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Original Research Communications |
1 From the Nutrition, Metabolism, and Exercise Laboratory, Donald W Reynolds Department of Geriatrics, University of Arkansas for Medical Sciences, Little Rock; the Geriatric Research, Education, and Clinical Center, Central Arkansas Veterans Healthcare System, Little Rock; the Noll Physiological Research Center and the Department of Nutrition, The Pennsylvania State University, University Park; and the Department of Kinesiology, McMaster University, Hamilton, Canada.
2 Supported by NIH RO1 AG11811, NIH R29 AG13409, NIH M01-RR10732, and an independent monetary gift from Nutrition 21, San Diego. The Keiser Sports Health Equipment Company, Fresno, CA, kindly donated the resistance-training equipment used in this study.
3 Address reprint requests to WW Campbell, Towbin Healthcare Center, NMEL/NLR, Room 3J106, 2200 Fort Roots Drive, North Little Rock, AR 72114. E-mail: campbellwaynew{at}exchange.uams.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Objective: The objective of this study was to assess whether the consumption of an omnivorous (meat-containing) diet would influence RT-induced changes in whole-body composition and skeletal muscle size in older men compared with a lactoovovegetarian (LOV) (meat-free) diet.
Design: Nineteen men aged 51–69 y participated in the study. During a 12-wk period of RT, 9 men consumed their habitual omnivorous diets, which provided 
50% of total dietary protein from meat sources (beef, poultry, pork, and fish) (mixed-diet group). Another 10 men were counseled to self-select an LOV diet (LOV-diet group).
Results: Maximal strength of the upper- and lower-body muscle groups that were exercised during RT increased by 10–38% (P < 0.001), independent of diet. The RT-induced changes in whole-body composition and skeletal muscle size differed significantly between the mixed- and LOV-diet groups (time-by-group interactions, P < 0.05). With RT, whole-body density, fat-free mass, and whole-body muscle mass increased in the mixed diet group but decreased in the LOV- diet group. Type II muscle fiber area of the vastus lateralis muscle increased with RT for all men combined (P < 0.01), and the increase tended to be greater in the mixed-diet group (16.2 ± 4.4 %) than in the LOV diet group (7.3 ± 5.1%). Type I fiber area was unchanged with RT in both diet groups.
Conclusion: Consumption of a meat-containing diet contributed to greater gains in fat-free mass and skeletal muscle mass with RT in older men than did an LOV diet.
Key Words: Elderly men • lactoovovegetarian diet • resistance training • strength training • lean body mass • fat-free mass • body fat • muscle fiber area • muscle creatine • obesity
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Research has established that resistance (strength) training (RT) is an effective way to increase the muscle strength and mass of older people (5–7). Limited data also suggest that what an older person eats during a period of RT may influence how much muscle mass is gained. For example, older men who consumed a nutritional supplement drink containing 2343 kJ (560 kcal) energy (17% of energy from protein, 43% from carbohydrate, and 40% from fat) daily during a 12-wk RT program gained more muscle mass than did age-matched men who did not consume the nutritional supplement drink (8). Campbell et al (9) showed that dietary protein intake influences the relative uptake and efficiency of use of nitrogen in older people during RT. However, contrary to the results of previous studies from the same research group (5, 6), muscle hypertrophy did not occur with 12 wk of RT in these older people (7, 9). Questioned was whether differences in the muscle hypertrophic responses among these studies related to the older subjects consuming controlled lactoovovegetarian (LOV) (meat-free) diets (7, 9) rather than self-selected habitual diets that presumably included meat (ie, omnivorous diets) (5, 6). If true, this would establish that nutrition and exercise interact to maintain and enhance skeletal muscle mass in older people and, more specifically, that dietary meat consumption by older people may promote skeletal muscle hypertrophy during RT.
