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Departments of
* Nutritional Sciences and
Kinesiology, and
** School of Allied Health, University of Connecticut, Storrs, CT 06269
3To whom correspondence should be addressed. E-mail: nancy.rodriguez{at}uconn.edu.
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ABSTRACT |
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 TOP ABSTRACT SUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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0.001], and NOLD tended to increase [128 ± 18 to 151 ± 19 µmol/(kg · h), P = 0.09] in response to training. These data indicate improved protein utilization in response to exercise training in weight-stable subjects. This study emphasizes the importance of dietary control, with specific regard to energy and protein intakes, in the characterization of protein utilization in response to an exercise intervention.
KEY WORDS: • protein turnover • body composition • nitrogen balance
Whole-body protein utilization is affected by energy intake (1), level of protein intake (2,3), and acute endurance exercise (4,5). The role of energy intake in influencing protein utilization has been recognized for half a century (6). Early nitrogen balance studies by Todd et al. (1) and Butterfield (7) showed that nitrogen retention was improved during periods of energy balance compared with periods of energy deficit (1,8). Achievement of energy balance reduces the reliance on amino acids for energy, thus permitting the body to utilize protein for nonenergy-yielding functions (8).
The level of dietary protein consumption influences whole-body protein utilization. With increasing dietary protein, there is an increase in nitrogen retention (9–12), an increase in the oxidation of leucine (2), and changes in the rates of protein turnover (10,11). Although the implications of the observed changes in rates of protein turnover in response to protein intake are not fully understood, it is clear that increases in dietary protein influence rates of protein turnover (2,11).
Whole-body protein turnover (WBPTO)4 is also affected by an acute bout of endurance exercise. Several studies found that whole-body protein breakdown increased during exercise (13–15), with rates postexercise either decreasing (16) or not differing from those at rest (17). Whole-body protein synthesis decreased (15,17) or did not change during exercise (13,14), but increased in the period after exercise (17,18). Leucine oxidation increases during exercise in an intensity-dependent manner and may contribute 2–3% of total energy expended during an exercise session (2–4).
Although there is not yet a consensus concerning the influence of an acute exercise bout on protein utilization, even less is known about the influence of chronic aerobic training on protein utilization. Because exercise generally lasts a relatively short period of time relative to time spent not exercising, studying protein turnover at rest may be of greater value to our understanding of the influence that chronic aerobic training has on WBPTO.
The purpose of this study was to build on the earlier work of Todd et al. (1) and Butterfield and Calloway (19), who found that exercise training improved nitrogen retention, even at marginal protein intakes, as long as energy balance was maintained. Therefore, we examined the effect of a 4-wk aerobic exercise training program on resting leucine kinetics in healthy, previously untrained men and women, consuming sufficient energy for weight maintenance throughout the training period and a protein intake of 0.88 g protein/(kg · d). The current investigation placed special emphasis on controlling factors identified by Butterfield (7) as being essential for meaningful interpretation of data regarding protein utilization and exercise (7). These factors include the maintenance of energy balance, control of protein intake, and measurements taken after the initial adaptation period to a new exercise program.
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SUBJECTS AND METHODS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Subjects. After project approval by the Institution Review Board at the University of Connecticut, 7 untrained healthy adults, aged 18–25 y, were recruited from the University community. Before selection for the study, participants were asked to provide a complete medical history, physical activity log, and a 3-d food record. Exclusion criteria were: 1) exercising > 90 min/wk; 2) reporting any metabolic (i.e., diabetes) or cardiovascular abnormalities (i.e., irregular heartbeat, high blood pressure), and gastrointestinal disorders (i.e., lactose intolerance, egg protein allergies); and 3) use of any nutritional/sports supplements or anabolic steroids; 4) men with VO2max > 45 mL/(kg · min) and women with VO2max > 40 mL/(kg · min). Women were eumenorrheic and nonpregnant as determined by self-report. Informed, written consent was obtained from subjects.
Dietary intervention.
Measured resting energy expenditure (REE) and data from dietary and physical activity records were used to establish energy requirements for maintenance of body weight throughout the study period. Once energy requirements were established, protein intakes were set at 0.8 g/(kg body weight · d). Using exchange lists, diets were designed so that the macronutrient percentages of the prescribed diets were 
60% carbohydrate, 10% protein, and 30% fat. Meals were provided for study participants for the duration of the 6-wk study. This included 2 wk for subject adaptation to the diet intervention before the baseline measures and the 4 wk of exercise training. All meals were prepared and provided by University of Connecticut catering services in a designated room on campus. Graduate research assistants were present at meals to weigh and serve the appropriate portions of food to each subject and recorded intakes. Diet records were analyzed using Nutritionist Pro SoftwareTM (First Data Bank, Version 1.1).
