Training-induced changes in architecture of human skeletal muscles: Current evidence and unresolved issues

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1 J Phys Fitness Sports Med, 5 (1): (2016) DOI: /jpfsm.5.37 JPFSM: Review Article Training-induced changes in architecture of human skeletal muscles: Current evidence and unresolved issues Ryoichi Ema 1,2*, Ryota Akagi 3, Taku Wakahara 4 and Yasuo Kawakami 5 1 Graduate School of Engineering and Science, Shibaura Institute of Technology, 307 Fukasaku, Minuma-ku, Saitama-shi, Saitama , Japan 2 Japan Society for the Promotion of Science, Kojimachi, Chiyoda-ku, Tokyo , Japan 3 College of Systems Engineering and Science, Shibaura Institute of Technology, 307 Fukasaku, Minuma-ku, Saitama-shi, Saitama , Japan 4 Faculty of Health & Sports Science, Doshisha University, 1-3 Tatara, Miyakodani, Kyotanabe, Kyoto , Japan 5 Faculty of Sport Sciences, Waseda University, Mikajima, Tokorozawa, Saitama , Japan Received: December 18, 2015 / Accepted: January 8, 2016 Abstract The present review summarizes current evidence and unresolved issues regarding training-induced changes in the architecture of human skeletal muscles. As architectural parameters, we focused on the fascicle length and pennation angle, which are related to force-generating capability of pennate muscles. Cross-sectional studies in sport athletes suggested changes in both the parameters following chronic sport-specific activities. Longitudinal training intervention experiments indicated direct evidence of the plasticity of the two parameters induced by resistance training, but no consensus has been reached regarding the factors influencing those changes. Considering the importance of fascicle arrangement on muscle function, future studies are required to explain the underpinning mechanisms of the adaptation. Keywords : muscle architecture, fascicle length, pennation angle, muscle hypertrophy, athlete, resistance training Introduction Muscle architecture (size and geometrical fascicle arrangement within a muscle) determines functional features of a skeletal muscle 1). Development of tissuevisualizing techniques enabled us to examine the muscle architecture in vivo in humans, which could only be acquired directly from cadavers previously 2,3). Regarding the fascicle arrangement, a large number of studies measured fascicle length and/or pennation angle using real-time B- mode ultrasonography (Fig. 1). Measurements of the two parameters have been conducted by attaching the probe to the skin parallel to the fascicle s longitudinal axis. In an ultrasound image, a fascicle length is defined as the distance between the intersection points of the fascicle and deep and superficial aponeuroses. In a strict sense, a pennation angle is defined as an angle between muscle fascicles and the muscle line of action. But the word is frequently used as the representation of an angle between the fascicles and aponeurosis of the muscle. Thus, in the present review, we use the term of pennation angle as the angle of between the fascicles and aponeurosis. Fascicle length is associated with the maximal shortening velocity 4) and force-length relationship 5). A pennation *Correspondence: i039491@sic.shibaura-it.ac.jp angle influences the efficiency of force transmission from a muscle to tendon 6). Also, the pennation angle could have a positive effect on muscle shortening velocity, at least, during unloaded joint motions 7). To our knowledge, in 1992, two studies for the first time reported the fascicle length and pennation angle in vivo in humans using ultrasonography. In one study, Henriksson-Larsen et al. 8) measured the fascicle length and pennation angle of the vastus lateralis (VL) and evaluated the repeatability of measurements. The results showed that acquisition of the longitudinal image of ultrasound can be applied for measurement in humans in vivo. In the other study, Rutherford and Jones 9) measured the pennation angle of VL and vastus intermedius (VI) before and after resistance training for 3 months. They failed to find significant changes in the pennation angle of either of the muscles. Since then, a number of cross-sectional studies which compared muscle architecture between athletes and untrained control subjects have suggested that competitive sport activities have substantial impact on muscle architecture. In addition, some reports indicated the relationship between sport performance and fascicle arrangement within a muscle. Longitudinal intervention studies provided direct evidence about the adaptations of fascicle arrangement due to several kinds of training. However,

