Positive Effects of Kangaroo Mother Care on Long-Term Breastfeeding Rates,Growth,and Neurodevelopment in Preterm Infants

Abstract

Background and Objectives:

Kangaroo mother care (KMC) benefits preterm infants' health through increasing breastfeeding, but the longitudinal effects of KMC remain unknown. This study investigates the impact of KMC on breastfeeding and health outcomes in Chinese preterm infants.

Methods:

A longitudinal randomized controlled study was conducted with 79 preterm infant–mother dyads. The KMC group (n = 36) was provided 2.5 hours/day KMC during the neonatal intensive care unit (NICU) hospitalization, while the control group (n = 43) received standard care. Infant's feeding regimens and physical growth were documented daily at NICU. Physical growth and Neonatal Behavioral Neurological Assessment were measured at 40 weeks, 3 months, and 6 months of corrected age (CA). Breastfeeding outcomes were documented at 6 months of CA.

Results:

Compared with the control group, KMC infants received higher mothers' milk proportion during hospitalization (B = 0.16, confidence interval [CI] = [0.11–0.21]) and less feeding intolerance at discharge (odds ratio [OR] = 0.11, CI = [0.02–0.43]); and higher exclusive breastfeeding proportion (OR = 14.6, CI = [3.5–60.9]) at 6 months CA. KMC infants also had significant increased body weight and body length at hospital discharge; and more increases of body weight, body length, and head circumference in follow-ups. The neurobehavioral score was also higher in the KMC group compared to the control group over time.

Conclusions:

Longitudinal KMC effects are significant in promoting preterm infants' breastfeeding outcomes, growth, and neurodevelopment. Early initiation of KMC practice is highly recommended to the parent–infant population in Chinese NICUs to promote breastfeeding and developmental outcomes.

Introduction

Prematurity is the leading cause of neonatal mortality and prolonged hospital stay.^1,2 From 2015 to 2016, the preterm birth rate in China was 7.3% among all births and 6.7% of all live births.³ Preterm infants not only have an increased difficulty adjusting to the external environment at birth but also face a multitude of health obstacles growing up, including neurological immature,⁴ growth problems,⁵ and comorbidity such as feeding intolerance.⁶ Although breastfeeding in preterm infants has been one of the major interventions to promote health, the breastfeeding rate in China falls below the World Health Organization (WHO) goal of exclusive breastfeeding in the first 6 months up to at least 50%,⁷ for instance, only 22.5% of Chinese preterm infants received exclusively breastfeeding at 6 months.⁸

To enhance health outcomes of preterm births, interventions must be taken into consideration to increase breastfeeding. However, the current medical and health care models utilized in the neonatal care practice in China pose barriers to early mother–infant interaction and contact as well as breastfeeding initiation and practice. For instance, it is a common practice in Chinese neonatal intensive care units (NICUs) to deny the family visitations due to infection and other concerns. Separation between mothers and newborns during their NICU stay has a negative impact on breast milk production⁹ and long-term consequences on providing life-saving breastfeeding, establishing positive family interaction, and parent–infant bond.¹⁰

Skin-to-skin contact or kangaroo mother care (KMC) was developed in 1978 to help decrease the mortality and morbidity in low bodyweight and preterm infants.^11,12 Evidence suggests that the preterm infant lying prone on the mother's bare chest during KMC can promote earlier initiation of breastfeeding and breastfeeding success.^13,14 KMC has been also shown to improve in infant body length, head circumference, neurobehavioral performance, and other health outcomes.^13,15–18

Along with 40 years of development, Chinese NICUs have been equipped with advanced neonatal care technologies, environments, and medical and nursing staff, however, many of them still hesitate to include parents' infant care, such as KMC and direct breastfeeding.^9,19 Although numerous benefits of KMC on breastfeeding and health in preterm infants have been demonstrated in studies worldwide, it has not been examined and applied as a routine care in Chinese NICUs. Therefore, our study aimed to examine the impact of KMC on breastfeeding outcomes, physical growth, and neurobehavioral outcomes in Chinese preterm infants during hospitalization and postdischarge through 6 months of infant corrected age (CA).

