Introduction
Aging is associated with various physiological changes that detrimentally affect the neuromuscular system, including a reduction in muscular strength and skeletal muscle mass (4,8 ). The loss of strength and muscle mass are 2 of the main reasons for a decrease in performance of daily life activities in older individuals and negatively affect health, functional autonomy, survival, and quality of life in older individuals (4,8,24 ). Older women are particularly susceptible to the damaging effects of sarcopenia and dynapenia because of hormonal alterations after menopause and because women usually have lower initial levels of strength and muscle mass than do men (4,18 ).
Resistance training (RT) promotes positive adaptations that attenuate the deleterious effects of aging (2,5,14 ). However, it has been demonstrated that older individuals display an altered response to RT compared with the young (21,23 ), thus investigations concerning the response of the elderly to various RT training programs or systems are warranted. Resistance training prescription involves a number of variables of which training volume and intensity are key components (2 ). Training volume is a summation of the total number of repetitions performed multiplied by the resistance used and is affected by the number of sets, repetitions, and exercises performed as well as training frequency (2 ). Intensity refers to the absolute or relative resistance used for a given exercise or movement (2 ) and is affected by the rest interval between sets and exercises and velocity of movement.
Studies indicate a clear dose-response relationship between the magnitude of load and muscular strength increase in older individuals (11,13,27,34 ). However, for muscular hypertrophy , greater loads do not necessarily result in maximal adaptations (29 ). Muscular hypertrophy is hypothesized to be stimulated by mechanical and metabolic stress, muscle damage, and the interaction between these factors (28 ), and moderate volume and intensity are purported to optimize hypertrophic adaptations (2 ). This is mainly due to the interdependence between intensity and volume; that is, high-intensity training does not allow a sufficient training volume to create an optimal anabolic environment. To optimize the hypertrophic response of RT systems that allow the use of higher intensities without drastic reductions in volume have been suggested.
The pyramid system (PR), because of its inherent characteristic of varying the resistance used and number of repetitions, permits exercise performance at higher intensities without necessarily causing a loss in volume, thus maintaining a favorable anabolic environment for increased muscle hypertrophy and thus strength gains. Hypothetically, if a PR system allows training with high intensity and maintains volume, the metabolic and mechanical stimuli necessary to maximize muscle growth may be optimized. Based on this information, we cannot rule out the possibility that the PR system may elicit greater improvements of adaptations induced by RT. However, although the PR system is widely used by practitioners, there is little scientific basis to support its actual effectiveness.
The main anabolic hormones involved in muscle growth and remodeling are testosterone and insulin-like growth factor (IFG-1) (30 ). Mechanical loading elicits acute increases in anabolic hormones such as testosterone and IGF-1, although the hypertrophic effects of this response remain equivocal (28–30 ). There is evidence that basal levels of testosterone and IGF-1 influence the anabolic response to RT (3,12 ). However, it remains largely unknown whether there are differential effects between RT systems with respect to changes in the basal hormonal levels.
Therefore, the main objective of this study was to investigate the effect of RT performed in a PR system and traditional (TD) system on muscular strength, muscle mass, and hormonal responses in older women. We hypothesized that the PR system would result in greater increases in muscular strength and hypertrophy compared with a TD system. The rationale for this hypothesis is based on the dose-response relationship between intensity and volume on muscular strength, and hypertrophy , because the PR system ostensibly allows for the use of higher intensities of load during the final sets of an exercise without impairing volume in the target repetition range (i.e., 8–12 repetition maximum [RM]).
