Acta Pdiatrica ISSN 08035253

REGULAR ARTICLE

Successful breastfeeding after discharge of preterm and sick newborn infants

S kerstrom (susanne.akerstrom@karolinska.se)1 , I Asplund1 , M Norman1,2
1.Department of Neonatology, Karolinska University Hospital, Stockholm, Sweden 2.Department of Clinical Science, Intervention and Technology, Karolinska Institute, Stockholm, Sweden

Keywords Breastfeeding, Neonatal unit, Newborn infant, Preterm Correspondence Susanne kerstrom, RN, Neonatal Unit, Danderyd Hospital, S-182 88 Stockholm, Sweden. Tel: +0046-8-6556608 | Fax: +0046-8-7533713 | Email: susanne.akerstrom@karolinska.se Reveived 5 May 2007; revised 25 June 2007; accepted 1 August 2007. DOI:10.1111/j.1651-2227.2007.00502.x

Abstract Aim: To determine the extent and duration of breastfeeding in preterm and sick newborn infants admitted to a level IIb neonatal unit (NU). Method: Hospital-based follow-up of 1730 infants born in 1996, 2001 and 2004, and studied from discharge to 6 months of post-natal age. Results: At discharge from the NU, 98% of term (n = 945) and 92% of preterm (n = 785) infants were exclusively or partly breastfed. Exclusive breastfeeding increased at 2 months of corrected post-natal age and 78% of term infants were still exclusively or partly breastfed at 6 months of corrected post-natal age. Duration of breastfeeding among preterm infants was signicantly shorter than in infants born at term. However, even among extremely preterm infants with a gestational age <28 weeks, 41% were still breastfeeding, exclusively or in part, at 6 months of post-natal age. There was no difference in breastfeeding after neonatal care in1996 as compared to 2004. Moreover, the study showed that the breastfeeding after neonatal care differed only slightly from population data for all infants in Sweden. Conclusion: Breastfeeding can be successfully established in most preterm and previously sick neonates.

INTRODUCTION Breastfeeding protects babies from infections (1), reduces the risk of atopic eczema (2) and promotes normal growth during the first year of life (3). In preterm infants, human milk seems to protect against necrotizing entercolitis (4). Infants who have been breastfed, especially those born small and preterm, exhibit a better cognitive function in childhood as compared to those fed formula in infancy (5). Breastfeeding has also been associated with a lower risk of obesity (6), high blood pressure (7) and glucose intolerance (8). As adverse growth and development early in life are thought to contribute to hypertension, diabetes and cardiovascular disease (910) in adults, the establishment of successful breastfeeding in preterm and sick infants is an effective way to promote both their immediate and future health. Preterm or sick newborn infants in need of active management usually must be separated from their mothers after birth. Initiation of breastfeeding is therefore delayed which involves extra emotional strain for the mother (11). After very preterm delivery (infants born before 32 gestational weeks), mothers may have to express milk for weeks or even months before their infants can breastfeed. These mothers more often become depressed (12) and despite relatively high percentage initiating breast milk production, it is not uncommon that breastfeeding fails (13). The information about breastfeeding patterns in previously sick and preterm infants is so far limited to fairly small cohorts (1417), to observations ending at hospital discharge (14,18,19) or to short-term follow-ups (17). In addition, effects of changes in obstetric and neonatal management, as well as in social factors, have to our knowledge not been longitudinally observed.

The aim of this study was to measure breastfeeding frequencies in large cohorts of preterm and sick newborn infants admitted to neonatal care, and to compare these findings with population data for all infants born in Sweden. Apart from feeding regimes at discharge from hospital, we investigated the proportions of infants still breastfed at 2, 4 and 6 months of corrected post-natal age. To elucidate any long-term changes in patterns of breastfeeding, we collected hospital and population data in 1996, 2001 and 2004. METHODS This study was performed at Danderyd Hospital, one of the four neonatal units (NU) in Stockholm County. Breastfeeding rates were studied in preterm and term, but initially sick, infants born in 1996, 2001 and 2004 and admitted to NU. Newborn infants with malformations (n = 20) that completely precluded breastfeeding or mothers with medical contraindications (e.g. maternal HIV infection or psychosis, n = 10) were excluded. Moreover, infants who after birth were permanently transferred to neonatal or paediatric units in other hospitals9.0% of all admissionsbecause the families did not reside in the catchments area or because of overcrowding in our unit were not included in the study. The gestational age or morbidity distribution among those infants did not differ from that of the remaining 91% who were discharged to their home. After these exclusions 1730 infants were included in the study, divided amongst the 3 years: 1996 (n = 534), 2001 (n = 564) and 2004 (n = 632). In the studied cohorts, 945 infants had been born at term (after 37 weeks of gestation) and 785 were born preterm (<37 weeks of gestation). Among preterm infants, 189 had

