Antenatal determinants of early childhood talking delay and behavioural difficulties

Infant Behavior and Development 57 (2019) 101388

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Antenatal determinants of early childhood talking delay and behavioural difficulties

T

Stephanie D’Souzaa,b,e, Caitlin N. Crawforda, Jude Buckleya, Lisa Underwoodb, Elizabeth R. Petersona,b, Amy Birdd, Susan M.B. Mortonb,c, Karen E. Waldiea,b,⁎ a

School of Psychology, The University of Auckland, Auckland, New Zealand Centre for Longitudinal Research - He Ara ki Mua, The University of Auckland, Auckland, New Zealand c School of Population Health, The University of Auckland, Auckland, New Zealand d School of Psychology, University of Wollongong, NSW, Australia e Centre of Methods and Policy Application in the Social Sciences, University of Auckland, Auckland, New Zealand b

ARTICLE INFO

ABSTRACT

Keywords: Antenatal Childhood Language delay Behaviour Longitudinal Comorbidity Milestone

The determinants of talking delay alone or its comorbidity with behavioural difficulties was examined in 5768 two-year-old members of the Growing Up in New Zealand longitudinal study. Using the MacArthur-Bates Communicative Development inventories and the total difficulties score from the preschool Strengths and Difficulties Questionnaire, a composite measure was created so that children were categorised as showing no language or behavioural concerns (72.5%), behavioural only difficulties (6.1%), language only difficulties (18.1%), and comorbid language and behavioural difficulties (3.3%). Analyses revealed that antenatal factors such as maternal perceived stress, inadequate folate intake, vitamin intake, alcohol consumption during the first trimester and maternal smoking all had a significant effect on child outcomes. In particular, low multivitamin intake and perceived stress during pregnancy were associated with coexisting language and behavioural difficulties. These findings support international research in showing that maternal factors during pregnancy are associated with developmental outcomes in the early childhood period, and demonstrate these associations within a NZ context. Interventions which address maternal stress management and health behaviours during pregnancy could be beneficial to offspring development.

1. Introduction Young children with language and behavioural difficulties are at increased risk of adverse outcomes across health (Fergusson, Horwood, & Ridder, 2007; Odgers et al., 2007), psychosocial (Botting & Conti-Ramsden, 2000; Fergusson, Horwood, & Ridder, 2005; Schoon, Parsons, Rush, & Law, 2010), social-relational (Clegg, Hollis, Mawhood, & Rutter, 2005; Fanti & Henrich, 2010), academic (Duncan et al., 2007; Yew & O’Kearney, 2013) and employment (Law, Rush, Schoon, & Parsons, 2009; Narusyte, Ropponen, Alexanderson, & Svedberg, 2017) domains and these difficulties can persist through life. The co-occurrence of language and behavioural difficulties in children is well documented (Benner, Nelson, & Epstein, 2002; Plomin, Price, Eley, Dale, & Stevenson, 2002; Tervo, 2007). Research suggests that child, and parent-child interaction factors (Carpenter & Drabick, 2011; Hartas, 2011), shared neurobiology

⁎

Corresponding author at: School of Psychology, Faculty of Science; University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand. E-mail address: [email protected] (K.E. Waldie).

https://doi.org/10.1016/j.infbeh.2019.101388 Received 24 April 2019; Received in revised form 3 October 2019; Accepted 4 October 2019 0163-6383/ © 2019 Elsevier Inc. All rights reserved.

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(Tomblin & Mueller, 2012), and community and family-related factors (Hughes, Sciberras, & Goldfeld, 2016) play key roles in explaining the co-occurrence of language and behavioural difficulties. Factors known to be associated with comorbidity of language and behavioural difficulties include children with poor emotion regulations skills or working memory deficits (Carpenter & Drabick, 2011), low parental responsiveness (Hartas, 2011), and families living in poverty or with drug or alcohol misuse (Anda et al., 1999). However, little is known about antenatal factors that predict the co-occurrence of these problems, though several antenatal factors have been linked to language and behavioural outcomes separately. These factors include antenatal maternal mental health (D’Souza et al., 2016; D’Souza, Waldie, Peterson, Underwood, & Morton, 2019; Koutra et al., 2017; Laplante et al., 2004) and lifestyle factors (Chatzi et al., 2012; Molloy, Kirke, Brody, Scott, & Mills, 2008; Roebuck, Mattson, & Riley, 1998; Schoeps et al., 2018). 1.1. Maternal mental health Poor maternal mental health during pregnancy is associated with a variety of adverse neurodevelopmental outcomes in childhood (e.g., Buss, Davis, Muftuler, Head, & Sandman, 2010; D’Souza et al., 2016, 2019; Gutteling et al., 2006; O’Connor et al., 2005; O’Connor, Monk, & Fitelson, 2014; Waldie et al., 2014). The association between maternal mental health and child outcomes is complex, and not all studies have found a link between the two (Bernard-Bonnin, 2004). Much research, however, shows that antenatal depression and stress adversely influence a spectrum of childhood cognitive and behavioural disorders (e.g., Bergman, Sarkar, O’Connor, Modi, & Glover, 2007; Buss et al., 2010). For instance, antenatal depression is linked to impaired prosocial behaviour, increased hyperactivity, and peer relationship difficulties in offspring (Batenburg‐Eddes et al., 2013; Koutra et al., 2017; Velders et al., 2011; Waters, Hay, Simmonds, & van Goozen, 2014). Depression during pregnancy also appears to increase the risk of the child experiencing language difficulties (Sohr-Preston & Scaramella, 2006). Similarly, elevated antenatal maternal stress is associated with delayed language development in infancy (Davis & Sandman, 2010) and lower language skills in early and middle childhood (D’Souza et al., 2016; Laplante et al., 2004; Laplante, Brunet, Schmitz, Ciampi, & King, 2008), and has been associated with internalising and externalising problems in 2 year olds (Gutteling et al., 2005). Furthermore, the effects of high stress during pregnancy appear to confer a greater risk of developing language difficulties (Laplante et al., 2008) and behavioural problems in childhood, even after controlling for the effects of postnatal mental health and other antenatal, obstetric and psychosocial risks (Davis & Sandman, 2010; O’Connor, Heron, Golding, Beveridge, & Glover, 2002). 1.2. Maternal lifestyle factors Maternal micronutrient intake (folic acid and vitamins) has been linked to children’s language outcomes. For instance, folic acid supplementation prior to conception and during pregnancy is associated with improved receptive and expressive communication skills in children at 18 months (Chatzi et al., 2012), whereas a lack of periconceptional folic acid supplementation has been associated with significant language delays in children at 3 years of age (Roth et al., 2011). The lack, or delay, in initiating folic acid use during pregnancy has also been linked to internalising behavioural problems, increased levels of hyperactivity, and peer problems in infancy and early childhood (Roza et al., 2010; Steenweg-de Graaff et al., 2012). Together, this work suggests that periconceptional folic acid intake may be essential for promoting optimal neurodevelopment, thereby contributing to behaviour and language development (Schmidt et al., 2012). Deficient intake of other vitamins during pregnancy has also been linked to adverse language and behavioural outcomes in children (Veena et al., 2016). For instance, vitamin D insufficiency during pregnancy is associated with significant language impairment in children at 5 and 10 years of age but not with internalising and externalising behavioural difficulties (Whitehouse et al., 2012). Similarly, vitamin B12 deficiency during pregnancy negatively impacts brain development in infancy (Benton, 2012) and is associated with lower receptive language skills at age 3 years (Villamor, Rifas‐Shiman, Gillman, & Oken, 2012). Higher serum concentrations of antioxidant vitamins (vitamins A and E) in maternal blood and cord blood after delivery have been positively associated with children’s language and behavioural development in the first two years of life (Chen et al., 2009). Other maternal lifestyle factors, such as smoking and alcohol intake during pregnancy, have been linked to adverse language outcomes. For example, prenatal exposure to smoking has been associated with poor language development (Wehby, Prater, McCarthy, Castilla, & Murray, 2011), such as a lower ability to discriminate between sounds and a delayed response to sound after birth (Key et al., 2007). Maternal smoking during pregnancy also confers an increased risk of language impairment and poor performance on language tasks (Eicher et al., 2013) that adversely impact later language skills (Molfese, 2000). Some studies have also found an association between prenatal alcohol exposure and language difficulties, though findings are generally mixed (O’Keeffe, Greene, & Kearney, 2014). Considerable research has shown an association between prenatal nicotine exposure and higher likelihood for attention-deficit/ hyperactivity disorder (ADHD) or ADHD symptoms (see Rosenthal & Weitzman, 2011; Tiesler & Heinrich, 2014 for reviews). Likewise, there is strong evidence linking maternal smoking during pregnancy to conduct or externalising behaviour problems (e.g., Herrmann, King, & Weitzman, 2008; Wakschlag, Pickett, Cook, Benowitz, & Leventhal, 2002). The increased risk for externalising problems in children of mothers who smoked during pregnancy is present from very early childhood (Brion et al., 2010; Stene-Larsen, Borge, & Vollrath, 2009). Moreover, in non-smoking mothers, exposure to environmental tobacco smoke during pregnancy is associated with higher symptom scores for conduct disorder in children (Gatzke-Kopp & Beauchaine, 2007). Although less consistent, there is evidence that prenatal exposure to nicotine is associated with internalising behaviour problems in children and adolescents even after controlling for covariates (Ashford, van Lier, Timmermans, Cuijpers, & Koot, 2008). The link between high alcohol intake and deleterious effects on children’s cognitive and behavioural development is well 2

