REVIEW ARTICLE

Sports Medicine 14 (I): 27-42. 1992 0112.1642/92/0007.0027/$08.00/0 © Adis International Limited. All rights reserved. SP01147

Oxidation of Carbohydrate Ingested During Prolonged Endurance Exercise John A. Hawley, Steven C. Dennis and Timothy D. Noakes MRC/UCT Bioenergetics of Exercise Research Unit, Department of Physiology, University of Cape Town Medical School, Observatory, South Africa

Contents 27 28 30 30 30 32 32 32 33 34 34 36 36 36 36 37 38 39 39

Summary

Summary l. Historical Development 2. Fuel Stores of the Body 3. Gastric Emptying of fluids 4. Carbohydrate Digestion and Absorption 5. Methods of Quantifying Ingested Carbohydrate Oxidation During Exercise 5.1 Respiratory Exchange Ratio 5.2 Naturally Labelled I3C-Enriched Carbohydrates 5.3 Radioactive 14C-Labelled Carbohydrates 6. Oxidation of Glucose Ingested During Exercise 6.1 Effects of Feeding Schedule 6.2 Effects of Glycogen Depletion and Fasting 6.3 Effects of Exercise Intensity 7. Oxidation of Carbohydrates Other than Glucose 7.1 Fructose 7.2 Maltose 7.3 Sucrose 7.4 Glucose Polymer 8. Practical Implications and Guidelines for the Athlete

Classic studies conducted in the 1920s and 1930s established that the consumption of a high carbohydrate (CHO) diet before exercise and the ingestion of glucose during exercise delayed the onset of fatigue, in part by preventing the development of hypoglycaemia. For the next 30 to 40 years, however, interest in CHO ingestion during exercise waned. Indeed, it was not until the reintroduction of the muscle biopsy technique into exercise physiology in the 1960sthat a series of studies on CHO utilisation during exercise appeared. Investigations by Scandinavian physiologists showed that muscle glycogen depletion during prolonged exercise coincided with the development of fatigue. Despite this finding, attempts to delay fatigue during prolonged exercise focused principally on techniques that would increase muscle glycogen storage be/ore exercise. The possibility that CHO ingestion during exercise might also delay the development of muscle glycogendepletion and hence, at least potentially, fatigue, was not extensively investigated. This, in part, can be explained by the popular belief that water replacement to prevent dehydration and hyperthermia was of greater importance than CHO replacement during prolonged exercise.

Sports Medicine 14 (1) 1992

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This position was strengthened by studies in the early 1970s which showed that the ingestion of CHO solutions delayed gastric emptying compared with water, and might therefore exacerbate dehydration. As a result, athletes were actively discouraged from ingesting even mildly concentrated (>S g/100ml) CHO solutions during exercise. Only in the early 1980s, when commercial interest in the sale of CHO products to athletes was aroused, did exercise physiologists again begin to study the effects of CHO ingestion during exercise. These studies soon established that CHO ingestion during prolonged exercise could delay fatigue; this finding added urgency to the search for the optimum CHO type for ingestion during exercise. Whereas in the earlier studies, estimates of CHO oxidation were made using respiratory gas exchange measurements, investigations since the early 1970s have employed stable I3C and radioactive 14Cisotope techniques to determine the amount of ingested CHO that is oxidised during exercise. Most of the early interest was in glucose ingestion during exercise. These studies showed that significant quantities of ingested glucose can be oxidised during exercise. Peak rates of glucose oxidation occur ~7S to 90 minutes after ingestion and are unaffected by the time of glucose ingestion during exercise. Rates of oxidation also appear not to be influenced to a major extent by the use of different feeding schedules. Irrespective of whether subjects ingest glucose as single or multiple feedings, around 20g of glucose is oxidised in the first hour of exercise. Since repetitive feedings would be expected to accelerate the rate of delivery of glucose from the stomach to the duodenum, the similar rates of ingested glucose oxidation after single and multiple feedings suggest that exogenous CHO oxidation may not be limited by the rate of gastric emptying. Instead, studies in which rates of both gastric emptying and of ingested CHO oxidation were measured have shown that ingested glucose oxidation in the first 60 to 90 minutes of exercise must be limited by factors distal to the stomach; that is, either by the rate of glucose absorption into the bloodstream, or by the rate of exogenous glucose oxidation by the active muscles. Other data, however, indicate that it is the rate of absorption of glucose into the bloodstream, rather than its oxidation by muscle, which limits the rate of exogenous CHO oxidation. Thus, in glycogen-depleted or fasted subjects exogenous CHO oxidation is not increased. Further, the rate of exogenous CHO oxidation plateaus when the exercise intensity increases above SO% of maximal oxygen consumption (V02max), suggesting that glucose delivery to the blood may be limiting. Comparisons between glucose and fructose ingested by fed subjects during exercise show that the rate of oxidation of fructose is less than that of glucose. Oxidation rates of ingested maltose, sucrose and glucose polymer solutions are very similar to those reported for glucose provided the CHO is ingested in sufficiently large volumes. The practical implications of these findings for optimal performance in endurance events are that athletes should be encouraged to maximise CHO delivery to the working muscles. This is best achieved by ingesting a pre-exercise bolus feeding (200 to 400ml) of a mildly concentrated (S to 7 g/100ml) long-chain glucose polymer solution, followed by repetitive, multiple feedings (100 to ISOml) of the same solution every 10 to IS minutes for the first 2 hours of prolonged exercise. Thereafter, athletes should ingest a single (200 to 300ml) bolus of a more concentrated (1S to 20 g/100ml) long-chain glucose polymer solution followed by 100 to ISOml of the same drink every 10 to IS minutes until the completion of exercise. This drinking pattern will ensure that both fluid and CHO delivery are maintained at rates necessary to sustain performance during the later stages of prolonged, exhaustive exercise.

