Evidence-based intervention for young children born premature: Preliminary evidence for associated changes in physiological regulation

Abstract

The current study examined whether changes in maternal behaviors following an evidence-based treatment—Parent–Child Interaction Therapy (PCIT)—was associated with improvements in cardiac vagal regulation in young children born premature. Participants included 28 young children (mean age = 37.79 months) that were born premature and presented with elevated externalizing behavior problems. To assess cardiac vagal regulation, resting measures of respiratory sinus arrhythmia (RSA) and RSA change (withdrawal or suppression) to a clean-up task were derived pre and post-treatment. Results indicated that an increase in behaviors mothers are taught to use during treatment (i.e., do skills—praise, reflection, and behavioral descriptions) was associated with an improvement in children's post-treatment RSA suppression levels. The current study illustrates the important role of caregiver behavior in promoting physiological regulation in children born premature.

Introduction

Broadly speaking, self-regulation refers to an individual's efforts to alter his or her inner states or responses (Baumeister & Vohs, 2004). Recent work in both developmental and clinical psychology has noted a significant association between child self-regulation skills and adaptive functioning across a range of domains, such as behavioral, social, and academic (Baumeister and Vohs, 2004, Calkins and Fox, 2002, Graziano et al., 2007b, Keenan, 2000, Shaw et al., 1997). Self-regulation is a multi-level construct with control efforts that rely on physiological, attentional, emotional, and behavioral processes. These processes are hierarchically organized and become more sophisticated and integrated throughout development (Calkins, 2007). For example, recent psychophysiological research has highlighted the maturation of the parasympathetic branch of the autonomic nervous system as a critical factor in supporting the development of these increasingly sophisticated biobehavioral regulation processes (Calkins, 2007, Porges, 2007). Specifically, cardiac vagal tone—an index of the parasympathetic influence on the heart—has emerged as a psychophysiological marker for many aspects of self-regulation (e.g., emotion regulation) in both children and adults (Beauchaine, 2001, Calkins, 1997, Calkins, 2007, Grossman and Taylor, 2007, Porges, 1995, Porges, 2003, Porges, 2007).

Assessing the functional output of the vagal pathways on the heart is accomplished non-invasively by quantifying the amplitude of respiratory sinus arrhythmia (RSA), a component of heart rate variability. Research has indicated that RSA, under controlled respiratory conditions, is uninfluenced by variations in sympathetic activity, and provides a sensitive index of cardiac vagal tone, even when alterations in parasympathetic activity are small (Grossman, Stemmler, & Meinhardt, 1990). Of particular interest to researchers studying self-regulation is measurement of vagal regulation of the heart when the organism is challenged. Vagal regulation refers to a withdrawal in RSA during a challenging state (i.e., vagal tone decreases from baseline to challenging task, reflected by a positive vagal regulation score) or to an augmentation in RSA (i.e., vagal tone increases from baseline to challenging task, reflected by a negative vagal regulation score). According to polyvagal theory, successful vagal regulation is marked by RSA withdrawal, which is thought to facilitate a child's ability to cope with challenging states by mediating metabolic output via heart rate increases (Porges, 2003, Porges et al., 1996). Indeed, research has shown that young children with greater levels of RSA withdrawal or suppression display better self-regulation and active coping skills, social competence, sustained attention, and fewer behavior problems (Calkins, 1997, Calkins and Dedmon, 2000, Calkins and Keane, 2004, Calkins et al., 2007, DeGangi et al., 1991, El-Sheik and Whitson, 2006, Graziano et al., 2007a, Huffman et al., 1998, Porges, 1991, Porges, 1995, Porges, 2001, Porges et al., 1996, Propper and Moore, 2006, Suess et al., 1994, Wilson and Gottman, 1996). Given these findings, considerable empirical and theoretical research has recently been conducted to examine the predictors of individual differences in RSA suppression.

In the current study, we were particularly interested in the role of the caregiver behavior in supporting the development of vagal regulation. Research has documented that early in development, children's successful self-regulation largely depends on caregiver support and flexible responding (Calkins and Fox, 2002, Kopp, 1982, Sroufe, 2000). Caregivers must be able to accurately read children's signals/needs and respond in sensitive ways that minimize distress and encourage positive interactions. Maternal behaviors indicative of emotional support, such as the use of praise, display of warmth/positive affect, responsiveness and sensitivity, and taking the child's developmental level into consideration are viewed as crucial scaffolding behaviors towards the development of self-regulation skills during infancy and throughout childhood (Landry, Miller-Loncar, Smith, & Swank, 2002). On the other hand, maternal behaviors that do not provide emotional support negatively affect children's self-regulation development. For example, harsh parenting behaviors such as being hostile, punitive, and expressing high levels of negativity is associated with high levels of stress and emotional overarousal in children, which may affect their ability to self-regulate (Blair, 2002, Hoffman, 2000). Intrusive behaviors that are characterized by the use of excessive demands and re-directing without sensitivity to the child's cues may be particularly frustrating for children who are beginning to engage in more autonomous behaviors (Calkins & Johnson, 1998).

