MYTH AND DEFINITION
The underlying myth that strength training requires extremely high dietary protein intakes to maximize the muscular adaptive processes has resulted in an unnecessary high increase in protein consumption for many athletes (55).
The fundamental relationship of strength being proportional to an increase in lean body mass (LBM) accentuates the above belief (54). As a result, important aspects of sport-specific neural adaptations (49) become de-emphasized. This review will outline the effects of resistance exercise (RE) on the individual pathways of protein accretion in skeletal muscle, in both trained and novice subjects, to provide protein requirements for strength training.
“Strength training” can be defined as “anaerobic conditioning,” which means that it is predominantly the ATP-CP and glycolytic system that are stressed during strength-based activity (2,3,35,61). These anaerobic activities can be categorized as any type of activity performed against an external resistance, using sets and repetitions interspersed with rest periods, which can induce muscular adaptations, including strength and hypertrophy. RE, including the use of dumbbells, barbells, and weight machines, is easily quantifiable, monitorable, and progressive and hence, is the most common mode of strength training, often synonymous with a “strength athlete” (30). It is worth noting that strength training principles applied to repetition, sets, and rest are implemented to train for the individual aspects within the strength continuum ranging from strength endurance to maximum strength (48). Following the traditional periodization model, the aim of a “strength endurance phase” is to increase work capacity and, as a side effect, produce body composition changes such as muscle hypertrophy within a rep range of 8–20 reps, 3–5 sets, 1–3 sessions per day, and 3–4 days a week (22,48). Following on “strength to maximum strength phases” are characterized by a reduction in volume and an increase in intensity eliciting neural–muscular adaptations with no more than 6 reps, 3–5 sets, and between 3 and 6 days per week (48).
OVERVIEW OF PROTEIN METABOLISM AND HABITUAL INTAKES
The major functions of dietary protein can be summarized as structural (collagen of bone and skin), regulatory (peptide hormones), contractile (actin and myosin filaments), transport (hemoglobin), catalytic (enzymatic), and energetic (gluconeogenic) (64). Proteins are made up of amino acids ( AAs) that serve as building blocks and stimulate muscle protein synthesis (MPS) (17,31,67). Non-essential AAs (non-EAAs) can be synthesized within our body, whereas EAAs must be obtained from the diet (55). To reach equilibrium, synthesized protein from the AA pool (Figure 1) needs to restore the continually degrading body protein (31). If there are insufficient AAs, caused by inadequate dietary protein intake in the free AA pool, the rate of protein synthesis cannot match the rate of protein degradation. This could result in losses to strength, body mass, and athletic performance (31).
The current Recommended Daily Allowance (RDA) of protein for the normal population is 0.8 g/kg body weight per day (18). The RDA only covers 97.5% of the population, and it would be appropriate to assume that most athletes, specifically those concerned with gaining LBM, that is, strength athletes, would fall within the 2.5% that is not covered within this recommended protein allowance (44).
Habitual protein intakes of strength athletes range from 1.6 to 2.8 g/kg body weight per day, averaging 2 g/kg body weight per day (55), which clearly highlights a considerable increase in protein consumption above the RDA for the sedentary population of 0.8 g/kg body weight per day.
Optimal protein intake promotes maximal functioning of all protein requiring processes, emphasizing protein synthesis. It does not allow an elevation in urea synthesis (nitrogen loss), AA oxidation, or reliance of protein oxidation during prolonged exercise. Furthermore, optimal protein intake causes the continuation or maintenance of sports specific adaptations, that is, maintaining LBM, under less optimal circumstances such as during periods of reduced caloric intake (44).
THE RELIABILITY OF THE MEASUREMENT MODELS OF PROTEIN TURNOVER
THE NITROGEN BALANCE METHOD
The body excretes nitrogen compounds, and proteins consist of 16% nitrogen (60). Total measurement of nitrogen intake in comparison to total excretion either results in a positive (anabolic) or negative (catabolic) state (42). The use of the nitrogen balance (NBAL) method presents various concerns.
