Clinical Biomechanics 112 (2024) 106194

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Clinical Biomechanics
journal homepage: www.elsevier.com/locate/clinbiomech

Epimuscular myofascial force transmission between the levator scapulae

muscle and the upper fiber of the serratus anterior or rhomboid
minor muscles
Keita Kawabuchi a, *, Kenta Yamane a, Shota Maniwa a, Kyohei Inoue a, Masatoshi Nakamura b
a
Rehabilitation Room, Tottori Prefectural Central Hospital, 730 Ezu, Tottori City, Tottori 680-0901, Japan
b
Faculty of Rehabilitation Science, Nishi Kyushu University, 4490-0 Ozaki, Kanzaki, Saga 842-8585, Japan

A R T I C L E I N F O A B S T R A C T

Keywords: Background: This study investigated the epimuscular myofascial force transmission between the levator scapulae,
Epimuscular myofascial force transmission serratus anterior, and rhomboid minor muscles.
Levator scapulae Methods: The participants included 10 healthy males (a total of 20 shoulders). Differences in the shear moduli of
Serratus anterior
the levator scapulae, serratus anterior, and rhomboid minor muscles were measured in the resting and levator
Rhomboid minor
Fascia
scapulae stretching positions using shear wave elastography. The correlation between the rates of change for
each muscle was also verified.
Findings: The results demonstrated a notable increase in the shear modulus from the resting to stretching posi­
tions for levator scapulae (42.9 ± 17.6 kPa vs. 52.4 ± 15.2 kPa) and serratus anterior (32.8 ± 12.9 kPa vs. 58.4
± 18.5 kPa) (P = 0.02, P < 0.01). However, there was no significant difference in the shear modulus for the
rhomboid minor between the resting (44.0 ± 19.2 kPa) and stretching (41.0 ± 20.2 kPa) positions (P = 0.40).
Moreover, a significant positive correlation was observed between rates of change for the levator scapulae and
serratus anterior muscles (P = 0.04, r = 0.459).
Interpretation: These findings indicate that the shear modulus of the serratus anterior increased with the
stretching of the levator scapulae, suggesting the occurrence of epimuscular myofascial force transmission be­
tween these two muscles with different muscle insertions.

1. Introduction
Optimal scapular positioning and movement are necessary for
normal shoulder joint function (Umehara et al., 2019). Among the
muscle groups involved in the scapular movement, the levator scapulae
(LS) is essential for facilitating scapular elevation and internal rotation
(Crowe and Elhassan, 2016). It collaborates with other periscapular
muscles to maintain scapular stability and mobility (Castelein et al.,
2015). However, overuse of the LS muscle may cause downward rota­
tion of the scapula, increasing the risk of subacromial impingement
(Castelein et al., 2017). Moreover, increased muscle activity might affect
the downward rotation of the scapula in patients with symptomatic
rotator cuff tears (Ishikawa et al., 2021; Shinozaki et al., 2014).
LS is characterized by continuity with other muscles. The upper fiber
of the serratus anterior muscle (SA) attaches from the first and second
ribs to the superior angle of the scapula. It is characterized by a short
muscle length and a broad cross-section (Hamada et al., 2008). Based on
these anatomical characteristics, SA is considered to cooperate with the
LS to stabilize or control the scapula (Hamada et al., 2008). The rhom­
boid minor muscle (Rm) originates from the spinous processes of C7 and
T1 and inserts at the level of the scapular spine (Meininger et al., 2011).
Connective tissues interconnect LS and Rm. This is called “the levator-
rhomboid fascia,” which allows the neck and shoulder to move freely
by protecting the neurovascular bundles, creating a sliding space with
other tissues (Kulow et al., 2022). These muscles stabilize the scapula by
compressing it against the thorax, which is necessary for upper ex­
tremity muscle activity (Castelein et al., 2015). Furthermore, the
anatomical findings show that the LS, SA, and Rm muscles are inner­
vated by the fifth cervical nerve, and their neurological resemblances
imply their potential collaboration in controlling scapular movement
(Hamada et al., 2008; Nasu et al., 2012). The fascia connecting these
muscle groups coordinates posture and movement and transmits

* Corresponding author.
E-mail address: k.keita.chubyoriha.pt@gmail.com (K. Kawabuchi).

https://doi.org/10.1016/j.clinbiomech.2024.106194
Received 28 September 2023; Accepted 31 January 2024
Available online 6 February 2024
0268-0033/© 2024 Elsevier Ltd. All rights reserved.

