- Email: [email protected]
Recovery from mild head injury in pediatric populations
Recovery from Mild Head Injury in Pediatric Populations Matthew D. Thompson and James W. Irby Jr This article provides an overview of the diagnosis, classification, and pathophysiology of mild head injury (MHI) in children. The difficulties associated with determination of MHI severity are outlined. Also, recently published research pertaining to pediatric MHI is reviewed. The recent research pertaining to MHI in children is generally consistent with the conclusions reached by the authors of the most recent comprehensive review, which reported that children who have suffered MHI often experience a symptomatic phase that could extend up to a few months, but these symptoms usually resolve. Numerous preinjury variables have been identified, including premorbid learning and behavior problems, disadvantaged socioeconomic status, premorbid neurodevelopmental abnormalities, and adverse family conditions, that appear to explain the persistence of some symptoms experienced by a subset of children with MHI. Directions for future research are provided. © 2003 Elsevier Inc. All rights reserved.
H
EAD INJURY during childhood and adolescence is a major cause of acquired disability. Although estimates of incidence vary widely, a comprehensive review by Kraus revealed an average annual incidence of 180 head injuries per 100,000 children per year.1 Mild head injury (MHI) appears to be the most prevalent form of head injury in children and adults. The U.S. National Coma Data Bank2 indicates that approximately 85% of all head injuries requiring medical treatment are classified as mild. The National Pediatric Trauma Registry3 also indicates a predominance of MHIs, with 76% of injuries classified as mild. Reports pertaining to the frequency of MHI in children are likely to underestimate the actual incidence, due to the high number of unreported MHIs and head injuries that are overlooked due to a focus on orthopedic or other non– central nervous system (CNS) injuries.4,5 The long-term impact of severe head injury is well-documented,6-8 but outcome associated with MHI is less clear. Before the early 1980s, studies on the effect of MHI in children were limited, possibly due to the misunderstanding of the longaccepted plasticity hypothesis, which suggests that neurobehavioral recovery after brain injury is better tolerated by children than by adults.9 A surge of
From Children’s Hospital, Department of Psychology and Department of Pediatrics, Louisiana State University Health Sciences Center, New Orleans, LA and Laboratoria de Estudos de Linguagem, Centro de Estudios Egas Moniz, Hospital Santa Maria, Lisbon, Portugal. Address reprint requests to Matthew D. Thompson, PsyD, Children’s Hospital, Department of Psychology, 200 Henry Clay Avenue, New Orleans, LA 70118. © 2003 Elsevier Inc. All rights reserved. 1071-9091/03/1002-0000$30.00/0 doi:10.1016/S1071-9091(03)00021-4 130
interest and research in pediatric MHI was prompted in the early 1980s by Boll,10 who stated that MHI in children was a silent epidemic. More recently, even more interest in MHI in children has been spurred by the increased attention to sportsrelated head injuries.11 Comprehensive reviews pertaining to the cognitive status of children who have experienced MHI have differed in their conclusions.12,13 Since the publication of the most recent comprehensive literature reviews, several well-constructed empirical studies have been published that contribute valuable information to the growing body of literature on pediatric MHI. This article provides general information on the diagnosis, pathophysiology, and outcome of MHI in children, particularly as described in recent publications. DIAGNOSIS AND CLASSIFICATION OF MILD HEAD INJURY
Various head injury classification and diagnostic systems have been proposed. Most of these systems involve the assessment of mental status and other neurologic variables. The most commonly used classification system is the Glasgow Coma Scale (GCS),14 which evaluates three variables: eye opening, motor response, and verbal response. Each variable is graded (eye opening, 1 to 4; motor response, 1 to 6; verbal response, 1 to 5), with a lower score indicating greater impairment. The total score ranges from 3 (most severe) to 15 (essentially normal). Traditionally, GCS scores from 13 to 15 represent mild injuries, scores from 9 to 12 represent moderate injuries, and scores of 8 or less represent severe injuries.15 Several factors associated with GCS assessment introduce considerable variability into empirical studies as well as clinical interpretation. One of these factors is the Seminars in Pediatric Neurology, Vol 10, No 2 (June), 2003: pp 130-139
RECOVERY FROM MILD HEAD INJURY
Table 1.
131
MHI Definition Proposed by the American Congress of Rehabilitation Medicine
A patient with mild traumatic brain injury is a person who has had a traumatically induced physiologic disruption of brain function as manifested by at least one of the following: 1. Any period of loss of consciousness 2. Any loss of memory for events immediately before or after the accident 3. Any alteration in mental state at the time of the accident (e.g., feeling dazed, disoriented, or confused) 4. Focal neurologic deficit(s) that may or may not be transient, but where the severity of the injury does not exceed the following: 1. Loss of consciousness of approximately 30 minutes or less 2. After 30 minutes, an initial Glasgow coma scale score of 13-15 3. Posttraumatic amnesia not greater than 24 hours.
amount of time elapsed since injury at the time that the GCS assessment is obtained. If a child has been intubated or sedated at the time of GCS assessment, the score will be depressed. Also, GCS assessment with infants and toddlers who are preverbal may result in an artificially depressed score. Length of posttraumatic amnesia (PTA) is also used to grade the severity of head injury. Although definitions vary, PTA is usually described as the lack of memory for ongoing events (ie, anterograde amnesia).6 Significant variability exists in opinions pertaining to the length of PTA and its corresponding severity level, but in general, PTA of less than 24 hours duration is generally considered to represent a mild head injury, whereas PTA of 1 to 7 days duration is considered moderate and PTA of 8 or more days duration is considered severe.6 The assessment of PTA, when conducted retrospectively, is complicated by the subjective nature of self-report. This difficulty is magnified in children due to developmental limitations. At least one formal measure of PTA, the Children’s Orientation and Amnesia Test (COAT), has been designed for use with children.16 The COAT consists of 16 items evaluating (1) general orientation to person and place and recall of biographical information, (2) temporal orientation, and (3) memory (immediate, short-term, and remote). Normative data are available for the COAT, and cutoff scores have been established that have adequate predictive validity.17 In a group of children who sustained closed-head injury, both verbal and nonverbal memory scores were significantly more impaired at 6 and 12 months after the injury in patients with PTA persisting for at least 3 weeks (as determined by serial COAT administration) than in patients whose disorientation, confusion, and gross amnesia resolved within 1 week. Duration of postinjury unconsciousness, opera-
tionally defined as the length of time between injury and ability to follow a command, has also been used as an index of head injury severity. This variable is similar to the motor response portion of the GCS, in which a score of 6 is recorded when the child is able to follow a motor command. A severe injury is usually considered to have occurred when the duration of unconsciousness exceeds 24 hours,17 but there continues to be some inconsistency and debate regarding the duration of unconsciousness associated with the classification of mild or moderate head injury. The most recent and inclusive definition of MHI, which was designed with the goal of promoting uniformity across studies, was developed by the Mild Traumatic Brain Injury Committee of the Head Injury Interdisciplinary Special Interest Group of the American Congress of Rehabilitation Medicine (ACRM)18 and is presented in Table 1. Although this definition clearly defines the upper limits of MHI, the lower limits are less clear. Under the definition proposed by the ACRM, individuals with a mechanical force applied to the head and alteration in mental status (eg, feeling dazed) are considered to have a mild traumatic brain injury and would be grouped with individuals with up to 30 minutes of unconsciousness. More recently, the MHI classification has been further delineated by designating a complicated MHI category, which describes an injury that would be classified as mild based on GCS score, duration of unconsciousness, and duration of PTA, but where there is evidence of an abnormality seen on computed tomography (CT) or magnetic resonance imaging (MRI), including brain lesions and/or skull fractures.19 In adults, patients with uncomplicated MHI had a better outcome at 6 months postinjury relative to patients with complicated MHI.19 It should be noted that many patients
132
with complicated MHI, as defined here, would have been included in the moderate traumatic brain injury (TBI) group in many studies.20 The term concussion has been used interchangeably with MHI, but it usually refers to milder injuries on the MHI spectrum. The precision of MHI description and classification can be augmented by considering various systems that describe the severity of a concussion. These classification systems are usually applied in the context of athletic injuries and return-to-play decisions.21 In 1991, the Sports Medicine Committee of the Colorado Medical Society developed definitions of three levels of concussion (mild, moderate, and severe) along with guidelines for management.22 Each level of concussion was described according to length of unconsciousness: no loss of consciousness, less than a 5-minute loss of consciousness, and more than a 5-minute loss of consciousness. The most recent concussion severity rating scale was published by the Quality Standards Subcommittee of the American Academy of Neurology (AAN) in 1997.23 Under the AAN guidelines, a grade 1 concussion is defined as symptoms lasting less than 15 minutes, with transient confusion and no loss of consciousness. Grade 2 concussion involves symptoms lasting more than 15 minutes, no loss of consciousness, and transient confusion. Grade 3 concussion is defined as loss of consciousness that is either brief or prolonged. The AAN guidelines are notable for the emphasis on confusion and amnesia, whereas previous guidelines had placed more emphasis on loss of consciousness. PATHOPHYSIOLOGY OF MILD HEAD INJURY
The neuropathologic effects of MHI are controversial relative to the known adverse effects of severe head injury. Head trauma can cause brain injury as a result of three mechanisms: (1) focal hemorrhagic and nonhemorrhagic lesions, (2) diffuse axonal injury (DAI), and (3) secondary injury caused by edema and space-occupying hemorrhages.24 DAI is of particular interest in the study of MHI. DAI is defined as widespread injury to axons in the white matter of the brain induced by transient application of tensile strain.25 The definition and use of the term DAI has evolved over the years. The original definition of DAI was prolonged traumatic coma not associated with mass lesions or
THOMPSON AND IRBY
