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School-age outcomes of late preterm infants in New York City

      Objective

      This study compares school-age outcomes among preterm (PT) (32 0/7-<34 weeks), late PT (LP) (34 0/7-<37 weeks), and full-term (FT) infants to assess cognitive sequelae of LP births.

      Study Design

      We obtained linked birth and educational data for all nonanomalous singleton infants born 1994 through 1998 in New York City who had a third-grade standardized test score (n = 215,138).

      Results

      Children delivered LP and PT had 30% and 50% higher adjusted odds of needing special education than those delivered FT (adjusted odds ratio, 1.34; 95% confidence interval, 1.29–1.40; and adjusted odds ratio, 1.53; 95% confidence interval, 1.30–1.69). They also had lower adjusted math and English scores than those delivered FT (math: 7% and 10% of SD, respectively; English: 4% and 6% of SD). A linear association between gestational age and test scores was seen through 39 weeks' gestation.

      Conclusion

      There is a significant risk of developmental differences in PT and LP infants compared with FT infants.

      Key words

      Despite multiple interventions to reduce the rate of preterm (PT) delivery, the PT birth rate has continued to increase over the past decade.
      • Martin J.A.
      • Hamilton B.E.
      • Sutton P.D.
      • et al.
      Births: final data for 2007.
      Most of this increase is among infants born toward the end of the PT period, at 34-36 completed weeks of gestation, during the time known as late PT (LP).
      • Martin J.A.
      • Kirmeyer S.
      • Osterman M.
      • Shepherd R.A.
      • et al.
      Born a bit too early: recent trends in late preterm births.
      • Davidoff M.J.
      • Dias T.
      • Damus K.
      • et al.
      Changes in the gestational age distribution among US singleton births: impact on rates of late preterm birth, 1992 to 2002.
      The rate of LP births increased 20% from 1990 through 2006 and accounted for >70% of all singleton PT deliveries in the United States during that time period.
      • Martin J.A.
      • Hamilton B.E.
      • Sutton P.D.
      • et al.
      Births: final data for 2007.
      For Editors' Commentary, see Table of Contents
      See related editorial, page 191
      Mounting evidence has shown that infants born LP are less healthy than infants born at term. They are more likely than term infants to suffer from mortality
      • Pulver L.S.
      • Guest-Warnick G.
      • Stoddard G.J.
      • Byington C.L.
      • Young P.C.
      Weight for gestational age affects the mortality of late preterm infants.
      and short-term morbidity such as increased temperature instability, hypothermia, hypoglycemia, hyperbilirubinemia, rehospitalization, and respiratory distress.
      • Wang M.L.
      • Dorer D.J.
      • Fleming M.P.
      • Catlin E.A.
      Clinical outcomes of near-term infants.
      • Engle W.A.
      • Tomashek K.M.
      • Wallman C.
      Committee on Fetus and Newborn American Academy of Pediatrics
      “Late-preterm” infants: a population at risk.
      Evidence has also suggested that infants born LP have similar risks of adverse neonatal morbidities as PT infants delivered at 32-33 weeks and 6 days' gestation.
      • Bastek J.A.
      • Sammel M.D.
      • Paré E.
      • Srinivas S.K.
      • Posencheg M.A.
      • Elovitz M.A.
      Adverse neonatal outcomes: examining the risks between preterm, late preterm, and term infants.
      Recent studies also suggest that risks decrease as gestation increases, even up to 39 completed weeks of gestation.
      • Morse S.B.
      • Zheng H.
      • Tang Y.
      • Roth J.
      Early school-age outcomes of late preterm infants.
      • Moster D.
      • Lie R.T.
      • Markestad T.
      Long-term medical and social consequences of preterm birth.
      • Chyi L.J.
      • Lee H.C.
      • Hintz S.R.
      • Gould J.B.
      • Sutcliffe T.L.
      School outcomes of late preterm infants: special needs and challenges for infants born at 32 to 36 weeks gestation.
      • Cheng Y.W.
      • Nicholson J.M.
      • Nakagawa S.
      • Bruckner T.A.
      • Washington A.E.
      • Caughey A.B.
      Perinatal outcomes in low-risk term pregnancies: do they differ by week of gestation?.
      • Talge N.M.
      • Holzman C.
      • Wang J.
      • Lucia V.
      • Gardiner J.
      • Breslau N.
      Late-preterm birth and its association with cognitive and socioemotional outcomes at 6 years of age.
      In 2005, the National Institute of Child Health and Human Development called for research regarding long-term morbidity for LP births as there is a paucity of data on long-term neurodevelopmental status.
      • Raju T.N.
      • Higgins R.D.
      • Stark A.R.
      • Leveno K.J.
      Optimizing care and outcome for late-preterm (near-term) infants: a summary of the workshop sponsored by the National Institute of Child Health and Human Development.
      One study suggests that long-term health risks may include cerebral palsy, significantly higher rates of developmental delay and disability, and disorders of psychological development, behavior, and emotion.
      • Petrini J.R.
      • Dias T.
      • McCormick M.C.
      • Massolo M.L.
      • Green N.S.
      • Escobar G.J.
      Increased risk of adverse neurological development for late preterm infants.
      However, a significant knowledge gap remains about the educational outcomes of the large population of LP and PT infants once they reach school age.
      • Morse S.B.
      • Zheng H.
      • Tang Y.
      • Roth J.
      Early school-age outcomes of late preterm infants.
      We performed a retrospective cohort study to evaluate school-age educational outcomes among singleton LP infants compared with outcomes of PT and full-term (FT) infants. Differences in outcomes between PT and FT births and the impact of advancing gestational age in weeks on mean test score achievement were also examined. We hypothesized that school-age outcomes of LP infants would be significantly better than outcomes of PT infants, and significantly worse than those of FT infants.

