Development and Psychopathology (2021), 33, 1566–1583
doi:10.1017/S0954579421001000
Special Issue Article
Prenatal substance exposure and maternal hostility from
pregnancy to toddlerhood: Associations with temperament profiles
at 16 months of age
Brendan D. Ostlund1
, Koraly E. Pérez-Edgar1, Shannon Shisler2, Sarah Terrell3, Stephanie Godleski4,
Pamela Schuetze5 and Rina D. Eiden1
1
Department of Psychology, The Pennsylvania State University, University Park, USA; 2Research Institute on Addictions, University at Buffalo, State University of
New York, Buffalo, USA; 3Department of Human Development and Family Studies, The Pennsylvania State University, University Park, USA; 4Department of
Psychology, Rochester Institute of Technology, Rochester, USA and 5Department of Psychology, State University of New York, Buffalo, USA
Abstract
We investigated whether infant temperament was predicted by level of and change in maternal hostility, a putative transdiagnostic vulnerability for psychopathology, substance use, and insensitive parenting. A sample of women (N = 247) who were primarily young, low-income,
and had varying levels of substance use prenatally (69 nonsmokers, 81 tobacco-only smokers, and 97 tobacco and marijuana smokers)
reported their hostility in the third trimester of pregnancy and at 2, 9, and 16 months postpartum, and their toddler’s temperament
and behavior problems at 16 months. Maternal hostility decreased from late pregnancy to 16 months postpartum. Relative to pregnant
women who did not use substances, women who used both marijuana and tobacco prenatally reported higher levels of hostility while pregnant and exhibited less change in hostility over time. Toddlers who were exposed to higher levels of prenatal maternal hostility were more
likely to be classified in temperament profiles that resemble either irritability or inhibition, identified via latent profile analysis. These two
profiles were each associated with more behavior problems concurrently, though differed in their association with competence. Our results
underscore the utility of transdiagnostic vulnerabilities in understanding the intergenerational transmission of psychopathology risk and are
discussed in regards to the Research Domain Criteria (RDoC) framework.
Keywords: hostility, maternal smoking in pregnancy, prenatal marijuana exposure, Research Domain Criteria (RDoC), temperament
(Received 28 January 2021; revised 12 July 2021; accepted 15 July 2021)
A mother’s mood during the transition from pregnancy to parenthood may be characterized by periods of both stability and change.
Recent work in perinatology and developmental psychopathology
converge on the suggestion that a mother’s emotional experience
while pregnant and in the first years of life influences her child’s
long-term development, including elevated risk for neurodevelopmental and behavioral problems from infancy to adolescence (see
Van den Bergh et al., 2017 for review). For example, pre- and
early postnatal maternal emotion marked by anxiety has been
linked to infant negative affect and childhood internalizing symptoms (e.g., Lawrence, Creswell, Cooper, & Murray, 2020; Spry
et al., 2020). These effects likely vary by the type, timing, and intensity of a pregnant woman’s pre- or postnatal emotional experience,
which itself may be exacerbated by other stressors, such as substance use and poverty (e.g., Eiden et al., 2011). Building on
Author for Correspondence: Rina D. Eiden, The Pennsylvania State University, 256
Moore Building, University Park, PA 16802; E-mail: rde5106@psu.edu
Cite this article: Ostlund BD, Pérez-Edgar KE, Shisler S, Terrell S, Godleski S,
Schuetze P, Eiden RD (2021). Prenatal substance exposure and maternal hostility from
pregnancy to toddlerhood: Associations with temperament profiles at 16 months of
age. Development and Psychopathology 33, 1566–1583. https://doi.org/10.1017/
S0954579421001000
these findings, we argue three significant gaps in our literature
must be addressed to aid parents, practitioners, and policymakers
in determining how best to support pregnant women and their
infants. Specifically, studies to date have often limited the assessment of a mother’s emotional experience to monolithic clinical
diagnoses, relied on static measures of maternal mental health,
and have largely failed to disentangle the influence of pre- and
postnatal maternal mood on infant neurobehavior.
The purpose of this study was to examine whether individual
differences in infant temperament could be predicted by a mother’s
level of hostility, a putative transdiagnostic vulnerability for psychopathology, substance use, and insensitive parenting (Eiden et al.,
2011; Schuetze, Eiden, & Dombkowski, 2006). We assessed hostility
during pregnancy and across the first 16 postnatal months in a
sample of women who were primarily young, low-income, and
had varying levels of substance use prenatally. Using a prospective
longitudinal design, we sought to address some of the methodological limitations in the extant literature. Namely, we examined both
level and change in hostility to characterize the role of pre- and
postnatal maternal emotion on infant dysregulation within the context of high sociodemographic risk. In order to further knowledge
on the intergenerational transmission of psychopathology risk, we
© The Author(s), 2021. Published by Cambridge University Press. This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence
(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution, and reproduction in any medium, provided the original work is properly cited.
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integrated this approach into the National Institute of Mental
Health (NIMH)’s Research Domain Criteria (RDoC) – an initiative
aimed at describing patterns of both dysfunction and adaptive
functioning across levels of analysis to clarify how psychopathologies manifest across development (Franklin, Jamieson, Glenn, &
Nock, 2015; Insel et al., 2010; Kozak & Cuthbert, 2016).
Hostility: a transdiagnostic vulnerability evident in the
perinatal period
Perinatal psychiatric disorders are common obstetric complications linked to adverse child outcomes from birth onward
(Gluckman, Hanson, Cooper, & Thornburg, 2008; Howard &
Khalifeh, 2020; Van den Bergh et al., 2017). Included in these
diagnostic categories, however, are heterogeneous subgroups of
individuals with symptom clusters that often do not fit neatly
into traditional psychiatric taxonomy (e.g., Putnam et al., 2017;
Walsh et al., 2019), a common problem in clinical research.
Consequently, the NIMH introduced RDoC to aid researchers
in identifying intermediate phenotypes – defined by functioning
along a continuum of neural, cognitive, emotional, and behavioral
activity – that may explain heterogeneity within, as well as comorbidities between, psychiatric disorders (Casey, Oliveri, & Insel,
2014; Cuthbert & Insel, 2010; Insel et al., 2010). Burgeoning evidence suggests that this approach may be particularly useful when
considering risk subgroups identified based on vulnerabilities that
cut across diagnostic categories (Blau, Orloff, & Hormes, 2020;
Lin et al., 2019; Obeysekare et al., 2020; Ostlund et al., 2019). A
focus on symptoms manifested in the pre- and early postpartum
period may also help identify patterns of functioning and mental
health outcomes across two generations.
Transdiagnostic vulnerabilities are relatively stable, trait-like
patterns of behavior that range from normal to abnormal.
Exceptionally high (or low) levels of these vulnerabilities contribute to a range of psychiatric disorders, demonstrating their clinical
utility (Beauchaine, Zisner, & Sauder, 2017; Dalgleish, Black,
Johnston, & Bevan, 2020; Harvey, Watkins, Mansell, & Shafran,
2004; Krueger & Eaton, 2015; Nolan-Hoeksema & Watkins,
2011). However, there is a dearth of evidence describing transdiagnostic vulnerabilities among pregnant women. To address
this shortcoming, Lin et al. (2019) examined whether a pregnant
woman’s level of emotion dysregulation, a known contributor to
psychopathology risk across the lifespan (Beauchaine, 2015;
Cole, Hall, & Hajal, 2013), was associated with measures of mental health and physiological responding to stress. The authors
found that a mother’s level of emotion dysregulation while pregnant was related to more chronic and episodic stress, higher trait
and pregnancy-specific anxiety, more self-injurious thoughts and
behaviors, and more self- and interviewer-reported depressive and
borderline symptoms. They also found that pregnant women with
higher levels of emotion dysregulation exhibited a blunted parasympathetic response to an ecologically valid infant cry stressor,
reflecting a diminished physiological reactivity to infant cues
that may thwart responsive caregiving efforts (Ablow, Marks,
Feldman, & Huffman, 2013; Del Vecchio, Walter, & O’Leary,
2009; Schuetze & Zeskind, 2001). Utilizing the same sample,
Ostlund et al. (2019) found that newborns whose mother reported
higher levels of emotion dysregulation while pregnant exhibited
blunted arousal and attention soon after birth.
Despite elevated psychopathology risk, few studies that have
examined prenatal transdiagnostic vulnerabilities investigate
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these risk processes among pregnant women who are high risk
by virtue of sociodemographic factors such as age, race/ethnicity,
or socioeconomic status (e.g., Ostlund et al., 2019; see Walsh
et al., 2019 for exception). Whether these transdiagnostic vulnerabilities adequately capture psychopathology risk among women
who are predominately young, low-income, and used illicit substances while pregnant remains to be seen. This clustering of
demographic, economic, and structural stressors increases risk
for maladaptive outcomes for both a mother and her developing
child, making this a particularly vulnerable population.
