The Protein Paradox: Part II
by Greg Bradley-Popovich, MS, MS
There are several factors that can confound the results of experiments designed to assess protein needs of anaerobic trainees. Such extraneous variables have likely prevented some independent variables from reaching significance. Perhaps of greatest importance is energy balance. It is well established that there is an inverse relationship between energy intake and protein requirements in both sedentary people and in resistance-trained individuals (Lemon, 1995). This is due to the protein-sparing effect of dietary carbohydrate and fat. This issue especially presents problems in the study of recreational and competitive body builders who, in an attempt to minimize body fat, often establish a caloric deficit.
Surprisingly, the issue of energy balance was not fully addressed in the majority of the studies that were plotted. Although most studies stated the amount of energy consumed, few made an estimate of the total amount of energy expended by the subjects. Thus, it is unknown which test subjects make have been in negative, neutral, or positive energy balances. It is well established that energy status has a profound effect on nitrogen retention. Energy above needs results in nitrogen retention, whereas an energy deficit results in losses; quantitatively, this effect of energy on nitrogen retention amounts to about 2 g N for each 1000 kcal surplus of deficit (Munro, 1964). This unknown variable certainly could introduce error into the interpretation of such studies, and may help account for the inability of this report to show a significant correlation between nitrogen retention and energy intake irrespective of energy expenditure.
Another variable of paramount importance to nitrogen balance is possible anabolic androgenic steroid use by the test subjects. The importance of drug-free subjects for these studies cannot be overemphasized. It is widely recognized by those familiar with the sports of body building and weight lifting that a surprising number of body builders, especially those who compete, self-administer a number of prescription drugs including anabolic-androgenic steroids (Eliot, Goldberg, Kuehl, and Catlin, 1987; Friedl, 1994; Hatfield, 1993, p. 30; Hurley, et al., 1984; Kersey, 1993; Sherwood, 1993, p. 239; Tesch, 1992). It has been estimated that 90 percent of male professional body builders use anabolic-androgenic steroids at any given time (Catlin, Wright, Pope, and Liggett, 1993). Anabolic androgenic steroids with their profound affect on protein synthesis and degradation (Lombardo, 1993) could affect nitrogen balance studies. However, of the nine studies closely examined, only two studies, those of Lemon et al. (1992) and Walberg et al. (1988), reported an attempt to control for this variable. These researchers merely asked their participants if they had ever used steroids as opposed to actually testing for them. Due to the illegal status of steroids used for non-medical purposes and the possibility of expulsion from a study promising monetary reward, it is unlikely that such surveys would be answered with total honesty.
Of the remaining studies, it is very probable, based on previously cited references, that steroids were used among the competitive subjects in the studies of Celejowa and Homa and Laritcheva et al. On the contrary, it is extremely unlikely that the older neophytes in Campbell's study would have used physique-enhancing drugs. For the four remaining studies, it is unknown if any subjects had used or were using anabolic-androgenic steroids.
The age of the study participants was very consistent with most subjects being in their early to mid-twenties, with the sole exception of the study by Campbell et al. which focused on individuals averaging in their mid-sixties. Older individuals, it could be proposed, do not digest and absorb protein with the same efficiency as younger individuals and may therefore have different requirements. This argument alone would require an increase in dietary protein consumption to compensate, but the data are inconclusive in the sedentary elderly in general (National Academy of Sciences National Research Council, 1989). On the other hand, older trainees do not possess the same anabolic hormonal milieu as do younger trainees (LeMar, 1998a; LeMar, 1998b) and should not expect the same absolute increase in nitrogen retention from resistance training.
Also very consistent throughout the studies was the use of exclusively male subjects, with the exception of the study using senior citizens which used both males and females. It is unlikely that there is an intersex difference between males and females in their ability to utilize protein with the same efficiency (National Academy of Sciences National Research Council, 1989). However, it is possible that females cannot incorporate as much nitrogen daily for muscle growth since they secrete approximately one tenth as much of the anabolic hormone testosterone as males do (Holloway, 1994). Testosterone also elicits the secretion of other growth-promoting hormones that affect muscle protein metabolism (Kraemer, 1992 a). The hypertrophic response may even vary with the menstrual cycle (Kraemer, 1992 b). The role of gender on nitrogen retention deserves further exploration.
