Functional recovery following head injury among children

Functional recovery following head injury among children

Functional Recovery Following Head Injury* Among Children Arlene I. Greenspan, DrPH, PT H e a d injury is a p r i m a r y cause of death and disabilit...

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Functional Recovery Following Head Injury* Among Children Arlene I. Greenspan, DrPH, PT H e a d injury is a p r i m a r y cause of death and disability a m o n g children and adolescents. In 1985 approximately 78,000 children u n d e r the age of 15 were hospitalized for treatment of head injury. 1 On the basis of pilot data f r o m statewide surveillance systems in Colorado, Missouri, Oklahoma, and Utah, the Centers for Disease Control and P r e v e n t i o n (CDC) estimates the incidence of traumatic head injury at 93 per 100,000 for children u n d e r 5 years of age and 70 per 100,000 for children aged 5 to 14 years. 2 Improvements in acute management of head injury has resulted in greater s u r v i v o r s h i p a m o n g children w h o sustain severe head injury; however, m a n y of these children will be left with lifelong disabilities. In addition, changes in health care policy h a v e r e s u l t e d in shorter lengths of stay, f e w e r hospitalizations, and a greater involvement of the primary-care physician as a gatekeeper. As a result, pediatricians and other primary care physicians m a y be increasingly i n v o l v e d in the m a n a g e m e n t of children w h o have sustained head injuries.

* Researchers are increasingly using the term traumatic brain injury instead of head injury to describe cranio-cerebraltrauma. For this article, however, the term head injury is used throughout the text. While head injury and traumatic brain injury often are used interchangeably, head injury is a more inclusive term that includes brain and other intracranial injuries as well as skull fractures. Since several of the articles reviewed for this paper used the term head injury instead of traumatic brain injury, the more general term was chosen for both consistency and accuracy. Arlene I. Greenspan, DrPH, PT, is assistant professor in the departments of Rehabilitation Medicine and Neurology at Emory University School of Medicine. Curr Probl Pediatr 1996;26:170-7 Copyright 9 1996 by Mosby-Year Book, Inc. 0045-9380/96/$6.00 + .10 53/1/73544

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Although recovery from head injury has not been studied as extensively in children as in adults, a limited n u m b e r of l o n g i t u d i n a l studies h a v e been cond u c t e d over the past 15 to 20 years. These studies of children's recovery v a r y in quality; m a n y have small sample sizes, n o n u n i f o r m or subjective assessments of outcome, and short periods of follow-up. Further, very few of these studies have examined correlates of outcome b e y o n d stratifying the analysis b y severity of injury, age, and gender. Despite the shortcomings, these studies have p r o v i d e d some important insights about the extent and nature of sequelae, demonstrating a constellation of physical cognitive, and neuropsychological deficits associated with moderate and severe pediatric head i n j u r y Y 6 This article reviews the literature regarding functional r e c o v e r y f o l l o w i n g m o d e r a t e and severe head injury a m o n g children. Factors influencing r e c o v e r y will be discussed with emphasis on the influence of injury severity and the child's age at the time of injury. The m a i n p u r p o s e of this r e v i e w is to alert pediatricians and other primary care physicians about the functional deficits their patients m a y experience after a head injury, h o w these problems m a y change over time, and h o w new problems m a y emerge as children mature or b e c o m e more aware of their o w n limitations. Finally, recommendations for post-acute evaluation and treatment will also be addressed.

Severity of Injury The extent of cognitive, motor, a n d p s y c h o m o t o r deficits has been s h o w n to be correlated with the severity of the injury as defined by duration of posttraumatic amnesia (PTA) a n d b y d u r a t i o n and d e p t h of c o m a . 4"8'9'14'1s,17q9 Several studies have also demonstrated

