Carbohydrate during exercise: research of last 10 years turned into new recommendations

ASKER Jeukendrup

Gatorade Sports Science Institute, Barrington, IL, USA

School of Sport and Exercise Sciences

University of Birmingham, Edgbaston, Birmingham, UK

Introduction

We are all aware that carbohydrates and fats are the most important fuels during exercise. This has not always been the case. Till the late 1800s it was believed that protein was the most important source of energy for muscle. In the early 1900s it was discovered that not protein but carbohydrate was an important fuel for exercise [27]. In 1939 a paper was published that showed that carbohydrate use during exercise could be influenced by diet and that this could improve exer­cise tolerance [4]. In the 1960s it became clear that muscle glycogen played a significant role [2] and in the 1980s the first studies showed that carbohy­drate ingestion during exercise improved exercise capacity [5, 7]. In the years that followed the field did not advance much until 2004, which marked the beginning of a series of major breakthroughs with respect to car­bohydrate feeding during exercise. These break­throughs and their effects on sports nutrition guide­lines will be discussed in this review article.

As new information became available over time, recommendation for athletes evolved as well. Although on most recent guidelines, it is generally accepted that carbohydrate intake is important to optimise endurance performance, recommendations are not very specific [36]. For example, the most recent guidelines by the American College of Sports Medicine state that a carbohydrate intake of 30-60 grams per hour is recommended during exercise, but does not specify the type of activity, the level of athlete etc. Does this mean that these general recommen­dations are appropriate for everyone from recrea­tional football player to professional cyclist?

With the evidence from studies and new insights obtained in the last 5-10 years it is possible to provide much more prescriptive and precise advice to athletes. It is beyond the scope of this review to discuss all the underlying evidence in great detail, as this has been done in several other recent reviews [17, 19-21, 23], but the purpose of this review is to bring all the different pieces of infor­mation together and translate our current understan­ding into practical guidelines for athletes competing in different events.

Carbohydrate ingestion during exercise and performance

Although the exact mechanisms are still not completely understood, it has been known for some time that carbohydrate ingestion during exercise can increase exercise capacity and improve exer­cise performance [18, 19]. In general during exercise longer than 2 hours, carbohydrate feeding will prevent hypogly-caemia, will maintain high rates of carbohydrate oxi­dation and increase endurance capacity compared with placebo ingestion. As little as 20 g/h carbohy­drate is already sufficient to observe a performance benefit during prolonged exercise [12, 28]. It was be­lieved that the exercise duration had to be around 2h or longer for the carbohydrate feeding to be ef­fective.

However, more recently, it has become clear that also during shorter duration exercise of higher inten­sity (for example 1h around 75%VO₂max), carbohy­drate ingestion during exercise can improve perfor­mance. The mechanism behind these performance improvements is completely different. In fact it was demonstrated that when glucose was infused into the systemic circulation, this glucose was taken up at high rates but no performance effect was found. This provides evidence that increasing glucose availability, as a substrate to the working muscle, has no effect during this type of activity. Interesting­ly, however, when subjects rinsed their mouth with a carbohydrate solution this resulted in performance improvements [21] and these were similar to the improvements seen with carbohydrate ingestion. There are numerous studies now that confirm these initial findings. These studies are reviewed in several recent papers reviews [17, 19-21, 23]. This would suggest that the beneficial effects of carbohy­drate feeding during exercise are not confined to its conventional metabolic advantage but may also con­tribute top a more positive afferent signal capable of modifying motor output [14]. These effects are specific to carbohydrate and are independent of taste [3].

It is likely that receptors in the oral cavity me­diate these effects but such receptors have not yet been identified in humans and the exact role of various brain areas is not clearly understood. However, it has been convincingly demonstrated that carbohydrate is detected in oral cavity by uni­dentified receptors and this can be linked to im­provements in exercise performance [21]. New guide­lines suggested here take these findings into ac­count (Table 1).

Table 1. Carbohydrate intake recommendations during exercise for exercise of different durations

Practical implications of the mouth rinse studies

These results suggest that it is not necessary to ingest large amounts of carbohydrate during exer­cise lasting approximately 30 min to 1 hour and a mouth rinse with carbohydrate may be sufficient to get a performance benefit (Table 1). In most condi­tions the performance effects with the mouth rinse were similar to ingesting the carbohydrate drink, so there does not seem to be a disadvantage of con­suming the drink, although occasionally athletes may complain of gastro-intestinal distress when con­suming larger amounts. When the exercise is more prolonged (2h or more), carbohydrate becomes a very important fuel and to prevent a decrease in per­formance it is essential to ingest carbohydrate. As will be discussed below, larger amounts of carbohy­drate may be required for more prolonged exercise.

