The Science of Ketogenic Exercise

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There is remarkably little scientific research available around exercise while on a Ketogenic Diet. For a long time, the only useful research was a single study by Phinney in 1983. While this is a fascinating study, it has few subjects, it has not been confirmed with other studies and the results of the study are somewhat ambiguous. A 2016 study on race walkers has provided more insight, and I've covered both studies in some detail. I've also included some other studies that are on Non-Ketogenic Low Carbohydrate Diets.

1 Burke's Study of Race Walkers

Unlike the Phinney study described below, the study by Burke[1] is not performed by proponents of a low carbohydrate or ketogenic diet. The study seems to have a reasonable approach, though it's not without its flaws. The main problem with this study is that it looks at a relatively small number of subjects, and the subjects are all elite athletes. This means that the findings may not translate to recreational athletes, or even sub-elite athletes. However, I'd argue this is probably the best study we have so far on the ketogenic diet for athletes. The high-level finding of the study is that athletes performed worse on a low carbohydrate, ketogenic diet. The fundamental problem that the study highlights with a low carbohydrate, ketogenic diet is that it requires more oxygen to produce a given amount of energy from fat than it does from carbohydrate. This problem is highlighted not just in the somewhat artificial, laboratory tests, but also in race performances.

  • The study subjects were 21 elite race walkers. Their event is the 20Km race walk, which takes an elite athlete 75-80 minutes and is completed at about 90% of V̇O2max[2]. That means the subjects are focused on a moderate lengths endurance event, roughly similar to runners in a half marathon. The high intensity of this event means that the results might not translate to ultramarathons in the same way.
  • The study took place during a three-week intense training block, that included weight training, race walking, and endurance cross training using running, cycling, or swimming.
  • The subjects were divided into 3 different groups; one group was given a standard high carbohydrate diet (HCHO), another group was given a Low CHO, high fat (LCHF), and the third group cycled between high carb and low carb (Periodised CHO or PCHO). All 3 diets were matched for overall energy intake.
    • The High Carb (HCHO) group got 60-65% of their calories from carbohydrate, 15-20% protein, 20% fat.
    • The Periodised CHO (PCHO) group had the same average nutrient balance as the high carb diet, but performed some of their training in a low carbohydrate or fasted state.
    • The Low CHO, high fat (LCHF) was 75-80% fat, 15-20% protein, and less than 50g of carbohydrate per day. The study doesn't give as many details on the ketone levels as I'd like, but they do measure BOHB (beta-hydroxybutyrate) and show levels well above 1.0 when measured at rest. This indicates the low carbohydrate athletes are clearly in ketosis during the testing phase. Given the overall protocol, I think it's reasonable to conclude that the athletes were keto adapted by the end of the study.
  • There were a number of tests performed, including V̇O2peak, 25Km long walk, and simulated 10Km race. The simulated race even had prize money as incentive, so one could perhaps think of this as more of a true race than a race simulation. In fact, four of the subjects set personal best times in the simulated race, and one even said a national record.
  • The low carbohydrate athletes had problems during training, with higher rates of perceived exertion, and higher heart rates, and the inability to complete some of the training sessions. It's unclear if these problems were only at the beginning of the training, before they'd adapted to the low carbohydrate diet, or if they persisted through to the end.
  • LCHF had problems completing the training, complaining of higher perceived effort and inability to complete the training sessions. (Adaptation period?)
  • The oxygen cost of exercise was higher in the low carbohydrate group than a high carbohydrate group, while the periodised carbohydrate group had a slightly lower oxygen cost and the high carbohydrate group.
  • The subjects performed the simulated race before and after the dietary intervention. The race times were improved in the high carbohydrate group by an average of 190 seconds (114-266) and in the periodised carbohydrate group by 124s (62-186). However, the low carbohydrate group was slower by an average of 23 seconds (162 faster-208 slower). It looks like the low carbohydrate athletes increased their V̇O2peak at the end of the study, but this increase was negated by the impaired economy of higher oxygen cost of exercise. (Note that figure 4 on the early copies of the PDF is wrong on the performance for the low carb group, something I confirmed with the authors.)
  • The low carbohydrate group burned more fat during the end of study tests by a rather dramatic amount.

