Newborn & Infant Nursing Reviews 16 (2016) 78–91

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Newborn & Infant Nursing Reviews

journal homepage: www.nainr.com

A Critical Review of Interventions Supporting Transition from Gavage to

Direct Breastfeeding in Hospitalized Preterm Infants
Mona Ziadi, RN, MSc a, Marjolaine Héon, RN, PhD a,b,c,⁎, Marilyn Aita, RN, PhD a,b,d
a
Faculty of Nursing, Université de Montréal, 6128 Succ. Centre-ville, Montreal, QC, Canada, H3C 3J7
b
Quebec Nursing Intervention Research Network (RRISIQ), Montreal, QC, Canada
c
School of Nursing, Université de Sherbrooke, Sherbrooke, QC, Canada.
d
Research Center, CHU Sainte-Justine, Montreal, QC, Canada.

a r t i c l e i n f o a b s t r a c t

Keywords: Even though direct breastfeeding holds many benefits for preterm infants, the transition from gavage to direct
Interventions breastfeeding remains suboptimal in this population. Failing this transition can contribute to an early cessation
Transition of direct breastfeeding and jeopardize the preterm infants’ growth and development. Preterm infants could ben-
Gavage efit from interventions that promote the transition to direct breastfeeding and thus facilitate this challenging
Direct breastfeeding step. This review identifies and analyzes interventions classified in four categories: non-nutritive sucking
Preterm infants
(NNS) and oral stimulation, promotion of direct breastfeeding experience and avoidance of bottles, cue-based
feeding approach, and exposure to human milk odor. All of these interventions improved the preterm infants’
sucking competency, decreased their hospitalization length or increased the breastfeeding rates at discharge.
NNS and oral stimulation, and promotion of direct breastfeeding experience and avoidance of bottles are the in-
terventions with the highest evidence level, with the most potential for NICU implementation.
© 2016 Elsevier Inc. All rights reserved.

Human milk is the most appropriate nutriment for preterm infants,1
as it is beneficial for their nutritional and immunological status, gastro-
intestinal health, and neurological development.2 Direct breastfeeding
also holds many benefits for preterm infants, such as an improved oxy-
genation and temperature regulation during feedings, as well as a better
oral development reflected in an optimal mandibular development, a
strengthening of the jaws muscles, and a greater breathing efficiency.3
Furthermore, engaging in close physical contact with their mother at
each feeding contributes to mother–infant bonding.4
However, the transition from gavage to direct breastfeeding is
a challenging step for preterm infants 3,5,6 while failing the transition
to oral nutrition, in general, may jeopardize their growth and
development.7,8 In the short term, it may affect the preterm infants’ de-
velopmental coordination of sucking, swallowing, and breathing, and it
may prompt the occurrence of oral aversion. 9 These consequences
could delay the attainment of full oral feeding,10 and ultimately hospital
discharge. 2,11–13 In the longer term, it can have consequences such as
dysphagia,14 altered oral sensitivity,15 as well as impaired growth and
neurological development.16
Furthermore, inefficient management of the transition from gavage to
direct breastfeeding by healthcare professionals can also threaten the inci-
dence and duration of direct breastfeeding in preterm infants.2,3 The cur-
rent management of this transition, and to oral feeding in general, is
inconsistent from one NICU to another.7 While the practice of some
⁎ Corresponding author.
E-mail addresses: mona.ziadi@umontreal.ca (M. Ziadi), marjolaine.heon@umontreal.ca
(M. Héon), marilyn.aita@umontreal.ca (M. Aita).
units is to start preterm oral feeding with a bottle and then switch to direct
breastfeeding once these oral feedings are established, others allow direct
breastfeeding initially and supplement the preterm infants with a bottle
when the mother is not present at the bedside.12 As a result, at discharge,
less than half of the preterm infants are fed exclusively human milk,17 and
an even a lower percentage is only fed directly at the breast.18,19
Over the last decade, a growing body of literature has reported dif-
ferent interventions that may greatly facilitate the transition of preterm
infants from gavage to oral feeding in general, 20 and to direct
breastfeeding specifically. 12 More and more, an evidence-based ap-
proach is used in the NICUs to optimize preterm infants’ health and de-
velopmental outcomes.21 Therefore, it is imperative to review effective
interventions in order to support preterm infants throughout their tran-
sition from gavage to direct breastfeeding, according to the current best
evidence. The aim of this manuscript is to offer a critical review by iden-
tifying and analyzing these interventions and their effects on the transi-
tion to direct breastfeeding in preterm infants.
Methods
The search for studies was performed in the scientific databases of
CINAHL, PubMed, Cochrane Review, Embase and Medline. The follow-
ing keywords were used in combination: intervention; transition OR
progression; gavage OR “enteral feeding”; breastfeeding; “premature
infant” OR “preterm infant”; oral feeding. The search was restricted to
original research articles or systematic reviews in English and French
and limited to literature published between 2004 and 2015. A first