Methods

Study design

A longitudinal randomized study was conducted to investigate the effects of KMC on infants' feeding, growth, and developmental outcomes during the NICU hospitalization, at discharge, and 3 and 6 months follow-ups. The study was approved by the Medical Ethics Committee of Beijing Obstetrics and Gynecology Hospital, Capital Medical University (protocol #2017-KY-008-01) and was conducted in accordance with the Consolidated Standards of Reporting Trials statement (Fig. 1). Informed consents were obtained from the infants' mothers to participate in the study. The infant–mother dyads were assigned to either the KMC or the control group using a simple randomization method with a computer-generated random number table used. The data collectors/research assistants who did the chart reviews and phone interviews were blinded to the study group allocation.

FIG. 1.

Flow diagram of the recruitment and randomization process.

Setting and participants

The study was conducted in the NICU of Beijing Obstetrics and Gynecology Hospital, which is one of the largest maternal and child health centers in China. This NICU provides the highest level of neonatal care for infants and their families, with range of 450–500 admissions per year. Preterm infants and their parents were recruited using convenience sampling.

Inclusion criteria of the participants were preterm infants who were (1) 33 0/7 to 35 6/7 weeks gestational age at birth; (2) with no known congenital anomalies; (3) with no respiratory difficulties; and (4) mother was ≥18 years of age and Chinese speaking. Exclusion criteria of the participants were infants who had severe or critical illness, including congenital anomalies, severe periventricular/intraventricular hemorrhage, or minor or major surgery.

The sample size was estimated based on the results from Cong et al.²⁰ by G*power software 3.1.9.6. With a two-sided type-I error of 0.05 and an effect size of 0.81, 25 infants in each group were needed to provide 80% power to detect the differences between the two groups. The sample size was increased to total 79 to account for potential dropouts.

KMC intervention and control condition

KMC intervention

The infants in the KMC group received 2.5 hours/day KMC during NICU stay. The KMC room in the NICU was equipped an independent bath room and electrocardiogram monitors. Before starting KMC, one research nurse assessed the infant's vital signs and changed his/her diaper. The mother was required to clean her breast and wear a front opening gown provided by the hospital. The mother sat in a recliner, and a diaper-clad infant was placed on his/her mother's chest, skin-to-skin, in a prone and upright position with head angled at a 30–40° incline.²¹ The mother was encouraged to perform direct breastfeeding to her infant during KMC.

Control condition

The study NICU has a visitation restriction policy that is commonly applied in the majority of NICUs in China, where parents or any other visitors are not allowed to visit the infants until discharge to prevent infection or other complications. Therefore, our control group was only provided with standard care according to the NICU policy.

Measurements

Demographics and characteristics

A questionnaire with 26-items was developed by researchers to measure maternal sociodemographic, breastfeeding background and plan, maternal knowledge resources, and infants' characteristics.

Breastfeeding self-efficacy and knowledge

The Chinese version of the Breastfeeding Self-Efficacy Scale-Short Form (BSES-SF)²² was used to collect data of mothers' breastfeeding background and feeding plan at NICU admission.

Breastfeeding outcomes at NICU stay

Infant feeding data, including daily intake of breast milk (mL) and formula (mL), were retrieved from the nursing care chart by research nurses during NICU stay. For the infants who received direct breastfeeding, the body weight was measured before and after each feeding to calculate the amount of breast milk intake. The infant might be given an extra amount of formula if his/her mother had low breast milk supply, to meet the preterm infant's daily nutritional requirements.

Feeding intolerance at NICU stay

Gastric residual volume (GRV) was evaluated before the next feeding through nasal-gastric tube if applicable, and was documented during each shift by the NICU nurse. According to the NICU protocol, the feeding intolerance was diagnosed when GRV was more than 50% of previous feeding volume or more than 2 mL/kg body weight daily, infant vomiting, and/or abdominal distension (abdominal girth >1.5 cm).²³ Data of infant feeding intolerance were retrieved and documented by the research nurses daily at NICU discharge.

