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Regional Elastic Properties of the Achilles Tendon Is Heterogeneously Influenced by Individual Muscle of the Gastrocnemius

Regional Elastic Properties of the Achilles Tendon Is Heterogeneously Influenced by Individual... Hindawi Applied Bionics and Biomechanics Volume 2019, Article ID 8452717, 10 pages https://doi.org/10.1155/2019/8452717 Research Article Regional Elastic Properties of the Achilles Tendon Is Heterogeneously Influenced by Individual Muscle of the Gastrocnemius 1 2 1 1 3 Jiping Zhou, Jiafeng Yu, Chunlong Liu, Chunzhi Tang, and Zhijie Zhang Clinical Medical College of Acupuncture, Moxibustion, and Rehabilitation, Guangzhou University of Chinese Medicine, Guangzhou, China Department of Rehabilitation Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Luoyang Orthopedic Hospital of Henan Province, Orthopedic Hospital of Henan Province, Luoyang, China Correspondence should be addressed to Zhijie Zhang; sportspt@163.com Received 6 April 2019; Revised 2 August 2019; Accepted 19 September 2019; Published 3 November 2019 Academic Editor: Craig P. McGowan Copyright © 2019 Jiping Zhou et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Background. Anatomical studies and the mechanical property studies showed that there is a strong correlation between Achilles tendon (AT) elasticity and individual gastrocnemius muscle (the medial head of gastrocnemius (MG) and the lateral head of gastrocnemius (LG)) elasticity. Limited ankle dorsiflexion range of motion has been correlated with decreased flexibility of the MG/LG/AT complex. However, no studies have been conducted to examine the exact correlation between the Achilles tendon and the individual muscle of the gastrocnemius. Purposes. The purposes of the present study were (1) to evaluate intra- and interoperator reliabilities of elastic property measurements in the gastrocnemius muscle-Achilles tendon complex by using the shear wave elastography (SWE) and (2) to examine the correlation between the regional elastic properties of the AT and the individual muscle of the gastrocnemius. Methods. Twenty healthy subjects (mean age: 22.50 (3.02) years) were recruited in this study. The elastic properties of the AT and the individual muscle of the gastrocnemius were quantified using the SWE. Findings. The SWE has comparatively high reliability in quantifying the elastic properties of the muscle-tendon range from good to excellent. The intraoperator ICC of the gastrocnemius muscle-Achilles tendon complex was 0.77 to 0.95, while the interoperator ICC was 0.76 to 0.94. The minimal detectable change (MDC) of the muscle was 1.72 kPa, while the AT was 32.90 kPa. A significant correlation was found between the elastic modulus of AT and the elastic modulus of the MG (r =0:668 and p =0:001 at the relaxing position and r =0:481 and p =0:032 at the neutral position). Conclusions. The SWE has the potential to assess localized changes in muscle-tendon elastic properties, provide more intuitive relations between elastic properties of the muscle tendon and function, and evaluate the therapeutic effect of the muscle tendon. A significant correlation between the AT and the MG was found, and it may provide a new treatment idea (targeted to the tight muscle heads) for the clinical setting to treat subjects with AT disorders. they descend but do not run in parallel to each other [4]. In 1. Introduction addition, the posterior part (i.e., superficial part) of the Achil- The Achilles tendon (AT), which is the conjoined tendon of les tendon is formed by the fascicles of the tendons of the the gastrocnemius and soleus muscles, is the strongest and medial gastrocnemius (MG), while the anterior part (i.e., largest tendon in the body [1, 2]. Anatomical studies describe deep part) consists of the lateral gastrocnemius (LG) and the Achilles tendon as the tendon that starts at the musculo- soleus muscles [5]. Furthermore, the LG is shorter and tendinous junction of the soleus and gastrocnemius, which smaller than the MG so that the lateral head and the medial becomes rounded and flattened in the junction with the gas- head of the gastrocnemius vary in their force contribution trocnemius [3]. The twisted structure of the Achilles tendon to the Achilles tendon [3]. It has been reported that flexibility is formed by individual subtendons which instead rotate as is a component of joint fitness, as it is thought to be 2 Applied Bionics and Biomechanics associated with athletic performance and the incidence of and reliable tool to estimate the elastic properties of the ten- injury [6, 7]. Note that in all the previous studies, flexibility don. There is a significant correlation between the elastic was assessed by measuring the maximal range of passive joint modulus of the tendon captured from SWE and the tangent motion [8, 9]. However, the passive range of joint motion traction modulus computed from a material testing system depends on muscle flexibility or, alternatively, tendon exten- [23]. In addition, Eby et al. revealed that the SWE is valid sibility. However, previous studies did not conduct studies of technique to estimate the elastic properties of the muscle. the individual muscle of the triceps calf muscle, and current A positive significant correlation was found between the research is still focused on mixed muscles or group muscles. elastic modulus of the muscle from the SWE and the elastic Besides, Green et al. found that muscle heads of the soleus modulus from a material testing system [24]. Furthermore, versus the gastrocnemius may differ when exercise induced the SWE was also used to examine the elastic properties of passive muscle tension on the muscle [10]. In summary, there the infraspinatus, erector spinae, and gastrocnemius mus- is a strong correlation between the Achilles tendon and the cles, rotator cuff, sternocleidomastoid, Achilles tendon, and gastrocnemius. However, no studies have been conducted patellar tendon [25–29]. Thus, the SWE can provide an to examine the exact correlation between the Achilles tendon opportunity to monitor the change in the elastic modulus and the gastrocnemius. of the gastrocnemius and the Achilles tendon at various The main function of the AT is the plantar flexion of the angles of the ankle joint. ankle, determining the human body’s jumping and running The objectives of this study were (1) to evaluate intra- [11]. Joint flexibility is influenced by musculotendinous and interoperator reliabilities of the elastic modulus mea- surement in the gastrocnemius muscle-Achilles tendon com- structures around the joint. The tendinous tissues are known plex by using the SWE and (2) to examine the correlation to possess elastic characteristics which are a critical determi- nant of the proper muscle force transmission and movement between the regional elastic properties of the Achilles tendon and the individual muscle of the gastrocnemius during vari- generation [12]. Muscle elasticity is the key determinant of ous angles of ankle joint flexion. the capacity of the muscle to contract [13]. Although there are different functions between the skeletal muscle and the 2. Methods tendon, modulation in the elastic properties of the muscle tendon can reflect the pathological change and recovery 2.1. Ethics Statement. This study was approved by the Human effect. In our previous study, we have explored the interplay Subjects Ethics committee of the Clinical Medical College of between passive muscle tension of the vastus lateralis and Acupuncture, Moxibustion, and Rehabilitation. All subjects rectus femoris muscles and patellar tendon stiffness. Greater were fully informed of the purpose and experimental proce- passive tension in the vastus lateralis was associated with dures and signed the informed consent before the study. higher patellar tendon stiffness in male athletes. In addition, previous studies have investigated that stiffer AT and gas- 2.2. Participants. Twenty healthy subjects (14 males and 6 trocnemius have been found to be risk factors associated with females; age: 18–28 years) were recruited in this study. Inclu- Achilles tendinitis [14–17]. Reduced flexibility of the gastroc- sion criteria were that all participants were healthy and did nemius muscle and the AT can lead to an increase in lower- not have a history of ongoing neuromuscular diseases or extremity injuries. Increasing the stiffness of the muscle ten- musculoskeletal injuries specific to the ankle or knee joints don could limit the range of joint