A randomized controlled trial of the effects of antenatal milk expression on breastfeeding among first-time mothers in China


 Background

Limited research outside China suggest that antenatal milk expression in late pregnancy (AME) may promote breastfeeding. A few studies have evaluated the safety and efficacy of AME in women with diabetes in pregnancy, little or no evidence exists to explore its effects on breastfeeding self-efficacy and early breastfeeding, particularly in first-time mothers. The objective of this study was to explore the effect of AME on breastfeeding for the first-time mothers during the postpartum hospitalization.
Methods

A randomized controlled trial was conducted in a tertiary hospital in Haikou, Hainan. We recruited pregnant women who had completed 37 weeks of gestation and randomly assigned them to either the intervention group (n = 45) or the control group (n = 45). The pregnant women in the intervention group were advised to rhythmic self-massage of breasts three times daily at any time. The control group was given routine midwifery and obstetric care. The breastfeeding self-efficacy scale(BSES)was used to measure the self-efficacy of breastfeeding at 37 weeks, 38 weeks and the third day postpartum. The time to lactogenesis II and the rate of exclusive breastfeeding was measured three times every day by the researcher in the ward.
Results

Compared with the control group, the intervention group had higher breastfeeding self-efficacy scores measured by the scale of BSES(P < 0.05), the intervention group had higher exclusive breastfeeding rate on the first day, second day, third-day postpartum, and the difference was statistically significant༈P < 0.05). The time to lactogenesis II in the intervention group was earlier than that in the control group(P < 0.05).
Conclusions

Antenatal breast milk expression at term improved the confidence in the ability to breastfeed and produce milk postpartum, thus significantly improving the behavior of exclusive breastfeeding, and increasing the percentage of breastfed infants during their hospital stay, these infants were able to avoid infant formula milk in this important early period.


Abstract Background
Limited research outside China suggest that antenatal milk expression in late pregnancy (AME) may promote breastfeeding. A few studies have evaluated the safety and e cacy of AME in women with diabetes in pregnancy, little or no evidence exists to explore its effects on breastfeeding self-e cacy and early breastfeeding, particularly in rst-time mothers. The objective of this study was to explore the effect of AME on breastfeeding for the rst-time mothers during the postpartum hospitalization.

Methods
A randomized controlled trial was conducted in a tertiary hospital in Haikou, Hainan. We recruited pregnant women who had completed 37 weeks of gestation and randomly assigned them to either the intervention group (n = 45) or the control group (n = 45). The pregnant women in the intervention group were advised to rhythmic self-massage of breasts three times daily at any time. The control group was given routine midwifery and obstetric care. The breastfeeding self-e cacy scale(BSES)was used to measure the self-e cacy of breastfeeding at 37 weeks, 38 weeks and the third day postpartum. The time to lactogenesis II and the rate of exclusive breastfeeding was measured three times every day by the researcher in the ward.

Results
Compared with the control group, the intervention group had higher breastfeeding self-e cacy scores measured by the scale of BSES(P < 0.05), the intervention group had higher exclusive breastfeeding rate on the rst day, second day, third-day postpartum, and the difference was statistically signi cant P < 0.05). The time to lactogenesis II in the intervention group was earlier than that in the control group(P < 0.05).

Conclusions
Antenatal breast milk expression at term improved the con dence in the ability to breastfeed and produce milk postpartum, thus signi cantly improving the behavior of exclusive breastfeeding, and increasing the percentage of breastfed infants during their hospital stay, these infants were able to avoid infant formula milk in this important early period.

Plain English Summary
Limited research outside China suggests that antenatal milk expression (AME) in late pregnancy may promote breastfeeding. A few studies have evaluated the safety and e cacy of AME in women with diabetes in pregnancy, but no one has yet to explore its effects on breastfeeding self-e cacy and early breastfeeding, particularly in rst-time mothers. This study aimed to explore the effect of AME on breastfeeding for the rsttime mothers during the postpartum hospitalization by undertaking a randomized controlled trial.
Women who were advised to express breastmilk from 37 weeks' gestation were more likely to be con dent in ability to breastfeed and produce milk postpartum, and the proportion of infants who were exclusively breastfed in the rst three days of life was larger than that receiving standard care. Moreover, This study showed evidence of a bene cial effect on lactogenesis II. The study showed that AME is an effective way to promote pregnant women con dence inability to breastfeed and produce milk postpartum, thus signi cantly improving the behavior of exclusive breastfeeding, and increasing the percentage of exclusively breastfed infants during their hospital stay, these infants were able to avoid infant formula milk in this important early period.

