Dietary Fat and Sports Performance

Dietary Fat and Sports Performance

C H A P T E R 47 Dietary Fat and Sports Performance Michael Puglisi Nutritional Sciences, University of Connecticut, Storrs, CT, United States INTRO...

437KB Sizes 0 Downloads 1 Views


47 Dietary Fat and Sports Performance Michael Puglisi Nutritional Sciences, University of Connecticut, Storrs, CT, United States

INTRODUCTION Dietary fat is an important part of an athlete’s diet, providing essential fatty acids and enhancing absorption of fat-soluble vitamins. Dietary fat is also crucial for ensuring adequate caloric intake to meet the elevation in expenditure which occurs with physical activity. Triacylglycerol is the main component of dietary fat, consisting of a glycerol molecule esterified to three fatty acid molecules. Dietary fats are distinguished by the degree of saturation, with saturated fatty acids containing no double bonds, monounsaturated fatty acids containing a single double bond, and polyunsaturated fatty acids consisting of two or more double bonds. The 2015–20 Dietary Guidelines for Americans no longer focuses on a limit for total fat intake but still recommends limiting saturated fat to 10% of calories or less to prevent elevation of low-density lipoprotein (LDL) cholesterol [1]. The Academy of Nutrition and Dietetics and the American College of Sports Medicine recommend that dietary fat provide 20%–35% of total calories, which is the current acceptable macronutrient distribution range [2]. This recommendation is grounded on the finding that fat intake above 35% of calories usually coincides with saturated fat consumption in excess of recommended amounts, and diets too low in fat and high in carbohydrate result in lower high-density lipoprotein (HDL) cholesterol concentrations, interfering with the antiatherogenic effects of reverse cholesterol transport. The focus on fatty acid type has resulted in promotion of greater intake of omega-3 polyunsaturated fatty acids and reduced intake of saturated fatty acids and trans fats, unsaturated fats that have been made solid by the addition of hydrogen bonds.

FATTY ACIDS AND HEALTH It is clear that increasing dietary intake of saturated fatty acids results in greater LDL cholesterol, although individual saturated fatty acids have varied effects: 12 carbon, 14 carbon, and 16 carbon saturated fatty acids raise LDL cholesterol, whereas stearic acid (18 carbons) does not alter LDL cholesterol [3,4]. Despite elevating LDL cholesterol, the link to health is less established for saturated fatty acids. Various research groups have reported that substituting carbohydrates with saturated fatty acids has failed to increase cardiovascular disease risk [5–8]. Replacing 5% of calories as saturated fat with polyunsaturated fat has resulted in reduction in cardiovascular disease risk by approximately 10%, and the effects of replacing saturated fat with monounsaturated fat are less clear [9]. Replacing saturated fat with polyunsaturated fat and monounsaturated fat will lower LDL cholesterol, although the effect appears to be larger for polyunsaturated fat [10]. A metaanalysis completed by Schwingshackl and Hoffmann [11] indicates a reduced incidence of cardiovascular events by 9% and cardiovascular mortality by 12% for people in the highest third of monounsaturated fat intake compared with the bottom third but found that only olive oil was associated with lower risk. More research needs to be carried out to determine the specific effects of monounsaturated fats on health. Polyunsaturated fatty acids have been widely touted for their health benefits, especially the omega-3 fatty acids found in fish and fish oil, eicosapentaenoic acid (EPA), and docosahexaenoic acid (DHA). Intake of 250 mg or greater of EPA and DHA from fish or fish oil was associated with a 36% reduction in the risk of cardiovascular mortality in

Nutrition and Enhanced Sports Performance, Second Edition


© 2019 Elsevier Inc. All rights reserved.



a pooled analysis of prospective cohort trials and randomized clinical trials [12]. This may be associated with the triglyceride- and blood pressure–lowering effects [13–15], as well as the antiinflammatory effects of omega-3 fatty acids, which may reduce not only risk of atherosclerosis [16] but also several other disease conditions associated with inflammation [17]. Data support a beneficial effect in rheumatoid arthritis, but more research is required to assess the effects of omega-3 fatty acids on obesity, diabetes, cancer, and various other diseases [17]. The effects of omega-6 polyunsaturated fatty acids on health are not clear. Data aggregated from various studies by Harris et al. [18] indicate that increasing intake of omega-6 fatty acids to 5%–10% of calories or more is associated with a reduced risk of cardiovascular disease. However, analysis of data from a large randomized control trial found that substituting saturated fatty acids with linoleic acid, the largest source of omega-6 fatty acids in the diet, resulted in an increase in cardiovascular disease risk, coronary heart disease, and death from all causes [19]. While the specific health effects of types of fatty acids are not well established, replacing carbohydrates with dietary fat appears to result in no change or an improvement in risk factors for cardiovascular disease. As mentioned previously, several studies have reported no change in risk with substitution of saturated fat for carbohydrate. Researchers have found that replacing carbohydrate with saturated, monounsaturated, and polyunsaturated fatty acids resulted in greater concentration of larger LDL particles and reductions in the amount of smaller, more atherogenic LDL particles in circulation [20,21]. This profile is enhanced to an even greater extent with reduction of carbohydrate intake to 10% of calories or less, with elevation of LDL cholesterol, but also increased HDL cholesterol, improved insulin sensitivity, and lowered circulating triglycerides and atherogenic, small, dense LDL particles [22,23]. The findings of studies on low-carbohydrate diets warrant research into their effects on cardiovascular disease, especially for those with insulin resistance, type 2 diabetes, or metabolic syndrome.

DIETARY FAT AS FUEL FOR EXERCISE Carbohydrates and fat provide the majority of the energy required for muscle contraction in endurance exercise [24]. Fat is the predominant fuel for moderate-intensity exercise, with maximal fat oxidation being reached at approximately 59%–64% of VO2max in endurance-trained athletes and 47%–52% of VO2max in untrained individuals, according to Achten and Jeukendrup [25]. As intensity rises, carbohydrate utilization increases, with glycogen as the primary source of this fuel [26]. Fat oxidation decreases to almost zero by an intensity of about 90% of VO2max [25]. Endurance training results in various adaptations that improve the ability of skeletal muscle to produce ATP for energy: increased capillary density [27]; greater glucose transporter 4 expression and plasma fatty acid transfer protein concentrations to enhance substrate delivery [28,29]; and increased mitochondrial volume and enzymes for metabolic pathways for breakdown of fat for fuel. Endurance training also increases glycogen storage in skeletal muscle, as well as intramuscular triglyceride content [30,31]. These training adaptations increase utilization of fat for fuel at submaximal exercise, sparing muscle glycogen.

DIETARY FAT RESTRICTION AND ENDURANCE EXERCISE Dietary fat restriction could result in difficulty meeting energy needs for athletes, especially those involved in endurance events. Consuming an adequate amount of calories is critical to optimize performance and should be a focus for athletes [32]. Energy restriction that could occur from reducing fat intake can disrupt endocrine function in females [33–36], reduce strength and endurance, and compromise immune function [37]. Adequate caloric intake is also necessary to spare amino acids for protein synthesis and building or preservation of lean tissue, instead of utilizing amino acids for energy [38,39]. Perturbations resulting from inadequate caloric intake place athletes at great risk of injury, illness, and fatigue [40]. Energy restriction may also result in dehydration and inadequate intake of nutrients, especially fat-soluble vitamins, if dietary fat is restricted, as well as a greater tendency to adapt disordered eating practices [40]. Clearly, severe energy restriction is contraindicated, given the negative effects described previously. However, the effects of energy deficits of short duration or relatively mild restriction on sports performance have been mixed. No negative effects on performance were reported in studies in which short-term hypocaloric diets were followed by wrestlers [41] and aerobically trained athletes [42]. Other studies reported decreased time to exhaustion for male recreational athletes [43] and reduced strength for judo fighters [44]. These studies undertook a more severe energy restriction, which could have contributed to the detrimental effect on performance. Based on these data, the authors indicated that performance is less likely to be compromised when weight loss is slower and carbohydrate intake is


