Maternal sensitivity moderates the impact of prenatal anxiety disorder on infant responses to the still-face procedure

Infant Behavior & Development 33 (2010) 453–462

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Infant Behavior and Development

Maternal sensitivity moderates the impact of prenatal anxiety disorder on infant responses to the still-face procedure Kerry-Ann Grant a,b,∗ , Catherine McMahon a , Nicole Reilly b , Marie-Paule Austin b,c a b c

Centre for Emotional Health, Department of Psychology, Macquarie University, North Ryde, NSW 2109, Australia Black Dog Institute, Hospital Road, Randwick, NSW 2031, Australia School of Psychiatry, University of New South Wales, Sydney, NSW 2052, Australia

a r t i c l e

i n f o

Article history: Received 22 December 2009 Received in revised form 13 April 2010 Accepted 17 May 2010 Keywords: Pregnancy Anxiety Maternal sensitivity Still-face procedure

a b s t r a c t Animal studies have demonstrated the interactive effects of prenatal stress exposure and postnatal rearing style on offspring capacity to manage stress. However, little is known about how parenting quality impacts the association between maternal prenatal anxiety and stress reactivity in human infants. This prospective study examined the impact of prenatal anxiety disorder and maternal caregiving sensitivity on infants’ responses to a standardised interactive stressor (still-face procedure). Eighty-four women completed a clinical interview during pregnancy to assess anxiety symptoms meeting DSM-IV diagnostic criteria. At infant age 7 months, maternal sensitivity to infant distress and infant negative affect were observed and coded during the still-face procedure. Maternal postnatal (concurrent) anxiety and depression were also assessed at this time. Results indicated a negative association between maternal sensitivity to infant distress and infant negative affect responses to the still-face procedure. An unexpected finding was a positive association between parity and infant reactivity. The main effect for sensitivity was qualified by a significant interaction, p < .05, suggesting that the impact of sensitivity was particularly marked among infants of women who experienced an anxiety disorder during pregnancy. This finding is consistent with a cumulative risk model suggesting that maternal prenatal anxiety and quality of maternal care act in concert to shape infant outcomes. © 2010 Elsevier Inc. All rights reserved.

1. Introduction The ability to regulate distress and negative emotions in infancy is considered one of the most important predictors of socio-emotional adjustment later in life (Sroufe, 1996). One area of research that seeks to understand the earliest origins of regulation examines the prospective impact of prenatal exposure to maternal stress on offspring neurodevelopment and behaviour. Recent studies have documented links between anxiety in pregnancy and changes in the regulation of behavioural and emotional reactivity that can be observed as early as during the fetal period (for reviews, see Austin, Hadzi-Pavlovic, Leader, Saint, & Parker, 2005; Van den Bergh, Mulder, Mennes, & Glover, 2005). Prenatal anxiety effects during infancy include poor state regulation (Brouwers, van Baar, & Pop, 2001; Field et al., 2004; Rieger et al., 2004), difficult temperament (e.g., Austin, Hadzi-Pavlovic, et al., 2005; Huizink, De Medina, Mulder, Visser, & Buitelaar, 2002; Werner et al., 2007), and heightened reactivity in response to novelty or challenge (Davis et al., 2004; Mohler, Parzer, Brunner, Wiebel, & Resch, 2006).

∗ Corresponding author at: Department of Psychology, Macquarie University, North Ryde, NSW 2109, Australia. Tel.: +61 2 9850 6750; fax: +61 2 9850 8062. E-mail address: [email protected] (K.-A. Grant). 0163-6383/$ – see front matter © 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.infbeh.2010.05.001

