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Original Communication

Nutrition Therapy in a Pediatric


Intensive Care Unit: Indications,
Monitoring, and Complications

Journal of Parenteral and


Enteral Nutrition
Volume 35 Number 4
July 2011 523-529
2011 American Society for
Parenteral and Enteral Nutrition
10.1177/0148607110386610
http://jpen.sagepub.com
hosted at
http://online.sagepub.com

Patrcia Zamberlan, MSc1; Artur Figueiredo Delgado, MD2; Cludio Leone, PhD3;
Rubens Feferbaum, MD4; and Thelma Suely Okay, PhD4
Financial disclosure: None declared.
Background: Nutrition therapy (NT) is essential for the care of
critically ill children. Inadequate feeding leads to malnutrition
and may increase the patients risk of morbidity and mortality.
The aim of this study was to describe the NT used in a tertiary
pediatric intensive care unit (PICU). Methods: The authors
evaluated NT administered to 90 consecutive patients who
were hospitalized for 7 days in the PICU of Instituto da
Criana, Hospital das Clnicas, Universidade de So Paulo,
Brazil. NT was established according to the protocol provided
by the institutions NT team. NT provided a balance of fluids
and nutrients and was monitored with a weekly anthropometric nutrition assessment and an evaluation of complications.
Results: NT was initiated, on average, within 72 hours of hospitalization. Most children (80%) received enteral nutrition
(EN) therapy; of these, 35% were fed orally and the rest via

nasogastric or postpyloric tube. There were gastrointestinal


complications in patients (5%) who needed a postpyloric tube.
Parenteral nutrition (PN) was used in only 10% of the cases,
and the remaining 10% received mixed NT (EN + PN). The
average calorie and protein intake was 82 kcal/kg and 2.7 g/kg
per day. Arm circumference and triceps skinfold thickness
decreased. Conclusions: The use of EN was prevalent in the
tertiary PICU, and few clinical complications occurred. There
was no statistically significant change in most anthropometric
indicators evaluated during hospitalization, which suggests
that NT probably helped patients maintain their nutrition status. (JPEN J Parenter Enteral Nutr. 2011;35:523-529)

Clinical Relevancy Statement

Introduction

Undernutrition is highly prevalent in critically ill children


around the world, mainly in tertiary pediatric intensive care
units. Nutrition intervention with a focus on adequate
delivery of micro- and macronutrients guided by protocols
can improve the quality of treatment and aid in avoiding
further undernutrition. Knowledge of the sequential
anthropometric condition of admitted patients is essential
in providing early and sufficient nutrition support.

Despite technological advances, malnutrition is still widespread in pediatric intensive care units (PICUs). Studies
have shown that 24% to 55% of patients present with
acute or chronic malnutrition on admission and that
deterioration of nutrition status commonly occurs during
hospitalization.1-3
Critically ill children have a high risk of malnutrition because of stress-induced changes in intermediary
metabolism; these changes are characterized by an
increased basal metabolic rate and intensive protein
catabolism.4-6 In general, the development or perpetuation of malnutrition during hospitalization in the PICU
is due to illness, unknown nutrition condition, and an
inadequate supply of nutrients.7,8 In these patients, malnutrition is associated with physiologic instability. As a
result, more intensive clinical care is required, and the
mortality rate is high.6
Nutrition care studies have proposed that an early
intervention that targets nutrition assessment can prevent or minimize the complications of malnutrition.9,10
Nutrition therapy (NT) is indicated when a patient is
unable to receive calories and nutrients orally for a long
period of time. Enteral nutrition (EN) is preferred

Keywords: nutrition assessment; anthropometry; children;


nutrition therapy; enteral nutrition; parenteral nutrition

From the 1Division of Nutrition and 2Pediatric Intensive Care


Unit, Nutritional Team of Instituto da Criana do Hospital das
Clnicas da Faculdade de Medicina da Universidade de So
Paulo, So Paulo, Brazil; 3Department of Mother and Child
Health, Faculdade de Sade Pblica da Universidade de So
Paulo, So Paulo, Brazil; and 4Department of Pediatrics,
Faculdade de Medicina da Universidade de So Paulo, So
Paulo, Brazil.
Received for publication January 15, 2010; accepted for publication August 7, 2010.
Address correspondence to: Patrcia Zamberlan, Division of
Nutrition, Nutritional Team of Instituto da Criana do Hospital das
Clnicas da Faculdade de Medicina da Universidade de So Paulo,
So Paulo, Brazil; e-mail: pzamberlan@uol.com.br.

