REVIEW ARTICLE
Periodized Nutrition for Athletes
Asker E Jeukendrup1
Published online: 22 March 2017
Ó The Author(s) 2017. This article is published with open access at Springerlink.com
Abstract It is becoming increasingly clear that adaptations,
initiated by exercise, can be amplified or reduced by
nutrition. Various methods have been discussed to optimize
training adaptations and some of these methods have been
subject to extensive study. To date, most methods have
focused on skeletal muscle, but it is important to note that
training effects also include adaptations in other tissues
(e.g., brain, vasculature), improvements in the absorptive
capacity of the intestine, increases in tolerance to dehydration,
and other effects that have received less attention
in the literature. The purpose of this review is to define the
concept of periodized nutrition (also referred to as nutritional
training) and summarize the wide variety of methods
available to athletes. The reader is referred to several other
recent review articles that have discussed aspects of periodized
nutrition in much more detail with primarily a focus
on adaptations in the muscle. The purpose of this review is
not to discuss the literature in great detail but to clearly
define the concept and to give a complete overview of the
methods available, with an emphasis on adaptations that
are not in the muscle. Whilst there is good evidence for
some methods, other proposed methods are mere theories
that remain to be tested. ‘Periodized nutrition’ refers to the
strategic combined use of exercise training and nutrition, or
nutrition only, with the overall aim to obtain adaptations
that support exercise performance. The term nutritional
training is sometimes used to describe the same methods
and these terms can be used interchangeably. In this
review, an overview is given of some of the most common
methods of periodized nutrition including ‘training low’
and ‘training high’, and training with low- and high-carbohydrate
availability, respectively. ‘Training low’ in
particular has received considerable attention and several
variations of ‘train low’ have been proposed. ‘Traininglow’
studies have generally shown beneficial effects in
terms of signaling and transcription, but to date, few
studies have been able to show any effects on performance.
In addition to ‘train low’ and ‘train high’, methods have
been developed to ‘train the gut’, train hypohydrated (to
reduce the negative effects of dehydration), and train with
various supplements that may increase the training adaptations
longer term. Which of these methods should be used
depends on the specific goals of the individual and there is
no method (or diet) that will address all needs of an individual
in all situations. Therefore, appropriate practical
application lies in the optimal combination of different
nutritional training methods. Some of these methods have
already found their way into training practices of athletes,
even though evidence for their efficacy is sometimes scarce
at best. Many pragmatic questions remain unanswered and
another goal of this review is to identify some of the
remaining questions that may have great practical relevance
and should be the focus of future research.
1 Introduction
The adaptive response to exercise training is determined by
a combination of factors: the duration, the intensity, and the
type of exercise as well as the frequency of training, but
also by the quality and quantity of nutrition in the pre- and
post-exercise periods. It is becoming increasingly clear that
adaptations, initiated by exercise, can be amplified or
& Asker E Jeukendrup
a.e.jeukendrup@lboro.ac.uk
1
School of Sport, Exercise and Health Sciences,
Loughborough University, Loughborough, Leicestershire
LE11 3TU, UK
123
Sports Med (2017) 47 (Suppl 1):S51–S63
DOI 10.1007/s40279-017-0694-2
dampened by nutrition. For example, it is well established
that in the absence of protein feeding post-exercise, net
protein synthesis is low and the muscle may actually be in
negative protein balance. There is also evidence that lowering
carbohydrate availability can promote specific
adaptations in the muscle. In contrast, high-dose antioxidant
supplementation has the potential to reduce training
adaptations [1–3]. Research has mostly focused on adaptations
in skeletal muscle. Critically, there are many
adaptations in other organs that are influenced by nutritional
intake and that are important to sports performance.
Such changes and their relevance for athletes are often
overlooked or have received significantly less attention.
Examples include, but are not limited to, the vasculature,
the brain, and the intestine. For example, there is evidence
of the upregulation of carbohydrate transporters in the
intestine in response to carbohydrate feeding and there are
alterations in gut micro flora in response to changes in diet.
Such changes could alter the delivery of nutrients and
potentially affect performance.
There are thus numerous interactions between nutrition
and exercise and numerous effects of nutrition per se that
ultimately determine long-term exercise performance outcomes.
From a practical point of view, it is important to
have an understanding of these interactions to optimize
specific adaptations that one might be interested in. There
are numerous reviews that have discussed aspects of this.
For example, several reviews have discussed the potential
benefits of training with low-carbohydrate availability
[4–6], some have discussed high-carbohydrate availability
or both [7, 8], others have discussed the potential impact of
antioxidants on mitochondrial biogenesis [9] or other
modulators of training adaptation [10]. The purpose of this
review is two fold: to clearly define the concept of periodized
nutrition, and to provide a holistic overview of the
methods that could fall under the umbrella term ‘periodized
nutrition’.
2 Historical Perspective
The links between diet and exercise have long been recognized.
In the late 1800s, the term training was used to
describe a regime that included diet as well as exercise, not
just exercise. Training was and is still often defined as ‘‘the
action of undertaking a course of exercise and diet in
preparation for a sporting event’’. At one point in history,
nutrition was such an important part of athletes’ preparation
that the definition of training was more related to diet
than the actual physical preparation itself. Below are some
excerpts from a book on training by Montague Shearman in
1887 [11].
