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Review Article

World Journal for Pediatric and


Congenital Heart Surgery
Nutrition Support for Children Undergoing 2015, Vol. 6(3) 443-454
ª The Author(s) 2015
Reprints and permission:
Congenital Heart Surgeries: A Narrative sagepub.com/journalsPermissions.nav
DOI: 10.1177/2150135115576929
Review pch.sagepub.com

Judith J. M. Wong, MBBCh, BAO, MRCPCH1,


Ira M. Cheifetz, MD, FCCM, FAARC2, Chengsi Ong, MS, RD3,
Masakazu Nakao, MD, FRCSCTh4, and
Jan Hau Lee, MBBS, MRCPCH, MCI5,6

Abstract
Energy imbalance in infants and children with congenital heart disease (CHD) is common and influenced by age, underlying cardiac
diagnoses, and presence or absence of congestive heart failure. During the surgical hospitalization period, these children are
prone to nutritional deterioration due to stress of surgery, anesthetic/perfusion techniques, and postoperative care. Poor
nutrition is associated with increased perioperative morbidity and mortality. This review aims to examine various aspects of
nutrition in critically ill children with CHD, including (1) energy expenditure, (2) perioperative factors that contribute to energy
metabolism, (3) bedside practices that are potentially able to optimize nutrient delivery, and (4) medium- to long-term impact of
energy balance on clinical outcomes. We propose a nutrition algorithm to optimize nutrition of these children in the perioperative
period where improvements in nutrition status will likely impact surgical outcomes.

Keywords
cardiac intensive care, children, congenital heart disease, congenital heart surgery, nutrition, pediatric, intensive care

Submitted December 02, 2014; Accepted February 16, 2015.

Introduction palliative surgeries (Table 1). This review aims to examine


various aspects of nutrition in critically ill children with CHD,
Children with underlying congenital heart disease (CHD) are at
including (1) energy expenditure, (2) perioperative factors
risk of energy imbalance and malnutrition.1,2 Infants with iso-
that contribute to energy metabolism, (3) bedside practices
lated cardiac defects are generally born with a normal birth
that are potentially able to optimize nutrient delivery, and
weight but develop nutritional and growth difficulties there-
after.3,4 Factors causing failure to thrive in these children
include the underlying cardiac disease, presence/absence of
1
congestive cardiac failure, decreased energy intake (eg, feeding Department of Pediatric Medicine, KK Women’s and Children’s Hospital,
difficulties, anorexia, and hepatomegaly causing reduced gas- Singapore
2
Department of Pediatrics, Division of Pediatric Critical Care Medicine, Duke
tric volume), and disturbances in gastrointestinal function University Medical Center, Durham, NC, USA
(eg, gut edema, reflux).5,6 In addition, children with CHD asso- 3
Department of Nutrition and Dietetics, KK Women’s and Children’s
ciated with an underlying syndrome/genetic condition (eg, Hospital, Singapore
4
Down syndrome and Turner syndrome) are at an even higher Department of Paediatric Cardiothoracic Surgery, KK Women’s and
risk of energy imbalance.5,7 Children’s Hospital, Singapore
5
Department of Pediatric Subspecialties, Children’s Intensive Care Unit, KK
Malnutrition is associated with poor outcomes in children Women’s and Children’s Hospital, Singapore
with CHD.8-10 Contributing factors in this group of children 6
Office of Clinical Sciences, Duke-NUS Graduate School of Medicine,
include malnutrition-induced myocardial dysfunction, vascu- Singapore
lar endothelial dysfunction, skeletal muscle atrophy, immuno-
suppression, insulin resistance, and lipolysis.10-12 Therefore, Corresponding Author:
Jan Hau Lee, Department of Pediatric Subspecialties, Children’s Intensive Care
it is crucial for care providers of patients with CHD to under- Unit, KK Women’s and Children’s Hospital, 100 Bukit Timah Road, Singapore
stand energy metabolism in these children and innovate ways 229899.
to improve nutrition delivery before and after corrective and Email: lee.jan.hau@kkh.com.sg

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444 World Journal for Pediatric and Congenital Heart Surgery 6(3)

