Carbohydrate intake and recovery from exercise

Hydrates de Carbone et Récupération après exercice

Clyde Williams *

School of Sport and Exercise Sciences, Loughborough University, Leicestershire LE11 3 TU, UK

Available online 02 August 2004

Abstract

Prolonged heavy exercise, whether as part or training or competition, can only be continued when there is an adequate amount ofcarbohydrate available to fuel muscles and the brain. Fatigue is closely associated with depletion of the limited stores of carbohydrate in themuscle and in the liver. Therefore, it is not surprising that strategies have been developed to ensure that not only are the carbohydrate stores wellstocked before exercise but that they are also restored as soon as possible after exercise. Consuming carbohydrate immediately after exerciseincreases the rate of muscle glycogen resynthesis and also results in greater endurance capacity during subsequent exercise. A recovery dietthat is high in carbohydrate (~10 g kg–1 body mass/day) will allow athletes to restore their exercise capacity on the following day, which is notthe case when they eat a mixed diet with matching energy content. The type of carbohydrate in the recovery diet also has an influence onendurance capacity the following day. A recovery diet that contains low glycaemic index carbohydrates result in a higher rates of fat oxidationand greater endurance running capacity than diets that are contain mainly high glycaemic index carbohydrate foods. Although consumingcarbohydrate–protein mixtures during recovery from exercise increases the insulin response, and possibly glycogen resynthesis rate, thereappears to be no greater recovery of endurance capacity than following the consumption of carbohydrate alone.© 2004 Elsevier SAS. All rights reserved.

Résumé

La poursuite d’un exercice intensif et prolongé n’est possible que dans la mesure où les muscles et le cerveau peuvent disposer des quantitésnécessaires en hydrates de carbone. L’apparition de la fatigue est étroitement associée à l’épuisement des stocks en glycogène musculaire ethépatique. Par conséquent, il n’est pas étonnant que des stratégies aient été élaborées pour s’assurer de la quantité et de la qualité des réservesen glycogène ainsi que de la rapidité de leur reconstitution après l’exercice. Une absorption glucidique après un exercice augmente le taux deresynthèse du glycogène musculaire et a également un effet bénéfique sur les performances à venir. Une ration de récupération, riche enhydrates de carbone (10 g/kg par masse de poids corporel et par jour) permet aux athlètes de reconstituer leur capacité d’exercice le joursuivant, ce qui n’est pas le cas quand ils absorbent une alimentation diversifiée, répondant aux besoins énergétiques. La nature de l’hydrate decarbone du régime de récupération a également une influence sur la capacité de résistance le jour suivant. Une ration de récupération contenantdes hydrates de carbone à index glycémique bas d’index augmente la capacité des graisses, d’où une amélioration des qualités d’endurance parrapport à un régime à base d’hydrates de carbone à index glycémique élevé. Bien que la consommation d’un mélange hydrates decarbone–protéines pendant la phase de récupération augmente la sécrétion d’insuline, et probablement le taux de resynthèse du glycogène, ilne semble pas que la capacité de résistance soit supérieure à celle qui suit une absorption d’hydrates de carbone seuls.© 2004 Elsevier SAS. All rights reserved.

Keywords: Carbohydrate; Exercise; Fatigue; Recovery

Mots clés : Hydrate de carbone ; Exercice ; Fatigue ; Récupération

* Tel.: +44-1509-226309; fax: +44-1509-226300. www.sportsnutrition.lboro.ac.ukE-mail address: c.williams@lboro.ac.uk (C. Williams).