an association between behavior changes and head injury severity, but this relationship appears to be weaker for behavioral changes than for cognitive deficits.6,2~In addition, the association between behavior changes and head injury severity may be limited to specific behaviors,s,16 Investigators generally agree that severity of injury is an important determinant of outcome, b u t there is little consensus about which measures best predict outcome. Consequently, comparisons among studies are difficult because of differences in measures and criteria used. Coma depth as measured by the Glasgow Coma Score (GCS), 21 duration of unconsciousness, PTA, and the Abbreviated Injury Score (AIS)22 are commonly used as measures of head injury severity. The GCS-one of the most widely used measures of head injury severity--is based on motor, verbal, and visual responses. Scores range from 3 to 15; a score of 8 or less typically is used to classify children with severe head injury; a score from 9 to 12 indicates moderate head injury, and 13 to 15 indicates mild head i n j u r y . 23 Duration of unconsciousness appears to be as good a predictor of outcome as GCS. 24 It is often difficult, however, to obtain an accurate measure of duration of unconsciousness, especially among children with mild to m o d e r a t e head injury, because injuries m a y be unwitnessed or witnessed by other children who may not be reliable at determining duration of unconsciousness. 24 Duration of PTA is the length of time the patient is unable to demonstrate ongoing memory of the events surrounding him or her. However, until the recent development of the Children's Orientation and Amnesia Test (COAT), measurement of PTA among children has lacked a standardized operational definition.25 The AIS is a widely used measure of injury severity that is based on anatomic descriptors of the injury22 with ordinal values ranging from 1 (minor injury) to 6 (maximum injury, virtually unsurvivable). The Injury Severity Score (ISS), based on AIS scores from different body regions, also provides a method for characterizing the combined effect of multiple injuries. 26 While each of these indices is associated with outcome, the literature suggests that measures that take into account not only the depth but the duration of impaired consciousness are most predictive of later disability. MacDonald et al.2. found that PTA as measured by the number of days to achieving 75% on the COAT and the number of days to achieving a GCS 15 were the two measures most associated with initial and 1-year outcomes. In another study, Michaud et al. 27 found that the GCS and motor GCS at 72 hours were more predictive of disability at discharge than initial GCS or ISS scores. Studies have also used different criteria to group patients by head injury severity. Investigators com-

monly classify head-injured children and adolescents into mild, moderate, and severe groups, s,12a5,18,28 However, comparisons across studies are further impeded because some investigators have compared children with severe head injuries with a combined mild and moderate g r o u p , 9-11,19,20,25 and others have compared children with mild head injuries with those children with severe head injuries. 4-6

Age Previous studies report conflicting findings about the influence of age on recovery from head injury. While some studies report similar or better outcomes among younger children in comparison with adolescents or adults,4'7-2931 others suggest that infants and young children may be at a disadvantage with respect to mortality, morbidity, and residual disability9,27,32-3s and that older children and adolescents may have better recoveries than adults. 32,37Differences in findings may be due to differences in methodology, specific outcomes measured, or age groups examined. For example, Chadwick et al.4 found no significant differences in cognitive recovery among severely head injured children aged 5 to 14, w h o were split into two g r o u p s according to whether they were older or younger than 10 years at the time of injury. However, their sample included children in a narrow age range and did not include preschool-aged children. Although Klonoff et al.7 included preschool-aged children in their follow-up of children with head injury, inclusion of all children under 9 years in the younger age group could have obscured any differential findings among preschool-aged children. In contrast, some recent studies that have included infants and preschool-aged children as a separate group generally have found worse outcomes among this youngest age g r o u p . 27"32'39'4~Age-related differences in etiology and mechanism of injury may result in different complications and outcomes even when neurologic indices of severity, e.g., GCS scores, are the same. 9,41 For example, Levin42 suggests that poorer outcomes among very young children may reflect a higher proportion of very young children who are victims of assault. Differences in outcome may also reflect increased vulnerability of the developing brain to traumatic insultY,3a Finally, Levin et aI. 1~hypothesize that specific cognitive and behavioral sequelae may not become apparent until the child is older and by then it may be difficult to attribute the problem to the initial head injury.