‘‘To the athlete of early times, the essential part and
chief characteristic of training was not the taking of proper
preparatory exercise, but the sudden and violent change of
diet’’. ‘‘Going into training was taken to mean the commencement
of a peculiar diet of half-cooked beefsteaks and
dry bread and the reduction of the daily drink to a minimum,
and not to imply the beginning of the proper training
or cultivation of the muscles required for a race.’’
Although these practices themselves may not have stood
the test of time and may not be supported by scientific
evidence, it is clear that also in those early days, a clear
link was assumed between diet and exercise performance.
Although these effects aim at short-term performance
benefits, more recently, studies have focused on longer
term effects. It has been suggested that by careful planning
and integration of nutrition and training, the longer term
training adaptations might be improved. The terms ‘periodized
nutrition’ and ‘nutritional training’ are sometimes
used to refer to such strategies.
3 What is Periodized Nutrition?
It is important to define the terms ‘periodized nutrition’ and
‘nutritional training’. The words ‘training’ and ‘periodized’
by definition refer to a structured and planned process. In
reality, there is often little planning when it comes to
nutrition and limited integration of training and nutritional
practices. What athletes consume post-exercise may
depend on the training, but careful planning ahead of
training, with long-term goals in mind, is still relatively
uncommon. Clear guidelines are still lacking as this
developing field of research is only in its infancy. Most
nutritional recommendations for athletes aim to promote
acute recovery after exercise without acknowledging the
specific goal of the exercise and often without taking into
account the severity and type of exercise or the longer term
goals.
In this review, I provide an overview of potential
strategies aimed at enhancing specific adaptations that
could help athletic performance, and I define the term
‘periodized nutrition’. In the literature, the term ‘periodized
nutrition’ is sometimes used, but a clear definition and a
common interpretation is lacking. The term periodization
in the context of exercise training refers to a long-term
progressive approach designed to improve athletic performance
by systematically varying training throughout the
year. The term nutrition periodization is typically used to
describe changes in nutritional intake in response to certain
periods of training [12–14]. For example, during certain
periods of training there is a focus on weight management
and lower energy intake, whereas during other periods
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there is a focus on recovery and performance and higher
carbohydrate intake. Mujika et al. [14] concluded that
‘‘Nutrition should be periodized and adapted to support
changing individual goals, training levels, and requirements
throughout a season and/or training cycle’’. Hawley
and Burke [4] discussed the importance of a long term
periodized training-nutrition program as a way to enhance
performance. The authors stated ‘‘… it seems prudent to
suggest that competitive athletes may wish to manipulate
carbohydrate availability before, during, or after selected
training sessions that form part of a long-term periodized
training-nutrition plan to promote metabolic training
adaptations that should, in theory, promote endurancebased
performances’’. In this statement, there is a strong
focus on carbohydrate availability as a driver of training
effects, and the training effects are mostly in the muscle
and metabolic in nature. For example, training the extension
of the stomach wall as discussed in Jeukendrup [15]
would not be included in this definition of periodized
nutrition.
Therefore, I propose the following definition: periodized
nutrition refers to the planned, purposeful, and strategic use
of specific nutritional interventions to enhance the adaptations
targeted by individual exercise sessions or periodic
training plans, or to obtain other effects that will enhance
performance longer term.
The definition of periodized nutrition (or nutritional
training) introduced above includes all methods that use
nutrition (in the presence or absence of training) to improve
long-term performance. These methods include manipulations
of nutrient availability before, during, and after
training, but could also include practices that prepare other
organs for competition through nutritional manipulation
(e.g., improving stomach comfort by regularly drinking
large volumes [15]). The definition of nutritional training is
not restricted to adaptations of the muscle (and could relate
to adaptations in all organs), but will always have longterm
performance improvements as the main goal.
4 Nutritional Training: Specific Goals Require
Specific Methods
The terms periodized nutrition and nutritional training can be
used interchangeably and the selection of nutritional training
methods is highly specific to the goals. For example, if the
goal is to develop fat metabolism specifically, there may be a
role of training with low-carbohydrate availability that will
achieve these specific adaptations. However, to achieve
adaptations of the gastrointestinal (GI) absorptive capacity
[15] for carbohydrates, an increased carbohydrate intake
would be recommended. There may be a role for both of
these seemingly contrasting methods in the training
approach of an athlete. In the future, we are likely to see more
planning of nutrition as part of the training plan of athletes.
Specific workouts will be accompanied by specific nutritional
goals. Nutrition can be planned as much as training can
be planned and can be made more purposeful. This will also
allow inter-individual differences in both physiology and
goals to be taken into account.
Different nutritional training methods can be used to
achieve specific goals (see Table 1). It is beyond the scope
of this review to discuss all methods in great detail and
several methods have been discussed at length in various
excellent recently published reviews [4, 5, 7–10]. I refer to
these reviews in the relevant sections, rather than discussing
the same studies in detail. In this review, I only
summarize the different nutritional training tools that have
been studied, and explain briefly the underlying principles
and potential benefits. Periodized nutrition does not refer to
long-term diet composition or any form of dieting, unless
this diet is strategically altered to accommodate specific
needs during specific periods. In Table 1, an overview of
some of the available nutritional training methods is provided.
This list may not be exhaustive but it represents the
most important variations that have received attention from
researchers where there is at least some supporting evidence
in the scientific literature.
