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BRUNNSTROM
BRUNNSTROM
DOI 10.1007/s11517-016-1597-3
ORIGINAL ARTICLE
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
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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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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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• 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
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
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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