Original Paper
Neonatology 2017;112:211–216
DOI: 10.1159/000472247
Short versus Extended Duration of Trophic
Feeding to Reduce Time to Achieve Full Enteral
Feeding in Extremely Preterm Infants:
An Observational Study
Ariel A. Salas Nazia Kabani Colm P. Travers Vivien Phillips
Namasivayam Ambalavanan Wally A. Carlo
Department of Pediatrics, University of Alabama at Birmingham, Birmingham, AL, USA
Keywords
Minimal enteral feeding · Feeding practices ·
Necrotizing enterocolitis · Premature infants ·
Extremely low-birth-weight infants
Abstract
Background: Trophic feeding compared to no enteral feed-
ing prevents atrophy of the gastrointestinal tract. However,
the practice of extending the duration of trophic feeding of-
ten delays initiation of full enteral feeding in extremely pre-
term infants. We hypothesized that a short duration of tro-
phic feeding (3 days or less) is associated with early initiation
of full enteral feeding. Methods: A total of 192 extremely
preterm infants (23–28 weeks’ gestation) born between
2013 and 2015 were included. Infants were divided into 2
groups according to the duration of trophic feeding (short
vs. extended). The primary outcome was time to achieve full
enteral feeding and the safety outcome was necrotizing en-
terocolitis (NEC) and/or death. Results: A short duration of
trophic feeding was associated with a reduction in time to
achieve full enteral feeding after adjustment for birth weight,
gestational age, race, sex, type of enteral nutrition, and day
© 2017 S. Karger AG, Basel
E-Mail karger@karger.com
www.karger.com/neo
Received: February 10, 2017
Accepted after revision: March 27, 2017
Published online: July 14, 2017
of initiation of trophic feeding (mean difference favoring a
short duration of trophic feeding: –4.1 days; 95% CI: –2.3 to
–5.8; p < 0.001). A short duration of trophic feeding was not
associated with a higher risk of NEC and/or death after
achieving full enteral feeding (AOR: 0.91; 95% CI: 0.30–2.77;
p = 0.87). Conclusions: A short duration of trophic feeding is
associated with early initiation of full enteral feeding. A short
duration of trophic feeding is not associated with a higher
risk of NEC, but our study was underpowered for this safety
outcome. Randomized trials are needed to test this study hy-
pothesis. © 2017 S. Karger AG, Basel
Introduction
In current clinical practice, many clinicians initiate a
3- to 5-day course of minimal enteral feeding or trophic
feeding (≤24 mL/kg/day) within the first 4 days after
birth in extremely preterm infants. Trophic feeding is
then typically followed by progressive feeding (small in-
crements of feeding volumes usually by 20 mL/kg/day
each day) until full enteral feeding is achieved (≥120 mL/
158.232.240.120 - 10/11/2017 3:19:02 PM
Ariel A. Salas, MD, MSPH
HINARI Syrian Arab Republic
Department of Pediatrics, University of Alabama at Birmingham
1700 6th Ave. South, Women and Infants Center Suite 9380
Birmingham, AL 35233 (USA)
Downloaded by:
E-Mail asalas @ peds.uab.edu
kg/day) [1–3]. Some clinicians delay the initiation of
trophic feeding (after the first 4 days after birth), extend
the duration of trophic feeding to 6 or 7 days [4], or initi-
ate progressive feeding without offering trophic feeding
[5, 6].
Some clinical evidence suggests that trophic feeding
before progressive feeding is safe and effective at decreas-
ing the risk of necrotizing enterocolitis (NEC) [4, 6, 7].
However, trophic feeding often delays achievement of full
enteral feeding [8, 9]. Delayed initiation of full enteral
feeding prolongs the use of parenteral nutrition, increas-
es the risk of serious bacterial infections, extends the
length of hospital stay, and increases the risk of postnatal
growth restriction in extremely preterm infants [8–14],
particularly if parenteral nutrition is suboptimal or inad-
equate. Postnatal growth restriction is an important risk
factor for long-term disability in extremely preterm in-
fants [15].
Recent systematic reviews report no evidence of in-
creased risk of NEC after early introduction of progres-
sive feeding (between 1 and 4 days after birth) in very
preterm infants (<32 weeks’ gestation) [8, 9]. However,
data in extremely preterm infants (≤28 weeks’ gestation)
are limited. The risks and benefits of a short duration of
trophic feeding followed by early progressive feeding
