Tetsuo Fukunaga, Yoshiho Ichinose, Masamitsu Ito, Yasuo Kawakami and Senshi Fukashiro J Appl Physiol 82:354-358, 1997. You might find this additional information useful... This article cites 18 articles, 3 of which you can access free at: http://jap.physiology.org/cgi/content/full/82/1/354#BIBL This article has been cited by 18 other HighWire hosted articles, the first 5 are: Quantitative diffusion tensor MRI-based fiber tracking of human skeletal muscle D. A. Lansdown, Z. Ding, M. Wadington, J. L. Hornberger and B. M. Damon J Appl Physiol, August 1, 2007; 103 (2): 673-681. [Abstract] [Full Text] [PDF] Intensity- and muscle-specific fascicle behavior during human drop jumps F. Sousa, M. Ishikawa, J. P. Vilas-Boas and P. V. Komi J Appl Physiol, January 1, 2007; 102 (1): 382-389. [Abstract] [Full Text] [PDF]

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rapid communication Determination of fascicle length and pennation in a contracting human muscle in vivo TETSUO FUKUNAGA, YOSHIHO ICHINOSE, MASAMITSU ITO, YASUO KAWAKAMI, AND SENSHI FUKASHIRO Department of Life Sciences, The University of Tokyo, Komaba 3–8–1, Meguro, Tokyo 153, Japan

vastus lateralis muscle; ultrasound; pennation angle; muscle contraction

THE FORCE EXERTED BY MUSCLE fibers is modified by their geometric arrangement, structures of the joint, and the angle and location of the tendon in respect to the bone, before it appears at the joint as moments ( joint torque). Thus the sole observation of joint actions gives little information on muscle actions within. For instance, the relationship between joint position and torque does not disclose the length-force characteristics of the muscle. This is especially true for pennate muscles in which short fibers are arranged at an angle to the line of action of the muscle, and the angle as well as muscle fiber length change during contraction. Knowledge of the geometric arrangement of muscle fibers, i.e., muscle architecture, is therefore important when studying muscle functions and the resultant joint actions. To date, parameters such as the length, crosssectional area, and pennation angles of fibers have been investigated (1–3, 6, 7, 10, 11, 15, 19, 20, 23), and it has been shown that the muscle architecture considerably affects the manner in which muscle force is transmitted

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to the tendons and bones (11, 15). Many of the previous studies on human muscle architecture have been done through a direct dissection of cadaver specimens. However, muscles in the embalmed cadavers have been reported to change their morphological characteristics because of factors such as shrinkage (7). Besides, this method does not allow to study the effect of muscle contraction and changes in joint position on muscle architecture. The purpose of the present study was to determine architecture of a human muscle, both at rest and during contractions. We employed real-time ultrasonography to visualize fascicles in vivo (12, 13). The relationships between knee joint angles and fascicle lengths as well as angles of pennation for the vastus lateralis muscle were investigated. METHODS

Six healthy men (age 25 6 1 yr, body height 174.5 6 2.6 cm, body mass 72.1 6 4.4 kg) participated as subjects. The nature and possible consequences of the study were explained to each subject, and informed consent was obtained beforehand. A real-time ultrasonic apparatus (SSD-2000, 7.5 MHz, Aloka, Japan) was used. Precision and linearity of the image have been confirmed by the authors elsewhere (12). The level of 50% of the thigh length (50% of the distance from the greater trochanter to the lateral epicondyle of the femur) was determined. At this level, the width of the vastus lateralis muscle was measured by the use of the ultrasound apparatus, and the position of one-half of the width was marked with a pen. At this position, a longitudinal ultrasonic image was obtained, and fascicles were visualized. One of the fascicles in the image was carefully traced by moving the scanning head on the dermal surface proximally and distally, and ultrasound images containing the whole fascicle from the proximal and distal ends were obtained. From them, the length of the fascicle was measured by the use of a digital curvimeter (Comcurve-8, Koizumi-Sokki, Japan). The measurement was repeated five times for each subject. The coefficients of variation ranged from 0.5 to 4.3%. The pennation angles (fascicle angles), defined as the angles between the echoes of the deep aponeurosis of vastus lateralis and the echoes from interspaces among fascicles (9, 12, 17), were also measured. During measurement, the subject was seated on a test bench of an electric dynamometer (MYORET, Asics, Japan) with a backrest and was secured by using straps around the waist, breast, and the knee. The axis of the lever arm of the

