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Journal of the American College of Nutrition, Vol. 25, No. 3, 188-194 (2006)
Published by the American College of Nutrition

Influence of Branched-Chain Amino Acid Supplementation on Urinary Protein Metabolite Concentrations after Swimming

Fu-Chun Tang, PhD

Graduate Institute of Nutritional Sciences and Education, National Taiwan Normal University, Taipei, TAIWAN, ROC

Address reprint requests to: Fu-Chun Tang, Ph.D. 9F, #32, Lane 171, Fu-Shing S. Rd. 2nd, Taipei, TAIWAN, ROC. E-mail: t10013{at}ntnu.edu.tw


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Objective: The influence of branched-chain amino acid (BCAA) supplementation on urinary urea nitrogen, hydroxyproline (HP), and 3-methylhistidine (3MH) concentrations after 25 min of breast stroke exercise (65–70% maximum heart rate reserved, 65–70% HRRmax) followed by a 600 m crawl stroke competition was investigated in a double-blind, counter-balanced study.

Methods: Male university students (19–22 years old) majoring in physical education participated in the study. Based on the previous swimming time of a 600 m crawl stroke, the participants were divided into two groups: placebo (n = 9, BMI = 24.2 ± 2.1 kg/m2; 12 g of glucose/day; in capsules) and BCAA (n = 10, BMI = 22.7 ± 1.5 kg/m2; 12 g of BCAAs/day; in capsules: leucine 54%, isoleucine 19%, valine 27%) groups. The participants maintained a regular dietary intake (except the prescribed breakfast on day 15) and exercise activity at a moderate/low intensity (60–70% HRRmax, swimming and rowing, ~1.5 hour/day) during the 15-day study. A prescribed exercise program was performed on day 15. Urinary and blood samples were collected before, during, and after the prescribed exercise for the measurements of the urinary urea nitrogen, HP, and 3MH concentrations in urine, as well as the glucose, lactate, glutamine, alanine, and BCAA concentrations in plasma.

Results: Two weeks of dietary supplementation did not induce any changes in the plasma glucose and total BCAA concentrations of either group, nor in the urinary urea nitrogen, HP, and 3MH concentrations in urine. On day 15, after 25 min of breast stroke exercise and a 600 m crawl stroke competition, plasma glucose concentration decreased significantly (p < 0.05) whereas plasma lactate concentration increased significantly (p < 0.05) in both groups. The exercise program prescribed in the study did not affect urinary urea nitrogen, HP, and 3MH concentrations. Twenty hours after the competition, however, a significant increase in the concentrations of urinary urea nitrogen, HP, and 3MH was found in the placebo group (p < 0.05), but not in the BCAA group.

Conclusions: The results obtained in this study suggest that swimming induced muscle proteolysis was prevented by BCAA supplementation. The mechanism could be attributed to the availability of ammonia provided by the oxidation of supplemented BCAAs during exercise.

Key words: branched-chain amino acids, urinary urea nitrogen, hydroxyproline, 3-methylhistidine, swimming


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 
A previous study [1] provided the evidence that, with a very-low-calorie dietary intake, the plasma branched-chain amino acid (BCAA; leucine, isoleucine, and valine) concentrations of none-obese, male college students decreased significantly after a week of daily 30 min moderate/low intensity (60–80% maximum heart rate) running, as compared with those of the same dietary treatment nonexercise controls. The BCAA concentrations in plasma actually reflect the amounts of BCAAs in muscle, which comprise about 35% of the indispensable amino acids in muscle proteins [2]. As muscle protein mass decreases, muscle strength is affected. Subsequently, exercise performance deteriorates. BCAAs have been shown to suppress muscle protein catabolism [3]. The administration of BCAAs has been proved useful in reducing both muscle proteolysis and urea nitrogen production in trauma patients with sepsis [4]. One potential benefit of BCAA supplements during exercise may be the attenuation of muscle protein degradation [5,6]. Such an effect may be of greater significance during recovery from exercise, since protein synthesis is depressed during exercise and this change leaves amino acids available for catabolic processes [7]. Studies have demonstrated that BCAAs are removed by active skeletal muscle during exercise [8] and that their oxidation increases as exercise progresses [9–11].