Feeding outcomes at follow-ups

After discharged from the NICU, the infant–mother dyad was followed by a phone interview at 6 months CA. The mother was assessed by recalling her breastfeeding practice within the past 24 hours using a questionnaire developed by Wang et al.⁸ Three types of feeding were defined based on the WHO guideline.²⁴ (1) Exclusive breastfeeding was defined as feeding completely with human milk; (2) exclusive formula feeding was defined as feeding completely with formula; and (3) mixed feeding was defined as feeding mixed with both human milk and formula. The proportion of human milk or formula was documented and analyzed by research nurses.

Infant physical growth

Each infant's weight was measured and documented at birth, daily in the morning shift of the NICU stay, and at discharge. Infant length and head circumference were also measured at birth and at discharge. After discharge, parents brought infants to outpatient settings for follow-up appointments at 40 weeks, 3 months, and 6 months CA. The follow-up data of infant weight, length, and head circumference were obtained by research nurses in the outpatient office.

Infant neurobehavioral development

The impact of both KMC and breastfeeding on neurobehavior development was evaluated by the Neonatal Behavioral Neurological Assessment (NBNA) scale, which is based on Amiel-Tison Neurological Assessment at Term and then formulated by Bao et al.²⁵ and Gosselin et al.²⁶ Stability and reliability of the measuring system were verified in preterm infants to predict their future risk of behavioral problems.^25,27 The Chinese version of the NBNA²⁸ was applied in this study, which includes two scales, Scale One for the measurement at the neonatal stage and Scale Two for the postneonatal stage to 6-year-old of Chinese children. The newborn scale (Scale One) includes behavior (six items), passive tone (four items), active tone (four items), primary reflexes (three items), and general assessment (three items).²⁸ A score of 0–3 is assigned to each item, and the total score ranges from 0 to 40 accordingly.²⁸ A testing score is equal or less than 37 will be considered abnormal. The newborn scale was used in our study when the infant reached 40 weeks of CA. Scale Two of the NBNA assesses five developmental components: gross motor skill, fine motor skill, adaptive development, language skill, and social development. Levels of children's development are classified as advanced development (total score ≥130), high average (111–129), average (80–109), borderline of retardation (70–79), and retardation (<70). The NBNA Scale Two was used in the study when the infants reached 3 and 6 months of CA. Infants' developmental outcomes were assessed and evaluated, and the NBNA scores were documented by a licensed rehabilitation therapist in the outpatient setting of the study site.

Data collection procedures

Demographic data, health characteristics, and previous breastfeeding experience were obtained from the infant's medical record through an interview with the mother at enrollment of the study. Both study groups received standard NICU care during their hospital stay; meanwhile, in the KMC group, the mother provided daily 2.5 hours of KMC when she was physically or mentally ready. The research nurses obtained the daily data of infants' weight (g) and breast milk and formula intake (mL) through chart review during NICU stay. At 40 weeks, 3 months, and 6 months CA follow-ups, the data of infants' weight (g), length (cm), head circumference (cm), and NBNA scores were collected. At 6 months of CA, feeding outcomes (exclusive breastfeeding, formula, and mixed feeding) were gathered through telephone interviews by research nurses.

Statistical analysis

We performed statistical analyses using statistical package for the social science (IBM SPSS statistics) version 25 and R 3.6.3. Demographic data were analyzed using descriptive methods. Randomization of baseline variables and difference in outcomes of interest between the KMC and the control group was checked by two-sample hypothesis tests.

The proportion of breast milk during hospitalization was modeled by linear regression, adjusting for hospitalization days, birth weight, sex, gestational age, and birth type. Feeding intolerance at discharge was modeled by a logistic regression with the same adjusting covariates aforementioned. Feeding outcomes at the 6 months of CA were analyzed as an ordinal outcome with three levels, formula only, formula mixed with breast milk, and exclusive breastfeeding. We performed an ordinal logistic regression, controlling for sex, gestational age, birth type, and maternal characteristics, which were not randomized well in this study.

