The Experience of Human Milk Banking for 8 Years: Korean Perspective

Breast milk has all the nutrients and protective immune components that infants need for healthy development, and seems to decrease the risk of allergic and infectious diseases, such as otitis media, and gastrointestinal tract and respiratory disease in infancy (1, 2, 3, 4). Components of breast milk, such as immunoglobulins, lactoferrin, lysozyme, oligosaccharides, nucleotides, growth factors, enzymes, antioxidant factors, and cellular components, provide adequate host defense against infections, actively regulate the immune response, and modify intestinal bacterial colonization. Breastfeeding is the most suitable source of nutrition for preterm infants, and aids the cognitive development of premature babies; the psychological advantages have a positive effect on long-term prognosis (5, 6, 7). Thus, it is generally accepted that mother’s milk is the best single source of nutrition for the first 6 months of life and is the optimal diet for healthy infants for the first 2 or more years of life (8, 9, 10).

However, sometimes a mother’s own milk is unavailable or insufficient for numerous reasons despite the benefits of breast-feeding, and infants are often fed artificial formula. The World Health Organization (WHO), the United Nations International Children’s Emergency Fund (UNICEF), and the American Academy of Pediatrics (AAP) state that the use of donor human milk should be the first alternative when maternal milk is not available, particularly for preterm neonates (11, 12). A human milk bank (HMB) systematically collects, screens, processes, and dispenses excess human breast milk donated by healthy nursing mothers (13).

In 2010, we reported 2-year data for the HMB in the Kyung Hee University Hospital at Gangdong, from August 2007 to August 2009 (14). This is the second time that data about breast milk donors and recipients were collected as part of this survey. We report the operational status of the HMB for 8 years (from 2008 to 2015) in this hospital, to determine the direction of development and growth of the HMB.

The HMB in Kyung Hee University Hospital at Gangdong was opened in August 2007, and is a nonprofit milk bank that accepts donations of surplus milk from healthy breastfeeding women and dispenses donor human milk, primarily to premature and ill infants. This is the first established nationwide HMB in a Korean university hospital, and is still the only national level HMB in Korea. Our HMB follows the annually revised “Guidelines of Human Milk Banking Association of North America (HMBANA).” Target users of our Guidelines are health care workers of the HMB, nurses and doctors of the neonatal intensive care unit (NICU), and administrators of the HMB. As part of the process of this HMB, donors are checked for eligibility. Safety checks are performed on collected breast milk from qualifying donors. At this time, unsuitable breast milk is discarded, and safe milk is pasteurized and provided to recipients. Table 1 shows the processes.

Table 1
Summary of the operation of a human milk bank in Kyung Hee University Hospital at Gangdong, Seoul, Korea

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A donor is excluded if she has received an organ/tissue transplant within the prior 12 months or blood transfusion/blood products within the prior 4 months; regularly takes more than 2 ounces of alcohol or its equivalent, or 3 caffeinated drinks per day; uses illegal drugs, tobacco, or nicotine products; is taking radioactive or other drugs, has chemical or environmental exposures, or takes over-the-counter prescriptions or megadoses of vitamins known to be toxic to the neonate and are excreted in breast milk, and/or herbal products used as medication; has a positive blood test result for human immunodeficiency virus (HIV), hepatitis B virus (HBV), hepatitis C virus (HCV), or syphilis; has a history of leukemia or lymphoma, or treatment for any other cancer within the prior 3 years; has a sexual partner with HBV, HIV, HCV, or sexually transmitted infections, or if either partner has high-risk behavior for contracting these in the prior 12 months; has had tattoos with non-sterile needles or dyes used by multiple persons at an unregulated site, permanent makeup applied with nonsterile needles, ear or other body parts pierced with other than single-use instruments in the prior 12 months; has mastitis or fungal infection of the nipple or areola, active herpes simplex or varicella zoster infections in the mammary or thoracic region; is a strict vegetarian who does not supplement their diet with vitamin B12; or has been incarcerated or has had a sexual partner who was incarcerated for more than 72 consecutive hours in the prior 12 months (11, 15, 16, 17).

