In vivo determination of fascicle curvature in contracting human skeletal muscles

Transcription

1 J Appl Physiol 92: , In vivo determination of fascicle curvature in contracting human skeletal muscles TADASHI MURAMATSU, 1 TETSURO MURAOKA, 2 YASUO KAWAKAMI, 2 AKIRA SHIBAYAMA, 2 AND TETSUO FUKUNAGA 2 1 Institute of Physical Education, Keio University, Kohoku, Yokohama ; and 2 Laboratory of Sports Sciences, Department of Life Sciences, Graduate School of Arts and Sciences, University of Tokyo, Meguro, Tokyo , Japan Received 15 June 2001; accepted in final form 27 August 2001 Muramatsu, Tadashi, Tetsuro Muraoka, Yasuo Kawakami, Akira Shibayama, and Tetsuo Fukunaga. In vivo determination of fascicle curvature in contracting human skeletal muscles. J Appl Physiol 92: , Fascicle curvature of human medial gastrocnemius muscle (MG) was determined in vivo by ultrasonography during isometric contractions at three (distal, central, and proximal) locations (n 7) and at three ankle angles (n 7). The curvature significantly (P 0.05) increased from rest to maximum voluntary contraction (MVC) ( m 1 ). In addition, the curvature at MVC became larger in the order dorsiflexed, neutral, plantar flexed (P 0.05). Thus both contraction levels and muscle length affected the curvature. Intramuscular differences in neither the curvature nor the fascicle length were found. The direction of curving was consistent along the muscle: fascicles were concave in the proximal side. Fascicle length estimated from the pennation angle and muscle thickness, under the assumption that the fascicle was straight, was underestimated by 6%. In addition, the curvature was significantly correlated to pennation angle and muscle thickness. These findings are particularly important for understanding the mechanical functions of human skeletal muscle in vivo. medial gastrocnemius muscle; intramuscular variability THE ARCHITECTURE OF THE SKELETAL muscle has been defined as the arrangement of the fascicle (bundle of the muscle fibers) within the muscle (10, 12, 18). Knowledge of the architecture of the skeletal muscle is essential to understanding its function (force and excursion ability) (10, 18). Therefore, many studies have dealt with the architecture in animals (7, 23, 35), human cadavers (6, 34), and human in vivo (3, 13, 21, 25, 28). In many cases, muscle architecture is characterized by the length (fascicle length), the angle (pennation angle) with respect to the tendinous tissues, and the thickness of the muscle (3, 13, 21, 25, 28). Another parameter that is necessary for better understanding the architecture is the curvature (reciprocal of the radius of a circle) of the fascicle (26, 32). Curved fascicles could produce pressure toward the concave side (2, 5, 30, 32). It has been reported, from Address for reprint requests and other correspondence: T. Muramatsu, Setagaya, Setagaya-ku, Tokyo , Japan ( mura@hc.cc.keio.ac.jp). the prediction using a muscle model, that curving of the fascicle increases the intramuscular pressure and therefore affects blood flow (30, 32). In addition, Sejersted et al. (30) reported that fascicle curving reduces the force transmitted to the bone and that fascicle stress could be calculated if the curvature, intramuscular pressure, and recording depth were known. Thus it is clear that information on the degree and distribution of fascicle curving is essential to understanding skeletal muscle function. As for the degree of fascicle curving, no study has reported experimental data on humans, although several studies have qualitatively observed curving in humans in vivo (3, 8, 13, 21). Several studies also observed that the degree of curving increased when muscle length decreased (13, 35). As for the distribution of fascicle curving, Otten (26) predicted that fascicles in a unipennate muscle curved in a way that induced bulging of the whole muscle, whereas Van Leeuwen and Spoor (32) predicted, as for the human MG, that fascicles curved in the same direction with the same curvature along the muscle. However, no study has reported experimental data on humans in vivo. Intersubject variability has been reported for the architectural parameters. Between muscle thickness and pennation angle, consistent relationships have been reported (11, 12, 14, 15). Similarly, the degree of fascicle curving could be related to other architectural parameters, considering that curving has been related to pennation angle (13). The purposes of the present study were 1) to estimate the fascicle curvature in vivo at different contraction levels (at rest and during contraction) and at different muscle lengths, 2) to examine the intramuscular distribution of the fascicle curvature, and 3) to examine the relationships between fascicle curvature and the other architectural parameters. Our hypotheses were that 1) the fascicle curvature is increased by contraction and by decrease in muscle length, 2) the direction and the degree of curving are uniform along 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 /02 $5.00 Copyright 2002 the American Physiological Society 129

