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Med Biol Eng Comput (2017) 55:1367–1378

DOI 10.1007/s11517-016-1597-3

ORIGINAL ARTICLE

A novel fuzzy approach for automatic Brunnstrom stage


classification using surface electromyography
Luca Liparulo1 · Zhe Zhang2 · Massimo Panella1 · Xudong Gu3 · Qiang Fang2 

Received: 23 September 2015 / Accepted: 7 November 2016 / Published online: 1 December 2016
© International Federation for Medical and Biological Engineering 2016

Abstract  Clinical assessment plays a major role in post- separating surfaces. Experiments using sEMG data col-
stroke rehabilitation programs for evaluating impairment lected from stroke patients have been carried out to exam-
level and tracking recovery progress. Conventionally, this ine the validity and feasibility of the proposed method. In
process is manually performed by clinicians using chart- order to ensure the generalization capability of the classi-
based ordinal scales which can be both subjective and inef- fier, a cross-validation test has been performed. The results,
ficient. In this paper, a novel approach based on fuzzy logic verified using the evaluation decisions provided by an
is proposed which automatically evaluates stroke patients’ expert panel, have reached a rate of success of the 92.47%.
impairment level using single-channel surface electromyo- The proposed fuzzy classifier is also compared with other
graphy (sEMG) signals and generates objective classifica- pattern recognition techniques to demonstrate its superior
tion results based on the widely used Brunnstrom stages performance in this application.
of recovery. The correlation between stroke-induced motor
impairment and sEMG features on both time and frequency Keywords  Stroke rehabilitation · Brunnstrom approach ·
domain is investigated, and a specifically designed fuzzy Surface electromyography · Pattern recognition · Fuzzy
kernel classifier based on geometrically unconstrained logic
membership function is introduced in the study to tackle
the challenges in discriminating data classes with complex
1 Introduction

* Qiang Fang Stroke is an acute cerebrovascular disease caused by cer-


john.fang@rmit.edu.au ebral hemorrhage or infarction and is considered as the
Luca Liparulo leading cause of death and long-term disabilities in the
luca.liparulo@uniroma1.it world [7, 17, 40]. During a stroke incident, the interrup-
Zhe Zhang tion of brain blood supply, increased intracranial pressure
zhe.zhang@rmit.edu.au and toxic effects of the released blood can induce severe
Massimo Panella damage to the brain tissues. Depending on the location of
massimo.panella@uniroma1.it the lesion, various body-functioning impairments can be
Xudong Gu resulted including muscle weakness, sensory loss and cog-
jxgxd@hotmail.com nitive deficits which can have great impacts on the living
1 quality of the stroke survivors. Although the tissue damage
Department of Information Engineering, Electronics
and Telecommunications, University of Rome “La Sapienza”, is often irreversible, it has been proven that it is possible
Via Eudossiana 18, 00184 Rome, Italy to partially regain the body functions by utilizing brains
2
School of Electrical and Computer Engineering, RMIT remodeling ability [36] and the post-stroke rehabilitation
University, Melbourne, VIC 3000, Australia programs can have significant contributions in maximiz-
3
Rehabilitation Medical Centre, Jiaxing 2nd Hospital, ing the positive outcomes of the recovery process [39, 59].
Jiaxing 314000, Zhejiang, China However, the current rehabilitation programs can be greatly

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1368 Med Biol Eng Comput (2017) 55:1367–1378

