For at least the last century, nearly every track and field coach in America has ended practice the day before a big meet with the same advice: "make sure you carbo-load tonight!" This dogma that successful athletes must consume a diet rich in carbohydrates has gone mostly unchallenged. Yet, over the past 2 million or so years since we evolved from our nearest ape ancestors, the human body's energy reserves have come almost exclusively from fats and not from carbohydrates.¹ Only in the last 10,000 years has agrarian culture grown enough to shift human diets to starch-laden regimens. Have our green thumbs outsmarted eons of metabolic evolution? Or has this dietary change been an ill-advised pivot away from low carbohydrate diets?

With the "keto craze" sweeping the country,² physicians are frequently faced with questions around both the safety and the efficacy of low carbohydrate diets. A ketogenic diet by definition is one in which less than 10% of total daily caloric intake (approximately 10-30 grams) come from carbohydrates, with remaining calories largely coming from fats (approximately 50-60%) and protein (approximately 20-30%). By depriving the body of carbohydrates over prolonged periods, the body depletes glycogen reserves and instead metabolizes fat stores for energy via a process called ketosis. During ketosis, fats are converted to ketone bodies. The body utilizes ketones as fuel, preferentially first by the brain but eventually also by skeletal and cardiac muscle. One could imagine many positive changes from a persistent low glucose and low insulin state, including weight loss, improvement in glycated hemoglobin A1c, and perhaps even lowering serum cholesterol. Given the higher energy content per unit mass in fats relative to carbohydrates and the greater overall amount of fat stores in the body, one could further postulate that being able to efficiently mobilize fat during exercise could lead to greater athletic performance, specifically benefiting human endurance.

There is great interest among the general population around the potential for low carbohydrate diets to result in weight loss and to reduce cardiovascular risk.³ Early data has been promising, but far from conclusive. In the short to intermediate term, low carbohydrate diets have been effective in increasing early weight loss, improving appetite control, improving glycemic control, decreasing insulin levels, decreasing insulin resistance, and reducing serum triglycerides. There have been admittedly variable effects on serum low-density lipoprotein levels.⁴ Multiple meta-analyses comparing low-carbohydrate diets to isoenergetic diets with greater carbohydrate contents have found small but notable differences in net weight loss at 6 and 12 months.^5-7 There are signs that the low carbohydrate diets may be superior for weight maintenance after the initial period of weight-loss.⁸ In response to these findings, a consensus statement was recently released from the National Lipid Association asserting that "low carbohydrate diets may be an option for short-term initial weight loss, [but for] long-term weight maintenance and cardiovascular health it is recommended to gradually increase carbohydrate intake".⁴ We suspect there is, at a minimum, a role for short term use of a low carbohydrate diet to accelerate weight loss and instill behavioral change.

A question more specifically directed to the Sports Cardiologist from athletes is, "will a low carbohydrate diet improve my performance?" Physiologically, carbohydrate-loading is ostensibly rational. Muscles burn glycogen – stores of carbohydrates in the body – rapidly, with few intermediate metabolic steps.⁹ Glycogen, however, is a limited resource in the body. High-intensity exercise capacity and performance quickly deteriorate with reduced carbohydrate availability.¹⁰ When athletes run out of glycogen stores, the dramatic and sudden decrease in performance even has a colloquial name: "hitting the wall."¹¹ Compared to glycogen, the body's adipose reserves are much more abundant. Even the thinnest of endurance runners harbors in excess of 30,000 kilocalories in the form of fat.¹ The downside of this energy source is that fat is not as readily metabolically available as carbohydrates. Long fatty-acid chains must be broken down in a multistep process to form ketone bodies. During low and even moderate intensity exercise, the body primarily utilizes these ketones for energy. During high intensity exercise, on the other hand, lipolysis cannot meet the body's energy requirements. High intensity exercise necessitates a gradual shift towards glycolysis and eventually anaerobic metabolism to predominate energy production.¹² But are lipolysis rates fixed, or can they be ramped up with the right diet and training? Can lipolysis fuel high-intensity exercise?

In 1983, Phinney et al conducted two studies demonstrating the process of keto-adaptation. Keto-adaptation is the ability of the body to augment rates of ketone production when the body is deprived of carbohydrates.^13,14 During the first week of Phinney's study, serum beta-hydroxybutyrate levels rose and endurance capacity waned in the test subjects. Beta-hydroxybutyrate is the prominent ketone produced during lipolysis. Subjects felt fatigued and irritable, a fact which anyone who has trialed a low carbohydrate diet can easily believe. By the fourth week, though, the subjects' moods had improved and impressively greater than 90% of the fuel the subjects utilized during sub-maximal exercise tests was derived from fatty oxidation. While there was no net difference in endurance capacity in the low carbohydrate group compared to the mixed diet group, the study was an important proof-of-concept that a low carbohydrate diet, when maintained for an extended period of time, can provide adequate energy production during sub-maximal exercise. In endurance athletes, the augmentation of lipolysis rates theoretically can facilitate extended performance without the need for ongoing carbohydrate replacement. It remains to be seen if lipolysis can augment quickly enough to provide adequate energy production for high intensity exercise, but as of now there is no known ceiling on keto-adaptation.¹⁵