Here, the focus is on maternal hostility while pregnant and in
the first two years postpartum, a putative transdiagnostic vulnerability related to substance use, interpersonal discord, and psychopathology. Hostility is defined by a dysfunctional pattern of
cognition – one that is prone to negative, cynical, and denigrating
thoughts and feelings, along with antagonistic attitudes toward
and in evaluation of others (e.g., viewing others as distrustful
and purposefully hurtful; Berkowitz, 1993; Buss, 1961; Miller,
Smith, Turner, Guijarro, & Hallet, 1996). This oppositional cognitive bias abets intense and persistent anger and resentment,
and may incite aggressive behavior (e.g., Eckhardt, Norlander, &
Deffenbacher, 2004; Houston & Vavak, 1991; Ramirez & Andreu,
2006). Among women, high levels of hostility have been linked
to increased rates of depression, stress, and antisocial behavior
(Eiden et al., 2011; Sellers et al., 2014), as well as substance use disorders (Robinson, Brower, & Gomberg, 2001). Further, mothers
who use illicit substances and are high in hostility are more likely
to engage in harsh and insensitive parenting practices compared
to their peers (Eiden, Peterson, & Coleman, 1999; Schuetze et al.,
2006). This pattern of parenting among mothers prone to hostility
has, in turn, been linked to more behavior problems in their children (Rubin, Burgess, Dwyer, & Hastings, 2003; Schuetze, Lopez,
Granger, & Eiden, 2008).
Maternal use of marijuana and tobacco while pregnant
Smokers are more likely to report negative attitudes toward other
people and frequent, intense bouts of anger and aggression compared to nonsmokers (Miller et al., 1996). Trait hostility is also a
consistent predictor of smoking among both men and women
(e.g., Whiteman, Fowkes, Deary, & Lee, 1997) and associated
with lower rates of abstinence after treatment for smoking cessation (Kahler, Strong, Niaura, & Brown, 2004). In contrast to the
consistent associations between hostility and smoking, the literature on the association between hostility and marijuana use is
more mixed. Studies collecting daily data on marijuana use and
mood symptoms report that marijuana use is often preceded by
increases in negative affect (see Wycoff, Metrik, & Trull, 2018
for review). There are also reports of acute effects of marijuana
use on hostility, with some studies reporting increases in hostility
following marijuana use while others have reported general
decreases in negative affect, including hostility (Wycoff et al.,
2018). Little is known about the associations between co-use of
tobacco and marijuana and changes in hostility over time.
In one of the few studies examining hostility among pregnant
smokers, authors reported that maternal hostility prospectively
predicted persistent smoking during pregnancy, even in the context of other mood disorder symptoms, such as depression (Eiden
et al., 2011). This is particularly important since tobacco is one of
the most commonly used substances in pregnancy, with rates as
high as 23%, especially among young, low-income women, as
noted in the Surgeon General’s Report (U.S. Department of
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Health and Human Services (USDHHS), 2014). Tobacco in the
form of cigarettes delivers significant amounts of chemical toxins
to the fetus via the maternal bloodstream (USDHHS, 2014) and
increases norepinephrine, dopamine, acetylcholine, and serotonin
concentrations in the developing brain (Lichtensteiger, Ribary,
Schlumpf, Odermatt, & Widmer, 1988; Slotkin et al., 2015).
There are robust causal linkages between prenatal tobacco exposure and infant morbidity and mortality, including risk for prematurity, low birthweight, and sudden infant death syndrome
(USDHHS, 2014). Behaviorally, prenatal cigarette exposure
increases risk for irritability and higher arousal in the early neonatal period (Stroud et al., 2009), problems with self-soothing
and attention/orienting in the later neonatal period (Espy et al.,
2011; Stroud et al., 2016), disruptive behavior, including aggression, conduct disorder, and attention-deficit/hyperactivity disorder (ADHD) diagnosis in later childhood (Clark, Espy, &
Wakschlag, 2016; Estabrook et al., 2016; USDHHS, 2014), and
substance use in adolescence (Scott-Goodwin, Puerto, &
Moreno, 2016; Slotkin, 2008).
Although the literature on prenatal cigarette exposure is large,
there are two major open issues worth noting. First, many studies
have clear methodological shortcomings that limit interpretation.
These include a large number of retrospective studies that have
operationalized maternal smoking in pregnancy via single item
and/or self-report measures, as well as studies that lack a chemically verified, demographically similar comparison group that has
abstained from smoking (Molnar et al., 2017). Perceived social
stigma as well as possible legal ramifications may prevent a
woman from disclosing her substance use while pregnant, making
it difficult to obtain accurate information. While no approach is
perfect, measuring a woman’s substance use during pregnancy
via multiple methods (e.g., self-report, saliva sampling) may
increase the likelihood that we are characterizing her behavior
accurately and reliably. Accurately characterizing prenatal substance use is particularly important when working with a highrisk sample of pregnant women (i.e., young, single, low-income)
since the prevalence of smoking in pregnancy, as well as the developmental salience of these sociodemographic risks for child outcomes, tend to be higher.
Second, many studies to date have not considered prenatal use
of other substances that may have additive or synergistic effects,
such as cannabis. In a special issue devoted to co-use of tobacco
and cannabis in pregnancy, De Genna, Stroud, and Eiden (2019)
noted that the literature on developmental outcomes is quite small
despite rates of co-use ranging from 45% to approximately 85%
among substance users, which are higher than the use of
marijuana or tobacco alone (Chabarria et al., 2016; ColemanCowger, Schauer, & Peters, 2017; El Marroun et al., 2011; Ko,
Farr, Tong, Creanga, & Callaghan, 2015). Marijuana use during
pregnancy is concerning given significant increases in the potency
of the main psychoactive component of marijuana (i.e., delta-9tetrahydrocannabinol or THC) since the 1990s (Mehmedic
et al., 2010) and the increasing perception among pregnant
women that marijuana use in pregnancy is safe (Bayrampour,
Zahradnik, Lisonkova, & Janssen, 2019). Both tobacco and cannabis interfere with neurotransmitter levels, brain biochemistry, and
brain morphology for a developing child (Downer, Gowran, &
Campbell, 2007; El Marroun et al., 2016; Scott-Goodwin et al.,
2016). Results from both preclinical and human studies indicate
that nicotine and tetrahydrocannabinol – the psychoactive compounds in tobacco and cannabis – interfere with dopaminergic,
serotonergic, and GABAergic systems (DiNieri et al., 2011;
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B.D. Ostlund et al.
England et al., 2017; Morena, Patel, Bains, & Hill, 2016), and
alter neuronal development through their impact on nicotinic
and cannabinoid receptors (see Bara, Ferland, Rompala,
Szutorisz, & Hurd, 2021 and England et al., 2017; for detailed
reviews). Both substances cross the placenta and enter the fetal
bloodstream (Little & VanBeveren, 1996) and may have stronger
additive or synergistic effects than either substance alone.
In a recent study of neonatal neurobehavior with repeated
assessments across the first month of life, co-use was associated
with nearly double the need for external soothing (as opposed
to self-soothing) of newborns. Co-use also demonstrated 42%–
75% stronger associations with lower neonatal attention and lethargy compared to tobacco exposure alone (Stroud et al., 2018).
Using data from the present sample, Eiden, Schuetze, Shisler,
and Huestis (2018a) found that co-use of tobacco and cannabis
was also associated with higher infant autonomic dysregulation
compared to tobacco alone. Finally, using data from the present
sample, co-use has been associated with higher internalizing
behaviors and more sleep problems among girls at preschool
age (Eiden et al., 2018b) and blunted stress-reactivity patterns at
school age (Eiden et al., 2020) compared to tobacco alone or nonexposed children. No studies, to our knowledge, have examined
whether co-use of tobacco and marijuana impacts individual differences in temperamental reactivity, despite the fact that temperament is an early indicator of childhood psychopathology risk.
Temperament and RDoC
Among studies that have examined pre- and early postnatal predictors of temperament, a vast majority have focused on a single
dimension of infant behavior, chiefly domains of negative affect
(Van den Bergh et al., 2017). Although examination of individual
traits has its relative merits, this approach tends to undervalue the
phenotypic heterogeneity inherent to aberrant and normative
behavior that may be better captured by a constellation of traits.
To this end, RDoC promotes the use of quantitative approaches
that reduce complex data from multiple dimensions into homogenous phenotypes, which reflect a profile of traits related to psychological health and dysfunction (Cuthbert, 2014). This
approach has rarely been applied to pediatric samples (see
Karalunas et al., 2014 for an exception), limiting our understanding of the developmental trajectories of RDoC constructs and, by
extension, the etiology of early childhood psychopathology.
