nutrients
Review
Nutrition and Supplement Update for the Endurance
Athlete: Review and Recommendations
Kenneth Vitale
1,
* and Andrew Getzin
2
1
Department of Orthopaedic Surgery, Division of Sports Medicine, University of California San Diego,
La Jolla, CA 92037, USA
2
Sports Medicine, Cayuga Medical Center, Ithaca, NY 14850, USA; [email protected]g
* Correspondence: [email protected]; Tel.: +1-858-657-8634
Received: 9 April 2019; Accepted: 6 June 2019; Published: 7 June 2019
Abstract:
Background: Endurance events have experienced a significant increase in growth in the new
millennium and are popular activities for participation globally. Sports nutrition recommendations
for endurance exercise however remains a complex issue with often opposing views and advice by
various health care professionals. Methods: A PubMed/Medline search on the topics of endurance,
athletes, nutrition, and performance was undertaken and a review performed summarizing the
current evidence concerning macronutrients, hydration, and supplements as it pertains to endurance
athletes. Results: Carbohydrate and hydration recommendations have not drastically changed in
years, while protein and fat intake have been traditionally underemphasized in endurance athletes.
Several supplements are commercially available to athletes, of which, few may be of benefit for
endurance activities, including nitrates, antioxidants, caffeine, and probiotics, and are reviewed here.
The topic of “train low,” training in a low carbohydrate state is also discussed, and the post-exercise
nutritional “recovery window” remains an important point to emphasize to endurance competitors.
Conclusions: This review summarizes the key recommendations for macronutrients, hydration,
and supplements for endurance athletes, and helps clinicians treating endurance athletes clear up
misconceptions in sports nutrition research when counseling the endurance athlete.
Keywords:
athletes; physical endurance; sports nutritional sciences; nutritional requirements;
dietary supplements
1. Introduction
Participation in endurance events has increased both nationwide and globally, with 2.5 million
triathlon participants in the US in 2015 [1] and 3.5 million individuals worldwide [2]. In recent years,
there has been a shift in running from standard marathon races to “other distance” races such as mud
runs, color runs, and obstacle course races [
3
]. Furthermore, ultra-endurance events are also gaining
popularity [
1
,
3
]. Ultra-endurance activities are typically defined as events lasting at least 4 [
4
] to 6 h [
5
]
duration. Prior studies have illustrated the challenges that ultra-endurance exercise exerts on the
body in terms of fatigue, sub-optimal nutrition, and energy deficit [
4
,
5
], and brings awareness to the
potential medical complications of ultra-endurance exercise [
5
] underscoring the importance of an
individualized nutritional approach [
4
]. Due to the popularity of endurance and ultra-endurance
events, there is a need to define nutritional needs of the athletes. Our goal with this review is to provide
the reader with a comprehensive review in a consolidated form and offer practical, evidence-based
recommendations that are valuable and directly applicable to the clinician involved in athlete care.
Although there have been significant advances in the understanding of nutritional requirements
for endurance athletes, many gaps still exist in the literature. The science of nutrition remains a complex
topic, continually evolving, and sometimes contradictory. “Sports nutrition” involves the fields of sports
Nutrients 2019, 11, 1289; doi:10.3390/nu11061289 www.mdpi.com/journal/nutrients
Nutrients 2019, 11, 1289 2 of 20
medicine, sports science, dietetics, cultural influences, and even popular media. Especially when it
comes to elite athletes and specifically “what to eat,” nutritionists, registered dietitians, sports scientists,
physicians, and other healthcare professionals often debate on the ideal diet.
This review summarizes the current available evidence regarding macronutrients and highlights
new areas of research regarding select supplements of interest to endurance athletes. The goal is
to bring clarity in areas of uncertainty involving optimal nutrition for endurance exercise, and to
provide recommendations for athletes trying to optimize their health and performance. To cover
every vitamin, mineral, and supplement available in the arena of “nutrition for athletes” however is
beyond the scope of this paper, so this review shall focus on the major macronutrient requirements
including carbohydrate (CHO), protein and fat needs, hydration requirements, and select specific
topics including caffeine, nitrates, probiotics, and antioxidants as they relate to endurance athletes.
In the authors’ clinical experience treating endurance athletes, these topics were included to provide
clinicians with information regarding the more commonly asked questions by endurance athletes.
In reality there are numerous supplements and strategies that may be employed by endurance athletes.
However, in the authors’ experience caffeine and nitrates are frequently investigated and used by
athletes. Furthermore, antioxidants and probiotics are commonly explored topics by injured athletes
and are steadily-growing fields of research. Lastly, “hot topics” and controversial views in endurance
exercise are covered such “train low” vs. “train high” states, branched-chain amino acids vs. essential
amino acids, vegetable vs. animal vs. milk proteins, and drinking to plan vs. drinking to thirst.
2. Materials and Methods
A PubMed/Medline search was performed for articles between 1980 and December 2018
using search terms “nutrition for athletes,” “sports nutrition,” “endurance athlete nutrition,”
“supplementation endurance,” and the above MeSH keywords, without restrictions on language, sex
or age. Additionally, references of extracted articles were manually searched. Sixty-seven articles
were retrieved, duplicates were removed, and the remaining articles were screened for relevance.
Twelve articles were excluded as they either contained clinical studies on non-athletes, or mainly
non-endurance (strength and power) athletes or were animal-based studies. Fifty-two were included
and further categorized into macronutrients, hydration, and supplements; see Figure 1 for the PRISMA
search strategy. A systematic review was not done due to extreme heterogeneity of studies and data;
a clinical/descriptive review was thus performed.
From the selected studies, clinical recommendations are provided according to the American
Academy of Family Physicians’ Strength-of-Recommendation Taxonomy (SORT) grading scale [
6
].
The scale levels are derived from the 2002 United States Department of Health and Human Services’
Agency for Healthcare Research and Quality (AHRQ) report that addresses three key research elements:
quality, quantity, and consistency of evidence [
7
]. Most studies were position stands, reviews,
and current best-evidence statements of several international organizations (see below) with Level
1 “consistent and good quality patient-oriented evidence” data with a strength of recommendation
(SORT) rating of A.
Sections are divided into Carbohydrate (with subsections on pre-competition “loading” vs. during
competition “fueling” requirements), Protein (subsections on daily vs. pre-, during, and post-exercise
requirements), Fat, Hydration, and finally Supplements and “Hot Topics.” When available, new and
controversial or opposing views to traditional sports nutrition recommendations are presented.
This better provides the clinician with up-to-date knowledge of progressive and alternative options
that endurance athletes may seek in attempt to improve health and athletic performance.
Nutrients 2019, 11, 1289 3 of 20
Figure 1. PRISMA flow diagram search strategy.
3. Results
3.1. Carbohydrate
Carbohydrate requirements for the endurance athlete can be a fiery topic, often leading to
passionate (and sometimes confrontational) debates on ideal intake amongst the fitness and medical
community. The joint position stand of the Academy of Nutrition and Dietetics (AND), Dietitians of
Canada (DC), and the American College of Sports Medicine (ACSM) recommends that moderate
exercise (1 h/day (h/day)) requires 5–7 g per kilogram of bodyweight per day (g/kg/day) of CHO,
while moderate to high intensity exercise (1–3 h/day) mandates 6–10 g/kg/day. Ultra-endurance
athletes with extreme levels of commitment to daily activity (4–5 h of moderate to high intensity
exercise every day) may need up to 8–12 g/kg/day [
8
]. The International Society of Sports Nutrition
(ISSN) recommends in order to maximize glycogen stores athletes should employ an 8–12 g/kg/day
high CHO diet [9].
Carbohydrate (as blood glucose and muscle glycogen) has the advantage of generating more ATP
per volume of oxygen (O
2
) compared to fat [
10
] but exhaustion of liver and muscle CHO stores is
associated with fatigue, reduced work, and impaired concentration [
8
,
11
,
12
]. It is the often-described
feeling by athletes of “hitting the wall,” or “bonking.” Therefore, fueling strategies both before and
during the race/event have been developed and outlined below. An important point to the clinician
however, is that even after 4.5 h of cycling at 70% of maximum O
2
consumption (VO
2max
) when CHO
stores should be entirely depleted, elite athletes can still run at 16 km/h for an additional 2.5 h at 66%
VO
2max
[
13
]. Consequently, glycogen depletion must not be the sole determiner of fatigue. Other CHO
sources such as lactate utilization and other mechanisms such as increased capability to oxidize fat
(see below) are postulated [
14
] to account for this effect and clinicians should consider this when
counseling athletes.
Nutrients 2019, 11, 1289 4 of 20
3.1.1. Pre-Competition, “Loading”
Prior to the race (if the event is to last <90 min, a simple “topping-off” of glycogen stores to
replenish muscle and liver glycogen lost during the prior day has been recommended typically with
a CHO-rich diet of at least 6 g/kg [
12
] and up to 7–12 g/kg [
8
] in the 24 h period before the event.
For events lasting >90 min however, glycogen supercompensation, or “carbo loading,” in the preceding
36–48 h may help improve performance by 2–3% [
11
]. Traditionally it had been recommended that in
order to double glycogen stores in the classical supercompensation model [
15
], one had to exhaust
glycogen stores with high-intensity exercise prior to high CHO intake. However recent studies show
that short-term high-intensity exercise (or even complete physical inactivity) followed by a 1-day
high (10–12 g/kg/day) intake of CHO similarly achieves glycogen supercompensation, and this is
maintained for 3 days [
11
,
16
]. This latter point is particularly important to consider clinically, as it gives
the athlete additional flexibility in athletes with gastrointestinal (GI) intolerability or GI distress prior
to competition. In the final 1–4 h prior to the event, a single dose of 1–4 g/kg CHO is recommended
for a final top-off of liver glycogen stores, as typically endurance events occur in the early morning
directly after the overnight fast which depletes liver glycogen [8].
3.1.2. During Competition, “Fueling”
For events lasting <60 min, no exogenous CHO ingestion is required [
8
,
14
]. However, for activities
>60 min, active fueling strategies are recommended to maintain CHO accessibility. For events lasting
1–2.5 h, 30–60 g/h is commonly recommended [
8
,
14
] in a 6–8% CHO solution (concentrations typically
found in commercial sports drinks) ideally consumed every 10–15 min [
9
] to maximally spare glycogen
stores. For events lasting >2.5 h, higher CHO intakes of 60–70 g/h, and up to 90 g/h if tolerable are
associated with improved performance [
8
]. This higher intake recommendation stems from research
demonstrating that exogenous CHO oxidation peaks at a CHO ingestion rate of 1.0–1.1 g/min, due to
the maximal GI absorption at this rate [
11
,
17
]. Including multiple CHO sources (glucose/fructose
mixtures) at higher ingestion rates of 1.8 g/min can further increase oxidation up to 1.2–1.3 g/min
due to differential intestinal transport mechanisms, and these glucose/fructose combinations also
improve GI tolerance [
8
,
11
,
12
,
17
,
18
]. At these higher ends of intake, the authors recommend athletes
routinely practice their fueling plan to assess GI comfort (e.g., liquid CHO may be more tolerable than
solid) and practicality of their fueling plan. Fueling chances may vary according to rules of sport,
e.g., halftimes during games, minimal/no fueling opportunity during swim portion of triathlon vs.
ideal opportunity during bike, etc., and should be rehearsed. We also recommend athletes should
practice their fueling plan at race/game intensity, as GI tolerability can be decreased on race day
due to the increased stress response and sympathetic/parasympathetic imbalance on “game day.”
