It is well known that muscle strength decreases with aging (1,9), and it has also been suggested that a steeper decline of muscle strength begins after the age of 50 yr (35,38). According to previous findings (1,25), the decline of muscle strength with aging has been ascribed to the declines of muscle mass and neural drive to muscle. Some previous researches demonstrated that a decline in muscle thickness and cross-sectional area with aging starts after the age of 60 yr (9,24). On the other hand, no studies have ever tried to investigate when the age-related changes in the neural drive to muscle starts, although some previous researchers have made comparison of the neural drive to muscle between younger and elderly (25).
Previous findings obtained from animal and human cadaver experiments showed that the ultimate strength and Young's modulus of the tendons decreased with specimen age (5,11,20). Recently, studies have demonstrated the age-related changes in the human tendon properties in vivo (14,18,30). For example, Onambele et al. (30) report that middle-aged and older individuals (46 ± 1 yr, 68 ± 1 yr) had lower stiffness and Young's modulus of the Achilles tendon than did younger individuals (24 ± 1 yr). We have observed that the maximal strain of the human tendon structures in knee extensors decreased significantly with aging (18). However, according to these previous studies, which have used both human cadaver and in vivo experiments, it is not clear at which age this impairment begins.
In recent years, the number of middle-aged and elderly people who participate in sports has been increasing in those societies with the longest average life expectancy. As a result, injuries from overuse are becoming recognized in middle-aged and elderly people (13). In particular, the human Achilles tendon is the most common tendon to rupture during sports and daily activities (12). Furthermore, some previous researchers have indicated that the rupture of this tendon often occurs in men in their 30s (10,19,29). However, the reason for this phenomenon is not clear at present.
It remains an unsettled question whether the process of age-related changes in the morphology and the function of human muscle and tendon are the same. The purpose of this study was to determine age-related changes in the plantar flexor muscles and Achilles tendon in 59 healthy men aged between 20 and 77 yr.
METHODS
Subjects.
A total of 59 male subjects agreed to participate in the present study. The subjects were distributed into four age groups: a 20-yr group (ages 20-27 yr, N = 19), a 30-yr group (ages 31-38 yr, N = 15), a 50-yr group (ages 46-57 yr, N = 10), and a 70-yr group (ages 62-77 yr, N = 15). The physical characteristics of the subjects are shown in Table 1. The subjects in the study were either sedentary or mildly to moderately active men, but none were involved in any type of resistance exercise program at the time of the study. The procedures, purpose, and risks associated with the study were explained to all the subjects before they gave their written informed consent to participate in this investigation. This study was approved by the office of the department of sports sciences, University of Tokyo, and complied with their requirements for human experimentation.
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TABLE 1: Physical characteristics and steps numbers.
Numbers of steps.
For a 2-wk period, the numbers of steps of each subject were measured to document their physical activity levels during daily life. Subjects put the pedometer (FB-714, TANITA, Tokyo, Japan) on their belt or waistband as soon as they woke up each morning, removed it before going to bed every night, and recorded their number of steps each day. The total numbers of steps each day were recorded on daily log sheets. In the present study, the mean numbers of steps during 2 wk were used as an index of physical activity level during daily life.
Muscle thickness.
The muscle thickness of the plantar flexors was measured with an ultrasonic apparatus (SSD-2000, Aloka, Japan) at six anatomic sites: on the posterior medial and lateral surfaces, 20, 30, and 40% between the lateral malleous of fibula and the lateral condyle of the tibia. The anatomic sites for the measurements are presented in Figure 1. Each subject remained in a prone position with the legs straight and the muscles relaxed. The anthropometric locations of the measurement sites were precisely determined and marked by experienced technicians before the ultrasonic measurement. A transducer with a 7.5-MHz scanning head was coated with water-soluble transmission gel, which provided acoustic contact without depressing the dermal surface. The muscle thickness of each site was measured to the nearest 0.1 mm using a vernier caliper. The mean values of muscle thickness at all measured sites were adopted as their representative of the muscle size of the plantar flexor muscles.
FIGURE 1: Thick bars represent the locations of sonographic scanning sites for plantar flexors (six sites). The mean values of muscle thickness at all measured sites were adopted as their representative of muscle thickness.
Muscle strength and central neuromuscular activation.
Maximal voluntary isometric strength (MVC) of the plantar flexor muscles was determined using an electrical dynamometer (Myoret, Asics, Japan). The subject lay prone on a test bench, and the waist and shoulders were secured by adjustable lap belts and were held in position. The right ankle joint was set at 90° (anatomic position) with the knee joint at full extension, and the foot was securely strapped to a foot plate connected to the lever arm of the dynamometer. Before the test, the subject performed a standardized warm-up and submaximal contractions to become accustomed to the test procedure. The subjects performed more than two trials within a 1-min rest period. The highest among two trials was accepted as the muscle strength.
