QUADRICEPS_FATIGUE_PFPS

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Electromyographic fatigue characteristics
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INTRODUCTION between the VMO and VL (Voight & Weider 1991).
Manual Therapy (2001) 6(1), 27–33
# 2001 Harcourt Publishers Ltd
doi:10.1054/math.2000.0380, available online at http://www.idealibrar
Patellofemoral pain syndrome (PFPS) is a multi-
factorial problem that consists of a myriad of
structural, biomechanical and subtle soft tissue
abnormalities. Amid such diagnostic diculties,
attempts have been made to classify the many
aetiological factors (Wilk et al. 1998). Of the soft
tissue causes of PFPS, there has been a plethora of
research into the quadriceps muscle group with a
number of studies investigating the proposed imbal-
ance in motor control between vastus medialis
oblique (VMO) and vastus lateralis (VL) and
subsequent patella malalignment during knee move-
ment (Souza & Gross 1991). Surface electromyogra-
phy (SEMG) has been used to look at the magnitude
of motor unit activity of the VMO and VL (Lieb &
Perry 1971), the ratio between the muscles (Karst &
Jewett 1993) and the timing of onset of contraction
However, these studies have produced contradictory
results leading to equivocal conclusions due to
differences in methodology, materials and large
inter-subject variation (Herrington 1998). Indeed,
some authors have stated that the argument for
neuromuscular timing of the quadriceps in PFPS is
tenuous leaving doubts as to the existence of VMO
insuciency (Powers 1998). Despite these reserva-
tions, most clinicians continue to use exercise as the
mainstay of conservative treatment for PFPS, treat-
ing quadriceps imbalance or weakness and focusing
on VMO dysfunction.
It has been proposed that electromyographic
(EMG) parameters used in previous studies on
PFPS, though popular, may be inappropriate and
has been suggested that the fatigue resistance of
the VMO relative to the VL may be a worthy yet
under investigated area of research (Kasman et al.
1998a).
Fatigue is a condition that describes the decline in
performance or work output associated with repeti-
tive or sustained activity (Mannion & Dolan 1996).
This can be measured by a failure point during
sustained contractions but there are a number of
practical disadvantages with this method (De Luca
1997). SEMG is a useful technique for non-invasive
Received 21 January 2000
Revised 12 August 2000
Accepted 5 November 2000
Michael J. Callaghan, MPhil, MCSP, Research Physiotherapist,
Christopher J. McCarthy, MCSP, MMACP, Jacqueline A.Oldham,
BSc PhD, Centre for Rehabilitation Science, Manchester Royal
Infirmary, Manchester Royal Infirmary, Oxford Road, Manchester
M13 9WL, Manchester UK.
syndrome
M. J. Callaghan, C. J. McCarthy, J. A. Oldham
Centre for Rehabilitation Science, Manchester Royal In
SUMMARY. This study compared the fatigue charac
lateralis (VL) and rectus femoris (RF) muscles. Ten he
syndrome (PFPS) performed an isometric leg press for 60
EMG. The power spectrum was analyzed and the extra
regression slope for each muscle. A repeated measures AN
the groups (P=0.592) nor the muscles (P=0.434). Ho
between the two groups with similar slopes for the RF. Th
group. The VMO:VL ratio calculated from these slopes f
was 1.78. These results may indicate unusual features in
Harcourt Publishers Ltd.
Correspondence to MJC, Tel. & Fax: +44(0) 1612766672;
E-mail: michael.callaghan@man.ac.uk
27
of the quadriceps in patellofemoral pain
rmary, Manchester, UK
eristics of the vastus medialis oblique (VMO), vastus
lthy subjects with 10 patients with patellofemoral pain
seconds at 60% MVIC with data collected using surface
cted median frequency normalised to calculate a linear
OVA revealed no significant differences, neither between
ever, the slopes for the VMO and VL were different
re was much larger variability of MF values in the PFPS
or the healthy subjects was 1.17 and for the PFPS group
the fatigue indices of the quadriceps in PFPS. # 2001
y.com on
examination of fatigue. Analysis using power spec-
trum and extraction of the median frequency has
28 Manual Therapy
become an accepted way of using EMG for monitor-
ing fatigue (Basmajian & De Luca 1987), yet there
have been few studies investigating quadriceps
fatigue. Grabiner et al. (1991), using SEMG, in-
vestigated the effects of fatiguing static and dynamic
knee extension on the VMO and VL in 10 healthy
subjects. A maximum voluntary isometric contrac-
tion (MVIC) at 30% and then 60% held at 208 of
knee flexion was maintained until exhaustion. Using
power spectrum analysis to calculate the percentage
slope coecients of the SEMG signal, the grand
means of normalized slope coecients revealed a
VMO/VL ratio of 1.0 (VMO=70.20; VL=70.2) at
60% MVIC. They concluded that there was no
preferential fatigue of the VMO relative to the VL
using the knee extension exercise. Kaljumae et al.
