Factors Associated with Breast Milk Feeding of Very Preterm Infants from Birth to 6 Months Corrected Age

Abstract

Objectives:

To investigate factors that may affect breast milk feeding (BMF) practices among very preterm infants.

Materials and Methods:

This retrospective study included infants born before 32 weeks gestational age (GA) and monitored up to 6 months corrected age (CA). Feeding method was assessed at day 14 of life, 36 weeks GA, 6 weeks after home discharge, and 6 months CA. Multivariable logistic regression analysis was used to examine which factors were associated with BMF initiation at cessation.

Results:

Of 181 infants who qualified for the study, 146 (81%) initiated BMF. Of these, 80% were mainly BMF (≥75% of daily nutrition volume). At 36 weeks GA, 6 weeks postdischarge, and 6 months CA, 130 (71.8%), 87 (48%), and 36 (19.9%) infants, respectively, continued to receive some BMF. Multivariate analysis revealed that initiation of BMF was more common with younger GA and higher level of maternal education. Infants whose mothers failed to supply ≥75% of daily nutrition as BMF at day 14 were more likely to be exclusively formula fed 6 weeks after discharge. Cessation of BMF at 6 months CA was associated with birth at >28 weeks.

Conclusions:

Successful BMF can be commenced and maintained throughout hospitalization in the majority of very preterm infants. Despite a significant dropout rate occurring within several weeks after discharge, in this select cohort, infants with lower GA were more likely to be breastfed after discharge.

Introduction

The beneficial effect of breast milk feeding (BMF) for infants has been thoroughly studied and is considered a health decision that has an impact on the early and long-term outcomes of infants and mothers. Among preterm infants, the benefits of BMF over formula diet include prevention and reduction of the severity of necrotizing enterocolitis (NEC), retinopathy of prematurity (ROP), and late-onset sepsis.^1,2 BMF is also associated with better neurodevelopmental outcomes.³ The American Academy of Pediatrics (AAP) recommends BMF for all infants for the first year of life regardless of gestational age (GA).⁴ The AAP also noted that the protective effect of BMF is a combined function of its duration and exclusivity.⁵ Providing breast milk to preterm infants may be challenging for many reasons, among them are the infants' medical conditions, the need for prolonged mechanical expression of milk due to infants' inability to breast-feed orally, and maternal stress. Data from previous studies showed that although initiation of BMF among mothers of preterm infants can be encouraged, a high percentage of mothers will stop BMF by the time of discharge (39–80%) and this trend continues even more dramatically after home discharge.^6–10 Various factors were found to be associated with initiation and duration of BMF among mothers of preterm infants, including maternal age, race, marital status, and education, as well as multiple birth, infant GA, and birth weight (BW), length of hospitalization, intended length of lactation, and amount of milk supply at 6 weeks.^7–14 Data are still lacking regarding duration and causes of ceasing maternal breast milk supplementation for very preterm infants.

This study aims to describe the incidence of breastfeeding at our hospital among very preterm infants and to identify risk factors for its cessation at different time points from birth to 6 months corrected age (CA).

Materials and Methods

Included in the study was a cohort of very preterm infants (<32 weeks GA) born between January 2012 and August 2014 at the Sheba Medical Center and monitored at the Preterm Follow-up Clinic. Excluded from the study were patients who died before discharge from the neonatal intensive care unit (NICU), those with major congenital malformations or known genetic disorders, those who were part of triplet pregnancies (as they reflect a different population with respect to maternal challenges in starting and continuing BMF), and infants born to mothers who could not breast-feed due to medical conditions: surrogate pregnancy, medications which are not compatible with lactation, or severe maternal clinical condition following pregnancy complications. Data were collected retrospectively from infants' computerized charts during initial hospitalization and from maternal reports at the visits to the follow-up clinic.

The computerized system of our neonatal department (MetaVision) served as a platform for organizing the data, which included maternal age, parity and gravida, fertility treatment, maternal diseases, and medical treatment during pregnancy. Other maternal data were recorded from the follow-up clinic and included previous children in the family, marital status, education (years), and income (according to the mean income/family in Israel).

