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Long-Term Executive FunctioningOutcomes for Complicated andUncomplicated Mild Traumatic BrainInjury Sustained in Early ChildhoodJennifer Papoutsisab, Robyn Stargattab & Cathy Catroppaa

a Murdoch Childrens Research Institute, Parkville, Australiab Department of Psychology, La Trobe University, Bundoora, AustraliaPublished online: 03 Dec 2014.

To cite this article: Jennifer Papoutsis, Robyn Stargatt & Cathy Catroppa (2014) Long-Term ExecutiveFunctioning Outcomes for Complicated and Uncomplicated Mild Traumatic Brain Injury Sustained inEarly Childhood, Developmental Neuropsychology, 39:8, 638-645, DOI: 10.1080/87565641.2014.979926

To link to this article: http://dx.doi.org/10.1080/87565641.2014.979926

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DEVELOPMENTAL NEUROPSYCHOLOGY, 39(8), 638–645Copyright © 2014 Taylor & Francis Group, LLCISSN: 8756-5641 print / 1532-6942 onlineDOI: 10.1080/87565641.2014.979926

Long-Term Executive Functioning Outcomesfor Complicated and Uncomplicated Mild Traumatic

Brain Injury Sustained in Early Childhood

Jennifer Papoutsis and Robyn StargattMurdoch Childrens Research Institute, Parkville, Australia, and

Department of Psychology, La Trobe University, Bundoora, Australia

Cathy CatroppaMurdoch Childrens Research Institute, Parkville, Australia

This study investigated long-term executive functioning following early mild traumatic brain injury(TBI), differentiating between complicated (n = 34) and uncomplicated injuries (n = 18). Childrenpost mild TBI were compared to 33 controls at least 7-years post-injury. The complicated mild TBIgroup performed significantly worse on divided attention compared to both groups, with younger ageat injury and neurological symptoms predictors of outcome. No significant group differences existedon speed of information processing, selective attention, working memory, or goal setting. These find-ings indicate that specific aspects of executive function are compromised by early complicated mildTBI and argue for a stratified definition of mild TBI.

Infants and toddlers present with the highest rate of traumatic brain injury (TBI), with approx-imately 80% of these being classified as mild (Brun & Hauser, 2003; Crowe, Babl, Anderson,& Catroppa, 2009). This is concerning given that early injuries potentially disrupt ongoing brainmaturation and the development of future skills, placing them at greater risk to residual deficitscompared to older children (DeLuca & Leventer, 2008; Dennis, 1989; Kolb, 1995). Furtherincreasing the risk of brain injury, young children also have weaker neck muscles that leadsto less resistance to the force of an impact and thin skulls that result in a greater diffuse patternof injury (Ommaya, Goldsmith, & Thibault, 2002). Despite a growing body of research in thisarea, outcomes following mild TBI in very young children are yet to be well understood as youngchildren are often excluded from studies due to limitations inherent in testing pre-verbal children.Alternatively, young children are included as part of a larger sample of “pre-school”-aged chil-dren (i.e., up to and including children aged 6 years), which is problematic given the variability ofneuronal development at different ages (Anderson & Moore, 1995; Catroppa, Anderson, Godfrey,& Rosenfeld, 2011; Gerard-Morris et al., 2010).

Correspondence should be addressed to Jennifer Papoutsis, Murdoch Childrens Research Institute, FlemmingtonRoad, Parkville, VIC 3052, Australia. E-mail: jennifer.papoutsis@mcri.edu.au

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IMPACT OF EARLY MILD TBI ON EXECUTIVE FUNCTIONING 639

Adding to this complexity is variability in the definition of mild TBI (Bigler, 2008). Recently,a stratified definition of mild TBI has been proposed to distinguish minor head injuries fromthose at the more “severe” end of the mild spectrum. The underlying notion is that a “thresh-old” of injury severity may need to be met for persisting cognitive and/or behavioral sequelaeto be apparent (McKinlay, Grace, Horwood, Fergusson, & MacFarlance, 2009). This stratifieddefinition has generated support in the adult literature, with studies showing that those who sus-tained injuries at the “severe” end of the mild spectrum presented with greater negative outcomes(Borgaro, Prigatano, Kwasnica, & Rexer, 2003; Hessen, Anderson, & Nestvold, 2008). Similarfindings have also been documented in pre-school-aged children, with greater longer-term behav-ioral problems reported in adolescence for those who received inpatient medical care comparedto those who were treated as outpatients (McKinlay, Dalrymple-Alford, Horwood, & Fergusson,2002; McKinlay et al., 2009).

