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Maternal Prepregnancy Weight and Children’s Behavioral and Emotional Outcomes

      Introduction

      This study investigated associations between maternal prepregnancy BMI and child behaviors at ages 9–11 years and examine interaction by race and gender.

      Methods

      The National Longitudinal Survey of Youth and the Children and Young Adults surveys are U.S.-based, ongoing longitudinal studies, initiated in 1979 and 1986, respectively. Mothers (n=2,952) reported pregnancy and child (n=5,660) developmental information at multiple time points. Child total, internalizing, and externalizing problems at ages 9–11 years were assessed using the Behavior Problems Index (BPI), collected biennially until 2012. Associations between prepregnancy BMI and child BPI outcomes were examined, as well as two- and three-way interactions by race and gender. Analyses were conducted in 2017.

      Results

      Boys whose mothers had higher prepregnancy weights exhibited higher total BPI and externalizing scores at ages 9–11 years versus those with normal-weight mothers. Boys with severely obese mothers had higher total BPI (mean difference=7.99, 95% CI=3.53, 12.46) and externalizing (mean difference=5.77, 95% CI=1.50, 10.04) scores. Prepregnancy underweight was associated with boys’ higher total BPI (mean difference=2.34, 95% CI=0.02, 4.66) and externalizing (mean difference=3.30, 95% CI=0.69, 5.91); these associations were not significant in sensitivity analyses. No associations emerged for girls or internalizing problems. Two-way interactions by race and three-way interactions by race and gender were not significant.

      Conclusions

      Maternal prepregnancy weight was associated with BPI level among boys. Boys with severely obese mothers exhibited markedly higher behavioral problems at ages 9–11 years versus those with normal-weight mothers, regardless of race. Maintaining healthy prepregnancy weight may be important for preventing boys’ deleterious behavior outcomes in middle childhood.

      Introduction

      The prevalence of both maternal obesity and child neurodevelopmental problems has increased in the U.S.
      National Academy of Medicine, National Research Council
      Weight Gain During Pregnancy: Reexamining the Guidelines.

      U.S. Environmental Protection Agency. Neurodevelopmental Disorders. In: America’s Children and the Environment. 3rd ed. Publisher unknown; 2013:233–253.

