Nutrition and Supplement Update for the Endurance Athlete: Review and Recommendations

Background: Endurance events have experienced a signi cant 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 bene t for endurance activities, including nitrates, antioxidants, ca eine, 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 de ned as events lasting at least 4 [4] to

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 de ned 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 de cit [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 de ne nutritional needs of the athletes. Our goal with this review is to provide the reader with a comprehensive review in a consolidated form and o er practical, evidence-based recommendations that are valuable and directly applicable to the clinician involved in athlete care. Although there have been signi cant 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 elds of sports Nutrients2019,11, 1289; doi:10.3390 /nu11061289 /journal/nutrients

Nutrients2019,11, 1289 2 of 20 medicine, sports science, dietetics, cultural in uences, and even popular media. Especially when it comes to elite athletes and speci cally “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 speci c topics including ca eine, 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 ca eine and nitrates are frequently investigated and used by athletes. Furthermore, antioxidants and probiotics are commonly explored topics by injured athletes and are steadily-growing elds 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

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 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 nally 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.

Nutrients2019,11, 1289 3 of 20 Figure 1.PRISMA ow 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 [ Carbohydrate (as blood glucose and muscle glycogen) has the advantage of generating more ATP per volume of oxygen (O2) 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 O2consumption (VO2max) when CHO stores should be entirely depleted, elite athletes can still run at 16 km/h for an additional 2.5 h at 66% VO2max[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 e ect and clinicians should consider this when counseling athletes.

Nutrients2019,11, 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-o ” 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 exibility in athletes with gastrointestinal (GI) intolerability or GI distress prior to competition. In the nal 1–4 h prior to the event, a single dose of 1–4 g/kg CHO is recommended for a nal top-o 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)

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 di erential 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% VO2maxand 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% VO2max) and glucose oxidation pathways at higher intensities (>70% VO2max). However, prolonged time spent in “train low” may reduce ability to generate maximal power in high-intensity situations [12,19]. In

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% VO2max) and glucose oxidation pathways at higher intensities (>70% VO2max). 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 bene ts from increasing fat oxidative enzyme pathways outweigh the negative e ects of the lowered training load and training adaptations when racing in the high

Nutrients2019,11, 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 a ect 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 di erence 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 bene cial e ect through its contribution to energy expenditure as only about 10–20% of ingested CHO is actually oxidized in the rst 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

oxidized in the rst 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 e ect 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 e ect 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% VO2max) 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 nal “top-o ” 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 the above CHO requirements. Post-exercise refueling

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 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. 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 de ciency, not optimize performance.

Nutrients2019,11, 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 ( rst 24 h) 1.0–1.2 g/kg/h ( rst 3–5 h) or 0.8 g/kg/h+protein (0.3 mg/kg/h) or ca eine (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 uid with 150% of uid 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

A comprehensive review of nutritional needs and recommendations for endurance athletes.