Downloaded from bjsm.bmj.com on June 5, 2014 - Published by group.bmj.com
BJSM Online First, published on May 26, 2014 as 10.1136/bjsports-2014-093824
Editorial
Low-carbohydrate diets for athletes: what evidence? Timothy Noakes,1 Jeff S Volek,2 Stephen D Phinney3 Exercise scientists teach that since muscle glycogen utilisation occurs at high rates (during high-intensity exercise in carbohydrate-adapted athletes), all athletes must be advised to ingest large amounts of carbohydrate before and during exercise.1 2 But this does not seem entirely logical. Why, for example, should athletes involved in prolonged submaximal exercise—probably the most common form of exercise performed by most elite and recreational athletes in training and competition—need always to eat highcarbohydrate diets in which at least 40–60% of calories are derived from carbohydrates? Surely our abundant body fat stores could provide most if not all the energy necessary to fuel activities of a submaximal intensity? Might our ability to use fat as a fuel during most activities explain the opinion that ‘a conclusive endorsement of a high-carbohydrate diet (for improved athletic performance) based on the literature is difficult to make’.3
LONG-TERM HEALTH RISKS OF HIGH-CARBOHYDRATE DIETS What of the long-term health consequences of habitually eating a highcarbohydrate diet especially for that increasing number of recreational athletes who may be unaware that they are insulin resistant (IR)4–6 and for whom carbohydrates pose a major health hazard including the risk of developing type 2 diabetes mellitus? The recent finding that habitual marathon runners can have marked coronary artery disease,7–9 worse than that present in sedentary individuals, despite similar or lower coronary risk factors, invites sober reflection.10 Is it possible that there is a dietary component to this? Could a high-carbohydrate diet in marathon runners with IR induce an inflammatory state promoting coronary 1
Department of Human Biology, University of Cape Town and Sports Science Institute of South Africa, Newlands, South Africa; 2Department of Human Sciences, Ohio State University, Columbus, Ohio, USA; 3 School of Medicine (emeritus), University of California Davis, Davis, California, USA Correspondence to Professor Timothy Noakes, Department of Human Biology, University of Cape Town and Sports Science Institute of South Africa, Newlands, South Africa; [email protected]
atherosclerosis? And is the poor dental and overall health of many Olympic athletes11 the result of eating a highcarbohydrate diet and frequently ingesting sugary sports drinks? Perhaps the time has come to question the popular advice that all athletes must only ingest highcarbohydrate diets.
ASSESSING THE CURRENT STATE OF KNOWLEDGE What is the current state of knowledge of carbohydrate-restricted diets for athletes?12 We note that the survival of humans in the frozen Arctic eating diets that contain little or no carbohydrate shows that modern humans have no essential requirement for carbohydrate— indeed a human carbohydrate deficiency disease has yet to be described. Historic reports that human explorers in the Arctic and Antarctic could adapt to a carbohydrate-free diet inspired the first modern study of human exercise adaptations to a low-carbohydrate diet in 1983.13 That study found that humans can adapt to this diet without any impairment or improvement in submaximal exercise performance. We could trace just 10 other studies of the performance effects of lowcarbohydrate diets in humans published in the past 31 years. Of the total of 11 studies, 3 found that exercise performance improved with adoption of a lowcarbohydrate diet; another 4 showed equivocal results favouring the lowcarbohydrate diet but limited by small sample sizes; 2 found no beneficial effect and 2 reported an adverse outcome. However, none of the studies evaluated chronic (6–12 months) adaptations to the diet; only one involved very prolonged exercise (a 200 km cycling time trial); none compared the effects of dietary change in athletes with normal carbohydrate metabolism to those with known IR; and none was properly placebo-controlled (if that is indeed possible). Missing are studies addressing the effects of lowcarbohydrate diets on the ease of weight control in athletes, on their capacity to train and their ability to recover, on their immune function and injury risk, or on their hand-eye coordination or capacity to concentrate in sports like golf and cricket,
Noakes T, et al. Br JArticle Sports Medauthor Month 2014 0 No 0employer) Copyright (orVoltheir