We performed the linear regression to model the effect of the KMC group on physical growth (weight, height, and head circumference) at discharge. Total hospitalization days, baseline body measurements at birth, sex, gestational age, and birth type were adjusted in each model. Longitudinal growth measurements at 40 weeks, 3 months, and 6 months CA were analyzed by the linear mixed model (LMM) using the R package “lmerTest.”²⁹ To model the heterogeneity in different infants, we added an infant-level random intercept in the LMM. We set group and time points as fixed effects in each model, and added body measurements at birth, sex, gestational age, birth type, and maternal characteristics, which were not randomized well in this study to control potential confounding factors. The longitudinal NBNA score was also analyzed by LMM with the same adjusting covariates as those in the analysis of longitudinal body weight. Statistical inference was performed by the t-test with Satterthwaite's approximated degree of freedom, which has a better type-I error control compared with other inference methods for LMM. The study was approved by the Institutional Review Board (IRB) of the study site.³⁰

Results

Demographic and maternal characteristics of the preterm infants

A total of 85 dyads of eligible preterm infants and their mothers were enrolled in the study and six dyads were withdrawn from the study due to mothers' health conditions. More than half of the infants were female and delivered by cesarean section (Table 1). There were no significant differences in infants' demographic characteristics between the two groups, except that birth weight was higher in the control group than the KMC group. Maternal characteristics were similar in the two groups except for mother's age, self-confidence of enough breastfeeding, occupation, and family location (Table 2). Therefore, these factors were added as adjusting covariates in the LMM for longitudinal body measurements and NBNA scores.

Table 1.

Demographic and Health Characteristics of Preterm Infants at Baseline

Demographic variables	Control group, n (%)	KC group, n (%)	p
Gender of infants
Female	25 (58.14)	22 (61.11)	0.789
Male	18 (41.86)	14 (38.89)	0.789
Birth type
C-section	30 (69.77)	23 (63.89)	0.580
Vaginal	13 (30.23)	13 (36.11)	0.580
Gestational age
33 Weeks	6 (13.95)	6 (16.67)	0.313
34 Weeks	13 (30.23)	16 (44.44)
35 Weeks	18 (41.86)	8 (22.22)
36 Weeks	6 (13.95)	6 (16.67)
Birth plurality
Singleton	25 (58.1%)	26 (72.2%)	0.192
Twin	18 (41.9%)	10 (27.8%)	0.192

	Mean ± SD	Mean ± SD
Birth weight (g)	2196.05 ± 236.91	2096.25 ± 209.62	0.051
Birth length (cm)	45.02 ± 1.93	45.11 ± 2.11	0.849
Birth HC (cm)	31.34 ± 0.95	31.18 ± 0.9	0.433

HC, head circumference; KC, kangaroo care; SD, standard deviation.

Table 2.