      Materials and Methods

      The study population was drawn from the Longitudinal Study of Early Development data warehouse, which was constructed using probabilistic linkage technology to join child records from the New York City Department of Health and Mental Hygiene (DOHMH) Bureau of Vital Statistics birth and death certificates; the DOHMH Early Intervention Program and Lead Poisoning Prevention Program registries; and New York City Department of Education (DOE) enrollment, special education, and achievement data.
      • Pfeiffer M.R.
      • Mavinkurve M.
      • Slopen M.E.
      • Sedlar S.
      Creation of a child-centric inter-agency data warehouse: the Longitudinal Study of Early Development Statistics Canada 2010 International Methodology Symposium.
      The warehouse was constructed using probabilistic linkage software (Quality Stage; IBM, Armonk, NY) to link records based on values for identifiers including the child's name, date of birth, sex, address, social security number, mother's name and date of birth, and father's name. Final samples were reviewed to verify a low false match rate (<1%).
      • Jaro M.A.
      Probabilistic linkage of large public health data files.
      Our study population included 215,138 children born 1994 through 1998 to mothers residing in New York City. We included all nonanomalous singleton infants who were delivered from 32 0/7-42 0/7 weeks' gestation and were enrolled at DOE in grade 3. This cohort represents 47% of the eligible sample in New York City at birth as children who moved before beginning school, enrolled in private school, were homeschooled, or died were not part of the data set. Additionally, children who were born outside of New York City but who were enrolled in New York City public schools were excluded because their birth information was not available. Clinical estimate of gestational age came from the birth certificate, where it is reported in weeks and days. Exposure was defined as gestational age at delivery, which was classified into 3 groups: 32 0/7-33 6/7 weeks (PT), 34 0/7-36 6/7 weeks (LP), and ≥37 0/7 weeks (FT). Children recorded as having an Individualized Education Plan at any time <2007 (aged 9-13 years) were identified as having an educational disability necessitating special education services. Cognitive outcomes were assessed using standardized scores from DOE-administered third-grade English Language Arts (ELA) and math tests. These scores reflect mastery of the curriculum in math and ELA, and are used to measure performance within students over time as well as across students, schools, and school districts in all nonspecialized public schools in New York City. To permit comparisons across instruments and to facilitate interpretation of effect sizes, we transformed all test scores to z-scores by the child's year of birth.
      Maternal demographic and pregnancy characteristics, as well as birth outcomes of the child, all obtained from birth records, were examined as covariates and potential confounders. Maternal demographic characteristics included age (<20, 20-35, >35 years), level of education (≤high school, >high school), employment at the time of birth, race/ethnicity, insurance status, and parity (nulliparous or multiparous). Pregnancy characteristics included tobacco use during pregnancy, presence of any maternal medical risk factors (anemia, cardiac disease, lung disease, gestational diabetes, chronic diabetes, chronic hypertension, previous PT or small for gestational age infant, and/or renal disease), any complication of labor and delivery (preeclampsia, eclampsia, placenta previa, seizures during labor, cord prolapse, placental abruption, and/or fetal distress), and mode of delivery (vaginal or cesarean).
      We controlled for whether the child was born at <10th percentile of birthweight for gestational age based on sex-specific US standard birthweights,
      • Oken E.
      • Kleinman K.P.
      • Rich-Edwards J.
      • Gillman M.W.
      A nearly continuous measure of birth weight for gestational age using a United States national reference.
      reported need for neonatal intensive care, 5-minute Apgar score (<7, ≥7), and infant sex. We also included days absent in third grade (from the DOE records) as a covariate in our models to account for the direct relationship between attendance and test scores.

