You are on page 1of 8

Specic Language Difculties and School Achievement in Children Born at 25 Weeks of Gestation or Less

DIETER WOLKE, PHD, MUTHANNA SAMARA, MSC, MELANIE BRACEWELL, MD, FOR THE EPICURE STUDY GROUP*
AND

NEIL MARLOW, MD,

Objective To determine whether language and educational problems are specic or due to general cognitive decits 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) for the peer group. Extremely preterm children had an increased risk of language problems (odds ratio [OR] 10; 95% condence interval [CI] 3 to 32), speech problems (OR 4.4; 95% CI 3 to 7), and overall school difculties (OR 25; 95% CI 12 to 54). Extremely preterm boys were twice as likely to show decits as extremely preterm girls, but no such sex-based differences were apparent in the comparison group. Differences in general cognitive scores explained specic language or phonetic awareness decits, but not speech ratings or educational difculties, in the extremely preterm children. Conclusions Language or phonetic difculties are not specic and indicate general cognitive functional difculties. The ndings have implications for models of global deviation of brain development in extremely preterm children. (J Pediatr 2008;152:256-62) higher prevalence of cognitive impairments and poorer educational achievement has been repeatedly observed in children born preterm or with low birth weight compared with children born at full term.1 Other developmental disorders, such as language delays and decits,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 or learning disorders may be associated with general cognitive impairment, or they can be specic and independent of cognitive function or environmental disadvantage.2 Specic developmental language impairments or specic learning disorders are diagnosed when there is a clear discrepancy between general intellectual development as measured by, for example, performance IQ and language or learning achievement scores.6,7 Long-term adverse cognitive, language, and psychosocial outcomes have been reported in children with normal IQ but with specic language impairment.8 Specic decits may suggest either damage to or inhibition of normal development in specic areas of the brain.9 Few previous studies have evaluated whether these developmental or From the Department of Psychology and learning problems truly represent specic developmental disorders or can be accounted for Warwick Medical School, Health Sciences by general cognitive decits in VLBW children.10 Research Institute, University of Warwick, A recent longitudinal analysis of VLBW children suggests that learning difculties Coventry, UK (D.W., M.S.) and the Institute of Neuroscience, University of Notare not specic, but rather are more likely due to global decits in cognitive function and tingham, Nottingham, UK (M.B., N.M.). 4 may require different interventions than those developed for full-term children. HowSubmitted for publication Mar 30, 2007; ever, the children included in these cohorts were born before the widespread introduction last revision received Jun 18, 2007; accepted Jun 28, 2007. of antenatal corticosteroid and surfactant replacement therapy, which are important Reprint requests: Dieter Wolke, PhD, Univer11 determinants of the increased survival of extremely preterm infants that can be expected sity of Warwick, Department of Psychology to enhance long-term outcome and also possibly alter patterns of disability. These cohorts and Health Sciences Research Institute, War-

CI K-ABC MPC OR

Condence interval Kaufman Assessment Battery for Children Mental Processing Composite Odds ratio

PAT PLS-3 SD VLBW

Phonological Abilities Test Preschool Language Scale-3 Standard deviation Very low birth weight

wick Medical School, Coventry CV4 7AL, UK. E-mail: D.Wolke@warwick.ac.uk. *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

included very few extremely preterm children, whose survival has increased over the past 15 years and whose high risks of disability and general cognitive problems have been described previously.12 In this report, we describe the results of language, speech, phonetic, and educational difculties during the early school age period in a geographically based sample of children born before 26 weeks gestation, of whom 60% were exposed to antenatal steroid treatment and 84% received surfactant.13 We investigate the extent to which the language and learning difculties observed in this population are specic impairments or are in line with general cognitive abilities.