An earlier study [12] indicated that a high carbohydrate (CHO) diet would enhance the exercise performance of Chinese elite swimmers. Recently, however, Tang and Lee [13] found that muscle homeostasis is still affected by high-intensity exercise even if the energy (~84% CHO) provided was sufficient. Their report [13] showed significantly high concentrations in urinary hydroxyproline (HP) and 3-methylhistidine (3MH) following exhaustive running after a pre-exercise CHO feeding. Urinary HP is almost exclusively associated with collagen, the most abundant protein of mammalian tissues. During collagen degradation, the HP that is not reused is then discharged into the urine [14]. Hence, it has been used as a reliable index of collagen degradation [15] and bone resorption [16]. For the same purpose and mechanism, urinary 3MH has been used as a marker of skeletal muscle protein breakdown [17]. Young and Munro [18] indicated that 3MH is an amino acid formed by the methylation of specific histidine residues in the muscle contractile proteins. Since it is not reutilized by the body and is excreted quantitatively in the urine, 3MH excretion is assumed to be an index of contractile protein degradation. Furthermore, amino acid degradation is linked with urea formation; increases in blood, urine, or sweat urea also indicate an increase in protein degradation [19]. Thus, the measurements of urinary urea nitrogen, HP, and 3MH excretions can help to clarify the effect of exercise on protein and/or amino acid degradation.

As a result of endurance exercise, gluconeogenesis is significantly enhanced. During such a situation, skeletal muscle becomes largely responsible for providing substrates for this metabolic reaction by increasing its release of amino acids [20]. Among the amino acids released by the muscle, alanine and glutamine by far exceed the others [20]. Together, alanine and glutamine represent 60–80% of the amino acids released from skeletal muscle while they account for only 18% of the amino acids in muscle protein [21,22]. Harper et al. [22] stated that amino groups from BCAAs are being used for synthesis of alanine and glutamine in muscle metabolism. In turn, these two amino acids provide a shuttle for transfer of BCAA nitrogen from muscle to liver for urea formation [23]. Alanine and glutamine are also the major amino acid precursors for gluconeogenesis in the liver and kidney, respectively [24,25]. Thus, the measurements of plasma alanine and glutamine concentrations can help in understanding the effect of exercise on muscle homeostasis. Swimming is one type of whole body muscle exercise; and muscle, which makes up 35–40% of total body weight [22], should contribute substantially to total body BCAA utilization. The study, therefore, was designed to investigate the protective effect of BCAA supplementation from proteolysis induced by swimming exercise.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 
Participants
Nineteen healthy male university physical education students (19–22 years old) enrolled in swimming course level II (familiar with breast stroke and crawl stroke but not highly trained competitive athletes) were recruited for this double-blind, counter-balanced study. All participants (swimmers) were asked not to take any medication that would affect dependent variables. Prior to their participation, a verbal and written explanation of the procedure and potential risks were provided. In turn, the swimmers gave their written informed consent to participate in this investigation and were instructed to maintain their regular dietary intake and exercise activity of moderate/low-intensity (60–70% maximum heart rate reserved, 60–70% HRRmax; swimming and rowing, ~1.5 h/day), and to avoid vigorous exercise, alcohol and caffeine consumption as well as smoking during the entire study. Swimmers were grouped based on their previous swimming time for 600 m of a crawl stroke (score before supplementation): placebo (n = 9; body mass index, BMI = 24.2 ± 2.1 kg/m2; 12 g of glucose/day; in capsules) and BCAA (n = 10; BMI = 22.7 ± 1.5 kg/m2; 12 g of BCAAs/day; in capsules, leucine 54%, isoleucine 19%, valine 27%) groups. The composition of BCAAs was prescribed based on our previous study [26], which did not cause any side effects in our participants. The Human Experiment Review Board of National Taiwan Normal University approved this study.