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Further recent findings suggest longer term effects, such as behaviour problems at 4 (O’Connor, Heron, Glover, & the ALSPAC Study Team, 2002; O’Connor, Heron, Golding, Beveridge, & Glover, 2002) and 9 years (Van den Bergh & Marcoen, 2004), and problems with regulation at the cognitive level during adolescence (Van den Bergh, Mennes, et al., 2005). These outcomes are consistent with the notion of prenatal programming, the process by which fetal development is altered due to changes in the uterine environment (for reviews, see Huizink, Mulder, & Buitelaar, 2004; Talge, Neal, & Glover, 2007). Interestingly, however, there is evidence from animal studies suggesting that the period of sensitivity during which programming may occur extends beyond the prenatal period. Specifically, rearing quality has been shown to be an important characteristic of the postnatal environment that can have long-term organisational effects on offspring behaviour. Animal studies have shown that ordinary variations in maternal care can modify both behavioural and biological outcomes associated with exposure to prenatal stress (Francis, Szegda, Campbell, Martin, & Insel, 2003; Wakshlak & Marta, 1990). In the human literature, the idea that sensitive, responsive care supports the development of infant self-regulation is a central tenet of attachment theory. Maternal sensitivity requires that mothers accurately interpret and contingently respond to their infant’s cues, provide appropriate stimulation, and moderate levels of infant arousal (Ainsworth, Blehar, Waters, & Wall, 1978; Bowlby, 1969). Through interactions with caregivers, infants learn strategies for controlling and managing behaviour and emotions that, in turn, contribute to adaptive socio-emotional functioning, particularly the development of secure attachment relationships (Ainsworth et al., 1978) and the achievement of autonomous and self-regulated behaviour (Kopp, 1982; Sroufe, 1996). While sensitive caregiving in general is important for the development of self-regulation, there is evidence to suggest that sensitivity to infant distress is a key and unique factor in children’s early social-emotional adjustment (Del Carmen, Pedersen, Huffman, & Bryan, 1993; Leerkes, Blankson, & O’Brien, 2009; McElwain & Booth-LaForce, 2006). Indeed, it has been proposed that sensitivity in response to fearful, anxious or distressed infant behaviours may be a better predictor of attachment security than sensitivity displayed in non-stressful contexts (Thompson, 1997). Although there is extensive empirical support for the role of sensitive caregiving as an external regulator of behavioural and physiological arousal during the first year of life (for reviews, see Calkins, 1994; Crockenberg & Leerkes, 2000), the extent to which quality of care buffers or accentuates the effects of exposure to prenatal anxiety has only recently begun to be explored. In one study, Bergman, Sarkar, Glover, and O’Connor (2008) found that attachment classification (insecure/resistant) moderated the effect of prenatal stress on laboratory-assessed fearfulness in children aged 17 months, after controlling for postnatal stress and other social and demographic covariates. However, quality of caregiving was inferred from the child’s attachment classification, stressful life events rather than anxiety were assessed, and life events during pregnancy were assessed retrospectively in the postnatal period. In another prospective study of forty-seven women, Kaplan, Evans, and Monk (2008) reported that maternal sensitivity, but not maternal prenatal psychiatric status, predicted heart rate variability and responsiveness in 4-month-old infants. Interestingly, maternal sensitivity was shown to moderate the impact of prenatal psychiatric diagnosis on infants’ resting cortisol levels. The measures, however, were not taken in response to a stressor or stimulus, and thus cannot inform how maternal sensitivity interacts with antenatal psychiatric status to influence infant stress reactivity. The present study aimed to extend this emerging research by examining the separate and combined influences of maternal prenatal anxiety disorder and postnatal caregiving sensitivity on infants’ capacity to manage distress. A modified version of the still-face procedure was employed for the observation of mother–infant interaction because it provides a developmentally appropriate context for assessing dyadic distress management under controlled laboratory conditions (for a recent review, see Mesman, van Ijzendoorn, & Bakermans-Kranenburg, 2009). We predicted that maternal sensitivity to infant distress would moderate the relationship between prenatal anxiety diagnosis and infant outcomes such that infants whose mothers were anxious during pregnancy, and who were also insensitive caregivers would display heightened negative reactivity in response to challenge. 2. Method 2.1. Participants One hundred and forty-nine predominantly middle-class, Caucasian women were recruited during their first prenatal health care visit at a large obstetric hospital in Sydney, Australia. English-speaking women with singleton, uncomplicated pregnancies, and with no known substance/alcohol abuse problems or chronic psychiatric disorders were eligible to participate. Further screening based on an antenatal risk questionnaire (ANRQ: Austin, 2003) yielded a sample in which women at highest risk for perinatal anxiety disorder was over-represented. The ANRQ is routinely administered to all women during their first prenatal clinic visit and asks about psychosocial risk factors known to be associated with the onset of perinatal distress, including recent life stresses, social support, tendency to worry, and self-esteem. The ANRQ is a short form of the Pregnancy Risk Questionnaire (PRQ: Austin, Hadzi-Pavlovic, et al., 2005), an antenatal screening tool validated against the Composite International Diagnostic Interview (CIDI: World Health Organisation, 1997) for the identification of women at risk for postnatal mood disorders. Of the 149 women initially recruited, 56.4% (n = 84) were identified as “high risk” using a cut-off score of 23 on the ANRQ. Participants were subsequently lost to analyses due to obstetric complications (n = 17), scheduling difficulties (n = 10), relocation (n = 9), illness (n = 2), and inability to contact (n = 7). Additional cases were removed due to technical (camera failure, n = 4) and other reasons, including speaking in a non-English language (n = 3), failure to complete all question-