The purpose of the present study was to examine the effect of consuming either an omnivorous or an LOV diet during a 12-wk period of RT on whole-body composition and skeletal muscle size in older men. No published studies that we know of have examined the relationship between meat consumption and RT. We hypothesized that men who consumed an omnivorous diet would exhibit greater RT-induced gains in indexes of whole-body FFM and skeletal muscle mass than would men who consumed a LOV diet. The rationale for this hypothesis was established from previous research that showed that muscle hypertrophy occurred with RT in older people who consumed their habitual, uncontrolled (presumably meat-containing) diets (5, 6) but not in older people who consumed LOV diets (7, 9).
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SUBJECTS AND METHODS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Experimental design
The 13-wk study consisted of a 1-wk sedentary period (baseline), followed by a 12-wk period of RT. Tests and evaluations were done at baseline and weeks 6 and 12 of RT, as shown in Table 1
and described below. The first 9 men recruited into the study consumed their habitual unrestricted diets during most of the study (mixed-diet group). The second set of men recruited into the study (n = 11) underwent the same RT program and were counseled to self-select a LOV diet starting at week 1 of RT (LOV-diet group). All the men in the mixed-diet group completed the study protocol before the men in the LOV-diet group started the protocol. This study design was chosen to enable the LOV-diet group to attend counseling sessions with the research dietitian and to reduce the possibility that men in the mixed-diet group would alter their habitual dietary patterns as a result of interactions with men in the LOV-diet group. All RT, body-composition analyses, and muscle biopsy histochemical tests were conducted in an identical manner by the same investigators and research technicians in both the mixed- and LOV-diet groups. Data from one man in the LOV-diet group were excluded from the analyses because of considerable body weight loss during the study, which was inconsistent with the objectives of the study.
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For 5 d during baseline and at weeks 6 and 12 of RT, all men from both groups consumed a diet consisting of LOV foods prepared and provided by the metabolic kitchen staff at the Noll Physiological Research Center on the basis of a 2-d rotating menu. Diets for both the groups contained 15% of energy from protein, 30% from fat, and 55% from carbohydrate (11). Total energy intake was provided according to each man's total energy needs, estimated to be 1.5 times resting energy expenditure as predicted from the Harris-Benedict equation (12). The men were asked to consume all the foods and beverages provided and not to consume any other foods or beverages (other than water) during these times. The men in both groups were instructed not to purposely attempt to gain or lose body weight during the entire study period.
Three-day food records were completed by all men at weeks 1 and 11 of RT and were used to estimate total energy and macronutrient intakes. Additional 3-d food records were completed the week before the study by the men in the LOV-diet group to obtain an indication of the habitual diets of these men before they began the study and to compare the habitual diets of the LOV-diet group with those of the mixed-diet group. Total energy and macronutrient intakes were calculated by using NUTRITIONIST IV software (version 4.0; N-Squared Computing, First Data Bank, San Bruno, CA).
Resistance training protocol
During weeks 1–12 of RT, all men participated in 23 resistance exercise sessions (1 man in the mixed-diet group participated in only 22 sessions). Each man trained twice weekly on nonconsecutive days, performing 3 sets of repetitions at 80% of the maximum load to lift through the full range of motion of a joint one time only [1 repetition maximum (1RM)]. Each repetition was done in a slow, uniform motion, and a rest period of 1 min was allowed between each set. For the first 2 sets, each man completed 8 repetitions per set; for the third set, each man was instructed to perform as many repetitions as possible until muscular fatigue (ie, when he could not voluntarily complete a repetition by using proper techniques), up to a maximum of 12 repetitions. Each man's 1RM was evaluated during the first 2 RT sessions at week 1 of RT and again at weeks 6 and 12 of RT. Adjustments were made accordingly to maintain a constant training intensity of 80% of 1RM throughout the 12-wk training period. Five exercises were used to train the major muscle groups of both the upper and lower body: unilateral knee extension, unilateral seated leg curl, double leg press, seated arm pull, and seated chest press. Exercise sessions were preceded and followed by warm-up and cool-down periods consisting of 10 min of stationary cycling at low resistance and slow speed (heart rate <100 beats per minute) as well as 10 min of stretching of the muscle groups involved in the resistance exercises. All men were supervised and instructed on proper techniques and proper form. All RT was performed on Keiser pneumatic strength-training equipment (Keiser Sports Health Equipment, Fresno, CA).
