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. Author manuscript; available in PMC: 2012 Sep 1.
Published in final edited form as: Arch Pediatr Adolesc Med. 2011 Sep;165(9):819–825. doi: 10.1001/archpediatrics.2011.137

Learning Problems in Kindergarten Students with Extremely Preterm Birth

H Gerry Taylor 1, Nancy Klein 2, Marcia G Anselmo 3, Nori Minich 1, Kimberly A Espy 4, Maureen Hack 1
PMCID: PMC3298457  NIHMSID: NIHMS358756  PMID: 21893648

Abstract

Objective

To assess learning problems in extremely preterm children in kindergarten and identify risk factors.

Design

Cohort study.

Setting

Children’s hospital.

Participants

A cohort of extremely preterm children born January 2001 – December 2003 (n=148), defined as <28 weeks gestation and/or <1000 g birth weight, and term-born normal birth weight classmate controls (n=111).

Main Interventions

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

Main Outcome Measures

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

Results

The extremely preterm children had lower mean standard scores than controls on tests of spelling (8.52 points, 95% CI: 4.58, 12.46) and applied mathematics (11.02 points, 95% CI: 6.76, 15.28). They also had higher rates of substandard learning progress by teacher report in written language (OR = 4.23, 95% CI: 2.32, 7.73) and mathematics (OR = 7.08, 95% CI: 2.79, 17.95). Group differences on mathematics achievement and in teacher ratings of learning progress were 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 extremely preterm children, yet many of the children with problems were not in a special education program.

Conclusion

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


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

Unfortunately, we know little about the educational progress of EP children during this critical period of schooling. Several studies have documented academic difficulties at early school age on tests or teacher ratings of achievement.11,12,1424 However, this previous research has not examined the nature and predictors of learning problems in kindergarten. Knowledge regarding early academic outcomes is vital in appraising the educational needs of these children and their prospects for future learning problems.2529 Information on neonatal and early childhood factors related to poor achievement in kindergarten would also be useful in identifying the children most in need of careful monitoring.

Our primary objectives were to assess early learning progress in EP children compared with term-born normal birth weight (NBW) controls and examine associations of educational outcomes in the EP group with neonatal 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: (a) group differences would remain even when excluding children with more severe deficits20,30; (b) many children in the EP group with academic problems would not be receiving special assistance in school;10,31,32 and (c) 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

METHODS

PARTICIPANTS

Two hundred forty six children born with <28 weeks gestational age and/or <1000 g birth weight were admitted to the neonatal intensive care unit of Rainbow Babies & Children’s Hospital in Cleveland, Ohio during the period January 2001 – December 2003, excluding 8 infants with congenital infections or abnormalities. Of the 198 (80%) who survived, 148 (75%) were enrolled in the study. Reasons for non-participation included failure to locate families (21 cases), moves out of the region (16 cases), and refusals or no-shows (5 cases). Eight children could not be assessed due to custody issues or because they were non-English speaking. Comparison of participants with non-participants failed to reveal significant differences in ethnicity, sex, or neonatal risk factors. The children were followed longitudinally and contacted during their initial year in kindergarten. One hundred twenty nine EP children attended regular classrooms, 16 were in full-time special education programs, and 3 were home-schooled.

The EP group comprised 56 (38%) children had birth weight <750 g, 32 (22%) with gestation <25 weeks, and 37 (25%) with birth weight <10th percentile for gestational age.44 Neonatal complications included abnormal ultrasound defined as Grade III/IV intraventricular hemorrhage, periventricular leukomalacia, or ventricular dilatation at discharge (15, 10%); brochopulmonary dysplasia defined as supplemental oxygen at 36 weeks corrected age (77, 52%); infection and/or necrotizing enterocolitis (67, 45%); and severe retinopathopathy of prematurity defined as Stage 4 or 5 retinopathy or receipt of cryotherapy or laser therapy45 (27, 18%). At 20 months corrected age, 60 EP children (41%) had neurodevelopmental impairment defined as cerebral palsy (CP) (13, 9%), blindness or deafness (6, 4%), or a score <70 on the Mental Development Index of the Bayley Scales of Infant Development, 2nd Edition46 (57, 39%).

The control group consisted of 111 term-born NBW (>36 weeks gestational age, >2500 g) 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 age at assessment, sex, and ethnicity. Controls were not recruited for children who were home-schooled 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 finding matches.

