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Article |

Learning Problems in Kindergarten Students With Extremely Preterm Birth FREE

H. Gerry Taylor, PhD; Nancy Klein, PhD; Marcia G. Anselmo, MEd; Nori Minich, BS; Kimberly A. Espy, PhD; Maureen Hack, MB, ChB
[+] Author Affiliations

Author Affiliations: Department of Pediatrics, Case Western Reserve University and Rainbow Babies & Children's Hospital, University Hospitals Case Medical Center (Drs Taylor and Hack and Ms Minich), and Department of Education, Cleveland State University (Dr Klein), Cleveland, Ohio; and Office of Research and Department of Psychology, University of Nebraska–Lincoln (Dr Espy). Ms Anselmo is an educational consultant in Gates Mills, Ohio.


Arch Pediatr Adolesc Med. 2011;165(9):819-825. doi:10.1001/archpediatrics.2011.137.
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Objectives To assess learning problems among kindergarten students with extremely preterm birth and to identify risk factors.

Design Cohort study.

Setting Children's hospital.

Participants A cohort of 148 children born between January 1, 2001, and December 31, 2003, with extremely preterm birth, defined as less than 28 weeks' gestation or having a birth weight of less than 1000 g, and 111 classmate control individuals born at term with normal birth weight.

Interventions The children were enrolled in the study during their first year in kindergarten and were assessed on measures of learning progress.

Main Outcome Measures Achievement testing, teacher ratings of learning progress, and individual educational assistance.

Results Children with extremely preterm birth had lower mean standard scores than controls on achievement tests of spelling (8.52; 95% confidence interval, 4.58-12.46) and applied mathematics (11.02; 6.76-15.28). They had higher rates of substandard learning progress by teacher report in written language (odds ratio, 4.23; 95% CI, 2.32-7.73) and mathematics (7.08; 2.79-17.95). Group differences in mathematics achievement and in teacher ratings of learning progress were statistically significant even in children without neurosensory deficits or low global cognitive ability. Neonatal risk factors, early childhood neurodevelopmental impairment, and socioeconomic status predicted learning problems in children with extremely preterm birth; however, many children with problems were not enrolled in a special education program.

Conclusions Learning problems in children with extremely preterm birth are evident in kindergarten and are associated with neonatal and early childhood risk factors. Our findings support efforts to provide more extensive monitoring and interventions before and during the first year of school.

Children with extremely preterm birth (hereafter referred to as EP children) born before 28 weeks' gestation or with a birth weight of less than 1000 g are at high risk for neurodevelopmental disorders.1 These disorders range from severe conditions, such as cerebral palsy, sensory deficits, and overall mental deficiency, to more subtle impairments in cognition, behavior, and academic achievement, with many EP children requiring special educational assistance during their school-aged years.212 Academic difficulties are of particular concern once EP children begin kindergarten because failure to recognize these difficulties can delay special educational interventions.13

We know little about the educational progress of EP children during this critical period of schooling. Studies11,12,1424 have documented academic difficulties at early school age per test results or per teacher ratings of achievement. However, this previous research did not examine the nature and predictors of learning problems in kindergarten. Knowledge pertaining to early academic outcomes is vital in appraising the educational needs of these children and their risks for future learning problems.2529 Information regarding neonatal and early childhood factors related to poor achievement in kindergarten also would be useful to identify children most in need of careful monitoring.

Our primary objectives were to assess early learning progress among EP children vs that of control individuals born at term with normal birth weight (hereafter referred to as NBW controls) and to examine associations of educational outcomes in the EP group with neonatal risk factors, early childhood neurodevelopmental impairment, and socioeconomic status (SES). The primary hypothesis was that rates of academic problems and learning assistance would be higher for EP children than for NBW controls.3,12,21,23,24,29 Secondary hypotheses were that group differences would remain even when excluding children with more severe deficits,20,30 that many EP children with academic problems would not be receiving special assistance in school,10,31,32 and that higher rates of learning problems in the EP group would be associated with neonatal risk factors, early childhood neurodevelopmental impairment, and lower SES.3,18,19,25,3343

PARTICIPANTS

Excluding 8 infants with congenital infections or abnormalities, 246 EP children born at less than 28 weeks' gestation or with a birth weight of less than 1000 g were admitted to the neonatal intensive care unit of Rainbow Babies & Children's Hospital, Cleveland, Ohio, between January 1, 2001, and December 31, 2003. Of 198 (80.5%) who survived, 148 (74.7%) were enrolled in the study. Reasons for nonparticipation included failure to locate families (21 children), relocation out of the region (16 children), and refusals or no-shows (5 children). Eight children could not be assessed because of custody issues or because they were non–English speaking. Comparison of participants with nonparticipants failed to reveal statistically significant differences in sex, race/ethnicity, or neonatal risk factors. The children were followed up longitudinally and were contacted during the initial year in which they attended kindergarten. One hundred twenty-nine EP children were in regular classrooms, 16 were in full-time special education programs, and 3 were homeschooled.

