The Journal of Nutrition

Supplement: Achieving Optimal Growth in Preterm Infants and Children

A Systematic Review of Practice Surveys on

Parenteral Nutrition for Preterm Infants1–3
Alexandre Lapillonne4–6* and Elsa Kermorvant-Duchemin4,5
4
Paris Descartes University, Paris, France; 5APHP Necker-Enfants Malades University Hospital, Paris, France; and 6ChildrenÕs Nutrition
Research Center, Baylor College of Medicine, Houston, TX

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Abstract
Significant efforts have been made to improve the nutritional support of preterm infants in neonatal intensive care units
(NICUs) to avoid cumulative nutritional deficits, reduce postnatal growth restriction, and promote optimal long-term
development. The objective of this systematic review was to compare the characteristics and results of all surveys published
in the past 10 y (2002–2012) that used a questionnaire to survey at least 2 NICUs receiving preterm infants with an intention
to treat with parenteral nutrition (PN) and that reported information on at least 1 macronutrient. A total of 6 surveys were
identified, which were conducted in the United States (n = 2) or Europe (n = 4). There was wide variability in the response
rate (23–100%), with a higher response rate in the smaller studies (81–100%; 8–64 respondents) compared with the larger
studies (23–58%; 296–809 respondents). Large differences were observed in the nutritional protocols both among the NICUs
in the individual surveys and between surveys. PN was initiated on the first day of life (DOL) by only 24–54% of respondents
(4 surveys) and within the second DOL by 67–94% of respondents (5 surveys). Lipids were initiated before the third DOL for
46–96% of respondents (3 surveys). The results of this systematic review suggest that continuous education is needed and
that greater efforts are required to disseminate and implement guidelines. Repeated surveys are needed to highlight trends in
clinical practices and level of compliance of NICUs with existing guidelines. J. Nutr. 143: 2061S–2065S, 2013.

Introduction
Clinical studies have shown that improving nutritional intake
reduces the cumulative energy and protein deficit that may occur
in preterm infants, promoting postnatal growth and improving
neurodevelopmental outcomes (1–6).
Clinical practice guidelines for the nutritional needs of pre-
term infants have been regularly revised over recent decades,
leading to the development of the most recent guidelines on
pediatric parenteral nutrition (PN)7 in Europe from the Euro-
1
Presented at the 4th Congress of the European Academy of Paediatric Societies
(EAPS) conference, held in Istanbul, Turkey, 5 October 2012. The symposium was
sponsored by Baxter Healthcare International. The views expressed in these
papers are not necessarily those of the Supplement Coordinator or Guest Editors.
The Supplement Coordinator for this supplement was Louise Profit, Gardiner-
Caldwell Communications. Supplement Coordinator disclosures: Louise Profit is
an employee of Gardiner-Caldwell Communications, a medical communications
company that received financial remuneration from Baxter Healthcare for
coordination of the supplement, medical editing, and medical writing support.
This supplement is the responsibility of the Guest Editor to whom the Editor of The
Journal of Nutrition has delegated supervision of both technical conformity to the
published regulations of The Journal of Nutrition and general oversight of the
scientific merit of each article. The Guest Editor for this supplement was Harry
Dawson. Guest Editor disclosure: Harry Dawson had no conflicts to disclose.
Publication costs for this supplement were defrayed in part by the payment of
page charges. This publication must therefore be hereby marked "advertisement"
in accordance with 18 USC section 1734 solely to indicate this fact. The opinions
expressed in this publication are those of the authors and are not attributable to the
sponsors or the publisher, Editor, or Editorial Board of The Journal of Nutrition.
* To whom correspondence should be addressed. E-mail: alexandre.lapillonne@
nck.aphp.fr.
pean Society of Paediatric Gastroenterology, Hepatology, and
Nutrition and the European Society for Clinical Nutrition and
Metabolism in 2005 (7), and globally in the book entitled ‘‘Nu-
tritional Needs of the Preterm Infant: Scientific Basis and
Practical Guidelines’’ published in 2005 (8).
Reports from neonatal intensive care units (NICUs) world-
wide have shown that nutritional intake in preterm infants
is inadequate (9,10). The causes of this inadequate intake,
particularly in the early neonatal phase, may be multifactorial
and partly iatrogenic. It may depend not only on the infantÕs
metabolic capacities but also on the availability and safety of the
solutions used, the type of venous access, the departmentÕs usual
practice, and the prescriberÕs knowledge of the infantÕs nutri-
tional needs (11).
Although the prescriberÕs knowledge and compliance with
PN guidelines is difficult to examine, several surveys have been
conducted to determine the nutritional protocols and practices
in preterm infants in NICUs. The objective of this systematic
2
Gardiner-Caldwell Communications was funded by Baxter Healthcare Corporation
for support in editing and styling this manuscript. The Association pour la Recherche
et la Formation En Neonatologie (ARFEN) provided technical assistance.
3
Author disclosures: A. Lapillonne and his institution have collaborated scientifically
with the following manufacturers of parenteral nutrition solutions: Baxter Healthcare
and Fresenius-Kabi. He has received honoraria for consulting or lecturing from
Baxter Healthcare and Fresenius-Kabi. E. Kermorvant-Duchemin, no conflicts of
interest.
7
Abbreviations used: AA, amino acid; DOL, day of life; NICU, neonatal intensive
care unit; PN, parenteral nutrition; VLBW, very low birth weight.