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established (O’Leary, 2004). However, research has yet to reach a consensus on the effects of moderate to low levels of exposure to alcohol on child outcomes. Nonetheless, there is some evidence that even low-level prenatal alcohol exposure (< 1 drink per day) may adversely impact neurodevelopment (Flak et al., 2014; Williams & Ross, 2007). For instance, low to moderate levels of prenatal alcohol exposure have been linked to adverse behavioural outcomes in children (Flak et al., 2014; Sood et al., 2001). 1.3. The foetal programming hypothesis A dominant mechanism thought to underlie the association between antenatal factors and child outcomes is the foetal programming hypothesis (Barker, 1998; Beydoun & Saftlas, 2008). This hypothesis assumes that exposure to adverse conditions (e.g. poor maternal mental health or adverse lifestyle factors) during the antenatal period (i.e. a time of rapid neurodevelopment) can impact brain functioning, thereby influencing children’s developmental outcomes later on in life. Specifically, this adverse gestational environment can occur as a result of maternal nutrition (e.g. antenatal supplements) (Eyles et al., 2009; Roza et al., 2010), hormones (as a result of stress or depression) (Beydoun & Saftlas, 2008; Field et al., 2004), or exposure to toxins (e.g. smoking or alcohol) (Huizink & Mulder, 2006). Given that foetal programming is thought to underlie the links between antenatal factors and both behavioural and language outcomes (when evaluated separately), one can assume that these factors may also be associated with the co-occurrence of language and behavioural difficulties in children (Andersen, 2003; Beydoun & Saftlas, 2008; Burdge & Lillycrop, 2010). 1.4. Child characteristics and sociodemographic factors Child characteristics and sociodemographic factors have been linked to child developmental outcomes (Bradley & Corwyn, 2002; Sommerfelt, Ellertsen, & Markestad, 1993). For instance, low birth weight (Stanton-Chapman, Chapman, Bainbridge, & Scott, 2002) and low levels of maternal education have been associated with early language impairment (Reilly et al., 2010). Moreover, an increased risk of language delay and behaviour problems have been linked to children of ethnic minority status (Deater–Deckard, Dodge, Bates, & Pettit, 1998; Neisser et al., 1996) and those born preterm (Arpi & Ferrari, 2013; Caesar et al., 2016). Socioeconomic disadvantage has also been associated with behaviour problems throughout childhood (Fitzsimons, Goodman, Kelly, & Smith, 2017). On the other hand, increasing maternal age is associated with children having better language, and fewer behavioural difficulties (Sutcliffe, Barnes, Belsky, Gardiner, & Melhuish, 2012). The effects of gender (Gao, Paterson, Abbott, Carter, & Iusitini, 2007) and parity (Oshima‐Takane, Goodz, & Derevensky, 1996) on childhood outcomes appear equivocal. 1.5. The present study The literature indicates that antenatal maternal health and lifestyle factors can influence the risk of a child developing behavioural and language problems. However, despite evidence of maternal antenatal factors independently impacting language and behavioural development, there is a dearth of knowledge regarding the influence of maternal mental health and lifestyle on the comorbidity of language and behaviour difficulties in childhood. Based on the foetal programming hypothesis, the mechanism thought to underlie these associations, one can hypothesise that these antenatal factors would also be associated with showing comorbid language and behavioural difficulties. Towards this end, the aim of the present study was to examine whether antenatal factors that have been separately associated with language and behavioural problems are also risk factors for the co-occurrence of language and behavioural problems in children at two years of age. This will be examined while also controlling for child characteristics and sociodemographic factors that have been associated with language and behavioural outcomes. 2. Methods 2.1. Participants Participants in the study were members of the Growing Up in New Zealand birth cohort. Details of the study’s design and recruitment procedure can be found elsewhere (2014, Morton et al., 2013). Briefly, the study’s cohort consists of a socioeconomically and ethnically diverse sample of children, born to 6822 mothers who resided within the geographical regions covered by Auckland, Counties-Manukau or Waikato district health boards (Morton et al., 2013). All children born to mothers with expected delivery dates between 25th April 2009 and 25th March 2010 within these three district health board areas were eligible for inclusion within the study. No other inclusion or exclusion criteria were applied (Morton et al., 2010). Children within the study are broadly generalizable to current NZ births (Morton et al., 2015). Major data collection waves (DCWs) have occurred during the late antenatal period (i.e. third trimester), and when the child was aged 9 months and 2 years. Computer Assisted Personal Interviews (CAPIs) were used at each face to face DCW to gather information relating to six inter-connected domains of child development: health and wellbeing; cognitive and psychosocial; education; family and whānau (extended family); culture and identity; and neighbourhoods and societal context. Ethical approval was granted from the Ministry of Health Northern Y Regional Ethics Committee (NTY/08/06/055), and mothers provided written informed consent for their own and their children’s participation in the study. The sample for this study included children who had mother-reported data available for language and behaviour, our outcomes of interest, at the 2 year DCW (N = 5768). Compared to children included in the study sample, children not included in the sample were 3

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more likely to have mothers who showed significant depressive symptoms, did not take folate or multivitamins during pregnancy, were of non-European ethnicity, were under 30 years and had only a secondary school or no secondary school education (p < 0.01). Children not included in the sample also had mothers who experienced greater perceived stress and were more likely to have exposure to second hand smoke during pregnancy (p < 0.01). Children not included in the sample were also less likely to be first born children or part of a planned pregnancy, and were more likely to have a low birth weight or be born preterm (p < 0.05). 2.2. Measures 2.2.1. Comorbidity of language and behavioural difficulties Language skills in children were assessed at 2 years using the MacArthur-Bates Communicative Development inventories (CDIs; Fenson, Marchman, Thal, Dale, & Reznick, 2007). In the current study, children’s total CDI score was converted into a z-score and those who fell one standard deviation below the mean were then categorised as showing delayed talking, with all other children classified as not delayed. This method is based on the procedure used to identify those with borderline intellectual functioning or less when using IQ scores (Alloway, 2010). Behavioural difficulties were assessed using the total difficulties score from the mothers’ report of the preschool Strengths and Difficulties Questionnaire (SDQ; Goodman, 1997). The SDQ measures four difficulties subscales (emotional symptoms, peer problems, hyperactivity-inattention and conduct problems) as well as a strengths-based prosocial behaviour subscale. The total difficulties score is the combined score for the four difficulties subscale, and therefore encompasses both internalising (emotional symptoms) and externalising (hyperactivity-inattention, conduct problems) difficulties. The score ranges from 0 to 40, with higher scores reflecting greater total behavioural difficulties. We have previously found that preschool SDQ shows acceptable psychometric properties in the current cohort at 2 years, with a Cronbach’s alpha of 0.84 (D’Souza, Waldie, Peterson, Underwood, & Morton, 2017; D’Souza, Waldie, Peterson, Underwood, & Morton, 2017). In the current study, the SDQ total difficulties were dichotomised into normal/borderline and abnormal, based on whether scores fell into the clinically significant abnormal range (i.e. within the 90th percentile; D’Souza et al., 2017a; Goodman, 1997). To obtain a measure of comorbidity between language and behavioural difficulties, a composite measure was created using the 2 year categorised CDI language (i.e., delayed & not delayed talking) and SDQ total difficulties (i.e., normal/borderline & abnormal) measures. Children were categorised as showing no language or behavioural concerns, behavioural only difficulties, language only difficulties, and comorbid language and behavioural difficulties. 2.2.2. Maternal mental health Information relating to maternal mental health during pregnancy was obtained during the antenatal DCW. Antenatal depression was measured using the Edinburgh Postnatal Depression scale (EPDS; Cox, Holden, & Sagovsky, 1987). The scale ranges from 0 to 30, with women who scored 13 or greater categorised as having clinically significant depressive symptoms (Waldie et al., 2015). Prenatal perceived stress in mothers was measured using the Perceived Stress Scale (PSS), which measures the degree to which one perceives their lives as being unpredictable, overloaded and uncontrollable in the month prior (Cohen, Kamarck, & Mermelstein, 1983). Scores for the PSS range from 0 to 40, with higher scores reflective of greater perceived stress. Cronbach’s alpha coefficients were satisfactory for both the EDPS and PSS, with values of 0.85 and 0.87 respectively. 2.2.3. Maternal lifestyle factors The antenatal questionnaire asked mothers about their intake of folate or folic acid. Specifically, mothers were asked about intake before pregnancy, during the first trimester, and after the first trimester. It is recommended that women should begin taking folic acid supplements at least 4 weeks prior to when they intend on becoming pregnant and continue throughout the first trimester (Stewart, 2006). Therefore, in the current study, a composite variable was created to indicate whether mothers took folate or folic acid supplements during the recommended period. Mothers were categorised as taking folic acid before and during the first trimester, during the first trimester only, and taking no folic acid. Information was also obtained on whether or not mothers took multivitamins during pregnancy. Smoking behaviour during pregnancy (categorised as never smoked, stopped smoking, and continued smoking) as well as frequency of exposure to another smoker in the same room (categorised as no exposure vs some exposure) were also assessed at the antenatal DCW. Information on prenatal alcohol intake, both during the first trimester and after the first trimester, was also obtained. Women were dichotomised as being non-drinkers or consuming 1 drink or more per week. Only maternal alcohol consumption during the first trimester is included in the current study due to low observed cell counts when cross-tabulating comorbidity of language and behavioural difficulties and alcohol consumption after the first trimester (data not shown). 2.2.4. Child characteristics and sociodemographic factors Several sociodemographic and child characteristic variables were adjusted for in the current study. These included mother’s ethnicity (European, Maori, Pacific, Asian/Other), mother’s education (no secondary school, secondary school/diploma/trade certificate, Bachelor’s degree or higher), mother’s age when pregnant (< 20 years, 20–29 years, > 30 years), parity (first born or subsequent birth), whether or not the pregnancy was planned, and area-level deprivation at the 2 year DCW. Area-level deprivation was measured using the NZDep2006, based on indicators of socioeconomic deprivation from the 2006 NZ census. Based on scores from these indicators, census areas known as meshblocks are given a decile value ranging from 1 (least deprived) to 10 (most 4

