Optimal Pennation Angle of the Primary Ankle Plantar and Dorsiflexors: Variations With Sex, Contraction Intensity, and Limb

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1 Journal of Applied Biomechanics, 2006; 22: Human Kinetics, Inc. Optimal Pennation Angle of the Primary Ankle Plantar and Dorsiflexors: Variations With Sex, Contraction Intensity, and Limb Kurt Manal, Dustyn P. Roberts, and Thomas S. Buchanan University of Delaware Center for Biomedical Engineering Research Ultrasonography was used to measure the pennation angle of the human tibialis anterior (TA), lateral gastrocnemius (LG), medial gastrocnemius (MG), and soleus (Sol). The right and left legs of 8 male and 8 female subjects were tested at rest and during maximum voluntary contraction (MVC). Joint angles were chosen to control muscle tendon lengths so that the muscles were near their optimal length within the length tension relationship. No differences in pennation angle were detected between the right and left legs. Another consistent finding was that the pennation angle at MVC was significantly greater than at rest for all muscles tested. Optimal pennation angles for the TA, MG, and Sol were significantly greater for the men than for the women. Optimal pennation angles for the TA, LG, MG, and Sol for the male subjects were 14.3, 23.7, 34.6, and 40.1 respectively, whereas values of 12.1, 16.3, 27.3, and 26.3 were recorded for the female subjects. The results of this study suggest the following: (1) similar values for pennation angle can be used for the right and left TA, LG, MG, and Sol; (2) pennation angle is significantly greater at MVC than at rest for all muscles tested; and (3) sex-specific values for optimal pennation angle should be used when modeling the force-generating potential of the primary muscles responsible for ankle plantar and dorsiflexion. The authors are with the Center for Biomedical Engineering Research, Department of Mechanical Engineering, University of Delaware, Newark, DE Key Words: ultrasound, in vivo, isometric contraction, modeling, gender The medial gastrocnemius (MG), lateral gastrocnemius (LG), and the soleus (Sol) combine to form the triceps surae muscle group. This group converges into the Achilles tendon and comprises the dominant plantar flexors of the ankle, generating the largest of the lower limb sagittal plane joint moments during walking (Eng & Winter, 1995). How the MG, LG, and Sol contribute to this large plantar flexion moment and knowledge about the relative timing of these forces can enhance our understanding of normal and pathological gait. Direct measures of muscle force are not yet practical and therefore indirect methods are used to estimate muscle forces in vivo. Buchanan and colleagues described one such method; an EMG-driven Hill model, which has been used to estimate joint moments and individual muscle forces (Buchanan et al., 2004, 2005). The maximum isometric force a muscle generates occurs when the fibers are at an optimal length and the muscle is fully activated. The corresponding pennation angle is the optimal pennation angle, and it is an important consideration when using musculoskeletal models to estimate muscle force (Zajac, 1989). Real-time Ultrasonography can be used to image architectural features of muscle in vivo (Fukashiro et al., 2006), and therefore it is possible to use ultrasound to measure subject-specific estimates of optimal pennation angle. 255

2 256 Manal, Roberts, and Buchanan When it is not possible to measure subject-specific pennation angles, estimates can be obtained from the literature. One source commonly used by those constructing musculoskeletal models is a summary of cadaver-based measures tabulated by Yamaguchi and colleagues (Yamaguchi et al., 1990). For example, Bogey et al. (2005) used pennation angles for the triceps surae originally reported by Wickiewicz and colleagues (1983). Pennation angle for the LG measured from three cadavers ranged between 5 and 10, whereas in vivo ultrasound recordings from six male subjects during maximum voluntary contraction (MVC) averaged 31 ± 6 (Kawakami et al., 1998). Pennation angles in both studies were measured with the limbs in the same configuration (i.e., knee extended and ankle in plantar flexion), and therefore this large difference (>20 ) resulted because cadaveric material does not contract. Muscle contraction causes fiber shortening, leading to an increase in fiber pennation angle. Since optimal pennation angle is the pennation angle at maximum isometric force, literature values recorded from cadaveric specimens tend to underestimate this value and contribute to erroneous muscle force estimates. Narici and