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REVIEW
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Beyond muscle hypertrophy: why dietary protein is important
for endurance athletes1
Daniel R. Moore, Donny M. Camera, Jose L. Areta, and John A. Hawley
Abstract: Recovery from the demands of daily training is an essential element of a scientifically based periodized program
whose twin goals are to maximize training adaptation and enhance performance. Prolonged endurance training sessions induce
substantial metabolic perturbations in skeletal muscle, including the depletion of endogenous fuels and damage/disruption to
muscle and body proteins. Therefore, increasing nutrient availability (i.e., carbohydrate and protein) in the post-training
recovery period is important to replenish substrate stores and facilitate repair and remodelling of skeletal muscle. It is well
accepted that protein ingestion following resistance-based exercise increases rates of skeletal muscle protein synthesis and
potentiates gains in muscle mass and strength. To date, however, little attention has focused on the ability of dietary protein to
enhance skeletal muscle remodelling and stimulate adaptations that promote an endurance phenotype. The purpose of this
review is to critically discuss the results of recent studies that have examined the role of dietary protein for the endurance
athlete. Our primary aim is to consider the results from contemporary investigations that have advanced our knowledge of how
the manipulation of dietary protein (i.e., amount, type, and timing of ingestion) can facilitate muscle remodelling by promoting
muscle protein synthesis. We focus on the role of protein in facilitating optimal recovery from, and promoting adaptations to
strenuous endurance-based training.
Key words: endurance exercise, cell signalling, training adaptation, muscle protein synthesis, dietary protein, remodelling,
recovery.
Résumé : La récupération consécutive aux dépenses suscitées par l’entraînement quotidien est un élément essentiel d’un
programme scientifique de périodisation dont le double objectif est de maximiser l’adaptation à l’entraînement et d’améliorer
la performance. Les séances d’entraînement prolongé en endurance suscitent d’importantes perturbations métaboliques dans le
muscle squelettique notamment la déplétion des carburants endogènes et les lésions/dommages aux muscles et aux protéines
organiques. Il est donc important d’accroître la disponibilité des nutriments (hydrates de carbone et protéines) durant la période
de récupération postexercice afin de refaire les réserves de substrats et faciliter la réparation et le remodelage du tissu musculaire squelettique. Il est généralement admis que l’ingestion de protéines après une séance d’exercices contre résistance accroît
le taux de synthèse des protéines du muscle squelettique et potentialise le gain de masse et de force musculaires. Jusqu’à ce jour,
cependant, il y a peu d’études sur le rôle des protéines alimentaires dans l’amélioration du remodelage du muscle squelettique
et la stimulation de l’adaptation à un phénotype d’endurance. Cette analyse documentaire se propose de traiter de façon critique
les résultats des études récentes sur le rôle des protéines alimentaires chez l’athlète d’endurance. Notre principal objectif est de
prendre en compte les résultats des recherches contemporaines qui ont amélioré nos connaissances sur l’utilisation des
protéines alimentaires (quantité, type et moment de l’ingestion) pour promouvoir la synthèse des protéines musculaires dans le
remodelage du muscle. On met l’accent sur le rôle des protéines pour faciliter la récupération optimale et favoriser les
adaptations à un entraînement intense en endurance. [Traduit par la Rédaction]
Mots-clés : exercice d’endurance, signalisation cellulaire, adaptation à l’entraînement, synthèse des protéines musculaires,
protéines alimentaires, remodelage, récupération.
Introduction
Appropriate recovery from the stress of exercise is an essential
component of any periodized program aimed at maximizing
training-induced physiological adaptations and enhancing athletic performance. Prolonged, sustained endurance training
sessions exert significant metabolic demands that include the depletion of endogenous fuel stores (e.g., liver and muscle glycogen),
loss of body fluid and electrolytes, hormonal perturbations, and
damage/disruption to skeletal muscle and body proteins. As
such, recovery strategies for competitive athletes engaged in
endurance-based training typically focus on 3 inter-related approaches: refuelling, rehydration, and repair. Given the high energy demands of daily endurance training (Stepto et al. 2002),
many athletes recognize the importance of replenishing fuel
stores through suitable postexercise carbohydrate ingestion protocols (Burke et al. 2004). In addition, there is an awareness of the
role that hydration and rehydration play in optimizing training
outcomes and performance (Murray 2007; Sawka et al. 2007). As
Received 18 December 2013. Accepted 3 February 2014.
D.R. Moore. Faculty of Kinesiology and Physical Education, University of Toronto, Toronto ON, M5S 2W6, Canada.
D.M. Camera and J.L. Areta. Exercise and Nutrition Research Group, Department of Exercise Sciences, Australian Catholic University, Fitzroy,
Victoria, Australia.
J.A. Hawley. Exercise and Nutrition Research Group, Department of Exercise Sciences, Australian Catholic University, Fitzroy, Victoria, Australia;
Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, UK.
Corresponding author: Daniel R. Moore (e-mail: [email protected]).
1This paper is a part of a Special Issue entitled Nutritional Triggers to Adaptation and Performance.
Appl. Physiol. Nutr. Metab. 39: 1–11 (2014) dx.doi.org/10.1139/apnm-2013-0591
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2
such, many competitive endurance athletes already appreciate
the need to refuel and rehydrate after training. However, 1 aspect
of the recovery process that is often neglected is the role of dietary
protein in providing the “building blocks” (i.e., amino acids) to
repair and regenerate damaged proteins as well as synthesize a
variety of new proteins (including both contractile myofibrillar
and energy producing mitochondrial proteins and associated enzyme complexes). It is this repair and remodelling of muscle proteins that provides the basis for many of the training-induced
adaptations that underpin the increases in muscle quality (i.e.,
mitochondrial density and (or) cross-sectional area) that ultimately lead to improved performance.