First, NBAL is achievable with decreased protein intake resulting in a more efficient AA reutilization and a lower AA flux (42,57), thus underestimating optimal functioning. As a result, physiological adaptations desired for strength training, that is, muscle hypertrophy are significantly reduced. Second, high-positive NBAL does not result in expected LBM accrual (59,70,71). Third, NBAL cannot detect changes in the various components of protein metabolism (31). Furthermore, at high protein intakes, there is an overestimation of nitrogen retention coupled with an underestimation of nitrogen excretion (32,57,59,70,71) and an appreciable amount of nitrogen can be lost through the skin, which is difficult to measure (42).
The conceptual framework, comprised by Young et al. (70,71) using stable isotopes tracers, consists of 4 states: first, “protein deficiency,” defined as the maximal reduction in AA oxidation/protein synthesis to all but the essential organs; second, “accommodation,” where NBAL is achieved with a decrease in physiological relevant processes; third, “adaptation,” in which optimal dietary protein intake for growth, interorgan AA exchange, and immune function are present; and finally, “excess,” characterized by AAs oxidization for energy and excretion via urea (24,55,59,72), resulting in no further stimulation of protein synthesis (57). Protein intake would be optimal at a value that corresponded with where AA oxidation and urea production starts to increase exponentially with a plateau in protein synthesis (72). The use of stable isotopes tracers makes it possible to investigate the individual components of protein metabolism, that is, synthesis, breakdown, and oxidation (Figure 1), allowing a far more detailed analysis as portrayed by the conceptual framework outlined above.
RE can result in an increase in strength, power, and/or LBM over time depending on the specified goal for the relevant training period (29). Optimal protein requirements for this training period will be influenced by factors such as volume/intensity, carbohydrate intake, and timing of nutrient intake (14,25,26,37,61). A useful study to advance this area would be to provide a large group (n > 40) of untrained/trained people with various protein intakes determining which intake at which time promotes optimal physiological adaptations, that is, muscle strength and muscle mass. As this would be very time consuming and expensive, dietary protein recommendations need to be taken from smaller studies and, therefore, an “uncertainty factor” (54) based on the understanding of the above limitations needs to be included into any recommendation.
EFFECTS OF RESISTANCE EXERCISE ON PROTEIN METABOLISM
Muscle hypertrophy and the resultant increase in LBM is a desired aim for athletes engaging in strength training (54). RE stimulates repair and remodeling of structural proteins (4), but for this to occur, there must be a net positive protein balance which means synthesis must exceed breakdown (Figure 2). It is important to note that myofibrillar protein turnover, part of the repair and remodeling process, requires a period of prolonged stimulus of 6–8 weeks because it is relatively slow (51).
An early study carried out by Chesley et al. (13), using the tracer method, showed that there is an increase in MPS between 4 and 24 hours postexercise, however, increases in MPS immediately after exercise (0–4 hours) could only be assumed. Additionally, this study did not clarify whether the subjects were experienced or novice strength athletes. It has been shown that strength athletes have higher resting levels of whole body protein synthesis (WBPS) in comparison to sedentary individuals (45,47). This is very likely a chronic adaptation rather than an acute effect of RE, as mixed MPS at similar levels were observed during, and 2 hours after, a resistance-based exercise session (56). However, several stable isotope studies have shown that RE stimulates MPS in the postexercise period from 3 to 24 hours in trained subjects (5,27,38,46,69), returning to resting levels by 36 hours (13,34) and >48 hours in untrained subjects (46). There is a weakened rise in MPS to acute resistance training in trained versus untrained individuals (47). This provides support for the idea that RE is anabolic and results in the conservation of body protein not loss (44).
Distinguishing between mixed MPS and myofibrillar MPS is of uttermost importance because hypertrophy involves the accumulation of myofibrillar proteins (27). It has been assumed that changes in myofibrillar MPS would be similar to those seen in mixed MPS in trained subjects after resistance training. However, the change pattern of myofibrillar MPS is significantly different (27). The same rise in myofibrillar protein was observed within trained versus untrained states, yet untrained subjects also showed a rise in mixed MPS. This concludes that the elevation of WBPS in a trained state consists of nonfibrillar proteins showing that the signaling pathway in the trained state is defined with preference toward synthesis of myofibrillar proteins (27). Hence, mixed MPS, which includes subfractions of collagen, sarcoplasmic, and mitochondrial proteins, in trained individuals, does not have a significant contribution to protein accrual, which as noted above occurs within the first 24 hours after RE (46).
