Journal Pre-proof Maternal Psychological Stress Moderates Diurnal Cortisol Linkage in Expectant Fathers and Mothers during Late Pregnancy Stephen H. Braren, Rosemarie E. Brandes-Aitken Annie Ribner Andrew Perry, Blair Clancy, the New Fathers and Mothers Study (NewFAMS) Team
PII:
S0306-4530(19)30636-5
DOI:
https://doi.org/10.1016/j.psyneuen.2019.104474
Reference:
PNEC 104474
To appear in:
Psychoneuroendocrinology
Received Date:
8 July 2019
Revised Date:
10 September 2019
Accepted Date:
8 October 2019
Please cite this article as: Braren SH, Brandes-Aitken Annie Ribner Andrew Perry RE, Clancy B, Maternal Psychological Stress Moderates Diurnal Cortisol Linkage in Expectant Fathers and Mothers during Late Pregnancy, Psychoneuroendocrinology (2019), doi: https://doi.org/10.1016/j.psyneuen.2019.104474
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Maternal Psychological Stress Moderates Diurnal Cortisol Linkage in Expectant Fathers and Mothers during Late Pregnancy
Braren, Stephen H.1*, Brandes-Aitken, Annie, Ribner, Andrew, Perry, Rosemarie E.1, Blair,
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Clancy1, and the New Fathers and Mothers Study (NewFAMS) Team1,2,3
Department of Applied Psychology, 246 Greene Street, Kimball Hall, 8th Floor, New York
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Leiden University, Leiden, Netherlands University of Cambridge, Cambridge, United Kingdom
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University, New York, NY, 10012, United States
Phone: +1 347 356 8422
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*Corresponding Author Address: 627 Broadway, 8th Floor, New York, NY, 10012, United States
Highlights
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E-mail:
[email protected] (S. Braren)
Diurnal cortisol linkage was observed among first-time expectant parents (N=385).
Cortisol linkage was moderated by maternal psychological stress.
Cortisol linkage was stronger in couples with higher maternal psychological stress.
Cortisol linkage was not observed for couples with lower maternal psychological stress.
At higher maternal stress, paternal cortisol may buffer or amplify maternal cortisol.
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Abstract
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Using data from a large international sample (N=385) of first-time expectant parents, the current analysis investigated whether expectant parents demonstrated diurnal cortisol linkage in late pregnancy and whether self-reported psychological stress moderated this linkage. At approximately 36 weeks gestation, mothers and fathers collected saliva samples in their home at three times on two consecutive days and reported on their psychological stress. Results from multilevel models indicated that there was significant positive within-couple diurnal cortisol
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linkage on average for the whole sample. However, this linkage was moderated by maternal self-
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reported psychological stress. Specifically, for couples with higher maternal psychological stress, cortisol linkage was strong. Conversely, for couples with lower maternal psychological stress,
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maternal and paternal cortisol were unrelated. These findings suggest that among higher-
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maternal-stress couples, lower paternal cortisol may buffer maternal cortisol, whereas higher paternal cortisol may amplify maternal cortisol. Our results support the idea that interpersonal
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psychological and physiological stress in close relationships is interdependent and mutually influenced. Further, our findings contribute to the field’s understanding of interpersonal
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processes during pregnancy, which may have health-related implications in the prenatal and postnatal periods for both parents and the developing child.
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Keywords: cortisol, synchrony, parenting, prenatal, stress, interpersonal physiology
1. Introduction
The regulation of maternal cortisol during pregnancy is critical for the healthy functioning and development of both the mother and her child. Cortisol is essential for normative maternal and fetal glucose metabolism and also for healthy growth and maturation of the fetus (Morsi et al., 2018). Although cortisol regulation depends on individual characteristics such as psychological
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stress and emotional well-being, cortisol is also influenced by social factors such as interpersonal relationships (Butler, 2011; Cox & Paley, 1997; Sbarra & Hazan, 2008). A growing literature shows that in close relationships partners share similar patterns of cortisol activity over time (Timmons et al., 2015). Such physiological “linkage” may reflect the capacity for couples to modulate and coregulate one another’s stress physiology. Given the significance of cortisol for fetal health and development, cortisol linkage between partners during pregnancy may play an
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especially prominent role in the social regulation of maternal glucocorticoids. Only a few studies
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with small samples, however, have examined cortisol linkage between partners during
pregnancy. Notably, several studies with non-expectant couples indicate that cortisol linkage is
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stronger among couples with high levels of psychosocial stress (Timmons et al., 2015). Because
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pregnancy is a time of heightened mental and emotional strain, cortisol linkage may be most important for mothers reporting high levels of psychological stress but whose partners have low
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cortisol levels. No studies with expectant parents to our knowledge, however, have examined associations between psychological stress and cortisol linkage. Understanding relations between
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stress and the social regulation of cortisol during pregnancy will provide important insight regarding possible targets for promoting fetal health and development. 1.1. Cortisol linkage in close relationships Physiological linkage can be defined broadly as the temporal association between a dyad’s
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physiological activity. Theory and research suggest that physiological linkage is a dynamic, interpersonal process of communication, co-regulation, and affiliative bond formation (Feldman, 2017; Field, 2012; Sbarra & Hazan, 2008; Timmons et al., 2015). Several studies have documented cortisol linkage between partners in romantic relationships (see Timmons et al., 2015 for a review). These studies found that cortisol linkage was positively associated with
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physical proximity and time spent together (Laws et al., 2015; Papp et al., 2013; Saxbe & Repetti, 2010), suggesting that linkage results from shared experiences and environments. However, cortisol linkage has also been associated with marital strain, aggression, and conflict (Laws et al., 2015; Liu et al., 2013; Saxbe & Repetti, 2010; Saxbe et al., 2015; Schneiderman et al., 2014). In general, previous research on cortisol linkage in romantic relationships indicates that some degree of cortisol linkage is seen in higher quality relationships, but stronger linkage is
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found in poorer quality relationships.
