2. application over the tendon, a decrease in H-Reflex was observed,
showing a reduction of neuromotor excitability in normal (Kukulka
et al.,1986) and hemiparetic patients (Leone Kukulka,1988), after
applied pressure on the Achilles tendon. This likely to be a centrally
mediated inhibition has also been suggested to be a possible cause
for the observed force reduction after a series of massage applica-
tions to the iliotibial band (Hunter et al., 2006). A decline in the
power reduction was also reported after the massage of the
gastrocnemius muscle (Shin Sung, 2015). On the other hand, a
comprehensive study has shown that massage reduces neuromotor
excitability without affecting twitch contractile properties when
interpreted by analyzing the peak torque and derived parameters
(Behm et al., 2013). Therefore, to get some information about the
changes of the contractile properties of the muscle after massage,
the combined approach of using surface sensors became a plausible
method depicting EC coupling of active contractile properties of
muscle and force transmission of parallel elastic components of
muscle, both contributors to the overall EMD (Esposito et al., 2011;
Esposito et al., 2009). In the mentioned approach, combined sen-
sors such as EMG, MMG and Strain gauge were timely synchronized
where EMG provides important information of motor unit neural
activation during muscle contraction, MMG provides information
about dimensional changes of the transverse diameter of the muscle
fibers and Strain gauge provides information about force output
during a muscle contraction. The time lag between the onset of EMG
and MMG signal generation during contraction was attributed to EC
coupling while the time lag between MMG and Strain gauge signal
generation was attributed to force transmission along parallel
elastic components. In this approach, an MMG sensor was used as an
external sensor placed over the muscle belly and a signal displayed
was the summation of the surface oscillations including muscle,
sub-cutaneous tissue and the skin itself. Very recently this method
has been renewed where instead of an MMG sensor; an ultrafast
ultrasound was used depicting muscle oscillations from a certain
depth of the muscle tissue itself, therefore, excluding tissues above
the muscle and possible artifacts produced thereby (Begovic et al.,
2014). In this method, combined and timely synchronized EMG,
Ultrafast ultrasound and Strain gauge prompted an investigation
which would unveil potential changes of the contractile properties
and force transmission after TFM applied over the quadriceps fem-
oris tendon. These changes are displayed in terms of time delays
between generations of each signal where time delay between EMG
and US (muscle disturbance depicted from inside) onset provides an
indication of EC coupling duration, while a time between US and
Strain Gauge signal onset provides information about force trans-
mission and stiffness of series elastic components. Hence the aim of
our study was to find out what effects are produced in the muscle-
tendon complex as a result of TFM applied over mechanoreceptor-
rich tendon and myotendinous junction (MTJ). The time delays,
belonging to EC coupling and force transmission, both contributing
to EMD were computed during voluntary muscle contractions
before and after TFM. It was hypothesized that TFM may produce
twitch contractile changes (EC coupling) inside the muscle when
detected by centrally mediated voluntary muscle contraction.
2. Methods
2.1. Subjects
Fifteen healthy male subjects and fifteen age-gender matched
control subjects were recruited for the randomized control trial.
Upon enrollment, participants were randomly assigned to TFM and
control group using simple computer program to generate
randomness. One of the subjects from TFM group was not
compliant with experimental procedure; therefore, the subject was
excluded from the study and final number of subjects included in
TFM group was fourteen. All subjects were recruited from the Di-
vision of Interdisciplinary Biomedical Engineering with a very
identical age. They were without any history of previous injury,
metabolic or neurologic disease. Not one of them was involved in
any vigorous exercise on a daily basis. Not one of subjects was
familiar with particular group assignment or experimental proce-
dure until the familiarization session. The human subject ethical
approval was obtained from The Hong Kong Polytechnic
UniversityHSEARS20140215001.
2.2. Experimental design
Before visiting the laboratory of the Interdisciplinary Biomedical
Engineering Division at the Hong Kong Polytechnic University for
experimental procedure, subjects participated in a familiarization
session. The tested dominant leg including TFM was chosen as the
leg with which the subject preferred to kick a ball. After the
anthropometric measurements, subject was seated on the cali-
brated dynamometer (Humac/Norm Testing and Rehabilitation
System, Computer Sports Medicine, Inc., MA,USA). The 30 of knee
flexion was chosen to activate the muscle with minimum pre-
stretching of the muscle fibers (Sasaki et al., 2011).