2 130 HUMAN FASCICLE ARCHITECTURE IN VIVO the muscle, and 3) the fascicle curvature is related to the other architectural parameters. METHODS Subjects The subjects of this study were 11 healthy men [age yr, height cm, weight kg (means SD)]. The purposes and procedures were explained to the subjects before their consent to participate in the study was obtained. Joint Position Settings and Torque Measurements We used the same techniques as described in our laboratory s recent study (24). Briefly, we used an electric myometer (model Myoret RZ-450, Asics, Tokyo, Japan) to fix the ankle joint and to measure plantar flexion torque. Each subject lay prone on a bed, with the left foot fixed to the myometer (Fig. 1). After a warm-up session, the subjects were instructed to exert isometric torque from relaxation to MVC with a visual aid of the developed torque on an oscilloscope with a ramp increase in torque at 10% MVC/s. Average values over three measurements were adopted. Test 1 (three regions). The ankle was set at neutral anatomic position, with the sole of the foot at 90 to the tibia. The measurement was repeated three times for each of the three parts (see Ultrasonography). We executed this test for seven subjects. Test 2 (three angles). The ankle was set at 120 (plantar flexed), 90, and 75 (dorsiflexed). The measurement was repeated three times for each of the three ankle angles at the central part of the medial gastrocnemius (MG). We also executed this test for seven subjects. That is, three subjects participated in both tests, four subjects participated only in test 1, and the other four subjects participated only in test 2. For each of test 1 and 2, at least 3 min of rest were taken between trials. We adopted average values over three measurements. Ultrasonography The muscle tested in this study was human MG. The technique used was also described in our laboratory s previous study (24). Briefly, we used the ultrasonic apparatus (model SSD-2000, Aloka, Tokyo, Japan) with an electronic linear array probe of 7.5-MHz wave frequency. The precision Fig. 1. Schematic illustration of the human medial gastrocnemius muscle (MG). Measurement sites (distal, central, proximal) are also shown. and linearity of the image using ultrasonography have been confirmed by Kawakami et al. (11), who compared the distance between pins struck on an acoustic standoff and the distance between the pins in the reconstructed image. The probe was longitudinally attached to the dermal surface by an adhesive tape, which restrained the probe from sliding (4, 16, 22), over the mediolateral center of MG. To obtain architectural parameters from different portions in MG, we scanned distal, central, and proximal parts of MG by ultrasonography (Fig. 1). In each part, we could find a fascicle whose echo was clear from the superficial to the deep aponeuroses throughout the contraction (Fig. 2). Therefore, it should be reasonable to suppose that the plane of the ultrasonogram is parallel to the fascicle (13). We randomized the order of experiments among each part. In each trial, the targeted fascicle moved slowly enough for the investigator to scan successfully. The ultrasound images were transferred to a personal computer (model Powerbook G3, Apple, Tokyo, Japan) at 30 Hz for obtaining architectural parameters (see below). Estimation of Curvature and Other Architectural Parameters On each of the ultrasonographic images, four architectural parameters ( d, s, H, T) defined in Fig. 3 were measured three times, and averaged values were adopted for further analyses. From d, s, and H, the curvature of the fascicle was determined (see below). The fascicle was assumed to be the arc (29, 32, 33) with radius r (the curvature to be 1/r). Then the following should be formed (for the meaning of each symbol, see Fig. 3) tan d x 1 /y 1 tan s x 2 /y 2 y 2 y 1 H x 2 1 y 2 1 r 2 x 2 2 y 2 2 r 2 We could solve these equations for the curvature (1/r) 1/r cos 2 d cos 2 s / 2H cos d cos s Then, to ascertain the validity of the value of the curvature, we compared the fascicle length (Lf arc), calculated from the curvature, with the actual fascicle length (Lf trc) measured on the ultrasonographic image. Lf arc corresponds to the arc P1P2 (Fig. 3) and is calculated by the following. Lf arc r d s (Note that the unit of d and s is radian in this equation.) We measured Lf trc by tracing along its path with the curvature taken into consideration on the ultrasonographic images (13, 20). In addition, fascicle length estimated from the following equation (Lf hyp), which had often been used in previous studies (12, 15, 17, 19), was calculated Lf hyp T/sin d This method of estimating the fascicle length was based on the assumption that the fascicle was not curved. We also compared Lf hyp with Lf trc to understand, although indirectly, the effect of the fascicle curvature on the estimation of the fascicle length. The comparison among Lf arc, Lf hyp, and Lf trc was made only at the central part of MG. Note that H and T in Fig. 3 are different. In the present study, we did not use the assumption that the aponeuroses were