Executive functioning is an umbrella term that encompasses the cognitive skills necessary forpurposeful, goal-directed behavior (Lezak, Howieson, & Loring, 2004). The prefrontal cortex,which subserves the executive functions and is relatively immature in childhood, is a commonsite of damage in TBI (Anderson & Catroppa, 2005). In terms of young children, Gerard-Morriset al. (2010) found that children who sustained a mild TBI between the ages of 3 and 6 yearsperformed more poorly on tasks of auditory working memory and inhibition at 18-months post-injury. At 10-years post-injury, Catroppa et al. (2011) found that children who sustained a mildTBI between the ages of 1 and 7 years old performed more poorly than controls on measuresof freedom from distractibility but not on other measures of attention. In contrast, Anderson,Catroppa, Morse, Haritou, and Rosenfeld (2005) failed to find differences between controls andchildren who sustained a mild TBI between the ages of 2- and 7-years on tasks of sustained atten-tion, selective attention, response inhibition or processing speed 30-months post-injury. Similarly,Nadebaum, Anderson, and Catroppa (2007) also failed to identify deficits in attentional control,cognitive flexibility, goal setting and information processing at 5-years post-injury for a sampleof children who sustained a mild TBI aged 7 years or younger. These differences among studiesmay represent methodological variations, particularly regarding the definition of mild TBI, age atinjury, time since injury, and the different measures used. Behavioral measures of executive func-tioning have also been measured using the Behavioral Rating Inventory of Executive Function(BRIEF; Gioia, Isquith, Guy, & Kenworthy, 2000), a caregiver questionnaire that measures exec-utive functioning in everyday life. Results from school-aged children suggest that behavioralmeasures of executive function are poorer in children with TBI but there are no known studies todate that have investigated this in very young children following mild TBI (Mangeot, Armstrong,Colvin, Yeates, & Taylor, 2002; Sesma, Slomine, Ding, & McCarthy, 2008; Vriezen & Pigott,2002).

In light of these, the purpose of this study was to investigate cognitive and behavioral mea-sures of executive functioning in children who sustained an early mild TBI, distinguishingbetween complicated and uncomplicated mild TBI. Given the protracted development of theexecutive functions, this study focused on examining outcomes several years after injury, aswell as the injury symptoms and demographics associated with outcome. It is hypothesizedthat the children with complicated mild TBI will perform more poorly compared to both theuncomplicated mild TBI and control groups on cognitive and behavioral measures of executivefunctioning.

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640 PAPOUTSIS, STARGATT, CATROPPA

METHOD

Participants

Two-hundred and fifty-eight children aged 4 years and younger who were diagnosed with a mildTBI were retrospectively identified from the Emergency Department admissions/presentationdatabase at the The Royal Childrens Hospital, Victoria, from January 2000 to December 2001.Medical records provided information about the patient’s personal details, a brief triage descrip-tion of the injury, primary language spoken, and the patient’s discharge destination. For childrenmeeting initial inclusion criteria (outlined below), the medical file was examined for general med-ical information, symptoms and medical investigations associated with the injury and qualitativeobservations of the child. Of this sample, one-hundred and seventeen children were excluded asEnglish was a second language (n = 53), significant medical or developmental delay (n = 43),additional head injury (n = 8), family located interstate (n = 8), non-accidental injury (n = 4),and child was deceased (n = 1). Of the remaining 141 eligible participants, fifty-one could not becontacted and 38 declined to participate. Fifty-two children participated in the study, representinga participation rate of 36.9% of eligible participants. There were no significant differences regard-ing age at injury between uncontactable families, those that declined and the recruited sample,F(2, 138) = 1.85, p = .16. Gender ratios were also similar (48% female for the uncontactable,declined sample and 56% for the mild TBI group).

