ebook img

Nutrient timing revisited: is there a post-exercise anabolic window? PDF

0.22 MB·English
Save to my drive
Quick download
Download
Most books are stored in the elastic cloud where traffic is expensive. For this reason, we have a limit on daily download.

Preview Nutrient timing revisited: is there a post-exercise anabolic window?

AragonandSchoenfeldJournaloftheInternationalSocietyofSportsNutrition2013,10:5 http://www.jissn.com/content/10/1/5 REVIEW Open Access Nutrient timing revisited: is there a post-exercise anabolic window? Alan Albert Aragon1 and Brad Jon Schoenfeld2* Abstract Nutrient timing is a popular nutritional strategy that involves the consumption of combinations of nutrients–primarily protein and carbohydrate–in and around an exercise session. Some have claimed that this approach can produce dramatic improvements in body composition. It has even been postulated that the timing of nutritional consumption may be more important than the absolute daily intake of nutrients. The post-exercise period is widely considered the most critical part of nutrient timing. Theoretically, consuming the proper ratio of nutrients during this time not only initiates the rebuilding of damaged muscle tissue and restoration of energy reserves, but it does so in a supercompensated fashion that enhances both body composition and exercise performance. Several researchers have made reference to an anabolic “window of opportunity” whereby a limited time exists after training to optimize training-related muscular adaptations. However, the importance - and even the existence - of a post-exercise ‘window’ can vary according to a number of factors. Not only is nutrient timing research open to question in terms of applicability, but recent evidence has directly challenged the classical view of the relevance of post-exercise nutritional intake with respect to anabolism. Therefore, the purpose of this paper will be twofold: 1) to review the existing literature on the effects of nutrient timing with respect to post-exercise muscular adaptations, and; 2) to draw relevant conclusions that allow practical, evidence-based nutritional recommendations to be made for maximizing the anabolic response to exercise. Introduction wellascausingdamagetomusclefibers.Theoretically,con- Over the past two decades, nutrient timing has been the suming the proper ratio of nutrients during this time not subject of numerous research studies and reviews. The only initiates the rebuilding of damaged tissue and restor- basisofnutrienttiminginvolvestheconsumptionofcombi- ation of energy reserves, but it does so in a supercompen- nationsofnutrients--primarilyproteinandcarbohydrate--in sated fashion that enhances both body composition and and around an exercise session. The strategy is designed to exerciseperformance. Several researchers havemade refer- maximize exercise-induced muscular adaptations and facili- ence to an “anabolic window of opportunity” whereby a tate repair of damaged tissue [1]. Some have claimed that limited time exists after training to optimize training- such timing strategies can produce dramatic improvements relatedmuscularadaptations[3-5]. in body composition, particularly with respect to increases However, the importance – and even the existence – infat-freemass[2].Ithasevenbeenpostulatedthatthetim- of apost-exercise ‘window’can vary according toa num- ingofnutritionalconsumptionmaybemoreimportantthan ber of factors. Not only is nutrient timing research open theabsolutedailyintakeofnutrients[3]. to question in terms of applicability, but recent evidence The post-exercise period is often considered the most hasdirectlychallengedthe classicalviewoftherelevance critical part ofnutrient timing. An intenseresistancetrain- of post-exercise nutritional intake on anabolism. There- ingworkoutresultsinthedepletionofasignificantpropor- fore, the purpose of this paper will be twofold: 1) to re- tionofstoredfuels(includingglycogenandaminoacids)as view the existing literature on the effects of nutrient timing with respect to post-exercise muscular adapta- tions, and; 2) to draw relevant conclusions that allow *Correspondence:[email protected] evidence-based nutritional recommendations to bemade 2DepartmentofHealthScience,LehmanCollege,Bronx,NY,USA formaximizingtheanabolic response toexercise. Fulllistofauthorinformationisavailableattheendofthearticle ©2013AragonandSchoenfeld;licenseeBioMedCentralLtd.ThisisanOpenAccessarticledistributedunderthetermsofthe CreativeCommonsAttributionLicense(http://creativecommons.org/licenses/by/2.0),whichpermitsunrestricteduse, distribution,andreproductioninanymedium,providedtheoriginalworkisproperlycited. AragonandSchoenfeldJournaloftheInternationalSocietyofSportsNutrition2013,10:5 Page2of11 http://www.jissn.com/content/10/1/5 Glycogenrepletion or muscle protein synthesis (MPS) during the early (4 h) A primary goal of traditional post-workout nutrient timing postexercise recovery period. The discrepancy between recommendationsistoreplenishglycogenstores.Glycogen studiesisnotclearatthistime. is considered essential to optimal resistance training per- Glycogen availability also has been shown to mediate formance,with asmuchas80% ofATPproductionduring muscleproteinbreakdown.LemonandMullin[19]found suchtrainingderivedfromglycolysis[6].MacDougalletal. that nitrogen losses more than doubled following a bout [7] demonstrated that a single set of elbow flexion at 80% of exercise in a glycogen-depleted versus glycogen-loaded of1repetitionmaximum(RM)performedtomuscularfail- state. Other researchers have displayed a similar inverse urecauseda12%reductioninmixed-muscleglycogencon- relationship between glycogen levels and proteolysis [20]. centration, while three sets at this intensity resulted in a Considering the totality of evidence, maintaining a high 24% decrease. Similarly, Robergs et al. [8] reported that 3 intramuscular glycogen content at the onset of training sets of 12 RM performed to muscular failure resulted in a appearsbeneficialtodesiredresistancetrainingoutcomes. 26.1% reduction of glycogen stores in the vastus lateralis Studies show a supercompensation of glycogen stores whilesixsetsatthisintensityledtoa38%decrease,primar- whencarbohydrateisconsumedimmediatelypost-exercise, ilyresulting from glycogen depletionin typeII fibers com- and delaying consumption by just 2 hours attenuates the pared to type I fibers. It therefore stands to reason that rate of muscle glycogen re-synthesis by as much as 50% typical high volume bodybuilding-style workouts involving [21]. Exercise enhances insulin-stimulated glucose uptake multiple exercises and sets for the same muscle group following a workout with a strong correlation noted be- woulddepletethemajorityoflocalglycogenstores. tween the amount of uptake and the magnitude of glyco- Inaddition,thereisevidencethatglycogenservestome- gen utilization [22]. This is in part due to an increase in diateintracellularsignaling.Thisappearstobedue,atleast the translocation of GLUT4 during glycogen depletion inpart,toitsnegativeregulatoryeffectsonAMP-activated [23,24]therebyfacilitatingentryofglucoseintothecell.In protein kinase (AMPK). Muscle anabolism and catabolism addition,thereisanexercise-inducedincreaseintheactiv- are regulated by a complex cascade of signaling pathways. ityofglycogensynthase—theprincipleenzymeinvolvedin Several pathways that have been identified as particularly promotingglycogenstorage[25].Thecombinationofthese important to muscle anabolism include mammalian target factors facilitates the rapid uptake of glucose following an of rapamycin (mTOR), mitogen-activated protein kinase exercise bout, allowing glycogen to be replenished at an (MAPK),andvariouscalcium-(Ca2+)dependentpathways. acceleratedrate. AMPK, on the other hand,is a cellular energysensor that Thereisevidencethataddingproteintoapost-workout serves to enhance energy availability. As such, it blunts carbohydrate meal can enhance glycogen re-synthesis. energy-consuming processes including the activation of Berardietal.