In this study, we reviewed the basic characteristics of donors (regional distribution, age, occupations, motivation and information on donation, donation time after delivery) and recipients (regional distribution, age), the number of donors and recipients, frequency of donation, amount of human milk for collection and processing, bacterial contamination rate of donor milk after pasteurization, donor milk containing cytomegalovirus (CMV) before pasteurization, indication for receiving donated milk, and additional issues to be resolved between January 2008 and December 2015. A standardized data form was used to collect information from the HMB.

After passing the exclusion criteria, all milk samples are transported to the milk bank, frozen, and maintained in freezers at −20°C for up to 6 months. Frozen milk samples are thawed in batches at 1°C–4°C and processed by the pasteurization standard for bottled human milk. Before processing, 3–4 samples from each individual donation are mixed to obtain homogenous fat contents and wide range of immune mechanisms, thereafter sent to the microbiology laboratory in the hospital to be screened for CMV using a real-time polymerase chain reaction (PCR) assay. After processing, pasteurized milk undergoes bacteriological testing to ensure the absence of detectable bacterial growth. In the hospital microbiology laboratory, each milk sample was inoculated onto blood agar plate and incubated aerobically at 36°C for 48 hours (11, 15, 16, 17, 18). All contaminated milk is discarded.

The benefits of breast milk are widely known. The Baby Friendly Hospital Initiative (BFHI) by WHO/UNICEF recommends that newborns be breastfed within 30 minutes of birth, and exclusively breastfed until 6 months of age. Breast milk is a superior nutritional source that contains high levels of important immunological components that protect against infections. In addition, breastfeeding promotes emotional and motor development in babies (19, 20). Breastfeeding also reduces the risk of necrotizing enterocolitis, sepsis, retinopathy of prematurity, and hospital readmission of preterm infants after discharge (12, 21).

Unfortunately, there are circumstances where mothers are not able to breastfeed their babies for a number of reasons despite the various benefits. Commercial infant formula is a common replacement for breast milk in these instances. However, donor breast milk can be an excellent alternative to formula. The role of an HMB is to ensure that this alternate route to breastfeeding is safe and efficient. On-line breast milk transactions have recently increased as a result of internet promotion and increasing awareness of the benefits of breast milk. However, such transactions include the risks of infection and spoilage (22). Therefore, donating and receiving breast milk through an HMB is essential.

The first HMB was founded in 1909 in Vienna, Austria. The USA, Germany, and the UK followed shortly thereafter. However, early HMBs were not equipped to provide systematic and sanitary processing of breast milk. In 1985, the modern Human Milk Banking Association of North America (HMBANA) was founded in an effort to establish necessary standards for safe and efficient milk banking. Upon the establishment of standardized guidelines, human milk banking took off full force (14, 16). In the mid-1980s, with the advent of AIDS (Acquired Immune Deficiency Syndrome), stringent blood testing, and donor screening, many HMBs closed. Since the 1990s, research on the safety of breast milk and breastfeeding has prompted active plans to establish HMBs in many developed countries around the world (23). In many countries, HMBs have been incorporated into child health policy and are protected, promoted, and supported as an extension of national breastfeeding policies (13, 24, 25, 26). Currently, there are 24 established and 5 developing HMBs in North America and 210 active and 17 planned HMBs in Europe. Brazil is an international leader, with 217 HMBs and 162 collection centers distributed throughout the country in 2012 (27, 28, 29).