Prolonged exercise and multiple transportable carbohydrates

Different carbohydrates ingested during exer­cise may be utilised at different rates [19] but until a landmark publication in 2004 [16] it was believed that carbohy­drate ingested during exercise could only be oxi­dised at a rate no higher than 1 g/min (60 g/h) independent of the type of carbohydrate [22]. This is reflected in guide­lines which typically recommend an upper limit of intake around 60 grams of carbohydrate per hour during endurance exercise (>1h) [39].

It appears that exogenous carbohydrate oxida­tion is limited by the intestinal absorption of carbo­hydrates. It is believed that glucose uses a sodium dependent transporter SGLT1 for absorption, which becomes saturated at a carbohydrate intake around 60 grams per hour. When glucose is ingested at this rate and another carbohydrate (fructose) that uses a different transporter is ingested simultaneously, oxi­dation rates that were well above 1 g/min (1.26 g/min) [16] can be observed. A se­ries of studies followed in an attempt to work out the maximal rate of exogenous carbohydrate oxidation. In these studies the rate of carbohydrate ingestion was varied and the types and combinations of carbo­hydrates varied. All studies confirmed that multiple transportable carbohydrates resulted in (up to 75%) higher oxidation rates than carbohydrates that use the SGLT1 transporter only [18, 19]. Interestingly such high oxidation rates could not only be achieved with carbohydrate ingested in a beverage but also as a gel [34] or a low fat, low protein, low fibre energy bar [35].

There are several studies that link the increased exogenous carbohydrate oxidation rates observed with multiple transportable carbohydrates to delayed fatigue and improved exercise performance. Ratings of perceived exertion (RPE) during prolonged exercise may be lower with a mixture of glucose and fructose than with glucose alone and cadence might be better maintained in cyclists [25, 38]. It was also demonstrated that a glucose : fructose drink could improve exercise performance [9]. Cyclists exercised for 2 hours on a cycle ergometer at 54%VO₂max during which they ingested either a carbohydrate drink or placebo and where then asked to perform a time trial that lasted approximately 60 min. When the subjects ingested a glucose drink (at 1.8 g/min), they improved their power output by 9% (254W versus 231W). However, when they ingested glucose : fructose there was an­other 8% improvement of the power output over and above the improvement by glucose ingestion (275W versus 254W). Other studies confirmed the bene­fits of glucose: fructose compared with glucose only [37, 44].

Performance benefits have generally be ob­served in studies that are 2.5h or longer and ef­fects start to become visible in the third hour of exercise [25]. When exercise duration is shorter, or intakes are below 70 g/h multiple transportable carbohydrates may not have the same performance benefits [15], but is must be no­ted that in these situations the effects are at least similar to other carbohydrate sources.

Carbohydrate during exercise and performance: dose response

Very few well controlled dose-response stu­dies on carbohydrate ingestion during exercise and exercise performance have been published. Most of the older studies had serious methodologi­cal issues that made it difficult to establish a true dose response relationship between the amount of carbohydrate ingested and performance. Until a few years ago the conclusion seemed to be that you needed a minimum amount of carbohydrate (probably about 20 grams per hour based on one study) but it was generally assumed that there was no dose response relationship [36]. Good dose-response studies, however, were noticeably absent at that time.

More recently, however, evidence has been accumulating for a dose response relationship between carbohydrate ingestion rates, exogenous carbohydrate oxidation rates and performance. In one recent carefully conducted study, endurance performance and fuel selection was measured during prolonged exercise while ingesting glucose (15, 30, and 60 g/h) [42]. Twelve subjects cycled for 2-h at 77% VO₂ peak followed by a 20-km time trial. The results suggest a relationship between the dose of glucose ingested and improvements in endurance performance. The exogenous glucose oxidation in­creased with ingestion rate and it is possible that an increase in exogenous carbohydrate oxidation is directly linked with, or responsible for, exercise per­formance.