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deprived) (Salmond, Crampton, & Atkinson, 2007). In the current study, deprivation was categorised into high (deciles 8–10), medium (deciles 4–7), and low (deciles 1–3) deprivation. Child’s gender, gestational age (preterm: < 37 weeks or term: > 37 weeks), birthweight (low: < 2500 g, appropriate: 2500–4000 g, high: > 4000 g) and age in months at the 2 year DCW were also included in the analyses (Bird et al., 2017). 2.3. Data analysis Bivariate associations between comorbidity of language and behavioural difficulties and other variables were examined using analysis of variance (for continuous variables) and chi-square tests (for categorical variables). A multinomial logistic regression was then conducted to evaluate the predictors of showing difficulties in either language, behaviour, or both outcomes. Comorbidity of language and behavioural difficulties was specified as the outcome variable and all prenatal variables were included in the model, with the analysis adjusting for the aforementioned child characteristics and sociodemographic factors. As the multinomial logistic regression uses casewise deletion, resulting in the removal of cases with any missing data, multiple imputation was used to account for missing data for this analysis. Five imputed datasets were created from the original data and results are reported pooled across all five datasets. Analyses were carried out using R version 3.3.1 and SPSS version 25, and statistical significance was given at an alpha level of 0.05. 3. Results Of the 5768 children in our sample, 4180 were categorised as showing no language or behavioural concerns (72.5%), 353 showed behavioural only difficulties (6.1%), 1046 had language only difficulties (18.1%), and 189 had both behavioural and language difficulties (3.3%). Descriptive information for predictors and control variables across the comorbidity variable are presented in Tables 1 and 2; Table 1 presents this information for continuous variables, while Table 2 shows descriptive information for categorical variables. Bivariate associations between predictors or control variables and the comorbidity variable are also presented in Tables 1 and 2. All variables were significant associated with comorbidity of language and behavioural difficulties, except for parity and birthweight. Results from the multinomial logistic regression on the imputed data are presented in Table 3. Results using the original data are presented in the Supplementary Material (Table S1). Our analysis found that maternal perceived stress during pregnancy was associated with an increased odds of showing behavioural only difficulties (OR = 1.05, p < 0.01) compared to no difficulties. Greater antenatal perceived stress was also associated with an increased odds of showing comorbid difficulties in talking and behaviour (OR = 1.06, p < 0.01) compared to no difficulties. Relative to children whose mothers took folate periconceptionally (i.e. pre-pregnancy and in the first trimester), children whose mothers took no folate had a 1.60 increased odds of showing language only difficulties than no difficulties (p < 0.01). Lack of antenatal multivitamin intake was a significant risk factor for comorbid difficulties; children whose mothers took no multivitamins during pregnancy had a 1.56 increased odds of comorbid difficulties than no difficulties, relative to children whose mothers took multivitamins (p < 0.05). Children whose mothers continued smoking during pregnancy had an increased odds of showing behavioural only difficulties than no difficulties, relative to children whose mothers never smoked (OR = 1.66, p < 0.01). Alcohol consumption during the first trimester was associated with a reduced odds of children showing language only difficulties than no difficulties (OR = 0.61, p < 0.01) Several sociodemographic factors were also identified as significant risk factors for behavioural and/or language difficulties. Children whose mothers were of Maori, Pacific or Asian/Other ethnicities all had an increased odds of showing behavioural only, language only and comorbid difficulties than no difficulties (ps < 0.01), with effect sizes ranging from small to large (see Table 3; Chen, Cohen, & Chen, 2010). Maternal education lower than a Bachelor’s degree was associated with an increased odds of showing behavioural only difficulties than no difficulties (ps < 0.01). Compared to children whose mothers received a Bachelor’s degree or higher, children whose mothers only received a secondary school education had an increased odds of showing language only difficulties (p < 0.05) and children whose mothers did not finish secondary school had an increased odds of showing comorbid difficulties (p < 0.05). Children from medium and high deprivation areas also had an increased odds of showing language only difficulties relative to children from low deprivation areas (ps < 0.01). Older maternal age (30 years and over) was associated with a reduced odds of a child showing behavioural only difficulties than no difficulties, when compared to children with teenage mothers at birth (ps < 0.01). Females also had reduced odds of behavioural only, language only and comorbid difficulties than no difficulties Table 1 Descriptive statistics and bivariate associations between continuous variables and comorbidity in language and behavioural difficulties.

Prenatal perceived stress Child’s age at 2 years (days)

No difficulties M (SD)

Behavioural only difficulties M (SD)

Language only difficulties M (SD)

Comorbid difficulties M (SD)

F- value

12.47 (6.18) 26.76 (1.80)

16.84 (6.40) 27.69 (2.80)

13.03 (6.37) 27.19 (2.39)

16.48 (6.49) 27.34 (2.45)

64.59** 35.35**

Note: **p < 0.01. 5

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Table 2 Descriptive statistics and bivariate associations between categorical variables and comorbidity of language and behavioural difficulties.

Prenatal depression Not depressed Depressed Folate intake Pre-pregnancy and first trimester Pre-pregnancy or first trimester No folate intake Multivitamin intake Multivitamins No multivitamins Prenatal smoking Non-smoker Stopped smoking Continued smoking Exposure to another smoker No exposure Some exposure Alcohol in 1st trimester Non-drinker 1 or more drinks Mother’s ethnicity European Maori Pacific Asian/Other Mother’s education No secondary school Secondary school Diploma or trade certificate Bachelor’s degree or higher Mother’s age < 20 years 20 to 29 years 30 years and over Parity First born Subsequent birth Planned pregnancy Yes No Area-level deprivation Low Medium High Child’s gender Male Female Gestational age Preterm Term Birthweight Low Appropriate High

No difficulties N (%)

Behaviour only difficulties N (%)

Language only difficulties N (%)

Comorbid difficulties N (%)

3451 (90.4) 366 (9.6)

231 (76.7) 70 (23.3)

827 (87.0) 124 (13.0)

133 (79.2) 35 (20.8)

71.82**

1772 (46.5) 1613 (42.3) 427 (11.2)

57 (19.0) 154 (51.3) 89 (29.7)

269 (28.3) 422 (44.4) 260 (27.3)

26 (15.5) 70 (41.7) 72 (42.9)

373.05**

2543 (66.6) 1273 (33.4)

136 (45.3) 164 (54.7)

505 (53.1) 446 (46.9)

58 (34.5) 110 (65.5)

155.92**

3186 (83.7) 334 (8.8) 285 (7.5)

172 (57.3) 48 (16.0) 80 (26.7)

765 (80.6) 98(10.3) 86 (9.1)

122 (72.6) 23 (13.7) 23 (13.7)

161.19**

3624 (95.0) 192 (5.0)

247 (82.1) 54 (17.9)

884 (93.1) 66 (6.9)

148 (88.1) 20 (11.9)

88.54**

3596 (86.2) 576 (13.8)

278 (79.0) 74 (21.0)

945 (90.8) 96 (9.2)

155 (83.3) 31 (16.7)

35.28**

2869 (68.8) 464 (11.1) 289 (6.9) 546 (13.1)

112 (31.8) 102 (29.0) 92 (26.1) 46 (13.1)

317 146 247 332

(30.4) (14.0) (23.7) (31.9)

31 33 81 43

(16.5) (17.5) (43.1) (22.9)

991.32**

204 (4.9) 823 (19.7) 1220 (29.2) 1927 (46.2)

57 (16.2) 104 (29.5) 145 (41.2) 46 (13.1)

61 (5.9) 292 (28.0) 324 (31.1) 364 (35.0)

23 60 64 39

(12.4) (32.3) (34.4) (21.0)

269.27**

131 (3.1) 1417 (33.9) 2632 (63.0)

44 (12.5) 190 (53.8) 119 (33.7)

42 (4.0) 440 (42.1) 563 (53.9)

15 (7.9) 105 (55.6) 69 (36.5)

263.89**

1798 (43.1) 2378 (56.9)

146 (41.5) 206 (58.5)

429 (41.1) 615 (58.9)

74 (39.4) 114 (60.6)

2.28

2791 (67.0) 1374 (33.0)

134 (38.1) 218 (61.9)

584 (56.3) 454 (43.7)

85 (45.7) 101 (54.3)

165.6**

1334 (32.6) 1612 (39.4) 1143 (28.0)

52 (15.0) 101 (29.2) 193 (55.8)

180 (17.6) 348 (34.1) 494 (48.3)

24 (12.8) 41 (21.8) 123 (65.4)

336.82**

2069 (49.5) 2111 (50.5)

191 (54.1) 162 (45.9)

622 (59.5) 424 (40.5)

113 (59.8) 76 (40.2)

39.04**

190 (4.6) 3983 (95.4)

16 (4.5) 337 (95.5)

69 (6.6) 975 (93.4)

8 (4.3) 180 (95.7)

7.87*

139 (3.3) 3336 (79.9) 702 (16.8)

9 (2.5) 283 (80.2) 61 (17.3)

53 (5.1) 806 (77.1) 187 (17.9)

7 (3.7) 150 (79.4) 32 (16.9)

9.62

X2

Note: **p < 0.01, *p < 0.05.

when compared to males (ps < 0.05). Children born at term had a reduced odds of showing language only difficulties than no difficulties relative to preterm children (p < 0.05). Older age of the child (in days) at the 2 year DCW was associated with an increased odds of behavioural only difficulties than no difficulties (OR = 1.06, p < 0.01). 4. Discussion The aim of the present study was to determine the associations between antenatal maternal mental health and lifestyle factors and comorbid early childhood language and behavioural difficulties. Given that antenatal factors have been previously associated with both language and behavioural difficulties separately, we were interested in testing whether these factors also predicted comorbidity 6

Prenatal perceived stress Prenatal depression Not depressed Depressed Folate intake Pre-pregnancy and first trimester Pre-pregnancy or first trimester No folate intake Multivitamin intake Multivitamins No multivitamins Prenatal smoking Non-smoker Stopped smoking Continued smoking Exposure to another smoker No exposure Some exposure Alcohol in 1st trimester Non-drinker 1 or more drinks Mother’s ethnicity European Maori Pacific Asian/Other Mother’s education No secondary school Secondary school Diploma or trade certificate Bachelor’s degree or higher Mother’s age < 20 years 20 to 29 years 30 years and over 2.86 2.31 2.64

0.69 0.46

−0.38 (0.22) −0.79 (0.25)

1.31

0.27 (0.19)

1.05 (0.25) 0.84 (0.20) 0.97 (0.19)

1.25 1.66

0..22 (0.19) 0.51 (0.18)

2.37 3.39 2.27

1.09

0.08 (0.14)

0.86 (0.17) 1.22 (0.19) 0.82 (0.19)