Cognitive Recovery Children who sustain head injuries can experience periods of PTA, anterograde amnesia, and retrograde

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amnesia that, once resolved, may leave children with intellectual as well as specific cognitive sequelae. Deficits in memory are one of the most commonly reported long-term sequelaeY Deficits in motor and processing speed, 5,8,~8,44attention and concentration,45,46and adaptive learning and problem solvingTM have also been reported. In addition, the acquistion of new skills may be more vulnerable to the effects of head injury than those skills requiring the use of already established processes. Since children's cognitive processes may not yet be fully established, they may be less able than adults to adapt to their impairments and may have more difficulty functioning in the environment.

Intelligence Investigators have generally reported an association between head-injury severity and intelligence scores, most notably performance IQ. 4,8.12-14,18In two separate studies Chadwick et al. 4 and Knights et al. 8 examined the impact of head injury on intelligence. While Chadwick et al. compared children with severe head injuries with a control group of children with orthopedic injuries and children with mild head injury, Knights et al. followed a cohort of children with mild, moderate, and severe head injury. Results from these two studies suggest: (1) an association between headinjury severity and intelligence scores as reported on the Wechsler Intelligence Scale for Children--Revised (WISC-R), (2) greater impairment with regard to performance compared to verbal IQ scores, and (3) greater speed and extent of recovery d u r i n g the first few months after injury. A l t h o u g h improvements were greatest in the first 3 to 4 months after injury, children continued to improve at a slower rate for the length of each of the study periods (9 months for Knight et al. and 2.3 years for Chadwick et al.). In addition, both studies found that children with the most severe injuries demonstrated persisting intellectual deficits, while children with mild and moderate injuries demonstrated either transient or no intellectual impairment. More recently, Jaffe et al. 12-18conducted a 3-year prospective follow-up of school-aged children with mild, moderate, and severe head injuries. Children with head injuries were compared with a control group matched for age, gender, school grade, and academic performance. In contrast to previous findings, Jaffe et al. reported intellectual deficits among children with moderate as well as severe head injuries. Recovery patterns also differed from previous studies. For overall and performance IQ scores, Jaffe et al. 15 reported recovery only during the first year after injury. With respect to verbal ability, scores remained essentially unchanged, indicating no recovery among children with moderate and severe head injuries compared with matched con-

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trols. Similar to previous studies, 5,8 Jaffe et al. 12-14reported higher scores in verbal performance and did not observe intellectual impairment among children with mild head injuries.

Specific Cognitive Deficits Deficits in specific cognitive abilities such as memory, problem solving, and processing speed may occur in the absence of any apparent intellectual deficit as indicated by the WISC-R after injury.8,18,47,48However, these cognitive deficits alone or in combination, can have a major effect on academic progress and success. Studies that have examined the effect of head injury on memory have identified persisting deficits in verbal and nonverbal recall?,1~ Yet, the extent and duration of recovery as well as the strength of the association between memory and head injury severity remain equivocal. In their study of the effects of closed head injury on immediate recall, Levin et al.9,1~reported deficits in both visual recognition and verbal recall of newly learned words among children and adolescents. Their findings demonstrated an association between deficits in verbal and visual memory and head-injury severity. While all groups demonstrated initial deficits that improved over the course of the year, at one year, only children and adolescents who had sustained severe head injuries continued to function below age level. The association b e t w e e n head injury severity and m e m o r y deficits was also demonstrated by EwingCobbs et al.28 whose cohort of 37 children and adolescents showed an association between verbal and nonverbal memory functions and duration of PTA at 6 and 12 months after injury. Moreover, patients whose PTA lasted 3 or more weeks demonstrated particularly poor outcomes. In contrast, Donders 49 examined the effects of head injury on immediate and delayed recall and did not find an association between head-injury severity and verbal recall and f o u n d only a n o n statistical trend between head-injury severity and figure recall. While children demonstrated deficits in both immediate and delayed recall, further deterioration between immediate and delayed recall was demonstrated only for verbal memory. Differences in findings may be due to relatively small sample sizes and differences in the timing of follow-up (e.g., the timing of the Donders study was not specified). Despite some conflicting results, all of these studies report residual deficits among children sustaining severe head injuries but most only report transient or minor deficits among children who have sustained mild to moderate head injuries. In contrast to these earlier studies, Fay et al. 14 demonstrated persisting short- and long-term verbal memory deficits among school-aged