A large scale multicentre study by Smith, Zach­wieja, Horswill et al. [41] also investigated the re­lationship between carbohydrate ingestion rate and cycling time trial performance to identify a range of carbohydrate ingestion rates that would enhance performance. In their study, across 4 research sites, 51 cyclists and triathletes completed four exercise sessions consisting of a 2-hour constant load ride at a moderate to high intensity. Twelve dif­ferent beverages (consisting of glucose : fructose in a 2:1 ratio) were compared, providing participants with 12 different carbohydrate doses raging from 10 to 120 g carbohydrate/h during the constant load ride. The carbohydrates used were multiple transportable carbohydrates (glucose : fructose). At all four sites, a common placebo that was artifi­cially sweetened, colored, and flavored and did not contain carbohydrate was provided. The order of the beverage treatments was randomized at each site (3 at each site). Immediately following the cons­tant load ride, participants completed a computer simulated 20-km time trial as quickly as possible. The ingestion of carbohydrate significantly im­proved performance in a dose dependent manner and the authors concluded that the greatest per­formance enhancement was seen at an ingestion rate between 60-80 g carbohydrate/h. Interesting­ly, these results are in line with an optimal carbo­hydrate intake proposed by a recent meta-analysis [48].

Based on the studies mentioned above carbohy­drate intake recommendation for more prolonged exercise can be formulated and are listed in newly proposed guidelines in Figure 1.

Training status

A question that often arises is whether the re­sults of these studies (often conducted in trained or even very well trained individuals) may translate to less trained or untrained individuals. A few studies compared a group of trained individuals with un­trained. No differences were found in exogenous car­bohydrate oxidation between trained and untrained [24, 47].

It is possible that there is an absolute exercise intensity below which exogenous oxidation rates are lower and this may be more important than the training status of the athlete. It is unlikely that the runner who completes the marathon in 5 h would need an intake of 90 carbohydrate per hour as this would be close to, or could even exceed, the total car­bohydrate use, at that absolute exercise intensity.

Effect of body weight

The guidelines for carbohydrate intake during exercise, presented here, are expressed in grams per hour of exercise and that these figures are not corrected for body mass. In the most recent posi­tion statement by the American Dietetics Associa­tion (ADA) and ACSM [36], advice with respect to carbohydrate intake during exercise is expressed in g/kg. The rationale for this was un­clear as there appears to be no correlation between body mass and exogenous carbohydrate oxidation [19]. The reason, for this lack of cor­relation between body weight and exogenous carbo­hydrate oxidation, is probably that the limiting factor is carbohydrate absorption and absorption is largely independent of body mass. It is likely, however, that the absorptive capacity of the intestine is modified by carbohydrate content of the diet as it has been shown in animal studies that intestinal transporters can be upregulated with increased carbohydrate in­take. Since exogenous carbohydrate is independent of body mass or muscle mass, but dependent on ab­sorption and to some degree the absolute exercise intensity (at very low absolute intensities, low carbo­hydrate rates may also restrict exogenous carbohy­drate oxidation), the advice given to athletes should be in absolute amounts. These results clearly show that there is no rationale for expressing carbohy­drate recommendations for athletes per kilogram body mass (Figure 1).

In summary, individual differences in exoge­nous carbohydrate oxidation exist, although they are generally small. These differences are not re­lated to body mass but more likely to a capacity to absorb carbohydrates. This in turn could be diet related.

Training the gut

Since the absorption of carbohydrate limits exo­genous carbohydrate oxidation, and exogenous carbohydrate oxidation seems to be linked with exercise performance, an obvious potential strategy would be to increase the absorptive capacity of the gut. Anecdotal evidence in athletes would suggest that the gut is trainable and that individuals who regularly consume carbohydrate or have a high dai­ly carbohydrate intake may also have an increased capacity to absorb it. Intestinal carbohydrate trans­porters can indeed be upregulated by exposing an animal to a high carbohydrate diet [11]. To date there is limited evidence in humans. A re­cent study by Cox et al. [6] investigated whether altering daily carbohydrate intake affects substrate oxidation and in particular exogenous carbohydrate oxidation. It was demonstrated that exogenous car­bohydrate oxidation rates were higher after the high carbohydrate diet (6.5 g/kg bodyweight/day; 1.5 g/ kg BW provided mainly as a carbohydrate supple­ment during training) for 28 days compared with a control diet (5 g/kg bodyweight/day). This study pro­vided evidence that the gut is indeed adaptable and this can be used as a practical method to increase exogenous carbohydrate oxidation. We recently sug­gested that this may be highly relevant to the endu­rance athlete and may be a prerequisite for the first person to break the 2h marathon barrier [43]. Although more research is needed, it is recommended to practice the carbo­hydrate intake strategy in training, and dedicate at least some training to training with a relatively high carbohydrate intake.