The importance of adequate dietary protein to enhance recovery from resistance-based exercise is well accepted and is a fundamental tenet of nutrition for muscle growth (Churchward-Venne
et al. 2012). Factors that influence the extent and magnitude of
muscle remodelling with resistance exercise include the amount,
type, and timing of protein ingestion (Burd et al. 2009). Only recently, however, has it been recognized that the results from studies of resistance-trained athletes may have relevance to athletes
training for and competing in endurance events. Accordingly, the
general purpose of this review is to summarize recent information on the importance of dietary protein for the endurance athlete with a focus on the role of protein in facilitating optimal
recovery from, and adaptation to, strenuous endurance training
Although a brief overview of the protein requirements of the
endurance athlete will be provided, our primary focus will be to
discuss the results from recent research that has advanced our
knowledge of specific aspects of increased protein availability
that facilitate muscle remodelling by promoting muscle protein
synthesis. Given the current lack of evidence regarding the impact
of protein ingestion on postexercise muscle remodelling (i.e., increasing muscle protein turnover) after endurance training, appropriate studies that have utilized resistance-based training will
be highlighted and placed into the context for the endurance
athlete.
Amino acids as a fuel
Carbohydrate (CHO)-based fuels (muscle and liver glycogen,
blood glucose, blood, muscle, and liver lactate) are the predominant energy for muscle contraction during continuous endurance
events lasting up to 2 h (Hawley and Hopkins 1995). In endurance
events lasting from 2–10 h (i.e., Ironman triathlon) there is still a
heavy reliance on CHO for oxidative metabolism, but fat-based
fuels (adipose and intramuscular triglycerides as well as bloodborne free fatty acids) play an increasingly important role in energy provision (Jeukendrup 2011). Because endogenous CHO stores
are limited, nutritional strategies to either slow their rate of oxidation during exercise and (or) increase their availability before
and (or) during exercise have received widespread scientific enquiry (Burke et al. 2011). However, amino acid oxidation (from free
amino acids in blood and liver pools as well as the protein stores
that are at equilibrium) can provide up to 10% of total energy
during endurance exercise (Tarnopolsky 2004). This enhanced oxidation arises to a significant extent from the breakdown of muscle proteins into their constituent amino acids (Howarth et al.
2010), which are subsequently released from the muscle for hepatic gluconeogenesis and (or) deaminated and oxidized within
the muscle mitochondria as a direct source of fuel (such is the
primary fate of the branched chain amino acids and especially
leucine) (Tarnopolsky 2004).
The oxidation of endogenous amino acids can be enhanced
by several factors, such as exercise intensity and (or) duration
(Haralambie and Berg 1976; Lamont et al. 2001), low muscle glycogen availability (Howarth et al. 2010; Lemon and Mullin 1980), a
habitually high-protein diet (i.e., ⬃1.8 g/(kg·day) (Bowtell et al.
1998), and sex (Phillips et al. 1993). Endurance training lowers the
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
maximal activity of branched-chain ketoacid dehydrogenase (the
rate-controlling enzyme for branched-chain amino acid oxidation) during exercise while also blunting the exercise-induced
stimulation of leucine oxidation (McKenzie et al. 2000), suggesting muscle from endurance-trained individuals has a refined
metabolism that can reduce its reliance on amino acids as an
alternative source of fuel. While the common practice of consuming CHO during endurance exercise attenuates amino acid oxidation, whole-body rates remain significantly elevated above rest
(Bowtell et al. 2000). Indeed, leucine, an amino acid with key
regulatory roles in protein metabolism (discussed subsequently),
can be oxidized at a rate of ⬃8 mg/(kg·h) in endurance athletes
performing moderate-intensity (⬃60% of maximal aerobic power
(V̇O2max)) continuous exercise (Bowtell et al. 1998), resulting in an
estimated total body leucine loss of ⬃1.2 g over 2 h. Assuming
muscle protein is ⬃9% leucine (Burd et al. 2013), this could mean
the equivalent of ⬃13 g of protein is catabolized during this type
of exercise. Paradoxically, despite an exercise-induced increase in
leucine oxidation, there is little effect of this extra protein demand on 24-h net leucine balance during acute metabolic trials
(Forslund et al. 1999). These data suggest that over the course of a
day metabolic accommodation may occur to spare net leucine
loses, perhaps through an attenuated postexercise leucine oxidation (Devlin et al. 1990). However, for the athlete who trains on a
daily basis (or on several occasions in a single day) and (or) who is
targeting an optimal recovery strategy that aims to meet or exceed net leucine (protein) balance, this potential accommodation
in protein metabolism may not be ideal to support their long-term
training goals. Given that oxidized amino acids (and especially the
essential amino acid leucine) are essentially lost from the body
and do not contribute to the increased muscle protein synthesis
observed during recovery, they must ostensibly be replaced
through dietary sources.
Protein requirements of endurance athletes
Energy balance
Current population requirements for protein to maintain nitrogen balance are set at 0.8 g/(kg·day). However, active persons,
particularly athletes involved in strenuous endurance and resistance training, have a greater daily protein requirement than
their sedentary counterparts. As such, these individuals need to
ingest more dietary protein to reach nitrogen balance (Phillips
et al. 1993; Tarnopolsky et al. 1988). Indeed, it has been suggested
that the protein needs of such athletes may be ⬃40%–100% greater
than the current recommended dietary allowance (Tarnopolsky
2004). This increased protein requirement is thought to reflect the
enhanced amino acid oxidation that occurs during exercise in
these athletes (Tarnopolsky 2004). However, the importance of
maintaining nitrogen balance in athletes has been questioned,
given that it has little direct link to any performance measure or
even lean muscle mass per se (Phillips 2006; Phillips et al. 2007;
Tipton and Witard 2007). Moreover, the majority of endurancetrained athletes are likely meeting their total daily energy
requirements and therefore probably ingest protein in amounts
that are already higher than the minimal recommended levels
(Tarnopolsky 2004). As discussed subsequently, the type of protein
and the timing of intake are likely to play more important roles in
maximizing recovery from, and adaptation to, endurance training than merely meeting or exceeding current protein recommendations on a daily basis (Tarnopolsky 2004)).
Negative energy balance
During periods of intensified training and (or) voluntary weight
loss (i.e., whole-body energy restriction), endurance athletes are
faced with a period of reduced energy availability (Loucks 2007).