[26]demonstratedthatconsumingaprotein- mTORC1 mediated by insulin and mechanical tension, as carbohydratesupplementinthe2-hourperiodfollowinga well as heightening catabolic processes such as glycolysis, 60-minute cycling bout resulted in significantly greater beta-oxidation,andproteindegradation[9].mTORiscon- glycogen resynthesis compared to ingesting a calorie- sidered a master network in the regulation of skeletal equated carbohydrate solution alone. Similarly, Ivy et al. muscle growth [10,11], and its inhibition has a decidedly [27] found that consumption of a combination of protein negative effect on anabolic processes [12]. Glycogen has and carbohydrate after a 2+ hour bout of cycling and been shown to inhibit purified AMPK in cell-free assays sprintingincreasedmuscleglycogencontentsignificantly [13], and low glycogen levels are associated with an more than either a carbohydrate-only supplement of enhancedAMPKactivityinhumansinvivo[14]. equalcarbohydrateorcaloricequivalency.Thesynergis- Creeretal.[15]demonstratedthatchangesinthephos- tic effects of protein-carbohydrate have been attributed phorylation of protein kinase B (Akt) are dependent on toamorepronouncedinsulin response[28],althoughit pre-exercise muscle glycogen content. After performing 3 should be noted that not all studies support these find- setsof10repetitionsofkneeextensionswithaloadequat- ings [29]. Jentjens et al. [30] found that given ample ing to 70% of 1 repetition maximum, early phase post- carbohydratedosing(1.2g/kg/hr),theadditionofapro- exercise Akt phosphorylation was increased only in the tein and amino acid mixture (0.4 g/kg/hr) did not in- glycogen-loaded muscle, with no effect seen in the creaseglycogensynthesisduringa3-hourpost-depletion glycogen-depleted contralateral muscle. Glycogen inhib- recoveryperiod. ition also has been shown to blunt S6K activation, impair Despite a sound theoretical basis, the practical signifi- translation,andreducetheamountofmRNAofgenesre- cance of expeditiously repleting glycogen stores remains sponsible for regulating muscle hypertrophy [16,17]. In dubious. Without question, expediting glycogen resynth- contrast tothese findings, arecent study by Camera etal. esisisimportantforanarrowsubsetofendurancesports [18] found thathigh-intensity resistancetrainingwithlow where the duration between glycogen-depleting events is muscle glycogen levels did not impair anabolic signaling limited to less than approximately 8 hours [31]. Similar AragonandSchoenfeldJournaloftheInternationalSocietyofSportsNutrition2013,10:5 Page3of11 http://www.jissn.com/content/10/1/5 benefits could potentially be obtained by those who per- time. It has been theorized that insulin-mediated phos- form two-a-day split resistance training bouts (i.e. morn- phorylation of PI3K/Akt inhibits transcriptional activity ing and evening) provided the same muscles will be of the proteolytic Forkhead family of transcription fac- worked during the respective sessions. However, for tors, resulting in their sequestration in the sarcoplasm goals that are not specifically focused on the perform- away from their target genes [44]. Down-regulation of ance of multiple exercise bouts in the same day, the ur- other aspects of the ubiquitin-proteasome pathway are gency of glycogen resynthesis is greatly diminished. also believed to play a role in the process [45]. Given High-intensity resistance training with moderate volume that muscle hypertrophy represents the difference be- (6-9 sets per muscle group) has only been shown to re- tween myofibrillar protein synthesis and proteolysis, a duce glycogen stores by 36-39% [8,32]. Certain athletes decrease in protein breakdown would conceivably en- are prone to performing significantly more volume than hanceaccretion ofcontractile proteins andthus facilitate this (i.e., competitive bodybuilders), but increased vol- greater hypertrophy. Accordingly, it seems logical to ume typically accompanies decreased frequency. For ex- conclude that consuming a protein-carbohydrate supple- ample, training a muscle group with 16-20 sets in a ment following exercise would promote the greatest re- single session is done roughly once per week, whereas duction in proteolysis since the combination of the two routines with 8-10 sets are done twice per week. In sce- nutrients has been shown to elevate insulin levels to a narios of higher volume and frequency of resistance greaterextentthancarbohydrate alone [28]. training, incomplete resynthesis of pre-training glycogen However, while the theoretical basis behind spiking in- levels would not be a concern aside from the far-fetched sulin post-workout is inherently sound, it remains ques- scenario where exhaustive training bouts of the same tionable as to whether benefits extend into practice. muscles occur after recovery intervals shorter than 24 First and foremost, research has consistently shown that, hours. However, even in the event of complete glycogen in the presence of elevated plasma amino acids, the ef- depletion, replenishment to pre-training levels occurs fect of insulin elevation on net muscle protein balance well-within this timeframe, regardless of a significantly plateaus within a range of 15–30 mU/L [45,46]; roughly delayed post-exercise carbohydrate intake. For example, 3–4times normal fastinglevels. This insulinogenic effect Parkin et al [33] compared the immediate post-exercise is easily accomplished with typical mixed meals, consid- ingestion of 5 high-glycemic carbohydrate meals with a ering that it takes approximately 1–2 hours for circulat- 2-hour wait before beginning the recovery feedings. No ing substrate levels to peak, and 3–6 hours (or more) for significant between-group differences were seen in a complete return to basal levels depending on the size glycogen levels at 8 hours and 24 hours post-exercise. In of a meal. For example, Capaldo et al. [47] examined further support of this point, Fox et al. [34] saw no sig- various metabolic effects during a 5-hour period after nificant reduction in glycogen content 24 hours after de- ingesting a solid meal comprised of 75 g carbohydrate pletion despite adding 165 g fat collectively to the post- 37 g protein, and 17 g fat. This meal was able to raise exercise recovery meals and thus removing any potential