Methods
Experimental Approach to the Problem
The study was performed over a period of 36 weeks divided into 3 phases. In the first phase, participants were randomly separated into 2 groups that performed 8 weeks (weeks 3–10) of RT of either a TD and PR system. Phase 2 was a 12-week period of detraining (weeks 13–24) in which no resistance exercise was performed. The intent of the detraining phase was to return participant's physical fitness levels to baseline values. Phase 3 used a crossover so that subjects who performed the PR system in phase 1 underwent 8 weeks of training using the TD system (weeks 27–34) and those who previously performed the TD system engaged in an 8-week program using the PR system. At the beginning and the end of each phase of the experiment, 2 weeks were allocated for evaluations (weeks 1–2, 11–12, 25–26, and 35–36) consisting of anthropometric measures, tests of 1 repetition maximum (1RM), body composition analysis by dual-energy X-ray absorptiometry (DXA), and blood work for biochemical analysis. The experimental design is displayed in Figure 1 .
Figure 1.: Experimental design.
Subjects
Participants were recruited through newspaper and radio advertisements and home delivery of leaflets in residential neighborhoods. All participants completed health history and physical activity questionnaires and met the following inclusion criteria: 60 years old or older, physically independent, free from cardiac or orthopedic problems, not receiving hormonal replacement therapy, and not performing any regular physical exercise more than once a week during the 6 months before start of the study. Participants passed a diagnostic, graded exercise stress test with a 12-lead electrocardiogram reviewed by a cardiologist and were released by the cardiologist for participation in this study with no restrictions on physical activity. Forty older women were accessed for eligibility. After individual interviews, 11 women who did not meet the inclusion criteria were excluded. The remaining 29 older women were selected for participation and then were randomly assigned to 1 of 2 RT groups: a group that performed the TD system (n = 14) or a group that performed the PR system (n = 15) in the first phase of the study protocol. A total of 25 participants (67.6 ± 5.1 years, 65.9 ± 11.1 kg, 154.7 ± 5.8 cm, and 27.5 ± 4.5 kg·m−2 ) completed all stages of the study and were included in the analyses. The reasons for withdrawal from the study were reported as lack of time, transportation issues, lack of motivation, and personal reasons. Adherence to the program was satisfactory, with all subjects participating in >85% of the total sessions. Figure 2 is a schematic representation of participants' recruitment and group assignment.
Figure 2.: Schematic representation of participants' recruitment and allocation.
Written informed consent was obtained from all subjects after a detailed description of study procedures was provided. This investigation was conducted according to the Declaration of Helsinki and was approved by the local University Ethics Committee.
Anthropometry
Body mass was measured to the nearest 0.1 kg using a calibrated electronic scale (Balmak, Laboratory Equipment Labstore, Curitiba, Brazil), with the participants wearing light workout clothing and no shoes. The height was measured to the nearest 0.1 cm with a stadiometer attached to the scale with subjects wearing no shoes. The body mass index was calculated as body mass in kilograms divided by the square of height in meters.
Muscle Mass
Skeletal muscle mass was estimated by the predictive equation proposed by Kim et al. (20 ). The appendicular fat-free mass used for the equation was determined by a DXA scan (Lunar Prodigy, model NRL 41990; GE Lunar, Madison, WI). Before scanning, participants were instructed to remove their personal objects containing metal. Scans were performed with the subjects lying in the supine position along the table's longitudinal centerline axis. Feet were taped together at the toes to immobilize the legs while the hands were maintained in a pronated position within the scanning region. Subjects remained motionless during the entire scanning procedure. Both the calibration check and analysis were performed by a skilled laboratory technician. The equipment calibration was checked following the manufacturer's recommendations. Software generated lines using standard anatomical landmarks that separated the limbs from the trunk and head. These lines were adjusted, if needed, by the same technician using specific anatomical landmarks. Analyses during the intervention were performed by the same technician who was blinded to the intervention time point and which RE training program the participants were performing at the different time points of the study. Previous test-retest scans resulted in an SE of measurement of 0.29 kg and intraclass correlation coefficient of 0.997 for skeletal muscle mass.