3 HUMAN FASCICLE ARCHITECTURE IN VIVO 131 Fig. 2. Ultrasonographic images of longitudinal sections of MG muscle at distal, central, and proximal regions. Top: at rest; bottom: at maximal voluntary contraction (MVC). straight, which could induce errors in estimating architectural parameters. Reproducibility We evaluated the reproducibility of calculating the fascicle curvature, as for test 1, through three procedures (24) on the basis of a coefficient of variation (SD/mean) (9, 25): 1) interday reproducibility, which was tested for three subjects on two separate occasions, was on average 9.8%; 2) reproducibility of three trials for all subjects was on average 9.7%; and 3) reproducibility of measuring from the same ultrasonic image (images for all trials were digitized three times) was on average 6.1%. Statistics Values are presented as means SD. A two-way ANOVA with repeated measures was used to analyze the effects of 1) contraction levels (rest vs. MVC) and locations (distal, central, and proximal) on curvature (1/r) and fascicle length (Lf trc); 2) contraction levels (rest vs. MVC) and methods (Lf arc, Lf hyp, and Lf trc) on the estimated fascicle length; and 3) contraction levels and ankle angles (120, 90, and 75 ) on curvature. Significant differences among means were detected by using Tukey-Kramer s post hoc tests. To test the significance of the relationship of 1) the fascicle curvature and pennation angle, 2) the fascicle curvature and muscle thickness, and 3) the fascicle length between Lf trc and the other methods (Lf arc and Lf hyp), Pearson s correlation coefficient was calculated. A P 0.05 level of confidence was set for all analyses. RESULTS Fig. 3. Arc P1P2 corresponds to the fascicle. L1 corresponds to the tangent of the deep aponeurosis at P1, which is the intersection made by the fascicle and the deep aponeurosis. L2 corresponds to the tangent of the fascicle at P1. L3 corresponds to the tangent of the fascicle at P2, which is the intersection made by the fascicle and the superficial aponeurosis. r, Radius of circle; H, length of perpendicular dropped from P2 to L1; T, muscle thickness (minimum distance between P2 and deep aponeurosis); d, angle made by L1 and L2; s, angle made by L1 and L3. Test 1 The calculated curvature and measured Lf trc at three parts at rest and MVC are shown in Table 1. For each of the curvature and Lf trc, the effect of the contraction level was significant, whereas the effect of the location was not significant. The direction of curving was consistent along the muscle. That is, fascicles were concave on the proximal side. We found significant correlation between 1) the curvature and pennation angle at distal and central regions during MVC (Fig. 4), 2) the curvature and muscle thickness at distal and central regions during MVC (Fig. 5), and 3) Lf trc and each of Lf arc and Lf hyp [Fig. 6, A (at rest) and B (at MVC)]. Lf hyp was significantly smaller than Lf trc, whereas significant difference was not found between Lf arc and Lf trc.at MVC, Lf hyp was 6% smaller than Lf trc.

4 132 HUMAN FASCICLE ARCHITECTURE IN VIVO Table 1. Fascicle curvature and measured fascicle length at distal, central, and proximal parts Curvature, 1/m Fascicle Length, mm Distal Rest MVC Central Rest MVC Proximal Rest MVC Values are means SD; n 7. Effect of the contraction levels (rest vs. maximal voluntary contraction (MVC) was significant, whereas effect of the locations (distal, central, and proximal) was not significant at P Test 2 The calculated curvature at three ankle angles at rest and MVC is shown in Table 2. The effect of the difference of the ankle angle was significant. At MVC, significant difference among three angles was found: the value was in the order DISCUSSION Fig. 4. Relationship between pennation angle ( d) and fascicle curvature at 3 regions ({ and }, distal; and, central; and Œ, proximal). Open symbols indicate plots at MVC, and solid symbols indicate plots at rest. Fig. 5. Relationship between muscle thickness and fascicle curvature at 3 regions ({ and }, distal; and, central; and Œ, proximal). Open symbols indicate plots at MVC, and solid symbols indicate plots at rest. This is, to the best of our knowledge, the first study that quantitatively showed the fascicle curvature of the human skeletal muscle in vivo. We showed that 1) the curvature was increased by contractions and by decrease in muscle length, 2) intramuscular variability was observed neither in the degree nor the direction of curving, and 3) the curvature was correlated to muscle thickness and pennation angle. In the present study, to confirm the validity of the estimation of the curvature, the fascicle length calculated from the curvature (Lf arc ) was compared with the measured fascicle length (Lf trc ). There was remarkable conformity (Fig. 6). In addition, we superimposed the arc, drawn from the calculated curvature, onto the fascicle echo of the ultrasonographic image and found no visible deviation from each other. From these observations, we believe that the procedure to estimate the curvature was valid. Fascicle length (Lf hyp ) has sometimes been estimated from the pennation angle and muscle thickness (12, 15, 17, 19). The result of the present study suggests that this method significantly produces errors in estimating the fascicle length if the fascicle curves. The average underestimation was 6% (Fig. 6B), which might not seem to be critically large. However, the error would be substantially large in muscles with long fascicles such as vastus lateralis (8) and triceps brachii (12). Fascicles were almost straight at rest, which agrees with the report of Narici et al. (25), who described the MG of human cadavers. On the other hand, at MVC, we observed substantial curving of the fascicles as reported by several previous studies (13, 21). Although quantitative data of the curvature has not been reported as for the human skeletal muscles, assumptions have been made: Van Leeuwen and Spoor (32) assumed the curvature for the human MG to be 5.1 m 1, and Sejersted et al. (30) assumed it for the human vastus medialis to be m 1. These assumed values of the curvature were on the same order with those of the present study. The effects of muscle length (ankle angle) on the curvature was substantial (Table 2), which supports the observation of Kawakami et al. (13) and Zuurbier and Huijing (35), who reported that the fiber curvature of rat gastrocnemius resulted in an underestimation of fiber length of 2% when the muscle length