2 38 JPFSM: Ema R, et al. Fig. 1 An example of an ultrasound image of a pennate muscle. White straight line indicates a fascicle, and θ shows pennation angle. a consensus has not been reached. In the current review article, first, we focus on the validity and repeatability of measurement of the fascicle length and pennation angle. Then, we summarize previous cross-sectional and longitudinal observations regarding training-induced changes in the fascicle length and pennation angle of skeletal muscles, and show what we know and what remains unresolved. Basically, we reviewed the previous studies in which subjects were healthy humans, and resistance and competitive sport trainings were adopted as a training modality. Validity of measurement of fascicle length and pennation angle Validity of the fascicle length and/or pennation angle was examined thorough comparison between directly measured value and ultrasonographic value on cadavers. The number of validation studies is limited. Kawakami et al. 10) compared values of pennation angle of the triceps brachii (TB) obtained by ultrasonography and from cadavers. According to their results, it is possible to measure the pennation angle of TB in vivo with an error of less than 1. Using similar methods, following studies confirmed the validation in the medial gastrocnemius (MG) 11) and biceps femoris (BF) 12), with an error of ~8 mm for fascicle length, and ~3 for pennation angle, respectively. Recently, validation of the semitendinosus 13), VL 14), VI 14), vastus medialis (VM) 15) and rectus femoris (RF) 16) was confirmed. Taken together, the validity of ultrasound measurement was confirmed at least for large limb muscles, under a relaxed condition without joint motion 17). Repeatability of measurement of fascicle length and pennation angle Repeatability of measurement of the two parameters was reported in the 1990 s. Henriksson-Larsen et al. 8) measured the fascicle length and pennation angle of VL three times on different days. From the results of an analysis of variance (ANOVA) for the measured values, they regarded the measurement as a reliable method. The ANOVA, however, is not a valid way to evaluate the variation of the repeated data. The other indices, such as the coefficient of variation (CV) and intraclass correlation coefficient (ICC) are mainly reported to evaluate the repeatability of a measurement. Rutherford and Jones 9) measured the pennation angles of VL and VI, and the CV of repeated measurement on different days was 13.5%. Narici et al. 11) measured the fascicle length and pennation angle of MG seven times on a subject, and reported that the CVs were 5.9% and 9.8% for the fascicle length and pennation angle, respectively. Fukunaga et al. 18) measured VL fascicle length and pennation angle twice on different occasions and reported that the CVs were 2.1% and 0.8%, respectively. Day-to-day repeatability of VL pennation angle measurement was reported to be 3.2% (CV) and (ICC), respectively 19). These results indicate that repeatability of fascicle length and pennation angle measurements is high and warrant the use of ultrasonography for examining the architectural characteristics and plasticity of pennate muscles in vivo in humans. Plasticity of fascicle arrangement Cross-sectional study A number of cross-sectional studies indicated event-related profiles of the fascicle arrangement in athletes 10,20-34). Some of them suggested the importance of the arrangement on human movements and sport performance. Regarding the fascicle length, elite track-and-field sprinters had greater fascicle lengths of VL and MG compared to control subjects 21). A similar finding was indicated in sprinters fascicle length of the lateral gastrocnemius (LG) 35). A positive association was shown between the sprint performance and fascicle lengths of VL, MG

3 JPFSM: Training-induced changes in muscle architecture 39 and LG 32) or those of VL and LG 22). Sprint performance over the distance of a sprint to second base in female softball players was correlated with VL fascicle length 36). For recreationally active subjects, the fascicle length of RF was positively related to the 30 m sprint speed 37). Also, a positive relationship was indicated in swimmers between sprint performance of crawl and fascicle lengths of VL and LG 33,34). These findings may suggest that the fascicle length of lower extremity is an important factor for sprint ability, although the investigated muscles were limited to VL, RF or the gastrocnemius, and only a correlation was shown in each study. Furthermore, VL and TB fascicle length was positively associated with dynamic resistance performance in powerlifters 23). Sumo wrestlers, who need explosive power output during competitive activities, had longer fascicle lengths of TB, VL and MG than agematched untrained control subjects 30). Cross-sectional studies cannot deny a possibility of inherited profiles in athletes. However, since there were some variances in the fascicle length of MG between monozygous twin pairs, environmental factors as well as genetic factors would contribute to the variances in muscle fascicle arrangement 38). On the other hand, a recent study examined fascicle lengths of VL and MG in highly trained athletes (bodybuilders and rugby players) at three joint angles 24), and no differences were observed between the athletes and control subjects. These findings indicate that characteristics of fascicle length differ among the sport events. It is difficult to discuss the discrepancy in terms of the training regimens. The ratio of inclusion of sport-specific training (e.g., sprint training) and resistance training during daily competitive activities may depend on