Physical Therapy in Sport 32 (2018) 109e114

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Physical Therapy in Sport

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Original Research

Intra- and inter-rater reliabilities for novel muscle thickness

assessment during Co-contraction with dual-rehabilitative ultrasound
imaging
Hwang-Jae Lee a, Hyun-Geun Ha b, Joohee Hahn c, Seungyeop Lim c, Wan-hee Lee d, *
a
Department of Health Sciences and Technology, Samsung Advanced Institute for Health Science and Technology (SAIHST), Samsung Medical Center,
Sungkyunkwan University, Samsung Medical Center Irwon-ro 81, Gangnam-gu, Seoul, 135-710, Republic of Korea
b
Department of Physical Therapy, Namseoul University, Namseoul Univ., Seonghwan-eup, Seobuk-gu, Cheonan-si, Chungcheongnam-do, Cheonan-city,
331-707, Republic of Korea
c
Department of Physical Therapy, The Graduate School, Sahmyook University, 815, Hwarang-ro, Nowon-gu, 01795, Seoul, Republic of Korea
d
Department of Physical Therapy, College of Health and Welfare, Sahmyook University, 815, Hwarang-ro, Nowon-gu, 01795, Seoul, Republic of Korea

a r t i c l e i n f o a b s t r a c t

Article history: Objectives: This study aimed to investigate the intra- and inter-rater reliabilities of dual-rehabilitative
Received 19 October 2017 ultrasound imaging (D-RUSI) for the simultaneous measurement of the thickness of the tibialis ante-
Received in revised form rior (TA) and gastrocnemius (GCM) muscles in healthy young adults.
26 February 2018
Design: A single-group repeated-measures reliability study.
Setting: Rehabilitative ultrasound imaging analysis laboratory.
Keywords:
Participants: Thirty-six healthy participants (23 males; age ¼ 26.36 ± 5.57 years).
Co-contraction
Main outcome measures: D-RUSI was used for the simultaneous measurement of the muscle thickness of
Reliability
Sonography
the TA and GCM at rest and during maximum voluntary contraction. Two examiners acquired data from
Tibialis anterior all participants during three separate testing sessions.
Results: In the results for the intra-examiner reliability of the TA and GCM muscle thickness for two
sessions, all ICC values (95% CI) were good to very good, ranging from 0.72 to 0.95 (SEM 0.01e0.05 mm,
MDC 0.02e0.13 mm, respectively). In the results for the inter-examiner reliability of the TA and GCM
muscle thickness for three sessions, all ICC values (95% CI) were good to very good, ranging from 0.78 to
0.97 (SEM 0.01e0.10 mm, MDC 0.02e0.15 mm, respectively).
Conclusions: These results suggest the potential usefulness of D-RUSI measurements for making man-
agement decisions related to muscle function, including muscle co-contraction.
© 2018 Published by Elsevier Ltd.

1. Introduction Sbriccoli, Marzattinocci, & Felici, 2006) and reduces lower-

Muscle co-contraction is the simultaneous contraction of
agonist and antagonist muscles cross the joint (Mari et al., 2014). It
is considered to be an important motor control strategy to improve
joint stability and movement accuracy (Humphrey & Reed, 1983).
Actually, instantaneous co-contraction of antagonist muscles, by
stiffening the joints, produces upper-extremity stability during the
execution of tasks requiring positional accuracy (Bazzucchi,
* Corresponding author.
E-mail addresses: goodptlee@skku.edu, goodptlee@gmail.com (H.-J. Lee), ptha@
naver.com (H.-G. Ha), dakdagrr@naver.com (J. Hahn), sapns@naver.com (S. Lim),
whlee@syu.ac.kr (W.-h. Lee).
extremity instability during gait (Lee, Chang, Choi, Ryu, & Kim,
2017). Moreover, the increased muscle co-contraction due to
various sports or musculoskeletal injuries is commonly described
as a compensatory mechanism to increase join stiffness that
thereby enhance stability or to avoid pain caused by damage (Nagai
et al., 2011; Oliver, De Ste Croix, Lloyd, & Williams, 2014). Thus,
muscle co-contraction should be a crucial factor to consider during
functional motor rehabilitation in sports and musculoskeletal in-
juries. In particular, a recent analysis including the tibialis anterior
(TA) and gastrocnemius (GCM) muscles showed that the amplitude
and timing of muscle co-contraction are correlated with age and
gait velocity of healthy adults (Hortobagyi et al., 2009; Lee et al.,
2017). This is consistent with the observation that elderly persons
exhibit greater contraction of the TA and GCM during the mid-

https://doi.org/10.1016/j.ptsp.2018.05.010
1466-853X/© 2018 Published by Elsevier Ltd.