The EP group was composed of 56 children (37.8%) with less than 750 g birth weight, 32 children (21.6%) with less than 25 weeks' gestation, and 37 children (25.0%) with birth weight less than the 10th percentile for gestational age.44 Neonatal complications included infection or necrotizing enterocolitis in 60 children (40.5%), bronchopulmonary dysplasia (defined as supplemental oxygen at 36 weeks' corrected age) in 77 children (52.0%), severe retinopathy of prematurity (defined as stage 4 or 5 retinopathy or receipt of cryotherapy or laser therapy45) in 27 children (18.2%), and abnormal ultrasonographic findings (defined as grade III or IV intraventricular hemorrhage, periventricular leukomalacia, or ventricular dilatation at discharge) in 15 children (10.1%). At 20 months' corrected age, 60 EP children (40.5%) had neurodevelopmental impairment, defined as cerebral palsy (13 children [8.8%]), blindness or deafness (6 children [4.1%]), or a Mental Development Index of less than 70 on the second edition of the Bayley Scales of Infant Development46 (57 children [38.5%]).

The control group was composed of 111 term-born NBW children (>36 weeks' gestational age and >2500 g birth weight) from the same classrooms as the EP children (n = 93) or from other kindergarten classrooms (n = 18). To recruit controls, flyers were sent home with the students in each classroom. From the pool of students whose families responded, we recruited the classmate who most closely matched each EP child based on sex, race/ethnicity, and age at assessment. Controls were not recruited for children who were homeschooled or attending full-time self-contained special education programs (n = 19). Matches for the remaining 18 EP children in regular classrooms were not recruited because of school refusals, school locations too distant from the medical center, or difficulties in finding matches.

No group differences were observed in sex, race/ethnicity, or SES as defined by the mean of the sample's z scores for maternal education in years, caregiver occupation (averaged for 2-parent households),47 and median income for the neighborhood of residence based on data from the 2000 US Census (Table 1).48 The EP group was older than the NBW group in chronological age at school entry. However, the groups did not differ in age corrected for prematurity because proportionally more EP children had been held back a year before kindergarten entry (21.6% vs 2.7%, P < .001). Group comparisons also failed to reveal differences in age at testing, months in school when the teacher ratings were completed, or percentage of children in full-day kindergarten (83.7% vs 80.2%). Although a larger proportion of the EP group received early intervention services before school entry (83.1% vs 12.6%, P < .001), the groups showed little difference in rates of enrollment in preschool (83.8% vs 84.7%) or day care (49.3% vs 50.5%).

PROCEDURES AND MEASURES

Children were administered tests of achievement and cognitive ability by examiners who were masked to birth status; during that time, their parents completed interviews and questionnaires to obtain information regarding family characteristics and children's health status. Children's tests were administered in a fixed order during a single session. Six EP children were untestable on most measures because of cerebral palsy and severe cognitive impairment. Scores on achievement and intelligence measures for these children and others whose functioning was too low to be tested were assumed to be less than 85. The research was approved by the University Hospitals Case Medical Center Institutional Review Board; written informed consent from parents and teachers was obtained before participation.

Achievement measures included the letter and word identification, spelling, calculation, and applied problems subtests of the Woodcock-Johnson III Tests of Achievement.49 To take into account time in kindergarten, the scores on these tests were based on grade rather than on age standards. Test reliability for these measures is good, and validity has been documented relative to other achievement tests. Estimates of IQ were obtained using the age-standardized brief intelligence assessment (BIA) score from the Woodcock-Johnson III Tests of Cognitive Abilities.50

Teachers provided information regarding special education programs as defined by an individual educational plan (IEP). The IEPs were identified by parent report when the teacher report was unavailable. Teachers of children attending regular classrooms reported on accommodations for learning difficulties within the classroom and completed ratings of student learning progress in each of several curricular objectives based on State of Ohio–mandated goals.51 Using a previously validated method,52 0 was assigned for progress toward a given objective that was behind expectations by at least a full grading period, 1 for progress that was below expectations by less than a full grading period, and 2 for progress that was at or above expectations. An advantage of these ratings compared with formal testing is that they provided information regarding children's learning progress in specific areas of competency. Teachers were not informed of children's birth status.

STATISTICAL ANALYSIS

Analysis of covariance was used to compare the EP and NBW groups on the results of achievement testing and on the sum of teacher ratings of learning progress in written language and mathematics. Sex, race/ethnicity, and SES were included as covariates. Child race/ethnicity was defined by caregivers and was included in analyses to control for demographic background. Preliminary analyses failed to indicate any covariate × group interactions, justifying exclusion of interaction terms from the models.

