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Nutrition: Section Articles

Recovery Nutrition: Timing and Composition after Endurance Exercise

Millard-Stafford, Melinda; Childers, W. Lee; Conger, Scott A.; Kampfer, Angela J.; Rahnert, Jill A.

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Current Sports Medicine Reports: July-August 2008 - Volume 7 - Issue 4 - p 193-201
doi: 10.1249/JSR.0b013e31817fc0fd
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Abstract

INTRODUCTION

Exercise training is undertaken to achieve an optimal physiological adaptation from the functional overload of the exercise stimulus. This is true for elite athletes, recreational sport participants, and even general health purposes (e.g., prevention of sarcopenia in the elderly). To maximize adaptation to exercise training, it has become increasingly apparent that nutritional interventions, particularly if timed optimally, can facilitate the training adaptation (1). Post-exercise nutritional interventions also are aimed at speeding recovery from prolonged strenuous exercise for athletes competing multiple times per day (i.e., soccer tournaments, tennis matches, track, or swimming preliminary and final heats) or training several sessions per day.

For decades (2), the literature clearly has demonstrated the importance of carbohydrate (CHO) in the athlete's diet. It is recommended that endurance athletes consume approximately 8 g·kg body weight−1·h−1 CHO (~70% of total energy intake) during periods of intense training to facilitate resynthesis of muscle glycogen (1,3) and maintain exercise intensity/performance while improving mood state related to fatigue (4). However, there may be a ceiling effect of 500-600 gm of CHO consumed each day, above which no further increases in resynthesis may occur (5). Compared with fat storage, even when CHO intake is sufficient (1600 kcal or <400 g), muscle glycogen stores remain relatively limited considering that even ultra-endurance exercisers can oxidize up to 1.2 gm of CHO each minute during moderate intensity exercise less than 60% V˙O2max (6). Thus it is not surprising that traditional nutritional practices immediately after endurance training have emphasized CHO intake as the priority to restore muscle glycogen effectively and to improve the quality of subsequent training and competition.

In addition to the replenishment of muscle glycogen, there are other major objectives of postexercise nutrition that have been examined in the literature. These include restoration of body fluid balance, improved performance (or training stimulus) in subsequent exercise tasks, increased protein synthesis, attenuated protein degradation, and attenuated muscle damage/muscle soreness. The aim of this review is to focus specifically upon the effects of macronutrient intake (e.g., CHO and protein) ingested during the immediate postexercise (recovery) period after endurance exercise. The reader is referred to other excellent reviews regarding postexercise nutrition after resistance training (7-9) and accrual of muscle mass, particularly as it relates to the timing of protein intake. While such recommendations do not exclude the possibility of similar responses from nutritional interventions after endurance exercise, it was recently recognized that the stimulus of endurance versus resistance training may result in different signaling mechanisms within skeletal muscle (10). It would be naïve to assume that research focusing on nutritional impact on protein synthesis after resistance exercise would be identical to recovery from endurance training. Thus this review is limited specifically to postexercise macronutrient intake and its effect upon muscle glycogen resynthesis, subsequent endurance performance, and attenuated muscle damage/soreness after endurance exercise.

MUSCLE GLYCOGEN RESYNTHESIS

The postexercise recovery period is characterized by enhanced glucose uptake into muscle, which early on appears to be noninsulin dependent, followed later by a period of increased insulin sensitivity (11). The molecular mechanisms underlying this phenomenon likely include postexercise upregulation of glucose transporter (GLUT-4) gene and protein expression (12) and exercise-induced elevation of glycogen synthase activity (13). Thus CHO availability at the correct time during exercise recovery is critical for replenishing muscle glycogen. Notably, it is possible for muscle glycogen to be restored to levels above resting when CHO are consumed shortly after exercise (2). However, there appears to be a "window of opportunity" soon after exercise such that if CHO feedings are delayed by 2 h, the glycogen resynthesis rate is attenuated (14).

The dosage of CHO believed (optimally) to restore muscle glycogen early in recovery is at least 1.2 g·kg body weight−1·h−1 up through a 4-h period (14). The form (liquid, gel, and solid) or type of CHO (monomers of glucose, sucrose, or polymeric) that optimally results in greater glycogen resynthesis is not well documented. However, since insulin drives muscle glycogen synthesis several hours after cessation of exercise, it would seem plausible that a higher glycemic index CHO could prove beneficial. Auhlin (15) compared muscle resynthesis rates with a hypotonic (85 mOsm·kg−1) polymeric glucose (potato starch) versus isocaloric glucose monomer beverage (osmolality of 350 mOsm) following glycogen-depleting exercise and reported 67% greater rate of glycogen resynthesis with the hypotonic beverage at 2-h recovery. Because insulin and blood glucose were similar, the authors suggested a faster uptake of CHO across the gut wall and possibly matched by a facilitated transport into muscle. However, the higher synthesis rates obtained with hypotonic polymer CHO versus monomer CHO were not sustained after 2 h. Moreover, other studies examining preexercise feedings (3-4 h) on muscle glycogen (but not specifically associated with recovery from exercise) suggest improved muscle glycogen synthesis with high-glycemic CHO but subsequently offset by greater utilization during exercise 4 h later (16). Thus, there is no clear recommendation for a specific type or form of CHO to optimize storage of glycogen during recovery.

