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Nutritional aspects in ultra-endurance exercise

Edith M. Peters
Purpose of review Despite much current debate regarding central and peripheral neural mechanisms which may be responsible for the onset of fatigue during prolonged exercise, maintenance of nutritional and hydration status remains critical for successful participation in ultra-endurance exercise. This review focuses on substrate and fluid homeostasis during ultra-endurance exercise and the use of nutritional supplementation both as ergogenic aid and to attenuate exercise-induced immunosuppression. Recent findings Current evidence continues to support mandatory high carbohydrate intakes (1) before the event to maximize muscle glycogen stores, (2) during the event to prevent hypoglycaemia and (3) after the event to optimize post-event repletion of endogenous carbohydrate stores. No consistent performance benefit has yet been shown following a high-fat diet. Greater utilization of intrafascicular triglyceride stores appears to account for additional fat utilization in females. Recent trends towards excessive fluid intake have resulted in frequent reports of hyponatraemic hyperhydration in ultra-distance athletes, with greater incidence in women than in men. Carbohydrate supplementation during the event attenuates immunosuppressive hormonal and cytokine responses to ultraendurance exercise, but may impair vitamin C absorption, while the ergogenic value of caffeine supplementation in ultraendurance performance is currently being questioned. Summary Meeting macronutrient and fluid intake demands remains an important priority for ultra-endurance athletes. Yet these athletes are reported to present with a high incidence of disordered eating patterns during periods of training, and excessive fluid replacement strategies have resulted in an increased incidence of water intoxication with resultant central nervous system dysfunction. Keywords ultra-endurance, carbohydrate, fat, fluid, hyponatraemia, caffeine, immunosuppression
Curr Opin Clin Nutr Metab Care 6:427434.
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Introduction
Ultra-endurance exercise is classied as prolonged exercise longer than 4 h in duration and most commonly involves running, skiing, cycling or swimming. The combination of endurance activities into multi-sport events such as Ironman ultra-distance triathalons, which consist of a 3.8 km swim, 180 km cycle and 42.2 km marathon run, have increased in popularity in the last 15 years. While cardiac oxygenation, work rate at the lactate turnpoint, maximum power output and economy of motion are important physiological variables inuencing endurance performance [1 . .], the duration, intensity and extreme environmental conditions encountered during ultra-endurance events combine to produce different physiological stresses to those encountered in shorter endurance exercise. Central regulation of neural recruitment of motor units is known to occur in response to signals which are currently thought to include changes in (1) body temperature, (2) blood volume, (3) size of the muscle glycogen stores, (4) blood glucose concentration [1 . .,2] and (5) in the case of exercise at altitude, tissue oxygenation [1 . .]. A critical component of successful participation in ultraendurance events is thus the availability of both adequate substrate stores and the maintenance of hydration balance. In addition, the use of possible nutritional ergogenic aids and attenuation of exerciserelated immunosuppression by nutritional supplementation are also the subject of much current research endeavour. This review will be restricted to a discussion of these four components of sports nutrition as they relate to ultra-endurance exercise.

Substrate utilization and repletion


The extreme daily kilojoule expenditures of ultraendurance events [35] require a signicant contribution from all macronutrient energy sources. Although fat oxidation provides the greatest relative contribution to energy expenditure during low to moderate intensities of exercise with a peak recently shown to occur at 64+4% VO2 max [6 .] and becomes increasingly important as an energy source as the duration of exercise increases [1 . .], it is well established that exercise can only be maintained for prolonged periods without the onset of fatigue if sufcient carbohydrate is available for combustion [4,5,7]. Despite occasional anecdotal reports of successful performance following high-fat diets [8] and the known metabolic benets of greater relative percentages of fat oxidation [9], ofcial dietary guidelines currently continue to recommend that carbohydrate
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2003 Lippincott Williams & Wilkins.

Department of Physiology, Nelson Mandela Faculty of Health Sciences, University of Natal, Durban, South Africa Correspondence to Dr Edith M. Peters-Futre PhD, Department of Physiology, Nelson Mandela Faculty of Health Sciences, University of Natal, Private Bag 7, Congella 4013, South Africa Tel: +27 31 260 4237; fax: +27 31 260 4455; e-mail: futree@nu.ac.za Current Opinion in Clinical Nutrition and Metabolic Care 2003, 6:427434
# 2003 Lippincott Williams & Wilkins 1363-1950

