Medicine & Science in Sports & Exercise:
Basic Sciences: Original Investigations
Sex Differences in Single Muscle Fiber Power in Older Adults
KRIVICKAS, LISA S.1; FIELDING, ROGER A.2,3; MURRAY, ANGELIQUE1; CALLAHAN, DAMIEN2; JOHANSSON, ANDREAS1; DORER, DAVID J.4; FRONTERA, WALTER R.1
1Department of Physical Medicine and Rehabilitation, Spaulding Rehabilitation Hospital and Harvard Medical School, Boston, MA; 2Department of Health Sciences, Sargeant College of Health and Rehabilitation Sciences, Boston University, Boston, MA; 3Nutrition, Exercise Physiology, and Sarcopenia Laboratory, Jean Mayer USDA Human Nutrition Research Center on Aging at Tufts University, Boston, MA; and 4Biostatistics Center, Massachusetts General Hospital, Boston, MA
Address for correspondence: Lisa S. Krivickas, Spaulding Rehabilitation Hospital, 125 Nashua St., Boston, MA 02114; E-mail: firstname.lastname@example.org.
Submitted for publication December 2004.
Accepted for publication July 2005.
This work was supported by NIA grant AG-18844 and this work is based on work supported by the U.S. Department of Agriculture, under agreement No. 58-1950-4-401. Any opinions, findings, conclusion, or recommendations expressed in this publication are those of the author(s) and do not necessarily reflect the view of the U.S. Department of Agriculture.
Purpose: This study was conducted to determine whether differences in power at the single muscle fiber level contribute to sex differences in whole muscle power production in the elderly.
Methods: A total of 16 sedentary older persons (10 women, 6 men), mean age 72 yr, had percutaneous needle biopsy of musculus vastus lateralis. Chemically skinned single muscle fibers were activated with Ca2+ for maximal isometric force measurement (Po). The slack test was performed to determine maximal unloaded shortening velocity (Vo). Force–velocity and power curves were generated via a series of isotonic contractions, allowing measurement of peak power and specific power. Sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) was used to determine myosin heavy chain composition of single muscle fibers. Whole muscle strength, velocity, and power were measured for knee extension and double leg press.
Results: Men had greater whole muscle strength, power, and velocity compared with women. Studied were 274 type I and 33 type IIa single fibers. No significant sex differences were found for fiber size, Po, specific force, Vo, power, or specific power in type I or IIa fibers.
Conclusions: Single muscle fiber quality in older women is equivalent to that in older men and can not explain the differences seen in whole muscle strength, power, or function.
The ability of muscle to generate power is critical to perform activities of daily living. Power production is a function of both muscle strength and contractile speed. Loss of muscle strength with aging is a major contributor to impairment in the elderly. Recently, several investigators have suggested that loss of muscle power can have an even more deleterious effect on function than loss of strength in older individuals (2,8). Furthermore, power declines earlier in life and more severely than strength (24).
Older women tend to have greater functional impairment and a longer period of dependence before death when compared with older men (15,23). Sex-related differences in the ability of skeletal muscle to generate force and power may be largely responsible for this phenomenon (16). This is clinically relevant because leg extensor power is highly correlated with functional performance measures such as stair climbing and walking speed (1,28). In fact, leg extensor power can be a predictor of morbidity and mortality.
Previous studies have explored sex-related differences in muscle power in older adults at the whole muscle level, but few have specifically addressed this issue at the cellular level. Healthy older women produce significantly less leg extensor power than older men (1,28). Because power production is determined by both force generation and velocity of muscle contraction, it is influenced by the central nervous system when studied in vivo. The skinned single muscle fiber preparation allows study of the power-producing capacity of individual muscle cells in a fiber type–specific manner free from the influence of the central nervous system. Thus, studying power production at the cellular level in older men and women may assist in determining whether the greater power deficits seen in older women are caused primarily by central nervous system or muscle factors.
Trappe et al. (29) have studied single muscle fiber contractile properties, including power, in young and old men and women; and they did not find any sex- or age-related differences in single fiber power when normalized for cell size. In earlier separate studies of progressive resistance training in men and women (30,31), however, their data suggest that single fibers from older women generate more power than those from older men before training. Following training, power production increased in both sexes such that a significant sex difference was no longer seen (12). Thus, it remains unclear whether a sex difference in power production at the single muscle fiber level exists among older adults.
