Comparative Growth Outcomes in Preterm Infants Fed Either Mother's Own Milk or Donor Human Milk

Abstract

Objective:

To compare growth velocity (GV) in preterm infants fed mother's own milk (MOM) fortified with human milk-based fortifier (HMBF) to those who received donor human milk (DHM) fortified with HMBF.

Study Design:

A retrospective study of preterm infants with birth weight <1,250 g receiving an exclusive human milk diet. Maternal and infant charts were reviewed for feeding, growth, and short-term neonatal morbidities.

Results:

On regression analysis, after adjusting (gestational age, multiple births, antenatal steroids, and small for gestational age), no significant difference was observed between the two groups in GV from birth to 32 weeks postmenstrual age (β-coefficient 0.83, 95% confidence interval [CI]: −0.47 to 2.14, p = 0.21), GV from the day of regaining of birth weight to discharge (β-coefficient −0.015, 95% CI: −1.08 to 1.05, p = 0.98). The rate of Grade 3 and 4 intraventricular hemorrhage was significantly higher in the DHM group (19.6% compared to 5.5% in MOM, p = 0.03).

Conclusion:

At our institution, there was no difference in GV of preterm infants fed HMBF-fortified MOM versus HMBF-fortified DBM.

Introduction

Breast milk is considered the best form of nutrition for all infants.¹ It positively impacts the health outcomes in preterm infants; a lower incidence of sepsis, chronic lung disease of prematurity, necrotizing enterocolitis (NEC), retinopathy of prematurity (ROP), mortality, and improvement in neurodevelopmental outcomes have been reported in preterm infants fed human milk.^2–7 Donor human milk (DHM) has been recommended by the American Academy of Pediatrics (AAP)² World Health Organization (WHO)⁸ and the European Society for Pediatric Gastroenterology, Hepatology and Nutrition (ESPGHAN)⁹ as the preferred alternative to mother's own milk (MOM), when MOM is unavailable or is contraindicated, in low birth weight (WHO) and preterm (AAP, ESPGHAN) infants.

Several studies have reported inadequate weight gain in preterm infants with DHM compared to MOM and preterm formula.^10–15 DHM, obtained from mothers of term infants, is pooled, and subjected to screening and pasteurization to ensure safety. This causes alteration in its biological quality and micro and macronutrient composition. Compared with preterm mothers' milk, processed DHM has lower protein and lipid content, decreased Immunoglobulin A, Immunoglobulin G, and lactoferrin concentration, no Immunoglobulin M antibodies, B- and T-lymphocytes, loss of lipase and erythropoietin activity, and changes in microbiota—all these factors can impact growth and other advantages afforded by MOM.^16–18

DHM was introduced in our institution in 2019 for feeding preterm infants with birth weight <1,500 g and gestational age (GA) <32 weeks when MOM was not available. We use human milk-based fortifier (HMBF) for all infants receiving MOM or DHM. We previously reported that growth velocity (GV) and other short-term outcomes did not differ between preterm infants who received formula or MOM.¹⁹ However, there is scarcity of data on growth outcomes in infants receiving exclusive human milk diet with MOM and DHM. Our current study was aimed to compare GV and short-term neonatal outcomes in preterm infants who received MOM to those who received DHM.

Materials and Methods

This was a retrospective single-center cohort study conducted at Hutzel Women's Hospital, Detroit. Institutional Review Board approval was obtained from Wayne State University before study initiation. Infants, born between 2013 and 2021 with birth GA ≤29 6/7 weeks and birth weight ≤1,250 g and survived to discharge were included in the study. Infants who received DHM fortified with a HMBF were compared with infants who received MOM fortified with HMBF. We started using HMBF in 2013 at our institution for infants who were receiving MOM. DHM has been available at our institution since January 2019 for preterm infants and is used when MOM is unavailable or is contraindicated. The infants on DHM included in our study were born between 2019 and 2021 whereas the infants on MOM were born between 2013 and 2021.

