Comparison of Types of Breast Milk Fortification at Discharge from the Neonatal Intensive Care Unit and Breast Milk Feeding Rates and Growth at 4 Months Corrected Age

Abstract

Background:

Effects of breast milk (BM) enhancement on long-term BM feeding in preterm infants discharged from the neonatal intensive care unit (NICU) have not been examined previously. This study compares any BM feeding rates at 4 months corrected age (CA) in preterm infants discharged from the NICU on BM enhancement by fortification of expressed BM with infant formula additives (BM-F) versus BM supplemented with infant formula feeds (BM-S).

Subjects and Methods:

We compared infants born between January 1, 2013, and December 31, 2017, with gestational age <32 weeks or birth weight <1500 g, discharged home on BM-F or BM-S from two NICUs and followed at 4 months CA. Multivariate logistic regression with propensity scoring estimated the adjusted associations between nutrition at discharge and any BM feeding at 4 months CA.

Results:

Two hundred eighty-five infants were followed at 4 months CA. Infants discharged on BM-F were more likely to have mothers with multiple gestation, private insurance and not Caucasian, initiate feeds of human milk, be discharged from NICU-1, and receive any BM at 4 months CA (p < 0.03). No significant difference in growth parameters <10th percentile at 4 months CA was observed between the two groups. After adjusting for confounding factors, discharge from the NICU on BM-F was significantly associated with BM feeding at 4 months CA (odds ratio: 3.89, 95% confidence interval 1.66–9.14, p = 0.002).

Conclusion:

In this observational study, preterm infants receiving BM fortified with formula powder additives at discharge from the NICU had better BM feeding outcomes without poor growth at 4 months CA relative to those infants receiving BM supplemented with infant formula feeds.

Introduction

Human breast milk (BM) is the normative standard for all infant feeding and nutrition. The World Health Organization (WHO) and the American Academy of Pediatrics (AAP) recommend exclusive breastfeeding for the first 6 months of life and continued breastfeeding with the addition of age-appropriate foods for the first year.¹

BM feeding is associated with reduced risk of morbidity and mortality such as otitis media, lower respiratory tract infections, obesity, and sudden infant death syndrome in infants, and breast and ovarian cancer and type II diabetes in mothers.^2–5 In preterm infants at increased risk for short- and long-term morbidities, BM reduces the risk of sepsis, necrotizing enterocolitis, feeding intolerance, readmission in the first year of life, and neurodevelopmental impairment.^6–9 Duration as well as volume of BM feeding are also associated with improved long-term outcomes in preterm infants.⁷ However, compared with their term counterparts, initiation as well as duration of BM feeding in preterm infants is much lower.¹⁰

In preterm infants, although BM is strongly recommended, exclusive BM is often not sufficient to provide the high macro- and micronutrients including energy, protein, fat, calcium, and phosphorus needed for optimal postnatal growth.¹¹ In many neonatal intensive care units (NICUs), enhancement of expressed BM by adding human or bovine milk-based fortifiers is standard of care.¹¹ Despite these nutritional enhancements during the NICU stay, preterm infants continue to be at risk for growth failure at the time of discharge and require postdischarge enhancement of BM to promote continued optimal growth.¹²

There is no consensus on postdischarge nutrition practices for preterm infants discharged from the NICUs. Two methods of BM enhancement including fortification of BM by adding high-calorie nutrients to the expressed BM (BM-F) and supplementation of unfortified BM feeds with bottles of infant formula feeds (BM-S) are commonly used.¹³ However, the effects of these BM enhancement methods on postdischarge BM feeding rates in preterm infants are unknown. The purpose of our study was to compare postdischarge BM feeding rates among very low–birth weight (VLBW, birth weight <1500 g) or very preterm (VP, birth gestational age <32 weeks) infants discharged from the NICU on either BM-F or BM-S enhancement methods.

Materials and Methods

This was a retrospective study of VLBW or VP infants between January 1, 2013, and December 31, 2017, admitted to our two level III or IV NICUs within 7 days of birth, discharged home on any enhanced expressed BM feedings, and followed at 4 (±1) months corrected age (CA). Infants with major congenital anomalies, transferred out of the NICU or expired before discharge, and infants discharged on BM or formula feeds alone were excluded. Institutional Review Board approval was obtained.