ischemic damage.26 The question is whether DAI also occurs in MHI. DAI requires a sudden acceleration-deceleration force,25,27 which stretches delicate axonal fibers. If the injury-inducing forces are not too great, then the only injury to the axon is a temporary stagnation of axonal transport. If the forces are severe enough, then axonal transection may occur with death of the axonal segment and sealing off of the proximal axonal stump.28 The distal axon is subsequently phagocytosed by microglial cells, producing microglial clusters. Once axonal transport resumes, the products being transported from the cell body accumulate at the site of the axonal damage, causing it to balloon up into an axonal retraction ball.29 The amount of force needed to cause axonal stagnation is unknown, as is the threshold for axonal transection.30 Axon retraction balls and microglial clusters are microscopic indicators of DAI.30 Indirect evidence of severe DAI can be seen on MRI as small, ovoid, low-attenuation lesions with their long axis parallel to the direction of the affected axon.31 Other circumstantial evidence is the presence of petechial hemorrhages, particularly at the gray–white junction and corpus callosum.32 Definitive determination of DAI is possible only with pathologic examination. The most quoted study of pathologically confirmed DAI in cases of MHI has been Oppenheimer’s 1968 report on five patients who experienced MHI and subsequently died due to unrelated causes.33 In one case, microglial clusters and axon retraction balls were found in a patient who died of pneumonia 13 days after suffering a MHI. The patient had been knocked down by a motor scooter and suffered a parietal bruise but no skull fracture. Four other patients who suffered MHI but later died for reasons unrelated to their head injury were included in the study, and evidence of microglial clusters, but not axon retraction balls, was reported. Others have noted that microglial clusters may be seen as part of an immune response to such insults as anoxia.27,30 Oppenheimer’s study has not yet been replicated. Other investigators using a similar research design have found microscopic evidence of disturbed axonal transport, but not axon retraction balls or microglial clusters.26 When considered as a whole, the literature suggests that some people who suffer severe head injuries show evidence of DAI. Individuals with
RECOVERY FROM MILD HEAD INJURY
MHI, however, may experience a transient alteration of biochemical and cellular function in the brain, but there is not sufficient evidence to conclude that people with MHI develop DAI in the absence of a loss of consciousness and considerable deceleration forces. ACUTE EFFECTS OF MILD HEAD INJURY IN CHILDREN
The constellation of acute symptoms after MHI is typically referred to as postconcussion syndrome (PCS). In adults, these symptoms include somatic complaints (headache, dizziness, fatigue, blurry or double vision, noise intolerance, and light sensitivity), emotional changes (depression, anxiety, irritability), and cognitive difficulties (subjective complaints of poor concentration and impaired memory). Diagnostic criteria for PCS are included in the International Statistical Classification of Diseases and Related Health Problems, 10th edition (ICD-10),34 and research criteria for PCS are included in the Diagnostic and Statistical Manual of Mental Disorders, 4th edition (DSM-IV).35 Several studies have determined that children also experience similar somatic and emotional postconcussive symptoms in the weeks after sustaining MHI.20,36-38 Farmer et al36 compared the behavioral symptoms from a large sample (n ⫽ 247) of children with MHI with those from a control group of 280 children who had sustained injuries to other areas of the body. Within the first week after injury, complaints of irritability, clinging behavior, and sleep disturbance were common in both groups, but only headaches were more frequently experienced by the head-injured children relative to the control group. Ponsford et al38 found that relative to children with other injuries (n ⫽ 96), children with MHI (n ⫽ 130) experienced not only significantly more headaches, but also more dizziness and fatigue at 1 week postinjury. By 3 months postinjury, the postconcussion symptoms had resolved. Other studies have found no adverse postconcussion effects at 4 months39 or 6 months postinjury.40,41 However, Ponsford et al38 noted that at 3 months postinjury, 17% of the children with MHI in her study were experiencing significant ongoing postconcussion symptoms and problems, which appeared to be related to preexisting factors (ie, previous head injury or preexisting learning, neurologic, or psychosocial problems). Yeates et al37 also reported that
133
postconcussion symptoms observed at 3 months postinjury in a series of 26 children with MHI were associated with premorbid neurologic and psychosocial problems. Mittenberg et al20 specifically examined the self-reports of postconcussion symptoms in 38 children with MHI, 27 children with moderate head injury, and 47 children with orthopedic injuries. At 6 weeks postinjury, the head injury groups reported significantly more symptoms than did the orthopedic injury group. The symptoms were related to the severity of head injury and also to the child’s anxiety level. Luis and Mittenberg42 also found that relative to children who sustained orthopedic injuries, children who sustained MHI were at an increased risk for developing anxiety and depression 6 months postinjury. Regarding acute cognitive symptoms after MHI in children, Ponsford et al38 found no evidence of cognitive impairment at 1 week or 3 months postinjury, even among the 17% of the MHI group who reported continuing postconcussion symptoms. However, it was noted that the cognitive assessment battery was relatively limited. Using a more extensive battery, Anderson et al43 did not find any significant effects on measures of intelligence, spatial memory, or auditory comprehension in young children (age 3 to 7) 3 months post-MHI, but children with MHI performed significantly worse than normal controls on measures of story recall and verbal fluency. Catroppa and Anderson44,45 also found that MHI children performed below age expectations 3 months postinjury, further suggesting that MHI in children may impact a child’s ability to encode and consolidate new verbal information in the months after the injury. It was noted, however, that MHI children made ongoing and often dramatic improvement in verbal abilities at 6 months, 12 months, and 30 months postinjury.43,44 In summary, MHI in children results in increased rates of somatic and emotional complaints including headaches, dizziness, and fatigue in the first few weeks after MHI, but these symptoms usually resolve by 3 months postinjury. In some children, cognitive difficulties are also evident on tests of higher-order cognitive processes (ie, verbal fluency and verbal memory consolidation) in the first several months postinjury, but these also usually resolve over time. These findings are also consistent with the acute effects of concussion as
134
THOMPSON AND IRBY
documented in the sports-related concussion literature.46,47 Despite the finding that cognitive and somatic symptoms usually resolve in most children, it appears that a subset of children continue to experience postconcussion difficulties after MHI. We address the variables associated with this subset of children later in this article. LONG-TERM OUTCOME OF MILD HEAD INJURY IN CHILDREN
There is considerable controversy regarding the long-term outcome after MHI. Some of the earlier reviews10,12,48 suggested that MHI in children led to symptoms that affected cognitive, academic, and psychosocial functioning and that these symptoms could be devastating to a child’s development. However, in their influential review, Satz et al13 pointed out that many of the studies on which these earlier reviews were based had methodologic flaws that significantly limited their generalizability (eg, pooling moderate and mild head injury cases and making inferences from adult populations). Satz et al suggested six key methodologic criteria essential for research in this area: (1) inclusion of an appropriate control group, (2) use of a longitudinal design with follow-up assessment after the injury, (3) clear definition of MHI, with no inclusion of children with more severe injuries, (4) control for preinjury factors, (5) inclusion of at least 20 children with MHI, and (6) use of standardized assessment measures. Based on 40 outcome studies of MHI in children published between 1970 and 1995 that met at least four of these six research criteria, Satz reached the conclusion that MHI in children might result in a mild but transitory alteration in cognitive functioning (ie, attention and memory), but no reliable changes in academic or psychosocial functioning. However, Satz pointed out that the studies that found no effect on academic or psychosocial functioning were cases selected from the very mild end of the severity spectrum, whereas the studies that found weak but transient cognitive alterations came from the more severe end of this spectrum. Satz also noted that as severity within the MHI spectrum increased, more variability in findings was reported, suggesting that within the spectrum of MHI, there may be a degree of mild injury that reaches a threshold of concern. Since the publication of the review by Satz et al, several studies have been published that have incorporated Satz’s suggested research criteria. Us-
ing a prospective longitudinal design, Anderson et al43 examined the effect of MHI in 17 young children (age 3 to 7) using standardized measures of adaptive, behavioral, and cognitive functioning at the time of initial hospitalization and at 6 and 30 months postinjury. The children were recruited from a neurosurgery ward where they had been admitted after sustaining a MHI, which was defined as an admission GCS score of 13 to 15, an indication of some alteration of consciousness, no deterioration of consciousness after admission, no mass lesion seen on CT/MRI, and no neurologic deficit. Children were excluded if they had any previous history of head injury and any evidence of neurologic, psychiatric, or developmental disorder. Preinjury adaptive and behavioral functioning was gathered from the parents at the time of initial admission. A group of 35 healthy children matched as closely as possible on demographic variables was used as a control group. No significant differences were noted between the two groups on most cognitive measures (ie, intellectual, speed of processing, attention, everyday and spatial memory, receptive vocabulary, and auditory comprehension) at the acute stage and at 30 months postinjury. No significant differences between the two groups were noted on parent-reported measures of adaptive and behavioral functioning at the acute stage and at 30 months postinjury, although trends toward slightly more reported symptoms of social incompetence and internalization/somatic complaints were noted for the MHI group at 12 and 30 months postinjury. Also, the MHI group performed significantly worse than the control group on measures of story recall at all time points and verbal fluency at 30 months postinjury, suggesting that MHI may produce impairment in certain high-level language-based skills. Anderson et al noted that the MHI group demonstrated ongoing improvements on these measures over time, and suggested that their impairments represented a transient interruption of brain function and a resultant delay in skill acquisition rather than a permanent deficit. Based on their overall findings, the authors concluded that their study provides support for a generally good outcome for children sustaining a MHI during the preschool years. Light et al49 investigated behavior problems and academic performance in a group of children with MHI at 1 year postinjury. Children between age 8 and 16 who sustained MHI (n ⫽ 137) were pro-
RECOVERY FROM MILD HEAD INJURY