Body-composition and metabolic measurements
Nude body weight was measured for each man to the nearest 0.1 kg (model 2181; Toledo Scale, Toledo, OH) at each visit to the laboratory and was calibrated by standard dead-weight testing. Height in men without shoes was assessed to the nearest 0.1 cm with a wall-mounted stadiometer during baseline. BMI was calculated as weight divided by height squared (kg/m2). Midarm circumference was taken at the midpoint of the acromion process and the olecranon process. Thigh circumference was measured at the midpoint of the inguinal crease and the distal patellar edge. All measurements were taken on the right side of the body while the man relaxed and after a normal exhalation. Intrainvestigator CVs of 1.4% and 0.6% for midarm and midthigh measurements, respectively, were achieved.
Whole-body density was measured by using hydrostatic weighing (13) and in-water residual lung volume was measured by using the nitrogen dilution technique (14). Whole-body FFM and percentage body fat were estimated from body density by using the 2-compartment model equation of Siri (15). CVs of 1.6% and 1.9% in the estimation of FFM and body fat, respectively, were achieved with repeated measurements of body density by hydrostatic weighing.
Three consecutive 24-h urine samples were collected at baseline and weeks 6 and 12 of RT and were analyzed for creatinine concentration. For 2 d before and during these urine collection periods, all subjects consumed LOV diets provided by the metabolic kitchen staff at the Noll Physiological Research Center laboratory. This dietary control was done to standardize the diets of all subjects during these measurement periods and to exclude exogenous sources of creatine found in meat and meat products that might have influenced total urinary creatinine excretion (16). Urinary creatinine was measured by using the colorimetric Jaffè reaction on a Technicon Autoanalyzer II (Technicon Instrument Corporation, Tarrytown, NY). Muscle mass was estimated by using 18.5 kg muscle tissue/g urinary creatinine (16). Automated procedures using the Jaffè reaction have a precision of 1–2% in determining creatinine concentration in urine (17).
At baseline and week 12 of RT, a biopsy of the vastus lateralis muscle was performed on the dominant leg of each man by using the needle biopsy technique (18). One subject in the LOV-diet group refused to have an end-of-study muscle biopsy performed. Immediately after a muscle sample was obtained, a homogeneous section of the muscle sample, with the fibers positioned longitudinally, was placed into a gelatin capsule that had been cut in half lengthwise and partially filled with optimum-cutting-temperature embedding compound (OCT; Sakura Finetek, Torrence, CA). The encased muscle sample was covered with more OCT and quickly dipped into and frozen in liquid isopentane (2-methylbutane; Fisher Scientific, Pittsburgh) contained in a stainless steel cup that had been precooled to the temperature of liquid nitrogen. The encased muscle sample was then placed directly into liquid nitrogen and transported to a freezer (-70°C) for storage. The OCT-mounted muscle samples were sliced into 10-µm thick sections with a Cryocut 1800 (Leica Instruments, Nubloch, Germany). Sectioning was performed at -20°C. The NIH IMAGE PROGRAM (version 1.60a, as modified by Scion Corporation, Frederick, MD) was used to measure the area of NADH tetrazolium–stained muscle fibers and to view ATPase–stained muscle fibers for fiber typing. Fibers were traced on the computer screen and measured for area. A CV of 2.4% was established by the person who performed all the imaging analyses by repeatedly measuring the mean fiber area of a given muscle sample.