insulin 3 times above fasting levels within 30 minutes of advantageof high-glycemic conditions. consumption. At the 1-hour mark, insulin was 5 times greaterthanfasting.Atthe5-hourmark,insulinwasstill Proteinbreakdown double the fasting levels. In another example, Power Anotherpurportedbenefit ofpost-workoutnutrient tim- etal. [48]showed thata45gdoseofwheyproteinisolate ing is an attenuation of muscle protein breakdown. This takes approximately 50 minutes to cause blood amino is primarily achieved by spiking insulin levels, as acid levels to peak. Insulin concentrations peaked 40 opposed to increasing amino acid availability [35,36]. minutes after ingestion, and remained at elevations seen Studies show that muscle protein breakdown is only to maximize net muscle protein balance (15-30 mU/L, slightly elevated immediately post-exercise and then or 104-208 pmol/L) for approximately 2 hours. The in- rapidly rises thereafter [36]. In the fasted state, muscle clusion of carbohydrate to this protein dose would cause protein breakdown is significantly heightened at 195 insulin levels to peak higher and stay elevated even minutes following resistance exercise, resulting in a net longer. Therefore, the recommendation for lifters to negative protein balance [37]. These values are increased spike insulin post-exercise is somewhat trivial. The clas- as much as 50% at the 3 hour mark, and elevated prote- sical post-exercise objective to quickly reverse catabolic olysis can persist for up to 24 hours of the post-workout processes to promote recovery and growth may only be period [36]. applicable in the absence of a properly constructed pre- Although insulin has known anabolic properties exercise meal. [38,39], its primary impact post-exercise is believed to Moreover, there is evidence that the effect of protein be anti-catabolic [40-43]. The mechanisms by which in- breakdown on muscle protein accretion may be over- sulin reduces proteolysis are not well understood at this stated. Glynn et al. [49] found that the post-exercise AragonandSchoenfeldJournaloftheInternationalSocietyofSportsNutrition2013,10:5 Page4of11 http://www.jissn.com/content/10/1/5 anabolic response associated with combined protein and the post-exercise ‘window’ is the finding by Tipton et al. carbohydrate consumption was largely due to an eleva- [63] that immediate pre-exercise ingestion of the same tion in muscle protein synthesis with only a minor influ- EAA-carbohydrate solution resulted in a significantly ence from reduced muscle protein breakdown. These greater and more sustained MPS response compared to results were seen regardless of the extent of circulating the immediate post-exercise ingestion, although the val- insulin levels. Thus, it remains questionable as to what, idity of these findings have been disputed based on ifany, positiveeffectsare realized with respect to muscle flawed methodology [36]. Notably, Fujita et al [64] saw growth fromspikinginsulinafterresistance training. opposite results using a similar design, except the EAA- carbohydrate was ingested 1 hour prior to exercise com- Proteinsynthesis pared to ingestion immediately pre-exercise in Tipton Perhaps the most touted benefit of post-workout nutri- et al. [63]. Adding yet more incongruity to the evidence, ent timing is that it potentiates increases in MPS. Resist- Tipton et al. [65] found no significant difference in net ance training alone has been shown to promote a MPS between the ingestion of 20 g whey immediately twofold increase in protein synthesis following exercise, pre- versus the same solution consumed 1 hour post- which is counterbalanced by the accelerated rate of pro- exercise. Collectively, the available data lack any consist- teolysis [36]. It appears that the stimulatory effects of ent indication of an ideal post-exercise timing scheme hyperaminoacidemia on muscle protein synthesis, espe- formaximizingMPS. cially from essential amino acids, are potentiated by pre- It also should be noted that measures of MPS assessed vious exercise [35,50]. There is some evidence that following an acute bout of resistance exercise do not al- carbohydrate has an additive effect on enhancing post- ways occur in parallel with chronic upregulation of exercise muscle protein synthesis when combined with causative myogenic signals [66] and are not necessarily amino acid ingestion [51], but others have failed to find predictive of long-term hypertrophic responses to such abenefit[52,53]. regimented resistance training [67]. Moreover, the post- Several studies have investigated whether an “anabolic exercise rise in MPS in untrained subjects is not recapi- window” exists in the immediate post-exercise period tulated in the trained state [68], further confounding with respect to protein synthesis. For maximizing MPS, practical relevance. Thus, the utility of acute studies is the evidence supports the superiority of post-exercise limited to providing clues and generating hypotheses free aminoacidsand/orprotein (in variouspermutations regarding hypertrophic adaptations; any attempt to ex- with or without carbohydrate) compared to solely carbo- trapolate findings from such data to changes in lean hydrate or non-caloric placebo [50,51,54-59]. However, body massisspeculative,atbest. despite the common recommendation to consume pro- tein as soon as possible post-exercise [60,61], evidence- Musclehypertrophy based support for this practice is currently lacking. Anumberofstudieshavedirectlyinvestigatedthelong- Levenhagen et al. [62] demonstrated a clear benefit to term hypertrophic effects of post-exercise protein con- consuming nutrients as soon as possible after exercise as sumption. The results of these trials are curiously opposed to delaying consumption. Employing a within- conflicting, seemingly because of varied study design subject design,10 volunteers (5 men, 5 women) con- and methodology. Moreover, a majority of studies sumed an oral supplement containing 10 g protein, 8 g employedbothpre-andpost-workout supplementation, carbohydrate and 3 g fat either immediately following or makingitimpossibletoteaseouttheimpactofconsum- three hours post-exercise. Protein synthesis of the legs ing nutrients after exercise. These confounding issues and whole body was increased threefold when the sup- highlight the difficulty in attempting to draw relevant plement was ingested immediately after exercise, as conclusions as to the validity of an “anabolic window.” compared to just 12% when consumption was delayed. What follows is an overview of the current research on A limitation of the study was that training involved the topic. Only those studies that specifically evaluated moderate intensity, long duration aerobic exercise. Thus, immediate (≤ 1 hour) post-workout nutrient provision the increased fractional synthetic rate was likely due to arediscussed(seeTable1forasummaryofdata). greater mitochondrial and/or sarcoplasmic protein frac- Esmarck et al. [69] provided the first experimental evi- tions, as opposed to synthesis of contractile elements dence that consuming protein immediately after training [36].IncontrasttothetimingeffectsshownbyLevenha- enhanced muscular