Role of a Ketogenic Diet on Body Composition, Physical Health, Psychosocial Well-Being and Sports Performance in Athletes: A Scoping Review

Background: Recently, a focus has been placed on investigating the potential bene ts of adherence to a ketogenic diet in enhancing body composition, physical health, psychological well-being, and performance of athletes from various sporting disciplines. As the available research is yet to be collated and analyzed in a single review, this scoping review aims to analyze and draw conclusions from the available literature that exists on the e cacy of a ketogenic diet among athletic populations. Methods: Several primary research databases and any relevant citation lists were searched to locate appropriate studies for inclusion in this scoping review. Studies that investigated the e ects of adherence to a ketogenic diet (KD), de ned by a carbohydrate intake of less than 5% of total energy intake, on body composition, physical health, psychological well-being, and performance among an athletic population were included in the review. From 814 articles screened, 12 were identi ed as meeting the inclusion criteria and were included in the nal scoping review. Results: Adherence to a KD has bene cial e ects on body weight and fat mass. Varying e ects were identi ed on physical health with the diet, eliciting positive e ects on fat oxidation but potentially deleterious e ects on stool microbiota and iron metabolism. Con icting results were reported regarding the e ects of a KD on sporting performance. Bene ts were reported regarding athlete well-being following commencement of a KD, but only after week two. Conclusions: The results of this scoping review demonstrate that there are both bene cial and detrimental e ects associated with adherence to a KD among athletic populations.

metabolism. Con icting results were reported regarding the e ects of a KD on sporting performance. Bene ts were reported regarding athlete well-being following commencement of a KD, but only after week two. Conclusions: The results of this scoping review demonstrate that there are both bene cial and detrimental e ects associated with adherence to a KD among athletic populations. It is understood that further research is required to make any concrete recommendations regarding a KD to athletes. Keywords:ketogenic; athletes; body composition; physical health; well-being 1. Introduction Over the past 60 years, an emphasis has been placed on the consumption of adequate amounts of carbohydrate pre-exercise/training to ensure adequate muscle glycogen content. It has long been understood that su cient muscle glycogen stores are required for optimal sporting performance. Advice from major sports nutrition organizations has re ected this ideology, promoting carbohydrate-focused diets for athletes [1]. More recently, an interest in low-carbohydrate alternatives, including the ketogenic diet (KD) has increased. Similar to a low-carbohydrate, high-fat diet, the KD induces an augmentation in free fatty acids circulating within the body. The diet elicits this physiological response by involving a restriction in dietary carbohydrate (<5% of energy intake per day), elevation of fat intake(>60% ofdietary Sports2020,8, 131; doi:10.3390 /sports8100131 /journal/sports

Sports2020,8, 131 2 of 16 intake), and adequate protein consumption. This restriction in dietary carbohydrate is associated with relative decreases in glucose availability, inducing a physiological metabolic state known as ketosis [2]. Ketosis is characterized by an increase in circulating ketone bodies, namely, acetoacetate (AcAc) and B-hydroxybutyrate (BHB). BHB is acknowledged as the chief ketone body within the peripheral tissues and is the transporter of energy to these tissues [2]. Thus, the elevation of blood BHB levels above 0.5 mmol/L [2] within the body are utilized to demonstrate the presence of nutritional ketosis. During nutritionally induced ketosis, these particular ketone bodies are used as an alternative to glucose and become the main energy source for the brain and other bodily tissues [2]. The KD has gained signi cant attention due to its potential as a medical intervention for epilepsy [3,4] and its ability to induce weight loss and body composition changes in obese and overweight individuals [5–7]. In more recent times, a KD has generated interest among the sports nutrition community, with evidence suggesting that a reduction in dietary carbohydrate and increases in circulating ketone bodies results in a shift in substrate utilization during submaximal exercise bouts, namely, from glycogen to body fat [8]. A preliminary search of the academic literature did not indicate that a systematic review has taken place to examine whether a KD in athletes' in uences body composition, physical health, psychological well-being, or sports performance. As such, we conducted a scoping review to summarize the current literature to provide an overview of the e ects of adherence to a KD. This review sought to determine the e ects that occur within athletic populations on both short- and long-term body composition, physical health, psychological well-being, and sports performance in athletes. 2. Materials and Methods 2.1. Methods This scoping review has been conducted in accordance with the Joanna Briggs Institute (JBI) methodology for scoping reviews [9,10]. 2.2. Search Strategy For the purposes of this scoping review, we accessed a number of primary health research databases (PubMed, Embase, CINAHL, Web of Science, Scopus, SPORTDiscus, and Cochranes Database) in conjunction