4.1 Training Low
Training low is a general term to describe training with
low-carbohydrate availability. This low-carbohydrate
availability could be low muscle glycogen, low liver
glycogen, low-carbohydrate intake during or after exercise,
or combinations thereof. The rationale for reducing carbohydrate
availability is derived from early studies that
observed links between carbohydrate availability (muscle
glycogen) and gene expression [16] because it is generally
believed that training adaptations are the result of accumulated
small changes in protein synthesis that result in an
altered phenotype and improved performance. For this
protein synthesis to occur, it is important that there is a
stress signal, transcription, and translation, that messenger
RNA remains stable, and that sufficient amino acids are
available for protein synthesis. Many of these factors are
influenced by nutrition. For example, the metabolic changes
that occur as a result of muscle contraction, including a
rise in AMP-activated protein kinase (AMPK), are important
factors in regulating gene transcription. A single bout
of endurance exercise will increase AMPK and transcription
and/or messenger RNA content for various metabolic
and stress-related genes. Typically, transcriptional activity
peaks within the first few hours of recovery, returning to
baseline within 24 h. These findings have led to the overall
hypothesis that training adaptations in skeletal muscle may
Periodized Nutrition for Athletes S53
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be generated by the cumulative effects of transient
increases in gene transcription during recovery from
repeated bouts of exercise [17]. Although it is clear that
gene transcription alone is not a guarantee that protein
synthesis will occur, it is a necessary step for protein
synthesis to occur. Studies have also demonstrated a link
between muscle glycogen and AMPK expression, as lower
muscle glycogen results in greater AMPK expression [18].
It is likely that muscle glycogen directly influences AMPK
because a subunit of AMPK binds to specific glycogenbinding
sites, which prevents it from being phosphorylated
by upstream kinases [19]. However, when glycogen is
broken down, this AMPK becomes more active [19] and
with low concentrations of glycogen, high AMPK activity
is observed [18, 20]. Other signaling molecules such as p38
mitogen-activated protein kinase [21] and p53 [22], as well
as the expression of peroxisome proliferator-activated
receptor-c coactivator 1-alpha [23] may be enhanced to a
greater extent when exercise is performed under conditions
of carbohydrate restriction. It has also been demonstrated
in rats that peroxisome proliferator-activated receptorgamma
transcriptional activity is sensitive to the combined
effect of skeletal muscle contraction and glycogen depletion
[24]. Glycogen thus plays an important role in regulating
gene transcription in the muscle, which can alter
protein synthesis and ultimately the training adaptation.
Manipulating glycogen stores may therefore be a tool to
optimize training adaptation. Training low has received
considerable attention in the last few years. Here, I summarize
the principles of the different methods, but for a
more detailed discussion the reader is referred to several
excellent recent review papers [4, 6, 7, 25–29].
4.1.1 Training Twice a Day
The first study to use this principle was a study by Hansen
et al. [30] who used a one-legged kicking model to compare
training daily, once a day, vs. training twice a day,
every other day. The second exercise bout was performed
with low muscle glycogen and essentially, therefore,
Table 1 Nutritional training methods: while some methods have more supporting evidence than others, these are the potential nutritional
training tools that athletes and coaches can use to periodize the athlete’s nutrition
Train low Training twice a day Limited or no carbohydrate intake between the two sessions. The first training
will lower muscle glycogen so that the second training is performed in a lowglycogen
state. This may increase the expression of relevant genes
Training fasted Training is performed after an overnight fast. Muscle glycogen may be normal or
even high but liver glycogen is low
Training with low exogenous
carbohydrate availability
No or very little carbohydrate is ingested during prolonged exercise. This may
exaggerate the stress response
Low-carbohydrate availability
during recovery
No or very little carbohydrate is ingested post-exercise. This may prolong the
stress response
Sleep low Train late in the day and go to bed with carbohydrate intake restricted.
Essentially the same idea as low-carbohydrate availability after training but the
period post-exercise is extended. Muscle and liver glycogen will be low for
several hours during sleep
Low-carbohydrate high-fat/
ketogenic diets
Long-term low-carbohydrate stores
Train high Training with high muscle and
liver glycogen
Carbohydrate intake is high before training when glycogen is important and there
is a focus on glycogen restoration post-exercise
Training with a highcarbohydrate
diet
Carbohydrate intake is high on a daily basis independent of training, but may be
especially high around training (during and after)
Training the gut Training of stomach comfort Increasing volume of intake with or without exercise
Training gastric emptying Repeated use of meals to increase/improve gastric emptying of fluids or nutrients
(carbohydrate) and reduce stomach discomfort
Training absorption Increasing daily carbohydrate intake and/or intake during exercise to improve
absorptive capacity of the gut and reduce intestinal discomfort
Training race nutrition Training all aspects of a nutrition strategy as on race day
Training dehydrated Training in a dehydrated state Training with limited/no fluid intake to allow dehydration
Improving training
adaptations with
supplements
Supplements Supplements that may allow more training to be performed (see Table 2)
Supplements that may initiate or increase protein synthesis and/or increase
myofibrillar protein synthesis (see Table 2)
Supplements with the potential to increase mitochondrial biogenesis (see
Table 2)
S54 A. Jeukendrup
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subjects trained 50% of the time with low muscle glycogen.