labor-intensive and costly. By 2007, there are 62 million needed due to the relatively simple and noninvasive pro-
stroke survivors worldwide and 55–75% of them suffer cedure compared to intramuscular EMG [14, 16]. Due to
from various degrees of body-functioning impairment and the ability of reflecting critical neural activities such as
requires rehabilitation services [15, 57]. The large expendi- motor unit recruitment and synchronization, sEMG has
ture associated with the ever-growing stroke population has already been proven effective for detecting neuromuscular
driven substantial amount of researches into finding auto- abnormalities, fatigue and voluntary motion intention [3,
matic solutions to improve the effectiveness and cost-effi- 4, 8].
ciency of post-stroke rehabilitation [22, 45, 46, 68–70, 72]. Implementation of sEMG analysis can also be found
The clinical evaluation of motor function has been an in post-stroke rehabilitation applications [9, 71]. After
important part of post-stroke rehabilitation. The deteriora- stroke incident, the upper motor neuron lesion can lead
tion of motor function caused by stroke can greatly reduce to imbalanced excitatory and inhibitory input to alpha
patients muscle strength and dexterity which have direct motor neurons and cause abnormal muscle excitability or
impact on patients ability of independent living [53]. By spasticity which eventually results in significant limita-
conducting motor function assessments throughout a reha- tion on patients motion [41]. Therefore, by investigating
bilitation program, clinicians are able to track the patients the abnormalities in sEMG signals, valuable information
recovery progress and customize the training prescriptions about stroke patients motor function impairment can be
for optimal rehabilitation outcome. Conventionally, the obtained. In [71], high-density sEMG with 89 channel
assessments are performed manually by experienced reha- recordings has been used for classifying different training
bilitation experts using chart-based ordinal scales such as motions performed by stroke patients. A Hidden Markov
Brunnstrom stage of recovery [5, 6], Fugl-Meyer Assess- Multivariate Autoregressive (HMM-mAR) network-based
ment (FMA) [20], Barthel Index [32] and National Insti- approach for bisectional stroke impairment classification
tutes of Health Stroke Scale (NIHSS) [31]. The labor-inten- has been introduced in [9], and the result suggests that
sive assessment methods are not only inefficient but also it is possible to identify post-stroke impairments using
lacking in consensus between assessors which makes the sEMG. Finally, in [61] the authors have hypothesized that
comparison of patients data across different institutes and two electromyographic (EMG) channel recordings could
regions very difficult. In order to improve the efficiency provide useful information for evaluating the outcome of
and reliability of motor function assessment in post-stroke rehabilitation determining the spatial characteristics of
rehabilitation, automatic and objective assessment methods motor activity. The analysis has been carried out defining
are required. 14 different movements and using support vector machines
The study on motor impairments caused by stroke has (SVMs) with the implementation of radial basis function
attracted substantial amount of research attentions to (RBF) kernels. However, in order to replace the current
improve rehabilitation outcome. One solution, proposed human experience based on motor function assessment,
in several researches, is to introduce an automatic man- multi-level stroke impairment classification needs to be
agement system which is capable of unsupervised motion investigated.
recording and classification during a rehabilitation training In this paper, a novel fuzzy kernel-based approach is pro-
program and thus the doctors will be able to track patients’ posed to automatically classify stroke patients motor func-
training performance without having to attend every train- tion impairment based on Brunnstrom scale using sEMG.
ing session [18]. Inertial Measurement Unit (IMU)-based As for other similar applications [33, 43], the system is
motion tracking system is commonly considered as most designed to be efficient and practical for implementation in
suitable due to its advantages of being compact, cost-effec- rehabilitation programs, especially where human supervi-
tive and relatively easy to operate compared to its counter- sion is reduced such as home- or community-based training
parts such as visual-based tracking systems [19]. Therefore, environment. Therefore, single-channel sEMG data sam-
to achieve high accuracy and optimal efficiency, the selec- pled during dynamic training movements are adopted in
tion of data processing methods and classification algo- this research. The validity of the proposed method is tested
rithms is crucial. with 93 sEMG samples collected from 9 stroke patients.
Surface electromyography (sEMG) records the electri- The participating patients motor function impairment lev-
cal activities produced by skeletal muscle groups using els are classified based on Brunnstrom stage of recovery by
electrodes attached to the skin surface. sEMG signals an expert panel prior to the experiment, and the automatic
can provide rich information about muscle activation and classification results generated by the proposed system are
functioning from neuro-electrophysiology perspective compared with the experts judgment. Both 10-fold and
and thus to aid the analysis and assessment of neurologi- leave one out (LOO) cross-validation methods have been
cal diseases. It is commonly adopted in clinical settings taken to ensure repeatable results and to estimate the gener-
when repetitive assessment of general muscle activation is alization capability of the trained classifier.