Children with mild TBI were divided into severity groups based on Yeates and Taylor’s(2005) definition (see Table 1 for injury characteristics): complicated mild TBI (n = 34):(i) A reduced Paediatric Coma Scale score of one to two points below the age-adjusted highestscore and/or (Reilly, Simpson, Sprod, & Thomas, 1988); (ii) an observed LOC of 30 min-utes or less, and/or; (iii) two or more post concussive symptom including altered mental state

TABLE 1Demographics and Symptom Characteristics of the Complicated and Uncomplicated

Mild TBI Injury and Control Groups

Injury CharacteristicsComplicated Mild TBI

n = 34Uncomplicated Mild TBI

n = 18Controln = 33

Age at assessment (months)M (SD)

118.88 (14.04) 114.00 (15.81) 116.48 (20.48)

Gender 19 (55.88%) 10 (55.56%) 18 (54.54%)Socioeconomic status 1.88 (1.20) 1.78 (1.31) 1.79 (1.25)Age at injury (months) M (SD) 23.09 (13.58) 19.72 (14.58) —Reduced PCS n (%) 4 (11.76%) 0%LOC n (%) 8 (23.52%) 0%

<3 mins n (%) 7 (87.5%)>3 mins n (%) 1 (12.5%)

Postconcussive SymptomsDrowsiness 27 (79.4%) 0%Neurological Symptoms 10 (29.41%) 0%

Note. LOC = loss of consciousness; PCS = post concussive symptom; TBI = traumatic brain injury.

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IMPACT OF EARLY MILD TBI ON EXECUTIVE FUNCTIONING 641

(i.e., excessive drowsiness and lethargy) or neurological symptoms (dilated pupils, seizure orataxia); uncomplicated mild TBI (n = 18): (i) Normal Paediatric Coma Scale as adjusted for age;and (ii) no loss of consciousness; and (iii) no postconcussive symptoms. Other post-concussivesymptoms such as posttraumatic amnesia, nausea, headache, diplopia, and dizziness were notincluded as these cannot be reliably assessed in pre-verbal children. Across the complicated anduncomplicated mild TBI groups, there was an equal ratio of males to females, and there was nosignificant differences for age at injury, F(1, 50) = 4.39, p = .13.

A control sample of 33 typically developing children was recruited by advertisements placedat various locations inviting families to contact the researchers. Children were excluded from thestudy if English was their second language, they had a significant medical condition or develop-mental delay or were located outside of the state. The control group was selected to be comparableto the two injury groups based on age, gender ratios and social economic status. There were nosignificant differences noted between the groups based on age at assessment (F(2, 82) = .52,p = .59) or socioeconomic status (SES) (F(2, 82) = .39, p = .67) as measured by the Australianand New Zealand Classification of Occupations (ANSCO, 2006). To ensure that the groups werecomparable on intellectual functioning, their verbal and perceptual intellectual functions wereassessed, as measured by prorating Similarities and Vocabulary for Verbal Comprehension Indexand Matrix Reasoning and Block Design for Perceptual Reasoning Index as per instruction inthe Wecshler Intelligence Scale for Children–Fourth edition (WISC–IV), respectively F(2, 82) =.96, p = .39 and F(2, 82) = .07, p = .93.

Materials

Cognitive measures. Standardized cognitive measures in general clinical use wereselected. Scaled scores with a mean (M) of 10 and a standard deviation (SD) of 3 are reported inTable 2.

1. Speed of information processing. The Coding subtest from the WISC–IV was used tomeasure speed of information processing. This subtest requires children to copy basicgeometric symbols paired with numbers.

2. Working Memory. The Digit Span Backwards from the Digit Span subtest from theWISC–IV. In this task, children are required to reverse a sequence of numbers.

3. Attentional Control. The Sky Search subtest from the Test of Everyday Attention forChildren (TEA-Ch) requires children to locate identical pairs of spaceships amongdistracter items. Accuracy and speed of completion are used to calculate an overallattentional control score.