2 Phinney's Study of Elite Cyclists

A classic study was performed in 1983 by Stephen Phinney on the effect of four weeks on a Ketogenic Diet on 5 elite cyclists, and found that on average their endurance was maintained[3]. However, this average represents two subjects that dramatically improved their endurance, one that didn't change and two subjects that had dramatically reduced endurance. One of the subjects that had reduced performance was Overtrained, and if their results are excluded the average is a 13% improvement.

  • The diet was 15% of calories from protein, 85% from fat, with less than 20g of carbohydrate.
  • Subjects performed V̇O2max and endurance tests before and after the Ketogenic Diet.
  • The five subjects had an endurance time of 147 minutes on the normal diet and 151 minutes on the Ketogenic Diet. However, the individual responses are rather different.
    • Two subjects dramatically increased their endurance time on the Ketogenic Diet, one by 57% and another by 30%.
    • One subject had an almost identical endurance time.
    • Two subjects had a dramatic decrease in their endurance, one by 36% and another by 28%. The subject that decreased their performance by 36% had complained of overtraining and had reduced his training level the month before the trial.
  • Of the five subjects (see table below for details):
    • JP: Endurance improved by 57% and had much lower final muscle Glycogen levels on the Ketogenic Diet than the normal diet (41.5 compared with 59.2).
    • IK: Endurance improved by 30% and had similar final Glycogen levels on normal and Ketogenic Diets.
    • MK: Endurance was the similar (2% improvement) and had higher final Glycogen levels on the Ketogenic Diets.
    • BK: Endurance reduced by 28% and had higher final glycogen levels after the ketogenic endurance test than the normal diet (38.1 compared with 58.4).
    • WB: Endurance reduced by 36%.
      • WB was Overtrained and reduced training volume from 300 miles/week to 100 miles/week.
      • WB had higher final glycogen levels after the ketogenic endurance test than the normal diet.
      • WB had higher VO2 on the Ketogenic Diet.
    • It seems that the low carbohydrate diet is as likely to harm performance as it is to improve it, at least in this study.
  • Blood levels of the Ketone 3-hydroxybutyrate (BOHB), which indicates ketogenisis, were insignificant at rest (0.04 mmol/L) on the normal diet and elevated (1.28 mmol/L) on the Ketogenic Diet. This level of resting BOHB is quite low compared with some levels seen on the ketogenic diet. After the endurance test, the high carbohydrate diet resulted in a slightly elevated blood ketone level of 0.46 mmol/L, which is below the threshold that would normally be considered ketogenic. Rather interestingly, on the ketogenic diet the athletes blood ketone levels actually rose to finish at 2.44 mmol/L. this is a little different to other reports, where led ketone levels start higher, and actually fall during endurance exercise.
  • Unlike typical fat metabolism, the oxygen cost of calories was not different on the Ketogenic Diet. This is a huge deal, as the big problem with burning fat is that it requires more Oxygen to produce the same amount of energy. However Phinney provides no details of the power outputs.
  • The RQ on the VO2max test dropped from 1.04 to 0.9, and on the endurance test from 0.83 to 0.72, indicating a shift in substrate metabolism. However, because Ketone metabolism can produce RQ values that vary significantly, it's not possible to estimate what fuel is being metabolized[4]. (The conversion of fat to Ketones consumes Oxygen without producing Carbon dioxide, the metabolism of Ketones has an RQ of 1.0, with the overall RQ matching that of Fat[4].)
  • The endurance test did not include any fuel, just water. It is likely that the endurance test would have had a better result in the control condition with carbohydrate supplementation. This biases the experiment in favor of low carbohydrate outcomes.
  • The low carbohydrate test was four weeks after the high carbohydrate test, which means the athletes had an extra four weeks of training, which is hard to account for. It seems likely that the athletes should have performed better on the second test, suggesting the low carb diet offset the extra training.
  • Blood glucose during the endurance test was similar after the Ketogenic Diet to before, but the rise and fall were somewhat reduced. At no point did blood glucose drop to the point of hypoglycemia. Blood glucose provided an estimated 28% of calories on the normal diet and 9% of calories on the Ketogenic Diet.
  • Muscle Glycogen levels where higher before the endurance test on the normal diet than on the Ketogenic Diet (143 and 53 respectively). Both tests had similar muscle glycogen levels after the endurance tests. It is interesting to see that muscle glycogen levels were replenished somewhat on the Ketogenic Diet, even though the subjects continued normal training for the four weeks.
Endurace-1 Endurance-2 Change Glycogen Pre-1 Glycogen Post-1 Drop in Glycogen Glycogen Pre-2 Glycogen Post-2 Drop in Glycogen Change in final levels Difference in drop VO2-1 VO2-2 Change RQ-2
JP 148 223 51% 144.8 59.2 -59% 81.7 41.5 -49% -30% -10% 3.30 3.20 -3% 0.65
IK 100 130 30% 179.7 62.9 -65% 67.5 63.5 -6% 1% -59% 3.10 2.97 -4% 0.75
MK 178 181 2% 142.8 46.6 -67% 65.1 57.6 -12% 24% -56% 3.09 3.01 -3% 0.72
BK 169 121 -28% 120.8 38.1 -68% 80.7 58.4 -28% 53% -41% 3.79 3.97 5% 0.72
WB 140 89 -36% 124.9 57.8 -54% 82.6 60.1 -27% 4% -26% 2.61 2.95 13% 0.74
Average 4% -63% 75.5 -24% 10% -38% 2%
Exclude WB 13% -65% 73.8 -24% 12% -41% -1%

