Breastfeeding Promotion for Infants in Neonatal

Breastfeeding promotion for infants in neonatalunits: a systematic reviewcch_1018 165..178

M. J. Renfrew,* L. Dyson,* F. McCormick,* K. Misso,† E. Stenhouse,‡ S. E. King* andA. 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 George’s Hospital Medical School, University of London, London, UK

Accepted for publication 28 June 2009

Keywordsbreastfeeding,breastfeeding definitions,clinical interventions,neonatal units, publichealth intervention,systematic review

Correspondence:Mary J Renfrew, RM, PhD,Mother and InfantResearch Unit,Department of HealthSciences, University ofYork, Heslington, YorkYO10 5DD, UKE-mail: [email protected]

AbstractBackground 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 identified 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 identified, 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

identified 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 definitions

are proposed.

This article ‘Breastfeeding promotion for infants in neonatal units: a systematic review’ was written by M. J. Renfrew, L. Dyson, F. McCormick, K. Misso ofUniversity 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 thepermission of the Controller of HMSO and the Queen’s Printer for Scotland.

Child: care, health and developmentOriginal Article doi:10.1111/j.1365-2214.2009.01018.x

© 2009 Crown copyright 165

Introduction

Promotion, protection and support of breastfeeding and of

feeding with breastmilk in neonatal units are vital to the pres-

ervation 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 identified 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 low-

birthweight infants have five times the risk of necrotizing

enterocolitis, a condition associated with a mortality of

approximately 20% and significant 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 low-

birthweight infants fed on formula (Anderson et al. 1999; Smith

et al. 2003; Vohr et al. 2006, 2007; Kramer et al. 2008), an impor-

tant finding in a group where cognitive impairment is a fre-

quent adverse outcome (Costeloe & EPICure Study Group

2006). Feeding from the breast may facilitate other beneficial

outcomes, for example a reduction in procedural pain (Gray

et al. 2000; Carbajal et al. 2003; Shah et al. 2006).

Many factors make breastfeeding difficult in this setting. The

fragility of preterm and sick infants, their changing nutritional

and health needs, separation of mother and baby, difficulty in

producing breastmilk (Cregan et al. 2000; Hartmann & Ramsay

2006; Henderson et al. 2008), and anxiety, distress and fear pro-

voked 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 mother’s scent, skin-to-skin care and family

involvement in care (Liu et al. 2007), all of which are inherent in

breastfeeding. The mother’s 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 breast-

milk 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 fields 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 inter-

ventions (cf. Collins et al. 2003; Conde-Agudelo et al. 2003;

Flint et al. 2007) and has been conducted using rigorous sys-

tematic 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 Dissemina-

tion (Centre for Reviews and Dissemination 2001).

Structured searches were conducted on 19 electronic data-

bases 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 pub-

lished August 2009).

Eligible studies had to fulfil the following criteria:

• Participants: infants, or mothers of infants, who were admit-

ted 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 breast-

feeding or feeding with breastmilk in neonatal units or fol-

lowing discharge.

• Outcomes: Primary outcomes: measures of breastfeeding and

breastmilk feeding. In studies where these were reported, sec-

ondary outcomes examined included clinical/health, process,

psychosocial and cost-effectiveness outcomes.

• Study designs: RCTs, randomized crossover studies, concur-

rent comparisons before/after studies.

166 M. J. Renfrew et al.

© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178

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

definitions of study quality were used based on National Insti-

tute 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 fulfilled and where they

were not met, the study conclusions were

thought very unlikely to alter

Moderate quality: some criteria fulfilled and where they were

not met, the study conclusions were thought

unlikely to alter

Poor quality: few criteria fulfilled and the conclusions of

the study were thought very likely to alter.

Serious caution is warranted in interpreta-

tion 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 field. Studies were conducted from

1984 to 2007 in 17 countries; 11 resource-poor and six indus-

trialized countries. Nine topic categories were identified. 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-low-

birthweight and premature infants on respiratory support.

Several included twins and multiple births, but only one (Blay-

more Bier et al. 1997) reported analyses separately for these.

Psychosocial data were very limited and virtually no cost out-

comes 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 unfa-

miliar 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 cal-

culate outcome data as relative risks (RR) where appropriate, and

95% confidence 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 (Griffin 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

mother–infant 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 (Griffin 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

Breastfeeding promotion for infants in neonatal units 167


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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 summa-

rized in Fig. 1 (QUORUM flowchart) 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 before–after

designs. Twelve (57%) were conducted in industrialized settings

(five of these from the UK). Six of the original nine study topic

categories are reported below.

Enhanced mother–infant 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 mother’s breasts. The timing and duration

of contact varied across the studies and between participants.