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been born before 32 weeks (very preterm) and 47 were born before 28 weeks of gestation (extremely preterm: n = 21 at 27 weeks, n = 14 at 26 and n = 12 at 25 weeks or less). In 1996, data on breastfeeding was only grouped according to pretermterm, and not stratified into the three different categories (preterm, very and extremely) of preterm birth. Antenatal steroid treatment to pregnant women with threatening preterm delivery was clinical routine during the complete study period. The NU at Danderyd hospital is a level IIB-IIIA nursery according to definitions proposed by American Academy of Pediatrics (20). The unit provided care for newborn infants with gestational age 27 weeks. Treatment with mechanical ventilation for brief periods (less than 24 h) and continuous positive airway pressure could be provided. Deliveries before 27 completed weeks of gestation were, if possible, referred before birth to the neonatal intensive care unit at Karolinska Hospital as well as infants in need of mechanical ventilation for longer periods. Once these extremely preterm infants, and other mechanically ventilated infants, had been stabilized and weaned off the ventilator, they were transferred back to the NU at Danderyd Hospital. Patients in need of surgery because of malformations were transferred to other regional or national centres. To characterize the 3 year cohorts and changes over time, the following variables were recorded: maternal age, parity, smoking in pregnancy, mode of delivery, rate of preterm birth, number of infants with Apgar score <7 at 5 min, perinatal mortality, neonatal admissions, number of days with infants on continuous positive airway pressure (CPAP) and length of stay (LOS) in the NU, Table 1. Evaluation of breastfeeding Breastfeeding data at discharge were recorded by two of the authors. At 6 months of corrected post-natal age, that is

6 months after 40 weeks of post-conceptional age, a previously unannounced questionnaire was sent home to all families (1730). No reminders were sent. A total of 1379 families responded: 84% (n = 449) in 1996, 81% (n = 456) in 2001 and 75% (n = 474) in 2004. The distributions of gestational age and breastfeeding at discharge from hospital among nonresponders did not differ from those of responding families. The mothers answered three written questions relating to whether their infants were exclusively, partly or not breastfed at 2, 4 and 6 months of corrected post-natal age. The questionnaire was in Swedish and not translated into other languages. Definitions were provided with the questionnaires. Exclusive breastfeeding was defined as infants who received all feedings from the mothers breast. Infants who were breastfeeding and received expressed breast milk by bottle, or infants who received breast milk together with formula and other foods, were defined as partly breastfed. Infants fed formula alone or together with other foods were considered as not breastfed. Population data on breastfeeding were retrieved from the Swedish Medical Birth Registry using public descriptive statistics and software accessible (in Swedish) on the internet (http://www.socialstyrelsen.se). Ethics Data collection about the prevalence of breastfeeding at hospital discharge is part of the national quality assurance. Parts of the data presented herein (from 1996 and 2001) have previously been reported in Swedish (21). The study protocol and questionnaire were approved by the local ethics committee at Karolinska Institute and all parents gave their informed consent to participate. Statistical analysis Data are presented as proportions or relative frequencies (per cent) of breastfeeding (outcome) in relation to gestational (term or preterm) and post-natal ages. Confidence intervals (CI 95%) for all frequencies were calculated. For comparisons between groups, the chi-square test was used. A p-value <0.05 was considered as statistically significant. All calculations were done using the JMP version 5.1 (SAS Institute, Inc., Cary, NC, USA). RESULTS Breastfeeding at hospital discharge (Table 2) At discharge from the NU, 95% of all 1730 infants were breastfed, 60% exclusively and 35% in part. More term infants (65%) than preterm infants (53%) were exclusively breastfed (p < 0.05). Relative frequencies of partly breastfed infants were similar in the two groups (32% and 40%, respectively). Stratifying data according to gestational age, the difference at discharge was ascribed to a significantly lower rate of exclusive breastfeeding in the most immature infants, those born very preterm before 32 weeks of gestation (p < 0.05). In contrast, no differences in breastfeeding were found between infants born slightly preterm (gestational age 3236 weeks) and those born at term.

