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University of Connecticut, School of Nursing, 231 Glenbrook Road U-4026, Storrs, CT 06269-4026, United States
Bolton School of Nursing, Case Western Reserve University, United States
Connecticut Children's Medical Center, University of Connecticut School of Medicine, United States
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Connecticut Children's Medical Center, University of Connecticut School of Nursing, United States
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a r t i c l e
i n f o
Article history:
Received 24 February 2015
Received in revised form 23 April 2015
Accepted 25 April 2015
Keywords:
Oxytocin
Cortisol
Maternal skin-to-skin contact
Paternal skin-to-skin contact
Pre-term infants
Anxiety
a b s t r a c t
Objective: Maternal skin-to-skin contact (M-SSC) has been found to reduce adverse consequences of prematurity, however, its neurobiological mechanisms have been unknown. The purpose of the study was
to examine oxytocin mechanism in modulating parental stress and anxiety during M-SSC and P-SSC
(paternal SSC) with their pre-term infants.
Methods: Twenty-eight stable pre-term infants and their parents (triads) were recruited in a 2-day
cross-over study and 26 mothers and 19 fathers completed the study protocol. Each triad was randomly
assigned to one of the two sequences: M-SSC was conducted on day-1 and P-SSC on day-2; and P-SSC on
day-1 and M-SSC on day-2. Parents' saliva samples for oxytocin and cortisol assays and visual analog
anxiety levels were collected pre-SSC, 30-min during-SSC, and 30-min post-SSC.
Results: Both maternal and paternal oxytocin levels were signicantly increased during-SSC from baseline.
Maternal oxytocin dropped post-M-SSC, but paternal oxytocin continued to be maintained at a higher level
during post-P-SSC. Both maternal and paternal cortisol levels signicantly decreased during-SSC from
baseline. Maternal cortisol continuously dropped post-M-SSC, but paternal cortisol increased post-P-SSC.
Both mothers' and fathers' anxiety levels decreased during-SSC from baseline, and then increased
post-SSC. Motherfather dyads also showed correlated or synchronized stress and anxiety responses in
the NICU.
Conclusion: M-SSC and P-SSC activated the oxytocin release and reduced stress and anxiety responses in
mothers and fathers of pre-term infants.
Practice implications: 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.
2015 Elsevier Ireland Ltd. All rights reserved.
1. Introduction
Half a million premature births occur each year in the United States
[1]. Pre-term birth is itself a source of stress for parents, with high
levels of stress negatively impact parenting behaviors and parenting
competence [2]. Furthermore, the placement of a pre-term baby in the
NICU, may add to parents' stress in an unfamiliar environment. Physical
separation from the newborn is known to increase maternal stress and
anxiety [3], and it may have similar effects on the father, but, little is
Corresponding author. Tel.: +1 860 486 2694 (Ofce); fax: +1 860 486 0001.
E-mail addresses: xiaomei.cong@uconn.edu (X. Cong), Susan.Ludington@case.edu
(S.M. Ludington-Hoe), Hussain@uchc.edu (N. Hussain), regina.cusson@uconn.edu
(R.M. Cusson), stephen.walsh@uconn.edu (S. Walsh),
victoria.vazquez@huskymail.uconn.edu (V. Vazquez), CBriere@ccmckids.org (C.-E. Briere),
dorothy.vittner@uconn.edu (D. Vittner).
http://dx.doi.org/10.1016/j.earlhumdev.2015.04.012
0378-3782/ 2015 Elsevier Ireland Ltd. All rights reserved.
402
nucleus tractus solitarius, the locus ceruleus, and the vagal motor
nucleus of the brain stem to modulate attachment, parenting behaviors,
physiologic stability, emotion, anxiety and stress [5]. The oxytocinergic
system supports parentinfant interactions by a bio-behavioral
feedback loop involving OT: maternalinfant contact and touch stimulates the expression of OT, while the release of OT, in turn, leads to the
promotion of increased maternalinfant proximity [7].