During MVC, evoked twitch contractions were imposed by supramaximal electric stimulations. The experimental procedures have been described in detail previously (4). The stimulating lead electrodes were placed on the skin of the right popliteal fossa and were oriented longitudinally to the estimated path of the tibial nerve with the anode distal. A high-voltage stimulator (SEN-3301, with a specially modified isolator SS-1963, Nihon-Koden, Japan) generated rectangular pulses (triple stimuli, with a 500-μs duration for one stimulus and an interstimulus interval of 10 ms). The stimulation intensity was confirmed by setting the output of the stimulator to a level at which there was no further increase in twitch torque. In all subjects, the stimuli increased the force during MVC at the appropriate latency. Shortly (within 1-2 s) after MVC, when the potentiation effect of the contraction still persisted, the same stimulation was given to the muscle at rest (control twitch). Thevoluntary force at the instant of stimulation was used as the MVC force. Two separate efforts were made routinely, and a third extension was performed if more than a 5% difference existed. The measured values that are shown below are the means of two trials. The twitch force (difference between peak twitch force and MVC force) was measured, and from this, the level of muscle activation with voluntary effort (% activation) was assessed from the following equation (twitch interpolation technique (4)): % activation = {1 − (twitch force during MVC/control twitch force)} × 100 (%), where control twitch represents the twitch imposed on the resting muscle after MVC. In the present study, the activation level for the 70-yr group was not measured because of ethical issues and scheduling limitations.
Elongation of the Achilles tendon.
The experimental setup has previously been described in detail (16,17). The subject was instructed to develop a gradually increasing force from a relaxed state to maximal voluntary contraction (MVC) within 5 s. The task was repeated two times per subject, with at least 3 min between trials. The measured values shown below are the means of two trials. An ultrasonic apparatus (SSD-2000, Aloka, Tokyo, Japan) with an electronic linear-array probe (7.5-MHz wave frequency with 80-mm scanning length; UST 5047-5, Aloka) was used to obtain longitudinal ultrasonic images of the medial gastrocnemius muscle. The probe was longitudinally attached to the dermal surface with adhesive tape, which restrained the probe from sliding. A marker (black arrows in Fig. 2) was placed between the skin and the ultrasonic probe as the landmark to confirm that the probe did not move during measurements. To evaluate the elongation of the Achilles tendon, the displacement of the distal myotendinous junction (dL; Fig. 2) of the medial gastrocnemius muscle in the transition from rest to MVC was measured (16,26). In the present study, the Achilles tendon was defined as the distance between the Achilles tendon insertion and the distal myotendinous junction of the medial gastrocnemius muscle (16,26). The ultrasonic images were recorded on videotape at 30 Hz and were synchronized with force recordings using a clock timer for subsequent analyses.
FIGURE 2: Ultrasonic images of longitudinal sections of the Achilles tendon at rest and MVC. The black arrows point to the shadow generated by an echo-absorptive marker attached by adhesive to the skin. P1 and P2 moved proximally during isometric torque development from rest to MVC. The distance traveled by P1 and P2 (dL) was defined as the elongation of the Achilles tendon during contraction.
The tendon displacement can be attributed to both angular rotation and contractile tension, because any angular joint rotation occurs in the direction of ankle plantarflexion during an isometric contraction (16,21,26). To monitor ankle-joint angular rotation, an electrical goniometer (Penny and Giles) was placed on the lateral aspect of the ankle. To correct the measurements taken for the elongation of the Achilles tendon, additional measurements were taken under passive conditions. The displacement of the myotendinous junction of the medial gastrocnemius muscle caused by rotating the ankle from 90 to 70° was digitized in sonographs taken as described above. Thus, for each subject, the displacement of the myotendinous junction obtained from the ultrasound images could be corrected for that attributed to joint rotation alone (16,21). In the present study, only values corrected for angular rotation are reported.
To calculate the strain values from the measured elongation, we measured the respective length of the Achilles tendon, from the myotendinous junction (position of the probe) to the insertion of Achilles tendon (16,26). In a preliminary study, the coefficient of variation (100 × SD/mean) for repeated measurements of the maximal elongation of the Achilles tendon in one subject was 7.4%.
Statistics.
Descriptive data include means ± SD. One-way analysis of variance (ANOVA) was used for the comparison among the four groups. If the F-statistic of the analysis of variance was significant, differences between groups were assessed by the Scheffe test. The level of significance was set at P < 0.05.
RESULTS
Height, body mass, and lower-leg length in the 70-yr group were significantly lower than those of the other groups (all P < 0.01), whereas no significant differences were observed among the 20-, 30-, and 50-yr groups (Table 1). There was no significant difference in the number of steps per day among all the groups.
