Co-Ingestion of Branched-Chain Amino Acids and Carbohydrate Stimulates Myofibrillar Protein Synthesis Following Resistance Exercise in Trained Young Men

in International Journal of Sport Nutrition and Exercise Metabolism

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Sarah R. Jackman Public Health and Sport Sciences, University of Exeter Medical School, Faculty of Health and Life Sciences, University of Exeter, Exeter, United Kingdom

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Gareth A. Wallis School of Sport, Exercise and Rehabilitation Sciences, University of Birmingham, Birmingham, United Kingdom

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Jinglei Yu School of Biosciences, University of Birmingham, Birmingham, United Kingdom

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Andrew Philp Centre for Healthy Ageing, Centenary Institute, Sydney, NSW, Australia

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Keith Baar Department of Neurobiology, Physiology and Behavior, University of California, Davis, CA, USA

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Kevin D. Tipton Institute for Performance Nutrition, Edinburgh, Scotland
Research Institute for Sport and Exercise Sciences, Liverpool John Moores University, Liverpool, United Kingdom

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Oliver C. Witard Centre for Human and Applied Physiological Sciences, Faculty of Life Sciences and Medicine, King’s College London, London, United Kingdom

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Branched-chain amino acids (BCAA) and carbohydrate (CHO) are commonly recommended postexercise supplements. However, no study has examined the interaction of CHO and BCAA ingestion on myofibrillar protein synthesis (MyoPS) rates following exercise. We aimed to determine the response of MyoPS to the co-ingestion of BCAA and CHO following an acute bout of resistance exercise. Ten resistance-trained young men completed two trials in counterbalanced order, ingesting isocaloric drinks containing either 30.6-g CHO plus 5.6-g BCAA (B + C) or 34.7-g CHO alone following a bout of unilateral, leg resistance exercise. MyoPS was measured postexercise with a primed, constant infusion of L-[ring13C6] phenylalanine and collection of muscle biopsies pre- and 4 hr postdrink ingestion. Blood samples were collected at time points before and after drink ingestion. Serum insulin concentrations increased to a similar extent in both trials (p > .05), peaking at 30 min postdrink ingestion. Plasma leucine (514 ± 34 nmol/L), isoleucine (282 ± 23 nmol/L), and valine (687 ± 33 nmol/L) concentrations peaked at 0.5 hr postdrink in B + C and remained elevated for 3 hr during exercise recovery. MyoPS was ∼15% greater (95% confidence interval [−0.002, 0.028], p = .039, Cohen’s d = 0.63) in B + C (0.128%/hr ± 0.011%/hr) than CHO alone (0.115%/hr ± 0.011%/hr) over the 4 hr postexercise period. Co-ingestion of BCAA and CHO augments the acute response of MyoPS to resistance exercise in trained young males.

Nutritional modulation of the muscle anabolic response to exercise is underpinned by changes in muscle protein turnover at the metabolic level (Tipton & Wolfe, 2001). Ingesting an amino acid source following resistance exercise stimulates muscle protein synthesis (MPS), leading to a positive net muscle protein balance (Biolo et al., 1997) and muscle hypertrophy. An exogenous source of essential amino acids (EAA) is necessary for stimulation of MPS (Tipton et al., 1999); that is, endogenous non-EAA are sufficient to support increased rates of MPS stimulated by exercise and exogenous EAA. The branched-chain amino acids (BCAA), especially leucine, are known to stimulate MPS, as evidenced by in vitro (Atherton et al., 2010) and in vivo rodent (Anthony et al., 1999) and human (Jackman et al., 2017; Wilkinson et al., 2013) studies. Thus, BCAA supplementation is a popular nutritional approach to enhance muscle anabolism, relevant to both athletic and clinical populations (Attlee et al., 2018; Ruano & Teixeira, 2020).

We previously demonstrated that ingestion of BCAA alone enhanced the MPS response to resistance exercise (Jackman et al., 2017). However, the MPS response to BCAA following exercise (Jackman et al., 2017) appeared to be inferior, at least in qualitative terms, to the response to intact protein containing the same amount of BCAA measured in a separate study using identical methods (Witard et al., 2014). The lack of sufficient EAA for substrate to sustain the MPS response during the latter stages of postexercise recovery has been proposed to explain this reduced anabolic response (Jackman et al., 2017; Stokes et al., 2018). Direct evidence for this idea stems from a study in which the stimulation of MPS by BCAA ingestion alone was directly compared to ingestion of a source of intact protein (Fuchs et al., 2019). The early (0–2 hr) response of MPS was similar between conditions, but as the postprandial period progressed (2–5 hr), MPS was not sustained following ingestion of BCAA alone. Thus, the efficacy of postexercise BCAA supplementation to maximize muscle anabolism has been questioned (Plotkin et al., 2021).

Carbohydrate (CHO) ingestion is commonly recommended as a postexercise nutritional strategy. Muscle glycogen is decreased by resistance exercise (Koopman et al., 2006), and postexercise CHO is often recommended to stimulate the resynthesis of muscle glycogen during recovery (Roy & Tarnopolsky, 1998; Slater & Phillips, 2011). CHO supplementation also has been shown to elevate the release of potentially anabolic hormones such as insulin and stimulate a net MPS during recovery from resistance exercise (Borsheim, Cree, et al., 2004). Given the popularity of BCAA and CHO supplementation after training, it is important to understand the interaction between these nutrients on muscle anabolism. Co-ingestion of CHO and an amino acid source has been recommended to enhance the muscle anabolic response following resistance exercise (Borsheim, Aarsland, et al., 2004; Miller et al., 2003), attributed to an increased stimulation of MPS and relatively minor attenuation of muscle protein breakdown (Glynn et al., 2010). However, to date, no study has reported the impact of adding BCAA (i.e., no other EAA) to CHO ingestion on the muscle anabolic response to resistance exercise in humans.

It is not clear whether ingestion of BCAA in addition to CHO following resistance exercise enhances muscle anabolism. Elevating insulin concentrations increases mixed MPS rates, while potentially reducing circulating amino acid availability for MPS in the exercised muscle (Borsheim, Cree, et al., 2004). Since the response of MPS to BCAA ingestion is limited by EAA availability (Fuchs et al., 2019; Jackman et al., 2017), a further reduction in EAA availability due to CHO ingestion may not be desirable. Thus, the aim of this study was to determine the response of myofibrillar protein synthesis (MyoPS) to the addition of BCAA to CHO ingestion following resistance exercise in trained, young men.

