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Severe small size for gestational age and cognitive function: catch-up phenomenon possible

      Objective

      We sought to compare cognitive functioning in children born with birthweight <3% vs ≥3% for gestational age (GA) between 9 months and kindergarten.

      Study Design

      Nonanomalous singletons from the Early Childhood Longitudinal Study–Birth Cohort were included. Associations between weight for GA and cognitive functioning were examined using a series of confounder-adjusted general linear models.

      Results

      Of 3633 cohorts, 585 (16%) were <3% for GA. At 9 months, cognitive performance of newborns <3% was about 12 percentile points lower than their normal counterparts (P < .001). By 2 years, however, no significant cognitive differences between these groups were observed (P = .668). Academic performance at preschool age (around 3.5 years) was not different for reading (P = .245) or math (P = .880), nor different at kindergarten age.

      Conclusion

      Newborns <3% for GA exhibit catch-up cognitive functioning by 2 years, with relatively no decrements in academic functioning observed by kindergarten.

      Key words

      Severe small size for gestational age (SGA), defined as birthweight <3% for gestational age (GA), is linked with neonatal morbidity such as neonatal seizures, proven sepsis, need for intubation, retinopathy, and mortality within 28 days of birth.
      American College of ObstetriciansGynecologists
      Intrauterine growth restriction: ACOG practice bulletin no. 12.
      • McIntire D.D.
      • Bloom S.L.
      • Casey B.M.
      • Leveno K.J.
      Birth weight in relation to morbidity and mortality among newborn infants.
      • Garite T.J.
      • Clark R.
      • Thorp J.A.
      Intrauterine growth restriction increases morbidity and mortality among premature neonates.
      Additionally, the Practice Bulletin Intrauterine Growth Restriction from the American Congress of Obstetricians and Gynecologists (ACOG) acknowledges that while normal infants with SGA will exhibit “catch-up” growth by 2 years, they are at 2-fold increased risk for major neurologic sequelae. The link between abnormal growth and cognitive delay is based on a comparison of 714 neonates of appropriate size for age with 347 SGA neonates, derived from several studies.
      American College of ObstetriciansGynecologists
      Intrauterine growth restriction: ACOG practice bulletin no. 12.
      The potential problem with linking neurologic sequelae with suboptimal growth is that the neurologic sequelae vary across studies, as do the definitions of growth restriction and the assessments used for neurologic or cognitive functioning. Thus, there is a need to reassess the association between growth restriction and cognitive development using consistent standardized measurements and methods.
      For Editors' Commentary, see Contents
      The purpose of this study was to utilize the nationally representative Early Childhood Longitudinal Study–Birth Cohort (ECLS-B) data to determine if newborns at <3% for GA, when compared to those ≥3%, are at risk for sustained cognitive deficits and subsequent problems with academic achievement. For this analysis we sought to assess the difference between <3% vs ≥3% because the likelihood of morbidity is significantly greater when birthweight is <3% rather than 4-10%.
      • McIntire D.D.
      • Bloom S.L.
      • Casey B.M.
      • Leveno K.J.
      Birth weight in relation to morbidity and mortality among newborn infants.

