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Can endurance athletes perform well with a very low carbohydrate diet? (Part 1).

Introduction

Nutrition for endurance athletes has long been centered on carbohydrate consumption. Whether looking at pre- and post-competition nutrition, or looking at nutritional patterns over the course of a training year, most recommendations include a diet based predominantly on carbohydrate (1,2). The resurgence in popularity of low carbohydrate diets in the early 2000s centered mostly upon weight loss and the management of disease. Though there were limited data available at that time, there have since been hundreds of studies supporting the efficacy of low carbohydrate diets for weight loss and for managing chronic disease, most specifically type 2 diabetes. Low carbohydrate diets consistently and predictably reduce fasting and postprandial triglycerides and often lead to increases in HDL-cholesterol along with favorable changes in lipid particle profile (3). Due to these types of findings, there are recent calls for changes in the Dietary Guidelines for Americans (4,5), citing, among many other factors, that basing the diet on carbohydrate may be predisposing many people to obesity and the related comorbidities.

Panning over to the subset of our population that is endurance athletes, at first glance it may seem counterintuitive to even consider a low carbohydrate diet. First, just about every recommendation available to endurance athletes over the past several decades has the majority of kilocalories coming from carbohydrate. Consuming a low carbohydrate diet would go completely against almost every recommendation in print. Second, endurance athletes are probably thought to be some of the people at the lowest risk for obesity and type 2 diabetes.

Though interconnected, the topics of guidelines for health and performance and the effects of dietary pattern on treating metabolic disease are not the focus of this paper. This paper is about performance. Ultimately, the question to be answered is "can an endurance athlete perform well while consuming a very low carbohydrate diet"?

Defining low carbohydrate diet

Table 1 was created based on several sources (6,7). No single, widely-accepted definition of a low carbohydrate diet exists. Regardless, restriction of carbohydrate is probably better depicted on a continuum with thresholds for various degrees of restriction.

Given the lack of any widely-accepted definition, when reviewing literature germane to low carbohydrate diets, it is important to understand what participants actually ate. As our group reported previously, literature examining low carbohydrate diets ranges from carbohydrate intakes of 5-40% of total kcal (8). That range could have a difference of hundreds of grams of carbohydrate per day. If the typical American is eating approximately 50% of their kilocalories from carbohydrate, then eating 40% of kilocalories from carbohydrate is a form of restriction, but would have very different effects on physiology as compared to a diet with 10% of kilocalories from carbohydrate.

Ketones and ketoadaptation

A "ketogenic" diet or a "very low carbohydrate diet" is the intake pattern with the fewest dietary carbohydrates consumed. Most evidence supports that the intake of fewer than 50 grams/day of dietary carbohydrate leads to the production of measurable amounts of ketones (7,9). Figures 1A aid IB depict how ketogenesis becomes upregulated when switching from habitual diet (Figure 1A) to a ketogenic diet (Figure IB). Ketogenesis begins when liver glycogen becomes reduced, as is seen in either fasting or low consumption of dietary carbohydrate. With adoption of a very low carbohydrate diet, the onset of traceable ketones generally takes 2-4 days. The ketone formation is a result of accelerated fat utilization; the pathways of lipolysis, fatty acid transport, and beta oxidation are all increased (7). The result of increases in these pathways is an elevated amount of acetyl-CoA being available for oxidation in the Krebs Cycle. Acetyl-CoA enters die Krebs cycle by combining with oxaloacetate to form citrate. This match between Acetyl-CoA and oxaloacetate occurs on a 1:1 basis.

[FIGURE 1A OMITTED]

When the generation of Acetyl-CoA exceeds the capacity of oxaloacetate, the Acetyl-CoA is then diverted to the synthesis of ketone bodies, Figure IB, which include [beta]-hydroxybutyrate, acetoacetate, and acetone. Ketone generation occurs mostly in the liver in the mitochondrial matrix. Blood ketone levels reach approximately 1-3 mmol/L during a ketogenic diet (vs approximately 0.1 mmol/L under a typical habitual diet), an environment often referred to as "physiological ketosis" (10). During these conditions, cells dependent on glycolysis (ex: red blood cells) use glucose derived from gluconeogesis, the precursors for which are glycerol, lactate, and glucogenic amino acids. Ketones spare the use of amino acids and glucose, being used as a fuel source for many tissues, including the brain (11).

Interestingly, reducing dietary carbohydrate imposes many of the same metabolic effects of starvation (12-14), yet people are not actually starving.