Methods

Participants and Study Design

A total of 11 healthy (body mass [BM]: 86.9 ± 9.5 kg; percent lean mass: 69% ± 5%) resistance-trained (≥two sessions per week for ≥6 months) young (21 ± 1 years) males were recruited for this crossover, double-blind, randomized, and counterbalanced study. Due to an unrelated skin condition that caused issues with biopsy healing, only 10 volunteers completed both trials. A power calculation (G*Power version 3.1) conducted a priori based on Jackman et al. (2017) suggested that a sample size of 10 participants (effect size: 0.97; power: 0.85) would be sufficient to detect a difference in MPS between conditions.

Following screening, informed consent, and preliminary testing, participants reported to the laboratory on five occasions, including two isotope infusion trials. Trials were separated by ∼3 weeks. Prior to trials, body composition was assessed using dual-energy X-ray absorptiometry and maximal strength, that is, one-repetition maximum (1RM), was predicted for each leg individually. Approximately 1 week later, each participant returned to the laboratory to confirm their single-leg 1RM. Two or 3 days later, participants performed their first blinded trial in which they consumed either a BCAA and CHO containing beverage (B + C) or a CHO only (CON) beverage (GlaxoSmithKline; Table 1). Participants performed a unilateral bout of resistance exercise prior to consuming the test drink. MyoPS was determined by measurement of the incorporation of L-[ring-13C6] phenylalanine into myofibrillar proteins during a primed continuous infusion. The infusion protocol was repeated on the contralateral leg ∼3 weeks after the first trial. Trial and exercised leg order were counterbalanced and randomized. All trials were conducted in accordance with the Declaration of Helsinki and following ethical approval by the National Research Ethics Service Ethics Board (Warwickshire, UK) and registered as a clinical trial (ISRCTN98737111).

Table 1

Test Drink Composition

B + CCON
Calories (kcal)141140
Leucine (g)2.80
Isoleucine (g)1.40
Valine (g)1.90
Carbohydrate (g)30.634.7
Fat (g)0.10.1
Sodium (mg)277276

Note. Tests drinks were consumed after the unilateral bout of resistance exercise and were either B + C or CON. B + C = branched-chain amino acid containing beverage; CON = carbohydrate only beverage.

Preliminary Testing

Strength Testing

Prediction of 1RM was completed using a published method (Verdijk et al., 2009). Briefly, following a warm-up on each leg, participants completed as many repetitions of leg press or leg extension as possible with an applied resistance equating to their self-predicted 80% 1RM. Values for load and repetitions were inserted into Equation 1 to estimate 1RM (Mayhew et al., 1995).
1RM=Load(1.02780.0278)×reps.
Confirmation of each participant’s 1RM was completed 2–3 days prior to each trial day (Kraemer & Fry, 1995). Briefly, volunteers completed the maximum number of repetitions possible at a load of 90% from Equation 1. The load was then increased by 5%–10% until only one repetition could be completed. A rest period of 3 min was provided between each effort.

Diet and Physical Activity

Prior to the experimental trial, participants completed a 3-day diet diary that represented their habitual daily intake. The average energy intake (2,816 ± 701 kcal) and macronutrient composition (protein: 1.8 ± 0.7 g·kg BM−1·day−1; CHO: 3.9 ± 1.5 g·kg BM−1·day−1; fat: 1.2 ± 0.4 g·kg BM−1·day−1) from the diet diary were used to calculate the participant’s diet before the experimental trial. Food parcels that matched each participant’s habitual energy and macronutrient intakes were supplied for 48 hr before the experimental trial. Participants were instructed to consume only food and drink sources provided by investigators and to consume their final meal no later than 22:00 on the evening before the experimental trial. Participants also were asked to refrain from alcohol consumption and exercise during this 2-day period. Diet analysis was performed using commercially available software (Wisp version 3.0, Tinuviel Software). The final meal prior to infusion day was consumed prior to 22:00.

Body Composition

Whole-body and segmental body composition was assessed using dual-energy X-ray absorptiometry (Hologic Discovery W), as described previously (Jackman et al., 2017).

Experimental Protocol

The experimental protocol is summarized in Figure 1. On the morning of the trial, each participant reported to the laboratory following an overnight fast. Height and BM were recorded. Next, a cannula was inserted in a forearm vein, and a resting blood sample was obtained. Participants were fed a standardized breakfast (30 kJ/kg BM) with 30% total energy provided by protein. Participants rested for 75 min before a primed (2 μmol/kg BM) constant infusion (0.050 μmol·min−1·kg BM−1) of L-[ring-13C6] phenylalanine (Cambridge Isotope Laboratories Inc.) was started. A hand or wrist vein of the contralateral arm was then cannulated and heated (∼55°C) for frequent arterialized blood sampling throughout the remainder of the protocol. Participants then performed a single bout of unilateral leg resistance exercise 105 min after initiating the infusion that lasted ∼25 min. A warm-up on the leg press machine (Cybex International) was performed as previously described (Jackman et al., 2017). After 2-min rest, the exercise protocol was completed consisting of 4 × 10 repetitions at 70% and 75% 1RM on leg press and leg extension machines, respectively. A rest period of 2 min was provided between sets, and participants were verbally encouraged throughout the exercise routine. In the event of a failed lift, load was decreased by 4.5 kg. Rating of perceived exertion (RPE) was recorded after each set (Borg, 1982). Arterialized blood samples and a muscle biopsy from the exercised leg were collected within 5 min of exercise cessation (t = 0). Arterialized blood samples also were collected at t = −145, −85, −25, 0, 15, 30, 45, 60, 75, 90, 120, 150, 180, and 240 min. A second muscle biopsy was collected at t = 240 min.

Figure 1
Figure 1

—Schematic diagram of the infusion protocol. A baseline blood sample was collected before participants consumed an energy-rich, high-protein breakfast. A bout of unilateral leg resistance exercise was performed 3 hr after breakfast. Muscle biopsies (vastus lateralis) were collected from the exercised leg immediately prior (0 hr), and 4 hr postdrink ingestion. Drink ingestion was either a B + C or CON. Multiple blood samples were collected throughout the protocol. Note. B + C = branched-chain amino acid and carbohydrate containing beverage; CON = carbohydrate only.

Citation: International Journal of Sport Nutrition and Exercise Metabolism 33, 4; 10.1123/ijsnem.2023-0015

Muscle Biopsy Collection and Analysis

Biopsies were obtained from the vastus lateralis of the exercised leg under local anesthesia (1% lidocaine) using a 5-mm Bergstrom needle with suction. Different incisions (∼1 cm apart) were used for each biopsy to minimize the impact of local inflammation on the muscle tissue. Muscle samples were immediately rinsed and blotted of excess blood, visible fat and connective tissue were removed, and the biopsy was divided, before being frozen in liquid nitrogen, and stored at −80 °C until later analysis. Muscle samples were analyzed for enrichment of L-[ring-13C6] phenylalanine in the intracellular pool and bound myofibrillar protein fractions.

