Efficacy of Popular Diets Applied by Endurance Athletes on Sports Performance: Beneficial or Detrimental? A Narrative Review

ndurance athletes need a regular and well-detailed nutrition program in order to ll their energy stores before training/racing, to provide nutritional support that will allow them to endure the harsh conditions during training/race, and to provide effective recovery after training/racing. Since exercise-related gastrointestinal symptoms can signi cantly affect performance, they also need to develop strategies to address these issues. All these factors force endurance athletes to constantly seek a better nutritional strategy. Therefore, several new dietary approaches have gained interest among endurance athletes in recent decades. This review provides a current perspective to ve popular diet approaches: (a) vegetarian diets, (b) high-fat diets, (c) intermittent fasting diets, (d) gluten-free diet, and (e) low fermentable oligosaccharides, disaccharides, monosaccharides and polyols (FODMAP) diets. We reviewed scienti c studies published from 1983 to January 2021 investigating the impact of these popular diets on the endurance performance and health aspects of endurance athletes. We also discuss all the bene cial and harmful aspects

diets, (b) high-fat diets, (c) intermittent fasting diets, (d) gluten-free diet, and (e) low fermentable oligosaccharides, disaccharides, monosaccharides and polyols (FODMAP) diets. We reviewed scienti c studies published from 1983 to January 2021 investigating the impact of these popular diets on the endurance performance and health aspects of endurance athletes. We also discuss all the bene cial and harmful aspects of these diets, and offer key suggestions for endurance athletes to consider when following these diets. Keywords:diet; fat; carbohydrate; protein 1. Introduction Endurance performance, especially prolonged training, requires greater metabolic and nutritional demands from athletes [1]. As endurance athletes face harsh conditions during training periods, they seek alternative dietary strategies to improve endurance performance and metabolic health [2]. It is of paramount importance that a popular diet should be scienti cally proven before being adopted in the athletic population [3]. Vegetarian diets [4], high-fat diets (HFD) [5], intermittent fasting (IF) diets [6], gluten-free diet (GFD) [7] and low fermentable oligosaccharides, disaccharides, monosaccharides and polyols (FODMAP) diets [8] are very popular among endurance athletes. In this review, we will discuss both the bene cial and harmful aspects of these diets on metabolic health and endurance performance. 2. Methods We searched both the PubMed and Cochrane databases for the terms “diet*”, “track- and- eld”, “runner*”, “marathoner*”, “cyclist”, “cycling”, “triathlete”, “endurance”, and “endurance athletes” in the title, abstract, and keywords to detect the most applied diets between 2015 and 2021 in endurance athletes. We obtained 217 results in PubMed and 80 trials in the Cochrane database. We de ned the most recurrent diets in endurance athletes, including “High CHO availability”, “High-carbohydrate diet”, “Ketogenic diet”, Nutrients2021,13, 491.