Table 1 Perinatal characteristics for mothers and infants in three cohorts from the same hospital in 1996, 2001 and 2004 Study year Delivery unit Maternal age (mean years) 1-para (%) Smoking in pregnancy (%) Deliveries (n) C-sections (%) VE or forceps (%) Preterm delivery (%) AS <7 at 5 min (%) Perinatal mortality () Neonatal unit Admissions (n) CPAP (days/year) Mean LOS (days) 1996 31.2 (28.9) m.d. (41) m.d. (16) 4771 14 (12) 6.7 (6.7) 5.2 (5.7) m.d. (1.2) 3.7 (5.2) 576 694 12.7 2001 32.4 (29.8) 46 (44) 5 (11) 6324 18 (16) 9.3 (7.8) 5.3 (5.7) 1.0 (1.2) 3.5 (5.6) 639 1052 11.0 2004 32.6 (30.2) 48 (45) 3 (9) 8129 20 (17) 8.0 (8.1) 5.3 (5.9) 1.0 (1.1) 3.6 (4.8) 819 1849 10.0

Figures in parentheses indicate population average (data from Swedish Medical Birth Registry). p < 0.05. VE = vacuum extraction; AS = Apgar score; CPAP = continuous positive airway pressure; m.d. = some missing data from Danderyd Hospital in 1996; LOS = length of stay.

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Table 2 Breastfeeding at discharge from the neonatal unit and at 2, 4 and 6 months of corrected post-natal age Gestational age Questionnaire responders Breastfed at discharge (%) Exclusively Partly Not breastfed < 28 weeks, n = 29 n = 27 38 (2056) 38 (2056) 24 (840)

2831 weeks, n = 103 n = 82 34 (2543) 50 (4060) 16 (923)

3236 weeks, n = 404 n = 301 56 (5161) 40 (3545) 4 (26) 66 (6171) , 24 (1929) 10 (713) 51 (4557) 28 (2333) 21 (1626)

37 weeks, n = 660 n = 517 63 (5967) 35 (3139) 2 (13) 83 (8086) 11 (814) 6 (48) 70 (6674) 19 (1622) 11 (814) 24 (2028) 54 (5058) 22 (1826)

Breastfed at 2 months of corrected age (%) Exclusively 44 (2563) Partly 19 (434) Not breastfed 37 (1955) Breastfed at 4 months (%) Exclusively Partly Not breastfed Breastfed at 6 months (%) Exclusively Partly Not breastfed 26 (943) 30 (1347) 44 (2363) 4 (011) , 37 (1955) 59 (4078)

44 (3355) 28 (1838) 28 (1838)

34 (2444) 21 (1230) 45 (3456) 6 (111) , 41 (3052) 52 (4163)

17 (1321) 48 (4254) 35 (3040)

Individual data from 2001 and 2004 pooled and presented as proportions (95% condence intervals for proportions within parenthesis). p < 0.05, versus infants born at term. p < 0.05, versus exclusive breastfeeding at discharge.

Follow-up at 2, 4 and 6 months of post-natal age (Table 2) Exclusive breastfeeding increased from discharge to 2 months of corrected post-natal age, among term and slightly preterm infants (p < 0.05 in both groups). Although the numbers then gradually declined, a high percentage (78%) of term infants admitted to neonatal care at birth was still breastfed, exclusively or in part, at 6 months of age. Although significantly fewer preterm infants were exclusively breastfed for longer periods than those born at term (p < 0.05 for all gestational age strata at 2 and 4 months of corrected post-natal age), 41% of the extremely preterm infants (<28 weeks of gestational age at birth) were still breastfed exclusively or partly at 6 months of corrected post-natal age. Breastfeeding patterns 1996, 2001 and 2004 In infants discharged from the NU, especially in those born at term, rates of exclusive breastfeeding decreased from 70% in 1996 to 54% in 2001 (p < 0.05). However, in 2004, breastfeeding was again as common as in 1996. Comparison with population data for all Swedish newborn infants Exclusive breastfeeding in preterm and term newborn infants admitted to our NU differed slightly from pooled population data for all Swedish newborn infants born in the same period of time (1996: n = 95 627, 2001: n = 91 815 and 2004: n = 101 261) and there were no differences in the number of infants who did not breastfeed at all. At 2 months of post-natal age, 79% of infants were exclusively breastfed (13% in part) in the population as compared to an average of 72% exclusive breastfeeding (18% in part) in infants discharged from the neonatal care unit

