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
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
Tab
le1
.C
ateg
orie
s,su
b-to
pics
,nu
mbe
rsan
dqu
alit
yof
stu
dies
show
ing
both
thos
ein
clu
ded
inth
efu
llre
view
and
thos
ere
port
edin
this
pape
r
Cat
ego
ries
of
stu
dy
top
ics
iden
tifi
ed
Sub
-to
pic
sid
enti
fied
infu
llre
view
(su
b-t
op
ics
rep
ort
edin
this
pa
per
)R
CTs
*(q
ual
ity
rate
dg
oo
d,
mo
der
ate,
po
or)
Oth
erco
ntr
olle
dst
ud
ies
(qu
alit
yra
ted
go
od
,m
od
erat
e,p
oo
r)
Tota
lstu
die
sin
the
full
revi
ew(q
ual
ity
rate
dg
oo
d,
mo
der
ate,
po
or)
Tota
lstu
die
sre
po
rted
inth
isp
aper
(qu
alit
yra
ted
go
od
,mo
der
ate)
Enh
ance
dm
oth
er–i
nfa
nt
con
tact
Kan
gar
oo
care
,ka
ng
aro
osk
in-t
o-s
kin
con
tact
,sk
in-t
o-s
kin
care
9(0
,8,
1)3
(0,
1,2)
12(0
,9,
3)7
RC
Ts(0
,7)
Inte
rim
feed
ing
met
ho
ds
and
rela
ted
inte
rven
tio
ns
Cu
pvs
.bo
ttle
,pa
cifi
ervs
.no
pa
cifi
er,n
aso
-gas
tric
tub
evs
.bo
ttle
,nip
ple
shie
lds
5(1
,2,
2)1
(0,
1,0)
6(1
,3,
2)3
RC
Ts(1
,2)
Met
ho
ds
of
exp
ress
ing
bre
astm
ilkSi
mu
lta
neo
us
vs.s
equ
enti
al
pu
mp
ing
,nov
elm
anu
alp
um
pvs
.sta
nd
ard
elec
tric
pu
mp
,ele
ctri
cp
um
pvs
.p
edal
op
erat
edp
um
pvs
.h
and
exp
ress
ion
6†(1
,3,
2)0
6(1
,3,
2)3
RC
Ts(1
,2)
Met
ho
ds
of
enh
anci
ng
bre
astm
ilkp
rod
uct
ion
Rela
xati
on
tap
e,b
reas
tm
assa
ge,
ther
apeu
tic
tou
ch,
syn
toci
no
nn
asal
spra
y,h
um
ang
row
thh
orm
on
e,M
eto
clo
pro
mid
e,D
om
per
ido
ne
7‡(1
,6,
0)0
7(1
,6,
0)0
Sup
po
rtin
go
pti
mal
nu
trit
ion
alin
take
fro
mb
reas
tmilk
Hin
dm
ilkfe
edin
g,te
ach
ing
mo
ther
sto
mea
sure
fat
con
ten
to
fth
eir
milk
,in
-ho
me
mea
sure
men
tso
fin
fan
tw
eig
ht
2(0
,0,
2)1
(1,
0,0)
3(1
,0,
2)0
Bre
astf
eed
ing
sup
po
rtan
ded
uca
tio
nfo
rm
oth
ers
Peer
sup
po
rt,h
osp
ita
lla
cta
tio
nco
nsu
lta
nt
sup
po
rt
3(2
,1,
0)3
(0,
2,1)
6(2
,3,
1)2
RC
Ts(2
,0)
2b
efo
re–a
fter
stu
die
s(0
,2)
Staf
fed
uca
tio
nan
dtr
ain
ing
Tra
inin
g/e
du
cati
on
ofh
ealt
hp
rofe
ssio
na
ls0
2(0
,2,
0)2
(0,
2,0)
2b
efo
re–a
fter
stu
die
s(0
,2)
Earl
yh
osp
ital
dis
char
ge
wit
hh
om
esu
pp
ort
Ho
me
visi
tsan
dsu
pp
ort
incl
ud
ing
ho
me
gav
age
feed
ing
2(0
,1,
1)0
2(0
,1,
1)0
Org
aniz
atio
no
fca
reU
nic
efB
aby
Frie
nd
lyIn
itia
tive
acc
red
ita
tio
no
fa
sso
cia
ted
ma
tern
ity
ho
spit
al,
oth
erst
and
ard
(s)
04
(1,
1,2)
4(1
,1,
2)2
bef
ore
–aft
erst
ud
ies
(1,
1)
Tota
ls34
*(5
,21
,8)
14(2
,7,
5)48
(7,
28,
13)
15RC
Ts(4
,11
)6
bef
ore
–aft
erst
ud
ies
(1,
5)To
tal2
1(5
,1
6)
RCT,
ran
do
miz
edco
ntr
olle
dtr
ail.
*In
clu
din
gth
ree
ran
do
miz
edcr
oss
over
stu
die
s,w
hic
hw
ere
alle
xclu
ded
fro
mth
isp
aper
.†F
ive
RC
Tsan
do
ne
ran
do
miz
edcr
oss
over
stu
dy.
