Archives of Disease in Childhood 1994; 71: 64-70

Impact of cyanotic heart disease on schoolperformance

M Wright, T Nolan

AbstractSurgical correction greatly decreasesthe mortality and cardiac morbidity ofcyanotic congenital heart disease, butchildren remain at risk of long termdifficulties in other areas. A historicalcohort study was conducted to determinethe relation between heart disease andschool performance in 29 children aged7 to 12 years old with simple transposi-tion of the great arteries or tetralogy ofFallot. All children had surgical correc-tion of their lesion before 2*5 years ofage. Those at greater risk of schooldifficulties because ofrecognised compli-cations of their heart disease or forreasons other than directly attributableto the heart disease were excluded.Comparison was made with 36 childrenwho had presented with cardiac mur-murs at a similar age, but who did notrequire treatment. Children with cyan-otic disease showed significantly poorerperformance in all academic areasassessed by the Wide Range AchievementTest-Revised; the difference in groupmean score (adjusted for differences inmaternal education, sex, and parentaloccupational prestige) for reading was103 points (confidence interval (CI) 1P25to 19-34), for spelling 7-8 (CI 111 to14.52), and for arithmetic 6-8 (CI 019 to13.39). The differences in adjusted groupmeans for the Wechsler IntelligenceScale for Children - Revised full scale,performance and verbal IQs were signifi-cant, particularly the later at 10*1 points(CI 2 59 to 17.61). Teacher reports indi-cated significant differences in arith-metic when outcome was dichotomised to'below grade' or 'not below grade'. Therewere no significant associations betweenoutcome measures and the medicalor perioperative parameters, however,including those related to hypoxia. It isconcluded that the increased incidenceof academic problems and the natureof the cognitive difficulties in childrenwith uncomplicated corrective cardiacsurgery for cyanotic heart disease arenot fully explained by chronic hypoxia, orby other factors related to the cardiacsurgery.(Arch Dis Child 1994; 71: 64-70)

Cyanotic congenital heart disease has a birthprevalence of approximately 2/1000.1 Theprimary structural lesions are varied; tetralogyof Fallot and transposition of the great

arteries are the most common, accountingfor about 80% or more of cases. Continuingimprovements in operative and medicalmanagement have seen cumulative survivalrates increase dramatically in the last 30years.2 Because these children are beingoperated on at an earlier age with the expecta-tion of a 'normal' duration and quality oflife, it is particularly important to determineadverse outcomes which supervene despiteearly normalisation of their cardiopulmonarystate.An important, but often unrecognised

concomitant of childhood illness is poor schoolperformance,34 a risk that is greatest whenthe central nervous system has beeninvolved.5 There is evidence to suggest thatchildren with cyanotic heart disease are atparticular risk because of factors specific totheir illness - chronic hypoxia, anaesthetic,and surgery conditions.612 Most studies, how-ever, have focused on IQ, failing to examinefunctional measures of long term outcome(such as school performance), or have simplyassumed hypoxia to be the major contributingfactor6 8-1113-16 when the actual effects ofchronic (compared with acute) hypoxia on thedeveloping human nervous system are not wellknown. Neuropsychological and behaviouralfindings suggested as evidence for the effects ofchronic hypoxia have had to be drawn mainlyfrom the study of children with acute perinatalhypoxia and adults with chronic obstructiveairways disease.10 17 Such data suggest thatvigilance and attention are decreased, and theprocessing of information inhibited. As aresult, some subscales of IQ tests such as theWechsler Intelligence Scale for Children -

Revised (WISC-R), such as arithmetic, digitspan, and coding, would be affected more thanothers, as would neuropsychological testsfocusing on processing and behaviouralmeasures that are particularly influenced bydecreased attention.The aim of this study was to assess school

performance, using a comprehensive set ofvalidated measures with information frommultiple sources, in children who hadhad a corrective operation for cyanotic heartdisease and who were not otherwise expectedto be at significantly greater risk of havingschool difficulties. It was hypothesised that(a) children with cyanotic heart diseasewould have significantly worse academicperformance than controls, (b) there wouldbe strong associations with the durationand severity of preoperative hypoxia andperioperative factors, and (c) the nature ofcognitive deficits and behavioural problemswould be related to hypoxia.