performance in athletes. 2. Materials and Methods 2.1. Methods This scoping review has been conducted in accordance with the Joanna Briggs Institute (JBI) methodology for scoping reviews [9,10]. 2.2. Search Strategy For the purposes of this scoping review, we accessed a number of primary health research databases (PubMed, Embase, CINAHL, Web of Science, Scopus, SPORTDiscus, and Cochranes Database) in conjunction with a review of citation indexes and reference lists to locate peer-reviewed studies relevant to the research question. The search was conducted from inception until June 2020 and considered only English manuscripts. The search terms used to explore the databases were ketogenic, keto, very low carbohydrate, athlete, sport, and exercise. 2.3. Inclusion Criteria and Outcome Measures In order to be deemed appropriate for inclusion in this scoping review, studies must have investigated the e ects of a KD, de ned by a protocol that involves dietary contribution from carbohydrate of less than 5% of energy intake per day, or blood ketone levels of>0.5 mmol/L BHB [2], and have been implemented longer than or equal to 21 days. Studies were considered if they included male or female participants who were either trained or well-trained in their chosen sport. Reported outcomes may encompass a range of areas including, but not limited to, body composition (i.e., fat mass and lean body mass), physical health (i.e., blood composition, pH, iron status, immune function), psychological well-being (i.e., perceived wellness), and sporting performance (e.g., laboratory- and eld-based test performance). In addition, the length of study, outcome measure, and the instrument used to measure the outcomes was reported. For this review, it is important to clarify how health and well-being were de ned when searching the current literature. As this scoping review focused on athletic populations, we decided that various measures of health and well-being speci c to athletes would be examined. Body composition,

Sports2020,8, 131 3 of 16 namely, body fat and body weight, were investigated, as this is a particularly important measure of health in athletes that is conducive to their overall performance. Other measures of physical health such as metabolic characteristics (i.e., fat oxidation, circulating metabolites, and muscle glycogen availability), blood pro le (i.e., lactate levels, bicarbonate concentrations, iron levels, and blood pH), heart rate, and exercise performance (i.e., maximal exercise capacity and strength) were all considered when searching for appropriate studies. Psychological well-being was identi ed as pertaining to athletes' perceptions of the ketogenic diet and their overall thoughts and feelings regarding this dietary intervention and the potential e ects on their psychological well-being, training, and exercise performance. 2.4. Data Extraction After applying the inclusion criteria to the studies obtained from each of the relevant databases, we obtained data on study citation details (author, title, journal, and publication year), context of the study (sport involved), participants (age, gender, and sample size), dietary protocol (length and macronutrient distribution), and nal outcomes, all of which was entered into an Excel spreadsheet. Each article was grouped by the outcome measured (body composition, physical health, sports performance, athlete well-being), with three articles measuring more than one outcome. For these articles, each outcome measure was represented separately in the appropriate group. Due to the nature of the research question, the literature included in the nal qualitative evaluation predominantly consisted of studies that employed either a crossover design, non-randomized allocation to a dietary intervention group, or pre–post testing methods. Following selection, each of the articles were critically appraised against the relevant JBI or Centre for Disease-Based Management Critical Appraisal Checklist and were deemed appropriate for inclusion in the nal scoping review. 3. Results 3.1. Search The search revealed a total of 814 articles related to the search terms, however, only 12 articles met each of the criteria stipulated for article inclusion (see Figure). After removing 117 duplicate articles, a further 665 articles were also deemed unsuitable for inclusion, as these involved non-athletic populations, included carbohydrate intakes>5% total energy intake, or involved dietary protocols that were<21 days

