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Nutrition and Performance in Sport

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Christophe Hausswirth

Chapter 1. Nutrition: from training to competition

Topic 5. Fuelling strategies to enhance recovery

Christophe Hausswirth et Xavier Bigard

Résumé

In order to compensate for protein loss during exercise, the timing of post-exercise protein supplementation is important. The efficiency of protein synthesis in the whole body is improved by ingesting 10 g of protein rapidly after exercise, with significant effects observed up to t + 3 hours. Another challenge is the refuelling with carbohydrate supply. When time is short between fuel demanding events, it makes sense to start refuelling as soon as possible. The immediate target should be around 1 g of carbohydrate per kg of body mass, repeated every hour until meal patterns take the achievement of daily fuel needs.

Texte intégral

1. Introduction

1Nutritional factors play an essential role. One of the basic rules requires a balance between nutritional needs and diet to be maintained. Biological constants can be restored if there is balance, which must be understood both in terms of calories (quantitative balance) and in terms of macronutrients and micronutrients (qualitative balance).

2The aims of nutritional recovery are specific to each athlete and to each training period, and appear thus to be determined by a group of factors.

3■ Physiological and homeostatic modifications resulting from training, including:

  • the extent of depletion in energy substrates (mainly glycogen),

  • the extent of dehydration (see previous pages),

  • the extent of muscle injury or protein catabolism.

4■ The goals in terms of performance improvement or adaptation of training sessions, including:

  • the increase in muscle size or strength

  • the reduction in per cent body fat

  • the increase in enzymes, functional proteins or synthesis of functional cells or tissues (e.g. red blood cells, capillaries, etc.)

  • the level of substrates ingested and the hydration status before the next exercise.

5■ The duration of the period separating two exercises, including:

  • total recovery time

  • other obligations or needs during the recovery period (e.g. sleep, travel, etc.).

6■ The availability of food for ingestion during the recovery period, including:

  • immediate availability of food after training

  • athletes’ appetite and the opportunity to consume food and beverages during the recovery period.

2. Proteins and recovery

2.1 Protein metabolism and recovery

7It has been shown that physical exercise affects protein metabolism. Regular strength or aerobic training sessions influence protein metabolism by different processes depending on the type of activity. We know that strength training leads to increased muscle mass while endurance training tends to increase oxidative enzymes. In both cases, protein synthesis is favoured. This protein synthesis is essential for development and growth, but also for the maintenance of body mass. While sugars represent the main source of energy supplied during exercise, regular exercise significantly increases daily needs in nitrogen-containing compounds. Indeed, Rennie et al. (1981) showed, during experiments on human subjects, that reduced protein synthesis combined with a concomitant increase in proteolysis and amino acid oxidation inevitably led to a nitrogen debt within the muscle. As shown in Figure 1, proteolysis during exercise is greater than protein synthesis. The degradation/synthesis difference is about 5 g of protein per hour of activity. This value relates to that measured through urea production due to amino acid oxidation. The protein balance is therefore negative during exercise: nitrogen expenditure is not covered by protein intake.

8In specific conditions, some amino acids are susceptible to oxidation, and thus constitute energy substrates in themselves. However, all the proteins present in the body play a precise functional role, and in contrast to carbohydrates and lipids, no reserve of amino acids is available. Where necessary, amino acids derived from structural or functional proteins will be used. Among the amino acids making up the proteins of the body, only substituted amino acids (leucine, isoleucine, valine), alanine, glutamate and aspartate are oxidized in muscles (Goldberg and Odessey, 1972). Only these amino acids are capable of contributing to the energy needed for ATP resynthesis during exercise. In addition, some experimental evidence indicates that, among these amino acids, those harbouring a substituted group play a bigger role in energy metabolism (Lemon, 1991). It is clear, however, that the contribution of amino acid oxidation to energy provision depends strictly on the type of exercise, its relative intensity, its duration, the athlete’s fitness and nutritional status (Lemon, 1991).

9We know very little about the level of protein synthesis in athletes during recovery. It is, however, well established that an increase in amino acid levels in the sarcoplasm is observed in the hours following exercise, of whatever type; Goldley and Goodman (1999) were able to show that this accumulation is observable from the fourth hour after application of the workload. Intra-sarcoplasmic accumulation of amino acids during recovery from physical exercise has been attributed to a specific effect of muscle use, resulting in increased transmembrane transport (Goldberg et al. 1975). The increased membrane transport of amino acids occurs at the same time as glucose transport. Despite the absence of direct experimental proof, post-exercise amino acid accumulation in muscle fibres creates favourable conditions for protein resynthesis, and it is now well established that the sarcoplasmic accumulation of amino acids and protein synthesis are strongly correlated (Goldley and Goodman, 1999).

Figure 1: Protein metabolism in humans over 3.75 h of moderate exercise. Protein flux is expressed in g of protein and amino acids metabolized per hour, during resting or active periods.

Figure 1: Protein metabolism in humans over 3.75 h of moderate exercise. Protein flux is expressed in g of protein and amino acids metabolized per hour, during resting or active periods.

(Adapted from Rennie et al. (1981) with the authorization of Clinical Sciences).

2.2 Proteins, contractile activity and muscle development during recovery

10It is remarkable to note that, in regularly trained athletes, consuming excess dietary proteins during recovery has a double result: primarily, to ensure the repair of morphological lesions as a result of exercise; and, to allow the synthesis of structural proteins. However, it is now well established that the anabolic effect of proteins depends strictly on muscle contraction. According to Décombaz (2004) three factors must coincide to activate net muscle protein synthesis: muscle contraction, amino acid availability and insulin circulation.