Logistic regression analysis was conducted to examine group differences in learning problems as defined by standard scores of less than 85 on the achievement tests, substandard teacher ratings of learning progress (ie, 0 or 1), special education (as defined by an IEP or related services), and any classroom accommodation. Covariates in these analyses were the same as those included in the corresponding analysis of covariance. The variable of months in school was controlled for in analyses of IEPs because these placements increased during the school year.

To determine if learning deficits in the EP children could be attributed to the subset of children with cerebral palsy, blindness, deafness, or low global cognitive ability (as defined by a BIA of less than 85), group comparisons were repeated with these children excluded from the analysis. To determine if these deficits were identifiable based on having an IEP, group comparisons also were rerun after excluding this subset of children. Associations of poor achievement test performance and substandard learning progress with IEPs and classroom accommodations were investigated using χ2 analysis.

Associations of learning problems with neonatal risk factors, neurodevelopmental impairment at 20 months, and SES were examined using logistic regression analysis. Each predictor was examined in a separate analysis. Sex, race/ethnicity, and SES were covariates in analyses of the neonatal and neurodevelopmental factors.

Bonferroni-corrected α levels were used to determine statistical significance, with adjustments on a familywise basis within the domains of written language and mathematics. Therefore, α level was .05 divided by 3 (ie, .02) for each of 3 primary measures within each domain (ie, 2 test scores and the sum of teacher ratings for the analyses of covariance; deficits on the results of 2 tests and any indication of substandard learning progress for the logistic regression analyses). For the sample size, the power was 0.80 with 2-sided α = .05 for detecting effect sizes of 0.33 and differences in event rates of 15.0%. Differences of at least this magnitude were anticipated based on previous research with similar samples.3

The EP children had lower mean scores on achievement tests of spelling (8.52; 95% confidence interval, 4.58-12.46) and applied problems (11.02; 6.76-15.28) and lower sum teacher ratings of learning progress in written language and mathematics than NBW controls (Table 2). A larger proportion of the EP group compared with the NBW group was untestable or failed to reach basal levels of performance in mathematics calculation (52.1% vs 20.7%, P < .001). Even when excluding children with neurosensory disorders or a BIA of less than 85 (ie, 65 EP children and 12 NBW children), the EP group had lower scores on applied problems and lower sum teacher ratings of learning progress than the NBW group. Several of the group differences also remained statistically significant when excluding children with IEPs.

Table Graphic Jump LocationTable 2. Study Group Comparison Based on Measures of Achievement and Learninga

Consistent with these results, the EP group had higher rates of IEPs and classroom accommodations (Table 3). Several group differences remained statistically significant in analyses that excluded children with neurosensory deficits or a BIA of less than 85 or those with IEPs.

Table Graphic Jump LocationTable 3. Study Group Comparison Based on Rates of Learning Problems and Educational Interventionsa

Children with IEPs and classroom accommodations had higher rates of poor achievement test performance and substandard learning progress in written language and mathematics (P < .05 for all). However, 26 of 70 EP children (37.1%) with a score of less than 85 on 1 or more achievement tests did not have an IEP. Low-achieving EP children were less likely to have an IEP if they had normal neurosensory status and a BIA of 85 or higher (n = 14) vs a neurosensory deficit or a BIA of less than 85 (n = 12) (P = .01). Low-achieving EP children without an IEP had statistically significantly higher scores on spelling and applied problems and lower rates of less than 25 weeks' gestation, abnormal ultrasonographic findings, and neurodevelopmental impairment at 20 months compared with those with an IEP.

Within the EP group, neonatal risk factors, neurodevelopmental impairment at 20 months, and SES were associated with learning problems (Table 4). Less than 25 weeks' gestation and bronchopulmonary dysplasia were associated with higher rates of IEPs and classroom accommodations even when children with neurodevelopmental impairment at 20 months were excluded from analysis.

Table Graphic Jump LocationTable 4. Neonatal and Early Childhood Risk Factors Significantly Related to Learning Problems Among Children in the EP Groupa

Survival of EP children has reached a previously unsurpassed level but is offset by high rates of neonatal morbidity.53 As increasing numbers of these children are reaching school age, it is critical that we identify their problems at school entry and factors related to early educational difficulties. Our results reveal that the EP children performed worse on achievement tests, were making less learning progress, and had higher rates of IEPs and classroom accommodations than NBW controls. Academic problems were evident based on the results of tests of written expression and mathematics and in teacher ratings of learning progress in these areas. A 2009 study20 of academic outcomes among 6-year-olds born in the 1990s with gestation of 33 or fewer weeks indicated higher rates of academic problems compared with NBW controls even for the subset of EP children without neurosensory deficits or low global cognitive ability. Our results suggest similar outcomes for children born more recently. Although other studies12,18,20,21,23,54,55 have reported deficiencies in academic readiness or initial achievement skills among preterm children, ours is the first study to date, to our knowledge, that demonstrates the pervasiveness of learning deficiencies during the first year in school among EP children born since 2000. The EP and NBW groups were similar in sociodemographic characteristics, indicating that neonatal brain insults and subsequent abnormalities in neural development may have contributed largely to the higher rates of educational difficulties for the former group.56,57

