Abstract
Background:
In 2015, we implemented a comprehensive lactation bundle named Liquid Gold. Lactation bundles in the neonatal intensive care unit have not been well studied.
Materials and Methods:
This is an ongoing quality improvement breastfeeding project of racially diverse mothers and infants of extremely low birth weight (≤1,000 g). Four epochs were assessed; baseline (B; January 2012–July 2013), transition (T; human milk [HM]-derived fortifier; August 2013–December 2014), Liquid Gold (LG; full bundle, including staff education, colostrum oral care, kangaroo care, antenatal and postpartum counseling, provision of pasteurized donor HM, and breast pumps; January 2015–February 2016), and current (C; ongoing impact, Spanish-speaking lactation consultant, and HM cream; March 2016–April 2019).
Results:
Four hundred twenty-three mother–infant dyads were assessed. The rate of exclusive mother's own milk at discharge increased significantly in LG compared with previous epochs and was sustained over time. During LG, African American (AA) mothers had a significant surge of breastfeeding initiation (30% in B and 41% in T versus 78% in LG), but this was not sustained in C. AA mothers also experienced a significant decline in the use of exclusive formula feeding in the C epoch (68% in LG versus 46% in C). Hispanic and White mothers sustained their breastfeeding rates over time.
Conclusions:
Our Liquid Gold lactation bundle led to a significant increase in the provision of HM in the NICU and at discharge in the most vulnerable infants. AA mothers experienced the highest surge in breastfeeding initiation and greatest reduction in formula use. Breastfeeding goals and support need to be tailored to each mother with specific consideration for racial/ethnic background for optimal success.
Introduction
Both the American Academy of Pediatrics (AAP) and the American College of Obstetricians and Gynecologists (ACOG) recommend an exclusive human milk (EHM) diet for nearly all infants, recognizing the short-term and long-term benefits for both mothers and infants. These recommendations extend to premature infants with a distinct endorsement to provide pasteurized donor human milk (PDHM) when mother's own milk (MOM) is unavailable or insufficient.1,2 The benefits of breastfeeding for premature infants include improved tolerance of feeds; reduced time on parental nutrition; reduced incidence of necrotizing enterocolitis (NEC), intraventricular hemorrhage (IVH), retinopathy of prematurity (ROP), bronchopulmonary dysplasia (BPD), and sepsis; and reduced risk of neurodevelopmental delays, even in the setting of slower postnatal growth on EHM.3–6 The benefits of breastfeeding for women include lower risks of postpartum depression, breast cancer, ovarian cancer, diabetes, hypertension, and heart disease. 7
According to the Centers for Disease Control (CDC) Breastfeeding Report Card, many mothers initiate breastfeeding; however, the duration and exclusivity continue to fall short of the Healthy People 2020 targets.8,9 Furthermore, despite overall improvements in breastfeeding rates, significant racial disparities persist. Breastfeeding rates for African American (AA) mothers and infants consistently remain at the bottom of all breastfeeding indicators, even when controlled for family income and educational level. Interventions specifically addressing barriers to breastfeeding for AA women and other minority women are needed.10–13
There have been a few breastfeeding initiatives for preterm infants, most notably the World Health Organization and United Nations Children's Fund (WHO/UNICEF) Baby-Friendly Hospital Initiative (BFHI) and the Spatz 10-Step System to Improve Human Milk and Breastfeeding Outcomes.14,15 In 2011, the U.S. Surgeon General's Call to Action to Support Breastfeeding described specific steps for a society-wide approach to support mothers and babies who are breastfeeding. 16 Multiple factors influence a mother's decision to start and continue breastfeeding. Inadequate information and limited knowledge about breastfeeding and the benefits of a HM diet, concerns regarding milk supply, cultural norms, and societal support (i.e., unsupportive work environments and insufficient childcare options) are among the barriers many mothers face in meeting their breastfeeding goals. Many of these disproportionally affect AA mothers and other minorities.10–13
The HM diet has been found to optimize growth and outcomes in the subpopulation of extremely low-birth-weight (ELBW, BW ≤1,000 g) infants, who are particularly susceptible to adverse outcomes due to their immature physiology.3,17 Mothers of ELBW infants face even greater barriers to the provision of MOM compared with mothers of term infants. Maternal and infant health complications, the stress of having a baby in the neonatal intensive care unit (NICU), delayed normal physiologic adaptations, and physical separation from their infant, as well as delay in lactogenesis, may lead to inadequate milk supply. 18 Skin-to-skin care, staff education, peer counselors, provision of colostrum, and PDHM have all been individually assessed providing high-quality evidence of effectiveness in increasing the rates of breastfeeding in preterm infants.19–21 However, currently, there is a paucity of literature supporting the use of any one intervention and there is no standardized approach combining individual components. There are no benchmarks for the attainment of breastfeeding rates for ELBW infants, but presumably they should be higher than the Healthy People 2020 targets.