The objective of this study was to directly compare whole muscle and single muscle fiber power production in older men and women to elucidate any sex-related differences.
We studied 16 sedentary older subjects (10 women and 6 men), ranging in age from 65 to 84 yr, who demonstrated functional limitation as defined by a score of ≤9 (mean = 8.1 ± 0.2) on the Short Physical Performance Battery (SPPB) (14). The SPPB is a 12-point summary scale characterizing performance for three tests, including balance, habitual gait, and repeated chair-rise. The study was approved by the human studies committee of Boston University where the biopsies were performed, and participants gave written informed consent. Participants were eligible for the study if they were community dwelling and aged ≥65 yr. They were excluded if they had acute or terminal illness, cognitive impairment as defined by a score of 23 or below on the Folstein Mini Mental State Examination (9), suffered from symptomatic coronary artery disease, unstable congestive heart failure, or had a myocardial infarction or bone fracture in the previous 6 months. Other exclusion criteria included uncontrolled hypertension (>150/90 mm Hg) and the presence of neuromuscular disease or drugs affecting neuromuscular function. Participants meeting these preliminary qualifications were examined by a physician and had a supervised graded exercise test on a treadmill before enrollment.
Whole muscle strength, velocity, and power.
Strength, velocity, and power were tested for the left and right knee extensors (LKE and RKE) and bilateral hip extensors (DLP) using Keiser pneumatic strength training equipment (Keiser Sports Health Equipment Inc., Fresno, CA). This equipment utilizes cylinders pressurized with air to provide resistance. Actuation of the lever arm compresses air in the cylinder, while metered compression of the gas within the cylinder provides resistance. An ultrasonic system mounted on the cylinder monitors relative movement over time, allowing for the calculation of distance, velocity, and, consequently, work and power. Strength as determined by the one-repetition maximal (1RM) was measured as reported previously (7). Throughout the testing procedure, a rest period of approximately 2 min was provided between repetitions. Power and velocity were then tested after a 5-min rest. Each participant was instructed to perform a single repetition as quickly as possible through a full range of motion at a resistance equal to 40% of 1RM. This was repeated four more times for a total of five repetitions, each separated by 30 s. The highest measured velocity was recorded. External resistance was then raised to 70% 1RM, and the participant was again instructed to extend the leg as quickly as possible through five repetitions. The highest measured power was recorded. We specifically chose these two relative intensities because we have previously shown participants generate maximal power (70% 1RM) and maximal velocity (40% 1RM) under these conditions (5). Software engineered for the testing equipment calculated work and power during the concentric phase of each repetition by sampling system pressure (equivalent to force) and position 400 times per second. Average power and velocity were calculated from data collected between 5 and 95% of the concentric phase. The first and last five percent of measured range of motion are not analyzed on this equipment to minimize the effect of signal noise at the beginning and end of each movement. No significant differences were noted for measurements of strength or power between right and left legs, and data are presented for the right leg only.
Muscle biopsies and single fiber preparation.
Percutaneous biopsy specimens were taken from the vastus lateralis muscle 12–15 cm proximal to the superior pole of the patella under local anesthesia using the Bergstrom biopsy needle (3). The specimens were placed in relaxing solution (see below) at 4°C. Bundles of approximately 50 fibers were dissected free from the samples and then tied with surgical silk to glass capillary tubes at slightly stretched lengths. The fibers were chemically skinned for 24 h in relaxing solution containing 50% (v/v) glycerol at 4°C and were then stored at −20°C (19).
On each day that experiments were performed, one bundle of fibers was used, and fibers were randomly dissected from the bundle. On a typical day, experiments were performed on six fibers from the bundle, and the remainder of the tissue was discarded. Thus, for each subject, the data were derived from four or five bundles of fibers.
On the day of an experiment, the bundle of fibers was placed for 30 min in relaxing solution containing 0.5% Brij-58 (polyoxyethylene 20 cetyl ether; Sigma Chemical Co., St. Louis, MO) before mounting the fibers in an experimental apparatus, similar to the one described previously (26). A fiber segment length of approximately 1.5 mm was left exposed to the solution between connectors leading to a force transducer (Model 400A, Aurora Scientific, Ontario, Canada) and a DC torque motor (Model 308B, Aurora Scientific). The apparatus was mounted on the stage of an inverted microscope (Olympus IX70, Tokyo, Japan). While the fibers were in relaxing solution, sarcomere length was set to 2.75–2.85 μm by adjusting the overall segment length. A sarcomere length of 2.80 μm is optimal for maximal force generation (22). The segments were observed through the microscope at a magnification of 320×.
