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Early Human Development 91 (2015) 401406

Contents lists available at ScienceDirect

Early Human Development


journal homepage: www.elsevier.com/locate/earlhumdev

Parental oxytocin responses during skin-to-skin contact in


pre-term infants
Xiaomei Cong a,, Susan M. Ludington-Hoe b, Naveed Hussain c, Regina M. Cusson a, Stephen Walsh a,
Victoria Vazquez a, Carrie-Ellen Briere d, Dorothy Vittner a
a

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
d
Connecticut Children's Medical Center, University of Connecticut School of Nursing, United States
b
c

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.

known about paternal stress and anxiety when the newborn is


premature.
Skin-to-skin contact (SSC, or Kangaroo Care), has been shown to
reduce parental stress and anxiety, but the bio-behavioral mechanism
involved are still not well known [4]. Oxytocin (OT) release has been
suggested as one of the mediators for these effects and it seems to be
critical for optimal parenting of pre-term infants [5]. OT is a mammalian
neuropeptide which was originally thought to be a female hormone
because of its important roles in birth and lactation. However, the
function of the oxytocinergic system has been recently found to play a
key role in attachment bond formation and parenting across all
mammalian species in both females and males [6]. OT is produced
primarily in the supraoptic nucleus and paraventricular nucleus (PVN)
of the hypothalamus and is released within the brain both from
parvocellular neurons originating in the PVN and from dendrites of
magnocellular PVN neurons [5]. OT bers reach the amygdala, the

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X. Cong et al. / Early Human Development 91 (2015) 401406

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.

X. Cong et al. / Early Human Development 91 (2015) 401406


Table 1
Study conditions and procedures.
Study Phases
Time (pm)
Parental Data
(mother or
father)

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

2.3. Outcome measurements


2.3.1. Salivary oxytocin assay
Batched assays of salivary cortisol were done using enzyme
immunoassay (EIA) kit from Salimetrics (State College, PA). This
OT assay method is similar to that specically developed and validated
for salivary OT by Carter et al. [18]. A required extraction step as
described in the OT kit manual concentrated the saliva sample 3.2
times. Then, OT levels in extracted saliva were measured using the OT
EIA and samples from the same subject were kept in the same batch
to eliminate within subject inter-assay variance. The sensitivity limit
of the assay without correcting for the concentration was 11.7 pg/mL
and the lower limit of sensitivity was 2.0 pg/mL with correction for
the extraction process. The intra- and inter-assay variations for this
assay were 4.8% and 8%, respectively. Assay Designs reports crossreactivity for similar neuropeptides found in mammalian sera to be
0.001%.
2.3.2. Salivary cortisol
Batched assays of salivary cortisol were done using enzyme
immunoassay (EIA) kit from Salimetrics (State College, PA). On the
day of analysis, thawed saliva samples were centrifuged at 3000 rpm
for 15 min before assay. Detection limit of this assay was b0.007 g/
dL. The average intra- and inter-assay coefcients of variation were
4.13% and 8.89%, respectively. Any samples exceeding limits of the standard curve were reanalyzed after dilution. Samples were tested in duplicate and the average of the duplicates for each sample was used in the
analysis. All samples from an individual were run in the same assay
batch to eliminate within subject inter-assay variance.
2.3.3. Parental anxiety
A validated 8-item visual analog scale (VAS) was used to measure
parental emotional responses including anxiety, irritability, depression,
uselessness, relaxation, happiness, certainty, and closeness [19]. Each
VAS item consists of a 100-mm line preceded by a statement, such as
I have been very worried and anxious. The end points of each VAS
line are indicated by statements, such as from not at all to worse
than I have ever been before. High VAS scores thus indicated more
negative responses. The instrument has been tested in women during
pregnancy and post-partum and shown to be sensitive to changes
over time after childbirth [19]. In current study, the mother or father
was asked to mark the extent to which that statement had been
true in the previous 24 h before SSC, 30-min during-SSC, and 30-min
post-SSC.
2.4. Data analysis
Data were analyzed using IBM SPSS Statistics 20.0 (Armonk, NY).
Data on pre-, during-, and post-SSC phases were combined across the
two sequences of SSC (M-SSC followed by P-SSC or P-SSC followed
by M-SSC). Combining data in this way reected a decision not to
investigate order effects that could occur within the study's crossover
design. Evidence in the literature implies that the 24-hour separation