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2.1 Brunnstrom stages of recovery

Brunnstrom approach is a classification method which


models the motor recovery process following stroke-
induced hemiplegia with a six-stage ordinal scale [5, 6].
It is commonly adopted in post-stroke rehabilitation and
research programs as an assessment tool for evaluating
stroke patients body function impairment due to its reli-
ability, simplicity and clinically proven validity [27, 38, 52,
55, 62]. The Brunnstrom stages of recovery cover the com-
plete motor recovery progression from the initial stage of
complete flaccidity and no voluntary movement to the final
stage when spasticity disappears and near normal isolated
joint movements become possible. Brunnstrom approach
emphasizes on the unique patterns associated with stroke
recovery including the development of motor spasticity,
synergies patterns and voluntary motions. The simple six-
stage assessment system not only makes the Brunnstrom
approach easy to be implemented as a repetitive follow-
up test but also improves the communication efficiency
with patients by allowing them to easily understand their
own recovery progress [55]. This advantage can be further
extended by introducing the automatic assessment methods
introduced in this study.

Fig. 1  Flowchart of the proposed sEMG-based automatic 2.2 Fuzzy classification


Brunnstrom stage classification system
Pattern recognition is considered as an efficient approach
for analyzing either small or large amounts of data. It can
The rest of the paper will be arranged as follows: the be described as a method of grouping and dividing objects
experiment setup and the proposed algorithm will be intro- using a variety of measures of similarity or dissimilarity
duced in Sect. 2; the results will be presented in Sect. 3 and based on a suitable number of features that can represent a
discussed in Sect. 4. In Sect. 5, we will draw our conclu- dataset [60]. The applications of pattern recognition can be
sions and we will explain the future works. found in almost every field in science and technology. Early
in the twentieth-century, a large number of algorithms
and related variants have been proposed in the literature,
2 Methods and many of them were designed to suit specific applica-
tions. When the a priori knowledge of the data permits the
The overview of the proposed motion classifier system is label assignment within a number of categories or classes,
shown in Fig. 1. The sEMG data are first sampled from the process is known as supervised classification [21, 25].
stroke patients during a repetitive rehabilitation training This type of classification algorithms learn in a data-driven
movement. The raw signal is then preprocessed before fashion based on predetermined input and output pairs, and
features are extracted. A normalization step is also per- produce models that are capable of labeling new input pat-
formed before classifier training in order to accommodate terns autonomously.
every feature of the data space in the range between 0 and An important component of a classification process is
1. During the cross-validation test, the data are segregated the selection of a suitable number of features to represent
into three groups: the training, validation and testing data- the data [48]. Various methods using suited pattern recog-
set. The classifier is first trained and validated using the nition approaches are illustrated in [42], in order to estab-
training and validation set in order to optimize the internal lish feature ranking, selection and extraction, including the
parameter, and then the performance of the system is exam- dimensionality reduction that is often a critical procedure
ined using the testing data. Both 10-fold and LOO cross- for the computational cost management. Once a set of fea-
validation methods have been adopted to ensure the gener- tures has been selected and extracted from the available
alizability of the proposed system. dataset, a classification model from the input space of the