Muscular Strength
Maximal dynamic strength was evaluated using the 1RM test assessed for the chest press, knee extension, and preacher curl performed in the order listed. Testing for each exercise was preceded by a warm-up set (6–10 repetitions), with approximately 50% of the estimated load used in the first attempt of the 1RM. This warm-up was also used to familiarize the subjects with the testing equipment and lifting technique. The testing procedure was initiated 2 minutes after the warm-up set. The subjects were instructed to try to accomplish 2 repetitions with the load in 3 attempts in all exercises tested. The rest period was 3–5 minutes between each attempt and 5 minutes between exercises. The 1RM was recorded as the last resistance lifted in which the subject was able to complete only 1 repetition (1 ). The technique for each exercise was standardized and continuously monitored to ensure reliability. All 1RM testing sessions were supervised by 2 experienced researchers to maximize safety and test reliability. Verbal encouragement was given throughout each test. Three 1RM sessions were performed separated by 48 hours (intraclass correlation coefficient ≥0.96). The highest load achieved among the 3 sessions was used for analysis in each exercise. Total strength was determined as the sum of the 3 exercises.
Biochemical Analysis
Serum levels of testosterone and IFG-1 were measured after 12 hours of fasting with blood taken from the antecubital vein. The subjects were instructed not to perform vigorous exercise for the preceding 24 hours and to avoid alcohol or caffeinated beverages 72 hours before the blood collections. Measurements were performed by standard methods in a University Hospital laboratory. Samples were collected in vacutainers with a gel separator without anticoagulant and were centrifuged for 10 minutes at 3,000 rpm for serum separation. Interassay and intra-assay CVs were <10% as determined in human serum. Serum testosterone and IGF-1 concentrations were determined by a chemiluminescence method using a Liaison XL Immunoassay Analyzer (DiaSorin S.p.A, Saluggia, Italy).
Volume Load
During every RT session, the load and number of repetitions performed during each set of the 8 exercises were recorded. The volume for each set of all exercises was calculated by multiplying the load times the number of repetitions in each set performed. Volume of each exercise per session was calculated as the sum of the volume of all 3 sets for each exercise. The total volume per session was calculated as the sum of all 8 exercises. Weekly volume was calculated as the sum of the 3 sessions performed in a week.
Resistance Training Program
Supervised RT was performed during the morning hours in the State University facilities. The protocol was based on recommendations for RT in an older population to improve muscular strength and hypertrophy (2,14 ). All participants were personally supervised by physical education professionals to help ensure consistent and safe exercise performance. Subjects performed RT using a combination of free weights and machines. The sessions were performed 3 times per week on Mondays, Wednesdays, and Fridays. The RT program was a whole-body program of 8 exercises with 1 exercise performed with free weights and 7 with machines. Exercises were performed in the following order: chest press, horizontal leg press, seated row, knee extension, preacher curl (free weights), leg curl, triceps pushdown, and seated calf raise.
Participants of the TD group performed 3 sets of 8–12 RM with the same load for all 3 sets, whereas the participants of the PR group performed 3 sets of 12, 10, and 8 RM. For both systems, the participants carried sets to muscle failure or an inability to sustain exercise performance with proper exercise technique.
Participants were instructed to inhale during the eccentric phase and exhale during the concentric phase of each repetition while maintaining a constant velocity of movement at a ratio of approximately 1:2 (concentric and eccentric phases, respectively). Participants were allowed 1–2 minutes of rest between sets of an exercise and 2–3 minutes between exercises. Researchers adjusted the loads of each exercise according to the subject's abilities and improvements in exercise capacity throughout the study to ensure that the subjects were exercising with as much resistance as possible while maintaining proper exercise technique. The incremental adjustment of loads from set to set was in the magnitude of approximately 2–5%. Progression for the TD occurred when the upper limits of the repetition zone was completed for 2 consecutive training sessions. Progression for the PR occurred when the participant was able to perform 12 and 10 repetitions with the 12 and 10 RM loads and 10 repetitions with the 8 RM load. Progression for both training systems was accomplished by increasing the load for the upper limb and lower limb exercises by 2–5% and 5–10%, respectively, in the next session (2 ).
