Background
Every year, approximately 15 million babies are born preterm (gestational age (GA) less than 37 weeks), and more than 60% of these preterm births occur in Africa and South Asia [
1]. China ranks second in the top 10 countries with the greatest number of preterm deliveries [
2]. According to the National Health and Family Planning Commission of the People’s Republic of China, preterm births account for approximately 7.0% of the total births in China, and they are the main cause of infant mortality [
3]. Although the survival rate of preterm infants has increased because of the recent advances in neonatal care, premature births can cause varying degrees of adverse long-term neurodevelopmental impairment, which burdens both the family and country [
4].
Preterm birth interrupts the normal process of brain maturation, putting infants at great risk of neurodevelopmental vulnerability and fragility [
5]. During the third trimester, brain volume increases approximately 2.7-fold from 29 to 41 weeks postconception, which means that very preterm infants have a significantly smaller total brain volume than their term-born peers [
6]. These reductions persist throughout childhood and adolescence [
7]. Regional brain volumes near term are a promising marker for predicting disturbances in cognitive and behavioral outcomes in preterm infants [
8]. Moreover, newborns must be exposed to the extrauterine environment in the neonatal intensive care unit (NICU) while the immature preterm brain is not yet ready to process various stimuli, including lights, noise, and painful interventions [
9]. The infants’ sensory experience before term may cause negative effects on brain development and alter brain function and structure [
10,
11].
Among those adverse stimuli, painful invasive procedures are the prominent experience that infants must undergo within the context of the NICU. Evidence shows that preterm infants experience a median of 10 painful procedures per day during hospitalization, 79.2% of which occur without specific analgesia [
12,
13]. Unrelieved repeated pain exposure is associated with subsequent alterations in pain sensitivity, which may result in deleterious consequences including emotional, behavioral, and learning disabilities [
14].
Nevertheless, preterm infants’ developmental outcomes appear to be modified by improving the NICU environmental experience and providing neuroprotective caregiving practices, as supported by the concept that the young brain has the ability of neuroplastic response [
9]. This considerable plasticity of the brain can be expected at approximately 3 months before term age [
15]. These critical and sensitive periods of brain development can create “windows of opportunity” for NICU-based interventions that may be beneficial for neurodevelopment [
16].
Skin-to-skin contact, also known as kangaroo care (KC), is one of the recommended interventions to improve preterm birth outcomes according to the WHO [
17]. SSC is globally accepted under different circumstances. In low-income settings, SSC is ideally provided for 24 h/day as a health care strategy; in affluent settings, SSC is considered an alternative option to shorten the length of parent-infant separation [
18]. Regardless of how SSC is applied, multiple lines of evidence have suggested the short-term benefits of SSC for preterm infants. SSC has been used as a pain treatment to attenuate behavioral responses as well as to decrease cortisol levels. Studies found that Premature Infant Pain Profile (PIPP, a behavioral measure of pain for premature infants) scores and salivary and serum cortisol were lower on response to heel sticks in preterm infants who received SSC than in those who were treated with incubator care [
19,
20].
Furthermore, infants who received SSC were found to have more organized sleep patterns, with longer periods in the alert wakefulness and quiet sleep states [
21]. SSC infants showed a more mature neurodevelopmental profile [
21,
22] and scored higher on the Bayley Scales of Infant Development and Psychomotor Developmental Index at 6 months [
23]. In addition to these existing behavioral sleep findings, more rigorous neurophysiologic results measured by electroencephalographic/polysomnographic records also demonstrated that fewer rapid eye movements, more quiet sleep, and lower arousal were noted in SSC preterm infants than in the control cohort [
24,
25], indicating the effect of SSC on improving sleep organization and accelerating brain maturation. Because sleep is vital for normal development, SSC may be used as an intervention to promote better sleep patterns within the context of the NICU environment. In addition to the above benefits, it is acknowledged that SSC helps establish parent-infant attachment.