Dietary Fat Restriction and Endurance Exercise


sufficient to ensure glycogen replenishment for endurance athletes [45]. More research is required to determine the specific effects of energy restriction on performance. In a systematic review by Heydenreich et al. [46], both male and female athletes were found to have a negative net energy balance in the preparatory phase (period of moderate-intensity, high-volume training before main competitions begin) and competitive phase (lower volume, high-intensity training while main competitions occur) of training. Overall, males consumed 4.7% less calories than were expended, whereas females came up short by 27.8%. Underreporting is a major issue with dietary records and a significant limitation to these findings. However, the authors noted that the athletes would still have been in negative energy balance for a large duration of their training periods after adjusting for the expected level of underreporting [46]. Horvath et al. [47] assessed caloric and nutrient intake for male and female runners who selected one of the three fat levels: low (17% of energy), medium (31% of energy), and high (44% of energy). The runners aged between 18 and 65 years and averaged 42 miles per week. Energy consumption, as determined by dietary records, was below the estimated energy expenditure for all groups; however, this energy deficit was significantly smaller for the two higher fat groups [47]. As with the study discussed previously, it is likely that subjects underreported intake and that overestimation of energy expenditure is a possibility. However, given the large difference reported between energy intake and expenditure, especially for the females consuming a low-fat diet (intake was estimated to meet ∼60% of their needs), it is likely that limiting fat to 17% of total calories resulted in inadequate intake that could negatively affect the performance and health of these endurance athletes. Interestingly all three diets provided carbohydrate at or near the amount required for maintaining glycogen stores [48]. Protein intake met the recommended dietary allowance (RDA) of 0.8 g/kg of body weight for all levels of fat intake; however, the RDA is likely too low for runners, given elevations in protein breakdown with high-intensity exercise. Findings from research point to an intake of 1.2–1.7 g/kg of body as an appropriate amount for endurance athletes [45,49]. All groups consumed protein within this recommended range, except for the females consuming a low-fat diet. Consumption of vitamin A and vitamin E was above the RDA for all groups in the study by Horvath et al. [47], although vitamin E intake increased with greater fat intake. Given that these nutrients are fat soluble, absorption may have been compromised on the low-fat diet. There is inconsistency in the literature, but some researchers suggest that the RDA is not sufficient for vitamin E for athletes, given its antioxidant properties and the elevation of oxidative stress which result from endurance training [50–52]. Zinc intake was below the RDA for all groups, and consumption of this nutrient also increased as fat intake was raised. This is a concern for athletes as poor zinc intake may affect not only health but also strength and endurance, resulting in hindering of athletic performance [53,54]. Muoio et al. [55] assessed the effects of restricting fat for 7 days on performance in trained middle-distance runners. Each runner consumed three diets for 7 days, while maintaining their normal training regimen: their normal diet (61.2% carbohydrate, 24.3% fat, and 13.7% protein), a high-fat diet (50% carbohydrate, 38% fat, and 12% protein), and a high-carbohydrate diet (73% carbohydrate, 15% fat, and 12% protein). A VO2max test and an endurance test were completed after consumption of each diet for 7 days. VO2max was highest and time to exhaustion was greatest after consumption of the high-fat diet. Interestingly, subjects consumed approximately 700 calories less than their estimated expenditure on their normal diet, but intake closely matched requirements for the prescribed diets. Despite the fact that energy intake was apparently adequate for the high-carbohydrate, low-fat diet in the study by Muoio et al. [55], performance was negatively impacted. Muoio et al. [55] put forth the possibility that a low-fat diet impaired performance by reducing the availability of intramuscular triglycerides as a fuel substrate [56–58]. This may be crucial as fat mobilization from adipose tissue to muscle could be limited, resulting in inadequate energy when intramuscular triglyceride stores are depleted. Research indicates that intramuscular triglyceride content is reduced significantly during prolonged exercise [59,60], but it is unclear if this depletion of stores is related to exercise performance. Given that carbohydrate is utilized predominantly at high intensities, it seems unlikely that performance in a maximal test or time to exhaustion at high intensity would be impacted primarily from depletion of intramuscular triglyceride stores. However, it may take 3–7 days for replenishment of intramuscular triglycerides after exercise if a high-carbohydrate diet is consumed [61,62], compared with 12–24 h for a moderate-fat diet (∼35% of total calories) [63]. If dietary fat intake is severely restricted, this could potentially lead to chronic depletion of intramuscular triglycerides, especially for endurance athletes completing high-volume training regimens. This chronic depletion may interfere with the glycogen-sparing benefits that result from greater fat utilization with training and adequate dietary fat intake. Dietary fat intakes of 35% of total energy or greater have been shown to supercompensate intramuscular triglyceride stores after exercise, potentially maximizing this glycogen-sparing adaptation [64,65]. Intramuscular triglycerides are an important fuel source during exercise, accounting for approximately a quarter of the energy expended during low- to moderate-intensity bouts [26,66]. While exercise intensity is the largest factor in substrate use, with fat utilized predominantly at lower intensities and carbohydrate required more as intensity




increases, shifts in carbohydrate and fat oxidation also occur based on the availability of substrate [67]. Greater intramuscular triglyceride concentrations result in a fat substrate that is readily available in the working muscle. The number of lipid droplets increases, while droplet volume is unchanged [68,69], which increases surface area to volume ratio, facilitating hydrolysis by lipases [70]. Depletion of intramuscular triglycerides is considerable with prolonged exercise of moderate intensity, with findings of 50%–70% depletion after exercise bouts lasting 2–3 h [71–75]. The adaptations that occur with exercise training and adequate dietary fat to increase intramuscular triglyceride content may be instrumental in glycogen sparing during extended periods of exercise. Inadequate dietary fat intake could blunt this adaptation, resulting in exhaustion from glycogen depletion. Taken together, research indicates that a low-fat diet could provide an inadequate amount of energy, protein, and micronutrients for endurance athletes, increasing the potential for oxidative stress, impaired immune function, loss of lean body mass, and compromised endocrine function, resulting in fatigue, poor performance, and greater risk of illness and injury. The specific amount of dietary fat is not known at this time; however, fat consumption below 30% of total calories would not be recommended.

DIETARY FAT INTAKE AND BODY COMPOSITION Many athletes attempt to reduce weight and fat mass, although weight loss may negatively affect performance in the preparatory and competitive phases. Although both low-fat and high-fat, low-carbohydrate diets can promote weight loss, high-fat, low-carbohydrate diets have been shown to cause greater weight and fat loss in long-term studies. A large metaanalysis of 32 randomized controlled trials with ∼54,000 subjects found that low-fat diets followed for a minimum of 6 months result in modest weight loss [76]. Some researchers define low-carbohydrate diets as an intake of this macronutrient at or below 45% of total calories, given that the acceptable macronutrient distribution range for carbohydrate is 45%–65% of calories. Hu et al. [77] completed a metaanalysis based on this definition and found no difference in weight loss in studies of 6 months or longer in which subjects consumed low-carbohydrate diets (carbohydrate providing 4%–45% of total calories) compared with subjects consuming low-fat diets (fat contributing 10%–30% of total calories). A separate metaanalysis of 11 randomized controlled trials with 1369 participants [78] assessed the effects of more severely restricted carbohydrate diets (20% of calories or less, high fat). In this assessment of studies lasting 6 months or longer, greater weight loss was achieved for subjects consuming low-carbohydrate, high-fat diets than those consuming low-fat diets. Researchers assessing body composition changes with low-carbohydrate, high-fat diets report similar patterns to those seen in studies evaluating body weight. A metaregression of 87 studies by Krieger et al. [79] found that energyrestricted diets in which the carbohydrate intake was in the lowest quartile (less than 41.4% of calories) resulted in significantly greater reductions in body fat percentage than the carbohydrate intake in the three highest quartiles. A trend was reported for studies of 12 weeks or less, but studies longer in duration reported average percent body fat reductions 3.55% greater than the three higher quartiles for carbohydrate intake, which is a significant difference. A separate metaanalysis by Hashimoto et al. [80] reported greater fat loss for obese subjects eating high-fat, very low–carbohydrate diets (10% of calories from carbohydrate or less) than for subjects consuming control diets after 12 months. But, akin to the findings of studies assessing body weight, no difference in fat loss was found compared with controls when subjects consumed mildly restricted carbohydrate diets (approximately 40% of calories from carbohydrate) [80]. To maximize fat loss, more restrictive low-carbohydrate, ketogenic diets that are high in fat may be the most effective for greater fat loss than high-carbohydrate, low-fat diets [81,82] and also may allow for greater retention of fat-free mass [82]. Incorporating exercise with diet is recommended and necessary to promote optimal weight loss. Jabekk et al. [83] compared the effects of a 10-week resistance training program alone with a combination of the training program and a high-fat, low-carbohydrate diet (6% carbohydrate, 66% fat, 22% protein, and 5% alcohol) in overweight women. Training alone resulted in a 1.6-kg gain in lean body mass, with no change in fat mass. The combination of resistance training and a high-fat, low-carbohydrate diet allowed for preservation of lean mass, with a reduction in fat mass of 5.6 kg [83]. Quann [84] compared the effects of a high-fat, low-carbohydrate diet (less than 15% of calories) with those of a low-fat diet (less than 25% of calories) with or without resistance exercise for 12 weeks on untrained men. The combination of carbohydrate restriction and exercise was the most effective intervention. Lean body mass was not only preserved but actually slightly increased for the subjects who performed resistance training [84]. The group that followed the high-fat, low-carbohydrate diet, combined with resistance training, had an average body fat loss of 7.7 kg, compared with 3.5 kg for the low-fat resistance training group [84].