All studies were conducted among infants defined 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) identified increased dura-

tion of any breastfeeding prior to, at, or up to 1 month after

hospital discharge. Three of these (Whitelaw et al. 1988; Blay-

more Bier et al. 1997; Boo & Jamli 2007) evaluated short dura-

tion 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 significant increase in the duration of any breast-

feeding at chosen time points including: prior to hospital dis-

charge (kangaroo contact: 21/64, control: 6/62; RR 3.39, 95% CI

1.47–7.83) (Boo & Jamli 2007); at hospital discharge (kangaroo

contact: 19/64, control: 9/62; RR 2.05, 95% CI 1.00–4.17) (Boo

& Jamli 2007), kangaroo contact: 19/21, control: 11/20; RR 1.65,

95% CI 1.08–2.50) (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 1.03–3.70) (Whitelaw et al.

1988), kangaroo contact: 10/21, control: 2/20; RR 4.76, 95% CI

1.19–19.10) (Blaymore Bier et al. 1997). The findings in one

study (Boo & Jamli 2007) may have been influenced 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 significant 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 0.91–3.08).

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 [kan-

garoo 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]

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

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

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

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

Citations referred to third reviewer (n=119)

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)

Papers excluded from further evaluation (n=87)

Studies included in this paper (n=21) comprising:

RCTs (n=15) Industrialized countries ( n=12)

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)

Figure 1. Summary of review flow. The following flowchart is based onthe QUORUM statement flow diagram [The Lancet (1999) http://www.consort-statement.org/index.aspx?o=1345, downloaded on 23 October2008] to summarize the review flow for the identification of relevantstudies. RCT, randomized controlled trial. *Reported in 51 papers.



Tab

le2

.D

etai

lsof

incl

ude

dst

udi

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per

incl

usi

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iter

iafo

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ispa

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clu

ded

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die

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ud

yd

esig

nQ

ual

ity

nre

po

rted

(sta

rted

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om

men

tsP

arti

cip

ants

1.En

han

ced

mo

ther

–in

fan

tco

nta

ct/k

ang

aro

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in-t

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kin

con

tact

Bo

o&

Jam

li(2

007)

Mal

aysi

aRC

T Dai

lyco

nta

ct1

h(in

terv

enti

on

up

tod

isch

arg

e)

Mo

der

ate

126

(128

)In

fan

ts<1

500

gM

inim

alve

nti

lato

rysu

pp

ort

Roja

set

al.(

2003

)U

SRC

T Dai

lyco

nta

ctu

pto

8h

intw

o4-

hp

erio

ds

(inte

rven

tio

nu

pto

dis

char

ge)

Mo

der

ate

57(6

0)C

om

plia

nce

low

inb

oth

gro

up

s

Infa

nts

<150

0g

Min

imal

ven

tila

tory

sup

po

rt

Wh

itel

awet

al.(

1988

)U

KRC

T Dai

lyco

nta

ctat

ho

spit

alvi

sits

(mea

n2.

1h

)(in

terv

enti

on

up

toan

db

eyo

nd

dis

char

ge)

Mo

der

ate

71(7

1)Va

riab

leco

mp

lian

ce

Infa

nts

<150

0g

No

oxyg

eneq

uip

men

t

Bla

ymo

reB

ier

etal

.(19

97)

US

RCT D

aily

con

tact

10m

in(in

terv

enti

on

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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 exclu-

sive breastfeeding at discharge with the exception of one site. In

one study, the intensity of daily contact was not reported (kan-

garoo 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 1.00–1.22; Site 2: kangaroo contact:

40/50, control: 40/50; RR 1.00, 95% CI 0.82–1.22, Site 3: kan-

garoo 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 significantly lower in Site

3, influencing study findings (Cattaneo et al. 1998).

Secondary outcomes from these studies indicated important

differences in health outcomes in the infants indicating a posi-

tive 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.

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 pacifier use vs. no

pacifier use. Three RCTs (Mosley et al. 2001; Rocha et al. 2002;

Collins et al. 2004) that measured breastfeeding outcomes were

identified; 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 significant compliance problems.

Confounding factors included the use of pacifiers and caregiv-

ers’ fingers 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 allo-

cated to cup feeding (Cup: 92/151, Bottle: 72/152; RR 1.29, 95%

CI 1.04–1.59). 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 0.44–1.78). Infants allocated to the cup feeding

group were discharged slightly later but findings were con-

founded 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 paci-

fiers vs. no pacifiers in the same group of infants, who were

ready for oral feeds. No differences were identified between the

groups for any breastfeeding at discharge (pacifiers: 108/151, no

pacifiers: 107/152; RR 0.98, 95% CI 0.85–1.14), at 3 months

after discharge (pacifiers: 53/151, no pacifiers: 58/152; RR 1.09,

95% CI 0.81–1.46) and at 6 months after discharge (pacifiers:

34/151, no pacifiers: 43/152; RR 1.26, 95% CI 0.85–1.85). Again,

significant 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 dura-

tion 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

significantly more at a single feed during the first 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 26.52–46.22]. Mean fat concentra-

tion 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 identified in another study (Groh-

Wargo 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 advan-

tage over a novel hand pump (Fewtrell et al. 2001) (hand pump

62/89, electric pump 53/78; RR 1.03, 95% CI 0.84–1.26).

