Download The effect of a low-carbohydrate diet on performance, hormonal and

Eur J Appl Physiol (1997) 76: 128±133
Ó Springer-Verlag 1997
ORIGINAL ARTICLE
J. Langfort á R. Zarzeczny á W. Pilis á K. Nazar
H. Kaciuba-Us citko
The effect of a low-carbohydrate diet on performance, hormonal
and metabolic responses to a 30-s bout of supramaximal
exercise
Accepted: 31 January 1997
Abstract The aim of this study was to ®nd out whether a
low-carbohydrate diet (L-CHO) a€ects: (1) the capacity
for all-out anaerobic exercise, and (2) hormonal and
metabolic responses to this type of exercise. To this
purpose, eight healthy subjects underwent a 30-s bicycle
Wingate test preceded by either 3 days of a controlled
mixed diet (130 kJ/kg of body mass daily, 50% carbohydrate, 30% fat, 20% protein) or 3 days of an isoenergetic L-CHO diet (up to 5% carbohydrate, 50% fat,
45% protein) in a randomized order. Before and during
1 h after the exercise venous blood samples were taken
for measurement of blood lactate (LA), b-hydroxybutyrate (b-HB), glucose, adrenaline (A), noradrenaline
(NA) and insulin levels. Oxygen consumption (V_ O2 ) was
also determined. It was found that the L-CHO diet diminished the mean power output during the 30-s exercise
bout [533 (7) W vs 581 (7) W, P < 0.05] without changing the maximal power attained during the ®rst or
second 5-s interval of the exercise. In comparison with
the data obtained after the consumption of a mixed diet,
after the consumption of a L-CHO diet resting plasma
concentrations of b-HB [2.38 (0.18) vs 0.23
(0.01) mmol á l)1, P < 0.001] and NA [4.81 (0.68) vs 2.2
(0.31) nmol á l)1, P < 0.05] were higher, while glucose
[4.6 (0.1) vs 5.7 (0.2) mmol á l)1, P < 0.05] and insulin
concentrations [11.9 (0.9) vs 21.8 (1.8) mU á l)1] were
lower. The 1-h post-exercise excess of V_ O2 [9.1 (0.25) vs
10.6 (0.25) l, P < 0.05], and blood LA measured 3 min
after the exercise [9.5 (0.4) vs 10.6 (0.5) mmol á l)1,
P < 0.05] were lower following the L-CHO treatment,
whilst plasma NA and A concentrations reached higher
values [2.24 (0.40) vs 1.21 (0.13) nmol á l)1 and 14.30
(1.41) vs 8.20 (1.31) nmol á l)1, P < 0.01, respectively].
In subjects on the L-CHO diet, the plasma b-HB con-
J. Langfort á K. Nazar á H. Kaciuba-Us citko (&)
Department of Applied Physiology, Medical Research Centre,
Polish Academy of Sciences, Warsaw, Poland
R. Zarzeczny á W. Pilis
Department of Physiology, University of Czstochowa, Poland
centration decreased quickly after exercise, attaining
30% of the pre-exercise value within 60 min, while insulin and glucose levels were elevated. The main conclusions of this study are: (1) a L-CHO diet is detrimental to
anaerobic work capacity, possibly because of a reduced
muscle glycogen store and decreased rate of glycolysis; (2)
reduced carbohydrate intake for 3 days enhances activity
of the sympathoadrenal system at rest and after exercise.
Key words Wingate test á Diet á Ketoacids á Lactate á
Catecholamines
Introduction
It is known that physical performance and the pattern of
substrate utilization during exercise may be altered by a
change of diet. Studies on animals, including human
subjects concerning the in¯uence of a low-carbohydrate
(L-CHO), fat-rich diet have documented reduced carbohydrate stores and enhanced utilization of fat by
working muscles together with a decreased contribution
of muscle glycogen to the energy yield (Holloszy 1990).
This was accompanied by an elevation of pre- and postexercise levels of plasma adrenaline (A), noradrenaline
(NA) and cortisol, and decreased insulin (IRI) concentrations (Langfort et al. 1996). Most of the studies
showed deleterious e€ects of a L-CHO diet on performance during endurance or short-term aerobic e€orts
(Christensen and Hansen 1939; Galbo et al. 1979; Zinker
et al. 1990; Helge et al. 1996). However, some authors
failed to demonstrate such e€ects. Thus, Phinney et al.
