Prediction of Fetal State From The Cardiotocogram Recordings Using Adaptive Neuro-Fuzzy Inference Systems

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Neural Comput & Applic (2013) 23:1583–1589

DOI 10.1007/s00521-012-1110-3

ORIGINAL ARTICLE

Prediction of fetal state from the cardiotocogram recordings


using adaptive neuro-fuzzy inference systems
Hasan Ocak • Huseyin Metin Ertunc

Received: 23 November 2011 / Accepted: 23 July 2012 / Published online: 9 August 2012
© Springer-Verlag London Limited 2012

Abstract In this study, a new scheme was presented for 1 Introduction


the prediction of fetal state from fetal heart rate (FHR) and
the uterine contraction (UC) signals obtained from car- Cardiotocography (CTG), introduced into clinical practice
diotocogram (CTG) recordings. CTG recordings are widely in the late 1960s, is the continuous recording and the
used in pregnancy and provide very valuable information monitoring of the fetal heart rate (FHR) and the uterine
regarding fetal well-being. The information effectively contractions (UC) during pregnancy, typically in the third
extracted from these recordings can be used to predict trimester. Figure 1 depicts a typical CTG recording in
pathological state of the fetus and makes an early inter- which FHR and UC are at the upper and lower parts of the
vention possible before there is an irreversible damage to figure, respectively. Since the fetus is not available for
the fetus. The proposed scheme is based on adaptive neuro- direct observations, CTG is widely used by obstetricians
fuzzy inference systems (ANFIS). Using features extracted for assessing fetal well-being. This information is of great
from the FHR and UC signals, an ANFIS was trained to importance since it allows for the early identification of a
predict the normal and the pathological state. The method pathological state (i.e., congenital heart defect, fetal dis-
was tested with clinical data that consist of 1,831 CTG tress or hypoxia, etc.) and assists the obstetrician to predict
recordings. Out of these 1,831 recordings, 1,655 of them future complications and intervene before there is an irre-
were classified as normal and the remaining 176 were versible damage to the fetus.
classified as pathological by a consensus of three expert Despite its usefulness, there has been some controversy
obstetricians. It was demonstrated that the ANFIS-based as to the utility and the effectiveness of CTG monitoring,
method was able to classify the normal and the pathologic especially in low-risk pregnancies [1]. The debates mainly
states with 97.2 and 96.6 % accuracy, respectively. originate from the fact that the recordings are visually
analyzed by experts, thus the interpretations are subjective
Keywords Fetal state · Prediction · Fetal heart rate and are not reproducible. In addition, it was shown that
(FHR) · ANFIS over-reliance on the test has led to increased misdiagnosis
of fetal distress and hence increased cesarean deliveries [2].
Although guidelines were developed for assessing the
information present in the CTG recordings, inter-observer
and intra-observer variations in the interpretations and the
misdiagnosis of fetuses (false positives) due to different
experience level of the experts still constitute a big
· M. Ertunc
H. Ocak (&) H. dilemma [3–5]. To increase the utility and the effectiveness
Department of Mechatronics Engineering, Kocaeli University, of the CTG monitoring and minimize the inconsistencies in
Umuttepe Campus, 41380 Kocaeli, Turkey the interpretations, a lot of effort has been devoted by
e-mail: hocak@kocaeli.edu.tr researchers from both medical and engineering back-
H. M. Ertunc grounds toward developing computerized systems for the
e-mail: hmertunc@kocaeli.edu.tr analysis and the classification of CTG recordings.