There are numerous other possible off-target benefits of a low carbohydrate diet that may interest the athlete. Ketone metabolism is believed to directly decrease exercise-associated inflammation through several pathways, including decreased lactate production, reduced histone-deacetylase enzymatic activity, and reduced production of reactive oxygen species.¹ It is no surprise then that some ultra-marathoners have anecdotally reported decreased soreness and faster recovery times with low carbohydrate diets.¹ Gastrointestinal (GI) upset is one of the most common causes of marathon runners to fail to finish races. Many runners have had significant success at eliminating symptoms after keto-adaptation.¹⁶ This decrease of GI upset may similarly be due to decreased inflammation, though more stable serum levels of fuel could also play a role. A more stable fuel source has also been cited as causing less fluctuation in mental status, helping to avoid the confusion that can occur when the athlete "hits the wall". While all of these data are preliminary, the benefits, theoretical or anecdotal, coupled with the suggestion of enhanced endurance from more efficient lipolysis, merit further exploration of the role low carbohydrate diets in athletic training. Interestingly, many have suggested there may be a role for focused durations of training with a low carbohydrate diet and then transitioning away from ketosis back towards carbohydrates closer to competition.¹⁷

Early work in this field is promising, but further research on low carbohydrate diets regarding the safety, optimal duration, and impact on cardiovascular outcomes are needed. While weight loss is known to lower cardiovascular events and mortality, the vast majority of studies of the low carbohydrate diet do not include data regarding event reduction. One notable short-term safety concern for athletes is ketosis-induced volume depletion, a not uncommon side effect that is manageable with direct patient conseling.¹⁸ There is also a weak suggestion of increased risk for sudden death and myotoxicity with initiation of a low carbohydrate diet.^18,19 The risk, if it exists at all, is likely quite small but it merits long-term follow-up. Lastly, it can be challenging to craft a palatable experience under the restrictions of the low carbohydrate diet, but it is not impossible. A related pragmatic concern with the low carbohydrate diet has been the replacement of carbohydrates with higher risk saturated fats like butter, cream, and deserts with potentially negative cardiovascular effects. This may be reflected in the higher low-density lipoprotein levels seen in some studies of the low carbohydrate diet.^5-7 Consuming healthier fat sources such as nuts, avocados, unsaturated oils, dairy, and even a few low carbohydrate fruits and vegetables is preferable. A diet focusing on these foods may mitigate the lipogenesis seen in some earlier studies of the low carbohydrate diet.⁴ With appropriate guidance from a dietician and associated resources, it is feasible to craft a safe and effective diet utilizing ketogenic principles.^4,16

The longest study examining the cardiovascular benefits of low-carbohydrate diets is two years in length. In the athletic population, studies which investigated low-carbohydrate diets were just weeks in duration, and they may have had inadequate carbohydrate restrictions in order to even achieve steady state nutritional ketosis.^10,20,21 However, the biochemical plausibility of superior performance sustainability with a low carbohydrate diet remains.¹⁷ Low carbohydrate diets have also been associated with challenges in long-term sustainability, but we propose that benefit from these diets is likely optimal in short duration as a tool to instill behavioral change in nutritional habits.²²

Overall, there are multiple short-term advantages to low carbohydrate diets beyond just the benefit of weight-loss.⁴ The long-term cardiovascular effects of a low carbohydrate diet clearly require further study. For the athlete, after achieving and sustaining nutritional ketosis, the human body can increase lipolysis rates to provide almost all of the body's fuel for exercise, particularly for exercise of low to moderate intensity.^1,14 This can theoretically provide a distinct advantage over carbohydrate-based metabolism, especially for endurance athletes tapping into their much larger fat-store reservoirs. There are multiple "off-target" effects, including decreased inflammation and decreased gastrointestinal upset. While the low carbohydrate diet is not for every athlete, the invested athlete may improve his or her performance with keto-adaptation. Future study should also investigate periodization of diets, such as the "train low, race high" strategy,¹⁷ perhaps maximizing benefits of both low and more traditional high carbohydrate approaches. In the end, dietary options are not a "one size fits all", and the discussion must be tailored appropriately for each individual athlete.