Another important clinical consideration is in hot conditions; clinicians should counsel athletes to
reduce CHO intake by 10% due to lowered CHO oxidation rates in hot environments [11].
In recent years, some athletes have manipulated their carbohydrate levels using a “train low”
strategy involving lower intakes of CHO and higher intakes of fat. Periodically training in low
glycogen/low glucose availability states may stimulate upregulation of fat oxidation pathways,
spare glycogen stores, and may prolong time to exhaustion [
12
,
19
,
20
]. This low glucose state may
be of advantage in ultra-endurance events where exercise is typically under 70% VO
2max
and fuel
sources are predominantly fats. Some athletes then decide to carbo load just prior to the event, so that
they can in essence “train low, race high”: maximize both fat oxidation pathways at lower intensities
(<70% VO
2max
) and glucose oxidation pathways at higher intensities (>70% VO
2max
). However,
prolonged time spent in “train low” may reduce ability to generate maximal power in high-intensity
situations [
12
,
19
]. In the authors’ clinical experience, “train low” may improve oxidative enzymes,
but an athlete’s tolerability to maintain their training load decreases, and their quality of workouts and
quality of their overall training stress (and therefore adaptation) declines. The hope is that by training
in a low CHO state, the potential benefits from increasing fat oxidative enzyme pathways outweigh
the negative effects of the lowered training load and training adaptations when racing in the high
Nutrients 2019, 11, 1289 5 of 20
glucose state. In other words, “train low” may help improve an athlete’s “low gears” (maximizing fat
oxidation) for prolonged exercise at lower intensities, but at the expense of losing the athlete’s “high
gear” (maximal glucose oxidation) often needed during race situations. In addition, “train low” may
adversely affect other types of training such as altitude training and consequently adaptation [
21
,
22
].
Furthermore, many of the “train low” studies are in a laboratory setting and not in a “real world”
race situation. An interesting study by Cox et al. showed that while “train low” induced changes in
mitochondrial enzyme activity (e.g., citrate synthase), there was no performance difference in actual
exercise situations with either trained cyclists or triathletes involving steady-state exercise and time
trial cycling [
23
]. Therefore, many suggest it could be a “tool in the tool belt” as part of an athlete’s
overall training and nutrition plan but should not be employed in high-intensity training or race
situations due to performance concerns [12,19].
Another recent technique is utilizing a CHO mouth rinse during endurance exercise [
18
,
21
] as a
way to stimulate taste receptor cells and the central nervous system (CNS) to improve performance,
without actual ingestion of CHO. A proposed mechanism of action is that it modulates the central
governor theory [
13
], a CNS-established safe level of exertion during exercise to preserve an emergency
reserve margin. The question was originally posed by Jeukendrup [
24
], who demonstrated time trial
cycling performance improvements with glucose compared to placebo even in short-term (1 h) exercise.
In his discussion, he concluded that it was unlikely CHO ingestion exerts its beneficial effect through
its contribution to energy expenditure as only about 10–20% of ingested CHO is actually oxidized in
the first hour of exercise, so “the explanation for this increased performance remains to be established.”
Some proposed that it was simply the CHO presentation in the oral cavity that stimulated the CNS.
A later study by Carter supports this showing that even an intravenous infusion of glucose during
a 1 h time trial, despite increases in plasma glucose for oxidation and evidence of increased glucose
uptake into the tissues, had no effect on 1-h cycling time trial performance [
25
]. A follow up study by
the same group showed even a CHO mouth rinse (without ingestion) has a positive effect on 1 h time
trial performance [
26
] and is likely mediated by CHO receptors in the mouth associated with CNS
motivation pathways. A systematic review demonstrated that rinsing every 5–10 min (of at least 5–10 s
of oral contact) with a 6.4–10% carbohydrate solution may improve performance by ~2–3% [
21
] in high
intensity (>70% VO
2max
) exercises bouts of up to 1 h. We therefore suggest that for athletes with GI
distress during high-intensity exercise that precludes actual oral carbohydrate intake, this strategy
may be of value if the event is 1 h or less. However, any exercise of ~2 h or more, formal carbohydrate
ingestion is imperative for performance [
18
] and only mouth rinsing without carbohydrate ingestion is
not recommended.
In summary, daily CHO requirements vary according to level of exercise, from 5–7 g/kg/day
(1 h/day of moderate exercise), 6–10 g/kg/day (1–3 h/day of exercise), to 8–12 g/kg/day (4
≥
h/day of
exercise). Pre-competition (“Loading”) recommendations also vary according to duration of exercise,
from 6 g/kg/day (<90 min of exercise) to 10–12 g/kg/day (>90 min of exercise) with a 1–4 g/kg final
“top-off” 1–4 h prior to event. During competition (“Fueling”) requirements similarly range from
30–60 g/h for <2.5 h of exercise, 60–70 g/h if >2.5 h of exercise, and up to 90 g/h for >2.5 h of exercise
(if tolerable). As daily, pre-exercise, during exercise, and post-exercise CHO requirements are tiered
to exercise level and can become confusing to the athlete, Table 1 provides a concise reference on
the above CHO requirements. Post-exercise refueling of CHO is also a complex topic and separately
discussed below in “Recovery Nutrition” and also outlined in Table 1.
3.2. Protein
Traditionally, endurance athletes have placed less of a priority on protein in comparison
to carbohydrate. However, adequate protein intake and timing of intake are critical to any
athlete, whether endurance or resistance trained. An outdated model is simply following nitrogen
balance, which was originally designed to prevent nutrient deficiency, not optimize performance.
Nutrients 2019, 11, 1289 6 of 20
Athletes require higher protein intakes [
27
] than the current Recommended Daily Allowance (RDA) of
0.8 g/kg/day in order to achieve training adaptations and improve performance [27,28].
Table 1.
Key recommendations for macronutrients, hydration, and supplements (exercise duration is
listed in italics within parentheses).
Nutrient Daily Requirements Pre-Exercise During Exercise Post-Exercise
Carbohydrate
5–7 g/kg/day (1 h/day)
6–10 g/kg/day (1–3 h/day)
8–12 g/kg/day (4≥ h/day)
6 g/kg/day (<90 min)
10–12 g/kg/day (> 90
min) + 1–4 g/kg (1–4 h
prior to event)
30–60 g/h (<2.5 h)
60–70 g/h (>2.5 h)
90 g/h (>2.5 h, if
tolerable)
8–10 g/kg/day (first 24 h)
1.0–1.2 g/kg/h (first 3–5 h)
or 0.8 g/kg/h + protein
(0.3 mg/kg/h) or caffeine
(3 mg/kg)
Protein
1.4 g/kg/day
0.3 g/kg every 3–5 h
0.3 g/kg immediately
prior (or post–exercise)
0.25 g/kg/h (if high
intensity/eccentric
exercise)
0.3 g/kg within 0–2 h (or
pre-exercise)
Fat
Do not restrict to <20% total caloric energy
Unclear role of CLA, omega-3, MCT supplements
Consider limiting fat intake only during carbohydrate loading, or pre-race if GI comfort concerns
Water
Try initial hydration plan at ~400–800 mL/h;
Adjust according to individual athlete variations (sweat rates, sweat sodium
content, exercise intensity, body temperature, ambient temperature,
bodyweight, kidney function)
Follow thirst mechanism, monitor parameters (bodyweight, urine color)
Replace fluid with 150%
of fluid lost
Sodium
Try initial sodium plan at 300–600 mg/h if high sweat rate (>1.2 L/h),
subjective “salty sweater,” or prolonged exercise >2 h
Adjust intake according to individual athlete variations (sweat rates, sweat
sodium content, exercise intensity, body temperature, ambient temperature,
bodyweight, kidney function)
Improved water
repletion observed with
>60 mmol/L sodium
content (~1380 mg/L)
Nitrates
300–600 mg of nitrate (up to 10 mg/kg or 0.1 mmol/kg) or 500 mL beetroot juice or 3–6 whole beets within
90 min of exercise onset
Consider multi-day dosing e.g., 6 days of a high-nitrate diet prior to event
Antioxidants
Avoid prior to exercise to maximize training adaptation
Take prior to exercise only if recovery needed within 24 h
Many options: whole foods, dark berries, dark greens, green tea
e.g., 8–12oz tart cherry juice twice a day (1oz if concentrate) 4–5 days prior and 2–3 days after event e.g.,
green tea extract (270–1200 mg/day)
Caffeine
3–6 mg/kg taken 30–90 min prior to exercise
Consider “topping-up” every 1–2 h as needed
≥
9 mg/kg does not further enhance performance, may have undesirable side
effects, + drug test
≤3 mg/kg can also be ergogenic without side effects
3 mg/kg with
carbohydrate enhances
glycogen repletion
Probiotics Lactobacillus and Bifidobacteria may help with upper respiratory and/or GI symptoms
3.2.1. Daily Protein Requirements
The AND, DC, and ACSM all recommend protein ingestion for athletes in the range of
1.2–2.0 g/kg/day [
8
], with the ISSN recommending 1.4–2.0 g/kg/day [
9
]. Strength and power
athletes are typically recommended to consume in the higher range and endurance athletes the
lower range, based on individual needs. Temporary ingestion of higher quantities during intense
training may provide additional benefit [
9
,
27
]. Muscle protein synthesis (MPS) is upregulated for
24 h following exercise and is due to the increased sensitivity to oral protein intake during this
time [
8
,
29
]. This increased absorption provides an ideal time to optimize protein intake in order
to maintain muscle mass after endurance exercise, as prolonged endurance exercise may induce
a catabolic state and resultant muscle breakdown [
8
,
9
,
30
]. Timing and dose are also shown to be
important; 0.25–0.3 g/kg of a quality protein source (see below) in the immediate 0–2 h post exercise
provides approximately 10 g of essential amino acids (EAA) (which maximally stimulate MPS and
the MPS associated signaling proteins mTOR, p70s6k, Akt needed for protein synthesis) [
8
,
9
,
28
,
30
].