Carbohydrate intake in real life events

Relatively few studies have investigated how much carbohydrate athletes ingest during races and whether they meet the guidelines. In a study by Kimber, Ross, Mason and Speedy [26] the average carbohydrate intake during an Ironman distance triathlon was 1.0 g/kg BW/h in female triathletes and 1.1 g/kg BW/h in male triathletes. They achieved these carbohydrate intakes by in­gesting very large amounts of carbohydrate during cycling (approximately 1.5 g/kg BW/h). Most of the intake occurred during the cycling leg where intake was almost 3 times as high as during running leg. In male athletes carbohydrate intake was positively correlated with finish time but this relationship could not be confirmed in females. A large study of endurance events by Pfeiffer et al. [32], demonstrated wide variation in carbo­hydrate intake reported by athletes between and within events, with highest intakes in cycling and triathlon events and lowest in marathons. In this study it was also found that in Ironman races car­bohydrate intake was related to finish time with greater carbohydrate intake correlating to bet­ter performance. These findings appear to be in agreement with the recent dose response studies by Smith, Pascoe et al. [40] and Smith, Zachwieja et al. [41, 42].

Different advice for different endurance sports

With carbohydrate feeding during cycling is it has repeatedly been shown that muscle glycogen breakdown is unaffected. During running, however, there are suggestions that muscle glycogen break­down is reduced in particular in type I muscle fibres [45]. Therefore carbohydrate feeding results in improved performance in cycling and running, although the mechanism by which this occurs may not necessa­rily be the same. This issue is discussed in more de­tail in an excellent review by Tsintzas and Williams [45]. Exogenous carbohydrate oxidation appears to be similar in cycling and running [33] sug­gesting that the advice for cyclists and runners is not different.

Intermittent and skill sports

The vast majority of studies has been per­formed with endurance athletes performing con­tinuous exercise. Most team sports have a high­ly intermittent nature with bursts of very high intensity exercise followed by relatively low inten­sity recovery periods. Besides this, performance in these sports is often dependent on other factors than maintenance of speed or power and factors like agility, timing, motor skill, decision making, jumping, and sprinting may all play a role. Never­theless, carbohydrate ingestion during exercise has also been shown to enhance endurance ca­pacity in intermittent activities. A large number of studies have demonstrated that if carbohydrate is ingested during intermittent running, fatigue can be delayed and time to exhaustion can be in­creased [10, 13, 29-31].

More recently, studies have incorporated mea­surements of skill into their performance measure­ments. Currell, Conway and Jeukendrup [8] de­veloped a 90 min soccer simulation protocol that included measurements of skill, such as agility, dribbling, shooting and heading. The soccer pla­yers performed 90 min of intermittent exercise that mimicked their movement patterns during a game. During the 90 min, skill performance measurements were performed at regular intervals. Agility, drib­bling and accuracy of shooting were all improved but heading was not affected with carbohydrate in­gestion. Other studies have found similar effects [1]. Although typically a number of the skills measured in these studies were improved with carbohydrate feeding, the mechanisms behind these improvements are unknown and have not been studied in any detail.

It appears that carbohydrate intake during team sports and other sports with an element of skill has the potential to improve not only fatigue resistance but also the skill components of a sport, especially towards the end of a game. The practical challenge is often to find ways to ingest carbohydrate during a game within the rules of the sport.

Summary

In summary, there have been significant changes in the understanding of the role of carbohydrate du­ring exercise in recent years and this allows for more specific and more individualised advice with regards to carbohydrate ingestion during exercise. The new guidelines proposed take into account the dura­tion (and intensity) of exercise and advice is not res­tricted to the amount of carbohydrate, it also gives direction with respect to the type of carbohydrate. The recommendations presented here are derived mostly from studies with trained and well-trained ath­letes. Athletes who perform at absolute intensities that are lower will have lower carbohydrate oxidation rates and the amounts presented here should be ad­justed (downwards) accordingly. The recommended carbohydrate intake can be achieved by consuming drinks, gels of low fat, low protein and low fibre solid foods (bars) and selection should be determined by personal preference. Athletes can adopt a mix and match strategy to achieve their carbohydrate intake goals. However, the carbohydrate intake should be balanced with a fluid intake plan and it must be noted that solid foods and highly concentrated carbohydrate solutions have been shown to reduce fluid absorption. Although, a slowing of gastric emptying and absorp­tion can partly be prevented by using multiple trans­portable carbohydrates, this is something the athlete needs to consider when developing their nutrition strategy. Although more research is needed, it is high­ly recommended to train the nutrition strategy to re­duce the chances of gastro-intestinal discomfort and to increase the absorptive capacity of the intestine.

Finally it must be noted that most studies are based on findings in runners and cyclist and more work is needed to establish the effects and underlying mechanisms of carbohydrate in­gestion on skill components in intermittent team sports.

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