spectively recruited after emergency room admission and compared with 132 children with injuries that did not involve the brain or head and 114 children with no injuries. None of the children in the MHI group required hospitalization. Based on preinjury and postinjury parental ratings of the children’s behavior and academic records obtained from the schools, a significant difference was noted between the two injured groups of children and the healthy controls at 1 year postinjury. A greater degree of preinjury behavioral problems was found in the MHI group and other-injured group relative to the noninjured control group, differences that might have been attributed to MHI had the authors not included an other-injured control group. As described previously in the discussion of acute effects of MHI, Ponsford et al38 evaluated 130 children between age 6 and 15 with MHI as defined by the ACRM. At approximately 1 week postinjury, a significant proportion of these children reported postconcussion symptoms, but no cognitive impairments were measured for the children as a group relative to controls, even though the cognitive assessment battery was relatively limited. Three months later, the postconcussion symptoms had largely resolved in the group, but 17% exhibited ongoing problems. Investigation of premorbid status revealed that the symptomatic children were more likely to have a history of previous head injury, learning difficulties, neurologic or psychiatric problems, or family stressors. McKinlay et al,50 incorporating all six of Satz’s recommendations, followed annually to age 10 to 13 all of the children born in their region of New Zealand during an approximate 4-month period in 1977. Of the 1265 children born during that period, 132 sustained MHI before age 10. (In this study, a child with MHI was defined as any child who received medical attention for concussion or suspected concussion.) Children were excluded if loss of consciousness lasted longer than 20 minutes, if hospitalization was for more than 2 days, or if skull fracture occurred. Children with nonspecific head injuries were also excluded. In an attempt to operationalize and grade the severity of MHI, the cases were divided into those receiving outpatient care (n ⫽ 96) and those receiving inpatient care (n ⫽ 36). Because of the epidemiologic nature of the study, it was possible to use a large control group (n ⫽ 613 to 807) that was identical in age and highly comparable in terms of education, fam-
135
ily background, and socioeconomic status, and thereby control for some of the potential confounding factors related to preinjury factors or family characteristics. Throughout the course of the study, data were gathered from the participant’s families and teachers, and a range of standardized cognitive, academic, and behavioral assessment measures were used at regular intervals. The results indicated that children who received inpatient care for MHI between age 0 and 10 displayed increased hyperactivity/inattention and conduct disorder behavior between age 10 and 13, especially if the injury occurred before age 5. These results were reliable after statistical control of a wide range of potential confounding factors, including preinjury factors, was applied. No significant effects were noted on cognitive or academic measures, regardless of injury severity, and no significant differences were noted between the outpatient MHI participants and the noninjured control group on psychosocial measures. McKinlay et al concluded that although most cases of MHI in children do not produce adverse effects, it is not always a completely benign event, and long-term problems in psychosocial functioning are more likely at the upper end of the MHI severity spectrum. In another study involving a large cohort of children with MHI, Bijur et al51 assessed the cumulative effects of multiple MHI on cognitive functioning. The sample included 1586 children with 1 MHI, 278 children with 2 MHIs, and 51 children with 3 or more MHIs between birth and age 10 years. The control group included children without head injuries but matched to the clinical sample on total number of injuries. The numbers of head injuries and nonhead injuries were found to be associated with decreasing performance on measures of cognitive and academic functioning. After adjusting for psychosocial variables, the relationship between number of injuries and cognitive outcomes became nonsignificant. Ponsford et al52 studied a group of 119 children with MHI as defined by ACRM criteria. Sixty-one participants were assigned to an intervention group and evaluated 1 week and 3 months after injury, and 58 participants were assigned to a nonintervention group and assessed 3 months after injury. They were compared with two control groups of children with minor injuries not involving the head. Parents and children in the intervention group were provided with a booklet describing
136
THOMPSON AND IRBY
typical MHI symptoms and coping methods. Preinjury behavioral adjustment of children in the intervention group and the control groups was assessed by asking parents to complete behavioral rating inventories as they applied to premorbid behavior and psychological adjustment. Standardized measures of postconcussion symptoms and neuropsychological skills were also administered. Children with MHI reported more symptoms than controls at 1 week postinjury but demonstrated no impairment on neuropsychological measures. Initial postconcussion symptoms had resolved for most children by 3 months postinjury, but a small group of children who had a previous head injury or a history of learning or behavioral difficulties reported ongoing problems. The group not seen at 1 week postinjury and not given the information booklet (ie, the nonintervention group) reported more symptoms overall and was more symptomatic 3 months after injury. PSYCHOSOCIAL RISK FACTORS
As illustrated by many of the MHI studies described thus far, psychosocial risk factors emerge as a critical factor in recovery from MHI. Psychosocial risk factors in the context of MHI include premorbid learning and behavior problems, disadvantaged socioeconomic status, premorbid neurodevelopmental abnormalities, or adverse family conditions. For example, Light et al49 found that children with injuries necessitating a visit to the emergency room had slightly elevated rates of behavioral problems, regardless of the type of injury (eg, CNS or non-CNS). Ponsford et al38 found that children with MHI who exhibited residual symptoms were more likely to have a history of previous head injury, learning difficulties, neurologic or psychiatric problems, or family stressors. The importance of considering preinjury risk factors is also exemplified by the University of California Los Angeles study of MHI,40 which indicated that for certain outcome measures, the effects of certain preinjury factors (eg, history of learning and school problems) were larger than the effects of MHI. Likewise, Bijur et al51 found that adverse cognitive and academic outcomes were explained by premorbid psychosocial factors rather than acquired brain damage. Compared to research pertaining to the role of psychosocial variables in children with MHI, rel-
atively more research has been conducted investigating the role of these variables in children with moderate and severe head injuries, and the findings from these studies consistently indicate that environmental and psychosocial disadvantages exacerbate the adverse effects of head injury. For example, general measures of socioeconomic status and family demographics have been found to influence outcome.53 Concerning more specific measures of premorbid family functioning as well as postinjury family functioning, Yeates et al54 documented a significant correlation between performance on neuropsychological tests and formal measures of family functioning in a group of children with severe head injuries. The same correlation was not found in a group of children with orthopedic injuries, suggesting an interaction between environmental variables and injury type. The same study reported that measures of family environment accounted for 25% of the variance in level of outcome, after controlling for severity of head injury. Interestingly, after controlling for family environment, age at injury, and ethnic status, head injury severity accounted for only 20% of the variance in outcome. Given the growing body of literature indicating the significant role of psychosocial variables in the outcome of pediatric head injury, considering these factors in clinical practice and empirical research is critical. Satz13 recommended controlling for premorbid risk factors in future studies not by exclusion, but rather by using designs that permit statistical as well as experimental controls. SUMMARY AND CONCLUSIONS
The conclusions from this review of recent studies on the effect of MHI on children are generally consistent with those of Satz et al.13 Most children who experience MHI will experience few, if any, permanent adverse cognitive, behavioral, or psychosocial outcomes, especially if the injury is on the mild end of the MHI severity spectrum. The most common symptoms during the first week after MHI are headaches, dizziness, and fatigue, which are usually completely resolved within the first month postinjury.36-41 Despite these postconcussive symptoms, some studies suggest most children do not experience significant cognitive dysfunction immediately after MHI,38 but other studies suggest that some children with head inju-
RECOVERY FROM MILD HEAD INJURY
137
ries toward the severe end of the MHI spectrum (ie, required hospital admission) may experience subtle difficulties with encoding and consolidation of new verbal information during the acute phase.43-45 Long-term follow-up studies reveal a generally positive outcome for most children with MHI; however, several studies have reported that there is a sizable minority of children who continue to experience ongoing cognitive and psychosocial difficulties in the months after MHI.38,45,49,51,52 It appears that those children who develop persistent symptoms are more likely to have preexisting neurologic, psychiatric, or family problems,38,45,49,51,52 but one recent study did find evidence that even previously healthy children may experience a transient delay in acquisition of higher-level language-based skills.43 Also, another group found that preexisting difficulties do not fully account for all adverse, long-term psychosocial consequences (eg, hyperactivity/inattention and conduct problems), particularly if the head injury occurs during the preschool years and is toward the severe end of the MHI severity spectrum.50 One of the key issues in the MHI literature, for both children and adults, is defining MHI and determining the severity of MHI. Research over the past several years has generally supported the notion that there is a threshold of concern within the spectrum of MHI. The parameters of this threshold, and how they are determined, remains an issue of debate and a subject for further research. Satz and his colleagues have argued that head injury severity is a dimensional construct that does not easily lend itself to arbitrary cutoff points, and that attempts to establish a consensus definition of MHI tend to reify arbitrary distinctions. Rather, it is argued that operational definitions of closed head injury severity are needed along multiple dimensions (eg, loss of consciousness, posttraumatic amnesia). Hence one important area for future research is in the further validation of such assessment techniques as the COAT. Given the potential that some children, particu-
larly those with premorbid risk factors, may experience an incomplete recovery following MHI, it behooves the clinician to monitor the symptoms of MHI for several months so that appropriate interventions can be implemented. Toward this end, Ponsford52 has demonstrated that providing parents with an information booklet reduces anxiety among the families of children who have suffered MHI and lowers the reported incidence of ongoing postconcussive symptoms. Roberts55 conceptualized the difficulties that some children experience after MHI as episodic in nature and suggested that these difficulties may not always be observed in the office setting. Clinicians often overlook such episodic symptoms, and Roberts argued for the paramount importance of specifically querying for these symptoms during the clinical interview. One of the reasons MHI is such a contentious area in the adult literature is due to litigation, which has fueled a considerable amount of research into the effects of litigation status on selfreport of postconcussion symptoms and performance on neuropsychological tests. In general, it has been demonstrated that litigation status has a significant impact on the persistence of postconcussion symptoms.56,57 We have not come across any studies that have investigated the impact of litigation status on the outcomes of children with MHI, but it is not unreasonable to consider whether involvement in litigation poses a threat to the validity of parent reports pertaining to their children who have suffered a MHI. The recent research pertaining to MHI in children is generally consistent with the conclusions reached by the authors of the most recent comprehensive review,13 which reported that children who have suffered MHI often experience a symptomatic phase that could extend up to a few months, but these symptoms usually resolve. Recent research has also identified risk factors that often explain the persistence of certain symptoms in a subset of children.