DOI: 10.1097/01.mco.0000078986.18774.90

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should be the main fuel consumed during ultraendurance exercise to supplement endogenous muscle and liver glycogen stores and maintain blood glucose concentrations [7]. Current recommendations regarding carbohydrate ingestion have recently been reviewed by Burke and Hawley [10]. Carbohydrate intakes in the diets of ultra-distance athletes range from 5 to 7 g/kg/day in regular diets during training to 710 g/kg/day during the 34 days prior to competition [7]. Ingestion of a pre-event meal containing carbohydrates with different glycaemic indices does not appear to affect subsequent blood glucose and insulin concentrations when 60 g of carbohydrate are ingested per hour during a 2.5 h event [11]. Current consensus favours addition of any palatable carbohydrate, in either liquid or solid form, at rates of 4080 g/h during prolonged running events [10] and more than 90 g/h during prolonged cycling events [12]. The use of carbohydrate in the form of glucose, maltose, fructose polymers, branched chain starches with high glycaemic indices in uid replacement beverages at a concentration of 7.512% are recommended in order to provide carbohydrate late in exercise as muscle and liver glycogen stores become depleted and the risk of hypoglycaemia is increased [13]. In view of limited endogenous carbohydrate stores, increasing reliance on fat oxidation during exercise remains a focus of attention in current research. While reduced lipolysis and fat oxidation following highcarbohydrate diets is well described [14], Burke et al. [15 . .] have shown that the greater rates of fat oxidation following high-fat diets can be maintained with increased carbohydrate availability during and directly before 2 h of cycling at 70% VO2 max, but without evidence of either improved or impaired performance during a subsequent 25 min time-trial. Examination of the potential benet of such a strategy for ultraendurance events lasting more than 4 h, such as the Ironman triathalon or Tour de France, is an important direction for future research. Much recent work has focused on gender differences in substrate utilization, with women showing a tendency to oxidize more lipid and less carbohydrate at a given workload than men [16]. Kimber et al. [17 .] found that nishing time in triathletes participating in an Ironman event (3.8 km swim, 180 km run, 42.2 km run) is inversely related to carbohydrate intake during the marathon run for males (r = 0.75, P50.05), but not for females. They suggest that although increasing carbohydrate ingestion during the run may be a useful strategy for improving Ironman performance in male triathletes, other factors including greater utilization of lipid stores, difculties associated with digesting and absorbing large

amounts of solid carbohydrate-containing foods and longer average nishing times may account for the absence of an inverse relationship between carbohydrate intake and race nishing times in females. This work relates well to the ndings of Paul et al. [18], which showed that despite increasing pre-exercise muscle glycogen stores in female trained cyclists, pre-event carbohydrate loading did not signicantly improve cycling time-trial performance during the follicular phase of the menstrual cycle. It is interesting that although Roepstorff et al. [19 .] were unable to show a difference between genders in the relative contribution from carbohydrate and lipid to the oxidative metabolism across the leg during submaximal exercise at the same relative workload, they did show greater use of intracellular triglycerides in females and hypothesized that men relied more on oxidation of triglycerides located between the active muscle bres. A further recent focus has been the inuence of age on substrate utilization during prolonged exercise. Although total carbohydrate ulilization has been found to be lower in boys than in men during 60 min of cycling at 70% of VO2 max, the relative oxidation of ingested carbohydrate is considerably higher in boys than in men [20 .]. Elderly individuals oxidize more glucose and less fat during moderate intensity exercise, but endurance training in elderly individuals has been shown to increase muscle respiratory capacity and increase reliance on fat oxidation [21]. This is supported by recent ndings [22 .] that in middle-aged men, endurance training results in reduced carbohydrate oxidation and increased insulin sensitivity during exercise of moderate intensity. In applying carbohydrate-loading principles to military service, Bell et al. [23 .] investigated the effects of commercial sports drinks versus light meal combat rations during a 2 h march followed by a 1 h run at 70% VO2 max and conrmed that the amount of calories ingested was related to exhaustion time and that commercial sports drinks could be used to replace light meal combat rations. In terms of post-exercise recovery time, the faster muscle glycogen stores can be replenished in the early hours of recovery from exercise, theoretically, the faster the recovery process [1 . .]. While low muscle glycogen content enhances the transcriptional activation of metabolic genes enhancing both glucose uptake and glycogen synthetase activity during the initial few hours of recovery [24 . .], it is well established that the sooner and more frequently after exercise carbohydrate is consumed, the greater the rate of post-exercise muscle glycogen resynthesis [25]. Supplementing at 30 min intervals at a rate of 1.21.5 g carbohydrate/kg body mass/h has, for example, been shown to

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maximize glycogen resynthesis during the rst 45 h following exercise [26]. Ivy et al. [27 . .], however, have shown that a carbohydrateprotein supplement (80 g carbohydrate, 28 g protein, 6 g fat) is more effective for the rapid replenishment of muscle glycogen than a carbohydrate supplement of equal caloric value or equal carbohydrate content if provided immediately after and 2 h after exercise. An added benet of this combined carbohydrateprotein supplementation regime would be the stimulation of amino acid transport, protein synthesis and muscle tissue repair. Use of a proteincarbohydrate compound, however, has not been shown to be as effective as very large doses of carbohydrate provided at more frequent intervals (such as every 15 min), in replenishing muscle glycogen stores [28]. Despite the attention given in the literature to methods of optimizing substrate availability to muscle during and after prolonged exercise, DiGioacchino DeBate et al. [29 .], in the largest survey conducted on the eating patterns of 583 male and female ultra-distance triathletes to date, found that 28% of females and 11% of males scored below the mid-point range for the Eating Attitude Test-26 construct, Preoccupation with Food and Weight, and 39% and 23% of females and males, respectively, scored below the midpoint range for the construct, Calorie Control. The triathalon has been identied as a multi-sport event that is susceptible to a high prevalence of disordered eating with subclinical eating disorder characteristics among both male and female athletes. Besides excessive preoccupation with body weight and an intense fear of gaining weight and dissatisfaction with body size, the triathletes also revealed attempts to reduce body weight by means of energy restriction, severe limitation of food groups and excessive exercise (71%). Only 26% of the female and male triathletes met the recommended intakes for bread, cereal, rice and pasta, resulting in a carbohydrate intake below that recommended for healthy, active persons. This supports previous ndings indicating kilojoule intakes in the usual, in-training diets of ultra-marathoners ranging between 8.2 and 23.3 MJ/day [30,31]. It is of concern that ultra-distance athletes have thus been identied as a high-risk group for the onset and maintenance of disordered eating. While an open area for future research is an analysis of physical and biochemical characteristics of these athletes including menstrual disorders and macro and micronutrient status, the emphasis currently appears to be shifting towards greater focus on nutritional education and counseling for individual athletes to ne-tune their eating habits appropriately.