Department ofPaediatrics, UniversityofMelbourneM Wright

Clinical Epidemiologyand Biostatistics Unit,Department ofPaediatrics, UniversityofMelbourneT Nolan

Correspondence to:Dr Martin Wright,University of Melbourne,Department of Paediatrics,Royal Children's Hospital,Parkville, Victoria, Australia3052.

Accepted 17 March 1994

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MethodsCASESThis study was approved by the RoyalChildren's Hospital human ethics committee.Cardiac surgery records at the RoyalChildren's Hospital, Melbourne (the onlypaediatric cardiac surgery facility in the state ofVictoria, which has a population of 4A4 million)were used to obtain the names and clinicaldetails of all children who had had a correctiveoperation for tetralogy of Fallot or transposi-tion of the great arteries between February1979 and February 1984. Comparable surgicaland anaesthetic support was provided through-out this time, with all the transposition ofthe great arteries children having Senningprocedures.

Other eligibility criteria were (a) only smallto moderate sized ventricular septal defects inassociation with tetralogy of Fallot and apatent ductus arteriosus and/or no tosmall ventricular septal defect in those withtransposition of the great arteries, (b) ageless than 2-5 years at the time of the correctiveoperation (and therefore between 6 and12 years of age when studied, in at leasttheir second year of school), (c) residence inVictoria at the time of the study, (d) gestationgreater than 33 weeks and birth weightgreater than 2000 g, (e) no significantperinatal problems such as birth asphyxiaor seizures, (f) no non-cardiac clinicalmalformations, (g) no evidence of postnatalneurological impairment including cerebro-vascular accident or other complications of theheart condition or its treatment, (h) normalcardiopulmonary function (postoperativeoxygen saturation greater than 92% andable to participate in daily activities withoutsymptoms or requiring drugs active on thecardiovascular system), and (i) at least oneparent and child English speaking.

CONTROLSComputerised outpatient lists were used toobtain the names and details of childrenseen in cardiology outpatients at the RoyalChildren's Hospital between February 1979and 1984, in whom the diagnosis was of eitheran innocent murmur or a small ventricularseptal defect subsequently closing spontane-ously and not requiring treatment. The sameeligibility criteria were used. The controlsample base will have differed from that of thecases as children with minor cardiac lesionsand coming from higher socioeconomic statusfamilies would have been more likely to be seenin private rooms than referred to the cardiologypatients.

It was hoped that, by using children withfunctional murmurs or insignificant cardiaclesions, control for some of the psychologicaleffects of diagnosis of a cardiac disorder in ayoung child would be possible, while allowingconsideration of medical and surgical para-meters that had been hypothesised as associa-tions with adverse outcomes. The controlsused were therefore not 'normal' in terms ofearly environmental factors.

ENROLMENTContact was attempted with potential casesand controls by letter and then by telephone ifthere was no reply within two weeks. TheDepartment of Social Security was used topass on letters to families that could not becontacted, and who were on their records asreceiving a government allowance. For thoseagreeing to participate, informed consent wasobtained, questionnaires mailed to parents andteachers, and the child seen for one three hoursession at the Royal Children's Hospital.

MEASURESParents provided information includingparental age, education, and occupation, andwhether they felt their child had been affectedby his or her heart condition academically,physically, socially, or behaviourally. They alsolisted childhood illnesses and developmentalmilestones, which were verified where possibleusing the hospital records. Parents completedthe child behaviour checklist (CBCL), whichwas used to obtain behavioural ratings,'8 andthe teachers completed the teacher's reportform (TRF).'9