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K. Kawabuchi et al. Clinical Biomechanics 112 (2024) 106194

mechanical forces to adjacent muscles in vivo (Moccia et al., 2016; Wilke
et al., 2018). Wilk et al. reported soft tissue slides in the semi­
membranosus muscle through gastrocnemius muscle stretching (Wilke
and Tenberg, 2020). Moreover, Bojsen et al. showed the distal
displacement of the gastrocnemius muscle upon electrical stimulation
and passive knee extension without ankle joint motion (Bojsen-Møller
et al., 2010). Thus, mechanical force transmission of the fascia also af­
fects adjacent muscles in vivo (Wilke et al., 2018).
This force transfer between skeletal muscles and their surrounding
tissues is known as epimuscular myofascial force transmission (EMFT)
(Huijing, 2007), which has been shown to manifest in vivo (Cruz-Mon­
tecinos et al., 2016). Yanase et al. used ultrasound shear wave elastog­
raphy (SWE) to demonstrate increased shear modulus in the lateral and
medial vastus medialis muscles, both monoarticular knee muscles, upon
rectus femoris muscle extension, indicating potential EMFT in the
human quadriceps muscle (Yanase et al., 2021a). A robust linear asso­
ciation between SWE elasticity and passive muscle tone has been shown,
serving as an indirect marker of muscle stretch tension (Koo et al.,
2013). Therefore, SWE can be used to quantify EMFT occurring among
adjacent muscles through fascial and connective tissue.
This study aimed to investigate the EMFT between the LS, SA, and
Rm using SWE. All muscles have similar attachment sites from the su­
perior angle or the medial border of the scapula (Pinto et al., 2019).
However, each muscle's origin is different: the transverse processes of
the 1st–4th cervical spine (C) for the LS (Pinto et al., 2019), 1st–2nd rib
for the SA (Smit and Todd, 2019), and C7 to the spinous process of the
1st thoracic spine (T) for the Rm (Meininger et al., 2011). We hypoth­
esize that only the LS is stretched during isolated neck movements
without scapular movement (Jeong et al., 2017). However, tension
transmission by connective tissue may cause shear modulus changes
across the SA and Rm, not just the LS. Furthermore, this muscle tension
modulation can be quantified via EMFT using SWE, causing changes in
the muscle shear modulus.
2. Methods
2.1. Participants
The study included 10 healthy men (20 shoulders). Participants with
current or previous neurological or orthopedic disorders affecting the
upper limbs and those in occupations that involve overuse of the upper
extremities, such as athletes and personnel conducting overhead tasks,
were excluded from the study. Power analysis was performed using
G*Power 3.1 with β error = 0.8, Effect size = 0.6, and α = 0.05, resulting
in 20 shoulders in this study. Effect sizes were calculated based on a
preliminary study (Yanase et al., 2021b). The participants' average age,
height, and weight were 29.3 ± 3.3 years old, 172.2 ± 6.8 cm, and 63 ±
15.1 kg, respectively. This study was approved by the Ethics Committee
of Tottori Prefectural Central Hospital (approval number 2020–7). The
participants were fully informed about the purpose and methods of this
study and provided their consent.
2.2. Experimental protocol
The postures were the resting position with the neck in the neutral
position (Rest) and the contralateral bend and contralateral rotation of
the neck in the LS stretching position (Stretch). In the Rest position, the
participant sat comfortably on a stool, with eyes gazing forward, the feet
grounded on a parallel floor surface, the knee and hip joints at 90◦ each,
and the upper limbs hanging down toward the trunk (Fig. 1A). The
Stretch position was measured after rest. The participants were
instructed to actively move to the contralateral bend and rotate their
heads toward the non-examined side (Jeong et al., 2017). The partici­
pants performed contralateral bends and rotations within their pain-free
range of motion (Fig. 1B). The examiner manually applied resistance
toward the contralateral bend from the end of a range of LS stretching
position to 10 N using a hand-held dynamometer (μTasF-1, Anima, Inc.
Tokyo, Japan) to the participant's external occipital protuberance to
maintain a constant stretching load (Fig. 1C). The torque value at the
final stretching position was set to a constant to account for individual
differences in muscle stretching. This was preferred over quantifying the
stretching position using the cervical spine angle. Throughout the
measurement, the posture was maintained with full visual and verbal
attention to the correction of the trunk and shoulder blades, without
using belts or other means to correct the posture.
2.3. SWE
The shear moduli were measured using SWE with the Aplio i700
ultrasound imaging system (Canon Medical Systems, Inc., Tochigi,
Japan). A linear probe I18L X5 (frequency 4–18.3 MHz, peripheral fre­
quency 10 MHz) was used. The evaluated muscles were LS, SA, and Rm
(Fig. 1A). The shear modulus (kPa) was measured after the fibers of each
muscle were visualized along the long axis in the B mode. The ROIs were
consecutively set within the muscle fiber without the surrounding con­
nective tissue. The shear modulus was calculated by Q-Box™ consisting