      Maternal weight, before and during pregnancy, is linked to child behavior. Two recent reviews support an association between high maternal weight and a range of neurodevelopmental and psychiatric problems, including cognitive deficits, attention deficit hyperactivity disorder, and internalizing problems.
      • Van Lieshout R.J.
      Role of maternal adiposity prior to and during pregnancy in cognitive and psychiatric problems in offspring.
      • Van Lieshout R.J.
      • Taylor V.H.
      • Boyle M.H.
      Pre-pregnancy and pregnancy obesity and neurodevelopmental outcomes in offspring: a systematic review.
      Many studies suggest that maternal prepregnancy obesity is associated with children’s externalizing problems, including attention deficit hyperactivity disorder.
      • Antoniou E.E.
      • Fowler T.
      • Reed K.
      • Southwood T.R.
      • McCleery J.P.
      • Zeegers M.P.
      Maternal pre-pregnancy weight and externalising behaviour problems in preschool children: a UK-based twin study.
      • Buss C.
      • Entringer S.
      • Davis E.P.
      • et al.
      Impaired executive function mediates the association between maternal pre-pregnancy body mass index and child ADHD symptoms.
      • Hinkle S.N.
      • Sharma A.J.
      • Schieve L.A.
      • Ramakrishnan U.
      • Swan D.W.
      • Stein A.D.
      Reliability of gestational weight gain reported postpartum: a comparison to the birth certificate.
      • Rodriguez A.
      • Miettunen J.
      • Henriksen T.B.
      • et al.
      Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts.
      • Van Lieshout R.J.
      • Robinson M.
      • Boyle M.H.
      Maternal pre-pregnancy body mass index and internalizing and externalizing problems in offspring.
      Less attention has focused on internalizing problems (e.g., depression), but mixed evidence points to a similar association.
      • Rodriguez A.
      Maternal pre-pregnancy obesity and risk for inattention and negative emotionality in children.
      • Robinson M.
      • Zubrick S.R.
      • Pennell C.E.
      • et al.
      Pre-pregnancy maternal overweight and obesity increase the risk for affective disorders in offspring.
      • Tanda R.
      • Salsberry P.J.
      Racial differences in the association between maternal prepregnancy obesity and children’s behavior problems.
      • Van Lieshout R.J.
      • Schmidt L.A.
      • Robinson M.
      • Niccols A.
      • Boyle M.H.
      Maternal pre-pregnancy body mass index and offspring temperament and behavior at 1 and 2 years of age.
      Several gaps and challenges exist in the literature, however. First, comparing results is challenging because studies often adjust for different sets of covariates, raising questions about whether associations are the result of confounding due to unmeasured covariates.
      • Brion M.J.
      • Zeegers M.
      • Jaddoe V.
      • et al.
      Intrauterine effects of maternal prepregnancy overweight on child cognition and behavior in 2 cohorts.
      Second, although maternal underweight before or during pregnancy could influence children’s behaviors,
      • Polańska K.
      • Muszyński P.
      • Sobala W.
      • Dziewirska E.
      • Merecz-Kot D.
      • Hanke W.
      Maternal lifestyle during pregnancy and child psychomotor development—Polish Mother and Child Cohort study.
      • Hinkle S.N.
      • Schieve L.A.
      • Stein A.D.
      • Swan D.W.
      • Ramakrishnan U.
      • Sharma A.J.
      Associations between maternal prepregnancy body mass index and child neurodevelopment at 2 years of age.
      through its associations with pregnancy complications including preterm birth,
      • Wise L.A.
      • Palmer J.R.
      • Heffner L.J.
      • Rosenberg L.
      Prepregnancy body size, gestational weight gain, and risk of preterm birth in African-American women.
      most attention has been focused on maternal obesity. Third, only one known study examined the modifying roles of both ethnicity and gender.
      • Pugh S.J.
      • Hutcheon J.A.
      • Richardson G.A.
      • et al.
      Gestational weight gain, prepregnancy body mass index and offspring attention-deficit hyperactivity disorder symptoms and behaviour at age 10.
      Finally, many studies focus on young children and do not capture the emergence of behavior problems later in childhood.
      • Van Lieshout R.J.
      Role of maternal adiposity prior to and during pregnancy in cognitive and psychiatric problems in offspring.
      • Van Lieshout R.J.
      • Taylor V.H.
      • Boyle M.H.
      Pre-pregnancy and pregnancy obesity and neurodevelopmental outcomes in offspring: a systematic review.
      To the authors’ knowledge, no studies of maternal BMI and child neurodevelopment have examined effect modification by race and gender simultaneously (three-way interaction). A study of children aged 10 years born to high-risk women suggested an association between maternal obesity and child behavior, with no effect modification by race or gender.
      • Pugh S.J.
      • Hutcheon J.A.
      • Richardson G.A.
      • et al.
      Gestational weight gain, prepregnancy body mass index and offspring attention-deficit hyperactivity disorder symptoms and behaviour at age 10.
      By contrast, using the U.S. National Longitudinal Survey of Youth 1979 (NLSY79), Tanda et al.
      • Tanda R.
      • Salsberry P.J.
      Racial differences in the association between maternal prepregnancy obesity and children’s behavior problems.
      concluded that overweight and obese white, but not African American, women are at elevated risk for having children with behavioral problems at ages 8–9 years.
      • Tanda R.
      • Salsberry P.J.
      Racial differences in the association between maternal prepregnancy obesity and children’s behavior problems.
      The present study also uses the NLSY79 to investigate whether maternal prepregnancy BMI is associated with behavioral problems among school-age children. Effect modification is examined by race or gender, as well as by race and gender simultaneously. Because early puberty is a time when behavioral problems emerge, this study focuses on children aged 9–11 years. Potentially important covariates that often have been excluded from previous studies are included in the analysis.

      Methods

      Study Population

      The NLSY79 recruited participants using a multistage sampling design, and the weighted data are representative of the U.S. population in 1979. This analysis included female NLSY79 cohort participants (N=4,932) and their biological children, who were studied between 1986 and 2012 as part of the NLSY Children and Young Adults (NLSYCYA) cohort (N=11,512). Study details for both cohorts are available.
      Center for Human Resource Research
      NLSY79 User’s Guide.
      Center for Human Resource Research
      NLSY79 Child and Young Adult Data User’s Guide.
      Children were included if their mothers reported their prepregnancy weight and height and had complete questionnaire data at ages 9–11 years for the Behavior Problems Index (BPI) composite measures described below. Given previous NLSYCYA research showing black–white differences,
      • Tanda R.
      • Salsberry P.J.
      Racial differences in the association between maternal prepregnancy obesity and children’s behavior problems.
      only respondents classified as non-Hispanic black or non-Hispanic, non-black (the latter is 88% white) were included.

      Bureau of Labor Statistics. National Longitudinal Study of Youth: Household, Geography, & Contextual Variables. www.nlsinfo.org/content/cohorts/nlsy79/topical-guide/household/race-ethnicity-immigration-data. Accessed August 24, 2016.