There were no group differences in sex, ethnicity, or SES as defined by a mean of the sample 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 the 2000 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, as proportionally more EP children had been held back a year prior to kindergarten entry (22% vs. 3%, p<.001). Group comparisons also failed to reveal differences in age at testing, time in school when the teacher ratings were completed, or the percentage of children in full-day kindergartens (84% vs. 80%). Although a larger proportion of the EP group received early intervention services prior to school entry (83% vs. 13%, p<.001), the groups did not differ in rates of enrollment in preschool (84% vs. 85%) or daycare (49% vs. 51%).

Table 1.

Birth, Demographic, and School Entry Characteristics

Variable EP Group
(n = 148)
NBW Group
(n = 111)
Birth and Neonatal Data:
Birth weight in grams, Mean (SD)a 818.37 (174.01) 3382.25 (445.86)
Gestational age in weeks (SD) a 25.85 (1.64) >36 weeks
Multiple birth* 31 (21%) 0
Maternal Demographic Datab
  Married 69 (47%) 65 (59%)
  Education:
    <high school 20 (14%) 14 (13%)
      high school or GED 33 (22%) 16 (14%)
    >high school 95 (64%) 81 (73%)
  Median family income (SD)c 59.10 (32.37) 56.20 (23.67)
Child Status at School Entryd
African Americane 91 (61%) 61(55%)
Males (%) 68 (46%) 51(46%)
Age at kindergarten entry, mean years (SD)* 5.60 (.42) 5.43 (.30)
Age at testing, mean years (SD) 5.96 (.37) 5.96 (.31)
Months in school at testing* 4.25 (2.34) 6.38 (1.72)
Age at time of teacher rating of progress, mean years (SD)* 6.18 (.37) 6.03 (.31)
Months in school at teacher rating 7.16 (1.75) 7.11 (1.68)

Abbreviations: EP = extreme prematurity; NBW = term-born normal birth weight; Bayley Scales of Infant Development, 2nd Edition Mental Development Index; 46 GED = General Education Diploma.

a

Birth weight and gestational ages of NBW group based on maternal report; groups different by definition.

b

Refers to primary caregiver, which was the biologic or adoptive mother for 143 (97%) of the EP children and 105 (95%) of the NBW group.

c

Based on data on the neighborhood tract of the family residence from the 2000 US Census.48 Family income is in thousands of dollars.

d

The EP children and controls attended 113 different schools within 57 school districts located in the region surrounding Cleveland, Ohio.

e

All others Caucasian except for 4 Asian (2 in each group).

*

Significant group difference, p<.01.

PROCEDURES AND MEASURES

Children were administered tests of achievement and cognitive ability by examiners who were blinded to their birth status while their parents completed interviews and questionnaires to obtain information about family characteristics and children’s health status. Child tests were administered in a fixed order during a single session. Six EP children were untestable on most measures due to CP and severe cognitive impairment. Scores on achievement and intelligence measures for these children and others who were too low functioning to be tested were assumed to be <85. The research was approved by the University Hospitals Case Medical Center Institutional Review Board and written informed consents from parents and teachers were obtained prior to participation.

Achievement measures included the Letter/Word Identification, Spelling, Calculation, and Applied Problems subtests of the Woodcock Johnson Tests of Achievement, 3rd Edition.49 To take into account time in kindergarten, the scores on these tests were based on grade rather than age standards. Test reliability for these measures is good and validity has been documented in relation to other achievement tests. IQ was estimated using the age-standardized Brief Intelligence Assessment score (BIA) from the Woodcock Johnson Tests of Cognitive Ability, 3rd Edition.50

Teachers provided information on special education programs as defined by an Individual Educational Plan (IEP). IEPs were identified from parent report when teacher report was unavailable. Teachers of children attending regular classrooms also 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 over formal testing is that they provided information on children’s learning progress in specific areas of competency. Teachers were not informed of children’s birth status.

DATA ANALYSIS

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

Logistic regression was conducted to examine group differences in learning problems as defined by standard scores <85 on the achievement tests, substandard teacher ratings of learning progress (i.e., 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 ANCOVA. Time in school was controlled in analysis of IEPs as 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 CP, blindness or deafness, or low global cognitive ability as defined by BIA<85, group comparisons were repeated with these children excluded from analysis. To determine if these deficits were identifiable based on having an IEP, group comparisons were also re-run after excluding this subset of children. Associations of poor test performance and substandard learning progress with IEPs and classroom accommodations were investigated using chi-square analyses.