      Statistical analysis

      Criteria for significance were set at alpha <0.05 for all analyses. We assessed bivariate relationships between categorized gestational age and all other variables using the χ2 statistic. We also examined bivariate relationships between each outcome variable and all potential predictor variables. Logistic regression was used to determine the odds that a child needed special education, and generalized linear models were constructed to assess the impact of gestational age category and of gestational age in weeks on test score achievement. We then assessed the effect of gestational age in continuous weeks on mean test scores adjusting for maternal characteristics, pregnancy characteristics, and birth outcomes, and determined the gestational age at which the relationships no longer hold. The multivariable models included all hypothesized covariates found to be significantly associated with test scores (chisq P < .05). All analyses were conducted using software (SAS System, version 9.2; SAS Institute, Cary NC). This study was approved by the New York City DOHMH Institutional Review Board.

      Results

      Of the 215,138 infants in the study, 2332 (1.1%) were PT, 13,207 (6.1%) were LP, and 199,599 (92.8%) were FT. Baseline characteristics of our study sample, stratified by gestational age category, are presented in Table 1. Maternal race/ethnicity differed between all comparison groups as did tobacco use (both P < .001). There were a higher proportion of black, non-Hispanic women delivering PT than LP, and LT than FT. Similarly, tobacco use was more prevalent among mothers with PT than LT deliveries and those with LT than FT babies. The maternal demographic and pregnancy characteristics of the PT group were similar to the LP group for the majority of the other covariates, and the LP group differed significantly from the FT group. The proportion of women with complications of labor and delivery was significantly higher in the PT compared with the LP group and the LP group compared with women who delivered FT infants (24.9% vs 16.0% and 16.0% vs 7.8%).
      TABLE 1Characteristics by gestational age at delivery
      CharacteristicPT 32-<34 wk (n = 2332)LP 34-<36 wk (n = 13,207)FT 37-42 wk (n = 199,599) (%)
      (%)PT vs LP, P value(%)LP vs FT, P value
      Maternal age, y.64.003
       <2015.214.612.8
       20-3566.167.872.8
       >3518.717.614.4
      Maternal education.13< .0001
       ≤HS34.636.633.1
       >HS60.759.463.9
      Mother's employment.24< .0001
       Employed25.924.829.3
       Not employed74.173.070.7
      Race/ethnicity< .0001< .0001
       Black, non-Hispanic46.139.831.8
       White, non-Hispanic10.612.316.6
       Hispanic35.038.439.8
       Asian/PI6.88.510.9
       Other0.80.60.5
      Insurance status.78.27
       Medicaid65.165.963.7
       HMO8.07.99.1
       Other third party18.417.020.2
       Self7.16.64.8
       Unknown2.22.62.2
      Parity.98.0005
       Nulliparous29.729.731.1
       Multiparous70.370.368.9
      Tobacco.0002< .0001
       Yes13.010.45.8
       No87.089.694.2
      Medical risk factors
      Anemia, cardiac disease, lung disease, gestational diabetes, chronic diabetes, chronic hypertension, previous PT or small for gestational age infant, and/or renal disease;
      .77< .0001
       Yes14.614.38.2
       No85.485.791.8
      Complications of labor and delivery
      Preeclampsia, eclampsia, placenta previa, seizures during labor, cord prolapse, placental abruption, and/or fetal distress.
      < .0001< .0001
       Yes24.916.07.8
       No75.184.092.2
      Mode of delivery< .0001< .0001
       Vaginal65.475.178.4
       Cesarean section33.323.620.1
      FT, full term; HMO, health maintenance organization; HS, high school; LP, late preterm; PI, Pacific Islander; PT, preterm.
      Lipkind. School-age outcomes of late preterm infants. Am J Obstet Gynecol 2012.
      a Anemia, cardiac disease, lung disease, gestational diabetes, chronic diabetes, chronic hypertension, previous PT or small for gestational age infant, and/or renal disease;
      b Preeclampsia, eclampsia, placenta previa, seizures during labor, cord prolapse, placental abruption, and/or fetal distress.
      Table 2 presents the birth outcomes of PT, LP, and FT infants in our study population. The mean gestational age of delivery was 32.5 weeks in the PT group, 35.4 weeks in the LP group, and 39.4 weeks in the FT group. All covariates differed significantly for infants born PT as compared with LP and LP as compared with FT except for infant sex, which was similar between the PT and LP groups.
      TABLE 2Birth characteristics by gestational age at delivery