This chronic adaptation of constant, elevated, mixed MPS at rest consists of an overall increased rate of protein turnover other than myofibrillar proteins that is reflected in increased damaged protein clearance rates and protein renewal (26,52,53). The limitations of this study are that it was done in a fasted state, which could be a reason for the weakened mixed MPS response within the trained subject. Furthermore, all subjects were untrained, and an 8-week 3× per week resistance protocol will significantly elevate MPS in untrained subjects (47). As myofibrillar proteins by weight comprise of approximately 60% of all proteins (65), it is reasonable to postulate, given the magnitude of the increase observed in the current and previous studies (4,13,46,47,69), that an increase in the myofibrillar and cellular synthetic rate would occur (4,13,46,47,69). As a result, hypertrophy on both levels, myofibrillar and cellular, that is, the expansion of cellular proteins containing sarcoplasmic constituents is induced (28,33,45,47). The fact that the resting state of MPS is elevated in the trained state, and no further acute increase after RE was observed, could be an indication of insufficient overload and intensity.
To further strengthen the above evidence, further research is necessary that examines the relationship of mixed MPS and myofibrillar MPS using a maintenance routine and a sufficient-enough overload routine on experienced athletes, assuming cellular hypertrophy is exhausted.
It has been shown that RE increases the muscle protein breakdown (MPB) (46), although to a lesser degree than increasing MPS, thus rendering the muscle in a less negative net protein balance. Furthermore, the elevated protein breakdown rates return to baseline rates twice as quick as the protein synthesis rates (12 hours compared to 24 hours) (46).
Taken together, the postexercise effects of resistance training on MPS and MPB form the basic argument for a protein intake, such as 20 g, or in a ratio of 1:3 (26,40) in conjunction with carbohydrate using the insulin-mediated permissive effect on protein synthesis and attenuation of protein breakdown (12,39,55,61) within the first 30 minutes after exercise (25,26).
RECOMMENDED PROTEIN REQUIREMENTS FOR STRENGTH TRAINING
RE results in muscle hypertrophy meaning net muscle accrual, where MPS exceeds MPB (31,43). Nevertheless, RE alone cannot induce hypertrophy unless combined with additional AA feeding as the protein balance is less negative, hence still catabolic, and not yet positive/anabolic (5,55). However, the extent of this increase in demand of AAs is dependent on various factors such as the trained status of the individual (novice/advanced) (27,55), duration, intensity, and frequency of the training program (20,29).
Various studies have shown that RE, with protein intake close to the RDA, facilitates accommodation rather than adaptation through increased nitrogen utilization efficiency, lowering the rate of WBPS in novice (63) and older strength athletes (11).
An early study undertaken by Tarnapolsky et al. (59) has shown that protein requirements for strength athletes are between 1.0 and 1.2 g/kg body weight per day and only slightly higher than the RDA of 0.8 g/kg body weight per day. The resistance routine used within this study did not increase net protein catabolism, and in addition, LBM can be maintained with protein intakes considerably less than previously suggested and/or habitually consumed. However, the athletes in this study carried out a maintenance routine which in general is a reduction in frequency and duration and not inductive for hypertrophy (30). Hence, for maintaining LBM, a modest increase in protein intake is required only for supporting the higher turnover (57). Furthermore, the above could be a result of accommodation rather than adaptation. A combination of NBAL and the tracer method would have been useful in determining the individual effected processes.
A comparison study of 6 sedentary to 7 novice strength athletes measuring NBAL, WBPS, leucine oxidation, and protein breakdown at different levels of protein intakes showed that protein synthesis seemed to plateau at about 1.4 g/kg body weight per day, but the exact point of increase in AA oxidation could not be established (57). However, at 2.8 g/kg body weight per day, leucine oxidation nearly doubled, showing that excess protein was oxidized for energy. The small numbers involved in this study (n = 4), and the fact that there was an aerobic element present (football/rugby drills and a circuit resistance routine), could have increased the protein requirements slightly, as endurance athletes require up to twice the RDA depending on intensity, which in this case, would be reasonably high, that is, >60% V[Combining Dot Above]O2max (55).