While animal studies have clearly shown that caregiver behaviors can affect offspring's stress reactivity and physiological regulation (Calatayud et al., 2004, Caldji et al., 1998, Champagne and Meaney, 2001, Francis et al., 1999), fewer studies have examined similar association in humans. Preliminary findings indicate that children with higher RSA suppression tend to have mothers who concurrently display high levels of responsiveness/warmth, good co-regulated communication patterns, and low levels of intrusiveness/hostility (Calkins et al., 1998, Haley and Stansbury, 2003, Kennedy et al., 2004, Moore and Calkins, 2004, Porter, 2003). The context of children's physiological regulation also provides evidence for the importance of maternal behaviors as children display significantly greater RSA suppression during mother–child interaction tasks compared to more independent tasks (Calkins and Keane, 2004, Calkins et al., 2008). Additionally, greater levels of maternal sensitivity have also been shown to buffer genetic risk factors (e.g., DRD2 risk allele) in the prediction of infants’ RSA suppression levels (Propper et al., 2008). A longitudinal study also found that a mother–child relationship quality consisting of low levels of hostility, high levels of positive behaviors, and low levels of dysfunctional interactions predicted improvements in children's RSA suppression from age 2 to 5.5 (Calkins et al., 2008). What remains unexplored, however, is the extent to which treatment targeting changes in parent–child interactions can also lead to improvements in young children's vagal regulation.

Examining this research question within a sample of young children born premature is particularly relevant because of their well-documented difficulties in physiological and behavioral regulation thought to be due to prenatal and perinatal risk factors affecting brain stem and limbic functioning (Geva and Feldman, 2008, Minde, 2000). For example, research has demonstrated that preterm infants born premature display lower levels of baseline RSA and RSA suppression compared to full-term infants (Porges et al., 1996, Portales et al., 1997). The importance of preterm infants’ physiological regulation for later adaptive functioning has also been documented such that maturation of baseline RSA during infancy was associated with better social competence at 3 years of age (Doussard-Roosevelt, McClenny, & Porges, 2001). A more recent longitudinal study employed structural equation modeling to demonstrate that low baseline RSA of preterm neonates predicts a higher prevalence of behavior problems at 5 years both directly and indirectly via emotional and attentional processes during the first 2 years of life (Feldman, 2009). Given the above findings, determining the extent to which evidence-based interventions can improve underdeveloped physiological regulation in children born premature is of significant importance because it would provide information as to whether such treatments are targeting an underlying physiological mechanism that contributes to such adaptive functioning problems.

Parent-training interventions are the treatment of choice for young children with externalizing behavior problems (Eyberg, Nelson, & Boggs, 2008), who inherently have significant self-regulation difficulties across several domains (Keenan & Shaw, 2003). Parent–Child Interaction Therapy (PCIT) is an evidence-based parent-training intervention that been shown to be effective in reducing externalizing behavior problems in young children born premature (Bagner, Sheinkopf, Vohr, & Lester, 2010). Consistent with our discussion of caregiver behaviors that support children's emotional functioning, in the first phase of PCIT (described in more depth in Section 2), parents are taught to use “do skills” (e.g., praise, reflection, behavioral descriptions) to improve warmth and responsiveness in the parent–child relationship during a child-directed play. Parents are also taught to avoid “don’t skills” (e.g., commands, questions, and negative statements) and ignore inappropriate child behaviors.

The effectiveness of parent-training interventions such as PCIT in improving children's behavioral regulation are well documented (Nixon et al., 2003, Schuhmann et al., 1998, Zisser and Eyberg, 2010), but few treatment studies have measured changes in children's physiological regulation. In addition, those studies have typically examined children's physiological functioning as a moderator of treatment outcome rather than an outcome of treatment. For example, school-age children with higher baseline heart rate before treatment were reported by parents as having greater reductions in externalizing behavior problems after receiving Pelham's 2-week summer treatment program (2000) in conjunction with a parent training component (Stadler et al., 2008). Another significant limitation in these past studies is that physiological functioning was measured during a restful or baseline period and not in response to more challenging tasks. Therefore, children's actual physiological regulation was not examined. In addition, none of these previous studies or any to our knowledge have examined whether an evidence-based intervention is associated with improvements in children's RSA suppression.

The current study is the first to examine whether PCIT, an evidence-based intervention, is associated with improvements in children's physiological regulation as indexed by RSA suppression. In addition, no study has examined the relationship between changes in physiological regulation and treatment response among children born premature, a population at risk for behavior problems and difficulties with physiological regulation (Geva and Feldman, 2008, Minde, 2000). Recent findings also show that infants born premature with low cardiac baseline vagal tone receive the lowest amounts of maternal supportive behavior (e.g., positive affect, affectionate touch) and infant–mother synchrony compared to infants born premature with high cardiac baseline vagal tone (Feldman & Eidelman, 2007). Given the susceptibility of dysregulated preterm infants in eliciting appropriate care, the focus on improving maternal interactions in PCIT represents an ideal evidence-based intervention to implement and study with this at-risk population.

Consistent with past developmental work in which positive caregiver behaviors that provide emotional support promote the development of self-regulation, we expected that mothers’ increase in do skills taught during PCIT to be associated with improvements in children's RSA suppression. Given that PCIT also aims to decrease parent's use of excessive questions, commands, and negative statements, a reduction in these don’t skills was also expected to be associated with improvements in children's RSA suppression. Finally, it is important to examine an interactive effect between positive and negative parental behaviors on children's physiological regulation. Specifically, past research examining the efficacy of PCIT has shown greater effect sizes in parents’ increase in use of do skills versus decrease in use of don’t skills following treatment (Bagner & Eyberg, 2007). It may be the case that increasing parents’ use of positive do skills is what is accounting for children's improvements in various outcomes, even while parents continue to engage in some don’t skills. It is also important to note that the use of excessive commands that capture the essence of don’t skills are different from more hostile and punitive parenting behaviors that are associated with worse child outcomes, including physiological functioning (Calkins et al., 1998, Luecken and Lemery, 2004). Therefore, mothers’ improved use of do skills may buffer any potential negative association between continued use of don’t skills and children's RSA suppression.