Among the nine studies examined, there were great differences in the training regimens regarding frequency, intensity, and duration. Though an attempt was made to normalize the data for average daily training time, this information is not very meaningful without an idea of how intense, or difficult, the workout protocols were. The vast majority of studies failed to report the intensity of the exercise programs. In addition, in some studies, the subjects each maintained their own personal resistance routine. It is true that the training strategies employed were highly variable, not necessarily productive, and could account largely for discrepancies between studies.
Studies such as Lemon's, which focus on the first few weeks of training for a novice trainee, have their place in the literature, for they suggest that protein needs are increased at the beginning of an exercise regimen. However, it appears that a leveling off occurs after a few weeks or months as the body learns to conserve protein. While this information may be helpful for those individuals just beginning a program, McCarthy quotes Butterfield as suggesting that these studies may partially account for inflated estimates of protein needs among athletes of various levels of experience. Butterfield expresses a need for long-term studies so that true protein needs may be accurately assessed (McCarthy, 1989).
Other extraneous variables exist that make designing, conducting, interpreting, and comparing studies assessing the adequacy of protein intake among anaerobic participants difficult. For example, variation in the quality (biological value) of the protein consumed in different studies would certainly be a consideration. A more recent concern is timing of the protein consumption relative to the strength-training bout, because it is postulated that protein utilization may be higher immediately following a workout (Lemon, 1997). Even the timing of post-workout carbohydrate ingestion can have effects on nitrogen retention (Roy, Tarnopolsky, MacDougall, Fowles, and Yarasheski, 1997).
Nitrogen balance studies, besides being quite difficult to employ due to their requiring collection of all urine, feces, sweat, etc., possess inherent errors that favor underestimation of nitrogen losses (Lemon and Proctor, 1991). Thus, an individual may appear to be in a positive nitrogen balance when that person is not, a situation referred to as a "false positive" (Reeds and Beckett, 1996). Energy deficits can further complicate nitrogen balance techniques. Even with these well-known short-comings, nitrogen balance studies have overwhelmingly supported the usefulness of high protein diets in increasing nitrogen retention. Additionally, the variability in nitrogen retention study results is often such that although perhaps the subjects were on average in a positive nitrogen balance, a few subjects were actually in a negative nitrogen balance. It must also be remembered that the objective of resistance training for most individuals should not be simply attaining a positive nitrogen balance, but attaining the most positive nitrogen balance possible while not compromising other dietary or health aspects.
Other shortcomings on nitrogen balance studies for the purpose of assessing resistance trainees have been published. Tarnopolsky, Atkinson et al. commented on an unidentified inherent error in the nitrogen balance method that may lead one to conclude that an excessive protein intake is of ergogenic benefit. Tarnopolsky, Atkinson et al. cite other studies in addition to theirs that point to a discrepancy between nitrogen balance and other measures of whole-body protein synthesis. Thus, they recommend that nitrogen balance be used in conjunction with other techniques.
A common misconception regarding nitrogen balance studies is that muscle hypertrophy is impossible when an individual is in negative nitrogen balance. In fact, muscle growth can occur when protein intake is insufficient by the stealing of amino acids from other organs. However, this process cannot continue indefinitely and a higher protein diet would likely prove superior (Lemon, 1995).
Much debate continues in regards to the possible health risks associated with a diet high in protein. Issues such as increased calcium excretion, increased saturated fat consumption, and renal damage are at the forefront of such controversy.
The belief that increased dietary protein results in a perturbation of calcium balance arises at least partly from studies which administered protein isolates devoid of their natural phosphorus while keeping dietary calcium and phosphorus constant. Such was the case with the study of Anand and Linkswiler (1974) which tested calcium retention against diets containing 47, 95, and 142 g protein/day, with the protein above 47 g/day being supplied as protein isolates. They found that the protein significantly increased urinary calcium excretion. Similarly, Allen, Oddoye, and Margen (1979) tested a diet containing 75 g protein daily versus 225 g protein daily while attempting to hold phosphorus intake constant. (Actually, the phosphorus content declined slightly in the high-protein group.) They, too, concluded that the high protein diet increased calcium excretion, also showing that maximum calcium excretion occurs within 3-5 days of beginning a high-protein diet and remains elevated for at least 3 months. A minimum of eight other studies were conducted in a similar fashion, keeping calcium and phosphorus intakes constant across various protein levels (Hegsted, Schutte, Zemel, and Linkswiler, 1981).
