Pediatric Traumatic Brain Injury andAttention DeficitMarsh Königs, MSca, Hugo A. Heij, MD, PhDb, Johannes A. van der Sluijs, MD, PhDc, R. Jeroen Vermeulen, MD, PhDd,J. Carel Goslings, MD, PhDe, Jan S.K. Luitse, MDf, Bwee Tien Poll-Thé, MD, PhDg, Anita Beelen, PhDh,i, Marleen van der Wees, PhDj,Rachèl J.J.K. Kemps, PhDk, Coriene E. Catsman-Berrevoets, MDl, Jaap Oosterlaan, PhDa,m

abstractBACKGROUND: We investigated the impact of pediatric traumatic brain injury (TBI) on attention,a prerequisite for behavioral and neurocognitive functioning.

METHODS: Children aged 6 to 13 years who were diagnosed with TBI (n = 113; mean 1.7 yearspostinjury) were compared with children with a trauma control injury (not involving the head)(n = 53). TBI severity was defined as mild TBI with or without risk factors for complicated TBI(mildRF+ TBI, n = 52; mildRF2TBI, n = 24) or moderate/severe TBI (n = 37). Behavioral functioningwas assessed by using parent and teacher questionnaires, and the Attention Network Testassessed alerting, orienting, and executive attention. Ex-Gaussian modeling determined thecontribution of extremely slow responses (lapses of attention) to mean reaction time (MRT).

RESULTS: The TBI group showed higher parent and teacher ratings of attention and internalizingproblems, higher parent ratings of externalizing problems, and lower intelligence than the controlgroup (P, .05, d$ 0.34). No effect of TBI on alerting, orienting, and executive attention was observed(P $ .55). MRT was slower in the TBI group (P = .008, d = 0.45), traced back to increased lapses ofattention (P = .002, d = 0.52). The mildRF2TBI group was unaffected, whereas the mildRF+ TBI andmoderate/severe TBI groups showed elevated parent ratings of behavior problems, lower intelligence,and increased lapses of attention (P# .03, d$ 0.48). Lapses of attention fully explained the negativerelation between intelligence and parent-rated attention problems in the TBI group (P = .02).

CONCLUSIONS: Lapses of attention represent a core attention deficit in children with mildRF+ TBI(even in the absence of intracranial pathology) or moderate/severe TBI, and relate to daily lifeproblems after pediatric TBI.

WHAT’S KNOWN ON THIS SUBJECT: Attention isa prerequisite for neurocognitive and behavioralfunctioning, having a crucial role in academicand social child development. Children withtraumatic brain injury have pronounced deficitsin attention, but the nature and consequences ofthese deficits remain unclear.

WHAT THIS STUDY ADDS: Lapses of attentionrepresent a core attention deficit after pediatricmild traumatic brain injury with risk factors forcomplicated traumatic brain injury, ormoderate/severe traumatic brain injury.Importantly, lapses of attention explain therelation between intelligence and parent-ratedattention problems.

aDepartment of Clinical Neuropsychology, VU University Amsterdam, Amsterdam, Netherlands; bPediatric SurgicalCenter of Amsterdam, Emma Children’s Hospital Academic Medical Centre and VU University Medical Center,Amsterdam, Netherlands; Departments of cPediatric Orthopedics, and dPediatric Neurology, VU University MedicalCenter, Amsterdam, Netherlands; eTrauma Unit, and Departments of fEmergency Medicine, and gPediatricNeurology, Academic Medical Center, Amsterdam, Netherlands; hMerem Rehabilitation Center ‘De Trappenberg,’Huizen, Netherlands; iDepartment of Rehabilitation, Academic Medical Centre, Amsterdam Netherlands; jLibraRehabilitation Medicine and Audiology ‘Blixembosch’, Eindhoven, Netherlands; kLibra Rehabilitation Medicine andAudiology ‘Leijpark’, Tilburg, Netherlands; lDepartment of Pediatric Neurology, Erasmus Medical Centre,Rotterdam, Netherlands; and mEmma Children’s Hospital Academic Medical Centre, Amsterdam. Netherlands

Mr Königs and Prof Oosterlaan conceptualized and designed the study; Mr Königs carried out theanalyses and drafted and revised the manuscript; Professors Heij, Vermeulen, Goslings, Poll-Thé,and Oosterlaan, Drs Sluijs, Beelen, van der Wees, Kemps, Mr Luitse, and Ms Catsman-Berrevoetsreviewed and revised the manuscript; and all authors approved the final version of the manuscript.

www.pediatrics.org/cgi/doi/10.1542/peds.2015-0437

DOI: 10.1542/peds.2015-0437

Accepted for publication Jun 15, 2015

Address correspondence to Mr Marsh Königs, VU University Amsterdam, Clinical Neuropsychology,van der Boechorststraat 1, Amsterdam, Netherlands 1081BT. E-mail: m.konigs@vu.nl

PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275).