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naires (n = 11), infants too distressed to participate in the still-face procedure (n = 2). We report data from the remaining 84 mother–infant dyads with complete data. Women lost to the study did not differ from women retained on prenatal anxiety diagnosis, depression symptoms, maternal demographic variables or infant characteristics, all p-values > .10. 2.2. Procedures summary Diagnostic clinical interviews were administered between 35 and 39 weeks gestation (M = 36.95 weeks, SD = .76 weeks) to assess anxiety symptoms over the last 6 months of pregnancy meeting DSM-IV criteria. Self-reported depression symptoms, demographic data and details of substance use during pregnancy were also assessed at this time. Data regarding birth outcomes were obtained from hospital medical records. The follow-up at child age 7 months comprised (i) completion of self-report inventories for the assessment of maternal postnatal (concurrent) symptoms of anxiety and depression, and (ii) a 1 h laboratory session during which mother–infant dyads were exposed to an interactive stress paradigm (the still-face procedure). 2.2.1. Still-face procedure The still-face procedure is an interactive social stressor that has been extensively used to evaluate regulatory capacities of infants in the context of variations in maternal behaviour (e.g., Haley & Stansbury, 2003; Kogan & Carter, 1996). The standard procedure comprises a sequence of three, 2-min episodes: a free–play interaction, a still-face episode, and a resumption of play episode (Weinberg & Tronick, 1994). Because we were interested in maternal and infant capacity to manage distress, we sought to increase the stressful impact of the procedure by including a 1-min period during which the mother left the testing room. This period of absence followed the initial free–play interaction. Infants were seated in a high-chair facing their mother at eye-level, 1 m away. For the play sequences, mothers were instructed to play with their infant as they would usually do at home. During the maternal absence phase, they were to leave the room for 1 min, closing the door behind them. A researcher concealed behind a partition remained in the room with the infant. For the still-face episode, mothers were instructed to adopt and maintain a neutral facial expression and not to touch or respond to their infant. The beginning and end of each episode were prompted by the experimenter. The entire procedure was videotaped using a single wide-angle lens camera concealed behind a partition. A mirror placed adjacent to the mother-infant dyad facilitated recording the mother’s facial expression which was later coded to ensure that instructions to adopt and maintain a “still-face” were followed. Mothers generally followed instructions, maintaining a neutral facial expression and refraining from touching their infant for the duration of the episode. 2.3. Maternal anxiety and mood measures 2.3.1. Prenatal anxiety The Mini-Plus International Neuropsychiatric Interview version 5.0.0 (MINI: Sheehan et al., 1998) was administered by trained personnel to assess anxiety symptoms over the last 6 months of pregnancy meeting DSM-IV criteria. It is a short, structured, diagnostic interview containing questions addressing the intensity, frequency, and duration of specific symptoms, and the degree of distress or impairment associated with them. Participants were assessed using the panic disorder, agoraphobia, social phobia, post-traumatic stress disorder, and generalised anxiety disorder components of the MINI. The MINI is reliable and valid (Lecrubier et al., 1997; Sheehan et al., 1997) and demonstrates good concordance with the Structured Clinical Interview for DSM diagnoses (SCID: Spitzer, Williams, Gibbon, & First, 1990) and the Composite International Diagnostic Interview for ICD-10 (CIDI: World Health Organisation, 1990). 2.3.2. Pre- and postnatal depression The 10-item Edinburgh Postnatal Depression Scale (EPDS: Cox, Holden, & Sagovsky, 1987), also validated for use during pregnancy (Murray & Cox, 1990) was completed both pre- and postnatally. The scale demonstrates good reliability with Cronbach’s alphas reported at .86 and .87 for the pre- and postnatal assessments, respectively. 2.3.3. Maternal postnatal (concurrent) anxiety The state scale of the Spielberger State-Trait Anxiety Inventory (STAI: Spielberger, Gorusch, & Lushene, 1987) was administered at the time of follow-up to assess concurrent symptoms of maternal anxiety. The STAI is a reliable and valid self-report measure that has been used with both clinical and non-clinical populations (Spielberger et al., 1987), and with childbearing women (Austin, Leader, & Reilly, 2005; Brouwers et al., 2001; Grant, McMahon, & Austin, 2008; Van den Bergh & Marcoen, 2004). The state anxiety scale consists of 20 items that evaluate current feelings of tension, anxiety, and nervousness. Internal consistency in the present study was high (Cronbach’s alpha = .95).