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Fukunaga, Tetsuo, Yoshiho Ichinose, Masamitsu Ito, Yasuo Kawakami, and Senshi Fukashiro. Determination of fascicle length and pennation in a contracting human muscle in vivo. J. Appl. Physiol. 82(1): 354–358, 1997.—We have developed a technique to determine fascicle length in human vastus lateralis muscle in vivo by using ultrasonography. When the subjects had the knee fully extended passively from a position of 110° flexion (relaxed condition), the fascicle length decreased from 133 to 97 mm on average. During static contractions at 10% of maximal voluntary contraction strength (tensed condition), fascicle shortening was more pronounced (from 126 to 67 mm), especially when the knee was closer to full extension. Similarly, as the knee was extended, the angle of pennation (fascicle angle, defined as the angle between fascicles and aponeurosis) increased (relaxed, from 14 to 18°; tensed, from 14 to 21°), and a greater increase in the pennation angle was observed in the tensed than in the relaxed condition when the knee was close to extension (,40°). We conclude that there are differences in fascicle lengths and pennation angles when the muscle is in a relaxed and isometrically tensed conditions and that the differences are affected by joint angles, at least at the submaximal contraction level.

FASCICLE LENGTH AND PENNATION IN CONTRACTING HUMAN MUSCLE

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dynamometer was visually aligned with the estimated center of the knee joint. An ankle cuff on the lever arm was attached proximal to the lateral malleolus. The knee joint angles were changed every 10° from full extension to flexion at 110°, and, at each joint angle, ultrasonic measurement was performed. The subject relaxed knee extensor muscles during measurement. After the measurement in the relaxed condition, measurements were carried out while the muscles were in a tensed condition. After the subject familiarized himself with the testing procedures and after a warm-up session of several submaximal and maximal exertions, the subject was encouraged to perform maximal isometric knee extension at the joint angles from flexion at 110° to full extension, with an interval of 10°, and the peak torque during exertion was recorded. Rest periods were .1 min between contractions to prevent fatigue and ensure a maximal contraction at each joint angle. After the maximal torque measurement, 10% of the maximal torque was calculated for each joint angle. At respective joint angles, the subject exerted knee extension torque at 10% of the maximum, with a visual aid of the torque displayed with the target torque on a monitor screen. The ultrasonic measurement was done after confirmation that torque became stable at the target level. The lengths and angles of the fascicles in the relaxed and tensed conditions were measured on two different occasions. Reproducibility was tested by computing coefficients of varia-

tion (CV) according to the following equation CV 5 (SD/ xc) 3 100 where SD is the square root of the between-test variance obtained from the one-way repeated-measures analysis of variance, and xc is the combined mean of the two measurements (5). In addition, a paired t-test was performed for two measurements in each condition and at each joint angle to test their statistical difference. To investigate the effect of the conditions (relaxed and tensed) and knee joint angles on the lengths and angles of the fascicles, a two-way analysis of variance with repeated measures was used (2 3 12, conditions 3 knee joint angles). For those variables for which a significant effect was found, a Tukey post hoc test was used. A P , 0.05 level of confidence was set for all analyses. RESULTS

In the ultrasonic image obtained from vastus lateralis muscle of one subject (Fig. 1), one can clearly observe the echoes reflected from fascicles. The CV of repeated measurements of the fascicle lengths ranged from 0 to 6.8% (relaxed, mean: 2.1%) and from 0 to 6.1% (tensed, mean: 3.0%) for the knee angles tested; CV values of the fascicle angles ranged from 0 to 2.0% (relaxed, mean: 0.8%) and from 0 to 3.8% (tensed, mean: 1.7%). The

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Fig. 1. Ultrasonic longitudinal image of vastus lateralis muscle. Ultrasonic transducer was placed on skin over the muscle at 50% distance from greater trochanter to lateral epicondyle of femur. Fascicle length (fL) was determined as length of a line drawn along ultrasonic echo parallel to fascicle. Fascicle angle (u) was determined as angle between echoes obtained from fascicles and deep aponeurosis in ultrasonic image. k, Distal end of a fascicle.

