The aging process is accompanied by skeletal muscle changes including reductions in mass, strength, and muscular quality, which are also known as sarcopenia (25,32). It has been well established that skeletal muscle mass begins to decline around the fourth to fifth decade of life and progresses at a rate of 8–15% per decade, with more accelerated loss occurring after 65–70 years of age (18,28,29). The muscle mass loss associated with age involves reductions both in muscle fiber size and number, especially type II fibers (1,29). A preferential decrease in muscle mass in the lower body is observed in the elderly (18), which is directly related to functional capacity and independence (45).
Despite strong evidence of a progressive decline in muscle strength with aging, the capacity to generate eccentric force seems to be more preserved in older adults. It is estimated that deficits in concentric strength can reach 56%, whereas a decline of only 25% is expected for eccentric strength (47). Neural, mechanical, and cellular mechanisms have been speculated to be contributors to age-related differences between concentric and eccentric strength (40,47).
Age-related changes in the neural drive (impaired agonist activation and increased antagonist coactivation) could contribute to the differences between eccentric and concentric strength in the elderly, because concentric force production is more dependent on agonist/antagonist activity than eccentric force (11,22). It is important to note that the exact mechanisms underlying neural modulation during eccentric contractions remain unknown, as do age-related changes in it (10). So, there is more evidence to support the idea that eccentric preservation with aging is related to noncontractile and structural properties intrinsic to the muscle (40,47). Some authors suggest that accumulation of connective tissue in the muscles with age increases passive stiffness, which in turn could enhance resistance and offer a mechanical advantage during lengthening actions (20,47). On the muscle fiber level, the preserved ability to improve force after a quick active stretch, which in turn increases the instantaneous stiffness, would also contribute to the maintenance of eccentric strength in the elderly (40,47).
In addition to age-related changes in muscle mass and strength (29), Hortobágyi et al. (16) observed that healthy older adults perform activities of daily living (ADLs) near their maximal torque capabilities, suggesting that the difficulty presented by older subjects during ADLs may be due more to working at a higher level of effort relative to their maximum capability than to the absolute functional demands imposed by the task. During stair descent, for example, the knee and ankle of the stance leg perform a large amount of negative work while the swing leg steps down (9). At the end of the stair descent, the large knee flexion causes the center of this joint to move forward and, consequently, the ground reaction force tends to flex the knee. This fact augments the demand on the knee extensor muscles, which respond by increasing the eccentric contraction (46). Recently, Samuel et al. (49) showed that level and stair walking placed high demands on the knee extensors in older adults, leaving little reserve capacity for them to lead to unexpected circumstances. Considering the great demand imposed on the lower limb (9,46,49) and the high prevalence of fall during descending stairs (53), the torque generated in the lower limbs seems to be critical for safe stair descent in older individuals (44).
Based on the studies discussed above, it seems that eccentric torque-producing capacity has an important role in the maintenance of the physical functioning in the elderly. In this respect, studying the torque-angle relationship through a functional range of motion, crucial to perform some ADL (chair rise, stair, and level walking), would provide important information for the rehabilitation and geriatric fields. Thus, the aim of this investigation was to compare the effects of age on isokinetic performance and torque production through a functional range of motion of knee flexion-extension of healthy men.
Materials and Methods
Experimental Approach to the Problem
The maximal torque and torque-producing capacity in a functional range of motion were assessed by an isokinetic dynamometer (Biodex Multi Joint System III; Biodex Medical System, Inc., Shirley, NY, USA). All subjects were subjected to concentric and eccentric knee extension and flexion at 60 and 120°·s−1. These velocities were chosen because fast-velocity eccentric exercise causes greater muscle damage than slow-velocity exercise (4). Also, it has been previously reported that these velocities presented very good reliability for isokinetic knee extension and flexion testing in the elderly (13). Considering that the knee joint range of motion used during many ADLs (sit and stand from a standard chair, stair and level walking) does not exceed 90–100° knee flexion (48) and the maximum knee joint movement while descending stairs occurs between 30 and 80° knee flexion (44), the range of 30–90° knee flexion (0° = full extension) was chosen and referred to as a functional range of motion in this study.
