Expert Opinion: "Crazy for Ketones" – The Ketogenic Diet in Athletes: Variable Effects on Athletic Performance with Potential for Cardiovascular Harm

Athletic performance and physique have been closely associated with diet and nutrition for ages. From the high-carbohydrate, predominantly vegetarian diet of gladiators, warriors referred to as hordearii meaning "barley men," to the creation of Gatorade in 1965, there is a countless number of diet plans touted as ideal for maximizing athletic performance.1,2 One such diet is the ketogenic diet, increasingly favored by many athletes. Despite its growing recognition, in my opinion, I do not recommend athletes follow this diet due to the high variability in performance results and its capacity to cause detrimental cardiovascular effects.

Traditional fueling strategies have emphasized high carbohydrate utilization for maximal athletic performance in endurance sports. However, in recent years, the ketogenic diet has grown in popularity due to reported benefits from reducing carbohydrate availability and maximizing fatty acid activation as the predominant fuel source for exercise.3 The original ketogenic diet is centered upon 75-80% fat intake, 15% protein, and less than 5% carbohydrates per day. This anticipates that glucose reserves will be depleted after as little as five days, thus halting normal fat oxidation and glucose supply to the brain and central nervous system and leading to the accumulation of ketone bodies.4,5

Although there are no long-term studies comparing the effects of ketogenic to high carbohydrate diets on athletic performance, conclusions from short-duration studies are mixed. One study examining the effects of high-fat and high-carbohydrate diets on metabolism and athletic performance in endurance cyclists showed that high-fat conditions over a 2-week period were associated with greater lipolysis and fuel availability, lower plasma insulin concentration before exercise, and a 2.5 to 2.9-fold significant increase in fat-oxidation rates. Additionally, power increased by 2% for every 10% energy increase in fat, though this result was not statistically significant.6 In contrast, oxygen demand at a specific speed in elite race walkers, who were adapted to a ketogenic low carbohydrate-high fat diet over 3 weeks, increased and effectively negated the significant improvement in oxygen consumption.7 Ultimately, the variability in performance in athletes following a ketogenic diet is highly dependent upon exercise intensity with greater impairment seen in high intensity, anaerobic exercise. In Dr. Stephen Phinney's 1980's study of five well-trained cyclists following a high fat diet with significant carbohydrate restriction (<20 grams/day), their ability to exercise anaerobically was significantly impaired.8,9 While endurance training may enhance an athlete's capacity for fat oxidation, the increase in fatty acid availability for fuel cannot compensate for the low muscle glycogen stores, which can subsequently impair exercise capacity.10

An individual athlete generally decides his/her preference for sport nutrition based upon performance goals. However, as sports cardiologists, it is imperative that we discuss the longitudinal impact of specific diets on an athlete's cardiovascular health, particularly since diets that increase cardiac risk may hinder future athletic performance. The ketogenic diet is predicated on high fat consumption for fat-adaptive fueling as well as increased protein consumption, with carbohydrate intake typically less than 30 grams per day.11 Consequently, the type of fat (saturated versus unsaturated) and protein (animal versus plant) can influence cardiovascular risk. While mitigating cardiovascular risk is important for athletes of all ages, masters athletes (age 35 years or greater) are particularly susceptible to greater risk of cardiovascular morbidity and mortality with ketogenic diets that incorporate high saturated fat and animal protein consumption. Additionally, athletes with a family history of premature coronary artery disease and myocardial infarction should also be counseled on reducing animal-based food sources to reduce saturated fat intake and inherently cardiac risk.

Not only does diet impact athletic performance, but it also provides a means to develop sport-specific body composition that supports the level of athleticism required. For instance, athletic performance in weightlifters is predicated upon building muscle mass, and thus the macronutrient composition (protein, fat, carbohydrate) of their diets is skewed towards high protein and low carbohydrate intake. Although a low carbohydrate-ketogenic diet shows benefit in achieving an optimal power-to-weight ratio without compromising lifting performance, the cardiovascular consequences persist depending upon food source (plant versus animal).12 American football linemen require an increase in both muscle mass and total body mass, often relying on heavy intake of all macronutrients, which is synonymous with increased caloric intake. Fat, being the most calorically dense macronutrient, is a key component to these athletes' diet, and more often than not, saturated fat intake far outweighs unsaturated fat intake. In a study assessing dietary composition in 88 National Collegiate Athletic Association (NCAA) Division III (DIII) football players, players consumed an excessive amount of saturated fat with dietary cholesterol intake three times greater than the recommended amount. Over 80% of football players consumed dairy products daily. Additionally, consumption of cardioprotective foods such as plant-based carbohydrates, fiber, and unsaturated fats was quite low.13