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FASCICLE LENGTH AND PENNATION IN CONTRACTING HUMAN MUSCLE

variability of CV was not affected by the knee joint angles. Also, there were no significant differences between mean values of the repeated measurements both for the lengths and angles of the fascicles. When the knee was fully extended passively from the flexed position (110°, full extension corresponds to 0°; relaxed condition), the fascicle length decreased by 27% from 132.9 6 8.3 to 96.7 6 6.9 (SE) mm (Fig. 2). When static voluntary contractions were performed at several joint angles at 10% of the maximal voluntary contraction (MVC) strength, fascicle lengths decreased, and the magnitude was greater (30%) when the knee was closer to full extension than when the knee was flexed (5%) (Fig. 2). The effect of different conditions was significant at each joint angle except at 110°.

Fig. 3. Changes in fascicle angles as a function of knee angles. Significantly larger fascicle angles in tensed than in relaxed conditions were observed at extended positions (i.e., knee angle ,30°). Error bars indicate 1 SE between subjects. * Significantly different between relaxed (r) and tensed (s) conditions, P , 0.05.

DISCUSSION

The muscle architecture is an intermediate level that affects conversion of the force and excursion of muscle fibers into joint actions. Understanding of this level is important when we estimate events that are happening in the muscle from observations at the joint, but analysis of this level is often ignored (8). It has been shown that architectural parameters such as muscle fiber length and pennation angles affect functional characteristics of a muscle (e.g., maximal shortening velocity and maximal tension) as well as intrinsic ones, such as fiber composition (4, 18). In some previous studies, human muscle architecture has been observed in cadaver specimens and related to functional characteristics (2, 3, 6, 10, 21), but very little data are available in living human muscles. In the present study, fascicle length and pennation angles were determined in vivo in a contracting human muscle, which is the first attempt as long as the authors’ knowledge can reach. We considered that the arrangement of a fascicle, which is connected to proximal and distal tendons, is important when one studies how muscle force is transmitted to tendons and bones. Changing knee position passively from 110° to full extension resulted in change of fascicle length from 133 to 97 mm on average. When the muscle was actively contracting in an isometric manner, the change in knee position by the same amount corresponded to fascicle shortening from 126 to 67 mm. The larger shortening would have been caused by taking up of the elongated series elastic component. The 30-mm difference between the relaxed and tensed conditions is as much as one-half of the optimal fiber length of the vastus lateralis muscle (64–67 mm; Ref. 20). The results also show that the range of the fascicle length change is beyond the optimal length of the vastus lateralis muscle

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Fig. 2. Changes in fascicle lengths at various angles of knee joint. Measurements were done in 2 conditions: a relaxed (r) condition with no muscle contraction and a tensed condition (s), where subject performed static knee extensions at 10% of maximal voluntary strength using an electrical dynamometer. Error bars indicate 1 SE between subjects. * Significantly different between relaxed and tensed conditions, P , 0.05.

The fascicle angle increased from 14 to 18° during knee extension (Fig. 3). At the same joint angle, larger fascicle angles were observed in tensed than in relaxed conditions, especially when the knee was in extended positions with joint angles ,40° (statistically significant at 0, 10, 20, and 30°). Angles of pennation for vastus lateralis muscle have been reported to be 5–20° in cadavers (23) and 6–27° in healthy subjects (9, 17). These results are in good agreement with our measurements. The relationships between fascicle angles, fascicle lengths, and knee joint angles differed between relaxed and tensed conditions. When the knee was flexed beyond 90°, fascicle length in the tensed condition was slightly but significantly shorter than in the relaxed condition, with no apparent difference in fascicle angles. When the knee joint angle was between 90 and 40°, shorter fascicle lengths were more pronounced in the tensed condition, with fascicle angles being somewhat smaller than in the relaxed condition. When the knee was extended ,40°, fascicle lengths were much shorter in the tensed condition, with a large significant increment in fascicle angles.