Maintenance of hydration balance


A vibrant area of sports nutrition research in recent years has been that of uid replacement and maintenance of appropriate hydration balance in ultra-endurance exercise. Much concern initially revolved around dehydration following intense, short-term exercise, showing that cognitive function and physical work capacity are impaired once the body water decit exceeds 2% of body weight [32]. Recent work, however, has focused on the high incidence of uid overload and symptomatic exercise-induced hyponatraemia following ultra-endurance events [3335]. The American College of Sports Medicines current position statement on uid intake during exercise recommends intake of 6001200 ml/h palatable, cooled uid (15228C) containing 45% carbohydrate and 0.5 0.7 g/l of sodium in events greater than 1 h in duration [36]. Recent research ndings are, however, questioning the appropriateness of these recommendations. The volume is considered too high for ultra-distance athletes competing at relatively low intensities or for smaller athletes with relatively low metabolic and sweat rates during exercise. It has also been emphasized that female ultra-distance athletes may have lower uid requirements and are at signicantly greater risk of developing hyponatraemia due to uid overload [33] in ultradistance triathalons than are average men [35]. This is thought to be due to (1) lower sweat rates as they are usually smaller and have smaller uid compartments, and (2) the longer time taken by women to complete events [33]. Exercise-induced hyponatraemia is currently one of the most commonly reported medical complications reported following ultra-distance triathalons [37,38]. In the 1998 New Zealand Ironman Triathalon, 18% of nishers were diagnosed with hyponatraemia [39]. While recent studies have not shown a signicant inverse relationship between body weight changes and post-race rectal temperature or impaired performance [1 . .,40,41 .], a number of reports show a clear inverse correlation between actual body weight changes and serum sodium concentrations during and after an Ironman triathalon (3.8 km swim, 180 km cycle, 42.2 km run), with athletes who gain weight during the race presenting with the greatest reduction in serum sodium concentrations [41 .,42]. The reduced uid requirements during very prolonged exercise are, however, not simply the result of reduced sweat rates and are not always well correlated with weight loss data. For example, participants in an Ironman triathalon presented with a mean weight loss of 2.8 kg, but a 10.8% mean increase in plasma volume and a 28% incidence of hyponatraemia ([Na]

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128133 mmol/l) [42]. Following an ultra-distance triathalon twice the length of an Ironman triathalon, a mean plasma volume increase of 15.4% was recently reported [43]. This supports numerous data which we have in our own laboratory of plasma volume increases of more than 10% following participation in a 90 km ultramarathon event (E.M. Peters, V. Jogessar, unpublished data). While weight loss includes the loss due to oxidation of fat and glycogen and release of metabolic water stored with glycogen, which has been estimated to account for up to 2 kg [44], an increase in plasma volume may, in addition to the reduced diuresis induced by activation of vasopressin secretion and the angiotensin reninaldosterone mechanism during exercise, occur due to the decrease in intracellular osmolytes including glycogen, proteins and triglycerides, which results in a shift of water to the extracellular compartment during very prolonged exercise [42]. Alternatively, the possibility also exists that the commonly used plasma volume determination formula [45] may overestimate plasma volume increases as it does not adjust for intravascular haemolysis [38,39]. While it is evident that weight changes before and after an ultra-distance event do not provide an accurate indication of hydration status, recent data appear to provide conclusive evidence that exercise-induced hyponatraemia is related to uid overload and is unrelated to sodium losses [33,35,41 .,42,46]. Ultra-distance athletes are therefore advised to adhere to more conservative uid intake volumes than their counterparts exercising more intensively for shorter periods. In Ironman triathalon events this recommendation is to limit uid intake to 500800 ml/h during the cycle and 300500 ml/h during the run, with lightweight men and women being advised to drink lower volumes. It is now accepted that 510% concentrations of glucose, glucose polymers (maltodextrins) and other simple sugars do not impair gastric emptying, making it possible to simultaneously achieve uid and carbohydrate requirements of endurance exercise [10]. Oral sodium supplementation has been associated with a slight, but statistically insignicant increase in [Na] concentration and a decrease in the extent of weight loss during an Ironman distance triathalon [47 .], indicating that it may have a role in maintaining hydration balance during ultradistance exercise. This, however, requires further conrmation. In terms of optimizing post-event uid replacement, Kovacs et al. [48 .] have conrmed earlier ndings [49] that gastric volume is the major factor inuencing gastric emptying rates during prolonged exercise. This showed that high volume (60%, 40%, 20% body mass loss in the rst, second and third hour) results in a faster rate of plasma volume and uid balance restoration in cyclists

following 3% body weight dehydration than lower ingestion rates (24% per hour for 5 h).

