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Effect of initial muscle glycogen levels on protein catabolism during exercise

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Serum urea increases with exercise duration suggest prolonged exercise may be analogous to starvation where protein catabolism is known to occur. The purpose of this investigation was to alter muscle glycogen levels and to study the effect on protein catabolism. Six subjects (27-30 yr) pedaled a cycle ergometer for 1 h at 61% VO2max (mean VO2 = 2.33 +/- 0.7 1 . min-1) 1) after CHO loading (CHOL) and 2) after CHO depletion (CHOD). The following urea N measures were made: pre-exercise serum and urine, exercise serum and sweat (15-min serial samples), and serum and urine during 240 recovery min. Results demonstrated that 1) exercise serum urea N increased in CHOD attaining significance (P less than 0.01) at 60 min; 2) serum urea N increases continued into recovery at all measurement points of CHOD (P less than 0.01) and at 240 min of CHOL (P less than 0.05); 3) sweat urea N increased 154.2-fold (CHOD) and 65.6-fold (CHOL) (P less than 0.05). Calculations indicate that CHOD sweat urea N excretion was equivalent to a protein breakdown of 13.7 g . h-1 or 10.4% of the total caloric cost. It was concluded that protein is utilized during exercise to a greater extent than is generally assumed and that under certain conditions protein carbon may contribute significantly to exercise caloric cost.
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Effect of initial muscle glycogen levels on
protein catabolism during exercise
P, W. R. LEMON AND J. P. MULLIN
Biodynamics Laboratory, University
of
Wisconsin, Madison, Wisconsin 53706
LEMON,
P.
W. R., AND J, P. MULLIN. Effect of initial musck
glycogen levels on protein catabolism during exercise.
J. Appl.
Physiol.: Respirat. Environ. Exercise Physiol.
48(4): 624-629,
1980.-Serum urea increases l;Yith exercise duration suggest
prolonged exercise may be analogous to starvation where pro-
tein catabolism is known to occur. The purpose of this investi-
gation was to alter muscle glycogen levels and to study the
effect on protein catabolism. Six subjects (27-30 yr) pedaled a
cycle ergometer for
1
h at 61% v02 max (mean 902 = 2.33 & 0.7
Lmin?) I) after CHO loading (CHO,) and 2) after CHO
depletion (CHOD). The following urea N measures were made:
pre-exercise serum and urine, exercise serum and sweat (15min
serial samples), and serum and urine during 240 recovery min.
Results demonstrated that 1) exercise serum urea N increased
in CHOn attaining significance (P <
0.01)
at 60 min; 2) serum
urea N increases continued into recovery at all measurement
points of CHOD (P <
0.01)
and at 240 min of CHOI, (P < 0.05);
3) sweat urea N increased X&&fold (CHOKE) and 65.6-fold
(CHUL) (P < 0.05). Calculations indicate that CHOr:, sweat urea
N excretion was equivalent to a protein breakdown of 13.7 g.
h-’ or 10.4% of th e o a ca oric cost. It was concluded that t t 1 1
protein is utilized during exercise to a greater extent than is
generally assumed and that under certain conditions protein
carbon may contribute significantly to exercise caloric cost.
serum; urine; sweat; urea nitrogen; prolonged exercise; substrate
utilization; carbohydrate loading; branched chain amir,o acids;
glucose-alanine cycle; starvation
THE STUDY OF SUBSTRATE UTILIZATION
during exercise
has been
the
topic of a great many publications over the
years dating back
to at
least the mid-1800s (34). The bulk
of this literature has led to the general consensus that, in
the isocaloric state, glycogen and free fatty acids (FFA)
constitute the major energy sources, at least during ex-
ercise of short duration, A number of authors, however,
have provided evidence in support of an active protein
utilization particularly during long-duration exercise (4,
12-14, 18, 27-29, 32, 33, 36, 37). Interest in this area of
study was renewed by the observation of a large increased
output (proportional to work intensity) of the amino acid
alanine from working skeletal muscle (9). Because no
evidence for
a
specific alanine-rich protein within skeletal
muscle has been found (21), it was suggested that amino
acids may be transaminated within skeletal muscle re-
sulting in the formation of alanine from glucose-derived
pyruvate carbon, i.e., de novo alanine synthesis (9, 10).
The branched chain amino acid-glucose alanine. cycle (9,
10) has become perhaps the most prevalent
theory to
explain the observed increased protein utilization during
prolonged exercise.
Studies demonstrating an intramuscular enzyme efflux
following exercise (14,18,28,33,37) suggest that a second
possibility may exist to account for the increased protein
involvement, It has been demonstrated in an isolated
preparation that this efflux occurs only after a muscle’s
work capacity is markedly reduced by fatigue (33). More-
over, it has been suggested that intracellular protein
retention may be directly related to the concentration of
available ATP (37). The exact mechanism is uncertain
but it appears that ATP may be involved in the mainte-
nance
of the
cellular membrane,
since ATP is known to
be necessary in the synthesis of phospholipids, an impor-
tant
component of cellular membrane structure (22).
Perhaps when the ability
to
synthesize ATP decreases,
due
to
muscle glycogen depletion, cellular membrane
structure
is adversely affected, resulting in intramuscular
enzyme efflux. If these effluxed enzymes are degraded
into
their component amino acids and subsequently
deaminated, the resulting C skeletons could be oxidized.