Experimental Design
As shown in Fig. 1, before any treatment, urinary samples (urine 0, baseline) and 10 hour overnight fasting blood samples (blood 0, baseline) were collected at ~7:30 am of day 0. During the mealtime, placebo or BCAA supplements were given directly to each swimmer, three times (4 g/time) per day, by the same investigator for 14 days. During this time, the swimmers were also asked if they had fully complied with the instructions, and all reported full compliance. Urinary and fasting blood samples were also taken on day 7 (urine 1 and blood 1) and day 14 (urine 2 and blood 2). During the entire experimental period, swimmers were required to maintain their regular dietary intake. Three days prior to the onset of exercise and the day of competition (day 15), swimmers were instructed to avoid meat consumption in order to eliminate exogenous 3MH and creatinine contributions [17]. On day 15, after urinary and fasting blood samples (urine 3 and blood 3) were taken, the swimmers consumed a prescribed breakfast (prepared by the research team: carbohydrate 58.5%, protein 14.4%, lipid 27.1%; ~11 kcal/kg body weight, slightly less than 1/3 of their daily caloric intake to avoid gastrointestinal distress during exercise) along with the placebo or the BCAA supplements at ~7:30 am. Two and a half hours later (~10:00 am), the swimmers were required to continuously perform a 25 min breast stroke exercise at an intensity of 65–70% HRRmax, and their heart rates were recorded with heart rate monitors (Polar AccurexPlusTM, Polar Electro Oy, Kempele, Finland). Urinary and blood samples (urine 4 and blood 4) were obtained immediately after swimmers left the pool (~10:30 am) and placebo or BCAA supplements were then given again. According to the heart rate monitor record, all swimmers maintained their exercise intensity within 65–70% HRRmax during the 25 min breast stroke exercise. Following a one hour rest (~11:30 am), the 600 m crawl stroke competition (score after supplementation) was initiated. The exercise protocol was designed to investigate the effect of BCAA supplements on recovery (examined by the heart rate recorded) after exercise (breast stroke) induced fatigue. Before the competition, the swimmers were informed that the best six competitors would be rewarded. During the competition, all swimmers were also verbally encouraged by the investigators to achieve their highest level of performance. After the competition, a urinary sample (urine 5), along with the blood sample (blood 5), was taken immediately after each swimmer was out of the pool, and the third dosage of the supplements was then given. After breakfast, the swimmers were allowed to consume only water until their urinary and blood samples, on day 15, were taken. In order to measure the urinary protein metabolite concentrations after each swimming, a total of three urinary samples (urine 3–5) were separately collected from each swimmer on the day of competition. Since measurements of 24 hour urinary excretion would be very difficult and improper in this study, ‘spot checks’ were then used. Urinary creatinine concentration was determined and used to standardize all other urinary constituents [27]. On day 16, the last sample (urine 6 and blood 6, recovery) of this study was collected (~7:30 am) after a 10 hour overnight fast (Fig. 1). Between the collection of each urinary sample and blood sample, body composition was also measured (SBIA, InBody 3.0, Biospace Co., Ltd., Seoul, Korea), and this data has been published elsewhere [28].


Figure 1
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  		Fig. 1. Experimental Diagram. HRRmax, maximum heart rate reserved. No meat consumption on day 12–15. *Fasting blood sample. **Placebo group: 12 g of glucose/day. BCAA group: 12 g of BCAAs/day (BCAAs: branched-chain amino acids; leucine 54%, isoleucine 19%, valine 27%). ***Carbohydrate 58.5%, protein 14.4%, lipid 27.1%; ~11 kcal/kg body weight.

 
Assessment
All blood samples were collected by a registered nurse from a forearm antecubital vein and centrifuged (150 x g, 4°, 20 min). Plasma was immediately separated from cells and then stored at –70°C to assess the concentrations of glutamine, alanine, valine, isoleucine, and leucine (HPLC, AccQ TAG method, Waters Co., Milford, MA, USA), glucose (Beckman, ASTRA system, Brea, CA, USA), and lactate (Kodak Ektachem 500, Eastman Kodak Co., Rochester, NY, USA). Urinary samples were analyzed to measure HP and 3MH concentrations (HPLC, AccQ TAG method, Waters Co., Milford, MA, USA), creatinine and urea nitrogen concentrations (alkaline picrate and urease methods, respectively; Beckman, ASTRA system, Brea, CA, USA), and pH value (Ion analyzer M-3000, Suntex Co., Indianapolis, IN, USA). Before HPLC analysis, plasma was deproteinized with 20mMHCl, then, filtered (ultrafree-MC, UFC3LGC00, Millipore, USA) and centrifuged; urine was hydrolyzed with 6NHCl, at 110°C for 3.5 hours, in order to determine the concentrations of free HP and 3MH. All data were subjected to an analysis of variance using the generalized linear model procedure of SAS (Version 8e for Windows, SAS Institute Inc., Cary, NC, USA) and expressed as mean ± SD. Duncan’s new multiple range test was used for all comparisons of mean values at a significant level of p < 0.05; within each measurement and each group, data with different letters are significantly different (Table 1 and Fig. 2). The difference between the placebo and BCAA groups in swimming time (sec) changes of 600 m crawl stroke (score after supplementation – score before supplementation) was tested by a Student’s t-test, to investigate the effect of BCAA supplementation on exercise performance.


