| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
1 Nutritional Biochemistry and 3 Stable Isotope Laboratories, Space and Life Sciences Directorate, National Aeronautics and Space Administration/Johnson Space Center, Houston, Texas 77058; 2 The Committee on Human Nutrition and Nutritional Biology, University of Chicago, Department of Medicine, Chicago, Illinois 60637; and 4 Health Sciences, University of Wisconsin, Milwaukee, Wisconsin 53201
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
ACKNOWLEDGEMENTS
FOOTNOTES
REFERENCES
ABSTRACT 
Gretebeck, Randall J., Dale A. Schoeller, Rick A. Socki,
Janis Davis-Street, Everett K. Gibson, Leslie O. Schulz, and Helen W. Lane. Adaptation of the doubly labeled water method
for subjects consuming isotopically enriched water. J. Appl. Physiol. 82(2): 563-570, 1997.
The use of
doubly labeled water (DLW) to measure energy expenditure is subject to
error if the background abundance of the oxygen and hydrogen isotope
tracers changes during the test period. This study evaluated the
accuracy and precision of different methods by which such background
isotope changes can be corrected, including a modified method that
allows prediction of the baseline that would be achieved if subjects
were to consume water from a given source indefinitely. Subjects in
this study were eight women (4 test subjects and 4 control subjects)
who consumed for 28 days water enriched to resemble drinking water aboard the United States space shuttle. Test subjects and control subjects were given a DLW dose on days
1 and 15,
respectively. The change to an enriched water source produced a bias in
expenditure calculations that exceeded 2.9 MJ/day (35%), relative to
calculations from intake-balance. The proposed correction based on the
predicted final abundance of 18O
and deuterium after equilibration to the new water source eliminated this bias, as did the traditional use of a control group. This new
modified correction method is advantageous under field conditions when
subject numbers are limited.
deuterium; oxygen-18; mass spectrometry; energy expenditure
INTRODUCTION THE DOUBLY LABELED WATER (DLW) method is ideally suited
for measuring total energy expenditure (TEE) under field conditions, i.e., when subjects cannot be confined to a laboratory. This method is
based on the isotopic equilibration of water labeled with deuterium (2H) and
18O with body water and
bicarbonate. After a loading dose of DLW is given, the
2H is eliminated from the body as
water, whereas the 18O is
eliminated from the body as water and
CO2. The difference between the
elimination rates of 2H and
18O, therefore, is proportional to
CO2 production
( The use of DLW to measure energy expenditure in human subjects is
complicated when those subjects consume water of different isotopic
proportions shortly before or during the period of measurement. This
change can result in changes in baseline isotope abundance and, therefore, can interfere with the accuracy of energy-expenditure measurements (4, 7). For example, energy expenditure by United States
space shuttle astronauts is measured with DLW before and during
flights, but these subjects consume water from at least three sources
(Johnson Space Center in Houston, TX; Kennedy Space Center at Cape
Canaveral, FL; and the space shuttle itself) shortly before or during
energy-expenditure measurements. Of these, the potable water on the
space shuttles is a particular isotopic problem, as it is produced by
fuel cells during production of electrical power. Shuttle fuel cells
convert gaseous hydrogen and oxygen to water, which is enriched in
2H and
18O in accordance with the
isotopic enrichment of the gases. This enrichment, although not harmful
to the crew, might affect both the accuracy and the precision of the
DLW technique for measuring energy expenditure.
The simplest solution to the problem posed above would be to increase
the dose of the isotope markers to the point at which errors in the
natural background become negligible. Dose size influences accuracy and
precision in two ways. First, a larger dose produces a larger signal
relative to the random error in the isotopic measurement, improving the
precision of the measurement. Second, a larger dose increases the
signal relative to variations in the natural abundance of
2H and
18O in body water. These
variations in natural abundance arise both from isotopic fractionation
and from the isotopic constituents of the food, water, and air that
enter the body (2, 3, 21, 22). However, this solution is impractical
for two reasons, the first being the expense of
18O and the second the
complications associated with measuring high enrichments from such
large doses accurately with current gas-inlet isotope-ratio mass
spectrometers.