3 Other studies

There are a few other studies that are of interest, though they do not directly deal with exercise capacity and the Ketogenic Diet.

3.1 Metabolic characteristics of keto-adapted ultra-endurance runners (FASTER)

This study compares the characteristics of 20 elite endurance athletes, 10 of them having been on a long-term low carbohydrate diet[5]. The study is sometimes referred to by the backronym FASTER (Fat Adapted Substrate use in Trained Elite Runners.) The study has some significant flaws and it's hard to find any useful conclusions. The athletes on the low carbohydrate diet had higher levels of fat burning than their high carbohydrate comparisons, but did not seem to have any of the benefits that high fat burning would normally convey.

  • The subjects were 20 elite ultrarunners or triathletes, finishing in the top 10%, some of them with course records, or national/international records. The athletes had broadly similar average characteristics.
  • While the title of the study suggests that the athletes are on a Ketogenic Diet, this does not appear to be the case. The low carbohydrate athletes had resting Ketone Levels of ~0.7 mmol/L, which I feel is borderline for Ketosis. Their diet indicates their Ketogenic Ratio was only 1:1, which is far too low for Ketosis and there is no information provided to indicate they are Keto-adapted.
  • The study consists of two tests on consecutive days. The first day involved a V̇O2max test and the second day a sub-maximal three-hour treadmill endurance run. The V̇O2max test was after a 4 hour fast, and the endurance run was 90 minutes after a nutrient shake that was different for the high and low carbohydrate athletes. This difference in nutrient intake makes the results endurance run hard to interpret as it's impossible to know if the differences in results are due to the prior nutrition and training, or due to the different nutrient intake.
  • The V̇O2max test resulted in the low carbohydrate athletes had a 2.3x higher peak fat burning capability than the low carbohydrate athletes, both from an absolute and as a percentage of V̇O2max where the peak fat burning occurred. This might suggest that athletes on a low carbohydrate diet adapt to being able to burn fat at a higher rate, or it might suggest that athletes with naturally higher fat burning capability are more likely to choose a low carb diet.
  • The overall V̇O2max for the two groups was broadly similar with an average of 64.7 and 64.3, though both groups had a wide range of 55-76. Therefore it's hard to reach any conclusion on the impact of a low carb diet on V̇O2max.
  • The endurance test was not to exhaustion and is more of a long training run. The intensity was 64% of V̇O2max, which a pace of about 100 seconds/mile slower than marathon pace.
  • The biggest problem with interpreting the endurance test is that not only are the two group of athletes different, but the groups were given a shake with different nutrition 90 minutes before the test. It's impossible to know what variation between the groups results is due to prior training and what is due to the shake.
  • The low carb shake consisted of heavy cream, olive oil, whey protein, walnut oil, and strawberries, which is seems to be a good choice of ingredients. Constructing a shake that is low in carbs but palatable is tricky.
  • The high carb shake is more problematic: It also consisted of the heavy cream, olive oil, whey protein, walnut oil, and strawberries from the low carb shake, plus bananas and agave syrup. The high carb shake is nothing like the nutrition a reasonable athlete would consume. The carbohydrate in agave syrup is 67-90% Fructose[6][7], and this level of Fructose makes this a remarkably poor choice for athletes (or anyone else) as it is extremely slow to digest. The inability to digest the Fructose can be seen in the way the high carb athletes' blood glucose does not rise. It's impossible to know if this was simply a poor choice or if it constitutes an intentional bias intended to promote low carb nutrition.
  • During the endurance test the low carb athletes burned more fat and less carbohydrate than the high carb athletes. Normally an increased fat burning capability is seen as a good thing in athletes as it helps preserves Glycogen, which is typically a limiting factor in endurance events. However, both groups burned through similar amounts of Glycogen. The test was a fixed 3 hour run, so there's no way of knowing if either group would last longer before reaching voluntary exhaustion, but it seems likely that Glycogen levels would limit both groups equally. It also seems likely that a reasonable source of carbohydrate for the high carb group would have resulted in them using less Glycogen than the low carb group. (The study noted that the low carb athletes burned more Glycogen than the estimate for their total carbohydrate burn, which is rather strange.)