The mismatch between energy intake and energy expenditure can
lead to a reduction in total body mass, especially lean body (i.e.,
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Moore et al.
muscle) mass. The implications of a loss of lean tissue on training
capacity and (or) performance outcomes are obvious. Furthermore if this reduced energy intake does not replenish muscle (and
liver) glycogen stores prior to subsequent training sessions, there
is likely to be an increased muscle catabolism and amino acid
oxidation during subsequent exercise (Howarth et al. 2010), which
would ultimately necessitate a greater dietary intake of the oxidized amino acids (e.g., leucine) to replenish these amino acid
stores. Studies in nonathletic populations (Josse et al. 2011;
Pasiakos et al. 2013) and with different training modalities (i.e.,
resistance exercise) (Mettler et al. 2010) show that providing dietary protein at levels in excess of recommended dietary allowances attenuates the loss of lean body mass during periods
of reduced energy availability; this strategy appears to have
preliminary support in athletes involved in endurance sports
(Haakonssen et al. 2013). While the protein requirements of endurance athletes during periods of deliberate negative energy balance has not been systematically investigated, it is likely that
these individuals would benefit from higher dietary protein availability (Tipton and Witard 2007), similar to resistance-trained athletes (Helms et al. 2013). However, any additional dietary protein
intake should not be at the expense of achieving adequate CHO
goals, which are essential if an athlete aims to maintain training
quality (i.e., intensity) and performance (Jarvis et al. 2002;
Macdermid and Stannard 2006).
Exercise-induced skeletal muscle remodelling
Skeletal muscle is a highly plastic tissue undergoing constant
remodelling through the continuous and simultaneous processes
of muscle protein synthesis (MPS) and muscle protein breakdown.
The net balance between these 2 processes (“turnover”) ultimately
determines whether skeletal muscle tissue is increasing (hypertrophy) or decreasing (atrophy) total protein content (Rennie et al.
2004; Burd et al. 2009). In the case of athletes training for endurance sports, muscle remodelling is essential to break down old
and (or) damaged protein and resynthesize new functional proteins. Whether this energetically costly process represents a net
expansion of a specific protein pool may be of relative inconsequence (e.g., myofibrillar proteins) or may be a targeted training
outcome (e.g., increased mitochondrial biogenesis). Nevertheless,
the pre-eminence of the stimulation of muscle protein synthesis
is that qualitative changes in the synthesis of muscle protein
fractions (e.g., force-generating myofibrillar proteins vs. energyproducing mitochondrial proteins) provides insight into the ultimate adaptive response to training (e.g., larger vs. more fatigue
resistant muscles) (Wilkinson et al. 2008).
Numerous studies have reported increases in mixed muscle
protein synthesis following a single bout (Harber et al. 2010;
Mascher et al. 2011) of exercise, and both short-term (i.e., 4 weeks)
(Pikosky et al. 2006) and chronic (i.e., 4 months) (Short et al. 2004)
endurance training. Such increases in mixed muscle protein synthesis likely reflect enhanced remodelling of muscle proteins that
may include mitochondrial-related proteins/enzymes, angiogenic
proteins (e.g., endothelial and smooth muscle cells within capillaries), and myofibrillar proteins. The cellular mechanism(s) underlying the observed increases in muscle protein synthesis
following endurance exercise training have only recently begun
to be explored. In this regard, the downstream target of rapamycin complex 1 (mTORC1) intracellular signalling cascade is an
important contraction- and nutrient-stimulated pathway that regulates translation initiation and subsequent protein synthesis in
skeletal muscle (Drummond et al. 2009; Dickinson et al. 2011).
Endurance exercise in the form of either prolonged, constant
loading, or higher intensity repeated sprints stimulates mTORC1
signalling independent of protein feeding (Benziane et al. 2008;
Coffey et al. 2011; Mascher et al. 2007). Indeed, we have previously
shown a similar time course for mTOR-mediated signalling during
3
the early (60-min) recovery period between resistance and endurance exercise (Camera et al. 2010). Regardless, activation and subsequent upregulation of aspects of the cell signalling machinery
regulating protein synthesis after endurance-based exercise is a
necessary prerequisite for the increased gene translation and
subsequent protein expression that ultimately generates the
exercise-induced phenotype associated with this type of training.
However, additional work is necessary to elucidate the appropriate molecular “signature” that may translate into altered rates of
muscle protein synthesis, as there are some reports of a dissociation between these acute “snapshot” markers of kinase activity
and kinetic subsequent protein remodelling (Greenhaff et al.
2008; Wilkinson et al. 2008).
Dietary protein to enhance rates of muscle protein
synthesis
The ingestion of dietary amino acids enhances muscle protein
synthesis during recovery from resistance-based exercise (Burd
et al. 2009). This enhanced exercise-induced increase in protein
synthesis, which may persist for up to 72 h (Cuthbertson et al.
2006; Miller et al. 2005), facilitates the skeletal muscle remodelling process that can ultimately enhance training-induced gains
in lean body mass (Cermak et al. 2012). In addition, recent work
has demonstrated that protein ingestion can also increase the
rates of muscle protein synthesis after prolonged, strenuous
endurance exercise (Breen et al. 2011; Howarth et al. 2009;
Levenhagen et al. 2002; Lunn et al. 2012) (see Table 1). Therefore,
general nutritional guidelines to enhance recovery from exercise,
regardless of the modality, recommend the intake of protein to
maximize postexercise rates of muscle protein synthesis (Phillips
and van Loon 2011). In this regard, recent research has provided
specific information relating to the most effective nutritional
strategies that enhance muscle protein remodelling after exercise
and have determined that the amount, type, and timing of protein
ingestion can all impact the extent and magnitude of postexercise
skeletal muscle remodelling (Fig. 1); these tenants of periodized
protein ingestion are discussed subsequently. Given the lack of
studies that have directly evaluated the factors related to dietary
protein ingestion after endurance exercise, our discussion will
draw on the results from the resistance training literature and,
where appropriate, contrast them with the demands of the endurance athlete.