Also, this study is among the first to examine educational interventions for EP children in kindergarten and the correspondence of these interventions with learning problems. More EP children than NBW controls were receiving special assistance at school; however, many EP children with low scores on an achievement test did not have an IEP. Low-achieving EP children without an IEP had higher achievement scores and lower rates of neurosensory deficit, poor cognitive ability, and neonatal complications than those with an IEP, suggesting that children with less severe impairments are more likely to be underidentified. It is also possible that IEPs had not been completed for some children despite parent or teacher awareness of learning difficulties. Our results imply that the educational needs of EP children are not met fully.

Achievement deficits in the EP group were evident in spelling and applied mathematics but not in word recognition. When children with neurosensory deficits or low global cognitive ability were excluded from analysis, only the deficit in mathematics in applied problems remained statistically significant. These findings are consistent with other data indicating that among preterm children, difficulties in mathematics are more prominent and selective than problems in reading.1,6,20,35,5860

Neonatal risk factors associated with the learning problems of EP children in kindergarten included less than 25 weeks' gestation, abnormal cranial ultrasonographic findings, bronchopulmonary dysplasia, and infection. Neurodevelopmental impairment at 20 months and lower SES also predicted learning problems. Previous studies3,18,19,31,32,34,36,37,3943,61,62 have reported similar risks for deficits in school readiness skills and special education interventions. Therefore, these risk factors may be useful in identifying the children most in need of developmental monitoring and early childhood interventions before school entry.

A limitation of this study was that teacher ratings of learning progress were obtained only for EP children attending regular classrooms. This procedure was warranted to ensure that expectations for progress could be judged relative to the general kindergarten population but is likely to have underestimated the effect of EP on learning progress. A further limitation is that information regarding IEPs was provided by teachers and parents, so we had no means of determining the extent to which these plans were implemented or addressed the children's learning problems. Our EP cohort was hospital based, and we were unable to follow up 25.3% of the families. The sample was predominantly urban and African American and, although largely reflective of EP births within the region, was not representative of the population of the United States as a whole. Educational interventions may have varied from those provided elsewhere in the United States. Because of privacy issues, parents of NBW children were selected from among those who agreed to be contacted, introducing possible bias in the selection of controls. However, the children attended many schools throughout the region; and no differences were observed in background factors between participants and nonparticipants or between the EP and NBW groups. Our results are similar to those from previous studies20,21,30 of early educational outcomes.

In older school-aged children with very low birth weight, poor reading skills are associated with reduced cerebellar volume63 and mathematics difficulties with reduced gray matter in the left parietal lobe.64 Further studies are needed to investigate the neural basis of early academic difficulties in EP children and to examine the cognitive and behavioral problems associated with these difficulties. Deficits in specific skill areas, such as processing speed and working memory, may be related closely to academic difficulties, with different patterns of association for reading and mathematics disabilities.11,59,65 Additional study of environmental influences on academic achievement at school entry is needed to identify characteristics of families and schools that buffer or exacerbate the effects of extremely preterm birth on early learning progress.29,66

In conclusion, our findings reveal high rates of learning problems and educational interventions among EP children at the time of school entry, as well as associations of these outcomes with neonatal risk factors and neurodevelopmental impairment at 20 months. The results underscore that many EP children with learning problems in kindergarten are not receiving special interventions and that teacher ratings of learning progress hold promise as a simple and effective means to screen for these problems. Efforts to minimize the adverse effects of EP on later academic achievement may need to include more extensive developmental and educational interventions beginning in kindergarten or earlier.1821,2527 A system of follow-up care that provides ongoing monitoring of children's status and needs from birth through school age, such as a medical home,26 may be helpful in ensuring early detection and intervention.

Correspondence: H. Gerry Taylor, PhD, Department of Pediatrics, Rainbow Babies & Children's Hospital, University Hospitals Case Medical Center, 10524 Euclid Ave, Cleveland, OH 44106-6038 (hgt2@case.edu).

Accepted for Publication: March 15, 2011.

Author Contributions: Dr Taylor had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Taylor, Klein, Anselmo, Minich, Espy, and Hack. Acquisition of data: Taylor, Klein, and Hack. Analysis and interpretation of data: Taylor, Klein, Anselmo, Minich, Espy, and Hack. Drafting of the manuscript: Taylor and Hack. Critical revision of the manuscript for important intellectual content: Taylor, Klein, Minich, Espy, and Hack. Statistical analysis: Taylor and Minich. Obtained funding: Taylor, Minich, Espy, and Hack. Administrative, technical, and material support: Taylor, Anselmo, and Hack. Study supervision: Taylor, Klein, Minich, and Hack.