Copyright © 2015 by the American Academy of Pediatrics

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Traumatic brain injury (TBI) is theleading cause of death and acquireddisability in children andadolescents.1 Children with TBIsuffer from neurocognitiveimpairments and are at risk forderailed academic and socialdevelopment.2,3 Attention isa prerequisite for behavioral andneurocognitive functioning, byselecting environmental sensoryinformation for perception andgating the information flow to andfrom memory.4–6 Therefore,attention deficits may play a key rolein the consequences of pediatric TBI.

Interacting neural networks directalerting, orienting, and executiveattention, facilitating the abilities to(1) achieve and maintain an alertstate, (2) spatially orient toenvironmental information, and (3)resolve conflict between competingresponses, respectively.7 A review ofstudies investigating attention afterpediatric TBI revealed that deficits inattention are prominent in thesubacute phase of recovery and oftenpersist into the chronic phase.8

Attention deficits have been observed#10 years postinjury, in particularafter severe TBI.9 Aspects of attentionrelated to executive attention aremost consistently affected, but resultsheavily depend on the tests used tomeasure attention.8 The disparatefindings in the literature mayoriginate partly from the use oftraditional paper-and-pencil tests,which often lack the ability to isolateaspects of attention from processingspeed and visuomotorcoordination,8,10 while thesefunctions have consistently beenfound to be affected after TBI.11,12

The Attention Network Test (ANT)has been developed to measure theefficiency of alerting, orienting, andexecutive attention and overcomesdrawbacks of traditional measures bycorrecting for processing speed andminimizing the load on visuomotorfunctions.13 One study used the ANTto investigate attention in adolescents

with mild TBI, identifying a deficit inexecutive attention 1 monthpostinjury.14 Recent evidence fromadults additionally suggests that TBIcauses momentary lapses of attention(ie, short moments of attention loss)that cause extremely slow responseson timed tasks.15

The current study uses the ANT toidentify the nature of attentionproblems after pediatric TBI alongthe complete span of injury severity.We hypothesized that children withTBI have impaired executiveattention and increased lapses ofattention. In addition, the role ofattention deficits in behaviorproblems and intelligence wasexplored.

METHODS

Participants

Sample

This study compared a TBI group of113 children to a trauma control(TC) group of 53 children withtraumatic injury not involving thehead, to control for preinjury riskfactors of traumatic injury andpsychological effects ofhospitalization and medicalinterventions.16 All children wereretrospectively recruited froma consecutive cohort of 3 university-affiliated level I trauma centers andseveral rehabilitation centers in theNetherlands. Inclusion criteria were(1) age 6 to 13 years, (2) proficientin the Dutch language, (3) hospitaladmission with a clinical diagnosis ofTBI for inclusion in the TBI group,(4) hospital admission for traumaticinjuries below the clavicle17 forinclusion in the TC group, and (5).2months postinjury. Exclusion criteriawere (1) previous TBI, (2) visualdisorder interfering withneurocognitive testing, or (3) currentcondition, other than TBI, affectingthe central nervous system. Of all375 children admitted from October2009 to October 2013 who wereeligible for inclusion (TBI, n = 232;

TC, n = 143), 54 were not reached(TBI, n = 39; TC, n = 15) and 137declined participation (TBI, n = 68;TC, n = 69). Main reasons not toparticipate were as follows: notinterested (TBI, 25%; TC, 32%), notime (TBI, 22%; TC, 22%), or load onchild (TBI, 8%; TC, 16%). Eighteenchildren were excluded (TBI: n = 6not proficient in Dutch, n = 5 ageexceeding criterion, n = 1 motorretardation; TC: n = 3 not proficientin Dutch, n = 1 previous TBI, n = 1brain tumor, n = 1 mentalretardation). Participation rate washigher in the TBI group (n = 113,49%) than the TC group (n = 53,37%) (P = .03), but study samplesdid not differ from their respectivecohorts in age or gender (P $ .14).