This mechanism, if valid, would be of relatively minor
importance however, due to the magnitude of the total
enzyme C available.
Finally, as a third possibility, the protein involvement
may be related to the supply of available substrate.
Haralambie and Berg (13) have demonstrated, using
their own data and that of several others, that serum
urea increased nearly linearly with exercise duration
beginning at -70 min. Moreover, they also observed a
fall in serum amino nitrogen beginning at the same time.
It is indeed interesting, as they point out, that these two
observations occur simultaneously and at a time when
liver glycogen is considerably lowered (16) and muscle
glycogen is severely depleted (3, 6). It may be that, in
terms of substrate supply to working skeletal muscle, the
situation during prolonged exercise is analogous to short-
term starvation where protein catabolism is known to
occur (31).
It follows, therefore, that if protein catabolism occurs
during and/or after prolonged exercise, it may be related
to glycogen depletion (and the subsequent decreasing
ability
to
synthesize ATP) and not exercise duration per
se.
The purpose of the present investigation was to alter
initial muscle glycogen levels and to study the possibility
that the utilization of protein is a glycogen-related phe-
nomenon,
624 o16T-7567/80/0000-0000$01.25
Copyright
0 1980 the American
Physiological Society
MUSCLE GLYCOGEN AND PROTEIN CATABOLISM
625
METHODS
Six healthy physically active male subjects (ages 27-
30) worked for 60 min on an electrically braked bicycle
ergometer (N. V.. Godart, Lanooy type) at 61% of their
predetermined VOW maxs Physical characteristics are
shown in Table 1. All experimental sessions took place at
1O:OO
A.M+
following an overnight fast. Laboratory con-
ditions for temperature and relative humidity were main-
tained at Zl-25°C and 50-58%, respectively. Two hours
before the beginning of the experiment, the subjects
voided and a ZO-gauge 1.25”in. Teflon catheter (Deseret
Pharmaceutical, Sandy, UT) was inserted into a periph-
eral vein in the antecubital area. Immediately before the
subjects began exercising, resting samples of blood and
TABLE
1. Physical characteristics
Subj
LG
30
FINAL “20 ASSUMED RESI? EXERCISE KCAL \
A RATE = BOW WT -BUtP WT +lNTAKE -Hz0 LOSS* - l l L*KG-I
CL*HR-’ > CKGI CKGI C KC) CKG) 7700 KCAL* KG-’
w kg
lmmin-’
%
VO 2 max
61.7 3.50
61.3 3.25
70.5 3,76
72.7 3.88
61.4 3.40
88-5 5.87
53.4 ; 1,000
55.4 I 900
66.3 ! 1,500
60
65
56
60
62
60
69.4 3.94 I 56.3 1,016 60.5
k10.6 -t-o.94 1 k5.1 t240 k2.9
Exptl
urine were obtained. Serial exercise blood and sweat
samples were collected at 15min intervals throughout
the work bout. Recovery measures were as follows: blood,
15, 60, and 240 min; urine, immediately after (if possible)
60 and 240 min. The blood samples were allowed to
coagulate and then centrifuged at 2,500 g. Sweat was
collected in test tubes from the subjects’ backs and
filtered to remove dirt and dermal debris. All three fluids
(sweat, serum, and urine) were frozen for later analysis
of urea N by the diacetyl monoxime reaction (2) and read
calorimetrically dn a Bausch and Lomb Spectronic 20 at
a wavelength of 365 nm. A dilution factor of 1:20 was
used for sweat and L:400 for urine. During the experi-
mental sessions, the subjects were allowed free access to
water, Sweat rate and sweat urea N excretion were
calculated as outlined in Fig. 1.
Each subject completed the work bout on two separate
occasions: 1) after carbohydrate (CHO) loading and 2)
after CHO depletion. More specifically, the above two
conditions were obtained by the following procedures.
CHO-loaded condition (CHOL). A 60-min exercise
bout on the bicycle ergometer at 70-75% vop max was
followed by 3 days of high CHO diet (2,000-2,500 kcal
CHO) (30).
CHO-depleted condition (CHOD). In the afternoon of
the day before the experimental session, each subject
completed a 60-min exercise bout on the bicycle ergom-
eter at 70-75%
VO2
maxt followed by an evening meal that
FIG. I. Sweat calculations.
Mitchell et al. (24). *From
SWEAT UREA 15’ CONC. 30’ CONC. 45’ CONC. 60’ CONC.
8 N EXCRETION = CMG*L-‘1 + CMG*L-5 +CMG*L-I) $-CMG*L-5 *SWEAT RATE
CMG-“R-j 1 4 CLMR-‘1
L
EXERCISE-+-RECOVERY 5
T
FIG. 2. Serum urea N vs. time.
8 I I 1 1 I I
0 15 30 45 60 15R 60R 240R
TIME CMINUTES)
626
Pm W. R. LEMON AND J. P, MULLIN
consisted of essentially zero CHO. data indicate dramatic increases in sweat urea N of 65.6-
Repeated measures three-factor ANOVA (subject
x
and 154.2-fold in the CHOL and CHOn, respectively. The
treatment
x
time) were performed on serum and urine sweat urea N of the CHOn was significantly greater than
data, while the sweat results were subjected to a repeated the CHOL (P <
0.05).
measures two-factor ANOVA (subject x treatment) (20).