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These findings are consistent with family systems theory and negative affect reciprocity theory, which broadly posit that each partner’s stress is not an isolated affair, but a shared,
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interpersonal experience driven by reciprocal feedback processes between partners (Butler, 2011;
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Cox & Paley, 1997; Levenson & Gottman, 1983; Sbarra & Hazan, 2008). More specifically, it has been theorized that couples with closely linked levels or patterns of cortisol may be more
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susceptible to each other’s stress. These couples can get caught in a positive feedback cycle of negative emotionality in which partners continually and mutually up-regulate each other’s
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physiological and psychological stress, thus becoming increasingly physiologically linked. Alternatively, couples with moderate degrees of cortisol linkage may be better able to downregulate each other’s stress. However, much still remains to be understood about when linkage is “good” or “bad,” especially during pregnancy.
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1.2. Pregnancy, psychological stress, and cortisol linkage Cortisol linkage may be particularly important during pregnancy because it is a sensitive period of development not only for the fetus, but also for the parents (Glynn et al., 2018; Saxbe et al., 2018). As such, during this time of transformation, expectant parents are likely especially susceptible to influence by each other’s psychological and physiological stress. Despite this
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significance, only a few studies with small samples have investigated associations between expectant parents’ cortisol activity. These studies found that partners’ cortisol levels were correlated at various times during pregnancy (Edelstein et al., 2015; Storey et al., 2000; Berg & Wynne-Edwards, 2002). However, these studies did not evaluate the role of moderators, which previous research on cortisol linkage indicates is an important consideration in evaluating whether linkage is adaptive or maladaptive.
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Several factors are potentially related to cortisol linkage among expectant parents, but in
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particular psychological stress is likely a principal moderating factor, especially among first-time parents. Psychological stress is a common feature of pregnancy because it is a time of immense
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change for both partners (Philpott et al., 2017; Saxbe et al., 2018). Physiologically, mothers and
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fathers both experience drastic yet normative hormonal changes, such as increases in cortisol (Gettler, 2014; Glynn & Sandman, 2011). Likewise, transitions in roles and routines accompany
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shifts in behaviors and emotions, which are often associated with heightened stress, including increased risk for compromised emotional and mental health (Baldwin et al., 2018; Saxbe et al.,
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2018). Furthermore, psychological stress during pregnancy has been associated with altered cortisol activity in both parents (Kivlighan et al., 2008; Obel, et al., 2005; Feinberg et al., 2013; Kuo et al., 2018). Relatedly, psychological stress and cortisol have been related to postnatal factors in both the parents and child (e.g., Bos, 2017; Bos et al., 2018; Zijlmans et al., 2015;
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Barrett & Fleming, 2011). For these reasons, examining associations between psychological stress and cortisol linkage during pregnancy is important for understanding how interpersonal psychophysiology may shape parent and child health and development. 1.3. The present study
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The present study extends previous research on cortisol linkage by using a large international sample of first-time expectant parents to investigate interactions between partners’ psychological and physiological stress during pregnancy. Specifically, we aimed to investigate: 1) the extent to which expectant parents demonstrated diurnal cortisol linkage in late pregnancy; and 2) whether partner’s self-reported psychological stress moderated this linkage. Based on previous research we hypothesized that: 1) within couples, partners’ cortisol would be linked; and 2) this linkage
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would be stronger among dyads who reported higher levels of psychological stress.