      Hispanic participants (n=1,168) were not included because cell sizes were too small to obtain reliable estimates for interaction by ethnicity. For example, there were only six Hispanic boys and 17 Hispanic girls whose mothers had severe (Class II/III) prepregnancy obesity. Also, this group was heterogeneous (69% Mexican or Mexican American, 15% Puerto Rican, and 6% other Hispanic, 4% Chicano, and 4% Cuban), limiting its generalizability. The Committee for Protection of Human Subjects at the University of California, Berkeley approved this study.

      Measures

      The NLSY79 women reported their heights in 1985, which were regression calibrated to National Health and Nutrition Examination Survey data.
      • Burkhauser R.V.
      • Cawley J.
      Beyond BMI: the value of more accurate measures of fatness and obesity in social science research.
      Prepregnancy weight was recalled in 1986 for prior pregnancies and, after 1986, reported at the interview following each pregnancy. Prepregnancy BMI was categorized as underweight (BMI <18.5); normal weight (BMI=18.5–24.9); overweight (BMI=25.0–29.9); obese Class I (BMI=30.0–34.9); and obese Classes II/III (BMI ≥35).

      WHO. Global database on body mass index: BMI classification. www.assessmentpsychology.com/icbmi.htm. Accessed May 2, 2017.

      In the NLSYCYA, behavioral problems were assessed biennially for children aged 4–14 years using maternal report of the BPI, a widely used 28-item questionnaire, to determine whether they exhibited specific behaviors in the past 3 months.
      • Achenbach T.M.
      • Edelbrock C.S.
      Behavioral problems and competencies reported by parents of normal and disturbed children aged four through sixteen.
      • Peterson J.L.
      • Zill N.
      Marital disruption, parent-child relationships, and behavior problems in children.
      The BPI was originally developed using items from the Child Behavior Checklist that were determined to be common in the population and that discriminated between children who were and were not receiving psychological services.
      • Zill N.
      Behavior Problem Scales Developed from the 1981 Child Health Supplement to the National Health Interview Survey.
      Responses were often true, sometimes true, and not true. Raw scores were calculated for total problems and two composite measures (externalizing and internalizing problems) based on Child Behavior Checklist guidelines.
      • Guttmannova K.
      • Szanyi J.M.
      • Cali P.W.
      Internalizing and externalizing behavior problem scores: cross-ethnic and longitudinal measurement invariance of the Behavior Problem Index.
      Scores were computed for children with complete BPI data. Standardized scores were created (mean=100, SD=15) using population-based age and gender norms from the Child Health Supplement of the National Health Interview Survey 1981 data.

      Minnesota Population Center and State Health Access Data Assistance Center, University of Minnesota. Integrated Health Interview Series: Version 4.0. www.ihis.us. Accessed August 24, 2016.

      Higher scores indicated worse problems. The reliability of the total BPI (α=0.90) was similar to that in past studies (α=0.89).
      • Zill N.
      Behavior Problem Scales Developed from the 1981 Child Health Supplement to the National Health Interview Survey.
      Covariates were selected a priori, taking previous research and temporal ordering into account, and included maternal Armed Forces Qualification Test score (<33%, 33%–66%, >66%; a proxy for IQ); parity (nulliparous, parous); and, at delivery, maternal age (19 years, 20–29 years, 30 years), education (<12 years, 12–15 years, 16 years), marital status (married, unmarried), employment status (full-time, part-time, unemployed), decade of birth (1970–1979, 1980–1989, 1990–1999, ≥2000), and annual equivalized household income
      • Rehkopf D.H.
      • Krieger N.
      • Coull B.
      • Berkman L.F.
      Biologic risk markers for coronary heart disease: nonlinear associations with income.
      in year 2000 dollars. Maternal race and child gender were potential effect modifiers.