Maternal demographics including age, race, medical insurance type, mode of delivery, and presence of multiple gestation were collected. Infant characteristics including sex and gestational age and infant morbidities including respiratory distress syndrome, patent ductus arteriosus, necrotizing enterocolitis (Bell's classification ≥Stage 2), intraventricular hemorrhage (Grade 3 or 4) or periventricular leukomalacia, and length of NICU stay were abstracted from the medical records.

Nutritional characteristics collected during the NICU stay included enteral feeding initiation type: mother's own milk, donor human milk, or formula and exposure to formula in the first 28 days of life (DOL). Information on enhancement of expressed BM and maximum calorie per ounce recommended at the time of discharge was obtained. At discharge, enhancement of BM was achieved by adding infant formula powder to expressed BM or by supplementing unfortified BM feeds with bottles of infant formula. Postdischarge transitional or term infant formulas were used. Infant birth and postmenstrual age (PMA) growth parameters including weight, length, and head circumference at 36 weeks were collected.

At 4 months CA follow-up, nutritional data including type of feedings: BM or infant formula and maximum calorie per ounce, and growth parameters were collected. For growth parameters, percentiles were calculated using the Fenton 2013 growth calculator for birth and 36 weeks of PMA and the WHO Growth Curve Standards for 4 months CA.^14,15

Statistical analyses

Statistical analyses were performed using SPSS V26.0 (IBM, Armonk, NY). The two discharge BM enhancement groups: BM-F and BM-S were compared on maternal and infant characteristics using the chi-square or Fisher exact test for categorical data and the Student t-test for continuous data. To compare groups on BM feeding rates at 4 months CA, a multivariable logistic regression with propensity score covariate adjustment was used.

Propensity scoring was used to adjust for baseline confounding variables associated with discharge BM enhancement type. Propensity scores were calculated from a logistic regression model that gave equal weight to identified risk factors for outcome of interest and were selected a priori. Covariables included in the model were maternal age, race and insurance type, multiple gestation, infant birth weight and gestational age, respiratory distress syndrome, initial feeding type, formula exposure in the first 28 DOL, length of NICU stay, and discharging NICU.¹⁶ Logistic regression with propensity score covariate adjustment was used to evaluate the association between discharge BM enhancement types and any BM feeding rates at 4 months CA follow-up. The Hosmer–Lemeshow goodness-of-fit test was used to assess how well the final model fit these data.

Results

A total of 847 VLBW or VP infants were admitted to our two level III or IV NICUs during the study period. After excluding infants admitted to the NICU after DOL 7, with genetic syndrome, expired or transferred out of the NICU before discharge, or discharged home on unfortified BM or formula alone, 330 (39%) were included. Of these, 45 (14%) infants were not followed at 4 months CA or were lost to follow-up. Of the 285 infants followed at 4 months CA, 147 (52%) were discharged from the NICU on BM-F and 138 (48%) were discharged on BM-S (Fig. 1). Infants lost to follow-up did not differ significantly from infants followed at 4 months CA, except those lost to follow-up were more likely to be born to mothers with state insurance (lost to follow-up: 25, 56%; followed: 102, 36%; p = 0.01).

FIG. 1.

Study population.

Maternal and infant characteristics and infant morbidities for the two study groups, BM-F and BM-S, are shown in Table 1. There were no significant differences in maternal age or mode of delivery between the two groups. Infants discharged on BM-F were less likely to be born to mothers who were Caucasian (p = 0.001), had multiple gestation (p = 0.02), and state medical insurance (p < 0.001). Infant characteristics including sex and gestational age and infant morbidities including patent ductus arteriosus, necrotizing enterocolitis, intraventricular hemorrhage (Grade 3 or 4) or periventricular leukomalacia, and length of NICU stay were similar between the two study groups. The incidence of respiratory distress syndrome was significantly lower in infants discharged on BM-F (p = 0.02). More infants in the BM-F group received human BM as their initial enteral feeds (p = 0.03), were not exposed to any formula during the first 28 DOL (p < 0.001), and were discharged on higher calories per ounce of feeds (p < 0.001) compared with infants in the BM-S group. Infants in the BM-F group were significantly smaller at birth (p < 0.03) and had lower growth velocity (p = 0.004) and weight at 36 weeks of PMA (p < 0.01) compared with infants in the BM-S group. There were no significant differences in length and head circumference at birth and 36 weeks of PMA between the two study groups. Infants discharged on BM-F were more likely to be discharged from NICU-1 (p < 0.001).