523

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524 Journal of Parenteral and Enteral Nutrition / Vol. 35, No. 4, July 2011

because it is more physiologic, promotes intestinal trophism, stimulates the immune system, and reduces the
incidence of bacterial translocation and sepsis; in addition, it presents fewer complications and costs less than
parenteral nutrition (PN).9,11,12 However, when it is
impossible to use the digestive tract, PN is the only
alternative for ensuring an adequate supply of nutrients
during hospitalization.13 The combination of PN and EN
may be useful for the first 72 hours of intensive clinical
care or when EN alone is not sufficient to meet the
nutrition demands of the patient.8,14-16
Although the consensus is that NT is essential in the
care of critically ill children, especially in the acute phase
of stress, its implementation remains the major challenge
in PICUs. Both PN and EN present risks. EN may be associated with gastric complications, which may affect tolerance and increase the risk of aspiration pneumonia. PN can
result in atrophy of the intestinal mucosa, liver abnormalities, hyperglycemia, and an increased risk of infectious complications.6,9
The main objective of this 1-year study was to
describe the restrictions, monitoring, and complications
associated with NT in a tertiary PICU.

Methods
Subjects
For this descriptive, prospective study, the participants
were selected from infants, preschool children, schoolchildren, and adolescents sequentially admitted to the
PICU of Instituto da Criana, Hospital das Clnicas da
Universidade de So Paulo, Brazil. This 15-bed, tertiary
ICU primarily attends to patients with chronic diseases,
according to the institutions specialties.
We studied 90 patients but did not include newborns,
those patients who stayed in the PICU for <7 days, and
children whose parents did not provide free and informed
consent.
This study was approved by the Research and Ethics
Committee of Instituto da Criana and the Commission
for Analysis of Research Projects, Faculty of Medicine,
Universidade de So Paulo.

Nutrition Therapy
NT was initiated after hemodynamic stabilization and followed the approach determined by the NT team of
Instituto da Criana, summarized in Figure 1. The calories and nutrients (macronutrients and micronutrients)
required for parenteral or enteral feeding were calculated
daily. Increases were made according to feeding tolerance
and always aimed to meet the nutrition requirements of
each individual patient.

Monitoring of complications was performed during


the period of the NT, and nutrition status was evaluated
weekly.

Anthropometric Nutrition Assessment


Anthropometric nutrition assessment was carried out in
the first 24 hours of admission and repeated a week later.
To minimize the possibility of errors, all measurements
were carried out by the main author (PZ) of the study.
The assessment included weight (W), height (H) or
length (L), arm circumference (AC), and triceps skinfold
thickness (TST), according to the standards proposed by
Frisancho.17,18
We measured W with a scale that was calibrated for
accuracy before each use. Children who weighed >16 kg
were weighed standing, and infants were weighed using a
scale accurate to 5 g. Children who could not be weighed
independently were held by an adult (a parent or evaluator)
while being weighed. The childs weight was obtained by
subtracting the weight of the adult from the total weight of
the child and adult. L was measured in children aged 3 years
or younger using a pediatric anthropometer with an accuracy of 0.1 cm. Children were supine for the measurement.
In children older than 3 years, H was measured
using a wooden stadimeter with an accuracy of 0.1 cm.
In children whose condition prevented the use of conventional measuring techniques (eg, those patients who
were mechanically ventilated or taking vasoactive drugs),
H was predicted from measurements of the distance
between the knee and ankle with the child kept in the
supine position. The length between the heel and the
anterior surface of the leg at the knee (femoral condyle)
was measured with a pediatric anthropometer. There
were the following equations proposed by Chumlea
et al19 in 1994:
White girls = 43.21cm + (2.15cm distance knee / ankle)
Black girls = 46.59cm + (2.02cm distance knee / ankle)
White boys = 40.54cm + (2.22cm distance knee / ankle)
Black boys = 39.60cm + (2.18cm distance knee / ankle)
Using the data for W and H or L, we obtained the
following indices: W/age (A), H/A or L/A, W/H or W/L.
We calculated body mass index for age (BMI/A) with the
following equation: BMI/A = W (kg)/H2 (m).
AC was measured with a metric tape marked in 0.5cm increments. Measurements were taken at the midpoint of the distance between the acromion and the
olecranon with the arm extended along the body.
TST was obtained using a Lange skinfold caliper
(Cambridge Scientific Industries, Cambridge, MD) with
constant pressure of 10 g/mm2 on the contact surface.
The measurement was taken on the back of the arm,