Financial Disclosure: None reported.

Funding/Support: This work was funded by grant HD050309 from the National Institutes of Health (principal investigator, Dr Taylor), which provided financial support for the design and conduct of the study.

Additional Contributions: Anne Birnbaum, AA, Elizabeth Roth, PhD, Dan Maier, MA, Andrea Barkoukis Gefteas, MS, Michelle R. Jacobs, MA, Alice Kostiuc, BA, and Ketrin Lengu, BA, assisted in recruitment, data collection, and coding.

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PubMed   |  Link to Article
Msall ME, Buck GM, Rogers BT, Merke D, Catanzaro NL, Zorn WA. Risk factors for major neurodevelopmental impairments and need for special education resources in extremely premature infants [published correction appears in J Pediatr. 1992;120(5):838].  J Pediatr. 1991;119(4):606-614
PubMed   |  Link to Article
Sell EJ, Gaines JA, Gluckman C, Williams E. Early identification of learning problems in neonatal intensive care graduates.  Am J Dis Child. 1985;139(5):460-463
PubMed
Short EJ, Klein NK, Lewis BA,  et al.  Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes.  Pediatrics. 2003;112(5):e359-e366
PubMed  |  Link to Article   |  Link to Article
Vohr BR, Garcia Coll CT. Neurodevelopmental and school performance of very low-birth-weight infants: a seven-year longitudinal study.  Pediatrics. 1985;76(3):345-350
PubMed
Yudkin PL, Aboualfa M, Eyre JA, Redman CWG, Wilkinson AR. New birthweight and head circumference centiles for gestational ages 24 to 42 weeks.  Early Hum Dev. 1987;15(1):45-52
PubMed   |  Link to Article
Schmidt B, Asztalos EV, Roberts RS, Robertson CMT, Sauve RS, Whitfield MF.Trial of Indomethacin Prophylaxis in Preterms (TIPP) Investigators.  Impact of bronchopulmonary dysplasia, brain injury, and severe retinopathy on the outcome of extremely low-birth-weight infants at 18 months: results from the Trial of Indomethacin Prophylaxis in Preterms.  JAMA. 2003;289(9):1124-1129
PubMed   |  Link to Article
Bayley N. Bayley Scales of Infant Development. 2nd ed. San Antonio, TX: Psychological Corp; 1993
Hauser RM, Warren JR. Socioeconomic indexes for occupations: a review, update, and critique.  Soc Methodology. 1997;27(1):177-298
Link to Article
Federal Financial Institutions Examination Council.  Geocoding system. Federal Financial Institutions Examination Council Web site. http://www.ffiec.gov/geocode/default.aspx. Accessed June 8, 2011
Woodcock RW, McGrew KS, Mather N. Woodcock-Johnson III Tests of Achievement. Itasca, IL: Riverside Publishing; 2001
Woodcock RW, McGrew KS, Mather N. Woodcock-Johnson III Tests of Cognitive Abilities. Itasca, IL: Riverside Publishing; 2001
Ohio Department of Education.  A Standards Guide for Families: What Is Expected in Grade K. Columbus: Ohio Dept of Education; 2003
Taylor HG, Anselmo M, Foreman AL, Schatschneider C, Angelopoulos J. Utility of kindergarten teacher judgments in identifying early learning problems.  J Learn Disabil. 2000;33(2):200-210
PubMed   |  Link to Article
Stoll BJ, Hansen NI, Bell EF,  et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network.  Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network.  Pediatrics. 2010;126(3):443-456
PubMed   |  Link to Article
Halsey CL, Collin MF, Anderson CL. Extremely low birth weight children and their peers: a comparison of preschool performance.  Pediatrics. 1993;91(4):807-811
PubMed
Woodward LJ, Moor S, Hood KM,  et al.  Very preterm children show impairments across multiple neurodevelopmental domains by age 4 years.  Arch Dis Child Fetal Neonatal Ed. 2009;94(5):F339-F344
PubMed   |  Link to Article
Nosarti C, Giouroukou E, Healy E,  et al.  Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome.  Brain. 2008;131(pt 1):205-217
PubMed
Volpe JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances.  Lancet Neurol. 2009;8(1):110-124
PubMed   |  Link to Article
Klebanov PK, Brooks-Gunn J, McCormick MC. School achievement and failure in very low birth weight children.  J Dev Behav Pediatr. 1994;15(4):248-256
PubMed   |  Link to Article
Taylor HG, Espy KA, Anderson PJ. Mathematics deficiencies in children with very low birth weight or very preterm birth.  Dev Disabil Res Rev. 2009;15(1):52-59
PubMed   |  Link to Article
Aarnoudse-Moens CSH, Oosterlaan J, Duivenvoorden HJ, van Goudoever JB, Weisglas-Kuperus N. Development of preschool and academic skills in children born very preterm.  J Pediatr. 2011;158(1):51-56
PubMed   |  Link to Article
Horwood LJ, Mogridge N, Darlow BA. Cognitive, educational, and behavioural outcomes at 7 to 8 years in a national very low birthweight cohort.  Arch Dis Child Fetal Neonatal Ed. 1998;79(1):F12-F20
PubMed   |  Link to Article
Sullivan MC, Margaret MM. Perinatal morbidity, mild motor delay, and later school outcomes.  Dev Med Child Neurol. 2003;45(2):104-112
PubMed   |  Link to Article
Allin M, Matsumoto H, Santhouse AM,  et al.  Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term.  Brain. 2001;124(pt 1):60-66
PubMed   |  Link to Article
Isaacs EB, Edmonds CJ, Lucas A, Gadian DG. Calculation difficulties in children of very low birthweight: a neural correlate.  Brain. 2001;124(pt 9):1701-1707
PubMed   |  Link to Article
Mulder H, Pitchford NJ, Marlow N. Processing speed and working memory underlie academic attainment in very preterm children.  Arch Dis Child Fetal Neonatal Ed. 2010;95(4):F267-F272
PubMed   |  Link to Article
Belsky J, MacKinnon C. Transition to school: developmental trajectories and school experiences.  Early Educ Dev. 1994;5(2):106-119
Link to Article