colleagues discuss this limitation and others when using cadaveric data to characterize in vivo muscle function (Narici et al., 1996). In vivo ultrasound measures have shown that pennation angle for the triceps surae varies with joint angle (i.e., fiber length) and contraction intensity (Maganaris, 2003; Maganaris et al., 1998; Narici et al., 1996). Perhaps the most dramatic example of this was a 45 increase for the MG, increasing from 22 at rest with the knee extended and ankle in dorsiflexion to 67 at MVC with the knee flexed and the ankle in plantar flexion (Kawakami et al., 1998). This large increase was not an isolated case, but rather the average of six male subjects. The relationship between fiber length and contraction intensity for the triceps surae has not been reported for women. Other factors that should be considered when obtaining pennation angle values from the literature include sex, age, and perhaps even side-to-side differences, which may be related to limb dominance. For example, ultrasound recordings of pennation angles for the MG, LG, and Sol measured at rest were significantly greater for men compared with women (Chow et al., 2000). Similar sex differences for the MG at rest have been reported by others (Abe et al., 1998; Kanehisa et al., 2003; Kubo et al., 2003b). It is unclear from these studies whether differences in optimal pennation angle exist between men and women because these data were recorded while the subjects were at rest. Interestingly, Kubo and colleagues found differences only between young men and women, but not for older men. Previous research suggests that muscle fiber pennation angle increases through adolescence (Binzoni et al., 2001), reaches a plateau that extends until later in life, and then decreases with further aging (Kubo et al., 2003a). Thus, age is a potentially confounding factor when making fiber pennation angle comparisons or when selecting a value from the literature. The tibialis anterior (TA) acts as an antagonist to the MG, LG, and Sol, and therefore accurate estimates of pennation angle for the TA are of interest when modeling the ankle joint. Pennation angles for the TA range between 10 and 20 depending on the ankle angle and contraction intensity (Hodges et al., 2003; Ito et al., 1998; Maganaris & Baltzopoulos, 1999). Note that data for male and female subjects were averaged in the Hodges study and the Ito study, whereas Maganaris and Baltzopoulos tested only male subjects. No study has reported gender-specific optimal pennation angle for the TA. There is a void in the literature reporting femalespecific estimates of optimal pennation angle for the primary ankle plantar and dorsiflexors (TA, MG, LG, and Sol). This information is important when investigating sex difference in muscle function (e.g., strength, excursion, contraction velocity) and modeling the force-generating potential of these muscles. Thus, the primary goal of our study was to record optimal pennation angle for these muscles and to investigate whether significant differences exist between men and women. Of secondary interest was to document fiber pennation angle changes from rest to MVC, and to assess whether pennation angles differ from side-to-side. Methods Eight male and eight female subjects between the ages of 20 and 50 with no history of musculoskeletal injury were recruited from the general University of Delaware population. This age range was chosen to minimize the potentially confounding effect of age. The mean (range) weight, height, and age of the subjects was 181 ( ) lb, 70 (67 75) in.,

3 Optimal Pennation Angle 257 and 24 years (20 30) for the men and 146 ( ), 65 (63 69), and 24 (21 34) for the women, respectively. All subjects provided written informed consent prior to participation, and the study was approved by the Human Subjects Review Board of the University of Delaware. Maximum isometric force varies with joint angle. In this study, muscles were tested at joint angles that corresponded to their optimal fiber length, i.e., the length at which the muscle generates the greatest force. This was approximated using a lower extremity biomechanical model of the leg (Delp et al., 1990). With the knee fully extended, the model estimated that the TA produces the most force near the limit of plantar flexion (about 30 ) and the triceps surae (MG, LG, and Sol) force peaks all occur around the natural limit of dorsiflexion (20 ). Maximum isometric force for these muscles is plotted as a function of ankle angle (Figure 1). Subjects were seated in the chair of a Biodex System 3 dynamometer (Biodex, Shirley, NY). The knee was fully extended and the foot placed in the heel cup of the ankle