Ergogenic supplementation
The use of nutritional manipulations in an attempt to improve performance is persisting in current times. In addition to emphasis on carbohydrate and fat-loading (described above), the most recent ndings of interest to performance in ultra-endurance events have been those relating to the use of glycerol, caffeine and selected amino acids as possible performance enhancers. In a study examining the effects of prior glycerol loading on competitive Olympic distance triathalon performance in high and mild ambient temperatures [50 . .], ingestion of a 0.5 M glycerol solution containing 1.2 g of glycerol per kg body mass combined with 25 ml/kg body mass carbodydrate, over a 60 min period, 2 h prior to the event, resulted in a signicantly lower increase in triathalon completion time on the hot day than in a placebo group receiving 25 ml of a 0.75 g/kg body mass carbohydrate solution in the same environmental conditions. The glycerol loaded athletes also presented with reduced urinary output, greater uid retention and plasma volume, but without an increase in sweat loss. These results suggest that glycerol hyperhydration prior to Olympic distance triathalons in high ambient temperatures may provide protection against the negative performance effects of competing in the heat. Noakes [1 . .], however, warns of the likelihood of elite athletes using the increment in plasma volume (and reduced hematocrit) resulting from glycerol supplementation to mask erythropoietin use. Of particular interest to performance in ultra-endurance events is the previously well accepted fact that caffeine stimulates mobilization of fatty acids from fat tissue and can be used by endurance athletes to spare muscle glycogen [51]. Indeed, ingestion of between 3 and 6 mg/kg caffeine approximately 1 h before endurance cycling improved time to fatigue by 2050% [52]. Hunter et al. [53 . .], however, have more recently found that caffeine ingestion (6 mg/kg 60 min before and a caffeine maintenance dose of 0.33 mg/kg every 15 min) did not improve a 100 km time-trial performance. At present, the premise that caffeine may enhance time to fatigue by activating metabolic receptors in skeletal muscle, which slows the rate of muscle glycogen use [51], is being reexamined. Noakes [1 . .] postulates that the prolongation of fatigue may purely be due to stimulation of the release of central nervous system neurotransmitters and its ergogenic value in events longer than 1 h in duration is presently being questioned [1 . .]. Despite the present uncertainty surrounding the ergogenic value of caffeine for ultra-distance performance,

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recent research continues to focus on practical aspects pertaining to caffeine ingestion. As simultaneous caffeine and ephedrine ingestion have been shown to be associated with vomiting and nausea [54], Bell et al. [55] found that a dose of 5 mg/kg caffeine + 0.8 mg/kg ephredrine resulted in an ergogenic effect of similar magnitude with reduced incidence of side effects. In a subsequent study, Bell and McLellan [56 .] showed that both the duration and magnitude of the ergogenic effect that followed a 5 mg/kg dose of caffeine were greater in nonusers than in users, indicating an adaptive response to habitual intake. Mougios et al. [57 .] most recently found that ingestion of coffee containing 5 mg caffeine/ kg triggered a lower lipolytic response with no alterations in the ratio of unsaturated to saturated nonesteried fatty acids in human plasma. The potential ergogenic benets of amino acid ingestion is another area of recent research interest. While branched chain amino acid ingestion does not appear to affect fatigue during prolonged exercise, administration of 150 mg/kg body weight of monosodium glutamate resulted in increased glutamate availability during exercise with elevated plasma asparatate, taurine, alanine and insulin concentrations [58]. The practical implications of these ndings, however, require further examination. Although glutamine has been shown to stimulate muscle glycogen synthesis, its addition to carbohydrate supplements has not been shown to provide any additional benet over ingestion of carbohydrate alone [59 .].

triathalon not only attenuated the decline in plasma glutamine concentrations, but also the decline in mitogen-stimulated lymphocyte proliferation during exercise. Convincing evidence in favour of attentuation of exercise-induced immunosuppression following carbohydrate loading has been presented in the last decade. Bishop et al. [63,64], in two recent studies, have reported a reduction in post-exercise plasma cortisol and interleukin (IL)-6, IL-10 and IL-1ra concentrations, circulating neutrophil counts as well as lipopolysaccharide-stimulated neutrophil degranulation, conrming numerous earlier works of Nieman et al. [6567]. In addition to evidence of attenuation of post-exercise oxidative stress following an acute period of vitamin C supplementation [68,69], reductions in post-exercise serum cortisol, and plasma adrenaline, IL-10, and IL1ra concentrations [7072], plasma IL-6, monocyte respiratory burst and natural killer cell numbers [73], plasma malondialdehyde and IL-6 concentrations [74], tumour necrosis factor, IL-1b and IL-6 [75 .] and, in the most recent, as yet, unpublished work, neutrophil oxidative burst activity [76] have been reported in vitamin C supplemented athletes following endurance and ultra-endurance events. The role of vitamin C in attenuating apparent suppression of immune function following ultra-endurance exercise, has, however, not been conrmed in three recent studies performed on ultra-distance athletes [77,78,79 .]. Closer examination of the above-mentioned studies [6874,75 .,7678,79 .], however, reveals a discrepancy in the amounts of carbohydrate ingested before and during the exercise, which is conrmed by large variance in the plasma glucose concentrations. High blood glucose concentrations have not only been shown to reduce adrenal release of ascorbate into the circulation [80], but have also been shown to be a potent inhibitor of ascorbate uptake by a variety of different cell types, including immune and inammatory cells, as well as endothelial cells and intestinal brush vessels [81]. + L-Ascorbate transport is a Na dependent, electrogenic process which is known to be modulated by glucose; glucose has been shown to interfere with the ascorbate transporter from the internal side of the membrane [80]. The antagonistic effects of glucose on ascorbate absorption may therefore well account for the discrepancy in the ndings reported in recent studies. This potential vitamin Ccarbohydrate interaction during prolonged exercise is an important future research direction. At this stage, conclusive evidence therefore only exists in favour of exercise-induced suppression of immune function, following carbohydrate supplementation. The

Nutritional supplementation and attentuation of exercise-induced immunosuppression