Our feeding guidelines were implemented in 2013 and there were no changes until 2021 except addition of HMBF in 2013 and DHM in 2019. Infants who received bovine milk-based fortifier (BMBF), mixed human and formula feeds, or mixed MOM and DHM feeds before 32 weeks postmenstrual age (PMA) were excluded from our study. We also excluded infants with chromosomal/major congenital anomalies, with missing data, and those who were transferred out.

We follow a standardized feeding protocol at our institution. DHM is obtained from commercial milk bank (Prolacta+ H2 MF; Prolacta Bioscience, Monrovia, CA). HMBF, obtained from the same milk bank, (Prolacta+ H2 MF; Prolacta Bioscience) is used for fortification in infants who receive human milk (MOM/DHM). Fortification is usually done when infant tolerates 80–100 mL/(kg·d) of enteral feeds. Parental consent is obtained before initiation of DHM or HMBF. Infants on DHM are transitioned to preterm formula at 32 weeks PMA over a period of 3 days. Similarly, for infants on MOM, HMBF is substituted with BMBF at 32 weeks PMA.

Maternal charts were reviewed for demographics, including maternal age and race; medical history, including prenatal care, insulin dependent diabetes, pregnancy induced, and chronic hypertension, Group B Streptococcus colonization and delivery history for mode of delivery, prolonged rupture of membranes (>18 hours), administration of antenatal steroids, indomethacin, magnesium sulfate and antibiotics. Data collected from infants' charts included birth GA, sex, APGAR scores at 1 and 5 minutes, small for gestational age (SGA) status (defined as <10th percentile for GA); feeding history for day of initiation of feeds, time to full enteral feeds, number of Nil per Oral (NPO) days, day of fortification, parental nutrition days.

Other information collected include central line days, hospital length of stay, growth parameters at 32 weeks PMA and at discharge, data on neonatal morbidities, including culture proven early onset sepsis defined as positive blood or cerebrospinal fluid culture within 72 hours of birth, culture proven late onset sepsis (LOS) after 72 hours of birth, administration of surfactant for respiratory distress syndrome, respiratory support after birth, postnatal steroid use, echocardiogram confirmed patent ductus arteriosus (PDA), treatment for PDA and vasopressor use after birth, NEC stage IIa and above, defined by modified Bells Criteria,²⁰ Grade 3 or 4 intraventricular hemorrhage (IVH) using Papile's classification on cranial ultrasound,²¹ and bronchopulmonary dysplasia (BPD) defined as use of supplemental oxygen at 36 weeks PMA and ROP (any stage).

Time to full enteral feeds was defined as the day of life when 100% of caloric requirements of the infant were met by enteral feeds without the need for any intravenous supplementation. NPO days were determined by calculating the number of days feeds were stopped for more than 24 hours.

Our primary outcome was to determine GV from birth to 32 weeks PMA in the two groups. We also compared GV from the time of regain of birth weight to 32 weeks PMA. We chose 32 weeks for comparison as the infants were transitioned to cow's milk/BMBF after 32 weeks. Exponential model was used to calculate GV.²² Z-scores for weight and head circumference at birth, 32 weeks PMA, and at discharge were calculated using Fenton growth chart-based electronic PediTools.²³ Data on linear growth were not reported due to lack of inconsistent length recordings and nonutilization of length boards for measurement of length.

Statistical analysis

All analyses were performed using the software package Stata/IC 16.0 (Statacorp, College Station, TX). Based on data from our center,¹⁹ which showed a mean GV of 10.1 ± 2.6 gm/(kg·d) from birth to 32 weeks in preterm infants fed MOM fortified with HMBF, the total sample size needed for current study was 96 (48 in each group) to demonstrate a 15% difference in the GV in the two groups for a two-sided type 1 error of 5% and power of 80%.

Continuous variables were compared using the Student's t test or Mann–Whitney U test as appropriate and categorical variables were compared using the chi-square test or Fisher exact test. Linear regression analysis was conducted to compare the GV between the groups after adjusting for GA, multiple births, antenatal steroids, and SGA status. These variables were selected a-priori as these are known to affect the growth in preterm infants. A p-value of <0.05 was considered statistically significant.