      VariablePT 32-<34 wk (n = 2332)LP 34-<36 wk (n = 13,207)FT 37-42 wk (n = 199,599) (%)
      (%)PT vs LP, P value(%)LP vs FT, P value
      SGA 10th percentile.001< .0001
       Yes14.116.714.3
       No85.983.385.8
      NICU admission< .0001< .0001
       Yes56.624.65.4
       No32.459.975.7
      5-min Apgar <7< .0001< .0001
       Yes3.71.50.5
       No96.398.599.5
      Infant sex.22.0004
       Male50.348.350.1
       Female49.751.749.9
      FT, full term; LP, late preterm; NICU, neonatal intensive care unit; PT, preterm; SGA, small for gestational age.
      Lipkind. School-age outcomes of late preterm infants. Am J Obstet Gynecol 2012.
      Table 3 presents the results of logistic and linear modeling of the school-age outcomes by gestational age category. The unadjusted rate of the need for special education was 28.9% in the PT group, 25.4% in the LP group, and 19.1% in the FT group. After adjusting for child sex, maternal age, maternal race/ethnicity, insurance status, parity, low Apgar score, medical risk factors, complications of labor and delivery, neonatal intensive care unit admission, days absent in third grade, and small for gestational age <10th percentile, children who were delivered LP had 30% higher adjusted odds of needing special education (adjusted odds ratio [aOR], 1.34; 95% confidence interval [CI], 1.29–1.40) compared with FT infants, and children who delivered PT had 50% higher adjusted odds of needing special education (aOR, 1.53; 95% CI, 1.30–1.69) compared with FT infants. There was a small but increased risk in the need for special education in PT infants as compared with LP infants (aOR, 1.14; 95% CI, 1.03–1.27).
      TABLE 3School-age outcomes by gestational age at delivery
      VariableSpecial education recommendation
      z-scores adjusting for child sex, maternal age, maternal race/ethnicity, insurance status, parity, low Apgar score, medical risk factors, complications of pregnancy, neonatal intensive care admission, days absent in third grade, and small for gestational age <10th percentile.
      Adjusted math test score
      z-scores adjusting for child sex, maternal age, maternal race/ethnicity, insurance status, parity, low Apgar score, medical risk factors, complications of pregnancy, neonatal intensive care admission, days absent in third grade, and small for gestational age <10th percentile.
      Adjusted ELA test score
      z-scores adjusting for child sex, maternal age, maternal race/ethnicity, insurance status, parity, low Apgar score, medical risk factors, complications of pregnancy, neonatal intensive care admission, days absent in third grade, and small for gestational age <10th percentile.
      OR (95% CI)SD % (95% CI)SD % (95% CI)
      PT vs FT1.53 (1.30–1.69)–10.4% (–14.3 to –6.5)–5.7% (–9.7 to –1.7)
      LP vs FT1.34 (1.29–1.40)–6.7% (–8.4 to –5.1)–4.0% (–5.7 to –2.3)
      PT vs LP1.14 (1.03–1.27)–3.8% (–7.9 to 4.0)–2.0% (–6.2 to 2.3)
      CI, confidence interval; ELA, English Language Arts; FT, full term; LP, late preterm; OR, odds ratio; PT, preterm.
      Lipkind. School-age outcomes of late preterm infants. Am J Obstet Gynecol 2012.
      a z-scores adjusting for child sex, maternal age, maternal race/ethnicity, insurance status, parity, low Apgar score, medical risk factors, complications of pregnancy, neonatal intensive care admission, days absent in third grade, and small for gestational age <10th percentile.
      Children who delivered LP had 6.7% of SD lower adjusted math scores and 4.0% of SD lower adjusted ELA scores than those who delivered FT (both P < .001). Children who delivered PT had 10.4% of SD lower adjusted math test scores and 5.7% of SD lower adjusted ELA test scores compared with children who were delivered FT (both P < .001). There were no significant differences in adjusted test scores between children who delivered PT and LP.
      Generalized linear models estimated increases in ELA and math test scores of 0.73% (P < .0001) and 0.12% (P < .0001) of SD, respectively, for each 1-week increase in gestational age after adjusting for the same variables as our logistic and linear models. The Figure depicts mean ELA and math test scores by weeks' gestation, adjusted for covariates. The linear trends observed in the Figure flatten out between 39-40 weeks' gestation for both ELA and math. Although the overall trend was linear, nonlinear trends were seen between 33-34 weeks and again at 40-42 weeks. However, these differences were small and not statistically significant.
      Figure thumbnail gr1
      FIGUREAdjusted mean test scores (z-score) by completed weeks' gestation
      Lipkind. School-age outcomes of late preterm infants. Am J Obstet Gynecol 2012.

