The Critical Window of Opportunity: Lactation Initiation Following Cesarean Birth

Abstract

Introduction:

Cesarean birth is reported to be risk factor for the delayed onset of maternal lactation. The purpose of this study was to describe the timing of lactation initiation, subsequent feeding/milk expression patterns, and daily milk volumes among women who had a cesarean birth of an infant with a known congenital anomaly during the 3-day postpartum hospital stay.

Materials and Methods:

Retrospective descriptive cohort study. The electronic medical records of dyads, between 2014 and 2017 at the study setting, were abstracted for demographic and clinical data. Milk expression and milk volume data were abstracted from maternal lactation logs. Data were analyzed using descriptive statistics.

Results:

Among the cohort (n = 468 dyads), the mean time from infant delivery by cesarean to lactation initiation was 257.5 minutes. The cohort was divided into three groups by the timing of lactation initiation: EARLY (≤60 minutes; n = 112), MID (>60 minutes to ≤360 minutes; n = 309), and LATE (>360 minutes; n = 47). Statistically significant differences are seen between groups for the daily means: number of feeds/pumps and maternal milk volumes (irrespective of the presence of lactation risk factors).

Discussion:

This is the first study to explore the relationship of lactation initiation among women postcesarean birth whose infants have a known congenital anomaly. The time between the infant's birth and the first feed/milk expression, and the patterns of feeding/milk expression during the postpartum hospital stay, are key drivers for maternal milk supply.

Introduction

Human milk production has a critical window surrounding the period of transition from secretory differentiation, which begins around the 16th prenatal week, to secretory activation. This transition is marked by a decrease in the hormone, progesterone, and an increase in the hormone, prolactin, coupled with the removal of milk from the breast. Secretory activation classically occurs between 30 and 72 hours after the delivery of the placenta.¹ The delayed onset of secretory activation is defined as delayed copious secretion of breast milk after 72 hours postpartum and affects 17–44% of all breastfeeding mothers, with primiparous women in the United States experiencing rates estimated between 23% and 44%.^2–4 The delayed onset on secretory activation can lead to clinically significant negative lactation outcomes for families that hold a personal goal to provide mother's own milk for their infants after birth as the delay is strongly associated with higher rates of formula supplementation and decreased exclusivity and duration of breastfeeding.^2,5–7

Research has shown many associated risk factors for delayed onset of secretory activation. Identified maternal risk factors include women who are primiparous, obese, and gestational diabetics,^4,8,9 whereas cesarean sections, prolonged stage 2 labor, the use of some labor pain medications, and postpartum edema are also highly associated with delayed onset of secretory activation.^10,11 Of importance, women who hold perceptions of ineffective breastfeeding in the first days after the birth are also at increased risk.^5,12

The clinical presentation of the risk factors associated with delayed onset of secretory activation mirror the experiences of mothers with known, prenatally diagnosed fetal anomalies with anticipated intensive care needs after birth. In this population, rates of cesarean sections are high owing to the nature of the infants' diagnoses and the use of labor pain medications is common. In addition, these infants require the care and support of a neonatal or cardiac intensive care unit immediately after birth. Therefore, that physical separation further contributes to a delay in the timing of lactation initiation (by direct feeding at the breast or milk expression by breast pump and/or hand).^13–16 Numerous research studies have demonstrated the negative consequences of maternal infant separation with regard to lactation initiation and the ongoing maintenance of a robust milk supply in the context of an intensive care unit setting.^17–20

With regard to best supporting those families with a preference to provide an exclusive mother's own milk diet for their infants with congenital anomalies, clinicians can draw upon research conducted in other vulnerable infant populations. Interventions to attain a transition within the expected parameters include early initiation of direct breast feeds or early milk expression. Among term infants, researchers have demonstrated an association of early initiation of lactation with extended durations of breastfeeding, increased maternal milk volume on postpartum day 5, and an earlier onset of the transition from secretory differentiation to activation.^6,21 Similar outcomes have been demonstrated among mothers of very low birth weight infants and in the maternal-preterm infant population with early initiation of expression associated with increased maternal milk volume and an earlier transition to secretory activation.^22–28

However, the implications of the timing of lactation initiation for women who will deliver an infant with a known congenital anomaly by cesarean section remain unknown. Therefore, this retrospective descriptive study aimed to describe a cohort of patients with prenatally diagnosed fetal anomalies and their milk expression patterns and maternal milk supply in the context of the 3-day postcesarean section hospital stay.