11What is essential in the relationship between recovery and endocrinology, is that the very nature of nutrients influences growth hormone release. In man, it has been show that the absorption of 500 calories as carbohydrates (maltodextrin) or 500 calories as proteins (commercially available supplement made up of a complex of several amino acids) was followed by a reduction in growth hormone release (Matzen et al. 1990). After this initial drop, protein-based nutrition has the particularity of inducing a peak of growth hormone secretion. This starts 90 minutes after absorption of the supplement, and extends into the fourth hour (Fig. 2). These results show that the composition of the daily diet plays an important role in the control of growth hormone release. We can easily hypothesize that this stimulation of growth hormone release, observed after the ingestion of dietary proteins, is a factor favouring anabolism of contractile and structural proteins in skeletal muscles. However, there seems to be a plateau for protein synthesis. Above this threshold, amino acids from excess dietary proteins are more likely to be oxidized than stored (above 1.5 g.kg-1.d-1) [Tarnopolsky et al. 1988]. These results cast a significant shadow of doubt over the advantages of consuming very large quantities of proteins – i.e. above the needs induced by exercise – for the development of muscle mass during recovery.

Figure 2: Growth hormone release over time after ingestion (at time 0) of a bolus of carbohydrates or proteins.

Figure 2: Growth hormone release over time after ingestion (at time 0) of a bolus of carbohydrates or proteins.

(Adapted from Matzen et al. (1990) with the authorization of the Scandinavian Journal of Clinical Laboratory Investigation).

2.3 Chrono-recovery and proteins

12In terms of protein metabolism, results are qualitatively similar for the very large range of exercise types, from brief, very intense exercise to long-term endurance exercises. Thus, all exercise links reduced protein synthesis and increased degradation, while the reaction is reversed during the recovery period (Poortmans, 1993). Therefore, the notion of temporal recovery, with regards to nutrition – most specifically for proteins – is an essential factor in the rapid restoration of energy substrates.

13In animal experiments as early as 1982, muscular protein synthesis was shown to increase over the two hours following completion of a period of high-intensity exercise (Booth et al. 1982). The increase in protein content in the muscle, both total and myofibrillar proteins (25% for the Gastrocnemius muscle), depends on the intensity and duration of exercise (Wong and Booth, 1990). Similar results were reported in humans after four hours’ running on a treadmill (Carraro et al. 1990) or after repeated strength training at 80% of maximal capacity (Chesley et al. 1992). In order to compensate for protein loss during exercise – 60 minutes at 60% of maximal oxygen consumption – one recent study investigated the importance of the timing of post-exercise protein supplementation. Levenhagen et al. (2001) were able to show that efficiency of protein synthesis in the whole body was improved by ingesting 10 g of proteins rapidly after exercise, with significant effects observed up to t + 3 hours (Fig. 3). When proteins were ingested more than three hours after exercise, recovery did not allow complete restoration of proteins to basal levels. The authors conclude that insulin may play a central role in the regulation of protein synthesis. Thus, it appears important to consume a source of proteins immediately after long duration, or brief duration but very high-intensity, exercise.

Figure 3: Protein synthesis over time for a group of ten athletes ingesting proteins either immediately, or 3 hours after exercise.

Figure 3: Protein synthesis over time for a group of ten athletes ingesting proteins either immediately, or 3 hours after exercise.

*: significant difference between the “early intake” and “late intake” conditions (P<0.05).
(Adapted from Levenhagen et al. (2001) with the authorization of the
American Journal of Physiology – Endocrinology and Metabolism).

14The athlete’s carbohydrate (CHO) reserves at the end of a period of exercise must also be taken into account during recovery. Although they are difficult to measure in the muscle, it seems important to be able to estimate their level from the extent of energy expenditure. Indeed, the availability of energy substrates, and particularly CHO, is known to be an essential factor in the level of amino acid oxidation. In this context, Lemon and Mullin (1980) measured urea excretion as a marker of oxidation of nitrogen-containing compounds. They compared glycogen depletion during exercise and while resting, and found that during exercise it induced a greater increase in urea excretion. The availability of glycogen therefore contributes to regulating amino acid oxidation. These observations appear essential to the understanding of recovery: athletes with low glycogen stores during exercise will see an increase in their nitrogen balance. Tarnopolsky et al. (1988) estimated the minimal protein intake to avoid a negative nitrogen balance in endurance athletes to be 1.2 to 1.4 g/kg/d. Given the significant levels of inter-individual variability in terms of protein digestibility and assimilation, for endurance athletes, a daily intake of 1.5 to 1.7 g/kg body weight is recommended (Martin, 2001). This corresponds to between 12 and 16% of total daily energy intake. For athletes performing strength sports, and for those in whom muscle mass must be maintained, sufficient protein intake to equilibrate the nitrogen balance is estimated at between 1.4 and 1.6 g.kg-1.d-1. This so-called “safety” intake is indicated for high nutritional value proteins. For athletes wishing to increase their muscle mass, increased dietary protein intake, varying between 2 and 2.5 g.kg-1.d-1, may be offered for limited periods. However, high protein intake must not be prolonged, and must not exceed six months per year (Martin, 2001). Given our current knowledge, it seems difficult to justify intakes sometimes exceeding 3 g.kg-1.d-1. It is also logical to suppose that excess dietary protein may be bad for the athlete’s health, in particular for renal function. It is especially important to note that urinary excretion of nitrogen induces increased fluid loss. This is why fluid intake must be closely monitored and adjusted in these populations. The absence of visible alarm signals should not be used to encourage consumption of abnormal protein quantities, particularly since we now know that there is no proven scientific justification for this practice.