The pathway of ketogenesis is also highly upregulated in the presence of very low levels of insulin, as seen in type 1 diabetes. An important note is that ketone levels seen diabetic ketoacidosis tire > 25 mmol/L, which exceeds levels seen during starvation or with the consumption of low levels of dietary carbohydrate 3-4 fold, and is known as "pathological ketosis" due to effects on the blood pH (10). When people are consuming a ketogenic diet, urinary ketones are often measured as a metric of compliance (15), given that consumption of more than 50 grams of carbohydrate per day almost instantly results in ketone levels being reduced to below traceable levels.

Typically, when people are consuming a ketogenic diet they would consume unlimited quantities of fish, meat, poultry, and eggs, cheese, and non-starchy vegetables, with limited quantities of starch vegetables as well as nuts and berries. There are no limits on type or quantity of dietary fats or dietary cholesterol. People would avoid cereal, bread, pasta, rice, desserts, many fruits, and all fruit juices and soft drinks (16). The carbohydrate present in the diet is residual, and mostly from the vegetable intake. The diet is not necessarily a "high protein" diet (generally 20-35% of kilocalories); the diet is based on fat, and proper care should be taken for adequate fat intake. Furthermore, mineral intake is also an important consideration, with particular focus on sodium and potassium since an inadequate intake of these minerals is more likely on a very low carbohydrate diet (6,17). There are a number of resources available with detailed examples of dietary plans, recipes, etc. (7,10,18,19). As carbohydrate intake increases, but remains below average intake, the type of carbohydrate restriction can be categorized as in Table 1.

Generally, when people eat carbohydrate, they use carbohydrate as a predominant source for fuel. When carbohydrate is not available, or ingested carbohydrate is present in insufficient amounts to meet fuel demands, reliance for energy shifts to fat (20). When people switch from a habitual diet to a ketogenic diet, the predominant fuel source becomes fat. The transition from relying largely on carbohydrate to relying on fat and ketones for fuel is referred to as "ketoadaptation," and the process of ketoadaptation has been known for some time with documentation of the concept more than 130 years ago (10). Ketoadaptation involves the upregulation of enzymes in pathways utilizing ketones and fatty acids for fuel, and takes from one to four weeks (6,10,17). Whether or not an individual is ketoadapted is a very' important consideration when evaluating performance measures.

[FIGURE 1B OMITTED]

Evidence supporting low carbohydrate intake in endurance athletes

The energy demands for endurance athletes have been depicted elsewhere. Briefly, the predominant source for ATP while exercising below the lactate threshold is fat but the degree to which fat is used varies between individuals. The majority' of any competitive endurance event is spent at intensities below the lactate threshold. As people become more trained, they are able to complete more work at a given exercise intensity, and the more individuals are able to rely on fat as the primary energy source, the more they are able to conserve glucose. Ultimately, becoming the best "fat burner" possible is probably, in theory, an excellent way to approach the energetics goals of an endurance athlete. As is eloquently described by Volek and Phinney (19), we have VASTLY more fat energy stored in our bodies than carbohydrate (20 fold or more), so it is unfortunate that any endurance athlete could experience a "bonk" with an incredible fuel reserve still present.

Considerable evidence exists to support the use of ketogenic diets in endurance athletes. One of the earliest studies done was by Phinney et al in 1980 (12). Participants were not endurance athletes, but moderately obese sedentary adults (n=6) who underwent an in-patient, protein-supplemented (1.2 g/kg/d) fast for six weeks, and no exercise training occurred during the treatment period. Exercise capacity, as measured by VO2max, was measured at baseline and week six. Since weight loss was an average of 10.6 kg by week six, the amount of weight lost by each participant was placed in a backpack and worn by the participant at the post-testing. VO2max was unchanged from baseline to week six. Two very interesting findings emerged. In addition to the VO2max testing, participants completed an endurance test to exhaustion at baseline and week six and had a muscle biopsy taken before and after the endurance exercise test to measure muscle glycogen. Time to exhaustion was 155% longer at week six as compared to baseline; however, it is important to note that exercise intensity at the post test (60 [+ or -] 1%) was completed at a significantly lower percentage of VO2max as compared to the baseline test (75 [+ or -] 3%). The pre-exercise muscle glycogen at week six was 32% lower at week six than at baseline. However, at baseline, muscle glycogen decreased by 15% after the endurance test, whereas at week six, muscle glycogen remained virtually unchanged (-2%). Secondly, the respiratory quotient (RQ; indicator of fuel utilization) values decreased significantly during the endurance exercise test at week six when compared to baseline, indicating an increased reliance on lipid. The robust change in fat utilization and glycogen sparing are very interesting in this early study, but a number of factors Emit these findings.