Where indicated, Tukey post hoc tests were employed to
determine the location of significance (20) l
DISCUSSION
A recent study by Gontzea et al. (12) may provide
some insight with regard to the similarities between
prolonged exercise and starvation, These authors re-
ported the nitrogen balance of 12 subjects (ages 21-29
yr) on a standard diet (1 g protein g kg body wt-l l day-‘)
for
5
wk. During the first 2 wk, all subjects were sedentary
and 10 of 12 were in positive nitrogen balance. For the
remaining 3 wk of the experiment, all subjects completed
120 min of bicycle exercise each day with a mean caloric
cost of 1,192 kcale day? In spite of the fact that their
caloric intake was 10% higher than their expenditure, the
nitrogen balance became negative in all
12
subjects on
the 1st day of exercise. This nitrogen loss continued to
increase, reaching a peak at day 3-4 and then gradually
began to decrease, reaching close to zero nitrogen balance
by U-12 days of exercise. This observed pattern of initial
increased protein catabolism followed by protein conser-
vation is similar in time course to the events during
starvation
(31).
RESULTS
Serum urea N results (means t SE) are presented in
Fig. 2. At rest there was no significant difference (P >
0.05) between the two conditions. During exercise in the
CHOp, serum urea N increased
7.0, 8.6, 10.7,
and 16.3%
(P <
0.01)
at
15, 30, 45,
and
60
min, respectively. During
recovery, serum urea N continued to increase at all
measurement times attaining its greatest increase (31%)
at 240 min (P < 0.01). This same trend during exercise
was not apparent in the CHOL as little or no change
occurred until recovery, where increases of 6.5% at
60
min and 10.9% (P < 0.05) at
240
min were observed.
Urine urea N excretion results (means t SE) are
presented in Fig. 3. At rest there was a 59.7% increase (P
< 0.05) in the CHOn when compared to the CHOL.
Following the experimental work bout there was a de-
crease of
18.3%
in the CHOL and 31.3% in the CHOn. The
values observed at 60 and 240 min of recovery were still
.
reduced below res ting values for both conditi .ons.
Sweat urea N excretion resu .lts (means $- SE ) are
presented in Fig. 4. When compared to rest values, these
I IO01 1
i
EXERCISE ---+- RECOVERY
1000 -
I SEM i
-
CHOL
C -
500 -
Y ;
400 -
I
d
60 60R 240R
TIME CMINUTESI
FIG. 3. Urine urea
N
vs. time.
Because it was not possible to obtain
a postexercise urine sample from 2 subjects in CHOD, A, A represent
mean of 60-min exercise and 60-min recovery urine samples for all
subjects in CHQl and CHOL, respectively. *n = 4.
The present experiment was designed to create a sit-
uation where initial muscle glycogen levels were suffi-
ciently different to demonstrate the relationship between
protein catabolism and muscle glycogen, if one exists. It
is felt that this objective was obtained, since the proce-
dure employed to increase muscle glycogen levels has
become well established (1) and has pr&iously been
shown to approach a doubling of rest glycogen levels (30) ;
while the procedure for depletion has resulted in a de-
crease to one-half normal rest levels (II). In addition, the
observation of 1.36-2.27 kg weight gain in the CHOL is
further evidence that the CHO loading was successful.
Recently, MacDougall et al. (23) have demonstrated that
muscle glycogen levels, following supramaximal intermit-
tent exercise to exhaustion, may return to approximately
67 and 102% of their original levels after
12
and 24 h,
respectively. It might be suggested, therefore, since the
experimental sessions in the current study occurred 15-
19 h after the depletion session, that it is possible the
muscle glycogen levels of the CHOD were in fact ap-
proaching
pleted the normal rest
experimental levels when
session. It is the
felt ?
subjects com-
however, that
the continuous protocol for depletion employed in this
study more closely resembles the studies reported by
Piehl (25) or Bergstrom et al. (3) where muscle glycogen
levels remained partially depleted until approximately
46
h (for discussion, see Ref. 23).
The increase (P < 0.01) in serum urea N observed over
time in the CHOD is interesting and suggests that during
exercise and recovery, urea N production was increased
and/or excretion decreased. The failure of the exercise
urinary urea N decreases to reach statistical significance
(0.16 > P > 0.05) indicates urinary excretion was un-
changed. A large intersubject variability may, however,
account for this finding. It appears that urinary data
must be considered with caution, since voluntary mictu-
MUSCLE GLYCOGEN AND PROTEIN CATABOLISM
627
rition may be unreliable. Catheters would, of course, be
preferable. State of hydration during both conditions of
the experiment was not grossly different, since water
intake (CHOn 765 vs. CHOL 708 ml), urine volume
(CHOo 346 vs. CHOL 361 ml), and sweat rate (CHOn
1,492 vs. CHOL 1,490 ml) were similar (P > 0.05) (Table
2). If the conservative assumption is made that the
observed urinary decreases are real, it is still difficult to
explain the increased serum urea N in the CHOn in terms
of a decreased excretion because, if this were so, one
would expect to observe a serum increase under both
conditions. The fact that the increase occurred only in
the CHOo suggests that initial muscle glycogen levels
may be a regulating factor in exercise protein catabolism.
observation of the highest serum values under both con-
ditions in recovery after sweating has stopped. The ear-
lier observation of no change in serum urea until -70
min duration (4, 13) may, therefore, be related not only
to initial muscle glycogen levels but also to the urea N
excretory capacity of the sweat. One might expect, there-
fore, that in individuals with reduced sweating capability
serum urea N values would be further elevated.