Infant data included GA and BW, appropriate/small/large for GA (AGA, SGA, and LGA), gender, delivery mode multiple, and Apgar scores at 1 and 5 minutes. Analysis of neonatal morbidity included rates of respiratory distress syndrome, bronchopulmonary dysplasia defined as oxygen dependency at 36 weeks GA and typical chest X-ray, proven NEC¹⁵ (i.e., stage ≥2 according to Bell's criteria), high grade (III–IV) intraventricular hemorrhage,¹⁶ cystic periventricular leukomalacia, ROP requiring treatment,¹⁷ sepsis (positive blood cultures), need for assisted mechanical ventilation (MV), duration of oxygen supplementation, and length of hospital stay.

Our department protocol prioritizes individual BMF. Donor breast milk is not yet available in Israel. Mothers are strongly encouraged and guided by the medical team and lactation consultants to pump their own milk for their babies soon after birth. An individualized developmental care program carried out in the NICU includes early skin-to-skin care as well as parental education for active care of infants from admission until discharge. This program is directed by a developmental team comprising three physiotherapists and an occupational therapist, as well as a physician and three dedicated nurses who are in NIDCAP (neonatal individualized care and assessment program) training. Moreover, lactation consultants and a speech therapist guide support the parents of very preterm infants on a daily basis from admission until discharge. Feeding at the breast is commenced when the infant reaches 33 weeks. Infants are discharged home at 36 weeks GA if the following criteria are met: weight >1.9 kg, temperature stability, free of apneic episodes, and mature oral feeding with adequate growth. All very preterm infants are invited to the follow-up clinic within 6 weeks after discharge and at 6 months CA for physical and developmental assessment.

Data regarding infant feeding during the first month of life were recorded: BMF, formula, or combined feeding. Data regarding infants' feeding after home discharge were collected from the follow-up clinic records. For the purpose of the study, we determined the following definitions for neonatal feeding: Exclusive formula fed (EFF)—infants whose mothers did not express breast milk at all and were exclusively formula fed. Any BMF—infants whose nutrition included some breast milk either by lactation or by bottle. Mainly BMF—if ≥75% of the enteral nutrition per day consisted of maternal breast milk. For the sake of clarity, in this study, the authors refer to any BMF as BMF, while specifically indicating mainly BMF. The feeding habits as described above as well as risk factors for weaning from BMF were assessed at four different time points:

• Day of life (DOL) 14, assuming that all mothers planning BMF would be able to supplement it by this time.

• Thirty-six weeks GA, discharge time for healthy and stable preterm infants.

• Six weeks post discharge, which is the time of the first appointment at the follow-up clinic.

• Six months CA, time of the second appointment at the follow-up clinic.

This study was approved by the Sheba Medical Center (SMC) Institutional Review Board.

Statistical analysis

Differences between BMF infants and EFF infants at the different time points were assessed using the chi-square test for categorical variables and independent sample t-test or Mann–Whitney test for continuous variables. At time point 1, a comparison was made between those who initiated BMF and those who were EFF. To identify risk factors for terminating BMF, at time points 3 and 4, we compared those who continued BMF with those who dropped out. Variables with p values of less than 0.1 were used as predictors in the logistic regression models. Continuous variables were dichotomized at their respective median (oxygen days, intravenous line days). Three separate logistic regression models (14 days, 6 weeks postdischarge, and 6 months CA) were run using the forward likelihood ratio technique. Bonferroni correction was used for multiple comparisons. The SPSS software was used for the statistical analysis.