Of note, either 0–2 h post-exercise or immediate pre-exercise protein intake both yield similar benefits
Nutrients 2019, 11, 1289 7 of 20
(in non-ultra-endurance activities) [
9
,
30
]. Clinicians can educate athletes regarding this useful fact and
let the decision be a matter of athlete preference and GI tolerance.
Athletes may think “more is better” and increase protein beyond recommendations. Daily intake
of protein above the recommended level (1.2–2.0 g/kg/day and/or individual meals/doses beyond
~0.3 g/kg) have not been shown to be additionally beneficial, and MPS can only be stimulated with
doses at least 3–5 h apart [
8
]. Temporary increases beyond 2.0 g/kg/day may be beneficial during short
periods of intensified training beyond the athlete’s typical program, but routine higher total daily
protein intake beyond this does not further benefit endurance athletes. In one study, 1.5 g/kg/day
compared to 3.0 g/kg/day while keeping carbohydrate intake the same, did not result in improved
endurance performance [
4
]. Therefore, the AND, DC, and ACSM recommend spreading protein dosing
at ~0.3 g/kg every 3–5 h throughout the day [8].
3.2.2. Pre-, During, and Post-Exercise Protein Requirements
Compared to resistance exercise, few studies have been done on pre- and during exercise protein
intake with endurance activities, but available evidence shows it may improve same day and next
day endurance performance [
30
]. In addition, importantly to competitive athletes, no studies have
shown it hinders performance [
30
]. Exhaustive endurance exercise and significant eccentric activities
e.g., marathons, downhill running, and obstacle course races can result in catabolism of muscle,
especially in the setting of inadequate protein or reduced energy availability and does raise muscle
creatine kinase levels (a marker of muscle damage) [
8
,
9
,
11
]. If tolerable, the athlete may therefore
consider a pre-exercise dose of 0.3 g/kg protein according to GI tolerance. During endurance exercise
(if particularly intense or significant eccentric exercise), approximately 0.25 g/kg protein per hour when
taken along with carbohydrate is recommended by the ISSN to minimize potential muscle damage [
9
].
This can reduce creatine kinase elevations, improve subjective feelings of muscle soreness, and may
increase MPS and net protein balance [
9
,
11
]. Post-exercise protein added to carbohydrate can increase
muscle glycogen synthesis by 40–100% if in the setting of suboptimal post-exercise carbohydrate intake
(i.e., <1 g/kg/h), however will not further increase glycogen synthesis if the athlete already has high
carbohydrate intake (>1.2 g/kg/h) [11].
Traditionally, proteins containing branched-chain amino acids (BCAAs leucine, isoleucine,
and valine) have garnered much attention in both popular media and research due to their role
in protein metabolism, nerve function, and glucose/insulin regulation. However, in recent years,
protein with higher EAA and leucine content (700–3000 mg) have emerged to be the ideal source to
stimulate MPS [
9
]. Branched-chain amino acid supplementation still may help endurance athletes via
central governor theory modulation [
13
]. BCAAs compete with tryptophan for transport across the
blood brain barrier, and increased tryptophan may increase serotonin and contribute to feelings of
fatigue [
13
]. However, BCAA supplements alone if not taken with a complete protein (i.e., adequate EAA
content) may not adequately stimulate MPS [
9
]. Therefore, the authors suggest educating athletes on
EAA (which contain BCAA) protein sources rather than solely BCAA which still pervade lay texts and
popular media.
Many athletes (endurance and resistance athletes alike) continue to debate with passion their
“go to” protein source, and part of the argument may relate to internal feelings and/or culture regarding
their chosen diet (e.g., vegan, vegetarian, paleo, Mediterranean, flexitarian, the pesco-pollo-ovo-lacto
vegetarian spectrum, etc.). From a scientific standpoint, dairy-based proteins (whey, casein and whole
milk), lean meats, egg, and soy all stimulate MPS effectively [
8
]. However dairy-based proteins may be
superior to other sources due to the higher leucine content and improved digestion/absorption kinetics
of the EAAs found in liquid-based dairy foods [8].
In summary, protein doses of 0.3 g/kg (or ~20–40 g of protein covering the range of typical athlete
builds), provides ~10–12 of EAA and ~1–3 g of leucine. When taken every 3–5 h spread throughout
the day (including a dose immediately before or 0–2 h post-exercise) to a total of ~1.2–2.0 g/kg/day,
this strategy may promote positive nitrogen balance and optimally benefit endurance athletes.
Nutrients 2019, 11, 1289 8 of 20
3.3. Fat
In comparison to carbohydrate, proper fat intake gathers less consideration by endurance athletes
but is a worthy fuel source (oxidation of glycogen provides only ~2500 kilocalories of energy before
depletion, whereas oxidation of fat provides at least 70,000–75,000 kilocalories of energy, even in
a lean adult [
31
]). While the prototypical endurance athlete may prefer a carbohydrate-based diet
due to the above explained benefits in the previous section, some ultra-endurance athletes have
recently become interested in ketoadaptation (becoming “fat-adapted,” or “training low”) with a
high fat, low carbohydrate diet [
32
]. This renewed interest is based on the higher oxidation of
fat vs. glucose in lower intensity (<70% VO
2max
) exercise states typically seen in ultra-endurance
events [
19
]. In the “train low” state of low carbohydrate availability, upregulation of lipid oxidation
pathways does occur (such as citrate synthase and 3-hydroxyacyl-CoA dehydrogenase (3HAD)),
albeit at the expense of carbohydrate metabolism downregulation [
8
,
19
,
32
]. If performance is not an
issue, becoming fat-adapted and exercising at low (<70% VO
2max
) intensities therefore may improve
lipolysis and promote weight loss in the overweight athlete. However, if the athlete’s focus is on racing
and improving performance times, a high fat, low carbohydrate diet restricts that athlete’s ability to
train and race and higher intensities [8] and may negatively affect their race outcome [8,12,19].
This is not to say that fat intake is irrelevant to athletes; fats are fundamental components
of cell membranes, playing roles in signaling and transport, nerve function, providing insulation
and vital organ protection, and are the source of essential dietary fatty acids [
33
]. Athletes who
chronically restrict fat to <20% of total energy are at risk of low intake of fat-soluble vitamins and
carotenoids, essential fatty acids including n-3 (omega-3) fatty acids [
8
,
33
], and possibly conjugated
linoleic acids (CLA).
Conjugated linoleic acids are isomers of the essential n-6 linoleic acid, synthesized in the
gut by bacteria and supplied in dairy products and ruminant meats (cow, sheep, goat, deer) [
32
].
Limited evidence shows that CLA may inhibit atherogenesis and carcinogenesis [
32
], important for
athlete general health. Furthermore, and relevant to endurance athletes seeking to maintain body
weight, CLA may reduce adipocyte uptake of lipids [
32
]. Knowledge of CLA’s effects on endurance
exercise is currently limited and often conflicting, and most research has been on overweight subjects.
In one placebo-controlled study, CLA at 0.9 g/day for 14 days significantly increased exercise time to
exhaustion and tended to decrease perceived exertion in athletes [
34
], while 0.8 g/day for 8 weeks in
another study showed no effect on time to exhaustion, VO
2max
, or body composition in healthy young
men [
35
]. The ISSN acknowledges that while CLA animal studies are impressive, human studies are
not yet convincing and currently considers CLA to have little evidence regarding supplementation [
36
].
Conjugated linoleic acids at higher doses (up to 6 g/day) and omega-3 rich fish oil supplementation
may play a role in testosterone biosynthesis [
27
]. Proposed fish oil and CLA mechanism of action
is to modulate CYP17A1 and HSD3B2 enzymes which decreases glucocorticoid metabolism and
increases androgen pathway sex hormone metabolism [
37
]. This effect overall promotes an anabolic
environment, important to endurance athletes who are susceptible to declines in testosterone seen with
overtraining [
37
]. This point should especially be considered as a possible supplementation option in
endurance athletes during periodization training at exceptionally high intensity training times or any
athlete who is overreaching or overtrained and thereby risking testosterone suppression.
Medium-chain triglycerides (MCTs) have also gained attention in recent years, as MCTs can
directly enter mitochondria and be used for energy via beta-oxidation [
36
]. This in theory provides the
athlete with a readily available fat source for energy and thereby sparing glycogen [
36
]. While some
studies suggest improved cycling performance with MCTs, other studies actually show ergolytic effects
when taking MCTs versus carbohydrate, and furthermore most studies report GI complaints [
36
];
the ISSN currently considers MCTs in the category of “little to no evidence to support efficacy and/or
safety” [36].
Endurance athletes are encouraged to follow public health guidelines to ensure adequate fat
intake, and only consider limiting fat intake pre-race during a CHO loading phase or pre-race if
Nutrients 2019, 11, 1289 9 of 20
there are GI comfort concerns [
8
]. Conjugated linoleic acids, fish oil, and MCTs may have promise,
but further studies are needed to specifically define their role in endurance athletes.
3.4. Hydration
Fluid intake recommendations for endurance athletes have evolved [
38
–
40
]. Traditionally,
athletes were told by coaches and other training staff that thirst is not a good indicator of hydration status.
The theory espoused was that “once you’re thirsty you’re already dehydrated.” In a 1969 landmark
study by Wyndham [
41
] assessing marathon participants in two endurance races, individuals who lost
>2% of their body weight had elevated rectal temperatures, putting them at risk for hyperthermia.
This prompted several individuals to suggest increasing fluid intake under the presumption that
the thirst mechanism is an inadequate indicator of hydration. Interestingly however, the winner
in both events of the Wyndham study actually had the highest overall rectal temperature and was
asymptomatic at the end of the race. In retrospect this should have prompted further thought as not
being as serious a health risk as believed. As late as 1996 the ACSM noted in their fluid replacement
position stand [
38
] that “perception of thirst...cannot be used to provide complete restoration of water
by sweating” and that “athletes should start drinking early and at regular intervals...or consume the
maximal amount that can be tolerated.”
Consequently, athletes have historically tried to stay ahead of dehydration and drank before they
were thirsty. However as clinical observations of overhydration mounted, the dangers became clearer.
In the Boston marathon [
42
], an alarming 13% of finishers had hyponatremia which was even considered
an underestimation, and 0.6% (90 finishers) were critical (
≤
120 mmol/L). Excessive consumption of
fluids was the single most important risk factor in development of hyponatremia [
42
]. Lighter and
slower runners are also at risk of positive fluid balance [
43
]. Exercise-associated hyponatremia (EAH)
is used to describe hyponatremia occurring during or within 24 h after physical activity. It is defined by
a serum, plasma, or blood sodium concentration below the reference laboratory range, which for most
laboratories is <135 mmol/L [
44
]. Exercise-associated hyponatremia is serious and one of the potential
causes of exercise-associated collapse [
45
] which can be fatal [
42
]. While sometimes asymptomatic,
EAH can result in a myriad of signs and symptoms mimicking other conditions, including confusion,
dyspnea, nausea, delirium, even coma and death [
39
,
45
]. In the authors’ clinical experience, it is often
nonspecific and GI complaints may be the primary presenting symptom.