To address limitations of the 1980 study, Phinney et al. (14) then recruited five highly-trained cyclists who were fed a eucaloric ketogenic (<20 grams carbohydrate per day) diet for four weeks, while maintaining their training routine. VO2max and exercise time to exhaustion at 6264% of VO2max was unchanged from baseline to week four. However, the RQ dropped significantly from baseline to week four, which corresponded to an average fat oxidation of 1.5 grams per minute (21). That finding is extremely significant since the upper limit of fat oxidation is thought to be approximately 1.0 gram per minute in people eating a mixed diet (22). Glucose oxidation was three times lower at week four than at baseline. Furthermore, muscle glycogen utilization was four times lower during exercise to exhaustion at week four when compared to baseline (14). These results indicate that a ketogenic diet led endurance athletes to significantly increase fat oxidation capacity and more effectively spare glucose, with no decrement in performance.

Using a crossover design, Zajac (23) examined the effects of a four-week ketogenic diet on aerobic performance measures in eight trained off-road cyclists. Compared to a mixed diet, the ketogenic diet led to increased fat utilization during exercise, as well as increases in relative VO2max and increased oxygen consumption at the lactate threshold. Importantly, these changes in oxygen consumption and relative capacity were explained by the changes in body weight that accompanied the ketogenic diet. The maximum work load and the work done at the lactate threshold were higher after the mixed diet as compared to the ketogenic diet. These data support the use of a ketogenic diet during lower to moderate intensity, higher volume endurance exercise, but limitations may exist during maximal-effort attempts or sustained, higher intensity training. Others have also reported similar findings of increased capacity for fat oxidation after a low carbohydrate diet (24-26).

One of the limitations of the studies done on ketogenic diets is that they are of a relatively short term (i.e. only a matter of weeks). Recently, Volek et al. (21) reported on the Fat Adapted Substrate use in Trained Elite Runners (FASTER) study, which was designed to examine the metabolic differences between competitive ultra-marathoners and ironman-distance triathletes consuming low carbohydrate and high carbohydrate diets. Participants were matched for anthropometries and competition characteristics. Participants underwent two days of testing; on the first day testing was completed to determine VO2max and peak fat oxidation. On the second day participants completed a three-hour treadmill run at 64% of their VO2max. The low carbohydrate group had been consuming less than 10% of kilocalories from carbohydrate for 9-36 months, whereas the high carbohydrate group had been consuming approximately 59% of kilocalories from carbohydrate for at least six months. The primary Ending was that peak fat oxidation was 2.3 times higher in the low carbohydrate group as compared to the high carbohydrate group. Interestingly, the peak fat oxidation in the low carbohydrate group ranged from 1.15 to 1.74 grams per minute, and every subject in that group had a value that exceeded the highest value in the high carbohydrate group (0.4-0.87 grams per minute). The total energy used during the endurance run were not different between groups, but the low carbohydrate group had a much higher contribution from fat (88%) compared to the high carbohydrate group (56%). These results confirm earlier findings by Phinney et al. (14) in terms of maximum fat utilization values after adaptation to a very low carbohydrate diet, and further support the evidence that adopting a very low carbohydrate diet significantly increases the reliance on fat while performing endurance exercise.

More work has also been done examining the sedentary, obese population than with endurance athletes. The findings are similar in that a ketogenic diet increases fat oxidation and either no change (27) or an increase in VO2max (28) as compared to a high-carbohydrate diet. Not all studies are in agreement about the effects of a ketogenic diet on endurance exercise performance (29). Due to methodological and subject differences, changes in body weight, and the importance of ketoadaptation, considerable additional work is necessary in this area to improve upon the understanding of the ketogenic diet as related to exercise performance.