The experimental procedure was well standardised with a
minimised risk of experimental bias as data acquisition and anal-
ysis were performed independent of each other at different times.
The experimental procedure and signal analysis were performed
mainly by authors, while TFM was performed by only one physical
therapist.
Muscle activity during voluntary isometric contractions was
recorded simultaneously by sEMG, Strain gauge and ultrafast US,
while the subject was seated on the calibrated dynamometer with
the knee flexion angle adjusted at 30 (Begovic et al., 2014) (Fig 1A).
The test procedure consisted of 4 repeated isometric contractions
followed by massage in TFM group and resting in control group and
ended up again with 4 repeated contractions of the QF muscle.
Between each contraction, a resting period of 2 min was allowed to
prevent muscle fatigue (Shi et al., 2007). During the test, the subject
was asked to apply maximum isometric contraction as quickly as
possible in 1 s and to keep it approximately for 3 s. Verbal order was
given to the subject about the start and termination of the muscle
contraction. The order “start” was given immediately after starting
the collection of A-mode signals in the ultrafast US device. After the
termination of each contraction, the position of the US probe was
checked to ensure that there was no displacement of the probe
caused by the movement artifact of the muscle during contraction
(Begovic et al., 2014; Shi et al., 2008; Shi et al., 2007; Strasser et al.,
2013; Guo et al., 2010; Wang et al., 2014).
2.3. Electromyography
Two surface EMG bipolar AgeAgCl electrodes (Axon System,
Inc., NY, USA) for differential EMG detection were attached on the
RF muscle belly, approximately at the 50e60% of the distance be-
tween the spina iliaca anterior superior and superior patellar
margin. To reduce the skin impedance, skin was cleaned with iso-
propyl alcohol and abraded with fine sandpaper. The ground elec-
trode was placed over the tibial crest. Interelectrode distance
between two sEMG electrodes was 30 mm. The sEMG signal was
amplified by a custom designed amplifier with a gain of 2000,
filtered by 10e1000 Hz bandpass analog filter within the amplifier,
and digitized with a sampling rate of 4 KHz (Begovic et al., 2014;
Guo et al., 2010).
H. Begovic et al. / Manual Therapy 26 (2016) 70e76 71
3. 2.4. Torque and rate of force development
A dynamometer with a back inclination of 80 and knee flexion
angle of 30 below the horizontal plane was used to measure tor-
que Tti
. The torque signals were digitized with a sampling rate of
4 KHz, and stored on a personal computer. The RFD was also esti-
mated using the torque:
RFD ¼ ðTt1
À Tt0
Þ=ðt1 À t0Þ
Where t0 is the force onset time, and t1 is the time of reaching 10%
maximum force. The average torque during the period of voluntary
isometric contraction was manually identified from the torque
wave. (Shimose et al., 2014; Zhou et al., 1995)
2.5. Ultrasound
The US recording was made by a custom program installed in a
programmable ultrasound scanner (Ultrasonix Touch, Analogic
Corporation, Massachusetts, USA) with a 7.5 MHz linear array ul-
trasound probe (Ultrasonix L14-5/35) to achieve a very high frame
ultrasound scanning at a selected location. The US probe was placed
as close as possible to the sEMG electrodes and longitudinally
(Fig.1A,B). The A-mode US signal was collected at a frame rate of 4 k
frames/s during 10s. After the first frame of A-mode signal was
collected, a signal was generated by the US scanner and outputted
as an external trigger signal, which was inputted into the device for
EMG/FORCE signal collection. The recorded US signal was pro-
cessed to detect the root mean square value (RMS) of the selected
region of interest (ROI). This RMS value obtained from each frame of
US signal was then substracted by the RMS value of the first frame
and the result was used to form a new signal representing the US
signal disturbance induced by the muscle contraction (Begovic
et al., 2014; Hug et al., 2011a; Mannion et al., 2008).