Sarcomere length, segment width, and segment length between the connectors were measured with an image analysis system (Image-Pro Plus, Media Cybernetics, Silver Spring, MD). Fiber depth was measured by recording the vertical displacement of the microscope nosepiece while focusing on the top and bottom surfaces of the fiber. The coefficient of variation for three depth measurements performed by the same observer is 3.7% (11). Fiber cross-sectional area (CSA) was calculated from the width and depth, assuming an elliptical circumference. Specific force (SF) was calculated as maximal force (Po) normalized to CSA and was corrected for the 20% swelling that is known to occur during skinning (13,26).
Relaxing and activating solutions contained (nM): 4 MgATP, 1 free Mg2+, 20 imidazole, 7 EGTA, 14.5 creatine phosphate, and sufficient KCl to adjust the ionic strength to 180 nM. The pH was adjusted to 7.0. The concentration of free Ca2+ was 10−9 M (relaxing solution) and 10−4.5 M (maximal activating solution) and was expressed as pCa (-log[Ca2+]). Immediately preceding each activation, the fiber was immersed for 10–20 s in a solution with a reduced Ca2+–EGTA buffering capacity (25). This solution is identical to the relaxing solution, except that EGTA is reduced to 0.5 mM, which results in a more rapid attainment of steady tension during subsequent activation.
Isometric contractile measurements.
Maximal unloaded shortening velocity (Vo) was measured by the slack test procedure (6,18). Fibers were activated at pCa 4.5, and once steady tension was reached, various amplitudes of slack, ranging from 7 to 13% of the fiber segment length, were rapidly introduced (within 1–2 ms) at one end of the fiber. The time required to take up the imposed slack was measured from the onset of the length step to the beginning of the tension redevelopment. For each amplitude of slack, the fiber was reextended while relaxed to minimize nonuniformity of sarcomere length. The procedure was repeated with nine slack amplitudes. A straight line was fitted to a plot of slack length versus time, using least-squares regression, and the slope of the line divided by the segment length was recorded as Vo for that fiber. Po was calculated as the difference between the total tension in activating solution (pCa 4.5) and the resting tension measured in the same segment while in the relaxing solution. All contractile measurements were carried out at 15°C.
Isotonic contractile measurements.
Force velocity curves were generated by performing a series of isotonic contractions of the muscle fiber after completion of the slack test (32). The muscle fiber was placed in activating solution, and once Po was reached, a series of three isotonic steps varying from 8 to 78% of Po was performed. Step duration was 150 ms. A custom software program, together with a data acquisition processor (Microstar Laboratories model DAP5200/526a, Bellevue, WA), were used to collect data from the force transducer and the lever arm as well as to control the lever arm's position. The data acquisition processor runs a software proportional integral derivative (PID) controller algorithm to control the lever arm so that the desired force level is maintained during each step. During each step, the velocity of muscle fiber shortening (i.e., rate of lever arm movement) required to maintain the desired force level was calculated by fitting a first degree polynomial, y(x) = kx+m, to the lever arm position signal; k is the velocity. Velocity was measured during the epoch comprising approximately the middle third of each step and was normalized by fiber segment length. Following the series of contractions, the fiber was allowed to relax. A total of six series of isotonic contractions was performed generating 18 pairs of relative force (%Po) and velocity measurements.
Velocity was plotted as a function of %Po generating a hyperbolic curve, and the Hill equation was fit to the data using an iterative nonlinear curve fitting procedure, the Levenberg–Marquardt optimization algorithm. The Hill equation states that (P+a)(V+b) = (Po+a)/b, where P = force, V = velocity, and Po = maximal isometric force. From the fitted curve, Hill constants a and b, having dimensions of force and velocity, respectively, were derived. Figure 1 shows a typical force velocity curve. The parameter a·Po−1 describes the concavity of the curve; the lower the ratio, the more concave the curve. Next, the power generated during each isotonic step, calculated as force times velocity, was plotted as a function of %Po. The fitted velocity curve was multiplied by the corresponding force points to generate a fitted power curve (Fig. 2). Peak power (μN·FL·s−1) was defined as the peak of this curve. Peak power was then normalized for fiber CSA to yield a measure of specific power (kN·m−1·FL·s−1). The %Po at which peak power occurs on the fitted power curve was also noted.
