A ketogenic diet (KD) traditionally comprises high fat, moderate/low protein, and very low carbohydrate (CHO) intake and aims to induce a state of nutritional ketosis (2). Under normal physiological conditions, cells acquire energy from glucose in a process called glycolysis. When CHO intake is severely limited, glycogen (the body's stored form of glucose) stores in the liver (8) and skeletal muscle stores (12) diminish. The body often responds by shifting a portion of its fuel source burden toward dietary fats and adipose tissue, the byproduct of which is ketone bodies. Thus, “ketosis” is a metabolic state in which the body generates energy from these ketone bodies (rather than glucose) at a rate capable of fueling the brain and body (blood concentrations are typically ∼≥0.5–3.0 mg/dL) (5).
Unfortunately, ketosis is frequently confused with “ketoacidosis,” a pathological metabolic state characterized by extreme and uncontrolled ketosis resulting in severe accumulation of keto acids and a subsequent decrease in blood pH. Amino acid deamination (breakdown) also contributes to the production of ketone bodies. Thus, ketoacidosis is most likely to occur in individuals either (a) with type 1 diabetes mellitus or (b) participating in a high fat, high protein, and very low CHO diet for extended periods (i.e., >months). The scientific evidence is difficult to interpret, as this critical detail (i.e., traditional KD vs high fat and low CHO, but also high protein) is often unaccounted for, unreported, or uncontrolled. That understood, this column will provide a brief summary of the reported physical benefits of very low CHO (≤50 g CHO per day), high fat, but not hypocaloric diets; typically called “KD.”
Studies dating back to the 1980's provide evidence of enhanced aerobic performance while on KD (12,13). Zajac et al. (20) observed significant improvements in cycling maximal oxygen uptake (V̇o2max) and lactate threshold. Rhyu and Cho (15) found a significant reduction in the time required to finish a 2,000 m sprint cycle. Multiple studies have shown significant reductions in respiratory exchange ratio (RER) (12,13,20), glucose utilization (12,13), resting blood lactate levels (13,20), and/or aerobic fatigue (13,15). Volek et al. (17) demonstrated similar results in a more recent study comparing KD with a normal CHO diet in elite ultramarathoners and ironman triathletes. When compared with their traditional CHO intake counterparts, elite athletes consuming a 10% CHO diet showed an ∼2-fold increase in peak fat oxidation, as well as a 59% increase in mean fat oxidation during submaximal exercise. Enhanced fat oxidation produces a lower RER. A significant association exists between RER and physical fitness variables (e.g., V̇o2max, lactate threshold, and maximum heart rate), with trained individuals having a lower RER than untrained individuals (14).
Although the beneficial effects of a KD on aerobic performance are fairly well established, recent evidence also indicates a possible benefit for weight-class sport athletes. In such sports, the ability to effectively reduce body weight could provide significant advantages. The weight restriction methods typically practiced by these athletes (e.g., caloric restriction, excessive training, dehydration, self-induced vomiting, diuretics, etc.) can be dangerous and detrimental to performance (15). Mental fatigue, confusion, and reduced vigor are symptoms often experienced by athletes undertaking rapid weight loss practices (4). However, gradual weight loss practices have been shown to attenuate some side effects such as the loss of muscular power (4). If cutting weight is required, research indicates combining gradual weight reduction methods with KD may yield greater benefits than gradual weight reduction methods alone. Substantial reductions in CHO intake significantly diminish liver (8) and skeletal muscle glycogen stores (13,19). One gram of glycogen stores ∼3 grams of water, reduction of glycogen can result in notable weight loss due to decreases in total body water content (10). In addition, a lack of CHO lowers resting blood insulin levels (13,20) which in turn induces a natriuretic effect (excretion of sodium), further reducing total body water content (1,16). Thus, weight-class sports that rely mostly on the adenosine triphosphate (ATP)-PC systems (e.g., baseball, weightlifting, powerlifting, gymnastics, etc.) may benefit from KD as part of a gradual weight reduction strategy.