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

Bonferroni-corrected alpha levels were used to determine statistical significance, with adjustments on a family-wise basis within the domains of written language and mathematics. Thus, alpha level was .05/3=.017 for each of the three primary measures within each domain (i.e., two test scores and sum of teacher ratings for the ANCOVAs; and deficits on two tests and any indication of substandard learning progress for the logistic regressions). For the sample size, power was .80 with a two-sided alpha of .05 for detecting effect sizes of .33 and differences in event rates of 15%. Differences of at least this magnitude were anticipated based on previous research with similar samples.3

RESULTS

EP children had lower scores on Spelling and Applied Problems 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 NBW group was untestable or failed to reach basal levels of performance on Calculation (52% vs. 21%, p<.001). Even when excluding children with neurosensory disorders and/or BIA <85 (65 EP and 12 NBW), 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 significant when excluding children with IEPs.

Table 2.

Comparison of Extremely Preterm and Normal Birth Weight Groups on Measures of Achievement and Learning

EP Group NBW Group F (df) from 95% CI
Domain/Measure n Adj M (se) n Adj M (se) ANCOVA for difference
Written language:
 Letter/Word Identification 142 106.07 (1.13) 111 110.05 (1.28) 5.43 (1,248) 0.61, 7.33
 Spelling 140 92.09 (1.33) 111 100.61 (1.49) 18.12 (1,246) 4.58, 12.46**b
 Sum of teacher ratings of learning progress in written language 110 6.74 (0.26) 106 8.94 (0.27) 34.19 (1,211) 1.45, 2.93**ab
Mathematics:
  Calculation 69 102.40 (1.19) 88 105.46 (1.05) 3.72 (1,152) −0.07, 6.19b
  Applied Problems 140 95.10 (1.44) 111 106.12 (1.61) 26.95 (1,246) 6.76, 15.28**ab
  Sum of teacher ratings of learning progress in mathematics 110 4.95 (0.13) 106 5.83 (0.14) 21.42 (1,211) 0.51, 1.27**ab

Abbreviations: EP = extremely preterm; NBW = term-born normal birth weight; 95% CI = 95% confidence interval for difference (adjusted mean for NBW – adjusted mean for EP); Adj M (se) = adjusted mean (standard error); ANCOVA = analyses of covariance, adjusted for socioeconomic status, ethnicity, and sex.

Note: Achievement tests are from the Woodcock Johnson Tests of Achievement, 3rd Edition.49 Scores reported are grade standardized to take into account the time of year when testing occurred. With exception of Calculation, on which many children were untestable, lack of child cooperation accounted for reduced sample size on the achievement tests. Reduced sample sizes for the teacher ratings were related to the procedure of collecting ratings only from teachers of regular classrooms and a small number of teacher or school refusals.

a

Significant when excluding children with neurosensory disorders and/or a Brief Intelligence Assessment (BIA) <85 on the Woodcock Johnson Tests of Cognitive Abilities, 3rd Edition.50

b

Significant when excluding children with individual educational plans.

**

Bonferroni – adjusted p<.01.

Consistent with these results, the EP group had higher rates of poor test performance on Spelling and Applied Problems, substandard teacher ratings of learning progress, IEPs, and classroom accommodations (Table 3). Several group differences remained significant in analyses that excluded children with neurosensory deficits and/or BIA<85 or those with IEPs.

Table 3.

Comparison of Extremely Preterm and Normal Birth Weight Groups on Rates of Learning Problems, Individual Education Plans, and Classroom Accommodations

Outcome EP Group
No. (%)
NBW Group
No. (%)
Adjusted
OR (95% CI)
Deficit in written language:
  Letter/Word Identification <85 15/146 (10) 4/111 (4) 2.84 (0.90, 9.01)
  Spelling <85 48/145 (33) 10/111 (9) 5.43 (2.49, 11.86)*
  0 or 1 teacher ratings of progress in written language:
    Identifies letter names 32/110 (29) 5/106 (5) 8.21 (3.01, 22.41)**ab
    Identifies letter sounds 43/110 (39) 15/106 (14) 3.88 (1.95, 7.70) **b
    Identifies number of sounds in short words 58/110 (53) 25/106 (24) 3.65 (1.98, 6.73)**ab
    Answers questions about what has been read out loud to child 45/109 (41) 14/106 (13) 4.73 (2.33, 9.59)**ab
    Applies letter-sound correspond-dences to spell words 62/110 (56) 22/106 (21) 5.12 (2.73, 9.60)**ab
    Any 0 or 1 teacher rating 69/110 (63) 31/106 (29) 4.23 (2.32, 7.73)**ab
Deficit in mathematics:
  Calculation <85 20/85 (24) 9/89 (10) 2.68 (1.12, 6.45)
  Applied Problems <85 50/144 (35) 12/111 (11) 4.67 (2.24, 9.73)**
  0 or 1 teacher rating of progress in mathematics:
    Names numeral 1–10 26/110 (24) 4/105 (4) 7.97 (2.63, 24.11)**ab
    Counts objects 1–10 with 1-1 correspondence 26/110 (24) 3/106 (3) 10.29 (3.00, 35.31)**
    Matches numerals with set of objects 1–10 31/110 (28) 5/106 (5) 7.76 (2.86, 21.08)**ab
    Any 0 or 1 teacher rating 33/110 (30) 6/106 (6) 7.08 (2.79, 17.95)**ab
Individual education plan (IEP)c 61/147 (41) 12/111 (11) 4.53 (2.16, 9.47)**a
Classroom accommodationd 64/109 (59) 31/107 (29) 3.53 (1.95, 6.37)**a