1.09 1.09

0.09 (0.18) 0.08 (0.23)

0.91

0.99

−0.00 (0.19)

−0.09 (0.16)

1.05

0.05 (0.01)

7 0.45-1.06 0.28-0.74

1.75-4.69 1.56-3.44 1.83-3.81

1.69-3.31 2.34-4.92 1.55-3.32

0.67-1.24

0.90-1.91

0.87-1.80 1.17-2.36

0.83-1.41

0.77-1.55 0.69-1.70

0.68-1.45

1.03-1.08

2.95 10.06**

17.38** 17.13** 26.71**

25.37** 41.63** 17.93**

0.35

1.98

1.42 8.00**

0.36

0.24 0.14

0.003

15.65**

Wald

−0.03 (0.21) −0.04 (0.22)

−0.03 (0.19) 0.22 (0.11) 0.07 (0.10)

0.79 (0.13) 1.60 (0.13) 1.58 (0.10)

−0.49 (0.13)

0.04 (0.17)

0.06 (0.13) 0.03 (0.16)

0.06 (0.09)

0.12 (0.10) 0.47 (0.14)

0.03 (0.13)

−0.01 (0.01)

0.97 0.96

0.97 1.25 1.08

2.21 4.93 4.84

0.61

1.04

1.06 1.03

1.07

1.13 1.60

1.07

0.99

OR

0.65-1.46 0.63-1.47

0.67-1.39 1.02-1.54 0.89-1.30

1.72-2.83 3.82-6.35 3.99-5.87

0.48-0.79

0.74-1.44

0.81-1.38 0.76-1.41

0.90-1.27

0.93-1.39 1.21-2.10

0.83-1.39

0.98-1.01

95% CI

B (SE)

95% CI

B (SE)

OR

No difficulties vs Language difficulties

No difficulties vs Behavioural difficulties

0.02 0.03

0.03 4.50* 0.58

38.23** 151.09** 257.35**

14.58**

0.04

0.17 0..04

0.52

1.46 11.25**

0.29

0.99

Wald

−0.19 (0.33) −0.60 (0.36)

0.40 (0.34) 0.32 (0.24) 0.26 (0.23)

1.18 (0.29) 2.32 (0.27) 1.81 (0.26)

−0.01 (0.22)

0.17 (0.28)

−0.12 (0.27) −0.17 (0.30)

0.44 (0.19)

0.18 (0.30) 0.55 (0.34)

−0.06 (0.24)

0.06 (0.02)

B (SE)

0.83 0.55

1.48 1.38 1.29

3.27 10.13 6.11

0.99

1.19

0.89 0.85

1.56

1.20 1.74

0.86

1.06

OR

0.34 2.74

1.39* 1.74 1.23

17.06** 73.53** 49.36**

0.001

0.36

0.19 0.33

5.39*

0.36 2.65

0.38

11.71**

Wald

(continued on next page)

0.43-1.57 0.27-1.12

0.77-2.86 0.86-2.22 0.82-2.03

1.86-5.72 5.96-17.19 3.69-10.13

0.64-1.54

0.68-2.07

0.53-1.51 0.47-1.52

1.07-2.26

0.66-2.19 0.88-3.42

0.54-1.38

1.02-1.09

95% CI

No difficulties vs Comorbid difficulties

Table 3 Results from the pooled multinomial logistic regression, evaluating factors associated with behavioural only, language only and comorbid difficulties relative to no difficulties.

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8

Note: **p < 0.01, *p < 0.05.

First born Subsequent birth Planned pregnancy Yes No Area-level deprivation Low Medium High Child’s gender Male Female Gestational age Preterm Term Birthweight Low Appropriate High Child’s age (2 years)

Parity

Table 3 (continued)

Wald

1.03 1.16 1.01 1.23 0.79 0.86 0.62 1.06 1.06

0.01 (0.13)

0.07 (0.14)

0.01 (0.18) 0.21 (0.19)

−0.10 (0.12)

−0.07 (0.32)

−0.48 (0.41)

0.06 (0.16) 0.06 (0.02)

0.78-1.44 1.02-1.11

0.28-1.37

0.46-1.61

0.62-0.99

0.71-1.45 0.86-1.77

0.88-1.54

0.79-1.33

0.13 6.79**

1.40

0.24

4.17*

0.01 1.24

1.11

0.04

0.10 (0.10) 0.001 (0.02)

0.13 (0.21)

−0.17 (0.18)

−0.20 (0.08)

0.23 (0.11) 0.47 (0.11)

−0.01 (0.09)

−0.01 (0.08)

1.10 1.00

1.13

0.68

0.63

1.26 1.60

0.97

0.97

OR

0.90-1.34 0.97-1.04

0.76-1.70

0.48-0.97

0.54-0.73

1.02-1.55 1.28-1.99

0.81-1.16

0.83-1.14

95% CI

B (SE)

95% CI

B (SE)

OR

No difficulties vs Language difficulties

No difficulties vs Behavioural difficulties

0.89 0.94

0.37

4.42*

37.24**

4.78* 17.53**

0.14

0.11

Wald

−0.08 (0.21) −0.03 (0.03)

0.15 (0.47)

0.02 (0.44)

−0.23 (0.16)

−0.18 (0.27) 0.37 (0.26)

−0.05 (0.18)

−0.01 (0.18)

B (SE)

0.93 0.98

1.16

1.04

0.59

0.84 1.44

0.89

0.98

OR

0.61-1.41 0.91-1.04

0.46-2.92

0.44-2.46

0.43-0.81

0.49-1.42 0.86-2.42

0.62-1.26

0.69-1.39

95% CI

No difficulties vs Comorbid difficulties

0.13 0.52

0.10

0.01

10.96**

0.44 1.94

0.45

0.01

Wald

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with these outcomes. Overall, multivariable analysis revealed that the most significant antenatal determinants of adverse 2-year old outcomes included antenatal perceived stress, periconceptional folate and multivitamin intake, and alcohol and smoking during pregnancy. However, not all of these factors predicted comorbidity of language and behavioural difficulties. 4.1. Maternal mental health Antenatal maternal perceived stress was associated with behavioural problems only as well as with co-existing behavioural and language difficulties. This is consistent with earlier work indicating that antenatal perceived stress is associated with adverse cognitive (Brouwers, van Baar, & Pop, 2001; Laplante et al., 2004) and behavioural (O’Connor et al., 2002; O’Connor, Heron, Golding, Glover, & the AL SPAC Study Team, 2003; Slykerman et al., 2015; Van den Bergh & Marcoen, 2004) outcomes. Although antenatal stress was significant in our multivariable results, antenatal depression was not, suggesting that maternal stress exerted unique effects on child developmental outcomes in our study. It is unclear why antenatal depression was not associated with child outcomes in the current study, as there is some evidence that antenatal depression and stress exert independent effects on child outcomes (Madigan et al., 2018). However, other research has also similarly found that stress but not depression is predictive of developmental outcomes in children. For example, O’Connor et al. (2002) demonstrated links between antenatal stress (but not depression) and total difficulties in children at 4 years using the SDQ scales. We have similarly found a significant association between antenatal stress and child behavioural difficulties, but no significant effect of antenatal depression (D’Souza et al., 2019). It is noteworthy that, not only do our findings support the notion that antenatal stress is linked to disturbances in psychopathologies childhood, but that these concerns are evident as early as 2 years. Our results also provide novel evidence that antenatal stress is associated with co-existing developmental delays and behavioural concerns. 4.2. Maternal lifestyle factors Periconceptional folate intake was associated with delayed talking, with children of mothers who did not take folate both before pregnancy and in the first trimester being at increased odds of developmental language delay. Our findings support earlier research that stresses the importance of periconceptional folate intake for language development (Chatzi et al., 2012; Roth et al., 2011). Chatzi et al.’s findings indicated that children of mothers who took folic acid supplements in excess of the daily-recommended quantity showed improvements in both receptive and expressive communication skills at 18 months, indicating that high levels folic acid supplements during early gestation could promote the development of comprehension and communication skills. Furthermore, Roth et al. found that a lack of periconceptional folate use was associated with severe language delay in offspring at 3 years of age. Multivitamin intake during the pregnancy period was also associated with child outcomes at 2 years; specifically multivitamin intake during pregnancy was associated with reduced odds of comorbid difficulties. This is consistent with previous research that has demonstrated a positive association between pregnancy intake or serum concentrations for specific vitamins and subsequent language and behavioural outcomes in children (Chen et al., 2009; Villamor et al., 2012; Whitehouse et al., 2012). However, as we looked at overall multivitamin intake in pregnant mothers, we were unable to isolate the specific vitamins contributing to this association. Nevertheless, our results suggest that vitamin intake during pregnancy is associated with comorbid language and behavioural difficulties in offspring as early as 2 years. However, more research is needed into the long-term consequences of antenatal vitamin deficiencies on child outcomes, and the mechanisms by which this phenomenon occurs. Exposure to smoking during pregnancy was associated with abnormal levels of total difficulties, and these effects remained significant in the presence of the sociodemographic control variables. Several studies have observed an association between prenatal nicotine exposure and externalising problems in children (see Tiesler & Heinrich, 2014). Our results add further support for this association. Antenatal nicotine exposure is thought to have neuroteratogenic effects on the developing foetus, where such exposure may result in deficits in synaptic connections and subsequently alter foetal brain development (Ernst, Moolchan, & Robinson, 2001). Unexpectedly maternal alcohol consumption during the first trimester was associated with a reduced odds of language only difficulties at two years, with no significant association with behaviour or comorbid difficulties present. There are inconsistencies regarding alcohol consumption during gestation and its effects on child cognitive outcomes (Alati et al., 2008), which may be due to the categorisation of alcohol consumption in analyses. Meta-analyses of alcohol consumption during pregnancy have indicated that, although mild to moderate exposure to alcohol during gestation may not be associated with adverse outcomes in child cognition, binge prenatal alcohol exposure (defined as more than 4 drinks on a single occasion during gestation) may be (Flak et al., 2014). Due to the low number of individuals reporting alcohol use consistent with binge drinking during pregnancy in our cohort, our analysis looked at alcohol consumption during pregnancy as a binary variable: mothers were separated into those who reported abstaining from drinking during pregnancy and those who reported having one or more drinks a week on average. It is likely that results would be different if our sample of pregnant drinkers was larger and enabled us to split them into mild, moderate and severe drinking behaviours, and/or to measure alcohol consumption per episode. 4.3. The foetal programming hypothesis Our focus on antenatal factors and their association with child outcomes was due to our interest in testing the foetal programming hypothesis (Barker, 1998). Specifically, given that our antenatal predictors have been separately linked to children’s language and behavioural outcomes, and the foetal programming hypothesis was thought to underlie these associations, we were interested in evaluating whether these factors were also related to co-occurring language and behavioural difficulties. However, only maternal 9