Amount of protein
One of the most important nutritional considerations that facilitate an increase in the rates of muscle protein synthesis is the
amount of protein consumed. Both mixed muscle and myofibrillar protein synthetic rates are enhanced after resistance exercise
with small (5–10 g) amounts of protein (Moore et al. 2009; Tang
et al. 2007), but are further augmented after the ingestion of
larger (20 g) protein feedings (Moore et al. 2009; Witard et al. 2014).
Rates of MPS plateau at around 20 g of ingested protein with
additional quantities (up to 40 g) failing to stimulate protein synthesis further, at least not statistically (Moore et al. 2009; Witard
et al. 2014). Rather, at these larger protein intakes, there are increases in amino acid oxidation and urea production (Moore et al.
2009; Witard et al. 2014). While these data appear robust for athletes in energy balance, we have preliminary data to suggest that
protein requirements to elicit maximal rates of muscle protein
synthesis may be higher (i.e., >20 g) for athletes in energy deficit
(Areta et al. 2014). To the best of our knowledge, no study has
systematically determined the dose–response characteristics to
protein ingestion following endurance exercise. However, muscle
protein synthesis can be increased after endurance exercise with
as little as 10 g of protein (Levenhagen et al. 2002), with the repeated ingestion of small (10 g) amounts of protein immediately
and 30 min after a single bout of endurance exercise enhancing
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Study
(reference)
Subjects
V̇O2max
(mL/(kg·min)) Exercise stimulus
8 males,
⬃53
recreationally
active
Howarth et al. 2009 6 males,
48.9±3.3
recreationally
active
Harber et al. 2010
Lunn et al. 2012
8 males,
53.1±1.6
recreationally
active
8×5 reps at 80% 1RM,
0.5 h cycling at 70%
V̇O2max
10×6-s maximal
sprints, 54 s recovery
1 h cycling at ⬃70%
V̇O2max
2 h variable intensity
cycling at 50%–80%
V̇O2max
45 min treadmill at 65%
V̇O2max
1.5 h cycling at ⬃70%
V̇O2max
Protein type
Control condition
Outcome
10.2 g protein and
25.4 g CHO at 0
and 0.5 h of recovery
25 g protein at
0 h of recovery
Whey
25.2 g CHO at 0 and
0.5 h of recovery
Myofibrillar FSR
(0–4 h recovery)
1.25 (0.25–2.15)
Whey
Fasted
(no nutrition)
Myofibrillar FSR
(1–4 h recovery)
0.88 (−0.19–1.85)
24 g protein,
4.8 g leucine,
50 g CHO
⬃27 g protein,
62 g CHO, and ⬃2 g fat
at 0 and 1 h of recovery
0.4 g/(kg·h) protein
and 1.2 g/(kg·h)
CHO (at 15-min intervals)
from 0–3 h recovery
16 g protein/58 g CHO
at 0 h of recovery
Whey
Fasted
(no nutrition)
Myofibrillar FSR
(0–4 h recovery)
0.99 (−0.10–1.97)
Milk (20% whey, Fasted
80% casein)
(no nutrition)
Mixed muscle FSR
(2–6 h recovery)
0.49 (−0.53–1.46)
10.2 g protein and
25.4 g CHO at 0 and
0.5 h of recovery
25 g protein at
0 h of recovery
8×5 reps at 80% 1RM,
0.5 h cycling at 70%
V̇O2max
10×6-s maximal
24 g protein,
sprints, 54 s of recovery
4.8 g leucine,
50 g CHO
Whey
1.6 g/(kg·h) CHO (at
Mixed muscle FSR
15-min intervals)
(0–4 h recovery)
from 0–3 h recovery
Milk (20% whey, 74 g CHO at 0 h of
80% casein)
recovery
MPS ES* (95% CI)
1.51 (0.13–2.65)
Mixed muscle FSR
(0–3 h recovery)
0.79 (−0.27–1.76)
Mean ES (95% CI)
0.95 (0.53–1.38)
Whey
25.2 g CHO at 0 and
0.5 h of recovery
Mitochondrial FSR −0.15 (−1.02–0.74)
(0–4 h recovery)
Whey
Fasted
(no nutrition)
Mitochondrial FSR 0.34 (−0.67–1.31)
(1–4 h recovery)
Whey
Fasted
(no nutrition)
Mitochondrial FSR 0.08 (−0.91–1.05)
(0–4 h recovery)
Note: 1RM, 1-repetition maximum; CI, confidence interval; CHO, carbohydrate; FSR, fractional synthetic rate; V̇O2max, maximal aerobic capacity.
*MPS ES: muscle protein synthesis effect size of protein ingestion relative to control condition.
†D.M Camera, D.W.D. West, S.M. Phillips, T. Rerecich, T. Stellingwerff, J.A. Hawley, and V.G. Coffey. Unpublished.
Mean ES (95% CI)
0.07 (−0.48–0.62)
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
Mitochondrial fractional synthetic rate
Breen et al. 2011
10 males,
66.5±5.1
endurance
trained
Camera et al.
8 males,
46.7±4.4
(unpublished)†
recreationally
active
Coffey et al. 2011
8 males,
51.3±5.6
trained
1.5 h cycling at
⬃70% V̇O2max
Nutritional
intervention
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Mixed muscle and myofibrillar FSR
Breen et al. 2011
10 males,
66.5±5.1
endurance
trained
Camera et al.
8 males,
46.7±4.4
(unpublished)†
recreationally
active
Coffey et al. 2011
8 males,
51.3±5.6
trained
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Table 1. Studies investigating the effects of protein ingestion on muscle protein synthesis after endurance or high-intensity sprint exercise.
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Fig. 1. Overview of the potential effects of protein ingestion on supporting the recovery from endurance-based exercise as means to enhance
endurance capacity and performance. Potential metchanisms include (i) oxidation of amino acids to be used for hepatic gluconeogenesis and
(or) deaminiation, or as a fuel source by skeletal muscle mitochondria; (ii) increases in mitochondrial protein synthesis to enhance substrate
metabolism and utilization; (iii) promotion of myofibrillar remodelling to maintain muscle protein quality and function by removing old or
damaged proteins; (iv) stimulation of net myofibrillar protein synthesis to enable greater muscle force/power output; and (v) promotion of
glycogen resynthesis when co-ingested with carbohydrate (CHO). The capacity for protein ingestion to modulate such adaptive signals may be
influenced by peripheral factors such as the timing, amount and type of protein intake. MPB, muscle protein breakdown; MPS, muscle protein
synthesis; ?, speculative/requires further research.
