Isocaloric

Gilbert

diets: effects of dietary changes12

A Leveille,

Phi)3

and Paul

F Cloutier,

Discussion

158

Am

J C/in

Nuir

l987;45:

158-63.

Printed

planning
diets. (For research
purposes
it must
be clear that the Atwater
factors are rounded
values.)
The discussion
thus far would suggest that
energy intake can be conveniently
partitioned
and that the energy value of foods is a constant.
Unfortunately, while it is a fact that the absolute energy content of a food is essentially
constant,
the efficiency
with which it is used
varies and is influenced by numerous factors.
In the experimental
design of animal
studies, it is important
to recognize
the complexities associated
with comparing
diets. Because
of the greater caloric density
of fat compared
to carbohydrate
or protein
(9 kcal/g
vs 4
kcal/g), alteringthe percentage of fat in a diet
changes
the ratio of nutrients
to energy.
An
increase in percentage of One component, eg,
fat, necessitates
a decrease
in one or more of
the
other
components,
eg, carbohydrate
and/or
protein.
A change
in the relative
proportion
of protein,
carbohydrate,
or fat may
influence
eating patterns.
For example,
rats
fed diets with low or inadequate
protein
tend
to eat more in an apparent
effort to obtain
sufficient
protein.
Thus, studies involving
dietary manipulations
often require
the use of
pair-feeding.
If control of caloric intake and/or
meal pattern
is considered
necessary,
yokefeeding
may be used. In this procedure,
when
the animal
fed ad libitum
presses a lever to
obtain
food, the pair-fed
partner
simultaneously receives the same amount
of food (7).
Forbes and colleagues
(8, 9) published
several papers in 1946 on the relationship
between
the level of fat in the diet of adult rats and the

From Nutrition
Corporation,
White
2Adcfr
reprint

and Health Sciences, General

Plains, NY.
requests
to: Paul F Cloutier,

Foods
PhD,

General
Foods Corporation,
250 North
Street, White
Plains, NY 10625.
3Present
address:
Nabisco
Brands
Inc., Technology
Center, P.O. Box 1943, East Hanover,
NJ 07936-1943.

in USA.

1987 American

Society

for Clinical

Nutrition

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The laws of thermodynamics

apply to animal energy balance just as they apply to nonliving systems.
The chemical
energy in food
is converted
to work, heat, or stored energy,
predominantly
as fat, by the bodys metabolic
processes.
Figure 1(1-3)
depicts a partitioning
of energy
intake that has evolved
over time
(2,4,5).
It is important
to recognize,
however,
that this model has limitations,
the primary
shortcoming
being the inability
to account
easily for metabolic
adaptations.
Gross energy is the total amount
of energy
in food. It can be measured
using bomb calorimetry
and includes
both digestible
and
nondigestible
(ie, crude fiber) sources.
Digestible energy is not the total energy available
to
the animal
because
it still includes
incompletely
oxidized
products,
such as urea excreted in urine and possibly
ketones
excreted
in urine and expired
air.
Metabolizable
energy is the energy directly
available
to the animal.
Some of it is lost as
heat in what has been referred
to as specific
dynamic
action (SDA) or heat increment
of
foods. Essentially,
this heat is considered
waste
heat
although
it may
contribute
to the
maintenance
of body temperature.
The remaining
energy
is net energy;
it is used for
maintenance
of basal body
functions,
for
physical
activity
resulting
in the performance
of work, and for productive
processes
including growth,
pregnancy,
and lactation.
Around the turn of the century,
Atwater and
Bryant measured
caloric value of various foods
and diets consumed
by humans
with diets that
were popular
in the late 19th century.
From
their calculations,
the Atwater
factors,
still
commonly
used today, were derived.
A summary of these data is shown in Table 1 (6).
These values, usually expressed
as kcal/g, are
estimates
of metabolizable
energy;
they are
useful for estimating
caloric
intake
and for

PhD

ISOCALORIC

DIETS

159

GROSS ENERGY
100

Fecal energy

I:

DIGEST] BLE ENERGY

Urinary

energy

METABOLfl A8LE

ENERGY

25

NET ENERGY
Maintenance
Work
Productive

Functions

10

30

Percent

of

Fat

in Diet

FIG 2. Efficiency of use and heat production

of food
energy in diets with increasing percentage of fat content
and constant gross energy, protein,and essentialnutrients
(based on data from ref8, 9).