children with moderate as well as severe head injuries 3 years after injury compared with matched controls. Although children with moderate and severe head injuries showed improvement during the first year after injury, no subsequent improvement was observed2 s In fact, while children with m o d e r a t e head injuries achieved scores similar to their matched controls and those with mild head injuries 1 year after injury, 1Bby 3 years children with moderate head injuries fell below their matched controls in both short- and long-term verbal performance. 15 As with memory, deficits in problem solving may become more evident over time. While Fay et al. ~4 reported deficits in adaptive problem solving among children with moderate and severe head injuries 3 years after injury, these deficits were not evident at 1-year testing for children with moderate head injury. Fay et al. concluded that moderate to severe head injury may disrupt the normal sequence of cognitive development and may interfere with the learning of new concepts needed in all areas of academic development. Finally, several investigators have observed deficits in activities that require speeded performance. 5~'~s'44 Bawden et al. 44 found that 1 year after injury, children with severe head injuries did significantly worse performing activities that required speeded cognitive processing or speeded movement than their counterparts with mild and moderate head injuries. In addition, their performance was worse on high-speed activities compared with activities that required moderate or low speed. Although Jaffe et al. ~5 and Fay et a124 also reported deficits in speeded performance 3 years after injury among children with severe head injury, they also found that performance of children with moderate injury was between performances of children with severe and mild injuries. Recent findings suggest that children with moderate as well as severe head injuries may be at risk for intellectual and specific cognitive deficits. Furthermore, children who score in the normal range on the WISC-R after head injury may still exhibit specific cognitive delays. Most important, deficits may not be evident immediately after injury and can take 2 to 3 years to become apparent. By then it is likely that children will no longer be undergoing rehabilitation and it may be up to the child's pediatrician to recognize emerging deficits and make referrals to appropriate specialists. Parents and teachers may be instrumental in recognizing a child's emerging problems and obtaining schoolbased services, although special educational services might not meet all of the child's rehabilitation needs. During routine or follow-up medical visits, parents should be q u e r i e d about their child's intellectual and academic performance. Evaluation by a neuro-

psychologist specializing in head injury should be considered, if problems become apparent.

Psychosocial Recovery/Behavior The extent and nature of b e h a v i o r a l and psychosocial consequences among children and adolescents with severe head injury are less well documented than cognitive deficits. Yet behavioral sequelae can be as, or more, disruptive to the child and family than cognitive or physical deficits. Very early behaviors of a patient recovering from a coma include confusion, agitation, aggressiveness, irritability, and lack of impulse controlY These behaviors can last from days to months and either stop or are replaced by other behaviors. The later sequelae are often the same disorders that appear among children w h o have not had head injury: hyperactivity, impulsivity, and aggressiveness. 8,5~Beyond this there are certain symptoms that appear more characteristic of the head-injured group, most striking of which is the syndrome of social disinhibition, 6,5~but the presence of behavior problems distinct to the head-injured population has also been disputed.20, 51 The relationship between behavior and head-injury severity appears weaker than the relationship between cognition and injury severity. 2~176While some investigators have not found significant differences among children with mild, moderate, or severe head injuries, 16,5~others report a weak relationship between behavior problems and injury severity. 6,s,2~Brown et al., 6 in their prospective follow-up of children with mild and severe head injuries, found that children who had sustained severe head injury and had no reported psychiatric disorder before the injury were more than twice as likely to have a psychiatric disorder after injury when compared with matched orthopedically injured controls. On the other hand, children with mild head injuries did not appear to be at any increased risk for psychiatric disorder after injury. In contrast to their findings about cognitive impairment, the appearance of psychiatric disorders appeared influenced by pre-injury behavioral characteristics and psychosocial adversity as well as by head-injury severity. These factors may account for the apparent weak relationship between head-injury severity and behavioral or psychiatric sequelae. Likewise, Knights et al. 8 reported an increase in behavior problems, including impulsivity, hyperactivity, irritability, and distractibility only among children with severe head injury. Fletcher et al. ~~ also found their group with severe head injuries to demonstrate declines in adaptive behavior, 6 and 12 months after the injury. In addition, while Greenspan and MacKenzie 16 did not find statistically significant differ-