This produced marked improvements in the markers
of oxidative capacity [activity of the mitochondrial
enzymes 3-hydroxyacyl-CoA dehydrogenase (HAD) and
citrate synthase (CS)] and increased glycogen levels compared
with training in a glycogen-loaded state all the time
[30]. This sparked a reaction by various researchers and
coaches who argued that a single-legged kicking model did
not reflect a real-life situation. In addition, the study used
untrained individuals, thus the real-life relevance for athletes
was still unknown. Studies with the same design and
performed in parallel in the UK and Australia by Hulston
et al. [31] and Yeo et al. [20] investigated the effects in a
more realistic athletic setting. In both studies, cyclists
trained twice a day every other day or once every day. Both
studies produced similar results. The first observation in
both studies was that the cyclists who trained twice a day
(train low) could not maintain the same intensity as the
cyclists who trained once a day. Despite the fact that the
former performed less work, some of the adaptations were
greater. For example, Hulston et al. [31] reported that HAD
and fatty acid translocase (FAT/CD36) protein content was
increased more when ‘training low’ and the ability to use
fat as a fuel was improved [20, 31]. Morton et al. [32] also
observed beneficial adaptations (increased succinate
dehydrogenase activity) when training with low muscle
glycogen. However, there were no differences in performance
after 3 weeks of training low compared with the
control [20, 31], but perhaps the relatively short training
period in these studies was insufficient to demonstrate
changes in performance. It appears that training twice a day
may result in adaptations that favor fat metabolism, but it is
too early to definitely conclude that this training method
will also result in long-term performance benefits.
4.1.2 Training Fasted
Perhaps the most common way to ‘train low’ is training in
an overnight fasted state. Typically, the last meal is consumed
between 8 and 10 P.M. the night before, and exercise
is performed in the morning before breakfast is
consumed. This situation is different from the previous
methods, where muscle glycogen was reduced by prior
exercise. When training fasted, muscle glycogen should be
unaffected by the overnight fast, but liver glycogen will be
very low [33].
Studies by Hespel and coworkers [34, 35] demonstrated
that training in the fasted state may induce more profound
adaptations then training in the fed state (a carbohydratecontaining
breakfast and consuming carbohydrates during
exercise). For example, in one study it was demonstrated
that oxidative enzymes such as CS and HAD were upregulated
to a greater degree (47 and 34%, respectively) when
fasted was compared with fed after 6 weeks of training
(4 9 per week, 1–1.5 h at 75% maximal oxygen uptake)
[34]. The authors concluded that training in the fasted state
was more effective to increase muscle oxidative capacity
than training in the fed state. They also observed that
intramuscular fat utilization was increased with fasted
training and noted improvements in the regulation of blood
glucose levels. The mechanisms are likely to be different
from training with low glycogen. Van Proeyen et al. [36]
found no differences in AMPK in subjects training in the
fasted vs. fed state, but did observe differences in postexercise
eukaryotic elongation factor 2 phosphorylation
(elevated after carbohydrate feeding but not after fasting).
De Bock et al. [35] showed that exercise in the fasted state
facilitated intramuscular fat use during exercise and
improved glycogen resynthesis [35]. It was also demonstrated
that carbohydrate ingestion blunted uncoupling
protein 3 gene expression, whereas training in the fasted
state resulted in a marked increase in uncoupling protein 3
gene expression [35]. Another study by the same research
group did not result in any marked improvements with
training in the fasted state [37]. In this study, small changes
were observed in proteins involved in the regulation of fat
metabolism but this did not result in measurable changes in
fat oxidation. The results of these studies are promising and
there appear to be potential benefits of training in the fasted
state. However, there are still a number of practical questions
that need to be answered such as how many days of
training per week are needed? What is the type of training
(intensity and duration) that is most suitable for fasted
training? How many weeks should this training be performed
to see meaningful effects? In addition, studies to
date have focused on metabolic adaptations and few have
addressed the potential effects on exercise performance,
Table 2 Categories of supplements suggested to promote training
adaptations based on their mechanism of action
Supplements that may allow more
training to be performed
Caffeine
Bicarbonate
Creatine
Nitrates (beetroot)
Supplements that may initiate or
increase protein synthesis and/or
increase myofibrillar protein synthesis
Essential amino acids
Leucine
Branched-chain amino
acids
b-Hydroxy b-
methylbutyrate
Supplements with the potential to
increase mitochondrial biogenesis
Epigallocatechin gallate
and green tea extracts
(-)Epichatechins
Resveratrol
Quercetin
Conjugated linoleic acid
Periodized Nutrition for Athletes S55
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such as whether fasted training results in performance
improvements over time?
4.1.3 Training Adaptation with Low Exogenous
Carbohydrate Availability
Although the benefits of carbohydrate ingestion during
exercise are generally recognized [38–41], carbohydrate
supplementation during exercise may not have only positive
effects. The positive effects may refer to the acute
situation, but it has been suggested that chronic use of
carbohydrate during exercise may limit training adaptations.