‡Fiv
eR
CTs
and
two
ran
do
miz
edcr
oss
over
stu
die
s.
168 M. J. Renfrew et al.
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
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.
Breastfeeding promotion for infants in neonatal units 169
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
Tab
le2
.D
etai
lsof
incl
ude
dst
udi
esas
per
incl
usi
oncr
iter
iafo
rth
ispa
per
Cat
ego
ry/i
nte
rven
tio
nIn
clu
ded
stu
die
sSt
ud
yd
esig
nQ
ual
ity
nre
po
rted
(sta
rted
)C
om
men
tsP
arti
cip
ants
1.En
han
ced
mo
ther
–in
fan
tco
nta
ct/k
ang
aro
osk
in-t
o-s
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
10d
ays)
Mo
der
ate
47(5
0)in
fan
ts39
(41)
mo
ther
s
Infa
nts
<150
0g
Gav
age
fed
Kad
amet
al.(
2005
)In
dia
RCT D
aily
con
tact
1h
(inte
rven
tio
nu
pto
dis
char
ge)
Mo
der
ate
89(8
9)in
fan
tsIn
fan
ts<1
800
gO
no
ralf
eed
s
Cat
tan
eoet
al.(
1998
)3
site
s:Et
hio
pia
Ind
on
esia
Mex
ico
RCT D
aily
con
tact
20h
(inte
rven
tio
nu
pto
40th
wee
kp
ost
nat
alag
e)
Mo
der
ate
279
(285
)in
fan
tsM
any
diff
eren
ces
bet
wee
nsi
tes
Sin
gle
ton
infa
nts
1000
–199
9g
On
ente
ralf
eed
s
Slo
anet
al.(
1994
)Ec
uad
or
RCT D
aily
con
tact
no
tre
po
rted
(inte
rven
tio
nu
pto
dis
char
ge)
Mo
der
ate
268
for
bf
atd
isch
arg
e(3
00)
Au
tho
rsu
pp
lied
bre
ast-
feed
ing
dat
ao
nre
qu
est
Sin
gle
ton
infa
nts
<200
0g
On
ente
ralf
eed
s
2.In
teri
mfe
edin
gm
eth
od
s/cu
pfe
edin
gvs
.bo
ttle
feed
ing
Mo
sley
etal
.(20
01)
UK
RCT
Mo
der
ate
n=
14(1
6)Ve
rysm
allp
ilot
stu
dy
Infa
nts
bo
rnat
30–3
7w
eeks
Roch
aet
al.(
2002
)B
razi
lRC
TM
od
erat
en
=78
(83)
Infa
nts
of
32–3
6w
eeks
,<17
00g
Co
llin
set
al.(
2004
)A
ust
ralia
RCT 2
¥2
des
ign
,cu
pfe
edin
gvs
.b
ott
lefe
edin
g(a
nd
pac
ifier
svs
.n
op
acifi
ers)
Go
od
n=
303
(319
)H
igh
rate
so
fn
on
-co
mp
lian
ce
Infa
nts
<34
wee
ks
2.In
teri
mfe
edin
gm
eth
od
s/p
acifi
ers
vs.n
op
acifi
ers
Co
llin
set
al.(
2004
)A
ust
ralia
RCT 2
¥2
des
ign
,pac
ifier
svs
.no
pac
ifier
s(a
nd
cup
feed
ing
vs.
bo
ttle
feed
ing
)as
abov
e
Go
od
n=
303
(310
)H
igh
rate
so
fn
on
-co
mp
lian
ceas
abov
e
Infa
nts
<34
wee
ksas
abov
e
3.M
eth
od
so
fex
pre
ssin
gb
reas
tmilk
/seq
uen
tial
vs.
