Energy expenditure in infants in health and...

Energy expenditure in infantsin health and disease

ROSS SHEPHERD MD FRACP

R SHEPHERD. Energy expenditure in infants in health and dis-ease. Can J Gastroenterol 1997;11(1):101-104. Measurementof energy balance represents a basic theoretical concept in the de-termination of nutritional and fluid requirements in humans inhealth and disease. Infants have special nutrient requirements,more limited reserves and relative immaturity of organ function.Energy requirements of infants have been based either retrospec-tively on intakes required to achieve normal growth or on equa-tions derived from energy expenditure studies performed early thiscentury. Recently, improved techniques for studying resting en-ergy expenditure (REE), total energy expenditure (TEE) and me-tabolically active body compartments in infants have facilitatedmore accurate estimates of energy requirements. Such studies in-dicated that current reference values for energy requirements areoverestimates, and that compared with measured values, pre-dicted values vary markedly between the various predictive equa-tions with wide co-efficients of variation. In disease states withaltered body composition, such as cystic fibrosis and end-stageliver disease, predictive equations markedly underestimate bothenergy and fluid requirements. In cystic fibrosis, both TEE andREE are 25% higher than values in healthy infants. In extrahe-patic biliary atresia, energy expenditure per unit body cell mass ismarkedly elevated, suggesting that this is a catabolic condition ininfants. Current estimates of energy and fluid requirements inboth health and disease in infants need reappraisal. Bedside andfree living energy expenditure methodology should be used to de-fine accurately components of energy requirement in individualinfants.

Key Words: Biliary atresia, Cystic fibrosis, Energy expenditure, In-fants

Dépense énergétique chez des nourrissons ensanté et malades

RÉSUMÉ : La mesure de l’équilibre énergétique représente un conceptthéorique fondamental pour la détermination des besoins nutritionnels etliquidiens chez l’humain en santé et chez l’humain malade. Les nourrissonsont des besoins nutritifs particuliers, des réserves moindres et une relativeimmaturité de leurs fonctions organiques. Le calcul des besoins énergé-tiques des nourrissons s’est fondé, soit rétrospectivement sur l’apport néces-saire pour l’obtention d’une croissance normale, soit sur des équationstirées d’études sur les dépenses énergétiques effectuées au début du siècle.Récemment, l’amélioration des techniques visant à étudier la dépense én-ergétique au repos (DÉR) et la dépense énergique totale (DÉT), ainsi queles comportements métaboliquement actifs de l’organisme de nourrissonsont permis le calcul plus précis des besoins énergétiques. De telles étudesont révélé que les valeurs de référence actuelles pour ce qui est de l’apporténergétique sont surestimées et en comparaison avec les valeurs mesurées,les valeurs prédites varient considérablement selon les équations deprévisibilité et ce, avec de forts coefficients de variation. En présence demaladie et d’un déséquilibre organique, par exemple en présence de muco-viscidose ou de maladie hépatique terminale, les équations prédictivessous-estiment nettement les besoins énergétiques et liquidiens. Dans lamucoviscidose, les DÉR et les DÉT sont de 25 % plus élevées que chez lenourrisson sain et cela est principalement dû à des variations génotypiques.Dans l’atrésie biliaire, la dépense énergétique par masse cellulaire unitaireest nettement plus élevée, ce qui donne à penser qu’il s’agit d’une maladiecatabolique chez les nourrissons. Les calculs actuels des besoins énergé-tiques et liquidiens, tant chez le nourrisson en santé que chez le nourrissonmalade, doivent être réévalués. Les méthodes portant sur les dépenses én-ergétiques au repos ou non doivent être utilisées pour définir des compo-santes plus précises des besoins énergétiques des nourrissons.