Breastfeeding education and support

The studies identified in this section examined provision of

education and support for mothers of infants admitted to neo-

natal units. Four studies are reported; two moderate-quality



before–after 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 before–after study (Pereira et al. 1984) and the Phil-

ippines 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 intro-

duction of peer support (before 32/192, after 64/210; RR 1.83,

95% CI 1.25–2.66). The study from the Philippines (Agrasada

2005) noted higher prevalence in the group allocated to breast-

feeding 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 1.45–3.29; exclusive breast-

feeding from birth to 6 months, peer counselling 32/68, no

counselling 0/69, RR 65.94, 95% CI 4.12–1055.60).

A US before–after 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 mother’s milk in hospital (before 54/175, after 82/175;

RR 1.52,95% CI 1.16–1.99) and at discharge (before 40/175,after

65/175; RR 1.63, 95% CI 1.16–2.27). 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 0.78–1.42) nor at any time point up to 1

year. The participants in both groups were relatively affluent and

accessed other lactation consultants in the community.

Staff training

Studies in this category examined interventions intended to

enhance staff training in breastfeeding/breastmilk feeding in

neonatal units. Two moderate-quality before–after studies were

identified, one from the UK (Jones et al. 2004) and one from the

USA (Pineda 2006). Both examined a multifaceted and multi-

disciplinary 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

1.03–1.29) and more were put to the breast (before: 57/90, after:

65/76; RR 1.35, 95% CI 1.13–1.62), but rates of breastfeeding at

discharge did not differ significantly (before: 49/90, after: 54/76;

RR 1.31, 95% CI 1.03–1.65) (Jones et al. 2004). After the US

intervention there was an increase in the number of mothers

breastfeeding in hospital (before: 21/81, after: 24/54; RR 1.71,

95% CI 1.07–2.75) but no change in the proportion of breast

milk ever provided in hospital (before: 60/81, after: 46/54; RR

1.15, 95% CI 0.97–1.36) or at discharge (before: 29/81, after:

22/54; RR 1.14, 95% CI 0.74–1.76) (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 before–after 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 preva-

lence (Bicalho-Mancini & Velasquez-Melendez 2004).

The US study (Merewood et al. 2003) reported significant

increases in the number of infants receiving any breastmilk

during the first week of enteral feeds (before: 38/110, after:

87/117; RR 2.15, 95% CI 1.63–2.84) and the number of infants

receiving any breastmilk at two weeks (before: 12/43, after:

27/41; RR 2.36, 95% CI 1.39–4.00). Both studies reported sig-

nificant 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 1.24–1.86) (Bicalho-

Mancini & Velasquez-Melendez 2004).

Discussion and conclusions

This review has systematically characterized the evidence base

underpinning interventions which could increase the preva-

lence 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 identified effective interventions including close

contact between mother and infant, staff training, support for

mothers, and enhancing the organization of care. These inter-

ventions 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



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 hospi-

tal. Feeding from a cup as opposed to a bottle was shown to

increase rates of exclusive breastfeeding at discharge, but appli-

cability of this finding 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 illus-

trative of a broader difficulty with interpretation of evidence in

this field where understaffing is a serious problem and current

practice in supporting breastfeeding and feeding with breast-

milk is widely acknowledged to be suboptimal (Redshaw &

Hamilton 2006; BLISS 2008).

Importantly, the interventions we have identified 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 breast-

feeding rates in neonatal units within a Unicef Baby Friendly

accredited maternity service. It is also congruent with the evi-

dence base for term infants and their mothers, where multifac-

eted 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 breast-

feed (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.

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

of the Unicef Baby Friendly Initiative. More support for mothers

is clearly needed; the process of care should include encourage-

ment and support for breastmilk feeding and timely initiation of

breastfeeding. Kangaroo skin-to-skin contact should be encour-

aged when infants are clinically stable and facilities and support

provided to facilitate effective expression and storage of breast-

milk. Achieving these developments will require multidisci-

plinary staff training, but maximizing parent–infant contact also

has broader implications for service provision such as improving

the design of hospital facilities, provision of parents’ accommo-

dation, 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, par-

ticularly if combined with measures of health outcomes and

costs. The development of consensus definitions 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 definitions:

• 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 mother’s own or donor breast milk

should be noted, as should the method).

For the mother: the mother has attempted to express breast-

milk by any method.

Implications for research

We identified 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 indicat-

ing 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. High-

quality studies to examine infant feeding and associated health



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; res-

earch 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 out-

comes in neonatal units as suggested above would also facilitate

the design of large multi-centre intervention studies.

Additional gaps in the evidence identified related to the care

of less clinically stable infants and those with special needs, a

vulnerable group who could potentially derive greatest benefit

from breastfeeding. We also found that the impact of public

health and policy interventions, the role of family and commu-

nity 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 Scul-

pher, Sarah O’Sullivan, Amanda Sowden, Louise Wallace.

Additional expert input: Jake Abbass, Sue Ashmore, Martin

Bland, Victoria Dugbartey, Nick Embleton, Alan Fenton, Kirs-

teen 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 Dis-

semination, University of York, contributed substantively to this

review.

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