Maternal Characteristics of Preterm Infants

Maternal variables	Control group, n (%)	KC group, n (%)	p
Gravidity
At least one	17 (39.53)	18 (50)	0.351
Zero	26 (60.74)	18 (50)	0.351
Parity
At least one	7 (16.28)	12 (33.33)	0.077
Zero	36 (83.72)	24 (66.67)	0.077
No. of delivery
Delivered baby before	8 (18.6)	13 (36.11)	0.079
First time	35 (81.4)	23 (63.89)	0.079
Ethnicity
Han	39 (90.70)	34 (94.44)	0.683
Minority	4 (9.30)	2 (5.56)	0.683
Education
Above bachelor degree	26 (60.47)	26 (72.22)	0.273
Below associate degree	17 (39.53)	10 (27.78)	0.273
Occupation
Full time job	22 (51.16)	29 (80.56)	0.007^*
Housewife or jobless	21 (48.84)	7 (19.44)	0.007^*
Location
City	29 (67.44)	32 (88.89)	0.031^*
Suburban	14 (32.56)	4 (11.11)	0.031^*
Method of payment
Insurance	32 (74.42)	36 (100)	0.001^*
Self-pay	11 (25.58)	0 (0.00)	0.001^*
Comorbidity
Yes	16 (37.21)	16 (44.44)	0.514
No	27 (62.79)	20 (55.56)
BF background and plan
BF experience
Yes	6 (13.95)	8 (22.22)	0.338
No	37 (86.05)	28 (77.78)	0.338
Professional guidance
Yes	35 (81.40)	31 (86.11)	0.573
No	8 (18.60)	5 (13.89)	0.573
BF course
Yes	35 (81.4)	26 (72.22)	0.333
No	8 (18.60)	10 (27.78)	0.333
Planned BF method
Mixed or formula	21 (48.84)	14 (38.89)	0.375
Mothers' milk	22 (51.16)	22 (61.11)	0.375
Planned BF time
1–5 Months	10 (23.26)	4 (11.11)	0.238
At least 6 months	33 (76.74)	32 (88.89)	0.238
BF knowledge resource
Medical profession
Yes	26 (60.47)	29 (80.56)	0.053
No	17 (39.53)	7 (19.44)	0.053
Grandma's knowledge
Yes	8 (18.60)	11 (30.56)	0.216
No	35 (81.40)	25 (69.44)	0.216
Husband's knowledge
Yes	3 (6.98)	1 (2.78)	0.621
No	40 (93.02)	35 (97.22)	0.621
Internet
Yes	17 (39.53)	22 (61.11)	0.056
No	26 (60.47)	14 (38.89)	0.056
Journal or book
Yes	14 (32.56)	16 (44.44)	0.278
No	29 (67.44)	20 (55.56)	0.278
TV
Yes	7 (16.28)	6 (16.67)	0.963
No	36 (83.72)	30 (83.33)	0.963
	Mean ± SD	Mean ± SD
Mother's age	34.37 ± 4.5	32.08 ± 4.14	0.021^*
Confidence of enough BF	6.42 ± 2.67	7.58 ± 2.22	0.052

Significant difference (p-value < 0.05) denoted by ^*.

BF, breastfeeding; SD, standard deviation.

Comparison of feeding outcomes between the KMC and control groups

We visualized and compared the breast milk proportion during hospitalization, feeding intolerance at discharge, and feeding type at 6 months of CA between the two groups in Figure 2. Compared with the control group, the KMC group reported a higher proportion of breast milk intake (0.41 ± 0.13 versus 0.24 ± 0.15; p < 0.001) and lower risk of feeding intolerance at discharge (13.9% versus 37.2%; p = 0.020, odds ratio [OR] = 0.27, 95% confidence interval [CI] = [0.09–0.84]). At 6 months of CA, the KMC group had a significantly higher proportion (p < 0.001) of exclusive breastfeeding (46.9% versus 2.9%) and lower proportion of formula feeding (9.4% versus 42.9%) compared with the control group.

FIG. 2.

Comparison of the breastfeeding performance between the KMC and control groups. (A) Mothers' milk proportion during hospitalization. (B) Proportion of feeding intolerance at discharge. (C) Proportion of feeding types at 6 months CA. BF, breastfeeding; CA, corrected age; KMC, kangaroo mother care.

Comparison of growth and neurodevelopmental outcomes between the KMC and control groups

Infants in the KMC group had similar physical growth at discharge compared with the control group (Fig. 3). However, due to the nearly significant heavier birth weight in the control group, we still expected that the infants in the KMC group gained more weight than those in the control group. In addition, growth measurements at discharge were highly impacted by the body measurements at birth and hospitalization duration. Thus, we further analyzed the growth outcomes by linear regression controlled for these factors aforementioned. In terms of the body measurements in follow-up, the KMC group reported higher growth outcomes than the control group at 40 weeks, 3 months, and 6 months of CA. With respect to the neurological assessment of the infants, the KMC group performed higher NBNA score than the control group at 40 weeks (36.9 ± 1.0 versus 38.8 ± 0.6; p < 0.001), 3 months of CA (83.9 ± 4.6 versus 90.6 ± 1.8; p < 0.001), and 6 months of CA (85.1 ± 4.1 versus 91.0 ± 2.6; p < 0.001) as shown in Figure 3.