Another more practical alternative is to use control subjects who are
not given DLW (4, 6, 7) so that the background isotopic abundance of
the two groups can be compared over time. This method has been used
under conditions of moderate change in the isotopic abundance of
drinking water but has never been rigorously validated (under
controlled conditions) (4). Inclusion of control subjects in two
studies (4, 7) maintained the accuracy of the DLW method, but the
precision of the TEE measurements was 7% (4, 7). This approach is not
ideal for space research, because the numbers of astronaut subjects
available for study are limited. Moreover, the isotopic abundance in
the water consumed during space shuttle flights tends to be greater
than that reported in the studies described above (4, 7) and thus may
degrade precision still further.
A third alternative has been to allow a period of equilibration
(usually 1-3 wk) during which subjects consume water from the new
source before the DLW dose is given (16). This approach, which also has
been validated (16), preserves the accuracy and precision of TEE
measurements, but the time required for equilibration may be a limiting
factor, especially if the rate of water turnover is low or the
difference between the initial and subsequent sources of drinking water
is large. An equilibration period is particularly impractical for space
crew members, because current space shuttle missions typically last
only 7-13 days.
A fourth approach has been to predict the change in baseline as a
function of time and the difference in isotopic abundances of the two
water sources in question (8). These changes are added to (or
subtracted from) the apparent enrichments of each postdose sample in a
time point-by-time point basis to obtain the enrichment relative to the
shifting baseline value. We recently realized that in the presence of a
step change in the abundance of any of the inputs to the body it is
possible to simplify this correction by only estimating the abundance
of the baseline after the subject equilibrates to the new source of
oxygen and hydrogen.
The purpose of this study was to investigate a new means of adjusting
for shifts in isotope abundance, which is a modification of the method
by Jones et al. (8) in that it does not require a time function. This
method involves predicting the new baseline isotopic abundance, as
though subjects had undergone a full period of equilibration to a new
water source. We present the theoretical basis for this correction as
well as validations and comparisons with other methods.
METHODS Table 1.
Subject characteristics
CO2) and, hence, energy
expenditure (18). This method is accurate to 1-2%, with precision
ranging from 3 to 8% depending on the isotope dose, duration of study,
rate of energy expenditure, and related conditions (10, 15).
Subject
Age, yr
Height, cm
Weight, kg
%Fat
REE, MJ/day
Test group
1
45
160
56.6
26.1
4.56
2
35
166
62.4
26.0
5.24
3
45
165
62.4
27.0
5.76
4
31
160
49.0
26.9
4.45
Control group
5
47
171
58.6
17.7
6.27
6
35
155
45.7
28.2
5.20
7
33
168
55.4
21.8
6.24
8
35
155
62.3
26.7
5.80
Mean ± SD
38.3 ± 6.3
163 ± 5.9
56.6 ± 6.3
25.1 ± 3.5
5.44 ± 0.7
REE, postabsorptive resting energy expenditure.
) received a doubly labeled water (DLW) dose on
day 1 and control subjects (
) on
day 15. Thus total energy expenditure
(TEE) was determined during days
1-14 for test subjects and during
days 15-28 for control subjects.
Body composition was determined by dual energy X-ray absorptiometry
(DEXA) at the beginning, middle, and end of study.
Resting energy expenditure. Resting energy expenditure was measured on days 1, 15, and 28. Subjects arrived at the laboratory in the morning, after having fasted for at least the previous 8 h and rested supine in a darkened room for 20 min before the measurements were begun. Measurements were taken over 45-min periods by using a critical care monitor with a canopy system (Medical Graphics, St. Paul, MN) for breath-by-breath analysis of
CO2 and oxygen uptake
(O2). Subjects were
instructed to rest quietly but remain awake during the measurements.
Diet. Enriched water was made fresh
every 3-4 days to minimize bacterial growth during storage by
adding 8.75 ml of
H218O
10 atom percent excess (APE) and 0.25 ml
2H2O
(99.8 APE) to 10 liters of Houston tap water. The isotopic abundance of
randomly selected enriched water samples averaged 34.6 ± 2.7
for 18O and 123 ± 10 for 2H. These
concentrations were designed to represent the average isotope abundance
in water samples retrieved after two space shuttle missions and were 34 ± 2.8 for 18O and 125 ± 70.7 for 2H. The
day-to-day SD within each mission averaged 0.7 for
18O and 2.8 for
2H. The enriched water was carried
by the subjects throughout the day and used to prepare drinks and
rehydrate foods as well as for direct consumption.