This idea stems from observations that muscle
glycogen stores are related to the expression of genes relevant
to the adaptation to training. It is generally thought
that training adaptations are the result of recurrent changes
in gene expression, which occur with every bout of exercise,
leading to a change in phenotype such as increases in
fatty acid transport and oxidation. Long-term glucose
ingestion might negatively affect the expression of relevant
genes. Glucose ingestion can attenuate the rise in AMPK
[42], and long-term suppression of AMPK in turn could
reduce the increase in CS activity [43] and reduce muscle
glycogen accumulation [44], two common markers of
training adaptation. Glucose ingestion will suppress lipolysis
and reduce the concentration of fatty acids in the
plasma, and this possibly attenuates some of the traininginduced
adaptations. It has been shown that glucose
ingestion during exercise may suppress the expression of
carnitine palmitoyl transferase mRNA, mitochondrial
uncoupling protein 3, and FAT/CD36 [45]. However, in a
carefully conducted study by Akerstrom et al. [46] in which
a 10-week leg extension training program was followed by
the subjects, glucose ingestion did not alter training adaptations
related to substrate metabolism, mitochondrial
enzyme activity, glycogen content, or performance. Significant
increases were observed in CS and HAD activities
after the 10-week training program but there was no effect
of carbohydrate supplementation on these changes. It
appears that the effects of glucose ingestion during exercise
were distinctly different from those induced by exercising
with low muscle glycogen. It is interesting to note that
Morton et al. [32] observed improvements in succinate
dehydrogenase activity with low-glycogen training in the
presence or absence of exogenous carbohydrate feeding.
4.1.4 Low-Carbohydrate High-Fat or Ketogenic Diets
Another way to train low would be to remove carbohydrate
from the diet and have a long-term, low-carbohydrate,
high-fat diet. It was demonstrated in the 1920s that
reducing carbohydrate intake and increasing fat intake will
result in higher rates of fat oxidation [47]. However, it was
also observed that subjects felt more fatigued [47] and
exercise capacity was reduced with this practice [48].
Burke and colleagues [49–52] performed a series of shortterm,
low-carbohydrate, high-fat diet studies and one of
their observations was that 5 days on a low-carbohydrate,
high-fat diet already showed some adaptations to that diet
that could not be reversed completely by refilling muscle
glycogen stores. Enzymes involved in fat oxidation were
upregulated and fat oxidation was increased [49]. In none
of the studies, however, were any improved performance
effects observed [50–52]. When athletes were training over
a longer period of time (7 weeks) with either a high-fat
(62% fat, 21% carbohydrate) or a carbohydrate-rich (20%
fat, 65% carbohydrate) diet, it was observed that both
groups improved with training, but training effects were
more profound in the high-carbohydrate group.
There is one study that is always referred to as evidence
for the benefits of a ketogenic diet. In the 1980s, a study
with five subjects showed that a ketogenic diet, containing
less than 20 g of carbohydrate per day, for a prolonged
period of time (4 weeks) resulted in hyperketonemia and
increases in fat oxidation [53]. In this study, exercise
capacity was only tested at a low intensity and showed a
large degree of variation both between subjects and within
subjects. On average, there was no difference in exercise
capacity before and after the ketogenic diet. As expected,
fat oxidation was increased and some adaptations occurred
in the muscle.
A study by Stellingwerff et al. [54] demonstrated that
although a high-fat diet will increase fat oxidation, perhaps
by increasing enzyme activity related to fat metabolism, it
can reduce enzyme activities related to carbohydrate
metabolism. Thus, whilst many studies observed
improvements in HAD, for example, Stellingwerff et al.
[54] demonstrated compromised pyruvate dehydrogenase
activity. It may therefore be that fat oxidation is increased,
at least partly, as a result of an inability to use carbohydrates.
Because carbohydrates are important substrates for
high-intensity exercise, such adaptations would be
unwanted. In fact, a carefully controlled study by Burke
et al. [55] demonstrated that there were no benefits of a
ketogenic vs. a high-carbohydrate diet, or a mixed
approach (higher or lower carbohydrates depending on
training) in elite endurance athletes. In fact, performance of
high-intensity exercise was not improved by 3 weeks of
intensified training in the ketogenic diet group (-1.6%),
while athletes consuming the other diets made substantial
performance improvements (6.6% in the high-carbohydrate
group and 5.5% in the mixed group).
The ketogenic diet has received considerable attention
in the popular press and many claims have been made
recently. However, it is important to realize that, to date,
not a single study has demonstrated performance benefits
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of a ketogenic diet, including the early study that is often
referred to [53]. Thus, at present, there are no data on
ketogenic diets in athletes on which to base performance
claims.
4.1.5 Carbohydrate Restriction During Recovery
Another concept is restricting carbohydrate intake in the
first hours after exercise. The time course of transcriptional
activation for many exercise-induced genes stretches
across the first few hours of recovery and usually returns to
baseline within 24 h [56]. Traditionally, it was recommended
to consume carbohydrate immediately after exercise
as this results in the highest rates of glycogen synthesis
[56]. When studying the effects on gene expression postexercise
with or without carbohydrates, interesting observations
were made by Pilegaard et al. [57]: activation of
metabolic genes was augmented following 75 min of
cycling exercise when carbohydrate intake was restricted
for over 5 h compared with controls [57]. Cochran et al.
