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. 2019 May 5;6(2):160–183. doi: 10.3934/publichealth.2019.2.160

Table 1. Summary of articles included in the integrative review: maternal engagement in U.S. NICUs.

Author/Date Title Research Question/Aim Design Methods Sample Results/Conclusion
Affonso et al., 1993 Reconciliation and healing for mothers through skin-to-skin contact provided in an American tertiary level intensive care nursery To determine the feasibility and safety of SSC through KC as well as any effect on the mother's emotional care. Qualitative Mothers participated in three sets of semi-structured interviews after KC. N = 8 mother/preterm infant dyads, infant weight between 1,250 and 1,750 g, 24–32 weeks GA. Qualitative themes of reconciliation and healing when mothers placed their infant STS over three consecutive weeks.
Bloch-Salisbury et al., 2014 Kangaroo care: Cardio-respiratory relationships between the infant and caregiver To investigate physiological relationships between the infant/caregiver during SSC, and if respiratory stability of the premature infant is influenced by the caregiver's heartbeat. Prospective cross-control study Infant physiological markers were collected during SSC and a control period. N = 11 parent/pre-term infants (GA < 35 weeks); mean PCA 32 weeks. During SSC, infant respiratory instability and apnea incidence were each related to care giver heartrate variance instead of directly related to their own heartrate variance as in the control.
Cong et al, 2009 Kangaroo care modifies preterm infant heart rate variability in response to heel stick pain: Pilot study To determine if KC results in improved balance in autonomic responses to heel stick pain than the standard method where infants remain in IC for the heel stick. Prospective randomized cross-over trial (two group) Infant physiological markers and reactions to routine heel sticks (using ABSS) were collected during 24 hours of KC-inclusive care and 24 hours of routine IC. N = 14 mother/preterm infant dyads, infants 30–32 weeks GA and less than 9 days postnatal age. Infants experienced better balance in response to KC than IC condition as shown by more autonomic stability during heel stick, KC may be helpful in mediating physiologic response in preterm infants.
Cong et al., 2012 Effects of skin-to-skin contact on autonomic pain responses in preterm infants To determine the effects on autonomic responses in preterm infants for 30 minutes sessions of KC, 15 minutes of KC, and IC before and throughout heel stick. Prospective randomized cross-over trial (three group) Infant physiological markers and reactions to routine heel sticks (using ABSS) were collected during KC for durations of 30 minutes, 15 minutes, and IC. N = 26 mother/preterm infant dyads, infants 28 to less than 32 weeks GA and less than 14 days postnatal age. This study showed that KC has a significant effect on reducing autonomic pain responses in preterm infants. The findings support that KC is a safe and effective pain intervention in the NICU.
Cong et al., 2015 Parental oxytocin responses during skin-to-skin contact in pre-term infants To determine if oxytocin modulates parent stress and anxiety during maternal and paternal SSC with preterm infants. Prospective randomized cross-over trial (two group) The effects of KC on the mother's and father's hormone levels were observed pre-KC, during KC, and post-KC. Parents self-rated their anxiety during each stage. N = 28 Parent/preterm infant triads, infants were stable and between 30 to less than 35 weeks GA, and 3–10 days postnatal age. SSC activated the oxytocin release and reduced stress and anxiety responses in mothers and fathers of pre-term infants. SSC plays a positive role in early post-partum period and patterns of maternal and paternal bio-behavioral responses to SSC with pre-term infants might be different.
Gale et al, 1993 Skin-to-skin (kangaroo) holding of the intubated premature infant To determine if SSC affects visitation, attachment or caregiving behaviors among substance abusing mothers. Mixed methods; Prospective cohort and qualitative Demographics and physiological information was gathered. Parents were interviewed concerning their NICU and KC experiences. N = 25 Parent/intubated infant dyad/triads, infants of any GA (Range = 28–33 weeks GA at first holding). This study suggests that STS with small intubated infants may offer some parents an effective method to overcome some of the barriers to attachment imposed by the infant's hospitalization.
Goyna et al., 2017 Investigating skin-to-skin care patterns with extremely preterm infants in the NICU and their effect on early cognitive and communication performance: A retrospective cohort study To investigate how patterns of SSC might impact infant early cognitive and communication performance. Retrospective cohort study Medical record extraction. Multistep process of logistic regressions, t-tests, χ2 tests and Fisher's exact tests followed with exploratory network analysis using novel visual analytic software. N = 97 extremely preterm infants, GA < 27 weeks who completed 6-month and 12-month developmental assessments in the follow-up clinic. This study suggests an association between early and frequent skin-to-skin care with extremely preterm infants and early cognitive and communication performance.