In contrast to the above findings, another study raised protein and phosphorous consumption proportionately. Protein intakes were 50 versus 150 g/day. No significant disturbances to calcium balance were documented (Hegsted, et al.). It is noteworthy that, to this point, all previously cited studies allowed only 500 mg calcium/day (<40% of the 1989 RDA). A more recent study showed that an increase in meat protein accompanied by an increase in inherent phosphorus minimized calcium losses. This study also tested a high-protein group including dairy products to bring the calcium ingestion from 590 mg/day to 1370 mg/day, which resulted in a highly positive calcium balance. Dairy products are helpful not just because of their calcium content, but because lactose may enhance calcium absorption (National Academy of Sciences National Research Council, 1989).
Epidemiological studies have failed to show a negative impact of high amounts of dietary protein on bone. Two studies, one on fracture rate and another on cortical bone mass, showed no adverse effects of protein on bone (Arnaud and Sanchez, 1996).
Regarding calcium losses and protein ingestion, the National Research Council states, "Urinary calcium excretion increases with increased protein intake if phosphorus intake is constant. If phosphorus intake increases with protein intake, as it does in U.S. diets, the effect of protein is minimized. It has been suggested, but not demonstrated, that a habitual high intake of protein might contribute to osteoporosis. This seems unlikely based on present evidence, at least for the range of intake for most people in the United States" (National Academy of Sciences National Research Council, 1989, p. 72).
The National Academy of Sciences National Research Council (1989, p. 178) further expounds on the relationship of phosphorus and protein intakes to calcium status: "The level of protein and phosphorus can affect the metabolism of and requirement for, calcium, primarily as a result of their opposing effects on urinary calcium brought about by changes in fractional tubular reabsorption of calcium. The effect on urinary excretion outweighs the small effects mentioned above on absorption [that show phosphorous only as phytate hinders absorption of calcium and protein enhances absorption]. An increase in protein intake reduces fractional tubular reabsorption and results in an increase in urinary calcium excretion. In contrast, an increase in phosphorus intake increases fractional reabsorption and causes urinary calcium to decrease. Because of the opposing effects of protein and phosphorus on urinary calcium and calcium retention, a simultaneous increase in the intake of both, a pattern characterized by milk, eggs, and meat ingestion, has but little effect on calcium balance at recommended levels of calcium intake."
In consideration of the resistance training enthusiast, even many protein supplements for strength-training enthusiasts are fortified with 25-100% of the RDA of phosphorus and 25-160% of the RDA for calcium. It must also be considered that resistance training itself is a strong stimulus for bone mineralization (Burr, 1997; Conroy and Earle, 1994).
In view of this mass of evidence, it is unlikely that increased protein consumption will have negative sequelae on calcium retention in individuals engaged in resistance training who consume the majority of protein as meats, eggs, dairy products, and even fortified whole-protein supplements.
The link between a high-protein diet and saturated fat consumption is not without import. However, studies on the dietary habits of recreational and competitive resistance trainees have repeatedly shown very low total fat and saturated fat consumption (Kleiner, Bazzarre and Ainsworth, 1994; Vega and Jackson, 1996). In addition, body building-type exercise has been shown to positively affect blood lipid parameters both acutely (Wallace, Moffatt, Haymes, and Green, 1991) and chronically (Eliot et al.; Goldberg, Elliot, Schutz, and Kloster, 1984; Ullrich, Reid, and Yeater, 1987). These positive effects, however, are not seen in trainees who abuse anabolic-androgenic steroids (Hurley et al.). So long as a steroid-free resistance trainee makes an effort to maintain a moderate intake of saturated fat by opting for lean meats and reduced-fat dairy products, high-protein diets are not an atherogenic health risk.
Possible negative effects of a high-protein diet on renal function were postulated by Brenner et al. (1982). This team proposed that renal glomerular sclerosis, which is commonly part of the aging process, is accelerated by excess protein intake. Brenner deemed this possible risk "acceptable" within healthy individuals. The National Research Council indicates that there is no human study supportive of excess protein leading to renal glomerular sclerosis (National Academy of Sciences National Research Council 1989). A diet with excess protein and a high-protein diet, as referred to in this report, must be distinguished. A diet with excess protein is just that: a diet with protein that must be degraded and its nitrogenous waste products excreted in the urine. A high-protein diet for the resistance trainee, on the other hand, should provide enough protein to maintain nitrogen balance and a little extra for growth. Hence, a high-protein diet in a strength-trained individual is not necessarily an excessive protein diet and would not impose any additional load on the renal system.