High-Fat Diets and Exercise Performance


The effects of a high-fat, carbohydrate-restricted diet on body composition have also been evaluated for trained subjects. Wilson et al. [85] randomized resistance-trained males to a low-fat (55% carbohydrate, 20% protein, and 25% fat) or a very low–carbohydrate, high-fat ketogenic diet (5% carbohydrate, 20% protein, and 75% fat). The subjects adapted to the diets for 2 weeks before starting a 9-week resistance training program. The low-carbohydrate, high-fat group had carbohydrates slowly reintroduced into their diet in the final week, whereas the low-fat group consumed the same diet for the entire 11 weeks. Lean body mass increased and fat mass decreased for both groups. Interestingly, lean body mass gains were not different between groups at week 10, but the low-carbohydrate group had significant gains in lean body mass between week 10 and 11, resulting in greater gains overall. However, the authors attributed this to gains in water and concluded that actual lean body mass gains were likely similar between groups [85]. More research is needed to determine the effects of high-fat, low-carbohydrate diets on body composition in trained and untrained individuals, especially over an extended period. There has been much speculation over the reasons that high-fat, very low–carbohydrate diets often result in greater weight and fat loss than other diets. First, it is likely that large caloric deficits are created as subjects report being satiated and often spontaneously consume few calories, even with ad-lib diets [86]. A second explanation that has been postulated is that the greater protein intake that accompanies very low–carbohydrate diets could be responsible [86]. Consuming a high-protein diet (1.2–1.6 g/kg) improves body composition compared with diets in which protein is near the RDA (0.8 g/kg) [86–90]. This finding was also confirmed by the metaregression of 87 studies completed by Krieger et al. [79], which indicated significantly greater retention of fat-free mass for diets with protein intake above 1.05 g/kg in studies lasting 12 weeks or longer. The positive effects of higher protein diets on weight and fat loss may be in part due to alterations in energy expenditure. A metaanalysis of 24 randomized controlled trials revealed that average resting energy expenditure was approximately 150 calories per day greater for subjects consuming energy-restricted diets that were high in protein and low in fat compared than for those consuming low-fat diets with protein levels near the RDA [91]. Researchers in a separate study reported no difference in energy expenditure, as determined by closed-circuit indirect calorimetry, after regular consumption of a high-fat diet compared with a high-carbohydrate diet [92]. Therefore one may expect comparable elevation of energy expenditure for high-fat, high-protein diets. A study comparing the effects of a high-fat, low-carbohydrate diet with those of a low-fat diet found greater weight loss for the high-fat, low-carbohydrate group, despite failing to detect a difference in caloric intake or resting energy expenditure between the groups [93]. However, protein intake was only 1.0–1.1 g of protein per kg of body weight for the low-carbohydrate group, which may have been too low to affect energy expenditure. Energy expenditure was estimated, and dietary intake was self-reported, leading the authors to attribute the difference in weight loss to underreporting for the group consuming the low-fat diet [93]. Two compelling explanations for greater weight and fat loss with very low–carbohydrate, high-fat diets that require more research have been put forth. Feinman and Fine [94] pointed out that more energy is expended in protein turnover for gluconeogenesis and that this process would be increased to a large enough degree to raise energy expenditure significantly for the body when carbohydrates are severely limited, as with a high-fat ketogenic diet. Volek et al. [95] linked fat loss to lowering of insulin, citing a positive correlation between reductions in insulin concentrations and fat loss (R2 = 0.67). Lower circulating insulin mobilizes free fatty acids from adipose stores [96], and Volek et al. [95] postulate that this would contribute significantly to reductions in body fat. This link between a key function of insulin, inhibition of lipolysis, and reductions in body fat needs to be investigated further in the context of a low-carbohydrate, high-fat diet. Research to confirm these hypotheses is lacking at this point. In addition to the studies described previously [92,93], a metaanalysis by Hall and Guo [97] of 32 controlled feeding studies with 563 subjects assessed the effects of varying dietary carbohydrate and fat intake on body fat and energy expenditure. Contrary to what might be expected, energy expenditure for subjects on the low-fat diets was slightly higher than that for those on the lowcarbohydrate, high-fat diets (26 calories per day). The authors concluded that there is basically no difference in the effect of dietary carbohydrate compared with that of dietary fat on energy expenditure [97].

HIGH-FAT DIETS AND EXERCISE PERFORMANCE Several studies have assessed the effects of a high-fat diet on endurance exercise; however, many questions persist. Increased fat utilization for fuel at relative submaximal intensities which occurs with endurance training helps to prevent expending glycogen, which is a limited fuel source. The nearly unlimited fuel source provided by adipose tissue makes high-fat diets an appealing alternative. Studies have consistently reported an increase in fat oxidation




during submaximal exercise after adaptation to high-fat diets, with an approximate doubling of the oxidation rates normally reported with restriction to the degree that would bring about ketosis (Table 47.1) [108–110]. High-fat diets result in greater intramuscular triglyceride stores, enhancing substrate availability [110]. In addition, elevated hormone-sensitive lipase and transport proteins fatty acid translocase (FAT)/CD36 and carnitine palmitoyltransferase increase transfer of triglyceride into muscle tissue [110]. Adaptations appear to occur quickly as FAT/CD36 mRNA and protein content in muscle were shown to be greater after only 5 days of a high-fat diet [104]. Carnitine palmitoyltransferase 1 activity was reported to increase after 15 [99] and 28 days [111] of fat adaptation. Although upregulation of fat oxidation occurs with high-fat diets, the necessary shift to carbohydrate use for fuel for higher intensity exercise would appear to be a limitation of this diet for athletes choosing this dietary approach. Phinney et al. [98] has contributed significantly to the seminal work in this area and reported no difference in time to exhaustion for trained cyclists after following a high-fat, very low–carbohydrate diet for 4 weeks, but this test was completed at 62%–64% of VO2max, with a short adaptation time. Research findings since have been mixed, with studies reporting improvements, no change, or impairment in bouts in some instances (Table 47.1). Lately, Burke et al. [108] assessed performance of racewalkers in a 10,000-m racewalking before and after 3 weeks on three different diets: high carbohydrate (60%–65% carbohydrate, 15%–20% protein, and 20% fat); periodized carbohydrate (same macronutrient breakdown as high carbohydrate, but with low carbohydrate days followed by high carbohydrate to maximize muscle glycogen), and low carbohydrate (less than 5% carbohydrate or below 50 g/day, 15%–20% protein, and 75%–80% fat). Racewalkers in all the three groups improved their aerobic capacity with training, as assessed by VO2 peak. Whole-body fat oxidation during exercise increased for the low-carbohydrate group, as found in previous research with low-carbohydrate/high-fat diet interventions [108]. Performance in the 10,000-m racewalk improved for the high-carbohydrate and periodized carbohydrate group but did not change from baseline for the low-carbohydrate group. Zinn et al. [112] completed a pilot study of longer duration, with five athletes consuming a high-fat ketogenic diet for 10 weeks. Performance factors, as assessed by an incremental cycle test, were negatively affected, with a reduction in time to exhaustion by 2 min and decreased peak power (P = .07). However, the athletes’ body weights were decreased by an average of 4 kg in the 10-week period. Athletes once again had greater whole-body fat oxidation during exercise. Active weight loss, combined with increased feelings of fatigue and difficulty to complete high-intensity training, likely contributed to the decrease in performance for the athletes in this study. Burke et al. [108] and Zinn et al. [112] both reported an increase in oxygen cost for substrate utilization with the lowcarbohydrate diets due to the increased use of fat for fuel. Zajac et al. [113] completed a study in which cyclists followed a ketogenic and mixed diet, in a crossover design, but for only 4 weeks. Athletes on the ketogenic diet had reductions in body weight and fat mass, but aerobic capacity was actually improved on this diet, as determined by VO2max and lactate threshold. However, power output was lower at maximal intensity, when compared to performance after the mixed diet. The greater oxygen cost for athletes performing the exercise bout after the ketogenic diet was displayed by a lower respiratory exchange ratio. The authors called into question the limits of ATP production with fat as a primary fuel because the maximum amount of ATP that can be resynthesized from circulating free fatty acids has been calculated as 0.4 mol/min, compared with 1.0–2.0 mol/min for glycogen [114]. Rate of breakdown at high intensities would be too high to match synthesis from free fatty acids, impairing performance in high-intensity bouts. Another issue in question for endurance athletes following a low-carbohydrate diet is the effect the diet has on high-intensity training sessions, as well as within races of long duration. Endurance athletes often complete interval training near maximal intensity, and pace can vary considerably in races with hill climbs, breakaways, and sprints at the finish in which maximal intensity is reached [108,115,116]. At maximal intensity, carbohydrate is relied on for fuel [117]. Research completed by Volek et al. [109] suggests that glycogen may be spared for these high-intensity spurts if adaptation time is allowed for glycogen homeostasis, making carbohydrate stores available for high-intensity spurts; however, research is still necessary. High-fat, ketogenic diets may require a significant amount of time for adaption. It is common for people to report fatigue and a lack of energy for the first few weeks after adapting a ketogenic diet, which could compromise training and performance in the competitive season. Volek et al. [109] have indicated that several months may be necessary for adaptation, for the symptoms of fatigue to subside, as well as for adjustment of glycogen homeostasis. In a recent study by this group [109], fat oxidation and glycogen utilization were assessed in a 3-h submaximal run for endurance athletes (64% of VO2max) consuming a high-fat, low-carbohydrate ketogenic diet (<20% of total calories from carbohydrate, >60% from fat) or high-carbohydrate diet (greater than 55% of total calories from carbohydrate). The athletes had been consuming these diets for an average of 20 months before the submaximal test, allowing sufficient time for adaptation. Fat oxidation was 1.54 g/min for the low-carbohydrate group, compared with 0.67 g/min for the high-carbohydrate group. Interestingly, muscle glycogen did not differ between groups, at rest or after the


TABLE 47.1 Summary of Studies Investigating Fat Adaptation With and Without Carbohydrate Restoration on Whole-Body Metabolism, Skeletal Muscle Adaptation, and Performance FATox (vs. Cont)

Skeletal Muscle Adaptation (vs. Cont)

1-wk eucaloric balanced diet followed by 4-wk ketogenic diet (<20 g CHO/d)

Threefold ↓ in glucose oxidation; fourfold ↓ in glycogen utilization

1-wk eucaloric balanced diet followed by 4-wk ketogenic diet (<20 g CHO/d)

↓ Glycogen content (resting); ↓ glycogen utilization (exercise)




Phinney et al. [98]

n = 5 M: well-trained cyclists (>65 mL/kg  per min)

Fisher et al. [139]

n = 5 M: well-trained cyclists (5.1 L/min)

↑ CPT activities; ↓ HK Muoio et al. [55]

n = 5 M: trained cyclists (4.2 L/min)

Cont: Normal (6.5 g/kg CHO, 1.1 g/kg fat)

Expt: HCHO (9.7 g/kg CHO, 0.9 g/kg fat)

Expt: HFAT (6.7 g/kg CHO, 2.2 g/kg fat)