Materials and Methods

This study was approved by the Institutional Review Board of Children's Hospital of Philadelphia (CHOP).

Participants and setting

To be eligible for study inclusion, the mother must have delivered her infant by cesarean section between January 1, 2014 and June 30, 2017 at the study setting, initiated lactation, and kept a maternal lactation log during the 3-day postpartum hospital stay. Women who experienced palliative care and/or fetal demise, and women who gave birth to multiples were excluded from the study (for consistency of sample).

The research was conducted at CHOP, a free-standing pediatric hospital with an internal prenatal center, the Center for the Fetal Diagnosis and Treatment (CDFT), and labor and delivery unit, the Garbose Special Delivery Unit. The CDFT is an international referral center for infants with known congenital anomalies and >70% of families travel from >100 miles away to receive care at CHOP.^29,30

Lactation-related care and support are integrated into the setting's prenatal care program. A critical element of the care is focused in providing all families with opportunities to make informed feeding decisions for their children.³¹ Upon referral to the study setting, all families are offered an individualized prenatal nutrition consultation with a member of the hospital's Lactation Program. During this consultation, the consultant begins with gaining an understanding of the family's goals and balances those goals with realistic expectations related to lactation, breastfeeding, and their infant's diagnosis.³² When discussing the benefits of a mother's own milk diet, the consultant shares research demonstrating how mother's own milk improves the health and developmental outcomes of vulnerable children. The consultant focuses teaching on specific components of the milk and how they work to protect infants from disease and illness (e.g., antibodies antioxidants, human milk oligosaccharides, stem cells, lactoferrin, osteopontin, and white blood cells).

Families are also taught the basic physiology of lactation and the consultant emphasizes that if the infant cannot feed enterally at birth, every drop of milk will immediately be used for mother's own milk oral care for their infant.³³ A physical demonstration on the operation and cleaning of the Medela Symphony^® hospital-grade double electric breast pump is carried out with each family. It is important to note that owing to the critical nature of infants born at the study setting, very few (<5 infants per month) are able to directly feed at the breast after delivery as the majority require immediate intubation and respiratory support. Therefore, for families that hold a goal to provide mother's own milk, the consultant provides the family with anticipatory guidance for initiating lactation with the Medela Symphony breast pump with Initiation Technology™ ideally within the first hour after birth.^27,28

Toward the end of the consultation, the consultant answers any remaining questions and then provides the family with a gift bag with all the supplies needed to safely initiation lactation with a breast pump: sterile pump kit, milk storage bottles (in two sizes), labels (including colostrum-specific labels), dish soap, microsteam bag for sterilization, and written handouts (10 tips for family and friends and the setting's comprehensive “Family Pump Log”).³⁴ Finally, the consultant reflects on the family's initial goals and preferences and then helps the family to set and document their desired goals in the study setting's electronic health record.^32,35

As a standard of care, clinicians in the study setting encourage women to keep a maternal lactation log during their postpartum period.³⁴ At the time of discharge from the Special Delivery Unit, the lactation log is collected with permission, photocopied, and the maternal lactation data are then entered into a secure database managed by the hospital's Lactation Program.

Data collection and management

Participant demographic and clinical data were abstracted from the electronic medical record and securely managed in a single private REDCap database. Maternal demographics and clinical characteristics included the following: age, race, ethnicity, employment status, gravida, para, pregravida weight, maternal weight gain during pregnancy, gestational diabetes, use of antenatal steroids, and the planned route of delivery. In addition, the study team collected the documented maternal feeding intentions (breastfeeding/expression/mother's own milk, infant formula only, or combination) if the woman completed a prenatal nutrition consultation at the study setting during the course of her prenatal care. The date and time of the infant's birth and the date and time of the placenta delivery were also abstracted from the electronic medical record. Infant demographics and clinical characteristics included gestational age, birth weight, primary diagnosis, and initial length of stay.

Maternal milk expression and milk volume data were abstracted from the maternal lactation logs. Daily totals, over the mother's 3-day hospital stay, for both the number of feeds/pumps and maternal milk volumes were calculated and then entered into the same private REDCap database.

