Download Relationship between knee joint angle and fine

Relationship between knee joint angle
and fine-wire EMG activity of the four
quadriceps femoris muscles
Gustaf Rönquist
THE SWEDISH SCHOOL OF SPORT
AND HEALTH SCIENCES
Master degree project 36:2015
Master of Science (30 credits) in Sport Science 2013-2015
Supervisor: Maria Ekblom
Examiner: Karin Söderlund
Abstract
The purpose of the present study was to investigate the electromyography (EMG)-knee joint
angle relationship and the differences in activity among the four quadriceps femoris (QF)
muscles during maximal voluntary isometric knee extensions. Ten well-trained healthy male
volunteers (mean ± 1 standard deviation (SD) age 33 ± 11 years, height 1.83 ± 0.07 m, body
mass 79 ± 4.7 kg) performed maximal isometric knee extensions in a seated position at four
different knee joint angles (90º, 65º, 40º, and 15º of knee flexion). Myoelectric activity was
simultaneously recorded from rectus femoris (RF), vastus lateralis (VL), vastus medialis
(VM), and vastus intermedius (VI) using fine-wire EMG. Root-mean-square (RMS) was
calculated during a sustained phase of one second at each of the different knee joint angles
tested. Results showed that the RMS value of the VM was significantly higher at 90º
compared to 40º (P < 0.05). When comparing 90º-normalized RMS values among the four QF
muscles collapsed across the three most extended positions (65º, 40º, and 15º of knee
flexion), significantly lower normalized RMS value was observed for the VM compared to
that of the RF (P < 0.01) and VL (P < 0.05), respectively. No significant differences in RMS
values between knee joint angles were observed for any of the other QF muscles (RF, VL, and
VI). These results suggest that VM muscle activity is highest at more flexed knee joint angles
during a seated knee extension task. Further, as the knee gets more extended, muscle activity
of the VM decreases and VM becomes less active than the VL and RF, respectively.
Sammanfattning
Syftet med denna studie var att undersöka sambandet mellan elektromyografisk aktivitet
(EMG) och vinkel i knäled, samt att jämföra skillnaden i aktiveringsgrad mellan quadriceps
femoris (QF) fyra delmuskler vid maximala viljemässiga isometriska knäextensioner. Tio
vältränade friska män (medelvärde ± 1 standardavvikelse, ålder 33 ± 11 år, kroppslängd 1,83
± 0,07 m, kroppsvikt 79 ± 4,7 kg) deltog frivilligt i studien. Samtliga deltagare genomförde
maximala isometriska knäextensioner i sittande position vid fyra olika vinklar i knäled (90º,
65º, 40º och 15º knäflexion). Myoelektrisk aktivitet registrerades samtidigt från rectus
femoris (RF), vastus lateralis (VL), vastus medialis (VM) och vastus intermedius (VI) med
hjälp av intramuskulär EMG (trådelektroder). Det kvadratiska medelvärdet (engelska rootmean-square, RMS) beräknades under en en-sekundersperiod vid respektive ledvinkel.
Resultaten visade att RMS-värdet för VM var signifikant högre vid 90º jämfört med 40º (P <
0,05). Vid en jämförelse av 90º-normaliserade RMS-värden mellan QF olika delmuskler för
de tre mest extenderade positionerna (65º, 40º och 15º knäflexion) observerades signifikant
lägre normaliserade RMS-värden för VM jämfört med RF (P < 0,01) respektive VL (P <
0,05). Inga signifikanta skillnader i RMS-värde mellan de olika ledvinklarna sågs för någon
av de övriga delmusklerna (RF, VL och VI). Dessa resultat tyder på att VM är som mest aktiv
vid mer flekterade knäledsvinklar under sittande knäextensioner. Vidare kommer aktiviteten i
VM att minska allteftersom knäet blir mer extenderat, och dess aktivitet blir då lägre jämfört
med VL respektive RF.
Abbreviations
ACL
anterior cruciate ligament
ANOVA
analysis of variance
BMC
biomechanics and motor control
EMG
electromyography
e.g.
exempli gratia
i.e.
id est
MRI
magnetic resonance imaging
MVC
maximal voluntary contraction
PAP
post activation potentiation
QF
quadriceps femoris
RF
rectus femoris
RMS
root-mean-square
SD
standard deviation
VI
vastus intermedius
VL
vastus lateralis
VM
vastus medialis
VML
vastus medialis longus
VMO
vastus medialis obliquus
Table of content
1 Introduction ............................................................................................................................. 1
1.1 History of electromyography ........................................................................................... 1
1.2 Background ...................................................................................................................... 2
1.3 Sport science relevance .................................................................................................... 6
1.4 Aim ................................................................................................................................... 7
2 Materials and methods ............................................................................................................ 7
2.1 Subjects ............................................................................................................................ 8
2.2 Fine-wire electrode preparation ....................................................................................... 8
2.3 Electromyographic recordings ......................................................................................... 9
2.3 Experimental protocol .................................................................................................... 10
2.4 Data analysis .................................................................................................................. 11
2.5 Statistics ......................................................................................................................... 12
2.5 Ethical considerations .................................................................................................... 12
3 Results ................................................................................................................................... 13
4 Discussion ............................................................................................................................. 15
4.4 Conclusion...................................................................................................................... 25
Acknowledgements .................................................................................................................. 26
References ................................................................................................................................ 27
Appendix 1 Literature search
Appendix 2 Health declaration questionnaire
Appendix 3 Written form of consent
List of figures
Figure 1 – Approximate insertion sites for the intramuscular electrodes .................................. 9
Figure 2 – Screenshots from the ultrasound during electrode insertion ................................... 10
Figure 3 – Normalized RMS values for RF, VL, VM, and VI at different knee joint angles .. 14
Figure 4 – Comparison of normalized RMS values between RF, VL, VM, and VI ................ 15
Figure 5 – Torque values at the four different knee joint angles ............................................. 15
1 Introduction
Understanding how different muscles interact may play an important role when designing
rehabilitation or sports performance enhancing strength training programs. Even though many
previous studies have investigated the activity of the individual muscles comprising the
quadriceps femoris (QF) muscle group during isometric knee extensions, there is still
uncertainty concerning how the activity level is affected by different knee joint angle settings
(Hasler, Denoth, Stacoff & Herzog 1994; Brownstein, Lamb & Mangine 1985; Eloranta 1989;
Pincivero, Salfetnikov, Campy & Coelho 2004; Watanabe & Akima 2011a; Saito & Akima
2013; Hallén & Lindahl 1967; Lieb & Perry 1971; Salzman, Torburn & Perry 1993; Zabik &
Dawson 1996), and whether the activity level differs between the individual muscles
(Salzman et al. 1993; Pincivero et al. 2004; Watanabe & Akima 2011a; Saito & Akima 2013).
QF muscle activity is most commonly studied using electromyography (EMG) with surface
electrodes, which are placed on top of the skin over the muscle of interest. However, this
method can be considered to be non-specific, since the signal recorded is often contaminated
with myoelectric activity originating from adjacent or deeper muscles other than the muscle
of interest (De Luca & Merletti 1988; De Luca 1997; Türker 1993). This problem is
eliminated if fine-wire electrodes, which are percutaneously inserted into the muscle, are used
instead (Türker 1993; De Luca 1997). To our knowledge, no previous study has used finewire EMG to fully investigate how the activity level of the individual QF muscles are affected
by different knee joint angle settings, and if the activity level differs between the individual
muscles. Therefore, we intend to investigate the EMG-knee joint angle relationship and the
differences in activity among the four QF muscles during maximal voluntary isometric knee
extensions using fine-wire electrodes.