have not been well explored in extremely preterm infants
[16]. The objective of this study was to test the hypothesis
that a short duration of trophic feeding (3 days or less) is
associated with early initiation of full enteral feeding and
is not associated with a higher risk of NEC and/or death.
Methods
Subjects
Extremely preterm infants with gestational ages between 23
and 28 weeks’ gestation admitted to the neonatal unit of the Uni-
versity of Alabama at Birmingham (UAB) Hospital between July
2013 and July 2015 were included in this retrospective cohort
study. Infants were excluded if they had major congenital/chromo-
somal anomalies and if they developed spontaneous intestinal per-
foration (SIP), NEC, or died before achieving full enteral feeding.
The study was approved by the UAB Institutional Review Board.
Exposure and Outcome Measurements
Two comparison groups were selected, taking into consider-
ation the duration of trophic feeding. Infants that received trophic
feeding for 3 days or less were included in the short trophic feeding
group. Infants that received trophic feeding for more than 3 days
were included in the extended trophic feeding group. In our unit,
the duration of trophic feeding is not standardized and is based on
daily clinician assessment. Birth weight (BW) influences the dura-
tion of trophic feeding, with smaller infants (BW <750 g) usually
212 Neonatology 2017;112:211–216
DOI: 10.1159/000472247
receiving 5 days of trophic feeding and larger infants (BW ≥750 g)
usually receiving 3 days of trophic feeding.
The primary efficacy outcome of this study was time to achieve
full enteral feeding. This outcome was defined as the time interval
in days between the day of birth and the day that full enteral feed-
ing (>120 mL/kg/day) was achieved. The primary safety outcome
was NEC stage 2 or 3 according to modified Bell’s staging criteria
[17] or death after full enteral feeding. Secondary outcomes in-
cluded duration of progressive feeding (time interval between
completion of trophic feeding and achievement of full enteral
feeding) as a surrogate marker of feeding intolerance, weight at
time of discharge, length at time of discharge, and length of hos-
pital stay.
Feeding Practices
As part of the routine feeding practices in our unit, when co-
lostrum is available, buccal colostrum is offered to all extremely
preterm infants from day of admission to day of initiation of tro-
phic feeding. Trophic feeding is typically initiated between 1 and
4 days after birth via intermittent bolus gavage feeding every 3 h
with either expressed unpasteurized maternal milk or preterm for-
mula. Continuous feeding given by infusion pumps over periods
greater than 30 min is strongly discouraged. Donor human milk is
not routinely offered as an alternative to maternal milk. Events of
feeding intolerance are managed per clinician preference. Early
amino acid supplementation is initiated on admission to provide
an average protein intake of 2.5–3 g/kg/day. Total parenteral nutri-
tion is generally started within 48 h after birth (average protein
intake: 3–4.5 g/kg/day) and discontinued once enteral feeding vol-
umes are close to 100 mL/kg/day. Initiation of human milk forti-
fication with bovine-based products is usually delayed until full
enteral feeding is achieved.
Data Analysis
Because the primary outcome of this study was analyzed as a
continuous measure, an independent comparison of means be-
tween unexposed (infants that receive trophic feeding for more
than 3 days) and exposed (infants that receive trophic feeding for
3 days or less) with 2 unexposed infants per 1 exposed infant was
proposed. A sample size of 144 patients (at least 96 in the unex-
posed group and 48 in the exposed group) was necessary to detect
a 3-day difference in the average time to achieve full enteral feeding
with a standard deviation (SD) of 6 days, a 0.05 level of signifi-
cance, and an 80% power.
Baseline and feeding characteristics were compared using χ2 for
categorical variables and t test or Wilcoxon text for continuous
variables. For analysis of the primary outcome, an adjusted com-
parison of the mean time to full enteral feeding was performed. For
analysis of the primary safety outcome of NEC and/or death, the
risk of NEC and death in the short trophic feeding group was com-