ã 2013 American Society for Nutrition.

Manuscript received March 6, 2013. Initial review completed May 17, 2013. Revision accepted September 9, 2013. 2061S
First published online October 9, 2013; doi:10.3945/jn.113.176982.
review was to compare the characteristics and results from those

Physicians (specialist registrars)

Physicians, dieticians, neonatal

surveys published in the past 10 y, to compare the variation in

nurse practitioner
nutritional protocols over time, and to evaluate adherence to

This survey was not entirely focused on nutrition and comprised 15 sections addressing clinical conditions commonly encountered during the management of VLBW infants, of which fluid, electrolytes, and nutrition were 1 section.
respondents

Pharmacists
Position of
guidelines.

Physicians

Physicians
Physicians
Methods
A PubMed, Embase, and Cochrane Central Register of Controlled Trials
search was conducted from 1 January 2002 to 31 December 2012. The
following search terms were used with regard to the following: type of
survey (‘‘questionnaire’’ OR ‘‘survey’’ OR ‘‘nutritional survey’’), topic

Response rate

physicians)
100 (91% of
(‘‘nutrition’’ OR ‘‘parenteral nutrition’’), and population surveyed
(‘‘preterm infant’’ OR ‘‘premature infant’’ OR ‘‘very low birth weight

95

81

23

58
37
%
infant’’). The search was limited to human studies. A manual search of
the reference lists of all relevant articles was also performed. The

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citations with abstracts were uploaded into a reference database and
checked for duplicates.

52/64 (48 units analyzed)

8/8 (29/32 physicians)
surveyed/contacted
Studies were included if they met all of the following criteria: survey

176/775 individuals
Number of units
on PN, use of a questionnaire, intention to treat, information on at least

172/296
297/809
1 macronutrient, neonatal units receiving preterm infants, and at least

54/57
2 units surveyed. Studies reporting actual prescriptions of PN in preterm
infants were excluded because they reflect the real practice, which may
substantially differ from the intention to treat for various reasons (11).
Both reviewers (A.L. and E.K.-D.) read the selected articles. A. L. ex-
tracted, assessed, and coded all data for each study by using a form that

E-mail and mail

administration
was designed specifically for this review. E. K.-D. checked the extraction

Method of
process and validity of the data. At each stage, any discrepancies were

E-mail
Phone

Mail

Mail
Mail
resolved by discussion.
The following information was extracted from the articles and
entered into a spreadsheet to allow direct comparison of the survey
characteristics and results: year of survey, country, type of institution,

ELBW, VLBW, LBW

type of preterm infants [i.e., extremely low birth weight, very low birth

ELBW (,1000 g)
Type of infant

Not described
weight (VLBW), or low birth weight], format (i.e., open, closed, or