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2. Methods 2.1. Participants
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Data were drawn from the New Fathers and Mothers Study (NewFAMS), a large-scale,
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prospective longitudinal study on the transition to parenthood and infant development in three countries. We recruited 484 co-habitating couples in heterosexual partnerships prior to the birth
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of their first child from hospitals, prenatal classes and clinics, and parenting fairs in the United States (N = 131), United Kingdom (N = 221), and Netherlands (N = 132). Eligibility criteria for
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inclusion in the study required that couples be first-time parents, expecting delivery of a healthy singleton baby, planning to speak to their baby primarily in English (or Dutch in the Netherlands), living together with their baby, and having no history of serious mental illness or substance use. Data for the present study come from the prenatal assessment point when mothers
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were in their third trimester at approximately 36 weeks gestation. Of the 484 families recruited, 445 were seen at the prenatal time point. A total of 23 families withdrew from the study prior to the first data collection timepoint, 6 were unable to participate in data collection due to scheduling issues, and 10 were ineligible to continue due to changes in status regarding inclusionary criteria. Mothers were mostly White (90%), had an undergraduate degree or higher
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(85%), and were employed full-time (77%). Fathers were also mostly White (92%), had an undergraduate degree or higher (76%), and were employed full-time (92%). Couples’ annual household income was on average over 200% (M = 205.2; SD = 140.8) of the respective median income for the smallest geographical area for which data were available (i.e., New York state, Cambridgeshire, and the Netherlands). Thus, couples were considered to be middle to high
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income. See Table 1 for an overview of descriptive statistics for the current analytic sample. 2.2. Procedures
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When mothers were approximately 36 weeks pregnant, both parents reported a variety of
psychosocial and demographic information via online surveys, including reports of individual
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income, educational attainment, and ethnicity. Parents also completed online surveys and
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questionnaires related to their own mental health, psychological stress, and relationship functioning. Around the same time that surveys and questionnaires were completed, each parent
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also collected saliva samples in the home.
This study was reviewed and approved by the Institutional Review Board at the
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corresponding universities (New York University, Leiden University, and University of Cambridge). Written informed consent was obtained from all adult participants, in accordance with the Declaration of Helsinki. All participation was voluntary, with participants being informed prior to the study that they could remove their consent at any time.
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2.3. Measures
2.3.1. Psychological stress. A latent factor score of parent psychological stress was
created for each mother and father using scores on the Center for Epidemiological StudiesDepression (CES-D; Radloff, 1977), the State-Trait Anxiety Inventory (STAI; Spielberger et al., 1983), and the General Health Questionnaire (GHQ; Goldberg et al., 1997). Each individual
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scale demonstrated adequate internal reliability (CES-D: Mother α = .80, Father α =.83; STAI: Mother α = .77, Father α =.73; GHQ: Mother α = .74, Father α =.79). Confirmatory factor analysis without rotation fit the data well (χ2(10) = 19.44, p = .0351; RMSEA = .045 [.012, .074] p = .571, CFI = .989) and all indicators loaded significantly in the expected direction (CES-D: Mother β = .93, Father β =.94; STAI: Mother β = .56, Father β =.60; GHQ: Mother β = .68, Father β =.71; all ps < .001). Questionnaires were administered and validated in English in the
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U.S. and U.K. and administered and validated in Dutch in the Netherlands.
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2.3.2. Cortisol. Parents were instructed to collect saliva samples on 2 typical, consecutive days at 3 times on each day, yielding a potential maximum of 6 samples for each participant.
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Sample 1 was collected immediately upon waking, sample 2 was collected 30 minutes after
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sample 1, and sample 3 was collected immediately before bedtime. Saliva was collected using a 30mm cotton swab placed beneath the tongue for two minutes after which the swab was placed
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in a storage tube in their home freezer. Parents were given detailed instructions on saliva collection protocol and were instructed for each sample to not consume alcohol at least 12 hours
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before, to not eat at least 1 hour before, to not consume dairy at least 20 minutes before, and to not consume caffeine or brush teeth at least 45 minutes before sample collection. Parents were also given a saliva diary and asked to record for each sample the date and time of sampling, as well as other relevant information that may affect cortisol activity (outlined below). Lastly,
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parents were instructed to store the samples in their freezer, and were later picked up by research assistants, transported on ice, and stored in a freezer (−20°C) until shipped on dry ice for processing. Saliva samples were shipped to and assays were conducted at Universität Trier, Germany. All samples were assayed in duplicate and the average of the 2 values for each sample
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were used in all analyses. Inter- and intra-assay coefficients of variation were on average 6% and 5%, respectively. 2.4. Control covariates 2.4.1. Sociodemographic covariates. We included several socioeconomic and demographic variables in our analyses to control for any potential differences related to age, race or ethnicity, data collection site, education, employment status, and household income.
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Household income was computed as the couples’ averaged income proportional to median
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income for smallest granular area for which data were available (i.e., New York State, Cambridgeshire, and the Netherlands).