All subjects were evaluated at the same time of the day to consider circadian influence on physiological variables. The experiments were carried out in a climate-controlled room (22–23° C) with relative air humidity of 50–60%. Each subject was instructed to avoid caffeine and alcoholic beverages and to avoid moderate-to-heavy exercise on the day before the protocols were run. Before beginning the test on each experimental day, the subjects were interviewed and examined to confirm good health and whether they had sufficient sleep on the previous night.
Sixteen older men (mean age: 62.7 ± 2.5 years, age range: 60–68 years, height: 1.68 ± 0.05 cm, weight: 73.6 ± 7.7 kg, and body mass index: 26.13 ± 2.2 kg·m−2) and 11 young men (mean age: 24.2 ± 2.9 years, age range: 18–29 years, height: 1.79 ± 0.07 m, weight: 81.3 ± 4.4 kg, and body mass index: 25.3 ± 1.0 kg·m−2) volunteered to participate in this study. All subjects were in good health based on a clinical and physical examination and laboratory tests. The exclusion criteria included currently smoking, the presence of cardiovascular, musculoskeletal and neurologic diseases, the use of any medications, or participation in a regular strength training program for at least 6 months before the study. All subjects were informed about the experimental procedures and signed an informed consent form approved by the Institution's Ethics Committee to participate in the study (Protocol No.: 218/2006).
To ensure a good performance and a valid test (coefficient of variance ≤15%), all subjects were subjected at least to 1 familiarization session before the testing protocol. During familiarization, subjects practiced trials of both concentric and eccentric exercise. The subjects were subjected to the testing protocol at least 1 week apart from the familiarization session to ensure adequate recovery.
Before testing, each subject performed a light 3-minute warm-up on a cycle ergometer followed by quadriceps and hamstring muscle stretching as in a previously published study (30). The subject was then seated in the dynamometer and stabilized with pelvis, chest, and thigh straps, as recommend by the manufacturer. All subjects were subjected to 4 different isokinetic exercises as follows: (a) concentric contraction at 60°·s−1, (b) concentric contraction at 120°·s−1, (c) eccentric contraction at 60°·s−1, and (d) eccentric contraction at 120°·s−1. To avoid the influence of fatigue on performance, the order of the isokinetic exercises was randomly applied to each subject. They then performed 3 sets of 5–7 maximal repetitions of knee flexion-extension movement for each isokinetic exercise described above. During the maximal effort trials, the subjects were motivated with loud and consistent verbal encouragement. The trials were classified by the coefficient of variance. After this, the trial with the highest torque values between the 2 with lower coefficient of variance was used for all analysis. Because the angular velocity was not maintained at the extremities of the movement (i.e., 30 and 90° of knee flexion), the torque was calculated from 35 to 85°. The term “muscle length,” used hereafter, was preferred rather than “joint angle” for clarity in the presentation and discussion of the results. Therefore, a range between 35 and 45° knee joint angle corresponded to shortened for the extensor muscles and stretched for flexor muscles, 50–70° was considered the intermediate length for both muscle groups, and 75–85° corresponded to stretched for the extensor muscles and shortened for the flexor muscles.
The calculation of sample size was based on the results of previous studies (30,34,37,51,52). A sample size of 11 subjects in each group was needed to detect differences of 50 N·m in the primary outcome (i.e., eccentric peak torque values), assuming a standard deviation of 40 N·m, a power of 80%, and a significance level of 5%.
All statistical analyses were carried out using the statistical software package SPSS (v.20; Chicago, IL, USA) for Macintosh. The parametricity of the data was determined using the Shapiro-Wilk and Levene's tests. Age, contraction type, and angular velocity effects on peak torque and optimal peak torque angle were assessed by mixed-design analysis of variance (ANOVA), where age (2 levels) was set as a between-group factor and angular velocity (2 levels) and contraction (2 levels) were set as repeated measures. Differences between groups in the torque as a function of the muscle length were also measured by mixed-design ANOVA, where age (2 levels) was set as a between-group factor and angular velocity (2 levels) and muscle length (11 levels) were set as repeated measures. Wherever the assumption of sphericity was violated, the Greenhouse-Geisser correction was used. When significant main effects were detected, comparisons using paired and independent t-tests with Bonferroni correction were carried out. All data are presented as mean (SEM), and the level of significance was set at p ≤ 0.01.
