The Metabolic Features of Keto-Adapted (20 Months) Ultra Athletes [Comparative Study]

The Metabolic Features of Keto-Adapted (20 Months) Ultra Athletes - Study Timeline

Introduction

First well designed and conducted study of keto-adapted athletes? Let’s see…

Many think that keto-adaptation is the result of 2-3 weeks of ketosis. Simply put, that is delusional.

I encourage you not to believe me. Listen to Barry Murray who works with fat adapted athletes and who observed how the process could take from at least 6 months to more than 2 years, widely varying between individuals. And, I’ve seen it on myself.

I’ve been using ketosis (the metabolic state where fat becomes the primary source of fuel) since October 2013. I’ve been in ketosis 98% of the time. My personal approach does not resemble the fat-laden ketogenic diet that’s preached out there; one of the focal points of my strategy is micronutrient optimization.

With constant ketosis it took me a couple of months to recover the high-intensity performance that I had prior to ketosis (kickboxing, soccer, and strength training). Endurance training adaptation may not take as long.

As of the present day, when I go to the gym (heavy lifting) I am at least 18-20 hours fasted. It still surprises me how well I can perform on an empty stomach. I’d like to see research on short-burst-high-intensity workout adaptation to long term ketosis. If you happen to know of any, kindly leave a comment below.

More specifically, I’m interested in the energy systems dynamics (ATP-CP and anaerobic glycolysis) of this situation; and I have a suspicion of the results from what I learned through my own n=1.

Until this type of research is out, let’s see what happens to keto-adapted endurance athletes in terms of performance when they are compared to non-keto-adapted athletes.

Non-Keto-Adapted vs. Keto-Adapted Athletes

There’s nothing wrong with being a non-keto-adapted or keto-adapted athlete. It’s a matter of personal choice, personal genomics, and many other factors.

In this study [1], we look at the performance of 20 elite ultra-marathoners and Ironman triathletes. They have been divided into two groups and they were asked to perform:

“a maximal graded exercise test and a 180 min submaximal run at 64% VO2max on a treadmill to determine metabolic responses.”[1]

One group (10 athletes): consumed a traditional high carbohydrate diet

%carbohydrate:protein:fat = 59:14:25

The other group (10 athletes): consumed a low carbohydrate diet

%carbohydrate:protein:fat = 10:19:70

The low-carbohydrate diet group has been following the diet for an average of 20 months (range 9 to 36 months).

In short

“Despite these marked differences in fuel use between LC and HC athletes, there were no significant differences in resting muscle glycogen and the level of depletion after 180 min of running (−64% from pre-exercise) and 120 min of recovery (−36% from pre-exercise).

Compared to highly trained ultra-endurance athletes consuming an HC diet, long-term keto-adaptation results in extraordinarily high rates of fat oxidation, whereas muscle glycogen utilization and repletion patterns during and after a 3 hour run are similar.”

The Nitty-Gritty (Detailed View)

Even though there is no essential requirement for dietary carbohydrates, the authors acknowledge the importance of glycogen:

“After a few weeks of starvation when glycogen levels significantly decrease, hepatic ketone production increases dramatically to displace glucose as the brain’s primary energy source, while fatty acids supply the majority of energy for skeletal muscle. Glucose production from noncarbohydrate sources via gluconeogenesis supplies carbons for the few cells dependent on glycolysis.”

They still use the word “starvation” to emphasize a non-eating state. In fact, real starvation occurs when bodyfat stores are at the low-bottom (<3%) and the metabolism starts tapping into lean tissue for survival. Until then, you are merely fasting. So, there’s no need to use dramatic words.

Methods

Day 1 – maximal oxygen consumption test to determine peak fat oxidation
Day 2 – three-hour treadmill run, 64% VO2Max to determine metabolic responses before, during, and after exercise.

Participants

Male ultra-endurance runners 21–45 years old.

They were in the “top 10% of finalists competing in sanctioned running events ≥50 km and/or triathlons of at least half Ironman distance (113 km).”[1]

To be included in the low-carb diet group (LC), subjects had to have been consuming <20% of their energy from carbohydrates and >60% from fat for at least 6 months prior to the tests.

To be included in the high-carb diet group (HC), subjects had to have consistently been consuming >55% of their energy from carbohydrates.

The Metabolic Features of Keto-Adapted (20 Months) Ultra Athletes - Habitual Daily Nutrient Intake

The Metabolic Features of Keto-Adapted (20 Months) Ultra Athletes - Subject Characteristics

This study is very reflective of the different metabolic responses of subjects adhering (for the long-term) to different macronutrient partitioning protocols (long-term high-carb vs. long-term low carb). If you want to learn more about the competition between metabolic fuels, you can study The Randle Cycle.

