings are consistent with results after early brain damage reported in the animal literature31,32 and cognitive findings, which argue that early injuries are particularly detrimental to ongoing cognitive development.33

These findings support the predicted relationship between age at injury and injury severity with respect to outcomes. Although age at injury seems to be unrelated to recovery for mild injuries, this is not the case for more severe insults. In such circumstances, younger age at injury is associated with poorer outcomes, in keeping with previous research indicating the vulnerability of the immature brain.2,12,16 This vulnerability may be present at various levels. First, the brain of a young child is less mature and perhaps more vulnerable to the effects of significant cerebral damage, with disruptions occurring to rapidly developing neural networks, including subcortical and frontal regions. Brain damage may be attributable to the primary impact of injury plus secondary interruptions of ongoing cerebral development.16 Furthermore, young children possess little established skill and knowledge. Slowed processing and attentional impairment can affect future acquisition of cognitive and social skills, leading to cumulative impairment.33 In contrast, recovery from severe injury among older children is dramatic and consistent with adult recovery.33 Differences between these age groups could not be explained in terms of gender, SES, family factors, or preinjury abilities.

Outcomes for Specific Cognitive Domains (Children Injured at >3 Years of Age)
In the nonverbal domain, results are consistent with previous research29 that reported significant recovery after the insult. Furthermore, separation of perceptual and speed components of nonverbal tasks illustrated that, regardless of age at injury, both skill domains were more impaired after severe TBI and recovered significantly in the 30 months after injury. In contrast to reports from previous studies, verbal abilities were also reduced significantly for severely injured children, with these skills demonstrating little evidence of improvement after injury. Although previous research argued that this lack of "recovery" might reflect the relative stability of verbal skills in the context of early brain injury, our results showed a reduction in verbal skills immediately after the insult.

Specifically, verbal knowledge, word knowledge, abstract thought, and comprehension skills were depressed in both the early- and late-injured groups with severe TBI; this suggests impairment of verbal skills, which are in a rapid state of development throughout childhood. Finally, although attentional difficulties caused by TBI have been argued to underlie both verbal and nonverbal deficits, these skills were intact and stable over time in our sample. Such a finding might reflect the absence of attentional problems after TBI, although interpretation needs to be offered cautiously, because it is also possible that the measures used to assess attention were insensitive to the type of attentional problems caused by TBI.


   CONCLUSIONS
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
In the development of theoretical models for understanding the consequences of childhood brain injury, a wide range of factors must be considered. The present study has identified 2 such factors, ie, injury severity and age at injury. The previously established influence of injury severity was supported strongly by our data, with clear distinctions in performance between mild, moderate, and severe brain insults, both acutely and in the longer term after injury. Additional research, using more sophisticated neuroimaging techniques, may be able to delineate more clearly the aspects of injury most predictive of outcomes. The relative vulnerability of the immature brain to insult was supported for moderate and severe TBI but not for mild TBI, which argues for a "double-hazard" effect,34 in which a combination of severe injury and young age at insult leads to the poorest outcomes.

Long-term outcomes for children who exhibit both risk factors are also uncertain; however, our results support the importance of long-term clinical follow-up for children, to monitor cognitive recovery and to identify appropriate rehabilitation. It remains unclear whether these findings represent a permanent deficit or a delay in maturation and slowed recovery processes, with catch-up development observed in the subsequent months and years. Additional follow-up monitoring, with larger samples, is required to address this issue. Results encourage future studies examining chemical and structural correlates of these neurobehavioral recovery patterns, to achieve a better understanding of their biological bases.


   ACKNOWLEDGMENTS
 
This research was supported by grants from the National Health and Medical Research Council of Australia and the Royal Children’s Hospital Research Institute.

We thank the children and families who generously contributed their time to this research.


   FOOTNOTES
 
Accepted Feb 28, 2005.

Address correspondence to Vicki Anderson, PhD, Department of Psychology, Royal Children’s Hospital, Parkville, Victoria 3052, Australia. E-mail: vicki.anderson{at}rch.org.au

Author contributions were as follows: study supervisors: Dr Anderson and Ms Morse; study concept and design: Dr Anderson, Dr Catroppa, Ms Haritou, Ms Morse, and Mr Rosenfeld; acquisition of data: Dr Anderson, Dr Catroppa, Ms Haritou, Ms Morse, and Mr Rosenfeld; analysis and interpretation of data: Dr Anderson, Dr Catroppa, Ms Haritou, Ms Morse, and Mr Rosenfeld; drafting of the manuscript: Dr Anderson, Dr Catroppa, Ms Haritou, Ms Morse, and Mr Rosenfeld; critical revision of the manuscript for important intellectual content: Dr Anderson, Dr Catroppa, Ms Haritou, Ms Morse, and Mr Rosenfeld.

No conflict of interest declared.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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PEDIATRICS (ISSN 1098-4275). ©2005 by the American Academy of Pediatrics




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