Although there is no direct link between apparent increased susceptibility to infection following participation in ultra-endurance events and the formidable body of evidence which exists suggesting suppression of both innate and adaptive immune function during the 372 h following prolonged exercise [60], considerable attention has been paid to the effects of nutritional supplements in attenuating markers of post ultra-distance immunosuppression in recent years. At this stage there is little support from controlled studies to recommend glutamine for enhanced immune function. While it has been suggested that glutamine supplements may be benecial by maintaining the plasma glutamine concentration, hence fuelling macrophage and lymphocyte function, no effects on the exercise-induced fall in natural killer and lymphokineactivated killer cell activities or mitogen-stimulated lymphocyte proliferation have recently been found [61]. It is of interest that Bassit et al. [62 .], however, subsequently reported the novel nding that supplementation with branched chain amino acids prior to a

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12 Saris WHM, Goodplaster BH, Jeukendorp AE, et al. Endogenous carbohydrate oxidation from different carbohydrate sources during exercise. J Appl Physiol 1993; 75:21682172. 13 Saris WHM, van Erp-Baart MA, Brouns E, et al. Study on food intake and energy expenditure during extreme sustained exercise. The Tour de France. Int J Sports Med 1989; 10:S26S31. 14 Coyle EF, Jeukendorf AE, Oseto MC. Low fat diet alters intramuscular substrates and reduces lipolysis and fat oxidation during exercise. Am J Physiol Endocrinol Metab 2001; 280:E391E398.
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potential value of vitamin C, glutamine and branched chain amino acid supplementation are areas requiring further examination.

Conclusion
Meeting nutritional and uid intake demands is a rst priority to ultra-endurance athletes. Yet the literature is presenting a paradoxical image, both in terms of nutrient and uid intake. While enhanced energy and nutrient demands are critical, participants in ultra-distance exercise are reported to present with a high incidence of disordered eating patterns during periods of training, and while adequate uid replacement is essential, excessive uid replacement strategies have resulted in the incidence of hyponatraemic hyperhydration causing hyponatraemic encephalopathy and death. Despite well recognized potential hazards of chronically elevated blood glucose levels [82 .,83,84], the current evidence in support of attenuation of exercise-induced immunosuppression following carbohydrate supplementation is strong, while the value of current micronutrient and caffeine supplementation practices are, at this stage, uncertain.

15 Burke LM, Hawley JA, Angus DJ, et al. Adaptations to short term high fat diet persist during exercise despite high carbohydrate availability. Med Sci Sports Exerc 2002; 34:8391. This study established whether the metabolic adaptations of a 5-day high-fat diet would persist following a 36 h period of high carbohydrate availability before and during exercise when compared with those of an isoenergetic 5-day highcarbohydrate diet. The novel finding was that the carbohydrate-sparing effect of the high-fat diet persisted, but without a beneficial performance effect. 16 Tarnopolsky MA, Ruby BC. Sex differences in carbohydrate metabolism. Curr Opin Clin Nutr Metab Care 2001; 4:521526.

17 Kimber NE, Ross JJ, Mason SL, Speedy DB. Energy balance during an ironman triathlon in male and female triathletes. Int J Sport Nutr Exerc Metab 2002; 12:4762. Finishing time during the marathon run of an Ironman triathalon was inversely related to carbohydrate intake in males, suggesting greater value of carbohydrate ingestion during the run for males than females. 18 Paul DR, Mulroy SM, Horner JA, et al. Carbohydrate loading during the follicular phase of the menstrual cycle: effects on muscle glycogen and exercise performance. Int J Sport Nutr Exerc Metab 2001; 11:430441.

References and recommended reading


Papers of particular interest, published within the annual period of review, have been highlighted as: . of special interest .. of outstanding interest Noakes TD. Lore of running. 4th edition. London: Oxford University Press; 2002. Overviews current state of the knowledge regarding physiological and metabolic aspects of ultra-distance running including nutritional and fluid replacement considerations, ergogenic aids and related medical aspects. Highly recommended for both athlete and medical scientist interested in ultra-endurance exercise. 1 2 St Clair Gibson A, Schabort EJ, Noakes TD. Reduced neuromuscular activity and force generation during prolonged exercise. Am J Physiol Regul Integr Comp Physiol 2000; 281:R187R196. Hausswirth C, Lehenaff D. Physiological demands of running during long distance runs and triathlons. Sports Med 2000; 31:679689. Laursen PB, Rhodes EC. Factors affecting performance in an ultraendurance triathlon. Sports Med 2001; 31:195209. Burke LM. Nutritional practices of male and female endurance cyclists. Sports Med 2001; 31:521532.

19 Roepstorff C, Steffensen CH, Madsen M, et al. Gender differences in substrate utilization during submaximal exercise in endurance-trained subjects. Am J Physiol Endocrinol Metab 2002; 282:E435E447. In females, greater utilization of myocellular intramuscular triglycerides while in men, greater utilization of triglycerides located between the muscle fibres (intrafascicular) is suggested.

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20 Timmons BW, Bar-Or O, Riddel MC. Oxidation rate of exogenous carbohydrate during exercise is higher in boys than men. J Appl Physiol 2003; 94:278284. Good application of 13C stable isotope methodology to measure substrate utilization during exercise. It presents the novel finding that healthy young boys oxidize relatively more carbohydrate during 60 min of exercise than do healthy young men. 21 Mittendorfer B, Klein S. Effect of aging on glucose and lipid metabolism during endurance exercise. Int J Sports Nutr Exerc Metab 2001; 11 (Suppl):S86S91.

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22 Manetta J, Brun JF, Perez-Martin A, et al. Fuel oxidation during exercise in middle aged men: role of training and glucose disposal. Med Sci Sports Exerc 2002; 34:423429. Substrate utilization was evaluated using indirect calorimetry. Endurance training results in reduced carbohydrate oxidation and increased insulin sensitivity in middle-aged men during exercise of moderate intensity.

