Journal of Applied Physiology AJP: Regulatory, Integrative and Comparative Physiology
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J Appl Physiol 102: 942-948, 2007. First published November 22, 2006; doi:10.1152/japplphysiol.00067.2006
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Muscle size, neuromuscular activation, and rapid force characteristics in elderly men and women: effects of unilateral long-term disuse due to hip-osteoarthritis

C. Suetta,1 P. Aagaard,1,2 S. P. Magnusson,1 L. L. Andersen,3 S. Sipilä,4 A. Rosted,5 A. K. Jakobsen,1 B. Duus,6 and M. Kjaer1

1Institute of Sports Medicine, Bispebjerg Hospital, University of Copenhagen, 2Institute of Sports Science and Clinical Biomechanics, University of Southern Denmark, and 3National Institute of Occupational Health, Copenhagen, Denmark; 4Department of Health Sciences, University of Jyväskylä, Jyväskylä, Finland; and Departments of 5Radiology and 6Orthopedics, Bispebjerg Hospital, University of Copenhagen, Copenhagen, Denmark

Submitted 19 January 2006 ; accepted in final form 10 November 2006


   ABSTRACT
TOP
 ABSTRACT
METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Substantial evidence exists for the age-related decline in muscle strength and neural function, but the effect of long-term disuse in the elderly is largely unexplored. The present study examined the effect of unilateral long-term limb disuse on maximal voluntary quadriceps contraction (MVC), lean quadriceps muscle cross-sectional area (LCSA), contractile rate of force development (RFD, {Delta}force/{Delta}time), impulse ({int}force dt), muscle activation deficit (interpolated twitch technique), maximal neuromuscular activity [electromyogram (EMG)], and antagonist muscle coactivation in elderly men (M: 60–86 yr; n = 19) and women (W: 60–86 yr; n = 20) with unilateral chronic hip-osteoarthritis. Both sides were examined to compare the effect of long-term decreased activity on the affected (AF) leg with the unaffected (UN) side. AF had a significant lower MVC (W: 20%; M: 20%), LCSA (W: 8%; M: 10%), contractile RFD (W: 17–26%; M: 15–24%), impulse (W: 10–19%, M: 19–20%), maximal EMG amplitude (W: 22–25%, M: 22–28%), and an increased muscle activation deficit (–18%) compared with UN. Furthermore, women were less strong (AF: 40%; UN: 39%), had less muscle mass (AF: 33%; UN: 34%), and had a lower RFD (AF: 38–50%; UN: 41–48%) compared with men. Similarly, maximum EMG amplitude was smaller for both agonists (AF: 51–63%; UN: 35–61%) and antagonist (AF: 49–64%; UN: 36–56%) muscles in women compared with men. However, when MVC and RFD were normalized to LCSA, there were no differences between genders. The present data demonstrate that disuse leads to a marked loss of muscle strength and muscle mass in elderly individuals. Furthermore, the data indicate that neuromuscular activation and contractile RFD are more affected by long-term disuse than maximal muscle strength, which may increase the future risk for falls.

aging; rate of force development; neural activity; muscle activation

IT IS WELL KNOWN FROM ANIMAL and human studies that a chronic reduction in neuromuscular activity results in marked muscle atrophy (4, 28), reduced muscle strength (2, 33), and diminished neural drive to muscle fibers (9). For people older than 45 yr of age, >33% suffer from joint pain, and osteoarthritis (OA) has been shown to be the most common cause of inactivity and long-term disability in people aged ≥65 yr (12). However, most of the current knowledge with respect to the effects of inactivity and immobilization on neuromuscular function is based on animal data (2, 8) or on studies performed on healthy young individuals (4, 28). This is contrasted by the fact that the elderly population more often undergoes periods of immobilization and disuse, not only due to joint pain, but also due to a higher degree of comorbidity and hospitalization (32). Studies in healthy young adults have demonstrated that immobilization leads to rapid decreases in maximal muscle strength, muscle mass, and neural activation (4, 19); however, recent studies indicate that skeletal muscle in aged animals and humans is more vulnerable to muscle unloading than that in young individuals (8, 41). Furthermore, recent data from Yasuda et al. (43) show that there might be a gender-specific response to unloading, as evidenced by a more pronounced decrease in specific strength in young women compared with young men after 14 days of unilateral limb immobilization. Yet the lack of investigations into the effect of unloading or disuse in elderly humans makes it difficult to distinguish the extent with which reductions in muscle mass or reduced physical activity level are responsible for the observed decrease in muscle force production with aging.

