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American Journal of Clinical Nutrition, Vol. 71, No. 4, 969-977, April 2000
© 2000 American Society for Clinical Nutrition

Original Research Communications

Use of infrared thermographic calorimetry to determine energy expenditure in preterm infants1,2,3

Alexandra K Adams, Ralph A Nelson, Edward F Bell and Cesar A Egoavil

1 From the Department of Family Medicine, University of Wisconsin, Madison; the Department of Medical Research, The Carle Foundation, Urbana, IL; the Department of Internal Medicine, University of Illinois at Urbana-Champaign; the Department of Pediatrics, University of Iowa, Iowa City; and the University of Illinois College of Medicine, Chicago.

2 Supported in part by Summer Medical Student Research Fellowship (to AKA) from the Society for Pediatric Research and NIH grants HD26945 and RR00059.

3 Address reprint requests to RA Nelson, Department of Medical Research, The Carle Foundation, 611 West Park Street, Urbana, IL 61801. E-mail: ralph.nelson{at}carle.com.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Measurement of infant energy expenditure in the clinical setting is difficult and is rarely done. Both indirect and direct calorimetry require long measurement periods and frequent calibration.

Objective: The objective of this study was to validate in infants a newly developed method of determining energy expenditure, infrared thermographic calorimetry (ITC), against an established method, respiratory indirect calorimetry (IC). ITC measures mean infant body surface temperature. ITC was used in conjunction with heat loss theory to calculate radiant, convective, evaporative, and conductive heat losses and thereby determine total energy expenditure.

Design: Ten healthy preterm infants were studied by obtaining concurrent ITC and IC measurements over a 3.5–5.5-h study period. Continuous IC measurements were compared with ITC measurements taken every 10 min during study periods. IC values were summed over 10-min intervals covering the 5 min before and 5 min after each ITC measurement, to allow comparisons between the 2 methods.

Results: Comparison of paired ITC and IC mean measurements for all 10 infants over the entire study period showed no significant difference between the 2 methods. However, individual paired IC and ITC values were significantly different for 7 of 10 infants. The overall mean difference between the 2 methods was 1.3%.

Conclusions: ITC is an accurate, noninvasive method for measurement of heat loss and energy expenditure in healthy preterm infants, and therefore it may be a useful clinical and research tool.

Key Words: Infrared thermographic calorimetry • energy expenditure • heat loss • indirect calorimetry • preterm infants • premature infants • metabolism • energy requirement • neonatology • neonatal nutrition • infant nutrition


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
For more than a century, investigators have been able to determine the energy expenditure of human subjects by direct and indirect calorimetry. Direct calorimetry is the determination of energy expenditure from measurement of heat loss by the body; indirect calorimetry (IC) is a method of indirectly calculating the heat produced by oxidative metabolism. Under appropriate conditions, these 2 methods have produced similar results, especially over longer periods (1, 2). Most studies of energy expenditure in infants have used indirect calorimetry because of the technical difficulties involved in using direct calorimetry. IC is easier to use than direct calorimetry technically, but IC is still rarely used for infants in the clinical setting because of the long measurement times and frequent calibration required.

Partitional calorimetry is the determination of the various forms of heat loss, which are summed to get overall energy expenditure; this method has been used previously in infants (3–7). Determinations of convective and radiant heat losses (3, 4) have been based on estimates of mean body surface temperature (MBST) derived from measurements of skin temperature at several sites. The use of thermistors and weighting of the resulting temperatures by proportional surface area to calculate estimates of nonevaporative heat loss requires assumptions about the distribution of body surface temperatures. The resulting estimates of mean surface temperature cannot be verified and may not reflect changes in vasomotor tone.

