br nutritional status children congenital...

Br HeartJ_ 1995;73:277-283

Nutritional status of children with congenitalheart disease

I M Mitchell, RW Logan, J C S Pollock, M P G Jamieson

AbstractObjective-To assess the nutritional sta-tus of children with congenital heart dis-ease.Design-Six anthropometric, 24 bio-chemical, and five haematologicalmarkers of nutritional wellbeing weremeasured in children with congenitalheart disease.Setting-The west of Scotland.Patients-48 children admitted consecu-tively for surgical correction of congeni-tal heart disease.Main outcome measures-Height,weight, and triceps and subscapular skinfold thicknesses were considered abnor-mal if they were below the third centilecompared with standard reference datafor age matched British children. Mid-arm circumference and arm muscle cir-cumference were considered abnormal ifthey fell below the fifth centile comparedwith standard data. Biochemical andhaematological data were compared withage matched and locally validated labora-tory normals.Results-A marked degree ofundernutri-tion was evident in all children; 52% hadweight less than the third centile, 37%were below the third centile for height,and 12-5% were below the third centilefor triceps skin fold thickness and 18-8%for subscapular skin fold thickness. Mid-arm circumference and arm muscle cir-cumference were below the fifth centile in20*1% and 16*7% of children respectively.Five or more of the 29 biochemical andhaematological measurements wereabnormal in 83-3% of patients; 10 ormore were abnormal in 12-5% ofpatients.Conclusions-Children with congenitalheart disease are frequendy undernour-ished, irrespective of the nature of car-diac defect and the presence or absenceof cyanosis.

(Br HeartJ_ 1995;73:277-283)

Keywords: nutritional status; congenital heart disease;paediatrics

Congenital heart disease accounts for moreinfant deaths than all other congenital defectsput together' 2; about half of those who surviverequire surgery within the first year of life,equivalent to an "infant surgery rate" ofapproximately 1400 per million live births.34Despite this significant workload and recent

advances in medical and surgical managementthe pre-existing state of nutrition is one aspectof congenital heart disease that has receivedlittle attention.

It is a popular view that children with con-genital heart disease are often small andundernourished. Several studies have exam-ined height, weight, and protein status5--17 butthere has been no detailed assessment ofnutrition. As nutritional status is one of themajor determinants of the magnitude of themetabolic response to surgery 8-20 and since ithas become increasingly common to operateat an early age, poor body reserves in thesechildren may be an even more significant factorin militating against a successful outcome.

Assessment of the state of nutrition is madedifficult by the number of factors that con-tribute to nutritional wellbeing (proteinstores, fat stores, trace elements, etc.).Clinical examination alone appears to be apoor indicator of nutritional status2' 22 andmost studies therefore depend on the mea-surement of specific markers. Weight is thetraditional guide but in reality is a crude esti-mate which may be affected as much by thedegree of oedema as by the true body mass.Similarly, protein status is a useful biochemi-cal guide, but measurement of this variablealone gives no estimate of other body reserves.This argument is true of all measurementsand there is clearly no single variable which,on its own, can accurately define the state ofnutrition.2324 The Seltzer index (relying on thealbumin concentration and lymphocytecount),25 and the nutritional assessment ofBlackburn et al,23 are more useful, yet there isno scoring system which can adequately com-bine multiple measurements into a moreaccurate "nutritional index" that can be cal-culated and compared with reference data. Inthe absence of such an index we haveattempted to define the state of nutrition asaccurately as possible by making multiplemeasurements of anthropometric, biochemi-cal, and haematological factors in order toconstruct a nutritional profile.The aim of this study was therefore to

determine the nutritional status of a cohort ofchildren with congenital heart disease aboutto undergo corrective open heart surgery andto define which groups of patients were mostseverely undernourished.

Patients and materialsPATIENTSThis study was approved by the local hospital

Department ofCardiac Surgery,Royal Hospital forSick Children,Yorkhill, GlasgowI M MitchellJ C S PollockM P G JamiesonDepartment ofBiochemistry, RoyalHospital for SickChildren, Yorkhill,GlasgowRW LoganCorrespondence to:Mr I M Mitchell,Department of CardiacSurgery, Leeds GeneralInfirmary, Great GeorgeStreet, Leeds LS 1 3EX.Accepted for publication17 October 1994

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ethics committee and informed consent wasobtained from the parents of the children.