(1980) reported a preserved capacity for moderate exercise in obese subjects after 6 weeks on a low-energy,
ketogenic diet. In a subsequent study from the same
laboratory (Phinney et al. 1983) it was shown that in
elite cyclists time to exhaustion during exercise at 60%
of maximum oxygen consumption (V_ O2 max ) was not
reduced after 4 weeks of an isoenergetic, ketogenic diet,
in spite of markedly diminished (by 50%) muscle
glycogen content before exercise.
129
Very little is known about the in¯uence of diet on
ability to perform a brief all-out supramaximal exercise.
Thus, the present study was undertaken to ®nd out
whether a 3-day, low-carbohydrate, ketogenic diet affects performance during a 30-s Wingate test. This test
allows the estimation of maximal power output (Pmax)
and anaerobic work capacity [i.e., the mean power
(Pmean) or the total work performed during the 30 s]. A
number of authors have shown that during 30-s,
sprinting, creatine phosphate (CP) degradation, anaerobic glycolysis and aerobic metabolism can provide
55%, 25% and 20%, respectively, of the ATP required
for muscle contractions (Serresse et al. 1988; Smith and
Hill 1991; Withers et al. 1991; Trump et al. 1996). In
addition to the performance indices measured in the
present study, blood lactate (LA), b-hydroxybutyrate
(b-HB), glucose (BG), catecholamine and IRI concentrations were measured before and after exercise to
elucidate the mechanisms linking dietary modi®cations
to subsequent exercise performance.
Methods
Subjects
Eight healthy men volunteered to take part in this study, which was
approved by the Ethical Committee at the Medical Research
Centre of Polish Academy of Sciences in Warsaw. Mean values
(with standard deviations) of the subjects age, height, body mass
and V_ O2 max were: 22 (0.5) years, 175.9 (6.1) cm, 75.8 (5.3) kg and
3.87 (0.38) l á min)1, respectively. Their body fat content did not
exceed 15.5% of body mass, as calculated from skinfold measurements (Durnin and Womersley 1974). The subjects were not engaged in any competitive sport activity.
Experimental procedure
The subjects performed, in a randomized order, two all-out 30-s
Wingate tests (WT; Bar-Or 1980) on a cycle ergometer (MonarkCrescent, Varberg, Sweden) preceded by either 3 days on a normal
(controlled) mixed (M) diet (50% carbohydrate, 30% fat and 20%
protein), or 3 days on a ketogenic diet containing less than 5%
carbohydrate, 50% fat and 45% protein. Both of the diets had the
same energy content (130 kJ/kg body mass, daily). All food was
provided for the subjects in the students' canteen. During the dietary treatment the subjects refrained from strenuous exercise but
performed their habitual activities. No ca€eine, alcohol, or tobacco
was permitted during the 48 h before and during the trial.
On the day of the exercise testing the subjects reported to the
Laboratory after an overnight fast. Half an hour before the exercise
they had a catheter inserted into the antecubital vein for blood
sampling. The catheter was rinsed frequently with 0.9% saline. The
exercise, to which was added a resistance 0.75 Ns á m)1, started
3 min after a 5-min warm-up at an intensity 75±125 W with three
interspersed sprints of 5±6 s. The warm-up was identical in the two
trials. During the WT the frequency of wheel revolutions was
recorded using magnets placed on the ¯ywheel and an electronic
counter. Power output was calculated online every 5 s during the
test by a computer. The Pmax, usually during the second interval,
and the Pmean during the whole 30 s were analysed.
Pulmonary ventilation, oxygen uptake (V_ O2 ) and carbon dioxide output were determined before exercise (for 15 min), and
then during the 1st, 3rd, 15th and 60th min after exercise using a
Beckman Metabolic Measurement Cart. Based on these measurements the 1-h excess post-exercise V_ O2 (EPOC) was calculated.
Venous blood samples, for determinations of LA and BG,
plasma b-HB and IRI concentrations, were withdrawn before the
exercise and then at 3, 15, 30 and 60 min following the cessation of
exercise. Plasma levels of catecholamines were measured before the
e€ort and at 3, 15 and 30 min after its termination.