Teachers indicated whether the child hadbeen referred for extra assistance at schoolor repeated a grade, and gave a subjectiveassessment of their current level of academicperformance compared with the others inthe grade (on a five point Likert scale). Thechildren were seen by a psychologist, blindedto their case status, who administered theWide Range Achievement Test - Revised(WRAT-R) as a measure of academic achieve-ment,20 and the full WISC-R (both standard-ised with mean 100 and SD 15 points).2' Theywere also seen by a paediatrician (not blindedto their case status, but using a standardisedscore sheet) who examined for neurologicalabnormalities22 and residual cardiovascularsigns. He also administered the self perceptionprofile for children (a measure of a number ofdomains of self perception completed by thechild),23 the Corsi block span (a test of shortterm visual memory in which there is no con-tamination by the use of verbal memory, as thelayout of the cubes inhibits numbering andsubvocalisation by the child),24 the Rey audi-tory verbal (RAV) learning test (through therecall of a wordlist repeatedly read out, assess-ing short term auditory memory andprocessing skills in a manner more specificto the learning environment than a digitspan),25 26 the Rey figure visual (RFV) learningtest (a test of perceptual organisation andvisual memory in which the child is firstlyasked to copy a drawing of a complexshape, and then later draw the shape frommemory),25 27 and selected subtests from theBruininks-Oseretsky test of motor proficiency,examining fine and gross motor abilities andvisuomotor performance.28 After the session,parents were sent a written report of thefindings which summarised their child'sperformance, indicating areas of concern.Follow up was offered through the departmentofpsychology at the Royal Children's Hospital.

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Table 1 Baseline characteristics

Cases Controls(n=29) (n=36)

Age at assessment (months)Mean (SD) 114 (14) 113 (14)Range 84-137 89-135

No (%/o) boys 20 (69) 20 (56)Gestation (weeks)Mean (SD) 39-3 (1-6) 39-6 (2.4)Range 36-43 33-43

Birth weight (g)Mean (SD) 3245 (640) 3341 (600)Range 2270-4470 2041-4950

Mean (SD) occupational prestige* 4-5 (1-2) 5 (1 1)Maternal education (percentage less than 11 years) 55 50Maternal age at assessment (years)Mean (SD) 37 (3-7) 35 (4-8)Range 26-43 26-48

Marital status (No (%) single parent) 2 (7) 6 (16)

*Lower score equals greater prestige.

ANALYSISAnalysis was performed using the SAS statisti-cal package.29 Basic comparative analyses usedthe x2 test (or Fisher's exact test), and a t testfor independent samples for outcomesexpressed as proportions and continuousscores respectively. Standardised effect sizeswere calculated for continuous outcomesto further aid comparison of the two groups.Risk ratios (RR) and 95% confidence intervals,with the control group as the denominator,were calculated for proportions where appro-priate. Where continuous scores such asthe CBCL did not conform to a normaldistribution, adjusted means were comparedusing non-parametric bivariate analysis withthe Wilcoxon two sample test. Linear multipleregression was used to determine potentialconfounders and adjustment was made forgender, socioeconomic status (operationalisedas parental occupational prestige),30 andmaternal education using analysis of covari-ance (ANCOVA). ANCOVA was also used toadjust for differences in age distribution whenthe test results were not standardised (forexample, digit span and self perception).Bivariate correlations and their 95% confi-dence intervals (CIs) were determined withmajor outcomes as the dependent variablesand medical and surgical parameters as theindependent variables.

ResultsIn total, 42 children fulfilled the entryrequirements from the information available intheir cardiac surgery and hospital records.Of these, 40 could be contacted. Parents ofseven children refused consent and a further

Table 2 Results from the WRA T-R. Values are mean (SD) values

Cases Controls 95% CIfor difference(n=29) (n=36) p Value in adjusted means

ReadingCrude 82-9 (18-49) 93-6 (18-45)Adjusted* 83-9 (17-77) 94-2 (18-50) 0-026 1-25 to 19-34

SpellingCrude 81-0 (12-27) 89-5 (14-64)Adjusted 82-3 (13-17) 90 1 (13-72) 0-023 1-11 to 14-52

ArithmeticCrude 88-1 (13-38) 95 5 (11-82)Adjusted 88-6 (12-96) 95-4 (13-49) 0-044 019 to 13-39

*Adjusted for group differences in socioeconomic status, gender and matemal education.Note: WRAT-R norms are standardised to mean= 100, SD= 15.

four were excluded when information aboutdisorders not managed at the Royal Children'sHospital was available from the parentalquestionnaires. One had a history of three focalseizures not temporally related to the cardiacoperation, one had required bilateral legcallipers for the first three years of life due tobilateral upper motor neuron damage, onehad pneumococcal meningitis a number ofyears after the operation, and the other haddeveloped a right hemiplegia after the cardiacoperation. Therefore 29/38 (76%) wereincluded. Those who refused or were unable tobe contacted may not all have fulfilled entrycriteria, but were of similar age when the studywas performed and at the corrective operation.Of this group, six (66%) had tetralogy ofFallot and eight (89%) were boys, v 12 (41%)and 20 (69%) in the final study group. Thesedifferences were not statistically significant(p=0- 15 and 0-24 respectively).