2.6. Transverse friction massage
TFM was applied transversely to the pull line of the QF muscle
tendon by the top of the index and middle fingers (Fig 1C). Duration
of TFM was about 15 min (Loew et al., 2014; Brosseau et al., 2002).
After TFM, the lower leg was detached from the dynamometer lever
arm because of uncomfortable feeling of tightness produced by the
straps over the lower part of the lower leg. The subject was advised
not to place the knee into deep flexion angle during TFM so to avoid
stretching effect of the QF muscle and tendon.
2.7. Data acquisition and analysis
Collected signals were processed off-line using a program
written in MatLab (version 2008a, USA). The EMG signal was
rectified and condition of three standard deviations (SD) from the
mean baseline noise was observed to detect the onset of each
signal. In order to define crossing time as the onset time, a condi-
tion for signal to stay 10 ms above the threshold level was set by the
program and visually examined. The time delays between onsets
(DtEMG-US, DtUS-FORCE and DtEMG-FORCE), TORQUE and RFD
were calculated off-line for each contraction. The same experi-
mental procedure was repeated immediately after an applied TFM
in massage group and a resting period in control group (Fig 2).
Fig. 1. Experimental set-up. A: Simultaneous recording of the Force signal, sEMG and Ultrafast US while subject performs an isometric contraction of the QF muscle. B: Application
of TFM by experienced physiotherapist. C: Position of the fingers above the QF tendon checked on US image before application of TFM.
H. Begovic et al. / Manual Therapy 26 (2016) 70e7672
4. 2.8. Statistical analysis
The data were analyzed with a software package SPSS V.19
(IBM,SPSS, Statistics for Windows, Version 19.0. Armonk,NY,USA).
The normal distribution of the data was analyzed by the Kolmo-
goroveSmirnov test. The One-Way Analysis of Variance (ANOVA)
for repeated measures was used to check whether there are any
differences between repeated contractions within the pre-
measurements of both TFM and control groups. An average and
SD were calculated if there was no difference between contractions
and this was used for the comparison between pre-TFM and post-
TFM in the massage group and between pre-resting and post-
resting in the control group. The paired sample T-test was used
for comparison of the means within groups, whilst, 2-way ANOVA
was used for comparisons between groups.
3. Results
The results about demographic characteristics of the subjects
are demonstrated in Table 1. All data was normally distributed,
therefore, One-Way ANOVA for repeated measures revealed that
there was no difference at all between 4 contractions in all data
from the pre and post tests (DtEMG-US, DtUS-FORCE, DtEMG-
FORCE, TORQUE and RFD, p 0.05), thus, averages were calculated
and used for comparisons.
After TFM, a significant increase in time delays of DtEMG-US
(pre:19.2 ± 9.0 ms, post:28.5 ± 8.8 ms, p 0.01) and DtEMG-FORCE
(pre:49.7 ± 9.9 ms, post:54.1 ± 11.8 ms, p 0.05) was found, whilst
the time delay of DtUS-FORCE (pre:30.5 ± 11.9 ms,
post:25.5 ± 11.3 ms, p 0.01) showed a decrease after TFM (Fig. 3).
In the control group, no significant difference between any
average of time delays was found when compared to the before and
after resting period of 15 min (DtEMG-US; pre 16.8 ± 6.9 ms,
post:16.6 ± 8.7 ms, p 0.05: DtUS-FORCE, pre:31.2 ± 8.5 ms,
post:30.7 ± 9.3 ms, p 0.05: DtEMG-FORCE; pre 48.0 ± 8.4 ms,
post:47.5 ± 9.9 ms, p 0.05). However, expectedly, there was also
no difference found between pre-measurements of TFM and the
control groups (DtEMG-US, p 0.05: DtUS-FORCE, p 0.05:
DtEMG-FORCE, p 0.05).
Since comparison before and after resting measurements in the
control group did not reveal any significant difference, the pre-
resting results were compared with after-TFM results and signifi-
cant increase of time delay was found in DtEMG-US, p 0.01 and
DtEMG-FORCE, p 0.01 and significant decrease was found inDtUS-
FORCE, p 0.01) (Fig. 4).