Nutrients2021,13, 491 2 of 40 “Low-CHO diet”, “Low-CHO, high-fat diet”, “Ketogenic low-carbohydrate, high-fat diet”, “Low-carbohydrate ketogenic diet”, “Low-carbohydrate, high fat, ketogenic diet”, “High- fat, low carbohydrate diet”, “Ketone ester supplementation”, “time-restrictive eating”, “Ketone supplementation”, “Intermittent fasting”, “fasting during Ramadan”, “Vegan diet”, “Lacto-Ovo vegetarian diet”, “Vegetarian diet”, “Low fermentable oligo-, di-, monosaccha- ride, and polyol diet”, and “Gluten-free diet”. Since we all know that high-carbohydrate diet is already well proven to enhance endurance performance [2], we targeted other diets for in-depth investigation by categorizing them as “vegan/vegetarian diets”, “high-fat diets”, “intermittent fasting”, “low-FODMAP diet, and “gluten-free diet”. We included studies on endurance athletes and popular diets, including vegetarian diets, high-fat diets, intermittent fasting, gluten-free diet, and low-FODMAP diet. Using PubMed, Cochrane Library, and Web of Science databases, we aimed to identify studies on races and endurance training. Two researchers (A.D.L and L.H.) independently reviewed the literature. In cases of con ict, a third investigator (B.K.) resolved the disagreement. We identi ed the studies published from 1983 to 2021. To de ne the studies on endurance athletes and diets to be included in the current narrative review, we searched MeSH terms ((“Diet, Ketogenic” (Majr); “Diet, High-Fat” (Majr); “Diet, Carbohydrate-Restricted” (Majr); “Ketone Bodies” (Majr); “Diet, Vegetarian” (Majr); “Diet, Vegan” (Majr); “Fasting” (Majr); “Diet, Gluten- Free” (Majr); “athletes” (Majr); “physical endurance” (Majr); “Diet Therapy” (Majr); “ Oligosaccharides” (Majr), “Disaccharides” (Majr)) and MeSH terms found below this term in the MeSH hierarchy recommended by PubMed and Cochrane Library. We also searched by adding the terms “FODMAP diet”, “low-FODMAP diet”, “FODMAP*”, “Fermentable oligosaccharides, disaccharides and polyols”, “Fermentable, poorly absorbed, short chain carbohydrates”, “Inulin”, “Xylitol”, “Mannitol”, “Maltitol”, “Isomalt”, “Fructose”, “Fruc- tans”, “Galactooligosaccharides”, “fructooligosaccharides”, and “Polyols” to all databases, as no MeSH terms for the low-FODMAP diet were de ned. We discussed the ndings after determining the clinical and practical relevance of the studies by considering only human studies. We included studies available in English clearly describing the applied diet and investigating the effect of diet on endurance athletes as the primary goal. In addition, we included studies where diets were applied according to the dietary description. We

de ned. We discussed the ndings after determining the clinical and practical relevance of the studies by considering only human studies. We included studies available in English clearly describing the applied diet and investigating the effect of diet on endurance athletes as the primary goal. In addition, we included studies where diets were applied according to the dietary description. We ex- cluded studies not explicitly addressing the impact of the diet on endurance performance or health-related parameters, that were not written in English, and were conducted on animals orin vitro. Based on our inclusion and exclusion criteria, we identi ed 57 research articles (Table). We organized the narrative review by considering both the bene cial and detrimental aspects of all ve diets for endurance athletes. 3. Popular Diets Applied to Improve Sports Performance in Endurance Athletes 3.1. Vegetarian Diets Worldwide, it is estimated that around four billion people follow vegetarian diets [9]. In addition to many books and documentaries on vegetarian diets along with various types of practice (Table) and many well-known athletes who have adopted vegan diets and improved their performance [10], vegan diets have become more acceptable and feasible in the athletic population [11]. Looking at the athletic population, using a survey- based study conducted with 422 marathon runners, approximately 10% (n= 39) of the athletes consumed vegetarian/vegan/pescatarian diets [12]. However, in the NURMI study, the authors used the prevalence of vegetarian diets in ultra-endurance runners, primarily living in Austria, Germany, and Switzerland [13]. The ndings revealed that the ratio of vegetarian and vegan athletes was 18.4% and 37.1%, respectively.

