Vol. 85, Issue 1, 223-230, July 1998
Direct measurement of the energy expenditure of physical
activity in preterm infants
Patti J.
Thureen,
Robert E.
Phillips,
Karen A.
Baron,
Mark P.
DeMarie, and
William W.
Hay Jr.
Section of Neonatology, Department of Pediatrics, University of
Colorado Health Sciences Center, Denver, Colorado 80262
 |
ABSTRACT |
The energy cost of physical activity (EEA) has been estimated to
account for 5-17% of total energy expenditure (TEE) in neonates. To directly measure EEA, a force plate was developed and validated to
measure work outputs ranging from 0.3 to 40 kcal · kg
1 · day
1.
By use of this force plate plus indirect calorimetry, TEE and EEA were
measured and correlated with five activity states in 24 infants with
gestational age of 31.6 ± 0.5 (SE) wk and postnatal age of 24.8 ± 3.7 days. TEE and EEA were 69.2 ± 1.5 and 2.4 ± 0.2 kcal · kg
1 · day
1,
respectively. EEA per state was 0.5 ± 0.0 (quiet sleep), 2.4 ± 0.2 (active sleep), 2.8 ± 0.4 (quiet awake), 7.5 ± 0.8 (active awake), and 15.1 ± 2.3 (crying)
kcal · kg
1 · day
1.
This provides the first direct measurement of the contribution of
physical activity to TEE in preterm infants and will enable measurement
of caloric expenditure from muscle activity in various disease
conditions and development of nursing strategies to minimize unnecessary energy losses.
force plate; indirect calorimetry; oxygen consumption; carbon
dioxide production
 |
INTRODUCTION |
THE ENERGY COST of physical activity (EEA) has been
estimated to account for 5-17% of overall energy expenditure in
neonates (3, 5, 8, 9). These values are usually derived from indirect
calorimetry studies, which provide measurement of total energy
expenditure (TEE), resting metabolic rate (RMR), and diet-induced thermogenesis (DIT). EEA can then be estimated by TEE
(RMR + DIT). Other estimates have come from determination of
O2 consumption (
O2) in different activity
states. If these estimates are valid, EEA can account for a significant
portion of the daily energy expenditure in these infants, and in
infants with poor growth, EEA could represent a portion of the energy
balance that can be manipulated by changes in care practices.
To measure the contribution of EEA to overall energy expenditure and to
determine its contribution to the variability in TEE in preterm
infants, we sought to directly measure EEA. A force plate system was
designed that provides real-time measurements of mechanical work. In
this system the infant lies on the force plate, and the force the
infant exerts on the plate is converted to work measurements. By use of
this device in conjunction with indirect calorimetry, metabolic
measurements (i.e., TEE,
O2, CO2 production, and respiratory
quotient) and EEA determinations were performed in enterally fed,
preterm infants. TEE and EEA were also determined for different
activity states. This provides the first direct measurement of EEA as a
component of TEE in this population.
 |
METHODS |
Force Plate Design
The force plate consists of two aluminum plates (15 × 7.5 × 1/4 in. thick) with a foil strain-gauge sensor (Mini-UTC-0.75,
A. L. Design, Buffalo, NY) secured between the plates at each
corner. The full-scale range of each force sensor is 10 lbs. The system uses an 8-channel, 12-bit analog-to-digital converter (model ACE, Cybermedic, Boulder, CO) interfaced to the parallel port of a laptop
computer (model 325X, Compuadd, Houston, TX). The data-acquisition unit
provides the excitation voltage (8.3 V) for the strain-gauge sensors,
and each sensor output is routed to a separate analog-to-digital channel. The computer samples all four sensors synchronously at a
sample rate of 128 Hz. The analog signals are filtered using a 30-Hz
low-pass (antialiasing) filter before being digitized. Forces from
movement on the plate are processed to provide a continuous calorie-equivalent measurement, which is presented as 1-min rolling averages expressed as kilocalories per kilogram per day. This plate is
placed inside the isolette or calorimetry chamber and becomes the floor
of the infant bed.
Force Plate Calibration and Validation
Static calibration.
The strain-gauge sensors were individually characterized as follows:
the plate surface was divided into 50 equal 1.5 × 1.5-in. grids.
