Specific Language Difficulties and School Achievement in Children Born at 25 weeks of gestation or less

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    Specific Language Difficulties and School Achievement in Children Bornat 25 Weeks of Gestation or Less

    DIETERWOLKE, PHD, MUTHANNA SAMARA, MSC, MELANIE BRACEWELL, MD, AND NEIL MARLOW, MD,FOR THE EPICURE STUDY GROUP*

    Objective To determine whether language and educational problems are specific or due to general cognitive deficits in

    children born at 25 weeks gestation or less.

    Study design A national cohort study assessed 241 of 308 (78%) surviving children at a median age of 6 years, 4 months

    along with 160 of these childrens classmates. Formal tests included standard cognitive, language, phonetic, and speech

    assessments. The childrens school achievement was rated by classroom teachers.

    Results Mean cognitive scores for index children were 82 (standard deviation [SD] 19) compared with 106 (SD 12) forthe peer group. Extremely preterm children had an increased risk of language problems (odds ratio [OR] 10; 95% confidence

    interval [CI] 3 to 32), speech problems (OR 4.4; 95% CI 3 to 7), and overall school difficulties (OR 25; 95% CI 12 to 54). Extremely preterm boys were twice as likely to show deficits as extremely preterm girls, but no such sex-based

    differences were apparent in the comparison group. Differences in general cognitive scores explained specific language or

    phonetic awareness deficits, but not speech ratings or educational difficulties, in the extremely preterm children.

    Conclusions Language or phonetic difficulties are not specific and indicate general cognitive functional difficulties. The

    findings have implications for models of global deviation of brain development in extremely preterm children.

    (J Pediatr 2008;152:256-62)

    Ahigher prevalence of cognitive impairments and poorer educational achievement has been repeatedly observed inchildren born preterm or with low birth weight compared with children born at full term.1 Other developmentaldisorders, such as language delays and deficits,2 articulation problems,3 and learning disorders (eg, poor reading, writing,

    and numerical and mathematic skills4,5) also are more common in very low birth weight (VLBW) children. Such language orlearning disorders may be associated withgeneral cognitive impairment, or they can be specific and independent of cognitivefunction or environmental disadvantage.2 Specific developmental language impairments or specific learning disorders arediagnosed when there is a clear discrepancy between general intellectual development as measured by, for example, performanceIQ and language or learning achievement scores.6,7

    Long-term adverse cognitive, language, and psychosocial outcomes have beenreported in children with normal IQ but with specific language impairment. 8 Specificdeficits may suggest either damage to or inhibition of normal development in specific areasof the brain.9 Few previous studies have evaluated whether these developmental orlearning problems truly represent specific developmental disorders or can be accounted forby general cognitive deficits in VLBW children.10

    A recent longitudinal analysis of VLBW children suggests that learning difficultiesare not specific, but rather are more likely due to global deficits in cognitive function and

    may require different interventions than those developed for full-term children.4 How-ever, the children included in these cohorts were born before the widespread introductionof antenatal corticosteroid and surfactant replacement therapy, which are importantdeterminants of the increased survival of extremely preterm infants11 that can be expectedto enhance long-term outcome and also possibly alter patterns of disability. These cohorts

    CI Confidence intervalK-ABC Kaufman Assessment Battery for ChildrenMPC Mental Processing CompositeOR Odds ratio

    PAT Phonological Abilities TestPLS-3 Preschool Language Scale-3SD Standard deviationVLBW Very low birth weight

    From the Department of Psychology and

    Warwick Medical School, Health Sciences

    Research Institute, University of Warwick,

    Coventry, UK (D.W., M.S.) and the Insti-

    tute of Neuroscience, Univers ity of Not-

    tingham, Nottingham, UK (M.B., N.M.).Submitted for publication Mar 30, 2007;

    last revision received Jun 18, 2007; ac-

    cepted Jun 28, 2007.

    Reprint requests:DieterWolke, PhD,Univer-

    sity of Warwick, Department of Psychology

    and Health Sciences Research Institute, War-

    wick Medical School, Coventry CV4 7AL, UK.

    E-mail:[email protected].

    *A list of EPICURE Study Group members

    is available at www.jpeds.com.

    0022-3476/$ - see front matter

    Copyright 2008 Mosby Inc. All rights

    reserved.