Methods of analysis

Baseline and demographic characteristics, as well as milk expression data and milk volume data, were summarized using descriptive measures (means and standard deviations for continuous variables and percentages for categorical variables). After an analysis of the full cohort, the research team then divided the cohort into three groups by the timing of lactation initiation and the delivery time of the infant: EARLY (≤60 minutes), MID (>60 minutes to ≤360 minutes), and LATE (>360 minutes). To detect differences in clinical characteristics (categorical variables), significance was detected using Crosstabs with chi-square. For differences in feeding and milk expression patterns and maternal milk volumes, nonparametric statistics were used (ANOVA test for means and Kruskal–Wallis test for medians).

Results

A total of 468 dyads were included in the study. The mean timing of breastfeeding or breast expression from the time of the infant delivery and the placenta delivery was 257.5 minutes (median 180 minutes) and 257.2 minutes (median 178 minutes), respectively. Demographic and clinical characteristics are given in Table 1.

Table 1.

Cohort Demographics

Demographic	n (%)	$\bar{x}$ , Median [range]
Maternal age, years	468	30.2, 30 [17–50]
Maternal ethnicity
Hispanic or Latino	51 (10.9)
Not Hispanic or Latino	417 (89.1)
Maternal race
American Indian or Alaska Native	1 (0.2)
Asian	15 (3.2)
Black or African American	58 (12.4)
Native Hawaiian or other Pacific Islander	2 (0.4)
White	330 (70.5)
Other	59 (12.6)
Payor
Charity care	3 (0.6)
Medicaid	100 (21.4)
Private	345 (73.3)
Self-pay	3 (0.6)
Unknown/not documented	17 (3.6)
Maternal employment
Employed	306 (65.4)
Not employed outside the home	98 (20.9)
Unknown/not documented	64 (13.7)
Parity
0	215 (45.9)
1	165 (35.3)
>2	88 (18.8)
Maternal pregravida weight, kg	462	71.6, 68.7 [35.4–152.7]
Maternal weight gain during pregnancy, kg	462	12, 11.4 [−9.7–44.7]
Maternal gestational diabetes	46 (9.8)
Antenatal steroids	96 (20.5)
Prenatal nutrition consultation	324 (69.2)
Documented prenatal maternal infant feeding intention	286 (88.3)
Breastfeeding/human milk only	277 (96.9)
Infant formula only	5 (1.7)
Combination	4 (1.4)
Planned route of infant delivery
Cesarean section	342 (73.1)
Vaginal	126 (26.9)
Time to lactation initiation
Infant delivery, minutes	468	257.5, 180 [0–4,620]
Placenta delivery, minutes	460	257.3, 178 [0–4,619]
Infant diagnosis
Neurologic anomalies	143 (30.6)
Cardiac anomalies	137 (29.3)
Congenital diaphragmatic hernia	29 (6.2)
Sacrococcygeal teratoma	5 (1.1)
Lymphangioma	13 (2.8)
Abdominal wall defects (gastroschisis, omphalocele, giant omphalocele)	43 (9.2)
Gastrointestinal anomalies (duodenal atresia, tracheal esophageal fistula)	13 (2.8)
Multiple congenital anomalies	23 (4.9)
Other	62 (13.2)
Infant birth weight, kg	468	2.97, 2.98 [0.41–5.26]
Infant gestational age, weeks	468	37.1, 37.5 [24.7–40.7]
Infant length of stay, days	468	33.7, 19 [2–334]

The mean number of daily feeds/pumps and daily total maternal milk volumes on the day of delivery were 2.96 feeds/pumps and 3.1 ± 8.1 (median 0, range 0–82) milliliters. On postpartum day 1, the mean values were 5.51 feeds/pumps per day and 5.8 ± 13.8 (median 0, range 0–141) milliliters. On the last day of the maternal hospital stay (postpartum day 2), the mean number of feeds/pumps and maternal milk volumes were 5.71 and 36 ± 65.1 (median 10, range 0–570) milliliters, respectively.

Upon dividing the cohort into three groups by the onset of lactation and the delivery time of the infants: EARLY (n = 112), MID (n = 309), and LATE (n = 47), the three groups showed no statistically significant differences except maternal weight gain during pregnancy. However, statistically significant differences (p ≤ 0.05) were identified when considering the timing of initiation of lactation and subsequently, the number of daily feeds/pumps on delivery day (p = 0.000), postpartum day 1 (p = 0.000) and postpartum day 2 (p = 0.010) as well as maternal milk volumes on delivery day (p = 0.000), and postpartum day 2 (p = 0.005) (Table 2). The analysis accounted for lactation risk factors (first pregnancy, advanced maternal age, gestational diabetes, antenatal steroids, and maternal weight gain during pregnancy) and the presence or absence of lactation risk factor(s) did not impact the three groups in relation to the timing of lactation initiation and the subsequent feeding/milk expression patterns or maternal milk volumes (p > 0.05).