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110 H.-J. Lee et al. / Physical Therapy in Sport 32 (2018) 109e114
stance phase at various gait speeds, suggesting increased co-
contraction across the ankle joint (Lee et al., 2017). In professional
soccer player, due to excessive co-contraction of the ankle joint it
has been reported that increases the risk of injury to a strong stress
on the joints (Oliver et al., 2014).
The ability of the muscles to generate force depends directly on
the structural properties (Blazevich & Sharp, 2005). In most studies,
the complex relationship between agonist activation and antago-
nists underlying muscle co-contraction is commonly examined
using surface electromyography (Hortobagyi et al., 2009; Lee et al.,
2017; Macaluso et al., 2002). Unlike traditional diagnostic tools,
such as surface electromyography, used to assess patients with
muscle problems, ultrasound imaging has been used to evaluate
the morphologic characteristics of muscles and related soft tissues
while the patient is at rest and during contracted states such as
walking and functional tasks (Linek, Saulicz, Wolny, & Mysliwiec,
2015). In the field of musculoskeletal research, ultrasound imag-
ing has been successfully used to studying the function of various
muscles (Overas, Myhrvold, Rosok, & Magnesen, 2017; Young,
Stokes, & Crowe, 1984). Heckmatt et al. studied muscle atrophy
and related pathological changes with ultrasound imaging was
excellent indicator for muscle wasting (Heckmatt, Pier, & Dubowitz,
1988). Peculiarly, rehabilitative ultrasound imaging (RUSI) has been
recommended as a noninvasive method of quantifying muscle
morphology, activation, and functional movement, and has been
increasingly used both in research and as a clinical tool throughout
the rehabilitative process (Whittaker et al., 2007). Furthermore,
RUSI has been used to assist in the application of therapeutic
intervention, providing feedback to the patient and physical ther-
apist (Teyhen, 2006). Through the measurement of muscle
contraction with RUSI, muscle thickness is the most easily and
readily obtained ultrasound measure of muscle size and has also
shown strong relationships to maximal torque (Abe, Loenneke, &
Thiebaud, 2015). However, conventional ultrasonic instruments
have only one probe for image measurements, limiting the number
of muscle that can be measured in real time to only one. Thus, the
conventional ultrasound equipment has been impossible to use for
the measurement of muscle co-contraction. To solve this problem,
the dual-RUSI (D-RUSI) device, which can possibly simultaneously
measure the contraction of two muscles (agonist and antagonist
muscles) with its two probes, and with the two muscle measure-
ments displayed on the screen of one personal computer, was
developed at TELEMED (dual-MicrUs EXT; TELEMED, Vilnius,
Lithuania) (Fig. 1).
Therefore, the main purpose of this study was to investigate the
intra- and inter-rater reliabilities of D-RUSI for the simultaneous
measurement of muscle thickness during co-contraction of the TA
and GCM with rest and maximal dorsiflexion in healthy young
adults. We hypothesized that RUSI is suitable reliable study and
clinical tool for the measurement of co-contraction of ankle joint
muscles.
2. Materials and methods
2.1. Participants
This study applied a single-group repeated-measures design.
Two examiners acquired the images from all participants on two
separate test sessions with an interval of 7 days. Thirty-six healthy
young participants aged 20e36 years (23 men, 13 women) were
included in the study. The participants had no history of muscu-
loskeletal pain or disease within the last 3 months. The exclusion
criteria were musculoskeletal or neuromuscular disorders in the
lower extremity, pregnancy, and body mass index >30 kg/m2.