Injury Severity

Diagnosed injuries, the lowest scoreon the Glasgow Coma Scale (GCS) onthe day of admission, and admissionduration were extracted from medicalfiles, as well as risk factors forcomplicated mild TBI according to theEuropean Federation of NeurologicSocieties guidelines on mild TBI:impaired consciousness (GCS # 15),focal neurologic deficits, persistentvomiting ($3 episodes), postinjuryepileptic insults, progressiveheadache, and abnormal headcomputed tomography scan.18 Injuryseverity was categorized into mildTBI (GCS 15 to 13, loss ofconsciousness duration #30 minutes,posttraumatic amnesia duration#1 hour) without risk factors(mildRF– TBI, n = 24) or with $1 riskfactor (mildRF+ TBI, n = 52) andmoderate/severe TBI (GCS 12 to 3,loss of consciousness duration $30minutes, posttraumatic amnesiaduration $1 hour; n = 37).19

Measures

Demographic Information

Data on gender, age, socioeconomicstatus (SES), and diagnosedpsychiatric or learning disorderswere collected by using a parentalquestionnaire. SES was defined as the

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average level of parental educationranging from 1 (no education) to8 (postdoctoral education).20

Behavioral Functioning

Parent and teacher ratings ofattention problems, internalizingproblems (eg, anxiety), andexternalizing problems (eg,aggression) were obtained by usingthe widely used Child BehaviorChecklist, Strength and DifficultiesQuestionnaire, and their teacherequivalents, which have adequatepsychometric properties.21,22

Questionnaire scales measuringhighly overlapping symptom domains(0.88 $ r $ 0.72) were collapsed forparents and teachers separately(sum of z-transformed raw scores) toyield aggregated parent and teacherratings of attention and internalizingand externalizing problems.

Intelligence

Full-scale IQ (FSIQ) was estimated byusing a short form of the WechslerIntelligence Scale for Children III(including the subtests Vocabulary,Similarities, Block Design, and PictureArrangement), with excellent validity(r = 0.93) and reliability (r = 0.93) inestimating FSIQ.23

Attention Performance

We used a child-friendly adaptationof the ANT (Fig 1).13 Childrenresponded to a target presented onthe left or right side of a computerscreen by pressing thecorresponding button. Targetsappeared in 4 trial types containingno cue, a central cue, a valid locationcue, or an invalid location cue. Themain dependent measure was meanreaction time (MRT). Alerting,orienting, and executive attentionwere assessed by the difference inMRT between (1) no-cue trials andcentral-cue trials, (2) central-cuetrials and valid-location-cue trials,and (3) valid-location-cue trials andinvalid-location-cue trials. Speed ofprocessing was assessed by MRT onno-cue trials to prevent attention

networks from contaminating theanalysis. As lapses of attention causeextremely slow responses that inflateMRT, we used so-called ex-Gaussianmodeling of reaction timedistributions to calculate thecontribution of extremely slowresponses to MRT (t), measuringlapses of attention.24 Likewise, wecalculated MRT as corrected forextremely slow responses (m),measuring processing speedadjusted for lapses of attention.Background information on ex-Gaussian modeling and its clinicalutility for psychiatric and neurologicdisorders is providedelsewhere.24–26 Table 1 provides anoverview of measures derived fromthe ANT.

Procedure

The families of eligible children weresent an information letter andcontacted by telephone 2 weekslater. After written informed consentwas provided by parents andchildren aged .11 years, trainedexaminers administered a fixedneurocognitive test battery whileparents filled out questionnaires in

a waiting room. Thereafter, teacherswere contacted to fill outquestionnaires. The ANT wasadministered using 15-inch laptopsat 50-cm viewing distance withstandardized instructions in a coverstory, 30 practice trials, and 6 blocksof 60 experimental trials presentedin fixed randomized order (duration26 minutes). This study was part ofa study registered at Clinicaltrials.gov (NCT01720979) and wasapproved by the VU UniversityMedical Centre medical ethicscommittee (NL37226.029.11).

Statistical Analyses

Statistical analyses were performedby using SPSS 22.0. All dependentvariables were screened for outliers(P , .001) that were rescaledaccording to Tabachnick and Fidell.27

Missing data (1% to 6%) wereimputed by using multipleimputation.28 Differences indemographics, injury-relatedinformation, and clinical diagnoseswere assessed between all groupsusing independent t tests andx2 tests.