Evidence for breastfeeding bundles in the NICU is limited, but the utility of other care bundles has been well documented, most notably for neonatal nosocomial infections, unplanned extubation, surfactant administration, pain management, and HM provision. 22 Thus, we sought to develop a breastfeeding bundle, incorporating the available evidence-based interventions with proven individual effects, with the aim of ameliorating many of the barriers and improving breastfeeding outcomes of mothers of ELBW infants.23–25 Our Liquid Gold bundle consists of antenatal counseling and postnatal lactation support, medical staff education, early colostrum collection and colostrum oral care (COC), provision of a double electric breast pump before maternal discharge, provision of EHM diet with MOM, bridged by PDHM, and preterm PDHM from our own milk bank, appropriately fortified with HM-derived fortifier.26–35 Over time, we improved access to lactation consultants (LCs) in labor and delivery (L&D), postpartum and outpatient, included a Spanish-speaking LC, and incorporated an HM cream fortifier, all in an effort to increase the lactation success of these high-risk mothers.36,37 The primary purpose of this study was to assess the success of our Liquid Gold bundle in the provision of MOM over time, specifically at first enteral feed and at discharge. The secondary aim was to assess the impact of our bundle across racial subgroups to determine whether disparities would persist despite this standardized approach.
Materials and Methods
Study population
We studied all ELBW infants who were admitted to our Regional Perinatal Center (RPC) at the Maria Fareri Children's Hospital Level IV NICU at Westchester Medical Center in Valhalla, New York, within 96 hours of life and who received their first feed at the same location between January 2012 and April 2019. We excluded infants with any major congenital or genetic anomalies. The study was approved by the New York Medical College and Westchester Medical Center Institutional Review Boards.
Study protocol/bundle creation
The study population was divided accordingly into four time epochs:
(1) Baseline (B; January 2012–July 2013); in this time period, infants who needed supplementation to MOM received bovine milk-derived fortifier (Enfamil® HMF) and preterm formula. There was no NICU-dedicated LC.
(2) Transition (T; August 2013–December 2014); in this time period, HM-derived multicomponent fortifier (Prolact+H2 MF®) was provided to infants who received a diet of exclusive MOM. The remainder of the infants received MOM when available, fortified with bovine-based fortifier, and supplementation with preterm formula. During this period, we also reviewed the evidence and developed the bundle.
(3) Liquid Gold (LG; January 2015–February 2016); this time period was marked by implementation of the full bundle, including the following:
Staff education consisting of a 30-minute online training module with pre- and post-tests.
Standardized skin-to-skin care protocol dependent on infant stability and driven by nursing policy and annual nursing competencies. The skin-to-skin care was done daily for all infants with the frequency and duration dependent on the infant's condition and mother's availability and comfort level.
COC within 24 hours of birth.
Assistance with expression of breast milk within 6 hours postpartum.
HM as the first enteral feed (MOM or PDHM).
Provision of exclusive HM diet supported by PDHM and HM fortifier (Prolact+H2 MF).
Daily rounds to assess lactation progress with a multidisciplinary team, including physicians, nurses, nurse practitioners, dieticians, and therapists; LCs performed independent lactation rounds based on mother availability at the bedside.
Access to a certified LC in the L&D unit and for postpartum counseling.
Provision of food trays for mothers when they visited their babies in the NICU.
Elimination of all formula promotional materials.