to name but a few obvious research questions. Clearly there is still much to be done. However, studies of elite athletes chronically adapted to low-carbohydrate diets has uncovered one unexpected finding— their extraordinary ability to produce energy at very high rates purely from the oxidation of fat. Thus some highly adapted runners consuming less than 10% of energy from carbohydrate are able to oxidise fat at greater than 1.5 g/min during progressive intensity exercise and consistently sustain rates of fat oxidation exceeding 1.2 g/min during exercise at ∼65% VO2max,12 13 thereby providing 56 kJ/min during prolonged exercise.14 The remaining energy would comfortably be covered by the oxidation of blood lactate, ketone bodies and glucose derived from gluconeogenesis.14 Thus a fully fat-adapted athlete able to oxidise fat at 1.5 g/min would cover his or her energy cost during an Ironman Triathlon without needing to ingest exogenous fuels especially carbohydrate. This contrasts with the need of carbohydrate-adapted athletes to ingest 90–105 g/h during prolonged exercise if they wish to maintain their performance.1 2 Indeed this simple calculation identifies the key difference in the low and highcarbohydrate dietary approach for endurance athletes. Once they deplete their endogenous carbohydrate reserves, athletes chronically adapted to highcarbohydrate diets likely become entirely dependent on exogenous carbohydrate for their performance. In contrast, athletes adapted to a low-carbohydrate diet carry all the energy they need in their abundant fat reserves. And because they live and train with chronically low blood insulin concentrations, they have instantaneous access to those fat reserves at all times. Just as should occur in a metabolism crafted by our evolutionary history as predatory hunters.15 The recent study by Shimazu et al16 has established another unexpected potential benefit of the low-carbohydrate diet. They showed that chronic ketosis in mice downregulates the expression of the class-1 histone deacetylase (HDAC) enzymes. Reduced HDAC activity lowers oxidative stress. Nutritional ketosis is also associated with a reduced generation of reactive oxygen species by mitochondria.17 Together these ketosis-induced adaptations should reduce oxidative stress and might influence rates of recovery from demanding exercise, an advantage anecdotally reported by athletes chronically adapted to a low-carbohydrate diet.12
2014. Produced by BMJ Publishing Group Ltd under licence.
1
Downloaded from bjsm.bmj.com on June 5, 2014 - Published by group.bmj.com
Editorial All this evidence suggests that there should be more to dietary prescription for athletes than an exclusive highcarbohydrate diet. There is a proven need for research of low-carbohydrate diets in all sports, not just those involving endurance. Now is the time to determine whether the conclusion that ‘there is very little or no evidence to support the use of high-fat diets’ by athletes18 is an eternal truth. Competing interests None.
2
3
4
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6
Provenance and peer review Not commissioned; externally peer reviewed. To cite Noakes T, Volek JS, Phinney SD. Br J Sports Med Published Online First: [ please include Day Month Year] doi:10.1136/bjsports-2014-093824
7
Accepted 8 May 2014 Br J Sports Med 2014;0:1–2. doi:10.1136/bjsports-2014-093824
8
9
REFERENCES 1
2
Jeukendrup A. The new carbohydrate intake recommendations. Nestle Nutr Inst Workshop Ser 2013;75:63–71.
Burke LM, Hawley JA, Wong SH, et al. Carbohydrates for training and competition. J Sports Sci 2011;29(Suppl 1):S17–27. Erlenbusch M, Haub M, Munoz K, et al. Effect of high-fat or high-carbohydrate diets on endurance exercise: a meta-analysis. Int J Sport Nutr Exerc Metab 2005;15:1–14. Reaven GM. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes 1988;37:1595–607. Reaven G. Insulin resistance and coronary heart disease in nondiabetic individuals. Arterioscler Thromb Vasc Biol 2012;32:1754–9. Brukner P. Challenging beliefs in sports nutrition: are two ‘core principles’ proving to be myths ripe for busting? Br J Sports Med 2013;47: 663–4. Schwartz RS, Kraus SM, Schwartz JG, et al. Study finds that long-term participation in marathon training/racing is paradoxically associated with increased coronary plaque volume. Missouri Med 2014; March/April. Mohlenkamp S, Bose D, Mahabadi AA, et al. On the paradox of exercise: coronary atherosclerosis in an apparently healthy marathon runner. Nat Clin Pract Cardiovasc Med 2007;4:396–401. Mohlenkamp S, Leineweber K, Lehmann N, et al. Coronary atherosclerosis burden, but not transient troponin elevation, predicts long-term outcome in recreational marathon runners. Basic Res Cardiol 2014;109:391.