      Comment

      This study adds to the small but growing body of literature that demonstrates significant long-term developmental differences in both PT and LP infants compared with FT infants. We found both PT and LP infants have higher odds of needing special education and lower third-grade test scores than FT infants, but we found no statistical difference in test scores between PT and LP infants. There is a slightly increased odds of needing special education among PT infants compared with LP infants. Linear trends in test scores with increasing gestational age leveled off >39 weeks' gestation.
      Children born LP and PT had adjusted ELA scores 4% of SD and 6% of SD lower, respectively, than their FT peers. The effect on math scores was even greater, at 7% of SD and 10% of SD. In educational research, effect sizes between 5-10% of SD are considered small but not trivial, and an effect size of 10% is viewed as considerable.
      • Vernez G.
      • Zimmer R.
      Interpreting the effects of Title I supplemental educational services Prepared for the US Department of Education, under review at US Department of Education 2007.
      • Konstantopoulos S.
      • Chung V.
      What are the long-term effects of small classes on the achievement gap? Evidence from the Lasting Benefits Study.
      The average effect size of educational interventions is 7% of SD.
      • Hill C.J.
      • Bloom H.S.
      • Black A.R.
      • Lipsey M.W.
      Empirical benchmarks for interpreting effect sizes in research.
      Our findings, documenting differences between LP and FT infants with regard to need for special education, and lower math and ELA test scores, are consistent with the findings from the 3 other published studies on this topic. Specifically, Morse et al
      • Morse S.B.
      • Zheng H.
      • Tang Y.
      • Roth J.
      Early school-age outcomes of late preterm infants.
      found that the risk for developmental delay, suspension in kindergarten, educational disability in prekindergarten, and retention in kindergarten were all increased among healthy LP infants compared with FT infants. Chyi et al
      • Chyi L.J.
      • Lee H.C.
      • Hintz S.R.
      • Gould J.B.
      • Sutcliffe T.L.
      School outcomes of late preterm infants: special needs and challenges for infants born at 32 to 36 weeks gestation.
      found children born LP to be at increased risk for special education and to have lower first-grade reading scores than their FT counterparts, but found no difference in first-grade math scores. Talge et al
      • Talge N.M.
      • Holzman C.
      • Wang J.
      • Lucia V.
      • Gardiner J.
      • Breslau N.
      Late-preterm birth and its association with cognitive and socioemotional outcomes at 6 years of age.
      found that LP birth was associated with behavioral problems and lower intelligence quotient at the age of 6 years, independent of maternal intelligence quotient, residential setting, and sociodemographics in comparison with term infants. Our work confirms these findings and demonstrates a linear relationship between gestational age and standardized test scores that continues through 39 weeks' gestation.
      As expected, we also found increased odds of needing special education among PT infants compared with those born FT. It is also interesting that the odds of needing special education among children born PT are very similar to the LP group. This may point to the need for children born LP to be monitored as closely as PT infants so that they can benefit from earlier detection and remediation of conditions associated with a future need for special education.
      Our findings have biological plausibility given that considerable brain development occurs in the last 4 weeks of gestation. It is estimated that at 35 weeks' gestation, the surface of the brain shows significantly fewer sulci, and the weight of the brain is only 60% that of FT infants. Over the final 4 weeks of gestation, dramatic growth has been seen in the sulci, gyri, synapses, dendrites, astrocytes, and microglia.
