Abstract
Background
Aging promotes neuromuscular loss, significantly reducing muscle strength. The magnitude of loss of strength seems to be different between the limbs, probably because of differences in activities of daily living (ADL). Therefore, the present study compared the muscle strength of the elbow flexors and knee extensors in younger (n = 7, mean age 23.3 ± 1.2 years) and older (n = 5, mean age 61.8 ± 2.6 years) men matched by ADL level.
Methods
The study participants performed maximal concentric, isometric, and eccentric contractions of the elbow flexors and knee extensors using an isokinetic dynamometer following a crossover study design. Changes in the dependent variables were compared using mixed model analysis (limb versus age).
Results
The main results demonstrated that concentric, eccentric, and mean contraction torques for knee extensors were significantly (P < 0.05) higher for younger men than for elderly men. On the other hand, no statistically significant difference (P > 0.05) was found in concentric, isometric, eccentric, and mean torques for elbow flexors between younger and older individuals.
Conclusion
These results show that elbow flexors maintain better strength than knee extensors through aging, even when comparing individuals with similar ADL levels.
Introduction
Advancing age is associated with loss of muscle mass and function.Citation1–Citation4 The amount of reduced muscle mass is replaced by an infiltration of conjunctive tissue and fat.Citation2 In addition, aging jeopardizes action potential conduction velocity in muscle fibersCitation5 and efficiency in recruitment of motor units.Citation6 Impaired neuromuscular function as a result of advancing age contributes to significantly reduced muscle strength.Citation7 Interestingly, it has been shown that this reduction in muscle strength through aging is greater for the lower limb muscles than for those of the upper limb.Citation8–Citation10 However, to date, the reasons for these differences in limb susceptibility to loss of strength due to aging are not well understood.
Lynch et alCitation9 studied 703 volunteers aged 19–93 years and, using peak concentric and eccentric torques, demonstrated that aging promoted greater loss of muscle strength in the lower limbs than in the upper limbs. These authors speculated that there is greater disuse of leg muscles than of arm muscles with increasing age.Citation9 Similarly, Frontera et al,Citation8 in a 12-year longitudinal study, documented that the mean annual reduction in strength was in the range of 1.4%–2.5%, with elbow flexors having a mean loss of isokinetic strength at 60° per second of 16.4% (annual loss approximately 1.4%) and knee extensors having significantly greater loss of strength (23.7%, annual loss about 2.0%). Candow and ChilibeckCitation10 also analyzed elbow flexor and knee extensor torques (among other muscle groups) in young and elderly subjects, and found that strength in the lower body muscles is more affected by age than that of the upper body muscles. The extent to which activities of daily living (ADL) may have influenced the results of these studies is unknown,Citation8,Citation9 or whether the younger subjects performed more moderate and strenuous intensity exercise than the older subjects.Citation10
It has been shown clearly that ADL and physical activity level can influence the magnitude of muscle strength.Citation11,Citation12 Therefore, the ADL level may possibly explain the greater loss of strength in lower limb muscles than in upper limb muscles with aging. However, none of the above-mentioned studiesCitation8–Citation10 matched participants (young and old) for their ADL level. Equalizing the ADL level, it is possible that age-related loss of strength is similar between elbow flexors and knee extensors.
Therefore, the present study compared maximal strength of the elbow flexors and knee extensors (using maximal concentric, eccentric, isometric, and mean torques) in younger and older men with the same level of ADL. It was hypothesized that young individuals would have more strength in the elbow flexors and knee extensors than their elderly counterparts, and that matching ADL level to age, similar losses of muscle strength could be expected for elbow flexors and knee extensors.
Materials and methods
Subjects
The number of participants required for the present study was determined by sample size estimation utilizing G*Power (version 3.0.10)Citation13 based on data from a previous studyCitation9 that analyzed the strength of elbow flexors and knee extensors in young and old individuals. The estimation was based on a difference in loss of strength of about 6% between elbow flexors and knee extensors with aging. We used an α level of 0.05 and a power (1 − β) of 0.95. Calculations demonstrated that a total of eight individuals were needed to test our hypothesis.
We recruited 12 healthy men (seven younger and five older subjects) for the present study, and their characteristics are shown in . The inclusion criteria were: no cardiac disease, arterial hypertension, or diabetes mellitus; no participation in a resistance training program for at least 12 months prior to the study; and no musculoskeletal injuries of the upper or lower extremities. All volunteers were evaluated by a medical doctor and were considered to be able to perform maximal strength tests. All participants provided their informed consent and the study was approved by the ethics committee at our institution. The study was conducted in conformity with the policy statement regarding use of human subjects by the Declaration of Helsinki.
