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. 2018 Dec 28;10(1):70–79. doi: 10.1093/advances/nmy087

TABLE 1.

Effects of negative energy balance, dietary protein, exercise, and environment on body composition and muscle and whole-body protein turnover1

Study category;  author (ref) Volunteers Energy deficit Intervention Primary findings
Energy deficit and protein intake
 Carbone et al. (8) 39 recreationally active men (n = 32) and women (n = 7) 21 d, 40% (∼1000 kcal/d) Dietary protein intake at 0.8, 1.6, or 2.4 g · kg−1 · d−1; postabsorptive and postprandial (mixed-meal; 20 g protein) measures ED did not significantly alter ubiquitin-mediated proteolysis, but it was suppressed by acute feeding regardless of chronic dietary protein intake.
 Hector et al. (9) 40 overweight and obese men (n = 19) and women (n = 21) 2 wk, 28–34% (range: 680–860 kcal/d) Twice-daily isonitrogenous whey or soy or isoenergetic carbohydrate supplementation, resulting in dietary protein intakes of 1.3, 1.3, or 0.7 g · kg−1 · d−1, respectively ED suppressed postabsorptive muscle PS. Whey supplementation attenuated postabsorptive, and enhanced postprandial, muscle PS response, relative to soy or carbohydrate.
 Pasiakos et al. (10) 39 recreationally active men (n = 32) and women (n = 7) 21 d, 40% (∼1000 kcal/d) Dietary protein intake at 0.8, 1.6, or 2.4 g · kg−1 · d−1; postabsorptive and postprandial (mixed-meal; 20 g protein) measures Consuming higher-protein diets (double and triple the RDA) maintained the anabolic response to feeding during ED and preserved LBM during weight loss, compared with protein intake at the RDA.
 Pasiakos et al. (11) 39 recreationally active men (n = 32) and women (n = 7) 21 d, 40% (∼1000 kcal/d) Dietary protein intake at 0.8, 1.6, or 2.4 g · kg−1 · d−1; postabsorptive and postprandial (mixed-meal; 20 g protein) measures ED attenuated whole-body protein flux, PS, and PB, regardless of dietary protein intake. Acute feeding increased whole-body protein flux and PS, regardless of dietary protein intake. Higher-protein intakes increased protein oxidation and decreased net protein balance.
Energy deficit and exercise
 Carbone et al. (12) 10 recreationally active men (n = 6) and women (n = 4) 10 d, 20% (500 kcal/d) Postabsorptive measures taken after rest or after a 45-min moderate-intensity run ED increased muscle PB and caspase-3 activation without altering ubiquitin ligase expression or proteasome activity.
 Karl et al. (13) 23 male (n = 17) and female (n = 6) US soldiers 2 d, 93% (∼3680 kcal/d) Postabsorptive measures taken before and after significant exercise-induced energy expenditure (∼1300 kcal/d) during 2-d energy balance and subsequent 2-d ED High exercise-induced energy expenditure suppressed whole-body protein flux, PS, and PB. Subsequent ED increased PB without altering flux and PS, driving net protein balance more negative.
 Margolis et al. (14) 21 male Norwegian soldiers 4 d, 50% (3390 kcal/d) Postabsorptive measures after a 4-d, 54-km cross-country ski march Ski march and associated ED increased postabsorptive whole-body protein flux, PS, and PB.
 Margolis et al. (15) 73 male (n = 71) and female (n = 2) Norwegian soldiers 4 d, 50–60% (3000–3600 kcal/d) 24-h measures after a 4-d, 51-km cross-country ski march Ski march and associated ED suppressed 24-h whole-body protein flux, PS, and PB.
 Moberg et al. (16) 24 male (n = 17) and female (n = 7) Swedish soldiers 8 d, 29% (1690 kcal/d) for men and 15% (750 kcal/d) for women Postabsorptive measures before and after an 8-d military training exercise 8-d military training increased autophagy-related proteolysis without eliciting impactful changes in ubiquitin-mediated proteolysis.
Energy deficit, exercise, and protein intake
 Areta et al. (17) 15 resistance-trained men (n = 8) and women (n = 7) 5 d, 33% (−15 kcal · kg FFM−1 · d−1; ∼900 kcal/d) REX, postexercise placebo or 15 or 30 g whey protein ED suppressed muscle PS, but REX and postexercise protein increased muscle PS during ED.