Assistance with obtaining a double electric breast pump, as mandated by the Affordable Care Act and covered by private and Medicaid insurance plans. Practical support was provided to each mother when needed. All mothers had access to hospital-grade pumps when visiting their babies in the NICU. A hospital-grade pump for home use was also provided to any mother with low milk supply whose infant had NEC.
4. Current (C; March 2016–April 2019); in this time period, the ongoing impact of the LG bundle was evaluated. Additional interventions included the following:
Implementation of HM cream (Prolact+CR®)—an HM-derived caloric fortifier intended to supply more lipids and achieve adequate growth.
Addition of a Spanish-speaking LC and increase in the full-time equivalent LC support to 2.0.
Outcome measures
Our primary outcome was exclusive MOM diet at discharge. Secondary outcomes included rates of HM intake (MOM, PDHM, or both) at first and full enteral feeds, defined as 150 mL/kg/day. We also tracked survival and the incidence of the most common NICU morbidities (i.e., NEC, IVH, BPD, ROP, and sepsis), using standard definitions. We categorized mothers across epochs over time and subgrouped each cohort by self-identified race of AA, Hispanic, White, or other.
Data collection and analysis
This study was a prospective quality improvement initiative with historical controls, continual adjustments, and added interventions throughout the course of the study with a goal of improving breastfeeding in our RPC Level IV NICU. Eligible infants were identified by reviewing the daily admission log. Data were extracted from medical records and summarized by using mean and standard deviation for continuous variables and analyzed by analysis of variance (ANOVA) and post hoc comparison with Tukey's honest significant difference test, while categorical variables were analyzed by chi-squared or Fisher's exact test with Bonferroni correction. In addition to comparing categorical outcome variables between different epochs, we tested for linear trends in proportions using the appropriate extension of the test of proportions. A p-value of <0.05 was considered statistically significant. Data were analyzed using R, version 3.6.2 (R Foundation for Statistical Computing, Vienna, Austria, 2019). 38
Results
Four hundred twenty-three ELBW infants were included: 102 infants in B, 84 infants in T, 75 infants in LG, and 162 infants in C epochs. The clinical and demographic characteristics of the maternal and infant study population did not differ significantly across epochs (Tables 1 and 2). The primary outcome of exclusive MOM at discharge increased overall from 18% in B, 13% in T, 29% in LG, and 30% in C epochs. There was a statistically significant trend of increasing MOM exclusivity at discharge over time. HM as the first enteral feed (via a nasogastric tube or orally) was progressively higher by epoch (39% B, 46% T, 93% LG, and 100% C, p < 0.05). HM diet at full feed was also significantly higher in LG and C (96% and 100%, respectively) epochs compared with B and T (36% and 35%, respectively) epochs. In LG and C epochs, 99% and 100%, respectively, of infants received HM (MOM or PDHM) during hospitalization, which is significantly above the WHO 2020 Healthy People target for term infants (81.9%) 8 (Table 3).
Maternal Demographics of Study Population
Race was self-reported.
p-Value <0.05 for significant difference (ANOVA for continuous data or chi-squared/Fisher's exact test for categorical data with Bonferroni adjustment).
LG, Liquid Gold; SD, standard deviation.
Neonatal Characteristics of Study Population
Bold values represent statistically significant p-values.
There was a statistically significant difference in EUGR in the C epoch compared with B and T epochs, with p ≤ 0.0001, which was not seen when the LG epoch was compared with B, T, or C epochs.
p-Value <0.05 for significant difference (ANOVA for continuous data or chi-squared/Fisher's exact test for categorical data with Bonferroni adjustment).
p-Value <0.05 for significant trend (chi-squared test for trend in proportions).
ANOVA, analysis of variance; APGAR, Appearance, Pulse, Grimace, Activity, and Respiration; B, baseline; BW, birth weight; C, current; DC, discharge; EUGR, extrauterine growth restriction; GA, gestational age; HC, head circumference; LG, Liquid Gold; NA, not applicable; SD, standard deviation; SGA, small for gestational age; T, transition.
Breastfeeding Outcomes
There was a statistically significant difference between all epochs except between B and C.