      Materials and Methods

      The ECLS-B (US Department of Education) is a national multisource, multimethod study, conducted by the National Center for Education Statistics, designed to evaluate the influences on children's early development, school readiness, and early academic performance. The sample was drawn from children born in 2001, with an oversampling of specific minority groups (eg, American Indian and Asian and Pacific Islander infants), low birthweight infants, and twins, which allowed for more statistical power in examining outcomes related to these subpopulations. Births were sampled using a 2-stage cluster-based system developed by the National Center for Health Statistics.
      US Department of Education
      Early childhood longitudinal study, birth cohort, 9 month data collection.
      It uses a nationwide cluster sampling strategy of birth certificate data to select a representative sample of infants born in 2001. The ECLS-B utilized an oversampling strategy that included low and very low birthweight infants, creating an overall sample that allowed for more statistical power in examining outcomes related to these subpopulations. Participants were followed through their kindergarten year, with data collection waves occurring at 9 months, 2 years, 3.5 years, and 5 years.
      During the 9-month and 2-year visits, participants were administered the research edition of the Bayley Scales of Infant Development (BSID). This test of early child cognitive and motor development is age-normed and designed for children from early infancy to 3 years of age. It produces 2 subscale scores: the Motor score taps fine and gross motor skills; and the Mental (MNT) score taps expressive and receptive language, reasoning and problem-solving, and emotion regulation. Since the focus of our study was cognitive function, we used the MNT score in analyses.
      Generally, tests of abilities or characteristics must show a consistency in measurement within the test and between administrations of the tests, with coefficients measuring these criteria being considered good when above a threshold of about 0.70. Within the ECLS-B, the research edition of the BSID demonstrated good internal reliability (MNT score, coefficient alpha = 0.78-0.93) as well as good test-retest reliability (MNT score, r = 0.83). Correlations between the BSID and the McCarthy Scales of Children's Abilities,
      US Department of Education
      Early childhood longitudinal study, birth cohort: methodology report for the 9-month data collection, vol 1 Psychometric characteristics.
      another well-regarded early childhood cognitive assessment, ranged from 0.57–0.79.
      At the preschool (3.5 years) and kindergarten (5 years) waves of the ECLS-B, participants were administered direct cognitive tests that tapped early reading and math abilities. These cognitive assessments were developed for the ECLS-B using item-response theory and adaptive testing to allow for accurate measurement of children with widely varying abilities. The reading portion of this assessment taps basic skills, vocabulary, global understanding of context, interpretation of stories, and overall comprehension. The math portion of the assessment taps sense of numbers, measurement, spatial sense, understanding of probability, and identification of patterns. As the ECLS-B team developed these tests,
      US Department of Education
      Early childhood longitudinal study, birth cohort: preschool-kindergarten psychometric report.
      several rounds of testing and refinement were used to generate tests that ultimately showed good internal consistency (reading reliability coefficient = 0.84-0.93; math = 0.89-0.92).
      From the birth certificate, GA and birthweight were obtained. Using the normative birthweight conversion tables published by Oken et al,
      • 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.
      birthweight for GA was calculated as a percentile for each case. We did not use the more frequently cited national reference published by Alexander et al
      • Alexander G.R.
      • Himes J.H.
      • Kaufman R.B.
      • Mor J.
      • Kogan M.
      A United States national reference for fetal growth.
      because it categorized newborns as <5% or <10% for GA, and not <3%, the threshold for significantly higher neonatal morbidity.
      • McIntire D.D.
      • Bloom S.L.
      • Casey B.M.
      • Leveno K.J.
      Birth weight in relation to morbidity and mortality among newborn infants.
      A series of multivariate general linear models (GLM) that adjusted for the complex sampling design of the ECLS-B were fitted to examine the overall differences in developmental trajectories of cognitive functioning between newborns with weight <3% vs ≥3% for GA. Additional univariate GLM at each time point were used to explore this further. All models were adjusted to control for child race (categorized as Caucasian, African American, Hispanic, and other), child sex, maternal education (years of school), maternal socioeconomic status (a composite index of occupational status, income, and education), and prematurity. All analyses were conducted using the standard and complex samples modules of SPSS software (version 19; SPSS Inc, Chicago, IL). Because the ECLS-B dataset used in this study contains no information that can be used to identify subjects, the Institutional Review Board at Eastern Virginia Medical School reviewed this study and determined that it does not fall under human subjects research regulatory requirements.