sim
ult
aneo
us
pu
mp
ing
Gro
h-W
arg
oet
al.(
1995
)U
SARC
TM
od
erat
en
=36
(po
ssib
ly>3
6)N
B:C
Isb
yg
rou
pre
po
rted
by
stu
dy
auth
or
wer
eu
sed
toca
lcu
late
SDs
and
sam
ple
t-te
sts
by
revi
ewau
tho
rs.T
hes
ed
ata
are
no
tb
ased
on
anin
ten
tio
n-t
o-t
reat
anal
ysis
Mo
ther
sh
adto
exp
ress
milk
for
atle
ast
4w
eeks
tob
ein
clu
ded
VLB
Win
fan
ts(�
1500
g)a
tle
ast
7d
ays
old
Jon
eset
al.(
2001
)U
KRC
TA
lso
stu
die
dm
assa
ge
vs.n
om
assa
ge
bef
ore
exp
ress
ing
;re
sult
sfo
rn
om
assa
ge
on
lyh
ere
for
com
par
iso
nw
ith
Gro
h-W
arg
o19
95
Mo
der
ate
n=
36(5
2)M
oth
ers
of
rece
ntl
yb
orn
infa
nts
170 M. J. Renfrew et al.
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
3.M
eth
od
so
fex
pre
ssin
gb
reas
tmilk
/nov
elm
anu
alp
um
pvs
.sta
nd
ard
elec
tric
pu
mp
Few
trel
leta
l.(2
001)
UK
RCT
Go
od
n=
118
(145
)A
llm
oth
ers
wer
ere
cru
ited
wit
hin
3d
ays
of
bir
th
Mo
ther
sp
rovi
din
gm
ilkfo
rth
eir
infa
nt(
s)In
fan
tsb
orn
at<3
5w
eeks
ges
tati
on
Sin
gle
ton
sre
po
rted
sep
arat
ely
4.B
reas
tfee
din
ged
uca
tio
nan
dsu
pp
ort
/bre
astf
eed
ing
sup
po
rtfr
om
trai
ned
pee
rsu
pp
ort
ers
Pere
ira
etal
.(19
84)
USA
Bef
ore
–aft
erM
od
erat
en
=40
2(4
02)
Sup
po
rter
sw
ere
ho
me-
bas
edvo
lun
teer
s
Reco
rds
of
adm
issi
on
sb
efo
rean
daf
ter
the
inte
rven
tio
nIn
fan
tsw
ho
die
dw
ere
excl
ud
ed
Ag
rasa
da
(200
5)Ph
ilip
pin
esRC
Tw
ith
thre
eg
rou
ps:
bre
astf
eed
ing
pee
rco
un
selli
ng
(BC
),ch
ildca
rep
eer
cou
nse
llin
g(C
C)a
nd
no
pee
rco
un
selli
ng
(C)
Go
od
n=
179
(204
)In
terv
enti
on
beg
anfo
llow
ing
ho
spit
ald
isch
arg
eSu
pp
ort
ers
wer
eh
om
e-b
ased
Firs
t-ti
me
mo
ther
s�
18ye
ars,
inte
nd
ing
tob
reas
tfee
dSi
ng
leto
n,h
ealt
hy
LBW
(<25
00g
)in
fan
ts,b
orn
vag
inal
lyat
term
(37–
42w
eeks
)an
dd
isch
arg
edo
no
rb
efo
rep
ost
nat
ald
ay3
4.B
reas
tfee
din
ged
uca
tio
nan
dsu
pp
ort
/ho
spit
al-b
ased
sup
po
rtfr
om
lact
atio
nco
nsu
ltan
ts
Go
nza
lez
etal
.(20
03)
USA
Bef
ore
–aft
erM
od
erat
en
=35
0(3
50)
Inte
rven
tio
nw
asIB
CLC
serv
ice
Ran
do
msa
mp
leo
fre
cord
so
fad
mis
sio
ns
bef
ore
and
afte
rin
terv
enti
on
Pin
elli
etal
.(20
01)
Can
ada
RCT
Go
od
n=
115
at1
year
(128
ran
do
miz
ed)
Inte
rven
tio
nd
eliv
ered
by
rese
arch
lact
atio
nco
nsu
ltan
t
Sin
gle
ton
VLB
Win
fan
ts(<
1500
g)
fed
mo
ther
’sm
ilkb
yp
aren
tal
cho
ice
5.St
aff
trai
nin
g/fi
veta
ug
ht
mo
du
les
(to
tal1
0h
toco
mp
lete
)plu
sp
ract
ical
asse
ssm
ents
and
tuto
rial
s
Jon
eset
al.(
2004
)U
KB
efo
re–a
fter
Mo
der
ate
34(4
2)st
aff
140
(140
)set
so
fre
cord
s
Reco
rds
of
infa
nts
adm
itte
db
efo
rean
daf
ter
the
inte
rven
tio
nM
oth
ers
inte
nd
edto
bre
astf
eed
5.St
aff
trai
nin
g/s
elf-
stu
dy
or
in-s
ervi
cetr
ain
ing
(1M
arch
–14
Ap
ril2
005)
Pin
eda
(200
6)U
SAB
efo
re–a
fter
Mo
der
ate
56(5
6)st
aff
(to
tals
taff
88)
135
(135
)set
so
fre
cord
s
VLB
Win
fan
tsad
mit
ted
bef
ore
and
afte
rth
ein
terv
enti
on
6.O
rgan
izat
ion
of
care
/in
tro
du
ctio
no
fch
ang
eso
nth
eu
nit
lead
ing
tob
aby
frie
nd
lyac
cred
itat
ion
Mer
ewo
od
etal
.(20
03)
USA
Bef
ore
–aft
erG
oo
dn
=22
7(2
27)f
or
bre
astf
eed
ing
init
iati
on
n=
84(8
4)at
2w
eeks
old
Infa
nts
dir
ectl
yad
mit
ted
toth
est
ud
yu
nit
bef
ore
and
afte
rth
ein
terv
enti
on
38%
incl
ud
edin
fan
tsw
ere
>37
wee
ksg
esta
tio
nB
ical
ho
-Man
cin
i&Ve
lasq
uez
-Mel
end
ez(2
004)
Bra
zil
Bef
ore
–aft
erM
od
erat
eO
utc
om
esre
po
rted
as%
,nu
ncl
ear
(495
sets
of
reco
rds)
Infa
nts
dir
ectl
yad
mit
ted
tost
ud
yu
nit
bef
ore
and
afte
rin
terv
enti
on
22.5
%in
fan
ts>3
7w
eeks
ges
tati
on
;430
/495
(87%
)ap
pro
pri
ate/
larg
efo
rg
esta
tio
nal
age
LBW
,lo
wb
irth
wei
gh
t;RC
T,ra
nd
om
ized
con
tro
lled
tria
l;C
I,co
nfid
ence
inte
rval
;VLB
W,v
ery
low
bir
thw
eig
ht;
IBC
LC,I
nte
rnat
ion
alB
oar
dC
erti
fied
Lact
atio
nC
on
sult
ant.