Blood Collection and Analysis

Blood was collected in lithium heparin, ethylenediaminetetraacetic acid, and serum separator tubes and centrifuged at 3,500 revs./min for 15 min at 4 °C. Plasma and serum were frozen at −80 °C for subsequent analysis. Plasma glucose and urea concentrations were analyzed using an automated blood metabolite analyzer (Instrumentation Laboratory). Serum insulin concentrations were measured using a commercially available enzyme-linked immunosorbent assay (DRG Diagnostics).

Amino Acid Concentrations and Enrichments

13C6 tyrosine and phenylalanine enrichments were determined by gas chromatography–mass spectrometry (model 5973, Hewlett Packard), as previously described (Jackman et al., 2017). Phenylalanine, leucine, threonine, isoleucine, and valine concentrations were measured using an internal standard method (Jackman et al., 2017).

Myofibrillar Protein Enrichment

The enrichment of L-[ring-13C6] phenylalanine was analyzed in the myofibrillar protein fraction. Myofibrillar proteins were isolated from ∼30 mg of tissue as previously described (Jackman et al., 2017).

Intracellular Protein Enrichment

Approximately 20 mg of muscle tissue was used to obtain intracellular 13C6 phenylalanine enrichments. Frozen tissue was powdered under liquid nitrogen using a mortar and pestle and 500 μl of 1 M perchloric acid. The mixture was centrifuged at 10,000g for 10 min. The supernatant was then neutralized with 2 M potassium hydroxide and 0.2 M perchloric acid and combined with 20 μl of urease for removal of urea. The free amino acids from the intracellular pool were purified on cation-exchange columns as described above. Intracellular amino acids were converted to their N-Methyl-Ntert-butyldimethylsilyltrifluoroacetamide derivative, and 13C6 phenylalanine enrichment was determined by monitoring at ions 234/240 using gas chromatography–mass spectrometry (model 5973, Hewlett Packard).

Calculations

Fractional Synthetic Rate

The fractional synthetic rate of myofibrillar proteins was calculated using the standard precursor-product method (Biolo et al., 1997):
FSR (%×h1)=(ΔEmEP×t)×100,
where ΔEm is the change in bound 13C6 phenylalanine enrichment between two biopsy samples, Ep is the intracellular precursor enrichment, and t is the time between muscle biopsies.

Phenylalanine Kinetics

Phenylalanine was chosen as the tracer as it is not oxidized in the muscle or synthesized in the body. Therefore, the appearance rate of phenylalanine in the blood can be attributed to protein breakdown. Whole-body phenylalanine appearance was calculated according to Equation 3 (Tipton et al., 1996).
Ra=iEp,
where i is the infusion rate of the tracer (μmol·h−1·kg BM−1), and Ep is the enrichment of phenylalanine.

Data Presentation and Statistical Analyses

Area under the curve (AUC) was calculated for serum insulin concentrations and phenylalanine Ra using GraphPad Prism (version 9.5.0, GraphPad Software). Baseline was set at the insulin concentration measured at t = 0 (immediately predrink) resulting in incremental AUC. Baseline was set at 0 μmol·min−1·kg BM−1 when calculating AUC for phenylalanine Ra resulting in total AUC.

Plasma and serum concentrations of glucose, insulin, amino acids, and urea were analyzed using a two-way repeated-measures analysis of variance. Where significance was detected, a least significant difference correction was applied for post hoc analysis. A paired samples t test was used to analyze differences in exercise variables, MyoPS, and AUC of serum insulin concentrations and phenylalanine kinetics during the postexercise period. Significance for all analyses was set at p < .05 and effect sizes (ηp2 or Cohen d), and 95% confidence intervals were reported where appropriate. All statistical tests were completed using Statistical Package for Social Sciences (version 28.0). All values are presented as mean ± SD unless otherwise stated.

Results

Exercise Variables

There were no differences in RPE (>18) or total weight lifted throughout the exercise protocol (including warm-up) between trials (B + C: 10,698 ± 756 kg; CON: 10,236 ± 801 kg, p > .050).

Blood Metabolites

Plasma glucose concentrations (Figure 2a) increased following breakfast and drink ingestion in both trials (p = .179), and there was a significant Time × Trial interaction effect (p < .001, ηp2=.462) such that greater glucose concentrations were detected in CON versus B + C at 15 (95% CI [0.069, 0.89], p = .027); 30 (95% CI [0.732, 2.388], p = .002); and 45 min (95% CI [0.201, 0.559], p < .010) postdrink. At 60 min postexercise (95% CI [0.201, 0.0559], p = .034), glucose concentrations were greater in B + C than CON.

Figure 2
Figure 2

—Plasma glucose (a) and serum insulin (b) concentrations in response to consumption of preexercise breakfast (−240 min) and ingestion of B + C (closed circles) or CON (open circles) beverage following resistance exercise (0–240 min). Data are presented as mean ± SEM. Note. B + C = branched-chain amino acid plus carbohydrate; CON = carbohydrate.

Citation: International Journal of Sport Nutrition and Exercise Metabolism 33, 4; 10.1123/ijsnem.2023-0015

Serum insulin concentrations changed over time (p < .001, ηp2=.859); however, there were no differences between trials (Figure 2b). The incremental AUC for insulin over 240 min following drink ingestion was similar (p = .091) between B + C (38 ± 11 μIU/mL × 240 min) and CON (46 ± 12 μIU/ML × 240 min).

Amino Acid Concentrations

Main effects of time and trial and a Time × Trial interaction were observed for all BCAA concentrations (Figure 3). Peak leucine (514 ± 34 μM), isoleucine (282 ± 23 μM), and valine (687 ± 33 μM) concentrations were observed at 30 min postdrink ingestion. From 15 min postdrink until the end of measurement period, leucine (p < .002) and valine (p < .001) concentrations were higher in B + C than CON. Isoleucine concentrations were higher in B + C than CON from 15 min postdrink to 120 min postdrink (p < .005). Threonine concentrations were increased following breakfast (p < .05); however, following exercise there was a significant decrease in threonine concentrations compared to preexercise levels. There were no differences in threonine concentrations between trials.