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  		Table 1. Plasma Metabolite Concentrations as the Functions of Branched-Chain Amino Acid Supplementation and/or Swimming*

 

Figure 2
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  		Fig. 2. Urinary metabolite concentrations as the functions of branched-chain amino acid supplementation and/or swimming. See legend for Fig. 1 and footnote for Table 1. Filled symbol, bold error bar and letters represent BCAA group. Urine 0: day 0 (baseline); Urine 1: day 7; Urine 2: day 14; Urine 3: day 15 (competitive day); Urine 4: day 15 (after breast stroke); Urine 5: day 15 (after crawl stroke); Urine 6: day 16 (recovery).

 

   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
ACKNOWLEDGMENTS
 REFERENCES
 
Body composition, including BMI, fat-free mass, and fat mass, was affected neither by the supplementation nor the exercise prescribed [28]. After the swimming competition, no significant difference was found in any of time scores (score before supplementation: placebo vs. BCAA = 942.8 ± 365.0 sec vs. 1014.1 ± 204.3 sec; score after supplementation: placebo vs. BCAA = 836.6 ± 202.5 sec vs. 884.3 ± 160.2 sec) recorded between the two groups either, although the improvement (placebo vs. BCAA = –101.3 ± 188.3 sec vs. —129.8 ± 91.2 sec) in the time score of the 600 m crawl stroke was numerically higher in the BCAA group.

Blood Analysis
Table 1 shows the concentrations of plasma glucose, lactate, and selected amino acids (glutamine, alanine, and BCAAs). Plasma glucose and lactate concentrations were not affected by the 14 days of supplements. After the breast stroke and the crawl stroke sequences (blood 3–5), the plasma glucose concentrations in the placebo group (p < 0.05) and BCAA group (p < 0.05) decreased significantly, whereas the plasma lactate concentrations in the placebo and BCAA groups increased significantly (p < 0.05). After twenty hours (blood 6), the plasma glucose and lactate concentrations of both groups returned to their respective baselines. However, there was no difference between the two groups at each corresponding interval. The plasma glutamine concentrations of both groups were slightly affected by the supplementation, but the only significant difference found between the two groups (p < 0.05) was after the 600 m crawl stroke competition (blood 5). After recovery, the plasma glutamine concentration of the placebo group was significantly higher than that of its baseline (blood 6 vs. blood 0, p < 0.05). However, this phenomenon was not observed in the BCAA group.

When comparing the plasma alanine concentration, the placebo group showed slight variation, whereas the BCAA group remained in the same range (Table 1). After recovery, the plasma alanine concentration of the placebo group decreased significantly (p < 0.05) while that of the BCAA group remained constant (blood 6 vs. blood 5). Before the onset of exercise (blood 0–3), there was no difference found in plasma BCAA concentrations between the two groups, although a dosage of 12 g of BCAAs/day was consumed by the subjects in the BCAA group for more than two weeks. However, after exercise—either breast stroke 25 min (blood 4) or crawl stroke 600 m (blood 5), the plasma BCAA concentrations of the BCAA group increased significantly (p < 0.05), whereas the plasma BCAA concentrations of the placebo group decreased significantly (p < 0.05). Therefore, the main differences between the two groups were found in the plasma BCAA concentrations after breast stroke (p < 0.05) and crawl stroke (p < 0.05). After twenty hours, this concentration returned to its baseline for each group.