search revealed a total of 814 articles related to the search terms, however, only 12 articles met each of the criteria stipulated for article inclusion (see Figure). After removing 117 duplicate articles, a further 665 articles were also deemed unsuitable for inclusion, as these involved non-athletic populations, included carbohydrate intakes>5% total energy intake, or involved dietary protocols that were<21 days in duration. The topics that were included in the nal review were body composition, physical health, sports performance, and athlete well-being. 3.2. Ketogenic Diet The characteristics of each of the articles included in this scoping review are displayed in Table. The total sample was comprised of 101 athletes (84 males, 17 females) from seven sports. The athletes ranged in age from 15 to 41 years. As detailed in Table, each of the relevant studies involved dietary protocols that restricted carbohydrate to less than 5% of energy intake per day. In 10 of the included studies, fat intake was above 75% of total dietary intake. Additionally, in two of the studies, protein intakes were considerably high (40% of total daily energy intake). Of the 12 studies included in the nal review, seven investigated the e ects of a KD over a three-week period, four ran over a four-week period, and one considered the e ects of a KD over a 12-week period.

Sports2020,8, 131 4 of 16Sports 2020, 8, x FOR PEER REVIEW 4 of 15 Figure 1. Prisma flowchart describing the study selection pathway. 3.2. Ketogenic Diet The characteristics of each of the articles included in this scoping review are displayed in Table 1. The total sample was comprised of 101 athletes (84 males, 17 females) from seven sports. The athletes ranged in age from 15 to 41 years. As detailed in Table 1, each of the relevant studies involved dietary protocols that restricted carbohydrate to less than 5% of energy intake per day. In 10 of the included studies, fat intake was above 75% of total dietary intake. Additionally, in two of the studies, protein intakes were considerably high (40% of total daily energy intake). Of the 12 studies included in the final review, seven investigated the effects of a KD over a three-week period, four ran over a four-week period, and one considered the effects of a KD over a 12-week period. Records identified through database searching (n = 808) Records after duplicates removed (n = 697) Records screened (n = 697) Records excluded (n = 665) Full-text articles assessed for eligibility (n = 32) Full-text articles excluded, with reasons (n = 20) 7 Irrelevant Outcomes (CHO > 5% energy) 5 Irrelevant Outcomes (Non-Athletes) 8 Review/Discussion/Commentary only Studies included in qualitative synthesis (n = 12) Additional records identified through handsearching reference lists (n = 6) IDENTIFICAT ION ELIGIBILITY INCLUDED Figure 1.Prisma owchart describing the study selection pathway.

Sports2020,8, 131 5 of 16 Table 1.General characteristics and main ndings of the studies included in this scoping review. Study Citation Details Context Participants Dietary Protocol Main Findings Body Composition Paoli, A.; Grimaldi, K.; D'Agostino, D.; Cenci, L.; Moro, T.; Bianco, A.; et al.: Ketogenic diet does not a ect strength performance in elite artistic gymnasts Artistic Gymnastics 15–26 years, Male; n=9 Athletes acted as own controls with adherence to KD followed by western diet. Thirty-day KD dietary protocol; 40% PRO,<5% CHO, 55% FAT. Signi cant di erences were exhibited in body weight (PRE 69.6 7.3 kg vs. POST 68.0 7.5 kg), % lean body mass (PRE 92.4 1.4% vs. POST 95.0 1.0%), fat mass (PRE 5.3 1.3 g vs. POST 3.4 0.8 g), and fat % (PRE 7.6 1.4% vs. POST 5.0 0.9%) following adherence to a KD. Lean body mass and muscle mass remained relatively unchanged following adherence to a KD. There were no signi cant di erences in performance following KD intervention. Rhyu, H.; Cho, S.: The e ect of weight loss by ketogenic diet on the body composition, performance-related physical tness factors and cytokines of Taekwondo athletes. Taekwondo 15–17 years, Male; n=20 Randomized design with assignment to either a non-KD or a KD. Three-week KD dietary protocol; 40% PRO,<5% CHO, 55% FAT. Signi cant decreases were observed in weight, % body fat, FFM, and fat mass, however, there was no di erence in e ect between groups. Physical Health Heikura, I.; Burke, L.; Hawley, J.; Ross, M.; Garvican-Lewis, L.; Sharma, A.; et al.: A short-term ketogenic diet impairs markers of bone health in response to exercise. Elite race walking 24–31 years, 25 Male, 5 Female;n=30 Non-randomized allocation to either a high CHO or KD. Three-week KD dietary protocol; 2.1 g/kg PRO,<5% CHO, 75–80% FAT. Compared to baseline measures, bone resorption was increased (+22% CI 9, 35) and bone formation decreased ( 14% CI 19, 9) following a KD. Bone metabolism also decreased ( 25% CI 35, 14) among KD participants. Congruent results were also observed post-exercise. Krystztof, D.; Nowaczyk, P.; Siedzik, K.: E ect of a