In outlining the developmental aspect of RDoC, the NIMH
recognizes that, “many areas of the child psychopathology literature (e.g., reward sensitivity, cognitive and emotional dysregulation, behavioral inhibition) serve as a more compatible model
for a dimensionally based approach compared to the highly specified categories of adult psychopathology” (NIMH, 2018).
Building on this definition, a young child’s behavior may be characterized as an emergent property of multiple RDoC constructs,
including, but not limited to, social communication (social processes system), acute threat and frustrative nonreward (negative
valence systems), attention and cognitive control (cognitive system), and motor action (sensorimotor system). These RDoC constructs map onto core dimensions of temperament that together
comprise a unique constellation of proclivities that define a
young child’s behavior – affect, regulation, attention, activity,
and arousal (Shiner et al., 2012). We argue that temperament is
well suited to serve as a link between extant developmental evidence and the RDoC framework, as temperament is a dimensionally based approach focused on the mechanisms that underlie the
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manifestation and change of numerous traits over time (see
Ostlund, Myruski, Buss, & Pérez-Edgar, 2021 for further
discussion).
While the constituent dimensions of temperament are largely
agreed upon (Shiner et al., 2012), researchers still disagree on how
individual differences in the constellation of a young child’s traits
ought to be characterized. Recent findings point to personcentered approaches, using analytical methods such as latent profile analysis (LPA), as one promising data-driven method for
identify subgroups of infants who are phenotypically similar.
Underlying this approach is the assumption that the complex
interplay among multiple dimensionally based temperamentrelevant behaviors gives rise to finite patterns of trait expression
that are shared among subgroups of children. Classifying distinct,
homogeneous groups of young children provides researchers (as
well as parents) with a readily interpretable, holistic representation of multiple traits to better understand a specific child and
their potential trajectory (e.g., Clauss, Avery, & Blackford, 2015;
Liu et al., 2010).
Although the number of profiles tends to vary depending on
sample characteristics (e.g., child’s age, assessment via parental
report versus behavioral observation), most researchers identify
3–5 temperament profiles in early childhood (Beekman et al.,
2015; Caspi & Silva, 1995; Gartstein et al., 2017; Janson &
Mathiesen, 2008; Komsi et al., 2006; Lin, Ostlund, Conradt,
Lagasse, & Lester, 2018; Planalp & Goldsmith, 2020; Putnam &
Stifter, 2005; Sanson et al., 2009; Scott et al., 2016). One commonly identified profile is characterized by above-average levels
of activity and negative affect. This profile is highly heritable
(Planalp & Goldsmith, 2020; Scott et al., 2016), stable across
early childhood (Beekman et al., 2015; Komsi et al., 2006; Van
Den Akker, Deković, Prinzie, & Asscher, 2010), and predicts
externalizing and, to a lesser extent, internalizing problems
(Janson & Mathiesen, 2008; Sanson et al., 2009; Van Den Akker
et al., 2010). Due to inconsistencies in naming conventions, this
profile has been referred to by various names including undercontrolled (Janson & Mathiesen, 2008; Komsi et al., 2006), high reactive (Prokasky et al., 2017), reactive/inhibited (Sanson et al., 2009),
and active reactive (Beekman et al., 2015).
A second often-identified profile is likewise characterized by
high negative affect, but also includes below average levels of positive affect, activity, and regulatory capabilities (e.g., negative reactive, Beekman et al., 2015; negative reactive, dysregulated, Lin
et al., 2018; unregulated, Prokasky et al., 2017; dysregulated, negative reactive, Scott et al., 2016). A similar profile characterized
specifically by high fear relative to other dimensions of negative
affect has also been identified (Beekman et al., 2015; Janson &
Mathiesen, 2008; Putnam & Stifter, 2005; Van Den Akker et al.,
2010). These profiles predict childhood behavior problems as
well (Lin et al., 2018; Stifter, Putnam, & Jahromi, 2008), and
are reminiscent of the behavioral inhibition typology identified
by Kagan and colleagues (Garcia-Coll, Kagan, & Reznick, 1984;
Kagan & Snidman, 1991).
Two additional profiles are also commonly identified. One
profile includes infants who exhibit high levels of positive affect
and self-regulation (e.g., positive reactive, Beekman et al., 2015;
high positive affect, well regulated, Lin et al., 2018; well regulated,
positive reactive, Scott et al., 2016), and another includes infants
who are average to slightly below average levels on all temperament
dimensions (e.g., unremarkable, Janson & Mathiesen, 2008; moderately low reactive, moderately dysregulated, Lin et al., 2018; typical,
Planalp & Goldsmith, 2020; low/low, Putnam & Stifter, 2005;
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average, Prokasky et al., 2017). Together, these profiles offer a
robust and reliable representation of infant behavior, and may
serve to link a mother’s transdiagnostic vulnerabilities to psychopathology risk in her offspring.
Present study
Our goals for the present study were threefold. First, we sought to
characterize individual differences in the trajectory of maternal
hostility from pregnancy to 16 months postpartum. Few studies
have examined the trajectories of maternal emotionality during
the transition to parenthood, with the majority of the published
findings focused on clinical symptoms. Putnam and colleagues
(Putnam et al., 2017), for example, found that trajectories of
depressive symptoms for 95% of women in their sample (N =
615) were best characterized as stable or decreasing from pregnancy to 5 years postpartum. In line with these longitudinal studies of clinical symptoms, we hypothesized that, on average,
hostility would decrease linearly across time, although trajectories
would differ between mothers. However, to our knowledge, no
study to date has examined trajectories of maternal hostility
from pregnancy through the first two years postnatal. Given the
dearth of research on the topic, we consider this an exploratory
hypothesis that may inform future research.
Second, we examined whether level (prenatal) and change
(pregnancy to 16 months postnatal) in maternal hostility were
predicted by prenatal substance use. We hypothesized that pregnant women who used both marijuana and tobacco would report
higher levels of hostility concurrently and would maintain higher
levels over time relative to pregnant women who used only
tobacco prenatally, as well as women who did not use either substance. We considered this hypothesis to be exploratory given the
dearth of research on trajectories of co-use in pregnancy and
maternal emotionality.
Third, we tested the hypothesis that 16-month-old infants of
mothers who reported higher hostility while pregnant and maintained higher levels over time would exhibit a dysregulated temperament phenotype. We predicted that four temperament
profiles would be identified, consistent with prior research on
similarly aged infants from high-risk backgrounds (Beekman
et al., 2015; Lin et al., 2018). We hypothesized that higher levels
of prenatal hostility and larger increases in hostility across time
would be associated with an infant’s membership in a temperament profile characterized by above average levels of negative
affect and below average levels of attention and inhibitory control
(e.g., negative reactive, Beekman et al., 2015; negative reactive, dysregulated, Lin et al., 2018). Consistent with prior research (Lin
et al., 2018), we did not expect a mother’s substance use while
pregnant to be directly related to her infant’s membership in a
specific temperament profile. Given established links between prenatal substance use and maternal hostility, as well as between
maternal hostility and child behavior, we explored whether maternal hostility mediated the association between a mother’s substance use while pregnant and her infant’s membership to a
temperament profile.
Method
Procedure
All procedures for the current study were approved by the university’s Institutional Review Board (see Eiden et al., 2020 for detail
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discussion of sample selection). Women came in to the laboratory
during each trimester of pregnancy, with informed written
consent collected at the first trimester visit. Mother–infant
dyads returned for additional laboratory assessments at 2, 9,
and 16 months postpartum.
Participants
Women in their first trimester of pregnancy were recruited from a
local hospital at their first prenatal appointment. Women were eligible if they were < 20 weeks’ gestation, having a singleton birth,
aged 18 years or older, using no illicit drugs other than cannabis,
no heavy alcohol use (women drank < 4 drinks per occasion and
did not average > 1 drink a day), and were able to complete the
self-report screening form in English. Use of cigarettes, alcohol,
and illicit substances (e.g., cannabis, methamphetamine, cocaine,
opioids) were assessed via the Time Follow-Back Interview (TLFB;
Sobell & Sobell, 1992) and salivary assays at the end of each trimester. Newborn meconium was also tested to determine fetal
exposure to cigarettes and a range of illicit substances. Given
the initial goal of the study to examine effects of maternal prenatal
tobacco use on developmental mechanisms and outcomes of their
offspring, tobacco users were oversampled based on this initial
screener so that the closest eligible nonsmoking woman (matched
on maternal age and highest educational attainment) was
recruited for every two smoking women. This allowed for a full
range of light to heavy smokers, and accounted for the likely scenario of greater attrition among tobacco smokers.
A total of 258 mother–infant dyads participated in the
2-month appointment, at which time they were considered
officially enrolled. One mother–infant dyad was excluded from
analyses because infant meconium was positive for methamphetamine, two infants were excluded because they had hydrocephaly,
two were excluded because of a later diagnosis of autism, one was
excluded because of maternal binge drinking during pregnancy,
and one additional participant was excluded due to low maternal
cognitive functioning. Finally, four participants were excluded
because they were assigned to the tobacco control group, but
were smoking moderate amounts of marijuana during pregnancy,
resulting in a final sample size of 247 (69 nonsmokers, 81
tobacco-only smokers, and 97 tobacco and marijuana smokers).
