5Archives of Disease in Childhood 1994; 70: 5-9

ORIGINAL ARTICLES

Energy expenditure in congenital heart disease

J S Barton, P C Hindmarsh, C M Scrimgeour, M J Rennie, M A Preece

AbstractGrowth failure is a well recognisedconsequence of severe congenital heartdisease. Total daily energy expenditure(TDEE) was investigated in eight infantswith severe congenital heart disease todetermine whether an increase in thisparameter is an important factor in theirfailure to thrive, and to estimate the energyintake that would be required to allownormal growth. The infants were studiedover a seven day period before surgeryusing the doubly labelled water method.Growth failure was evident; their mean agestandardised body mass index was 80% ofthe expected value. Mean TDEE was 425kJlkg, significantly greater than in healthyinfants (mean TDEE/kg SD score=+l14;95% confidence interval+0 27 to +2.57).In contrast, their energy intake was only82% of the estimated average require-ments. It was estimated that in earlyinfancy a gross energy intake of 600kJ/kg/day is required for normal growthin patients with congenital heart disease.This is unlikely to be achieved by energysupplements alone and early recourseto nasogastric feeding should be con-

sidered.(Arch Dis Child 1994; 70: 5-9)

International GrowthResearch Centre,Institute of ChildHealth, LondonJ S BartonP C HindmarshM A Preece

Department ofAnatomy andPhysiology, Universityof DundeeC M ScrimgeourM J Rennie

Correspondence to:Dr J S Barton, Children'sDepartment, Royal Devonand Exeter Hospital(Wonford), Barrack Road,Exeter EX2 5SQ.

Accepted 14 September1993

Growth failure is a recognised consequence ofsevere congenital heart disease, particularlywhen associated with a large left to right shuntand pulmonary hypertension.' The character-istic reductions in energy intake and increasesin resting energy expenditure2 seen in theseinfants may be responsible for their failure tothrive. Data on total daily energy expenditure(TDEE) in congenital heart disease wouldbe of value in understanding the growth failureof these infants and in planning adequatenutritional support. The measurement ofTDEE is difficult, however. Traditionalmethods of direct or indirect calorimetryrequire the isolation of the subject for pro-

longed periods, which would be inappropriatefor these infants, and extrapolation fromshorter periods of respiratory gas exchange isassociated with significant errors,3 especially as

activity cannot be standardised. TDEE cannow be measured non-invasively in free livinginfants using the doubly labelled watermethod; normal values for energy expenditurehave been reported for healthy breast and

bottle fed infants during the first year of life.4The aim of this study was to obtain com-parable information for a small group ofinfants with severe congenital heart disease, insome both before and after corrective cardiacsurgery.

Patients and methodsEight infants (four boys, four girls), all withsevere congenital heart disease, aged0-23-0-58 years, and weighing 3-57-6&53 kgwere studied. In each infant corrective cardiacsurgery had become the preferred treatmentwithin the first six months of life because ofpoor symptom control and failure to thrive,despite the best possible medical management.Patients were identified from the surgical wait-ing list and were studied at home over a five toseven day period before admission to hospital.The studies were repeated in four of the infantsafter surgical intervention.Energy supplements to a normal diet taken

by mouth were used in four patients and naso-gastric feeding in one (patient 2); in thesepatients the energy density was between 300and 350 kJ/100 ml, the carbohydrate contentwas 8-12%, and the fat content was3'6-3-8%. All those with a left to right shuntwere treated with frusemide (1 mg/kg/day)and spironolactone (3 mg/kg/day), with theaddition of digoxin (0-01 mg/kg/day) orcaptopril (1-3 mg/kg/day) for those in heartfailure. All the patients were free from inter-current infection or other illness at the time ofstudy.TDEE was determined using the doubly

labelled water technique and compared withdata from healthy infants of the same age.4This technique for estimating energy expendi-ture has previously been validated in infants inhospital after surgery.5 Briefly, water contain-ing two stable, non-radioactive isotopes ofoxygen and hydrogen (H2180 and 2H20) wereadministered, taking care to avoid any spillage,via a syringe, feeding bottle, or nasogastrictube according to the child's usual method offeeding. The labelled water was weighed to thenearest 0-01 g and given in doses of 0 3 gH2180 and 0-25 g 2H20 for each kg of esti-mated total body water. Water labelled with180 (Isotec, Miamisburg, USA) and with 2H(Sigma, Poole) were 9-8 and 99-8 atom O/orespectively.