Results

A total of 106 infants were included in our study: 55 in MOM group and 51 in DHM group. Our study cohort had a mean (standard deviation [SD]) GA of 26 (1.8) weeks and birth weight of 829 (216) grams; 47 (44.3%) were male and 2 (1.9%) were SGA. Table 1 compares the baseline maternal and neonatal characteristics in both groups. There was a significantly higher proportion of multiple births in the MOM group compared to DBM (27.3% versus 9.8%, p = 0.02) and higher proportion of mothers in MOM received antenatal steroids (98.2% versus 88.2%, p = 0.04).

Table 1.

Baseline Characteristics of Study Cohort

Characteristic	MOM (N = 55), n (%)	DHM (N = 51), n (%)	p
Maternal characteristics
Maternal age, mean (SD)	28.5 (6.1)	29.4 (5.3)	0.45
African American race	44 (80.0)	43 (84.3)	0.08
Prenatal care	47 (85.5)	47 (92.2)	0.28
Insulin-dependent diabetes	4 (7.3)	1 (2.0)	0.20
Hypertension	12 (21.8)	17 (33.3)	0.18
Rupture of membranes >18 hours	19 (34.6)	13 (25.5)	0.31
GBS colonization	8 (14.6)	8 (15.7)	0.87
Multiple births	15 (27.3)	5 (9.8)	0.02
Prenatal indomethacin	8 (14.6)	11 (21.6)	0.35
Antenatal steroids	54 (98.2)	45 (88.2)	0.04
Prenatal magnesium	51 (92.7)	47 (92.2)	0.56
Prenatal antibiotic use	52 (94.6)	47 (92.2)	0.58
Neonatal characteristics
GA, in weeks, mean (SD)	25.6 (1.5)	26.6 (1.9)	<0.001
BW in grams, mean (SD)	786 (189)	875 (235)	0.03
Birth head circumference in cm, mean (SD)	22.7 (1.8)	24.1 (2.3)	0.001
Birth length in cm, mean (SD)	32.0 (2.8)	33.6 (3.4)	0.01
Z-score birth weight, median (IQR)	0.04 (−0.45 to 0.59)	0.1 (−0.47 to 0.4)	0.53
Z-score birth length, median (IQR)	−0.39 (−0.69–0.4)	−0.29 (−0.92 to 0.52)	0.80
Z-score birth head circumference
Median (IQR)	−0.32 (−0.74 to 0.41)	0.15 (−0.5 to 0.68)	0.09
Males	28 (51.0)	19 (37.3)	0.16
Cesarean delivery	34 (61.8)	42 (82.4)	0.02
SGA	2 (3.6)	0	0.38
APGAR <5 at 5 minutes	13 (23.6)	10 (19.6)	0.62
Surfactant use	48 (87.3)	44 (86.3)	0.58
Respiratory support after birth			0.03
None	0	1
Noninvasive ventilation	8 (14.3)	17 (33.3)
Mechanical ventilation	47 (85.5)	33 (64.7)
PDA medical treatment	17 (31)	11 (22)	0.21
Surgical closure of PDA	4 (7.3)	9 (17.7)	0.13
Vasopressor use	15 (27.3)	4 (7.8)	0.009
Early onset sepsis	1 (1.8)	1 (1.8)	0.96
Postnatal steroid use	10 (18.2)	4 (7.8)	0.11

Bold values are statistically significant.

BW, birth weight; DHM, donor human milk; GA, gestational age; GBS, Group B Streptococcus; IQR, interquartile range; MOM, mother's own milk; PDA, patent ductus arteriosus; SD, standard deviation; SGA, small for gestational age.

Infants in the MOM group were significantly more immature (mean GA 25.6 weeks versus 26.6; p < 0.001) and had lower mean birth weight (BW) (786 versus 875 g, p = 0.03). A significantly higher proportion of infants in MOM group required mechanical ventilation after birth (85.5% versus 64.7%, p = 0.03) and received vasopressors (27.3% versus 7.8%, p = 0.009) compared to DHM group. No significant differences were observed in the use of postnatal steroids, rate of early onset sepsis, and medical or surgical closure of PDA between the two groups.