Conclusion

High carbohydrate diets increase muscle glycogen and have been shown to improve performance, but also increase the rate of carbohydrate use during exercise. Since we have a limited ability to store carbohydrate, sources must be regularly replenished during endurance training and competition. The potential for endurance athletes to switch to becoming preferential and efficient fat users can be realized through the adoption of a ketogenic diet. Research is still somewhat limited, but anecdotal accounts are increasingly common. Nutrition is a very individualized subject; the aforementioned evidence supports ketogenic diets as an option for some endurance athletes. Adoption of a ketogenic diet must be done with care, and proper resources should be consulted (19). Of particular importance are sodium and potassium intake, moderating protein intake, and optimizing fat intake. Furthermore, a period of ketoadaptation is critical and should be accounted for in any training/ competition periodization planning. Although the safety of ketogenic diets has been shown through a considerable body of research and clinical application, concern about side effects for competitive athletes still exist, including dehydration and kidney stones (23), and should be considered on an individual basis by athletes.

Ketogenic diets are becoming well-known among trainers and athletes. Part II of this series will discuss the practical aspects of a ketogenic diet. It will include issues such as implementation, monitoring, and possible side effects when used as part of an overall endurance training program.

REFERENCES

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(12.) Phinney SD et al. Capacity for moderate exercise in obese subjects after adaptation to a hypocaloric ketogenic diet. J Clin Invest 1980;66(5):1152-61.

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(15.) Sharman M and Volek JS. Weight loss leads to reductions in inflammatory biomarkers after a very-low-carbohydrate diet and a low-fat diet in overweight men. Clin Sci 2004;107(4):365-9.

(16.) Sharman M et al. Very low-carbohydrate and low-fat diets affect fasting lipids and postprandial lipemia differently in overweight men. J Nutr 2004;134(4):880-5.

(17.) Phinney SD. Ketogenic diets and physical performance. J Nutr Metab 2004;1:2.

(18.) Phinney SD and Volek JS. The Art and Science of Low Carbohydrate Living: An Expert Guide to Making the Life-Saving Benefits of Carbohydrate Restriction Sustanable and Enjoyable. Beyond Obesity LLC, 2011.

(19.) Volek JS and Phinney SD. The Art and Science of Low Carbohydrate Performance. Beyond Obesity LLC, 2012.

(20.) Flatt JP McCollum Award Lecture, 1995: diet, lifestyle, and weight maintenance. AJCN 1995;62(4):820-36.

(21.) Volek JS et al. Metabolic characteristics of keto-adapted ultra-endurance runners. Metabolism 2016;65(3):100-10.

(22.) Venables MC et al. Determinants of fat oxidation during exercise in healthy men and women: a cross-sectional study. J Appl Physiol 2005;98(1):160-7.

(23.) Zajac A et al. The effects of a ketogenic diet on exercise metabolism and physical performance in off-road cyclists. Nutrients 2014;6:2493-2508.

(24.) Burke LM et al. Adaptations to short-term high-fat diet persist during exercise despite high carbohydrate availability. MSSE 2002;34(1):83-91.

(25.) Lambert EV et al. High-fat versus habitual diet prior to carbohydrate loading. Effects on exercise metabolism and cycling performance. Int J Sports Nutrition Exerc Metab 2001;11:209-225.

(26.) Helge JW et al. Fat utilization during exercise: adaptation to a fat-rich diet increases utilization of plasma fatty acids and very low density lipoprotein-triacylglycerol in humans. J Physiol 2001;15:1009-20.

(27.) Brinkworth GD et al. Effects of a low carbohydrate weight loss diet on exercise capacity and tolerance in obese subjects. Obesity 2009;17(10):1916-23

(28.) Wycherley TP et al. Long-term effects of a very low-carbohydrate weight loss diet on exercise capacity and tolerance in overweight and obese adults. J Am Coll Nutr 2014;33(4):267-73.

(29.) White AM et al. Blood ketones and directly related to fatigue and perceived effort during exercise in overweight adults adhering to low-carbohydrate diets for weight loss: a pilot study. J Am Dietetic Assoc 2007;107(10):1792-6.

By Richard Wood, PhD

Dr. Richard Wood is an associate professor of exercise science at Springfield College in Springfield, Massachusetts, where his research interests focus on how dietary changes impact chronic metabolic disease and sport performance. Dr. Wood was a speaker at the AMAA's 45th annual Sports Medicine Symposium at the Boston Marathon (2016) in April. His website focuses on helping people understand nutrition and can be found at www.drrichwood.com. He is an avid hockey player and youth coach.
Table 1

Reference                Percent of                Grams of
Term                    kcal from CHO             CHO / day

Western Diet                 ~50        [greater than or equal to] 250
Reduced Carbohydrate        25-40                  125-200
Low Carbohydrate            10-25                   50-125
Very Low Carbohydrate
/ Ketogenic                  <10                     <50
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Date:Mar 22, 2016
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