The rise in plasma insulin in response to CHO or protein consumption activates insulin receptor-mediated signaling pathways to stimulate glycogen synthesis and/or protein synthesis (Fig. 1). Moreover, blood borne proteins/amino acids can act directly on signaling molecules within the muscle cell that also stimulate protein synthesis. Thus it is not surprising that recent studies on the impact of CHO coingested with protein (17) have focused upon the measurement of phosphorylation states of enzymes involved in the pathways leading to both protein or glycogen synthesis (Fig. 1). Circulating insulin binds to the insulin receptor activating PI3K, which in turn, activates Akt/PKB and mTOR signaling molecules. The Akt/PKB pathway releases inhibition of glycogen synthase to promote glycogen synthesis as well as increase protein synthesis through mTOR. Increased plasma concentrations of branched chain amino acids (BCAA), particularly leucine, also can stimulate insulin release; however, BCAA ingestion during and after 1-h cycling did not affect insulin but improved net protein balance (18). Therefore, BCAA (valine, isoleucine, leucine) may act via other insulin-independent pathways to stimulate protein synthesis (19,20) illustrated in Figure 1. While it is tempting to speculate about such molecular changes with protein (e.g., BCAA) added to CHO, the translation regarding meaningful changes in glycogen synthesis merits additional studies such as those done by Ivy et al. (17).

Figure 1
Figure 1:
Influence of exercise and nutrition on protein synthesis and glycogen synthesis. Exercise increases the sensitivity of the insulin receptor (I-R) to insulin while ingestion of carbohydrates and proteins increase levels of circulating insulin. Upon binding to its receptor, insulin activates intracellular signaling cascades leading to protein synthesis and glycogen synthesis. In addition, specific amino acids (BCAA) may have direct effects on pathways involved in protein synthesis. Akt/PKB- Protein kinase B; AMPK- AMP-activated protein kinase; BCAA- Branched-chain amino acids; eIF4E-eukaryotic initiation factor 4E; eIF2B- eukaryotic initiation factor 2B; GS- Glycogen synthase; GSK-3B- Glycgen synthase kinase 3B; MAPK- mitogen activated protein kinase; ERK1/2- extracellular regulated kinase 1/2; p38- protein 38- 38kDa stress-activated protein kinase (SAPK); mTOR- mammalian target of rapamycinp; PI3-K- phosphatidylinositol 3-kinase; p70s6K- 70kDa ribosomal subunit 6 kinase; rsp6- ribosomal subunit protein 6; TSC1/2-tuberous sclerosis complex 1/2 4E-BP1- eIF-4E-binding protein 1.

Foods such as dairy products (e.g.,milk) have been compared with specialty sport beverages. Van Loon (21,22) observed different types of protein coingested with CHO can increase the insulinemic profile during exercise recovery. Casein may have greater insulinemic response compared with CHO alone (23). Whether enhanced insulin response translates into greater muscle glycogen both short-term and sustained long-term is a key question.

In general, results from investigations (Table 1) comparing CHO with CHO+ protein beverages ingested during recovery are mixed, at best, when examining muscle glycogen resynthesis, particularly when calories are not matched in the design (24-29). When CHO intake is higher than recommended levels of 1.2 g·h−1, no significant difference in muscle glycogen is found compared with higher calorie CHO with added protein (30,31). Three studies (24,26,32) indicated a muscle-glycogen resynthesis benefit with CHO+ protein postexercise, but only two used a CHO treatment that was isocaloric. Although Williams (32) found greater muscle glycogen and performance improvements, the CHO was a relatively low dosage and represented approximately 30% of the calories obtained with the CHO+ protein treatment. In addition, enhanced glycogen resynthesis has not necessarily translated into performance benefits (24). Exercise intensity dictates glycogen stores remaining after exercise, and in turn, the magnitude of muscle glycogen depletion has an effect upon the rate of glycogen resynthesis (11). It also is unclear whether there is an intensity-specific effect regarding the test used during the "depletion exercise" on glycogen resynthesis rates and then subsequent performance in the postrecovery test.