Table 1. Factors that Influence Energy Expenditure in Children With


Abbreviations and Acronyms Congenital Heart Disease.
CHD congenital heart disease
CHF congestive heart failure Factors that contribute to preoperative resting energy expenditure
CI confidence interval  Age (younger children have higher energy expenditure)
CPB cardiopulmonary bypass  Underlying cardiac diagnosis
EN enteral nutrition  Cyanotic congenital heart disease
GER gastroesophageal reflux  Significant left to right shunts
IC indirect calorimetry
LOS length of stay Factors that contribute to the immediate postoperative resting energy
OR odds ratio expenditure
PICU pediatric intensive care unit
PN parenteral nutrition  Preoperative nutritional status
REE resting energy expenditure  Preoperative fasting
TEE total energy expenditure  Sedation and neuromuscular blockade
TSFZ triceps skinfold Z score  Cardiopulmonary bypass
WHO World Health Organization  Perioperative thermoregulation
 Inotropes/other drugs
(4) medium- to long-term effects of energy balance on clinical
outcomes. patients. Its use has been validated in large-scale adult stud-
ies.16,17 The REE is best measured using indirect calorimetry
(IC). The difference between TEE and REE is attributed to the
Methods energy expended during physical activity. In children with
We carried out an online search in MEDLINE using the follow- CHD, it is likely that these activities are more energy costly
ing key words and MESH terms: enteral nutrition, feeding, than healthy children, as patients with CHD may experience
nutrition support, energy requirements, congenital heart dis- increased work of breathing and cardiac output for the same
ease, cardiac surgery, pediatrics, pediatric intensive care unit level of physical exertion.2
(search strategy for MEDLINE is outlined in Supplementary
Appendix A). Based on our review of the current literature, Cyanotic CHD. For the purpose of this review, we considered cya-
we summarized pertinent studies with the intention to provide notic CHD as cardiac lesions with resultant arterial oxygen desa-
some recommendations for the nutritional support of children turation with the exception of single-ventricle lesions, which we
with CHD during the perioperative period. These recommenda- considered separately. We found three studies examining energy
tions and algorithms are proposed based on the consistency and expenditure in children with cyanotic CHD (Table 2). The TEE
strength of the underlying evidence. but not REE was observed to be significantly higher in patients
with cyanotic CHD compared to healthy controls. This is postu-
lated to be due to energy expended during physical activity.
Results Interestingly, differences in blood oxygenation were not demon-
Energy Expenditure of Children With CHD strated to influence oxygen consumption.18
Total energy expenditure (TEE) is the sum of all energy Congestive heart failure. The hallmark of congestive heart failure
expended in daily life including resting energy expenditure (CHF) is increased cardiorespiratory work and sympathetic
(REE), diet-induced thermogenesis, physical activity, and, in activity.2,19 It is also observed that patients with CHF have
children, growth. These components vary with age and body higher resting oxygen consumption and more severe growth
composition—the energy used for growth is high in the first retardation.3,20 Although few in number, several observational
three months of life (45% of energy consumed) and decreases studies consistently reported increased energy expenditure in
as the child grows older (4% of energy consumed after patients with CHF when compared to patients without CHF
12 months of age).13 The TEE can be measured using the dou- (Table 1).21,7 In patients with VSD, a strong positive correla-
bly labeled water technique, which allows patients to be mon- tion was shown between the magnitude of pulmonary blood
itored without major alterations to their daily care settings.14 flow to systemic blood flow ratio (Qp-Qs) with TEE (r ¼ .73,
The doubly labeled water technique is a noninvasive procedure P  .0001) and energy expenditure from physical activity
involving the ingestion of a quantity of water labeled with a (r ¼ .62, P  .0002), indicating that the larger the left-to-right
known concentration of stable isotopes of hydrogen and oxy- shunt, the larger increase in energy expenditure.
gen.15 As energy is expended in the body, hydrogen isotopes
are eliminated as water, and oxygen isotopes are eliminated Single-ventricle defects. There is little known about the energy
as both water and carbon dioxide. The differences between metabolism and requirements for patients with univentricu-
the isotope elimination rates are used to calculate TEE. Other lar physiology.22 Three studies explored postoperative
than requiring periodic sampling of body fluids (eg, urine), this energy expenditure in children with single-ventricle defects
method is nonrestrictive and ideally suited to use in free-living (Table 2).1,22,23 Of note, eight hours postsurgery, patients

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Table 2. Summary of Studies Examining Energy Expenditure in Children With Congenital Heart Disease During Perioperative Period.
Mean REE + SD, kcal/kg/d

Study Subgroups of CHD Preop Postop POD1 POD2 POD3 POD5 POD  1 Week Healtdy Controls