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2.4. Behaviour rating/coding Videotapes of the still-face procedure were rated by a trained coder who was blind to maternal anxiety status and the study hypotheses. A second coder rated 20% of cases (randomly selected) to establish reliability. Inter-rater reliability was assessed using intra-class correlations. 2.4.1. Infant negative reactivity Infant negative reactivity during each of the still-face episodes was coded using the vocalisations component of BraungartRieker, Garwood, Powers, and Notaro’s (1998) infant negative affect scale. The scale measures intensity of negative vocalisations on a four-point scale: 0 (no negative vocalisations), 1 (mild fuss), 2 (crying), and 3 (screaming). Each episode was divided into 5-s intervals and the highest intensity of negative affect was rated for each interval. Average negative intensity scores were created for each episode (sum of intensity ratings/number of completed 5-s intervals). Inter-rater reliability was based on average negative intensity ratings for each episode and intra-class correlations ranged from .85 to .98. 2.4.2. Maternal caregiving sensitivity The Global Rating Scales of Mother–Infant Interaction (Murray, Fiori-Cowley, Hooper, & Cooper, 1996) were used to rate five dimensions of maternal sensitivity: (i) Warmth, or the expression of love and affection. A mother who is warm makes many positive comments about her infant (e.g., “what a nice, big smile”), her face and voice express affection, and she may hold or touch her infant in a supporting, caressing way. (ii) Acceptance of the infant’s behaviour and experience. An accepting mother never criticises, ignores, dampens, or makes substitutions for her infant’s expressions or behaviour. (iii) Responsiveness to the infant’s cues. A responsive mother picks up and responds to all her infant’s signals, even the very small ones. This dimension includes both appropriate and inappropriate responses. (iv) The dimension of Sensitivity considers the impact of the mother’s responses on her infant’s behaviour; how she empathises and identifies with her infant and understands (correctly) what response is needed at a particular moment. (v) The Non-Demanding Behaviour scale assesses the extent to which mother does not demand behaviours that conform to mother’s model of a “good infant”. For example, she never suggests that her infant smile, unless in a playful manner and his or her state permits it. Scoring is on a five-point scale (1–5) with scores close to 5 indicating the most optimal maternal behaviours. Following the manual, the individual dimension scores are summed then divided by five to arrive at a mean sensitivity index for each episode (individual dimension scores are given equal weight in the calculation of this score). A mother who scores close to 5 responds to her infant’s cues in a way that is appropriately adjusted to her infant’s behaviour and is warm and accepting of her infant’s experience. Internal consistency of the scales was high (Cronbach’s alpha = .83), and intra-class correlations ranged from .80 to .97 across episodes and dimensions. 3. Results 3.1. Descriptive analyses 3.1.1. Study sample Women were classified as either anxious (DX) or non-anxious controls (NC) on the basis of their prenatal anxiety diagnosis. Anxious (n = 16) women met DSM-IV diagnostic criteria for at least one anxiety disorder during the last 6 months of pregnancy. Controls (n = 68) did not meet diagnostic criteria during this 6-month period. Maternal demographic characteristics are shown separately for each group of women in Table 1. Infants were 46 boys and 38 girls (M = 7.04 months, SD = .54 months). All infants were born at term (37–42 weeks). Infant demographic and clinical characteristics are summarised in Table 2. Independent samples t-tests and Chi-square analyses did not reveal any differences between prenatally anxious and non-anxious women on any maternal demographic or substance use variable, or on any obstetric or infant characteristic, all p-values > .10. 3.1.2. Infants’ responses to the still-face procedure A repeated measures analysis of variance (ANOVA) was computed entering mean infant negative affect for each still-face episode (episodes 1–4) as the within-subjects factor and maternal prenatal anxiety diagnosis (NC, DX) as the between subjects factor. The episode × prenatal anxiety diagnosis interaction was non-significant, p > .10, however, a significant quadratic trend for episode was obtained, F(1, 81) = 42.60, p < .001. Both groups of infants reacted to the procedure with a significant increase in negative affect from episode 1 (initial play) to episode 3 (still-face), p < .001, followed by a significant decrease in negative affect during resumption of play, p < .005. Infants’ reactions to the stressful procedure were negatively and significantly correlated with their subsequent recovery, r = −.43, p < .001. 3.1.3. Maternal sensitivity and associations with prenatal anxiety and infants’ responses to the still-face procedure Descriptive data for the maternal sensitivity measure are shown in Table 3. Mean sensitivity for the group overall was close to four on the five-point scale for both episode 1 (initial play): M = 3.71, SD = .61, range = 2.40–4.80, and episode 4 (resumption of play): M = 3.68, SD = .63, range = 1.80–4.80. There were no significant differences in maternal sensitivity between the NC

