Accepted Manuscript
Carbohydrate Restriction: Friend or Foe of Resistance-Based
Exercise Performance?
Jason M. Cholewa , Daniel E. Newmire , Nelo Eidy Zanchi
PII: S0899-9007(18)30953-5
DOI: https://doi.org/10.1016/j.nut.2018.09.026
Reference: NUT 10333
To appear in: Nutrition
Please cite this article as: Jason M. Cholewa , Daniel E. Newmire , Nelo Eidy Zanchi , Carbohydrate
Restriction: Friend or Foe of Resistance-Based Exercise Performance?, Nutrition (2018), doi:
https://doi.org/10.1016/j.nut.2018.09.026
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Carbohydrate Restriction 1
Highlights:
 The metabolic glycolytic response to resistance exercise is diverse and likely most
attributable to volume, duration, and intensity of effort
 Low muscle glycogen may not impair all resistance exercise performance, but increasing
blood glucose prior to exercise may enhance higher volume, longer duration performance
 Carbohydrate-restricted hypocaloric diets are effective for reducing fat mass during
resistance exercise, but carbohydrate-sufficient hypercaloric diets are likely optimal for
inducing muscle hypertrophy
Carbohydrate Restriction: Friend or Foe of Resistance-Based Exercise
Performance?
Carbohydrate Restriction: Friend or Foe of Resistance-Based Exercise
Performance?
Jason M. Cholewa1*
, Daniel E. Newmire2
, Nelo Eidy Zanchi3,4
1- Department of Kinesiology, Coastal Carolina University, Conway, SC, United States.
2- Department of Kinesiology and Military Science, University of Texas A&M, Corpus Christi, TX, United States
3- Department of Physical Education, Federal University of Maranhão, São Luís, Brazil.
4- Laboratory of Cellular and Molecular Biology of Skeletal Muscle (LABCEMME), São Luís, Brazil.
*Corresponding Author
Jason Cholewa
Coastal Carolina University
100 Independence Drive
Conway, SC 29576
jcholewa@coastal.edu
P: 843-349-2041
F: 843-349-2800
Authorship
This research did not receive any specific grant from funding agencies in the public, commercial, or
not-for-profit sectors.
N.E.Z. and J.M.C. developed the topic for review. J.M.C., D.E.N., N.E.Z. conducted literature searchers
and drafted the paper.
All authors aprove the submitted draft.
Word Count without references: 8907; with references: 12,833
Number of Tables: 0
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Carbohydrate Restriction 2
Number of Figures: 1
Running Head: Carbohydrate Restriction
Abstract
It is commonly accepted that adequate carbohydrate availability is necessary for
optimal endurance performance. However, for strength- and physique-based athletes,
sports nutrition research and recommendations have focused on protein ingestion, with far
less attention given to carbohydrate. Varying resistance exercise protocols, such as
differences in intensity, volume, and intra-set rest prescriptions between strength-training
and physique-training goals elicit different metabolic responses, which may necessitate
different carbohydrate needs. The results of several acute and chronic training studies
suggest that while severe carbohydrate restriction may not impair strength adaptations
during a resistance training program, consuming an adequate amount of carbohydrate in
the days leading up to testing may enhance maximal strength and strength-endurance
performance. Although several molecular studies demonstrate no additive increases in postexercise
mTORC1 phosphorylation with carbohydrate and protein compared protein
ingestion alone, the effects of chronic resistance training with carbohydrate restriction on
muscle hypertrophy are conflicting and require further research to determine a minimal
carbohydrate threshold necessary to optimize muscle hypertrophy. This review summarizes
the current knowledge regarding carbohydrate availability and resistance training outcomes
and poses new research questions that will better help guide carbohydrate
recommendations for strength and physique athletes. Additionally, given that success in
physique sports is based on subjective appearance, and not objective physical performance,
we also review the effects of sub-chronic carbohydrate ingestion during contest preparation
on aesthetic appearance.
Key Words: Muscle hypertrophy; protein metabolism; bodybuilding; body composition;
glycogen; muscular strength; muscular endurance
Introduction
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Glucose availability is important for muscular performance lasting greater than 30
seconds, and dietary carbohydrates are now considered the most important of the three
macronutrients to fuel endurance sports [1]. However, prior to the late 19th
century,
athletes, coaches, and even some scientists believed protein was the major source of energy
for muscular activity [2]. From a historical perspective, Zuntz [3, 4], Frentzel and Reach [5],
and Krogh and Lindhard [6] demonstrated through a series of landmark experiments that
carbohydrates and lipids fuel exercise, with the varying proportions of the two
macronutrients in the diet and the intensity of work determining the proportions in which
they were oxidized. In 1924, researchers from Harvard Medical School conducted
experiments in the Boston Marathon to investigate the role of carbohydrates on exercise
performance [7]. It was observed that blood glucose levels were reduced in several Boston
marathon runners who crossed the finish line, thus establishing a relationship between
blood glucose, carbohydrate consumption and performance [7]. In the following year, many
of these same athletes were supplemented with a large amount of carbohydrate the day
before the race, and they were allowed to eat sugar candy before and during the event [8].
Blood glucose concentrations following completion of the marathon were sampled by
researchers and they found that by normalizing blood glucose concentrations (before and
during running), symptoms of fatigue and stupor were prevented and mental focus was
increased [8]. This was one of the first studies to establish a causal link between
carbohydrate consumption and sport performance. In the 1960´s, it was demonstrated that
high carbohydrate diets improved endurance performance and carbohydrate feedings
during exercise delayed fatigue [9, 10, 11]. Finally, in the 1970’s, research revealed that
manipulation of dietary carbohydrate levels from a carbohydrate-free diet, mixed diet and
high carbohydrate diet increased muscle glycogen content, and consequentially increased
the time of moderate exercise to exhaustion [12]. The supra-cited effects of manipulation of
carbohydrate ingestion leading to increased muscle glycogen content are currently known
as ‘‘carbohydrate loading’’ [13, 14]. Those studies were essential to paving the road for the
carbohydrate saga in sports nutrition.
It is now fully appreciated that adequate carbohydrate ingestion is necessary for
optimal endurance performance, with recommendations well established in sports nutrition
societies [15]. However, for strength- and physique-based athletes, sports nutrition
recommendations have focused more on amino acid and protein ingestion [16], with much
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less attention given to carbohydrate requirements. In fact, the role of dietary carbohydrates
in strength training performance and adaptation are currently under debate, with some
researchers questioning whether dietary carbohydrates impart any ergogenic or adaptive
benefit to strength training at all [17]. For strength- and physique-based athletes,
carbohydrates are consumed for four main purposes. 1) to maintain high muscle glycogen
levels to sustain muscle contractions during high intensity strength training sessions. 2) to
enhance muscle recovery and adaptation (via increasing protein synthesis and suppressing
protein breakdown) between exercise sessions [18]. 3) to enhance aesthetics acutely,
especially for physique competitions, whereby carbohydrate loading increases muscle
glycogen and intermuscular water content leading to a more “muscular” appearance [19],
and 4) to improve body composition via reductions in fat mass, however in this case, most
individuals reduce carbohydrates consumption in an attempt to mobilize more fatty acids
from the adipose tissue [20]. In all four situations described above, carbohydrates are
important (either in high/adequate amounts or low amounts) for the strength training and
the physique athlete and will be discussed in detail after a brief explanation of carbohydrate
metabolism.
Carbohydrate Metabolism
Ingested carbohydrates are degraded by extensive enzymatic systems in the body,
initially found in saliva (salivary amylase), then in the pancreatic juice (pancreatic amylase)
and finally by intestinal microvilli enzymes (maltase, lactase and sucrase). After being
digested, they are absorbed as glucose or fructose in the intestine, via glucose/fructose
transporters [21]. In sports nutrition, the choice of a given source of carbohydrates is
extremely important for several reasons, from palatability to digestion and absorption [15].
Since carbohydrate consumption directly effects the postprandial glycemic response, and
because glucose is the major source of fuel for the central nervous system and erythrocytes
(besides being important for high intensity muscle contractions), maintaining blood glucose
levels is fundamental for both exercise performance and survival [22].
In mammals, hepatocytes are fundamental for blood glucose regulation, and it has
been hypothesized that hepatocytes have evolved to guarantee extra glucose supply for the
brain [22]. In the post-absorptive period for example, when food is no longer available and
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blood glucose levels begin to decrease, glucose is released by the liver, to counter balance
glucose utilization by the peripheral tissues [23]. This process of glucose release from the
liver to the circulatory system and peripheral tissues depends on several contra-regulatory
hormones such as glucagon, cortisol, epinephrine and several others secreted by different
organs [24, 25]. Because hepatocytes contain the enzyme glucose 6 phosphatase, which
splits off the phosphate molecule from the glucose carbon, glycogen from the liver can be
released back into circulation to supply the peripheral tissues [26]. Contrarily, after a meal,
glucose is stored in the liver and in peripheral tissues, in a process highly regulated by
insulin [25, 24]. It is interesting to note that the human body only stores ~100 g of glycogen
in the liver and ~400 g or 1.5 g  100 g-1
of glycogen in skeletal muscle glycogen in muscles
(or more, depending on the amount of lean mass and training status of an individual), but
humans easily store 20kg of triglyceride in adipose tissue [22]. Under this perspective,
glycogen is, if compared to fats, scarce in the body, and may be reduced as a result of
fasting, low dietary carbohydrate intake, and/or exercise. The availability of muscle glycogen
has been postulated to be essential in the evolutionary process [22]. For example,
performance of high intensity muscle contractions may have been essential for survival of
our ancestors to evade predators. Since muscle glycogen is an important source for high
energy anaerobic generation [23], sparing muscle glycogen would have been of ultimate
relevance for survival [22]. Replenishment of muscle glycogen, not only after exercise but
also after feast and famine periods would have been another important issue for survival
[22, 23]. In a modern view, sports nutrition for strength training athletes would be a sum of
all these factors: 1) Perform high intensity muscle contractions; 2) Utilize muscle glycogen;
3) Replenish muscle glycogen; 4) Perform better (survive and adapt), in athletic settings.
Muscle Contractions and Glucose Metabolism
Muscle contraction is a process dependent on intramuscular ATP being replenished
by bioenergetic systems [23]. During efforts lasting 30 - 180 seconds, the ATP required for
muscle contractions are mainly powered through glycolysis [27]. Glycolysis is a set of 10 step
reactions generating 2 or 3 ATP, depending if glucose or glycogen is the initial substrate,
respectively [27]. During anaerobic exercises, when available, glycogen is the preferred
source of energy [28]. Blood glucose also contributes to muscle glycolysis, increasing its
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contribution as muscle glycogen is utilized [29]. However, muscle performance decreases as
muscle glycogen is depleted [12]. During anaerobic glycolysis, by-products of metabolism
such as hydrogen ions and lactate are produced [30]. Hydrogen ions has been considered
inhibitors of muscle contraction either by inhibiting key enzymes of glycolysis (such as
phosphofructokinase) [30] or by competing with calcium for the troponin binding site [31].