METHODS
Subjects The derivation and characteristics of this study population have been described previously,13,14 as have the details of the 6-year evaluation.12 The population represents all surviving children born at 25 weeks, 6 days gestational age or less between March and December 1995. Of the 308 children known to be alive at age 30 months, the parents of 241 consented to the study. A total of 204 children were in mainstream education. For each child assessed in a mainstream school, we sought an age- and sex-matched classmate as a comparison.12 Thus, we were able to assess 160 full-term born children, who form the comparison population. All children were assessed by a pediatrician and a psychologist trained in the techniques used for the study (see Appendix; available at www.jpeds.com). All appointments were made by the study administrator, and the assessors were blinded to the childrens group status. All parents gave written informed consent, and the study was approved by the Trent Multicentre Research Ethics Committee and the local education authorities in Scotland. Assessment General cognitive ability was assessed using the Kaufman Assessment Battery for Children (K-ABC),12,15 composed of 2 summative scales: the Mental Processing Composite (MPC), comprising Sequential and Simultaneous Processing subscales, which provides a global measure of the childs cognitive ability, and the Achievement Scale, an assessment of knowledge of facts, language concepts, and school-related skills. Receptive and expressive language abilities were evaluated using the Preschool Language Scale-3 (UK) (PLS-3), which comprises Auditory Comprehension and Expressive Communication scales.16 Articulation difculties were assessed according to 19 speech sounds in the initial or nal positions of consonant-vowel-consonant words, which the child is asked to imitate in the PLS assessment. We used the Phonological Abilities Test (PAT)17 to assess skills predictive of reading acquisition.18 The PAT comprises 4 subtests: rhyme detection, phoneme deletion (both beginning and end sounds), and a test of letter knowledge.17 Quality of speech was rated by the psychologists using published scales;19 phonological disorder (315.39) and stuttering (307)

were diagnosed according to criteria specied in the Diagnostic and Statistical Manual of Mental Disorders, 4th edition (DSM-IV).7 Cognitive impairment or disability precluded the use of the K-ABC in 41 index children.12 These children were evaluated using either the Grifths Scales of Mental Development20 (in 35 children) or the NEPSY Neuropsychology Assessment21 (in 6 children). The Grifths quotient or mean NEPSY standardized score was used to estimate a score. If this score was 40 (the lowest score on the K-ABC), then the child was assigned a score of 39. To give a measure of cognitive 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 for the K-ABC subscales or in reporting other test results. Teachers rated the scholastic performance of the index and comparison children against the national expected level of attainment for a child of the same age in English, mathematics, science, technology, geography, history, and information technology. These ratings were combined to yield a total academic achievement score.22 Eight experienced developmental psychologists were recruited to perform the assessments described above. All attended a course in which they were trained in all aspects of the study evaluation. After the training course, every second childs session was videotaped and for random quality check by the senior assessment psychologist.

Statistical Analysis Categorical outcomes were compared using the 2 test for trends, as appropriate, or Fishers exact test. Continuous outcomes were compared using an independent Student t test. All statistical tests were 2-sided. Differences in results between the extremely preterm and comparison children and between boys and girls (and their interactions) were evaluated using a generalized linear model if scales were normally distributed. A priori dichotomized outcomes were determined using a cutoff of 2 standard deviations (SDs) or the 10th/90th percentiles as appropriate. The comparison scores served as comparison norms for all tests. Testing for the presence of specic learning disabilities was done using multiple regression, with the overall cognitive score (MPC) as a covariate. All analyses were then repeated after excluding children with severe physical disability (eg, blindness, hearing loss requiring aids, cerebral palsy).

RESULTS
Cognitive Scores The mean scores for all children and boys and girls separately have been reported in detail previously.12 The mean MPC score was 105.7 (SD 1.8) for the comparison children and 82.1 (SD 19.2) for the extremely preterm children, a difference of 23.6 points (95% condence interval [CI] 20.3 to 26.8). In the comparison group, boys and girls had similar scores. In contrast, index boys (mean, 77.1
257

Specic Language Difculties and School Achievement in Children Born at 25 Weeks of Gestation or Less