FIGURE 1Schematic representation of the ANT. ISI, interstimulus interval; RT, reaction time.

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Parent and teacher ratings ofattention and internalizing andexternalizing problems weresubjected to multivariate analysis ofvariance (MANOVA) with group asbetween-subject factor (TBI-TC), andANOVA assessed group differences inFSIQ. To assess alerting, orienting,and executive attention, MRT wassubjected to 3 repeated-measuresANOVAs, with group as between-subject factor (TBI-TC) and trial typeas within-subject factor (no cue/central cue, central cue/valid spatialcue, and valid spatial cue/invalidspatial cue). Differences betweengroups in (1) processing speed, (2)lapses of attention, and (3)processing speed adjusted for lapsesof attention were assessed bycomparing MRT, t, and m,respectively, using ANOVA. Whena group difference for t was found,we investigated whether this wasdriven by more frequent and/orlonger lapses by comparing thenumber and MRT of extremely slowresponses (reaction time . m + 2SD)between groups. Variables for whicha significant group difference wasobtained were analyzed for theirassociation with time since injuryusing Pearson correlationcoefficients to analyze recoveryeffects. Likewise, analysesdifferentiating between TBI severity

groups were performed on onlythose variables that showeddifferences between the TBI and TCgroup, to reduce the risk of type Ierrors while maintaining acceptablestatistical power in comparing therelatively small groups. Statisticaltesting was 2-sided at a = 0.05, andeffect sizes of group differences werecalculated as Cohen d.29

RESULTS

Demographics, Injury-RelatedInformation, and Clinical Diagnoses

The TBI group (n = 113) did notdiffer from the TC group (n = 53) indemographics, injury-relatedinformation, or clinical diagnoses(Table 2), except for lower SES in theTBI group and more extracranialfractures and orthopedic surgery inthe TC group. Likewise, the TBIseverity groups did not differ fromthe TC group in demographicvariables, except for lower SES in themildRF+ TBI and moderate/severeTBI groups. The moderate/severeTBI group had longer hospitaladmission, lower GCS scores, andmore neurosurgery than all othergroups (P # .001), whereasprogressively more cranial fracturesand intracranial pathology wereobserved in the mildRF2, mildRF+, and

moderate/severe TBI groups(P , .01). Differences in theprevalence of psychiatric conditionsreached significance only betweenthe mildRF+ TBI and TC groups (P = .05).

Behavior Problems and IntelligenceAfter TBI

TBI Versus TC Group

Parent ratings of attention andinternalizing and externalizingproblems were higher for the TBIgroup than the TC group (Table 3). TheTBI group also showed higher teacherratings of attention and internalizingproblems than the TC group, while nodifferences were observed onexternalizing problems. The TBI grouphad lower FSIQ than the TC group.Time postinjury in the TBI group wasnot related to ratings of behaviorproblems or FSIQ (r # 0.10, P # .29).

TBI Severity Groups

The mildRF2 TBI group did not differfrom the TC group in parent andteacher ratings of attention orinternalizing and externalizingproblems (P $ .07, d = 20.07 to 0.57)or FSIQ (P = .44, d = 20.20), except forhigher teacher ratings of internalizingproblems (P = .04, d = 20.61). ThemildRF+ TBI group showed higherparent ratings of attention andinternalizing and externalizingproblems (P # .03, d = 0.48 to 0.63),higher teacher ratings of attention andinternalizing problems (P = .002,d = 0.59, and P = .008, d = 0.56,respectively), and lower FSIQ (P = .01,d = 20.52) than the TC group. Themoderate/severe TBI group had higherparent ratings of internalizing andexternalizing problems (P = .001,d = 0.75, and P = .005, d = 0.61,respectively), higher teacher ratings ofinternalizing problems (P = .003,d = 0.70), and lower FSIQ (P = .03,d =20.50) than the TC group. Differencesbetween the moderate/severe TBI andTC groups in parent and teacher ratingsof attention problems did not reachsignificance (P . .12), althoughexploratory analyses revealed thatchildren with severe TBI (n = 21) did

TABLE 1 Measures Derived From the ANT

Variable Description

Alerting attention The ability to achieve and maintain an alert state, measured bythe decrease in MRT between ANT no-cue trials and central-cue trials.

Orienting attention The ability to spatially orient to environmental information,measured by the decrease in MRT between ANT central-cuetrials and valid-cue trials.