Myosin heavy chain (MyHC) composition.
After mechanical measurements, each fiber was placed in sodium dodecyl sulfate sample buffer in a plastic microfuge tube and stored at −20°C. The MyHC composition of single fibers was determined by sodium dodecyl sulfate-polyacrylamide gel electrophoresis (SDS-PAGE) (17). The acrylamide concentration was 4% (v/v) in the stacking gel and 6% in the running gel, and the gel matrix included 30% glycerol. Sample loads were kept small (equivalent to approximately 0.05 mm of fiber segment) to improve the resolution of the MyHC bands (types I, IIa, IIx). Gels were silver-stained. Proteins were identified using a combination of purified human myosins from the vastus lateralis muscle [for details and references, see Larsson and Moss (18)]. Figure 3 depicts a typical gel.
FIGURE 3Sodium dodec...Image Tools
The R statistical package (version 1.9.1; http://www.R-project.org) was used for statistical computations. A P value <0.05 was considered statistically significant.
Because the women in this study were heavier than the men and had greater body mass index (BMI), sex comparisons for whole muscle strength, power, and velocity data were performed by ANCOVA taking BMI into account.
Because of the multiple measurements taken on each participant, mixed linear models were used to analyze the data. In Tables 3 and 4, the effects for men and women are listed. These effects are weighted means of the observations. The P value is for the contrast between men and women in the model with an effect for sex and a random intercept for each individual. The standard deviations are from the model. These represent the standard deviation for multiple observations on a single individual “within SD (w-SD)” and the standard deviation for measurements of different individuals, “between SD (b-SD).” The model assumes that each subject has his or her own mean measurement, which has a normal distribution between subjects, and each measurement within a subject is also normally distributed around this mean. The P value tests the hypothesis that a difference exists in these mean measurements between male and female subjects.
The general characteristics of the subjects are presented in Table 1.
Whole muscle strength, power, and velocity.
Measures of right knee extensor and double leg press 1RM, peak velocity, and peak power are summarized in Table 2. The double leg press strength and velocity and right knee extension power were greater in men than in women, but no statistically significant difference was found between men and women for the other parameters.
Isometric contractile properties.
A total of 274 type I fibers (176 female, 98 male) and 33 type IIa fibers (21 female, 12 male) were studied. We also studied 6 type I and IIa hybrid fibers (2 female, 4 male), which were not analyzed statistically because of their small number. Thus, a mean of 19.6 single fibers per subject were studied. The number of type IIa fibers was limited because, in our experience, they are not prevalent in the musculus vastus lateralis in this elderly population. In fact, 10 of the 16 subjects had one or no type IIa fibers among the single fibers randomly selected for study. The isometric contractile properties (Po, CSA, SF, Vo) are summarized in Table 3. No significant differences between women and men were detected for type I or type IIa fibers.
Isotonic contractile properties.
Peak power, specific power, a·Po−1, and %Po for 250 type I (161 female, 89 male) and 28 type IIa fibers (16 female, 12 male) are summarized for men and women in Table 4. Of the single fibers from which isometric contractile properties were obtained, 24 failed during isotonic testing or did not generate technically adequate data and were excluded from the analysis. Type I and IIa fibers of men and women had no statistically significant differences in specific power or peak power based on sex. Likewise, no sex differences were found in a·Po−1 or %Po.
At the whole muscle level, the men in this study generated greater knee extensor and double leg press strength, power, and velocity than did the women. The major finding of this study is that, despite differences in whole muscle function, no significant sex differences were noted in single muscle fiber–specific force, Vo, power, or specific power in sedentary older men and women. Thus, single muscle fiber quality in this group of older women is equivalent to that of the older men and cannot explain the differences seen in whole muscle strength, power, or function. Our findings are important because, when combined with the similar findings of others (29), they definitively suggest a need to look beyond the contractile elements to explain sex differences in whole muscle strength and power. Single fiber power generation may be considered the basic building block for whole muscle power generation. The fact that this basic building block is no different in women than in men suggests that it may be possible to close the gender gap seen in whole muscle power by using appropriate training and nutritional interventions.