Anthropometric measurements. Body mass and height was measured using a balance beam scale equipped with a measuring rod (Health-o-meter). Body weight was assessed at baseline and twice weekly throughout the study to ensure body weight maintenance.
Body composition. The bone densitometer, DPX-MD (LUNAR) was used to measure whole-body bone mineral density, yielding the complete analysis of body composition. Dual X-ray absorptiometry measurements were made at baseline and after 4 wk of exercise training.
VO2max testing. Maximal graded exercise cardiopulmonary testing was conducted before the start of the study (baseline) and after the 4-wk endurance training program. VO2max was determined via breath by breath analysis of expired gases during testing using an open circuit respiratory apparatus (MedGraphics CPX/D, Medical Graphics) on a treadmill (Quinton MedTrack ST55) containing a ventilation flow meter, oxygen analyzer, and carbon dioxide analyzer (20).
Exercise training. Beginning at wk 3, subjects attended group workout sessions consisting of stretching and aerobic training. Graduate research assistants supervised all exercise sessions. The progressive exercise training program consisted of running, or walking and running, 4–5 d/wk, 35 to 45 min/session, so that subjects were exercising at an intensity between 65 and 85% of their maximal heart rate for the duration of the exercise session. After wk 3 and 4, which consisted of 4 sessions of 35 min each, the subjects progressed to 4 sessions of 40 min at wk 5 and were running 5 d/wk for 45 min sessions at wk 6. Progressive increases were made weekly in volume and speed of running to achieve increases in fitness. Heart rate monitors (Polar Electronics) were used during training sessions to determine mean time spent in target heart rate zone and mean heart rate. Mean energy expended for each exercise session was estimated using metabolic equivalents, measured REE values, and time spent exercising (21). The time to complete a 4.8-km course before and after the 4 wk of training served as a measure of fitness gains.
Determination of WBPTO for pre-training and post-training.
Subjects reported to the Metabolic Assessment Laboratory in the Department of Nutritional Sciences at 0700 h after an overnight fast (
10 h after last meal) and 40 h after the last exercise session, to minimize the influence of the last meal and last exercise session on WBPTO variables. A 20-gauge Teflon catheter (7.78 cm, Jelco, Critikon) was inserted into an antecubital vein for isotope infusion. Another catheter (3.97 cm) was placed in the contralateral hand, and the hand heated with a heating pad, for the sampling of "arterialized" blood (22). Women were tested in mid-follicular phase of their menstrual cycle.
After providing baseline blood and breath samples, a primed continuous infusion of L-[1-13C] leucine [4 µmol/kg; 4.8 µmol/(kg · h); Cambridge Isotope] was initiated (Razel Syringe Pump, Razel Scientific Instruments) and continued for 180 min. At 120 min, blood and breath measurements were collected at 15-min intervals for 1 h. Plasma samples were stored at –80°C for subsequent analyses. For 13CO2 breath enrichments, subjects breathed into a Douglas bag for 2 min at specified time intervals. Breath samples were then transferred to 20-mL Venoject containers for isotope ratio analysis. Plasma 13C-KIC and 13CO2 enrichments were determined by GC and infrared MS (IR-MS), respectively, by a commercial laboratory (Metabolic Solutions).
Blood 13C-KIC and breath 13CO2 data were reviewed at 4 time points (135, 150, 165, and 180 min) to confirm steady-state conditions. Leucine Ra, Ox, and NOLD were then calculated using the reciprocal pool model (23).
Apparent nitrogen balance. Subjects were instructed to collect a 24-h urine sample before arrival at the metabolic laboratory for each WBPTO study. Total nitrogen content of the urine was determined using a micro-Kjeldahl apparatus (Tecator Kjeltec System). Urinary nitrogen, nitrogen intake from the urine collection day, and estimates of other nitrogen losses (fecal, integumental, miscellaneous) were used to calculate apparent nitrogen balance (9,24).
REE and substrate oxidation. REE and substrate oxidation were estimated on the mornings before the infusion protocols by open-circuit indirect calorimetry using a metabolic cart (MedGraphics CPX/D, Medical Graphics). These analyses were performed at baseline (before initiating dietary interventions) and after the 4-wk training program. REE was assessed for 20 min with the subject lying in a quiet, temperature-regulated room. Values determined for 24-h urinary nitrogen measures, which coincided with the day of indirect calorimetry, were entered, and substrate oxidation was estimated using software supplied by the metabolic cart manufacturer.