Based on research conducted with healthy individuals and even body builders specifically, there seems to be no basis for fear of supra-physiological protein consumption in healthy persons (Di Pasquale; Lemon, 1994). In fact, at least one animal study has shown a beneficial effect of high-protein diets on renal function (Sterck, Ritskes-Hoitinga, and Beynen, 1992). The National Research Council supports these views on safety, writing, "Habitual intakes of protein in the United States are substantially above the requirement, and although there is no firm evidence that these intake levels are harmful, it has been deemed prudent to maintain an upper bound of no more than twice the RDA for protein" [1.6 g/kg/day] (National Academy of Sciences National Research Council, 1989, pp. 72-73).
Despite the methodological problems mentioned earlier, evidence is continuing to mount that suggests resistance-trained subjects usually respond positively to protein intakes above those traditionally recommended by sources such as the RDA. So convincing are the data that in 1987, the American Dietetic Association published a position statement that revised the RDA for all types of athletes, modestly increasing the recommended intake from 0.8 g/kg/day to 1.0 g/kg/day (McCarthy). It is the opinion of most leading authorities, with few exceptions (Sargent and Hohn, 1993), that anaerobic athletes achieve the best results when protein consumption exceeds the RDA (Lemon, 1995; Lemon and Proctor; Paul, 1989; Reimers; Tarnopolsky, Atkinson, MacDougall, Chesley, et al.).
In Lemon's most recent analysis (1995) he proposes a need of about 1.4-1.8 g/kg/day for anaerobic athletes. This recommendation assumes an adequate caloric intake and a diet of mixed-quality proteins. Variability of need within this range will depend upon factors such as training experience, intensity, duration, and frequency of the anaerobic regimen, addition of an aerobic training component (common to body builders), anabolic androgenic steroid use (which enhances protein synthesis), and age (growing athletes need additional protein). Lemon suggests that two standard deviations be added to the value arrived at by linear regression to cover approximately 98% of all resistance trainees (Lemon 1997), similar to the RDA. Tarnopolsky contends that due to the small numbers of individuals in the resistance training studies, adding one standard deviation is more appropriate because there is greater variability among fewer individuals (Tarnopolsky, Atkinson, et al.).
Simple regression analysis of the studies as a whole estimates neutral nitrogen balance, not necessarily the highest retention, would occur at 1.35 g protein/kg/day (.215 g N/kg/day). After adding one to two standard deviations (12.5% per SD) (National Academy of Sciences National Research Council, 1989) to cover up to 98% of resistance-trained individuals, the figure becomes 1.52 g protein/kg/day (.243 g N/kg/day) or 1.69 g protein/kg/day (.270 g N/kg/day). A more cautious approach would be to start with the protein "requirement" for neutral nitrogen balance at 1.35 g/kg/day and add, for example, a reasonable amount for growth such as the 5.5 g protein/day mentioned earlier. Perhaps once a resistance trainee has reached full genetic potential (when further hypertrophy ceases to occur in the absence of overtraining), that trainee could gradually reduce protein intake to maintain nitrogen balance. These figures arrived at by linear regression and simple arithmetic are in agreement with at least one other review, falling within the range of 1.4-1.8 g protein/kg/day proposed by Lemon (1995).
Based on the more cautious calculations presented in this report, a 65 kg person may require about 94 g protein/day for a positive nitrogen retention (1.35 X 65 = 88; 88 + 5.5 = 94 g protein/day). However, this needs to be confirmed, and no recommendations can be made at this time due to the requirement itself being uncertain.
The immediate implications of these data for the resistance trainee are probably inconsequential. It is well-documented that the vast majority of Americans, especially anaerobic athletes, already consume protein in amounts greatly surpassing the conventional recommendations (Lemon and Proctor, 1991; Munro; Vega and Jackson). Assuming protein quality is at least average, it is unlikely that many resistance trainees will have to modify their current protein intakes. In fact, many anaerobic athletes, particularly body builders, consume an abundance of high quality protein (Vega and Jackson), which would actually decrease their protein needs.