15The importance of an anabolic environment was indicated by a recent study in which immediate intake – five minutes after muscle reinforcement training – of a dietary supplement including 19 g of milk proteins (rich in essential amino acids), over 12 weeks, produced muscular hypertrophy and strength gain at increased levels compared to when intake was delayed for two hours. This was observed in a population of master athletes (Esmarck et al. 2001). In parallel to this study, the authors investigated the relevance of food intake just before exercise, and its incidence on athletes’ recovery. In this case, Tipton et al. (2001) suggest that taking essential amino acids (EAA) before exercise mainly based on resistance, has a more marked effect on later protein synthesis than if they are taken after exercise (Fig. 4).

Figure 4: Net phenylalanine production in the blood over four periods (rest, exercise, Hr 1 PE: one hour post-exercise, and Hr 2 PE: two hours post-exercise).

Figure 4: Net phenylalanine production in the blood over four periods (rest, exercise, Hr 1 PE: one hour post-exercise, and Hr 2 PE: two hours post-exercise).

Pre” indicates intake of essential amino acids five minutes before exercise.
“Post” indicates intake of essential amino acids five minutes after exercise.
*: significant difference with the “Post” condition (P<0.01).
(Adapted from Tipton et al. (2001)
with the authorization of the
American Journal of Physiology – Endocrinology and Metabolism).

16These authors compared situations before and after exercise, and showed higher protein synthesis when athletes were given a solution of 6 g EAA and 35 g glucose before performing resistance exercises. The indicator of muscle protein synthesis used was based on the net rate of phenylalanine production from amino acids circulating in the blood. These results could be explained by an increased rate of blood flow, favouring a greater influx of amino acids (AA) to the muscles, and thus a reduction in the lag time for protein synthesis. The authors also showed that this protein synthesis persists for one hour after exercise when EAA were taken five minutes before (in comparison with the situation in the “Post” group). In agreement with this result, it is of note that the effect of increased AAs on protein synthesis is of short duration, despite efforts to maintain consistently high blood concentrations (Bohe et al. 2001). Thus, it is more practical to have several small intakes of dietary proteins at regular intervals (lunch, snack, dinner, etc.), this allows for several protein concentration peaks during the recovery period. The acute effect observed by Tipton et al. (2001) over the first two hours of recovery seems to be prolonged (positive nitrogen balance) over 24 hours (Tipton et al. 2003). This suggests that muscle mass could grow if the protein intake – preferably of dietary proteins – was repeated over an extended period. We lack convincing evidence that, in young athletic adults, exercise combined with supplements induces a more positive protein balance in the long term than exercise without supplements. It is also necessary to take into account the possible influences of physical exercise on protein metabolism over the remainder of the day (various meals, sleep, etc.). However, it must be borne in mind that most of the results described here were obtained for a single variable (i.e. protein synthesis), which, although necessary, is not sufficient for muscular hypertrophy. Measurements in real life, possibly showing a benefit in terms of strength or muscle diameter after several weeks, are difficult to carry out.

2.4 Combining proteins, carbohydrates and leucine for muscle recovery

17The availability of energy substrates, and in particular carbohydrates, is an essential determinant in the level of amino acid oxidation. Indeed, glycogen depletion during exercise induces a greater increase in urea excretion than during rest. As we have seen, urea excretion is a reflection of the use of nitrogen-based compounds (Lemon, 1997). It seems clear that oxidation of amino acids during exercise is closely related to the availability of other energy substrates. The enzymatic complex: branched chain alpha-keto acid dehydrogenase (BCKA-DH), is a major actor in this process. It is the limiting enzyme in the leucine catabolism pathway, and its activity is controlled by factors such as intensity and duration of exercise. Experiments based on animal models have shown that BCKA-DH activity in the muscle increases with running speed (Kasperek and Snider, 1987). Similarly, endurance training induces an increase in leucine oxidation during exercise by increasing the activity of muscle BCKA-DH.

18A first study by Anthony et al. (1999) showed the effects of leucine supplementation on recovery. In various rat populations leucine was found to significantly stimulate protein synthesis following exercise on a treadmill. More recently, studies carried out in humans highlighted the fact that ingestion of carbohydrates combined with proteins and/or amino acids often affected how plasma insulin levels were regulated (Pitkanen et al. 2003). It is assumed that these high insulin concentrations can stimulate uptake of selected amino acids along with the rate of protein synthesis (Gore et al. 2004). In addition, insulin is known to inhibit proteolysis (Biolo et al. 1997). Very recently, Howarth et al. (2009) got long distance athletes to perform two hours of cycling and then ingest various solutions over the following three hours. The solutions contained: a medium concentration of carbohydrates (1.2 g.kg-1.h-1 L-CHO), a very high concentration of carbohydrates (1.6 g.kg-1.h-1 H-CHO) or a medium concentration of carbohydrates in addition to proteins (1.2 g.kg-1.h-1 CHO and 0.4 g.kg-1.h-1 PRO). Consuming PRO–CHO during recovery allowed a significant increase in the net protein balance four hours after the end of aerobic exercise, as well as an increase in the rate of protein synthesis. The results from the group consuming PRO–CHO during recovery led the authors to conclude that there is a possible adaptation of the muscle, on the one hand, and muscular anabolism, on the other, to repair the damage induced by long duration exercise. Another recent study was carried out on several high level athletes running for 45 minutes on a treadmill (Koopman et al. 2005, Fig. 10). Immediately after exercise the athletes consumed energy drinks composed of: carbohydrates (0.3 g.kg-1.h-1 CHO); carbohydrates and proteins (0.3 g.kg-1.h-1 CHO and 0.2 g.kg-1.h-1 PRO); or, carbohydrates, protein and free leucine (0.3 g.kg-1.h-1 CHO; 0.2 g.kg-1.h-1 PRO and 0.1 g.kg-1.h-1 Leu). The results show, primarily, that the net protein balance was significantly higher in the “CHO + PRO + Leu” condition compared to the other two. In addition, as indicated in Figure 5, ingestion of a CHO + PRO + Leu energy drink allowed a higher insulin response compared to the other two situations. Plasma insulin levels were also increased in the “CHO + PRO” condition compared to the “CHO alone” condition. It seems that the ingestion of proteins during recovery, with an additional charge in leucine (a substituted amino acid), allows greater stimulation of protein synthesis when associated with CHO than when the drink consumed contains carbohydrates alone. Leucine therefore stimulates protein synthesis – in an insulin-dependent manner – by different pathways. Leucine has the particularity of working as a nutritional signalling molecule modulating protein synthesis. Leucine was also shown to potentially affect muscle protein metabolism by reducing degradation (Nair et al. 1992). This is most likely achieved through increasing circulating insulin and phosphorylating key proteins involved in regulating protein synthesis (Karlsson et al. 2004). However, while most in vivo or in vitro studies on animals report that administering leucine can inhibit protein lysis and stimulate its synthesis, in vivo studies in humans show that the ingestion of leucine and/or branched-chain amino acids reduces proteolysis, but does not otherwise stimulate protein synthesis. The maximal rates of protein synthesis during post-exercise recovery probably require signalling from these amino acids (i.e. substituted and branched), but also from the anabolic signal provided by exercise.