    10.1016/j.jpeds.2007.06.043

    256

    http://mail%20to:[email protected]/http://mail%20to:[email protected]/http://mail%20to:[email protected]/http://www.jpeds.com/http://www.jpeds.com/http://mail%20to:[email protected]/http://www.jpeds.com/
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    included very few extremely preterm children, whose survivalhas increased over the past 15 years and whose high risks ofdisability and general cognitive problems have been describedpreviously.12

    In this report, we describe the results of language, speech,phonetic, and educational difficulties during the early school ageperiod in a geographically based sample of children born before26 weeks gestation, of whom 60% were exposed to antenatalsteroid treatment and 84% received surfactant.13We investigatethe extent to which the language and learning difficulties ob-served in this population are specific impairments or are in line

    with general cognitive abilities.

    METHODS

    Subjects

    The derivation and characteristics of this study populationhave been described previously,13,14 as have the details of the6-year evaluation.12The population represents all surviving chil-dren born at 25 weeks, 6 days gestational age or less betweenMarch and December 1995. Of the 308 children known to bealive at age 30 months, the parents of 241 consented to the study.

    A total of 204 children were in mainstream education. For eachchild assessed in a mainstream school, we sought an age- andsex-matched classmate as a comparison.12Thus, we were able toassess 160 full-term born children, who form the comparisonpopulation. All children were assessed by a pediatrician and apsychologist trained in the techniques used for the study (see

    Appendix; available at www.jpeds.com). All appointmentswere made by the study administrator, and the assessors wereblinded to the childrens group status. All parents gave writteninformed consent, and the study was approved by the TrentMulticentre Research Ethics Committee and the local edu-

    cation authorities in Scotland.

    Assessment

    General cognitive ability was assessed using the Kauf-man Assessment Battery for Children (K-ABC),12,15 com-posed of 2 summative scales: the Mental Processing Com-posite (MPC), comprising Sequential and SimultaneousProcessing subscales, which provides a global measure of thechilds cognitive ability, and the Achievement Scale, an as-sessment of knowledge of facts, language concepts, andschool-related skills. Receptive and expressive language abil-

    ities were evaluated using the Preschool Language Scale-3(UK) (PLS-3), which comprises Auditory Comprehensionand Expressive Communication scales.16 Articulation diffi-culties were assessed according to 19 speech sounds in theinitial or final positions of consonant-vowel-consonant words,

    which the child is asked to imitate in the PLS assessment. Weused the Phonological Abilities Test (PAT)17 to assess skillspredictive of reading acquisition.18 The PAT comprises 4subtests: rhyme detection, phoneme deletion (both beginningand end sounds), and a test of letter knowledge.17 Quality ofspeech was rated by the psychologists using publishedscales;19 phonological disorder (315.39) and stuttering (307)

    were diagnosed according to criteria specified in the Diagnos-tic and Statistical Manual of Mental Disorders, 4th edition(DSM-IV).7

    Cognitive impairment or disability precluded the use ofthe K-ABC in 41 index children.12 These children wereevaluated using either the Griffiths Scales of Mental Devel-opment20 (in 35 children) or the NEPSY Neuropsychology

    Assessment21 (in 6 children). The Griffiths quotient or meanNEPSY standardized score was used to estimate a score. Ifthis score was40 (the lowest score on the K-ABC), then thechild was assigned a score of 39. To give a measure ofcognitive function for all of the index children, these values

    were merged with the MPC to give an overall cognitive score.No other substitutions for untestable children were made forthe K-ABC subscales or in reporting other test results.

    Teachers rated the scholastic performance of the indexand comparison children against the national expected level ofattainment for a child of the same age in English, mathemat-ics, science, technology, geography, history, and informationtechnology. These ratings were combined to yield a totalacademic achievement score.22

    Eight experienced developmental psychologists wererecruited to perform the assessments described above. Allattended a course in which they were trained in all aspects ofthe study evaluation. After the training course, every secondchilds session was videotaped and for random quality checkby the senior assessment psychologist.

    Statistical Analysis

    Categorical outcomes were compared using the 2 testfor trends, as appropriate, or Fishers exact test. Continuousoutcomes were compared using an independent Student ttest.

    All statistical tests were 2-sided. Differences in results be-tween the extremely preterm and comparison children andbetween boys and girls (and their interactions) were evaluatedusing a generalized linear model if scales were normally dis-tributed. A priori dichotomized outcomes were determinedusing a cutoff of 2 standard deviations (SDs) or the 10th/90thpercentiles as appropriate. The comparison scores served ascomparison norms for all tests. Testing for the presence ofspecific learning disabilities was done using multiple regres-sion, with the overall cognitive score (MPC) as a covariate.