Demographic information was collected at the first trimester
appointment. Maternal age ranged from 18 to 39 (M = 24.09,
SD = 5.00), and mothers were 51% African-American, 31%
Caucasian, 19% Hispanic, and 8% other or mixed race with several
mothers reporting more than one race. Approximately 46% percent
of women were married or living with their partner at the first
prenatal appointment, 33% were in a relationship but not living
with their partner, 20% were single, and 1% were divorced.
Approximately 29% of women had less than a high-school education, 29% completed high school, 29% completed some college
courses but did not earn a degree, 9% had a vocational degree or
technical training degree, and 4% received a Bachelor’s degree.
Thus, the sample consisted of primarily young, unmarried,
women of color with lower levels of educational attainment.
Demographic information for the sample is presented in Table 1.
Measures
Maternal prenatal substance use
Maternal prenatal substance use was measured through multiple
methods including self-reports and biological assays. We
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B.D. Ostlund et al.
administered the TLFB (Sobell & Sobell, 1992) toward the end
of each trimester, which yielded daily data regarding maternal
substance use. Mothers were provided with a calendar on which
they identified approximate conception date as well as important
events (e.g., holidays, birthdays, parties, sports events, anniversaries, funerals, vacations) as anchor points to aid recall. The TLFB
is a reliable and valid method of obtaining daily data on patterns
of substance use, including tobacco and cannabis (Robinson,
Sobell, Sobell, & Leo, 2014), has good test–retest reliability, and
is highly correlated with other intensive self-report substance
use measures (Brown et al., 1998). The TLFB yielded data on
the average number of cigarettes and joints smoked per day across
the entire pregnancy, as well as the average number of standard
alcoholic drinks per day across pregnancy. All mothers smoked
combustible cigarettes and none were e-cigarette users.
In addition to maternal self-reports, maternal oral fluid samples were collected at each trimester and analyzed by the US
Drug Testing Laboratory (Des Plaines, IL) for cotinine, the primary nicotine biomarker, and for THC, the primary psychoactive
component of cannabis. Cotinine assays were conducted with
enzyme-linked immunosorbent assay (ELISA) or liquid
chromatography-tandem mass spectrometry (LC-MS/MS) at
10 ng/mL cutoff, and ranged from 0 to 569 ng/mL. Assays for
THC were conducted with immunoassay screening (4.0 μg/L cutoff) and GC–MS confirmation (4.0 μg/L cutoff). Infant meconium samples were collected across several days after delivery
until the appearance of milk stool, and were assayed with a validated LC–MSMS method (Gray et al., 2010a) at 2.5 ng/g nicotine,
1 ng/g cotinine, and 5 ng/g OHCOT, and with a validated twodimensional GC–MS analytical method for THC, 11-hydroxyTHC; 8,11-dihydroxy-THC; 11-nor-9-carboxy-THC (THCCOOH),
and cannabinol (Gray et al., 2010b). Limits of quantification for cannabinoid meconium assays were 10 ng/g for all analytes, except
11-hydroxy-THC at 15 ng/g.
Mothers were assigned to the tobacco smoking group if they
self-reported smoking during pregnancy on the screener or the
TLFB, if oral fluid samples were cotinine positive, or if infant
meconium was positive for cotinine, nicotine, or trans-3′ hydroxycotinine (OHCOT). Mothers were assigned to the co-exposed
group (tobacco and marijuana smokers) if, in addition to meeting
the criteria for the tobacco group, they also self-reported cannabis
use during pregnancy, or if infant meconium was positive for cannabinoids, or if maternal oral fluid was positive for Δ9-THC in
any of the three trimesters. Mothers were assigned to the control
group if all of the above criteria were negative each trimester during pregnancy.
Sociodemographic risk
Sociodemographic risk was calculated as a composite of maternal
race, education, occupation, and partner status. For all items, a
higher score was indicative of greater risk. The maternal race variable acted as a proxy for structural barriers and bias faced by
individuals from marginalized groups. Risk was coded as positive
(1) if mothers indicated that they were nonwhite (69% met this
criterion). For maternal education, risk was positive (1) if the participant had not received a high school diploma or equivalent
(29.1% met this criterion). Maternal occupation was coded
using the Hollingshead scale (M = 2.06, SD = 1.60, Range = 1–8).
The score was then divided by the maximum value of 9 in
order to create a proportion, and was then recoded so that higher
numbers indicated greater risk (lower occupational status). For
partner status, risk was positive (1) if the participant was not
1571
Development and Psychopathology
Table 1. Demographic information.
N
M/%
SD
Range
Age (years)
247
24.09
5.00
18–39
Education (years)
247
12.31
1.89
7–16
African-American
126
51%
Hispanic/Latino
47
19%
113
46%
THC & tobacco
69
28%
Tobacco only
81
33%
97
39%
247
0.49
0.25
0.04–0.89
Prenatal
229
2.71
0.72
1.18–4.82
2 months
241
2.48
0.71
1.21–4.50
9 months
210
2.36
0.65
1.11–4.11
16 months
200
2.41
0.70
1.04–4.46
Female
116
47%
Gestational age (weeks)
247
38.89
1.82
26–42
Birth weight (grams)
247
3234.09
577.57
767–4795
Birth length
241
50.10
2.78
33.00–57.50
Maternal characteristics
Married/living with partner
Prenatal substance use
None
Sociodemographic risk
a
Hostility (BPQ)b
Infant characteristics
Small for gestational age
a
31
12.65%
Sociodemographic risk composite of maternal race, education, occupation, and partner status.
Buss–Perry Aggression Scale (Buss & Perry, 1992).
b
married or living with a partner (54.7% met this criterion). The
final sociodemographic cumulative risk variable was created by
averaging the four items described above, with a possible maximum score of 1 (M = 0.49, SD = 0.25, range = 0.04–0.89).
Maternal pre-/postnatal hostility
Maternal hostility was self-reported in the third trimester (M = 2.71,
SD = 0.72), and at child age of 2 (M = 2.48, SD = 0.71), 9 (M = 2.36,
SD = 0.65), and 16 months (M = 2.41, SD = 0.70) using the
Buss-Perry Aggression Questionnaire (Buss & Perry, 1992), which
contains 29 items measuring anger and hostility (e.g., ‘I have
become so mad that I have broken things’). Items are measured
on a 5-point scale ranging from 1 (extremely uncharacteristic of
me) to 5 (extremely characteristic of me), thus higher scores reflect
more hostility. Internal consistency was excellent across all time
points, with Cronbach’s α ranging from .91 to .92.
Infant temperament
Infant temperament was assessed via maternal report of the
Toddler
Behavior
Assessment
Questionnaire
(TBAQ;
Goldsmith, 1996) at the 16-month appointment. The TBAQ consists of 120 items measuring 11 different domains of temperament. Each item is rated on a Likert-type scale ranging from 1
(never) to 7 (always). Subscales include activity level, anger, interest, object fear, pleasure, sadness, social fear, and soothability (10
items each), as well as perceptual sensitivity (11 items), inhibitory
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control (13 items), and appropriate attentional allocation (16
items). Internal consistency was good for most subscales (αs ranging from .71 to .79). Reliability was lower for interest (α = .69),
sadness (α = .65), social fear (α = .58), activity level (α = .58),
inhibitory control (α = .54), and attention (α = .53) subscales.
Descriptive information and correlations among temperament
dimensions are reported in Table 2.
Infant behavioral reactivity was assessed via a standardized
paradigm intended to elicit anger and frustration (Goldsmith &
Rothbart, 1999). In this paradigm, infants were allowed to play
with an attractive toy for 30 s while seated in a high chair. The
caregiver was seated next to the child, but was asked not to engage
with the child during the assessment. Once the child was engaged
in the toy, a research assistant standing behind the high chair
placed her hands on the child’s forearms, moved them to the
child’s sides, and held them there for 30 s, while maintaining a
neutral expression. After the first trial, the research assistant
engaged the child with the toy for another 30 s followed by a second 30-s trial of arm restraint. The session was stopped (N = 5) if
the child reached a maximum distress code, defined as the child
reaching the highest intensity of negative affect of a full cry, or at
the caregiver’s request. Following the Laboratory Temperament
Assessment Battery (LabTAB) manual (Goldsmith & Rothbart,
1999), these children were assigned the maximum distress code
for the remainder of the session. The child was allowed to play
with the toy at the end of the two trials.