      Statistical Analysis

      Analyses were conducted in 2017 using R, version 3.2.2, and Stata, version 14.0.
      R Core Team R
      A language and environment for statistical computing..
      Sample characteristics were examined stratified by prepregnancy BMI. Rao–Scott
      • Rao J.N.K.
      • Scott A.J.
      On chi-squared tests for multiway contigency tables with proportions estimated from survey data.
      chi-square tests and linear regression models were used to test for differences in covariate distributions by exposure. Linear regression analyses were conducted to estimate crude mean differences in BPI total and composite scores between prepregnancy BMI categories in the full sample, as well as in gender subsets when interactions with gender were significant. Main effects were significant at p<0.05 and interactions at p<0.10. Multivariate linear regression models were used to estimate mean BPI differences compared to children of mothers of normal prepregnancy weight, adjusted for covariates.
      • Lumley T.
      Analysis of complex survey samples.
      In one set of models, Wald tests were used to assess gender by BMI interactions. A second set of models was estimated with race by BMI interactions. Three-way interactions (prepregnancy BMI X race X gender) were assessed in a final set of models. All regression models were weighted. Robust SEs were calculated to account for NLSY79’s complex survey design, as well as within-family correlation.
      To address covariate missingness (0%–22.1%; median, 3.4%), multiple imputation by chained equations was used for multivariate models.
      • van Buuren S.
      • Groothuis-Oudshoorn K.
      Mice: multivariate imputation by chained equations in R.
      The imputation model included BPI measures, prepregnancy BMI, covariates, and quintiles of the sampling weights to reduce bias from the sampling design.
      • Rosenbaum P.R.
      • Rubin D.B.
      The central role of the propensity score in observational studies for causal effects.
      Fifty data sets were imputed using a 50-step iterative process, and estimates, variances, and test statistics were pooled.
      Because the sample consisted in part of siblings, a sensitivity analysis was conducted in the sibling subsample (n=1,823 mothers, 4,531 children) using fixed effects regression to control for unmeasured shared familial characteristics. These models consider maternal- and family-level factors that are constant across a mother’s pregnancies, such as genetic and some environmental factors. Implicit in this approach, only the children of mothers who changed BMI categories between pregnancies (n=672 mothers, 1,794 children) contributed to the estimates of the associations. SEs were adjusted for clustering at the highest level of sampling.