Figure 3
Figure 3

—Plasma concentrations of (a) leucine, (b) isoleucine, (c) valine, (d) threonine, and (e) phenylalanine following consumption of preexercise breakfast (Time −240 min) and pre- and postingestion of either B + C (closed circles) or CON (open circles) beverage following intense resistance exercise (Time 0). Data are presented as mean ± SEM. *Significant difference between trials. Note. B + C = branched-chain amino acid and carbohydrate; CON = carbohydrate.

Citation: International Journal of Sport Nutrition and Exercise Metabolism 33, 4; 10.1123/ijsnem.2023-0015

There was a significant Time × Trial interaction for phenylalanine concentrations (p = .001). In both trials, phenylalanine concentrations were elevated at 150 min following breakfast (p < .001) compared with baseline, and decreased below baseline from 60 min following exercise until 180 min postexercise. Relative to pre-exercise levels, there was a decrease in phenylalanine concentration from 60 min postdrink ingestion until the end of the testing period in both trials. Phenylalanine concentrations were significantly lower in B + C than CON a 75, 90, 150, 180, and 240 min postexercise (all p < .050).

Urea Concentrations

Plasma urea concentrations declined (p = .002, ηp2=.437) from t = 0 (end of exercise; B + C: 6.27 ± 1.23 mmol/L; CON: 6.59 ± 1.18 mmol/L) trials at 180 (B + C: 5.98 ± 1.08 mmol/L CON: 6.06 ± 1.23 mmol/L, p < .05) and 240 min (B + C: 5.78 ± 0.99 mmol/L; CON: 5.73 ± 0.89 mmol/L, p < .05) postexercise in both trials. No main effect of trial (p = .749) or Time × Trial interaction (p = .356) was observed between B + C and CON.

Phenylalanine Kinetics

13C6 Phenylalanine Enrichments

Plasma 13C6 phenylalanine enrichment remained stable for the duration of tracer incorporation in both B + C and CON (Figure 4). Intracellular 13C6 phenylalanine enrichments remained stable over the tracer incorporation period for B + C and CON (2.7 ± 1.2 t/T and 2.8%t/T ± 1.2%t/T, respectively, for both time points combined). Trial order did not influence plasma or muscle intracellular 13C6 phenylalanine tracer enrichments.

Figure 4
Figure 4

—Plasma 13C6 enrichments following consumption of pre-exercise breakfast (time −240 min) and pre- and postingestion of either B + C (closed circles) or CON (open circles) beverage following resistance exercise (Time 0). Data are presented as means ± SEM. Note. B + C =branched-chain amino acid and carbohydrate; CON = carbohydrate.

Citation: International Journal of Sport Nutrition and Exercise Metabolism 33, 4; 10.1123/ijsnem.2023-0015

Phenylalanine Ra

A decrease in phenylalanine Ra was observed during the postdrink period compared to baseline in both trials (time effect: p < .001, ηp2=.847; Figure 5a). The total AUC of phenylalanine Ra expressed as total AUC over the entire 4 hr postdrink period was ∼7% lower (95% CI [−20.9, −7.8], p < .001, Cohen’s d = 1.6) in B + C than CON (Figure 5b).

Figure 5
Figure 5

—Phenylalanine rate of appearance (Ra; following ingestion of B + C [closed circles] or CON [open circles] beverage following resistance exercise [Time 0 min]). Data (mean ± SEM) are expressed over time (a) and as area under the curve (b). *Significant difference compared to CON. Note. B + C = branched-chain amino acid plus carbohydrate; CON = carbohydrate only.

Citation: International Journal of Sport Nutrition and Exercise Metabolism 33, 4; 10.1123/ijsnem.2023-0015

Myofibrillar Protein Synthesis

Mean myofibrillar fractional synthetic rate was ∼15% greater (95% CI [−0.0018, 0.0280], p = .039, Cohen d = 0.63) over the 240-min recovery period in B + C than CON (Figure 6).

Figure 6
Figure 6

—FSR of myofibrillar protein following ingestion of either a B + C or CON beverage following intense resistance exercise. Data are presented as means and individual data points. *Significantly higher compared to CON. Note. B + C = branched-chain amino acid plus carbohydrate; CON = carbohydrate alone; FSR = fractional synthesis rate.

Citation: International Journal of Sport Nutrition and Exercise Metabolism 33, 4; 10.1123/ijsnem.2023-0015

Discussion

We investigated the response of MyoPS to the addition of BCAA to CHO ingestion following resistance exercise. Our results indicate that adding BCAA to CHO following resistance exercise increases MyoPS during acute recovery. In qualitative terms, this increase (15%) was similar to the 22% increase in MyoPS with BCAA ingestion alone compared to a nonenergetic placebo reported previously (Jackman et al., 2017). Thus, there is no apparent additive effect of BCAA co-ingestion with CHO with regard to the postexercise stimulation of MyoPS.

The effectiveness of combining an amino acid source with CHO to provide a maximal muscle anabolic response following resistance exercise is controversial. Hyperinsulinemia from CHO ingestion presumably is responsible for any anabolic response to CHO. Previous work demonstrates that hyperinsulinemia using local insulin infusion eliminates the systemic decrease in amino acid concentrations and thus availability of amino acids to skeletal muscle, resulting in increased stimulation of MPS (Biolo et al., 1995, 1999). The modulatory role of hyperinsulinemia in stimulating MPS is less clear following exercise (Biolo et al., 1999). Nevertheless, in a more physiological situation, increasing insulin concentration with the addition of CHO to ingested protein does not potentiate rates of MPS at rest (Glynn et al., 2013) or following exercise (Koopman et al., 2007; Miller et al., 2003; Staples et al., 2011). However, the efficacy of adding a source of amino acids, including BCAA, to CHO is less well studied. The addition of EAA to CHO administered in two boluses following resistance exercise resulted in an increased stimulation of MPS compared to CHO alone (Miller et al., 2003). Moreover, Koopman et al. (2005) compared the response of MPS to CHO alone, with CHO plus protein (casein hydrolysate) and CHO plus protein and supplemental leucine after exercise. Whereas mixed MPS was not increased with ingested protein in addition to CHO, MPS was greater than CHO alone when leucine was ingested in addition to CHO and protein. These results are generally consistent with our previous findings; that is, adding a sufficient source of leucine to CHO following exercise increases MPS (Jackman et al., 2017). Moreover, the increase in MPS when BCAA are ingested in addition to CHO relative to ingesting CHO alone (∼15%) is not dissimilar to the increase observed when BCAA alone are ingested compared to a placebo (∼22%; Jackman et al., 2017). Indeed, a retrospective statistical comparison of the differences in MyoPS between respective BCAA and control conditions in past (Jackman et al., 2017) and present studies revealed no significant differences in the magnitude of increased stimulation of MyoPS with BCAA ingestion. Hence, taken together, these results suggest no clear interaction exists between BCAA and CHO that impacts MPS following exercise. Hence, while combining CHO and BCAA following exercise is often recommended, the efficacy of such a strategy for stimulation of muscle anabolism does not appear to be supported.