REFERENCES 1. Kraus JF: Epidemiological features of brain injury in children: Occurrence, children at risk, causes and manner of injury, severity, and outcomes, in Broman SH, Michel ME (eds): Traumatic Head Injury in Children. New York, Oxford University Press, 1995, pp 22-39 2. Luerssen TG, Klauber MR, Marshall LF: Outcome from head injury related to patient’s age: A longitudinal prospective
study of adult and pediatric head injury. J Neurosurg 68:409416, 1988 3. Lescohier I, DiScala C: Blunt trauma in children: Causes and outcomes of head versus intracranial injury. Pediatrics 91:721-725, 1993 4. Elson L, Ward C: Mechanisms and pathophysiology of mild head injury. Semin Neurol 14:8-18, 1994
138
5. Evans R: The postconcussion syndrome and the sequelae of mild head injury. Neurol Trauma 10:815-847, 1992 6. Levin HS, Benton AL, Grossman RG: Neurobehavioral Consequences of Closed Head Injury. New York, Oxford University Press, 1982 7. Ewing-Cobbs L, Fletcher JM, Levin HS, et al: Longitudinal neuropsychological outcome in infants and preschoolers with traumatic brain injury. J Int Neuropsychol Soc 3:581-591, 1997 8. Yeates KO, Taylor HG, Wade SL, et al: A prospective study of short- and long-term neuropsychological outcomes after traumatic brain injury in children. Neuropsychology 16: 514-523, 2002 9. Kennard M: Cortical reorganization of motor function. Arch Neurol Psychiatry 48:377-397, 1942 10. Boll, T: Minor head injury in children: Out of sight but not out of mind. J Clin Child Psychol 12:74-80, 1983 11. Powell J, Barber-Foss K: Traumatic brain injury in high school athletes. JAMA 282:958-963, 1999 12. Beers S: Cognitive effects of mild head injury in children and adolescents. Neuropsychol Rev 3:281-320, 1992 13. Satz P, Zaucha K, McCleary C: Mild head injury in children and adolescents: A review of studies (1970-1995). Psychol Bull 122:107-131, 1997 14. Teasdale G, Jennett B: Assessment of coma and impaired consciousness: A practical scale. Lancet 2:81-84, 1974 15. Williamson DJ, Scott J, Adams RL: Traumatic brain injury, in Adams RL, Parsons OA, Culbertson JL, et al (eds): Neuropsychology for Clinical Practice: Etiology, Assessment, and Treatment of Common Neurological Disorders. Washington, DC, American Psychological Association, 1996, pp 9-64 16. Ewing-Cobbs L, Levin HS, Fletcher JM, et al: The Children’s Orientation and Amnesia Test: Relationship to severity of acute head injury and recovery of memory. Neurosurgery 27:683-691, 1990 17. Fletcher JM, Ewing-Cobbs L, Francis DJ, et al: Variability in outcomes after traumatic brain injury in children: A developmental perpective, in Broman SH, Michel ME (eds): Traumatic Head Injury in Children. New York, Oxford University Press, 1995, pp 3-21 18. Mild Traumatic Brain Injury Committee of the Head Injury Interdisciplinary Special Interest Group of the American Congress of Rehabilitation Medicine: Definition of mild traumatic brain injury. J Head Trauma Rehabil 8:86-87, 1993 19. Williams DH, Levin HS, Eisenberg HM: Mild head injury classification. Neurosurgery 27:422-428, 1990 20. Mittenberg W, Wittner MS, Miller LJ: Postconcussion syndrome occurs in children. Neuropsychology 11:447-452, 1997 21. Maroon JC, Lovell MR, Norwig J, et al: Cerebral concussion in athletes: Evaluation and neuropsychological testing. Neurosurgery 47:659-669, 2000 22. Kelly J, Nichols JS, Filley C, et al: Concussion in sports: Guidelines for the prevention of catastrophic outcome. JAMA 266:2867-2869, 1991 23. Quality Standards Subcommittee, American Academy of Neurology: Practice parameter: The management of concussion in sports (summary statement). Neurology 48:581-585, 1997 24. Gennarelli TA: Cerebral concussion and diffuse brain injuries, in Cooper PR (ed): Head Injury (ed 3). Baltimore, MD, Williams & Wilkins, 1994, pp 137-158
THOMPSON AND IRBY
25. Gennarelli TA, Thibault LE, Adams JH, et al: Diffuse axonal injury and traumatic coma in the primate. Ann Neurol 12:564-574, 1982 26. Blumbergs PC, Scott G, Manavis J, et al: Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet 344:1055-1056, 1994 27. Gennarelli TA, Thibault LE, Graham DI: Diffuse axonal injury: An important form of traumatic brain damage. Neuroscientist 4:202-215, 1998 28. Maxwell WL, Povlishock JT, Graham DL: A mechanistic analysis of nondisruptive axonal injury: A review. J Neurotrauma 14:419-440, 1997 29. Povlishock JT: Pathobiology of traumatically induced axonal injury in animals and man. Ann Emerg Med 22:41-47, 1993 30. Margulies S: The postconcussion syndrome after mild head trauma: Is brain damage overdiagnosed? Part 1. J Clin Neurosci 7:400-408, 2000 31. Gentry LR, Godersky JC, Thompson B: MR imaging of head trauma: Review of the distribution and radiopathological features of traumatic lesions. Am J Neuroradiol 9:101-110, 1988 32. Levi L, Guilburd JN, Lemberger A, et al: Diffuse axonal injury: Analysis of 100 patients with radiological signs. Neurosurgery 27:429-432, 1990 33. Oppenheimer DR: Microscopic lesions in the brain following head injury. J Neurol Neurosurg Psychiatry 31:299-306, 1968 34. World Health Organization: International Statistical Classification of Diseases and Related Health Problems (ed 10). Geneva, Switzerland, World Health Organization, 1992 35. American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders (ed 4). Washington, DC, American Psychiatric Association, 1994 36. Farmer MY, Singer HS, Mellitus ED, et al: Neurobehavioral sequelae of minor head injuries in children. Pediatr Neurosci 13:304-308, 1987 37. Yeates KO, Luria J, Bartkowski H, et al: Postconcussive symptoms in children with mild closed head injuries. J Head Trauma Rehabil 14:337-350, 1999 38. Ponsford J, Willmott C, Rothwell A, et al: Cognitive and behavioral outcome following mild traumatic head injury in children. J Head Trauma Rehabil 14:360-372, 1999 39. Chadwick O, Rutter M, Brown B, et al: A prospective study of children with head injuries: II. Cognitive sequelae. Psychol Med 11:49-61, 1981 40. Asarnow RF, Satz P, Light R, et al: The UCLA study of mild closed head injury in children and adolescents, in Broman SH, Michel ME (eds): Traumatic Head Injury in Children. New York, Oxford University Press, 1995, pp 117-146 41. Fletcher JM, Ewing-Cobbs L, Miner ME, et al: Behavioral changes after closed head injury in children. J Consult Clin Psychol 58:93-98, 1990 42. Luis CA, Mittenberg W: Mood and anxiety disorders following pediatric traumatic brain injury: A prospective study. J Clin Exp Neuropsychol 24:270-279, 2002 43. Anderson V, Catroppa C, Morse S, et al: Outcome from mild head injury in young children: A prospective study. J Clin Exp Neuropsychol 23:705-717, 2001 44. Catroppa C, Anderson V: Recovery in memory function
RECOVERY FROM MILD HEAD INJURY
in the first year following TBI in children. Brain Inj 16:369-384, 2002 45. Anderson VA, Catroppa C, Rosenfeld J, et al: Recovery of memory function following traumatic brain injury in preschool children. Brain Inj 14:679-692, 2000 46. McCrea MM, Kelly JP, Kluge J, et al: Standardized assessment of concussion in football players. Neurology 48: 586-588, 1997 47. Moser RM, Schatz P: Enduring effects of concussion in youth athletes. Arch Clin Neuropsychol 17:91-100, 2002 48. Boll TJ, Barth J: Mild head injury. Psychiatry Devel 1:263-275, 1983 49. Light R, Asarnow R, Satz P, et al: Mild closed-head injury in children and adolescents: Behavior problems and academic outcomes. J Consult Clin Psychol 66:1023-1029, 1998 50. McKinlay A, Dalrymple-Alford JC, Horwood LJ, et al: Long term psychosocial outcomes after mild head injury in early childhood. J Neurol Neurosurg Psychiatry 73:281-288, 2002 51. Bijur PE, Haslum M, Golding J: Cognitive outcomes of multiple mild head injuries in children. J Dev Behav Pediatr 17:143-148, 1996 52. Ponsford J, Willmott C, Rothwell A, et al: Impact of
139
early intervention on outcome after mild traumatic brain injury in children. Pediatrics 108:1297-1303, 2001 53. Taylor HG, Yeates KO, Wade SL, et al: Influences on first-year recovery from traumatic brain injury in children. Neuropsychology 13:76-89, 1999 54. Yeates KO, Taylor HG, Drotar D, et al: Premorbid family environment as a predictor of neurobehavioral outcomes following pediatric traumatic brain injury. J Int Neuropsychol Soc 3:617-630, 1997 55. Roberts RJ: Epilepsy spectrum disorders in the context of mild traumatic brain injury, in Varney NR, Roberts RJ (eds): The Evaluation and Treatment of Mild Traumatic Brain Injury. Mahwah, NJ, Lawrence Erlbaum, 1999, pp 209-247 56. Hoffman RG, Scott JG, Emick MA, et al: The MMPI-2 and closed head injury: Effects of litigation and head injury severity. J Forensic Neuropsychol 1:3-13, 1999 57. Paniak C, Reynolds S, Toller-Lobe G, et al: A longitudinal study of the relationship between financial compensation and symptoms after treated mild traumatic brain injury. J Clin Exp Neuropsychol 24:187-193, 2002
H
EAD INJURY during childhood and adolescence is a major cause of acquired disability. Although estimates of incidence vary widely, a comprehensive review by Kraus revealed an average annual incidence of 180 head injuries per 100,000 children per year.1 Mild head injury (MHI) appears to be the most prevalent form of head injury in children and adults. The U.S. National Coma Data Bank2 indicates that approximately 85% of all head injuries requiring medical treatment are classified as mild. The National Pediatric Trauma Registry3 also indicates a predominance of MHIs, with 76% of injuries classified as mild. Reports pertaining to the frequency of MHI in children are likely to underestimate the actual incidence, due to the high number of unreported MHIs and head injuries that are overlooked due to a focus on orthopedic or other non– central nervous system (CNS) injuries.4,5 The long-term impact of severe head injury is well-documented,6-8 but outcome associated with MHI is less clear. Before the early 1980s, studies on the effect of MHI in children were limited, possibly due to the misunderstanding of the longaccepted plasticity hypothesis, which suggests that neurobehavioral recovery after brain injury is better tolerated by children than by adults.9 A surge of
From Children’s Hospital, Department of Psychology and Department of Pediatrics, Louisiana State University Health Sciences Center, New Orleans, LA and Laboratoria de Estudos de Linguagem, Centro de Estudios Egas Moniz, Hospital Santa Maria, Lisbon, Portugal. Address reprint requests to Matthew D. Thompson, PsyD, Children’s Hospital, Department of Psychology, 200 Henry Clay Avenue, New Orleans, LA 70118. © 2003 Elsevier Inc. All rights reserved. 1071-9091/03/1002-0000$30.00/0 doi:10.1016/S1071-9091(03)00021-4 130
interest and research in pediatric MHI was prompted in the early 1980s by Boll,10 who stated that MHI in children was a silent epidemic. More recently, even more interest in MHI in children has been spurred by the increased attention to sportsrelated head injuries.11 Comprehensive reviews pertaining to the cognitive status of children who have experienced MHI have differed in their conclusions.12,13 Since the publication of the most recent comprehensive literature reviews, several well-constructed empirical studies have been published that contribute valuable information to the growing body of literature on pediatric MHI. This article provides general information on the diagnosis, pathophysiology, and outcome of MHI in children, particularly as described in recent publications. DIAGNOSIS AND CLASSIFICATION OF MILD HEAD INJURY