Fig. 1. Probe location for muscle. A) The resting and B) stretching positions; C: The stretching position maintained using a hand-held dynamometer for: a) levator
scapulae (LS); b) upper fiber of serratus anterior (SA); c) rhomboid minor (Rm) muscles. A: The probe location for the A) LS, B) SA, and C) Rm muscles were: in the
long axis from the superior angle of the scapula toward the first cervical spine (probe orientation was the first cervical spine), in the long axis from the superior angle
of the scapula toward the first or second ribs (probe orientation was first and second ribs), and from the scapular spine triangle toward the seventh cervical vertebra
and first thoracic spine excluding the surrounding connective tissue (probe orientation was to the seventh cervical vertebra and first thoracic spine), respectively.

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K. Kawabuchi et al. Clinical Biomechanics 112 (2024) 106194

of a circular area (5 mm in diameter) on the ultrasound system. The
average of three values was considered as the representative value. The
probe was compressed carefully so as not to affect the shear moduli. In
LS, the probe was placed on the long axis from the superior angle of the
scapula toward C1, a long-axis image of the LS was delineated, and the
ROI was set within the muscle fibers on the second rib. The Q-Box™ was
placed consecutively around the second rib, totaling three placements.
(Fig. 2A). The SA was probed on the long axis from the superior angle of
the scapula toward the first and second ribs and delineated at a depth of
the trapezius muscle. The ROI was set within the muscle fibers on the
second rib, taking care to exclude the surrounding connective tissue. A
long-axis image of the LS was delineated, and the ROI was set within the
muscle fibers on the second rib. The Q-Box™ were placed consecutively
around the second rib totaling three placements. (Fig. 2B), the Rm was
probed from the triangle of the spine scapular to C7 and T1, and the ROI
was set within the muscle fibers of the medial border of the scapular
without surrounding connective tissue. Then, the Q-Box™ was consec­
utively placed from the medial border of the scapula, totaling three
placements. (Fig. 2C). The measurement results obtained were used to
calculate the rate of change by dividing each muscle's post-stretch shear
modulus by the pre-stretch value to determine if the changes in SA and
Rm were related to the changes before and after LS stretching. All sub­
jects were evaluated in the evening to minimize changes in the shear
modulus due to the time of day. To eliminate any potential effects of
measurement order, two forms containing a randomized order of mea­
surement of the studied muscles were prepared. Moreover, the stretch­
ing position was held for a minimal amount of time, approximately 10 s
or less, to allow full muscle extension as captured by the ultrasound
device. An experienced physical therapist, who has at least three years of
experience with ultrasound devices conducted the imaging procedures.
Three other physical therapists with 5–8 years of experience set and
recorded the ROI randomly. The reliability of the measurements was
examined using 10 participants before the study, and intraclass corre­
lation coefficients (ICC) were used to evaluate reliability. The repre­
sentative ROI values calculated for each muscle were compared with
those measured under the same conditions on different days. The ICC
