Partition of Energy Metabolism and Energy Cost of Growth in the Very Low-Birth-Weight Infant

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446 PEDIATRICS

Vol. 69 No. 4 April 1982

Partition

of Energy

Metabolism

and

Energy

Cost

of Growth

in the

Very

Low-Birth-Weight

Infant

Brian

L. Reichman,

MB, ChB,

Philippe

Chessex,

MD,

FRCP(C),

Guy

Putet,

MD, Gaston

J. E. Verellen,

MD,

John

M. Smith,

PhD,

MASc,

Tibor

Helm,

MD,

PhD,

and

Paul

R. Swyer,

MB,

FRCP(London),

FRCP(C)

From the Departments of Paediatrics and Medical Engineeing, University of Toronto and Research Institute, The Hospital for Sick Children, Toronto

ABSTRACT. Energy requirements are partitioned be-tween needs for maintenance (including resting metabo-ham, thermoregulation, and muscular activity) and needs

for synthesis and storage of new tissue. The partition of

energy utilization was evaluated by 22 metabolic and

nutritional balance studies in 13 formula-fed (SMA 20/

24), growing, appropriate-for-gestational age, very

low-birth-weight infants (mean ± SE birth weight, 1,155±39

gm; study weight, 1,271 ± 60 gm; age at study, 21 ± 2

days; weight gain, 16.8 ± 1 gm/kg/day). Continuous

open-circuit, indirect calorimetry was performed for periods of

6 ± 0.25 hours in a thermoneutral environment. Results

expressed as mean kilocalones per kilogram per day (±

SE) were: energy intake, 148.6 (± 3.9); stool and urine

losses, 18.2 (± 1.5); metabolizable energy, 130.4 (± 3.5);

“basal” metabolic rate, 47.0 (± 0.75); energy cost of activ-ity, 4.3 (± 0.9); thermic effect offood, 11.3 (± 0.65); energy stored in new tissue, 67.8 (± 3.0). These results provide a

partition of energy utilization in very low-birth-weight

infants under thermoneutral conditions. Increased

activ-ity and a thermal environment outside the neutral range

will augment maintenance energy requirements, thus

de-creasing the amount of energy available for growth if

metabolizable energy intake remains constant. The

en-ergy cost of growth (ie, for synthesis of, and storage in, new tissue) was determined as 4.9 kcal/gm ofweight gain.

To attain the equivalent rate of intrauterine weight gain,

a metabolizable energy intake of approximately 60 kcal/

kg/day in excess of maintenance requirements of 51.3

kcal/kg/day must be provided. Pediatrics 69:446-451, 1982; energy metabolism, very low-birth-weight infant, energy cost of growth.

With modern methods of neonatal care, an

in-creasing number of preterm very low-birth-weight

Received for publication Feb 13, 1981; accepted May 19, 1981. Reprint requests to (P.R.S.) Division of Perinatal Medicine, The

Hospital for Sick Children, Toronto, Ontario, M5G 1X8, Canada.

American Academy of Pediatrics.

(VLBW) infants survive. The quality of the out-come depends on satisfactory growth during the

critical postnatal period.’3 The Committee on

Nu-trition of the American Academy of Pediatrics

states that “the goal of feeding regimens for

low-birth-weight infants is to obtain a prompt postnatal

resumption of growth to a rate approximating

intra-uterine growth.”3 These energy and nutritional

re-quirements are partitioned between needs for

main-tenance, including resting metabolism and energy

expended in thermoregulation and activity, as well

as needs for growth.

The energy balance equation46 has been defined

as: energy intake = losses in excretions + “basal”

metabolic rate + energy cost of activity +

thermo-regulatory costs + energy cost of tissue synthesis

+ energy stored in new tissue. The energy cost of

growth includes the energy required for new tissue

synthesis and the energy stored in the components

of this new tissue. The cost of tissue synthesis has

been measured as the thermic effect (or specific

dynamic action) of food.7’8 This represents energy

required for synthesis and organization of the

corn-ponents of new tissue,7’8 and has been shown to

increase with weight gain.9

We have delineated the components of this

equa-tion in VLBW formula-fed growing infants and have

determined the energy cost of growth for the first

time by continuous calorimetric studies over rela-tively long periods.