Our results indirectly support the notion that BCAA ingestion stimulates MyoPS, but without a source of exogenous EAA, the amplitude of the acute postexercise increase in MyoPS is not maximized. We acknowledge that caution must prevail when comparisons are made between studies that did not use identical methods to measure MPS. Nonetheless, this observation is consistent with previous data (Koopman et al., 2005; Miller et al., 2003) that demonstrated ingestion of a source of amino acids in addition to CHO stimulated a robust increase in MPS that was, at least qualitatively, greater than observed in the present study with combined BCAA and CHO ingestion. Participants in both Miller et al. (2003) and Koopman et al. (2005) ingested an amino acid source that provided all EAA in addition to BCAA, thus preventing the decline in plasma EAA concentrations observed in our previous (Jackman et al., 2017) and current (Figure 3) study. This observation supports the notion that BCAA ingestion without co-ingestion of a full complement of amino acids may not result in an optimal muscle anabolic environment following resistance exercise.

Both insulin and BCAA modulate protein breakdown as well as protein synthesis. Hyperinsulinemia decreases protein breakdown on both whole-body (Denne et al., 1991; Shangraw et al., 1988) and muscle (Biolo et al., 1995, 1999; Meek et al., 1998) levels at rest. BCAA ingestion decreases whole-body (Louard et al., 1990; Nair et al., 1992) and muscle protein breakdown at rest (Ferrando et al., 1995) and following resistance exercise (Borsheim, Cree, et al., 2004). Muscle protein breakdown was not directly measured in the present study, but our results indicate that whole-body protein breakdown was decreased by adding BCAA to CHO. Indicators of whole-body protein breakdown; that is, urea concentration and phenylalanine Ra, decreased with BCAA ingestion in addition to CHO. Since the insulin response was identical between trials, the response of whole-body protein breakdown appears to be due to BCAA ingestion, as indicated in our previous study (Jackman et al., 2017). Thus, as with MPS, these collective results suggest no interaction exists between BCAA and insulin on whole-body protein breakdown. However, our results should not be interpreted to indicate that BCAA ingestion reduced myofibrillar protein breakdown since the responses of whole-body and muscle metabolism to various stimuli do not necessarily match (Tipton & Wolfe, 1998). Moreover, based on recent findings generated within a home-based resistance exercise setting (Waskiw-Ford et al., 2022), we speculate that the provision of all EAA rather than BCAA alone would be required to further attenuate the decline in protein breakdown following exercise.

Conclusion

To conclude, our results demonstrate for the first time that the addition of BCAA to CHO ingestion results in an increased stimulation of MyoPS following resistance exercise. The combined ingestion of BCAA and CHO supports greater MyoPS rates after exercise than CHO alone.

Acknowledgments

AuthorshipConceptualization: Jackman, Witard, Tipton, Wallis. Data curation: Jackman, Witard, Tipton, Wallis, Baar, Philp, Yu. Formal analysis: Jackman, Witard, Tipton, Philp, Baar, Yu. Funding acquisition: Tipton. Investigation: Jackman, Witard. Methodology: Jackman, Witard, Wallis, Tipton. Project administration: Jackman, Wallis, Tipton. Supervision: Witard, Tipton. Writing original draft: Jackman, Witard, Tipton. Writing review and editing: Jackman, Witard, Tipton, Wallis, Philp, Baar. Funding: Supported by GlaxoSmithKline Healthcare (research grant to Tipton).

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    • Search Google Scholar
    • Export Citation
  • Attlee, A., Haider, A., Hassan, A., Alzamil, N., Hashim, M., & Obaid, R.S. (2018). Dietary supplement intake and associated factors among gym users in a University Community. Journal of Dietary Supplements, 15(1), 8897. https://doi.org/10.1080/19390211.2017.1326430

    • Search Google Scholar
    • Export Citation
  • Biolo, G., Declan Fleming, R.Y., & Wolfe, R.R. (1995). Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. The Journal of Clinical Investigation, 95(2), 811819. https://doi.org/10.1172/JCI117731

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Biolo, G., Tipton, K.D., Klein, S., & Wolfe, R.R. (1997). An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. The American Journal of Physiology, 273(1 Pt 1), E122E129. https://doi.org/10.1152/ajpendo.1997.273.1.E122

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Biolo, G., Williams, B.D., Fleming, R.Y., & Wolfe, R.R. (1999). Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Diabetes, 48(5), 949957. https://doi.org/10.2337/diabetes.48.5.949

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Borg, G.A. (1982). Psychophysical bases of perceived exertion. Medicine & Science in Sports & Exercise, 14(5), 377381. https://www.ncbi.nlm.nih.gov/pubmed/7154893

    • Search Google Scholar
    • Export Citation
  • Borsheim, E., Aarsland, A., & Wolfe, R.R. (2004). Effect of an amino acid, protein, and carbohydrate mixture on net muscle protein balance after resistance exercise. International Journal of Sport Nutrition and Exercise Metabolism, 14(3), 255271. https://doi.org/10.1123/ijsnem.14.3.255

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Borsheim, E., Cree, M.G., Tipton, K.D., Elliott, T.A., Aarsland, A., & Wolfe, R.R. (2004). Effect of carbohydrate intake on net muscle protein synthesis during recovery from resistance exercise. Journal of Applied Physiology, 96(2), 674678. https://doi.org/10.1152/japplphysiol.00333.2003

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Denne, S.C., Liechty, E.A., Liu, Y.M., Brechtel, G., & Baron, A.D. (1991). Proteolysis in skeletal muscle and whole body in response to euglycemic hyperinsulinemia in normal adults. The American Journal of Physiology, 261(6, Pt. 1), E809E814. https://doi.org/10.1152/ajpendo.1991.261.6.E809

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ferrando, A.A., Williams, B.D., Stuart, C.A., Lane, H.W., & Wolfe, R.R. (1995). Oral branched-chain amino acids decrease whole-body proteolysis. Journal of Parenteral and Enteral Nutrition, 19(1), 4754. https://doi.org/10.1177/014860719501900147