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 Serious impairment (<2 SD) 1.9%* 4.2% 0% 1.3% 2.8% 0% 1.3%* 2.8% 0% 2.5% 4.2% 1.1% Extremely preterm group Mean (SD) 89.6 (20.1)* 85.1 (22.2) 93.6 (17.1) 88.7 (16.7)* 84.2 (18.2) 92.7 (14.1) 92.6 (21.1)* 88.8 (24.2) 96.0 (17.4) 32.7 (7.7) 31.3 (9.2) 34 (5.7) Serious impairment (<2 SD) 15.6%* 21.3% 10.5% 9.5% 12.8% 6.6% 12.1%* 20.2% 4.8% 9.1% 13.8% 4.8% OR (95% CI) for serious impairment 9.6 (2.9 to 32.3)*

n Total PLS-3 score Boys Girls Auditory comprehension Boys Girls Expressive communication Boys Girls Articulation screener Boys Girls 159 71 88 159 71 88 159 71 88 159 71 88

Mean (SD) 103.9 (14.4)* 102.8 (17.3) 104.8 (11.6) 101.3 (14.2)* 100.1 (17.5) 102.3 (10.8) 105.4 (15.2)* 104.5 (17.5) 106.2 (13.2) 34.9 (4.6) 34.3 (6.4) 35.4 (2.4)

n 199 94 105 200 94 106 199 94 105 198 94 104

8.2 (1.9 to 35.7)

11 (2.5 to 47.6)

3.8 (1.3 to 11.6)

Mean and SD for standardized scores are shown together with the proportion with scores below 2 SDs of the comparison group. 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.

19.6) scored lower than index girls (mean, 87.2 17.4); the difference in means was 10.1 points (95% CI 5.4 to 14.8), and the sex by group interaction was signicant (P .01). These effects remained after exclusion of children with severe physical 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 only the children tested using the K-ABC were considered (4.6 points; 95% CI 1.1 to 8.1). Compared with the control children (contemporary norms, 1.3%; n 2), 98 (40.6%) extremely preterm children had a general cognitive ability score (MPC) 2 SD, indicating moderate to severe cognitive impairment (P .001).12 Compared with extremely preterm girls (32%; n 38), extremely preterm boys (49%; n 60) were twice as likely to have serious impairment in overall cognitive scores (OR 2.1; 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 preterm children exhibited poorer performance in all of the PLS-3 composite scores and total score than the comparison children (Table I). The extremely preterm children were more likely to have serious language impairment, as evaluated by the total PLS-3 score and auditory comprehension, expressive communication, and articulation subtests (Table I); boys had higher rates of impairment than girls (total PLS, P .01; auditory comprehension, P .01; expressive communication, P .05; articulation, P .01). No sex differences were found in the comparison group. Although the interaction between group and sex was not signicant in the PLS-3 using continuous
258 Wolke et al

scores, extremely premature boys were more likely to have moderately or severely impaired scores than extremely premature girls (total PLS-3: OR 2.3, 95% CI 1 to 5.1, P .05; auditory comprehension: OR 2.1, 95% CI 0.8 to 5.5, 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 population, children who scored below the 10th percentile in the PAT or above the 90th percentile for the speech and language ratings were considered to be in the clinical, or abnormal, range. The extremely preterm children were more likely to have difculties on all subscales of the PAT and were more often rated in the clinical range in speech production and grammatical correctness in language by the assessors (Table II). Signicant sex differences in the phoneme deletion beginning sounds (P .01) and in grammatical correctness ratings (P .01) were found, with an excess of boys in the clinical range. Compared with their peer group, the extremely preterm children were rated as using less developmentally appropriate speech sounds for age and dialect (17.6% vs 6.3%; OR 3.2; 95% CI 1.5 to 6.6; P .01) and had more difculties in speech sound production, dened as interfering with academic achievement or with social communication (14.6% vs 3.1%; OR 5.3; 95% CI 2 to 13.9; P .001). These factors compose the DSM-IV classication phonological disorder (315.39).7 Similarly, the extremely preterm children had more disturbances in the normal uency 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).
The Journal of Pediatrics February 2008