Urine was extracted from cotton wool ballsplaced in disposable napkins.6 Samples were

Barton, Hindmarsh, Scrimgeour, Rennie, Preece

collected before administration of the labelledwater, about five hours later (for total bodywater estimation), and then daily for five toseven days to determine the relative rates of lossof 2H and 180 from the body water pool. Thecollection time of each sample was recorded.

Isotopic enrichment of the urine samples wasmeasured relative to a local standard by isotoperatio mass spectrometry (Finnigan MAT ModelDelta D) using previously described methods.7A rate constant for the disappearance of eachisotope was then determined. The difference inthe elimination rates of the two isotopes isproportional to the total carbon dioxide produc-tion as, through the action of carbonic anhy-drase, 180 elimination is the result of bothcarbon dioxide production and loss of waterfrom the body, whereas 2H is lost only as water.The mean TDEE over the study period canthen be calculated using Weir's equation8assuming a predicted respiratory quotient of0-85 reported for healthy infants of this age.9Some of the infants studied, however, werereceiving carbohydrate supplements whichmight be expected to increase their foodquotient. In healthy subjects who maintainenergy balance the food quotient is equivalentto the respiratory quotient over the relativelylong period of a double isotope study.9 Dietarydata were available from seven of the infantsstudied from which food quotients could bederived for each individual patient. The mean(SE) food quotient allowing for the growthobserved over the study period of the infantsstudied was 0-87 (0005). Using the individualfood quotient values to determine energyexpenditure for each subject would have re-duced the TDEE by a maximum of 3-6% in onepatient with a mean reduction of less than 2%.Body weight was measured to the nearest 10

g at the beginning and end of the study period;supine length was recorded at the outset. Theage standardised body mass index (BMI),equal to weight/height2 (%BMI), which relatesweight and height to the expected (50thcentile) value for age, was calculated accordingto the method of Cole.'0

Total body water (TBW) was estimatedfrom the H2180 dilution in basal urine samplesand urine samples taken five hours after thedose of radiolabelled water.11 Fat free mass(FFM) was calculated, assuming the watercontent of the FFM at this age to be 80% byweight,'2 as FFM=TBW/0-8; body fat=totalbody weight-FFM.

As far as we are aware the doubly labelledwater technique has not previously been usedto determine the TDEE in subjects withcongenital heart disease and it is thereforeimportant to consider how abnormalities influid metabolism might influence the data onenergy expenditure obtained using thismethod. An increase in interstitial water(oedema) due to cardiac failure would prolongthe time necessary for isotope equilibration tooccur throughout the body water pool. Failureto allow for this would result in an under-estimate of the TBW and consequently in theestimated TDEE. All of the infants in thisstudy were receiving long term treatment withdiuretics and none was clinically oedematousor in poorly controlled cardiac failure whenstudied. The TBW value was therefore calcula-ted from the 180 dilution in urine obtained atthe usual time after isotope administration."ITreatment with diuretics, tachypnoea, andexcessive sweating might all be expected toincrease the water turnover rate in patientswith congenital heart disease. Providing thatthe difference between the rate constants for180 and 2H is sufficiently large to be accuratelydetermined, however, a rapid turnover of bodywater will not influence the calculation ofTDEE and had the advantage of shorteningthe necessary study period which depends onthe isotopes' biological half lives.The infants studied were all receiving

a mixed diet. During the study period athree day dietary record was kept using house-hold measures to estimate the amountconsumed. These records were analysedusing computerised food composition tables(Diet 2000, B&W Electronic Systems,Portsmouth).The study was approved by the ethics

committee of the Hospital for Sick Children,Great Ormond Street, and written parentalconsent was obtained in all instances.

STATISTICAL ANALYSISThe mean and 95% confidence interval (CI)were calculated for normally distributed datausing the Student's t distribution, otherwisethe median and range are reported. TDEEdata were compared with reference standardsusing graphical methods and by calculating SDscores by interpolation from log transformeddata using the geometric mean and log SDvalues published by Davies et al.4

Table 1 Diagnosis, growth, and energy expenditure before the operation of infants studied

Age Length Weight %BMI TDEE TDEE TDEE TBW(years) Sex (cm) (kg) (%o) (MJ) (MJ/kg) (MJ/kg°5) (kg)

TGA, previous BAS 0-32VSD, PHT, CCF 0 53VSD, PHD, CCF 0-31AVSD, PHT, CCF,Down's syndrome 0-23

AVSD, PHT, CCF,Down's syndrome 0-32

VSD,PHT 0-58VSD 0-39ToF 0 47

0-39 (

M 59-8 4-68M 59-9 4-69M 62-8 5-23

78-7 1-53 033 0776-6 3 13 0-66 1-4480-4 2-17 0 41 0 95

3-693-293-75

FFM(kg)