Age, Contraction Type, and Angular Velocity Effects
The older group presented lower knee extension and flexion peak torque (maximum value of torque observed during the contractions studied) than the younger group (age effect) for both concentric (extension: F(1,25) = 33.05, p < 0.001 and flexion: F(1,25) = 26.15, p < 0.001) and eccentric exercises (extension: F(1,25) = 28.29, p < 0.001 and flexion: F(1,25) = 12.31, p < 0.01) (Figure 1). Compared with the young group, the older group presented a peak torque deficit near 30% for concentric contractions (extension at 60°·s−1 = 30%, extension at 120°·s−1 = 33%, flexion at 60°·s−1 = 29%, and flexion at 120°·s−1 = 27%) and 29% for eccentric contractions (extension at 60°·s−1 = 32%, extension at 120°·s−1 = 32%, flexion at 60°·s−1 = 27% and flexion at 120°·s−1 = 24%). For both muscular groups tested, eccentric contractions generated higher peak torque than concentric contractions (contraction effect), independently of angular velocity (extension at 60°·s−1: F(1,25) = 72.25, p < 0.001; extension at 120°·s−1: F(1,25) = 205.67, p < 0.001; flexion at 60°·s−1: F(1,25) = 54.37, p < 0.001; and flexion at 120°·s−1: F(1,25) = 207.28, p < 0.001) (Figure 1). Concentric peak torque for knee flexion and extension was lower at 120°·s−1 than at 60°·s−1 for both groups (angular velocity effect, extension: F(1,25) = 141.42, p < 0.001 and flexion: F(1,25) = 57.43, p < 0.001). Unlike concentric contraction, eccentric peak torque was not affected by velocity (Figure 1). The angle of knee extension and flexion at which peak torque occurred differed between concentric and eccentric exercises (contraction effect) for both angular velocities tested (extension at 60°·s−1: F(1,25) = 10.33, p < 0.01; extension at 120°·s−1: F(1,25) = 31.58; flexion at 60°·s−1: F(1,25) = 9.622, p < 0.01; and flexion at 120°·s−1: F(1,25) = 13.48, p < 0.01). In the older group, the peak torque for eccentric knee extension occurred at a lower muscle length than in the young group (age effect, F(1,25) = 16.06, p < 0.001) (Figure 1).
Torque Vs. Muscle Length
Torque values as a function of muscle length are presented in Figure 2. In all contractions tested, the older group maintained lower extension (concentric: F(1,25) = 33.55, p < 0.001 and eccentric: F(1,25) = 38.11, p < 0.001) and flexion torques (concentric: F(1,25) = 25.53, p < 0.001 and eccentric: F(1,25) = 21.64, p < 0.001) during movement compared with the young group. As observed for peak torque, a significant main effect of angular velocity was only found for concentric contractions (extension: F(1,25) = 142.94, p < 0.001 and flexion: F(1,25) = 57.17, p < 0.001) but not for eccentric contractions. A significant main effect of muscle length was observed for both concentric (extension: F(2,52) = 160.96, p < 0.001 and flexion: F(2,54) = 78.01, p < 0.001) and eccentric contractions (extension: F(2,39) = 115.85, p < 0.001 and flexion: F(2,61) = 60.96, p < 0.001), which was expected considering the force-length relationship (i.e., force production is lower at either extremity of muscle length). Concentric contraction at 60°·s−1 generated higher torques than concentric contraction at 120°·s−1 over the range of motion tested (angular velocity and muscle length interaction effect, extension: F(3,87) = 24.98, p < 0.001 and flexion: F(4,100) = 19.79, p < 0.001). Eccentric knee extension was the only exercise tested that showed an interaction effect between age and muscle length (F(2,39) = 17.39, p < 0.001), suggesting a different behavior of the eccentric knee extension torque between groups, when accounting for muscle length (Figure 2). Compared with the young group, the eccentric knee extension torque was 22–56% lower in the older group, with the deficits being lower in shortened (22–27%) muscle lengths and higher in stretched (33–56%) muscle lengths. However, deficits in concentric knee extension torque remained more constant during the movement (26–36%).