Results

Of 288 potential very preterm infants born during the study period, 107 (37.1%) were excluded for the following reasons: 32 (11.1%) died before discharge, 9 (3%) had genetic abnormalities or major congenital malformations, 39 (13.5%) were lost to follow-up, 21 (7.3%) infants were part of triplet pregnancies, 3 (1%) were born to mothers for whom BMF was not recommended due to medication taken, 2 (0.7%) were born through surrogate pregnancies, and 1 mother (0.3%) had a severe medical condition. The final cohort consisted of 181 infants born to 139 mothers. Table 1 shows characteristics of the study infants versus those who were lost to follow-up. There were no significant differences between the groups. The study group comprised 81 (44.8%) singletons and 100 (55.2%) twins. The rates of infants fed by any breast milk were 146 (80.6%), 130 (71.8%), 87 (48%), and 36 (19.9%) over the four study time points, respectively. At DOL 14, 117 (80%) of the 146 BMF infants were mainly BMF. The characteristics of those who received any BMF versus those who were exclusively formula fed at DOL 14 are shown in Table 2. Infants born to single mothers, those with less than 14 years of education, as well as those with older GA and increased BW, female gender, and appropriate for their GA were less likely to be BMF at DOL 14. A logistic regression analysis applied to the abovementioned parameters demonstrated that infants whose BW was <1 kg were 6.8 times (95% CI 1.55–30.12) more likely to be BMF at DOL 14. Likewise, higher maternal education (>14 years) was associated with a 2.6 times (95% CI 1.190–5.676) greater likelihood to be BMF at the above time point. The other variables did not reach significance in the logistic regression model. At 36 weeks GA (second time point), 130 infants continued to be BMF, a drop of 8.2% from baseline. The small number of dropouts did not allow statistical analysis; therefore, we related further comparisons with DOL 14. Table 3 compares the characteristics of those who continued to be BMF after home discharge (at 6 weeks and 6 months CA) with those whose mothers ceased BMF at each of these time points. At 6 weeks postdischarge, BMF was terminated in 59 (40.4%) of the 146 infants who were BMF at DOL 14; older maternal age and surgical delivery were associated with cessation of BMF at this time point. A logistic regression analysis conducted for the relevant characteristics showed that the only factor to predict BMF cessation at 6 weeks postdischarge was failure to mainly BMF at DOL 14 with OR of 3.28 (95% CI 1.304–8.272). BMF was terminated for 51 infants between 6 weeks after discharge and 6 months CA. Older GA, BW, shorter duration of MV, and infusion, as well as shorter duration of hospitalization, were associated with cessation of BMF. A logistic regression analysis for the confounders that were statistically significant demonstrated that older GA (>28) was the only predictor of ceasing BMF (OR 5.48, 95% CI 1.58–18.94) at this time point.

Table 1.

Comparison Between the Study Group and Those Lost to Follow-Up

	Study group, N = 181, N (%)	Lost to follow-up, N = 39, N (%)	p^a
GA, mean ± SD	29.9 ± 1.8	30.1 ± 1.7	0.471
Birth weight, mean ± SD	1270.3 ± 314.2	1291.5 ± 330.5	0.715
SGA	15 (8.3)	6 (15.43)	0.110
Male	94 (51.9)	23 (58.3)	0.302
Maternal age, mean ± SD	31.96 ± 5.8	30.47 ± 6.5	0.174
IVF	54 (29.8)	10 (25.0)	0.724
Singleton	81 (44.8)	15 (38.4)	0.323
Married	166 (91.7)	36 (92.3)	0.993
Income level^a
Low	73 (40.7)	4 (16)
Middle	42 (23.4)	6 (24.0)	0.172
High	54 (30.1)	15 (0.6)
Education >14 years	101 (56.7%)	21 (53.8)	0.534
First child	110 (60.7)	19 (48.7)	0.155
CS delivery	118 (65.2)	30 (76.9)	0.099
MV	80 (44.2)	20 (51.3)	0.223
i.v. >7 days	106 (58.5)	25 (64.1)	0.419
O₂ >2 days	121 (66.8)	27 (69.2)	0.575
Early complications^b	42 (23.3)	9 (23.0)	0.539
Brain injury^c	13 (7.2)	5 (12.8)	0.157
Neonatal complications^d	57 (31.5)	9 (23.0)	0.182
BMF at day of life 14	146 (80.7)	31 (79.5)	0.573
BMF at 36 weeks	131 (72.4)	23 (58.9)	0.072

Data available for 25 infants in the lost to follow-up group.

Early complications: hypotension requiring treatment or 5-minute Apgar <6, pneumothorax.

Brain injury (central nervous system) complication: intraventricular hemorrhage grade III or IV or periventricular leukomalacia.

Neonatal complications: necrotizing enterocolitis stage >2 or ROP requiring treatment or sepsis or oxygen requirement at 36 weeks GA.

