Carbohydrates as a source of energy1’2

Eric J#{233}quier

ABSTRACT Carbohydrates are the main energy source of cose metabolism represents a small proportion, 2 mol Al?, com-
the human diet. The metabolic disposal of dietary carbohydrates pared with 38 mol ATP synthesized by complete oxidation of 1
is direct oxidation in various tissues, glycogen synthesis (in liver mol glucose, ie, 5% of the total Al? synthesis resulting from
and muscles), and hepatic de novo lipogenesis. This latter path- aerobic glucose metabolism.
way is quantitatively not important in man because under most A major nutritional and metabolic question is that of the reg-
conditions the rate of de novo lipogenesis does not exceed the ulation of body weight and the mechanisms involved in the
concomitant rate of lipid oxidation in the whole body. Thus, di- pathogenesis of obesity. It is true that body weight stability usu-
etary carbohydrates do not appear to increase an individual’s fat ally reflects energy balance, ie, that energy intake must be equal
content by de novo lipogenesis. The intake of dietary carbohy- to energy expenditure during prolonged periods of time. This
drates mainly has the effect of inhibiting fat oxidation while glu- means that the maintenance of a constant body weight and body
cose oxidation is increased. Dietary carbohydrates are involved composition depends on the simultaneous achievement of pro-
in the control of energy balance because the regulation of food tein, carbohydrate, and fat balances. The ability to maintain pro-
intake depends, in part, on the carbohydrate need of the individ- tein balance over a large range of protein intake has been well
ual. Because there is an obligatory requirement for glucose in established; in adult individuals there is an adjustment of amino
several organs such as the brain, a spontaneous increase in food acid oxidation to the protein intake. In contrast, carbohydrate and
intake is seen when the diet has a low-carbohydrate, high-fat fat intakes are the major determinants of changes in body weight
content. Therefore, the present nutritional advice of increasing (1). It is, therefore, important to study the mechanisms involved
the proportion of carbohydrate energy while decreasing that of in achieving carbohydrate and fat balances in man.
fat in the everyday diet has strong scientific support in terms of
the regulation of the energy balance. Am J Clin Nutr
1994;59(suppl):682S-5S. Metabolic disposal of carbohydrates

During the postprandial phase, glucose is the main carbohy-

KEY WORDS Carbohydrates, glucose, fat, body weight,
drate that is absorbed. Its metabolic disposal includes three main
obesity
pathways: 1) uptake and direct oxidation in various tissues, 2)
uptake and glycogen synthesis in the liver and muscles, and 3)
Introduction uptake and lipid synthesis in the liver.
After an oral load of 100 g glucose, glycemia reaches a peak
The heat of combustion of starch is 17.5 kJ/g, whereas that of value in 45 mm and then declines to basal concentrations after
glucose is 15.7 kJ/g; this difference is due to the relative pro- ,3 h (Fig 1) (2). Plasma insulin concentrations follow an ap-
portion of carbon, oxygen, and hydrogen atoms in their mole- proximately similar pattern, although the stimulation of glucose
cules (1 g starch hydrolyzed yields 1.11 g glucose). oxidation is of longer duration, ie, 6 h after the glucose load
The energy expended within the body to maintain electro- (Figure 1). This shows that glucose oxidation is stimulated not
chemical gradients, to support biosynthetic processes, and to gen- only by the rise in glucose and insulin concentrations (early re-
crate muscular contraction is mainly dependent on AlP hydro- sponse), but that it is also a consequence of the increased gly-
lysis. It is the rate of AlP utilization that determines the rate of cogen storage in both the liver and skeletal muscles (later re-
substrate oxidation, and therefore, the rate of oxygen consump- sponse). The same pattern is observed after a mixed meal and
tion to resynthesize ATP molecules with a mean energy cost of these responses are not influenced by the fat content of the meal
s’75 kJ for every mole of ATP resynthesized. When 1 mol of (3). This indicates that carbohydrate intake, as a single load or
glucose is metabolized, substrate level phosphorylation in the with a mixed meal, promotes both carbohydrate oxidation and
glycolytic pathway results in the synthesis of 2 mol ATP without glucose storage as glycogen. On a 24-h basis, carbohydrate ox-
oxygen consumption. This anaerobic production of ATP is a idation must obviously correspond with carbohydrate intake, be-
unique feature of glucose metabolism, in that fatty acid or amino cause the daily changes in the body’s glycogen stores are small
acid oxidation is coupled to ATP synthesis through oxidative
phosphorylation only. The anaerobic production of ATP is an ‘From the Institute of Physiology, University of Lausanne,
important component of the oxygen deficit that occurs during Switzerland.
2 Address reprint requests to E J#{233}quier,
Institut de physiologic, 7 rue
high intensity exercise and is illustrated by a rise in plasma lactic
acid concentrations. However, the ATP yield from anaerobic glu- du Bugnon, 1005 Lausanne, Switzerland.