Various head injury classification and diagnostic systems have been proposed. Most of these systems involve the assessment of mental status and other neurologic variables. The most commonly used classification system is the Glasgow Coma Scale (GCS),14 which evaluates three variables: eye opening, motor response, and verbal response. Each variable is graded (eye opening, 1 to 4; motor response, 1 to 6; verbal response, 1 to 5), with a lower score indicating greater impairment. The total score ranges from 3 (most severe) to 15 (essentially normal). Traditionally, GCS scores from 13 to 15 represent mild injuries, scores from 9 to 12 represent moderate injuries, and scores of 8 or less represent severe injuries.15 Several factors associated with GCS assessment introduce considerable variability into empirical studies as well as clinical interpretation. One of these factors is the Seminars in Pediatric Neurology, Vol 10, No 2 (June), 2003: pp 130-139
RECOVERY FROM MILD HEAD INJURY
Table 1.
131
MHI Definition Proposed by the American Congress of Rehabilitation Medicine
A patient with mild traumatic brain injury is a person who has had a traumatically induced physiologic disruption of brain function as manifested by at least one of the following: 1. Any period of loss of consciousness 2. Any loss of memory for events immediately before or after the accident 3. Any alteration in mental state at the time of the accident (e.g., feeling dazed, disoriented, or confused) 4. Focal neurologic deficit(s) that may or may not be transient, but where the severity of the injury does not exceed the following: 1. Loss of consciousness of approximately 30 minutes or less 2. After 30 minutes, an initial Glasgow coma scale score of 13-15 3. Posttraumatic amnesia not greater than 24 hours.
amount of time elapsed since injury at the time that the GCS assessment is obtained. If a child has been intubated or sedated at the time of GCS assessment, the score will be depressed. Also, GCS assessment with infants and toddlers who are preverbal may result in an artificially depressed score. Length of posttraumatic amnesia (PTA) is also used to grade the severity of head injury. Although definitions vary, PTA is usually described as the lack of memory for ongoing events (ie, anterograde amnesia).6 Significant variability exists in opinions pertaining to the length of PTA and its corresponding severity level, but in general, PTA of less than 24 hours duration is generally considered to represent a mild head injury, whereas PTA of 1 to 7 days duration is considered moderate and PTA of 8 or more days duration is considered severe.6 The assessment of PTA, when conducted retrospectively, is complicated by the subjective nature of self-report. This difficulty is magnified in children due to developmental limitations. At least one formal measure of PTA, the Children’s Orientation and Amnesia Test (COAT), has been designed for use with children.16 The COAT consists of 16 items evaluating (1) general orientation to person and place and recall of biographical information, (2) temporal orientation, and (3) memory (immediate, short-term, and remote). Normative data are available for the COAT, and cutoff scores have been established that have adequate predictive validity.17 In a group of children who sustained closed-head injury, both verbal and nonverbal memory scores were significantly more impaired at 6 and 12 months after the injury in patients with PTA persisting for at least 3 weeks (as determined by serial COAT administration) than in patients whose disorientation, confusion, and gross amnesia resolved within 1 week. Duration of postinjury unconsciousness, opera-
tionally defined as the length of time between injury and ability to follow a command, has also been used as an index of head injury severity. This variable is similar to the motor response portion of the GCS, in which a score of 6 is recorded when the child is able to follow a motor command. A severe injury is usually considered to have occurred when the duration of unconsciousness exceeds 24 hours,17 but there continues to be some inconsistency and debate regarding the duration of unconsciousness associated with the classification of mild or moderate head injury. The most recent and inclusive definition of MHI, which was designed with the goal of promoting uniformity across studies, was developed by the Mild Traumatic Brain Injury Committee of the Head Injury Interdisciplinary Special Interest Group of the American Congress of Rehabilitation Medicine (ACRM)18 and is presented in Table 1. Although this definition clearly defines the upper limits of MHI, the lower limits are less clear. Under the definition proposed by the ACRM, individuals with a mechanical force applied to the head and alteration in mental status (eg, feeling dazed) are considered to have a mild traumatic brain injury and would be grouped with individuals with up to 30 minutes of unconsciousness. More recently, the MHI classification has been further delineated by designating a complicated MHI category, which describes an injury that would be classified as mild based on GCS score, duration of unconsciousness, and duration of PTA, but where there is evidence of an abnormality seen on computed tomography (CT) or magnetic resonance imaging (MRI), including brain lesions and/or skull fractures.19 In adults, patients with uncomplicated MHI had a better outcome at 6 months postinjury relative to patients with complicated MHI.19 It should be noted that many patients
132
with complicated MHI, as defined here, would have been included in the moderate traumatic brain injury (TBI) group in many studies.20 The term concussion has been used interchangeably with MHI, but it usually refers to milder injuries on the MHI spectrum. The precision of MHI description and classification can be augmented by considering various systems that describe the severity of a concussion. These classification systems are usually applied in the context of athletic injuries and return-to-play decisions.21 In 1991, the Sports Medicine Committee of the Colorado Medical Society developed definitions of three levels of concussion (mild, moderate, and severe) along with guidelines for management.22 Each level of concussion was described according to length of unconsciousness: no loss of consciousness, less than a 5-minute loss of consciousness, and more than a 5-minute loss of consciousness. The most recent concussion severity rating scale was published by the Quality Standards Subcommittee of the American Academy of Neurology (AAN) in 1997.23 Under the AAN guidelines, a grade 1 concussion is defined as symptoms lasting less than 15 minutes, with transient confusion and no loss of consciousness. Grade 2 concussion involves symptoms lasting more than 15 minutes, no loss of consciousness, and transient confusion. Grade 3 concussion is defined as loss of consciousness that is either brief or prolonged. The AAN guidelines are notable for the emphasis on confusion and amnesia, whereas previous guidelines had placed more emphasis on loss of consciousness. PATHOPHYSIOLOGY OF MILD HEAD INJURY
The neuropathologic effects of MHI are controversial relative to the known adverse effects of severe head injury. Head trauma can cause brain injury as a result of three mechanisms: (1) focal hemorrhagic and nonhemorrhagic lesions, (2) diffuse axonal injury (DAI), and (3) secondary injury caused by edema and space-occupying hemorrhages.24 DAI is of particular interest in the study of MHI. DAI is defined as widespread injury to axons in the white matter of the brain induced by transient application of tensile strain.25 The definition and use of the term DAI has evolved over the years. The original definition of DAI was prolonged traumatic coma not associated with mass lesions or
THOMPSON AND IRBY
ischemic damage.26 The question is whether DAI also occurs in MHI. DAI requires a sudden acceleration-deceleration force,25,27 which stretches delicate axonal fibers. If the injury-inducing forces are not too great, then the only injury to the axon is a temporary stagnation of axonal transport. If the forces are severe enough, then axonal transection may occur with death of the axonal segment and sealing off of the proximal axonal stump.28 The distal axon is subsequently phagocytosed by microglial cells, producing microglial clusters. Once axonal transport resumes, the products being transported from the cell body accumulate at the site of the axonal damage, causing it to balloon up into an axonal retraction ball.29 The amount of force needed to cause axonal stagnation is unknown, as is the threshold for axonal transection.30 Axon retraction balls and microglial clusters are microscopic indicators of DAI.30 Indirect evidence of severe DAI can be seen on MRI as small, ovoid, low-attenuation lesions with their long axis parallel to the direction of the affected axon.31 Other circumstantial evidence is the presence of petechial hemorrhages, particularly at the gray–white junction and corpus callosum.32 Definitive determination of DAI is possible only with pathologic examination. The most quoted study of pathologically confirmed DAI in cases of MHI has been Oppenheimer’s 1968 report on five patients who experienced MHI and subsequently died due to unrelated causes.33 In one case, microglial clusters and axon retraction balls were found in a patient who died of pneumonia 13 days after suffering a MHI. The patient had been knocked down by a motor scooter and suffered a parietal bruise but no skull fracture. Four other patients who suffered MHI but later died for reasons unrelated to their head injury were included in the study, and evidence of microglial clusters, but not axon retraction balls, was reported. Others have noted that microglial clusters may be seen as part of an immune response to such insults as anoxia.27,30 Oppenheimer’s study has not yet been replicated. Other investigators using a similar research design have found microscopic evidence of disturbed axonal transport, but not axon retraction balls or microglial clusters.26 When considered as a whole, the literature suggests that some people who suffer severe head injuries show evidence of DAI. Individuals with
RECOVERY FROM MILD HEAD INJURY
MHI, however, may experience a transient alteration of biochemical and cellular function in the brain, but there is not sufficient evidence to conclude that people with MHI develop DAI in the absence of a loss of consciousness and considerable deceleration forces. ACUTE EFFECTS OF MILD HEAD INJURY IN CHILDREN