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Table 1 Maternal characteristics by prenatal diagnostic group. Variables

Sample (n = 84) M

Demographics Age (years) Education level (n, %) High school Tertiary Ethnicity (n, %) Caucasian Asian Partner (n, %) Parity (n, %) One child Two children Three children Prenatal substance use Cigarettes per day Standard drinks per day

Anxious (n = 16) SD

M

Controls (n = 68) SD

M

SD

31.94

4.25

31.25

4.57

32.10

4.19

n = 12 n = 72

14.3% 85.7%

n=3 n=3

18.8% 81.2%

n=9 n = 59

13.2% 86.8%

n = 79 n=5 n = 77

94.0% 6.0% 91.6%

n = 14 n=2 n = 14

87.5% 12.5% 87.5%

n = 65 n=3 n = 63

95.6% 4.4% 92.6%

n = 61 n=9 n=4

72.6% 22.6% 4.8%

n=8 n=7 n=1

50.0% 43.8% 6.2%

n = 53 n = 12 n=3

77.9% 17.6% 4.5%

.51 .11

2.65 .26

.94 .16

3.75 .44

.40 .09

2.35 .20

Table 2 Infant characteristics by prenatal diagnostic group. Variables

Obstetric Mode of delivery (n, %) Normal vaginal Caesarean section Instrumental APGAR score (5 min) GA at birth (weeks) Birth weight (kg) Birth length (cm) Head circumference (cm) Postnatal follow-up Age (weeks) Sex (n, %) Male Female Breastfed (n, %)

Sample (n = 84)

Anxious (n = 16)

Controls (n = 68)