A second sample of the vastus lateralis muscle was quickly frozen directly into liquid nitrogen and transferred to a -70°C freezer for storage. The creatine and phosphocreatine concentrations of freeze-dried muscle samples were determined by standard methods (19, 20) with a fluorometer (REM-150; Shimadzu, Mandel Scientific Co, Ltd, Kyoto, Japan). The intraassay CVs for creatine and phosphocreatine were 6.4% and 5.5%, respectively. Total muscle creatine concentration was calculated as the sum of the creatine and phosphocreatine concentrations.
Statistical methods
Values are reported as means ± SEMs. For all variables, a comparison of group mean values was performed on baseline data by using the nonpaired t test. Two-way repeated-measures analysis of variance was used to determine the main effects of time (representative of the effect of RT) and group (representative of the effect of diet) and the time-by-group interaction on the dependent variables. The statistical package PROC GLM (version 6.11; SAS Institute Inc, Cary, NC) was used to perform all calculations. Data processing was performed by using MICROSOFT EXCEL 5.0 (Microsoft Corporation, Redmond, WA). Results were considered significant if P < 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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. Subjects in the LOV- and mixed-diet groups were not significantly different in age, height, weight, or BMI at baseline. Mean (± SEM) body weight was unchanged in the mixed-diet group at the end of the 12-wk RT period but decreased by 1.1 ± 0.5 kg in the LOV-diet group (time-by-group interaction, P = 0.014). Midarm and midthigh body-circumference measurements were not significantly different between the groups at baseline or at week 12 of RT.
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After the 12 wk of RT, no significant changes from baseline were observed in mean type I fiber area in either group. Mean type II fiber area increased over time (P = 0.005; n = 18), indicating that type II muscle fiber area increased with 12 wk of RT. The mean increase in type II muscle fiber area was 7.3 ± 5.1% in the LOV-diet group and 16.2 ± 4.4% in the mixed-diet group, but the apparent difference in group response was not significant.
Muscular strength
Maximum dynamic muscular strength (as measured by 1RM) increased significantly in all muscle groups exercised in both dietary groups (Table 3). Statistical analysis showed no differences in baseline strength or increases in strength with RT between groups for any of the exercises performed. A 10–38% gain in mean muscular strength was observed for the exercises performed after 12 wk of RT.
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). Over time (between baseline and week 12 of RT), the muscle creatine concentration and the ratio of phosphocreatine to creatine did not change significantly, wheareas phosphocreatine and total creatine concentrations changed in a group-dependent manner. Mean phosphocreatine and total creatine concentrations increased in the LOV-diet group and decreased in the mixed-diet group. For all subjects combined (n = 18), regression analyses indicated that the within-subject changes over time in the concentrations of creatine (R, 0.711; P = 0.0009) and total creatine (R, 0.610; P = 0.0072), but not phosphocreatine (R, 0.394; P = 0.106) were related to the baseline concentration of the given compound. There were no significant linear relations between the changes in muscle creatine, phosphocreatine, or total creatine and changes in whole-body muscle mass (from urinary creatinine excretion).
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. As estimated from 3-d food records, habitual total energy (P < 0.01) and fat (P < 0.02) intakes were greater and carbohydrate, ethanol, and protein intakes were not significantly different between the LOV-diet group (prestudy) and the mixed- diet group (week 1 of RT). When the men assigned to the LOV-diet group started to self-select their LOV diets, their protein and fat intakes trended down, wheareas the energy, carbohydrate, and ethanol intakes did not change significantly (prestudy compared with week 1 of RT). For both the LOV-diet and the mixed-diet groups, there were no significant differences in mean dietary energy or macronutrient intakes between weeks 1 and 11 of RT. There were no significant differences in energy or macronutrient intakes between the LOV-diet and mixed-diet groups at weeks 1 and 11 of RT when the LOV-diet group was adhering to the dietary intervention.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONSUBJECTS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The RT program used in this study effectively and comparably improved muscle strength in both groups of men. The observed 10–38% increases in strength of the various muscle groups are fully consistent with the results of previous research that showed improved strength in older adults who undertook RT (5–7). The lack of difference in strength gains between the mixed-diet group and the LOV-diet group most likely reflects the small contribution of muscle hypertrophy to initial RT-induced strength gains relative to the contribution of the nervous system and improved neuromuscular control (2, 22).