Accumulation of hydrogen ions from glycolysis has also been postulated to be partially
responsible for muscle fatigue, which at first glance, would be negative for muscle
performance. However, it should be considered that fatigue is an important determinant for
a greater muscle fiber recruitment [32, 33, 34], which seems to be important for muscle
growth [35].
Skeletal muscle tissue accounts for ~ 40% of total body weight, contains 50–75% of
all body proteins, and accounts for 30–50% of whole-body protein turnover in humans. The
composition of skeletal muscle is mainly water (75%), protein content (20%) and other
products such as minerals, lipids, and carbohydrates (5%) [36]. Additionally, in respect to
glucose uptake and glycogen storage, skeletal muscle tissue is the main reservoir and tissue
of deposition. It has been observed in the postprandial state in humans and under
euglycemic-hyperinsulinemic conditions, 80% of glucose uptake occurs in skeletal muscle.
Studies using the euglycemic-hyperinsulinemic clamp and femoral artery/vein
catheterization to quantify glucose uptake have shown that adipose tissue uses ~5% of an
infused glucose load and bone is metabolically inert. This suggests that the majority of
glucose is deposited into skeletal muscle [37, 38].
In regard to the glucose transport, it has been thought that several mechanisms act
collectively to maintain a constant glucose flux to the contracting muscles. For example,
muscle contractions increase cytoplasmic calcium and modify the energy status of muscle
cells (increasing the AMP/ATP ratio) and both are considered important triggers for an
increased muscle glucose uptake response [39, 40]. Reactive oxygen species and hypoxia
may also be additional triggers in the muscle contraction process mediating increased
glucose uptake [39, 41]. The increased transport of glucose mediated by muscle
contractions utilizes specific carrier proteins called glucose transporters. In muscle cells the
glucose transporter number 4 (GLUT-4) is the major isoform expressed [42]. The movement
of this transporter from the sarcoplasm to the sarcolemma occurs by exocytosis, trafficking,
docking, and fusion of GLUT4-containing storage compartment or “vesicles” into the cell-
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surface membranes [23]. Following exercise, glycogen synthase is activated, and muscle
glycogen concentrations are allowed to increase, especially in the presence of proper
dietary carbohydrate consumption [11, 14]. Additionally, although glycogen depletion
seems to be an important factor in the rate of restoration of muscle glycogen levels after
exercise [43], this phenomenon has yet to be explored with the use of resistance exercise.
Metabolic Demands of Strength/Power Athlete Training and Physique Athlete Training
Resistance training variable prescriptions (volume, intensity, rest between sets,
repetition tempo, etc.) vary widely based upon the desired outcome. Consequentially,
metabolic demand and substrate utilization will also differ between resistance training
prescriptions. During the yearly training plan, strength and power athletes often divide their
training into periods of general preparation, defined in part by performing higher volumes
and lower intensities to optimize work capacity and hypertrophy, and specific preparation,
defined by lower volumes and higher intensities to optimize force and power output [44].
Though debate exists over the optimal intensity range to maximize hypertrophy [45],
physique athletes generally perform high volumes (15-20 sets per muscle group) with
moderate to higher repetitions (8 to 16 repetitions), and incomplete recovery periods (~1
minute) [46]. Although there is a wealth of research examining differences in metabolic
demand and substrate use between various aerobic exercise protocols, research examining
the difference in metabolic responses between resistance exercise protocols is lacking. For
this reason, we will split the following discussion into training for strength outcomes:
characterized by low repetitions (< 6), higher intensities (> 85% 1RM), and longer rest
periods (>3 min), and; hypertrophy outcomes, characterized by higher repetitions (> 8),
moderate intensities (60-80% 1 RM), and incomplete rest periods (< 2 min).
Several studies have investigated the energy cost of resistance training. The results
of these studies suggest that the more musculature used, especially the larger muscles of
the lower body, the greater the energy expenditure. For example, Ratamess et al. [47]
reported mean VO2 consumptions of 19.6 ml  kg-1
 min-1
and 12.5 ml  kg-1
 min-1
when
performing 3 sets of squats or bench press to muscular failure at 75% 1RM, respectively.
Similarly, Reis et al. [48] reported energy costs of 25.7 ml  kg-1
 min-1
and 11.41 ml  kg-1

min-1
for 1 set of leg press and bench press to muscular failure with 80% 1RM, respectively.
Although not surprising, performing multiple sets per exercise results in greater energy
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expenditures than performing a single set per exercise (49). Additionally, it appears that
higher repetitions (10 RM) and shorter rest intervals (30-60 sec) results in greater energy
expenditures than lower repetitions (5 RM) and shorter rest periods (3-5 min) [50]. These
differences in energy expenditure are both positively related to the total amount of work
performed during the set [51] as well as the total time under tension [52]; however, energy
expenditure during the recovery period may not differ between higher-repetition and
lower-repetition training and shows little to no correlation with the amount of work
performed [51].
Only a few studies have investigated glycogen utilization during resistance exercise.
Roy and Tarnopolsky [53] reported a 36% reduction in vastus lateralis muscle glycogen
following 3 rounds of a full-body circuit that contained 3 sets of leg press and 6 sets of leg
extension in addition to 6 upper body exercises each with 10 repetitions at 80% 1 RM.
Pascoe et al. [54] reported a 29% reduction in glycogen following 6 sets of 6 repetitions of
leg extension with 70% 1RM. Tesch et al. [55], using a volume prescription that more closely
resembles what might be performed by athletes engaged in a hypertrophy phase of
resistance training, had subjects perform front squats, back squats, leg presses and knee
extensions for 5 sets of 6-12 repetitions to muscular failure with a work:rest ratio of 1:2
(providing approximately 60-90 sec rest between sets). Muscle glycogen was reduced
approximately 26% and post exercise muscle lactate averaged 17.3 mmol  kg-1
wet weight.
Haff et al. [56] reported a 40% reduction in muscle glycogen following 3 sets of 10
repetitions of isokinetic knee extensions, back squats (65% 1RM), speed squats (45% 1RM),
and single-leg squats (10% 1 RM). Given that resistance exercise tends to recruit more high
threshold motor units compared to aerobic exercise, Koopman et al. [57] investigated the
differences in glycogen depletion between type I and II fibers following 8 sets of 8
repetitions at 75% 1RM in the leg press and leg extension exercises. An average 33%
reduction in muscle glycogen was found, with significant differences between type II fibers
(40-44% reduction) and type I fibers (24% reduction.
While it is clear that resistance training depends heavily on glycolytic metabolism,
less is known about how varying intensities affect glycogen depletion during resistance
exercise. To our knowledge, only two studies have directly accessed this question. In the
first study, Tesch et al. [58] investigated the difference in glycogen depletion between 5 sets
of 10 repetitions of concentric-only leg extension with either 30, 45, or 60% of the
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concentric 1RM. All sets were separated by 2 min and each intensity protocol was separated
by 45 min, such that all exercises were completed on the same day. Mixed muscle glycogen
depletion was related to the percentage of type IIAX/X fibers recruited, which was dictated
almost exclusively by the load used. In this study, glycogen depletion was greatest in the
60% 1RM condition, whereas the 30 and 45% 1RM conditions produced minimal glycogen
depletion in type IIAB/B fibers. There are three major limitations to consider when
interpreting the results of this study. First, exercise conditions were carried out on the same
day, spaced 45 min apart. Therefore, it is possible that pre-existing reductions in glycogen
and/or fatigue from the previous sessions may have influenced the subsequent sessions.
Second, muscle glycogenesis rates of up to 11 mmol kg-1
wet  wt-1
 hr-1
have been reported
following resistance exercise in the absence of any post-exercise caloric intake [59], further
confounding the differences in glycogen depletion between conditions. Finally, the
predetermined number of repetitions prescribed in the lower intensity (30 and 45% 1RM)
conditions are not representative of the common prescription of “repetitions to failure” in
current low-intensity resistance training protocols that have been demonstrated to induce
changes in muscle hypertrophy or strength [60]. In a later study, Robergs et al. [59]
evaluated differences in glycogen depletion following 6 sets of 6 repetitions of leg extension
with 70% 1RM or 6 sets of 12 repetitions matched for total work with 35% 1RM. Despite a
two-fold greater rate of glycogenolysis in the 70% 1RM condition compared to the 35% 1RM
condition (46 mmol kg-1
wet  wt-1
 sec-1
vs. 21 mmol kg-1
wet  wt-1
 sec-1
, respectively), no
differences in total mixed muscle glycogen depletion between conditions (~30% depletion)
were reported. Therefore, it appears that the volume of work performed, when of a higher
intensity of effort (approaching muscular failure), in addition to the total duration of the
training session, have the biggest impacts on glycogen use during resistance exercise.
In comparison to endurance or high intensity interval training, studies examining
substrate utilization during resistance exercise are scarce. Keul et al. [61] conducted one of
the first studies to examine energy metabolism in relation to resistance training. In this
study, competitive weight lifters performed 6 sets of 10, 5, 3, 2, 1, and 1 repetitions with a
progressively increasing load and 2 min of rest in the bench press, deadlift, and squat
exercise. The authors found increases in blood lactate only following the first set of 10
repetitions and concluded that for typical strength orientated training (low-repetition, highload)
the catabolism of high-energy phosphates is responsible for nearly all ATP
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Carbohydrate Restriction 10
regeneration. Utilizing a protocol more similar to hypertrophy-oriented training, Tesch et al.
[55] had bodybuilders perform five sets of front squats, back squats, leg press, and leg
extension to muscular failure (resulting in approximately 6-10 repetitions per set) with 80%
1RM and 60 seconds of rest between sets. Compared to pre-exercise, post-exercise PCr and
glycogen were reduced by approximately 49% and 26%, respectively, however muscle
biopsies were obtained 30 seconds after the completion of the final set, and it was likely
that PCr levels had increased since exercise cessation. Markers of glycolysis such as
intramuscular glucose, glucose-6-phosphate, and alpha-glycero-phosphate were increased
by approximately 1130%, 384%, and 246%, respectively. These results suggest that
resistance training programs typically employed during the general preparation phase or by
physique athletes have high phosphate and glycolytic requirements. It is interesting to note
that resting glycogen levels in this group of bodybuilders were 50-100% greater than those
reported in non-athletic populations. This was an interesting discovery, as it was previously
thought by some coaches at the time that resistance training did not significantly enhance
glycogen storage. In a pioneering study, MacDougall et al. [62] had bodybuilders perform
either 1 set or 3 sets of unilateral arm curl to muscular failure with 80% 1RM and assessed
changes in intramuscular ATP, creatine phosphate (PCr), glycogen, and lactate.
Intramuscular PCr was reduced by 64% and 50% following 1 and 3 sets, respectively.
Glycogen was reduced by 12 and 24%, and intramuscular lactate increased to 91.4 and 118
mmol/kg, following 1 set and 3 sets, respectively. Based on this data, Lambert and Flynn
(46) estimate that for the single set performed to muscular failure stored ATP provided
1.6%, PCr hydrolysis provided 16.3%, and glycolysis provided 82.1% of ATP demands.
Based off the aforementioned data, we speculate that energy expenditures and rates
of glycolysis are likely greater during training sessions focused on developing hypertrophy
compared to training sessions focused on developing maximal strength or power.