Feeding and growth-related outcomes are presented in Table 2. Infants in MOM group regained birth weight later compared to DHM group (12 versus 10 days, p = 0.02) but had fewer NPO days >24 hours (1 versus 5 days, p < 0.001). Fortification of milk was done early in the DHM group (13 versus 21 days after birth, p = 0.01). No difference was noted in central line days or parenteral nutrition days between the two groups. The z-scores for birth weight, length, head circumference, weight at 32 weeks PMA, discharge weight, and head circumference were not different between the two groups.

Table 2.

Feeding and Growth Outcomes During the Hospital Stay

Characteristic	MOM (N = 55)	DHM (N = 51)	p
Day birth weight regained
Median (IQR)	12 (10–15.0)	10 (9–13)	0.02
Mean (SD)	13.2 (4.9)	11.1 (3.9)
NPO >24 hours
Median (IQR)	1 (0–6.0)	5 (3–9)	<0.001
Mean (SD)	2.9 (3.5)	7.2 (7.3)
Parenteral nutrition days
Median (IQR)	22 (17–32)	20 (14–25)	0.50
Mean (SD)	25.6 (11.0)	23.7 (18.2)
Central line days
Median (IQR)	25 (19–35)	21 (16–29)	0.79
Mean (SD)	28.6 (11.5)	27.7 (22.2)
Day of life feeds initiated
Median (IQR)	4 (3–5)	3 (2–5)	0.48
Mean (SD)	4.8 (3.7)	4.2 (5.3)
Postnatal day of fortification, median (IQR)	21 (16–27)	13 (11–22)	0.01
Weight at 32 weeks PMA, grams, mean (SD)	1,230 (201)	1,280 (181)	0.19
SGA at 32 weeks PMA, n (%)	27 (49.1)	19 (37.3)	0.22
Z-score weight at 32 weeks PMA, median (IQR)	−1.29 (−1.80 to −1.02)	−1.18 (−1.55 to −0.87)	0.08
Discharge weight, grams, mean (SD)	2,362 (400)	2,872 (775)	<0.001
SGA at discharge, n (%)	50 (90.9)	40 (78.4)	0.07
Z-score discharge weight, median (IQR)	−1.72 (−2.46 to −1.12)	−1.36 (−1.91 to −0.94)	0.05
Discharge head circumference, cm, mean (SD)	32 (2.0)	33.6 (2.5)	<0.001
Z-score, discharge head circumference, median (IQR)	−1.11 (−1.81 to −0.17)	−0.85 (−1.48 to −0.24)	0.47
Discharge length, cm, mean (SD)	44.5 (3.0)	47.3 (3.4)	<0.001
Weight GV, g/(kg·d) (birth-32 weeks PMA), mean (SD)	10.2 (2.5)	10.2 (3.9)	0.99
Weight GV, g/(kg·d) (birth-discharge), mean (SD)	12.3 (2.1)	12.6 (1.9)	0.48
Weight GV g/(kg·d) (day regain of birth weight −32 weeks PMA), mean (SD)	15.0 (4.8)	15.7 (6.2)	0.53
Weight GV g/(kg·d) (day regain of birth weight—discharge), mean (SD)	14.6 (2.7)	14.5 (2.4)	0.86
Change in weight z-score from birth to 32 weeks, mean (SD)	−1.60 (1.89)	−1.01 (0.76)	0.03
Change in weight z-score from birth to discharge, mean (SD)	−1.76 (0.69)	−1.31 (1.12)	0.01

Bold values are statistically significant.

DHM, donor human milk; GV, growth velocity; IQR, interquartile range; MOM, mother's own milk; NPO, Nil per oral; PMA, postmenstrual age; SD, standard deviation; SGA, small for gestational age.