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1370 Med Biol Eng Comput (2017) 55:1367–1378

data can be learnt. The performance of the model is meas-


ured by assessing its ability to correctly label new obser-
vations. In order to obtain an unbiased examination of the
generalization error, 10-fold cross-validation and LOO are
adopted in the study [37].
Conventional (crisp) classification algorithms allow a
binary decision only, which assigns each input pattern a
single class [35]. Conversely, fuzzy algorithms are able to Fig. 2  MF computation for a simple 2-D case using (2): a cone-
shaped kernel is placed at each point within the class
tolerate the overlapping of classes and to deal with uncer-
tainty within data, as the estimated classification models
yield fuzzy labels using a degree of membership of any
input pattern to each class with a range between 0 and 1
[49, 63–65]. Non-exclusive classification based on fuzzy
models is therefore able to produce an extended interpreta-
tion of data structures [47, 66], where overlapping classes
may exist, and makes more robust the successive decision-
making process, when a single class must be necessar-
ily determined, for example, by using a Winner-Takes-All
(WTA) strategy.
The feature vectors extracted by complex signals
obtained from the sEMG data, collected from post-stroke
patients characterized by different Brunnstrom stages, are
Fig. 3  The structure of the proposed fuzzy kernel classifier
associated with overlapping data structures. In fact, some
patients might be likely assigned to several Brunnstrom
stages with a certain degree of uncertainty. This means that In our approach, each linear kernel is associated with a
input patterns related to those patients should be character- MF represented by a number L of points corresponding to
ized by a partial membership to different classes, each class the patterns belonging to that class; this is inversely related
representing a particular Brunnstrom stage. to the distance of a pattern from the cluster boundaries.
The underlying idea of this paper is to prove that the This method exploits the superposition of an appropriate
combined use of fuzzy logic with a more flexible geometry number of functions for building the MF of each cluster.
of the classification model, which will be based on a suited Let L × N be a matrix V, where N is the number of data
prototype of fuzzy membership function (MF) [28–30], can features:
solve the problem of the sEMG-based classification of the    
Brunnstrom stage by assigning each pattern a fuzzy label v1 v11 · · · v1N
with a typical decision-making procedure based on WTA V =  ...  =  ... .. 
(1)
  
. 
strategy in order to determine the most appropriate stage. vL vL1 · · · vLN
In addition, an innovative and extended type of information
will be provided to Clinicians. Let x be the pattern whose MF to the class must be com-
puted, the MF for that point is represented by:
2.3 Unconstrained MF
L
  γ 
A flexible and computationally affordable MF is adopted in
µ(x) = max 0, 1 − d2 (x, vi ) , (2)
δ
i=1
the proposed study to cope with the complex shaped data
clusters and improve the classification performance. A MF where d2 (x, vi ), i = 1 . . . L, is the pattern-to-ith-point
is constructed by combining cone-shaped linear kernels Euclidean distance and δ is the maximum distance that can
evaluated for each pattern based on point-to-boundary dis- occur between two patterns. This value can be determined
tance. As a result, it does not have the constraints derived simply based on the total number of features using the fol-
from specific geometrical structures (such as hypercubes, lowing expression:
hyperspheres, regular polytopes) and can adapt to various √
shapes depending on the structure of data clusters. This δ = N. (3)
approach was originally introduced in [29, 30], where the An example of cone-based MF is illustrated in Fig. 2. It is
results have proven that the unconstrained MF is effective based on a toy example with a single class composed by 12
and feasible when dealing with complex clustering tasks. randomly generated patterns. The graphical representation

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Med Biol Eng Comput (2017) 55:1367–1378 1371

of the MF is obtained by taking the summation of the 12


overlapped kernel functions constructed over each pattern
within the class. The MF is normalized within a range from
0 to 1.

2.4 Proposed fuzzy classifier

The design of the proposed fuzzy classifier is presented in


Fig. 3. After acquiring the normalized input dataset a label
vector L vector for any pattern x is evaluated:
 