4-614-114-68

F 53-8 3-57 75-7 1-5 0-42 0-8 2-75 3-44

M

FFF

(0 04)

55.967-358-461-559-9 (1-5)

4.496-534.395-374-87 (0-31)

88-482-976-282-580-2 (1-5)

1-632-171-972-432-07 (0-19)

0-360 330440440 43 (0 04)

0 770-850931-040 93 (0 08)

3-164-433 073.543 46 (0-18)

3.955-543-844-434-33 (0 23)

TGA=transposition of great arteries; BAS=balloon atrial septostomy; VSD=ventricular septal defect; PHT=pulmonary hypertension; CCF=congestive cardiacfailure; AVSD=atrioventricular septal defect; ToF=tetralogy of Fallot; BMI=body mass index; TBW=total body water; and FFM=free fat mass.

DiagnosisPatientNo

1234

5

678Mean (SIE)

6

7Energy expenditure in congenital heart disease

Table 2 Weight gain, energy intake and total daily energy expenditure (TDEE) before and after cardiac surgery

BirthPatient wueightNo (g)

2*34*567*8*Mean (SE)

27602500335029302200304026102670

Before study

WeightAge Weight gain(years) (kg) (giday)

0-320*530-310-230 320-580*390-47

4-684-695-233-574.496-534.395-37

16-311-316-57-619-416-612-515-914-5 (1-3)

TDEE(kJ/kg/day)

Energy intake(kJ/kg/day)

Weight gain duringstudy (g/kg/day)

Before After Before After Before Aftersurgery surgery surgery surgery surgery surgery

329662412422360331440444

197315582

430

499730434491

220t464539483 (57)

51363 2-5421 32- -0 5- 2-2_ 1-9

419 7-1_ 6

0 99-66

6

3 4 (0 9)

*Infants receiving energy supplements. tThis very low energy intake is unexplained. Clearly, if sustained at this rate, weight losswould result.

ResultsTable 1 gives the diagnostic an

metric features of the eight infantshowed significant preoperative g

with a mean daily weight gain of 111-4 to 1 7-7) g, considerably less tcentile rates of 31 and 26 g/daygirls respectively over the initial t

E._

a)

Q

CL

x

a)

C1Cu

0H-

4

3

2

1

n 0*1 0 0 0 0

Age (years)Figure 1 Energy expenditure in infants wiheart disease. Total daily energy expendituwdetermined before the operation by the doubmethod and plotted against age in eight inficongenital heart disease (for details, see texderivedfrom data obtained in normal infanet al.4

a)

0..

ic

x

0)Cu

c

-0

HE

0.8 r

0 70

0-6

0 5 F

04

030

0 2 k

0-1

"0.0 0-1 0-2 03 04 05

Age (years)Figure 2 Total daily energy expenditure (adjustedfor body size in infants with conge?disease. TDEE before the operation adjusteweight in the same eight infants illustratedCentiles are derivedfrom data obtained in Xby Davies et al.4

of life'3 (table 2). As a result, at the time ofId anthropo- study, the median weight centile was on the:s. All infants first and the median length centile the sixth ofrowth failure the Tanner et al standards.'4 Weight was moreA45 (95% CI severely affected than length, resulting in athan the 50th markedly reduced mean BMI of 8022% (95%in boys and CI 76-7 to 83 7). Before surgery total bodyhree months fat (body weight-FFM) (table 1) was signifi-

cantly reduced; when expressed as a per-centage of body weight, the mean percentageof body fat was 10-5% (95% CI 6 to 15%)compared with a value of 25% in reference

90th children of the same age.'2The TDEE data from our eight patients

50th with congenital heart disease were similar tothose obtained from healthy infants4 when

10th expressed as MJ/day (fig 1). The mean (95%CI) SD score for TDEE (MJ/day) was -0-27(- 1P03 to +0A49). Total energy expenditure isdependent on body size, however, and inparticular the metabolically active tissue mass,and when expressed on a weight basis (fig 2) inthe infants with congenital heart disease it

l lJ appeared to be significantly increased (mean06 07 08 TDEE/kg SD score +140, 95% CI +0-27 to

+2 57).ith congenital Expressing energy expenditure in early

rlylabelledwater infancy on the basis of the square root of bodyants with serious weight limits the influence of body weight ont). Centiles are energy expenditure.'5 When expressed in thiszts by Davies way these data suggest that infants with con-

genital heart disease tend to have an increasedenergy expenditure, but with the small numberstudied the difference did not reach statisticalsignificance: mean TDEE MJ/kg0 5 SDscore=+0-60 (95% CI -0-36 to + 1-57).