Figure 4 demonstrates the dramatic importance of
sweat urea N excretion during exercise. It appears that
the sweat mechanism is very effective at both preventing
a serum rise under the CHOL and attenuating the rise
under the CHOn, at least until the 60-min exercise sample
when muscle glycogen is lowest and, therefore, presum-
ably protein catabolism is greatest. The importance of
the sweat mechanism is further demonstrated by the
The procedure of sampling sweat urea N was consid-
ered valid inasmuch as sweat samples taken from the
back have been shown to be representative of total body
sweat urea N concentration (5). The possibility exists,
however, that the present method of collection may have
resulted in an overestimation of sweat urea N concentra-
tion due to evaporation. Although this could affect the
measurement of absolute sweat urea N excretion, it does
not alter the relative comparison between CHOL and
CHOn. Any error introduced cannot be precisely deter-
mined from the present data, however, calculations in-
dicate that it could amount to -11%. It should be pointed
out, however, that other sweat collection methods could
have resulted in errors also. The arm bag method would
be of questionable value because urea N concentration
from this procedure is not representative of total body
sweat (5). In addition, due to the high sweat rates of the
present subjects, the gauze square method (5) may have
been invalid also for the following reason. If the gauze
squares became supersaturated early in the 60-min effort,
localized sweating would decrease (hidromeiosis). Be-
cause sweat urea concentration is largely a function of
sweat rate (4, 5), unless the gauze squares were changed
frequently, this method could produce an overestimation
of sweat urea N excretion.
TABLE
2. Subjects’ hydration state
Water Intake, ml Urine Output, ml Sweat Rate, ml
Subj CHOo CHOI. CHO,, CHOr. CHOu CHOI.
PN 1,054 1,123 / 512 303 1,250 1,530
RD 950 857 j 308 223 1,030 1,650
J-ML 328 200 344 302 1,320 920
PL 960 1,040 270 325 2,130 1,760
BB 1,075 830 340 682 1,370 1,360
LG 225 200 301 332 1,850 1,720
Mean 765.3 708.3 345.8 361.2 1,491.7 1,490.o
&SE t156.4 -r-166.7 -135.0 266.1 t168.5 t128.4
CHO,,, CHO-depleted condition; CHOI,, CHO-loaded condition.
1480 -
‘; 1280-
I
z
z 1080 -
2
I)
2 sm-
E
680 -
I SEM
CHOL CHOD
FIG. 4. Comparison of sweat urea N at rest, under CHO-loaded
condition (CHOL), and CHO-depleted condition (CHOn). *Rest
value taken from Cerny (4). Variation around rest value represents
range.
To determine whether the serum urea N results reflect
increased protein catabolism or simply decreased excre-
tion, total urea N excretion must be assessed. When both
methods of urea N excretion, i.e., urine and sweat, are
considered it is apparent that the observed nonsignificant
(P > 0.05) exercise decreases in kidney excretion (Fig. 3)
were more than compensated for by sweat urea’N in-
creases of 616.0 mg.h-’ (65.6-fold) and 1,440.l mg.h-’
(154.2-fold) in the CHOL and CHOn, respectively. It
appears, therefore, that the increased serum urea N
values reflect increased protein catabolism and not sim-
ply decreased excretion. As well, it should be noted that,
concerning this data, a number of factors may be oper-
ating in combination to produce an underestimation of
the actual amount of protein catabolized. These factors
are 1) urea N production in man accounts for only BO-
90% of the total protein catabolized during exercise (4);
2) 15-30s of the synthesized urea in man is hydrolyzed
in the alimentary tract (35), and 3) final urea N excretion
may continue for time periods longer than 240 min (27,
29). Previously, Young et al. (38) observed that urinary
N excretion was not affected by exercise. Data in the
present study are similar in that no clear change in
urinary urea N excretion during work was apparent. This
being the case, when calculating the amount of protein
catabolized, it would not be necessary to subtract the
observed kidney exercise decreases from the increased
sweat excretion values.