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2.4.2. Cortisol covariates. Following previous guidelines (Stalder et al., 2012; Gunnar &
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Talge, 2007; Adam & Kumari, 2009), we evaluated several covariates potentially related to cortisol. For each sample, covariates included: time of collection; whether or not the participant
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had brushed their teeth, consumed caffeine, or smoked within 45 minutes prior to saliva collection; whether or not the participant had consumed dairy within 20 minutes, alcohol within
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12 hours, or taken any medication within 12 hours prior to sample collection. For each day of collection, covariates for both parents included: time of waking, time to bed, sleep quality, and sleep duration. Furthermore, because maternal cortisol levels change drastically over the course of pregnancy, we controlled for gestational age in all analyses. Lastly, circulating cortisol in late
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pregnancy is associated with health conditions such as pre-eclampsia and gestational diabetes and thus, we included infant birth weight and gestational age at birth as peri-natal indicators of fetal and maternal health.
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2.5. Exclusions and missing data To ensure our results were not biased because participants did not adhere to the saliva collection protocol, we adopted a conservative approach by excluding morning samples that were not collected either within 15 minutes of waking (for sample 1) and/or within 15-45 minutes of waking (for sample 2). Of the 445 couples seen at the prenatal assessment, 384 (86%) had at least one saliva sample collected according to the protocol guidelines on either sampling day and
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were thus included in the analyses. Of those included in the analysis, 28% of mothers had all six
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samples, 56% had at least five samples, 80% had at least four samples, and 93% had at least
three samples. For fathers, 31% had all six samples, 56% had at least five samples, 81% had at
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least four samples, and 92% had at least three samples. To control for potential bias due to
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missing data, we fit all models using full information maximum likelihood (FIML) estimation (Enders, 2010).
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2.6. Analytic strategy
2.6.1. Calculation of cortisol variables. Natural log transformations were applied to the
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cortisol values to correct for positive skew. Cortisol values greater than +/- 3 SD after transformation were excluded from analyses. Following previous recommendations, we removed linear trends from mother’s and father’s diurnal cortisol by regressing each cortisol sample on time of day (Curran & Bauer, 2011; Helm et al., 2018). This ensures that any similarity in
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parent’s cortisol was not due merely to partners displaying similar normative trajectories across the day (i.e., diurnal decline). More specifically, each log-transformed cortisol sample was regressed on (grand-mean centered) time of sample collection and any other relevant covariate(s) significantly correlated with the respective cortisol sample. These residualized cortisol values were the main dependent and independent level 1 variables.
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2.6.2. Preliminary and main analyses. For preliminary analyses, we conducted one-way ANOVAs and repeated measures t-tests to assess between-country and within-couple differences in self-reported psychological stress and cortisol, as well as multilevel models to test within- and between-person associations between cortisol and psychological stress. For the main analyses, we used multilevel modeling to assess cortisol linkage. Because our data had three levels of nesting (samples nested within days, days nested within persons, and persons nested within
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countries), we first tested for differences in cortisol between countries and days using multilevel
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modeling and ANOVAs. Because there were no significant differences in cortisol between days or countries, we used a 2-level model in which cortisol samples were nested within persons for
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of cortisol activity (Saxbe et al., 2008; Adam, 2006).
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our main models. This strategy of combining days is a common approach to multilevel modeling
At level 1, all 6 maternal cortisol samples (log transformed and residualized, controlling
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for time of day) were entered as the dependent variable and all 6 paternal cortisol samples (log transformed and residualized, controlling for time of day) as the level 1 time-varying
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independent variable. At level 2 we entered all grand-mean centered between-person variables. We included both random intercepts and slopes in all models after confirming there was significant variance in both random effects. Cortisol linkage was conceptualized as a concurrent, non-directional, over-time process
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(Butler, 2011; Helm et al., 2018). Statistically, linkage was defined as the significant withincouple (level 1) association between mother’s and father’s 6 saliva samples. Specifically, withincouple cortisol linkage reflected the relation between mother’s cortisol at one time point with father’s cortisol at the same time point. The level 2 slope coefficient reflected average withindyad cortisol linkage for the whole sample. We centered each person’s cortisol on their own
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cortisol mean (group-mean centering). Thus, the slope coefficient for the regression of each person’s cortisol on their partner’s reflected the within-couple correlation between mother’s and father’s cortisol relative to each individual’s mean. For example, a significant positive slope coefficient means that when a father’s cortisol is higher than his average of his 6 cortisol samples, mother’s cortisol is also higher than her average of all 6 samples. To test for moderators of cortisol linkage, we evaluated cross-level interactions between
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level 2 between-person variables and the level 2 slope (i.e., linkage) coefficient. To interpret
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significant interactions, we used simple slopes analyses to evaluate effects at high and low levels of the independent variable(s), which were defined, respectively, as one SD above and one SD
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below the mean (Aiken & West, 1991). Final models were determined by systematically
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removing (or adding) covariates and comparing nested model fit using AIC/BIC criteria. Covariates not contributing significantly were removed from the final models to preserve degrees
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of freedom and model parsimony. For all models, diagnostics were conducted visually and statistically to ensure that residuals were normally distributed and that there were no points of
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significant leverage or influence based on Cook’s d. To estimate effect sizes, we calculated standardized coefficients reported as betas (β), which are in units of standard deviations. Descriptive and preliminary analyses were done using SPSS Statistics Version 22 (IBM). Final models were estimated using Mplus v.8 (Muthén and Muthén, 1998-2012).