Executive attention The ability to resolve conflict between competing responses,measured by the increase in MRT between ANT valid-cuetrials and invalid-cue trials.

Processing speed Information processing speed, measured by MRT on ANT no-cuetrials.

t The contribution of extremely slow responses (ie, shortmoments of attention loss, lapses of attention) toinformation processing speed (MRT), calculated using so-called ex-Gaussian analysis.24–26

m Information processing speed adjusted for the impact ofextremely slow responses (lapses of attention), calculatedusing so-called ex-Gaussian analysis.24–26

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have higher parent ratings of attentionproblems than the TC group (P = .04,d = 0.53). There were no significantdifferences between the TBI severitygroups on behavior ratings or FSIQ(P$ .08), except for higher teacher ratingsof attention problems in the mildRF+ TBI

group compared with the moderate/severe TBI group (P = .03, d = 0.47).

Attention Function After TBI

TBI versus TC Group

Although children with TBI showedslower performance in all trial types,

no differences were observed in theefficiency of alerting attention (P = .69,d = 0.04), orienting attention (P = .55,d = 0.18), and executive attention(P = .84, d = 0.07), indicating that childrenwith TBI have no specific deficits inthese aspects of attention (Fig 2).

TABLE 2 Analysis of Demographic and Injury-Related Characteristics in TBI and TC Groups

Characteristic Group Contrast TBI Severity Group Contrast

TBI TC P d MildRF2 (1) MildRF+ (2) Moderate/Severe (3)

n 113 53 24 52 37DemographicsMale gender 56 51 .56 46 60 57Age at testing, y 8.8 (2.0) 9.3 (2.1) .11 -0.27 8.7 (2.1) 8.8 (2.0) 8.8 (2.0) NSSES 5.3 (1.3) 5.9 (1.2) .006a -0.47 5.3 (1.2) 5.3 (1.3) 5.3 (1.4) TC . 2 and 3

Injury-related informationAge at injury, y 7.1 (2.3) 7.8 (2.2) .07 -0.30 7.0 (2.4) 7.1 (2.2) 6.9 (2.5) NSLowest GCS 12.6 (3.5) 15.0 (0.0) 14.6 (0.7) 8.3 (2.8) 1 and 2 . 3Hospital admission, d 6.8 (18.2) 1.4 (1.8) 0.9 (0.3) 2.3 (2.8) 17.0 (29.4) 3 . TC, 1, and 2Time since injury, y NSMean (SD) 1.7 (1.1) 1.6 (0.8) .37 0.15 1.7 (1.0) 1.7 (1.0) 1.8 (1.2)Range 0.3–5 0.4–4 0.5–4 0.3–4 0.4–5

Extracranial fracture 15 76 ,.001a 4 15 22 TC . 1, 2, and 3More than 1 extracranial fracture 6 8 .74 0 6 11 NSCranial fracture 36 0 35 62 3 . 2 . 1Intracranial pathology 36 0 31 68 3 . 2 . 1Orthopedic surgery 8 79 ,.001a 4 14 3 TC . 1, 2, and 3Neurosurgery 11 0 0 32 3 . 1 and 2

Diagnosed conditionsPsychiatric disorder 8 2 .13 4 12 5 2 . TCPremorbid ADHD 4 0 .17 0 6 3 NSLearning disorder 8 6 .60 8 8 8 NS

Values are expressed as % or mean (SD). ADHD, attention deficit/hyperactivity disorder; NS, not significant.a Statistically significant at P , .05.

TABLE 3 Analysis of Parent and Teacher Ratings of Behavior, FSIQ, and ANT Performance in TBI and TC Groups

Characteristic Group Contrast TBI Severity Groups Contrast

TBI TC P d MildRF2 (1) MildRF+ (2) Moderate/Severe (3)

n 113 53 24 52 37Parent ratingsa .003b

Attention problems 0.2 (1.9) 20.5 (1.8) .02b 0.40 0.1 (1.5) 0.4 (2.0) 0.1 (2.1) 2 . TCInternalizing problems 0.3 (2.0) 20.7 (1.4) ,.001b 0.60 0.09 (1.8) 0.3 (2.0) 0.6 (2.2) 2 and 3 . TCExternalizing problems 0.3 (2.0) 20.6 (1.2) .004b 0.49 0.2 (1.6) 0.2 (1.9) 0.5 (2.5) 2 and 3 . TC