motion and increase the during the previous six months. Exclusion criteria included risk of injury [18]. Moreover, Gajdosik et al. found that the pain in the gastrocnemius and Achilles tendon, participants flexibility of the ankle joint depends on the extensibility of taking fluoroquinolone antibiotics, lower limb fracture, post- musculotendinous structures, especially the gastrocnemius operative rupture of the Achilles tendon, or anomaly on [19]. Similarly, the gastrocnemius-Achilles tendon unit has ultrasound. been suggested to be a major contributor to passive joint stiff- ness [20]. Both of them cannot separate the muscle-tendon 2.3. Equipment and Parameter Setting. An ultrasound shear unit into respective components. Thus, accurately quantify- wave elastography system (Aixplorer Supersonic Imagine, ing the elastic properties of isolated regional areas of the France) with a 40 mm linear array transducer (SL10-2, Super- MG, LG, and AT may provide a more comprehensive under- sonic Imagine, France) was used. The settings of the SWE standing about the biomechanics of the MG, LG, and AT. system were set as follows: the instrument was set in the mus- Shear wave elastography (SWE) is a noninvasive tech- culoskeletal mode. The frequency was 2~10 MHz. The SWE nique to quantify the elastic properties of soft tissues. It can Opt was the penetration mode. The opacity was 85%. The be used to estimate the elastic modulus of the regional area elastic modulus range of the gastrocnemius was 0~200 kPa, through the shear wave speed. The principle of SWE is (1) while the elastic modulus range of the Achilles tendon was to create a shear wave through acoustic radiation force, (2) 0~800 kPa. The color scale used in the shear modulus (in to use sonography to map the distortion induced by the wave kPa) showed the lowest values in blue to the highest values in the measuring object, and (3) to trace the wave back to the in red. The depth of the B-scan was 3.0 cm [30]. For the mechanical properties of the measuring object by using the Achilles tendon, the size of the regions of interest (ROI) relationship E =3pc had to be set to 25 ∗ 12 mm and the Q-Box™ diameter was [21]. The SWE was used to quantify the elastic properties of the skeletal muscle and tendon. The defined by the thickness of the tendon, which was the dis- stiffer the tissue, the greater the shear modulus (kPa) [22]. tance between the superior and inferior borders of the Achil- Our previous studies demonstrated that the SWE is a valid les tendon [23]. For the MG and LG, the size of the ROI had Applied Bionics and Biomechanics 3 each subject’s Achilles tendon, MG, and LG over a 1-hour to be set to 10 ∗ 10 mm and the diameter of the Q-Box™ is 5 ∗ 5mm [31]. The transducer was positioned along period and by operator ZJ with a 2-hour interval. In the sec- the longitudinal axis of the AT, MG, and LG. ond test, the same subjects attended at the same time 5 days later, which was repeated by operator ZJP for the intraopera- 2.4. Experimental Design and Protocol tor investigation. Subjects were explicitly asked to refrain from any additional exercise throughout the duration of test- 2.4.1. Measurement Position. The dominant leg was identified ing but to maintain their normal daily walking activity [28]. by kicking a ball [32]. Before testing, subjects were asked to The results were not communicated between operators ZJP wear loose-fitting clothes. During testing, each subject was and ZJ until all subjects had been examined. allowed to lie in the prone position with the foot relaxed and hung over the lower edge of the treatment bed, the hip and knee joints fully extended, and the upper limbs placed 2.4.3. Statistical Analysis. Statistical analysis was performed on both sides of the body [32]. The joint was fixed using a using SPSS Version 19.0 (SPSS, Chicago, IL). All data were customized and movable ankle foot orthosis (AFO) at the presented by the mean (standard deviation). The intraclass neutral anatomical position (the strap of the AFO was tight- correlation coefficient (ICC) was calculated to determine ened until a 90 ankle joint position was achieved, measured the intra- and interoperator reliabilities. The coefficient of by a hand-held goniometer [33]) and resting ankle angle variance (CV), the standard error measurement (SEM), and (participants took what they perceived to be a “relaxed” foot the minimal detectable change (MDC) were calculated (all position [34, 35]). The measurement site of the Achilles ten- based on the following formulae: CV = ðstandard deviation/ pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi don was defined as 0 cm (the most proximal outline of the meanÞ ×100%, SEM = standard deviation × ð1 − ICCÞ,and pffiffiffi calcaneus) and 3 cm above the calcaneal tuberosity [36], MDC = 1:96 × SEM × 2). Pearson correlation analysis (r) while the MG and LG were defined as the proximal 30% of was used to examine the correlation between the shear mod- the lower leg length [37]. The length of the MG is that mea- ulus of the Achilles tendon and the gastrocnemius muscle. sured from the popliteal fossa to the lateral malleolus, where The strength of reliability coefficients was classified as fol- cross-sectional areas of the gastrocnemius are almost maxi- lows: excellent (more than 0.90), good (0.71–0.90), moderate mum. As for the LG, the length is that measured from the (0.50–0.70), and poor (less than 0.50) [39]. The statistical sig- popliteal fossa to the medial malleolus. The length was mea- nificance was set at an alpha level of p <0:05 (α =0:05). sured by a tape measure, and a black pen was used to mark the location of the measurement site (Figure 1). In addition, to reduce experimental errors, subjects were explicitly asked 3. Results to keep the lower extremity as fully relaxed throughout the duration of testing and refrain from high intensity exercise 3.1. Intra- and Interoperator Reliabilities. The intra- and for 48 hours before testing [32]. Room temperature was interoperator reliabilities of the shear modulus exponent of maintained at 25 Cto reduce the effect of temperature on the MG, LG, and Achilles tendon is shown in Tables 1 and the elasticity of musculature [38]. 2, respectively. The results indicated that the intraoperator ICC for the MG, LG, AT0cm, AT3cm was 0.77 to 0.95 and 2.4.2. Ultrasound Shear Wave Elastography. Before measure- the interoperator ICC was 0.76 to 0.94. The intraoperator ments, subjects were asked to relax for 5 min to ensure that reliability for the measurement site of the LG (relaxing posi- the triceps surae was relaxed. During measurements, enough tion), MG (neutral position), LG (neutral position), and ultrasound gel was applied between the skin and the trans- AT0cm (neutral position) is excellent. The interoperator ducer to avoid skin deformation. The midpoint of the trans- reliability for the measurement site of the LG (relaxing posi- ducer was placed perpendicularly on the skin’s surface with tion) and AT3cm (neutral position) is excellent. The rest of a light pressure where we marked before, and then the the ICC values reveal good intra- and interoperator reliabil- mode of the SWE was activated to examine the shear wave ities. The MDC (kPa) for the MG, LG, AT0cm, and AT3cm modulus of the muscle or tendon [32]. During the acquisi- were 3.24 to 8.07, 1.72 to 6.44, 35.91 to 60.28, and 32.90 to tion of the mode of the SWE, the transducer was kept 43.42, respectively. motionless for about 5-8 s [23]. Then, the gray scale image showed the appearance of the muscle or tendon under the longitudinal section. Image quality was closely monitored 3.2. The Relationship between the Shear Modulus of AT and throughout the measurements. When the color in the ROI MG and LG. The r values and P values of the AT and MG was uniform and several muscle fibers or the superior and and LG for different ankle joint positions are shown in inferior borders of the tendon were continuously visible, Table 3. A significant correlation was found between the the images were frozen and then put on the Q-Box™ to AT0cm and MG (r =0:668 and p =0:001 at the relaxing posi- obtain the shear wave modulus from the system and stored tion and r =0:481 and p =0:032 at the neutral position) for off-line analysis (kPa) (Figure 2). Three images were (Figure 3). In addition, the correlation between the MG and captured at each measurement site of the tendon and mus- AT3cm was weak (r =0:146 at the resting position and cle. The mean of the elastic modulus from all 3 images was r =0:358 at the neutral position). Furthermore, no significant used for further analyses. correlation was apparent in the shear wave modulus results Two operators (ZJP and ZJ) participated in the intero- between the LG and AT, in which the correlation coefficient perator investigation. The operators took turns to examine is 0.078 to 0.199. 