      Results

      The ECLS-B sampled 13,921 live births in 2001 and 10,688 newborns completed the first major data collection point, when the child was 9 months old. A subsampling scheme determined by the ECLS-B study team yielded a total of 6420 children who completed the kindergarten wave, which represents a 5-year retention rate of 74% for the selected subsample. We excluded 2787 newborns for the following reasons: 1643 twins, 599 with incomplete birth certificate data, 516 missing cognitive and academic data, and 29 anomalous. There were no significant differences in SGA rates between cases retained and lost to follow-up (16% vs 15.8%; P = .72). Our final sample size for analysis was 3633 children (Figure 1).
      Figure thumbnail gr1
      FIGURE 1Case selection
      F/U, follow-up.
      *1643 twins, 599 with incomplete birth certificate data, 516 who were missing data, and 29 anomalous newborns.
      Paulson. Catch-up phenomenon in SGA. Am J Obstet Gynecol 2012.
      Among the 3633 children, 51% were male with a racial distribution of: 42% (1516) white, 15% (567) Asian, 15% (554) Hispanic, 14% (497) African American, and 14% (499) others. Preterm births comprised 9.2% of our sample and 16% (581) were SGA, consistent with the ECLS-B oversampling strategy. Among infants who were SGA, 8.4% were born <37 weeks' gestation, vs 1.7% among newborns with weight of ≥3% (P < .001). Moreover, severe SGA children were more likely to have 5-minute Apgar scores <7 (1.3%) than those with weight of 3% or more (0.6%; P = .038). No differences were observed between severe SGA and children who weighed >3% for GA on race/ethnicity, maternal age, or route of delivery (Table 1). Comparisons between severe SGA vs newborns >3% indicate significantly poorer cognitive functioning (by 12 percentile points) at age 9 months, but no significant differences in cognitive or academic performance at later time points (Table 2).
      TABLE 1Sample characteristics
      CharacteristicBW <3% for GA, n = 581BW ≥3% for GA, n = 3025P value
      Maternal age, y28.7 (28.2–29.3)29.3 (29.0–29.5)
       <192.0% (22)
      Actual cell counts reported. Percentages and χ2 reflect weighted rates.
      1.8% (80).767
       19-3475.8% (436)78.0% (2343)
       ≥3522.2% (127)20.2% (633)
      Ethnicity
       African American15.7% (118)12.1% (379).155
       Caucasian54.4% (270)61.3% (1246)
       Hispanic19.1% (84)17.8% (470)
       Asian6.5% (66)3.9% (501)
       Other4.2% (47)5.0% (452)
      GA, wk37.6 (37.4–37.9)39.4 (39.37–39.52)
       24-2800.1% (30)< .001
       29-322.3% (58)0.4% (73)
       33-342.9% (72)0.4% (21)
       34-363.1% (45)0.7% (28)
       ≥3791.6% (410)98.3% (2835)
      Route of delivery
       Vaginal74.1% (347)76.1% (2284).536
       Cesarean25.9% (237)23.9% (729)
      Apgar score at 5 min
       <71.3% (27)0.6% (41).038
       ≥798.7% (558)99.4% (2987)
      Data presented as % (n) or means and 95% confidence intervals (for maternal age and GA).
      BW, birthweight; GA, gestational age.
      Paulson. Catch-up phenomenon in SGA. Am J Obstet Gynecol 2012.
      a Actual cell counts reported. Percentages and χ2 reflect weighted rates.
      TABLE 2Cognitive function
      VariableBW <3% for GA, n = 581BW ≥3% for GA, n = 3025P value
      BSID Mental
       9 mo42.754.7< .001
       2 y47.548.7.668
      Early reading ability
       Preschool48.751.4.245
       Kindergarten52.051.7.880
      Early math ability
       Preschool48.749.4.803
       Kindergarten47.650.6.211
      Data are presented as age-adjusted percentile scores. All model results are adjusted for child race, child sex, maternal education, and maternal socioeconomic status.
      BSID, Bayley Scales of Infant Development; BW, birthweight; GA, gestational age.
      Paulson. Catch-up phenomenon in SGA. Am J Obstet Gynecol 2012.
      A series of multivariable GLM were constructed to evaluate differences between children who were <3% vs ≥3% for GA at 9 months, 2 years, preschool, and kindergarten. These models accounted for the complex sampling design and weighting used in the ECLS-B. At the age of 9 months, severe SGA infants' cognitive performance was, on average, 12 percentile points lower than that of their normal counterparts (P < .001). By 2 years, however, no significant cognitive differences between these groups were observed (P = .67). Similarly, academic performance at preschool age (around 3.5 years) was not different for reading (P = .24) or math (P = .88). By kindergarten, no differences were evident between SGA and normal groups for reading (P = .803) or math (P = .21). Across all models, the interaction between prematurity and SGA was tested but found to be nonsignificant. To visualize this pattern of differences, all scores were standardized to a mean of 0 and SD of 1 (z-score transformation) and were plotted across time and between <3% vs ≥3% for GA (Figure 2).
      Figure thumbnail gr2
      FIGURE 2Cognitive functioning of newborns <3% vs ≥3% for gestational age
      Data presented as z-scores, with mean = 0, SD = 1.
      Paulson. Catch-up phenomenon in SGA. Am J Obstet Gynecol 2012.
      Post hoc sample size calculations indicates that the sample size of 3633 permitted 0.80 power at alpha of 0.05 to detect differences as small as about 3.5 percentile points around typical (50th percentile) performance, with greater sensitivity at extreme values.