Nutrients2021,13, 491 3 of 40 Table 1. Studies investigating the potential effects of vegetarian, fasting, high-fat, gluten-free, and low-FODMAP diets on athletes' endurance performance. Subjects Study Design Diet/Application Duration Exercise Protocol(s) Main Findings Ref. High-Fat Diets Endurance-trained male athletes (n= 20) A non-randomized control trial K-LCHF diet (n= 9; %CHO:fat:protein = 6:77:17) or HCD (n= 11; 65:20:14) 12 weeks A 100-km TT performance, a 6-s sprint, and a CPT #Body mass #Body fat percentage "Average relative power during the 6 s sprint sprint and CPT "Fat oxidation during exercise $100 km TT endurance performance [14] Recreational male athletes (n= 14) A randomized, crossover design K-LCHF diet (<10%CHO, 75% fat) and 2 week HCD (>50% CHO), >2 weeks washout period in between 2 weeks A 90-min bicycle ergometer exercise test at 60%Wmax #Exercise-induced cortisol response; however, better results observed in HCD #Exercise capacity "Fat oxidation during exercise "Perceived exertion after exercise $Post-exercise s-IgA levels at week 2 [15] Professional male race walkers (n= 25) A mix of repeated-measures and parallel-group design K-LCHF diet (n= 10; 75–80% FAT, <50 g CHO, 17% protein), HCD (n= 8; 60–65% CHO, 20% FAT, 15–20% protein), or PCD, (n= 7; 60–65% CHO, 20% FAT, 15–20% protein) 3 weeks - walking economy and VO2peak test on treadmill - walk ( eld) - standardized race walk $VO2peak #10 km race walk performance "Perceived exertion after exercise "Oxygen cost "Fat oxidation during exercise [16] Male and female elite race walkers (n= 24) A mix of repeated-measures and parallel-group design K-LCHF diet (n= 9; 75–80% FAT, <50 g CHO, 15–20% protein), HCD (n= 8; 60–65% CHO, 20% FAT, 15–20% protein), or PCD, (n= 7; 60–65% CHO, 20% FAT, 15–20% protein) 3 weeks - walking economy and VO2peak test on treadmill $VO2peak $Blood acid-base status [17] Endurance-trained male athletes (n= 8) A randomized repeated-measures crossover study K-LCHF diet (75–80% FAT, <50 g CHO, 15–20% protein), HCD (43% CHO, 38% FAT, 19% protein) 4.5 weeks - metabolic test to exhaustion - performance at 70% VO2max $TTE performance $Perceived exertion after exercise #Exercise ef ciency above 70% VO2max $Exercise ef ciency above 70%

$VO2peak $Blood acid-base status [17] Endurance-trained male athletes (n= 8) A randomized repeated-measures crossover study K-LCHF diet (75–80% FAT, <50 g CHO, 15–20% protein), HCD (43% CHO, 38% FAT, 19% protein) 4.5 weeks - metabolic test to exhaustion - performance at 70% VO2max $TTE performance $Perceived exertion after exercise #Exercise ef ciency above 70% VO2max $Exercise ef ciency above 70% VO2max [18] Recreationally competitive male runners (n= 8) A pre–post-test K-LCHF diet (<50 g CHO, 70% FAT (ad libitum), or HCD (habitual diet de ned as moderate to high CHO) 3 weeks - running bouts at multiple individual race paces in the heat, 20-min rest, then a 5 km TT performance after 50 min of running in challenging environmental conditions $5 km TT performance $Perceived exertion after exercise "Fat oxidation during exercise #Body mass #Skinfold thickness $Exercise-induced cardiorespiratory, thermoregulatory, or perceptual responses [19] Elite male cyclists (n= 5) A pre–post-test K-LCHF diet (<20 g CHO, 85% FAT, 15% protein) for 3 weeks immediately after a 1 week HCD (66% CHO, 33%FAT, 1.75 g protein/kg BW/d) 4 weeks (3 weeks LCKD after 1 week HCD) - 2max test on cycle ergometry - 60–65% VO2max at two time points: after HCD and K-LCHF diet $VO2max $TTE performance "Fat oxidation $Blood glucose levels during TTE performance [20] Recreational athletes (n= 5) Case study K-LCHF diet (ad libitum FAT, <50 g CHO, 1.75 g protein/kg BW/d) 10 weeks - performance - test - 2max test #TTE performance "Fat oxidation during exercise even at higher intensities #Body mass #Skinfold thickness [21]

