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Original Research

Parent Engagement Correlates With Parent and Preterm Infant Oxytocin Release During Skin-to-Skin Contact

Vittner, Dorothy PhD, RN, CHPE; Butler, Samantha PhD; Smith, Kelsey MA; Makris, Nefeli BS, RN; Brownell, Elizabeth PhD; Samra, Haifa PhD, RN-NIC, FAAN; McGrath, Jacqueline PhD, RN, FNAP, FAAN

Section Editor(s): Dowling, Donna PhD, RN; Section Editors; Thibeau, Shelley PhD, RNC-NIC; Section Editors

Author Information
doi: 10.1097/ANC.0000000000000558
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Abstract

More than 15 million premature infants are born annually around the world, and approximately 1 million children die from related complications.1 For survivors, the long-term implications of prematurity including differences in brain development, cognition, educational achievement, and behavior (including social and emotional regulation) are significant.2,3 Research indicates that the early social environment influences the neurobiology of the infant brain and thus socialization, through parent engagement, is an important factor in the health of a premature infant.4 Given the decreased synchrony or responsiveness and difficulty interpreting the subtle behavioral cues of premature infants, parents of preterm infants are more likely to have difficulty with attachment than mothers of full-term infants.5–7 Evidence suggests that early dysfunctional contacts due to the infant's disorganized behavioral patterns during infant and parent interactions lead to poorer attachment and increased probability for behavioral problems in childhood.7,8 Conversely, early responsive and synchronous contacts may positively influence cognitive and developmental outcomes for the child.9

Parent engagement is a compelling research concept in neonatal care that examines the synchronous factors between parents and infants that influence preterm infant health. It is a dynamic process focused on enhancing and supporting the parent–infant experience, specifically targeting the acquisition of skills for parent problem solving and provision of appropriate infant care based on the infant's strengths and weaknesses.10–12 Through parents' involvement and self-motivation to set goals and utilize informational resources about the unique care necessary for their child, parents can increase their engagement while improving the progression of their infant's health.12,13 Weber and colleagues4 describe the necessity for increased research into clinical interventions to improve infant outcomes through promoting mother–infant contact, monitoring infant physiological regulation, understanding resiliency of the mother–infant dyad to stress, as well as understanding the oxytocin pathways in both the parent and the infant.

Fundamental to the infant's developmental trajectory is early parent–infant contact. Parental–infant contact through touch, especially during skin-to-skin contact (SSC), has the potential to reduce the adverse consequences of prematurity. These benefits are thought to occur through physiological changes in the infant and parents that facilitate increased feelings of comfort, attachment, and physiological stability.14 SSC is an evidence-based holding strategy that increases the opportunity for parental proximity and provides a continuous interactive environment known to enhance infant physiological stability and affective closeness within the parent–infant dyad.14–16 SSC has been identified as a strategy to enhance developing relationships by increasing oxytocin levels and synchronous, responsive interactions between mothers, fathers, and infants.17,18 It is becoming increasingly more understood how the oxytocinergic system plays a key role in the establishment of attachment and parenting throughout early childhood.19 Oxytocin is also involved in the control of stress, anxiety, and autonomic functions such as heart rate. In addition, high oxytocinergic activity is stress relieving and anxiolytic in both animals and humans.20 Conversely, acute stress causes an increase in salivary cortisol and thus is frequently used as a biomarker of psychological stress.21,22 Further understanding of how these biomarkers can be used to explain biobehavioral mechanisms within the paradigm of increasing the development of parent engagement is needed.

The purpose of the primary study was to examine biobehavioral mechanisms of SSC for parents (both mothers and fathers) and preterm infants. The research question for the current exploratory pilot study was defined as follows: What is the relationship between parental engagement measured using the Parent Risk Evaluation on Engagement Model and Instrument (PREEMI) and biobehavioral markers of salivary oxytocin and cortisol? The relationship between parental engagement and parent anxiety at the time of SSC was also examined. This is the first study to systematically explore the association between parent engagement and biobehavioral markers and was not examined in the previous analysis. We hypothesized that during and after SSC, parents and preterm infants would show increased oxytocin levels, decreased cortisol levels, and decreased parent anxiety and also that parents would report increased parent engagement at hospital discharge following initiation of SSC during the first 2 weeks of their infant's hospitalization. The long-term goal of this research is to work toward identifying strategies to increase endogenous oxytocin release for parents and infants in the neonatal intensive care unit (NICU) to reduce stress and improve parent–infant relationships. Uncovering the biobehavioral basis of early parent–infant interactions via biomarkers is an important step in developing therapeutic modalities to increase parent engagement and improve health outcomes.