growth compared to delayed protein gen et al. [62], previous work by Rasmussen et al. [56] intake. Thirteen untrained elderly male volunteers were showed no significant difference in leg net amino acid matched in pairs based on body composition and daily balance between 6 g essential amino acids (EAA) co- protein intake and divided into two groups: P0 or P2. ingested with 35 g carbohydrate taken 1 hour versus 3 Subjectsperformedaprogressive resistance trainingpro- hours post-exercise. Compounding the unreliability of gram of multiple sets for the upper and lower body. P0 hA ttp://wragon wa wnd .jissnSch Table1Post-exercisenutritionandmusclehypertrophy .com/cooenfeld EeSsttmuadla.yr[c6k9] 1eS3ludbeujrnelytcrtamsinaeleds S1e0iuthpgeprmleimimlkm/esneodtyaiapttiroeolntyeoinrc2ohmobuorscaoftnesruemxeedrcise wYPeriosthteCinonmtraotcl?hed MibMnioRsetIparassuynumdreemmntuesnctle TPcorroangisnriseintsingsigvpeorrofetmsoisuctolatinlpcleestreatisnionfglat SwRiegitsnhuifliimtcsamntediniactreeavsse.dinelmayuesdcleCSA ntent/10/1 Journalof pulldown,legpressandknee supplementation /5 the extensionperformed3days/wk In for12wk te rn a Cribband 23young 1g/kgofasupplementcontaining40g Yes DXAandmuscle Progressiveresistancetraining Significantincreasesinleanbody tio Hayes[70] recreationalmale wheyisolate,43gglucose,and7gcreatine biopsy consistingofexercisesforthe massandmuscleCSAoftypeII n a bodybuilders monohydrateconsumedeitherimmediately majormusclegroupsperformed fibersinimmediatevs.delayed lS beforeandafterexerciseorintheearly 3days/wkfor10wks supplementation oc morningandlateevening iety o Willoughby 19untrained 20gproteinor20gdextroseconsumed No Hydrostatic Progressiveresistancetraining Significantincreaseintotalbody f etal.[71] youngmales 1hourbeforeandafterexercise weighing,muscle consistingof3setsof6–8repetitions mass,fat-freemass,andthigh Sp o biopsy,surface forallthemajormusclesperformed masswithproteinvs.carb rts measurements 4days/wkfor10wks supplementation N u Hetualml.i[72] 3yo1uunngtrmainaeleds 1im5mgewdhiaeteylyisobleaftoereorapnldacaefbteorceoxenrscuismeed No MbioRIp,smyuscle Prersoigstraenscsievet,rapineriniogdiczoendsitsotitnaglboofd2y–5 SvaigsntuifsiclaantetrianlicsrebausteninotCoSfAthoefthe trition setsof5–20repetitionsperformed otherquadricepsmusclesin 20 2days/wkfor21wks. supplementedgroupversus 13 , placebo. 1 0 Verdijk 28untrained 10gcaseinhydrolysateorplacebo No DXA,CT,and Progressiveresistancetrainingconsisting Nosignificantdifferencesin :5 etal.[73] elderlymales consumedimmediatelybeforeandafter musclebiopsy ofmultiplesetsoflegpressandknee muscleCSAbetweengroups exercise extensionperformed3days/wkfor 12wks Hoffman 33well-trained Supplementcontaining42gprotein(milk/ Yes DXA Progressiveresistancetrainingconsisting Nosignificantdifferencesintotal etal.[74] youngmales collagenblend)and2gcarbohydrate of3–4setsof6–10repetitionsofmultiple bodymassorleanbodymass consumedeitherimmediatelybeforeand exercisesfortheentirebodypeformed4 betweengroups. afterexerciseorintheearlymorningand days/wkfor10weeks. lateevening Erskine 33untrained 20ghighqualityproteinorplacebo No MRI 4-6setsofelbowflexionperformed Nosignificantdifferencesin etal.[75] youngmales consumedimmediatelybeforeandafter 3days/wkfor12weeks muscleCSAbetweengroups exercise P a g e 5 o f 1 1 AragonandSchoenfeldJournaloftheInternationalSocietyofSportsNutrition2013,10:5 Page6of11 http://www.jissn.com/content/10/1/5 received an oral protein/carbohydrate supplement im- untrained male subjects were randomly assigned to mediately post-exercise while P2 received the same sup- either receive 20 g of protein or 20 grams dextrose plement 2 hours following the exercise bout. Training administered 1 hour before and after resistance exercise. was carried out 3 days a week for 12 weeks. At the end Training consisted of 3 sets of 6–8 repetitions at 85%– of the study period, cross-sectional area (CSA) of the 90% intensity. Training was performed 4 times a week quadriceps femoris and mean fiber area were signifi- over the course of 10 weeks. At the end of the study cantly increased in the P0 group while no significant period, total body mass, fat-free mass, and thigh mass increase was seen in P2. These results support the pres- was significantly greater in the protein-supplemented enceofapost-exercisewindowandsuggestthatdelaying group compared to the group that received dextrose. post-workout nutrient intake may impede muscular Given that the group receiving the protein supplement gains. consumed an additional 40 grams of protein on training In contrast to these findings,Verdijk et al. [73] failed to days, it is difficult to discern whether results were due detect any increases in skeletal muscle mass from con- to the increased protein intake or the timing of the suming a post-exercise protein supplement in a similar supplement. population of elderly men. Twenty-eight untrained sub- In a comprehensive study of well-trained subjects, jectswererandomlyassignedtoreceiveeitheraproteinor Hoffman et al. [74] randomly assigned 33 well-trained placebo supplement consumed immediately before and males to receive a protein supplement either in the immediately following the exercise session. Subjects per- morning and evening (n=13) or immediately before and formed multiple sets of leg press and knee extension 3 immediately after resistance exercise (n=13). Seven par- days per week, with the intensity of exercise progressively ticipants served as unsupplemented controls. Workouts increased over the course of the 12 week training period. consisted of 3–4 sets of 6–10 repetitions of multiple No significant differences in muscle strength or hyper- exercises for the entire body. Training was carried out trophywerenotedbetweengroupsattheendofthestudy on 4 day-a-week split routine with intensity progres- period indicating that post exercise nutrient timing strat- sively increased over the course of the study period. egiesdonotenhancetraining-relatedadaptation.Itshould After 10 weeks, no significant differences were noted be- be noted that, as opposed to the study by Esmark et al. tween groups with respect to body mass and lean body [69]thisstudyonlyinvestigatedadaptiveresponsesofsup- mass. The study was limited by its use of DXA to assess plementationonthethighmusculature;itthereforeisnot body composition, which lacks the sensitivity to detect clearbasedontheseresultswhethertheupperbodymight small changes in muscle mass compared to other im- respond differently to post-exercise supplementation than agingmodalitiessuchasMRI andCT[76]. thelowerbody. Hulmi et al. [72] randomized 31 young untrained male In an elegant single-blinded design, Cribb and Hayes subjects into 1 of 3 groups: protein supplement (n=11), [70] found a significant benefit to post-exercise protein non-caloric placebo (n=10) or control (n=10). High- consumption in 23 recreational male bodybuilders. Sub- intensity resistance training was carried out over 21 jects were randomly divided into either a PRE-POST weeks. Supplementation was provided before and after group that consumed a supplement containing protein, exercise. At the end of the study period, muscle CSA carbohydrate and