L = µ(1) (x) µ(2) (x) . . . µ(K) (x) , (4)
where the kth element of L represents the fuzzy MF of the
pattern to the kth class. The fuzzified input is then directly
passed to a Winner-Takes-All (WTA) process for decision Fig. 4  Fuzzy MF evaluation with various γ values
making and the corresponding crisp label of the largest
value in the L vector will be chosen as the most suitable
class for pattern x. within the phase of stroke recovery using computer tomog-
The original data pool is first divided into training and raphy (CT) or magnetic resonance imaging (MRI). In order
validation sets for determining the optimal parameters to meet safety and ethics requirements, following inclusion
for the model learning. By applying the aforementioned criteria were imposed:
method (2), the proposed classifier can then establish a set
of fuzzy MFs to classify input patterns to the corresponding 1. no hemodynamic instability;
Brunnstrom stages. 2. no severe cognitive impairments;
The γ value is the only parameter to be optimized in the 3. no dementia;
training phase. It defines the slope of the MF: the greater 4. no major post-stroke complication;
the value of γ , the faster the function falls to zero as the 5. able and willing to give consent.
distance increases and vice versa as revealed in Fig. 4. The
optimization process is critical for achieving the best esti- Although sEMG-based approach can effectively detect
mation of the clusters. An excessively small value might voluntary motion intention for stroke patients even at very
result in unwanted class overlapping, while a large value early stage of recovery, no stage I patients were involved
may cause indeterminable clusters as the area covered by in the experiment due to unstable condition and high risk
MFs will be insufficient and the degree of membership to of complications. All subjects were examined by an expert
all the known classes could be very close to zero. panel for Brunnstrom stages prior to the sampling experi-
ment. Three panel members are selected from the rehabili-
2.5 Experimental setup tation doctors, who have:

In order to examine the performance of the proposed sys- 1. extensive clinical experience with stroke patients and
tem, an experiment with data sampled from actual stroke stroke rehabilitation;
patients has been conducted. The detail of the dataset, 2. experience in conducting stroke rehabilitation related
experimental setup and processing procedure will be medical research.
presented.
Ninety-three distinct sEMG time series have been collected
2.5.1 Experiment protocol using a Noraxon TeleMyo DTS 2400 system sampled at
3 kHz with Ag/AgCl surface electrodes. An arm abduction
The sEMG data samples are collected from the stroke and adduction movement was used during the sampling
patients in the Jiaxing 2nd hospital rehabilitation centre, experiment, and the sEMG data were sampled from mid-
Zhejiang, China. The data access and experiments have dle deltoid muscle. The movement starts with arms being
been approved by the ethic committees of RMIT University relaxed at side of the body with fingers pointing down nat-
and Jiaxing 2nd hospital. Nine stroke patients (3 males, 6 urally. The patient then smoothly raises the arm which is
females, mean age 67.2 ± 29.2) with various level of body being sampled sideways to reach the maximum angle pos-
function impairment (Brunnstrom stages II– IV) have par- sible before slowly lowering it back to the starting position
ticipated in the experiment. The subjects were verified to be and get ready for the next repetition. At the beginning of

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1372 Med Biol Eng Comput (2017) 55:1367–1378

the data sampling process, the experiment procedure and


involved exercise movements are first explained to the par-
ticipating patients. Enough time has been given for prac-
tice and rest before the actual sEMG sampling. The surface
electrodes are placed on the muscle belly with an interval
of 2 cm. The reference electrode is located at where no
muscle activation can be detected during the movement.
The skin surface is prepared with gauze and alcohol to
remove dead skins and clean the excess of oil before elec-
trodes placement. During each recording, no more than 5
repetitions of the movement are done by each patient to
reduce the influence of muscle fatigue which may signifi-
cantly affect the sample quality for early recovery stage
or elderly patients. The sampling process is repeated 2–3
times for each individual with new electrodes and re-ini-
tialized setup which gives the patients enough time to rest
Fig. 5  The segmentation of a sEMG signal sampled from a stage-3
and also introduces variability such as the change in skin patient. The high-frequency blue waveform in the background is the
impedance. The sEMG data were collected from both the original filtered sEMG signal. The slow varying green thin line is the
impaired and healthy sides of the body for comparison. rectified signal obtained using a 2048 points Hamming window. The
horizontal dashed line indicates the amplitude threshold for activation
detection which is set to be 40% of the signal median. The red rec-
2.5.2 Feature extraction tangles are the windows for signal segmentation (color figure online)