4 Applied Bionics and Biomechanics MG LG AT3 cm AT0 cm (a) (b) (c) Figure 1: The location of the measurement site. (a) MG: at the midpoint of the oblique line connecting the inside of the popliteal transverse line and the highest point of the malleolus lateralis. (b) LG: at the midpoint of the oblique line connecting the outside of the popliteal transverse line and the highest point of the malleolus medialis. (c) AT0cm: 0 cm above the calcaneal tuberosity; AT3cm: 3 cm above the calcaneal tuberosity. (a) (b) (c) (d) Figure 2: Changes of the elastic modulus of MG converted from the resting ankle angle to the neutral anatomical position (from (a) to (b)). The elastic modulus of AT0cm and AT3cm in the resting ankle angle (from (c) to (d)). The color-coded box presentation of muscle-tendon elasticity is shown in the upper images. The longitudinal grey scale sonograms of the muscle tendon are shown in the bottom images. The Q-Box™ is shown on the right. 4. Discussion ities to quantify the elastic modulus of the gastrocnemius- Achilles tendon complex and a significant positive correla- The main findings of the present study were that the SWE tion was obtained between the elastic modulus of the AT0cm had moderate to excellent intra- and interoperator reliabil- and MG, but not found for LG. Applied Bionics and Biomechanics 5 Table 1: Intraoperator reliability of mean elastic modulus values of MG, LG, and AT. Measurement position Test 1 (kPa) Test 2 (kPa) MDC (kPa) 95% CI CV (%) SEM (kPa) ICC MG (R) 17:82 ± 2:92 17:85 ± 3:47 3.24 0.61-0.94 16.39 1.17 0.84 14:19 ± 3:28 14:60 ± 2:53 LG (R) 1.98 0.79-0.97 17.33 0.72 0.92 426:04 ± 34:62 422:83 ± 32:91 AT0cm (R) 43.75 0.42-0.91 7.78 15.78 0.77 415:19 ± 38:44 402:59 ± 35:75 AT3cm (R) 42.04 0.54-0.93 8.88 15.17 0.82 49:49 ± 9:21 49:98 ± 9:50 MG (N) 7.66 0.78-0.96 18.61 2.76 0.91 39:14 ± 7:01 38:95 ± 6:71 LG (N) 4.16 0.88-0.98 17.91 1.50 0.95 563:52 ± 54:37 568:53 ± 51:84 AT0cm (N) 43.11 0.76-0.96 9.12 15.55 0.91 529:07 ± 44:86 525:27 ± 41:51 AT3cm (N) 39.86 0.71-0.95 7.90 14.38 0.88 R: relaxing position; N: neutral position; LG: lateral gastrocnemius; MG: medial gastrocnemius; AT: Achilles tendon; MDC: minimal detectable change; 95% CI: 95% confidence interval; CV: coefficient of variation; SEM: standard error in measurement; ICC: intraclass correlation coefficient. Table 2: Interoperator reliability of mean elastic modulus values of MG, LG, and AT. Measurement position Operator ZJP (kPa) Operator ZJ (kPa) MDC (kPa) 95% CI CV (%) SEM (kPa) ICC 17:82 ± 2:92 18:21 ± 3:96 MG (R) 3.97 0.39-0.90 16.39 1.43 0.76 14:19 ± 3:28 14:19 ± 2:54 LG (R) 1.72 0.84-0.97 17.90 0.62 0.94 426:04 ± 34:62 428:83 ± 39:48 AT0cm (R) 35.91 0.70-0.91 8.13 12.95 0.86 415:19 ± 38:44 407:43 ± 32:66 AT3cm (R) 43.42 0.43-0.91 8.02 15.66 0.77 49:49 ± 9:21 51:68 ± 9:42 MG (N) 8.07 0.76-0.96 18.61 2.91 0.90 39:14 ± 7:01 41:36 ± 7:87 LG (N) 6.44 0.73-0.96 17.91 2.32 0.89 563:52 ± 54:37 565:39 ± 60:93 AT0cm (N) 60.28 0.61-0.94 9.65 21.75 0.84 529:07 ± 44:86 535:78 ± 42:13 AT3cm (N) 32.90 0.84-0.97 7.86 11.87 0.93 4.1. Intra- and Interoperator Reliabilities. The results of the Table 3: Relationships of the elastic modulus between the AT and MG and LG. present study demonstrated that the SWE has high intra- and interoperator reliabilities for quantifying the elastic mod- AT0cm (R) AT3cm (R) ulus of the AT, MG, and LG. The relatively low SEM and ∗∗ MGR 0.668/0.001 0.146/0.540 MDC values revealed good precision of the measurements. The MDC is the smallest change in score that likely reflects LGR 0.09/0.970 0.078/0.745 true change (not measurement error alone). Comparing with AT0cm (N) AT3cm (N) those of previous studies, our study results revealed good to 0.481/0.032 MGN 0.358/0.121 excellent intra- and interoperator reliabilities for quantifying LGN 0.199/0.399 0.143/0.547 the shear modulus of the Achilles tendon and gastrocnemius ∗∗ Data are r value/P value. R: relaxing position; N: neutral position. p <0:01 muscle. Chino et al. found that ultrasound elastography was a and p <0:05. reliable and valid quantitative method for quantifying the stiffness of the gastrocnemius muscle, in which interoperator reliability was 0.77~0.89 [40]. Also, Fu et al. evaluated the elasticity of the normal Achilles tendon among 326 healthy during rest, in which the intraoperator reliability of MG was subjects older than 18 years which were divided into different 0.98, while the AT was 0.82~0.93 [42]. groups by age. The results of this study were that the intrao- In addition, a threshold of ≤12% for the CV is regarded as perator reliability was 0.93 [28]. In addition, Taş et al. made a an acceptable level of biological measurement [43]. The study to examine the intra- and interoperator reliability levels results of the present study indicated that the CV of the for the stiffness of the rectus femoris muscle and patellar ten- MG and LG was 16.39% to 18.61%, which were a little differ- don. They found that the intraoperator reliability of the patel- ent with the CV values of recent research. There is corrobo- lar tendon was 0.81~0.83 and the interoperator reliability was ration with the study by Lima et al. who observed values of 0.71. For the stiffness of the rectus femoris muscle, the intrao- 17.29% to 20.95% for the MG [42], while Chino and Takaha- perator reliability was 0.93~0.94 and the interoperator reli- shi observed values of 19.4% for the MG [44]. The possible ability was 0.95 [41]. Furthermore, Lima et al. found good reason is that we cannot ensure that the probe was completely intraoperator reliability between the AT and MG, bilaterally, parallel to the muscle fibers. However, the shear wave 6 Applied Bionics and Biomechanics 460 600 400 500 340 400 12 14 16 18 20 22 24 35 40 45 50 55 60 65 70 MG at relaxing position MG at neutral position (a) (b) Figure 3: The plots show the correlations of AT0cm and MG at different angles. (a) Relaxing position: r =0:668, p =0:001; (b) neutral position: r =0:481, p =0:032. modulus values depend on the probe in relation to the fiber muscle-tendon shear modulus of the abnormal side) and treatment (pretreatment vs. posttreatment) [53]. Moreover, direction [45]. Brum et al. showed that the shear wave veloc- ity dispersion was influenced by viscosity when the probe is SWE has the characteristics of tracking the changes in the perpendicular to the fibers, but it was not found parallel to shear modulus of the gastrocnemius muscle and Achilles ten- the fibers [46]. Although the CV of the MG and LG in the don. It may provide a basis to reflect a real change for exam- present study was slightly higher than 12%, the ICC of the ining the effectiveness of an intervention [50]. MG and LG values were 0.76 to 0.95, so the data of the muscle were all classified as acceptable. The CV of the Achilles ten- 4.2. The Relationship between the Shear Modulus of AT and don were 7.78% to 9.65%, which confirmed the high reliabil- MG and LG. A significant positive correlation was obtained between the elastic modulus of the MG and AT, but not ity of the shear elastic modulus values of the Achilles tendon, in agreement with a previous study (7.2% to 9.4%) [47]. found for LG. This is the first study wherein a concurrent Furthermore, the MDC was calculated to provide a value investigation of the gastrocnemius muscles and regions to reflect a real change that could be interpreted as a real dif- within the Achilles tendon has been undertaken. In the view ference exceeding the measurement error, which can serve of biomechanics, the transmission and generation of triceps surae muscle forces were affected by the compliance of the as a reference for future study. Our results showed that the MDC of the muscle was 1.98 kPa (the same operator) and AT. Increasing AT compliance can alter the gastrocnemius 1.72 kPa (different operator), while the Achilles tendon was muscle and soleus muscle fiber operating lengths and muscle 32.90 kPa (the same operator) and 39.86 kPa (different excitations. And these effects in gastrocnemius muscles are operator). Therefore, the shear wave modulus of the MG more pronounced than in soleus muscles, which possibly arise from essential differences of muscle-tendon behavior. and