This study showed that peak torque values were lower in older than in young subjects, independent of contraction type. The older group presented similar peak torque deficits for both concentric (∼30%) and eccentric (∼29%) exercises. As expected, eccentric contractions generated higher peak torque than concentric contractions, independent of age. When accounting for muscle length, torque-producing capacity during eccentric knee extension contraction differed between groups. In a more stretched position, the eccentric knee extension torque of the older group presented a different pattern, which resulted in a great torque deficit (33–56%) compared with the young group.
Although there is strong evidence that concentric strength is affected more by aging than eccentric strength (17,38,39,54), this is not a consensus view (28). In most studies, the concentric peak torque of older subjects ranges from 30 to 55% less than younger subjects, vs. a 20–38% deficit for eccentric peak torque (17,38,39,54). Even considering the differences among the studies in terms of subject characteristics and methodological approaches, some mechanisms have been proposed to explain the age-related differences between concentric and eccentric strength (40,47) as follows.
Age-related changes in the central neural command result in impaired agonist activation and increased antagonist coactivation. These neurologic changes could contribute to greater deficits in isometric and concentric strength in the elderly, because the influence of agonist and antagonist activity on eccentric force generation seems to be much lower (11,22). However, as the exact mechanism underlying the unique neural modulation of eccentric contractions is unknown (10), the role of the neural mechanism on eccentric preservation in the elderly needs to be further studied (10). For example, the degree to which the aging process affects voluntary activation is unclear and might differ between muscle groups (6). Although muscular activation seems to be equal in both young and older men for the knee extensors (24), the opposite results have been shown for ankle dorsiflexors (7). In addition, Klass (21) found no differences in the voluntary activation level for isometric, concentric, and eccentric contractions between young and older adults. The authors concluded that deficits during concentric and isometric contractions of the ankle dorsiflexors in advanced age cannot be explained by impaired voluntary activation and also suggested that age-related mechanisms that preserve force in eccentric contractions appeared to be located at the muscular level.
Changes in collagen and elastin structures over the years might contribute to increased passive muscle stiffness (20). Considering that skeletal muscle-tendon unit acts as a spring, absorbing elastic strain energy during eccentric contractions, it is possible that increased passive stiffness improves the capacity to generate passive work during this type of muscle contraction (21,47). At the muscle fiber level, some authors suggested that eccentric strength preservation with age is related to an augmentation in force production by each cross-bridge during this type of contraction. In addition to the maintenance of recruitment of weakly bound cross-bridges into a strongly bound state, a specific characteristic of eccentric contraction, the slowing of some steps of the cross-bridge cycle may also be involved in relative eccentric strength preservation at an older age (35).
The degree to which eccentric strength is reported to be preserved differs in the literature, which could be partly explained by differences in normalization methods, velocities tested, and the sex and age of the participants (28,38,47,54). For example, Poulin et al. (38) observed that eccentric knee torque was 20–22% lower in older men than younger men, whereas deficits in concentric knee torque ranged between 31 and 32%. In addition, the age-related preservation of eccentric strength seems to be more evident in women than in men (28,47,54). However, Lindle et al. (28) reported no significant preservation of eccentric torque in a large cohort (654 subjects of both sexes) covering a broad age range (20–93 years). Their study showed almost identical declines in concentric (33%) and eccentric (31%) strength in older men, whereas the difference between concentric (35%) and eccentric (22%) loss was greater, although not significant, in older women.
In this study, the older group presented lower peak torques than the younger group, independent of contraction type, which is also in accordance with a recent study by Power et al. (41). It is important to note that eccentric peak torque deficits observed here are similar to previous studies (28,41,54), suggesting that similarity between the 2 contractions studied occurred because concentric strength was not affected so much as reported by others (54). As muscle mass loss accelerates after the age of 65–70 years, it is possible that the older subjects studied here were not old enough to show significant differences between concentric and eccentric torques (18,28,29). The low angular velocities used may also have contributed to our results, because eccentric torque production capacity is not affected by increasing velocity (3), as also confirmed in this study. So, it is quite possible that differences between concentric and eccentric also increase as a function of angular velocity, enhancing the effects of aging on shortening contractions.