 Berryman et al. (18) 63 male US Marines 7 d, ∼4200 kcal/d 7-d intensive military training with accompanying ED, followed by 27-d refeeding period providing supplemental protein (7, 84, or 133 g/d) to ad libitum diet Training and concomitant ED increased whole-body PB while lowering whole-body PS and net protein balance. Refeeding increased postabsorptive whole-body PS, PB, and net protein balance. Protein supplementation of a higher-protein diet (∼2.0 g · kg−1 · d−1) did not alter whole-body protein turnover.
 Hector et al. (19) 24 untrained men 10 d, 40% (1360 kcal/d) Dietary protein intake at 1.20 or 2.35 g · kg−1 · d−1; 5 REX sessions during 10-d ED ED suppressed muscle PS, but inclusion of REX abolished this decrease. Muscle PB was not significantly influenced by ED or REX.
 Josse et al. (20) 90 premenopausal overweight and obese women 16 wk, ∼25% (470 kcal/d) AEX and REX; high (30% kcal) or adequate (15% kcal) dietary protein intake High protein consumption during exercise- and diet-induced weight loss resulted in more favorable body composition changes than adequate protein, including greater LBM gain and fat mass loss.
 Longland et al. (21) 40 recreationally active, overweight men 4 wk, 40% (∼1560 kcal/d) HIIT and REX; high (35% kcal) or adequate (15% kcal) dietary protein intake Combining higher protein consumption with HIIT and REX induced greater LBM gain and fat mass loss than observed with adequate protein intake.
 Murphy et al. (22) 20 overweight and obese older men 4 wk, 300 kcal/d 2-wk ED followed by 2-wk ED with 3-d/wk REX; dietary protein provided at 1.3 g · kg−1 · d−1 either evenly distributed (25%/meal × 4 meals) or skewed (7%, 17%, 72%, 4%) over 4 meals ED suppressed myofibrillar PS. REX increased myofibrillar PS during ED. Evenly distributed protein intake increased postprandial myofibrillar PS, relative to skewed intake. Combining REX with evenly distributed protein intake, but not skewed intake, during ED restored myofibrillar PS rates to those observed during energy balance.
 Smiles et al. (23) 15 resistance-trained men (n = 8) and women (n = 7) 5-d, 33% (−15 kcal · kg FFM−1 · d−1; ∼900 kcal/d) REX, postexercise placebo or 30 g whey protein ED suppressed autophagy-related protein expression, but REX with postexercise protein consumption during ED enhanced the autophagy response.
Energy deficit, exercise, environment, and protein intake
 Berryman et al. (24) 17 recreationally active men 21-d, 70% (∼1840 kcal/d) 21-d acclimatization to HA (4300 m) with accompanying ED; dietary protein intake at 1.0 or 2.0 g · kg−1 · d−1 HA and accompanying ED induced significant loss of body weight and LBM, independent of dietary protein intake, and suppressed postabsorptive whole-body PS and PB. Higher-protein intake increased postabsorptive protein oxidation and drove whole-body protein balance more negative.
 Margolis et al. (25) 8 recreationally active men 21 d, 70% (∼1840 kcal/d) 21-d acclimatization to HA (4300 m) with accompanying ED; dietary protein intake at 1.0 or 2.0 g · kg−1 · d−1; acute aerobic exercise and postexercise recovery protein (25 g whey) ingestion HA exposure suppressed postexercise and recovery mTORC1 stimulation, an effect that was compounded by ED. Ubiquitin-mediated proteolysis was largely unaffected by HA.
Energy deficit and miRNA
 Margolis et al. (26) 16 sedentary, overweight, older men 28 d, 30% (800 kcal/d) Dietary protein at 1.0 g · kg−1 · d−1; plasma miRNA and 24-h whole-body protein turnover measures pre- and post-ED Expression of protein synthetic inhibitory miRNA increased after ED; this increase was inversely associated with whole-body PS.
 Parr et al. (27) 40 overweight and obese men and women 16 wk, ∼25% (500 kcal/d) Volunteers classified as either high- or low-responders based on body mass lost during ED (>10% vs. <5%) Specific miRNAs associated with exercise, dietary intervention, and/or weight loss were higher pre- and post-ED in hyper-responders, or increased post-ED regardless of weight-loss response.
1

AEX, aerobic exercise; ED, energy deficit; FFM, fat-free mass; HA, high altitude; HIIT, high-intensity interval training; LBM, lean body mass; miRNA, micro-RNA; mTORC1, mammalian target of rapamycin complex 1; PB, protein breakdown; PS, protein synthesis; ref, reference; REX, resistance exercise.