Depletion of glycogen stores was associated with fatigue and a high carbohydrate diet maintained glycogen levels as well as physical performance. This has been confirmed by a number of studies. With regard to athletes, traditionally, diets with relatively high levels of carbohydrates are used to enhance performance. However, the human body’s metabolism allows great flexibility in terms of the percentage intake of macronutrients. However, it has been shown by research that in situations of prolonged fasting – starvation, the human body changes its energy use, preferring metabolic pathways involving the use of fat (ketosis) and glucose production through gluconeogenesis.

Similar adaptations were observed after a long-term low-carbohydrate diet that also drove the body into a ketosis state. The low carbohydrate (CHO) diet – low carb high fat (LCHF) has recently become the choice of many endurance – ultra endurance athletes, focusing on specific adaptations to aerobic capacity, recovery from exercise-induced fatigue, and prevention of exercise-induced muscle and organ damage.

In addition, because ultra-marathon efforts present gastrointestinal problems related to the reduced ability to absorb the carbohydrate intake necessary for the effort, dietary ketosis is presented as a potential solution to the problem. But is it? And to what extent?

From the review of the literature that follows, the following conclusions were drawn.

Endurance athletes who were fed a low-carbohydrate, keto-adapted diet had an extremely higher rate of fat oxidation than athletes fed a high-carbohydrate diet. Glycogen consumption and replenishment patterns appeared similar in both cases. Ketogenic diet does not appear to improve performance, at least in endurance efforts in which the CHO intake rate can cover consumption without the presence of gastrointestinal disturbances.

The following is a review of relevant scientific literature

Physiological responses – variations of ketogenic nutrition in endurance and endurance athletes.

TZANETAKIS IOANNIS Msc Exercise Physiology and Training

INDIVIDUAL LITERATURE REVIEW

Introduction
In the 1960s it was discovered that depletion of glycogen stores was associated with fatigue and a high carbohydrate diet maintained glycogen levels as well as physical performance. This was confirmed by numerous studies in the following decades. With regard to athletes, traditionally, relatively high carbohydrate diets have been used to enhance performance (Febbraio, Chiu, Angus, Arkinstall & Hawley, 2000; Hargreaves, Costill, Coggan, Fink & Nishibata, 1984). However, the human body’s metabolism allows great flexibility in terms of the percentage intake of macronutrients. During the same period it was demonstrated that in situations of prolonged fasting – starvation, the human body changes its energy use, preferring metabolic pathways involving the use of fat (ketosis) and glucose production through gluconeogenesis.

Similar adaptations were observed after a long-term low-carbohydrate diet that also drove the body into a ketosis state. The low carbohydrate (CHO) diet – low carb high fat (LCHF) has recently become the choice of many endurance – ultra endurance athletes, focusing on specific adaptations to aerobic capacity, recovery from exercise-induced fatigue, and prevention of exercise-induced muscle and organ damage. (Ma, Suzuki, 2019)

In the study by (Phinney, Bistrian, Evans, & Blackburn 1983) ten well-trained cyclists followed a calorie-neutral diet with 1.75 g protein/kg body weight/day and the balance of calories 2/3 from CHO and 1/3 from fat for one week. They then varied the macronutrient ratio, keeping protein at the same level, CHO less than 20 g and the remainder of calories with fat, so that the total intake equalled the previous dietary approach. Ergometric assessment on an ergometer showed that VO2max remained unaffected between the first week of control, ‘conventional’ diet and the third week of ketogenic diet. In the test to exhaustion at 62-64% of VO2max, the time increased by 4 minutes while the athletes were in their 4^th week of nutritional ketosis. In the constant constant intensity aerobic test the respiratory quotient decreased from 0.83 to 0.72 indicating an increase in carbohydrate use. Following these findings, a 300% reduction in glucose oxidation and a 400% reduction in muscle glycogen utilization were recorded. No hypoglycaemia was observed during steady aerobic effort and maintenance of limited endogenous CHO stores was found. Aerobic endurance effort is not undermined by 4 weeks of nutritional ketosis. However, due to the relatively small sample size, no firm conclusions can be drawn.