LG should be greater than 1.72 kPa and the Achilles tendon should greater than 32.90 kPa to reflect changes with Gastrocnemius muscle fiber negative work decreased pro- retested tests. gressively with increasing AT compliance during the stretch- Recently, due to the high specificity and sensitivity of the ing phase while that of soleus muscles increased for 5% [54]. SWE, it has been used in practical applications [48]. For In addition, an imbalance of force generation between the MG and LG has also been speculated to contribute to the example, Point et al. found that the SWE can monitor the increase of muscle stiffness after cryotherapy induction development and/or persistence of Achilles tendinopathy or [49]. On the other hand, the SWE can be used to detect the pain of the Achilles tendon [55]. On the one hand, both side-to-side differences in tendon geometry and mechanical the MG and LG have the same function of plantarflexion properties in tendon structure in individuals with Achilles but have different degrees of contribution, with the MG pro- viding more than 70% of the muscle force [2]. On the other tendon rupture. This information may give clinical staff a clear understanding of the relationship between tendon hand, the possible explanation is that the MG is longer and structure and clinical manifestation [50]. Furthermore, it larger and extends more distally in the calf than the LG [3] has been reported that the stiffness of congenital myopathies and muscle volume of the MG was higher than the LG [56]. was changed. For example, the stiffness of cerebral palsy and Furthermore, a study reported that the Achilles tendon has a unique structure that is the twisted descending structure, Duchenne muscular dystrophy were increased, while decreased in GNE (UDP-N-acetylglucosamine 2- epimerase/N-acetyl- which enables it to handle the functional loads applied to mannosamine kinase) [22, 51, 52]. Thus, the SWE can be the tendon [57]. Pękala et al. found that the torsion of the used to quantify the shear modulus of the gastrocnemius MG is significantly lower than the LG wherein the rotation muscle and Achilles tendon for assisting the clinical diagnosis angle of the LG is about 5 times that of the MG (the fibers (the muscle-tendon shear modulus of the normal side vs. the originating from the LG rotate on average 135:98 ± 33:58 AT0cm at relaxing position AT0cm at neutral position Applied Bionics and Biomechanics 7 not measure the deep muscle. Thirdly, the ankle of partici- while the MG twist 28:17 ± 15:15 ) [1]. In addition, the larg- est component of AT insertion into the calcaneal bone is the pants was placed in a “relaxed” position; muscle tension MG (the mean width of the footprint was 28.3 mm), and the may be affected by the mass moment of inertia of the foot. Further studies will be conducted to investigate the modula- smallest is the LG (the mean width of the footprint was 14.4 mm) [5]. In all the above views of biomechanics, the tion of elastic properties of the mass moment of inertia of changes of the Achilles tendon are closely related to the the foot. Finally, only healthy subjects and only 2 angles of MG, and the proportion of the MG contribution is larger the ankle were recruited in this study. Further studies will than that of the LG contribution to the Achilles tendon. be conducted to investigate the modulation of elastic proper- ties of the Achilles tendon and gastrocnemius among indi- The elastic properties of the Achilles tendon were closely related to the MG in various exercise programs. For example, viduals with Achilles tendon disorders. during an acute bout of eccentric heel drop exercise, the gas- trocnemius muscles were shown to bear larger mechanical 5. Conclusion loads than the Achilles tendon [58]. Stenroth et al. found that the longer distance walked in a 6-minute walk test was signif- The SWE can be used to quantify regional elastic properties icantly associated with the MG [59]. Besides, Hirata et al. of the Achilles tendon and gastrocnemius. We also found a reported that the passive muscle stiffness differs among the significant correlation between the elastic modulus of the triceps surae. They found a higher elastic modulus of the Achilles tendon and the elastic modulus of the MG, but MG than the LG. After static stretching, a significant reduc- not for the LG. These findings suggested that an increase tion in the elastic modulus of the MG was observed, but in tension of the MG muscle may increase the tension of not found for the LG [60]. Masood et al. reported that there the Achilles tendon. was a significant difference in activity of the MG and LG. 5.1. Perspectives. Different ankle angle positions notably The electromyography (EMG) was used to assess the activity of the MG and LG. They found an increase in the activity of affect the tension of the gastrocnemius muscle and Achilles tendon. The present study suggests a significant correlation the MG (34%) and LG (21%) during sustained submaximal isometric exercise [61]. between the elastic modulus of the Achilles tendon and the Most studies have demonstrated there is a relationship elastic modulus of the MG, but not for the LG. This finding may provide a new treatment idea for the clinical setting to between the gastrocnemius and Achilles tendon or foot func- tion. Park et al. used the extracorporeal shock wave therapy treat subjects with Achilles tendon disorders. A reduction of tension of the MG may be considered to be one effective on the medial head of the gastrocnemius muscle to relax the ankle in children with spastic cerebral palsy. They found method to prevent and treat the injury of the Achilles tendon. that the passive range of motion of the ankle joint was signif- This study was limited to participants who were healthy and did not have a history of ongoing neuromuscular diseases or icantly increased after ESWT (extracorporeal shock wave therapy) [62]. In addition, eccentric training is effective to musculoskeletal injuries specific to the ankle or knee joints. The same kind of experiment could be valuable to analyze reduce pain and improve function among subjects with Achilles tendinopathy. Crill et al. has reported that eccentric the correlation between the elastic modulus of the Achilles training could reduce pain and improve function among sub- tendon and the elastic modulus of the MG in Achilles tendon disorders. More research is needed to explore whether cur- jects with Achilles tendinopathy. They also found the fascicle length of the MG increased 12%, but not found for LG. The rent management programs for Achilles tendon disorders need to be tailored to the MG. findings of the present study indicated that there is a greater response to eccentric training for the MG than the LG [63]. Based on previous studies, there is a strong correlation Abbreviations between the Achilles tendon and gastrocnemius. However, no studies have been conducted to examine the exact correla- SWE: Shear wave elastography tion between the Achilles tendon and gastrocnemius. Our AT: Achilles tendon study is the first to reveal a positive correlation between the MG: The medial head of the gastrocnemius muscle elastic modulus of the Achilles tendon and the elastic modu- LG: The lateral head of the gastrocnemius muscle lus of the MG. Therefore, a reduction of tension of the MG AT0cm: The position of the Achilles tendon at 0 cm above was considered to be one effective method to prevent and the calcaneal tuberosity treat the injury of Achilles tendon disorders. AT3cm: The position of the Achilles tendon at 3 cm above the calcaneal tuberosity. 4.3. Limitations. The present study has some limitations. Firstly, EMG was not used during the tests to monitor the Data Availability muscle activity to ensure no contraction of the muscle. How- ever, all participants were verbally instructed to stay relaxed, The data used to support the findings of this study are and no signs of muscle contraction were visible on the B- available from the corresponding author upon request. mode image. Based on this, we are confident that partici- pants remained in a passive state while their legs were fully Conflicts of Interest supported. Secondly, due to the limitation of the SWE, the soleus muscle was involved in this study. The SWE could The authors declare that they have no conflicts of interest. 8 Applied Bionics and Biomechanics a chronic spinal cord injury,” Journal of Biomechanics, vol. 73, References pp. 60–65, 2018. [1] P. A. Pękala, B. M. Henry, A. 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Regional Elastic Properties of the Achilles Tendon Is Heterogeneously Influenced by Individual Muscle of the Gastrocnemius