Expt: 2-wk HFAT

˙ 2max ; Cycle TTE (∼60% VO ∼150 min) ↔ ˙ 2max ; and running HFAT ↑ VO TTE

↓ Glycogen content (resting); glycogen utilization (exercise) ↔

Cont: 2-wk HCHO

˙ 2max ; Cycle TTE (62%–64% VO ∼150 min) ↔

˙ 2max ; HFAT ↑ TTE (60% VO 80 vs. 43 min) ˙ 2max ; 8–13 min) TTE ↔ (90% VO

Maximal PO ↔(30-s Wingate test; 804–862 W) Goedecke et al. [99]

Burke et al. [100]

n = 16 M: trained cyclists (63.5 mL/kg  per min)

Cont: Habitual (5.6 g/kg CHO, 1.4 g/kg fat)

n = 8 M: well-trained cyclists (64.4 mL/kg  per min)

Cont: 6-d HCHO (9.6 g/kg CHO, 0.7 g/kg fat)

Expt: HFAT (2.6 g/kg CHO, 4.1 g/kg fat)

Expt: 5-d HFAT (2.4 g/kg CHO, 4.0 g/kg fat) + 1-d HCHO Venkatraman et al. [141]

Carey et al. [101]

n = 12 M. 13 F: recreationally trained runners (F. 50 mL/kg per min; M, 58 mL/kg  per min)

Cont: 4-wk low-fat diet (0.5 g/kg F, 0.5 g/kg M)

n = 7 M: well-trained cyclists (5.06 L/min)

Cont: 7-d HCHO (9.0 /kg CHO, 1.8 g/kg fat)

↓ Estimated rates of glycogen oxidation ↑

↑ High- and moderate-fat diet ↑ running TTE (F, 39–47 min; M, 44–56 min)

↑ 60-min TT (km) with 4-h (65% ˙ 2peak ) preload ↔ VO ↑ Continued


Expt: 6-d HFAT (2.5 g/kg CHO, 4.6 g/kg fat) + 1-d HCHO

↑ CPT activities; CS and β-HAD ↔ ↓ Glycogen content (resting) after 5-d TT performance (7 kJ/kg; HFAT but restored after 1-d HCHO; 30–35 min) with 120-min ↓ glycogen utilization (exercise) preload (∼150 min in total) ↔

Expt: 4-wk moderate-fat diet (1.2 g/kg BM F, 1.4 g/kg BM M) Expt: 4-wk HFAT (1.8 g/kg BM F, 2.1 g/kg BM M)

40-km TT ↔ (∼65 min)

High-Fat Diets and Exercise Performance


Lambert et al. [140]

n = 6 M: well-trained runners (63.7 mL/kg per min)

Performance (vs. Cont)




Lambert et al. [102]

n = 5 M: well-trained cyclists (4.9 L/min)

Cont: 10-d habitual diet + 3-d HCHO Expt: 10-d HFAT + 3-d HCHO

Rowlands and Hopkins [142]

Cameron-Smith et al. [104]

Havemann et al. [105]

Yeo et al. [107]

↑ Estimated rates of muscle glycogen Expt. ↑ 20-km TT performance and lactate oxidation (∼30 min) with 150-min ˙ 2peak preload at 70% VO (∼180 min in total)

Cont: 14-d HCHO (9.1 g/kg CHO, 0.9 g/kg fat) ↑

Expt 2: 11.5-d HFAT + 2.5-d HCHO

n = 8 M: well-trained cyclists (68.6 mL/kg per min)

Cont: 6-d HCHO (9.3 g/kg CHO, l.1 g/kg fat)

n = 14 M: well-trained cyclists and triathletes (67 mL/kg per min)

Cont: 5-d HCHO (9.6 g/kg CHO, 0.7 g/kg fat)

n = 8 M: well-trained cyclists (57.8 mL/kg per min)

Cont: 7-d HCHO (7.5 g/kg CHO, 0.8 g/kg fat)

Expt: 5-d HFAT (2.5 g/kg CHO, 4.3 g/kg fat) + 1-d HCHO

Expt: 5-d HFAT (2.4 g/kg CHO, 4.0 g/kg fat)

n = 7 M: well-trained cyclists (60.7 mL/kg per min)

Cont: 6-d HCHO (2.5 g/kg CHO, 4.6 g/kg fat)

n = 8 M: well-trained cyclists (61.5 mL/kg per min)

Cont: 6-d HCHO (10.3 /kg CHO, 1.0 g/kg fat)

Expt: 5-d HFAT (10.3 g/kg CHO, 1.0 g/kg fat) + 1-d HCHO

Expt: 5-d HFAT (2.5 g/kg CHO, 4.6 g/kg fat) + 1-d HCHO

Performance (vs. Cont)

Expt. 1 and 2 attenuated the decline in power output

Expt 1: 14-d HFAT (2.4 g/kg CHO, 4.7 g/kg fat)

Expt: 6-d HFAT (1.9 g/kg CHO, 3.3 g/kg fat) + 1-d HCHO Stellingwerff et al. [106]

Skeletal Muscle Adaptation (vs. Cont)

During the last 5 km of a 100km (∼155-min) TT

Plasma glucose uptake ↔ ↑

TT performance (7 kJ/kg; ∼25 min) with 120-min preload (∼145 min in total) ↔

HFAT ↑ FAT/CD36 (protein and mRNA) and β-HAD mRNA ↑ Normalized EMG amplitude during 1-km sprint ↔ ↑

Expt. ↓ PO during 1-km sprint but not during 4-km; sprint at designated distances during a 100-km TT; 100-km TT performance (100 km; ∼155 min) ↔

↓ PDH activity (resting and exercise); ↓ glycogenosis (exercise) ↑

↓ Estimated substrate phosphorylation (exercise) ↑ Resting TG; ↑ resting AMPKα1 and α2 activity;

↑ p-ACC postexercise

↑ increase; ↓, decrease; ↔, unchanged; β-HAD, β-hydroxyacyl-CoA-dehydrogenase; AMPK, 5′AMP-activated protein kinase; CHO, carbohydrate; Cont, control group; CPT, carnitine palmitoyltransferase; CS, citrate synthase; EMG, electromyogram; Expt, experimental group; F, female; FAT/CD36, fatty acid translocase; HCHO, high-carbohydrate diet; HFAT, high-fat diet; HK, hexokinase; M, male; p-ACC, phosphorylation of ˙ 2max , maximal oxygen consumption. acetyl-CoA-carboxylase; PDH, pyruvate dehydrogenase; PO, power output; TG, triglyceride; TT, time trial; TTE, time to exhaustion; VO Reprinted from Yeo WK, Carey AL, Burke L, Spriet LL, Hawley JA. Fat adaptation in well-trained athletes: effects on cell metabolism. Appl Physiol Nutr Metab (Physiologie appliquee, nutrition et metabolisme) 2011;36(1):12–22. © Canadian Science Publishing or its licensors.



Burke et al. [103]

n = 7 M: well-trained cyclists (72 mL/kg per min)

FATox (vs. Cont)


TABLE 47.1  Summary of Studies Investigating Fat Adaptation With and Without Carbohydrate Restoration on Whole-Body Metabolism, Skeletal Muscle Adaptation, and Performance—cont’d

Dietary Fat and Resistance Training


3-h run. This is in contrast to a study by Phinney et al. [98] which reported muscle glycogen concentrations half that of high-carbohydrate counterparts at rest for elite cyclists who followed a high-fat, low-carbohydrate diet for 4 weeks. Additional research is necessary to determine the amount of time required for adaptation, but it seems that a period of months is required, making a transition to this way of eating more appropriate outside of an athlete’s competitive season. Alteration of the pyruvate dehydrogenase complex during exercise which occurs when following a high-fat diet and the implications of this change may be important for a better understanding of how this diet affects endurance exercise performance. The pyruvate dehydrogenase complex regulates decarboxylation of pyruvate to acetyl-CoA, a process required for oxidation of carbohydrates in the mitochondria of skeletal muscle [118]. Gudiksen et al. [119] reported no difference in skeletal muscle pyruvate dehydrogenase activity for trained subjects and untrained subjects exercising at the same relative submaximal intensity. However, trained subjects had greater pyruvate dehydrogenase activity after high-intensity exercise, indicating greater capacity for carbohydrate oxidation [119]. Pyruvate dehydrogenase activity is decreased during exercise after a fat adaptation period as short as 3–5 days [106,120,121]. In the context of low-carbohydrate, high-fat diets, glycogen sparing through increased use of fat as fuel has been described as an instrumental adaption that benefits athletes. On the other hand, Burke et al. [120] have described the reduction of pyruvate dehydrogenase activity as an impairment of glycogen regulation [106], lowering the ability to utilize glycogen for fuel during high-intensity exercise. If athletes are unable to upregulate pyruvate dehydrogenase activity at high intensities to oxidize carbohydrate to adequately fuel skeletal muscle, this may impair maximal performance. Most researchers have assessed performance after short periods and have not allowed time for proper adaptation before assessing pyruvate dehydrogenase activity and performance at high intensities. Volek et al. [109] allowed an extended period of time for adaptation, but the focus of the research was metabolic adaptations to the diet, not exercise performance. Future research allowing months for adaptation, with the addition of a maximal test and assessment of pyruvate dehydrogenase activity, will help to elucidate the effects of high-fat, low-carbohydrate diets on high-intensity exercise, as well as the role the pyruvate dehydrogenase complex plays in the context of this dietary approach.