It would be myopic (love the word) to compare high-carb athletes to low-carb athletes, when the latter have not been conditioned (for several months) to efficiently use fat as a metabolic substrate. Yet, most of the studies out there are designed like that.

In this study, VO2Max measurements and blood samples were taken at different intervals during the treadmill run:

“The treadmill was stopped briefly at 60 and 120 min to obtain blood.

After 180 min of running, subjects moved to a wheel chair and blood was obtained immediately. Subjects were moved to a bed and a second muscle biopsy was performed ~15 min after completing the run. Subjects then consumed a shake identical to the pre-run shake. Indirect calorimetry measurements and blood were taken at 30, 60, and 120 min post exercise. A final muscle biopsy was taken 120 min post exercise. The entire day of testing lasted about 8 hours finishing mid-afternoon.”

The Metabolic Features of Keto-Adapted (20 Months) Ultra Athletes - Study Timeline

Results

“There were no significant differences between groups in physical characteristics or aerobic capacity (Table 1). Two athletes in each group were ironman distance triathletes while the remainder competed primarily in running events ranging from 80 to 161 km (50 to 100 miles). The main difference between groups was their habitual diet (Table 2). Average time on an LC diet was 20 months (range 9 to 36 months).”

I think both (dietary) strategies are fine if you are or want to become an elite athlete. Making sure you follow a well formulated diet and you minimize the consumption of processed products (sugar and fat laden) should be at the top of the priority list.

“In the LC group, an overwhelming majority of energy intake was derived from fat (70%), primarily saturated and monounsaturated fatty acids. Only ~10% of their energy intake was from carbohydrate.

Conversely, the HC group consumed over half their energy as carbohydrate (59%).

Absolute protein was not significantly different between groups, but LC athletes consumed a greater relative amount than HC athletes (19 vs 14% of total energy).”

Peak-Fat Oxidation

The Metabolic Features of Keto-Adapted (20 Months) Ultra Athletes - Peak Fat Oxidation

Adaptation to a carbohydrate-based metabolism results in different fat-oxidation rates compared to the adaptation to a fat-based metabolism. The results are significantly different. Once again, I’d highly recommend studying the Randle Cycle for a better picture of fuel competition. You will understand that those following an IIFYM (if it fits your macros) may not make the best decision about their healthspan.

“During 3 hours of exercise, RER fluctuated between 0.73 and 0.74 translating into relatively stable and higher fat oxidation rates of ~1.2 g/min in the LC group, whereas fat oxidation values were significantly lower in the HC group at all time points (Fig. 3A).

The average contribution of fat during exercise in the LC and HC groups were 88% and 56%, respectively.”

Circulating Metabolites

As you can see in the graphics if you read the entire study, lipid metabolism was increased in the LC group. They are, after all, adapted to burning fat primarily.

“Circulating markers of lipid metabolism indicated a significantly greater level of ketogenesis (Fig. 4A) and lipolysis (Fig. 4B) in the LC athletes.
Serum non-esterified fatty acids were higher at the start of exercise in LC athletes, but peak levels at the end of exercise were not significantly different between groups (Fig. 4C).
Plasma triglycerides were not different between groups (Fig. 4D).
Plasma glucose and serum insulin were not significantly different between groups at rest and during exercise but increased during the last hour of recovery in the HC athletes, likely due to the greater amount of carbohydrate in the shake.”

Enhanced lipolysis (along with beta-oxidation) leads to higher rates of acetyl-CoA, which furthers down the TCA cycle.

The authors provide reference to a study of trained sledge Alaskan dogs (diet of 16% carbs) showing unexpected high rate of carbohydrate oxidation during exercise that was associated with a significant increase in gluconeogenesis from glycerol and increased lactate oxidation [2].

This is a very different pattern of fuel utilization compared to trained humans consuming a carbohydrate rich diet. But, on a closer look:

“A provocative finding was that LC athletes appeared to break down substantially more glycogen (>100 g) than the total amount of carbohydrate oxidized during the 3 hour run. This was the case in all ten LC athletes.”

It begs the question:

“Why would athletes with high rates of acetyl CoA generation from fatty acids bother breaking down muscle glycogen if those carbons are not terminally oxidized?”