Parentinfant touch activates the oxytocinergic system, resulting in
release of OT in both animals [8] and humans [9]. SSC between mothers
and newborns, a form of parentinfant touch, is hypothesized to
activate the oxytocinergic system in both the infant and parent,
reducing stress and anxiety. The pain and stress reducing effects of
maternal SSC (M-SSC) have frequently been measured in infants [10],
but have been studied less in parents, with some indirect evidence of
reduction of maternal stress [11], but the effects of paternal SSC
(P-SSC) on fathers' stress are largely unknown. The specic aims
of this study were to: 1) determine differences in the levels of OT,
salivary cortisol, and self-reported anxiety scale before, during, and
after M-SSC and P-SSC with hospitalized newborn pre-term infants;
and 2) establish relationships between maternal and paternal levels
of OT, stress, and anxiety scale during the different phases of SSC.
2. Methods
2.1. Study design, setting, and participants
A randomized cross-over design was used over a 2-day study
period. The motherfatherinfant triad was assigned to one of the two
study sequences: the M-SSC condition was conducted on day-1 and
the P-SSC occurred on day-2; and P-SSC on day-1 and M-SSC on
day-2. The order of the sequences for each triad was determined
randomly by a computer-program using simple random assignment.
The study was conducted in a level IV NICU in Connecticut. Infant
motherfather triads were recruited using a convenience sampling
approach. Inclusion criteria were: male and female stable pre-term
infants who were 30 0/734 6/7 weeks gestational age at birth and
310 days old post-natal age; cared for in an incubator; and either
NPO or on bolus feeds to control for feeding effects on cortisol levels.
Exclusion criteria were: infants who were intubated and receiving
mechanical ventilation; had known congenital anomalies; had severe
periventricular/intraventricular hemorrhage ( Grade III); or had
undergone minor or major surgery. Parents had to be 18 years and
older without a history of depression so that the inuences on OT [12]
and cortisol levels [13] were minimized. Parents' history of depression
were based on self-report and maternal medical record.
Power analysis was conducted to determine the sample size.
Previous study suggested medium effect sizes for maternal and paternal
changes in OT during highly affectionate or stimulatory contact with
their infants [14]. A sample of 27 subjects can provide 80% levels
of power for M-SSC/P-SSC, to detect such effects when applying
one-sided tests at the 5% level of statistical signicance.
2.2. Study conditions and procedures
The study protocol was approved by the institutional review
boards of the participating hospital and university. The research nurse
in the NICU identied eligible infants daily, approached potential
parents, and obtained consent from both mother and father. The
infantmotherfather triad was then randomized to one of the two
study sequences i.e., M-SSC on day-1 or P-SSC on day-1 and data
collection were done during the same time frame each day.
Sampling time of the day is an important consideration in assessing
cortisol and OT levels. For adults, both cortisol and OT may display
diurnal patterns of highest in the morning and lowest at midnight
[15], therefore, establishing consistency in sampling times was important to reduce noise from circadian variation [15]. Study procedures
and data collection occurred in the early afternoon on each study day.
Based on the individual infant's feeding schedule, the period of 1 to
3 pm is about 1 h following the previous feeding and 1 h before the
next feeding, and about 1 h after parents' lunch. Mothers' breast milk
pumping was another consideration, therefore, the selection of this
time can control for diurnal changes and feeding/eating inuences
on OT and cortisol responses. Each study condition, M-SSC or P-SSC
included three study phases: pre-SSC, during-SSC, and post-SSC. The
procedures of each study phase were as follows and shown in Table 1.
2.2.1. Pre-SSC phase (10 min)
The mother or father was asked to arrive at the NICU at least 10 min
before SSC and rest in a chair for several minutes. Then his/her
saliva sample was collected rst, after which he/she was asked to
self-rate his/her own anxiety level on a validated visual-analog scale.
The infant remained in the incubator during this study phase.
2.2.2. During-SSC phase (30 min)
The mother or father was instructed to hold the infant skin-to-skin
for a 30-min period. A 30-min SSC was selected because previous
studies have shown that 30 min of SSC is effective in reducing infants'
stress and pain response as well as parental stress [16]. 1) M-SSC
condition: The mother was instructed to dress in a hospital gown
opened in the front and move to the La Fuma recliner chair with a
footrest especially used for SSC. After she was seated, the chair was
reclined. The infant was transferred by the researcher from the
incubator into SSC position using a standard transfer technique [17].