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1584 Neural Comput & Applic (2013) 23:1583–1589

In this study, we proposed an ANFIS-based fetal state


prediction scheme. ANFIS, the less-known approach
compared with ANN, is a soft computing technique that
combines the benefits of feed-forward calculation of output
and back-propagation of learning capability of artificial
neural networks and human-like reasoning style of fuzzy
logic. ANFIS-based models are very powerful universal
approximators with the ability of interpretable IF–THEN
rules, and they are applied in many fields such as system
identification, fuzzy control, data processing.
Almost all methods presented in the literature used
features extracted only from FHR signals to classify fetal
states. An extensive set of diagnostic features extracted
Fig. 1 A sample CTG recording (upper graph is FHR and the lower
one is UC) from both FHR and UC signals were used in this work. The
FHR- and UC-based features were used to train an ANFIS,
Various techniques have been proposed in the literature which is then used to predict fetal state being normal or
for the prediction and classification of fetal state from CTG abnormal. On contrary to existing FHR classification and
recordings. In a study presented in [6], FHR signals prediction schemes that were tested with a limited clinical
recorded between 38 and 40 week gestation were classified data set, we tested the new scheme with an extensive
using a statistical method. Auto-regressive moving-average clinical data that consist of 1,831 CTG recordings, out
(ARMA) model parameters of 3 min FHR segments were which 1,655 were classified as normal and the remaining
used as features for a retrospective classification of the 176 were classified as pathological by a consensus of three
FHR segments, using a linear discriminant function. expert obstetricians. It was shown that the new scheme was
Compared with visual classification results, the computer/ able to predict fetal state with a very high accuracy. When
observer classification agreement was found to be 85 %. In compared with widely used artificial neural network
another study [7], 36 FHR patterns belonging to hypoxic (ANN), the proposed ANFIS-based scheme performs an
(low supply of oxygen) and normal fetuses were classified average of 2 % better in terms of classification accuracies.
using hidden Markov models (HMMs). Twelve time and
frequency domain features were used to train two separate
models for the two fetal states. The models were then used
to identify the fetal state as being either hypoxic or normal. 2 Technical background on ANFIS
A maximum overall classification rate of 83 % was ANFIS is one of the first neuro-fuzzy systems and was
reported after testing of various HMM configurations. The introduced by Jang in 1993 [14]. Basically, ANFIS is a
authors of [8] used time domain parameters such as mean, multilayer feed-forward network consisting of nodes and
standard deviation, approximate entropy and frequency directional links, which combines the learning capabilities
domain parameters obtained from the power spectral den- of a neural network and reasoning capabilities of fuzzy
sity (PSD) of the FHR signals along with fuzzy inference logic. This hybrid structure of the network can extend the
systems (FIS) to identify two very common fetal patho- prediction capabilities of ANFIS beyond ANN and fuzzy
logical conditions: intra-uterine growth retardation (IUGR) logic techniques when they are used alone. Analyzing the
and type-I diabetes. Support vector machines (SVM) were mapping relation between the input and output data,
used in another study [9] to identify fetuses compromised ANFIS can establish the optimal distribution of member-
and suspicious of developing metabolic acidosis. Data set ship functions using either a back-propagation gradient
consisted of 80 FHR recordings. The authors reported descent algorithm alone or in combination with a least-
77 % classification accuracy. The method proposed in [10] squares method.
uses nonlinear features such as fractal dimension, approx-
ANFIS uses the fuzzy if–then rules involving premise
imate entropy and Lempel–Ziv complexity along with
and consequent parts of Sugeno-type fuzzy inference sys-
naive Bayes and support vector machine (SVM) classifiers
tem [14]. For the sake of simplicity, it is assumed that the
to classify FHR signals as normal or pathological. Results
inference system has two inputs x and y and one output f.A
based on 189 recordings revealed an overall sensitivity and
typical rule set with two fuzzy if–then rules for a first-order
specificity of 70 %. Methods based on wavelets [11] and
Sugeno fuzzy model can be expressed as,
neural networks [12] have also been proposed. A com-
parative study of neural networks and statistical methods is 1. If x is A1 and y is B1, then f1 ¼ p1 x þ q1 y þ r1
presented in [13]. 2. If x is A2 and y is B2, then f2 ¼ p2 x þ q2 y þ r2