coaches and competitive levels, which might be associated with the discrepancy. In fact, the top level of competitive weightlifters, who frequently include resistance training in their training activities, had a greater VL pennation angle than resistance-trained subjects with a similar VL muscle thickness between the two groups 39). With respect to the pennation angle, Kawakami et al. 10) showed that bodybuilders had a much larger pennation angle (mean, 33, range 15 to 55 ) of TB compared to untrained control subjects (mean, 15 ). This large pennation angle in bodybuilders can reduce the efficacy of force transmission from muscle fibers to tendon. In fact, a negative relationship between pennation angle and muscle force per its anatomical cross-sectional area 25-27) and resistance exercise performance 23) have been shown in highly trained athletes. Highly trained bodybuilders and rugby players had greater pennation angles of VL and MG compared to control individuals 24). Ichinose et al. 25) examined event-related and gender differences in TB pennation angle of highly trained soccer players, gymnasts and judo athletes, and demonstrated that judo athletes had the largest pennation angle, and the gymnasts only showed a gender difference. A unique observation was reported in VL. Kearns et al. 30) observed a significant difference in TB, MG, and LG pennation angles between the sumo wrestlers and untrained subjects, but failed to find a corresponding difference in VL pennation angle. A positive correlation was indicated between muscle thickness and pennation angle of TB, but not of VL, in football players 20) and power lifters 23). On the other hand, Kawakami et al. 40) obtained data of muscle thickness and pennation angle of VL, MG and TB from 711 subjects, including sedentary individuals to highly trained athletes. They demonstrated a clear relation between muscle thickness and pennation angle in the three muscles (Pearson product-moment correlation coefficients, r = 0.81, 0.61, 0.56 for TB VL, and MG, respectively). This clear relation in TB was also shown in competitive athletes without a sport-specific difference 26). Kawakami et al. 40) added further evidence that the CVs of the muscle thickness and pennation angle were highest in TB, followed by VL and MG. These cross-sectional data raise a possibility that the magnitude of training-induced adaptation of the pennation angle differs among the above three muscles, although this has not been substantiated by direct evidence. Longitudinal study Evidence for fascicle length change In animal experiments, it has been shown that training induces an increase in serial sarcomere number 41,42). For example, Lynn et al. 42) observed that concentric and eccentric training resulted in an increase in the serial sarcomere number in rats. This suggests that resistance training can induce an increase in fascicle length of human muscles in vivo. In the 2000s, some studies showed an increase in fascicle length following resistance or competitive training 43-53). Overall, training-induced increases in fascicle length are accompanied by an increase in muscle size (muscle hypertrophy, which is defined as an increase in muscle fiber area, muscle thickness, anatomical crosssectional area or volume in this article), although four studies failed to find muscle hypertrophy 45,52,54,55) and two studies did not show the data on muscle size 56,57). Two studies observed a decrease in fascicle length of the gastrocnemius with 58) and without 59) muscle hypertrophy, and Timmins et al. 55) showed a decrease in the fascicle length of BF without muscle hypertrophy. It should be noted that some reports 43,45) calculated fascicle length as the muscle thickness divided by the sine component of the pennation angle determined by small probe width, which could involve a large error 14). One of the functional significances of an increase in fascicle length is a corresponding increase in muscle shortening velocity. To the best of our knowledge, however, no studies examined the relations between the changes in these two factors. Recent studies have suggested that eccentric contraction training increases the fascicle length, but concentric training does not, or that the extent of increase in fascicle length is greater after eccentric contraction training than after concentric contraction or conventional (both con-

4 40 JPFSM: Ema R, et al. centric and eccentric) training 55,60-63). A recent investigation provided evidence for the importance of lengthening velocity during resistance training 57). Four eccentric contraction training protocols were designed: at 65% of maximal voluntary contraction (MVC) load with 90 /s from 25 to 100 knee joint angle (full extension = 0 ), at MVC load with 90 /s from 25 to 100 knee joint angle, at MVC load with 90 /s from 25 to 65 knee joint angle, and at MVC load with 240 /s from 25 to 100 knee joint angle; and the fascicle length of VL before and after the interventions was compared. They demonstrated that only high muscle lengthening velocity training induced an increase in VL fascicle length. However, other research groups indicated an increase in fascicle