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Energy intake required to maintain body weight is not

affected by wide variation in diet composition13

Rudolph L Leibel, Jules Hirsch, Burton E Appel, and Gregg C Checani

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ABSTRACT Diets rich in fat may promote obesity by lead- One group of investigators concluded that “fat intake may play
ing to a greater deposition of adipose-tissue triglycerides than a role in obesity that is independent of energy intake” (4).
do isoenergetic diets with less fat. This possibility was examined The ultimate test of the validity of such a proposition is the
by a retrospective analysis of the energy needs of 16 human long-term effect on metabolic efficiency of perturbations of diet
subjects (1 3 adults, 3 children) fed liquid diets ofprecisely known composition. Using the technique of caloric titrimetry (9), in
composition with widely varied fat content, for 15-56 d (33 ± 2 which a formula diet ofspecified composition is fed over a period
d, i ± SE). Subjects lived in a metabolic ward and received fluid ofweeks under circumstances ofcontrolled physical activity, we
formulas with different fat and carbohydrate content, physical examined the effect on metabolic efficiency (as reflected by
activity was kept constant, and precise data were available on changes in body weight) ofextreme changes in the composition
energy intake and daily body weight. Isoenergetic formulas con- ofotherwise isoenergetic diets. This technique was made possible
tamed various percentages ofcarbohydrate as cerelose (low, 15%; by the careful collection ofdata on the effects offormula feeding,
intermediate, 40% or 45%; high, 75%, 80%, or 85%), a constant in studies done over many years by EH Ahrens and his colleagues
15% of energy as protein (as milk protein), and the balance of at the Hospital of the Rockefeller University ( 10, 1 1).
energy as fat (as corn oil). Even with extreme changes in the fat-
carbohydrate ratio (fat energy varied from 0% to 70% of total Subjects and methods
intake), there was no detectable evidence ofsignitlcant variation
in energy need as a function of percentage fat intake. Am J The records of all subjects studied by the Lipid Laboratory
Cliii Nuir l992;55:350-5. ofthe Rockefeller University Hospital between 1955 and 1965
who were fed liquid-formula diets ofvarious carbohydrate (CHO)
and fat composition were reviewed. These diets were prepared
KEY WORDS Obesity, dietary fat, dietary carbohydrate,
in the research kitchen of the Rockefeller University Hospital.
diet composition, energy requirements Protein (20.9 Id/g), which represented a constant 1 5% of energy,
was derived from milk protein. Fat (37.7 kJ/g) was from corn
Introduction oil. CHO (16.7 kJ/g) was supplied as cerelose, a hydrated form
of glucose. Coefficients of digestibility were used to determine
Sixty years ago, LH Newburgh and his colleagues examined the final available energy value ofthe constituents ofthe formula
the possibility that so-called endogenous obesity might be the (12): protein, 0.92; fat, 0.95; and carbohydrate, 0.98. Data re-
result of special metabolic factors unrelated to energy intake or garding bomb calorimetry of these formulas are not available.
physical activity (I). They found no evidence for such purely Bomb calorimetry performed on eight batches ofsimilar formula
endogenous obesity and also demonstrated that the long-term prepared in the research kitchen of the Rockefeller University
effect of any diet on body weight is related only to the total Hospital between April 1988 and July 1990 had a coefficient of
energy content of the diet. Other features of the diet such as variation for Id/g of 1 .9%. Such formula shows a ±0.2% cor-
carbohydrate or fat content did not, in the long run, have con- respondence between bomb calorimetric and calculated energy
sequential effects on body weight. content. In studies designed to examine the effects of dietary
In recent years the adverse effects of high-fat diets on health lipid type and quantity on lipoprotein metabolism, the per-
have been emphasized, and the possibility that a high-fat intake centage of CHO in the diet was systematically altered by iso-
may be accompanied by some special in vivo economy of energy
metabolism has led to speculation on the role ofdiet composition
I From the Laboratory of Human Behavior and Metabolism and the
in the production of obesity. Various investigators have reported
Pew Center ofNutritional Excellence, Rockefeller University, New York.
a positive correlation between body fat and the percentage of 2 Supported in part by grants DK 30583 and RROO 102 from the Na-
fat in isoenergetic diets fed to rodents (2, 3) and humans (4, 5)
tional Institutes of Health.
and a lack of effect of dietary fat on respiratory quotient (RQ)
3Address reprint requests to RL Leibel, Laboratory of Human Be-
in human subjects studied for 9 or 24 h after the feeding of fat havior and Metabolism, Rockefeller University, 1230 York Avenue, New
(6, 7). Additionally, 24-h energy balance in a respiratory chamber York, NY 10021.
is reported to be due almost exclusively to differences in fat Received October 25, 1990.
balance and unrelated to carbohydrate or protein balance (8). Accepted for publication March 6, 1991.