METHODS

Design

This exploratory pilot study examined parent engagement at discharge for both mothers and fathers using a randomized crossover design over a 3-day time frame with an SSC intervention conducted in the NICU in central Connecticut between November 2015 and June 2016 for collection of data for salivary oxytocin and cortisol levels. This study received university and hospital institutional review board approval. Portions of the biobehavioral data have been reported elsewhere in relationship to the SSC intervention.17

Sample

Convenience sampling techniques were utilized to recruit and consent 32 stable preterm infants and their mothers and fathers. To recruit healthy preterm infants, infant inclusion criteria included infants between and weeks' gestational age at birth and between 3 and 10 days old at the start of the study.17 Exclusion criteria included infants who (1) were intubated and receiving mechanical ventilation, (2) had known congenital anomalies, (3) had severe periventricular/intraventricular hemorrhage (grade III), (4) had undergone minor or major surgery, (5) were receiving sedatives or vasopressors or analgesics to control for the effect of sedative medication on behavioral states, (6) had positive drug exposure history to control for the effect of drugs on behavioral states and autonomic responses, or (7) were receiving continuous feedings, as these interfere with salivary oxytocin and cortisol sampling. The salivary samples were obtained 1 hour after intermittent feeding finished for all infants.17

Parental eligibility criteria were (1) age older than 18 years, (2) English speaking, and (3) without a history of depression.17 For parental history of depression, we relied on self-report during the consent process and review of infant medical records. After informed consent, demographic characteristic variables were collected from the primary caregiver. All parents in the primary study participated in the parent engagement exploratory study.

Measures

Parental engagement was measured using the PREEMI just prior to the infant's hospital discharge. The PREEMI is a parent survey that measures the degree of parent engagement with their infant on a 7-point Likert scale (1 = never, 7 = always). The instrument includes 5 conceptual subscales: Self-efficacy, Social Support, Outcome Expectations and Intent, Knowledge and Awareness of Development, and Perception of Risk. A composite score is obtained by adding the score of all items together. A higher score on the PREEMI, as well as in each of the subscales, represents increased parent engagement with their infant.

Parent anxiety scores were measured using a validated 8-item visual analog scale.17,18,23 Mothers and fathers completed the tool before SSC, during SSC, and after SSC and were asked to rate their perspectives on whether the statements were true and then a composite score was generated for each data point (before SSC, during SSC, and after SSC). Each item represented an emotion such as “I am very worried and anxious” and was scored by the parents using a 100-mm line rating their feelings from “not at all” to “worse than I have ever before.” There are 2 primary constructs or dimensions associated with the parent anxiety scale determined using principal component analysis. The α reliability of the data was calculated at .93.

Procedures

For collection of the biobehavioral data, each triad was randomly assigned to one of 2 sequences: maternal-SSC (M-SSC) on day 1 and paternal-SSC (P-SSC) on day 2; or P-SSC on day 1 and M-SSC on day 2. Infants' and parents' saliva samples for oxytocin and cortisol were collected 15-minute pre-SSC, 60-minute during-SSC, and 45-minute post-SSC. Timing of sample collection was modeled after Cong et al,15 with modification to control for differences they found in mother and father responses, and to remain consistent within the 3-hour time interval for the standard nursing care practices within each of the NICUs. We collected parent saliva samples using the unstimulated passive drool method.24 We obtained infant saliva samples using infant swab methods (Salimetrics LLC, State College, Pennsylvania). The salivary samples were frozen in a −80°C freezer until thawed for analysis. We completed the salivary oxytocin assay analysis using a method similar to that specifically developed and validated for salivary oxytocin analysis by Carter and colleagues25 and previously reported.17 The salivary cortisol analysis was completed via an enzyme immunoassay (Salimetrics LLC). Although neonatal infants may not show a circadian pattern, oxytocin and cortisol were collected from the infants on the basis of the infant's feeding schedule between 1 and 3 pm to control for diurnal changes and feeding/eating influences on oxytocin and cortisol responses.26,27 The salivary samples were frozen in a −80°C freezer until thawed for analysis. The analysis was completed as soon as enough samples were obtained to run the assay kit. The first batch of samples was rerun to ensure data were correct and that data were consistent when rerun.