length of VL after isometric training 54,64), slow (30 /s) isokinetic concentriconly and eccentric-only training 46) and eccentric-only (60 / s) training 44). Therefore, it is difficult to conclude that eccentric training, especially at high speed, can induce a preferential increase in fascicle length. Unfortunately, most of the previous studies, in which eccentric contraction training was conducted, did not mention any possible factors regarding inconsistencies among the studies. McMahon et al. 48) showed a substantial impact of range of motion of the knee joint (i.e., muscle length change) during training on VL fascicle length change. They demonstrated that fascicle length of VL increased after resistance training for 8 weeks regardless of range of motion, but the magnitude was greater at longer range of motion (0 to 90 ) than at shorter range of motion (0 to 50 ) conditions. In addition, the same research group observed the greater increases in fascicle length and anatomical cross-sectional area of VL following resistance training at lengthened (40 to 90 ) than at shortened (0 to 50 ) muscle positions 65). The optimal length of VL corresponds to about 70 of knee joint 66). Considering the results, fascicle length adaptation might be related to the regions of forcelength characteristics that are operated during training regimens. Future research is needed to clarify this point. Some reports measured a fascicle length at several sites along VL 45,48,54,65,67,68), and observed regional differences in the changes before and after intervention 45,54). Noorkoiv et al. 54) demonstrated that isometric training at a long muscle length position induced an increase in VL fascicle length in the distal region, whereas at a short muscle length position, an increment was shown in the middle region. The underpinning mechanisms for the regional difference in the changes in fascicle length are unclear, but the inconsistent findings about fascicle length adaptation might be partly attributable to such regional differences. Evidence against fascicle length change A lot of previous examinations observed no increase in fascicle length of agonist muscles with significant muscle hypertrophy after isometric 69), conventional 68,70-74) and isoload eccentric 75) resistance training. The above studies 68,70-73,75) observed an increase in pennation angle without an increase in fascicle length. In other words, studies which showed a lack of both fascicle length and pennation angle increases despite significant muscle hypertrophy are limited 76,77). The two studies examined the fascicle arrangement before and after intervention for elderly individuals, implying that adaptation of the fascicle arrangement may be unlikely to occur in elderly people. Evidence for pennation angle change An increase in pennation angle has been considered to be a space-saving strategy for packing muscle fibers with increased diameters into a limited area of aponeurosis 78). Consistent with this idea, a large number of longitudinal studies showed an increase in pennation angle with muscle hypertrophy following resistance training 73,79), although some evidence for a decrease in pennation angle also exists 45,55,80). The majority of previous studies targeted VL 19,46,48-53,61-63,65,69,72,75,79,81,82). Aagaard et al. 79) examined the change in pennation angle of VL induced by several kinds of resistance training for 14 weeks. The results demonstrated a 35.5% increase in pennation angle of VL. Reeves et al. 49) observed a 13% increase in pennation angle of VL following resistance training for 14 weeks in elderly subjects. The same research group 50) confirmed up to 35% increase in pennation angle of VL after the same training program as that of Reeves et al. 49). Blazevich et al. 46) examined the change in pennation angle of VL induced by concentric- or eccentric-only contraction training. They showed a 13.3% increase of the VL pennation angle in the concentric group and a 21.4% increase in the eccentric group, but there was no difference in the extent of increase between the two groups. Compared to VL, investigation of other muscles is limited. Studies have found changes in the pennation angle of each muscle of the quadriceps femoris 68), as well as VL, RF 83,84), BF 55), MG 85), LG 59,86), TB 70,73,87,88), biceps brachii 89), brachialis 89) and supraspinous 90). A positive correlation was shown between the absolute values of muscle thickness and pennation angle for TB 73) and each muscle of the quadriceps femoris 68) before and after the interventions. Moreover, relative changes in muscle size were associated with relative changes in pennation angle for the quadriceps femoris 68) and elbow flexors 89). These studies strongly suggest that a generic hypertrophic process in a pennate muscle is accompanied by an increase in pennation angle. On the other hand, an increase in pennation angle of the gastrocnemius without hypertrophy was indicated after marathon training 59) and complex training (strength and power sets within a single session) 58) or of BF after concentric-only training 55). These results cannot be explained by the strategy mentioned above. It should be noted that the three studies observed a decrease in the fascicle length 55,58,59). Inter- and intra-muscle differences in the changes in pennation angle were also confirmed 45,68,71,84). Resistance training for 12 weeks resulted in an increment in penna-