We did not find any significant difference on unadjusted analysis in the GV from birth to 32 weeks and time of regain of birth weight to 32 weeks PMA. On regression analysis after adjusting for GA, multiple births, antenatal steroid exposure, and SGA status, the results remained unchanged. No significant difference was observed between the two groups in GV from birth to 32 weeks PMA (β-coefficient 0.83, 95% confidence interval [CI]: −0.47 to 2.14, p = 0.21) and from time of regain of birth weight to 32 weeks PMA (β-coefficient 0.46, 95% CI: −1.85 to −2.78, p = 0.69). GV from time of regain of birth weight to discharge was also comparable between the two groups (β-coefficient −0.015, 95% CI: −1.08 to 1.05, p = 0.98).

Short-term neonatal outcomes are presented in Table 3. No difference was noted between the two groups in time to full feeds, length of hospital stay, LOS, BPD, NEC >stage IIa, and any ROP. The rate of severe IVH (≥grade 3) was significantly higher in DHM group compared to MOM (19.6% versus 5.5%, p = 0.03).

Table 3.

Neonatal Outcomes

Characteristic	MOM (N = 56), n (%)	DHM (N = 55), n (%)	p
Time to full feeds, days
Median (IQR)	24 (19–34)	20 (15–25)	0.11
Mean (SD)	27.25 (10)	23.0 (16.4)
Length of stay, days
Mean (SD)	94.9 (38.9)	96 (31.6)	0.87
Late onset culture proven sepsis, n (%)	6 (10.9)	4 (7.8)	0.59
Grade 3 and 4 intraventricular hemorrhage, n (%)	3 (5.5)	10 (19.6)	0.03
Necrotizing enterocolitis (>stage IIa), n (%)	2 (3.6)	5 (9.8)	0.21
BPD, n (%)	29 (52.7)	36 (70.6)	0.06
Any ROP	14 (25.5)	8 (15.7)	0.22

BPD, bronchopulmonary dysplasia; DHM, donor human milk; IQR, interquartile range; MOM, mother's own milk; ROP, retinopathy of prematurity; SD, standard deviation.

Discussion

In our population of “exclusive human milk fed preterm infants,” we demonstrated no significant difference in GV from birth to 32 weeks PMA in infants fed MOM or DHM. The GV remained similar between the two groups from birth to discharge as well. Majority of the infants in both groups were appropriate for gestational age at birth (mean z-score at birth in MOM 0.015 [51%ile], DHM −0.074 [47%ile]). The average weight z-scores dropped at 32 weeks PMA (MOM −1.60 [5.6%ile], DHM – 1.01 [14%ile]) and a further drop was noted at the time of discharge (MOM −1.75 [4%ile], DHM −1.39 [8%ile]) suggesting an increase in the number of SGA infants. The change in z-scores at 32 weeks and discharge was significantly higher in MOM group compared to DHM group.

Extrauterine growth restriction remains a challenging problem in preterm infants.^24,25 Slower growth rate in preterm infants is attributed to inadequate protein and energy intake.^26,27 Our nutrition guidelines recommend starting proteins at 2 gm/(kg·d) in preterm infants immediately after birth. We speculate that other factors, including practice variation among neonatologists such as fluid restriction in some infants leading to lower total calorie intake, possible delayed fortification (20 and 13 days in MOM and DHM respectively), and increasing trend to early extubation resulting in higher calorie consumption, might contribute to postnatal growth failure and increase in the number of SGA infants at discharge.

We use Prolacta in our center that provides standard nutrition. The caloric content in MOM is not constant. It will be different for each mother and will vary from birth to discharge. This may explain a significantly higher drop in weight z-scores at 32 weeks PMA and at the time of discharge in infants receiving MOM compared to those receiving DHM.

The benefits of MOM extend beyond nutritional support. MOM provides factors promoting growth, immune function, and gut microbiota in infants.^28,29 DHM, the best substitute for MOM, may not provide these benefits. DHM is pooled milk obtained from volunteers who delivered healthy term infants. The macronutrient composition and energy density of banked DHM is different from freshly expressed MOM.³⁰ Processing of DHM such as freezing and holder pasteurization may further affect various macro- and micronutrients such as lipid content, immunoglobulins, anti-inflammatory cytokines, various enzymes, growth factors, hormones, and beneficial microbiota.^18,31–34 Together, these can further contribute to the growth deficit in DHM-fed infants.