Statistical analysis.
Primary outcome measures were WBPTO (Ra, Ox, NOLD) at baseline (pre-training) and after training at wk 6 (post-training). Ra, Ox, NOLD data at 4 time points were averaged for each subject and group means calculated. Means were compared using repeated-measures ANOVA with group differences determined using Tukey’s post hoc analysis with an 
level of 0.05. Simple correlations between changes in fitness (i.e., change in time to complete 4.83 km run and VO2max) and changes in protein turnover (i.e., Leucine Ra, NOLD, Ox, nitrogen balance, and protein oxidation) were calculated using SPSS® 11.0 Statistical Software. Because no gender differences were noted, data for men and women were combined and are presented as one group. Values in the text are means ± SEM.
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RESULTS |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Exercise training.
Subjects consistently exercised in the upper range of the target heart rate (82% of maximum heart rate) and closely followed the exercise prescription, increasing time spent exercising to 40 min per session, 5 d/wk during wk 6. Exercise time for the 4-wk program was 38.0 ± 2.2 min, and estimated energy expenditure was 1518 ± 37 kJ/session.
WBPTO for pre-training and post-training. Steady-state isotopic enrichments of plasma 13C-KIC and breath 13CO2 were achieved for pre-training (wk 2) and post-training (wk 6) infusion protocols. 13C-leucine infusion rates were 4.83 ± 0.11 and 4.82 ± 0.01 µmol/(kg · h) for pre-training and post-training protocols, respectively.
Leucine Ra, Ox, and NOLD. Leucine Ra did not differ as a result of training [146.3 ± 18.4 vs. 165.0 ± 20.2 µmol/(kg · h), P = 0.14] (Fig. 1). NOLD values tended to increase from pre-training to post-training [128.2 ± 18.0 vs. 150.8 ± 19.2 µmol/(kg · h), P = 0.09]. Leucine Ox decreased [18.1 ± 1.5 vs. 14.9 ± 1.5 µmol/(kg · h), P < 0.01] after the 4-wk training period. There was a strong correlation between increases in REE and both Ra (r = 0.77, P < 0.001) and NOLD (r = 0.76, P < 0.001).
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Substrate oxidation. Protein oxidation was greater (P = 0.02) pre-training (14.5%) than post-training (10.7%) (Fig. 2). The oxidation of lipid and carbohydrate did not differ after the training program.
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DISCUSSION |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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11% of total intake), which falls in the range of the current Dietary Reference Intakes recommending that protein comprise 10–35% of energy intake (25). Major findings from this study were a reduction in leucine Ox (oxidation) at rest, no change in leucine Ra (proteolysis), and a tendency for NOLD (an indicator of protein synthesis) to increase. These kinetic data were accompanied by a greater retention of nitrogen and an increased REE after the 4-wk aerobic exercise training program. Previous studies are limited regarding the influence of aerobic training on resting leucine kinetics. Unlike the present study, investigations by Lamont et al. (4), McKenzie et al. (5) and Short et al. (26) found no effect of training on resting leucine oxidation. The Lamont study (4) initially observed trained individuals to have higher rates of resting leucine Ox; however, once data were corrected for fat-free mass, these differences disappeared. It is important to point out that the Lamont study was a cross-sectional design that compared 2 distinct groups, i.e., a trained and untrained group. Findings from the present study are strengthened by the study design used in which weight-stable subjects served as their own controls, before and after the 4-wk aerobic exercise training program.
Studies by McKenzie et al. (5) and Short et al. (26) are more similar in design to the current study, in that leucine kinetics was measured in the same individuals before and after 38 d and 4 mo of aerobic training, respectively. Discrepancies in leucine Ox from these studies and the present may be due to variations in protein intake. In the McKenzie et al. study (5), dietary intake reflected subjects’ habitual intakes, resulting in dietary protein consumption that exceeded that of the present study [1.2–1.7 vs. 0.88 g/(kg · d)] (5). Similarly, subjects in the Short et al. study (26) consumed a greater percentage of energy from protein than in the present study (15 vs. 11%). The increased availability of leucine, subsequent to the higher protein intakes in these 2 studies, may have masked an attenuation of leucine Ox in response to exercise training, given that leucine Ox can be influenced by leucine availability (2,27).