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Hindawi Applied Bionics and Biomechanics Volume 2019, Article ID 8452717, 10 pages https://doi.org/10.1155/2019/8452717 Research Article Regional Elastic Properties of the Achilles Tendon Is Heterogeneously Influenced by Individual Muscle of the Gastrocnemius 1 2 1 1 3 Jiping Zhou, Jiafeng Yu, Chunlong Liu, Chunzhi Tang, and Zhijie Zhang Clinical Medical College of Acupuncture, Moxibustion, and Rehabilitation, Guangzhou University of Chinese Medicine, Guangzhou, China Department of Rehabilitation Medicine, The First Affiliated Hospital of Zhengzhou University, Zhengzhou, China Luoyang Orthopedic Hospital of Henan Province, Orthopedic Hospital of Henan Province, Luoyang, China Correspondence should be addressed to Zhijie Zhang; sportspt@163.com Received 6 April 2019; Revised 2 August 2019; Accepted 19 September 2019; Published 3 November 2019 Academic Editor: Craig P. McGowan Copyright © 2019 Jiping Zhou et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Background. Anatomical studies and the mechanical property studies showed that there is a strong correlation between Achilles tendon (AT) elasticity and individual gastrocnemius muscle (the medial head of gastrocnemius (MG) and the lateral head of gastrocnemius (LG)) elasticity. Limited ankle dorsiflexion range of motion has been correlated with decreased flexibility of the MG/LG/AT complex. However, no studies have been conducted to examine the exact correlation between the Achilles tendon and the individual muscle of the gastrocnemius. Purposes. The purposes of the present study were (1) to evaluate intra- and interoperator reliabilities of elastic property measurements in the gastrocnemius muscle-Achilles tendon complex by using the shear wave elastography (SWE) and (2) to examine the correlation between the regional elastic properties of the AT and the individual muscle of the gastrocnemius. Methods. Twenty healthy subjects (mean age: 22.50 (3.02) years) were recruited in this study. The elastic properties of the AT and the individual muscle of the gastrocnemius were quantified using the SWE. Findings. The SWE has comparatively high reliability in quantifying the elastic properties of the muscle-tendon range from good to excellent. The intraoperator ICC of the gastrocnemius muscle-Achilles tendon complex was 0.77 to 0.95, while the interoperator ICC was 0.76 to 0.94. The minimal detectable change (MDC) of the muscle was 1.72 kPa, while the AT was 32.90 kPa. A significant correlation was found between the elastic modulus of AT and the elastic modulus of the MG (r =0:668 and p =0:001 at the relaxing position and r =0:481 and p =0:032 at the neutral position). Conclusions. The SWE has the potential to assess localized changes in muscle-tendon elastic properties, provide more intuitive relations between elastic properties of the muscle tendon and function, and evaluate the therapeutic effect of the muscle tendon. A significant correlation between the AT and the MG was found, and it may provide a new treatment idea (targeted to the tight muscle heads) for the clinical setting to treat subjects with AT disorders. they descend but do not run in parallel to each other [4]. In 1. Introduction addition, the posterior part (i.e., superficial part) of the Achil- The Achilles tendon (AT), which is the conjoined tendon of les tendon is formed by the fascicles of the tendons of the the gastrocnemius and soleus muscles, is the strongest and medial gastrocnemius (MG), while the anterior part (i.e., largest tendon in the body [1, 2]. Anatomical studies describe deep part) consists of the lateral gastrocnemius (LG) and the Achilles tendon as the tendon that starts at the musculo- soleus muscles [5]. Furthermore, the LG is shorter and tendinous junction of the soleus and gastrocnemius, which smaller than the MG so that the lateral head and the medial becomes rounded and flattened in the junction with the gas- head of the gastrocnemius vary in their force contribution trocnemius [3]. The twisted structure of the Achilles tendon to the Achilles tendon [3]. It has been reported that flexibility is formed by individual subtendons which instead rotate as is a component of joint fitness, as it is thought to be 2 Applied Bionics and Biomechanics associated with athletic performance and the incidence of and reliable tool to estimate the elastic properties of the ten- injury [6, 7]. Note that in all the previous studies, flexibility don. There is a significant correlation between the elastic was assessed by measuring the maximal range of passive joint modulus of the tendon captured from SWE and the tangent motion [8, 9]. However, the passive range of joint motion traction modulus computed from a material testing system depends on muscle flexibility or, alternatively, tendon exten- [23]. In addition, Eby et al. revealed that the SWE is valid sibility. However, previous studies did not conduct studies of technique to estimate the elastic properties of the muscle. the individual muscle of the triceps calf muscle, and current A positive significant correlation was found between the research is still focused on mixed muscles or group muscles. elastic modulus of the muscle from the SWE and the elastic Besides, Green et al. found that muscle heads of the soleus modulus from a material testing system [24]. Furthermore, versus the gastrocnemius may differ when exercise induced the SWE was also used to examine the elastic properties of passive muscle tension on the muscle [10]. In summary, there the infraspinatus, erector spinae, and gastrocnemius mus- is a strong correlation between the Achilles tendon and the cles, rotator cuff, sternocleidomastoid, Achilles tendon, and gastrocnemius. However, no studies have been conducted patellar tendon [25–29]. Thus, the SWE can provide an to examine the exact correlation between the Achilles tendon opportunity to monitor the change in the elastic modulus and the gastrocnemius. of the gastrocnemius and the Achilles tendon at various The main function of the AT is the plantar flexion of the angles of the ankle joint. ankle, determining the human body’s jumping and running The objectives of this study were (1) to evaluate intra- [11]. Joint flexibility is influenced by musculotendinous and interoperator reliabilities of the elastic modulus mea- surement in the gastrocnemius muscle-Achilles tendon com- structures around the joint. The tendinous tissues are known plex by using the SWE and (2) to examine the correlation to possess elastic characteristics which are a critical determi- nant of the proper muscle force transmission and movement between the regional elastic properties of the Achilles tendon and the individual muscle of the gastrocnemius during vari- generation [12]. Muscle elasticity is the key determinant of ous angles of ankle joint flexion. the capacity of the muscle to contract [13]. Although there are different functions between the skeletal muscle and the 2. Methods tendon, modulation in the elastic properties of the muscle tendon can reflect the pathological change and recovery 2.1. Ethics Statement. This study was approved by the Human effect. In our previous study, we have explored the interplay Subjects Ethics committee of the Clinical Medical College of between passive muscle tension of the vastus lateralis and Acupuncture, Moxibustion, and Rehabilitation. All subjects rectus femoris muscles and patellar tendon stiffness. Greater were fully informed of the purpose and experimental proce- passive tension in the vastus lateralis was associated with dures and signed the informed consent before the study. higher patellar tendon stiffness in male athletes. In addition, previous studies have investigated that stiffer AT and gas- 2.2. Participants. Twenty healthy subjects (14 males and 6 trocnemius have been found to be risk factors associated with females; age: 18–28 years) were recruited in this study. Inclu- Achilles tendinitis [14–17]. Reduced flexibility of the gastroc- sion criteria were that all participants were healthy and did nemius muscle and the AT can lead to an increase in lower- not have a history of ongoing neuromuscular diseases or extremity injuries. Increasing the stiffness of the muscle ten- musculoskeletal injuries specific to the ankle or knee joints don could limit the range of joint motion and increase the during the