Figure 5: Plasma insulin concentration response to two hours’ recovery and three ingestion conditions (CHO: carbohydrates; CHO + PRO: carbohydrate + proteins; CHO + PRO + Leu: carbohydrate + proteins + leucine).

Figure 5: Plasma insulin concentration response to two hours’ recovery and three ingestion conditions (CHO: carbohydrates; CHO + PRO: carbohydrate + proteins; CHO + PRO + Leu: carbohydrate + proteins + leucine).

*: Values significantly different from the CHO condition (P<0.01).
**: Values significantly different from the CHO + PRO condition (P<0.01).
(Adapted from Koopman et al. (2005) with the authorization of the
American Journal of Physiology – Endocrinology and Metabolism).

19Finally, no studies of the benefits of other substituted amino acids (such as isoleucine and valine) on protein synthesis during recovery have been carried out. The complexity of, and metabolic interrelationships within, pathways involving amino acids do not favour analysis of their transformation.

2.5 Amino acid ingestion and post-exercise mental performance

20The “central fatigue hypothesis” states that branched-chain amino acids (BCAAs) competitively inhibit tryptophan transfer across the blood-brain barrier. Oral supplementation aiming to regulate the BCAA concentration in the blood would reduce the conversion of tryptophan to serotonin in the brain. Serotonin is a neurotransmitter playing a role in sensing fatigue. The serotonin response and evolving prolactin concentrations accompany modifications of substituted amino acid (SAA) – valine, isoleucine, leucine – concentrations in plasma. From this observation, Newsholme (1986) formulated the hypothesis that changes to the concentration of SAA can regulate the central mechanisms of fatigue by increasing the speed of serotonin synthesis. These arguments led researchers to propose SAA or tryptophan supplementation in humans, in order to test Newsholme’s hypothesis. Different studies, not very numerous, showed an improvement in mental performances during a football match after ingesting a 6% CHO solution and BCAAs (Blomstrand et al. 1991). To our knowledge, a single recent study of top level athletes investigated the influence of BCAA and their impact on mental performance during the recovery phase. Portier et al. (2008) studied the effects of a diet enriched in SAA (50% valine, 35% leucine and 15% isoleucine) on a short-term memory test taken just after a sailing competition(Fig. 6). The results show that a diet enriched in SAA during a competition allows better conservation of mental performances during the recovery phase than the carbohydrate-based diet generally observed in this sport. This could be an interesting application where, in cases like sailing, competitive legs follow each other throughout the day with very limited recovery periods.

Figure 6: Mental responses symbolized by the percentage of errors made during the “four letter memorization” test just after a sailing competition. During the competition, subjects ingested either a control CHO solution, or a CHO + branched-chain amino acids (BCAA) solution.

Figure 6: Mental responses symbolized by the percentage of errors made during the “four letter memorization” test just after a sailing competition. During the competition, subjects ingested either a control CHO solution, or a CHO + branched-chain amino acids (BCAA) solution.

*: significant difference between the values obtained for the “Before race” and “After race” conditions (P<0.05).
**: significant difference between the values obtained for control and “Substituted amino acids” conditions (P<0.05).
(Adapted from Portier et al. (2008) with the authorization of the
European Journal of Applied Physiology).

21Recommendations on protein intake during recovery

22■ For the stimulation of glycogen storage in muscles after exertion, all the data underline the importance of early food intake (from the end of exercise) and somewhat reduce the role of increased insulin, as well as the relevance of ingesting insulogenic proteins and amino acids (Ivy et al. 2002).

23■ Intake of substituted amino acids – mainly leucine (0.1 g.kg-1.h-1) – associated with carbohydrates (0.3 g.kg-1.h-1) and proteins (0.2 g.kg-1.h-1), is recommended in order to stimulate post-exercise protein synthesis, and thus recovery (Koopman et al. 2003).

24■ The importance of an anabolic environment was shown by an immediate intake, after muscle reinforcement exercise, of 19 g of milk proteins (rich in essential amino acids) over 12 weeks: the strength gain was increased compared to when intake was delayed for two hours (Esmarck et al. 2001).