    All analyses were then repeated after excluding children withsevere physical disability (eg, blindness, hearing loss requiringaids, cerebral palsy).

    RESULTS

    Cognitive Scores

    The mean scores for all children and boys and girlsseparately have been reported in detail previously.12The meanMPC score was 105.7 (SD 1.8) for the comparison chil-dren and 82.1 (SD 19.2) for the extremely preterm chil-dren, a difference of 23.6 points (95% confidence interval[CI] 20.3 to 26.8). In the comparison group, boys and girlshad similar scores. In contrast, index boys (mean, 77.1

    Specific Language Difficulties and School Achievement in Children Born at 25 Weeks of Gestation or Less 257

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    19.6) scored lower than index girls (mean, 87.2 17.4); thedifference in means was 10.1 points (95% CI 5.4 to 14.8),and the sex by group interaction was significant (P .01).

    These effects remained after exclusion of children with severephysical disability (mean scores: 81.9 15.2) and 90.6 13.5, respectively; difference of means, 8.7 points; 95% CI 5.1 to 12.3; sex by group interaction, P .01) or when onlythe children tested using the K-ABC were considered (4.6points; 95% CI 1.1 to 8.1).

    Compared with the control children (contemporarynorms, 1.3%; n 2), 98 (40.6%) extremely preterm childrenhad a general cognitive ability score (MPC) 2 SD, indi-cating moderate to severe cognitive impairment (P .001).12

    Compared with extremely preterm girls (32%; n 38), ex-tremely preterm boys (49%; n 60) were twice as likely tohave serious impairment in overall cognitive scores (OR2.1; 95% CI 1.2 to 3.5; P .01).

    Language Abilities

    Findings similar to those presented above were observed

    when language tests were considered. The extremely pretermchildren exhibited poorer performance in all of the PLS-3composite scores and total score than the comparison children(Table I). The extremely preterm children were more likely tohave serious language impairment, as evaluated by the totalPLS-3 score and auditory comprehension, expressive commu-nication, and articulation subtests (Table I); boys had higherrates of impairment than girls (total PLS, P .01; auditorycomprehension, P .01; expressive communication, P .05;articulation, P .01). No sex differences were found in thecomparison group. Although the interaction between groupand sex was not significant in the PLS-3 using continuous

    scores, extremely premature boys were more likely to havemoderately or severely impaired scores than extremely prema-ture girls (total PLS-3: OR 2.3, 95% CI 1 to 5.1, P.05; auditory comprehension: OR 2.1, 95% CI 0.8 to5.5, P .107; expressive communication: OR 5.1, 95%CI 1.8 to 14.3, P .01; articulation: OR 3.2, 95%CI 1.1 to 9.3, P .05).

    Using the comparison group as a reference popula-tion, children who scored below the 10th percentile in thePAT or above the 90th percentile for the speech andlanguage ratings were considered to be in the clinical, orabnormal, range. The extremely preterm children weremore likely to have difficulties on all subscales of the PATand were more often rated in the clinical range in speechproduction and grammatical correctness in language by theassessors (Table II). Significant sex differences in the pho-neme deletion beginning sounds (P .01) and in gram-matical correctness ratings (P .01) were found, with anexcess of boys in the clinical range.

    Compared with their peer group, the extremely pre-term children were rated as using less developmentallyappropriate speech sounds for age and dialect (17.6% vs6.3%; OR 3.2; 95% CI 1.5 to 6.6; P .01) and hadmore difficulties in speech sound production, defined asinterfering with academic achievement or with social com-munication (14.6% vs 3.1%; OR 5.3; 95% CI 2 to13.9; P .001). These factors compose the DSM-IVclassification phonological disorder (315.39).7 Similarly,the extremely preterm children had more disturbances inthe normal fluency and time patterning of speech(DSM-IV stuttering [307] (5% vs 0.6%; OR 8.3; 95%CI 1.1 to 66.7; P .05).