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 Number/number with information PAT Rhyme detection Boys Girls Phoneme deletion beginning sounds Boys Girls Phoneme deletion end sounds Boys Girls Letter knowledge Boys Girls Speech rating Boys Girls Grammatical correctness rating Boys Girls 22/160 11/71 11/89 33/160 16/71 17/89 45/160 25/71 20/89 32/160 19/71 13/89 32/158 14/71 18/87 23/158 10/71 13/87 Percent 13.8* 15.5 12.4 20.6* 22.5* 19.1* 28.1* 35.2 22.5* 20* 26.8 14.6* 20.3* 19.7* 20.7* 14.6* 14.1* 14.9 Extremely preterm group Number/number with information 66/203 37/96 29/107 104/203 57/96 47/107 115/203 57/96 58/107 76/202 36/96 40/106 106/200 48/92 58/108 66/200 37/92 29/108 Percent 32.5* 38.5 27.1 51.2* 59.4* 43.9* 56.7* 59.4 54.2* 37.6* 37.5 37.7* 53* 52.2* 53.7* 33* 40.2* 26.9 OR (95% CI) 3.1 (1.8 to 5.2)*

4.1 (2.5 to 6.5)*

3.3 (2.1 to 5.2)*

2.4 (1.5 to 3.9)*

4.4 (2.8 to 7.1)*

2.9 (1.7 to 4.9)*

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.

Academic Achievement The Total Academic Achievement Score classies children scoring below average in contrast to average or above average performance.22 A score was assigned to 169 extremely preterm children and 150 comparison children by mainstream class teachers. Missing data are due to teachers not returning complete ratings. Of the extremely preterm children in mainstream 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 had children 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 mainstream schools 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). Specic Language or General Academic Impairment We explored the possibility of specic language impairment using multiple regression to adjust PLS-3 scores, clinical ratings for PAT/language scales, and teacher assessments for the general cognitive score (MPC). Cognitive impairment explained the differences between extremely preterm children and comparison children in PLS-3 total score and the 3 subscale scores independent of whether all children (Table

III) or only those without severe disability (not shown) were analyzed. For example, although the observed mean difference in the comparison childrens unadjusted PLS-3 total score was 14.3 points (95% CI 10.6 to 18.0), after adjustment, this fell to 1.8 points (95% CI 6.6 to 3). Categorical comparisons produced similar results. Cognitive impairment also accounted for the differences in impairment in phonetic awareness and language ratings (Table IV), but not for the differences in speech ratings and academic achievement (P .01 and .001 after adjustment, respectively). Speech impairments were still 2.6 times more frequent in the extremely preterm children (95% CI 1.5 to 4.6) after adjustment for general cognitive ability. Similarly, educational problems could not be attributed solely to general cognitive decits but remained 4.9 times more frequent (95% CI 2 to 11.5) after general cognitive score adjustment (Table IV).

DISCUSSION
In this entire population cohort of extremely preterm children in the UK and Ireland, we found considerable differences in general cognitive ability (IQ), language, phonetic awareness, articulation, and scholastic achievement compared with their classmates of the same age. These differences were more pronounced in this population than those observed in other studies of more mature very preterm or VLBW popu259

Specic Language Difculties and School Achievement in Children Born at 25 Weeks of Gestation or Less

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)
Unadjusted mean (95% CI) 89.6 (86.8 to 92.4) 103.9 (101.6 to 106.2)* 88.7 (86.4 to 91.1) 101.3 (99.1 to 103.5)* 92.6 (89.6 to 95.5) 105.4 (103.1 to 107.8)* 32.7 (31.7 to 33.8) 34.9 (34.2 to 35.6) Adjusted mean (95% CI) 96.7 (94.3 to 99.2) 98.5 (95.4 to 101.5) 94.1 (91.9 to 96.3) 96.5 (93.7 to 99.3) 100 (97.4 to 102.6) 100.5 (97.2 to 103.8) 34.3 (33.3 to 35.3) 34.5 (33.2 to 35.8) Unadjusted OR for serious impairment (95% CI) 9.6 (2.9 to 32.2)* Adjusted OR for serious impairment (95% CI) 1.3 (0.3 to 5.3)

PLS-3 Total score Extremely preterm Comparison Auditory comprehension Extremely preterm Comparison Expressive communication Extremely preterm Comparison Articulation screener Extremely preterm Comparison