Although the present data showed similar age-related deficits in eccentric and concentric peak torque of knee extensors and flexors muscle groups, the ability to maintain the eccentric extension torque in more stretched positions seems impaired in the older group. During eccentric knee extension, it was also observed that the peak torque occurred at shortened muscle length in the older group compared with the young. The present findings agree in part with those of Power et al. (41) who, in a study designed to evaluate age-related changes in residual force enhancement, found that the optimal peak torque angle during eccentric contraction occurred at shortened muscle length in the older group, besides similar torque-length relationship (normalized by peak torque) between young and older groups. In this study, both young and older groups experienced a similar level of residual force enhancement, contradicting previous findings of the same group (42) that showed an increased force enhancement in older men, which was also correlated with eccentric strength maintenance of the ankle dorsiflexors. As previously suggested by Lanza et al. (26), it is possible that age-related changes in muscular performance differ between muscle groups in which the knee extensor muscles seem more affected by age than others.
Considering that eccentric muscle contractions occur during many ADLs (9), eccentric strength deficits could contribute to reductions in the functional capacity of the older people and also reduce their ability to deal with high demand environments, as explained below. It is well established that the ability to perform the ADLs declines with increasing age (50). Besides the contributions of age-related changes in cardiovascular and musculoskeletal systems to physical functioning (5), Hortobágyi et al. (16) suggested that older adults execute the ADLs at a higher level of effort relative to their maximum capability, explaining in part the decline in ADLs performance. Furthermore, the reduction in the physiological reserves could increase the demand placed on the lower limb during the ADLs, reducing the ability of older adults to deal with unexpected circumstances (49). During stair negotiation, Samuel et al. (49) showed that the demand on knee extensors exceeds the maximal isometric capacity of older adults by 3% in stair ascent and 20% in stair descent phases. It is important to note that in the end of the descent phase (when lowering the body to the next step), the large knee flexion causes the center of the knee to move forward and, consequently, the ground reaction force tends to flex the knee (46). This fact augments the demand on the knee extensor muscles, which respond by increasing the eccentric contraction. In addition, the demand imposed on the lower limb during stair climbing is also influenced by stair inclinations. Riener et al. (46) observed that joint ranges and maximum flexion angles increased with increasing staircase slope. Moreover, peak knee moment values increased concomitantly with inclination during both ascent (10.6%) and descent (18.4%). So, deficits in the eccentric knee extension strength, mainly in more stretched muscle length (deficits in knee eccentric extensor torque of the older group were over 33% compared with the young group), may contribute to increased risk of falling during stair descent at older age, especially when frail elderly individuals deal with high-demand environments.
Further studies are needed to determine possible mechanisms involved in the impaired capacity to maintain the eccentric extensor torque in stretched muscle length, observed in the older group. So, the absence of other similar studies in the literature only permits us to pose some suppositions to explain our findings. Considering the underlying mechanisms related to eccentric strength preservation with aging discussed above (11,21,23,27,35,47), it is hard to believe that the deficit in the eccentric torque observed here originates only in the muscle. However, it is important to note that passive muscle stiffness is regulated by components other than the connective tissue (12). Reeves and Narici (43), for example, showed that muscle fascicle behaved quasi-isometrically during eccentric contraction, suggesting that the series elastic components (e.g., tendons and cross-bridges) act as a mechanical buffer during active lengthening, and the elongation seems to occur at the expense of the tendon. It is possible that the interaction between muscle and tendon during eccentric contraction allows the muscle to work in a more favorable region of the force-length relationship (2). Thus, the tendon properties can directly affect fascicle behavior (14) and, consequently, force production (31).
Besides the contradictory results on the effects of aging on tendon properties, current research supports the view that tendon stiffness decreases with advancing age (25,33). Using imaging ultrasound, Narici et al. (33) showed “in vivo” that tendons of older subjects were approximately 15% more compliant than those of younger subjects. Similarly, Karamanidis and Arampatzis (19) demonstrated that aging results in reduced stiffness of the quadriceps femoris tendon and aponeurosis. In addition to the age-related increase in tendon compliance (19,33), some authors suggest that older subjects use tendon elasticity less efficiently than younger individuals (15). Thus, it is possible that the muscle-tendon interaction of older subjects might be impaired, mainly in the stretched muscle length.