Analytical methods
Blood samples, except those used for catecholamine determination,
were taken directly from the catheter to heparinized tubes. The
whole-blood aliquots that were to be used for LA and b-HB
measurement were deproteinized immediately with perchloric acid
and centrifuged at 2,000 g. The supernatant was stored at 5°C and
analysed on either the same or the next day. The additional wholeblood aliquots that were to be used for BG determination were
deproteinized with uranyl acetate (URAC, Boehringer, Manheim,
Germany) and centrifuged at 2,000 g. The supernatant was kept at
5°C until it was analyzed on the same day. The remaining heparinized blood was taken for plasma IRI determination. It was
centrifuged at 4°C at 2,000 g and the plasma was kept frozen at
)70°C until it was analysed. Blood samples that were to be used for
catecholamine determination were taken to ice-chilled tubes containing an anticoagulant and antioxidant (ethyleneglycol-bisCoxonitrilo tetra acetate and glutathione). The plasma was separated
by refrigerated centrifugation, and samples were subsequently
stored at )70°C until they were assayed. Plasma b-HB was measured enzymatically (Williamson et al. 1962).Blood LA and BG
concentrations were determined enzymatically using commercial
kits (Boehringer, Mannheim, Germany). Plasma IRI was determined by radioimmunoassay with the sets produced by the Institute of Atomic energy, SÂwierk, Poland. The plasma concentrations
of free A and NA were measured radioenzymatically, according to
the method of DaPrada and Zurcher (1979), using reagent sets
(REA KIT, Chemapol, Czech Republic).
Statistics
A statistical evaluation of the mean di€erences between the two
diets was made using one-way analyses of variance followed by
Newman-Keul's test or Student's t-test for paired observations.
P < 0.05 was accepted as the level of statistical signi®cance. All
results are presented as the mean (SE), unless otherwise stated.
Results
The Pmean attained during the WT after the L-CHO diet
was 553 (21) W and was signi®cantly lower than that
attained after the M diet [581 (18) W, P < 0.05]. there
was no di€erence in Pmax between the two trials (Fig. 1).
The EPOC, measured during a 1-h period (Fig. 1),
amounted to 10.62 (0.71) l following the M diet and to
9.11 (0.72) l after the L-CHO diet (P < 0.05).
The L-CHO diet caused a considerable increase in the
plasma b-HB concentration. During the 1-h post-exercise recovery the plasma b-HB levels decreased progressively, but even at the 60th min of this period they
were signi®cantly higher than the values observed in the
same subjects after the M diet (Fig. 2).
The BG concentration was signi®cantly lower after
the L-CHO than after the M diet at rest, whereas during
the recovery period the L-CHO diet resulted in higher
BG values compared with those obtained following the
M diet (P < 0.05, Fig. 2). The pre-exercise blood LA
concentration was similar in the two trials, but at the 3rd
130
and 15th min of the recovery period it was lower after
the L-CHO than after the M diet (P < 0.05 and
P < 0.01, respectively). Prior to the WT plasma NA
concentration was enhanced after the L-CHO diet
(P < 0.05), and there was a tendency towards an increase in the plasma A level compared with the M diet.
During 30 min of the recovery period both plasma A
and NA concentrations were signi®cantly higher following the L-CHO compared with the M diet (Fig. 3).
Plasma IRI concentration at rest was reduced after the
L-CHO diet (P < 0.001) and was signi®cantly lower
than after the M-diet at the 3rd (P < 0.05), and the
60th min of the recovery period (Fig. 3).
Fig. 1 Maximal power output (PMAX), mean power output (PMEAN)
and 1-h post-exercise oxygen consumption (EPOC ) following 3 days
on the low-carbohydrate (L-CHO; black bars) and normal mixed
(M; white bars) diets. Values are means (SE; n = 8). Asterisks indicate
a signi®cant di€erence between the two trials (*P < 0.05)
Discussion
The most important ®nding of this study is that the
L-CHO diet reduced the Pmean attained during 30-s bout
of all-out exercise without changing the Pmax. This was
accompanied by a lower post-exercise blood LA concentration that found after the M diet. The latter e€ect
suggests that the more rapid power decline that occurred
after the L-CHO diet was a result of a limitation of the
rate of glycolysis. However, the possibility cannot be
excluded that the post-exercise blood LA concentration
observed after this diet was lower because less work was
done within the 30 s of exercise compared with the M
diet.
As mentioned previously, anaerobic glycolysis represents an important supply of ATP during a 30-s bout
of supramaximal exercise. A maximal rate of anaerobic
glycolysis is attained after 15 s of this exercise after
which the rate decreases (Yamamoto and Kenehisa
1995). The rate of glycolysis depends upon a number of
local and systemic factors. Among them the most important is the substrate supply via glycogenolysis. Occurrence of a high level of sympathetic activity after the
L-CHO diet, as evidenced by the plasma catecholamine
concentration, would be expected to increase the rate of
glycogenolysis in muscle. However, this e€ect might not
be apparent because of the reduced muscle glycogen
content and the inhibitory action of increased plasma
free fatty acid (FFA) concentration on the rate of both
glycogenolysis and glycolysis under this dietary condition.