All foods and fluids consumed throughout the study were weighed on
calibrated electronic scales by the subjects and recorded in a
standardized diary. All diets were self-selected from food items
provided aboard the space shuttle vehicles. The majority of these food
items were dehydrated, packaged individually, and reconstituted with
enriched water. The use of a controlled inventory of supplied foods
greatly enhanced the accuracy of food records that were reviewed weekly
with a dietitian. All shuttle foods were analyzed for energy, fat,
protein, and moisture content, with carbohydrate content calculated by
difference.
Body composition. Body composition was
determined at the beginning, middle, and end of the study by
dual-energy X-ray absorptiometry (Hologic model QDR 1000/W, Hologic,
Waltham, MA). Whole body scans were obtained in the pencil-beam mode
while the subjects rested supine, and scans were analyzed by using
Hologic's whole body-analysis software (version 5.35).
Body-composition results were reported as lean mass, bone mass, fat
mass, and total mass. Percent body fat was calculated by dividing total
fat mass by total body mass. The precision of the whole body scan
within our laboratory was 0.87% for lean body mass and 1.71% for fat
mass, respectively (20).
DLW doses. Isotopes were purchased
from Icon Services (Summit, NJ), and the doses were calculated as
follows: 6.2 atom-percent H218O
mixed with 99.8 atom-percent
2H2O
to reach a 100-APE dose of 0.5 g of
H218O
and 0.24 g of
2H2O
per kilogram of lean body mass (estimated from body weight). DLW was
administered in the morning after an overnight fast. Subjects continued
their fast for an additional 5 h.
Sample analyses. Urine and saliva
samples were centrifuged in the presence of activated charcoal,
filtered, and stored frozen in cryogenically stable tubes at
20°C until analysis by gas-inlet isotope-ratio mass
spectrometry. Samples were analyzed for
2H2O
by zinc reduction at the University of Chicago, Department of Medicine
(14), and for
H218O
by CO2 equilibration at the
Johnson Space Center, Stable Isotope Laboratory (19). Aliquots (2 µl) were introduced into an evacuated side arm and
allowed to distill over to a 6-mm OD quartz tube containing 40 mg of
zinc reagent (Biogeochemistry, Bloomington, IN) and were then cooled to
liquid nitrogen temperatures. The tubes were sealed and heated to
500°C for 30 min. 2H analyses
were performed in triplicate; SD values ranged from 1.5 for
enrichments of <200 to 4.5 for enrichments
approaching 2,000 when measured with a triple-inlet Nuclide
3-60 HD isotope ratio mass spectrometer (PATCO, Belefonte, PA).
The CO2 equilibration technique
involved dispensing 1.5 ml of sample into a 7-ml evacuated tube with
150 mmol of 99.9% pure CO2.
Samples were then shaken in a water bath at 25°C for at least 12 h,
and the CO2 was cryogenically
removed and stored in 6-mm break-seal tubes. Samples were analyzed on a
Finnigan MAT 251 stable-isotope mass spectrometer at Johnson Space
Center. The reproducibility of this technique in this laboratory is
±0.05 or better at the 1 SD confidence level (19).
Dilution spaces for
H218O
and
2H2O
were calculated from the baseline and the 5-h-after dose samples by
using the equation
![N (mol) = (WA /18.02a)/[(&dgr;<SUB>a</SUB> − &dgr;<SUB>t</SUB>)/(&dgr;<SUB>s</SUB> − &dgr;<SUB>p</SUB>)]](/content/vol82/issue2/fulltext/563/img001.gif)
|
(1) |
is the enrichment of the dose
(a), of the tap water
(t), of the 5-h-after dose
sample (s), or of the
baseline sample (p).
CO2 rate
(rCO2) was
calculated as described by Schoeller et al. (18) and Racette et al.
(12) by using the
equation
|
|
(2) |
1.041 kH). (The isotope-elimination
rates for these 8 subjects averaged 0.114 ± 0.020 mol/day for
18O and 0.092 ± 0.018 mol/day
for 2H.)
O2 was derived for each
subject by dividing the CO2
rate by the food quotient, which was derived from analysis of diet composition (1). TEE was calculated as described by de Weir (5).