The constellation of acute symptoms after MHI is typically referred to as postconcussion syndrome (PCS). In adults, these symptoms include somatic complaints (headache, dizziness, fatigue, blurry or double vision, noise intolerance, and light sensitivity), emotional changes (depression, anxiety, irritability), and cognitive difficulties (subjective complaints of poor concentration and impaired memory). Diagnostic criteria for PCS are included in the International Statistical Classification of Diseases and Related Health Problems, 10th edition (ICD-10),34 and research criteria for PCS are included in the Diagnostic and Statistical Manual of Mental Disorders, 4th edition (DSM-IV).35 Several studies have determined that children also experience similar somatic and emotional postconcussive symptoms in the weeks after sustaining MHI.20,36-38 Farmer et al36 compared the behavioral symptoms from a large sample (n ⫽ 247) of children with MHI with those from a control group of 280 children who had sustained injuries to other areas of the body. Within the first week after injury, complaints of irritability, clinging behavior, and sleep disturbance were common in both groups, but only headaches were more frequently experienced by the head-injured children relative to the control group. Ponsford et al38 found that relative to children with other injuries (n ⫽ 96), children with MHI (n ⫽ 130) experienced not only significantly more headaches, but also more dizziness and fatigue at 1 week postinjury. By 3 months postinjury, the postconcussion symptoms had resolved. Other studies have found no adverse postconcussion effects at 4 months39 or 6 months postinjury.40,41 However, Ponsford et al38 noted that at 3 months postinjury, 17% of the children with MHI in her study were experiencing significant ongoing postconcussion symptoms and problems, which appeared to be related to preexisting factors (ie, previous head injury or preexisting learning, neurologic, or psychosocial problems). Yeates et al37 also reported that
133
postconcussion symptoms observed at 3 months postinjury in a series of 26 children with MHI were associated with premorbid neurologic and psychosocial problems. Mittenberg et al20 specifically examined the self-reports of postconcussion symptoms in 38 children with MHI, 27 children with moderate head injury, and 47 children with orthopedic injuries. At 6 weeks postinjury, the head injury groups reported significantly more symptoms than did the orthopedic injury group. The symptoms were related to the severity of head injury and also to the child’s anxiety level. Luis and Mittenberg42 also found that relative to children who sustained orthopedic injuries, children who sustained MHI were at an increased risk for developing anxiety and depression 6 months postinjury. Regarding acute cognitive symptoms after MHI in children, Ponsford et al38 found no evidence of cognitive impairment at 1 week or 3 months postinjury, even among the 17% of the MHI group who reported continuing postconcussion symptoms. However, it was noted that the cognitive assessment battery was relatively limited. Using a more extensive battery, Anderson et al43 did not find any significant effects on measures of intelligence, spatial memory, or auditory comprehension in young children (age 3 to 7) 3 months post-MHI, but children with MHI performed significantly worse than normal controls on measures of story recall and verbal fluency. Catroppa and Anderson44,45 also found that MHI children performed below age expectations 3 months postinjury, further suggesting that MHI in children may impact a child’s ability to encode and consolidate new verbal information in the months after the injury. It was noted, however, that MHI children made ongoing and often dramatic improvement in verbal abilities at 6 months, 12 months, and 30 months postinjury.43,44 In summary, MHI in children results in increased rates of somatic and emotional complaints including headaches, dizziness, and fatigue in the first few weeks after MHI, but these symptoms usually resolve by 3 months postinjury. In some children, cognitive difficulties are also evident on tests of higher-order cognitive processes (ie, verbal fluency and verbal memory consolidation) in the first several months postinjury, but these also usually resolve over time. These findings are also consistent with the acute effects of concussion as
134
THOMPSON AND IRBY
documented in the sports-related concussion literature.46,47 Despite the finding that cognitive and somatic symptoms usually resolve in most children, it appears that a subset of children continue to experience postconcussion difficulties after MHI. We address the variables associated with this subset of children later in this article. LONG-TERM OUTCOME OF MILD HEAD INJURY IN CHILDREN
There is considerable controversy regarding the long-term outcome after MHI. Some of the earlier reviews10,12,48 suggested that MHI in children led to symptoms that affected cognitive, academic, and psychosocial functioning and that these symptoms could be devastating to a child’s development. However, in their influential review, Satz et al13 pointed out that many of the studies on which these earlier reviews were based had methodologic flaws that significantly limited their generalizability (eg, pooling moderate and mild head injury cases and making inferences from adult populations). Satz et al suggested six key methodologic criteria essential for research in this area: (1) inclusion of an appropriate control group, (2) use of a longitudinal design with follow-up assessment after the injury, (3) clear definition of MHI, with no inclusion of children with more severe injuries, (4) control for preinjury factors, (5) inclusion of at least 20 children with MHI, and (6) use of standardized assessment measures. Based on 40 outcome studies of MHI in children published between 1970 and 1995 that met at least four of these six research criteria, Satz reached the conclusion that MHI in children might result in a mild but transitory alteration in cognitive functioning (ie, attention and memory), but no reliable changes in academic or psychosocial functioning. However, Satz pointed out that the studies that found no effect on academic or psychosocial functioning were cases selected from the very mild end of the severity spectrum, whereas the studies that found weak but transient cognitive alterations came from the more severe end of this spectrum. Satz also noted that as severity within the MHI spectrum increased, more variability in findings was reported, suggesting that within the spectrum of MHI, there may be a degree of mild injury that reaches a threshold of concern. Since the publication of the review by Satz et al, several studies have been published that have incorporated Satz’s suggested research criteria. Us-
ing a prospective longitudinal design, Anderson et al43 examined the effect of MHI in 17 young children (age 3 to 7) using standardized measures of adaptive, behavioral, and cognitive functioning at the time of initial hospitalization and at 6 and 30 months postinjury. The children were recruited from a neurosurgery ward where they had been admitted after sustaining a MHI, which was defined as an admission GCS score of 13 to 15, an indication of some alteration of consciousness, no deterioration of consciousness after admission, no mass lesion seen on CT/MRI, and no neurologic deficit. Children were excluded if they had any previous history of head injury and any evidence of neurologic, psychiatric, or developmental disorder. Preinjury adaptive and behavioral functioning was gathered from the parents at the time of initial admission. A group of 35 healthy children matched as closely as possible on demographic variables was used as a control group. No significant differences were noted between the two groups on most cognitive measures (ie, intellectual, speed of processing, attention, everyday and spatial memory, receptive vocabulary, and auditory comprehension) at the acute stage and at 30 months postinjury. No significant differences between the two groups were noted on parent-reported measures of adaptive and behavioral functioning at the acute stage and at 30 months postinjury, although trends toward slightly more reported symptoms of social incompetence and internalization/somatic complaints were noted for the MHI group at 12 and 30 months postinjury. Also, the MHI group performed significantly worse than the control group on measures of story recall at all time points and verbal fluency at 30 months postinjury, suggesting that MHI may produce impairment in certain high-level language-based skills. Anderson et al noted that the MHI group demonstrated ongoing improvements on these measures over time, and suggested that their impairments represented a transient interruption of brain function and a resultant delay in skill acquisition rather than a permanent deficit. Based on their overall findings, the authors concluded that their study provides support for a generally good outcome for children sustaining a MHI during the preschool years. Light et al49 investigated behavior problems and academic performance in a group of children with MHI at 1 year postinjury. Children between age 8 and 16 who sustained MHI (n ⫽ 137) were pro-
RECOVERY FROM MILD HEAD INJURY
spectively recruited after emergency room admission and compared with 132 children with injuries that did not involve the brain or head and 114 children with no injuries. None of the children in the MHI group required hospitalization. Based on preinjury and postinjury parental ratings of the children’s behavior and academic records obtained from the schools, a significant difference was noted between the two injured groups of children and the healthy controls at 1 year postinjury. A greater degree of preinjury behavioral problems was found in the MHI group and other-injured group relative to the noninjured control group, differences that might have been attributed to MHI had the authors not included an other-injured control group. As described previously in the discussion of acute effects of MHI, Ponsford et al38 evaluated 130 children between age 6 and 15 with MHI as defined by the ACRM. At approximately 1 week postinjury, a significant proportion of these children reported postconcussion symptoms, but no cognitive impairments were measured for the children as a group relative to controls, even though the cognitive assessment battery was relatively limited. Three months later, the postconcussion symptoms had largely resolved in the group, but 17% exhibited ongoing problems. Investigation of premorbid status revealed that the symptomatic children were more likely to have a history of previous head injury, learning difficulties, neurologic or psychiatric problems, or family stressors. McKinlay et al,50 incorporating all six of Satz’s recommendations, followed annually to age 10 to 13 all of the children born in their region of New Zealand during an approximate 4-month period in 1977. Of the 1265 children born during that period, 132 sustained MHI before age 10. (In this study, a child with MHI was defined as any child who received medical attention for concussion or suspected concussion.) Children were excluded if loss of consciousness lasted longer than 20 minutes, if hospitalization was for more than 2 days, or if skull fracture occurred. Children with nonspecific head injuries were also excluded. In an attempt to operationalize and grade the severity of MHI, the cases were divided into those receiving outpatient care (n ⫽ 96) and those receiving inpatient care (n ⫽ 36). Because of the epidemiologic nature of the study, it was possible to use a large control group (n ⫽ 613 to 807) that was identical in age and highly comparable in terms of education, fam-