The sEMG signals sampled at 3000 Hz are first fed through


a 10th order digital ellipse bandpass filter with a pass-band classification. The details of each feature are presented
from 20 to 500 Hz and 30 dB attenuation on stop-bands for below:
noise reduction. The filtered samples are also rectified for
activation detection using root-mean-square (RMS) method • Maximum amplitude The maximum amplitude reached
with a sliding Hamming window as presented in the fol- in the rectified signal.
lowing. Let x be the filtered EMG input signal, the rectifi- • Mean amplitude The mean amplitude of the rectified
cation process can be written as: signal.
 • Activation duration The length of data segment which
1 n+L−1 represents the duration of the muscle activation as illus-
s(n) = [x(k)w(k)]2 , 1 ≤ n ≤ N, (5)
L k=n
trated in Fig. 5.
where N is the number of windowed segments, L is the • Signal energy The energy estimated using Teager Kaiser
window length, and w(k) is the Hamming window function Energy Operator (TKEO) during muscle activation. The
defined as: TKEO in discrete form is given in [23, 24] as:

ψ[x(n)] = x(n)2 − x(n + 1)x(n − 1),


 
k (7)
w(k) = 0.54 − 0.46 cos 2π , 1 ≤ k < L. (6)
L−1
where x(n) is the sEMG data sequence. The signal
The muscle activations were then automatically localized energy can then be calculated as:
by setting a threshold in relation to signal magnitude. The
N
segmentation process of a sEMG signal sampled from a 
stage-3 patient is illustrated in Fig. 5. It can be seen that
ENE = ψ[x(n)]. (8)
n−1
rectangular windows are applied over the detected move-
ment onsets. The window length is calculated to be 20% • Maximum changing rate the peak value in the first
larger than the activation period determined by an ampli- derivative of the rectified sEMG signal.
tude threshold to cover the complete movement. The acti- • The 2nd and 3nd linear prediction coefficient (LPC)
vation periods which are too close to the beginning or the The 2nd and 3nd LPC is computed by constructing a
end of the sample are disposed to avoid the inclusion of 2nd order forward linear predictor of the sEMG sam-
unintended or incomplete movements. ple signal and minimizing the prediction error with
Ten features on both time and frequency domain are least-squares method using the ‘lpc’ function in MAT-
extracted from the segmented sEMG samples before LAB.

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Med Biol Eng Comput (2017) 55:1367–1378 1373

• Average zero crossing (ZC) rate the ZC rate is calcu- Table 1  Results regarding the correlation between sEMG signal
lated by counting the zero crossing events of the origi- attributes and the progression of post-stroke recovery
nal sEMG signal within a window which is defined as: Feature InfoGain ReliefF Pearson Significance

n+L−1 Maximum amplitude 1.017 0.130 0.71 P < 0.001


1 
C(n) = sgn(x(k)x(k + 1)), (9) Mean amplitude 1.201 0.149 0.73 P < 0.001
L
k=n Activation duration 0.286 0.036 −0.36 P < 0.001
Signal energy 1.231 0.042 0.57 P < 0.001
where L is the window length and x is the original
sEMG signal. The average ZC rate is computed as: Maximum changing rate 0.677 0.117 0.73 P < 0.001
2nd LPC 0.548 0.076 0.32 P < 0.001
N
1  3rd LPC 0.228 0.086 −0.03 P = 0.388
AZC = C(n). (10) Average zero crossing 0.386 0.047 0.50 P < 0.001
N
n=1 rate
MPF 0.652 0.091 0.60 P < 0.001
• Mean power frequency (MPF) The MPF is the centroid
MF 0.641 0.091 0.64 P < 0.001
frequency of the signal power spectrum defined as:
N
n=1 P(n)f (n)
MPF = N , (11)
n=1 P(n)

where P is the power spectrum estimated using Welch’s


modified periodogram method and f is the normalized
frequency vector.
• Median frequency (MF) MF is the frequency which
divides the sEMG power spectrum into two equal por-
tions with same accumulated power. It can be defined as
the value such that:
MF N N
  1
P(n) = P(n) = P(n). (12)
2
n=1 n=MF n=1