Calculation of isotopic enrichment of body
fluids. The appearance of
2H and
18O in body water after a step
change in the enrichment of drinking water follows a single-exponential
time course
|
(3) |
If a subject is given a dose of labeled water after having equilibrated to the new water source, then the elimination of the label is also described by a single-exponential function
![E = C<SUB><IT>t</IT></SUB> − C<SUB>bl</SUB> = [C<SUB>0</SUB> − C<SUB>bl</SUB>]<IT>e</IT><SUP>−k<IT>t</IT></SUP>](/content/vol82/issue2/fulltext/563/img005.gif)
|
(4) |
|
|
(5) |
![k = &Dgr;[ln (C<SUB><IT>t</IT></SUB> − C<SUB>f</SUB>)]/&Dgr;<IT>t</IT>](/content/vol82/issue2/fulltext/563/img008.gif)
|
(6) |
|
(7) |
|
|
(8) |
O2 in the lung. The
variables used in these calculations are listed in Table 2.
|
||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
|
(9) |
Cf and K(2) = Cf Cbl. The CONSAAM program for PC
(version 29; National Institutes of Health/National Cancer Institute,
Bethesda, MD) was used to fit the model. The third method was to fit
another exponential model to the isotopic abundance changes in control
subjects who changed water sources but were not given the DLW dose
until 15 days later. The control subjects did not receive DLW until
day 15, so the isotope appearance in these subjects could be used to correct for background changes in the
test subjects who received DLW on day
1. That model was
![C<SUB><IT>t</IT></SUB> = K(3)[1 − <IT>e</IT><SUP>−kt</SUP>] + K(4)](/content/vol82/issue2/fulltext/563/img013.gif)
|
(10) |
Cbl and K(4) = Cbl.
Statistical analyses. Results are
presented as means ± SD. Energy expenditure calculations from the
three enrichment adjustment methods were compared with calculations
from the energy intake balance method by using paired
t-tests. Variances were compared by
using F-tests.
RESULTS
Samples of tap water collected at the Johnson Space Center were found
to contain 4.4 18O
and 25.2 2H,
relative to standard mean ocean water
(SMOW). Urine samples collected
before subjects began consuming the enriched water contained 0.49 ± 1.6 18O and 12.65 ± 6.3 2H (means and
SD values for 8 subjects).
The change in isotopic enrichment of body fluids for those subjects who
consumed the enriched water for 2 wk before receiving the DLW dose
(isotope appearance) is shown in Fig. 3.
The equilibrated baseline abundance predicted from mass balance
(Eqs. 7 and 8) for these subjects was
20.0 for 18O and
110.9 for 2H.
Table 3 presents isotopic abundance values from urine samples collected before and after consumption of enriched water. Baseline isotopic abundance after equilibration to the enriched water was estimated from isotope-appearance (Eq. 10) and -disappearance (Eq. 9) kinetics. The value estimated from the appearance kinetics (Eq. 10, extrapolated to infinite time) (Table 3) was similar to that predicted from mass balance. The average values predicted from the disappearance kinetics (Eq. 9, extrapolated to infinite time) were not different; however, the individual values were unexpectedly variable (Table 3).
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Energy expenditure. The criterion
method for assessing energy expenditure was energy intake-balance,
where intake was obtained from the controlled inventory of the same
prepackaged foods used on the space shuttle. Mean energy consumed
during the 2-wk energy-expenditure periods was 7.65 ± 1.26 MJ/day.
Subjects tended to be in negative energy balance during the 2 wk
(0.47 ± 1.06 MJ/day), as indicated by small energy losses
from body stores (Table 4).
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Energy expenditure was calculated from DLW results for the four test
subjects (those who had no equilibration period) from their individual
(predose) isotopic baselines, from the mass balance-predicted baseline
for the group, from the individual baselines estimated from the isotope
disappearance kinetics, and from the change in baseline for the control
subjects (Table 5). As expected, the use of
the individual (predose) measured baselines produced substantial error
in the estimate of energy expenditure (Table 5). In contrast, energy-expenditure values from the isotope mass balance predicted baseline underestimated energy expenditure (relative to intake-balance calculations) by only 0.87 ± 1.67 MJ/day (not significant).
The use of the correction based on the observed changes in baseline in
the control group also generated accurate estimates. The use of the
baseline predicted from disappearance kinetics was accurate for the
test group but was imprecise (P < 0.05 vs. the isotope balance predicted baseline,
F-test), as might be expected from the
variability in the estimated isotopic abundances at infinite time.