http://dx.doi.org/10.1053/j.nainr.2016.03.013
1527-3369/© 2016 Elsevier Inc. All rights reserved.
 M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91
search resulted in 533 articles. Each title and abstract were reviewed to
select research articles that addressed single or combined interventions
aiming to promote the transition of preterm infants (born before
37 weeks post-menstrual age [PMA]), from gavage to direct
breastfeeding. Also, the interventions had to be introduced during hos-
pitalization in the neonatal intensive care unit [NICU], either before or
during the transition to direct breastfeeding. Thoyre’s definition 22 of
the term transition period was considered in this review as being the pe-
riod of time that extends from the day a first oral feed is introduced until
the day exclusive oral feeds are attained.
One main issue encountered in this review, which may in part be
due to the difficulty to grasp the complexity of breastfeeding in the
NICU, was the lack of clarity regarding the method of feeding used in
the studies. This variability in the terminology used in the literature
caused difficulties in identifying studies that were relevant to the tran-
sition to direct breastfeeding specifically. Often, the researchers use
terms such as oral feeding or nipple feeding as general terms that include
breastfeeding as well as bottle-feeding. Also, other terms, such as direct
breast-feeding, direct sucking at the breast, or human milk feeding, were
used. Thus, the term breastfeeding could represent feeding the preterm
infant human milk either with a bottle or directly at the breast. The
search was conducted by the main author and the results were submit-
ted to the co-authors for validation. An agreement between the authors
was reached at each step of the review. To be consistent with the search
criteria and ensure uniformity in this literature review, studies in which
the feeding method was not specified were not selected. Thus, a number
of 411 articles, including 47 duplicates, were excluded because they did
not meet the selection criteria. Seven articles identified through the ref-
erence lists searching were added to the review. A total of 129 articles
were fully reviewed to assess their relevance. After this review, 115 ar-
ticles were excluded because they were not aiming to specifically facil-
itate the transition to direct breastfeeding. Finally, 14 articles complying
with the search criteria were included in this review and analyzed
(Fig. 1). For this critical review, the analysis mainly focused on depen-
dent variables that implied a transition to partial or exclusive direct
breastfeeding in preterm infants. These variables are inspired by
IDENTIFIED ARTICLES
533 articles identified + 7 articles identified
through database searching through reference searching
SCREENED ARTICLES
540 articles screened by 411 articles excluded
title and abstract (including 47 duplicates)
ELIGIBLE ARTICLES
129 articles found eligible 115 articles excluded
INCLUDED ARTICLES
14 articles included in the critical review
Fig. 1. Selection of articles.
79
Greene, O’Donnell, and Walshe’s 23 primary outcome measures for oral
interventions (i.e. time taken to achieve exclusive oral feeding, total
hospital stay, and maturation in sucking strength) and adapted to a
breastfeeding context. Partial and exclusive breastfeeding rates at dis-
charge were also considered.
Results
Several interventions promoting transition in preterm infants to di-
rect breastfeeding were identified in the scientific literature and were
classified in four categories: non-nutritive sucking (NNS) and oral
stimulation, 24–27 promotion of direct breastfeeding and avoidance of
bottles,28–32 cue-based feeding approach,33–35 and exposure to human
milk odor. 36,37 The results of each study, grouped by intervention, are
summarized in Table 1. The level of evidence, based on Melnyk and
Fineout-Overholt’s classification 38 (Fig. 2) has also been specified for
each study in Table 1.
NNS and Oral Stimulation
NNS is an intervention that promotes sucking in preterm infants,
through the use of a pacifier, 39 a gloved finger or an emptied breast.25
Oral stimulation, consisting of peri-oral and intra-oral stimulation inter-
ventions using a gloved finger or a pacifier, can have beneficial effects on
oral feeding performance when applied before or during oral feedings in
medically stable preterm infants. 40 It is noteworthy that NNS is often
used as an intervention in oral stimulation programs, such as the one
developed by Fucile, Gisel, and McFarland’s 41 consisting of 15 min of
multiple peri-oral activities, such as the stimulation of the upper lip
and the internal cheek, aiming to improve muscle intractability,
strength and orientation reflexes.
Two studies with the purpose of evaluating the effectiveness of
NNS 25,27 and three studies evaluating the combination of NNS and
oral stimulation 24–26 on the transition to direct breastfeeding were
identified through this review. The identified studies had evidence
levels from II (randomized controlled trials) to VI (single descriptive
study) to, according to Melnyk and Finout-Overholt’s 38 classification
(Fig. 2).
One quasi-experimental study27 and one descriptive study 25 exam-
ined NNS as a single intervention. Their sample sizes varied from 35 to
90 preterm infants aged between 31 and 32.58 weeks PMA. NNS was
administered via a pacifier by a researcher,27 a gloved finger by speech
therapists or the mothers’ empty breast.25 In Yildiz and Arikan’s study, 27
NNS was administered three times a day during gavage feeds, from the
initiation of oral feeds until the infant proceeded to full-oral feeding. In
this study, NNS decreased the time needed to attain direct breastfeeding
(mean in the pacifier group = 7.7 days vs. 11.7 days in the control
group) and the length of hospital stay (mean in the pacifier group =
15.4 days, vs. 21.7 days in the control group). Also, NNS with a pacifier
helped preterm infants to achieve higher scores on the LATCH
breastfeeding Charting System (Table 1). In the study of Medeiros and
colleagues,25 NNS was needed for an average of 4.54 days to achieve ex-
clusive direct breastfeeding but the frequency of the intervention was
not specified.
Lastly, two RCTs assessed the effectiveness of a combination of NNS
with oral stimulation on the transition to full or partial direct
breastfeeding.24,26 Sample sizes varied from 86 to 98 preterm infants,
with gestational age at birth ranging between 26 and 33 weeks PMA
(Table 1). In both studies, the oral stimulation programof Fucile and
colleagues 41 was used. The stimulation was performed once a day for
at least 10 days. 24,26 Besides, the stimulation was administered either
by speech therapists 25 or by trained nurses and members of the medical
staff.24 The studies resulted in higher rates of exclusive breastfeeding at
discharge24,26 and in a decrease of the length of hospitalization.26 In the
study of Bache and colleagues 24 the combination of NNS and oral stim-
ulation did not lead to the same rapid transition to direct breastfeeding
 80
Table 1
Interventions promoting transition from gavage to direct breastfeeding.

Author(s) Country Study Design Level of evidence Participants Methods Outcomes relevant to transition from Main Outcomes
gavage to direct breastfeeding

Intervention: Non-nutritive sucking/Oral stimulation

Pimenta Brazil Randomized clinical II 98 preterm infants were
et al.26 trial randomized (96 stayed in the
study until they reached 6 months
of age): 1) PMA between
26 weeks and 32 weeks and
6 days,
2) adequate or
small for gestational age,
3) birth weight b 1500 g
The goal of the study was to
determine the influence of NNS
and oral stimulation programs on
breastfeeding rates at discharge,
at 3 and 6 months of corrected
age in preterm infants with very
low birth weight.
Experimental group (n = 47)
received sensory–motor–oral
stimulation and NNS (using a
gloved finger for intraoral and
perioral stimulation and a
pacifier) once a day for 15 min for
- Length of stay. • The main outcome was length of
- Frequency of breastfeeding at stay. The experimental group had a
discharge. significant shorter length of stay
[41.81 days] than the control group
[52.37 days].
• Breastfeeding rate at discharge was
a secondary outcome.
• The rates of breastfeeding at dis-
charge, at 3 months, and 6 months
were significantly higher in the ex-
perimental group (76%; 47%; 27%)
than the control group (47%; 18%;
10%).