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Neural Comput & Applic (2013) 23:1583–1589 1585

where p1, p2, q1, q2, r1 and r2 are linear parameters in the Layer 4 This is the de-fuzzy layer having adaptive nodes
consequent parts, while A1, A2, B1 and B2 are nonlinear and marked by square nodes. The node function in this
parameters. layer is given by a nonfuzzy equation
The corresponding equivalent ANFIS architecture for O4;i ¼ wifi ¼ wiðpix þ qiy þ riÞ; i ¼ 1; 2: ð4Þ
two-input first-order Sugeno fuzzy model with two rules is
shown in Fig. 2. The architecture of the ANFIS system where wi is the normalized firing strength output from the
consists of five layers, namely, the fuzzy layer, product previous layer and {pi, qi, ri} is the parameter set of this
layer, normalized layer, de-fuzzy layer and total output node. These parameters are linear and referred as conse-
layer. The node functions in the same layer are of the same quent parameters of this node.
function family as described in the following [14]: Layer 5 This is the last layer that simply computes the
Layer 1 This first layer is called fuzzy layer. The overall system output as the summation of all incoming
adjustable nodes in this layer are represented by square signals. Every node in this layer is a fixed node, marked by
nodes and marked by A1, A2, B1 and B2 with x and y out- circle node and labeled by R. The node function is given by
P
puts. A1, A2, B1 and B2 are the linguistic labels (small, X i wi f
O5;i ¼ wifi ¼ P ; i ¼ 1; 2: ð5Þ
large, etc.) used in the fuzzy theory for dividing the
i i wi
membership functions. The node function in this layer that
determines the membership relation between the input and Note that the system output is the weighted sum of the
output functions can be given by results of the rules. The number of fuzzy sets is determined
O1;i ¼ lAi ðxÞ; i ¼ 1; 2; by the number of nodes in Layer 1. On the other hand, the
ð1Þ dimension of Layer 4 determines the number of fuzzy rules
O1;j ¼ lB ðyÞ; j ¼ 1; 2: employed in the architecture that shows the complexity and
where O1,i and O1,j denote the output functions, and lAi and flexibility of the ANFIS architecture.
lB denote the appropriate membership functions. Similar to ANNs, an ANFIS network can be trained
Layer 2 This is the product layer, and every node is a based on supervised learning to reach from a particular
fixed node marked by a circle node and labeled by G. The input to a specific target output. In the forward pass of the
output w1 and w2 are the weight functions of the next layer. hybrid algorithm of the ANFIS, the node outputs go for-
The output of this layer, O2,i, is the product of the input ward until Layer 4, and consequent linear parameters (pi,
signals and given by qi, ri) are identified by the least-squares method using
training data. In the backward pass, the error signals
O2;i ¼ wi ¼ lAi ðxÞlBi ðyÞ; i ¼ 1; 2: ð2Þ
propagate backwards and the premise nonlinear parameters
The output signal of each node, wi, represents the firing (ai, bi, ci) are updated by gradient descent. In other words,
strength of a rule. while the adjustment of the consequent parameters is
realized in the forward pass, antecedent parameters are
Layer 3 This is the normalized layer, and every node in
adjusted during the backward pass. In short, the parameters
this layer is a fixed node, marked by a circle node and
associated with membership functions will change during
labeled by N. The nodes normalize the firing strength by
this procedure. As seen in Fig. 2, the circular parameters
calculating the ratio of firing strength for this node to the
are not adaptive, that is, they are fixed nodes with no
sum of all the firing strengths, that is,
changing parameters, while the square nodes are adaptive
wi in which the parameters are changed during training. Jang
O3;i ¼ w ¼ ; i ¼ 1; 2: ð3Þ
w1 þ w2 et al. [15] provided the detailed description and the math-
ematical background of the hybrid learning algorithm.
When the premise parameters are kept at fixed values, the
overall output can be represented as a linear combination of
the consequent parameters.