Based on the above factors, a theoretical estimate of
628
AVE. N
COMPOSITION
UREA OF
HYDROLYZED P ROTEI NS
CORRECTION IS 16%
1 I
(1440.1 i ,775 +
t
.85 X 6.25 X .0044 KCAMC-I)=$& = 10.4 %
1
CHOD TOTAL I
SWEAT UREA N PROTEIN TOTAL
CMG*HR-‘I CATABOLIZED EXERCISE
CORRECTION KCAL
FIG. 5. Protein contribution calculation.
the contribution of protein to total exercise calories dur-
ing the CHOD was constructed (Fig. 5). This
10.4%
con-
tribution is equivalent to a protein breakdown of 13.7 go
h-l. For comparison purposes a similar calculation in the
CHOL revealed a protein breakdown of 5.8 gmh-’ or
4.4%
of the total exercise calories. Since the protein in this
calculation (Fig. 5) is endogenous, the standard physio-
logical fuel value of 4.0 kcal$’ protein is not appropri-
ate. Rather the correct equivalent would be somewhere
between
4.78 [ii65
kcaLg-’ (crude protein) -0.866 kcal+
g-’ (urea) = 4.78 kcal l g-l] and 4.4 [5.65 kcal l g-’ (crude
protein) - 1.25 kcal.g-l (urinary energy) = 4.4 kcale
g-l]. Based on the rationale above, 4.4 kcal+g+’ was
selected as a conservative estimate of the caloric equiv-
alent of the endogenous protein oxidized. In addition to
this calculation, if the 24-h urinary N excretion is elevated
on the exercise day, as has been observed recently (8,27,
29), the contribution of protein would be even greater.
The potential overestimation in absolute sweat urea N
excretion due to evaporation of sweat (-II%) would
reduce the protein contribution calculation (Fig. 5) from
10.4
to 9.3%. It is the opinion of the authors, however,
that this error does not detract from the significance of
this calculation especially inasmuch as the conservative
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assumptions utilized in its derivation could increase the
estimate by a similar magnitude.
It is perhaps interesting to speculate that the increased
protein catabolism observed may be facilitated by hor-
monal changes. It is reasonable to suggest that increased
glucocorticoid and decreased insulin levels occurred in
response to the type of exercise studied (15, 26). If these
responses were greater in the CHOD, as one might expect,
protein degradation might increase
(17).
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may well account for at least part of the observed in-
creased protein breakdown in the CHOD. The procedure
of CHO loading frequently employed by most endurance
athletes may, therefore, have a significant “protein spar-
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In conclusion, these data suggest that protein catabo-
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catabolism cannot be determined from the present data.
Recent work employing 3-methylhistidine excretion to
estimate myofibrillar protein breakdown associated with
exercise has provided contradictory results. One study
noted an increased degradation in rats (19) whereas
another with humans found no change (7). It is probable
that a number of mechanisms are involved in this in-
creased protein utilization including
1)
the branched
chain amino acid-glucose alanine cycle, 2) the oxidation
of C skeletons from effluxed intracellular enzymes, and
3) possibly a contribution of protein carbon to exercise
calories when muscle glycogen supply is compromised.
Future studies are necessary to indicate the relative
contributions of these mechanisms.
The authors express their appreciation to Dr. F. J. Nagle and Dr. N.
J. Benevenga for their critical review of the manuscript.
Present address of P. W. R. Lemon: Applied Physiology Research
Laboratory, Kent Stale University, Kent, OH 44242.
Received 20 March 1979; accepted in final form 28 November 1979.
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... Excessive glycogen depletion can contribute to muscle fatigue by lowering ATP synthesis [7,9], and possibly also by lowering muscle excitation and impairing calcium release from the sarcoplasmic reticulum [10,11]. Endurance exercise in a significantly glycogen-depleted state can also increase protein oxidation and reduce muscle protein synthesis [12,13]; however, low pre-exercise glycogen availability has not been found to significantly affect anabolic signaling or muscle protein synthesis after strength training [12,13]. While low glycogen availability per se may not be detrimental for muscle anabolism, it can impair strength performance and training volume [14,15]. ...
... Excessive glycogen depletion can contribute to muscle fatigue by lowering ATP synthesis [7,9], and possibly also by lowering muscle excitation and impairing calcium release from the sarcoplasmic reticulum [10,11]. Endurance exercise in a significantly glycogen-depleted state can also increase protein oxidation and reduce muscle protein synthesis [12,13]; however, low pre-exercise glycogen availability has not been found to significantly affect anabolic signaling or muscle protein synthesis after strength training [12,13]. While low glycogen availability per se may not be detrimental for muscle anabolism, it can impair strength performance and training volume [14,15]. ...
... The high-protein drink resulted in greater performance on aggregate test performance, though not on any individually analyzed test. Since amino acids are theoretically unlikely to aid strength training performance via mechanisms not shared by carbohydrates (e.g., providing glucose via gluconeogenesis or insulin-mediated suppression of protein breakdown), protein's positive effect may have resulted from greater muscle protein synthesis and subsequent recovery [12,13,78] in between the two workouts, rather than an acute ergogenic effect per se. Thus, Lynch's [36] findings may be interpreted as a null effect of carbohydrate intake and a positive effect of protein intake, not a positive effect of carbohydrate restriction. ...