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[INSERT TABLE 1 HERE] 3. Results
3.1. Preliminary analyses Preliminary analyses assessed initial within-person, between-person, within-couple, and between-country relations between self-reported, psychological stress, and cortisol. Results from one-way ANOVAs showed that there were no differences in maternal (F2, 380 = 1.18, p = .31) or
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paternal (F2, 379 = 2.02, p = .13) mean cortisol between countries. Additionally, there were no differences in psychological stress between countries for mothers (F2, 379 = 1.05, p = .35), but there were for fathers (F2, 362 = 14.76, p < .001). Bonferroni post-hoc tests revealed that fathers in the Netherlands reported lower levels of stress compared to the U.S. (p < .001) and U.K. (p < .001). There was no difference in reported stress between fathers in the U.S. and U.K. Results from repeated measures t-tests comparing maternal and paternal mean cortisol
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and psychological stress indicated that there was no within-couple difference in average cortisol
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between mothers and fathers (t (381) = .15, p = .88), and no difference in psychological stress (t (364) = .99, p = .32). Lastly, results from a multilevel model assessing the extent to which each
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parent’s cortisol was related to psychological stress indicated that maternal stress (b = .05, β =
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.07, SE = .03, p = .08), but not paternal stress (b = .01, β = .001, SE = .03, p = .71) was marginally related to maternal cortisol. However, neither paternal stress (b = .07, β = .05, SE =
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.05, p = .15) nor maternal stress (b = .01, β = .001, SE = .04, p = .988) was related to paternal cortisol.
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3.2. Mother-father cortisol linkage
To address our first hypothesis regarding diurnal cortisol linkage, we evaluated the level 2 slope coefficient from the level 1 regression of mother’s 6 cortisol samples on father’s 6 cortisol samples. As shown in Table 2, results revealed that there was a significant small positive
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association between maternal cortisol and paternal cortisol (b = .04, β = .07, p = .04), such that when fathers had cortisol levels higher than their average level, mothers also had higher cortisol levels than their average. This result suggests that there was evidence of within-dyad cortisol linkage for the sample overall. [INSERT TABLE 2 HERE] 3.2. Moderation of cortisol linkage
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To address our second hypothesis regarding moderation of cortisol linkage by psychological stress, we evaluated level 2 predictors of the level 2 linkage slope (i.e., cross-level interactions). As shown in Table 2, results indicated that there was a significant positive relation between maternal psychological stress and cortisol linkage (b = .13, β = .18, p < .001), but no relation between paternal stress and cortisol linkage (b = .01, β = .01, p = .81). This result indicates that within-couple cortisol linkage was dependent on maternal psychological stress. No other
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demographic or socioeconomic variables were associated with cortisol linkage.
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To interpret the interaction between maternal stress and paternal cortisol predicting
maternal cortisol, we used a simple slopes analysis and evaluated associations at low and high
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levels of maternal stress. As shown in Figure 1, at higher maternal stress there was a positive
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association between maternal and paternal cortisol (b = .12, β = .16, p < .001), but no association at lower maternal stress (b = -.03, β = .04, p = .33). This result suggests that cortisol linkage was
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present among couples with higher maternal psychological stress. To further interpret this interaction, we also tested simple slopes at high and low levels of paternal cortisol. Results
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revealed that at higher paternal cortisol there was an association between maternal psychological stress and maternal cortisol (b = .13, β = .22, p = .001). However, at lower paternal cortisol, there was no association between maternal stress and maternal cortisol (b = -.04, β = .07, p = .21). [INSERT FIGURE 1 HERE]
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4. Discussion
In the present study we investigated diurnal cortisol linkage among expectant parents and examined whether mother’s or father’s self-reported psychological stress moderated this linkage. Using data from a large, international sample of first-time expectant parents in heterosexual partnerships, we found significant positive within-couple diurnal cortisol linkage on average
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across our sample. However, cortisol linkage was stronger among dyads characterized by higher maternal psychological stress. To our knowledge, this is the first study to examine relations between cortisol linkage and psychological stress during pregnancy. Broadly, our results support the idea that interpersonal psychological and physiological stress in close relationships is interdependent and mutually influenced (Butler, 2011; Cox & Paley, 1997; Feldman, 2017; Sbarra & Hazan, 2008). Further, our findings contribute to the field’s understanding of
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interpersonal family processes during pregnancy, which may have health-related implications in
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the prenatal and postnatal periods for both parents and the developing child. 4.1. Cortisol linkage in expectant parents
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Regarding our first hypothesis, we found significant within-couple associations between
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mother’s and father’s diurnal cortisol activity. This result indicates that cortisol linkage was present on average across our sample. Importantly, because we controlled for the effect of time
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by detrending each partner’s cortisol, we can infer that linkage was not due simply to the typical pattern of cortisol decrease over the day. That is, cortisol linkage was present above and beyond