The absolute muscle thickness of the 70-yr group (59.4 ± 5.6 mm) was significantly lower than that of the other group (all P < 0.05), whereas no significant differences were observed among the 20-yr (63.8 ± 5.1 mm), 30-yr (64.4 ± 3.9 mm), and 50-yr (64.7 ± 4.5 mm) groups (Fig. 3A). There was no significant difference in relative muscle thickness (to limb length) among all the groups (Fig. 3B).
FIGURE 3: Absolute (upper) and relative (to limb length; lower) muscle thickness of plantar flexor muscles from the four age groups. Values are means ± SD. * P < 0.05.
The absolute MVC of the 70-yr group (63.4 ± 18.4 N·m) was significantly lower than that of the other groups (all P < 0.05), and that of the 50-yr group (105 ± 24 N·m) was significantly lower than that of the 20-yr group (P = 0.031) (Fig. 4A). The difference in MVC between the 20-yr (124 ± 24 N·m) and 30-yr (119 ± 21 N·m) groups was not significant (P = 0.599). The relative MVC (to body mass) did not alter these observations, although the differences among groups were smaller (Fig. 4B).
FIGURE 4: Absolute (upper) and relative (to body mass; lower) maximal strength of plantar flexor muscles from the four age groups. Values are means ± SD. * P < 0.05.
The activation level of the 50-yr group (83.9 ± 6.7%) was significantly lower than that of the 20-yr (94.1 ± 4.7%; P < 0.001) and 30-yr (93.0 ± 7.8%; P = 0.037) groups, and the difference in activation level between the 20- and 30-yr groups was not significant (P = 0.607) (Fig. 5).
FIGURE 5: Activation level of plantar flexor muscles from the three age groups, except for the 70-yr group. Values are means ± SD. * P < 0.05.
The maximal strain of the Achilles tendon of the 70-yr group (3.1 ± 0.7%) was significantly lower than that of the other groups (all P < 0.01), and that of the 50-yr group (4.0 ± 0.5%) was also lower than that of the 20-yr group (P = 0.003) (Fig. 6). Furthermore, the maximal strain of the Achilles tendon of the 30-yr group (4.4 ± 0.8%) tended to be lower than that of the 20-yr group (5.1 ± 0.8%) (P = 0.062).
FIGURE 6: Maximal strain of the Achilles tendon from the four age groups. Values are the mean ± SD. * P < 0.
DISCUSSION
The present study has shown the age-related decrease in the maximal strain of the Achilles tendon (Fig. 6). Recently, we have also reported that the maximal strain of tendon structures in the knee extensors decreased significantly with aging (18). On the other hand, other researchers have shown different findings concerning age-related changes in human tendon properties (14,28,30). For example, Karamanidis and Arampatzis (14) have reported that there were no significant differences in maximal strain stiffness of the Achilles tendon between young (21-32 yr) and elderly subjects (60-69 yr). Onambele et al. (30) have shown that the maximal gastrocnemius tendon strain values of middle-aged (46 ± 1 yr) and older (68 ± 1 yr) individuals were significantly greater than those of younger subjects (24 ± 1 yr). Unfortunately, we cannot say the reasons for this discrepancy. On the other hand, previous findings obtained from human cadaver experiments have shown that ultimate strength and Young's modulus of the tendons decreased with specimen age (5,11,20). With regard to the collagen fibers of tendons, the mean area and diameter of collagen fibers have been shown to decrease with aging (27,34). The density and structure of cross-links and the fibril morphology in collagenous tissues have been shown to change with aging, in a manner that could be correlated with age-related changes in mechanical properties (32). Furthermore, age-related increases in connective tissue and collagen cross-linking have been reported that might decrease the tendon extensibility during muscle contractions (3). In fact, some previous studies using animals have shown that the maximal strain of rat-tail tendon decreases during aging (36,37). According to these previous findings, however, it is not clear at which age this impairment begins. An interesting finding of this study was that the maximal strain of the Achilles tendon in the 30-yr group tended to be lower than in the 20-yr group (P = 0.062). Therefore, the age-related changes of the Achilles tendon (i.e., decline in tendon extensibility) was already observed in men in the 30-yr group.
We should present a stress-strain relationship to compare the tendon properties of the different age groups accurately. In addition to the tendon extensibility, therefore, it would be necessary to consider the age-related difference in the morphological characteristics of tendon (i.e., cross-sectional area). Recently, Magnusson et al. (22) have demonstrated that elderly women had a greater Achilles tendon cross-sectional area compared with young women. Magnusson et al. (22) state that a greater tendon size may reduce the risk of injury to the tendon in elderly individuals. On the contrary, Onambele et al. (30) have reported that the cross-sectional area of the Achilles tendon was significantly smaller in older men than in young men. Thus, the data concerning the age-related difference in the human tendon size in vivo seem inconsistent and inconclusive.