Achten J, Gleeson M, Jeukendrup AE. Determination of the exercise intensity that elicits maximal fat oxidation. Med Sci Sports Exerc 2002; 34:9297. Fat oxidation rates were estimated in 10 moderately trained men using indirect calorimetry during graded exercise (5 min bouts in 35 W increments) as well as four to six continuous prolonged exercise tests at constant work rates. 7 Burke LM, Cox GR, Culmmings NK, Desbrow B. Guidelines for daily carbohydrate intake: do athletes achieve them? Sports Med 2001; 31:267 299. Allen M. Training secrets from the Elite. In: Almanac B, Stevenson A, editors. The total triathalon. Palo Alto, CA: The Trimarket Company; 1996. pp. 86 98. Staudacher HM, Carey AL, Cummings NK, Hawley JA. Short term high fat diet alters substrate utilization during exercise, but not glucose tolerance in highly trained athletes. Int J Sports Nutr 2001; 11:273286.

23 Bell DG, McLellan TM, Boyne S. Commercial sports drinks versus light meal combat rations: effect on simulated combat maneuvers. Mil Med 2002; 167:692697. During simulated combat manoeuvres including a 2 hour march at 50% of maximal aerobic capacity, a subsequent 1-hour run at 70% VO2 max and a run to exhaustion at 80% VO2 max, three different commercial sports drinks were compared to a light meal combat ration in terms of the their effect on exhaustion time, O2 consumption, heart rate and rate of perceived exertion. 24 Pilegaard H, Keller C, Steensberg A, et al. Influence of pre-exercise muscle glycogen content on exercise-induced transcriptional regulation of metabolic genes. J Physiol 2002; 541:261271. Nuclei and RNA were isolated from biopsies obtained from the vastus lateralis muscle of nonexercised control and glycogen-depleted legs before and after 2.5 h of one-legged cycling. The possibility that signaling mechanisms sensitive to glycogen content and availability may be linked to the transcriptional control of exercise-responsive genes is suggested, supporting the central governor theory [1, . .2]. 25 Van Loon JC, Saris WHM, Kruijshoopoon M, et al. Maximising post exercise glycogen synthesis: carbohydrate supplementation and the application of amino acid and protein hydrolysate mixtures. Am J Clin Nutr 2001; 72:106 111.

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10 Burke LM, Hawley JA. Carbohydrate and exercise. Curr Opin Clin Nutr Metab Care 1999; 2:515520. 11 Burke LM, Claasen A, Hawley JA, Noakes TD. Carbohydrate intake during prolonged cycling minimizes the effect of glycaemic index of pre-exercise meal. J Appl Physiol 1998; 85:22202226.

26 Ivy JL. Dietary strategies to promote glycogen synthesis after exercise. Can J Appl Physiol 2001; 26 (Suppl):S236S245.

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27 Ivy JL, Goforth HW, Damon BM, et al. Early post exercise muscle glycogen recovery is enhanced with a carbohydrate-protein supplement. J Appl Physiol 2002; 93:13371344. Nuclear magnetic resonance spectroscopy was used to monitor muscle glycogen in vastus lateralis before and after an exercise protocol of more than 2 h designed to deplete liver glycogen stores in individuals studied on three separate occasions; after carbohydrate + protein, high-carbohydrate and low-carbohydrate diets. 28 Jentjens RLPG, Van Loon LJC, Mann CH, et al. Addition of protein and amino acids to carbohydrates does not enhance postexercise muscle glycogen resynthesis. J Appl Physiol 2001; 91:839846. 29 DiGioacchino DeBate R, Wethington H, Sargent R. Sub-clinical eating . disorder characteristics among male and female triathletes. Eat Weight Disord 2002; 7:210220. Scores for eating attitude test-26 (EAT-26) including constructs for preoccupation with food and weight and calorie control were obtained from 583 triathletes. 30 Singh A, Evans P, Gallager KL Deuster PA. Dietary intakes and biochemical profiles of nutritional status of ultra-marathoners. Med Sci Sports Exerc 1993; 25:328334. 31 Peters EM, Goeztske JM. Dietary practices of South African ultra-distance runners. Int J Sports Nutr 1997; 7:80103. 32 Sawka MN. Physiological consequences of hypohydration: exercise performance and thermoregulation. Med Sci Sports Exerc 1992; 24:657670. 33 Speedy DB, Noakes TD, Schneider C. Exercise-associated hyponatraemia: a review. Emerg Med 2001; 13:1727. 34 Hiller WDB, OToole ML, Massimimo F, et al. Plasma electrolyte status in athletes receiving medical care at an ultra-distance triathalon. Clin J Sports Med 1995; 5:116122. 35 Speedy DB, Noakes TD, Rodgers IR, et al. Hyponatraemia in ultradistance triathletes. Med Sci Sports Exerc 1999; 31:809815. 36 Convertino VA, Armstrong LE, Coyle EF, et al. The American College of Sports Medicine position stand: exercise and fluid replacement. Med Sports Sci Exerc 1996; 28:Ivii. 37 Laird RH. Medical care at ultra-endurance triathalons. Med Sci Sports Exerc 1989; 21 (Suppl):222225. 38 Speedy DB, Rogers IR, Noakes TD, et al. Diagnosis and prevention of hyponatraemia at an ultra-distance triathalon. Clin J Sports Med 2000; 10:5258. 39 Speedy DB, Noakes TD, Rogers IR, et al. Hyponatraemia in ultra-distance athletes. Med Sci Sports Exerc 1999; 31:809815. 40 Noakes TD, Myburg KH, Du Plessis J, et al. Metabolic rate, not percent dehydration, predict rectal temperature in marathon runners. Med Sports Sci Exerc 1990; 23:443449.
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50 Coutts A, Reaburn P, Mummery K, Holmes M. The effect of glycerol hyperhydration on Olympic distance triathalon performance in high ambient temperatures. Int J Sports Nutr Exerc Metab 2002; 12:519. Although conducted on an endurance distance event, this well regulated field work provides convincing evidence to support ergogenic effects and possible protective effects of glycerol loading prior to competing in heat stressful conditions. 51 Dodds SL, Herb RA, Powers SK. Caffeine and exercise performance: an update. Sports Med 1993; 15:1423. 52 Graham TE, Spriet LL. Performance and metabolic responses to a high caffeine dose during prolonged exercise. J Appl Physiol 1991; 71:2292 2298.