METHODS

In order to secure a homogeneous group of

in-fants, the following criteria were prerequisites for

inclusion in the study: (1) birth weight 1,300 gm;

at Viet Nam:AAP Sponsored on September 7, 2020

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N1JTRITINC6CL BIACL#{212}CNE _____________________________

URINARY NITROGEN

INDIRECT CALORIMETRY

U

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447

(2) appropriate size for gestational age; (3) growth as shown by increasing weight, length, and head

circumference; (4) formula-fed (SMA 20/24, Wyeth

Laboratories, Philadelphia). Twenty-two studies in

13 infants fulfilled these criteria and formed the

basis of this report. Repeat studies at weekly

inter-vals were undertaken in seven infants. Their clinical

characteristics (mean ± SE) are as follows: birth

weight, 1,155 ± 39 gin; gestational age, 29.3 ± 0.4

weeks; age at study, 21 ± 2 days; weight at study,

1,271 ± 60 gui; weight gain, 16.8 ± 1.0 grn/kd/day;

length gain, 1.02 ± 0.1 cm/wk; occipitofrontal

cir-cumference gain, 0.94 ± 0.08 cm/wk. Each study

comprised the following measurements: (1) energy

expenditure by indirect calorimetry; (2) nutritional

balance on three consecutive days; (3)

anthro-pornetry. The study design is shown in Fig 1.

In-formed parental consent was obtained prior to each

study.

Indirect Calorimetry

Metabolic rate (MR) was measured over a period

of 6 ± 0.25 hours by continuous, open-circuit,

mdi-rect calorimetry’0 as previously reported.”2 This

measured MR represents the infant’s total energy

expenditure including, basal metabolism, activity,

thermic effect of food over at least two meals, and

energy requirements for thermoregulation:

meta-bolic rate = basal metabolism + activity + tissue

synthesis + thermoregulation.

Each infant was studied in an incubator within

the thermoneutral range’3 under a plastic heat

shield to minimize radiant heat loss. The constancy

of the thermal conditions, assured by continuous

monitoring of environmental temperatures, and the

infants’ core and skin temperature at six different

sites, minimized heat loss or storage. Hence, energy

requirements for thermoregulation were negligible

by comparison with the other elements in the heat

balance equation. Each infant’s head was enclosed

in a plastic hood, with a plastic sleeve around the

neck. Incubator air was drawn through the hood,

which was vented through a manifold at a rate of 1

to 1.5 liter/kg/mm, precisely measured (±0.005

li-ter/min) by a Fleisch pneumotachograph e/i 7317

#00 (Dynasciences Medical Products, Blue Bell,

PA). The air leaving the hood, which was

approxi-mately 0.5% poorer in 02 and richer in CO2 as a

result of the infant’s oxygen consumption and CO2

production, was passed through a dual-channel

par-amagnetic 02 analyzer (Taylor Servornex OA184,

Crowborough, England) and an infrared CO2

ana-lyzer (Beckman LB2, Palo Alto, CA); the incubator

air was simultaneously analyzed. From the

differ-ences in 02 and CO2 concentration between air

entering and leaving the hood, together with the

ANITHROPOMETRY

WEIGHT

#{149}

S S S S #{149}

#{149}

LENGTH S

.