1.1 History of electromyography
In the late 18th century, Luigi Galvani showed that electrical stimulation of the crural muscle
nerves in frog hind-limb preparations produces muscle contraction and force development
(Piccolino 1998). However, it was not until 1849 that DuBois first demonstrated that
myoelectric signals could be detected during a voluntary contraction in human subjects (De
Luca 2006). The first method to record and quantify action potentials from a single motor unit
in human subjects was presented in 1929 by Adrian and Bronk. Using a needle electrode that
was inserted into the triceps brachii muscle and then connected to an amplifier and a loud
speaker, they were able to make both visual and auditory recordings of myoelectric activity
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during voluntary contractions. (Adrian & Bronk 1929) In 1948, Hodes, Larrabee, and German
were first to measure the combined potential of several individual muscle fibers during
percutaneous electrical nerve stimulation, using electrodes placed on the surface of the skin
(Hodes, Larrabee & German 1948). Today EMG provides many important and useful
applications, such as biofeedback in rehabilitation (Giggins, Persson & Caulfield 2013), gait
analysis (Sutherland 2001), and clinical diagnosis for muscular disorders (Ghaoui, Clarke,
Hollingworth & Needham 2013). Myoelectric signals that are generated by active muscle
fibers can be registered using surface electrodes or indwelling electrodes. The surface
electrodes are placed on top of the skin directly over the muscle, therefore providing a noninvasive alternative, whereas indwelling electrodes are percutaneously inserted into the
muscle. EMG registration using indwelling electrodes, often called intramuscular EMG, can
be done using either needle electrodes or fine-wire electrodes. (Kamen & Gabriel 2010, p. 5663)
1.2 Background
The QF muscle group consists of four individual muscles: rectus femoris (RF), vastus lateralis
(VL), vastus medialis (VM), and vastus intermedius (VI). All four of these act as extensors of
the knee joint. RF is the only one of the QF muscles that is bi-articular, also contributing to
flexion at the hip joint. Based on theoretical estimations from anatomical measures in human
cadavers, Herzog, Hasler, and Abrahamse (1991) reported that the individual QF muscles
display different force-length relationship curves. Further, they found that a summation of
these estimated force-length relationship curves agreed well with force-length relationship
curves obtained experimentally during isometric knee extensions. Thus it appears that the
possible contribution of the individual QF muscles to knee extension torque differs between
knee joint angles. (Herzog et al. 1991)
Muscle force production is primarily affected by its activation (Herzog et al. 1991), and an
increase in muscle force is generally associated with an increase in EMG signal amplitude
(De Luca 1997). Therefore, EMG measures can be used to confidently determine the onset
time of muscle activation, if muscle activation is present or not, and if the activation level in a
non-fatigued muscle is increasing or decreasing over a period of time. The EMG signal
amplitude can also provide information about the force contribution of individual muscles
acting on a joint during a specific task. However, for precise calculations of muscle force
production and its contribution to the resultant muscular moment acting on a joint there are
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several other factors to consider. (De Luca 1997) For example, muscle force production is
positively correlated with muscle cross-sectional area (Maughan, Watson & Weir 1983).
Further, muscle force production is also affected by muscle fiber length, and as muscle length
changes so does the length of the muscle moment arm (De Luca 1997). Previous studies have
reported differences in QF moment length-angle curves between cyclist and runners
(Savelberg & Meijer 2003), and De Luca (1997) has stated that muscle moment arm length
varies between individuals. Consequently, depending on the joint angle setting and due to
individual anatomical variations, the resultant muscular moment acting on a joint can slightly
differ, even if the muscle force production or EMG signal amplitude is equal. The EMG
signal amplitude is also affected by other factors, like muscle activation type (e.g. concentric
or eccentric), contraction velocity, and muscle fatigue (Potvin 1985). Summarized, EMG
provides the possibility to study the fore production of individual muscles in vivo. However,
the relationship between EMG signal amplitude, muscle force production, and joint net
moment is difficult to precisely quantify. (De Luca 1997)
Previous EMG studies reporting on the relationship between knee joint angle and the
activation of individual QF muscles during isometric knee extensions have presented
conflicting results. For example, QF muscle activity has been reported to be both higher
(Hasler et al. 1994) and lower (Brownstein et al. 1985; Eloranta 1989; Pincivero et al. 2004;
Watanabe & Akima 2011a; Saito & Akima 2013) towards full extension, while others have
reported consistent muscle activity across different knee joint angles (Hallén & Lindahl 1967;
Lieb & Perry 1971; Salzman et al. 1993; Zabik & Dawson 1996). Regarding comparison of
EMG activity between the muscles comprising the QF muscle group, some previous studies
have reported no differences (Salzman et al. 1993), while others have reported significant
differences in normalized values during an isometric knee extension task (Pincivero et al.
2004; Watanabe & Akima 2011a; Saito & Akima 2013).
A majority of these previous studies have registered the muscle activity using surface
electrodes (Hallén & Lindahl 1967; Brownstein et al. 1985; Eloranta 1989; Hasler et al. 1994;
Zabik & Dawson 1996; Pincivero et al. 2004; Watanabe & Akima 2011a; Saito & Akima
2013). Active muscle fibers generate action currents that spread throughout the extracellular
fluid and surrounding tissue. This is termed volume conduction, and allows registration of
muscle activity at some distance from the source. Therefore, volume conduction is
fundamental for registration of the EMG activity with surface electrodes. (De Luca & Merletti
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1988; Kamen & Gabriel 2010, p. 23) An important aspect is that the EMG signal registered
with surface electrodes can be considered to reflect a summation of volume conducted action
currents from several simultaneously active motor units (De Luca & Merletti 1988). Due to
volume conduction, EMG signals detected with surface electrodes is often contaminated with
electrical activity originating from adjacent or deeper muscles other than the muscle of
interest. This is referred to as “crosstalk”, and can lead to misinterpretation of the signal
information (De Luca & Merletti 1988; De Luca 1997; Türker 1993).
The presence and amount of crosstalk in surface EMG recordings has been evaluated in
several previous studies, including muscles in the lower leg (Perry, Easterday & Antonelli
1981; De Luca & Merletti 1988; De Luca, Kuznetsov, Gilmore & Roy 2012), hamstrings
(Koh & Grabiner 1992), and the QF muscle group (Farina, Merletti, Indino, Nazzaro & Pozzo
2002; Byrne, Lyons, Donnelly, O'Keeffe, Hermens & Nene 2005; Barr, Miller & Chapin
2010; Beck, DeFreitas & Stock 2010;Wong, Straub & Powers 2013).
De Luca and Merletti (1988) electrically stimulated the tibialis anterior muscle in human
subjects and found that up to 16.6% and 8.4% of the tibialis anterior EMG amplitude could be
recorded from surface electrodes placed above the peroneus brevis muscle and soleus muscle,
respectively. De Luca et al. (2012) later reported on up to 49% crosstalk contamination when
recording EMG activity from the tibialis anterior muscle during voluntary isometric
contractions. Koh & Grabiner (1992) have displayed crosstalk in surface EMG recordings
from both the lateral and medial hamstrings when electrically stimulating the nerve of the
quadriceps muscle.
In previous studies investigating the relationship between knee joint angle and the activation
of individual QF muscles during isometric knee extensions, the inter-electrode distance
between the surface electrodes has varied between around 10 mm (Brownstein et al. 1985;
Watanabe & Akima 2011a; Saito & Akima 2013), 20mm (Pincivero et al. 2004), 30 mm
(Hasler et al. 1994), and 50 mm (Eloranta 1989). The amount of crosstalk between RF, VL,
and VM has been shown to be on average 17.8 % when using surface electrodes with an interelectrode distance of 10 mm (Farina et al. 2002). Further, DeLuca et al. (2012) displayed that
crosstalk amplitudes increase more than that of the target muscle when inter-electrode
distance is increased. Byrne et al. (2005) and Barr et al. (2010) have both concluded that
accurate measures of RF muscle activity are not possible when using surface electrodes due to
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crosstalk from the vasti muscles. It has also been suggested that EMG recordings from VM
can be susceptible to crosstalk from the adductor magnus muscle when using surface
electrodes (Wong et al. 2013).
