care, health and development Child: Original Article

doi:10.1111/j.1365-2214.2009.01018.x

Breastfeeding promotion for infants in neonatal units: a systematic review

cch_1018 165..178

M. J. Renfrew,* L. Dyson,* F. McCormick,* K. Misso, E. Stenhouse, S. E. King* and A. F. Williams

*Mother and Infant Research Unit, Department of Health Sciences, University of York, York Centre for Reviews and Dissemination, University of York, York Faculty of Health and Social Work, University of Plymouth, Plymouth, and St Georges Hospital Medical School, University of London, London, UK Accepted for publication 28 June 2009

Abstract
Background Breastfeeding/breastmilk feeding of infants in neonatal units is vital to the preservation of short- and long-term health, but rates are very low in many neonatal units internationally. The aim of this review was to evaluate the effectiveness of clinical, public health and health promotion interventions that may promote or inhibit breastfeeding/breastmilk feeding for infants admitted to neonatal units. Methods Systematic review with narrative synthesis. Studies were identied from structured searches of 19 electronic databases from inception to February 2008; hand searching of bibliographies; Advisory Group members helped identify additional sources. Inclusion criteria: controlled studies of interventions intended to increase breastfeeding/feeding with breastmilk that reported breastmilk feeding outcomes and included infants admitted to neonatal units, their mothers, families and caregivers. Data were extracted and appraised for quality using standard processes. Study selection, data extraction and quality assessment were independently checked. Study heterogeneity prevented meta-analysis. Results Forty-eight studies were identied, mainly measuring short-term outcomes of single interventions in stable infants. We report here a sub-set of 21 studies addressing interventions tested in at least one good-quality or more than one moderate-quality study. Effective interventions identied included kangaroo skin-to-skin contact, simultaneous milk expression, peer support in hospital and community, multidisciplinary staff training, and Unicef Baby Friendly accreditation of the associated maternity hospital. Conclusions Breastfeeding/breastmilk feeding is promoted by close, continuing skin-to-skin contact between mother and infant, effective breastmilk expression, peer support in hospital and community, and staff training. Evidence gaps include health outcomes and costs of intervening with less clinically stable infants, and maternal health and well-being. Effects of public health and policy interventions and the organization of neonatal services remain unclear. Infant feeding in neonatal units should be included in public health surveillance and policy development; relevant denitions are proposed.

Keywords breastfeeding, breastfeeding denitions, clinical interventions, neonatal units, public health intervention, systematic review Correspondence: Mary J Renfrew, RM, PhD, Mother and Infant Research Unit, Department of Health Sciences, University of York, Heslington, York YO10 5DD, UK E-mail: mjr505@york.ac.uk

This article Breastfeeding promotion for infants in neonatal units: a systematic review was written by M. J. Renfrew, L. Dyson, F. McCormick, K. Misso of University of York, E. Stenhouse of University of Plymouth, S. E. King of University of York and A. F. Williams of University of London. It is published with the permission of the Controller of HMSO and the Queens Printer for Scotland.

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M. J. Renfrew et al.

Introduction
Promotion, protection and support of breastfeeding and of feeding with breastmilk in neonatal units are vital to the preservation of short- and long-term health. Studies in high-risk environments (Narayanan et al. 1982; El-Mohandes et al. 1997; Schanler 2001; Furman et al. 2003) have identied greater risk of incidence of invasive infection in low-birthweight infants fed with formula. A meta-analysis of randomized controlled trials (RCTs; Boyd et al. 2007) has shown that formula-fed lowbirthweight infants have ve times the risk of necrotizing enterocolitis, a condition associated with a mortality of approximately 20% and signicant long-term healthcare costs among survivors (Bisquera et al. 2002). Formula feeding delays the transition from parenteral to enteral nutrition (Lucas et al. 1994), increasing the associated cost and infection risk. Reduced neuro-developmental attainment has been shown among lowbirthweight infants fed on formula (Anderson et al. 1999; Smith et al. 2003; Vohr et al. 2006, 2007; Kramer et al. 2008), an important nding in a group where cognitive impairment is a frequent adverse outcome (Costeloe & EPICure Study Group 2006). Feeding from the breast may facilitate other benecial outcomes, for example a reduction in procedural pain (Gray et al. 2000; Carbajal et al. 2003; Shah et al. 2006). Many factors make breastfeeding difcult in this setting. The fragility of preterm and sick infants, their changing nutritional and health needs, separation of mother and baby, difculty in producing breastmilk (Cregan et al. 2000; Hartmann & Ramsay 2006; Henderson et al. 2008), and anxiety, distress and fear provoked in mothers and family members are all problematic. Moreover, healthcare staff in hospital and community may not have time or skills needed to support breastfeeding (Redshaw & Hamilton 2006). It has been argued that supporting mothers in breastfeeding and providing breastmilk is an essential aspect of humane care, and promotes attachment (Chalmers et al. 2003). Such care includes gentle touch, decreased negative stimulation, exposure to the mothers scent, skin-to-skin care and family involvement in care (Liu et al. 2007), all of which are inherent in breastfeeding. The mothers unique involvement in the feeding and care of her infant may also alleviate her shock, fear and grief following the birth, and reduce the estrangement from her baby associated with care in a neonatal unit (Phillips & Tooley 2005; Redshaw & Hamilton 2006; Flacking et al. 2007; BLISS 2008). Improvement in survival has increased the numbers of infants in neonatal units with complex needs (Costeloe & EPICure Study Group 2006). Lack of breastfeeding and breastmilk feeding is thus an important, costly and growing problem that needs to be addressed successfully. Over-representation of

families from lower socio-economic groups in neonatal units (Macfarlane & Mugford 2000; Furman et al. 2002), suggests that implementing effective measures to promote breastfeeding would also help to address inequalities in health.