Infrared thermographic calorimetry (ITC) is an excellent method for determining MBST. When used in conjunction with heat transfer theory, MBST can be used to calculate heat losses from the body by radiation, convection, conduction, and evaporation. Total heat loss, and therefore energy expenditure, can be determined. Occasionally, corrections are necessary for changes in body temperature, which reflect heat storage. ITC is an innovative technique that enables the accurate study of heat loss, changes in energy expenditure, and metabolic heat production. ITC is a portable, fast, and noninvasive method, making it valuable for the study of human subjects in their natural environments. In adults, ITC has been used successfully to determine energy expenditure (8). ITC has been validated against IC in adults under a variety of conditions: during fasting, in patients receiving continuous parenteral nutrition, and during exercise at 30% of maximal work (8–10). The aim of this study was to validate ITC for determining the energy expenditure of infants by comparing it with the more established method of respiratory IC.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects
Ten preterm infants were enrolled. All the infants had birth weights appropriate for their gestational ages, were gaining weight at the time of study, and were in stable condition. None of the infants required supplemental oxygen or ventilatory support and none were receiving intravenous amino acids or lipids. Infant 5 was receiving intravenous dextrose and electrolytes and was the only subject that had had a serious complication, a grade 4 intraventricular hemorrhage with hydrocephalus. Four infants were initially diagnosed with respiratory distress syndrome and 2 infants, infants 8 and 10, were receiving caffeine and theophylline, respectively. Seven of the infants were fed by orogastric tube during the study period, whereas 3 infants (infants 1, 2, and 7) were removed from the incubator and bottle-fed.

Written informed consent was obtained from the infants' parents, and all infants were judged by their physicians to be in stable condition before each study. The study was approved by the University of Illinois and Carle Foundation Institutional Review Boards and the University of Iowa Human Subjects Review Committee.

Equipment
To perform simultaneous IC and infrared thermography measurements, a specially designed incubator was used. The incubator (C-86 Isolette; Air-Shields, Hatboro, PA) had a rectangular opening (43 cm long x 21 cm wide) cut in the top, with a polytetrafluoroethylene (hard, clear plastic) lid that opened for infrared scans. All of the infants were studied in this incubator regardless of the type of bed usually used (ie, crib or incubator) to minimize differences among study conditions for different infants.

Before each study, the incubator was set overnight to an air temperature equal to the infant's usual incubator temperature, or to 30°C for cradled infants. Infants 1 and 2 were studied with the incubator in the skin-temperature-servocontrol mode (incubator temperature was controlled by using a skin probe on the infant's back), but because the air temperature fluctuations were large (>1°C) with these infants, infants 3–10 were studied with the incubator set to air temperature control.

Study protocol
On the morning of the study, infants were placed into the warm incubator {approx}30 min after their first morning feeding. Infants were placed naked and prone, with their lower abdomen on a diaper. A thermistor probe was attached to the infant's back just above the iliac crest. After an equilibration period of 30 min, the incubator lid was opened briefly for the initial infrared scan, which was followed by a 10-min IC calibration period (described below). After this calibration period, a head hood was placed on the infant and respiratory IC measurements began. Oxygen consumption (O2) and carbon dioxide production (CO2) were measured continuously. The infant's respiratory and heart rates were continuously monitored and were recorded at 10-min intervals. Infant activity level was graded every 5 min by using the Brück scale, which ranges from -4 (eyes closed, no movement) to 5 (crying) (11). Infrared scans were done every 10 min throughout the IC data collection period, and scans without the calorimetry hood were performed before and after the IC data collection period. Infrared scans lasted {approx}10–30 s. Relative humidity in the incubator was recorded (Hygrotest 6100; Testotherm Inc, Randolph, NJ) every 10 min, before each infrared scan. Barometric pressure was measured (Airguide Barometer; Airguide Instrument Co, Chicago) at the beginning and end of each experiment. Most infants were fed room-temperature formula or milk via indwelling feeding tubes, but 3 infants were removed from the incubator and fed orally. For these infants, measurements were suspended during feeding and the protocol described above was simply repeated; after an equilibration period, a second measurement period began. Infants were fed between 2 and 3 h into each study. Infant 6 was fed with an infusion pump on a 3-h-on, 1-h-off cycle. The length of the study period differed for each infant; the mean length was 281 ± 50 min (range: 220–340 min).

Temperature and environmental measurements
Temperatures were measured with thermistor probes (Series 400 probes; Yellow Springs Instrument Co, Yellow Springs, OH) attached to a data logger (Data-Logging System, model 2280B; John Fluke Manufacturing Co, Everett, WA) that recorded measurements at 15-s intervals. Each probe had been tested against a certified mercury thermometer (US National Bureau of Standards, Washington, DC) in a water bath, and correction equations generated for each probe were programmed into the data logger. The temperatures of incubator air (10 cm below the center of the top), room air, the incubator wall (inner slanted surface of the front top wall), the inner wall of the polytetrafluoroethylene head hood, hood air, infant skin (midback, above the iliac crest), and the 3 black bodies (reference temperature standards for the infrared camera) were also recorded by the data logger every 15 s. Infant axillary temperature, used as a measure of infant core temperature (12), was measured several times throughout the experiment with a mercury-in-glass thermometer. Incubator temperature was adjusted if axillary temperatures were <36.5°C or >37.4°C (11).