When using EMG, muscle activity is primarily detected within an area close to where the
electrodes are placed. In dynamic contractions, or when performing several isometric
contractions at different joint angles, the muscle length will change. However, the surface
electrodes will remain in the same position since they are attached to the skin. Consequently,
as muscle length changes the relative position between active muscle fibers and the surface
electrodes will also change. Alterations in the distance between active fibers and the surface
electrodes will in turn lead to changes in EMG signal amplitude. (De Luca 1997) This
methodological problem is not a factor when using fine-wire electrodes, since they are lodged
between muscle fibers and move within the muscle without external indications (Basmajian &
De Luca 1985, p. 30-45).
When using intramuscular electrodes, recorded motor unit potentials are also usually free
from volume conduction (Türker 1993). Therefore, intramuscular EMG is considered to be far
less susceptible to crosstalk (De Luca 1997), and it has been stated that fine-wire electrodes
are suitable when recording EMG activity from a single muscle selectively (Onishi, Yagi,
Akasaka, Momose, Ihashi & Handa 2000). Several previous studies have used intramuscular
EMG as a reference to validate the use of surface electrodes for selectively measuring the
activity of individual QF muscles (Byrne et al. 2005; Barr et al. 2010; Watanabe & Akima
2011a; Watanabe & Akima 2011b; Wong et al. 2013). Further, intramuscular EMG using
fine-wire electrodes has been used to successfully investigate the relationship between knee
joint angle and EMG-activity in the hamstrings muscles during isometric contractions
(Mohamed, Perry & Hislop 2002; Onishi, Yagi, Oyama, Akasaka, Ihashi & Handa 2002).
Lieb & Perry (1971) were amongst the first to attempt to measure muscle activity across
different knee joint angles in all four of the quadriceps muscles using fine-wire electrodes.
However, action potential frequency was used as a measure of muscle activity, and the
amplitude values were not considered. Further, the inter-electrode distances were not
controlled, which in turn led to large variations in EMG values among subjects. As a result,
group values were not analyzed. (Lieb & Perry 1971) Salzman et al. (1993) successfully
measured muscle activity in all four QF muscles using fine-wire electrodes. However,
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subjects only performed isometric knee extensions at 15º and 60º of knee flexion in
combination with different hip joint angle settings. (Salzman et al. 1993)
1.3 Sport science relevance
In many sports related movements, like pushing or pulling, the QF highly contributes to the
total force production. In jumping or running activities the QF plays an important role
assisting in extending at the knee joint (Blazevich, Gill & Zhou 2006), and previous studies
have shown high QF muscle activity in other sports related tasks like jump landing (Ebben,
Fauth, Petushek, Garceau, Hsu, Lutsch & Feldmann 2010) and side-step cutting (Ebben et al.
2010; Hanson, Padua, Troy Blackburn, Prentice & Hirth 2008).
The QF muscles are often mentioned in different rehabilitation contexts. Around 20 percent of
all acute sports related injuries in soccer and ice-hockey are located in the knee (Kujala,
Taimela, Antti-Poika, Orava, Tuominen & Myllynen 1995). Anterior cruciate ligament (ACL)
injuries have been estimated to occur up to 250,000 times every year in the United States
(Failla, Arundale, Logerstedt & Snyder-Mackler 2015). Based on data from the National
Swedish Patient Register between 2001 and 2009, overall incidence of cruciate ligament
injury in Sweden was calculated to be 78 per 100,000 persons. For men aged 21 to 30 years,
the incidence was almost three times higher than average at 225 per 100,000 persons.
(Nordenvall, Bahmanyar, Adami, Stenros, Wredmark & Felländer-Tsai 2012) After an ACL
injury, muscle atrophy in the lower leg muscles can be seen. The QF muscles are especially
affected, and within the QF primarily the VM. It has therefore been suggested that exercises
should be performed to selectively target VM in order to reduce this imbalance. (Gerber,
Hoppeler, Claassen, Robotti, Zehnder & Jakob 1985)
Early cadaver studies by Lieb and Perry (1968) presented results suggesting that the VM
should be considered as two separate muscles, with separate innervation, and divided by a
fascial plane. The distal portion had a more horizontal fiber alignment and was therefore
termed it as the vastus medialis obliquus (VMO), whereas the proximal portion was regarded
as the vastus medialis longus (VML). They argued that VMO activation counters the lateral
patellar displacement that occurs due to forces produced by the VL, thus maintaining patellar
alignment. (Lieb & Perry 1968) Others have suggested that variations in the ratio between
VMO and VL strength may be associated with patellar instability (Farahmand, Senavongse &
Amis 1998). It has also been implied that an imbalance between the VMO and VL muscles
6
may be an aetiological factor in the development of patellofemoral pain syndrome (Smith,
Bowyer, Dixon, Stephenson, Chester & Donell 2009a). However, recent studies have shown
little evidence to support the observation of a fascial plane, and the division of the VM into
two separate portions has been highly debated (Smith, Nichols, Harle & Donell 2009b).
In summary, there is still uncertainty concerning the coordination of the muscles comprising
the QF muscle group. To our knowledge, no previous studies have fully investigated the
EMG-knee joint angle relationship for all four of the QF muscles (RF, VL, VM, and VI)
simultaneously using intramuscular EMG. A better understanding of how these muscles
interact at different knee joint angles may facilitate the design and optimization of various
strength training programs, used for example in rehabilitation after sports related knee injuries
or for sport performance enhancing purposes.
1.4 Aim
The purpose of the present study was to investigate the electromyography (EMG)-knee joint
angle relationship and the differences in activity among the four quadriceps femoris muscles
during maximal voluntary isometric knee extensions.
Research questions:
1. What effect does knee joint angle have on EMG-activity of each of the four quadriceps
femoris muscles?
2. Does the modulation in EMG-activity between knee joint angles differ between the four
quadriceps muscles?
2 Materials and methods
This study was part of a larger project that included simultaneous fine-wire EMG registration
of the four QF muscles (RF, VL, VM, and VI) and the four hamstrings muscles
(semitendinosus, semimembranosus, biceps femoris caput longum, and biceps femoris caput
brevis) during isometric and dynamic knee extension, isometric and dynamic knee flexion,
and stationary cycling. The present study only included fine-wire EMG registration of the
four quadriceps muscles during isometric knee extension.
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2.1 Subjects
Ten healthy male volunteers (mean ± 1standard deviation (SD) age 33 ± 11 years, height 1.83
± 0.07 m, body mass 79 ± 4.7 kg) were recruited for this study. Five of the subjects were nonelite triathletes, recruited through project advertisement at different triathlete federation
internet-based forums. The other five subjects, three non-elite cyclists and two well-trained
students from a physical education program, were recruited using convenience sampling. All
subjects met the inclusion criteria which were: male between 18-50 years of age, performing
different types of high level physical activities in which one of these was cycling, having no
history of severe knee injury (e.g. cruciate ligament damage), nor experiencing ongoing knee
pain or functional knee joint problems.
The inclusion criteria were based on previous studies that have shown pain-induced reduction
in agonist and antagonist muscle activity, especially at higher intensity contractions (Bank,
Peper, Marinus, Beek & van Hilten 2013). Further, it is also known that knee joint injuries
can lead to long-lasting inability to fully activate the quadriceps muscle, a process termed
arthrogenic muscle inhibition (Rice & McNair 2010). It has been reported that there are
significant sex differences in quadriceps and hamstring muscle control strategies (Krishnan,
Huston, Amendola & Williams 2008), and QF muscle activation during knee extensions
(Krishnan & Williams 2009). Several previous studies that were considered of special interest
to compare to our results have included male subjects only (Watanabe & Akima 2011a;
Akima & Saito 2013; Saito & Akima 2013; Saito, Watanabe & Akima 2013). Therefore, only
male subjects were included in the present study.
