What Is Known
- Postdischarge feeding recommendations exist to support growth and development in preterm infants.
- Little is known about how very-low-birth-weight infants are fed postdischarge, including duration and exclusivity of breast-feeding, introduction of solids, and iron and vitamin D supplementation.
What Is New
- Adherence to breast-feeding and iron recommendations are suboptimal after hospital discharge for a high proportion of very-low-birth-weight infants.
- Postdischarge feeding practices are primarily associated with maternal education and ethnicity, suggesting groups for targeted intervention and support.
Infant feeding guidelines are important public health strategies to promote optimal growth, development, and reductions in chronic disease. Few data are available to evaluate adherence among the most nutritionally vulnerable infants, including preterm infants born of very-low-birth-weight (VLBW, <1500 g) after hospital discharge (1–5).
Recommendations for preterm infants postdischarge published by the Canadian Paediatric Society include exclusive mother's milk for the first 4 to 6 months corrected age (CA) with nutrient fortification as appropriate; introduction of solids at 4 to 6 months CA; iron supplementation; and vitamin D supplementation for those fed mother's milk (5). Although published in 1995, these guidelines are generally consistent with current Canadian and American guidelines for healthy term-born infants except, the latter recommend exclusive breast-feeding for the first 6 months of life with subsequent introduction of solids (2,6). The latest statement on the nutritional needs of preterm infants postdischarge by the American Academy of Pediatrics recommends exclusive mother's milk until 6 months CA, at least 2 mg · kg−1 · day−1 of iron until 12 months of age and vitamin D supplements for breast-fed infants and those receiving a standard term formula versus postdischarge formula (2). There are no specific recommendations for the introduction of solids for preterm infants.
Although significant effort has been made to improve nutritional intakes of VLBW infants in hospital, comparatively little work has been conducted postdischarge (4). Most VLBW infants are sent home before their expected date of term birth and the majority, particularly infants with comorbidities or predominantly human milk fed, exhibit extrauterine growth restriction, reduced fat-free mass, less bone mass, and poor iron stores at hospital discharge (7–11). Feeding guidelines acknowledge nutrient-enriched feeds are likely required for preterm infants born small and demonstrating extrauterine growth restriction at discharge (2,5,7). A better understanding of actual feeding practices postdischarge will inform the development of strategies that optimize the health of nutritionally vulnerable VLBW infants.
The purpose of the present study was to compare actual feeding practices of VLBW infants at hospital discharge and at 4 and 6 months CA with preterm infant feeding guidelines. Relationships between select parental and infant sociodemographic characteristics and adherence to national feeding guidelines were also examined.
This was a prospective, longitudinal substudy of a double-blinded, randomized clinical trial entitled Greater Toronto Area-Donor Milk for Improved Neurodevelopmental Outcomes (GTA-DoMINO) (12). Human ethics approval was obtained from the Research Ethics Board of each participating hospital. In the GTA-DoMINO trial, 363 infants at 4 tertiary neonatal intensive care units (NICUs) from Southern Ontario were randomized between October 2010 and December 2012 to receive pasteurized human donor milk or preterm formula any time mother's milk was unavailable during hospitalization. In the province of Ontario, infants born <1500 g are typically admitted to level III NICUs. The Ontario system of regionalized care dictates that infants are transferred to level II NICUs for convalescence when acute care is no longer needed. At the time of the present study, donor milk was not routinely available in participating NICUs. The study feeding intervention ended at discharge and infants were fed according to parental choice thereafter. Follow-up neurodevelopmental assessments were completed in July 2015.
VLBW infants expected to begin enteral feeds within 7 days of age were eligible for the GTA-DoMINO trial and were enrolled within 96 hours of birth. Infants with chromosomal anomalies that could contribute to poor neurodevelopment or severe birth asphyxia were ineligible. Infants were also excluded if there was a potential they would be transferred to a nonparticipating NICU. Only infants who survived and were followed to a minimum of 6 months CA were included in the present analyses.