Science & Sports 19 (2004) 239–244

www.elsevier.com/locate/scispo

© 2004 Elsevier SAS. All rights reserved.doi:10.1016/j.scispo.2004.05.005

Athletes preparing for competition must recover quicklyin order to cope with heavy training. Recovery from exercisedepends on the nature of the exercise, its intensity, durationand the time available for recovery. Successful recoveryinvolves the completion of several key physiological andmetabolic processes that act in concert to prepare the athletefor the next bout of exercise. Assuming that the athlete hasnot suffered injury or severe muscle soreness then the keycomponents of recovery are rehydration and resynthesis ofthe body’s carbohydrate stores. Carbohydrate is stored as apolymer of glucose called ‘glycogen’ mainly in the liver andin skeletal muscles. This fuel store is of limited capacity andrepresents only about 2% of the energy stored in the body asfat.

As exercise intensity increases when, for example, goingfrom walking to running, the fuels recruited to provide thesubstrate for energy production in working muscles changefrom mostly fatty acids to mainly muscle glycogen and somefatty acids [1,2]. The contribution of glycogen to energyproduction during moderate to high intensity exercise isnecessary because glycogen can be degraded rapidly to pro-duce ATP both aerobically and anaerobically. The oxidationof fatty acids cannot provide ATP fast enough to support thecontractile activity of skeletal muscles even though theyprovide more ATP per unit than the degradation of the sameamount of glycogen.

Fatigue during prolonged exercise is closely associatedwith the depletion of muscle glycogen stores. During pro-

longed continuous running, depletion of glycogen occursfirst in the type 1 fibres (slow contracting, slow fatiguing) andthen in the type 2 fibres (fast contracting, fast fatiguing).During prolonged intermittent exercise, glycogen loss in thetype 2 fibres appears to be more rapid than in the type 1 fibres[3]. Nicholas et al. [4] used an intermittent running protocolthat was designed to be similar to the activity pattern that iscommon in football (Fig. 1). The 90 min intermittent exercisetest (LIST) includes 66 timed sprints over 15 m. Sprint timeswere significantly slower during the last 15 min than duringthe first 15 min of the LIST [3]. Therefore, it is not surprisingthat there was a significant decrease in muscle glycogenstores during the 90 min LIST. However, drinking a carbohy-drate–electrolyte solution throughout the LIST resulted inless glycogen degradation in the muscle sampled, especiallythe type 2 fibres, than when the participants consumed anon-carbohydrate placebo [3]. This slower rate of glycogendegradation or ‘glycogen sparing’ may help explain the im-proved endurance capacity when football players completed75 min of the LIST and then sprinted the 20 m shuttles tofatigue (Fig. 2). They ran 33% longer when they consumed acarbohydrate–electrolyte solution throughout the 75 min ofthe LIST than when they consumed a placebo [5]. Thesestudies on prolonged intermittent high intensity running con-tribute to the growing literature that suggest that those par-ticipating in sports that involved prolonged intermittent exer-cise such as football may benefit by consuming well

6x 15 min periods of shuttle running

Warm-Up Rest Rest Rest Rest Rest

Walk Walk Walk Sprint Run 95%

V02mx

Run 95% V02mx

Run 95% V02mx

Run 55%

V02mx

Run 55%

V02mx

Run 55% V02mx

Activity during one 15 min period

Fig. 1. The Loughborough Intermittent Shuttle Test (LIST).

240 C. Williams / Science & Sports 19 (2004) 239–244

formulated sports drinks before and during match-play[6–9].

Recovery of muscle glycogen stores underpins the recov-ery of endurance capacity for moderate to high intensityexercise. Low intensity exercise can be pursued when muscleglycogen stores have not been restored fully but duration andintensity will be limited by the inadequacy of the carbohy-drate stores. Therefore, eating sufficient carbohydrate fol-lowing prolonged heavy exercise is an essential part of anyrecovery strategy. The amount of carbohydrate ingested isimportant because earlier studies have shown that a dailycarbohydrate intake of 4 g/kg body mass or less is too little toreplete glycogen stores between each day’s exercise [10,11].