Aim of the review

The primary aim of this review was to evaluate the effectiveness of clinical, public health and health promotion interventions that may promote or inhibit breastfeeding or feeding with breastmilk for infants admitted to neonatal units. A concurrent cost-effectiveness analysis was conducted and is reported in a related paper (S. Rice et al., unpublished). Five reviews in related elds have been published (Collins et al. 2003; Conde-Agudelo et al. 2003; Edmond & Bahl 2006; McInnes & Chambers 2006; Flint et al. 2007). This review differs from these in that it addresses the wide range of potential interventions (cf. Collins et al. 2003; Conde-Agudelo et al. 2003; Flint et al. 2007) and has been conducted using rigorous systematic review methods (cf. Edmond & Bahl 2006; McInnes & Chambers 2006).

Methods
A systematic review of the literature was undertaken using guidelines published by the Centre for Reviews and Dissemination (Centre for Reviews and Dissemination 2001). Structured searches were conducted on 19 electronic databases from inception to February 2008. There was no limitation by language or country of origin. Details of databases searched and search strategies will be available in the full report of the study at http://www.ncchta.org/project/htapubs.asp (to be published August 2009). Eligible studies had to full the following criteria: Participants: infants, or mothers of infants, who were admitted to neonatal units; and those linked to such infants and women, including fathers/partners, other family members or health professionals. This included studies that examined such infants and families following discharge. Interventions: any type of intervention that addressed breastfeeding or feeding with breastmilk in neonatal units or following discharge. Outcomes: Primary outcomes: measures of breastfeeding and breastmilk feeding. In studies where these were reported, secondary outcomes examined included clinical/health, process, psychosocial and cost-effectiveness outcomes. Study designs: RCTs, randomized crossover studies, concurrent comparisons before/after studies.

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Data were extracted and appraised for quality using standard structured tables relevant for each study design (see full report http://www.ncchta.org/project/htapubs.asp). Data extraction and quality assessment were independently checked by a second reviewer. Disagreements in data extraction or quality appraisal were resolved by discussion or by a third reviewer. The following denitions of study quality were used based on National Institute for Health and Clinical Excellence guidance development methodology (2004) (National Institute for Health and Clinical Excellence 2005) and the Cochrane Handbook (2008) (The Cochrane Collaboration 2008): Good quality: most or all criteria fullled and where they were not met, the study conclusions were thought very unlikely to alter Moderate quality: some criteria fullled and where they were not met, the study conclusions were thought unlikely to alter Poor quality: few criteria fullled and the conclusions of the study were thought very likely to alter. Serious caution is warranted in interpretation of the results of these studies Results from primary studies were assessed and summarized in a qualitative synthesis for each type of intervention and across types of intervention. Relative risks for outcomes were estimated on an intention-to-treat (ITT) basis where possible; the ITT analysis was adjusted where appropriate for legitimate post-randomization exclusions.

Results
Overview of studies
A total of 48 studies met the selection criteria, of which 65% (31/48) were RCTs, and 19 of which had not been included in any previous reviews in the eld. Studies were conducted from 1984 to 2007 in 17 countries; 11 resource-poor and six industrialized countries. Nine topic categories were identied. These are summarized in Table 1, which also shows the numbers and quality ratings of studies in each category. Studies were heterogeneous in terms of design, intervention, participants and outcomes measured. Virtually all examined infants who were described as clinically stable although they ranged from term low-birthweight infants to very-lowbirthweight and premature infants on respiratory support. Several included twins and multiple births, but only one (Blaymore Bier et al. 1997) reported analyses separately for these.

