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260
A.S.P.E.N. Clinical Guidelines / Mehta et al 261
Table 2
Nutrition Support Guideline Recommendations in the Critically Ill Child
# Guideline Recommendations Grade
1 1A) Children admitted with critical illnesses should undergo nutrition screening to identify those with existing D
malnutrition and those who are nutritionally-at-risk.
1B) A formal nutrition assessment with the development of a nutrition care plan should be required, especially in E
those children with premorbid malnutrition.
2 2A) Energy expenditure should be assessed throughout the course of illness to determine the energy needs of D
critically ill children. Estimates of energy expenditure using available standard equations are often unreliable.
2B) In a subgroup of patients with suspected metabolic alterations or malnutrition, accurate measurement of E
energy expenditure using indirect calorimetry (IC) is desirable. If IC is not feasible or available, initial energy
provision may be based on published formulas or nomograms. Attention to imbalance between energy intake
and expenditure will help to prevent overfeeding and underfeeding in this population.
3 There are insufficient data to make evidence-based recommendations for macronutrient intake in critically ill E
children. After determination of energy needs for the critically ill child, the rational partitioning of the major
substrates should be based upon understanding of protein metabolism and carbohydrate- and lipid-handling
during critical illness.
4 4A) In critically ill children with a functioning gastrointestinal tract, enteral nutrition (EN) should be the C
preferred mode of nutrient provision, if tolerated.
4B) A variety of barriers to EN exist in the pediatric intensive care unit (PICU) Clinicians must identify and D
prevent avoidable interruptions to EN in critically ill children.
4C) There are insufficient data to recommend the appropriate site (gastric vs post-pyloric/transpyloric) for enteral C
feeding in critically ill children. Post-pyloric or transpyloric feeding may improve caloric intake when compared
to gastric feeds. Post-pyloric feeding may be considered in children at high risk of aspiration or those who have
failed a trial of gastric feeding.
5 Based on the available pediatric data, the routine use of immunonutrition or immune-enhancing diets/nutrients D
in critically ill children is not recommended.
6 A specialized nutrition support team in the PICU and aggressive feeding protocols may enhance the overall E
delivery of nutrition, with shorter time to goal nutrition, increased delivery of EN, and decreased use of
parenteral nutrition. The affect of these strategies on patient outcomes has not been demonstrated.
and morbidity.4,5 Children admitted to the PICU are fur- and resting energy expenditure (REE). Albumin, which
ther at risk of longstanding altered nutrition status and has a large pool and much longer half-life (14-20 days), is
anthropometric changes that may be associated with mor- not indicative of the immediate nutrition status. Indepen
bidity.13 Hulst et al observed a correlation between energy dently of nutrition status, serum albumin concentrations
deficits and deterioration in anthropometric parameters may be affected by albumin infusion, dehydration, sepsis,
such as mid-arm circumference and weight in a mixed trauma, and liver disease. Thus, its reliability as a marker
population of critically ill children.13 These anthropo- of visceral protein status is questionable. Prealbumin
metric abnormalities accrued during the PICU admis (also known as transthyretin or thyroxine-binding preal-
sion returned to normal by 6 months after discharge.1 bumin) is a stable circulating glycoprotein synthesized in
Using reproducible anthropometric measures, Leite et al the liver. It binds with retinol binding-protein and is
reported a 65% prevalence of malnutrition on admission involved in the transport of thyroxine as well as retinol.
with increased mortality in this group.5 On follow up, a Prealbumin, so named by its proximity to albumin on an
significant portion of these children had further deterio- electrophoretic strip, has a half-life of 24-48 hours.
ration in nutrition status (Table 3). Nutrition assessment Prealbumin serum concentration is diminished in liver
of children during the course of critical illness is desirable disease and may be falsely elevated in renal failure.
and can be quantitatively assessed by routine anthropo- Prealbumin is readily measured in most hospitals and is a
metric measurements. Routine monitoring of weight is a good marker for the visceral protein pool.14,15 Visceral
valuable index of nutrition status in critically ill children. proteins such as albumin and prealbumin do not accu-
However, weight changes and other anthropometric rately reflect nutrition status and response to nutrition
measurements during the PICU admission should be intervention during inflammation. In children with burn
interpreted in the context of fluid therapy, other causes injury, serum acute-phase protein levels rise within 12–24
of volume overload, and diuresis. Nutrition assessment hours of the stress, because of hepatic reprioritization
can also be achieved by measuring the nitrogen balance of protein synthesis in response to injury.16 The rise is
A.S.P.E.N. Clinical Guidelines / Mehta et al 263
Table 3
Anthropometric Changes During Pediatric Critical Illness and Role of Nutrition Assessment
Study Population
Year Intervention Sample Clinical Outcome
Grade Outcome Measured Size Results Comments
Hulst Children in a multidisciplinary N = 261 Mean Energy deficits (over a Mixed population.
et al1,13 ICU maximum of 14 days) were Negative energy and protein
2004 a) Total actual intakes of calories 27 kcal/kg—Preterm neonates balance in this population
Level III and protein were recorded. 20 kcal/kg—Term neonates correlated with decreasing
Balance was calculated by sub- 12 kcal/kg—Older children anthropometric parameters.
tracting actual intake from RDA, Mean Protein deficits: A 14-day period of monitoring
over a maximum of 14 days. 0.6 g/kg/day—Preterm may not be adequate for
Relations between balance and 0.3 g/kg/day—Term Newborns anthropometric changes.
clinical factors and change in 0.2 g/kg/day—Children Energy balance was
anthropometry Cumulative deficits—related to calculated from estimates of
b) Patients were also followed up decrease in weight and arm RDA and not measured by
to 6 months for anthropometric circumference SD-scores. indirect calorimetry.
parameters. Negative correlation with age, At 6 months follow up, almost
length of stay in the ICU and all children had recovered
duration of mechanical their nutrition status.
ventilator support.
Hulst et al18 Children in a multidisciplinary N = 105 Prevalence of hypomagnesemia, Except for uremia, no
2006 PICU hypertriglyceridemia, uremia significant association was
Level III Serum urea, albumin, triglycerides and hypoalbuminemia were found between
and magnesium were measured 20%, 25%, 30% and 52%, abnormalities in
in 105 children (age, 7 days to respectively, with no significant biochemical parameters and
16 years) within the first 24 associations between the changes in SD scores of
hours after admission. different disorders. anthropometric
Association with anthropometric measurements.
outcomes parameters
Leite et al5 PICU N = 46 65% of the patients presented with A significant number of
1993 Anthropometry at admission and indices of malnutrition. Of patients are nutritionally-at-
Level III follow-up these, chronic malnutrition was risk at the time of hospital
predominant. admission, and there is an
Mortality was higher in association between
malnourished individuals (20% nutrition status and hospital
vs 12.5%). course.