With increasing age, human skeletal muscle morphology and function decay, which is dramatically evident by the sixth decade and onward (20, 27). This deterioration is known to be caused to a great extent by morphological changes, like decreased muscle mass, both due to a loss of muscle fibers and a decrease in the individual muscle fiber size (29). However, studies comparing groups of young and old human subjects indicate that the loss in muscle force cannot be entirely explained by these quantitative changes (35, 42). Accordingly, it has been suggested that the loss of muscle strength in aging may exceed that of the morphological changes, resulting in a decreased muscle quality in the elderly (7, 42), although it has not been a universal finding (17). In addition, aging is also associated with neurological changes, which affects maximum voluntary force production (34), as well as the capacity for rapid muscle force production; i.e., contractile rate of force development (RFD) (42). The ability to develop force rapidly (i.e., RFD) seems to be an important muscle mechanical performance parameter in aging subjects in several tasks of daily life, such as walking and attempting to avoid falls (13, 39). At the same time, reduced muscle strength in older people, for example after a period of immobilization or disuse, may be associated with muscle atrophy (6), a lowered ability to produce force rapidly, and thereby an increased risk of falling (13).

Reduced contractile RFD has been demonstrated in elderly compared with young individuals of both genders (5, 42). However, to what extent reductions in muscle mass or size, suppression in voluntary muscle activation, elevated coactivation of antagonist muscles, or a general reduction in the physical activity level is responsible for the decrease in muscle strength in the elderly remains unclear. It, therefore, appears of paramount importance to gain a better understanding of how prolonged disuse affects mechanical muscle characteristics and neuromuscular activation in the elderly and, furthermore, try to ascertain what effects can be attributed to activity level and the aging process, respectively. In the present study, individuals who suffered from diagnosed hip OA, with symptoms lasting >1 yr, were studied. The fact that OA was unilateral allowed for a comparison between the affected (AF) lower limb and the contralateral unaffected (UN) side.

The aim of the present study was to investigate the side-to-side difference in maximal muscle strength, muscle size, rapid force characteristics, and neuromuscular activation in elderly individuals with long-term unilateral OA. It was hypothesized that maximal muscle strength and muscle mass would be reduced on the AF side compared with the UN side, and furthermore that rapid force characteristics and neuromuscular activation parameters would be affected by the chronic disuse to a greater extent than muscle mass and strength.


   METHODS
TOP
 ABSTRACT
 METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Subjects.   Thirty-nine elderly individuals, 20 women (W; age range 60–86 yr) and 19 men (M; age range 60–79 yr), volunteered to participate in the study. Eligibility criteria included age >60 yr and primary unilateral hip-OA clinical and radiological, verified according to Kellgren and Lawrence grade >2 (36). All subjects had symptoms lasting >1 yr and were scheduled for primary unilateral hip-replacement surgery at Bispebjerg University Hospital, Copenhagen, Denmark. A careful physical examination was obtained by a physician to exclude subjects with cardiopulmonary, neurological, or cognitive problems. All subjects ambulated with a walking aid; however, lower limb problems other than hip-OA and/or pain during testing, as measured on a visual analog scale (VAS, 0–10), was considered an exclusion criteria (VAS > 3). The study was approved by the ethics committee of Copenhagen and Frederiksberg, in accordance with the Helsinki declaration, and written, informed consent was obtained from all participants.