[21] also showed that carbohydrate ingestion post-exercise,
and not necessarily changes in muscle glycogen content per
se, altered the metabolic response to repeated sessions of
high-intensity interval exercise. Specifically, it was
observed that p38 MAPK was activated more when carbohydrate
intake was restricted and this has been linked to
enhanced expression of peroxisome proliferator-activated
receptor-c coactivator 1 and an improved metabolic
adaptation to exercise. Other studies, however, could not
confirm this and found no differences between a high- and
a low-carbohydrate intake during recovery [58–60]. A
recent study [60] investigated the effects of post-exercise
carbohydrate intake vs. carbohydrate restriction on glycogen
and gene expression. The carbohydrate intake resulted
in partial glycogen replenishment but gene expression was
not different between the two groups. After 24 h, glycogen
replenishment was similar in the two groups (a finding that
seems consistent in well-trained individuals) and gene
expression levels returned to baseline levels in both groups.
It is not impossible that changes in gene expression levels
went unnoted because the timing of the relatively small
number of sampling points may not have been perfect.
Thus, the effect of carbohydrate manipulation in the
recovery phase is still uncertain.
4.1.6 Sleep Low
The concept of carbohydrate restriction during recovery
was extended by Lane et al. [61]. They performed the first
study into the concept of ‘train high-sleep low’, which
refers to a hard workout in the evening resulting in lowered
carbohydrate availability (muscle and liver glycogen) followed
by sleep. This practice goes against the typical
advice to athletes to consume carbohydrates post-exercise
(and before going to sleep) to speed up recovery. Training
high and sleeping low, however, resulted in a greater
upregulation of several exercise responsive signaling
markers with roles in lipid oxidation the following morning
compared with when an evening meal was consumed [61].
In this study, ‘train high-sleep low’ did not elicit a greater
upregulation of cellular markers of mitochondrial biogenesis.
The study only addressed the acute changes and did
not intend to study the long-term effects on metabolism or
performance.
A follow-up study performed in France studied the
longer term effects of the ‘train high-sleep low’ approach.
Two groups of triathletes undertook the same endurance
training program for 3 consecutive weeks [62]. One group
(n = 11) followed a ‘sleep low’ strategy for manipulating
carbohydrate availability (high-intensity workout with
high-carbohydrate availability followed by a carbohydraterestricted
recovery plus an overnight fast; then a prolonged
submaximal workout the following morning commenced
with low-carbohydrate availability) in the training schedule.
The control group (n = 10) maintained regular carbohydrate
intake throughout the day and undertook each
training session with normal/high carbohydrate availability.
The triathletes performed a simulated triathlon race at
the start and end of the intervention period. The authors
found a small but significant effect on performance as
10-km running performance increased after 3 weeks in the
‘sleep-low’ group but not in the control group. Interestingly,
the authors also reported improvements in supramaximal
cycling time to exhaustion with sleep low but not
control.
These are the only two studies on the concept of ‘train
high-sleep low’ and it may be too early to draw firm
conclusions. However, the studies do provide promising
results. From a practical point of view, it is important to be
aware of other potential side effects and unknowns of this
approach: what are the effects on recovery when applied
frequently, the effects on immune function, and perhaps
most importantly, the effects on quantity and quality of
sleep?
4.2 Training High
Training high refers to training with high carbohydrate
availability. Muscle and liver glycogen levels are high at
the start of exercise and/or carbohydrates are supplemented
during exercise. There are two main reasons for using this
approach. First, carbohydrates have been shown to be
important to maintain the quality of endurance training
[31, 63] and reduce symptoms of fatigue and overreaching
[64–67]. The second reason for training high is related to
intestinal function. In longer events, it is clear that
Periodized Nutrition for Athletes S57
123
ingesting carbohydrates and increasing exogenous carbohydrate
oxidation will result in improved endurance performance
in most events [38–41, 68]. The effects of
training high on intestinal function has been discussed in
detail in a separate review article in this Sports Medicine
Supplement issue [15].
It is often argued by coaches that it is essential to
maintain a high quality of training to optimize long-term
training adaptations and there are a few studies that support
such beliefs. Simonsen et al. [67] evaluated a group of
trained rowers who performed daily hard training (twice
daily) for 4 weeks whilst consuming a normal carbohydrate
(5 g/kg/day) or a high-carbohydrate diet (10 g/kg/day).
Mean power output in 2500-m time trials increased 10.7%
in the high-carbohydrate group and 1.6% in the normal
carbohydrate group. We simulated a training camp scenario
where athletes performed 1–2 weeks of intensified training,
resulting in extreme fatigue and decreased performance by
the end of the intensified training period [64, 66]. A consistent
finding in these studies was that when athletes were
supplemented with carbohydrates, and had a higher overall
carbohydrate intake, reductions in performance were less
profound and the symptoms of overreaching were reduced,
despite the fact that they performed more work in training
[64, 66]. Therefore, there is evidence that during extreme
training with repeated high-intensity work, a higher carbohydrate
approach is preferred. However, it must be noted
that these studies used an extreme training volume to
simulate a training camp situation and the result after 1–2
weeks was a decreased performance in all groups.
Although the train-high group seemed to recover better, the
effects on longer term performance or the effects of more
moderate training with higher or lower carbohydrate are
understudied.
4.3 Training the Gut
In addition to the direct effects of training high on performance,
there may be other benefits through reducing GI
problems. Gastrointestinal problems are very common
amongst endurance athletes, ranging from mild to severe. It
is possible that some of these symptoms are caused by the
fact that the intestine is not adapted to absorb nutrients well
under stress. It is likely that these symptoms are at least
partly related to the fact that blood flow to the intestine is
reduced during intense and prolonged exercise and dehydration
seems to exacerbate this effect. It is also known that
intestinal absorption is the main barrier to delivering carbohydrate
to the contracting muscle [69]. Training the gut
could potentially help with the development of gut adaptations
that improve the delivery of nutrients (especially
carbohydrate), and reduce the prevalence or severity of GI
symptoms during exercise.