Urinary Analysis
Fig. 2 shows the concentrations of urinary urea nitrogen, HP, and 3MH as well as the urinary pH value. Before exercise (urine 0–3), supplements did not affect the concentrations of these excretions except urinary HP (placebo group only) excreted on day 7 (urine 1). After exercise (urine 4–5), the urinary urea nitrogen concentration of the placebo group decreased slightly while that of the BCAA group remained constant. Meanwhile, the urinary HP and 3MH concentrations of the placebo group remained constant while those of the BCAA group decreased slightly. After recovery, however, the urinary urea nitrogen, HP, and 3MH concentrations of the placebo group increased significantly (p < 0.05) whereas those of the BCAA group remained constant (urine 6 vs. urine 5). The urinary pH value of the placebo group was not affected by the supplements at all and exercise did not affect the urinary pH value either. However, the urinary pH value of the BCAA group was affected by the supplements, regardless of exercise. Furthermore, exercise tended to increase the urinary pH value of the BCAA group. After twenty hours (urine 6), the urinary pH value returned to its baseline for each group. The significant differences between the two groups were found in the urinary urea nitrogen concentration after breast stroke (p < 0.05), and urinary pH value after breast stroke (p < 0.05) and crawl stroke (p < 0.05).


   DISCUSSION
 
The purpose of this study was to examine the effect of 15 days of BCAA supplementation on protein homeostasis after 25 min of 65–70% HRRmax breast stroke exercise followed by a 600 m crawl stroke competition. The supplements of BCAAs did not make any impact in plasma glucose and lactate concentrations, which is in line with the findings of MacLean and Graham [29] and MacLean et al. [6]. During the exercise period, plasma lactate concentration increased as plasma glucose concentration decreased; after the crawl stroke competition, the plasma glucose concentration reached the lowest level and the plasma lactate concentration reached the highest level of the entire study, regardless of the supplementation. After 14 days of supplements, the plasma glutamine and alanine concentrations of the BCAA group were consistently lower than those of the placebo group, but only the glutamine concentration of the BCAA group after the crawl stroke competition was significantly lower. Similarly, the alanine concentration in the plasma of the BCAA group after the crawl stroke competition was also lower but it did not reach a significant level. The higher glutamine concentration in the plasma of the placebo group indicated significant amounts of amino acids released by the muscle [30] as compared with the BCAA group. Furthermore, after twenty hours, the urinary urea nitrogen, HP, and 3MH concentrations in the urine of the placebo group increased significantly, but these changes were not observed in the urine of the BCAA group. BCAAs appeared to be important energy substrates for exercising muscle. Immediately after breast stroke exercise and/or the crawl stroke competition, however, the changes in the urinary metabolite concentrations were insignificant for both groups, which could be due to the fact that renal clearance is reduced during exercise [30].

As exercise intensity increased, plasma glucose concentration decreased while lactate increased. During intense exercise, the increased demand for glucose and energy enhanced gluconeogenesis, lipolysis, and proteolysis. The increased plasma lactate concentration, however, inhibited free fatty acids released from adipose tissues [31]. Hence, proteolysis was increased in order to provide the substrates for gluconeogenesis and replenish the intermediates of the tricarboxylic acid cycle. Therefore, during the crawl stroke competition, amino acids (e.g. BCAAs) released from proteolysis were utilized to meet this demand, and subsequently plasma BCAA concentrations decreased in both groups. Moreover, due to the supplements and oxidation induced by exercise, the plasma BCAA concentrations of the BCAA group immediately after breast stroke exercise and the crawl stroke competition were significantly higher than those of the placebo group. This phenomenon, however, did not occur before the onset of exercise. A possible explanation is that the supplemented BCAAs were uptaken by the tissues (mainly muscle), and then, after utilization, discharged into the urine in the form of urea. This assumption is based on the observation that the urinary urea nitrogen concentration and urinary pH value of the BCAA group were consistently higher than those of the placebo group. Further studies are required in this area.