Mean incubator wall temperature was estimated from the upper front wall temperature by using the following equation:


This equation was empirically determined on the basis of preliminary studies in which the mean incubator wall temperature was computed as the average of the temperatures of all walls weighted according to their areas. This estimate of wall temperature was then used to determine radiant heat loss (described below). Air velocity in the incubator was measured with the IC pump on and was found to be 0.01–0.02 m/s (Air Velocity Meter; Kurz Instruments Inc, Carmel Valley, CA), indicating that forced convection was negligible. The incubator lid was never opened for >1 min and no decrease in incubator temperature was noted.

Indirect calorimetry
Open-circuit respiratory IC was used to measure O2 and CO2 (7). The infant's head was enclosed in a polytetrafluoroethylene hood, the top of which had been replaced by a thin (1.3 x 10–5 m) clear polyethylene film (Glad Wrap; Union Carbide Co, New York) to minimize the effects of the hood on radiant heat loss from the head. The hood was airtight except for the exhaust ports and the opening around the neck, which was adjusted according to the size of each infant. Incubator oxygen and carbon dioxide concentrations were analyzed at the beginning and end of each measurement period. The mixture of expired gas and incubator air was drawn from the hood at a rate of 3 L•min-1•kg-1 body wt. This sample gas was passed through a drying column and the temperature and flow rate were measured. The gas was then pumped into the oxygen analyzer (Servomex OA540; Taylor Instrument Co, Rochester, NY) and carbon dioxide analyzer (Beckman LB2; Schiller Park, IL). The analyzers were attached to integrating recorders (model 252; Linear Instruments Corp, Irvine, CA) and to the data logger and the data were sampled and stored every 15 s. The gas analyzers were calibrated before each measurement period with a mixture of pure nitrogen and a calibration gas of {approx}21% oxygen and 0.8% carbon dioxide. Flow through the analyzers was controlled with an electronic flow controller and mass flow meter (Mass Flow Controller no. 8240–0414; Matheson, Lyndhurst, NJ). Mean O2 and CO2 were expressed as mL•kg body wt-1•min-1. Heat production was calculated from the mean O2 and CO2 according to the equation of Lusk (13):


Nitrogen elimination was not determined, because neglecting protein metabolism has little effect on the calculation of heat production with this method (7).

Infrared thermographic calorimetry
Infrared thermography was performed with an infrared camera (model 525; Inframetrics, Bedford, MA) that can accurately and rapidly measure body surface temperature. The infrared imaging radiometer is a small, lightweight field instrument that produces a television-compatible video output signal. A subject's naturally emitted infrared radiation (8–12 µm) is converted by a liquid-nitrogen-cooled Hg-Cd-Te detector to an electrical signal that is processed into a television picture of the thermal patterns in the scene that the camera is viewing.

A calibrated gray scale with 256 divisions (from white to black) presented across the bottom of the image in normal scanning mode provides a means of determining the temperature differential. Video processing is set such that for the 10°C surface temperature range of these studies, the central portion of the scale represents 160 gray levels, each with an associated discrete temperature. Consecutive gray levels differ in temperature by 0.06–0.07°C. This system was used and described previously (8). Figure 1Go is an infrared image of a study infant in the incubator; the gray scale is shown at the bottom of the image.



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  		FIGURE 1. Infrared image of an infant in the study incubator before application of the head hood. A gray scale is shown along the bottom of the image, with the darker end of the scale representing cooler areas and the lighter end representing hotter areas.