Statistical Analyses

The overall sample size of 28 complete triads provides 80% levels of power for M-SSC/P-SSC with 1-sided tests at the 5% level of statistical significance.17 Data were analyzed using IBM SPSS version 18; data were not normally distributed; therefore, Pearson's correlation was used to measure the relationship between maternal and paternal engagement composite scores with salivary oxytocin and cortisol levels. Multivariable linear regression models were used to model the effects of maternal and paternal oxytocin and cortisol levels independently on engagement composite scores, adjusting for infant oxytocin and cortisol levels, respectively, given that the engagement level occurred after collection of the biomarker data.

RESULTS

Participating infants were born at a mean of 33 weeks' (SD = 1.57) postmenstrual age.17 The majority of infants were white (61%) males (68%). Most mothers (89%) held their infants in SSC prior to the study participation, whereas only some of the fathers (27%) previously held their infant SSC. Only a small percentage of parents (32% of mothers, 21% of fathers) had previous SSC experience with another infant. Specific details of sample and demographic characteristics are described previously.17 The majority of parents were white (68%) and college educated (93% of mothers and 89% of fathers). The mothers' mean age was 32 years, whereas the fathers' age was 33 years. The infants were relatively healthy, with a mean Score for Neonatal Acute Physiology with Perinatal Extension (SNAPPE-ll) of 3.93. This score is a valid indicator of an infant's severity of illness and predictor of mortality risk.

Oxytocin levels significantly increased and cortisol levels decreased for mothers, fathers, and infants during SSC as compared with baseline.17 As previously reported by Vittner and colleagues,17 there were no differences for the infants' salivary oxytocin or cortisol response whether the infant was held by the mother or the father.

The PREEMI mean composite score for parents was 261, with a range of 199 to 305, indicating a moderate to high level of parental engagement for all participants. To identify the relationship between salivary oxytocin levels and parental engagement, a significant negative correlation was noted between paternal oxytocin levels (father) and paternal engagement (father) at discharge (r = −0.43; P = .03) and a significant negative correlation between infant oxytocin levels and maternal engagement at discharge (r = −0.54; P = .004). There was no significant interaction between maternal oxytocin or cortisol levels and maternal engagement scores (see Table 1). However, the adjusted linear regression model (see Table 2) for infant salivary oxytocin and cortisol levels showed that as infant oxytocin levels increased by 1 unit, maternal engagement scores significantly decreased by 0.04 units (β = −.04; 95% CI, −0.07 to −0.01; P = .01). A standardized β coefficient compares the strength of the effect of each individual independent variable with the dependent variable, with the higher the absolute value of the β coefficient, the stronger the effect. The unadjusted linear regression model (see Table 3) showed that as paternal oxytocin levels increased, paternal engagement scores significantly decreased (β = −.14; 95% CI, −0.26 to −0.02; P = .03). Linear regression, adjusted for infant oxytocin and cortisol levels, showed that as paternal oxytocin levels increased by 1 unit, paternal engagement score significantly decreased by 0.16 units (β = −.16; 95% CI, −0.28 to −0.03; P = .03) and as paternal cortisol levels increased, there was a significant decrease in paternal engagement (β = −68.97; 95% CI, −136.8 to −1.2; P = .05).

TABLE 1. - Correlation Between Parental and Infant Oxytocin and Cortisol Levels and Parental Engagement
Variables Father Composite Score Mother Composite Score
Pearson's r P Pearson's r P
Father
Oxytocin −0.43 .03 ... ...
Cortisol −0.32 .10 ... ...
Mother
Oxytocin ... ... 0.23 .27
Cortisol ... ... −0.02 .92
Infant
Oxytocin 0.05 .80 −0.54 .004
Cortisol −0.08 .68 −0.08 .69

TABLE 2. - Relationship Between Maternal Oxytocin and Cortisol Levels and Maternal Engagement
β 95% CI P
Unadjusted
Maternal oxytocin .04 −0.03 to 0.11 .27
Adjusted
Maternal oxytocin .02 −0.05 to 0.09 .53
Infant oxytocin −.04 −0.07 to −0.01 .01
Unadjusted
Maternal cortisol −2.80 −59.3 to 53.7 .92
Adjusted
Maternal cortisol −2.16 −59.8 to 55.5 .94
Infant cortisol −15.27 −94.3 to 63.8 .69
Significance identified p<0.05.