682S Am J Cliii Nutr 1994;59(suppl):682S-5S. Printed in USA. © 1994 American Society for Clinical Nutrition

Downloaded from https://academic.oup.com/ajcn/article-abstract/59/3/682S/4732269

by guest
on 23 February 2018
 CARBOHYDRATES AS A SOURCE OF ENERGY 683S

ered to play an important role in the development of obesity.

Consequently, obese patients are frequently given advice to re-
1400 strict their carbohydrate intake. However, some evidence shows
that de novo lipogenesis does not play an important role in the

! 1200
synthesis and
mans is mainly a hepatic
hydrate in adipose tissue
deposition of body
process,
fat in man.
and fat synthesis
is of little importance (6).
from
Lipogenesis in hu-
carbo-

Hepatic lipogenesis is stimulated when carbohydrate intake is

I
.2 1000 increased (7). However, even after an extremely large oral load
of carbohydrate, 480 g ingested within 2 h by young adult men,
fat synthesis did not exceed fat oxidation (8). Thus, this study
shows that dietary carbohydrate intake mainly has the effect of
reducing fat oxidation, while glucose oxidation is increased. Un-
der conditions of a usual maintenance mixed diet, the rate of de
novo lipogenesis does not exceed the concomitant rate of fatty
acid oxidation in the whole body. Thus, dietary carbohydrates do
not increase an individual’s fat content by de novo lipogenesis
and fat deposited in the adipose tissue comes mainly from in-
E gested lipids. Because the conversion of carbohydrate to fat is a
minor pathway, carbohydrate and fat balances can be studied
E separately. Carbohydrate balance is usually achieved within 24
h. It is therefore likely that the body weight gain, which finally
0 results in obesity, is due to an inability to achieve fat balance.
Nevertheless, net de novo lipogenesis can be observed in hu-
mans under artificial conditions of carbohydrate overfeeding. The
capacity for storing large amounts of dietary carbohydrate by
conversion to glycogen was studied by Acheson et al (9), who
performed a 7-d carbohydrate overfeeding protocol in healthy
young men. This study showed that glycogen stores must in-
crease by 500 g before appreciable de novo lipogenesis begins.
When the glycogen stores become saturated, the only way to

I:
dispose of excess carbohydrate, other than maximal glucose ox-
idation, is through fat synthesis. These findings suggest that the
body’s glycogen stores are not completely filled under normal ad
libitum conditions of food intake. This further supports the con-
clusion that when people consume a regular mixed diet, net de
novo lipogenesis from carbohydrate is a quantitatively minor
pathway in the disposal of dietary carbohydrates.
To investigate the fate of the various sources of energy in
0 60 120 180 240 300 360 420 480 humans, an experimental approach has been to carry out short-
Time term overfeeding studies. The results of one of these studies are
FIG 1. Glucose oxidation, glycernia, and insulinemia measured in briefly summarized here (10). Five young men were overfed for
eight healthy young subjects during 480 miii following an oral load of 9 d at 1.6 times their maintenance requirements (> 8000 kJ/d).
100 g glucose. The overall energy expenditure measured with a respiration
chamber after 9 d of overfeeding increased by 2000 kJ/d, which
corresponds to 25% of the excess energy intake. After 9 d of
in relation to the daily carbohydrate turnover. On a regular mixed
overfeeding, carbohydrate balance calculated on a 24-h basis was
maintenance diet, the rate of carbohydrate utilization matches
achieved (Fig 2), whereas lipid balance was markedly positive
carbohydrate intake to prevent excessive exhaustion or accu-
(Fig 3). These results clearly show that carbohydrate balance was
mulation of glycogen reserves. Thus, it can be concluded that
achieved even under artificial conditions of overfeeding, and the
carbohydrate balance tends to be achieved even when carbohy-
positive fat balance entirely accounted for the altered energy bal-
drate intake varies daily.
ance.