Multiple short-term studies (<10 weeks) support this hypothesis and report significant reductions in body mass (3,10,20), in particular body fat (3,10,20), with concomitant maintenance of lean body mass (10,15) in KD compared with higher CHO diets. One study of elite male gymnasts found similar body composition changes with no adverse effects on muscular power or strength (11). A recent short-term (10-week) training study reported no difference in resistance-training–induced strength gains or muscle thickness (hypertrophy) between a KD and a standard diet (when equated for total calories) (6). KD may also be an attractive option for athletes in these sports who have difficulty adhering to the caloric consumption requirements needed to maintaining a specific body weight. Westman et al. (19) noted a spontaneous reduction in food intake as well as perceived hunger in participants on a KD. Likewise, the high protein intakes that occasionally accompany a KD are both satiating and thermogenically advantageous in comparison with low protein intakes (7,18). This seems to coincide with normal blood (10,13), liver (13), and kidney (10,13) function. It is important to emphasize the potential need for higher protein intake while on a KD for athletes due to the increased demands of gluconeogenesis (9). For example, the aforementioned elite male gymnasts consumed 2.8 g/kg body weight of protein per day. Subjects in a similar study consumed 1.2 g/kg body weight of protein per day when consuming a CHO-free diet (13).
The differentiation between KD with low protein (traditional KD) or high protein (as suggested above) needs scientific vetting. Several of the available KD studies also failed to measure or report ketone body concentrations, making the results difficult to interpret as the achievement of a “ketogenic state” was only speculative. Countless questions in areas such as high-intensity intervals, recovery, hypertrophy, sex, aging, and motor control also remain unanswered. Nonetheless, the current evidence supports the use of KD in some specific situations. Implementation of KD in athletes shows clear promise in long duration endurance performance, as well as for short-term implementation in weight class, highly anaerobic sports (if combined with high protein intake). However, we strongly encourage consultation with coaching staff, a registered dietitian, and a medical professional before implementing.
A KD typically contains high fat (∼≥80% of total caloric intake), moderate to low protein (by athlete standards) of 10–15%, and ≤5–10% CHO (7,9,13,16). Often athletes must restrict CHO intake to ∼<50 g/d (roughly equivalent to 2 bananas) to produce ketone bodies at a rate sufficient to be considered in a state of nutritional ketosis (ketone levels >0.5 mmol/L) (16). KDs have been shown to increase the amount of fat the body can use for cellular energy (15). Moreover, they increase production of various “ketone bodies,” that can also be oxidized by various tissues for fuel. The main ketone bodies are acetoacetate (AcAc), beta-hydroxybutyrate (BHB), and acetone (14). Combustion (break down) of BHB through heat liberates 487.2 kcal/mol, whereas palmitate (fat) yields 2,384.8 kcal/mol and glucose 669.9 kcal/mol (13). Moreover, 100 g of glucose, BHB, and acetoacetate generate 8.7 kg, 10.5 kg, 9.4 kg of ATP (the molecule all cells use for energy), respectively (5). However, this does not take into account the cellular kinetics (i.e., how fast this energy can be used by the body during exercise). Glucose is well known to be a faster fuel source than free fatty acids. A 2013 study used rodents to show that ketosis induces a moderate uncoupling state and less oxidative efficiency compared with glucose oxidation (10). This means that while an upregulation of fat metabolism and ketones may enhance long duration, steady-state aerobic endurance performance (17), it may negatively affect activities, such as strength and power sports, that rely on CHO metabolism, glycolysis, and the ATP-PC cycle (8,9). Unfortunately, few studies exist in this area.
In the classic KD study by Phinney et al. (8), 5 elite cyclists exposed to chronic KD (without caloric restriction) were tested while exercising at ∼60–65% of their V̇o2max. Although there was a change in the respiratory quotient (similar to RER) that demonstrated a greater use of fat/ketones, there was no mean change in endurance performance. A postexercise muscle biopsy revealed slow-twitch fiber (not fast-twitch) glycogen depletion, indicating the fast-twitch fibers were not recruited or used to power the exercise. The authors acknowledged a “throttling of function near V̇o2max, apparently by limitation of CHO utilization,” suggesting a restriction in the ability to perform anaerobic work. In fact, examination of the data suggests performance after CHO repletion was highly individualized; 2 riders got better, 1 neutral (within 3 minutes difference), and 2 actually got worse.