Statistical Analyses
Two-way analysis of variance for repeated measures was used for comparisons of the 2 training groups. When an F-ratio was significant, Bonferroni's post hoc test was used to identify where the mean differences were significant. The comparison between RT systems for the number of repetitions performed was assessed by Student's dependent t test. The effect size (ES) was calculated as posttraining mean minus pretraining mean divided by pooled SD before and after training (9 ). For all statistical analyses, significance was accepted at p ≤ 0.05. The data were analyzed using STATISTICA software version 10.0 (StatSoft, Inc., Tulsa, OK, USA).
Results
The average of number of repetitions per exercise performed throughout the training was statistically (p < 0.001) different between systems with more repetitions per exercise performed during the TD training (32.2 ± 1.6, 95% confidence interval [CI] = 31.4–32.8) compared with PR training (30.1 ± 0.3, 95% CI = 30.0–30.3). The total training loads in both the first and the last week of the RT program are depicted in Table 1 . There was a significant main effect of group (p ≤ 0.05), in which, as expected, the PR presented higher values than did the TD. There was a significant main effect of time (p ≤ 0.05) with both groups showing increases; however, no group-by-time interaction was noted (p > 0.05).
Table 1.: Training loads (in kg) at the first and last week of the resistance training program.*
Figure 3 shows the results for muscular strength, fat-free mass, and skeletal muscle mass before and after training for both groups. There was no significant group-by-time interaction (p > 0.05) for any of the exercises analyzed and for the sum of the 3 exercises. However, a significant main effect of time was observed (p < 0.001), in which increases were observed for chest press (TD = 12.4% and ES = 0.86 vs. PR = 11.5% and ES = 0.74), knee extension (TD = 12.5% and ES = 0.61 vs. PR = 11.8% and ES = 0.62), preacher curl (TD = 10.9% and ES = 0.63 vs. PR = 8.6% and ES = 0.54), and total strength (TD = 11.6% and ES = 0.78 vs. PR = 10.6% and ES = 0.71). For body composition, there was no significant group-by-time interaction for any of the components determined (p > 0.05). However, a significant main effect of time (p < 0.001) was observed in which both groups had increased fat-free mass (TD = 2.1% and ES = 0.27 vs. PR = 1.3% and ES = 0.18) and skeletal muscle mass (TD = 3.6% and ES = 0.32 vs. PR = 2.4% and ES = 0.24).
Figure 3.: Muscular strength (A-D), fat-free mass (E), and skeletal muscle mass (F) at pre- and posttraining. *p ≤ 0.05 vs. pretraining. Data are expressed as mean and SD . There was no statistically significant group-by-time interaction.
Figure 4 depicts the weekly volume load. There was a significant group-by-time interaction (p < 0.001), in which differences between both groups started from the third week, with the TD system reaching higher volume loads in comparison with PR system.
Figure 4.: Weekly volume of load during a resistance training program in older women according to resistance training system. *p ≤ 0.05 vs. previous week. **p ≤ 0.05 vs. 2 previous weeks. §p ≤ 0.05 vs. pyramid. There is a statistically significant group-by-time interaction.
Resting values before and after training for IGF-1 and testosterone are presented in Table 2 . There were no significant differences for the hormones tested (p > 0.05). The effect of 12 weeks of detraining is presented in Table 3 ; there was no group-by-time interaction (p > 0.05) for any of the outcomes analyzed, which indicates that the TD and PR systems showed similar loss of adaptations due to detraining.
Table 2.: Anabolic hormones in older women before and after training according to the resistance training system.*
Table 3.: Changes after 12 weeks of detraining.*
Discussion
The main and novel finding of this study was that the RT performed in the PR system is equally as effective as a TD system for promoting adaptations in muscular strength and hypertrophy in older women. Based on the premise that intensity and volume of training are 2 primary variables that stimulate neuromuscular adaptations (2,28 ), we had hypothesized that the PR system would produce superior results. Specifically, it was speculated that the PR system would allow the use of higher intensities of load during the final sets of an exercise without impairing volume in the target repetitions range (i.e., 8–12 repetitions maximum). The greatest gains in maximum strength are achieved by training with higher loads, and there is a dose-response relationship between magnitude of load and muscular strength in older adults (11,13,27,34 ). Contrary to our hypothesis, the results of this study failed to demonstrate superiority of the PR over the TD system.