previous six months. Exclusion criteria included risk of injury [18]. Moreover, Gajdosik et al. found that the pain in the gastrocnemius and Achilles tendon, participants flexibility of the ankle joint depends on the extensibility of taking fluoroquinolone antibiotics, lower limb fracture, post- musculotendinous structures, especially the gastrocnemius operative rupture of the Achilles tendon, or anomaly on [19]. Similarly, the gastrocnemius-Achilles tendon unit has ultrasound. been suggested to be a major contributor to passive joint stiff- ness [20]. Both of them cannot separate the muscle-tendon 2.3. Equipment and Parameter Setting. An ultrasound shear unit into respective components. Thus, accurately quantify- wave elastography system (Aixplorer Supersonic Imagine, ing the elastic properties of isolated regional areas of the France) with a 40 mm linear array transducer (SL10-2, Super- MG, LG, and AT may provide a more comprehensive under- sonic Imagine, France) was used. The settings of the SWE standing about the biomechanics of the MG, LG, and AT. system were set as follows: the instrument was set in the mus- Shear wave elastography (SWE) is a noninvasive tech- culoskeletal mode. The frequency was 2~10 MHz. The SWE nique to quantify the elastic properties of soft tissues. It can Opt was the penetration mode. The opacity was 85%. The be used to estimate the elastic modulus of the regional area elastic modulus range of the gastrocnemius was 0~200 kPa, through the shear wave speed. The principle of SWE is (1) while the elastic modulus range of the Achilles tendon was to create a shear wave through acoustic radiation force, (2) 0~800 kPa. The color scale used in the shear modulus (in to use sonography to map the distortion induced by the wave kPa) showed the lowest values in blue to the highest values in the measuring object, and (3) to trace the wave back to the in red. The depth of the B-scan was 3.0 cm [30]. For the mechanical properties of the measuring object by using the Achilles tendon, the size of the regions of interest (ROI) relationship E =3pc had to be set to 25 ∗ 12 mm and the Q-Box™ diameter was [21]. The SWE was used to quantify the elastic properties of the skeletal muscle and tendon. The defined by the thickness of the tendon, which was the dis- stiffer the tissue, the greater the shear modulus (kPa) [22]. tance between the superior and inferior borders of the Achil- Our previous studies demonstrated that the SWE is a valid les tendon [23]. For the MG and LG, the size of the ROI had Applied Bionics and Biomechanics 3 each subject’s Achilles tendon, MG, and LG over a 1-hour to be set to 10 ∗ 10 mm and the diameter of the Q-Box™ is 5 ∗ 5mm [31]. The transducer was positioned along period and by operator ZJ with a 2-hour interval. In the sec- the longitudinal axis of the AT, MG, and LG. ond test, the same subjects attended at the same time 5 days later, which was repeated by operator ZJP for the intraopera- 2.4. Experimental Design and Protocol tor investigation. Subjects were explicitly asked to refrain from any additional exercise throughout the duration of test- 2.4.1. Measurement Position. The dominant leg was identified ing but to maintain their normal daily walking activity [28]. by kicking a ball [32]. Before testing, subjects were asked to The results were not communicated between operators ZJP wear loose-fitting clothes. During testing, each subject was and ZJ until all subjects had been examined. allowed to lie in the prone position with the foot relaxed and hung over the lower edge of the treatment bed, the hip and knee joints fully extended, and the upper limbs placed 2.4.3. Statistical Analysis. Statistical analysis was performed on both sides of the body [32]. The joint was fixed using a using SPSS Version 19.0 (SPSS, Chicago, IL). All data were customized and movable ankle foot orthosis (AFO) at the presented by the mean (standard deviation). The intraclass neutral anatomical position (the strap of the AFO was tight- correlation coefficient (ICC) was calculated to determine ened until a 90 ankle joint position was achieved, measured the intra- and interoperator reliabilities. The coefficient of by a hand-held goniometer [33]) and resting ankle angle variance (CV), the standard error measurement (SEM), and (participants took what they perceived to be a “relaxed” foot the minimal detectable change (MDC) were calculated (all position [34, 35]). The measurement site of the Achilles ten- based on the following formulae: CV = ðstandard deviation/ pffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi don was defined as 0 cm (the most proximal outline of the meanÞ ×100%, SEM = standard deviation × ð1 − ICCÞ,and pffiffiffi calcaneus) and 3 cm above the calcaneal tuberosity [36], MDC = 1:96 × SEM × 2). Pearson correlation analysis (r) while the MG and LG were defined as the proximal 30% of was used to examine the correlation between the shear mod- the lower leg length [37]. The length of the MG is that mea- ulus of the Achilles tendon and the gastrocnemius muscle. sured from the popliteal fossa to the lateral malleolus, where The strength of reliability coefficients was classified as fol- cross-sectional areas of the gastrocnemius are almost maxi- lows: excellent (more than 0.90), good (0.71–0.90), moderate mum. As for the LG, the length is that measured from the (0.50–0.70), and poor (less than 0.50) [39]. The statistical sig- popliteal fossa to the medial malleolus. The length was mea- nificance was set at an alpha level of p <0:05 (α =0:05). sured by a tape measure, and a black pen was used to mark the location of the measurement site (Figure 1). In addition, to reduce experimental errors, subjects were explicitly asked 3. Results to keep the lower extremity as fully relaxed throughout the duration of testing and refrain from high intensity exercise 3.1. Intra- and Interoperator Reliabilities. The intra- and for 48 hours before testing [32]. Room temperature was interoperator reliabilities of the shear modulus exponent of maintained at 25 Cto reduce the effect of temperature on the MG, LG, and Achilles tendon is shown in Tables 1 and the elasticity of musculature [38]. 2, respectively. The results indicated that the intraoperator ICC for the MG, LG, AT0cm, AT3cm was 0.77 to 0.95 and 2.4.2. Ultrasound Shear Wave Elastography. Before measure- the interoperator ICC was 0.76 to 0.94. The intraoperator ments, subjects were asked to relax for 5 min to ensure that reliability for the measurement site of the LG (relaxing posi- the triceps surae was relaxed. During measurements, enough tion), MG (neutral position), LG (neutral position), and ultrasound gel was applied between the skin and the trans- AT0cm (neutral position) is excellent. The interoperator ducer to avoid skin deformation. The midpoint of the trans- reliability for the measurement site of the LG (relaxing posi- ducer was placed perpendicularly on the skin’s surface with tion) and AT3cm (neutral position) is excellent. The rest of a light pressure where we marked before, and then the the ICC values reveal good intra- and interoperator reliabil- mode of the SWE was activated to examine the shear wave ities. The MDC (kPa) for the MG, LG, AT0cm, and AT3cm modulus of the muscle or tendon [32]. During the acquisi- were 3.24 to 8.07, 1.72 to 6.44, 35.91 to 60.28, and 32.90 to tion of the mode of the SWE, the transducer was kept 43.42, respectively. motionless for about 5-8 s [23]. Then, the gray scale image showed the appearance of the muscle or tendon under the longitudinal section. Image quality was closely monitored 3.2. The Relationship between the Shear Modulus of AT and throughout the measurements. When the color in the ROI MG and LG. The r values and P values of the AT and MG was uniform and several muscle fibers or the superior and and LG for different ankle joint positions are shown in inferior borders of the tendon were continuously visible, Table 3. A significant correlation was found between the the images were frozen and then put on the Q-Box™ to AT0cm and MG (r =0:668 and p =0:001 at the relaxing posi- obtain the shear wave modulus from the system and stored tion and r =0:481 and p =0:032 at the neutral position) for off-line analysis (kPa) (Figure 2). Three images were (Figure 3). In addition, the correlation between the MG and captured at each measurement site of the tendon and mus- AT3cm was weak (r =0:146 at the resting position and cle. The mean of the elastic modulus from all 3 images was r =0:358 at the neutral position). Furthermore, no significant used for further analyses. correlation was apparent in the shear wave modulus results Two operators (ZJP and ZJ) participated in the intero- between the LG and AT, in which the correlation coefficient perator investigation. The operators took turns to examine is 0.078 to 0.199. 