(1,2) for LS, SA, and Rm at rest were 0.71 (95% confidence interval [CI]:
0.64–0.98), 0.70 (95% CI: 0.49–0.94), and 0.88 (95% CI: 0.43–0.98),
respectively. During the stretch, the ICC values were 0.93 (95% CI:
0.78–0.98) for LS, 0.93 (95% CI: 0.75–0.98) for SA, and 0.91 (95% CI:
0.79–0.99) for Rm. The standard error of measurement (SEM) for LS, SA,
and Rm at rest was 6.75, 3.55, and 6.22, respectively, while, during
stretch, the values were 5.36, 4.69, and 4.7, respectively (Weir, 2005).
2.4. Statistical analysis
All statistical analyses were performed using EZR version 1.52
(Saitama Medical Center, Jichi Medical University, Saitama, Japan).
Significant differences and correlations of the percentage change be­
tween each variable were determined. After confirming normality using
the Shapiro–Wilk test, significant differences and 95% CI for Rest and
Stretch were assessed using the corresponding t-test and Wilcoxon
signed rank test. The correlation of the percentage change in the shear
modulus between each muscle was determined using Spearman's rank
correlation coefficient. The significance level was set at 5% (P < 0.05).
The results are shown as mean ± SD.
3. Results
3.1. Comparison of the shear modulus between the resting and stretching
positions
Table 1 and Fig. 3 show the changes in the shear modulus of each
muscle in Rest and Stretch. The results demonstrated a notable increase
in the shear modulus from the Rest for LS (42.9 ± 17.6 kPa) and SA (32.8
± 12.9 kPa) to the Stretch for LS (52.4 ± 15.2 kPa) and SA (58.4 ± 18.5
kPa) (P = 0.02, 95%CI [1.8 to 17.0] and P < 0.01, 95%CI [15.4 to 32.0]),
respectively. However, there was no significant difference observed in
Rm between Rest (44.0 ± 19.2 kPa) and Stretch (41.0 ± 20.2 kPa),
respectively (P = 0.40, 95%CI [− 5.6 to 11.6]).
3.2. Correlation coefficient of the rate of change in each muscle
The correlation coefficients of the rate of change for each muscle
indicate a moderate yet significant positive correlation between LS and
SA (P = 0.04, r = 0.459, 95%CI [0.021 to 0.75]) (Table 2 and Fig. 4).
However, there were no significant differences between LS and Rm or
between SA and Rm (P = 0.3, r = − 0.245, 95%CI [− 0.62 to 0.22] and P
Table 1
Comparison of the shear modulus at Rest and Stretch positions.
Rest (kPa) Stretch (kPa) 95%CI P-value
LS 42.9 ± 17.6 52.4 ± 15.2* (1.8 to 17.0) 0.02
SA 32.8 ± 12.9 58.4 ± 18.5* (15.4 to 32.0) < 0.01
Rm 44.0 ± 19.2 41.0 ± 20.2 (− 5.6 to 11.6) 0.4
The shear modulus (kPa) and 95% confidence interval (CI) at rest and in the
stretching position for the levator scapulae (LS), the upper fiber of serratus
anterior (SA), and rhomboid minor (Rm) muscles.*Statistically significance at P
< 0.05.

Fig. 2. Elastogram windows of each muscle. A) Long-axis image of the levator scapulae muscle with a circular region of interest within the muscle fibers on the
second rib. The Q-Box™ were placed consecutively around the second rib, totaling three placements. B) Long-axis image of the upper fiber of the serratus muscle with
a circular region of interest within the muscle fibers on the second rib. The Q-Box™ were placed consecutively around the second rib, totaling three placements. C)
Long-axis image of the Rhomboid minor muscle with a circular region of interest within the muscle fibers on the medial side of the scapula. The Q-Box™ were
consecutively placed, starting from the inner edge of the scapula, totaling three placements. The white line indicates the medial side of the scapula.