 
Because the camera is cooled by liquid nitrogen and cannot be tilted, it was necessary to modify the system for scanning infants by placing a front surface mirror at a 45° angle above the incubator lid. The infrared camera was positioned opposite the mirror on the other side of the incubator and scans were done by opening the lid and scanning the infant's reflected image in the mirror. Use of the mirror at this angle produces <0.06% distortion of the image (14). Infrared thermographic scans were performed without the head hood before and after the IC measurements and every 10 min during the IC measurements with the head hood in place. Although scanning can be done continuously, changes in incubator temperature were minimized by limiting each scan to 10–30 s. Before each scan, 3 black bodies were scanned as temperature references. Two of the black bodies were heated to {approx}31 and 38°C, respectively, and were used to calibrate the ratio of gray level to temperature for thermal images. Thermal patterns of heat loss (infrared scans) were recorded on videotape and digitized by microcomputer, and body surface temperatures were generated by using software programs for image analysis (IMAGE MEASURE, IM 5200 module; Microscience Inc, Seattle). The radiant, convective, evaporative, and conductive heat losses were calculated by using MBST, relative humidity, barometric pressure, and other recorded measurements in conjunction with heat loss theory.

Analysis of infrared images
For each infant, {approx}20–30 thermal images were obtained. Images that were taken without the head hood before and after IC measurements were analyzed as described above. However, for images taken during IC measurements (with the head hood for respiratory gas collection interposed between the infant's head and the infrared camera), amounts of heat loss from the infant's head and body were analyzed separately. To determine the mean surface temperature of the infant's head, a transmittance of 98% (determined experimentally) through the polyethylene film was used and temperatures were adjusted accordingly. Values for radiant, convective, and evaporative heat losses from the head were added to heat losses from the body to give total heat loss at each time point. To determine changes in MBST over time, the MBST for the infant's entire body was calculated for each time point. MBST was calculated by weighting head and body surface temperatures according to the fractional area represented by each (derived from the number of pixels in each part) and adding the values to obtain total MBST.

In a separate study, we determined the percentage of an infant's surface area that was in contact with the mattress, including areas of contact for the head and the body not including the head (15). These data were compared with the infant's surface area as estimated by using the 19 surface-area measurements of DuBois (16), and separate values for total, head, and body surface areas were calculated. The results of this study showed that the mean contact area for an infant's entire body was 19.5% of the total surface area (30.9% of the head surface and 17.0% of the remaining body area were touching the mattress). Estimated areas of radiant, convective, and evaporative heat loss were determined by subtracting the area in contact with the mattress from the total surface area.

Heat loss equations
The following equations were used in this study.

Radiant heat loss
For radiant heat loss (R) (17):


where


{epsilon} is emissivity for human skin (0.99)

AD is the DuBois surface area of total body, head, or body without head, in m2 (16)

fr is the radiating fraction of surface area. This value was calculated to be the value for a standing adult (18) minus the value for percentage of surface area contacting the mattress (15) as follows:

facl is the factor by which clothing changes the radiating fraction of the surface area, which = 1 for the nude state (19)

Ts is the mean skin surface temperature, determined by ITC, converted to Kelvin:

For the infant's head: Ts = mean temperature of the infant's head assuming 98% transmittance of infrared through the polyethylene film.

Trad is the mean temperature of the incubator wall, converted to Kelvin; this was determined by measuring the upper front wall and by using an experimentally derived regression equation as described above.

For the infant's head: Trad = 65% of incubator wall and 35% of hood wall temperatures as measured by thermistors. On the basis of surface area measurements, it was estimated that {approx}65% of the infant's head was radiating (through the polyethylene film) to the incubator wall and the remainder, 35%, was radiating to the polytetrafluoroethylene wall of the head hood.

Convective heat loss
Convective heat loss (C) equals the sum of convective heat losses from the skin (Cskin) and the respiratory tract (L).

Skin.
For convective heat loss from the skin (Cskin) (17):


where free convection was assumed because of the low recorded air flows in the incubator

hc is the natural convective heat exchange coefficient in W•m-2•°C-1, derived from Stolwick and Hardy's (20) values for humans standing indoors. It was calculated by weighting hc values based on surface areas of body surface regions for each infant. For the head, a uniform value of 3.0 was used, and for the body, the individual weighted hc for the entire body was used.

Afrac is the percentage of body surface area (which was measured in m2) available for convective heat exchange (ie, all areas not contacting the mattress). Afrac is 1 - the area contacting the mattress:

Ta is the air temperature inside the incubator or infant head hood.