To summarize, my research findings indicate that zero nitrogen balance would occur at a protein intake of 1.35 g/kg body weight/day. There is a strong need for additional protein requirement studies on resistance trainees under controlled conditions to determine what level of protein consumption results in the most positive nitrogen balance. An issue that must be confronted is the decreasing efficiency of protein utilization that results from prolonged periods of supraphysiological protein consumption.
Look for the next installment in this series that will explain how to cope with the fact that when you increase protein intake, you inevitably increase the wastefulness of the body.*** *** ***
Greg Bradley-Popovich holds a B.S. in Biology from Fairmont State College, an M.S. in Exercise Physiology from the School of Medicine at West Virginia University, and a second M.S. in Human Nutrition, also from WVU. He is currently a Doctor of Physical Therapy scholar at the highly acclaimed Creighton University in Omaha, Nebraska where he received the 1999 Developing Clinician Award. He is coauthor of the book Rational Strength Training, available at www.i-a-r-t.com. He is also a contributing author to the upcoming textbook Sports Supplements: A Complete Guide to Physique and Athletic Enhancement due out from Williams & Wilkins in the fall of 2000. Those interested in Greg's freelance scientific discussions on fitness and nutrition can contact him at firstname.lastname@example.org.
Reprinted from Exercise Protocol, summer 1999.*** *** ***
Allen, L. H., Oddoye, E. A., & Margen, S. (1979). Protein-induced hypercalciuria: a longer term study. American Journal of Clinical Nutrition, 32, 741-749.
Anand, C. R. & Linkswiler, H. M. (1974). Effect of protein intake on calcium balance of young men given 500 mg calcium daily. Journal of Nutrition, 104, 695-700.
Arnaud, C. D. & Sanchez, S. D. (1996). Calcium and phosphorus. In: E. E. Zigler & L. J. Filer, Jr. (Eds.), Present knowledge in nutrition, (7th ed.; pp. 245-255). Washington, D. C.: ILSI Press.
Brenner, B. M., Meyer, T. W., & Hostetter, T. H. (1982). Dietary protein intake and the progressive nature of kidney disease: The role of hemodynamically mediated glomerular injury in the pathogenesis of progressive glomerular sclerosis in aging, renal ablation, and intrinsic renal disease. The New England Journal of Medicine, 307, 652-659.
Brotherhood, J. R. (1984). Nutrition and sports performance. Sports Medicine, 1, 350-389.
Burr, D. B. (1997). Bone, exercise, and stress fractures. In: J. L. Holloszy (Ed.), Exercise and sport sciences reviews (pp. 171-194). Baltimore, MD: Williams and Wilkins.
Campbell, W. W., Crim, M. C., Young, V. R., & Evans, W. J. (1994). Increased energy requirements and body composition changes with resistance training in older adults. American Journal of Clinical Nutrition, 60, 167-175.
Campbell, W. W., Crim, M. C., Young, V. R., Joseph, L. J., & Evans, W. J. (1995). Effects of resistance training and dietary protein intake on protein metabolism in older adults. American Journal of Physiology, 268 (June), 1143E.
Catlin, D., Wright, J., Pope, H., Jr., & Liggett, M. (1993). Assessing the threat of anabolic steroids. The Physician and Sports Medicine, 21 (8), 36-41, 44.
Celejowa, I. & Homa, M. (1970). Food intake, nitrogen, and energy balance in Polish weight lifters during a training camp. Nutrition and Metabolism, 12, 259-74.
Conroy, B. P. & Earle, R. W. (1994). Bone, muscle, and connective tissue adaptations to physical activity. In: T.R. Baechle (Ed.), Essentials of strength and conditioning (pp. 51-66). Champaigne, IL: Human Kinetics.
Consolazio C. F., Johnson, H. L., Nelson, R. A., Dramise, J. G., & Skala, J. H. (1975). Protein metabolism during intensive physical training in the young adult. American Journal of Clinical Nutrition, 28, 29-35.
Di Pasquale, M. G. (1997). Amino acids and proteins for the athlete-the anabolic edge. Volume in I. Wolinsky (Series ed.), Nutrition in exercise and sport. New York, NY: CRC Press.
Durnin, J. V. (1978). Protein requirements and physical activity. In J. Parizkova & V. A. Rogozkin (Eds.) Nutrition, physical fitness and health (pp. 53-60) Baltimore: University Press.