FIG. 3.

Comparison of physical measurements and NBNA score between the KMC and control groups over time. (A) Body weight. (B) Body length. (C) Head circumference. (D) NBNA score. KMC, kangaroo mother care; NBNA, neonatal behavioral neurological assessment. *p < 0.05; **p < 0.01; ***p < 0.001.

KMC effects on feeding, growth, and neurodevelopmental outcomes

The preterm infants in the KMC group had better breastfeeding performance at hospitalization as well as follow-up period (Table 3). At NICU hospitalization, the proportion of breast milk intake in the KMC group was estimated to be 16% (95% CI = [0.11–0.21]) higher than that in the control group. Meanwhile, the KMC group were 0.11 (95% CI = [0.02–0.43]) times less likely to have feeding intolerance at discharge than the control group. In follow-up, the KMC infants were 14.6 times (95% CI = [3.5–60.9]) more likely to have a better level of breastfeeding type than those in the control group at 6 months of CA.

Table 3.

Regression Models for Outcome Measurements at Discharge and in the Follow-Up Period

	B coefficient	95% CI	p
Breastfeeding performance
Mothers' milk proportion at NICU^a R²: 0.54
KC group	0.16	0.11 to 0.21	<0.001
Feeding intolerance at discharge^b
KC group	−2.23	−3.96 to −0.84	0.004
Feeding type at 64 weeks (CA)^c
KC group	2.68	1.25 to 4.11	<0.001
Physical growth measurement at discharge^a
Body weight (g), R²: 0.83
KC group	45.18	9.66 to 80.71	0.013
Body length (cm), R²: 0.93
KC group	0.74	0.47 to 1.01	<0.001
Head circumference (cm), R²: 0.74
KC group	0.20	−0.03 to 0.43	0.090
Physical growth measurement in follow-up^d
Body weight (g)
KC group	417.0	161.1 to 672.8	0.004
Body length (cm)
KC group	2.20	1.20 to 3.19	<0.001
Head circumference (cm)
KC group	1.28	0.92 to 1.64	<0.001
Neurodevelopment assessment in follow-up
NBNA score^d
KC group	4.29	3.21 to 5.37	<0.001

Linear regression controlled for hospitalization day, baseline measurement at birth, sex, gestational age, and birth type.

Logistic regression controlled for hospitalization day, birth weight, sex, gestational age, and birth type.

Ordinal logistic regression controlled for sex, gestational age, birth type, mother's age, mother's self-confidence of enough breastfeeding milk, mother's occupation, and family location.

Linear mixed model with subject random intercept, controlled for time point, baseline body measurements at birth, sex, gestational age, birth type, mother's age, mother's self-confidence of enough breastfeeding milk, mother's occupation, and family location.

CA, corrected age; CI, confidence interval; NBNA, neonatal behavioral neurological assessment; NICU, neonatal intensive care unit.

As shown in Table 3, the KMC group had better physical growth and neurological assessment at discharge as well as in follow-up. With respect to the physical measurements at discharge, preterm infants in the KMC group are estimated to be 45.18 g heavier (95% CI = [9.66–80.71]), 0.74 cm taller (95% CI = [0.47–1.01]), and 0.20 cm longer (95% CI = [−0.03 to 0.43]) in head circumference than those in the control group. In follow-up, infants in the the KMC group were estimated to be 417 g heavier (95% CI = [161.1–672.8]), 2.20 cm taller (95% CI = [1.20–3.19]), and 1.28 cm longer (95% CI = [0.92–1.64]) in head circumference over time than the control group. In addition, the KMC group was estimated to have 4.29 (95% CI = [3.21–5.37]) higher NBNA score over time compared with the control group.