Article
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High carbohydrate intakes are commonly recommended for athletes of various sports, including strength trainees, to optimize performance. However, the effect of carbohydrate intake on strength training performance has not been systematically analyzed. A systematic literature search was conducted for trials that manipulated carbohydrate intake, including supplements, and measured strength, resistance training or power either acutely or after a diet and strength training program. Studies were categorized as either (1) acute supplementation, (2) exercise-induced glycogen depletion with subsequent carbohydrate manipulation, (3) short-term (2–7 days) carbohydrate manipulation or (4) changes in performance after longer-term diet manipulation and strength training. Forty-nine studies were included: 19 acute, six glycogen depletion, seven short-term and 17 long-term studies. Participants were strength trainees or athletes (39 studies), recreationally active (six studies) or untrained (four studies). Acutely, higher carbohydrate intake did not improve performance in 13 studies and enhanced performance in six studies, primarily in those with fasted control groups and workouts with over 10 sets per muscle group. One study found that a carbohydrate meal improved performance compared to water but not in comparison to a sensory-matched placebo breakfast. There was no evidence of a dose-response effect. After glycogen depletion, carbohydrate supplementation improved performance in three studies compared to placebo, in particular during bi-daily workouts, but not in research with isocaloric controls. None of the seven short-term studies found beneficial effects of carbohydrate manipulation. Longer-term changes in performance were not influenced by carbohydrate intake in 15 studies; one study favored the higher- and one the lower-carbohydrate condition. Carbohydrate intake per se is unlikely to strength training performance in a fed state in workouts consisting of up to 10 sets per muscle group. Performance during higher volumes may benefit from carbohydrates, but more studies with isocaloric control groups, sensory-matched placebos and locally measured glycogen depletion are needed.
... Dietary protein supports athlete's training and adaptation by providing the essential amino acid building blocks for the remodeling of muscle and body proteins. While carbohydrate and fat represent the primary energy sources during exercise, amino acid oxidation may contribute up to 10% of energy during exercise when carbohydrate availability is low [1,2]. Thus, research has clearly established that daily protein requirements are elevated above the current minimum daily recommended allowance of ~ 0.8 g/kg/day across the spectrum of sport disciplines [3]. ...
... These approaches, whether intentional or due to dietary deficiencies, are a feature of many elite endurance athlete training programs [137]. However, training with low carbohydrate availability has also been shown to augment amino acid oxidative losses as a compensatory energy source [2] that can increase daily protein requirements by ~ 10 to 15% [138], which Master athletes need to be mindful of if they incorporate this type of training into their plans. ...
... Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, 2 Daily meals refer to all meals throughout the day with the exception of the post-exercise meal 3 Endurance training refers to aerobic-based exercise of moderate-high intensity (e.g. ≥ 70% VO 2peak ) 4 Resistance training refers to high effort, externally loaded muscle contractions (e.g. ...
Article
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It is established that protein requirements are elevated in athletes to support their training and post-exercise recovery and adaptation, especially within skeletal muscle. However, research on the requirements for this macronutrient has been performed almost exclusively in younger athletes, which may complicate their translation to the growing population of Master athletes (i.e. > 35 years old). In contrast to older (> 65 years) untrained adults who typically demonstrate anabolic resistance to dietary protein as a primary mediator of the ‘normal’ age-related loss of muscle mass and strength, Master athletes are generally considered successful models of aging as evidenced by possessing similar body composition, muscle mass, and aerobic fitness as untrained adults more than half their age. The primary physiology changes considered to underpin the anabolic resistance of aging are precipitated or exacerbated by physical inactivity, which has led to higher protein recommendations to stimulate muscle protein synthesis in older untrained compared to younger untrained adults. This review puts forth the argument that Master athletes have similar muscle characteristics, physiological responses to exercise, and protein metabolism as young athletes and, therefore, are unlikely to have protein requirements that are different from their young contemporaries. Recommendations for protein amount, type, and pattern will be discussed for Master athletes to enhance their recovery from and adaptation to resistance and endurance training.
... In support of this premise, the same group previously showed ingestion of 18 g of egg protein was insufficient to replace oxidative losses associated with continuous, steady-state aerobic exercise (60 min treadmill running at 70% VO 2peak ) [91]. Multiple previous studies have demonstrated increased amino acid oxidation rates in response to aerobic-based exercise through stimulation of MPB rates [75,92,93]. Prolonged endurance training has been shown to preferentially oxidize branched-chain amino acids (BCAAs) [94,95], while replacement of amino acid losses due to hepatic gluconeogenesis [96] provides further support for ingestion of high-quality, leucine-enriched protein during endurance training [27,96]. ...
Article
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Background Systematic investigation of muscle protein synthesis (MPS) responses with or without protein ingestion has been largely limited to resistance training. Objective This systematic review determined the capacity for aerobic-based exercise or high-intensity interval training (HIIT) to stimulate post-exercise rates of MPS and whether protein ingestion further significantly increases MPS compared with placebo. Methods Three separate models analysed rates of either mixed, myofibrillar, sarcoplasmic, or mitochondrial protein synthesis (PS) following aerobic-based exercise or HIIT: Model 1 (n = 9 studies), no protein ingestion; Model 2 (n = 7 studies), peri-exercise protein ingestion with no placebo comparison; Model 3 (n = 14 studies), peri-exercise protein ingestion with placebo comparison. Results Eight of nine studies and all seven studies in Models 1 and 2, respectively, demonstrated significant post-exercise increases in either mixed or a specific muscle protein pool. Model 3 observed significantly greater MPS responses with protein compared with placebo in either mixed or a specific muscle fraction in 7 of 14 studies. Seven studies showed no difference in MPS between protein and placebo, while three studies reported no significant increases in mitochondrial PS with protein compared with placebo. Conclusion Most studies reporting significant increases in MPS were confined to mixed and myofibrillar PS that may facilitate power generating capacity of working skeletal muscle with aerobic-based exercise and HIIT. Only three of eight studies demonstrated significant increases in mitochondrial PS post-exercise, with no further benefits of protein ingestion. This lack of change may be explained by the acute analysis window in most studies and apparent latency in exercise-induced stimulation of mitochondrial PS.