2.2 Fine-wire electrode preparation
Quad polytetrafluoroethylene coated multistand wires (seven silver wires coated with four
layers of Teflon-insulation) with a diameter of approximately 0.25 mm were used to record
myoelectric activity from all muscles. Electrode preparation included carefully manually
scraping off 2 mm of the insulation at the tip of the wire with a scalpel, thus exposing the
silver wires. The wire was thread through a needle (0.8 mm diameter) and the silver wires at
the tip were hooked onto the needle. Insertion of the wire was made via the hub of the needle
to reduce the risk of insulation scarring by the sharp tip of the needle. Around 5 mm of the
insulation was then scraped off at the other end of the wire. Finally, all electrodes, including
the needle, were sterilized using an autoclave.
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2.3 Electromyographic recordings
EMG was recorded unilaterally on the right thigh in all subjects. Two fine-wire electrodes
where percutaneously inserted into each of the following muscles: rectus femoris, vastus
lateralis, vastus medialis, vastus intermedius, semitendinosus, semimembranosus, biceps
femoris caput longum, and biceps femoris caput brevis. Approximate insertion sites for the
QF muscles are shown in Figure 1.
Insertions were made by an experienced radiologist under guidance of real-time highresolution ultrasound. This allowed visualization of the individual QF muscle boundaries and
the shaft and tip of the needle (Figure 2), thereby ensuring correct electrode placement and an
inter-electrode distance close to 5 mm. Ultrasound has been used in several previous studies
to guide intramuscular electrode insertion into deep muscles like the diaphragm (Hodges &
Gandevia 2000), posterior fibers of gluteus medius (Hodges, Kippers & Richardson 1997),
psoas (Andersson, Oddsson, Grundström, Nilsson & Thorstensson 1996; Andersson, Nilsson,
Ma & Thorstensson 1997), quadratus lumborum (Andersson et al. 1997), and transversus
abdominis (Eriksson Crommert, Ekblom & Thorstensson 2014). All subjects in the present
study were offered, but declined, the use of hypodermic local anesthesia during insertion.
Prior to needle insertion the skin area around the insertion site was cleaned using
chlorhexidine–alcohol.
Figure 1 Approximate insertion sites for the
fine-wire electrodes. Rectus femoris (RF) and
vastus lateralis (VL) electrodes were inserted 20
cm proximal to the knee joint axis. Vastus
intermedius (VI) electrodes were inserted
through the RF muscle, 20 cm proximal to the
knee joint axis, and laterally to the RF electrodes.
Vastus medialis (VM) electrodes were inserted
into the middle of the distal portion of the visible
muscle belly. Original image from Feneis and
Dauber (2006, p. 123).
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Figure 2 Screenshots from the ultrasound during electrode insertion. The tips of the electrodes are marked with a white (+),
showing inter-electrode distance in (from left to right): rectus femoris, vastus lateralis, vastus medialis, and vastus
intermedius.
Once the electrodes were confirmed to be in the correct location the needle was withdrawn.
This step was done with caution and under thorough inspection, to ensure that the wire was
not pulled out along with the needle. To verify that this had not occurred, the electrode
placement was checked immediately afterwards using ultrasound. In order to avoid accidental
electrode dislodgement, the wires were taped to the skin with a loop at the skin entrance. The
knee joint was then passively moved through the whole range of motion, followed by a series
of voluntary contractions with gradual increase in force to reduce the risk of electrode
migration (De Luca 2006).
A single surface reference electrode (Blue Sensor M, Ambu A/S, Denmark) was placed over
the proximal head of the fibula. Prior to placement, the skin area was shaved, abraded with
emery cloth, and then scrubbed with 70% isopropyl alcohol. The fine-wire electrodes were
hooked on to a customized cable (a hook clip cable soldered to a nickel-plated brass stud) and
then connected to an electromyographic system (MyoSystem 1400A, Noraxon Inc., USA).
The EMG signals were differentially preamplified (500 times), sampled at 5 kHz for each
muscle using a 16-bit analogue-to-digital converter (Micro 1401-3 with ADC12 3001-3 and
Spike2 Expansion 3001-9, CED, Cambridge, UK). Signals were acquired together with torque
measures from the dynamometer using the Spike2 (v. 7.09a) software (CED, Cambridge, UK)
and then stored on a computer disk for subsequent analysis.
2.3 Experimental protocol
All subjects first completed a 5-minute warm-up consisting of submaximal cycling on a cycle
ergometer. Cycling cadence and resistance was self-selected by each subject, under
10
instructions that the intention was to achieve an adequate warm-up without inducing any
significant muscle fatigue.
Isometric knee extension torque was measured using an isokinetic dynamometer (Isomed
2000, D&R Ferstl Gmbh, Henau, Germany). High test-retest reliability has been reported
when testing maximal torque during isometric knee extensions in male sports students (ICC >
0.90) (Zech, Witte & Pfeifer 2008). Subjects were seated in an upright position with their
back supported at approximately 90º of hip flexion. The knee joint flexion-extension axis was
aligned with the rotational axis of the dynamometer. Straps for the torso, waist, and distal
shank were used to secure a stable position. A gravity correction procedure was performed for
each subject using Isomed 2000 built-in software prior to any measurements, thus accounting
for the torque created by the weight of the dynamometer lever arm and subjects lower leg.
This was done with the subject seated in the dynamometer with the leg strapped to the lever
arm. Visual inspection of the EMG-signals was used to ensure that subjects relaxed, while the
dynamometer passively performed knee joint flexion-extension movement through the full
range of motion (between 90º and 15º of knee flexion).
All subjects performed maximal isometric knee extensions at 90º, 65º, 40º, and 15º of knee
flexion. The order in which repetitions at the different knee joint angle was performed was
randomized for each subject. At each knee joint angle, and in accordance with the
recommendations put forward by De Luca (1997), all subjects performed a total of three
three-second contractions with a two-minute rest interval. For all contractions, subjects were
asked to relax and then on the count of three exert maximal force with a maximal rate of force
development. Verbal encouragement was used during all contractions. To minimize the risk
of accidentally pulling out any wire electrodes during the knee extensions task, subjects were
required to fold their arms across the chest and grab the straps at the opposite shoulder.
2.4 Data analysis
Torque measures and EMG signals were analyzed using Spike2 (v. 7.09a) software (CDE,
Cambridge, UK). During the sustained phase of each maximal voluntary contraction (MVC),
mean torque values were calculated for a period of one second. The MVC that produced the
highest mean torque value for each knee joint angle (90º, 65º, 40º and 15º), respectively, was
selected for further EMG analysis. EMG signals were digitally bandpass-filtered between 10
and 1000 Hz to eliminate any movement artifacts. As a measure of signal amplitude, root11
mean-square (RMS) was calculated (De Luca 1997) during a sustained phase of one second
for all selected MVCs. Due to technical problems, one subject performed an additional
maximal isometric knee extension at each of the four different knee joint angles prior to
completing the test protocol. For this subject, RMS and torque values from the additional
MVCs were used in the statistical analysis.
For each subject, the inter-electrode distance can somewhat differ between the individual QF
muscles. Variations in inter-electrode distance will in turn affect signal amplitudes (Kamen &
Gabriel 2010, p. 67). Therefore, in order to compare the level of activity between the
individual muscles, all RMS values need to be normalized. The normalization process
involves dividing all RMS values of a muscle by the RMS value of the same muscle during a
reference contraction. Hence, instead of presenting the level of muscle activity with the RMS
value (mV), it is expressed as a percentage of the reference value. This allows more accurate
comparisons between muscles. (Burden 2010) For each subject, RMS values at knee joint
angles of 65º, 40º, and 15º were therefore normalized to the RMS values at 90º.
2.5 Statistics
Statistical analyses were performed using Statistica (v. 12.0) software (Statsoft Inc., USA). A
separate repeated measures analysis of variance (ANOVA) was performed for the RMS
values of each muscle and the knee extension torque values to detect differences between
knee joint angles. A two-way (muscle x knee joint angle) repeated measures ANOVA of
normalized RMS values were applied for detecting differences in normalized RMS values
between muscles at different knee joint angles. When a significant main effect or interaction
was found, post hoc analyses (Tukey’s honestly significant difference method) were applied.