Krauss 1975a (n ¼ 7) CHF 63 + 12

No CHF 45 + 8

Gebara 1992b (n ¼ 26) Mixed 55 + 8

Mitchell 1994d (n ¼ 53) Mixed 116 + 31d 75 + 21d 112 + 6d

Barton 1994d (n ¼ 12) Mixed 101 + 25d 91 + 39d

42 + 9 44 + 14
Ackerman 1998b,d (n ¼ 18) VSD
88 + 11d 62 + 10d

64 + 17 56 + 7
Leitch 1998b,d (n ¼ 22) Cyanotic
94 + 23d 72 + 13d

67 + 8 58 + 8
Leitch 2000b,d (n¼17) Cyanotic
70 + 14d 76 + 9d

Avitzur 2001b (n ¼ 29) Cyanotic 57 + 13 59 + 10

Acyanotic 58 + 9 62 + 10
b,d
Farrel 2001 (n ¼ 30) 52 + 14 44 + 12
CHF
92 + 20d 61 + 9d

44 + 8
No CHF
77 + 17d

van der Kuip 2003d (n ¼ 34) Mixed 91 + 10d 71 + 9d

Jia Li 2003c (n ¼ 17) Single ventricle 43 + 11 39 + 8 39 + 8 41 + 6


b
Nydegger 2009 (n ¼ 38) Mixed 59 + 9 49 + 9 50 + 5
b
De Wit 2010 (n ¼ 21) Overall 68 + 15 52 + 3 77 + 15 40 + 10

Cyanotic 66 + 17

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Acyanotic 70 + 14

Require CPB 74 + 15

No CPB 58 + 11

Mehta 2012b (n ¼ 26) Single ventricle 57 + 20

Irving 2013b (n ¼ 93) Overall 324 + 55e 328 + 52e

Single ventricle 325 + 59e

Double ventricle 322 + 54e

Abbreviations: CHF, congestive heart failure; CHD, congenital heart disease; Preop, preoperative; Postop, postoperative; POD, postoperative day; REE, resting energy expenditure; SD, standard deviation; VSD,
ventricular septal defect.
a
Diaferometry used to determine REE.
b
Indirect calorimetry used to determine REE.
c
Respiratory mass spectrometry was used to determine oxygen consumption (VO2) and carbon dioxide production (VCO2). REE was then calculated using the modified Weir equation.
d

445
Doubly labeled water used to determine total energy expenditure.
e
kcal/d.
446 World Journal for Pediatric and Congenital Heart Surgery 6(3)