Contact was made with 45 of 80 controls, ofwhom 41 consented to the study. Five of thesewere excluded when further information fromthe parents indicated insufficient English(four) or that the child had a persistentsymptomatic cardiac defect requiring ongoingtreatment (one). Table 1 gives the baselinecharacteristics of the two groups. The greaternumber of boys in the case group was partlyrelated to the greater incidence of transpositionof the great arteries in boys (approximately 2'3to 1, boys to girls). The mean (SD) haemo-globin concentration and oxygen saturationrecorded before and closest to the time of thecorrective operation were 162 (31 0) g/l and 84(9 4)% respectively. The cases were between4 and 120 weeks old when operated on (mean45*7 weeks), 20 of them having had earlierpalliative surgery. The mean (SD) durationof cardiac bypass and cardiac arrest were61 (16-7) and 39 (7 5) minutes respectively.

ACADEMIC OUTCOMEWhen adjusted for differences in maternaleducation, socioeconomic status, and sex, thecases performed significantly worse than thecontrols in all three of the subscales of theWRAT-R (table 2). WRAT-R reading,spelling, and arithmetic group mean scoreswere on the 13th, 12th, and 21st centilesfor the cases and on the 34th, 25th, and37th centiles for the controls. Approximatestandardised effect sizes were moderatelylarge, between 0 5 and 0-6. When furtheradjustment was made for differences in fullscale IQ, these differences were lessenedand became statistically non-significant. Theteacher ratings of school performance werestratified into 'below grade level' or 'at orabove grade level' and the two groups com-pared. There was a significant difference inarithmetic (p=0 03), but not reading orspelling. Eight (28%) of the cases and onlyfour (11%) of the controls had been referredfor extra assistance at school (p=0 114; RR2-48; CI 0-81 to 7 58). Two of the cases andone control were reported to have repeated agrade. Ten of the 29 teachers of the cases

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Table 3 Bivariate correlations between medical and peioperative parameters, and IQand WRAT-R reading performance

Dependent variable Independent variable r Value 95% CIfor r

WISC-R full scale IQ Age at operation -0 07 -0-42 to 0-31Duration of cardiac bypass -0-26 -0-58 to 0- 11Duration of cardiac arrest* -0-36 -0-68 to 0 07Temperature for operation -0-10 -0-45 to 0-28Duration of rewarming 0-28 -0-10 to 0-58Oxygen tensiont 0 05 -0-48 to 0 54Oxygen saturationt 0-26 -0-17 to 0-61pH§ 0 05 -0 45 to 0 53Haemoglobin -0-02 -0-69 to 0 35

WRAT-R reading Age at operation -0-01 -0 55 to 0-36Duration of cardiac bypass -0-16 -0-37 to 0-22Duration of cardiac arrest* -0-41 -0 70 to 0-02Temperature for operation -0-10 -0 45 to 0-27Duration of rewarming 0-02 -0 35 to 0-68Oxygen tensiont 0-22 -0 33 to 0-66Oxygen saturationt 0-16 -0-27 to 0 54pH§ 0 05 -0-46 to 0 53Haemoglobin -0-17 -0-51 to 0-21

*n=22 as seven cases with tetralogy of Fallot not operated under cardiac arrest.tn= 15 because of missing data.#n=23 because of missing data.Sn= 16 because of missing data.

indicated that they knew the child had acardiac disorder. Though these childrentended to have lower WRAT-R reading scoresthan the 19 other cases, the differences werenot statistically significant (p=007).

ASSOCIATION OF CURRENT FUNCTIONING WITHMEDICAL AND SURGICAL PARAMETERSSimple linear regression was used withWISC-R full scale IQ and the three WRAT-Rsubscales separately as outcome measuresto examine correlations with individual medicaland surgical parameters. There was no statisti-cally significant association with any of themedical or surgical parameters. Duration ofcardiac arrest, however, approached signifi-cance and the correlation with WRAT-Rreading was moderate (table 3).