Dry respiratory heat loss.
The equation for calculating dry respiratory heat loss (L) (18) is as follows:


where VE is pulmonary ventilation in kg air/h:


This is based on an estimated Ve in L/min for each infant. Ve was estimated by using a tidal volume of 7.5 mL/kg for infants weighing <1.5 kg and 9.5 mL/kg for infants weighing >=1.5 kg. Thus Ve equals the estimated tidal volume (mL/kg)•infant weight (kg)•breaths/min. An average number of breaths per minute was obtained from {approx}5 counts of respiratory rate taken during the experimental period for each infant.

cp is the heat capacity of the air (0.24 kcal•°C-1•kg-1)

Te (in °C) is the temperature of expired air, which is calculated for each infant (21) as follows:


where H2Oin is inspired water vapor in g/L.

Evaporative heat loss
Evaporative heat loss (E) equals the sum of losses from the skin (Edif) and respiratory tract (Eresp).

Insensible water loss from the skin.
Insensible water loss from the skin (Edif) (22, 23) was calculated as follows:


where fpcl is the Nishi moisture permeation factor for clothing in W•m-2•mm Hg-1, which = 1.00 for bare skin (22)

w is the wettedness factor, the fraction of the total body surface from which evaporative heat loss takes place, which was assumed to be 0.06 (a minimal value when there is no sweating) (24)

he is the mass transfer heat coefficient (23):


{phi} a is the relative humidity of ambient air, assumed to be equal in the head hood to the incubator humidity. Evaporative heat loss in infants was assumed to be occurring by insensible water loss only, with no regulatory losses as a result of sweating.

Respiratory water loss.
Respiratory water loss (Eresp) (18, 21) was calculated as follows:


where We - Wi equals the difference in humidity between expired and inspired air, which equals 0.029 - 0.00066 Pa (kg water/kg dry air), and hfg equals heat of vaporization of water at 35°C, which equals 575 kcal ({approx}2406 kJ)/kg water.

Conductive heat loss
Conductive heat loss (K) was estimated as 6.45% of radiant, convective, and evaporative heat loss, or 6.01% of total heat loss based on previous studies with infants (15). Therefore,



All values were obtained in kcal•kg-1•h-1 and were converted to kJ•kg-1•h-1 by multiplying by 4.184.

Anthropometric data
Weight, length, and the 19 surface area measurements of DuBois (16) were obtained from undressed infants with an electronic balance (model 4800; Scale-Tronix Inc, Wheaton, IL), a standard length board with centimeter measurements, and a flexible plastic measuring tape, respectively. Information on gestational age, birth weight, medical condition, and dietary intake was obtained from the infants' medical records. Measurements were made after completion of the IC and ITC measurements.

Data analysis
To enable comparisons between the 2 methods, IC values were averaged over 10-min intervals covering the 5 min before and 5 min after each ITC measurement point. Each infant had ITC scans done at the beginning and end of the entire study period (without head hood) and every 10 min during the IC data collection period (with head hood). In addition, 3 infants had to be removed from their incubators to be fed; for these infants, additional beginning and ending ITC scans were done for the second study period. As a consequence, infants had different numbers of paired IC and ITC measurements, ranging from 19 to 30, but they always had more ITC than IC measurements.

Three approaches were taken to compare the results of IC and ITC. First, within each infant's data, paired analyses of individual IC and ITC values were done with the Student's t test for paired samples (26). Second, for all 10 infants, paired analyses of mean ITC and IC energy expenditure values were done with the mean ITC and IC values for each infant based on 19 time points. We decided to use the same number of data points for each infant (the initial 19 time points) to minimize differences among the infants studied. Third, for all 10 infants, paired analyses were done of mean ITC and IC energy expenditure values, with the mean ITC and IC energy expenditure values based on all time points collected for each infant. Paired IC and ITC values were compared by using the Student's t test for paired samples.