with single-ventricle defects were demonstrated to be either University. Caloric intake and weight-for-age Z scores signifi-
hypometabolic or normometabolic when compared with cantly correlated with each other (r ¼ .55, P < .01).39 The pre-
World Health Organization (WHO) equation-estimated REE operative nutritional status was also associated with changes in
in the majority of patients (73%).1 energy metabolism in the postoperative period. Those with
poorer nutritional status preoperation had a higher REE in the
postoperative period. A negative correlation was demonstrated
Intraoperative Factors That Affect Energy Expenditure
between weight-for-height Z scores (r ¼ .521, P < .005),
Postcardiac Surgery weight-for-age Z scores (r ¼ .584, P < .005), and postopera-
Studies examining energy expenditure in children with CHD tive REE.28
and the effect of cardiac surgery are summarized in Table 2. The impact of poor nutritional status on postoperative out-
Factors that influence energy metabolism during surgery are comes in children with CHD is highlighted by the following
discussed subsequently. studies. In 100 infants aged 5.1 (range: 2.4-10) months under-
going bidirectional Glenn procedure with preoperative weight-
Cardiopulmonary bypass. Patients who undergo cardiopulmonary for-age Z score of 1.3 (range 3.9-0.6), demonstrated that,
bypass (CPB) exhibit complex neuroendocrine responses that independent of hemodynamic or echocardiographic variables,
lead to hypercatabolism.24-27 There is only one clinical study of a lower weight-for-age Z score was associated with a longer
21 patients postcardiac surgery, which found that REE was higher postoperative hospital stay.40 Among 55 infants aged 47 (range
in patients who underwent CPB compared to those without CPB 18–71) months undergoing Fontan surgery, those with a
(73.69 + 15.11 vs 58.31 + 10.88 kcal/kg/d; P ¼ .02).28 weight-for-age Z score of less than 2.0 were more likely to
have postoperative infections (odds ratio [OR] 8.7; 95% confi-
Neuromuscular blockade. There is conflicting data on oxygen
dence interval [CI]: 1.5-48.6).41 Data from the Society of Thor-
consumption and energy expenditure in patients with neuro-
acic Surgeons Congenital Heart Surgery Database also
muscular blockade.29-33 The likely explanation for this discre-
demonstrated the association between lower weight-for-age Z
pancy is the patients who were deeply sedated and did not have
score and poor surgical outcomes.42 In patients undergoing
regular movements before paralysis did not demonstrate a
Fontan surgery, independent of patient and center characteris-
decrease in oxygen consumption after establishing paralysis.33
tics, weight-for-age Z score <2.0 was associated with
Inotropic drugs. Early physiological studies in healthy humans increased in-hospital mortality (OR 2.73; 95% CI: 1.09-6.86),
showed a dose-dependent increase in metabolic rate during Fontan failure (OR 2.59, 95% CI: 1.24-5.40), and longer length
adrenaline infusion.34 However, in the clinical setting, only one of stay (mean difference þ1.2 days, 95% CI: 0.1-2.4).42
study examined the effect of inotropes on energy expenditure A prospective double-center cohort study (n ¼ 71) involving
and showed that the degree of inotropic support (including children less than 5 years of age who required surgery for CHD
adrenaline, noradrenaline, dopamine, and milrinone) was not showed an association between preoperative total body fat
associated with increased REE.28 mass and markers of acute and chronic indices of malnutrition
and postoperative clinical outcomes.43 After adjusting for age,
gender, and severity of heart disease, investigators found that
Energy Expenditure After Cardiac Surgery low triceps skinfold Z score (TSFZ) was significantly associ-
After surgical correction of the underlying cardiac lesion, REE ated with longer pediatric intensive care unit (PICU) length
is expected to decrease to within normal levels within one week of stay (LOS), duration of mechanical ventilation, and dopa-
(Table 2).35 Beyond two years, TEE and REE continue to mine and milrinone infusion hours. These investigators also
match that of healthy controls, and anthropometric measure- demonstrated a relationship between TSFZ and preoperative
ments were on par, indicating satisfactory catch-up growth.36 plasma pro-brain natriuretic peptide (BNP) levels (indicator
Successful cardiac surgery, therefore, is expected to be fol- of myocardial function) as well as postoperative duration of
lowed by improvements in weight within a few months, with inotropic infusion. The same study showed that a higher albu-
height and head circumference catching up within a year.37 min level was associated with decreased BNP.43 Larsen et al
found that patients who had a ‘‘low-caloric intake (below
mean for the group)’’ had longer duration of mechanical ven-
Nutritional Status and Outcomes in CHD tilation, duration of parenteral nutrition (PN) use, and PICU
Poor preoperative nutrition is associated with poor clinical out- LOS.44 Both acute and chronic protein energy malnutrition
comes. The nutritional status is partially attributed to insuffi- states were prevalent (51.2% and 40.5%, respectively) in
cient caloric intake (as well as increased energy expenditure patients undergoing cardiac surgery and associated with lon-
as discussed above).38 Weight for age, growth rates, and daily ger hospital LOS.45
metabolizable energy intake per kg has been shown to be lower A case–control study involving children (n ¼ 74) who have
in infants with CHD compared to normal infants.20 When undergone open heart surgery showed that patients who died
viewed in relation to actual weight, energy intake in children had progressively decreasing median weight-for-age Z score
with CHD averaged 88% + 17% of that recommended by the from birth, operation, and last recorded weight (0.12, 1.31,
Food and Agriculture Organization, WHO, and United Nations and 2.09, respectively) in comparison with the control

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Wong et al 447

Table 3. Barriers and Strategies to Optimize Nutrition.

Barriers to Optimal Nutrition Strategies to Optimize Nutrition

Inadequate intake: Facilitate enteral feeding:


 Feeding difficulties  Nasogastric, small bowel, gastrostomy feeding
 Poor suck swallow coordination  Continuous feeds
 Vocal cord dysmotility  High-calorie feeds
 Feed refusal  Enteral feeding protocol
 Early satiety  Supplementation with parenteral nutrition
 Referral to feeding specialist
Inability to absorb nutrients:
 Gastroesophageal reflux disease (GERD)  Treat GERD (may involve medical therapy, continuous feeding, small
 Feed intolerance bowel feeding or gastrostomy with fundoplication)
 Gut edema  Treat congestive cardiac failure
Inpatient/perioperative factors:
 Fluid restriction  High-calorie feeds
 Supplementation with parenteral nutrition
Frequent feed interruptions:
 Hemodynamic instability  Enteral feeding protocol to minimize feed interruptions
 High lactate levels
 High ventilator requirements
 Hyperglycemia
 Concerns of necrotizing enterocolitis/bowel ischemia
 Radiological procedures
 Surgical procedures (including chest tube insertion/
removal, cardiac catheterization, etc)
 Intubation and extubation
Energy estimation:
 Over- or underestimation of energy expenditure  Regular and accurate nutritional assessments including use of indirect
calorimetry when indicated
 Individualized nutrition prescription
Special conditions
 Chylothorax  Treat the underlying condition
 Acute kidney injury/oliguria