3.2 Non-Ketogenic Low Carbohydrate Diet (NKLCD) and Exercise

A 1994 study looked at the effect of a low carbohydrate diet on cycling performance[8]. This study explicitly avoiding being ketogenic, providing calories from 67% fat, 7% carbohydrate and 25% protein, with a control condition of 70% carbohydrate. The exercise test protocol was rather unusual; a maximum strength test was followed by a Wingate test, then a high intensity (85% V̇O2max) endurance test to exhaustion, a 20 minute rest, then a moderate intensity (50% V̇O2max) endurance test to exhaustion. The high fat and high carbohydrate conditions were not statistically different except for the moderate intensity test where the low carbohydrate condition produced significantly better endurance (80 minutes rather than 43.) However, while the high intensity exhaustion test was not significantly different, the low carbohydrate condition was only 8.3 minutes rather than 12.5. This is not statistically significant, but it does suggest the high carbohydrate condition could have been far more tiring than the low carbohydrate condition. There have also been other studies showing that a rest period between exercise bouts can produce low blood glucose[9], so this study might be the result of the rather unusual structure.

3.3 Exercise capacity in obese subjects undergoing Protein Sparing Modified Fast

An earlier study by Phinney looked at untrained, obese subjects that were treated using a Protein Sparing Modified Fast (PSMF) that provided 500-750 Calories/Day[10]. Because a PSMF requires medical supervision, the subjects were in admitted to a medical facility for the 8 week study. Using a treadmill walking test to exhaustion showed that endurance dropped to 80% of baseline after one week, but after Ketoadaptation their capacity increased to 155%. This is a fascinating study, but the nature of the subjects, their weight loss, and the difference between the PSMF and a Ketogenic Diet, all make it hard to draw general conclusions.

3.4 Post-exercise ketosis in post-prandial exercise- effect of glucose and alanine

A study of 33 trained endurance runners on a low carbohydrate diet looked at the effect of glucose and alanine (an amino acid)[11]. The diet was not ketogenic as their blood BOHB was only 0.23 and they were on the diet for only 48 hours before the tests (no Ketoadaptation). This study showed that 50g (200 Calories) of Glucose before or immediately after a 90 minute half-marathon distance run did not impact blood ketone levels. (Taking 50g 2 hours after exercise will cause a dramatic drop in ketone levels). However, the alanine reduced ketone levels when taken before or after the run.

3.5 The effects of a ketogenic diet on exercise metabolism and physical performance in off-road cyclists

This study looks promising, but sadly it does not appear to actually use the Ketogenic Diet[12]. The diet the study used consisted of 70% fat, 15% protein and 15% carbohydrates, and provided an average of 2,865 Calories, which works out to ~145g of carbohydrate per day, a level generally considered far too high to be Ketogenic. In addition, while the Ketone Levels increased, the level of BOHB only rose to 0.15 mmol/L. The recommended minimum level to be considered Ketogenic is 0.2 mmol/L (BOHB+AcAc)[13], though other researchers recommend a BOHB level of 0.5[14]. While the study was not Ketogenic, it had the subjects on the low carbohydrate diet for four weeks to allow adaptation. The low carbohydrate diet reduced body fat, which explained some improved performance metrics. The low carbohydrate diet also resulted in a higher oxygen requirement.