Table 4 WISC-R scores. Values are crude means (SD) above, with adjusted means(SD) below

Cases Controls 95% CIfor difference(n=29) (n=36) p Value in adjusted means

Information 10-1 (3 80) 10-8 (2.26)9-7 (3 02) 10-8 (2-91) 0-15 -0-41 to 2-55

Similarities 7-3 (4 60) 10-2 (3-00)6-9 (3 77) 10-3 (3 66) 0.001 1-57 to 5-27

Arithmetic 91 (3-10) 10-2 (2 80)8-9 (3 02) 10-2 (2-91) 0-08 -0-16 to 2-81

Vocabulary 8-7 (3 60) 10-2 (2 30)8-5 (2-91) 10-3 (2 88) 0-02 0-32 to 3-19

Comprehension 8-6 (2 80) 9-6 (2 40)8-6 (2-53) 9-7 (2 46) 0 09 -0-17 to 2-31

Digit span* 8-1 (2 80) 8-7 (2 70)8-2 (3 77) 8-7 (2 76) 0 55 -1-18 to 2-18

Picture completion 9-4 (2 50) 10-0 (2 80)9-3 (2 85) 10-0 (2 76) 0-34 -0-73 to 2-06

Picture arrangement 9-8 (3 30) 9-9 (2 70)9-9 (3-18) 10-0 (3 06) 0-89 -1-47 to 1-68

Block design 11 1 (3.70) 12-6 (3.40)10-7 (3 57) 12-5 (3 44) 0 04 0-09 to 3-60

Object assembly 10-8 (3 90) 12-4 (3 30)10-5 (3-72) 12-4 (3 60) 0 04 0-06 to 3-73

Coding 8-5 (2 60) 10-2 (3 40)8-4 (3 23) 10-0 (3-12) 0 04 0 05 to 3-20

Verbal scale IQ 92-2 (19-60) 100-6 (12-10)90-8 (15-29) 100-9 (14-76) 0-009 2-59 to 17-61

Performance scale IQ 99-4 (17-20) 106-9 (14-40)98-2 (16-59) 106-5 (16-02) 0 05 0-11 to 16-41

Full scale IQ 95-2 (18-90) 103-8 (12-10)93-8 (15-67) 103-8 (15-12) 0-01 2-32 to 17-72

*Data available for only 16 of the cases for digit span.Note: WISC-R norms are standardised to mean= 100, SD= 15.Values adjusted for differences between the two groups in gender, maternal education, andoccupational prestige.

COGNrTIVE OUTCOMEThere were statistically and clinically signifi-cant differences between the group means infull scale IQ, performance IQ, verbal IQ, andin similarities, vocabulary, block design, objectassembly, and coding subscales (table 4). Inall, the difference in adjusted means wasgreater than half a standardised standarddeviation, and the full scale IQ differencerepresents a moderate to large effect size oftwothirds. Using a paired t test for both cases andcontrols, verbal scores were significantly lowerthan performance scores (p=0007, CI 2-2 to12-3 for the cases; and p=0-02, CI 10 to 115for the controls).

SHORT TERM MEMORYANCOVA was used to adjust for differencesin distribution of age as well as socioeconomicstatus, sex, and maternal education. Using themaximum number of digits retained forwardfrom the digit span subtest of the WISC-R,there was no significant difference in shortterm auditory memory (p=0-80; CI -033 to0A47). ANCOVA was also performed using thenumber of blocks retained in the Corsi blockspan test. There was no significant difference(p=068; CI -035 to 053).

BEHAVIOUR/ADJUSTMENTThere was a significant difference between thetwo groups in the maladjustment rate recordedby the parents (p=0-015; CI for the differencein percentages 5°/O to 49%) and the parents ofthe cases were more likely to believe that thecardiac disorder had affected their child behav-iourally (p=0035), but not in the other areas(table 5). The maladjustment rate for the caseswas significantly higher than the NorthAmerican test norms (p<0001). Althoughthere was no significant difference in any of themajor and narrow band scales other thanhyperactive (p=003), the cases scored higherin all but one narrow band scale. There was nodifference between cases and controls inteacher reported incidence of maladjustment,both were similar to the North Americannorms, and there was no significant differencein the narrow or broad band scales of the TRF.