Calibration masses (Rice Lake Bearing, Rice Lake, WI) ranging from 50 to 2,500 g were placed in each grid multiple times, and the force
reading from each sensor was recorded. After subtraction of the
unloaded static force reading from each sensor's output, the
uncorrected force readings were subjected to a multiple linear regression with the expected sum of the four sensor outputs equal to
the calibrated mass. The evaluation of this regression provided a scale
factor for each sensor that was then used to correct the individual
sensor output values.
Static validation.
Static validation studies were performed to determine whether the above
scale factors for each sensor accurately measured the force produced by
a mass placed at any point on the plate. Precision masses ranging from
50 to 2,500 g were placed in each grid in multiple trials. These masses
were chosen in that they were expected to represent the minimal and
maximal masses that might be generated by the body of a preterm infant.
In initial testing it was determined that the strain-gauge sensors were
temperature sensitive over an environmental temperature range of
2-34°C. Therefore, all validation studies were conducted at
approximately the same temperature range measured inside the infant
study chamber.
Dynamic validation.
A motor-pulley arrangement was used to vertically reciprocate (i.e.,
move up and down) a known mass over a range of velocities (see
APPENDIX for apparatus design and work
calculation). For each trial, different masses, mass velocities, and
mass positions on the plate were tested. Data are expressed as work
extrapolated to a 24-h measurement
(kcal · kg
1 · day
1).
Results are presented as measured work as a percentage of predicted work.
Clinical Study
Study population.
The eligible study population consisted of nonventilated, stable,
enterally fed, growing preterm infants who weighed
2 kg at birth and
received care in the Neonatal Intensive Care Unit at the University of
Colorado Health Sciences Center. Enrollment criteria excluded infants
who had acute intercurrent illnesses or congenital anomalies. Infants
could be the appropriate size for gestational age (AGA) or small for
gestational age (SGA). Written parental consent for infant
participation was obtained before the study. The protocol was approved
by the Institutional Review Board at the University of Colorado Health
Sciences Center.
Study methods and measurements.
To determine metabolic measurements (i.e.,
O2,
CO2 production, and TEE), indirect
calorimetry was performed for ~6 h in each infant with use of a
calorimeter designed specifically for use in preterm infants, including
those who require supplemental O2
(18). Six-hour studies were performed, since this has been determined
to be the minimum measurement duration that accurately reflects daily
TEE in preterm infants (1). Calorimetry results are presented as 1-min
average values. Studies were conducted as previously described (18)
with the infant placed in a clear, Plexiglas chamber. Humidified
medical-grade compressed tank gas was used for the inspiratory gas
source (40-60% relative humidity, with relative humidity stable
within 10% for each subject, monitored using humidity and temperature
indicator HMI 31, Vaisala, Helsinki, Finland). Ambient temperature was
maintained by placing the chamber under a servo-controlled radiant
warmer. Continuous electrocardiogram and respiratory rate monitoring,
pulse oximetry, and axillary temperature measurements were performed.
After the infant was placed in the study chamber, metabolic
measurements were not recorded until after an equilibration period of
20 min. Most infants were removed from the calorimetry chamber for
feeding and nursing care for 10-20 min before each feeding.
Activity measurements were visually assigned every 1 min by
modifications of several activity scales (4, 17). Basic features of the
five activity states are shown in Table 1.
Two observers (K. A. Baron and P. J. Thureen) made all state
assignments on all infants in the study population, and interobserver
correlation of state assignments was 91%. Because the rate of activity
may change within 1 min, the primary state observed over 1 min was recorded. Work measurements made while the infant was pressing against
the side of the calorimetry hood were deleted, since this may produce
falsely high work values.
Data Analysis
Metabolic measurements were offset by 2 min after the EEA
determinations. This accounts for the average lag time between an observed infant physical event and the time required for the infant's exhaled breath to be analyzed by the calorimeter. This lag time was
previously determined for our system as the average lag time (i.e., 2 min) for a preterm infant of approximately the same size as the infants
in this study and with similar gas flows through the chamber. The
length of time used for our metabolic measurement offset is comparable
to that reported in other preterm infant studies (5, 6).
Values are means ± SE. Unpaired Student's
t-test was used to compare differences
between groups.
 |
RESULTS |
Force Plate Calibration and Validation
Static validation.
Precision masses ranging from 20 to 1,000 g were placed in each grid on
multiple trials. Results are shown in Table
2.
Dynamic validation.