In the present study, there was no significant difference in the relative muscle thickness (to limb length) of the plantar flexors among the four age groups (Fig. 3B). This result is inconsistent with the previous findings that declines in muscle thickness and cross-sectional area with aging start after the age of 60 yr (9). In these previous studies, however, age-related difference in the knee extensor and knee flexor muscles were investigated. According to our previous finding (15), there was no significant difference in the relative muscle thickness of medial gastrocnemius muscle between young and elderly groups, although in vastus lateralis muscle, the relative muscle thickness of the elderly group was significantly lower than that of the younger group. The reasons for the differences in the declines in muscle thickness with aging are unclear, but several possibilities exist. These discrepancies may be attributable to differences in the daily activity levels between the knee extensors and plantar flexors. We have considered that the relative activation level of plantar flexors would be higher than that of knee extensors during normal walking. In fact, Ericson et al. (6) state that the important role of the plantar flexors during walking was reflected in the comparatively high muscular activity at push-off. In any case, further investigations are needed to clarify this point.
It is well known that muscle strength decreases with aging, and this decrease is especially pronounced in populations beyond 50 yr (35,38). The age-related decrease in muscle force-generating capacity may be attributable to muscle atrophy and decreases in activation level (1,24). In the present study, the muscle strength and activation levels of the 50-yr group were significantly lower than those of the 20-yr group. In addition, according to the findings of Morse et al. (25), who used a procedure similar to that of the present study, the activation level of the elderly group (age 74 ± 4 yr) was 78%, and this value tended to be lower than that of the 50-yr group (84%) in the present study. On the other hand, there was no difference in relative muscle thickness among the four age groups (Fig. 3B). Considering these points, these results indicate that the decreases in muscle strength observed in the 50- and 70-yr groups were mainly caused by the age-related decrease in the activation level.
No significant differences in the muscle strength and activation level of the plantar flexor muscles were observed between the 20- and 30-yr groups (Figs. 4 and 5). Previous studies have indicated that under normal conditions, human muscle strength reaches its peak between the ages of 20-30 yr, after which time it remains more or less unchanged for more than 20 yr (31,35,38). Therefore, it seems reasonable to suppose that the force-generating capacity and activation level of the plantar flexor muscles remain steady until almost 40 yr.
On the other hand, the age-related changes of the Achilles tendon (i.e., decline in the tendon extensibility) was already observed in men in their 30s, as mentioned above. Similarly, Sargon et al. (33) have reported that the diameter of the collagen fibers taken from the 30- to 39-yr group was smaller than that of the 20- to 29-yr group. They stated that the decreases in diameter of collagen fibers in the 30- to 39-yr group would play a role in the frequency of Achilles tendon ruptures. It is well known that the tendons play a role in storing and releasing elastic energy during walking and running (2). In addition, tendon elasticity acts as a mechanical buffer, protecting the muscle from damage during high-intensity contractions (8). From this point of view, the present results imply that Achilles tendons in people in their 30s are apt to be injured during various activities. The Achilles tendon is one of the most frequently injured tendons in the human body (12). In particular, there is a peak in the occurrence of the Achilles tendon rupturing in men in their 30s (10,19,29). Taking the present results into account, together with the previous findings cited above (31,33,35,38), it is likely that a main reason for the high frequency of Achilles tendon ruptures in men in the 30-yr group is that the Achilles tendons of men in this age group are less able to cope with repetitive biomechanical stress because of the decrease in the tendon elasticity, although the muscle strength and activation levels in the 30-yr group were similar to those of the 20-yr group.
In the present study, the Achilles tendon was defined as the distance between the Achilles tendon insertion and the distal myotendinous junction of the medial gastrocnemius muscle (16,26). However, "Achilles tendon" as defined in this study included the aponeurosis of soleus muscle. According to some previous findings (7,23), the strain of aponeurosis in plantar flexor muscles was lower than that in free Achilles tendon. Therefore, the maximal strain of the free Achilles tendon would be greater than that of the present study. In addition, if the ratio of soleus muscle mass to gastrocnemius muscle mass increased with aging, the main results of this study (decline in maximal strain with aging) would be affected by the stiffer aponeurosis of soleus muscle. As far as we know, however, there have been no studies concerning these points. Therefore, we believe that the definition of Achilles tendon in the present study is valid for comparisons across different age groups, because we used the same methods for all subjects.
In conclusion, the age-related changes in human plantar flexor muscles and in the Achilles tendon were different from each other. In particular, the age-related changes of the Achilles tendon (i.e., decline in the tendon extensibility) was observed in men in their 30s, whereas there were no differences in muscle strength and activation levels between the 20- and 30-yr groups. These results indicate that the high frequency of Achilles tendon ruptures in men in the 30-yr group was caused by these differences in the aging processes of muscle and tendon.
This research was supported by grants from the Meiji Yasuda Foundation for Health Science.
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