ELBW, extremely low birth weight; LBW, low birth weight; NICU, neonatal intensive care unit; VLBW, very low birth weight.
VLBW2

VLBW

VLBW
multiple-choice questions), method of administration (i.e., phone,
e-mail, or mail), number of units surveyed/contacted, type of respon-
dents (e.g., physicians), response rate, timing of initiation of nutrition
(i.e., amino acids, lipids, glucose, and calories), and target intake of each
nutrient and the dosage used. To assess compliance with the most recent

Multiple-choice and
Type of questions

guidelines, the initiation and dose of nutrients were compared with those

Multiple-choice
Not described3

open-ended
Not described
recommended by the European (7) and global (8) guidelines.
Characteristics of the surveys included in the systematic review1

Closed
Open

Results
Of the 380 identified articles, we excluded 362 on the basis of a
review of the title and abstract because they did not report any
$5 intensive care cots
NICU with $6 intensive

Level III or II NICU with

survey data. The full text of the remaining 18 articles was

Type of institution

extensively reviewed to determine whether the articles met the

care cots

inclusion or exclusion criteria. Eight articles did not meet our

NICUs

NICUs

NICUs
NICUs

inclusion criteria (survey on enteral nutrition, n = 2; not a survey,

n = 4; review article, n = 1; study reported actual prescriptions,
n = 1). We excluded another 3 articles because they did not
report data for the use of at least 1 nutrient. Of the remaining
7 articles, 2 reported the same survey, but with additional data
Country

Ireland

France

published in separate articles, and both articles were kept in the

USA

USA
UK

UK

Clinical case of a 28-wk VLBW infant (1.1 kg).

systematic review.

Characteristics of the evaluated surveys. The characteristics

2005–2006
Year of

of the surveys are provided in Table 1. Four of the surveys were

study

2002

2005

2006

2006
2007

conducted in Europe, and 2 in the United States. Two surveys

(12,13) were conducted before the availability of the European
Society of Paediatric Gastroenterology, Hepatology, and Nu-
Lapillonne et al. (17,21)

trition guidelines published in 2005. The majority of the

Fleming et al. (13)

respondents were physicians (5 surveys) with only 1 study (14)

Ahmed et al. (12)

Grover et al. (14)

Kiefer et al. (15)

Hans et al. (16)
TABLE 1

evaluating pharmacistsÕ responses. The type of preterm infants

studied, the means of administration of the survey (e-mail,
Survey

phone, or mail), the format of the questions (open, closed, or

multiple-choice) also varied among surveys (Table 1).
1

2062S Supplement
 The objectives and the focus of the survey questionnaires also

3 to 4 (66% of respondents)
varied; 2 studies (13,15) reviewed current practice in the
management of VLBW and extremely-low-birth-weight infants,

Target for lipids

Median dose: 3
which not only included questions on nutrition but also on other

g/(kg
d)
N/A

N/A

N/A

N/A
aspects of management, such as respiratory care. Two studies
(12,14) reviewed current practices in PN administration and
management, and 2 studies (16,17) compared current nutri-
tional practices according to published recommendations.

Survey response and risk of bias. There was wide variability

$2 (8.1% of respondents)
in the response rate for these surveys (23–100%). There was a

0.5 (78% of respondents)

0.5 (45% of respondents)

1 (46% of respondents)
Initial dose of lipids
higher response rate (81–100%) in the 3 smaller studies (8–64

Median dose: 1

VLBW: 0 to 3
ELBW: 0 to 3

LBW: 0 to 3
respondents) compared with the response rate (23–58%) in the

g/(kg
d)
N/A

N/A
larger studies (296–809 respondents) (Table 1).

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Nutritional outcomes. An overview of the results from each
survey for the timing of initiation of PN (amino acids and lipids),
target intakes of each nutrient, and the initial dosage is shown in

Current practice for parenteral nutrition (amino acids and lipids) in neonatal intensive care units responding to the surveys1
Table 2.