Table 1 Participant characteristics and Baecke score
The subjects were asked and reminded not to perform any physical exercise for at least 96 hours before and during the study period. All volunteers were evaluated for their physical activity level using the Baecke questionnaire.Citation14 This questionnaire evaluates the ADL level for the past 12 months, taking into account occupational physical activities, physical exercises practiced during leisure time, and physical activities practiced during leisure time and locomotion (excluding physical exercise).Citation15 Limb circumference was measured by an experienced investigator using a constant-tension tape (with 1 mm resolution) at the mid portion of each limb (at the middle point between the acromion and the olecranon for elbow flexors, and at the middle point between the inguinal ligament and the top edge of the patella for knee extensors). The circumference of the elbow flexors and knee extensors was defined as the perpendicular perimeter of the longitudinal axis of the humerus and femur, respectively. The investigator measured the circumference three times for each limb while the volunteer stood with arms relaxed beside the body. The average of three measurements for elbow flexors and knee extensors was used as the circumference value.
Experimental protocol
All volunteers were familiarized with the study equipment and tests before collection of data. Three days later, the strength protocols for elbow flexors and knee extensors were performed in a random and counterbalanced order between ages and limbs, with two weeks of rest between the elbow flexor and knee extensor tests according to a crossover design. All tests were performed using the nondominant limb (determined by the writing hand and leg used to kick a ball with precisionCitation16) in an isokinetic dynamometer (Biodex System 4 Pro, Biodex Medical Systems, Shirley, NY, USA) to standardize the velocity of execution and range of motion and also to quantify the peak torque. A warm-up consisting of two sets of three repetitions (concentric/concentric) at 90° per second was performed before all procedures on the isokinetic dynamometer. The volunteers were positioned in the dynamometer chair and fixed by straps at the chest, lap, and leg to limit extraneous movement. For elbow flexor exercise, the shoulder joint was positioned at 90° of flexion and 0° of abduction, and the forearm was supinated, holding the lever arm of the dynamometer. For knee extensor exercise, the hip joint was positioned at 85° of flexion with the arms folded in front of the chest.Citation17 The dynamometer rotation axis was visually aligned with the elbow joint or knee joint for the elbow flexor and knee extensor exercises, respectively. All subjects were verbally encouraged to achieve maximum strength at each strength test (concentric, isometric, and eccentric), and the maximum torque developed was calculated by the software of the isokinetic dynamometer.
Concentric torque
To quantify maximum concentric contraction torque, the volunteers performed a set of four maximum concentric contractions at 60° per second for the elbow flexors and the knee extensors.Citation17 The range of motion of each contraction was 60° (20°–80° for elbow flexors; 90°–30° for knee extensors). Anatomical zero for both limbs was considered to be 0°.Citation17 This procedure was selected because older subjects could have a reduced range of motion,Citation18 so they might not reach the 120° range of motion, as other study with young subjects applied.Citation19 Even with a 90° range of motion, previous study have shown that the elderly may have problems reaching a full range of motion.Citation20 The maximum contraction torque for four concentric contractions was used for further analysis.
Isometric torque
Maximum isometric contraction torque was achieved by three maximal isometric attempts at 50° for the elbow flexors and 60° for the knee extensors,Citation17 with 60 seconds of rest between attempts. The maximum isometric contraction torque of three attempts was used for further analysis.
Eccentric torque
A set of six maximum eccentric repetitions at 90° per second in the isokinetic dynamometer was used to quantify the maximum eccentric contraction torque of the elbow flexors and knee extensors. The range of motion was the same as for the concentric test, ie, 60° (80°–20° for elbow flexors and 30°–90° for knee extensors). Anatomical zero for both limbs was considered to be 0°.Citation17 Immediately before each maximum eccentric contraction, the volunteers performed one second of isometric contraction at the initial position to warrant maximal eccentric contraction since the beginning of the movement. The movement return was realized passively at 5° per second, resulting in 12 seconds of rest between contractions. Maximum eccentric contraction torque developed at the set was used for further analysis.
Mean torque
The arithmetic mean for the concentric, isometric, and eccentric contraction torques was calculated for each limb (elbow flexors and knee extensors) and each age group (young and old) in order to establish the general strength of each limb. The results are presented as mean torque values.
Reliability
The reliability of the strength measures was established comparing two baseline measures separated by three days. Our calculations showed a high intraclass correlation coefficient (0.995–0.998) and a low coefficient of variation (3.4%–5.4%).