Abbreviations: EP: extremely preterm; NBW: term-born normal birth weight; OR (95% CI) = odds ratio (95% confidence interval) as obtained from logistic regression. ORs are adjusted for socioeconomic status, ethnicity, and sex and reflect an increase in the likelihood of deficit in EP children vs. NBW controls.

Note: Achievement tests are from the Woodcock Johnson Tests of Achievement, 3rd Edition.49 <85 signifies standard scores more than 1 standard deviation below kindergarten standards and takes into account time of year when testing occurred.

a

Significant when excluding children with neurosensory disorders and/or a Brief Intelligence Assessment (BIA) <85.

b

Significant when excluding children with IEPs.

c

IEP classifications included Specific Learning Disability (23 EP, 4 NBW), Speech or Language Impairment (19 EP, 6 NBW), Other Health Impaired (3 EP), Multiple Disabilities (5 EP), Preschooler with Disability (3 EP), Autism (1 EP), Mental Retardation (1 EP), Orthopedic Impairment (2 EP), Hearing Impairment (1 EP), Visual Impairment (1 EP), Emotional Disturbance (1 NBW), and Related Services (1 NBW). The classification for two EP children could not be determined, one because of inadequate information and a second because of placement in a private school for children with special needs.

d

The EP group also had significantly higher rates of each type of accommodation, including reduced assignments, alternative ways of testing, individual assistance from an adult besides the teacher, different grading criteria, individual teaching or modified instructions, and classroom modifications such as special seating.

**

Bonferroni-adjusted p<.01.

Children with IEPs and classroom accommodations had higher rates of poor test performance on all achievement tests and of substandard learning progress in both written language and mathematics (all p’s<.05). However, 26 of 70 EP children (37%) with a score <85 on one or more of the 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 BIA ≥85 (n = 14, 28%) than a neurosensory deficit and/or BIA <85 (n = 12, 60%, p = .012). Low-achieving EP children without an IEP also had significantly higher scores on Spelling and Applied Problems and lower rates of gestation <25 weeks, abnormal ultrasounds, and neurodevelopment impairment at 20 months than those with an IEP.

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

Table 4.

Neonatal and Early Childhood Risk Factors Significantly Related to Learning Problems in Extremely Preterm Group

Learning Problem Risk Factor Risk
Present
No. (%)
Risk
Absent
No. (%)
Adjusted
OR (95% CI)
Letter/Word Identification <85: NDIa 11/58 (19) 3/85 (4) 5.90 (1.48, 23.44)*
AbnUS 4/15 (27) 11/131 (8) 6.18 (1.45, 26.36)*
Spelling <85: NDI 33/57 (58) 14/85 (16) 5.88 (2.55, 13.55)**
AbnUS 8/15 (53) 40/130 (31) 6.79 (1.60, 28.69)*
SESb 0.40 (.68, .24)**
0 or 1 teacher ratings of progress in written language: SES 0.44 (.69, .28)**
Calculation <85: NDI 17/30 (57) 3/54 (6) 29.06 (6.14, 137.54)**
Applied Problems <85: NDI 33/57 (58) 14/84 (17) 5.48 (2.40, 12.53)**
AbnUS 8/15 (53) 42/129 (33) 6.61 (1.55, 28.23)*
SES 0.39 (.66, .23)**
Individual education plan (IEP): NDI 40/59 (68) 19/85 (22) 6.82 (2.56, 18.16)**
AbnUS 11/15 (73) 50/132 (38) 21.42 (2.67, 171.89)**
BPD 40/77 (52) 21/69 (30) 2.71 (1.14, 6.45)*c
NI 31/60 (52) 30/87 (34) 2.62 (1.07, 6.40)*
GA<25 weeks 23/32 (72) 38/115 (33) 5.49 (1.89, 15.95)**c
SES 0.62 (.97, .40)*
Classroom accommodation:d NDI 33/42 (79) 30/65 (46) 4.15 (1.57, 11.02)**
BPD 38/54 (70) 25/54 (46) 2.77 (1.19, 6.49)*c
GA<25 weeks 18/23 (78) 46/86 (53) 3.20 (1.00, 10.21)*c
SES 0.63 (.93, .43)*