Maximal isometric muscle strength and RFD.   Maximal muscle strength was measured as the maximum voluntary isometric knee extension torque [maximum voluntary contraction (MVC)] exerted in an isokinetic dynamometer (KinCom; Kinetic Communicator, Chattecx, Chattanooga, TN), according to procedures described in detail elsewhere (39). Individual setting of the seat, backrest, dynamometer head, and lever arm length was registered, so identical subject positioning was ensured throughout the study. All torque values were corrected for the effect of gravity (1). Subjects were carefully instructed to contract as fast and hard as possible. Visual feedback was provided to the subjects as real-time display of the dynamometer force output on a computer screen (22). After a standardized warm-up, including dynamic and submaximal isometric contractions, subjects performed three maximal isometric knee extensions of 3-s duration, each separated by a 45-s pause, and after 3-min rest three maximal isometric knee flexions were performed in a similar manner. All MVCs were performed at a knee joint angle of 60° (0° = full knee extension). The trial with the highest maximal knee joint torque for each direction was selected for further analyses (1, 39). All measurements were performed for both legs separately and were preceded by a familiarization session (2–4 days before test 1). On all test occasions, UN was tested first to minimize subjects' discomfort with the procedure. Contractile RFD was defined as the average slope of the torque-time curve in the initial contraction phase ({Delta}force/{Delta}time) at 0–30, 0–50, 0–100, and 0–200 ms relative to the onset of contraction (1, 39). Onset of contraction was defined as the instant where torque increased 3.5 N·m above the resting baseline level (corresponding to ~2% of the peak torque). Contractile impulse was determined as the area under the torque-time curve ({int}torque dt) in the same time intervals (1). Normalized RFD was calculated as RFD divided by CSA.

Estimation of muscle activation.   To evaluate the ability to activate the quadriceps muscle of AF as well as the UN, an electrically evoked muscle twitch was superimposed onto a maximal voluntary muscle contraction. The subjects were seated in an upright position with the thigh placed horizontally and knee flexed at a right angle. A steel cuff was strapped around the lower leg, 1 in. above the malleoli. The cuff was connected via a rigid steel bar to a strain-gauge load cell (Bofors KRG-4, Bofors), which was connected to a preamplifier (BK15, Nobel Elektronik) and an amplifier (Gould 5900, Gould, Valley View, OH). The strain-gauge force signal was sampled at 1,000 Hz. Each test procedure began with the determination of the maximal twitch response. For evoking twitch responses from the knee extensors, percutaneous surface stimulation electrodes (Bioflex, model PE3590) were placed over the distal and proximal muscle belly of the quadriceps femoris. Contractions were evoked using single square-wave pulses of 0.1-ms duration delivered by a direct current stimulator (Digitimer Electronics, model DS7). Before the MVC, a maximal baseline twitch (Pt) was defined where a stepwise increment in current delivered every 30 s resulted in no further increases in force. Following a short rest, three voluntary contractions (with 2-min rest between each contraction) were performed with the addition of supramaximal single pulses. The subject was asked to push as hard and fast as possible and maintain the contraction for 3–5 s. The force recording of each contraction was viewed on a computer screen in real time, which enabled stimuli to be triggered manually on top of a MVC. The height of the superimposed twitch during this peak portion was measured, and an estimate of muscle activation was then calculated as follows: activation (%) = [1 – (Pts/Pt)] x 100, where Pts is the force from the superimposed twitch, and Pt is the force from the resting twitch.

Electromyogram recordings.   After careful preparation of the skin by shaving and cleaning with alcohol, pairs of surface electrodes (Medicotest Q-10-A, 20-mm interelectrode distance) were placed over the belly of vastus lateralis (VL), vastus medialis (VM), rectus femoris (RF), biceps femoris (BF), and semitendinosus (ST). The electromyogram (EMG) electrodes were connected directly to small custom-built preamplifiers, and the EMG signals were led through shielded wires to custom-built amplifiers with a frequency response of 10–10,000 Hz and common mode rejection ratio exceeding 100 dB (1). EMG and dynamometer strain-gauge signals were synchronously sampled at a 1,000-Hz analog-to-digital conversion rate using an external analog-to-digital converter (dt 2801-A, Data Translation, Marlboro, MA). Subsequently, during later offline analysis, EMG signals were digitally high-pass filtered with a fourth-order, zero-lag Butterworth filter with a 5-Hz cut-off frequency, followed by a moving symmetric root-mean-square filter with a time constant of 50 ms (1). Maximum EMG amplitude of the root-mean-square-filtered signal was identified within the entire contraction phase, which included a 70-ms time period prior (1, 39). The magnitude of antagonist muscle cocontraction was calculated by dividing maximal antagonist hamstring EMG by maximal agonist hamstring EMG measured during maximal knee flexion.