Finally, there are some limitations that should be acknowledged and addressed regarding this study. The older subjects studied here were not very old and were independent, thus the deficits found in the eccentric torques probably have low influence on their functional capacity. Although kinetic and kinematic analysis allows the evaluation of joint moments during ADLs, the exact eccentric torques produced during these activities are unknown. So, it is difficult to determine to what extent the eccentric knee extension deficit observed in this study may influence ADLs performance capacity in the elderly, especially while descending stairs. The influence of other factors in our results cannot also be discarded. As muscle activation reduces with increasing angular velocity for both concentric and eccentric contraction (8), it is possible that neural control has more influence in force production during slow velocities, such as used in this study (i.e., reflex adjustments in the recruitment and firing rates are more likely to occur if the contraction lasted long) (36). Moreover, our experimental design only permits us to make suppositions about the mechanisms involved in the preservation of eccentric strength with aging and why older subjects had an impaired capacity to produce eccentric knee extensor torque when the muscle was in a stretched position.
In summary, the results of this investigation suggest that, in older healthy subjects, eccentric knee extension torques seem to be dependent on the muscle length. At the stretched muscle length, the capacity to generate extension eccentric torque was impaired in the older subjects, which may have a great impact on ADLs such as descending stairs. More studies are needed to assess the mechanisms involved in eccentric strength preservation with aging and its relationship with muscle length, especially in the frail elderly.
Age-related changes in muscle mass and strength have a great impact on mobility and independence in the elderly. The relative eccentric strength preservation with aging is well accepted in the literature. It is important to note that the majority of the studies supporting this concept are based on the maximum peak torque values. However, our results showed that healthy older adults have a great deficit in the eccentric knee extension torque in stretched muscle length, contributing to a more functional and applicable perspective on the age-related decline in muscle strength and its evaluation. So, we believe that our findings should be useful for strength and conditioning professionals working with elderly people, because the information about the influence of muscle length on the eccentric strength production provided here can be incorporated into the strength conditioning and fall prevention programs for this population.
The authors are grateful for financial support provided by CAPES and CNPq. The authors declare no conflict of interest. Jim Hesson of AcademicEnglishSolutions.com revised the English.
1. Andersen JL. Muscle fibre type adaptation in the elderly human muscle. Scand J Med Sci Sports 13: 40–47, 2003.
2. Bobbert MF. Dependence of human squat jump performance on the series elastic compliance of the triceps surae: A simulation study. J Exp Biol 204: 533–542, 2001.
3. Carney KR, Brown LE, Coburn JW, Spiering BA, Bottaro M. Eccentric torque–velocity and power–velocity relationships in men and women. Eur J Sport Sci 12: 139–144, 2012.
4. Chapman D, Newton M, Sacco P, Nosaka K. Greater muscle damage induced by fast versus slow velocity eccentric exercise. Int J Sports Med 27: 591–598, 2006.
5. Chodzko-Zajko WJ, Proctor DN, Fiatarone Singh MA, Minson CT, Nigg CR, Salem GJ, Skinner JS. Exercise and physical activity for older adults. Med Sci Sports Exerc 41: 1510–1530, 2009.
6. Clark BC, Taylor JL. Age-related changes in motor cortical properties and voluntary activation of skeletal muscle. Curr Aging
Sci 4: 192–199, 2011.
7. Connelly DM, Rice CL, Roos MR, Vandervoort AA. Motor unit firing rates and contractile properties in tibialis anterior of young and old men. J Appl Physiol (1985) 87: 843–852, 1999.
8. Connelly DM, Vandervoort AA. Effects of isokinetic strength training on concentric and eccentric torque development in the ankle dorsiflexors of older adults. J Gerontol A Biol Sci Med Sci 55: B465–B472, 2000.
9. DeVita P, Helseth J, Hortobágyi T. Muscles do more positive than negative work in human locomotion. J Exp Biol 210: 3361–3373, 2007.
10. Duchateau J, Baudry S. Insights into the neural control of eccentric contractions. J Appl Physiol (1985) 116: 1418–1425, 2014.
11. Duchateau J, Enoka RM. Neural control of shortening and lengthening contractions: Influence of task constraints. J Physiol 586: 5853–5864, 2008.
12. Gajdosik RL. Passive extensibility of skeletal muscle: Review of the literature with clinical implications. Clin Biomech (Bristol, Avon) 16: 87–101, 2001.
13. Hartmann A, Knols R, Murer K, de Bruin ED. Reproducibility of an isokinetic strength-testing protocol of the knee and ankle in older adults. Gerontology 55: 259–268, 2009.