The first HMB in Korea was founded in 2007 by the Children and Maternal Health Center of Gangdong Kyung Hee University. Other HMBs currently in operation in Korea include one run by the Seoul Injeong Hospital, Incheon’s “Shared Love” milk bank (the only milk bank run by an Oriental medicine clinic), and one run by the obstetric department of Jeonbuk Iksan Jeil hospital, all of which operate in cooperation with the Korea Breastfeeding Association. The HMB process in Gangdong Kyung Hee University is as follows. Collected breast milk is processed in a designated area by staff members wearing face masks, aprons, and sanitary gowns. The milk is kept frozen at −20°C. Breast milk collected from a minimum of 3 individuals is thawed at 1°C–4°C for 3 days. Thawed breast milk subsequently goes through a process of mixing and pooling which ensures homogenous nutritional composition and immunological properties. Mixed breast milk is distributed in sterilized glass containers and pasteurized at 62.5°C for 30 minutes. The pasteurization process is designed to eliminate the risks of infection including HIV and CMV (30). Pasteurized breast milk is then rapidly cooled in an ice bath for 30 minutes to ensure an effective vacuum seal. Samples of processed breast milk are selected for microbiological examination including bacteria. If safety is proven, the milk is kept frozen at −20°C until use. Each container is labeled with an expiration date 6 months from the date of bottling. Recipients apply for the program via telephone calls. The first priority is given to premature infants in clinics, followed by infants in the NICU, infants with formula allergies, adopted infants or infants whose birth mothers passed away, and adults who are receiving cancer treatment.

Following the above described process, a total of 916 donors participated in the milk banking program run by Gangdong Kyung Hee University during the 8-year period between 2008 and 2015, with a total of 1,724 donations and an average of 1.9 donations per donor. The total amount of donated breast milk during the 8-year period was 10,820 L, 9,541.6 L of which was processed. In the beginning, the number of new donors and the number of donations increased each year, which is attributed to active promotion efforts via websites, internet cafes, media coverage, and various expos. The increasing trend in donors and donations between 2008 and 2011 started to decline afterwards, and peaked again in 2015, suggesting that human milk banking did not achieve steady quantitative growth. Considering the fact that 76% of donors are inspired by on-line sources, greater promotional efforts will have to be invested in electronic sources including the internet. In addition, promoting milk banking and improving accessibility through various events designed to attract pregnant women and breastfeeding mothers in their 20s and 30s appears to be critical for continued growth of milk banking. In terms of donor occupations, although stay-at-home mothers accounted for the majority at 62.3%, working mothers and students accounted for 37.7% of the total, suggesting that their participation is important. As for geographical distribution of donors, Seoul, Gyeonggi-do, and Incheon areas accounted for a significant majority at 71.3%. However, other areas supplied 28.7% of the total, indicating nationwide participation.

Bacterial growth was positive in 12.6% of processed breast milk. HMBs in many other countries perform bacteriological screening both before and after processing (18, 31). However, we perform screening only after processing as a way to reduce cost and deal with a shortage of healthcare professionals. Although precise statistics have not been calculated, most cases involved Bacillus species. Spore-forming Bacillus species are known to survive routine Holder pasteurization, but unlike cow’s milk, this is a rare contaminant of human breast milk and is detectable by surveillance cultures performed before and after pasteurization (32, 33). CMV tested positive in 52.5% of breast milk before being processed. CMV disease caused by postnatally acquired infection is uncommon in full-term infants, presumably because of protection from passive transfer of maternal antibodies that occurs mostly in the third trimester, and the infant’s more mature immune system (34, 35). However, infants born at less than 32 completed weeks of gestational age or very low birth weight (VLBW) infants (< 1,500 g) may be at higher risk of developing symptomatic postnatal CMV disease, characterized by hepatopathy, thrombocytopenia, neutropenia, petechiae, respiratory distress syndrome, and a sepsis-like syndrome (36). Therefore, our HMB only provides breast milk tested negative for CMV to infants born at less than 32 completed weeks of gestational age, or to VLBW infants until 34 completed weeks of corrected age.