Twenty-eight infantmotherfather triads were recruited in the


study. Parents of two infants did not provide either M-SSC or P-SSC to
their newborn after recruitment, and the reason was unknown. In
the nal sample of 26 triads, 14 triads were randomized to sequence 1
(M-SSC on day-1 and P-SSC on day-2) and 12 triads were in sequence
2 (P-SSC on day-1 and M-SSC on day-2). Twenty-six mothers and 19
fathers completed the study protocol (Table 2). The majority of parents
were white (77% of mothers; 68% of fathers) and with college or higher
education (62% of mothers; 79% of fathers). Six-nine present of
mothers and 53% of fathers had M-SSC or P-SSC experience since the
infant's birth before they participated in the study.
3.2. Maternal and paternal oxytocin responses
Maternal oxytocin levels were signicantly increased from baseline
(50.49 20.05 pg/mL) to during-M-SSC (57.95 25.07 pg/mL), and
then dropped in post-M-SSC phase (51.50 24.13 pg/mL), F(2, 50) =
4.27, p b 0.05 (Fig. 1). Paternal OT levels were also signicantly
increased from baseline (41.25 25.74 pg/mL), to during-P-SSC
(49.78 25.39 pg/mL), and continued to maintain at a higher level
during post-30 min of P-SSC (50.10 31.50 pg/mL), F(2, 36) = 4.52,
p b 0.05 (Fig. 1). Paternal OT levels at pre-P-SSC were signicantly
higher in fathers who had previous P-SSC experience with the same
infant than fathers who had no P-SSC experience prior to the study,
50.40 21.66 vs. 19.67 6.35 pg/mL, t(17) = 2.55, p b 0.05.
Table 2
Characteristics of study participants (N = 26 infantmotherfather triads).
Parent characteristics

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

Note: GA = gestational age; PNA = post-natal age; M-SSC = maternal skin-to-skin


contact; P-SSC = paternal skin-to-skin contact.

404

X. Cong et al. / Early Human Development 91 (2015) 401406

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.

3.3. Maternal and paternal cortisol responses


Maternal cortisol levels were signicantly decreased from baseline (0.15 0.12 g/mL) to during-M-SSC (0.12 0.10 g/mL),
and continuously dropped in post-M-SSC phase (0.10 0.07 g/mL),
F(2, 50) = 4.15, p b 0.05 (Fig. 2). Paternal cortisol levels were signicantly
decreased from baseline (0.30 0.29 g/mL), to during-P-SSC (0.24
0.19 g/mL), and then increased during post-P-SSC (0.45 0.62 g/mL)
(Fig. 2), F(2, 36) = 4.55, p b 0.05. Additionally, data showed that
parental cortisol levels were signicantly correlated at baseline of preSSC phase in motherfather dyads, r = 0.78, p b 0.05.
3.4. Maternal and paternal anxiety measures
Mothers' anxiety levels were signicantly decreased from baseline
(24.31 26.25) to during-M-SSC (5.85 11.75), and then returned
to the baseline levels of anxiety in post-M-SSC (23.35 26.28),
F(2,50) = 11.29, p b 0.01 (Fig. 3). Fathers' anxiety levels were signicantly decreased from baseline (19.98 21.22) to during-P-SSC
(5.80 6.85), and then increased post-P-SSC (9.81 15.95),
F(2, 36) = 9.15, p b 0.01 (Fig. 3). Maternal and paternal anxiety levels
(VAS scores) were signicantly correlated at pre-SSC (r = 0.61,
p b 0.05), during-SSC (r = 0.48, p b 0.05), and post-SSC (r = 0.71,
p b 0.01), in motherfather dyads.
4. Discussion
To the best of our knowledge, the present study is the rst to
report parental salivary OT and cortisol levels and anxiety/stress
0.68