There was a statistically significant difference in the % of infants on HM by full feeds between epochs B and T when either was compared with the LG or C epoch, with p ≤ 0.0001, which was not seen when the B epoch was compared with T epoch or the LG epoch was compared with C epoch.
A statistically significant difference was seen only between T and C epochs.
p-Value <0.05 for significant difference (ANOVA for continuous data or chi-squared/Fisher's exact test for categorical data with Bonferroni adjustment).
p-Value <0.05 for significant trend (chi-squared test for trend in proportions).
ANOVA, analysis of variance; DC, discharge; HM first, human milk at first feed; LG, Liquid Gold; MOM, mother's own milk; NA, not applicable; T, transition.
Among infants in the LG epoch, the first feed was predominantly MOM (78%), with only 22% of infants receiving PDHM. In the C epoch, the use of PHDM at first feed increased to 55%, and although not an intended effect, it allowed for complete elimination of formula. The main benefit of PDHM in preterm infants is a reduction in the incidence of NEC, particularly when compared with formula feeding.31–33 We observed a steady reduction of NEC, although the study was not powered to detect significance (15% in B, 11.8% in T, 13% in LG, and 10.4% in C).
During the LG epoch, AA mothers had a significant surge in breastfeeding initiation (78%), higher than any other racial group (Hispanic mothers 53% and White mothers 50%), which was not sustained in the C epoch when the rate decreased to 30%. We postulate that this effect may have been due to the presence of an AA LC and an AA neonatal fellow in the LG epoch.
The most encouraging result seen over time was in the increased percentage of AA mothers providing exclusive MOM (16% in LG and 28% in C) and any MOM (32% in LG and 54% in C) and in the decline of exclusive formula use (68% in LG and 46% in C) at discharge. Hispanic mothers maintained their breastfeeding initiation rates (53% in LG versus 50% in C), but increased their exclusive formula use at discharge over time (36% in LG versus 50% in C). White mothers not only maintained similar rates of initiation and sustainment over time but also had a decrease in exclusive MOM at discharge (50% in LG versus 37% in C) (Fig. 1).

Breastfeeding rates at first feed and at discharge by race in the LG and current epochs. *p-Value <0.05. C, current; LG, Liquid Gold; MIXED, mixed diet of MOM and formula; MOM, mother's own milk; PDHM, pasteurized donor human milk.
There was no statistically significant change in the rates of ROP, IVH, late-onset sepsis, or NEC in our patient population. A statistically significant trend was noted for survival to discharge (83% in B, 85% in T, 88% in LG, and 96% in C) (Table 2).
Discussion
This quality improvement study is the first to demonstrate the positive effect of a comprehensive lactation bundle in increasing the rates of exclusive MOM diet at discharge over the course of the entire hospital stay of ELBW infants. Previous quality improvement initiatives focused on VLBW infants and aimed to increase either HM within the first 14 days of life 24 or the rate of receipt of any MOM at discharge. 25 Similar to our findings, Kalluri et al. found an improvement in the initiation of breastfeeding with early implementation of breastfeeding support in a racially diverse NICU similar to ours. Bagga et al. further showed successful initiation and sustainment of exclusive breastfeeding at discharge in mothers of VLBW infants through continuous quality improvements in a Level III NICU in India. Both authors outline the unique barriers to breastfeeding that mothers of premature infants face, which often preclude them from successfully initiating and sustaining breastfeeding.39,40 Studies have shown that multimodal approaches to breastfeeding, including peer counseling, breastfeeding teams, and hospital policy changes, yield better results than singular interventions in overcoming barriers to breastfeeding and improving infant health outcomes.26–35,39,40
AA mothers face unique barriers to breastfeeding. Support from family, specifically fathers and maternal grandmothers, and friends; attendance of childbirth classes; and community support during prenatal and postnatal periods have been shown to be effective in improving breastfeeding rates among AA mothers.10–13 However, these are not always available. By establishing institutional policies and procedures, we were not only effective in putting forth a consistent message on breastfeeding for our mothers of ELBW infants but also in providing basic information on the immense importance of breast milk and its personalized medicinal properties. Once management of HM feedings in the NICU is seen as no different from any other care issue, any conflicting advice that families might get about breastfeeding is eliminated. In our RPC, we addressed the institutional barriers of inadequate staff knowledge about the benefits of HM for the ELBW infant by developing an online staff training module with pre- and post-tests. This training ensured that all nursing staff and members of the health care team became more informed and consistent in supporting the breastfeeding mother during each and every encounter.