1. Historical Development The importance of the body's carbohydrate (CHO) stores for the maintenance of CHO metabolism during prolonged exercise (>90 minutes) was first recognised by Levine et al. (1924). These

workers studied some of the participants in the 1923 Boston Marathon and observed a marked decline in plasma glucose concentrations in many of the runners after the race. They proposed that hypoglycaemia could explain the fatigue and poor physical condition of these runners. To test this pos-

Oxidation of Exogenous Carbohydrate

sibility they encouraged a number of competitors to consume CHO during the following year's marathon. This practice, in combination with a high CHO diet before the race, enhanced running performance and prevented hypoglycaemia (Gordon et al. 1925). This was probably the first study to suggest that fatigue could be postponed and performance improved by the ingestion of CHO during prolonged exercise at 60 to 75% of maximal oxygen consumption (V02max). The importance of CHO for improving work capacity was further demonstrated by Dill et al. (1932). They showed that when their dogs, Joe and Sally, ran without being fed CHO, they became hypoglycaemic and fatigued after 4 to 6 hours. However, when provided with CHO during exercise, the same dogs could run to 17 to 23 hours. In the classic studies of Christensen and Hansen (1939a,b,c), the essential role of CHO for the performance of prolonged exercise was verified. They showed that the ingestion of a large quantity of glucose (200g) at the point of exhaustion enabled subjects to perform an additional hour of exercise, a finding in agreement with an earlier study (Boje 1936). These investigations clearly established the importance ofCHO ingestion during prolonged exercise. It was not until the 1960s when the percutaneous needle muscle biopsy technique was reintroduced, that studies of CHO utilisation during exercise again became popular (Ahlborg et al. 1967; Bergstrom & Hultman 1966, 1967; Bergstrom et al. 1967; Hermansen et al. 1967). Hermansen et al. (1967) showed that fatigue during prolonged exercise coincided with the near total depletion of muscle glycogen stores. Yet, despite the apparent association between the depletion of body CHO stores and fatigue, interest for the next decade focused on the importance of fluid rather than CHO replacement (Noakes 1991a). The results of Wyndham and Strydom (1969) and Costill and Saltin (1974) promoted the concept that fluid replacement alone was of primary importance for optimising performance during prolonged exercise. Because CHO ingestion delayed gastric emptying (Costill & Saltin 1974), water, in large volumes,