    Table I. Language abilities in the PLS-3 assessed at 6 years for 241 children born at 25 weeks of gestation

    or less and 160 age matched classmates for comparison

    Comparison group Extremely preterm group

    OR (95% CI) for

    serious impairmentn Mean (SD)

    Serious

    impairment

    (

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    Academic Achievement

    The Total Academic Achievement Score classifies chil-dren scoring below average in contrast to average or aboveaverage performance.22A score was assigned to 169 extremelypreterm children and 150 comparison children by mainstreamclass teachers. Missing data are due to teachers not returningcomplete ratings. Of the extremely preterm children in main-stream schools, 50.3% were rated below average, compared

    with 5.3% of their peers (OR 17.9; 95% CI 8.3 to 38.9;P .001). The actual risk would have been higher hadchildren enrolled in special schools (who perform well below

    what would be expected for age) been included (OR 25;95% CI 12 to 54). Extremely preterm boys in mainstreamschools were more likely to have below-average ratings than

    extremely preterm girls in mainstream schools (OR 2.4;95% CI 1.3 to 4.4; P .01).

    Specific Language or General Academic Impairment

    We explored the possibility of specific language impair-ment using multiple regression to adjust PLS-3 scores, clin-ical ratings for PAT/language scales, and teacher assessmentsfor the general cognitive score (MPC). Cognitive impairmentexplained the differences between extremely preterm childrenand comparison children in PLS-3 total score and the 3subscale scores independent of whether all children (Table

    III) or only those without severe disability (not shown) wereanalyzed. For example, although the observed mean differ-

    ence in the comparison childrens unadjusted PLS-3 totalscore was 14.3 points (95% CI 10.6 to 18.0), after adjust-ment, this fell to 1.8 points (95% CI 6.6 to 3). Categor-ical comparisons produced similar results. Cognitive impair-ment also accounted for the differences in impairment inphonetic awareness and language ratings (Table IV), but notfor the differences in speech ratings and academic achieve-ment (P .01 and .001 after adjustment, respectively).Speech impairments were still 2.6 times more frequent in theextremely preterm children (95% CI 1.5 to 4.6) afteradjustment for general cognitive ability. Similarly, educationalproblems could not be attributed solely to general cognitive

    deficits but remained 4.9 times more frequent (95% CI 2 to11.5) after general cognitive score adjustment (Table IV).

    DISCUSSION

    In this entire population cohort of extremely pretermchildren in the UK and Ireland, we found considerable dif-ferences in general cognitive ability (IQ), language, phoneticawareness, articulation, and scholastic achievement compared

    with their classmates of the same age. These differences weremore pronounced in this population than those observed inother studies of more mature very preterm or VLBW popu-

    Table II. Scores in the clinical range or language abilities on the PAT and speech and language ratings

    assessed at 6 years for 241 children born at 25 weeks of gestation or less and 160 age-matched classmates

    for comparison

    Comparison group Extremely preterm group

    OR (95% CI)

    Number/number

    with information Percent

    Number/number

    with information Percent

    PAT

    Rhyme detection 22/160 13.8* 66/203 32.5* 3.1 (1.8 to 5.2)*Boys 11/71 15.5 37/96 38.5

    Girls 11/89 12.4 29/107 27.1

    Phoneme deletion beginning sounds 33/160 20.6* 104/203 51.2* 4.1 (2.5 to 6.5)*

    Boys 16/71 22.5* 57/96 59.4*

    Girls 17/89 19.1* 47/107 43.9*

    Phoneme deletion end sounds 45/160 28.1* 115/203 56.7* 3.3 (2.1 to 5.2)*

    Boys 25/71 35.2 57/96 59.4

    Girls 20/89 22.5* 58/107 54.2*

    Letter knowledge 32/160 20* 76/202 37.6* 2.4 (1.5 to 3.9)*

    Boys 19/71 26.8 36/96 37.5

    Girls 13/89 14.6* 40/106 37.7*

    Speech rating 32/158 20.3* 106/200 53* 4.4 (2.8 to 7.1)*

    Boys 14/71 19.7* 48/92 52.2*

    Girls 18/87 20.7* 58/108 53.7*

    Grammatical correctness rating 23/158 14.6* 66/200 33* 2.9 (1.7 to 4.9)*

    Boys 10/71 14.1* 37/92 40.2*

    Girls 13/87 14.9 29/108 26.9

    Values shown are the proportions scoring over the 90th percentile for the comparison group (PAT) or under the 10th percentile for the comparison group (speech and grammar ratings).ORs are calculated by logistic regression with sex as a covariate.*P .001.P .01.P .05 for differences between extremely preterm and comparison groups.