Psychosocial data were very limited and virtually no cost outcomes were reported in any of the studies. Study heterogeneity precluded meta-analysis. Descriptions of standard care used in these studies were limited, but it was evident that the norm involved a high degree of separation between mothers and infants with very limited opportunity for intimate contact, that staff were generally unfamiliar with and untrained in the management of breastfeeding, and that bottles and teats were the normal method of oral feeding until direct feeding from the breast was possible. In this paper we report only on primary outcomes of those interventions with at least one good-quality study, or more than one moderate-quality study, for which we could extract or calculate outcome data as relative risks (RR) where appropriate, and 95% condence intervals (CI). Use of these quality criteria excluded 13 studies rated poor quality (Bell et al. 1995; Paul et al. 1996; Hurst et al. 1997, 2004; Hill et al. 1999; Kliethermes et al. 1999; Ortenstrand et al. 1999, 2001; Roberts et al. 2000; Oddy & Glenn 2003; Gilks & Watkinson 2004; Senn 2004; Wilhelm 2005; Amali-Adekwu et al. 2007), 11 that were each the only study of moderate quality to evaluate an intervention (Feher et al. 1989; Wahlberg et al. 1992; Mersmann 1993; Gunn et al. 1996, 2000; Charpak et al. 1997, 2001; Meier et al. 2000; da Silva et al. 2001; Hansen et al. 2005; Slusher et al. 2007) and two where outcome data were lacking (Grifn et al. 2000; Merewood et al. 2006). We also do not report in detail one good-quality study (Fewtrell et al. 2006) that examined the effect of oxytocin spray on early milk output in mothers expressing milk for preterm infants because it is not licensed in the UK. In total, 27/48 (56%) of the studies included in the main report are not reported in this paper. The interventions thereby excluded from this paper were motherinfant contact other than kangaroo skin-to-skin contact (Wahlberg et al. 1992; Charpak et al. 1997, 2001; Hurst et al. 1997; Roberts et al. 2000; Wilhelm 2005), naso-gastric tube vs. bottle feeding (Kliethermes et al. 1999), nipple shields for women with breastfeeding problems (Meier et al. 2000), hand expression (Paul et al. 1996), pedal-operated breast pump (Slusher et al. 2007), relaxation tape (Feher et al. 1989), breast massage (one element of Jones et al. 2001), therapeutic touch (Mersmann 1993), pharmaceutical galactagogues [four different interventions with one study each (Gunn et al. 1996; da Silva et al. 2001; Hansen et al. 2005; Fewtrell et al. 2006)], hindmilk feeding (Amali-Adekwu et al. 2007), teaching mothers to measure the fat content of their milk (Grifn et al. 2000), in-home measurement of infant weight (Hurst et al. 2004), early hospital discharge with home support (Ortenstrand et al. 1999, 2001; Gunn et al. 2000), and organization of care other than Unicef Baby Friendly accreditation of the associated maternity

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Table 1. Categories, sub-topics, numbers and quality of studies showing both those included in the full review and those reported in this paper RCTs* (quality rated good, moderate, poor) 9 (0, 8, 1) 3 (0, 1, 2) 12 (0, 9, 3) 7 RCTs (0, 7) Other controlled studies (quality rated good, moderate, poor) Total studies in the full review (quality rated good, moderate, poor) Total studies reported in this paper (quality rated good, moderate)

Categories of study topics identied

Sub-topics identied in full review (sub-topics reported in this paper)

M. J. Renfrew et al.

Enhanced motherinfant contact 5 (1, 2, 2) 1 (0, 1, 0) 6 (1, 3, 2) 3 RCTs (1, 2)

Interim feeding methods and related interventions 6 (1, 3, 2) 0 6 (1, 3, 2) 3 RCTs (1, 2)

Methods of expressing breastmilk

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Methods of enhancing breastmilk production

7 (1, 6, 0)

7 (1, 6, 0)

Supporting optimal nutritional intake from breastmilk

2 (0, 0, 2)

1 (1, 0, 0)

3 (1, 0, 2)

Breastfeeding support and education for mothers 0 2 (0, 1, 1) 0 2 (0, 2, 0)

3 (2, 1, 0)

3 (0, 2, 1)

6 (2, 3, 1)

2 RCTs (2, 0) 2 beforeafter studies (0, 2) 2 (0, 2, 0) 2 (0, 1, 1) 2 beforeafter studies (0, 2) 0

Staff education and training

Early hospital discharge with home support 0

Organization of care

Kangaroo care, kangaroo skin-to-skin contact, skin-to-skin care Cup vs. bottle, pacier vs. no pacier, naso-gastric tube vs. bottle, nipple shields Simultaneous vs. sequential pumping, novel manual pump vs. standard electric pump, electric pump vs. pedal operated pump vs. hand expression Relaxation tape, breast massage, therapeutic touch, syntocinon nasal spray, human growth hormone, Metoclopromide, Domperidone Hindmilk feeding, teaching mothers to measure fat content of their milk, in-home measurements of infant weight Peer support, hospital lactation consultant support Training/education of health professionals Home visits and support including home gavage feeding Unicef Baby Friendly Initiative accreditation of associated maternity hospital, other standard(s) 4 (1, 1, 2) 4 (1, 1, 2) 34* (5, 21, 8) 14 (2, 7, 5) 48 (7, 28, 13)

2 beforeafter studies (1, 1)

Totals

15 RCTs (4, 11) 6 beforeafter studies (1, 5) Total 21 (5, 16)

RCT, randomized controlled trail. *Including three randomized crossover studies, which were all excluded from this paper. Five RCTs and one randomized crossover study. Five RCTs and two randomized crossover studies.