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Nutrition Therapy in Pediatric Intensive Care / Zamberlan et al 525

Nutrition assessment

NT

Is gastrointestinal tract
functioning?

No?

Yes?

EN

EN + PN

PN

Complete polymeric diet by


polyurethane or silicone
NGT

Intermittently every 3 or 4
hours
Gastric residue
(>50% of the volume infused),
abdominal distension,
vomiting, diarrhea

Failure 3 consecutive
times?

Medical
assessment

Continuous infusion 18 or
24 hours
Failure with
continuous infusion?

Tube placed in postpyloric


position; complete oligomers
diet
Failure?

PN

Figure 1. NT flow chart of Instituto da Criana, Hospital das Clnicas, Universidade de So Paulo, Brazil. EN, enteral nutrition;
NGT, nasogastric tube; NT, nutrition therapy; PN, parenteral nutrition.

parallel to the longitudinal axis, at the midpoint between


the acromion and olecranon. We used the average of 3
consecutive measurements.
Arm muscle circumference (AMC) and arm muscle
area (AMA) were calculated from the values of AC and
TST with the following equations: AMC (cm) = AC
(TSTx); AMA (cm2) = AMC2/4.

Nutrition status was determined from the z score for the


following indices: W/A, H/A or L/A, W/H or W/L, BMI/A,
AC/A, and AC/H. We used reference values from the
National Center for Health Statistics (NCHS)20 for children
older than 5 years and from the World Health Organization
(WHO)21 for children younger than 5 years old. EPI
Info, 2000 and WHO Anthro, 2006 were used for the

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526 Journal of Parenteral and Enteral Nutrition / Vol. 35, No. 4, July 2011

13 (14%)

36 (41%)

Table 2. Frequency of Malnutrition on Admission to


the Pediatric Intensive Care Unit (n = 90)a
Indicator

20 (22%)
21 (23%)

<2 years
2 to <5 years
5 to <10 years
10 to 20 years

Figure 2. Distribution of children (n = 90) assessed in the


pediatric intensive care unit (by age).

H/A or L/A
W/A
W/H or W/L
BMI/A
AC/A
TST
AMC
AMA

Cutoff Point

- 2 dp
- 2 dp
- 2 dp
- 2 dp
- 2 dp
p5
p5
p5

% Patients
50.0
27.7
8.0
13.3
47.8
33.0
46.6
45.5

A, age; AC, arm circumference; AMA, arm muscle area; AMC,


arm muscle circumference; BMI, body mass index; H, height; L,
length; TST, triceps skinfold thickness; W, weight.
a
According to various anthropometric indicators used in the
screening.