8.3 (1.9 to 35.7)

1.6 (0.3 to 9.8)

10.7 (2.5 to 45.5)*

1.2 (0.2 to 6.5)

3.9 (1.2 to 11.6)

1.1 (0.3 to 4)

*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 Adjusted OR for clinical score clinical score (95% CI) (95% CI) PAT rhyme detection PAT phoneme deletion beginning sound PAT phoneme deletion end sound PAT letter knowledge Speech ratings Language ratings Teachers academic achievement scale 3 (1.8 to 5.2)* 4 (2.5 to 6.5)* 1.6 (0.8 to 3.2) 1.2 (0.7 to 2.1)

3.3 (2.1 to 5.2)* 2.4 (1.5 to 3.9)* 4.3 (2.7 to 6.8)* 2.9 (1.7 to 5)* 24.9 (11.6 to 53.6)*

1.1 (0.7 to 2) 1.3 (0.7 to 2.4) 2.6 (1.5 to 4.6) 1.2 (0.6 to 2.3) 4.9 (2 to 11.5)

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

lations, in whom disadvantages have been described over a wide range of cognitive functions, including information processing, language, phonetic awareness, and educational achievement.1,19,23,24 In school and everyday settings, children are compared not with children born in the 1970s, but rather with their classmates. Therefore, for all statistical comparisons, including the classication of impairment, as a reference we used the scores of the comparison group rather than the often outdated historical test norms, which are subject to signicant secular trends in adults and children25 and result in underestimation
260 Wolke et al

of impairment.12,26 Using this comparison, we found that 40.6% of extremely preterm children had general cognitive decits, and that these children were 56 times more likely to suffer moderate to severe cognitive decits compared with mainstream classmates born at full term. This nding of substantial general cognitive decits and language, phonetic, and speech impairments cannot be attributed to selective dropout of high achievers. Previously reported analysis indicated no differences regarding medical variables, growth, or early disability between those lost to follow-up and those assessed.12 Rather, dropout was more likely in disadvantaged families, which would be expected to reduce cognitive and language achievement,19,27 and thus we may have underestimated the language decit in our population. When controlling for general cognitive performance, no specic language difculties or phonetic decits were observed, a nding reported in previous studies of more mature VLBW and extremely preterm children.19,24 Thus, there is little evidence that language or phonetic processing problems in extremely preterm children are due to specic decits previously speculated to be a result of damage to or inhibition of normal development in specic areas of the brain.9 Rather, these and previous analyses in 2 other samples19,24 suggest that language abilities are substantially explained by general cognitive decits in extremely or very preterm children. This nding may have its equivalence in brain development, in that general cognitive impairments in extremely preterm children may have their origin in global changes in brain development in terms of size and complexity28-30 and generally are not the result of damage to specic brain regions. These ndings add to our understanding of the neuropathologic pathways associated with later language function in extremely preterm children.
The Journal of Pediatrics February 2008