dietary protocol; 2.1 g/kg PRO,<5% CHO, 75–80% FAT. Compared to baseline measures, bone resorption was increased (+22% CI 9, 35) and bone formation decreased ( 14% CI 19, 9) following a KD. Bone metabolism also decreased ( 25% CI 35, 14) among KD participants. Congruent results were also observed post-exercise. Krystztof, D.; Nowaczyk, P.; Siedzik, K.: E ect of a four-week ketogenic diet on exercise metabolism in CrossFit-trained athletes CrossFit 25–33 years, 11 Male, 11 Female;n=22 Four-week ketogenic dietary protocol; 1.7 g/kg PRO, 5% CHO, 75% FAT. Gender di erences were apparent regarding fat oxidation during a KD. Males exhibited increases in the rate of fat oxidation at lower exercise intensities, i.e., 35% (habitual diet 0.006 g/min/kg FFM vs. KD 0.0095 g/min/kg FFM) and 50–65% VO 2 max, and females experienced increases in fat oxidation rates at higher exercise intensities (85% VO 2 max(habitual diet 0.002 g/min/kg FFM vs. KD 0.009 g/min/kg FFM)). Males exhibited higher AUC of fat utilization and lower CHO utilization at 65% VO 2 max.

Sports2020,8, 131 6 of 16 Table 1.Cont. Study Citation Details Context Participants Dietary Protocol Main Findings McKay, A.; Peeling, P.; Pyne, D.; Welvaert, M.; Tee, N.; Leckey, J.; et al.: Chronic adherence to a ketogenic diet modi es iron metabolism in elite athletes. Elite race walking 22–32 years, 31 Male, 6 Female;n=37 Non-randomized allocation (chosen by athletes) to either a high CHO, periodized CHO, or KD. Three-week KD dietary protocol; 17% PRO,<5% CHO, 78% FAT. Total dietary iron intake was signi cantly lower in the KD group (13.7 2.1 mg/day) than the high CHO/periodized CHO groups (17.8 4.5 mg/day). Signi cant di erences in serum ferritin from baseline to postintervention were exhibited between groups, however, there was a greater decrease among CHO diet participants (KD 23% vs. CHO diets 37%). A greater post-exercise IL-6 response was exhibited among the KD group (KD 0.6 0.8 to 10.8 0.8 pg/mL vs. CHO diets 0.7 6.6 to 6.3 0.6 pg/mL) during postintervention testing, potentially due to a decrease in muscle glycogen stores. McKay, A.; Pyne, D.; Peeling, P.; Sharma, A.; Ross, M.; Burke, L.: The impact of chronic carbohydrate manipulation on mucosal immunity in elite endurance athletes. Elite race walking 21–32 years, 19 Male, 7 Female;n=26 Non-randomized allocation (chosen by athletes) to either a high CHO, periodized CHO, or KD. Three-week KD dietary protocol; 17% PRO,<5% CHO, 78% FAT. Regardless of the particular dietary protocol, s-IgA concentration increased post-exercise. No signi cant di erences observed between diet groups for resting s-IgA concentration, ow rate, or secretion rate. In regard to athlete well-being, those in the KD group reported initial decreases in perceptions of general health and physical readiness from baseline to week 2, however, this was followed by increases from week 2 to 3. There was no clear change in perceived soreness or fatigue from baseline to end of trial among participants in the KD group. Murtaza, N.; Burke, L.; Vlahovich, N.; Charlesson, B.; O'Neill, H.; Ross, M.; et al.: The e ects of dietary pattern during intensi ed training on stool microbiota of elite race walkers. Elite race walking 21–32 years, Male;