We speculate that the focus on early colostrum collection and mothers' participation in COC will lead to stimulation of lactogenesis and provide added motivation and engagement, further boosting maternal breastfeeding success. All of our infants received COC within 24 hours of life and continued until the first oral feed. Colostrum provides several immunobiological factors, including secretory IgA, growth factors, lactoferrin, anti-inflammatory cytokines, and oligosaccharides—all of which play an important role in preventing infection and inflammation. Colostrum primes the ELBW infant's gut, increasing the diversity of its microbiota.27–30
The availability of PDHM has also been a vital component of our lactation bundle, allowing every ELBW infant to receive exclusive HM as the first feed. A national report by the CDC showed that all preterm infants when compared with term infants are less likely to receive HM, with AA and American Indian/Alaskan Native infants particularly affected by this disparity. 41 In our NICU, PDHM is offered as a “bridge” until MOM “comes in.” Its increased use in the C epoch was not associated with decreased MOM at discharge. It was particularly effective in supporting AA mothers who, although experiencing a drop in MOM at first feed, increased their provision of MOM by discharge and decreased the use of formula.
Previous studies have shown that countries with a high ratio of LCs had a higher prevalence of breastfeeding at 6 weeks and significant cost benefit attributed to reduced infant morbidities. Positive correlations have been seen in NICUs with dedicated LCs in increasing breastfeeding rates through discharge.34–37 In our own institution, we have seen an increase in the percentage of neonates receiving any HM, especially in the outborn population, 37 with the addition of a dedicated LC. We were able to financially support increase in LC staffing by receiving grants from the W.K. Kellogg Foundation, Heckscher Foundation, and Countess Moira Foundation, as well as through income generated from outpatient lactation consults. With this staffing, we were able to provide outpatient and inpatient antenatal counseling as well as postnatal counseling to mothers while their babies were in the NICU. Many mothers change their predelivery breastfeeding goals after giving birth to a preterm infant and a focused lactation support during this critical period has the potential to change their narrative. 42 Due to financial restrictions, we still do not have LCs on night and weekend shifts and many mothers are only able to visit the NICU during these hours. This lapse in staffing may be limiting our success in sustaining breastfeeding. During the COVID pandemic, two of our LCs moved to telemedicine lactation and reported being able to reach more mothers in the comfort of their own homes. We are currently evaluating the effects of this service.
The composition of our team changed during the C epoch, with two AA providers—an LC and a neonatal fellow—retiring and graduating, respectively. We speculate that their presence may have contributed to the significant increase in breastfeeding initiation in AA mothers during the LG epoch. It is unclear if this observation is a result of AA mothers having more confidence in, or less hesitation to engage with, AA providers; whether AA providers are more likely to gravitate toward AA mothers; or whether there may be an implicit bias with non-AA providers. Our study was not designed to discern this effect, but future studies should explore a possible correlation. Nonetheless, the overall provision of MOM by AA mothers at discharge increased (28% exclusive and 26% mixed) despite an observed delay in initiation of breastfeeding (30%), underscoring the positive effects of the bundle on sustainment of breastfeeding (Fig. 1).
Early antenatal counseling in L&D was provided in the C epoch with a particular focus on mother's vital role in providing nourishment for her infant, especially the first feed. This assisted mothers in rewriting their pregnancy narrative, from self-guilt and feeling of failure to empowerment, by emphasizing their role in providing breast milk and its attendant benefits to their infants. Our LCs were also available to assist mothers with their first milk expression and often delivered colostrum to the infant's bedside in the NICU, while educating mothers about the benefits of breast milk for the health of their baby and themselves. Additionally, the antenatal consults addressed the mothers' concerns, which included coping with breastfeeding and pumping and the fear that their bodies would fail them with inadequate milk supply after being unable to carry their baby to term.