Abbreviations: EP: extremely preterm; OR (95% CI) = odds ratio (95% confidence interval) as obtained from logistic regression; SES = socioeconomic status. ORs are adjusted for SES, ethnicity, and sex and reflect an increase in the odds of the specified learning problem with the risk factor being present; NDI = neurodevelopmental impairment as defined by a neurosensory disorder and/or Mental Development Index <70 on the Bayley Scales of Infant Development, 2nd Edition at 20 months corrected age;46 AbnUS = abnormal cranial ultrasound; BPD = bronchopulmonary dysplasia; NI = neonatal infection; GA = gestational age.

Note: Achievement tests are from the Woodcock Johnson Tests of Achievement, 3rd Edition.49 <85 signifies standard scores more than 1 standard deviation below kindergarten standards, taking into account the number of months a child is in kindergarten.

a

Data missing for 3 children in group with EP.

b

ORs for SES reflect a decrease in the odds of the specified learning problem given a 1 SD increase in SES.

c

Significant when excluding children with NDI.

d

Classroom accommodations include reduced assignments, ways of testing, individual assistance from an adult besides the teacher, different grading criteria, individual teaching or modified instructions, and classroom modifications such as special seating.

*

Bonferroni-adjusted p<.05;

**

Bonferroni-adjusted p<.01.

COMMENT

Current survival of EP children has reached a level previously unsurpassed but with high rates of neonatal morbidity.53 As increasing numbers of these children are reaching school age, it is critical that we identify the problems they have at school entry and factors related to early educational difficulties. Our results reveal that the EP children performed more poorly on achievement tests, were making less learning progress, and had higher rates of IEPs and classroom accommodations than NBW controls. Academic problems were evident on tests of written expression and mathematics and in teacher ratings of learning progress in these areas. A recent report of academic outcomes in 6-year-olds of ≤33 weeks gestation born in the 1990s 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.20 Our results suggest similar outcomes for children born in the 2000s. Although other studies have reported deficiencies in academic readiness or beginning achievement skills in preterm children,12,18,20,21,23,54,55 to our knowledge this is the first study to demonstrate the pervasiveness of learning deficiencies during the first year in school among EP children born since 2000. Because the EP and NBW groups were similar in sociodemographic characteristics, neonatal brain insults and subsequent abnormalities in neural development may contribute in large part to their higher rates of educational difficulties.56,57

This study is also 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, yet 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, low cognitive ability, and neonatal complications than those with an IEP, suggesting that children with less severe impairments are more likely to be under-identified. 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 fully met.

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

Neonatal risk factors associated with learning problems of EP children in kindergarten included gestation <25 weeks, abnormal cranial ultrasounds, bronchopulmonary dysplasia, and infection. Neurodevelopmental impairment at 20 months and lower SES also predicted learning problems. Previous studies have reported similar risks for deficits in school readiness skills and special education interventions.3,18,19,31,32,34,36,37,3943,61,62 These risk factors may thus have utility in identifying the children most deserving of developmental monitoring and early childhood interventions prior to school entry.

A limitation of this study was that teacher ratings of educational progress were only obtained for EP children attending regular classrooms. This procedure was warranted to insure 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 on IEPs was provided by teachers and parents and we had no means to determine 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 25% of the families. The sample was predominantly urban and African American and, although largely reflective of EP births within the region, not representative of the U.S. as a whole. Educational interventions may also vary from those provided elsewhere in the U.S. Because of privacy issues parents of NBW children were selected from among those who agreed to be contacted, introducing possible bias in selection of controls. However, the children attended a multitude of schools throughout the region, there were no differences in background factors between participants and non-participants or between the EP and NBW groups, and our results are similar to previous reports of early educational outcomes.20,21,30

Although poorer reading skills in older school-age children are associated with reduced cerebellar volume and mathematics difficulties with reduced gray matter in the left parietal lobe,63,64 further studies are need to investigate the neural basis of early academic difficulties in EP children and examine the cognitive and behavior problems associates with these difficulties. Deficits in specific skill areas, such as processing speed and working memory, may be closely related 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 also needed to identify characteristics of families and schools that buffer or exacerbate early learning progress.29,66

In conclusion, our findings reveal high rates of learning problems and special learning interventions in 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 findings also underscore the fact that many EP children with learning problems in kindergarten are not receiving special interventions, and they show 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,” may be especially helpful in insuring early detection and intervention.26