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ences regarding behavior problems among children with mild, moderate, and severe head injuries, children with severe head injuries d e m o n s t r a t e d a slightly greater frequency of behavior problems. The literature thus suggests that behavior problems may be a direct result of the head injury or could be part of or exacerbated by the child's premorbid personality. As children regain cognitive skills and become more aware of their deficits, anxiety and depression may also become evident. Since even children with mild or moderate head injury can exhibit behavior problems, pediatricians should alert parents to possible problems and encourage them to call if problems arise. Parental concerns should be quickly addressed and children who demonstrated changes in personality, behavior problems, anxiety, or depression should be evaluated by a psychologist, neuropsychologist, or psychiatrist who specializes in treating children with head injury.

Motor Recovery Few studies have focused on motor recovery after pediatric head injury. Studies that have examined neuropsychological recovery after head injury report motor deficits in skills that require speeded m o v e m e n ~ but provide little detail concerning specific limitations and their impact on function. In one early follow-up of 46 children who were comatose for more than 1 week, Brink et al. 3 reported motor deficits in more than 90% of the children at least 1 year after injury. The most common motor deficits were spasticity and ataxia. All children demonstrated motor recovery, and 87% could walk i n d e p e n d e n t l y at least a short distance after completion of a comprehensive rehabilitation program. More recently, Chaplin et al. 52compared 14 children with moderate to severe head injury with non-headinjured controls using the Bruinink-Oseretsky Test for Motor Proficiency. Children were aged 5 to 15 years at testing and were more than I year post-injury. Although children with head injury scored significantly worse than controls on gross motor activities and scored similar to controls on fine motor tests, gross motor tests consisted of timed tests that required speeded movements. In the one fine-motor subtest that was timed, head-injured patients also scored significantly worse than non-head-injured controls. The investigators concluded that motor limitations after head injury persisted and were most likely to affect skills that required speed and precision. In another study, G r e e n s p a n and MacKenzie 16 interviewed the parents of 95 children, aged 5 to 15 years, with mild, moderate, and severe head injuries. One year after injury, 45% of parents reported at least one limitation in their child's physical health; of these, 40% reported limitations in their child's

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role activity (e.g., participation in school and play), 31~ limitations in physical activity, and 19% limitations in self-care or mobility. Although, poor physical health was associated with more severe injuries, children with mild and moderate head injuries also had significantly greater limitations when compared with children from the general population. While cognitive deficits may be more limiting to overall functioning than motor deficits, continuing problems in motor performance, especially activities requiring speed, will further affect the child's overall development and should be addressed with physical or occupational therapy.

Speech and Language Recovery As with motor recovery, few studies have focused on the speech and language sequelae after head injury among children. Early studies have reported deficits in verbal fluency and object naming 3,5,1s,19but did not provide comprehensive testing to determine the extent and nature of speech and language deficits. In a more recent study, Ewing-Cobbs et al. 38 conducted a followup of 56 school-aged children and adolescents with closed head injury 5 months after injury to determine the extent and nature of their language function. While they concurred with earlier findings of deficits in verbal fluency and naming, they also identified deficits in written-language skills that were more pronounced among children than adolescents. This finding is consistent with the hypothesis that emerging skills are more likely to be affected by cerebral insult than functions that are well established? 3 Although dysarthria is clearly apparent and is likely to result in referral to speech therapy, problems in language development may be more insidious. If children begin to demonstrate poor academic achievement, language delays should be considered. Evaluation in speech and language may be requested through the child's school or privately. A speech pathologist who has experience with children with head injuries should be requested.