Gross energy intakes, estimated fromprospective dietary records (seven infants)taken during the study were variable (table 2).

90t1- The highest value was observed in an infant50 P (patient 2) who was fed an enriched milk

formula via a nasogastric tube. Intake appeared1 O- to be reasonable when expressed relative to

body weight (mean 483 (95% CI 344 to 622)kJ/kg/day), but was less than that recom-mended for age,'6 the mean being only 82% ofthe estimated average requirement (95% CI 64

06 07 08 to 101%).No relation was observed between either

TDEE) energy intake or 'spare' energy defined asnital heart (energy intake-TDEE) and weight gaindfor body during the preoperative study period (Pearson

norma infants correlation coefficients r=0 01 and 0 11respectively).

n-n

5

.0 0-1 0-2 0-3 0-4 0-5 C

Barton, Hindmarsh, Scrimgeour, Rennie, Preece

In four patients it was possible to repeat thestudy postoperatively with a median surgery torestudy interval of 63 days (range 51 to 91).No significant changes in median %BMI (76%before v 76% after the operation), sum of tri-ceps and subscapular skinfold thickness (23.2v 26-7 mm), nor percentage body fat(11*4 v 11 0%) occurred over this period.No consistent pattern of change in energyexpenditure was observed in this small group(table 2).

DiscussionTDEE is the sum of the energy used tomaintain essential metabolic processes and topreserve a constant body mass (maintenanceenergy requirements) and the energy expendedin muscular activity plus that required tosynthesise new tissue as a result of growth.An increase in resting oxygen consumption

in congenital heart disease has previously beenreported by a number of workers,17 18 particu-larly in patients with pulmonary hypertensionand cardiac failure. This hypermetabolism hasbeen related to an increased oxygen con-sumption by the hypertrophied heart and astimulation of metabolism due to increasedcatecholamine secretion.'9 TDEE has notpreviously been measured in congenital heartdisease. Although maintenance energy require-ments are likely to be increased, reflecting theincrease in resting oxygen consumption, theenergy expended in activity is typically reducedin sick and malnourished children,20 and whengrowth is slow less energy is required for thesynthesis of new tissue.Under these circumstances the TDEE can-

not simply be predicted from changes in rest-ing metabolic rate. The TDEE is, however,important in calculating energy requirementsfor normal growth and activity. Metabolisableenergy intake (energy absorbed and availablefor metabolic purposes) must be sufficient tomeet the TDEE and energy stored in newtissue, calculated from the tissue compositionand its rate of accretion.

Healthy infants investigated using themethods of this study had an estimated mean(SD) TDEE of 280 (60) kJ/kg/day at 3 monthsof age.4 These subjects were all growing nor-mally and, presumably, had normal levels ofactivity, in marked contrast with our patientswith congenital heart disease, none of whomwere thriving.When the TDEE in infants with congenital

heart disease was estimated from respiratory gasexchange during the intervals between feeds itwas found to be increased2l (mean (SD) TDEE341 (12) kJ/kg/day), though not to the extentobserved in our slightly older patients (mean(SE) 425 (38) kJAkg/day). Although extendingthe period ofrespiratory gas exchange to includea complete feed cycle reduces the error inestimating 24 hour energy expenditure,3 thisapproach can only provide a rough estimate ofthe TDEE as individual activity varies consider-ably over a 24 hour period. Furthermore, theactivity level was scored on a crude four pointscale and then related to oxygen consumption,

which inevitably introduces additional errors.Finally, in the paper by Jackson and Poskittenergy expenditure was not measured duringfeeding, a physically demanding activity forinfants with cardiorespiratory problems, so thatthe 24 hour energy expenditure reported waslikely to have been an underestimate.2' Incontrast, our data represent the first attempt toactually measure carbon dioxide productionand thence energy expenditure in free livinginfants with congenital heart disease, and tocalculate energy requirements on the basis ofmeasured daily energy expenditure.Weight gain was less than that expected for

age in five of the eight infants during the pre-operative study period (table 2) and wassignificantly slower than normal from birth,even in those infants receiving dietary supple-ments. Our inability to detect any relationbetween energy intake and weight gain in theseinfants is not surprising given the smallnumber of infants studied and the imprecisemethod used to estimate energy intake.Furthermore such a relation can usually onlybe shown during periods of rapid growth,2'21whereas before surgery our infants weregrowing slowly.Four patients were studied after surgery. Of