350 Am J C/in Nuir l992;55:350-5. Printed in USA. © 1992 American Society for Clinical Nutrition

Anthropometry and diet characteristics of adults


Mean Days Percent Percent CORREC

ID Sex Age weight WT INTS Height BMIt on diet CHO fat Energy Id

y kg kg cm d % % Id kJ

1 M 56 76.01 75.59 165 27.9 24 45 40 10067 9071

76.10 76.19 - - 32 75 10 10067 10242
2 M 43 75.28 75.41 167.5 26.8 43 45 40 9937 10113
75.42 75.68 - - 28 85 0 9991 10519
3 M 55 96.21 95.46 173.5 32.0 23 15 70 13862 12016

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95.95 96.21 - - 18 85 0 13862 14652
4 M 53 59.42 59.03 157.5 24.0 39 15 70 9 100 8690
58.81 58.19 - - 44 75 10 9100 8280
5 M 41 62.26 62.31 164.5 23.0 15 15 70 10330 10330
64.02 63.87 - - 39 45 40 10330 10096
6 M 54 65.93 66.25 178 20.8 34 45 40 10201 10728
66.11 66.13 - - 38 85 0 10201 10200
7 M 49 63.80 63.95 164 23.7 25 45 40 9414 9765
64.13 63.92 - - 42 85 0 9414 9 121
8 M 41 70.72 70.87 170 24.5 22 45 40 10590 10590
71.04 71.09 - - 42 85 0 10590 10590
9 M 57 61.58 60.98 175 20.1 52 45 40 10330 9657
61.56 61.79 - - 47 85 0 9284 9577
10 M 64 70.24 70.68 165 25.8 25 15 70 8498 9493
70.55 70.78 - - 18 85 0 8498 9201
11 F 49 45.70 45.42 163.5 17.1 28 45 40 7452 6895
46.95 46.92 - - 18 85 0 6929 6929
12 F 64 52.64 52.84 156 21.6 56 15 70 7322 7468
52.68 52.38 - - 34 75 10 7322 6824
13 F 57 49.07 48.98 155.5 20.3 15 15 70 7322 7322
48.55 48.57 - - 28 85 0 7707 7707

* Time zero intercept of regression line of weight vs days.

t Body mass index, in kg/rn’.
t Id corrected for any weight change during the period of formula feeding.

energetic replacement with fat. These formula diets of varied The daily weights of each subject were examined by regression
composition were fed in random order. Vitamin and mineral analysis ofweight vs time. We found no evidence ofearly changes
supplements were given daily in addition to 2 g NaCI. All subjects in slope for these functions as the 2-wk period proceeded, sug-
lived in the Clinical Research Center (Rockefeller University gesting that acute changes in water excretion and retention were
Hospital); physical activity was constant at activities of daily not occurring with changes in diet composition. This is most
living with no additional exercise. The formulas were always fed likely the result of feeding exactly 2 g NaCI/d in all dietary pe-
in quantities sufficient weight as
to maintain a constant body riods. Therefore, all days on a given diet were included in these
nearly as possible. Interim adjustments in the quantity of formula analyses. The slope of each weight-vs-time plot was examined
were made to achieve this goal. Weights (to nearest 0. 1 kg) were for significant deviation from zero. If the P value of this rela-
obtained each morning with the subject clothed in underwear. tionship was < 0.05, the energy requirement for the individual
Though stools were not collected from these subjects, similar was corrected for this intercurrent change in weight. In making
subjects on similar diets did not show differences in the fraction this correction we assigned the conservative (high) value of 29.3
of energy intake excreted in the stool (EH Ahrens, personal Id/g to the weight change. The corrected daily energy require-
communication, 1991). ment was calculated as:
The records of all patients
studied from 1955 to 1965 were
searched for consecutive in which patients
periods were fed for- CORREC KJ = Id formula - 29.3
mula diets of differing CHO-to-fat ratios. For inclusion in this x (regression slope in grams per day).
analysis, each period of formula feeding had to be 2 wk and