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perceived stress and multivitamin intake during pregnancy were associated with comorbid difficulties, with other factors were associated with behavioural only and language only difficulties. It is unclear why this may be the case, though one possibility may be that neurodevelopment is differentially impacted by specific exposures during pregnancy. Further research would be needed to explore this possibility and the reasons underlying our findings 4.4. Child characteristics and sociodemographic factors We found that a number of child characteristics and sociodemographic factors were significantly associated with behavioural difficulties and/or developmental delays in our multivariable analyses. Maternal ethnicity was significantly associated with difficulties. Children of mothers who identified as NZ European were less likely to show all difficulties relative to the other ethnicities. Indices of deprivation were also shown to be significantly associated with delayed talking. Children of mothers with a Bachelor’s degree or higher were less likely to show difficulties than children of mothers with a lower education level. Compared to children born to teenage mothers at the time of childbirth, children born to mothers 30 years or older were less likely to show behavioural only difficulties. Boys were also more likely to show behavioural only, language only and comorbid difficulties than girls. Although our study provides us with valuable insight into early behavioural and language difficulties, it is not without limitations. A key limitation in our study design is the use of maternal self-report data. Specifically, self-report bias could be of concern in the case of measures of maternal lifestyle factors such as smoking behaviour and alcohol consumption. Exploration of such predictors using such measures will always be somewhat limited due to the social stigma that surrounds these behaviours during pregnancy, with the risk of participants under-reporting these behaviours being likely (Flak et al., 2014). Nevertheless, self-report is the most common and cost effective way of obtaining this information and was the general method used for obtaining information on smoking and alcohol intake in prior research (e.g., Brion et al., 2010; Eicher et al., 2013; Key et al., 2007; Sood et al., 2001; Stene-Larsen et al., 2009) It should also be noted that the current model does not specifically consider the postnatal home environment. It could be argued that maternal experience of postnatal depression negatively impacts child language and behavioural difficulties, and that the associations with maternal antenatal distress reflect this. However, we do not consider this likely, given it was maternal antenatal stress and not depressive symptoms that predicted child comorbid difficulties in the multivariable model. In addition, research with this cohort demonstrates considerable ‘churn’ between those mothers experiencing distress antenatally and postnatally (Underwood, Waldie, D’Souza, Peterson, & Morton, 2017). Further research with this cohort could examine whether there are moderating or additive effects of postnatal and prenatal maternal mental health in relation to child outcomes. Another limitation is that, though the cohort is large, the number of children who were included in the multinomial model was reduced. However, we mitigated some of this reduction by using multiple imputation to account for missing data. Moreover, because there was a small proportion of children who met the criteria for talking delays and/or behavioural difficulties at 2 years of age, there are concerns regarding statistical power; power analyses indicated that we may not be able to detect effect sizes (i.e. odds ratios) less than 1.60 for low base rate events (2008, Demidenko, 2007). However, this is a relatively small effect size (Chen et al., 2010) and therefore may not be as meaningful as larger, detectable effects. The reduction in sample representativeness as a result of attrition is also something that needs to be noted. Compared to children in our sample, children that were not included in the analyses (either due to being lost to follow up or not having outcome data) were more likely to have been exposed to adverse antenatal factors and experience negative birth outcomes (i.e. low birth weight and preterm birth). These children were also more likely to have mothers who were non-European, younger and less educated. As such, our results are reflective of our sample and not necessarily the broader NZ population. Nevertheless, it is worth noting that attrition is common with longitudinal studies such as GUiNZ and a strength of the study is its high retention rates relative to other birth cohorts (Teague et al., 2018). The sample also remains socioeconomically and ethnically diverse in spite of attrition. The prospective study design is another key strength, as it allowed us to gather data on antenatal factors without being subject to significant recall bias. Our research is among the first to explore the links between antenatal factors and associations with behavioural and language comorbidities in young children, using prospective cohort data. We found that maternal perceived stress and multivitamin intake in pregnancy were associated with comorbid behavioural and language difficulties in children, whereas periconceptual folate and antenatal alcohol intake were associated with language only difficulties. Antenatal smoking was linked to behavioural only difficulties. While we did not find that all antenatal factors were associated with comorbid language and behavioural difficulties, this does open up avenues for future research to investigate the underlying reasons for these findings (i.e. why are some antenatal factors associated with comorbid difficulties whereas others are not). Further, we demonstrated that antenatal factors are still associated with early childhood language and behavioural difficulties (though not necessarily comorbidity between the two) even in the presence of sociodemographic factors such as deprivation, ethnicity, maternal age and education, showing some support for the foetalprogramming hypothesis in a NZ context. Overall, our findings support previous research in showing that antenatal factors are likely to play a critical role in the early developmental trajectories of children, emphasising the importance of promoting antenatal health and wellbeing in expectant mothers. Declaration of Competing Interest All authors declare no conflict of interest.

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Acknowledgements Growing Up in New Zealand has been funded by the New Zealand Ministries of Social Development, Health, Education, Justice and Pacific Island Affairs; the former Ministry of Science Innovation and the former Department of Labour (now both part of the Ministry of Business, Innovation and Employment); the former Ministry of Women’s Affairs (now the Ministry for Women); the Department of Corrections; the Families Commission (now known as the Social Policy Evaluation and Research Unit); Te Puni Kokiri; New Zealand Police; Sport New Zealand; the Housing New Zealand Corporation; and the former Mental Health Commission, The University of Auckland and Auckland UniServices Limited. Other support for the study has been provided by the NZ Health Research Council, Statistics New Zealand, the Office of the Children’s Commissioner and the Office of Ethnic Affairs. The study has been designed and conducted by the Growing Up in New Zealand study team, led by the University of Auckland. The authors acknowledge the contributions of the original study investigators: Susan M.B. Morton, Polly E. Atatoa Carr, Cameron C. Grant, Arier C. Lee, Dinusha K. Bandara, Jatender Mohal, Jennifer M. Kinloch, Johanna M. Schmidt, Mary R. Hedges, Vivienne C. Ivory, Te Kani R. Kingi, Renee Liang, Lana M. Perese, Elizabeth Peterson, Jan E. Pryor, Elaine Reese, Elizabeth M. Robinson, Karen E. Waldie, Clare R. Wall. The views reported in this paper are those of the authors and do not necessarily represent the views of the Growing Up in New Zealand investigators. Appendix A. Supplementary data Supplementary material related to this article can be found, in the online version, at doi:https://doi.org/10.1016/j.infbeh.2019. 101388. References Alati, R., MacLeod, J., Hickman, M., Sayal, K., May, M., Smith, G. D., & Lawlor, D. A. (2008). Intrauterine exposure to alcohol and tobacco use and childhood IQ: Findings from a parental-offspring comparison within the avon longitudinal study of parents and children. Pediatric Research, 64(6), 659–666. https://doi.org/10. 1203/PDR.0b013e318187cc31. Alloway, T. P. (2010). Working memory and executive function profiles of individuals with borderline intellectual functioning. Journal of Intellectual Disability Research, 54(5), 448–456. https://doi.org/10.1111/j.1365-2788.2010.01281.x. Anda, R. F., Croft, J. B., Felitti, V. J., Nordenberg, D., Giles, W. H., Williamson, D. F., & Giovino, G. A. (1999). Adverse childhood experiences and smoking during adolescence and adulthood. JAMA, 282(17), 1652–1658. https://doi.org/10.1001/jama.282.17.1652. Andersen, S. L. (2003). Trajectories of brain development: Point of vulnerability or window of opportunity? Neuroscience and Biobehavioral Reviews, 27(1), 3–18. https://doi.org/10.1016/S0149-7634(03)00005-8. Arpi, E., & Ferrari, F. (2013). Preterm birth and behaviour problems in infants and preschool-age children: A review of the recent literature. Developmental Medicine and Child Neurology, 55(9), 788–796. https://doi.org/10.1111/dmcn.12142. Ashford, J., van Lier, P. A. C., Timmermans, M., Cuijpers, P., & Koot, H. M. (2008). Prenatal smoking and internalizing and externalizing problems in children studied from childhood to late adolescence. Journal of the American Academy of Child and Adolescent Psychiatry, 47(7), 779–787. https://doi.org/10.1097/CHI. 0b013e318172eefb. Barker, D. J. (1998). In utero programming of chronic disease. Clinical Science (London, England: 1979), 95(2), 115–128. Batenburg‐Eddes, T. V., Brion, M. J., Henrichs, J., Jaddoe, V. W. V., Hofman, A., Verhulst, F. C., ... Tiemeier, H. (2013). Parental depressive and anxiety symptoms during pregnancy and attention problems in children: A cross-cohort consistency study. Journal of Child Psychology and Psychiatry, 54(5), 591–600. https://doi. org/10.1111/jcpp.12023. Benner, G. J., Nelson, J. R., & Epstein, M. H. (2002). Language skills of children with EBD: A literature review. Journal of Emotional and Behavioral Disorders, 10(1), 43–56. https://doi.org/10.1177/106342660201000105. Benton, D. (2012). Vitamins and neural and cognitive developmental outcomes in children. The Proceedings of the Nutrition Society, 71(1), 14–26. https://doi.org/10. 1017/S0029665111003247. Bergman, K., Sarkar, P., O’Connor, T. G., Modi, N., & Glover, V. (2007). Maternal stress during pregnancy predicts cognitive ability and fearfulness in infancy. Journal of the American Academy of Child and Adolescent Psychiatry, 46(11), 1454–1463. https://doi.org/10.1097/chi.0b013e31814a62f6. Bernard-Bonnin, A.-C. (2004). Maternal depression and child development. Paediatrics & Child Health, 9(8), 575–583. https://doi.org/10.1093/pch/9.8.575. Beydoun, H., & Saftlas, A. F. (2008). Physical and mental health outcomes of prenatal maternal stress in human and animal studies: A review of recent evidence. Paediatric and Perinatal Epidemiology, 22(5), 438–466. Bird, A. L., Grant, C. C., Bandara, D. K., Mohal, J., Atatoa‐Carr, P. E., Wise, M. R., & Morton, S. M. B. (2017). Maternal health in pregnancy and associations with adverse birth outcomes: Evidence from growing up in New Zealand. The Australian & New Zealand Journal of Obstetrics & Gynaecology, 57(1), 16–24. https://doi. org/10.1111/ajo.12557. Botting, N., & Conti-Ramsden, G. (2000). Social and behavioural difficulties in children with language impairment. Child Language Teaching and Therapy, 16(2), 105–120. https://doi.org/10.1177/026565900001600201. Bradley, R. H., & Corwyn, R. F. (2002). Socioeconomic status and child development. Annual Review of Psychology, 53(1), 371–399. https://doi.org/10.1146/annurev. psych.53.100901.135233. Brion, M.-J., Victora, C., Matijasevich, A., Horta, B., Anselmi, L., Steer, C., ... Smith, G. D. (2010). Maternal smoking and child psychological problems: Disentangling causal and noncausal effects. Pediatrics, 126(1), e57–e65. https://doi.org/10.1542/peds.2009-2754. Brouwers, E. P., van Baar, A. L., & Pop, V. J. (2001). Maternal anxiety during pregnancy and subsequent infant development. Infant Behavior & Development, 24(1), 95–106. Burdge, G. C., & Lillycrop, K. A. (2010). Nutrition, epigenetics, and developmental plasticity: Implications for understanding human disease. Annual Review of Nutrition, 30, 315–339. Buss, C., Davis, E. P., Muftuler, L. T., Head, K., & Sandman, C. A. (2010). High pregnancy anxiety during mid-gestation is associated with decreased gray matter density in 6–9-year-old children. Psychoneuroendocrinology, 35(1), 141–153. https://doi.org/10.1016/j.psyneuen.2009.07.010. Caesar, R., Boyd, R. N., Colditz, P., Cioni, G., Ware, R. S., Salthouse, K., ... Baer, E. (2016). Early prediction of typical outcome and mild developmental delay for prioritisation of service delivery for very preterm and very low birthweight infants: A study protocol. BMJ Open, 6(7), e010726. https://doi.org/10.1136/ bmjopen-2015-010726. Carpenter, J. L., & Drabick, D. A. G. (2011). Co-occurrence of linguistic and behavioural difficulties in early childhood: A developmental psychopathology perspective. Early Child Development and Care, 181(8), 1021–1045. https://doi.org/10.1080/03004430.2010.509795. Chatzi, L., Papadopoulou, E., Koutra, K., Roumeliotaki, T., Georgiou, V., Stratakis, N., & Kogevinas, M. (2012). Effect of high doses of folic acid supplementation in early pregnancy on child neurodevelopment at 18 months of age: The mother–Child cohort “Rhea” study in Crete, Greece. Public Health Nutrition, 15(9),