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Citations identified after de-duplication from search process (n=10184)

(ve of these from the UK). Six of the original nine study topic categories are reported below.
Citations referred to third reviewer (n=119)

Enhanced motherinfant contact

This section examined enhanced contact between mother and infant, over and above standard care. Seven studies, all RCTs of moderate quality, were included. All seven RCTs (Whitelaw et al. 1988; Sloan et al. 1994; Blaymore Bier et al. 1997; Cattaneo et al. 1998; Rojas et al. 2003; Kadam et al. 2005; Boo & Jamli 2007) evaluated kangaroo skin-to-skin contact, where the infant is held between the mothers breasts. The timing and duration of contact varied across the studies and between participants. All studies were conducted among infants dened as clinically stable, including some receiving minimal respiratory support. Four studies (Whitelaw et al. 1988; Blaymore Bier et al. 1997; Rojas et al. 2003; Boo & Jamli 2007) identied increased duration of any breastfeeding prior to, at, or up to 1 month after hospital discharge. Three of these (Whitelaw et al. 1988; Blaymore Bier et al. 1997; Boo & Jamli 2007) evaluated short duration of daily kangaroo skin-to-skin contact (ranging from 10 min up to 2 h) among infants of very low birthweight in industrialized settings, including the UK. All of these reported a statistically signicant increase in the duration of any breastfeeding at chosen time points including: prior to hospital discharge (kangaroo contact: 21/64, control: 6/62; RR 3.39, 95% CI 1.477.83) (Boo & Jamli 2007); at hospital discharge (kangaroo contact: 19/64, control: 9/62; RR 2.05, 95% CI 1.004.17) (Boo & Jamli 2007), kangaroo contact: 19/21, control: 11/20; RR 1.65, 95% CI 1.082.50) (Blaymore Bier et al. 1997); and up to 1 month after hospital discharge (kangaroo contact: 17/31, control: 9/32; RR 1.95, 95% CI 1.033.70) (Whitelaw et al. 1988), kangaroo contact: 10/21, control: 2/20; RR 4.76, 95% CI 1.1919.10) (Blaymore Bier et al. 1997). The ndings in one study (Boo & Jamli 2007) may have been inuenced in favour of the intervention by between-group differences in the infants postmenstrual age and maternal education at baseline. A fourth study (Rojas et al. 2003) evaluated daily kangaroo skin-to-skin contact of medium duration (8 h in two four-hourly sessions) among infants of very low birthweight in the USA. A positive, but not statistically signicant effect on the duration of any breastfeeding prior to hospital discharge was found (kangaroo contact: 18/31, control: 9/26; RR 1.68, 95% CI 0.913.08). One small study conducted in India among infants of less than 1800 g found that kangaroo skin-to-skin contact for short periods daily did not lead to earlier feeding at the breast [kangaroo contact: (n = 44) 4.7 days (SD 3.3), control: (n = 45) 5.6 days (SD 3.9); mean difference 0.90, 95% CI -0.60 to 2.40]

Potentially relevant papers ordered for more detailed evaluation (n=154)

Papers not obtained (n=16) (did not arrive, n=7) (not available in UK, n=5) (ongoing study, n=2) (no response from author, n=2)

Potentially relevant papers obtained for more detailed evaluation (n=138)

Papers excluded from further evaluation (n=87)

Relevant studies included in the full effectiveness review (n=48)*

Studies excluded from this paper (n=27) due to: Poor quality (n=13) Insufficient evidence of adequate quality per topic (n=11) additional reasons as stated (n=3)

Studies included in this paper (n=21) comprising: RCTs (n=15) Industrialized countries (n=12)

Figure 1. Summary of review ow. The following owchart is based on the QUORUM statement ow diagram [The Lancet (1999) http://www. consort-statement.org/index.aspx?o=1345, downloaded on 23 October 2008] to summarize the review ow for the identication of relevant studies. RCT, randomized controlled trial. *Reported in 51 papers.

hospital (Bell et al. 1995; Oddy & Glenn 2003). Full details of all 48 studies appear in the full report of the review (available by August 2009 at http://www.ncchta.org/project/htapubs.asp). The review process to identify included studies is summarized in Fig. 1 (QUORUM owchart) and details of individual, included studies are reported in Table 2. With the exception of one study (Jones et al. 2001), all results have been recalculated by review authors using an ITT analysis, adjusted for legitimate post-randomization exclusions (e.g. because of death). Twenty-one studies of good (5, 24%) or moderate (16, 76%) quality conducted between 1984 and 2007 are therefore reported here. Six of these have not been reported in previous reviews. Fifteen (71%) were RCTs and six used beforeafter designs. Twelve (57%) were conducted in industrialized settings

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Table 2. Details of included studies as per inclusion criteria for this paper
Included studies Boo & Jamli (2007) Malaysia Moderate 126 (128) Moderate 57 (60) Compliance low in both groups Moderate 71 (71) Variable compliance Infants <1500 g No oxygen equipment Infants <1500 g Minimal ventilatory support Rojas et al. (2003) US Infants <1500 g Minimal ventilatory support Study design Quality n reported (started) Comments Participants

Category/intervention

M. J. Renfrew et al.

1. Enhanced motherinfant contact/kangaroo skin-to-skin contact

Whitelaw et al. (1988) UK

Blaymore Bier et al. (1997) US Kadam et al. (2005) India Cattaneo et al. (1998) 3 sites: Ethiopia Indonesia Mexico Sloan et al. (1994) Ecuador Moderate 279 (285) infants Many differences between sites RCT Daily contact not reported (intervention up to discharge) RCT Moderate 47 (50) infants 39 (41) mothers Moderate 89 (89) infants

Infants <1500 g Gavage fed Infants <1800 g On oral feeds Singleton infants 10001999 g On enteral feeds