Comparison of the TORQUE and RFD between pre and post
measurements did not reveal any significant difference in both
control (Torque, pre:86.6 ± 21 Nm, post:83.8 ± 16 Nm: RFD,
pre:182.6 ± 68.1 Nm/s, post:164.9 ± 49.0 Nm/s) and TFM groups
(Torque, pre:93.7 ± 33 Nm, post:90.2 ± 34 Nm: RFD,
pre:181.3 ± 108.8 Nm/s, post:167.7 ± 114.5 Nm/s) (Fig. 5).
4. Discussion
The TFM has produced an increase of both the time required for
the EC coupling (DtEMG-US] and an overall time delay named as
the EMD [DtEMG-FORCE] after TFM and when compared with the
control. A force transmission through non-contractile elements,
when measured as a time delay between the onset of the fiber
motion and the onset of the force output (DtUS-FORCE], has dis-
played a significant decrease after TFM and also when compared
with the control group.
To justify the effect of manual therapy, such as TFM, prior
studies had often been focused on the measurement of a resting
EMG activity and muscle inhibition signs (Bennett et al., 2014;
Bialosky et al., 2009). The neurophysiological mechanism
involved in manual therapy is likely to originate from a peripheral
mechanism, spinal cord mechanism and/or supraspinal mechanism
but an advanced modification of research methodology, such as
ours, was needed to find out peripheral changes first within con-
tractile and non-contractile elements.
Fig. 2. An example of signal processing off-line using a program written in MatLab. Simultaneous recording of sEMG, US and Force was acquired during isometric contractions
before and after TFM. As onsets of each signal were coming out in a sequential order, time delays [Dt] were calculated off-line and statistically analyzed. A: automatically rectified
sEMG signal in designed MatLab program. B: disturbance signal acquired by ultrafast ultrasound from the selected region of interest. C: force signal acquired by active isometric
contraction of QF muscle.
H. Begovic et al. / Manual Therapy 26 (2016) 70e76 73
5. 4.1. Changes in electromechanical delay
It is likely that TFM, applied predominantly over the tendon and
MTJ, increases the EMD between the moment of the action po-
tential generation measured by surface EMG and force generation
measured by dynamometer. This time course has been used as a
reliable measure under different experimental circumstances,
when muscle dynamics were a matter of investigation (Esposito
et al., 2011; Begovic et al., 2014; Zhou, 1996; Grosset et al., 2009;
Hug et al., 2011(a); Hug et al., 2011(b)). The EMD has been attrib-
uted to the inside changes emerging from the musculotendinous
compliance and stiffness (Shin Sung, 2015), where the key role
players are contractile (active) and non-contractile (passive) com-
ponents of the musculotendinous complex (Esposito et al., 2011;
Hug et al., 2011(a); Hug et al., 2011(b)). It was reported that subjects
who showed the greatest increase in EMD also showed the greatest
decrease in musculotendinous stiffness, and vice versa (Grosset
et al., 2009) but without detailed investigation of the stiffness
changes in contractile and non-contractile elements.
4.2. Changes in EC coupling
EC coupling is one of the initial events inside the EMD, where
presented time is thought to be the time between action potential
generation and cross-bridge formation between contractile com-
ponents (Esposito et al., 2011; Hug et al., 2011(a); Hug et al.,
2011(b)). When a muscle is stretched or massaged as a whole
anatomic structure without focused application over the muscle or
tendon, detachment of the cross-bridges happens (Esposito et al.,
2011; Reisman et al., 2009) and the time required for the EC
coupling is expected to be increased. In our study, some measures
of precaution have been taken not to massage the muscle tissue
itself, relying on a popping feeling caused by the tendon motion
beneath the fingers, and ensuring that massage is applied over the
tendon. In this case, without massaging the muscle itself, detected
increase of time delay belonging to the EC coupling suggests that
TFM applied over the tendon may indirectly affect the twitch
contractile properties, via some afferent pathways and therefore
decreasing the active muscle stiffness. Since EC coupling has been
detected incorporating an US signal from inside the muscle,
detecting the onset of the muscle tissue motion, we could suggest
that increase in both EC coupling and EMD could be the conse-
quence of the reduction in the excitation of a-motor neurons. It is
likely that this inhibition is being initiated by stimulated Golgi-
tendon organs, which are predominantly located in the MTJ
(Guissard and Duchateau, 2006), causing presynaptic inhibition of
the a-motor neurons. It was also established that deep pressure
Table 1
Physical and anthropometric characteristics of the participants of both massage and
control group.