M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91

a period of at least 10 days.
The control group (n = 49)
received a sham stimulation
program that consisted of
standing around the incubator for
a period of time similar to that
spent for the experimental group,
adequately positioning the infant,
providing the diet via gavage, not
performing the stimulus and not
using a pacifier during gavage.
Medeiros Brazil Experimental study IV 35 preterm infants, with mean The sample was divided into two
et al.25 PMA at birth of 32.5 weeks. groups. Group 1 (n = 22 preterm
infants) with no medical
complications, and group 2
(n = 13 preterm infants) with
important medical complications.
NNS training (speech-language
pathology intervention) was
administered by either “gloved
finger” or “empty breast” (in the
presence of the mother).
Yildiz and Turkey Quasi-experimental III 90 premature infants, with mean The aim of the research was to
Arikan27 and prospective gestational age 31 weeks PMA. study the effect of pacifiers and
- Corrected gestational age when
oral feeding was started.
- Number of days the infant was
stimulated through NNS.
- Corrected gestational age when
oral feeding was achieved.
- LATCH Breastfeeding Charting
System.
• No statistical differences were
noted between the experimental
and control groups in terms of:
birth weight, gestational age, days
of life upon reaching clinical stabil-
ity, gestational age upon reaching
clinical stability and maternal vari-
ables that could influence
breastfeeding rates.
• Both groups showed no differences
for the studied parameters (gesta-
tional age at birth, birth weight,
weight and corrected gestational
age during speech-language pa-
thology evaluation, corrected ges-
tational age when started oral
feeding, number of days stimulated
through the NNS technique,
corrected gestational age when oral
feeding started and when they
were discharged from speech-lan-
guage pathology intervention, and
total number of days under speech-
language pathology intervention).
The preterm infants remained in
the speech-language pathology in-
tervention from gavage to
breastfeeding for an average of
12.31 days. The NNS training lasted
an average of 4.54 days. Exclusive
oral feeding was achieved at an av-
erage of 36.95 weeks PMA.
• Mean weight during the speech-
language pathology evaluation was
higher in G2 = 1850.77 g
(G1 = 1712.05 g).
• No differences between the inter-
vention and control groups in
 study listening to lullabies on the
transition period to full oral
feeding, sucking success and vital
signs of preterm infants. Data
were collected three times a day
The control group (n = 30)
received no intervention.
In the pacifier group (n = 30), the
implementation of the pacifier
was initiated at the beginning of
the gavage feed until the feeding
was completed. This
implementation continued three
times a day, until the preterm
infant reached total oral feeding.
In the lullaby group (n = 30), a
lullaby was started at the
beginning of the gavage feed and
terminated at the end of the
feeding. This implementation was
carried out until full oral feeding
was reached.
The LATCH Breastfeeding Charting
System form was filled twice for
each group (once right after the
preterm infants reached full oral
feeding and the second one 24 h
later): L (latch on breast), A
(audible swallowing), T (type of
nipple), C (comfort breast/nipple),
H (hold/help).
Peak heart rate, respiration rate,
and oxygen saturation were
collected before, during, and after
feeding, and were monitored until
the preterm infant proceeded to
oral feeding. Daily weights were
recorded and preterm infants
were weighed before the first
meal until they were discharged
from the hospital.
Bache Luxembourg Prospective II 86 preterm infants born between The study aimed to determine the
et al.24 randomized 26 and 33 weeks PMA. effectiveness of NNS.
controlled clinical Preterm infants in the
trial intervention group (n = 40)
received an oral stimulation
program (stimulation of the oral
structures for 15 min, 15 to
30 min before tube feeding once
daily, for at least 10 days before
the introduction of oral feeds). In
the control group (n = 46),
preterm infants received neither
oral stimulation nor a pacifier
- Transition period to oral feedings.
- Duration of hospital stay.
- Weight at discharge.
- PMA at introduction to oral
feeding.
- Days of life at introduction to oral
feeding.
- Weight at full oral feeding.
- PMA at full oral feeding.
- Days of life at full oral feeding.
- Duration between full gavage
diet and full oral feeding.
- Duration between introduction
to oral feeding and 1 oral feeding.
terms of gender, gestational age,
birth weight, height, head circum-
ference measurement and Apgar
scores at 1–5 min.
• The group who proceeded to the
oral feeding in the shortest period
was the pacifier group (184.2 h vs.
280.3 for the control group and
243.03 for the lullaby group). Also,
the highest sucking success was
achieved by infants in the pacifier
group (8.57/10 vs. 7.27/10 in the
control group and 7.95/10 in the
lullaby group).
• No differences were found in terms
of peak heart rate between the
groups before, during, and after the
first gavage feeding. During the last
feeding, no differences were found
between the groups before and
M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91
after the feeding. There was how-
ever a difference during the feeding
(mean peak heart rate in control
group = 135.67, pacifier
group = 129.42, and lullaby
group = 130.08).
• No statistically significant differ-
ences were noted in the averages of
discharge weights between the in-
terventions and control groups.
No statistically significant differ-
ences between groups in terms of
the average respiration rate and
oxygen saturation. However, the
preterm infants’ saturation during
and after feeding of the last gavage
feeding meal significantly in-
creased in both experimental
groups:- During the last feeding
(mean saturation):
pacifier = 97.04, lullaby = 96.61,
in comparison with control
group = 95.76- After the last feed-
ing: pacifier = 96.50,
lullaby = 96.00, in comparison
with control group = 95.52.
• Breastfeeding rates (partial and/or
exclusive direct breastfeeding at
discharge) were higher in the in-
tervention group (70% vs. 45.6% in
the control group). Rate of exclu-
sive direct breastfeeding was
higher in the intervention group
(25% vs. 15% in the control group).
• No statistical differences in the
length of the transition period or
hospital stay.
• No statistical differences were
noted in terms of gestational age,
81
(continued on next page)
 82
Table 1 (continued)

Author(s) Country Study Design Level of evidence Participants Methods Outcomes relevant to transition from Main Outcomes
gavage to direct breastfeeding

before or during gavage feeding.
Oral feeds were started at
34 weeks PMA for both the
intervention and the control
group.
- Duration between introduction
to oral feeding and 3 oral
feedings.
- Duration between introduction
to oral feeding and full oral
feeding.
- Length of hospital stay.
- Partial and/or full breastfeeding
at discharge.
days of life, weight at the introduc-
tion of oral feeding and at full oral
feeding, duration between full ga-
vage diet and full oral feeding, du-
ration between introduction of oral
feeding and full oral feeding.
• In the intervention group, 52.5% of
the preterm infants needed CPAP
support between 32 and 34 weeks
(in comparison with 52.5% in the
control group). 35% of the preterm
infants in the intervention group
needed high-flow oxygen during
the same period (21.7% in the con-
trol group). For these infants, the

M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91

pre-feeding stimulation was per-
formed during a 15-min period of
time when the CPAP or high-flow
was interrupted, without any re-
spiratory supported when
tolerated.

Intervention: Avoidance of bottles and promotion of at-breast experience

Collins Australia (1), Cochrane I Five trials of a total of 543 preterm Cochrane systematic review - Not breastfeeding or only partial • Cup feeding significantly decreased
et al.28 United Systematic Review infants were included in the including four trials that used a breastfeeding compared with “no breastfeeding or only partial
Kingdom (2), review. cup feeding strategy and one trial fully breastfeeding on discharge breast feeding” on discharge home
Brazil (1), that used a tube feeding strategy home and at three and six (n = 455). The same decrease in
United States when supplements to breast feeds months post-discharge. this outcome was noted in the 3
of America (1) were needed. Instead of bottles, - Not breastfeeding compared with studies (n = 371) comparing
alternative feeding devices were any breastfeeding on discharge breast feeds supplemented with
used for supplementing at-breast home and at three and six cup vs. breast feeds supplemented
feeds: gavage tube, cup, or other. months post-discharge. with bottle.
Control intervention consisted in - Time (days) to reach full sucking • A significant decrease in the out-
supplementing at-breast feeds feeds. come “no breastfeeding or only
with bottles during the transition - Average daily weight gain (g/day partial breastfeeding at three
to at-breast feeds. or g/kg/day) to discharge home. months post discharge” in the
- Length of hospital stay (days). breastfeeding plus avoidance of
- Duration (minutes) of supple- bottles group.
mentary or complementary feed. • A significant decrease in the out-
- Volume of supplementary feed come “no breastfeeding or only
taken compared to volume pre- partial breastfeeding at six months
scribed (milliliters). of age” in the avoidance of bottles
group (breastfed infants supple-
mented by tube).
• A significant decrease in the no
breastfeeding at all at discharge
home”, at three months and six
months post-discharge outcomes.
• Three studies (n = 416) showed a
significant increase in the “days to
reach full sucking feeds” outcome
in the breastfeeding preterm in-
fants supplemented by cup.
• No statistically significant differ-
ences in terms of weight gain.
 • Duration of supplementary feed
was measured in one trial and no
significant difference was found
between the breastfeeding preterm
infants supplemented with cups
and the breastfeeding plus bottles
group.
• Fewer apneic and bradycardic inci-
dents reported in the breastfeeding
plus avoidance of bottles group
compared with bottle. The
breastfeeding plus bottle group had
significantly more episodes that re-
quired stimulation. No significant
statistical differences in the mean
of oxygen saturation during feeds
or desaturation episodes (less than
90%) during feeds, as reported by
one trial.
• No milk aspiration was noted in the