We explained to all participants the purpose and requirements
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of our study and voluntarily signed the informed consent form. The
study was approved by the (xx) Institutional Review Board.
2.2. Examiners
Two physical therapists participated in the reliability analysis as
examiners. Examiner 1 was a physical therapist for 5 years and
Examiner 2 was a physical therapist for 25 years. Before the start of
this study, both examiners underwent 7 days (2 h a day for a total of
14 h). of specific training in image capturing and measurement of
the thickness of the TA and medial GCM muscles, with a profes-
sional instructor who is a professor of physical therapy experienced
with the specific D-RUSI protocol used in this study.
2.3. Study protocol
The two examiners acquired ultrasound images of all partici-
pants in two individual measurement sessions (1st test and 2nd
test). After the 1st test was performed, the 2nd test was performed
one week later. Measurement sessions were held at the same time
of the day for each participant. Researcher instructed participants
not to do much activity for 7 days after measuring 1st test and also
checked the activity of all participants for 7 days before measuring
2nd test.
2.4. Measurement procedure
Before the first measurement, the anthropometric variables of
the participants were measured by one skilled rater. The calf
circumference and tibial length were measured at the thickest part
of the calf muscle belly by using a tape measure. The D-RUSI device
used in the study to measure the muscle thickness of the TA and
GCM was an imaging unit set in real-time B-mode with a 7.5-MHz
dual-linear array transducer. Presets were standardized at a fre-
quency of 13 MHz and depth of 4 cm. Measurements of muscle
thickness for the TA and GCM at rest and during maximum
voluntary contraction were performed on the dominant side of
each participant. Each participant was asked to perform dorsi-
flexion and plantarflexion of the ankle joint to the maximum extent
possible. Strong verbal encouragement was given during every
contraction to promote maximal effort. The muscle thickness of the
TA was defined as the distance between the superficial and central
aponeurosis(Maganaris & Baltzopoulos, 1999). Furthermore, the
muscle thickness of the GCM was defined as the distance between
the superficial and deep aponeurosis (Konig, Cassel, Intziegianni, &
Mayer, 2014) (Fig. 2). These parameters have been considered to
determine whether aponeuroses are parallel.
To assess the muscle thickness of the TA and GCM during ankle
dorsiflexion, the participants sat on a chair with a backrest. Images
of the co-activation during ankle dorsiflexion were obtained with
the ankle joint in neural position (90 ) and at maximal isometric
contraction (Keep ankle dorsiflexion 15 for 5 s) with manual
resistance by the examiner. The maximal isometric contraction
values were obtained by using a digital manual muscle tester (Po-
wer Track II; JTECH Medical, Salt Lake City, UT, USA). The time point
of the measurement was obtained at 5 s point in the maximal
isometric contraction state. The scan image of the TA was taken at a
point 20% of the superior distance from the head of the fibula to the
tip of the lateral malleolus(McCreesh & Egan, 2011). The distance
between the head of the fibula to the tip of the lateral malleolus
was measured by using a measuring tape. Furthermore, the scan
image of the GCM was taken at a point 30% of the tibial length,
defined as the distance from the popliteal crease to the midpoint of
the medial malleolus (Raj, Bird, & Shield, 2012) (Fig. 2). Initially, in
order to standardize the position of the transducer for each
 H.-J. Lee et al. / Physical Therapy in Sport 32 (2018) 109e114 111