Parents or guardians provided informed consent for their infant to be enrolled in the GTA-DoMINO trial after study staff explained the study. Infant and parental characteristics were collected from the medical chart or parental report at study enrollment. Infant characteristics included sex, birth weight, gestational age at birth, mode of delivery, 5-minute Apgar score, Score for Neonatal Acute Physiology-II (SNAP-II) (13), length of stay in hospital, and discharge weight. Weight-for-age z scores were calculated using the Fenton preterm growth chart and the World Health Organization growth standards after 50 weeks CA (14,15). Maternal characteristics included age, education, living above or below the 2005 to 2006 Statistics Canada poverty line (16), ethnicity, single parenting, previous breast-feeding experience, and multiple birth status. Paternal education was also considered. Using ESPGHAN criteria that nutrient-enriched feeds be given to infants discharged with suboptimal weight-for-age, we assessed the percentage of infants with discharge weights <10th percentile (z score = −1.28) who were discharged receiving nutrient-enriched mother's milk or formula (7).
Trained team members completed a standardized infant feeding questionnaire monthly by telephone after infants were discharged. In the event that families could not be reached, they were approached at their infant's 4 and 8 months CA routine neonatal follow-up visit to obtain feeding information. During calls, families were asked whether they were providing mother's milk, infant formula, or cow's milk and the frequency of provision. If they discontinued mother's milk, they were asked to recollect the last date provided. Details on nutrient fortification of mother's milk, formula brand and concentration, date solids were introduced, and supplemental iron and vitamin D usage were also collected. Fortified mother's milk feeds (eg, nutrient enriched with formula) were considered mother's milk feedings. For the purpose of this study the terminology “breast-fed” was used to describe mother's milk (fresh or frozen) fed at the breast or by feeding tube or bottle. Breast-feeding metrics (eg, duration and exclusivity) in the infant feeding questionnaire were previously validated against 3-day test weighing of preterm infants at 4, 8, and 12 weeks postdischarge (17).
In order to explore the potential impact of adherence to feeding guidelines on outcomes, we performed post-hoc exploratory analyses of the associations between any breast-feeding at 6 months CA and neurodevelopment at 18 months CA. Previous systematic reviews and meta-analyses of the literature report breast-feeding (yes/no or shorter/longer) in primarily term-born infants is associated with increased intelligence (18,19). As reported previously, cognitive, language (receptive, expressive), and motor (fine, gross) development of study participants were assessed by trained testers using the Bayley Scales of Infant and Toddler Development, 3rd Edition (Bayley-III) (12,20). Composite scores were standardized to a mean of 100 and standard deviation (SD) of 15. Testers demonstrated >80% agreement on videotaped sessions before assessing study infants.
Demographic data and postdischarge feeding practices were reported using descriptive statistics. Relationships between parental and infant demographics and infant feeding recommendations were initially assessed using chi-square statistics. Maternal demographics considered in the analyses were age (≤28, 29–32, 33–36, 37–56 years), education (≤high school, college/vocational diploma, undergraduate degree, postgraduate degree), socioeconomic status (above or below poverty line), single parent status (yes/no), ethnicity (European, Middle Eastern/South Asian, Asian, Other/Mixed/African/Hispanic), previous breast-feeding (yes/no), and multiple birth status (yes/no). Paternal education was also considered in the analyses. Infant demographics considered by quartiles in the analyses were gestational age at birth (≤26, 26.01–27.71, 27.72–29.64, 29.65–35.29 weeks), SNAP-II score (≤5, 6–9, 10–19, 20–42), and length of hospital stay (≤55, 56–77.5, 77.6–107, 108–248 days). Infants were considered adherent to feeding recommendations if they demonstrated the desirable feeding practice within 2 weeks of the target timeframe. Following univariate analysis, multiple logistic regression analysis was performed using a stepwise backwards elimination strategy until only those with a P value of <0.05 remained. As gestational age at birth and length of hospital stay were found to be colinear using a variance inflation factor >2.5, length of hospital stay was removed from these analyses. We did not include exclusive breast-feeding at 4 or 6 months CA in our multiple regression analyses due to the low number of participants affirmative for this feeding practice. Post-hoc exploratory analysis using analysis of covariance was conducted to explore associations between any breast-feeding at 6 months CA and neurodevelopment as assessed by cognitive, motor, or language composite scores on the Bayley-III (20). In statistical models, site refers to the recruitment centre only and due to the small numbers recruited at McMaster Children's Hospital, results from this center were pooled with Mount Sinai Hospital as measures of acuity were similar (eg, SNAP-II scores). Data were analyzed using SAS Version 9.4 for Windows (SAS Institute, Cary, NC).