HEAD CIRC.

f

, ,

DAY 0 1 2 3 4 5 6 7

Fig 1. Protocol for investigation of energy metabolism

and growth in very low-birth-weight (VLBW) infants. Each study comprised a three-day nutritional balance measuring energy intake, and losses in excretions; energy

expenditure by indirect calorimetry on second day of

balance; and anthropometric measurements.

flow rate, the infants’ 02 consumption (O2), CO2

production (CO2), and respiratory quotient (R)

were calculated. The measured gas volumes were

reduced to standard temperature and pressure, dry,

and corrected for volume changes due to variation

in R from 1.0.’#{176}During the test, urine was collected

and the urinary nitrogen excretion rate was

deter-mined, enabling calculation of the nonprotein R

and Vo2. The metabolic rate (kcal/kg/day or kJ/

kg/day) was calculated from the caloric value of 02

for the specific nonprotein R and V02. The gas

analyzers were calibrated at the start and end of

each study using analyzed gases for CO2, and air for

02. Furthermore, we have determined the accuracy

of the indirect calorimeter in measuring Vo2, Vco2,

and R to be ± 2% by the combustion of weighed

amounts of butane gas (E. Stettler and E. J#{233}quier,

personal communication, 1979) which yield an R of

0.615.

Activity state was monitored continuously and

scored on the Brilck scale,’5 enabling differentiation

of metabolic rate measured under resting

condi-tions, from the metabolic rate measured during the

whole experiment. Resting metabolic rates were

determined for periods of ten to 30 minutes

pre-prandially (within one hour prior to a feed) and

postprandially (within one hour subsequent to a

feed) with the infant in a resting state (Brilck scale:

-3, -4) for at least ten minutes prior to the

mea-surements. Resting preprandial measurements were

obtained in 14 studies; resting postprandial

mea-surements in 12 studies; only in eight studies were

both measurements obtained.

Nutritional Balance

The nutritional balance was determined by

mea-surernents of intake (formula) and output (urine

and stool) over a period of three days. Infants were

fed measured volumes of SMA 20/24 by gavage or

bottle as tolerated, aiming to provide a gross caloric

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448

ENERGY

COST

OF GROWTH

intake of 140 kcal/kg/day by 2 weeks of age. Energy

content of the formula was determined using the

manufacturer’s stated content (SMA 20/24: grams!

100 ml) for fat (3.6/4.32), carbohydrate (7.2/8.64),

and protein (1.5/1.8). These values were confirmed

by random analysis of 15 aliquots of formula.

Ca-loric values of 9.25 kcal/gm for fat, 3.95 kcal/gm for

lactose, and 5.65 kcal/gm for protein, representing

the energy of combustion for milk products,’6 were

used for the calculation of the energy content of the

formula as well as the energy losses in urine and

stool. Stool and urine were collected separately and

stored at -20 C until analyzed. Urinary and stool

nitrogen was measured by the micro-Kjeldhal

method.’7 The urinary and stool carbohydrates

were measured after alcoholic hydrolysis by the

method of Huggett and Nixon.’8 The fat content of

the stools was determined by the method of van de

Kamer et al.’9 Metabolizable energy intake was

determined by subtracting energy losses in the urine

and stool from the gross energy intake. The

incom-plete oxidation of protein to urea represents a

fur-ther loss of energy (5.4 kcal/gm of nitrogen in

urea).#{176}In the preterm infant 50% to 72% of urinary

nitrogen is in the form of urea.2”22 This energy loss

has been included in the calculation of the

meta-bolizable energy intake (Table).

Anthropometry

Growth pattern was evaluated from

measure-ments of weight, length, and head circumference.

The baby’s weight was determined using an Air

Shields balance (Narco Health Co, Hatboro, PA).

From these daily weight measurements the weight

gain during the week of the balance study was

averaged and expressed as grams per kilogram per

day.

RESULTS

Energy

Intake

(Table)

The routine feeding schedule provided an energy

intake of approximately 140 to 150 kcal/kg/day

(180 to 200 mi/kg/day). The mean ± SE gross

energy intake was 148.6 ± 3.9 kcal/kg/day (621 kJ/

kg/day). Losses in the urine and stool were 18.2 ±

1.5 kcal/kg/day (76 kJ/kg/day), thus the mean

metabolizable energy intake was 130.4 ± 3.5 kcal/

kg/day (546 kJ/kg/day) or 87.8 ± 1% of the gross

energy intake. The major component (77.5%) of

energy loss consisted of stool fat.