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was considered to be the optimal fluid replacement beverage for ingestion during endurance exercise. The findings of the pioneering studies of the 1920s and 1930s, which clearly showed the benefit of ingesting CHO during prolonged exercise, were largely ignored (Noakes 1991a). Despite some lone voices in the wilderness which suggested that the performance of trained athletes could be improved by the ingestion of CHO during prolonged exercise (Noakes et al. 1983), the question of whether water or CHO replacement should be emphasised was not fully resolved until the end of the 1980s. At that time, commercial interest revived research into the value of CHO ingestion during exercise; whereas water has no commercial value, CHO added to water can be marketed to millions of athletes worldwide. The modern studies of Coyle et al. (1983, 1986) and Coggan and Coyle (1987, 1988, 1989) marked the re-emergence of investigations into CHO metabolism during exercise and, in particular, the role of exogenous CHO ingestion. These researchers demonstrated that fatigue during prolonged exercise could be postponed by the ingestion of CHO. They established that premature fatigue during prolonged exercise of moderate intensity was due to the effect of low muscle glycogen content, hypoglycaemia and a reduced rate of CHO oxidation. They observed that CHO feedings during prolonged exhaustive exercise maintained norrnoglycaemia and high rates of CHO oxidation, and delayed the onset of fatigue. For a more comprehensive commentary on these studies the reader is referred to the recent review of Coggan and Coyle (1991). These findings were the stimulus for the recent interest in the formulation of the optimal CHO solution for ingestion during prolonged exercise (Flynn et al. 1987; Hawley et al. 1992; Massicotte et al. 1986, 1989; Mitchell et al. 1989a,b; Moodley et al. 1992; Sole & Noakes 1989). In a recent article in the Journal, the contribution of total plasma glucose oxidation to energy supply during prolonged exercise was reviewed (Coggan 1991). Here we supplement that review by analysing the data on ingested CHO oxidation dur-

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Sports Medicine 14 (1) 1992

ing prolonged exercise in humans. Investigations employing both stable (13C) and radioactive (14C) isotope techniques are discussed.

2. Fuel Stores of the Body It is generally accepted that endogenous CHO is an essential fuel for exercise of moderate to high intensity (Bergstromet al. 1967; CostillI984). CHO reserves, however, are limited. Most of the body's fuel is stored as fat. In a 70kg nonobese male, fat stores correspond to 586 MJ (140 000 kcal), whereas body CHO reserves correspond,to only 8.37 MJ (2000 kcal) [Felig & Wahren 1975]. CHO is stored principally as muscle and liver glycogen. The breakdown of muscle glycogen provides a direct source of energy for exercise, while the conversion of liver glycogen to glucose provides an additional fuel for the working muscles. Except in prolonged starvation during which the kidney produces glucose, the liver is the sole site of glucose production and release into the bloodstream. As moderate to high-intensity exercise of prolonged duration (3 to 4 hours) eventually depeletes endogenous CHO stores (Lamb & Brodowicz 1986), it has become common practice to ingest CHO during endurance exercise. Glucose absorbed from the gastrointestinal tract into the bloodstream spares liver glycogen (Bosch, personal communication) and increases endurance performance (Brooke et al. 1975; Coggan et al. 1987, 1988, 1989; Coyle et al. 1983, 1986; Millard-Stafford et al. 1990; Williams et al. 1990).

3. Gastric Emptying of Fluids It has been assumed that the rate of gastric emptying is the primary factor limiting the rate of CHO delivery to the blood and working muscles (Costill & Saltin 1974). Thus, there has been considerable emphasis on the effect of osmolality and energy content on the gastric emptying of ingested solutions (Costill 1990;Costill & Saltin 1974; Hunt & Pathak 1960; Hunt & Stubbs 1975). Solutions containing as little as 2.5 g/lOOml of CHO have

been shown to reduce the rate of gastric emptying (Costill & Saltin 1974; Coyle et al. 1978; Foster et al. 1980). Thus, in the late 1980s the practical advice to athletes was to ingest solutions with low « 2.5 g/lOOml) CHO content during prolonged exercise (American Collegeof Sports Medicine 1987). A number of recent studies, however, have shown that gastric volume may be a more important determinant of gastric emptying during exercise than either solute energy content or osmolality (Hawley et al. 1992; Mitchell et al. 1988, 1989b, 1991; Moodley et al. 1992; Noakes et al. 1991 b; Owen et al. 1986; Rehrer et al. 1989, 1990b; Ryan et al. 1989;Sole & Noakes 1989).These studies have shown that the rates of gastric emptying for solutions with vastly different CHO contents are quite similar when they are ingested repeatedly during exercise (Noakes et al. 1991 b). For further details the reader may refer to the recent reviews of Costill (1990), Maughan (1991) and Noakes et al. (1991b).