attachment and positioned perpendicular to the shank. This ankle angle was defined as 0. The axis of rotation of the dynamometer was aligned to coincide with an approximate sagittal plane ankle axis passing through the lateral malleolus. The thigh was strapped to the chair to minimize translations of the leg during contractions, and the chair back was angled slightly to decrease strain on the biarticular muscles that cross the hip and knee. The subjects wore sneakers and the shoe was strapped tightly to the footplate to maintain a given joint angle during contraction. Data for the TA trial were collected at 30 of plantar flexion, and the MG, LG, and Sol trials were done at 20 of dorsiflexion. The analogue moment output from the Biodex was sampled at 1 khz. Ultrasound images were obtained with a variable frequency 60-mm linear transducer (Aloka- 5000, Tokyo, Japan). For the TA, LG, and MG, the transducer was placed over the muscle belly and adjusted until aligned in the plane of the muscle fibers. It has been shown that there is no significant change in muscle architecture over the length of these muscles (Maganaris & Baltzopoulos, 1999; Maganaris et al., 1998). The Sol was imaged deep to both the MG and LG. Most images were taken at 10 MHz B-mode, with an occasional adjustment to 7.5 MHz for subjects with thicker calf muscles. The depth, B-mode gain (brightness), and orientation of the probe was set on each scan to obtain an optimal image. All images were stored in DICOM format on magneto-optical disks for later analysis. Resting values for the TA pennation angle were taken with the ankle in 30 of plantar flexion. Two maximum voluntary contractions (MVCs) were then collected while simultaneously recording Figure 1 Estimated maximum isometric force of the primary ankle plantar and dorsiflexors as a function of ankle angle. MG = medial gastrocnemius, LG = lateral gastrocnemius, Sol = soleus, TA = tibialis anterior. Note that the MG, LG, and Sol muscles all generate maximum force at approximately 20 of dorsiflexion and the TA generates maximum force at approximately 30 of plantar flexion.

4 258 Manal, Roberts, and Buchanan ultrasound data. A period of 5 s was allowed for each contraction, and the ultrasound image was frozen during the plateau region of the contraction when the joint moment displayed on the Biodex monitor had stabilized. A similar process was conducted for the triceps surae. Key differences were as follows: (1) the ankle was set at 20 of dorsiflexion and (2) a complete sequence of resting and MVC trials were collected for the LG, and then repeated for the MG. The Sol was imaged deep to both the LG and MG during all contractions. Pennation angles for the TA, MG, and LG represent the average of two trials for each muscle, whereas the pennation angle for the Sol was the average of four trials (i.e., two trials deep to the MG and two deep to the LG). Pennation angles for all muscles were measured off-line using the angle measurement function on the Aloka unit. The pennation angle for the TA was measured as the angle of insertion of the superficial fibers to the central aponeurosis of the muscle. Pennation angles for the MG, LG, and Sol were measured as the angle the fascicles inserted into the deep aponeurosis between the gastrocnemius and soleus muscles (see Figure 2). A three-factor ANOVA with two repeated measures (contraction intensity and limb) was used to test for differences in pennation angle with a level of significance set at Separate ANOVAs were conducted for each muscle. In addition, a preliminary analysis using different data than reported herein was conducted to assess the reliability of our ultrasound measurements. This process is described in the following section. Results Reproducibility of the ultrasound measurements was assessed for the right LG of one healthy male subject with the knee fully extended and the ankle in 20 of dorsiflexion. The thickest superior/inferior and medial/lateral portion of the calf in a relaxed state was marked and a total of twenty images were taken from the marked site. After each individual scan, the image was stored and the ultrasound transducer removed and repositioned for the next scan, with an elapsed time of approximately 1 min between successive scans. Images were then retrieved and measured with the angle measurement function of the ultrasound unit while the investigator was blinded to the measured angle. The coefficient of variation (COV) was used to assess the repeatability, where COV equals the standard deviation divided Figure 2 Ultrasound image of the MG (α) and Sol (β). The aponeurosis deep to the MG is clearly visible separating the MG and the Sol.