Conversely, Hartman et al. (23) observed a significant LBM increase in novice strength athletes while consuming 1.2 g/kg body weight per day and a reduction in whole body protein turnover increasing whole body protein retention. However, various flaws could be highlighted in this study. First, if a higher dosage of protein was used per day, there may have been even greater muscle hypertrophy suggesting that the used dosage was not optimal but accommodational. Second, the subject's body mass index averaged at >25. As the subjects were “novice” athletes and no body fat data was provided, it could be assumed that they were overweight (68). It would have been more appropriate to measure protein requirements against LBM, which in this case could be considerably higher. The hypothesis would be that RDA compared to LBM was already sufficient and any increase would result in more positive NBAL still not providing optimal amounts of AAs. However, the recommended protein requirements for novice resistance-based athletes are widely gauged at around 1.5–1.7 g/kg body weight per day (31,32).
The above studies clearly expel the myth of excess protein requirements in strength athletes, although exact measures can only be assumed, as it is near impossible to set a study protocol that accurately measures the point of an exponential increase in AA oxidation and a plateau in protein synthesis. However, any excess protein above the optimal point for growth or maintenance will be diverted into oxidative pathways (55). It is worth noting that unnecessarily high protein intakes, such as the 2.7 g/kg body weight per day habitually consumed by strength athletes (59), in combination with pre-existing renal disease may cause an acceleration of the disease (19). There is, however, no evidence that this risk also applies to healthy individuals (62).
In light of the above, further research needs to be undertaken to narrow the range of optimal protein requirements for novice strength athletes by controlling subject selection. For example, a forward within rugby could already be classified as an experienced strength athlete because of the nature of his positional sporting movements, that is, maximum push and squatting actions with intermediate to long recoveries.
Besides the fact that an advanced strength athlete has a higher WBPS as part of a chronic adaptation to RE (27,45,47,56), no research to date has estimated when an initial acute adaptation becomes chronic. Hence, a longitudinal study should be undertaken to follow willing subjects from sedentary to novice to advanced strength athletes using periodized resistance programs, where the aerobic element is minimized.
TIMING AND AMOUNT OF PROTEIN
Having established the ranges of protein requirements for novice and experienced strength athletes, it is essential to consider the timing of protein intake. Although the net protein balance is less negative because of an increase in MPS and a lesser increase in MPB, a positive protein balance has only been observed once combined with AAs ingestion stimulating MPS (5).
Large daily protein intakes, such as 2.8 g/kg body weight per day (57), can stimulate protein oxidation and will only have a limited anabolic effect on synthesis (55) by attenuating the fractional synthetic rate of the muscle (9). It has been shown that the metabolic response within the skeletal muscle is comparative in stimulating MPS when 3–6 g of EAAs are ingested at 1 and 2 hours pre-RE (10). In a study undertaken by Tipton et al. (61), the consumption of 15 g of EAAs before and 1 hour after RE has shown to cause an anabolic response. Delaying protein consumption by 2 hours can have a significant negative effect on muscle hypertrophy (16). Although it should be noted, that the subjects in this study were elderly and not athletes. A diminished hypertrophic response to strength training in the elderly has been evidenced because of an underestimation of training load based on age-related diminished baseline strength (21,65). Hence, the possibility of not reaching the threshold for the amount of weight that must be lifted before hypertrophy was induced (36), which is unknown in young and old groups, could have exaggerated the above negative outcome.
Protein intake of 20 g immediately after RE has been shown to induce optimal MPS in novice athletes (40), with anything greater than 20 g increasing protein oxidation (40). Nevertheless, this should only be used as a rough guideline for elite athletes, as their requirements could be slightly lower because of the chronic elevation of MPS observed in trained subjects (27,45,47,56).
It is important to note the effects of combined carbohydrate and protein ingestion to aid recovery. Carbohydrate ingestion immediately after exercise aids glycogen resynthesis (25) and when consumed in isolation, it has a positive effect on NBAL via an insulin-induced mechanism (12,39,60). This increases the AA transport 3-fold, which reduces MPB, but there is no effect on MPS (6).
The interactive effect of carbohydrate and AAs forms the basis of a combined recovery intake (39), offsetting muscle damage (1), with solid and liquid forms promoting similar levels of resynthesis (58). It is worth noting that intact dietary proteins such as milk, which includes both fast (whey) and slow (casein) dietary protein, further increase the rate of MPS compared to fast proteins alone such as soy (66).
In conclusion, the consumption of carbohydrate and protein within the first 30 minutes after exercise (25), during exercise (7,8), and pre-RE (61) needs to be considered to elicit maximal myofibrillar adaptations (7,14,27,40,61).