Quadriceps muscle composition.   Cross-sectional area (CSA) of the quadriceps femoris muscle was obtained by computed tomography (CT; Picker 5000) with an image matrix of 512 x 512 pixels, slice thickness of 8 mm, and scanning time of 5 s. All CSA scans were obtained at the midpoint between the great trochanter and lateral joint line of the knee. CT scans were analyzed using software developed for cross-sectional CT image analysis (Geanie 2.1, BonAlyse Oy, Jyväskylä, Finland). Quadriceps muscles were encircled manually to exclude subcutaneous fat and other muscles from the region of interest. Lean tissue cross-sectional area (LCSA) and inter- and intramuscular fat CSAs were measured using CT density limits for fat and lean tissue (37). Mean attenuation [Hounsfield unit (HU)] of the lean tissue area was also recorded. Each scan was blinded for both leg and gender, and the coefficient of variation between two consecutive measurements is <1% for lean tissue HU and 1–2% for LCSA (37).

Statistical analysis.   Statistical analyses were performed by using GraphPad Prism 4.0 (GraphPad Software, San Diego, CA, 2003). Data from maximal muscle strength measurements (MVC), quadriceps muscle composition (total CSA, LCSA, muscle density), MVC/LCSA, muscle activation (interpolated twitch technique), neural activity (EMG), and hamstring cocontraction were analyzed by a two-factor ANOVA, with gender and side as factors. Data on contractile RFD, contractile impulse, normalized RFD, and muscle activation (interpolated twitch technique) were analyzed with paired Student's t-test. Data are presented as mean values ± SE, and a P value of <0.05 was considered significant.


   RESULTS
TOP
 ABSTRACT
 METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Subjects.   Men and women were similar in age (M: 69 ± 1 yr, W: 70 ± 1 yr) and body mass index (M: 29 ± 1 kg/m2 vs. W: 27 ± 1 kg/m2), and men were significant taller (M: 173 ± 2 cm, W: 163 ± 1 cm) and had a greater body mass than women (M: 85.8 ± 3.6 kg, W: 71.5 ± 3.6 kg).

Quadriceps muscle composition.   Total quadriceps muscle CSA (TCSA), quadriceps muscle LCSA, and mean HU were significant smaller on AF compared with UN, both for men (TCSA: –7.5%, LCSA: –9.5%, HU: –7.0%) and women (TCSA: –6.0%, LCSA: –7.9%, HU: –8.7%) (Table 1). Furthermore, women showed lower CSA compared with men, both in AF (TCSA: –32.0%, LCSA: –33.3%) and UN (TCSA: –33.0%, LCSA: –34.1%). However, there was no gender difference with respect to muscle density expressed in HU on either of the two sides (Table 1).


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  		Table 1. Quadriceps muscle composition

 
Maximal isometric strength.   Maximal voluntary muscle strength was lower on AF compared with UN in both men (AF: 149.6 ± 8.8 N·m, UN: 186.5 ± 9.1 N·m, reduced 19.8%) and women (AF: 90.6 ± 4.8 N·m, UN: 113.4 ± 6.2 N·m, reduced 20.3%) (Fig. 1). Compared with men, the elderly women had 39.5% less maximal isometric strength on AF and 39.2% on UN (Fig. 1). The self-reported pain score (VAS) obtained during the strength measurements was 1.2 ± 0.3 for men and 1.1 ± 0.2 for women for AF. None of the subjects reported any pain during testing of UN.


Figure 1
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  		Fig. 1. Maximal isometric strength. Maximal isometric strength is shown for the affected (AF) vs. the unaffected (UN) leg for women and men. Data are presented as means ± SE. *P < 0.05, AF significantly different from UN. #P < 0.05, women significantly different from men. Solid bars: AF leg; shaded bars: UN leg.

 
Force per unit LCSA.   When MVC was expressed relative to LCSA (MVC/LCSA), there was a difference between AF and UN for both men (AF: 2.58 ± 0.14 N·m·cm–2, UN: 2.96 ± 0.13 N·m·cm–2, reduced 12.8%, P < 0.05) and women (AF: 2.34 ± 0.14 N·m·cm–2, UN: 2.73 ± 0.12 N·m·cm–2, reduced 14.3%, P < 0.05) (Fig. 2). There was no gender difference for specific strength on either side.