FASCICLE LENGTH AND PENNATION IN CONTRACTING HUMAN MUSCLE

In the present study, the length and angle of fascicles were determined from the midbelly of the vastus lateralis muscle at the level of 50% of the thigh length. Although it has been shown that there is marked uniformity of fiber length throughout a muscle (20), some studies have reported heterogeneity of fascicle angles along the length of the muscle (10, 19). Thus the relationships between joint angles and fascicle arrangement might differ in the different portions of the muscle, which remain to be determined. Besides, in this study, only the muscle activity at 10% MVC was tested in the tensed condition. Architectural behavior of fascicles would change at different activation levels, a fact that also deserves further studies. To date, architectural data of human skeletal muscles have been derived mainly from cadaver specimens (1–3, 6, 7, 11, 15, 20, 21, 23). The present results clearly show that the architecture of actively contracting muscle fibers differs considerably from that in which the movement is passively induced. Although caution is certainly merited in interpreting the present results, it should be pointed out that the use of the architectural data obtained in vivo would greatly contribute to the understanding of contracting human muscles. Address for reprint requests: Y. Kawakami, Dept. of Life Science (Sports Science), The Univ. of Tokyo, Komaba 3–8–1, Meguro, Tokyo 153, Japan (E-mail: [email protected]). Received 16 January 1996; accepted in final form 10 September 1996. REFERENCES 1. Amis, A. A., D. Dowson, and V. Wright. Muscle strengths and musculo-skeletal geometry of the upper limb. Eng. Med. 8: 41–48, 1979. 2. An, K. N., F. C. Fui, B. F. Morrey, R. L. Linscheid, and E. Y. Chao. Muscles across the elbow joint: a biomechanical analysis. J. Biomech. 14: 659–669, 1981. 3. Brand, R. A., D. R. Pedersen, and J. A. Friedrich. The sensitivity of muscle force predictions to changes in physiologic cross-sectional area. J. Biomech. 19: 589–596, 1986. 4. Burkholder, T. J., B. Fingado, S. Baron, and R. L. Lieber. Relationship between muscle fiber types and sizes and muscle architectural properties in the mouse hindlimb. J. Morphol. 221: 177–190, 1994. 5. Chilibeck, P., A. Calder, D. G. Sale, and C. Webber. Reproducibility of dual-energy x-ray absorptiometry. Can. Assoc. Radiol. J. 45: 297–302, 1994. 6. Edgerton, V. R., P. Apor, and R. R. Roy. Specific tension of human elbow flexor muscles. Acta Physiol. Hung. 75: 205–216, 1990. 7. Friedrich, J. A., and R. A. Brand. Muscle architecture in the human lower limb. J. Biomech. 23: 91–95, 1990. 8. Gans, C., and A. S. Gaunt. Muscle architecture in relation to function. J. Biomech. 24: 53–65, 1991. 9. Henriksson-Larsen, K., M.-L. Wretling, R. Lorentzon, and L. Oberg. Do muscle fibre size and fibre angulation correlate in pennated human muscles? Eur. J. Appl. Physiol. Occup. Physiol. 64: 68–72, 1992. 10. Huijing, P. A. Architecture of the human gastrocnemius muscle and some functional consequences. Acta Anat. 123: 101–107, 1985. 11. Jacobson, M. D., R. Raab, B. M. Fazeli, R. A. Abrams, M. J. Botte, and R. L. Lieber. Architectural design of the human intrinsic hand muscles. J. Hand Surg. 17A: 804–809, 1992. 12. Kawakami, Y., T. Abe, and T. Fukunaga. Muscle-fiber pennation angles are greater in hypertrophied than in normal muscles. J. Appl. Physiol. 74: 2740–2744, 1993.