3 Methods

3.1 Clinical data and feature set

The data used in this study were obtained from UCI


Fig. 2 The architecture of ANFIS Machine Learning Repository [16] and originated from a

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Table 1 Summary of the ECG features relationship between the input and output parameters. The
LB FHR baseline (beats per minute) output of the ANFIS model was trained to be 0 for the
AC # of accelerations per second normal data and 1 for the pathological data. Each input
FM # of fetal movements per second variable, which varies within a range, are clustered into
UC # of uterine contractions per second several cluster values in Layer 1 to build up fuzzy rules,
DL # of light decelerations per second and each fuzzy rule is associated with several parameters of
DS # of severe decelerations per second membership functions in Layer 2 of the ANFIS architec-
DP # of prolonged decelerations per second
ture given in Fig. 2. As the number of rules is increased, the
ASTV Percentage of time with abnormal short-term variability
number of parameters of the membership functions
increases as well. Therefore, the data were divided into
MSTV Mean value of short-term variability
groups called as clusters using the subtractive clustering
ALTV Percentage of time with abnormal long-term variability
method to generate fuzzy inference system. Since the
MLTV Mean value of long-term variability
subtractive fuzzy clustering can automatically determine
Width Width of FHR histogram
the number of clusters, the Sugeno-type fuzzy inference
Min Minimum of FHR histogram
system was implemented to obtain a concise representation
Max Maximum of FHR histogram
of a system’s behavior with a minimum number of rules.
Nmax # of histogram peaks
The linear least square estimation was used to determine
Nzeros # of histogram zeros
each rule’s consequent equation. The fuzzy c-means was
Mode Histogram mode used as a data clustering technique wherein each data point
Mean Histogram mean belongs to a cluster to some degree that is specified by a
Median Histogram median membership grade. Therefore, a radius value was given in
Variance Histogram variance the MATLAB program to specify the cluster center’s range
Tendency Histogram tendency: -1 = left asymmetric; of influence to all data dimensions of both input and output.
0 = symmetric; 1 = right asymmetric
The neuro-fuzzy algorithm should be trained using a proper
set of training data so that the outputs can be esti- mated
study conducted in University of Porto. The data set con- based on the input–output data. Therefore, the data were
sists of measurements of fetal heart rate and uterine con-
trained to identify the parameters of Sugeno-type fuzzy
traction features on 1,831 CTG recordings classified by inference system based on the hybrid algorithm combining
three expert obstetricians. A consensus classification label
the least square method and the back-propaga- tion gradient
was assigned to each of the data. Out of the 1,831 descent method. After training, fuzzy infer- ence
recordings, 1,655 were classified as normal fetal state and calculations of the developed model were performed. Then,
the remaining 176 were classified as pathological. The the input vectors from both the training and the test data set
CTG recordings were automatically processed by an were presented to the trained network and the responses of
automated CTG analysis program SisPorto 2.0 [17], and 21
the network, that is, the predicted output parameters, were
diagnostic features were extracted from the recordings. The compared with the actual ones scored by
features are illustrated in Table 1.
the experts.
3.2 Prediction stage
4 Results and discussion
In order to develop an ANFIS model for the experimental
system, the available data set, which consists of 1,831 input As mentioned in the previous section, the ANFIS model
vectors, was divided into training and test sets. Out of the was trained to generate a value of 0 for the normal CTG
1,655 normal CTG recordings, 828 (50 %) recordings were data and 1 for the pathological CTG data. In order to
included in the training and the remaining 827 (50 %) maximize the performance of the ANFIS model, the cluster
recordings were included in the test data set. Similarly, out radius should be tuned properly. The cluster radius defines
of the 176 pathological CTG recordings, 88 (50 %) the neighborhood of a cluster center. If the cluster radius
recordings were included in the training and the remaining was specified by a small number, then there will be many
88 (50 %) recordings were included in the test data set. small clusters in the data, resulting in many rules. In con-
Data included in the training and test data sets were ran- trast, specifying a large cluster radius will yield a few large
domly selected from the normal and pathological data sets. clusters in the data, resulting in fewer rules. The detailed
The ANFIS model was developed using MATLAB Fuzzy algorithm and process of implementing the subtractive
Logic Toolbox [18]. In this model, a subtractive fuzzy fuzzy clustering into ANFIS model for various values of
clustering was generated to establish a rule base cluster radius can be found in [19, 20]. The values of the