Breastfeeding promotion for infants in neonatal units 171
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
(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
172 M. J. Renfrew et al.
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
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
Breastfeeding promotion for infants in neonatal units 173
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
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
174 M. J. Renfrew et al.
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
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.
References
Agrasada, G. V. (2005) Postnatal Peer Counselling on Exclusive
Breastfeeding of Low-Birthweight Filipino Infants: Results of a
Randomised Controlled Trial. Acta Universitatis Upsaliensis,
Uppsala, Sweden.
Amali-Adekwu, O., Ogala, W. & Bode-Thomas, F. (2007) Hindmilk
and weight gain in preterm very low-birthweight infants. Pediatrics
International, 49, 156–160.
Anderson, J. W., Johnstone, B. M. & Remley, D. T. (1999)
Breast-feeding and cognitive development: a meta-analysis.
American Journal of Clinical Nutrition, 70, 525–535.
Bell, E. H., Geyer, J. & Jones, L. (1995) A structured intervention
improves breastfeeding success for ill or preterm infants.
MCN. The American Journal of Maternal Child Nursing, 20,
309–314.
Bicalho-Mancini, P. G. & Velasquez-Melendez, G. (2004) [Exclusive
breastfeeding at the point of discharge of high-risk newborns at a
Neonatal Intensive Care Unit and the factors associated with this
practice]. Jornal de Pediatria, 80, 241–248.
Bisquera, J. A., Cooper, T. R. & Berseth, C. L. (2002) Impact of
necrotizing enterocolitis on length of stay and hospital charges in
very low birth weight infants. Pediatrics, 109, 423–428.
Blaymore Bier, J. A., Ferguson, A. E., Morales, Y., Liebling, J. A., Oh,
W. & Vohr, B. R. (1997) Breastfeeding infants who were extremely
low birth weight. The American Academy of Pediatrics, 150,
1265–1269.
BLISS (2008) Breastfeeding or Expressing for A Sick or Premature Baby.
An Overview of 500 Women’s Experiences. BLISS, London, UK.
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 mea-
sured resulting in diverse conclusions and confusion in
practice; a broad and rigorous review was needed.
• Nineteen studies not previously included in reviews have
been identified, and effective clinical, education and public
health interventions have been identified that are not in
current routine practice. These include kangaroo skin-to-
skin contact, simultaneous expression in the early weeks,
peer support in hospital and community, multidisci-
plinary 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 breastfeed-
ing targets, and routine monitoring; definitions have been
proposed for this purpose.
Breastfeeding promotion for infants in neonatal units 175
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
Boo, N. Y. & Jamli, F. M. (2007) Short duration of skin-to-skin
contact: effects on growth and breastfeeding. Journal of Paediatrics
and Child Health, 43, 831–836.
Boyd, C. A., Quigley, M. A. & Brocklehurst, P. (2007) Donor breast
milk versus infant formula for preterm infants: a systematic review
and meta-analysis. Archives of Disease in Childhood. Fetal and
Neonatal Edition, 92, F169–F175.
Carbajal, R., Veerapen, S., Couderc, S., Jugie, M. & Ville, Y. (2003)
Analgesic effect of breast feeding in term neonates: randomised
controlled trial. British Medical Journal, 326, 13.
Cattaneo, A., Davanzo, R., Worku, B., Surjono, A., Echeverria, M.,
Bedri, A., Haksari, E., Osorno, L., Gudetta, B., Setyowireni, D.,
Quintero, S. & Tamburlini, G. (1998) Kangaroo mother care for
low birthweight infants: a randomized controlled trial in different
settings. Acta Paediatrica, 87, 976–985.
Centre for Reviews and Dissemination (2001) Undertaking
systematic reviews of research on effectiveness: CRD’s guidance for
those carrying out or commissioning reviews. CRD Report No 4
(2nd edition) March 2001.
Chalmers, B., Levin, A. & Van Pampus, M. G. (2003) Humane
perinatal care. Journal of Psychosomatic Obstetrics & Gynecology,
24, 53–54.