(1994) used SEMG to show an increase in vastii
muscle endurance with an 8% greater effect in vastus
medialis relative to VL. They also noted a concomi-
tant decrease in quadriceps strength. The only
investigation so far on PFPS patients examined 21
patients with arthroscopically diagnosed chondroma-
lacia patellae who performed 20 isokinetic dynamic
contractions over 60 seconds (Vaatainen et al. 1991).
Significant differences were found between the VMO
values for zero crossing rate (ZCR) on the affected
compared to the unaffected knees and a group of
healthy subjects. The aim of the present study was to
evaluate and compare to a healthy group, the fatigue
characteristics under isometric conditions of the
VMO, VL and RF in patients with PFPS.
METHODS
Initially, 24 patients were referred from orthopaedic
clinics with a diagnosis of patellofemoral pain. After
screening and further clinical assessment using the
criteria listed below 14 were excluded leaving 10
patients (age 31.3+6.6; BMI 25.9+4.8; duration of
symptoms 2.5 years+1.8) who were then assessed
with SEMG. Pain level at the time of assessment was
4(+1.8) using a 10 cm visual analogue scale (0¼ no
pain and 10¼worse pain ever). Ten healthy subjects
(age 29.7+5.4; BMI 23.6+3.3) constituted a con-
venience sample of the hospital and university
community. All patients and subjects had the
protocol and procedures explained to them, were
given an information sheet, and were asked to sign a
consent form if they wished to enter the study. The
study was approved by the ethics committee of the
Central Manchester NHS Healthcare Trust.
Inclusion criteria
Patients were included if they had atraumatic
peripatellar pain for greater than 6 months and not
longer than 3 years. Patients had patellofemoral pain
Manual Therapy (2001) 6(1), 27–33
provoked by one of the following alone or in
combination: prolonged sitting, deep squatting,
ascending or descending stairs (Post 1997). Patients
were also included if they had a normal radiograph,
MR scan or arthroscopy. The healthy subjects had no
present or past knee injury.
Exclusion criteria
Patients were excluded from the study if they had
epilepsy, cancer, a cardiac pacemaker, a suspected
heart problem, or if they had recent surgery (not
including arthroscopy). In order to exclude abnormal
foot and ankle pronation as the cause of PFPS the
patients were screened by kinetic gait analysis (Kistler
Bio-mechanics Ltd, Switzerland) to detect abnormal
values of mediolateral force, as described by Cal-
laghan & Baltzopoulos (1994).
Clinical examination
Patients had further clinical examination to assess
their suitability and to determine the presence of
other lower extremity dysfunction that may account
for the knee symptoms. These included referred pain
from the lumbar spine and hip joint, severe leg length
discrepancy, knee ligament, quadriceps tendon and
meniscal pathologies, Hoffa’s syndrome, medial plica
syndrome, femoral anteversion and tibial torsion.Examination was also performed to detect loss of
flexibility of the soft tissue structures such as the
quadriceps, hamstrings, triceps surae and iliotibial
band which have been associated with PFPS (Wilk
et al. 1998).
Instrumentation
Extension torque of the lower limb was measured
using the Biodex system 2 isokinetic dynamometer
(Biodex systems Inc., Shirley, NY, USA) with a
closed kinetic chain (CKC) leg press attachment as
supplied by the manufacturers. The CKC method
was chosen in preference to the standard isokinetic
lever arm (knee extension) because CKC exercise has
been advocated for patients with PFPS due to a
lessening of the patellofemoral joint reaction force
and patellofemoral stress (Steinkamp et al. 1993). A
CKC method of assessment may not only lessen
patients’ symptoms but also lead to improvement in
perceived function in patellofemoral pain syndrome
(Steine et al. 1996). Indeed, during MVIC open
kinetic chain (OKC) knee testing, Doxey and Eisen-
man (1987) commented that nearly all their patients
with PFPS complained of pain, with a corresponding
decrease in integrated EMG activity of the
quadriceps. This was due to patellofemoral stress
causing an increase in pain, which resulted in
subjects’ apprehension to produce maximum force.