4. Carbohydrate Digestion and Absorption Most of the CHO that is ingested by humans is in the form of plant starch. About 20% of starch comprises unbranched a-I ,4-linked polysaccharide chains, called amylose. The other 80% is branched a-I,4- and a-I,6-linked polysaccharide molecules of larger molecular weight, called amylopectin. In addition some CHO is also ingested in the form of di- and monosaccharides. Common disaccharides are sucrose and lactose and common monosaccharides are glucose and fructose. Digestion of starch is catalysed by the a-amylases that are present in saliva and in the pancreatic secretion that is delivered into the lumen of the duodenum. a-Amylases hydrolyse the a-I,4-links in the middle of the chain to produce maltose, maltotriose and a-I,6-branched limit dextrins (fig. 1). Maltose, maltotriose and branched-chain limit dextrins are then further broken down by a number of different oligosaccharidases that are attached to the microvillae of the intestinal villae of the jejunum and most of the ileum. Included among

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Oxidation of Exogenous Carbohydrate

Starch

Maltose

Maltotriose

Limit dextrin

Fig. 1. Digestion of amylopectin in starch. Open circles represent C6 glucose units.

these enzymes are: (a) ~-galactosidase, which cleaves lactose to galactose and glucose; (b) sucrose a-Dglucohydrolase, which hydrolyses both the a-l,6linkages of the branch limit dextrins and sucrose to fructose and glucose; and (c) exo-l,4-a-D-glucosidase, which catalyses the sequential release of terminal glucose units from the nonreducing end of linear oligosaccharides. Interestingly, the glucosidase enzymes are thought to be functionally linked to the glucose transporter in the luminal membranes of the columnar epithelial (absorptive) cells. Duodenal perfusion studies have shown that glucose released from infused maltose is more rapidly absorbed into the bloodstream than infused glucose (Jones et aI. 1983). Transport of glucose (and galactose) across the columnar epithelial cells occurs by a number of independent processes (Stevens et aI. 1984). Amongst the transport mechanisms are 2 Nat-dependent carriers on the luminal border. One has a relatively low external affinity for glucose (and galactose) and a high capacity of 2Na+(glucose or galactose transport. The other has a much higher external affinity for glucose (or galactose) but a relatively low transport capacity (fig. 2). When glucose concentrations in the gut become very high after a meal, some

glucose can also cross the brush border passively, that is, without being driven by the inward Na" gradient. Glucose entering the columnar epithelial cells is released into the bloodstream from the serosal border via a low affinity, very high capacity glucose transporter (fig. 2). This glucose transporter strongly resembles that present in other cell types, except that it is not insulin-sensitive. Some glucose (~20%) also enters the glycolytic pathway in the columnar epithelial cells and is released as lactate. Fructose is transported across the brush border by a separate carrier (fig. 3). Compared with the glucose transporters, the fructose carrier has a rather low overall capacity and is not dependent on Na". After an oral load of fructose, the portal blood carries first a fructose peak and then a peak of glucose derived from the fructose to glucose conversion in the columnar epithelial cells. As occurs after glucose ingestion, some of the ingested fructose is converted to lactate in the columnar epithelium. Fructose absorption is stimulated by the presence of glucose (Holdsworth & Dawson 1964). Once hexose and triose molecules from CHO digestion appear in the systemic circulation, they become available for use as fuels by the working

Lumen

Columnar epithelium

Serosa

2 Na" + glucose Glucose 2 Na + + glucose

Low affinity V. high capadty

Fig. 2. A scheme to illustrate the glucose transporters in the columnar epithelium of the small intestine. The presence of an 'unstirred water layer' complicates measurements of the binding affinities of these transporters for glucose.

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Sports Medicine 14 (1) /992

Lumen

Columnar epithelium

Serosa

Fructose (early)

Glucos e (late)

When steady-state conditions are attained during exercise, gas exchange measurements can be used to estimate the total CHO oxidised at any time, using the formula described by Consolazio et al. (1963): Total CHO oxidation = 4.55 VC02 - 3.21 V02 (Eq. I) where VC02 is the volume of C02 in the expired air measured in Lzmin, and V02 is oxygen uptake during the same period measured in the same units. 5.2 Naturally Labelled I3C-Enriched Carbohydrates

Fig. 3. A scheme to illustrate the fructose transporters in the columnar epithelium of the small intestine. Unlike the transport ofglucose, the transport of fructose is not dependent on sodium.

muscles. Techniques to monitor the oxidation of CHO are described below.