TABLE 3. - Relationship Between Paternal Oxytocin and Cortisol Levels and Paternal Engagement
β 95% CI P
Unadjusted
Paternal oxytocin −.14 −0.26 to −0.02 .03
Adjusted
Paternal oxytocin −.16 −0.28 to −0.03 .03
Infant oxytocin .03 −0.03 to 0.08 .31
Unadjusted
Paternal cortisol −50.8 −112.8 to 11.3 .10
Adjusted
Paternal cortisol −68.97 −136.8 to −1.2 .05
Infant cortisol −106.21 −274.8 to 62.4 .21

To identify the relationship between parent anxiety levels and parent engagement, a significant negative correlation was also seen with paternal anxiety scores before SSC holding and paternal composite engagement scores (r = −0.52, P = .01), as well as with paternal anxiety scores after SSC and paternal composite engagement scores (r = −0.44, P = .02). There were no significant relationships identified with maternal anxiety scores and composite engagement scores. As paternal anxiety scores increased, their engagement scores decreased (95% CI, −0.16 to −1.01; P = .02).

DISCUSSION

This study demonstrated significant relationships between parent engagement at NICU discharge and salivary oxytocin and cortisol levels during SSC early in the NICU stay. We found that the PREEMI mean composite scores indicating the amount of engagement were in the moderate to high range. This is not surprising, as the primary study included an SSC intervention and thus many of the parents continued with daily SSC after study participation throughout the infant's hospitalization, which may have influenced their engagement scores at discharge. Interestingly, for fathers, the SSC intervention was often the first time they held their infants. Anecdotally, the researchers observed upon participation in the study that fathers consistently participated in SSC throughout the infant's hospitalization after the 1-time study intervention even when they had been reluctant to participate.

In addition, the overall oxytocin levels increased during SSC for parents and infants whereas cortisol levels decreased for parents and infants during SSC, thus indicating the calming and beneficial impact of SSC for both parents and infants. Oxytocin facilitates social sensitivity and attunement necessary for developing relationships and nurturance for emotional and physical health.12,25 The changes in oxytocin and cortisol levels provide robust support to advocate for increased SSC during infancy, especially for the vulnerable infant in the NICU.

Measuring parent engagement using the PREEMI provides us with insight into the relationship between parent engagement and biobehavioral markers. We speculate that together the increases in oxytocin levels and concurrent decreases in cortisol levels during SSC allow both the infant and the parent to develop a more synchronous relationship that enhances opportunities for bonding and attachment, especially in the challenging environment of the NICU. Our results demonstrated that parents with lower cortisol and higher oxytocin levels activated during an episode of SSC session in the first 2 weeks after birth were significantly related to parent engagement before discharge. We believe these findings suggest that parents with a lower salivary cortisol level as seen with SSC (decreased stress) may facilitate increased parental engagement. Previous research related to parent engagement has shown that parents who are more engaged are more likely to have the appropriate outcome expectations for their infants, be confident in care of their infant, and access resources to meet the unique needs of their infant.12 This study provides further evidence that using the PREEMI provides a window into parent engagement that could be used as an assessment for the degree of engagement (low vs high) and thus who and when to intervene with to increase engagement. In the adult literature, patient engagement is used synonymously with patient activation in relationship to the self-management of their own healthcare. We hypothesize that degree of parent engagement can be used as a measure of the parents' ability to manage their high-risk infant's healthcare needs after discharge.

An important feature of the oxytocinergic system is the formation of an affectionate bond that is modified by experience.26,28 Fathers in this study showed an increased oxytocin levels during SSC; however, contrary to expectations, this increase was negatively correlated to paternal engagement. Research on the oxytocinergic system in human fathers is limited; yet, fathers are important in shaping an infant's development.29 Past research noted that father salivary oxytocin increased during play with their infant along with increases in infant's salivary oxytocin levels and engagement behavior.30 In addition, oxytocin levels have been found to be similar in mothers and fathers and related to parent-specific mode of tactile contact. Parents, especially fathers, providing higher levels of affectionate contact showed an oxytocin increase following interaction but not when they were less interactive.26 While these studies support the finding of increased paternal oxytocin during interaction, they do not explain why decreased paternal engagement ratings would be related to oxytocin increase.