Discussion

Our study focuses on the longitudinal impact of KMC in Chinese preterm infants, which is one of the first studies addressing KMC effects on feeding, growth, and developmental outcomes of mother–infant dyads in China. Even though KMC has been widely studied and practiced in many other countries, few studies have been conducted in China. Findings of our study demonstrated that KMC mothers provided more breast milk to their preterm infants at NICU stay and a higher proportion of exclusive breastfeeding at 6 months of CA. The current study contributes to the feasibility and efficacy of KMC in improving breastfeeding, growth, and development after birth through 6 months of CA in Chinese preterm infants.

Many mothers and their preterm infants worldwide face the challenge of increasing breast milk intake and success in breastfeeding in infants' early life. It may be more difficult for Chinese mother–infant dyads to encounter this obstacle, largely due to the culture and policy of limited visitation access in many NICUs in China.^9,31 Our study showed that providing 2.5 hours daily KMC to preterm infants during their hospitalization effectively improved breast milk intake, lowered the risk of feeding intolerance at NICU stay, and significantly increased exclusive breastfeeding rate at 6 months follow-up compared with the control group. These findings are consistent with previous studies and meta-analysis^13,14,17,32 and demonstrate that early maternal skin-to-skin contact with premature infants can stimulate the oxytocinergic system and facilitate breast milk production as well as mother–infant interaction and bonding.³³ The KMC effects were not only shown to be significant during the first couple of weeks of the infant's life at NICU but also effectively carried over to 6 months of CA follow-up in improving the exclusive breastfeeding practice in our study. The exclusive breastfeeding rate in our KMC group at 6 months of CA was 47%, approaching the 50% rate recommended by the WHO.²⁴ However, the standard care control group's exclusive breastfeeding rate was meager in the current study (3%), which is even much lower than that in our previous study in Chinese preterm infants and other studies in China.^8,34 The reasons may be associated with a long period of mother–infant separation during intensive care, high C-section birth rate, less previous breastfeeding experience, low level of breastfeeding self-efficacy, and lack of breastfeeding knowledge and resources.⁸ Changes to neonatal care protocols and policies are critically needed in Chinese NICUs to promote parent's visitation and increase early mother–infant skin-to-skin contact to improve breastfeeding outcomes.

Feeding intolerance is a common digestive issue in preterm infants that further interrupts infant feeding plan and increases hospital stay and even mortality.^6,35 Our study demonstrated that the rate of feeding intolerance at hospital discharge was significantly lower in the KMC group than the control group, which is consistent with a previous report showing that the upright KMC position could facilitate the feeding process and enhance the comfort level in preterm infants.³⁶ Early initiation of breastfeeding can also help meconium evacuation and contribute to decreasing the feeding intolerance, where increasing the mothers' milk intake in early life is one of the benefits of KMC.

KMC positively impacted infants' physical growth in our study, including better outcomes of body weight, length, and head circumference in the KMC group at hospital discharge and follow-ups. Suboptimal growth in early life may lead to adverse health outcomes, delayed brain development, and altered neurodevelopment.^5,37 Even though the baseline infant body weight was heavier in the control group than the KMC group before the initiating of the intervention in our study, KMC effectively promoted weight gain through infant NICU stay and continuously enhanced bodyweight for 6 months CA. These findings are consistent with previous randomized trials investigating the KMC effects on preterm infants' growth.^11,12,37 The mechanism can explain these effects that mother–infant skin-to-skin contact stabilizes the infants' body temperature, blood glucose level, and cardiorespiratory system and decreases the maternal and infants' stress.³⁸ Thus, KMC conserves infants' energy for growth and thriving.

