Does epimuscular myofascial force transmission occur between the human quadriceps muscles in vivo during passive stretching?
Introduction
Force transmission between skeletal muscle and its surrounding structures, also referred to as epimuscular myofascial force transmission (Huijing, 2009), has been suggested to occur during both passive stretching and muscle contraction conditions (Maas and Finni, 2017, Maas and Sandercock, 2010). However, in vivo investigation of epimuscular myofascial force transmission in humans is scarce. Recently, muscle shear modulus quantified by means of ultrasound-based shear wave elastography, has been shown to be strongly correlated with skeletal muscle passive force (Koo et al., 2013) and to Young’s modulus (Eby et al., 2013). Therefore, muscle shear modulus can be interpreted as a passive force index. For instance, based on ex vivo validity experiments performed on fresh roaster chicken skeletal muscles (Koo et al., 2013), a small change in shear modulus could reflect a non-negligible alteration in muscle passive tension (e.g. change of 10 kPa ≈ 0.55–1.21 N). Recently, some studies have reported region-dependent changes in muscle shear modulus when stretching neighbouring muscles (Ateş et al., 2018, Yoshitake et al., 2018). For instance, the distal region of soleus from healthy human individuals was reported to exhibit a higher shear modulus during passive ankle rotations with the knee fully extended compared to a 90° knee flexion position, while the proximal soleus region showed a lower shear modulus (Ateş et al., 2018). However, whether this phenomenon is present in other muscle groups remains to be investigated.
The aponeuroses from each of the quadriceps’ muscle components merge into the patellar tendon (Grob et al., 2016), and a recent investigation performed in human cadavers described a connective tissue linkage between the vastus medialis (VM) and both the rectus femoris (RF) and vastus intermedius (Grob et al., 2017). In addition, there is anatomical evidence that vastus lateralis (VL) attaches into the iliotibial band (Becker et al., 2010). Thus, it is likely that the passive force of monoarticular quadriceps components within the muscles bellies may be altered when there is a change in the length of RF or tensor fasciae latae, such as during changes in hip position. Previous studies have only compared the shear modulus of the quadriceps muscles during passive stretching with the hip in a fixed position (Coombes et al., 2018, Xu et al., 2016). In addition, contradictory findings have been reported regarding the shear modulus of the quadricep muscles under resting conditions. Coombes et al. (2018) reported that VL had the highest shear modulus of the quadriceps muscles (excluding vastus intermedius), whereas Xu et al. (2016) reported that RF had the highest shear modulus. These contradictory findings are likely to reflect the different hip position used: flexed (Coombes et al., 2018) or neutral position (Xu et al., 2016). Another relevant methodological aspect, that could possibly explain the aforementioned contradictory findings, refers to the measurement location. Le Sant et al. (2017) recently observed that the shear modulus of the medial gastrocnemius was heterogeneous, i.e., differences between proximal and distal regions were observed.
Thus, the primary aim of this study was: (i) to investigate the existence of epimuscular myofascial force transmission between the quadricep muscles during passive knee flexion (i.e., quadriceps stretching), by comparing the shear modulus within the VM and VL muscle bellies with the hip flexors at two lengths by changing the hip position: hip flexed (80°) vs. hip neutral (0°) positions. Secondly, we aimed to compare the shear modulus (ii) between and (iii) within (i.e., proximal vs. distal regions) the quadricep muscles (VM, VL, RF), with the hip flexors at different lengths. We hypothesized that: (i) both the VM and VL would present a higher shear modulus when hip flexors assumed a lengthened condition, due to the potential epimuscular myofascial force transmission; (ii) VL would show the highest shear modulus with the hip flexed, while the RF would show the highest shear modulus with the hip in neutral position; and (iii) distal muscle regions would show greater shear modulus due to its proximity to the joint being mobilized.
Section snippets
Participants
Twelve healthy and recreationally active male individuals (age: 23.7 ± 3.6 yrs; height: 1.76 ± 0.08 m; body mass: 71.2 ± 8.9 kg) volunteered for this study. Participants provided written informed consent, and reported no history of neuromuscular injuries in the lower limbs. Sample size was estimated using the G*Power software (v3.1.9.2, Düsseldorf, Germany), for a test-retest reliability outcome of 0.75, effect size of 0.2, statistical power of 80% and significance of 5%. This study was
Results
A typical shear modulus response for the tested muscles can be observed in Fig. 1B. A high to very high shear modulus measurement repeatability was found across muscles (RF: ICC3,1 = 0.73–0.99; VL: ICC3,1 = 0.77–0.98; VM: ICC3,1 = 0.74–0.99). A very low muscle electrical activity was observed during the stretching maneuvers (VL = 0.3–0.5%, RF = 0.4–0.5%, VM = 0.7–1.3%), with no significant difference between hip positions (p = 0.25–0.43) nor knee ROM percentiles (p = 0.22–0.31); suggesting that
Discussion
This study investigated the existence of epimuscular myofascial force transmission between the quadriceps muscles during passive knee flexion. We compared VM and VL shear modulus with the hip flexors at two lengths by manipulating the hip position: flexed (80°) and neutral (0°). The present study results contradict our hypothesis that both VM and VL would present a higher shear modulus with the hip in a neutral position (i.e., hip flexors more lengthened). Instead, we observed no differences
Acknowledgements
The authors are grateful to all study participants. MC is funded by FONDECYT 11161033, Ring Initiative ACT1402, Millennium Science Initiative P09-015- F and DAAD (57220037 & 57168868). JRV was funded by NIH P20GM109090.
Conflict of interest statement
The authors disclose no conflict of interest.
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