36% of patients showed a decrease The anthropometric nutrition
in weight-for-height on follow evaluation is a simple,
up. reproducible and objective
tool for nutrition
assessment of the critically
ill child.
ICU, intensive care unit; PICU, pediatric intensive care unit; RDA, recommended daily allowance; SD, standard deviation.
Overfeeding may also impair liver function by inducing feeding in a select group of chronically ill children at high
steatosis and cholestasis, and increase the risk of infection risk of obesity is currently sporadic. In general, the energy
secondary to hyperglycemia. Hyperglycemia associated goals should be assessed and reviewed regularly in
with caloric overfeeding has been associated with critically ill children.
prolonged mechanical ventilator requirement and PICU Table 4 summarizes studies examining the performance
LOS.27 The use of the respiratory quotient (RQ) as a of estimated energy needs in relation to measured REE in
measure of substrate use in individual children cannot be critically ill children requiring mechanical ventilator
recommended. However, a combination of acute phase support. In general, these small sized, prospective or
proteins (CRP) and RQ may reflect transition from the retrospective cohort studies demonstrate the variability of
catabolic hypermetabolic to the anabolic state. There are the metabolic state and the uniform failure of estimated
no data in general pediatric populations for the role of energy needs in accurately predicting the measured REE
hypocaloric feeding. The application of hypocaloric in critically ill children. In the absence of REE, some
A.S.P.E.N. Clinical Guidelines / Mehta et al 265
Table 4
Estimated Energy Expenditure vs Measured Resting Energy Expenditure (REE)
Study Population
Year Intervention Clinical Outcome
Grade Outcome Measures Sample Size Results Comments
De Klerk Children needing > 24 hours of N = 18 Variability in total daily energy Single measurement
et al28 mechanical ventilator support expenditure appears to accurately
2002 in a PICU (40-64 kcal/kg/d) reflect total daily energy
Level III Serial measured REE CV was < 10% requirement.
Respiratory Quotient (RQ) Positive energy balance in Results of this study do not
Energy balance = actual energy many children (n=8) suggest the need for
intake – total energy [Average RQ in this group was serial REE.
expenditure 0.89] RQ was marginally affected
Negative balance (n=10) by energy balance.
[Average RQ in this group was
0.84]
White et al29 Mechanically ventilated children N = 11 30-minute REE Small numbers. No
1999 in the PICU CV was 7.2% ± 4.5% correlation examined
Level III 24 h indirect calorimetry 30-min vs 24 h: no difference with clinical state.
measurement (P < 0.69) 30-minute REE accurately
30 minute steady state REE No diurnal variation represented the 24-h
compared to 24-h total energy Between-day CV = 21% ± 16% values.
expenditure The authors recommend
Daily CV in measured REE was serial REE measure-
calculated ments based on signi-
ficant between-day CV.
White et al30 Mechanically ventilated children N = 100 A new equation for estimated The authors concluded
2000 in a PICU (derivation) REE was derived, that there is no
Level III Clinical variables N = 25 incorporating age, weight, substitute for measured
REE by indirect calorimetry (validation) temperature, days in the REE.
PICU, and disease. Their derived equation
performed better than
existing standard
equations.
Derumeaux- Obese children N = 471 REE equation using fat-free Special equations may be
Burel BMI z score ≥ 2 (derivation) mass was more accurate than necessary for obese
et al31 Measured REE N = 211 weight-based equations children.
2004 Fat free mass—obtained by (validation) Body composition is an
Level III bioelectric impedance important factor in REE.
assessment Measured REE is ideal.
Predicted equations
Mlcak et al32 Children < 18 years with total N = 100 (40 REE was expressed in 3 Increased REE persisted
2006 body surface area burn > 40%, female) different ways: actual REE in for over 12 months after
Level III and consent to return at 6, 9, kcal per day, percent of burn injury.
and 12 months for post-burn predicted REE, and actual
follow up REE divided by the BMI.
Measured REE vs Harris- Hypermetabolism persisted 12
Benedict equation and months after burn injury.
corrected by BMI Female children exerted a
REE measurements were decreased hypermetabolic
repeated at 6, 9, and 12 response compared with
months post-burn when the male children.
patients returned for
outpatient surgery.
(continued)
266 Journal of Parenteral and Enteral Nutrition / Vol. 33, No. 3, May/June 2009
Table 4 (continued)
Study Population
Year Intervention Clinical Outcome
Grade Outcome Measures Sample Size Results Comments
underfeeding in selected subjects, and the cost-benefit response. This allows for maximal physiologic adaptability
analyses of its application in the PICU are desirable. The at times of injury or illness. Although children with criti-
effect of energy intake on outcomes needs to be examined cal illness have increases in both whole-body protein
in pediatric populations especially in those on the extremes degradation and whole-body protein synthesis, it is the
of body mass index (BMI). former that predominates during the stress response.
Thus, these patients manifest net negative protein and
nitrogen balance characterized by skeletal muscle wast-
Appendix 1
ing, weight loss, and immune dysfunction. The catabo-
Children at high risk for metabolic alterations who lism of muscle protein to generate glucose and
are suggested candidates for targeted measurement of inflammatory response proteins is an excellent short-term
REE in the PICU include the following: adaptation, but it is ultimately limited because of the
reduced protein reserves available in children and neo-
• Underweight (BMI < 5th percentile for age), at risk nates. Unlike during starvation, the provision of dietary
of overweight (BMI > 85th percentile for age) or carbohydrate alone is ineffective in reducing the endoge-
overweight (BMI > 95th percentile for age) nous glucose production via gluconeogenesis in the
• Children with > 10% weight gain or loss during metabolically stressed state.35 Therefore, without elimina-
ICU stay
tion of the inciting stress for catabolism (ie, the critical
• Failure to consistently meet prescribed caloric goals
• Failure to wean, or need to escalate respiratory
illness or injury), the progressive breakdown of muscle
support mass from critical organs results in loss of diaphragmatic
• Need for muscle relaxants for > 7 days and intercostal muscle (leading to respiratory compro-
• Neurologic trauma (traumatic, hypoxic and/or isch- mise), and to the loss of cardiac muscle. The amount of
emic) with evidence of dysautonomia protein required to optimally enhance protein accretion is
• Oncologic diagnoses (including children with stem higher in critically ill than in healthy children. Infants
cell or bone marrow transplant) demonstrate 25% higher protein degradation after surgery
• Children with thermal injury and a 100% increase in urinary nitrogen excretion with
• Children requiring mechanical ventilator support bacterial sepsis.36,37 The provision of dietary protein suf-
for > 7 days ficient to optimize protein synthesis, facilitate wound
• Children suspected to be severely hypermetabolic
healing and the inflammatory response, and preserve
(status epilepticus, hyperthermia, systemic inflam-
matory response syndrome, dysautonomic storms,
skeletal muscle protein mass is the most important nutri-
etc) or hypometabolic (hypothermia, hypothyroid- tion intervention in critically ill children. The quantities
ism, pentobarbital or midazolam coma, etc.) of protein recommended for critically ill neonates and
• Any patient with ICU LOS > 4 weeks may benefit children are based on limited data. Certain severely
from IC to assess adequacy of nutrient intake. stressed states, such as significant burn injury, may
require additional protein supplementation to meet meta-
bolic demands. Excessive protein administration should
3. Macronutrient Intake During Critical Illness be avoided as toxicity has been documented, particularly
There are insufficient data to make evidence- in children with marginal renal and hepatic function.