0.88
0.95
0.98
0.60
0.71
0.84
0.88
0.94
0.95
1.00
1.12
0.99
SD
Note: * p < .05, ** p < .01, *** p < .001. “Struggle” = behavioral reactivity based on observational assessment of an arm restraint task (Goldsmith & Rothbart, 1999). Scores on all temperament dimensions excluding “Struggle” were calculated based on
maternal report of infant behavior at 16-months of age via the Toddler Behavior Assessment Questionnaire (TBAQ; Goldsmith, 1996). Scores for TBAQ subscales were not calculated if subscale was missing 50% of their respective items.
5.48
4.06
198
198
3.35
196
3.93
194
3.84
4.35
200
199
5.09
189
3.60
197
3.93
1.47
Mean
194
199
3.92
190
N
2.50
—
—
0.36***
0.23**
0.17*
0.61***
0.16*
0.31***
0.06
0.06
0.13
−0.20**
0.21**
0.46***
−0.04
−0.08
−0.28***
0.15*
0.09
−0.09
0.12
0.15*
11. Interest
12. Pleasure
—
0.12
—
0.48***
−0.14*
0.27***
−0.30***
0.22**
−0.04
0.42***
−0.14
−0.07
0.06
0.23**
0.44***
−0.15*
0.06
0.09
9. Attention
10. Perceptual sensitivity
0.58***
—
—
−0.51***
0.31***
−0.35***
−0.15*
−0.08
−0.51***
−0.11
8. Inhibitory control
—
−0.17*
0.44***
−0.17*
0.16*
−0.21**
−0.24***
0.13
0.43***
0.13
0.14
6. Soothability
7. Activity
−0.29***
—
—
0.19*
0.38***
0.25***
0.21**
0.65***
0.19*
−0.14
4. Social fear
5. Sadness
—
0.44***
—
0.12
−0.01
2. Anger
3. Object fear
—
1. Struggle
−0.04
11.
10.
9.
8.
7.
6.
5.
4.
3.
2.
1.
Table 2. Descriptive information and correlations among temperament dimensions.
200
B.D. Ostlund et al.
12.
1572
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Both trials were coded in six 5-s epochs. Intensity of anger and
intensity of struggle were the primary measures used in the current analyses. For each 5-s epoch, the peak intensity of anger
was scored using Affex (Izard, Dougherty, & Hembree, 1983),
adapted from Izard’s Maximally Discriminative Facial
Movement Coding System (1979). Both peak intensity of anger
and struggle were coded on a scale ranging from 0 to 3, with
higher scores indicating higher intensity of anger and struggle.
The affect expression scores for each 5-s epoch were averaged
for each trial in order to create two composite scores for each
trial, reflecting average intensity of anger and sadness for Trial
1 and Trial 2. Higher scores indicated higher arousal or reactivity.
Two coders blind to all information about the families coded
behavioral reactivity. Interrater reliability was calculated for 10%
of the tapes with intra-class correlation coefficients ranging
from .91 to .96.
Infant behavior problems and competences
Infant behavior problems and competence were assessed at the
16-month appointment via maternal report of the Brief
Infant-Toddler Social and Emotional Assessment (BITSEA; Carter
& Briggs-Gowan, 2005). The BITSEA is a 42-item scale with
answers ranging from 0 (not true/rarely) to 2 (very true/ often).
For the current study, the problem subscale (31 items, e.g., “Cries
or has tantrums until he or she is exhausted.”) and competence subscale (11 items, e.g., “Tries to help when someone is hurt (e.g., gives
a toy).”) were used. The problem subscale reflects maladaptive patterns of child behavior (e.g., age-inappropriate impulsivity, defiance,
or aggressiveness), whereas the competence subscale is viewed as
reflecting age-appropriate social–emotional skills, such as compliance, attention regulation, emotional awareness, and prosocial
peer behavior (Carter, Briggs-Gowan, Jones, & Little, 2003).
Scores on the problem scale of ≥ 15 for boys and ≥ 13 for girls indicate children in the possible problem range, while competence
scores of ≤ 14 for boys and girls suggests the possible deficit/
delay range. Internal consistency of the scale was good for the problem scale (α = .83) and lower for the competence scale (α = .67).
Analytic strategy
Data analysis was conducted in R v4.0.2 (R Core Team, 2020). We
first estimated latent profiles of infant temperament using standardized scores for the arm restraint and TBAQ using the
tidyLPA package (Rosenberg, Beymer, Anderson, van Lissa, &
Schmidt, 2018). Missing data were handled using missForest
(Stekhoven & Bühlmann, 2012), an iterative machine learning
imputation method (Breiman, 2001; Tang & Ishwaran, 2017).
The best fitting model was determined based on the following criteria: a small Bayesian information criteria (BIC), indicating better relative model fit (Schwarz, 1978), a large entropy, indicating
higher confidence in classification (Celeux & Soromenho, 1996), a
minimum of 25 infants as members of the smallest profile (Lubke
& Neale, 2006), and interpretable profile solutions. Infant membership to a temperamental profile from the best fitting class solution was dichotomized (yes/no) in relation to a reference group
and included in subsequent analyses. We examined whether
infant temperament profiles were associated with key health and
demographic variables, including maternal age at recruitment,
maternal relationship status, maternal education, infant sex, gestational age, birth weight, and whether the infant was born small for
gestational age (i.e., age-adjusted birth weight below tenth percentile). Variables that were associated with temperament profiles
1573
Development and Psychopathology
Table 3. Summary of fit statistics for latent class analysis of infant
temperament.
Class
BIC
Entropy
Smallest profile
1
7165.24
2
6940.50
0.77
84 (41%)
3
6880.06
0.80
32 (16%)
4
6819.74
0.82
32 (16%)
5
6841.12
0.82
23 (11%)
—
—
Note: N = 207.
BIC = Bayesian information criteria
were included as covariates in the path analysis (Maxwell,
Delaney, & Kelley, 2018).
Next, we fit an unconditional latent growth curve model to
examine level and change in maternal hostility from pregnancy
to 16 months postnatal. Analyses were conducted using maximum likelihood estimation with robust standard errors (MLR)
and full information maximum likelihood (FIML) in the lavaan
package (Rosseel, 2012). Paths to observed variables were set to
1 for the latent intercept variable. For the latent slope variable,
paths to observed variables were set to 0, 1, 2.75, and 4.50, to
reflect the number of months from the prenatal assessment
divided by a constant (4).
The unconditional latent growth curve model was then used to
assess whether a mother’s substance use prenatally, as well as her
hostility while pregnant and from pregnancy to 16 months postnatal, predicted individual differences in her infant’s temperament
(i.e., conditional latent growth curve model). A mother’s prenatal
substance use was effects coded, yielding two comparisons: (a)
pregnant women who used both marijuana and tobacco or
tobacco only were compared to pregnant women who did not
use substances prenatally, and (b) pregnant women who used
tobacco but not marijuana were compared to women who used
both marijuana and tobacco. Comparison 1 examined the effect
of prenatal substance use (vs. no use) on infant outcomes, while
Comparison 2 assessed differences between co-use and use of
tobacco alone. Model fit was considered good if the following criteria were met: a comparative fit index (CFI) > 0.95, a root mean
square error of approximation (RMSEA) < 0.06, a standardized
root mean square residual (SRMR) < 0.08, and a nonsignificant
χ 2 test (Hu & Bentler, 1999). We tested the significance of the
latent growth parameters as mediators of the proposed link
between prenatal maternal substance use and toddler temperament profiles within the same path model based on 10,000 bootstrapped samples with 95% bias-corrected confidence intervals
(CIs). Finally, we examined post hoc comparisons between temperament profiles and the problem behavior and competences
scales of the BITSEA to aid interpretation of these personcentered variables.
Results
Temperament profiles
Descriptive data and bivariate correlations among infant temperament dimensions assessed at 16 months of age are presented in
Table 2. Model fit indices, entropy, and sample size for a solution’s smallest profile are presented in Table 3. The BIC was lowest for the four-class solutions. The four- and five-class solutions
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had the largest entropy values. Given that it had the lowest BIC, a
large entropy, and interpretable and adequately sized profiles, the
four-class solution was deemed the most parsimonious.
Temperament profiles from the four-class solution were used in
all subsequent analyses and are presented in Figure 1 (see
Supplementary Information for density plots of each temperament dimension based on profile membership).
High reactive
The first profile consisted of 28% of the sample (n = 57; 27
females, 30 males). This profile was labeled high reactive because
it comprised infants with higher levels of anger, sadness, and
object fear, in combination with low levels of soothability and
inhibitory control. In addition, these infants were characterized
by above average perceptual sensitivity.
Low reactive
The second profile described the plurality of infants and included
40% of the sample (n = 83; 38 females, 45 males). This group was
named low reactive because these infants struggled the least in
response to the arm restraint task and had above average inhibitory control. Further, these infants had moderately below average
scores across the majority of domains, including interest, pleasure,
anger, sadness, and perceptual sensitivity.