According to the regulation theory of Schore [
26], early maternal-infant separation can pose risk on attachment patterns, which is associated with alterations in brain structure and function. Research showed that very low birth weight (LBW) preterm infants with neurological impairment were more likely to develop an insecure quality of attachment [
27]. Maternal-infant interactions were less synchronous at 3 months [
28], and mothers of preterm infants were more likely to suffer from psychiatric illness (depression, anxiety) [
29], which contributed to adverse attachment outcomes [
30]. The physical closeness and sensory stimulations of SSC play an important role in regulating maternal-infant interaction. Evidence demonstrates that SSC can attenuate the negative psychological effects of premature birth by enhancing mothers’ sense of competence and sensitivity towards their infants, by decreasing mothers’ stress scores and increasing maternal-infant attachment scores [
31‐
33], and by facilitating a better maternal-infant interactive style [
34,
35].
Although it remains unclear whether SSC has long-lasting effects on preterm infants in terms of neurodevelopmental outcomes, studies show that KC may have a direct effect on infant neurophysiological organization [
23]. Long-term follow-up studies have found that KC preterm infants show attenuated stress responses, have organized sleep and better cognitive control, and maintain long-lasting social and behavioral protective effects even after 10 and 20 years [
36,
37].
KC has been recognized as an evidence-based intervention to improve health outcomes for LBW/preterm infants; however, it is not common in China. According to the national policy in China, parents are not allowed to enter the NICU to stay with their infants. Parent-infant separation begins after delivery until the infant is discharged, which accounts for a long period of time. This model of NICU care is accepted because it avoids the incidence of infection and also because of the ease of managing the patients. For severely ill infants, one of the preventive measures is to reduce the incidence of infection, which should be addressed by professionals. However, for medically stable preterm infants, a meta-analysis showed that LBW infants who received KC had reduced incidence of mortality, nosocomial infection, and severe illness compared to those who did not receive KC [
38]. These results also support the idea that parents entering the NICU wards did not increase the risk of LBW infants becoming infected [
38,
39]. Furthermore, the concept of family-centered care (FCC), which allows parents to participate in taking care of the baby, has been increasingly considered an important component of the NICU [
40]. Evidence shows that FCC is feasible and safe, and it does not increase the rates of nosocomial infection; the incidence of necrotizing enterocolitis (NEC) was significantly lower in the FCC group in previous studies [
41,
42]. These results indicate that allowing parents to visit their infants and perform SSC with adequate hygiene practice is safe, and it could be applied in Chinese NICUs.
According to the definition of KC, the mother is the optimal provider for SSC, to promote breastfeeding. However, in China, women are encouraged to stay at home and to rest completely for 1 month after birth (called “doing the month”) for recovery [
43]. These traditional postpartum practices are accepted regardless of a woman’s age and education [
44]. This resting period results in mothers not being able to perform even one or a few hours’ session of SSC per day after discharge from the hospital, which will greatly delay mother-infant exposure in the first month. In this case, father-infant SSC is an optimal alternative.
Whereas most studies focus on the effects of maternal-infant SSC, few studies have researched the father’s participation in SSC. Ludington-Hoe et al. and Erlandsson et al. found that infants who received father-infant SSC maintained higher skin temperature and had better state behavior responses [
45,
46]. In addition, no negative effects were observed on the metabolic rate and energy balance in performing paternal SSC [
47,
48]. Evidence also suggested that, to some extent, father-infant SSC was capable of decreasing pain response in preterm infants [
49‐
51]. Infants who received KC cried less, and fathers communicated more vocally not only with the newborn but with the mother. Fathers who provided SSC were more willing to be involved in infant care [
52], which established bonding and attachment [
53] with the infant and created a more stimulating, more harmonious, and generally better family environment [
54] beneficial for infant development [
23]. Qualitative studies also reported that fathers felt grateful for being needed; they also felt more included in the process, which facilitated their attainment of a paternal role and achievement of equal parenthood [
55‐
58].