based recommendations for macronutrient Studies using high protein allotments of 4–6 g/kg/day
intake in critically ill children. After determi- have been associated with adverse effects such as azotemia,
nation of energy needs for the critically ill metabolic acidosis, and neurodevelopmental abnormali-
child, the rational partitioning of the major ties.38 A similar evaluation of the effects of high protein
substrates should be based upon basic under- administration using newer formulas is desirable. Although
standing of protein metabolism and carbohy- the precise amino acid composition to best increase
drate- and lipid-handling during critical illness. whole-body protein balance has yet to be fully deter-
Grade E mined, stable isotope techniques now exist to study this
issue. Estimated protein requirements for injured
children of various age groups are as follows: 0–2 years,
Rationale
2–3 g/kg/day; 2–13 years, 1.5–2 g/kg/day; and 13–18
Critical illness and recovery from trauma or surgery are years, 1.5 g/kg/day.
characterized by increased protein catabolism and turn- Once protein needs have been met, safe caloric provi
over. An advantage of high protein turnover is that a con- sions using carbohydrate and lipid energy sources have
tinuous flow of amino acids is available for synthesis of similar beneficial effects on net protein synthesis and
new proteins. Specifically, this process involves a redistri- overall protein balance in critically ill patients. Glucose is
bution of amino acids from skeletal muscle to the liver, the primary energy used by the brain, erythrocyte, and
wound, and other tissues involved in the inflammatory renal medulla and is useful in the repair of injured tissue.
268 Journal of Parenteral and Enteral Nutrition / Vol. 33, No. 3, May/June 2009
Glycogen stores are limited and quickly depleted in illness generally restricted to a maximum of 30%–40% of total
or injury, resulting in the need for gluconeogenesis. In calories, although this practice has not been validated by
injured and septic adults, a 3-fold increase in glucose clinical trials.
turnover and oxidation has been demonstrated as well as
an elevation in gluconeogenesis. A significant feature of
4. Route of Nutrient Intake (Enteral Nutrition)
the metabolic stress response is that the provision of
dietary glucose does not halt gluconeogenesis. Conse 4A) In critically ill children with a functioning
quently, the catabolism of muscle protein to produce gastrointestinal tract, enteral nutrition (EN)
glucose continues unabated, and attempts to provide should be the preferred mode of nutrient pro-
large carbohydrate intake in critically ill patients have vision, if tolerated. Grade C
been abandoned. 4B) A variety of barriers to EN exist in the PICU.
The Surviving Sepsis Campaign has recommended Clinicians must identify and prevent avoidable
tight glucose control in critically ill adults based on interruptions to EN in critically ill children.
results of a single trial that showed decreased mortality in Grade D
critically ill adults randomized to this strategy. Subsequent 4C) There are insufficient data to recommend
studies examining the role of strict glycemic control in the appropriate site (gastric vs post-pyloric/
adults have yielded conflicting results and the incidence transpyloric) for enteral feeding in critically ill
of hypoglycemia in these studies is concerning.39 children. Post-pyloric or transpyloric feeds
Hyperglycemia is prevalent in critically ill children and may improve caloric intake when compared to
has been associated with poor outcomes in retrospective gastric feeds. Post-pyloric feeding may be con-
studies.27,40,41 The etiology of hyperglycemia during the sidered in children at high risk of aspiration or
stress response is multifactorial. Despite the prevalence those who have failed a trial of gastric feeding.
of hyperglycemia in the pediatric intensive care population, Grade C
no data exist currently evaluating the effects of tight
glycemic control in the pediatric age group. Both
Rationale
hypoglycemia and glucose variability also are associated
with increased LOS and mortality, and hence are Following the determination of energy expenditure and
undesirable in the critically ill child.42 In the absence of requirement in the critically ill child, the next challenge is to
definitive data, aggressive glycemic control cannot be select the appropriate route for delivery of nutrients. In the
recommended as yet in the critically ill child. critically ill child with a functioning gastrointestinal tract,
Lipid turnover is generally accelerated by critical the enteral route is preferable to parenteral nutrition (PN).
illness, surgery, and trauma.43 Recently, it has been EN has been shown to be more cost-effective without the
shown that critically ill children do, indeed, have a added risk of nosocomial infection inherent with PN.47,48
higher rate of fat oxidation.44 Thus, this suggests that However, the optimal route of nutrient delivery has not been
fatty acids are, in fact, the prime source of energy in systematically studied in children and there is no RCT com-
metabolically stressed children. Because of the increased paring the effects of EN vs PN. Current practice in many
demand for lipid use in critical illness coupled with the centers includes the initiation of gastric or post-pyloric
limited fat stores in the pediatric patient, critically ill enteral feeding within 48-72 hours after admission. PN is
children are susceptible to the evolution of biochemically being used to supplement or replace EN in those patients
detected essential fatty acid deficiency if administered a where EN alone is unable to meet the nutrition goal.
fat-free diet.45 Clinically, this syndrome presents as In children fed with EN, there are insufficient data to
dermatitis, alopecia, thrombocytopenia, and increased make recommendations regarding the site of enteral
susceptibility to bacterial infection. To avoid essential feeding (gastric vs post-pyloric). Meert et al examined the
fatty acid deficiency in critically ill or injured infants, role of small bowel feeding in 74 critically ill children,
the allotment of linoleic and linolenic acid is randomized to receive either gastric or post-pyloric
recommended at concentrations of 4.5% and 0.5% of nutrition.49 The study was not powered to detect
total calories, respectively. The provision of commercially differences in mortality. EN was interrupted in a large
available intravenous fat emulsions (IVFE) to parenterally number of subjects in this study and caloric goals were
fed critically ill children reduces the risk of essential met in a small percentage of the population studied. This
fatty acid deficiency, results in improved protein use, unblinded RCT did not show difference in microaspiration,
and does not significantly increase CO2 production or enteral access device displacement, and feed intolerance
metabolic rate.46 Most centers, therefore, start IVFE between the gastric or post-pyloric fed groups. A higher
supplementation in critically ill children at 1 g/kg/day percentage of subjects in the small bowel group achieved
and advance over a period of days to 2-4 g/kg/day, with their daily caloric goal compared to the gastric fed group.