Forty eight unselected, consecutive admis-sions to the paediatric cardiac surgical unitwere studied at the Royal Hospital for SickChildren, Glasgow. The study comprised 23males and 25 females (mean (range) age 1 52(2 days-4-77) years) with congenital heart dis-ease who were about to undergo urgent orelective surgery involving cardiopulmonarybypass. Children who had had previoussurgery (cardiac or otherwise), those with fociof active infection or inflammation, or withany other coexisting pathological condition orchromosomal abnormality, those of non-Caucasian ethnic origin and children whohad recently lived abroad or who were takingany form of dietary supplement wereexcluded.The cardiac defects in this group of chil-

dren represented a typical distribution of con-genital heart disease (table). Twelve patientshad cyanosis.

NUTRITIONAL SURVEYThirty five variables were measured in eachpatient to determine the overall state ofnutrition. These measurements were dividedinto three categories: anthropometric (six),biochemical (24) and haematological (five).

AnthropometryAnthropometric measurements were per-formed on the day before operation, using thesame equipment throughout the study, by oneof us (IMM) to eliminate inter-observererror.26 27

Height was measured in centimetres andnude weight in kilograms. Mid-arm circum-ference was measured at a point mid-waybetween the acromion process of the scapulaand the olecranon process of the ulna in thedependent left arm, with the elbow flexed to90°. This was recorded in centimetres, using aflexible, non-stretch tape.

Triceps skin fold thickness was measuredwith the arm by the patient's side, at the samemidpoint and in a vertical line up from theolecranon. Subscapular skin fold thicknesswas measured just below the angle of thescapula also on the left side. The same pairof Harpenden skinfold calipers (BritishIndicators, St Albans) was used throughoutand the measurement recorded on each occa-sion was the average of three attempts.27

Distribution of congenital heart disease in 48 children fromthe west ofScodand

No ofpatients

Atrial septal defect 11Ventricular septal defect 9Tetralogy of Fallot 7Transposition of the great arteries 5Atrial septal defect/pulmonary stenosis 4Atrioventricular septal defect 3Double outlet right ventricle 3Aortic stenosis 2Double outlet left ventricle IPartial anomalous pulmonary venous drainage 1Total anomalous pulmonary venous drainage 1Tricuspid valve membrane 1

The arm muscle circumference (AMC) wascalculated from direct measurements of mid-arm circumference (MAC) and triceps skinfold thickness (TST) using the formula28:

AMC = MAC - 7r(TST)

where AMC and MAC are in centimetres andTST is in millimetres.

Anthropometric measurements wereassessed in terms of centile distribution, asthis method of analysis allows easy recogni-tion of abnormal groups within a normallydistributed population.29 Height, weight, tri-ceps skin fold thickness, and subscapular skinfold thickness were compared with standardreference data for British children(Castlemead Publications, Welwyn GardenCity) based on studies conducted by Tannerand Whitehouse.30-32 Measurements weredeemed abnormal if they were less than orequal to the third centile.Mid-arm circumference and arm muscle

circumference were compared with datareported by Jelliffe28 and considered as abnor-mal if they fell below the fifth centile.33

Validation of reference data The standardanthropometric tables quoted here are thosecurrently in use in most nutrition clinics.These were constructed from data largelyobtained in the 1960s based on observationsmade in the Midlands and the southeast ofEngland. Clearly, growth patterns of childrenfrom the west of Scotland in the 1990s maydiffer, but construction of local referencetables would be a major undertaking andbeyond the scope of this investigation. In anattempt to validate use of the published data,however, height, weight, triceps skin foldthickness, subscapular skin fold thickness,mid-arm circumference, and arm muscle cir-cumference were measured in a cohort of 35children of similar age attending the hospitalday unit for minor surgery. These childrenwere not by definition a random sample fromthe community but can be considered as typi-cal. None had any illness or abnormality otherthan that for which they were attending; theseincluded minor otolaryngological problems,requiring tonsillectomy, insertion of grom-mets, etc., ophthalmic problems (squints,etc.), and minor general surgical conditions(phimosis, hernia, etc.).