M

SD

M

SD

M

SD

n = 55 n = 19 n = 10 9.06 39.94 3.45 51.21 34.54

65.5% 22.6% 11.9% 0.57 1.16 0.48 3.01 1.49

n = 12 n=3 n=1 9.25 39.77 3.36 50.06 34.56

75.0% 18.7% 6.3% 0.45 1.13 0.34 2.68 1.14

n = 43 n = 16 n=9 9.01 39.98 3.47 51.49 34.54

63.2% 23.5% 13.3% 0.59 1.17 0.51 3.04 1.57

32.27

2.62

32.31

2.62

32.26

2.64

n = 46 n = 38 n = 50

54.8% 45.2% 59.5%

n=7 n=9 n=8

43.8% 56.2% 50.0%

n = 39 n = 29 n = 42

57.4% 42.6% 61.8%

and DX groups across episodes, p-values > .05. Sensitivity across play episodes indicated that maternal sensitivity during initial play was moderately correlated with sensitivity to infant distress (resumption of play) for the group overall, r = .39, p < .001. Pearson correlation revealed a moderate, negative association between maternal sensitivity observed during resumption of play (episode 4) and infant reactivity (change in negative affect from episode 1 to episode 3), r = −.38, p < .05. All other associations between maternal sensitivity and infant responses to the still-face procedure were non-significant, p-values > .10.

Table 3 Maternal sensitivity subscales and total scores. Variables

Episode 1 M

Episode 4 SD

M

SD

Overall sensitivity

3.71

.61

3.67

.63

Subscale scores Warm Accepting Responsive Sensitive responding Non-demanding

3.61 3.71 3.92 3.07 4.26

.60 .89 .70 1.02 .66

3.37 3.57 4.15 3.00 4.24

.64 .98 .64 .99 .70

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Table 4 Maternal symptom measures of anxiety and depression. Variables

M Prenatal Depression – EPDS Postnatal State anxiety – STAI Depression – EPDS

Anxiousa (n = 16)

Sample (n = 84) SD

M

Controls (n = 68) SD

M

5.71

4.74

11.13

5.93

4.44

35.95 5.63

10.92 4.69

42.31 8.25

12.66 6.51

34.46 5.01

SD 3.36** 9.99** 3.96 ns

a Generalised anxiety disorder (GAD) only n = 8, GAD and agoraphobia n = 1, GAD and social phobia n = 1, GAD and panic disorder n = 1, GAD and posttraumatic stress disorder (PTSD) n = 1, agoraphobia only n = 1, social phobia only n = 1, and panic disorder only n = 2. ** p < .01.

Table 5 Final regression models for the prediction of infant reactivity and recovery. Variable

Reactivity B

Covariates Parity Prenatal depression symptoms Postnatal depression symptoms Postnatal state anxiety Reactivity

Recovery SE

ˇ

B

SE

ˇ

.60 .03 −.02 .00

.15 .03 .03 .01

.41** .19 −.13 .03

−.11 .02 −.01 .00 .51

.11 .02 .02 .01 .08

−.11 .17 −.09 −.07 .70**

Study variables Sensitivity to distress Prenatal anxiety DX

−.40 −.18

.14 .25

−.31** −.09

.44 .01

.10 .17

.46** .00

Interactions Prenatal anxiety DX × sensitivity to distress

−.76

.34

−.24*

−.23

.23

* **

−.10

p < .05. p < .01.