Additionally, PCr and glycolytic flux rates are greater when sets are taken to muscular failure
compared to when an equal amount of work is performed but sets are ceased well short (3-
5 repetitions) of muscular failure [63]. Given that training to muscular failure is more
prominent during hypertrophy training, we speculate that physique athletes and
strength/power athletes performing a general preparation phase catabolize more
carbohydrates than strength/power athletes performing a specific preparation phase. More
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research, however, is necessary to explore energy expenditure and substrate utilization
differences between hypertrophy and strength-oriented resistance training.
Muscle Glycogen Availability and Dietary Carbohydrate
Affect Resistance-Based Muscular Performance
Maintaining muscle glycogen via adequate carbohydrate consumption (4-7 g/kg/day)
is recommended to optimize both acute strength performance (i.e.: a power lifter who must
execute three 1RM attempts for the squat, bench press, and deadlift with 15-30 min of rest
between attempts during competition) and supporting high weekly volumes of resistancetraining
[63]. From a mechanistic perspective, it would appear that maintaining glycogen is
indeed important for performance in both acute and training scenarios. Glycogen is
localized to three distinct compartments within the muscle cell: subscarcolemmal,
intermyofibrillar (located between the myofibrils and in close proximity to the
mitochondria), and intramyofibrillar (located within the myofibrils, often in the I-band near
the sarcoplasmic reticulum and t-tubule triad junction) [64]. Intramyofibrillar glycogen is
theorized to provide the fuel for the sarcoplasmic reticular calcium release and calciumtransporting
ATPases [65]. Rapid calcium kinetics in type II muscle fibers would likely require
greater ATP to sustain contractile force, however, type II muscle fibers store approximately
40-50% less intramyofibrillar glycogen than type I fibers [66], likely because increasing
intramyofibrillar concentrations push contractile filaments closer to each other and
compromise shortening velocity [64]. To investigate the relationship between Ca2+
kinetics
and glycogen, Nielson et al. [67] stimulated intact mouse flexor digitorum brevis muscle
fibers with for 0.35 seconds every 10 seconds for 42 contractions. Fibers were then divided
into fatigued (>75% force decrements) or non-fatigued (<50% force decrements).
Intramyofibrillar glycogen was reduced by 68% in the fatigued fibers whereas no significant
changes occurred in the non-fatigued fibers. For all fatigued fibers in the study, a strong
correlation between low intramyofibrillar glycogen and decreasing tetanic Ca2+
concentrations existed. In an in vitro human study, Ortenblad et al. [65] demonstrated that
replenishing glycogen via carbohydrate feeding restored sarcoplasmic reticulum Ca2+
release
4 hr post-exercise whereas in the absence of carbohydrate intake sarcoplasmic reticulum
Ca2+
release rate remained depressed by 77%. Given that Ca2+
handling is also negatively
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Carbohydrate Restriction 12
impacted in preparations where global ATP is held constant but intramyofibrillar glycogen is
reduced [67], glycogen reductions have been suggested to reduce acute force output in an
indirect fashion. For example, metabolic disturbances caused by glycogen depletion may
occur in a structural nature, as enzymes associated with the glycogen particle may modulate
the sarcoplasmic reticulum Ca2+
release channels involved in excitation-contraction coupling
[68]. Collectively, this data suggests that maintaining intramuscular glycogen via adequate
carbohydrate consumption is necessary to both meet the direct metabolic demands during
resistance-exercise as well as to indirectly to support rapid calcium kinetics in contracting
type II muscle fibers.
Several studies have used diet and exercise to investigate how changes in glycogen
may affect resistance exercise performance, however, to our knowledge, only one study
directly measured glycogen levels prior to testing. In that study, Jacobs et al. [69] reported
significant reductions in type I and II muscle fiber glycogen content following a prolonged
aerobic and sprint interval exercise protocol. Muscular strength during a single maximal
effort dynamic contraction was reduced following glycogen depletion. However, since the
strength assessment took place 2 hours following the glycogen depletion protocol it is
unclear whether the reductions in force were the result of glycogen depletion or general
fatigue due to the prolonged exercise. Leveritt and Abernethy [70] used a similar glycogen
depletion protocol followed by two days of restricted carbohydrate intake (1.2 + 0.5 g  kg-1
,
19 + 3% energy intake). Compared to a control condition, carbohydrate restriction reduced
the total amount of repetitions performed during isoinertial squat with 80% 1RM but did
not affect isokinetic torque during the knee extension. Mitchell et al. [71] subjected subjects
to a similar depletion protocol followed by two days of a high (7.6 g  kg-1
) or low (0.34 g  kg-
1
) carbohydrate diet. In contrast to Leveritt and Abernethy [70], no differences in total
repetitions of squat, leg press, or leg extensions were found between conditions. These
conflicting results seem paradoxical. Subjects in Mitchell et al. [71] performed a higher
volume of resistance exercise, likely requiring greater glycolytic energy production, and
consumed approximately 33% less g  kg-1
carbohydrate following depletion. One may
assume that low muscle glycogen would have impaired resistance exercise performance
more under this protocol than Leveritt and Abernethy, however, this was not the case.
Lambert and Flynn [46] suggested that as a result of shorter rest periods and each set being
taken to failure, intramuscular acidosis may have been the cause of fatigue in Mitchell et al.
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Carbohydrate Restriction 13
[71], rather than carbohydrate availability. A second explanation may have been preexercise
blood glucose concentrations. Subjects completed the resistance exercise in
Mitchell et al. [71] in the fasted state, and blood glucose concentrations were similar
between conditions at baseline. While the exercise protocol was similar to what resistance
athletes perform in the field, very few athletes perform resistance training in the fasted
state. Given that pre-exercise carbohydrate feeding and subsequent increases in blood
glucose have been shown in several [72, 73, 74, 75, 76] studies to enhance resistanceexercise
performance, it is interesting to speculate that had an isocaloric meal matching the
respective high carbohydrate and low carbohydrate ratios been provided prior to resistance
exercise, baseline blood glucose would be different between conditions, and performance
may have been affected. Hypothetically, if performance was affected, then perhaps preexercise
blood glucose is more important than muscle glycogen to maintain high volumes of
resistance-resistance; however, future research is necessary to investigate this hypothesis.
Studies examining the effects of pre-exercise carbohydrate feeding/supplementation
on resistance exercise performance have produced mixed results. Lambert et al. [77]
reported improvements in leg extension performance with the ingestion of 1 g  kg-1
glucose
polymer pre-exercise. In this study subjects performed sets of 10 repetitions using their 10
RM with 3 min of rest for as many sets as possible until 7 repetitions could no longer be
completed. Haff et al. [78] reported similar results, where pre-exercise carbohydrate
ingestion improved total work and average power during 16 sets of isokinetic leg extension
exercise. In another study, Haff et al. [79] investigated the effects of pre-exercise
carbohydrate supplementation during twice-daily resistance training. A morning resistance
training session was completed followed by either the consumption of carbohydrate or
placebo, and four hours later subjects performed sets of squats with 10 repetitions and 55%
1RM to fatigue. Compared to placebo, subjects completed more repetitions and more sets
with carbohydrate ingestion. Most recently, Krings et al. [80] reported improvements in
bench press repetitions with 73% 1RM and a trend for improved total repetitions as part of
a battery of high intensity resistance exercise, plyometrics, and sprint interval work. On the
other hand, Conley et al. [81] reported no difference in multiple sets of 10 repetition squats
with 65% 1RM to failure when carbohydrate (oats) were consumed prior to exercise.
Vincent et al. [82] reported that pre-exercise carbohydrate ingestion did not affect isokinetic
work, power, or torque following a free weight training session consisting of 8 different
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exercises, and Kulik et al. [83] reported no differences in total repetitions and work between
carbohydrate and placebo during five sets of five repetition squats with 85% 1RM. It is likely
that the duration of the sessions in combination with the volume of work completed
explains these differences in outcomes. In the studies where ergogenic effects were
reported, session durations all lasted at least 50 min. In contrast, in 3 of the 4 studies where
an ergogenic effect was not present the exercise sessions lasted less than 40 min. In the
study where the exercise protocol lasted longer than 40 min [82], total volume completed
during the free weight resistance training sessions between conditions was not reported. It
appears that when combined with a standard diet (> 55% kcal from carbohydrate), preexercise
carbohydrate ingestion may only provide an ergogenic benefit when the total
training session is longer in duration (> 50 min), higher in volume (> 10 sets), and employs a
moderate intensity (50-75% 1 RM). Given that this is the most common exercise
prescription for hypertrophy outcomes, it is likely that pre-exercise carbohydrate ingestion
is most beneficial to physique athletes and athletes in the general preparation phase.
However, additional research is necessary to investigate the ergogenic effects of preexercise
carbohydrate intake prior to a typical power lifting or specific preparation type
training session (5-6 exercises with 5-6 sets of 2-6 repetitions) before further
recommendations can be made.
Researching examining the effects of non-acute low-carbohydrate intakes on
resistance exercise performance in healthy subjects engaged in a resistance training
program are limited. Three studies reported no difference between conditions for peak
knee extension/flexion torque, hand grip maximal strength [84], squat jump peak or mean
power [85], or 1 RM bench press and knee flexion/extension peak torque [86] following 7-
21 days of reduced carbohydrate intakes. Given the ambiguity of carbohydrate
recommendations for strength athletes [17], it is unclear whether the carbohydrate
restriction in these studies was severe enough to affect performance. Carbohydrate intakes
in these were 30% vs. 55% for 7 days, 4.4 g  kg-1
vs. 6.5 g  kg-1
for 4 days, and 42% vs. 62%
for 21 days, respectively. On the other hand, Escobar et al. [87] reported a trend toward an
increase in repetitions during a 12-minute workout when CrossFit athletes increased
carbohydrate consumption from approximately 3 to 6 g  kg-1
per day for three days. Given
the low volume of work and type of tests conducted in the first three studies, it appears that
moderate carbohydrate restriction (30-42% total energy intake) does not affect strength-
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based performance but increasing carbohydrate consumption could enhance general
preparation phase performance (i.e.: muscular endurance or resistance training density).
The effects of more severe carbohydrate restriction on resistance exercise
performance are less clear. For example, Sawyer et al. [88] reported consuming
approximately 30 g  day-1
carbohydrate resulted in small, yet significant, increases in back
squat 1RM, hand grip strength, and vertical jump, but not bench press 1 RM or power. Body
weight decreased by ~ 1.8 kg during the carbohydrate restriction, but not standard diet,
which may have positively changed the power to mass ration and thereby explain the
improvement in vertical jump. Additionally, the order of conditions may have influenced the
results. Subjects completed 7 days of standard diet, were tested, then completed 7 days of
carbohydrate restriction prior to being tested again. Therefore, due to lack of
randomization, or baseline testing, it is possible that a learning effect took place. Using a
within subjects cross-over design, Paoli et al. [89] reported no differences in vertical jump
nor body weight tests of muscular endurance following 30 days of a ketogenic or standard
diet in elite gymnasts. In contrast to Sawyer et al. [88], vertical jump did not improve despite
a decrease in body weight in the ketogenic group. The results of this study, however, are
confounded by the supplements administered during the ketogenic, but not standard diet,
conditions. For example, the sources of caffeine (guarana, coffee) and herbal antioxidant
supplements taken during the ketogenic condition may have influenced the training
adaptations. Wilson et al. [90] investigated the effects of a 10-week ketogenic diet
compared to a standard diet in conjunction with 8 weeks of resistance training in trained
men. Bench press and back squat 1 RM increased similarly in both groups. A one-week
carbohydrate loading (approximately 265 g  day-1
) period then followed week 10 posttesting.