A 24 h recovery diet that provides 9–10 g/kg body mass ofcarbohydrate is effective in restoring endurance running ca-pacity [12]. Fallowfield et al. [17] reported that when runnerscompleted 90 min of treadmill running (70% VO2max) andthen were fed either a high carbohydrate (9 g/kg body mass,CHO) or isocaloric mixed diet (6 g/kg body mass, CHO)during a 22 h recovery only those runners on the high CHOdiet were able to match their previous day’s run time of90 min. The early study of Jacobs et al. [13], describing themuscle glycogen utilisation during a professional footballmatch, concluded that high carbohydrate diet is essential forsuccessful recovery. Using the same dietary interventionNicholas et al. [35] reported that intermittent running capac-ity was also restored following the consumption of a highcarbohydrate (10 g/kg body mass) recovery diet. Therefore,this nutritional intervention can be adopted by football play-ers so that they can train or compete the next day.

The process of glycogen resynthesis begins immediatelyexercise ends. The uptake of glucose by the formerly activemuscle fibres is accelerated by the appearance at the musclemembrane of specific glucose transporter proteins (GLUT4). The GLUT 4 proteins are released from storage vesiclesin the cytoplasm of the muscle fibres apparently as a conse-quence of the contractile activity and or, the reduction inglycogen concentration (Fig. 3) [14,15]. They remain in an

active state during the immediate post-exercise period. Theenzyme that speeds up glycogen resynthesis is glycogensynthase, which is activated mainly as a consequence of areduction in glycogen stores. Furthermore, carbohydrate in-take not only provides substrate for glycogen resynthesis, butalso increases insulin concentration that in turn helps prolongthe activity of the glucose transporter proteins. It is suggestedthat the presence of insulin contributes to glycogen resynthe-sis by either extending the time period over which the GLUT4 transporters are active or stimulates the release of moretransporters from a different storage site [15].

Therefore, it is not surprising that consuming carbohy-drate immediately after exercise helps to resynthesize muscleglycogen more rapidly than when food intake is restricted.The early studies on post-exercise glycogen resynthesis rec-ommended that the optimum amount of carbohydrate isabout 1–1.5 g/kg body weight, consumed immediately afterexercise and at 2 h intervals until the next meal (for reviewsee [16]) While these studies on post-exercise synthesis ofmuscle glycogen contribute to a better understanding ofcarbohydrate metabolism during and after exercise, they alsohave practical applications. For example it is quite commonfor athletes to train twice a day with as little as 4–6 h betweentraining sessions. Furthermore, in some sports, athletes par-ticipating in tournaments may have to compete in the morn-ing and then again in the afternoon. Following the recom-mendation to consume carbohydrate immediately afterexercise may help the recovery process, even over a shortperiod of time. Fallowfield and Williams [17] reported thatrunners who had completed a 90 min treadmill run (70%VO2max) were able to exercise for 20 min longer following a4 h recovery during which they consumed the equivalent of1 g/kg body mass of carbohydrate immediately after exerciseand then again 2 h later. Even following the simple recom-mendation to consume about 50 g of carbohydrate immedi-ately after exercise [18] results in greater endurance capacityduring subsequent exercise than consuming only water dur-ing a 4 h recovery period [19]. However, increasing thecarbohydrate intake immediately after exercise may not pro-duce parallel improvements in endurance capacity duringsubsequent exercise. Wong et al. [19] gave a group of runners50 g of carbohydrate (6.5% carbohydrate–electrolyte solu-tion) immediately after 90 min of treadmill running (70%

Prolonged Intermittent High Intensity Exercise

Warm

-15 15 30 45 60 75 +(min)

Exercise time = 75 + min: Total Rest time = 15 min

Modified LIST

Warm up

Loughborough Intermittent Shuttle Running Test (LIST)

IntermittentExercise

Fig. 2. The modified LIST protocol.

Fig. 3. Glucose transport into musle fibres.