group.46 Those who had a drop in weight-for-age Z score >0.67 types of CHD over the perioperative period have also demon-
had increased odds of dying (OR 13.5, 95% CI: 3.6-51). strated similar slow rate of establishment of optimal nutrient
In summary, poor anthropometry in children with CHD is delivery.47,51
associated with increased morbidity (eg, frequent hospitaliza- Fluid restriction is the single most important barrier in post-
tions, poor surgical outcomes, and persistent growth retardation) cardiac surgery nutrition.52,53 After cardiac surgery, fluid restric-
and mortality. Because of this association, it is important for tion is common to avoid fluid retention and its associated
clinical care providers to innovate techniques to improve pre- morbidities. Fluid administration is regulated meticulously so
and perioperative nutrition delivery. In the following section, that total fluid intake does not exceed a specific volume over a
we will discuss the barriers to nutrition in patients with CHD and 24-hour period.49 This leaves very little room for nutritive solu-
propose some methods to overcome them. tions.54 The PN offers some benefit in this regard as it is capable
of providing a concentrated form of nutrition.49 However, it
lacks other benefits of EN such as promotion of gut integrity,
Barriers to Optimal Nutrition in Children With Congenital
motility, and immune function. Some clinicians have therefore
Heart Disease initiated trophic feeding while supplementing nutrition with
When admitted for surgery, children with CHD are at risk of PN until target calories can be achieved via the enteral route.55,56
further nutritional depletion (Table 3).47-50 A retrospective Feed interruption is another important barrier to optimal
study (n ¼ 47) examining postoperative nutrition found declin- nutrition. A retrospective chart review of 100 neonates under-
ing median weight-for-age Z score between admission for stage going cardiac surgery with CPB demonstrated that enteral
1 palliation (1.14, range: 2.3 to 0.6) and hospital discharge feeds were interrupted temporarily 21.1% of the time for pro-
(1.81, 4.9 to 0.5). Enteral nutrition (EN) was started on cedures (eg, cardiac catheterization, magnetic resonance ima-
median postoperative day 4 (range: 1-12), and caloric intake ging of the brain, and placement of gastrostomy tube).57 In
took more than two weeks to reach a target of 110 to 120 addition, feeding difficulties including feed refusal and paren-
kcal/kg/d.48 Other studies conducted in children with different tal distress due to feeding pose significant challenges.58-62

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448 World Journal for Pediatric and Congenital Heart Surgery 6(3)

One important postoperative complication that results in patients consistently receive at least 100 kcal/kg/d.57 Intrave-
profound difficulty in providing nutrition support is chy- nous lipid can be administered without central access.57 At the
lothorax. Chylothorax is an uncommon complication of car- moment, there is insufficient evidence to support the use of
diac surgery with a reported incidence of 1% to 9% of intravenous lipid supplementation as routine practice, however,
cardiac surgeries.63-65 It often leads to severe and prolonged it can be considered on a case-by-case basis. Because of the
protein, fat, and fat-soluble vitamin deficits. The management ability to attenuate the inflammatory response from CPB, some
of chylothorax after cardiac surgery may include a diet low in investigators have proposed supplementing with lipid emul-
long-chain triglycerides and enriched with medium-chain tri- sions containing eicosapentaenoic and docosahexaenoic acid
glycerides or total parenteral nutrition to allow gut rest.65 Pro- during the pre- and postoperative period.76,77 These studies
teins including immunoglobulins, electrolytes, and fat-soluble show improvement in surrogate markers of the inflammatory
vitamins also need replacement. We refer the reader to other response (eg, tumor necrosis factor-alpha, leukotriene B4, pro-
reports on chylothorax for a more in-depth discussion.65,66 calcitonin, and lymphocyte count).