During the 8-year period, a total of 861 recipients benefited from donated human milk, including 836 infants (97.1%) and 25 adults (2.9%). Breast milk was provided to a relatively wide range of age groups, and 63.9% was distributed to infants aged 0–3 months. A total of 8,174.7 L of donor milk was supplied during the 8-year period. A total of 1,544 distributions were made, for an average of 5.3 L per person. The most common reason for receiving donated breast milk was a premature baby, which appears to be growing in proportion in recent years. Although the majority of the recipients were preterm infants, donor milk was also being ordered for babies and children for a variety of other reasons, including adoption, atopic dermatitis, baby’s refusal of formula, milk allergy, decreased amount of mother’s breast milk, and mother receiving chemotherapy for cancer or underlying diseases. A notable trend in recent years is that premature babies made up a significant proportion of recipients. The survival rate in premature babies born with respiratory issues has increased due to advances in respiratory treatment, but necrotizing enterocolitis (NEC) is still a major factor in neonatal morbidity. According to guidelines, early trophic feeding using breast milk helps reduce the risk of NEC (12, 37). However, most donor breast milk is provided by women who have delivered at term and they donate their milk in later lactation. Several months after delivery, this milk from mothers of term infants is low in protein, fat, and many bioactive molecules compared to preterm milk provided in the first few weeks after delivery and pasteurization has detrimental effects on the bioactive components of human milk and results in significant decreases in sIgA, lactoferrin, lysozyme, insulin-like growth factors, hepatocyte growth factor, water-soluble vitamins, bile salt-stimulated lipase, lipoprotein lipase, and anti-oxidant activity (6, 38). Pasteurized donor breast milk is therefore likely to be less beneficial than mother’s own unpasteurised milk, and the maximum effort should always be put in supporting and promoting breastfeeding mother’s own milk prior to donor breast milk being used. However, because preterm infants stay in the NICU and spend long hours separated from their mothers, breastfeeding becomes more challenging than breastfeeding full-term infants. Therefore, breast milk whose safety has been verified by HMBs is especially needed for preterm infants, and clinics with a NICU should consider having an HMB on site (39).

Our HMB provides a free shipping unit to mother’s home to collect all the milk who are interested in donating and accept frozen breast milk expressed prior to the screening as well as long as it has not been frozen for over 3 months using post office home-delivery. The post office’s great assets are the door-to-door delivery system and speedy delivery service of a day. Quite a few area are inaccessible, however, we cannot accept their breast milk even though there are mothers who want to donate.

In 2015, there were 13 hospitals in the Seoul/Gyeonggi area receiving donor breast milk from the HMB in the Kyung Hee University Hospital at Gangdong. Breast milk demand for bank milk exceeds expectations yearly especially for preterm babies, and donations even have exceeded our processing capacity. Current fund for operation of our HMB was mostly from the Kyung Hee University Hospital at Gangdong. We cannot expand HMB space or buy refrigerators anymore. Maybe it is time to concern how ethically to allocate this scarce resource.

Fees generated from our banked milk are $2.80/100 mL for babies in outside hospitals and outpatients, and free for babies in NICU at Kyung Hee University Hospital at Gangdong. The processing fee of each month in the HMB is around $1,730 except personnel expenses. We want to obtain better quality control on operation and less loss of milk nutrients to benefit all infants and aim to analyze the nutritional components of the donor milk, and distributed to preterm babies at different stages individually. However, a single institution’s effort is not sufficient for quantitative and qualitative growth in milk banking. Sustainability and quality improvement of the milk bank need long-term financial support by health authorities.

There is a growing body of evidence and expert opinion to support the use of donor human milk for hospitalized preterm or sick infants. A great deal of human resources, equipment, costs associated with testing and logistics are required to operate HMBs, which is a factor impeding proliferation of new milk banks. Meeting the growing demand for donor human milk will require leadership organizations and health care professionals at the national and local levels to develop strategic initiatives for new milk banks as well as increasing the number of breastfeeding mothers who donate milk. However, there are no governmental models that incorporate the need for donor milk into comprehensive breastfeeding strategies for improving maternal and child health outcomes. Thus, local governmental-level funding is necessary. Additionally, establishing a nationwide network similar to blood banking will further contribute to the progress of milk banking. It is expected that Gangdong Kyung Hee University’s milk bank will serve as the hub of progress based on the past 9 years of experience as the nation’s leader in milk banking.