the subject had to have remained weight stable (to within 1 kg) The time zero intercepts (WT INT) of these plots are given in
within that period. Reasons for rejection of records were lack Table 1. The clinical characteristics and diet specifications for
of feeding of two different formulas or the absence of feeding each adult subject are given in Table 1.
periods of 2 wk. A total of 47 patient records were reviewed Many ofthese subjects were fed a no-fat diet for several weeks
to obtain 16 (13 adults and 3 children) fitting the above criteria. at a time. At the time these studies were done, it was uncertain

whether essential fatty acid (EFA) deficiency would occur in TABLE 2

adult humans. Only one subject (subject 6, Table 1) developed Anthropornetry and energy requirements of 13 adult subjects
symptoms possibly related to EFA deficiency (ie, mild eczema on various carbohydrate diets
relieved by the addition of fat to the diet). Intermediate
This study was approved by the Institutional Review Board Low CHO CHO High CHO
of the Rockefeller University. (n=6) (n=8) (n=12)
Energy requirements of each subject were expressed both ab-
Weight (kg) 65.0 ± 6.9 64.4 ± 3.4 65.7 ± 3.9
solutely and corrected for significant slope ofthe weight-vs-time Energy (Id) 9406 ± 1004 9791 ± 356 9401 ± 527
plots. In addition each subject’s requirements were expressed kJCORREC 9217±732 9611±431 9485±607
per unit of body surface area (13) or per amount of body Age(y) 55.7 ± 3.5 48.7 ± 2.3 53.5 ± 2.1
weight#{176}73.Both body surface area and weight#{176}”provide good Days on diet (d) 28.8 ± 6.5 33.4 ± 3.8 32.4 ± 3.1
(kg) 22.8 ± 1.8 22.9 ± 0.9 23.0 ± 1.0
indirect estimates of metabolic mass (14). Statistical analyses
were performed on a VAX PDP 1 1/780 computer running UNIX (U/rn’) 5519±305 5611 ± 113 5422± 151

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BMDP (1 5) and UNIXSTA T (16) programs. Energy/wt#{176}7’
(U/IgO.7i) 410 ± 17 427 ± 8 410 ± 8
Results (kY/rn’) 5439 ± 180 5506 ± 163 5448 ± 180
406 ± 13 418 ± 13 410 ± 8

Six subjects had been maintained on low CHO formula, eight * i ± SE. Thirteen subjects were studied on two diets, hence a total
on intermediate CHO, and 12 on high CHO. The mean period of 26 feeding periods. The characteristics of all subjects examined on
on each diet was 32 ± 2 d (i ± SE). A plot of the daily weight each diet (low, intermediate, or high CHO) are given.
is shown in a typical patient (subject 12) who received a 10%-
fat diet for 5 wk followed by a 70%-fat diet for 8 wk (Fig 1). The
small corrections, calculated as described, are shown in Table [difference of means (low - high) = -51.5 Id; I = -0.2236; P
1. The absence of effect ofdiet composition on energy require- = 0.8305).