Both back squat and bench press 1 RM increased in the ketogenic group compared
to week 10 but remained the same in the standard diet group. Although pre-exercise blood
glucose was not reported, given the difference in diet composition in the ketogenic group
between week 10 and 11, and the difference in performance outcomes, these results lend
some evidence to our hypothesis that pre-exercise blood glucose availability may influence
low volume, high load strength-based performance to a greater degree than muscle
glycogen. The results of these studies, while limited, seem to suggest that while severecarbohydrate
restriction may not impair strength adaptations during a resistance training
program, consuming an adequate amount of carbohydrate in the days leading up to testing
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(may enhance strength-based performance (i.e.: a powerlifting competition) and strengthendurance
based performance (i.e.: Crossfit, physique training, or general preparation
phase workouts).
Dietary Carbohydrate and Muscle Glycogen Affect Post-Resistance Exercise Adaptations
Insulin and insulin growth factor 1 (IGF-1) have been shown to play a large role in
skeletal muscle anabolism and potentially more importantly, restricting protein breakdown.
The receptors of insulin (IR) and IGF-1 (IGF-1R) have a 45-65% homology between their
ligand binding domains and 60-85% in their tyrosine kinase substrate recruitment domains.
It has been suggested that their respective genes have evolved from an ancestral gene that
has been highly conserved in the vertebrate family. This hormone/receptor communication
initiate metabolic, cellular growth, and differentiation responses from environmental
conditions and nutrient availability [91]. The consumption of carbohydrate stimulates an
insulin response, which then initiates an intramuscular cellular signaling process that
promotes glucose uptake, yet also promotes muscle protein synthesis (MPS) and restricts
the rate of protein breakdown (MPB). This signaling process involves the hormone insulin
binding and phosphorylating the insulin receptor and insulin receptor substrate‐1/2 (IRS‐
1/2) on tyrosine residues, and activates of phosphatidylinositol 3‐kinase (PI3-K). The
resulting phosphoinositol triphosphate promotes phosphorylation of protein kinase B/Akt,
which then phosphorylates various substrates that orchestrate the various physiological
effects. Increased glucose uptake is mediated predominantly through phosphorylation of
Akt substrate of 160kDa (TBC1D4) and TBC1D1, and thus facilitating the translocation of
GLUT-4 vesicles to the plasma membrane as well as disinhibition of glycogen synthesis by
phosphorylation of glycogen synthase kinase-3(GSK-3). The Akt promoted activation of
mTORC1, and subsequent ribosomal protein p70S6 kinase and eukaryotic translation
initiation factor 4E-binding protein 1 (4E-BP1), is responsible for muscle protein synthesis
(Figure 1). Concurrently, Akt-mediated inhibition of forkhead transcription factors (FOXOs)
activity reduces expression of the E3 ubiquitin ligases that are principally responsible for
mediating muscle atrophy via atrogin-1/ muscle atrophy F-box (MAFbx) and muscle RING
finger-1 (MuRF-1) [92, 93, 94, 95].
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[Insert Figure 1 About Here]
It has been shown that an acute bout of resistance exercise may reduce glycogen
content by ~23-36 % [59, 53]. This may influence and upregulation of 5′ adenosine
monophosphate-activated protein kinase (AMPK), which is an enzyme that appears to
function as a metabolic sensor in skeletal muscle because it becomes activated in response
to decreased ATP levels. It inhibits ATP-consuming pathways such as MPS and activates
pathways involved in CHO and fatty acid catabolism to facilitate resynthesis and restoration
of ATP levels. It is responsive to both acute exercise and has an adaptive response to chronic
exercise training [96]. Additionally, AMPK directly phosphorylates at least two proteins to
induce rapid suppression of mTORC1 activity, the TSC2 tumour suppressor and the critical
mTORC1 binding subunit raptor [97] and 4E-BP1 protein activity [98]. However, newer
human model research assessing concurrent training (endurance and resistance exercise)
has shown that AMPK may not influence downstream mTORC1 protein translational activity
[99]. With respect to resistance training and carbohydrate availability, Camera et al. [100]
reported no difference in AMPK, mTORC1 phosphorylation, or MPS following resistance
exercise in a glycogen depleted compared to replete state. Moreover, and perhaps more
importantly for athletes that train in fasted state and then consume food post-training, the
authors reported glycogen content did not affect the mTORC1 and MPS response to postexercise
carbohydrate and protein ingestion.
Proponents of nutrient timing in the fitness industry have suggested carbohydrate
ingestion is necessary to induce the anti-catabolic/anabolic effects of insulin following
resistance exercise. It should be noted that insulin does indeed promote muscle protein
synthesis and slow muscle protein breakdown. However, recently it has been suggested that
while insulin, in general, promotes the phosphorylation of intramuscular proteins related to
MPS: Akt, mTORC1, p70S6K, and eIF4E-binding protein-1 (4E-BP1), insulin concentrations
from 30 up to 167 IU/ml did not influence a further rise in MPS [101]. Wilkes et al [102]
supported this with data using a euglycemic clamp method showing that a minimal
concentration of insulin ~ 15 IU/ml (3 × post-absorptive) are sufficient to maximally
suppress leg MPB by 47% in the younger subjects. This was further supported by a metaanalysis
that showed no significant effect of insulin on MPS. The anti-catabolic effect of
insulin acting on MPB was confirmed in a recent systematic review and meta-analysis of 44
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human studies, which concluded insulin did not significantly affect MPS but has a crucial
role in reducing MPB. This group revealed that in healthy individuals, the effect of insulin on
MPS only becomes significant with an increase of essential amino acid (EAA) delivery to the
skeletal muscle [103]. In another systematic review by Trommelen et al. [104] again
supported that the effect of insulin on MPS is limited. They concluded that concurrent and
exogenous insulin and amino acid administration (ingestion or infusion) effectively increase
MPS, however this effect is mainly attributed to the hyperaminoacidemia rather than
hyperinsulinemia. Moreover, exogenous insulin administration systemically mediates
hypoaminoacidemia (amino acid uptake) which adverts any insulin stimulated effect on
MPS. With respect to resistance exercise adaptations, several studies have investigated the
effects of adding carbohydrate to protein in the post-exercise feeding. Koopman et al. [105]
reported the addition of either 0.15 g/kg or 0.6 g/kg carbohydrate did not further enhance
the MPS response to 0.3 g/kg protein during a 6-hour recovery period from resistance
exercise. Despite a 5-fold greater insulin area under the curve, and greater phosphorylation
of Akt, Staples et al. [106] reported the addition of 50 g of carbohydrate did not influence
the increase in MPS or reduction in MPB response to the ingestion of 25 g of protein alone.
Based on these studies, it appears that, acutely, neither glycogen content nor post-exercise
carbohydrate ingestion effects the molecular adaptations to resistance exercise when a
sufficient dose of protein is consumed.
Effects of Carbohydrate Manipulation on Body Composition Outcomes
When an organism consumes less calories than expended for a consistent period
(i.e.: longer than 24-48 hours) weight loss from reductions in body tissue occur; however, a
variety of factors that affect eating behavior and activity will influence both the rate as well
as the composition of the weight lost [107]. Given the risk of cardiovascular and metabolic
diseases associated with excess adiposity, even in individuals with BMI’s < 25 [108], and the
importance of maintaining muscle mass to reduce the risk sarcopenia, cardiovascular and
metabolic diseases [109], a wealth of studies have been conducted over the past decade
examining how different diet compositions affect fat and lean mass changes during a period
of caloric deficit. Differences in protein intake has been a major criticism of the greater
reductions in fat mass observed in carbohydrate-restricted groups compared to fat-
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restricted groups [107]. A recent meta-analysis by Hall and Guo [110] assessed 32 studies
comparing carbohydrate vs. fat restriction in overweight/obese subjects. Only studies where
protein was matched between groups and food was provided to control for errors in
reporting were included. The results of this meta-analysis demonstrated no differences in
fat loss between groups. Individuals in the fitness industry have criticized this research by
claiming it does not account for genetic differences, and contend that differences in
genotype will determine the success of a low-carbohydrate vs. low-fat diet. In a large (N =
208), long term (12 month) clinical trial, Gardner et al. [111] investigated the relationship
between genotype pattern, diet composition, and weight loss. Overweight subjects were
randomly divided into a low-carbohydrate group (30% carbohydrate, 45% fat, 23% protein)
or low-fat group (48% carbohydrate, 29% fat, 21% protein) and then further stratified into
either low-fat genotype (hypothesized to respond better to a low-fat diet), lowcarbohydrate
genotype (hypothesized to respond better to a low-carbohydrate diet, or a
neutral genotype. No differences were reported between dietary composition groups for
weight loss or percent body fat reductions. Additionally, there were no interactions
between genotype and dietary composition, indicating that subjects’ mis-matched for
hypothesized dietary composition (i.e.: a low-fat genotype consuming a low-carbohydrate
diet) did not lose more fat than those correctly matched. The results of the aforementioned
studies seem to suggest that when protein intake is held constant, there is no advantage to
adopting a low-carbohydrate diet over a low-fat diet, or vice versa. These studies, however,
were conducted in overweight/obese subjects not taking part in a resistance training
regimen.
The interaction between carbohydrate-restricted diets and resistance training
induced body composition outcomes in healthy individuals has not been well studied. The
first study to our knowledge to investigate this phenomenon in strength-based athletes was
conducted by Paoli et al. [89]. In this study, 30 days of a very-low-carbohydrate diet (~22
CHO  day-1
) resulted in greater reductions in weight and fat mass than a standard western
diet in elite male gymnasts. Given the positive association between higher protein intakes
and body composition outcomes, especially in lean athletes [112], these results are not
unexpected, and likely not attributable to restricted carbohydrates, as total energy intake
was lower and protein intake was approximately 2.4-fold greater during the carbohydraterestricted
condition. In another study, Kephart et al. [113] assigned CrossFit athletes to
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either a ketogenic low-carbohydrate diet or a control diet for three-months. While there
were no significant differences between groups for any body composition variables, a trend
was found for a decrease in fat mass and vastus lateralis muscle thickness in the ketogenic
diet group. These outcomes are also not unexpected, as the ketogenic diet group consumed
less self-report calories and a trend for more protein compared to baseline measurements.
Unfortunately, small sample sizes and lack of dietary reporting in the control group make it
difficult to draw further inferences from these results.
As of the writing of this review, only two studies have been conducted whereby a
carbohydrate-restricted diet was consumed for greater than two-months in conjunction
with strength training in trained individuals. In the first study, Wilson et al. [90] reported
similar increases in lean mass and vastus lateralis muscle thickness between a proteinmatched
ketogenic diet and control diet following 8 weeks of resistance. Although subjects
were placed on an eucaloric diet, similar decreases in fat mass were observed between
groups. In the second study, Vargas et al. [114] had trained men consume a moderate
hyperenergetic diet matched for protein (2 g  kg-1
 day-1
) of either 55% or < 10%
carbohydrate for 8 weeks in conjunction with four resistance training workouts per week.