25■ The availability of glycogen regulates amino acid oxidation. Thus, athletes whose glycogen stores are depleted during exercise will see an increase in their nitrogen balance. In order to avoid a negative nitrogen balance in endurance athletes, the minimal protein intake seems to be between 1.2 and 1.4 g.kg-1.d-1 (Tarnopolsky et al. 1988).

26■ Even if SAA appear to help maintain post-exercise mental performance, to date there is no quantitative evidence affirming that supplements targeting essential amino acids would be useful, on a continuous basis, to athletes in good health (Bigard and Guezennec, 2003).

27■ Dietary composition plays an important role in the control of growth hormone release. Stimulation of this, observed one hour after the ingestion of dietary protein, favours anabolism of contractile and structural proteins in skeletal muscle (Matzen et al. 1990).

28■ There is a threshold for protein synthesis; above it, amino acids from excess dietary proteins are oxidized rather than stored (above 1.5 g.kg-1.d-1) [Tarnopolsky et al. 1988].

3. Sugars and recovery

3.1 Role of sugars

29The majority of energy needs are met by sugars (carbohydrates) and lipids. In the sugars category, glucose plays a predominant role, as it is immediately available. It is transported in the blood, and its catabolism supplies cells with energy. All cells therefore use blood glucose. For example, it covers half the energy needs of the central nervous system, the remainder coming from the degradation of ketone bodies. However, the body’s glucose reserves are low (25 g), this requires the human body to permanently import new glucose molecules from food sources. When they are not used to renew the glycogen stores of various tissues, excess dietary sugars are converted into lipids in the liver and in adipocytes. Glucose alone represents 80 to 90% of the energy supplied by sugars. In aerobic conditions, complete oxidation of a mole of glucose leads to the formation of 38 moles of adenosine triphosphate (ATP). When resting, during postprandial periods, glucose absorption is discontinuous. For 100 g absorbed during a meal, it is estimated that 60 g are oxidized over the following three hours. This use of glucose allows relative lipid savings. The cost of glucose storage (for later use) is 5%.

3.2 Glycogen resynthesis during recovery

3.2.1 Influence of the sugar type

30Reductions in muscle glycogen as a result of prolonged exercise stimulate the metabolic pathways leading to glycogen synthesis during recovery. Ingesting sugar-containing foods during this recovery phase leads to two phenomena: on the one hand, an increased rate of resynthesis, and on the other, an increased level of glycogen, above those present prior to exercise. Glycogen resynthesis capacities differ depending on the nature of the sugars available. The speed of muscle glycogen resynthesis is identical during the recovery phase after ingestion of glucose or glucose polymers, but it is slower with fructose (Blom et al. 1987). In contrast, fructose increases the resynthesis rate for hepatic glycogen, to the extent that glycogen synthesis is promoted by insulin activity. It is therefore more efficient, during recovery, to administer carbohydrates with a high glycaemic index.

31These data were confirmed a few years later, taking the notion of glycaemic index (GI) into consideration. The GI allows the physical response to oral intake of carbohydrates (CHO) to be characterized. It is defined as the area under the curve for glycaemic response after the ingestion of a sugar-containing food. This curve reflects, on the one hand, the speed of appearance of sugar in the blood, and on the other, its speed of capture by the tissues using it. The GI thus allows foods to be compared. In this way, for a population of highly trained cyclists, Burke et al. (1993) were able to show that the maximum muscle glycogen resynthesis (Vastus Lateralis muscle) observed 24 hours after exercise (two hours at 75% of the VO2max) was obtained when post-exercise alimentation was based on high GI carbohydrates (Fig. 7). This result cannot be totally explained by variations in insulin and glucose concentrations. Indeed, the extent of glycogen resynthesis post-exercise is about 30% of the pre-exercise level, this cannot be explained by smaller variations in insulin and glucose levels over 24 hours. These data are essential when the athlete must train repeatedly during the day and/or when competitions are repeated.

Figure 7: Muscle glygogen concentrations, immediately and 24 hours after performing prolonged exercise in subjects having consumed 10 g of carbohydrate (CHO) per kg body weight over the 24 hours following exercise. These CHO are sugars with a low or high glycaemic index.

Figure 7: Muscle glygogen concentrations, immediately and 24 hours after performing prolonged exercise in subjects having consumed 10 g of carbohydrate (CHO) per kg body weight over the 24 hours following exercise. These CHO are sugars with a low or high glycaemic index.

*: significantly different from the use of sugars with a low glycaemic index (P<0.05).
(Adapted from Burke et al. (1993) with the authorization of the
Journal of Applied Physiology).

32In order to better explain the mechanisms relating to the lower efficacy of low GI CHOs, some authors have evoked poor intestinal absorption (Wolever et al. 1986; Jenkins et al. 1987). Indeed, Joszi et al. (1996) recently showed that the low digestibility of a mixture with a high concentration of starch amylose (low GI) was responsible for a lower restoration of glycogen observed during 13 hours’ post-exercise recovery compared with the ingestion of glucose or maltodextrins (high GI). These authors therefore show that the poor digestibility of some CHOs leads to overestimation of their availability in the intestine (Joszi et al. 1996). We think, in addition, that these studies should be reinforced by others, during which real food should be ingested. Nevertheless, a longitudinal study, carried out over 30 days, showed that an active population exposed to a low GI daily diet showed reduced glycogen synthesis, compared to initial values and values for a similar population consuming a high GI diet (Kiens and Richter, 1996). From this observation, we must therefore be careful when we recommend only diets with a low GI, to the extent that these do not always favour glycogen resynthesis. While the composition of CHO solutions appears crucial for the recovery phase, the timing of intake also influences muscle glycogen resynthesis.