ments to maintain weight are shown in Table 2. This table pro- Because the no-fat diet might have induced subclinical EFA
vides summary data on the weight-maintenance energy require- deficiency, a separate analysis was done ofthe nine subjects who
ments of the 13 adult subjects studied on two diets of differing received a 0-fat diet vs the 17 dietary periods of those on 10-
percent carbohydrate. Regression plots of diet vs various body 70% fat intake. Linear-regression analysis of energy and COR-
size indexes for the three diet compositions are shown in Figure REC Id vs SA and O.7S was performed for these two groups,
2. This
figure examines the relationship of measured energy in- and ANOVA of regression coefficients over groups showed no
take (Id) and corrected energy intake (CORREC Id) regressed significant differences between lines of regression for no-fat and
on surface area (SA) and also on weight#{176}75(%,.J1’O.l5). Although fat-containing diets (Table 4). Thus, there was no aberration of
energy requirements were highly significantly related to body energy requirement in those receiving a no-fat diet.
size indexes, analysis of variance (ANOVA) of regression coef-
ficients over groups did not indicate any significant between-
group difference, regardless of the body size index used in the Table 5 shows data for the three children studied. Although
abscissa (Table 3). Five of the subjects who had received both energy for weight maintenance
need was 30-40% higher (ku
very-low-CHO (1 5%) and very-high-CHO (75-85%) diets were kg#{176}”)
than that for adults, no significant effect of diet compo-
separately examined.Paired t tests of the energy requirements sition on energy requirements is seen in children, as is the case
(CORREC Id) of these subjects on the two diets indicated no with adults.
difference due to diet composition [difference of means (low
- high) = -334.7 Id; t = -0.558; P = 0.6 1]. Similarly, a com- Discussion
parison (paired t test) ofenergy requirements in the seven subjects
who received both moderate-CHO (45%) and very-high-CHO The energy content of foodstuffs is conventionally determined
(75, 85%) diets indicated no difference due to diet composition by measuring heat released by the complete combustion of the


1O%Fat 70% FatS

FIG 1. A l3-wk study ofsubject 12, first on 10% (75% CHO) ofenergy intake as fat and then on 70% (15% CHO)
ofenergy intake as fat. During both periods, 7322 U per day were fed. Actual Id combusted were corrected, as described
in Subjects and Methods, to 7468 U and 6824 Id per day, respectively. It is notable that there was only 1 kg of weight
variation during the entire study.

14000 0 16000
c DO 10000
0 0
8000 U

6000 6000
1 .4 1 .6 1 .8 2.0 2.2 2.4 1 .4 1 .6 1 .8 2.0 2.2 2.4

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14000 0 16000

, C C.)
. 10000 w
8000 U c0
.00 8000

6000 6000
15 20 25 30 35 15 20 25 30 35

wr 0.75
& LOWCHO=15%
. INTERMEDIATE CHO = 40% or 45%
0 HIGH CHO = 75%, 80% or 85%

FIG 2. Regression analyses of 24-hr energy intakes vs either body surface area (SA) or body weight#{176}”(WT#{176}75)
liquid-formula diets
of different CHO content. n = 6, 8, and 12, respectively, for low-CHO, intermediate, and high-
CHO diets. All subjects are adults.

specific components of the diet. A recent analysis of the energy ofthe energy value offoodstuffs as used to calculate total energy
in foodstuffs showed that conventional food fats have a heat of expenditure by indirect calorimetry may be in error by 5% of
combustion of 37.690-40.091 Id/g. The metabolizable energy the true value even under the most careful circumstances (17,
(corrected for urea) of conventional food protein varies from 1 8). There could be even greater error if, because of differences
I 7.43 1 to 2 1 . 1 50 Id/g. CHOs vary less: starches, 17.48 1 Id/g; in the metabolic handling of different foods, the actual contri-
glucose, 1 5.560 Id/g; and sucrose, 16.481 kJ/g (17). An analysis bution to systemic fuel oxidation is not directly predicted by
energy release as measured in vitro. Specifically, the ATP re-
TABLE 3 quired for the activation of amino acids preparatory to their
Regression equations (y = rnx + b) for the plots in Figure 2 incorporation into proteins and the ready interconversion of
glucose to and from glycogen via energy-requiring steps could
Plot Equation r P(cx) reduce the actual energy value of these substrates in terms of

Low CHO y = 9699x - 6950 0.92 0.009
Intermediate CHO y = 699 1 x - 2393 0.88 0.005 TABLE 4
HighCHO y=9025x-6146 0.93 0.000 For each of the four plots, the separate regressions for each of the
B three levels of CHO feeding examined for differences in regression
Low CHO y = 7243x - 2992 0.94 0.004 coefficients by ANOVA*
Intermediate CHO y = 7979x - 4297 0.83 0.0 16
High CHO y = 9443x - 8962 0.96 0.000 Plot ANOVA P (a)
LowCHO y=5l5x-2330 0.92 0.010
A: Id vs SA F14,01 = 0.464 0.761
B: CORREC U vs SA F14201 = 1 . 1 77 0.351
Intermediate CHO y 310x - 2720 0.79 0.020
High CHO y = 473x - 1477 0.92 0.000
C: Id vs O.75 F14,,1 = 0.830 0.522
D: CORREC Id vs O.73 F14201 = 1.236 0.328
Low CHO y = 38 1 x - 590 0.93 0.008 * There was no significant correlation between the occasional small
Intermediate CHO y = 339x - 1883 0.72 0.050
shifts in apparent body energy stores (Id - CORREC U) and either SA
High CHO y = 556x - 3343 0.95 0.000
(r = -0.027, P = 0.89) or O.75 (r = 0.15, P = 0.94).