The diaper-clad infant was placed on the mother's chest, skin-to-skin
and chest-to-chest, in a prone and upright position at an incline of
3040. The infant was covered across the back with a blanket and
with the mother's cover gown. If the father was present, the father
was asked to sit on a chair near the motherinfant pair. A folding screen
was placed around the family to ensure their privacy. During the last
5 min of the 30-min M-SSC, maternal saliva was collected, and
then the mother was asked to self-rate her anxiety measurement.
2) P-SSC condition: The data collection procedure during P-SSC condition was the same as M-SSC, except that the father was holding the infant throughout the SSC. The father's saliva sample and anxiety
measurements were similarly obtained during the last 5 min of P-SSC.
2.2.3. Post-SSC phase (30 min)
The infant was transferred back to his/her incubator after 30 min
of SSC. The mother or father was asked to dress-back and sit at the
side of the incubator within their designated private area for another
30 min. During the last 5 min of the 30-min post-SSC, the mother's or
father's saliva was collected, and then they were asked to self-rate
their anxiety level.
2.2.4. Saliva collection procedure
Saliva samples from parents were collected using a standard
unstimulated passive drool method. Because several components can
confound salivary cortisol measurement, the parents were instructed
not to eat, drink alcohol, smoke, or exercise 1 h before the data collection. When the mother or father arrived at the NICU, the parent was
required to rinse her/his mouth thoroughly with water to remove any
food particles. Before saliva collection, any contaminating components
in the mouth were visually checked by the study coordinator. To
standardize collection for each sample, the parent was asked to reserve
saliva in her/his mouth without swallowing for 1 to 2 min. After saliva
reservation, with head tilted forward, the parent used a 2-inch plastic
drinking straw to expectorate saliva into two pre-chilled 2 mL Cryovials
(Salimetrics, State College, PA), which were suspended in a cup of ice
throughout the collection process. The Cryovials were then transferred
and stored in the 80 C freezer until assay.
Pre-M-SSC/
Pre-P-SSC
(10 min)
1:00
1:09
Rest in chair
OT & Cort
Anxiety
During-M-SSC/
During-P-SSC
(30 min)
1:10
1:40
SSC with her/
his infant
OT & Cort
Anxiety
Post-M-SSC/
Post-P-SSC
(30 min)
1:41
2:10
SSC finished,
parent rested OT & Cort
Anxiety
Note: Table shows a data collection timeline if the infant has a 3-hour feeding schedule and
a feeding time at 12 pm. M-SSC: maternal skin-to-skin contact with infant; P-SSC: paternal
skin-to-skin contact with infant; OT: salivary oxytocin; Cort: salivary cortisol.
403
between M-SSC and P-SSC periods will be sufcient for wash out to
occur [20]. Testing differences between periods for parental OT, cortisol,
and anxiety levels were conducted using repeated-measures analysis of
variance (RM-ANOVA), with the study phase (pre-, during, and
post-SSC) as the repeated factor in a two-tailed test with a 5% level of
signicance analysis. Maternal and paternal stress and anxiety
responses were also examined for correlations between motherfather
dyads.