BMF, breast milk feeding; CS, cesarean section; GA, gestational age; i.v., intravenous infusion; IVF, in vitro fertilization; MV, mechanical ventilation; ROP, retinopathy of prematurity; SD, standard deviation; SGA, small for GA.

Table 2.

Maternal and Infant Characteristics According to Infant Nutrition (Breast Milk Versus Exclusive Formula) at Day of Life 14

	BMF, N = 146, N (%)	Formula, N = 35, N (%)	p^a
GA, mean ± SD	29.7 ± 1.89	30.3 ± 1.4	0.035
Birth weight, mean ± SD	1254 ± 331	1335 ± 223	0.090
Birth weight <1000 g	41 (28.1)	2 (5.7)	0.003
SGA	15 (10.3)	0	0.034
Male	81 (55.5)	13 (37.1)	0.039
Maternal age, mean ± SD	31.5 ± 5.5	33.5 ± 6.8	0.073
IVF	41 (28.1)	13 (37.1)	0.197
Singleton	69 (47.3)	12 (34.3)	0.115
Married	137 (93.8)	29 (82.9)	0.045
Income level
Low	62 (43.1)	11 (31.4)	0.452
Middle	40 (27.8)	12 (34.3)
High	42 (29.2)	12 (34.3)
Education >14 years	106 (73.1)	18 (51.4)	0.013
First child	90 (61.6)	20 (57.1)	0.380
CS delivery	96 (65.8)	22 (62.9)	0.445
MV (yes)	64 (43.8)	16 (45.7)	0.494
i.v. >7 days	87 (60.4)	19 (54.3)	0.317
O₂ >2 days	100 (78.7)	21 (80.8)	0.527

BMF, breast milk feeding; CS, cesarean section; GA, gestational age; i.v., intravenous infusion; IVF, in vitro fertilization; SD, standard deviation; SGA, small for GA; MV, mechanical ventilation.

Table 3.

Maternal and Infant Characteristics According to Infant Nutrition (Breast Milk Versus Exclusive Formula) at 6 Weeks Postdischarge and 6 Months CA

	BMF 6 weeks, N = 87	Dropped 6 weeks, N = 59	p	BMF 6 months, N = 36	Dropped 6 months, N = 49	p
GA	29.6 ± 1.8	29.8 ± 1.9	0.458	29.0 ± 1.9	30.0 ± 1.66	0.011
Birth weight	1274 ± 310	1225 ± 360	0.385	1205 ± 352	1319 ± 271	0.113
Weight <1000 g	22 (25.3)	19 (32.2)	0.234	14 (38.9)	8 (16.3)	0.018
SGA	5 (5.7)	10 (16.9)	0.29	3 (8.3)	2 (4.1)	0.355
Male	51 (58.6)	30 (50.8)	0.224	23 (63.9)	28 (57.1)	0.344
Maternal age	30.7 ± 5.1	32.7 ± 5.9	0.039	29.7 ± 4.8	31.9 ± 4.9	0.053
IVF	20 (23.0)	21 (35.6)	0.071	5 (13.9)	15 (30.6)	0.060
Singletons	44 (50.6)	25 (42.4)	0.210	20 (55.6)	22 (44.9)	0.226
Married	83 (95.4)	54 (91.5)	0.269	36 (100)	45 (91.8)	0.105
Income
Low	37 (43.5)	25 (42.4)		18 (52.9)	17 (34.7)
Middle	24 (28.2)	16 (27.1)	0.957	10 (29.4)	14 (28.6)	0.128
High	24 (28.2)	18 (30.5)		6 (17.6)	18 (36.7)
Education >14 years	67 (77.9)	39 (66.1)	0.084	29 (82.9)	37 (75.5)	0.297
First child	49 (56.3)	41 (69.5)	0.075	18 (50)	29 (59.2)	0.267
CS	52 (59.8)	44 (74.6)	0.046	20 (55.6)	30 (61.2)	0.381
MV	39 (44.8)	25 (42.4)	0.451	22 (61.1)	17 (34.7)	0.014
i.v. >7 days	56 (65.9)	31 (52.5)	0.076	29 (80.6)	25 (53.2)	0.008
Exclusive BMF at day of life 14	78 (89.7)	38 (64.4)	<0.001	33 (91.7)	43 (87.8)	0.418
Brain injury	9 (10.3)	4 (6.8)	0.333	3 (8.3)	5 (10.2)	0.540
Neonatal complications	31 (35.6)	17 (28.8)	0.249	14 (38.9)	17 (34.7)	0.432
Age at discharge (weeks)	37.2 ± 1.4	37.5 ± 1.8	0.267	37.5 ± 1.5	37.0 ± 1.4	0.197
Weight at discharge	2278 ± 305	2255 ± 439	0.718	2283 ± 331	2275 ± 291	0.910
Length of stay	53.3 ± 17.5	53.8 ± 21.4	0.887	59.5 ± 19	49.3 ± 15.3	0.008