Teacher ratingsa .004Attention problems 0.2 (2.0) 20.5 (1.8) .03b 0.37 20.1 (1.8) 0.7 (2.2) 20.2 (1.6) 2 . TCInternalizing problems 0.3 (2.0) 20.7 (1.3) .001b 0.56 0.2 (1.8) 0.3 (2.0) 0.5 (2.0) 1, 2, and 3 . TCExternalizing problems 0.0 (1.9) 20.1 (1.8) .61 0.09

FSIQ 98.4 (15.6) 105.0 (14.4) .01b 20.43 102.0 (16.3) 97.3 (15.4) 97.6 (15.4) TC . 2 and 3ANT performancec

MRT in ms 619 (122) 563 (130) .008b 0.45 600 (136) 615 (124) 637 (110) 2 and 3 . TCEx-Gaussian parameterst, ms 164 (69) 131 (51) .002b 0.52 158 (79) 160 (70) 173 (62) 2 and 3 . TCLapses, sum 58.0 (15.5) 54.1 (16.7) .14 0.25Lapse duration, ms 744 (153) 676 (159) .009b 0.44 713 (156) 746 (153) 772 (152) 3 . TCm, ms 454 (69) 432 (96) .09 0.28

Values are expressed as mean (SD).a Aggregated ratings (sum of z-transformed raw scores).b Statistically significant at P , .05.c Based on ANT no-cue trials.

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Analyses on MRT, t, and m in no-cue trials are displayed in Table 3.The TBI group showed higher MRTthan the TC group, suggesting thatchildren with TBI had slowerprocessing speed. However, theTBI group also had higher t than theTC group, whereas no groupdifference was obtained for m.These findings indicate thatchildren with TBI demonstrateincreased lapses of attention relativeto the TC group, while havingunaffected processing speed whenaccounting for lapses of attention.The number of lapses of attentiondid not differ between the TBI andTC groups, but lapses of attentionwere found to be longer in the TBIgroup (Table 3). t was not relatedto time postinjury in the TBI group(r = 0.00, P = .97).

TBI Severity Groups

The mildRF2 TBI group did notsignificantly differ from the TC groupon t (P = .08, d = 0.46). Relative tothe TC group, t was higher in themildRF+ TBI group (P = .02, d = 0.49)and moderate/severe TBI group(P = .002, d = 0.77), driven by longerlapses of attention in the moderate/severe TBI group (P = .02, d = 0.52).There were no significant differences

between the TBI severity groupson t (P $ .35).

Exploring the Role of Lapses ofAttention

The literature indicates thatintelligence is predictive of behaviorproblems in children with TBI,a relationship hypothesized toreflect the importance ofneurocognitive functioning forbehavioral regulation.30 In line withthis hypothesis, lower FSIQ wasrelated to higher parent and teacherratings of attention and internalizingproblems and parent ratings ofexternalizing problems in the TBIgroup (P , .02). We exploredwhether lapses of attention mayaccount for the negative relationshipbetween FSIQ and behavioral ratingsin children with TBI, usingbootstrapping mediation models (asFSIQ is age-corrected, we likewiseage-adjusted behavior ratings and t

using linear regression).31 LowerFSIQ was related to higher t (Fig 3,Path A), and higher t was in turnrelated to higher parent ratings ofattention (Path B). Importantly, tmediated the relation between FSIQand parent ratings of attention(P = .02), fully accounting for theobserved relation betweenintelligence and attention problems(Path C9). t was not related to parent

ratings of internalizing andexternalizing problems or teacherratings of attention and internalizingproblems (P . .15), indicating thatlapses of attention did not mediateinternalizing and externalizingproblems or teacher ratings ofattention.

Influence of Confounders

To investigate the potential influenceof SES on the observed differencesbetween the mildRF+ and moderate/severe TBI groups relative to the TCgroup, the latter was matched on SES1:2 (62) to a collapsed mildRF+ andmoderate/severe TBI group.Demographic variables did not differbetween the matched TC group(n = 44) and the original TC group(P = .95 to .13) or the collapsedmildRF+ moderate/severe TBI group(n = 88; P = .46 to .16). All reportedgroup differences were replicatedwhile (1) comparing the matched TCgroup and collapsed mildRF+ andmoderate/severe TBI group,indicating that SES did not confoundthe reported results; (2) using datawithout missing value imputation;and (3) excluding all children withintracranial pathology (n = 16) orpremorbid attention deficit/hyperactivity disorder (n = 3) fromthe mildRF+ TBI group, indicatingthat intracranial pathology orpremorbid attention deficit/hyperactivity disorder did notaccount for the reported deficits inchildren with mildRF+ TBI.