In contrast, the HP and 3MH concentrations in the urine of the BCAA group were consistently lower than those of the placebo group, but these were not found to be significant. After recovery, however, all the metabolite concentrations (urinary urea nitrogen, HP, and 3MH) increased significantly in the urine of the placebo group, but not in the BCAA group. The significantly high proteolysis in the subjects of the placebo group might be due to ammonia being required to facilitate the energy production during intense exercise. According to the findings of MacLean et al. [6], BCAA supplementation results in significantly greater muscle ammonia production during exercise. Lowenstein [32] has suggested that the purine nucleotide cycle (PNC) might function catalytically in the conversion of amino groups from amino acids to ammonia. The primary function of the PNC is to help maintain the energy state of the cell by removing AMP and allowing the adenylate kinase reaction to move in the direction of ATP production. Hence, during the competition, the inhibited or reduced proteolysis observed in the subjects of the BCAA group might be due to the contribution of PNC.

In conclusion, although the 15 days of BCAA supplementation did not affect the body composition nor the exercise performance of the swimmers, it might prevent or reduce muscle proteolysis induced by intense exercise. The mechanism might be due to the availability of ammonia provided by supplemented (exogenous) BCAA oxidation during exercise. Without the supply of exogenous BCAAs, muscle might have to rely on endogenous BCAAs to fulfill the energy demands due to exercise. Further studies are needed in the investigation of the duration and dosage of BCAA supplementation in relation to the protein homeostasis during exercise.


   ACKNOWLEDGMENTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 ACKNOWLEDGMENTS
REFERENCES
 
This study would not have been possible without the dedication and cooperation of each volunteer. The author thanks Yi-Zhen Ko, Chih-Peng Lin, and Chien-Hui Lin, Graduate Institute of Nutritional Sciences and Education, National Taiwan Normal University, for their assistance and is indebted to the National Science Council, ROC for support of this research (NSC 90-2320-B-003-006).

Received July 2, 2004. Accepted November 18, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 ACKNOWLEDGMENTS
 REFERENCES
 