The stimulation of protein synthesis only requires EAA with non-EAAs offering no additional benefit (62). EAAs, in comparison to intact proteins, double the anabolic stimulus and increase the reutilization of AAs, which would normally be excreted or wasted (11). Therefore, high-quality protein only stimulates MPS in proportion to the amount of EAAs that it consists of, in general, making up 40–45% of high-quality protein, such as whey or casein (17).
Knowing that the habitual protein intake of a strength athlete is on average 2 g/kg body weight per day (54), it is safe to say that whether novice or advanced, protein requirements for maintaining and/or gaining LBM are being met. Evidence has clearly shown that actual protein requirements for strength training are significantly lower at 1.2 g/kg body weight per day for advanced and 1.5–1.7 g/kg body weight per day for novice (31,32,43,57,59).
Furthermore, there is clearly a placebo effect that is due to the myth or mind-set and resultant habit adopted by most strength athletes (41). Such an effect is defined as the psychological or psychophysiological effect produced by placebos (50). The emphasis of high protein intakes and its relationship to LBM accrual as a result of RE could be a psychological contributing factor to program adherence in itself (15). It would be interesting to study the effects on performance if a reduced but adequate protein dosage is consumed with an increase in carbohydrate.
Nevertheless, negating the limitations of the reviewed studies and the reliability issues of methods used to examine protein turnover, such as the NBAL method, an important fact has been brought to light. Ingestion of 6 g of protein in conjunction with 35 g of carbohydrate before exercise (60), 40 g coupled with 6 g of EAA during exercise (7,8), and 1.5 g/kg body weight of carbohydrate together with 20 g of protein within the first 30 minutes postexercise (8,14,25,27,40,61) has shown to increase recovery and maximize adaptive process within the muscle, assuming overall daily protein requirements will be met.
Finally, the current recommendations and their applicability to elite athletes partaking in strength training are limited, as either novice or recreationally experienced athletes were used in the studies reviewed. Further research investigating optimal protein requirements linked to the individual aims of a periodized strength program over time at the elite level and its effect on performance is essential.
1. Baty JJ, Hwang H, Ding Z, Bernard JR, Wang B, Kwon B, Ivy JL. The effect of a carbohydrate and protein supplement on resistance exercise
performance, hormonal response, and muscle damage. J Strength Cond Res 21: 321–329, 2007.
2. Beachle TR, Earle RW. Essentials of Strength and Conditioning (2nd ed). Champaign, IL: Human Kinetics, 2000. pp. 64–66, 393–424.
3. Beachle TR, Earle RW. Essentials of Strength and Conditioning (2nd ed). Champaign, IL: Human Kinetics, 2000. pp. 140–141.
4. Biolo G, Maggi SP, Williams BD, Tipton KD, Wolfe RR. Increased rates of muscle protein turnover
and amino acid transport after resistance exercise
in humans. Am J Physiol 268: E514–E520, 1995.
5. Biolo G, Tipton KD, Klein S, Wolfe RR. An abundant supply of amino acids enhances the metabolic effect of exercise on muscle protein. Am J Physiol 273: E122, 1997.
6. Biolo G, Williams BD, Flemming RY, Wolfe RR. Insulin action on muscle protein kinetics and amino acid transport during recovery after resistance exercise
. Diabetes 48: 949–957, 1999.
7. Bird SP, Tarpenning KM, Marino EF. Independent and combined effects of liquid carbohydrate/essential amino acid ingestion on hormonal and muscular adaptations following resistance training in untrained men. Eur J Appl Physiol 97: 225–238, 2006.
8. Bird SP, Tarpenning KM, Marino FE. Liquid carbohydrate/essential amino acid ingestion during a short-term bout of resistance exercise
suppresses myofibrillar protein degradation. Metabolism 55: 570–577, 2006.
9. Bolster DR, Pikosky MA, Gaine PC, Martin W, Wolfe RR, Tipton KD, Maclean D, Maresh CM, Rodriguez NR. Dietary protein intakes impacts human skeletal muscle protein fractional synthetic rates after endurance exercise. Am J Physiol Endocrinol Metab 289: E648–E657, 2002.
10. Borsheim E, Tipton KD, Wolf SE, Wolfe RR. Essential amino acids and muscle protein recovery from resistance exercise
. Am J Physiol Endocrinol Metab 283: E648, 2002.