pared to the risk of NEC and death in the extended trophic feeding
group. For all adjusted analyses, BW, gestational age (GA), small
for gestational age (SGA), race, sex, type of enteral nutrition, and
day of initiation of trophic feeding were included as covariates.
Adjusted analyses for the primary outcome were performed using
a mixed model of analysis of variance. Adjusted analyses for the
primary safety outcome were performed using logistic regression.
A post hoc correlation analysis between duration of trophic feed-
ing and time to full enteral feeding was also performed. All statisti-
cal analyses were done with JMP Pro (version 12.0).
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Salas/Kabani/Travers/Phillips/
HINARI Syrian Arab Republic
Ambalavanan/Carlo
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65 infants were included in the brief
Fig. 1. Patient eligibility. NEC, necrotizing trophic feeding group
enterocolitis; SIP, spontaneous intestinal
perforation.
Results
Of a total of 256 eligible extremely preterm infants ad-
mitted between July 2013 and July 2015, 192 achieved full
enteral feeding and were included in the analysis (Fig. 1).
Baseline characteristics of the study population are shown
in Table 1. The mean BW was 726 g, and the median GA
was 26 weeks. More than one-half of infants were of non-
Hispanic black race/ethnicity. BW and GA values were
lower and SGA was more common in the extended tro-
phic feeding group. The short trophic feeding group in-
cluded 19 infants (29%) with BW <750 g and the extend-
ed trophic feeding group included 82 infants (65%) with
BW <750 g.
Trophic feeding was initiated within the first 4 days
after birth in 85% of infants. The median duration of tro-
phic feeding was 5 days (IQR: 3–6) and the median time
to full enteral feeding was 11 days (IQR: 8–13). Duration
of trophic feeding had a strong linear correlation with
time to achieve full enteral feeding in the overall study
population (r = 0.71).
Duration of progressive feeding was similar in both
groups (Table  2). After adjustment for BW, GA, SGA,
race, sex, type of enteral nutrition, and day of initiation of
trophic feeding, an extended period of trophic feeding
(more than 3 days) was not associated with a shorter du-
ration of progressive feeding (mean difference favoring
Trophic Feeding in Extremely Preterm
Infants
256 infants met inclusion criteria
3 had congenital malformations
12 died before trophic feeding
23 died during trophic feeding
13 developed SIP during trophic feeding
205 infants completed trophic feeling
11 developed SIP orNEC
2 died of causes unrelated to SIP or NEC
192 infants achieved full enteral feeding
127 infants were included in the
extended trophic feeding group
an extended period of trophic feeding: –0.2 days; 95% CI:
–1.4 to 1.1; p = 0.78). Full enteral feeding was achieved
earlier after a short duration of trophic feeding (12.5 vs. 9
days; p < 0.001). A short duration of trophic feeding was
associated with early achievement of full enteral feeding
after adjustment for the same covariates (mean difference
favoring a short duration of trophic feeding: –4.1 days;
95% CI: –2.3 to –5.8; p < 0.001).
The risk of NEC, death, and the combined outcome of
NEC or death did not differ between groups. After adjust-
ment for BW, GA, SGA, race, sex, type of enteral nutri-
tion, and day of initiation of trophic feeding, a short du-
ration of trophic feeding was not associated with a higher
risk of NEC or death (AOR: 0.91; 95% CI: 0.30–2.77; p =
0.87).
A short duration of trophic feeding was not associated
with a higher mean weight (3,216 vs. 3,128 g; p = 0.51) or
mean length (46.4 vs. 46.8 cm; p = 0.59) at time of dis-
charge after adjustment for BW, GA, SGA, race, sex, type
of enteral nutrition in the first 28 days after birth, day of
initiation of trophic feeding, and length of hospital stay.
Among those 11 infants excluded from the study for
diagnosis of SIP or NEC before achievement of full en-
teral feeding, 5 infants received a short duration of tro-
phic feeding and 6 infants received an extended period of
trophic feeding. The mean duration of trophic feeding
was 4 days in these 11 infants (range: 2–6 days).
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DOI: 10.1159/000472247
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 Table 1. Baseline characteristics