Figure 2
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  		Fig. 2. Force per unit lean muscle cross-sectional area (LCSA) [maximum voluntary contraction (MVC)/LCSA]. Force per unit LCSA is shown for the AF leg vs. the UN leg for women and men. Data are presented as means ± SE. *P < 0.05, AF leg significantly different from UN leg. No difference was observed between women and men. Solid bars: AF leg; shaded bars: UN leg.

 
Contractile RFD and impulse.   In men, contractile RFD was reduced (P < 0.05) on AF compared with UN for peak RFD (15%), and at 0–50 ms (24%), 0–100 ms (19%), and 0–200 ms (18%) (Fig. 3). In women, contractile RFD was lower on AF compared with UN for peak RFD (26%) and at 0–50 ms (18%) and 0–100 ms (17%) (Fig. 3). When RFD was normalized to LCSA (RFD/LCSA), AF of the men showed reduced RFD compared with UN at 0–100 ms (13%) and 200 ms (–18%), and for the women, normalized peak RFD (15%) AF remained reduced (Table 2). Similarly, contractile impulse was reduced on AF compared with UN in both men and women at 0–50 ms (M: 19% vs. W: 18%), 0–100 ms (M: 20% vs. W: 19%), and 0–200 ms (M: 19% vs. W: 10%) (Table 2).


Figure 3
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  		Fig. 3. Contractile rate of force development (RFD). Contractile RFD of the AF leg vs. the UN leg for men and women is shown. RFD ({Delta}force/{Delta}time) was calculated in time intervals of 0–30, 50, 100, and 200 ms. Data are presented as means ± SE. *P < 0.05, AF leg significantly different from UN leg. Notice the difference in absolute values between men and women, which was statistically significant for all parameters, P < 0.05.

 

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  		Table 2. Contractile rate of force development and impulse

 
In addition, significant differences emerged between genders (Table 2). Thus, compared with men, the women demonstrated smaller absolute RFD values for peak RFD (AF: 50%; UN: 43%) and at 0–30 ms (AF: 42%; UN: 48%), 0–50 ms (AF: 45%; UN: 48%), 0–100 ms (AF: 42%; UN: 43%), and 0–200 ms (AF: 38%; UN: 41%) (Table 2). However, no statistically significant differences between genders were found when RFD was normalized to LCSA. Furthermore, contractile impulse was reduced in women compared with men at 0–30 ms (AF: 29%; UN: 32%), at 0–50 ms (AF: 40%; UN: 41%), at 0–100 ms (AF: 42%; UN: 42%), and at 0–200 ms (AF: 39%; UN: 41%) (Table 2).

Neuromuscular activity (EMG).   During maximal voluntary knee extension contraction, maximum EMG amplitude of the VL and VM muscle was lower on AF compared with UN in men (VL: 28%; VM: 22%), while there was no side difference for RF (Table 3). Similarly, there was no side difference for the ST or BF muscles during knee flexor MVC (Table 3). In women, maximum EMG amplitude of the RF was lower (RF: 22%) on AF compared with UN, while there was no side difference for VL and VM (Table 3). During maximal voluntary knee flexion, BF was lower on AF compared with UN (BF: 25%). There was no side difference in the magnitude of hamstring antagonist cocontraction for men or women (Fig. 4). Compared with male subjects, maximum EMG amplitude during MVC in women was significantly smaller for VL (AF: 58%; UN: 61%), VM (AF: 51%; UN: 35%), and RF (AF: 63%; UN: 50%) (Table 3). Correspondingly, during isometric knee flexion, the maximum EMG amplitude of the BF (AF: 49%; UN: 36%) and ST (AF: 64%; UN: 58%) muscles was lower in women compared with men (Table 3). During isometric knee extension, men showed lower antagonist cocontraction in the ST muscle of AF compared with women (M: 0.13 ± 0.03 vs. W: 0.25 ± 0.04), whereas there was no difference in magnitude of cocontraction in ST (M: 0.15 ± 0.02 vs. W: 0.19 ± 0.02) on UN or in BF on AF (M: 0.37 ± 0.07 vs. W: 0.44 ± 0.05) or UN (M: 0.27 ± 0.03 vs. W: 0.35 ± 0.04) (Fig. 4).