135
ily background, and socioeconomic status, and thereby control for some of the potential confounding factors related to preinjury factors or family characteristics. Throughout the course of the study, data were gathered from the participant’s families and teachers, and a range of standardized cognitive, academic, and behavioral assessment measures were used at regular intervals. The results indicated that children who received inpatient care for MHI between age 0 and 10 displayed increased hyperactivity/inattention and conduct disorder behavior between age 10 and 13, especially if the injury occurred before age 5. These results were reliable after statistical control of a wide range of potential confounding factors, including preinjury factors, was applied. No significant effects were noted on cognitive or academic measures, regardless of injury severity, and no significant differences were noted between the outpatient MHI participants and the noninjured control group on psychosocial measures. McKinlay et al concluded that although most cases of MHI in children do not produce adverse effects, it is not always a completely benign event, and long-term problems in psychosocial functioning are more likely at the upper end of the MHI severity spectrum. In another study involving a large cohort of children with MHI, Bijur et al51 assessed the cumulative effects of multiple MHI on cognitive functioning. The sample included 1586 children with 1 MHI, 278 children with 2 MHIs, and 51 children with 3 or more MHIs between birth and age 10 years. The control group included children without head injuries but matched to the clinical sample on total number of injuries. The numbers of head injuries and nonhead injuries were found to be associated with decreasing performance on measures of cognitive and academic functioning. After adjusting for psychosocial variables, the relationship between number of injuries and cognitive outcomes became nonsignificant. Ponsford et al52 studied a group of 119 children with MHI as defined by ACRM criteria. Sixty-one participants were assigned to an intervention group and evaluated 1 week and 3 months after injury, and 58 participants were assigned to a nonintervention group and assessed 3 months after injury. They were compared with two control groups of children with minor injuries not involving the head. Parents and children in the intervention group were provided with a booklet describing
136
THOMPSON AND IRBY
typical MHI symptoms and coping methods. Preinjury behavioral adjustment of children in the intervention group and the control groups was assessed by asking parents to complete behavioral rating inventories as they applied to premorbid behavior and psychological adjustment. Standardized measures of postconcussion symptoms and neuropsychological skills were also administered. Children with MHI reported more symptoms than controls at 1 week postinjury but demonstrated no impairment on neuropsychological measures. Initial postconcussion symptoms had resolved for most children by 3 months postinjury, but a small group of children who had a previous head injury or a history of learning or behavioral difficulties reported ongoing problems. The group not seen at 1 week postinjury and not given the information booklet (ie, the nonintervention group) reported more symptoms overall and was more symptomatic 3 months after injury. PSYCHOSOCIAL RISK FACTORS
As illustrated by many of the MHI studies described thus far, psychosocial risk factors emerge as a critical factor in recovery from MHI. Psychosocial risk factors in the context of MHI include premorbid learning and behavior problems, disadvantaged socioeconomic status, premorbid neurodevelopmental abnormalities, or adverse family conditions. For example, Light et al49 found that children with injuries necessitating a visit to the emergency room had slightly elevated rates of behavioral problems, regardless of the type of injury (eg, CNS or non-CNS). Ponsford et al38 found that children with MHI who exhibited residual symptoms were more likely to have a history of previous head injury, learning difficulties, neurologic or psychiatric problems, or family stressors. The importance of considering preinjury risk factors is also exemplified by the University of California Los Angeles study of MHI,40 which indicated that for certain outcome measures, the effects of certain preinjury factors (eg, history of learning and school problems) were larger than the effects of MHI. Likewise, Bijur et al51 found that adverse cognitive and academic outcomes were explained by premorbid psychosocial factors rather than acquired brain damage. Compared to research pertaining to the role of psychosocial variables in children with MHI, rel-
atively more research has been conducted investigating the role of these variables in children with moderate and severe head injuries, and the findings from these studies consistently indicate that environmental and psychosocial disadvantages exacerbate the adverse effects of head injury. For example, general measures of socioeconomic status and family demographics have been found to influence outcome.53 Concerning more specific measures of premorbid family functioning as well as postinjury family functioning, Yeates et al54 documented a significant correlation between performance on neuropsychological tests and formal measures of family functioning in a group of children with severe head injuries. The same correlation was not found in a group of children with orthopedic injuries, suggesting an interaction between environmental variables and injury type. The same study reported that measures of family environment accounted for 25% of the variance in level of outcome, after controlling for severity of head injury. Interestingly, after controlling for family environment, age at injury, and ethnic status, head injury severity accounted for only 20% of the variance in outcome. Given the growing body of literature indicating the significant role of psychosocial variables in the outcome of pediatric head injury, considering these factors in clinical practice and empirical research is critical. Satz13 recommended controlling for premorbid risk factors in future studies not by exclusion, but rather by using designs that permit statistical as well as experimental controls. SUMMARY AND CONCLUSIONS
The conclusions from this review of recent studies on the effect of MHI on children are generally consistent with those of Satz et al.13 Most children who experience MHI will experience few, if any, permanent adverse cognitive, behavioral, or psychosocial outcomes, especially if the injury is on the mild end of the MHI severity spectrum. The most common symptoms during the first week after MHI are headaches, dizziness, and fatigue, which are usually completely resolved within the first month postinjury.36-41 Despite these postconcussive symptoms, some studies suggest most children do not experience significant cognitive dysfunction immediately after MHI,38 but other studies suggest that some children with head inju-
RECOVERY FROM MILD HEAD INJURY
137
ries toward the severe end of the MHI spectrum (ie, required hospital admission) may experience subtle difficulties with encoding and consolidation of new verbal information during the acute phase.43-45 Long-term follow-up studies reveal a generally positive outcome for most children with MHI; however, several studies have reported that there is a sizable minority of children who continue to experience ongoing cognitive and psychosocial difficulties in the months after MHI.38,45,49,51,52 It appears that those children who develop persistent symptoms are more likely to have preexisting neurologic, psychiatric, or family problems,38,45,49,51,52 but one recent study did find evidence that even previously healthy children may experience a transient delay in acquisition of higher-level language-based skills.43 Also, another group found that preexisting difficulties do not fully account for all adverse, long-term psychosocial consequences (eg, hyperactivity/inattention and conduct problems), particularly if the head injury occurs during the preschool years and is toward the severe end of the MHI severity spectrum.50 One of the key issues in the MHI literature, for both children and adults, is defining MHI and determining the severity of MHI. Research over the past several years has generally supported the notion that there is a threshold of concern within the spectrum of MHI. The parameters of this threshold, and how they are determined, remains an issue of debate and a subject for further research. Satz and his colleagues have argued that head injury severity is a dimensional construct that does not easily lend itself to arbitrary cutoff points, and that attempts to establish a consensus definition of MHI tend to reify arbitrary distinctions. Rather, it is argued that operational definitions of closed head injury severity are needed along multiple dimensions (eg, loss of consciousness, posttraumatic amnesia). Hence one important area for future research is in the further validation of such assessment techniques as the COAT. Given the potential that some children, particu-
larly those with premorbid risk factors, may experience an incomplete recovery following MHI, it behooves the clinician to monitor the symptoms of MHI for several months so that appropriate interventions can be implemented. Toward this end, Ponsford52 has demonstrated that providing parents with an information booklet reduces anxiety among the families of children who have suffered MHI and lowers the reported incidence of ongoing postconcussive symptoms. Roberts55 conceptualized the difficulties that some children experience after MHI as episodic in nature and suggested that these difficulties may not always be observed in the office setting. Clinicians often overlook such episodic symptoms, and Roberts argued for the paramount importance of specifically querying for these symptoms during the clinical interview. One of the reasons MHI is such a contentious area in the adult literature is due to litigation, which has fueled a considerable amount of research into the effects of litigation status on selfreport of postconcussion symptoms and performance on neuropsychological tests. In general, it has been demonstrated that litigation status has a significant impact on the persistence of postconcussion symptoms.56,57 We have not come across any studies that have investigated the impact of litigation status on the outcomes of children with MHI, but it is not unreasonable to consider whether involvement in litigation poses a threat to the validity of parent reports pertaining to their children who have suffered a MHI. The recent research pertaining to MHI in children is generally consistent with the conclusions reached by the authors of the most recent comprehensive review,13 which reported that children who have suffered MHI often experience a symptomatic phase that could extend up to a few months, but these symptoms usually resolve. Recent research has also identified risk factors that often explain the persistence of certain symptoms in a subset of children.