monitoring of triglyceride levels. IVFE administration is Sanchez et al report better tolerance in critically ill
A.S.P.E.N. Clinical Guidelines / Mehta et al 269
children receiving early (< 24 hours after PICU admission) population. Consistently underachieved EN goals are
vs late (started after 24 hrs) post-pyloric nutrition.50 Of thought to be one of the reasons for the absence of
the 526 children in their cohort who were deemed to have beneficial effect in multiple studies and meta-analysis of
intolerance to EN, 202 received early post-pyloric the efficacy of immunonutrition in preventing infection.56
nutrition and had decreased incidence of abdominal Awareness of these factors hindering the achievement of
distension. Despite evidence to suggest that it is reasonably EN goals is essential in order to address preventable
tolerated, the routine use of postpyloric feeding in the interruptions in enteral feeding in critically ill children.
critically ill child cannot be recommended. It may be There is not enough evidence to recommend the use of
prudent to consider this option in patients who do not prokinetic medications or motility agents (for EN
tolerate gastric feeding or those who are at a high risk of intolerance or to facilitate enteral access device
aspiration. Postpyloric or transpyloric feeding may be placement), prebiotics, probiotics, or synbiotics in
limited by the ability to obtain small bowel access, and critically ill children.
the expertise and resources in individual PICUs are likely
to be variable. A standardized approach to optimizing
Future Research
benefits and minimizing risks with EN delivery will help
clinicians identify patients who would benefit from small Future studies may be directed at examining methods to
bowel feeding. ensure optimal prescription and delivery of nutrient
Despite the absence of sound evidence to support the intake at the bedside, identifying and preventing common
superiority of one route of feeding over the other, the reasons for avoidable interruptions in nutrient intake,
enteral route has been successfully used for nutrition selection of children at risk of aspiration in the PICU,
support of the critically ill child.51-53 In another unblinded and the role of EN (gastric vs postpyloric feeds) in this
RCT, Horn et al randomized 45 children admitted to subgroup. The advantages of EN in terms of its role in gut
the PICU to receive gastric tube feeding either continu immunity, prevention of PN related complications and
ously or intermittently every 2 hours. The main outcome the cost benefit analysis when compared to PN require
measure examined in this study was tolerance of enteral further evaluation.
feedings. The small sample size and the short observation
period of < 66 hours makes any meaningful interpretation
5. Immunonutrition in the PICU
difficult. However, the number of daily stools, diarrheal
episodes, or vomiting episodes was similar between the 2 Based on the available pediatric data, the routine
groups. Intolerance to enteral feedings may limit intake use of immunonutrition or immune-enhancing
and supplementation with PN may be required. Prospective diets/nutrients in critically ill children is not
cohort studies and retrospective chart reviews have recommended. Grade D
reported the inability to achieve daily caloric goal in
critically ill children.54,55 The most common reasons for
Rationale
suboptimal enteral nutrient delivery in these studies are
fluid restriction, interruptions to EN for procedures, and The use of specific nutrients aimed at modulating the
EN intolerance due to hemodynamic instability. The inflammatory or immune response has been reported for
percent of estimated energy expenditure actually several years. Despite several RCTs employing immunonu
administered to these subjects was remarkably low. In a trition in critically ill patients, a positive treatment effect
study examining the endocrine and metabolic response of of immunonutrition or the use of immune-enhancing
children with meningococcal sepsis, goal nutrition was diets (IED) has not been demonstrated. These studies
achieved in only 25% of the cases.19 Similar observations are flawed by their poor methodology and small sample
have been made in a group of 95 children in a PICU size. The studies were conducted using a variety of nutri-
where patients received a median of 58.8% (range ents in combination that were administered to heteroge-
0%-277%) of their estimated energy requirements. In this neous patient populations. The studies do not allow
review, EN was interrupted on 264 occasions for clinical meaningful interpretation of the safety or efficacy of indi-
procedures. In another review of nutrition intake in 42 vidual nutrients and fail to detect significant differences
patients in a tertiary-level PICU over 458 ICU days, in relevant clinical outcomes. Arginine, glutamine, amin-
actual energy intake was compared with estimated energy opeptides, w-3 fatty acids and antioxidants are some of
requirement.55 Only 50% of patients were reported to the nutrients studied for their immune modulation effects.
have received full estimated energy requirements after a Systematic reviews of immunonutrition studies in adults
median of 7 days in the ICU. Protocols for feeding use of have cautioned against the use of arginine and other
transpyloric feeding tubes and changing from bolus to nutrients due to potential for harm in septic and critically
continuous EN during brief periods of intolerance are ill patients.59 Fish oils, borage oils, and antioxidants
strategies to achieve estimated energy goals in this may have a role in patients with acute respiratory distress
270 Journal of Parenteral and Enteral Nutrition / Vol. 33, No. 3, May/June 2009
Table 5
Clinical Outcomes Associated With Enteral Feeding
Study Population
Year Intervention Sample Clinical Outcome
Grade Outcome Measures Size Results Comments
Meert et al49 Critically ill children (<18yrs) in N = 74 Daily caloric goal achieved was Small number of patients
2004 a PICU significantly lower (p < 0.01) studied.
Level II RCT comparing gastric vs small in gastric group (30 ± 23%) vs Difficult to blind such a
bowel continuous tube feeds small bowel group (47 ± 22%). study at the bedside (due
Percentage of caloric goals Proportion of patients with to need for radiographic
achieved, pepsin positive microaspiration, tube confirmation of
tracheal secretions, and feed displacement, and EN placement of tip of
tolerance (vomiting, diarrhea intolerance were similar enteral access device).
or abdominal distension) were between the 2 groups. Fairly high number of
the main outcome variables. subjects in the study
experienced EN
interruptions and percent
of caloric goals met was
low in both groups.