Dynamic validation results (Table 3)
indicate that work recovery from the plate averaged 88.0 ± 1.1 and
97.2 ± 2.5% for work simulations of <1 and >1
kcal · kg
1 · day
1,
respectively. The plate was sensitive enough to determine the caloric
expenditure from respiratory activity at rest (Fig.
1). A typical 10-min activity
recording is shown in Fig. 2.

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Fig. 1.
Ten-second force plate recording from infant in deep sleep with no
visually detected motion. Data at 128 Hz were smoothed using a 2-s
rolling average. Respiratory rate in this infant averaged 48-50
breaths/min on cardiorespiratory monitor during this period of deep
sleep, and heart rate was 148-160 beats/min. Respiratory pattern
is identical to that detected by cardiorespiratory monitor.
|
|
Patient Studies
Twenty-four infants were enrolled in the study. Infant characteristics,
energy intake, O2 requirements,
and metabolic measurements are shown in Table
4. All infants were fed every 3 h. Five
infants were exclusively gavage fed, four were nipple fed from a
bottle, and the remainder were fed by a combination of nipple and
gavage. The EEA, TEE, and percentage of TEE accounted for by EEA for
each patient are shown in Fig. 3.
TEE was significantly greater in SGA than in AGA infants (72.7 ± 2.3 vs. 65.8 ± 1.6 kcal · kg
1 · day
1,
P < 0.05), although this was not the
case for EEA (2.5 ± 0.4 and 2.3 ± 0.3 kcal · kg
1 · day
1
for AGA and SGA infants, respectively). Medications that might affect
energy expenditure were noted. Nine infants were treated with caffeine
for apnea of prematurity, and one of these infants was receiving a
small once-daily dose of dexamethasone (Decadron) for chronic lung
disease at the end of a prolonged Decadron-tapering schedule (i.e.,
day 40 of 42 total days of therapy).
No infants were receiving sedative medications. There were no
differences in TEE or EEA when the mean values for infants receiving
caffeine were compared with those for infants not receiving caffeine.

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Fig. 3.
Energy expenditure of physical activity (top), total energy
expenditure (middle), and percentage of total energy
expenditure accounted for by energy expenditure of physical activity
for each infant (bottom). Values are means ± SE; infants
are numbered as in Table 4 (i.e.,
1-24).
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|
The mean time spent in each of five activity states and the mean
caloric expenditure in each of these states are shown in Fig.
4. As has been described by other
investigators (12), preterm infants in this study spent an average of
80-90% of their time in sleep (quiet sleep plus active sleep in
Fig. 4, top).

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Fig. 4.
Time spent in each of 5 activity states (top) and for caloric
expenditure in each of these states for all infants (bottom).
Values are means ± SE.
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|
RMR in infants is generally considered to be the energy expenditure
determined by indirect calorimetry while an infant is quietly sleeping
2.5-3 h after the last meal. In this study RMR averaged 63.8 ± 1.6 kcal · kg
1 · day
1.
Energy expended for quiet breathing (i.e., the only visible motor
movement such as seen in Fig. 1) averaged 0.32 ± 0.03 kcal · kg
1 · day
1.
Not all infants actively cried during the study, but for those who did,
the increase in energy expenditure above that seen in quiet sleep
ranged from 12 to 55%. There was a linear correlation between the mean
TEE in each activity state and the numerical assignment for each state
(Fig. 5).

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Fig. 5.
Relationship between total energy expenditure in each activity state
and numerical assignment for each state. Values are means ± SE for all infants.
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|
We compared our direct measurement of EEA with an estimate of EEA based
on our data using one of the estimation methods reported in the
literature. Freymond et al. (5) estimated EEA by subtracting the
postmeal resting energy expenditure (obtained by regressing mean
recorded energy expenditure vs. activity state) from the TEE and
arrived at an EEA of 68.4
64.8 = 3.6 kcal · kg
1 · day
1.
In our study, mean postmeal RMR for all infants was 66.2 kcal · kg
1 · day
1,
and therefore EEA estimated by the technique of Freymond et al. would
be 69.2
66.2 = 2.3 kcal · kg
1 · day
1.
This estimate is very close to our mean direct EEA measurement of 2.4 kcal · kg
1 · day
1.