4 Applied Bionics and Biomechanics MG LG AT3 cm AT0 cm (a) (b) (c) Figure 1: The location of the measurement site. (a) MG: at the midpoint of the oblique line connecting the inside of the popliteal transverse line and the highest point of the malleolus lateralis. (b) LG: at the midpoint of the oblique line connecting the outside of the popliteal transverse line and the highest point of the malleolus medialis. (c) AT0cm: 0 cm above the calcaneal tuberosity; AT3cm: 3 cm above the calcaneal tuberosity. (a) (b) (c) (d) Figure 2: Changes of the elastic modulus of MG converted from the resting ankle angle to the neutral anatomical position (from (a) to (b)). The elastic modulus of AT0cm and AT3cm in the resting ankle angle (from (c) to (d)). The color-coded box presentation of muscle-tendon elasticity is shown in the upper images. The longitudinal grey scale sonograms of the muscle tendon are shown in the bottom images. The Q-Box™ is shown on the right. 4. Discussion ities to quantify the elastic modulus of the gastrocnemius- Achilles tendon complex and a significant positive correla- The main findings of the present study were that the SWE tion was obtained between the elastic modulus of the AT0cm had moderate to excellent intra- and interoperator reliabil- and MG, but not found for LG. Applied Bionics and Biomechanics 5 Table 1: Intraoperator reliability of mean elastic modulus values of MG, LG, and AT. Measurement position Test 1 (kPa) Test 2 (kPa) MDC (kPa) 95% CI CV (%) SEM (kPa) ICC MG (R) 17:82 ± 2:92 17:85 ± 3:47 3.24 0.61-0.94 16.39 1.17 0.84 14:19 ± 3:28 14:60 ± 2:53 LG (R) 1.98 0.79-0.97 17.33 0.72 0.92 426:04 ± 34:62 422:83 ± 32:91 AT0cm (R) 43.75 0.42-0.91 7.78 15.78 0.77 415:19 ± 38:44 402:59 ± 35:75 AT3cm (R) 42.04 0.54-0.93 8.88 15.17 0.82 49:49 ± 9:21 49:98 ± 9:50 MG (N) 7.66 0.78-0.96 18.61 2.76 0.91 39:14 ± 7:01 38:95 ± 6:71 LG (N) 4.16 0.88-0.98 17.91 1.50 0.95 563:52 ± 54:37 568:53 ± 51:84 AT0cm (N) 43.11 0.76-0.96 9.12 15.55 0.91 529:07 ± 44:86 525:27 ± 41:51 AT3cm (N) 39.86 0.71-0.95 7.90 14.38 0.88 R: relaxing position; N: neutral position; LG: lateral gastrocnemius; MG: medial gastrocnemius; AT: Achilles tendon; MDC: minimal detectable change; 95% CI: 95% confidence interval; CV: coefficient of variation; SEM: standard error in measurement; ICC: intraclass correlation coefficient. Table 2: Interoperator reliability of mean elastic modulus values of MG, LG, and AT. Measurement position Operator ZJP (kPa) Operator ZJ (kPa) MDC (kPa) 95% CI CV (%) SEM (kPa) ICC 17:82 ± 2:92 18:21 ± 3:96 MG (R) 3.97 0.39-0.90 16.39 1.43 0.76 14:19 ± 3:28 14:19 ± 2:54 LG (R) 1.72 0.84-0.97 17.90 0.62 0.94 426:04 ± 34:62 428:83 ± 39:48 AT0cm (R) 35.91 0.70-0.91 8.13 12.95 0.86 415:19 ± 38:44 407:43 ± 32:66 AT3cm (R) 43.42 0.43-0.91 8.02 15.66 0.77 49:49 ± 9:21 51:68 ± 9:42 MG (N) 8.07 0.76-0.96 18.61 2.91 0.90 39:14 ± 7:01 41:36 ± 7:87 LG (N) 6.44 0.73-0.96 17.91 2.32 0.89 563:52 ± 54:37 565:39 ± 60:93 AT0cm (N) 60.28 0.61-0.94 9.65 21.75 0.84 529:07 ± 44:86 535:78 ± 42:13 AT3cm (N) 32.90 0.84-0.97 7.86 11.87 0.93 4.1. Intra- and Interoperator Reliabilities. The results of the Table 3: Relationships of the elastic modulus between the AT and MG and LG. present study demonstrated that the SWE has high intra- and interoperator reliabilities for quantifying the elastic mod- AT0cm (R) AT3cm (R) ulus of the AT, MG, and LG. The relatively low SEM and ∗∗ MGR 0.668/0.001 0.146/0.540 MDC values revealed good precision of the measurements. The MDC is the smallest change in score that likely reflects LGR 0.09/0.970 0.078/0.745 true change (not measurement error alone). Comparing with AT0cm (N) AT3cm (N) those of previous studies, our study results revealed good to 0.481/0.032 MGN 0.358/0.121 excellent intra- and interoperator reliabilities for quantifying LGN 0.199/0.399 0.143/0.547 the shear modulus of the Achilles tendon and gastrocnemius ∗∗ Data are r value/P value. R: relaxing position; N: neutral position. p <0:01 muscle. Chino et al. found that ultrasound elastography was a and p <0:05. reliable and valid quantitative method for quantifying the stiffness of the gastrocnemius muscle, in which interoperator reliability was 0.77~0.89 [40]. Also, Fu et al. evaluated the elasticity of the normal Achilles tendon among 326 healthy during rest, in which the intraoperator reliability of MG was subjects older than 18 years which were divided into different 0.98, while the AT was 0.82~0.93 [42]. groups by age. The results of this study were that the intrao- In addition, a threshold of ≤12% for the CV is regarded as perator reliability was 0.93 [28]. In addition, Taş et al. made a an acceptable level of biological measurement [43]. The study to examine the intra- and interoperator reliability levels results of the present study indicated that the CV of the for the stiffness of the rectus femoris muscle and patellar ten- MG and LG was 16.39% to 18.61%, which were a little differ- don. They found that the intraoperator reliability of the patel- ent with the CV values of recent research. There is corrobo- lar tendon was 0.81~0.83 and the interoperator reliability was ration with the study by Lima et al. who observed values of 0.71. For the stiffness of the rectus femoris muscle, the intrao- 17.29% to 20.95% for the MG [42], while Chino and Takaha- perator reliability was 0.93~0.94 and the interoperator reli- shi observed values of 19.4% for the MG [44]. The possible ability was 0.95 [41]. Furthermore, Lima et al. found good reason is that we cannot ensure that the probe was completely intraoperator reliability between the AT and MG, bilaterally, parallel to the muscle fibers. However, the shear wave 6 Applied Bionics and Biomechanics 460 600 400 500 340 400 12 14 16 18 20 22 24 35 40 45 50 55 60 65 70 MG at relaxing position MG at neutral position (a) (b) Figure 3: The plots show the correlations of AT0cm and MG at different angles. (a) Relaxing position: r =0:668, p =0:001; (b) neutral position: r =0:481, p =0:032. modulus values depend on the probe in relation to the fiber muscle-tendon shear modulus of the abnormal side) and treatment (pretreatment vs. posttreatment) [53]. Moreover, direction [45]. Brum et al. showed that the shear wave veloc- ity dispersion was influenced by viscosity when the probe is SWE has the characteristics of tracking the changes in the perpendicular to the fibers, but it was not found parallel to shear modulus of the gastrocnemius muscle and Achilles ten- the fibers [46]. Although the CV of the MG and LG in the don. It may provide a basis to reflect a real change for exam- present study was slightly higher than 12%, the ICC of the ining the effectiveness of an intervention [50]. MG and LG values were 0.76 to 0.95, so the data of the muscle were all classified as acceptable. The CV of the Achilles ten- 4.2. The Relationship between the Shear Modulus of AT and don were 7.78% to 9.65%, which confirmed the high reliabil- MG and LG. A significant positive correlation was obtained between the elastic modulus of the MG and AT, but not ity of the shear elastic modulus values of the Achilles tendon, in agreement with a previous study (7.2% to 9.4%) [47]. found for LG. This is the first study wherein a concurrent Furthermore, the MDC was calculated to provide a value investigation of the gastrocnemius muscles and regions to reflect a real change that could be interpreted as a real dif- within the Achilles tendon has been undertaken. In the view ference exceeding the measurement error, which can serve of biomechanics, the transmission and generation of triceps surae muscle forces were affected by the compliance of the as a reference for future study. Our results showed that the MDC of the muscle was 1.98 kPa (the same operator) and AT. Increasing AT compliance can alter the gastrocnemius 1.72 kPa (different operator), while the Achilles tendon was muscle and soleus muscle fiber operating lengths and muscle 32.90 kPa (the same operator) and 39.86 kPa (different excitations. And these effects in gastrocnemius muscles are operator). Therefore, the shear wave modulus of the MG more pronounced than in soleus muscles, which possibly arise from essential differences of muscle-tendon behavior. and LG should be greater than 1.72 