Table 1.

Maternal and Infant Characteristics, Infant Morbidities, Nutrition, and Growth Parameters

	BM-F	BM-S	p
N	147	138
Maternal characteristics
Age (years)	32 (5.4)	31 (5.8)	0.2
Caucasian	72 (49)	95 (69)	0.001
Private insurance	110 (75)	73 (53)	<0.001
Caesarean section	114 (78)	107 (78)	1.0
Multiple gestation	42 (29)	58 (42)	0.02
Infant characteristics
Male	64 (44)	73 (53)	0.1
Gestational age (weeks)	28.8 (2.8)	29.3 (2.6)	0.1
Infant morbidities
Respiratory distress syndrome	89 (61)	101 (73)	0.02
Patent ductus arteriosus	42 (29)	30 (22)	0.2
Necrotizing enterocolitis (≥Stage 2)	1 (1)	3 (2)	0.4
Intraventricular hemorrhage (Grade 3 or 4) or periventricular leukomalacia	4 (3)	5 (4)	0.7
Discharge from NICU 1	135 (92)	26 (19)	<0.001
Length of NICU stay (days)	66.4 (32)	60.1 (29.3)	0.09
Infant nutrition
Initial feeds of BM	146 (99)	130 (95)	0.03
Formula feeds in the first 28 DOL	17 (11.6)	49 (35.5)	<0.001
Maximum calories per ounce at discharge	24.5 (1.6)	23.6 (1.8)	<0.001
Infant growth parameters
Birth
Weight (g)	1145 (334)	1230 (316)	0.03
Length (cm)	37.5 (4.4)	38.2 (3.6)	0.1
Head circumference (cm)	26.3 (2.6)	26.7 (2.2)	0.2
36 weeks of PMA
Growth velocity (g/day)	20.9 (5.2)	23.8 (11.2)	0.004
Weight (g)	2102 (343)	2217 (402)	0.01
Weight <10th percentile	75 (51)	60 (44)	0.2
Length (cm)	44.5 (2.9)	43.9 (2.9)	0.09
Length <10th percentile	64 (44)	65 (50)	0.3
Head circumference (cm)	31.2 (1.5)	31.5 (1.5)	0.1
Head circumference <10th percentile	53 (36)	40 (30)	0.3

Categorical data are shown as n (%), and continuous data are shown as mean (SD).

BM, breast milk; BM-F, expressed BM fortified with formula powder additives; BM-S, expressed unfortified BM supplemented with formula bottle feeds; DOL, day of life; NICU, neonatal intensive care unit; PMA, postmenstrual age; SD, standard deviation.

Table 2 presents the nutrition and growth characteristics of infants in the two study groups at 4 months CA follow-up. The CA at follow-up did not differ significantly between the two groups. Thirty-four percent of infants were receiving any BM feedings at 4 months CA. Compared with infants discharged on BM-S, a significantly higher percentage of infants discharged on BM-F were receiving any BM feedings at 4 months CA (p = 0.02). Infants discharged on BM-F were also receiving significantly higher calories per ounce of feeds at follow-up (p = 0.003). Infants in the BM-F group were significantly smaller in weight (p < 0.001), length (p = 0.045), and head circumference (p = 0.002) compared with infants in the BM-S group. However, there was no significant difference in growth restriction between the two study groups. The rates of weight, length, and head circumference <10th percentile for CA equivalent were similar between the two groups. At 4 months CA, there was a significant difference in weight >50th percentile for CA between the two groups (BM-F: 26, 18%; BM-S: 51, 37%; p < 0.001).

Table 2.