One important feature of the oxytocinergic system is the formation of an affectionate bond that is modified by experience.26,28 Research on the oxytocinergic system in human fathers is limited; yet, fathers are important in shaping an infant's development.29 An explanation could be that prior research looked at oxytocin levels with fathers and their older healthy infants (4-6 months) in an outpatient setting. Interaction with a fragile infant in the NICU could add additional variables that effect parental engagement and oxytocin levels. In the traditional NICU, fathers may spend less physical time with the infant at the bedside whereas mothers are often present. Fathers in this study were less likely to have held their infants prior to measurements of SSC and, overall, have had less interaction with their child at the time of both oxytocin and engagement measurement. Future research might consider remeasuring biobehavioral markers at a subsequent SSC interaction to see whether there is change over time in oxytocin levels and whether the number of paternal interactions is related to oxytocin measurement and rating of engagement.

The differences in timing of data collection have implications that cannot be ignored when considering our results. Parent engagement was measured at discharge and the biomarkers were measured in relationship to the SSC intervention, and although it would seem the outcomes are related, given the existing evidence about developing parent–infant relationships, more data are needed to establish whether these relationships among the variables truly exist, such as measurements of parent engagement at different points in the infant's hospitalization.

In addition, maternal oxytocin levels are elevated in situations related to affectionate touch whereas paternal oxytocin is associated with stimulatory touch by facilitating movement toward objects and directing an infant's attention to their environment.26,29 SSC in this study could be categorized as more affectionate touch rather than stimulatory touch and thus less likely to provide the type of behaviors more typically seen in paternal responding and initiation of bonding. However, more data points for understanding how these biobehavioral markers change over time are needed to better understand these relationships.

Limitations

In terms of limitations, although interesting relationships and correlations were identified within the data, because of the exploratory nature of this pilot study and randomized crossover design of the primary study, no clear causality can be delineated. In addition, the measures used in our comparison were taken at 2 different times during the NICU, which could have affected the results. The authors recommend caution in generalizing the findings to other settings and age groups. Regardless, these data provide a better understanding of the degree of parent engagement in the NICU environment. Also, this study uses salivary oxytocin and cortisol levels, which are peripheral measures of oxytocin and cortisol rather than central measures, again limiting our ability to make generalizations. Although the PREEMI is a published reliable tool, more research with larger sample sizes is needed to appropriately interpret the results to make any generalizations. The inconsistency of the NICU environment throughout the infant's hospitalization may influence in how parent engagement evolved over time; yet, for each episode of SSC data collection that was early in the infant's hospitalization, the sensory environment was muted with dimmed lighting and decreased random sounds. In future studies, we recommend measuring parent engagement and oxytocin levels at different points during the NICU admission to increase our understanding of how parent engagement may change over time and may change in relationship to other factors related to hospitalization. The study also only looks at preterm infants in the NICU, with parents just getting to know their infants. It would be helpful to measure the impact of SSC on older infants and parents who have been in interaction with their children for longer periods of time.

CONCLUSIONS

Mother, father, and infant salivary oxytocin and cortisol levels appear to have a significant influence on parental engagement. Yet, more research is needed to better understand these relationships. Oxytocin facilitates social sensitivity and attunement necessary for developing relationships and nurturance for emotional and physical health, whereas cortisol can impact the ability to bond. Early parent–infant contact is the cornerstone of the infant's health and well-being. Parent–infant relationships are difficult to establish, especially when parents confront challenges during the early postpartum period such as hospitalization in the NICU. Defining parent engagement is a means for identification of parent risks and needs for intervention to optimize outcomes for premature infants. Interventions such as SSC can increase endogenous oxytocin release for parents and infants in the NICU to reduce stress with the potential to improve parent–infant interactions. Uncovering the biobehavioral basis of early parent–infant interactions is an important step in developing therapeutic modalities to improve infant health outcomes.

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Keywords:

oxytocin; parental engagement; PREEMI; preterm infant; skin-to-skin contact

© 2018 by the National Association of Neonatal Nurses.