Nasogastric, small bowel, and gastrostomy feeding. After cardiac


Strategies to Optimize Nutrient Intake in Children With surgery, children are at significant risk of aspiration and pul-
Congenital Heart Disease monary injury due to vocal cord dysfunction, gastroesophageal
Individualized nutrition prescriptions. Metabolic profiles of chil- reflux (GER), and dysphagia. Surgical injury to the recurrent
dren with CHD evolve throughout the postoperative period. laryngeal nerve, associated neurodevelopmental delay, and
Predictive equations had been demonstrated to be inaccurate suck–swallow–breathe incoordination are potential causes.
in estimating energy requirements.1,18,27 Where possible, IC Another significant risk factor is prolonged postoperative intu-
should be used to assess individual energy requirements, and bation (>7 days). Prolonged intubation is associated with the
the frequency of assessments needs to depend on the course of risk of dysphagia and directly increases the risk of not achiev-
the acute phase response. Indirect calorimetry, however, has ing oral feeding by time of discharge by 10% per day for each
limitations due to equipment availability, staffing, and cost.67 day of intubation.73,78 As a result, many infants depend on tube
The accuracy of measurements is also affected by low tidal feeding to achieve nutritional needs during hospital stay and
volumes, low oxygen consumption, and high fraction of some even after hospital discharge.61,73,79
inspired oxygen.68 Transpyloric feeding allows a larger volume of feeds to be
Optimizing nutrition support in these children encompasses delivered in critically ill children and may be safer in the peri-
meeting not only energy needs but also macro- and micronutri- extubation period. It does not, however, prevent aspiration of
ent needs. Providing sufficient energy without sufficient pro- gastric fluids. In a retrospective study involving 17 patients
tein may result in overall muscle breakdown and decreased with CHD, a duodenal tube facilitated enteral feeding and
lean body mass. Recommendations for protein intake range resulted in improvement in weight gain and reduced clinical
from 1.5 to 2.5 g/kg/d in infants and 0.8 to 1.5 g/kg/d in older symptoms of persistent emesis or respiratory wheezing after
children.69,70 In the immediate postoperative period, recom- feeding.80
mended protein requirements are generally 2 to 3 g/kg/d for Another strategy to optimize caloric intake may be early
children between 0 and 2 years, 1.5 to 2 g/kg/d for children placement of gastrostomy feeding tubes, especially in infants
between 2 and 13 years, and 1.5g/kg/d for children between who are exclusively fed via a nasogastric tube.57 This route
13 and 18 years.71 However, specific studies on protein is particularly useful in patients with evidence of GER. Percu-
requirement in children with CHD, using either nitrogen bal- taneous endoscopic gastrostomy can be performed under deep
ance studies or stable isotope methodology, are lacking.72 Lit- sedation and allows EN support without the disadvantages
tle is also known about micronutrient requirements in children related to long-term nasogastric tube feeding.81 Complications
with CHD. are uncommon, and the tube can be removed when enteral sup-
port is no longer necessary.
Parenteral nutrition. Most children undergoing open heart sur-
gery are initiated on enteral feeds within 3 to 4 days.47,48,51,73 High-calorie enteral and continuous feeds. High-caloric feeds refer
Some patients with feeding difficulties require a prolonged to concentrated formula feeds or feeds with additives (eg, glu-
period of time to reach full enteral feeds.73 The PN can be used cose polymers) that increase caloric content. High-calorie feeds
to supplement the enteral route until sufficient calories can be have been reported in this population in two studies. The first
achieved by feeding. Good use of PN according to internation- involved 14 infants with CHD and failure to thrive who were
ally accepted guidelines allows the provision of concentrated given high-energy feeds by addition of glucose polymers to
nutrition to accommodate fluid restrictive policies.74,75 achieve an energy density of 125% standard formula.82 They
Nevertheless, PN has been associated with increased risk of measured physiological variables and conducted bomb calori-
infection.10 Because of this risk, most centers will stop PN once metry to determine energy content of vomit, urine, and stools.
enteral feeds reach 90 to 100 mL/kg/d. However, given the fre- This study showed that the mean gross energy intakes increased
quency of feed interruptions, some investigators propose the by 31.7% on high-energy feeding, with mean weight gain
use of intravenous lipids in addition to enteral feeds until these improving from 1.3 to 5.8 g/kg/d. There was no difference in

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Wong et al 449

Figure 1. Proposed preoperative nutrition algorithm.