M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91

two trials reporting this outcome.
• Cup feeding significantly increased
length of hospital stay by 10 days.
The one trial of a tube alone ap-
proach significantly reduced “no
breastfeeding or only partial
breastfeeding” and “no
breastfeeding at all” at all time pe-
riods but the results need to be
interpreted with caution due to the
high risk of bias.
• A high degree of noncompliance in
the largest study of cup feeding un-
derlies dissatisfaction with this
method by staff and/or parents.
Flint et al.29 Australia, UK, Cochrane I Four trials were included in this Randomization to supplemental Primary outcome measures: • No significant reduction in the pro-
Brazil. Systematic Review review for a total of 472 preterm feeds to cup or bottle; portion of infants not breastfeeding
infants from 29 to 35 weeks of at discharge, 3 months and
- Not breastfeeding at discharge,
gestation 6 months;
3 months and 6 months;
• A significant increase in the pro-
- Not fully breastfeeding at hospi-
portion of infants exclusively
tal discharge, 3 months and
breastfeeding at hospital discharge
6 months.
for those in the cup feeding group;
Secondary outcome measures:
• No significant reduction in the pro-
portion of infants not fully
- Average time per feed; breastfeeding at 3 months and
- Number of reported physiological 6 months;
instability events; • No significant difference in the av-
- Length of hospital stay; erage time per feed;
- Weight gain. • No significant difference between
mean of lowest oxygen saturation;
• A significant increase in length of
hospital stay (10 days) for infants
in the cup feeding group;
• No significant difference for infants’
weight gain.
de Aquino Brazil Descriptive study VI 432 preterm infants with Relactation group (n = 274): A - PMA at beginning of transition. • 90.3% of the infants were
and using retrospective PMA b 37 weeks. number 4 gastric tube is fixed - PMA at discharge. discharged on exclusive
Osorio30 data from medical alongside the mother’s nipple, and - Type of feeding. breastfeeding, 6% on breastfeeding
records the other end is attached to a 20- - Transition time.

83
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Table 1 (continued)
Author(s) Country Study Design Level of evidence Participants Methods
mL syringe containing pasteurized
banked human milk or formula.
When put to breastfeed, the infant
stimulates the nipple, and hence
milk production, while feeding by
tube.
Translactation group (n = 111):
same as relactation intervention
except that milk given is milk
previously expressed from the
mother.
Breast–OG tube group (n = 47):
the infants would breastfeed then
receive expressed human milk by
OG tube.
Pineda31 United States Restrospective IV 66 mother–infant dyads. The chart review was performed
of America study Gestational age at birth was 24 to to gather information about
35 weeks PMA. initiation of human milk feedings,
the number of times the mother
put the infant to breast, the
gestational age of the first direct
breast-feeding, whether the first
oral feeding was at the breast, the
duration of human milk feedings
and whether human milk feedings
continued until NICU discharge.
Yilmaz Turkey Randomized II 522 preterm infants aged between The preterm infants were
et al.32 Controlled Study 32 to 35 weeks PMA. randomly assigned to two groups.
The cup-fed group (254) and
bottle-fed group (268).
Outcomes relevant to transition from
gavage to direct breastfeeding
- Complications during transition.
- Initiation of human milk
feedings.
- Frequency of at-breast feeds dur-
ing hospitalization.
- PMA of the first direct breast-
feeding.
- Duration of human milk feedings.
- Exclusive breastfeeding at
discharge.
- Length of hospital stay.
- Feeding problems.
- Weight gain in the hospital.
84
Main Outcomes
plus complement, and 3.7% on for-
mula only.
• Median transition time in the
relactation group = 10 days,
translactation group = 9 days,
breast–orogastric feeding
group = 5 days.
• Median daily weight gain in the
relactation group = 18 g/d,
translactation group = 15 g/d,
breast–orogastric group = 16 g/d.
• Median weight gain during exclu-
sive breastfeeding in the relactation
group = 45 g, translactation
group = 55 g, breast–orogastric
M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91
feeding group = 50 g.
• Positive associations were found
between human milk feedings at
discharge and mothers putting
their infants directly to breast in
the NICU (P = 0.0005) (100% had
put their infants directly to breast
at least once).
• Length of stay of the sample ranged
10 to 108 days (mean
66.4 ± 27.4 days).
• Mean gestational age for the first
breast-feeding was
33.1 ± 1.59 weeks.
• Duration of human milk feeds
ranged from 12 to 108 days. Of
those who initiated human milk
feeds, 32.8% continued to provide
some human milk at discharge and
only 22.4% provided exclusive
human milk at discharge.
• Factors associated with the dura-
tion of human milk feedings in-
cluded: the number of times the
infant was put directly to breast, if
the infant was ever directly breast-
fed, the first oral sucking feeding
being at the breast and the gesta-
tional age at the first direct breast-
feed.
• Factors associated with the number
of times directly breast-fed in the
NICU included: if the first oral
sucking feeding was at the breast
and the gestational age of the first
direct breast-feeding.
• Preterm infants in the cup-fed
group were more likely to be ex-
clusively breastfed at discharge
(72%) vs. 46% in the bottle-fed
group. They were also more likely
 to be breastfeeding at 3 months
after discharge and 6 months after
discharge.
• No significant differences in the
length of hospital stay, the time
spent feeding, feeding problems or
weight gain in the hospital.

Intervention: Cue-based feeding approach

Kirk et al.33 United States Prospective study III 53 preterm infants (born In the study group (n = 29), oral - PMA at full oral feeding. • Study group achieved earlier at-
of America vs. historic cohort b37 weeks PMA) selected on a feedings were managed by - Length of hospital stay. tainment of full oral feeds. No dif-
controls computer-randomized list. neonatal nurses, relying on infant - Rate of weight gain. ferences between both groups in
behavioral readiness signs to length of stay.
initiate and advance oral feedings. • An equal number of infants re-
In the control group (n = 24), ceived a combination of both bottle
oral feedings were managed by and breastfeeding (n = 19 study;
physicians. n = 19 control).
• PMA at full oral feeding for study
group = 252 days (36 weeks), for
the control group = 258 days (36