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RCT Daily contact 1 h (intervention up to discharge) RCT Daily contact up to 8 h in two 4-h periods (intervention up to discharge) RCT Daily contact at hospital visits (mean 2.1 h)(intervention up to and beyond discharge) RCT Daily contact 10 min (intervention 10 days) RCT Daily contact 1 h (intervention up to discharge) RCT Daily contact 20 h (intervention up to 40th week postnatal age) Singleton infants <2000 g On enteral feeds Mosley et al. (2001) UK RCT Infants born at 3037 weeks Infants of 3236 weeks, <1700 g Infants <34 weeks Rocha et al. (2002) Brazil Collins et al. (2004) Australia Moderate 268 for bf at discharge (300) Author supplied breast-feeding data on request Moderate n = 14 (16) Very small pilot study Moderate n = 78 (83) Good n = 303 (319) High rates of non-compliance Good n = 303 (310) High rates of non-compliance as above Collins et al. (2004) Australia Groh-Wargo et al. (1995) USA RCT 2 2 design, cup feeding vs. bottle feeding (and paciers vs. no paciers) RCT 2 2 design, paciers vs. no paciers (and cup feeding vs. bottle feeding) as above RCT Infants <34 weeks as above Mothers had to express milk for at least 4 weeks to be included VLBW infants (1500 g) at least 7 days old Jones et al. (2001) UK RCT Also studied massage vs. no massage before expressing; results for no massage only here for comparison with Groh-Wargo 1995 Moderate n = 36 (possibly >36) NB: CIs by group reported by study author were used to calculate SDs and sample t-tests by review authors. These data are not based on an intention-to-treat analysis Moderate n = 36 (52) Mothers of recently born infants

2. Interim feeding methods/cup feeding vs. bottle feeding

2. Interim feeding methods/ paciers vs. no paciers

3. Methods of expressing breastmilk/sequential vs. simultaneous pumping

3. Methods of expressing breastmilk/novel manual pump vs. standard electric pump Fewtrell et al. (2001) UK RCT Good n = 118 (145) All mothers were recruited within 3 days of birth Pereira et al. (1984) USA Beforeafter

4. Breastfeeding education and support/breastfeeding support from trained peer supporters Agrasada (2005) Philippines RCT with three groups: breastfeeding peer counselling (BC), child care peer counselling (CC) and no peer counselling (C) Moderate n = 402 (402) Supporters were home-based volunteers Good n = 179 (204) Intervention began following hospital discharge Supporters were home-based

Mothers providing milk for their infant(s) Infants born at <35 weeks gestation Singletons reported separately Records of admissions before and after the intervention Infants who died were excluded

4. Breastfeeding education and support /hospital-based support from lactation consultants Gonzalez et al. (2003) USA Pinelli et al. (2001) Canada RCT Beforeafter

First-time mothers 18 years, intending to breastfeed Singleton, healthy LBW (<2500 g) infants, born vaginally at term (3742 weeks) and discharged on or before postnatal day 3 Random sample of records of admissions before and after intervention Singleton VLBW infants (<1500 g) fed mothers milk by parental choice

Jones et al. (2004) UK

Beforeafter

Moderate n = 350 (350) Intervention was IBCLC service Good n = 115 at 1 year (128 randomized) Intervention delivered by research lactation consultant Moderate 34 (42) staff 140 (140) sets of records

Pineda (2006) USA Merewood et al. (2003) USA Beforeafter

5. Staff training/ve taught modules (total 10 h to complete) plus practical assessments and tutorials 5. Staff training/self-study or in-service training (1 March14 April 2005) 6. Organization of care/ introduction of changes on the unit leading to baby friendly accreditation Beforeafter Bicalho-Mancini & Velasquez-Melendez (2004) Brazil Beforeafter

Moderate 56 (56) staff (total staff 88) 135 (135) sets of records Good n = 227 (227) for breastfeeding initiation n = 84 (84) at 2 weeks old Moderate Outcomes reported as %, n unclear (495 sets of records)

Records of infants admitted before and after the intervention Mothers intended to breastfeed VLBW infants admitted before and after the intervention Infants directly admitted to the study unit before and after the intervention 38% included infants were >37 weeks gestation Infants directly admitted to study unit before and after intervention 22.5% infants >37 weeks gestation; 430/495 (87%) appropriate/large for gestational age

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LBW, low birthweight; RCT, randomized controlled trial; CI, condence interval; VLBW, very low birthweight; IBCLC, International Board Certied Lactation Consultant.

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(Kadam et al. 2005). Two further studies from a total of four sites in resource-poor countries also found no effect on exclusive breastfeeding at discharge with the exception of one site. In one study, the intensity of daily contact was not reported (kangaroo contact: 124/140, control: 141/160; RR 1.01, 95% CI 0.93 1.09) (Sloan et al. 1994). The other evaluated daily contact for 20 h at three sites (Site 1: kangaroo contact: 51/52, control: 48/54; RR 1.10, 95% CI 1.001.22; Site 2: kangaroo contact: 40/50, control: 40/50; RR 1.00, 95% CI 0.821.22, Site 3: kangaroo contact: 37/47, control: 5/32; RR 5.04, 95% CI 2.22 11.43) (Cattaneo et al. 1998). Authors noted the exclusive breastfeeding rates at enrolment were signicantly lower in Site 3, inuencing study ndings (Cattaneo et al. 1998). Secondary outcomes from these studies indicated important differences in health outcomes in the infants indicating a positive effect of kangaroo skin-to-skin care; these are reported in the full report of this study (available by August 2009 at http:// www.ncchta.org/project/htapubs.asp). All trials reported no adverse effects.

ready for oral feeds. No differences were identied between the groups for any breastfeeding at discharge (paciers: 108/151, no paciers: 107/152; RR 0.98, 95% CI 0.851.14), at 3 months after discharge (paciers: 53/151, no paciers: 58/152; RR 1.09, 95% CI 0.811.46) and at 6 months after discharge (paciers: 34/151, no paciers: 43/152; RR 1.26, 95% CI 0.851.85). Again, signicant compliance problems were reported.