FAT LOADING/CARBOHYDRATE RESTORATION PROTOCOLS To attempt to upregulate fat oxidation during exercise, while also ensuring sufficient glycogen stores, researchers have assessed the effects of fat loading for a short period of time (5–14 days), followed by 1–3 days of carbohydrate loading [100–103,106,107,110,122]. Given that 1 day of carbohydrate loading has been shown to be adequate to restore muscle glycogen [100,106,107], researchers in this area have adjusted to limiting the loading time to a single day. Fat oxidation is indeed increased above baseline with this protocol, but below oxidation rates found before carbohydrate loading [100,106,107], with a glycogen-sparing effect. However, this approach does not appear to have consistent effects on performance, with researchers reporting improved performance, no change, or worse performance after following this kind of dietary protocol (Table 47.1). Most of the studies assessing this technique have looked at performance at submaximal intensity. Havemann et al. [105] assessed both submaximal and high-intensity exercise performance. In this study, eight cyclists took part in a crossover study in which they completed two 100-km time trials, after consuming a high-carbohydrate (68% of calories as carbohydrate) or high-fat diet (68% of calories as fat) for 6 days, followed by a carbohydrate-loading day. Performance in the time trial was not significantly different after the diet interventions. Sprint performance was assessed by determining power output during 1- and 4-km sprints that were completed at set points throughout the time trials. Performance in the 4-km sprints was not different in the time trials; however, power output was significantly lower in the 1-km sprints after consuming the high-fat diet. Given that glycogen stores were adequate for both trials, this may point to an inability to access this fuel source in high-intensity exercise (above 90% of maximum power output) as the authors cited “metabolic inflexibility” at this very high intensity as the cause for this impairment of performance [105]. It is unclear if this impairment in performance in high-intensity exercise would be present after a longer period of fat adaptation, thus requiring future studies with longer adaptation periods, as discussed in the previous section.

DIETARY FAT AND RESISTANCE TRAINING Anecdotally, many strength athletes follow high-fat, low-carbohydrate diets, yet research in this area is extremely limited at this point. Strength and power were improved for both the low-carbohydrate, high-fat (5% carbohydrate, 20% protein, 75% fat) and low-fat (55% carbohydrate, 20% protein, 25% fat) groups in the study described previously




by Wilson et al. [85], with no difference between groups. The subjects adapted to the diets for 2 weeks before starting a 9-week resistance training program. Maintenance of strength while reducing body fat and improving body composition was also reported for gymnasts [123] and resistance-trained subjects [124] on a high-fat, very low–carbohydrate diet. Based on the evidence in the field to this point, low-carbohydrate, high-fat diets appear to be a potentially effective method for altering body composition without negatively affecting strength and power in trained individuals. If body composition is improved by a high-fat, low-carbohydrate diet, it would make intuitive sense that the amount of force relative to body weight would increase [125]. Future research, with longer adaptation periods, will be required. The athletes who could benefit the most may be those who require weight loss or an effective way to improve body composition in the preseason period, before the start of competition.

DIETARY FAT INTAKE FOR PERFORMANCE IN TEAM SPORTS Team sports are characterized by prolonged low- to moderate-intensity work, with repeated high-intensity spurts that may approach maximal effort, with short recovery times [126,127]. Given the worldwide popularity of soccer, research involving team competition has focused primarily on this sport. Average oxygen consumption throughout a soccer match has been estimated at 70%–80% VO2max [128,129], leading to significant glycogen depletion [130]. Glycogen depletion during a soccer match has been associated with reduced speed and distance covered [131–133]. Glycogen depletion could not only affect performance in the latter stages of games [130,133], limiting training ­volume and stifling improvements in conditioning. In a study by Souglis et al. [134], professional soccer players completed two matches after 3.5 days of consuming a high-carbohydrate (78% of calories from carbohydrate, 14% from fat) or high-fat, moderately low–carbohydrate diet (29.5% of total calories from carbohydrate, 58% of calories from fat). The distance covered by athletes after the high-carbohydrate diet was approximately 1300 m further than that covered by athletes after the high-fat diet, representing a 17% difference. The soccer players completed more work not just at high intensities but all intensities. This appears to have potentially translated into better performance as the team that consumed the high-carbohydrate diet won the match in both instances. Similarly, Balsom et al. [130] reported that soccer players completed more high-intensity exercise during a 4-to-a-side 90-min match after following a diet with 8 g of carbohydrate per kg of body weight than consuming a diet of 3 g of carbohydrate per kg of body weight (high fat) for 2 days. Researchers reported higher muscle glycogen concentrations before the match after consuming the high-carbohydrate diet. They did not assess muscle glycogen concentrations after the matches but speculated that glycogen depletion resulted in fatigue and a decrease in exercise completed at high intensity. Various researchers have reported that higher level soccer players complete more high-intensity exercise over the course of a match than lower level players, displaying the importance of high-intensity work for elite athletes in team sports [132,135–138]. Research findings clearly indicate that following a moderately restricted carbohydrate, high-fat diet for a short period can impair performance. However, research is yet to be completed determining the effects of adaptation to a high-fat diet over a long period. As with endurance exercise, it is likely that adaptation to high-fat, low-carbohydrate diets that result in ketosis would increase fat oxidation and reduce glycogen utilization. This may impair sprint performance and decrease work output rate, especially at high intensity, but evaluation of these issues is still needed.

CONCLUSIONS Dietary fat is often overlooked by athletes as focus tends to be on carbohydrate for endurance sports for replacement of glycogen and protein for individuals striving to increase muscle strength and power. However, dietary fat is a critical macronutrient as fat restriction can result in energy deficits and suboptimal intake of zinc and fatsoluble vitamins, leading to fatigue, poor performance, and greater risk of illness or injury. A fat intake of ∼35% of total calories may be most prudent for endurance athletes, based on current research, allowing for adequate caloric intake and supercompensation of intramuscular triglyceride stores, while providing room in the diet for carbohydrate for glycogen replacement. However, high-fat, low-carbohydrate diets have been reported to enhance body composition, increase fat oxidation during submaximal exercise bouts, and improve risk factors for cardiovascular disease. Long-term research assessing performance still needs to be completed in the context of high-fat, low-carbohydrate diets.




References [1] USDHHS, USDA. 2015–2020 Dietary guidelines for Americans. 8th ed. 2015. Washington (DC). [2] Manore MM. Exercise and the Institute of Medicine recommendations for nutrition. Curr Sports Med Rep 2005;4(4):193–8. [3] Grande F, Anderson JT, Keys A. Comparison of effects of palmitic and stearic acids in the diet on serum cholesterol in man. Am J Clin Nutr 1970;23(9):1184–93. [4] Nicolosi RJ. Dietary fat saturation effects on low-density-lipoprotein concentrations and metabolism in various animal models. Am J Clin Nutr 1997;65(5 Suppl.):1617S–27S. [5] Astrup A, Dyerberg J, Elwood P, Hermansen K, Hu FB, Jakobsen MU, Kok FJ, Krauss RM, Lecerf JM, LeGrand P, Nestel P, Riserus U, Sanders T, Sinclair A, Stender S, Tholstrup T, Willett WC. The role of reducing intakes of saturated fat in the prevention of cardiovascular disease: where does the evidence stand in 2010? Am J Clin Nutr 2011;93(4):684–8. [6] Dehghan M, Mente A, Zhang X, Swaminathan S, Li W, Mohan V, Iqbal R, Kumar R, Wentzel-Viljoen E, Rosengren A, Amma LI, Avezum A, Chifamba J, Diaz R, Khatib R, Lear S, Lopez-Jaramillo P, Liu X, Gupta R, Mohammadifard N, Gao N, Oguz A, Ramli AS, Seron P, Sun Y, Szuba A, Tsolekile L, Wielgosz A, Yusuf R, Hussein Yusufali A, Teo KK, Rangarajan S, Dagenais G, Bangdiwala SI, Islam S, Anand SS, Yusuf S. Prospective Urban Rural Epidemiology (PURE) study investigators. Associations of fats and carbohydrate intake with cardiovascular disease and mortality in 18 countries from five continents (PURE): a prospective cohort study. Lancet (Lond Engl) 2017;390(10107):2050–62. [7] Mozaffarian D, Micha R, Wallace S. Effects on coronary heart disease of increasing polyunsaturated fat in place of saturated fat: a systematic review and meta-analysis of randomized controlled trials. PLoS Med 2010;7(3):e1000252. [8] 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(6):384–90. [9] Micha R, Mozaffarian D. Saturated fat and cardiometabolic risk factors, coronary heart disease, stroke, and diabetes: a fresh look at the evidence. Lipids 2010;45(10):893–905. [10] Mensink R. Effects of saturated fatty acids on serum lipids and lipoproteins: a systematic review and regression analysis. Geneva: World Health Organization; 2016. [11] Schwingshackl L, Hoffmann G. Monounsaturated fatty acids, olive oil and health status: a systematic review and meta-analysis of cohort studies. Lipids Health Dis 2014;13. 154-511X-13-154. [12] Mozaffarian D. Fish and n-3 fatty acids for the prevention of fatal coronary heart disease and sudden cardiac death. Am J Clin Nutr 2008;87(6):1991S–6S. [13] Cabo J, Alonso R, Mata P. Omega-3 fatty acids and blood pressure. Br J Nutr 2012;107(Suppl. 2):S195–200. [14] Harris WS, Bulchandani D. Why do omega-3 fatty acids lower serum triglycerides? Curr Opin Lipidol 2006;17(4):387–93. [15] Roche HM, Gibney MJ. Effect of long-chain n-3 polyunsaturated fatty acids on fasting and postprandial triacylglycerol metabolism. Am J Clin Nutr 2000;71(1 Suppl.):232S–7S. [16] Chang CL, Deckelbaum RJ. Omega-3 fatty acids: mechanisms underlying ‘protective effects’ in atherosclerosis. Curr Opin Lipidol 2013;24(4):345–50. [17] Calder PC. Marine omega-3 fatty acids and inflammatory processes: effects, mechanisms and clinical relevance. Biochim Biophys Acta 2015;1851(4):469–84. [18] Harris WS, Mozaffarian D, Rimm E, Kris-Etherton P, Rudel LL, Appel LJ, Engler MM, Engler MB, Sacks F. Omega-6 fatty acids and risk for cardiovascular disease: a science advisory from the American Heart Association Nutrition Subcommittee of the Council on nutrition, physical activity, and metabolism; Council on Cardiovascular Nursing; and Council on Epidemiology and Prevention. Circulation 2009;119(6):902–7. [19] Ramsden CE, Zamora D, Leelarthaepin B, Majchrzak-Hong SF, Faurot KR, Suchindran CM, Ringel A, Davis JM, Hibbeln JR. Use of dietary linoleic acid for secondary prevention of coronary heart disease and death: evaluation of recovered data from the Sydney Diet Heart Study and updated meta-analysis. BMJ (Clin Res Ed.) 2013;346:e8707. [20] Faghihnia N, Tsimikas S, Miller ER, Witztum JL, Krauss RM. Changes in lipoprotein(a), oxidized phospholipids, and LDL subclasses with a low-fat high-carbohydrate diet. J Lipid Res 2010;51(11):3324–30. [21] Krauss RM, Blanche PJ, Rawlings RS, Fernstrom HS, Williams PT. Separate effects of reduced carbohydrate intake and weight loss on atherogenic dyslipidemia. Am J Clin Nutr 2006;83(5):1025–31. quiz 1205. [22] Volek JS, Fernandez ML, Feinman RD, Phinney SD. Dietary carbohydrate restriction induces a unique metabolic state positively affecting atherogenic dyslipidemia, fatty acid partitioning, and metabolic syndrome. Prog Lipid Res 2008;47(5):307–18. [23] Volek JS, Sharman MJ, Gomez AL, DiPasquale C, Roti M, Pumerantz A, Kraemer WJ. Comparison of a very low-carbohydrate and lowfat diet on fasting lipids, LDL subclasses, insulin resistance, and postprandial lipemic responses in overweight women. J Am Coll Nutr 2004;23(2):177–84. [24] Cermak NM, van Loon LJ. The use of carbohydrates during exercise as an ergogenic aid. Sports Med (Auckl NZ) 2013;43(11):1139–55. [25] Achten J, Jeukendrup AE. Optimizing fat oxidation through exercise and diet. Nutrition (Burbank Los Angel County Calif) 2004;20(7–8):716–27. [26] van Loon LJ, Greenhaff PL, Constantin-Teodosiu D, Saris WH, Wagenmakers AJ. The effects of increasing exercise intensity on muscle fuel utilisation in humans. J Physiol 2001;536(Pt 1):295–304. [27] Hermansen L, Wachtlova M. Capillary density of skeletal muscle in well-trained and untrained men. J Appl Physiol 1971;30(6):860–3. [28] Andersen PH, Lund S, Schmitz O, Junker S, Kahn BB, Pedersen O. Increased insulin-stimulated glucose uptake in athletes: the importance of GLUT4 mRNA, GLUT4 protein and fibre type composition of skeletal muscle. Acta Physiol Scand 1993;149(4):393–404. [29] Talanian JL, Holloway GP, Snook LA, Heigenhauser GJ, Bonen A, Spriet LL. Exercise training increases sarcolemmal and mitochondrial fatty acid transport proteins in human skeletal muscle. Am J Physiol Endocrinol Metab 2010;299(2):E180–8. [30] Gollnick PD, Armstrong RB, Saubert 4th CW, Piehl K, Saltin B. Enzyme activity and fiber composition in skeletal muscle of untrained and trained men. J Appl Physiol 1972;33(3):312–9. [31] Hoppeler H, Luthi P, Claassen H, Weibel ER, Howald H. The ultrastructure of the normal human skeletal muscle. A morphometric analysis on untrained men, women and well-trained orienteers. Pflug Arch Eur J Physiol 1973;344(3):217–32.