Anthropometry and diet characteristics of children


Mean Days Percent Percent CORREC

ID Sex Age weight WT INT Height BMI on diet CHO fat Energy kJ

y kg kg cm d % % k.J

14 M 9 19.91 19.66 115 15.0 36 40 40 6146 5766

20.77 20.37 - - 41 80 0 6146 5590
15 M 10 20.80 20.59 115.5 15.7 40 40 40 5623 5330
21.44 21.18 - - 30 80 0 5623 5125
16 F 8 26.19 26.10 137 20.0 42 40 40 6590 6590
25.88 25.91 23 80 0 6590 6590

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- -

net energy provision for in vivo chemical respiration. Conversely, Although the number ofsubjects studied was relatively small,
the presumably lower rate and energy cost of hydrolysis and each individual was studied for extended periods of time (15-
reesterification offree fatty acids might result in greater efficiency 56 d, i 33 d) on two diets. Comparable studies concluding no
ofhandling ofdietary fats and hence an apparent relative increase difference in energy requirements on diets of differing CHO
in net in vivo generation of ATP. Differences in the thermic content were conducted for a maximum of 6 d ( 19-22). The
effect of feeding when CHOs are compared with protein or fat extended period of our diets adds considerable power to the
is yet an additional cause for potential systematic differences in design of this study, as demonstrated by the following calcula-
the energy value of foods in vivo as compared with laboratory tions: our assignment ofa value of29.3 kJ/g to any intercurrent
measures of heat of combustion. weight changes is extremely conservative, a more likely figure
Short-term studies (24-48 h) in humans suggest that a sub- being I 3- 1 7 Id/g. Nonetheless, by using the figure of 29.3 Id!
stantial (4l00 Id) dietary fat supplement does not immediately g, the confidence interval (level 0.95) around the slope of weight
promote the use offat as a metabolic fuel (7). Our results suggest vs days (±8.2 g/d) and the total energy ingested by each adult
that this phenomenon does not operate in a more extended time subject minus the 95% confidence limits (range) ofthe differences
frame ( 8 wk) to produce preferential storage of dietary fat in in energy requirements on diets ofdiffering composition equals
adult humans. This point was in fact made by Schutz et al (7), ± 7853 Id/32 days which equals ± 2.7% of total kilojoules in-
who emphasized that human subjects achieve weight equilibrium gested. Thus, despite the relatively small number of subjects
on high-fat diets despite the operation of these short-term phe- studied, when the large number of total kilojoules fed to each
nomena. Other investigators, studying subjects over shorter time subject during each diet period are taken into account, it is un-
periods than we used here, reported no effect on various aspects likely that we failed to detect a 5% difference in energy effi-
ofenergy expenditure (24-h expenditure, resting metabolic rate) ciency between diets. However, very small differences in the
of high- vs low-CHO diets (19-23). On the other hand, Prewitt efficiency of energy metabolism integrated over prolonged pe-
et al (24) recently compared the effects on energy need and body riods oftime can theoretically lead to clinically significant shifts
composition of switching 18 outpatient female subjects (BMI in body composition. For example, 2% greater metabolic effi-
18-44) from a 37% fat diet (1 4 wk) to a 21.4% fat diet (1 20 ciency of one isoenergetic diet vs another would (assuming
wk). On average, while ingesting the lower fat diet, these subjects 10 460 Id/d intake and 29.3 Id/g weight gain) lead to a 3.2 kg
required an average of 10.5% more calories and lost 2.8% (1 1.3% weight gain in 1 y.
ofbody fat) despite efforts to feed sufficient calories to maintain A formal analysis ofthese data can be made. However, such
weight. Differences in physical activity and noncompliance on analysis is very sensitive to sample size and cannot readily be
the lower-fat diet may account for some of the observed differ- made to account for the special power of this study in the large
ences. number ofdays for which each subject was maintained on each
Forbes (25) recently reviewed a series of studies in which hu- diet. With this caveat in mind, the /3 (type II) error can be es-
man subjects were overfed for 2- 1 2 wk and found that although timated in two ways. 1) The variance about the slope of the
obese individuals appear to deposit a larger proportion of excess regression equation relating CORREC Id to surface area (plot
energy intake as fat, the energy cost ofweight gain in either lean B, Fig 2) may be used to estimate the likelihood of missing dif-
or obese subjects was not significantly influenced by the com- ferences ofany desired magnitude between energy requirements
position of the excess energy fed. on formulas of different composition. Assuming, for example,
The lack of agreement between our data and those obtained a 10% decrease in energy efficiency (CORREC Id) conferred by
in rodents (2, 3) may be because rodents are growing continu- the high-CHO (75% or 85%) formula (n = 12 adult studies) and
ously, introducing a possible effect ofgrowth itselfon the response variance proportional to that for the high-CHO formula, the
to diet composition. Against this explanation is our finding of probability ofa /3 error (acceptance of a false null hypothesis) is
lack of diet-composition effect on energy requirements in three P = 0.1 1 (26). 2) A direct comparison between the distributions
children in this study (Table 5). These rodents were also fed ad ofCORREC Id for the seven adult subjects studied on both 45%
libitum (permitting weight gain), whereas our human subjects’ (intermediate) and 75% or 85% (high) CHO gives paired
intake was designed to maintain body weight. = -0.2236, P(a) = 0.8304, and SD ofdifferences = 607 Id. For