Nutrients2021,13, 491 4 of 40 Table 1.Cont. Subjects Study Design Diet/Application Duration Exercise Protocol(s) Main Findings Ref. Endurance-trained male athletes (n= 8) A randomized, repeated-measures, crossover study K-LCHF diet (75–80% FAT, <50 g CHO, 15–20% protein), HCD (43% CHO, 38% FAT, 19% protein) 4.5 weeks - metabolic test to exhaustion - performance at 70% VO2max Preservation of mucosal immunity "Both pro- and anti-in ammatory T-cell-related cytokine responses to a multiantigen in vitro [22] Elite race walkers (n= 25) A mix of repeated-measures and parallel-group design K-LCHF diet (n= 10; 75–80% FAT, <50 g CHO, 17% protein), HCD (n= 8; 60–65% CHO, 2% FAT, 15–20% protein), or PCD, (n = 7; 60–65% CHO, 20% FAT, 15–20% protein) 3.5 weeks - walking economy and VO2peak test - track race After CHO re- adaptation: - walking $VO2peak #10 km race walk performance "Perceived exertion after exercise "Oxygen cost "Whole-body fat oxidation [23] Male ultra-endurance runners (n= 20) A cross-sectional study design K-LCHF diet (n= 10, 10:19:70) diet or Habitual high-CHO (n= 10, %CHO:protein:fat = 59:14:25) diet An average of 20 months (range 9–36 months) - exercise test - 65% VO2max on a treadmill "Fat oxidation $Muscle glycogen utilization and repletion after 180 min of running and 120 min of recovery [24] Male competitive recreational distance runners (n= 7) A randomized counterbalanced, crossover design K-LCHF diet (n= 10; 75–80% FAT, <50 g CHO, 17% protein), or HCD (n = 8; 60–65% CHO, 20% FAT, 15–20% protein) 6 weeks - 2max test - performance (day 4, 14, 28, and 42) $VO2max $TT performance "Fat oxidation [25] Endurance-trained male cyclists (n= 5) Crossover design A high-fat diet (70% FAT) or an equal-energy, high-carbohydrate diet (70% CHO) 2 2 weeks, 2 week washout period in between (ad libitum diet during washout period) - output test - exercise to exhaustion at 90% VO2max, 20-min rest, and followed with a cycling exercise to exhaustion at 50% VO2max "TTE performance during MIE $Endurance performance during HIE "Fat oxidation [26] Highly trained male ultra-endurance runners (n= 20) A cross-sectional study design Habitual low CHO (n= 10; <20% CHO, >60% FAT) or

libitum diet during washout period) - output test - exercise to exhaustion at 90% VO2max, 20-min rest, and followed with a cycling exercise to exhaustion at 50% VO2max "TTE performance during MIE $Endurance performance during HIE "Fat oxidation [26] Highly trained male ultra-endurance runners (n= 20) A cross-sectional study design Habitual low CHO (n= 10; <20% CHO, >60% FAT) or high CHO (n= 10; >55% CHO) At least 6 months "Circulating total cholesterol, LDL-C, and HDL-C concentrations "Fewer small, dense LDL-C particles [27] Trained male off-road cyclists (n= 8) A crossover design A mixed diet (%CHO:fat:protein = 50:30:20) or a NK-LCHF diet (15:70:15) 4 weeks A continuous exercise protocol on a cycling ergometer with varied intensity (90 min at 85% LT, then 15 min at 115% LT) "VO2max #Body mass #Body fat percentage "Fat oxidation #Post-exercise muscle damage #CK and LDH concentration at rest and during the 105 min exercise protocol in the NK-LCHF diet trial [28] Endurance trained cyclists (n= 16) A randomized, controlled study design A NK-LCHF diet (19:69:10) or a habitual diet (%CHO:fat:protein = 53:30:13) 15 days a 2.5-h constant-load ride at 70% VO2peak followed by a simulated 40-km cycling TT while ingesting a 10% 14C-glucose + 3.44% MCT emulsion at a rate of 600 mL/h "Fat oxidation $TT performance [29]