Table 2.

Lactation Patterns and Milk Supply by Group

	Full cohort (n = 468), $\bar{x}$	EARLY ≤60 minutes (n = 112), $\bar{x}$	MID >60 minutes to ≤360 minutes (n = 309), $\bar{x}$	LATE >360 minutes (n = 47), $\bar{x}$	p^*
Number of feeds/pumps, delivery day	2.96	3.86	2.92	1.09	0.000^*
Maternal milk volume, mL, delivery day	3.1 ± 8.1	4.5 ± 10.7	3 ± 7.5	0.1 ± 0.7	0.000^*
Maternal milk volume, mL, delivery day	0 (median), 0–82 (range)	0 (median), 0–64 (range)	0 (median), 0–82 (range)	0 (median), 0–5 (range)	0.000^*
Number of feeds/pumps, postpartum day 1	5.51	5.97	5.56	4.04	0.000^*
Maternal milk volume, mL, postpartum day 1	5.8 ± 13.8	4.9 ± 8.9	6.5 ± 15.7	3.1 ± 9.8	0.084
Maternal milk volume, mL, postpartum day 1	0 (median), 0–141 (range)	0 (median), 0–45 (range)	0 (median), 0–141 (range)	0 (median), 0–61 (range)	0.084
Number of feeds/pumps, postpartum day 2	5.71	6	5.75	4.77	0.010^*
Maternal milk volume, mL, postpartum day 2	36 ± 65.1	38 ± 56.3	36.7 ± 68.9	26.7 ± 59.5	0.005^*
Maternal milk volume, mL, postpartum day 2	10 (median), 0–570 (range)	16.8 (median), 0–370 (range)	10 (median), 0–570 (range)	0 (median), 0–297 (range)	0.005^*

Statistically significant difference: p ≤ 0.05.

Discussion

This is the first research study to clearly support that it is not solely the cesarean birth that impacts milk supply, but rather, the clinical management of the mother after delivery is highly significant. Cesarean birth rates are high in the United States as well as in many other countries of the world. As health care providers, a shift in the prenatal care paradigm is imperative to empower families regarding their ability to provide milk for their infants.

When a family has a high-risk pregnancy and/or is expecting a cesarean birth, during the prenatal care period the family should be prepared realistically about the importance of expression early and often. Previous research, among term infant-mother dyads, has demonstrated favorable outcomes of early initiation of lactation with extended durations of breastfeeding and increased maternal milk volume on postpartum day 5.^6,21 Similar favorable outcomes have been shown in preterm infant–mother dyads and very low birth weight infant–mother dyads.^22–28 However, this is the first study to show statistically significant differences in milk expression patterns (delivery day, postpartum day 1, and postpartum day 2) and maternal milk volumes (delivery day and postpartum day 2) among a large sample during the traditional 3-day postpartum hospital stay by groups depending on the timing of initial breastfeeding or expression. This study demonstrates the clinical significance of early initiation of lactation (within the first hour) and the resulting positive outcomes for increased frequency of milk expression sessions per day, as well as overall increased maternal milk volume per day, compared with women who initiated lactation 1–6 hours, and >6 hours after the birth.

The results of this cohort study show the participants did not achieve the recommended 8–10 feeds or expression sessions per day (day of delivery, mean 2.96 feeds/pumps; postpartum day 1, mean 5.51 feeds/pumps; postpartum day 2, mean 5.71 feeds/pumps). On the day of delivery, it is important to note the time of day of the infant's birth. For those infants born later in the day, there are fewer opportunities for feeding and/or expression. However, the results do show statistically significant differences on the daily mean number of feeds/pumps by group (EARLY, MID, and LATE).

Although the study setting is unique in that the population consists only of women with prenatally diagnosed fetal anomalies, this research has utility for all families expecting or having cesarean births as the cohort contained dyads of a healthy mother with a traditional 3-day hospital stay. In addition, in the study's sample, a quarter of the cohort anticipated a vaginal delivery but for many reasons had a cesarean section. Therefore, the findings of this research should be shared with all families at the time of prenatal counsel.