An athlete's biological age is also important for determining the appropriate composition of macronutrients needed to support performance goals within the confines of growth and changes in body composition with aging. For instance, adolescent athletes require energy deposition in growing tissues and energy expenditure for tissue synthesis. Protein intake must remain adequate to avoid its use as an energy substrate. Carbohydrate intake must also be sufficient to accommodate the wide variability in competition intensity, frequency, and format and to fuel athletes who participate in multiple different sports of varying intensities.14 Upon reaching age 20-30 years, muscle mass and strength peaks and then begins to decline at 40-50 years. As a result, the dietary needs for optimal athletic performance in masters athletes is quite different from that of adolescents and is influenced by gender. Male masters athletes require greater total protein intake (1.6-1.8 g/kg daily) to maintain strength and power while women require 25% less intake due to a decrease in amino acid oxidation that is mediated by estrogen. As females exit menopause, protein intake requirements become similar to male counterparts. Carbohydrate supplementation of greater than 8.0 g/kg daily is also beneficial to masters athletes, particularly in female masters endurance athletes where carbohydrate intake appears to be reduced and can contribute to the development of syndromes associated with low energy availability (e.g. Relative Energy Deficiency in Sports, RED-S) that inevitably lead to poor athletic performance and increased risk of physical and multisystem injury.14

A significant number of animal and human studies use saturated fats as the predominant fat source when examining effects of the ketogenic diet. The primary storage units for body fat include intramuscular triglyceride, blood lipids, and adipose tissue.10,11 There is a general consensus that diets high in saturated fat contribute to increases in LDL-C concentration and overall cardiovascular mortality.15,16 Thus, a ketogenic diet dependent upon high saturated fat intake will likely contribute to dyslipidemia, a well-known cardiovascular risk factor and mediator for progressive atherosclerosis and cardiac events.11 In a meta-analysis of 13 studies investigating cardiovascular risk management and weight loss in a very low carbohydrate ketogenic diet (maximum of 50 grams of carbohydrates daily) versus a low-fat diet (less than 30% of daily energy from fat), individuals following a very low carbohydrate ketogenic diet over a 12-month period had significantly increased LDL-C and HDL-C levels.17 An additional meta-analysis comparing low-carbohydrate to low-fat diets revealed similar findings with increased LDL-C levels, despite weight loss, suggesting that ketogenic diets may not be beneficial to individuals with heightened cardiovascular risk.18 Fortunately, replacing saturated fat with polyunsaturated fat is associated with lower risk of cardiovascular disease. In an analysis of a summed cohort of 222,234 adults in the Health Professionals Follow-Up, Nurses' Health Study and the Nurses Health Study II, a 24% reduction in cardiovascular disease risk was seen by replacing 5% of energy intake from dairy fat with polyunsaturated fat.19 An additional meta-analysis investigating low- vs high-fat diets and effect on lipid profiles also revealed that lower saturated fat intake was associated with lower LDL-C levels.20

In addition to increased fat consumption, the proportion of protein for total energy intake is also increased. With a near-complete elimination of carbohydrates, pure protein sources are limited to animal sources or synthetic protein powder, as most plant proteins are compound macronutrients. The source of protein – whether animal or plant – dictates cardiovascular risk. In a prospective cohort study of 131,342 health care professionals, higher animal protein intake was associated with significantly higher cardiovascular disease mortality, whereas higher plant protein intake was associated with lower cardiovascular mortality. In a subgroup analysis comparing individuals with healthy lifestyle behaviors to those with unhealthy behaviors, there was greater association between animal protein consumption and increased cardiovascular risk with the unhealthy group.21

By markedly reducing carbohydrate intake in ketogenic diets, foods rich in complex carbohydrates such as fruits, vegetables, and legumes are virtually eliminated from consumption. Authors of a meta-analysis of eight prospective studies assessing legume consumption within the Mediterranean diet showed significant reduction in cardiovascular disease outcomes, including cardiovascular mortality, coronary artery disease, myocardial infarction, and stroke.22 Additional meta-analyses and randomized controlled trials demonstrated that legume consumption was inversely associated with coronary artery disease risk, improved glycemic control by reducing postprandial blood glucose, reduction in LDL-C, and reduction in systolic blood pressure.23,24

Whether we, as sports cardiologists, can extrapolate data collected in non-athletic populations to competitive athletes and highly recreational individuals, is debatable. However, the evidence demonstrating benefits and harm of specific sources of macronutrients appears to be quite generalizable. While a ketogenic diet may be favorable for maximizing fatty acid utilization in prolonged endurance sports, the incorporation of healthy, cardiovascular risk-reducing plant-based complex carbohydrates and plant protein is compromised for the sake of performance. The short-term effects of this dietary commitment may not lead to a measurable increase in cardiovascular risk. However, while there is a paucity of longitudinal investigations of the ketogenic diet and cardiovascular risk in athletes, I suspect that consuming a ketogenic diet as a long-term strategy to maximize athletic performance increases the risk of progressive atherogenesis and poor cardiovascular outcomes that would ultimately impede athletic performance. Should an athlete still aspire to incorporate a ketogenic diet to maximize athletic performance, I recommend using a shared-decision making model to generate a list of macronutrient sources that do not increase risk of cardiovascular disease (Figure 1).