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  		Table 3. Maximum EMG amplitude of the quadriceps and hamstring muscles

 

Figure 4
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  		Fig. 4. Hamstring cocontraction. Hamstring antagonist cocontraction during quadriceps MVC in the AF leg and the UN leg for men and women, respectively, is shown. Data are presented as means ± SE. #P < 0.05, men significantly different from women. Solid bars: AF leg; shaded bars: UN leg.

 
Muscle activation.   In a subgroup of 17 subjects (12 men and 5 women), the magnitude of muscle activation was estimated by the superimposed twitch technique. Due to the limited number of subjects, it was not possible to make gender comparisons. There was a remarkable, insufficient muscle activation on both sides (AF: 57.6 ± 5.0%, UN: 70.7 ± 3.6%), although this deficit was more pronounced on AF (–18.5%, P < 0.01).


   DISCUSSION
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The present study investigated maximal muscle strength, muscle size, neural activation, and rapid muscle force characteristics in elderly individuals with unilateral hip-OA. The data demonstrate a marked side-to-side difference with decreased muscle mass, maximal muscle strength, neuromuscular activation, and rapid muscle force characteristics (RFD, impulse) on the arthritic side compared with the healthy side.

Despite the fact that elderly persons are particularly exposed to periods of immobilization and disuse, either due to joint pain or hospitalization (12), most of the current knowledge concerning the effect of immobilization on skeletal muscle is based on studies in healthy young individuals (4, 28). Furthermore, comparisons between young and old subjects per se make it difficult to ascertain what effects can be attributed to activity level and the aging process, respectively. The model of disuse in the present study clearly presents some limitations; however, we believe that comparing two legs with a different activity level in the same person can provide new information as to how decreased activity affects muscle function in elderly individuals. One of the limitations of the study was that the exact activity level was not obtained. It could be speculated that subjects with unilateral hip-OA would favor the healthy limb and thereby spare the AF side. Another possibility could be that the overall activity level of these persons would decrease because of joint pain; however, since both MVC and CSA of UN side in these subjects were similar to those of healthy age-matched subjects measured in our laboratory (10, 26) and in other studies (14, 17), we were probably observing a combination of increased loading on the UN side and an overall decreased activity level. Furthermore, supporting our hypothesis that long-term disuse has a similar effect on muscle mass as a standardized period of limb immobilization, both men and women had smaller quadriceps muscle CSA (LCSA) on AF compared with UN (M: –9.5%, W: –7.9%), which is comparable to 4 wk of bed rest in young healthy individuals (28).

Although muscle mass is an important determinant of strength loss with age and immobilization, it is clearly not the sole factor involved in this process. In addition, changes in structural components, such as increased intramuscular fat and connective tissue (29), likely contributes to the strength loss with aging. Previous studies have demonstrated a reduced specific strength (MVC/LCSA) in elderly compared with young individuals (31, 42), although not all studies have been able to detect such a difference (23). While women in the present study had a lower MVC on both sides (AF: –39.5%, UN: –39.2%) compared with men, no gender difference could be detected when corrected for lean muscle tissue (MVC/LCSA), which is in agreement with earlier investigations (30, 42). However, MVC/LCSA on AF was lower compared with UN in both genders (M: –13.7%, W: –11.6%), in line with D'Antona et al. (6), who demonstrated decreased specific force in single muscle fibers of the quadriceps muscle in immobilized elderly individuals, indicating a disuse-related decrease in muscle quality on the immobilized side. These results are supported by Klitgaard et al. (25), who demonstrated that sedentary elderly subjects showed a decline in specific strength, whereas elderly subjects with a long-term history of strength or endurance training demonstrated specific strength that was equal to those of young subjects. Compared with the side-to-side difference in MVC (M: –19.8%, W: –20.3%), the decline in specific strength (M: –12.8%, W: –14.3%) with inactivity and disuse suggests that ~60–70% (M: 12.8/19.8 = 65%, W: 14.3/20.3 = 70%) of this difference may be explained by qualitative changes within the muscle tissue; i.e., changes in neuromuscular activation, fiber type or muscle architectural components, and/or increased ratio of noncontractile to contractile tissue (6, 31).