TABLE 1
TABLE 1:
Summary of investigations on the effect of carbohydrate (CHO) and CHO+ protein (PRO) beverages on glycogen synthesis after recovery from exercise.

Recent findings challenge the dogma that athletes always benefit from attempts to enhance muscle glycogen synthesis following endurance training. A "train low, compete high" concept of muscle glycogen has been put forward since multiple markers (resting glycogen, oxidative enzymes) suggesting improved training adaptation were observed when muscle glycogen was kept below normal during training sessions in untrained subjects, but this has not yet been verified in trained subjects (33). Hawley et al. (1) caution that it is premature to extend this recommendation to athletes due to the potential for their inability to perform the rigors of training when muscle glycogen becomes chronically depleted.

To summarize, in order to replenish glycogen after endurance exercise, the optimal blend of CHO or protein is not well characterized. The dosage of CHO believed to restore muscle glycogen optimally early in recovery (<4 h) appears to be in the range of 1.2-1.5 g·kg body weight−1·h−1. Determinants of glycogen synthesis rate during recovery could be the caloric content of the beverage and/or the intensity of the preceding glycogen depleting exercise. Whether small increases in muscle glycogen resynthesis can be sustained after 4 h and into the next day also remain to be verified. If sufficient CHO intake cannot be achieved postexercise, the addition of protein to meet this minimum caloric intake appears to be at least as good with possible additional short-term benefits. The utility of milk-based products or other protein-containing beverages or foods are other options athletes could consider during recovery from training or competition.

ENDURANCE EXERCISE PERFORMANCE

Evidence whether enhanced muscle glycogen resynthesis from optimal postexercise nutrition unequivocally translates into performance benefits is surprisingly limited in the prevailing literature. This is particularly true for studies which examined if protein coingested with CHO increase performance over and above that of CHO alone. One of the previously mentioned studies that reported improved ride time to fatigue with the recovery ingestion of CHO+ protein was biased by caloric imbalance with significantly greater calories provided during the CHO+ protein trial (32). Saunders (34) demonstrated a performance benefit, but consumption also occurred during exercise, and in the latter case treatments were not isocaloric. Because most experiments often have subjects initiate the exercise protocol in a fasted state, the lack of an isocaloric treatment is an important limitation since caloric imbalance can have multiple, subtle influences (35). Moreover, the fact that cyclists typically do not fast before competition or training limits the findings in terms of generalizability and application to real-world practice. Whether small acute changes in insulin response or glycogen synthesis extend to meaningful performance differences over longer periods of time (24 h) also is not well documented (27).

The method selected to assess exercise performance may yield conflicting conclusions. It appears that when exercise to fatigue protocols are used to assess performance, ergogenic benefits are more likely to be observed (32,34,36,37), and even these sometimes fail to elicit performance benefits with calorically matched protein coingested with CHO (38,39). For example, chocolate milk compared with an isocaloric CHO+ protein recovery drink resulted in better performance as assessed by time to exhaustion at 70% V˙O2max (39), but higher calorie chocolate milk was not superior to a traditional sports drink. Utility of this type of protocol does not translate into real-world athletic performance and is well recognized for greater variability (40). Studies that have used a fixed task (e.g., 5-km run) to assess performance with an isocaloric comparison group (41-43) have not demonstrated a short-term performance benefit with protein coingested with CHO. Thus additional comprehensive studies that combine biomarkers (glycogen, muscle damage) with reliable performance tests are still too few in number.

MUSCLE DAMAGE/SORENESS

When individuals perform unaccustomed exercise, particularly of high intensity or consisting of eccentric muscle actions (e.g., downhill running), considerable muscle soreness or damage can occur. It has been suggested (35,41) that nutritional intervention during the immediate recovery period following endurance exercise might attenuate muscle damage and soreness. This could have a profound impact for previously inactive individuals who become discouraged because of the discomfort that accompanies the initiation of an exercise program. Although several studies have documented attenuation of indirect markers of exercise-induced muscle injury when adding protein/amino acids to a CHO supplement (35,41-43), this finding has not been consistent or verified with a protocol explicitly designed to elicit muscle damage (44) (Table 2).

TABLE 2
TABLE 2:
Summary of selected protein with carbohydrate treatments during recovery from endurance exercise and attenuation of exercise-induced muscle damage/soreness.