The increased body density, whole-body muscle mass, and vastus lateralis muscle type II fiber area in the mixed-diet group are consistent with the results of previous RT studies in older men and women who consumed unrestricted diets (6, 23–26). Likewise, the unchanged or slight reduction in body density and whole-body muscle mass and the trend toward a smaller increase in vastus lateralis muscle type II fiber area in the LOV-diet group are consistent with the results of previous research of RT in older adults who consumed an LOV diet (7, 9).
Although these independent measures of body composition showed general agreement in the direction of change, the magnitude of the changes did not always match. For example, in the mixed-diet group the mean increase in muscle mass estimated from urinary creatinine excretion was 5.5 kg, whereas the mean increase in FFM estimated from body density was 1.7 kg. Similarly, in the LOV-diet group the mean decrease in muscle mass was 2.5 kg, whereas the mean decrease in FFM was 0.8 kg. Collectively, these data suggest that the qualitative results were similar for the hydrostatic weighing and urinary creatinine excretion methods but that the quantitative estimates of the change in muscle mass from urinary creatinine excretion exceeded estimates of the change in FFM from body density by hydrostatic weighing.
Indeed, a 5.5-kg mean increase in whole-body muscle mass exceeds reasonable expectations for a 12-wk RT program and reflects a probable overestimation of the actual change in muscle mass by the urinary creatinine excretion method. However, possible causes for this apparent overestimation of the changes in muscle mass in the mixed diet group remain to be established. The 18% increase in urinary creatinine excretion with RT in the mixed-diet group is consistent with a 15% increase measured in young men who undertook RT for 8 wk (27). Further research is required to determine whether the assumptions related to body creatine pool size and location, rates of conversion of creatine to creatinine, and renal handling of creatinine (16) remain valid in response to RT. Until then, the use of urinary creatinine excretion as a quantitative index of RT-induced changes in whole-body muscle mass must be considered unvalidated.
It is important to note that a variety of meat sources (eg, beef, pork, chicken, fish) were habitually consumed by the mixed-diet group and that all meat-containing foods were excluded from the diets of the LOV-diet group. Thus, this study did not distinguish among the different types of meat. Further research is required to assess whether the FFM gains and muscle hypertrophy in the mixed-diet group were due to unique properties of a specific source of meat.
The apparent decrease over time in energy intake observed in the LOV-diet group may have contributed to the observed decline in body weight. However, 3-d food records provide crude estimates, at best, of energy and nutrient intakes and serve primarily as general descriptors of actual food intake. The usefulness of 3-d food records is especially limited when such records are used to quantify changes in energy and nutrient intakes. Thus, we caution against reading too much into the quantitative results provided in these data. Whether the small decrease in body weight might have contributed to the slight declines in body FFM and muscle hypertrophy is questionable. Indeed, the small loss of body weight in the LOV-diet group in our study is a limitation that must be better controlled in future dietary and RT studies. However, previous research showed that FFM was maintained in subjects who consumed very-low-energy diets (28) and that skeletal muscle hypertrophy occurred in older men who lost weight during RT (8). Thus, we believe that the differences in body composition and skeletal muscle responses to the RT in the mixed- and LOV-diet groups were not solely due to differences in body-weight changes.