Background
Breastfeeding is an unequaled feeding pattern for infants, having important bene ts of health for mothers and their infants [1]. The WHO recommends that infants should be exclusively breastfed for 6 months and continued breastfeeding until 2 years of age or beyond [2]. However, the breastfeeding rate in china remain below, the rate of 6-month-old infants is only 29.2% [3].
Maternal breastfeeding experience from 1 hour to the rst few days after delivery is critical to establish breastfeeding, and the rate of exclusive breastfeeding during postpartum hospitalization is signi cantly associated with the rate of exclusive breastfeeding at 6 weeks postpartum [4,5]. Among the most prevalently cited barries to the establishment of breastfeeding are impaired breastfeeding self-e cacy and delayed lactogenesis II [6-8]. Women with low breastfeeding self-e cacy will more likely to add formula in hospital or even completely arti cial feeding [9,10] leading to premature stopping of breastfeeding [11][12][13]. Stopping breastfeeding within 4 weeks postpartum is associated with delayed lactation initiation [8]. Delayed lactogenesis II is usually de ned as the onset of copious milk secretion 72 h postpartum. Women who delayed lactogenesis II are more likely to stop breastfeeding prematurely than that do not.
Antenatal milk expression (AME) has been suggested as a potential intervention to address these issues [14][15][16]. AME refers to extracting colostrum from the breast before birth by hand expressing. Limited studies have been conducted to evaluate the impact of AME intervention on breastfeeding for women with diabetes, and indicate that AME might help to enhance women's breastfeeding con dence, prevent delayed lactogenesis II and improve exclusive breastfeeding rate [17][18][19][20]. However, the impacts of AME to women who are not being with diabetes, particularly in rst-time mothers have not previously been evaluated. This study was therefore designed to examine the effects of AME on the term primipara.

Study design and participants
We did a single-blind, two-group, randomized controlled trial at a tertiary hospital in Hainan, China. The study was approved by the human research ethics committees of the A liated Hospital of Hainan Medical University.
Eligible women were between 18 and 34 years old, 35 and 36 weeks' gestation with a singleton pregnancy, healthy fetus, planning to breastfeed. Exclusion criteria were any pregnancy complication, such as preterm labor, diabetes, polycystic ovarian syndrome and hypertension; severe postpartum complication, such as postpartum Bleeding; fetal growth restriction; gestational week<38 weeks of delivery; the neonatal maternal separation; newborn birth weight <2500g; shortened lingual frenulum.
Randomization was done by a computerized random number, and the random numbers were reordered. After reordering, 1~45 were assigned to the intervention group, 46~90 digits were allocated to the control group, participants were masked to block size and group allocation.

Procedures
Women in the control group received standard care that included breastfeeding health education and guidance, as follows. (1) 28-34 weeks of gestation: bene ts of breastfeeding, the importance of early contact and early sucking, breastfeeding posture method of deep inclusion. (2) 35 -37 weeks of gestation: bene ts of colostrum, the size of the stomach capacity of the newborn, importance of breastfeeding on demand. (3) postpartum hospitalization: assist the mother and newborn to make early contact, suck, instruct the mother at the bed to correctly include the nipple and evaluate the effectiveness of sucking, emphasize to mothers and primary caregivers the importance of breastfeeding on demand. (4) Postpartum follow-up: follow-up of the problems or doubts of the parturient by telephone, and give guidance.
Women in the intervention group received standard care, as well as instructions on hand expressing breast milk: (a) Before each hand expressing, women¢s hands were washed for 1 min with soap; (b) Place the thumb above the nipple and the index nger below the nipple forming a "C" shape on the edge of the areola(usually 2-3cm away behind the nipple). Using the power of the ngertips to squeeze gently toward the chest wall, then relax and repeat building up a rhythm; (c) From the rst day of 37 weeks of gestation, women were encouraged to hand expressing breast milk three times a day for 10 min until admission to hospital to give birth; and (d) In the weekly follow-up visit, women were encouraged to hand expressing breast milk under the electronic fetal monitoring, to evaluate whether it is correctly master the method of hand expressing, and monitor the fetal heart rate and uterine contraction while hand expressing. Women should continue to hand expressing, unless electronic fetal monitoring indicated that fetal intrauterine anoxia. Besides, the researcher contacted them via phone or WeChat every day.
Demographic data (including maternal age, ethnicity, height, pre-pregnancy weight, education, family monthly income) were obtained by questionnaire at recruitment before randomization. and are lled in by the research subjects on the day of admission. obstetric and neonatal medical outcomes (including gestational age of the childbirth, the mode of delivery, the sex of the newborn, the birth weight) were abstracted from the medical record after delivery.

