Flexibility and muscular strength and power are important functional capacity components that affect the efficacy of daily living activities in older adults. In this context, the improvement of muscular force and flexibility performance is routinely recommended to attenuate the deleterious effects of aging on these functional capacity components (2,19). However, the best way to include the development of both components within a single training session remains unclear (23).
Static stretching (SS) exercises traditionally have been incorporated at the beginning of training sessions to reduce the risk of injuries (14), improve performance (25), and increase range of motion (13). However, Pope et al. (21) concluded that stretching exercises do not reduce the risk of injuries; in addition, contradictory results have been reported with regard to the acute effect of stretching exercise on neuromuscular function. Recent studies have not demonstrated any effect of stretching exercise on muscle force performance (3,4,7). Nevertheless, reports have confirmed that different SS routines decrease both isometric and dynamic muscle strength (5,10,15,26). Contradictory results may arise from different sample characteristics, including training status, kind of exercise program, and experimental protocol. Therefore, when analyzing the results in the literature, the context of such characteristics must be taken into account.
Two main mechanisms have been proposed to explain the stretching-induced force deficit: a) structural changes in the musculotendinous unit and b) neural factors, such as decreases in motor neuron pool excitability, that may reduce peripheral muscular activation (10). The aging process is accompanied by alterations in both mechanisms. Increased complacence in the musculotendinous unit may partially explain the force reduction in older adults, and also complacence may be affected by SS exercises. Despite the reduction in neural activity observed during the aging process, stretching-mediated autogenic inhibition typically occurs only when extremely intense and long-lasting routines are used (10). For example, in young adults, Fowles et al. (10) reported a reduction in maximal voluntary contraction (MVC) and electromyographic (EMG) activity for the plantar flexors after 30 minutes of SS (13 sets at 135 s each). However, such routines are not representative of those used in practical settings. Yet, current recommendations to older adults include routines that are composed of 3 to 4 sets, with durations of 10 to 30 seconds each (18).
These findings and recommendations suggest that the following research question be addressed: Can such a recommended protocol promote decreases in both muscle force or activation? In older adults, it has not been established whether short periods of SS decrease the MVC or the ability to rapidly produce muscle force. We hypothesized that, when current recommendations for SS by older adults are applied, muscle force may be reduced without any change in muscle activation. Therefore, the purpose of this study was to investigate, in older women, the acute affect of SS on both muscle activation and force output.
Experimental Approach to the Problem
The recordings of the force-time curve and EMG activity during maximal effort made it possible to measure both muscle force output (rate of force development [RFD] and MVC) and muscle activation (integrated EMG [iEMG] activity). Each participant visited the laboratory on 3 occasions and was instructed not to perform any intense physical activity in the 24 hours preceding their evaluations. The objective of the first visit was to familiarize the participants with the procedures adopted in the isometric force-time curve measurement of the lower limbs and to determine the locations at which the electrodes should be placed to record the EMG signal (vastus medialis [VM]; vastus lateralis [VL]; and biceps femoris [BF] muscles). In the remaining 2 visits (with an interval of 48 hr between visits), the isometric force-time curve and the EMG activity were recorded simultaneously, using 1 of 2 different experimental conditions (SS or control without SS [C]). That is, each participant was tested in 1 of the conditions during 1 visit and in the remaining condition during the subsequent visit, in randomized order. To avoid circadian variations in muscular force, all participants performed their sessions at the same hour of the day.
Twenty-three older women (aged 64.6 ± 7.1 yr; height 156.8 ± 5.6 cm; weight 73.8 ± 14.7 kg) participated in this study. All of the participants were physically active and had participated regularly in a program of physical exercise at a frequency of 3 times a week for at least 3 months. The participants performed a localized muscular resistance program with small dumbbells and bats (shoulder side lifts; biceps and triceps curls: 3 sets each of 15 repetitions), a task involving body-weight resistance (squats: 3 sets of 15 repetitions), and walking. A physician examined the participants, and no recent skeletal-muscular lesions were reported. Participants were informed orally about the procedures they would undergo, and each signed an informed consent form. The Committee of Ethics in Research at São Paulo State University approved this study.