Horn et al57 Children < 18y in a PICU with N = 45 Number of stools/d (1.5 vs 1.6), Small number of patients
2003 EN mean episodes of diarrhea/d studied.
Level II RCT comparing gastric EN (0.32 vs 0.64), mean number The duration of study was
administered either of vomiting episodes/person too small to detect
continuously or every 2 h (0.64 vs 0.22) were similar meaningful differences—
Tolerance—number and type of between the continuous and median 64.5 and 66
stools, diarrhea and vomiting intermittent gastric fed group. hours for the 2 groups.
De Oliveira Children in a PICU with N = 55 EN started on day 3 ± 1 and Energy requirements were
Iglesias EN ≥ 2 d maintained for 6 ± 3 d. 71% estimates and not
et al58 Required (estimates) vs received the required calories measured.
2007 prescribed vs. delivered calories (38% of which reached caloric Barriers to EN remain a
Level III were recorded. goal by d 5 of PICU significant challenge to
Variables associated with not admission). Daily average ensuring the delivery of
achieving caloric goals were caloric intake was 60% of prescribed calories to
recorded. required and 85% of patients in the PICU.
prescribed.
Barriers to EN were procedures,
clinical instability, use of
inotropic agents, enteral
access device displacement,
postoperative fasting, and
feeding intolerance
(abdominal distension,
vomiting, and diarrhea).
Sanchez Children over 10 years of age N = 526 Clinical characteristics, nutrients Retrospective cohort
et al50 admitted to a PICU were (202 were delivered and incidence of Children tolerate early
2007 eligible for transpyloric tube fed early) diarrhea were similar in both postpyloric feeds.
Level III placement if they were deemed groups.
to not tolerate enteral feedings Abdominal distension was less
within 24-48 hrs after frequent in early EN group
admission. (3.5%) vs late (7.8%); P < .05.
Tolerance of feeds was compared
between patients started on
transpyloric feeds early (< 24
hours after admission) vs those
started late (> 24 hrs)
Calories delivered, duration of
nutrition, abdominal distension
and diarrhea were recorded.
(continued)
A.S.P.E.N. Clinical Guidelines / Mehta et al 271
Table 5 (continued)
Study Population
Year Intervention Sample Clinical Outcome
Grade Outcome Measures Size Results Comments
Rogers Children admitted to a PICU N = 42 Patients received 37.7% (median) of PICU patients, especially
et al55 with length of stay >3 d (18 Cardiac their EER. cardiac surgical patients,
2003 and EN intake surgical) Cardiac surgical patients had lower do not receive their energy
Level III The proportion of patients caloric intake than others. goals. Fluid restriction in
reaching estimated energy Only 52% of the pts received full both groups is the major
requirement goals was energy intake goal at any time reason for inability to meet
recorded. during the PICU stay. Significant energy goals.
weight decrease was noted in Fasting for procedures and
cardiac surgical patients. EN interruptions due to
Major barrier to caloric intake—fluid intolerance were other
restriction barriers to nutrition in
Minor barriers—feed interruption this study.
for procedures and intolerance
Taylor Children admitted to PICU N = 95 59% were fed within 24 hours of Poor % energy intake goal
et al54 with length of stay ≥3 d admission. achieved with EN.
2003 Information on nutrition EN was administered 54% of time. Procedure-related feeding
Level III delivery was recorded. 10% received PN; 9.5% did not interruptions were
receive any nutrition support. significant.
PICU pts received 58.8%, median The study highlights the
(range 0–277%) of their energy need for a proactive
intake goal. approach to bridge the
Energy intake was greater when gap between desirable
supplemented by PN. and achieved nutrient
EN was interrupted 264 times intake.
(mainly for procedures).
For up to 75% of study time,
children had abnormal bowel
patterns. 79% were constipated for
3-21 days. And 43% had diarrhea
of unknown etiology.
EER, energy efficiency ratio; EN, enteral nutrition; PICU, pediatric intensive care unit; RCT, randomized controlled trial.
syndrome (ARDS). Glutamine may have beneficial effects Another small pilot RCT reported improved outcomes
in adults with burn injury and trauma. in children fed with a glutamine-enriched formulation,
The role of immune-enhancing EN in children during although the numbers are too small for meaningful
critical illness has not been extensively studied. Briassoulis conclusions.60 The use of a specialized adult immune
et al reported their results of a blinded RCT in children modulating enteral formula in pediatric burn victims has
admitted to the PICU with expected LOS and need for been associated with improvement in oxygenation and
mechanical ventilation of ≥ 5 d.22 EN was started in these pulmonary compliance in a retrospective review.61
patients within 12 h of admission to PICU. Patients were
randomized to receive either a formulation containing
Future Research
glutamine, arginine, w-3 fatty acids, and antioxidants or
standard age-appropriate formulation. Protocolized increase Future pediatric studies in this field must focus on exam-
in EN ensured that goal feeds were reached by day 4. The ining the effects of single (vs combination of) nutrients,
study did not show any outcome differences in the 25 in large (multicenter) trials, on homogeneous PICU
children in each arm, although authors report a trend populations designed to detect differences in important
toward a decrease in nosocomial infection rates and outcome measures. This approach will ensure that results
positive gastric aspirate culture rates in the treatment arm. allow meaningful inferences to be made about sound
The immunologically active formula used in this study was hypotheses on single immune modulating nutrients and
not specifically tailored for children and transient diarrhea will prevent the current absence of strong conclusions
was noted in children receiving this formula, which had despite a large amount of investment in this area of
a higher osmolarity compared to the control formula. research in adult ICU populations.
272 Journal of Parenteral and Enteral Nutrition / Vol. 33, No. 3, May/June 2009
Table 6
Immune-Enhancing Nutrients in Critically Ill Children
Study Population
Year Intervention Clinical Outcome
Grade Outcome Measures Sample Size Results Comments
Briassoulis Children admitted to the PICU, N = 50 Negative nitrogen balance noted on Mortality was not
et al22 with an expected LOS and (25 patients day 1 in both groups affected (but
2005 need for mechanical in each Increased serum osmolality, urea and sample size is
Level II ventilation of ≥ 5 d group) sodium in intervention group small). The trends
No renal disease, no chronic GI 64% patients with positive nitrogen in decreased
disease, or no PN balance in intervention vs 40% in nosocomial
EN started within 12 h of control group by day 5 infection and
admission Caloric intake was 120% predicted gastric cultures
Intervention group received the basal metabolic rate. are not
study formula providing No changes in mortality statistically
glutamine/arginine/ Decreasing trends in nosocomial significant.
antioxidants (Zn, vitamin E, b infection rates and positive gastric Formulation was not
carotene, copper, selenium) aspirate culture rates; P < .05. adapted to
and w-3 fatty acids Transient diarrhea, possibly due to children.