Noakes et al., helped bring EAH to the forefront with studies on ultra-endurance athletes
demonstrating the pathophysiology of EAH including voluntary hyperhydration, increased sweat
sodium loss, and loss of normal anti-diuretic hormone (ADH) suppression, called the syndrome
of inappropriate ADH secretion (SIADH) [
39
,
46
]. Since the excretory capacity of the kidneys is
~800–1000 mL/h and fluid loss from exercise is estimated at an additional ~500 mL/h, in theory an
athlete could conceivably consume up to 1.5 L/h without theoretical water retention [
39
]. However,
dilution of serum sodium causing EAH commonly occurs at much lower water intake rates, placing the
athlete at risk [
39
,
45
]. For practical recommendations, clinicians can explain to the athlete if he/she
were to consume 1 L of fluid at rest, it would most likely simply be excreted with normally functioning
kidneys. During exercise however, even small increases in ADH can markedly reduce kidney excretory
capacity, thereby causing the athlete to retain fluid even if drinking less than 800–1000 mL/h [
44
].
The stimuli for SIADH include nausea/vomiting, hypoglycemia, hypotension, interleukin-6 (IL-6)
release, and hyperthermia, all of which can occur with prolonged exercise [
44
,
45
]. Athletes are advised
to monitor for SIADH stimuli e.g., nausea although as mentioned above, clinical symptoms of EAH
may be nonspecific.
It was not until Noakes’ pivotal study in 2003 where the dangers of over-drinking were clearly
described, and recommendations were updated [
47
]. The Advisory Statement by Noakes and the
International Marathon Medical Directors Association suggest the athlete start with a hydration
plan in the range of 400–800 mL/h [
47
], which was also adopted in the ACSM Position Stand in
2007 [
40
] recommending athletes drink ad libidum, in the suggested range of 400–800 mL/h. However,
Nutrients 2019, 11, 1289 10 of 20
a hydration plan is individual to each athlete, and varies with sweat rates, sweat sodium content,
intensity of exercise, body temperature and ambient temperature, bodyweight, kidney function,
and many other factors. The ACSM suggests higher hydration rates for faster, heavier athletes
competing in warm environments, and lower rates for slower, lighter athletes competing in cooler
environments [
40
]. More specifically, a simulation study shows a 600 mL/h rate may be appropriate for
a 70 kg athlete in cool or temperate (18
◦
C) running at speeds of 8.5–15 km/h [
48
]. However, it may
produce overhydration in a 50 kg athlete running
≤
10 km/h, or dehydration in a 90 kg athlete running
≥
12.5 km/h. All athletes risk dehydration in warmer (28
◦
C) environments, however 50 kg athletes still
risk overhydration at higher (800 mL/h) intakes and lower (
≤
12.5 km/h) speeds [
48
], further supporting
that lighter slower runners are at increased risk and a hydration plan should be individualized [43].
Similarly, a sodium intake plan needs to be customized to an athlete’s experience, sweat rate and
sweat sodium content, exercise intensity and environmental conditions. The AND, DC, and ACSM
all recommend sodium ingestion during exercise in athletes with high sweat rates (>1.2 L/h),
subjective “salty sweaters,” and prolonged exercise >2 h [
9
]. Although widely variable, average sweat
rates range from 0.3 to 2.4 L/h [
9
] and the average sodium sweat content is 1 g/L (50 mmol/L) [
9
].
A sports drink containing sodium in the range of 10–30 mmol/L (230–690 mg/L) results in optimal
absorption and prevention of hyponatremia [
11
], a concentration found in typical commercial sports
drinks. The ACSM recommendations for sodium intake during exercise is to start with ~300–600 mg/h
(1.7–2.9 g salt) during a prolonged exercise bout and adjust intake accordingly [
36
]. Post-exercise fluid
and sodium repletion recommendations are discussed in Recovery Nutrition section below.
Therefore, following the instinctive thirst mechanism and monitoring bodily parameters such
as body weight, urine color, race pace, body temperature, and environmental temperature with each
workout can help the athlete fine tune their individual hydration needs and avoid complications
of EAH [
19
]. Further advice for the overdrinking athlete could include presenting the dichotomy
illustrated in the 2007 ACSM position stand: while dehydration can impair exercise performance and
contribute to heat illness or exacerbate exertional rhabdomyolysis, exercise-associated hyponatremia
can produce grave illness or even death [40].
3.5. Supplements and “Hot Topics”
3.5.1. Nitrates
Dietary nitrate has been used for years in medical conditions such as cardiovascular disease and
hypertension [
49
]. It has gained significant attention in the endurance athlete population after a pivotal
2007 study [
50
] by Larsen that showed a decreased oxygen cost for submaximal exercise workloads.
Since then several publications have surfaced: a PubMed search on “nitrate supplementation exercise”
yielded only 52 publications in the previous 10 years (2004–2013), but over 180 publications in the last
5 years (2014–2018). Certain vegetables such as beets, and beetroot juice, contain high levels of inorganic
nitrate (NO3
−
). Once consumed, NO3
−
is converted to NO2
−
by oral bacteria, and then to nitric
oxide (NO) in the gut [
51
,
52
]. Nitric oxide has numerous bodily effects relevant to endurance athletes,
ranging from vasodilation, blood flow and O
2
regulation in working muscle, mitochondrial respiration
and biogenesis, glucose uptake, and overall muscle contraction/relaxation
[49,51,52]
. Cumulatively,
these effects can improve muscle economy, efficiency and mitigate fatigue, positively impact
cardiorespiratory performance by decreasing effort at submaximal workloads, and in some studies
improve time trial performance (albeit mainly in non-elite athletes) [12,51–53].
Beetroot juice specifically (compared to other forms of dietary nitrate) has been studied in
athletes. If taken up to 2–3 h prior to endurance exercise it can reduce oxygen cost during exercise,
may improve time to exhaustion, cardiorespiratory performance at anaerobic threshold, and VO
2max
[
45
].
Results however are currently mixed and sometimes contradictory; many positive studies are on
subjects of 10 or fewer, and effects may be less pronounced or not even benefit already trained/elite
athletes due to their nutrition plan (already containing adequate nitrate) and/or improved metabolic
Nutrients 2019, 11, 1289 11 of 20
efficiency from maximizing training adaptations [
12
,
53
]. Furthermore, multi-day high nitrate intake
or supplementation may help raise nitrate levels and improve performance compared to a control
diet. In one study, 6 days of a high nitrate diet (8.2 mmol/day from vegetables and fruits) compared to
a control diet (2.9 mmol/day) induced a significant rise in plasma nitrate and was associated with a
reduced oxygen cost during moderate intensity cycling, higher muscle work during high-intensity
fatiguing leg exercise, and improved performance during repeated sprints [
54
]. This study may help
further explain the variability in results with acute single-day supplementation, and help the athlete
target healthy nitrate intake levels.
Dosing also varies, and in studies typically ranges from either 300–600 mg of nitrate supplement and
up to 10 mg/kg, 0.1 mmol/kg with minimum 6–8 mmol total, 500 mL of beetroot juice, or approximately
3–6 whole beets [
12
,
36
,
51
]. Timing may also play a role in the variability of results. Recent data show
that beetroot juice consumption should ideally commence within 90 min of exercise rather than 2–3 h
prior as in earlier studies, since NO levels peak at 2–3 h and then sharply fall leaving the athlete
in a potentially suboptimal time interval for exercise [
51
,
55
,
56
]. Manner of ingestion must also be
considered when interpreting study results. Mouth rinse, oral antiseptics, or limited nitrate supplement
oral contact time can all limit NO3
−
to NO2
−
conversion [
12
,
19
,
51
]. Since 500 mL of beetroot juice
pre-race can have significant GI distress in some athletes (and may contribute to overhydration),
beetroot juice concentrate, powders, and “shots” have been commercially developed and may be
an option.
A few commonly missed practical points are worth mentioning. One is the significant expense of
commercial nitrate or beet supplements. Athletes could consider just eating sufficient high-nitrate
vegetables or actual beets which supply similar levels of nitrates. In the Larsen study the daily nitrate
dose used were in amounts achievable through a diet rich in vegetables, specifically “the amount
normally found in 150 to 250 g of a nitrate-rich vegetable such as spinach, beetroot, or lettuce” [
50
].
Additionally, in the authors’ experience nitrate supplements may become rancid if left out and powders
can easily harden with moisture rendering scooping impossible, so supplements should be tightly
sealed, refrigerated and kept out of direct light. Athletes should be alerted to the possibility of beeturia
and red bowel movements, which is normal [
52
]. Lastly, dietary nitrate supplements also mildly
lower diastolic and mean arterial blood pressure [
57
], which may be an issue in those with low blood
pressure, orthostasis, or at risk for hypotension.
3.5.2. Antioxidants
The role of antioxidant supplements in sport was notably questioned by Gomez-Cabrera [
58
–
61
]
who highlighted the potential blunting of the training adaptation response to exercise. Consuming high
doses of single antioxidants (such as vitamins C and E) may inhibit the signaling pathways normally
triggered by the oxidative stress of exercise during training. The pro-oxidant environment including
the buildup of reactive oxygen species (ROS) from exercise triggers adaptations in the form of
increased superoxide dismutase and glutathione peroxidase enzymes, muscle repair, and mitochondrial
biogenesis pathways [
58
–
62
]. While a healthy diet for athletes should naturally include a variety
of antioxidants, supraphysiologic high doses of single antioxidants may impair or prevent training
adaptations in endurance athletes and are not recommended. However, once an endurance athlete has
already peaked in training, and their main goal is timely recovery, a food or supplement containing a
variety of antioxidants (e.g., dark berries, dark leafy greens) may help to speed recovery and return
to competition [
62
]. In a review, tart cherry juice at 8–12 oz twice a day (or 1 oz if concentrate),
taken 4–5 days prior and 2–3 days after an event may promote recovery [
62
]. This may be useful for
multi-day endurance events such as cycling tours, multi-stage races, etc.