Despite being prescribed a caloric surplus, both groups lost body fat, however, the change
was only significant in the ketogenic diet group (~ 1 kg). Conversely, there was a significant
increase in lean mass only in the conventional diet group (~ 1.3 kg). Total body water
increased in the conventional diet group, and slightly, but not significantly, decreased in the
ketogenic diet group. A major limitation to this study is the lack of dietary reporting in both
groups. It is possible that an appetite suppressive effect took part in the ketogenic group,
resulting in insufficient energy being consumed to support muscle hypertrophy. Based on
these results, however, we can conclude that while consuming a severely carbohydraterestricted
diet may be a viable option for enhancing changes in body composition via
reductions in body fat, consuming an adequate amount of carbohydrates in conjunction
with a caloric surplus is necessary to optimize muscle hypertrophy during resistance
training. More research, however, is necessary to determine a carbohydrate consumption
threshold to support hypertrophy in resistance training athletes.
Effects of Carbohydrate Manipulation on Aesthetic
Outcomes in Competitive Physique Athletes
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Physique athletes (i.e.: bodybuilding, physique, figure, and bikini divisions) are
assessed based on their presentation of an ‘aesthetic’ appearance, defined by appropriate
levels of muscularity, bilateral symmetry, aesthetic balance between various muscle groups,
and a low body fat [115]. Ergo, although two athletes of similar stature and muscular
development may present with differing body fat percentages, the athlete with the lower
measured body fat percentage may not always win. As such, physique athletes must not
only dramatically reduce body fat while minimizing reductions in lean mass, but may also go
through extreme, sometimes dangerous, protocols in the days leading up to competition
(peak week) to reduce subcutaneous extracellular water and increase intracellular water in
an attempt to present a “hard” appearance. For example, physique athletes will sometimes
significantly increase water intake and sodium consumption at the start of the peak week,
and then restrict water and sodium in the days leading up to competition to “reduce
subcutaneous water retention” [116]. However, this practice of dehydration will likely
reduce intramuscular water and plasma volume [117], which may lead to lower muscle
volume and reduce the efficacy of “pumping up” prior to posing in competition [118].
Carbohydrate and glycogen manipulation during peak week is a popular strategy
employed by physique athletes to “harden” their appearance [119]. Classically, physique
athletes would severely restrict carbohydrate intake and perform several glycogen depleting
workouts at the start of the week and then carbohydrate load 1-3 days prior to competition.
This approach has been modified by some, but not all contemporary coaches, whereby
physique athletes taper training and increase carbohydrate intake during peak week [116].
Though never measured, it is hypothesized that physique athletes will have reduced levels
of glycogen due to prolonged periods (generally 15-30 weeks) of calorie- and carbohydraterestricted
diets employed during contest preparation [118]. Thus, with adequate
carbohydrate loading, even without exhaustive exercise, a level of glycogen
supercompensation should occur [120]. It’s commonly accepted that each gram of glycogen
binds 2.7 – 4.0 grams of water [121] and increases in body water with carbohydrate loading
are predominantly the result of an increase in intercellular water [122]. Therefore,
carbohydrate loading during peak week should increase muscular volume, which,
theoretically, would increase subcutaneous tension thereby stretching the skin over the
musculature and leading to a more muscular and leaner appearance. However, during
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physique competition, competitors hold isometric contractions intermittently for 30 to 60
sec with intermittent breaks as they present one pose after another. As a result,
intramuscular blood flow may be compromised due to higher pressures [123], leading to a
dynamic exchange in fluid between intra- and extracellular fluid compartments. How
varying levels of muscle glycogen affect this dynamic requires further investigation.
Studies examining the quantitative and qualitative effects of this practice are limited.
Balon et al. [124] conducted the first study examining the effects of carbohydrate loading on
muscle girth in recreationally resistance-trained men. Subjects completed three days of
intense resistance training followed by 3 three days of taper. In the glycogen depletionrepletion
protocol, subjects consumed a eucaloric diet consisting of <10% calories from
carbohydrate for three days followed by three days of 80% carbohydrate intake. Girth
measurements of the upper and lower limbs as well as the chest were not different
following glycogen repletion nor different from the training only condition. Because there
were no differences in body weight between the control diet and the carbohydrate rich diet,
it's possible that either glycogen depletion did not occur to an appreciable level during the
carbohydrate-restricted period, or that the carbohydrate loading did not contain enough
total calories to induce glycogen supercompensation. Additionally, the subjects in this study,
although recreational weight lifters, were not as lean as physique athletes during peak
week. Subjects in Balon et al. [124] had an average body fat percentage of 10+1%. On the
other hand, male physique athletes often have body fat percentages of 4-8% for
competition [20, 125]. Therefore, it is possible that changes in muscle volume were not
detectable beneath the underlying subcutaneous tissue in this cohort. Finally, comparisons
in girth were not made between depleted and repleted states, which are more reflective of
the goals of physique athletes during peak week. In support of this hypothesis, Bamman et
al. [126] reported a 4.9% increase in biceps thickness the day before competition with
carbohydrate loading compared to six weeks prior. While this was likely the result of
carbohydrate loading, intramuscular glycogen was not directly assessed. To our knowledge,
only one published study has directly assessed the relationship between carbohydrate
loading and muscle volume. Nygren et al. [127] had trained men perform intense cycling for
45 minutes followed by four days of very low carbohydrate (25 g  day-1
) feeding. For the
next four days subjects consumed a very high carbohydrate, low fat diet. Muscle glycogen in
the depleted state decreased to 281 mmol  kg-1
 dry-1
dry weight and then increased 225%
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to 634 mmol  kg-1
 dry-1
weight following carbohydrate loading. Vastus muscle and thigh
cross sectional increased by 2.5 and 4 cm2
, respectively, compared to measures taken in the
depleted state. The results of this study demonstrate that carbohydrate loading in a state of
partially reduced glycogen leads to an increase in muscle volume. Given that subjects in
Nygren et al. [127] were untrained, resistance training increases the capacity to store
glycogen [128], bodybuilders store 50% more glycogen than untrained individuals [55], and
physique athletes have more muscle mass than non-resistance trained individuals, we
speculate that carbohydrate loading during peak week may result in both a greater absolute
and relative increase in muscle volume, that in very lean individuals would manifest in
visually detectable changes in muscularity and leanness during competition; however, more
research is necessary to explore this hypothesis.
Conclusions and Future Perspectives
The metabolic response to resistance training is distinct from endurance training and
differs from high-intensity interval training due to longer time under tension and more
prolonged eccentric contractions [46]. Moreover, variances in resistance training variable
prescription, such as the differences in volume, intensity, and inter-set rest between typical
strength and hypertrophy prescriptions, results in varying metabolic responses. Research
examining the effects of varying levels of carbohydrate restriction has produced conflicting
results. From this body of research, it appears that low glycogen and/or carbohydrate
availability does negatively affect acute resistance exercise performance when the volume
(< 8 sets) and duration (< 45 min) of exercise is low and the intensity is high (> 85% 1 RM).
On the other hand, increasing carbohydrates following a period of constriction may enhance
both acute strength performance (i.e.: 1 RM testing during a powerlifting competition) and
muscular endurance (i.e.: CrossFit). Additionally, increasing blood glucose prior to acute
resistance exercise via carbohydrate ingestion may result in greater work performed during
longer duration (> 50 min) resistance training sessions with a higher volume (> 10 sets) and
moderate intensity (50-75% 1RM). Given that volume is closely related to muscle
hypertrophy [129], pre-exercise carbohydrate ingestion may be especially important for
hypertrophy outcomes, such as offseason physique athletes and strength athletes
completing a general preparation phase. If carbohydrates are restricted to only the pre-
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exercise period, then it is likely that muscle glycogen will remain low during a period of
higher-volume resistance exercise. More research is therefore necessary to investigate the
effects of increasing blood glucose in a state of partial glycogen depletion on resistance
exercise performance.
The results from a number of molecular studies reveal that reduced glycogen and
blood glucose does not negatively influence the acute MPS stimulating effects of postexercise
protein ingestion. However, the effects of resistance training with chronicallyrestricted
carbohydrate ingestion is conflicting. Protocols where protein ingestion was not
matched between groups or varying levels of carbohydrate-restriction (i.e.: 0.5 g  kg-1
, g 
kg-1
, 10%, 30% total energy have all been defined as restrictive) are likely responsible for
differences in lean mass outcomes. Although studies with resistance training subjects are
limited, it appears that non-severe levels of carbohydrate restriction (i.e.: 30-40% total
energy) do not negatively influence hypertrophy adaptations, but severe carbohydrate
restriction (i.e.: < 10% total energy, or ketogenic diets) may compromise muscle
hypertrophy during a caloric surplus. In light of these discrepancies, more research is
necessary to investigate where a minimal carbohydrate threshold exists in relation to
hypertrophy outcomes during a caloric surplus.
Success in physique sports require attaining high levels of muscularity, low body fat
percentages, and the ability to display an aesthetic physique on stage during competition.
Based upon studies in the overweight/obese populations and one study in resistance
trained subjects, in conjunction with a higher (1.8 – 2.2 g  kg-1
) protein consumption,
maintaining a hypocaloric condition via carbohydrate-restriction seems to be a viable
strategy to reduce body fat while minimizing lean mass loss. Whether carbohydrate
restriction is superior or inferior to fat restriction for improving body composition in
strength and physique athletes remains to be answered and necessitates further research.
Finally, carbohydrate loading is a popular pre-competition strategy to enhance aesthetics in
physique athletes. While increasing carbohydrate consumption following glycogen depletion
increases muscle cross-sectional area, future research is necessary to address whether these
increases translate to increases in whole muscle volume in very lean individuals. If so, does
carbohydrate loading lead to visually noticeable improvements in physique?
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REFERENCES
[1] Applegate EA, Grivetti LE. Search for the competitive edge: a history of dietary fads and
supplements. J Nutr. 1997; 127: 869S-873S. doi: 10.1093/jn/127.5.869S.
[2] Hawley JA, Maughan RJ, Hargreaves M. Exercise Metabolism: Historical Perspective. Cell
Metab. 2015; 22:12-7. doi:10.1016/j.cmet.2015.06.016.
[3] Zuntz N. Über die Rolle des Zuckers im tierischen Stoffwechsel. Arch. f. Physiol. 1896;
538-542.
[4] Zunt . ber die Bedeutung der versehiedenen a hrstoffe als r- zeuger der
Muskelkraft. Pflugers Arch. 1901; 83: 557-571.
[5] Frentzel J, Reach F. Untersuchungen zur Frage nach der Quelle der Muskelkraft. Pflugers
Arch. 1901; 83: 477-508.
[6] Krogh A, Lindhard J. Relative value of fat and carbohydrate as source of muscular energy.
Biochem. J. 1920; 14: 290-363.
[7] Levine SA, Gordon B, Derick CL. Some changes in the chemical constituents of the blood
following a marathon race. J. Am. Med. Assoc. (1924) 82: 1778-1779.