5 Optimal Pennation Angle 259 by the mean (Rutherford & Jones, 1992). In this case, the average pennation angle was 13.3 with a standard deviation of 1.1, yielding a COV of 8.5% for repeat scanning. The reproducibility of the angle measurement was tested on one image of the previous set. Ten measurements of pennation angle were carried out on the same image. The average pennation angle was 12.9 with a standard deviation of 0.5, yielding a COV of 4.2% for repeat measurements. These variations compare favorably with values reported in the literature (Fukunaga et al., 1997; Maganaris et al., 1998). Sex, contraction intensity, and limb-specific pennation angle measurements are reported in Table 1. Two findings are evident when inspecting this table. First, pennation angles for the right and left legs were similar at a given contraction intensity within sex for each muscle. The main effect of limb (right vs. left) was not statistically significant for any of the muscles tested. This finding is depicted in Figure 3. Another consistent finding was that pennation angle increased between rest and MVC (p < for all muscles), with men exhibiting a greater increase compared with women. This relationship is illustrated in Figure 4. With regards to the comparison of primary interest, the male subjects had significantly larger optimal pennation angles for the TA, MG, and Sol muscles compared with the females (Figure 5). Optimal pennation angle for the LG was 7 larger for the male subjects; however, the difference was not statistically significant (p = 0.093). Table 1 Pennation Angle Measured at Rest and Maximum Voluntary Contraction for the Right (R) and Left (L) Legs of the Male And Female Subjects. Pennation Angle Is Reported as Degrees With Standard Deviations in Parentheses. Tibialis Anterior (TA) Lateral Gastrocnemius (LG) Medial Gastrocnemius (MG) Soleus (Sol) Male Female Male Female Male Female Male Female Rest R L R L R L R L R L R L R L R L (2.2) (1.4) (1.0) (1.0) (4.2) (2.4) (3.3) (3.4) (2.7) (3.3) (2.3) (1.6) (7.4) (4.6) (4.3) 16.4 (3.8) MVC 14.7 (2.3) 14.0 (2.2) 12.1 (1.4) 12.1 (1.5) 23.4 (8.9) 24.0 (10.6) 15.2 (3.8) 17.4 (5.5) 34.9 (6.4) 34.3 (7.3) 27.5 (5.5) 27.1 (7.4) 40.4 (7.6) 39.9 (7.8) 25.3 (8.4) 27.3 (7.5) Figure 3 The main effect of limb (right vs. left) was not statistically different for any of the muscles tested. The bars atop each column represent the standard error of the mean.

6 Figure 4 Relationship between contraction intensity (rest vs. maximum voluntary contraction [MVC]) and sex. Note that the pennation angle at MVC was greater than at rest for both men and women and that the increase was greater for the male subjects. The bars represent the standard error of the mean at each contraction intensity. Figure 5 Optimal pennation angle was significantly greater for the male subjects (p < 0.05) for the muscles denoted by an asterisk. The bars atop each column represent the standard error of the mean. 260

7 Optimal Pennation Angle 261 Discussion The results of our study reveal several important findings that should be considered when choosing pennation angle values from the literature. For example, we found that the pennation angles for the primary plantar and dorsiflexors for the right and left ankles were similar for a given muscle. The motivation for this comparison stemmed from findings that subjects with hypertrophied arm muscles had larger pennation angles than control subjects (Kawakami et al., 1993). This led to the question whether side-to-side differences in muscle architecture might be related to limb dominance. In a study by Tate et al. (2006), vastus medialis muscle volume was observed to be larger in the dominant legs of young athletes whereas vastus lateralis was observed to be larger in the nondominant legs. Kearns and colleagues examined side-to-side differences in soccer players and found that muscle thickness and fascicle length for the MG between the dominant and nondominant limbs was greater for soccer players than for controls (Kearns et al., 2001). However, fiber pennation angle was not statistically different. In another study, increases in quadriceps strength and cross-sectional area were reported following a 3-month training period; however, fiber pennation angle for the vastus lateralis and intermedius did not change (Rutherford & Jones, 1992). Taken together, and in light of our findings, it appears that the same pennation angle can be used for the right and left legs for the TA, LG, MG, and Sol muscles. Another finding that was consistent for all muscles was that pennation angle at MVC was significantly greater than the angle measured at rest (p < for all muscles). Not only were the differences significant, the magnitude of the increase for the triceps surae