Repeated-measures analysis of variance was used to determine whether feeding had any effect on energy expenditure as determined by either method and whether feeding had an effect on the differences between the 2 methods over time. Because the postfeeding time when each study began differed among the infants, study periods were divided into periods A and B for purposes of comparison. Infant 6, who was receiving continuous orogastric feedings, was excluded from the feeding analysis. For the other 9 infants, period A was 85–135 min after the infant was fed and first placed into the incubator. For the 6 infants who received noncontinuous orogastric feedings, period B was the second feeding period (10–120 min), done during the study. Period B was not analyzed for the 3 bottle-fed infants because they needed a longer equilibration time (30 min) before beginning the second study period as a result of being removed from the incubator for feeding. The effects of time postfeeding, method (ITC compared with IC), and the time-by-feeding interaction were analyzed. Significance was defined as P < 0.05 and all statistical analyses were completed with SAS (version 5.18; SAS Institute, Cary, NC) (26).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
For the 10 infants, mean (±SD) values were as follows: birth weight, 1.28 ± 0.47 kg; gestational age, 31 ± 3 wk; study weight, 1.74 ± 0.23 kg; and age at the time of the study, 34 ± 23 d (Table 1Go). Mean O2 was 9.03 ± 0.98 mL•kg-1•min-1 and CO2 was 9.69 ± 0.98 mL•kg-1•min-1 and mean respiratory quotient was 1.08 ± 0.04 (Table 2Go).


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  		TABLE 1. Clinical characteristics of subjects
 

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  		TABLE 2 . Results of indirect calorimetry1
 
Mean air temperature in the study incubator was 31.7 ± 1.9°C (range: 29.7–34.7°C) for all infants (Table 3Go). The first 2 infants experienced the highest mean incubator air temperatures (34.7 and 34.4°C); these infants were studied with the incubator in the skin temperature control mode. Incubator air temperature was also more variable for these infants, with a range of > 1.0°C. The rest of the infants were studied with the incubator in the air temperature control mode, and the variability in air temperature decreased, with a range of <0.6°C. Mean incubator wall temperature was 30.2 ± 0.9°C for all infants and varied less than air temperature. Relative humidity was similar for the infants, with a mean of 29.6%. Activity levels were similar among the infants, with most of the activity scores being <-2 (mean: -2.4 ± 0.5).


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  		TABLE 3 . Temperature and activity measurements
 
MBST did not differ between scans done with and without head hoods (Table 3Go). MBST was significantly correlated (r = 0.90, P < 0.05) with incubator air and wall temperatures but not with skin (back) temperature as measured by thermistor probe (r = 0.31). Six infants showed increases in surface temperature over time (MBST, final - initial) over time. The mean difference between beginning and ending temperatures for infants 3–10 was sufficiently small to justify neglecting heat storage in the calculation of energy expenditure, with the largest increases in infants 1 and 2 (Table 3Go). Four infants showed slight decreases in MBST over time.

Variability of energy expenditure was greater for values determined by IC than for those determined by ITC. Use of mean O2 and CO2 data over 10-min intervals to determine energy expenditure limited the minute-to-minute variability in the IC data, but significant variability in energy expenditure was still apparent. Respiratory data were quite dependent on respiratory rate and activity level. Even brief periods (<1 min) of crying caused large fluctuations in O2 and CO2. In addition, infants sometimes moved and disturbed the head hoods momentarily, causing changes in O2 and CO2. Usually these small variations are not significant because values are summed over long periods (typically hours), thereby minimizing the effect of such small perturbations.

No significant differences in energy expenditure were found among paired ITC and IC results (within-infant comparisons) for 3 of 10 infants, but significant differences were found for the other 7 infants (Table 4Go). The direction of the differences was not consistent. For the purpose of discussion, infants were divided into 3 groups: group 1 (infants 1, 2, and 10), where ITC < IC; group 2 (infants 5, 8, and 9), where ITC = IC; and group 3 (infants 3, 4, 6, and 7), where ITC > IC based on individual results of paired ITC and IC values (Table 4Go).


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  		TABLE 4. Summary of heat loss and heat production data used for within-infant comparisons1
 
The results for group 1 may be explained by a heat-gaining environment for infants 1 and 2, causing considerable heat storage that was not dissipated during the study period. Infant 10 was receiving theophylline, which may explain some of the increased O2. In group 2, although O2 and heat loss fluctuated over time, their means (± SDs) were not significantly different. This would be expected in the fasting state (as occurred at both ends of the study periods) or under conditions of constant energy infusion (infant 5). It is interesting to note that the methods agreed most closely in infant 5, who was receiving a continuous intravenous infusion of dextrose. For the remaining infants (group 3), IC was greater than ITC in the first half-hour postfeeding and then ITC was greater than IC during the remaining time. In this group, the difference between ITC and IC increased with time since feeding. The thermic effect of feeding may account for this, with the heat being stored initially and then being dissipated.

