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pilepsy Research (2011) 97, 112—123

j ourna l ho me pag e: www.elsev ier .com/ locate /ep i lepsyres

cademic achievement in children with epilepsy: review

olin Reillya,∗, Brian G.R. Nevilleb

Research and Psychology Department, National Centre for Young People with Epilepsy, Lingfield, Surrey, United KingdomUCL Institute of Child Health, London, United Kingdom, and National Centre for Young People with Epilepsy, Lingfield, Surrey,nited Kingdom

eceived 9 March 2011; received in revised form 23 July 2011; accepted 31 July 2011vailable online 15 September 2011

KEYWORDSLow academicachievement;Academicunderachievement;Prevalence;Correlates;Learning disability

SummaryObjective: To examine published studies which have focussed on academic achievement inchildren with epilepsy with respect to prevalence rates of academic difficulties and possiblecorrelates of academic achievement.Methods: This review examines studies which have focussed on prevalence rates of academicdifficulties and correlates of academic achievement in children with epilepsy from 1990 to 2010.Prevalence rates of low academic achievement and academic underachievement are reportedand correlates of academic achievement including seizure/epilepsy variables, demographicvariables, and child/family variables are examined with respect to published studies.Results: Published studies suggest that low academic achievement is more common than aca-demic underachievement (achievement below that expected on basis of IQ scores) and it isnot clear from published studies if rates of academic underachievement are significantly higherthan in the general population. Clear patterns with regard to the identification of correlates ofacademic underachievement have not emerged although low achievement may be influencedin many cases by lower than average levels of cognitive functioning. Most studies have not

focussed on the IQ-achievement discrepancy definitions of (specific) learning disability.Conclusion: Children with epilepsy who are experiencing academic difficulties may not qual-ify for formal educational supports to address these difficulties if eligibility criteria for such

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pilepsy can be conceptualised a broad-spectrum dis-ase that may include abnormalities in cognition,

∗ Corresponding author. Tel.: +44 1342 832243.E-mail address: creilly@ireland.com (C. Reilly).

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920-1211/$ — see front matter © 2011 Elsevier B.V. All rights reserved.oi:10.1016/j.eplepsyres.2011.07.017

nt discrepancy.served.

ehaviour/psychiatric status, and psychosocial func-ioning (Jensen, 2011). Children with epilepsy have beenong reported to have a high risk of significant school relatedifficulties (Pond and Bidwell, 1960; Rutter et al., 1970;

oldsworth and Whitmore, 1974). Rates of intellectualisability (ID) (IQ < 70) in children with epilepsy have rangedrom 17.9% to 30% (Berg et al., 2008; Ellenberg et al.,984; Murphy et al., 1995), and as there is a significant

Academic achievement in children with epilepsy 113

Table 1 Computer database search for academic achievement in children with epilepsy.

Terms PubMed PsycINFO ERIC

Epilepsy + achievement/underachievement 13 17 4Epilepsy + academic 18 19 4Epilepsy + school 102 51 14

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association between epilepsy and ID it is likely that someof the association with school and educational difficultiesrelate to this association (Sillanpää, 2004). As well as globalcognitive deficits, other potential contributory factors toschool related difficulties include specific cognitive deficits,behavioural difficulties, and academic delays.

As well as a reported excess of children with epilepsyreceiving special educational services (Berg et al., 2005) ithas been reported that children with epilepsy are at riskfor academic difficulties compared with unaffected typi-cally developing peers (Oostrom et al., 2003), others withchronic illnesses of childhood (Austin et al., 1998, 1999;Bailet and Turk, 2000), and siblings (Bailet and Turk, 2000).These academic difficulties has been shown to be presenteven in some children with epilepsy who are functioning ator near the average level of cognitive functioning (Oostromet al., 2003), and are often overlooked or overridden by thepressing medical problems associated with epilepsy (McNeliset al., 2005). Determining the relative contributions ofunderlying causes of academic difficulties has proved dif-ficult, and factors that lead to academic difficulties inchildren with epilepsy are not well understood (Seidenbergand Berent, 1992; Bourgeois, 1998), and are likely to differfrom child to child with causes of academic difficulties likelyto be the result of many variables (Williams, 2003; McNeliset al., 2005). General school related difficulties and aca-demic difficulties may have long-term detrimental effectson children with epilepsy and a follow-up study in Finlandindicated that children with epilepsy were less likely to havecontinued their education than controls even in the case ofthose with ‘uncomplicated epilepsy’ (Sillanpää et al., 1998).