In a 12-week study according to McSwiney et al(2018) divided their sample – 20 men trained in endurance activities – into a high CHO group fed a high CHO diet at rates of carbohydrate, 65% protein, 14% and 20% fat, and a low CHO ketogenic diet group at rates of : 6% for CHO,17% for protein and 77% for fat. Both groups were trained in endurance training at 56-68% of VO2max 7 hours per week, 2 resistance training sessions in leg press or squat and 2 HIIT sessions of 10X1 min at 70% peak power with 1 min rec. They were evaluated in individual 100km time trials, 6 sec sprints and critical power tests. Also with DXA scan fat percentages were assessed. Much greater body fat loss was observed in athletes who were in nutritional ketosis. Although the difference in improvement in the 100km individual time trial between the low CHO group and the high CHO group is not considered statistically significant, the difference of 3 minutes of greater improvement is of great practical importance, considering that first place from second place in the Tour de France can be judged in seconds. They showed greater improvement in both the 6 sec sprints , and the critical power test.

In the prevalence study according to Volek et al (2016) comparing two groups of 20 elite overweight athletes fed either, the 1^st group, a high carbohydrate (HC) diet, or, the 2^nd group, a low carbohydrate (LC) diet. 20 ultramarathon runners and IRONMAN triathletes (age 21-45 years), underwent a maximal graded test and a submaximal 180 min running test at 64% of VO2max to determine metabolic responses. One group was fed 59% carbohydrate 14% protein and 25% fat while another group was fed 10% carbohydrate 19% protein and 70% fat averaged over the last 20 months (9-36 months). Athletes underwent a running test of maximal aerobic capacity, a submaximal test of 180 min duration at 64% of VO2max, and values were measured by rest-exercise calorimetry, blood sampling, muscle biopsy, heart rate recording. They also underwent DXA scan. The rate of maximal fat oxidation (fat max) was 2.3-fold higher for the low-carbohydrate (LC) group (1.54 ± 0.18 vs. 0.67 ± 0.14 g/min) and was noted at a higher percentage of VO2max (70.3 ± 6.3 vs. 54.9 ± 7.8%). The mean rate of fat oxidation was 59% greater for the LC group (1.21 ± 0.02 vs. 0.76 ± 0.11 g/min) corresponding to a greater energy participation of fat (88 ± 2 vs. 56 ± 8%).Despite all these notable differences between LC and HC athletes, there was no statistically significant difference in resting glycogen stores, and the level of depletion of this after 180 min of running effort.

In the study by Lambert, Speechly, Dennis & Noakes (1994) 5 male cyclists followed a 2 week high fat dietary intervention at a ratio of 67.3% fat, 7.1% CHO, 25.5% protein and another 2 weeks of high CHO at 12% fat, 73.6% CHO, 13.6% protein. In both interventions the sample was subjected to the same ergometric cycling tests. The first was repeated 5-sec sprints with 1 min recovery between attempts, the second, 30-sec Wingate test, the third, test to exhaustion at ~90% VO2max, and the fourth, test to exhaustion at ~60% VO2max. In the high-intensity tests, no statistically significant difference was observed in: mean and peak power,VO2max, RQ, pulmonary ventilation, heart rate, and time to exhaustion. There were also no differences in glucose, blood lactate values interestingly, and beta-hydroxybutyrate values were stable for both interventions and did not increase. This fact demonstrates that the specific proportions of the high-fat dietary intervention were not able to put individuals in a state of nutritional ketosis. So fat burning in these efforts followed the normal beta oxidation and not the metabolic pathway of ketone body production. Although the sample was not in a ketosis state, it was observed in the moderate and steady-state effort in the high fat condition that it had 2 times longer time to exhaustion than in the high carbohydrate fed condition.

In the cross-sectional, repeated measures study by Shaw, Merien, Braakhuis, Maunder & Dulson (2019) 8 endurance athletes followed two nutritional interventions for 31 days with a 14-21 day wash out period in between. In one of the two , athletes followed a ¨normal¨ diet , with rates of 43% CHO, 38% fat and ~19% protein, and in the second leading to nutritional ketosis with rates of 4% CHO,78% fat and ~18% protein. Athletes underwent a submaximal graded stage test and VO2max was determined and a test to exhaustion at 70% of VO2max . The ketogenic diet maintained work capacity at submaximal intensities, and athletes performed the same training programs during both interventions. However, in the ketosis condition they became less efficient-efficient at intensities greater than 70% of VO2max, while their economy remained unaffected at intensities below 60% of VO2max.