Fig. 1. Configuration of Dual-Rehabilitative Ultrasound Imaging (D-RUSI) equipment.

Fig. 2. (A) RUSI imaging of muscle thickness of TA (right) and scanning position (left), (B) RUSI imaging of muscle thickness of TA (right) and scanning position (left).
RUSI: Dual-Rehabilitative Ultrasound Imaging, TA: tibialis anterior, GCM: gastrocnemius.

measurement location it is marked on the skin. This location was was used to hold the ultrasound probe on the predefined location.
marked on the skin with a marker pen. To allow the quantification We analyzed both the imaging and calculated measurements of
of the independent influence of probe positioning, a Velcro strap muscle thickness by using Echo Wave II 3.6.1. b (TELEMED). All

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112 H.-J. Lee et al. / Physical Therapy in Sport 32 (2018) 109e114
measurements were taken two times for each participant by an
individual examiner, and the average value was used for statistical
analysis.
2.5. Statistical analysis
All statistical analyses were conducted with SPSS version 22.0
(IBM, Armonk, NY, USA), and the level of significance was set at
0.05. To illustrate the reliability of D-RUSI measurements, we
calculated the intra-class correlation coefficients (ICCs) with 95%
confidence interval (CI) for the muscle thickness of TA and GCM
between the two ankle positions (rest and maximal voluntary
contraction condition). ICCs values less than or equal to 0.02 were
considered poor, 0.21e0.40 fair, 0.41e0.60 moderate, 0.61e0.80
good, and 0.81e1.00 very good(Mota, Pascoal, Sancho, & Bo, 2012).
Additionally, standard error of measurement (SEM) and minimal
detectable change (MDC) were calculated. MDC was calculated as
1.96  SEM  √2, where 1.96 derives from 95% CI of no change and
the √2 is included because 2 measures were involved in measuring
change. (Beckerman et al., 2001). Statistical significance was
defined at p < 0.05.
3. Results
Thirty-six participants (mean ± SD, 26.36 ± 5.57 years)
completed this study. The demographics and baseline characteris-
tics of participants are shown in Table 1. The results for the intra-
examiner reliability of the TA and GCM muscle thickness for two
sessions for the two examiners are summarized in Table 2. All ICC
values (95% CI) were good to very good, ranging from 0.720 to 0.945
and CI was within an acceptable range from 0.720 to 0.945. The
SEM values ranged between 0.08 and 0.49 mm for TA and GCM
muscle thickness. In addition, MDC ranged between 0.021 and
0.127 mm for TA and GCM muscle thickness.
A summary of the results for the inter-examiner reliability of the
TA and GCM muscle thickness for three sessions for the two ex-
aminers is shown in Table 3. All ICC values were good to very good,
ranging from 0.889 to 0.966, whereas the SEM ranged from 0.008 to
0.102. Additionally, the MDC ranged from 0.022 to 0.233 mm.
4. Discussion
The evaluation and monitoring of most musculoskeletal disor-
ders is expanding due to technological advancements associated
with Magnetic Resonance Imaging (MRI), computed tomography
(CT) and ultrasound imaging. These imaging techniques provide
useful qualitative and quantitative measures concerning the
muscular architecture (e.g. muscle thickness, fascicle length and
pennation angle), including the consequential muscular atrophy
shown to be common in patients with musculoskeletal disorder
and sports injury patients (Djordjevic, Djordjevic, &
Konstantinovic, 2014; Heinonen, McKay, Whittall, Forster, &
Table 1
General characteristics of the participants.
Parameters Male (n ¼ 23) Female (n ¼ 13) Overall (n ¼ 36)
Age (years) 26.61 (5.60) 25.92 (5.81) 26.36 (5.57)
Height (cm) 172.96 (5.97) 162.08 (3.90) 169.03 (7.46)
Weight (kg) 65.91 (7.48) 55.62 (3.86) 62.19 (8.09)
Body mass index (kg/m2) 22.05 (2.45) 21.17 (1.73) 21.74 (2.23)
Tibial lengtha (cm) 33.92 (1.01) 32.21 (0.81) 32.93 (1.49)
Calf circumference (cm) 28.63 (2.58) 25.80 (2.42) 27.61 (2.84)
Values are expressed as n or mean (SD).
a
The distance from the popliteal crease to the midpoint of the lateral malleolus.
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Khan, 2001; J. H.; Kim et al., 2013). Specifically, ultrasound imag-