Even though food records are not quantitatively reliable, they do give an indication of dietary patterns. Total protein intake in the LOV-diet group trended lower as these men switched from an omnivorous to an LOV diet. Also, as expected, the sources of dietary protein changed dramatically. With the exclusion of any meat or meat-containing foods, the relative intake of protein increased for dairy and "other" food sources. The notion that the lack of FFM gain and muscle hypertrophy in the LOV-diet group was due to low dietary protein intakes cannot be ruled out but is not supported by research by Campbell et al (7, 9). In these studies, muscle hypertrophy did not occur after 12 wk of RT in older men and women who consumed LOV diets providing either the recommended dietary allowance (RDA) of protein (0.8 g protein•kg-1•d-1) or twice the RDA (1.6 g protein•kg-1•d-1)(29).
Alternative explanations for the differences in RT-induced changes in body composition between the mixed- and LOV-diet groups might relate to androgen hormone status and to diet-specific responses to protein metabolism, specifically, whole-body protein synthesis, breakdown, and net protein balance. Testosterone is an androgen hormone that functions to help regulate and stimulate the synthesis of proteins. Although unmeasured in our study, serum testosterone concentrations in young endurance-trained men were shown to be lower after a 6-wk period of consuming a high-protein LOV diet than after a similar period of consuming a high-protein, meat-containing diet (30). Recent data from Pannemans et al (31) showed that elderly women who consumed a diet high in vegetable protein (15.1% of energy; 5.0% from animal protein) did not experience postprandial inhibition of protein breakdown to the same extent as with a diet high in animal protein (14.5% of energy; 5.1% from vegetable protein), as assessed by using primed, continuous infusions of the stable isotope L-[1-13C]leucine. The result was a lower net protein synthesis for the diet high in vegetable protein than for an equivalent amount of protein provided in a diet high in animal protein. One might speculate that, if similar diet-specific responses to feeding occurred in the 2 groups of men in our study, differences in the rates of net protein synthesis between the mixed- and LOV-diet groups would contribute, over time, to differences in RT-induced whole-body protein accumulation and changes in FFM and muscle mass.
Muscle total creatine concentrations were lower in this group of older men than in young adults (32). These findings are consistent with those of Forsberg et al (33), who reported lower concentrations of total creatine in healthy men and women aged 61–85 y than in younger adult men and women, even when total creatine concentrations were expressed relative to DNA. The lower total creatine concentration in aged muscle might be explained by lower creatine transport in the muscles of older people. Creatine is transported into muscle by an insulin- and sodium-dependent transporter (34). Lower insulin sensitivity, a structural impairment of creatine transporter sarcolemal incorporation, or both, is possible.
The group-specific changes in muscle phosphocreatine and total creatine concentrations (increases in the LOV-diet group and decreases in the mixed diet group; Table 4
) were largely contrary to a priori expectations. We hypothesized that the muscle total creatine concentration would decline in the LOV-diet group over time, which is consistent with cross-sectional data showing lower total muscle creatine concentrations in vegans (32). In contrast, we hypothesized that total muscle creatine concentration would be unchanged in the mixed-diet group over time, which is consistent with results from several RT studies in young adults (see reference 35 for review). Although untested in our study, the observed group-specific changes may in part relate to changes in the rate of creatine synthesis in the kidney related with the rate-limiting enzyme glycine amidinotransferase (EC 2.1.4.1), which is fully activated when a creatine-free vegetarian diet is consumed and is repressed when creatine from meat sources is consumed (16).
The aim of this study was to assess whether the exclusion of all sources of meat from the diet influenced the ability of older men to achieve gains in FFM and muscle hypertrophy with RT. The results support our hypothesis and show that older men who consumed an LOV diet during a 12-wk period of RT did not achieve gains in FFM and muscle hypertrophy similar to those of older men who consumed an unrestricted omnivorous diet. We conclude that moderate incorporation of meat into the diet, following dietary recommendations (36), contributes to RT-induced gains in FFM and muscle hypertrophy in older men. This research provides a foundation for studying the importance of, and relations between, diet and exercise in the treatment of sarcopenia.
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ACKNOWLEDGMENTS |
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REFERENCES |
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