physiological variables and energy losses from vomit, urine, and nutritional supplementation were given continuous enteral
and stools, showing good tolerability. It was recommended that feeds, and this approach improved mean daily caloric intake
infants with CHD and failure to thrive should be fed on high- and weight gain.87 A randomized controlled trial of 19 infants
energy diets from the time of diagnosis to optimize growth. showed that continuous feeds were effective in improving
Of note, there was reduced gastric emptying in one small study nutritional status as measured by weight-for-age Z scores and
involving seven patients who received feeds supplemented length. The patients were randomly assigned to one of the fol-
with glucose polymers. However, the net transfer of energy lowing three feeding groups: group 1 (n ¼ 7) received continu-
to the intestine was larger after the supplemented feed than the ous 24-hour nasogastric alimentation, group 2 (n ¼ 5) received
standard feed.83 overnight 12-hour nasogastric infusions plus daytime oral feed-
In another cohort of 46 infants, investigators used standard ings as tolerated, and group 3 (n ¼ 7) received oral feedings
formula on day 1 postoperation (0.67 kcal/mL), 1.18 times con- alone.88 The trial period lasted over five months, and the group
centration (0.79 kcal/mL) on day 2, 1.36 times concentration on continuous nasogastric alimentation showed marked
(0.9 kcal/mL) from day 3 onward, and 1.5 times concentration increases in mid-arm muscle circumference and triceps and sub-
(1 kcal/mL) from discharge.84 They found that with this scapular skinfold thicknesses compared to the other two groups.
regime, patients received higher energy intake (median per-
centage of the estimated energy requirement before discharge Enteral feeding protocols. Even with accurate energy estimation,
was 98% vs 78% in control group), had greater median weight delivering nutrition to critically ill children can be challen-
gain (þ20 g/d vs 35 g/d), and were discharged from the hos- ging.89-91 It was found that only 38% of the nutrition prescrip-
pital earlier. A similar study of 21 infants receiving standard tion is received by the patient.89 Reasons for this include the
density formula and high-density formula showed higher frequent interruptions of enteral feeds as discussed earlier.
energy and protein intake per body weight, weight gain, and Implementation and adherence to a feeding protocol have
serum albumin in the latter group without an increase in demonstrated to improve the amount of prescribed nutrition
adverse effects.85 that is actually received.
Continuous feeding is another option to improve nutrient Investigators have shown that feeding protocols improve
delivery.86 A study of 11 infants with CHD who were not gain- nutrition delivery.10,56,92-94 A systematic review that included
ing weight adequately despite the use of hypercaloric formulas nine studies (two of which involved a cohort of neonates with

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450 World Journal for Pediatric and Congenital Heart Surgery 6(3)

Figure 2. Proposed perioperative nutrition algorithm.

hypoplastic left heart syndrome) showed that feeding protocols their use as surrogate markers of nutritional status have been
improve time to initiation of feeds, decrease time to achieving studied—including serum albumin, prealbumin, transferrin,
goal feeds, reduce gastrointestinal and infective complications, transerythrin, retinol-binding protein, and C-reactive protein.
and improve safety.95 In the two studies that involved postopera- In the population with CHD, albumin is the most widely
tive patients with hypoplastic left heart syndrome, the feeding studied biomarker.98 Leite et al (n ¼ 30) prospectively studied
protocol group had more rapid advancement of feeds with no children with CHD admitted after cardiac surgery and found
significant increased incidence of necrotizing enterocolitis.96,97 that preoperative albumin of less than 3 g/dL was associated
We propose a nutrition algorithm for children with CHD to with increased postoperative infections (P ¼ .0026) and mor-
optimize their nutrition in the perioperative period (Figures 1 tality (P ¼ .0138).99 Patients with postoperative (postoperative
and 2). These are crucial periods where improvements in nutri- day 2) albumin of less than 3 g/dL had longer hospital stay
tion status will likely impact surgical outcomes. In general, the compared to those greater than or equal to 3 g/dL (median
preoperative goal should be to improve existing nutritional sta- 14.5 vs 10 days, P < .05). Another study showed that a higher
tus (eg, weight for age Z scores) and to maintain this score dur- albumin (and prealbumin) level was associated with a decrease
ing the postoperative period. in BNP and a trend toward lower inotrope duration.43