10 11
12 13
14 15
16
17
18
Noakes T. Time to quit that marathon running? Not quite yet! Basic Res Cardiol 2014;109:395. Needleman I, Ashley P, Petrie A, et al. Oral health and impact on performance of athletes participating in the London 2012 Olympic Games: a cross-sectional study. Br J Sports Med 2013;47:1054–8. Volek JS, Noakes TD, Phinney SD. Rethinking fat as a performance fuel. Eur J Sport Sci (in press) 2014. Phinney SD, Bistrian BR, Evans WJ, et al. The human metabolic response to chronic ketosis without caloric restriction: preservation of submaximal exercise capability with reduced carbohydrate oxidation. Metabolism 1983;32:769–76. Noakes TD. Lore of running. 4th edn. Champaign, IL: Human Kinetics Publishers, 2003. Lieberman DE, Bramble DM. The evolution of marathon running: capabilities in humans. Sports Med 2007;37:288–90. Shimazu T, Hirschey MD, Newman J, et al. Suppression of oxidative stress by beta-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 2013;339:211–14. Sato K, Kashiwaya Y, Keon CA, et al. Insulin, ketone bodies, and mitochondrial energy transduction. FASEB J 1995;9:651–8. Jeukendrup AE. High-carbohydrate versus high-fat diets in endurance sports. Sports Med Sports Traumatol 2003;51:17–23.
Noakes T, et al. Br J Sports Med Month 2014 Vol 0 No 0
Downloaded from bjsm.bmj.com on June 5, 2014 - Published by group.bmj.com
Low-carbohydrate diets for athletes: what evidence? Timothy Noakes, Jeff S Volek and Stephen D Phinney Br J Sports Med published online May 26, 2014
doi: 10.1136/bjsports-2014-093824
Updated information and services can be found at: http://bjsm.bmj.com/content/early/2014/05/26/bjsports-2014-093824.full.html
These include:
References
This article cites 15 articles, 6 of which can be accessed free at: http://bjsm.bmj.com/content/early/2014/05/26/bjsports-2014-093824.full.html#ref-list-1
P
BJSM Online First, published on May 26, 2014 as 10.1136/bjsports-2014-093824
Editorial
Low-carbohydrate diets for athletes: what evidence? Timothy Noakes,1 Jeff S Volek,2 Stephen D Phinney3 Exercise scientists teach that since muscle glycogen utilisation occurs at high rates (during high-intensity exercise in carbohydrate-adapted athletes), all athletes must be advised to ingest large amounts of carbohydrate before and during exercise.1 2 But this does not seem entirely logical. Why, for example, should athletes involved in prolonged submaximal exercise—probably the most common form of exercise performed by most elite and recreational athletes in training and competition—need always to eat highcarbohydrate diets in which at least 40–60% of calories are derived from carbohydrates? Surely our abundant body fat stores could provide most if not all the energy necessary to fuel activities of a submaximal intensity? Might our ability to use fat as a fuel during most activities explain the opinion that ‘a conclusive endorsement of a high-carbohydrate diet (for improved athletic performance) based on the literature is difficult to make’.3
LONG-TERM HEALTH RISKS OF HIGH-CARBOHYDRATE DIETS What of the long-term health consequences of habitually eating a highcarbohydrate diet especially for that increasing number of recreational athletes who may be unaware that they are insulin resistant (IR)4–6 and for whom carbohydrates pose a major health hazard including the risk of developing type 2 diabetes mellitus? The recent finding that habitual marathon runners can have marked coronary artery disease,7–9 worse than that present in sedentary individuals, despite similar or lower coronary risk factors, invites sober reflection.10 Is it possible that there is a dietary component to this? Could a high-carbohydrate diet in marathon runners with IR induce an inflammatory state promoting coronary 1
Department of Human Biology, University of Cape Town and Sports Science Institute of South Africa, Newlands, South Africa; 2Department of Human Sciences, Ohio State University, Columbus, Ohio, USA; 3 School of Medicine (emeritus), University of California Davis, Davis, California, USA Correspondence to Professor Timothy Noakes, Department of Human Biology, University of Cape Town and Sports Science Institute of South Africa, Newlands, South Africa; [email protected]
atherosclerosis? And is the poor dental and overall health of many Olympic athletes11 the result of eating a highcarbohydrate diet and frequently ingesting sugary sports drinks? Perhaps the time has come to question the popular advice that all athletes must only ingest highcarbohydrate diets.