3.2.2 Importance of the timing of post-exercise food intake

33Intake of CHO and its precise “timing” during the recovery phase largely influence the quality of glycogen resynthesis. These strategies are very important during unique restrictive situations (such as triathlon or marathon), but also during events where competitive legs are repeated throughout the day (such as swimming, middle-distance racing or repeated judo combats). The sooner carbohydrates are consumed after completing exercise, the higher the amount of muscle glycogen resynthesized. Thus, when some CHO is ingested immediately after exercise, the quantity of muscle glycogen measured 6 hours later is higher than when the intake of CHO is delayed for two hours after the end of exercise (Ivy et al. 1988a). It is now accepted that exercise increases both sensitivity to insulin (Richter et al. 1989) and permeability of the muscle cell membrane to glucose, and that the highest rates of muscle glycogen resynthesis are recorded during the first hour (Ivy et al. 1988a, Fig. 8). This is mainly due to the fact that the enzyme glycogen synthase is activated by glycogen depletion (Wojtaszewski et al. 2001). Sugar-based nutrition immediately after exercise takes advantage of these effects, as reflected by the higher rates of glycogen storage (7.7 mmol.kg-1.h-1) over the first two hours of recovery. The usual rates of glycogen storage (4.3 mmol.kg-1.h-1), are judged insufficient in this context [Ivy et al. 1988a]. This study showed the basis for recovery with regards to glycogen: ingestion of too little CHO immediately after exercise induces very low rates of glycogen resynthesis, rates which are not inclined to promote repeated performances (training or competition). In addition, delaying food-based CHO intake for four hours after the end of exercise does not allow high rates of glycogen resynthesis, in contrast with immediate post-exercise intake. These results are particularly relevant for relatively short recovery periods between exercises (between six and eight hours). When recovery is longer (between 8 and 24 hours), dietary intake of CHO immediately after exercise does not result in accelerated glycogen resynthesis (Parkin et al. 1997, Fig. 13). As part of twice-daily training sessions for high-performance athletes, it is preferable to favour early food intake after exercise, with a view to promoting replenishment of glycogen stores and thus avoid penalizing the second training session. In the case of athletes not training more than once per day, it is not so much a question of rushing to consume CHO just after exercise as of favouring consumption of a meal or snack with adequate CHO before the next training session. However, in the case of exercises requiring a high rate of energy expenditure and of long duration, sugar sources should be provided during training.

Figure 8: Timing of carbohydrate (CHO) intake and glycogen resynthesis.

Figure 8: Timing of carbohydrate (CHO) intake and glycogen resynthesis.

(Adapted from Burke et al. (2004) with the authorization of the Journal of Applied Physiology).

34Several CHO ingestion strategies are often noted: either the athletes prefer to eat solid, sugar-rich foods as part of their main meals, or else several snacks are offered during the different days of training. Studies interested in the 24-hour recovery period have shown that large meals based on complex carbohydrates twice a day or carbohydrate-based snacks repeated seven times per day, have equivalent power to reconstitute muscle glycogen stores (Costill et al. 1981). More recently, similar results were found for high-performance athletes ingesting four complex carbohydrate-based meals per day or 16 snacks, one per hour (Burke et al. 1996). In this last study, although the glycogen resynthesis rates were similar in both conditions, the blood glucose and insulin concentrations were different over the course of the 24 hours (Burke et al. 1996). In addition, very high rates of glycogen synthesis have been reported over the first 4 to 6 hours of recovery when high quantities of CHO were ingested at 15 to 30 minute intervals (Doyle et al. 1993; van Hall et al. 2000; van Loon et al. 2000; Jentjens et al. 2001). These high rates were attributed to the maintenance of insulin and blood glucose levels, as a result of this dietary protocol. The apparent conflict between these last results seems to reside in the fact that the concentrations are not compared to those obtained in protocols where several CHO-based snacks are offered to athletes. It seems, however, that the maximal rate of glycogen resynthesis measured during recovery, is obtained for athletes consuming 0.4 g.kg-1 body weight every 15 minutes (i.e. 120 g CHO per hour for a 75 kg subject) over the four hours immediately following completion of exercise (Doyle et al. 1993, Fig. 9). In addition, the authors indicate in this study that glycogen resynthesis is not comparable depending on the type of exhausting exercise performed (concentric-contraction or eccentric-contraction) over the previous 48 hours. Indeed, glycogen restoration is 25% lower when exercise involved eccentric contraction compared to concentric contractions. In line with the importance of the timing of ingestion of CHO, it is of note that glucose penetration into cells is insulin-dependent, requiring specific transporters (GLUTs) [Williams, 2004, Fig. 10]. During exercise, insulin and muscle contraction stimulate glucose capture in the muscles via GLUT-4 transporters (Holloszy and Hansen, 1996). Even if a dissociated and cumulative effect of insulin and muscle contraction exists, the mechanisms leading to translocation of GLUT-4 transporters seem to be distinct (Nesher et al. 1985). Muscle contraction and insulin favour the recruitment of GLUT-4 from different intracellular pools (Thorell et al. 1999). In rats, it has been suggested that the increase in muscle GLUT-4 protein levels after a strenuous day’s exercise is responsible for the improved glycogen synthesis capacity of the muscle, as compared with sedentary rats (Richter et al. 1989). More recently, in a population of eleven cyclists McCoy et al. (1996) investigated the influence of GLUT-4 transporters on restoring glycogen stores after two hours’ pedalling at 70% of VO2max, followed by 4 × 1 minute bursts at 100% VO2max, with two minutes’ recovery between bouts. These authors showed that high concentrations of GLUT-4 correlated significantly with the highest levels of glycogen resynthesis during the six-hour post-exercise recovery period (r = 0.63, P<0.05). In addition, the increase in permeability of the muscle membrane to glucose, in post-exercise conditions, is due to the number of glucose transporters integrated in the plasma membrane, and probably, to the increase in intrinsic transporter activity (Ivy and Kuo, 1998). In this context, Goodyear et al. (1990) found that, on an isolated skeletal muscle plasma membrane, the rate of glucose transport was quadrupled immediately after exercise, while the number of glucose transporters was only doubled. Thirty minutes after exercise, glucose transport was approximately halved while the number of glucose transporters associated with the plasma membrane decreased by just 20%. After two hours’ recovery, the transport and number of transporters at the level of the plasma membrane had returned to basal pre-exercise levels. Very interestingly, the decreased time for glucose transport observed by Goodyear et al. (1990), is identical to the initial triggering time for insulin in the glycogen synthesis phase described by Price et al. (1996) [see Fig. 10].