241C. Williams / Science & Sports 19 (2004) 239–244

VO2max) and then rehydrated them by providing either wateror a 6.5% carbohydrate–electrolyte solution in sufficientquantity to cover 150% of the body mass lost during theinitial 90 min treadmill run. There was no difference inrunning time to exhaustion when the runners had consumed175 g of carbohydrate or simple 50 g during the 4 h recovery.This latter study confirmed the results of an earlier studyfrom our laboratory where we found no differences in runtime to exhaustion following a 4 h recovery during which therunners ingested the equivalent of either 1 or 3 g/kg bodymass of carbohydrate from a 6.5% carbohydrate–electrolytesolution [20].

A subsequent study that used exactly the same recoveryrehydration procedure showed that there was a significantincrease in muscle glycogen concentration during the 4 hrecovery when the runners ingested the larger amount ofcarbohydrate [21]. These results are paradoxical because itwould be reasonable to expect an improved exercise capacityfollowing short term recovery during which more carbohy-drate was consumed. Possible explanation(s) include a ratelimited uptake of glucose during the recovery period and/oran insulin-induced reduction in the availability and oxidationof fatty acids. The consumption of carbohydrate may besufficient to depress fat oxidation but insufficient to make upthe deficit in substrate provision and so overall there is no netgain in endurance capacity.

When glycogen resynthesis per se is the main objectivethen there appears to be advantages in increasing the post-exercise insulin concentration. Ivy et al. [22–24] wereamongst the first to report that consuming a carbohydrate–protein mixture immediately after exercise increased the rateof post-exercise muscle glycogen resynthesis beyond thatwhich occurs with carbohydrate alone. However, not allauthors report an increase in glycogen resynthesis followingthe ingestion of carbohydrate–protein mixtures immediatelyafter exercise [25–27]. Ivy and colleagues also explored theinfluences of ingesting a carbohydrate–protein mixture (4:1,CHO/Protein) immediately after exercise on subsequent en-durance capacity. In their initial study their subjects per-formed prolonged cycling to deplete muscle glycogen con-centration and then ingested either the carbohydrate–proteinmixture or a sports drink (6% CHO) immediately after exer-cise and again 2 h later. After a recovery of 4 h their subjectscycled to exhaustion at an intensity equivalent to 85%VO2max. The time to exhaustion following the ingestion ofthe CHO–Protein mixture was 55% greater than followingthe ingestion of the commercially available sports drink [28].Unfortunately they did not compare like with like becausethe CHO provided during the recovery period was far greaterduring the CHO–Protein trial than during the Sports Drinktrial. More recently, they showed that when subjects ingesteda carbohydrate–protein mixture before and during exerciseof varying intensities their performance was improved [29].However, the authors were unable to offer a metabolic expla-nation for the improvement in exercise performance follow-ing the ingestion of the supplement.

The type of carbohydrate consumed may also have aninfluence on the recovery process and performance duringsubsequent exercise. Consuming carbohydrate before or af-ter exercise results in an insulin-mediated decrease in fattyacid mobilisation and oxidation. Providing carbohydrate toboost or replenish glycogen stores also decreases the contri-bution of fat to energy metabolism and so extra carbohydratemust be oxidised to make up this deficit in substrate supply.Therefore, providing carbohydrate during the recovery with-out producing a large insulin-induced decrease in fatty acidoxidation is an attractive option. Low glycaemic index (LGI)carbohydrates produce a lower insulin responses than whenan equivalent amount of high glycaemic index (HGI) carbo-hydrates are ingested [30]. The consumption of a LGI carbo-hydrate meal, 3 h before exercise, results in a greater rate offat oxidation during subsequent treadmill running (~70%VO2max) than following the consumption of a HGI carbohy-drate meal [31,32]. Eating a LGI carbohydrate meal afterprolonged exercise promotes a greater rate of fat oxidationduring treadmill running 4 h later. However, it does notappear to result in a greater endurance running capacitycompared to a HGI carbohydrate recovery meal even thoughthe insulin responses to the LGI carbohydrate meal are lower(Wu et al. unpublished). However, when the recovery periodwas extended to 22 h then treadmill running time to exhaus-tion at a speed equivalent to 70% VO2max was greater whenrunners consumed a LGI carbohydrate recovery diet thanwhen the consumed an isocaloric HGI carbohydrate diet[33]. On the following morning the runners felt better and therate of fat oxidation during the run to exhaustion was higherafter consuming the LGI carbohydrate recovery diet. Thiswas a surprising result because Burke et al. [34] have shownthat muscle glycogen resynthesis, after a 24 h recovery fromprolonged exercise, was greater when their subjects con-sumed HGI carbohydrate meals than when they consumedLGI carbohydrate meals. However, Burke et al. [34] did notassess the exercise capacity of their subjects after the 24 hrecovery on the two different carbohydrate diets. During therun to exhaustion, following the 24 h recovery, the rate of fatoxidation was significantly greater when the runners con-sumed the LGI diet than when they consumed the HGI diet. Itis reasonable to assume that the greater rate of fat oxidationduring the run to exhaustion would have reduced the rate ofglycogen degradation and so delayed the point at which thislimited carbohydrate store became insufficient to continue tosupport muscle metabolism.