Greene et al, 2015 Maternal psychological distress and visitation to the neonatal intensive care unit To examine any association between maternal visitation, psychological distress, and preterm infant post-NICU discharge outcomes. Prospective longitudinal and questionnaires Distress questionnaires given at 1 month post birth, 2 weeks prior to discharge, post discharge at 4 month CA. Visitation in NICU was recorded, as well as infant clinic attendance and rehospitalization. N = 69 mother/VBLW preterm infant dyads. Distress is an important predictor of visitation. In turn, visitation is associated with long-term maternal distress.
Hane et al., 2015 Family Nurture Intervention improves the quality of maternal caregiving in the neonatal intensive care unit: Evidence from a randomized controlled trial To determine the impact of FNI on maternal caregiving behavior. Intervention study; Randomized control trial Maternal caregiving behavior was coded during 30 minute holding and feeding periods prior to NICU discharge as an evaluation of FNI. N = 65 mother/preterm infant dyads. This is the first study to demonstrate that in-unit MCB can be enhanced by a hospital-based intervention. FNI provides a new rationale for integrating nurture-based interventions into standard NICU care.
Holditch-Davis et al., 2014 Maternally administered interventions for preterm infants in the NICU: Effects on maternal psychological distress and mother-infant relationship To determine if ATVV and KC affect maternal distress and mother-infant relationship. Intervention study; Randomized control trial (three group) Mothers completed questionnaires at 2, 6, and 12 months CA. At 2 and 6 months, mothers were videotaped interacting with their infant. N = 240 mother/preterm infant dyads, infants weighed < 1750 g at birth. These findings suggest that as short-term interventions, KC and ATVV, have important effects on mothers and their preterm infants, especially in the first half of the first year.
Hurst et al., 1997 Skin-to-skin holding in the neonatal intensive care unit influences maternal milk volume To evaluate the effect of early initiation of STS holding on lactation. Prospective cohort (for study participants) and Retrospective cohort (for control) A repeated-measures analysis of variance adjusting for baseline volumes (1 week after delivery) was used to evaluate the difference in milk volumes between STS and control groups. N = 23 mother/preterm infant dyads. STS holding of LBW infants in the early intensive care phase can result in a significant increase in maternal milk volume, thereby overcoming the frequently seen insufficient lactation experienced by these mothers.
Johnson, 2007 The maternal experience of kangaroo holding. To describe the maternal experience of kangaroo holding premature infants in the NICU. Qualitative, naturalistic inquiry design Semi-structured, open-ended interviews conducted with mothers. N = 18 mother/preterm infant dyads. Results identify maternal experiences of and responses to kangaroo holding in the intensive care environment, leading to the increased understanding of the multifaceted advantages of kangaroo holding on maternal attachment behaviors.
Lau et al., 2007 Ethnic/racial diversity, maternal stress, lactation and very low birthweight infants To compare maternal characteristics and psychological stress profile mothers with LBW infants and determine association between psychosocial factors, milk expression frequency, SSC, lactation performance. Repeated questionnaire Self-reported psychological questionnaires were given every 2 weeks after delivery over 10 weeks. Milk expression frequency, STS, and socioeconomic variables were collected. N = 124 mother/preterm infant dyads, infants born between 26–29 weeks GA. The response bias to self-reported questionnaires may not provide an accurate profile of maternal psychosocial profile. Lactation performance can be best enhanced with a multi-faceted intervention program including incorporating parental involvement in infant care and encouragement for frequent milk expression and STS.
Lester et al., 2016 18-Month follow-up of infants cared for in a single-family room Neonatal Intensive Care Unit To determine whether the SFR-NICU is associated with improved 18-month neurodevelopmental outcome, especially in infants of mothers with high maternal involvement. Prospective longitudinal study Infants divided into high versus low maternal involvement groups over a period of 18-month follow-up. Covariates of maternal, infant, and medical characteristics were abstracted from medical records. N = 216 mother/infant dyads, infants born < 30 weeks GA. High maternal involvement is associated with improved 18-month neurodevelopmental outcome, especially in infants cared for in a SFR-NICU.
Lewis et al., 1991 Visitation to a Neonatal Intensive Care Unit To examine and describe visitation patterns to a NICU as a function of neonatal and family variables. Longitudinal study Daily number of visits to NICU-admitted infants were logged. Health markers, physical conditions, and demographic information were extracted from medical records of the infants. N = 164 mother/infant dyads, infant birth weight < 2001 g. The greater the number of days with no visitors, the poorer the likelihood that the infant was brought to a 3-month follow-up clinic appointment.