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any shared patterns of cortisol due merely to diurnal time. As such, in our analysis, cortisol linkage more likely reflects a unique process of interpersonal functioning. This finding is similar to that of several other studies that have found cortisol linkage among non-expectant romantic couples (Laws et al., 2015; Papp et al., 2013; Saxbe & Repetti, 2010). Additionally, our finding
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converges with the few studies that have evaluated cortisol linkage during pregnancy and found significant associations between partners’ cortisol at various points during pregnancy (Berg & Wynn-Edwards, 2002; Edelstein et al., 2015; Storey et al., 2000). Results from these prior studies are likely not generalizable, however, given the small sample sizes in each. Our findings
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expand upon these studies given that we had a considerably larger sample than previous research. Although the function and mechanisms are not yet understood, research suggests that physiological linkage is an interpersonal process in which individuals mutually influence one another’s physiological activity for better and for worse. Similar to other researchers, we conceptualized physiological linkage broadly as a process that includes other more specific
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interpersonal processes such as attunement, coregulation, contagion, and transmission (Butler,
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2011; Timmons et al., 2015).
During pregnancy, physiological linkage may play a particularly important role in the
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social regulation of hormones between partners and other close family members (Gettler, 2014;
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Rosenbaum & Gettler, 2018). Specifically, convergent cross-species research suggests that the related hormonal changes between partners during pregnancy support the transition to
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parenthood and may have evolved for adaptive reasons (Abraham & Feldman, 2018; Gettler, 2014). Glucocorticoids are likely key targets of linkage processes during pregnancy, given that
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cross-species research has shown that cortisol and corticosterone regulate parenting behaviors (Barrett & Fleming, 2011; Bos, 2017; Kuo et al., 2018; Saltzman & Ziegler, 2014). Several studies in human and nonhuman primates have shown that, like expectant mothers, expectant fathers also show changes in cortisol during pregnancy that are similar to their partner’s (Storey
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& Ziegler, 2016; Storey et al., 2000). Additionally, some research points to glucocorticoids playing a unique role in the interpersonal coordination of hormones during the transition to parenthood. Specifically, Ziegler and colleagues have hypothesized that the female’s change in glucocorticoids during pregnancy may operate as a mechanism of glucocorticoid signaling to stimulate similar hormonal changes in the male to prepare him for his parenting role (Storey &
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Ziegler, 2016; Ziegler et al., 2004). That is, increased glucocorticoids in mothers may facilitate the communication of certain behavioral cues between partners. In turn, these cues may elicit similar glucocorticoid increases in males. Evolutionarily this theory makes sense, as physiological linkage increases the odds of survival of the offspring by enlisting the support of a co-parent. 4.2. Moderation of cortisol linkage
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With regards to our second hypothesis, we found that cortisol linkage depended on mother’s self-
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reported psychological stress such that higher maternal stress was associated with stronger
cortisol linkage. Specifically, paternal cortisol was positively related to maternal cortisol for
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dyads characterized by higher maternal psychological stress relative to dyads with lower
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maternal psychological stress. This suggests that for higher maternal stress dyads, higher paternal cortisol may potentiate or sensitize maternal cortisol. In contrast, for dyads characterized by
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higher maternal psychological stress but lower paternal cortisol, maternal cortisol was also lower, suggesting that paternal cortisol can potentially buffer maternal cortisol.
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One interpretation of this finding is that for mothers with higher psychological stress, their physiological stress is more attuned or sensitized to their partner’s physiological stress. This finding is in line with other human studies with non-expectant romantic couples that have found cortisol linkage to be positively associated with negative psychosocial factors (Laws, 2015; Liu
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et al., 2013; Saxbe & Repetti, 2010; Schneiderman et al., 2014). In general, it may be the case that in poorer-quality and higher-stress relationships, partners more easily transmit their stress to one another. Notably, in our sample, this potential stress transmission only appears when mothers have high psychological stress and fathers also have high cortisol levels. This finding supports the idea that stress heightens physiological linkage and emotional transmission between
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partners, which is consistent with family systems theory and negative affect reciprocity (Levenson & Gottman, 1983; Cox & Paley, 1997). Our results are also consistent with the idea that pregnancy is a sensitive period of plasticity during which a mother may be more attuned to and influenced by environmental or social cues (Glynn et al., 2018). Enhanced maternal sensitivity or vigilance during pregnancy likely has evolutionary roots, preparing the mother to respond to environmental threats as a
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means of protecting her developing child (Abraham & Feldman, 2018). Indeed, some studies
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have found support for the notion that pregnant mothers are more responsive to certain social cues, such as emotional facial expressions (Pearson et al., 2009; Senese et al., 2018).