# 2001 Harcourt Publishers Ltd
Electromyographic fatigue characteristics of the quadriceps in patellofemoral pain syndrome 29
Furthermore, CKC activity should be analyzed
because of the proposed integration of all joints and
segments in a CKC movement, such as lower limb
extension, which is more preferable than the isolated
motion of a OKC activity, such as seated knee
extension (Rivera 1994).
MVIC measurement
The 100% MVIC was measured with hip flexion set
at 908 and the knee angle set at 458 flexion. The knee
angle was previously determined as the most appro-
priate to reduce patellofemoral stress to a minimum
during testing (Steinkamp et al. 1993). Practice
contractions were performed prior to data collection
to familiarize the subjects with this method and to
ensure that they were able to maintain a knee angle
of 458. A twitch interpolation technique was used to
ensure a maximum voluntary quadriceps contraction
(Belanger & McComas 1981; Rutherford et al. 1986).
Subjects performed three maximum contractions of
10 sec duration with 2min rest between each con-
traction; data were collected for the maximum single
torque value (peak torque). Fifteen min rest was
allowed before the EMG fatigue protocol started
(Arendt-Neilsen & Mills 1988).
Fatigue assessment
Fatigue indices of the vastus medialis oblique
(VMO), vastus lateralis (VL), and rectus femoris
(RF) were assessed by bipolar electrode surface
electromyography (EMG). This approach simulta-
neously monitors median frequency (MF) from
multiple electrode sites during a sustained contraction
when the power density spectrum undergoes com-
pression towards the lower frequencies (Oddsson
et al. 1997). With the patient supine, the skin was
prepared by shaving and scrubbing with isopropyl
alcohol. Electrode position was determined by using
a protractor and tape measure and was marked on
the skin with a pen. Pairs of pre-gelled Ag/AgCl
electrodes (Niko Medical Product, Gloucester, UK)
were placed on the skin parallel to the alignment of
the muscle fibres with an inter-electrode distance of
50mm. These positions have been described pre-
viously (Howe 1994): VMO at 508 from the long axis
of the femur and 5 cm from the superior medial
border of the patella; VL at 12–158 from the long axis
of the femur 15 cm from the superior lateral border of
the patella; RF at the mid-point of the muscle belly,
halfway between the anterior superior iliac spine and
the superior pole of the patella. The ground electro-
des were placed locally on sites or muscles unrelated
to those being investigated (Turker 1993); specifically,
adductor longus for RF, iliotibial tract for VL and
the medial tibial condyle for VMO. For the contrac-
tion period, patients were asked to perform a 60 sec
# 2001 Harcourt Publishers Ltd
contraction at a level of 60% of their MVIC which
had already been calculated by an isometric test. The
60% level was shown to patients via a computer
generated line on the Biodex screen. Data collection
did not commence until the target was reached and
terminated at 60s after which the patient stopped
contracting.
The electrodes were connected to a TEL100M four
channel remote amplifier/transmitter system with
filtering, offset and gain controls for each channel
(Biopac Systems Inc., CA, USA). This was connected
via a cable to a TEL100D receiver module, which was
in turn connected to the MP100 acquisition unit. The
raw signal was amplified, analogue-to-digital con-
verted at a sample rate of 1024Hz and band pass
filtered at 8Hz to 500Hz. The signal gain was 5000.
On line real time analysis of the EMG signal from
each muscle was performed every second by the
LabVIEW system (National Instruments, TX, USA).
This monitored the raw EMG signal during the
contraction and was subjected to Fast Fourier
Transformation to determine the power density
spectrum and extract the median frequency. After
the test, the data was exported to Microsoft Excel
(‘97) for off line analysis of the raw signal checking
for artefacts or signal anomalies. MF was normalized
against initial median frequency and a linear regres-
sion was constructed from which was derived a slope
indicating rate of change per second using the
methods described by Basmajian & DeLuca (1987).
The normalized MF slope could also describe the rate
of change over the contraction time of 60 seconds and
used to express a fatigue rate (Roy et al. 1995). The
ambient temperature was monitored for all tests and
remained constant at 208C (Bell 1993).
Reliability
The Biodex system 2 dynamometer has been found to
be reliable using the CKC attachment (Callaghan
et al. 2000) with intraclass correlation coecients
(ICC2,1) estimates of 0.82 for healthy subjects and
0.89 for PFPS patients in the extension isometric
mode. EMG reliability was also assessed in 20
healthy subjects to assess the inter-session relability
of the MF. ICC2,1 inter-session estimates were good
for VMO (ICC2,1=0.72) and VL (ICC2,1=0.74) but
poor for RF (ICC2,1=0.33).