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Energy expenditure also was calculated for the control subjects from their (predose) urine samples, from individual baselines estimated from the isotope-appearance kinetics, from the isotope-disappearance kinetics, and from isotope balance predicted baselines (Table 6). Control subjects had 2 wk to partially equilibrate to the enriched water (which corresponds to ~2 biological half-lives). The energy-expenditure values from DLW were accurate with the use of any of the methods. However, the precision of the elimination predicted baseline was reduced relative to that of the test subjects from the isotope balance predicted baseline (P < 0.01). The precision predicted from appearance kinetics tended to be worse than that of the isotope balance predicted baseline; however, the difference did not reach statistical significance (P > 0.05, F-test).
|
|||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
DISCUSSION
This is the first controlled investigation of how a change in isotope abundance affects the accuracy and precision of the DLW method. Previous investigations have involved either observations of background changes in largely uncontrolled situations in natural settings (4, 7), clinical situations in which the control was dictated by medical practice (8, 9, 16), or situations in which only computer simulations were possible (13, 21). Moreover, the background changes imposed in this investigation were larger than those encountered under most conditions. This combination of control plus a large change in background provided an excellent opportunity to demonstrate that background changes can negatively affect this method. More importantly, we were able to demonstrate that the deleterious effects could be mitigated by using approaches applied by previous investigators or a new approach that is based on estimates of final equilibrated isotope abundance.
The potential for error under changing background conditions was illustrated clearly by the average error of 2.9 MJ for the four test subjects, when the isotope-disappearance rates were calculated without considering the change in background. Intersubject variability was not inflated and did not provide any indication of problems, because the subjects all showed the same changes in background that could be expected from introducing a new water source.
This 2.9-MJ bias is much larger than that reported by DeLany et al. (4) or Jones et al. (7), who used the DLW method to measure energy expended by soldiers who had been transported to a new location to engage in field exercises. However, subjects in these studies consumed water from natural sources, with isotopic compositions close to the meteoric water line (3). Thus the ratio of change in baseline isotopic abundance was roughly 6:1 2H/oxygen, which resembles the enrichment of these isotopes in body water after standard doses. Therefore, the errors produced in the rates of disappearance of 2H and oxygen isotopes were covariant and largely canceled each other out in the calculations of energy expenditure, because this calculation depends on the difference between the two elimination rates.
The present study confirms the utility of using an equilibration period when the isotopic enrichment of the water source for subjects is altered. The 2-wk period used in this study was adequate for the calculation despite its being insufficient for full equilibration to the new water source. Indeed, the predose isotopic abundance in the control subjects had reached only ~75% of the estimated final equilibration. Nonetheless, no bias was detected nor relative precision lost. These results indicated that partial equilibration was sufficient to obviate the problems of the unusual isotopic composition of the enriched water. The isotopic composition of the experimental water source in the present study was chosen to mimic the water that astronauts consume aboard the space shuttles. The bias observed in this study, however, documents the estimates of bias made by Schoeller et al. (16) and Pullicino et al. (11), whose subjects were fed intravenously with water that had an unusual isotopic composition arising from the distillation process (11).
The present study also confirms the validity of using control groups to track changes in isotope backgrounds when full or partial equilibration periods are not feasible. In addition, we have demonstrated that baseline changes can be corrected equally well without a control group but, instead, by calculating the final equilibrated-baseline isotope abundance from isotope mass balance. The coefficient of variation for this correction was 13%, which is similar to that reported by Jones et al. (8) but worse than the 7-8% reported by DeLany et al. (4) using a control group. A 13% coefficient of variation also characterized the control group in the present study, suggesting that poor precision was due to the isotopic composition of the enriched water rather than to the method itself.
The use of isotope-disappearance kinetics to predict final baselines
failed, probably because of the need to extrapolate too far from the
final data point, as indicated by model-derived uncertainties in the
estimated final isotopic abundances of 21 for oxygen and 145 for 2H. This
variability might have been reduced if urine samples had been collected
during two additional biological half-lives during the evaluation
period.