Children with difficulties in academic achievement maypresent with ‘underachievement’ or ‘low achievement’across a range of academic subjects. Underachievementoccurs when a child’s performance in an academic subjectis significantly discrepant from that expected based on theirIQ score. Low achievement on the other hand is independentof IQ and is performance below the mean for that particularacademic area. This distinction between underachievementand low achievement may be important in that criteria foreligibility for educational supports may be based on a childunderachieving as opposed to displaying low achievement.An important concept in determining eligibility for educa-tional supports is that of (Specific) Learning Disability (US) orSpecific Learning Difficulty (UK). One of the most influentialdefinitions of Specific Learning Disability (SLD) was that pro-vided by the U.S. Office of Education in 1977 which requireda ‘‘severe discrepancy’’ between achievement and intellec-

tual ability in one or more areas of academic achievement.According to Kavale and Spaulding (2008) the discrepancydefinition of SLD was in the ascendancy until 1995 when itsuse for SLD identification was questioned. An alternative

riti

27 1

efinition of SLD is a low achievement definition whereby child is deemed to have an SLD if they perform at a levelignificantly below the school or national norms regardlessf their IQ score. This low-achievement approach negateshe need for IQ testing and involves the specification of cut-oints for low achievement provided the child is deemedot to be at risk for ID (Siegel, 1992; Stanovich and Siegel,994). However, given the known association between child-ood epilepsy and cognitive impairment IQ testing is likely toe particularly helpful in understanding the educational per-ormance of children with epilepsy. Fastenau et al. (2008)sed both IQ-achievement discrepancy and low achievementpproaches with regard to the definition and subsequentdentification of SLD in children with epilepsy, and foundhat more children reached the criteria for an SLD when lowchievement criteria were used.

For the purposes of this review academic ‘under-chievement’ is defined with respect to IQ whereas ‘lowchievement’ is defined with respect to norms on standard-sed achievement tests. The first objective of the review waso identify all studies published from 1990 to 2010 whichocussed on the prevalence of academic underachieve-ent/low achievement in children with epilepsy. The second

bjective of the study was to identify all studies publishedrom 1990 to 2010 which focussed on possible correlates ofcademic underachievement/low achievement.

ethodology

literature search was completed for all relevant stud-es published between January 1990 and December010. A computer search of databases of PsychINFO,ubMed and ERIC was conducted using the keywordsn ‘Title’: epilepsy + achievement/underachievement,pilepsy + academic, epilepsy + school, epilepsy + learningifficulty/disability. Table 1 displays the results of theatabase searches.

For the review of the prevalence of academic diffi-ulties, studies were included if they included measuresf school achievement, were focussed on children withpilepsy, were published in peer reviewed journals and pub-ished in the English language. Many of the articles had to bexcluded as they did not include data on prevalence ratesf academic underachievement/low achievement. Studiesere only included if they included school achievementata on 20 or more children with epilepsy. Studies which

eported on measurement of academic achievement viandividual assessment, group/whole class assessment andeacher reports of performance were included. Fifteen stud-es (see Table 2) met inclusion criteria.

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Table 2 Studies which have included prevalence rates of low academic achievement or underachievement of children with epilepsy (1990—2010).

Authors andyear

Samplesize

Type ofepilepsy/seizures

Inclusion/exclusioncriteria

(Meanage)Agerange

Criteria forunderachieve-ment

Domains ofachievement(standardisedtools)

Main findings in relation toprevalence of academicdifficulties

Tedrus et al.(2009)

38 CWE31 CONT

BECTS childrendivided in 2groups: BECTS-EP(classified ashaving educationalproblems)BECTS-N(classified as nothaving educationalproblems)

CWE had BECTSaccording to ILAE(2000) and thecriteria of DallaBernadina et al.(1985)

(9.29)8—11

2 Categoriesused: Superioror Average —best 75%,Inferior —lowest 25%

Reading,writing, andmathematics(Brazilian SPT)

— Reading — 51.6% ofBECTS-N and 100% of BECTS-EPhad inferior performancecompared with 24.3% of CONT— Writing — 48.4% of BECTS-Nand 85.7% of BECTS-EP hadinferior performance comparedwith 32.4% of CONT— Arithmetic — 35.5% ofBECTS-N and 53.1% of BECTS-EPhad inferior performancecompared with 32.4% of CONT

Fastenau et al.(2008)

164 CWE IDIO/CRY (69.9%)Familial (15.4%)SYM (14.7%)

CWE wereexcluded if theyhad a history oftraumatic braininjury, otherchronic physicalconditions, or ID

(11.8)8—15

3 were used —1 SD belowestimated IQ,1.0 SD and 1.5SD below meanforachievementtests

Reading,writing andmathematics(WJ-R)

— For IQ-achievement —reading (12.8%), math (20.1%),writing (37.8%)— For low achievement 1 SDbelow test mean — reading(32.2%), math (38.4%) andwriting (56.1%)— For low achievement 1.5 SDbelow test mean — reading(20.1%), math (26.8%) andwriting (34.8%)

Piccinelli et al.(2008)