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53 Hunter AM, Gibson A, Collins M, et al. Caffeine ingestion does not alter performance during a 100-km cycling time-trial performance. Int J Sport Nutr Exerc Metab 2002; 12:438452. The effect of caffeine ingestion 60 min before (6 mg/kg) and a maintenance dose of 0.33 mg/kg every 15 min on electromyography amplitude and the mean power frequency spectrum was analysed in eight highly trained cyclists undergoing a 100 km time trial including 1 and 4 km bouts of high-intensity cycling. This outstanding work provides evidence that caffeine may be without ergonenic benefit during ultra-endurance exercise. 54 Bell DG, Jacobs I, Zamecnik J. Effects of caffeine, ephedrine and their combination on time to exhaustion during high intensity exercise. Eur J Appl Physiol 1998; 77:427433. 55 Bell DG, McLellanTM, Zamecnik J. Reducing the dose of combined caffeine and ephededrine preserves ergonenic effect. Aviat Space Environ Med 2000; 71:415419.

56 Bell DG, McLellan TM. Exercise endurance 1, 3, and 6 hours after caffeine ingestion in caffeine users and nonusers. J Appl Physiol 2002; 93:1227 1234. Investigated the ergogenic effects of caffeine on habitual and nonhabitual caffeine users to establish the difference following adaptation. 57 Mougios V, Ring S, Petridou A, et al. Duration of coffee and exercise induced changes in the fatty acid profile of human serum. J Appl Physiol 2003; 94:476484. Individual serum nonesterified fatty acid and triglyceride groups were determined by a combination of thin-layer chromatography and capillary gas chromatography. May be useful in elucidating mechanisms mediating the effects of exercise training on fatty acid metabolism. 58 Hargreaves MH, Snow R. Amino acids and endurance exercise. Int J Sports Nutr Exerc Metab 2001; 11:133145.

59 Mourtzakis M, Graham TE. Glutamate ingestion and its effects at rest and during exercise in humans. J Appl Physiol 2002; 93:12511259. Study on seven male subjects suggests that increased glutamate availability during exercise alters its distribution in transamination reactions. 60 Pedersen BK, Ullum HNK. Response to physical activity: possible mechanisms of action. Med Sci Sports Exerc 1994; 26:140144. 61 Krzywkowski K, Petersen EW, Ostrowski K, et al. Effect of glutamine supplementation on exercise-induced changes in lymphocyte function. Am J Physiol Cell Physiol 2001; 281:C1259C1265.

41 Sharwood K, Collins M, Goedecke J, et al. Weight changes, sodium levels, and performance in the South African Ironman triathlon. Clin J Sport Med 2002; 12:391399. Body mass changes, rectal temperature and performance time were related to post-race serum sodium concentrations in 356 triathletes. The findings support the theory that exercise-associated hyponatraemia results from fluid overload. 42 Speedy DB, Noakes TD, Kimber NE, et al. Fluid balance during and after an ironman triathlon. Clin J Sport Med 2001; 11:4450. 43 Gastman U, Dimeo F, Huonker M. Ultra-triathalon related blood-chemical and endocrinological responses in nine athletes. J Sports Med Phys Fitness 1988; 38:1823. 44 Brouns F. Heatsweatdehydrationrehydration: a praxis oriented approach. J Sports Sci 1991; 9:143152. 45 Dill DB, Costill DL. Calculation of percentage changes of blood, plasma and red cells in dehydration. J Appl Physiol 1974; 37:247248. 46 Speedy DB, Noakes TD, Boswell DR. Response to a fluid load in athletes with a history of exercise induced hyponatraemia. Med Sci Sports Exerc 2001; 33:14341442.

62 Bassit RA, Sawada LA, Bacurau RF, et al. Branched-chain amino acid supplementation and the immune response of long-distance athletes. Nutrition 2002; 18:376379. Decreased post-Olympic triathalon plasma glutamine concentrations attenuated by branched chain amino acid supplementation and increased IL-2 and interferon production by lymphocytes after exercise. 63 Bishop NC, Walsh NP, Haines DL, et al. Pre-exercise carbohydrate and immune responses to prolonged cycling: I. Effect on neutrophil degranulation. Int J Sports Nutr Exerc Metab 2001; 11:490502. 64 Bishop NC, Walsh NP, Haines DL, et al. Pre-exercise carbohydrate and immune responses to prolonged cycling: II. Effect on plasma cytokine concentration. Int J Sports Nutr Exerc Metab 2001; 11:503512. 65 Nieman DC, Nehlsen-Cannarella SL, Fagoaga OR, et al. Influence of mode and carbohydrate on the cytokine response to heavy exertion. Med Sci Sports Exerc 1998; 30:671678.