In contrast, speech problems and a global rating of educational difculties could not be explained solely by lower IQ, a nding replicating the results reported for VLBW children in Germany.19 Speech difculties often involve oral motor problems31 and may be signicantly affected by specic motor problems and controlled by specic brain areas. Oral motor problems, such as in eating difculties, have long been suspected to be associated with later speech problems32 and warrant further exploration. Furthermore, our ndings regarding educational problems are consistent with those reported by Taylor et al,24 who found specic mathematical achievement decits in children with birth weight 750 g. Wolke and Meyer19 found that numerical abilities were not solely accounted for by IQ in a German VLBW sample. A recent longitudinal study comparing extremely and very preterm children and full-term control children showed that general cognitive impairment had a strong initial impact on specic abilities (phonetic accuracy, letter and number knowledge) that are prerequisites for learning reading, writing, and mathematical skills. However, attained reading, writing, and mathematical abilities are the mediating link to longer-term educational success in both full-term and preterm children.4 Furthermore, other factors, such as working memory,33 attention decit and peer relationship problems,1,34 motor problems,35 and family socioeconomic factors,4,24 also contribute to educational problems in extremely premature children and need to be further explored in longitudinal analysis. This is relevant, because motor or behavioral management programs may be able to increase educational performance in extremely preterm children. A range of adverse perinatal outcomes has been described in males, ranging from death,36 perinatal brain injury,37 cerebral palsy, and delayed lung maturation38 to preterm birth and stillbirth. Signicant sex differences in cognitive functioning have been reported in some cohorts38 but not in others.19 We found a substantial and clinically relevant increase in cognitive, language, and educational difculties in extremely preterm boys compared with extremely preterm girls. This is in the context of the lower survival and greater frequency of neonatal problems13 and higher rates of disability14 in males in this population. It may be speculated that sex differences in intrauterine development may make the male fetus/extremely preterm infant particularly vulnerable to perinatal adversity and may have important consequences for later development.39 The gestational age at which male vulnerability is no longer demonstrable remains to be determined, but it would seem to be particularly evident at very low gestational age. The present study has some limitations. We required the cooperation of the childrens teachers to obtain parental consent to communicate the contact details of the control children to the investigators. Lack of teacher cooperation or of parental consent was the major reason why we did not have a class control for all target children. We found no pattern or lack of cooperation according to regional variation or social deprivation in the area that the school was serving; thus, we consider 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 been achieved in all cases, considering that the extremely preterm children were on average smaller, more often required correction for sight, and more often had a motor disability. This may have provided clues to the assessors regarding group membership. In conclusion, our ndings demonstrate that adverse cognitive, language, phonetic, and educational sequelae are more frequent in extremely premature children than in more mature preterm populations and that the cognitive impairment is general rather than specic. Cognitive impairments explain only part of the educational difculties experienced by these children, and future analysis needs to take into account other areas of function, including behavioral, motor, and social difculties. Our ndings of patterns of functional difculties may have important implications for brain imaging research.40 Extremely preterm birth and very early extrauterine development may alter the pattern of brain development across a range of brain regions, including all areas of the cortex and deeper brain structures,28 and may be responsible for the global decits in neuropsychological function seen in this vulnerable population.

REFERENCES
1. 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 understanding of developmental mechanisms. Acta Paediatr 1999;88:488-90. 3. Largo RH, Molinari L, Kundu S, Duc G. Intellectual outcome, speech and school performance in high-risk preterm children with birth weight appropriate for gestational age. Eur J Pediatr 1990;149:845-50. 4. Schneider W, Wolke D, Schlagmller M, Meyer R. Pathways to school achievement 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 low birth weight: neuropsychological ndings. 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 dening 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 Child Psychol 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 control children 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 rst 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 Med 2000;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.

Specic Language Difculties and School Achievement in Children Born at 25 Weeks of Gestation or Less

261

18. Bryant P, Nunes T, Bindman M. Awareness of language in children who have reading difculties: 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 of 6-year-old very preterm children and their peers: the Bavarian Longitudinal Study. Dev Med Child Neurol 1999;41:94-109. 20. Grifths 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 Developmental Neuropsychological 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 in sequelae 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 how methodological 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 Child Adolesc Psychiatry 2000;39:1229-37. 28. Inder TE, Wareld SK, Wang H, Huppi PS, Volpe JJ. Abnormal cerebral structure 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 psychological 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;40:239 56. 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 decits 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

APPENDIX
The EPICure Investigator Group: K Costeloe (London), AT Gibson (Shefeld), EM Hennessy (London), N Marlow (Nottingham), AR Wilkinson (Oxford), D Wolke (Warwick). Developmental Panel: Psychologists: Emma Luck, Catherine Bamford, Helen Betteridge, Hanne Bruhn, Sandra Johnson, Iliana Magiati, Maria Morahan, 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 paediatricians in 276 maternity units across the UK and Ireland who contributed data to the study, whose invaluable help we acknowledge. The investigator group was responsible for the original study cohort identication and studies up to 2.5 years of age and the developmental panel performed the data collection and validation.

Specic Language Difculties and School Achievement in Children Born at 25 Weeks of Gestation or Less

262.e1

You might also like