Well regulated
The third profile included approximately 16% of the sample (n =
32; 18 females, 14 males). This group was labeled well regulated
because these infants were characterized by low levels of negative
affect – including low anger, sadness, and object and social fear –
as well as high levels of inhibitory control and soothability. These
infants also had lower activity levels and above average attention,
interest, and pleasure. This profile was included as the reference
condition in all models.
Dysregulated
Lastly, the fourth profile comprised 17% of the sample (n = 35; 18
females, 17 males). This group was named dysregulated due to
having above average levels of anger and sadness in combination
with below average levels of inhibitory control. These infants were
additionally characterized by high activity levels and below average attention and interest.
Maternal hostility
Self-reported hostility for each mother from the third trimester of
pregnancy to 16 months postnatal is presented in Figure 2.
Repeated measures analysis of variance (ANOVA)
Results from a one-way repeated measures ANOVA showed that
maternal hostility significantly differed across time points, although
the effect size was small, F(2.88, 486.38) = 19.65, p < .001, η2g = 0.03.
Pairwise comparisons (Benjamini–Hochberg adjusted; Benjamini
& Hochberg, 1995) revealed that maternal hostility while pregnant
was significantly higher than hostility at each time point ( ps <
.001). Maternal hostility at 2 months postnatal was significantly
higher than hostility at 9 months postnatal ( p = .03), and marginally higher than hostility at 16 months postnatal ( p = .07). Maternal
hostility at 9 and 16 months postnatal did not significantly differ
( p = .40).
1574
B.D. Ostlund et al.
Figure 1. Temperament profiles at 16 months of age. Mean standardized scores on temperament dimension from the Toddler Behavior Assessment Questionnaire
(Goldsmith, 1996) and an arm restraint task (Goldsmith & Rothbart, 1999) are presented. “Struggle” = behavioral reactivity to an arm restraint task at 16 months of
age. “Obj. fear” = object fear. “Inh. control” = inhibitory control. “Perc. sensitivity” = perceptual sensitivity.
Figure 2. Trajectories of self-reported maternal hostility
from the third trimester of pregnancy to 16 months
postnatal. Data from each mother across time are represented by a unique color (a); the solid red line indicates
linear fit. Data from a random 10% of mothers who had
data at each time point are presented in black to exemplify maternal trajectories (b); the remainder of the sample is presented in gray.
Latent growth curve models
The latent growth curve model adequately fit the data; χ2(5) =
32.47, p < .001, CFI = 0.94, RMSEA = 0.15, SRMR = 0.07. The
mean level of hostility in the third trimester of pregnancy
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(intercept) was 2.59. The variance of the latent intercept mean
was significant (z = 8.61, p < .001), indicating that women differed
in their level of hostility while pregnant. The mean slope for hostility was statistically significant and negative (b = −0.06, p < .001),
1575
Development and Psychopathology
Figure 3. Final path model with standardized path coefficients. Solid lines reflect significant associations. A mothers’ prenatal substance use was effects coded,
yielding two comparisons: (a) pregnant women who used both marijuana and tobacco or tobacco only (“THC + Tob. & Tob. only”) were compared to pregnant
women who did not use either substance (“none”); and (b) pregnant women who used tobacco but not marijuana (“tobacco only”) were compared to women
who used both marijuana and tobacco (“THC + Tob.”). Time coding for the latent growth variables reflects the number of months from the prenatal assessment
divided by a constant (4). Temperament profiles were dummy coded; the well-regulated profile served as the reference group for all comparisons.
indicating that, on average, maternal hostility decreased from the
third trimester of pregnancy to 16 months postnatal. Trajectories
of hostility did not significantly differ between mothers (z = 0.53;
p = .59). The latent intercept and slope variables were not correlated (β = −0.05, p = .88).
Path models
Prenatal substance use and prenatal sociodemographic risk were
included as predictors of maternal and infant variables
(Figure 3). The model fit the data adequately; χ2(20) = 61.95,
p < .001, CFI = 0.94, RMSEA = 0.09, SRMR = 0.05. We chose
the well-regulated profile as the reference group and excluded it
from subsequent analyses based on prior findings among infants
with prenatal substance exposure (Lin et al., 2018), and the fact
that this profile was characterized by low negative affect and
high attention, soothability, and inhibitory control (Figure 1).
Associations with temperament profiles were therefore interpreted relative to the well-regulated profile.
Results indicate that, relative to pregnant women who did not
use substances, women who used both marijuana and tobacco
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reported higher levels of hostility while pregnant ( p < .001)
and exhibited less change in hostility over time ( p = .03).
Infants of women who reported higher levels of hostility while
pregnant were more likely to be classified in the high reactive
( p = .03) and dysregulated ( p = .01) profiles. No other paths
were significant ( ps > .11). The model that included infant
birth weight – the only covariate significantly associated with a
temperament profile (low reactive) in multinomial regression
analyses (all other ps > .19 relative to well-regulated reference
group) – also fit the data adequately; χ2(22) = 54.85, p = .001,
CFI = 0.95, RMSEA = 0.08, SRMR = 0.04. Results of this model
indicate that, relative to pregnant women who did not use substances, women who used both marijuana and tobacco reported
higher levels of hostility while pregnant ( p < .001) and exhibited
less change in hostility over time ( p = .05). Moreover, infants of
women who reported higher levels of hostility while pregnant
were more likely to be classified in the dysregulated profile
( p = .04), relative to the well-regulated profile. No other paths
were significant ( ps > .16). We tested whether maternal hostility
while pregnant mediated the link between prenatal substance use
and infant membership in either the high reactive or dysregulated
1576
B.D. Ostlund et al.
Figure 4. Post hoc comparisons among infant temperament profiles and the (A) problem behavior and (B) competence scales of the Brief Infant-Toddler Social and
Emotional Assessment (BITSEA) (Carter & Briggs-Gowan, 2005).
temperament profiles. Neither the path to the high reactive profile
(95% CI [−0.004, 0.026]) nor the dysregulated profile (95% CI
[−0.005, 0.034]) was significant.
Post hoc analyses
To establish criterion validity and aid interpretation, we conducted post hoc comparisons among the observed temperament
profiles and the problem behavior (N = 200, M = 12.50, SD =
6.91) and competence (N = 201, M = 16.31, SD = 3.11) scales of
the BITSEA (Carter & Briggs-Gowan, 2005). Problem behavior
and competence scores were not correlated, r(200) = −.06,
p = .42. One competence score from an infant in the high reactive
profile was identified as an outlier; results remained the same
when this infant was excluded from analyses (results available
upon request). Problem behavior and competence scores were
still not correlated, r(199) = −.05, p = .50.
Using a one-way ANOVA, we found that infant’s problem
behavior significantly differed based on temperament profile
membership, F(3,196) = 15.49, p < 001 (Figure 4). Tukey post
hoc comparisons showed that problem behavior was higher for
infants in the high reactive profile (M = 16.52, SD = 7.49) relative
to both the low reactive (M = 10.87, SD = 5.78) and well-regulated
(M = 7.98, SD = 5.23) profiles ( ps < .001). Problem behavior was
also higher for infants in the dysregulated profile (M = 13.76, SD
= 5.96) relative to the well-regulated profile ( p = .001), but not relative to the low reactive profile ( p = .11). Problem behavior did
not differ between infants in the low reactive and well-regulated
profiles ( p = .13), or between infants in the dysregulated and
high reactive profiles ( p = .17).
Similarly, we found that infant’s competences significantly differed based on temperament profile membership, F(3,197) = 9.70,
p < .001 (Figure 4). Tukey post hoc comparisons showed that
competence was higher for infants in the well-regulated profile
(M = 18.16, SD = 2.68) relative to the dysregulated (M = 15.51,
SD = 2.91) and low reactive (M = 15.31, SD = 2.81) profiles
( ps < .003). Competence was also higher for infants in the high
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reactive profile (M = 17.14, SD = 3.20) relative to the low reactive
profile ( p = .002) as well as the dysregulated profile ( p = .05).
There was no significant difference between the dysregulated
and low reactive profiles ( p = .99), nor between the well-regulated
and high reactive profiles ( p = .40).
Lastly, we examined whether a mother’s level of hostility was
correlated with her 16-month-old infant’s scores on the
BITSEA. Infant problem behavior was positively associated
with maternal hostility during pregnancy (r = .16, p = .03) and
at 2- (r = .23, p = .001), 9- (r = .27, p < .001), and 16- (r = .27,
p < .001) months postnatally. Infant competence was marginally
associated with maternal hostility at 9 months postnatal
(r = −0.13, p = .07); otherwise, these variables were not significantly correlated ( p > .21).