In this study, infants spent a majority of their time in the two
sleeping states. These states accounted for the lowest EEA. Although
some infants were gavage fed during the measurements, no work
measurements were made during nursing care or feedings involving infant
handling, since measured work might be secondary to the caregiver's
movement that is detected by the plate and not work of the infant. To
estimate the additional EEA expended during nursing care, two
investigators independently performed state assignments each minute
during nursing interventions in a subpopulation of the study infants
(n = 5). The time spent in each state
was determined, and the energy expenditure of nursing care was
determined from the product of the time in each times the average daily
energy expenditure for each state as determined from the study. In
these five infants, care periods averaged 11 min with a range of
4-25 min. One infant slept through the care periods and gavage
feeding, while at the other extreme one infant spent the majority of
the 18-min care period in states 4 and 5, with an
average EEA during this period of 19 kcal · kg
1 · day
1.
If this latter infant received care every 3 h, several more kilocalories per kilogram per day would be added to this infant's estimated EEA.
 |
DISCUSSION |
We have reported the design, validation, and clinical use of a force
plate system for measuring the mechanical work of movement in infants.
This is the first study to directly measure the EEA in preterm infants.
Previous determinations of the amount of energy expended in movement in
these infants have been estimates determined by a variety of different
techniques. In general, these have involved subtracting the measurable
components of energy expenditure from TEE.
A force plate system was designed to provide real-time measurements of
mechanical work in preterm infants. This system is analogous to the
floor-sized force plates that have been recently described in adult
whole- room calorimeters (15, 16). The authors of these studies state
that, at the time of publication, their force plate system was the most
accurate method to determine mechanical work in humans over extended
periods of time. Our system is based on the same principles.
With physical activity, internal (metabolic or muscular) and external
(mechanical) work are performed. Virtually all mechanical work done by
the body is work performed when the body moves against gravity, and
"downward" force vectors, which can be detected by load cells,
are created. Activities such as walking involve up-and-down movement of
the extremities against gravity plus movement of the body's center of
gravity, both of which generate downward forces. As such, when an
infant makes horizontal "swimming" motions with the arms and
legs, the infant's center of gravity changes, and this is detected by
our force platform and converted to work equivalents. Occasionally,
horizontal movement occurs without a change in the center of gravity if
this movement is countered by an equal and opposite movement, and the
summation of the mechanical work performed does not produce a net
downward force. In our experience involving hundreds of hours of
close infant observation, even the smallest arm or leg motions are
detected by the force platform.
This force platform allows for reasonable estimates of external work.
The measurement of internal work is extremely difficult, because it
involves measurement of TEE by a technique such as indirect calorimetry
with the subtraction of other sources of energy expenditure (i.e.,
mechanical work, DIT, basal metabolic rate, and energy expenditure of
growth), and some of these values are indirectly derived. In this study
we sought to measure only external or mechanical work. The internal
work of physical activity was not, and cannot practically be, measured.
There have been several attempts to estimate energy expenditure at
different levels of activity (3, 13, 14). The first detailed
determination of the relationship of activity score to energy
expenditure was by Freymond et al. (5). They described a curvilinear
relationship (3rd-degree regression curve,
r = 0.752) between the full (10-point)
Bruck's activity score and energy expenditure but a linear
relationship with use of a simplified scale that more closely resembled
the modified scale used in our study. In our study there was a strong
linear correlation between the mean TEE in each activity state and the
numerical assignment for each state (Fig. 5). All activity
scales have somewhat arbitrary numerical assignments. However, they are
useful in assessment of activity.
The TEE in our study of 69.2 kcal · kg
1 · day
1
is comparable to the values of 66.4 kcal · kg
1 · day
1
reported by Sauer et al. (11) in infants after the 1st wk of life and
68.4 kcal · kg
1 · day
1
reported by Freymond et al. (5). The somewhat higher TEE in our study
than in similar populations in other reports (1, 3, 9, 12) may have
been partly due to the large number of SGA infants in this study, and
as a group their TEE was higher than that of AGA infants.
The mechanical work of quiet breathing in this study was 0.32 ± 0.03 kcal · kg
1 · day
1, or
0.4% of simultaneous TEE, and in this population of healthy, growing
preterm infants it had a minimal effect on overall energy expenditure.