Our study also revealed that infant neurobehavioral outcomes (NBNA scores) were better in the KMC group than the control group across all three follow-up visits. Preterm infants are subjected to numerous stressors during the NICU stay, including prolonged maternal–infant separation, daily stressful and painful experience, and hypoxia and infection, which result in a high risk of neurodevelopmental deficits and chronic mental illness later in life.³⁹ Our results are consistent with other findings that intensive, maternal involvement in infant care, such as KMC and breastfeeding, contributes to improved infants' neurobehavioral outcomes.⁴⁰ The underlying mechanisms of these KMC effects are through multisensory stimulation of skin-to-skin contact, touching, talking, and breastfeeding to facilitate the network building between the neurons within the infant's brain.⁴¹ Early mother–infant contact has been shown to facilitate infants' attention and emotion regulation,⁴² promote infants' language development and learning abilities, and increase the period of deep sleep⁴³ and alert wakefulness.⁴⁴ Importantly, increased breast milk proportion and breastfeeding were shown in the KMC group that effectively promoted early weight gain and head circumference increase and further resulted in better neurodevelopmental outcomes in our study, which are consistent with previous reports.⁴⁵ Mother's own breast milk are especially ideal for preterm infants' growth, immunity, and neurodevelopment.⁴⁶ The composition of mothers' milk, for example, macro-, micronutrients, hormones, immune components, and other metabolites has been found to be dynamically adjusted to support the infants' nutritional requirements along with different developmental phase to promote fast early brain maturation.⁴⁶ Prolonged breastfeeding also strengthens the mother–infant bond, decreases maternal stress, and activates hormone stimulation, therefore positively influences infant development.⁴⁷ Our study supports the KMC effects on mitigating adverse consequences of prematurity, mother–infant separation, and other environmental insults in early life along with promoting breastfeeding and neurobehavioral outcomes in this high-risk population.

Even though strong evidence supports the benefits of KMC in preterm health care, many barriers that hinder the implementation of KMC exist in China. One of the most common concerns is that family-integrated-care may increase the risk of infection in the NICU, although the previous study⁴⁸ as well as our current study showed that KMC was safe and infants in the KMC condition had no infection occurred. Other barriers of conducting KMC in China include lack of knowledge and experience of KMC, staff shortage, extra costs for providing KMC environment, lack of the trust relationship between the health care professional and the parents, transportation issues of the parents, Chinese culture of postpartum confinement, and policy concerns.⁴⁹ To overcome these obstacles and promote KMC practice in China, strategies are recommended to focus on providing KMC education and training to health care providers and parents, building trust and rapport between staff and families, and importantly, making policy changes of maternal and infant health care and developing culturally specific KMC protocols in China.

The limitation of our study includes that it was only conducted at one metropolitan hospital in northeast of China, which may hinder the generalization of our results to other settings. Another limitation is small sample size of the study and the simple randomization method used resulted in an unequal number of participants among two groups. Finally, data collection on feeding outcomes at 6 months of CA used the last 24 hours recalls, which may miss feeding information between the period of NICU discharge and 6 months of CA.

Conclusion

The results demonstrate that KMC is a feasible and effective intervention in the Chinese NICU to prevent feeding intolerance and promote breastfeeding, growth, and neurobehavioral outcomes over hospitalization and through 6 months of CA. Strategies to facilitate KMC practice and promote breastfeeding for Chinese preterm infants are demanded, both in the NICU and after discharge. Further research is also needed to investigate the longitudinal impact of early initial of KMC on maternal and infant health outcomes in China.

Footnotes

Acknowledgments

The study was supported by the NICU of Beijing Obstetrics and Gynecology Hospital, Capital Medical University in Beijing, China. The authors are pleased to acknowledge Dr. Stephen Walsh (School of Nursing, University of Connecticut), who provided statistic opinions to aid in the data analysis.

Authors' Contributions

Conceptualization, Y.W. and X.C.; Data Collection and management, Y.W., X.C., and S.L.; Data analysis, T.Z., Y.Z., and X.C.; Writing and editing: Y.W., T.Z., Y.Z., and X.C.

Disclosure Statement

No competing financial interests exist.

Funding Information

This study was funded by the Beijing Obstetrics and Gynecology Hospital, Capital Medical University (FCYY 201616; PI: Wang). IRB approval number was 2017-KY-008-01.

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