Summary of Author Recommendations:

  • Sports cardiologists should regularly inquire about an athlete's nutritional preference to determine whether the diet type supports an athlete's energy demands without compromising systemic and cardiovascular health.
  • Age, gender, and sport-type influence an athlete's dietary needs.
  • The ketogenic diet is not a favorable choice in athletes who prefer to consume saturated fats and predominantly animal-based protein, as evidence suggests both of these forms of macronutrients are associated with increased risk of developing cardiovascular disease.
  • Athletes whose dietary intake predominantly consists of unsaturated fats and plant-based proteins may be able to follow a ketogenic diet to meet performance goals in endurance and weight-lifting events, provided that they understand the limitations this diet poses in high-intensity/anaerobic-metabolic states of exercise.
  • A shared-decision model is ideal when discussing diet types and macronutrient sources that will best support athletic performance and reduce cardiovascular disease risk.

Figure 1: Dietary sources of macronutrients in a ketogenic diet, "heart-healthy" diet, and combination ketogenic-cardiac diet (DI = daily intake).12

Macronutrient Ketogenic Diet
(Fat 75% DI, Protein 15% DI, Carb <5% DI)
"Heart Healthy" Diet Combination Ketogenic/Cardiac Diet
Fat Saturated Animal-based
Butter, ghee, lard
Egg yolk
Bone marrow
Cod liver oil
Chicken/duck/goose fat
Dairy products
Fish (e.g. salmon)

Plant-based
Coconut products
Animal-based
Lean, white meats
Controversial: egg yolks, dairy12
Fish (e.g. salmon)

Plant-based
Controversial: coconut products12
Animal-based
Fatty fish (e.g. salmon)
Controversial: dairy, eggs12

Plant-based
Controversial: Coconut products12
Unsaturated Oils (peanut, flaxseed, sunflower, canola, cottonseed, corn)
Nuts & Seeds
Avocado/Avocado oil
Olives/Olive oil
Olive oil
Avocado oil
Flaxseed oil
Nuts and seeds
Olive oil
Avocado oil
Flaxseed oil
Nuts and seeds
Protein Animal-based
Chicken, turkey, duck
Dark meats
Eggs
Fish
Gelatin
Organ meats
Pork
Shellfish
Whey protein
Dairy products

Plant-based
Soy
Nuts & Seeds, nut flour
Legumes
Beans
Lentils
Grains (whole wheat, quinoa)
Animal-based
Lean, white meats
Egg whites
Fish
Controversial: dairy

Plant-based
Soy
Nuts & Seeds, nut flour
Legumes
Beans
Lentils
Grains (whole wheat, quinoa)
Animal-based
Lean, white meats
Egg whites
Fish
Controversial: dairy12

Plant-based
Soy
Nuts & Seeds, nut flour
Legumes
Beans
Lentils
Grains (whole wheat, quinoa)
Carbohydrates Fruits
Limit fresh berries
Cranberries
Lemon, lime

Vegetables
Asparagus
Avocado
Greens, bok choy
Cabbage
Celery
Collards
Kohlrabi
Summer squash
Zucchini
Radishes

Limit: root vegetables (parsnips, leeks, pumpkin, potatoes, rutabaga)
Fruits and vegetables Fruits
Limit fresh berries
Cranberries
Lemon, lime

Vegetables
Asparagus
Avocado
Greens, bok choy
Cabbage
Celery
Collards
Kohlrabi
Summer squash
Zucchini
Radishes

Limit: root vegetables (parsnips, leeks, pumpkin, potatoes, rutabaga)