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fuchs, C.J., Hermans, W.J.H., Holwerda, A.M., Smeets, J.S.J., Senden, J.M., van Kranenburg, J., Gijsen, A.P., Wodzig, W., Schierbeek, H., Verdijk, L.B., & van Loon, L.J.C. (2019). Branched-chain amino acid and branched-chain ketoacid ingestion increases muscle protein synthesis rates in vivo in older adults: A double-blind, randomized trial. American Journal of Clinical Nutrition, 110(4), 862872. https://doi.org/10.1093/ajcn/nqz120

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Glynn, E.L., Fry, C.S., Drummond, M.J., Dreyer, H.C., Dhanani, S., Volpi, E., & Rasmussen, B.B. (2010). Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 299(2), R533R540. https://doi.org/10.1152/ajpregu.00077.2010

    • Search Google Scholar
    • Export Citation
  • Glynn, E.L., Fry, C.S., Timmerman, K.L., Drummond, M.J., Volpi, E., & Rasmussen, B.B. (2013). Addition of carbohydrate or alanine to an essential amino acid mixture does not enhance human skeletal muscle protein anabolism. Journal of Nutrition, 143(3), 307314. https://doi.org/10.3945/jn.112.168203

    • Search Google Scholar
    • Export Citation
  • Jackman, S.R., Witard, O.C., Philp, A., Wallis, G.A., Baar, K., & Tipton, K.D. (2017). Branched-chain amino acid ingestion stimulates muscle Myofibrillar protein synthesis following resistance exercise in humans. Frontiers in Physiology, 8, Article 390. https://doi.org/10.3389/fphys.2017.00390

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Koopman, R., Beelen, M., Stellingwerff, T., Pennings, B., Saris, W.H., Kies, A.K., Kuipers, H., & van Loon, L.J. (2007). Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis. American Journal of Physiology Endocrinology and Metabolism, 293(3), E833E842. https://doi.org/10.1152/ajpendo.00135.2007

    • Search Google Scholar
    • Export Citation
  • Koopman, R., Manders, R.J., Jonkers, R.A., Hul, G.B., Kuipers, H., & van Loon, L.J. (2006). Intramyocellular lipid and glycogen content are reduced following resistance exercise in untrained healthy males. European Journal of Applied Physiology, 96(5), 525534. https://doi.org/10.1007/s00421-005-0118-0

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Koopman, R., Wagenmakers, A.J., Manders, R.J., Zorenc, A.H., Senden, J.M., Gorselink, M., Keizer, H.A., & van Loon, L.J. (2005). Combined ingestion of protein and free leucine with carbohydrate increases postexercise muscle protein synthesis in vivo in male subjects. American Journal of Physiology Endocrinology and Metabolism, 288(4), E645E653. https://doi.org/10.1152/ajpendo.00413.2004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kraemer, L., & Fry, A. (1995). Strength testing: Development and evaluation of methodology. In P.J. Maud, Foster, C. (Eds.), Physiological assessment of human fitness (pp. 115138). Human Kinetics.

    • Search Google Scholar
    • Export Citation
  • Louard, R.J., Barrett, E.J., & Gelfand, R.A. (1990). Effect of infused branched-chain amino acids on muscle and whole-body amino acid metabolism in man. Clinical Science, 79(5), 457466. https://doi.org/10.1042/cs0790457

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mayhew, J.L., Prinster, J.L., Ware, J.S., Zimmer, D.L., Arabas, J.R., & Bemben, M.G. (1995). Muscular endurance repetitions to predict bench press strength in men of different training levels. Journal of Sports Medicine and Physical Fitness, 35(2), 108113. https://www.ncbi.nlm.nih.gov/pubmed/7500624

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Meek, S.E., Persson, M., Ford, G.C., & Nair, K.S. (1998). Differential regulation of amino acid exchange and protein dynamics across splanchnic and skeletal muscle beds by insulin in healthy human subjects. Diabetes, 47(12), 18241835. https://doi.org/10.2337/diabetes.47.12.1824

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Miller, S.L., Tipton, K.D., Chinkes, D.L., Wolf, S.E., & Wolfe, R.R. (2003). Independent and combined effects of amino acids and glucose after resistance exercise. Medicine & Science in Sports & Exercise, 35(3), 449455. https://doi.org/10.1249/01.MSS.0000053910.63105.45

    • Search Google Scholar
    • Export Citation
  • Nair, K.S., Schwartz, R.G., & Welle, S. (1992). Leucine as a regulator of whole body and skeletal muscle protein metabolism in humans. The American Journal of Physiology, 263(5 Pt 1), E928E934. https://doi.org/10.1152/ajpendo.1992.263.5.E928

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Plotkin, D.L., Delcastillo, K., Van Every, D.W., Tipton, K.D., Aragon, A.A., & Schoenfeld, B.J. (2021). Isolated leucine and branched-chain amino acid supplementation for enhancing muscular strength and hypertrophy: A narrative review. International Journal of Sport Nutrition and Exercise Metabolism, 31(3), 292301. https://doi.org/10.1123/ijsnem.2020-0356

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Roy, B.D., & Tarnopolsky, M.A. (1998). Influence of differing macronutrient intakes on muscle glycogen resynthesis after resistance exercise. Journal of Applied Physiology, 84(3), 890896. https://doi.org/10.1152/jappl.1998.84.3.890

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ruano, J., & Teixeira, V.H. (2020). Prevalence of dietary supplement use by gym members in Portugal and associated factors. Journal of the International Society of Sports Nutrition, 17(1), Article 11. https://doi.org/10.1186/s12970-020-00342-z

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Shangraw, R.E., Stuart, C.A., Prince, M.J., Peters, E.J., & Wolfe, R.R. (1988). Insulin responsiveness of protein metabolism in vivo following bedrest in humans. The American Journal of Physiology, 255(4 Pt 1), E548E558. https://doi.org/10.1152/ajpendo.1988.255.4.E548

    • PubMed
    • Search Google Scholar
    • Export Citation
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  • Waskiw-Ford, M., Hodson, N., Fung, H.J.W., West, D.W.D., Apong, P., Bashir, R., & Moore, D.R. (2022). Essential amino acid ingestion facilitates leucine retention and attenuates myofibrillar protein breakdown following bodyweight resistance exercise in young adults in a home-based setting. Nutrients, 14(17), Article 532. https://doi.org/10.3390/nu14173532

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  • Wilkinson, D.J., Hossain, T., Hill, D.S., Phillips, B.E., Crossland, H., Williams, J., Loughna, P., Churchward-Venne, T.A., Breen, L., Phillips, S.M., Etheridge, T., Rathmacher, J.A., Smith, K., Szewczyk, N.J., & Atherton, P.J. (2013). Effects of leucine and its metabolite beta-hydroxy-beta-methylbutyrate on human skeletal muscle protein metabolism. Journal of Physiology, 591(11), 29112923. https://doi.org/10.1113/jphysiol.2013.253203

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  • Witard, O.C., Jackman, S.R., Breen, L., Smith, K., Selby, A., & Tipton, K.D. (2014). Myofibrillar muscle protein synthesis rates subsequent to a meal in response to increasing doses of whey protein at rest and after resistance exercise. American Journal of Clinical Nutrition, 99(1), 8695. https://doi.org/10.3945/ajcn.112.055517

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Jackman (s.jackman@exeter.ac.uk) is corresponding author.

