Professional Documents
Culture Documents
Nutrition Support For Children Undergoing
Nutrition Support For Children Undergoing
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
Study Subgroups of CHD Preop Postop POD1 POD2 POD3 POD5 POD 1 Week Healtdy Controls
No CHF 45 + 8
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
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
Cyanotic 66 + 17
Require CPB 74 + 15
No CPB 58 + 11
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
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
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).
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
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
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.
children with CHD, the feasibility of using individual nutrition 7. Ackerman IL, Karn CA, Denne SC, Ensing GJ, Leitch CA. Total
prescriptions based on IC measurements should be explored but not resting energy expenditure is increased in infants with
and investigated. The need for accurate provision of nutrition ventricular septal defects. Pediatrics. 1998;102(5): 1172-1177.
is further strengthened by the demonstration of possible detri- 8. Hulst J, Joosten K, Zimmermann L, et al. Malnutrition in critically
mental effects of over- and underfeeding.100,101 An algorithm ill children: from admission to 6 months after discharge. Clin Nutr
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.
References 19. Pittman JG, Cohen P. The pathogenesis of cardiac cachexia.
1. Mehta NM, Costello JM, Bechard LJ, et al. Resting energy expen- N Engl J Med. 1964;271: 453-460.
diture after Fontan surgery in children with single-ventricle heart 20. Menon G, Poskitt EM. Why does congenital heart disease cause
defects. JPEN J Parenter Enteral Nutr. 2012;36(6): 685-692. failure to thrive? Arch Dis Child. 1985;60(12): 1134-1139.
2. Lees MH, Bristow JD, Griswold HE, Olmsted RW. Relative 21. Krauss AN, Auld PA. Metabolic rate of neonates with congenital
hypermetabolism in infants with congenital heart disease and heart disease. Arch Dis Child. 1975;50(7): 539-541.
undernutrition. Pediatrics. 1965;36: 183-191. 22. Li J, Zhang G, Herridge J, et al. Energy expenditure and caloric
3. Leitch CA. Growth, nutrition and energy expenditure in pediatric and protein intake in infants following the Norwood procedure.
heart failure. Prog Pediatr Cardiol. 2000;11(3): 195-202. Pediatr Crit Care Med. 2008;9(1): 55-61.
4. Naeye RL. Anatomic features of growth failure in congenital 23. Irving SY, Medoff-Cooper B, Stouffer NO, et al. Resting energy
heart disease. Pediatrics. 1967;39(3): 433-440. expenditure at 3 months of age following neonatal surgery for
congenital heart disease. Congenital Heart Dis. 2013;8(4): 39. Hansen SR, Dorup I. Energy and nutrient intakes in congenital
343-351. heart disease. Acta Paediatr (Oslo, Norway: 1992). 1993;82(2):
24. Milne E, Elliott M, Pearson D, Holden M, Ørskov H, Alberti K. 166-172.
The effect on intermediary metabolism of open-heart surgery with 40. Anderson JB, Beekman RH III, Border WL, et al. Lower weight-
deep hypothermia and circulatory arrest in infants of less than 10 for-age z score adversely affects hospital length of stay after the
kilograms body weight. a preliminary study. Perfusion. 1986; bidirectional Glenn procedure in 100 infants with a single ventri-
1(1): 29-40. cle. J Thorac Cardiovasc Surg. 2009;138(2): 397-404. e1.
25. Hersio K, Takala J, Kari A, Huttunen H. Changes in whole body 41. Anderson JB, Kalkwarf HJ, Kehl JE, Eghtesady P, Marino BS.
and tissue oxygen consumption during recovery from hypother- Low weight-for-age Z-score and infection risk after the fontan
mia: effect of amino acid infusion. Crit Care Med. 1991;19(4): procedure. Ann Thorac Surg. 2011;91(5): 1460-6.