Figure 9: Rate of muscle glycogen resynthesis over the four to ten hours following the end of exercise. Use of low-osmolarity maltodextrin (approximately 1.6g.kg-1. h-1).

Figure 9: Rate of muscle glycogen resynthesis over the four to ten hours following the end of exercise. Use of low-osmolarity maltodextrin (approximately 1.6g.kg-1. h-1).

(Adapted from Doyle et al. (1993) with the authorization of the Journal of Applied Physiology).

Figure 10: Glucose transport and transporters in muscle fibres.

Figure 10: Glucose transport and transporters in muscle fibres.

(Adapted from Williams et al. (2004), with the authorization of Science et Sports.

3.2.3 Influence of the quantity of carbohydrates consumed

35The first studies investigating quantities of carbohydrate consumed during post-exercise recovery date from 1981 (Costill et al. 1981). These authors report that consuming 150 to 600 g of CHO per day induced greater replenishment of glycogen stores over a 24-hour period than lower CHO quantities. A few years later, it was shown that the intake of 1.5 g CHO per kilogram of body weight over the two hours following an exhausting exercise induced an appropriate rate of glycogen resynthesis. This rate was not improved when the CHO quantity was doubled (i.e. 110 g CHO per hour for a 75 kg subject) [Ivy et al. 1988b]. In addition, Sherman and Lamb (1988) were similarly able to show that no difference was recorded with post-exercise CHO quantities of 460 or 620 g per day. In contrast, doses of 160 and 360 g per day induced significantly lower resynthesis when comparing muscle glycogen levels before and after exercise (Fig. 11).

36The quantity of carbohydrates to be consumed during recovery after exercise is often questioned. Thus, different energy drinks have been marketed to maintain athletes’ plasma and blood volumes. As part of this, Criswell et al. (1991) tested the influence of a drink at 7% glucose (and containing electrolytes) on the levels of haematocrit and haemoglobin after a football match in comparison with a drink containing no glucose. The data obtained from 44 football players showed that the energy drink allowed plasma volumes to be stabilized during recovery, while the non-glucose drink with electrolytes did not allow maintenance of blood volume (i.e. a 5% reduction in plasma volume). However, the energy drink did not influence the drop in anaerobic performance.

Figure 11: Glycogen resynthesis after exhausting exercise. Using four concentrations, low level of CHO (160 and 360 g.d-1) or very rich in CHO (460 and 620 g.d-1).

Figure 11: Glycogen resynthesis after exhausting exercise. Using four concentrations, low level of CHO (160 and 360 g.d-1) or very rich in CHO (460 and 620 g.d-1).

*: significantly different from the “160” condition (P<0.05).
**: significantly different from the “360” condition (P<0.05).
(Adapted from Sherman and Lamb (1988), with the authorization of
Lamb & Murray Eds).

3.2.4 Co-ingestion of carbohydrates and proteins

37For a few years, the association of carbohydrates (CHO) with proteins (PRO) has been suggested to improve the speed of glycogen resynthesis. This seems to be linked to induction of higher levels of insulin secretion by the combination than those provoked by CHO alone (Pallotta and Kennedy, 1968). Currently, somewhat contradictory results have been obtained regarding the potential benefit of associating CHO and PRO, the differences obtained might be attributable to the experimental protocol itself, to the frequency of supplementation or to the quantities of CHO and PRO offered to athletes. For example, in studies where benefits with regard to glycogen resynthesis were found for the combination of CHO with PRO, subjects were fed every two hours (Zawadzki et al. 1992; Ivy et al. 2002). Studies which did not show any effect of the addition of proteins on glycogen resynthesis often used renutrition intervals of between 15 and 30 minutes (Tarnopolsky et al. 1997; Carrithers et al. 2000; van Hall et al. 2000; Jentjens et al. 2001). In addition, in some of these studies, very high quantities of CHO were administered (van Hall et al. 2000; Jentjens et al. 2001), while in others, a low proportion of protein was added (Tarnopolsky et al. 1997; Carrithers et al. 2000). Independent of the experimental procedures used, it seems obvious that CHO-rich post-exercise nutrition at very frequent intervals reduces the benefit of protein supplementation during recovery (see summary in table 1).

Table 1: Comparison of studies where proteins (PRO) were added to carbohydrates (CHO) in the diet consumed during recovery.

Table 1: Comparison of studies where proteins (PRO) were added to carbohydrates (CHO) in the diet consumed during recovery.

*: Indicates that the addition of proteins to carbohydrates allowed significant muscle glycogen resynthesis during post-exercise recovery.