Green tea contains various bioactive phytochemicals, including high levels of the antioxidant
polyphenols epigalocatechin gallate (EGCG), catechin, epicatechin, epigalocatechin, and epicatechin
gallate (commonly known as catechins). The proposed health benefits of green tea are typically
attributed to its antioxidant properties that can scavenge ROS and free radicals associated with
Nutrients 2019, 11, 1289 12 of 20
many chronic diseases [
63
,
64
]. Relevant to endurance athletes, green tea extracts have been shown
to stimulate fat oxidation and weight loss at ranges of 270–1200 mg/day [
63
]. The catechins
work as a catechol-o-methyltransferase (COMT) inhibitor (potentiating effects of norepinephrine,
thermogenesis and fat oxidation) and phosphodiesterase inhibitor (preventing breakdown of cyclic
adenosine monophosphate (cAMP) which stimulates hormone-sensitive lipase) [
63
]. In a review,
green tea extract was shown to enhance fat oxidation and improve performance during endurance
exercise [
65
]. Furthermore, green tea extract’s effect is more pronounced with additional caffeine
supplementation [
65
,
66
]. Endurance athletes looking to maximize fat oxidation and spare glycogen
during longer, lower intensity events may find this valuable. Asian populations have higher
concentrations of high-activity COMT polymorphism than Caucasians, and so there may be a
population-specific effect in Asian populations [
67
]. Of note, few human studies exist regarding green
tea extract on athletic performance. Commonly referenced studies that claim an 8–24% increase in time
to exhaustion with swimming [
68
] and a 30% increase in time to exhaustion with running [
69
] due
to increased fat oxidation, while very impressive results, were actually animal studies. In a review
documenting later studies in humans, green tea has not shown a similar performance enhancement [
63
],
and the few studies that did suggest improvements were only in untrained sedentary populations.
Therefore, it remains to be seen if green tea catechins exert a significant performance effect on trained
and non-overweight athletes. Additionally, a final word of warning bears consideration: since the
methods of growing, harvesting, and preparing green tea vary widely (and any supplement may
contain contaminants or banned substances), athletes should exercise caution. When selecting green
tea, green tea extract, or any other supplement, the authors advocate to choose wisely from trusted
sources (e.g., Institute of National Anti-Doping Organizations, Council for Responsible Nutrition, UL
®
,
Informed-Choice.org) [70].
3.5.3. Caffeine
Caffeine, a popular supplement in the general population, has been heavily researched in sports
for its ergogenic effects. Caffeine is a trimethylxanthine, similar to adenosine in chemical structure [
71
].
It has numerous proposed mechanisms of action. Centrally, by blocking adenosine receptors in the CNS
it acts as a stimulant to increase neurotransmitter release [
72
,
73
], increases cognitive performance [
72
],
and suppresses pain by increasing
β
-endorphins [
72
,
73
]. Peripherally, caffeine increases motor
unit recruitment [
73
] and helps mobilize calcium to increase muscle contraction [
72
]. Systemically,
caffeine assists in mobilization of fatty acids for energy (decreasing dependence on glycogen) and
increases thermogenesis [
72
]. There is good consensus on dosage and timing; meta-analyses and
reviews [
72
,
73
] all recommend a moderate caffeine dose of 3–6 mg/kg 30–90 min prior to exercise to
maximize effects. This dosing can improve sustained maximal endurance (e.g., time trial) performance
and vigilance during endurance tasks [
72
]. Of additional practical importance is the synergistic
effect of caffeine when consumed with carbohydrate. Taking the two together improves cycling
work production compared to caffeine or carbohydrate alone, while perception of work remains
unchanged [
74
]. Of note in one study, the anhydrous form of supplemental caffeine may have a greater
ergogenic effect than drinking coffee [
75
], although in this study the caffeine capsule was actually
taken with water. Therefore, the authors question if practically this ultimately may be similar to
drinking coffee.
Higher caffeine doses of 9 mg/kg do not further enhance performance [
72
,
76
], and can result
in very undesirable side effects including GI distress, nervousness, confusion, disturbed sleep [
77
].
Athletes may also be concerned about severe or systemic side effects with this level of dosing. A recent
review proposes that caffeine does not result in more serious complications such as water-electrolyte
imbalances, dehydration, hyperthermia, or reduced exercise-heat tolerance [
78
]. However, doses above
9 mg/kg may result in urinary caffeine detection and considered above the doping threshold in many
professional sports organizations [
36
]. Fortunately, lower doses <3 mg/kg can be similarly ergogenic
Nutrients 2019, 11, 1289 13 of 20
in endurance cycling and running research, improving vigilance, mood, and cognitive function,
without any major side effects [77].
Traditionally, there has been a long-held paradigm that habitual caffeine intake may blunt the
ergogenic effects of acute pre-exercise caffeine consumption. Research has shown that the performance
benefit of caffeine lessens after 15–18 days of daily low dose (3 mg/kg) caffeine ingestion during
peak cycling power in Wingate and incremental exercise cycling tests [
79
]. By 4 weeks at the same
3 mg/kg dose the cycling performance benefit was no longer apparent in time trial performance [
80
].
However other research has shown that athletes with low, moderate, or even high habitual caffeine
intake exhibit similar absolute and relative improvements in cycling time-trial performance to an acute
6 mg/kg caffeine dose [81].
Furthermore, caffeine may also be helpful during prolonged (>2 h) exercise. In one study, upon a
2 h cycling at 60% VO
2max
interspersed with bouts of high-intensity (82% VO
2max
) exercise followed
by a cycling time-trial, athletes were given either low dose (1.5 mg/kg) or moderate dose (2.9 mg/kg)
caffeine at 80 min in to the cycling challenge. Both caffeine groups had faster time-trial completion
compared to placebo, and the moderate dose group had improved performance to a greater extent
than the low dose group [
82
]. This study suggests the concept of “topping-up” of caffeine periodically
during prolonged exercise, and therefore may also be helpful for ultra-endurance events.
The authors recommend that athletes begin at lower doses if they are not caffeine tolerant and
adjust accordingly. Some athletes find it useful to cycle caffeine with periods of abstaining from
coffee during lower intensity training or prior to races, then resuming coffee at race time or during
high intensity training. A safe starting dose may be up to 3 mg/kg. With daily caffeine intake, the
performance benefit begins to decline at about 15–18 days and may disappear by 4 weeks. For habitual
coffee drinkers an acute 6 mg/kg supplementation may be an option on race day if tolerated. Periodic
topping-up during prolonged exercise (authors suggest every 1–2 h as needed) may also be of benefit.
3.5.4. Probiotics
Probiotics are considered “live food ingredients” that provide a beneficial effect to the host
organism [
83
] and occur naturally in fermented foods such as yogurt, kimchee, sauerkraut, miso and
natto, or can be taken in supplement form. Most commonly Lactobacillus and Bifidobacteria are the
primary species used [
83
] and produce lactic acid from carbohydrates to provide the sour taste in
fermented foods. Probiotics have many proposed health benefits including antimicrobial activity
to improve diarrheal illness and reduce urogenital infection, assisting with lactose intolerance,
preventing constipation, improving immune function, and possibly even having anticarcinogenic
effects to the colon [
83
]. Endurance athletes are susceptible to upper respiratory infection (URI),
and elite athletes have a higher rate of URI than recreational athletes [
84
]. Probiotics may play a role
in reducing these symptoms [
85
]. The field of probiotic research in athletes is still in its early stages,
and few studies exist regarding performance outcomes [
86
]. In a review of the literature, only six
studies were found, and while two did show an ergogenic effect on performance, one study was in
mice [86].
A recent review in healthy physically active people and athletes showed probiotics may help with
reduction of GI and upper respiratory symptoms [
85
]. Endurance athletes when fatigued show similar
clinical characteristics of patients who experience reactivation of Epstein Barr virus (less T-cell secretion
of interferon gamma) and exhibit diminished natural killer cell activity [
83
]. Probiotic supplementation
can improve mucosal T-cell interferon concentration to normal levels and attenuate the reduction
in natural killer cell activity [
83
]. The probiotic strain, dose, period of consumption and form of
administration however (e.g., capsules, probiotic sachets, fermented food) likely play a role in its
effect; multiple strain probiotics, in the form of fermented food or sachet when taken for a longer
compared to shorter periods of time appear to show better results [
85
]. These benefits may help the
athlete in terms of comfort and recovery from exercise, and therefore indirectly may play a role in
Nutrients 2019, 11, 1289 14 of 20
performance. Endurance athletes prone to URI or GI symptoms, those susceptible to infection, or who
travel frequently for events and are exposed to travel-related illness, may especially find benefit.
3.5.5. Recovery Nutrition
A note should be made on the topic of recovery, as many athletes may not know of the
post-exercise nutritional “window of opportunity” to facilitate a timely recovery to pre-exercise
status. Carbohydrate and water have the most research, but the role of post-exercise protein, caffeine,
and antioxidants may have important impacts on endurance athletes. Studies have shown that high
carbohydrate (8–10 g/kg/day) refeeding can restore pre-exercise glycogen values within 24 h [
11
].
Aggressive carbohydrate refeeding at 1.2 g/kg/h for the first few hours post-exercise should be
implemented if glycogen repletion is needed quickly for another event with <4 h recovery time [
11
,
30
].
In these situations, high glycemic index foods (>70) are preferred [
30
]. Ideally, dosing at 15–30-min
intervals achieve the highest glycogen synthesis rates in the early first 3–5 h recovery period [
11
]. If an
athlete cannot tolerate this carbohydrate volume, the addition of caffeine (3 mg/kg, even up to 8 mg/kg
if no side effects) can boost glycogen repletion up to 66% more [30,87]. If the athlete can only tolerate
0.8 g/kg/h of carbohydrate, adding protein at 0.2–0.4 g/kg/h can also boost glycogen repletion [
30
,
87
].
Adding protein to carbohydrate intakes of
≥
1.2 g/kg/h does not further improve glycogen synthesis
however [
11
]. If the exercise had a significant eccentric component leading to significant muscle damage
(marathons, downhill running), post-exercise protein with a high leucine content (700–1300 mg) within
the first 2 h can stimulate MPS and recovery [
9
,
30
]. Similarly, eccentric and highly stressful exercise
bouts that raise free radical and ROS levels can delay recovery to peak form due to the excessive
oxidant load surpassing the innate antioxidant system [
58
–
61
]; ingestion of high antioxidant foods
such as tart cherry juice may improve recovery [62].
Long endurance bouts can challenge hydration status; fluid and therefore bodyweight loss is
expected with exercise and 0.1–3.0% bodyweight loss after exercise is still defined as euhydration
[44,45]
.
Typical recommendations are to replace fluid with 150% of fluid lost based on bodyweight, and more of
this fluid is retained when there is moderate to high sodium content (>60 mmol/L) [
11
]. This translates
roughly to >1380 mg of sodium/L, amounts significantly higher than in typical sports drinks.
Some athletes turn to salt packets or tablets, especially if they are “salty sweaters,” training in
hot environments, or have a history of exercise-associated muscle cramps [
12
]. However, the authors
caution this strategy in hypertensives or those needing to restrict total sodium intake. Interestingly,
addition of potassium does not show any additional rehydration benefit [11].
