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Archives of Physical Medicine and Rehabilitation

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Archives of Physical Medicine and Rehabilitation 2014;95:1521-6

ORIGINAL ARTICLE

Diagnostic Accuracy of the Electromyography


Parameters Associated With Anterior Knee Pain in
the Diagnosis of Patellofemoral Pain Syndrome
Deisi Ferrari, MSc,a,b Heloyse Uliam Kuriki, PhD,a,b Cristiano Rocha Silva, MSc,c
Neri Alves, PhD,a,b Fabio Mcolis de Azevedo, PhDa
From the aPhysical Therapy Department, School of Science and Technology, University of Sao Paulo State, Presidente Prudente, SP;
b
Bioengineering Postgraduate Program, Sao Carlos School of Engineering, University of Sao Paulo, Sao Carlos, SP; and cNeuroscience Program
and Biomedical Engineering Laboratory, University of Sao Paulo, SP, Brazil.

Abstract
Objective: To assess the diagnostic accuracy of the surface electromyography (sEMG) parameters associated with referred anterior knee pain in
diagnosing patellofemoral pain syndrome (PFPS).
Design: Sensitivity and specificity analysis.
Setting: Physical rehabilitation center and laboratory of biomechanics and motor control.
Participants: Pain-free subjects (nZ29) and participants with PFPS (nZ22) selected by convenience.
Interventions: Not applicable.
Main Outcome Measure: The diagnostic accuracy was calculated for sEMG parameters reliability, precision, and ability to differentiate
participants with and without PFPS. The selected sEMG parameter associated with anterior knee pain was considered as an index test and was
compared with the reference standard for the diagnosis of PFPS. Intraclass correlation coefficient, SEM, independent t tests, sensitivity,
specificity, negative and positive likelihood ratios, and negative and positive predictive values were used for the statistical analysis.
Results: The medium-frequency band (B2) parameter was reliable (intraclass correlation coefficientZ.80e.90), precise (SEMZ2.71e3.87
normalized unit), and able to differentiate participants with and without PFPS (P<.05). The association of B2 with anterior knee pain showed
positive diagnostic accuracy values (specificity, .87; sensitivity, .70; negative likelihood ratio, .33; positive likelihood ratio, 5.63; negative predictive value, .72; and positive predictive value, .86).
Conclusions: The results provide evidence to support the use of EMG signals (B2 e frequency band of 45e96Hz) of the vastus lateralis and
vastus medialis muscles with referred anterior knee pain in the diagnosis of PFPS.
Archives of Physical Medicine and Rehabilitation 2014;95:1521-6
2014 by the American Congress of Rehabilitation Medicine

Patellofemoral pain syndrome (PFPS), described as anterior or


peripatellar pain, is one of the most common complaints in orthopedic practices and accounts for 25% to 40% of all knee
problems in sports medicine centers.1 Its reported incidence is
10% to 28% of the general population,2,3 affecting 1 in 4 of the
total population.1 The pain limits participation in sports and daily
activities because these activities, such as stair climbing, squatting, or remaining seated, intensify the pain. Up to 90% of the
individuals with this condition have recurrent or chronic pain.4
Supported by the Sao Paulo Research Foundation (grant no. 2011/04808-7).
Disclosures: None.

There is an association between PFPS and the development of


patellofemoral osteoarthritis.5,6
The early and precise diagnosis of PFPS is indicated to avoid
evolution of the disease. Although there is no criterion standard
for diagnosis, there are many accepted reference standards. In
clinical practice, many tests are used to diagnose PFPS, such as
patellar tracking, patellar apprehension, compression test, Waldron test, and patella palpation.7,8 According to 2 systematic reviews currently published, there is no consistent evidence
regarding the accuracy of these clinical tests. Both studies reported poor diagnostic accuracy of the clinical tests,7,8 and when 2
or more studies investigated the same clinical test, the diagnostic