Brain injury: intraventricular hemorrhage grade 3 or 4, periventricular leukomalacia or cerebellar hemorrhage, Neonatal complications: necrotizing enterocolitis or late-onset sepsis, or oxygen, requirement at 36 weeks GA or retinopathy of prematurity.

BMF, breast milk feeding; CA, corrected age; CS, cesarean section; GA, gestational age; i.v., intravenous infusion; IVF, in vitro fertilization; LOS, length of stay; MV, mechanical ventilation; SGA, small for GA.

Discussion

This observational study demonstrates that the vast majority of very preterm infants born at SMC were successfully BMF during their initial hospitalization. Moreover, once BMF has been commenced, almost 90% continued to be breastfed until discharge. A significant dropout occurred within several weeks after discharge, and this trend continued during the following several months so that by 6 months CA, only 20% of the initial cohort was BMF. We also demonstrated that risk factors for cessation of BMF vary at different time points, suggesting that different interventions may be needed to prolong BMF among very preterm infants.

In the present study, 146 infants (80.6%) initiated BMF on DOL 14 and, of these, 117 (80.0%) were mainly BMF. Moreover, almost 90% of those who were BMF at this time point continued to be BMF until close to discharge. These rates of BMF initiation are high compared with those published in the United States (54–70.3%), Canada (58%), and Switzerland (75%).^5,10,14,18 The above studies, however, were conducted more than a decade ago, during a period characterized by a different understanding and different attitude regarding the importance of breast milk. More recently, BMF rates that are similar to those presented in the current study have been reported in Brazil (84%) and Sweden (74%).^18,19 Comparison with the present study cohort is limited due to enrollment on the basis of BW rather than on the basis of GA, which may be associated with inclusion of more mature infants in whom different factors may affect transitioning to BMF.

Initiation and continuation of BMF among preterm infants during NICU hospitalization are challenging. Maternal medical conditions may delay milk pumping and affect lactogenesis.^20,21 Moreover, the need for pumping for a long period is time-consuming, while the mother wants to spend time with her premature infant and often has other home and family duties.²² In spite of these obstacles, admission to the NICU has been shown to have a positive influence on breastfeeding continuation, especially among mothers of very preterm infants.⁶ Moreover, an increase in BMF rates among preterm infants in the NICUs has been reported over time.^9,23 Scientific evidence for the beneficial medical effect of BMF, especially for preterm infants, along with implementation of intervention programs that promote BMF in the NICU, such as those recommended by the Baby Friendly Hospital Initiative and by individualized developmental care, has been suggested to contribute to this change.^{8,9,20,24–31} The high rates of initiation and continuation of BMF in the present cohort may be attributed to the relatively high weight and advanced prematurity of the study population providing good feedback to moms. In addition, these rates support the evidence that BMF throughout hospitalization in the NICU is feasible when mothers are given close guidance and support throughout their infants' hospitalization. The results also suggest that once BMF is initiated, there is a high probability for it to continue until time of discharge.