Charpak, N. (2008) Morbi-mortality of the low birth weight infant
and kangaroo mother care: the Colombian experience – Kangaroo
Foundation, Bogota. Oral Presentation, Proceedings of 7th
International Workshop on Kangaroo Mother Care, 8–11 October
2008. Sweden, Uppsala. Available at: http://kangaroo.javeriana.
edu.co/encuentros/7encuentro/workshop/NathalieCharpak.pdf
(last accessed 24 August 2009).
Charpak, N., Ruizpelaez, J. G., Figueroa, Z. D. & Charpak, Y. (1997)
Kangaroo mother versus traditional care for newborn infants
<=2000 grams: a randomized, controlled trial. Pediatrics, 100,
682–688.
Charpak, N., Ruiz-Pelaez, J. G., De Figueroa, C. Z. & Charpak, Y.
(2001) A randomized, controlled trial of kangaroo mother care:
results of follow-up at 1 year of corrected age. Pediatrics, 108,
1072–1079.
Collins, C. T., Makrides, M. & Mcphee, A. J. (2003) Early discharge
with home support of gavage feeding for stable preterm infants
who have not established full oral feeds (Review). Cochrane
Database of Systematic Reviews 4, CD003743. DOI: 10.1002/
14651858.CD003743.
Collins, C. T., Ryan, P., Crowther, C. A., McPhee, A. J., Paterson, S. &
Hiller, J. E. (2004) Effect of bottles, cups, and dummies on breast
feeding in preterm infants: a randomised controlled trial. British
Medical Journal, 329, 193–196.
Conde-Agudelo, A., Diaz-Rossello, J. L. & Belizan, J. M. (2003)
Kangaroo mother care to reduce morbidity and mortality in low
birthweight infants. [update of Cochrane Database of Systematic
Review, 2000;(4):CD002771; PMID: 11034759]. Cochrane Database
of Systematic Reviews, 4, CD002771.
Costeloe, K. & EPICure Study Group (2006) EPICure: facts and
figures; why preterm labour should be treated. An International
Journal of Obstetrics and Gynaecology, 113 (Suppl. 3), 10–12.
Erratum in: An International Journal of Obstetrics and Gynaecology,
2008; 115, 674–675.
Cregan, M. D., De Mello, T. R. & Hartmann, P. E. (2000) Pre-term
delivery and breast expression: consequences for initiating
lactation. Advances in Experimental Biology, 478, 427–428.
Cuttini, M., Rebagliato, M., Bortoli, P., Hansen, G., De Leeuw, R.,
Lenoir, S., Persson, J., Reid, M., Schroell, M. & De Vonderweid, U.
(1999) Parental visiting, communication, and participation in
ethical decisions: a comparison of neonatal unit policies in
Europe. Archives of Disease in Childhood Fetal & Neonatal Edition,
81, 84F.
Dyson, L., McCormick, F. M. & Renfrew, M. J. (2005) Interventions
for promoting the initiation of breastfeeding. Cochrane Database
of Systematic Reviews 2, CD001688. DOI: 10.1002/14651858.
CD001688.pub2.
Dyson, L., Renfrew, M. J., Mcfadden, A., Mccormick, F. M., Herbert,
G. & Thomas, J. (2006) Promotion of Breastfeeding Initiation and
Duration. Evidence into Practice Briefing. National Institute for
Health and Clinical Excellence, London, UK.
Edmond, K. & Bahl, R. (2006) Optimal Feeding of Low-Birth-Weight
Infants: Technical Review. World Health Organization, Geneva,
Switzerland.
El-Mohandes, A. E., Picard, M. B., Simmens, S. J. & Keiser, J. F.
(1997) Use of human milk in the intensive care nursery decreases
the incidence of nosocomial sepsis. Journal of Perinatology, 17,
130–134.
Feher, S. D., Berger, L. R., Johnson, J. D. & Wilde, J. B. (1989)
Increasing breast milk production for premature infants with a
relaxation/imagery audiotape. Pediatrics, 83, 57–60.
Fewtrell, M. S., Lucas, P., Collier, S., Singhal, A., Ahluwalia, J. S. &
Lucas, A. (2001) Randomized trial comparing the efficacy of a
novel manual breast pump with a standard electric breast pump in
mothers who delivered preterm infants. Pediatrics, 107, 1291–
1297.
Fewtrell, M. S., Loh, K. L., Blake, A., Ridout, D. A. & Hawdon, J.
(2006) Randomised, double blind trial of oxytocin nasal spray in
mothers expressing breast milk for preterm infants. Archives of
Disease in Childhood Fetal & Neonatal Edition, 91, F169–F174.
Flacking, R., Wallin, L. & Ewald, U. (2007) Perinatal and
socioeconomic determinants of breastfeeding duration in very
preterm infants. Acta Paediatrica, 96, 1126–1130.
Flint, A., New, K. & Davies, M. W. (2007) Cup feeding versus other
forms of supplemental enteral feeding for newborn infants unable
to fully breastfeed. Cochrane Database of Systematic Reviews:
Reviews 2. John Wiley & Sons, Ltd, Chichester, UK. DOI: 10.1002/
14651858.CD005092.pub2.