Pu. = 0.05, the between-diet difference is 912 Id (one tail). That 8. Abbott WGH, Howard BV, Christin L, et al. Short-term energy
is, the probability of a difference between the two diets as large balance: relationship with protein, carbohydrate, and fat balances.
as 9 12 kJ/d escaping detection is 0.05. This difference represents Am J Physiol l988;255:E332-7.
9.5% of total energy intake per day. For reasons discussed 9. Leibel RL, Hirsch J. Reduced energy requirements in reduced-obese
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above, such calculations overstate the probable error in this study.
10. Ahrens EH, Insull W, Hirsch J, et al. The effect on human serum-
Similar results might not have been obtained in a group of
lipids of a dietary fat, highly saturated, but poor in essential fatty
obese individuals or lean individuals susceptible to obesity. There
acids. Lancet l959;l:l15-9.
may be an interaction of diet composition and predisposition 1 1. Ahrens EH. The use ofliquid formula diets in metabolic studies: 15
to obesity, with higher dietary fat content facilitating the expres- years’ experience. Adv Metab Disord l970;4:297-332.
sion ofa more efficient metabolic phenotype (27). In this regard 12. Watt BK, Merrill AL. Composition of Foods: raw, processed, pre-
it is of interest to note that the three subjects (subjects 1-3 in pared. Agriculture handbook no. 8. Washington, DC: US Govern-
Table 1) with highest BMIs had lower CORREC Id on the higher- ment Printing Office, 1963.
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equal or higher CORREC U on the higher-fat diets. It is also area ifheight and weight be known. Arch Intern Med l9l6;17:863-
possible that fat’s putative enhanced efficiency as a metabolic 71.
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Malabar, FL: Robert E Krieger, 1975.
15. Dixon WJ, ed. BMDP statistical software manual. Berkeley, CA:
Finally, the physical activity of some of our subjects was
University of California Press, 1988.
somewhat diminished by their restriction to a metabolic ward.
16. Perlrnan G. Unixstat. Data analysis programs for UNIX. Tyngsboro,
There may be interactions between physical activity and diet
MA: Wang Institute ofGraduate Studies, 1986.
composition that predispose to fat accumulation (28); such in- 17. Livesey G, Elia M. Estimation of energy expenditure, net carbo-
teractions were not examined in this study. hydrate utilization, and net fat oxidation and synthesis by indirect
It has been noted that obese individuals have a preference for calorimetry: evaluation of errors with special reference to the detailed
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