11

Infant Behavior and Development 57 (2019) 101388

S. D’Souza, et al.

1728–1736. https://doi.org/10.1017/S1368980012000067. Chen, H., Cohen, P., & Chen, S. (2010). How big is a big odds ratio? Interpreting the magnitudes of odds ratios in epidemiological studies. Communications in Statistics Simulation and Computation, 39(4), 860–864. https://doi.org/10.1080/03610911003650383. Chen, K., Zhang, X., Wei, X., Qu, P., Liu, Y., & Li, T. (2009). Antioxidant vitamin status during pregnancy in relation to cognitive development in the first two years of life. Early Human Development, 85(7), 421–427. https://doi.org/10.1016/j.earlhumdev.2009.02.001. Clegg, J., Hollis, C., Mawhood, L., & Rutter, M. (2005). Developmental language disorders – A follow-up in later adult life. Cognitive, language and psychosocial outcomes. Journal of Child Psychology and Psychiatry, 46(2), 128–149. https://doi.org/10.1111/j.1469-7610.2004.00342.x. Cohen, S., Kamarck, T., & Mermelstein, R. (1983). A global measure of perceived stress. Journal of Health and Social Behavior, 24(4), 385–396. Cox, J. L., Holden, J. M., & Sagovsky, R. (1987). Detection of postnatal depression. Development of the 10-item edinburgh postnatal depression scale. The British Journal of Psychiatry, 150(6), 782–786. Davis, E. P., & Sandman, C. A. (2010). The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development. Child Development, 81(1), 131–148. https://doi.org/10.1111/j.1467-8624.2009.01385.x. Deater–Deckard, K., Dodge, K. A., Bates, J. E., & Pettit, G. S. (1998). Multiple risk factors in the development of externalizing behavior problems: Group and individual differences. Development and Psychopathology, 10(3), 469–493. https://doi.org/10.1017/S0954579498001709. Demidenko, E. (2007). Sample size determination for logistic regression revisited. Statistics in Medicine, 26(18), 3385–3397. https://doi.org/10.1002/sim.2771. Demidenko, E. (2008). Sample size and optimal design for logistic regression with binary interaction. Statistics in Medicine, 27(1), 36–46. https://doi.org/10.1002/sim. 2980. D’Souza, S., Backhouse-Smith, A., Thompson, J., Slykerman, R., Marlow, G., Wall, C., ... Waldie, K. E. (2016). Associations between the KIAA0319 dyslexia susceptibility gene variants, antenatal maternal stress, and reading ability in a longitudinal birth cohort. Dyslexia, 22(4), 379–393. D’Souza, S., Waldie, K. E., Peterson, E. R., Underwood, L., & Morton, S. M. (2017a). Psychometric properties and normative data for the preschool Strengths and Difficulties Questionnaire in two-year-old children. Journal of Abnormal Child Psychology, 45(2), 345–357. D’Souza, S., Waldie, K. E., Peterson, E. R., Underwood, L., & Morton, S. M. B. (2017b). The Strengths and Difficulties Questionnaire: Factor structure of the fatherreport and parent agreement in 2-year-old children. Assessment1073191117698757. https://doi.org/10.1177/1073191117698757. D’Souza, S., Waldie, K. E., Peterson, E. R., Underwood, L., & Morton, S. M. B. (2019). Antenatal and postnatal determinants of behavioural difficulties in early childhood: Evidence from growing up in New Zealand. Child Psychiatry and Human Development, 50(1), 45–60. https://doi.org/10.1007/s10578-018-0816-6. Duncan, G. J., Dowsett, C. J., Claessens, A., Magnuson, K., Huston, A. C., Klebanov, P., ... Japel, C. (2007). School readiness and later achievement. Developmental Psychology, 43(6), 1428–1446. https://doi.org/10.1037/0012-1649.43.6.1428. Eicher, J. D., Powers, N. R., Cho, K., Miller, L. L., Mueller, K. L., Ring, S. M., & Gruen, J. R. (2013). Associations of prenatal nicotine exposure and the dopamine related genes ANKK1 and DRD2 to verbal language. PloS One, 8(5), e63762. https://doi.org/10.1371/journal.pone.0063762. Ernst, M., Moolchan, E. T., & Robinson, M. L. (2001). Behavioral and neural consequences of prenatal exposure to nicotine. Journal of the American Academy of Child and Adolescent Psychiatry, 40(6), 630–641. https://doi.org/10.1097/00004583-200106000-00007. Eyles, D. W., Feron, F., Cui, X., Kesby, J. P., Harms, L. H., Ko, P., ... Burne, T. H. J. (2009). Developmental vitamin D deficiency causes abnormal brain development. Psychoneuroendocrinology, 34, S247–S257. https://doi.org/10.1016/j.psyneuen.2009.04.015. Fanti, K. A., & Henrich, C. C. (2010). Trajectories of pure and co-occurring internalizing and externalizing problems from age 2 to age 12: Findings from the National Institute of Child Health and Human Development Study of Early Child Care. Developmental Psychology, 46(5), 1159–1175. https://doi.org/10.1037/a0020659. Fenson, L., Marchman, V. A., Thal, D. J., Dale, P. S., & Reznick, J. S. (2007). MacArthur-Bates communicative development inventories: User’s guide and technical manual. Baltimore, MD: Brookes. Fergusson, D. M., Horwood, J. L., & Ridder, E. M. (2005). Show me the child at seven: The consequences of conduct problems in childhood for psychosocial functioning in adulthood. Journal of Child Psychology and Psychiatry, 46(8), 837–849. https://doi.org/10.1111/j.1469-7610.2004.00387.x. Fergusson, D. M., Horwood, L. J., & Ridder, E. M. (2007). Conduct and attentional problems in childhood and adolescence and later substance use, abuse and dependence: Results of a 25-year longitudinal study. Drug and Alcohol Dependence, 88, S14–S26. https://doi.org/10.1016/j.drugalcdep.2006.12.011. Field, T., Diego, M., Dieter, J., Hernandez-Reif, M., Schanberg, S., Kuhn, C., & Bendell, D. (2004). Prenatal depression effects on the fetus and the newborn. Infant Behavior & Development, 27(2), 216–229. https://doi.org/10.1016/j.infbeh.2003.09.010. Fitzsimons, E., Goodman, A., Kelly, E., & Smith, J. P. (2017). Poverty dynamics and parental mental health: Determinants of childhood mental health in the UK. Social Science & Medicine, 175, 43–51. https://doi.org/10.1016/j.socscimed.2016.12.040. Flak, A. L., Su, S., Bertrand, J., Denny, C. H., Kesmodel, U. S., & Cogswell, M. E. (2014). The association of mild, moderate, and binge prenatal alcohol exposure and child neuropsychological outcomes: A meta-analysis. Alcoholism, Clinical and Experimental Research, 38(1), 214–226. https://doi.org/10.1111/acer.12214. Gao, W., Paterson, J., Abbott, M., Carter, S., & Iusitini, L. (2007). Maternal mental health and child behaviour problems at 2 years: Findings from the Pacific Islands Families Study. The Australian and New Zealand Journal of Psychiatry, 41(11), 885–895. https://doi.org/10.1080/00048670701634929. Gatzke-Kopp, L. M., & Beauchaine, T. P. (2007). Direct and passive prenatal nicotine exposure and the development of externalizing psychopathology. Child Psychiatry and Human Development, 38(4), 255–269. https://doi.org/10.1007/s10578-007-0059-4. Goodman, R. (1997). The strengths and difficulties questionnaire: A research note. Journal of Child Psychology and Psychiatry, 38(5), 581–586. Gutteling, B. M., de Weerth, C., Willemsen-Swinkels, S. H. N., Huizink, A. C., Mulder, E. J. H., Visser, G. H. A., & Buitelaar, J. K. (2005). The effects of prenatal stress on temperament and problem behavior of 27-month-old toddlers. European Child & AdolescentPsychiatry, 14(1), 41–51. https://doi.org/10.1007/s00787-005-0435-1. Gutteling, B. M., de Weerth, C., Zandbelt, N., Mulder, E. J. H., Visser, G. H. A., & Buitelaar, J. K. (2006). Does maternal prenatal stress adversely affect the child’s learning and memory at age six? Journal of Abnormal Child Psychology, 34(6), 787–796. https://doi.org/10.1007/s10802-006-9054-7. Hartas, D. (2011). Children’s language and behavioural, social and emotional difficulties and prosocial behaviour during the toddler years and at school entry. British Journal of Special Education, 38(2), 83–91. https://doi.org/10.1111/j.1467-8578.2011.00507.x. Herrmann, M., King, K., & Weitzman, M. (2008). Prenatal tobacco smoke and postnatal secondhand smoke exposure and child neurodevelopment. Current Opinion in Pediatrics, 20(2), 184–190. Hughes, N., Sciberras, E., & Goldfeld, S. (2016). Family and community predictors of comorbid language, socioemotional and behavior problems at school entry. PloS One, 11(7), e0158802. https://doi.org/10.1371/journal.pone.0158802. Huizink, A. C., & Mulder, E. J. H. (2006). Maternal smoking, drinking or cannabis use during pregnancy and neurobehavioral and cognitive functioning in human offspring. Neuroscience and Biobehavioral Reviews, 30(1), 24–41. https://doi.org/10.1016/j.neubiorev.2005.04.005. Key, A. P. F., Ferguson, M., Molfese, D. L., Peach, K., Lehman, C., & Molfese, V. J. (2007). Smoking during pregnancy affects speech-processing ability in newborn infants. Environmental Health Perspectives, 115(4), 623–629. https://doi.org/10.1289/ehp.9521. Koutra, K., Roumeliotaki, T., Kyriklaki, A., Kampouri, M., Sarri, K., Vassilaki, M., ... Chatzi, L. (2017). Maternal depression and personality traits in association with child neuropsychological and behavioral development in preschool years: Mother-child cohort (Rhea Study) in Crete, Greece. Journal of Affective Disorders, 217, 89–98. https://doi.org/10.1016/j.jad.2017.04.002. Laplante, D. P., Barr, R. G., Brunet, A., Du Fort, G. G., Meaney, M. L., Saucier, J.-F., ... King, S. (2004). Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatric Research, 56(3), 400–410. https://doi.org/10.1203/01.PDR.0000136281.34035.44. Laplante, D. P., Brunet, A., Schmitz, N., Ciampi, A., & King, S. (2008). Project Ice Storm: Prenatal maternal stress affects cognitive and linguistic functioning in 5 1/2year-old children. Journal of the American Academy of Child and Adolescent Psychiatry, 47(9), 1063–1072. Law, J., Rush, R., Schoon, I., & Parsons, S. (2009). Modeling developmental language difficulties from school entry into adulthood: Literacy, mental health, and employment outcomes. Journal of Speech, Language, and Hearing Research: JSLHR, 52(6), 1401–1416. https://doi.org/10.1044/1092-4388(2009/08-0142). Madigan, S., Oatley, H., Racine, N., Fearon, R. M. P., Schumacher, L., Akbari, E., & Tarabulsy, G. M. (2018). A meta-analysis of maternal prenatal depression and anxiety on child socioemotional development. Journal of the American Academy of Child and Adolescent Psychiatry, 57(9), 645–657. https://doi.org/10.1016/j.jaac. 2018.06.012 e8. Molfese, D. L. (2000). Predicting dyslexia at 8 years of age using neonatal brain responses. Brain and Language, 72(3), 238–245. https://doi.org/10.1006/brln.2000.

