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nutrients Article Whey Protein Supplementation Enhances Whole Body Protein Metabolism and Performance Recovery after Resistance Exercise: A Double-Blind Crossover Study Daniel W. D. West 1 , Sidney Abou Sawan 1 , Michael Mazzulla 1 , Eric Williamson 1 and Daniel R. Moore 2, * 1 Faculty of Kinesiology and Physical Education, University of Toronto, Toronto, ON M5S 1A1, Canada; daniel.west@utoronto.ca (D.W.D.W.); sidney.abousawan@mail.utoronto.ca (S.A.S.); m.mazzulla@mail.uto
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  nutrients  Article Whey Protein Supplementation Enhances WholeBody Protein Metabolism and Performance Recoveryafter Resistance Exercise: A Double-BlindCrossover Study Daniel W. D. West  1  , Sidney Abou Sawan  1  , Michael Mazzulla  1  , Eric Williamson  1 andDaniel R. Moore  2, * 1 Faculty of Kinesiology and Physical Education, University of Toronto, Toronto, ON M5S 1A1, Canada;daniel.west@utoronto.ca (D.W.D.W.); sidney.abousawan@mail.utoronto.ca (S.A.S.);m.mazzulla@mail.utoronto.ca (M.M.); eric.williamson@mail.utoronto.ca (E.W.) 2 Kinesiology and Physical Education University of Toronto 100 Devonshire Place, Toronto,ON M5S 2C9, Canada *  Correspondence: dr.moore@utoronto.ca; Tel.: +1-416-946-4088Received: 13 June 2017; Accepted: 5 July 2017; Published: 11 July 2017 Abstract:  No study has concurrently measured changes in free-living whole body protein metabolism and exercise performance during recovery from an acute bout of resistance exercise. We aimedto determine if whey protein ingestion enhances whole body net protein balance and recoveryof exercise performance during overnight (10 h) and 24 h recovery after whole body resistance exercise in trained men. In a double-blind crossover design, 12 trained men (76 ± 8 kg, 24 ± 4 years old, 14%  ±  5% body fat; means  ±  standard deviation (SD)) performed resistance exercise in theevening prior to consuming either 25 g of whey protein (PRO; MuscleTech 100% Whey) or anenergy-matched placebo (CHO) immediately post-exercise (0 h), and again the following morning(~10 h of recovery). A third randomized trial, completed by the same participants, involving no exercise and no supplement served as a rested control trial (Rest). Participants ingested [ 15 N]glycine to determine whole body protein kinetics and net protein balance over 10 and 24 h of recovery.Performance was assessed pre-exercise and at 0, 10, and 24 h of recovery using a battery of tests.Net protein balance tended to improve in PRO (  p  = 0.064; effect size (ES) = 0.61, PRO vs. CHO)during overnight recovery. Over 24 h, net balance was enhanced in PRO (  p  = 0.036) but not inCHO (  p  = 0.84; ES = 0.69, PRO vs. CHO), which was mediated primarily by a reduction in protein  breakdown (PRO < CHO;  p  < 0.01. Exercise decreased repetitions to failure (REP), maximal strength(MVC), peak and mean power, and countermovement jump performance (CMJ) at 0 h (all  p  < 0.05 vs. Pre). At 10 h, there were small-to-moderate effects for enhanced recovery of the MVC (ES = 0.56), mean power (ES = 0.49), and CMJ variables (ES: 0.27–0.49) in PRO. At 24 h, protein supplementationimproved MVC (ES = 0.76), REP (ES = 0.44), and peak power (ES = 0.55). In conclusion, whey protein supplementation enhances whole body anabolism, and may improve acute recovery of exercise performance after a strenuous bout of resistance exercise. Keywords:  net protein balance; dietary protein; ergogenic aid; strength; power 1. Background Consuming a source of protein after resistance exercise is essential to maximize muscle proteinsynthesis and net protein balance [ 1 , 2 ], both of which are required to support muscle hypertrophywith training. Current research supports the consumption of a moderate dose (~20–25 g) of rapidlydigested, leucine-rich proteins to optimize muscle protein synthesis [ 3 – 5 ]; this ostensibly positions Nutrients  2017 ,  9 , 735; doi:10.3390/nu9070735 www.mdpi.com/journal/nutrients  Nutrients  2017 ,  9 , 735 2 of 18 whey protein as a valuable supplemental source for individuals aiming to maximize their recoveryfrom and adaptation to resistance exercise. Individuals who train at night due to preference and/orlifestyle may be particularly sensitive to nutrition interventions given that muscle and whole body protein balance is negative during the overnight period in the absence of dietary protein [ 6 , 7 ]. Res andco-workers[ 7 ]recentlyreportedthatingesting40gofcaseinbeforesleepimprovedwholebodyproteinsynthesisandnetbalance,andenhancedmuscleproteinsynthesisduringovernightrecoverycomparedto a carbohydrate placebo. Post-exercise/pre-bedtime protein ingestion for evening exercisers may alsotranslate into greater increases in muscle strength and hypertrophy with chronic training and protein consumption [ 8 ]. Thus, research to date points toward the importance of protein feeding to enhance protein accretion after resistance exercise, especially if normal dietary patterns preclude the ability to eat during prolonged (e.g., 8–12 h) overnight recovery in evening exercisers. Whether rapidly digestedwhey protein, also enhances