In other studies, greater sex differences in whole muscle strength and power have been reported. Compared with the men in this study, the women produced 82% as much strength with right knee extension and 83% as much strength with double leg press. They generated 68% as much power with right knee extension and 75% as much power with double leg press. In the recent work of Trappe et al. (29), knee extensor power in older women was only 50% that of older men. One explanation for this discrepancy may be that the women in this study were considerably heavier than those of Trappe (mean weight 78 vs 62 kg) and, in fact, outweigh the men in our study. We attempted to account for this by correcting for BMI in our statistical analysis. In the work of Skelton et al. (28), healthy older women aged 70–74 yr have absolute knee extensor strength that is 74% that of their male counterparts; when normalized for body weight, the strength of the women is 89% that of the men. In the same study, leg extension power of the women was 54% that of the men in absolute terms and 64% that of the men when normalized for body weight. The normalized ratios correspond well with our findings. In all of these studies, the sex difference is greater for power than for strength measurements.
In our study, we found no significant sex differences in isometric contractile properties at the cellular level. This finding differs from those of earlier work in our laboratory. In a cross-sectional study of 12 older men and 12 older women of similar age, we found that women had smaller type IIa fibers than did men (10); however, no sex differences were found in SF. In the same group of subjects, women had lower Vo than did men for both fiber types (type I: 0.70 vs 0.77 FL·s−1; type IIa: 1.51 vs 1.78 FL·s−1) (16). One explanation for the differences in these results may be related to the fitness status of the two study populations. The subjects in the earlier study were more fit, and resistance training has been shown by others to increase Vo in older men but not in older women (30,31). Thus, one might hypothesize that the men in the earlier study had increased their Vo relative to the women because they were more physically fit. Trappe et al. (29) recently reported reduced type IIa fiber size in older women, similar to our earlier work (10); as in our present study, no sex differences existed for specific force or Vo.
With respect to isotonic single muscle fiber contractile properties, we did not find any significant sex difference in power or specific power. These findings confirm those reported by Trappe et al. in the only other sex comparison of single fiber power in older adults (29).
A weakness of this study is that we are limited by a small sample size for the type IIa fibers. This difficulty also has been reported by others (29) and is not surprising because loss of fast-twitch fibers is known to occur with aging (20,21). The relatively small number of subjects is similar to that reported by others using the skinned single muscle fiber preparation, which is very labor intensive (10,29–32).
A critical question that remains to be answered is why single muscle fiber contractile function does not explain in vivo muscle function sex differences. One consideration is that power is measured differently in vivo and in vitro. The in vivo measurements are direct, whereas the in vitro measurements are derived indirectly from a force velocity curve. Different activation systems are involved in the in vivo and in vitro measurements. In vivo, muscle fibers are activated centrally by the nervous system, and a series of steps must occur before muscle fiber contraction; these steps include central activation of motor neurons, neural transmission, neuromuscular junction transmission, and excitation contraction coupling. In vitro, muscle fibers are activated by the addition of exogenous calcium without any of the previously mentioned processes occurring. In addition, a number of mechanical processes modify single fiber muscle power before it is translated into in vivo whole muscle power; force transduction must occur from the single muscle fiber to adjacent muscle fibers, tendon, and bone before joint movement occurs.
In conclusion, it appears that sex differences in muscle power in older adults are not caused by differences in the isometric or isotonic contractile properties of individual muscle fibers. The power-generating capacity of single fibers of older women is equal to that of older men. The primary factor responsible for greater power production in men appears to be greater muscle mass. Thus, the sex difference is primarily a quantitative one rather than a qualitative one. Additional contributory factors might include hormonal influences, which can affect calcium kinetics, and thus excitation contraction coupling (27), and differences in central nervous system activation strategies reducing the velocity component of power in women. During jumping movements, the principal factor reducing leg muscle power production in older women, when compared with older men, is reduced velocity according to one study (4). These additional factors that may contribute to reduced whole muscle power production in older women all require further study. Optimal muscle power–generating capacity is critical to the performance of activities of daily living in the elderly. Understanding the etiology of whole muscle power decline in older women is the first step toward developing programs to improve function and reduce impairment and dependency during old age.
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