Discussion
Using a prospective longitudinal design, we examined the preand postnatal influence of a transdiagnostic maternal vulnerability
on infant temperament, specifically within the context of varying
levels of substance use exposure in utero. Our study adds to extant
evidence by showing that maternal hostility (a) decreases from the
third trimester of pregnancy to 16 months postpartum, (b) positively associates with co-occurring marijuana and tobacco use
while pregnant, and (c) predicts membership to two behaviorally
dysregulated temperament profiles in their infant. This effect was
specific to the prenatal period: maternal hostility while pregnant
predicted specific infant temperament profiles above and beyond
the influence of postnatal hostility. These temperament profiles
(high reactive and dysregulated) are potential intermediate risk
phenotypes on the path to childhood psychopathology. Our
results underscore the utility of transdiagnostic vulnerabilities,
particularly while pregnant, in understanding the intergenerational transmission of psychopathology risk.
RDoC highlights intermediate phenotypes of psychological
health and dysfunction, encouraging the use of quantitative
approaches that reduce data from multiple dimensions to identify
Development and Psychopathology
individuals who are phenotypically alike. Consistent with this recommendation, we used a person-centered approach and observed
four distinct, homogenous groups of infants based on twelve
dimensions of temperament. These profiles mirror groups identified by multiple other researchers who have used similar analytic
approaches (Beekman et al., 2015; Gartstein et al., 2017; Janson &
Mathiesen, 2008; Komsi et al., 2006; Planalp & Goldsmith, 2020;
Prokasky et al., 2017; Putnam & Stifter, 2005; Sanson et al., 2009;
Scott et al., 2016; Van Den Akker et al., 2010), although not all
studies identified the same four groups in their analyses (see
Ostlund et al., 2021 for discussion).
Most notably, three of the observed temperament profiles –
high reactive, low reactive, and well regulated – resemble groups
identified in two different samples reported on by Lin et al.
(2018), the only other study to our knowledge that has examined
temperament profiles in infants who were prenatally exposed to
substances. Pregnant women in each sample examined by Lin
and colleagues had varying levels of polysubstance use, including
smoking (53%–54%) and marijuana use (18%–23%), despite
being recruited for either cocaine (Maternal Lifestyle Study;
Lester et al., 2001) or methamphetamine (Infant Development,
Environment, and Lifestyle study; Smith et al., 2006) use. The replicability of these profiles is particularly impressive given that
prior studies have utilized a variety of temperament measures
(e.g., Lin et al., 2018; Planalp & Goldsmith, 2020) with children
of various ages (e.g., Beekman et al., 2015; Scott et al., 2016), lending support for the utility of these temperament profiles in
describing phenotypically similar children beginning in the first
year of life. Incorporating evidence from temperament research
may serve to expand RDoC by providing an established theoretical perspective on developmental change, and should be taken
into consideration going forward (Ostlund et al., 2021).
The observed profiles characterize variation on dimensions of
temperament that reflect functioning along continua of multiple
RDoC constructs. In our sample, activity (sensorimotor systems),
anger and sadness (negative valance systems), attention, perceptual sensitivity, and inhibitory control (cognitive systems) were
influential in determining an infant’s membership to a specific
profile. However, when identifying phenotypes that portend
childhood psychological health and dysfunction, the whole may
be greater than the sum of its parts. That is, it may be the confluence of multiple RDoC constructs (characterized by temperament
traits) that gives rise to individual differences in infant behavior.
For instance, given low levels of negative affect (fear, anger,
sadness), high self- and co-regulatory capacities (soothability,
inhibitory control, attention), high level of engagement and
enjoyment in activities such as solitary play (interest, pleasure),
we would expect infants in the well-regulated profile to show
the most adaptive social and emotional outcomes. Post hoc analyses support this prediction, showing that infants in this profile
are reported to have the highest levels of competence concurrently. Inhibitory control and attentional capacities modulate negative affect, become increasingly employed as a young child
develops, and are used together in service of goal-directed behavior (Braungart-Rieker, Hill-Soderlund, & Karrass, 2010; Morales,
Fu, & Pérez-Edgar, 2016). In this way, an infant’s behavior may be
considered as an emergent property of multiple RDoC constructs
that becomes increasingly intertwined across early development
and may be reliably captured via person-centered temperament
profiles. By measuring multiple RDoC constructs, personcentered approaches allow us to pinpoint strengths and weaknesses among homogeneous groups of infants.
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1577
It is also worth considering the caregiving environment in
which an infant’s temperamental proclivities may be displayed
in early childhood. Indeed, infants were more likely to be classified in the well-regulated profile, relative to the high reactive or
dysregulated profiles, if their mothers reported lower levels of hostility while pregnant. Given the negative association between
maternal levels of hostility and sensitive parenting (Eiden et al.,
1999; Schuetze et al., 2006), it follows that these well-regulated
infants may experience a more supportive, nurturing environments relative to their peers. While genetic influences between
maternal hostility and infant temperament cannot be ruled out,
it is worth noting that these infants may ultimately have the
most adaptive outcomes by virtue of a good “match” between
their dispositional traits and their parents’ proclivity toward sensitive parenting (Thomas & Chess, 1977).
Relative to the well-regulated profile, infants were more likely
to be classified in the high reactive or dysregulated profiles if
their mothers reported higher levels of hostility while pregnant.
Both of these temperament profiles were related to higher levels
of problem behavior concurrently. A core feature of each of
these profiles is anger, suggesting homotypic continuity in the
affective repertoire of a highly hostile pregnant women and her
behaviorally dysregulated infant. Perra, Paine, and Hay (2020)
identified subgroups of infants at differential risk for externalizing
psychopathology at age 7 years based on early levels of angeraggressiveness (see also Liu et al., 2018). While infants in the
high anger/high aggressive group tended to maintain risk over
time, the authors found that warm parenting was a protective factor that protected against the escalation in aggression over early
development. On the other hand, socioeconomic adversity predicted membership in the high anger/high aggressive group,
while a mother’s own history of antisocial behavior predicted
escalation in aggression over early development (Perra et al.,
2020).
Unfortunately, the caregiving environment of mothers who are
high in hostility and use marijuana and tobacco prenatally tends to
be characterized by insensitivity (Eiden et al., 1999; Schuetze et al.,
2006). To this end, coercion theory (Patterson, Debaryshe, &
Ramsey, 1989) posits that negative reinforcement patterns in the
caregiver–child relationship contribute to the development of psychopathology when paired with insensitive and inconsistent caregiving. Over time, an infant’s temperament may transact with
their early caregiving environment to increase (or decrease) psychopathology risk (e.g., NICHD Early Child Care Research
Network, 2004; Shaw, Lacourse, & Nagin, 2005). These temperamental differences may therefore affect the dynamic interplay
between the young child and their early environment, which may
lay the foundation for subsequent psychopathology risk throughout
development (Crowell, Puzia, & Yaptangco, 2015).
The two behaviorally dysregulated temperament profiles
diverge, however, when fearfulness, perceptual sensitivity, and
regulatory capacities are considered. Specifically, the constellation
of features that define infants in the dysregulated and high reactive
profile correspond to early behavioral indices of trait irritability
(Beauchaine et al., 2017; Leibenluft & Stoddard, 2015) and behavioral inhibition (Garcia-Coll et al., 1984; Kagan & Snidman,
1991), respectively. Trait impulsivity is thought to be heritable,
possibly via shared sensitivity in mesolimbic dopaminergic functioning (Beauchaine et al., 2017; Gatzke-Kopp, 2011). Indeed,
Field and colleagues (Field et al., 2002, 2008) noted that newborn
level of peripheral dopamine is associated with maternal dopamine levels, and that dopamine levels are lower among newborns
1578
of mothers who reported high levels of anger. Elevated hostility
while pregnant may further potentiate the sensitivity of mesolimbic dopaminergic functioning.
For an infant in the high reactive profile, the proclivity toward
high perceptual sensitivity and negative reactivity may require
greater co-regulatory support from their caregiver during distress
recovery. The dyadic attunement needed for co-regulation is likely
negatively impacted by both maternal hostility and maternal substance use, each of which are independently associated with lower
levels of sensitivity (Eiden et al., 1999; Schuetze et al., 2006).
Based on the prior literature (Beauchaine et al., 2017; Clauss
et al., 2015), the divergence between the two profiles would suggest that infants in the dysregulated profile are at increased risk for
irritability and externalizing problems, while high reactive infants
are more likely to demonstrate social withdrawal and internalizing
difficulties.
It is worth noting that the temperamental characteristics that
define infants in the high reactive profile – perceptual sensitivity,
attention, and negative affect – may also increase these infant’s
sensitivity to both positive and negative aspects of the early caregiving environment (Ellis, Boyce, Belsky, Bakermans-Kranenburg,
& van Ijzendoorn, 2011; Slagt, Semon, Deković, & van Aken,
2016). Specifically, adaptive calibration models suggest that temperamentally reactive infants show an enhanced biological sensitivity to the environment and parental behavior, which in turn is
a core conduit through which the environment “gets under the
skin” to shape psychobiological development (Del Giudice, Ellis,
& Shirtcliff, 2011). Follow-up work will need to more closely capture the temporal dynamics of maternal hostility, maternal behavior, and infant profiles (e.g., latent transition analysis) in order to
better disentangle the mechanisms influencing individual
trajectories.