20 CWE21 CONT

Rolandic Epilepsy CWE had ‘TypicalRolandic Epilepsy’according to ILAE(1989)

(10.25)7—12

2 SDs belowmean onstandardisedachievementtests

Reading,mathematics,and writing(included BDE)

— 45% of CWE had specificdifficulties in reading or writingcompared with 9.5% of CONT— 31.3% of CWE had specificdifficulties in Mathematicscompared with 5.9% of CONT

McNelis et al.(2007)

121 CWE GEN-TC (40)ABS (10)ELEPAR (10)CPS (29)PARSGEN (17)UNK (2)MUL (13)

CWE hadrecognised seizurein last 6 weeks,and had no otherchronic medicalcondition or ID

(9.50)4—14

Mean scores onschoolachievementtests and TRP

Reading andmathematics(TRF)

— At baseline CWE notexperiencing academicdifficulties

Academic

achievement

in children

with

epilepsy

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McNelis et al.(2005)

67 CWE No information onepilepsy type

CWE had no otherchronic medicalconditionsrequiringlong-term care,and did not haveID according toparental report

(11.26)8—15

1 SD Belownational meanon standardisedtests and 1 SDbelow mean onteacher ratings

Unspecifieddomains ofachievement(TRF)

— Most CWEperforming withinaverage range onachievement tests— 22.8% of CWE scored 1SD below mean onteacher ratings— 16.7% of CWE scored 1SD below on the nationalmean on a total batteryscore

Aldenkampet al. (2005)

167 CWE113CONT

IDIO-GEN (30),LOC-related (121),SYM-GEN (25)

CWE wasattending regu-lar/mainstreamschool

(9.6)6—12

12 monthsdifference ineducationalachievementbetween CWEand CONT

Reading andMathematics(HTL, HTR)

— Children withIDIO-GEN had similarperformance to controls— Children withLOC-related had a delayof about 14 months(compared with CONT)— Children with SYM-GENhad delays of about 26months (about 21/2school years)

Oostrom et al.(2003)

51 CWE48 CONT

BECTS (15)ABS (10)Other GEN (3)CRY with temporalfocus (5)CRY with Frontalfocus (8)CRY not specified(10)

CWE attendedmainstreamschool, hadepilepsy of IDIO orCRY cause, noother neurologicdisorder/chronicillness and noprevious use ofAEDs

(10.1)7—16

Comparisonwith mean ofmatchedcontrols

Measures ofreading,writing, andmathematics(test names notreported)

— CWE scored worseon measures of academicskills (meanperformance of CWE wasapproximately 0.4 SDbelow mean of controls)

116

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Table 2 (Continued)

Authors andyear

Samplesize

Type ofepilepsy/seizures

Inclusion/exclusioncriteria

(Meanage)Agerange

Criteria forunderachieve-ment

Domains ofachievement(standardisedtools)

Main findings in relation toprevalence of academicdifficulties

Williams et al.(2001)

65 CWE 44 CPS21 GEN

CWE who had ID, adiagnosed SLD,ADHD, or a historyof severe headinjury wereexcluded.CWE had to haveAED monotherapyand wellcontrolled seizures

(10.5)8—13

Comparisonswith meanscores onstandardisedmeasures ofacademicachievement

Reading,spelling, andmathematics(WJ-R)

— CWE performed withinaverage ranges on standardisedmeasures of academicachievement

Bailet and Turk(2000)

75 CWE23 CONT13 CWM

IDIO IQ ≥ 80Children with SYMor CRY epilepsy orabnormal CT orMRI were excluded

(9.6)8—13

Comparisonswith siblingcontrols andCWM

Reading,spelling andarithmetic(WRAT-R)

— CWE scored significantlylower than sibling controls andCWM on measures of academicachievement at time 1 (readingand spelling) and time 3(reading, spelling andarithmetic) but they also hadsignificantly lower IQ scores attime 1 and time 2

Schoenfeldet al. (1999)

57 CWE27 CONT

CPS CWE had no MRIabnormality, nocomorbidneurological ordevelopmentaldisorder or ID andBECTS excluded

(10.78)7—16

Comparisonswith siblingcontrols

Reading,spelling, andarithmetic(WRAT-3)

— CWE scored significantlylower in 3 domains ofachievement compared withCONT even when IQ used as acovariate

Austin et al.(1999)

98 CWE96 CWA

NR CWE had to havebeen takingmedication for atleast a year andhave been free ofany other chronicillnesses ordevelopmentaldisabilitiesincluding ID

(14.5)12—16

Comparisonswith norms onstandardisedachievementtests

Mathematicsand reading(schooladministeredachievementmeasures)

— CWE who were designatedas low-severity or inactive hadmean scores comparable tonational norms— CWE had lower mean scoresthan CWA in all achievementareas— CWE who were designated ashigh-severity had scores 3—5points below national normsbut national norms were gradeand not age based