      Comment

      The US Department of Education's National Center for Education Statistics in the Institute of Education Sciences, in collaboration with other education and health policy agencies, sponsored ECLS-B, a prospective nationally longitudinal study, which focuses on children born in 2001 and followed up from birth to kindergarten. The program provides national data on children's status at birth and at various points thereafter.
      • Snow K.
      • Derechoaa A.
      • Wheeless S.
      • et al.
      Early childhood longitudinal study, birth cohort (ECLS-B), kindergarten 2006 and 2007 data file user's manual (2010-010).
      • Woythaler M.A.
      • McCormick M.C.
      • Smith V.C.
      Late preterm infants have worse 24-month neurodevelopmental outcomes than term infants.
      The data from the study were previously used to compare the neurodevelopment outcomes of late vs term births,
      • Woythaler M.A.
      • McCormick M.C.
      • Smith V.C.
      Late preterm infants have worse 24-month neurodevelopmental outcomes than term infants.
      ascertain association between maternal mood disorder and childhood attachment,
      • Huang Z.J.
      • Lewin A.
      • Mitchell S.J.
      • Zhang J.
      Variations in the relationship between maternal depression, maternal sensitivity, and child attachment by race/ethnicity and nativity: findings from a nationally representative cohort study.
      ascertain the role of maternity leave on the duration of breast-feeding,
      • Ogbuanu C.
      • Glover S.
      • Probst J.
      • Liu J.
      • Hussey J.
      The effect of maternity leave length and time of return to work on breastfeeding.
      and assess the relationship between maternal prepregnancy body mass index to Hispanic preschooler overweight/obesity.
      • Kitsantas P.
      • Pawloski L.R.
      • Gaffney K.F.
      Maternal prepregnancy body mass index in relation to Hispanic preschooler overweight/obesity.
      Considering the generalizability of the data, and the rigorous nature of data collection, we used ECLS-B to assess the cognitive development of children who at birth were <3% vs ≥3% for GA.
      Our analysis indicates that, compared to newborns with weight of ≥3% for GA, severe SGA newborns have significant relative deficits in cognitive functioning at 9 months but their performance demonstrates a catch-up phenomenon by 2 years (Table 2 and Figure 2). Reading and math abilities were similar among these 2 groups at preschool and kindergarten. Our finding of cognitive catch-up phenomena contradicts some earlier reports
      • Agostoni C.
      Small-for-gestational-age infants need dietary quality more than quantity for their development: the role of human milk.
      • Geva R.
      • Eshel R.
      • Leitner Y.
      • Fattal-Valevski A.
      • Harel S.
      Verbal short-term memory span in children: long-term modality dependent effects of intrauterine growth restriction.
      • Geva R.
      • Eshel R.
      • Leitner Y.
      • Valevski A.F.
      • Harel S.
      Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study.
      • Leitner Y.
      • Fattal-Valevski A.
      • Geva R.
      • et al.
      Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study.
      • Petersen S.G.
      • Wong S.F.
      • Urs P.
      • Gray P.H.
      • Gardener G.J.
      Early onset, severe fetal growth restriction with absent or reversed end-diastolic flow velocity waveform in the umbilical artery: perinatal and long-term outcomes.
      • Smedler C.
      • Faxelius G.
      • Bremme K.
      • Lagerstrom M.
      Psychological development in children born with very low birth weight after severe intrauterine growth retardation: a 10-year follow-up study.
      • Hadders-Algra M.
      • Touwen B.C.
      Body measurements, neurological and behavioral development in six-year-old children born preterm and/or small-for-gestational-age.
      and an ACOG Practice Bulletin on the topic,
      American College of ObstetriciansGynecologists
      Intrauterine growth restriction: ACOG practice bulletin no. 12.
      which noted persistence of neurologic impairment among SGA, but are consistent with other publications.