    Specific Language Difficulties and School Achievement in Children Born at 25 Weeks of Gestation or Less 259

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    lations, in whom disadvantages have been described over awide range of cognitive functions, including informationprocessing, language, phonetic awareness, and educationalachievement.1,19,23,24

    In school and everyday settings, children are comparednot with children born in the 1970s, but rather with theirclassmates. Therefore, for all statistical comparisons, includ-ing the classification of impairment, as a reference we used thescores of the comparison group rather than the often outdatedhistorical test norms, which are subject to significant seculartrends in adults and children25 and result in underestimation

    of impairment.12,26 Using this comparison, we found that40.6% of extremely preterm children had general cognitivedeficits, and that these children were 56 times more likely tosuffer moderate to severe cognitive deficits compared withmainstream classmates born at full term.

    This finding of substantial general cognitive deficits andlanguage, phonetic, and speech impairments cannot be attrib-uted to selective dropout of high achievers. Previously re-ported analysis indicated no differences regarding medical

    variables, growth, or early disability between those lost to

    follow-up and those assessed.12

    Rather, dropout was morelikely in disadvantaged families, which would be expected toreduce cognitive and language achievement,19,27 and thus wemay have underestimated the language deficit in our popula-tion.

    When controlling for general cognitive performance, nospecific language difficulties or phonetic deficits were ob-served, a finding reported in previous studies of more matureVLBW and extremely preterm children.19,24 Thus, there islittle evidence that language or phonetic processing problemsin extremely preterm children are due to specific deficitspreviously speculated to be a result of damage to or inhibition

    of normal development in specific areas of the brain.

    9

    Rather,these and previous analyses in 2 other samples19,24 suggestthat language abilities are substantially explained by generalcognitive deficits in extremely or very preterm children. Thisfinding may have its equivalence in brain development, in thatgeneral cognitive impairments in extremely preterm childrenmay have their origin in global changes in brain developmentin terms of size and complexity28-30 and generally are not theresult of damage to specific brain regions. These findings addto our understanding of the neuropathologic pathways asso-ciated with later language function in extremely preterm chil-dren.

    Table III. Mean performance and frequency of serious impairment in the EPICure cohort and comparison

    group for language abilities on the PLS-3 before and after adjustment for general cognitive scores (MPC)

    PLS-3

    Unadjusted mean

    (95% CI)

    Adjusted mean

    (95% CI)

    Unadjusted OR for

    serious impairment

    (95% CI)

    Adjusted OR for

    serious impairment

    (95% CI)

    Total score

    Extremely preterm 89.6 (86.8 to 92.4) 96.7 (94.3 to 99.2) 9.6 (2.9 to 32.2)* 1.3 (0.3 to 5.3)

    Comparison 103.9 (101.6 to 106.2)* 98.5 (95.4 to 101.5)

    Auditory comprehension

    Extremely preterm 88.7 (86.4 to 91.1) 94.1 (91.9 to 96.3) 8.3 (1.9 to 35.7) 1.6 (0.3 to 9.8)

    Comparison 101.3 (99.1 to 103.5)* 96.5 (93.7 to 99.3)

    Expressive communication

    Extremely preterm 92.6 (89.6 to 95.5) 100 (97.4 to 102.6) 10.7 (2.5 to 45.5)* 1.2 (0.2 to 6.5)

    Comparison 105.4 (103.1 to 107.8)* 100.5 (97.2 to 103.8)

    Articulation screener

    Extremely preterm 32.7 (31.7 to 33.8) 34.3 (33.3 to 35.3) 3.9 (1.2 to 11.6) 1.1 (0.3 to 4)

    Comparison 34.9 (34.2 to 35.6) 34.5 (33.2 to 35.8)

    *P .001.P .05 for differences between the extremely preterm and comparison groups.P .01.

    Table IV. ORs for clinical scores in language

    abilities and below-average academic performance

    on the Total Academic Achievement Score for the

    EPICure cohort, before and after adjustment for

    general cognitive scores (MPC)

    Unadjusted OR for

    clinical score

    (95% CI)

    Adjusted OR for

    clinical score

    (95% CI)

    PAT rhyme detection 3 (1.8 to 5.2)* 1.6 (0.8 to 3.2)

    PAT phoneme

    deletion beginning

    sound

    4 (2.5 to 6.5)* 1.2 (0.7 to 2.1)

    PAT phoneme

    deletion end sound

    3.3 (2.1 to 5.2)* 1.1 (0.7 to 2)

    PAT letter knowledge 2.4 (1.5 to 3.9)* 1.3 (0.7 to 2.4)

    Speech ratings 4.3 (2.7 to 6.8)* 2.6 (1.5 to 4.6)

    Language ratings 2.9 (1.7 to 5)* 1.2 (0.6 to 2.3)

    Teachers academic

    achievement scale

    24.9 (11.6 to 53.6)* 4.9 (2 to 11.5)

    *P .001.P .01 for differences between the extremely preterm and comparison groups.