TFM group (n ¼ 14) Control group (n ¼ 15)
Age (years) 28.2 ± 3.25 29 ± 4.69
Weight (kg) 71.8 ± 10.16 73.6 ± 11.1
Height (cm) 172.4 ± 5.84 175.6 ± 7.5
BMI 24.1 ± 2.62 23.8 ± 2.72
Mid-sagital
thickness of
the RF (mm)
20.4 ± 2.40 12.3 ± 3.95
Fig. 3. Comparison of the Mean ± SD of 4 isometric contractions before and after
application of the TFM.
Fig. 4. Comparison of the means ± SD between pre-resting measurements of the
control and post-massage measurements of the TFD group.
Fig. 5. Comparison of the means ± SD torque and RFD results between PRE and POST in both control and TFD groups.
H. Begovic et al. / Manual Therapy 26 (2016) 70e7674
6. may produce synaptic changes in the brain, so that leads to the
reduction of the reflex activity (Roberts, 2011). This may likely be an
additional mechanism for the increased time of EC coupling
because of the involvement of the cortical areas during voluntarily
produced muscle contraction in our study.
With indirect evidence, it has been demonstrated that pressure-
sensitive and stretch-sensitive free nerve endings, connect to
inhibitory neurons, and therefore play a role in reducing motor-
neuron pool excitability (Lee et al., 2009; Ackermann PW, 2013).
On the other hand, it has been established that some group-III
afferent fibers, responsible for mediating mechanoreception,
terminate in intramuscular connective tissue and within muscle
spindles, which implies that the mechanoreceptors within the
muscle might respond to tendon stretch or pressure applied over
tendon (Nakamoto and Matsukawa, 2007).
Given the fact that our results were detected during voluntary
contraction; a remaining question is whether increased EC coupling
is caused by central mediation involving cortical area or some reflex
mechanisms inside a muscle? To unveil the central mediation, a
very recent study using different methodological approaches
detected the mean time delay between corticomotoneuronal cell
firing and the onset of facilitation of distal forelimb muscle activity.
Many results have been reported this time course ranging from 60
to 122 ms while a very recent study implementing an invasive
procedure applied spike and stimulus triggered averaging of EMG
activity and found this time delay ranging from 6.7 to 9.8 ms,
depending on the muscle group tested (Van Acker et al., 2015).
However, we are not able to bring any explanation as to the possible
variation of this time delay along the corticospinal pathway after
transverse friction massage because an onset time in our mea-
surement method was not from the cortical area. The contractions
in our experiment were voluntary muscle contractions, therefore,
we measured the onsets of muscle dynamics (peripheral actions)
by EMG, US and FORCE sensors relative to onset of the cortical area.
The time delay between EMG and FORCE is well known and
described as EMD including EC coupling and force transmission,
therefore, under our experimental circumstances, an increase of EC
coupling after TFM applied over tendon and excluding muscle itself
may show a decrease in the active stiffness of the muscle itself.