Furman, L., Minich, N. & Hack, M. (2002) Correlates of lactation in
mothers of very low birth weight infants. Pediatrics, 109, e57.
Furman, L., Taylor, G., Minich, N. & Hack, M. (2003) The effect of
maternal milk on neonatal morbidity of very low-birth-weight
infants. Archives of Pediatrics & Adolescent Medicine, 157, 66–71.
Gilks, J. & Watkinson, M. (2004) Improving breast feeding rates in
preterm babies: cup feeding versus bottle feeding. Journal of
Neonatal Nursing, 10, 118–120.
176 M. J. Renfrew et al.
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
Gonzalez, K. A., Meinzen-Derr, J., Burke, B. L., Hibler, A. J., Kavinsky,
B., Hess, S., Pickering, L. K. & Morrow, A. L. (2003) Evaluation of
a lactation support service in a children’s hospital neonatal
intensive care unit. Journal of Human Lactation, 19, 286–292.
Gray, L., Watt, L. & Blass, E. M. (2000) Skin-to-skin contact is
analgesic in healthy newborns. The American Academy of Pediatrics,
105, e14.
Griffin, T. L., Meier, P. P., Bradford, L. P., Bigger, H. R. & Engstrom,
J. L. (2000) Mothers performing creamatocrit measures in the
NICU: accuracy, reactions, and cost. JOGNN – Journal of Obstetric,
Gynecologic, & Neonatal Nursing, 29, 249–257.
Groh-Wargo, S., Toth, A., Mahoney, K., Simonian, S., Wasser, T. &
Rose, S. (1995) The utility of bilateral breast pumping system for
mothers of premature infants. Neonatal Network: The Journal of
Neonatal Nursing, 14, 31–36.
Gunn, A. J., Gunn, T. R., Rabone, D. L., Breier, B. H., Blum, W. F. &
Gluckman, P. D. (1996) Growth hormone increases breast
milk volumes in mothers of preterm infants. Pediatrics, 98,
279–282.
Gunn, A. J., Gunn, T. R. & Mitchell, E. A. (2000) Is changing the sleep
environment enough? Current recommendations for SIDS. Sleep
Medicine Reviews, 4, 453–469.
Hansen, W. F., Mcandrew, S., Harris, K. & Zimmerman, M. B.
(2005) Metoclopramide effect on breastfeeding the preterm
infant: a randomized trial. Obstetrics and Gynecology, 105,
383–389.
Hartmann, P. E. & Ramsay, D. T. (2006) Mammary anatomy and
physiology. In: Feeding and Nutrition in the Preterm Infant, 1st edn
(eds E. Jone, C. King), pp. 53–68. Elsevier Churchill Livingstone,
London, UK.
Henderson, J. J., Hartmann, P. E., Newnham, J. P. & Simmer, K.
(2008) Effect of preterm birth and antenatal corticosteroid
treatment on lactogenesis II in women. Pediatrics, 121, e92.
Hill, P. D., Aldag, J. C. & Chatterton, R. T. (1999) Effects of pumping
style on milk production in mothers of non-nursing preterm
infants. Journal of Human Lactation, 15, 209–216.
Hurst, N. M., Valentine, C. J., Renfro, L., Burns, P. & Ferlic, L.
(1997) Skin-to-skin holding in the neonatal intensive care unit
influences maternal milk volume. Journal of Perinatology, 17,
213–217.
Hurst, N. M., Meier, P. P., Engstrom, J. L. & Myatt, A. (2004) Mothers
performing in-home measurement of milk intake during
breastfeeding of their preterm infants: maternal reactions and
feeding outcomes. Journal of Human Lactation, 20, 178–187.
Jones, E., Dimmock, P. W. & Spencer, S. A. (2001) A randomised
controlled trial to compare methods of milk expression after
preterm delivery. Archives of Disease in Childhood Fetal & Neonatal
Edition, 85, F91–F95.
Jones, E., Jones, P., Dimmock, P. & Spencer, A. (2004) Evaluating
preterm breastfeeding training. The Practising Midwife, 7,
19–21.
Kadam, S., Binoy, S., Kanbur, W., Mondkar, J. A. & Fernandez, A.
(2005) Feasibility of kangaroo mother care in Mumbai. Indian
Journal of Pediatrics, 72, 35–38.
Kliethermes, P. A., Cross, M. L., Lanese, M. G., Johnson, K. M. &
Simon, S. D. (1999) Transitioning preterm infants with nasogastric
tube supplementation: increased likelihood of breastfeeding.
JOGNN: Journal of Obstetric, Gynecologic, and Neonatal Nursing,
28, 264–273.
Kramer, M. S., Aboud, F., Mironova, E., Vanilovich, I., Platt, R. W.,
Matush, L., Igumnov, S., Fombonne, E., Bogdanovich, N. &
Ducruet, T. (2008) Breastfeeding and child cognitive development:
new evidence from a large randomized trial. Archives of General
Psychiatry, 65, 578.