    260 Wolke et al The Journal of Pediatrics February 2008

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    In contrast, speech problems and a global rating ofeducational difficulties could not be explained solely by lowerIQ, a finding replicating the results reported for VLBWchildren in Germany.19 Speech difficulties often involve oralmotor problems31 and may be significantly affected by spe-cific motor problems and controlled by specific brain areas.Oral motor problems, such as in eating difficulties, have longbeen suspected to be associated with later speech problems32

    and warrant further exploration. Furthermore, our findingsregarding educational problems are consistent with those re-ported by Taylor et al,24 who found specific mathematicalachievement deficits in children with birth weight 750 g.

    Wolke and Meyer19 found that numerical abilities were notsolely accounted for by IQ in a German VLBW sample. Arecent longitudinal study comparing extremely and very pre-term children and full-term control children showed thatgeneral cognitive impairment had a strong initial impact onspecific abilities (phonetic accuracy, letter and number knowl-edge) that are prerequisites for learning reading, writing, andmathematical skills. However, attained reading, writing, and

    mathematical abilities are the mediating link to longer-termeducational success in both full-term and preterm children.4

    Furthermore, other factors, such as working memory,33 at-tention deficit and peer relationship problems,1,34 motorproblems,35 and family socioeconomic factors,4,24 also con-tribute to educational problems in extremely premature chil-dren and need to be further explored in longitudinal analysis.

    This is relevant, because motor or behavioral managementprograms may be able to increase educational performance inextremely preterm children.

    A range of adverse perinatal outcomes has been describedin males, ranging from death,36 perinatal brain injury,37 cerebralpalsy, and delayed lung maturation38 to preterm birth andstillbirth. Significant sex differences in cognitive functioninghave been reported in some cohorts38 but not in others.19Wefound a substantial and clinically relevant increase in cogni-tive, language, and educational difficulties in extremely pre-term boys compared with extremely preterm girls. This is inthe context of the lower survival and greater frequency ofneonatal problems13 and higher rates of disability14 in malesin this population. It may be speculated that sex differences inintrauterine development may make the male fetus/extremelypreterm infant particularly vulnerable to perinatal adversityand may have important consequences for later develop-ment.39The gestational age at which male vulnerability is nolonger demonstrable remains to be determined, but it wouldseem to be particularly evident at very low gestational age.

    The present study has some limitations. We requiredthe cooperation of the childrens teachers to obtain parentalconsent to communicate the contact details of the controlchildren to the investigators. Lack of teacher cooperation orof parental consent was the major reason why we did not havea class control for all target children. We found no pattern orlack of cooperation according to regional variation or socialdeprivation in the area that the school was serving; thus, weconsider any bias to be minimal. All assessors were unaware of

    the childrens group status and family background; however,total blinding throughout the assessment may not have beenachieved in all cases, considering that the extremely pretermchildren were on average smaller, more often required correc-tion for sight, and more often had a motor disability. Thismay have provided clues to the assessors regarding groupmembership.

    In conclusion, our findings demonstrate that adversecognitive, language, phonetic, and educational sequelae aremore frequent in extremely premature children than in moremature preterm populations and that the cognitive impair-ment is general rather than specific. Cognitive impairmentsexplain only part of the educational difficulties experienced bythese children, and future analysis needs to take into accountother areas of function, including behavioral, motor, andsocial difficulties. Our findings of patterns of functional dif-ficulties may have important implications for brain imagingresearch.40 Extremely preterm birth and very early extrauter-ine development may alter the pattern of brain developmentacross a range of brain regions, including all areas of the cortexand deeper brain structures,28 and may be responsible for theglobal deficits in neuropsychological function seen in this

    vulnerable population.