STATISTICAL ANALYSIS
Statistical analyses were performed using SPSS
(Statistical Package for the Social Sciences) for
Windows (v.7.5). The normalized slope coecients
of all three muscles were analysed by a repeated
measures ANOVA. This measure was also graphi-
cally represented to show the ratio of VMO to VL for
Manual Therapy (2001) 6(1), 27–33
the PFPS and healthy groups. A value of P50.05 was
considered statistically significant. The data were
analysed using a Kolomogorov–Smirnov test and
found to be normally distributed. Therefore para-
metric tests were performed.
Table 1. Grand means and VMO:VL ratios+SD for normalized slop
VMO VL
Normal 70.105+0.061 70.117+0.08
PFPS 70.140+0.196 70.079+0.07
VMO: vastus medialis oblique. VL: vastus lateralis. RF: rectus femor
30 Manual Therapy
RESULTS
A repeated measures ANOVA revealed no statisti-
cally significant differences between the fatigue slope
values per second between the three muscles
(P¼ 0.434) nor within the groups (P¼ 0.592). Table 1
shows the mean (SD) of the slope coecients for both
groups. The grand mean VMO:VL fatigue ratio for
all PFPS patients is 1.78+2.7 and for healthy
subjects is 1.17+0.73. The graphic representations
show a much wider spread of the VMO:VL fatigue
ratios in the PFPS group compared to the healthy
group (Fig. 1). Typical examples of the slopes and
lines of best fit are shown for a healthy subject
(Fig. 3) and a patient with PFPS (Fig. 2).
DISCUSSION
This study explored the differences in quadriceps
fatigue characteristics between healthy subjects and
patients withPFPS. Although quadriceps exercises
have been advocated as an important aspect of
conservative treatment, there remains considerable
debate as to whether exercises should be a generalized
strengthening programme or specifically targeted at
the VMO or VL muscles (Callaghan & Oldham
1996). SEMG has been used in many studies because
of its ability to examine each of the quadriceps
Fig. 1—VMO:VL fatigue ratios. PFPS v healthy subjects. PFPS:
patellofemoral pain syndrome patients; VMO: vastus medialis
oblique; VL: vastus lateralis.
Manual Therapy (2001) 6(1), 27–33
components during exercise. Although VMO:VL
activity ratio and onset timing have been studied by
numerous investigators, the use of SEMG in examin-
ing fatigue rates and characteristics of the quadriceps
has been a hitherto less common form of assessment.
However, if devising an exercise regime towards
improving quadriceps endurance is a more important
aspect of the biomechanical balance between the
VMO and VL than strength (Kaljumae et al. 1994),
then the use of EMG to measure fatigue character-
istics should be developed. The lack of statistical
significance between VMO and VL in the PFPS
patients (and hence between the two groups) is
probably due to the large variability in the MF
measures that is reflected in the widely spread values
for VMO and VL in the PFPS group (Fig. 1). This
large inter subject variation has been noted pre-
viously in the context of EMG and VMO:VL ratio,
and explained by VMO dominance being a ‘personal
trait’ (Cerny 1995). Moreover, unpublished work at
our centre has also noted large variability in fatigue
MF measures of the superficial quadriceps in knee
osteoarthritis. Although the sample size in this study
is comparable with others using SEMG to measure
quadriceps fatigue (Grabiner et al. 1991; Kaljumae
et al. 1994) the large variability mentioned above
coupled with the small sample size meant that any
significant differences between the groups could not
be demonstrated. Subsequent power calculations
(Elashoff 1997) based on our data revealed that a
sample size of 186 in each group would be required to
achieve 80% power in any new study. This indicates
that the results certainly have to be interpreted with
caution as power could not be achieved with this
sample size. There was good reliability in healthy
subjects for VMO and VL EMG MF, but reliability
obtained for the RF was poor. As this study was
predominantly interested in the relationships between
VMO and VL, reliability was considered good
enough to proceed, with caution being exercised
when interpreting the RF results. Fatigue resistance
of skeletal muscle is governed by Type I muscle fibres.
e coecients for VMO and VL at 60% MVIC
RF VMO:VL RATIO
5 70.086+0.129 1.17+0.73
4 70.096+0.083 1.78+2.70
is. PFPS: patellofemoral pain syndrome.