Table 1. Reasons for Hospitalization


Cause

n (%)

Sepsis or septic shock


Infection without sepsis
Postliver transplant
Postoperative
Respiratory failure
Epilepsy
Other, eg, Oncologic disease and dialytic
severe renal dysfunction
Total

22
20
11
9
5
1
22

(24.5)
(22.2)
(12.2)
(10.0)
(5.5)
(1.1)
(24.5)

90 (100.0)

calculations. TST, AMC, and AMA were classified by percentiles, according to the method of Frisancho.18

Statistical Analysis
The results were tabulated in an Excel (v 6.0; Microsoft,
Redmond, Washington) spreadsheet. The mean and standard deviation (SD) z scores were obtained for all anthropometric indicators (W/A, H/A or L/A, W/H, BMI/A,
AC/A, AC/H or AC/L, TST, AMC, and AMA) and for calories and protein.
To identify changes in anthropometric indicators over
time, we used the paired Student t test to perform comparative analyses between admission and the seventh day
of hospitalization. Data were considered statistically significant at P < .05, and a 95% confidence interval was
used for measures of central tendency.
We used SPSS Statistical Software (version 12.01;
SPSS Inc, Chicago, IL) to perform the calculations.

Results
Subjects
The study population consisted of 90 patients whose
median age was 35.5 months (2.9 years). The majority of

Figure 3. Types of nutrition therapy (NT) used during hospitalization in the pediatric intensive care unit. EN, enteral nutrition; PN, parenteral nutrition.

Oral
Ngt
Postpyloric Tube

Figure 4. Routes of enteral nutrition administration during


hospitalization in the pediatric intensive care unit. NGT,
nasogastric tube.

patients were younger than 2 years (Figure 2). There were


no statistically significant differences regarding gender
(46 females, 44 males).
During hospitalization in the PICU, 18 deaths
occurred, which corresponded to 20% of the cases. The

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Nutrition Therapy in Pediatric Intensive Care / Zamberlan et al 527

Table 3. Anthropometric Indicators (Means) on


Admission and on Day 7 of Hospitalization
Indicator

Admission

z W/A
z BMI/A
z AC/H
TST, mm
AMC, cm
AMA, cm2

0.95
0.43
1.37
9.2
12.5
13.2

Day 7 of Hospitalization
1.12
0.26
1.89
8.0
12.3
13.0

P
.152
.310
<.001a
<.001a
.221
.352

A, age; AC, arm circumference; AMA, arm muscle area; AMC,


arm muscle circumference; BMI, body mass index; H, height;
TST, triceps skinfold thickness; W, weight; z, z score.
a
Statistically significant (p < .05).

reasons for hospitalization in the PICU are shown in


Table 1. Of the 90 patients, 81 (90%) had an ailment. The
median length of stay in the PICU was 11 days.
Table 2 shows the frequency of malnutrition in 90
children admitted to the PICU, as determined by the
anthropometric indicators used in the screening.

Nutrition Therapy
Following hospitalization NT was started an average of 72
hours after hemodynamic stabilization. The sequential
nutrition assessment occurred on the seventh day of hospitalization, and most children (80%) had received EN; in
>50% of the EN recipients, the gastric route was used,
(Figures 3 and 4). Intermittent administration predominated, and only 1 child received continuous infusion. In
5% of the patients, the enteral tube was placed in the
duodenum because of the persistence of gastric residue
and/or abdominal distension; this procedure followed the
protocol of the NT team of Instituto da Criana, as previously described.
Among children who were prescribed oral diets, more
than half received no dietary restriction of nutrients, and
35% received a sodium-restricted diet, which was used
before hospitalization. The vast majority of patients admitted
to this tertiary PICU presented with an underlying disease
that required dietary restriction of nutrients (eg, sodium).
We chose a complete polymeric diet appropriate for
each age group, as suggested by the Dietary Reference
Intake (DRI) guidelines22; we administered these formulas via nasogastric tube. For postpyloric feeding, we chose
a complete oligomeric diet with a caloric density of 0.7
kcal/mL and 2 to 3 g of protein per 100 mL.
The average calorie and protein supply, with a week
of admission and during the course of therapy, corresponded to 82 kcal/kg/d (47 kcal/kg/d) and 2.7 g/kg/d
(1.9 g/kg/d), respectively, and the ratio of protein nitrogen to calories was 1:160. PN was used for 10% of the
children. In general, the volume and composition of the

PN formula met the macronutrient and micronutrient


recommendations suggested by the DRI.22

Sequential Anthropometric Nutrition Assessment


The comparative analysis (paired t test) between the
initial assessment (admission) and the seventh day of
hospitalization shows that there was a statistically significant difference in the z score mean of AC/H and in
the absolute average of TST (Table 3).