[32] Thomas DT, Erdman KA, Burke LM. Position of the Academy of Nutrition and Dietetics, Dietitians of Canada, and the American College of Sports Medicine: nutrition and athletic performance. J Acad Nutr Diet 2016;116(3):501–28. [33] Beals K, Houtkooper L. In: Burke L, Deakin V, editors. Disordered eating in athletes in clinical sports nutrition. Sydney: McGraw Hill; 2006. p. 201–26. [34] Beals K, Manore M. Nutritional considerations for the female athlete. In: Advances in sports and exercise science series. Philadelphia: Elsevier; 2007. p. 187–206. [35] Gabel KA. Special nutritional concerns for the female athlete. Curr Sports Med Rep 2006;5(4):187–91. [36] Sundgot-Borgen J, Torstveit MK. Prevalence of eating disorders in elite athletes is higher than in the general population. Clin J Sport Med 2004;14(1):25–32. [37] Burke LM, Loucks AB, Broad N. Energy and carbohydrate for training and recovery. J Sports Sci 2006;24(7):675–85. [38] Bartlett JD, Hawley JA, Morton JP. Carbohydrate availability and exercise training adaptation: too much of a good thing? Eur J Sport Sci 2015;15(1):3–12. [39] Stellingwerff T. Contemporary nutrition approaches to optimize elite marathon performance. Int J Sports Physiol Perform 2013;8(5):573–8. [40] Manore M, Meyer M, Thompson J. Sport nutrition for health and performance. 2nd ed. Champaign: Human Kinetics; 2009. [41] Mourier A, Bigard AX, de Kerviler E, Roger B, Legrand H, Guezennec CY. Combined effects of caloric restriction and branched-chain amino acid supplementation on body composition and exercise performance in elite wrestlers. Int J Sports Med 1997;18(1):47–55. [42] Zachwieja JJ, Ezell DM, Cline AD, Ricketts JC, Vicknair PC, Schorle SM, Ryan DH. Short-term dietary energy restriction reduces lean body mass but not performance in physically active men and women. Int J Sports Med 2001;22(4):310–6. [43] Jarvis M, McNaughton L, Seddon A, Thompson D. The acute 1-week effects of the Zone diet on body composition, blood lipid levels, and performance in recreational endurance athletes. J Strength Cond Res 2002;16(1):50–7. [44] Filaire E, Maso F, Degoutte F, Jouanel P, Lac G. Food restriction, performance, psychological state and lipid values in judo athletes. Int J Sports Med 2001;22(6):454–9. [45] American Dietetic Association, Dietitians of Canada, American College of Sports Medicine, Rodriguez NR, Di Marco NM, Langley S. American College of Sports Medicine position stand. Nutrition and athletic performance. Med Sci Sports Exerc 2009;41(3):709–31. [46] Heydenreich J, Kayser B, Schutz Y, Melzer K. Total energy expenditure, energy intake, and body composition in endurance athletes across the training season: a systematic review. Sports Med Open 2017;3(1). 8-017-0076-1. Epub 2017 Feb 4. [47] Horvath PJ, Eagen CK, Ryer-Calvin SD, Pendergast DR. The effects of varying dietary fat on the nutrient intake in male and female runners. J Am Coll Nutr 2000;19(1):42–51. [48] Helge JW, Richter EA, Kiens B. Interaction of training and diet on metabolism and endurance during exercise in man. J Physiol 1996;492(Pt 1):293–306. [49] Phillips SM. Dietary protein requirements and adaptive advantages in athletes. Br J Nutr 2012;108(Suppl 2):S158–67. [50] Clarkson PM. Antioxidants and physical performance. Crit Rev Food Sci Nutr 1995;35(1–2):131–41. [51] Ji LL. Oxidative stress during exercise: implication of antioxidant nutrients. Free Radic Biol Med 1995;18(6):1079–86. [52] Polidori MC, Mecocci P, Cherubini A, Senin U. Physical activity and oxidative stress during aging. Int J Sports Med 2000;21(3):154–7. [53] Lukaski HC. Vitamin and mineral status: effects on physical performance. Nutrition (Burbank Los Angel County Calif) 2004;20(7–8):632–44. [54] Volpe S. Vitamins, minerals and exercise. In: Dunford M, editor. Sports nutrition: a practice manual for professionals. Chicago: American Dietetic Association; 2006. p. 61–3. [55] Muoio DM, Leddy JJ, Horvath PJ, Awad AB, Pendergast DR. Effect of dietary fat on metabolic adjustments to maximal VO2 and endurance in runners. Med Sci Sports Exerc 1994;26(1):81–8. [56] Jacobs I, Lithell H, Karlsson J. Dietary effects on glycogen and lipoprotein lipase activity in skeletal muscle in man. Acta Physiol Scand 1982;115(1):85–90. [57] Kiens B, Essen-Gustavsson B, Gad P, Lithell H. Lipoprotein lipase activity and intramuscular triglyceride stores after long-term high-fat and high-carbohydrate diets in physically trained men. Clin Physiol (Oxf Engl) 1987;7(1):1–9. [58] Lithell H, Karlstrom B, Selinus I, Vessby B, Fellstrom B. Is muscle lipoprotein lipase inactivated by ordinary amounts of dietary carbohydrates? Hum Nutr Clin Nutr 1985;39(4):289–95. [59] Kiens B. Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol Rev 2006;86(1):205–43. [60] Watt MJ, Heigenhauser GJ, Spriet LL. Intramuscular triacylglycerol utilization in human skeletal muscle during exercise: is there a controversy? J Appl Physiol (Bethesda Md 1985) 2002;93(4):1185–95. [61] Kiens B, Richter EA. Utilization of skeletal muscle triacylglycerol during postexercise recovery in humans. Am J Physiol 1998;275(2 Pt 1):E332–7. [62] Starling RD, Trappe TA, Parcell AC, Kerr CG, Fink WJ, Costill DL. Effects of diet on muscle triglyceride and endurance performance. J Appl Physiol (Bethesda Md 1985) 1997;82(4):1185–9. [63] Decombaz J, Fleith M, Hoppeler H, Kreis R, Boesch C. Effect of diet on the replenishment of intramyocellular lipids after exercise. Eur J Nutr 2000;39(6):244–7. [64] Decombaz J, Schmitt B, Ith M, Decarli B, Diem P, Kreis R, Hoppeler H, Boesch C. Postexercise fat intake repletes intramyocellular lipids but no faster in trained than in sedentary subjects. Am J Physiol Regul Integr Comp Physiol 2001;281(3):R760–9. [65] Larson-Meyer DE, Newcomer BR, Hunter GR. Influence of endurance running and recovery diet on intramyocellular lipid content in women: a 1H NMR study, American journal of physiology. Endocrinol Metab 2002;282(1):E95–106. [66] Romijn JA, Coyle EF, Sidossis LS, Gastaldelli A, Horowitz JF, Endert E, Wolfe RR. Regulation of endogenous fat and carbohydrate metabolism in relation to exercise intensity and duration. Am J Physiol 1993;265(3 Pt 1):E380–91. [67] Spriet LL. New insights into the interaction of carbohydrate and fat metabolism during exercise. Sports Med (Auckl NZ) 2014;44(Suppl. 1):S87–96. [68] Shepherd SO, Cocks M, Tipton KD, Ranasinghe AM, Barker TA, Burniston JG, Wagenmakers AJ, Shaw CS. Sprint interval and traditional endurance training increase net intramuscular triglyceride breakdown and expression of perilipin 2 and 5. J Physiol 2013;591(3):657–75. [69] Tarnopolsky MA, Rennie CD, Robertshaw HA, Fedak-Tarnopolsky SN, Devries MC, Hamadeh MJ. Influence of endurance exercise training and sex on intramyocellular lipid and mitochondrial ultrastructure, substrate use, and mitochondrial enzyme activity. Am J Physiol Regul Integr Comp Physiol 2007;292(3):R1271–8. [70] Watt MJ, Cheng Y. Triglyceride metabolism in exercising muscle. Biochim Biophys Acta 2017;1862(10 Pt B):1250–9. 5.  MINERALS AND SUPPLEMENTS IN MUSCLE BUILDING



