Carbohydrate Availability and Training Adaptation: Effects on Cell Metabolism

John A. Hawley; Louise M. Burke


Exerc Sport Sci Rev. 2010;38(4):152-160. 

In This Article

Unanswered Questions and Directions for Future Research

Cell Signaling versus Functional Outcomes

A common finding from many of the studies reviewed is the mismatch between the changes in cellular "mechanistic" variables (typically reported as increases in the phosphorylation status of signaling molecules and/or increases in the expression of genes and proteins involved in mitochondrial biogenesis) and whole-body functional outcomes (changes in training capacity or measures of performance). Several themes can be proposed to help explain this disconnect, and each warrants further investigation. First, there may be no direct relationship between performance and some of the training-induced changes in selected cellular events that are typically measured; the functions achieved by upregulating various muscle proteins may be permissive in promoting the capacity for exercise but are not quantitatively correlated, or indeed rate limiting for athletic performance. Muscle function is only one factor in determining performance, which involves the integration of whole-body systems including the role of the central nervous system, in determining pacing strategies and perceptions of fatigue or effort. A second rationale is that we currently lack the appropriate tools to accurately measure exercise/sports performance, in particular, the ability to detect small changes that are worthwhile to a competitive athlete to change the outcomes of real-world events. Within sports science, there is much discussion of the challenges of measuring performance using valid and reliable protocols and of using different statistical analyses based on magnitude-based inferences to examine the likelihood that changes or differences in performance are meaningful. In some instances, the technical variability of various enzymatic assays and/or gene measurements exceeds the small biological changes that manifest as improvements in performance.

The third possibility is that some train-low strategies have negative effects on parameters related to an athlete's health or performance that either acutely or over the long term counteract the positive effects achieved on isolated muscle characteristics. Acute impairment might directly result because of the complex interactions between pathways of substrate utilization; as systems to upregulate one pathway occur, there may be a reciprocal downregulation of others. For example, in previous work using another dietary periodization strategy ("fat adaptation") in well-trained athletes, we found that 5-d exposure to a high-fat diet while undertaking a strenuous training regimen produced a robust enhancement of fat oxidation during submaximal exercise, even when carbohydrate availability was restored before, or maximized during, exercise.[7] However, we were not able to detect benefits from this strategy across a range of endurance exercise protocols.[7] In fact, further work clearly demonstrated a reduction in both the calculated rate of muscle glycogenolysis and the activity of the rate-limiting enzyme in carbohydrate metabolism, the PDH complex.[30] This impairment to carbohydrate metabolism would be expected to reduce high-intensity exercise performance. This is indeed the case. Havemann et al.[16] investigated the effect of a high-fat diet followed by 1 d of carbohydrate loading on substrate utilization and performance during a 100-km cycling time-trial. The 100-km time-trial incorporated 1-km high-intensity sprints performed at an intensity of ~90% of maximal aerobic power and longer, 4-km work bouts performed at ~80% of aerobic power. Although there was no difference in overall endurance performance (i.e., the time taken to complete 100 km) or the 4-km work bouts, sprint performance after fat adaptation was significantly reduced (P < 0.05).

An indirect outcome of dietary periodization may be a change in the training stimulus; a common finding when training sessions are undertaken with low carbohydrate availability is that subjects frequently chose a lower workload or intensity because they perceive the effort to be higher, at least in their initial exposure to training low.[35] This outcome would seem counterintuitive for the preparation of competitive athletes, where high-intensity workouts and the generation of high-power outputs are a critical component of a periodized training program. Interference with such sessions is likely to impair other adaptations to training (i.e., muscle fiber recruitment). Training with low carbohydrate availability also is likely to be associated with reduced immune function and expose the athlete to an increased risk of illness and/or injury.

Finally, it simply may be the case that current studies have not been sophisticated enough to integrate various combinations and permutations of train-low strategies into the periodized training programs of highly trained athletes. The preparation of elite athletes involves a range of training activities with various goals.[29] It may be that training low needs to be carefully integrated into parts of this complex system to allow a performance benefit to be achieved in concert with the measurable cellular changes. It also should be considered whether highly trained athletes have a different response or require a different stimulus to untrained or even moderately trained individuals. It has recently been reported that the mitochondrial content and oxidative capacity of skeletal muscle are key determinants of the activation of signaling proteins important to muscle plasticity.[22] The attenuation of kinase phosphorylation in muscle with high mitochondrial content suggests that these proteins may require a greater stimulus input for activation to propagate these cues downstream to evoke phenotypic adaptations.

Train Low: How Far and for how Long do you have to Go?

An aspect that is unclear from the present literature is the degree of glycogen depletion or restricted carbohydrate availability that is needed to potentiate the effect of the training stimulus on outcomes such as mitochondrial biogenesis or the length of time periodic low-glycogen training needs to be undertaken to demonstrate functional changes to training and/or performance outcomes (e.g., weeks to months; training macrocycles). To answer such questions, a complex series of studies would need to be undertaken that would systematically "titrate" levels of carbohydrate availability and determine subsequent cellular and performance response after a standardized training regimen. Unfortunately, few of the present studies have measured actual muscle glycogen content before and after training in the train-low or control conditions; some have simply assumed that restricted intake of carbohydrate and/or an abbreviated recovery period between training sessions will deliver depleted muscle glycogen stores for subsequent sessions. Investigations to date[15,35] have used a limited number of total training sessions during the study duration (18–45 sessions) when determining both muscle adaptation and functional performance outcomes. However, many elite endurance athletes undertake more than 450 total training sessions per year, of which ~25% to 30% would be classified as difficult or hard (T. Stellingwerff, e-mail, April 15, 2010). It is clearly impractical to extrapolate the effect of short-term, laboratory-supervised training studies to an entire year of periodized training and competition. Therefore, train low currently must be considered somewhat of a blunt tool.

Perhaps more importantly, we know surprisingly little about glycogen utilization during the training sessions typically undertaken by competitive athletes, or how their current real-world training and dietary practices interact to determine carbohydrate availability for various workouts. Indeed, although sports nutrition guidelines encourage practices to promote carbohydrate availability for training, particularly key sessions involving high-intensity workouts, it is likely that athletes already undertake some of their sessions with reduced carbohydrate availability, both deliberately and unintentionally. Some athletes have already adopted specific train-low practices because of the present and previous interests in this strategy; however, athletes also may restrict carbohydrate intake below training requirements as part of the reduced energy or carbohydrate-modified diets designed to achieve lower BM or fat levels. Inadvertent causes of training with lowered carbohydrate availability include poor nutrition knowledge and the practical challenges associated with consuming substantial amounts of carbohydrate before early morning training sessions or during workouts in which there is restricted access to food or fluid supplies. Fuel requirements during periods of high-volume training, with two to three sessions per day, may simply exceed maximal glycogen storage capacity, which is limited by both time and carbohydrate intake. Before train-low strategies can be recommended, it seems important to investigate what occurs in the sports world and whether some athletes have already developed successful protocols via trial and error or the art of coaching. For example, African distance runners, who often undertake two to three training sessions per day, perform much of their training in the fasted state (T. Stellingwerff and H. Stellingwerff, personal communication, 2010) albeit against a background diet that is higher in carbohydrate (in grams per kilogram and percentage of energy) than reported intakes from other free-living athletes.[26]


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