3. There was no clear change in perceived soreness or fatigue from baseline to end of trial among participants in the KD group. Murtaza, N.; Burke, L.; Vlahovich, N.; Charlesson, B.; O'Neill, H.; Ross, M.; et al.: The e ects of dietary pattern during intensi ed training on stool microbiota of elite race walkers. Elite race walking 21–32 years, Male; n=21 Non-randomized allocation (chosen by athletes) to either a high CHO, periodized CHO, or KD. Three-week KD dietary protocol; 17% PRO, 3.5% CHO (0.50 g/kg/day), 78% FAT. Adherence to a KD over a 3-week period had a greater e ect on gut microbiota than adherence to a high CHO or periodized CHO diet when compared with baseline measures. Signi cant decreases in prevalence ofFaecalibacteriumspp. and increases in abundance ofDoreaspp., andBacteroidesspp. were exhibited among the KD group, thus indicating that adherence to a KD has a signi cant selective pressure on athlete gut microbiota.

Sports2020,8, 131 7 of 16 Table 1.Cont. Study Citation Details Context Participants Dietary Protocol Main Findings Murtaza, N.; Burke, L.; Vlahovich, N.; Charlesson, B.; O'Neill, H.; Ross, M.; et al.: Analysis of the e ects of dietary pattern on the oral microbiome of elite endurance athletes. Elite race walking 21–32 years, Male; n=21 Non-randomized allocation (chosen by athletes) to either a high CHO, periodized CHO, or KD. Three-week KD dietary protocol; 17% PRO, 3.5% CHO (0.50 g/kg/day), 78% FAT. Oral microbiome changed among participants in the KD group when compared with the high and periodized CHO groups.Haemophilus, Neisseria, andPrevotellaspp. each decreased, and abundance ofStreptococcusspp. increased following the KD intervention period. Sports Performance Burke, L.; Ross, M.; Garvican-Lewis, L.; Welvaert, M.; Heikura, I.; Forbes, S.; et al.: Low carbohydrate, high fat diet impairs exercise economy and negates the performance bene t from intensi ed training in elite race walkers. Elite race walking 21–32 years, 21 Male;n=21 Non-randomized allocation (chosen by athletes) to either a high CHO, periodized CHO, or KD. Three-week KD dietary protocol; 17% PRO, 3.5% CHO, 78% FAT. VO 2 peakincreased signi cantly following 3-week adherence to a KD (66.3 90% CI: 63.9,68.7 vs. 71.1 90% CI 69.3,72.8), however, this result was negated by a signi cant increase in the O 2cost of exercise (VO 2 60 mL/kg/min vs. 65 mL/kg/min at graded economy test stage 4) exhibited among participants in the KD group. There was also a signi cant decrease in respiratory exchange ratios among the KD participants (PRE 1.10 vs. POST 0.97). Completion times for the 10 km race walk did not di er between baseline and at the end of KD protocol. Fat oxidation rates increased signi cantly in the KD group. Paoli, A.; Grimaldi, K.; D'Agostino, D.; Cenci, L.; Moro, T.; Bianco, A.; et al.: Ketogenic diet does not a ect strength performance in elite artistic gymnasts. Artistic Gymnastics 15–26 years, Male; n=9 Athletes acted as own controls with adherence to KD followed by western diet. Thirty-day KD dietary protocol; 40% PRO, <5% CHO, 55% FAT. There were no signi cant di erences in performance

The review examines the potential benefits and drawbacks of ketogenic diets for athletes.