    REFERENCES1. Saigal S, denOuden L, Wolke D, Hoult L, Paneth N, Streiner DL, et al.School-age outcomes in children who were extremely low birth weight from four

    international population-based cohorts. Pediatrics 2003;112:943-50.2. Wolke D. Language problems in neonatal at risk children: towards an understand-ing of developmental mechanisms. Acta Paediatr 1999;88:488-90.3. Largo RH, Molinari L, Kundu S, Duc G. Intellectual outcome, speech and schoolperformance in high-risk preterm children with birth weight appropriate for gestationalage. Eur J Pediatr 1990;149:845-50.4. Schneider W, Wolke D, Schlagmller M, Meyer R. Pathways to school achieve-ment in very preterm and full-term children. Eur J Psychol Educ 2004;19:385-406.5. Taylor HG, Minich N, Klein N, Hack M. Longitudinal outcomes of very lowbirth weight: neuropsychological findings. J Int Neuropsychol Soc 2004;10:149-63.6. Dyck MJ, Hay D, Anderson M, Smith LM, Piek J, Hallmayer J. Is the discrepancy

    criterion for defining developmental disorders valid? J Child Psychol Psychiatry 2004;45:979-95.7. Diagnostic and Statistical Manual of Mental Disorders. 4th edition. Washington,DC: American Psychiatric Association; 1994.8. Clegg J, Hollis C, Mawhood L, Rutter M. Developmental language disorders: a

    follow-up in later adult life. Cognitive, language and psychosocial outcomes. J ChildPsychol Psychiatry 2005;46:128-49.9. Mutch L, Leyland A, McGee A. Patterns of neuropsychological function in a low

    birth weight population. Dev Med Child Neurol 1993;35:943-56.10. Saigal S, Szatmarl P, Rosenbaum P, Campbell D, King S. Cognitive abilities and

    school performance of extremely low birth weight children and matched term controlchildren at age 8 years: a regional study. J Pediatr 1991;118:751-60.11. Fanaroff AA, Hack M, Walsh MC. The NICHD neonatal research network:

    changes in practice and outcomes during the first 15 years. Semin Perinatol 2003;

    27:281-7.12. Marlow N, Wolke D, Bracewell MA, Samara M. Neurologic and developmental

    disability at 6 years of age after extremely preterm birth. N Engl J Med 2005;352:9-19.13. Costeloe K, Hennessy E, Gibson AT, Marlow N, Wilkinson AR. The EPIcure

    Study: outcomes to discharge from hospital for infants born at the threshold of viability.Pediatrics 2000;106:659-71.14. Wood NS, Marlow N, Costeloe K, Gibson AT, Wilkinson AR, Group ES.

    Neurologic and developmental disability after extremely preterm birth. N Engl J Med2000;343:378-84.15. Kaufman A, Kaufman N. Kaufman Assessment Battery for Children. Circle Pines,MN: American Guidance Service, 1983.16. Zimmermann IL, Steiner VG, Pond RE. Preschool Language Scale-3. San

    Antonio, TX: Harcourt Brace Jovanovich; 1992.17. Muter V, Hulme C, Snowling M. Phonological Abilities Test (PAT). London:Psychological Testing Corp; 1997.

    Specific Language Difficulties and School Achievement in Children Born at 25 Weeks of Gestation or Less 261

  • 7/27/2019 Specific Language Difficulties and School Achievement in Children Born at 25 weeks of gestation or less

    7/8

    18. Bryant P, Nunes T, Bindman M. Awareness of language in children who havereading difficulties: historical comparisons in a longitudinal study. J Child Psychol

    Psychiatry 1998;39:501-10.19. Wolke D, Meyer R. Cognitive status, language attainment and prereading skills of6-year-old very preterm children and their peers: the Bavarian Longitudinal Study. Dev

    Med Child Neurol 1999;41:94-109.20. Griffiths R. Abilities of Young Children: A Comprehensive System of Mental

    Measurement for the First 8 Years of Life. Somerset, UK: Young and Son; 1970.21. Korkman M, Kirk U, Kemp S. Manual for the NEPSY: A DevelopmentalNeuropsychological Assessment. San Antonio, TX: Harcourt Brace Jovanovich;

    1998.22. Wolke D, Rizzo P, Woods S. Persistent infant crying and hyperactivity problems

    in middle childhood. Pediatrics 2002;109:1054-60.23. Aylward GP. Cognitive and neuropsychological outcomes: More than IQ scores.Ment Retard Dev Disabil Res Rev 2002;8:234-40.24. Taylor HG, Burant CJ, Holding PA, Klein N, Hack M. Sources of variability insequelae of very low birth weight. Child Neuropsychol 2002;8:163-78.25. Flynn JR. Searching for justice: the discovery of IQ gains over time. Am Psychol