503-508. 42. Wallace MC, Jaggers J, Li JS, et al. Center variation in patient age
26. Pons Leite H, Gilberto Henriques Vieira J, Brunow De Carvalho and weight at fontan operation and impact on postoperative out-
W, Chwals WJ. The role of insulin-like growth factor I, growth comes. Ann Thorac Surg. 2011;91(5): 1445-1452.
hormone, and plasma proteins in surgical outcome of children 43. Radman M, Mack R, Barnoya J, et al. The effect of preoperative
with congenital heart disease. Pediatr Crit Care Med. 2001; nutritional status on postoperative outcomes in children under-
2(1): 29-35. going surgery for congenital heart defects in San Francisco
27. Coss-Bu JA, Klish WJ, Walding D, Stein F, Smith EO, Jeffer- (UCSF) and Guatemala City (UNICAR). J Thorac Cardiovasc
son LS. Energy metabolism, nitrogen balance, and substrate Surg. 2014;147(1): 442-450.
utilization in critically ill children. Am J Clin Nutr. 2001; 44. Larsen BM, Goonewardene LA, Field CJm Joffe AR, Van Aerde
74(5): 664-669. Je, Olstad DL, Clandinin MT. Low energy intakes are associated
28. De Wit B, Meyer R, Desai A, Macrae D, Pathan N. Challenge of with adverse outcomes in infants after open heart surgery. JPEN
predicting resting energy expenditure in children undergoing sur- J Parenter Enteral Nutr. 2013;37(2): 254-260.
gery for congenital heart disease. Pediatr Crit Care Med. 2010; 45. Toole BJ, Toole LE, Kyle UG, Cabrera AG, Orellana RA, Coss-
11(4): 496-501. Bu JA. Perioperative nutritional support and malnutrition in
29. Palmisano BW, Fisher DM, Willis M, Gregory GA, Ebert PA. infants and children with congenital heart disease. Congenit Heart
The effect of paralysis on oxygen consumption in normoxic chil- Dis. 2014;9(1): 15-25.
dren after cardiac surgery. Anesthesiology. 1984;61(5): 518-522. 46. Eskedal LT, Hagemo PS, Seem E, et al. Impaired weight gain pre-
30. Vernon DD, Witte MK. Effect of neuromuscular blockade on dicts risk of late death after surgery for congenital heart defects.
oxygen consumption and energy expenditure in sedated, mechani- Arch Dis Child. 2008;93(6): 495-501.
cally ventilated children. Crit Care Med. 2000;28(5): 1569-1571. 47. Kelleher DK, Laussen P, Teixeira-Pinto A, Duggan C. Growth
31. Barton RG, Craft WB, Mone MC, Saffle JR. Chemical paralysis and correlates of nutritional status among infants with hypoplastic
reduces energy expenditure in patients with burns and severe left heart syndrome (HLHS) after stage 1 Norwood procedure.
respiratory failure treated with mechanical ventilation. J Burn Nutrition (Burbank, Los Angeles County, Calif ). 2006;22(3):
Care Rehabil. 1997;18(5): 461-468; discussion 0. 237-244.
32. Gebara BM, Gelmini M, Sarnaik A. Oxygen consumption, energy 48. Hong BJ, Moffett B, Payne W, Rich S, Ocampo EC, Petit CJ.
expenditure, and substrate utilization after cardiac surgery in chil- Impact of postoperative nutrition on weight gain in infants with
dren. Crit Care Med. 1992;20(11): 1550-1554. hypoplastic left heart syndrome. J Thorac Cardiovasc Surg.
33. Lemson J, Driessen JJ, van der Hoeven JG. The effect of neuro- 2014;147(4): 1319-1325.
muscular blockade on oxygen consumption in sedated and 49. Owens JL, Musa N. Nutrition support after neonatal cardiac sur-
mechanically ventilated pediatric patients after cardiac surgery. gery. Nutr Clin Pract. 2009;24(2): 242-249.
Intensive Care Med. 2008;34(12): 2268-2272. 50. Iannucci GJ, Oster ME, Mahle WT. Necrotising enterocolitis in
34. Fellows IW, Bennett T, MacDonald IA. The effect of adrenaline infants with congenital heart disease: the role of enteral feeds.
upon cardiovascular and metabolic functions in man. Clin Sci Cardiol Young. 2013;23(4): 553-559.