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Additionally, it may be the case that mothers are also more attuned to their own stress-related
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cues, which is to say that their physiological stress is likely coupled with their psychological stress. Indeed, we found in our preliminary analyses that there was a marginally significant
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association between maternal stress and maternal cortisol, but not paternal stress and maternal cortisol. Furthermore, in our main analysis, we also found that in couples characterized by higher
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paternal cortisol, maternal cortisol was correlated with maternal psychological stress. Thus, one possible reason why we found that maternal but not paternal stress moderated linkage is because psychological stress and cortisol are more coupled in expectant mothers, especially when fathers also have higher physiological stress, and thus is more likely to affect linkage.
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Heightened sensitivity to potentially threatening cues may be adaptive most of the time
for a pregnant mother. However, excessive sensitivity may also reflect a maladaptive or hypervigilant response. The fact that we found linkage in dyads with high, but not low maternal psychological stress may reflect a pregnant mother’s hypersensitivity to her partner’s cues. That is, pregnant mothers who report higher psychological stress may be better able to send and/or
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receive stress-related cues, and thus be more emotionally and physiologically linked with their partner. Alternatively, fathers with higher cortisol may more readily communicate their physiological stress, thereby sensitizing mothers with higher psychological stress and increasing maternal cortisol. In partial support of these ideas, some studies suggest that subtle, nonconscious cues, such as gestures, gaze, or posture, exchanged between individuals may allow for the transmission of physiological stress (e.g., Waters et al., 2014). Thus, as noted, linkage may
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function as a mechanism of stress transmission or contagion when mothers have high
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psychological stress and fathers have high physiological stress.
However, our results suggest that linkage may operate for better or worse as we found
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that low paternal cortisol was associated with low maternal cortisol among high-maternal stress
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couples. This result suggests that when partners are physiologically linked, it may allow for the opportunity for partners to buffer one another’s physiological stress. Being physiologically
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linked may be adaptive when, for instance, higher stressed mothers send signals to their lowerstressed partner to facilitate down-regulation of her physiological stress. Thus, as our findings
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suggest, cortisol linkage can operate as both a risk and protective factor. However, as our study is purely correlational, we cannot make any definitive inferences with respect to directionality or causality in our results. Further research is needed to parse the causal relations between cortisol linkage and psychological stress.
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4.3. Strengths and limitations
There are several important strengths to our analysis. First, compared to other studies on cortisol linkage during pregnancy, our sample is considerably larger and consists of participants from three different countries. Additionally, we applied strict exclusion criteria with respect to adherence to saliva collection protocol. Further, participant adherence to the saliva sampling
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cortisol was good. Notably, following previous recommendations (Curran & Bauer, 2011; Helm et al., 2018), we adopted a conservative, rigorous analytic approach that de-trends each participant’s diurnal slope. Detrending is important in our analysis because the gradual decrease of cortisol across the day is a robust, common phenomenon. Thus, in the absence of de-trending diurnal cortisol, it is plausible that linkage would be evident simply because most people exhibit the diurnal decline and thus, are likely to have correlated cortisol activity. By detrending cortisol
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(regressing out the effect of time), we can be more confident that cortisol linkage (or its absence)
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is not merely an artifact of typical cortisol functioning, but more likely attributable to
interpersonal dynamics. Lastly, we made every attempt to use the most conservative and
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stringent models to ensure our results were robust to potential confounds.
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One important limitation of our study is that we only used three cortisol samples across two days to model diurnal cortisol activity. Obtaining multiple samples across several days is
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ideal for establishing to most reliably measure one’s typical diurnal cortisol activity. Relatedly, it is important to note that glucocorticoids are regulated not only by the mother, but also the fetus
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and placenta, and thus our measure of maternal cortisol reflects the hormonal activity of all three regulating sources (Busada & Cidlowski, 2017; Morsi et al., 2018). Additionally, although our sample was drawn from three different countries, the vast majority of participants were white and had relatively high levels of income and education. Thus, the ability to generalize these
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results to other populations is constrained. More research is needed to examine how cortisol linkage during pregnancy functions in families of lower socioeconomic status, non-white, and non-Western populations. Additionally, as noted previously, our analysis is cross-sectional and thus, we are not able to infer any directionality in our results. In line with family systems theory and developmental psychobiological theory, it is important to recognize that relations between
Braren 21
interpersonal physiological and psychological stress are reciprocal and dynamic and continually interact with one another over time. Lastly, the extent to which cortisol linkage relates longitudinally to subsequent outcomes, such as postnatal parenting behavior and child development, will be an important area of future research. 4.4. Conclusions In conclusion, our results provide support for the idea that expectant mothers and fathers
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mutually influence one another physiologically, and that this activity is dependent on
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psychological factors. Specifically, during late pregnancy, expectant parents demonstrated
cortisol linkage and linkage was stronger when maternal psychological stress was high. These
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findings have implications for understanding interpersonal associations between expectant
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parents’ psychological and physiological stress, which can shape the prenatal environment and impact the developing child. Many questions remain regarding how and when interpersonal
lP
linkage functions during pregnancy, although our analysis provides some insight into these questions in finding that cortisol linkage is dependent on psychological stress. The extent to
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which expectant parents’ cortisol linkage might impact the prenatal environment and postnatal outcomes remains to be seen. Subsequent analyses with these data will examine these relations. In sum, cortisol linkage between expectant parents may be an important psychobiological pathway supporting or compromising the transition to parenthood by buffering or amplifying
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stress.