Rehabilitation Most children who sustain moderate or severe head injury will require initial hospitalization. At that time, patients should be evaluated to determine the number, nature, and extent of their impairments and functional limitations. Once medically stable, children with severe or multiple impairments may be transferred to an inpatient rehabilitation hospital. Rehabilitation hospitals or units that specialize in the treatment of traumatic head injury usually offer a coordinated approach to

rehabilitation and provide a broad array of services including neuropsychology, psychological and social w o r k counseling, physical therapy, occupational therapy, speech therapy, educational remediation, recreational therapy, rehabilitative nursing, and dietary/ nutritional monitoring, s4,55For children with less-severe impairments, services may be provided on an outpatient basis. Programs that provide coordinated and comprehensive outpatient rehabilitation are preferable to individual services but may not be available in all communities. As suck it may be necessary to refer patients to individual practitioners or therapists. Children may also benefit from school-based rehabilitation and special educational services. In addition, families may need counseling as well as a variety of social services to help them cope with their child's injury and resulting disability. Although the effectiveness of head injury rehabilitation has not been rigorously evaluated, recent evidence suggests that rehabilitation does not just expedite recovery, but improves functional outcomes over what would be expected from spontaneous recovery. 55,56 Yet, it has been estimated that only I in 20 persons with head injury receives appropriate rehabilitation services. 57 While percentages m a y vary, recent studies suggest that not all children are receiving needed services. In one study that identified predictors for referral to inpatient rehabilitation after pediatric injury, Osberg et al. s8 found that although discharge to an inpatient rehabilitation unit or center was influenced by the number and type of functional impairments present, children were also more likely to be referred for inpatient rehabilitation if they had received their initial care at a Level 1 trauma center or a trauma center with an onsite rehabilitation unit. While it appeared that there were few inappropriate referrals to inpatient rehabilitation from centers with onsite units, the results suggested that some patients who would have benefitted from inpatient rehabilitation were not referred. In another study, the parents of 95 children with head injuries were interviewed by telephone 1 year after injury. 59 Parents were read a list of 28 behavior problems and were asked to indicate whether their child exhibited any of the behaviors during the past 3 months. A total of 42 parents reported 14 or more behavior problems in their children, yet only 10 of those parents reported that their child had received any mental health services since the injury. Children with the most severe injuries were most likely to receive services, whereas children with mild to moderate injuries who may have exhibited more subtle problems or may not have been expected to have residual disability were least likely to receive any services. Pediatricians can play a pivotal role in ensuring that

their patients and their families receive appropriate services. First, some impairments may not be recognized until the child has gone home from the hospital, and the pediatrician may be the first provider to be consulted. Second, the pediatrician may be the only physician who knew the child before injury, and therefore may have insight into deficits that could be overlooked by specialists who have treated the child only since his or her injury. Third, problems with learning may become evident only as greater demands are placed on the child or with maturation. Such deficits may not become apparent until months or years after the injury, when the child is no longer being followed up for problems related to the head injury. Finally, knowledge of the family may be helpful when recommending services that will meet the child's needs and be realistic for the family.

Conclusions As more children with moderate and severe head injuries survive and return home, the pediatrician has become an important link among the child, the family, and the rehabilitation community. While children who have sustained severe head injuries are likely to demonstrate persisting deficits or problems in cognitive ability, behavior, motor ability, or speech and language function, recent evidence suggests that children with moderate head injuries may also be at increased risk for these same functional deficits. In addition, specific cognitive deficits may not become apparent for several months or years after the initial injury occurs. Once the initial rehabilitation process has been completed, the pediatrician may be the first person parents turn to when new problems arise, new deficits become apparent, or it becomes more difficult to manage those deficits that may worsen as their child matures. For some, the need for rehabilitation may not become apparent until the child is discharged home and increased demands illuminate more subtle deficits. For others, poor coordination of services, lack of communication about available services, or problems accessing services may result in less-than-optimal outcomes and inadequate service utilization. Pediatricians cannot be expected to be experts in identifying and treating deficits acquired from head injury, but they need to be aware that recovery from head injury is a dynamic process that does not end when the child is discharged from the hospital or when the acute phase of rehabilitation ends. Thus referral to rehabilitation services m a y be needed later, if the child begins to have difficulty with the acquisition of new skills or begins to have greater difficulty with the increasing demands and stresses of school, recreation, employment, and interpersonal relationships.

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Acknowledgment I appreciate the thoughtful comments of Drs. Joseph Sniezek, Rick Waxweiler, and Ellen MacKenzie

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