Masking of formulations increased osmolarity of study
Protocols for EN delivery: energy formulation
intake = 0.5, 1.1.25, 1.5 and
1.5 times predicted estimated
energy requirement on days 1,
2, 3, 4, and 5, respectively.
Thus, gradual increase in
intake with goal feeds to be
reached by day 4.
Note: energy intake was
predicted using FAO equations
with Schofield modifications
and with stress factors.
Barbosa Infants (1 m–2 y of age) N=9 Bacterial infections in 75% of placebo Very small study
et al60 admitted to PICU and 5 Glutamine (3/4) vs 20% in treatment group
1999 tolerating EN for at least 5 d 4 control Deaths: 2/4 in placebo and 0/5 in
Level V Diagnosis of sepsis/respiratory glutamine group
failure Duration of mechanical ventilation,
Exclusions: shock, multiple LOS in ICU and hospital were
organ failure, AIDS, HIV similar in both groups.
positivity, immunosuppressant
drugs, cancer, chemotherapy,
recent surgery, diabetes
mellitus, hepatic or renal
failure
2 groups randomized to receive
glutamine (commercial EN
formulation), casein + semi-
elemental formulation
100 kcal/kg/d and 3 g protein/
kg/d
AIDS, Acquired immune deficiency syndrome; FAO, Food and Agriculture Organization; GI, gastrointestinal; HIV, human immun-
odeficiency virus; ICU, intensive care unit; LOS, length of stay; PICU, pediatric intensive care unit.
6. Nutrition Support Team and Feeding the overall delivery of nutrition, with shorter
Protocols time to goal nutrition, increased delivery of
EN, and decreased use of parenteral nutrition.
A specialized nutrition support team in the PICU The effect of these strategies on patient out-
and aggressive feeding protocols may enhance comes has not been demonstrated. Grade E
A.S.P.E.N. Clinical Guidelines / Mehta et al 273
Table 7
Nutrition Support Team and Protocolized Feeding
Study Population
Year Intervention Sample Clinical Outcome
Grade Outcome Measures Size Results Comments
CI, confidence interval; EN, enteral nutrition; LOS, length of stay; NST, nutrition support team; OR, odds ratio; PICU, pediatric
intensive care unit; PN, parenteral nutrition; SOCI, sustained optimal caloric intake.
274 Journal of Parenteral and Enteral Nutrition / Vol. 33, No. 3, May/June 2009
Rationale Notice
Despite its widespread application, the practice of pro-
viding EN in the PICU is highly variable. A significant These A.S.P.E.N. Clinical Guidelines are general. They are
portion of children receiving EN does not meet caloric based upon general conclusions of health professionals who,
goals due to a multitude of reasons. Some studies have in developing such guidelines, have balanced potential ben-
assessed the role of a dedicated nutrition team and the efits to be derived from a particular mode of medical therapy
use of protocols and standardized prescriptions for nutri- against certain risks inherent with such therapy. However,
tion support therapy to implement optimal nutrition the professional judgment of the attending health profes-
practices in the PICU. A dedicated nutrition support sional is the primary component of quality medical care.
team (NST) has become an integral part of the multidis- Because guidelines cannot account for every variation
ciplinary critical care group. Recent surveys demonstrate in circumstances, practitioners must always exercise pro
the presence of such a team during rounds and their fessional judgment in their application. These Clinical
availability for expert advice and help in many centers Guidelines are intended to supplement, but not replace,
around the world. The role of the NST is evolving and professional training and judgment.
the clear benefit on patient outcomes in the PICU is
debatable. Gurgueira et al examined historical cohorts of
children admitted to their PICU at different intervals
Acknowledgment
during a phased implementation of a specialized NST.62
We appreciate the insight of Praveen Goday, MD, for
In their single center retrospective review of 323 patients
initial comments on the manuscript.
over 5 years, the authors reported an increase in EN rate
from 25% to 67% with a significant decrease in PN rates.
The enhanced use of EN correlated with the implemen- References
tation of the NST. Children in this study who received
EN during >50% of their LOS had 83% lower risk of 1. Hulst J, Joosten K, Zimmermann L, et al. Malnutrition in critically
death. A similar historical cohort review by Lambe et al ill children: from admission to 6 months after discharge. Clin Nutr
failed to show any significant difference in nutrition out- 2004;23:223-32.
2. Pollack MM, Wiley JS, Kanter R, Holbrook PR. Malnutrition in
comes (time to achieve sustained optimal caloric goal, critically ill infants and children. JPEN J Parenter Enteral Nutr
energy, and protein balance) in the PICU population 1982;6:20-4.
before and after implementation of a specialized NST.63 3. Mehta NM, Bechard L, Leavitt K, Duggan C. Cumulative energy
Feeding protocols may assist in implementing early imbalance in the pediatric intensive care unit: role of targeted
enteral feedings in critically ill children. Although the indirect calorimetry. JPEN J Parenter Enteral Nutr 2008;32.
4. Pollack MM, Ruttimann UE, Wiley JS. Nutritional depletions in
benefits of such an approach in affecting important critically ill children: associations with physiologic instability and
clinical outcomes in the PICU population have not been increased quantity of care. JPEN J Parenter Enteral Nutr 1985;9:
examined in RCTs, prospective cohort studies have 309-13.
demonstrated reasonable tolerance of feedings and 5. Leite HP, Isatugo MK, Sawaki L, Fisberg M. Anthropometric
improved time to achieving goal EN.52,64 If indeed early nutritional assessment of critically ill hospitalized children. Rev
Paul Med 1993;111:309-13.
EN is associated with improved patient outcomes, imple 6. A.S.P.E.N. Board of Directors. Guidelines for use of total paren-
mentation of an early aggressive EN protocol may be teral nutrition in the hospitalized adult patient. A.S.P.E.N. Board
desirable and could be assisted by a specialized NST. Such of Directors. JPEN J Parenter Enteral Nutr 1986;10:441-5.
protocols may identify caloric goal, route and time of 7. A.S.P.E.N. Board of Directors. Guidelines for use of total parenteral
initiation of EN, type of formulation, rate of increase in nutrition in the hospitalized adult patient. A.S.P.E.N. Board of
Directors. JPEN J Parenter Enteral Nutr 1993;17 (suppl):1SA-52SA.
infusion rate, and time to reach caloric goal. In addition, 8. A.S.P.E.N. Board of Directors and the Clinical Guidelines Task
protocols may use prokinetic medication therapy to enhance Force. Guidelines for the use of parenteral and enteral nutrition in
EN tolerance.65 However, despite the sporadic application adult and pediatric patients [erratum in JPEN 2002;26(2):144].
of feeding protocols and guidelines in the PICU, there is a JPEN J Parenter Enteral Nutr. 2002;26(1 suppl):1SA-138SA.
lack of systematic evidence to support their use. 9. Field MJ, Lohr KN, eds. Medicine Io. Committee to Advise Public
Health Service on Clinical Practice Guidelines, Institute of
Medicine. Clinical Practice Guidelines: Directions for a New
Future Research Program: National Academy Press, Washington, DC; 1990.