ACKNOWLEDGEMENTS

This work was funded by grant HD050309 from the National Institutes of Health, which provided financial support for the design and conduct of the study; collection, management, analysis, and interpretation of the data; and preparation, review, or approval of the manuscript. As principal investigator, 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. All authors have contributed substantively to the conceptualization and design of the study and interpretation of findings. Drs. Taylor and Hack played major roles in preparing the first draft of the manuscript. Dr. Klein led efforts to obtain data from teachers. In addition to her contributing to study design, Dr. Espy developed procedures for recruiting controls. Ms. Anselmo designed the teacher ratings and was instrumental in our decision to focus on children’s performance at school entry. Ms. Minich developed and executed the analytic plan. None of the authors have any conflicts of interest and all authors have critically reviewed and approved this manuscript for submission. We gratefully acknowledge the assistance of Anne Birnbaum, Dr. Elizabeth Roth, Dan Maier, Andrea Barkoukis Gefteas, Michelle R. Jacobs, Alice Kostiuc, and Ketrin Lengu in recruitment, data collection and coding.

RERFERENCES

  • 1.Anderson P, Doyle LW the Victorian Infant Collaborative Study Group. Neurobehavioral outcomes of school-age children born extremely low birth weight or very preterm in the 1990s. JAMA. 2003;289(24):3264–3272. doi: 10.1001/jama.289.24.3264. [DOI] [PubMed] [Google Scholar]
  • 2.Saigal S, Doyle LW. An overview of mortality and sequelae of preterm birth from infancy to adulthood. Lancet. 2008;271(9608):261–269. doi: 10.1016/S0140-6736(08)60136-1. [DOI] [PubMed] [Google Scholar]
  • 3.Taylor HG, Klein N, Drotar D, Schluchter M, Hack M. Consequences and risks for <1000-g birth weight for neuropsychological skills, achievement, and adaptive functioning. J Dev Behav Pediatr. 2006;27(6):459–469. doi: 10.1097/00004703-200612000-00002. [DOI] [PubMed] [Google Scholar]
  • 4.Aylward GP. Neurodevelopmental outcomes of infants born prematurely. J Dev Behav Pediatr. 2005;26(6):427–440. doi: 10.1097/00004703-200512000-00008. [DOI] [PubMed] [Google Scholar]
  • 5.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. doi: 10.1046/j.1440-1754.2002.00039.x. [DOI] [PubMed] [Google Scholar]
  • 6.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. doi: 10.1136/adc.2008.152793. [DOI] [PubMed] [Google Scholar]
  • 7.Saigal S, den Ouden L, Wolke D, et al. School-age outcomes in children who were extremely low birth weight from four international population-based cohorts. Pediatrics. 2003;112(4):943–950. doi: 10.1542/peds.112.4.943. [DOI] [PubMed] [Google Scholar]
  • 8.Bohm 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. doi: 10.1080/08035250410021379. [DOI] [PubMed] [Google Scholar]
  • 9.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. doi: 10.1097/DBP.0b013e31819e6a16. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 10.Litt J, Taylor HG, Klein N, Hack M. Learning disabilities in children with very low birth weight: Prevalence, neuropsychological correlates, and educational interventions. J Learn Disabil. 2005;38(2):130–141. doi: 10.1177/00222194050380020301. [DOI] [PubMed] [Google Scholar]
  • 11.Marlow N, Hennessy EM, Bracewell MA, Wolke D the EPICure Study Group. Motor and executive function at 6 years of age after extremely preterm birth. Pediatrics. 2007;120(4):793–804. doi: 10.1542/peds.2007-0440. [DOI] [PubMed] [Google Scholar]
  • 12.Wolke D, Samara M, Bracewell M, Marlow N. Specific difficulties and school achievement in children born at 25 weeks of gestation or less. J Pediatr. 2008;152(2):256–262. doi: 10.1016/j.jpeds.2007.06.043. [DOI] [PubMed] [Google Scholar]
  • 13.Avchen RN, Scott KG, Mason CA. Birth weight and school-age disabilities: A population-based study. Am J Epidemiol. 2001;154(10):895–901. doi: 10.1093/aje/154.10.895. [DOI] [PubMed] [Google Scholar]
  • 14.Caravale B, Tozzi C, Albino G, Vicari S. Cognitive development in low risk preterm infants at 3–4 years of life. Arch Dis Child Fetal Neonatal Ed. 2005;90(6):F474–F479. doi: 10.1136/adc.2004.070284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Klein N. Children who were very low birthweight: Cognitive abilities and classroom behavior at 5 years of age. J Spec Educ. 1988;22(1):41–54. [Google Scholar]