Before 3rd DOL (96% of respondents)

Before 3rd DOL (46% of respondents)

Before 3rd DOL (94% of respondents)
First DOL (40% of respondents)

First DOL (2% of respondents)

#48 h (54% of respondents)
.48 h (46% of respondents)
Amino acids. All surveys documented the day of life (DOL) on
which PN was initiated (introduction of amino acids) (Table 2).

Initiation of lipids
PN was initiated on the first DOL by 24–54% of respondents

N/A

N/A
(4 surveys) and on the second DOL by 67–94% of respondents
(5 surveys). One study in the United States (16) showed that the
mean age of PN initiation in VLBW infants was 1.25 d, although
some VLBW infants received PN as late as the fifth DOL. Of

AA, amino acid; DOL, day of life; ELBW, extremely low birth weight; LBW, low birth weight; N/A, not available; VLBW, very low birth weight.
those surveys reporting the initial dose of amino acids, the dose
ranged from 0.5 to 4 g/(kg
d). Knowledge of the target dose for
amino acids was largely unknown in 1 study conducted in 2002
(12), and the target dose was known to be $3 g/(kg
d) by only

ELBW, VLBW, and LBW: 2.5 to 4

Unknown (65% of respondents)

3.5–4.0 (44% of respondents)

$3 (27% of respondents)

$3 (92% of respondents)
27% of respondents in 1 survey conducted in 2006 (14). 3 (11% of respondents)
Target dose of AAs

.3 (none)
Lipids. Four surveys documented the DOL on which lipid
g/(kg
d)

N/A

N/A
emulsions were initiated (Table 2). Three surveys showed that
lipids were initiated before the third DOL for 46–96% of
respondents; they were initiated before the second DOL for 54%
of respondents in 1 study (12). The initial dose was frequently
between 0.5 and 1.0 g/(kg
d), except in 1 study in the United
States (15) in which the dose was 2 g/(kg
d) for 8% of
respondents. A target lipid dose of 3 to 4 g/(kg
d) was reported #1 (96% of respondents)

$2 (66% of respondents)
1 (34% of respondents)
Initial dose of AAs

by 66% of respondents in 1 survey (18).

Median dose: 0.5

VLBW: 0.5 to 4.0

ELBW: 0.5 to 4.0

LBW: 0.5 to 4

$2 (none)
Common indications to stop or decrease lipids in PN were
g/(kg
d)
N/A

N/A

described in 3 studies (12,16,17). The most frequently cited

indications were confirmed or suspected sepsis, increased liver
enzymes, conjugated or unconjugated hyperbilirubinemia, low
platelet count, disseminated intravascular coagulation, high
TGs, and acidosis. However, the perception by physicians of
these conditions as absolute or relative contraindications for
First 2 DOL (67% of respondents)

First 2 DOL (75% of respondents)

First 2 DOL (94% of respondents)

First 2 DOL (89% of respondents)

First 2 DOL (94% of respondents)
First DOL (24% of respondents)

First DOL (27% of respondents)

First DOL (54% of respondents)

First DOL (49% of respondents)

.48 h (33% of respondents)

lipid infusions varied dramatically within and between studies,

VLBW (1st to 5th DOL)
ELBW (1st to 3rd DOL)

LBW (1st to 6th DOL)

making it impossible to identify a common pattern.

Initiation of AAs

Glucose and calories. The current practice for PN (glucose

and calories) in NICUs responding to the surveys was detailed in
several studies (14,17,18) (Table 3). In an e-mail survey of
pharmacists performed in the United Kingdom between 2005
and 2006 (14), the median initial and target doses of glucose
were 5.9 and 14.1 g/(kg
d), respectively. The median initial
amount of calories initiated was 25.6 kcal/(kg
d), with a median
Lapillonne et al. (17,18)

target of 95.2 kcal/(kg
d).