Nutrients2021,13, 491 5 of 40 Table 1.Cont. Subjects Study Design Diet/Application Duration Exercise Protocol(s) Main Findings Ref. Trained male cyclists (n= 9) A repeated-measures, randomized, crossover study 2 0.35 g/kg KE or placebo (30 min before and 60 min after exercise) Acute ingestion A 85-min steady state exercise at 73% VO2max, followed by a 7 kJ/kg TT (~ 30 min) "Transient type-I T-cell immunity at the gen level [30] Endurance-trained male and female athletes (male/female, 9/3) A single-blind, randomized and counterbalanced, crossover design KE (330 mg/kg BW of HB containing beverage, or bitter- avored placebo drink before exercise Acute ingestion An incremental bicycle ergometer exercise test to exhaustion $Blood pH and HCO3levels $TTE performance [31] Endurance-trained athletes (male/female:5/1) A single-blind, random order controlled, crossover design A 400 mL, low-dose -HB KME 252 mg/kg BW, “low ketosis”; a high-dose HB KME (752 mg/kg BW, “high ketosis”, or a bitter- avored water (placebo) Acute ingestion, 60 min prior to exercise A 60-min continuous cycling exercise, consisting of 20 min intervals at 25%, 50% and 75% Wmax #Contribution of exogenous HB to overall energy expenditure "Exercise ef ciency when blood HB levels above 2 mmol/L "Nausea [32] High-performance athletes Study 1: A randomized crossover design Study 2, 3 and 5: A randomized, single-blind, crossover design Study 4: A two-way crossover study Study 1 (n= 6): A KE (573 mg/kg BW) drink at rest, and during 45 min of cycling exercise 40% and 75% of WMax; with 1 week washout period in between Study 2 (n= 10): - CHO (dextrose = CHO), KE (573 mg/kg BW), or FAT before test Study 3 (n= 8): - CHO and 40% of KE (573 mg/kg BW), a mixture of carbohydrates (CHO), or a no-calorie beverage with 1000 mg B3 before test Study 4 (n= 7): - CHO (dextrose) and 40% from KE, or a mixture of CHOs, 50% of the drink consumed at baseline, the remaining 50% at 30 min, 60 min, and 90 min during exercise as equal aliquots Study 5 (n= 6 male,n= 2 female): - CHO and KE (573 mg/kg BW), or a mixture

mg B3 before test Study 4 (n= 7): - CHO (dextrose) and 40% from KE, or a mixture of CHOs, 50% of the drink consumed at baseline, the remaining 50% at 30 min, 60 min, and 90 min during exercise as equal aliquots Study 5 (n= 6 male,n= 2 female): - CHO and KE (573 mg/kg BW), or a mixture of carbohydrates (CHO) Acute ingestion Study 1: - cycling exercise at 40% and 75% WMax Study 2 and 3: - intensity cycling exercise at 75% WMax for 60 min Study 4: - intensity bicycle ergometry test at 70%VO2max for 2-h Study 5: - steady state workload at 75% WMax followed by a blinded 30-min TT "TT performance following 1 h of high-intensity exercise "Fat oxidation #Plasma lactate levels during exercise "D- HB oxidation according to exercise intensity (from 0.35 g/min at 40% WMax to 0.5 g/min at 75% WMax) $Blood glucose levels [33] Trained male cyclists (n= 9) A repeated-measures, randomized, crossover study A drink containing 0.35 g/kg BW BD or placebo Acute ingestion (30 min before and 60 min during 85 min of steady state exercise) A steady state cycling at the power output eliciting 85% of their VT followed by a TT performance equivalent to 7 kJ/kg (~25–35 min) $TT performance and average power output $Blood glucose and lactate levels "Fat oxidation "GI symptoms [34] Elite male cyclists (n= 10) A randomized crossover design A 1,3-butanediol AcAc diester (2 250 mg/kg BW) or a viscosity and color-matched plasebo drink Acute ingestion, ~30 min before and immedi- ately prior to com- mencing the warm up ~A 31-km laboratory-based TT performance on a cycling ergometer #TT performance "GI symptoms (nausea and re ux) "Fat oxidation [35]