Ludington-Hoe et al., 2004 Randomized control trial of kangaroo care: Cardiorespiratory and thermal effects on health infants To determine the safety and effects on healthy preterm infants of three continuous hours of KC compared to standard NICU care by measuring cardiorespiratory and thermal responses. Randomized control trial, pretest-test-posttest design Cardiorespiratory and thermal responses during three inter-feeding intervals were observed consecutively on one day. N = 24 healthy preterm infants nearing discharge, infants 33–35 weeks gestation at birth. Mean cardiorespiratory and temperature outcomes remained within clinically acceptable ranges during KC. Apnea, bradycardia, and periodic breathing were absent during KC. Regular breathing increased for infants receiving KC compared to standard NICU care.
McCain et al., 2005 Heart rate variability responses of a preterm infant to kangaroo care To examine the heart rate variability responses of one preterm infant to a KC experience with his mother. Case study report Case study report of a 35-week old preterm infant's behavior and heart rate variability when placed STS on his mother's chest. N = 1 preterm infant HRV was increased with fussy behavior in the open crib and decreased with sleep during KC. KC produced changes in behavior and HRV that are illustrative of decreasing stress.
Neu et al., 2000 The impact of two transfer techniques used during skin-to-skin care on the physiologic and behavioral responses of preterm infants To compare the impact of two different transfer techniques used in SSC (nurse transfer and parent transfer) on physiologic stability and other descriptive measures of physiologic stability related to energy conservation in ventilated preterm infants during and after SSC. Prospective cohort Fifteen ventilated preterm infants were randomly assigned to receive either parent or nurse-to-parent transfer on the first of 2 consecutive days and the alternate method the following day. N = 15 ventilated preterm infants, mean weight 1094 g. Both transfer methods resulted in physiologic disorganization. However, during and after STS care, infants exhibited no signs of energy depletion.
Neu et al., 2009 Coregulation in salivary cortisol during maternal holding of premature infants To examine coregulation between mothers and preterm infants in hypothalamic-pituitary-adrenocortical activity. Exploratory study Maternal and infant cortisol levels were obtained at beginning and end of holding. Coregulation was operationalized as less difference between maternal-infant cortisol levels immediately after holding as compared to before holding. N = 20 mother/infant dyads, infants mean postconceptional age of 34.7 weeks and average postnatal age of 15 days. A coregulatory relationship in cortisol levels existed between mothers and infants during holding, which was moderated by sound levels. Nurses in the NICU can facilitate the mother–infant relationship by promoting a quiet environment, particularly around mothers who are holding their infants.
Neu et al., 2013 Influence of holding practice on preterm infant development To determine if nurse supported kangaroo holding of healthy preterm infants in the first eight weeks of the infant's life facilitates early behavioral organization and development. Randomized control trial (three group) KC and blanket-held groups received 8 weekly educational visits from a RN. Maternal holding diary kept. APIB was administered when infants were 40 to 44 weeks PCA. N = 87 mother/preterm infant dyads, infants born between 32–35 weeks GA. Infants in the kangaroo and blanket groups had more optimal scores than the control group in Robust Crying. When kangaroo holding is compared to blanket holding, both methods may provide equal early behavioral organization and developmental benefit to the infant.
Neu et al., 2014 Effect of holding on co-regulation in preterm infants: A randomized controlled trial To determine whether kangaroo holding of healthy preterm infants over the first eight weeks of the infant's life would facilitate co-regulation in salivary cortisol between mother and infant. Randomized control trial (three group) Similar methodology as Neu et al., 2013. N = 79 mother/preterm infant dyads, infants born between 32–35 weeks GA, with a mean postnatal age of 15 days. Decreasing level of cortisol in mothers/infants suggest that holding promoted the expected decline in stress hormone levels. Supported holding methods did not differentially affect co-regulation compared to controls. Stress may need to be present in order for mothers/infants to demonstrate co-regulation in cortisol levels.
Phillips et al., 2012 Prevention of postpartum smoking relapse in mothers of infants in the neonatal intensive care unit To reduce postpartum smoking relapse and prolong breastfeeding duration during the first 8 weeks postpartum in mothers who quit smoking just before/during pregnancy and have NICU-admitted infants. Randomized control trial (two group) In addition to weekly encouragement to remain smoke free and routine breastfeeding support, intervention group mothers were also given enhanced support for maternal-infant bonding and STS was encouraged. N = 49 mothers of preterm infants in a NICU. Interventions to support mother-infant bonding during a newborn's hospitalization in the NICU are associated with reduced rates of smoking relapse and prolonged duration of breastfeeding during the first 8 weeks postpartum.