4. Divided Attention. The Sky Search–Dual Task (Sky Search–DT) from the TEA-Ch usesthe stimuli from the Sky Search with the simultaneous requirement to attend to and counta series of sounds explosions that they hear across multiple trials. The difference in per-formance between Sky Search and Sky Search–DT is calculated to give a decrement scoreof divided attention.

5. Goal setting and organization. The Block Design (M = 10, SD = 3) subtest from theWISC–IV asks children to organize colored blocks to match a series of designs ofincreasingly complexity.

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642 PAPOUTSIS, STARGATT, CATROPPA

TABLE 2Executive Function Measures for the Complicated and Uncomplicated Mild TBI Groups and Controls

Control Uncomplicated Mild TBI Complicated Mild TBIM (SD) M (SD) M (SD)95% CI 95% CI 95% CIn = 33 n = 18 n = 34

WISC–IV: Coding 9.97 (2.14) 11.25 (2.68) 10.97 (2.72)8.89, 10.53 9.69, 12.31 9.72, 11.79

WISC–IV: Digit SpanBackwards

10.63 (2.75) 11.22 (3.4) 10.38 (2.77)9.66, 11.61 9.52, 12.92 9.41, 11.35

TEA-Ch: Sky Attention 8.62 (2.57) 7.67 (2.85) 8.44 (1.86)7.91, 10.08 5.89, 9.04 7.66, 9.09

TEA-Ch: Sky Search DualTask

8.91 (3.17) 8.18 (2.89) 5.97 (3.07)∗∗7.85, 10.14 6.01, 9.37 4.71, 6.95

WISC–IV: Block Design 11.09 (2.31) 10.04 (2.67) 11.56 (2.43)10.27, 11.91 8.98, 11.09 10.56, 12.56

BRIEF: Behavioral regulationindex

46.79 (8.85) 45.62 (9.43) 48.51 (8.50)43.05, 50.33 39.92, 51.31 45.32, 51.78

BRIEF: Metacognition index 51.0 (12.99) 50.46 (11.27) 48.10 (10.36)44.79, 57.20 43.65, 57.27 44.16, 52.05

Note. BRIEF = Behavior Rating Inventory of Executive Function; TEA-Ch = Test of Everyday Attention for Children;WISC–IV = Wechsler Intelligence Scale–Fourth Edition.

Behavioral aspects of executive functioning. The Behavioral Rating Inventory ofExecutive Function–Parent Rated (BRIEF; Gioia et al., 2000) is a standardized parent-rated ques-tionnaire that assesses children’s everyday executive skills. Eight clinical scales (inhibit, shift,emotional control, initiate, working memory, plan/organize, organization of materials, and moni-tor) can be combined into two summary scale T-scores: Behavioural Regulation Index (BRI) andMetacognition Index (MI). Higher scores indicate greater symptom severity, with scores overabove 65 considered to have potential clinical significance.

Procedure

Parents of children who met the selection criteria were invited to participate in the study. Writtenconsent was obtained, according to Hospital ethical guidelines. All assessments were conductedby a qualified provisional psychologist over a single 2-hour session. Order of test administrationwas counterbalanced to minimise fatigue effects. Parents completed the questionnaires while theirchild completed the assessment.

Statistical Analysis

Quantitative analyses were conducted using SPSS version 18.0. Prior to all statistical analy-ses, data were examined for violations of test assumptions. Group differences were comparedexamined using separate Analyses of Variance (ANOVA). Post Hoc comparisons were madeusing Tukey test when significant group differences were identified. Exploratory analyses were

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IMPACT OF EARLY MILD TBI ON EXECUTIVE FUNCTIONING 643

conducted using Pearson-product moment correlations and Spearman’s rho to examine the rela-tionship between significant findings, demographic and injury related variables (i.e., LOC, alteredmental state, neurological symptom/s, and age at injury).

RESULTS

Cognitive Aspects of Executive Function

Group differences existed for Sky DT, η2 = .17, F(2, 81) = 7.85, p = .00, indicating a small effectsize. Post-hoc comparison showed the complicated mild TBI group performed significantly worseon divided attention compared to the uncomplicated mild TBI and control group. There wereno significant group differences between the three groups on Digit Span Backwards, η2 = .00,F(2, 82) = .49, p = .61, Block Design, η2 = .00, F(2, 82) = 2.16, p = .81, Coding, η2 = .04,F(2, 82) = 1.85, p = .16, or Sky Attention, η2 = .02, F(2, 82) = .98, p = .39.