5 HUMAN FASCICLE ARCHITECTURE IN VIVO 133 Fig. 6. Calculated fascicle length plotted against measured length (Lf trc) at rest (A) and at MVC (B). E, Length calculated under the assumption that the fascicles were curved (Lf arc);, length calculated under the assumption that the fascicles were straight (Lf hyp). was above optimum and 5% when the muscle length was below optimum length. In other words, fiber curvature was larger when the muscle was shorter, which agrees with the present results. The measured fascicle length at three ankle angles at MVC was , , and mm, for 120, 90, and 75, respectively. That is, fascicles were longer when muscle is longer. Therefore, we could say that the curvature was larger at shorter fascicle length at MVC. At rest, muscle length did not significantly affect the curvature (Table 2). These results suggest that the curvature is affected by both contraction levels and fascicle length. In the present study, fascicles curved in the same direction with similar curvature along the muscle. This result coincided with that of Van Leeuwen and Spoor (32) on the human MG but was contrary to the findings of Otten (26), who predicted that fascicles in a unipennate muscle were curved in a way that induced bulging of the muscle; the direction of curving at distal part was different from that at proximal part. The former study reported that the compressive force produced by soleus and tibia onto the MG tendinous tissue should play an important role in arranging the tendinous tissue and therefore fascicles within the muscle, whereas the latter study did not assume such a compressive force. Muscles in vivo Table 2. Fascicle curvature at 3 ankle angles Ankle Angle Curvature, 1/m Plantar flexed, 120 Rest MVC * Neutral, 90 Rest MVC Dorsiflexed, 75 Rest MVC Values are means SD; n 7. At MVC, the effect of the difference in ankle angle was significant. * Significantly larger than neutral and dorsiflexed; significantly larger than dorsiflexed. are necessarily compressed by surrounding tissues that should affect the architecture of the muscle, which would be one reason that the architecture in vitro is not always applicable to that in vivo (27). Curving of fascicles has been related to the intramuscular pressure (1, 31). From the law of Laplace, the difference in pressure between the concave and the convex side of the fascicle has been supposed to be proportional to the curvature and stress of the fascicle (30). That is, when the tensed fascicle is curving, the pressure would be generated in the concave side (2, 5, 32). For example, Ameredes and Provenzano (1) assumed that the muscle bulging [onionlike configuration (30)] during contractions contributed to the high pressure in the central region in the canine gastrocnemius muscle. In the present study, the fascicles were concave in the proximal side. Therefore, the pressure could be higher in the proximal region in human MG during contractions, although we could not confirm it because there are no published data available concerning the distribution of human gastrocnemius intramuscular pressure. There were tendencies that curvature was proportional to muscle thickness and pennation angle (Figs. 4 and 5), which supports the prediction of Kawakami et al. (13). Styf et al. (31) reported that the intramuscular pressure would increase if the pennation angle increased. In the present study, subjects with larger pennation angle generally had larger curvature, which also convinces us to assume that subjects with larger pennation angle had larger intramuscular pressure. In conclusion, we showed that the curvature of the fascicle could be calculated from ultrasonographic images in vivo and that the curvature is affected by both contraction levels and fascicle length. In addition, the degree and the direction of curving were uniformly distributed. These findings are particularly important for understanding the mechanical functions of human skeletal muscle in vivo and for more accurate muscle modeling in future studies.

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