10. Seres D, Compher C, Seidner D, Byham-Gray L, Gervasio J,
The role of a specialized NST in the PICU in improving McClave S. 2005 American Society for Parenteral and Enteral
the accuracy of prescribed nutrition support, monitoring Nutrition (A.S.P.E.N.) Standards and Guidelines survey. Nutr Clin
Pract 2006;21:529-32.
of nutrition status, identification of metabolic alterations, 11. Dellinger RP, Carlet JM, Masur H, et al. Surviving Sepsis Campaign
selection of subjects for IC, and overall cost benefit of guidelines for management of severe sepsis and septic shock. Crit
such a team needs further examination. Care Med 2004;32:858-73.
A.S.P.E.N. Clinical Guidelines / Mehta et al 275
12. Guyatt GH, Haynes RB, Jaeschke RZ, et al. Users’ Guides to the 30. White MS, Shepherd RW, McEniery JA. Energy expenditure in
Medical Literature: XXV. Evidence-based medicine: principles 100 ventilated, critically ill children: improving the accuracy of
for applying the Users’ Guides to patient care. Evidence-Based predictive equations. Crit Care Med 2000;28:2307-12.
Medicine Working Group. JAMA 2000;284:1290-6. 31. Derumeaux-Burel H, Meyer M, Morin L, Boirie Y. Prediction of
13. Hulst JM, van Goudoever JB, Zimmermann LJ, et al. The effect of resting energy expenditure in a large population of obese children.
cumulative energy and protein deficiency on anthropometric para Am J Clin Nutr 2004;80:1544-50.
meters in a pediatric ICU population. Clin Nutr 2004;23:1381-9. 32. Mlcak RP, Jeschke MG, Barrow RE, Herndon DN. The influence
14. Robinson MK, Trujillo EB, Mogensen KM, Rounds J, McManus K, of age and gender on resting energy expenditure in severely burned
Jacobs DO. Improving nutritional screening of hospitalized patients: children. Annals of Surgery 2006;244:121-30.
the role of prealbumin. JPEN J Parenter Enteral Nutr 2003;27: 33. Framson CM, LeLeiko NS, Dallal GE, Roubenoff R, Snelling LK,
389-95; quiz 439. Dwyer JT. Energy expenditure in critically ill children. Pediatr Crit
15. Measurement of visceral protein status in assessing protein and Care Med 2007;8:264-7.
energy malnutrition: standard of care. Prealbumin in Nutritional 34. Vazquez Martinez JL, Martinez-Romillo PD, Diez Sebastian J,
Care Consensus Group. Nutrition 1995;11:169-71. Ruza Tarrio F. Predicted versus measured energy expenditure by
16. Dickson PW, Bannister D, Schreiber G. Minor burns lead to major continuous, online indirect calorimetry in ventilated, critically ill
changes in synthesis rates of plasma proteins in the liver. J Trauma children during the early postinjury period. Pediatr Crit Care Med
1987;27:283-6. 2004;5:19-27.
17. Letton RW, Chwals WJ, Jamie A, Charles B. Early postoperative 35. Long CL, Kinney JM, Geiger JW. Nonsuppressability of gluco-
alterations in infant energy use increase the risk of overfeeding. neogenesis by glucose in septic patients. Metabolism 1976;25:
Journal of Pediatric Surgery 1995;30:988-92; discussion 992-3. 193-201.
18. Hulst JM, van Goudoever JB, Zimmermann LJ, Tibboel D, 36. Keshen TH, Miller RG, Jahoor F, Jaksic T. Stable isotopic quantita-
Joosten KF. The role of initial monitoring of routine biochemical tion of protein metabolism and energy expenditure in neonates
nutritional markers in critically ill children. J Nutr Biochem on- and post-extracorporeal life support. J Pediatr Surg 1997;32:
2006;17:57-62. 958-62; discussion 962-3.
19. de Groof F, Joosten KF, Janssen JA, et al. Acute stress response in 37. Duffy B, Pencharz P. The effects of surgery on the nitrogen meta
children with meningococcal sepsis: important differences in the bolism of parenterally fed human neonates. Pediatr Res 1986;
growth hormone/insulin-like growth factor I axis between nonsur- 20:32-5.
vivors and survivors. J Clin Endocrinol Metab 2002;87:3118-24. 38. Premji SS, Fenton TR, Sauve RS. Higher versus lower protein
20. Coss-Bu JA, Jefferson LS, Walding D, David Y, Smith EO, Klish intake in formula-fed low birth weight infants. Cochrane Database
WJ. Resting energy expenditure and nitrogen balance in critically Syst Rev 2006:CD003959.
ill pediatric patients on mechanical ventilation. Nutrition 1998; 39. Wiener RS, Wiener DC, Larson RJ. Benefits and risks of tight
14:649-52. glucose control in critically ill adults: a meta-analysis. JAMA 2008;
21. Suman OE, Mlcak RP, Chinkes DL, Herndon DN. Resting energy 300:933-44.
expenditure in severely burned children: analysis of agreement 40. Faustino EV, Apkon M. Persistent hyperglycemia in critically ill
between indirect calorimetry and prediction equations using the children. J Pediatr 2005;146:30-4.
Bland-Altman method. Burns 2006;32:335-42. 41. Srinivasan V, Spinella PC, Drott HR, Roth CL, Helfaer MA,
22. Briassoulis G, Filippou O, Hatzi E, Papassotiriou I, Hatzis T. Early Nadkarni V. Association of timing, duration, and intensity of hyper-
enteral administration of immunonutrition in critically ill children: glycemia with intensive care unit mortality in critically ill children.
results of a blinded randomized controlled clinical trial. Nutrition Pediatr Crit Care Med 2004;5:329-36.
2005;21:799-807. 42. Wintergerst KA, Buckingham B, Gandrud L, Wong BJ, Kache S,
23. Goran MI, Kaskoun M, Johnson R. Determinants of resting energy Wilson DM. Association of hypoglycemia, hyperglycemia, and
expenditure in young children. J Pediatr 1994;125:362-7. glucose variability with morbidity and death in the pediatric inten-
24. Askanazi J, Rosenbaum SH, Hyman AI, Silverberg PA, Milic-Emili sive care unit. Pediatrics 2006;118:173-9.
J, Kinney JM. Respiratory changes induced by the large glucose 43. Jeevanandam M, Young DH, Schiller WR. Nutritional impact on
loads of total parenteral nutrition. JAMA 1980;243:1444-7. the energy cost of fat fuel mobilization in polytrauma victims.