... The potential requirement for greater doses of ingested protein to maximize MyoPS rates following endurance versus resistance exercise may be due to elevated rates of muscle protein breakdown during endurance exercise performed in the fasted state [84] and/or to oxidative amino acid losses during exercise [85,86] that ultimately must be replaced via dietary intake [85,87]. The oxidation of amino acids during exercise typically contributes ~ 5% of total energy provision [86]; however, amino acid utilization for oxidation increases with increased exercise intensity [88] and duration [89,90] as well as with reduced carbohydrate availability [84,91]. Acute tracer studies examining changes in muscle protein turnover in response to nutrition and/or exercise interventions are typically performed with participants in the overnight fasted state; however, individuals often undertake exercise training in the postabsorptive state or ingest nutrients (e.g., carbohydrates) during exercise to optimize performance. ...
Article
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Background Engaging in both resistance and endurance exercise within the same training program, termed ‘concurrent exercise training,’ is common practice in many athletic disciplines that require a combination of strength and endurance and is recommended by a number of organizations to improve muscular and cardiovascular health and reduce the risk of chronic metabolic disease. Dietary protein ingestion supports skeletal muscle remodeling after exercise by stimulating the synthesis of muscle proteins and can optimize resistance exercise-training mediated increases in skeletal muscle size and strength; however, the effects of protein supplementation on acute and longer-term adaptive responses to concurrent resistance and endurance exercise are unclear. Objectives The purpose of this systematic review is to evaluate the effects of dietary protein supplementation on acute changes in muscle protein synthesis and longer-term changes in muscle mass, strength, and aerobic capacity in responses to concurrent resistance and endurance exercise in healthy adults. Methods A systematic search was conducted in five databases: Scopus, Embase, Medline, PubMed, and Web of Science. Acute and longer-term controlled trials involving concurrent exercise and protein supplementation in healthy adults (ages 18–65 years) were included in this systematic review. Main outcomes of interest were changes in skeletal muscle protein synthesis rates, muscle mass, muscle strength, and whole-body aerobic capacity (i.e., maximal/peak aerobic capacity [VO2max/peak]). The quality of studies was assessed using the National Institute of Health Quality Assessment for Controlled Intervention Studies. Results Four acute studies including 84 trained young males and ten longer-term studies including 167 trained and 391 untrained participants fulfilled the eligibility criteria. All included acute studies demonstrated that protein ingestion enhanced myofibrillar protein synthesis rates, but not mitochondrial protein synthesis rates during post-exercise recovery after an acute bout of concurrent exercise. Of the included longer-term training studies, five out of nine reported that protein supplementation enhanced concurrent training-mediated increases in muscle mass, while five out of nine studies reported that protein supplementation enhanced concurrent training-mediated increases in muscle strength and/or power. In terms of aerobic adaptations, all six included studies reported no effect of protein supplementation on concurrent training-mediated increases in VO2max/peak. Conclusion Protein ingestion after an acute bout of concurrent exercise further increases myofibrillar, but not mitochondrial, protein synthesis rates during post-exercise recovery. There is some evidence that protein supplementation during longer-term training further enhances concurrent training-mediated increases in skeletal muscle mass and strength/power, but not whole-body aerobic capacity (i.e., VO2max/peak).
... This may be due to the need to replace oxidative losses of amino acids during exercise [80] and to provide substrates for the repair and rebuilding of body proteins after exercise [50]. If exercise is performed with low CHO availability, the contribution of protein to EEE may be as high as ~ 10% [43]. Given that XC skiers may fail to maintain high CHO availability on race days, protein catabolism during racing may exceed the values estimated above. ...
Article
The Tour de Ski (TDS: 6–9 sprint and distance races across 9–11 days) represents the most intense competition series of the cross-country (XC) ski season and is characterized by accumulated stress from consecutive days of high-intensity (~ 85%–160% VO2max) racing, travel, cold temperatures and low to moderate altitude (500–1500 m above sea level). Here, nutritional strategies play a key supportive role for optimized health, recovery and performance. This narrative review aims to provide an evidence-based discussion on the energetic demands of the TDS and recommendations for nutritional strategies to optimize health and performance of XC skiers during and following the TDS. We highlight several challenges that may arise during the TDS, including the following: poor energy availability (EA) due to decreased appetite or a pressure to maintain a low body weight, suboptimal carbohydrate availability due to a failure to replenish muscle glycogen stores across consecutive-day racing and increased risk of illness due to a combination of factors, including high-intensity racing, poor nutrition, sleep, travel and hygiene. We encourage XC skiers to maintain optimal overall EA across the ~ 1.5-week period, ensure high daily carbohydrate availability, as well as the use of strategies to maintain a healthy immune system. In addition, we include practical guidelines on the management of nutrition support prior to and during the TDS. We recognize that many nutritional questions remain unanswered both in the context of elite XC ski racing and specifically for extreme demands like the TDS that should be addressed in future investigations.