      • Slykerman R.F.
      • Thompson J.M.
      • Clark P.M.
      • et al.
      Determinants of developmental delay in infants aged 12 months.
      • Campos M.
      • Reyes G.
      • García L.
      Comparison of postdischarge growth in adequate for gestational age and small for gestational age very low birthweight infants.
      • Bassan H.
      • Stolar O.
      • Geva R.
      • et al.
      Intrauterine growth-restricted neonates born at term or preterm: how different?.
      The potential explanations for the contradictory findings between the various studies are small sample size in some,
      • Leitner Y.
      • Fattal-Valevski A.
      • Geva R.
      • et al.
      Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study.
      • Petersen S.G.
      • Wong S.F.
      • Urs P.
      • Gray P.H.
      • Gardener G.J.
      Early onset, severe fetal growth restriction with absent or reversed end-diastolic flow velocity waveform in the umbilical artery: perinatal and long-term outcomes.
      cohorts of the growth-restricted newborns being mostly preterm
      • Petersen S.G.
      • Wong S.F.
      • Urs P.
      • Gray P.H.
      • Gardener G.J.
      Early onset, severe fetal growth restriction with absent or reversed end-diastolic flow velocity waveform in the umbilical artery: perinatal and long-term outcomes.
      rather than term, and different measures of neurologic functions. Hadders-Algra and Touwen,
      • Hadders-Algra M.
      • Touwen B.C.
      Body measurements, neurological and behavioral development in six-year-old children born preterm and/or small-for-gestational-age.
      for example, evaluated mild problems with coordination and fine motor skills deficits while we utilized a more standardized test for cognitive functioning and early academic ability.
      There are various strengths of the study that merit mentioning. Unlike earlier reports,
      • Kitsantas P.
      • Pawloski L.R.
      • Gaffney K.F.
      Maternal prepregnancy body mass index in relation to Hispanic preschooler overweight/obesity.
      • Agostoni C.
      Small-for-gestational-age infants need dietary quality more than quantity for their development: the role of human milk.
      • Geva R.
      • Eshel R.
      • Leitner Y.
      • Fattal-Valevski A.
      • Harel S.
      Verbal short-term memory span in children: long-term modality dependent effects of intrauterine growth restriction.
      • Geva R.
      • Eshel R.
      • Leitner Y.
      • Valevski A.F.
      • Harel S.
      Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study.
      • Leitner Y.
      • Fattal-Valevski A.
      • Geva R.
      • et al.
      Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study.
      • Petersen S.G.
      • Wong S.F.
      • Urs P.
      • Gray P.H.
      • Gardener G.J.
      Early onset, severe fetal growth restriction with absent or reversed end-diastolic flow velocity waveform in the umbilical artery: perinatal and long-term outcomes.
      • Smedler C.
      • Faxelius G.
      • Bremme K.
      • Lagerstrom M.
      Psychological development in children born with very low birth weight after severe intrauterine growth retardation: a 10-year follow-up study.
      our cohorts were selected from across the country, thus, our findings are generalizable geographically within the United States. The tests used to assess cognitive functioning in this study are widely accepted
      • Alexander G.R.
      • Himes J.H.
      • Kaufman R.B.
      • Mor J.
      • Kogan M.
      A United States national reference for fetal growth.
      • Snow K.
      • Derechoaa A.
      • Wheeless S.
      • et al.
      Early childhood longitudinal study, birth cohort (ECLS-B), kindergarten 2006 and 2007 data file user's manual (2010-010).
      • Woythaler M.A.
      • McCormick M.C.
      • Smith V.C.
      Late preterm infants have worse 24-month neurodevelopmental outcomes than term infants.
      • Huang Z.J.
      • Lewin A.
      • Mitchell S.J.
      • Zhang J.
      Variations in the relationship between maternal depression, maternal sensitivity, and child attachment by race/ethnicity and nativity: findings from a nationally representative cohort study.