SELF PERCEPTIONUsing ANCOVA for each of the six subscalesin the Harter, there was no significantdifference between cases and controls. Whenthe cases were grouped into those performinggreater than 1 SD below the WRAT-R readingmean, and those doing better, the formergroup rated themselves significantly lower forscholastic perception only (p=004; CI for dif-ferences in adjusted means 04 to 9-55).

MOTOR AND NEUROLOGICAL EXAMINATIONAll the controls had a normal peripheralneurological examination. Five cases ( 17%)had mildly and symmetrically increasedreflexes, without abnormalities of tone or

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Table S CBCL and TRF major scales and maladjustment rates. Values are crude means(SD) above and adjusted means (SD) belowfor the CBCL

95% ConfidenceScale* Cases Controls p Valuet interval (CI)

CBCLSummaryT 58-9 (10-8) 54-9 (10 1)

59-2 (11-8) 55-8 (10-7) 0-11 -2-2 to 9 0Intemalising 58-6 (10-4) 54-7 (10-9)

59-5 (11-6) 54-5 (10-8) 0-08 -0-6 to 10-6Extemalising 58-3 (10-2) 54-2 (9 5)

58-5 (11 1) 54-2 (10 1) 0 10 -10 to 9-6Maladjustment ratet 41 14

TRFSummary T 49-7 (9 6) 52-1 (8 5) 0 30 -2-1 to 6-9Intemalising 51-9 (8 7) 54-1 (8 3) 0 30 -2-0 to 6-4Externalising 50-8 (8 2) 52-2 (7 9) 0-49 -2-6 to 5-4Maladjustment ratet 14 14

*n=29 for cases and 35 for controls.tThe p value quoted was obtained from a two tailed t test on the adjusted means.tPercentage of children with a summary behaviour problem t-score greater than one standarddeviation above the mean. Rate for normative sample is 10%.For the CBCL, RR (risk ratio cases relative to controls)=2-9. 95% CI for RR=0-62 to 4-06. x2with 1 DF=5-97 for the difference between cases and controls (p=0-015; CI for the differencein percentages 5 to 49%).Note: CBCL and TRF norms are standardised to mean=50, SD= 10.

plantar reflexes. This difference was significant(p=0-014; CI for difference in percentages 3 to31%). Cases performed worse on the balancesubscale of the Bruininks-Oseretsky test ofmotor proficiency (mean (SD) adjusted score9 0 (6 6) for cases and 12-9 (6 4) for controls;p=0-02; CI for difference in adjusted means055 to 7d17), used as a measure of gross motorperformance, but not on the visual motor orfine motor measures.To aid the consideration of whether the

only reason for between group differences inacademic and cognitive outcomes was thegreater incidence of neurological impairmentin the cases, and as the control group hadworse motor performance than the standardis-ation sample, WISC-R IQ and WRAT-Rscores were stratified according to the balancescore (greater than or equal to 2 SDs below thetest mean or above this value).Those with poor motor performance had an

equally poor outcome whether from the case orcontrol group (table 6). For those with highermotor scores (in all the categories having a bet-ter outcome than those from the same groupwith lower motor scores), the controls per-formed significantly better than the cases onthe WRAT-R scales and the WISC-R perfor-mance scale, with effect sizes between 0 5 and075. On the other WISC-R scales, though the

Table 6 Comparison of the WISC-R and the WRAT-R scores stratified by gross motorperformance on the balance subtest of the Bruininks-Oseretsky test of motor proficiency.Values are mean (SD)

Cases ControlsMotor pstatus* No No Value 95% CIt

WISC-R total A 10 88-4 (16-95) 6 89-7 (8-21) 0-84 -14-7 to 17-3B 18 99-1 (19-81) 28 107-6 (10-52) 0-11 -0-5 to 17-4

WISC-Rverbal A 10 87-7 (18-98) 6 91-0 (10-20) 0-66 -14-9 to 21-5B 18 95-2 (20 47) 28 103-5 (11-30) 0-13 -1-1 to 17-7

WISC-R performance A 10 91-3 (13-42) 6 90 3 (10-25) 0-87 -12-7 to 14-7B 18 86-1 (18 12) 28 97-2 (16-67) 0-043 -2-2to 16-4

WRAT-Rreading A 10 77-7 (19-67) 6 79-5 (19-71) 0-86 -20-2to23-8B 18 86-1 (18-18) 28 97-3 (16-67) 0-043 0-7to21-7