Liu, W. F., Laudert, S., Perkins, B., Macmillan-York, E., Martin, S. &
Graven, S. (2007) The development of potentially better practices
to support the neurodevelopment of infants in the NICU. Journal
of Perinatology, 27 (Suppl. 2), S48–S74.
Lucas, A., Morley, R., Cole, T. J. & Gore, S. M. (1994) A randomised
multicentre study of human milk versus formula and later
development in preterm infants. British Medical Journal, 70, 141.
Macfarlane, A. & Mugford, M. (2000) Birth Counts: Statistics of
Pregnancy and Childbirth, 2nd edn. University of Oxford, National
Perinatal Epidemiology Unit, Oxford, UK.
Mcinnes, R. & Chambers, J. (2006) Breastfeeding in Neonatal Units:
A Review of Breastfeeding Publications between 1990–2005. NHS
Health Scotland, Edinburgh, UK.
Meier, P. P., Brown, L. P., Hurst, N. M., Spatz, D. L., Engstrom, J. L.,
Borucki, L. C. & Krouse, A. M. (2000) Nipple shields for preterm
infants: effect on milk transfer and duration of breastfeeding.
Journal of Human Lactation, 16, 106.
Meier, P. P., Engstrom, J. L., Mingolelli, S. S., Miracle, D. J. &
Kiesling, S. (2004) The rush mothers’ milk club: breastfeeding
interventions for mothers with very-low-birth-weight infants.
Journal of Obstetric, Gynecologic, and Neonatal Nursing, 33,
164–174.
Merewood, A., Philipp, B. L., Chawla, N. & Cimo, S. (2003) The
baby-friendly hospital initiative increases breastfeeding rates in a
US neonatal intensive care unit. Journal of Human Lactation, 19,
166–171.
Merewood, A., Chamberlain, L. B., Cook, J. T., Philipp, B. L., Malone,
K. & Bauchner, H. (2006) The effect of peer counselors on
breastfeeding rates in the neonatal intensive care unit: results of a
randomized controlled trial. Archives of Pediatrics & Adolescent
Medicine, 160, 681–685.
Mersmann, C. A. (1993) Therapeutic Touch and Milk Letdown in
Mothers of Non-Nursing Preterm Infants. New York University, New
York, NY, USA.
Mosley, C., Whittle, C. & Hicks, C. (2001) A pilot study to assess the
viability of a randomised controlled trial of methods of
supplementary feeding of breast-fed pre-term babies. Midwifery,
17, 150–157.
Narayanan, I., Prakash, K., Prabhakar, A. K. & Gujral, V. V. (1982) A
planned prospective evaluation of the anti-infective property of
varying quantities of expressed breastmilk. Acta Paediatrica
Scandinavica, 71, 441–445.
National Institute for Health and Clinical Excellence (2005)
Guideline development methods chapters and appendices.
Breastfeeding promotion for infants in neonatal units 177
© 2009 Crown copyright, Child: care, health and development, 36, 2, 165–178
Available at: http://www.nice.org.uk/search/searchresults.
jsp?keywords=GUIDELINE%20DEVELOPMENT%20METHODS
%20MARCH%202005&startYear=0&startMonth=0&endYear=
0&endMonth=0&searchType=all&page=1.
Nyqvist, K. H. (2008) Evaluation of continuous KMC in a high tech
NICU, neonatal unit 95F, University Hospital, Uppsala and Dept of
Women’s and Children’s Health. Oral Presentation, Proceedings of
7th International Workshop on Kangaroo Mother Care, 8–11
October 2008. Available at: http://kangaroo.javeriana.edu.co/
encuentros/7encuentro/posters/YIVThemstromBlomqvist.pdf
Oddy, W. H. & Glenn, K. (2003) Implementing the baby friendly
hospital initiative: the role of finger feeding. Breastfeed Review, 11,
5–10.
Ortenstrand, A., Waldenström, U. & Winbladh, B. (1999) Early
discharge of preterm infants needing limited special care, followed
by domiciliary nursing care. Acta Paediatrica, 88, 1024–1030.
Ortenstrand, A., Winbladh, B., Nordstrom, G. & Waldenstrom, U.
(2001) Early discharge of preterm infants followed by domiciliary
nursing care: parents’ anxiety, assessment of infant health and
breastfeeding. Acta Paediatrica, 90, 1190–1195.
Paul, V. K., Singh, M., Deorari, A. K., Pacheco, J. & Taneja, U. (1996)
Manual and pump methods of expression of breast milk. Indian
Journal of Pediatrics, 63, 87–92.
Pereira, G. R., Schwartz, D., Gould, P. & Grim, N. (1984)
Breastfeeding in neonatal intensive care: beneficial effects of
maternal counseling. Perinatology Neonatology, 8, 35–42.
Phillips, S. J. & Tooley, G. A. (2005) Improving child and family
outcomes following complicated births requiring admission to
neonatal intensive care units. Sexual and Relationship Therapy, 20,
431–442.
Pineda, R. G. (2006) Breastfeeding Practices in the Neonatal Intensive
Care Unit Before and After an Intervention Plan. University of
Florida, Gainesville, FL, USA.