[8] Gordon B, Kohn LA, Levine SA, Matton M, Scriver, W. de M. Scriver, Whiting WB. Sugar
content of the blood in runners following a marathon race. J. Am. Med. Assoc. 1925; 85:
508-509. doi:10.1001/jama.1925.02670070028009.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 26
[9] Ahlborg, B., Bergstrom, J., Ekelund, L.-G. & Hultman, E. Muscle glycogen and muscle
electrolytes during prolonged physical exercise. Acta Physiol. Scand. 1967; 70: 129-142. doi:
10.1111/j.1748-1716.1967.tb03608.x
[10] Bergstrom J, Hultman E. Nutrition for maximal sports performance. J. Am. Med. Assoc.
1972; 221: 999-1006.
[11] Bergstrom J, Hultman E. Muscle glycogen synthesis after exercise: an enhancing factor
localized to the muscle cells in man. Nature. 1966; 210: 309-310.
[12] Karlsson J, Saltin B. Diet, muscle glycogen, and endurance performance. J Appl Physiol.
1971; 31: 203-6.
[13] Astrand, PO. Something old and something new - very new. Nutr. Today. 1968; 3: 9-11.
[14] Bergstrom J, Hermansen L, Hultman E, Saltin B. Diet, muscle glycogen and physical
performance. Acta Physiol. Scand. 1967; 71: 140-150.
[15] Cermak NM, van Loon LJ. The use of carbohydrates during exercise as an ergogenic aid.
Sports Med. 2013; 43: 1139-55. International Society of Sports Nutrition Position Stand:
protein and exercise. doi: 10.1007/s40279-013-0079-0.
[16] Jäger R, Kerksick CM, Campbell BI, Cribb PJ, Wells SD, Skwiat TM, Purpura M, Ziegenfuss
TN, Ferrando AA, Arent SM, Smith-Ryan AE, Stout JR, Arciero PJ, Ormsbee MJ, Taylor LW,
Wilborn CD, Kalman DS, Kreider RB, Willoughby DS, Hoffman JR, Krzykowski JL, Antonio J.
International Society of Sports Nutrition Position Stand: protein and exercise. J Int Soc
Sports Nutr. 2017 Jun 20; 14:20. doi: 10.1186/s12970-017-0177-8.
[17] Escobar KA, Vandusseldorp TA, Kerksick CM. Carbohydrate intake and resistance-based
exercise: Are current recommendations reflective of actual need? Br J Nutr. 2016; 116:
2053-65. doi:10.1017/S0007114516003949.
ACCEPTED MANUSCRIPT
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M
ANUSCRIPT
Carbohydrate Restriction 27
[18] Haff GG, Lehmkuhl MJ, McCoy LB, Stone MH. Carbohydrate supplementation and
resistance training. J Strength Cond Res. 2003; 17: 187-96.
[19] Chan ST, Johnson AW, Moore MH, Kapadia CR, Dudley HA. Early weight gain and
glycogen-obligated water during nutritional rehabilitation. Hum Nutr Clin Nutr. 1982; 36:
223-32.
[20] Chappell AJ, Simper T, Barker ME. Nutritional strategies of high level natural
bodybuilders during competition preparation. J Int Soc Sports Nutr. 2018; 15: 4. doi:
10.1186/s12970-018-0209-z.
[21] Gray GM. Carbohydrate digestion and absorption. Role of the small intestine. N Engl J
Med. 1975; 292: 1225-30.
[22] Chakravarthy MV, Booth FW. Eating, exercise, and "thrifty" genotypes: connecting the
dots toward an evolutionary understanding of modern chronic diseases. J Appl Physiol.
2004; 96: 3-10. doi: 10.1152/japplphysiol.00757.2003
[23] Mul JD, Stanford KI, Hirshman MF, Goodyear LJ. Exercise and Regulation of
Carbohydrate Metabolism. Prog Mol Biol Transl Sci. 2015; 135:17-37. doi:
10.1016/bs.pmbts.2015.07.020.
[24] Aronoff SL. Glucose Metabolism and Regulation: Beyond Insulin and Glucagon. Diabetes
Spectrum 2004; 17: 183-190. doi: 10.2337/diaspect.17.3.183.
[25] Kruger DF, Aronoff SL, Edelman SV. Through the looking glass: current and future
perspectives on the role of hormonal interplay in glucose homeostasis. Diabetes Educ. 2007;
33: 32S-46S. doi: 10.1177/0145721707299766.
[26] van Schaftingen E, Gerin I. The glucose-6-phosphatase system. Biochem J. 2002; 362:
513-32.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 28
[27] Baker JS, McCormick MC, Robergs RA. Interaction among Skeletal Muscle Metabolic
Energy Systems during Intense Exercise. J Nutr Metab. 2010; 2010: 905612. doi:
10.1155/2010/905612.
[28] Hargreaves, M. The metabolic systems; carbohydrate metabolism. In: Farrell, PA.;
Joyner, MJ.; Hartmann H, Wirth K, Keiner M, Mickel C, Sander A, Szilvas E. Short-term
Periodization Models: Effects on Strength and Speed-strength Performance. Sports Med.
2015; 45: 1373-86. doi:10.1007/s40279-015-0355-2.
[29] Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E, Wolfe RR.
Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity
and duration. Am J Physiol. 1993; 265: E380-E391. doi: 10.1152/ajpendo.1993.265.3.E380.
[30] Robergs RA, Ghiasvand F, Parker D. Biochemistry of exercise-induced metabolic
acidosis. Am J Physiol Regul Integr Comp Physiol. 2004; 287: R502-16.
31- Gulati J, Babu A. Effect of acidosis on Ca2+ sensitivity of skinned cardiac muscle with
troponin C exchange. Implications for myocardial ischemia. FEBS Lett. 1989; 245: 279-82.
[32] Houtman CJ, Stegeman DF, Van Dijk JP, Zwarts MJ. Changes in muscle fiber conduction
velocity indicate recruitment of distinct motor unit populations. J Appl Physiol. 2003; 95:
1045-54.
[33] Sahlin K, Soderlund K, Tonkonogi M, et al. Phosphocreatine content in single fibers of
human muscle after sustained submaximal exercise. Am J Physiol. 1997; 273: C172-8.
[34] Vollestad NK, Vaage O, Hermansen L. Muscle glycogen depletion patterns in type I and
subgroups of type II fibres during prolonged severe exercise in man. Acta Physiol Scand.
1984; 122: 433-41.
[35] Schoenfeld BJ. Potential mechanisms for a role of metabolic stress in hypertrophic
adaptations to resistance training. Sports Med. 2013; 43: 179-94.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 29
[36] Frontera WR, Ochala J. Skeletal muscle: a brief review of structure and function. Calcif
Tissue Int. 2015; 96: 183-195. doi:10.1007/s00223-014-9915-y
[37] DeFronzo RA, Tripathy D. Skeletal muscle insulin resistance is the primary defect in type
2 diabetes. Diabetes Care. 2009; 32: S157-S163. doi: 10.2337/dc09-S302.
[38] Thiebaud D, Jacot E, DeFronzo RA, Maeder E, Jequier E, Felber JP. The effect of graded
doses of insulin on total glucose uptake, glucose oxidation, and glucose storage in man.
Diabetes. 1982; 31: 957-963.
[39] Richter EA, Hargreaves M. Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol
Rev. 2013; 93:933–1017. doi: 10.1152/physrev.00038.2012.
[40] Rockl KS, Witczak CA, Goodyear LJ. Signaling mechanisms in skeletal muscle: acute
responses and chronic adaptations to exercise. IUBMB Life. 2008; 60:145–153. doi:
10.1002/iub.21.
[41] Görgens SW, Benninghoff T, Eckardt K, Springer C, Chadt A, Melior A, Wefers J, Cramer
A, Jensen J, Birkeland KI, Drevon CA, Al-Hasani H, Eckel J. Hypoxia in Combination With
Muscle Contraction Improves Insulin Action and Glucose Metabolism in Human Skeletal
Muscle via the HIF-1α Pathway. Diabetes. 2017; 66: 2800-2807. doi: 10.2337/db16-1488.
[42] Klip A, Paquet MR. Glucose transport and glucose transporters in muscle and their
metabolic regulation. Diabetes Care. 1990; 13: 228-243.
[43] Garcia Roves PM, Han DH, Song Z, Jones TE, Hucker KA, and Holloszy JO. Prevention of
glycogen supercompensation prolongs the increase in muscle GLUT4 after exercise. Am J
Physiol Endocrinol Metab. 2003; 285: E729-E736.
[44] Hartmann H, Wirth K, Keiner M, Mickel C, Sander A, Szilvas E. Short-term Periodization
Models: Effects on Strength and Speed-strength Performance. Sports Med 2015; 45: 1373-
86. doi:10.1007/s40279-015-0355-2.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 30
[45] Loenneke J. Skeletal Muscle Hypertrophy: How important is Exercise Intensity? J
Trainology 2012; 1: 28-31. doi: 10.17338/trainology.1.2_28.
[46] Lambert CP, Flynn MG. Fatigue during High-Intensity Intermittent Exercise. Sport Med.
2002; 32: 511-22. doi:10.2165/00007256-200232080-00003.
[47] Ratamess N, Rosenberg J, Klei S, BM D, Kang J, Smith CR, Ross RE, Faigenbaum AD.
Comparison of the acute Metabolic responses to traditional resistance, BW and Battling
Rope Exercises. J Strength Cond Res. 2015; 29: 47-57. doi: 10.1519/JSC.0000000000000584.
[48] Reis VM, Garrido ND, Vianna J, Sousa AC, Alves JV, Marques MC. Energy cost of isolated
resistance exercises across low- to high-intensities. PLoS One 2017; 12: 1-11.
doi:10.1371/journal.pone.0181311.
[49] Mookerjee S, Welikonich MJ, Ratamess NA. Comparison of energy expenditure during
single-Set vs. multiple-set resistance exercise. J Strength Cond Res. 2016; 30: 1447-52.
doi:10.1519/JSC.0000000000001230.
[50] Ratamess NA, Falvo MJ, Mangine GT, Hoffman JR, Faigenbaum AD, Kang J. The effect of
rest interval length on metabolic responses to the bench press exercise. Eur J Appl Physiol.
2007; 100: 1-17. doi:10.1007/s00421-007-0394-y.
[51] Scott CB, Leighton BH, Ahearn KJ, McManus JJ. Aerobic, anaerobic, and excess
postexercise oxygen consumption energy expenditure of muscular endurance and strength:
1-set of bench press to muscular fatigue. J Strength Cond Res 2011; 25: 903-8.
doi:10.1519/JSC.0b013e3181c6a128.
[52] Buitrago S, Wirtz N, Yue Z, Kleinöder H, Mester J. Mechanical load and physiological
responses of four different resistance training methods in bench press exercise. J Strength
Cond Res. 2013 Apr;27(4):1091-100. doi: 10.1519/JSC.0b013e318260ec77.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 31
[53] Roy BD, Tarnopolsky MA. Influence of differing macronutrient intakes on muscle
glycogen resynthesis after resistance exercise. J Appl Physiol 1998; 84: 890-896.