This force plate is not designed to measure work of breathing, but it
would probably give a good estimate of work of combined lung and
abdominal displacement involved with breathing. Although not easily
done, actual work of breathing is probably best measured by measuring
O2 per unit of ventilation
with the remainder of the body in a "quiet" state so that there
is no contribution to
O2 by
nonrespiratory muscles (10). Estimation of the work of breathing in
preterm infants with respiratory distress has been problematic. In the
first few days of life, there are reports of a strong correlation of
O2 with ventilatory index
(19) and no correlation between the two (7). In preterm infants with
more chronic lung disease, a correlation between ventilatory index
and
O2 has been demonstrated,
although the spontaneous breath rate did not vary (2). The small muscle
mass in these infants may limit the amount of energy that can be
expended with breathing.
Actual daily TEE of mechanical work is probably slightly higher than
that determined by our study for several reasons. First, work recovery
averaged 90%, as might be expected with a mechanical device, but this
would add only 0.3 kcal · kg
1 · day
1
to the work measurement value. In addition, no work measurements were
made during nursing care or feedings involving infant handling, since
measured work might be caused by caregiver movement that is detected by
the plate and not movement of the infant. Thus, on the basis of the
observational study during nursing care, it is not unreasonable to add
1-3
kcal · kg
1 · day
1
to our measured value of 2.4 kcal · kg
1 · day
1
(depending on an infant's relative activity compared with other infants) to derive a value for EEA in this patient population.
In summary, this study is the first to directly measure the EEA in
infants. The majority of variability in individual patient caloric
expenditure is attributable to the stress of nursing care. For most
stable preterm infants, work expended in motor activity accounts for
only a small component of TEE (3.5%). However, for infants with poor
growth, excessive irritability, or poor response to nursing care and
interventions, energy expenditure from physical activity could have a
major impact on growth.
 |
APPENDIX |
Dynamic validation model: calculation of predicted dynamic work.
A calibrated mass hanging from a circular pulley, which
is mounted on a fixed base (Fig. 6), is
moved to different positions on the platform. The calibrated mass,
radius of the pulley, and number of revolutions of the pulley per
minute can be varied to produce different amounts of work. The
predicted work is calculated as shown below and is compared with actual
work measured by the platform.

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Fig. 6.
Schematic of calibrated mass and pulley used to validate measurements.
Abbreviations are as follows: b and
x', points on pulley;
r, radius;
O, center; , angle;
m, mass.
|
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A circular pulley of radius
r0 and center
O rotates at a fixed rate
. A cable
runs from point x' of the
pulley, over point b, and attaches to
mass m0. As the
pulley rotates, the length of the cable segment from
x' to
b changes from a minimum of
(r1
r0)
to a maximum of
(r1 + r0).
The distance s moved by the mass as a
function of angle
is
This
distance translates to a relative height change against the force of
gravity. The total work (W) required
to raise or lower the mass is equal to the change in potential energy
of the mass
where
a0 is
acceleration due to gravity.
A discrete-time model of the mass motion may be obtained by computing
the value of
as a function of time and rotation rate
where
i is a discrete sample number,
t is
time-sampling interval, and
is rotation rate (in
revolutions/min).
The height at each sample point (s)
is computed with the distance equation above for each sample
i. The instantaneous velocity (v), acceleration
(a), and force (f) may then be
computed
The incremental work
(wi) at each
sample point is defined as force times (average) distance
The model thus provides predicted force and work signals given
an ideal distance signal. When the physical system is run, the force
platform records the force signal and derives the distance and work
signals
Figure 7 provides a sample of predicted and
measured force signals for a 560-g weight reciprocating at 105 revolutions/min. The force signal is mathematically filtered to remove
high-frequency noise and the effects of digital sampling. The repeating
jagged patterns are due to gear backlash in the motor drive train.

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Fig. 7.
Example of predicted and measured (filtered or smoothed) force signals
detected by force platform from a validation trial in which a 560-g
weight reciprocating at 105 revolutions/min was used.
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|
 |
ACKNOWLEDGEMENTS |
This work was supported by National Institutes of Health Grants
HD-01061, HD-27827, and 5MO1-RR-00069 and by a grant from Newborn Hope.
 |
FOOTNOTES |
This work was performed at the University of Colorado Health Sciences
Center.
Address for reprint requests: P. J. Thureen, Sect. of Neonatology,
B-195, University of Colorado Health Sciences Center, 4200 East 9th
Ave., Denver, CO 80262.
Received 21 November 1997; accepted in final form 18 February
1998.
 |
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