Measurement of Isometric Force-Time Curve
Previous to the isometric force-time curve measurement, 2 sessions of practice were conducted to familiarize the participants with the procedures (6). The maximum isometric force of the bilateral knee and hip extension was assessed by means of a force transducer (EMG System, 2,000 N), with the participants seated on the equipment as was described by Sahaly et al. (24), with knees flexed at 90°. Immediately before each evaluation, participants were instructed to produce an MVC, “as fast as possible,” for 5 seconds. As soon as the participants began the effort, they were verbally encouraged to exert a maximum effort. Each participant performed the test 3 times, with a recovery interval of 3 to 5 minutes between each trial. For the control (C) condition, the trial that presented the greatest MVC was adopted for later analysis. All trials in the static stretching (SS) condition were analyzed.
Signal acquisition was made using an analogic signal amplifier (EMG system) at a sample frequency of 2,000 Hz synchronized to all of the EMG signal recordings. The signal obtained from the force transducer was stored on a hard disk and analyzed afterward offline. First, the raw signal from the force transducer was filtered digitally by a fourth-order, zero lag Butterworth low-pass filter, using a cutoff frequency of 15 Hz. The onset of the contraction was defined as the point at which the muscular force value exceeded 2.5% of MVC above the baseline. The MVC was determined as the highest value registered within the 1-second window (500-1,500 ms) that corresponded to the onset of the muscular contraction in each trial. The peak (PRFD) was determined by the steepest slope of the curve, calculated within regular windows of 20 milliseconds (ΔForce/ΔTime), for the first 200 milliseconds after the onset of the contraction. Rate of force development values were obtained at time intervals of 0 to 50; 0 to 100; 0 to 150; and 0 to 200 milliseconds, relative to the onset of muscular contraction (1).
Electromyography Recording and Processing
Biological signals were obtained using an 8-channel module (EMG system), consisting of a signal conditioner with a band pass filter with cutoff frequencies at 20 to 500 Hz, an amplifier gain of 1,000X, and a common mode rejection ratio greater than 120 dB. A converting plate for A/D 12 bits signal was used to convert the analog to digital signals, with a sampling frequency of 2,000 Hz for each channel and an input range of 5 mV (8).
The EMG activities of the agonist VM and VL, as well as for the antagonist BF muscles, were registered by way of electrodes with a circular surface and a 10 mm capture area (silver/silver chloride). The distance from center to center of the interelectrodes was 23 mm. To lower the impedance of the skin, locations for electrode placement were carefully prepared (shaved, then cleaned with an abrasive and alcohol), and a layer of electrolytic gel was applied to the electrode surface. The positioning of the electrodes followed the recommendations of Hermens et al. (12).
The EMG signal was digitally filtered using a high-pass, fourth-order, zero lag Butterworth filter with a 5Hz cutoff frequency, followed by a moving root-mean-square filter with a time constant of 50 milliseconds (1). The iEMG activity was determined to be the area below the curve of the envelope signal for the different parameters of the isometric force-time curve. Thus, the iEMG was determined in time intervals of 0 to 50; 0 to 100; 0 to 150; and 0 to 200 milliseconds, relative to the onset of EMG integration. The onset of EMG integration was initiated 70 milliseconds before the individual onset of the contraction to account for the presence of an electromechanical delay (1). The iEMG activity for the MVC was determined within the 1-second window (500-1,500 ms) that corresponded with the onset of muscular contraction (11).
Static Stretching Protocol
In accordance with current international recommendations to older adults for maintaining the range of motion necessary to perform daily living activities, 3 30-second sets of SS exercises were applied to the major muscle and tendon groups of the lower limbs (18). The recovery interval between each set was 30 seconds. Discomfort caused by the stretching, as expressed by the participant, was used as a parameter to regulate the intensity of the exercise.
Stretching exercises, in order of performance, were as follows.
Standing Bilateral Hamstring Stretch
Standing with knees bent and with the feet apart and aligned with the hips, the participants were instructed to flex the hips toward the floor.