Biochemical measurementsBlood and urine samples for biochemical andhaematological tests were obtained betweenthe hours of 0800 and 1000 to eliminate thepossibility of diurnal variation.

Sample analysis was performed at thedepartment of biochemistry, Royal Hospitalfor Sick Children, Glasgow. The followingvariables were measured using standard labo-ratory techniques: sodium, potassium, chlo-ride, bicarbonate, urea, creatinine, calcium,phosphate, alkaline phosphatase, aspartatetransaminase, alanine transaminase, y glu-tamyl transferase, bilirubin, total protein,albumin, glucose, cholesterol, triglyceride,magnesium, zinc, copper, transferrin, Creactive protein, and urine 3-methylhistidine.



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Nutritional status of children with congenital heart disease

The results were compared with normal agematched reference data from our laboratory.

Haematological measurementsBlood samples were obtained as describedearlier and analysed to determine the haemo-globin concentration, white cell count, packedcell volume, and serum and red cell folateconcentrations. Sample analysis was per-formed at the department of haematology,Royal Hospital for Sick Children, Glasgowand results compared with our own agerelated normal reference data.

DATA ANALYSISData analysis was performed both for thewhole group and for subgroups to determinethe influence of cyanosis and different typesof congenital heart disease on the state ofnutrition.

ResultsVALIDATION OF ANTHROPOMETRIC REFERENCEDATAAnthropometric data from 35 children aboutto undergo minor surgery were compared

with standard reference charts (figs 1-3).Results, graded into centiles, conform toroughly normal distribution, and allowing forthe small sample size, these findings supportthe use of the standard reference data in ourcommunity and circumstances.

NUTRITIONAL SURVEY OF CHILDREN WITHCONGENITAL HEART DISEASEResults obtained from 48 patients about toundergo surgical correction of congenitalheart disease were considered in relation tothe whole group and to certain subgroups.

Whole Group analysisAnthropometry Figures 4-6 demonstrate amarked shift towards smaller size in thesix variables studied. For example, 52% ofchildren with congenital heart disease hada weight less than the third centile, morethan 37% were below the third centile forheight, 12-5% were below the third centile fortriceps skin fold thickness and 18-8% forsubscapular skin fold thickness, and 20 1%were below the fifth centile for mid-armcircumference and 16-7% for arm musclecircumference.

Figure 1 Gentiledistribution of (A) heightand (B) weight in 35normal children.

Figure 2 Centiledistribution of (A) tricepsand (B) subscapular skinfold thicknesses in 35normal children.

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Figure 3 Centiledistribution of (A) mid-arm and (B) arm musclecircumferences in 35normal children.

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Figure 4 Centiledistribution of (A) heightand (B) weight in 48children with congenitalheart disease.

Figure 5 Centiledistribution of (A) tricepsand (B) subscapular skinfold thicknesses in 48children with congenitalheart disease.

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Biochemistry and haematology These resultsdemonstrate that many biochemical andhaematological variables are abnormal in chil-dren with congenital heart disease. The inter-pretation, however, is difficult, as it isimpossible to ascertain the importance ofindividual variables to the overall wellbeing ofeach child. Albumin, transferrin, and serum

zinc are nevertheless generally accepted to beuseful indicators12"'49 and in this series were

abnormal in 64-6%, 29-2% and 16&7%respectively. In addition, urine 3-methylhisti-dine was abnormally high in 33 3%, suggest-ing a degree of active muscle wasting.C-reactive protein was minimally increased inthree patients and substantially abnormal inone (32 mg/l).