The transformation of carbohydrate into fat

It is often assumed that an excess in carbohydrate intake is The concept of the respiratory quotient-food quotient
readily transformed into fat in humans (4). Liver and adipose ratio
tissue contain the enzymes necessary for the conversion of car-
bohydrate into fat. In young rodents this metabolic process has To better understand the conditions that allow the maintenance
been extensively studied and shown to be important (5). This of body weight, Flatt (1) has defined the food quotient (FO) as
may be the reason why the carbohydrate intake is often consid- the ratio of carbon dioxide produced over oxygen consumed,

Downloaded from https://academic.oup.com/ajcn/article-abstract/59/3/682S/4732269

by guest
on 23 February 2018
 684S JEQUIER

500 g/day 250 giday

Intake
450 200 Intake
Utilization

400 150
Lipid
Storage
350 100

300 50
ization
Days Days
10 o 5 10

I1iMatean
10.9 Mi/d 17.4 MJ/d 10.9 Mi/d 17.4 Mi/d

FIG 2. Carbohydrate intake, utilization, and storage during a maintenance FIG 3. Lipid intake, utilization, and storage during a maintenance diet
diet and an overfeeding period of 9 d in five young men [redrawn from (10)]. and an overfeeding period of 9 d in five young men [redrawn from (10)].
Note that carbohydrate balance is achieved at the end of the protocol. Note that lipid balance is not achieved.

when a representative sample of the diet is oxidized in a bomb likely to be dependent on the carbohydrate than on the lipid bal-
calorimeter ance. The regulation of food intake depends, in part, on the car-
bohydrate need of an individual. Because several organs and tis-
FQ = CO2 produced/O2 consumed
sues, for example the brain, have an obligatory requirement for
When energy balance is achieved over 24 h, FQ is equal to the glucose, one should eat more food to ingest a minimal amount
mean respiratory quotient (RQ) of the subject. of carbohydrates when the diet has a low-carbohydrate, high-fat
content. This hypothesis was confirmed by Tremblay et al (1 1),
FQ = RQ and RQIFQ = 1.0 who showed that a low-carbohydrate, high-fat diet induced a
short-term increase in food intake in young male subjects. There-
This condition means that the fuel mix oxidized corresponds with
fore, a high-carbohydrate, low-fat diet should be a logical ap-
the nutrient intake. In contrast, conditions of positive energy bal-
proach for weight maintenance or reduction.
ance are characterized by an RQ greater than FQ (Fig 4). For
Some studies provide additional support for this concept by
positive energy balance
showing that a diet with a low-energy density causes spontaneous
RQ > FQ, and RQIFQ> 1.0 energy deficits (12- 16). These studies indicate a reduction in fat

This means that the fuel mix oxidized contains less fat than the
mixture supplied by the diet. As a consequence, there is a net
storage of dietary fat in adipose tissue. Another condition that ENERGY BALANCE
may explain an RQ > FQ is a fuel mix oxidized containing more (MJ/day)
7.5
carbohydrate than the mixture supplied by the diet. This leads to
a transient negative carbohydrate balance that is followed by a
compensatory increase in food intake. Therefore, a positive en- .
ergy (and lipid) balance is also expected to occur. 2 . I
Conditions of negative energy balance are characterized by an #{149}:k
RQ < FQ (Fig 4). For negative energy balance a

RQ < FQ, and RQIFQ < 1.0 2,5

This condition indicates that the amount oflipid oxidized exceeds .

the ingested amount, a condition resulting from endogenous fat
oxidation. 7.5 _______________________________

0.7 0.8 d’g i.o ii

RQ I FO
Dietary carbohydrates are involved in the control of
energy balance FIG 4. Relationship between the ratio of RQ to FQ (RQIFQ) and
energy balance in man. Each point represents the mean value for a subject
Regulation of food intake is of primary importance in achiev- measured over a 24-h period. For maintenance periods, RQ = 0.847
ing energy balance, because energy expenditure is little affected ± 0.010; for overfeeding periods, RQ = 0.902 ± 0.013; for underfeeding
by food intake. Spontaneous adjustments of food intake are more periods, RQ = 0.750 ± 0.011.