    1999;54:5-20.26. Wolke D, Ratschinski G, Ohrt B, Riegel K. The cognitive outcome of very

    preterm infants may be poorer than often reported: an empirical investigation of howmethodological issues make a big difference. Eur J Pediatr 1994;153:906-15.27. Laucht M, Esser G, Baving L, Gerhold M, Hoesch I, Ihle W, et al. Behavioral

    sequelae of perinatal insults and early family adversity at 8 years of age. J Am Acad ChildAdolesc Psychiatry 2000;39:1229-37.28. Inder TE, Warfield SK, Wang H, Huppi PS, Volpe JJ. Abnormal cerebralstructure is present at term in premature infants. Pediatrics 2005;115:286-94.29. Kesler SR, Ment LR, Vohr B, Pajot SK, Schneider KC, Katz KH, et al. Volu-

    metric analysis of regional cerebral development in preterm children. Pediatr Neurol

    2004;31:318-25.

    30. MacKendrick W. Understanding neurodevelopment in premature infants: applied

    chaos theory. J Pediatr 2006;148:427-9.

    31. Rejno-Habte Selassie G, Jennische M, Kyllerman M, Viggedal G, Hartelius L.

    Comorbidity in severe developmental language disorders: neuropediatric and psycho-

    logical considerations. Acta Paediatr 2005;94:471-8.

    32. Reilly S, Skuse D, Wolke D. The nature and consequences of feeding problems in

    infancy. In: Cooper PJ, Stein A, editors. Childhood Feeding Problems and Adolescent

    Eating Disorders. London: Routledge; 2006. p 7-40.

    33. Sansavini A, Guarini A, Alessandroni R, Faldella G, Giovanelli G, Salvioli G. Are

    early grammatical and phonological working memory abilities affected by preterm birth?J Commun Disord 2007;40:23956.

    34. Hille ETM, den Ouden AL, Saigal S, Wolke D, Lambert M, Whitaker A, et al.

    Behavioural problems in children who weigh 1000 g or less at birth in four countries.

    Lancet 2001;357:1641-3.

    35. Bracewell M, Marlow N. Patterns of motor disability in very preterm children.

    Ment Retard Dev Disabil Res Rev 2002;8:241-8.

    36. Mizuno R. The male/female ratio of fetal deaths and births in Japan. Lancet

    2000;357:738-9.

    37. Edwards D. Brain protection for girls and boys. J Pediatr 2004;145:723-4.

    38. Brothwood M, Wolke D, Gamsu H, Benson J, Cooper D. Prognosis of the very

    low birth weight baby in relation to sex. Arch Dis Child 1986;61:559-64.

    39. Kraemer S. The fragile male. BMJ 2000;321:1609-12.

    40. Woodward LJ, Edgin JO, Thompson D, Inder TE. Object working memory

    deficits predicted by early brain injury and development in the preterm infant. Brain

    2005;128:2578-87.

    262 Wolke et al The Journal of Pediatrics February 2008

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    APPENDIX

    The EPICure Investigator Group: K Costeloe(London), AT Gibson (Sheffield), EM Hennessy (Lon-don), N Marlow (Nottingham), AR Wilkinson (Oxford),D Wolke (Warwick). Developmental Panel: Psycholo-gists: Emma Luck, Catherine Bamford, Helen Betteridge,Hanne Bruhn, Sandra Johnson, Iliana Magiati, Maria Mo-rahan, Isabel Tsverik. Paediatricians: Melanie Bracewell,

    Michele Cruwys, Ruth MacGregor, Lesley McDonald,Margaret Morton, Margaret Morris, Sue Thomas. Muth-

    anna Samara (Psychological data analysis), Heather Palmer(Study Administrator).

    Funding: BLISS, PPP Foundation and WellBeing.The EPICure Study Group comprises the paediatri-

    cians in 276 maternity units across the UK and Ireland whocontributed data to the study, whose invaluable help weacknowledge. The investigator group was responsible for theoriginal study cohort identification and studies up to 2.5 years

    of age and the developmental panel performed the data col-lection and validation.

    Specific Language Difficulties and School Achievement in Children Born at 25 Weeks of Gestation or Less 262.e1