Liver function tests were abnormal in onlya few children: bilirubin and alanine trans-aminase were increased in 4-2% of patients,alkaline phosphatase in 8-3%, aspartatetransaminase in 25%, and y glutamyl trans-ferase in 2[1%. Of the remaining tests, abnor-mal concentrations were determined forplasma sodium in 4-2% of patients, chloridein 75%, bicarbonate in 54-2%, urea in 18-8%,creatinine in 45-8%, calcium in 27-1%, phos-phate in 2-1%, total protein in 45-8%, glucose

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in 4 2%, cholesterol in 20-8%, triglyceride in33-3%, magnesium in 8-3%, and copper in14-6%, potassium concentrations were nor-

mal. Abnormal values were recorded forhaemoglobin in 25% of patients (this was

expected as 25% had cyanosis), white cellcount in 4-2%, packed cell volume in 16-7%,serum folate in 41 2%, and red cell folate in25%.

Although combining results and assumingeach variable to be of equal importance maywell be invalid, this technique has been usedelsewhere40 and it is interesting that five or

more of the 29 measurements were abnormalin 83-3% of patients and 10 or more were

abnormal in 12-5% of patients.

Subgroup analysisCyanosis Twelve of 48 patients had cyanosisbefore surgery. Examination of each variable(anthropometric, biochemical, and haemato-logical) revealed no significant differencebetween those children with cyanosis andthose without cyanosis (P > 0-05; x2 test).Heart defect Children with atrial septal defects(n = 15) or tetralogy of Fallot (n = 7) were

present in sufficient numbers to be studied as

individual subgroups. There was no overall

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statistical difference between these patientsand the group as a whole with the exception ofthe plasma zinc concentration which wasabnormally low more frequently in patientswith atrial septal defects (P < 0 05; X2 test).

DiscussionThe maintenance of nutritional homeostasis isfundamental to normal health. In children,not only do the added demands of growthmake this goal more difficult to achieve, but inthose who undergo surgery, it is not surprisingthat the pre-existing state of nutrition shouldhave a profound effect on outcome. There is,for example, clear evidence of an associationbetween malnutrition and poor wound heal-ing,4l-43 impaired immunity,4"6 reduced mus-cle function,47 and an increased risk ofpostoperative pneumonia.48 In the long termmalnutrition is an important cause of cardiacdecompensation49 and myocardial atrophy.50 5'Malnutrition may also affect the stressresponse to surgery, although postoperativenitrogen losses may be less in malnourished,than in well nourished patients, because ofadaptation to cachexia and the developmentof nitrogen and protein sparing metaboliccycles.52 It has been suggested that patientsundergoing cardiac surgical procedures asso-ciated with hypothermia, narcotic analgesia,and neuromuscular blockade may have anattenuated catabolic response and lose lessnitrogen than other equivalent surgicalpatients.53 Against this suggestion, however, isthe lack of evidence correlating the degree ofhypothermia with the degree of postoperativemuscle protein breakdown.54

Adults undergoing cardiac surgery, with theexception of those patients with end stagevalvular heart disease,55-57 show little evidenceof malnutrition,5458 many patients are evenobese. It is unlikely that postoperative compli-cations leading to a relatively prolongedperiod of starvation would have much impacton the overall prognosis in patients with plen-tiful "reserves". Some patients, however, dodevelop cardiac cachexia and surgery in thisgroup is undoubtably associated with a highermortality and morbidity.55 56 59

In contrast to the adult population under-going cardiac surgery, children with congeni-tal heart disease often appear small andundernourished, but there are few studies thatformally document this,5-'4 and only three inthe modern era of cardiac surgery.'5-"7 Thecomplex nature of the operative and perfusiontechniques currently available, combined withprolonged recovery times and the possibilityof delay in starting an adequate feeding regi-men in the early postoperative period suggestthat pre-existing malnutrition might be associ-ated with a relatively poor prognosis, particu-larly in view of the trend towards earlysurgery.The origin of growth failure in children

with congenital heart disease may be unre-lated to the cardiac pathology, but perhaps isthe result of genetic or hereditary factors.Alternatively, it has been suggested that