11. Campbell WW, Crim MC, Young VR, Joseph LJ, Evans WJ. Effects of resistance training and dietary protein intake on protein metabolism in older adults. Am J Physiol 68: E1143–E1153, 1995.
12. Castellino P, Luzi L, Simonson DC, Haymond M, DeFronzo RA. Effect of insulin and plasma amino acid concentrations on leucine metabolism in man. Role of substrate availability on estimates of whole body protein synthesis. J Clin Invest 80: 1784–1793, 1987.
13. Chesley A, MacDougall JD, Tarnopolsky MA, Atkinson SA, Smith K. Changes in human muscle protein synthesis
after resistance exercise
. J Appl Physiol 73: 1383–1388, 1992.
14. Coburn JW, Housh DJ, Housh TJ, Malek MH, Beck TW, Cramer JT, Johnson GO, Donlin PE. Effects of leucine and whey protein supplementation during eight weeks of unilateral resistance training. J Strength Cond Res 20: 284–291, 2006.
15. Desharnais R, Jobin J, Cote C, Levesque L, Godin G. Aerobic exercise and the placebo effect: A controlled study. Psychosom Med 55: 149–154, 1993.
16. Esmarck B, Andersen JL, Olsen S, Richter EA, Mizuno M, Kjaer M. Timing of postexercise protein intake is important for muscle hypertrophy with resistance training in elderly humans. J Physiol 535: 301–311, 2001.
17. Ferrando AA, Tipton KD, Wolfe RR. Essential amino acids for muscle protein accretion. Strength Cond J 32: 87–92, 2010.
18. Food and Nutrition Board. Dietary Reference Intakes (DRIs): Recommended Intakes for Individuals, Macronutrients. Institute of Medicine: Washington, DC. 2010.
19. Friedman AN. High-protein diets: Potential effects on the kidney in renal health and disease. Am J Kidney Dis 44: 950–962, 2004.
20. Fry AC. The role of resistance exercise
intensity on muscle fibre adaptations. Sports Med 34: 663–679, 2004.
21. Grimby G, Saltin B. The ageing muscle. Clin Physiol 3: 209–218, 1983
22. Haff G. Roundtable discussion: Periodization of training—Part 1. Strength Cond J 26: 50–69, 2004.
23. Hartman JW, Moore DR, Phillips SM. Resistance training reduces whole-body protein turnover
and improves net protein retention in untrained young males. Appl Physiol Nutr Metab 31: 557–564, 2006.
24. Hickson JF, Hinkelmann K, Bredle DL. Protein intake level and introductory weight training exercises on urinary total nitrogen excretions from untrained men. Nutr Res 8: 725–731, 1988.
25. Ivy JL. Glycogen resynthesis after exercise: Effect of carbohydrate intake. Int J Sports Med 19: S142–S145, 1998.
26. Ivy JL, Goforth HW, Damon BM, McCauley TR, Parsons EC, Price TB. Early postexercise muscle glycogen recovery is enhanced with a carbohydrate-protein supplement. J Appl Physiol 93: 1337–1344, 2002.
27. Kim PL, Staron SR, Phillips SM. Fasted-state skeletal muscle protein synthesis
after resistance exercise
is altered with training. J Physiol 568(Pt 1): 283–290, 2005.
28. Klitgaard H, Ausoni S, Damiani E. Sarcoplasmic reticulum of human skeletal muscle: Age-related changes and effect of training. Acta Physiol Scand 137: 23–31, 1989.
29. Kraemer WJ, Deschenes MR, Fleck SJ. Physiological adaptations to resistance exercise
: Implications for athletic conditioning. Sports Med 6: 246–256, 1988.
30. Kraemer WJ, Ratames NA, Rubin MR. Basic principles of resistance training. In: Nutrition and the Strength Athlete. Ratzin Jackson CG, ed. Boca Raton, FL: CRC Press, 2001. pp. 1–31.
31. Lemon PW. Dietary protein requirements
in athletes. J Nutr Biochem 8: 52–60, 1997.
32. Lemon PW, Tarnopolsky MA, MacDougall JD, Atkinson SA. Protein requirements
and muscle mass/strength changes during intensive training in novice bodybuilders. J Appl Physiol 73: 767–775, 1992.