creatine immediately before and after was significantly greater in the protein-supplemented training or a MOR-EVE group that consumed the same group compared to placebo or control. A strength of the supplement in the morning and evening at least 5 hours study was its long-term training period, providing sup- outside the workout. Both groups performed regimented port for the beneficial effects of nutrient timing on resistance training that progressively increased intensity chronic hypertrophic gains. Again, however, it is unclear from70% 1RMto95% 1RMover the courseof10weeks. whether enhanced results associated with protein sup- Results showed that the PRE-POSTgroup achieved a sig- plementation were due to timing or increased protein nificantlygreaterincreaseinleanbodymassandincreased consumption. type II fiber area compared to MOR-EVE. Findings sup- Most recently, Erskine et al. [75] failed to show a port the benefits of nutrient timing on training-induced hypertrophic benefit from post-workout nutrient timing. muscular adaptations. The study was limited by the Subjects were 33 untrained young males, pair-matched addition of creatine monohydrate to the supplement, for habitual protein intake and strength response to a 3- which may have facilitated increased uptake following week pre-study resistance training program. After a 6- training.Moreover,thefactthatthesupplementwastaken week washout period where no training was performed, both pre- and post-workout confounds whether an ana- subjects were then randomly assigned to receive either a bolicwindowmediatedresults. protein supplement or a placebo immediately before and Willoughby et al. [71] also found that nutrient timing after resistance exercise. Training consisted of 6– 8 sets resulted in positive muscular adaptations. Nineteen of elbow flexion carried out 3 days a week for 12 weeks. AragonandSchoenfeldJournaloftheInternationalSocietyofSportsNutrition2013,10:5 Page7of11 http://www.jissn.com/content/10/1/5 No significant differences were found in muscle volume On the other hand, there are others who might train oranatomicalcross-sectionalarea between groups. before lunch or after work, where the previous meal was finished 4–6 hours prior to commencing exercise. This Discussion lag in nutrient consumption can be considered signifi- Despite claims that immediate post-exercise nutritional cant enough to warrant post-exercise intervention if intake is essential to maximize hypertrophic gains, muscle retention or growth is the primary goal. Layman evidence-based support for such an “anabolic window of [77] estimated that the anabolic effect of a meal lasts 5-6 opportunity”isfarfromdefinitive.Thehypothesisisbased hours based on the rate of postprandial amino acid me- largely on the pre-supposition that training is carried out tabolism. However, infusion-based studies in rats [78,79] inafastedstate.Duringfastedexercise,aconcomitantin- and humans [80,81] indicate that the postprandial rise crease in muscle protein breakdown causes the pre- in MPS from ingesting amino acids or a protein-rich exercise net negative amino acid balance to persist in the meal is more transient, returning to baseline within 3 post-exercise period despite training-induced increases in hours despite sustained elevations in amino acid avail- muscle protein synthesis [36]. Thus, in the case of resist- ability. It thus has been hypothesized that a “muscle full” ance training after an overnight fast, it would make sense status can be reached where MPS becomes refractory, to provide immediate nutritional intervention--ideally in and circulating amino acids are shunted toward oxida- the form of a combination of protein and carbohydrate-- tion or fates other than MPS. In light of these findings, for the purposes of promoting muscle protein synthesis when training is initiated more than ~3–4 hours after andreducingproteolysis,therebyswitchinganetcatabolic the preceding meal, the classical recommendation to stateintoananabolicone.Overachronicperiod,thistac- consume protein (at least 25 g) as soon as possible tic could conceivably lead cumulatively to an increased seems warranted in order to reverse the catabolic state, rateofgainsinmusclemass. which in turn could expedite muscular recovery and This inevitably begs the question of how pre-exercise growth. However, as illustrated previously, minor pre- nutrition might influence the urgency or effectiveness of exercise nutritional interventions can be undertaken if a post-exercise nutrition, since not everyone engages in significant delayinthepost-exercisemealisanticipated. fasted training. In practice, it is common for those with An interesting area of speculation is the generalizability the primary goal of increasing muscular size and/or of these recommendations across training statuses and strength to make a concerted effort to consume a pre- agegroups.Burdetal.[82]reportedthatanacuteboutof exercise meal within 1-2 hours prior to the bout in at- resistance training in untrained subjects stimulates both tempt to maximize training performance. Depending on mitochondrial and myofibrillar protein synthesis, whereas its size and composition, this meal can conceivably func- in trained subjects, protein synthesis becomes more pre- tion asbothapre- andanimmediate post-exercise meal, ferentialtowardthemyofibrillarcomponent.Thissuggests sincethetimecourseofitsdigestion/absorptioncanper- alessglobalresponseinadvancedtraineesthatpotentially sist well into the recovery period. Tipton et al. [63] warrants closer attention to protein timing and type (e.g., observed that a relatively small dose of EAA (6 g) taken high-leucine sources such as dairy proteins) in order to immediately pre-exercise was able to elevate blood and optimize rates of muscular adaptation. In addition to muscle amino acid levels by roughly 130%, and these trainingstatus,agecaninfluencetrainingadaptations.Eld- levels remained elevated for 2 hours after the exercise erly subjects exhibit what has been termed “anabolic re- bout. Although this finding was subsequently challenged sistance,” characterized by a lower receptivity to amino by Fujita et al. [64], other research by Tipton et al. [65] acidsandresistancetraining[83].Themechanismsunder- showed that the ingestion of 20 g whey taken immedi- lyingthisphenomenonarenotclear,butthereisevidence ately pre-exercise elevated muscular uptake of amino thatinyoungeradults,theacuteanabolicresponsetopro- acids to 4.4 times pre-exercise resting levels during exer- teinfeedingappearstoplateauatalowerdosethanineld- cise, and did not return to baseline levels until 3 hours erly subjects. Illustrating this point, Moore et al. [84] post-exercise. These data indicate that even minimal-to- found that 20 g whole egg protein maximally stimulated moderate pre-exercise EAA or high-quality protein post-exerciseMPS, while40gincreasedleucineoxidation taken immediately before resistance training is capable without any further increase in MPS in young men. In of sustaining amino acid delivery into the post-exercise contrast, Yang et al. [85] found that elderly subjects dis- period. Given this scenario, immediate post-exercise played