Well-rounded athletes should possess the ability to use all fuel substrates effectively for the following reasons (4). As the duration of exercise increases from very short (e.g., high-jump, weightlifting, powerlifting, etc.) to very long (i.e., ultraendurance events), the fuel mix changes from ATP-CP, to primarily CHO, to mostly fat. However, even strength and power athletes switch back to primarily fat-based aerobic metabolism during rest period between sets or training sessions. This switching of fuels from one substrate to the next and back is referred to as metabolic flexibility (4) and may be compromised when engaged in a KD. One approach to maintain metabolic flexibility could include the “periodization” of macronutrients based on the given training phase. For example, an athlete might use a KD for several weeks during the off-season, and then switch back to normal CHO consumption before competition. Literature indeed exists on this “train low, compete high” CHO approach (1). However, CHO use decreases when athletes use KD, most likely through a change in pyruvate dehydrogenase enzyme concentration (11,12). Phinney et al. (8) also reported a 4-week KD decreased resting muscle glycogen in elite cyclists by 50%, which resulted in a 4-fold drop in the rate of glycogen use during exercise.
However, a more recent study (2016) by Volek et al. (15) did not find that KD compromised muscle glycogen. These scientists had 20 elite ultramarathoners and ironman distance triathletes complete a 180-minute submaximal run at 64% V̇o2max. Half of the runners habitually consumed a high CHO diet (% CHO: Protein: Fat = 59:14:25), and the others a KD (% CHO: Protein: Fat = 10:19:70) diet for an average of 20 months prior. Peak fat oxidation in KD was 2-fold higher (also meaning CHO oxidation was significantly lower), and the rates of fat oxidation were the highest ever reported in the literature. Although ketone bodies may serve as a substitute for CHO, they may also paradoxically reduce endogenous CHO availability through inhibition of hepatic glucose output, therefore lowering the capacity to sustain higher intensity efforts (6,9). These findings emphasized the point that although glycogen levels in muscle and the liver may or may not be compromised with long-term KD, the athlete will likely lack the metabolic machinery needed to fully use them as fuel sources. It also suggests that while long-term KD may allow time for adaptation, short-term (i.e., 4 weeks) CHO restriction may compromise muscle glycogen stores.
In one of the few studies on strength athletes, Paoli and colleagues (7) investigated body composition and performance (hanging straight leg raise, ground push up, parallel bar dips, pull up, squat jump, countermovement jump, and 30 seconds continuous jumps) changes in 8 elite artistic gymnasts after 30 days of a modified KD (22 gram CHO/d: 54.8% fat, 40.7% protein, and 4.5% CHO). This was compared with a western diet group of 38.5% fat, 14.7% protein, and 46.8% CHO. Although the study findings (no difference in strength gains) seem to support KD, a major limitation was that like many others in the KD literature, it failed to measure blood ketone levels. This omission makes it impossible to determine whether the KD group was actually in nutritional ketosis, ketoacidosis, or otherwise. This is particularly concerning as participants in the KD group consumed 200.8 grams protein/d compared with only 83.5 grams/d in the western diet group. The fact that few KD studies verify blood ketone concentrations makes it difficult to identify whether or not a reported diet should truly be labeled as a “KD”. Moreover, no scientific consensus exists on the acceptable range of macronutrient composition for a diet to be considered KD. The validity, effectiveness, and efficacy of KD are therefore extremely difficult to determine at the current time.
Several other limitations exist. First, long-term studies examining performance and athlete health are lacking, especially when a KD and high protein are combined. Second, a KD may yield neutral, or even deleterious, effects on individuals participating in activities in the middle of the bioenergetic spectrum (i.e., >∼15 seconds, but < multiple hours of steady-state work). This may or may not also be true for weight class, but glycolytic endurance sports (e.g., wrestling, basketball, soccer, etc.), even when combined with high protein. Third, limited information exists on KD with young, old, and female athletes, or those aiming to maximize muscle hypertrophy.