They speculate this happens because of:

– the need for a source of glucose to power the PPP pathway (nucleotide synthesis, glutathione maintenance, etc).
– the need for a source of pyruvate to form OAA (oxalo-acetate).

The Pentose Phosphate Pathway (PPP) generates:

– G3P and F1,6BP for glycolysis => more ATP and more Pyruvate.

“Pyruvate may be necessary in a keto-adapted athlete for two reasons. First, pyruvate can be used as an anaplerotic substrate by pyruvate carboxylase to generate oxaloacetate.

At the onset of exercise several TCA cycle intermediates increase in concentration including fumarate, citrate and malate, however oxaloacetate remains low.

Thus, in the keto-adapted athlete glycogen breakdown may be necessary to ensure a constant source of oxaloacetate for optimal TCA functioning. Second, pyruvate can be converted to lactate or alanine in muscle, which may then serve as gluconeogenic substrate for the liver.”[1]

As they point out, muscle glycogen synthesis in humans is higher “when large amounts of carbohydrate are consumed immediately post-exercise” [3].

Interestingly enough, “the LC athletes had similar rates of glycogen repletion compared to the HC athletes, despite receiving a negligible amount of carbohydrate after exercise (4 vs 43 g) and more fat (31 vs 14 g).”

More on Muscle Glycogen (the sweet stuff)

Once again, one of the most surprising findings (to me) was with respect to glycogen dynamics:

“Compared to baseline, muscle glycogen was significantly decreased by 62% immediately post-exercise and 38% at 2 hours post-exercise in the HC group.

The LC group exhibited a similar pattern; muscle glycogen was decreased by 66% immediately post-exercise and 34% at 2 hours post-exercise (Fig. 6A).” [1]

The Metabolic Features of Keto-Adapted (20 Months) Ultra Athletes - Muscle Glycogen

So, what would be the carbon source for glycogen synthesis when no carbohydrate (or energy) is provided after prolonged exercise?

“Although speculative, lactate and/or glycerol, which were two-fold higher at the end of exercise in LC athletes and then sharply decreased during recovery, may have provided a source of carbons for glycogen synthesis during recovery” [4].

“Regardless of the mechanism, these results suggest that long-term consumption of a low-carbohydrate/high-fat diet in highly trained ultra-marathoners results in adaptations in the homeostatic regulation of muscle glycogen that acts to preserve levels similar to those observed when exogenous carbohydrate availability is high.

If this is true, then God save broscience and the supplements industry.

Take-Away Messages and Conclusion

In their (authors’) own words:

“The most notable findings were that compared to HC athletes, the LC keto-adapted runners showed:
(1) twofold higher rates of peak fat oxidation during graded exercise,
(2) greater capacity to oxidize fat at higher exercise intensities,
(3) two-fold higher rates of fat oxidation during sustained submaximal running, and
(4) no differences in pre-exercise muscle glycogen concentrations, the rate of glycogen utilization during exercise, and the rate of glycogen synthesis during recovery.

Thus, we show for the first time that chronic ketoadaptation in elite ultra-endurance athletes is associated with a robust capacity to increase fat oxidation during exercise while maintaining normal skeletal muscle glycogen concentrations.”

Even though the authors try to remain reserved and unenthusiastic about their findings, these final statements break it loose. There’s nothing wrong with that, as long as they strive to keep the experiment low on/free of biases.

Finally and most !!!importantly, you should balance your conclusions knowing that funding for this study was provided by Quest Nutrition and The Robert C. Atkins and Veronica Atkins Foundation.

Questions and comments below.

Resources:

  1. Volek, J. S., Freidenreich, D. J., Saenz, C., Kunces, L. J., Creighton, B. C., Bartley, J. M., … & Lee, E. C. (2016). Metabolic characteristics of keto-adapted ultra-endurance runners. Metabolism, 65(3), 100-110.
  1. Miller, B. F., Drake, J. C., Peelor, F. F., Biela, L. M., Geor, R. J., Hinchcliff, K. W., … & Hamilton, K. L. (2014). Participation in a 1000-mile race increases the oxidation of carbohydrate in Alaskan sled dogs. Journal of Applied Physiology, jap-00588.
  1. Jentjens, R., & Jeukendrup, A. E. (2003). Determinants of post-exercise glycogen synthesis during short-term recovery. Sports Medicine, 33(2), 117-144.
  1. Fournier, P. A., Fairchild, T. J., Ferreira, L. D., & Bräu, L. (2004). Post-exercise muscle glycogen repletion in the extreme: effect of food absence and active recovery. Journal of sports science & medicine, 3(3), 139.

Images: here

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