greater increases in MPS when consuming a post- protein dosing for the aim of mitigating catabolism exercise dose of 40 g whey protein compared to 20 g. seems redundant. The next scheduled protein-rich These findings suggest that older subjects require higher meal (whether it occurs immediately or 1–2 hours individualproteindosesforthepurposeofoptimizingthe post-exercise) is likely sufficient for maximizing recov- anabolic response to training. Further research is needed eryandanabolism. to better assess post-workout nutrient timing response AragonandSchoenfeldJournaloftheInternationalSocietyofSportsNutrition2013,10:5 Page8of11 http://www.jissn.com/content/10/1/5 across various populations, particularly with respect to Practicalapplications trained/untrainedandyoung/elderlysubjects. Distilling the data into firm, specific recommendationsis The body of research in this area has several limita- difficult due to the inconsistency of findings and scarcity tions. First, while there is an abundance of acute data, of systematic investigations seeking to optimize pre- controlled, long-term trials that systematically compare and/orpost-exercise proteindosageandtiming.Practical the effects of various post-exercise timing schemes are nutrient timing applications for the goal of muscle lacking. The majority of chronic studies have examined hypertrophy inevitably must be tempered with field pre- and post-exercise supplementation simultaneously, observations and experience in order to bridge gaps in as opposed to comparing the two treatments against the scientific literature. With that said, high-quality pro- each other. This prevents the possibility of isolating the tein dosed at 0.4–0.5 g/kg of LBM at both pre- and effects of either treatment. That is, we cannot know post-exercise is a simple, relatively fail-safe general whether pre- or post-exercise supplementation was the guideline that reflects the current evidence showing a critical contributor to the outcomes (or lack thereof). maximal acute anabolic effect of 20–40 g [53,84,85]. For Another important limitation is that the majority of example, someone with 70 kg of LBM would consume chronic studies neglect to match total protein intake be- roughly 28–35 g protein in both the pre- and post exer- tween the conditions compared. As such, it’s not pos- cise meal. Exceeding this would be have minimal detri- sible to ascertain whether positive outcomes were ment if any, whereas significantly under-shooting or influenced by timing relative to the training bout, or neglectingitaltogetherwouldnotmaximizetheanabolic simply by a greater protein intake overall. Further, dos- response. ing strategies employed in the preponderance of chronic Due to the transient anabolic impact of a protein-rich nutrient timing studies have been overly conservative, meal and its potential synergy with the trained state, providing only 10–20 g protein near the exercise bout. pre- and post-exercise meals should not be separated by More research is needed using protein doses known to more than approximately 3–4 hours, given a typical re- maximize acute anabolic response, which has been sistance training bout lasting 45–90 minutes. If protein shown to be approximately 20–40 g, depending on age is delivered within particularly large mixed-meals (which [84,85]. Thereis also a lack of chronic studies examining are inherently more anticatabolic), a case can be made the co-ingestion of protein and carbohydrate near train- for lengthening the interval to 5–6 hours. This strategy ing. Thus far, chronic studies have yielded equivocal covers the hypothetical timing benefits while allowing results. On the whole, they have not corroborated the significant flexibility in the length of the feeding win- consistency of positive outcomes seen in acute studies dows before and after training. Specific timing within examiningpost-exercise nutrition. this general framework would vary depending on indi- Another limitation is that the majority of studies on vidual preference and tolerance, as well as exercise the topic have been carried out in untrained individuals. duration. One ofmanypossibleexamplesinvolving a60- Muscular adaptations in those without resistance train- minute resistance training bout could have up to 90- ing experience tend to be robust, and do not necessarily minutefeeding windows on both sidesof the bout, given reflect gains experienced in trained subjects. It therefore central placement between the meals. In contrast, bouts remains to be determined whether training status influ- exceeding typical duration would default to shorter feed- ences the hypertrophic response to post-exercise nutri- ing windows if the 3–4 hour pre- to post-exercise meal tionalsupplementation. interval is maintained. Shifting the training session Afinallimitationoftheavailableresearchisthatcurrent closer to the pre- or post-exercise meal should be dic- methods used to assess muscle hypertrophy are widely tated by personal preference, tolerance, and lifestyle/ disparate, and the accuracy of the measures obtained are schedulingconstraints. inexact [68]. As such, it is questionable whether these Even more so than with protein, carbohydrate dosage tools are sensitive enough to detect small differences in and timing relative to resistance training is a gray area muscular hypertrophy. Although minor variances in lacking cohesive data to form concrete recommenda- muscle mass would be of little relevance to the general tions. It is tempting to recommend pre- and post- population, they could be very meaningful for elite ath- exercise carbohydrate doses that at least match or letesandbodybuilders.Thus,despiteconflictingevidence, exceedthe amounts of protein consumed in these meals. the potential benefits of post-exercise supplementation However, carbohydrate availability during and after exer- cannot be readily dismissed for those seeking to optimize cise is of greater concern for endurance as opposed to a hypertrophic response. By the same token, widely vary- strength or hypertrophy goals. Furthermore, the import- ingfeedingpatternsamongindividualschallengethecom- ance of co-ingesting post-exercise protein and carbohy- mon assumption that the post-exercise “anabolic window drate has recently been challenged by studies examining ofopportunity”isuniversallynarrowandurgent. the early recovery period, particularly when sufficient AragonandSchoenfeldJournaloftheInternationalSocietyofSportsNutrition2013,10:5 Page9of11 http://www.jissn.com/content/10/1/5 protein is provided. Koopman et al [52] found that after 12. IzumiyaY,HopkinsT,MorrisC,SatoK,ZengL,ViereckJ,HamiltonJA,Ouchi full-body resistance training, adding carbohydrate (0.15, N,LeBrasseurNK,WalshK:Fast/Glycolyticmusclefibergrowthreducesfat massandimprovesmetabolicparametersinobesemice.CellMetab. or 0.6 g/kg/hr) to amply dosed casein hydrolysate (0.3 g/ 2008,7(2):159–72. kg/hr) did not increase whole body protein balance dur- 13. McBrideA,GhilagaberS,NikolaevA,HardieDG:Theglycogen-binding ing a 6-hour post-exercise recovery period compared to domainontheAMPKbetasubunitallowsthekinasetoactasa glycogensensor.CellMetab.2009,9(1):23–34. the protein-only treatment. Subsequently, Staples et al 14. WojtaszewskiJF,MacDonaldC,NielsenJN,HellstenY,HardieDG,KempBE, [53] reported that after lower-body resistance exercise KiensB,RichterEA:Regulationof5’AMP-activatedproteinkinaseactivity (leg extensions), the increase in post-exercise muscle andsubstrateutilizationinexercisinghumanskeletalmuscle.AmJ PhysiolEndocrinolMetab2003,284(4):E813–22. proteinbalance from ingesting 25g whey isolatewasnot 15. CreerA,GallagherP,SlivkaD,JemioloB,FinkW,TrappeS:Influenceofmuscle improved by an additional 50 g maltodextrin during a 3- glycogenavailabilityonERK1/2andAktsignalingafterresistanceexercise hour recovery period. For the goal of maximizing rates inhumanskeletalmuscle.JApplPhysiol2005,99(3):950–6. 