3.5.6. Concern with High Carbohydrate Diets?
There has been considerable discussion in both the medical literature and popular media [
88
,
89
]
regarding the recent trend of low carbohydrate diets. Much of this concern may stem from the
obesity epidemic, the high carbohydrate content and lack of adequate fruit and vegetable intake of
typical Western diets, and the lack of adequate physical activity/sedentary lifestyle of well-developed
countries [
90
]. This leads to an overabundance of fuel in the form of carbohydrate and difficulties
with “glucose disposal” in the absence of adequate exercise to “burn the excess fuel.” Additionally,
continual exposure to elevated blood glucose levels may lead to neurodegeneration [
89
]. Dementia has
even been colloquially referred to as “type 3 diabetes.” Athletes may worry what potential effects
consuming high glycemic meals or foods have on training-related metabolic responses and exercise
performance. This very question was addressed in the joint position statement by the AND, DC,
and ACSM: there is “Grade I—Good evidence” that neither the glycemic load nor glycemic index of
carbohydrate-rich meals affects metabolic or performance outcomes when conditions are matched for
carbohydrate and energy content [8].
Nevertheless, endurance athletes may find it useful to purposefully exercise in lower carbohydrate
availability states. This may not only be for health concerns but as part of a periodization training plan,
to enhance the training stimulus, or even improve mental toughness and “grit” [
91
] by exercising in
Nutrients 2019, 11, 1289 15 of 20
low carbohydrate states. “Grit” is a concept of mental toughness developed by Angela Duckworth [
91
]
that describes one’s passion and perseverance toward a goal and holding steadfast to that goal despite
barriers. Endurance athletes may experience this when exercising in difficult conditions, such as
bad weather and low fuel availability. Exercising in low carbohydrate states can be achieved in
several ways: for example, reducing total carbohydrate intake at certain times of their training plan,
training in a fasted state, performing two training sessions in close proximity without adequate
refueling, or simply early morning training before breakfast [
8
]. Since mental toughness can play a key
role in performance [
91
], the nutritional variables above could be considered by endurance athletes
and incorporated into an athlete’s mental training.
4. Discussion
The world of endurance nutrition is continually evolving, and clinicians need to keep up-to-date
as research emerges on sports nutrition topics. Furthermore, the commercial supplement industry is
ever-changing. New products with purported benefits are being advertised to athletes as well as the
general population, claiming improvements in performance and general health. Elite athletes, after they
maximize training adaptations, often look to gain marginal benefits that they believe may be pivotal in
whether they make the podium or not. They may take supplements and/or adopt new diets faster than
medical research can keep up to make sound recommendations. This paper therefore summarizes
the latest evidence-based recommendations as well as highlights hot topics and controversial subjects
in order to equip the clinician dealing with the endurance athlete with current knowledge. Table 1
summarizes the key recommendations for macronutrients, hydration, and supplements.
High carbohydrate diets have long been tested and continues to be recommended in endurance
athletes. Most endurance athletes are familiar with high carbohydrate diets, but the importance of
protein (both total daily intake and immediate post-exercise consumption) may not be as well-known
by athletes. Attention to adequate intake is emphasized to improve recovery, ameliorate muscle
damage, and maintain muscle mass. Fats recently have been gaining popularity again, especially with
ultra-endurance athletes, although “training low” with a high-fat diet may not necessarily improve
performance. There has been a shift away from forced hydration plans and personalizing fluid intake
according to thirst and sweat rates to avoid exercise-associated hyponatremia.
Athletes commonly take supplements, and a few supplements may have merit in the endurance
world. Nitrates may help reduce oxygen cost and improve time to exhaustion, possibly cardiorespiratory
performance at anaerobic threshold, and even VO
2max
. Studies are mixed however, and nitrate may
preferentially benefit non-elite recreational athletes. Antioxidants may help an athlete who has already
peaked in terms of training adaptation, where the main goal is facilitating recovery and earlier return to
competition in multi-stage events. Caffeine has a very large body of research behind its ergogenic effects,
with side effects being the main limiting factor. There is a paucity of quality research on probiotics
for athletes, but chronic URI and GI symptoms common in endurance athletes may potentially be
attenuated with Lactobacillus and Bifidobacteria supplementation. Additionally, as with any supplement,
since the US Food and Drug Administration (FDA) is not authorized to review dietary supplement
products for safety and effectiveness before they are marketed, there is the risk of contaminants and
illicit substances in commercial supplements. These substances may not only present a safety risk
but may be on a banned substance list for professional athletes [
92
]. While it is recommended that
athletes obtain nutrition from whole foods, we acknowledge that athletes may take supplements and
recommend they choose from trusted sources.
We hope this review helps clinicians treating and counseling endurance athletes clear
up misconceptions athletes may have regarding sports nutrition and provide evidence-based
recommendations according to current research. In the absence of high-quality evidence, we also
provide practical recommendations on select supplements and offer our clinical advice on specific
topics based on years of treating endurance athletes. Future research may help shed new light on
the potential pleotropic benefits of probiotics, fats including CLA, fish oil, and MCTs, more clarity of
Nutrients 2019, 11, 1289 16 of 20
the roles of nitrates and antioxidants, and the ideal balance of low vs. high carbohydrate intake to
optimize both general athlete health and athletic performance.
Author Contributions:
Conceptualization, methodology, software, K.V.; Analysis, investigation, resources,
data curation, K.V. and A.G.; writing—original draft preparation, K.V.; writing—review and editing, K.V. and
A.G.; supervision, A.G.
Funding: This research received no external funding.
Conflicts of Interest: The authors declare no conflict of interest.
References
1.
Behind USAT and Ironman’s Efforts to Grow the Sport. March 2017. Available online: https://www.triathlete.
com/2017/03/lifestyle/behind-usat-ironmans-efforts-grow-sport_299133 (accessed on 25 May 2019).
2.
Shilton, A. Let’s Try a Triathlon—The New York Times. Available online: https://www.nytimes.com/guides/
well/triathlon-training (accessed on 2 April 2019).
3.
Miller, J.A. The Running Bubble Has Popped. (You Couldn’t Hear It in New York.)—The New York Times.
Available online: https://www.nytimes.com/2017/11/05/sports/ny-marathon-running.html (accessed on
2 April 2019).
4.
Costa, R.J.S.; Hoffman, M.D.; Stellingwerff, T. Considerations for Ultra-Endurance Activities:
Part 1—Nutrition. Res. Sports Med. 2019, 27, 166–181. [CrossRef] [PubMed]
5.
Nikolaidis, P.T.; Veniamakis, E.; Rosemann, T.; Knechtle, B. Nutrition in Ultra-Endurance: State of the Art.
Nutrients 2018, 10, 1995. [CrossRef] [PubMed]
6.
Ebell, M.H.; Siwek, J.; Weiss, B.D.; Woolf, S.H.; Susman, J.; Ewigman, B.; Bowman, M. Strength of
Recommendation Taxonomy (SORT): A Patient-Centered Approach to Grading Evidence in the Medical
Literature. AFP 2004, 69, 548. [CrossRef]
7.
U.S. Department of Health & Human Services, Agency for Healthcare Research and Quality.
Clinical Guidelines and Recommendations. Available online: https://www.ahrq.gov/professionals/clinicians-
providers/guidelines-recommendations/index.html (accessed on 25 May 2019).
8.
Jäger, R.; Kerksick, C.M.; Campbell, B.I.; Cribb, P.J.; Wells, S.D.; Skwiat, T.M.; Purpura, M.; Ziegenfuss, T.N.;
Ferrando, A.A.; Arent, S.M.; et al. International Society of Sports Nutrition Position Stand: Protein and
Exercise. J. Int. Soc. Sports Nutr. 2017, 14, 20. [CrossRef] [PubMed]
9.
Thomas, D.T.; Erdman, K.A.; Burke, L.M. Position of the Academy of Nutrition and Dietetics, Dietitians of
Canada, and the American College of Sports Medicine: Nutrition and Athletic Performance. J. Acad. Nutr.
Diet. 2016, 116, 501–528. [CrossRef]
10.
Spriet, L.L. New Insights into the Interaction of Carbohydrate and Fat Metabolism during Exercise. Sports Med.
2014, 44 (Suppl. 1), S87–S96. [CrossRef]
11.
Jeukendrup, A.E.; Jentjens, R.L.P.G.; Moseley, L. Nutritional Considerations in Triathlon. Sports Med.
2005
,
35, 163–181. [CrossRef] [PubMed]
12.
Getzin, A.R.; Milner, C.; Harkins, M. Fueling the Triathlete: Evidence-Based Practical Advice for Athletes of
All Levels. Curr. Sports Med. Rep. 2017, 16, 240–246. [CrossRef]
13.
Noakes, T.D. Physiological Models to Understand Exercise Fatigue and the Adaptations That Predict or
Enhance Athletic Performance. Scand. J. Med. Sci. Sports 2000, 10, 123–145. [CrossRef]
14.
Burke, L.M.; Hawley, J.A.; Wong, S.H.S.; Jeukendrup, A.E. Carbohydrates for Training and Competition.
J. Sports Sci. 2011, 29 (Suppl. 1), S17–S27. [CrossRef]
15.
Bergström, J.; Hermansen, L.; Hultman, E.; Saltin, B. Diet, Muscle Glycogen and Physical Performance.
Acta Physiol. Scand. 1967, 71, 140–150. [CrossRef] [PubMed]
16.
Bussau, V.A.; Fairchild, T.J.; Rao, A.; Steele, P.; Fournier, P.A. Carbohydrate Loading in Human Muscle:
An Improved 1 Day Protocol. Eur. J. Appl. Physiol. 2002, 87, 290–295. [CrossRef] [PubMed]
17.
Jeukendrup, A.E.; Moseley, L.; Mainwaring, G.I.; Samuels, S.; Perry, S.; Mann, C.H. Exogenous Carbohydrate
Oxidation during Ultraendurance Exercise. J. Appl. Physiol. 2006, 100, 1134–1141. [CrossRef] [PubMed]
18.
Jeukendrup, A. A Step Towards Personalized Sports Nutrition: Carbohydrate Intake During Exercise.
Sports Med. 2014, 44 (Suppl. 1), 25–33. [CrossRef] [PubMed]
Nutrients 2019, 11, 1289 17 of 20
19.
Getzin, A.R.; Milner, C.; LaFace, K.M. Nutrition Update for the Ultraendurance Athlete. Curr. Sports Med.
Rep. 2011, 10, 330–339. [CrossRef] [PubMed]
20.
Hansen, A.K.; Fischer, C.P.; Plomgaard, P.; Andersen, J.L.; Saltin, B.; Pedersen, B.K. Skeletal Muscle
Adaptation: Training Twice Every Second Day vs. Training Once Daily. J. Appl. Physiol.