Measurement
Breastfeeding self-e cacy which is the con dence in the ability to breastfeed and produce milk postpartum, was assessed by the breastfeeding self-e cacy scale at 37 weeks of gestation, 38 weeks of gestation and third day postpartum [21] The scale contains two dimensions of skills and inner activity, a total of 30 items, using a Likert 5-point scale (1~5 points), a total score of 30~150 points, the higher the score, the higher the maternal con dence in breastfeeding. The Cronbach'S a coe cient of this scale is 0.93, and the split-half reliability coe cient is 0.91.
Time to Lactogenesis II was evaluated three times daily began at 24 h pp by mother's perception of the onset of lactation which is a valid public health indicator of lactogenesis stage II [22]. The researcher evaluated the clinical symptoms of Lactogenesis II(i.e., breast fullness, swelling, leakage), and the time to Lactogenesis II was recorded to the nearest hour.
Exclusive breastfeeding rate was used to evaluate feeding methods during the rst three days of life, according to the retrospective method within 24 hours. Exclusive breastfeeding indicates that the infant received only breast milk, allowing for vitamin/mineral drops and medications [23].

Statistical analysis
Data were gathered by reachers and entered into Excel for analysis. The data analysis was performed using the SPSS 22.0 software, A p-value of less than 0.05 was considered signi cant. Measurement data normality was expressed as mean ± SD, tested with t-test or repeated-measures analysis of variance. Data that did not pass the variance test were compared with a nonparametric two-tailed Mann-Whitney rank-sum test. The enumeration data were expressed as n (%)and compared between groups by the or Fisher exact test, as appropriate.

Characteristics of participants
Between March 10, 2019, and August 30, 2019, we recruited 90 women who were randomly assigned to treatment: 45 to the intervention group and 45 to the control group (Fig.1). Six cases assigned to the intervention group were excluded for macrosomia in 1 case, delivered in another hospital in 1case, admission to NICU in 4 cases. Nine cases were excluded from the control group for one withdrew, delivered in another hospital in 2 cases, low birth weight infants in 1case, postpartum hemorrhage in 2 cases, admission to NICU in 3 cases. Finally, leaving 75 cases available for the primary analysis (39 in the intervention group and 36 in the control group).
Baseline characteristics for women and babies were similar between groups (Table 1), including maternal age, education, income, breastfeeding self-e cacy at 37 weeks of gestation, pre-pregnancy BMI, gestational weight gain, gestational week, delivery method, analgesia method, sex of baby and birth weight. There was no signi cant difference in the two groups (P>0.05).
Breastfeeding self-e cacy scores changes between the two groups There was no signi cant difference in the scores of breastfeeding self-e cacy between the two groups before intervention(P>0.05), while the postintervention scores were higher than those of the control group at 38 weeks and the third day after delivery (P<0.05)( Table 2). The breastfeeding self-e cacy scores in both groups increases with time. There were interaction effects between groups and a time effect of the breastfeeding selfe cacy scores. The intervention group shows a stronger increase in breastfeeding self-e cacy scores over time than the control group(P<0.05).
Comparison of the differences in time to lactogenesis II between the two groups Out of the 39 women in the intervention group, 19(48.7%) of the cases established full lactation 24 to 48 hours after delivery, whereas in the control group, out of 36 only 8 (22.2 %) of cases had established full lactation, indicating that the time to lactogenesis II in the intervention group was earlier than that in the control group (P<0.05) ( Table 3). Besides, the higher the frequency of expressing, the earlier the onset of lactogenesis II (Table   4).

Feeding mode during the rst three days of life
Of the women allocated to the intervention group, 22(56.4%) of 39 infants were feeding with exclusive breastfeeding on the rst-day pp, while the control group was mainly breastfeeding, accounting for 80.6%. On the second day pp, the exclusive breastfeeding rate of intervention group was 76.9%, while the control group was only 19.4%. On the third day pp, the exclusive breastfeeding rate in the intervention group was higher than that in the control group, and 22(61.1%) of 36 infants in the control group did not feeding with exclusive breastfeeding. There were statistically signi cant differences between the exclusive breastfeeding rate during the rst three days of life in the two groups (Table 5).