Figures

Tables

Table Graphic Jump LocationTable 2. Study Group Comparison Based on Measures of Achievement and Learninga
Table Graphic Jump LocationTable 3. Study Group Comparison Based on Rates of Learning Problems and Educational Interventionsa
Table Graphic Jump LocationTable 4. Neonatal and Early Childhood Risk Factors Significantly Related to Learning Problems Among Children in the EP Groupa

References

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Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood.  Lancet. 2008;371(9608):261-269
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Taylor HG, Klein N, Drotar D, Schluchter M, Hack M. Consequences and risks of <1000-g birth weight for neuropsychological skills, achievement, and adaptive functioning.  J Dev Behav Pediatr. 2006;27(6):459-469
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Bowen JR, Gibson FL, Hand PJ. Educational outcome at 8 years for children who were born extremely prematurely: a controlled study.  J Paediatr Child Health. 2002;38(5):438-444
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Johnson S, Hennessy E, Smith R, Trikic R, Wolke D, Marlow N. Academic attainment and special educational needs in extremely preterm children at 11 years of age: the EPICure study.  Arch Dis Child Fetal Neonatal Ed. 2009;94(4):F283-F289
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Böhm B, Smedler A-C, Forssberg H. Impulse control, working memory and other executive functions in preterm children when starting school.  Acta Paediatr. 2004;93(10):1363-1371
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Hack M, Taylor HG, Schluchter M, Andreias L, Drotar D, Klein N. Behavioral outcomes of extremely low birth weight children at age 8 years.  J Dev Behav Pediatr. 2009;30(2):122-130
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Litt J, Taylor HG, Klein N, Hack M. Learning disabilities in children with very low birthweight.   J Learn Disabil. 2005;38(2):130-141
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Wolke D, Samara M, Bracewell M, Marlow N.EPICure Study Group.  Specific language difficulties and school achievement in children born at 25 weeks of gestation or less.  J Pediatr. 2008;152(2):256-262
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Klein NK. Children who were very low birthweight: cognitive abilities and classroom behavior at five years of age.  J Spec Educ. 1988;22(1):41-54
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Larroque B, Ancel P-Y, Marret S,  et al; EPIPAGE Study group.  Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study).  Lancet. 2008;371(9615):813-820
PubMed   |  Link to Article
Mikkola K, Ritari N, Tommiska V,  et al.  Neurodevelopmental outcome at 5 years of age of a national cohort of extremely low birth weight infants who were born in 1996-1997.  Pediatrics. 2005;116(6):1391-1400
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Patrianakos-Hoobler AI, Msall ME, Marks JD, Huo D, Schreiber MD. Risk factors affecting school readiness in premature infants with respiratory distress syndrome.  Pediatrics. 2009;124(1):258-267
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Patrianakos-Hoobler AI, Msall ME, Huo D, Marks JD, Plesha-Troyke S, Schreiber MD. Predicting school readiness from neurodevelopmental assessments at age 2 years after respiratory distress syndrome in infants born preterm.  Dev Med Child Neurol. 2010;52(4):379-385
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Pritchard VE, Clark CAC, Liberty K, Champion PR, Wilson K, Woodward LJ. Early school-based learning difficulties in children born very preterm.  Early Hum Dev. 2009;85(4):215-224
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Schneider W, Wolke D, Schlagmuller M, Meyer R. Pathways to school achievement in very preterm and full term children.  Eur J Psychol Educ. 2004;19(4):385-406
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van Baar AL, van Wassenaer AG, Briët JM, Dekker FW, Kok JH. Very preterm birth is associated with disabilities in multiple developmental domains.  J Pediatr Psychol. 2005;30(3):247-255
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Vohr BR, Msall ME. Neuropsychological and functional outcomes of very low birth weight infants.  Semin Perinatol. 1997;21(3):202-220
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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(2):94-109