Factors that were shown to be associated with BMF initiation can be divided into four main causes: first, demographic parameters that reflect basic maternal condition, among them are age, education, income, marital status, ethnicity, other children in the family, and the like; second, infants' characteristics and medical status, such as infants' GA and BW, gender, multiple infant birth, medical condition, and length of hospitalization;^11,23,32 third, maternal perception of milk production and successful transfer of milk to the infant^9,22; and fourth, the mentality advocated by the NICU and interventions that promote, educate, and support mothers regarding BMF. Individualized developmental care in which parents are empowered and encouraged to care for their infants, as well as to practice skin-to-skin care, has been shown to improve BMF.^6,18,29–33 The current study found that infants of unmarried mothers with fewer years of education were less likely to engage in BMF. A potential explanation for this observation is either that more educated mothers can more easily access information regarding the beneficial effects of BMF or that once this information is provided to them by the NICU team, they are more likely to become active and start pumping. Other maternal parameters, including age, fertility treatments, first delivery, and delivery mode, were not found to correlate with BMF. Since our population is relatively homogeneous, we were unable to evaluate the impact of ethnicity. With respect to infant factors, our study results showed that mothers of infants born at lower GA and BW, as well as SGA, were more likely to pump breast milk. Although infants' medical condition regarding respiratory support and length of intravenous fluid administration was similar for the BMF and EFF groups, it may be that mothers of more premature infants were more aware of the importance of BMF and more motivated to devote increased efforts to breast milk pumping and/or may have received more counseling and assistance for breast milk production because of their higher risk status. The third factor was not assessed in the current study, while the fourth could not be assessed as individualized developmental care is provided homogeneously throughout the NICU.

Previous studies that were not restricted to very preterm infants indicated a mean duration of BMF ranging from 1.8 to 6 months from birth.^{7,14,21,34–36} In the present study, half of those who were BMF during their NICU stay ceased within 6 weeks after discharge and 80% ceased by 6 months CA. This significant dropout rate is surprising in light of the high rates of successful BMF throughout hospitalization. Previous studies suggest that negative predictors for BMF after discharge include cigarette smoking, low socioeconomic status, short planned duration of BMF, as well as poor technique, and provision of complementary feeding.^32,35,37 Concerns related to milk production and its transfer to the infant are the primary reasons for discontinuation of BMF, while early successful exclusive BMF at 6 weeks postpartum was found to be associated with successful BMF at 12 weeks postpartum.^{14,22,34,36,38} In the present cohort, failure to mainly BMF at DOL 14 was associated with its cessation within 6 weeks postdischarge. Taken together, these data suggest that failure to exclusively BMF at an early stage (day 14 of life) may be seen as a red flag for early BMF discontinuation. Severity of prematurity, neonatal morbidities (need for MV and IV lines), and longer hospitalization were more common among those who continued to be BMF at 6 months CA. This finding is not intuitive and is not in line with the literature. It is likely that local factors influence this finding. We hypothesize that mothers of younger and sicker infants may have received more psychological and educational support during the period their infants were hospitalized. That is, they met more frequently with the social worker, the developmental team, and the lactation consultants.

Since our study population is relative homogeneous and low risk in terms of sociodemographic characteristics, that is, middle-high income (58.5%), married, and >14 education years, the most probable known risk factors for BMF discontinuation are predelivery planning to BMF as well as concerns related to milk production and its transfer to the infant. Further prospective studies are planned to examine whether selective early intervention for those who present with the above difficulties during the third week after delivery may help prolong BMF after discharge. Our findings also point to the need for supportive programs after NICU discharge, as suggested by the SPIN (supporting premature infant nutrition) program.²² In the current study, socioeconomic factors were not identified as risk factors for BMF cessation after discharge. This may be related to the global medical insurance and 3 months of maternity leave provided in this country.

The study population contains an unusually high number of twins (55.3%). This high incidence of twins is normal at our institution at it serves as a referral center for high-risk twin pregnancies and is also an in vitro fertilization center. With regard to twin pregnancies, the statistical analysis was infant based (not mother based) and did not demonstrate differences between twins versus singletons, as shown in Tables 2 and 3.

The major limitations of the study are related to its retrospective nature and to the lack of maternal interviews, which could shed more light on individual decisions regarding discontinuation of BMF.

In conclusion, this study, which was conducted on a large cohort of very preterm infants, suggests that successful BMF rates during NICU stay are possible.

We speculate that the high rates of initiation and continuation of BMF among high BW and advanced GA (or more mature) infants in the current study population may be due to their ability to suck and tolerate feeding effectively, therefore providing good feedback to moms.

Footnotes

Disclosure Statement

No competing financial interests exist.

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