Energy Expenditure and Storage

The mean ± SE metabolic rate measured by

indirect calorimetry was 62.6 ± 0.8 kcal/kg/day

TABLE. Metabolizable Energy Intake and Breakdown of Energy Losses in Excretions (kcal/kg/day)5

Gross energy intake 148.6 ± 3.9

Energy losses Stool

Fat 14.1 ± 1.4

Carbohydrate 0.2 ± 0.1

Proteint 3.1 ± 0.3

Urine

Carbohydrate 0.40 ± 0.03

Nitrogen 0.46 ± 0.02

Total energy losses 18.2 ± 1.5

Metabolizable energy intake 130.4 ± 3.5

S Values are ± SE; n = 22.

t

Protein = nitrogen x 6.25.

t

Assuming 72% of urine nitrogen as urea nitrogen,22 and each gram of urea nitrogen has caloric value of 5.4 kcal.2#{176}

(262 kJ/kg/day). Of the metabolizable energy

in-take (130.4 kcal/kg/day), 62.6 kcal/kg/day was

ex-pended, and the remaining 67.8 ± 3 kcal/kg/day

(284 kJ/kg/day) represented the energy stored in

the components of new tissue. Thus for each gram

ofweight gain, 4.26 ± 0.26 kcal (17.8 kJ) were stored

in new tissue.

Energy Cost of Activity

In 12 studies we were able to determine the

energy cost of activity from the equation: metabolic

rate = resting postprandial MR + activity (where

resting postprandial MR = “basal” metabolism +

tissue synthesis).

By subtracting from the infants’ measured MR

(62.2 ± 1 kcal/kg/day), their resting postprandial

MR (57.9 ± 1.2 kcal/kg/day), the energy cost of

activity was determined as 4.3 ± 0.9 kcal/kg/day

(18 kJ/kg/day).

Energy Cost of Tissue Synthesis

The energy required for tissue synthesis or the

thermic effect of food was determined from the

postprandial increase in heat production. Eight

paired measurements of resting preprandial and

resting postprandial MR were obtained. In six

in-fants (fed every two hours) the MR rose from 55.4

± 1.7 preprandially to 59.0 ± 1.6 kcal/kg/day

post-prandially, an increase of 3.6 ± 0.25 kcal/kg/day. In

two infants (fed every three hours) the increase was

greater (8.15 and 8.75 kcal/kg/day, respectively). It

is likely that with a longer feeding interval the

increase in postprandial heat production would be

even greater. Therefore, this figure probably

under-estimates the real energy cost of tissue synthesis.

Applying the concept that the increase in metabolic

rate with increasing weight gain gives a measure of

the energy required for tissue synthesis,7 we have

reported23 in VLBW infants the cost of tissue

(4)

%of energy kcol/kg.d intake

Global

energy intake

(148.6)

Energy 67.8 45.6

stared

Growth (79.1)

Metabolizable’

energy intake

(130.4)

:Maintenance

Imetabolism (51.3)

Energy lasses (18.2)

ARTICLES

449

thesis to be 0.67 kcal (2.8 kJ)/gm of weight gain,

which for the present study group gaining weight at

a mean rate of 16.8 ± 1 gm/kg/day, equals 11.3 ±

0.65 kcal/kg/day (47 kJ/kg/day).

Basal Metabolism

Measurement of the true basal metabolic rate,

requiring at least a 12-hour fast cannot ethically be

determined in the preterm infant. The measured

MR (62.6 kcal/kg/day) included basal energy

re-quirements together with energy expended in

activ-ity (4.3 kcal/kg/day) and the thermic effect of food

(11.3 kcal/kg/day). By subtraction, the basal

met-abolic rate was therefore calculated as 47.0 ± 0.75

kcal/kg/day (97 kJ/kg/day).