5 JPFSM: Training-induced changes in muscle architecture 41 tion angles of each of the quadriceps femoris 68), and the magnitude was greater in RF than in VL, VM, and VI. Regional differences in the change in pennation angle of VI were also shown; there was an increase in the medial region, but not in the lateral region 68). Matta et al. 84) compared the effect of conventional and isokinetic resistance training on the pennation angle of RF in the distal and proximal regions. The results indicated a significant increase in RF pennation angle only in the distal region after conventional training. On the other hand, Erskine et al. 71) reported that the pennation angle of VL, but not of VM, VI or RF, increased after resistance training for 9 weeks. These findings indicate that the changes in the pennation angle observed in a certain muscle or a region cannot represent all synergistic muscles 68). Evidence against pennation angle change Some studies failed to find a change in pennation angle despite significant muscle hypertrophy 9,43,91,92). Rutherford and Jones 9) measured the pennation angle of VL and VI before and after knee extension training for 12 weeks, and failed to find significant changes in either of the two muscles. However, since the repeatability of measurement was not so good (the CV of repeated measurements was 13.5%), it may be the reason for the lack of changes in pennation angle. Hoffman et al. 92) found an increase in VL thickness after resistance training for 8 weeks, but did not find such an increase in its pennation angle. Because the subjects in Hoffman et al. 92) were resistance-trained men, and because adaptation of the pennation angle of VL was large within several weeks from the beginning of the training program 46), the lack of change in the pennation angle of VL may have been due to its low responsiveness. Lack of pennation angle adaptation was also demonstrated in MG 93,94) and BF 56), but these studies did not provide data on changes in muscle size. In the discussion of Ema et al. 68), they mentioned that inconsistent results regarding the responsiveness of the pennation angle can be partly explained by the difference in the magnitude of muscle hypertrophy when comparing previous studies. On the other hand, different kinds of training regimens may result in the different adaptations of the pennation angle. Alegre et al. 69) observed an increase in pennation angle of VL after isometric knee extension training at a long muscle length (90 flexion of knee joint) for 8 weeks, but did not after training at a short muscle length (50 flexion of knee joint). These results suggest that muscle length during training influences an adaptation of the pennation angle. However, the difference in response of pennation angle between the two training conditions may be due to the difference in the extent of muscle hypertrophy, because the extent of increase in muscle thickness was greater at the long muscle length than at the short muscle length 69). In fact, preferential muscle hypertrophy was also shown in other studies following isometric training at a long muscle length compared with isometric training at a short muscle length, although they did not measure the pennation angle 54,95). The muscle contraction mode (i.e., isometric, concentric or eccentric) during exercise may be related to the responsiveness of the pennation angle. No adaptations of the pennation angle of VL with muscle hypertrophy have been shown after isokinetic eccentric 44,60,75) or constant external load eccentric training 60). In addition, concentriconly resistance training induced an increase in the pennation angle of VL, but eccentric-only resistance training did not, despite a similar magnitude of muscle hypertrophy between the two training regimens 61,62). Furthermore, eccentric-only training resulted in the decrease in BF pennation angle 55). These findings suggest that eccentric contraction training does not induce an increase in the pennation angle. The reasons for the lack of an increase in the pennation angle remain unclear, but if the aponeurosis, on which hypertrophied muscle fibers are attached, expands substantially in response to resistance training, an increase in the pennation angle is not necessarily needed. Regarding this point, Wakahara et al. 82) indicated that changes in the aponeurosis width after resistance training did not substantially affect the increase in the pennation angle. Moreover, significant increases in pennation angles were also observed after isokinetic eccentric 46,90), isoload eccentric 75) and eccentric-cycling 83) training. Taken together, it is difficult to conclude that eccentric contraction training does not induce an increase in the pennation angle despite significant muscle hypertrophy. Methodological issues and future perspectives It should be noted that some methodological considerations are involved in the