Mauchly’s test of sphericity was used to evaluate whether the sphericity assumption had been
violated. In that case, to control for Type 1 error risk, the Greenhouse-Geisser correction
factor was used (Field 2005, p. 431). The level of significance was set at P < 0.05 and a
tendency was presented if 0.1 > P > 0.05.
2.5 Ethical considerations
All medical research involving human subjects, including the present study, should adopt the
ethical principles put forward by the World Medical Association (2013). In order to be able to
ensure the health of the subjects all electrode insertions where made by an experienced
radiologist under guidance of high-resolution ultrasound. To reduce pain and discomfort
12
during the electrode insertion, all subjects were offered hypodermic local anesthesia. In order
to minimize the risk of infections from skin penetration, all electrodes and needles where
thoroughly sterilized using an autoclave, the radiologist wore latex surgical gloves and
subjects’ skin was cleaned using chlorhexidine–alcohol. Electrode insertion may result in skin
bleeding. This could be suppressed by pressure from sterile gauze and would most likely lead
to no more than light bruising and subject discomfort. All experimental protocols were
conducted under the supervision of a medical doctor with several published studies involving
intramuscular EMG.
Before any participation all subjects were adequately informed of the aims, methods,
researcher affiliations, anticipated benefits of the study and the potential risks or discomforts
participation could entail. Subjects were also informed that participation was voluntary and
that they had the right to withdraw their consent to participate at any time without reprisal. All
subjects were insured under the Swedish Patient Injury Act. To protect subject privacy and
the confidentiality of their personal information, all subjects were given a code number used
during the data collection and analysis. The code list that linked data to participants’ identities
were held by a research staff member and stored in a locked secure location. All subjects
where asked if they would like to be informed about the general outcome and results of the
study. When seeking informed consent for participation in research studied it is important to
assess if the subjects are in a potential dependent relationship with the researcher (World
Medical Association 2013). Two of the subjects have had a student-teacher-relationship with
the researchers. During the study, none of them had an ongoing course where this relationship
was present.
We concluded that the importance of the objective, presented in “1.3 Sport science
relevance”, outweighed the risks and burdens to the research subjects. Before participation all
subjects filled out a health declaration questionnaire (Appendix 2) and signed a written form
of consent (Appendix 3). The experimental procedures were approved by the regional ethics
committee at Karolinska Institute, Stockholm, Sweden (No 2014/641-31/1).
3 Results
The repeated measure ANOVA showed a tendency for a difference in RMS values between
knee joint angles for the VM (Fdf,error=2.853,27, p=0.056) but not for the RF (Fdf,error=1.073,27),
VL (Fdf,error=1.473,27), or VI (Fdf,error=2.023,27). Post hoc analysis revealed that VM was
13
significantly more active at a knee joint angle of 90º compared to 40º (P < 0.05). Normalized
RMS values for all muscles at the four different knee joint angles are presented in figure 3.
Although RF, VL, and VI did not significantly differ between knee joint angles, they all
showed the highest mean activation at the most extended position (15º of knee flexion),
whereas VM had its highest mean activation at the most flexed position (90º of knee flexion).
Figure 3 Normalized RMS values for: (A) rectus femoris, (B) vastus lateralis, (C) vastus medialis, and (D) vastus
intermedius at the four different knee joint angles. Values are means and standard deviations. Note that there are no standard
deviations at 90º since all data were normalized to this value. Also note that the Y-axis scale differs between figures A, B, C
and D.
The 2way ANOVA of the normalized RMS values showed a main effect of muscle
(Fdf,error=6.093,27) but no interaction between muscle and angle (Fdf,error=1.246,54). Since all
RMS values were normalized to the corresponding value at 90º, this indicates that there was a
significant difference between the four QF muscles in how they change their activation from
90º to the three more extended positions (65º, 40º, and 15º knee flexion) (P < 0.05). Post hoc
analysis showed that normalized RMS values for VM was significantly lower than that of the
RF (P < 0.01) and VL (P < 0.05), respectively (Figure 4).
14
For torque values, Mauchly´s test indicated that the assumption of sphericity had been
violated (P < 0.05); therefore, degrees of freedom were corrected using Greenhouse-Geisser
estimates of sphericity (Ɛ = 0.556). The results showed that knee extension torque was
significantly affected by knee joint angle (Fdf,error=66.663,27, P < 0.001). Post hoc analysis
revealed that knee extension torque was significantly lower at 15º of knee flexion compared
40º, 65º, and 90º, respectively (P < 0.001), and significantly lower at 40º of knee flexion
compared to 65º and 90º, respectively (P < 0.001) (Figure 5).
Figure 4 Comparison of normalized RMS values between
RF, VL, VM, and VI. Values are summed means and
standard deviations for each muscle at the three most
extended positions (15º, 40º, and 65º) normalized to 90º. *P
< 0.05 vs the VL muscle; **P < 0.01 vs the RF muscle.
Figure 5 Torque values during isometric contractions at the
four different knee joint angles. *P < 0.001 vs knee joint
angle of 90º, 65º and 40º; #P < 0.001 vs 90º and 65º.
4 Discussion
One of the main findings in the present study was that VM muscle activity was highest at the
most flexed knee joint angle (90º of knee flexion), and that there was an overall decrease in
VM muscle activity as the knee got more extended with a significantly lower RMS values at
40º compared to that of 90º. This result was similar to those of previous studies using surface
electrodes to investigate the EMG-knee joint angle relationship of the superficial QF muscles
during maximal isometric knee extensions (Brownstein et al. 1985; Eloranta 1989; Pincivero
et al. 2004).
Pincivero et al. (2004) observed the lowest VM muscle activity at the most extended position
and an increasing pattern of muscle activity as knee flexion angle increased. Eloranta (1989)
observed a similar pattern for VM muscle activity, with peak EMG values occurring at the
most flexed position. However, contrary to the results in our study, Eloranta (1989) also
15
displayed similar patterns of decreasing activity for the RF and VL muscles, respectively,
towards full extension. When Byrne et al. (2005) and Barr et al. (2010) showed that surface
electrode EMG recordings of the RF are contaminated with crosstalk from the vasti muscles,
an inter-electrode distance of 17 mm and 22 mm, respectively, was used. Since crosstalk
contamination has been reported to increase along with increasing inter-electrode distances
(DeLuca et al. 2012), it is notable that an inter-electrode distance of 50 mm was used by
Eloranta (1989). Brownstein et al. (1985) reported significant variations in both VMO and
VML activity depending on knee joint angle, displaying higher muscle activity at more flexed
knee joint angles (50-90º compared to 10-40º of knee flexion). No significant differences
could be seen for any of the other QF muscles investigated (RF and VL). Though, when
analyzing the results for male subjects separately, no significant differences between knee
joint angle settings were found for either VMO or VML. This could be due to the relatively
small number of subjects, which in total were four male and seven female.
Contrary to Brownstein et al. (1985), VMO and VML muscle activity was not studied
separately in the present study. When Smith et al. (2009b) conducted a systematic review of
human subject papers investigating VM muscle fiber orientation, VM innervation, or the
presence of a facial plane, their conclusion was that there is insufficient evidence to state
whether the VM should be considered as two separate muscles. Seventeen of the reviewed
studies indicated that the distal portion (i.e. VMO) displayed a more horizontal muscle fiber
alignment compared to the proximal portion (i.e. VML), with a mean difference of 28º.
However, in a total of nine studies that had investigated the presence of a facial plane dividing
the VM into two separate portions, a distinct fascial plane was only observed in 160 subjects
of 731 cadavers. Regarding the number of nerve branches innervating the VM, a total of
eleven studies presented conflicting results. Out of 329 knees studied, 135 demonstrated VM
innervation from two separate nerve branches that both originated from the femoral nerve,
whereas the other 194 displayed VM innervation from a single nerve branch. (Smith et al.