  1. Tang FC: Plasma branched-chain amino acid changes during energetic stress.Nutr Sci J21 :27 –36,1996 .
  2. Harper AE, Block KP, Cree TC: Branched-chain amino acids: nutrition and metabolic interrelationships. In: Protein Metabolism and Nutrition, 4th Int Symp, Paris. (Arnal M, Pion R and Bonin D, eds).1 :159 –181,1983 .
  3. Williams MH: Protein: the tissue builder. In: "Nutrition for Health Fitness & Sport," 6th ed. New York: McGraw-Hill, pp201 –235,2002 .
  4. Bruzzone P, Siegel JH, Chiarla C, Wiles CE 3rd, Placko R, Goodarzi S: Leucine dose response in the reduction of urea production from septic proteolysis and in the stimulation of acute-phase proteins.Surgery109 :768 –778,1991 .[Medline]
  5. Blomstrand E, Newsholme EA: Effect of branched-chain amino acid supplementation on the exercise-induced change in aromatic amino acid concentration in human muscle.Acta Physiol Scand146 :293 –298,1992 .[Medline]
  6. MacLean DA, Graham TE, Saltin B: Branched-chain amino acids augment ammonia metabolism while attenuation protein breakdown during exercise.Am J Physiol267 :E1010 –E1022,1994 .[Medline]
  7. Dohm GL, Kasperek GL, Tapscott EB, Barakat HA: Protein metabolism during endurance exercise.Fed Proc44 :348 –352,1985 .[Medline]
  8. Ahlborg G, Felig P, Hagenfeldt L, Hendler R, Wahren J: Substrate turnover during prolonged exercise in man.J Clin Invest53 :1080 –1090,1974 .[Medline]
  9. Dohm GL: Protein as a fuel for endurance exercise.Exerc Sport Sci Rev14 :143 –173,1986 .[Medline]
  10. Hagg SA, Morse EL, Adibi SA: Effect of exercise on rates of oxidation turnover, and plasma clearance of leucine in human subjects.Am J Physiol242 :E407 –E410,1982 .[Medline]
  11. Wolfe RR, Goodenough RD, Wolfe MH, Roy GT, Nadel ER: Isotopic analysis of leucine and urea metabolism in exercising humans.J Appl Physiol52 :458 –466,1982 .[Abstract/Free Full Text]
  12. Tang FC: Effect of glycogen supercompensation on the endurance of Chinese elite athletes. 6th Asian Congress Nutr Proc pp.439 –447,1991 .
  13. Tang FC, Lee CW: Glycemic and insulinemic responses and muscle homeostasis following high-intensity running after pre-exercise carbohydrate feeding.Nutr Sci J27 :67 –76,2002 .
  14. Bornstein P: The biosynthesis of collagen.Annu Rev Biochem43 :567 –603,1974 .
  15. Prockop DJ, Kivirikko KI: Relationship of hydroxyproline excretion in the urine to collagen metabolism, biochemistry and clinical application.Ann Int Med66 :1234 –1267,1967 .
  16. Garrel DR, Delmas PD, Welsh C, Arnaud MJ, Hamilton SE, Pugeat MM: Effects of moderate physical training on prednisone-induced protein wasting: a study of whole-body and bone protein metabolism.Meta Clin Experi37 :257 –262,1988 .
  17. Munro HN, Young VR: Urinary excretion of 3-methylhistidine: a tool to study metabolic responses in relation to nutrient and hormonal status in health and disease of man.Am J Clin Nutr31 :1608 –1614,1978 .[Abstract/Free Full Text]
  18. Young VR, Munro HN: 3-methylhistidine and muscle protein turnover: a review.Fed Proc37 :2291 –2300,1978 .[Medline]
  19. Haralambie G, Berg A: Serum urea and amino nitrogen changes with exercise duration.Eur J Appl Physiol36 :39 –48,1976 .
  20. Pozefsky T, Tancredi RG, Moxley RT, Dupre J, Tobin JD: Effects of brief starvation on muscle amino acid metabolism in nonobese man.J Clin Invest57 :444 –449,1976 .[Medline]
  21. Ruderman NM: Muscle amino acid metabolism and gluconeogenesis.Ann Rev Med26 :245 –258,1975 .
  22. Harper AE, Miller RH, Block KP: Branched-chain amino acid metabolism.Ann Rev Nutr4 :409 –454,1984 .[Medline]
  23. Mallette LE, Exton JH, Park CR: Control of gluconeogenesis from amino acids in the perfused rat liver.J Biol Chem244 :5713 –5723,1969 .[Abstract/Free Full Text]
  24. Felig P, Pozefsky T, Marliss E, Cahill GF Jr: Alanine: key role in gluconeogenesis.Sci167 :1003 –1004,1970 .[Abstract/Free Full Text]
  25. Goodman AD, Fuisy RE, Cahill GF Jr: Renal gluconeogenesis in acidosis, alkalosis, and potassium deficiency: its possible role in regulation of renal ammonia production.J Clin Invest45 :612 –619,1966 .[Medline]
  26. Tang FC, Lee CW, Hsieh SY: Physiological and performance effects of adding branched-chain amino acids to a high carbohydrate formula diet during exercise.Nutr Sci J22 :361 –371,1997 .
  27. Owen JA, Iggo B, Scandrett FJ, Steward CP: The determination of creatinine in plasma or serum and in urine, a critical examination.Biochem J58 :426 –437,1954 .[Medline]
  28. Tang FC: Effect of branched-chain amino acid supplements on body composition measured with SBIA: an advanced BIA.Nutr Sci J28 :65 –73,2003 .
  29. MacLean DA, Graham TE: Branched-chain amino acid supplementation augments plasma ammonia responses during exercise in humans.J Appl Physiol74 :2711 –2717,1993 .[Abstract/Free Full Text]
  30. Paul GL, Gautsh TA, Layman DK: Amino acid and protein metabolism during exercise and recovery. In Wolinsky I (ed): "Nutrition in Exercise and Sport," 3rd ed. New York: CRC Press, pp125 –158,1998 .
  31. Williams MH: Fat: an important energy source during exercise. In: "Nutrition for Health Fitness & Sport," 6th ed. New York: McGraw-Hill, pp156 –200,2002 .
  32. Lowenstein JM: Ammonia production in muscle and other tissues: The purine nucleotide cycle.Physiol Rev52 :382 –414,1972 .[Medline]




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