      Results

      Table 1 describes characteristics for the 5,660 mother–child dyads, stratified by prepregnancy BMI and accounting for clustered sampling and oversampling of blacks and low-income whites. Total raw percentages are included to illustrate the ethnic diversity of the unweighted sample.
      Table 1Maternal and Child Characteristics of 5,660 Mother–Child Dyads in the NLSYCYA Cohort Ages 9–11 Years by Maternal Prepregnancy BMI
      CharacteristicsTotal (raw)Total (weighted) (n=5660)Under-weight (n=518)Normal weight (n=3708)Over-weight (n=927)Obese I (n=330)Obese II/III (n=177)p-value
      Total8.265.816.56.03.5
      Maternal characteristics
       Race/ethnicity, %0.235
        White/other63.981.481.182.279.379.179.2
        Black36.118.618.917.820.720.920.8
       Maternal education,
      Missingness in these variables ranged from 3.4% to 22.1%.
      %
      <0.001
        <12 years18.814.025.613.312.013.013.4
        12–15 years44.443.347.043.143.041.543.7
        ≥16 years36.842.727.443.644.945.642.9
       Maternal employment,
      Missingness in these variables ranged from 3.4% to 22.1%.
      %
      <0.01
        Unemployed38.533.342.132.333.731.034.5
        Part-time employment27.828.232.228.826.127.121.4
        Employed33.738.525.738.940.241.944.2
       Married at birth year,
      Missingness in these variables ranged from 3.4% to 22.1%.
      %
      65.775.765.376.479.174.471.5<0.01
       Age at birth, %
        <20 years19.912.928.014.07.33.00.8<0.001
        20–29 years57.355.855.256.656.352.146.9
        ≥30 years22.831.316.929.536.544.952.4
       Parous, %54.155.748.152.965.067.760.5<0.001
       AFQT score percentile,
      Missingness in these variables ranged from 3.4% to 22.1%.
      M (SD)
      40.1 (28.2)48.5 (28.4)39.8 (26.6)49.6 (28.4)49.3 (28.6)47.3 (27.1)46.0 (28.7)<0.01
      Family background
       Income at birth year,
      Missingness in these variables ranged from 3.4% to 22.1%.
      ,
      Equivalized family income in year 2000 dollars. AFQT, Armed Forces Qualifying Test; BPI, Behavior Problems Index; NLSYCYA, National Longitudinal Survey of Youth Children/Young Adults.
      M (SD)
      9.6 (1.3)9.9 (1.2)9.5 (1.3)9.9 (1.2)9.9 (1.0)9.9 (0.9)9.9 (1.0)<0.001
      Child characteristics
       Female, %50.049.248.249.348.050.053.00.810
       Age, %0.542
        60–71 months8.37.58.28.05.96.26.0
        72–83 months44.944.741.444.445.948.346.3
        84–95 months46.847.850.447.648.245.447.7
       Year of birth, %<0.001
        1970–197916.910.620.411.86.12.40.2
        1980–198954.851.057.252.548.242.134.4
        1990–199926.736.321.934.142.649.858.0
        2000–20091.72.20.41.63.15.67.4
       Behavior
        Total BPI score, M (SD)106.6 (16.2)105.5 (15.7)107.2 (15.9)105.0 (15.4)105.9 (15.7)105.8 (15.6)109.3 (19.3)0.104
        Externalizing BPI score, M (SD)110.6 (16.8)109.5 (16.4)111.8 (16.8)108.8 (16.1)109.9 (16.4)110.8 (17.5)111.4 (18.1)<0.05
        Internalizing BPI score, M (SD)108.2 (15.9)107.9 (15.7)108.7 (16.0)107.8 (15.5)107.6 (15.8)108.1 (16.1)110.3 (17.3)0.711
      Note: Boldface indicates statistical significance (p<0.05).
      a Missingness in these variables ranged from 3.4% to 22.1%.
      b Equivalized family income in year 2000 dollars.AFQT, Armed Forces Qualifying Test; BPI, Behavior Problems Index; NLSYCYA, National Longitudinal Survey of Youth Children/Young Adults.
      Sixty-six percent of the mothers were normal weight, 8% underweight, and 10% obese, of whom 3.5% were Class II/III. Maternal characteristics varied by prepregnancy BMI. More underweight mothers gave birth in the 1980s, whereas more obese Class II/III women gave birth in the 1990s, reflecting increases in BMI with maternal age and parity. Underweight women were younger, less likely to be married, and had the lowest education, income, and Armed Forces Qualifying Test scores (Table 1).
      Complete data on exposure and outcome were available for 74% of the eligible sample. The analyzed sample included younger (13% vs 10% aged <20 years, p<0.001); nulliparous (44% vs 34%, p<0.001); and employed (33% vs 38%, p=0.011) mothers and fewer children born after 1990 (39% vs 50%, p<0.001) than those excluded. Other characteristics were similar.
      In unadjusted analyses in the full sample, maternal prepregnancy underweight was related to higher total BPI and externalizing scores (not shown). These associations differed between boys and girls, such that maternal Class II/III obesity was significantly associated with total BPI and externalizing among boys, but not girls (Appendix Table 1, available online). There were no significant associations with internalizing problems.
      In the adjusted models for the full sample, prepregnancy BMI by gender interactions for total and externalizing scales were significant (p=0.07, 0.09, respectively). There were no associations between prepregnancy BMI and internalizing scores, and no two-way interaction with gender (p=0.36). Figure 1 shows adjusted results stratified by gender for total and externalizing outcomes. Children of the same gender whose mothers had normal prepregnancy BMI were the reference category. Among boys, higher prepregnancy BMI was associated with poorer total and externalizing scores; total scores were 7.99 points higher (95% CI=3.53, 12.46) and externalizing scores 5.77 points higher (95% CI=1.50, 10.04) in sons of mothers who were obese Class II/III prepregnancy compared with the reference group. Boys whose mothers were underweight also had increased total (2.34, 95% CI=0.02, 4.66) and externalizing (3.30, 95% CI=0.69, 5.91) scores. There were no significant associations for girls. As there was no gender interaction for internalizing, the graph is not stratified by gender for this outcome.
      Figure 1
      Figure 1Adjusted mean differences in BPI score associated with prepregnancy BMI in NLSYCYA children stratified by gender.
      Note: p-values for interaction: 0.07 (total problems); 0.09 (externalizing problems).
      BPI, Behavior Problems Index; NLSYCYA, National Longitudinal Survey of Youth Children/Young Adults.
      There were no two-way interactions with race/ethnicity for total, externalizing, and internalizing problems (p=0.70, 0.81, 0.87, respectively), nor were there three-way interactions (p=0.16, 0.29, 0.31).
      Fixed-effects sensitivity analysis was conducted to address the fact that the study included some siblings in the same family. Results suggested associations with maternal Class II/III obesity in boys that were slightly larger in magnitude compared with those from the standard multivariate analysis (Appendix Table 2, available online). Total problems scores increased 10.56 points and 10.74 points in sons of women with Class II/III obesity prepregnancy, accounting for characteristics shared by siblings. However, estimates were marginally significant (p<0.10), likely because of reduced power in this smaller sample. The associations with prepregnancy underweight were similar in magnitude to those from standard analysis, but were no longer significant for total and externalizing problems (p=0.480, 0.207, respectively).