M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91

6/7 weeks).
• Rate of weight gain during feeding
phase: study
group = 14.5 ± 11.4 g/kg/day,
control
group = 9.4 ± 13.0 g/kg/day,
Nyqvist34 Sweden Prospective VI 15 infants, born at PMA of 26 to Mothers used the Preterm Infant - Breastfeeding progress measured • Breastfeeding was initiated at
descriptive design 31 weeks Breastfeeding Behavior Scale through milestones: initiation of 29 weeks.
(PIBBS) for daily assessment of oral/breast feeding, initiation of • Weight gain when fully breastfed
their infant’s oral motor behavior. cup feeding, prescription of daily adequate.
Semi-demand feeding with milk volume, initiation of (semi) • The number of consecutive sucks
prescription was introduced demand feeding, attainment of was between 5 and 24 sucks
during the transition from full oral/breast feeding, early dis- (median = 17).
scheduled to demand feeding. charge, and discharge from • Full breastfeeding attained at a me-
hospital. dian of 35 weeks (between 32 and
- PIBBS scores. 38 weeks). The lowest PMA at
which exclusive breastfeeding was
attained was 32 weeks.
• 12 infants were supplemented by
cup starting from 31 weeks and 3
infants started bottle-feeding at
35.9 weeks.
Gelfer United States Cohort study IV 124 preterm infants An algorithm detailing an infant- - Time to reach ad libitum feeds • Infants in the post-intervention
et al.35 (aged ≥ 30 weeks PMA): 64 driven practice, a chart audit tool, - PMA at initiation of oral feeds phase reached ad libitum feeds ear-
infants in the pre-intervention educational programs for nurses - Length of hospital stay lier than those in the pre-interven-
phase and 60 infants in the post- and parents, as well as practice tion group (35.0 ± 1.1 vs.
intervention phase. guidelines were developed and 35.6 ± 1.1 weeks PMA; 95% CI
used with the intervention group 0.1–0.9, p = 0.008).
(n = 60). • The infant-driven practice inter-
vention did not influence PMAs at
initiation of oral feeds (33.6 ± 0.9
vs. 33.8 ± 0.6 weeks PMA, 95% CI
−0.1 to 0.4, p = 0.33) or at dis-
charge (36.3 ± 1.2 vs.
36.6 ± 1.1 weeks PMA, 95% CI
−0.1 to 0.7, p = 0.15).
• The infant-driven practice did not
compromise weight gain.

(continued on next page)