16. ChurchleyEG,CoffeyVG,PedersenDJ,ShieldA,CareyKA,Cameron-Smith of muscle gain, these findings support the broader ob- D,HawleyJA:Influenceofpreexercisemuscleglycogencontenton jective of meeting total daily carbohydrate need instead transcriptionalactivityofmetabolicandmyogenicgenesinwell-trained of specifically timing its constituent doses. Collectively, humans.JApplPhysiol2007,102(4):1604–11. 17. DennisPB,JaeschkeA,SaitohM,FowlerB,KozmaSC,ThomasG: these data indicate an increased potential for dietary MammalianTOR:ahomeostaticATPsensor.Science2001, flexibility while maintaining the pursuit of optimal 294(5544):1102–5. timing. 18. CameraDM,WestDW,BurdNA,PhillipsSM,GarnhamAP,HawleyJA,Coffey VG:Lowmuscleglycogenconcentrationdoesnotsuppresstheanabolic Competinginterests responsetoresistanceexercise.JApplPhysiol2012,113(2):206–14. Theauthorsdeclarethattheyhavenocompetinginterests. 19. LemonPW,MullinJP:Effectofinitialmuscleglycogenlevelsonprotein catabolismduringexercise.JApplPhysiol1980,48(4):624–9. Authors’contribution 20. BlomstrandE,SaltinB,BlomstrandE,SaltinB:Effectofmuscleglycogenon AAAandBJSeachcontributedequallytotheformulationandwritingofthe glucose,lactateandaminoacidmetabolismduringexerciseand manuscript.Bothauthorsreadandapprovedthefinalmanuscript. recoveryinhumansubjects.JPhysiol1999,514(1):293–302. 21. IvyJL:Glycogenresynthesisafterexercise:effectofcarbohydrateintake. Authordetails IntJSportsMed.1998,19(Suppl2):S142–5. 1CaliforniaStateUniversity,Northridge,CA,USA.2DepartmentofHealth 22. RichterEA,DeraveW,WojtaszewskiJF:Glucose,exerciseandinsulin: Science,LehmanCollege,Bronx,NY,USA. emergingconcepts.JPhysiol2001,535(Pt2):313–22. 23. DeraveW,LundS,HolmanGD,WojtaszewskiJ,PedersenO,RichterEA: Received:20December2012Accepted:25January2013 Contraction-stimulatedmuscleglucosetransportandGLUT-4surface Published:29January2013 contentaredependentonglycogencontent.AmJPhysiol1999,277 (6Pt1):E1103–10. References 24. KawanakaK,NolteLA,HanDH,HansenPA,HolloszyJO:Mechanisms 1. KerksickC,HarveyT,StoutJ,CampbellB,WilbornC,KreiderR,KalmanD, underlyingimpairedGLUT-4translocationinglycogen- ZiegenfussT,LopezH,LandisJ,IvyJL,AntonioJ:InternationalSocietyof supercompensatedmusclesofexercisedrats.AmJPhysiolEndocrinol SportsNutritionpositionstand:nutrienttiming.JIntSocSportsNutr. Metab2000,279(6):E1311–8. 2008,5:17. 25. O’GormanDJ,DelAguilaLF,WilliamsonDL,KrishnanRK,KirwanJP:Insulin 2. IvyJ,PortmanR:NutrientTiming:TheFutureofSportsNutrition.North andexercisedifferentiallyregulatePI3-kinaseandglycogensynthasein Bergen,NJ:BasicHealthPublications;2004. humanskeletalmuscle.JApplPhysiol2000,89(4):1412–9. 3. CandowDG,ChilibeckPD:Timingofcreatineorproteinsupplementation 26. BerardiJM,PriceTB,NoreenEE,LemonPW:Postexercisemuscleglycogen andresistancetrainingintheelderly.ApplPhysiolNutrMetab2008,33 recoveryenhancedwithacarbohydrate-proteinsupplement.MedSci (1):184–90. SportsExerc.2006,38(6):1106–13. 4. HulmiJJ,LockwoodCM,StoutJR:Effectofprotein/essentialaminoacids 27. IvyJL,GoforthHWJr,DamonBM,McCauleyTR,ParsonsEC,PriceTB:Early andresistancetrainingonskeletalmusclehypertrophy:Acaseforwhey postexercisemuscleglycogenrecoveryisenhancedwitha protein.NutrMetab(Lond).2010,7:51. carbohydrate-proteinsupplement.JApplPhysiol2002,93(4):1337–44. 5. KukuljanS,NowsonCA,SandersK,DalyRM:Effectsofresistanceexercise 28. ZawadzkiKM,YaspelkisBB3rd,IvyJL:Carbohydrate-proteincomplex andfortifiedmilkonskeletalmusclemass,musclesize,andfunctional increasestherateofmuscleglycogenstorageafterexercise.JAppl performanceinmiddle-agedandoldermen:an18-morandomized Physiol1992,72(5):1854–9. controlledtrial.JApplPhysiol2009,107(6):1864–73. 29. TarnopolskyMA,BosmanM,MacdonaldJR,VandeputteD,MartinJ,RoyBD: 6. LambertCP,FlynnMG:Fatigueduringhigh-intensityintermittent Postexerciseprotein-carbohydrateandcarbohydratesupplements exercise:applicationtobodybuilding.SportsMed.2002,32(8):511–22. increasemuscleglycogeninmenandwomen.JApplPhysiol1997, 7. MacDougallJD,RayS,SaleDG,McCartneyN,LeeP,GarnerS:Muscle 83(6):1877–83. substrateutilizationandlactateproduction.CanJApplPhysiol1999, 30. JentjensRL,vanLoonLJ,MannCH,WagenmakersAJ,JeukendrupAE: 24(3):209–15. Additionofproteinandaminoacidstocarbohydratesdoesnotenhance 8. RobergsRA,PearsonDR,CostillDL,FinkWJ,PascoeDD,BenedictMA, postexercisemuscleglycogensynthesis.JApplPhysiol2001,91(2):839–46. LambertCP,ZachweijaJJ:Muscleglycogenolysisduringdiffering 31. JentjensR,JeukendrupA:Determinantsofpost-exerciseglycogen intensitiesofweight-resistanceexercise.JApplPhysiol1991,70(4):1700–6. synthesisduringshort-termrecovery.SportsMed.2003,33(2):117–44. 9. GoodmanCA,MayhewDL,HornbergerTA:Recentprogresstoward 32. RoyBD,TarnopolskyMA:Influenceofdifferingmacronutrientintakeson understandingthemolecularmechanismsthatregulateskeletalmuscle muscleglycogenresynthesisafterresistanceexercise.JApplPhysiol1998, mass.CellSignal2011,23(12):1896–906. 84(3):890–6. 10. BodineSC,StittTN,GonzalezM,KlineWO,StoverGL,BauerleinR, 33. ParkinJA,CareyMF,MartinIK,StojanovskaL,FebbraioMA:Muscle ZlotchenkoE,ScrimgeourA,LawrenceJC,GlassDJ,YancopoulosGD:Akt/ glycogenstoragefollowingprolongedexercise:effectoftimingof mTORpathwayisacrucialregulatorofskeletalmusclehypertrophyand ingestionofhighglycemicindexfood.MedSciSportsExerc.1997, canpreventmuscleatrophyinvivo.NatCellBiol.2001,3(11):1014–9. 29(2):220–4. 11. JacintoE,HallMN:Torsignallinginbugs,brainandbrawn.NatRevMol 34. FoxAK,KaufmanAE,HorowitzJF:Addingfatcaloriestomealsafter CellBiol2003,4(2):117–26. exercisedoesnotalterglucosetolerance.JApplPhysiol2004,97(1):11–6. AragonandSchoenfeldJournaloftheInternationalSocietyofSportsNutrition2013,10:5 Page10of11 http://www.jissn.com/content/10/1/5 35. BioloG,TiptonKD,KleinS,WolfeRR:Anabundantsupplyofaminoacids 57. TangJE,ManolakosJJ,KujbidaGW,LyseckiPJ,MooreDR,PhillipsSM: enhancesthemetaboliceffectofexerciseonmuscleprotein.AmJ Minimalwheyproteinwithcarbohydratestimulatesmuscleprotein Physiol1997,273(1Pt1):E122–9. synthesisfollowingresistanceexerciseintrainedyoungmen.Appl 36. KumarV,AthertonP,SmithK,RennieMJ:Humanmuscleproteinsynthesisand PhysiolNutrMetab2007,32(6):1132–8. breakdownduringandafterexercise.JApplPhysiol2009,106(6):2026–39. 58. TiptonKD,ElliottTA,CreeMG,WolfSE,SanfordAP,WolfeRR:Ingestionof 37. PitkanenHT,NykanenT,KnuutinenJ,LahtiK,KeinanenO,AlenM,KomiPV, caseinandwheyproteinsresultinmuscleanabolismafterresistance MeroAA:Freeaminoacidpoolandmuscleproteinbalanceafter exercise.MedSciSportsExerc.2004,36(12):2073–81. resistanceexercise.MedSciSportsExerc.2003,35(5):784–92. 