      Discussion

      In this large sample of black and white mothers and their children aged 9–11 years, severe maternal prepregnancy obesity was associated with higher total and externalizing behavior problems for boys, but not girls. The heavier mothers were when they entered pregnancy, the higher the risk for behavior problem outcomes for their sons. Maternal prepregnancy underweight was also associated with higher total and externalizing problems for boys, although this finding was attenuated and not significant in the fixed-effects analysis, and requires replication. There were no significant associations for girls or for internalizing problems, and there were no differences across race. This study is the first to document gender differences in these associations, and one of a handful of studies to show that prepregnancy underweight, in addition to obesity, may be problematic.
      • Polańska K.
      • Muszyński P.
      • Sobala W.
      • Dziewirska E.
      • Merecz-Kot D.
      • Hanke W.
      Maternal lifestyle during pregnancy and child psychomotor development—Polish Mother and Child Cohort study.
      • Hinkle S.N.
      • Schieve L.A.
      • Stein A.D.
      • Swan D.W.
      • Ramakrishnan U.
      • Sharma A.J.
      Associations between maternal prepregnancy body mass index and child neurodevelopment at 2 years of age.
      The finding that boys are at special risk adds to previous literature linking maternal prepregnancy weight with children’s externalizing problems. A study of three Nordic cohorts (N=12,566) suggested that prepregnancy overweight/obesity was associated with teacher-rated attention deficit hyperactivity disorder symptoms at ages 7–12 years,
      • Rodriguez A.
      • Miettunen J.
      • Henriksen T.B.
      • et al.
      Maternal adiposity prior to pregnancy is associated with ADHD symptoms in offspring: evidence from three prospective pregnancy cohorts.
      but did not test for gender differences. Similarly, a U.S. study of 1,311 mother–child pairs showed that Class II/III prepregnancy obesity was associated with psychosocial problems at age 6 years,
      • Jo H.
      • Schieve L.A.
      • Sharma A.J.
      • Hinkle S.N.
      • Li R.
      • Lind J.N.
      Maternal prepregnancy body mass index and child psychosocial development at 6 years of age.
      but children were not followed to older ages; the sample comprised predominantly white families (87%); and interaction by gender was not examined. A recent study of 511 high-risk black and white Pennsylvania women reported that maternal obesity was associated with behavioral and emotional problems at age 10 years, but found no differences by race or gender.
      • Pugh S.J.
      • Hutcheon J.A.
      • Richardson G.A.
      • et al.
      Gestational weight gain, prepregnancy body mass index and offspring attention-deficit hyperactivity disorder symptoms and behaviour at age 10.
      The current findings build on this work by revealing gender differences, and showing risk associated with maternal prepregnancy underweight.
      Tanda and colleagues
      • Tanda R.
      • Salsberry P.J.
      Racial differences in the association between maternal prepregnancy obesity and children’s behavior problems.
      also analyzed school-aged children in the NLSY cohorts, and concluded that there was an association between prepregnancy obesity and BPI outcomes at ages 8–9 years among white, but not black, children.
      • Tanda R.
      • Salsberry P.J.
      Racial differences in the association between maternal prepregnancy obesity and children’s behavior problems.
      By contrast, the current study suggested a significant two-way interaction with gender but not by race. There are several possible explanations for differences in results between these two analyses of the NLSY79 cohort. First, the current study included a larger sample (5,660 vs 3,395) because multiple imputation was used to resolve missing data issues rather than omitting participants, and preterm and low birth weight children were not excluded. The age groups were not identical as the current study focused on slightly older children. In addition, the previous study included birth weight, gestational age, and child’s weight status as covariates, whereas these were excluded from the current analyses because they are potential mediators on the causal path. A unique aspect of this study was the use of fixed effects analysis to confirm that results were not solely attributable to unmeasured confounding among siblings. Therefore, although both studies suggest an association between maternal obesity and child development in the NLSY79 and NLSYCYA cohorts, these differences in study methods may explain differences in results.
      Research suggests that exposures in utero are associated with poor neurocognitive, behavioral, and emotional outcomes in offspring.
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      Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review.
      Prepregnancy obesity appears to confer negative effects for a developing fetus. Few studies, however, have focused on factors that mediate associations between prepregnancy weight and children’s behaviors. Obesity during pregnancy creates inflammation and causes metabolic changes that may affect gene expression and alter a fetus’s developing brain.
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      • Jonakait G.M.
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      In addition, lifestyle or behavioral factors associated with maternal obesity (e.g., prenatal diet, substance abuse, breastfeeding) or psychosocial factors (e.g., maternal mental health, stress) may influence child development.
      • Amir L.H.
      • Donath S.
      A systematic review of maternal obesity and breastfeeding intention, initiation and duration.
      • LaCoursiere D.Y.
      • Barrett-Connor E.
      • O’Hara M.W.
      • Hutton A.
      • Varner M.W.
      The association between prepregnancy obesity and screening positive for postpartum depression.