5. Methods of Quantifying Ingested Carbohydrate Oxidation During Exercise 5.1 Respiratory Exchange Ratio The respiratory exchange ratio (R), which is the ratio of C02 production to 02 consumption ("VC02/ V02), indicates the proportions of CHO and fat that are being oxidised. Whereas CHO oxidation alone gives an R value of 1.00, total dependence on fatty acid metabolism produces an R value of 0.70. R values, however, have to be interpreted with caution. First, there is the uncertainty of the contribution of amino acid oxidation to V02 and VC02 during prolonged exercise. Secondly, there is the question of the extent to which the rise in VC02 with increasing V02, especially during progressive exercise, is a respiratory compensation for the metabolic acidosis, displacing the plasma H+ + HC03 r=' C02 + H20 equilibrium to the right (Newsholme & Leech 1983).Thirdly, R values provide no indication of whether the CHO being oxidised comes from either ingested CHO or from the liver or muscle glycogen stores (fig. 4). When steady-state conditions are attained dur-

To investigate specifically the rate of oxidation of ingested CHO, isotopes must be added to the food or drink. One such isotope is 13C, which is naturally enriched in the CHO formed by photosynthesis in C4 plants, such as sugar cane, com and sorghum. In contrast to C3 plants which fix C02 directly onto 3-carbon 3-phosphoglycerate, C4 plants fix C02 into 3-phosphoglycerate via oxaloacetate in bundle-sheath cells. Investigations using naturally labelled [13C]glucose to determine the rate of oxidation of ingested CHO during prolonged exercise have been conducted by several groups (Jandrain et al. 1984, 1989; Krzentowski et al. 1984a,b; Lefebvre et al. 1975; Lefebvre 1979; Massicotte et al. 1986, 1989, 1990; Pallikarakis et al. 1986; Peronnet et al. 1990; Pimay et al. 1977a,b, 1982). Rates of ingested glucose oxidation were calculated from the VC02 and the y13C02/y12C02 ratio using the equivalent of equation 2 (section 5.3). Compared with the 14C isotope procedure (described later in section 5.3), 13C isotope studies have the advantage that subjects are not exposed to radioactivity and so they can be repeatedly tested. There are, however, several disadvantages; the relatively low 13C/12C enrichment necessitates corrections for the 13C that is present in all energyyielding substrates (Schoeller et al. 1980). Further, as the I3C enrichment of CHO is greater than that of fat (Jacobsen et al. 1970; Schoeller et al. 1984), any shift in the pattern of fuel utilisation will affect I3C02 production and thus complicate measurements of ingested CHO oxidation (Barstow et al.

Oxidation of Exogenous Carbohydrate

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value multiplied by 6, as there are 6 carbon atoms per molecule of monosaccharide absorbed into the blood; SACHO is the radioactivity in the ingested solution in dpm/rnl; CHOd is the CHO content of the drink in g/L; MWCHO is the molecular weight of the CHO; VC02 is the volume of expired C02 in L'min; and 1.35 is the number of grams of hexose oxidised to produce I L of C02. The advantage of using the 14C isotope rather than the 13C isotope is that there is virtually no naturally occurring background level of 14C that must be accounted for when calculating exogenous CHO oxidation (Wolfe et al. 1984). Further, the appearance of 14C in the blood can be used to estimate the rates of 14CHO appearance in the bloodstream; this gives an indirect measure of the rate of CHO digestion and absorption. It is only possible to determine the appearance of ingested 13C-Iabelled substrates in venous blood if the 13C enrichment is very high. However, as recently pointed out by Coggan and Coyle (1991), studies using [14C]glucose may still greatly underestimate the extent to which blood glucose is oxidised during exercise, because of the slow equilibration of 14C02 with the bicarbonate pool. Of course, the obvious disadvantage of using 14C is that it exposes the subject to radioactivity. The amounts of radioactivity, however, are minimal. Generally,

Oxidation of carbohydrate ingested during prolonged endurance exercise.

Classic studies conducted in the 1920s and 1930s established that the consumption of a high carbohydrate (CHO) diet before exercise and the ingestion ...
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