In human subjects alterations in dietary carbohydrate
intake do not have a great e€ect on muscle glycogen
content. Maughan and Williams (1982) and Knapik et al.
(1988) did not ®nd signi®cant decreases in muscle glycogen after 3 days of fasting in subjects whose physical
activity was considerably restricted. On the other hand,
b
Fig. 2 Blood glucose, lactate and plasma b-hydroxybutyrate concentrations before and after Wingate test performed following 3 days on
the L-CHO (black bars) and M (white bars) diets. Values are means
(SE; n = 8). Asterisks indicate a signi®cant di€erence between the two
trials (*P < 0.05, **P < 0.01, ***P < 0.001)
131
Fig. 3 Plasma adrenaline, noradrenaline and insulin concentrations
before and after a Wingate test performed following 3 days on the
L-CHO (black bars) and M (white bars) diets. Values are means (SE;
n = 8). Asterisks indicate a signi®cant di€erence between the two
trials (*P < 0.05, **P < 0.01)
Hultman (1967) demonstrated that when subjects consumed a L-CHO diet (< 5%) for 1 week and performed
their usual activities (but refrained from strenuous exercise) muscle glycogen concentration declined by 25±
50%. A similar reduction in muscle glycogen was found
during fasting for 2±5 days (Hultman 1967). Since in the
present study the physical activity of the subjects was not
restricted to a great extent it cannot be excluded that
their muscle glycogen content might have been reduced.
Studies on the perfused rat hindlimb have demonstrated a direct relationship between pre-contraction
muscle glycogen availability and the rate of glycogenolysis during electrical simulation (Richter and Galbo
1986; Hespel and Richter 1992). Likewise, the muscle
glycogen level is an important regulator of phosphorylase activity in skeletal muscle. A reduction of glycogen
content in the subjects muscles during 3 days of a
L-CHO diet may, therefore, be a factor decreasing the
rate of glycogenolysis and, subsequently, glycolysis.
However, studies in humans produced con¯icting results
concerning the in¯uence of muscle glycogen availability
on the rate of glycogenolysis. It was proved that the rate
of this process after glycogen depletion is diminished
during submaximal exercise (Gollnick et al. 1981; Hargreaves et al. 1995), but not during short-term electrical
stimulation (Ren et al. 1990).
Limitation of the rate of glycolysis after a L-CHO
diet might be also attributable to citrate-mediated inhibition of phosphofructokinase (PFK) activity due to the
elevated FFA availability for working muscles, according to the classic concept of the glucose-fatty acid cycle
proposed by Randle et al. (1963). An increase of circulating FFA by 40% after 3 days of a L-CHO diet has
been reported in our previous study (Langfort et al.
1996). An inhibition of PFK could also be produced by
ketoacids, which may increase considerably the mitochondrial acetyl-coenzyme A concentration and, subsequently, the cytoplasmic citrate level in muscle (Berger
et al. 1976; Newsholme 1976; Kreider and Thompson
1986). The current data showed an approximately tenfold increase in plasma b-HB after 3 days of a L-CHO
diet. Therefore, the inhibition of glycolysis by FFA and
ketoacid oxidation seems likely, at least at rest, before
exercise. It is not known whether the inhibition of PFK
activity persisted during the exercise. It should be noted
that the glucose-fatty acid cycle concept is based on
experiments using the rat heart and diaphragm muscles
and its operation in exercising skeletal muscles is therefore, questionable (Putman et al. 1995).
A more rapid decrease in muscle pH during exercise
after a L-CHO diet may be considered to be an inhibitor
of glycolysis as well as a performance-limiting factor
through changes in the sarcolemmal potential, excitation-contraction coupling and inhibition of cross-bridge
formation (MacLaren et al. 1989). Greenha€ et al.
(1987, 1988) postulated that a reduced duration of highintensity exercise after a high-fat diet might be related to
the occurrence of a mild resting metabolic acidaemia
and decreased bu€ering capacity. Accordingly, our
previous study showed that a 3-day L-CHO diet lowered
the blood pH measured after graded exercise performed
until maximum, as well as the initial and post-exercise
blood base excess and standard bicarbonate levels
(Langfort et al. 1996). However, Larson et al. (1994) did
not ®nd any di€erences between resting and post-exercise muscle pH, as measured by magnetic resonance
spectroscopy (MRS), in subjects exercising after 5 days
of high-carbohydrate and L-CHO diets. According to
these authors the most important mechanism performance-limiting during high-intensity exercise of 5 min
duration after a L-CHO (high fat) diet is a lowering of
the muscle CP content and an increase in the rate of its
132
early depletion. A lowering e€ect of glycogen depletion
on muscle CP was previously reported by Bertocci et al.