The resting preprandial MR (54.2 ± 1.3 kcal/kg/

day) represented the lowest measured value. This

was higher than the basal metabolic rate, as in

infants fed every two and three hours the gastric

emptying time is comparable to the feeding

inter-val,24 and the resting preprandial MR therefore

included a component of the thermic effect from

the previous feed.

Partition of Energy Utilization and Energy Cost

of Growth

The partition of the components of the energy

balance is shown in Fig 2, expressed both in absolute

terms and as a percentage of the energy intake. Of

the energy intake of 148.6 kcal/kg/day, 18.2 kcal/

kg/day were lost in the urine and stool. The basal

metabolic rate was 47.0 kcal/kg/day with 4.3 and

11.3 kcal/kg/day expended in activity and new

tis-sue synthesis, respectively. The energy cost of

growth comprised the energy stored in the

compo-nents of new tissue (67.8 kcal/kg/day or 4.26 kcal/

gm of weight gain) plus the energy cost of tissue

synthesis (11.3 kcal/kg/day or 0.67 kcal/gm of

weight gain). The energy cost of growth was 79.1

kcal/kg/day or 4.93 kcal/gm of weight gain,

repre-senting 53% of the gross energy intake.

DISCUSSION

Energy intake can either be stored in the form of

new tissue in the course of growth or it can be used

as a source of energy which may be either chemical,

electrical, or mechanical.” The final common

path-way for these forms of energy utilization leads to

the liberation of thermic energy,2#{176} which can be

measured by direct or indirect calorimetry. By

corn-bining continuous six-hour calorimetric

measure-ments with energy balance studies, we have

deter-mined the partition of the total energy intake in

formula-fed growing VLBW infants.

The metabolizable energy intake (87.8% of gross

‘‘sdh.sis fl.3 7.6 Activity 4.3 2.9

Basal’

metabolic 470 31.6

rote

Energylosses 18.2 12.2

Fig 2. Partition of energy utilization in very low-birth-weight formula-fed infants (n = 22), under thermoneutral conditions. Results are expressed as mean kilocalories per

kilogram per day and percent of gross energy intake.

energy intake), as determined by chemical analysis

of energy intake and losses, was similar to the

results obtained by Valman et al25 in a comparable

group of formula-fed (SMA S26) infants. Using a

bomb calorimetric technique for evaluation of

en-ergy intake and losses, others26’27 have similarly

shown that the mean energy retention ranges from

85.6% to 87.8% in the first six weeks of life. The

major source of energy loss was stool fat (77.5%),

which was possibly due to a decreased bile salt pool

in the premature mfant28’ or a deficiency of

pan-creatic lipase.#{176} An energy loss of 10% to 15% of

the gross intake should therefore be assumed when

determining the energy requirements of

formula-fed VLBW infants under normal clinical conditions.

The metabolic rate in infants is influenced by

age,43’32 calorie intake, and growth rate.9 In a

previous report, we have shown that the

increas-ing metabolic rate with postnatal age is

predomi-nantly due to increasing calorie intake and weight

gain. The value of 47 kcal/kg/day for the basal

metabolic rate obtained in this study is similar to

the figure quoted by Sinclair et al35 in the second to

fourth week oflife, and to measurements of minimal

resting metabolic rate determined by Brooke et al.26

Mestyan et al have obtained a figure of 39.6 kcal/

kg/day. This lower result is possibly due to a lesser

calorie intake (127 kcal/kg/day) and the fact that

their subjects were fasted for four hours prior to the study.

In our VLBW infants, only 3% of the energy

intake (4.3 kcal/kg/day) was used for activity.