33. Louis M, Poortmans JR, Francaux M, Berre J, Boisseau N, Brassine E, Cuthbertson DJ, Smith K, Babraj JA, Waddell T, Rennie MJ. No effect of creatine supplementation on human myofibrillar and sarcoplasmic protein synthesis after resistance exercise
. Am J Physiol Endocrinol Metab 285: E1089–E1094, 2003.
34. MacDougall JD, Gibala MJ, Tarnopolsky MA, MacDonald JR, Interisano SA, Yarasheski KE. The time course for elevated muscle protein synthesis
following heavy resistance exercise
. Can J Appl Physol 20: 480–486, 1995.
35. McArdle WD, Katch FI, Katch VL. Exercise Physiology, Energy, Nutrition and Human Performance (4th ed). Baltimore, MD: Williams and Wilkins, 1996. pp. 193–195.
36. McDonagh MJN, Davies CTM. Adaptive response of mammalian skeletal muscle to exercise with high loads. Eur J Appl Physiol 71: 644–650, 1991.
37. Mettler S, Mitchell N, Tipton KD. Increased protein intake reduces lean body mass loss during weight loss in athletes. Med Sci Sports Exerc 42: 326–327, 2010.
38. Miller SL, Tipton KD, Chinkes DL, Wolf SE, Wolfe RR. Independent and combined effects of amino acids and glucose after resistance exercise
. Med Sci Sports Exerc 35: 449–455, 2003.
39. Moller-Loswick AC, Zachrisson H, Hyltander A, Korner U, Matthews DE, Lundholm K. Insulin selectively attenuates breakdown of nonmyofibrillar proteins in peripheral tissues of normal men. Am J Physiol 266: E645–E652, 1996.
40. Moore DR, Robinson MJ, Fry JL, Tang JE, Glover EI, Wilkinson SB, Prior T, Tarnopolsky TA, Phillips SM. Ingested protein dose response of muscle and albumin protein synthesis after resistance exercise
in young men. Am J Clin Nutr 89: 161–168, 2009.
41. Nissen SL, Sharp RL. Effect of dietary supplements on lean mass and strength gains with resistance exercise
: A meta-analysis. J Appl Physiol 94: 651–659, 2003.
42. Pellet PL. Protein requirements
in humans. Am J Clin Nutr 51: 723–737, 1990.
43. Phillips SM. Protein requirements
and supplementation in strength sports. Nutrition 20: 689–695, 2004.
44. Phillips SM. Dietary protein for athletes: From requirements to metabolic advantage. Appl Physiol Nutr Metab 31: 647–654, 2006.
45. Phillips SM, Parise G, Roy BD, Tipton KD, Wolfe RR, Tamopolsky MA. Resistance-training-induced adaptations in skeletal muscle protein turnover
in the fedstate. Can J Physiol Pharmacol 80: 1045–1053, 2002.
46. Phillips SM, Tipton KD, Aarsland A, Wolf SE, Wolfe RR. Mixed muscle protein synthesis
and breakdown after resistance exercise
in humans. Am J Physiol 273: E99–E107, 1997.
47. Phillips SM, Tipton KD, Ferrando AA, Wolfe RR. Resistance training reduces the acute exercise-induced increase in muscle protein turnover
. Am J Physiol 276: E118–E124, 1999.
48. Plisk SS, Stone MH. Periodization strategies. Strength Cond J 25: 19–37, 2003.
49. Sale DG. Neural adaptations to resistance training. Med Sci Sports Exerc 20: S135–S145, 1988.
50. Shapiro AK, Shapiro E. Patient-provider relationships and the placebo effect. In: Behavioral Health: A Handbook of Health Enhancement and Disease Prevention. Matarazzo JD, Weiss SM, Heird JA, Miller NE, Weiss SM, eds. New York, NY: Wiley, 1984. pp. 371–383.
51. Staron RS, Karapondo DL, Kraemer WJ, Fry AC, Gordon SE, Falkel JE, Hagerman FC, Hikida RS. Skeletal muscle adaptations during early phase of heavy-resistance training in men and women. J Appl Physiol 76: 1247–1255, 1994.
52. Sultan KR, Dittrich BT, Leisner E, Paul N, Pette D. Fiber type-specific expression of major proteolytic systems in fast- to slow-transforming rabbit muscle. Am J Physiol Cell Physiol 280: C239–C247, 2001.