The advantage of the correction method described in this paper that is
based on the final isotope ratio of the fully equilibrated baseline
isotope abundance is that it does not require that a subset of subjects
be relegated to a control group, an important consideration when the
number of subjects is limited. The disadvantage of this method is that
it requires the isotopic composition of the various inputs to be
relatively constant and that the information be available to calculate
isotope balance. Furthermore, because the isotope-balance correction
method is sensitive to errors in the estimates of the input functions
(17), it does not provide quite as much confidence as would tracking a
change in baseline in a control group. Fortunately, most of the 19 factors needed to calculate mass balance (Table 2) are known and should
remain relatively constant. Only the isotopic abundance of the new
water source and the fractions of elemental influx and efflux are
highly variable. The constituents of the new water can be measured
readily, and the fractions of elemental influx and efflux can be
estimated (14). The prediction will never be perfect, however, because these parameters are subject to physiological variations. In general, these variations will cause the baseline abundance of both isotopes to
vary, typically with a 6:1 change in the per mill abundance of
2H and oxygen (3, 17). Thus it is
important to use isotope loading doses that produce 6:1
enrichments of these isotopes in body water and to limit the metabolic
period to less than two biological half-lives (2, 13, 18).
In summary, we have validated a new correction procedure for the DLW method for situations in which the background abundance of isotopes cannot be kept constant. In addition, we have validated the commonly used control subject correction method, which has been assumed to be valid. The new method has been validated under conditions that simulate space shuttle flight and thus will permit the DLW method to be used to assess human energy expenditure under the unique conditions of space flight.
ACKNOWLEDGEMENTS
The authors appreciate the efforts of Christine Wogan of KRUG Life Sciences in clarifying this presentation.
FOOTNOTES
Address for reprint requests: R. J. Gretebeck, c/o H. Lane, Nutritional Biochemistry Laboratory, Medical Sciences Division, Mail Code SD3, NASA-Johnson Space Center, Houston, TX 77058.
Received 20 May 1996; accepted in final form 26 August 1996.
REFERENCES
| 1. | Black, A. E., A. M. Prentice, and W. A. Coward. Use of food quotients to predict respiratory quotients for the doubly labeled water method of measuring energy expenditure. Hum. Nutr. Clin. Nutr. 40: 381-391, 1986. [Medline] |
| 2. | Coward, A., and T. Cole. Determination of optimal dosing ratios (Appendix 5). In: The Doubly Labeled Water Method For Measuring Energy Expenditure: Technical Recommendations for Use in Humans, edited by A. Prentice. Vienna, Austria: Intl. Dietary Energy Consultants Group, Intl. Atomic Energy Agency, 1990, p. 294-301. |
| 3. | Dansgaard, W. Stable isotopes in precipitation. Tellus 16: 436-468, 1964. |
| 4. |
DeLany, J. P.,
D. A. Schoeller,
R. W. Hoyt,
E. W. Askew,
and
M. A. Sharp.
Field use of D218O to measure energy expenditure of soldiers at different energy intakes.
J. Appl. Physiol.
67:
1922-1929,
1989.
|
| 5. | De Weir, J. B. New methods for calculating metabolic rate with special reference to protein metabolism. J. Physiol. Lond. 109: 1-9, 1949. |
| 6. |
Hoyt, R. W.,
T. E. Jones,
T. P. Stein,
G. W. McAninch,
H. R. Lieberman,
E. W. Askew,
and
A. Cymerman.
Doubly labeled water measurement of human energy expenditure during strenuous exercise.
J. Appl. Physiol.
71:
16-22,
1991.
|
| 7. |
Jones, P. J. H.,
I. Jacobs,
A. Morris,
and
M. B. Ducharme.
Adequacy of food rations in soldiers during an arctic exercise measured by doubly labeled water.
J. Appl. Physiol.
75:
1790-1797,
1993.
|
| 8. |
Jones, P. J. H.,
A. L. Winthrop,
D. A. Schoeller,
R. M. Filler,
and
T. Heim.
Evaluation of doubly labeled water for measurement of energy expenditure during changing nutrition.
Am. J. Clin. Nutr.
47:
799-804,
1988.
|
| 9. |
Mitchell, I. M.,
P. S. W. Davies,
J. M. E. Day,
J. C. S. Pollock,
M. P. G. Jamieson,
and
D. J. Wheatley.
Energy expenditure in children with congenital heart disease, before and after cardiac surgery.