2009b) Due to the horizontal alignment of the VMO, it has often been suggested that this
portion is important for maintaining patellar stability. However, the muscle fiber orientation
of the VMO has been shown to vary depending on the knee joint angle, displaying a more
efficient alignment to restrict lateral displacement in more flexed knee joint angles. (Andrish
2004) This is notable, since it has been reported that lateral displacement of the patella is
mainly prevented by the trochlear groove at knee joint angles greater than 30º of flexion
(Heegaard, Leyvraz, van Kampen, Rakotomanana, Rubin & Blankevoort 1994). Further,
16
Balcarek, Oberthür, Frosch, Schüttrumpf and Stürmer (2014) reported no significant
differences in morphological parameters of the VMO between patients with primary or
recurrent lateral patellar dislocation and asymptomatic subjects. And when Salzman et al.
(1993) studied the relative contribution of the individual QF muscles during maximal
isometric knee extensions using fine-wire EMG, no significant differences between VMO and
VML activity were found regardless of knee joint angle setting (15º or 60º of knee flexion).
In contrast to the results in the present study, Hallén and Lindahl (1967) found VM muscle
activity to be similar at joint angles between 90º of knee flexion and full extension during
maximal isometric knee extensions. Due to the insufficient description of the methodological
procedures used by Hallén and Lindahl (1967), it is difficult to speculate as to why their
results differ from that of the present study. Zabik and Dawson (1996) also found VM muscle
activity to be constant at different knee joint angles. These conflicting results could be due to
that peak EMG during contractions was used as a measure of muscle activity, instead of the
RMS value during a sustained phase of muscle contraction. The latter has been recommended
by De Luca (1997) when describing signal amplitudes during voluntary contractions, since it
represents signal power. Salzman et al. (1993) also presented conflicting results to that of the
present study, reporting constant QF muscle activity at different knee joint angles. However,
they compared the summed mean EMG activity of all of the individual QF muscles at
different knee joint angles, instead of analyzing each individual muscle separately.
Contrary to the results in the present study, Hasler et al. (1994) reported VM muscle activity
to be higher at the more extended position. In fact, all tested muscles (RF, VL and VM)
displayed significantly higher EMG values at knee joint angles of 170º compared to that of
130º (180º being full extension). However, the order in which the different knee joint angles
were tested was not randomized. All subjects performed six maximal isometric knee
extensions at each of three different knee joint angles tested (90º, 130º, and 170º), and
contractions at 170º was always performed last. It is well known that active movement
increases muscle temperature, which in turn has been shown to improve the transmission
speed of impulses in the central nervous system (see review, Bishop 2003a; 2003b). Further,
maximal or near-maximal voluntary contractions can lead to performance enhancing
mechanisms in subsequent activity, termed post activation potentiation (PAP). Among others,
the mechanism of PAP is suggested to be an elevation of potential transmittance across
synaptic junctions at the spinal cord, therefore resulting in increased post-synaptic potentials,
17
even though the pre-synaptic potential during subsequent activity is the same. It is also
suggested that the NA+-K+ pump activity at the muscle fibers increases as a result of prior
muscle activity. (Tillin & Bishop 2009) Therefore, the high EMG values observed by Hasler
et al. (1994) in the most extended position could be due to possible warm-up or PAP related
mechanisms following the initial contractions, or as a result of subject familiarization with the
experimental task.
Another main finding in the present study was that there were significant differences between
the QF muscles changing their activity from 90º to the more extended positions, with
significantly lower normalized RMS values for VM compared to that of the RF and VL,
respectively. This is similar to the results presented by Pincivero et al. (2004), who found
muscle activity of the VM to increase significantly more compared to that of the VL as knee
joint flexion angles increased. Further, when collapsed across knee joint angles tested (10º,
30º, 50º, 70º, and 90º of knee flexion); muscle activity of the VM was significantly higher
than that of the RF and VL muscles, respectively (Pincivero et al. 2004). Salzman et al.
(1993) also reported similar results to that of the present study, displaying no significant
differences in normalized fine-wire EMG between the RF, VL, and VI muscles. However, in
contrast to the results in the present study, Salzman et al. (1993) found no significant
differences in normalized fine-wire EMG between VM and any of the other QF muscles. This
could be due to subjects only performing maximal isometric knee extensions at 15º and 60º of
knee flexion, and therefore not testing higher knee flexion angles (e.g. 90º). In the present
study, RMS values from the individual QF muscles obtained at each knee joint angle was
normalized to the corresponding values at 90º of knee flexion. Therefore, it could be possible
that similar results for the VM, as presented in the present study, would have been observed
by Salzman et al. (1993) if higher knee flexion angles had been included in their test protocol.
Since the VI muscle is mainly located deep inside the QF muscle group, it is difficult to
measure its EMG activity without using indwelling electrodes. This is the most probable
explanation as to why a majority of the previous studies investigating QF muscle activity
using surface EMG have excluded VI (Hallén & Lindahl 1967; Brownstein et al. 1985;
Eloranta 1989; Hasler et al. 1994; Zabik & Dawson 1996; Pincivero et al. 2004). However,
Watanabe & Akima (2009a) recently presented a technique using surface electrodes in VI
EMG recordings. Via magnetic resonance imaging (MRI), they displayed that VI has a
superficial region at the distal lateral side of the thigh. Hence, by placing surface electrodes
18
over this region they state that EMG activity from the VI can be selectively registered.
(Watanabe & Akima 2009a) This technique has later been used in several studies, conducted
by the same group of researchers, to measure EMG activity of the VI during a knee extension
task (Watanabe & Akima 2009b; Watanabe & Akima 2010; Watanabe & Akima 2011a;
Akima, Saito, Watanabe & Kouzaki 2012; Saito Watanabe & Akima 2013; Akima & Saito
2013; Saito & Akima 2013).
Using surface EMG, Saito and Akima (2013) reported significantly lower VI muscle activity
in the more extended positions during isometric knee extensions. All subjects performed
maximal contractions, followed by submaximal contractions (20%, 40%, 60%, and 80% of
the MVC), at knee joint angles of 90º, 120º, and 150º (180º being full extension). In
submaximal contractions, VI muscle activity was significantly lower at 120º compared to 90º,
and significantly lower at 150º compared to 120º and 90º, respectively. In their report, Saito
and Akima (2013) also stated that “the EMG amplitude of the VI is smaller at knee joint angle
150 than that at 90 and 120” during the MVC, referring to figures of rectified EMG signals of
the QF muscles during the MVC at different knee joint angles. However, all RMS values
were normalized to the corresponding value obtained during the MVC at 90º. Therefore, the
RMS values from the MVCs were not included in the statistical analysis of muscle activity at
the different knee joint angles. In other words, the observed difference in VI EMG amplitude
at different knee joint angles during the MVC was not tested for statistical significance.
Saito and Akima (2013) also found significant differences in normalized EMG between VI
and the other QF muscles. During maximal isometric knee extensions at knee joint angles of
150º (180º being full extension), muscle activity of the VI was significantly lower than that of
the RF, VL, and VM, respectively (Saito & Akima 2013). Watanabe and Akima (2011) also
reported significant differences in muscle activity between the VI and the other QF muscles
during maximal isometric knee extensions. VI muscle activity was significantly lower than
that of the RF and VL, respectively, at knee joint angles of 115º, 140º, and 165º (180º being
full extension), and significantly lower to that of the VM at knee joint angles of 140º
(Watanabe & Akima 2011a). This is in contrast to the present study, where no significant
differences in muscle activity were found between VI and the other QF muscles.
As mentioned above, both these previous studies (Saito & Akima 2013; Watanabe & Akima
2011a) measured VI muscle activity using the surface electrode technique developed by
19
Watanabe and Akima (2009a). The superficial region of the VI in healthy young men is
reported to be relatively small (on average 32 x 43 mm) (Watanabe & Akima 2009a).