growth retardation may be indirectly relatedand due to chronic tissue hypoxia or anincreased incidence of respiratory disease,both the result of pulmonary congestion and aleft to right shunt.6 This view has been dis-puted,12 15 however, and genuine growth fail-ure has been recorded in various congenitaldefects, being particularly severe in thoseassociated with congestive heart failure"3 andcyanosis.5 1012 Furthermore, the severity of thegrowth failure has been linked to the severityof the cardiac defect,"3 the worst affectedbeing double outlet right ventricle, tetralogyof Fallot with pulmonary atresia, and transpo-sition of the great vessels.'0 Whether the surgi-cally corrected child shows a period ofaccelerated growth ("catch-up") is disputed,'4but may in part relate to the age at whichsurgery was performed; the earlier surgery iscarried out the more likely that catch-up willoccur."3 14 60Most previous studies of nutrition and con-

genital heart disease have largely depended onmeasurements of height and weight. Thisstudy has sought to investigate the state ofnutrition in greater depth, measuring 35 dif-ferent parameters of wellbeing. While we havedemonstrated profound undernutrition ingeneral, we have not shown any relationbetween the severity of undernutrition and thetype of cardiac defect nor have we demon-strated a link with cyanosis. Interestingly,Salzer et al'7 also cast doubt on an associationbetween cyanosis and the severity of growthfailure, their observations being based not juston height and weight measurements, but alsoon subscapular and triceps skin fold thick-nesses and serum albumin and prealbuminconcentrations.As some of the children with less severe

malformations such as secundum atrial septaldefects were younger than those in some otherseries, it could be argued that these childrenwere operated on early because of failure tothrive and therefore comprise a subgroup notrepresentative of the usual surgical popula-tion. There is, however, no difference in thedegree of undernutrition between the youngerand the older children in this series and itseems justified to conclude that although chil-dren with congenital heart disease may super-ficially appear well nourished, carefulexamination will frequently reveal that theyare not.

Long-term diuretic treatment depletes zincstores6'; whether the biochemical changeswere the result of drug treatment is uncertain,but this possibility seems unlikely as medica-tion was minimal. Several children, however,might have been expected to have abnormalliver function as a result of right heart failure,yet this condition was present only in a fewand it is also unlikely that this would bedirectly responsible for any significant under-nutrition.A genuine failure to thrive therefore seems

to be a common feature of children with con-genital heart disease. There are three possibleexplanations for this finding:

(1) Inadequacy of the food supply. It is



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unlikely that this would contribute to growthfailure in a modem society with the provisionof social services. Most parents aware of theirchild's poor development are particularly wellmotivated to help.16

(2) Malabsorption62-64 or feeding difficul-ties, arising from fatigue65 and breathlessness,9for example, may restrict intake. Evidence tosupport this hypothesis derives from theobservation that oxygen consumption relativeto lean body mass or surface area is similar innormal children and those with congenitalheart disease,'5 plus the finding that force-feeding results in an improved weight gain.63Two recent studies, however, refute thisexplanation.'6 17

(3) Hypermetabolism. Despite the possi-bility of tissue hypoxia children with congenitalheart disease may have relative hypermetabo-lism66 and exhibit growth failure if the nutri-tional intake is not increased in line withincreased requirements. Hypermetabolism isa feature of congestive heart failure in adultsand although the exact cause is uncertain, itprobably depends on increased catecholamineproduction and the abnormal demands ofvarious organs, in particular the muscles ofrespiration, the myocardium, and thehaematopoietic system. Excessive thyroxinedoes not seem to contribute.62

Eighteen (age range 4-33 months) of the48 children studied here participated in a fur-ther study which used the doubly labelledwater method to determine energy expendi-ture in the week before surgery.67 This groupcomprised six children with a secundum atrialseptal defect, five with tetralogy of Fallot,three with ventricular septal defects, and oneeach with a coarctation, a double outlet leftventricle, a univentricular heart, and a pri-mum atrial septal defect. Energy expenditure(measured in kcal/kg fat free mass) was com-pared with results from age matched normalchildren. There was clear evidence of hyper-metabolism in five children with congenitalheart disease (metabolic rate increased >20%); this was not the case in the remaindernor did the findings correlate with the type ofcardiac defect or the presence or absence ofcyanosis. The cause of the observed failure tothrive in children with congenital heart dis-ease therefore remains uncertain; althoughhypermetabolism is responsible in somepatients, clearly other factors are alsoimportant.

This study was funded by grants from the Association forChildren with Heart Disorders and Tenovus-Scotland.

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