Families of 840 eligible infants were approached for the GTA-DoMINO trial and 363 were randomized (Fig. 1). Of those randomized, 300 were included in the current analyses. Fifty-five percent of infants were boys and 57% were delivered via cesarean section. Mean (SD) infant birth weight was 1016 (267) g; 73% of infants were born <1250 g and 13% were small for gestational age (see Supplemental Digital Content 1, http://links.lww.com/MPG/B411). The majority of families had incomes above the poverty line and approximately half of mothers had an undergraduate or postgraduate degree (Table 1). At enrollment, 31% of women reported previously breast-feeding.
Human Milk Use and Nutrient-enriched Feeding at Discharge
During initial hospitalization, 98% of infants received some mother's milk. The day before discharge, 72% of infants received at least some mother's milk and 49% of infants were fed mother's milk exclusively. At discharge, 139 (46%) infants were <10th percentile for weight of which 66 (47%) of this subset of infants received a nutrient-enriched feeding immediately postdischarge (see Supplemental Digital Content 2, http://links.lww.com/MPG/B412).
Postdischarge Feeding Practices
At 4 and 6 months CA, 39% and 29% of infants continued to receive mother's milk, respectively (Table 2). Low rates (≤20%) of exclusive mother's milk feeding at 4 and 6 months CA were evident. The majority of infants receiving mother's milk received supplemental vitamin D, whereas approximately half of the infants, irrespective of mother's milk feeding, received an iron supplement at 6 months CA. Introduction of solids occurred between 4 and 6 months CA for almost 3 quarters of infants. Overall, 12% of participants adhered to the combination of all examined feeding recommendations: exclusive mother's milk for 4 to 6 months CA, introduction of solids at 4 to 6 months CA, iron supplementation, and vitamin D supplementation for mother's milkfed infants.
We also considered feeding practices based on infants’ postnatal age (PNA) and found higher proportions fed mother's milk at 4 and 6 months PNA versus CA. Vitamin D and iron supplementation rates were also higher at 6 months PNA compared to CA.
Parental and Infant Characteristics and Feeding Practices
Univariate associations between parental and infant characteristics and feeding practices are reported in Supplemental Digital Content 3 (http://links.lww.com/MPG/B413). Multiple logistic regression analyses revealed that mother's milk was more likely to be provided at discharge if infants were delivered at a greater gestational age and if fathers had a university education (Table 3). Mother's milk was more likely to be provided as the exclusive form of nutrition at discharge if mothers had a postgraduate degree and fathers had an undergraduate degree. Exclusive breast-feeding at discharge differed by ethnicity with mothers of Middle Eastern/South Asian or Asian descent having the lowest odds compared to mothers of European origin.
Similar to mother's milk feeding at hospital discharge, women with a university education were more likely to provide mother's milk at 4 and 6 months CA. University-educated women were also more likely to provide an iron supplement at 6 months CA. In addition, women of Middle Eastern/South Asian descent continued to have lower odds of providing mother's milk at 4 and 6 months CA compared to women of European descent. Infants born at a higher gestational age were more likely to be introduced to solids in the recommended timeframe. Multiple regression analysis of infant and parental sociodemographics and infant feeding practices at 4 and 6 months PNA are reported in Supplemental Digital Content 4 (http://links.lww.com/MPG/B414).