ASSESSING THE CURRENT STATE OF KNOWLEDGE What is the current state of knowledge of carbohydrate-restricted diets for athletes?12 We note that the survival of humans in the frozen Arctic eating diets that contain little or no carbohydrate shows that modern humans have no essential requirement for carbohydrate— indeed a human carbohydrate deficiency disease has yet to be described. Historic reports that human explorers in the Arctic and Antarctic could adapt to a carbohydrate-free diet inspired the first modern study of human exercise adaptations to a low-carbohydrate diet in 1983.13 That study found that humans can adapt to this diet without any impairment or improvement in submaximal exercise performance. We could trace just 10 other studies of the performance effects of lowcarbohydrate diets in humans published in the past 31 years. Of the total of 11 studies, 3 found that exercise performance improved with adoption of a lowcarbohydrate diet; another 4 showed equivocal results favouring the lowcarbohydrate diet but limited by small sample sizes; 2 found no beneficial effect and 2 reported an adverse outcome. However, none of the studies evaluated chronic (6–12 months) adaptations to the diet; only one involved very prolonged exercise (a 200 km cycling time trial); none compared the effects of dietary change in athletes with normal carbohydrate metabolism to those with known IR; and none was properly placebo-controlled (if that is indeed possible). Missing are studies addressing the effects of lowcarbohydrate diets on the ease of weight control in athletes, on their capacity to train and their ability to recover, on their immune function and injury risk, or on their hand-eye coordination or capacity to concentrate in sports like golf and cricket,
Noakes T, et al. Br JArticle Sports Medauthor Month 2014 0 No 0employer) Copyright (orVoltheir
to name but a few obvious research questions. Clearly there is still much to be done. However, studies of elite athletes chronically adapted to low-carbohydrate diets has uncovered one unexpected finding— their extraordinary ability to produce energy at very high rates purely from the oxidation of fat. Thus some highly adapted runners consuming less than 10% of energy from carbohydrate are able to oxidise fat at greater than 1.5 g/min during progressive intensity exercise and consistently sustain rates of fat oxidation exceeding 1.2 g/min during exercise at ∼65% VO2max,12 13 thereby providing 56 kJ/min during prolonged exercise.14 The remaining energy would comfortably be covered by the oxidation of blood lactate, ketone bodies and glucose derived from gluconeogenesis.14 Thus a fully fat-adapted athlete able to oxidise fat at 1.5 g/min would cover his or her energy cost during an Ironman Triathlon without needing to ingest exogenous fuels especially carbohydrate. This contrasts with the need of carbohydrate-adapted athletes to ingest 90–105 g/h during prolonged exercise if they wish to maintain their performance.1 2 Indeed this simple calculation identifies the key difference in the low and highcarbohydrate dietary approach for endurance athletes. Once they deplete their endogenous carbohydrate reserves, athletes chronically adapted to highcarbohydrate diets likely become entirely dependent on exogenous carbohydrate for their performance. In contrast, athletes adapted to a low-carbohydrate diet carry all the energy they need in their abundant fat reserves. And because they live and train with chronically low blood insulin concentrations, they have instantaneous access to those fat reserves at all times. Just as should occur in a metabolism crafted by our evolutionary history as predatory hunters.15 The recent study by Shimazu et al16 has established another unexpected potential benefit of the low-carbohydrate diet. They showed that chronic ketosis in mice downregulates the expression of the class-1 histone deacetylase (HDAC) enzymes. Reduced HDAC activity lowers oxidative stress. Nutritional ketosis is also associated with a reduced generation of reactive oxygen species by mitochondria.17 Together these ketosis-induced adaptations should reduce oxidative stress and might influence rates of recovery from demanding exercise, an advantage anecdotally reported by athletes chronically adapted to a low-carbohydrate diet.12
2014. Produced by BMJ Publishing Group Ltd under licence.
1
Downloaded from bjsm.bmj.com on June 5, 2014 - Published by group.bmj.com
Editorial All this evidence suggests that there should be more to dietary prescription for athletes than an exclusive highcarbohydrate diet. There is a proven need for research of low-carbohydrate diets in all sports, not just those involving endurance. Now is the time to determine whether the conclusion that ‘there is very little or no evidence to support the use of high-fat diets’ by athletes18 is an eternal truth. Competing interests None.