Infant Nutrition and Growth Outcomes at 4 Months Corrected Age Follow-Up

	BM-F	BM-S	p
N	147	138
Corrected age at follow-up (months)	4.3 (0.5)	4.4 (0.6)	0.6
Nutrition
Any BM feeding	60 (41)	37 (27)	0.02
Any formula feeding	126 (86)	128 (93)	0.05
Maximum calories per ounce	22.7 (2.3)	21.9 (1.9)	0.003
Growth parameters
Weight (kg)	6.2 (0.9)	6.7 (1.0)	<0.001
Weight <10th percentile	47 (32)	34 (25)	0.2
Length (cm)	61 (5.4)	62.1 (3.1)	0.045
Length <10th percentile	57 (39)	55 (40)	0.9
Head circumference (cm)	41.5 (1.6)	42.2 (1.8)	0.002
Head circumference <10th percentile	12 (8)	11 (8)	1.0

Categorical data are shown as n (%), and continuous data are shown as mean (SD).

Logistic regression with propensity score covariate adjustment was used to evaluate the associations between discharge BM enhancement type and BM feeding at 4 months CA taking into account possible confounders associated with discharge nutrition type and long-term BM feeding success. Using this model, discharge BM enhancement BM-F was significantly associated with any BM feeding at 4 months CA follow-up (odds ratio: 3.89; 95% confidence interval: 1.66–9.14; p = 0.002). The Hosmer–Lemeshow goodness-of-fit test was not statistically significant, indicating that these data fit the model adequately.

Discussion

In the comparison of VLBW or VP infants discharged from the NICU on BM enhancement with fortification of expressed BM and supplementation of BM with formula feeds, we found that infants who received BM-F have a 3.9-fold greater likelihood to receive any BM feedings at 4 months CA follow-up. We also report here that compared with infants on BM-S, infants discharged on BM-F were not growth restricted at 4 months CA follow-up.

There is significant improvement in BM feeding initiation rates in preterm infants. However, duration of BM feeding among preterm infants remains suboptimal.¹⁷ At discharge from the NICU, an estimated 50% of preterm infants receive any BM feedings, compared with 83% of term infants.^18,19 In our study cohort, 56% of VLBW or VP infants were discharged home on BM feedings. In addition to aggressive lactation support in the NICU, nutritional interventions may represent potential areas for improvement in BM feeding duration.^20,21 Brownell et al. identified optimal periods of exclusive breastfeeding that predicted breastfeeding duration through the first year of life. For our time point of interest at 4 months, the study identified the optimal minimum threshold duration of exclusive breastfeeding to be 11.1 weeks (Positive Predictive Value = 96.1), considerably longer than our average length of NICU stay of ∼8 weeks.²² Despite the need for bottle feeds of enhanced BM over exclusive breastfeeding among our study population of VLBW or VP infants, enhancement of BM by fortification of expressed BM did not appear to be a barrier to BM feeding duration. This is consistent with findings by Zachariassen et al., in VP infants discharged from the NICU on enhanced or unenhanced BM, they found no difference in mean duration of BM feeding.²³ O'Connor et al. found early exposure to artificial formula to be one of only two modifiable barriers to early exclusive breastfeeding at 3 months among term infants.²⁴ In our study cohort, exposure to formula within the first 28 DOL was significantly higher in the BM-S group (BM-S: 36%, BM-F: 12%, p < 0.001).

Current recommendations for preterm infant nutrition aim to support postnatal growth that mirrors the intrauterine growth trajectory of a fetus of the same gestation age.²⁵ However, even with aggressive nutrition practices in the NICU, 50% of VLBW infants exhibit poor growth at discharge from the NICU.²⁶ Although BM is the preferred primary nutrition source for all infants, regardless of gestational age, in many cases, unenhanced BM is inadequate to provide the macro- and micronutrients required for postdischarge optimal growth in preterm population.^12,27–29 Early improvement in growth has been linked to improved neurodevelopmental outcome in VLBW infants; however, preterm infants fed BM also have improved neurodevelopmental outcomes, despite the decreased growth velocity associated with BM feeding.^7,30,31