Short trophic Extended trophic p

feeding group feeding group
(n = 65) (n = 127)

Demographics
BW, g 812 ± 139 682 ± 142 <0.0001
GA, weeks 26 (25 – 27) 25 (24 – 27) 0.002
SGA status 2/65 (3) 31/127 (24) 0.0002
Male sex 25/65 (38) 50/127 (42) 0.90
Black race 36/65 (55) 70/127 (55) 0.97
Feeding practices
Initiation of trophic feeding, days 2 (2 – 3) 2 (1 – 3) 0.07
Exclusive human milk feeding in the first 28 days after birth
Postnatal day 1 – 7 46/65 (71) 83/127 (65) 0.45
Postnatal day 8 – 14 41/65 (63) 73/127 (57) 0.45
Postnatal day 15 – 21 32/65 (49) 62/127 (49) 0.96
Postnatal day 22 – 28 14/65 (22) 30/127 (22) 0.75

Values are presented as means ± SD, medians (IQR), or n/total (%). BW, birth weight; GA, gestational age;
SGA, small for gestational age.

Table 2. Feeding and safety outcomes

Outcomes Short trophic Extended trophic p

feeding group feeding group
(n = 65) (n = 127)

Duration of trophic feeding, days 2 (2 – 3) 6 (5 – 7) <0.0001

Duration of progressive feeding, days 5 (4 – 8) 6 (5 – 8) 0.46
Initiation of full enteral feeding, days 8 (7 – 10) 12 (10 – 15) <0.001
NEC or SIP before and after full enteral feeding, % 9/70 (6) 21/133 (12) 0.57
NEC after full enteral feeding, % 4/65 (6) 15/127 (12) 0.21
Mortality after full enteral feeding, % 6/65 (9) 17/127 (13) 0.40
Mortality before and after full enteral feeding, % 7/70 (9) 18/133 (13) 0.47
Length of hospital stay, days 86 (64 – 113) 104 (79 – 143) <0.01
NEC or death after full enteral feeding, % 10/65 (15) 24/127 (18) 0.54

Values are presented as n/total (%) or medians (IQR). NEC, necrotizing enterocolitis; SIP, spontaneous
intestinal perforation.

Discussion intolerance, or a lower risk of NEC or death after full en-

This observational study compared short versus ex-
tended periods of trophic feeding in extremely preterm
infants. A short duration of trophic feeding was associ-
ated with a significant reduction in time to achieve full
enteral feeding after adjustment for important confound-
ing factors such as BW, GA, and SGA status. An extended
period of trophic feeding was not associated with a short-
er duration of progressive feeding, a surrogate of feeding
teral feeding. The potential benefits of extending trophic
feeding to reduce the probability of feeding intolerance
during progressive feeding were not detected.
Previous studies have described benefits of early
achievement of full enteral feeding in extremely preterm
infants. These potential benefits include reduced dura-
tion of parenteral nutrition [8], reduced need for central
access, reduced risk of serious bacterial infections [8, 10,
11], and better growth at time of discharge [8]. Less seri-
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214 Neonatology 2017;112:211–216 Salas/Kabani/Travers/Phillips/

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DOI: 10.1159/000472247 Ambalavanan/Carlo