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

X. Cong et al. / Early Human Development 91 (2015) 401406

released in the posterior pituitary and enters the circulating


blood stream via this route. However, it appears that central and
peripheral releases of OT tend to be triggered in a coordinated
manner and this may explain the correlation with salivary OT levels
[18]. Because a direct demonstration of CNS and peripheral OT level
changes is not possible with human studies, we have to rely on
indirect measures of peripheral levels of OT as demonstrated in
our study. The rise in OT demonstrated in our study raises the possibility that SSC provides multi-sensory stimulation to the infant
parent dyads that not only activates the central brain nuclei but
also inuences circulating neuroendocrine signals.
Although OT is considered as an important component of the
neuroendocrinology of fatherhood, OT's role in the development of
human paternal behavior is not well understood. OT has been found
to be associated with fatherinfant affect synchrony in a social context
[26]. Recent studies showed that fathers who had intranasal OT
administration were more stimulating of their toddlers' exploration
and parentchild social behaviors [24]. Fathers in the present study
showed OT responses that were similar to the mothers in that their
salivary OT levels signicantly increased during 30 min P-SSC. Of
particular interest is the observation that paternal OT levels were
sustained at a higher level during 30 min post-P-SSC whereas maternal
OT dropped during post-M-SSC stage. Another compelling nding
is that paternal OT levels at baseline (pre-P-SSC) were signicantly
higher in fathers who had previous P-SSC experience with the same
infant than in fathers who had no P-SSC experience before our study,
however, this nding was not demonstrated in mothers.
The reasons for the differences between maternal and paternal
responses are unknown and point to some possibilities that warrant
further research. One explanation may be that the effects of touch on
OT response and parenting operate through different neuroendocrine
pathways in mothers and fathers. Another explanation may be based
on the observation that mothers experience pulsatile OT release during
M-SSC similar to during breastfeeding [23], but fathers may not.
Maternal breast milk pumping and timing of pumping may also potentially interact with OT and cortisol levels in mothers. Preparing for and
operating physical pumping can be effective in elevating maternal OT
levels and increasing prolactin release during the pumping, as well,
salivary cortisol concentrations have been found to be negatively
correlated with prolactin, but not with OT [27]. Although males lack
pregnancy-related hormones to facilitate paternal care, both animal
and human studies showed that paternal holding and contact with
infants can trigger multiple hormonal responses including increases
in prolactin, vasopressin, and OT levels and decrease in testosterone
values, thus supporting fathering behaviors [28,29]. The neurohormonal mechanisms underlying the difference in the post-SSC
effects between motherinfant and fatherinfant also need further
investigation.
Mothers and fathers of pre-term infants in the NICU experience
high levels of stress, distress, anxiety, as well as depressive symptoms
[30]. There is insufcient evidence to date for the best methods to
effectively treat the negative consequences of prematurity and early
persistent parental separation from infants. M-SSC has shown benecial
effects in reducing infants' stressful responses, including lower infant
serum and salivary cortisol levels [10]. There is also co-regulation of cortisol levels between motherinfant dyads during M-SSC, decreasing salivary cortisol in mothers [11]. M-SSC thus facilitates short and longterm motherinfant interactions and reduces maternal anxiety [31].
There have been no previous studies on the effect of P-SSC on paternal
stress and anxiety.
The present study results are consistent with and extend previous
studies on the positive effects of SSC in both mothers and fathers.
Specically we have demonstrated that 30 min of SSC with pre-term
infants effectively lowered salivary cortisol levels in both mothers
and fathers; and at 30 min of post-SSC, maternal cortisol continuously
dropped, but paternal cortisol signicantly increased. Meanwhile,

405

mothers' and fathers' self-reported anxiety levels signicantly


decreased during-SSC from baseline, and then increased at post-SSC
stage.
The observation that parental cortisol and anxiety responses
corresponded to the OT changes at pre-, during- and post-SSC stages
suggests that OT release in response to SSC may modulate the
autonomic nervous and stress-regulation systems and buffer
parental responses to stressors and anxiety. Such a relationship
was suggested by one study which showed that a longer duration
of SSC preceding sucking was associated with lower cortisol and
ACTH levels in breastfeeding mothers, suggesting that OT may be
involved in stress regulation [23]. One central nervous system
mechanism may be that, after OT is released from nerve terminals
in brain areas the corresponding high oxytocinergic activity can
decrease the activity within the HPA axis and can be stress relieving
and anxiolytic in animals and humans especially when OT is
inuenced by social behaviors [5,32]. OT released in the central
nervous system not only decreases release of corticotropin in the
PVN and inhibits release of ACTH in the anterior pituitary but also
circulating OT released via the posterior pituitary into the blood
stream seems to inuence the release of cortisol by a direct effect
on the adrenal cortex [33]. During M-SSC and P-SSC, OT plays a key
role in modulating maternal and paternal stress responses and
anxieties.
Another interesting nding is that motherfather stress and
anxiety responses seem synchronized and their baseline cortisol
levels along with anxiety measures were signicantly correlated
at pre-SSC, during-SSC, and post-SSC stages in motherfather
dyads. During the transition to parenthood, a mother's and father's
co-parenting support and behaviors have been found to develop a
synchrony with the spouse's interaction with the infant and OT
levels may inuence parental motivation between the two [34].
Similarities have been shown between OT levels in mothers and
fathers and OT was correlated with the degree of proximity and
affectionate contact between all members of the family system,
spouses and parentschildren [34]. Paternal post-partum depression has been also signicantly correlated with and predicted by
maternal depression [35]. Therefore, interventions to promote
pre-term infant health need to cover the whole family process,
including the mother, father and infant, and to highlight the role of OT
along with maternal and paternal touches during the initial stage of
family development.
In summary, both M-SSC and P-SSC activated OT release and
reduced stress and anxiety responses in mothers and fathers of
pre-term infants. However, generalization of these ndings may be
limited because of small sample size. Nonetheless, parental touch
during the early life period is critical for an infant's growth and
survival and also for parenting development. The present study
lends support to the involvement of an OT-related mechanism in
neuroendocrine pathways during parentinfant contact and human
parenting. This study lends further physiologic support to the positive role of SSC in the early post-partum period and more studies
are especially needed to investigate effects of P-SSC and its underlying mechanisms on infantfather interactions.

Conict of interest statement


None.

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

X. Cong et al. / Early Human Development 91 (2015) 401406

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