Discussion
Having a greater need for nutrients and limited energy
reserves will increase a childs risk of developing nutrition
deficiencies. This risk is especially high in critically ill children. Metabolic stress and an inadequate supply of nutrients
can result in malnutrition.7,23 Thus, assessment, monitoring,
and NT are of utmost importance in caring for these patients.
When we analyzed the characteristics of our study
population, we found no differences in gender and a predominance of children younger than 2 years of age, with
a median age of 2.9 years. Most children and adolescents
presented with an ailment. The PICU of Instituto da
Criana is considered tertiary and cares for children aged
2 months to 18 years, mainly those who are followed at
specialty clinics. The heterogeneity of this study population in terms of age and medical condition was acknowledged in Delgado et al,3 who studied the same population,
and by Alievi et al,24 who studied children in a PICU tertiary in Porto Alegre, Brazil.
Several studies have reported ICU mortality rates
between 9% and 38%,25,26 which are consistent with our
observed mortality rate of 20%.
In a study of the nutrition status of children in a tertiary, pediatric, neonatal ICU in the Netherlands, Hulst
et al1 reported that the nutrition status of their study participants was worse than that of the general population.
In this study, 24% of children were malnourished, and the
authors concluded that a considerable number of patients
required specialized NT during hospitalization in the
ICU. These characteristics were similar to those found in
our study. The high prevalence of malnutrition (H/A or
L/A = 50%, W/A = 27.7%, BMI/A = 13.3%, AC/A =
47.8%) among children and adolescents admitted to the
PICU could be explained by the high incidence of ailments (90%). In studies conducted in the 1980s, Pollack
et al27,28 found malnutrition rates ranging from 32% to
37% in patients with acute and chronic illnesses. In addition, Leite et al29 found 65% of their patients were malnourished, most of whom were recovering from cardiac
surgery. By comparing our results with theirs, we concluded that malnutrition in the PICU, as assessed by
anthropometry, has been present for the last 20 years and
is still very prevalent in these units. It is known that in

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528 Journal of Parenteral and Enteral Nutrition / Vol. 35, No. 4, July 2011

critically ill patients, anthropometric assessment is difficult to interpret because the measurements may be influenced by factors caused by disease or trauma, (eg, fluid
retention and swelling). However, the consensus is that
this assessment is very important for the nutrition evaluation and monitoring of patients in the PICU.1,3
Nutrition depletion is associated with physiologic
instability and an increased need for care in critically ill
children, and it could have a negative impact on growth
and neurologic development, especially in younger children. NT in the PICU is a challenge because it is common
to restrict liquids and discontinue feeding for diagnostic
and therapeutic procedures and also because some patients
have digestive intolerance.30 Nutrition intervention is
essential, and most PICUs should develop their own protocols and multidisciplinary teams for providing nutrition
support. In 2002, the American Society for Parenteral and
Enteral Nutrition updated guidelines for EN and PN
therapy, including strategies for critically ill children, such
as the following recommendations: nutrition assessment,
indirect calorimetry, predictive equations to avoid overfeeding, and administration of EN and PN.
EN has been the method of choice for NT in critically
ill patients. EN maintains the integrity of the intestinal
mucosa, thereby limiting bacterial translocation and
reducing the risk of sepsis; in addition, EN improves protein metabolism and caloric deficit.7 In general, EN is
safe and well tolerated by critically ill children, even those
who receive vasoactive drugs, which can reduce intestinal
perfusion.32,33 In our study, 80% of the patients received
EN, which was administered according to the PICUs NT
protocol. Since 2005, this EN protocol has enforced the
early use of NT that is specific for the clinical condition
of the patient. Although most patients received NT within
72 hours of hospitalization, others were treated later.
For most critically ill patients who receive EN, the
stomach is a more physiologic route, and tube placement
is simple and fast.34 However, some authors have documented that a nasogastric tube is not tolerated as well as a
postpyloric tube, particularly in patients who are being
mechanically ventilated; these patients often have reduced
gastric motility secondary to the administration of drugs
and the accumulation of gastric residue.35,36 Thus, a high
percentage of these children cannot receive adequate
nutrition, especially as a result of the frequent interruptions in EN.34 Postpyloric EN is an alternative because it
reduces the volume of gastric residue and the number of
interruptions in feeding.36,37 Because transpyloric EN
reduces gastric residue, it should also reduce the risk of
pulmonary aspiration and aspiration pneumonia. However,
this effect has not been observed. Meert et al32 found that
children with transpyloric EN achieved a higher caloric
intake than did those with gastric EN, but the incidence of
complications from gastric and pulmonary aspiration was
similar in both groups. In our study, a nasogastric tube was
used in 60% of children who received EN. Although most