References

1. Volek JS, Noakes T, Phinney SD. Rethinking fat as a fuel for endurance exercise. Eur J Sport Sci 2015;15:13-20.
2. Wiener-Bronner D. The keto craze is hitting the mainstream (CNN Business website). 2018. Available at: https://money.cnn.com/2018/09/17/news/companies/keto-diet-trend/index.html. Accessed December 15, 2019.
3. O'Connor A. The Keto diet Is popular, but is it good for you? (New York Times website) 2019. Available at: https://www.nytimes.com/2019/08/20/well/eat/the-keto-diet-is-popular-but-is-it-good-for-you.html. Accessed December 15, 2019.
4. Kirkpatrick CF, Bolick JP, Kris-Etherton PM, et al. Review of current evidence and clinical recommendations on the effects of low-carbohydrate and very-low-carbohydrate (including ketogenic) diets for the management of body weight and other cardiometabolic risk factors: a scientific statement from the National Lipid Association Nutrition and Lifestyle Task Force. J Clin Lipidol 2019;13:689-711.
5. Qian F, Korat AA, Malik V, Hu FB. Metabolic effects of monounsaturated fatty acid-enriched diets compared with carbohydrate or polyunsaturated fatty acid-enriched diets in patients with type 2 diabetes: a systematic review and meta-analysis of randomized controlled trials. Diabetes Care 2016;39:1448-57.
6. Schwingshackl L, Hoffmann G. Comparison of effects of long-term low-fat vs high-fat diets on blood lipid levels in overweight or obese patients: a systematic review and meta-analysis. J Acad Nutr Diet 2013;113:1640-61.
7. Naude CE, Schoonees A, Senekal M, Young T, Garner P, Volmink J. Low carbohydrate versus isoenergetic balanced diets for reducing weight and cardiovascular risk: a systematic review and meta-analysis. PloS One 2014;9:e100652.
8. Clifton PM, Keogh JB. Effects of different weight loss approaches on CVD risk. Curr Atheroscler Rep 2018;20:27.
9. Roach PJ, Depaoli-Roach AA, Hurley TD, Tagliabracci VS. Glycogen and its metabolism: some new developments and old themes. Biochem J 2012;441:763-87.
10. Zajac A, Poprzecki S, Maszczyk A, Czuba M, Michalczyk M, Zydek G. The effects of a ketogenic diet on exercise metabolism and physical performance in off-road cyclists. Nutrients 2014;6:2493-2508.
11. Rapoport BI. Metabolic factors limiting performance in marathon runners. PLoS Comput Biol 2010;6:e1000960.
12. Wolfe RR. Fat metabolism in exercise. Adv Exp Med Biol 1998;441:147-56.
13. Phinney SD, Bistrian BR, Evans WJ, Gervino E, Blackburn GL. The human metabolic response to chronic ketosis without caloric restriction: preservation of submaximal exercise capability with reduced carbohydrate oxidation. Metabolism 1983;32:769-76.
14. Phinney SD, Bistrian BR, Wolfe RR, Blackburn GL. The human metabolic response to chronic ketosis without caloric restriction: physical and biochemical adaptation. Metabolism 1983;32:757-68.
15. Cipryan L, Plews DJ, Ferretti A, Maffetone PB, Laursen PB. Effects of a 4-Week very low-carbohydrate diet on high-intensity interval training responses. J Sports Sci Med 2018;17:259-68.
16. Buyken AE, Mela DJ, Dussort P, et al. Dietary carbohydrates: a review of international recommendations and the methods used to derive them. Eur J Clin Nutr 2018;72:1625-43.
17. Jeukendrup AE. Periodized nutrition for athletes. Sports Med 2017;47:51-63.
18. Hartman AL, Vining EP. Clinical aspects of the ketogenic diet. Epilepsia 2007;48:31-42.
19. Bank IM, Shemie SD, Rosenblatt B, Bernard C, Mackie AS. Sudden cardiac death in association with the ketogenic diet. Pediatr Neurol 2008;39:429-31.
20. Fleming JA, Kris-Etherton PM. Macronutrient content of the diet: what do we know about energy balance and weight maintenance? Curr Obes Rep 2016;5:208-13.
21. Helge JW. A high carbohydrate diet remains the evidence based choice for elite athletes to optimise performance. J Physiol 2017;595:2775.
22. 4. Lifestyle Management: Standards of Medical Care in Diabetes-2018. Diabetes Care 2018;41:S38-s50.

Clinical Topics: Diabetes and Cardiometabolic Disease, Dyslipidemia, Prevention, Sports and Exercise Cardiology, Lipid Metabolism, Nonstatins, Diet

Keywords: Sports, Athletes, Ketone Bodies, Hemoglobin A, Weight Loss, Glycogen, Ketones, Energy Intake, Diet, Carbohydrate-Restricted, Ketosis, Athletic Performance, Myocardium, Cholesterol, Insulins, Glucose

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