Statistical analysis
Independent-samples t-tests were used to compare the anthropometric parameters, subject age, and ADL level calculated by the Baecke questionnaire. Levene’s test was used to evaluate the equality of variances in independent samples. To compare the changes in dependent variables between muscle strength and age, we used a mixed model analysis, with muscle groups (elbow flexors and knee extensors) and age (young and old) as fixed factors and subjects as a random factor. When a significant F was obtained, the Tukey post hoc test was used to identify any significant differences. Statistical significance was set at P < 0.05. All data are presented as the mean ± standard error of the mean.
Results
Concentric torque
It was demonstrated significant main effects for muscle, age, and interaction of muscle versus age (P < 0.001, P = 0.004, and P = 0.004, respectively). Concentric torque for the knee extensors in the young and old age groups was significantly greater than that of the elbow flexors (P < 0.001 and P = 0.001, respectively). Concentric torque for the elbow flexors was similar between the age groups (younger, 43.3 ± 2.6 Nm (Newton*meter); older, 45.3 ± 6.9 Nm; P = 0.93). However, for concentric torque of the knee extensors, the older group showed significantly lower values than the younger group (156.2 ± 15.4 Nm versus 208.3 ± 10.4 Nm, respectively, P = 0.002, ).
Figure 1 Concentric, isometric, and eccentric contraction torques for elbow flexors (EF) and knee extensors (KE) in younger and older men.
Isometric torque
Analysis of isometric torque for elbow flexors and knee extensors in the younger and older age groups showed only a significant main muscle effect (P < 0.001; age, P = 0.889 and interaction of muscle versus age, P = 0.616). The isometric torque of the knee extensors for the young and elderly (210.9 ± 11.1 Nm; 203.4 ± 9.2 Nm, respectively) was significantly (P < 0.001 for both) greater than that of elbow flexors (57.2 ± 4.5 Nm and 60.3 ± 9.0 Nm, respectively).
Eccentric torque
Mixed-model analysis demonstrated significant effects of muscle, age, and interaction of muscle versus age (P < 0.001, P = 0.043. and P = 0.02, respectively). Eccentric torque for the knee extensors in both age groups was significantly greater than for elbow flexors in younger and older men (P < 0.001 for both). shows that the eccentric torque for elbow flexors in the younger and older age groups was similar (62.0 ± 3.8 Nm and 63.8 ± 8.9 Nm, respectively, P = 0.972); however, eccentric torque for knee extensors in the younger men (278.7 ± 16.1 Nm) was significantly (P = 0.008) greater than that in the older men (268.9 ± 10.1 Nm).
Mean torque
Significant effects of muscle, age, and an interaction of muscle versus age (P < 0.001, P = 0.023, and P = 0.038, respectively) were found for mean torque. Mean torque for the knee extensors was significantly greater than that for elbow flexors in both young and older men (P < 0.001 for both). shows that mean torque for elbow flexors was similar between the age groups (young, 54.2 ± 3.5 Nm; old, 56.4 ± 8.2 Nm; P = 0.931). However, mean torque for knee extensors in older men (209.5 ± 10.9 Nm) was significantly (P = 0.01) lower than that in young men (232.6 ± 11.2 Nm, ).
Figure 2 Mean contraction torques for elbow flexors (EF) and knee extensors (KE) in younger and older men.
Discussion
The present study investigated the hypothesis that, matching the ADL level of younger and older men, loss of muscle strength due to aging should be similar between lower and upper limb muscles. However, the results show that elbow flexor strength did not vary with advancing aging, but that knee extensors had significantly less strength in older men than in young men. Thus, our results document that even with a similar ADL level; the upper limbs maintain better muscle strength than do the lower limbs with aging.
Participant characteristics did not differ between the age groups (), with the younger and older groups having the same body mass, height, body mass index, elbow flexor and knee extensor circumferences, and Baecke scores. This is important, and highlights the need for standardization with regard to the main comparison in the present study, ie, elbow flexor and knee extensor strength between younger and older subjects with the same level of ADL. Analyzing the muscle strength data (ie, concentric, isometric, eccentric, and mean contraction torques), it was found that younger and older men showed similar elbow flexor strength. This is consistent with previous research in menCitation18,Citation20,Citation21 and womenCitation22 demonstrating that younger and older individuals do not differ in isometric strength of the elbow flexors. With regard to eccentric strength in the elbow flexors, Lynch et alCitation9 documented results similar to those of the present study, ie, no difference between eccentric strength of the elbow flexors in younger (20–29 years) and older women (60–79 years). When the same comparison was made between younger (about 19 years) and middle-aged men (about 48 years), also no difference in isometric strength of the elbow flexors was found.Citation23 However, conflicting results have been found in other studies showing significant loss of elbow flexor strength in men as a result of aging.Citation8,Citation9 These contradictory results might reflect different ADL levels in the age groups included in these studies.Citation8,Citation9 It is possible that the similar levels of ADL in the age groups included in the present study could have been responsible for maintenance of elbow flexor strength with aging.