3 Results

The dataset D used in the experiment is a M × N matrix, as Fig. 6  Example of the classification output during the validation
phase. The γ ∗ corresponds to the best error rate and will be used in
in the following:
the testing phase
   
d1 d11 · · · d1N
D =  ...  =  ... .. ,
(13) the entropy of the feature. On the other hand, ReliefF [50]
  
. 
dM dM1 · · · dMN can examine how relevant the features are to the classifi-
cation problem by implementing an instance-based nearest
where M = 93 is the number of the motions performed by neighbor search. The labels of randomly selected samples
9 patients with various level of body function impairment are compared to the samples nearby and a large number of
(Brunnstrom stage II–IV) and N = 10 is the number of neighbors with different labels on a single axis can indicate
data features. an irrelevant feature. The Pearson correlation coefficients
The extracted features are first tested against Brunnstrom [54] and the p values are also calculated to demonstrate the
stages of recovery to investigate the correlation between strength and the significance of the correlation between the
sEMG signal attributes and the progression of post-stroke features and the Brunnstrom stages. The complete result is
recovery. Different evaluation methods including InfoGain, shown in Table 1. InfoGain and ReliefF are implemented
ReliefF and Pearson correlation coefficient are adopted in using WEKA data mining workbench, and the result listed
order to analyze the contribution, correlation strength and is the ranker output.
statistical significance of the selected features. InfoGain Figure  6 has demonstrated how the proposed fuzzy ker-
measures the contribution of each feature in terms of the nel classifier is tuned with cross-validation to realize accu-
information gain with respect to the labels. It is evaluated rate Brunnstrom stage classification. The learning phase has
by subtracting joint entropy of the feature and class from been performed by evaluating the classification error while

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Table 2  10-fold and leave one out cross-validation—error rate Table 3  The confusion matrix computed using the proposed uncon-
strained fuzzy kernel-based classifier applied to the test data with a
Algorithm used Error rate (%) Error rate (%) 10-fold cross-validation
(10 fold) (LOO)
Classified outcome Accuracy (%)
Fuzzy kernel classifier 7.53 8.60
II III IV Healthy
FIS classifier (Sugeno) 9.68 11.83
FIS classifier (Mamdani) 9.68 11.83 Actual value
Neuro-fuzzy classifier 11.83 17.20  Stage II 17 0 1 0 94.44
LDA 30.11 31.18  Stage III 0 30 2 0 93.75
QDA 17.20 19.35  Stage IV 3 0 11 0 78.57
NaiveBayes 24.73 23.66  Healthy 0 0 1 28 96.55
SVM 24.73 22.58 At stage II, passive movement and spasticity occur. At stage III,
CART 16.13 15.05 active movement starts with increased spasticity. At stage IV, signifi-
PNN 45.16 46.24 cant motor control emerges and at healthy stage, coordination reap-
pears and normal function returns