MPS: 20-25g
Amount Whole body net balance: >20g?
Dietary
Protein
Type
Timing
(Liver)
Gluconeogenesis
and/or direct
oxidaon
Decreased
MPB
Before: Reduce MPB during exercise?
During: Posive whole body net protein
balance?
Aer: Increased MPS to facilitate
muscle remodelling
(Muscle)
Myofibrils
Mitochondria
Amino Acid
Metabolism
Rapidly digested, leucine-enriched
proteins sources (whey)?
Remodelling/
Synthesis (?)
Increased energy
producon and
substrate ulizaon?
Remodelling
Breakdown + Repair
of old/damaged
proteins
Energy storage
Net Synthesis
Enhanced muscle
power output?
Glycogen
Resynthesis
Co-ingeson with
CHO to increase
resynthesis
Increased Recovery and
Endurance Adaptaon/ Performance ?
the rates of synthesis of the force-generating myofibrillar proteins
(Breen et al. 2011). Of note is that protein ingestion has little effect
on the ability to augment postexercise rates of mitochondrial
protein synthesis (Table 1), which is in contrast to the ability of
exogenous amino acid provision to upregulate the protein synthetic machinery at rest (Bohe et al. 2003). Perhaps the preeminence of energy provision to support cell function and
survival and the dependence on a constant supply of ATP dictates
that mitochondrial protein synthesis is prioritized in the postexercise period with fasted levels of amino acid sufficient to support
the remodelling of this vital organelle (Moore and Stellingwerff
2012). Nevertheless, given that maximal rates of muscle protein
synthesis have been reported after the ingestion of 20–25 g of
protein both at rest and after resistance exercise (Cuthbertson
et al. 2005; Moore et al. 2009), it seems prudent to recommend
that similar amounts should also be consumed after endurance
exercise to facilitate postexercise muscle remodelling.
It is presently unclear whether exercise of longer duration (i.e.,
greater than 2 h) further increases the acute requirements of
protein at the whole-body level. However, given that there is significant oxidation of amino acids (especially leucine) during prolonged endurance exercise, this would seem likely. Furthermore,
intense bouts of endurance exercise result in a redistribution of
cardiac output, with a shunting of blood away from the digestive
system, and a resultant hypoxia-mediated small intestinal injury
(van Wijck et al. 2011). Such effects are likely to be exacerbated
with longer duration exercise bouts, particularly those undertaken in either hot/humid or hypoxic environments. Ultimately,
the net effect of any exercise-induced intestinal injury as well as
the increased protein catabolism and amino acid oxidation may
have on the acute protein requirements to whole-body protein
recovery is unclear. For example, in the study by Levenhagen et al (2002),
10 g of dietary protein was sufficient to enhance muscle protein
synthesis and induce a positive net muscle protein balance after
only 60 min of moderate intensity exercise, but failed to induce a
positive whole-body protein balance. This is similar to the observations of Lunn et al. (2012) who demonstrated that the ingestion
of 500 mL of chocolate-flavored milk (⬃16 g of protein) enhanced
mixed muscle protein synthesis despite a negative whole-body
protein balance. Collectively, these results suggest that dietary
amino acids are preferentially utilized to support greater rates of
MPS in the immediate postexercise period with remodelling of
whole-body proteins (including the gut) occurring as a secondary
process. Therefore, it is currently unclear if either a slightly
greater amount of protein or perhaps a greater number of repeat
feedings is necessary to rapidly and fully restore whole-body protein balance after endurance exercise.
Timing of protein ingestion
Before and during exercise
Protein and amino acid ingestion prior to a bout of repeated
sprints has been shown to support greater postexercise rates of
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6
myofibrillar protein synthesis (Coffey et al. 2011), which is generally consistent with findings from studies employing a resistanceexercise stimulus (Tipton et al. 2007). These results suggest that
the recovery from relatively short, high-intensity endurancebased exercise can be enhanced with pre-exercise protein ingestion. However, prolonged endurance exercise stimulates the
increased oxidation of amino acids (especially the branched chain
amino acids) as an alternative fuel source and can depress normal
rates of protein synthesis as a means to prioritize muscle energy
stores towards fuelling contraction rather than the energetically
expensive process of protein synthesis (Rose and Richter 2009). As
such, the exercise period represents a net catabolic environment,
which can lead to the breakdown of skeletal muscle proteins and
net efflux of amino nitrogen from the muscle (Howarth et al. 2010;
van Hall et al. 1999). Endurance athletes who undertake prolonged (i.e., >1 h) training bouts or who train multiples times per
day (not always in a glycogen-replete state) could subject their
muscles to prolonged periods of net catabolism that presently has
unknown consequences on the optimal enhancement of muscle
protein synthesis and whole body and muscle protein balance
during the postexercise recovery period.
Koopman and colleagues (2004) were the first to demonstrate
that protein/CHO co-ingestion during prolonged endurance exercise in trained athletes resulted in a greater whole-body protein
oxidation compared with CHO alone. At the time it was suggested
that the greater oxidation was reflective of a greater use of dietary
as compared with body amino acids as a source of fuel, which
ultimately resulted in a more positive whole-body net protein
balance during exercise (Koopman et al. 2004). With respect to
local effects within the muscle, protein/CHO co-ingestion may
attenuate the typical exercise-induced increase muscle protein
breakdown as reflected by a decrease in amino acid release from
the muscle and a subsequently less negative net muscle protein
balance during exercise (Hulston et al. 2011). Collectively these
data suggest that athletes performing prolonged, strenuous training could benefit from the co-ingestion of protein in their daily
nutrition plan to limit the catabolic environment of exercise,
which ultimately may position them in a greater nutritional position during the postexercise recovery period. However, protein
ingestion during exercise may be of limited ergogenic value (Betts
and Williams 2010; Saunders 2007). Therefore, additional research
is necessary to elucidate the potential advantage of an attenuated
endogenous protein catabolism (either of muscle or whole body
stores) on supporting long-term training goals that are dependent
on the remodelling of skeletal muscle tissue.