Limitations

This research was conducted at a single free-standing pediatric hospital with a predominantly strong human milk culture. Furthermore, the study team only collected milk expression and milk volume logs during the mother's birth hospital stay and there are known limitations to self-reported data. However, research from Meier et al. demonstrates that the frequency of milk expression and milk volume in the first 3–5 days is predictive of normal lactation biomarkers and coming to volume.³⁶ Future research should be conducted in mothers who have cesarean births with presumed healthy infants.

Conclusions

This study aimed to describe a cohort of patients with prenatally diagnosed fetal anomalies and their milk expression patterns and maternal milk supply in the context of the 3-day postcesarean section hospital stay. By dividing the full cohort by the timing of lactation initiation, statistically significant differences are seen between groups (EARLY, ≤60 minutes; MID, >60 minutes to ≤360 minutes; and LATE, >360 minutes), for the daily mean number of feeds/pumps and mean daily milk volumes irrespective of the presence of lactation risk factors.

Adapting a proactive management style for women undergoing cesarean birth may allow the mother to effectively convert from secretory differentiation to activation. For those families holding a goal to provide mother's own milk for their infants, it is critical for health care providers to focus on essential windows of time: (1) the first hour after birth, (2) the first 6 hours after birth, and (3) the short time during the mother's hospital stay. For women who are exclusively expressing milk, mothers may be overwhelmed with the prospect of expressing every 2–3 hours for eight or more sessions in 24 hours. Clinicians can help to balance those feelings with evidence-based anticipatory guidance and teach families that the early initiation of lactation is associated with increased frequency in feedings/milk expression sessions per day and increased maternal milk volumes during the hospital stay on the maternity/delivery unit. This guidance can then benefit all families to support their ability to meet their personal breastfeeding goals regardless of mode of delivery.³⁵

Footnotes

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

References

Dewey

, Nommsen-Rivers

, Heinig

, et al. Risk factors for suboptimal infant breastfeeding behavior, delayed onset of lactation, and excess neonatal weight loss. Pediatrics, 2003; 112(Pt 1):607–619.

Brownell

, Howard

, Lawrence

, et al. Delayed onset lactogenesis II predicts the cessation of any or exclusive breastfeeding. J Pediatr, 2012; 161:608–614.

Preusting

, Brumley

, Odibo

, et al. Obesity as a predictor of delayed lactogenesis II. J Hum Lact, 2017; 33:684–691.

Matias

, Dewey

, Quesenberry

Jr , et al. Maternal prepregnancy obesity and insulin treatment during pregnancy are independently associated with delayed lactogenesis in women with recent gestational diabetes mellitus. Am J Clin Nutr, 2014; 99:115–121.

Chantry

, Dewey

, Peerson

, et al. In-hospital formula use increases early breastfeeding cessation among first-time mothers intending to exclusively breastfeed. J Pediatr 2014;164:1339–1345 e1335.

Chen

, Nommsen-Rivers

, Dewey

, et al. Stress during labor and delivery and early lactation performance. Am J Clin Nutr, 1998; 68:335–344.

Sievers

, Haase

, Oldigs

, et al. The impact of peripartum factors on the onset and duration of lactation. Biol Neonate, 2003; 83:246–252.

Bartok

, Schaefer

, Beiler

, et al. Role of body mass index and gestational weight gain in breastfeeding outcomes. Breastfeed Med, 2012; 7:448–456.

Nommsen-Rivers

, Chantry

, Peerson

, et al. Delayed onset of lactogenesis among first-time mothers is related to maternal obesity and factors associated with ineffective breastfeeding. Am J Clin Nutr, 2010; 92:574–584.

10.

Garcia-Fortea

, Gonzalez-Mesa

, Blasco

, et al. Oxytocin administered during labor and breast-feeding: A retrospective cohort study. J Matern Fetal Neonatal Med, 2014; 27:1598–1603.

11.

Lind

, Perrine

, Li

. Relationship between use of labor pain medications and delayed onset of lactation. J Hum Lact, 2014; 30:167–173.

12.

Chapman

, Perez-Escamilla

Identification of risk factors for delayed onset of lactation. J Am Diet Assoc 1999;99:450–454; quiz 455–456.

13.