We had hypothesized that GV in infants receiving DHM will be lower than those receiving MOM. Our study, however, failed to show any difference. Infants in DHM group regained birth weight early (Median of 10 versus 12 days, p = 0.02) compared to MOM. Higher GA and BW in the DHM group can possibly explain this observation. There was better tolerance of MOM compared to DHM as indicated by the number of NPO days that were significantly lower in MOM (mean [SD] days 2.9 [3.5] versus 7.2 [7.3], p < 0.001). We did not find any difference in most short-term outcomes, including LOS or NEC, although our study showed a higher rate of Grade 3 and 4 IVH in DHM infants compared to MOM. However, our study was not powered to evaluate these outcomes.

Few studies comparing DHM to MOM have reported conflicting outcomes. A randomized trial of 243 preterm infants born before 30 weeks GA, comparing MOM, DHM and preterm formula observed a lower incidence of LOS in the MOM group compared to combined DHM and preterm formula groups and no difference in rates of NEC and death between the three groups. No difference in weight gain between MOM and DHM was reported.¹² A prospective observational study of 48 preterm infants born before 32 weeks GA showed that the weight gain from birth to discharge reached statistical significance with increasing percentage of MOM.¹⁴ Another retrospective study of preterm infants with BW <1,250 g observed higher rates of SGA status at discharge in infants who received predominantly DHM compared to MOM.³⁵ A recent systemic review comparing DHM, and MOM found no difference in the incidence of NEC, LOS, BPD, and ROP between the two groups.³⁶

Our study is unique as all the infants received exclusive MOM or DHM—both fortified with HMBF until 32 weeks PMA. Since majority of the infants were getting both parenteral and enteral nutrition until 32 weeks PMA, the weight gain in infants might not be truly reflective of actual contribution of MOM and DHM. We do not have data on relative proportions of total parenteral nutrition and feeds for each day in these infants. Mothers who provide breast milk might be different from the ones who do not. We adjusted for common variables known to affect growth in infants; there still could be some unmeasured confounders. Based on our findings there appears to be no difference in terms of extrauterine growth until discharge between the two groups. The data do provide reassurance on the use of DHM in infants who are not able to receive MOM.

The strengths of our study include a single-center study with a standardized feeding protocol in the neonatal intensive care unit. Exclusion of infants on mixed feeds helps better delineate the effectiveness of DHM compared to MOM. We acknowledge the limitations of our study. A small sample size and predominantly African American infants included in the study might have introduced type 2 error and limit the generalizability of our findings. We use Prolacta DHM in our center that has standardized nutrition. That is not the case for many other donor milk banks that do not provide labeling of nutritional content. This may further restrict the applicability of our results.

The sample size in our study was not adequate to compare and draw meaningful conclusions on rare outcomes in preterm infants such as IVH, NEC, and LOS. Large sample sizes of subjects might be useful as randomization is not possible due to ethical consideration. The effect of DHM on neurodevelopmental outcomes was out of scope of this study. Future studies with adequate sample size and evaluating short-term and long-term neurodevelopmental outcomes will further help in comparing the effectiveness of DHM as an alternative to MOM.

Conclusions

In a single-center study of preterm infants, we did not find any difference in GV and short-term neonatal outcomes between DHM- and MOM-fed infants. When mother's own breast milk is unavailable or contraindicated, DHM can be used as alternative in very low birth weight preterm infants without compromising growth.

Footnotes

Authors' Contributions

P.K.V. and F.E.: Conceptualization, methodology, investigation, data curation, and writing original draft. H.E.: Investigation and data curation. M.L.-B.: Investigation. G.N.: Conceptualization and writing-review and editing. M.B.: Conceptualization, methodology, formal analysis, writing-review and editing, and supervision.

Disclosure Statement

All authors declare no conflict of interest.

Funding Information

No funding received to complete the study.

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