59. TiptonKD,ElliottTA,FerrandoAA,AarslandAA,WolfeRR:Stimulationof 38. BioloG,WilliamsBD,FlemingRY,WolfeRR:Insulinactiononmuscle muscleanabolismbyresistanceexerciseandingestionofleucineplus proteinkineticsandaminoacidtransportduringrecoveryafter protein.ApplPhysiolNutrMetab2009,34(2):151–61. resistanceexercise.Diabetes1999,48(5):949–57. 60. PhillipsSM,VanLoonLJ:Dietaryproteinforathletes:fromrequirements 39. FluckeyJD,VaryTC,JeffersonLS,FarrellPA:Augmentedinsulinactionon tooptimumadaptation.JSportsSci.2011,29(Suppl1):S29–38. ratesofproteinsynthesisafterresistanceexerciseinrats.AmJPhysiol 61. PhillipsSM:Thescienceofmusclehypertrophy:makingdietaryprotein 1996,270(2Pt1):E313–9. count.ProcNutrSoc2011,70(1):100–3. 40. DenneSC,LiechtyEA,LiuYM,BrechtelG,BaronAD:Proteolysisinskeletal 62. LevenhagenDK,GreshamJD,CarlsonMG,MaronDJ,BorelMJ,FlakollPJ: muscleandwholebodyinresponsetoeuglycemichyperinsulinemiain Postexercisenutrientintaketiminginhumansiscriticaltorecoveryof normaladults.AmJPhysiol1991,261(6Pt1):E809–14. legglucoseandproteinhomeostasis.AmJPhysiolEndocrinolMetab2001, 41. GelfandRA,BarrettEJ:Effectofphysiologichyperinsulinemiaonskeletal 280(6):E982–93. muscleproteinsynthesisandbreakdowninman.JClinInvest1987,80(1):1–6. 63. TiptonKD,RasmussenBB,MillerSL,WolfSE,Owens-StovallSK,PetriniBE, 42. HeslinMJ,NewmanE,WolfRF,PistersPW,BrennanMF:Effectof WolfeRR:Timingofaminoacid-carbohydrateingestionaltersanabolic hyperinsulinemiaonwholebodyandskeletalmuscleleucinecarbon responseofmuscletoresistanceexercise.AmJPhysiolEndocrinolMetab kineticsinhumans.AmJPhysiol1992,262(6Pt1):E911–8. 2001,281(2):E197–206. 43. KettelhutIC,WingSS,GoldbergAL:Endocrineregulationofprotein 64. FujitaS,DreyerHC,DrummondMJ,GlynnEL,VolpiE,RasmussenBB: breakdowninskeletalmuscle.DiabetesMetabRev.1988,4(8):751–72. Essentialaminoacidandcarbohydrateingestionbeforeresistance 44. KimDH,KimJY,YuBP,ChungHY:TheactivationofNF-kappaBthrough exercisedoesnotenhancepostexercisemuscleproteinsynthesis.JAppl Akt-inducedFOXO1phosphorylationduringaginganditsmodulation Physiol2009,106(5):1730–9. bycalorierestriction.Biogerontology2008,9(1):33–47. 65. TiptonKD,ElliottTA,CreeMG,AarslandAA,SanfordAP,WolfeRR: 45. GreenhaffPL,KaragounisLG,PeirceN,SimpsonEJ,HazellM,LayfieldR, Stimulationofnetmuscleproteinsynthesisbywheyproteiningestion WackerhageH,SmithK,AthertonP,SelbyA,RennieMJ:Disassociation beforeandafterexercise.AmJPhysiolEndocrinolMetab2007,292(1):E71–6. betweentheeffectsofaminoacidsandinsulinonsignaling,ubiquitin 66. CoffeyVG,ShieldA,CannyBJ,CareyKA,Cameron-SmithD,HawleyJA: ligases,andproteinturnoverinhumanmuscle.AmJPhysiolEndocrinol InteractionofcontractileactivityandtraininghistoryonmRNA Metab2008,295(3):E595–604. abundanceinskeletalmusclefromtrainedathletes.AmJPhysiol 46. RennieMJ,BoheJ,SmithK,WackerhageH,GreenhaffP:Branched-chain EndocrinolMetab2006,290(5):E849–55. aminoacidsasfuelsandanabolicsignalsinhumanmuscle.JNutr2006, 67. TimmonsJA:Variabilityintraining-inducedskeletalmuscleadaptation. 136(1Suppl):264S–8S. JApplPhysiol2011,110(3):846–53. 47. CapaldoB,GastaldelliA,AntonielloS,AulettaM,PardoF,CiociaroD,Guida 68. AdamsG,BammanMM:Characterizationandregulationofmechanical R,FerranniniE,SaccaL:Splanchnicandlegsubstrateexchangeafter loading-inducedcompensatorymusclehypertrophy.Comprehensive ingestionofanaturalmixedmealinhumans.Diabetes1999,48(5):958–66. Physiology2012,2829:2970. 48. PowerO,HallihanA,JakemanP:Humaninsulinotropicresponsetooral 69. EsmarckB,AndersenJL,OlsenS,RichterEA,MizunoM,KjaerM:Timingof ingestionofnativeandhydrolysedwheyprotein.AminoAcids.2009, postexerciseproteinintakeisimportantformusclehypertrophywith 37(2):333–9. resistancetraininginelderlyhumans.JPhysiol2001,535(Pt1):301–11. 49. GlynnEL,FryCS,DrummondMJ,DreyerHC,DhananiS,VolpiE,Rasmussen 70. CribbPJ,HayesA:Effectsofsupplementtimingandresistance BB:Muscleproteinbreakdownhasaminorroleintheproteinanabolic exerciseonskeletalmusclehypertrophy.MedSciSportsExerc.2006, responsetoessentialaminoacidandcarbohydrateintakefollowing 38(11):1918–25. resistanceexercise.AmJPhysiolRegulIntegrCompPhysiol2010,299(2): 71. WilloughbyDS,StoutJR,WilbornCD:Effectsofresistancetrainingand R533–40. proteinplusaminoacidsupplementationonmuscleanabolism,mass, 50. TiptonKD,FerrandoAA,PhillipsSM,DoyleDJr,WolfeRR:Postexercisenet andstrength.AminoAcids.2007,32(4):467–77. proteinsynthesisinhumanmusclefromorallyadministeredamino 72. HulmiJJ,KovanenV,SelanneH,KraemerWJ,HakkinenK,MeroAA:Acute acids.AmJPhysiol1999,276(4Pt1):E628–34. andlong-termeffectsofresistanceexercisewithorwithoutprotein 51. MillerSL,TiptonKD,ChinkesDL,WolfSE,WolfeRR:Independentand ingestiononmusclehypertrophyandgeneexpression.AminoAcids. combinedeffectsofaminoacidsandglucoseafterresistanceexercise. 2009,37(2):297–308. MedSciSportsExerc.2003,35(3):449–55. 73. VerdijkLB,JonkersRA,GleesonBG,BeelenM,MeijerK,SavelbergHH, 52. KoopmanR,BeelenM,StellingwerffT,PenningsB,SarisWH,KiesAK, WodzigWK,DendaleP,vanLoonLJ:Proteinsupplementationbeforeand KuipersH,vanLoonLJ:Coingestionofcarbohydratewithproteindoes afterexercisedoesnotfurtheraugmentskeletalmusclehypertrophy notfurtheraugmentpostexercisemuscleproteinsynthesis.AmJPhysiol afterresistancetraininginelderlymen.AmJClinNutr2009,89(2):608–16. EndocrinolMetab2007,293(3):E833–42. 74. HoffmanJR,RatamessNA,TranchinaCP,RashtiSL,KangJ,FaigenbaumAD: 53. StaplesAW,BurdNA,WestDW,CurrieKD,AthertonPJ,MooreDR,Rennie Effectofprotein-supplementtimingonstrength,power,andbody- MJ,MacdonaldMJ,BakerSK,PhillipsSM:Carbohydratedoesnotaugment compositionchangesinresistance-trainedmen.IntJSportNutrExerc exercise-inducedproteinaccretionversusproteinalone.MedSciSports Metab.2009,19(2):172–85. Exerc.2011,43(7):1154–61. 75. ErskineRM,FletcherG,HansonB,FollandJP:Wheyproteindoesnot 54. BorsheimE,CreeMG,TiptonKD,ElliottTA,AarslandA,WolfeRR:Effectof enhancetheadaptationstoelbowflexorresistancetraining.MedSci carbohydrateintakeonnetmuscleproteinsynthesisduringrecovery SportsExerc.2012,44(9):1791–800. fromresistanceexercise.JApplPhysiol2004,96(2):674–8. 76. LevineJA,AbboudL,BarryM,ReedJE,SheedyPF,JensenMD:Measuring 55. KoopmanR,WagenmakersAJ,MandersRJ,ZorencAH,SendenJM, legmuscleandfatmassinhumans:comparisonofCTanddual-energy GorselinkM,KeizerHA,vanLoonLJ:Combinedingestionofproteinand X-rayabsorptiometry.JApplPhysiol2000,88(2):452–6. freeleucinewithcarbohydrateincreasespostexercisemuscleprotein 77. LaymanDK:ProteinquantityandqualityatlevelsabovetheRDA synthesisinvivoinmalesubjects.AmJPhysiolEndocrinolMetab2005, improvesadultweightloss.JAmCollNutr2004,23(6Suppl):631S–6S. 288(4):E645–53. 78. NortonLE,LaymanDK,BunpoP,AnthonyTG,BranaDV,GarlickPJ:The 56. RasmussenBB,TiptonKD,MillerSL,WolfSE,WolfeRR:Anoralessential leucinecontentofacompletemealdirectspeakactivationbutnot aminoacid-carbohydratesupplementenhancesmuscleprotein durationofskeletalmuscleproteinsynthesisandmammaliantargetof anabolismafterresistanceexercise.JApplPhysiol2000,88(2):386–92. rapamycinsignalinginrats.JNutr2009,139(6):1103–9.

See more

The list of books you might like

Most books are stored in the elastic cloud where traffic is expensive. For this reason, we have a limit on daily download.