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ous bacterial infections and optimized nutritional out-
comes may reduce the risk of postnatal growth restriction
and improve long-term neurodevelopmental outcomes
of extremely preterm infants who survive to hospital dis-
charge.
Our results are in line with the current uncertainty on
whether extended periods of trophic feeding decrease the
risk of NEC in extremely preterm infants [9]. The feeding
methods and analytic approach [18] used in the first ran-
domized trial conducted between 1996 and 2000 favoring
extended periods of trophic feeding as compared to early
progressive feeding to decrease the incidence of NEC [4]
differ from current practices. Late initiation of enteral
feeding is now discouraged; the presence of umbilical
catheters or infusions of pressor agents are no longer con-
traindications to initiate enteral feeding; the use of ante-
natal steroids has increased substantially over the past de-
cade [19] and evidence from randomized trials [20] sup-
ports the concept that donor human milk reduces the risk
of NEC. These changes in practice could explain findings
of a recent randomized trial conducted between 2006
and 2009 reporting similar risks of NEC stage 2 or 3 in
growth-restricted infants ≤32 weeks’ gestation receiving
early progressive feeding (after a short duration of trophic
feeding) or late progressive feeding [8].
One of the main limitations of our study is the retro-
spective study design. The significant variation in days of
trophic feeding found in this study indicates that our cur-
rent guidelines to standardize duration of trophic feeding
based on BW cutoffs are not universally followed. This
finding suggests that duration of trophic feeding is main-
ly influenced by daily clinical assessments of the overall
status of the infant [21] and that feeding intolerance is
common during trophic feeding. Previous studies have
documented that feeding practices during the first week
after birth differ according to severity of illness. Feeding
is often initiated earlier and advanced more rapidly in less
critically ill preterm infants [21]. Accounting for severity
of illness may involve addition of more clinical covariates
in adjusted analyses to improve the precision of risk esti-
mates; however, because BW and GA define nearly 80%
of the variability in prediction of neonatal outcomes [22],
adjusted analyses with only these two important determi-
nants of outcomes in extremely preterm infants are still
considered a reasonable strategy to account for severity of
illness. When severity of illness is defined according to
days of mechanical ventilation during the first week after
birth, substantial differences in BW and GA between
more critically ill and less critically ill infants are found
[21]. Nevertheless, it is important to acknowledge that
Trophic Feeding in Extremely Preterm
Infants
adjustment for severity of illness to minimize selection
bias in retrospective studies is less effective than random-
ization.
The other important limitations are the insufficient
power to detect true differences in the incidence of NEC
between groups, the lack of specific criteria to define
feeding intolerance in the study, the external validity of
this single center study, and the exclusion of infants that
were unable to achieve full enteral feeding. As many oth-
er neonatal feeding studies, including randomized trials,
our study was not sufficiently powered for the outcome
of NEC. External validity is also an important consider-
ation because feeding practices in extremely preterm in-
fants differ significantly across centers [21, 23]. Exclu-
sion of infants that died before receiving trophic feeding
was inevitable because the exposure status under inves-
tigation (i.e., duration of trophic feeding) was impossible
to assess in those circumstances. Infants that developed
SIP during trophic feeding were also excluded because a
diagnosis of SIP or NEC during trophic feeding results in
discontinuation of feeding and, therefore, modification
of the trophic feeding plan. Exclusion of infants that de-
veloped SIP or NEC during progressive feeding but be-
fore achieving full enteral feeding was necessary to assess
the primary feeding outcome in all infants that complet-
ed trophic feeding. A detailed description of the patients
excluded for this specific indication was included in this
report.
One of the strengths of our analysis is the inclusion of
extremely preterm infants with substantial physiologic
immaturity of the gastrointestinal tract. Severe hypoten-
sion, hypoxemia, duration of mechanical ventilation,
presence of umbilical catheters, and infusions of pressor
agents were not exclusion criteria for this study.
In summary, these findings suggest that a short dura-
tion of trophic feeding may reduce the time to achieve full
enteral feeding without increasing the risk of NEC or
death in extremely preterm infants. Our results also indi-
cate that the practice of extending the duration of trophic
feeding may not have protective effects against NEC or
the number of feeding interruptions during progressive
feeding, a surrogate of feeding intolerance. An enteral
feeding plan aimed to reduce the duration of trophic feed-
ing and regulated by daily assessments of enteral toler-
ance could result in earlier achievement of full enteral
feeding in extremely preterm infants. Randomized con-
trolled trials on duration of trophic feeding could remove
some important confounders found in this study and de-
termine if there are other benefits associated with a short
duration of trophic feeding.
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DOI: 10.1159/000472247
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 Acknowledgements Funding Sources
We are indebted to our medical and nursery staff of the neona- This research did not receive any specific grant from funding
tal unit at UAB Hospital for their continuous support in imple- agencies in the public, commercial, or not-for-profit sectors.
mentation and evaluation of alternative feeding practices in ex-
tremely preterm infants.
Author Contributions

Disclosure Statement A.A.S. conceptualized and designed the study, collected the
data, performed statistical analysis of the data, drafted the initial
The authors declare no conflicts of interest. manuscript, revised the manuscript and approved the final manu-
script as submitted.
N.K., C.P.T., and V.P. assisted with the study design, collected
the data, revised the manuscript, and approved the final manu-
script as submitted.
W.A.C. and N.A. assisted with the study design, critically re-
viewed the manuscript, and approved the final manuscript as sub-
mitted.

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