Associations Between Any Breast-feeding at 6 Months Corrected Age and Neurodevelopment
A statistically significant difference in mean language composite scores at 18 months CA was found between infants receiving and not receiving any mother's milk at 6 months CA (unadjusted scores, 93.1 in any mother's milk group vs 85.6 in no mother's milk group) (Supplemental Digital Content 5, http://links.lww.com/MPG/B415). For the cognitive and motor composite scores, the interaction of recruitment site and any mother's milk at 6 months CA was found to be statistically significant (P = 0.0148 and P = 0.0248, respectively). Pair-wise comparisons (t tests) of cognitive and motor composite scores at each site revealed that mean differences were only statistically significant at site 3 in the direction anticipated.
There are limited data in the literature on actual feeding practices of VLBW infants after hospital discharge; among Canadian VLBW infants they are virtually nonexistent. Given the health benefits of breast-feeding and the nutritional vulnerability of VLBW infants, it is important to understand how they are fed after discharge to develop effective strategies to support optimal health and development. Our results suggest that more work is needed to align actual feeding practices with recommendations and that breast-feeding practices have the greatest gap between recommendations and adherence.
Mothers in the present study exhibited high breast-feeding initiation (98%). By discharge only 49% of infants were, however, exclusively mother's milk fed. Exclusive breast-feeding rates at discharge for preterm infants vary in the literature from 23% to 77% (21–23). Data on exclusive breast-feeding rates for VLBW infants to 6 months is sparse, but exclusive breast-feeding for term infants at 6 months has been reported as 24% in Canada (2012) and 22% in the United States (2013) (24,25). These values are comparable to exclusive breast-feeding rates of VLBW infants in the present study at 6 months PNA (23%), but higher than that at 6 months CA (6%). A Swedish study showed 4%, 6%, and 17% of infants born <28 weeks, 28 to 31 weeks, and 32 to 36 weeks, respectively, were exclusively breast-fed at 6 months CA (26).
Our data from a diverse sample of VLBW infants indicate significant disparities exist in providing any mother's milk to 6 months CA. For example, our results show mothers with undergraduate or postgraduate degrees had 3.2 and 7.1 times higher odds, respectively, of providing any mother's milk at 6 months CA versus mothers with high school education or less. These findings are consistent with Canadian term-born infant data; however, the magnitude of effect appears to be larger in VLBW infants (27–29). Our results also suggest that paternal education is associated with the provision of any and exclusive mother's milk at discharge; therefore, it is important for clinicians to take this into account and to counsel both caregivers on infant feeding. Although our findings indicate that mothers of Middle Eastern or South Asian descent were less likely to provide mother's milk at 6 months CA, the Canadian Community Health Survey demonstrated no differences in exclusive breast-feeding to 6 months by ethnicity, although only 4 categories were used: Asian, Black, White, and Other (30). Reports from the United States highlight ethnic disparities in breast-feeding and socioeconomic factors related to the provision of mother's milk at discharge among VLBW infants (31,32).
It is important for clinicians to be aware that high-risk families may need extra infant feeding support. The relationship between sociodemographics and the feeding practices of VLBW infants has not been previously described within the Canadian context. Our findings underscore the importance of acknowledging the social determinants of health in providing anticipatory guidance around breast-feeding in clinical practice. For term infants, a recent Cochrane review suggests that support from trained healthcare professionals or peer supporters reduces the risk of cessation of breast-feeding before 6 months (33). Similarly, a systematic review of breast-feeding promotion for NICU infants identified peer support in hospital and in the community as an effective intervention for increasing provision of human milk (34). Interventions to increase breast-feeding duration for preterm infants should likely start in hospital (including skin-to-skin care, setting maternal human milk feeding goals, and adapting the World Health Organization Baby-Friendly Hospital Initiative to the NICU), focus on both caregivers and emphasize continued support postdischarge by lactation consultants and peer supporters (35–37).