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  • Figure 1

    —Schematic diagram of the infusion protocol. A baseline blood sample was collected before participants consumed an energy-rich, high-protein breakfast. A bout of unilateral leg resistance exercise was performed 3 hr after breakfast. Muscle biopsies (vastus lateralis) were collected from the exercised leg immediately prior (0 hr), and 4 hr postdrink ingestion. Drink ingestion was either a B + C or CON. Multiple blood samples were collected throughout the protocol. Note. B + C = branched-chain amino acid and carbohydrate containing beverage; CON = carbohydrate only.

  • Figure 2

    —Plasma glucose (a) and serum insulin (b) concentrations in response to consumption of preexercise breakfast (−240 min) and ingestion of B + C (closed circles) or CON (open circles) beverage following resistance exercise (0–240 min). Data are presented as mean ± SEM. Note. B + C = branched-chain amino acid plus carbohydrate; CON = carbohydrate.

  • Figure 3

    —Plasma concentrations of (a) leucine, (b) isoleucine, (c) valine, (d) threonine, and (e) phenylalanine following consumption of preexercise breakfast (Time −240 min) and pre- and postingestion of either B + C (closed circles) or CON (open circles) beverage following intense resistance exercise (Time 0). Data are presented as mean ± SEM. *Significant difference between trials. Note. B + C = branched-chain amino acid and carbohydrate; CON = carbohydrate.

  • Figure 4

    —Plasma 13C6 enrichments following consumption of pre-exercise breakfast (time −240 min) and pre- and postingestion of either B + C (closed circles) or CON (open circles) beverage following resistance exercise (Time 0). Data are presented as means ± SEM. Note. B + C =branched-chain amino acid and carbohydrate; CON = carbohydrate.

  • Figure 5

    —Phenylalanine rate of appearance (Ra; following ingestion of B + C [closed circles] or CON [open circles] beverage following resistance exercise [Time 0 min]). Data (mean ± SEM) are expressed over time (a) and as area under the curve (b). *Significant difference compared to CON. Note. B + C = branched-chain amino acid plus carbohydrate; CON = carbohydrate only.

  • Figure 6

    —FSR of myofibrillar protein following ingestion of either a B + C or CON beverage following intense resistance exercise. Data are presented as means and individual data points. *Significantly higher compared to CON. Note. B + C = branched-chain amino acid plus carbohydrate; CON = carbohydrate alone; FSR = fractional synthesis rate.

  • Anthony, J.C., Anthony, T.G., & Layman, D.K. (1999). Leucine supplementation enhances skeletal muscle recovery in rats following exercise. Journal of Nutrition, 129(6), 11021106. https://doi.org/10.1093/jn/129.6.1102

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Atherton, P.J., Smith, K., Etheridge, T., Rankin, D., & Rennie, M.J. (2010). Distinct anabolic signalling responses to amino acids in C2C12 skeletal muscle cells. Amino Acids, 38(5), 15331539. https://doi.org/10.1007/s00726-009-0377-x

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Attlee, A., Haider, A., Hassan, A., Alzamil, N., Hashim, M., & Obaid, R.S. (2018). Dietary supplement intake and associated factors among gym users in a University Community. Journal of Dietary Supplements, 15(1), 8897. https://doi.org/10.1080/19390211.2017.1326430

    • Search Google Scholar
    • Export Citation
  • Biolo, G., Declan Fleming, R.Y., & Wolfe, R.R. (1995). Physiologic hyperinsulinemia stimulates protein synthesis and enhances transport of selected amino acids in human skeletal muscle. The Journal of Clinical Investigation, 95(2), 811819. https://doi.org/10.1172/JCI117731

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Biolo, G., Tipton, K.D., Klein, S., & Wolfe, R.R. (1997). An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. The American Journal of Physiology, 273(1 Pt 1), E122E129. https://doi.org/10.1152/ajpendo.1997.273.1.E122

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Biolo, G., Williams, B.D., Fleming, R.Y., & Wolfe, R.R. (1999). Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise. Diabetes, 48(5), 949957. https://doi.org/10.2337/diabetes.48.5.949

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Borg, G.A. (1982). Psychophysical bases of perceived exertion. Medicine & Science in Sports & Exercise, 14(5), 377381. https://www.ncbi.nlm.nih.gov/pubmed/7154893

    • Search Google Scholar
    • Export Citation
  • Borsheim, E., Aarsland, A., & Wolfe, R.R. (2004). Effect of an amino acid, protein, and carbohydrate mixture on net muscle protein balance after resistance exercise. International Journal of Sport Nutrition and Exercise Metabolism, 14(3), 255271. https://doi.org/10.1123/ijsnem.14.3.255

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Borsheim, E., Cree, M.G., Tipton, K.D., Elliott, T.A., Aarsland, A., & Wolfe, R.R. (2004). Effect of carbohydrate intake on net muscle protein synthesis during recovery from resistance exercise. Journal of Applied Physiology, 96(2), 674678. https://doi.org/10.1152/japplphysiol.00333.2003

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Denne, S.C., Liechty, E.A., Liu, Y.M., Brechtel, G., & Baron, A.D. (1991). Proteolysis in skeletal muscle and whole body in response to euglycemic hyperinsulinemia in normal adults. The American Journal of Physiology, 261(6, Pt. 1), E809E814. https://doi.org/10.1152/ajpendo.1991.261.6.E809

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ferrando, A.A., Williams, B.D., Stuart, C.A., Lane, H.W., & Wolfe, R.R. (1995). Oral branched-chain amino acids decrease whole-body proteolysis. Journal of Parenteral and Enteral Nutrition, 19(1), 4754. https://doi.org/10.1177/014860719501900147