      • Kinney H.C.
      The near-term (late preterm) human brain and risk for periventricular leukomalacia: a review.
      Our study adds to the literature suggesting negative outcomes for LP births, finding that test scores increased with each advancing week of gestation between 32-39 weeks. Although we were able to control for mode of delivery, complications of labor and delivery, and maternal medical risk factors, our study is limited because we were unable to examine specific delivery indications associated with delivery timing. In 2009, Holland et al
      • Holland M.G.
      • Refuerzo J.S.
      • Ramin S.M.
      • Saade G.R.
      • Blackwell S.C.
      Late preterm birth: how often is it avoidable?.
      examined a cohort of women who delivered in a large tertiary care hospital to describe indications for LP birth and found that up to 17% were potentially avoidable. The long-term consequences of LP delivery must be balanced against the risks of stillbirth if delivery is delayed, as the recent increase nationally in LP birth has also been associated with a decline in stillbirth and neonatal mortality.
      • Ananth C.V.
      • Joseph K.S.
      • Oyelese Y.
      • Demissie K.
      • Vintzileos A.M.
      Trends in preterm birth and perinatal mortality among singletons: United States, 1989 through 2000.
      • Donovan E.F.
      • Besl J.
      • Paulson J.
      • Rose B.
      • Iams J.
      Ohio Perinatal Quality Collaborative
      Infant death among Ohio resident infants born at 32 to 41 weeks of gestation.
      Further research on the implications of delaying delivery for both indicated and spontaneous PT delivery needs to be conducted, and long-term outcomes for specific maternal and fetal indications need to be explored.
      Our findings are important for clinical management of individual children, but also from the perspective of population health. To the extent that LP children do not reach their full academic potential, or require additional educational services that might have been avoided, the practice of delivering children early when they could be delivered later may represent a larger societal burden than previously recognized.
      There are other limitations to our study. As this was a retrospective study based on birth certificate data, misclassification of gestational age may have occurred in some cases. However, several studies have shown that obstetric/clinical estimates of gestational age provide a good approximation to menstrual dating.
      • Ananth C.V.
      Menstrual versus clinical estimate of gestational age dating in the United States: temporal trends and variability in indices of perinatal outcomes.
      Our study was limited to New York City public school children who completed citywide standardized testing in either ELA or math when in third grade. This group may differ from children enrolled in public school who were exempt or absent from testing (<1%), and from children who attend private schools. Our data also do not capture families who move either in or out of New York City. We do not know the extent to which the population composition of our sample biases our results and how to extrapolate these results to the entire population of LP infants in New York City.
      Despite these limitations, we report the largest cohort in the literature that examines school-age outcomes of LP deliveries. Our research found that later delivery is associated with higher test scores throughout the gestational age range until 39 weeks' gestation. The decision to deliver a 34- to 38 6/7-week infant should be made carefully, with consideration of many potential long-term risks, including educational school-age outcomes. When a PT birth is considered, the intellectual development of the child through the life course should be included in the risk/benefit analysis of delivery timing.

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