the other four two died perioperatively, onecould not be included because the protocolpostoperatively was not complied with, andone infant was lost to follow up. It is difficult todraw firm conclusions from such a small dataset, but a few points are of interest. The lack ofchange in body composition postoperatively isnot surprising as the interval between studiesinevitably included a period of starvation andcatabolism after surgery, followed by the slowresumption of growth and consequently littlenet difference in size or body fat whenrestudied. Patient 3 showed a threefoldincrease in the rate of weight gain when studiedafter closure of his ventricular septal defect.Gross energy intake was unchanged, but theTDEE had decreased, presumably allowingmore energy to be stored in new tissue. Catchup growth has continued in this child withlength and weight now lying above the 50thcentile at 18 months of age. In contrast, littlechange in energy intake, expenditure, orweight gain was observed in patient 7. Thisgirl's ventricular septal defect was of moderatesize but no postoperative acceleration in lengthor weight velocity has occurred, suggestingthat the cardiac anomaly was not a major influ-ence on energy metabolism or growth. Finally,the dramatic decrease in energy intakeobserved in patient 2 resulted from removal ofthe nasogastric tube after surgery, and may inpart have been responsible for his continuedslow weight gain despite a reduction in energyexpenditure.

Although our study population was smalland heterogeneous, including two infants withtrisomy 21, they are generally representative ofpatients with congenital heart disease present-ing in early life. Using data from this andother2l studies and a factorial approach toenergy utilisation it is possible to estimatethe energy requirements of an infant with

8

Energy expenditure in congenital heart disease

congenital heart disease which must be met ifnormal growth is to be sustained.

Payne and Waterlow have calculated thatthe energy cost of normal tissue deposition(Ecg) is 21 kj/g,22 300/o less than the 31 kJ/gestimated in infants with congenital heartdisease receiving high energy feeds.2' Agreater energy cost of growth probably reflectsthe greater fat content of new tissue in theinfants with congenital heart disease. This issupported by the significant increase in skin-fold thicknesses observed during high energyfeeding.21 Using this higher value for theenergy utilised in growth and assuming that75% of the energy cost of growth is stored innew tissue,20 whereas the remainder isexpended in synthesis (and thus included inthe TDEE), the current metabolisable energyintake in these subjects is about 2-4 MJ/day(TDEE plus observed weight gain multipliedby 0-75Ecg). From the deficit in weight gainobserved during this study, an additional 100kJ/day of metabolisable energy would berequired to allow normal growth during thisperiod. Careful balance studies have shownthat 85% of the gross energy intake is availablefor metabolic purposes in infants with con-genital heart disease.2l Consequently, the goalshould be to achieve an energy intake of about2-9 MJ/day (600 kJ/kg/day) to allow an averagerate of weight gain during the first threemonths of life. Of the infants we have studiedonly the one fed nasogastrically achieved sucha high energy intake. Energy supplements inthree other infants fed by mouth did notincrease the energy intake much above thatobserved in infants fed a regular milkformula because of the small volumesingested. The use of high energy feeds andnasogastric feeding regimens is well toleratedin congenital heart disease and result in catchup growth.23

Ronholt Hansen and Dorup, studying anolder group of children with congenital heartdisease, have also documented a significantreduction in energy intake.24 Protein intakewas adequate, but the intake of a number ofmicronutrients was less than the recom-mended daily allowance. We cannot accuratelyassess the usual mineral and vitamin intake ofthe infants in this study because of the briefperiod for which dietary intake data werecollected. Unlike the patients studied byRonholt Hansen and Dorup,24 however,infants in this study received feeds based on astandard infant formula enriched with mineralsand vitamins. Significant micronutrient defi-ciency is therefore less likely at this age thanlater when diet is based on unfortified cows'milk. Although the deficiency of anothernutrient might theoretically increase energyexpenditure through the inefficient use ofdietary energy, the excellent growth responseto energy supplements alone in young infantswith congenital heart disease2l 23 suggests thatadditional nutrient deficiency is not of majorimportance.

Although there are no data from infantsundergoing cardiothoracic surgery, postopera-tive morbidity has been reduced by improving

the nutritional status before cardiac surgery inadults25 and in children undergoing a variety ofother surgical procedures. As these nutritionalrequirements may be anticipated we suggestthat energy supplementation in conjunctionwith nasogastric feeding is instituted at thetime of diagnosis to prevent growth failure,particularly when immediate surgery is notpossible.We thank the physicians and surgeons of the cardiothoracicunit, Hospital for Sick Children, Great Ormond Street for per-mission to study their patients and Kabi Pharmacia, Stockholm,Sweden for their support of this study. JSB and PCH are gener-ously supported by Children Nationwide and Kabi Pharmacia.

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