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Fuchs, C.J., Hermans, W.J.H., Holwerda, A.M., Smeets, J.S.J., Senden, J.M., van Kranenburg, J., Gijsen, A.P., Wodzig, W., Schierbeek, H., Verdijk, L.B., & van Loon, L.J.C. (2019). Branched-chain amino acid and branched-chain ketoacid ingestion increases muscle protein synthesis rates in vivo in older adults: A double-blind, randomized trial. American Journal of Clinical Nutrition, 110(4), 862872. https://doi.org/10.1093/ajcn/nqz120

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Glynn, E.L., Fry, C.S., Drummond, M.J., Dreyer, H.C., Dhanani, S., Volpi, E., & Rasmussen, B.B. (2010). Muscle protein breakdown has a minor role in the protein anabolic response to essential amino acid and carbohydrate intake following resistance exercise. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 299(2), R533R540. https://doi.org/10.1152/ajpregu.00077.2010

    • Search Google Scholar
    • Export Citation
  • Glynn, E.L., Fry, C.S., Timmerman, K.L., Drummond, M.J., Volpi, E., & Rasmussen, B.B. (2013). Addition of carbohydrate or alanine to an essential amino acid mixture does not enhance human skeletal muscle protein anabolism. Journal of Nutrition, 143(3), 307314. https://doi.org/10.3945/jn.112.168203

    • Search Google Scholar
    • Export Citation
  • Jackman, S.R., Witard, O.C., Philp, A., Wallis, G.A., Baar, K., & Tipton, K.D. (2017). Branched-chain amino acid ingestion stimulates muscle Myofibrillar protein synthesis following resistance exercise in humans. Frontiers in Physiology, 8, Article 390. https://doi.org/10.3389/fphys.2017.00390

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Koopman, R., Beelen, M., Stellingwerff, T., Pennings, B., Saris, W.H., Kies, A.K., Kuipers, H., & van Loon, L.J. (2007). Coingestion of carbohydrate with protein does not further augment postexercise muscle protein synthesis. American Journal of Physiology Endocrinology and Metabolism, 293(3), E833E842. https://doi.org/10.1152/ajpendo.00135.2007

    • Search Google Scholar
    • Export Citation
  • Koopman, R., Manders, R.J., Jonkers, R.A., Hul, G.B., Kuipers, H., & van Loon, L.J. (2006). Intramyocellular lipid and glycogen content are reduced following resistance exercise in untrained healthy males. European Journal of Applied Physiology, 96(5), 525534. https://doi.org/10.1007/s00421-005-0118-0

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Koopman, R., Wagenmakers, A.J., Manders, R.J., Zorenc, A.H., Senden, J.M., Gorselink, M., Keizer, H.A., & van Loon, L.J. (2005). Combined ingestion of protein and free leucine with carbohydrate increases postexercise muscle protein synthesis in vivo in male subjects. American Journal of Physiology Endocrinology and Metabolism, 288(4), E645E653. https://doi.org/10.1152/ajpendo.00413.2004

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Kraemer, L., & Fry, A. (1995). Strength testing: Development and evaluation of methodology. In P.J. Maud, Foster, C. (Eds.), Physiological assessment of human fitness (pp. 115138). Human Kinetics.

    • Search Google Scholar
    • Export Citation
  • Louard, R.J., Barrett, E.J., & Gelfand, R.A. (1990). Effect of infused branched-chain amino acids on muscle and whole-body amino acid metabolism in man. Clinical Science, 79(5), 457466. https://doi.org/10.1042/cs0790457

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Mayhew, J.L., Prinster, J.L., Ware, J.S., Zimmer, D.L., Arabas, J.R., & Bemben, M.G. (1995). Muscular endurance repetitions to predict bench press strength in men of different training levels. Journal of Sports Medicine and Physical Fitness, 35(2), 108113. https://www.ncbi.nlm.nih.gov/pubmed/7500624

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Meek, S.E., Persson, M., Ford, G.C., & Nair, K.S. (1998). Differential regulation of amino acid exchange and protein dynamics across splanchnic and skeletal muscle beds by insulin in healthy human subjects. Diabetes, 47(12), 18241835. https://doi.org/10.2337/diabetes.47.12.1824

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Miller, S.L., Tipton, K.D., Chinkes, D.L., Wolf, S.E., & Wolfe, R.R. (2003). Independent and combined effects of amino acids and glucose after resistance exercise. Medicine & Science in Sports & Exercise, 35(3), 449455. https://doi.org/10.1249/01.MSS.0000053910.63105.45

    • Search Google Scholar
    • Export Citation
  • Nair, K.S., Schwartz, R.G., & Welle, S. (1992). Leucine as a regulator of whole body and skeletal muscle protein metabolism in humans. The American Journal of Physiology, 263(5 Pt 1), E928E934. https://doi.org/10.1152/ajpendo.1992.263.5.E928

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Plotkin, D.L., Delcastillo, K., Van Every, D.W., Tipton, K.D., Aragon, A.A., & Schoenfeld, B.J. (2021). Isolated leucine and branched-chain amino acid supplementation for enhancing muscular strength and hypertrophy: A narrative review. International Journal of Sport Nutrition and Exercise Metabolism, 31(3), 292301. https://doi.org/10.1123/ijsnem.2020-0356

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Roy, B.D., & Tarnopolsky, M.A. (1998). Influence of differing macronutrient intakes on muscle glycogen resynthesis after resistance exercise. Journal of Applied Physiology, 84(3), 890896. https://doi.org/10.1152/jappl.1998.84.3.890

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Ruano, J., & Teixeira, V.H. (2020). Prevalence of dietary supplement use by gym members in Portugal and associated factors. Journal of the International Society of Sports Nutrition, 17(1), Article 11. https://doi.org/10.1186/s12970-020-00342-z

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Shangraw, R.E., Stuart, C.A., Prince, M.J., Peters, E.J., & Wolfe, R.R. (1988). Insulin responsiveness of protein metabolism in vivo following bedrest in humans. The American Journal of Physiology, 255(4 Pt 1), E548E558. https://doi.org/10.1152/ajpendo.1988.255.4.E548

    • PubMed
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  • Wilkinson, D.J., Hossain, T., Hill, D.S., Phillips, B.E., Crossland, H., Williams, J., Loughna, P., Churchward-Venne, T.A., Breen, L., Phillips, S.M., Etheridge, T., Rathmacher, J.A., Smith, K., Szewczyk, N.J., & Atherton, P.J. (2013). Effects of leucine and its metabolite beta-hydroxy-beta-methylbutyrate on human skeletal muscle protein metabolism. Journal of Physiology, 591(11), 29112923. https://doi.org/10.1113/jphysiol.2013.253203

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