47 Speedy DB, Thompson JM, Rodgers I, et al. Oral salt supplementation during ultra-distance exercise. Clin J Sport Med 2002; 12:279284. Thirty-eight triathalon athletes given sodium supplementation and influences on changes in body weight, serum [Na] and plasma volume were monitored. 48 Kovacs EM, Schahl RM, Senden JM, Brouns F. Effect of high and low rates of fluid intake on post-exercise rehydration. Int J Sports Nutr Exerc Metab 2002; 12:1423. A faster rate of plasma volume and fluid balance restoration following ingestion of higher volumes (60%, 40%, 20% body mass) in the first 3 h of post-exercise recovery than 24% per hour during 5 h. 49 Noakes TD, Rehrer NJ, Maughan RJ. The importance of volume in regulating gastric emptying. Med Sci Sports Exerc 1991; 23:307313.

66 Nieman DC. Carbohydrates and the immune response to prolonged exertion. In: Nieman DC, Pederson BK, editors. Nutrition and exercise immunology. Florida: CRC Press; 2000. 67 Henson DA, Nieman DC, Nehlsen-Cannarella SL, et al. Influence of carbohydrate on cytokine and phagocytic responses to 2 h of rowing. Med Sci Sports Exerc 2000; 32:13841389. 68 Alessio HM, Goldfarb AH, Cao G. Exercise-induced oxidative stress before and after vitamin C supplementation. Med Sci Sports Exerc 1997; 25:208 214.

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69 Ashton T, Young IS, Peters JR, et al. Electron spin resonance spectroscopy, exercise, and oxidative stress: an ascorbic acid intervention study. J Appl Physiol 1999; 87:20322036. 70 Nieman DC, Peters EM, Henson DA, et al. Influence of vitamin C supplementation on cytokine changes following an ultra-marathon. J Interferon Cytokine Res 2000; 20:10291035. 71 Peters EM, Anderson R, Nieman DC, et al. Vitamin C supplementation attenuates the increases in circulating cortisol, adrenaline and antiinflammatory polypeptides following ultramarathon running. Int J Sports Med 2001; 22:537543. 72 Peters EM, Anderson R, Theron AJ. Attenuation of increase in circulating cortisol and enhancement of the acute phase protein response in vitamin Csupplemented ultra-marathoners. Int J Sports Med 2001; 22:120126. 73 Hurst TL, Bailey DM, Powell JR, Williams C. Immune function changes in downhill running subjects following ascorbic acid supplementation [abstract]. Med Sci Sports Exerc 2001; 33 (5 Suppl):251 74 Thompson D, Williams C, McGregor SJ, et al. Prolonged vitamin C supplementation and recovery from demanding exercise. Int J Sports Nutr 2001; 11:466481.
.

77 Pedersen EW, Ostrowski K, Ibfelt T, et al. The effect of vitamin supplementation on cytokine response and on muscle damage after exercise. Am J Physiol Cell Physiol 2001; 280:C1570C1575. 78 Nieman DC, Henson DA, Butterworth DE, et al. Vitamin C supplementation does not alter the immune response to 2.5 hours of running. Int J Sports Nutr 1997; 7:173184.
.

79 Nieman DC, Henson DA, McAnulty SR, et al. Influence of vitamin C supplementation on oxidative and immune changes after an ultra-marathon. J Appl Physiol 2002; 92:19701977. Placebo-controlled, vitamin C intervention field study performed on carbohydrate loaded runners. Lipid hydroperoxide, F2-isoprostane, immune cell counts, plasma IL-6, IL-10, IL-1-receptor antagonist, or IL-8 concentrations, or mitogen-stimulated lymphocyte proliferation and IL-2 and interferon-g production monitored before during and directly following participation in a 100 km ultramarathon. 80 Goralczyk R, Moser UK, Matter U, Weiser H. Regulation of steroid hormone metabolism requires L-ascorbic acid. Ann N Y Acad Sci 1992; 669:349351. 81 Malo C, Wilson JX. Glucose modulates vitamin C transport in adult human small intestinal brush border vesicles. J Nutr 2000; 130:6369.

75 Vassilakopoulos T, Karatza MH, Katsaounou P, et al. Antioxidants attenuate the plasma cytokine response to exercise in humans. J Appl Physiol 2003; 94:10251032. The effect of 60 days of anti-oxidant supplementation (200 mg vitamin E, 50 000 IU vitamin A, and 1000 mg vitamin C/day) was examined on untrained cyclists on tumor necrosis factor, IL-1b and IL-6 concentrations in both plasma (determined by enzyme-linked immunosorbent assay) and monocytes (determined by flow cytometry). 76 Robson PJ, Bouic PJ, Myburg KH. Antioxidant supplementation enhances neutrophil oxidative burst in trained runners following prolonged exercise. Int J Sports Nutr 2003; 24:(in press).

82 Umpierrez GE, Isaacs SD, Bazargan N, et al. Hyperglycemia: an independent marker of in-hospital mortality in patients with undiagnosed diabetes. J Clin Endocrinol Metab 2002; 87:978982. Newly-discovered hyperglycaemia was found to be an important marker of poor clinical outcome rate and a lower functional outcome and was associated with higher in-hospital mortality rate (16%). The hazards of glucotoxicity are highlighted. 83 Singh A, Falla Ml. Zinc supplementation. J Appl Physiol 1994; 76:2298 2303. 84 Nicollerat JA. Elevated plasma glucose levels increase risk for complications. Diabetes Educator 2000; 26 (Suppl):1113.