3.2. Covariates 3.2.1. Confounding symptomatology Descriptive statistics for symptoms of prenatal depression and postnatal (concurrent) anxiety and depression are reported separately for the anxious and control groups in Table 4. Women who met diagnostic criteria for anxiety in pregnancy were significantly more symptomatic than controls on all three measures, p-values < .05. Correlations revealed significant associations between prenatal anxiety diagnosis and postnatal anxiety symptomatology, r = .29, p < .01, and between preand postnatal symptoms of depression, r = .55, p < .01. Prenatal depression symptoms were also positively related to postnatal anxiety symptoms, r = .63, p < .001, and postnatal symptom measures of anxiety and depression were strongly related, r = .81, p < .001. Prenatal depression and postnatal (concurrent) symptoms of anxiety and depression were included as covariates in subsequent analyses. 3.2.2. Demographic and obstetric covariates Further correlations were conducted to examine associations among maternal demographic characteristics (age, ethnicity, education, partnership status, parity), infant characteristics (gender, age at follow-up, breastfeeding status), obstetric variables (mode of delivery, gestational age at birth, birth weight, length, and head circumference), and the independent and dependent variables. The only correlation to reach significance was the association between parity and infant reactivity to the still-face procedure, r = .26, p = .02. Parity was therefore retained in subsequent analyses. 3.3. Hypothesis testing Hierarchical multiple regression analyses were conducted to test the combined influences of maternal prenatal anxiety and maternal caregiving sensitivity on infants’ responses to the still-face procedure. In the first analysis, infant reactivity was the dependent variable. In the second, infant recovery from the stressor was the outcome variable of interest. Predictor variables were centered at the mean to reduce multicollinearity. The first step of each regression included the covariates (prenatal depression, postnatal anxiety and depression, parity). The second step included the predictor variables (prenatal anxiety diagnosis, maternal sensitivity to distress). The interaction term (prenatal anxiety × sensitivity to distress) was entered in the final step. The interaction term was created as a product of the centered predictor variables. Results of the analyses are presented in Table 5.

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Fig. 1. Prenatal anxiety diagnosis, maternal sensitivity to distress, and infant reactivity.

3.3.1. Infant reactivity The final model predicting infant reactivity to the still-face procedure was significant, F(7, 77) = 5.66, p < .001, accounting for 36.2% of the variance. The model indicated significant main effects for parity and maternal sensitivity to distress. While the main effect for parity indicated a positive association between number of children in the family and infant reactivity, b = .60, p < .001, the main effect for sensitivity to distress indicated a negative association between sensitivity to distress and infant reactivity, b = −.40, p < .01. Fig. 1 shows that maternal sensitivity to distress was associated with lower reactivity in infants of both NC, b = −.40, p < .01, and DX, b = −1.16, p < .001, women. However, this outcome was particularly marked among infants of women who experienced an anxiety disorder during pregnancy. This interaction effect was statistically significant, b = −.76, p < .05. 3.3.2. Infant recovery from the still-face procedure The final model predicting infant recovery from the still-face procedure was significant, F(8, 77) = 7.90, p < .001, explaining 47.8% of the variance. A significant main effect for reactivity indicated a positive association between infant reaction to the still-face procedure and their subsequent recovery, b = .51, p < .001. The results also indicated, that with reactivity taken into account, higher maternal sensitivity predicted a more complete recovery from the procedure, b = .44, p < .001. No other main effects or interactions reached significance, p-values > .05. 3.3.3. Post-hoc analysis Pearson correlations were conducted to determine whether the significant main effect for parity in relation to infant reactivity could be explained by maternal caregiving behaviour. Infant reactivity was not associated with either sensitivity during initial play, r = .17, p > .10, nor with sensitivity to distress, r = .09, p > .10. 4. Discussion Maternal sensitivity to distress emerged as a significant independent predictor of infants’ responses to the still-face procedure. Maternal sensitivity was linked to reduced infant reactivity following the stressful episodes and a better recovery following stressor offset. Moreover, the impact of sensitivity appeared to be most marked in the group where mothers had experienced clinically significant anxiety during pregnancy. Interestingly, parity also emerged as a significant factor influencing infant reactivity. Specifically, larger family size was associated with increased negative affect in response to the still-face procedure. This study extends the research on prenatal stress in humans and has important theoretical, methodological and clinical implications. Our results are consistent with the existing literature demonstrating that sensitivity to infant distress plays an important role in the modulation of negative affect and arousal during the first year of life (Del Carmen et al., 1993; Leerkes et al., 2009; McElwain & Booth-LaForce, 2006). Because the infant’s capacity for regulation of negative emotional states is very limited during the first year of life, external regulation through caregivers’ sensitive responding to distress or to bids for safety and protection may protect infants from excessive stress. Indeed, our results show that regardless of prenatal anxiety diagnosis, sensitive mothers appeared to be most successful in reducing their infants’ discomfort or distress. On the other hand, the least sensitive mothers had the most reactive infants suggesting that these women may have been unable to provide the external regulation needed to support their infant’s developing capacity to regulate state, behaviour and emotions. It is also possible that insensitive caregiving itself constitutes a source of stress and discomfort for infants, eliciting negative behaviours and heightened reactivity. Establishing the direction of causal links between maternal care and dysregulated infant behaviours is a major challenge for researchers in this field. For example, it is likely that there are some infants who demonstrate difficulties with regulation from early in life, and whose challenging behaviour in turn, constrains the quality of maternal care (Murray, Fiori-Cowley, et al., 1996; Murray, Stanley, Hooper, King, & Fiori-Cowley, 1996; van den Boom, 1994).