WRAT-R spelling A 10 79-0 (14-64) 6 78-2 (11-25) 09 -14-3 to 15-9B 18 82-2(11-42) 28 92-6(13-60) 0-008 2-8to 18-3

WRAT-Rarithmetic A 10 87-1 (16-69) 6 82-5(12-32) 054 -12-4to21-6B 18 88-4 (12-02) 28 97 9 (9-93) 0009 30 to 16-0

*A=Greater than or equal to 2 SDs below the gross motor test mean; B=less than 2 SDs belowthe mean.t95% CI for the difference in means.Note: test mean scores are 100, SD 15.

differences were not statistically significant,effect sizes were between 0-5 and 0-55.

REY LEARNING TESTSThere was no significant difference betweenthe two groups in the RAV when the scores forthe first five recalls were added (p=0-15; CI-1-27 to 7-87), or in the RFV recall test(p=0 16; CI - 1 -04 to 6-33). Differences in theRFV copy test were significant (p=0-002; CI0-17 to 8 55).

DiscussionChildren who had had successful surgicalcorrection of uncomplicated transposition ofthe great arteries or tetralogy of Fallot at anearly age, and who did not have evidence ofmajor nervous system trauma as a result of thecardiac lesion or its treatment, performedsignificantly worse in a standardised test ofacademic achievement than a control group ofchildren. The children with cardiac disorderswere also more likely to have been referred forextra school assistance, though this differencewas not statistically significant. Althoughmajor differences in IQ were present, andadjustment of academic performance forsuch variance decreased the above academicdifferences to being not statistically significant,this may have been a reflection of the lack ofstatistical power of the study. Furthermore,because the control group performed belowthe level of the normative sample on theWRAT-R, academic performance differencescould well have been greater if the controlgroup had been taken from the general popula-tion, as they probably would have if childrenhaving a corrective operation for more severeforms of cyanotic heart disease had beeneligible.

Other important findings were the lack of astatistically significant strong associationbetween cognitive or academic outcomes andmedical or perioperative parameters, as wellas the lack of processing difficulties andattentional problems in the cognitive and behav-ioural profiles. The latter would have beensuggestive ofhypoxia being a major determinantof poor performance. The cases were not ratedas being less attentive by their teachers on theTRF, and the TRF maladjustment rate was thesame for cases and controls, yet there weresignificant differences between the currentperceptions of the parents of children withcyanotic heart disease, the teachers of thesechildren, and the parents of the controlchildren. The CBCL maladjustment rates forcases and controls differed significantly, and theparents of cases were more likely to believe thatthe cardiac disorder had affected their child'sbehaviour. The maladjustment rate for caseswas also significantly greater than for thenormative sample.

Overall, these findings are consistent withenvironmental factors other than those con-trolled for by maternal occupation and parentaloccupational prestige (such as parent-childinteraction) contributing to the differences in

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outcome - academic, cognitive, and behav-ioural.3' The differences between the twogroups in neurological outcomes - gross motorperformance and peripheral neurologicalexamination - may suggest a neurological basisfor the group differences in academic andcognitive performance. Although asymmetricaland mild increases in reflexes without otherperipheral neurological findings is a commonphenomenon in this age group,32 childrenwith poor motor performance, regardless ofgroup, performed worse academically and hada poorer cognitive function. Nevertheless,children with cyanotic heart disease performedworse than the controls when motor perfor-mance was within the normal range. Thissuggests that, whether or not due to hypoxia,birth trauma or other insult, poor motor perfor-mance in either group is similarly associatedwith poor cognitive and academic outcomes.When motor performance was within thenormal range (and the likelihood ofneurologicaldamage was lower), the cases performedsignificantly worse than the controls.