0003-9993/14/$36 - see front matter 2014 by the American Congress of Rehabilitation Medicine
http://dx.doi.org/10.1016/j.apmr.2014.03.028

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D. Ferrari et al

accuracy values varied significantly.8 The poor outcome could be


associated with the subjectivity and wide variation in the standard
references used to determine the diagnostic accuracy of the clinical tests. It is worth noting that most studies had lower Quality
Assessment of Diagnostic Accuracy Studies scores, meaning that
the studies that analyzed the diagnostic accuracy were at a higher
risk of bias.7,8
Important findings regarding the PFPS have been observed in
biomechanical studies,9 but no studies have used biomechanics
parameters to diagnose PFPS. Among the various biomechanics
methods, surface electromyography (sEMG) parameters of the
vastus medialis (VM) and vastus lateralis (VL) muscles have been
widely studied. Alterations in the muscle activation or muscle
inhibition are reflected by changes in the spectral properties of the
electromyogram.10 A review by Lankhorst et al9 analyzed 47 articles related to factors associated with PFPS and reported 94
sEMG parameters of the VL and VM muscles. According to the
literature, individuals with PFPS present alterations in neuromuscular activity,11,12 which can be visualized using sEMG
parameters.11,13
In this context, the association between biomechanical and
clinical findings might be a new method for the problematic
diagnosis of PFPS. We believe that the sEMG parameters associated with referred anterior knee pain, with a level of at least 2cm
on a visual analog scale (VAS) and pain in functional activity,
could be used for diagnosing PFPS. The purpose of this study was
to assess the diagnostic accuracy of the sEMG parameters associated with referred anterior knee pain for diagnosing PFPS.

Methods

diagnosis of PFPS by a medical doctor; (2) anterior knee pain


during at least 2 of the following activities: remaining seated,
squatting, kneeling, running, climbing stairs, and jumping; (3)
pain during patellar palpation; (4) symptoms for at least 1 month
with an insidious start; (5) pain level up to 3cm on a 10-cm VAS in
the previous week; and (6) at least 3 positive clinical signs of the
following tests: Noble compression, McConnell, Waldron, Zohlers sign, Clarkes sign, Q angle higher than 18 , and patella
in the medial or lateral position. These criteria do not indicate
the severity of PFPS; they only classify as PFPS or not. The
participants needed to fulfill all 6 requirements to be allocated to
the PFPS group and could not present any signs or symptoms
of PFPS or other disease to be allocated to the control group
(pain-free).
Participants were excluded if they presented any condition
other than PFPS14-16: ligament tears, patellar tendon or meniscus
tears, bursitis, bilateral knee pain, osteoarthritis or chondral lesions, patellar subluxation or dislocation, presence of neurological
diseases, or inflammatory processes. The participants with knee
surgery and knee treatments such as arthroscopy, steroid injections, oral steroids, opiate treatment, or acupuncture or physiotherapy during the last 6 months were excluded from this study.
These criteria were evaluated by a medical doctor with at least 10
years of training in the orthopedic area and proven through clinical tests and, if necessary, by imaging examinations.
All the participants were screened according to the exclusion
and inclusion criteria by the same investigator and allocated to the
PFPS group or the control group. The participants underwent the
index test and were assessed by a second investigator with 6 years
of experience, who was blinded to the group assignments.

Participants

Index test

This prospective study followed the Standards for Reporting of


Diagnostic Accuracy. The study was approved by the University
Estadual Paulista Human Research Ethics Committee (process
number 16/2011).
The study involved 78 women recruited for convenience at the
Physical Rehabilitation Center of the State University of Sao
Paulo of Presidente Prudente. Before participating in the study, all
the participants were oriented regarding the purpose and nature of
the study. All the participants had to be women aged 18 to 30
years, had to sign informed consent, and had to speak Portuguese
to be included in the study.
The participants who reported knee pain during an orthopedic
consult were included in the study. All the included participants
were divided into either the PFPS group or the control group,
according to diagnostic criteria. The criteria used for the diagnosis
of PFPS were based on those used in other PFPS studies14-16: (1)