[71] De Bock K, Dresselaers T, Kiens B, Richter EA, Van Hecke P, Hespel P. Evaluation of intramyocellular lipid breakdown during exercise by biochemical assay, NMR spectroscopy, and Oil Red O staining, American journal of physiology. Endocrinol Metab 2007;293(1):E428–34. [72] De Bock K, Richter EA, Russell AP, Eijnde BO, Derave W, Ramaekers M, Koninckx E, Leger B, Verhaeghe J, Hespel P. Exercise in the fasted state facilitates fibre type-specific intramyocellular lipid breakdown and stimulates glycogen resynthesis in humans. J Physiol 2005;564(Pt 2):649–60. [73] Stellingwerff T, Boon H, Gijsen AP, Stegen JH, Kuipers H, van Loon LJ. Carbohydrate supplementation during prolonged cycling exercise spares muscle glycogen but does not affect intramyocellular lipid use. Pflug Arch Eur J Physiol 2007;454(4):635–47. [74] Stellingwerff T, Boon H, Jonkers RA, Senden JM, Spriet LL, Koopman R, van Loon LJ. Significant intramyocellular lipid use during prolonged cycling in endurance-trained males as assessed by three different methodologies, American journal of physiology. Endocrinol Metab 2007;292(6):E1715–23. [75] van Loon LJ, Koopman R, Stegen JH, Wagenmakers AJ, Keizer HA, Saris WH. Intramyocellular lipids form an important substrate source during moderate intensity exercise in endurance-trained males in a fasted state. J Physiol 2003;553(Pt 2):611–25. [76] Hooper L, Abdelhamid A, Bunn D, Brown T, Summerbell CD, Skeaff CM. Effects of total fat intake on body weight. Cochrane Database Syst Rev 2015;(8):CD011834. [77] Hu T, Mills KT, Yao L, Demanelis K, Eloustaz M, Yancy Jr WS, Kelly TN, He J, Bazzano LA. Effects of low-carbohydrate diets versus low-fat diets on metabolic risk factors: a meta-analysis of randomized controlled clinical trials. Am J Epidemiol 2012;176(Suppl. 7):S44–54. [78] Mansoor N, Vinknes KJ, Veierod MB, 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(3):466–79. [79] Krieger JW, Sitren HS, Daniels MJ, Langkamp-Henken B. Effects of variation in protein and carbohydrate intake on body mass and composition during energy restriction: a meta-regression 1. Am J Clin Nutr 2006;83(2):260–74. [80] Hashimoto Y, Fukuda T, Oyabu C, Tanaka M, Asano M, Yamazaki M, Fukui M. Impact of low-carbohydrate diet on body composition: meta-analysis of randomized controlled studies. Obes Rev 2016;17(6):499–509. [81] Volek JS, Phinney SD, Forsythe CE, Quann EE, Wood RJ, Puglisi MJ, Kraemer WJ, Bibus DM, Fernandez ML, Feinman RD. Carbohydrate restriction has a more favorable impact on the metabolic syndrome than a low fat diet. Lipids 2009;44(4):297–309. [82] Yancy Jr WS, Olsen MK, Guyton JR, Bakst RP, Westman EC. A low-carbohydrate, ketogenic diet versus a low-fat diet to treat obesity and hyperlipidemia: a randomized, controlled trial. Ann Intern Med 2004;140(10):769–77. [83] Jabekk PT, Moe IA, Meen HD, Tomten SE, Hostmark AT. Resistance training in overweight women on a ketogenic diet conserved lean body mass while reducing body fat. Nutr Metab 2010;7. 17-7075-7-17. [84] Quann EE. Carbohydrate restricted diets and resistance training: a powerful combination to enhance body composition and improve health. ACSM’s Certif News 2008;18:4. [85] Wilson JM, Lowery RP, Roberts MD, Sharp MH, Joy JM, Shields KA, Partl J, Volek JS, D’Agostino D. The effects of ketogenic dieting on body composition, strength, power, and hormonal profiles in resistance training males. J Strength Cond Res 2017. JSC.0000000000001935. Epub ahead of print. [86] Aragon AA, Schoenfeld BJ, Wildman R, Kleiner S, VanDusseldorp T, Taylor L, Earnest CP, Arciero PJ, Wilborn C, Kalman DS, Stout JR, Willoughby DS, Campbell B, Arent SM, Bannock L, Smith-Ryan AE, Antonio J. International society of sports nutrition position stand: diets and body composition. J Int Soc Sports Nutr 2017;14. 16-017-0174-y. eCollection 2017. [87] Arciero PJ, Edmonds RC, Bunsawat K, Gentile CL, Ketcham C, Darin C, Renna M, Zheng Q, Zhang JZ, Ormsbee MJ. Protein-pacing from food or supplementation improves physical performance in overweight men and women: the PRISE 2 study. Nutrients 2016;8(5). https:// [88] Arciero PJ, Ormsbee MJ, Gentile CL, Nindl BC, Brestoff JR, Ruby M. Increased protein intake and meal frequency reduces abdominal fat during energy balance and energy deficit. Obesity (Silver Spring Md) 2013;21(7):1357–66. [89] Layman DK, Evans E, Baum JI, Seyler J, Erickson DJ, Boileau RA. Dietary protein and exercise have additive effects on body composition during weight loss in adult women. J Nutr 2005;135(8):1903–10. [90] Layman DK, Evans EM, Erickson D, Seyler J, Weber J, Bagshaw D, Griel A, Psota T, Kris-Etherton P. A moderate-protein diet produces sustained weight loss and long-term changes in body composition and blood lipids in obese adults. J Nutr 2009;139(3):514–21. [91] Wycherley TP, Moran LJ, Clifton PM, Noakes M, Brinkworth GD. Effects of energy-restricted high-protein, low-fat compared with standardprotein, low-fat diets: a meta-analysis of randomized controlled trials. Am J Clin Nutr 2012;96(6):1281–98. [92] Abbott WG, Howard BV, Ruotolo G, Ravussin E. Energy expenditure in humans: effects of dietary fat and carbohydrate. Am J Clin Nutr 1990;258(2 Pt 1):E347–51. [93] Brehm BJ, Spang SE, Lattin BL, Seeley RJ, Daniels SR, D’Alessio DA. The role of energy expenditure in the differential weight loss in obese women on low-fat and low-carbohydrate diets. J Clin Endocrinol Metab 2005;90(3):1475–82. [94] Feinman RD, Fine EJ. Thermodynamics and metabolic advantage of weight loss diets. Metab Syndr Relat Disord 2003;1(3):209–19. [95] Volek JS, Sharman MJ, Love DM, Avery NG, Gomez AL, Scheett TP, Kraemer WJ. Body composition and hormonal responses to a carbohydrate-restricted diet. Metab Clin Exp 2002;51(7):864–70. [96] Jensen MD, Caruso M, Heiling V, Miles JM. Insulin regulation of lipolysis in nondiabetic and IDDM subjects. Diabetes 1989;38(12):1595–601. [97] Hall KD, Guo J. Obesity energetics: body weight regulation and the effects of diet composition. Gastroenterology 2017;152(7):1718–27.e3. [98] 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. Metab Clin Exp 1983;32(8):769–76. [99] Goedecke JH, Christie C, Wilson G, Dennis SC, Noakes TD, Hopkins WG, Lambert EV. Metabolic adaptations to a high-fat diet in endurance cyclists. Metab Clin Exp 1999;48(12):1509–17. [100] Burke LM, Angus DJ, Cox GR, Cummings NK, Febbraio MA, Gawthorn K, Hawley JA, Minehan M, Martin DT, Hargreaves M. Effect of fat adaptation and carbohydrate restoration on metabolism and performance during prolonged cycling. J Appl Physiol (Bethesda Md 1985) 2000;89(6):2413–21. [101] Carey AL, Staudacher HM, Cummings NK, Stepto NK, Nikolopoulos V, Burke LM, Hawley JA. Effects of fat adaptation and carbohydrate restoration on prolonged endurance exercise. J Appl Physiol (Bethesda Md 1985) 2001;91(1):115–22. [102] Lambert EV, Goedecke JH, Zyle C, Murphy K, Hawley JA, Dennis SC, Noakes TD. High-fat diet versus habitual diet prior to carbohydrate loading: effects of exercise metabolism and cycling performance. Int J Sport Nutr Exerc Metab 2001;11(2):209–25.