Pineda et al., 2018 Parent participation in the neonatal intensive care unit: Predictors and relationships to neurobehavior an developmental outcomes To define predictors of parent presence, holding/SSC in the NICU and investigate relationships between parent participation and early neurobehavior/developmental outcomes at age 4-5 years among preterm infants. Prospective longitudinal cohort study Parent presence and holding/SSC were tracked throughout NICU hospitalization. Neurobehavior at TEA/development at 4 to 5 years were determined using standardized assessments. N = 81 parent/preterm infant triads, infants born on or before 32 weeks GA, enrolled within 1 week of life in NICU. Social and medical factors appear to impact parent presence, holding, and STS care in the NICU. Parent holding is related to better developmental outcomes, which highlights the importance of engaging families in the NICU.
Reynolds et al., 2013 Parental presence and holding in the neonatal intensive care unit and associations with early neurobehavior To investigate the effects of parents' visitation and holding frequencies on infant development in the neonatal period. Prospective longitudinal cohort study Daily visits/holding activity recorded from birth until TE, supplemented with medical record extraction. Initial assessment used a modified version of the NISS, and later assessment used the NICU NNAS. N = 81 parent/preterm infant triads, infants born on or before 30 weeks GA. Infants who were visited and held more in the NICU had differences in early neurobehavior by term equivalent, which supports the need for and importance of early parenting in the NICU.
Roller, 2003 Getting to know you: Mothers' experiences of kangaroo care To reveal mothers' experiences of providing KC for their preterm newborns while still in the hospital. Qualitative, transcendental phenomenology Semi-structured interviews were conducted with mothers 1 to 4 weeks postpartum. N = 10 mothers who provided KC for their preterm newborns, 32–36 weeks GA, weighing 1500–3000 g. KC facilitates bonding and enhances maternal-infant acquaintance, even in the NICU environment. Mothers found that KC calmed them and their newborns.
Samra et. al., 2015 Effect of skin-to-skin holding on stress in mothers of late-preterm infants: A randomized controlled trial To examine the effect of SSC on stress perception between mothers who provided SSC to their late-preterm born infants and mothers who provided blanket holding. Longitudinal randomized control trial Maternal stress and physiologic stability was measured using the Parental Stressor intervention and SCRIP assessment respectively. Demographic and other covariates were extracted from medical records and daily logs were kept. N = 40 mother/late preterm infant dyads, infants born between 34 and less than 37 weeks GA. Mothers who provide SSC may experience more stress related to a more facilitated progression in the mother and infant relationship. The relationship between increased stress and the number of hours of SSC holding warrants further investigation.
Tully et al., 2016 A test of kangaroo care on preterm infant breastfeeding To test the effects of KC on breastfeeding outcomes in preterm infants. Secondary analysis of a randomized control trial (three group) The treatment groups were instructed in KC or ATVV intervention and the control group received only preterm infant care information. N = 231 racially diverse mother/preterm infant dyads, infants born weighing < 1,750 g. Mothers who practiced KC, regardless of randomly allocated group, were more likely to provide their milk than those who did not practice KC. As implemented in this study, assignment to the KC group did not appear to influence the measured breastfeeding outcomes.
Vittner et al., 2017 Increase in Oxytocin from skin-to-skin contact enhances development of parent-infant relationship To examine changes that occur in infant and parent salivary oxytocin/salivary cortisol levels during SSC and whether SSC alleviates parental stress and anxiety while supporting mother–father–infant relationships. Randomized crossover design Parental anxiety levels and saliva samples were collected from infants/mothers/fathers for oxytocin/cortisol measurement before, during, and after SSC. Parent–infant interaction was examined prior to discharge via video. N = 28 parent/preterm infant triads, infants born between 30 and less than 35 weeks GA, and 3–10 days postnatal age. Facilitation of SSC may be an effective intervention to reduce parent and infant stress in the NICU. Findings advance the exploration of oxytocin as a potential moderator for improving responsiveness and synchrony in parent–infant interactions.