Exploratory analysis examined the relationship between demographics and injury symptomswith performance on Sky-DT. Performance on Sky-DT was significantly negatively correlatedwith neurological symptoms (r = –.33, p = .03), suggesting that performance on Sky DT waslowest for children who presented with at least one neurological symptom following their injury.Age at injury (r = .33, p = .04) was also significantly correlated with Sky DT, such that youngerage at injury was associated with poorer performance. No significant correlations existed for LOC(r = .20, p = .13); SES (r = .05, p = .38), altered mental state (r = .09; p = .31). Significantvariables were entered into a multiple regression which showed that 28.6% of the variance of SkyDT was accounted for by neurological symptoms and age at injury, R2 = .29, F(2, 30) = 6.00,p = .01.

Behavioral Measures of Executive Functioning

No significant group differences were found for BRI, η2 = .03, F(2, 63) = 1.01 or p = .37; MI,η2 = .00, F(2, 63) = .06, p = .95.

DISCUSSION

The aim of this study was to investigate whether children who sustained a complicated mildTBI early in childhood performed more poorly on cognitive and behavioral measures of exec-utive functioning compared to those who sustained an uncomplicated mild TBI and typicallydeveloping children.

The findings partially supported the hypothesis as the complicated mild TBI group performedmore poorly on measures of divided attention compared to both the uncomplicated mild TBIand control group. No significant differences existed for other aspects of executive function-ing, including attentional control, goal setting, information processing, and working memory.The findings suggest that a complicated early TBI sustained early in life may disrupt the typicaldevelopment of some aspects of executive function. This finding is not surprising given that sub-components of executive function follow different developmental trajectories. Attentional control

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and working memory are considered one of the earliest executive skills to emerge, with the devel-opment of these basic skills increasing the processing capacity of the brain, which allows for thedevelopment of more specialized, higher-level skills such as divided attention.

Younger age at injury and neurological symptom/s (i.e., dilated pupils, seizure or ataxia) wasassociated with lowest performance on divided attention, suggesting that these symptoms mayhelp to identify children at greatest risk following mild complicated TBI. PCS, LOC, and alteredmental state were not predictive of outcome, possibly indicating that these measures may be lesssensitive in grading severities of mild TBI. Alternatively, it is possible that the assessments thatwere employed in this study were not sensitive enough to detect differences among groups.

Despite this significant finding in divided attention, there were no significant group differenceson behavioral measures of executive function. The BRIEF does not show a high consistency withcognitive measures of executive function and is thought to tap into different aspects of executivefunction (McAuley, Chen, Goos, Schachar, & Crosbie, 2010).

There were no differences between the controls and uncomplicated mild TBI group, suggest-ing that the latter suffered injuries that did not disrupt underlying brain function. In line withMcKinlay et al.’s (2009) view, the current findings argue for the adoption of a stratified defini-tion of mild TBI to help distinguish between those children who are more likely to have ongoingcognitive deficits as a result of brain injury from those with superficial head injuries. This studyadds to the emerging evidence that it is important to make this distinction between severities ofmild TBI. By not doing so researchers run the risk of “masking” outcome findings associatedwith these brain injuries.

This study examined children at a single time-point and as such provides little insight into thetrajectory of recovery. The uneven and small sample size can be associated with low statisticalpower and additional differences between groups may have been identified with a larger sample.It is also possible that the current measures used to measure executive functioning were notsensitive enough to pick up more subtle differences. This study relied on documented symptomsof TBI to characterize injury severity and it is likely that prospective studies would be able toprovide independent evidence of neuropathology.

Overall, the findings of this study suggest that complicated mild TBI sustained at the age offour years or younger may be associated with poor development of divided attention. In termsof risk factors, younger age at injury and neurological symptoms may potentially identify thosechildren at highest risk. These findings lend support to a stratified definition of mild and suggeststhat younger children with neurological symptoms on admission may be at increased risk to theimpact of traumatic brain injury.

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