Fibre type distribution has been investigated in the
quadriceps with 42.3% of Type I for VL and 52.6%
for VM (Johnson et al. 1973). This would suggest that
fatigue would occur slightly quicker in the VL
compared to the VMO as the contraction time
progressed and as the force became more dicult to
maintain. The results from the healthy subjects in this
study support this as there is a slightly steeper fatigue
# 2001 Harcourt Publishers Ltd
Fig. 2—Typical example decline in EMG median frequency for VMO [&] and VL [^] during 60 second isometric CKC contraction. PFPS
subject. VMO: vastus medialis oblique; VL: vastus lateralis; —: line of best fit.
Electromyographic fatigue characteristics of the quadriceps in patellofemoral pain syndrome 31
slope for VL (70.117) compared with VMO
(70.105). The VMO:VL ratios from the healthy
subjects in the present study also concur with those of
Grabiner et al. (1991) in that there was virtually no
difference between the VMO and VL linear slopes at
60% of MVIC with a slightly steeper slope for VL.
Our study has found that in the context of fatigue
rates of the quadriceps, the VMO:VL relationship for
the healthy volunteers (1.17) was closer to 1.0 than
the values of patients with PFPS (1.78).
In patients with PFPS, despite there being no
statistical significance for the reasons already men-
tioned, the grand mean linear slopes for VMO were
considerably different from those for VL indicating
that the fatigue resistance of the VMO (70.140) was
lower than that of the VL (70.079). This confirms
Kasman et al’s (1998a) earlier proposal and concurs
with Vaatianen et al. (1991) who examined patients
with chondromalacia patellae and found the zero
crossing rate of the vastus medialis during dynamic
isokinetic exercise to be greater than a healthy control
Fig. 3—Typical example of decline in EMG median frequency for V
Healthy patient. VMO: vastus medialis oblique; VL: vastus lateralis;
# 2001 Harcourt Publishers Ltd
group (P50.001). This deficit in fatigue resistance
has also been found in studies on recurrent patella
dislocation in which vastus lateralis biopsies revealed
an increased proportion of Type IIc fibres and a
decrease in Type I fibres compared to a control group
(Floyd et al. 1987). The VMO:VL ratio has been a
source of debate for some time with many studies
using root mean square or integrated amplitudes to
generate a mathematical ratio. Despite a variety of
methodologies and analyses the amplitude values
seem to generate a VMO:VL ratio in healthy subjects
of nearly 1.0. There are many clinical implications
from defining such a ratio and a note of caution has
already been issued that whereas a ratio of less than
1.0 may indicate VMO:VL muscle imbalance, a ratio
of nearer to 1.0 may not necessarily rule out
quadriceps dysfunction (Kasman et al. 1998b).
The use of the CKC device in this study may
account for different values of MVIC and absolute
EMG values compared to previous work. The CKC
method in this study was chosen in preference to the
MO [&] and VL [^] during 60 second isometric CKC contraction.
—: line of best fit.
Manual Therapy (2001) 6(1), 27–33
32 Manual Therapy
standard OKC isokinetic attachment after Doxey and
Eisenman (1987) showed that nearly all their patients
with PFPS complained of pain during OKC MVIC
knee testing, with a corresponding decrease in
integrated electromyographic activity of the quad-
riceps compared to the control limb. The choice of
device for testing knee joint pathology in general and
PFPS in particular needs to be considered carefully,
especially when trying to minimise the effect of pain
inhibition on muscle function.
CONCLUSION
This study has described the fatigue ratios between
VMO and VL in normal subjects and found
differences when compared to the fatigue character-
istics of the VMO and VL of patients with PFPS. It
also found large variability in the MF values for the
PFPS group. These results did not reach statistical
significance and although they provide an interesting
insight into the fatigue characteristics of the quad-
riceps, some caution should be exercised when
considering the results. Further work is being
proposed to examine the existence of these relation-
ships with an appropriate sample size.
Acknowledgements
The participation of the healthy volunteers and patients is
acknowledged, as is the statistical advice from Dr Julie Winstanley.
This work was supported by Smith & Nephew Healthcare Ltd and
the Health Technology Assessment Agency of the UK NHS.
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Electromyographic fatigue characteristics of the quadriceps in patellofemoral pain syndrome 33
# 2001 Harcourt Publishers Ltd
 Manual Therapy (2001) 6(1), 27–33
	INTRODUCTION
	METHODS
	Inclusion criteria
	Exclusion criteria
	Clinical examination
	Instrumentation
	MVIC measurement
	Fatigue assessment
	Reliability
	STATISTICAL ANALYSIS
	Table 1
	RESULTS
	DISCUSSION
	Figure 1
	Figure 2
	Figure 3
	CONCLUSION
	Acknowledgements
	References