Preterm infants are at increased risk for vitamin D deficiency and bone mineral disease and like term-born breast-fed infants, vitamin D supplementation is recommended (2,6,38). Most study infants receiving mother's milk at 6 months CA were supplemented with vitamin D (83%). This is higher than national Canadian data which show 58% of infants fed any mother's milk and 74% of exclusively breast-fed infants receive vitamin D supplementation (39). Of note, vitamin D deficiency rickets persists in Canada especially among children in the north and those with darker skin not supplemented with vitamin D (40).
Because of the interruption of iron transfer from mother to fetus in the third trimester, preterm birth is a risk for iron deficiency in childhood; hence, it is recommended that preterm infants receive iron supplementation until 12 months CA (41). Only 58% of infants in our cohort received an iron supplement at 6 months CA. Although national biochemical data are unavailable, Saunders et al (42) reported 2% and 10% of healthy children 12 to 72 months (n = 2614) from primary care practices in Toronto had iron deficiency anemia and iron deficiency without anemia, respectively. In the latter study, prolonged breast-feeding and total cow's milk intake were associated with iron deficiency. Given the association between iron deficiency and neurodevelopment, interventions to increase postdischarge breast-feeding must also address the low adherence of iron supplementation among VLBW infants (41).
Complementary foods given too early displace mother's milk in the diet and given too late may be associated with nutritional deficiencies (6,43). In our cohort, approximately 71% of infants were introduced to complementary foods in the recommended timeframe between 4 and 6 months CA. Although comparable data for preterm infants are unavailable in Canada, a national survey of term-born infants in 2003 indicated that 85% of infants were fed solids at 4 months (44). The timing for introducing solids may be affected by infant characteristics. In the present study, infants born 29 to 35 weeks gestational age were more likely to be introduced to solids in the recommended timeframe versus those born <29 weeks. Anecdotally clinicians report that despite recommendations, this may be because families consider their child's postnatal versus CA when introducing solids. Other studies report early introduction of solids was associated with maternal smoking, lower socioeconomic status, education, and newcomers to Canada born and raised in the Middle East (45–48). We found that mothers with an undergraduate degree had higher odds of introducing solids between 4 and 6 months CA compared to those with high school education or less.
VLBW infants are at risk for negative neurodevelopmental outcomes, which can be mitigated through nutritional strategies (49). A dose-response relationship has been shown between human milk received in the NICU and increased cognitive development at 20 months CA and, as previously noted, systematic reviews and meta-analyses report breast-feeding in primarily term-born infants is associated with increased intelligence (18,19,50). Results from our exploratory analysis in the present study of the composite neurodevelopment scores at 18 months CA and any breast-feeding at 6 months CA are consistent with this literature.
Strengths and Limitations
Strengths of the present study include the sample size of VLBW infants, diversity (ethnic, socioeconomic status), prospective data collection, and low participant attrition (95% of survivors to 6 months CA). There are certain limitations within the present study. Diagnoses of oral motor discoordination, gastroesophageal reflux, oral aversions, or recurrent aspiration postdischarge were not obtained and may have affected adherence to feeding recommendations. In addition, feeding data were collected by parental report; to minimize recall bias caregivers were telephoned monthly.
Adherence to postdischarge preterm infant feeding recommendations which include duration and exclusivity of breast-feeding, introduction of solids, and iron and vitamin D supplementation were low in our cohort of VLBW infants. Maternal education was most frequently associated with adherence to recommendations and maternal ethnicity also played an important role. Given evidence associating recommended feeding practices after discharge and optimal health, research efforts examining promising intervention strategies to support nutritional recommendations for VLBW infants, including breast-feeding at home, are urgently required.
The authors thank participating families and volunteers who assisted with data collection.
The GTA-DoMINO Feeding Group also included Simone Vaz, Mahmud Almadani, Shirley Sit, David Gryn, Munesh Singh, Karen Chang, Peter Azzopardi, Douglas Campbell, Shaheen Doctor, Anwar Asady, Ann Bayliss, Jelena Popovic, Charmaine van Schaik, Christoph Fusch, Sue Ekserci, Deborah Arts-Rodas, Sandra Gabriele, Carol Williams, Joan Brennan-Donnan, Michael Jory, and Aneta Plaga.
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