In contrast, the same LGI 24 h recovery diet failed toimprove run time to exhaustion during intermittent highintensity exercise on the day after football players completed90 min of the LIST. Furthermore, the LIST requires frequentsprinting as well as high speed running and so carbohydraterather than fat metabolism is the fuel of choice (Erith et al.unpublished). Nevertheless, our earlier studies showed that ahigh carbohydrate diet during recovery from the LIST resultsin a greater endurance capacity during the subsequent perfor-mance of this intermittent exercise than when participantsconsume an isocaloric mixed diet [35].

242 C. Williams / Science & Sports 19 (2004) 239–244

During multiple sprint sports participants accelerate, turnin different directions as well as slow down and then sprintagain. This activity pattern is not only more demanding thanconstant pace running, cycling or swimming but it alsocauses muscle soreness [36]. The soreness is the result ofmicro-tears in the membranes around muscle fibres and ten-dons. Evidence for the sub-clinical tears in muscle mem-branes is provided by the appearance in the blood of intra-cellar proteins particularly creatine kinase and myoglobin.These proteins are exclusive to the cytoplasm of muscle anddo not normally appear in the blood unless there is somedamage to the muscle membrane. Soreness is often experi-enced for several days after performing unaccustomed exer-cise and this is probably caused by an inflammatory reactionaround the site of the damaged muscle membrane [37]. Insome people soreness can be so severe that it prevents themfrom participating in almost any physical activity for severaldays. This degree of soreness is common during pre-seasonfootball training when players have not trained since theirlast game of the season. Soreness is a common experience forthose sportsmen and women who are returning to trainingfollowing recovery from injury, especially if they attempt todo too much exercise too soon. Different ways of reducingthe soreness have been explored in order to help playersreturn to training more quickly. More recently vitamin Csupplementation has been investigated as a prophylactic [38]and as part of the treatment of muscle soreness [39] withlimited success. The rationale for vitamin C supplementationis based on the realisation that free radicals are released aspart of the inflammatory response to injury. Vitamin C is anantioxidant that can quench the activities of the free radicalsand so reduce their impact on cells and tissue membranes.

This inflammatory response following exercise-induceddamage to skeletal muscle is offered as one explanation forthe reduction in the rate of glycogen resynthesis followingunfamiliar and therefore, demanding exercise [40]. The dam-aged membrane may disrupt the integrity of the glucosetransport process and so slow the delivery of glucose intomuscle and hence delay glycogen resynthesis. Therefore,when soreness is experienced after exercise it is important torecognise that the recovery of muscle glycogen may bedelayed.

In summary, the two most important nutritional interven-tions that contribute to a successful recovery are carbohy-drate and fluid replenishment. These along with adequate rest(sleep) help athletes to train hard and recovery quickly.

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