ing has advantage as a safe, cost-effective, portable and clinically
accessible method for gathering information about the static
muscle architectures, as well as muscle movement dynamic activity
(Jopowicz, Jopowicz, Czarnocki, Deszczynski, & Deszczynski, 2017).
Ultrasound imaging techniques have been used in the in-
vestigations of muscle activation and architecture in athlete with
soccer player (Idoate, Calbet, Izquierdo, & Sanchis-Moysi, 2011),
young children (Legerlotz, Smith, & Hing, 2010), elderly adults (Raj
et al., 2012), developing adults (Maganaris, Baltzopoulos, &
Sargeant, 1998) and patients with neuromuscular disorder (H. D.
Kim, You, Han, Eom, & Kim, 2014). In particular, physical therapists
in the sports and musculoskeletal rehabilitation field have recently
begun using RUSI to assess muscle function and action, and change
in the architecture of various muscles is considered an indicator of
the voluntary or automatic activity of the muscles (Dawes &
Seidenberg, 2014; Hannesschlager, Reschauer, Riedelberger, &
Stadler, 1988; Linek, 2018). Consequently, RUSI can play an newly
important role in the training and re-education of weak muscles as
well as assessment in physical therapeutic screening and rehabili-
tation program (Whittaker et al., 2007).
The main results of this study demonstrated that D-RUSI is a
sufficiently reliable tool for the measurement of the co-activation of
the TA and GCM muscles. This finding emphasizes an important
aspect that needs to be considered in the measurement of muscle
co-activation in the research and clinical fields. The reliability of
ultrasound imaging for TA evaluations in a previous study was high,
showing that it is a highly sensitive and quantitative method (ICC
for intra-rater reliability, 064e0.99; ICC for inter-rater reliability,
0.69e0.99) (Cho, Lee, & Lee, 2017). Also, RUSI measurement of
medial GCM muscle thickness showed a high reliability for the
evaluation of muscle activation in resistance trained males (ICC of
0.89e0.95), young children (ICC of 0.94e0.98), older adults (ICC of
0.92e0.99) and stroke patients (ICC for intra-rater reliability,
069e0.99; ICC for inter-rater reliability, 0.70e0.99) (Cho, Lee, & Lee,
2014; Legerlotz et al., 2010; McMahon, Turner, & Comfort, 2016; Raj
et al., 2012). Moreover, Chow et al. demonstrated that thickness
(male 13.8 mm and female 14.7 mm) of the medial GCM muscle
with rest condition in normal adults differed significantly between
male and female (Chow et al., 2000). The results of these previous
studies supported our results that RUSI measurements of TA and
GCM muscle thickness is adequately reliable for research and
clinical rehabilitation. Therefore, RUSI measured data could be used
to changes in muscle thickness in various target group. However,
most ultrasound imaging techniques have been limited to single
muscle measurements. This limitation makes it difficult to use ul-
trasound imaging equipment in a variety of muscle activation
studies. To overcome this limitation, D-RUSI was developed. An
interesting finding of the current study is that despite the simul-
taneous measurement of two muscles, the intra- and inter-rater
reliabilities of D-RUSI for measurements of the muscle thickness
of the TA and GCM were good to very good (Tables 2 and 3).
In the field of sports injury research, leg stiffness due to
increased muscle co-contraction during specific exercise in athlete
may be a necessary change to compensate for poor stability. More
important, excessive co-activation of the ankle joint muscles (TA
and GCM) is likely to increase the energy cost during specific ex-
ercise, thereby inducing fatigue and increasing Secondary Muscu-
loskeletal problems (Oliver et al., 2014). Therefore, muscle co-
activation is clinically important. However, in most of the previ-
ous studies, surface electromyographic analysis has been used to
evaluate muscle action and co-contraction during functional
movement and locomotion (Bautmans et al., 2011; Lee et al., 2017;
Mari et al., 2014). Assessment of simultaneous muscle co-activity
can provide information about only muscular torque signals
 H.-J. Lee et al. / Physical Therapy in Sport 32 (2018) 109e114 113