anabolism, similar to slowly digested casein, and exercise recovery when consumed after an evening training bout remains to be determined. Athletes aiming to maximize lean mass growth and post-exercise recovery would ostensibly benefit from enhancing whole body anabolism. The use of oral tracers such as [ 15 N]glycine have a long history of use in noninvasively measuring free-living whole body protein metabolism in a variety of populations (for an extensive review of the end-product method of measuring protein turnoverand its historical use, see [ 9 ]). This method can be used to measure whole body protein synthesis,protein breakdown, and net protein balance over both shorter (i.e., ~10 h) and longer (i.e., ~24 h)time frames [ 10 ], which highlights its utility in determining protein metabolism over early and laterpost-exercise recovery periods in controlled yet free-living scenarios (e.g., [ 11 – 13 ]). Moreover, the noninvasive nature of the tracer would minimize any residual effects of the tracer methodology (e.g., muscle biopsies) on subsequent performance tests. While measures of whole body protein metabolismcannot delineate an effect in any one tissue, nutritionally-mediated changes in whole body net protein  balance have been shown to qualitatively mirror that of myofibrillar protein synthesis over relatively prolonged (i.e., 12 h) post-exercise recovery periods [ 14 , 15 ]. Therefore, individuals who can maximize whole body net protein balance would likely also support greater skeletal muscle remodeling, which may persist for up to 24–48 h after an acute bout of exercise [16,17]. Strenuous training can result in changes in muscle function characterized by acute impairmentsin strength and exercise performance over the subsequent hours-to-days after a training bout [ 18 , 19 ]. While this acute loss of performance, potentially mediated by exercise-induced muscle damage [ 19 , 20 ],may be considered a normal byproduct of any training program, the rapid resolution of these negative effects could ultimately facilitate a higher quality training stimulus during in-season trainig and/orsport performance. Whereas the beneficial effect of protein supplementation on chronic muscularadaptations have been investigated extensively [ 12 , 21 – 23 ], little research has addressed whether post-exercise protein ingestion may facilitate the acute (e.g., ≤ 24 h) recovery of exercise performance. One study [ 24 ] reported improved force-generating capacity in sedentary men over a 24-h recovery period after whey hydrolysate ingestion. However, it is unclear whether these findings are similar in trainedathletesand/orwhenwheyisconsumedafteraneveningboutofexercise. Furthermore,studiesexamining the relationship between exercise recovery and protein ingestion post-exercise tend to use a between-group [ 24 , 25 ] rather than a repeated-measures experimental design, and sometimes withoutcontrolling for diet [ 24 , 26 ]. Both of these factors are potentially important in order to draw meaningful conclusions regarding the effect of a nutritional supplement towards enhancing performance [ 27 ]. Therefore, additional research is warranted to determine to what extent protein supplementation mayfacilitate a more rapid recovery of muscle performance after an acute bout of resistance exercise. Thus,in the present study, we employed a crossover design, controlled diet, and conducted a battery of tests to assess the recovery of exercise performance. The primary aim of the present study was to determine if consuming a whey protein supplement post-exercise enhances whole body net protein balance over a 10 h overnight recovery period. Moreover, given the unequal distribution of dietary protein typical of Western diets [ 28 ], a secondary  Nutrients  2017 ,  9 , 735 3 of 18 aim was to determine if the greater 10 h overnight response could be sustained over 24 h in a free-living environment by supplementing the breakfast meal with a second protein supplement. Finally, given the ability of whey protein to enhance post-exercise rates of muscle protein synthesis, which would presumably enhance the repair of exercise-induced muscle damage, we also conducted performance tests to assess the recovery of muscle strength and endurance as well as anaerobic power and neuromuscular function over 10 and 24 h of recovery. We hypothesized that protein supplementationwould enhance net protein balance at 10 and 24 h of recovery, primarily by enhancing protein synthesis, and that this response would be associated with greater indices of exercise performance. 2. Materials and Methods 2.1. Experimental Protocol Twelve healthy young men (76 ± 8 kg, 24 ± 4 years old, 14% ± 5% body fat; means ± standard deviation (SD)), who were resistance training two to four times per week for at least six months,provided written consent to participate in a protocol that was written in accordance with standardsset by the revised (2008) Declaration of Helsinki, and that was approved by the research ethics board at the University of Toronto, Toronto, Canada (protocol # 32576). Additional self-reported inclusion criteria to participate were as follows: non-smoking, no supplement consumption for at least 3 weeks prior to the trial’s commencement, and no medication that may affect protein metabolism (e.g., corticosteroids or non-steroidal anti-inflammatories). Participants completed a Physical Activity Readiness Questionnaire ([ 29 ], revised 2002 version) in order to help confirm that they could safely perform the exercise protocol. After an overnight fast, air displacement plethysmography (BOD-POD, COSMED USA Inc., Chicago, IL, USA) was used characterize participant lean mass, fat mass, and  body composition (Supplemental Table S1). 