Role of Funding Sources This work was supported by grants from the ESRC (ES/L016648/1); NWO (464-13-141); and NSF (1429152). The roles of the first and second authors were also supported by the NSF
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Graduate Research Fellowship Program under Grant No. DGE1342536. REP was supported by the National Science Foundation under Grant No. 1810208. Any opinions, findings, and conclusions or recommendations expressed in this material are those of the author(s) and do not necessarily reflect the views of the National Science Foundation.
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Conflict of Interest No authors have any conflicts of interest with regards to the work presented in this manuscript.
Braren 23
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Figure 1. Maternal psychological stress moderates the association between mother’s and father’s diurnal cortisol. Cortisol linkage was present at high maternal stress (b = .12, p < .001), but not lower maternal stress (b = -.04, p = .21). At high paternal cortisol there was an association between maternal psychological stress and maternal cortisol (b = .13, p = .001). However, at low paternal cortisol, there was no association between maternal stress and maternal cortisol (b = -.03, p = .33). Error bars represent standard errors.
Braren 31 Table 1. Descriptive Statistics
N
M or %
SD
Min
Max
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Gestational age (weeks) 374 36.37 1.78 31 41 Mother employment status (% full time) 375 77 Father employment status (% full time) 374 92 Mother ethnicity (% White) 385 90 Father ethnicity (% White) 385 92 Mother Age (years) 377 32.42 3.78 22.66 43.68 Father Age (years) 364 33.90 4.36 23.00 50.07 Mother highest level of education 379 6.42 1.25 3 9 Father highest level of education 365 6.15 1.52 1 10 Household income (ratio to median income) 369 2.75 1.32 0.69 8.63 Mother psychological stress (factor score) 382 0.04 1.00 -1.58 3.44 Father psychological stress (factor score) 365 0.07 1.02 -1.42 3.77 Mother cortisol sample 1 Day 1 (μg/dl) 302 0.47 0.17 0.15 1.25 Mother cortisol sample 2 Day 1 (μg/dl) 278 0.63 0.20 0.18 1.28 Mother cortisol sample 3 Day 1 (μg/dl) 377 0.17 0.07 0.01 0.49 Mother cortisol sample 1 Day 2 (μg/dl) 327 0.48 0.18 0.12 1.49 Mother cortisol sample 2 Day 2 (μg/dl) 314 0.63 0.23 0.18 1.70 Mother cortisol sample 3 Day 2 (μg/dl) 375 0.18 0.11 0.01 1.09 Father cortisol sample 1 Day 1(μg/dl) 298 0.36 0.18 0.06 1.22 Father cortisol sample 2 Day 1 (μg/dl) 280 0.46 0.20 0.05 1.18 Father cortisol sample 3 Day 1 (μg/dl) 379 0.06 0.08 0.01 0.64 Father cortisol sample 1 Day 2 (μg/dl) 328 0.37 0.16 0.05 0.88 Father cortisol sample 2 Day 2 (μg/dl) 308 0.47 0.20 0.01 1.13 Father cortisol sample 3 Day 2 (μg/dl) 369 0.06 0.08 0.01 0.71 Note: Household income was computed as the couples’ averaged income proportional to median income for smallest area for which data were available (i.e., New York State, Cambridgeshire, and the Netherlands).
Braren 32 Table 2. Multilevel model predicting diurnal maternal cortisol Maternal Cortisol S.E.
p
.039
.07
.019
.037
.009 .133 -.025 -.038 -.003
.01 .18 .08 .04 .01
.039 .033 .016 .047 .011
.813 <.001 .106 .416 .770
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β
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Level 1 Father cortisol (linkage coefficient) Cross-level interactions Father psychological stress (level 2) × Father cortisol (level 1) Mother psychological stress (level 2) × Father cortisol (level 1) Mother education (level 2) × Father cortisol (level 1) Household income (level 2) × Father cortisol (level 1) Gestational age (level 2) × Father cortisol (level 1) Note: S.E. = standard error; Bold statistics indicate p <0.01
b