This paper was part of a symposium entitled ‘Selected topics in pediatric gastroenterology and nutrition’ held in October 1995 to honour theacademic career of Dr Gordon G Forstner

Department of Gastroenterology, Hepatology and Nutrition, Royal Children’s Hospital, and Children’s Nutrition Research Centre, Departmentof Child Health, University of Queensland, Brisbane, Australia

Correspondence: Dr RW Shepherd, Department of Child Health, Royal Children’s Hospital, Herston, Brisbane, Queensland, Australia.Telephone 7-3-365-5476, fax 7-3-253-1981, e-mail [email protected]

PEDIATRIC GASTROENTEROLOGY

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Infants are entirely dependent on their attendants for food.Each vital function of the growing body has an energy de-mand that must be met. In this age group – in which there isstill relative immaturity of many organ functions – nutrientrequirements per unit body weight are greater than at anyother time of life and nutrient reserves are more limited. De-termination of energy requirement in infants has been basedeither on the retrospective evaluation of nutrient intakes toachieve normal growth or on equations derived from studiesof resting energy expenditure (REE), mostly performed dur-ing the first half of this century. These studies have also beenthe basis for estimating maintenance fluid requirements onthe assumption that about 115 mL of water is lost for every419 J expended. In 1919 Harris and Benedict (1) formulatedtheir predictive equations based on weight, height and age tothe nearest whole year, but very few infants were used in thatstudy. Talbot et al (2) and Talbot (3) generated data by indi-rect calorimetry that have formed the basis for the 1973Food and Agriculture Organization/World Health Organiza-tion/United Nations University (FAO/ WHO/UNU) rec-ommendations for energy requirements in childhood (4),but their data’s reliability was questioned by Schofield (5)who presented new equations derived from REE measure-ments pooled from a number of studies in limited age catego-ries (infants were in a ‘birth to three years’ age group).

The data from Talbot (3) formed the theoretical corner-stone for the prediction of maintenance fluid requirementsin infants developed by Holliday and Segar (6), and arewidely quoted in standard pediatric textbooks (7). Theseequations have also been used by some groups to evaluatechanges in energy expenditure in various disease states (8,9).Their validity is questioned, however, because of recognizedalterations in body composition in these states, particularlywith respect to the body cell mass which represents theoxygen-exchanging, work-performing, body compartment(10).

The total energy requirements of an infant can be dividedinto three major components: energy expended in maintain-ing essential body functions (basal metabolic rate), whichincludes the synthetic costs of growth; energy used in physi-cal activity and thermogenesis; and energy deposited as newtissue. Attempts to quantify these different components ofenergy requirement, until fairly recently, have been either oflimited accuracy or impossible. Although one can measurebasal metabolism by indirect calorimetry, the calorimetrictechniques probably are of limited accuracy for infants, andthe current equations used are of doubtful validity. The re-cent extension of the doubly labelled water method into thefield of infant nutrition and developments in field tech-niques such as heart rate monitoring now make the measure-ment of total energy expenditure (TEE) theoreticallyachievable. Combining these techniques with the use ofdedicated infant indirect calorimetry to measure REE, it ispossible to derive estimates for all components of energy re-quirement. With the advent of noninvasive methods ofmeasuring body cell mass and other body compartments, ap-propriate reference can be made to energy expenditure per

unit of metabolically active cell mass for the study of diseasestates where altered body composition is present. The bodycell mass, which can be measured by total body potassiummeasurements, appears to be the most appropriate frame ofreference against which energy expenditure should be stud-ied in these situations (10). The effect of disease states onresting energy and TEE in infants has been poorly studied.

At the Children’s Nutrition Research Centre, RoyalChildren’s Hospital, Brisbane, Australia, we developed tech-niques for measuring both TEE and REE in relation to non-invasive body composition analysis. Using them, we (11)reviewed the reliability of commonly used predictive equa-tions for estimating energy expenditure in infants in bothhealth and disease, and developed preliminary data for meas-uring both total and resting body expenditure in infants withspecific disease states known to affect body composition,such as cystic fibrosis (CF) (11,12) and end-stage liver dis-ease.

REE IN INFANCYMethodology: The author and co-workers have developed amicroprocessor-controlled, portable, indirect calorimeter de-signed primarily for use in spontaneously breathing infantsand young children (11). Details of the design have been pub-lished previously (11). The device has high resolution accu-racy and response time with an overall accuracy of0.6%� 2.2%. The associated software makes allowances fortemperature, relative humidity and barometric pressure, andenables calculations of the volumes of oxygen consumptionand carbon dioxide production to be displayed continuouslyto define steady state concentrations and to enable later edit-ing for noise from episodes of agitation. Usually two measure-ments of REE are obtained 3 h after feeding, separated by a

Shepherd

TABLE 1Equations used for estimation of basal energy expendi-ture in infants

Harris-Benedict (kcal/day)*Boys: REE = 66.473 + 5.003 x height (cm) + 13.752 x weight (kg)