Standing Unilateral Quadriceps Stretch
The participants were instructed to stand, assisted by the experimenter, while flexing one knee, using the hand to support the ankle. After 30 seconds, the contralateral limb was submitted to the same procedure.
Seated Bilateral Hip Adductor Stretch
Sitting on the floor, with feet apart and knees extended, the participants were instructed to flex the hips by pushing the trunk forward.
Hip Extensors (Gluteus Maximus)
With the participant in a supine position and knee bent, the experimenter flexed and laterally rotated the hip joint. The same procedure was repeated with the contralateral limb.
With the subject in the prone position, the 2 experimenters fully flexed the subject's knee joints by pushing the heels toward the buttocks; the knees were then lifted so that the hip joints were extended.
One-way analysis of variance (ANOVA) with repeated measures was conducted for comparison between the C condition and the 3 trials of the SS condition. When a significant F ratio was observed, Fisher's least squares difference test was used as a post hoc test. Intraclass correlation coefficient (R) was used to test the reliability of dependent variables between the familiarization session and the C condition. An alpha of p ≤ 0.05 was considered statistically significant for the comparisons.
The intraclass correlation coefficients (R) for MVC and PRFD were 0.94 (95% confidence interval [CI]; 0.85- 0.97) and 0.84 (95% CI; 0.63-0.93), respectively. The results for MVC, RFD (0-50; 0-100; 0-150; and 0-200 ms), and PRFD are shown in Table 1. The MVC statistically decreased for the 3 S trials in comparison with the C condition (p < 0.01), indicating a stretching effect. The PRFD showed a significant reduction only in the first 2 trials in the S condition in comparison with the C condition (p = 0.05). With regard to the percentage change in relation to the C condition, smaller modifications were verified for MVC in comparison with the RFD modifications that were obtained for the different time instants. However, the absolute values for all of the RFD analyzed presented no significant modifications (p > 0.05).
There were no statistically significant alterations in iEMG activity of the VM, VL, and BF muscles in comparison with the C condition and the 3 trials in the S condition for the different RFD time instants (p > 0.05) (Figure 1). A similar pattern was verified for iEMG activity obtained during MVC (Figure 2).
The recording of the isometric force-time curve allows the assessment of 2 important expressions of muscular force, RFD, a critical component of muscular power output expression (1), and MVC. The main finding in this study was that the stretching routine negatively affected the PRFD and MVC of the older women (Table 1). These alterations were not accompanied by significant modifications in the iEMG activity of the VM, VL, and BF muscles (Figures 1 and 2).
McBride et al. (16) sought to investigate the effect of stretching on the quadriceps (3 sets at 33 s each) during the production of isometric force in multi- and monojoint exercises in young subjects. A significant reduction in RFD, during the first 400 milliseconds, was observed for the multijoint exercise, with no alteration in MVC. In the monojoint exercise, only the MVC was reduced. This indicates that alterations in the pattern of different isometric force-time curve parameters, which are mediated by stretching, can be influenced by exercise type. In our investigation, the fact that PRFD and MVC were negatively affected during the performance of multi-articular exercise may be related to the stretching of all thigh muscle groups in contrast with the stretching solely of quadriceps. McBride et al. (16) suggested that the absence of a decrease in MVC during multijoint exercise may be a result of the compensation made by the unstretched synergist hamstring muscle groups. Such compensation may not have occurred during our study because of the previous stretching of different muscles, which may have resulted in a decrease in external force output measured in both initial (PRFD) and posterior (MVC) time instants (Table 1).