While the focus of our study was on any BM feedings at 4 months CA, our results show that an improvement in long-term BM feeding rates did not come at the detriment to postdischarge growth. In our study population, infants discharged on BM-F were not more likely to be growth restricted at 4 months CA compared with infants discharged on BM-S. We also showed that infants in the BM-S group were significantly more likely to have weights >50th percentile for CA equivalent and a trend toward weight percentile >85th percentile at 4 months CA (BM-F: 4%, BM-S: 8%). While poor postnatal growth among preterm infants has been associated with poor neurodevelopmental outcomes, rapid growth with higher weight percentiles may also be linked to long-term risks for obesity, higher body mass index, and other metabolic diseases.^32,33

Our study focused on two methods of BM enhancement, fortification of BM with formula powder (BM-F) and supplementation of unfortified BM with infant formula feeds (BM-S); however, there are no widely accepted recommendations for postdischarge nutrition. Other common practices include the use of human milk fortifiers, exclusive feeding with high-calorie formulas, and exclusive breastfeeding.^14,34,35 Few studies have compared growth and neurodevelopmental outcomes of preterm infants fed BM, enhanced BM, or infant formula postdischarge. Zachariassen et al. reported that infants fed formula had better growth parameters compared with those fed enhanced or unenhanced BM.²³ O'Connor et al. showed that infants fed enhanced BM had larger head circumference compared with those fed unenhanced BM.³⁶ Finally, da Cunha et al. observed no association between neurodevelopmental outcomes and BM enhancement, whereas O'Connor et al. found improved visual development among infants fed enhanced BM compared with unfortified BM.^37,38 In our study cohort, preterm infants fed BM enhanced with fortification of BM were lighter and shorter with smaller head circumference at 4 months CA compared with those fed BM enhanced with supplemental infant formula feeds. However, in our study, growth restriction rates at 4 months CA between the two groups were similar.

The findings of our study are subjected to several limitations. The retrospective design of the study limits the data available for analyses. However, data elements were derived from prospectively collected clinical databases in both our NICUs and the outpatient neonatal follow-up program. The care practices at the two NICUs are guided by same NICU policies, procedures, and guidelines. Neonatologists from the same Division of Neonatology staff the two NICUs. Also, at both NICUs, lactation consultants support mothers who want to provide BM for their preterm infants and donor human milk is available after consent when mothers' milk is unavailable. Infants from both NICUs are followed in the same outpatient neonatal follow-up program. Also, there were no significant differences in the rates of neonatal morbidities between the two NICUs, except lower rate of respiratory distress syndrome in infants discharged from NICU-1 (NICU-1: 95, 59%; NICU-2: 95, 77%; p = 0.002). Multivariable regression model with propensity scoring was used in our analysis to control for background characteristics that were closely associated with the two group assignments such as discharging NICUs. After controlling for confounding variables, the BM-F group continued to be significantly associated with BM feeding at 4 months CA in this model. Concerns related to poor bone mineralization have been reported in infants fed unenhanced or fortified BM compared with formula.³⁹ While we found no increased risk of growth restriction in the infants fed BM-F, the retrospective nature of the study prevented us from evaluating bone health at the 4 months CA follow-up. Finally, in this retrospective study, we report maternal and neonatal factors including maternal age, medical insurance type and presence of multiple gestation, infant gestational age, and length of NICU stay. However, information on postdischarge maternal socioeconomic factors such as household and work conditions and perceived worries related to inadequate BM supply that may influence her ability to provide BM was unavailable.⁴⁰ Prospective assessment of discharge nutrition, maternal socioeconomic conditions, and long-term BM feeding rates are important areas that warrant future research.

Conclusion

In conclusion, this retrospective study showed that infants born with birth weight <1500 g or gestational age <32 weeks discharged from level III or IV NICU on BM enhanced with fortification were more likely to receive any BM feeding without growth restriction at 4 months CA follow-up. Currently, there is no consensus on postdischarge nutrition practices in preterm infant population. Postdischarge nutrition may represent a crucial opportunity to optimize not only growth but also long-term BM feeding duration among high-risk preterm infants.

Footnotes

Acknowledgments

The authors thank Linda Mickelson, Nancy Cyr, Jean McNamara, Erica Burgess, and Stephanie Leahy for their help with data abstraction.

Disclosure Statement

No competing financial interests exist.

Funding Information

No funding was received for this article.

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