Therefore, misleading interpretations of the EMG signal could occur when using surface
electrodes, due to possible crosstalk contamination from adjacent muscles. In order to test
their own approach, Watanabe and Akima (2009a) investigated the presence of VL crosstalk
in VI surface EMG recordings by performing cooling of the skin above the VL for 20 minutes
using a rubber bag filled with ice cubes and water. Subjects performed maximal isometric
knee extensions at 90º of knee flexion before cooling, immediately after cooling, and after 5,
10, and 20 minutes of recovery after cooling. Surface EMG was recorded from all of the QF
muscles during the extension task. As a result of the cooling procedure, skin temperature of
the VL significantly decreased, whereas no significant changes in skin temperature were seen
for VI. EMG analysis revealed a significant reduction in median frequency immediately after
the cooling procedure and during the recovery period for the VL muscle but not for the VI
muscle. No significant changes in RMS values were displayed. (Watanabe & Akima 2009a)
However, the surface electrode for VL was placed at the midpoint between trochanter major
and the inferior edge of the patella, and skin temperatures were only measured near the
electrode sites. In other words, both the skin temperature and EMG of the VL was registered
relatively far away from the recording area of the VI electrodes. Crosstalk in surface EMG
recorded at the superficial region of the VI would most likely originate from the distal portion
of the VL, where neither skin temperature nor EMG was registered.
In a subsequent study by Watanabe and Akima (2011b), excellent correlations were displayed
between simultaneously recorded surface and needle electrode RMS values from the
superficial region of VI during isometric knee extensions. Further, RMS values recorded at
the middle portion of the VI using needle electrodes had excellent correlations with those
registered at the superficial region of the VI using surface and needle electrodes, respectively.
(Watanabe & Akima 2011b) However, subjects only performed submaximal contractions
(30% of the MVC) at 90º of knee flexion. Therefore, Watanabe and Akima (2011a)
conducted another study where submaximal isometric knee extensions (50% of the MVC)
were performed at knee joint angles of 90º, 115º, 140º, and 165º (180º being full extension).
EMG from the superficial region of the VI was registered using both surface and needle
electrodes, while VL muscle activity was registered using surface electrodes only. RMS
values at the three most extended knee joint angles were then normalized to the corresponding
value at 90º. Regardless of knee joint angle, no significant differences in normalized RMS
20
values of the VI were observed between surface and needle electrode recordings. However,
significant differences between muscles were observed. Normalized RMS values of the VI
recorded with surface electrodes were significantly lower than that of the VL at knee joint
angles of 140º and 165º. At knee joint angle of 165º, normalized RMS values of the VI
recorded with needle electrodes were also significantly lower than that of the VL.
In both previous studies comparing surface to needle electrode EMG recordings from the
superficial region of the VI (Watanabe & Akima 2011a; 2011b), subjects only performed
submaximal contractions. Previous studies have reported increasing crosstalk contamination
with force in both monopolar (Beck et al. 2010) and bipolar surface EMG recordings
(Solomonow, Baratta, Bernardi, Zhou, Lu, Zhu & Acierno 1994). Therefore, it is difficult to
assess the amount of crosstalk in surface electrode EMG recordings from the VI during
maximal contractions. In relation to this, Watanabe and Akima (2011b) stated that subjects in
their preliminary experiments had experienced pain near the needle electrodes, and that the
needle electrodes were deformed, when contractions above approximately 35-40% of the
MVC were performed. Pain originating from the skin, joint, muscle or tendon generally leads
to a reduction in EMG activity of the painful muscle (Bank et al. 2013). It is therefore notable
that Watanabe and Akima (2011) used contractions at 50% of the MVC in their other study
comparing surface with needle electrode EMG recordings of the VI.
In the present study, fine-wire electrodes were inserted into the middle anterior portion of the
VI, whereas the superficial region of the VI is situated at the distal lateral side of the thigh
(Watanabe & Akima 2009a). It has been reported that there are significant differences in fiber
length and pennation angles between the anterior and lateral portion of the VI, especially at
the distal end. This advocates the possibility of intramuscular differences in function, and that
different regions of a muscle may be activated uniquely during knee extension. (Blazevich et
al. 2006) Therefore, one could argue that the conflicting results regarding VI muscle activity
presented in previous studies (Watanabe & Akima 2011a; Saito & Akima 2013), compared to
that of the present study, could be due to differences in electrode placement. Watanabe and
Akima (2011b) found RMS values of the middle and distal portion of the VI to correlate when
using needle electrodes. However, and as mentioned above, only submaximal isometric knee
extensions at 90º of knee flexion were performed (Watanabe and Akima 2011b). Therefore,
uncertainty regarding the reliability and validity of surface electrode recordings from the
21
superficial region of the VI during maximal contractions at different knee joint angles
remains.
When registering EMG activity from the individual QF muscles during isometric knee
extensions at different knee joint angles, fine-wire electrodes have several methodological
advantages compared to surface or needle electrodes. For example, they provide the
possibility to record EMG from deeply located muscles (e.g. VI) selectively (Türker 1993; De
Luca 1997; Onishi et al. 2000), or from the RF muscle without crosstalk from the vasti
muscles (Byrne et al. 2005; Barr et al. 2010). When performing dynamic contractions or
isometric contractions at different knee joint angles, the fine-wire electrodes will move within
the muscle as the muscle length changes (Basmajian & De Luca 1985, p. 30-45). This will in
turn reduce the risk of signal amplitude alterations that can occur with surface electrodes, due
to changes in the distance between active fibers and the electrodes (De Luca 1997). Since the
cannula of the needle electrode remains inside the muscle during contractions, they are
generally more painful compared to fine-wire electrodes. This also makes them more
susceptible to movement, and therefore less suitable when dynamic contractions are
performed. (De Luca 2006; Kamen & Gabriel 2010, p. 63)
An issue when using fine-wire electrodes is ensuring that they are placed at the desired
location inside the muscle of interest, especially when it comes to deeply located muscles.
Insertion sites are often determined based on anatomical landmarks, and after electrode
insertions, correct placement is commonly confirmed by administrating a mild electrical
current through the wires, causing a visible or palpable contraction of the appropriate muscle
(Salzman et al. 1993; Onishi et al. 2002; Mohamed et al. 2002). However, neither of these are
possible for the VI muscle since it is deeply located inside the QF muscle group. In the
anatomical guide to intramuscular electrode insertions by Delagi and Perotto (1980), some of
the many pitfalls of relying on anatomical landmarks when inserting indwelling electrodes
into the QF muscles are described. For example, if the VI electrodes are placed too
superficially they will be in the RF, and if inserted too laterally, in the VL (Delagi & Perotto
1980, p. 191). Further, English and Weeks (1989) displayed crosstalk from adjacent muscle
compartments in fine-wire EMG recordings if the electrodes were placed near compartment
boundaries. Therefore, it may be important to place electrodes in the middle of the
compartment (English & Weeks 1989).
22
In the present study, electrode insertions were made under the guidance of real-time highresolution ultrasound. This allows distinct visualization of the individual muscle boundaries,
since the epimysium that surrounds the muscles is a highly reflective structure (Pillen & van
Alfen 2011). In previous studies it has been displayed that the accuracy in intramuscular
needle placement is superior when using ultrasound guidance compared to blind placement
based of superficial anatomical landmarks (Yun, Chung, Kim, So, Park, Oh & Lee 2015).
Further, if a blood vessel were to be accidentally ruptured by the needle during the insertions,
blood would flow out into the interstitial space. The electrical impedance between fine-wire
electrodes located in this pool of blood would then decrease, causing a short circuit. There is
also a risk of damaging nerves if the needles are inaccurately placed. Irritation of nerve
endings could in turn evoke spontaneous signals unrelated to the activation of muscles, which
are then registered by the electrodes. (Basmajian & De Luca 1985, p. 61) Compared to muscle
tissue, blood vessels are hypo- or anechoic, thus appearing as dark circles or dark lines in
ultrasound imaging. To further confirm the presence of arteries or veins, Doppler imaging can
be used to display blood flow. Nerves on the other hand are hyperechoic compared to muscle
tissue, which gives them a brighter appearance. (Pillen & van Alfen 2011) Therefore,
ultrasound guided electrode insertions not only ensures correct electrode placement. It also
makes it possible to stay clear of blood vessels and nerves during the insertion. This will in
turn lead to favorable technical advantages, which are described above, as well as reducing
the risk of generating subject discomfort or pain.