Downloaded from https://academic.oup.com/ajcn/article-abstract/59/3/682S/4732269

by guest
on 23 February 2018
 CARBOHYDRATES AS A SOURCE OF ENERGY 685S

intake may be a more effective strategy for weight loss than is abolic basis of experimental obesity. J Clin Endocrinol Metab
consumption of artificially sweetened foods. Advice aimed at the 1976;5:337-65.
reduction of habitual fat intake, without imposing limitation on 6. Sj#{246}str#{246}m
L. Adult human adipose tissue cellularity and metabolism.
Acta Med Scand Suppl 1972;544:1-52.
the quantity of low-fat food consumption, appears to be a prom-
7. Elwyn DH, Gump FE, Munro HN, et al. Changes in nitrogen balance
ising approach to avoid body weight regain in “postobese” in-
of depleted patients with increasing infusions of glucose. Am J Clin
dividuals after a hypoenergetic treatment. The choice of carbo- Nutr 1979;32:1597-61 1.
hydrates in the everyday diet is probably also important; starchy 8. Acheson IG, Flatt JP, J#{233}quier E. Glycogen synthesis versus lipogen-
foods that are digested slowly and produce low blood glucose esis after a 500 gram carbohydrate meal in man. Metabolism
and insulin responses (17) are of interest in appetite control of 1982;31:1234-40.
patients who must chronically restrict their energy intake (18). 9. Acheson KJ, SchuLz Y, Bessard T, Anantharaman K, Flatt JP,
In conclusion, dietary carbohydrates are of major importance J#{233}quier
E. Glycogen storage capacity and de novo lipogenesis during
in the regulation of energy balance. It is likely that the regulation massive carbohydrate overfeeding in man. Am J Chin Nutr
1988;48:240-7.
of food intake depends in part on the carbohydrate needs of the
10. Ravussin E, SchuLz Y, Acheson KJ, Dusmet M, Bourquin L, J#{233}quier
individuals (1 1). Because 1) carbohydrate intake promotes its
E. Short-term, mixed-diet overfeeding in man: no evidence for ‘ ‘lux-
own oxidation, 2) the net conversion of carbohydrate into fat is
uskonsumption.” Am J Physiol 1985;249:E470-7.
a minor pathway and, 3) the replenishment of glycogen stores 11. Tremblay A, Plourde G, Despres JP, Bouchard C. Impact of dietary
plays a role in the control of food intake, one can conclude that fat content and fat oxidation on energy intake in humans. Am J Clin
the present nutritional advice aimed at increasing the proportion Nutr 1989;49:799-805.
of carbohydrate energy while decreasing that of fat in the every- 12. Lissner L, Levitsky DA, Strupp Bi, Kalkwarf Hi, Roe DA. Dietary
day diet has strong scientific support in terms of the regulation fat and the regulation of energy intake in human subjects. Am J Cliii
of energy balance. U Nutr 1987;46:886-92.
13. Porikos KP, Booth G, Van Itallie TB. Effects of covert nutritive
dilution on the spontaneous food intake of obese individuals: a pilot
study. Am J Chin Nutr 1977;30:1638-44.
References 14. Porikos KP, Hesser MF, Van Itallie TB. Caloric regulation in nor-
mal-weight men maintained on a palatable diet of conventional
1. Flatt JP. Importance of nutrient balance in body weight regulation. foods. Physiol Behav 1982;28:293-300.
Diabetes Metab Rev 1988;4:571-81. 15. Glueck Ci, Hastings MM, Allen RD, et al. Sucrose polyester and
2. Ebiner JR, Acheson KJ, Doerner A, et al. Comparison of carbohy- covert caloric dilution. Am J Clin Nutr 1982;35:1352-8.
drate utilization in man using indirect calorimetry and mass spec- 16. Duncan KH, Bacon JA, Weinsier RL. The effects of high and low
trometry after an oral load of 100 g naturally-labelled (13C) glucose. energy density diets on satiety, energy intake, and eating time of
Br J Nutr 1979;41:419-29. obese and non-obese subjects. Am J Clin Nutr 1983;37:763-7.
3. Flatt JP, Ravussin E, Acheson KJ, J#{233}quier
E. Effects of dietary fat 17. W#{252}rsch P. Acheson K, Koellreuter B, J#{233}quierE. Metabolic effects
on postprandial substrate oxidation and on carbohydrate and fat bal- of instant bean and potato over 6 hours. Am J Clin Nutr
ances. J Clin Invest 1985;76:1019-24. 1988;48:1418-23.
4. Masoro El. Biochemical mechanisms related to the homeostatic reg- 18. Leathwood P. Pollet P. Effects of slow release carbohydrates in the
ulation of lipogenesis in animals. J Lipid Res 1962;3:149-64. form of bean flakes on the evolution of hunger and satiety in man.
5. Assimacopoulos-Jeannet F, Jeanrenaud B. The hormonal and met- Appetite 1988;10:1-1 1.

Downloaded from https://academic.oup.com/ajcn/article-abstract/59/3/682S/4732269

by guest
on 23 February 2018