J. Thorac. Cardiovasc. Surg.
107:
374-380,
1994.
|
| 10. | Prentice, A. M., E. O. Diaz, P. R. Murgatroyd, G. R. Goldberg, B. J. Sonko, A. E. Black, and W. A. Coward. Doubly labeled water measurements and calorimetry in practice. In: New Techniques in Nutritional Research, edited by R. G. Whitehead. New York: Academic, 1990. chapt. 8, p. 177-206. |
| 11. | Pullicino, E., A. Coward, and M. Elia. Total energy expenditure in intravenously fed patients measured by the doubly labeled water method. Metab. Clin. Exp. 42: 58-64, 1993. |
| 12. |
Racette, S. B.,
D. A. Schoeller,
A. H. Luke,
K. Shay,
J. Hnilicka,
and
R. F. Kushner.
Relative dilution spaces of 2H- and 18O-labeled water in humans.
Am. J. Physiol.
267:
E585-E590,
1994.
|
| 13. |
Roberts, S.,
W. A. Coward,
G. Ewing,
J. Savage,
T. J. Cole,
and
A. Lucas.
Effect of weaning on accuracy of doubly labeled water method in infants.
Am. J. Physiol.
254 (Regulatory Integrative Comp. Physiol. 23):
R622-R627,
1988.
|
| 14. | Schoeller, D. A. Changes in isotopic background In: The Doubly Labeled Water Method for Measuring Energy Expenditure: Technical Recommendations for Use in Humans, edited by A. Prentice. Vienna, Austria: Intl. Dietary Energy Consultants Group, Intl. Atomic Energy Agency, 1990. chapt. 8, p. 147-165. |
| 15. | Schoeller, D. A., and W. A. Coward. Practical consequences of deviations from the isotope elimination model. In: The Doubly Labeled Water Method For Measuring Energy Expenditure: Technical Recommendations for Use in Humans, edited by A. Prentice. Vienna, Austria: Intl. Dietary Energy Consultants Group, Intl. Atomic Energy Agency, 1990. chapt. 9, p. 166-192, 1990. |
| 16. |
Schoeller, D. A.,
R. F. Kushner,
and
P. H. Jones.
Validation of doubly labeled water for measuring energy expenditure during parenteral nutrition.
Am. J. Clin. Nutr.
44:
291-298,
1986.
|
| 17. | Schoeller, D. A., C. A. Leitch, and C. Brown. Doubly labeled water method: in vivo oxygen and hydrogen isotope fractionation. Am. J. Physiol. 251 (Regulatory Integrative Comp. Physiol. 20): R1137-R1143, 1986. |
| 18. |
Schoeller, D. A.,
E. Ravussin,
Y. Schutz,
K. J. Acheson,
P. Baertschi,
and
E. Jequier.
Energy expenditure by doubly labeled water: validation in humans and proposed calculation.
Am. J. Physiol.
250 (Regulatory Integrative Comp. Physiol. 19):
R823-R830,
1986.
|
| 19. | Socki, R. A., H. R. Karlsson, and E. K. Gibson. Extraction technique for the determination of oxygen-18 in water using preevacuated glass vials. Anal. Chem. 64: 829-831, 1992. [Medline] |
| 20. | Spector, E., A. LeBlanc, and L. Shackelford. Hologic QDR 2000 whole body scans: a comparison of three combinations of scan modes and analysis software. Osteoporosis Int. 5: 440-445, 1995. [Medline] |
| 21. |
Tatner, P.
Deuterium and oxygen-18 abundance in birds: implications for DLW energetics studies.
Am. J. Physiol.
258 (Regulatory Integrative Comp. Physiol. 27):
R804-R812,
1990.
|
| 22. | Zanconato, S., D. M. Cooper, Y. Armon, and S. Epstein. Effect of increased metabolic rate on oxygen isotope fractionation. Respir. Physiol. 89: 319-327, 1992. [Medline] |
This article has been cited by other articles:
|
|
 |
|
  K. Baek, A. A. Barlow, M. R. Allen, and S. A. Bloomfield Food restriction and simulated microgravity: effects on bone and serum leptin J Appl Physiol, April 1, 2008; 104(4): 1086 - 1093. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 From the Cover: Hydrogen and oxygen isotope ratios in human hair are related to geography PNAS, February 26, 2008; 105(8): 2788 - 2793.
|
|
|
|
|
|
R. Gudivaka, D. A. Schoeller, R. F. Kushner, and M. J. G. Bolt Single- and multifrequency models for bioelectrical impedance analysis of body water compartments J Appl Physiol, September 1, 1999; 87(3): 1087 - 1096. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