85

Table 1 (continued)
Author(s) Country Study Design Level of evidence Participants Methods
Intervention: Exposure to human milk odor
Raimbault France Randomized II 13 preterm infants, born between At 35 weeks PMA, the infants
et al.36 controlled trial 29 and 34 weeks PMA. were exposed to a stimulus
(either water: n = 6, or human
milk: n = 7) during a 120-s
session once a day, for five
consecutive days. The infant was
in the mother’s arm while being
exposed to a cotton-tipped
applicator moistened with water
or human milk.
The first breastfeeding experience
occurred one day before starting
the exposure to the stimulus.
Yildiz Turkey Quasi-experimental III 80 preterm infants, with mean The study group (n = 40) was
et al.37 study PMA of 31 weeks. stimulated by placement of a
sterile pad soaked in human milk
approximately 2 cm from the
infant’s nose. When the feeding
was completed, the human milk
odor stimulus was removed.
The control group (n = 40) was
not subjected to the simulation
and was gavage fed without being
taken out of the incubator.
Outcomes relevant to transition from
gavage to direct breastfeeding
- Nipple grasping latency (in
seconds).
- Longest sucking bout (seconds).
- Number of long sucking bouts.
- Quantity of milk consumed (in
grams).
- Duration of breastfeeding trial
(seconds).
- Weight at transition to total oral
feeding.
- Weight at discharge.
- Weight gain throughout
hospitalization.
- Time for transition to oral
feeding.
- Duration of hospitalization.
86
Main Outcomes
• Earlier hospital discharge
(26.5 days in the post-intervention
group vs. 28.2 days in the pre-in-
tervention group) and feeding
therapist consults (8.3% in the post-
intervention group vs. 18.8% in the
pre-intervention group) differ-
ences between both groups were
not statistically significant.
• The infants that were exposed to
the human milk odor displayed
longer sucking bouts, a greater
number of long sucking bouts (N7
sucking movements), and con-
M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91
sumed significantly more milk than
babies in the water-control condi-
tion. The time spent in the hospital
was significantly less for the milk-
odor group (median = 43 days vs.
55.5 days for the control group).
• The quantity of milk consumed was
10 g in the milk group vs. 0 g in the
water group at 35 weeks. This out-
come increased to 55 g in the milk
group vs. 10 g in the water group at
the release from NICU.
• The duration of breastfeeding trials
increased at 35 weeks from 819 s
in the milk group (1154 s in the
water group) to 1232 s at the re-
lease from NICU (1176 s in the
water group).
• The preterm infants who were
stimulated by the odor of human
milk during gavage feeding
transitioned to direct breastfeeding
3 days earlier than control subjects.
The mean hospitalization time of
these infants was 4 days shorter
(mean = 18.30 days) than in the
control group
(mean = 22.85 days). No signifi-
cant differences were noted in
mean weight gains between both
groups (a mean of 334 g in the
control group vs. 427 g in the study
group).
 M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91
Fig. 2. Levels of evidence. Figure adapted from Fineout-Overholt E, Melnyk, BM. Levels of Evidence for Interventions (figure). Fineout-Overholt: Pittsford, NY. 2002.38
as in the study of Pimenta and colleagues. 26 Indeed, in the study of
Bache and colleagues,24 there were no differences in terms of the length
of the transition period or the length of hospital stay between the
intervention and control groups. However, breastfeeding rates were
significantly higher in the intervention group (70% versus 45.6%).
Thus, the combination of NNS and oral stimulation did have an impact
on direct breastfeeding.
Promotion of Direct Breastfeeding and Avoidance of Bottles
Direct breastfeeding consists of allowing the preterm infants to suck
directly from the breast while gavage feeding continues. 31 The first at-
tempts at direct breastfeeding usually consist of skin-to-skin contact
or nuzzling at the breast while gavage feeds continue. 32 When transi-
tion to short periods of suckling at the breast is achieved, partial gavage
tube supplementation can be established. 31 The promotion of direct
breastfeeding can be achieved either by avoiding the bottles for
supplementing the preterm infants by tube only 28,30 or with
cups28,29,32 or by exposing preterm infants directly to the breast.30,31
One Cochrane systematic review28 including five clinical trials, in ad-
dition to three subsequent studies, which had the purpose of evaluating
the effectiveness of promoting direct breastfeeding, was included in this
review. 30–32 Sample sizes range from 66 to 543 preterm infants; aged
from 32 to 37 weeks PMA. The level of evidence of the studies ranged
from I (systematic review) to VI (descriptive study) according to
Melnyk and Fineout-Overholt’s classification.38
In their Cochrane systematic review, Collins and colleagues28 evalu-
ated the effect of avoidance of bottles during the establishment of
breastfeeding, since, at times, preterm infants need to be supplemented
before attaining exclusive direct breastfeeding. The supplementation of
preterm infants (either with expressed human milk or formula) in the
studies was performed using two different strategies: by tube or by
cup. The authors concluded that using a tube only approach during
the establishment of direct breastfeeding needed further research as
only one highly biased trial studied the efficacy of this supplementation
method and its impact of breastfeeding. 28 It is still worth mentioning
that the study did show that preterm infants in the intervention group
87
who were supplemented by gavage tube were 4.5 times more likely to
be breastfed at discharge and 9.4 times more likely to be fully breastfed
at discharge than preterm infants in the control group who received
bottle supplements. 42 There were no differences, however, between
the groups in terms of length of hospitalization or infant weight at
discharge.42
For the supplementation by cup, Yilmaz and co-investigators con-
cluded, following their RCT, that preterm infants (n = 522) supple-
mented by this method were more likely to be exclusively breastfed
(76%) at discharge, in comparison with bottle-fed preterm infants
(46%).32 Two systematic reviews28,29 report that the use of the cup de-
creased the rates of no breastfeeding or only partial breastfeeding at
discharge 28 and increased the rate of exclusive breastfeeding at
discharge.29 However, results on length of hospital stay are contradicto-
ry as both Cochrane systematic reviews report an increased infants’
length of hospital stay by 10 days, 28,29 whereas Yilmaz and colleagues
report that the supplementation by cup did not increase the length of
hospital stay for preterm infants participating in their study. 32
In a retrospective study (n = 66) by Pineda,31 promoting the expe-
rience of preterm infants at the breast by direct breastfeeding had a pos-
itive impact on attaining human milk feedings sooner. The first feed at
the breast as early as 30 weeks PMA was positively associated with an
increase in frequency of breastfeeding and in duration of human milk
feedings in comparison with mothers who never put their infant to
the breast during the hospitalization. 31 Therefore, mothers (n = 31)
who initiated human milk feedings during their preterm infant’s hospi-
talization, but who did not put them to breast in the NICU, were no lon-
ger providing human milk for their infants at discharge. 31
Lastly, relactation, translactation and breast–orogastric tube feed-
ings, which are interventions that combine both promotion of direct
breastfeeding and avoidance of bottles with supplementation by tube,
have been studied by de Aquino and Osorio. 30 Relactation is defined
as feeding pasteurized human milk from another woman or formula
to a preterm infant. A gavage tube is fixed alongside the mother’s nipple,
and the other end is attached to a 20-mL pistonless syringe containing
pasteurized banked human milk or formula. The infant stimulates
human milk production by sucking at the nipple while they are fed by
88 M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91
tube. Translactation occurs when a preterm infant receives their
mother’s own milk via the same procedure as with relactation. During
breast–orogastric tube feedings, preterm infants are breastfed as long
as they want, then their feed is complemented by their mother’s
expressed human milk through an orogastric gavage tube. High per-
centages of exclusive breastfeeding at discharge are explained by the
fact that the three interventions are physiological and do not use arti-
facts such as pacifiers that could induce nipple confusion.30 Moreover,
during these interventions, the preterm infants have the opportunity
to benefit from the experience at the breast while being frequently ex-
posed to their mother’s breast.
In the descriptive study of de Aquino and Osorio, 30 these three inter-
ventions were introduced in a group of 432 preterm infants (274 in the
relactation group, 111 in the translactation group, and 47 in the breast–
orogastric tube feedings group), with PMA b37 weeks, in a Brazilian
hospital. The interventions were introduced, between 31 and
37 weeks PMA, when the preterm infants were clinically stable and
able to coordinate the sucking–swallowing–breathing process. At dis-
charge, the percentage of exclusive direct breastfeeding in the
relactation group was 85%, while in the translactation and breast–
orogastric tube feeding groups the rate was 100%. The median transition
time was 10 days in the translactation group, 9 days in the relactation
group and 5 days in the breast–orogastric tube feedings group. The re-
sults emphasize the efficiency of these interventions to accelerate the
transition to full oral feedings with translactation and breast–
orogastric tube feeding being the most significant ones for a successful
transition.
Cue-Based Feeding Approach
The cue-based feeding approach is based on the observation and
identification of the infant’s readiness signs to start oral feedings. 43 Pre-
term behavioral feeding signals are known to be subtle 44 as they include
sucking on an empty breast, sucking on fingers or hands or tongue, hand
to mouth, swipes at mouth, tonguing and rooting. 44–46 Three studies
(one level III prospective study, one level IV cohort study, and one
level VI descriptive study) using variations of the cue-based feeding ap-
proach were identified in this review. 33–35 These studies included sam-