14. Hicks KM, Onambele-Pearson GL, Winwood K, Morse CI. Gender differences in fascicular lengthening during eccentric contractions: The role of the patella tendon stiffness. Acta Physiol (Oxf) 209: 235–244, 2013.
15. Hoffrén M, Ishikawa M, Komi PV. Age-related neuromuscular function during drop jumps. J Appl Physiol (1985) 103: 1276–1283, 2007.
16. Hortobágyi T, Mizelle C, Beam S, DeVita P. Old adults perform activities of daily living near their maximal capabilities. J Gerontol A Biol Sci Med Sci 58: M453–M460, 2003.
17. Hortobágyi T, Zheng D, Weidner M, Lambert NJ, Westbrook S, Houmard JA. The influence of aging
on muscle strength and muscle fiber characteristics with special reference to eccentric strength
. J Gerontol A Biol Sci Med Sci 50: B399–B406, 1995.
18. Janssen I, Heymsfield SB, Wang ZM, Ross R. Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol (1985) 89: 81–88, 2000.
19. Karamanidis K, Arampatzis A. Mechanical and morphological properties of human quadriceps femoris and triceps surae muscle-tendon unit in relation to aging
and running. J Biomech 39: 406–417, 2006.
20. Kent-Braun JA, Ng AV, Young K. Skeletal muscle contractile and noncontractile components in young and older women and men. J Appl Physiol (1985) 88: 662–668, 2000.
21. Klass M. Aging
does not affect voluntary activation of the ankle dorsiflexors during isometric, concentric, and eccentric contractions. J Appl Physiol (1985) 99: 31–38, 2005.
22. Klass M, Baudry S, Duchateau J. Voluntary activation during maximal contraction with advancing age: A brief review. Eur J Appl Physiol 100: 543–551, 2006.
23. Klass M, Baudry S, Duchateau J. Age-related decline in rate of torque development is accompanied by lower maximal motor unit discharge frequency during fast contractions. J Appl Physiol (1985) 104: 739–746, 2008.
24. Knight CA, Kamen G. Adaptations in muscular activation of the knee extensor muscles with strength training in young and older adults. J Electromyogr Kinesiol 11: 405–412, 2001.
25. Lang T, Streeper T, Cawthon P, Baldwin K, Taaffe DR, Harris TB. Sarcopenia: Etiology, clinical consequences, intervention, and assessment. Osteoporos Int 21: 543–559, 2010.
26. Lanza IR, Towse TF, Caldwell GE, Wigmore DM, Kent-Braun JA. Effects of age on human muscle torque, velocity, and power in two muscle groups. J Appl Physiol (1985) 95: 2361–2369, 2003.
27. Larsson L, Li X, Frontera WR. Effects of aging
on shortening velocity and myosin isoform composition in single human skeletal muscle cells. Am J Physiol 272: C638–C649, 1997.
28. Lindle RS, Metter EJ, Lynch NA, Fleg JL, Fozard JL, Tobin J, Roy TA, Hurley BF. Age and gender comparisons of muscle strength in 654 women and men aged 20-93 yr. J Appl Physiol (1985) 83: 1581–1587, 1997.
29. Macaluso A, De Vito G. Muscle strength, power and adaptations to resistance training in older people. Eur J Appl Physiol 91: 450–472, 2004.
30. Melo RC, Quitério RJ, Takahashi ACM, Silva E, Martins LEB, Catai AM. High eccentric strength
training reduces heart rate variability in healthy older men. Br J Sports Med 42: 59–63, 2008.
31. Muraoka T. Elastic properties of human Achilles tendon are correlated to muscle strength. J Appl Physiol (1985) 99: 665–669, 2005.
32. Narici MV, Maffulli N. Sarcopenia: Characteristics, mechanisms and functional significance. Br Med Bull 95: 139–159, 2010.
33. Narici MV, Maffulli N, Maganaris CN. Ageing of human muscles and tendons. Disabil Rehabil 30: 1548–1554, 2008.
34. Nogueira FRD, Libardi CA, Nosaka K, Vechin FC, Cavaglieri CR, Chacon-Mikahil MPT. Comparison in responses to maximal eccentric exercise between elbow flexors and knee extensors of older adults. J Sci Med Sport 17: 91–95, 2014.