Academic

achievement

in children

with

epilepsy

117

Aldenkampet al. (1999)

24 CWE24 CONT

LOC-related (9)IDIO-GEN (10)SYM-GEN (5)

CWE had to have a‘normal’ IQ

(8.9)NR

Comparisons withmean scores onschoolachievement index

Reading andmathematics (GSO)

— School achievement Indexfor CWE was 83.8 slightlybelow IQ but not significantlydifferent from Controls withlearning problems— CWE had slightly betterreading and spelling scores andsimilar Maths scores to controlswith learning problems

Williams et al.(1996)

84 CWE 4 groups ofCWE-controlledcomplex partial,controlled absence,uncontrolled complexpartial anduncontrolled absence

Exclusion criteriaincluded anydocumenteddiagnosis oflearningdisabilities, IDemotionaldisturbance, ADDor ODD

(10.1)5—16

Comparison withnational norms

Reading,mathematics andspelling (range ofschool administeredachievementmeasures)

— Achievement scoresindicated that mean readingscore was at 45th percentile,mean mathematics score was46th percentile and spellingwas at 49th percentile for CWEand thus within average range

Sturniolo andGalletti(1994)

41 CWE IDIO (22 with LOC and19 with GEN)

CWE attendedregular school anddid not havemajor neurologicaldeficits

(8.6)6—11

Children dividedinto three groupsbased on teachersjudgement ofSchoolachievement —good, adequateand poor

None — According to teacherjudgement 39% showed goodschool achievement, 32%showed adequate schoolachievement, and 29% showedpoor school achievement

Mitchell et al.(1991)

78 CWE Most children hadprimary generalisedepilepsies or epilepsyof undeterminedaetiology

CWE did not haveID, significantmotor or sensoryhandicaps

(8.6)4.8—12.9

1/2 SD below IQscore

Reading, readingcomprehensionspelling, andmathematics (PIAT)

— 38% of the groupunderachieving in readingcomprehension— 31% underachieving inmathematics— 32% underachieving inspelling

CWE, children with epilepsy; CONT, controls; BECTS, Benign Epilepsy with Centro-Temporal Spikes; IDIO, idiopathic; CRY, cryptogenic; SYM, symptomatic; GEN-TC, generalised tonic-clonic; ABS, absence; ELEPAR, elementary partial; CPS, complex partial; PARSGEN, partial with secondary generalisation; UNK, unknown; MUL, multiple; IDIO-GEN, idiopathic generalised;LOC, localization; SYM-GEN, symptomatic-generalised; NR, not reported; ID, intellectual disability; SD, standard deviation; TRF, teacher’s report form (Achenbach, 1991); WJ-R,Woodcock—Johnson psycho-educational test battery-revised (Woodcock and Johnson, 1989); CWM, children with migraine; CWA, children with asthma; wide range achievement test—revised (WRAT-R; Jastak and Wilkinson, 1984); wide range achievement test — 3rd ed. (WRAT-3; Jastak and Wilkinson, 1993); PIAT, peabody individual achievement test manual (Dunnand Markwardt, 1970); SPT, school performance test (Stein, 1994); BDE, battery for developmental dyscalculia (Biancardi and Nicoletti, 2004); HTL, Handleiding Tempotest Lezen (de Vos,1992); HTR, Handeleiding Tempotest Rekenen (de Vos, 1994); GSO, Groninger School Onderzoek (Kema and Kema-van Leggelo, 1987).

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For the review of studies on the correlates of academicifficulties studies had to a have a minimum of 20 childrenith epilepsy, be published in the English language, includet least one measure of possible correlates of achieve-ent difficulties, including epilepsy related factors (e.g.,

eizure type, epilepsy type/syndrome, use of AEDs, seizurerequency, seizure control, duration of epilepsy, age ofnset, and EEG findings), demographic factors (i.e., age ofhild, gender, socioeconomic status, caregiver education),hild/family factors (i.e., child behaviour, child compe-ency, child self-esteem, family mastery, and child attitude).n addition to the fifteen studies identified in the search fortudies on prevalence data four further studies were iden-ified as meeting inclusion criteria for this aspect of theeview.