Brooke et al26 evaluated the energy cost of activity

by applying oxygen costs for different activity levels

to the estimated proportion of the day spent in

these activity states. They found a high value of 23

kcal/kg/day expended in activity. This method of

calculation is subject to a number of limitations37

and may well overestimate the energy expended for

activity. Mestyan et al, using an approach similar

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450

ENERGY

COST

OF

GROWTH

to ours, estimated the energy cost of activity to be

6 kcal/kg/day, concluding that activity accounts for

only a small proportion of maintenance energy

me-tabolism in VLBW infants at neutral temperatures.

During our measurements the infants were

main-tamed under optimal conditions, with no blood

sampling, no diaper changing, and minimal

inter-ference with their environment, and they were

asleep more than 70% of the time. Deviation from

these experimental conditions would probably

in-crease the energy requirement for activity.

Further-more, under the thermoneutral conditions of our

study, the energy requirement for thermoregulation

was negligible. A thermal environment outside the

neutral range would increase maintenance energy

requirements, thus decreasing the amount of

en-ergy available for growth, if energy intake remained

constant.

Krieger7 and Ashworth8 relate postprandial heat

production to the chemical energy required for

growth, suggesting that the thermic effect of food is

a measure of the energy expended in the synthesis

of new tissue. The postprandial increase in heat

production can be determined from measurements

of resting preprandial and postprandial metabolic

rate. By this method we determined values of

ap-proximately 4 and 8 kcal/kg/day in infants fed

every two and three hours, respectively. With these

short feeding intervals the preprandlial

measure-ments will include a component of the thermic

effect of the previous meal, and this method will

therefore underestimate the cost of tissue synthesis.

The higher value of 11.3 kcal/kg/day reported in

this study was calculated using a figure for the cost

of tissue synthesis of 0.67 kcal/gm of weight gain.23

Sinclair4 has derived a similar value for the energy

cost of tissue synthesis (0.67 to 0.8 kcal/gm of

weight gain) for infants of similar weights. For the

infants studied, the energy cost of growth (79.1

kcal/kg/day) represented 53.2% of the mean energy

intake of 148 kcal/kg/day, comprising 7.6% as

en-ergy cost of synthesis and 45.6% as chemical energy

stored in new tissue. For each gram of weight gain,

4.93 kcal (20.6 kJ) were required in addition to the

maintenance energy need. This result is comparable

to those determined by others using different

tech-niques, in preterm infants6’26 and in children

re-covering from malnutrition.5

This study, as shown in Fig 2, provides a partition

of energy utilization in VLBW infants under

ther-moneutral conditions. The energy cost of deposition

of 1 gm of new tissue is 4.9 kcal. Thus, to attain the equivalent of the third trimester intrauterine weight

gain (10 to 15 gm/kg/day), a metabolizable energy

intake of 60 kcal/kg/day in excess of maintenance

energy requirement of 51.3 kcal/kg/day must be

provided.

ACKNOWLEDGMENTS

This work was supported by National Health and

Welfare of Canada grant 606-1482, Physicians Services

Incorporated Foundation, fund 9859, and Research

Insti-tute of The Hospital for Sick Children, fund 8073. Dr

Chessex is a Fellow of the Medical Research Council of

Canada; Dr Reichman is a Fellow of The Hospital for

Sick Children Foundation; Dr Putet was a Fellow of the

National Research Council of Canada (Franco-Canadian

Cultural Exchange); Dr Verellen held a NATO

Fellow-ship.

We thank Sulachona Chandramowli, Olga Stubna,

Robert Adams, and Joann Chabot for technical

assist-ance.

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DEVELOPMENTAL

PSYCHOLOGY

DEFINED

. . . is the science of the strange behavior of children in strange situations with

strange adults for the briefest possible periods of time.

Submitted by John T. McCarthy, MD.

-Urie Bronfenbrenner

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1982;69;446

Pediatrics

Tibor Heim and Paul R. Swyer

Brian L. Reichman, Philippe Chessex, Guy Putet, Gaston J. E. Verellen, John M. Smith,

Low-Birth-Weight Infant

Partition of Energy Metabolism and Energy Cost of Growth in the Very

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