Vittner et al., 2018 Parent engagement correlates with parent and preterm infant oxytocin release during skin-to-skin contact To examine relationships between parental engagement and salivary oxytocin and cortisol levels for parents participating in SSC intervention. Randomized crossover design Parental engagement was measured using PREEMI prior to hospital discharge. Saliva samples for oxytocin and cortisol levels were collected before, during, and after SSC. N = 28 parent/preterm infant triads, infants born between 30 and less than 35 weeks GA, and 3–10 days postnatal age. Significant relationships exist between parental engagement and salivary oxytocin and cortisol levels. Defining parent engagement facilitates identification of parent risks and needs for intervention to optimize preterm outcomes. The PREEMI can serve as a standardized instrument to examine parent engagement.
Welch et al., 2013 Randomized controlled trial of Family Nurture Intervention in the NICU: Assessments of length of stay, feasibility and safety To assess the effect of FNI on length of stay in the NICU and the feasibility and safety of its implementation in a high acuity level-IV NICU. Randomized control trial (two group) FNI was implemented by nurture specialists trained to facilitate affective communication between mother and infant during specified calming interactions. N = 150 mother/preterm infant dyads from 115 families, infants born between 26–35 weeks GA. There was no significant effect demonstrated with the FNI intervention amount on the primary short-term outcome, length of stay. FNI can be safely and feasibly implemented within a level-IV NICU.
Whipple, 2000 The effect of parent training in music and multimodal stimulation on parent neonate interactions in the Neonatal Intensive Care Unit To examine the effects of parent training in music/multimodal stimulation on the quantity/quality of parent-neonate interactions, weight gain, and length of hospitalization of premature/LBW infants in a NICU. Experimental/control group design Parents in the experimental group received approximately one hour of instruction in appropriate uses of music and multimodal stimulation. Parent-neonate interactions were observed in both groups. N = 20 mother/preterm infant dyads, infants born before 37 weeks GA, weight < 2500 g. Infant stress behaviors were significantly fewer and appropriateness of parent actions and responses were significantly greater. Parents with the intervention self-reported spending significantly more time visiting in the NICU. A post-discharge follow-up showed little difference between groups for parent-infant interactions in the home.
White-Traut et al., 2012 Frequency of premature infant engagement and disengagement behaviors during two maternally administered interventions To compare the frequency of premature infant engagement and disengagement behaviors during two maternally administered interventions, the multi-sensory ATVV intervention and KC. Randomized control trial (three group) Mothers in the ATVV intervention or KC groups administered the intervention a minimum of three times weekly and were video recorded weekly during intervention sessions. N = 26 mother/preterm infant dyads, infants born between 21–32 weeks GA, weight ranged from 1030–2693 g. The ATVV intervention elicited more disengagement, trended toward more engagement and more potent engagement, subtle disengagement, and potent disengagement behaviors than did KC. The ATVV intervention may be an intervention to promote the infant's learning how to regulate engagement and disengagement behaviors.
Zeskind et al., 1984 Effects of maternal visitation to preterm infants in the Neonatal Intensive Care Unit To investigate whether directing mothers to make weekly NICU visitation appointments would increase frequency of independent maternal visitation and affect maternal perceptions of the infant/infant's length of hospitalization. Randomized control trial Assessments of mothers' perceptions of their infants at the initiation of the intervention program, immediately following the first maternal visit, at discharge, and at a 6-week post-discharge follow-up. N = 32 mother/preterm infant dyads, healthy infants born between 30–36 weeks. Results suggest that the mother's greater contact and familiarity with her infant, as a result of increased visitation, resulted in more realistic observations of her preterm infant's behavior and may have facilitated the recovery of the infant.

Note: Abbreviations: ABSS—Anderson Behavioral Scoring System (assessment), APIB—Assessment of Preterm Infant Behavior (assessment), ATVV—Auditory Tactile Visual Vestibular (intervention), CA—Corrected Age, DMC—Dyadic Mutuality Code (assessment), FNI—Family Nurture Intervention (intervention), GA—Gestational Age, IC—Incubator Care, IMIS—Index of Mother-Infant Separation (assessment), KC—Kangaroo Care, LBW—Low Birth Weight, PCA—Postconceptional Age, PREEMI—Parental Risk Evaluation Engagement Model Instrument (assessment), NCAST—Nursing Child Assessment Satellite Training–Feeding Scale (assessment), NICU—Neonatal Intensive Care Unit, NICU NNAS—NICU Network Neurobehavioral Assessment Scale (assessment), NISS—Neonatal Infant Stressor Scale (assessment), RN—Registered Nurse, SCRIP- Stability of the Cardiorespiratory System in Preterm Infants score (assessment), SFR—Single Family Room, SSC—Skin-to-skin Care/contact, STS—Skin-to-skin, TE—Term Equivalent, TEA—Term Equivalent Age, VLBW—Very Low Birth Weight.