A recent study by Green et al. (44), however, examined such a scenario. Recreationally active women performed 30 min of downhill running, a protocol known to result in muscle damage, soreness, and functional loss in muscle strength. Immediately after and at 30 and 60 min, either a placebo, CHO (1.2 g·kg body wt−1), or CHO+ protein (with an additional 0.3 g·kg body wt−1) was ingested across three different groups. This study was novel in that it focused exclusively on women and was designed specifically to elicit muscle damage before the recovery nutritional intervention. Previous reports indicate that muscle glycogen resynthesis may be impaired after eccentrically invoked muscle damage (45). No advantage was observed with protein added to CHO in the restoration of muscle function (quadriceps strength), muscle soreness, or indirect markers of muscle damage such as plasma creatine kinase (CK). In fact, the validity of CK as evidence of muscle damage is weak (46) without other corroborating evidence of functional decrements in muscle performance. Therefore, none of the nutritional interventions (CHO or CHO+ protein) yielded any benefit over the subsequent 3 d compared with placebo. Thus when there is true myofibrillar damage resulting in functional impairments, the timing of recovery nutrition, no matter how optimal, may have limited impact.

This is in contrast to previous reports (34,35,41,47) of attenuated CK after exercise when protein is coingested with CHO, despite this observation not being consistently reproducible (37,42,44). Although exercise performance was improved along with lower CK in two studies, the treatments were not isocaloric, and consumption also occurred during the initial exercise bout (34,35). Another limitation was that muscle damage elicited from prolonged cycle ergometry was not verified with other functional markers of muscle damage. In an unpublished investigation depicted in Figure 2, we (37) attempted to replicate the original study (33) to determine whether markers of muscle damage would be attenuated with a 6.5% CHO - 1.5% whey protein hydrosylate versus traditional 6% CHO sports drink. Plasma myoglobin and CK were not elevated to an extent indicative of muscle damage, and performance of anaerobic power (Wingate), maximal voluntary strength, or muscle soreness remained unaffected by adding protein. Thus, CHO+ protein had no effect upon these corroborating markers despite a trend to extend cycling endurance capacity at 85% V˙O2max by approximately 25%. This suggests that potential performance benefits might not be explained by attenuated muscle damage in studies using a ride to fatigue test, and therefore, the possibility cannot be excluded that greater caloric intake contributes to performance benefits.

Figure 2
Figure 2:
Schematic of a performance testing protocol representative of recovery nutrition intervention studies (34,37,47). Note that additional tests (e.g., blood parameters, perceptual ratings) could occur at time points indicated by the bar along with performance measures such as MVC (maximal voluntary contraction). RTF = ride to fatigue protocol.

To examine adequately whether a post-exercise nutritional intervention can attenuate muscle damage or soreness is difficult because of research design issues. Human protocols are limited by the ability to establish pretest controls as well as minimize order effects. If a within-subject design is used, the protocol must elicit similar damage for each treatment arm. Because there is a known repeated bout protective effect that occurs after initial damaging exercise (48), this presents methodological challenges related to order effects. The other design option is to match subjects carefully and use a between-group design with one treatment per subject as used by Green et al. (44) However, greater inter-individual subject variability influences the response to the exercise or nutritional treatment.

Available studies have inherent limitations, making interpretation of findings difficult. In trained runners, muscle soreness and CK attenuation were examined using both of these research designs (42). Neither the within- nor the between-subject studies observed attenuated CK or performance benefits when protein was coingested with CHO after intense run training. However, in both study designs, a lower rating of muscle soreness was observed (Table 2). In that study, the CHO+ protein beverage was easily distinguishable from CHO, which made blinding of subjects problematic. While there is evidence from different laboratories that perceptual soreness responses after endurance exercise may be attenuated (35,41-43,47), the prevailing evidence that muscle fiber damage per se also is minimized is not strong. Thus it is uncertain whether protein added to CHO reduces the likelihood of muscle damage or muscle soreness. Certainly, there are no contraindications for ingesting both CHO and protein in the immediate recovery period, and it makes sense that food and beverages with both macronutrients can be effective. But the optimal form of protein and requisite amount to be included with CHO (after endurance exercise) remain to be investigated (21).

CONCLUSION

Consumption of macronutrients, particularly CHO and possibly lesser amounts of protein, within the first few hours after endurance exercise can enhance muscle glycogen resynthesis rates. A target of 1.2-1.5 g·kg body weight−1·h−1 CHO, broken into frequent dosages every 15-20 min, has been suggested. This rate of CHO intake could be sustained with either liquid or non-liquid forms rich in CHO and/or protein for maximizing muscle glycogen. Milk-based products may be effective in recovery nutrition. There is some evidence that perceived muscle soreness might be attenuated. Additional advantages of protein-containing beverages or food in facilitating possible muscle damage repair or increasing subsequent endurance training intensity or performance remain to be verified. However, there are no contraindications to the postexercise consumption of either milk or specialty CHO formulas with amino acids.

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