When ITC and IC means were compared for all 10 infants based on 19 paired measurements for each infant (among-infant comparison), no significant difference between the 2 methods was found (Table 5Go); the mean difference between the 2 methods was 0.15 ± 1.17 kJ•kg-1•h-1. Mean IC and ITC values based on these 19 time points (Table 5Go) were not significantly different from means based on all time points (Table 4Go). The mean difference between IC and ITC based on all time points was –0.24 ± 1.22 kJ•kg-1•h-1 (NS; Table 4Go). The mean energy expenditure (IC) was 11.62 ± 1.24 kJ•kg-1•h-1 (Table 5Go). In Figure 2Go, the mean (±SD) heat loss and heat production for the 10 infants over the entire time period are shown. The mean difference between the 2 methods for each infant is also presented. These numbers were derived from the summary data presented in Table 5Go. The minimum difference between the 2 methods was 0.004 kJ•kg-1•h-1, which is only 0.10 kJ•kg-1•d-1 (0.04% of the IC value). The maximum difference between the 2 methods was -2.14 kJ•kg-1•h-1, or 51.31 kJ•kg-1•d-1 (18% of the IC value). The 95% CI for the differ-ence between the 2 methods was -0.26 to -0.04 kJ•kg-1•h-1, or -10.51% to 4.79%.


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  		TABLE 5. Mean heat loss measured by infrared thermographic calorimetry (ITC) and heat production measured by indirect calorimetry (IC): data used for among-infant comparisons
 


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  		FIGURE 2. Mean (±SD) heat loss, as measured by infrared thermographic calorimetry (ITC; {diamondsuit}), and heat production, as measured by indirect calorimetry (IC; {square}), for all subjects (n = 10). The mean difference ({blacksquare}) between ITC and IC was -0.15 kJ•kg-1•h-1. Paired differences were not significant.

 
Results of the repeated-measures analysis of variance showed no significant difference between IC and ITC for period A, the initial postfeeding period (85–135 min), but a significant interaction between time and method occurred (P < 0.001). This may have been the result of slight decreases in IC values over this time period. For period B, the second postfeeding period (10–120 min), differences between the 2 methods were significant (P < 0.001). During this period, there was a small increase in IC results over the first 30 min postfeeding.


   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Few studies have simultaneously compared heat loss and heat production in infants. In this study, we described and validated ITC, a new method of determining infant heat loss and energy expenditure. ITC is an accurate method for the measurement of MBST and interferes less with the infant's environment than does IC. In conjunction with heat loss equations adapted for this purpose, ITC enables the determination of radiant, convective, evaporative, and conductive heat losses from infants. Ten preterm infants were studied with concurrent ITC and IC during study periods lasting a mean of 281 min. No significant difference was found between the 2 methods overall, with a mean difference (ITC - IC) of -0.15 kJ•kg-1•h-1, or 1.3%.

Similar results were obtained by other investigators who compared heat loss and heat production. Howland (1) performed simultaneous direct and indirect calorimetry in 2 infants and found a difference of <3% in 13 comparisons. In a study of 25 preterm infants, Day (3) used concurrent direct and indirect calorimetry and found no significant difference between the mean values for energy expenditure. Bell (27) used concurrent direct and indirect calorimetry to determine energy expenditure in 20 growing preterm infants during 2 consecutive postprandial periods; the mean difference between the 2 methods (2.4%) was not significant.

In our study, no significant difference was found between the 2 methods of determining energy expenditure overall, although the degree of concordance varied among infants. In 7 of 10 infants, within-infant paired t tests showed a significant difference between the 2 methods. Significant differences were not found for the remaining 3 infants. The range of differences found was 0.04–18.51%, and the larger difference was greater than the error of either method. However, because there was no consistent relation of ITC to IC, further adjustments of coefficients in the heat loss equations would not alter the individual differences. Most of the infants had differences of <10% between the 2 methods, which would result in minimal differences in energy expenditure per day if estimated by ITC alone compared with IC.

Studies by Benedict (28) showed that on only 8 occasions in 288 periods of 2 h each were direct and indirect calorimetry in agreement; the differences were in the range of ±10% of total energy expenditure. However, direct and indirect calorimetry were in nearly perfect agreement when summed over 24 h. Webb (29) also noted that heat production and heat loss rarely were the same over short periods of time. In infants, similar differences were found between direct and indirect calorimetry. In the group of 25 infants studied by Day (3), 17 of 50 cases had measurements that differed by >10%. In a study of concurrent direct and indirect calorimetry in 14 growing preterm infants, Sauer et al (30) found that energy expenditure determined by direct calorimetry was lower by an average of 7.4%.