Nutrients2021,13, 491 6 of 40 Table 1.Cont. Subjects Study Design Diet/Application Duration Exercise Protocol(s) Main Findings Ref. Male runners (n= 11) A randomized crossover design An energy matched 650 mL drink containing 60 g CHO + 0.5 g/kg BW 1.3-butanediol (CHO-BD) or 110 g 5 g CHO alone Acute ingestion (50% after baseline mea- surements + 25% after 30 min of seated rest, + 25% after 10 min rest period after completing submaximal running) A 60-min submaximal running, followed by a 5-km running time trial $TT performance $Overall lactate concentration "Blood glucose levels after TT performance "Fat oxidation [36] Highly trained male cyclists (n= 12) A randomized crossover design A KE drink (65 g (918,102 mg/kg, range: 722–1072 mg/kg) of KE [ 96% HB] or a viscosity- and taste-matched placebo Acute ingestion (at 60 and 20 min before and at 30 min during race) A simulated cycling race, which consisted of a 3-h intermittent cycling, a 15-min time trial, and a maximal sprint $High-intensity exercise performance in the nal stage of the event "Upper-abdominal discomfort #Appetite after exercise $Net muscle glycogen breakdown [37] Recreational male distance runners (n= 13) A randomized, double-blind, placebo-controlled, cross- over design Either one (KS1: 22.1 g) or two (KS2: 44.2 g) servings of the ketone supplement ( HB + MCT) or a avor-matched placebo drink Acute ingestion (60 min prior to exercise) A 5-km running TT on a treadmill $Post-exercise glucose concentration $TT performance $Perceived exertion after exercise Dose–response impact on cognitive function [38] Eight trained, middle- and long-distance runners (male/female, 7/1) A double-blind, randomized crossover design An 8% carbohydrate- electrolyte solution before and during exercise, either alone (CHO + PLA), or with 573 mg/kg of a ketone monoester supplement (CHO + KME) Acute ingestion A 60-min submaximal exercise at 65%VO2max immediately followed by a 10-km TT $TT performance $VO2max, running economy, RER, HR, perceived exertion $Cognitive performance $Plasma glucose and lactate levels "Fat oxidation [39] Male and female elite race walkers A non-randomized clinical trial A K-LCHF diet (n= 18; 75–80% FAT, <50 g CHO, 15–20% PRO) followed by an acute CHO restoration, or

A 60-min submaximal exercise at 65%VO2max immediately followed by a 10-km TT $TT performance $VO2max, running economy, RER, HR, perceived exertion $Cognitive performance $Plasma glucose and lactate levels "Fat oxidation [39] Male and female elite race walkers A non-randomized clinical trial A K-LCHF diet (n= 18; 75–80% FAT, <50 g CHO, 15–20% PRO) followed by an acute CHO restoration, or HCD (n= 14; 60–65% CHO, 20% FAT, 15–20% PRO) 3.5 weeks A hybrid laboratory/ eld test of 25 km (males) or 19 km (females) at around 50 km race pace at 75% VO2max #Bone resorption markers at rest and post-exercise "Bone formation markers at rest and throughout exercise Partial recovery of these effects following CHO restoration [40] Well-trained competitive male cyclists or triathletes (n= 7) A randomized, crossover design Day 1: a standard CHO diet (%CHO:fat:protein = 58:27:15) Day 2–7: either an HFD (16:69:15) or HCD (70:15:15) for 6 days Day 8: HCD (70:15:15) 6 day fat adaptation followed by 1 day CHO restoration, a 18 day washout period between Day 9: A 4-h cycling ergometer at 65% VO2peak, followed by a 60-min TT $TT performance "Fat oxidation [41] Well-trained competitive male cyclists or triathletes (n= 8) A randomized, crossover design Day 1–5: either an HFD (%CHO:fat:protein = 19:68:13) or an HCD (74:13:13) Day 6: HCD (74:13:13) 5 day fat adaptation followed by 1 day CHO restoration, a 2 week washout period between A 2-h cycling at 70% VO2max; followed by 7 kJ/kg TT $TT performance "Fat oxidation $Muscle glycogen utilization $Plasma glucose uptake [42] Well-trained competitive male cyclists or triathletes (n= 8) A randomized, double-blind crossover design Day 1–5: either an HFD (%CHO:fat:protein = 19:68:13) or an HCD (74:13:13) Day 6: HCD (74:13:13) Pre-exercise: a CHO breakfast (CHO 2 g/kg). During exercise: CHO intake (0.8 g/kg/h) 5 day fat adaptation followed by 1 day CHO restoration, a 2 week washout period between A 2-h cycling at 70% VO2max; followed by 7 kJ/kg TT $TT performance "Fat oxidation [43]

This review discusses five popular diet approaches for endurance athletes.