[103] Burke LM, Hawley JA, Angus DJ, Cox GR, Clark SA, Cummings NK, Desbrow B, Hargreaves M. Adaptations to short-term high-fat diet persist during exercise despite high carbohydrate availability. Med Sci Sports Exerc 2002;34(1):83–91. [104] Cameron-Smith D, Burke LM, Angus DJ, Tunstall RJ, Cox GR, Bonen A, Hawley JA, Hargreaves M. A short-term, high-fat diet up-regulates lipid metabolism and gene expression in human skeletal muscle. Am J Clin Nutr 2003;77(2):313–8. [105] Havemann L, West SJ, Goedecke JH, Macdonald IA, St Clair Gibson A, Noakes TD, Lambert EV. Fat adaptation followed by carbohydrate loading compromises high-intensity sprint performance. J Appl Physiol (Bethesda Md 1985) 2006;100(1):194–202. [106] 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, American journal of physiology. Endocrinol Metab 2006;290(2):E380–8. [107] Yeo WK, Lessard SJ, Chen ZP, Garnham AP, Burke LM, Rivas DA, Kemp BE, Hawley JA. Fat adaptation followed by carbohydrate restoration increases AMPK activity in skeletal muscle from trained humans. J Appl Physiol (Bethesda Md 1985) 2008;105(5):1519–26. [108] Burke LM, Ross ML, Garvican-Lewis LA, Welvaert M, Heikura IA, Forbes SG, Mirtschin JG, Cato LE, Strobel N, Sharma AP, Hawley JA. Low carbohydrate, high fat diet impairs exercise economy and negates the performance benefit from intensified training in elite race walkers. J Physiol 2017;595(9):2785–807. [109] 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. Metab Clin Exp 2016;65(3):100–10. [110] Yeo WK, Carey AL, Burke L, Spriet LL, Hawley JA. Fat adaptation in well-trained athletes: effects on cell metabolism. Appl Physiol Nutr Metab (Physiologie appliquee, nutrition et metabolisme) 2011;36(1):12–22. [111] Fisher EC, Evans WJ, Phinney SD, Blackburn GL, Bistrian BR, Young VR. In: Knuttgen HG, Vogel JA, Poortmans J, editors. Changes in skeletal muscle metabolism induced by a eucaloric ketogenic diet in Biochemistry of exercise. Champaign: Human Kinetics; 1993. p. 497–501. [112] Zinn C, Wood M, Williden M, Chatterton S, Maunder E. Ketogenic diet benefits body composition and well-being but not performance in a pilot case study of New Zealand endurance athletes. J Int Soc Sports Nutr 2017;14. 22-2017-0180-0. eCollection 2017. [113] 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(7):2493–508. [114] Spriet LL. Regulation of skeletal muscle fat oxidation during exercise in humans. Med Sci Sports Exerc 2002;34(9):1477–84. [115] Bentley DJ, Millet GP, Vleck VE, McNaughton LR. Specific aspects of contemporary triathlon: implications for physiological analysis and performance. Sports Med (Auckl NZ) 2002;32(6):345–59. [116] Fernandez-Garcia B, Perez-Landaluce J, Rodriguez-Alonso M, Terrados N. Intensity of exercise during road race pro-cycling competition. Med Sci Sports Exerc 2000;32(5):1002–6. [117] Hawley JA, Leckey JJ. Carbohydrate dependence during prolonged, intense endurance exercise. Sports Med (Auckl NZ) 2015;45(Suppl. 1):S5–12. [118] Pilegaard H, Neufer PD. Transcriptional regulation of pyruvate dehydrogenase kinase 4 in skeletal muscle during and after exercise. Proc Nutr Soc 2004;63(2):221–6. [119] Gudiksen A, Bertholdt L, Stankiewicz T, Tybirk J, Plomgaard P, Bangsbo J, Pilegaard H. Effects of training status on PDH regulation in human skeletal muscle during exercise. Pflug Arch Eur J Physiol 2017;469(12):1615–30. [120] Burke LM. Re-examining high-fat diets for sports performance: did we call the ‘nail in the coffin’ too soon? Sports Med (Auckl NZ) 2015;45(Suppl. 1):S33–49. [121] Putman CT, Spriet LL, Hultman E, Lindinger MI, Lands LC, McKelvie RS, Cederblad G, Jones NL, Heigenhauser GJ. Pyruvate dehydrogenase activity and acetyl group accumulation during exercise after different diets. Am J Physiol 1993;265(5 Pt 1):E752–60. [122] Hawley JA, Hopkins WG. Aerobic glycolytic and aerobic lipolytic power systems. A new paradigm with implications for endurance and ultraendurance events. Sports Med (Auckl NZ) 1995;19(4):240–50. [123] 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 2012;9(1). 34-2783-9-34. [124] Sawyer JC, Wood RJ, Davidson PW, Collins SM, Matthews TD, Gregory SM, Paolone VJ. Effects of a short-term carbohydrate-restricted diet on strength and power performance. J Strength Cond Res 2013;27(8):2255–62. [125] Volek JS, Quann EE, Forsythe CE. Low-carbohydrate diets promote a more favorable body composition than low-fat diets. Strength Cond J 2010;1(32):42–7. [126] Rampinini E, Bishop D, Marcora SM, Ferrari Bravo D, Sassi R, Impellizzeri FM. Validity of simple field tests as indicators of match-related physical performance in top-level professional soccer players. Int J Sports Med 2007;28(3):228–35. [127] Spencer M, Bishop D, Dawson B, Goodman C. Physiological and metabolic responses of repeated-sprint activities:specific to field-based team sports. Sports Med (Auckl NZ) 2005;35(12):1025–44. [128] Bangsbo J. The physiology of soccer–with special reference to intense intermittent exercise. Acta Physiol Scand Suppl 1994;619:1–155. [129] Jeukendrup AE. Carbohydrate intake during exercise and performance. Nutrition (Burbank Los Angel County Calif) 2004;20(7–8):669–77. [130] Balsom PD, Wood K, Olsson P, Ekblom B. Carbohydrate intake and multiple sprint sports: with special reference to football (soccer). Int J Sports Med 1999;20(1):48–52. [131] Ekblom B. Applied physiology of soccer. Sports Med (Auckl NZ) 1986;3(1):50–60. [132] Krustrup P, Mohr M, Steensberg A, Bencke J, Kjaer M, Bangsbo J. Muscle and blood metabolites during a soccer game: implications for sprint performance. Med Sci Sports Exerc 2006;38(6):1165–74. [133] Saltin B. Metabolic fundamentals in exercise. Med Sci Sports 1973;5(3):137–46. [134] Souglis AG, Chryssanthopoulos CI, Travlos AK, Zorzou AE, Gissis IT, Papadopoulos CN, Sotiropoulos AA. The effect of high vs. low carbohydrate diets on distances covered in soccer. J Strength Cond Res 2013;27(8):2235–47. [135] Andersson HA, Randers MB, Heiner-Moller A, Krustrup P, Mohr M. Elite female soccer players perform more high-intensity running when playing in international games compared with domestic league games. J Strength Cond Res 2010;24(4):912–9. [136] Dellal A, Hill-Haas S, Lago-Penas C, Chamari K. Small-sided games in soccer: amateur vs. professional players’ physiological responses, physical, and technical activities. J Strength Cond Res 2011;25(9):2371–81. [137] Mohr M, Krustrup P, Andersson H, Kirkendal D, Bangsbo J. Match activities of elite women soccer players at different performance levels. J Strength Cond Res 2008;22(2):341–9. 5.  MINERALS AND SUPPLEMENTS IN MUSCLE BUILDING



[138] Mohr M, Krustrup P, Bangsbo J. Match performance of high-standard soccer players with special reference to development of fatigue. J Sports Sci 2003;21(7):519–528. [139] Fisher EC, Evans WJ, Phinney SD, Blackburn GL, Bistrian BR, Young VR. Changes in skeletal muscle metabolism induced by a eucaloric ketogenic diet. In: Knuttgen HG, Vogel JA, Poortmans J, editors. Biochemistry of exercise. Champaign, Ill: Human Kinetics; 1983. p. 497–501. [140] Lambert EV, Speechly DP, Dennis SC, Noakes TD. Enhanced endurance in trained cyclists during moderate intensity exercise following 2 weeks adaptation to a high fat diet. Eur J Appl Physiol Occup Physiol 1994;69(4):287–93. [141] Venkatraman JT, Feng X, Pendergast D. Effects of dietary fat and endurance exercise on plasma cortisol, prostaglandin E2, interferon-g and lipid peroxides in runners. J Am Coll Nutr 2001;20(5):529–36. [142] Rowlands DS, Hopkins WG. Effects of high-fat and high-carbohydrate diets on metabolism and performance in cycling. Metabolism 2002;51(6):678–90.