25. Grohskopf LA, Sinkowitz-Cochran RL, Garrett DO, et al. A J Trauma 1990;30:147-54.
national point-prevalence survey of pediatric intensive care unit- 44. Coss-Bu JA, Klish WJ, Walding D, Stein F, Smith EO, Jefferson
acquired infections in the United States. J Pediatr 2002;140: LS. Energy metabolism, nitrogen balance, and substrate utilization
432-8. in critically ill children. Am J Clin Nutr 2001;74:664-9.
26. MacIntyre NR, Cook DJ, Ely EW, Jr., et al. Evidence-based guide- 45. Friedman Z, Danon A, Stahlman MT, Oates JA. Rapid onset of essen-
lines for weaning and discontinuing ventilatory support: a collec- tial fatty acid deficiency in the newborn. Pediatrics 1976;58: 640-9.
tive task force facilitated by the American College of Chest 46. Van Aerde JE, Sauer PJ, Pencharz PB, Smith JM, Heim T, Swyer
Physicians; the American Association for Respiratory Care; and PR. Metabolic consequences of increasing energy intake by adding
the American College of Critical Care Medicine. Chest 2001; 120 lipid to parenteral nutrition in full-term infants. Am J Clin Nutr
(6 suppl):375S-95S. 1994;59:659-62.
27. Alaedeen DI, Walsh MC, Chwals WJ. Total parenteral nutrition- 47. Kawagoe JY, Segre CA, Pereira CR, Cardoso MF, Silva CV,
associated hyperglycemia correlates with prolonged mechanical Fukushima JT. Risk factors for nosocomial infections in critically
ventilation and hospital stay in septic infants. J Pediatr Surg ill newborns: a 5-year prospective cohort study. Am J Infect Control
2006;41:239-44; discussion 44. 2001;29:109-14.
28. de Klerk G, Hop WC, de Hoog M, Joosten KF. Serial measure- 48. de Lucas C, Moreno M, Lopez-Herce J, Ruiz F, Perez-Palencia M,
ments of energy expenditure in critically ill children: useful in Carrillo A. Transpyloric enteral nutrition reduces the complication
optimizing nutritional therapy? Intensive Care Med 2002;28: rate and cost in the critically ill child. J Pediatr Gastroenterol Nutr
1781-5. 2000;30:175-80.
29. White MS, Shepherd RW, McEniery JA. Energy expenditure mea- 49. Meert KL, Daphtary KM, Metheny NA. Gastric vs small-bowel
surements in ventilated critically ill children: within- and between- feeding in critically ill children receiving mechanical ventilation: a
day variability. JPEN J Parenter Enteral Nutr 1999;23:300-4. randomized controlled trial. Chest 2004;126:872-8.
276 Journal of Parenteral and Enteral Nutrition / Vol. 33, No. 3, May/June 2009
50. Sanchez C, Lopez-Herce J, Carrillo A, Mencia S, Vigil D. Early 59. Heyland DK, Dhaliwal R, Drover JW, Gramlich L, Dodek P.
transpyloric enteral nutrition in critically ill children. Nutrition Canadian clinical practice guidelines for nutrition support in
2007;23:16-22. mechanically ventilated, critically ill adult patients. JPEN J Parenter
51. Briassoulis G, Zavras N, Hatzis T. Malnutrition, nutritional indi- Enteral Nutr 2003;27:355-73.
ces, and early enteral feeding in critically ill children. Nutrition 60. Barbosa E, Moreira EA, Goes JE, Faintuch J. Pilot study with a
2001;17:548-57. glutamine-supplemented enteral formula in critically ill infants.
52. Briassoulis GC, Zavras NJ, Hatzis MT. Effectiveness and safety of Rev Hosp Clin Fac Med Sao Paulo 1999;54:21-4.
a protocol for promotion of early intragastric feeding in critically ill 61. Mayes T, Gottschlich MM, Kagan RJ. An evaluation of the safety
children. Pediatr Crit Care Med 2001;2:113-21. and efficacy of an anti-inflammatory, pulmonary enteral formula in
53. Chellis MJ, Sanders SV, Webster H, Dean JM, Jackson D. Early the treatment of pediatric burn patients with respiratory failure. J
enteral feeding in the pediatric intensive care unit. JPEN J Parenter Burn Care Res 2008;29:82-8.
Enteral Nutr 1996;20:71-3. 62. Gurgueira GL, Leite HP, Taddei JA, de Carvalho WB. Outcomes in
54. Taylor RM, Preedy VR, Baker AJ, Grimble G. Nutritional support a pediatric intensive care unit before and after the implementation
in critically ill children. Clin Nutr 2003;22:365-9. of a nutrition support team. JPEN J Parenter Enteral Nutr 2005;
55. Rogers EJ, Gilbertson HR, Heine RG, Henning R. Barriers to ade- 29:176-85.
quate nutrition in critically ill children. Nutrition 2003;19:865-8. 63. Lambe C, Hubert P, Jouvet P, Cosnes J, Colomb V. A nutritional
56. Atkinson S, Sieffert E, Bihari D. A prospective, randomized, dou- support team in the pediatric intensive care unit: changes and
ble-blind, controlled clinical trial of enteral immunonutrition in factors impeding appropriate nutrition. Clin Nutr 2007;26:
the critically ill. Guy’s Hospital Intensive Care Group. Crit Care 355-63.
Med 1998;26:1164-72. 64. Petrillo-Albarano T, Pettignano R, Asfaw M, Easley K. Use of a
57. Horn D, Chaboyer W. Gastric feeding in critically ill children: a feeding protocol to improve nutritional support through early,
randomized controlled trial. Am J Crit Care 2003;12:461-8. aggressive, enteral nutrition in the pediatric intensive care unit.
58. de Oliveira Iglesias SB, Leite HP, Santana e Meneses JF, de Pediatr Crit Care Med 2006;7:340-4.
Carvalho WB. Enteral nutrition in critically ill children: are pre- 65. Bindl L, Buderus S, Ramirez M, Kirchhoff P, Lentze MJ. Cisapride
scription and delivery according to their energy requirements? reduces postoperative gastrocaecal transit time after cardiac sur-
Nutr Clin Pract 2007;22:233-9. gery in children. Intensive Care Med 1996;22:977-80.