      A recent review pointed to unhealthy diet during pregnancy and maternal distress as two leading risk factors for children’s poor neurodevelopment.
      • Monk C.
      • Georgieff M.K.
      • Osterholm E.A.
      Maternal prenatal distress and poor nutrition—mutually influencing risk factors affecting infant neurocognitive development.
      One study tested several prepartum and postpartum mediators, including gestational weight gain, gestational diabetes, breastfeeding, postpartum depression, and birth weight, but none of these factors explained associations between maternal obesity and child outcomes.
      • Jo H.
      • Schieve L.A.
      • Sharma A.J.
      • Hinkle S.N.
      • Li R.
      • Lind J.N.
      Maternal prepregnancy body mass index and child psychosocial development at 6 years of age.
      Research in this area is nascent, and future investigation is warranted.
      In the current study, there was some evidence that maternal prepregnancy underweight—in addition to overweight—may be linked to boys’ problems, although this requires replication. Maternal underweight may reflect poor nutrition and stress during pregnancy.
      • Neggers Y.
      • Goldenberg R.L.
      Some thoughts on body mass index, micronutrient intakes and pregnancy outcome.
      These factors may be linked to pregnancy behaviors, such as tobacco or other substance use or dieting behaviors, which also impact fetal development,
      • Polańska K.
      • Muszyński P.
      • Sobala W.
      • Dziewirska E.
      • Merecz-Kot D.
      • Hanke W.
      Maternal lifestyle during pregnancy and child psychomotor development—Polish Mother and Child Cohort study.
      and may continue after pregnancy, impacting children’s behaviors in early life and beyond. Unfortunately, these exposures were not well measured in the NLSY, which precluded investigation into their roles as mechanisms. Future research that documents behaviors before, during, and after pregnancy among diverse samples and tracks child outcomes downstream is warranted. Finally, no known studies have investigated whether child BMI or pubertal status may mediate these associations downstream. This examination was beyond the current scope, but represents an important area for future research.
      This study suggests gender differences in the association between maternal BMI and total behavior and externalizing problems. Metabolic exposures in utero may differentially influence a developing fetus. In studies of famine and nutrition, male fetuses consistently exhibit stronger risk due to undernutrition, and greater benefits from adequate nutrition, compared with girls.
      • Song S.
      Does famine influence sex ratio at birth? Evidence from the 1959–1961 Great Leap Forward Famine in China.
      • Mora J.O.
      • Sanchez R.
      • De Paredes B.
      • Guillermo Herrera M.
      Sex related differences of nutritional supplementation during pregnancy on fetal growth.
      • Navara K.J.
      Programming of offspring sex ratios by maternal stress in humans: assessment of physiological mechanisms using a comparative approach.
      During times of stress, boys are subject to higher fetal death rates than girls.
      • Navara K.J.
      Programming of offspring sex ratios by maternal stress in humans: assessment of physiological mechanisms using a comparative approach.
      • Catalano R.F.
      • Bruckner T.
      • Gould J.
      • Eskenazi B.
      • Anderson E.
      Sex ratios in California following the terrorist attacks of September 11, 2001.
      One suggested mechanism for stress-induced fetal programming of sex ratios is glucocorticoid exposure in utero because of maternal stress.
      • Navara K.J.
      Programming of offspring sex ratios by maternal stress in humans: assessment of physiological mechanisms using a comparative approach.
      Animal and human studies examining other environmental exposures also support sex differences in risk; for example, only male offspring appear to be at higher risk for behavior problems when exposed in utero to the chemical bisphenol A.
      • Mustieles V.
      • Pérez-Lobato R.
      • Olea N.
      • Fernández M.F.
      Bisphenol A: human exposure and neurobehavior.
      As such, boys may be more susceptible to certain insults in utero.
      Future research should examine whether the gender differences reported here for ages 9–11 years persist into adolescence or shift as children get older. In previous results from NLSY79, maternal prepregnancy overweight/obesity and excessive gestational weight gain predicted girls’ earlier menarche,
      • Deardorff J.
      • Berry-Millett R.
      • Rehkopf D.H.
      • Luecke E.
      • Lahiff M.
      • Abrams B.
      Maternal pre-pregnancy BMI, gestational weight gain, and age at menarche in daughters.
      which has been linked to poor behavioral and emotional outcomes in adolescence.
      • Mendle J.
      • Turkheimer E.
      • Emery R.E.
      Detrimental psychological outcomes associated with early pubertal timing in adolescent girls.
      • Stice E.
      • Presnell K.
      • Bearman S.K.
      Relation of early menarche to depression, eating disorders, substance abuse, and comorbid psychopathology among adolescent girls.
      • Deardorff J.
      • Hayward C.
      • Wilson K.A.
      • Bryson S.
      • Hammer L.D.
      • Agras S.
      Puberty and gender interact to predict social anxiety symptoms in early adolescence.
      • Deardorff J.
      • Gonzales N.A.
      • Christopher F.S.
      • Roosa M.W.
      • Millsap R.
      Early puberty and adolescent pregnancy: the influence of alcohol use.
      Even though the current study did not show associations between maternal BMI and internalizing problems, adolescence is also a time when anxiety and depression become more prevalent, particularly among girls.
      • Nolen-Hoeksema S.
      • Girgus J.S.
      The emergence of gender differences in depression during adolescence.
      Longer-term research may reveal gender differences at older ages, and therefore research examining pregnancy factors, adolescent outcomes, and gender is warranted.