esults

tudies of the prevalence of low academicchievement and academic underachievement inhildren with epilepsy

able 2 displays studies which have included prevalenceates of low academic achievement or underachievement inhildren with epilepsy. The prevalence rates of low achieve-ent and underachievement in epilepsy reported in Table 2

ave been based on studies of clinic based samples aspposed to population based samples, and thus it is notlear how representative the samples are in that many ofhe studies have used specific inclusionary/exclusionary cri-eria. All of the studies in Table 2 are cross sectional withhe exception of Bailet and Turk (2000) who reported testscores for children at three points in time. The rates of dif-culties in academic achievement experienced by childrenith epilepsy vary significantly in the 15 studies reported

n Table 2. There are a number of factors that are likelyo have contributed to this variation. Academic achieve-ent has been measured in different ways in the published

tudies with some studies reporting teacher reports of aca-emic performance, some reporting on school records ofcademic achievement, and some on individual assessmentsf children with epilepsy. The domains of achievement mea-ured have varied significantly across studies with mosttudies including measures of reading and mathematics butewer studies reporting on writing or reading comprehen-ion domains. Within domains of achievement, measures ofchievement have also varied significantly. For example,n mathematics some studies have focussed on arithmetichereas others focussed on written or computational math-matics. Studies have focussed on academic achievement atr close to the time of epilepsy onset whereas others havencluded children who have epilepsy over varying periods ofime.

One of the studies which suggested that children withpilepsy did not have significant academic difficulties (i.e.illiams et al., 2001) specifically excluded children with

LD and therefore excluded the children most likely to be

isplaying underachievement. With regard to other exclu-ionary criteria, having symptomatic epilepsy has been anxclusionary criteria in some studies (e.g., Bailet and Turk,000; Oostrom et al., 2003), and there is some evidence

e1Ms

C. Reilly, B.G.R. Neville

hat symptomatic aetiology is a risk factor for low achieve-ent although this low achievement may be accounted fory lower IQ scores reported in children with symptomaticetiology (e.g. Aldenkamp et al., 2005). A number of stud-es have included control children and in these studies theean achievement scores for the group of children with

pilepsy is lower than those of controls. However, whereontrols have been used, IQ scores have not always beeneported or in some but not all cases the group of chil-ren with epilepsy have had lower mean IQ scores suggestinghat in some of these studies, lower achievement scores areest categorised as low academic achievement as opposedo underachievement. All of the studies in Table 2 havesed the presence of intellectual disability (ID) (IQ < 70 ontandardised IQ tests) or a proxy (parental report of ID orttendance at a special school) as an exclusionary criteria.he criteria for low achievement or underachievement inhe published studies have varied significantly across stud-es. Most of the studies have used comparisons with thecores of controls or comparison with means on standard-sed achievement tests. Thus, with the exception of twotudies (Fastenau et al., 2008; Mitchell et al., 1991) an IQ-chievement discrepancy model has not been employed andherefore, estimating how many children might meet eligi-ility criteria for resources/supports under an SLD diagnosisased on the commonly used IQ-achievement discrepancy isot possible in the other studies.

tudies on the correlates of academic achievementn children with epilepsy

n order to examine possible correlates of low academicchievement and academic underachievement publishedtudies were examined with respect to reported corre-ates of academic achievement. Three broad categoriesf possible correlates were identified in published stud-es; epilepsy/seizure variables (i.e., seizure type, type ofpilepsy, AEDs, seizure frequency/severity, seizure con-rol, age of onset and EEG findings), demographic variablesi.e., child gender, child age, socioeconomic status, care-iver education) and child/family factors (i.e., childsychopathology, child self-esteem, child attitude familyastery, parental coping, parental anxiety). As well as these

hree categories reference is also made to possible neu-opsychological and school related correlates of academicchievement which have been less studied in comparison tohe other three categories.

eizure/epilepsy variableseizure type when measured has been found to be a signifi-ant correlate in only one published study (i.e., Fastenaut al., 2008), where it was reported that non-absenceeneralised seizures carried a significant risk for under-chievement in one domain of achievement (computationalaths) using an IQ-discrepancy model. Other studies have

ot found seizure type to be a significant risk factoror underachievement or low achievement (e.g., Fastenau

t al., 2004, 2009; Aldenkamp et al., 2005; Williams et al.,996; Sturniolo and Galletti, 1994; Mitchell et al., 1991).ost of the studies have not focussed on either epilepsy

yndrome or explicitly excluded certain syndromes. With

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Academic achievement in children with epilepsy

regard to type of epilepsy/epilepsy syndrome Fastenau et al.(2009) reported that children with generalised idiopathictonic-clonic and localization-related cryptogenic epilepsyscored significant lower than children with localization-related idiopathic epilepsy in the domain of writing in theirstudy of academic functioning at seizure onset in chil-dren. Aldenkamp et al. (2005) reported that children withlocalization-related (mostly cryptogenic) and symptomaticgeneralised epilepsy showed more difficulties in readingand mathematics compared with children with idiopathicepilepsy although the children with non-idiopathic epilepsyhad lower IQ scores than the idiopathic group. Most studiesthat have included AED use as a variable have not reportedan effect of AED use or type of AED on academic achieve-ment (e.g., Fastenau et al., 2008, 2009; McNelis et al., 2005;Williams et al., 2001; Mitchell et al., 1991).