Fleming et al. (13)
Ahmed et al. (12)

Grover et al. (14)

Kiefer et al. (15)

Hans et al. (16)
TABLE 2

Discussion
Survey

The results of individual surveys have previously demonstrated

that the knowledge and clinical practices of the respondents for
1

Parenteral nutrition for NICU patients 2063S

TABLE 3 Current practice for parenteral nutrition (glucose and calories) in neonatal intensive care units responding to the surveys
Survey Initiation of glucose Target dose of glucose
g/(kg
d)
Grover et al. (14) Median dose: 5.9
$17.3 (10.4% of respondents)
Lapillonne et al. (17,18) #6 (40% of respondents) #16 (42% of respondents)
17–18 (53% of respondents)
.18 (5% of respondents)
1
Not available.
the nutritional support of preterm infants varied greatly among
NICUs. The results from this systematic review further support
this finding by demonstrating that variations also exist between
surveys and countries.
The methodologic limitations of using surveys for the as-
sessment of nutritional protocols have been previously discussed
in detail (17), and it should be reiterated that these surveys
reflect the intention to treat of the personnel from the NICU who
respond to the survey and may not reflect the actual clinical
practice within the unit. Nevertheless, intention to treat reflects
one of the first steps of the dissemination of guidelines and thus
provides insight on compliance to guidelines.
The most recent European and U.S. guidelines recommended
a change in PN practice, specifying that amino acids should
be initiated earlier, on the first DOL with a minimum intake of
1.5–2 g/(kg
d) and a maximum intake of 4.0 g/(kg
d) [3.2–3.8
g/(kg
d) for VLBW infants] (7,8,19). Therefore, it is not
surprising that the results from those surveys conducted before
the publication of these guidelines demonstrate a failure to
comply with these recommendations. However, the results from
surveys conducted after the publication of these guidelines still
demonstrate that the recommended timing and dose of amino
acids are frequently not met. Furthermore, a survey performed in
Poland in 2007 (20) showed that PN was not used for the care of
preterm infants in approximately half of the 302 units that were
surveyed.
Current guidelines recommend that lipid administration be
initiated between the first and second DOL (7,8), and a recent
systematic review of the literature has demonstrated that ini-
tiation of lipids within the first 2 DOL in VLBW infants is safe
and well tolerated (21). The timing of initiation of lipid infusion
to VLBW infants has previously been reported to vary widely
among different NICUs (17). The results from this systematic
review confirm that the timing of lipid administration also varies
between surveys to a scale that is even larger than that for amino
acids. It was also found that there was a lack of consensus be-
tween surveys on the contraindications for lipids and/or indica-
tion for stopping lipids, reflecting the lack of scientific data and
absence of clear guidance on this topic.
In summary, although the level of compliance with current
guidelines is still unclear, the results of this systematic review
suggest that continuous education is needed and that greater
efforts are required to disseminate and implement them. The
limited or delayed availability of individualized PN solutions
(17), as well as difficulties in ordering individualized PN (3),
have previously been identified as reasons for noncompliance
with guidelines. Repeating these surveys is needed to determine
how much treatment variation in routine clinical practice may
still exist, to assess the level of compliance of NICUs with
existing clinical practice guidelines, and to highlight trends in
clinical practices over time. Larger surveys that include several
countries may also help to compare variations in practice
2064S Supplement
Calories initiated Target calories
g/(kg
d) kcal/(kg
d) kcal/(kg
d)
Median: 14.1 Median: 25.6 Median: 95.2
N/A1 #110 (31% of respondents)
120 (54% of respondents)
$130 (14% of respondents)
between countries and to determine the factors that may
promote or restrict implementation of guidelines at a national
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level. Given the need for continuous monitoring, it would be of
value for scientific societies (particularly those that publish
guidelines) to develop web-based standard reporting systems
that determine the actual compliance of in-house protocols with
guidelines. In the case of nutrition for preterm infants, a limited
number of questions on access to PN and the dose of nutrients
given would be sufficient to provide insight on the implementa-
tion of guidelines at a local level.
Acknowledgments
The authors thank Louise Profit of Gardiner-Caldwell Com-
munications for support in drafting and editing the manuscript.
A.L. designed the research; and A.L. and E.K.-D. analyzed the
data, wrote the manuscript, and had primary responsibility for final
content. Both authors read and approved the final manuscript.
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Parenteral nutrition for NICU patients 2065S