DISCUSSION

This study indicates that childrenwith TBI do not have persistingdeficits in alerting, orienting, orexecutive attention, but ratherexhibit impaired consistency asreflected by lapses of attention(ie, short moments of attentionloss), representing a core attentiondeficit after pediatric TBI. Lapses ofattention were found to explainthe negative relation betweenintelligence and parent ratings of

FIGURE 2ANT performance by the TBI and TC groups separated for trial types. Error bars represent SE.*P , .05, **P , .01, ***P , .001.

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attention problems, suggesting animportant role for lapses ofattention in daily life functioningafter pediatric TBI.

The results contrast with previousfindings indicating impairedexecutive attention in pediatric TBI,as established in a recent review ofthe literature.8 Most studies coveredin that review used traditionalpaper-and-pencil tests of attention,often not correcting for confoundingeffects of deficits in processingspeed or visuomotor functions thatmay co-occur after TBI.11,12 TheANT, which controls for theseconfounders, revealed no evidencefor impaired alerting, orienting, orexecutive attention, possiblyreflecting the importance ofcorrecting for processing speed andvisuomotor functions in tests ofattention. The results furtherrevealed no evidence for attentiondeficits after mildRF2 TBI, whileindicating that children with mildRF+

TBI or moderate/severe TBI haveincreased lapses of attention. Asexpected, we found that lapses ofattention (1) account for decreasedprocessing speed; (2) are driven byprolonged lapses of attention, not bymore lapses; (3) relate tointelligence and parent-observedattention problems; and (4) fully

explain the negative relationbetween intelligence and parentratings of attention problems. Theseresults suggest that lapses ofattention play an important role indaily life functioning after pediatricTBI, although the observedrelationships do not necessarilyimply causal mechanisms. Lapses ofattention were not related toteacher observations of attentionproblems, possibly becausebehavior associated with lapses ofattention goes unnoticed incrowded classrooms.32

This study has some weaknesses.The participation rate was higher inthe TBI group than the TC group,potentially accounting for the groupdifference on SES that was observeddespite the recruitment of a traumacontrol group to control forpreexisting trauma risk factors andpsychological effects ofhospitalization and medicalinterventions.33 Confoundinganalysis showed that SES did notaccount for the reported results. ThemildRF2 TBI group had a smallsample size, limiting the statisticalpower of group comparisons.Furthermore, this was a multicenterstudy, potentially introducingheterogeneity in the treatment of TBIwithin our sample; however, this also

increases the generalizability of ourresults.

CONCLUSIONS

This study proposes an importantrole of lapses of attention inattention performance, intelligence,and behavioral functioning ofchildren with TBI. Cliniciansshould be aware that slowerprocessing speed after pediatric TBImay actually reflect an attentiondeficit, characterized by momentarylapses of attention that likely playa role in daily life problems.Importantly, the long-term negativeeffects of mildRF+ TBI on lapses ofattention were even observed in theabsence of intracranial pathology,suggesting that clinicians shouldconsider routine screening ofchildren with mildRF+ TBI forneurocognitive and behavioralsymptomatology. Interventionsaimed at improving attention andprocessing speed should considerlapses of attention amongprimary outcomes. Pharmacologicstimulant treatment has proven toeffectively decrease lapses ofattention in children with ADHD34

and pediatric cancer survivors,35

possibly providing a promisingtreatment of children with TBI aswell.

ABBREVIATIONS

ANT: Attention Network TestFSIQ: full-scale IQGCS: Glasgow Coma ScaleMRT: mean reaction timeSES: socioeconomic statusTBI: traumatic brain injury

FINANCIAL DISCLOSURE: The authors have indicated they have no financial relationships relevant to this article to disclose.

FUNDING: This work was supported by the Netherlands Organization for Scientific Research, grant number 022.003.010.

POTENTIAL CONFLICT OF INTEREST: The authors have indicated they have no potential conflicts of interest to disclose.

FIGURE 3Mediation model testing the influence of t in the relation between FSIQ and parent ratings ofattention problems in the TBI group. B values reflect raw regression coefficients.

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