10.1152/jappl.1998.84.3.890.
[54] Pascoe DD, Costill DL, Fink WJ, Robergs RA, Zachwieja JJ. Glycogen resynthesis in
skeletal muscle following resistive exercise. Med Sci Sport Exerc. 1993; 25: 349-354.
[55] Tesch PA, Colliander EB, Kaiser P. Muscle metabolism during intense, heavy-resistance
exercise. Eur J Appl Physiol Occup Physiol. 1986; 55: 362-6.
[56] Haff GG, Koch AJ, Potteiger JA, Kuphal KE, Magee LM, Green SB, Jakicic JJ. Carbohydrate
supplementation attenuates muscle glycogen loss during acute bouts of resistance exercise.
Int J Sport Nutr Exerc Metab. 2000; 10: 326-39.
[57] Koopman R, Manders RJF, Jonkers RAM, Hul GBJ, Kuipers H, van Loon LJC.
Intramyocellular lipid and glycogen content are reduced following resistance exercise in
untrained healthy males. Eur J Appl Physiol. 2006; 96: 525-34. doi:10.1007/s00421-005-
0118-0.
[58] Tesch P, Ploutz-Synder L, Ystrom L, Castro M, Dudley G. Skeletal Muscle Glycogen Loss
Evoked by Resistance Exercise. J Strength Cond Res. 1998; 12: 67-73.
[59] Robergs RA, Pearson DR, Costill DL, Fink WJ, Pascoe DD, Benedict MA, Lambert CP,
Zachweija JJ. Muscle glycogenolysis during differing intensities of weight-resistance exercise.
J Appl Physiol. 1991; 70: 1700-1706. doi:10.1016/j.amjmed.2013.12.014.
[60] Morton RW, Oikawa SY, Wavell CG, Mazara N, McGlory C, Quadrilatero J, Baechler BL,
Baker SK, Phillips SM. Neither load nor systemic hormones determine resistance trainingmediated
hypertrophy or strength gains in resistance-trained young men. J Appl Physiol.
2016; 121: 129-38. doi:10.1152/japplphysiol.00154.2016.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 32
[61] Keul J, Haralambie G, Bruder M, Gottstein HJ. The effect of weight lifting exercise on
heart rate and metabolism in experienced weight lifters. Med Sci Sports 1978; 10: 13-5.
[62] MacDougall JD, Ray S, Sale DG, McCartney N, Lee P, Garner S. Muscle substrate
utilization and lactate production. Can J Appl Physiol. 1999; 24: 209-15.
[63] Slater G, Phillips SM. Nutrition guidelines for strength sports: sprinting, weightlifting,
throwing events, and bodybuilding. J Sports Sci. 2011; 29: S67-77.
doi:10.1080/02640414.2011.574722.
[64] Nielsen J, Ørtenblad N. Physiological aspects of the subcellular localization of glycogen
in skeletal muscle. Appl Physiol Nutr Metab. 2013; 38: 91-9. doi:10.1139/apnm-2012-0184.
[65] Ørtenblad N, Nielsen J, Saltin B, Holmberg HC. Role of glycogen availability in
sarcoplasmic reticulum Ca2+ kinetics in human skeletal muscle. J Physiol. 2011 Feb 1;589(Pt
3):711-25. doi: 10.1113/jphysiol.2010.195982.
[66] Nielsen J, Holmberg H-C, Schrøder HD, Saltin B, Ortenblad N. Human skeletal muscle
glycogen utilization in exhaustive exercise: role of subcellular localization and fibre type. J
Physiol. 2011; 589: 2871-85. doi:10.1113/jphysiol.2010.204487.
[67] Nielsen J, Cheng AJ, Ørtenblad N, Westerblad H. Subcellular distribution of glycogen
and decreased tetanic Ca2+ in fatigued single intact mouse muscle fibres. J Physiol. 2014;
592: 2003-12. doi:10.1113/jphysiol.2014.271528.
[68] Ørtenblad N, Westerblad H, Nielsen J. Muscle glycogen stores and fatigue. J Physiol.
2013; 591: 4405-13. doi:10.1113/jphysiol.2013.251629.
[69] Jacobs I, Kaiser P, Tesch P. Muscle strength and fatigue after selective glycogen
depletion in human skeletal muscle fibers. Eur J Appl Physiol Occup Physiol 1981; 46: 47-53.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 33
[70] Leveritt M, Abernethy P. Effects of Carbohydrate Restriction on Strength Performance. J
Strength Cond Res 1999; 13: 52-7.
[71] Mitchell JB, DiLauro PC, Pizza FX, Cavender DL. The effect of preexercise carbohydrate
status on resistance exercise performance. Int J Sport Nutr. 1997; 7: 185-96.
[72] Lambert CP, Costill DL, McConell GK, Benedict MA, Lambert GP, Robergs RA, Fink WJ.
Fluid replacement after dehydration: influence of beverage carbonation and carbohydrate
content. Int J Sports Med. 1992; 13: 285-92.
[73] Laurenson DM, Dubé DJ. Effects of carbohydrate and protein supplementation during
resistance exercise on respiratory exchange ratio, blood glucose, and performance. J Clin
Transl Endocrinol 2015; 2: 1-5. doi:10.1016/j.jcte.2014.10.005.
[74] Oliver JM, Almada AL, Van Eck LE, Shah M, Mitchell JB, Jones MT, et al. Ingestion of High
Molecular Weight Carbohydrate Enhances Subsequent Repeated Maximal Power: A
Randomized Controlled Trial. PLoS One 2016;11:e0163009.
[75] Wax B, Brown SP, Webb HE, Kavazis AN. Effects of carbohydrate supplementation on
force output and time to exhaustion during static leg contractions superimposed with
electromyostimulation. J Strength Cond Res 2012;26:1717–23.
doi:10.1519/JSC.0b013e318234ec0e.
[76] Wax B, Kavazis AN, Brown SP. Effects of supplemental carbohydrate ingestion during
superimposed electromyostimulation exercise in elite weightlifters. J Strength Cond Res
2013;27:3084–90. doi:10.1519/JSC.0b013e31828c26ec.
[77] Lambert CP, Flynn MG, Boone Jr Jb, Michaud TJ, Rodriguez-Zayas J. Effects of
carbohydrate feeding on Multiple-bout Resistance Exercise. 1991; 5: 192-197.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 34
[78] Haff GG, Schroeder CA, Koch AJ, Kuphal KE, Comeau MJ, Potteiger JA. The effects of
supplemental carbohydrate ingestion on intermittent isokinetic leg exercise. J Sports Med
Phys Fitness. 2001; 41: 216-22.
[79] Haff GG, Stone MH, Warren B, Keith R, Johnson R, Nieman D, et al. The Effect of
Carbohydrate Supplementation on Multiple Sessions and Bouts of Resistance Exercise. J
Strength Cond Res 1999; 13: 111-7.
[80] Krings BM, Rountree JA, McAllister MJ, Cummings PM, Peterson TJ, Fountain BJ, Smith
JW. Effects of acute carbohydrate ingestion on anaerobic exercise performance. J Int Soc
Sports Nutr. 2016; 13: 40.
[81] Conley M, Stone MH, Marsit JL, O’Bryant HS, Nieman D, Johnson J, et al. Effects of
Carbohydrate Ingestion on Resistance Exercise. J Strength Cond Res 1995; 9: 201.
[82] Vincent K, Clarkson P, Freedson P, DeCheke M. Effect of pre-exercise liquid, high
carbohydrate feeding on resistance exercise performance. Med Sci Sports Exerc 1993; 25:
S194.
[83] Kulik JR, Touchberry CD, Kawamori N, Blumert PA, Crum AJ, Haff GG. Supplemental
carbohydrate ingestion does not improve performance of high-intensity resistance exercise.
J Strength Cond Res 2008;22:1101–7. doi:10.1519/JSC.0b013e31816d679b.
[84] Dipla K, Makri M, Zafeiridis A, Soulas D, Tsalouhidou S, Mougios V, Kellis S. An
isoenergetic high-protein, moderate-fat diet does not compromise strength and fatigue
during resistance exercise in women. Br J Nutr. 2008; 100: 283-6.
[85] Hatfield DL, Kraemer WJ, Volek JS, Rubin MR, Grebien B, Gómez AL, French DN, Scheett
TP, Ratamess NA, Sharman MJ, McGuigan MR, Newton RU, Häkkinen K. The effects of
carbohydrate loading on repetitive jump squat power performance. J Strength Cond Res.
2006; 20: 167-71. doi:10.1519/R-18300.1.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 35
[86] Van Zant RS, Conway JM, Seale JL. A moderate carbohydrate and fat diet does not
impair strength performance in moderately trained males. J Sports Med Phys Fitness. 2002;
42: 31-7.
[87] Escobar KA, Morales J, Vandusseldorp TA. The Effect of a Moderately Low and High
Carbohydrate Intake on Crossfit Performance. Int J Exerc Sci. 2016; 9: 460-70.
[88] Sawyer JC, Wood RJ, Davidson PW, Collins SM, Matthews TD, Gregory SM, Paolone VJ.
Effects of a short-term carbohydrate-restricted diet on strength and power performance. J
Strength Cond Res. 2013; 27: 2255-62. doi:10.1519/JSC.0b013e31827da314.
[89] Paoli A, Grimaldi K, D’Agostino D, Cenci L, Moro T, Bianco A, Palma A. Ketogenic diet
does not affect strength performance in elite artistic gymnasts. J Int Soc Sports Nutr. 2012;
9: 34. doi:10.1186/1550-2783-9-34.
[90] Wilson JM, Lowery RP, Roberts MD, Sharp MH, Joy JM, Shields KA, Partl J, Volek JS,
D'Agostino D. The Effects of Ketogenic Dieting on Body Composition, Strength, Power, and
Hormonal Profiles in Resistance Training Males. J Strength Cond Res. 2017;
doi:10.1519/JSC.0000000000001935.
[91] Belfiore A, Frasca F, Pandini G, Sciacca L, Vigneri R. Insulin receptor isoforms and insulin
receptor/insulin-like growth factor receptor hybrids in physiology and disease. Endocr Rev.
2009; 30: 586-623. doi: 10.1210/er.2008-0047.
[92] Cleasby ME, Jamieson PM, Atherton PJ. Insulin resistance and sarcopenia: mechanistic
links between common co-morbidities. J Endocrinol. 2016; 229: R67-81. doi: 10.1530/JOE-
15-0533.
[93] Glass DJ. Skeletal muscle hypertrophy and atrophy signaling pathways. Int J Biochem
Cell Biol. 2005; 37: 1974-1984. doi:10.1016/j.biocel.2005.04.018.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 36
[94] Middelbeek RJ, Chambers MA, Tantiwong P, Treebak JT, An D, Hirshman MF, Musi N,
Goodyear LJ. Insulin stimulation regulates AS160 and TBC1D1 phosphorylation sites in
human skeletal muscle. Nutrition & diabetes. 2013; 3: e74. 10.1038/nutd.2013.13.
[95] Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M. Mechanisms regulating skeletal
muscle growth and atrophy. The FEBS journal. 2013; 280(17), 4294-4314. doi:
10.1111/febs.12253.