This study addresses many of the method-ological shortcomings of studies reportedpreviously. These include small study samplesizes,12 33 34 failure to exclude children athigher risk of cognitive difficulties and schooldysfunction (because of obvious neurologicalinsult, perinatal risk factors, congenital malfor-mations),8 10 33 35 36 the use of semistructuredinterviews or case descriptions rather thanvalidated measures, especially when consider-ing emotional and behavioural responses,6 37 38limited consideration of environmental andsocial factors (which may have as great orgreater impact on cognitive development andacademic performance),12 3940 the the use ofchildren with only one type of cardiaclesion, limiting generalisability to the majorityof children with cyanotic heart disease.7 9 12Some studies have drawn conclusions from theexamination of very young children, limitingtheir ability to make firm inferences aboutfuture functioning,4' 42 or have not usedcontrol groups.4' 43 Others have studied sub-jects with greatly variable ages, necessitatingthe use of different tests of cognitive andother functions, which may not be directlycomparable.35 41 44The inability to separately explain the effects

of decreased physical activity, parent-childinteractions, and other early environmentalfactors is a limitation of our study, thoughstudying a group on average younger at thetime of the corrective operation lessens theimpact of such factors compared with otherstudies.8 35 Because such specific informationis not recorded routinely, a prospective studywould be required using relevant validatedmeasures. Furthermore, the ability of this andother studies to determine whether hypoxia is asignificant contributor to adverse outcomesis constrained by the lack of availability ofsuitable biochemical and haematologicalmeasures which integrate fluctuations overtime." The failure to demonstrate significantassociations with these parameters may havebeen due to their imprecision as markers for

long term hypoxia. On the other hand, thoughmultiple sampling of oxygen saturation mayhave enabled a better overall estimate ofchronic hypoxia, it too has not been validatedfor this purpose.

Control group performance on the subscalesof the WRAT-R was 03 to 0-65 SDs belowthat of the normative mean,20 and motorperformance was also poorer than expected.The use of this control group may thereforehave resulted in a substantial underestimationof the true effect of cyanotic heart disease.Using children who had cardiac surgery foracyanotic heart disease as a third control groupmay have allowed the effects of cardiacsurgery to be separated from those of hypoxia,though differences in surgical and anaestheticconditions would still need to be considered.

Since the early to mid 1 980s the operation ofchoice for children with transposition of thearteries has been the arterial switch procedureperformed within the first few days of life,unless there is a more complicated cardiacdefect. This results in cardiac anatomy andfunction much closer to normal. Mortality andmorbidity (short term at least) haveimproved,45 and the potential adverse effectsof chronic hypoxia or physical restrictionhave been limited. The conclusions based onour study may therefore not apply to manychildren with transposition born morerecently. They do apply, however, to the largenumber of children with surgically amelioratedtransposition who are now in their middleschool years and beyond. Two follow upstudies have reported on the developmental,cognitive, and neurological outcome ofpreschool children who have undergonearterial switch procedures. Unfortunately,these studies have also not adequately consid-ered non-medical or other surgical factors.46 47Although there have been changes in themanagement of children with tetralogy, theyhave not been nearly as great, with anoperation still performed at a much later agethan for transposition.

ConclusionDespite continuing improvements in surgicaland medical management, children withcyanotic heart disease are at great risk ofhaving difficulties at school. This includesthose children without specific cardiac or non-cardiac factors which are likely to predisposeto a poorer outcome. Greater attention needsto be directed towards the factors influencingthe long term quality of life, such as thosethat affect school performance. To do this,there must be continuing assessment of non-cardiac outcome which takes account ofchanges in surgical management. This studysuggests that hypoxia may not be the mostimportant determinant of the increased schooldifficulties that these children experience.Further research needs to be directed towardsdeveloping a measure of chronic hypoxia andthe determination of its effects on cognitivedevelopment. Research is also needed tomore accurately describe the environmental

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influences on children with cyanotic heartdisease.

For the practising paediatrician, there needsto be recognition that children undergoingmajor medical intervention in the first yearsof life can have important developmentalproblems even when the operation is success-ful. Vigilant monitoring of cardiac patients'academic and behavioural development, withthe anticipation that counselling and tutoringmay be needed, is required. In addition,these results emphasise the importance ofcounselling parents to recognise the specialneeds of their child and the importance of'normalising' their child's existence to thegreatest possible extent. Prescribed disabilitymay be as deleterious as the consequences ofthe cardiac disease itself.

We gratefully acknowledge the assistance of Dr F Oberklaid inconceiving and initiating the study, Mr R Mee in obtaining thecardiac surgery data and providing invaluable surgical informa-tion, the staff of the clinical epidemiology and biostatistics unitin the analysis, and Dr V Anderson for neuropsychologicaladvice.

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