      Limitations

      This study was observational; therefore, the possibility of unmeasured confounding remains. Pregnancy-related weight data relied on maternal self-report. However, studies have shown that self-reported and clinically assessed prepregnancy weights are highly correlated,
      • Hinkle S.N.
      • Sharma A.J.
      • Schieve L.A.
      • Ramakrishnan U.
      • Swan D.W.
      • Stein A.D.
      Reliability of gestational weight gain reported postpartum: a comparison to the birth certificate.
      • Lederman S.A.
      • Paxton A.
      Maternal reporting of prepregnancy weight and birth outcome: consistency and completeness compared with the clinical record.
      and reliability between self-reported weights within 2 years of the pregnancy and prepregnancy weight has been shown previously in NLSY.
      • Ranchod Y.K.
      • Headen I.E.
      • Petito L.C.
      • Deardorff J.K.
      • Rehkopf D.H.
      • Abrams B.F.
      Maternal childhood adversity, prepregnancy obesity and gestational weight gain.
      Child outcomes also relied on maternal report, which may reflect biases that vary by race and gender. The study included siblings, and although fixed-effects models accounted for shared variance among siblings to the extent that confounders are consistent across pregnancies, three-way interactions could not be tested in these models because of small sample sizes. Hispanics were also omitted from this investigation given small cell sizes. Future studies should include measured or validated reports of maternal weights; adequate samples of Hispanics and other racial/ethnic groups; additional reporters (such as teachers) and objective measures of child problems assessed by trained professionals (such as diagnostic testing); and adequate measures of mediators.
      Study strengths include longitudinal follow-up of a large, longitudinal, intergenerational sample and assessment of effect modification by gender during an understudied and important developmental period.
      • Paus T.
      • Keshavan M.
      • Giedd J.N.
      Why do many psychiatric disorders emerge during adolescence?.
      • Lacourse E.
      • Côté S.
      • Nagin D.S.
      • Vitaro F.
      • Brendgen M.
      • Tremblay R.E.
      A longitudinal-experimental approach to testing theories of antisocial behavior development.
      The validated survey instrument allowed investigation of total, externalizing, and internalizing problems, instead of limiting this investigation to a single outcome.

      Conclusions

      Prepregnancy Class II and Class III obesity have recently doubled and tripled, respectively, in the U.S.
      National Academy of Medicine, National Research Council
      Weight Gain During Pregnancy: Reexamining the Guidelines.
      , and the behavioral problems studied here have implications for poor mental health trajectories through adolescence and into adulthood.
      • Holbrook J.R.
      • Cuffe S.P.
      • Cai B.
      • et al.
      Persistence of parent-reported ADHD symptoms from childhood through adolescence in a community sample.
      • Kessler R.C.
      • Amminger G.P.
      • Aguilar-Gaxiola S.
      • Alonso J.
      • Lee S.
      • Ustün T.B.
      Age of onset of mental disorders: a review of recent literature.
      In this large U.S. sample of children aged 9–11 years, maternal prepregnancy weight, particularly severe obesity, was related to markedly higher behavioral problems in boys. These results add new evidence that attaining and maintaining a healthy weight before pregnancy is crucial for children’s development.

      Acknowledgments

      The authors thank Stephanie Leonard and the University of California, Berkeley, National Longitudinal Survey of Youth – Adverse Childhood Events team for their helpful comments on analytic strategies and other aspects of the manuscript. This research was supported by Award Number R01MD006104 from the National Center on Minority Health and Health Disparities. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Center on Minority Health and Health Disparities or NIH. NIH had no role in study design; collection, analysis, and interpretation of data; writing the report; or the decision to submit the report for publication. This research was conducted with restricted access to Bureau of Labor Statistics data. The views expressed here do not reflect the views of the Bureau of Labor Statistics.
      JD collaborated on the conceptualization of the paper, guided the statistical approach, and interpreted the results. She oversaw all aspects of the study and the writing and takes full and final responsibility for the paper. LS prepared, analyzed, and interpreted the data. She assisted with writing the methods and results sections and wrote sections of the introduction and conclusion. LP helped determine the appropriate analytic approach and assisted with analyses; she wrote sections of the methods and results. HK assisted with the original conceptualization of the paper and conducted early analyses and writing; she provided critical feedback on the final paper. BA is the senior author on the paper; she secured funding for the study and has been involved in all aspects of the paper from conceptualization to analyses to writing. All authors critically read, provided feedback, and edited the final paper.
      No financial disclosures were reported by the authors of this paper.

      Appendix A. Supplementary material

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