(London, England: 1979). 1985;69(2): 215-222. 51. Nicholson GT, Clabby ML, Kanter KR, Mahle WT. Caloric
35. Nydegger A, Walsh A, Penny DJ, Henning R, Bines JE. Changes intake during the perioperative period and growth failure in
in resting energy expenditure in children with congenital heart infants with congenital heart disease. Pediatr Cardiol. 2013;
disease. Eur J Clin Nutr. 2009;63(3): 392-397. 34(2): 316-321.
36. Leitch CA, Karn CA, Ensing GJ, Denne SC. Energy expenditure 52. Leong AY, Cartwright KR, Guerra GG, Joffe AR, Mazurak VC,
after surgical repair in children with cyanotic congenital heart dis- Larsen BM. A Canadian survey of perceived barriers to initiation
ease. J Pediatr. 2000;137(3): 381-385. and continuation of enteral feeding in PICUs. Pediatr Crit Care
37. Rosenthal A, Castaneda A. Growth and development after cardi- Med. 2014;15(2): e49-e55.
ovascular surgery in infants and children. Prog Cardiovasc Dis. 53. Tume L, Carter B, Latten L. A UK and Irish survey of enteral
1975;18(1): 27-37. nutrition practices in paediatric intensive care units. Br J Nutr.
38. Huse DM, Feldt RH, Nelson RA, Novak LP. Infants with conge- 2013;109(7): 1304-1322.
nital heart disease. Food intake, body weight, and energy metabo- 54. Cooper DS, Nichter MA. Advances in cardiac intensive care.
lism. Am J Dis Child (1960). 1975;129(1): 65-69. Curr Opin Pediatr. 2006;18(5): 503-511.
55. Zaloga GP, Roberts PR, Marik P. Feeding the hemodynamically 72. Teixeira-Cintra MA, Monteiro JP, Tremeschin M, Trevilato TM,
unstable patient: a critical evaluation of the evidence. Nutr Clin Halperin ML, Carlotti AP. Monitoring of protein catabolism in
Pract. 2003;18(4): 285-293. neonates and young infants post-cardiac surgery. Acta Paediatr
56. Hamilton S, McAleer DM, Ariagno K, et al. A stepwise ent- (Oslo, Norway: 1992). 2011;100(7): 977-982.
eral nutrition algorithm for critically ill children helps achieve 73. Kogon BE, Ramaswamy V, Todd K, et al. Feeding difficulty in
nutrient delivery goals. Pediatr Crit Care Med. 2014;15(7): newborns following congenital heart surgery. Congenit Heart
583-589. Dis. 2007;2(5): 332-337.
57. Schwalbe-Terilli CR, Hartman DH, Nagle ML, et al. Enteral feed- 74. Koletzko B, Goulet O, Hunt J, Krohn K, Shamir R. Guidelines
ing and caloric intake in neonates after cardiac surgery. Am J Crit on Paediatric Parenteral Nutrition of the European Society of
Care. 2009;18(1): 52-57. Paediatric Gastroenterology, Hepatology and Nutrition (ESP-
58. Cabrera AG, Prodhan P, Bhutta AT. Nutritional challenges and GHAN) and the European Society for Clinical Nutrition and
outcomes after surgery for congenital heart disease. Curr Opin Metabolism (ESPEN), Supported by the European Society of
Card. 2010;25(2): 88-94. Paediatric Research (ESPR). J Pediatr Gastroenterol Nutr.
59. Davis D, Davis S, Cotman K, et al. Feeding difficulties and 2005;41(suppl 2): S1-S87.
growth delay in children with hypoplastic left heart syndrome ver- 75. Mehta NM, Compher C, Directors ASPENBo. A.S.P.E.N. clinical
sus d-transposition of the great arteries. Pediatr Cardiol. 2008; guidelines: nutrition support of the critically ill child. J Parenter
29(2): 328-333. Enteral Nutr. 2009;33(3): 260-276.