2005
, 98, 93–99.
[CrossRef] [PubMed]
21.
Silva, T.d.A.e.; de Souza, M.E.D.C.A.; de Amorim, J.F.; Stathis, C.G.; Leandro, C.G.; Lima-Silva, A.E.
Can Carbohydrate Mouth Rinse Improve Performance during Exercise? A Systematic Review. Nutrients
2013, 6, 1–10. [CrossRef] [PubMed]
22.
Jeukendrup, A.E.; Chambers, E.S. Oral Carbohydrate Sensing and Exercise Performance. Curr. Opin. Clin.
Nutr. Metab. Care 2010, 13, 447–451. [CrossRef]
23.
Cox, G.R.; Clark, S.A.; Cox, A.J.; Halson, S.L.; Hargreaves, M.; Hawley, J.A.; Jeacocke, N.; Snow, R.J.; Yeo, W.K.;
Burke, L.M. Daily Training with High Carbohydrate Availability Increases Exogenous Carbohydrate Oxidation
during Endurance Cycling. J. Appl. Physiol. 2010, 109, 126–134. [CrossRef]
24.
Jeukendrup, A.; Brouns, F.; Wagenmakers, A.J.; Saris, W.H. Carbohydrate-Electrolyte Feedings Improve 1 h
Time Trial Cycling Performance. Int. J. Sports Med. 1997, 18, 125–129. [CrossRef]
25.
Carter, J.M.; Jeukendrup, A.E.; Mann, C.H.; Jones, D.A. The Effect of Glucose Infusion on Glucose Kinetics
during a 1-h Time Trial. Med. Sci. Sports Exerc. 2004, 36, 1543–1550. [CrossRef]
26.
Carter, J.M.; Jeukendrup, A.E.; Jones, D.A. The Effect of Carbohydrate Mouth Rinse on 1-h Cycle Time Trial
Performance. Med. Sci. Sports Exerc. 2004, 36, 2107–2111. [CrossRef]
27.
Phillips, S.M.; Van Loon, L.J.C. Dietary Protein for Athletes: From Requirements to Optimum Adaptation.
J. Sports Sci. 2011, 29 (Suppl. 1), S29–S38. [CrossRef]
28.
Phillips, S.M. Dietary Protein Requirements and Adaptive Advantages in Athletes. Br. J. Nutr.
2012
,
108 (Suppl. 2), S158–S167. [CrossRef]
29.
Burd, N.A.; West, D.W.D.; Moore, D.R.; Atherton, P.J.; Staples, A.W.; Prior, T.; Tang, J.E.; Rennie, M.J.;
Baker, S.K.; Phillips, S.M. Enhanced Amino Acid Sensitivity of Myofibrillar Protein Synthesis Persists for up
to 24 h after Resistance Exercise in Young Men. J. Nutr. 2011, 141, 568–573. [CrossRef]
30.
Kerksick, C.M.; Arent, S.; Schoenfeld, B.J.; Stout, J.R.; Campbell, B.; Wilborn, C.D.; Taylor, L.; Kalman, D.;
Smith-Ryan, A.E.; Kreider, R.B.; et al. International Society of Sports Nutrition Position Stand: Nutrient
Timing. J. Int. Soc. Sports Nutr. 2017, 14, 33. [CrossRef]
31.
Wilmore, J.H.; Costill, D.L.; Kenney, W.L. Fuel for Exercising Muscle: Metabolism and Hormonal Control.
In Physiology of Sport and Exercise, 4th ed.; Wilmore, J.H., Costill, D.L., Kenney, W.L., Eds.; Human Kinetics:
Champaign, IL, USA, 2008; ISBN-13: 978-0-7360-5583-3.
32.
Volek, J.S.; Noakes, T.; Phinney, S.D. Rethinking Fat as a Fuel for Endurance Exercise. Eur. J. Sport Sci.
2015
,
15, 13–20. [CrossRef]
33.
Institute of Medicine, Food and Nutrition Board. Total fat and fatty acids. In Dietary Reference Intakes for
Energy, Carbohydrate, Fiber, Fat, Fatty Acids, Cholesterol, Protein, and Amino Acids; Institute of Medicine (U.S.),
Ed.; National Academies Press: Washington, DC, USA, 2005.
34.
Terasawa, N.; Okamoto, K.; Nakada, K.; Masuda, K. Effect of Conjugated Linoleic Acid Intake on Endurance
Exercise Performance and Anti-Fatigue in Student Athletes. J. Oleo Sci. 2017, 66, 723–733. [CrossRef]
35.
Tajmanesh, M.; Aryaeian, N.; Hosseini, M.; Mazaheri, R.; Kordi, R. Conjugated Linoleic Acid Supplementation
Has No Impact on Aerobic Capacity of Healthy Young Men. Lipids 2015, 50, 805–809. [CrossRef]
36.
Kerksick, C.M.; Wilborn, C.D.; Roberts, M.D.; Smith-Ryan, A.; Kleiner, S.M.; Jäger, R.; Collins, R.; Cooke, M.;
Davis, J.N.; Galvan, E.; et al. ISSN Exercise & Sports Nutrition Review Update: Research & Recommendations.
J. Int. Soc. Sports Nutr. 2018, 15, 38. [CrossRef]
37.
Macaluso, F.; Barone, R.; Catanese, P.; Carini, F.; Rizzuto, L.; Farina, F.; Di Felice, V. Do Fat Supplements
Increase Physical Performance? Nutrients 2013, 5, 509–524. [CrossRef]
38.
Convertino, V.A.; Armstrong, L.E.; Coyle, E.F.; Mack, G.W.; Sawka, M.N.; Senay, L.C.; Sherman, W.M.
American College of Sports Medicine Position Stand. Exercise and Fluid Replacement. Med. Sci. Sports
Exerc. 1996, 28, i–vii. [CrossRef]
39.
Noakes, T.D.; Sharwood, K.; Speedy, D.; Hew, T.; Reid, S.; Dugas, J.; Almond, C.; Wharam, P.; Weschler, L.
Three Independent Biological Mechanisms Cause Exercise-Associated Hyponatremia: Evidence from 2,135
Weighed Competitive Athletic Performances. Proc. Natl. Acad. Sci. USA
2005
, 102, 18550–18555. [CrossRef]
Nutrients 2019, 11, 1289 18 of 20
40.
American College of Sports Medicine Position Stand. Exercise and Fluid Replacement. -PubMed-NCBI.
Available online: https://www.ncbi.nlm.nih.gov/pubmed/17277604 (accessed on 3 April 2019).
41.
Wyndham, C.H.; Strydom, N.B. The Danger of an Inadequate Water Intake during Marathon Running. S. Afr.
Med. J. 1969, 43, 893–896.
42.
Almond, C.S.D.; Shin, A.Y.; Fortescue, E.B.; Mannix, R.C.; Wypij, D.; Binstadt, B.A.; Duncan, C.N.; Olson, D.P.;
Salerno, A.E.; Newburger, J.W.; et al. Hyponatremia among Runners in the Boston Marathon. N. Engl. J.
Med. 2005, 352, 1550–1556. [CrossRef]
43. Chorley, J.; Cianca, J.; Divine, J. Risk Factors for Exercise-Associated Hyponatremia in Non-Elite Marathon
Runners. Clin. J. Sport Med. 2007, 17, 471–477. [CrossRef]
44.
Hew-Butler, T.; Ayus, J.C.; Kipps, C.; Maughan, R.J.; Mettler, S.; Meeuwisse, W.H.; Page, A.J.; Reid, S.A.;
Rehrer, N.J.; Roberts, W.O.; et al. Statement of the Second International Exercise-Associated Hyponatremia
Consensus Development Conference, New Zealand, 2007. Clin. J. Sport Med. 2008, 18, 111–121. [CrossRef]
45.
Krabak, B.J.; Parker, K.M.; DiGirolamo, A. Exercise-Associated Collapse: Is Hyponatremia in Our Head?
PM R 2016, 8 (Suppl. 3), S61–S68. [CrossRef]
46.
Noakes, T.D.; Goodwin, N.; Rayner, B.L.; Branken, T.; Taylor, R.K. Water Intoxication: A Possible Complication
during Endurance Exercise. Med. Sci. Sports Exerc. 1985, 17, 370–375. [CrossRef]
47.
Noakes, T.; IMMDA. Fluid Replacement during Marathon Running. Clin. J. Sport Med.
2003
, 13, 309–318.
[CrossRef]
48.
Montain, S.J.; Cheuvront, S.N.; Sawka, M.N. Exercise Associated Hyponatraemia: Quantitative Analysis to
Understand the Aetiology. Br. J. Sports Med. 2006, 40, 98–105. [CrossRef]
49.
Shaltout, H.A.; Eggebeen, J.; Marsh, A.P.; Brubaker, P.H.; Laurienti, P.J.; Burdette, J.H.; Basu, S.; Morgan, A.;
Dos Santos, P.C.; Norris, J.L.; et al. Effects of Supervised Exercise and Dietary Nitrate in Older Adults with
Controlled Hypertension and/or Heart Failure with Preserved Ejection Fraction. Nitric Oxide
2017
, 69, 78–90.
[CrossRef]
50.
Larsen, F.J.; Weitzberg, E.; Lundberg, J.O.; Ekblom, B. Effects of Dietary Nitrate on Oxygen Cost during
Exercise. Acta Physiol. Oxf. 2007, 191, 59–66. [CrossRef]
51.
Dom
í
nguez, R.; Cuenca, E.; Mat
é
-Muñoz, J.L.; Garc
í
a-Fern
á
ndez, P.; Serra-Paya, N.; Estevan, M.C.L.;
Herreros, P.V.; Garnacho-Castaño, M.V. Effects of Beetroot Juice Supplementation on Cardiorespiratory
Endurance in Athletes. A Systematic Review. Nutrients 2017, 9, 43. [CrossRef]
52.
McMahon, N.F.; Leveritt, M.D.; Pavey, T.G. The Effect of Dietary Nitrate Supplementation on Endurance
Exercise Performance in Healthy Adults: A Systematic Review and Meta-Analysis. Sports Med.
2017
, 47,
735–756. [CrossRef]
53.
Jonvik, K.L.; Nyakayiru, J.; van Loon, L.J.C.; Verdijk, L.B. Can Elite Athletes Benefit from Dietary Nitrate
Supplementation? J. Appl. Physiol. 2015, 119, 759–761. [CrossRef]
54.
Porcelli, S.; Pugliese, L.; Rejc, E.; Pavei, G.; Bonato, M.; Montorsi, M.; La Torre, A.; Rasica, L.; Marzorati, M.
Effects of a Short-Term High-Nitrate Diet on Exercise Performance. Nutrients 2016, 8, 534. [CrossRef]
55.