53. Sultan KR, Dittrich BT, Pette D. Calpain activity in fast, slow, transforming, and regenerating skeletal muscles of rat. Am J Physiol Cell Physiol 279: C639–C647, 2000.
54. Tarnapolsky MA. Building muscle to maximise bulk and strength adaptations to resistance exercise
training. Eur J Sports Sci 8: 67–76, 2008.
55. Tarnapolsky MA. Protein and amino acid needs for training and bulking up. In: Clinical Sports Nutrition (4th ed). Burke L, Deakin V, ed. Sydney, Australia: McGraw Hill, 2010. pp. 61–89.
56. Tarnapolsky MA, Atkinson SA, MacDougall JD, Senor PW, Lemon WR, Schwarcz HP. Whole body leucine metabolism during and after resistance exercise
in fed humans. Med Sci Sports Exerc 23: 326–333, 1991.
57. Tarnapolsky MA, Atkinson SA, MacDougall JD, Chesley A, Phillips SM, Schwarz HP. Evaluation of protein requirements
for trained strength athletes. J Appl Physiol 73: 1986–1995, 1992.
58. Tarnapolsky MA, Gibala M, Jeukendrup AE, Phillips SM. Nutritional needs of elite endurance athletes. Part 1: Carbohydrate and fluid requirements. Eur J Sports Sci 5: 3–14, 2005.
59. Tarnapolsky MA, MacDougall JD, Atkinson SA. Influence of protein intake and training status on nitrogen balance and lean body mass. J Appl Physiol 64: 187–193, 1988.
60. Tessari P, Inchiostro S, Bioli G, Trevisan R, Fantin G, Marescotti MC, Iori E, Tiengo A, Crepaldi G. Differential effects of hyperinsulinemia and hyperaminoacidemia on leucine-carbon metabolism in vivo. Evidence for distinct mechanisms in regulation of net amino acid deposition. J Clin Invest 79: 1062–1069, 1987.
61. Tipton KD, Rasmussen BB, Miller SL, Wolf SE, Owens-Stovall SK, Petrini BE, Wolfe RR. Timing of amino acid-carbohydrate ingestion alters anabolic response of muscle to resistance exercise
. Am J Physiol Endocrinol Metab 281: E197–E206, 2001.
62. Tipton KD, Wolfe RR. Protein and amino acids for athletes. J Sports Sci 22: 65–79, 2004.
63. Torun B, Scrimshaw NS, Young VR. Effect of isometric exercises on body potassium and dietary requirements of young men. Am J Clin Nutr 30: 1983–1993, 1977.
64. Volek SJ. General nutritional considerations for strength athletes. In: Nutrition and the Strength Athlete. Ratzin Jackson CG, ed. Boca Raton, FL: CRC Press, 2001. pp. 31–52.
65. Welle S, Totternman S, Thornton C. Effect of age on muscle hypertrophy induced by resistance training. J Geront 51: 270–275, 1996.
66. Wilkinson SB, Tarnapolski MA, MacDonald MJ, MacDonald JR, Armstrong D, Phillips SM. Consumption of fluid milk promotes greater muscle protein accretion after resistance exercise
than does consumption of an isonitrogenous and isoenergetic soy-protein beverage. Am J Clin Nutr 85: 1031–1040, 2007.
67. Wolfe RW. Regulation of muscle protein by amino acids. J Nutr 132: 3219S–3224S, 2002.
68. World Health Organization. Obesity and overweight, Fact sheet N°311, Geneva, Switzerland. 2005.
69. Yarasheski KE, Zachwieja JJ, Bier DM. Acute effects of resistance exercise
on muscle protein synthesis
rate in young and elderly men and women. Am J Physiol 265: E210–E214, 1993.
70. Young VR, Bier DM. A kinetic approach to the determination of human amino acid requirements. Nutr Rev 45: 289–298, 1987.
71. Young VR, Bier DM, Pellett PL. A theoretical basis for increasing current estimates of the amino acid requirements in adult man with experimental support. Am J Clin Nutr 50: 80–92, 1989.
72. Young VR, Scrimshaw NS, Bier DM. Whole body protein and amino acid metabolism: Relation to protein quality evaluation in human nutrition. J Agric Food Chem 29: 440–446, 1981.