(1992) using MRS, and by Hultman et al. (1967) in their
classic muscle biopsy study.
The decrease in muscle CP content may be deleterious for performance during supramaximal exercise since
degradation of this compound covers a substantial part
of the energy requirement during the e€ort, particularly
in its early phase (Bogdanis et al. 1994). It seems unlikely, however, that the diet applied in the present study
caused any large decrement in the initial CP content
since the Pmax attained during the ®rst 10 s of the
Wingate test was not a€ected signi®cantly.
We assume that the inability to maintain the high
power output after 3 days on a L-CHO is attributable to
a combination of several factors such as a reduction in
muscle glycogen content, inhibition of glycolytic enzyme
activities and accelerated CP degradation. One can also
speculate that a L-CHO intake may a€ect the mechanisms of central fatigue associated with brain serotoninergic activity. It was found that carbohydrate
supplementation during endurance exercise decreased
markedly the free tryptophan (f-Trp) concentration in
blood and its ratio to the branched-chain amino acids,
which can diminish the rate of serotonin synthesis and
delay fatigue (Davis 1996). Since the plasma f-Trp concentration is directly related to FFAs, controlling Trp
binding to albumin it seems possible that the L-CHO
diet may have begun to promote serotonin synthesis
before the start of the exercise. However, in the present
study it was not possible to distinguish between the
central and peripheral fatigue mechanisms. In addition it
is not known whether the ``serotoninergic'' mechanism
of fatigue plays any important role during short-term
supramaximal exercise.
The present data showed signi®cant di€erences in
post-exercise metabolism between the two dietary conditions. The smaller 1-h EPOC that occurred after the
L-CHO diet can be attributed to the reduced amount of
work performed during the e€ort and the lower postexercise blood LA level that occurred after the L-CHO
compared with the M diet.
During the recovery period the BG concentration,
which was signi®cantly lower before exercise on the
L-CHO diet than on the M diet, attained higher values
after the L-CHO diet than after the M diet. This may be
due to greater contribution of fat-derived substrates,
particularly ketoacids, than glucose to the post-exercise
metabolism following the L-CHO diet. On the other
hand, the post-exercise elevation in BG under this condition may be caused by increased glucose release from
the liver stimulated by hormonal changes associated
with a L-CHO intake. These changes involve increased
catecholamine release and lowered IRI secretion. In our
previous investigation (Langfort et al. 1996), in addition
to increased plasma catecholamine and decreased circulating IRI levels, elevated plasma cortisol was reported following the same dietary procedure.
The plasma catecholamine levels were higher after
the L-CHO than after the M diet not only before the
exercise, but also after its cessation. Similar results have
been reported previously by Jansson et al. (1982), who
compared plasma levels of catecholamines after submaximal exercise preceded by carbohydrate-poor and
carbohydrate-rich diets. It is, however, intriguing that a
L-CHO intake modi®es the sympathoadrenal system
response to supramaximal exercise lasting only 30 s.
According to common opinion the early activation of
this system is related to the so-called ``central command'', that is, stimulation of the sympathetic brain
centres by irradiation of impulses from the motor cortex
(Kjaer 1989).
In summary, the present data show that 3 days of a
diet in which only 5% of the energy content comes from
carbohydrates diminishes anaerobic work capacity, as
re¯ected by the occurrence of a reduced Pmean during a
30-s bout of all-out cycling exercise and a lowered postexercise blood LA concentration. There was no signi®cant di€erence in the Pmax determined during the same
exercise test. The L-CHO diet was associated with enhanced resting plasma levels of b-HB and catecholamines as well as decreased concentrations of glucose
and IRI as compared to those attained after an isoenergetic, normal diet (M). The di€erence in plasma catecholamines between the two dietary conditions was even
more pronounced after exercise, while the di€erences in
plasma b-HB and IRI were reduced. Post-exercise BG
concentrations were even higher following the L-CHO
than after the M diet, probably as a result of the high
catecholamine levels.
Acknowledgements This work supported by the State Committee
for Scienti®c Research, grant No. 4 S404 028 07. Dr. R. Zarzeczny
was supported by the Foundation for Polish Science. The authors
are grateful to Dr. E. Titow-Stupnicka, Mrs. J. WeE_zowska and
Mrs. B. Kurek for plasma catecholamine and insulin determinations.
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