ples ranging from 15 to 124 preterm infants, aged from 26 to 36 6/
7 weeks PMA.
The study by Kirk and colleagues 33 used a clinical pathway based on
the attainment of specific milestones using behavioral feeding signs as
cues to advance feeds. The progress assessment was based on the neo-
natal nurse’s assessment. 33 Mothers in Nyqvist’s study 34 used, for a
mean of 35.5 days, the Preterm Infant Breastfeeding Behaviour Scale
(PIBBS) daily to assess preterm infant’s cues. The instrument assessed
rooting, areolar grasp, latching on the breast, sucking, longest sucking
bursts, and swallowing. 34 An infant-driven feeding algorithm and an
infant-driven breastfeeding algorithm were introduced in the study of
Gelfer and colleagues. 35 Coupled with an educational program for par-
ents and nurses, as well as a chart audit tool, the intervention improved
the time needed to reach ad libitum feeds in the post-intervention
group. 35 For all three studies, the main result was that the cue-based
group achieved an earlier attainment of full oral feeds (including
breastfeeding and bottle feeding) which was 6 days earlier in the
study of Kirk and colleagues, 33 and as early as 32 weeks PMA in the
Nyqvist study.34 So, the cue-based feeding approach helps preterm in-
fants to achieve a faster transition to full oral feeds.
Exposure to Human Milk Odor
It is a known fact that human newborn infants show a spontaneous
attraction to human milk. 47 Even if preterm infants, who might be hos-
pitalized for a long period of time, have very limited chemosensory ex-
perience of their mothers, 37 they are nevertheless able to distinguish
the odor of their mother’s human milk from other mothers’ milk. 48
Human milk, being a maternally derived odor, acts as an olfactory rein-
forcer of neonatal ingestive behavior and increases NNS. 49
Two studies (one level II RCT and one level III controlled trial [no ran-
domization]) assessing the effects of human milk odor on the transition
to exclusive direct breastfeeding were identified. 36,37 Sample sizes
ranged from 13 to 80 preterm infants, born between 29 and 34 weeks
PMA. In one study, the preterm infants were exposed, right before a
breastfeeding attempt, to a cotton-tipped applicator moistened with
human milk held at about 1 cm from the preterm infant’s nostrils, for
two minutes once a day for 5 days.36 In the second study, preterm in-
fants were exposed to a sterile pad soaked with human milk that was
placed in the incubator during gavage feeds. 37 In both studies, the con-
trol groups were exposed to a sham odor (water). Raimbault and
colleagues 36 report in their RCT that the preterm infants exposed to
the human milk odor group displayed significantly longer bouts (82 s
vs. 19.5 s) and more bursts (7 vs. 1.5) than the control group. As longer
sucking bursts have been linked to a more mature pattern of feeding, 50
exposing preterm infants to human milk odor right before a
breastfeeding session prepares them to engage in a more efficient suck-
ing activity.36 Preterm infants in the intervention group also consumed
more milk (10 g vs. 0 g) and spent less time at the hospital (median neo-
natal age = 43 days vs. 55.5 days), in comparison to infants who were
exposed to water odor.
The experimental study conducted by Yildiz and colleagues showed
that the time needed to achieve exclusive direct breastfeeding was sig-
nificantly 3 days shorter in the experimental group, and their length of
stay was 4 days shorter than infants in the control group.37 However, no
significant difference was found for the weight gain between both
groups. As a result, in both studies, preterm infants in the experimental
groups had shorter hospital stay because they attained exclusive direct
breastfeeding sooner compared to those in control groups.
Discussion
This review intended to identify and analyze interventions that sup-
port the transition from gavage to direct breastfeeding in preterm in-
fants. Classified in four categories, these interventions all showed a
positive effect on the transition to partial or exclusive direct
breastfeeding, and/or on the development of the sucking competency
in preterm infants, as measured through different outcomes.
NNS and oral stimulation, which were found to be the most fre-
quently and rigorously assessed interventions in the studies reviewed,
show encouraging evidence regarding the attainment of partial or ex-
clusive direct breastfeeding. NNS was either used alone 25,27 or com-
bined with an oral stimulation program. 24,26 Even though both
methods showed positive results, the level of evidence was higher for
NNS used in combination with oral stimulation than for NNS only. How-
ever, in one study, 24 this combination did not lead to the same rapid
transition to direct breastfeeding as in the study of Pimenta and
colleagues.26
In the study of Bache and colleagues,24 two differences were noticed
with the study of Pimenta and colleagues26 that might explain why NNS
and oral stimulation did not accelerate the transition to direct
breastfeeding. While the oral stimulation program was started at
32 weeks, the authors failed to specify if the infants did get an oral feed-
ing readiness assessment before the oral feeds were introduced.24 In the
study by Pimenta and colleagues,26 preterm infants underwent a formal
oral feeding readiness assessment by speech therapists before oral feeds
were initiated. Infant feeding readiness behavior is predictive of feeding
efficiency51 and an appropriate assessment to begin oral feeding may
lead to an improved feeding development. 52 Moreover, in study of
Bache and colleagues, 24 the oral stimulation program was not adminis-
tered by the same interventionist. The assessment of the infant’s oral
feeding readiness and administration of the oral stimulation program
by the same interventionist might have maximized the effects of NNS
and oral stimulation in the study of Pimenta and colleagues.26
 M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91
As for the interventions promoting direct breastfeeding and avoid-
ance of bottles, this review showed that there is an undeniable link be-
tween the optimal exposure of preterm infants to their mother’s breast
and breastfeeding attainment. 30,31 Having the first oral feeding at the
breast and putting preterm infants to breast during the NICU hospitali-
zation guaranteed increased direct breastfeeding at discharge.31 How-
ever, this can only be accomplished with an active involvement from
the neonatal nurses and mothers who should ensure that most of the
preterm infants’ feeds in the NICU are at the breast during the transition
from gavage to direct breastfeeding. Furthermore, the involvement of
mothers in the promotion of their preterm infant’s experience at the
breast can also have a positive impact on maternal confidence and
competence. 19 Hence, frequent exposure of the preterm infant to the
breast can positively influence infant and maternal outcomes.
If encouraging mothers’ involvement is the preferred choice, the use
of a supplementation method, such as the cup or tube, might palliate for
the times that they cannot be present at their preterm infants’ bedside
to feed them at the breast. 28,32 As already discussed, systematic
reviews28,29 concluded that the use of cups increased the length of hos-
pitalization, although the rates of breastfeeding at discharge were
higher in preterm infants receiving cup feedings. Therefore, if the goal
is to increase the success of breastfeeding at discharge, cup feedings
could be an appropriate intervention to be adopted by clinicians. Inter-
estingly, in the largest cup feeding study reviewed in one systematic
review, 28 there was a high degree of non-compliance from the staff
and parents, which, according to the authors, can indicate dissatisfac-
tion with this feeding method. Parents and the staff reported, among
other reasons, that the use of the cup took too long to feed preterm
infants.28 It is noteworthy that in the study of Yilmaz and colleagues,32
no significant difference was noted between the intervention and the
control group in terms of time spent feeding. To increase parents’ satis-
faction and involvement, it could be interesting to offer more support
when the cup is used as a method of supplementation. Besides, the ef-
fectiveness of other supplementation methods during the transition
from gavage to direct breastfeeding, such as a combination of an expo-
sure to the breast and supplementation with a gavage tube, could be
assessed. For example, de Aquino and Osorio explored the use of
relactation, translactation and breast–orogastric tube as alternative
supplementation methods. 30 Their study did show promising results,
especially high breastfeeding rates at discharge. It is worth mentioning
that since a frequent exposure to the breast may increase both the
preterm infant and their mother’s experience, this could have contribut-
ed to the positive results of the proposed interventions by de
Aquino and Osorio. 30 However, their study design was not rigorous
and further research is needed to assess the effectiveness of each of
the interventions. 30 Moreover, additional research needs to explore
the link between the effectiveness of such interventions and the valu-
able experience for the mother–infant dyad gained during exposure to
the breast.
As for the cue-based feeding approach intervention category, it re-
sulted in an earlier attainment of partial 33 or exclusive direct
breastfeeding. 34 The cue-based feeding approach proposes a method
of initiating and advancing feeds that complies with the preterm infant’s
behavioral cues,33 as opposed to the traditional method that consists of
getting preterm infants to feed orally, regardless of their readiness to do
so.53 The traditional method ignores the natural evolution of each infant
and is not developmentally appropriate,53 whereas the cue-based feed-
ing approach raises the importance of a thorough assessment before
starting the oral feeds. In their study, Kirk and colleagues 33 outlined
the neonatal nurse’s role in assessing the preterm infant’s signs of toler-
ance or intolerance of feeds during the transition from gavage to
breastfeeding. Having the neonatal nurse assess the infant’s feeding
progression and adjust its speed accordingly allows a smoother and
safer transition to exclusive direct breastfeeding. In addition to the clin-
ical pathway 33 and the PIBSS scale34 used in the identified studies in this
review, a number of readiness instruments have been developed, such
89
as the Early Feeding Skill (EFS) assessment tool,54 the Preterm Sucking