The term reference standard is defined as the best-available


method to determine the absence or presence of the condition of
interest.17 In this study, the reference standard was considered the
diagnostic criteria listed earlier. The index test, which is the test
under evaluation,17 was the association between 2 clinical criteria
and an sEMG parameter in this study. The sEMG signal was
obtained during stair climbing; sEMG parameters should be reliable, precise, and able to differentiate between participants with
PFPS and pain-free participants. The 2 clinical criteria were an
anterior knee pain level of at least 2cm on a 10-cm VAS in the last
month and anterior knee pain during at least 2 of the following
activities: remaining seated, squatting, kneeling, running, jumping, and climbing stairs.14-16 The time interval between the assessments by the reference standard and the index test was up to
1 week.

List of abbreviations:
ICC
LRL
LRD
NPV
PFPS
PPV
PSD
sEMG
VAS
VL
VM

intraclass correlation coefficient


negative likelihood ratio
positive likelihood ratio
negative predictive value
patellofemoral pain syndrome
positive predictive value
power spectrum density
surface electromyography
visual analog scale
vastus lateralis
vastus medialis

Instrumentation
The experimental design included a staircase of 7 steps, each
18cm high and 28cm deep, and a walkway in front of and behind
the staircase.
The sEMG signals were obtained using a conditioner module
(ADS1000-AC1160a) that used a fourth-order, zero-lag, band-pass
Butterworth digital filter with cutoff frequencies of 20 and 500Hz
and an amplifier with a gain of 50. The sample frequency used was
4000Hz. The preamplifier circuit on the electrode cable had a gain
of 20, a common mode rejection ratio of >80dB, and an impedance of 1012U. To collect the VM and the VL sEMG data, 2 pairs
of bipolar surface-capture Ag/AgCl electrodes (Medi-Traceb) with
diameters of 10mm were positioned on the VM and VL muscles at
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Diagnostic accuracy of electromyography in knee pain

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Table 1

Descriptive data of the sample

Variable

Control Group

PFPS Group

Age (y)
Height (m)
Weight (kg)
N

20.422.33
1.640.05
57.948.51
29

22.652.08
1.640.06
61.7910.65
22

.001*
.814
.200

NOTE. Values are mean  SD or as otherwise indicated.


* A significant difference (P<.05) between groups.

an interelectrode distance of 20mm. The positions of the electrodes were determined according to the location of the motor
point. The electrodes were positioned 2cm below the motor point
in the direction of the muscle belly.18 An electrostimulation device
(Nemesysc) was used to find the motor point. To reduce the
measurement variability that might be caused by the positions of
the electrodes, a template was developed that used the anatomic
references of the patella and the hip of the participant.
Processing data
The analyzed sEMG signals were referenced by the vertical
component of the ground reaction force measured by the force
plate in the fourth step; that is, the beginning and end values of all
the sEMG signals considered for analysis were determined in
accordance with the vertical component of the ground reaction
force measurement in the fourth step.
All the analyses were performed in MATLAB. The power
spectrum density (PSD) of the filtered sEMG time series was
calculated using the fast Fourier transform.19 The median frequency of the PSD was calculated as the frequency at which the
integral of the left side of the spectrum was equal to that of the
right side.20
The intensity of the PSD was normalized using the following
steps: (1) calculation of the spectral distribution function, which is
the cumulative sum of the power spectrum divided by its
maximum value and multiplied by 100, and (2) calculation of the
derived spectral distribution function to obtain a PSD with intensity values normalized between 0 and 100. From the normalized PSD, the mean intensity was calculated for each of the 3
frequency bands considered for analysis: low (15e45Hz), medium
(45e96Hz), and high (96e400Hz).21
Experimental protocol
For the reliability analysis, the trials were performed in the same
manner on 2 separate days, with an interval of 2 to 7 days between