– 6.755 x age (years)Girls: REE = 655.096 + 1.850 x height (cm) + 9.563 x weight (kg) –

4.676 x age (years)

Schofield (reference 5), weight only (MJ/day)Children younger than age three years

Boys: REE = 0.249 x weight (kg) – 0.127Girls: REE = 0.244 x weight (kg) – 0.130

Schofield (reference 5), weight and height (MJ/day)Children younger than age three years

Boys: REE = 0.0007 x weight (kg) + 6.349 x height (m) – 2.584Girls: REE = 0.068 x weight (kg) + 4.281 x height (m) – 1.730

FAO/WHO/UNU (kcal/day)*Children younger than age three years

Boys: REE = 60.9 x weight (kg) – 54Girls: REE = 61.0 x weight (kg) – 51

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102 C�� J G�� V�� 11 N� 1 J��/F�� 1997

30 min rest period. There is a 3 min stabilization period fol-lowed by 20 mins of sampling. Measurement is started onlyafter a steady state in the volume of oxygen and carbon diox-ide consumption is obtained as defined by variants of lessthan 5% for a 30 s period. Thereafter these two volumes arecalculated every 20 s.REE in healthy infants: The author and colleagues havestudied REE in 44 healthy infants aged 0.44�0.29 years.Mean � SD REE was 0.21�0.02 MJ/kg/day for both healthygirls and healthy boys. No significant differences were notedin mean REE for weight between those older versus youngerthan six months of age, those bottle-fed versus breast-fedand those in a percentile weight for age greater or less thanthe 90th percentile. Compared with measured values, pre-dicted values from the various equations available (Table 1)varied markedly among equations, generally overestimat-ing REE in these healthy infants (Harris Benedict equation,182%�63% of measured values; FAO/WHO/UNU equa-tion, 106%�14%; Schofield [5] 106%�11%) (11). Using ageneralized linear model of variance, the author and hisgroup observed marked variability in the variance of the fourdifferent values for REE (one measured and three predicted)for all subjects combined, as well as for the subsets analyzed(male versus female; age younger or older than six months;and ideal body weight versus below ideal weight). Thus, noneof the predictive equations gave an accurate estimate of REEin individual healthy infants. Hence, energy and fluid re-quirements in individual infants may be wildly overesti-mated. An example of the measured REE for a healthy 7 kgmale infant versus predicted values is given in Table 2. Re-view of the derivation of all of the currently used predictiveequations calls into question the validity of using them in in-fants.REE in infants with disease states – CF: The author andco-workers (11,12) evaluated REE in 20 infants with CF ina cross-sectional study. Mean REE for infants with the�F508/�F508 genotype was 0.27�0.03 MJ/ kg/day, whichwas significantly higher than mean REE of age-, sex- andheight-matched controls (P

Figure 1 illustrates the principle behind the doubly labelledwater method. An accurately weighed oral dose of water la-belled with the stable isotopes 2H and 18O is administered.The 2H labels the body’s water pool and the 18O labels bothwater and bicarbonate pools, which are in rapid equilibriumthrough the carbonic anhydrase reaction. The turnover ratesof the two isotopes are measured by analysis of serial urinesamples collected over five to seven days. The 2H rate con-stant represents water turnover and the 18O rate constantrepresents water plus carbon dioxide turnover, from whichcarbon dioxide production can be derived by determiningthe difference. Energy expenditure is calculated from carbondioxide production using indirect calorimetric calculationsthat require an estimate of the mean respiratory quotientover the entire measurement period.TEE in healthy infants: Davies et al (14) prospectivelyevaluated 41 normal, full-term infants at 1.5, three and six

months of age. Mean TEE was 0.27, 0.28 and 0.33 MJ/kg/day,respectively. These authors developed percentiles for TEE inearly infancy and suggested that the current dietary guide-lines for healthy infants may be a prescription for overfeeding(17) based on estimations of predictive equations.TEE in infants and disease states: Only limited studies ofTEE have been done in infants with altered body composi-tion and disease states. The author and his group studied CFinfants and children younger than two years of age withoutsignificant lung disease and found that TEE was 25% higherthan in healthy infants (15). These earlier studies were notcontrolled for alterations in body composition, although theCF group as a whole had reduced metabolically active cellmass compared with the control group, which tended to out-weigh the possible contribution of altered body compart-ments. These studies, in conjunction with the REE studiesindicated earlier, suggest that CF infants are unable to com-pensate for the increased REE by a reduction in activities,which accounts for the difference between TEE and REE in-cluding, in infants, the synthetic cost of growth, energy usedin physical activity, thermogenesis and energy deposited asnew tissue.