2
3
4
5
6
Provenance and peer review Not commissioned; externally peer reviewed. To cite Noakes T, Volek JS, Phinney SD. Br J Sports Med Published Online First: [ please include Day Month Year] doi:10.1136/bjsports-2014-093824
7
Accepted 8 May 2014 Br J Sports Med 2014;0:1–2. doi:10.1136/bjsports-2014-093824
8
9
REFERENCES 1
2
Jeukendrup A. The new carbohydrate intake recommendations. Nestle Nutr Inst Workshop Ser 2013;75:63–71.
Burke LM, Hawley JA, Wong SH, et al. Carbohydrates for training and competition. J Sports Sci 2011;29(Suppl 1):S17–27. Erlenbusch M, Haub M, Munoz K, et al. Effect of high-fat or high-carbohydrate diets on endurance exercise: a meta-analysis. Int J Sport Nutr Exerc Metab 2005;15:1–14. Reaven GM. Banting lecture 1988. Role of insulin resistance in human disease. Diabetes 1988;37:1595–607. Reaven G. Insulin resistance and coronary heart disease in nondiabetic individuals. Arterioscler Thromb Vasc Biol 2012;32:1754–9. Brukner P. Challenging beliefs in sports nutrition: are two ‘core principles’ proving to be myths ripe for busting? Br J Sports Med 2013;47: 663–4. Schwartz RS, Kraus SM, Schwartz JG, et al. Study finds that long-term participation in marathon training/racing is paradoxically associated with increased coronary plaque volume. Missouri Med 2014; March/April. Mohlenkamp S, Bose D, Mahabadi AA, et al. On the paradox of exercise: coronary atherosclerosis in an apparently healthy marathon runner. Nat Clin Pract Cardiovasc Med 2007;4:396–401. Mohlenkamp S, Leineweber K, Lehmann N, et al. Coronary atherosclerosis burden, but not transient troponin elevation, predicts long-term outcome in recreational marathon runners. Basic Res Cardiol 2014;109:391.
10 11
12 13
14 15
16
17
18
Noakes T. Time to quit that marathon running? Not quite yet! Basic Res Cardiol 2014;109:395. Needleman I, Ashley P, Petrie A, et al. Oral health and impact on performance of athletes participating in the London 2012 Olympic Games: a cross-sectional study. Br J Sports Med 2013;47:1054–8. Volek JS, Noakes TD, Phinney SD. Rethinking fat as a performance fuel. Eur J Sport Sci (in press) 2014. Phinney SD, Bistrian BR, Evans WJ, et al. The human metabolic response to chronic ketosis without caloric restriction: preservation of submaximal exercise capability with reduced carbohydrate oxidation. Metabolism 1983;32:769–76. Noakes TD. Lore of running. 4th edn. Champaign, IL: Human Kinetics Publishers, 2003. Lieberman DE, Bramble DM. The evolution of marathon running: capabilities in humans. Sports Med 2007;37:288–90. Shimazu T, Hirschey MD, Newman J, et al. Suppression of oxidative stress by beta-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 2013;339:211–14. Sato K, Kashiwaya Y, Keon CA, et al. Insulin, ketone bodies, and mitochondrial energy transduction. FASEB J 1995;9:651–8. Jeukendrup AE. High-carbohydrate versus high-fat diets in endurance sports. Sports Med Sports Traumatol 2003;51:17–23.
Noakes T, et al. Br J Sports Med Month 2014 Vol 0 No 0
Downloaded from bjsm.bmj.com on June 5, 2014 - Published by group.bmj.com
Low-carbohydrate diets for athletes: what evidence? Timothy Noakes, Jeff S Volek and Stephen D Phinney Br J Sports Med published online May 26, 2014
doi: 10.1136/bjsports-2014-093824
Updated information and services can be found at: http://bjsm.bmj.com/content/early/2014/05/26/bjsports-2014-093824.full.html
These include:
References
This article cites 15 articles, 6 of which can be accessed free at: http://bjsm.bmj.com/content/early/2014/05/26/bjsports-2014-093824.full.html#ref-list-1
P