With this same motivation in mind, we worked to separate
pre- and postnatal influences of maternal hostility on infant
behavioral dysregulation by simultaneously considering level
(prenatal) and change (pregnancy to 16 months postpartum).
Maternal hostility during each of these periods likely operates
via distinct mechanisms to affect the neural, physiological, and
behavioral parameters of the young child. Prenatally, instances
of acute hostility may, for example, be associated with a distinct
physiological profile marked by altered sympathetic activity,
which in turn may restrict uteroplacental blood flow to the
fetus via catecholaminergic pathways (see Rakers et al., 2015 for
animal model). Postnatally, any lasting biological shifts triggered
by in utero exposure could be potentiated by the insensitive and
noncontingent parenting behaviors previously associated with
elevated hostility.
From pregnancy to 16 months postnatal, we observed a linear
decrease in maternal hostility, a pattern that may reflect a regression to a homeostatic set point following normative biological and
behavioral changes from pregnancy to postpartum (e.g.,
Hendrick, Altshuler, & Suri, 1998). This shift may also reflect a
mother’s growing ease and confidence with the daily demands
of child rearing. Thus, infants whose mothers did not display
the typical decreasing trajectory may be particularly vulnerable
to poor adaptive outcomes.
Of course, maternal hostility is not acting in a vacuum. Indeed,
in the current sample, women who used both marijuana and
tobacco reported higher levels of hostility while pregnant and
exhibited less change in hostility over time. It is difficult to determine directionality when considering the association between
maternal hostility and use of marijuana and/or tobacco prenatally,
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B.D. Ostlund et al.
due to their high co-occurrence (Eiden et al., 2011). In addition,
mothers in this sample were disproportionately exposed to a
number of environmental and structural stressors that likely
increased levels of hostility, the incidence of substance use, and
when present, the differential impact of these factors on infants
relative to mothers with greater structural supports (e.g., education, income, and partner status).
These broader stressors likely also impacted other known risk
factors, such as sleep disturbances (e.g., Obeysekare et al., 2020;
Román-Gálvez et al., 2018), relatively poor nutrition (e.g.,
DeCapo, Thompson, Dunn, & Sullivan, 2019; Hurley, Caulfield,
Sacco, Costigan, & DiPietro, 2005), and elevated levels of stress
and distress (e.g., Walsh et al., 2019). More systematic studies
identifying how constellations of transdiagnostic vulnerabilities
influence the development (or maintenance) of intermediate
risk phenotypes in offspring may allow for more precise characterization of core dysfunctions for a mother and her infant that
can be targeted by prevention efforts.
To note some additional limitations in the current study, we
had multiple subscales of the TBAQ show relatively low
Cronbach’s alpha values. This may be attributable, in part, to
the fact that this measure was not designed with a high-risk population in mind, and may have operated differently in the current
sample. We discuss this limitation further in the Supplementary
Information. Nevertheless, the observed temperament profiles
mirror prior work with community samples (e.g., Gartstein
et al., 2017; Planalp & Goldsmith, 2020), lending support to
their replicability across risk status in early childhood. An additional limitation is that mothers reported on their own and
their infant’s behavior at each time point, which may inflate
common-method variance. Acknowledging this potential shortcoming, we did include a behavioral observation variable (arm
restraint) in the LPA. It is worth noting that behavioral reactivity
to the arm restraint task had a modest influence on group differentiation (see Supplementary Figure 2). Nevertheless, recent findings suggest that a mother’s mental health may not bias her report
of infant temperament (Olino, Guerra-Guzman, Hayden, & Klein,
2020), as is commonly assumed. Future research may benefit from
a broader assessment of behavioral data related to temperament as
a complement to parent-reported data. Furthermore, the number
of infants in each of the observed temperament profiles was relatively small, even though our findings correspond to profiles
observed in two other samples of infants prenatally exposed to
substances (Lin et al., 2018).
It is also worth noting that the current sample of pregnant
women were recruited primarily for tobacco use and a subsample
also used marijuana via smoking, which may limit the generalizability of our findings among pregnant women who use marijuana only and use marijuana without smoking (e.g., edible
marijuana). Given that the way in which marijuana is used may
vary based on geographic location and socioeconomic status in
the United States (e.g., Borodovsky, Crosier, Lee, Sargent, &
Budney, 2016), future research that includes a broader definition
of marijuana use and marijuana use without co-use of tobacco is
warranted. Moreover, in order to include ascertainment of substance use based on multiple indices, our analyses were limited
to comparing groups of women who were categorized based on
prenatal cigarette and marijuana use compared to non-use.
Future research might consider a recruitment strategy that is
not based on a case-control design and perhaps use other methods such as propensity score matching on demographics and use
the dose–response measures of substance use in analyses. This
1579
Development and Psychopathology
approach would complement the current findings and provide
insight into whether (and how) prenatal substance use relates to
early childhood temperament in a dose-dependent fashion.
A few strengths of our study are worth highlighting. We prospectively assessed a sample of primarily young, low-income
women and their infants from pregnancy to 16 months postpartum. We adopted a rigorous methodology for collecting longitudinal data, which included a detailed assessment of a woman’s
substance use while pregnant and the use of both parent-report
and behavioral observation data to characterize infant temperament
profiles. We also incorporated multiple statistical methods – latent
growth curve modeling and LPA – to examine how prenatal hostility, as well as change in maternal hostility, are associated with an
infant’s temperament profile membership. It is worth noting that
we only examined linear change in maternal hostility over time.
Yet, an infant’s development over the first 16 months of life is dramatic: a young child’s emotional, cognitive, and motor repertoire
quickly evolve from rudimentary and atomized to sophisticated
and contingent, introducing an ever-changing set of challenges a
parent must adapt to. Future research might consider examining
dynamic change (e.g., quadratic, piecewise) beginning in early pregnancy and proceeding through the first 2 years of life.
Finally, our sample of families was racially diverse (51%
African-American) as well as demographically and economically
high-risk (predominately young, low income, and single) relative
to many studies that examine pre- and early postnatal transdiagnostic vulnerabilities. Given the underrepresentation of diverse
populations in psychological research (Gatzke-Kopp, 2016), and
the disparate rates of perinatal morbidity and mortality among
African-American women (Moaddab et al., 2018; Saluja &
Bryant, 2020; Somer, Sinkey, & Bryant, 2017), future research
should build on our preliminary findings to further understand
and disrupt transdiagnostic vulnerabilities for mothers and
infants from historically underrepresented groups during the
pre- and postnatal period.
Conclusion
Our findings advance our understanding of the intergenerational
transmission of psychopathology risk in two important ways.
First, we measured trajectories of a transdiagnostic vulnerability
from pregnancy to 16 months postpartum, incorporating change
into our conceptualization of pre- and early postnatal maternal
risk. We showed that a mother’s level of hostility while pregnant
and across her infant’s early development are related to use of
marijuana and tobacco prenatally and, in the case of prenatal hostility, associates with her infant’s temperament. Second, we
replicated temperament profiles that have been identified by
other researchers in a sample of infants with varying levels of prenatal substance exposure and psychosocial stressors, demonstrating the utility of person-centered approaches for identifying
RDoC-informed phenotypes in the first two years of life.
Integrating a transdiagnostic perspective into our approach to
perinatal mental health and early child development may ultimately provide specific targets for preventative services aimed at
reducing childhood psychopathology, via early dissemination of
parenting interventions that challenge dysfunctional cognitive
biases, ameliorate familial risk, and support an infant’s emotional
development.
Supplementary Material. The supplementary material for this article can
be found at https://doi.org/10.1017/S0954579421001000
Downloaded from https://www.cambridge.org/core, subject to the Cambridge Core terms of use.
Acknowledgments. We would like to thank the families who participated in
our study. Special thanks to Dr. Amol Lele for collaboration on data collection
at Women and Children’s Hospital of Buffalo.
Author Contributions. S. Shisler, S. Godleski, P. Schuetze, and R.D. Eiden
contributed to the study concept and data collection. B.D. Ostlund and
S. Terrell performed the data analysis and interpretation under the supervision
of K. Pérez-Edgar and R.D. Eiden. All authors contributed to drafting the
manuscript. All authors approved the final version of the manuscript.
Funding Statement. This manuscript was supported by the National
Institute on Drug Abuse under award number R01DA01963201. The content
is solely the responsibility of the authors and does not necessarily represent the
official views of the National Institute on Drug Abuse or the National
Institutes of Health.
Conflicts of interest. None
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