FIG 1. Classificationof energy in food (adapted from

ref 1-3).

efficiency
of use of dietary
energy.
In those
studies
dietary
fat varied
from 2% to 30%,
while intake of gross energy, protein,
and essential
nutrients
remained
constant.
Researchers
observed
that as the dietary fat content increased,
relative
heat production
decreased.
Thus, with increasing
fat intake the
apparent
efficiency
of food use increased,
allowing for more energy to be stored in the animal carcass (see Fig 2). In essence,
more energy is stored as fat in the body as the proportion
of fat to carbohydrate
increases
in the
diet.
Increasing
the protein level of the diet at the
expense of carbohydrate
also results in changes
in apparent
energy efficiency.
Donald et al (10)
observed
that adult rats fed a high-protein
diet
gained more weight than a similar
group fed
TABLE
1
Basis for Atwater

factors*
Gross
energy

Digestible
energy

5.65

5.20

4.00

4.15

4.00
8.90

4.00
8.90

Metabolizable
energy

Atwater
factors

a low-protein
diet when the content
of dietary
fat was maintained
at a constant
level and levels of protein
varied from 5% to 25%. The animals had free access to food and water. Absolute food consumption,
ie, g/rat, was not
significantly
different
between
the 5% and 25%
groups.
Yet total body weight gain and body
fat were higher in the 25% group (Table 2).
Humans
appear
to respond
in much
the
same way as rats to changes
in dietary
composition.
Danforth
(11) noted that lean subjects
gained
weight
relatively
easily
when
overfed
fat but not when fed a mixed diet of
carbohydrate
and fat. In an earlier study by
Miller
and Mumford
(12), researchers
observed that students
overfed a high-protein
diet
gained more weight than a group of students
fed a low-protein
diet with a similar
number
of calories.
The weight gain for both diets was
less than the predicted
value.

TABLE 2
Final body weight and body fat of rats fed ad libitum
low- and high-protein diets of equal caloric contents
Protein

Protein (kcal/g)
Carbohydrate
(kcal/g)
Fats (kcal/g)
*

9.40

Based on original data of

Atwater

and

Bryant

9
(6).

Based

in diet

Body wt

Body fat

5
25

397
487

16
24

on ref(l0).

Downloaded from ajcn.nutrition.org by guest on September 29, 2014

Heat including
Specific dynamic action
or
Heat
increment
of foods

LEVEILLE

160

AND

PROTEIN

CARBOHYDRATE

Ji

Ketogenic

CO2

ACIDS

+
+

ENERGY

FIG 4. Metabolic
bohydrate.

pathways

with intake

of excess

car-

for the conversion

of amino acids to fat is high,
-24%. In the case of dietary carbohydrate
(Fig
4), complete
oxidation
would produce
essen-

PROTEIN

CAOHYDRATE

FAT(Triglycerides

GLrOSE

GLU ,SE

Glucogenic
AMINO
ACIDS

FAT Trig1ycerjj

FATTY

>P9LJVATE

<

Glucogenic

PYRIATE

> GLYCEROL

AMINO
ACIDS

1<

ii IKI__

5 GLYCEROL

>ACETYL

C0A<

>FATTY

ACIDS

Ketogenic

ACE

CoA

> FATTY

ACIDS

KREBS
CYCLE

#{231}LE

V
El

CO2

CO2

H20

H2O

ENERGY

ENERGY

FIG 3. Metabolic
tein.

pathways

with intake

of excess

pro-

FIGS. Metabolic
triglycerides.

pathways

with intake

of excess

fat as

Downloaded from ajcn.nutrition.org by guest on September 29, 2014

Level of dietary
energy
intake
has been
shown to influence
the use of dietary protein
in humans
(13). Inadequate
energy intake reduces the apparent
efficiency
of nitrogen
use.
On the other hand, excess energy intake may
increase
retention
of nitrogen.
Most studies in
humans
indicate
that the effects of energy and
protein
intakes
on fat metabolism
are interrelated
(14-16).
For example,
in studies
of
isocaloric
exchange
of fat for carbohydrate,
the
efficiency
of the use of dietary protein
was improved on diets in which more energy was derived
from
carbohydrates
than
from
fats.
This protein-sparing
effect was more noticeable under
situations
where energy
intakes
were marginal
and individuals
were losing
weight (17).
At least part of the observed
differences
in
efficiency
between
fat, carbohydrate,
and protein can be explained
on theoretical
grounds.
Figures 3,4, and 5 illustrate
schematically
the
metabolic
fate of protein,
carbohydrate,
and
fat, respectively.
For example,
as depicted
in
Figure 3, protein
that is not needed to replenish body protein
is degraded
to amino
acids,
which are deaminated
and oxidized
to provide
energy or are converted
to fat. The energy cost