3. Results
3.1. Characteristics of the participants
Mother (n = 26)
Father (n = 19)
Age (years):
Race
White
African American
Asian
Hispanic
Yes
No
Education
College or higher
High school
Marital status
Married/partner
Single
SSC experience since birth
Yes
No
Infant characteristics (n = 26)
GA at birth (weeks)
Birth weight (g)
Type of delivery
Vaginal
Cesarean section
PNA at study (days)
M-SSC
P-SSC
31.5 6.8
35.6 5.9
20 (76.9%)
5 (19.2%)
1 (3.8%)
13 (68.4%)
4 (21.0%)
2 (10.5%)
7 (26.9%)
19 (73.1%)
5 (26.3%)
14 (73.7%)
16 (61.5%)
10 (38.5%)
15 (78.9%)
4 (21.1%)
19 (73.0%)
7 (27.0%)
14 (73.7%)
5 (26.3%)
18 (69.2%)
8 (42.1%)
10 (52.6%)
9 (47.4%)
32.7 2.1
1650.1 585.8
8 (30.8%)
18 (69.2%)
7.5 1.5
8.0 1.6
404
30.00
67.00
25.00
57.00
52.00
Mother
47.00
Father
42.00
37.00
Anxiety Levels
Oxytcoin (pg/mL)
62.00
20.00
Mother
15.00
Father
10.00
5.00
32.00
Pre-SSC
During-SSC
0.00
Post-SSC
Pre-SSC
Fig. 1. Maternal and paternal salivary oxytocin values from pre-SSC to during-SSC
and post-SSC. Standards of error of means bar.
During-SSC
Post-SSC
Fig. 3. Maternal and paternal anxiety levels (VAS scores) from pre-SSC to during-SSC
and post-SSC. Standards of error of means bar.
Cortisol (ug/dL)
0.58
0.48
Mother
0.38
Father
0.28
0.18
0.08
Pre-SSC
During-SSC
Post-SSC
Fig. 2. Maternal and paternal salivary cortisol values from pre-SSC to during-SSC and
post-SSC. Standards of error of means bar.
responses during both mother and father SSC with their pre-term
infants. The results suggest, as predicted, that both maternal and
paternal OT levels were signicantly increased during 30 min of
M-SSC/P-SSC, compared to the baseline levels, but mothers and
fathers showed different OT response patterns at 30 min post-SSC.
Maternal OT dropped at post-M-SSC, but paternal OT continuously
maintained at a higher level at post-P-SSC. Meanwhile, both
maternal and paternal cortisol levels were signicantly decreased
during-SSC from baseline, and then maternal cortisol continuously
dropped in post-M-SSC, but paternal cortisol increased at postP-SSC. Both mothers' and fathers' anxiety levels were also signicantly decreased during-SSC from baseline, and then increased at
post-SSC. Motherfather dyads showed correlated or synchronized
stress and anxiety responses in the NICU.
Animal studies have shown that the neuropeptide OT plays a
key role in parentinfant bonding formation and other social and
affective behaviors. Maternal contact, such as licking-and-grooming
behavior in rats, activates the brain oxytocinergic system in both
mother and infant [8] and central OT injections can quickly induce
maternal behavior [21]. Although much less research has explored
OT and fathering of infants, OT level has been associated with
paternal exposure to pup stimuli and paternal care [7]. These
ndings suggest that the oxytocinergic system may modulate
parentinfant interactions by a bio-behavioral feedback loop of OT,
and maternal behaviors can further consolidate the OT system in
both mother and infant [7]. Early parentinfant touch may enhance
parenting and infantparent attachment through bio-behavioral
feedback between parental OT and parental behaviors, between
parental behaviors and infants' OT expression, and between infants'
OT and lifelong capacity for social afliation and stress management
[14]. There is some evidence that this may result in transgenerational
effects of OT through epigenetic mechanisms [7].
In a limited number of human studies, maternal plasma oxytocin
release was found to be stimulated by newborns' hands and mouths
touching their mothers' breasts in preparation for the rst breastfeeding and during breastfeeding [22]. SSC and the consequent
increase in OT may also contribute to the fact that breastfeeding
behavior is correlated to decreased levels of adrenocorticotropic
hormone (ACTH) and cortisol in mothers of full-term infants [23].
At 46 months post-partum, OT has been found to be involved in
motherinfant and fatherinfant attachment and well-adapted
parenting [24]. Our ndings of OT release in response to SSC
between both motherinfant and fatherinfant in the NICU are
consistent with and extend previous studies. Nonetheless, there
has been a controversy in the literature regarding a direct relationship between brain and peripheral levels of OT because they
may be regulated differently [25]. The peripheral OT is usually
405
Acknowledgments
This study was supported by the American Nurses Foundation
(Eastern Nursing Research Society and Pediatric Nursing Society) and
University of Connecticut School of Nursing Toner Fund.
406
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