As discussed in the review article in this issue of Sports
Medicine [15], the importance of the GI tract is often
underestimated by athletes. The GI tract plays a critical
role in delivering carbohydrates and fluids during prolonged
exercise and can therefore be a major determinant
of performance. The incidence of GI problems in athletes
participating in endurance events is high [70], indicating
that GI function is not always optimal in those conditions.
There is a substantial body of evidence that suggests that
the GI system is highly adaptable [15]. Gastric emptying as
well as stomach comfort can be ‘trained’, perceptions of
fullness decreased [71] and some studies have suggested
nutrient-specific increases in gastric emptying [72, 73].
There is also evidence that diet has an impact on the
capacity of the intestine to absorb nutrients [74]. For
example, a high-carbohydrate diet will increase the number
of sodium glucose co-transporter transporters in the intestine
as well as the activity of the transporters [75–78],
allowing greater carbohydrate absorption and oxidation
during exercise [74]. It is also likely that when such
adaptations occur, the chances of developing GI distress
are reduced. Future studies should include more human
studies and focus on a number of areas including the most
effective methods to induce gut adaptations and the time
line of adaptations. To develop effective strategies, it is
important to obtain a better understanding of the exact
mechanisms underlying these adaptations. It is clear that
‘nutritional training’ can improve gastric emptying and
absorption, and likely reduce the chances and/or severity of
GI problems, thereby improving endurance performance as
well as ensuring a better experience for the athlete. The gut
is an important organ for endurance athletes and should be
conditioned for the situations it will be required to function
in.
4.4 Training Race Nutrition
Training race nutrition refers to practicing your nutritional
intake plan for a race in the weeks leading up to the race.
There is considerable overlap between this type of training
and training the gut. If regularly performed, it is likely that
adaptations in absorption and gastric emptying will occur
[15]. The reverse may also be true: if certain nutrients are
avoided (e.g., when following a carbohydrate-restricted
diet), the capacity to absorb these nutrients is also reduced,
so that in competition, less carbohydrate can be oxidized
and thus intake should be reduced in competition as well.
There are other aspects that could be practiced that may
affect overall performance. Examples of this include a
marathon runner practicing drinking from a cup whilst
running at race pace or if a runner plans to run with a bottle
to also run with a bottle in training. Training race nutrition
refers to mimicking everything an athlete would encounter
S58 A. Jeukendrup
123
in a race. Whereas training the gut would focus on carbohydrate
absorption, for example, training race nutrition
includes also drinking, ingesting salt tablets, caffeine
intake, and other practices that are part of an athlete’s race
day nutrition plan.
4.5 Training Dehydrated
A concept that has been considered for some time but only
recently systematically investigated is whether training in a
hypohydrated state can improve performance when dehydrated.
Fleming and James [79] recruited ten recreationally
active individuals who performed four exercise tests in an
euhydrated or hypohydrated state. Euhydration and hypohydration
were induced by manipulating fluid intake in 24
h pre-exercise and a 45-min steady state run. Before and
after this short training period, the subjects performed a
45-min run followed by a 5-km performance task. It was
observed that dehydration reduced performance by 2.4%.
The main finding, however, was that training without fluids
resulted in smaller reductions in performance. On average,
the runners were 5.8% slower with euhydrated training and
only 1.2% slower when they trained in a dehydrated state.
Additionally, the rating of perceived exertion was normalized
after hypohydrated training. Thus, it appears from
this study that familiarization with hypohydration may
have the potential to improve performance in situations
where hypohydration may occur. However, at present there
is only one study to report these effects and more work is
needed before we can turn these findings into clear general
guidelines for athletes.
4.6 Supplements that may Enhance Chronic
Adaptations
There are a number of supplements that have been claimed
to enhance training adaptations. A prime example has been
leucine, an amino acid that has an important function in
stimulating protein synthesis. However, many other supplements
have been suggested to enhance specific aspects
of metabolism. Generally, supplements linked to promoting
training adaptation can be divided into three main
categories based on their mechanism of action (Table 2).
4.6.1 Supplements that Increase Quality of Training
There are a number of supplements that claim to increase
the quality as well as quantity of training, and by deduction
it is then suggested that performance should also be
enhanced. For both caffeine and sodium bicarbonate
(NaHCO3), there is evidence that these supplements can
enhance performance during exercise, provided the exercise
duration and intensity are in the range that these
supplements are effective [80]. There is also some evidence
that nitrates can improve exercise performance in specific
conditions [81, 82]. It must be realized that for caffeine,
most studies have studied exercise lasting around 1 h and
for NaHCO3 and nitrates typically between 1 and 10 min.
Creatine has been shown to increase the sprint capacity
when performing repeated sprints [83]. Such supplements
could potentially improve long-term training adaptations
because they would allow a greater training load or higher
quality of training.