      • Ogbuanu C.
      • Glover S.
      • Probst J.
      • Liu J.
      • Hussey J.
      The effect of maternity leave length and time of return to work on breastfeeding.
      and have good internal consistency.
      US Department of Education
      Early childhood longitudinal study, birth cohort: methodology report for the 9-month data collection, vol 1 Psychometric characteristics.
      Since the investigators administering the tests were probably unaware of the SGA status and the hypothesis of our study, the likelihood of bias is minimal. The post hoc calculation suggests that our sample size is sufficient to detect differences as small as about 3.5 percentile points around typical (50th percentile) performance. Our population was ethnically diverse with only 42% being white (Table 1). Lastly, we adjusted for maternal education and maternal socioeconomic status, as well as child's race and sex.
      Limitations of our studies should be acknowledged. We defined SGA as <3% as McIntire et al
      • McIntire D.D.
      • Bloom S.L.
      • Casey B.M.
      • Leveno K.J.
      Birth weight in relation to morbidity and mortality among newborn infants.
      did but not <10%, as ACOG does.
      American College of ObstetriciansGynecologists
      Intrauterine growth restriction: ACOG practice bulletin no. 12.
      Our reasons for selecting <3% for GA as the threshold for SGA were that if there is cognitive delay it is more likely to be among these newborns rather than those with birthweight ≥3%. Over 90% of newborns were at least 37 weeks, thus our findings may have limited applicability to preterm SGA. We do not have the data on whether these newborns were detected antenatally or had surveillance,
      • Manning F.A.
      • Bondaji N.
      • Harman C.R.
      • et al.
      Fetal assessment based on fetal biophysical profile scoring, VIII: the incidence of cerebral palsy in tested and untested perinates.
      which may influence cognitive function. Considering most
      • Mattioli K.P.
      • Sanderson M.
      • Chauhan S.P.
      Inadequate identification of small-for-gestational-age fetuses at an urban teaching hospital.
      SGA are undetected, we are uncertain on how the findings apply to children who underwent antepartum surveillance. Since we excluded multiple gestation, our findings do not apply to them, although the risk of SGA among twins has been noted to be as high as 47%.
      • Fox N.S.
      • Rebarber A.
      • Klauser C.K.
      • Roman A.S.
      • Saltzman D.H.
      Intrauterine growth restriction in twin pregnancies: incidence and associated risk factors.
      From the data it is difficult to ensure the GA but it is noteworthy that ECLS-B has been utilized to ascertain neurodevelopment outcomes of late vs term births.
      • Snow K.
      • Derechoaa A.
      • Wheeless S.
      • et al.
      Early childhood longitudinal study, birth cohort (ECLS-B), kindergarten 2006 and 2007 data file user's manual (2010-010).
      We acknowledge that we could not differentiate if the severe SGA was among complicated (eg, hypertensive disease, substance abuse) vs uncomplicated disease. The dataset does not have information on factors such as indications for preterm birth, neonatal acidosis, or seizure, which might influence performance on the evaluation. Lastly, our analysis did not control for the influence of early intervention in cognitive function.
      • Brooks-Gunn J.
      • Liaw F.R.
      • Klebanov P.K.
      Effects of early intervention on cognitive function of low birth weight preterm infants.
      Although participation in early intervention programs may be a mechanism for catch-up cognitive performance, the current study clearly demonstrates this phenomenon in a large and diverse national sample.
      In conclusion, although there is a significant difference in cognitive functioning at 9 months for newborns <3% vs ≥3% for GA, severe SGA children do demonstrate a catch-up phenomenon by 2 years. Additional studies with sufficient sample size and diversity are warranted to confirm our findings and to determine the plausible explanations for our findings.