Methods of expressing breastmilk

This section examined the equipment, techniques and regimens used to express breastmilk. Three studies, all RCTs, are reported here. Two were conducted in the UK (Fewtrell et al. 2001; Jones et al. 2001) and one in the USA (Groh-Wargo et al. 1995). One was rated good quality (Fewtrell et al. 2001) and two were rated moderate quality (Groh-Wargo et al. 1995; Jones et al. 2001). Participants were socio-economically mixed. Each study tested a unique combination of equipment, techniques and regimens, including double or simultaneous vs. single pumping, electrical and hand-operated pumps, and pumps using suction alone or suction with compression to remove the breastmilk. Studies predominantly measured the volume of milk produced in the short term with very limited assessment of exclusivity or duration of breastfeeding or breastmilk feeding or of breastmilk composition. Details of mothers and infants care including factors that may have acted as co-interventions were lacking. The heterogeneity of design and lack of detail limit results that can be reported. In a UK study mothers using an electric pump expressed signicantly more at a single feed during the rst 2 weeks when pumping their breasts simultaneously (double pumping, n = 17) rather than sequentially (single pumping, n = 19) (Jones et al. 2001) [difference between means (simultaneous minus sequential) 36.37 g, 95% CI 26.5246.22]. Mean fat concentration was not affected [difference between means (sequential minus simultaneous) 0.1 g/l, 95% CI -1.48 to 1.68]. At later time points no differences between single or double electrical pumping were identied in another study (GrohWargo et al. 1995) (simultaneous n = 16, sequential n = 16; mean difference 102.00 ml/week, 95% CI -1268.57 to 1472.57). A further study found that an electric pump offered no advantage over a novel hand pump (Fewtrell et al. 2001) (hand pump 62/89, electric pump 53/78; RR 1.03, 95% CI 0.841.26).

Interim feeding methods

Studies included in this section examined ways of feeding the baby enterally until direct feeding from the breast is possible. Studies examined cup vs. bottle feeding and pacier use vs. no pacier use. Three RCTs (Mosley et al. 2001; Rocha et al. 2002; Collins et al. 2004) that measured breastfeeding outcomes were identied; two (Mosley et al. 2001; Collins et al. 2004) from industrialized countries. One study was rated as good quality (Collins et al. 2004), but it had signicant compliance problems. Confounding factors included the use of paciers and caregivers ngers for non-nutritive sucking. Feeding using a bottle and teat was the standard method used in included trials, and both staff and mothers were less familiar with cup feeding. One good-quality trial comparing cup and bottle feeding (Collins et al. 2004) reported an increase in the proportion of infants exclusively breastfeeding at discharge in the group allocated to cup feeding (Cup: 92/151, Bottle: 72/152; RR 1.29, 95% CI 1.041.59). A much smaller trial of only moderate quality (Mosley et al. 2001) found no difference (Cup: 4/6, Bottle: 6/6; RR 0.89, CI 0.441.78). Infants allocated to the cup feeding group were discharged slightly later but ndings were confounded by hospital policy and poor compliance (Collins et al. 2004). Severe oxygen desaturation occurred more often in infants allocated to the bottle feeding group in the only trial to report this parameter (Rocha et al. 2002). One trial (Collins et al. 2004) also examined the use of paciers vs. no paciers in the same group of infants, who were

Breastfeeding education and support

The studies identied in this section examined provision of education and support for mothers of infants admitted to neonatal units. Four studies are reported; two moderate-quality

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beforeafter studies in US neonatal units (Pereira et al. 1984; Gonzalez et al. 2003), a good-quality Canadian RCT that recruited very-low-birthweight infants (Pinelli et al. 2001), and a good-quality RCT that recruited term LBW infants from the Philippines (Agrasada 2005). The Canadian study (Pinelli et al. 2001) included a large proportion of mothers of higher social class; the other studies recruited women from more mixed socio-economic backgrounds. One US beforeafter study (Pereira et al. 1984) and the Philippines RCT (Agrasada 2005) investigated provision of trained peer breastfeeding supporters. The US study (Pereira et al. 1984) found higher rates of any breastfeeding after the introduction of peer support (before 32/192, after 64/210; RR 1.83, 95% CI 1.252.66). The study from the Philippines (Agrasada 2005) noted higher prevalence in the group allocated to breastfeeding peer counselling (any breastfeeding at 3 months, peer counselling 49/68, no counselling 37/69, RR 1.34, 95% CI 1.03 1.75; any breastfeeding at 6 months, peer counselling 43/68, no counselling 20/69, RR 2.18, 95% CI 1.453.29; exclusive breastfeeding from birth to 6 months, peer counselling 32/68, no counselling 0/69, RR 65.94, 95% CI 4.121055.60). A US beforeafter study (Gonzalez et al. 2003) examined hospital-based support from lactation consultants and noted an increase after the intervention in the number of infants receiving their own mothers milk in hospital (before 54/175, after 82/175; RR 1.52, 95% CI 1.161.99) and at discharge (before 40/175, after 65/175; RR 1.63, 95% CI 1.162.27). The Canadian RCT (Pinelli et al. 2001), however, found no effect on breastfeeding rates at term (hospital lactation consultant support 38/64, standard care 36/64; RR 1.06, 95% CI 0.781.42) nor at any time point up to 1 year. The participants in both groups were relatively afuent and accessed other lactation consultants in the community.