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High PC.American Academy of Pediatrics Committee on Early Childhood, Adoption, and Dependent Care and Council on School Health.  School readiness.  Pediatrics. 2008;121(4):e1008-e1015
PubMed  |  Link to Article   |  Link to Article
Hintz SR, Kendrick DE, Vohr BR, Poole WK, Higgins RD.National Institute of Child Health and Human Development (NICHD) Neonatal Research Network.  Community supports after surviving extremely low-birth-weight, extremely preterm birth.  Arch Pediatr Adolesc Med. 2008;162(8):748-755
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Msall ME. Measuring outcomes after extreme prematurity with the Bayley-III Scales of Infant and Toddler Development: a cautionary tale from Australia.  Arch Pediatr Adolesc Med. 2010;164(4):391-393
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Duncan GJ, Dowsett CJ, Claessens A,  et al.  School readiness and later achievement [published correction appears in Dev Psychol. 2008;44(1):232].  Dev Psychol. 2007;43(6):1428-1446
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McClelland MM, Kessenich M, Morrison FJ. Pathways to early literacy: the complex interplay of child, family, and sociocultural factors.  Adv Child Dev Behav. 2003;31:411-447
PubMed
Saigal S, Szatmari P, Rosenbaum P, Campbell D, King S. Intellectual and functional status at school entry of children who weighed 1000 grams or less at birth: a regional perspective of births in the 1980s.  J Pediatr. 1990;116(3):409-416
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Resnick MB, Gueorguieva RV, Carter RL,  et al.  The impact of low birth weight, perinatal conditions, and sociodemographic factors on educational outcome in kindergarten.  Pediatrics. 1999;104(6):e74
PubMed  |  Link to Article   |  Link to Article
Roth J, Figlio DN, Chen Y,  et al.  Maternal and infant factors associated with excess kindergarten costs.  Pediatrics. 2004;114(3):720-728
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D’Angio CT, Sinkin RA, Stevens TP,  et al.  Longitudinal, 15-year follow-up of children born at less than 29 weeks' gestation after introduction of surfactant therapy into a region: neurologic, cognitive, and educational outcomes.  Pediatrics. 2002;110(6):1094-1102
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Hagen EW, Palta M, Albanese A, Sadek-Badawi M. School achievement in a regional cohort of children born very low birthweight.  J Dev Behav Pediatr. 2006;27(2):112-120
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Hansen BM, Dinesen J, Hoff B, Greisen G. Intelligence in preterm children at four years of age as a predictor of school function: a longitudinal controlled study.  Dev Med Child Neurol. 2002;44(8):517-521
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Hille ETM, den Ouden AL, Bauer L, van den Oudenrijn C, Brand R, Verloove-Vanhorick SP.Collaborative Project on Preterm and Small for Gestational Age (POPS) Infants in The Netherlands.  School performance at nine years of age in very premature and very low birth weight infants: perinatal risk factors and predictors at five years of age.  J Pediatr. 1994;125(3):426-434
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Hollomon HA, Dobbins DR, Scott KG. The effects of biological and social risk factors on special education placement: birth weight and maternal education as an example.  Res Dev Disabil. 1998;19(3):281-294
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Kirkegaard I, Obel C, Hedegaard M, Henriksen TB. Gestational age and birth weight in relation to school performance of 10-year-old children: a follow-up study of children born after 32 completed weeks.  Pediatrics. 2006;118(4):1600-1606
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McGrath MM, Sullivan MC, Lester BM, Oh W. Longitudinal neurologic follow-up in neonatal intensive care unit survivors with various neonatal morbidities.  Pediatrics. 2000;106(6):1397-1405
PubMed   |  Link to Article
Msall ME, Buck GM, Rogers BT, Merke D, Catanzaro NL, Zorn WA. Risk factors for major neurodevelopmental impairments and need for special education resources in extremely premature infants [published correction appears in J Pediatr. 1992;120(5):838].  J Pediatr. 1991;119(4):606-614
PubMed   |  Link to Article
Sell EJ, Gaines JA, Gluckman C, Williams E. Early identification of learning problems in neonatal intensive care graduates.  Am J Dis Child. 1985;139(5):460-463
PubMed
Short EJ, Klein NK, Lewis BA,  et al.  Cognitive and academic consequences of bronchopulmonary dysplasia and very low birth weight: 8-year-old outcomes.  Pediatrics. 2003;112(5):e359-e366