Nutrition-Based Biomarkers in Children With CHD Limitations


It is important to appreciate that even a simple nutrition assess- The published literature on energy metabolism in CHD
ment in children with CHD can be challenging. Although daily involves small numbers of patients as well as nonstandardized
weight estimation is routine in most centers, its value is limited, measurement methods and timing of measurements. These lim-
given significant fluid shifts and diuretic use in these patients.58 itations make comparisons and statistical pooling difficult.35
Triceps skinfold thickness and mid-arm circumference have The pathophysiology of CHD is also diverse, and there are
been used to estimate fat stores and lean body muscle mass, many physiological changes that occur from the age of infancy
respectively, but again, these measurements are affected by through childhood and play a major role in energy metabolism.
edema.72 Biochemical markers, therefore, seem appealing, and These factors are potential confounders in current studies. On

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Wong et al 451

the other hand, data from a solitary group of CHD at a partic- 5. Nydegger A, Bines JE. Energy metabolism in infants with conge-
ular age bracket may not be generalizable to other children with nital heart disease. Nutrition (Burbank, Los Angeles County,
other types of CHD. Calif). 2006;22(7-8): 697-704.
6. Mitchell IM, Davies PS, Day JM, Pollock JC, Jamieson MP.
Energy expenditure in children with congenital heart disease,
Future Directions
before and after cardiac surgery. J Thorac Cardiovasc Surg.
Because of the inherent differences across the spectrum of 1994;107(2): 374-80.
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prescriptions based on IC measurements should be explored but not resting energy expenditure is increased in infants with
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for safe initiation and optimization of enteral feeds in this group (Edinburgh, Scotland). 2004;23(2): 223-232.
of children is proposed, but this will likely need further modi- 9. Pollack MM, Ruttimann UE, Wiley JS. Nutritional depletions in
fication, taking into account local practices and resources. critically ill children: associations with physiologic instability and
increased quantity of care. JPEN J Parenter Enteral Nutr. 1985;
Conclusion 9(3): 309-313.
10. Mehta NM, Bechard LJ, Cahill N, et al. Nutritional practices and
Children with CHD are generally at risk of malnutrition, and their relationship to clinical outcomes in critically ill children—an
this is exacerbated by further nutritional depletion during the international multicenter cohort study*. Crit Care Med. 2012;
frequent hospital admissions. Poor anthropometry is associated 40(7): 2204-2211.
with increased morbidity and mortality. Energy metabolism is 11. Barton JS, Hindmarsh PC, Scrimgeour CM, Rennie MJ, Preece
affected by age, cardiac diagnoses, preoperative nutritional sta- MA. Energy expenditure in congenital heart disease. Arch Dis
tus, the surgery itself (surgical techniques, anesthesia manage- Child. 1994;70(1): 5-9.
ment and CPB strategies), and postoperative care. Nutrition 12. Cameron JW, Rosenthal A, Olson AD. Malnutrition in hospita-
algorithms can potentially optimize nutrition in these children lized children with congenital heart disease. Arch Pediatr Adoles-
during the perioperative period. cent Med. 1995;149(10): 1098-1102.
13. Wells JC, Davies PS. Estimation of the energy cost of physical
Authors’ Note
activity in infancy. Arch Dis Child. 1998;78(2): 131-136.
Judith JM Wong, Ira M Cheifetz, Chengsi Ong, Masakazu Nakao, and
14. Schoeller DA. Measurement of energy expenditure in free-living
Jan Hau Lee designed the structure of this review article, critically
humans by using doubly labeled water. J Nutr. 1988;118(11):
reviewed the manuscript, and approved the final manuscript as
submitted. 1278-1289.
15. Speakman JR. The history and theory of the doubly labeled water
Declaration of Conflicting Interests technique. Am J Clin Nutr. 1998;68(4): 932S-938S.
The author(s) declared no potential conflicts of interest with respect 16. Schoeller DA. Recent advances from application of doubly
to the research, authorship, and/or publication of this article. labeled water to measurement of human energy expenditure.
J Nutr. 1999;129(10): 1765-1768.
Funding 17. Trabulsi J, Troiano RP, Subar AF, et al. Precision of the doubly
The author(s) received no financial support for the research, labeled water method in a large-scale application: evaluation of a
authorship, and/or publication of this article. streamlined-dosing protocol in the Observing Protein and Energy
Nutrition (OPEN) study. Eur J Clin Nutr. 2003;57(11): 1370-1377.
Supplemental Material 18. Avitzur Y, Singer P, Dagan O, et al. Resting energy expenditure
The online [appendices/data supplements/etc] are available at in children with cyanotic and noncyanotic congenital heart dis-
http://pch.sagepub.com/supplemental’’ ease before and after open heart surgery. JPEN J Parenter Enteral
Nutr. 2003;27(1): 47-51.
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