In summary, although slight advantages for ultraendurance athletes may exist, more work is needed in that area before recommendations can be provided. This should not discourage experimentation with KD by practitioners and researchers as it has contributed a great amount to our understanding of metabolism, nutrition, health, and performance. For example, future work could investigate the use of exogenous ketone salts and esters combined with and without CHO as this may elevate blood ketones while maintaining appropriate CHO stores and enzymatic function, which may improve high-intensity exercise performance (2). The time needed to adapt (achieve a state of nutritional KD) remains in question, with most anecdotal reports indicating ∼2–3 weeks. Concerns also exist with the feasibility, logistics, practicality, and adherence of KD. Therefore, based on the available evidence and our current understanding of bioenergetics, the use of KD is generally not advised for strength and power or any athlete relying heavily on anaerobic or glycolytic metabolism. However, a few unique exceptions may exist. Individuals should consult a medical professional before attempting a KD as numerous risks may exist (3).
1. Burke LM. Fueling strategies to optimize performance: Training high or training low? Scand J Med Sci Sports 2(20 Suppl): 48–58, 2010.
2. Cox PJ, Kirk T, Ashmore T, Willerton K, Evans R, Smith A, Murray AJ, Stubbs B, West J, McLure SW, King MT, Dodd MS, Holloway C, Neubauer S, Drawer S, Veech RL, Griffin JL, Clarke K. Nutritional ketosis alters fuel preference and thereby endurance performance in athletes. Cell Metab 24: 256–268, 2016.
3. Kanikarla-Marie P, Jain SK. Hyperketonemia and ketosis increase the risk of complications in type 1 diabetes. Free Radic Biol Med 95: 268–277, 2016.
4. Kelley DE. Skeletal muscle fat oxidation: Timing and flexibility are everything. J Clin Invest 115: 1699–1702, 2005.
5. Manninen AH. Metabolic effects of the very-low-carbohydrate diets: Misunderstood “villains” of human metabolism. J Int Soc Sports Nutr 1: 7–11, 2004.
6. Owen OE, Reichard GA Jr, Markus H, Boden G, Mozzoli MA, Shuman CR. Rapid intravenous sodium acetoacetate infusion in man. Metabolic and kinetic responses. J Clin Invest 52: 2606–2616, 1973.
7. Paoli A, Grimaldi K, D'Agostino D, Cenci L, Moro T, Bianco A, Palma A. Ketogenic diet does not affect strength performance in elite artistic gymnasts. J Int Soc Sports Nutr 9: 34, 2012.
8. 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 32: 769–776, 1983.
9. Pinckaers PJ, Churchward-Venne TA, Bailey D, van Loon LJ. Ketone bodies and exercise performance: The next magic bullet or merely hype? Sports Med 2016. Jul 18. [Epub Ahead of print].
10. Prince A, Zhang Y, Croniger C, Puchowicz M. Oxidative metabolism: Glucose versus ketones. Adv Exp Med Biol 789: 323–328, 2013.
11. Spriet LL. New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med 1(44 Suppl): S87–S96, 2014.
12. Stellingwerff T, Spriet LL, Watt MJ, Kimber NE, Hargreaves M, Hawley JA, Burke LM. Decreased PDH activation and glycogenolysis during exercise following fat adaptation with carbohydrate restoration. Am J Physiol Endocrinol Metab 290: E380–E388, 2006.
13. Veech RL. The therapeutic implications of ketone bodies: The effects of ketone bodies in pathological conditions: Ketosis, ketogenic diet, redox states, insulin resistance, and mitochondrial metabolism. Prostaglandins Leukot Essent Fatty Acids 70: 309–319, 2004.
14. Veech RL, Chance B, Kashiwaya Y, Lardy HA, Cahill GF Jr. Ketone bodies, potential therapeutic uses. IUBMB Life 51: 241–247, 2001.
15. Volek JS, Freidenreich DJ, Saenz C, Kunces LJ, Creighton BC, Bartley JM, Davitt PM, Munoz CX, Anderson JM, Maresh CM, Lee EC, Schuenke MD, Aerni G, Kraemer WJ, Phinney SD. Metabolic characteristics of keto-adapted ultra-endurance runners. Metabolism 65: 100–110, 2016.
16. Volek JS, Noakes T, Phinney SD. Rethinking fat as a fuel for endurance exercise. Eur J Sport Sci 15: 13–20, 2015.
17. 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 6: 2493–2508, 2014.