As mentioned previously, premature birth can be stressful and traumatic for parents and can cause negative consequences for the natural establishment of the parent-infant relationship. The NICU environment interrupts parental involvement in caring for the infant and jeopardizes the process of attachment between parents and infant. It is recognized that fathers play an important role in the care of their children. Positive father-child interactions established at an early age have been shown to reduce cognitive delay in infants [
59]. A father’s involvement is associated with improved cognitive outcomes in preterm infants, which may suggest a possible intervention [
60]. Studies show that fathers of preterm infants often feel stressed [
61], overwhelmed, isolated, and out of control [
62]. Parental psychological well-being and parent-child interaction may affect infants’ development outcomes. However, these negative feelings appeared to be relieved by offering SSC, as fathers reported feeling in control and at ease when they were more involved in caring for their infants. By providing SSC, fathers consider themselves an important part in the course of caring for infants through physical closeness [
55].
The aim of the present study is to investigate whether paternal SSC is safe and how it affects outcomes for moderately preterm infants born at GA 320–346 weeks. We hypothesize that the practice of father-infant SSC in the NICU is feasible and will benefit both infants’ and fathers’ well-being.
Discussion
The design, outcome measures, sample size calculations, and procedures of this study protocol on paternal-infant skin-to-skin contact (SSC) for moderately preterm infants are in accordance with the Standard Protocol Items: Recommendations for Interventional Trials (SPIRIT) 2013 statement for clinical trial protocols (see Additional file
2).
KC is recognized worldwide as an evidence-based care method for preterm and/or LBW infants. The key component of KC is SSC between the baby and the mother. To improve preterm birth outcomes, the WHO recommends that KC should be provided as routine care for newborns weighing 2000 g or less at birth; the WHO also recommends that KC should be initiated in health care facilities as soon as the newborns are clinically stable [
17]. Among 10 countries with the greatest number of preterm births, China ranks second; in China, approximately 1,172,300 preterm infants were born in 2010 [
2]. However, practices in the NICU vary from province to province, and they depend on differences in economic status. Hence, practice is a factor that may have an essential influence on the scale-up and adoption of KC in China.
Generally, discharging vaginal and cesarean birth mothers on the third and seventh postpartum day, respectively, is the standard procedure. For vaginal birth mothers before discharge, performing KC in the NICU is still feasible if the mother is in good health. For cesarean births, mothers are not prepared to offer KC because of the surgical incision on their abdomen. Furthermore, women are encouraged to rest indoors for a month (“doing the month”) after giving birth to help facilitate postpartum recovery to improve future health and prevent diseases. Although “doing the month” has some negative effects, many Chinese women adhere to this conventional practice regardless of age and education [
43,
44,
76]. Consequently, implementing early and continuous KC for preterm infants in the NICU encounters additional setbacks after the mother is discharged.
However, fathers can also perform KC for infants, whether in the hospital or after discharge. According to the definition of KC, the mother is the optimal provider of KC because SSC between mother and infant is the basis of early successful and exclusive breastfeeding [
77,
78]. Nevertheless, the father and even other family members are suggested to perform KC while the mother is not available. Evidence shows that the father plays a significant role in infant care. Findings from previous studies show that fathers who provide SSC induce pain alleviation, paternal-infant attachment, and family bonding and create a more harmonious caregiving environment [
55,
57,
79,
80], which can be beneficial to infants’ development. However, studies on fathers providing SSC remain limited in China; thus, the effects of paternal SSC on both preterm infants and fathers have not been well studied.
This study aims to investigate the safety and effects of paternal SSC on neurodevelopmental outcomes in preterm infants. The data gathered in this study can be used to promote the implementation of early paternal SSC in the NICU and modify guidelines and procedures to facilitate the involvement of fathers in caring for their preterm babies when mothers are absent.
Trial status
The study is currently recruiting participants, and the first participant was recruited in September 2017. The official retrospective registration number of the study is ChiCTR-IOR-17012745. The entire study is expected to be completed by the end of December 2019.