2.2. Carbohydrate and Protein Supplemented Trials In a double-blind placebo-controlled crossover fashion, participants performed a strenuous bout of whole body resistance exercise in the evening prior to consuming one serving of MuscleTech100% Whey protein (PRO) or an energy-matched placebo (CHO). The supplements were consumed immediately after exercise as well as the following morning (i.e., after 10 h of recovery). One serving of the protein supplement contained 25 g of whey protein (a proprietary blend of whey peptides, isolates, and concentrates), 2.5 g fat, and 3 g carbohydrate, yielding ~130 kcal of energy. The supplements were consumed on each of the two trial days (two trial days per condition; see Figure 1) in addition tocontrolleddiets(describedbelow). Atthebeginningofeachtrial,participantscompletedaperformance test and then consumed a mixed-macronutrient meal (~18:00), which was a standardized proportion of their daily controlled diet: 28% kcal, 20% protein, 31% carbohydrate, and 31% fat. Participants then completed the remainder of the given trial (i.e., whole-body resistance exercise at 20:00, according to Figure 1). Trial randomization, study blinding, and supplement preparation were performed by an individual who was external to the study. Each trial was separated by approximately one week.  Nutrients  2017 ,  9 , 735 4 of 18   Figure 1.  A schematic representation of the trial day. Participants were free-living in recovery andconsumed a controlled diet that mimicked their habitual dietary intake. * Exercise: on supplementedtrials only; whole body, heavy resistance exercise.  †  Isometric maximal voluntary contraction,squat jump, Wingate test, knee extension repetitions to failure at 75% of 1-repetition maximum. ‡  Mixed-macronutrient meal. A twenty-five gram (25 g) whey protein supplement (PRO) or isocaloric carbohydrate (control; CTL) supplement. Q, nitrogen turnover; S, whole body protein synthesis; B, whole body protein breakdown; NB, whole body net protein balance. Urine collection was collected over two intervals: 0–10 h, and 10–24 h; after obtaining a sample from the 0–10 collection, both collections were pooled to obtain a 24 h recovery sample. 2.3. Rest Trial A third randomized trial involving no exercise and no supplement served as a rested control trial (Rest), and controlled for potential time-of-day effects in performance testing [ 30 ]. All of the aspects of the rested trial were identical to the supplemented trials described above, except that participants rested (sat quietly) in the laboratory instead of performing a whole body resistance exercise bout and consuming a supplement. 2.4. Dietary Controls Prior to the study trials, participants completed 3-day diet logs. The diet logs were analysed using ESHA (Elizabeth Stewart Hands and Associates, company founders) Research Food Processor Nutrition Analysis Software (Salem, OR, USA). Prepackaged diets were prepared by a registereddietician, and provided energy requirements estimated using the Harris–Benedict equation and a moderate activity factor (1.5). Participants were provided with four individualized meals on each of  the two trial days for each of the three conditions (Rest, CHO, PRO). The protein content providedin the controlled diets was equal to habitual intake, and was evenly distributed between the four meals. The carbohydrate content provided was 4–5 g/kg/day. Fat provided the balance of total energy. A food checklist was completed by each participant to track dietary compliance. Pilot data from our lab estimated that the energy expended as a result of the whole body exercise used in the present study was ~200 kcal. Given that each supplement (protein or carbohydrate placebo) provided after the exercise bout contained 130 kcal of energy, participants consumed an additional 70 kcal of energy in the form of a protein-free cookie [31] to help achieve energy balance during overnight recovery. 2.5. Exercise Participants were familiarized with performance test protocols and the whole body resistanceexercise bout approximately one week before the first trial. Participants’ three repetition maximum(RM) strength was determined for the exercises to be performed in the whole body exercise trials.The exercise bout (CHO and PRO trials only) consisted of supersets of barbell bench press and pulldown superset, and barbell overhead press and seated row, respectively, as well as leg press andleg extension (isolated). For all of the supersets or isolated exercises, participants performed 4 sets of 
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