Seizure frequency, seizure severity and seizure controlwhen measured, have been measured in varying ways instudies of academic achievement in children with epilepsyand thus comparisons across studies are difficult. Austinet al. (1998) reported that children with ‘high severity’, asopposed to ‘low severity’ epilepsy fared worse on a com-posite measure of academic achievement. However, otherstudies have not found this relationship with regard to fre-quency or severity (e.g. Mitchell et al., 1991). McNelis et al.(2005) reported that seizure severity was strongly associ-ated with teacher ratings of academic performance but notactual scores on achievement tests suggesting that teach-ers’ perceptions of academic performance were negativelyinfluenced by seizure severity. In terms of seizure controland achievement scores, significant findings with respectto academic performance have not been reported. Durationof epilepsy has not been found to a significant factor whenstudied (Jones et al., 2010; Fastenau et al., 2004; Williamset al., 2001; Sturniolo and Galletti, 1994; Mitchell et al.,1991). Piccinelli et al. (2008) reported that younger age ofonset (before age 8) of ‘typical rolandic epilepsy’ was pre-dictive of lower achievement compared with children whohad onset after age 8 but this relationship has not beenobserved in most studies of children with epilpesy (e.g.,Huberty et al., 1992; Sturniolo and Galletti, 1994). Fastenauet al. (2008) found that age of onset was not a risk factorfor underachievement in any domain but was a predictor oflow achievement in reading and mathematics. The relation-ship between EEG findings and achievement in children withepilepsy has been explored in a small number of studies.Fastenau et al. (2009) reported that the rate of epilepti-form activity was unrelated to academic achievement butwas related to slower processing speed in their study of chil-dren at seizure onset. Piccinelli et al. (2008) reported thatspecific learning difficulties were correlated with a markedincrease in epileptiform discharges during sleep. Aldenkampet al. (2005) and Sturniolo and Galletti (1994) did not findan association between rate of epileptiform activity on EEGand academic achievement.

Demographic variables

None of the published studies which have included genderas a possible correlate of academic achievement have founda significant gender effect on academic achievement in chil-dren with epilepsy with the exception of Austin et al. (1998,

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119

999). These two studies found that males with ‘high sever-ty’ epilepsy had significantly lower scores than females withinactive’ epilepsy for all of the assessed academic areas inhe 1999 study, and in all areas except mathematics in the998 study. Significant differences between males with ‘higheverity’ epilepsy and the two other groups of females (‘higheverity’ or ‘low severity ‘epilepsy) were not noted (Austint al., 1999). Child age was found to be a significant corre-ate by Fastenau et al. (2008) who reported that youngerhildren displayed higher rates of underachievement vian IQ-achievement discrepancy model, and suggested thatlder children may have a lower rate of underachievementue to having been identified as having difficulties (and thuseceived remediation) and/or were using compensatory cog-itive strategies. However, Mitchell et al. (1991) reportedhat older children were more likely to be underachievingn reading, reading comprehension and spelling. A signifi-ant relationship with age and achievement was not foundy Fastenau et al. (2004) or by McNelis et al. (2005). Socialackground (Sturniolo and Galletti, 1994) or socioeconomicackground (e.g., McNelis et al., 2005; Williams et al.,001) have not been found to be significantly associatedith academic achievement and levels of parental educa-

ion have not been correlated with academic achievementcores (Fastenau et al., 2004).

hild/family factorstudies of academic achievement in epilepsy have seldomncluded measures of general psychopathology or measuresf specific conditions and some studies have specificallyxcluded children with conditions such as ADHD (e.g.,illiams et al., 1996, 2001) despite the high risk of psy-

hopathology in children with epilepsy (e.g., Davies et al.,003). Fastenau et al. (2008) reported that the pres-nce of ADHD in children with epilepsy was a predictorf low achievement scores for reading, math and writ-ng but ADHD was not a predictor of underachievementsing an IQ-achievement discrepancy definition. Althoughturniolo and Galletti (1994) reported that the ‘behaviour’f children with epilepsy was not associated with poorercademic performance, ‘emotional maladjustment’ whichncluded social skill impairment and depressive symptomsas associated with poorer achievement. However, McNelist al. (2005) reported that scores on the Internalizingcale of the CBCL (Achenbach, 1991) were not relatedo academic achievement scores. Children with epilepsyave been noted to have lower-self esteem comparedith children with other chronic illnesses including dia-etes (Hoare and Mann, 1994), and lower self-esteem mayesult from the stigma associated with epilepsy (Oostromt al., 2000). Lower self-esteem has been associatedith difficulties with academic performance in childrenith epilepsy (Sturniolo and Galletti, 1994), but this

elationship was not found by McNelis et al. (2005) orastenau et al. (2004). Austin et al. (2008) reported thatower scores on the Child Attitude Towards Illness ScaleCATIS; Austin and Huberty, 1993) were associated with

ower achievement scores in all areas except reading sug-esting that child attitude towards epilepsy may be anmportant factor in school performance for affected chil-ren.