In the study by Burke et al. (2017), 21 high-level walkers participated in 3 groups, each of which had a different dietary condition; the first with high CHO, the second with a high-low CHO periodicity between days of the week, and the third with low CHO and high fat. Athletes were subjected to a submaximal graded test to determine VO2peak and effort economy in a 10km and 25km race-style walking test.The low CHO diet was associated with the highest rate of body fat oxidation ever reported with respect to exercise at all speeds and intensities. The change in fat metabolism selection preference (ketone production) greatly increased oxygen use for any given speed and thus worsened effort economy. And in this particular study, performance did not only improve in the group with the low-carbohydrate, high-fat dietary condition.

Conclusions
Endurance athletes who were fed a low-carbohydrate, keto-adapted diet had an extremely higher rate of fat oxidation than athletes fed a high-carbohydrate diet. And glycogen consumption and replenishment patterns appeared similar in both cases. Ketogenic diets do not appear to improve performance, at least in endurance efforts in which the CHO intake rate can cover consumption without the presence of gastrointestinal disturbances.

Carbohydrates (CHO), Protein (PRT), Eucaloric balanced diet (EBD), Eucaloric ketogenic diet (EKD), Ηigh-carbohydrate (HC), Low carbohydrate Ketogenic diet(LCKD), High intensity interval training (HIIT)), time trial (TT), six second sprint, (SSS), critical power test (CPT),beta-hydroxy butyrate (βHB),

Heart Rate (HR), Ventilation (VE), Respiratory quotient (RQ), High Fat (HF), Habitual Diet (HD), Ketogenic diet (KD), high CHO availability (HCHO), periodised CHO availability (PCHO), low CHO, high fat (LCHF).

Bibliography
Burke, L.M., Ross, M.L., Garvican – Lewis, L.A., Welvaert, M., Heikura, I.A., Forbes, S.G., Mirtschin, J.G., Cato, L.E., Strobel, N., Sharma, A.P., Hawley, J.A., (2017) Low carbohydrate, high fat diet impairs exercise economy and negates the performance benefit from intensified training in elite race walkers. Journal of Physiology. 1;595 (9), 2785-2807. doi: 10.1113/JP273230. Epub 2017 Feb 14.

Coggan, A., Costill, D., Fink, W. J., Hargreaves, M., Nishibata, I., (1984) Effect of carbohydrate feedings on muscle glycogen utilization and exercise performance. Medicine & Science in Sports & Exercise 16 (3) : 219-222.

Febbraio, M.A., Chiu, A., Angus, D.J., Arkinstall, M.J., Hawley, J.A., (2000)Effects of carbohydrate ingestion before and during exercise on glucose kinetics and performance. Journal of Applied Physiology 89, 2220–2226.

Lambert, E., Speechly, D., Dennis, S., Noakes, T., (1994) Enhanced endurance in trained cyclists during moderate intensity exercise following 2 weeks adaptation to a high fat diet. European Journal of Applied Physiology and Occupational Physiology, 69, 287–293.

Ma, S., Suzuki, K., (2019) Keto-Adaptation and Endurance Exercise Capacity, Fatigue Recovery, and Exercise-Induced Muscle and Organ Damage Prevention: A Narrative Review. Sports (Basel) 13;7 (2). pii: E40. doi: 10.3390/sports7020040.

McSwiney, F.T., Wardrop, B., Hyde, P.N., Lafountain, R.A., Volek, J.S., Doyle, L, (2018) Keto-adaptation enhances exercise performance and body composition responses to training in endurance athletes. Metabolism 81:25-34. doi: 10.1016/.metabolism .2017.10.010. Epub 2017 Nov 3.

Phinney, S.D., Bistrian, B.R., Evans, W.J., Gervino, E., Blackburn, G.L., (1983) Aug. The human metabolic response to chronic ketosis without caloric restriction: preservation of submaximal exercise capability with reduced carbohydrate oxidation. Metabolism 32 (8), 769-776.

Shaw, D.M., Merien, F., Braakhuis, A., Maunder, E.D., Dulson, D.K., (2019) Effect of a Ketogenic Diet on Submaximal Exercise Capacity and Efficiency in Runners.Medicine and Science in Sports and Exercise, 51 (10) : 2135-2146 DOI: 10.1249/mss. 0000000000002008 PMID: 31033901.

Volek, J., Freidenreich, D., Saenz, C., Kunces, L., Creighton, B., Bartley, J., Davitt, P., Munoz, C., Anderson, J., Maresh, C., Lee, E., Schuenke, M., Aerni, G., Kraemer, W., Phinney, S., (2016) Metabolic characteristics of keto-adapted ultra-endurance runners.
Metabolism Clinical and Experimental 65, 100-110.