Immediate (<3 h) postexercise recovery
Consistent with reports from the resistance exercise literature
(Burd et al. 2009), dietary protein ingestion after endurance exercise increases postexercise muscle protein synthesis, possibly as a
means to facilitate muscle remodelling and support the recovery
process (Breen et al. 2011; Howarth et al. 2009; Levenhagen et al.
2002; Lunn et al. 2012). This is evident in the moderate to large
effect sizes on mixed and myofibrillar (but not mitochondrial)
protein synthesis after protein ingestion compared with CHO
alone (Table 1). In contrast to the relatively prolonged (i.e., ≥24 h)
sensitivity of skeletal muscle to dietary amino acids induced by a
bout of resistance exercise (Burd et al. 2011), the immediate postexercise recovery period may be relatively important for enhancing muscle protein synthesis and net protein balance after
endurance compared with resistance exercise. For example, delaying the ingestion of 10 g of dairy-based protein by 3 h markedly
attenuates the anabolic effect of the dietary protein and fails
to enhance postexercise mixed muscle protein synthesis (Levenhagen
et al. 2001). Moreover, protein ingestion after training may be
especially important for athletes chronically consuming highprotein diets (i.e., >1.8 g/(kg·day)) as postexercise rates of mixed
muscle protein synthesis in the fasted state have been reported to
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
be suppressed relative to lower protein diets (Bolster et al. 2005).
This lower protein synthetic response after exercise in the fasted
state may be secondary to a diet-induced upregulation of amino
acid oxidative capacity, which subsequently may result in a reduced intracellular availability of amino acids for the repair and
remodelling of muscle tissue in the absence of an exogenous dietary source (Bolster et al. 2005; Gaine et al. 2007). Therefore,
while additional studies need to address the importance of protein timing after endurance exercise, in light of current evidence
of an attenuation of protein synthesis when feeding is delayed by
several hours (Levenhagen et al. 2001) the ingestion of dietary
protein in the first 30–60 min after endurance exercise should be
recommended to maximize rates of skeletal muscle protein synthesis and enhance recovery.
Prolonged (>3 h) postexercise recovery
In addition to the immediate postexercise recovery period
(i.e., ≤3 h), we have recently determined how feeding during a
prolonged (12 h) recovery period postexercise might further
support muscle remodelling. After a single bout of resistance exercise, undertaken in the morning, we found that rates of myofibrillar protein synthesis and whole-body net protein balance were
greater over a 12 h day when athletes consumed 20 g of protein
every 4 h as compared with isoenergetic amounts given as 2 × 40 g
every 6 h (typical of a 3-square meals approach) or multiple small
feeding 8 × 10 g of every 1.5 h (typical of a “grazing” pattern of
eating) (Areta et al. 2013; Moore et al. 2012). These data clearly
show that it is not just the quantity of protein an athlete consumes that is important for chronic muscle remodelling but the
pattern of protein ingestion. Given the importance of dietary protein for enhancing muscle protein synthesis after endurancebased exercise (Table 1), it is likely that athletes training and
competing in these activities would also benefit from a balanced
daily protein ingestion (i.e., repeated meal feedings of ⬃20 g of
protein every 3–4 h) to maximize their postexercise recovery. In
fact, given that small 10-g protein feeding appears to have little
effect on enhancing muscle rates of protein synthesis and net
protein balance 3 h after endurance exercise (Levenhagen et al.
2001), the balanced ingestion of sufficient protein intake (i.e., several 20-g feedings) may be even more critical to sustain maximal
rates of muscle protein remodelling in endurance athletes. This
pattern of meal-feeding to sustain daily rates of muscle protein
remodelling is likely also beneficial for athletes who are in negative energy balance and who wish to maintain lean mass while
losing fat mass, as has been suggested with other athletes during
periods of weight loss (Iwao et al. 1996).
Type of protein
Dietary proteins differ in their amino acid composition and
rates of digestion and absorption (i.e., the rate of appearance of
their constituent amino acids in the blood) (Boirie et al. 1997;
Pennings et al. 2011, 2012), both of which have been reported to
have measurable effects on the ability to enhance postexercise
muscle protein synthesis (Burd et al. 2009). From the standpoint of
nutritional protein quality, as characterized by the current reference criteria of protein-digestibility corrected amino acid score
(PDCAAS; for overview of definition and limitations, see
Schaafsma 2000), commonly recommended proteins for athletes
such as the dairy proteins whey and casein and the plant-based
protein soy are all considered “high quality” proteins (i.e.,
PDCAAS >1). However, given that muscle protein synthesis is primarily
regulated by the EAA content of a protein (Tipton et al. 1999a,
1999b), it is becoming evident that subtleties of dietary protein
characteristics can lead to differences in their ability to support
maximal rates of MPS after exercise and ultimately adaptation to
training (Phillips et al. 2009). For example, compared with casein
and soy sources of protein, whey protein has distinct anabolic
characteristics that result in a greater feeding-induced stimulaPublished by NRC Research Press
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Moore et al.
tion of muscle protein synthesis: this premise is true when ingested both at rest and after resistance exercise (Tang et al. 2009),
although blends of these protein sources have also been shown to
have efficacy for supporting postexercise muscle protein synthesis (Reidy et al. 2013). Nevertheless, a growing body of evidence has
implicated the essential amino acid leucine as a likely mediator of
this enhanced anabolic response with whey protein because of its
ability to “switch on” the cell signalling machinery governing
protein synthesis and serve as a substrate for protein synthesis
(Drummond et al. 2008; Phillips and van Loon 2011). Moreover,
independent of its amino acid profile, the rate at which a protein
is digested and its ability to induce rapid aminoacidemia and
leucinemia can modulate the extent of muscle remodelling as
evident by the greater stimulation of myofibrillar protein synthesis after resistance exercise with ingestion of 25 g of whey protein
as a single bolus as compared with an equivalent amount of whey
protein ingested as multiple small repeated pulses (West et al.