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Family factors and parent—child relationship have beendentified as potentially important predictors of child psy-hopathology (e.g. Rodenburg et al., 2006) and it is likelyhat they will also be important in terms of academicchievement. There has been an increasing emphasis onamily, home environment and parenting influences on aca-emic achievement although measures across studies havearied significantly. Mitchell et al. (1991) reported thatajor determinants of academic achievement were scores

n the Home observation for measurement of the environ-ent (HOME) Scale. The HOME scale assesses educationalaterials in the household and family participation inevelopmentally stimulating activities. Difficulties continu-ng their habitual parenting style were identified by Oostromt al. (2003) as a contributor to poorer academic scores.astenau et al. (2004) found that disorganised home environ-ents or unsupportive home environments were risk factors

or lower academic achievement particularly for writingchievement. However, McNelis et al. (2005) reported thathe mastery and health subscales of the Family Inventory ofesources for Management (FIRM; McCubbin and Thompson,987) were not correlated with academic achievement.arental mental health may contribute to difficulties forarents in supporting their children and Dunn et al. (2010)dentified high parental anxiety as a risk factor for academicifficulties.

europsychological and school related correlatesstablishing the presence of a deficit in a particular areaf cognition that is hypothesised to be related to aeficit in academic achievement (e.g., working memoryn reading) should be part of the process of determin-ng the presence of an SLD according to some definitionsf SLD (e.g., Flanagan et al., 2003). However, there haseen surprisingly little focus on particular neuropsycho-ogical deficits and their possible influence on academicchievement in children with epilpesy. Seidenberg et al.1988) reported that memory and attention skills wereeaker in children with epilepsy who displayed unsatis-

actory academic progress, while visual—spatial abilities,roblem-solving skills, nonverbal memory and motor skillsere not weaker. Deficits in attention were associatedith decreased scores in reading in a study by Williamst al. (2001). Using structured equation modelling Fastenaut al. (2004) identified a three factor model of neuropsy-hological function: Verbal/Memory/Executive (VME), Rapidaming/Working Memory (RN/WM), and psychomotor (PM).ith regard to academic achievement VME and RN/WM sig-

ificantly predicted reading, maths and writing; whereas PMignificantly predicted writing skills only.

School related factors are likely to have an impact on thehild’s academic performance but there has been very littleesearch focussed on the school environment or school basedactors with regard to understanding academic achievementn epilepsy (Bishop and Slevin, 2004). Studies focussing oneachers’ knowledge and attitudes towards epilepsy suggesthat most teachers do not feel that their current knowledge

s sufficient (Madsen, 1996; Pala and Vankar, 1997; Prpict al., 2003), and negative attitudes about epilepsy existmong a sufficiently large number of teachers to warrantoncern (Bishop and Slevin, 2004; Kankirawatana, 1999). It

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as been suggested that the presence of epilepsy may lowereacher expectations of the performance of children withpilepsy (Williams, 2003). With respect to school attendanceguiar et al. (2007) reported that 88% of children in theirtudy missed at least one school day due to having epilepsynd postulated that the impact of seizure frequency onchool attendance might play a role in academic difficulties.nother factor which may have an impact on school per-ormance is attitude towards epilepsy among peers. Austint al. (2002) reported that results of a survey of adolescentsn the US indicated that the social environment for adoles-ents with epilepsy is characterized by stigma and lack ofamiliarity and knowledge about epilepsy. However, as of yetchool factors have not been included as possible correlatesn studies of school achievement in children with epilepsy.

iscussion

he lack of population based studies makes it difficult touthoritatively comment on the true prevalence rate ofow achievement and underachievement in children withpilepsy. The studies of prevalence rates of academic dif-culties in children with epilepsy reported on in this reviewuggest that many children with epilepsy who do not haventellectual disability are performing within or close to theverage range, on both teacher ratings of school achieve-ent and on individual or group administered standardised

chool achievement tests. It is clear from nonpopulationased studies that some children with epilepsy without intel-ectual disability are achieving below peers and this lowchievement is evident across academic domains. A lowerercentage of children with epilepsy who have IQ’s outsidehe intellectually disabled range are underachieving withespect to IQ-achievement discrepancy (Fastenau et al.,008) and thus are performing below expected levels oferformance in academic areas. It is estimated that 5% ofhildren in the US are identified as having a specific learningisability (SLD) (Vaughn and Fuchs, 2003) and many of thesere identified via an IQ-achievement discrepancy model ofLD. Wodrich et al. (2006) reported that only 4 of 50 childrenith epilepsy (8%) were in receipt of special educational