changing the γ value in a computable range between 2 and


10 with a step of 0.1 as depicted in the graph. Therefore, the
γ ∗ chosen for the testing phase is the minimum value in cor-
respondence of the best error rate, calculated over a suited
validation set. Both 10-fold and LOO cross-validation meth-
ods have been performed on the above discussed data, and
the performance is evaluated based on the averaged accuracy
(number of correctly classified data divided by the total num-
ber of data, in percentage) calculated over each partition.
In order to demonstrate that the proposed method is able
to obtain the smaller error rate, different classification algo-
rithms, trained in the Matlab™ software (version R2013a),
have been also tested for comparison. All included methods
are tuned and optimized in the same cross-validation pro-
cess with the same dataset. The algorithms for comparison
are described as follows:
Fig. 7  Comparison of samples from paretic and non-paretic side
• A fuzzy inference system (FIS) both with Mamdani and
Sugeno type [34, 58], trained with the subtractive clus-
tering (SUBCL) method [12] and a neuro-fuzzy classi-
fier whose parameters are adapted by the scaled conju-
gate gradient method, is included as fuzzy approaches.
• Support vector machine (SVM) [13] and classification
and regression tree (CART) [51] are included as hard/
crisp approaches.
• Linear discriminant analysis (LDA) and quadratic dis-
criminant analysis (QDA) [26], Naive Bayes classifier
[2] and the feedforward probabilistic neural network
(PNN) [56] are included as probabilistic approaches.

In Table 2 the final results over the test set are shown. It
can be seen that all the tested fuzzy methods achieved bet-
ter performance compared to the others and the proposed
fuzzy classifier attained the minimum error rate and the
best performance in terms of accuracy. Fig. 8  Correlation between median frequency and Brunnstrom stages

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Med Biol Eng Comput (2017) 55:1367–1378 1375

The detailed performance result of the proposed fuzzy 5 Conclusions


classifier using 10-fold cross-validation is presented in
Table 3 in the form of a confusion matrix. In this paper, a novel fuzzy approach for automatic
Brunnstrom classification using sEMG has been proposed.
After investigating the sEMG data on both time and fre-
4 Discussion quency domain, strong correlations between the extracted
features and stroke patients’ recovery progress have been
By comparing the sEMG signal attributes and the progres- be observed. By implementing specifically designed fuzzy
sion of post-stroke recovery, it can be seen that the most of kernel classifier, the system is capable of automatically per-
features are strongly correlated with the Brunnstrom stages forming objective and reliable assessment of stroke patients
especially amplitude, changing rate and frequency domain motor impairment and produces highly accurate classifica-
features. Some of the results are visualized in Figs. 7 and 8. tion outcomes that agree with human expert’s decision as
Mean amplitude and median frequency both exhibit strong demonstrated in the experiment results. The automatic clas-
correlation with the recovery progress and contribute sig- sification system can be integrated into post-stroke rehabili-
nificant information gain which can benefit classification tation training programs to reduce the human effort involved
performance. As depicted in Fig. 7, the sEMG samples in the repetitive clinical assessment, especially in a training
from paretic and non-paretic group can almost be sepa- environment with reduced supervision such as committee-
rated using only the two features and the overlapping is or home-based rehabilitation programs. The objective pro-
relatively mild. It can be observed that the signal sam- cess can also serve as supplementary evidence for human
pled from unaffected limb usually has higher median fre- observation-based assessment and help to create unified
quency and stronger average amplitude. The correlation evaluation standards for more reliable data comparison
between the median frequency and Brunnstrom stages is across different institutions. In the future, it is expected that
demonstrated in Fig. 8 with the red-dotted line indicating the application of the proposed approach will be expanded
the strong Pearson correlation coefficient. As a result, the to more clinical assessment scales to suit various clinical
classification of stroke-impaired and unaffected samples situations. The classification system will also be integrated
as performed in [10, 11] can be achieved with sEMG fea- into rehabilitation programs for long-term evaluation.
tures without too much difficulty. However, the automatic
classification of stroke patients at different impairment
level or recovery stage has significantly greater value than
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1378 Med Biol Eng Comput (2017) 55:1367–1378

Xudong Gu  is the chairman Qiang Fang  is a Senior Lec-


of the Rehabilitation Centre at turer of Biomedical Engineering
Jiaxing 2nd Hospital, a profes- at RMIT University. His
sor at Jiaxing University, China, research focuses on bioelectron-
and a standing committee mem- ics and biomicroelectronics
ber of Chinese Medical Doctor especially in the areas of weara-
Association, Rehabilitation ble and implantable technolo-
Doctor Association. gies applicable to rehabilitation
and neurology.

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