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(20). This could mean that this muscle uses a descending limb of the length-tension relationship within the physiological range, which agrees with a previous report on hand muscles (16). Wickiewicz et al. (21) investigated in vivo forcevelocity characteristics of muscle fibers from torque and angle of the knee joint. In their study, fiber lengths of the knee extensor muscles were derived from cadavers. They measured knee extension torque using an isokinetic dynamometer at an angle of 30° from full extension. However, as shown in the present study, at this knee position, the length of the fascicle between relaxed and tensed conditions differs greatly (110 vs. 92 mm). In fact, the researchers estimated that the muscle fiber length change for 90° knee excursion was 15–23%, which was comparable to the present result for the relaxed condition (23%, Fig. 2), but in the tensed condition the change was much greater (43%). Therefore, the determination by Wickiewicz et al. of shortening velocity of the muscle fibers could have been underestimated. If the present results were interpolated to their data, the predicted maximal shortening velocity of fibers would be 589 not 315 mm/s (21). Because the force applied to the tendon by the contraction of muscle fibers is reduced by a factor of cosu (where u 5 pennation angle) from the sum of the forces of the individual fibers, the larger the pennation angles, the greater the reduction in force development (11, 12, 14, 15). Larger fascicle angles at the extended positions could, therefore, cause more mechanical disadvantage in the force transmission. However, present results show that the largest fascicle angle is 21° in the tensed condition; thus the loss of force during transmission would be 7% (5 cos21°) at the most. Considering also the accuracy of the present fascicle angle measurement, one could not put physiological significance on such a small result from the present study. Similarly, in the stance phase of walking, the knee joint moves between 40 and 0° of flexion (22). According to the present results, in this range of motion, the fascicle angle of the vastus lateralis muscle changes from 17 to 18° and from 18 to 21° in the relaxed and tensed conditions, respectively. The cosine of these angles then ranges from 0.93 to 0.96. Thus the expected loss of the force exerted by muscle fibers when it is transmitted to tendon would be ,4–7%. Considering, again, the accuracy of present measurements of fascicle angle, the impact of pennation angles on force transmission and the difference between the relaxed and tensed conditions would not be significant. However, the fascicle length showed larger variance between relaxed and tensed conditions, and this variance, possibly that of fascicle angles as well, would be larger if muscle activation were greater (e.g., MVC), in which case the difference between the two conditions could have functional importance. Care must be taken when estimating changes in muscle fiber length from the joint angle changes by using the data of the embalmed cadavers (2, 6, 15).

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13. Kuno, S., and T. Fukunaga. Measurement of muscle fibre displacement during contraction by real-time ultrasonography in humans. Eur. J. Appl. Physiol. Occup. Physiol. 70: 45–48, 1995. 14. Lieber, R. L. Skeletal Muscle Structure and Function. Baltimore, MD: Williams & Wilkins, 1992. 15. Lieber, R. L., and C. G. Brown. Quantitative method for comparison of skeletal muscle architectural properties. J. Biomech. 25: 557–560, 1992. 16. Lieber, R. L., G. J. Loren, and J. Friden. In vivo measurement of human wrist extensor muscle sarcomere length changes. J. Neurophysiol. 71: 874–881, 1994. 17. Rutherford, O. M., and D. A. Jones. Measurement of fibre pennation using ultrasound in the human quadriceps in vivo. Eur. J. Appl. Physiol. Occup. Physiol. 65: 433–437, 1992. 18. Sacks, R. D., and R. R. Roy. Architecture of the hind limb muscles of cats: functional significance. J. Morphol. 173: 185– 195, 1982.

19. Scott, S. H., C. M. Engstrom, and G. E. Loeb. Morphometry of human thigh muscles. Determination of fascicle architecture by magnetic resonance imaging. J. Anat. 182: 249–257, 1993. 20. Wickiewicz, T. L., R. R. Roy, P. L. Powell, and V. R. Edgerton. Muscle architecture of the human lower limb. Clin. Orthop. Rel. Res. 179: 275–283, 1983. 21. Wickiewicz, T. L., R. R. Roy, P. L. Powell, Perrine, J. J., and V. R. Edgerton. Muscle architecture and force-velocity relationships in humans. J. Appl. Physiol. 57: 435–443, 1984. 22. Winter, D. A. Kinematic and kinetic patterns in human gait: variability and compensating effects. Hum. Movement Sci. 3: 51–76, 1984. 23. Yamaguchi, G. T., A. G. U. Sawa, D. W. Moran, M. J. Fessler, and J. M. Winters. A survey of human musculotendon actuator parameters. In: Multiple Muscle Systems: Biomechanics and Movement Organization, edited by J. M. Winters and S. L.-Y. Woo. New York: Springer-Verlag, 1990, p. 717–773.

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