breastfeeding in hospital (before: 21/81, after: 24/54; RR 1.71, 95% CI 1.072.75) but no change in the proportion of breast milk ever provided in hospital (before: 60/81, after: 46/54; RR 1.15, 95% CI 0.971.36) or at discharge (before: 29/81, after: 22/54; RR 1.14, 95% CI 0.741.76) (Pineda 2006).

Organization of care
In this section studies that examined the process or organization of care were examined. One good-quality (Merewood et al. 2003) and one moderate-quality beforeafter study (Bicalho-Mancini & Velasquez-Melendez 2004) were included. Both examined changes related to Unicef Baby Friendly Hospital Initiative accreditation of the associated maternity hospital (World Health Organsiation 1989). Mothers in one study were mostly black American and Hispanic women with typically low breastfeeding prevalence (Merewood et al. 2003); the other was conducted among Brazilian women with typically high breastfeeding prevalence (Bicalho-Mancini & Velasquez-Melendez 2004). The US study (Merewood et al. 2003) reported signicant increases in the number of infants receiving any breastmilk during the rst week of enteral feeds (before: 38/110, after: 87/117; RR 2.15, 95% CI 1.632.84) and the number of infants receiving any breastmilk at two weeks (before: 12/43, after: 27/41; RR 2.36, 95% CI 1.394.00). Both studies reported signicant increases in the duration of exclusive breastfeeding; at two weeks (before: 4/43, after: 27/41; RR 4.2, 95% CI 1.53 11.50) (Merewood et al. 2003) and at hospital discharge (before: 90/250, after: 134/245; RR 1.52, 95% CI 1.241.86) (BicalhoMancini & Velasquez-Melendez 2004).

Discussion and conclusions

This review has systematically characterized the evidence base underpinning interventions which could increase the prevalence of breastfeeding for babies starting life in neonatal units, and thereby improve the health of babies and their mothers. Nineteen studies not previously included in previous systematic reviews were found in the main review of 48 studies, six of which are included in the sub-set of 21 studies reported in this paper. We identied effective interventions including close contact between mother and infant, staff training, support for mothers, and enhancing the organization of care. These interventions are not in routine use in neonatal units in the UK or internationally (Cuttini et al. 1999; Redshaw & Hamilton 2006), although there some examples of good practice (Meier et al. 2004; Charpak 2008; Nyqvist 2008). Important effective and achievable interventions included: kangaroo skin-to-skin contact; simultaneous milk expression

Staff training
Studies in this category examined interventions intended to enhance staff training in breastfeeding/breastmilk feeding in neonatal units. Two moderate-quality beforeafter studies were identied, one from the UK (Jones et al. 2004) and one from the USA (Pineda 2006). Both examined a multifaceted and multidisciplinary training programme for staff in neonatal units. In the UK study more infants received expressed breastmilk after staff training (before: 75/90, after: 72/76; RR 1.15, 95% CI 1.031.29) and more were put to the breast (before: 57/90, after: 65/76; RR 1.35, 95% CI 1.131.62), but rates of breastfeeding at discharge did not differ signicantly (before: 49/90, after: 54/76; RR 1.31, 95% CI 1.031.65) (Jones et al. 2004). After the US intervention there was an increase in the number of mothers

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from both breasts in the early weeks after birth; peer support in hospital and community; multidisciplinary staff training; and Baby Friendly accreditation of the associated maternity hospital. Feeding from a cup as opposed to a bottle was shown to increase rates of exclusive breastfeeding at discharge, but applicability of this nding to provision of care in the UK may be more limited. The observation that cup feeding may take more time may be associated with staff inexperience, but this seemed to limit its acceptance by both staff and mothers. This is illustrative of a broader difculty with interpretation of evidence in this eld where understafng is a serious problem and current practice in supporting breastfeeding and feeding with breastmilk is widely acknowledged to be suboptimal (Redshaw & Hamilton 2006; BLISS 2008). Importantly, the interventions we have identied inter-relate; interventions seem likely to be less effective if implemented individually. We noted that the greatest improvements were associated with multifaceted interventions, particularly those which included staff training or provided an environment in which mothers were encouraged and supported to breastfeed or express milk while maintaining close contact with their infants. This analysis is supported by the evidence of increased breastfeeding rates in neonatal units within a Unicef Baby Friendly accredited maternity service. It is also congruent with the evidence base for term infants and their mothers, where multifaceted interventions have been shown to be most effective (Dyson et al. 2006). Several interventions were shown to be more effective among women who intended to breastfeed. Although we found no public health or policy-related studies, this observation suggests that public health interventions in the antenatal period that increase generally the number of women intending to breastfeed (Dyson et al. 2005) could increase breastfeeding rates among mothers of infants in neonatal care. We have acknowledged that the evidence is limited by the low number and overall quality of studies. Moreover its contextual relevance to UK neonatal units is limited; we have particularly emphasized that most of the infants studied were clinically stable and likely to be untypical of the population served by tertiary neonatal units.