Table 2
Intra-examiner reliability between measures for muscle thickness test.

Test session F (p) ICC 95% CI SEM MDC

1st test (SEM) 2nd test (SEM)

TA Examiner 1 MT (mm) R 12.30 ± 3.37 (0.80) 12.44 ± 2.65 (0.63) 4.20 (0.001) 0.862 0.786e0.871 0.027 0.067
C 14.43 ± 2.85 (0.38) 14.30 ± 2.76 (0.37) 2.62 (0.001) 0.867 0.776e0.922 0.015 0.042
Examiner 2 MT (mm) R 12.93 ± 2.87 (0.32) 12.88 ± 3.34 (0.37) 3.50 (0.001) 0.888 0.813e0.925 0.048 0.127
C 14.47 ± 3.13 (0.58) 14.30 ± 2.76 (0.51) 5.44 (0.001) 0.836 0.780e0.900 0.008 0.021
GCM Examiner 1 MT (mm) R 13.68 ± 2.87 (0.29) 14.02 ± 3.23 (0.33) 9.87 (0.001) 0.899 0.824e0.945 0.012 0.048
C 14.51 ± 2.83 (0.35) 15.02 ± 3.22 (0.40) 8.01 (0.001) 0.876 0.783e0.932 0.015 0.031
Examiner 2 MT (mm) R 13.78 ± 3.37 (0.42) 13.86 ± 3.14 (0.40) 3.63 (0.001) 0.874 0.771e0.910 0.024 0.018
C 14.59 ± 3.72 (0.57) 14.67 ± 3.42 (0.52) 3.95 (0.001) 0.847 0.720e0.914 0.049 0.131

ICC: intraclass correlation coefficient, 95% CI: 95% confidence interval, SEM: standard error of the measurement, MDC: minimal detectable change, TA: tibialis anterior, GCM:
gastrocnemius, MT: muscle thickness, R: rest, C: contraction.

Table 3
Inter-examiner reliability between measures for muscle thickness test.

Muscles Conditions 1st test 2nd test

ICC 95% CI SEM MDC ICC 95% CI SEM MDC

TA thickness (mm) R 0.889 0.799e0.906 0.102 0.028 0.894 0.849e0.936 0.084 0.233
C 0.893 0.814e0.939 0.054 0.149 0.893 0.802e0.959 0.034 0.094
GCM thickness (mm) R 0.915 0.891e0.953 0.013 0.036 0.918 0.849e0.966 0.008 0.022
C 0.901 0.867e0.931 0.021 0.058 0.910 0.863e0.951 0.012 0.033

ICC: intraclass correlation coefficient, 95% CI: 95% confidence interval, SEM: standard error of the measurement, MDC: minimal detectable change, TA: tibialis anterior, GCM:
gastrocnemius, MT: muscle thickness, R: rest, C: contraction.

without the monitoring of muscle architecture. Muscle architecture Conflicts of interest

parameters such as muscle thickness, pennation angle, and cross-
sectional area are highly correlated with muscle function The authors declare that there are no conflicts of interest,
(English, Fisher, & Thoirs, 2012). Therefore, we believe that quan- financial or otherwise, related to the submitted manuscript or any
tifying the change in the muscle co-activation and architecture by aspect associated with this research.
using D-RUSI may provide an indirect means of measuring muscle
function and muscle recovery, and of monitoring interventions Ethical approval
designed to limit muscle problems.
Another interesting finding of this study is that despite the The study was approved by the Sahmyook University Institu-
differences in clinical experience between the examiners, D-RUSI tional Review Board (reference no. 2-1040781-AB-N-01-
was consistently shown to be a reliable method for measuring the 2016085HR).
co-activation of the TA and GCM because the examiners underwent
specific training in D-RUSI measurements. In our study, two phys- Funding
ical therapists with different lengths of clinical experience partici-
pated as examiners, which allowed investigating the measurement This study was supported by the Health Sciences for Speciali-
differences according to the clinical experience of examiners. The zation Project Fund of the Sahmyook University in 2016.
two examiners had 5 and 25 years of clinical experience,
respectively.
Acknowledgments
The current study has several limitations. First, the sample size
was very small. Thus, the results cannot be generalized to all human
The authors would like to thank the subjects who participated in
populations. Another limitation was that the study was limited to
this study.
the young age group. This study needs to be further performed in
participants of various ages. Moreover, in future studies, it is
Appendix A. Supplementary data
necessary to target patients with various neuromuscular disorders.

Supplementary data related to this article can be found at

https://doi.org/10.1016/j.ptsp.2018.05.010.

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