PubMed  |  Link to Article   |  Link to Article
Vohr BR, Garcia Coll CT. Neurodevelopmental and school performance of very low-birth-weight infants: a seven-year longitudinal study.  Pediatrics. 1985;76(3):345-350
PubMed
Yudkin PL, Aboualfa M, Eyre JA, Redman CWG, Wilkinson AR. New birthweight and head circumference centiles for gestational ages 24 to 42 weeks.  Early Hum Dev. 1987;15(1):45-52
PubMed   |  Link to Article
Schmidt B, Asztalos EV, Roberts RS, Robertson CMT, Sauve RS, Whitfield MF.Trial of Indomethacin Prophylaxis in Preterms (TIPP) Investigators.  Impact of bronchopulmonary dysplasia, brain injury, and severe retinopathy on the outcome of extremely low-birth-weight infants at 18 months: results from the Trial of Indomethacin Prophylaxis in Preterms.  JAMA. 2003;289(9):1124-1129
PubMed   |  Link to Article
Bayley N. Bayley Scales of Infant Development. 2nd ed. San Antonio, TX: Psychological Corp; 1993
Hauser RM, Warren JR. Socioeconomic indexes for occupations: a review, update, and critique.  Soc Methodology. 1997;27(1):177-298
Link to Article
Federal Financial Institutions Examination Council.  Geocoding system. Federal Financial Institutions Examination Council Web site. http://www.ffiec.gov/geocode/default.aspx. Accessed June 8, 2011
Woodcock RW, McGrew KS, Mather N. Woodcock-Johnson III Tests of Achievement. Itasca, IL: Riverside Publishing; 2001
Woodcock RW, McGrew KS, Mather N. Woodcock-Johnson III Tests of Cognitive Abilities. Itasca, IL: Riverside Publishing; 2001
Ohio Department of Education.  A Standards Guide for Families: What Is Expected in Grade K. Columbus: Ohio Dept of Education; 2003
Taylor HG, Anselmo M, Foreman AL, Schatschneider C, Angelopoulos J. Utility of kindergarten teacher judgments in identifying early learning problems.  J Learn Disabil. 2000;33(2):200-210
PubMed   |  Link to Article
Stoll BJ, Hansen NI, Bell EF,  et al; Eunice Kennedy Shriver National Institute of Child Health and Human Development Neonatal Research Network.  Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network.  Pediatrics. 2010;126(3):443-456
PubMed   |  Link to Article
Halsey CL, Collin MF, Anderson CL. Extremely low birth weight children and their peers: a comparison of preschool performance.  Pediatrics. 1993;91(4):807-811
PubMed
Woodward LJ, Moor S, Hood KM,  et al.  Very preterm children show impairments across multiple neurodevelopmental domains by age 4 years.  Arch Dis Child Fetal Neonatal Ed. 2009;94(5):F339-F344
PubMed   |  Link to Article
Nosarti C, Giouroukou E, Healy E,  et al.  Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome.  Brain. 2008;131(pt 1):205-217
PubMed
Volpe JJ. Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances.  Lancet Neurol. 2009;8(1):110-124
PubMed   |  Link to Article
Klebanov PK, Brooks-Gunn J, McCormick MC. School achievement and failure in very low birth weight children.  J Dev Behav Pediatr. 1994;15(4):248-256
PubMed   |  Link to Article
Taylor HG, Espy KA, Anderson PJ. Mathematics deficiencies in children with very low birth weight or very preterm birth.  Dev Disabil Res Rev. 2009;15(1):52-59
PubMed   |  Link to Article
Aarnoudse-Moens CSH, Oosterlaan J, Duivenvoorden HJ, van Goudoever JB, Weisglas-Kuperus N. Development of preschool and academic skills in children born very preterm.  J Pediatr. 2011;158(1):51-56
PubMed   |  Link to Article
Horwood LJ, Mogridge N, Darlow BA. Cognitive, educational, and behavioural outcomes at 7 to 8 years in a national very low birthweight cohort.  Arch Dis Child Fetal Neonatal Ed. 1998;79(1):F12-F20
PubMed   |  Link to Article
Sullivan MC, Margaret MM. Perinatal morbidity, mild motor delay, and later school outcomes.  Dev Med Child Neurol. 2003;45(2):104-112
PubMed   |  Link to Article
Allin M, Matsumoto H, Santhouse AM,  et al.  Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term.  Brain. 2001;124(pt 1):60-66
PubMed   |  Link to Article
Isaacs EB, Edmonds CJ, Lucas A, Gadian DG. Calculation difficulties in children of very low birthweight: a neural correlate.  Brain. 2001;124(pt 9):1701-1707
PubMed   |  Link to Article
Mulder H, Pitchford NJ, Marlow N. Processing speed and working memory underlie academic attainment in very preterm children.  Arch Dis Child Fetal Neonatal Ed. 2010;95(4):F267-F272
PubMed   |  Link to Article
Belsky J, MacKinnon C. Transition to school: developmental trajectories and school experiences.  Early Educ Dev. 1994;5(2):106-119
Link to Article

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