Stretching duration is an important variable with regard to muscular force deficit induction. Ogura et al. (20) submitted 10 volunteers to 2 different durations of SS (30 and 60 s) and observed no significant alterations in MVC after 30 seconds of stretching as compared with a nonstretching control condition. However, in the 60-second condition, the MVC was significantly reduced as compared with the 2 other conditions. Fowles et al. (10) also reported a reduction in MVC for the plantar flexors after 30 minutes of SS (13 sets at 135 s each). Nevertheless, this stretching protocol is extremely prolonged and nonrepresentative of routines commonly used for warm-up, or even to improve flexibility (22). In our investigation, the total stretching time was 90 seconds, with the exception of the quadriceps, which was 180 seconds. In addition, it appears possible that, in older women, even a moderate duration (30 s) of SS, performed in repetitive sets, may result in significant decreases in the capacity for rapid and maximum force production.
Nelson et al. (18) investigated the effect of SS on force deficits in different knee ranges of motion. The authors reported a decrease in MVC only at a 162° angle, in contrast with shorter ones (90°, 108°, 126°, and 144°). In our study, the force-time curve was assessed at a 90° angle only, but a deficit also was observed. The MVC reduction, in association with the modification in PRFD, may suggest that, in older women, such impairment in the production of force should occur at different angles throughout the range of motion.
It has been proposed that 2 primary mechanisms are responsible for the decrease in those manifestations of muscular forces that are mediated by SS. One is neural alterations (i.e., the inhibited excitability of alpha motor neurons or the central nervous system); the other is alterations in the musculotendinous unit, such as an increase in compliance and a reduction of stiffness (20).
In the present study, the reduction of PRFD and MVC, without concomitant alterations in iEMG activity (Figures 1 and 2), strongly suggests that these responses may be linked to modifications in the musculotendinous unit (10). Edman and Tsuchiya (9) concluded that the compliance of the tendon is affected during stretching exercise. Thus, an increase in the compliance of the musculotendinous unit might also lead to an increase in the amount of time needed for the stretching of this structure during the production of force. This means that, at the onset of force development, the tendon has less capacity to transmit muscle force quickly to the bone, which directly affects the pattern of the RFD (17). In addition, Wilson et al. (27) reported a significant relation between stiffness of the musculotendinous unit and isometric force performance, suggesting that a stiffer musculotendinous unit would be more effective during the initial transmission of force and thus increase the RFD.
The absence of statistically significant modifications in muscular activation (iEMG) observed in the present study may be partially explained by the stretching protocol used. Several neuromuscular feedback responses may contribute to alterations in muscular activation after SS exercises. First, as noted by Fowles et al. (10), a possible autogenic inhibition in muscular activation, mediated by the Golgi tendon organs, requires an extremely intense stretching routine. However, our stretching routine was performed in such a way as to limit discomfort and for a short duration period. Also, according to Fowles et al. (10), the mechanoreceptor (type III afferent) and nociceptor (type IV afferent) may reduce the central drive. In addition, pain or discomfort were not reported during the poststretch isometric force-time curve assessment (10).
A possible limitation of our study was the amount of time that passed between the stretching of the first and the last muscle groups and the start of the isometric force-time curve measurement. This could have affected the time-related effects on neural muscle activation or mechanical alterations in the musculotendinous unit and, consequently, the isometric force-time curve pattern. However, the SS routine used in this study is in accordance with those recommended to older adults by both the American College of Sports Medicine and the American Heart Association for improving flexibility in the lower limbs or as a warm-up before muscular force exercises (19).
The present study helps to illustrate that stretching can negatively influence older women's capacity to produce muscular force. The possible mechanism responsible for this pattern does not appear to be related to neurologic factors but to mechanical factors of the musclotendinous unit. It appears, therefore, that the investigation of the effects of other related variables (e.g., type or duration of stretching) might help improve recommendations for SS exercises that precede activities involving high muscular force requirements or even athletic events. In older adults, for example, the RFD has been reported to correlate with capacity to maintain postural control; therefore, it should be considered an important component in physical exercise programs. Although our results revealed that PRFD was diminished, it should be noted that the influence of SS on neuromuscular function is transient, and a better understanding of this phenomenon presents relevant implications in the design of physical exercise programs. Both components of functional capacity (force and flexibility) are essential to the performance of daily living activities by older adults. Thus, if SS is used to improve flexibility, then it is recommended that this stretching is not practiced just before the performance of activities that require high levels of muscular force.
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