4 See Also

5 References

  1. Louise M Burke, Megan L Ross, Laura A Garvican-Lewis, Marijke Welvaert, Ida A Heikura, Sara G Forbes, Joanne G Mirtschin, Louise E Cato, Nicki Strobel, Avish P Sharma, John A Hawley, Low Carbohydrate, High Fat diet impairs exercise economy and negates the performance benefit from intensified training in elite race walkers, The Journal of Physiology, 2016, ISSN 00223751, doi 10.1113/JP273230
  2. Drake, Andrew, et al. "Physiological variables related to 20 km race walk performance." Journal of Sports Sciences 21 (2003): 269-270.
  3. SD. Phinney, BR. Bistrian, WJ. Evans, E. Gervino, GL. Blackburn, The human metabolic response to chronic ketosis without caloric restriction: preservation of submaximal exercise capability with reduced carbohydrate oxidation., Metabolism, volume 32, issue 8, pages 769-76, Aug 1983, PMID 6865776
  4. 4.0 4.1 Y. Schutz, E. Ravussin, Respiratory quotients lower than 0.70 in ketogenic diets., Am J Clin Nutr, volume 33, issue 6, pages 1317-9, Jun 1980, PMID 7386422
  5. Jeff S. Volek, Daniel J. Freidenreich, Catherine Saenz, Laura J. Kunces, Brent C. Creighton, Jenna M. Bartley, Patrick M. Davitt, Colleen X. Munoz, Jeffrey M. Anderson, Carl M. Maresh, Elaine C. Lee, Mark D. Schuenke, Giselle Aerni, William J. Kraemer, Stephen D. Phinney, Metabolic characteristics of keto-adapted ultra-endurance runners, Metabolism, volume 65, issue 3, 2016, pages 100–110, ISSN 00260495, doi 10.1016/j.metabol.2015.10.028
  6. DP. Figlewicz, G. Ioannou, J. Bennett Jay, S. Kittleson, C. Savard, CL. Roth, Effect of moderate intake of sweeteners on metabolic health in the rat., Physiol Behav, volume 98, issue 5, pages 618-24, Dec 2009, doi 10.1016/j.physbeh.2009.09.016, PMID 19815021
  7. M. SRINIVASAN, IS. BHATIA, The carbohydrates of Agave vera cruz Mill. 2. Distribution in the stem and pole., Biochem J, volume 56, issue 2, pages 256-9, Feb 1954, PMID 13140183
  8. EV. Lambert, DP. Speechly, SC. Dennis, TD. Noakes, Enhanced endurance in trained cyclists during moderate intensity exercise following 2 weeks adaptation to a high fat diet., Eur J Appl Physiol Occup Physiol, volume 69, issue 4, pages 287-93, 1994, PMID 7851362
  9. M. Russell, D. Benton, M. Kingsley, Carbohydrate ingestion before and during soccer match play and blood glucose and lactate concentrations., J Athl Train, volume 49, issue 4, pages 447-53, doi 10.4085/1062-6050-49.3.12, PMID 24933430
  10. SD. Phinney, ES. Horton, EA. Sims, JS. Hanson, E. Danforth, BM. LaGrange, Capacity for moderate exercise in obese subjects after adaptation to a hypocaloric, ketogenic diet., J Clin Invest, volume 66, issue 5, pages 1152-61, Nov 1980, doi 10.1172/JCI109945, PMID 7000826
  11. JH. Koeslag, LI. Levinrad, JD. Lochner, AA. Sive, Post-exercise ketosis in post-prandial exercise: effect of glucose and alanine ingestion in humans., J Physiol, volume 358, pages 395-403, Jan 1985, PMID 3884775
  12. Adam Zajac, Stanisław Poprzecki, Adam Maszczyk, Miłosz Czuba, Małgorzata Michalczyk, Grzegorz Zydek, The Effects of a Ketogenic Diet on Exercise Metabolism and Physical Performance in Off-Road Cyclists, Nutrients, volume 6, issue 7, 2014, pages 2493–2508, ISSN 2072-6643, doi 10.3390/nu6072493
  13. AM. Robinson, DH. Williamson, Physiological roles of ketone bodies as substrates and signals in mammalian tissues., Physiol Rev, volume 60, issue 1, pages 143-87, Jan 1980, PMID 6986618
  14. Phd Stephen D. Phinney MD, Rd Jeff S. Volek Phd, The Art and Science of Low Carbohydrate Living: An Expert Guide to Making the Life-saving Benefits of Carbohydrate Restriction Sustainable and Enjoyable, 2011, publisher Beyond Obesity LLC, isbn 978-0-9834907-0-8, Page 31