12

Infant Behavior and Development 57 (2019) 101388

S. D’Souza, et al.

2287. Molloy, A. M., Kirke, P. N., Brody, L. C., Scott, J. M., & Mills, J. L. (2008). Effects of folate and vitamin B12 deficiencies during pregnancy on fetal, infant, and child development. Food and Nutrition Bulletin, 29(2_suppl1), S101–S111. https://doi.org/10.1177/15648265080292S114. Morton, S. M. B., Atatoa Carr, P. E., Bandara, D. K., Grant, C. C., Ivory, V. C., Kingi, T. R., et al. (2010). Growing up in New Zealand: A longitudinal study of new zealand children and their families. Report 1: Before we are born. Auckland: Growing up in New ZealandRetrieved fromhttps://researchspace.auckland.ac.nz/handle/2292/ 6120. Morton, S. M. B., Carr, P. E. A., Grant, C. C., Robinson, E. M., Bandara, D. K., Bird, A., & Wall, C. (2013). Cohort profile: Growing up in New Zealand. International Journal of Epidemiology, 42(1), 65–75. https://doi.org/10.1093/ije/dyr206. Morton, S. M. B., Grant, C. C., Carr, P. E. A., Robinson, E. M., Kinloch, J. M., Fleming, C. J., & Liang, R. (2014). How do you recruit and retain a prebirth cohort? Lessons learnt from growing up in New Zealand. Evaluation & the Health Professions, 37(4), 411–433. https://doi.org/10.1177/0163278712462717. Morton, S. M. B., Ramke, J., Kinloch, J., Grant, C. C., Carr, P. A., Leeson, H., & Robinson, E. (2015). Growing up in New Zealand cohort alignment with all New Zealand births. Australian and New Zealand Journal of Public Health, 39(1), 82–87. https://doi.org/10.1111/1753-6405.12220. Narusyte, J., Ropponen, A., Alexanderson, K., & Svedberg, P. (2017). Internalizing and externalizing problems in childhood and adolescence as predictors of work incapacity in young adulthood. Social Psychiatry and Psychiatric Epidemiology, 52(9), 1159–1168. https://doi.org/10.1007/s00127-017-1409-6. Neisser, U., Boodoo, G., Bouchard, T. J., Jr., Boykin, A. W., Brody, N., Ceci, S. J., & Urbina, S. (1996). Intelligence: Knowns and unknowns. The American Psychologist, 51(2), 77–101. https://doi.org/10.1037/0003-066X.51.2.77. O’Connor, T. G., Ben-Shlomo, Y., Heron, J., Golding, J., Adams, D., & Glover, V. (2005). Prenatal anxiety predicts individual differences in cortisol in pre-adolescent children. Biological Psychiatry, 58(3), 211–217. https://doi.org/10.1016/j.biopsych.2005.03.032. O’Connor, T. G., Heron, J., Golding, J., Beveridge, M., & Glover, V. (2002). Maternal antenatal anxiety and children’s behavioural/emotional problems at 4 years. The British Journal of Psychiatry, 180(6), 502–508. https://doi.org/10.1192/bjp.180.6.502. O’Connor, T. G., Heron, J., Golding, J., Glover, V., & the AL SPAC Study Team (2003). Maternal antenatal anxiety and behavioural/emotional problems in children: A test of a programming hypothesis. Journal of Child Psychology and Psychiatry, 44(7), 1025–1036. https://doi.org/10.1111/1469-7610.00187. O’Connor, T. G., Monk, C., & Fitelson, E. M. (2014). Practitioner Review: Maternal mood in pregnancy and child development – Implications for child psychology and psychiatry. Journal of Child Psychology and Psychiatry, 55(2), 99–111. https://doi.org/10.1111/jcpp.12153. Odgers, C. L., Caspi, A., Broadbent, J. M., Dickson, N., Hancox, R. J., Harrington, H., ... Moffitt, T. E. (2007). Prediction of differential adult health burden by conduct problem subtypes in males. Archives of General Psychiatry, 64(4), 476–484. https://doi.org/10.1001/archpsyc.64.4.476. O’Keeffe, L. M., Greene, R. A., & Kearney, P. M. (2014). The effect of moderate gestational alcohol consumption during pregnancy on speech and language outcomes in children: A systematic review. Systematic Reviews, 3(1), 1. https://doi.org/10.1186/2046-4053-3-1. O’Leary, C. M. (2004). Fetal alcohol syndrome: Diagnosis, epidemiology, and developmental outcomes. Journal of Paediatrics and Child Health, 40(1–2), 2–7. https:// doi.org/10.1111/j.1440-1754.2004.00280.x. Oshima‐Takane, Y., Goodz, E., & Derevensky, J. L. (1996). Birth order effects on early language development: Do secondborn children learn from overheard speech? Child Development, 67(2), 621–634. https://doi.org/10.1111/j.1467-8624.1996.tb01755.x. Plomin, R., Price, T. S., Eley, T. C., Dale, P. S., & Stevenson, J. (2002). Associations between behaviour problems and verbal and nonverbal cognitive abilities and disabilities in early childhood. Journal of Child Psychology and Psychiatry, 43(5), 619–633. Reilly, S., Wake, M., Ukoumunne, O. C., Bavin, E., Prior, M., Cini, E., & Bretherton, L. (2010). Predicting language outcomes at 4 years of age: Findings from early language in Victoria study. Pediatrics, 126(6), e1530–e1537. https://doi.org/10.1542/peds.2010-0254. Roebuck, T. M., Mattson, S. N., & Riley, E. P. (1998). A review of the neuroanatomical findings in children with fetal alcohol syndrome or prenatal exposure to alcohol. Alcoholism, Clinical and Experimental Research, 22(2), 339–344. https://doi.org/10.1111/j.1530-0277.1998.tb03658.x. Rosenthal, D. G., & Weitzman, M. (2011). Examining the effects of intrauterine and postnatal exposure to tobacco smoke on childhood cognitive and behavioral development. International Journal of Mental Health, 40(1), 39–64. Roth, C., Magnus, P., Schjølberg, S., Stoltenberg, C., Surén, P., McKeague, I. W., ... Susser, E. (2011). Folic acid supplements in pregnancy and severe language delay in children. JAMA, 306(14), 1566–1573. https://doi.org/10.1001/jama.2011.1433. Roza, S. J., van Batenburg-Eddes, T., Steegers, E. A. P., Jaddoe, V. W. V., Mackenbach, J. P., Hofman, A., & Tiemeier, H. (2010). Maternal folic acid supplement use in early pregnancy and child behavioural problems: The generation R study. The British Journal of Nutrition, 103(3), 445. https://doi.org/10.1017/ S0007114509991954. Salmond, C., Crampton, P., & Atkinson, J. (2007). NZDep2006 index of deprivation. Wellington: University of Otago (Department of Public Health). Schmidt, R. J., Tancredi, D. J., Ozonoff, S., Hansen, R. L., Hartiala, J., Allayee, H., ... Hertz-Picciotto, I. (2012). Maternal periconceptional folic acid intake and risk of autism spectrum disorders and developmental delay in the CHARGE (CHildhood Autism Risks from Genetics and Environment) case-control study. The American Journal of Clinical Nutrition, 96(1), 80–89. https://doi.org/10.3945/ajcn.110.004416. Schoeps, A., Peterson, E. R., Mia, Y., Waldie, K. E., Underwood, L., D’Souza, S., & Morton, S. M. B. (2018). Prenatal alcohol consumption and infant and child behavior: Evidence from the growing up in New Zealand Cohort. Early Human Development, 123, 22–29. https://doi.org/10.1016/j.earlhumdev.2018.06.011. Schoon, I., Parsons, S., Rush, R., & Law, J. (2010). Children’s language ability and psychosocial development: A 29-year follow-up study. Pediatrics, 