Our comprehensive bundle was successful in provision of HM to 100% of ELBW infants at first feed and full feeds. However, we found that the rate of MOM at discharge plateaued at 30% overall. Even in a traditionally probreastfeeding culture, researchers in Sweden have found that over the past 10 years, exclusive breastfeeding rates at discharge have been decreasing, especially in extremely preterm infants. They have speculated that increased attention to postnatal weight loss and increased fortification practices with introduction of formulas to promote optimal growth are undermining mothers' expectations and triggering insecurity and doubt about the quality of their milk. Other factors such as single-family rooms may be isolating mothers from other NICU mothers and decreasing staff availability. 43 Furthermore, the rates of initiating and sustaining breastfeeding in our study differed significantly among racial groups. Racial disparities in breastfeeding rates are associated with higher rates of infant morbidities in minority groups.10–12 When compared with Hispanic and White mothers, AA mothers experienced the greatest increase in the provision of their own milk at discharge, suggesting that a multimodal approach may be especially effective in helping AA mothers overcome unique obstacles to sustaining breastfeeding.
We did not specifically target any racial group, but hypothesized that a language barrier could hinder the engagement of Spanish-speaking mothers. Spanish-speaking Hispanic mothers are more likely to initiate, intend, and maintain breastfeeding compared with English-speaking Hispanic, White, and AA mothers. 11 For this reason, we added a Spanish-speaking LC during the C epoch. However, we found no improvement in the rate of breastfeeding in Hispanic women, suggesting that the language barrier may not be the primary impediment to encouraging Hispanic women to breastfeed. There is growing concern for the negative effect of acculturation on breastfeeding among the heterogenetic group of Hispanic mothers. 10
One of the limitations of our bundle was the absence of trained peer counselors. Previous studies have shown that peer counselors play an integral role in successful breastfeeding initiatives in predominantly AA populations.31,34 Former NICU mothers were found to be able to effectively support less experienced mothers, demonstrating the importance of establishing a supportive community. 34 We are currently seeking methods to engage family members and partners in providing personal and ongoing support to our lactating mothers. Our study was also not powered to assess the effects of individual components of the bundle or the effects of maternal socioeconomic status. Using Medicaid as a marker of socioeconomic status, the proportion of mothers on Medicaid in our NICU remained the same at 68%. Although additional unidentified factors such as the effect of public awareness campaigns, social media/private support groups, and prior breastfeeding experiences and other individual factors may have influenced the observed breastfeeding outcomes, it would be impossible to elucidate their independent influence. The increasing access to social media appears to be a double-edged sword—not only increasing access to care and support groups and opportunities for education but also potentially increasing anxiety, peer pressure, and insecurities rooted in unrealistic comparisons and expectations. In the absence of adequate societal and social support in our growing socially distanced communities, a multicomponent lactation bundle is essential in supporting mothers to achieve their greatest individual breastfeeding potential.
Conclusions
Our comprehensive, evidence-based Liquid Gold bundle improved breastfeeding rates in mothers of ELBW infants at an RPC Level IV NICU. The greatest increase in MOM provision and greatest reduction in formula use were seen in AA mothers of ELWB infants. Our findings raise the possibility that the ethnicity of the provider may play a role, particularly in initiation of breastfeeding, and a multicomponent support bundle is essential for providing mothers with the best chance for breastfeeding success. The results of our bundled approach are promising and may be particularly useful at other institutions in communities with significant racial disparities.
Footnotes
Acknowledgments
The authors are deeply indebted to the families who entrusted the care of their infants to them. This work would not have been possible without the support of the entire NICU staff—nurses, nurse practitioners, physician assistants, dieticians, and physicians.
Disclosure Statement
B.P. has received grants from the Kellogg Foundation and Heckscher Foundation to establish a hospital-based preterm milk bank. This article does not contain a discussion on any unapproved or investigative use of a commercial product or device. All other remaining authors cite no financial disclosures related to the conduct of this study or preparation of this article.
Funding Information
This study was supported by restricted grants from the Kellogg Foundation and Heckscher Foundation.