  • 16.Larroque B, Ancel P-Y, Marret S, et al. Neurodevelopmental disabilities and special care of 5-year-old children born before 33 weeks of gestation (the EPIPAGE study): A longitudinal cohort study. Lancet. 2008;371(9615):813–820. doi: 10.1016/S0140-6736(08)60380-3. [DOI] [PubMed] [Google Scholar]
  • 17.Mikkola K, Ritari N, Tommiska V, et al. Neurodevelopmental outcomes 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. doi: 10.1542/peds.2005-0171. [DOI] [PubMed] [Google Scholar]
  • 18.Partrianakos-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. doi: 10.1542/peds.2008-1771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Patrianakos-Hoobler A, 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. doi: 10.1111/j.1469-8749.2009.03343.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.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. doi: 10.1016/j.earlhumdev.2008.10.004. [DOI] [PubMed] [Google Scholar]
  • 21.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. [Google Scholar]
  • 22.van Baar AL, van Wassenaer AG, Briet JM, Dekker FW, Kok JH. Very preterm birth is associated with disabilities in multiple developmental domains. J Pediatr Psychol. 2005;30(3):247–255. doi: 10.1093/jpepsy/jsi035. [DOI] [PubMed] [Google Scholar]
  • 23.Vohr BR, Msall ME. Neuropsychological and functional outcomes of very low birth weight infants. Sem Perinatol. 1997;21(3):202–220. doi: 10.1016/s0146-0005(97)80064-x. [DOI] [PubMed] [Google Scholar]
  • 24.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(1):94–109. doi: 10.1017/s0012162299000201. [DOI] [PubMed] [Google Scholar]
  • 25.High PC the Committee on Early Childhood, Adoption, and Dependent Care and Council on School Health. School readiness. Pediatrics. 2008;121(4):e1008–e1015. doi: 10.1542/peds.2008-0079. [DOI] [PubMed] [Google Scholar]
  • 26.Hintz SR, Kendrick DE, Vohr GR, Poole WK, Higgins RD. Community supports after surviving extremely low-birth-weight, extremely preterm birth. Arch Pediatr Adolesc Med. 2008;162(8):748–755. doi: 10.1001/archpedi.162.8.748. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Msall M. Measuring outcomes after extreme prematurity with the Bayley-III scales of infant and toddler development. Arch Pediatr Adolesc Med. 2010;164(4):391–393. doi: 10.1001/archpediatrics.2010.25. [DOI] [PubMed] [Google Scholar]
  • 28.Duncan GJ, Dowsett DJ, Clasessens A, et al. School readiness and later achievement. Dev Psychol. 2007;43(6):1428–1446. doi: 10.1037/0012-1649.43.6.1428. [DOI] [PubMed] [Google Scholar]
  • 29.McClelland MM, Kessenich M, Morrison FJ. Pathways to early literacy: The complex interplay of the child, family, and sociocultural factors. Adv Child Dev Behav. 2003;31:411–447. doi: 10.1016/s0065-2407(03)31010-9. [DOI] [PubMed] [Google Scholar]
  • 30.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. doi: 10.1016/s0022-3476(05)82835-5. [DOI] [PubMed] [Google Scholar]
  • 31.Resnick MB, Gueorguieva RV, Carter RL, et al. The impact of low birth weight, prenatal conditions, and sociodemographic factors on educational outcome in kindergarten. Pediatrics. 1999;104(6):e74. doi: 10.1542/peds.104.6.e74. [DOI] [PubMed] [Google Scholar]
  • 32.Roth J, Figlio DN, Chen Y, et al. Maternal and infant factors associated with excess kindergarten costs. Pediatrics. 2004;114(3):720–728. doi: 10.1542/peds.2003-1028-L. [DOI] [PubMed] [Google Scholar]
  • 33.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. doi: 10.1542/peds.110.6.1094. [DOI] [PubMed] [Google Scholar]
  • 34.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. doi: 10.1097/00004703-200604000-00005. [DOI] [PubMed] [Google Scholar]
  • 35.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. doi: 10.1017/s0012162201002481. [DOI] [PubMed] [Google Scholar]
  • 36.Hille ETM, Den Ouden AL, Bauer L, van de Oudenrijn C, Brand R, Verloove-Vanhorick SP. 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. Pediatrics. 1994;125(3):426–434. doi: 10.1016/s0022-3476(05)83290-1. [DOI] [PubMed] [Google Scholar]
  • 37.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. doi: 10.1016/s0891-4222(98)00002-x. [DOI] [PubMed] [Google Scholar]
  • 38.Kirkegaard I, Obel C, Hedegaard M, Henriksen T. 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. doi: 10.1542/peds.2005-2700. [DOI] [PubMed] [Google Scholar]