References

  1. Curry A. The Gladiator Diet. Archaeology 2008;61:28.
  2. Dunford M. Fundamentals of Sport and Exercise Nutrition. 1st ed. Human Kinetics Publishers; 2010:208.
  3. Durkalec-Michalski- K Nowaczyk PM, Siedzik K. Effect of a four-week ketogenic diet on exercise metabolism in CrossFit-trained athletes. J Int Soc Sports Nutr 2019;16:16.
  4. McSwiney FT, Wardrop B, Hyde PN, Lafountain RA, Volek JS, Doyle L. Keto-adaptation enhances exercise performance and body composition responses to training in endurance athletes. Metabolism 2018;81:25-34.
  5. Harvey KL, Holcomb LE, Kolwicz SC Jr. Ketogenic diets and exercise performance. Nutrients 2019;11:2296
  6. Rowlands DS,Hopkins WG. Effects of high-fat and high-carbohydrate diets on metabolism and performance in cycling. Metabolism 2002;51:678-90.
  7. Burke LM, Ross ML, Garvican-Lewis LA, et al. Low carbohydrate, high fat diet impairs exercise economy and negates the performance benefit from intensified training in elite race walkers. J Physiol 2017;595:2785-2807.
  8. Phinney, SD, Bistrian BR, Evans W, 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.
  9. 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.
  10. Burke LM. Re-examining high-fat diets for sports performance: did we call the 'nail in the coffin' too soon? Sports Med 2015;45:33-49.
  11. Kosinski C, Jornayvaz FR. Effects of ketogenic diets on cardiovascular risk factors: evidence from animal and human studies. Nutrients 2017;9:517.
  12. Greene DA, Varley BJ, Hartwig TB, Chapman P, Rigney M. A low-carbohydrate ketogenic diet reduces body mass without compromising performance in powerlifting and olympic weightlifting athletes. J Strength Cond Res 2018;32:3373-82.
  13. Abbey EL, Wright CJ, Kirkpatrick CM. Nutrition practices and knowledge among NCAA Division III football players. J Int Soc Sports Nutr 2017;14:13.
  14. Burke LM, Castell LM, Casa DJ, et al. International Association of Athletics Federations Consensus Statement 2019: nutrition for athletics. Int J Sport Nutr Exerc Metab 2019;29:73-84.
  15. Freeman AM, Morris PB, Aspry, et al. A clinician's guide for trending cardiovascular nutrition controversies: Part II. J Am Coll Cardiol 2018;72:553-68.
  16. Siri-Tarino PW, Sun Q, Hu FB, Krauss RM. Saturated fatty acids and risk of coronary heart disease: modulation by replacement nutrients. Curr Atheroscler Rep 2010;12:384-90.
  17. Bueno NB, de Melo IS, de Oliveira SL, da Rocha Ataide T. Very-low-carbohydrate ketogenic diet v. low-fat diet for long-term weight loss: a meta-analysis of randomised controlled trials. Br J Nutr 2013;110:1178-87.
  18. Mansoor N, Vinknes KJ, Velerod MD, Retterstol K. Effects of low-carbohydrate diets v. low-fat diets on body weight and cardiovascular risk factors: a meta-analysis of randomised controlled trials. Br J Nutr 2016;115:466-79.
  19. Chen M, Li Y, Sun Q, et al. Dairy fat and risk of cardiovascular disease in 3 cohorts of US adults. Am J Clin Nutr 2016;104:1209-17.
  20. 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.
  21. Song M, Fung TT, Hu FB, et al. Association of animal and plant protein intake with all-cause and cause-specific mortality. JAMA Intern Med 2016;176:1453-63.
  22. Grosso G, Marventano S, Yang J, et al. A comprehensive meta-analysis on evidence of Mediterranean diet and cardiovascular disease: are individual components equal? Crit Rev Food Sci Nutr 2017;57:3218-32.
  23. Viguiliouk E, Blanco Mejia S, Kendall CW, Sievenpiper JL. Can pulses play a role in improving cardiometabolic health? Evidence from systematic reviews and meta-analyses. Ann N Y Acad Sci 2017;1392:43-57.
  24. Jayalath VH, de Souza RJ, Sievenpiper JL, et al. Effect of dietary pulses on blood pressure: a systematic review and meta-analysis of controlled feeding trials. Am J Hypertens 2014;27:56-64.

Clinical Topics: Diabetes and Cardiometabolic Disease, Dyslipidemia, Prevention, Sports and Exercise Cardiology, Atherosclerotic Disease (CAD/PAD), Lipid Metabolism, Nonstatins, Diet

Keywords: Sports, Athletes, Athletic Performance, Diet, Carbohydrate-Restricted, Diet, Ketogenic Diet, Diet, High-Fat, Cholesterol, Dietary, Glycogen, Ketone Bodies, Coronary Artery Disease, Cardiovascular Diseases, Exercise Tolerance, Risk Factors, Body Composition, Energy Metabolism, Oxygen Consumption, Myocardial Infarction, Fatty Acids, Dietary Supplements, Dietary Proteins


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