Table 2

the 2 collection periods. After the electrodes were placed on the


first day, their positions were marked on a template that was used
on the second day. Before the data collection, the participants
were trained for the activity, their skin was shaved and cleaned
with alcohol, and the electrodes were placed.
Movement began with the participant in a standing position on
the walkway in front of the stairs. The participant climbed the
stairs in a continuous movement, alternating legs until she reached
the end of the walkway after climbing the stairs. The participants
completed 10 trials on each assessment day.11

Statistical analyses
The descriptive values (means  SDs) were obtained using SPSS
software version 18.d The data were analyzed for normality of
distribution using the Shapiro-Wilk W test. Independent t tests
were used to quantify the differences between the groups. For a
relative measure of reliability, the intraclass correlation coefficient
(ICC)(2, k) model was used.22 ICC values in the .00 to .25 range
indicated little, if any, reliability; the .26 to .49 range indicated
poor reliability; the .50 to .69 range indicated moderate reliability;
the .70 to .89 range indicated high reliability; and the .90 to 1.0
range indicated very high reliability.23,24 The SEM was used to
express the reliability in absolute values,22 indicating the precision
of the measurement.25 A lower SEM indicated better reliability of
the measurement.24
After calculating the reliability of the sEMG parameters, the
diagnostic accuracy was determined. The term accuracy refers to
the amount of agreement between the information from the
reference standard and that of the index test.17 To examine the
diagnostic accuracy value of the index test, the sensitivity, specificity, positive and negative predictive values (PPVs and NPVs),
and positive and negative likelihood ratios (LR and LR) were
calculated.26,27
Determination of the true positive, false positive, true negative,
and false negative by the index test followed the criteria listed in
appendix 1. To determine the cutoff of the sEMG signal for
diagnosis, several confidence intervals (70%, 80%, 90%, and
95%) of the control group were considered and the sensitivity
and specificity of each interval was calculated. The confidence
interval selected was the one that showed the best sensitivity
and specificity.

Results
From May 2011 through June 2012, 78 participants were recruited
using the inclusion criteria, and after diagnosis, 51 participants

Mean, SD, ICC, and SEM values of the sEMG frequency domain parameters in the Control Group and the PFPS Group for the VM muscle
PFPS Group

Control Group

Day 1

Day 2

Day 1

Day 2

Parameter

Mean  SD

Mean  SD

ICC

SEM

Mean  SD

Mean  SD

ICC

SEM

MF (Hz)
B1 (nu)
B2 (nu)
B3 (nu)

57.4412.42
47.84*12.13
32.90*8.42
1.761.26

55.898.14
49.8911.47
32.848.03
1.590.87

0.82
0.85
0.90
0.63

5.8
5.83
3.52
0.79

52.718.0
55.68*10.56
28.21*5.0
1.470.78

51.377.44
56.08.52
27.744.67
1.430.61

0.83
0.87
0.81
0.91

4.05
4.53
2.71
0.28

Abbreviations: B1, low-frequency band; B2, medium-frequency band; B3, high-frequency band; MF, median frequency; nu, normalized unit.
* A significant difference (P<.05) between groups only for day 1.

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Table 3

D. Ferrari et al
Mean, SD, ICC, and SEM values of the sEMG frequency domain parameters in the Control Group and the PFPS Group for the VL muscle
PFPS Group
Day 1

Control Group

Day 2

Day 1

Day 2

Parameter

Mean  SD

Mean  SD

ICC

SEM

Mean  SD

Mean  SD

ICC

SEM

MF (Hz)
B1 (nu)
B2 (nu)
B3 (nu)

56.7712.95
48.1811.18
31.90*7.28
1.811.34

56.1210.51
49.2511.42
31.407.99
1.811.07

0.89
0.73
0.85
0.88

5.25
7.43
3.87
0.54

53.7711.87
54.9612.98
25.88*4.93
1.861.14

55.5712.43
52.6812.64
26.294.75
2.061.16

0.85
0.84
0.80
0.91

6.16
6.58
2.81
0.45

Abbreviations: B1, low-frequency band; B2, medium- frequency band; B3, high-frequency band; MF, median frequency; nu, normalized unit.
* A significant difference (P<.05) between groups only for day 1.