126(1), e73–e80. https://doi.org/10.1542/peds.2009-3282. Slykerman, R. F., Thompson, J., Waldie, K., Murphy, R., Wall, C., & Mitchell, E. A. (2015). Maternal stress during pregnancy is associated with moderate to severe depression in 11-year-old children. Acta Paediatrica, 104(1), 68–74. Sohr-Preston, S. L., & Scaramella, L. V. (2006). Implications of timing of maternal depressive symptoms for early cognitive and language development. Clinical Child and Family Psychology Review, 9(1), 65–83. https://doi.org/10.1007/s10567-006-0004-2. Sommerfelt, K., Ellertsen, B., & Markestad, T. (1993). Personality and behaviour in eight-year-old, non-handicapped children with birth weight under 1500 g. Acta Paediatrica, 82(9), 723–728. https://doi.org/10.1111/j.1651-2227.1993.tb12546.x. Sood, B., Delaney-Black, V., Covington, C., Nordstrom-Klee, B., Ager, J., Templin, T., & Sokol, R. J. (2001). Prenatal alcohol exposure and childhood behavior at age 6 to 7 years: I. Dose-response effect. Pediatrics, 108(2), e34–e34. Stanton-Chapman, T. L., Chapman, D. A., Bainbridge, N. L., & Scott, K. G. (2002). Identification of early risk factors for language impairment. Research in Developmental Disabilities, 23(6), 390–405. https://doi.org/10.1016/S0891-4222(02)00141-5. Steenweg–de Graaff, J., Roza, S. J., Steegers, E. A., Hofman, A., Verhulst, F. C., Jaddoe, V. W., & Tiemeier, H. (2012). Maternal folate status in early pregnancy and child emotional and behavioral problems: The Generation R Study. The American Journal of Clinical Nutrition, 95(6), 1413–1421. Stene-Larsen, K., Borge, A. I. H., & Vollrath, M. E. (2009). Maternal smoking in pregnancy and externalizing behavior in 18-month-old children: Results from a population-based prospective study. Journal of the American Academy of Child and Adolescent Psychiatry, 48(3), 283–289. https://doi.org/10.1097/CHI. 0b013e318195bcfb. Stewart, C. (2006). Food and nutrition guidelines for healthy pregnant and breastfeeding women: A background paper. Ministry of Health.. Sutcliffe, A. G., Barnes, J., Belsky, J., Gardiner, J., & Melhuish, E. (2012). The health and development of children born to older mothers in the United Kingdom: Observational study using longitudinal cohort data. BMJ, 345, e5116. Teague, S., Youssef, G. J., Macdonald, J. A., Sciberras, E., Shatte, A., Fuller-Tyszkiewicz, M., ... Hutchinson, D. (2018). Retention strategies in longitudinal cohort studies: A systematic review and meta-analysis. BMC Medical Research Methodology, 18. https://doi.org/10.1186/s12874-018-0586-7. Tervo, R. C. (2007). Language proficiency, development, and behavioral difficulties in toddlers. Clinical Pediatrics, 46(6), 530–539. https://doi.org/10.1177/ 0009922806299154. Tiesler, C. M. T., & Heinrich, J. (2014). Prenatal nicotine exposure and child behavioural problems. European Child & Adolescent Psychiatry, 23(10), 913–929. https:// doi.org/10.1007/s00787-014-0615-y. Tomblin, J. B., & Mueller, K. L. (2012). How can the comorbidity with ADHD aid understanding of language and speech disorders? Topics in Language Disorders, 32(3), 198–206. https://doi.org/10.1097/TLD.0b013e318261c264.

13

Infant Behavior and Development 57 (2019) 101388

S. D’Souza, et al.

Underwood, L., Waldie, K. E., D’Souza, S., Peterson, E. R., & Morton, S. M. (2017). A longitudinal study of pre-pregnancy and pregnancy risk factors associated with antenatal and postnatal symptoms of depression: Evidence from growing up in New Zealand. Maternal and Child Health Journal, 21(4), 915–931. Van den Bergh, B. R. H., & Marcoen, A. (2004). High antenatal maternal anxiety is related to ADHD symptoms, externalizing problems, and anxiety in 8‐and 9‐year‐olds. Child Development, 75(4), 1085–1097. https://doi.org/10.1111/j.1467-8624.2004.00727.x. Veena, S. R., Gale, C. R., Krishnaveni, G. V., Kehoe, S. H., Srinivasan, K., & Fall, C. H. (2016). Association between maternal nutritional status in pregnancy and offspring cognitive function during childhood and adolescence; a systematic review. BMC Pregnancy and Childbirth, 16(1), 220. https://doi.org/10.1186/s12884016-1011-z. Velders, F. P., Dieleman, G., Henrichs, J., Jaddoe, V. W. V., Hofman, A., Verhulst, F. C., ... Tiemeier, H. (2011). Prenatal and postnatal psychological symptoms of parents and family functioning: The impact on child emotional and behavioural problems. European Child & Adolescent Psychiatry, 20(7), 341–350. https://doi.org/ 10.1007/s00787-011-0178-0. Villamor, E., Rifas‐Shiman, S. L., Gillman, M. W., & Oken, E. (2012). Maternal intake of methyl‐donor nutrients and child cognition at 3 years of age. Paediatric and Perinatal Epidemiology, 26(4), 328–335. https://doi.org/10.1111/j.1365-3016.2012.01264.x. Wakschlag, L. S., Pickett, K. E., Cook, E., Benowitz, N. L., & Leventhal, B. L. (2002). Maternal smoking during pregnancy and severe antisocial behavior in offspring: A review. American Journal of Public Health, 92(6), 966–974. https://doi.org/10.2105/AJPH.92.6.966. Waldie, K. E., Peterson, E. R., D’Souza, S., Underwood, L., Pryor, J. E., Carr, P. A., ... Morton, S. M. (2015). Depression symptoms during pregnancy: Evidence from growing up in New Zealand. Journal of Affective Disorders, 186, 66–73. Waldie, K. E., Thompson, J. M., Mia, Y., Murphy, R., Wall, C., & Mitchell, E. A. (2014). Risk factors for migraine and tension-type headache in 11 year old children. The Journal of Headache and Pain, 15(1), 60. https://doi.org/10.1186/1129-2377-15-60. Waters, C. S., Hay, D. F., Simmonds, J. R., & van Goozen, S. H. M. (2014). Antenatal depression and children’s developmental outcomes: Potential mechanisms and treatment options. European Child & Adolescent Psychiatry, 23(10), 957–971. https://doi.org/10.1007/s00787-014-0582-3. Wehby, G. L., Prater, K., McCarthy, A. M., Castilla, E. E., & Murray, J. C. (2011). The impact of maternal smoking during pregnancy on early child neurodevelopment. Journal of Human Capital, 5(2), 207–254. https://doi.org/10.1086/660885. Whitehouse, A. J. O., Holt, B. J., Serralha, M., Holt, P. G., Kusel, M. M. H., & Hart, P. H. (2012). Maternal serum vitamin D levels during pregnancy and offspring neurocognitive development. Pediatrics, 129(3), 485–493. https://doi.org/10.1542/peds.2011-2644. Williams, J. H. G., & Ross, L. (2007). Consequences of prenatal toxin exposure for mental health in children and adolescents: A systematic review. European Child & Adolescent Psychiatry, 16(4), 243–253. https://doi.org/10.1007/s00787-006-0596-6. Yew, S. G. K., & O’Kearney, R. (2013). Emotional and behavioural outcomes later in childhood and adolescence for children with specific language impairments: Metaanalyses of controlled prospective studies: SLI and emotional and behavioural disorders. Journal of Child Psychology and Psychiatry, 54(5), 516–524. https://doi. org/10.1111/jcpp.12009.

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