4.3. Changes in force transmission
Since TFM was applied over the tendon, it is expected that the
mechanical properties (visco-elasticity) of the tendon tissue are
affected (Hunter, 1998) and consequently finding an increased
elongation of the tendon, possibly leading to an increase of the time
needed for the force transmission during voluntary muscle con-
tractions. Therefore, given the expectation to find out an increased
time belonging to the force transmission, and therefore affected
viscoelasticity, we have found a significant decrease, which is
contradictory to the known effect of TFM. This decrease also be-
comes statistically significant when compared with a control group
suggesting that TFM applied over a tendon actually may stiffen the
tendon material. Therefore, faster force transmission (an increased
loading of the tendon) may have happened during voluntary
muscle contraction. This time was calculated between the onset of
the fiber motion detected by the US signal and the onset of the force
output. During the testing procedure, subjects were asked to pro-
duce an isometric contraction within the first second which means
that the tendon underwent very fast loading. As contraction in-
tensity increases, the time needed for force transmission decreases
together with an increasing in the intramuscular pressure (Esposito
et al., 2009; Pfefer et al., 2009; Earp et al., 2014). This also causes a
curvilinear increase of tendon stiffness as the force acting on the
tendon increases, resulting in a decreased tendon lengthening at
higher force levels (Earp et al., 2014).
Very recently, a similar finding was the reason to raise a ques-
tion, whether the application of transverse force components
applied over the muscle could be the cause of an increase of the
longitudinal loading of the MTU (Rushton Spencer., 2011). Even
though in that study results were obtained at the same time while
massage was being performed, it is difficult to make an argument
because our results were detected several minutes after TFM.
In the present study, contraction intensity was standardised in
such a way that subjects were asked to apply maximal voluntary
contraction within the first second after the onset of the
synchronised recording. An investigation of the relationship of
loading (contraction) intensity and muscle-tendon unit behavior
showed that increasing intensity caused a decrease in tendon
lengthening in humans (Earp et al., 2014). The lesser tendon
lenghtening during high contraction intensities means lesser
tendon compliance, faster force transmission, increased RFD, and
therefore increased loading of the tendon (Blackburn et al., 2009).
With increasing rate of loading, the muscle gets stiffer and a shorter
display of the EMD is expected (Blackburn et al., 2009). On the other
hand, it has also been reported that during a sustained isometric
contraction, the intramuscular fluid and acid accumulate, and
therefore, intramuscular pressure and muscle volume increase
(Crenshaw et al., 2000). This finding might be seen as disadvantage
when investigating the effect of massage because of prevailing high
contraction intensity that may attenuate effect produced by the
massage (Hunter et al., 2006). Therefore, in our study, fast
contraction within 1 s should be discussed as a possible method-
ological limitation. On the other hand, there should be paid
attention to our results because there was found a significant
decrease of time of force transmission along series elastic
components after TFM. It means that TFM is causing the stiffening
of the series elastic components (tendon). If found decreased time
of force transmission was caused by the TFM, then TFM should be
applied carefully before applying it on some sportsman who per-
forms plyometric exercises or any form of forceful muscle
contraction at any state of the pathological condition. This is an
important issue because we do not desire the overloading of the
joint in certain pathological conditions, particularly in the chronic
stage of tendinitis.
4.4. Rate of force development and torque
In the present study, there has not been observed any significant
change, neither in Torque nor in RFD after TFM. This non-significant
change should be reinvestigated with redesigned methodology, in
order to find out the answer whether or how much a contraction
intensity, including RFD and torque, is important when investi-
gating a massage effect.
On the other hand, our results could be quite convincing since
TFM, even at high muscle contraction intensities, shows the
persistent influence on the neuro-motor driving mechanism (sug-
gested to be via afferent pathways) and eventually increases the
time within the EC coupling. Since this time has been detected
during voluntary muscle contraction, it could be suggested that
dynamic stiffness of the muscle is most likely modified by the
effected activation patterns of the muscle. According to our results,
suggested decreased stiffness after TFM, mainly preceded by timely
increased EC coupling, is convincingly supported by our additional
finding of an increased EMD, and eventually decreased active
stiffness of the muscle. On the other hand, increased force trans-
mission could suggest an increasing stiffness of the tendon.
Author’s contributions HB conceptualized the study. HB and
GQZ conducted the experiments and analyzed the data. GQZ
H. Begovic et al. / Manual Therapy 26 (2016) 70e76 75
7. redesigned analyzing software. HB wrote the manuscript. YPZ
provided experimental materials, conceptualized ultrafast ultra-
sound, supervised research process and integrated the system with
GQZ. SS reviewed the manuscript and provided feedbacks. All au-
thors read and approved the final manuscript.
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