Elliot, D. L., Goldberg, L., Kuehl, K. S., & Catlin, D. H. (1987). Chracteristics of anabolic-androgenic steroid-free competitive male and female body builders. The Physician and Sports Medicine, 15 (6), 169-179.
Fern, E. B., Bielinski, R. N., & Schutz, Y. (1991). Effects of exaggerated amino acid and protein supply in man. Experientia, 47, 168-72.
Friedl, K. E. (1994). Performance-enhancing substances: Effects, risks, and appropriate alternatives. In: T. R. Baechle (Ed.), Essentials of strength training and conditioning (pp. 188-209). Champaign, IL: Human Kinetics.
Goldenburg, L., Elliot, D. L., Schutz, R. W., & Kloster, F. E. (1984). Changes in lipid and lipoprotein levels after weight training. JAMA: The Journal of the American Medical Association, 252 (4), 504-506.
Hatfield, F. C. (1993). Hardcore bodybuilding: A scientific approach. Chicago, IL: Contemporary Books.
Hegsted, M., Schuette, S. A., Zemel, M. B., & Linkswiler, H. M. (1981). Urinary calcium and calcium balance in young men as affected by level of protein and phosphorus intake. Journal of Nutrition, 111, 553-562.
Holloway, J. B. (1994). Individual differences and their implications for resistance training. In: T. R. Baechle (Ed.), Essentials of strength training and conditioning (pp. 151-162). Champaign, IL: Human Kinetics.
Hurley, B. F., Seals, D. R., Hagberg, J. M., Goldberg, A. C., Ostrove, S. M., Holloszy, J. O., Wiest, W. G., & Goldberg, A. P. (1984). High-density lipoprotein cholesterol in body builders v powerlifters: Negative effects of androgen use. JAMA: The Journal of the American Medical Association, 252 (4), 507-513.
Kersey, R. D. (1993). Anabolic-androgenic steroid use by private health club/gym athletes. Journal of Strength and Conditioning Research, 7 (2), 118-126.
Kleiner, S. M., Bazzarre, T. L., & Ainsworth, B. E. (1994). Nutritional status of nationally ranked elite bodybuilders. International Journal of Sport Nutrition, 4, 54-69.
Kraemer, W. J. (1992 a). Hormonal mechanisms related to the expression of muscular strength and power. In: P. V. Komi (Ed.), Strength and power in sport (pp. 64-76). Cambridge, MA: Blackwell Science.
Kraemer, W. J. (1992 b). Endocrine responses and adaptations to strength training. In: P. V. Komi (Ed.), Strength and power in sport (pp. 291-304). Cambridge, MA: Blackwell Science.
Laritcheva, K. A., Yalovaya, N. I., Shubin, V. I., & Smirnov, P. V. (1978). Study of energy expenditure and protein needs of top weight lifters. In Parazkova & Rogozkin (Eds) Nutrition, physical fitness and health (pp. 144-163). Baltimore: University Press.
Lemar, H. J., Jr. (1998 a). Growth hormone use and abuse. In: M. T. McDermott (Ed.), Endocrine secrets, 2nd edition (pp. 172-179). Philadelphia, PA: Hanley and Belfus Medical Publishers.
Lemar, H. J., Jr. (1998 b). Use and abuse of anabolic-androgenic steroids. In: M. T. McDermott (Ed.), Endocrine secrets (2nd ed.; pp. 291-295). Philadelphia, PA: Hanley and Belfus Medical Publishers.
Lemon, P. W. R. (1987). Protein and exercise: update 1987. Medicine and Science in Sport and Exercise, 19 (5), S179-S190.
Lemon, P. W. R. (1994). Protein requirements of soccer. Journal of Sports Science, 12, S17-22.
Lemon, P. W. R. (1995). Do athletes need more dietary protein and amino acids? International Journal of Sport Nutrition, 5, S39-S61.
Lemon, P. W. R. (1997, September). Protein needs of athletes. Symposium conducted at the International Conference on Sport Nutrition, Williamsburg, Virginia.
Lemon, P. W .R. & Proctor, D. (1991). Protein intake and athletic performance. Sports Medicine, 12 (5), 313-325.
Lemon, P. W. R., Tarnopolsky, M. A., MacDougall, J. D., & Atkinson, S. A. (1992). Protein requirements and muscle mass/strength changes during intensive training in novice bodybuilders. Journal of Applied Physiology, 73, 767-775.