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Fig. 3. Graphs comparing the shear modulus at Rest and Stretched Positions. The shear modulus (kPa) at rest and in the stretching position for the levator scapulae
(LS), the upper fiber of serratus anterior (SA), and rhomboid minor (Rm) muscles.*Statistically significance at P < 0.05.

= 0.7, r = 0.09, 95%CI [− 0.36 to − 0.51]).

Table 2
Correlations of the percentage of changes.
4. Discussion
r 95%CI P-value

LS-SA 0.459* (0.021 to 0.75) 0.04 This study investigated the EMFT between LS, SA, and Rm by spe­
LS-Rm − 0.245 (− 0.62 to 0.22) 0.30 cifically stretching LS to measure the in vivo shear modulus changes in
SA-Rm 0.09 (− 0.36 to − 0.51) 0.70 SA or Rm using SWE. We hypothesize that the shear modulus of the LS,
LS: levator scapulae muscle, SA: upper fiber of serratus anterior muscle, Rm: SA, and Rm, as a whole, might change due to connective tissues, even
rhomboid minor muscle, CI: confidence interval.*Statistically significance at P during stretching of the LS alone. The results showed that the shear
< 0.05. moduli of the LS and SA significantly increased during stretch. A mod­
erate yet significant positive correlation between LS and SA confirmed
our hypothesis. However, the shear modulus of Rm exhibited no sig­
nificant difference before and after stretching, and the correlation co­
efficients of the rate of change were also not significant. These outcomes
were contrary to our initial hypothesis.

Fig. 4. Scatter plot of the correlations between percentage changes.

The correlation coefficients of the rate of change for levator scapulae (LS), the upper fiber of serratus anterior (SA), and rhomboid minor (Rm) muscles. The cor­
relation between the rates of changes in A) LS- SA, B) SA- Rm, and C) LS-Rm. *Statistically significance at P < 0.05.