2011). This greater stimulatory effect of rapid aminoacidemia
should be considered with athletes who wish to rapidly increase
muscle protein synthesis after an exercise bout with whole foods
as protein sources in liquid form are more rapidly digested than
those in solid food matrices (Burke et al. 2012). Therefore, although studies directly comparing different protein sources during the recovery from endurance exercise are currently lacking,
athletes who wish to enhance muscle protein synthesis during the
early recovery process would meet these goals with the ingestion
of rapidly digested, leucine-enriched proteins sources such as
whey (Breen et al. 2011).
Concurrent training
It is not uncommon for athletes training for endurance sports
to engage in resistance training to specifically enhance muscle
strength, power and (or) resistance to fatigue (Aagaard and
Andersen 2010). Conversely, athletes from the majority of team
sports often have physiological demands that require a combination of strength, a high lean mass, and superior endurance and
(or) sprint/power capacity to be successful in their discipline
(Bishop et al. 2011). As such, many athletes from a spectrum of
sports engage in concurrent training whereby both resistance and
endurance-based training sessions are performed either in a single session or during separate sessions during the same day.
Classic early studies investigating adaptation responses to concurrent training clearly demonstrated an “interference” in training adaptation when resistance and endurance training were
combined compared with when the resistance or endurance
workouts were performed in isolation (Dudley and Djamil 1985;
Hickson 1980). Potential molecular mechanisms explaining these
attenuated anabolic/strength adaptations with concurrent training have centred on alterations in muscle glycogen availability
and (or) activation of the cellular energy sensor AMP kinase
(AMPK) (Hawley 2009). However, we have reported little effect of
AMPK on anabolic cell signalling and rates of myofibrillar protein
synthesis in either the fasted (placebo ingestion) or fed (2 beverages at 0 and 2 h of recovery containing 20 g whey and 40 g CHO
each) state when trained subjects commenced a single bout of
strenuous resistance exercise (8 × 5 repetitions at 80% 1 repetition
maximum) with low (50% of resting, fed levels) muscle glycogen
(Camera et al. 2012). Thus, a causal relationship for reduced glycogen availability or AMPK-mediated attenuation of mTORC1 signalling in a concurrent training paradigm has yet to be established in
vivo human muscle.
Little research to date has examined the effect of protein ingestion in a concurrent training setting. We recently observed that
rates of myofibrillar, but not mitochondrial protein synthesis
were enhanced when 25 g whey protein (compared with a nonenergy placebo) was consumed following concurrent resistance and
endurance exercise (Camera et al., Table 1). Thus, protein inges-
7
tion may reduce the potential interference effect of endurance
exercise on skeletal muscle hypertrophy with chronic concurrent
training. Although less is known regarding the effects of protein
ingestion to augment endurance training-induced adaptations
(e.g., mitochondrial vs. myofibrillar protein synthesis) after concurrent training, whey protein has been shown to support rates of
mitochondrial protein synthesis following concurrent exercise
(Donges et al. 2012). However, in the absence of a protein-free
placebo in that study (Donges et al. 2012), it is unclear if the rates
of mitochondrial protein synthesis were indeed augmented by
protein ingestion or were simply enhanced by the exercise stimulus itself, similar to previous reports after endurance exercise
(Breen et al. 2011; Coffey et al. 2011; Wilkinson et al. 2008). Therefore, protein ingestion represents a practical means to increase
anabolic adaptations with concurrent exercise. Certainly increasing protein availability in these situations will not lead to diminished response–adaptations, although this is clearly a fertile area
of future research. Based on the ability of postexercise protein
ingestion to support increased rates of muscle protein synthesis
after a variety of exercises and in the absence of any plausible
evidence against, it seems prudent to recommend that athletes
involved in concurrent training modes follow similar protein
guidelines as for those athletes training solely for resistance and
power sports.
Benefits beyond muscle protein synthesis with
protein ingestion
Glycogen synthesis
As previously noted, CHOs are an important fuel for oxidative
metabolism during both repeated sprint-type training sessions
and less intense, prolonged workouts. In these situations, and in
the absence of exogenous CHO intake, muscle and liver glycogen
are the primary sources of fuel to support CHO oxidation. Even
when ingested at high rates (>1 g/min) during submaximal endurance exercise, the oxidation of blood glucose cannot be the sole
source of CHO by the working muscles (Coyle et al. 1986). As
endogenous CHO stores are limited to between 400–600 g of glycogen (depending on the athletes’ body mass and nutritional status), restoration of both muscle and liver glycogen is an important
consideration for the endurance athlete. Following prolonged endurance exercise, muscle glycogen is typically restored to preexercise levels within 24 h (Burke et al. 1995; Costill et al. 1981)
provided adequate (i.e., ⬃1.2 g/(kg·day)) postexercise carbohydrate
is ingested (Burke et al. 2011). However, for athletes who have do
not have access to adequate CHO and (or) have a smaller window
of opportunity in which refuelling can occur (i.e., multiple training sessions and (or) competitions in a day), alternate feeding
strategies have been explored to augment rates of glycogen resynthesis. One approach has been to augment normal CHO replenishment strategies with small amounts of protein as a means to
promote rapid rates of muscle glycogen resynthesis and maintain
subsequent exercise performance (Beelen et al. 2010).
It has been suggested that the increased insulin response with
the co-ingestion of protein and CHO may enhance glucose uptake
in the muscle via stimulation of glucose transporters, which ultimately would translate into a greater rate of muscle glycogen
resynthesis (van Loon et al. 2000a, 2000b). Indeed, leg glucose
uptake has been reported to be 3.5-fold higher following coingestion of protein and carbohydrate compared with CHO only
(Levenhagen et al. 2002). However, studies that have shown protein co-ingestion with carbohydrate augments muscle glycogen
synthesis during recovery have used feeding strategies that featured carbohydrate intakes that are suboptimal (<0.8 g/(kg·h)) for
maximal rates of glycogen synthesis (van Loon et al. 2000a;
Zawadzki et al. 1992). Indeed, co-ingestion of protein with CHO
does not appear to augment postexercise muscle glycogen synthesis rates when adequate amounts of carbohydrate (1.2 g/(kg·h)) are
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8
consumed (Burke et al. 2011; Jentjens et al. 2001). Therefore, athletes aiming to maximize fuel storage (i.e., muscle and liver glycogen resynthesis) should focus on attaining sufficient CHO
intake. Nonetheless, the co-ingestion of protein with CHO as a
means to replenish muscle glycogen stores may be of practical
importance in situations in which CHO cannot be consumed to
the optimal level (e.g., gastrointestinal distress, inadequate access
to CHO, etc.). Additionally, athletes engaging in multiple training
sessions a day with limited recovery times (e.g., <4 h) could benefit
from the co-ingestion of protein with CHO as a means to optimize
muscle glycogen concentrations as well as to provide amino acids
for the repair of muscle proteins.