kPa and the Achilles tendon should greater than 32.90 kPa to reflect changes with Gastrocnemius muscle fiber negative work decreased pro- retested tests. gressively with increasing AT compliance during the stretch- Recently, due to the high specificity and sensitivity of the ing phase while that of soleus muscles increased for 5% [54]. SWE, it has been used in practical applications [48]. For In addition, an imbalance of force generation between the MG and LG has also been speculated to contribute to the example, Point et al. found that the SWE can monitor the increase of muscle stiffness after cryotherapy induction development and/or persistence of Achilles tendinopathy or [49]. On the other hand, the SWE can be used to detect the pain of the Achilles tendon [55]. On the one hand, both side-to-side differences in tendon geometry and mechanical the MG and LG have the same function of plantarflexion properties in tendon structure in individuals with Achilles but have different degrees of contribution, with the MG pro- viding more than 70% of the muscle force [2]. On the other tendon rupture. This information may give clinical staff a clear understanding of the relationship between tendon hand, the possible explanation is that the MG is longer and structure and clinical manifestation [50]. Furthermore, it larger and extends more distally in the calf than the LG [3] has been reported that the stiffness of congenital myopathies and muscle volume of the MG was higher than the LG [56]. was changed. For example, the stiffness of cerebral palsy and Furthermore, a study reported that the Achilles tendon has a unique structure that is the twisted descending structure, Duchenne muscular dystrophy were increased, while decreased in GNE (UDP-N-acetylglucosamine 2- epimerase/N-acetyl- which enables it to handle the functional loads applied to mannosamine kinase) [22, 51, 52]. Thus, the SWE can be the tendon [57]. Pękala et al. found that the torsion of the used to quantify the shear modulus of the gastrocnemius MG is significantly lower than the LG wherein the rotation muscle and Achilles tendon for assisting the clinical diagnosis angle of the LG is about 5 times that of the MG (the fibers (the muscle-tendon shear modulus of the normal side vs. the originating from the LG rotate on average 135:98 ± 33:58 AT0cm at relaxing position AT0cm at neutral position Applied Bionics and Biomechanics 7 not measure the deep muscle. Thirdly, the ankle of partici- while the MG twist 28:17 ± 15:15 ) [1]. In addition, the larg- est component of AT insertion into the calcaneal bone is the pants was placed in a “relaxed” position; muscle tension MG (the mean width of the footprint was 28.3 mm), and the may be affected by the mass moment of inertia of the foot. Further studies will be conducted to investigate the modula- smallest is the LG (the mean width of the footprint was 14.4 mm) [5]. In all the above views of biomechanics, the tion of elastic properties of the mass moment of inertia of changes of the Achilles tendon are closely related to the the foot. Finally, only healthy subjects and only 2 angles of MG, and the proportion of the MG contribution is larger the ankle were recruited in this study. Further studies will than that of the LG contribution to the Achilles tendon. be conducted to investigate the modulation of elastic proper- ties of the Achilles tendon and gastrocnemius among indi- The elastic properties of the Achilles tendon were closely related to the MG in various exercise programs. For example, viduals with Achilles tendon disorders. during an acute bout of eccentric heel drop exercise, the gas- trocnemius muscles were shown to bear larger mechanical 5. Conclusion loads than the Achilles tendon [58]. Stenroth et al. found that the longer distance walked in a 6-minute walk test was signif- The SWE can be used to quantify regional elastic properties icantly associated with the MG [59]. Besides, Hirata et al. of the Achilles tendon and gastrocnemius. We also found a reported that the passive muscle stiffness differs among the significant correlation between the elastic modulus of the triceps surae. They found a higher elastic modulus of the Achilles tendon and the elastic modulus of the MG, but MG than the LG. After static stretching, a significant reduc- not for the LG. These findings suggested that an increase tion in the elastic modulus of the MG was observed, but in tension of the MG muscle may increase the tension of not found for the LG [60]. Masood et al. reported that there the Achilles tendon. was a significant difference in activity of the MG and LG. 5.1. Perspectives. Different ankle angle positions notably The electromyography (EMG) was used to assess the activity of the MG and LG. They found an increase in the activity of affect the tension of the gastrocnemius muscle and Achilles tendon. The present study suggests a significant correlation the MG (34%) and LG (21%) during sustained submaximal isometric exercise [61]. between the elastic modulus of the Achilles tendon and the Most studies have demonstrated there is a relationship elastic modulus of the MG, but not for the LG. This finding may provide a new treatment idea for the clinical setting to between the gastrocnemius and Achilles tendon or foot func- tion. Park et al. used the extracorporeal shock wave therapy treat subjects with Achilles tendon disorders. A reduction of tension of the MG may be considered to be one effective on the medial head of the gastrocnemius muscle to relax the ankle in children with spastic cerebral palsy. They found method to prevent and treat the injury of the Achilles tendon. that the passive range of motion of the ankle joint was signif- This study was limited to participants who were healthy and did not have a history of ongoing neuromuscular diseases or icantly increased after ESWT (extracorporeal shock wave therapy) [62]. In addition, eccentric training is effective to musculoskeletal injuries specific to the ankle or knee joints. The same kind of experiment could be valuable to analyze reduce pain and improve function among subjects with Achilles tendinopathy. Crill et al. has reported that eccentric the correlation between the elastic modulus of the Achilles training could reduce pain and improve function among sub- tendon and the elastic modulus of the MG in Achilles tendon disorders. More research is needed to explore whether cur- jects with Achilles tendinopathy. They also found the fascicle length of the MG increased 12%, but not found for LG. The rent management programs for Achilles tendon disorders need to be tailored to the MG. findings of the present study indicated that there is a greater response to eccentric training for the MG than the LG [63]. Based on previous studies, there is a strong correlation Abbreviations between the Achilles tendon and gastrocnemius. However, no studies have been conducted to examine the exact correla- SWE: Shear wave elastography tion between the Achilles tendon and gastrocnemius. Our AT: Achilles tendon study is the first to reveal a positive correlation between the MG: The medial head of the gastrocnemius muscle elastic modulus of the Achilles tendon and the elastic modu- LG: The lateral head of the gastrocnemius muscle lus of the MG. Therefore, a reduction of tension of the MG AT0cm: The position of the Achilles tendon at 0 cm above was considered to be one effective method to prevent and the calcaneal tuberosity treat the injury of Achilles tendon disorders. AT3cm: The position of the Achilles tendon at 3 cm above the calcaneal tuberosity. 4.3. Limitations. The present study has some limitations. Firstly, EMG was not used during the tests to monitor the Data Availability muscle activity to ensure no contraction of the muscle. How- ever, all participants were verbally instructed to stay relaxed, The data used to support the findings of this study are and no signs of muscle contraction were visible on the B- available from the corresponding author upon request. mode image. Based on this, we are confident that partici- pants remained in a passive state while their legs were fully Conflicts of Interest supported. Secondly, due to the limitation of the SWE, the soleus muscle was involved in this study. The SWE could The authors declare that they have no conflicts of interest. 8 Applied Bionics and Biomechanics a chronic spinal cord injury,” Journal of Biomechanics, vol. 73, References pp. 60–65, 2018. [1] P. A. Pękala, B. M. Henry, A. 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