Lombardo, J. (1993). The efficacy and mechanisms of action of anabolic steroids. In C. E. Yesalis (Ed.), Anabolic steroids in sport and exercise (pp. 89-106). Champaign, IL: Human Kinetics.
MacDougall, J. D. (1986). Morphological changes in human skeletal muscle following strength training and immobilization. In N. L. Jones, N. McCartney, & A .J. McComas (Eds.), Human muscle power (pp. 269-288). Champaign, IL: Human Kinetics.
McCarthy, P. (1989). How much protein do athletes really need? The Physician and Sports Medicine, 17 (5), (170-175).
Mitchell, H. H. (1924). A method of determining the biological value of protein. Journal of Biological Chemistry, 58, 873-903.
Munro, H. N. (1964). Introduction to part II. In: H.N. Munro & J.B. Allison (Eds.), Mammalian protein metabolism: Vol. 2. (pp. 1-39). New York, NY: Academic Press.
National Academy of Sciences National Research Council. (1989). Recommended dietary allowances ( 9th ed.) Washington, D.C.: National Academy Press.
Oser, B. L. (1965). Hawke's physiological chemistry. New York, NY: McGraw-Hill.
Paul, G. (1989). Dietary protein requirements of physically active individuals. Sports Medicine, 8, 154-176.
Poortmans, J. (1985). Postexercise proteinuria in humans: facts and mechanisms. Journal of the American Medical Association, 253, 236-240.
Reeds, P. J. & Beckett, P. R. (1996). Protein and amino acids. In: E. E. Zigler & L. J. Filer, Jr. (Eds.), Present knowledge in nutrition, (7th ed.; pp. 67-86). Washington, D.C.: ILSI Press.
Reimers, K. J. (1994). Evaluating a healthy, high performance diet. Strength and Conditioning, 16 (6), 28-30.
Roy, B. D., Tarnopolsky, M. A., MacDougall, J. D., Fowles, J., & Yarasheski, K. E. (1997). Effect of glucose supplement timing on protein metabolism after resistance training. Journal of Applied Physiology, 82 (6), 1882-1888.
Sargent, R. G. and Hohn, E. (1993). Protein needs for the athlete. National Strength and Conditioning Journal, 15 (1), 54-56.
Schutte, S. A. & Linkswiler, H. M. (1982). Effects of Ca and P metabolism in humans by adding meat, meat plus milk, or purified proteins plus Ca and P to a low protein diet. Journal of Nutrition, 112, 338-349.
Sherwood, L. (1993). Human physiology: From cells to systems, 2nd ed. St. Paul: West.
Sterck, J. G., Ritskes-Hoitinga J., & Beynen, A. C. (1992). Inhibitory effect of high protein intake on nephrocalcinogenesis in female rats. British Journal of Nutrition, 67 (2), 223-233.
Tarnopolsky, M. A., Atkinson, S. A., MacDougall, J. D., Chesley, A., Phillips, S., & Schwarcz, H. P. (1992). Evaluation of protein requirements for trained strength athletes. Journal of Applied Physiology, 73, 1986-1995.
Tarnopolsky, M. A., MacDougall, J. D., Atkinson, S. A., Blimkie, C., & Sale, D. (1986). Dietary protein requirements for body builders vs. sedentary controls [Abstract]. Medicine and Science in Sports and Exercise, 18, S64.
Tesch, P. A. (1992). Training for bodybuilding. In: P. V. Komi (Ed.), Strength and power in sport (pp. 370-380). Cambridge, MA: Blackwell Science.
Ullrich, I. H., Reid, C. M., & Yeater, R. A. (1987). Increased HDL-cholesterol levels with a weight-lifting program. Southern Medical Journal, 80 (3), 328-331.
Vega, F. & Jackson, R. T. (1995). Dietary habits of body builders and other regular exercisers. Nutrition Research, 16 (1), 3-10.
Walberg, J. L., Leedy, M. K., Sturgill, D. J., Hinkle, D. E., Ritchey, S. J., & Sebolt, D. R. (1988). Macronutrient content of a hypoenergy diet affects nitrogen retention and muscle function in weightlifters. International Journal of Sports Medicine, 9, 261-266.
Wallace, M. B., Moffatt, R. J., Haymes, E. M., & Green, N. R. (1991). Acute effects of resistance exercise on parameters of protein metabolism. Medicine and Science in Sport and Exercise, 23 (2), 199-204.
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