were selected and divided into the control group and PFPS group.
The sample loss was due to not following the diagnostic and
exclusion criteria used in this study. Table 1 presents the
descriptive data of the sample.
The data reliability of the electromyography parameters is
presented in tables 2 and 3. The results showed a moderate to very
high reliability associated with a low variability in the parameters
of domain frequency of the VM and VL muscles for both groups.
To compare the groups, the mean of day 1 was used, and the
differences were significant. The low-frequency band from the
VM muscle was able to differentiate the participants with and
without PFPS. The medium-frequency bands from both muscles
were reliable and able to differentiate between the control group
and the PFPS group (see tables 2 and 3).
The outcomes of the diagnostic accuracy of the index test refer
to the medium-frequency band because this parameter from both
muscles was able to differentiate the groups. The cutoff value
determined corresponds to a confidence interval of 95%. For the
VM muscle, the interval was between 26.72 and 31.26, and for the
VL muscle, the interval was between 24.75 and 29.01. The participants who reported values within these ranges were considered
pain-free, and the participants with values outside these ranges
were considered to have PFPS. The sensitivity, specificity, PPV
and NPV, and LR and LR results are presented in table 4.

Discussion
To our knowledge, this is the first study to explore the diagnostic
accuracy of the association of clinical and biomechanical parameters, represented by the electromyography variable, for
diagnosing PFPS. Our results revealed positive diagnostic accuracy values and suggest the use of the medium-frequency band
associated with anterior knee pain for the diagnosis of PFPS.

Table 4 Medium-frequency band associated with referred


anterior knee pain diagnostic values*
Index Test

Reference
Standard

Positive

Negative

Total

Positive
Negative
Total

19 (true positive)
8 (false negative)
27

3 (false positive)
21 (true negative)
24

22
29
51

* SensitivityZ0.70 (range, 0.51e0.84); specificityZ0.87 (range,


0.69e0.95); LRZ5.63 (range, 1.9e16.68); LRZ0.33 (range,
0.18e0.61); PPVZ0.86; NPVZ0.72.

In this study, the sensitivity, specificity, PPV and NPV, and


LR and LR tests recommended for diagnostic accuracy26,28
showed better results than did those of other studies. According
to the systematic review of Nunes et al,7 5 studies that investigated
the diagnostic accuracy of the 24 clinical tests for PFPS diagnosis
did not present consistent evidence regarding the diagnostic accuracy. That review showed that squatting was the most sensitive
test (91%) and that the VM coordination test had the best specificity (93%). Those tests had low specificity (50%) and low sensibility (16%).7 It is worth noting that those tests do not satisfy the
recommendation of the literature that the screening test should be
both sensitive and specific.26 The present study complies with the
diagnostic accuracy recommendations because the index test is
both sensitive (70%) and specific (87%).
The activity instability test had the highest PPV (100%) among
the tests presented in the review,7 but it had a low NPV (35%). The
test has a high chance of providing the correct diagnosis for
affected individuals, but it has a high chance of giving a wrong
diagnosis for individuals who are not affected.26,27 In the present
study, the PPV (86%) and NPV (72%) are balanced, so the test has
a greater chance of correctly diagnosing both evaluated conditions. This study showed the highest LR (5.6) compared with all
the tests presented in the review. According to the literature, the
likelihood ratio is considered the best statistic for summarizing the
usefulness of a diagnostic test.26,27 In the present study, the LR
(0.3) did not display strong diagnostic evidence28 but had the
second best results when compared with all the 24 tests cited in
the review.7
Previous studies29,30 have investigated the diagnostic accuracy
values of the combined tests, and the results showed no diagnostic
evidence because the LR was low (4.0) and the LR (0.5) was
high. The combination proposed in this study had better diagnostic
accuracy values (LR, 5.6; LR, 0.3). The difference between
the results might be due to the type of test involved. The clinical
tests for PFPS diagnosis are questionable because most of them
are dependent on the subjectivity of the examiner. Few studies
have investigated the reliability of the clinical tests, and those
studies reported poor reliability (.48e.59). The screening test
used in this study was conducted using a reliable and precise
sEMG parameter.
In conducting this study, our goal was to determine an sEMG
parameter that was reliable, precise, and able to differentiate individuals with and without PFPS in both muscles. The mediumfrequency bands fulfill these criteria, with ICC values ranging
from high reliability (ICCZ.81) to very high reliability
(ICCZ.90) associated with low SEM value means, ranging from
9.68% to 12.22%. The sEMG frequency domain parameters were
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Diagnostic accuracy of electromyography in knee pain