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Interestingly, prenatal anxiety diagnosis alone did not predict infant outcomes in the present study. Rather, it was the interaction between prenatal anxiety and maternal sensitivity to distress that was significant in predicting infant reactivity. Although it is likely that our small clinical group limited our statistical power to find a main effect for prenatal anxiety diagnosis, the significant interaction is consistent with the growing body of evidence suggesting that it is the combination of risk factors, rather than the presence of a single risk factor that explains numerous adverse outcomes in child development (e.g., Appleyard, Egeland, Dulmen, & Sroufe, 2005; Goodman & Gotlib, 1999; McMahon, Barnett, Kowalenko, & Tennant, 2006). Although further research is needed to elucidate the underlying mechanism, it could be speculated that poor quality care may have exacerbated a genetic predisposition, and/or a physiologically mediated vulnerability such as the one proposed by the fetal programming hypothesis (for reviews, see Huizink et al., 2004; Talge et al., 2007). A secondary finding of the study is that parity emerged as a significant, independent predictor of infant reactivity to the still-face procedure. Specifically, larger family size was associated with heightened reactivity in response to the stressor. Although it could be speculated that this effect was mediated by maternal behaviour, our post-hoc analysis did not support this. Nulliparous and multiparous women did not differ in observed sensitivity to infant distress. Parity differences in the quality of mother-infant interaction are not frequently reported in studies of stress and anxiety in pregnancy, however, this positive association suggests that family size may be a potentially important variable when studying reactivity in infancy. The present results have both conceptual and clinical implications. From a theoretical perspective, the data clearly demonstrate that a comprehensive model of early-life programming must be able to account not only for prenatal effects, but also for the effects of parenting quality and other potential moderating variables in the postnatal environment. Such a model will facilitate the early identification of potential risk and protective factors as well as the development of appropriately targeted interventions. Our results provide evidence for continued efforts to screen for psychological disturbances in pregnancy and for increased support for anxious women prior to birth (Austin et al., 2008). They also suggest, however, that addressing maternal psychopathology alone may not be sufficient and that interventions focused on improving motherinfant interaction are also required to ensure the best possible outcomes for infants (Forman et al., 2007; Murray, Cooper, Wilson, & Romaniuk, 2003). Interventions aimed at enhancing sensitivity have previously been shown to be successful in reducing infant irritability, with benefits sustained through toddlerhood (e.g., van den Boom, 1994; van den Boom, 1995). The current results also indicate that parity may be an important consideration in setting the parameters of both research and intervention programs. There are several limitations to the present study. Firstly, the extent to which our findings apply to women from different socio-economic backgrounds is unknown. Given that our middle-class, well-educated sample would have been largely buffered from additional risk factors associated with psychosocial adversity (e.g., teenage parenthood, unemployment, financial strain, housing problems), it is likely that our results are conservative. Countering this concern, however, the use of a low risk sample permitted a focus on maternal anxiety without the confounding influence of additional risk factors. Nonetheless, this may have constrained the range in maternal sensitivity, as lower maternal sensitivity is frequently reported in less socio-economically buffered samples (Murray, Fiori-Cowley, et al., 1996; Murray, Stanley, et al., 1996; van den Boom, 1994) Next, although we attempted to over-sample for women at risk for prenatal anxiety, our clinical group was small and this may have limited our statistical power to find a main effect for prenatal anxiety diagnosis. The group was also relatively homogenous with respect to diagnosis. 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