Although leucine Ra and NOLD did not increase significantly, both of these were correlated with the observed increase in REE. Indeed, previous research supports a strong relation between protein turnover and resting metabolic rate (28). Failure to detect significant difference may simply have been a reflection of insufficient power to detect changes. Power calculations indicate that 10 and 15 subjects would have been required to detect significant differences in NOLD and Ra, respectively. Although this increase in protein turnover was not significant, it may have ultimately driven the physiologic changes that resulted from training (i.e., increased REE, improved nitrogen balance, decreased protein oxidation and leucine Ox).
In the current study, protein oxidation was reduced after a 4-wk aerobic exercise training program. A shift toward a greater reliance on fat vs. carbohydrate for fuel is a widely accepted adaptation to endurance training (5,29). However, there is limited documentation of metabolic adaptations to aerobic training specific to the utilization of protein for fuel. Despite protein’s minimal contribution as an energy source, it is important to fully understand the effect of aerobic exercise training on WBPTO, given that nutritional supplementation can clearly regulate protein-related metabolic responses to exercise (30,31). Observations regarding protein oxidation in the present study are consistent with the noted decrease in leucine oxidation, and suggest that conservation of the essential amino acid leucine may be a possible adaptation to endurance exercise training. Such an adaptive response is reasonable, given the central role of this BCAA in muscle protein metabolism, especially during high-intensity exercise. Indeed, McKenzie et al. (5) found that aerobic training decreased the exercise-induced activation of the branched chain keto-acid dehydrogenase (BCKAD) enzyme in muscle despite training, resulting in an overall increased BCKAD capacity.
Increases in VO2max with exercise training have been associated with increases in mitochondrial density and oxidative enzyme activity (5,32,33). Although enzyme activity was not measured in this study, observed improvements in VO2max suggest that there was an increased oxidative capacity after training. Perhaps the synthesis of mitochondrial proteins offers a plausible explanation concerning why we observed aerobic exercise training to enhance nitrogen retention and conservation of leucine, despite no change in lean body mass.
The improvement in nitrogen retention, decreased reliance on protein as a fuel source, and maintenance of lean body mass suggest that a protein intake of 0.88 g/kg was sufficient for our exercising study population. This amount of protein consumed is similar to the amount deemed adequate in a study by Meredith et al. (10), who found that 0.94 g/(kg · d) was required to achieve nitrogen balance in exercising, weight-maintaining subjects.
Maintenance of energy balance is likely an important factor in sustaining nitrogen balance when daily protein intake is 0.9 g/kg, given the relation between energy and protein utilization. Exercise training influences this relation by requiring additional energy to meet the demands of increased expenditure. Although slight increases in energy intakes in response to exercise training were adequate for subjects to maintain body weight throughout the training intervention, it is important to note that the current study was limited by the fact that total daily energy expenditure was not measured precisely. Nevertheless, we contend that the adjustment in energy intake at the onset of training for the purpose of weight maintenance was likely critical to the observed exercise-induced improvements in protein utilization. This important relation among exercise training, energy balance, and protein utilization is supported by the earlier work of Todd et al. (1) and Butterfield and Calloway (19), who found that exercise improved nitrogen retention, even at marginal protein intakes, as long as energy balance was maintained.
Although inactivity results in the loss of lean body mass, the scientific literature is limited on the extent to which physical activity can improve protein utilization in healthy adults (8). The current investigation sheds light on this question in demonstrating that a 4-wk endurance exercise program resulted in improved protein utilization and nitrogen retention, in subjects consuming a weight maintaining diet containing 0.88 g protein/(kg · d). Leucine oxidation decreased in response to training, suggesting a possible conservation of this essential amino acid at rest. Additionally, this study provides further support for a relation between protein turnover and resting metabolic rate because we found strong correlations with the exercise-induced increases in these measurements. Future investigations designed to manipulate energy and protein intakes are warranted to further characterize the relations among energy balance, level of protein intake, and protein utilization in response to aerobic exercise training.
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FOOTNOTES |
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2 This study was supported by the American Egg Board.
4 Abbreviations used: BCKAD; branched-chain keto-acid dehydrogenase; NOLD, nonoxidative leucine disposal; Ox, oxidation; Ra, leucine rate of appearance; REE, resting energy expenditure; VO2max, maximal oxygen uptake; WBPTO, whole-body protein turnover.
Manuscript received 4 November 2004. Initial review completed 26 November 2004. Revision accepted 2 March 2005.
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LITERATURE CITED |
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TOPABSTRACTSUBJECTS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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