[96] Aschenbach WG, Sakamoto K, Goodyear LJ. 5' adenosine monophosphate-activated
protein kinase, metabolism and exercise. Sports Med. 2004; 34 : 91-103.
[97] Shaw RJ. LKB1 and AMP‐activated protein kinase control of mTOR signalling and
growth. Acta Physiol. 2009; 196: 65-80. doi: 10.1111/j.1748-1716.2009.01972.x.
[98] Dreyer HC, Fujita S, Cadenas JG, Chinkes DL, Volpi E, Rasmussen BB. Resistance exercise
increases AMPK activity and reduces 4 ‐BP1 phosphorylation and protein synthesis in
human skeletal muscle. J Physiol. 2006; 576: 613-624.
[99] Apró W, Moberg M, Hamilton DL, Ekblom B, van Hall G, Holmberg HC, Blomstrand E.
Resistance exercise-induced S6K1 kinase activity is not inhibited in human skeletal muscle
despite prior activation of AMPK by high-intensity interval cycling. Am J Physiol Endocrinol
Metab. 2015; 308: E470-81. doi: 10.1152/ajpendo.00486.2014.
[100] Camera DM, West DWD, Burd NA, Phillips SM, Garnham AP, Hawley JA, Coffey VG.
Low muscle glycogen concentration does not suppress the anabolic response to resistance
exercise. J Appl Physiol. 2012; 113: 206-14. doi:10.1152/japplphysiol.00395.2012.
[101] Phillips SM. Insulin and muscle protein turnover in humans: stimulatory, permissive,
inhibitory, or all of the above? Am J Physiol Endocrinol Metab. 2008; 295: E731.
doi:10.1152/ajpendo.90569.2008.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 37
[102] Wilkes EA, Selby AL, Atherton PJ, Patel R, Rankin D, Smith K, Rennie MJ. Blunting of
insulin inhibition of proteolysis in legs of older subjects may contribute to age-related
sarcopenia. Am J Clin Nutr. 2009; 90: 1343-1350. doi: 10.3945/ajcn.2009.27543.
[103] Abdulla H, Smith K, Atherton PJ, Idris I. Role of insulin in the regulation of human
skeletal muscle protein synthesis and breakdown: a systematic review and meta-analysis.
Diabetologia. 2016; 59: 44-55. doi: 10.1007/s00125-015-3751-0.
[104] Trommelen J, Groen BB, Hamer HM, de Groot LC, van Loon LJ. Mechanisms in
endocrinology: exogenous insulin does not increase muscle protein synthesis rate when
administrated systemically: a systematic review. European journal of endocrinology. 2015;
173: R25-34. doi: 10.1530/EJE-14-0902.
[105] Koopman R, Beelen M, Stellingwerff T, Pennings B, Saris WHM, Kies AK, Kuipers H, van
Loon LJ. Coingestion of carbohydrate with protein does not further augment postexercise
muscle protein synthesis. Am J Physiol Endocrinol Metab. 2007; 293: E833-42.
doi:10.1152/ajpendo.00135.2007.
[106] Staples AW, Burd NA, West DWD, Currie KD, Atherton PJ, Moore DR, Rennie MJ,
Macdonald MJ, Baker SK, Phillips SM. Carbohydrate does not augment exercise-induced
protein accretion versus protein alone. Med Sci Sports Exerc. 2011; 43: 1154-61.
doi:10.1249/MSS.0b013e31820751cb.
[107] Aragon AA, Schoenfeld BJ, Wildman R, Kleiner S, VanDusseldorp T, Taylor L, Earnest
CP, Arciero PJ, Wilborn C, Kalman DS, Stout JR, Willoughby DS, Campbell B, Arent SM,
Bannock L, Smith-Ryan AE, Antonio J. International society of sports nutrition position stand:
diets and body composition. J Int Soc Sports Nutr 2017; 14: 16. doi:10.1186/s12970-017-
0174-y.
[108] Maffetone PB, Rivera-Dominguez I, Laursen PB. Overfat and Underfat: New Terms and
Definitions Long Overdue. Front Public Heal. 2016; 4: 279. doi:10.3389/fpubh.2016.00279.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 38
[109] Wolfe RR. The underappreciated role of muscle in health and disease. Am J Clin Nutr.
2006; 84: 475-82. doi:10.1093/ajcn/84.3.475.
[110] Hall KD, Guo J. Obesity Energetics: Body Weight Regulation and the Effects of Diet
Composition. Gastroenterology. 2017; 152: 1718-1727.e3.
doi:10.1053/j.gastro.2017.01.052.
[111] Gardner CD, Trepanowski JF, Del Gobbo LC, Hauser ME, Rigdon J, Ioannidis JPA, Desai
M, King AC. Effect of Low-Fat vs Low-Carbohydrate Diet on 12-Month Weight Loss in
Overweight Adults and the Association With Genotype Pattern or Insulin Secretion: The
DIETFITS Randomized Clinical Trial. JAMA. 2018; 319: 667-79. doi:10.1001/jama.2018.0245.
[112] Helms ER, Zinn C, Rowlands DS, Brown SR. A systematic review of dietary protein
during caloric restriction in resistance trained lean athletes: a case for higher intakes. Int J
Sport Nutr Exerc Metab. 2014; 24: 127-38. doi:10.1123/ijsnem.2013-0054.
[113] Kephart WC, Pledge CD, Roberson PA, Mumford PW, Romero MA, Mobley CB, Martin
JS, Young KC, Lowery RP, Wilson JM, Huggins KW, Roberts MD. The Three-Month Effects of a
Ketogenic Diet on Body Composition, Blood Parameters, and Performance Metrics in
CrossFit Trainees: A Pilot Study. Sport (Basel, Switzerland) 2018; 6.
doi:10.3390/sports6010001.
[114] Vargas S, Romance R, Petro JL, Bonilla DA, Galancho I, Espinar S, Kreider RB, BenítezPorres
J. Efficacy of ketogenic diet on body composition during resistance training in trained
men: a randomized controlled trial. J Int Soc Sports Nutr. 2018; 15: 31. doi:10.1186/s12970-
018-0236-9.
[115] Dobbins B. Keeping Score: A Look at the IFBB Judging System. BodybuildingCom 2004.
https://www.bodybuilding.com/fun/billdobbins1.htm (accessed July 23, 2018).
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 39
[116] Mitchell L, Hackett D, Gifford J, stermann F, O’Connor H. Do Bodybuilders Use
Evidence-Based Nutrition Strategies to Manipulate Physique? Sport. 2017; 5: 76.
doi:10.3390/sports5040076.
[117] Costill DL, Coté R, Fink W. Muscle water and electrolytes following varied levels of
dehydration in man. J Appl Physiol 1976; 40: 6-11.
[118] Helms ER, Aragon AA, Fitschen PJ. Evidence-based recommendations for natural
bodybuilding contest preparation: nutrition and supplementation. J Int Soc Sports Nutr.
2014; 11: 20. doi:10.1186/1550-2783-11-20.
[119] Spendlove J, Mitchell L, Gifford J, Hackett D, Slater G, Cobley S, O'Connor H. Dietary
Intake of Competitive Bodybuilders. Sports Med. 2015; 45: 1041-63. doi:10.1007/s40279-
015-0329-4.
[120] Goforth HW, Laurent D, Prusaczyk WK, Schneider KE, Petersen KF, Shulman GI. Effects
of depletion exercise and light training on muscle glycogen supercompensation in men. Am J
Physiol Endocrinol Metab. 2003; 285: E1304-11. doi:10.1152/ajpendo.00209.2003.
[121] Olsson KE, Saltin B. Variation in total body water with muscle glycogen changes in
man. Acta Physiol Scand. 1970; 80: 11-8. doi:10.1111/j.1748-1716.1970.tb04764.x.
[122] Shiose K, Yamada Y, Motonaga K, Sagayama H, Higaki Y, Tanaka H, Takahashi H.
Segmental extracellular and intracellular water distribution and muscle glycogen after 72-h
carbohydrate loading using spectroscopic techniques. J Appl Physiol. 2016; 121: 205-11.
doi:10.1152/japplphysiol.00126.2016.
[123] Sejersted, O., Hargens, A. R., Kardel, K. R., Blom, P., Jensen, O., & Hermansen, L.
Intramuscular fluid pressure during isometric contraction of human skeletal muscle. J Appl
Physiol. 1984; 56: 287-295.
ACCEPTED MANUSCRIPT
ACCEPTED
M
ANUSCRIPT
Carbohydrate Restriction 40
[124] Balon TW, Horowitz JF, Fitzsimmons KM. Effects of carbohydrate loading and weightlifting
on muscle girth. Int J Sport Nutr. 1992; 2: 328-34.
[125] Robinson SL, Lambeth-Mansell A, Gillibrand G, Smith-Ryan A, Bannock L. A nutrition
and conditioning intervention for natural bodybuilding contest preparation: case study. J Int
Soc Sports Nutr 2015; 12: 20. doi:10.1186/s12970-015-0083-x.
[126] Bamman MM, Hunter GR, Newton LE, Roney RK, Khaled MA. Changes in body
composition, diet, and strength of bodybuilders during the 12 weeks prior to competition. J
Sports Med Phys Fitness. 1993; 33: 383-91.
[127] Nygren AT, Karlsson M, Norman B, Kaijser L. Effect of glycogen loading on skeletal
muscle cross-sectional area and T2 relaxation time. Acta Physiol Scand. 2001; 173: 385-90.
doi:10.1046/j.1365-201X.2001.00913.x.
[128] MacDougall JD, Ward GR, Sale DG, Sutton JR. Biochemical adaptation of human
skeletal muscle to heavy resistance training and immobilization. J Appl Physiol. 1977; 43:
700-3.
[129] Schoenfeld BJ, Ogborn D, Krieger JW. Dose-response relationship between weekly
resistance training volume and increases in muscle mass: A systematic review and metaanalysis.
J Sports Sci. 2016: 1-10. doi:10.1080/02640414.2016.1210197.
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Carbohydrate Restriction 41
Figure Legends
Figure 1: The coordinated effect of resistance exercise, nutrient intake, and hormonal responses to
resistance exercise that regulate and facilitate muscle protein turnover rates. Insulin receptor;
Insulin receptor substrate-1 (IRS-1); insulin growth factor-1 (IGF-1); phosphorylation (P);
phosphatidylinositol-3-kinase (PI3-K); protein kinase B (Akt); mitogen-activated protein kinase
(MAPK); Akt substrate of 160 kDa (AS160); glucose transporter type 4 (GLUT-4); forkhead box
protein family (FOXOs); muscle atrophy F-box protein (MAFbx); muscle ring factor-1 (MuRF-1);
mechanistic target of rapamycin complex-1 (mTORC1); phosphatidic acid (PA); diacylglycerol zeta
(DGKζ); amino acid transporter (AAT); Ras homolog, mTORC1 binding (Rheb); the ubiquitin
proteasome system (UPS); 5′ adenosine monophosphate-activated protein kinase (AMPK); tuberous
sclerosis complex (TSC). Adapted from (Cleasby et al., 2016; Escobar, VanDusseldorp, & Kerksick,
2016; Goodyear et al, 1998; Röckl, Witczak, & Goodyear, 2008).