Readiness (PTSR) scale 43 and the Preterm Oral Feeding Readiness
Scale (POFRS). 55 These tools provide a way to assess oral feeding readi-
ness in preterm infants. However, nurses should use these tools with
caution due to the lack of experimental studies assessing their effective-
ness with this population in a clinical setting.56
The exposure to human milk odor has also shown very promising re-
sults regarding the transition of preterm infants from gavage to direct
breastfeeding such as decreasing preterm infants’ hospital stay,36,37 as
well as oral performance, reflected in longer sucking bouts and more
bursts.36 It is worth mentioning that, in studies included in this review,
the exposure to human milk odor succeeded in having consistent posi-
tive results even though the preterm infants were in different condi-
tions: in their mother’s arms 36 or in incubator during gavage feed. 37
This observation demonstrates that, although preterm infants were
being exposed to human milk in different contextual environments,
this intervention had the same positive impact on their feeding behav-
ior. As a result, the exposure to human milk odor is a low cost and
risk-free intervention that could become part of the preterm infants’
care.36
Overall, most of the included studies (n = 9) had high levels of evi-
dence, with levels equal to or above level III, according to Melnyk and
Fineout-Overholt’s classification (Fig. 2). 38 The categories of interven-
tions supported by higher levels of evidence (with at least one level II
study) are those on NNS and oral stimulation, promotion of direct
breastfeeding and avoidance of bottles, in addition to exposure to
human milk odor. Even though some studies had less rigorous
designs, 30,34 the outcomes were consistent across studies from the
same intervention category.
Direct breastfeeding offers many benefits for the preterm infants
and their mothers, and the intervention categories identified in this re-
view have shown positive results during the transition to direct
breastfeeding. It is noteworthy that the incidence and duration of
breastfeeding remain subject to other factors, such as the establishment
and maintenance of an adequate milk supply 2,57 and the mother’s
ability to be present at her infant’s bedside. 57 Also, the length of mater-
nity leave, which widely varies between countries, 58–60 influences
breastfeeding initiation and duration.61 While the impact of these fac-
tors on the incidence and duration of breastfeeding is undeniable as it
has been thoroughly studied in the literature, 2,56,57,61 their influence
during the transition of preterm infants from gavage to direct
breastfeeding has not been addressed by any of the identified studies.
These mainly focused on assessing the effect of the interventions on
the transition to direct breastfeeding.
Recommendations for Nursing Practice
Nursing practice related to the transition of preterm infants from ga-
vage to direct breastfeeding could benefit from the results of this re-
view. NNS, which has shown benefits for promoting a more rapid
transition from gavage to direct breastfeeding, is an easy and affordable
intervention to be implemented in NICUs. Oral stimulation, based on a
program such as the one developed by Fucile and colleagues, 41 could
also be implemented in NICUs and even administered by trained
parents.62
The findings confirm as well that promoting preterm infants’ experi-
ences at the breast in the NICU increases the incidence of breastfeeding
at discharge and influences the transition to direct breastfeeding. Also, it
appears that experience is a strong predictor for nutritive sucking devel-
opment and preterm infants should be offered more opportunities to
feed orally. 63 Thus, nurses need to encourage mothers who wish to
breastfeed to be frequently present at the bedside to expose their pre-
term infants to the breast. For instance, NICU nurses could establish a
feeding schedule for breastfed preterm infants, with the collaboration
of their mothers to facilitate their involvement. Barriers impeding the
presence of breastfeeding mothers in the NICU should be discussed
90 M. Ziadi et al. / Newborn & Infant Nursing Reviews 16 (2016) 78–91
and addressed when possible. Moreover, mothers of preterm infants
might be pumping their milk for weeks or even months before a transi-
tion to direct breastfeeding is considered.64 Nurses should ensure that a
milk supply is well established before the initiation of transition to di-
rect breastfeeding, as there is evidence that a sufficient human milk sup-
ply is correlated with a more sustained lactation.39
Preterm infants are usually supplemented during their transition to
direct breastfeeding. The avoidance of bottles as a method of supple-
mentation, such as cup feeding, has shown promising results such as
higher breastfeeding rates at discharge. 32 Adequate preparation and
training of NICU nurses and parents could guarantee a higher compli-
ance with this feeding method.
Another intervention that could easily be implemented in NICUs is
the exposure to human milk odor with a cotton-tipped applicator or a
sterile pad moistened. This intervention can be easily performed by ei-
ther the parents or the neonatal nurses. Also, it could be heightening
parents’ empowerment during the transition of their preterm infant
from gavage to direct breastfeeding as feedings represent the perfect
opportunity for them to develop an interactive bond with their
infants. 65 Noteworthy, parents who were empowered during the transi-
tion of their infant from gavage to direct breastfeeding report at the
same time that they felt they were providing support to their preterm
infant and that it helped them to develop skills.65
Lastly, as nurses spend more time with the preterm infants and their
mothers than any other healthcare providers, 66 their role is crucial in
the achievement of the transition to breastfeeding. Nurses usually
show very limited knowledge due to a lack of training in breastfeeding
ill infants, 67 while educating them is a key factor in the transition to
breastfeeding. As most breastfeeding education programs for nurses en-
compass common topics such as lactogenesis, breast pumping issues,
human milk storage and positioning of the infant at the breast,68,69 con-
tent about the transition period from gavage to direct breastfeeding
should also be included to foster nurses’ knowledge about this challeng-
ing step and improve the support offered to mothers.
Recommendations for Nursing Research
The review outlined that some studies had less rigorous designs in
evaluating the effectiveness of some interventions such as the promo-
tion of experiences at the breast and the cue-based feeding approach.
Although the studies’ findings show promising results for the transition
of preterm infants to direct breastfeeding, research design producing a
higher level of evidence, such as RCTs, is needed. More research is also
called for to support the effectiveness of other interventions such as
the promotion of direct breastfeeding, especially regarding the inter-
ventions of relactation, translactation and breast–orogastric feeding. 30
These interventions could be an interesting alternative to the cup feed-
ing since they combine both a supplementation method and the promo-
tion of experiences at the breast. Outcomes, such as time to exclusive
direct breastfeeding, and length of hospital stay could be measured to
give an accurate portrayal of their effectiveness of the transition from
gavage to direct breastfeeding.
The effectiveness of combined interventions, mainly those with
higher levels of evidence, such as NNS and promotion of direct
breastfeeding for instance, could be assessed in future studies. The
combination of high evidence level interventions could possibly
have a cumulative effect on the preterm infants’ such as decreasing
the number of days required for their transition from gavage to exclu-
sive direct breastfeeding.
Furthermore, only one study explored the fact that empowering
parents during the transition is an opportunity for them to gain experi-
ence and a certain confidence with identifying their preterm infant’s
needs and cues. 34 Thus, further research should be conducted to evalu-
ate the effect of their involvement on the fastening the feeding transi-
tion, the development of preterm infants, and their parental and
relational outcomes.
Finally, as mentioned previously, one of the main difficulties en-
countered while doing this review was the lack of clarity in the classifi-
cations related to the transition to breastfeeding. It is recommended
that researchers clearly differentiate between direct breastfeeding and
providing expressed human milk in a bottle. 70 Researchers may be in-
clined to use the World Health Organization (WHO) guidelines,71 how-
ever, while these guidelines do differentiate between exclusive and
nonexclusive breastfeeding, they are simplified and do not provide a
precise definition of breastfeeding categories, such as direct
breastfeeding, or partial breastfeeding.71,72 Labbok and Starling recom-
mend that the development of consistent breastfeeding definitions take
into consideration each level and subcategory of breastfeeding. 72 These
classifications and definitions could be disseminated among researchers
to clarify the breastfeeding terminology in future research.
Conclusion
The aim of this review was to identify and analyze interventions that
promote the transition from gavage to direct breastfeeding in preterm
infants hospitalized in the NICU. Even though the review identified
only a limited number of research studies, the interventions brought
positive benefits for preterm infants during the transition from gavage
to direct breastfeeding, such as higher breastfeeding rates at discharge,
an acceleration of the transition to direct breastfeeding, and a decrease
of the length of hospitalization. Among the identified interventions,
NNS and oral stimulation, as well as the promotion of direct
breastfeeding and avoidance of bottles, were the interventions with
the highest level of evidence.
The wide variability in the breastfeeding terminology and the varie-
ty of outcomes used to measure the transition to direct breastfeeding in
the scientific literature make it difficult to draw a clearer image of the
transition phase and to compare findings. The use of specific descriptors
and definitions in future research related to this transition could help
with finding comparison and generalization.
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