35. Ochala J, Dorer DJ, Frontera WR, Krivickas LS. Single skeletal muscle fiber behavior after a quick stretch in young and older men: A possible explanation of the relative preservation of eccentric force in old age. Pflugers Arch 452: 464–470, 2006.
36. Onambele GNL, Bruce SA, Woledge RC. Effects of voluntary activation level on force exerted by human adductor pollicis muscle during rapid stretches. Pflugers Arch 448: 457–461, 2004.
37. Overend TJ, Versteegh TH, Thompson E, Birmingham TB, Vandervoort AA. Cardiovascular stress associated with concentric and eccentric isokinetic exercise
in young and older adults. J Gerontol A Biol Sci Med Sci 55: B177–B182, 2000.
38. Poulin MJ, Vandervoort AA, Paterson DH, Kramer JF, Cunningham DA. Eccentric and concentric torques of knee and elbow extension in young and older men. Can J Sport Sci 17: 3–7, 1992.
39. Pousson M, Lepers R, Van Hoecke J. Changes in isokinetic torque and muscular activity of elbow flexors muscles with age. Exp Gerontol 36: 1687–1698, 2001.
40. Power GA, Dalton BH, Rice CL. Human neuromuscular structure and function in old age: A brief review. J Sport Health Sci 2: 215–226, 2013.
41. Power GA, Makrakos DP, Rice CL, Vandervoort AA. Enhanced force production in old age is not a far stretch: An investigation of residual force enhancement and muscle architecture. Physiol Rep 1: e00004, 2013.
42. Power GA, Rice CL, Vandervoort AA. Increased residual force enhancement in older adults is associated with a maintenance of eccentric strength
. PLoS One 7: e48044, 2012.
43. Reeves ND, Narici MV. Behavior of human muscle fascicles during shortening and lengthening contractions in vivo. J Appl Physiol (1985) 95: 1090–1096, 2003.
44. Reeves ND, Spanjaard M, Mohagheghi AA, Baltzopoulos V, Maganaris CN. The demands of stair descent relative to maximum capacities in elderly and young adults. J Electromyogr Kinesiol 18: 218–227, 2008.
45. Reid KF, Naumova EN, Carabello RJ, Phillips EM, Fielding RA. Lower extremity muscle mass predicts functional performance in mobility-limited elders. J Nutr Health Aging
12: 493–498, 2008.
46. Riener R, Rabuffetti M, Frigo C. Stair ascent and descent at different inclinations. Gait Posture 15: 32–44, 2002.
47. Roig M, Macintyre DL, Eng JJ, Narici MV, Maganaris CN, Reid WD. Preservation of eccentric strength
in older adults: Evidence, mechanisms and implications for training and rehabilitation. Exp Gerontol 45: 400–409, 2010.
48. Rowe PJ, Myles CM, Walker C, Nutton R. Knee joint kinematics in gait and other functional activities measured using flexible electrogoniometry: How much knee motion is sufficient for normal daily life? Gait Posture 12: 143–155, 2000.
49. Samuel D, Rowe P, Nicol A. The functional demand (FD) placed on the knee and hip of older adults during everyday activities. Arch Gerontol Geriatr 57: 192–197, 2013.
50. Sjölund B-M, Wimo A, Qiu C, Engström M, von Strauss E. Time trends in prevalence of activities of daily living (ADL) disability and survival: Comparing two populations (aged 78+ years) living in a rural area in Sweden. Arch Gerontol Geriatr 58: 370–375, 2014.
51. Symons TB, Vandervoort AA, Rice CL, Overend TJ, Marsh GD. Reliability of a single-session isokinetic and isometric strength measurement protocol in older men. J Gerontol A Biol Sci Med Sci 60: 114–119, 2005.
52. Symons TB, Vandervoort AA, Rice CL, Overend TJ, Marsh GD. Effects of maximal isometric and isokinetic resistance training on strength and functional mobility in older adults. J Gerontol A Biol Sci Med Sci 60: 777–781, 2005.
53. Tinetti ME, Speechley M, Ginter SF. Risk factors for falls among elderly persons living in the community. N Engl J Med 319: 1701–1707, 1988.
54. Vandervoort AA, Kramer JF, Wharram ER. Eccentric knee strength of elderly females. J Gerontol 45: B125–B128, 1990.