To the best of the author's knowledge, no other study has investigated rapid muscle force characteristics in the elderly after a period of disuse or immobilization. In healthy elderly individuals, it has been demonstrated that the ability to develop force rapidly (i.e., contractile RFD) is reduced compared with that in young individuals of both genders (5, 42), likely due to the decreased number and size of type II muscle fibers in the elderly (29) and an increased amount of noncontractile intramuscular tissue (29). However, when RFD is normalized relative to MVC, a difference between young and old subjects is not a universal finding (5, 40). In the present study, absolute contractile RFD was lower on AF compared with UN in both men (~18%) and women (~25%). Notably, AF remained reduced compared with UN when RFD was normalized to LCSA in women (W: –17.6%), indicating qualitative changes with prolonged disuse. Although only rarely reported in the literature (1, 39), contractile impulse is an important strength parameter, since it reflects the specific time history of contraction by providing a measure of the accumulated area covered by the moment-time curve (1). In the present study, contractile impulse was reduced in the female subjects compared with male subjects on both the AF (28–41%) and UN (31–42%). Furthermore, contractile impulse was reduced on the AF compared with the UN in both men (19%) and women (10–19%).

In agreement with Berg et al. (4), who investigated the effect of bed rest on lower limb muscle function in young healthy individuals, there was reduced EMG response during maximal voluntary knee extensor MVC in the quadriceps muscle of AF compared with UN, in both men (VL, VM) and women (RF). These data suggest a general suppression in neuromuscular activity during maximum quadriceps contraction for men and women, indicating that the decreases in maximal isometric strength (MVC) and rapid force capacity (RFD, impulse) observed in AF were at least partially explained by changes in neuromuscular activation. However, it should be recognized that a multitude of confounding factors exist that may compromise the information that can be extracted from surface EMG data (11, 21). Thus side-to-side differences in EMG signal amplitude could also have been caused by a variety of nonneural factors, such as differences in limb fat distribution, muscle fiber size, and muscle fiber pennation angle. The amount of hamstring antagonist cocontraction was comparable to that previously reported for elderly individuals (24, 31). Notably, no difference was found in the magnitude of hamstring cocontraction between AF and UN, which suggests that the subjects were well familiarized with the test procedure. More importantly, this finding supports that the subjects did not experience pain on AF during the recording of maximal voluntary contraction strength and neuromuscular activity, since antagonist muscle coactivation is known to increase in the presence of muscle and/or joint pain (16). Notably, there was a pronounced muscle activation deficit on both sides (AF: –42.4%; UN: –29.3%), although more severe on AF (–18.5%) compared with UN. It should be noted, however, that single-twitch muscle stimulation, as used in the present study, is more susceptible to muscle fatigue than stimulation using paired twitches (15) and, furthermore, that the present resting twitches were recorded in an unpotentiated state (before contraction). Both of these factors are known to result in smaller resting twitches and thereby larger activation deficits (3, 15, 18). This does not, however, explain the difference in muscle activation observed between the AF and contralateral UN limb. Moreover, the observed AF activation deficit is very much in line with that observed by Stevens et al. (38) after 7 wk of cast immobilization in young subjects. In summary, the present study indicates that long-term limb disuse in the elderly is associated with marked decreases in maximal muscle strength, anatomical CSA of the quadriceps femoris muscle, maximal EMG amplitudes, and rapid muscle force characteristics (RFD, impulse). Furthermore, a side-to-side difference was observed in specific strength (MVC/LCSA) and normalized RFD (RFD/LCSA), which indicate that 40–70% of the observed changes with disuse may be explained by qualitative changes. The present results underline the need of effective neuromuscular rehabilitation regimes for the elderly after a period of immobilization. This need becomes particular important when considering the importance of restoring symmetry of lower limb strength and rapid muscle force capacity to avoid decremental impairments in postural balance, maximal walking speed, and other functional tasks of daily life.


   FOOTNOTES
 

Address for reprint requests and other correspondence: C. Suetta, Institute of Sports Medicine, Copenhagen, Bispebjerg Hospital, Bispebjerg Bakke 23, 2400 NV Copenhagen, Denmark (e-mail: cs08{at}bbh.hosp.dk)

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.


   REFERENCES
TOP
 ABSTRACT
 METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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