38Adding proteins to carbohydrates during recovery aims primarily to increase insulin production. This hormone is determinant for glycogen synthesis, acting both on glucose penetration into muscle fibres and on the activity of glycogen synthase, the limiting enzyme in glycogen synthesis. In most cases, consuming a mixture of CHO and PRO should allow a more marked insulin response. In this context, the first study showing the efficacy of the combination was carried out in athletes after two hours’ ergocycle training following 12 hours’ fasting (Zawadzki et al. 1992). Glycogen resynthesis was evaluated four hours after the consumption of solutions containing 112 g CHO, 40.7 g PRO or a mixture of CHO and PRO. The results of this study showed that the amount of glycogen formed per hour is significantly greater in athletes consuming the mixture of CHO and PRO. These results have, however, been questioned, since the quantity of CHO absorbed during recovery was not optimal. Thus, when using optimal CHO concentrations, van Hall et al. (2000) were not able to show a beneficial effect of adding proteins to CHO on glycogen resynthesis. In 2002, Ivy et al. Showed that after exhausting ergocycle training, intakes (spaced every two hours) of a mixture containing both CHO and proteins induced an increase in muscle glycogen resynthesis. In the same context, Williams et al. (2003) got eight endurancetrained cyclists to perform 2 hours’ of ergocycle at 65-75% VO2max, followed, after two hours’ recovery, by a limit-time at an intensity of 85% of VO2max. During recovery from this, CHO alone or a mixture of CHO and PRO was administered immediately after exercise and two hours later. Results show a significant improvement (128%) in muscle glycogen resynthesis for the “CHO–PRO” condition. As indicated in Figure 12, the solution composed of CHO and PRO allowed improvement of the time to exhaustion. A single cyclist showed lower performance in the “CHO–PRO” condition. All the others significantly improved their performances, the times to exhaustion being 31 minutes in the “CHO–PRO” condition and only 20 minutes with “CHO alone”.

Figure 12: Individual and average times to exhaustion for cyclists. XSB: average, CHO alone; XCHO-PRO: average, CHO-PRO.

Figure 12: Individual and average times to exhaustion for cyclists. XSB: average, CHO alone; XCHO-PRO: average, CHO-PRO.

(Adapted from Williams et al. (2003) with the authorization of the Journal of Strength and Conditioning Research).

39A final recent study (Berardi et al. 2006) studied the effect of one hour of against-the-clock cycling in six experienced cyclists. The study subjects then ingested different meals and solutions, immediately, one or two hours after exercise. The nutritional composition was as follows: (C + P: carbohydrate + proteins; CHO: carbohydrate; placebo: solid food placebo). After six hours’ recovery, a second one-hour against-the-clock trial was performed. Various muscle biopsies were taken pre- and post-exercise to quantify glycogen resynthesis (Fig. 13). Although cycling performances were similar over the two trials (P = 0.02), the rate of resynthesis of muscle glycogen was greater (+ 23 %) in the “C + P” condition than in the “CHO alone” condition. This final result has an undeniable impact: when post-exercise nutrition must be spaced out and when two exercise periods are to be performed with only a small recovery period, the combination of carbohydrates and proteins probably has great advantages with regards to increasing the speed of glycogen resynthesis.

Figure 13: Muscle glycogen resynthesis in the Vastus Lateralis over a 6-hour recovery period following 60 min of exhausting exercise. C + P: meal and solution rich in carbohydrate and proteins; CHO: meal and solution rich in carbohydrate; Placebo: solid meal with placebo carbohydrates.

Figure 13: Muscle glycogen resynthesis in the Vastus Lateralis over a 6-hour recovery period following 60 min of exhausting exercise. C + P: meal and solution rich in carbohydrate and proteins; CHO: meal and solution rich in carbohydrate; Placebo: solid meal with placebo carbohydrates.

*: significant difference with the CHO and Placebo conditions (P<0.05).
(Adapted from Berardi et al. (2006) with the authorization of
Med Sci Sports Exerc).

40Recommendations for carbohydrate consumption during recovery

41■ Immediate recovery after exercise (0 to 4 hours): 1.0 to 1.2 g.kg-1.h-1 consumed at frequent intervals (Jentjens and Jeukendrup, 2003)

42■ Recovery over a day: moderate to strenuous endurance training: 7 to 12 g.kg-1.day-1 (Tarnopolsky et al. 2005).

43■ Recovery over a day: severe exercise programme (> 4 to 6 hours per day): 10 to 12 g.kg-1.day-1 (Ivy et al. 1988b).

44■ Carbohydrate-rich meals are often recommended during recovery. The addition of proteins (meat, fish, eggs etc.) to the usual diet inevitably allows faster muscle glycogen resynthesis. Add 0.2 to 0.5 g of protein per day and per kilo to carbohydrates, in a 3:1 ratio (CHO: PRO). This is critical when the athlete’s training sessions are twice daily and/or very prolonged over time (Berardi et al. 2006; Ivy et al. 2002)

45■ When the period between training sessions is less than eight hours, the athlete must consume carbohydrate as soon as possible after exercise in order to maximize glycogen reconstitution. There is an observable advantage to splitting CHO intakes over the early recovery phase, particularly when the meal time is not soon (Ivy et al. 1988a).

46■ For longer recovery periods (24 hours), the athlete must organize the contents and timing of meals, as well as the CHO content of snacks, in line with what is practical and comfortable relative to his usual habits and schedule. It must be remembered that no difference was observed, with regard to glycogen replenishment, when carbohydrates are taken either as solids or in liquid form (Burke et al. 2004).

47■ Carbohydrates with moderate or high glycaemic indices supply energy rapidly for glycogen resynthesis during recovery, and should therefore constitute the main choice in post-exercise energy-restoring menus (Burke et al. 1993). The quantities ingested are crucial for muscle glycogen resynthesis. Athletes who do not consume enough calories often have difficulties reconstituting their glycogen stores: these populations must be carefully observed so as not to induce too high a deficit (Kerksick et al. 2008).

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