60. Hill G, Silverman A, Noel R, Bartz PJ. Feeding dysfunction in 76. Larsen BM, Field CJ, Leong AY, et al. Pretreatment with an intra-
single ventricle patients with feeding disorder. Congenit Heart venous lipid emulsion increases plasma eicosapentanoic acid and
Dis. 2014;9(1): 26-29. downregulates leukotriene B4, procalcitonin, and lymphocyte
61. Sables-Baus S, Kaufman J, Cook P, da Cruz EM. Oral feeding concentrations after open heart surgery in infants. JPEN J Paren-
outcomes in neonates with congenital cardiac disease undergoing ter Enteral Nutr. 2015;39(2): 171-179.
cardiac surgery. Cardiol Young. 2012;22(1): 42-48. 77. Larsen BM, Goonewardene LA, Joffe AR, et al. Pre-treatment with
62. Thommessen M, Heiberg A, Kase BF. Feeding problems in chil- an intravenous lipid emulsion containing fish oil (eicosapentaenoic
dren with congenital heart disease: the impact on energy intake and docosahexaenoic acid) decreases inflammatory markers after
and growth outcome. Eur J Clin Nutr. 1992;46(7): 457-464. open-heart surgery in infants: a randomized, controlled trial. Clin
63. Biewer ES, Zurn C, Arnold R, et al. Chylothorax after surgery on Nutr (Edinburgh, Scotland). 2012;31(3): 322-329.
congenital heart disease in newborns and infants -risk factors and 78. Einarson KD, Arthur HM. Predictors of oral feeding difficulty in
efficacy of MCT-diet. J Cardiothorac Surg. 2010;5: 127. cardiac surgical infants. Pediatr Nurs. 2003;29(4): 315-319.
64. Densupsoontorn NS, Jirapinyo P, Wongarn R, et al. Manage- 79. Medoff-Cooper B, Ravishankar C. Nutrition and growth in conge-
ment of chylothorax and chylopericardium in pediatric patients: nital heart disease: a challenge in children. Curr Opin Cardiol.
experiences at Siriraj Hospital, Bangkok. Asia Pacific journal of 2013;28(2): 122-129.
clinical nutrition. 2005;14(2): 182-187. 80. Kuwata S, Iwamoto Y, Ishido H, Taketadu M, Tamura M, Senzaki
65. Chan EH, Russell JL, Williams WG, Van Arsdell GS, Coles JG, H. Duodenal tube feeding: an alternative approach for effectively
McCrindle BW. Postoperative chylothorax after cardiothoracic promoting weight gain in children with gastroesophageal reflux
surgery in children. Ann Thorac Surg. 2005;80(5): 1864-1870. and congenital heart disease. Gastroenterol Res Pract. 2013;
66. Panthongviriyakul C, Bines JE. Post-operative chylothorax in 2013: 181604.
children: an evidence-based management algorithm. J Paediatr 81. Hofner G, Behrens R, Koch A, Singer H, Hofbeck M. Enteral
Child Health. 2008;44(12): 716-721. nutritional support by percutaneous endoscopic gastrostomy in
67. Sion-Sarid R, Cohen J, Houri Z, Singer P. Indirect calorimetry: children with congenital heart disease. Pediatr Cardiol. 2000;
a guide for optimizing nutritional support in the critically ill 21(4): 341-346.
child. Nutrition (Burbank, Los Angeles County, Calif ). 2013; 82. Jackson M, Poskitt EM. The effects of high-energy feeding
29(9): 1094-1099. on energy balance and growth in infants with congenital
68. Joosten KF, Verhoeven JJ, Hop WC, Hazelzet JA. Indirect calori- heart disease and failure to thrive. Br J Nutr. 1991;65(2):
metry in mechanically ventilated infants and children: accuracy of 131-143.
total daily energy expenditure with 2 hour measurements. Clin 83. Cavell B. Effect of feeding an infant formula with high energy
Nutr (Edinburgh, Scotland). 1999;18(3): 149-1452. density on gastric emptying in infants with congenital heart dis-
69. Bechard LJ, Parrott JS, Mehta NM. Systematic review of the ease. Acta Paediatr Scand. 1981;70(4): 513-516.
influence of energy and protein intake on protein balance in criti- 84. Pillo-Blocka F, Adatia I, Sharieff W, McCrindle BW, Zlotkin S.
cally ill children. J Pediatr. 2012;161(2): 333-339. e1. Rapid advancement to more concentrated formula in infants
70. Wu PY, Edwards N, Storm MC. Plasma amino acid pattern in after surgery for congenital heart disease reduces duration of
normal term breast-fed infants. J Pediatr. 1986;109(2): hospital stay: a randomized clinical trial. J Pediatr. 2004;
347-349. 145(6): 761-766.