REFERENCES 1. Kraus JF: Epidemiological features of brain injury in children: Occurrence, children at risk, causes and manner of injury, severity, and outcomes, in Broman SH, Michel ME (eds): Traumatic Head Injury in Children. New York, Oxford University Press, 1995, pp 22-39 2. Luerssen TG, Klauber MR, Marshall LF: Outcome from head injury related to patient’s age: A longitudinal prospective
study of adult and pediatric head injury. J Neurosurg 68:409416, 1988 3. Lescohier I, DiScala C: Blunt trauma in children: Causes and outcomes of head versus intracranial injury. Pediatrics 91:721-725, 1993 4. Elson L, Ward C: Mechanisms and pathophysiology of mild head injury. Semin Neurol 14:8-18, 1994
138
5. Evans R: The postconcussion syndrome and the sequelae of mild head injury. Neurol Trauma 10:815-847, 1992 6. Levin HS, Benton AL, Grossman RG: Neurobehavioral Consequences of Closed Head Injury. New York, Oxford University Press, 1982 7. Ewing-Cobbs L, Fletcher JM, Levin HS, et al: Longitudinal neuropsychological outcome in infants and preschoolers with traumatic brain injury. J Int Neuropsychol Soc 3:581-591, 1997 8. Yeates KO, Taylor HG, Wade SL, et al: A prospective study of short- and long-term neuropsychological outcomes after traumatic brain injury in children. Neuropsychology 16: 514-523, 2002 9. Kennard M: Cortical reorganization of motor function. Arch Neurol Psychiatry 48:377-397, 1942 10. Boll, T: Minor head injury in children: Out of sight but not out of mind. J Clin Child Psychol 12:74-80, 1983 11. Powell J, Barber-Foss K: Traumatic brain injury in high school athletes. JAMA 282:958-963, 1999 12. Beers S: Cognitive effects of mild head injury in children and adolescents. Neuropsychol Rev 3:281-320, 1992 13. Satz P, Zaucha K, McCleary C: Mild head injury in children and adolescents: A review of studies (1970-1995). Psychol Bull 122:107-131, 1997 14. Teasdale G, Jennett B: Assessment of coma and impaired consciousness: A practical scale. Lancet 2:81-84, 1974 15. Williamson DJ, Scott J, Adams RL: Traumatic brain injury, in Adams RL, Parsons OA, Culbertson JL, et al (eds): Neuropsychology for Clinical Practice: Etiology, Assessment, and Treatment of Common Neurological Disorders. Washington, DC, American Psychological Association, 1996, pp 9-64 16. Ewing-Cobbs L, Levin HS, Fletcher JM, et al: The Children’s Orientation and Amnesia Test: Relationship to severity of acute head injury and recovery of memory. Neurosurgery 27:683-691, 1990 17. Fletcher JM, Ewing-Cobbs L, Francis DJ, et al: Variability in outcomes after traumatic brain injury in children: A developmental perpective, in Broman SH, Michel ME (eds): Traumatic Head Injury in Children. New York, Oxford University Press, 1995, pp 3-21 18. Mild Traumatic Brain Injury Committee of the Head Injury Interdisciplinary Special Interest Group of the American Congress of Rehabilitation Medicine: Definition of mild traumatic brain injury. J Head Trauma Rehabil 8:86-87, 1993 19. Williams DH, Levin HS, Eisenberg HM: Mild head injury classification. Neurosurgery 27:422-428, 1990 20. Mittenberg W, Wittner MS, Miller LJ: Postconcussion syndrome occurs in children. Neuropsychology 11:447-452, 1997 21. Maroon JC, Lovell MR, Norwig J, et al: Cerebral concussion in athletes: Evaluation and neuropsychological testing. Neurosurgery 47:659-669, 2000 22. Kelly J, Nichols JS, Filley C, et al: Concussion in sports: Guidelines for the prevention of catastrophic outcome. JAMA 266:2867-2869, 1991 23. Quality Standards Subcommittee, American Academy of Neurology: Practice parameter: The management of concussion in sports (summary statement). Neurology 48:581-585, 1997 24. Gennarelli TA: Cerebral concussion and diffuse brain injuries, in Cooper PR (ed): Head Injury (ed 3). Baltimore, MD, Williams & Wilkins, 1994, pp 137-158
THOMPSON AND IRBY
25. Gennarelli TA, Thibault LE, Adams JH, et al: Diffuse axonal injury and traumatic coma in the primate. Ann Neurol 12:564-574, 1982 26. Blumbergs PC, Scott G, Manavis J, et al: Staining of amyloid precursor protein to study axonal damage in mild head injury. Lancet 344:1055-1056, 1994 27. Gennarelli TA, Thibault LE, Graham DI: Diffuse axonal injury: An important form of traumatic brain damage. Neuroscientist 4:202-215, 1998 28. Maxwell WL, Povlishock JT, Graham DL: A mechanistic analysis of nondisruptive axonal injury: A review. J Neurotrauma 14:419-440, 1997 29. Povlishock JT: Pathobiology of traumatically induced axonal injury in animals and man. Ann Emerg Med 22:41-47, 1993 30. Margulies S: The postconcussion syndrome after mild head trauma: Is brain damage overdiagnosed? Part 1. J Clin Neurosci 7:400-408, 2000 31. Gentry LR, Godersky JC, Thompson B: MR imaging of head trauma: Review of the distribution and radiopathological features of traumatic lesions. Am J Neuroradiol 9:101-110, 1988 32. Levi L, Guilburd JN, Lemberger A, et al: Diffuse axonal injury: Analysis of 100 patients with radiological signs. Neurosurgery 27:429-432, 1990 33. Oppenheimer DR: Microscopic lesions in the brain following head injury. J Neurol Neurosurg Psychiatry 31:299-306, 1968 34. World Health Organization: International Statistical Classification of Diseases and Related Health Problems (ed 10). Geneva, Switzerland, World Health Organization, 1992 35. American Psychiatric Association: Diagnostic and Statistical Manual of Mental Disorders (ed 4). Washington, DC, American Psychiatric Association, 1994 36. Farmer MY, Singer HS, Mellitus ED, et al: Neurobehavioral sequelae of minor head injuries in children. Pediatr Neurosci 13:304-308, 1987 37. Yeates KO, Luria J, Bartkowski H, et al: Postconcussive symptoms in children with mild closed head injuries. J Head Trauma Rehabil 14:337-350, 1999 38. Ponsford J, Willmott C, Rothwell A, et al: Cognitive and behavioral outcome following mild traumatic head injury in children. J Head Trauma Rehabil 14:360-372, 1999 39. Chadwick O, Rutter M, Brown B, et al: A prospective study of children with head injuries: II. Cognitive sequelae. Psychol Med 11:49-61, 1981 40. Asarnow RF, Satz P, Light R, et al: The UCLA study of mild closed head injury in children and adolescents, in Broman SH, Michel ME (eds): Traumatic Head Injury in Children. New York, Oxford University Press, 1995, pp 117-146 41. Fletcher JM, Ewing-Cobbs L, Miner ME, et al: Behavioral changes after closed head injury in children. J Consult Clin Psychol 58:93-98, 1990 42. Luis CA, Mittenberg W: Mood and anxiety disorders following pediatric traumatic brain injury: A prospective study. J Clin Exp Neuropsychol 24:270-279, 2002 43. Anderson V, Catroppa C, Morse S, et al: Outcome from mild head injury in young children: A prospective study. J Clin Exp Neuropsychol 23:705-717, 2001 44. Catroppa C, Anderson V: Recovery in memory function
RECOVERY FROM MILD HEAD INJURY
in the first year following TBI in children. Brain Inj 16:369-384, 2002 45. Anderson VA, Catroppa C, Rosenfeld J, et al: Recovery of memory function following traumatic brain injury in preschool children. Brain Inj 14:679-692, 2000 46. McCrea MM, Kelly JP, Kluge J, et al: Standardized assessment of concussion in football players. Neurology 48: 586-588, 1997 47. Moser RM, Schatz P: Enduring effects of concussion in youth athletes. Arch Clin Neuropsychol 17:91-100, 2002 48. Boll TJ, Barth J: Mild head injury. Psychiatry Devel 1:263-275, 1983 49. Light R, Asarnow R, Satz P, et al: Mild closed-head injury in children and adolescents: Behavior problems and academic outcomes. J Consult Clin Psychol 66:1023-1029, 1998 50. McKinlay A, Dalrymple-Alford JC, Horwood LJ, et al: Long term psychosocial outcomes after mild head injury in early childhood. J Neurol Neurosurg Psychiatry 73:281-288, 2002 51. Bijur PE, Haslum M, Golding J: Cognitive outcomes of multiple mild head injuries in children. J Dev Behav Pediatr 17:143-148, 1996 52. Ponsford J, Willmott C, Rothwell A, et al: Impact of
139
early intervention on outcome after mild traumatic brain injury in children. Pediatrics 108:1297-1303, 2001 53. Taylor HG, Yeates KO, Wade SL, et al: Influences on first-year recovery from traumatic brain injury in children. Neuropsychology 13:76-89, 1999 54. Yeates KO, Taylor HG, Drotar D, et al: Premorbid family environment as a predictor of neurobehavioral outcomes following pediatric traumatic brain injury. J Int Neuropsychol Soc 3:617-630, 1997 55. Roberts RJ: Epilepsy spectrum disorders in the context of mild traumatic brain injury, in Varney NR, Roberts RJ (eds): The Evaluation and Treatment of Mild Traumatic Brain Injury. Mahwah, NJ, Lawrence Erlbaum, 1999, pp 209-247 56. Hoffman RG, Scott JG, Emick MA, et al: The MMPI-2 and closed head injury: Effects of litigation and head injury severity. J Forensic Neuropsychol 1:3-13, 1999 57. Paniak C, Reynolds S, Toller-Lobe G, et al: A longitudinal study of the relationship between financial compensation and symptoms after treated mild traumatic brain injury. J Clin Exp Neuropsychol 24:187-193, 2002