  • 39.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. doi: 10.1542/peds.106.6.1397. [DOI] [PubMed] [Google Scholar]
  • 40.Msall ME, Buck GM, Rogers BT, Merke D, Catanzaro NL, Zorn WA. Risk factors for major neurodevelopmnental impairments and need for special education resources in extremely premature infants. J Pediatr. 1991;119(4):606–614. doi: 10.1016/s0022-3476(05)82415-1. [DOI] [PubMed] [Google Scholar]
  • 41.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. doi: 10.1001/archpedi.1985.02140070034025. [DOI] [PubMed] [Google Scholar]
  • 42.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. doi: 10.1542/peds.112.5.e359. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.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] [Google Scholar]
  • 44.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. doi: 10.1016/0378-3782(87)90099-5. [DOI] [PubMed] [Google Scholar]
  • 45.Schmidt B, Asztalos EV, Roberts RS, Robertson CMT, Sauve RS, Whitfield MF. 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. doi: 10.1001/jama.289.9.1124. [DOI] [PubMed] [Google Scholar]
  • 46.Bayley N. Bayley Scales of Infant Development. 2nd ed. San Antonio, TX: Psychological Corporation; 1993. [Google Scholar]
  • 47.Hauser RM, Warren JR. Socioeconomic indexes for occupations: A review, update, and critique. Socio Meth. 1997;27:177–298. [Google Scholar]
  • 48.Federal Financial Institutions Examinations Council Geocoding System. [Accessed January 1, 2010–November 1, 2010]; http://www.ffiec.gov/Geocode/default.htm.
  • 49.Woodcock RW, McGrew KS, Mather N. Woodcock-Johnson III Tests of Achievement. Itasca, IL: Riverside: 2001. [Google Scholar]
  • 50.Woodcock RW, McGrew KS, Mather N. Woodcock-Johnson III Tests of Cognitive Abilities. Itasca, IL: Riverside: 2001. [Google Scholar]
  • 51.Ohio Department of Education. A standards guide for families: What is expected in grade K. Columbus, OH: Author; 2004. [Google Scholar]
  • 52.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. doi: 10.1177/002221940003300208. [DOI] [PubMed] [Google Scholar]
  • 53.Stoll BJ, Hansen NI, Bell EF, et al. Neonatal outcomes of extremely preterm infants from the NICHD Neonatal Research Network. Pediatrics. 2010;126(3):443–456. doi: 10.1542/peds.2009-2959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Halsey CL, Collin MF, Anderson CL. Extremely low birth weight children and their peers: A comparison of preschool performance. Pediatrics. 1993;91(5):807–811. [PubMed] [Google Scholar]
  • 55.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. doi: 10.1136/adc.2008.146282. [DOI] [PubMed] [Google Scholar]
  • 56.Nosarti C, Giouroukou E, Healy E, et al. Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. Brain. 2008;131(1):205–217. doi: 10.1093/brain/awm282. [DOI] [PubMed] [Google Scholar]
  • 57.Volpe J. Brain injury in premature infants: A complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2009;8(1):110–124. doi: 10.1016/S1474-4422(08)70294-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 58.Klebanov PK, Brooks-Gunn J, McCormick MC. School achievement and failure in very low birthweight children. J Dev Behav Pediatr. 1994;15(2):248–256. [PubMed] [Google Scholar]
  • 59.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. doi: 10.1002/ddrr.51. [DOI] [PubMed] [Google Scholar]
  • 60.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. 2010;158(1):15–20. doi: 10.1016/j.jpeds.2010.06.052. [DOI] [PubMed] [Google Scholar]
  • 61.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. doi: 10.1136/fn.79.1.f12. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Sullivan MC, McGrath MM. Perinatal morbidity, mild motor delay, and later school outcomes. Dev Med Child Neurol. 2003;45(2):104–112. [PubMed] [Google Scholar]
  • 63.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(1):60–66. doi: 10.1093/brain/124.1.60. [DOI] [PubMed] [Google Scholar]
  • 64.Isaacs EB, Edmonds CJ, Lucas A, Gadian DG. Calculation difficulties in children of very low birthweight. Brain. 2001;124(9):1701–1707. doi: 10.1093/brain/124.9.1701. [DOI] [PubMed] [Google Scholar]
  • 65.Mulder H, Pitchford N, 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. doi: 10.1136/adc.2009.167965. [DOI] [PubMed] [Google Scholar]
  • 66.Belsky J, MacKinnon C. Transition to school: Developmental trajectories and school experiences. Early Educ Dev. 1994;5(2):106–119. [Google Scholar]

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