Discussion
This is the rst randomised controlled trial to report on the effects of antenatal expressing milk among rsttime mothers in China. We found that women who allocated to hand express three times daily from 37 weeks of gestation had a more positive in uence on breastfeeding self-e cacy. For those who completed the con dence measure, signi cantly increased breastfeeding self-e cacy scores were found in the intervention group between pre-and postintervention, but not in the control group. Explained by Bandura's social cognitive theory, direct experience is the positive reinforcement process by which individuals improve their skills through cognitive, behavioral, and self-discipline efforts, and is the main source of self-e cacy [10]. By repeatedly practicing hand expressing, pregnant women not only enrich breastfeeding knowledge, but also acquire important skills for breastfeeding, which is a concrete manifestation of direct experience. Also, Visualizing milk during AME, particularly when volume increases were observed, they evoked a sense of appreciation for one's body/breasts and gradually believed that they could produce milk postpartum. The high level of breastfeeding self-e cacy, the more conducive to the establishment and sustainability of breastfeeding [25].
An interesting finding of this study was AME promoted the lactogenesis II, and the time to lactogenesis II was advanced with the increase of AME frequency. Though another study had documented AME shortens the time taken to from initiation to full establishment of lactation, but the relationship between the frequency of AME and lactogenesis II was not been analyzed [16]. The baby sucking on the mother's nipple and effectively removes the milk plays a major role in the lactogenesis II [17]. Hand expressing through nerve re exes, re exive stimulation of serum prolactin (PRL) secretion increases, creating conditions for lactogenesis II, hand expressing effectively removes milk [26]. PRL is one of the lactation-related hormones and the most important breast synthesis hormone, which is essential for initiating and maintaining lactation. Hand expressing can be used as an effective measure to increase the frequency of milk removal, particularly when the newborn sucking is not well.
Our study showed signi cant improvements in exclusive breastfeeding rates among rst-time mothers during their hospital stay. This nding is in line with another study that advised women with diabetes in pregnancy to express breastmilk in late pregnancy, suggesting that AME may have a positive effect on breastfeeding [15].
This may have been the result of the deployment of breastfeeding self-e cacy at prenatal. Mothers who have a high level of breastfeeding self-e cacy are more likely to breastfeed after delivery and are more likely to respond in a positive way when encountering breastfeeding di culties [27]. Although breastfeeding is a natural process, studies have shown that more than 80% of primiparas will experience one or more breastfeeding di culties, and many of them say breastfeeding is more di cult than expected [28]. Common breastfeeding di culties such as getting the baby to latch on, nipple pain, maternal fatigue, perception of insu cient milk, and impaired breastfeeding self-e cacy were especially prominent in the early breastfeeding period [29]. Moreover, the time to lactogenesis II is advanced. Timing of maternal perception of onset of lactogenesis II generally begins 48 to 72 hours postpartum [30], but 17% to 44% of primiparas later than 72h [31][32][33]. Delayed onset of lactogenesis II DOL is an important reason for early exclusive breastfeeding failure [34]. Delayed onset of lactogenesis II, mothers often show anxiety and think that they cannot produce adequate milk, so that supply with formula for babies in hospital, which prevents the establishment of early breastfeeding. In this study, the time to lactogenesis II in the intervention group was earlier than that in the control group, which was not only conducive to the mother 's own rm belief in insisting on exclusive breastfeeding, but also conducive to the mother 's overcoming from the caregiver and his family that the early postpartum milk secretion could not meet the needs of the newborn.

Limitations
Our study mainly explored the impact of AME on breastfeeding during postpartum hospitalization. However, due to time, manpower, and nancial constraints, no discharge follow-up was conducted, and the effect of AME on long-term breastfeeding could not be discussed. Therefore, in future research, large-scale, long-term and lactation support studies are needed to explore its long-term effects.
Conclusion AME is an effective way to promote pregnant women con dence inability to breastfeed and produce milk postpartum, thus signi cantly improving the behavior of exclusive breastfeeding, and increasing the percentage of breastfed infants during their hospital stay, these infants were able to avoid infant formula milk in this important early period. The authors would like to thank the mothers for participating in the study. We thank the physicians and nurses from the A liated Hospital of Hainan Medical University.

Abbreviations
Authors' contributions YC-study conception and survey design, cleaned and analysed the data, prepared the initial manuscript draft and revised the manuscript. LPM and JJZ-recruited participants. HHG-contributed to data analysis. HYZ-study conception and survey design, revised the manuscript. All the authors read and approved the nal manuscript.

Funding
This work was supported by the Natural Science Foundation of Hainan Province (SQ2019QNJJ0440).

Availability of data and materials
The datasets used and/or analyzed during the current study are available from the corresponding author upon reasonable request.  c. F-value and P-value by the interaction effects. 11.281 P-value 0.024 Table 5 Comparison of the differences in the exclusive breastfeeding rate at three days pp