CLOUTIER

ISOCALORIC

DIETS

161

tially 100% of available

energy
as heat and
chemical energy stored as ATP. Conversion
of glucose to fat can occur at a cost of -28%
of available
energy. On the other hand, if cara)
bohydrate
is stored as glycogen,
only --5% of
available
energy is lost. Finally,
as shown in
FigureS,
dietary fat can be catabolized
to yield
a)
C
energy
or, if not immediately
used, can be
converted
into triglycerides
and deposited
into
RMR
a)
adipose tissue at a minimal
energy cost of only
-7% (18).
Energy expenditure
is normally
divided into
II
several components
as shown in Figure 6(11,
AA
1
2
3
19, 20). The resting metabolic
rate (RMR)
is
the energy expended
for essential
body funcTime in Hours
tions. The basal metabolic
rate (BMR),
the
FIG 7. Schematic
diagram of thermic effect of exercise
more familiar
term, is measured
early in the
(see data in ref 21, 22).
morning
upon wakening
after a 12-18-h
fast
and before any physical
activity.
It is a little
lower than the RMR. RMR typically
accounts
the basis of lean body mass. Starvation reduces
for 60-75%
of the total daily energy expenRMR,
while overeating causes an increase.
diture and varies with age, sex, and body comRegular
exercise also increases
RMR (21, 22).
position.
RMR appears
to be similar
in both
The second largest component
of energy
lean and obese individuals
when expressed
on
expenditure
is the thermic
effect of exercise
(TEE) or the amount
of energy used in phys70
ical activity (Fig 7). This component
is the
most variable and the one most subject to volRMR
untary changes to achieve energy balance.
60
Muscular activityisonly
30% efficient.For
I-.
BMR
sedentary
individuals TEE may account for
only 15% of daily energy expenditure
(11).
w
Q.
)<
The thermic effectof food (TEF) (also called
diet-induced
thermogenesis,
specific dynamic
action, and heat increment
offood)
is the increase in energy expenditure,
above the RMR,
TEE
during the several hours following a meal (Fig
8). TEF is presumably
determined by the
digestion, absorption, transport, metabolism,
and storage of ingested foods. The magnitude
TEF
of TEF isaffected by the composition and caloric content of the meal and the nutritional
10
status of the individual (2, 11, 23).
,4
Heat is produced
as part of RMR,
TEE,
<
UTEF, and adaptive
thermogenesis
(AT). This
lastcomponent
has been described
in animals
but is less understood
in humans.
AT is usually
-10
seen as a change in RMR as a result of adaptation to stressful conditions, such as
-ju
changes in food intake
and temperature.
A
good example of AT iscold adaptation in rats.
FIG 6. Compartmentalization
of energy expenditures
After a period of time, rats increase heat pro(adapted
from ref 19).
C

L.
C

VA

.
.

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162

LEVEILLE

AND

CLOUTIER

physical
formance

work, tissue storage,

and/or
of physiological
functions.

the per-

Conclusions

4,
S.

Protein
C
C

I.
4,

Fat

C
Lu

ii
Time

Meal

in Hours

diagram of the thermic

from ref 11, 20).

effect of food

duction
and maintain
normal
body temperatures without
shivering.
The source
of this
heat is located in the specialized
mitochondria
of brown adipose
tissue, which is distributed
predominantly
around
critical
organs
(24).
Another
example
of AT found in humans
and
animals
is the response
of RMR to changes
in
intake of nutrients. During prolonged
periods
of food restriction,
RMR is gradually
reduced.
When
intake
of nutrients
is excessive,
the
RMR increases.
In both cases, the changes are
more than can be predicted
from calculations
when energy condition
is in balance
(19).
The extra heat produced
from the ingestion
of food, as exemplified
by TEF and AT, is a
waste product
as far as the economy
of the
animal is concerned. One possible function
for this waste energy,
however,
is regulation
of body weight as a supplement
to appetite
control.
The mechanisms
involved
are not
understood
completely.
Some of the mechanisms for which evidence
exists include
sympathetic
nervous
system activity,
futile metabolic cycles, uncoupling of oxidative phosphorylation, and Na-K
ATPase
activity
(sodium
pump)
(20, 24).
The metabolizable
energy
from
food is
transformed
into heat and net energy. The degree of heat production
from all mechanisms
influences total net energy. Following the laws
of conservation
of energy, as less heat is produced,
more energy
becomes
available
for

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FIG 8. Schematic
after a meal (adapted

After

1) Research
involving
dietary
manipulations must consider
and control the nutrientto-energy
ratio of the diets and total caloric
intake.
2) The composition
of the diet with respect
to the proportion
of the major
nutrientsprotein,
fat, and carbohydrate-has
a profound and variable
effect on the efficiency
of
food energy use and ultimately
on the results
of an experiment.
3) The level of energy intake relative to
maintenance
can significantly
influence
energy
expenditure
and hence the net energy value of
diets and foods.

ISOCALORIC
13. Van Es AJH, Vogt JE, Niessen CH, et al. Human
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DP, Wayler AH, Scrimshaw
NS, Young
VR. Quantitative
effect of an isoenergetic
exchange
of fat for carbohydrate on dietary protein utilization
in healthy young men. Am J Clin Nutr l979;32:22l726.

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