Pinelli, J., Atkinson, S. A. & Saigal, S. (2001) Randomized trial of
breastfeeding support in very low-birth-weight infants. Archives of
Pediatrics & Adolescent Medicine, 155, 548–553.
Redshaw, M. & Hamilton, K. (2006) Networks, Admissions and
Transfers: The Perspectives of Networks, Neonatal Units and Parents.
National Perinatal Epidemiology Unit, Oxford, UK.
Roberts, K. L., Paynter, C. & Mcewan, B. (2000) A comparison of
kangaroo mother care and conventional cuddling care. Neonatal
Network, 19, 31–35.
Rocha, N. M. N., Martinez, F. E. & Jorge, S. M. (2002) Cup or bottle
for preterm infants: effects on oxygen saturation, weight gain, and
breastfeeding. Journal of Human Lactation, 18, 132–138.
Rojas, M. A., Kaplan, M., Quevedo, M., Sherwonit, E., Foster, L. B.,
Ehrenkranz, R. A. & Mayes, L. (2003) Somatic growth of preterm
infants during skin-to-skin care versus traditional holding: a
randomized, controlled trial. Journal of Developmental and
Behavioral Pediatrics, 24, 163–168.
Schanler, R. J. (2001) The use of human milk for premature infants.
The Pediatric Clinics of North America, 48, 207–219.
Senn, T. E. (2004) Development and evaluation of the lactation
education program to increase breastfeeding rates in hospitalized,
preterm infants. A dissertation submitted in partial fulfillment of
the requirements for the PhD Degree. Dept of Psychology,
Graduate School, Southern Illinois University, Southern Illinois U
Carbondale, US.
Shah, P. S., Aliwalas, L. L. & Shah, V. (2006) Breastfeeding or breast
milk for procedural pain in neonates (Cochrane Review). The
Cochrane Database of Systematic Reviews 3, CD004950.
DOI:10.1002/14651858.CD004950.
da Silva, O. P., Knoppert, D. C., Angelini, M. M. & Forret, P. A. (2001)
Effect of domperidone on milk production in mothers
of premature newborns: a randomized, double-blind,
placebo-controlled trial. Canadian Medical Association Journal,
164, 17–21.
Sloan, N. L., Rojas, E. P., Stern, C., Camacho, L. W. L., Maternidad
Isidro Ayora Study Team (1994) Kangaroo mother method:
randomised controlled trial of an alternative method of care for
stabilised low-birthweight infants. Lancet, 344, 782–785.
Slusher, T., Slusher, I. L., Biomdo, M., Bode-Thomas, F., Curtis, B. A.
& Meier, P. (2007) Electric breast pump use increases maternal
milk volume in African nurseries. Journal of Tropical Pediatrics, 53,
125–130.
Smith, M. M., Durkin, M., Hinton, V. J., Bellinger, D. & Kuhn, L.
(2003) Influence of breastfeeding on cognitive outcomes at age 6–8
years: follow-up of very low birth weight infants. American Journal
of Epidemiology, 158, 1075–1082.
The Cochrane Collaboration (2008) Cochrane Handbook for
Systematic Reviews of Interventions, Version 5.0.0 (updated February
2008) (eds J. P. T. Higgins, S. Green). The Cochrane Collaboration.
Available at: http://www.cochranehandbook.org
Vohr, B. R., Poindexter, B. B., Dusick, A. M., Mckinley, L. T., Wright,
L. L., Langer, J. C. & Poole, W. K. for the NICHD Neonatal
Research Network (2006) Beneficial effects of breast milk in the
neonatal intensive care unit on the developmental outcome of
extremely low birth weight infants at 18 months of age. Pediatrics,
118, e115–e123.
Vohr, B. R., Poindexter, N. N., Dusick, A. M., Mckinley, L. T.,
Higgins, R. D., Langer, J. C. & Poole, K. (2007) Persistent beneficial
effects of breast milk ingested in the neonatal intensive care unit
on outcomes of extremely low birth weight infants at 30 months of
age. Pediatrics, 120, e953–e959.
Wahlberg, V., Affonso, D. D. & Persson, B. (1992) A retrospective,
comparative study using the kangaroo method as a complement to
the standard incubator care. European Journal of Public Health, 2,
34–37.
Whitelaw, A., Heisterkamp, G., Sleath, K., Acolet, D. & Richards, M.
(1988) Skin to skin contact for very low birthweight infants and
their mothers. Archives of Disease in Childhood, 63, 1377.
Wilhelm, P. A. (2005) The Effect of Early Kangaroo Care on Breast
Skin Temperature, Distress, and Breastmilk Production in Mothers of
Premature Infants. University of Nebraska Medical Center, Omaha,
NE, USA.
World Health Organsiation (1989) Protecting, Promoting and
Supporting Breastfeeding: The Special Role of Maternity Services. A
Joint WHO/UNICEF Statement. WHO, Geneva, Switzerland.
178 M. J. Renfrew et al.
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