ervices under the category of SLD so the number of chil-ren with epilepsy meeting criteria for SLD may be closeo the population average. However, children with epilepsyay be receiving formal special educational supports for

cademic difficulties under special educational needs cat-gorisations for behavioural and/or emotional disorders.opulation based studies indicate that children with epilepsyre at significantly higher risk than the normal pediatric pop-lation for behavioural/psychiatric disorders. There is anncreased risk for ADHD (e.g., Berg et al., 2011), depressionnd anxiety (e.g., Davies et al., 2003) and Autism Spectrumisorder (ASD) (e.g., Steffenburg et al., 1996). There is alson increased risk for motor disorders inclusing Cererbal Palsye.g., Steffenburg et al., 1995). The impact of these condi-ions on academic achievement has yet to be studied in aystematic way in the context of childhood epilepsy.

It has proved difficult to disentangle factors that con-ribute most to academic difficulties in children withpilepsy and correlates of academic difficulties have beeneasured in different ways in clinic based studies. In most

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studies epilepsy related factors have not been found tobe significant. With regard to low achievement there islikely to be a significant influence of level of cognition.In any given case of underachievement, causes may besimple/unique or more complex/combined and contribu-tory factors may include epilepsy factors, specific cognitivedeficits, demographic factors, child/family factors, andschool related factors. The impact of these factors will varyfrom child to child and some may have an independentpositive/negative effect and some may act in combination.Although under studied there does appear to some evidencethat child attitude to epilepsy, child self-esteem and psy-chopathology as well as family adaptation to epilepsy maybe important with respect to academic difficulties in chil-dren with epilepsy. The identification of risk factors mayremain elusive in some situations given the heterogonousnature of the manifestation of epilepsy and the multiplefactors that may contribute uniquely or in combination todifficulties.

Butterbaugh et al. (2004) caution against the use ofsimple screening measures of specific learning skills asthey do not provide adequate measures of functional lit-eracy skills. Future studies of academic achievement inchildren with epilepsy need to include standardised mea-sures of multiple aspects of reading (i.e., word recognition,phonemic awareness, and reading comprehension), math-ematics (e.g., computational mathematics, mathematicalreasoning, and arithmetic), spelling, writing (e.g. writingto dictation and creative writing), listening comprehension,and oral expression. Assessment of academic achievementin children with epilepsy will also be enhanced by theinvolvement of multiple informants (i.e., child, parent, andteacher report) and methods (i.e., individual, group testing)particularly when test results and observations/observerreports appear at odds. Once-off standardised assessmentmay be adversely influenced by factors such fatigue, depres-sion, anxiety, and attention problems which all occur moreoften in children with epilepsy. There is a need to sam-ple teacher attitudes regarding education specific issues inepilepsy as there is evidence that teacher expectations ofacademic performance are influenced by knowledge of achild’s epilepsy status (Katzenstein et al., 2007), leadingin some cases to an underestimation of the ability of chil-dren with epilepsy (Katzenstein et al., 2007). In terms ofselection of participants in future research, it will be ben-eficial if samples can be population based and can includeall children regardless of intellectual ability (provided chil-dren have some literacy numeracy and writing skills), andtype of epilepsy, as this has not been the case in previousstudies. Including measurements of possible neuropsycho-logical correlates of academic difficulties (e.g., difficultieswith attention, working memory, processing speed) mayhelp identify specific cognitive difficulties contributing toacademic difficulties and help with development of inter-vention strategies. Understanding possible correlates ofacademic underachievement and low achievement will alsobe facilitated by studies which focus on the stability ofdifficulties in academic achievement and how changes in

academic performance might be related to active epilepsyproducing continuous seizures or epilepsy in remission(i.e., child no longer experiencing seizures and/or longeron AEDs).

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In conclusion, the lack of population based data makest difficult to accurately estimate prevalence rates of lowcademic achievement and academic underachievement inhildren with epilepsy. The range of instruments used andhildren studied makes it difficult to present a compre-ensive picture of the educational problems of childrenith epilepsy including difficulties in the area of academicchievement or of their needs. Low achievement wouldppear to be much more common than underachievementased on IQ-achievement discrepancy models. Therefore,ost children with epilepsy and academic difficulties will

ot qualify for formal educational supports using SLD cri-eria unless low achievement definitions of specific learningisability are employed. The correlates of academic difficul-ies in children with epilepsy are likely to differ from child tohild but in cases of low achievement the role of subaverageognitive functioning is likely to be important. Possible neu-opsychological and school related correlates of academicifficulties remain understudied and the inclusion of suchariables in future studies may provide further insight tohe contributors to academic difficulties in children withpilepsy. As yet no population based intervention studiesave been reported which indicate the level of surveillancend support which might be required and its effects on sup-orting children with epilepsy.

onflicts of interest

he authors have no conflict of interest to disclose.

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