... This protein oxidation may to some extent account for the reduction in GE in the PROTEIN group. It has been reported that protein oxidation contributes up to 10% of total oxygen consumption [69], and can vary depending on training status [70], habitual diet [71], muscle glycogen levels [72], and pre-exercise protein ingestion [73], but further quantification of the influence of the pre-exercise meal is needed. Finally, training studies are needed to determine if longer-term adaptations to continuous and/or HIIT may be differentially influenced by pre-exercise nutrition choices. ...
Article
Full-text available
Nutritional intake can influence exercise metabolism and performance, but there is a lack of research comparing protein-rich pre-exercise meals with endurance exercise performed both in the fasted state and following a carbohydrate-rich breakfast. The purpose of this study was to determine the effects of three pre-exercise nutrition strategies on metabolism and exercise capacity during cycling. On three occasions, seventeen trained male cyclists (VO2peak 62.2 ± 5.8 mL·kg−1·min−1, 31.2 ± 12.4 years, 74.8 ± 9.6 kg) performed twenty minutes of submaximal cycling (4 × 5 min stages at 60%, 80%, and 100% of ventilatory threshold (VT), and 20% of the difference between power at the VT and peak power), followed by 3 × 3 min intervals at 80% peak aerobic power and 3 × 3 min intervals at maximal effort, 30 min after consuming a carbohydrate-rich meal (CARB; 1 g/kg CHO), a protein-rich meal (PROTEIN; 0.45 g/kg protein + 0.24 g/kg fat), or water (FASTED), in a randomized and counter-balanced order. Fat oxidation was lower for CARB compared with FASTED at and below the VT, and compared with PROTEIN at 60% VT. There were no differences between trials for average power during high-intensity intervals (367 ± 51 W, p = 0.516). Oxidative stress (F2-Isoprostanes), perceived exertion, and hunger were not different between trials. Overall, exercising in the overnight- fasted state increased fat oxidation during submaximal exercise compared with exercise following a CHO-rich breakfast, and pre-exercise protein ingestion allowed similarly high levels of fat oxidation. There were no differences in perceived exertion, hunger, or performance, and we provide novel data showing no influence of pre-exercise nutrition ingestion on exercise-induced oxidative stress.
... In addition, in our previous study, the subjects did not meet the recommended carbohydrate intake during the high volume training phase [1]. An insufficient availability of carbohydrates causes an increase in the oxidative loss of endogenous proteins [42,43] and decreases the MPS [43]. In the current study, all subjects had a positive energy balance and a higher carbohydrate intake than recommended. ...
Article
Full-text available
The protein requirement in athletes increases as a result of exercise-induced changes in protein metabolism. In addition, the frequency, quantity, and quality (i.e., leucine content) of the protein intake modulates the protein metabolism. Thus, this study aimed to investigate whether nutritional practice (particularly, protein and amino acid intake at each eating occasion) meets the protein needs required to achieve zero nitrogen balance in elite swimmers during a training camp. Eight elite swimmers (age 21.9 ± 2.3 years, body weight 64.2 ± 7.1 kg, sex M:2 F:6) participated in a four-day study. The nitrogen balance was calculated from the dietary nitrogen intake and urinary nitrogen excretion. The amino acid intake was divided over six eating occasions. The nitrogen balance was found to be positive (6.7 ± 3.1 g N/day, p < 0.05) with protein intake of 2.96 ± 0.74 g/kg/day. The frequency and quantity of leucine and the protein intake were met within the recommended range established by the International Society of Sports Nutrition. Thus, a protein intake of 2.96 g/kg/day with a well-designated pattern (i.e., frequency throughout the day, as well as quantity and quality) of protein and amino acid intake may satisfy the increased need for protein in an elite swimmer.
Chapter
Skeletal muscle mitochondria are placed in close proximity of the sarcoplasmic reticulum (SR), the main intracellular Ca2 + store. During muscle activity, excitation of sarcolemma and of T-tubule triggers the release of Ca2 + from the SR initiating myofiber contraction. The rise in cytosolic Ca2 + determines the opening of the mitochondrial calcium uniporter (MCU), the highly selective channel of the inner mitochondrial membrane (IMM), causing a robust increase in mitochondrial Ca2 + uptake. The Ca2 +-dependent activation of TCA cycle enzymes increases the synthesis of ATP required for SERCA activity. Thus, Ca2 + is transported back into the SR and cytosolic [Ca2 +] returns to resting levels eventually leading to muscle relaxation. In recent years, thanks to the molecular identification of MCU complex components, the role of mitochondrial Ca2 + uptake in the pathophysiology of skeletal muscle has been uncovered. In this chapter, we will introduce the reader to a general overview of mitochondrial Ca2 + accumulation. We will tackle the key molecular players and the cellular and pathophysiological consequences of mitochondrial Ca2 + dyshomeostasis. In the second part of the chapter, we will discuss novel findings on the physiological role of mitochondrial Ca2 + uptake in skeletal muscle. Finally, we will examine the involvement of mitochondrial Ca2 + signaling in muscle diseases.
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