selected because altered muscle activation or muscle inhibition is
reflected in the changes in the spectral properties of an electromyogram.10 Healthy subjects show better control of the patella
than do patients with PFPS.12,31 Other electromyography parameters, such as the onset of the VM and VL, which could
explain this condition, have yielded controversial results.9,32
Another concern was the quality of the diagnostics by the standard reference. The criteria used as the standard references in this
study are in agreement with those of other studies: evaluating
each patient with a history of anterior knee pain, functional loss,
and positive clinical test and ruling out the presence of other
diseases.14-16
Two reviews have been published7,8 regarding the diagnostic
accuracy of the clinical tests for PFPS, and both reviews reported
that the studies evaluated presented low methodological quality
and their results are dubious. The results of the present study make
a great contribution to the field by presenting a new perspective in
diagnosing PFPS.

Study limitations
The use of the index test presented in this study showed positive
diagnostic accuracy values. This study was a preliminary investigation, and its applicability requires caution. This study has
some limitations that need to be considered for future studies, such
as a larger sample size and no restriction of gender. Although the
incorporation of part of the standard reference in the index test
might be considered bias, we are in search of the best method of
diagnosis and believe that the classical clinical questions cannot
be excluded from the diagnostic process.

Conclusions
The findings of this study revealed a positive outcome of the
diagnostic accuracy of the sEMG parameters associated with
referred anterior knee pain of a level of at least 2cm on a VAS and
pain in functional activity. The results of this study provide
diagnostic evidence for the use of this screening test in the diagnosis of PFPS.

Suppliers
a. Lynx, Rua Doutor Jose Elias, 358, Sao Paulo - SP, 05083-030,
Brazil.
b. Kendall, 15 Hampshire St, Mansfield, MA 02048.
c. Quark Medical, Rua do Rosario, 1519 - Centro, Piracicaba - SP,
13400-186, Brazil.
d. SPSS Inc, 233 S Wacker Dr, 11th Fl, Chicago, IL 60606.

Keywords
Anterior knee pain syndrome; Electromyography; Rehabilitation;
Sensitivity; Specificity

Corresponding author
Fabio Mcolis de Azevedo, PhD, Rua Roberto Simonsen, 305,
Presidente Prudente, SP 19060-900, Brazil. E-mail address:
micolis@fct.unesp.br.

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1525

Appendix 1 Criteria for the classification of


participants
True positive

False positive

True negative
False negative

 Anterior knee pain level of at least 2cm on a 10cm VAS in the last month
 Anterior knee pain during at least 2 of the
following activities: prolonged sitting, climbing
stairs, squatting, running, kneeling, and hopping
and jumping
 VM and/or VL altered in electromyography analyses
 Anterior knee pain level of at least 2cm on a 10cm VAS in the last month
 Anterior knee pain during at least 2 of the
following activities: prolonged sitting, climbing
stairs, squatting, running, kneeling, and hopping
and jumping
 VM and/or VL normal in electromyography analyses
 Not have pain in knee
 VM and/or VL normal in electromyography analyses
 Not have pain in the knee
 VM and/or VL altered in electromyography analyses

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