Physiologic factors are most likely the primary cause of differences between the 2 methods at individual time points. Heat production and heat loss are in constant flux and are affected by changes in environment, feeding, handling, activity, and medical condition. These influences on energy expenditure affect heat production and heat loss differently and there may be a time lag before the effects appear. Heat loss will exceed heat production if body core temperature rises and heat is stored, which in turn stimulates heat loss and suppresses metabolism. In this case, ITC would exceed IC. The opposite occurs if body temperature decreases; heat conservation is stimulated and metabolic rate increases. In that case, IC exceeds ITC. This negative feedback mechanism for maintaining normal body temperature is probably responsible for differences in heat production and heat loss over short periods of time (8).

Infants 1 and 2 showed the greatest differences between the 2 methods, with IC values being greater than ITC values. Mean skin temperature increased in these infants throughout the study period. Calculation of heat storage based on change in MBST showed values of 0.95 and 0.62 kJ•kg-1•h-1 for infants 1 and 2, respectively. Addition of these heat storage values to ITC values would significantly decrease the differences between the 2 methods for these infants. Calculation of heat storage by using this method for the remaining infants yielded values of <0.17 kJ•kg-1•h-1 and did not explain differences between the 2 methods.

Infants 3–7 (group 3), for whom ITC-derived values were greater than those of IC, had an expected increase in • VO2 in the half hour after feeding. As seen in studies of adults, for the remainder of the study periods, heat loss exceeded heat produced and the difference between ITC and IC increased. Infants in group 3 may have been showing an earlier or enhanced diet-induced thermogenesis compared with those in group 2. This may have been a result of differences in body composition, maturation, or ability to conserve heat. No trends in birth weight, age (in days), mode of feeding, activity level, or diagnosis were noted to influence differences between the 2 methods. Given that determinations of energy expenditure by IC are most accurate when summed over periods of hours (31) because of the variability of energy expenditure determined over shorter periods, it seems that the differences seen in this study were small and within the range of experimental and biological variation.

The O2 and CO2 data in this study were similar to results found in previous research with similar preterm infants (7). In our group of growing preterm infants, all respiratory quotients determined by IC were >1.0, which indicated a state of net lipogenesis (31). The variability of energy expenditure as determined by IC was greater than that determined by ITC, and was partly a result of the short (10-min) intervals of time used in the analyses. Bell et al (32) studied 24-h energy expenditure measured by IC on 9 occasions in 5 preterm infants. Their study showed that the CV in energy expenditure was relatively high, with a mean of 11% for 2-h periods. The error in estimating 24-h energy expenditure from 2-h periods was 2.8%, compared with 0.9% when estimated from a 6-h period.

ITC is an accurate method for the determination of energy expenditure in groups of healthy preterm infants over periods of several hours. Paired differences between ITC and IC over time were similar to previous observations (3, 8, 28, 29) and appeared to mainly reflect true differences between metabolic heat production and total heat loss. ITC may be less reliable for ascertaining the energy expenditure of individual infants; however, it should correctly assess changes in energy expenditure resulting from interventions, such as changes in the thermal environment, even in individual cases. Recent use of ITC in infants under radiant warmers was valuable for monitoring infant responses to changes in the thermal environment (33). In addition, because of the decreased intra-infant variability in ITC measurements compared with IC, estimation of energy expenditure by ITC may require a shorter period of measurement than IC. Further study will be necessary to determine the minimum number of ITC measurements needed to accurately quantify 24-h energy expenditure in infants. ITC is a portable and noninvasive method that holds promise for measuring the energy expenditure of infants in research and clinical settings. It makes possible the measurement of heat loss by each route—radiant, convective, evaporative, and conductive. Use of heat loss equations also allows prediction of changes in energy expenditure resulting from changes in environmental conditions.


   ACKNOWLEDGMENTS
 
We thank Karen J Johnson, who provided valuable assistance by helping to monitor the subjects during the studies.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Received for publication March 4, 1999. Accepted for publication August 18, 1999.





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