muscles was noteworthy, with increases of approximately 10, 16, and 21 for the LG, MG, and Sol measured for the male subjects. Similar trends have been reported in studies that compared changes in pennation angle to changes in torque or force produced by whole muscle groups (Ito et al., 2000; Maganaris et al., 1998; Narici et al., 1996). The female subjects in our study exhibited the same trend, although the increase in pennation angle was smaller than the males, with increases of approximately 5, 11, and 11 for the LG, MG, and Sol. Previous studies reported fascicle angles for the TA to range between 10 and 20 depending on the ankle angle and contraction intensity (Hodges et al., 2003; Ito et al., 1998; Maganaris & Baltzopoulos, 1999a). Fiber pennation angle for the TA in our study fell within this range, and there was only a small increase between rest and MVC of 3 and 5 for the female and male subjects respectively. It appears that the TA is less sensitive to changes in joint angle and contraction intensity than the triceps surae. Although the difference in optimal pennation angle for the TA was statistically significant, the actual difference was only a couple of degrees. These results suggest that one value for pennation angle can be used for both sexes and across a full range of contraction intensities without significantly affecting muscle force estimates. Isometric contraction causes muscle fibers to shorten, which is accompanied by changes in fascicle girth and muscle geometry (Otten, 1988). This dynamic chain of events highlights a limitation of cadaver-based estimates of pennation angle. Cadaveric material does not shorten, and thus pennation angle is primarily influenced by the limb configuration in which the cadaver was fixed. Limb configuration is also a concern when ultrasound is used to measure pennation angle in vivo. A striking example of this is seen in Table 1 of data reported by Kawakami and colleagues (1998). They reported a resting pennation angle of 32 ± 4 for the MG with the knee flexed and the ankle in plantar flexion, increasing to 59.5 ± 5 when the knee was extended and the ankle in dorsiflexion. Both measurements were taken at rest and therefore did not include the effect of contraction intensity. When maximally contracted, the pennation angle increased to 67. The physiological relevance of this value may be debatable given that such a limb configuration is not encountered during functional movements. However, other measurements at joint angles typical of walking clearly show that pennation angles for the triceps surae are in excess of 30. It appears that pennation angles of 30 or more are the norm for the triceps surae, in contrast to previous suggestions that pennation angles of this magnitude are rarely encountered (Lieber, 1992). From a modeling perspective, it may be advantageous to choose a pennation angle that was measured with the limb in approximately the same configuration as the joint angles that will be tested.

8 262 Manal, Roberts, and Buchanan What value to choose when modeling a dynamic task is less obvious because the joint angles are constantly changing. Our preference is to measure pennation angle with the limb positioned such that the muscles of interest are near their optimal fiber length (Figure 1). The pennation angle at this length with the muscle fully activated is the optimal pennation angle. One advantage of measuring optimal pennation angle is that it is an input parameter to our Hill muscle model (Buchanan et al., 2004), and as these models become increasingly subject-specific it is helpful to use sex-based values for optimal pennation angle, especially for muscles that are highly pennate. Muscles with large pennation angles allow more fibers to be arranged in parallel within a given cross-sectional area, increasing the force-generating potential. Clearly, different force estimates would result when using a 20 cadaver-based estimate of pennation angle and a value of 40 measured in vivo when modeling the force contribution of the Sol to the Achilles tendon force. Achilles tendon force during walking is large, in excess of 2,000 newtons (Finni et al., 1998; Komi et al., 1992), and thus to best represent the actual force generated by the fibers one should use anatomically realistic values for pennation angle. To this end, one of the main findings of our study was that male subjects had significantly larger optimal pennation angles for the TA, MG, and Sol compared with the female subjects (Figure 5). Even though the difference for the TA was only 2 and would not likely affect muscle force estimates, the difference for the gastrocnemii was approximately 7, and a 14 difference was noted for the Sol. 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