previous findings. Some human skeletal muscles have long (> 10 cm) fascicle lengths 96). Because of the insufficient probe width (e.g., 4.5 cm, 6 cm), it is difficult to visualize the whole fascicle length in an ultrasound image. Therefore, a lot of previous studies estimated the fascicle length using several methods such as the linear extrapolation technique and geometrical calculation from muscle thickness and pennation angle. As shown in the cross-sectional study section, athletes who need high-speed and explosive power had long fascicle lengths of the upper and lower extremities, and positive associations were shown between the fascicle length and sport performance 21-23,30,32-37). However, the studies estimated the fascicle length from the muscle thickness and sine of the pennation angle, which could involve a large error 14). In particular, the error should be higher for athletes, who have greater muscle thickness. For example, when muscle thickness is 20 mm, a difference in 1 of pennation angle (15 vs. 16 ) results in a 4.7 mm difference in the fascicle length. When muscle thickness is 30 mm, the corresponding difference in pennation angle leads to a 7.1 mm difference in the fascicle length. Considering this, over- or underestimation of fascicle length is

6 42 JPFSM: Ema R, et al. likely to occur in the data of athletes. This can also apply to longitudinal experiments which involve an increase in muscle thickness. Although validation of a fascicle length estimation using the linear extrapolation method can be confirmed 14), this cannot perfectly eliminate some possibility of error due to fascicle curvature 10) or underestimation of fascicle length due to a three-dimensional fascicle arrangement 97). Because the fascicle length and pennation angle are important parameters in muscle function, a more accurate methodology that takes the above problems into consideration is required. Overall, changes in fascicle arrangement are accompanied by changes in muscle size. The magnitude of an increase in muscle size was related to the extent of an increase in pennation angle 68,89), suggesting that the lack of significant change in pennation angle in the previous reports may result from small effect of training. Fig. 2 shows the relationship between relative changes in muscle size and fascicle length or pennation angle in the cited longitudinal studies. There were significant positive correlations between the relative changes in muscle size and fascicle length (r = 0.28, P = 0.014) or pennation angle (r = 0.34, P < 0.001). If we compare the magnitudes of changes in muscle size between the studies which showed a significant change in fascicle length or pennation angle and studies which did not, they are 12.4 ± 10.5% vs. 7.7 ± 8.9% for fascicle length, and 13.5 ± 10.5% vs. 7.7 ± 9.3% for pennation angle, respectively. These results clearly indicate that changes in fascicle arrangement induced by training are associated with the magnitude of sizable adaptation of the muscle. In contrast, some results showed a large extent of changes in muscle size and the two parameters, but with no statistical significance in the changes in the two parameters. These contrasting results may be due to the methodological issues mentioned above or insufficient reproducibility. Considering these points, one possible solution to overcome the discrepancies among the previous studies and to clarify the underpinning mechanisms for the adaptation of the fascicle arrangement is to re-examination the data using a more accurate methodology and several types of training regimens which induce 10% or greater muscle hypertrophy. Summary Previous cross-sectional and longitudinal studies revealed that fascicle arrangement has substantial plasticity. The characteristics of fascicle length in athletes suggest the importance of fascicle length in sprint performance, but this has not been substantiated by longitudinal observations and methodological consideration is involved. Sport-specific training and resistance training might cause a different response of fascicle length and pennation angle. In many cases, the changes in the two parameters are accompanied by changes in muscle size. Eccentric contraction training may result in a specific adaptation of Fig. 2 Relationships between relative changes in muscle size and fascicle length (left) or pennation angle (right) in previous longitudinal data. If a study investigated some muscles and/or regions, all data were involved. The results of control groups in each study were eliminated. The data was divided into four types of plots in terms of the existence of significant changes in muscle size, fascicle length and pennation angle. White circle ( ), significant changes in both muscle size and fascicle length or pennation angle; Gray triangle ( ), significant change in muscle size and insignificant change in fascicle length or pennation angle; Gray square ( ), insignificant change in muscle size and significant change in fascicle length or pennation angle; Cross ( ), insignificant changes in both muscle size and fascicle length or pennation angle.

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