Immune function
Periods of intensified training have been reported to predispose
athletes to a greater risk of developing upper respiratory tract
infections (Gleeson 2007), which may impair training quality and
alter the ability to recovery from illness. This increased susceptibility to opportunistic infection may be related in part to a
reduced immune surveillance characterized by attenuated circulating viral antigen-targeting CD8+ T-lymphocytes (Gleeson 2007;
Witard et al. 2012). However, a high (3 g/(kg·day)) but not a moderate (1.5 g/(kg·day)) protein diet restores the circulating concentration of these important immune cells to levels that are
comparable to those measured during normal training loads. Furthermore, higher protein intakes are associated with a reduction
in the self-reported incidence of upper respiratory tract infections
in athletes when undertaking intensified training loads (Witard
et al. 2012, 2013). In these studies (Witard et al. 2012, 2013) CHO
intake was lower than recommended levels for intense training
periods (i.e., ⬃6 vs >8 g/(kg·day), respectively) (Burke et al. 2011),
suggesting that in the absence of optimal CHO intake, protein
ingestion may improve markers of immune function (Nieman
1998) and help mitigate the risk of developing upper respiratory
infections in athletes. Future work is required to confirm these
initial positive findings and to elucidate their clinical significance in
maintaining athlete health.
Future perspectives
Dietary protein supplementation and muscle growth are inextricably linked. This is the product of a strength training culture
that promotes the use of protein supplements and a body of research that unequivocally supports increased protein availability
to enhance postexercise muscle protein synthesis and remodelling (Burd et al. 2009). In addition, a recent meta-analysis demonstrates that dietary protein supplementation is associated with
greater training-induced gains in lean mass growth and strength
increases (Cermak et al. 2012).
In contrast, our current understanding of the functional outcome of enhancing muscle protein synthesis during recovery
from endurance-based exercise is in its infancy: the role dietary
protein in supporting enhanced skeletal muscle remodelling has
only received recent scientific inquiry. Therefore, fundamental
questions of how optimal protein ingestion (i.e., amount, type,
timing) during and after endurance exercise can enhance muscle
recovery and subsequent adaptation to training need to be addressed. For example, although protein is able to enhance muscle
protein synthesis after endurance exercise, especially of the forcegenerating myofibrillar proteins (see Table 1), it is unclear if this
increased protein synthesis may translate into greater muscle
mass and (or) muscle power over a period of weeks to months;
such adaptations could be viewed as beneficial for endurance athletes involved in nonweight-bearing sports such as cycling, where
success is generally linked to an ability to sustain high power
outputs (Hawley and Noakes 1992). In contrast, despite a lack of
stimulation of mitochondrial protein synthesis with physiological (i.e., ⬃20 g) protein ingestion, the results from a number of
chronic (i.e., 4–6 weeks) studies have reported enhanced aerobic
Appl. Physiol. Nutr. Metab. Vol. 39, 2014
capacity after training with postexercise protein ingestion in
young (Ferguson-Stegall et al. 2011) and older adults (Robinson
et al. 2011). Replication of these results in well-trained endurance
athletes is warranted to elucidate the potential mechanisms for
these exercise-nutrient adaptations. Finally, although moderate
(i.e., ⬃20 g) protein ingestion appears to have little effect on the
postexercise increase in mitochondrial protein synthesis (Breen
et al. 2011), supplementation of the branched chain amino acids
(i.e., the equivalent of ⬃10 g/day) has been reported to increase
mitochondrial biogenesis and aerobic capacity in mice (D’Antona
et al. 2010). Whether similar results can be replicated in humans
remains to be determined. Preliminary evidence suggests that
high protein feeding (i.e., ⬃64 g over 3 h, a level that would exceed
the requirement to enhance muscle protein synthesis) during recovery from intense endurance exercise may elicit a gene expression profile that could be conducive to enhancing cellular energy
pathways (Rowlands et al. 2011). Therefore, future studies are
needed to elucidate the effect of maximizing muscle protein synthesis and the subsequent effects on altered gene expression profiles with optimal protein ingestion, and on the changes in muscle
mass, muscle quality, and (or) sports performance with prolonged
periods of supplementation (i.e., training). Additionally, the relevance of appropriate protein supplementation during periods of
energy deficit (as compared with energy balance) needs systematic exploration given the potential ergogenic benefits (e.g., reduced muscle soreness, enhanced exercise performance) that may
occur with periodized protein feeding during this compromised
nutritional state (Pasiakos et al. 2014).
Conclusion
The prevailing paradigm for the majority of athletes is that
dietary protein is for building muscle (i.e., hypertrophy). While a
vast body of research supports this “hypertrophy-centric” view,
recent research highlights a critical role for dietary protein in
supporting the recovery from endurance exercise. In addition to
the elevated protein requirements in this population, periodized
protein ingestion has been shown to augment the remodelling of
muscle and whole body proteins with endurance training. This
protein remodelling, which is primarily determined by changes in
muscle protein synthesis, is an important aspect of the acute recovery process after exercise that ultimately underpins the adaptations (e.g., greater muscle power, aerobic capacity) that accrue
with endurance training. While future research is required to
elucidate the most effective protein ingestion strategies to support and promote endurance training adaptations, the fact that
dietary protein provides the requisite building blocks for muscle
protein synthesis positions this macronutrient as a vital, and perhaps underappreciated, component of the endurance athlete’s
nutritional armour.
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