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K. Kawabuchi et al.
The contralateral bend and rotation motion of the neck signifi­
cantly increased the shear modulus of the LS. Yanase et al. investigated
specific stretching positions of the LS using SWE and showed that the
shear modulus increased significantly in the contralateral lateral bend,
consistent with the present findings (Yanase et al., 2021a). Interestingly,
the shear modulus also significantly increased in the SA with the
stretching of LS (Fig. 3). Further, the rates of changes between LS and SA
were moderately yet significantly correlated (Fig. 4). The SA originates
from the second rib and attaches to the superior angle of the scapula and
not to the cervical spine (Smit and Todd, 2019). Therefore, it might not
directly affect the limitation of lateral neck bend and can be interpreted
as passive stretching in conjunction with LS stretching. EMFT is trans­
mitted throughout the connective tissue, not just at the origin or inser­
tion of the muscle fibers (Huijing, 2007). A recent systematic scoping
review supported the existence of EMFT in vivo (Ajimsha et al., 2022).
Yoshitake et al. reported that EMFT of the upper extremity muscles
showed that a solitary stretch of the brachialis muscle by forearm
rotation altered the shear modulus of the biceps brachii muscle (Yosh­
itake et al., 2018). Therefore, the change in the shear modulus of SA at
Rest in response to specific stretching of the LS may be due to EMFT,
which might also exist during LS and SA of the periscapular muscles
stretching. The correlation coefficients of the rate of change for the shear
modulus of SA were larger than those of LS, probably because the area
measured in this study was the LS insert and not the origin or center of
the muscle. Moreover, the shorter muscle length of SA might cause a
change in the shear modulus. No significant difference was observed in
the shear modulus of Rm during Stretch, and no significant correlation
was found between the changes in the muscle shear modulus of LS and
Rm (Tables 1 and 2, Figs. 3 and 4). This might be due to the poor EMFT
effect between the LS and Rm due to muscle action. Generally, due to
their anatomical position, both the LS and Rm exhibit downward rota­
tion of the scapula (Ishikawa et al., 2021). Therefore, the downward
rotation force is probably generated at the scapular attachment site
when the LS is stretched. Thus, the shear modulus of Rm may not have
increased because of the relative muscle length toward the shortened
position, which may explain why EMFT was ineffective.
The clinical application of this study is to demonstrate that stretching
therapy affects the targeted muscle and its surrounding muscles.
Therefore, stretching and muscle-strengthening exercises that consider
EMFT are recommended. Fahmy et al. reported that treatment of
rhomboids resulted in improved neck pain and Neck Disability Index
scores, indicating the potential efficacy of physical therapy incorpo­
rating EMFT (Fahmy et al., 2021). Moreover, as an example of EMFT's
clinical application, if a patient desires to target the scapulothoracic
joint but has difficulty with scapular mobility due to pain or fracture,
incorporating EMFT into neck stretching might be an alternative
approach to improve joint flexibility. Further intervention studies are
required to investigate the potential benefits of this approach.
This study has some limitations. First, the participants included only
healthy males. Therefore, age-related, disease-specific, and gender dif­
ferences are unknown. Second, the relationship with other muscles,
particularly the trapezius, has not been evaluated. Upper trapezius fibers
(descending fibers) are stretched in cervical flexion with sides bent
away, while LS stretching comprises contralateral flexion and rotation
(El Laithy and Fouda, 2018). However, differences in cervical rotation
alone would not exclude the action of the trapezius muscle. Considering
these limitations, future research should include the upper trapezius and
other cervical muscles to clarify the force transfer between the muscles.
Resting muscle stiffness is defined as the absence of load or torque and is
confirmed by the lack of neuromuscular activity on electromyography
(Creze et al., 2018). Therefore, the changes in muscle stiffness should be
evaluated using electromyography. However, the muscles investigated
in this study were deep muscle groups, typically measured using fine-
wire electromyography (Castelein et al., 2015; Fennell et al., 2016).
Although electromyographic evaluation was not performed in this study
for technical and ethical reasons, further research is needed to consider
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Clinical Biomechanics 112 (2024) 106194
the effect of electromyography on the EMFT effect.
Furthermore, the correlation coefficient of the rate of change be­
tween LS and SA is a notable outlier, indicating a substantial change
(Fig. 4). Despite this outlier, the shear modulus values of LS and SA at
rest and after stretching did not significantly deviate from the norm
(Fig. 3). Consequently, they were not excluded as outliers in the corre­
lation coefficient of the rate analysis. Future investigations quantifying
muscle activity using electromyography are necessary to interpret these
data thoroughly. Moreover, while muscle shortening has been reported
in patients with scapular dyskinesis (Sağlam and Telli, 2022), this study
did not quantitatively evaluate or exclude scapular movement. There­
fore, during the subject inclusion phase in future studies, assessing the
scapular movement and performing muscle shortening tests is necessary.
5. Conclusion
This study indicated that the shear modulus of the SA changes when
the LS is stretched, suggesting the occurrence of EMFT between the LS
and SA. Therefore, our data indicates that force can be transmitted
through the fascia between muscles with different muscle insertions.
Funding
This study was not supported.
CRediT authorship contribution statement
Keita Kawabuchi: Writing – review & editing, Writing – original
draft, Supervision, Software, Resources, Project administration, Meth­
odology, Investigation, Formal analysis, Data curation, Conceptualiza­
tion. Kenta Yamane: Writing – original draft, Methodology,
Investigation, Data curation, Conceptualization. Shota Maniwa:
Writing – review & editing, Writing – original draft, Methodology,
Investigation, Data curation, Conceptualization. Kyohei Inoue: Writing
– review & editing, Writing – original draft, Project administration,
Methodology, Investigation, Conceptualization. Masatoshi Nakamura:
Writing – review & editing, Writing – original draft, Methodology,
Formal analysis, Conceptualization.
Declaration of competing interest
The authors report no competing interests.
Acknowledgments
The authors wish to thank their colleagues for their valuable insights
and discussions that have contributed to this research.
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