Clifford, T.; Constantinou, C.M.; Keane, K.M.; West, D.J.; Howatson, G.; Stevenson, E.J. The Plasma
Bioavailability of Nitrate and Betanin from Beta Vulgaris Rubra in Humans. Eur. J. Nutr.
2017
, 56, 1245–1254.
[CrossRef]
56.
McIlvenna, L.C.; Monaghan, C.; Liddle, L.; Fernandez, B.O.; Feelisch, M.; Muggeridge, D.J.; Easton, C.
Beetroot Juice versus Chard Gel: A Pharmacokinetic and Pharmacodynamic Comparison of Nitrate
Bioavailability. Nitric Oxide 2017, 64, 61–67. [CrossRef]
57.
Larsen, F.J.; Ekblom, B.; Sahlin, K.; Lundberg, J.O.; Weitzberg, E. Effects of Dietary Nitrate on Blood Pressure
in Healthy Volunteers. N. Engl. J. Med. 2006, 355, 2792–2793. [CrossRef]
58.
Gomez-Cabrera, M.-C.; Borr
á
s, C.; Pallard
ó
, F.V.; Sastre, J.; Ji, L.L.; Viña, J. Decreasing Xanthine
Oxidase-Mediated Oxidative Stress Prevents Useful Cellular Adaptations to Exercise in Rats. J. Physiol.
2005
,
567(Pt. 1), 113–120. [CrossRef]
59.
Gomez-Cabrera, M.-C.; Mart
í
nez, A.; Santangelo, G.; Pallard
ó
, F.V.; Sastre, J.; Viña, J. Oxidative Stress in
Marathon Runners: Interest of Antioxidant Supplementation. Br. J. Nutr.
2006
, 96 (Suppl. 1), S31–S33.
[CrossRef]
60.
Gomez-Cabrera, M.-C.; Domenech, E.; Romagnoli, M.; Arduini, A.; Borras, C.; Pallardo, F.V.; Sastre, J.;
Viña, J. Oral Administration of Vitamin C Decreases Muscle Mitochondrial Biogenesis and Hampers
Training-Induced Adaptations in Endurance Performance. Am. J. Clin. Nutr. 2008, 87, 142–149. [CrossRef]
Nutrients 2019, 11, 1289 19 of 20
61.
Gomez-Cabrera, M.-C.; Domenech, E.; Viña, J. Moderate Exercise Is an Antioxidant: Upregulation of
Antioxidant Genes by Training. Free Radic. Biol. Med. 2008, 44, 126–131. [CrossRef]
62.
Vitale, K.C.; Hueglin, S.; Broad, E. Tart Cherry Juice in Athletes: A Literature Review and Commentary.
Curr. Sports Med. Rep. 2017, 16, 230–239. [CrossRef]
63.
Bentley, D.J.; Ackerman, J.; Clifford, T.; Slattery, K.S.; Lamprecht, M. Green Tea Catechins and Sport
Performance. In Antioxidants in Sport Nutrition; Lamprecht, M., Ed.; CRC Press/Taylor & Francis: Boca Raton,
FL, USA, 2015; ISBN-13 978-1-4665-6757-3.
64.
Rourke, S. Drinking Tea: Are the Health Benefits Real? Available online: http://www.medscape.com/
viewarticle/907456 (accessed on 3 April 2019).
65. Kim, J.; Park, J.; Lim, K. Nutrition Supplements to Stimulate Lipolysis: A Review in Relation to Endurance
Exercise Capacity. J. Nutr. Sci. Vitaminol. 2016, 62, 141–161. [CrossRef]
66. Hursel, R.; Viechtbauer, W.; Dulloo, A.G.; Tremblay, A.; Tappy, L.; Rumpler, W.; Westerterp-Plantenga, M.S.
The Effects of Catechin Rich Teas and Caffeine on Energy Expenditure and Fat Oxidation: A Meta-Analysis.
Obes. Rev. 2011, 12, e573–e581. [CrossRef]
67.
Palmatier, M.A.; Kang, A.M.; Kidd, K.K. Global Variation in the Frequencies of Functionally Different
Catechol-O-Methyltransferase Alleles. Biol. Psychiatry 1999, 46, 557–567. [CrossRef]
68.
Murase, T.; Haramizu, S.; Shimotoyodome, A.; Nagasawa, A.; Tokimitsu, I. Green Tea Extract Improves
Endurance Capacity and Increases Muscle Lipid Oxidation in Mice. Am. J. Physiol. Regul. Integr. Comp.
Physiol. 2005, 288, R708–R715. [CrossRef]
69. Murase, T.; Haramizu, S.; Shimotoyodome, A.; Tokimitsu, I.; Hase, T. Green Tea Extract Improves Running
Endurance in Mice by Stimulating Lipid Utilization during Exercise. Am. J. Physiol. Regul. Integr. Comp.
Physiol. 2006, 290, R1550–R1556. [CrossRef]
70.
Partnerships Informed Choice. Available online: https://www.informed-choice.org/partnerships (accessed on
3 April 2019).
71. Paluska, S.A. Caffeine and Exercise. Curr. Sports Med. Rep. 2003, 2, 213–219. [CrossRef]
72.
Goldstein, E.R.; Ziegenfuss, T.; Kalman, D.; Kreider, R.; Campbell, B.; Wilborn, C.; Taylor, L.; Willoughby, D.;
Stout, J.; Graves, B.S.; et al. International Society of Sports Nutrition Position Stand: Caffeine and Performance.
J. Int. Soc. Sports Nutr. 2010, 7, 5. [CrossRef]
73.
Glaister, M.; Gissane, C. Caffeine and Physiological Responses to Submaximal Exercise: A Meta-Analysis.
Int. J. Sports Physiol. Perform. 2018, 13, 402–411. [CrossRef]
74.
Ivy, J.L.; Costill, D.L.; Fink, W.J.; Lower, R.W. Influence of Caffeine and Carbohydrate Feedings on Endurance
Performance. Med. Sci. Sports 1979, 11, 6–11. [CrossRef]
75.
Graham, T.E.; Hibbert, E.; Sathasivam, P. Metabolic and Exercise Endurance Effects of Coffee and Caffeine
Ingestion. J. Appl. Physiol. 1998, 85, 883–889. [CrossRef]
76.
Graham, T.E.; Spriet, L.L. Metabolic, Catecholamine, and Exercise Performance Responses to Various Doses
of Caffeine. J. Appl. Physiol. 1995, 78, 867–874. [CrossRef]
77.
Spriet, L.L. Exercise and Sport Performance with Low Doses of Caffeine. Sports Med.
2014
, 44 (Suppl. 2),
175–184. [CrossRef]
78.
Armstrong, L.E.; Casa, D.J.; Maresh, C.M.; Ganio, M.S. Caffeine, Fluid-Electrolyte Balance,
Temperature Regulation, and Exercise-Heat Tolerance. Exerc. Sport Sci. Rev. 2007, 35, 135–140. [CrossRef]
79.
Lara, B.; Ruiz-Moreno, C.; Salinero, J.J.; Del Coso, J. Time Course of Tolerance to the Performance Benefits of
Caffeine. PLoS ONE 2019, 14. [CrossRef]
80.
Beaumont, R.; Cordery, P.; Funnell, M.; Mears, S.; James, L.; Watson, P. Chronic Ingestion of a Low Dose
of Caffeine Induces Tolerance to the Performance Benefits of Caffeine. J. Sports Sci.
2017
, 35, 1920–1927.
[CrossRef]
81.
Gonçalves, L.S.; Painelli, V.S.; Yamaguchi, G.; Oliveira, L.F.; Saunders, B.; da Silva, R.P.; Maciel, E.; Artioli, G.G.;
Roschel, H.; Gualano, B. Dispelling the Myth That Habitual Caffeine Consumption Influences the Performance
Response to Acute Caffeine Supplementation. J. Appl. Physiol. 2017, 123, 213–220. [CrossRef]
82.
Talanian, J.L.; Spriet, L.L. Low and Moderate Doses of Caffeine Late in Exercise Improve Performance in
Trained Cyclists. Appl. Physiol. Nutr. Metab. 2016, 41, 850–855. [CrossRef]
83.
Nichols, A.W. Probiotics and Athletic Performance: A Systematic Review. Curr. Sports Med. Rep.
2007
, 6,
269–273. [CrossRef]
Nutrients 2019, 11, 1289 20 of 20
84.
Spence, L.; Brown, W.J.; Pyne, D.B.; Nissen, M.D.; Sloots, T.P.; McCormack, J.G.; Locke, A.S.; Fricker, P.A.
Incidence, Etiology, and Symptomatology of Upper Respiratory Illness in Elite Athletes. Med. Sci. Sports
Exerc. 2007, 39, 577–586. [CrossRef]
85.
Leite, G.S.F.; Resende Master Student, A.S.; West, N.P.; Lancha, A.H. Probiotics and Sports: A New Magic
Bullet? Nutrition 2019, 60, 152–160. [CrossRef]
86.
Coqueiro, A.Y.; de Oliveira Garcia, A.B.; Rogero, M.M.; Tirapegui, J. Probiotic Supplementation in Sports
and Physical Exercise: Does It Present Any Ergogenic Effect? Nutr. Health 2017, 23, 239–249. [CrossRef]
87.
Pedersen, D.J.; Lessard, S.J.; Coffey, V.G.; Churchley, E.G.; Wootton, A.M.; Ng, T.; Watt, M.J.; Hawley, J.A.
High Rates of Muscle Glycogen Resynthesis after Exhaustive Exercise When Carbohydrate Is Coingested
with Caffeine. J. Appl. Physiol. 2008, 105, 7–13. [CrossRef]
88.
Davis, W. Wheat Belly: Lose the Wheat, Lose the Weight, and Find. Your Path Back to Health; Rodale Books:
Emmaus, PA, USA, 2014; ISBN 13: 978-1-60961-479-9.
89.
Perlmutter, D. Grain Brain: The Surprising Truth about Wheat, Carbs, and Sugar—Your Brain’s Silent Killers;
Hachette: London, UK, 2018; ISBN 13: 978-0316234801.
90.
Piercy, K.L.; Troiano, R.P.; Ballard, R.M.; Carlson, S.A.; Fulton, J.E.; Galuska, D.A.; George, S.M.; Olson, R.D.
The Physical Activity Guidelines for Americans. JAMA 2018, 320, 2020–2028. [CrossRef]
91.
Duckworth, A. Grit: The Power of Passion and Perseverance (Vol. 124); Scribner: New York, NY, USA, 2016;
ISBN 13: 978-1-5011-1110-5.
92.
What You Need to Know about Dietary Supplements. Available online: https://www.fda.gov/food/
dietarysupplements/usingdietarysupplements/ucm109760.htm (accessed on 3 April 2019).
©
2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).