It has also been suggested that long-term NaHCO3
ingestion could result in improved training adaptations
[12]. One study used long-term NaHCO3 ingestion and
found that the group that consumed 400 mg of NaHCO3/kg
body mass 1.5 and 0.5 h before interval training (6–12 9 2
min at 100% maximal oxygen uptake), three times per
week over 8 weeks, had greater improvements in the lactate
threshold and short-term endurance performance during
high-intensity exercise (time to fatigue at 100% pretraining
VO2 peak intensity) compared with the placebo
group that did the exact same training [84]. The findings
were not reproduced in a study in well-trained rowers [85].
Although the rowers improved over a 4-week training
period, the addition of long-term NaHCO3 supplementation
during the training period did not significantly enhance
performance further. More studies are needed to confirm/or
contradict the early findings but also to study the effects of
long-term NaHCO3 supplementation on water retention
and resulting changes in body mass. Increases in body mass
could be unwanted in a number of settings and could be
counterproductive. As discussed in Sect. 4.2, carbohydrate
intake can also be used to improve the total amount of work
done in training. Although there is good evidence that
acutely these nutritional strategies improve performance
and thus could increase the quantity as well as quality of
training, there is far less evidence that such strategies also
result in superior adaptations long term.
4.6.2 Supplements that Increase Protein Synthesis
There is another category of supplements that claims to
increase protein synthesis (which would be relevant to both
strength as well as endurance sports) or more specifically
myofibrillar protein, which would benefit those athletes
who want to gain muscle mass and/or strength. It has
become apparent that it is mainly the essential amino acids
that drive the process of muscle protein synthesis [86].
However, perhaps the most important candidate is the key
essential amino acid leucine, as it alone appears to be the
metabolic trigger for muscle protein synthesis [87, 88].
Leucine, branch chain amino acids, or b-hydroxy bmethylbutyrate
would all potentially work through the
same mechanism of ‘triggering’ (activating) muscle protein
Periodized Nutrition for Athletes S59
123
synthesis. Extensive reviews have been written on this
topic and the reader is referred to these excellent papers for
a detailed discussion about the factors that influence protein
synthetic rates [89–91].
4.6.3 Supplements with the potential to increase
mitochondrial biogenesis
This category of supplements that claims to increase
mitochondrial biogenesis, fat oxidation, and endurance
capacity or performance is perhaps the largest group of
supplements, but it is also the one with the least solid
evidence. A host of ingredients have been linked to
improvements in cell signaling that could then trigger
mitochondrial biogenesis. These include, but are not limited
to the catechins epicatechin and epigallocatechin gallate,
polyphenols such as resveratrol and quercetin,
caffeine (reviewed in [10, 92]), and conjugated linoleic
acid [93]. Although there are some promising results,
especially in animal models, translation to healthy trained
athletes is often problematic. For example, while green tea
extracts (containing the active component epicatechin and
epigallocatechin gallate) have been shown to increase fat
oxidation and performance in mice [94], in humans, these
effects were not found [95] after 7–28 days of green tea
extract supplementation. Two recent review articles summarized
the effects of these small nutritional bioactives
[10, 92] and although there are some promising findings in
some areas, the evidence does not seem convincing enough
to formulate practical guidelines for the use of any of these
compounds.
4.7 Supplements that may Reduce Training
Adaptation
It is important to note that several studies have suggested
that certain supplements and, in particular, a high intake of
antioxidants could actually reduce the training adaptation
to exercise [9]. Not all studies have demonstrated such
effects and differences between studies may be a function
of the specific antioxidants used, and the dose and timing
of intake [96]. However, more work is clearly needed and it
seems wise to recommend avoiding high doses of antioxidants
at this point in time if the main goals are to develop
long-term training adaptations.
5 Conclusion
In summary, training adaptations are the result of a complex
interplay between nutrition and exercise. Therefore,
by manipulating nutritional intake, it is possible to promote
training adaptations. Several strategies have been
developed to this effect, some of which have more evidence
in support than others. The most common methods
are training with high-carbohydrate availability (train high)
and training with low-carbohydrate availability (train low).
There are many variations of each of these methods. In
addition, because the gut is an important organ, methods to
improve gut function (faster absorption and reduced GI
distress) have also been developed. There are also certain
ingredients (supplements) that may increase the effects of
training. All of these methods can be captured under the
umbrella of periodized nutrition. Nutritional training is
another term that is sometimes used and this term can be
used interchangeably.
Which of these methods should be used depends on the
specific goals of the individual and there are no methods
that will address all needs. Therefore, appropriate practical
application lies in the optimal combination of different
nutritional training methods. In the years to come, we will
undoubtedly begin to obtain a better understanding of the
molecular bases for training adaptations and find ways to
better incorporate and integrate periodized nutrition into
training methods.
Acknowledgements This article was published in a supplement
supported by the Gatorade Sports Science Institute (GSSI). The
supplement was guest edited by Lawrence L. Spriet who attended a
meeting of the GSSI expert panel in November 2015 and received
honoraria from the GSSI for his participation in the meeting. He
received no honoraria for guest editing the supplement. Dr. Spriet
selected peer reviewers for each paper and managed the process. Dr.
Asker Jeukendrup also attended the meeting of the GSSI expert panel
in November 2015 and received an honorarium from the GSSI, a
division of PepsiCo, Inc. for his meeting participation and the writing
of this manuscript. The views expressed in this manuscript are those
of the author and do not necessarily reflect the position or policy of
PepsiCo, Inc.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://
creativecommons.org/licenses/by/4.0/), which permits unrestricted
use, distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if changes were
made.
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