of the Unicef Baby Friendly Initiative. More support for mothers is clearly needed; the process of care should include encouragement and support for breastmilk feeding and timely initiation of breastfeeding. Kangaroo skin-to-skin contact should be encouraged when infants are clinically stable and facilities and support provided to facilitate effective expression and storage of breastmilk. Achieving these developments will require multidisciplinary staff training, but maximizing parentinfant contact also has broader implications for service provision such as improving the design of hospital facilities, provision of parents accommodation, and management of neonatal networks and transport. Infants starting life in neonatal units, and their mothers, should be included in future public health policy developments and breastfeeding targets. National and local surveillance of feeding for infants in neonatal units and following discharge is needed to inform future policy and practice development, particularly if combined with measures of health outcomes and costs. The development of consensus denitions would assist this; one issue is the need to separate receipt and production of breastmilk from feeding at the breast. In the context of neonatal care settings, we propose the following denitions: Initiation of breastfeeding The mother has put the infant to the breast and the infant has demonstrated nutritive sucking. Initiation of feeding with breastmilk For the infant: the infant has received breastmilk enterally (whether mothers own or donor breast milk should be noted, as should the method). For the mother: the mother has attempted to express breastmilk by any method.

Implications for research

We identied studies from a range of industrialized and resource-poor countries. The circumstances in which these were performed and the participating populations of mothers, babies, peer and professional supporters may have been very different from those prevailing in the UK. These factors affect delivery of both the intervention and type of standard care offered indicating a need to examine interventions within the context of current National Health Service neonatal service provision. Outcomes reported were often short-term measures of milk production rather than longer-term indicators of breastfeeding duration, infant health and development, or maternal well-being. This creates obstacles to establishing clearly a connection with improved health and well-being of the mother and baby. Highquality studies to examine infant feeding and associated health

Implications for practice and policy

We observed that the greatest effects were generally associated with provision of practical support and encouragement from someone peer or professional trained in the management of breastfeeding. This was most evident where an intervention formed part of a multifaceted package of care meeting standards

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outcomes of infants and their mothers are needed, particularly among women on low incomes and from diverse ethnic groups. Priorities include studies of supportive environments for mothers; initiating and sustaining milk production; and interim feeding methods. Our interpretation of current evidence differs from Flint and colleagues (2007) in regard to cup feeding; research conducted in an environment where staff are familiar with and supportive of the use of cups would illuminate this debate. Future studies should evaluate developmental outcomes and costs, and should incorporate the views of staff and parents in their design. Increased surveillance of infant feeding and outcomes in neonatal units as suggested above would also facilitate the design of large multi-centre intervention studies. Additional gaps in the evidence identied related to the care of less clinically stable infants and those with special needs, a vulnerable group who could potentially derive greatest benet from breastfeeding. We also found that the impact of public health and policy interventions, the role of family and community staff, and the organization of neonatal services including clinical networks had not been formally studied.

Acknowledgements
The study was funded by a grant from the National Institute for Health Research Health Technology Assessment programme: Grant No. 06-34/02. This paper does not represent the views of the NIHR or the Department of Health. Advisory Group: Gene Anderson, Rosie Dodds, Sandra Lang, Shelley Mason, Paula Meier, Josephine Patterson, Mark Sculpher, Sarah OSullivan, Amanda Sowden, Louise Wallace. Additional expert input: Jake Abbass, Sue Ashmore, Martin Bland, Victoria Dugbartey, Nick Embleton, Alan Fenton, Kirsteen Macleod, Rhona McInnes, Kerstin Nyqvist, Elizabeth Jones, Caroline King, Camilla Kingdon, Paula Sisk, Gillian Weaver: and four anonymous peer reviewers. Administration: Jenny Brown. The University of Plymouth supported Elizabeth Stenhouse during this study. Dawn Craig and Stephen Rice, Centre for Reviews and Dissemination, University of York, contributed substantively to this review.

Key messages
Breastfeeding/breastmilk feeding substantially increases the life chances of infants cared for in neonatal units, yet rates of initiation, duration and exclusivity are low in many countries. Existing reviews have been narrow in their scope or not methodologically rigorous, and existing studies are diverse in topic, method, sub-group studied and outcomes measured resulting in diverse conclusions and confusion in practice; a broad and rigorous review was needed. Nineteen studies not previously included in reviews have been identied, and effective clinical, education and public health interventions have been identied that are not in current routine practice. These include kangaroo skin-toskin contact, simultaneous expression in the early weeks, peer support in hospital and community, multidisciplinary staff training, and Baby Friendly accreditation of the associated maternity hospital. There are important evidence gaps related to public health and policy as well as clinical interventions. Feeding for infants in neonatal units should be included in future public health policy developments and breastfeeding targets, and routine monitoring; denitions have been proposed for this purpose.

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