In our study, analysis of concentric, eccentric, and mean contraction torques of the knee extensors revealed important differences between the age groups, ie, older men showed lower concentric, eccentric, and mean contraction torques than young men. Only isometric strength of the knee extensors showed no difference between the age groups. The method used to analyze isometric torque in this work (testing at a single fixed angle, ie, 50° for the elbow flexors and 60° for the knee extensors) might have influenced the results. It has been suggested that the pennation angle decreases with aging;Citation9 such that aging significantly affects muscle architecture.Citation24 Muscle architecture, eg, pennation angle and fascicle length, can change the optimum angle of peak torque.Citation25 Therefore, isometric torques at fixed angles might not precisely reflect peak torques in younger or older subjects. Accordingly, it has been suggested that age deficits in isometric torque are angle-specific.Citation26 On the other hand, peak eccentric and concentric contraction torques measured dynamically show lower values in older men than in younger men. Altogether, from the results presented (ie, for concentric, eccentric, and mean contraction torque), it is reasonable to suggest that aging promotes major losses in knee extensor strength even with the same level of ADL. The present study demonstrated about 25.0% of loss in concentric strength of the knee extensors (measure at 60° per second) in older men compared with younger men. A similar degree of loss was reported by Candow and Chilibeck,Citation10 who also measured peak isokinetic concentric torque at 60° per second for the knee extensors and found an approximate torque loss of 25.3% comparing younger and older subjects. Lynch et alCitation9 observed a difference of approximately 23.3% in concentric strength of the knee extensors (at 30° per second) for younger (20–29 years) and older men (60–69 years). Also analyzing concentric strength of the knee extensors at 60° per second, Frontera et alCitation8 showed a loss with aging of about 2.0% per year. These authors demonstrated that, over a period of 12 years, men had a loss of concentric strength in the knee extensors of about 23.7%. Also consistent with the present study, Balagopal et alCitation27 documented that isokinetic strength of the quadriceps (the main muscle group involved in knee extension) and strength of the knee extensors measured by one repetition maximum, decreased significantly with age (23 years versus 77 years). In addition, Ploutz-Snyder et alCitation28 demonstrated that concentric and eccentric strength in the knee extensors were lower in older than in younger women.
Interestingly, the present study demonstrated that knee extensor strength in younger men was significantly greater than that in older men, but that elbow flexor strength did not differ between the age groups, indicating that aging modulates muscle strength of the lower and upper limbs in different ways. Similar results have been found in previous studies, demonstrating that with aging, lower limb muscles (eg, knee extensors) show greater loss of muscle strength than the upper limbs (eg, elbow flexors).Citation8–Citation10,Citation29–Citation31 Most of the previous studies have considered the level of ADL relevant when interpreting their results. The novelty of the present study is that the same results were found even when matching older and younger men for their level of ADL. It has been proposed that aging may induce more inherent morphological changes in the knee extensors than in the elbow flexors,Citation29 ie, leg muscles might be more susceptible to loss of lean massCitation32,Citation33 and might suffer major changes in muscle contractile properties, connective tissue, and muscle architecture (eg, pennation angle) than arm muscles.Citation9 Further, it is possible that use of the legs in ADL is reduced to a greater extent than use of arm muscles.Citation8 One limitation of the present study is that our Baecke questionnaire on ADL does not segregate frequency and intensity of daily use of the arms and legs. In fact, this has been proposed beforeCitation10,Citation34 and might also explain the results of the present study, in that older individuals could supplement weaker lower body movements (such as rising from a chair) with contraction of the upper limb muscles. Future studies investigating the level and intensity of ADL in the arms and legs separately would be helpful to clarify these speculations.
The results of the present study are relevant in the context of physical training and health. For example, strength training programs should be structured with greater emphasis on gains in lower limb strength, given that the strength of the knee extensor muscles predicts levels of dependency and survival.Citation12,Citation35
We conclude that even when comparing younger and older men with similar levels of daily life activities, the elbow flexors maintain better strength than the knee extensors.
Acknowledgment
The authors extend their thanks to all volunteers who participated in this study.
Disclosure
The authors declare no financial support or relationship that might pose any conflicts of interest in this work.
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