CONCLUSIONSCurrent estimates and recommended energy and fluid re-quirements in infants in both health and disease need reap-praisal. Current predictive equations tend to overestimateenergy expenditure in healthy infants and underestimate en-ergy expenditure in infants with CF and liver disease. Theacquisition of bedside energy expenditure methodology isneeded to define accurately all components of energy re-quirement in individual infants. In particular, measurementof TEE by the doubly labelled water technique and its valid-ity in infants is superior to any other available method basedon measurement of either intake or expenditure. The 1985FAO/WHO/UNU Report (4) stated that, “in principle itwould be desirable to determine the requirements of childrenin the same way as for adults, from measurements of energyexpenditure”. This now appears to be possible.

Shepherd

Figure 1) Schematic explanation of the doubly labelled water method,where k is a rate constant for isotope disappearance, r is a production rate,and subscripts d and o refer to 2H and 18O, respectively

REFERENCES1. Harris J, Benedict FA. A Biometric Study of Basal Metabolism in Man

[Publication No 279]. Washington: Carnegie Institute of Washington,1919.

2. Talbot F, Wilson E, Worester J. Basal metabolism of girls:physiological background and application of standards. Am J DisChild 1937;53:274-7.

3. Talbot FB. Basal metabolism in children. In: Brennemann G, ed.Brennemann’s Practice of Pediatrics. Maryland: Prior, 1949.

4. World Health Organization. Energy and protein requirements: reportof a joint FAO/WHO/UNU expert consultation [WHO TechnicalReport Series No 724]. Geneva: World Health Organization, 1985.

5. Schofield C. Predicting basal metabolic rate, new standards and reviewof previous work. Hum Nutr Clin Nutr 1985;39C(Suppl 1):5-42.

6. Holliday MA, Segar WE. The maintenance need for water inparenteral fluid therapy. Pediatrics 1957,19:823-32.

7. Adelman RD, Solhung MJ. Fluid therapy. In: Behrman RE, KliegmanRM, Arvin AM, eds. Nelson Textbook of Pediatrics, 15th edn.Philadelphia: Saunders, 1996:206-10.

8. Tilden S, Watkins S, Thong T, Jeevanandam M. Measured energyexpenditure in pediatric intensive care patients. Am J Dis Child1989;143:490-2.

9. Vaisman N, Pencharz P, Corey M, et al. Energy expenditure ofpatients with cystic fibrosis. J Pediatr 1987;111:496-500.

10. Kinney JM, Lister J, Moore FD. Relationship of energyexpenditure to total exchangable potassium. Ann NY Acad Sci1963;110:711-22.

11. Thomson MA, Buccolo S, Quirk P, Shepherd RW. Measured versuspredicted resting energy expenditure in infants: a need for reappraisal.J Pediatr 1995;126:21-7.

12. Thomson MA, Wilmott RW, Wainwright C, Masters B, Francis PJ,Shepherd RW. Resting energy expenditure, pulmonary inflammationand genotype in the early course of cystic fibrosis. Pediatr Pulmol1995;2(Suppl 12):261. (Abst)

13. Greer R, Shepherd RW, Cleghorn GJ, Bowling FG, Holt T.Evaluation of growth in changes in body composition followingneonatal diagnosis of cystic fibrosis. J Pediatr Gastroenterol Nutr1991;13:52-8.

14. Davies PSW, Ewing G, Lucas A. Energy expenditure in early infancy.Br J Nutr 1989;62:621-9.

15. Shepherd RW, Holt TL, Vasques-Velasquez L, Coward WA, PrenticeA, Lucas A. Increased energy expenditure in young children withcystic fibrosis. Lancet 1988;i:1300-3.

16. Vasques-Velasquez L. Energy expenditure and physical activity ofmalnourished Gambian infants. Proc Nutr Soc 1988;47:233-9.

17. Prentice A, Lucas A, Vasques-Velasquez L, Davies PS, WhiteheardRG. Are current dietary guidelines for young children a prescriptionfor over-feeding? Lancet 1988;ii:1066-9.

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