Previously, Hunter et al. (19 ) investigated the effect of variable loads in older adults and observed that a varied daily loading approach (80, 65, and 50% of 1RM) reduced the difficulty of performing daily activity tasks to a greater extent than did training with a constant load (80% of 1RM) despite similar increases in muscular strength and fat-free mass between groups. However, some methodological differences between this study and the study by Hunter et al. (19 ) need to be pointed out. The study by Hunter et al. (19 ) had a wider variance of load and included both older men and women, which might affect the results because older women respond differently than older men to a RT program (25 ). Moreover, we used a crossover design, an experimental procedure that reduces interindividual bias, and therefore strengthens confidence in our findings.
A confounding issue when evaluating muscle mass increases in studies that compare different intensities of training is that the total volume often differs between models (32 ). When the aim is to analyze hypertrophic responses, studies show that the total volume does affect the hypertrophic response. For example, studies that compared different intensities with matched volumes did not find statistical differences in muscle hypertrophy between low and high intensities (6,31 ). Alternatively, studies without volume equalization generally show that lower intensity RT results in inferior hypertrophic gains compared with moderate intensities (7,26 ). The PR system theoretically allows training with higher loads, at least during the final sets of an exercise, without reducing the training volume from a loading zone standpoint. The results observed in this study indicate that increases in skeletal muscle mass are similar between the RT systems, despite a significantly lower volume load observed in the PR condition. A clear dose-response relationship has been reported between RT volume and muscular strength and hypertrophy (22 ). The current results show that the PR system did allow higher loads, but the weekly training volume was lower with the PR system than with the TD system. However, beneficial effects of increasing the volume undoubtedly follows an inverted-U curve, whereby once a given threshold is reached, any further increases in volume would have no further effect and at some point lead to regression in gains. The results of our study would seem to indicate that the threshold for volume in the population studied was achieved in the PR system, making the discrepancies in the volume of load irrelevant in terms of producing a hypertrophic response. Alternatively, it is possible that increased intensities of load used in the later sets may have compensated for the reduced volume, thereby balancing out gains between training groups. These hypotheses warrant further investigation.
Blood concentrations of anabolic hormones are diminished with aging (10,17,33 ), which may lead to attenuation of anabolic effects on muscles. No statistically significant changes were observed with respect to resting circulating testosterone and IGF-1 levels after the RT period. These results are in line with previous studies that investigated the effects of RT on testosterone and IGF-1 in older women (15,16 ). Despite low levels of anabolic hormones, older women nevertheless show significant increases in muscular hypertrophy after RT. Our study measured only serum hormonal values; it is possible that the RT program induced changes at the hormone receptor level that enhanced the anabolic processes (35 ).
It is important to note that this study has several limitations. The findings are specific to untrained older women and cannot necessarily be extrapolated to other populations. Whether results would differ for younger individuals, men, or those with previous RT experience remains to be determined. Moreover, our results are limited to a short-term RT period, and we cannot rule out the possibility that findings would differ over longer training durations.
We conclude that RT performed in a PR system is an effective method to promote positive short-term adaptations of muscular strength and hypertrophy in older women. However, it does not provide any inherent advantages over a TD system. Thus, the practitioner can decide which system to use depending on the trainees' personal preference.
Practical Applications
Our findings show that both RT systems (PR and TD) are equally effective for increasing strength and muscle mass in older women. The results indicate that practitioners have the flexibility of choosing the RT system based on the trainees' preference. Practitioners also have the option of using a combination of different RT systems over time, as this may help to maintain interest in and motivation to perform RT by allowing a varied RT program.
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