      References

        • American College of ObstetriciansGynecologists
        Intrauterine growth restriction: ACOG practice bulletin no. 12.
        American College of Obstetricians and Gynecologists, Washington, DC2000 (Reaffirmed 2010)
        • McIntire D.D.
        • Bloom S.L.
        • Casey B.M.
        • Leveno K.J.
        Birth weight in relation to morbidity and mortality among newborn infants.
        N Engl J Med. 1999; 340: 1234-1238
        • Garite T.J.
        • Clark R.
        • Thorp J.A.
        Intrauterine growth restriction increases morbidity and mortality among premature neonates.
        Am J Obstet Gynecol. 2004; 191: 481-487
        • US Department of Education
        Early childhood longitudinal study, birth cohort, 9 month data collection.
        US Department of Education, Washington, DC2005
        • US Department of Education
        Early childhood longitudinal study, birth cohort: methodology report for the 9-month data collection, vol 1.
        US Department of Education, Washington, DC2005
        • US Department of Education
        Early childhood longitudinal study, birth cohort: preschool-kindergarten psychometric report.
        US Department of Education, Washington, DC2010
        • 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.
        BMC Pediatrics. 2003; 3: 6
        • Alexander G.R.
        • Himes J.H.
        • Kaufman R.B.
        • Mor J.
        • Kogan M.
        A United States national reference for fetal growth.
        Obstet Gynecol. 1996; 87: 163-168
        • Snow K.
        • Derechoaa A.
        • Wheeless S.
        • et al.
        Early childhood longitudinal study, birth cohort (ECLS-B), kindergarten 2006 and 2007 data file user's manual (2010-010).
        National Center for Education Statistics, Institute of Education Sciences, US Department of Education, Washington, DC2009
        • Woythaler M.A.
        • McCormick M.C.
        • Smith V.C.
        Late preterm infants have worse 24-month neurodevelopmental outcomes than term infants.
        Pediatrics. 2011; 127: e622-e629
        • Huang Z.J.
        • Lewin A.
        • Mitchell S.J.
        • Zhang J.
        Variations in the relationship between maternal depression, maternal sensitivity, and child attachment by race/ethnicity and nativity: findings from a nationally representative cohort study.
        Matern Child Health J. 2012; 16: 40-50
        • Ogbuanu C.
        • Glover S.
        • Probst J.
        • Liu J.
        • Hussey J.
        The effect of maternity leave length and time of return to work on breastfeeding.
        Pediatrics. 2011; 127: e1414-e1427
        • Kitsantas P.
        • Pawloski L.R.
        • Gaffney K.F.
        Maternal prepregnancy body mass index in relation to Hispanic preschooler overweight/obesity.
        Eur J Pediatr. 2010; 169: 1361-1368
        • Agostoni C.
        Small-for-gestational-age infants need dietary quality more than quantity for their development: the role of human milk.
        Acta Paediatr. 2005; 94: 827-829
        • Geva R.
        • Eshel R.
        • Leitner Y.
        • Fattal-Valevski A.
        • Harel S.
        Verbal short-term memory span in children: long-term modality dependent effects of intrauterine growth restriction.
        J Child Psychol Psychiatry. 2008; 49: 1321-1330
        • Geva R.
        • Eshel R.
        • Leitner Y.
        • Valevski A.F.
        • Harel S.
        Neuropsychological outcome of children with intrauterine growth restriction: a 9-year prospective study.
        Pediatrics. 2006; 118: 91-100
        • Leitner Y.
        • Fattal-Valevski A.
        • Geva R.
        • et al.
        Neurodevelopmental outcome of children with intrauterine growth retardation: a longitudinal, 10-year prospective study.
        J Child Neurol. 2007; 22: 580-587
        • Petersen S.G.
        • Wong S.F.
        • Urs P.
        • Gray P.H.
        • Gardener G.J.
        Early onset, severe fetal growth restriction with absent or reversed end-diastolic flow velocity waveform in the umbilical artery: perinatal and long-term outcomes.
        Aust N Z J Obstet Gynaecol. 2009; 49: 45-51
        • Smedler C.
        • Faxelius G.
        • Bremme K.
        • Lagerstrom M.
        Psychological development in children born with very low birth weight after severe intrauterine growth retardation: a 10-year follow-up study.
        Acta Paediatr. 1992; 81: 197-203
        • Hadders-Algra M.
        • Touwen B.C.
        Body measurements, neurological and behavioral development in six-year-old children born preterm and/or small-for-gestational-age.
        Early Hum Dev. 1990; 22: 1-13
        • Slykerman R.F.
        • Thompson J.M.
        • Clark P.M.
        • et al.
        Determinants of developmental delay in infants aged 12 months.
        Paediatr Perinat Epidemiol. 2007; 21: 121-128
        • Campos M.
        • Reyes G.
        • García L.
        Comparison of postdischarge growth in adequate for gestational age and small for gestational age very low birthweight infants.
        Ethn Dis. 2008; 18: 118-122
        • Bassan H.
        • Stolar O.
        • Geva R.
        • et al.
        Intrauterine growth-restricted neonates born at term or preterm: how different?.
        Pediatr Neurol. 2011; 44: 122-130
        • Manning F.A.
        • Bondaji N.
        • Harman C.R.
        • et al.
        Fetal assessment based on fetal biophysical profile scoring, VIII: the incidence of cerebral palsy in tested and untested perinates.
        Am J Obstet Gynecol. 1998; 178: 696-706
        • Mattioli K.P.
        • Sanderson M.
        • Chauhan S.P.
        Inadequate identification of small-for-gestational-age fetuses at an urban teaching hospital.
        Int J Gynaecol Obstet. 2010; 109: 140-143
        • Fox N.S.
        • Rebarber A.
        • Klauser C.K.
        • Roman A.S.
        • Saltzman D.H.
        Intrauterine growth restriction in twin pregnancies: incidence and associated risk factors.
        Am J Perinatol. 2011; 28: 267-272
        • Brooks-Gunn J.
        • Liaw F.R.
        • Klebanov P.K.
        Effects of early intervention on cognitive function of low birth weight preterm infants.
        J Pediatr. 1992; 120: 350-359