Skelton

, Dahlen

, Psaila

, et al. Facilitating closeness between babies with congenital abnormalities and their parents in the NICU: A qualitative study of neonatal nurses' experiences. J Clin Nurs, 2019; 28:2979–2989.

14.

Demirci

, Caplan

, Brozanski

, et al. Winging it: Maternal perspectives and experiences of breastfeeding newborns with complex congenital surgical anomalies. J Perinatol, 2018; 38:708–717.

15.

Rendon-Macias

, Castaneda-Mucino

, Cruz

, et al. Breastfeeding among patients with congenital malformations. Arch Med Res, 2002; 33:269–275.

16.

Salvatori

, Foligno

, Occasi

, et al. Human milk and breastfeeding in surgical infants. Breastfeed Med, 2014; 9:491–493.

17.

Palmquist

AEL

, Holdren

, Fair

. “It was all taken away”: Lactation, embodiment, and resistance among mothers caring for their very-low-birth-weight infants in the neonatal intensive care unit. Soc Sci Med, 2020; 244:112648.

18.

Bower

, Burnette

, Lewis

, et al. I had one job and that was to make milk. J Hum Lact, 2017; 33:188–194.

19.

Hurst

, Engebretson

, Mahoney

. Providing mother's own milk in the context of the NICU: A paradoxical experience. J Hum Lact, 2013; 29:366–373.

20.

Rossman

, Kratovil

, Greene

, et al. “I have faith in my milk”: The meaning of milk for mothers of very low birth weight infants hospitalized in the neonatal intensive care unit. J Hum Lact, 2013; 29:359–365.

21.

Murray

, Ricketts

, Dellaport

. Hospital practices that increase breastfeeding duration: Results from a population-based study. Birth, 2007; 34:202–211.

22.

Furman

, Minich

, Hack

. Correlates of lactation in mothers of very low birth weight infants. Pediatrics, 2002; 109:e57.

23.

Hill

, Aldag

, Chatterton

. Effects of pumping style on milk production in mothers of non-nursing preterm infants. J Hum Lact, 1999; 15:209–216.

24.

Hill

, Brown

, Harker

. Initiation and frequency of breast expression in breastfeeding mothers of LBW and VLBW infants. Nurs Res, 1995; 44:352–355.

25.

Hoban

, Bigger

, Schoeny

, et al. Milk volume at 2 weeks predicts mother's own milk feeding at neonatal intensive care unit discharge for very low birthweight infants. Breastfeed Med, 2018; 13:135–141.

26.

Hopkinson

, Schanler

, Garza

. Milk production by mothers of premature infants. Pediatrics, 1988; 81:815–820.

27.

Parker

, Sullivan

, Krueger

, et al. Effect of early breast milk expression on milk volume and timing of lactogenesis stage II among mothers of very low birth weight infants: A pilot study. J Perinatol, 2012; 32:205–209.

28.

Parker

, Sullivan

, Krueger

, et al. Association of timing of initiation of breastmilk expression on milk volume and timing of lactogenesis stage II among mothers of very low-birth-weight infants. Breastfeed Med, 2015; 10:84–91.

29.

Howell

LJ.

The Garbose Family Special Delivery Unit: A new paradigm for maternal-fetal and neonatal care. Semin Pediatr Surg, 2013; 22:3–9.

30.

Howell

, Adzick

. Establishing a fetal therapy center: Lessons learned. Semin Pediatr Surg, 2003; 12:209–217.

31.

Spatz

DL.

Ten steps for promoting and protecting breastfeeding for vulnerable infants. J Perinat Neonatal Nurs, 2004; 18:385–396.

32.

Spatz

DL.

Say no to success-say yes to goal setting. MCN Am J Matern Child Nurs, 2017; 42:234.

33.

Froh

, Deatrick

, Curley

, et al. Making meaning of pumping for mothers of infants with congenital diaphragmatic hernia. J Obstet Gynecol Neonatal Nurs, 2015; 44:439–449.

34.

Spatz

, Froh

, Schwarz

, et al. Pump early, pump often: A continuous quality improvement project. J Perinat Educ, 2015; 24:160–170.

35.

Spatz

DL.

Helping mothers reach personal breastfeeding goals. Nurs Clin North Am, 2018; 53:253–261.

36.

Meier

, Johnson

, Patel

, et al. Evidence-based methods that promote human milk feeding of preterm infants: An expert review. Clin Perinatol, 2017; 44:1–22.