When Herzog et al. (1991) made theoretical estimations of force-length relationship curves
for the individual QF muscles; they found that the vasti muscles all appear to be able to
develop maximal force at 68º of knee flexion. Since the length of the RF muscle is affected
by hip joint angle, it was estimated to develop maximal force at more flexed knee joint angles
compared to the vasti muscles in seated knee extensions. Further, a summation of these
estimated force-length relationship curves appeared to be similar to those obtained
experimentally, which on average displayed the highest mean peak force at 75º of knee
flexion, and a decrease in force in further flexion or extension of the knee. (Herzog et al.
1991) This is similar to that of the present study where torque values displayed an increasing
pattern from 90º to 65º of knee flexion, followed by a decreasing pattern as the knee got more
extended. The peak torque value that was observed at 65º of knee flexion in the present study
is also similar to that of previous studies examining the relationship between torque (or force)
and knee joint angle during seated isometric knee extensions (Lindahl, Movin, Ringqvist
23
1969; Murray, Baldwin, Gardner, Sepic & Downs 1977; van Eijden, Weijs, Kouwenhoven &
Verburg 1987; Ng, Agre, Hanson, Harrington & Nagle 1994; Zabik, & Dawson 1996;
Welsch, Williams, Pollock, Graves, Foster & Fulton 1998; Becker & Awiszus 2001;
Newman, Jones & Newham 2003; Pincivero et al. 2004) (see Table 3 in Pincivero et al.
2004).
In the present study, none of the QF muscles displayed the highest activity at the knee joint
angle in which peak torque occurred (i.e. 65º of knee flexion). In fact, three of the QF muscles
(RF, VL, and VI) displayed the highest mean RMS values at the most extended position (15º
of knee flexion) where the lowest torque values were observed. This clearly shows that even
though increase in muscle force generally is associated with an increase in EMG signal
amplitude (De Luca 1997), there are several other factors that affect the resultant muscular
moment acting on a joint. For example, there might be differences in the ability to voluntarily
activate the QF muscle by means of maximal contraction between different knee joint angles.
This has been investigated in several previous studies using twitch interpolation technique
during isometric knee extensions (Becker & Awiszus 2001; Babault, Pousson, Michaut & van
Hoecke 2003; Newman, Jones & Newham 2003; Kubo, Tsunoda, Kanehisa & Fukunaga
2004). Becker and Awiszus (2001) reported that voluntary activation and torque values
display dissimilar patterns during isometric knee extensions at different knee joint angles.
Similar to that of the present study, average knee extension torque increased from 30º to 75º
of knee flexion, and then decreased in further knee flexion. However, voluntary activation of
the QF remained constant between knee joint angles of 30º to 65º of knee flexion. In further
flexion, an overall increase in voluntary activation was observed, with a maximum (90%
activation) occurring at 90º. Kubo et al. (2004) also reported voluntary activation to be
constant between knee joint angles of 40º to 60º of knee flexion. A gradual increase in
voluntary activation was observed at knee joint angles from 70º, 80º, to 90º of knee flexion,
to then remain constant in further flexion (Kubo et al. 2004). However, other studies have
presented conflicting results (Newman et al. 2003; Babault et al. 2003). Newman et al. (2003)
found no significant differences in voluntary activation of the QF between knee joint angles
(10º, 30º, 50º, 70º, 90º, and 110º of knee flexion), and Babault et al. (2003) reported
voluntary activation of the QF to be lower at higher knee flexion angles. However, the
differences in voluntary activation between knee joint angles observed by Babault et al.
(2003) were not statistically significant, and isometric knee extensions were only performed
at 35º, 55º, and 75º of knee flexion.
24
A methodological limitation of the present study to consider is the relatively low number of
subjects, which may have resulted in small differences in muscle activity going unnoticed.
Since the methodological procedures included relatively complex invasive aspects, the
number of subjects was intentionally kept low. The differences in quadriceps and hamstrings
EMG measures between sexes reported by Krishnan et al. (2008) was considered to be a
factor mainly for scope of the larger project (that the present study was a part of). Since only
male subjects were included in the present study, one can only speculate whether the observed
results can be generalized to women. However, when Krishnan and Williams (2009) reported
significant differences in QF EMG between sexes during knee extensions, it was only
observed in contractions at 10%, 20%, and 30% of peak torque. Further, Pincivero et al.
(2004) reported no significant differences between male and female subjects when
investigating QF EMG during maximal isometric knee extensions at different knee joint
angles.
4.4 Conclusion
The present study investigated the EMG-knee joint angle relationship and the differences in
activity among the four quadriceps muscles during maximal voluntary isometric knee
extensions using fine-wire electrodes. Our findings suggest that VM muscle activity is highest
at more flexed knee joint angles, and as the knee gets more extended, muscle activity of the
VM decreases and VM becomes less active than the VL and RF, respectively. No significant
differences in muscle activity between knee joint angles were observed for any of the other
QF muscles (RF, VL, and VI).
25
Acknowledgements
This project was carried out at the laboratory for biomechanics and motor control (BMC) at
the Swedish School of Sport and Health Sciences. During the project I´ve had the privilege
and pleasure of working alongside some outstanding people. I would like to express my
sincere appreciation and gratitude to the following people:
Associate professor Maria Ekblom1,2, my supervisor, for her amazing generosity and
invaluable support during this whole process, and for making the research facilities at the
BMC-laboratory available to me.
Associate professor Eva Andersson1,2, for introducing me to electromyography, and for
sharing her expertise as well as providing practical support during all the experiments.
Radiologist Helene Grundström3, for performing all the fine-wire electrode insertions, and for
letting us use the facilities and ultrasound equipment at Danderyds sjukhus.
Professor Tony Arndt1,4 and laboratory engineer Olga Tarassova1 for stimulating cooperation
and practical help throughout the experimental procedures.
The staff at the Library of the Swedish School of Sport and Health Sciences, for providing me
with the full manuscript of several relevant articles.
Martin Belak and Pål Török, for spreading information about the project thus helping with the
recruitment of subjects.
1.
2.
3.
4.
The Swedish School of Sport and Health Sciences, Stockholm, Sweden.
Department of Neuroscience, Karolinska Institute, Stockholm, Sweden.
Department of Radiology, Danderyds sjukhus, Stockholm, Sweden.
Institution CLINTEC, Karolinska Institute, Stockholm, Sweden.
26
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33
Appendix 1
Literature search
Aim:
The purpose of the present study was to investigate EMG-joint angle relationship and the
differences in activity among the four quadriceps muscles during maximal voluntary
isometric knee extensions.
Research questions:
1. What effect does knee joint angle have on EMG-activity of each of the four quadriceps
femoris muscles?
2. Does the modulation in EMG-activity between knee joint angles differ between the four
quadriceps muscles?
Search Keywords
quadriceps, “vastus lateralis”, “vastus medialis”, “vastus intermedius”, “rectus femoris”,
emg, electromyograph*, electromyogram, myoelectric, “knee extension”, “leg extension”
Database used
Pub Med
Searches that returned relevant results
Pub Med: (((quadriceps OR “vastus lateralis” OR “vastus medialis” OR “vastus
intermedius” OR “rectus femoris”)) AND (emg OR electromyograph* OR electromyogram
OR myoelectric)) AND ("knee extension" OR "leg extension")
Comments
I started off with a relatively broad search that resulted in approximately 600 hits. Articles'
relevance was first assessed by reference to its title. Second, all abstracts of the selected
articles were read in order to further evaluate their relevance. Finally, full manuscripts of the
articles´ which abstracts pertained to the research questions were ordered. The articles that
did not have an abstract available, but was considered relevant based on its title, were also
ordered in full manuscript for further evaluation. Relevant articles were also found when
reading the reference lists of the articles obtained in the literature search.
Appendix 2
Health declaration questionnaire
Appendix 3
Written form of consent