(p < 0.05). At 4 months of post-natal age, the corresponding figures were 67% and 61% for exclusive breastfeeding in the population as compared to infants born sick and/or preterm (p < 0.05), and 16% and 21% for breastfeeding in part. At 6 months of post-natal age, exclusive breastfeeding was reported to be 32% on a population level and 26% in our NU cohorts (p < 0.05) (40% and 46% for breastfeeding in part, respectively). DISCUSSION The most important finding in this observational study was that most of the preterm and initially sick newborn infants started and continued to breastfeed much to the same extent as healthy newborns. Although some of them were not exclusively breastfed at discharge from the NU, several mothers and infants succeeded in fulfilling this interaction at home. The present findings are important knowledge for doctors and nurses involved in neonatal care and underline that all mothers should be encouraged to express milk for their preterm and sick newborn infants as soon as possible after delivery and beyond. While this study showed that the successful breastfeeding might occur after neonatal care, it does not explain why. Nursing routines and active support to mothers who want to breastfeed their infants has been found to be important. Skin-to-skin care immediately after birth, breast contact for the infant as soon as possible and early expression of milk promote successful breastfeeding after preterm birth (22 24). Individualized care and regarding parents as central members of the nursing team is also very important (25). Accordingly, these interventions are practised in our hospital. Moreover, in randomized controlled trials, rates of exclusive

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breastfeeding at discharge were lower in preterm infants who had received bottle as compared to cup supplements during the transition from nasogastric tube to oral feeding (26,27). Cup feeding has therefore been used as method of choice in our NU. Promotion of breastfeeding, both public and within the primary health care system, and a social security system facilitating parental presence in the NU and during the infants first year are also likely to contribute to our findings. Breastfeeding of newborn infants has not always been prevalent in Sweden. Thirty-five years ago, only 31% at 2 months after birth and 13% of all 4-month-old infants were exclusively breastfed and the attitude towards breastfeeding was negative and knowledge about breastfeeding was poor. Women were recommended to breastfeed in a strictly timeregulated fashion (every fourth hour), much in the same way as bottlefeeding was practised. Focus was on the mother and her production of sufficient amounts of breast milk and little attention was given to the fact that once healthy, infants can regulate breastfeeding in relation to their needs. Today, antenatal motivation, as reflected by Swedish national statistics, is in general high. The lower rates of breastfeeding among very preterm infants may not only reflect their neonatal morbidity. As we recorded feeding routines at the corrected and not at the actual post-natal age, the mothers of the most premature infants had been expressing breast milk for a long time before discharge. Therefore, those who still breastfed their infants at 6 months of corrected post-natal age had in fact produced milk for an average of 9 months. WHO defines exclusive breastfeeding as breast milk as the infants only nourishment, regardless of how they are fed: from a cup, bottle or the breast (28). This definition is wider than ours in which infants were classified as exclusively breastfed only if they were feeding from the breast. If anything, our definition may have contributed to underestimation of breast milk intake and to lower rates of exclusive breastfeeding. There was no infant in our study that solely fed expressed breast milk by bottle after discharge. We found lower rates in exclusive breastfeeding in 2001 as compared to both 1996 and 2004. The observed changes underline the importance of re-evaluations and to maintain an optimal result, we suggest that the breastfeeding rates after neonatal care should be monitored on a regular basis. Present findings confirm those of others from Sweden and Canada (16,29,30). In view of the high response rate to our questionnaire (mean 80%) and the large number of unselected infants who participated in this study, we believe that our findings are representative and can be generalized to Swedish conditions. Variations in socio-economic factors as reflected by low maternal smoking, older mothers and more primiparae in our hospital population as compared to national average may limit these interpretations. In conclusion, breastfeeding can be successfully established in most preterm and previously sick neonates. Because breastfeeding is promoting short- and long-term health, this information is important and can reassure parents of preterm or sick newborn infants as well as the nursing staff.

ACKNOWLEDGEMENT This study was supported by the research foundations of Karolinska Institutet.

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