71. Mehta NM, Compher C. A.S.P.E.N. Clinical Guidelines: nutrition 85. Taniguchi-Fukatsu A, Matsuoka M, Amagai T. Effect of a high
support of the critically ill child. JPEN J Parenter Enteral Nutr. density formula on growth and safety in congenital heart disease
2009;33(3): 260-276. infants. Eur E J Clin Nutr Metab. 2010;5(6): e281-e283.
86. Bougle D, Iselin M, Kahyat A, Duhamel JF. Nutritional treat- support in critically ill children. J Hum Nutr Diet. 2009;22(5):
ment of congenital heart disease. Arch Dis Child. 1986;61(8): 428-436.
799-801. 95. Wong JJ, Ong C, Han WM, Lee JH. Protocol-driven enteral nutri-
87. Vanderhoof JA, Hofschire PJ, Baluff MA, et al. Continuous tion in critically ill children: a systematic review. JPEN J Paren-
enteral feedings. An important adjunct to the management of ter Enteral Nutr. 2014;38(1): 29-39.
complex congenital heart disease. Am J Dis Child (1960). 1982; 96. Braudis NJ, Curley MA, Beaupre K, et al. Enteral feeding
136(9): 825-827. algorithm for infants with hypoplastic left heart syndrome
88. Schwarz SM, Gewitz MH, See CC, et al. Enteral nutrition in poststage I palliation. Pediatr Crit Care Med. 2009;10(4):
infants with congenital heart disease and growth failure. Pedia- 460-466.
trics. 1990;86(3): 368-373. 97. del Castillo SL, McCulley ME, Khemani RG, et al. Reducing
89. Tume L, Latten L, Darbyshire A. An evaluation of enteral feeding the incidence of necrotizing enterocolitis in neonates with
practices in critically ill children. Nurs Crit Care. 2010;15(6): hypoplastic left heart syndrome with the introduction of an
291-299. enteral feed protocol. Pediatr Crit Care Med. 2010;11(3):
90. Keehn A, O’Brien C, Mazurak V, et al. Epidemiology of Interrup- 373-377.
tions to Nutrition Support in Critically Ill Children in the Pediatric 98. Ong C, Han WM, Wong JJ, Lee JH. Nutrition biomarkers and
Intensive Care Unit. JPEN J Parenter Enteral Nutr. 2015;39(2): clinical outcomes in critically ill children: a critical appraisal of
211-217. the literature. Clin Nutr (Edinburgh, Scotland). 2014;33(2):
91. Rogers EJ, Gilbertson HR, Heine RG, Henning R. Barriers to ade- 191-197.
quate nutrition in critically ill children. Nutrition (Burbank, Los 99. Leite HP, Fisberg M, de Carvalho WB, de Camargo Carvalho AC.
Angeles County, Calif). 2003;19(10): 865-868. Serum albumin and clinical outcome in pediatric cardiac surgery.
92. Slicker J, Hehir DA, Horsley M, et al. Nutrition algorithms for Nutrition (Burbank, Los Angeles County, Calif). 2005;21(5):
infants with hypoplastic left heart syndrome; birth through the 553-558.
first interstage period. Congenital Heart Dis. 2013;8(2): 89-102. 100. Mehta NM, Bechard LJ, Dolan M, Ariagno K, Jiang H,
93. Petrillo-Albarano T, Pettignano R, Asfaw M, Easley K. Use of a Duggan C. Energy imbalance and the risk of overfeeding in
feeding protocol to improve nutritional support through early, critically ill children. Pediatr Crit Care Med. 2011;12(4):
aggressive, enteral nutrition in the pediatric intensive care unit. 398-405.
Pediatr Crit Care Med. 2006;7(4): 340-344. 101. Prieto MB, Cid JL-H. Malnutrition in the critically ill child: the
94. Meyer R, Harrison S, Sargent S, Ramnarayan P, Habibi P, Laba- importance of enteral nutrition. Int J Environ Res Public Health.
darios D. The impact of enteral feeding protocols on nutritional 2011;8(11): 4353-4366.