patients were fasting when admitted to the hospital, they


received adequate nutrition support at the end of first
week, with an average energy intake of 82 kcal/kg/d and an
average protein intake of 2.7 g/kg/d. The patients clinical
condition was decisive in determining caloric requirements; however, there is always concern regarding hospital
malnutrition, which is a very important aspect for the
recovery of the patients. Moreover, these patients generally
have a deficient diet at home; their intake is influenced by
the clinical and nutrition aspects of the disease.
Only 5% of the patients required postpyloric EN because
of persistent gastric residues and/or abdominal distension. A
large proportion of critically ill patients receive gastric EN by
continuous infusion; this form of administration improves
feeding tolerance, reduces the gastric residual volume, and
thereby reduces the risk of aspiration. However, a recent
study found the same incidence of complications in patients
with continuous and intermittent EN. We used a form of
intermittent administration in most cases.
Compared with EN, the main disadvantage of PN is
the risk of infectious complications. In a group of 500
critically ill children evaluated prospectively, PN was
associated with an increased risk of infections.38 However,
in PICU patients who are unable to receive or tolerate
EN, PN should be indicated.6 In our study, 10% of the
children were unable to tolerate EN, and PN was indicated. To improve nutrition support, a mixed NT was
prescribed for 10% of the patients.
NT monitoring was performed by a sequential anthropometric assessment. We found a statistically significant
difference in H/A during hospitalization, and we believe
that this finding was caused by a potential measurement
error when there was a higher technical difficulty in
obtaining the L/H.
Metabolic stress causes intense proteolysis that
involves a large loss of muscle. In anthropometry, measurements of the arm, including AMC and AMA, are able
to estimate changes in the bodys protein stores. It is possible that critically ill patients exhibit decreased values of
these indicators during hospitalization in an ICU. In this
study, there was a statistically significant change in absolute average of TST and z score mean of AC/H, but we did
not observe a significant change in the median AMC or
AMA. However, it is difficult to determine whether
changes in nutrition status have taken place, because
anthropometric measurements can be influenced by
many factors, (eg, fluid shifts) in addition, 1 week of hospitalization is not necessarily long enough for significant
alterations to occur. Even so, anthropometric evaluation,
including nutrition assessment, is still important for a
critically ill patient. Delgado et al39 obtained similar findings, also justified by the short hospitalization time
(around 7 days) of these patients in an ICU. Furthermore,
although our study was descriptive, we observed that early
administration of NT was appropriate and possibly helped
our study participants maintain their nutrition status.

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Nutrition Therapy in Pediatric Intensive Care / Zamberlan et al 529

In summary, our data show that malnutrition is


prevalent in critically ill children. Nutrition intervention
in children, guided by a multidisciplinary team and nutrition support protocols and monitored by anthropometric
assessment, may help reduce nutrition deficits during
hospitalization in the PICU. It is possible to introduce
early gastric EN, and PN should be indicated when the
digestive tract is not functioning or when EN alone is
unable to meet the nutrition demands of the patient.

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