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Neural Comput & Applic (2013) 23:1583–1589 1587

Table 2 Characteristic parameters of the ANFIS model pathological. Based on these numbers, the correct predic-
Number of nodes 596
tion rates for both the normal and pathological data in the
Number of linear parameters 286
training data set were 100 %. Out of the 827 normal data in
the test data set, 804 were correctly classified as normal
Number of nonlinear parameters 546
and the remaining 23 were misclassified as pathological.
Total number of parameters 832
Out of the 88 pathological data in the test data set, 85 were
Number of training data pairs 1,282
correctly classified as pathological and only the remaining
Number of fuzzy rules 13
three were misclassified as normal. Based on these num-
bers, the correct prediction rates of the normal and patho-
other parameters are dependent on the cluster radius. As logical data in the test data set were 97.2 and 96.6 %,
mentioned earlier, decreasing the cluster radius results in respectively. Table 3 summarizes the prediction rates of
too many small clusters in the data. Consequently, the the ANFIS model. Besides the prediction rates, the table
number of rules and the total number of linear and non- also shows the number of data classified correctly along
linear parameters increase. However, this will decrease the with the number of misclassified data for the normal and
generalization ability of the ANFIS model. In other words, the pathological CTG. As illustrated in the table, the results
the prediction performance will be very high for the for the training data set are slightly better than the test data
training data, whereas the prediction performance will be set. This is an expected result since the model parameters
very low for the test data. In this paper, by trial and error, were tuned based on the training data. Still, the results for
the optimal cluster radius was determined as 0.6. Other the test data reveal that ANFIS modeling is an effective
characteristic parameters of the developed ANFIS model means of predicting the fetal state from the CTG
are given in Table 2. recordings.
A threshold value of 0.3 is applied to the output of the The proposed method was compared with widely used
ANFIS model. An output value below the threshold value artificial neural network (ANN)-based classifier for which a
is interpreted as normal CTG, and an output value above feed-forward back-propagation neural network was used.
the threshold value is interpreted as pathological CTG. The After testing with various configurations, the best perfor-
same threshold value, selected based on the training data mance was achieved with a network having two hidden
set, is used for both the training and the test data sets. The layers. There were five neurons in the in the first hidden
performance of the trained ANFIS model was evaluated layer and three neurons in the second hidden layer. Tan-
using both the training and the test data sets. Figures 3 and gent-sigmoid transfer functions were used in the hidden
4 depict the output of the ANFIS model for the training and layers, whereas a pure linear transfer function was used in
the test data sets, respectively. All of the 828 normal CTG the output layer. The network was trained using Leven-
data in the training data set were correctly classified as berg–Marquardt (LM) algorithm. The classifier was
normal. Similarly, all of the 88 pathological CTG data in implemented in MATLAB with the same training and the
the training data set were correctly classified as test data used for the proposed scheme. The classification

Fig. 3 Output of the ANFIS for Training results


the training data 2
Normal
Pathologic
1.5 Applied threshold
ANFIS output

0.5

-0.5
0 200 400 600 800 1000 1200 1400 1600 1800 2000
Data index

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Fig. 4 Output of the ANFIS for Test results


the test data 2
Normal
Pathologic
1.5 Applied threshold

ANFIS output
1

0.5

-0.5
0 200 400 600 800 1000 1200 1400 1600 1800 2000
Data index

Table 3 Summary of the prediction results in numbers and percentages


Training data set Test data set
Normal CTG Pathological CTG Normal CTG Pathological CTG

Proposed ANFIS-based scheme Predicted as normal 828 (100 %) 0 (0 %) 804 (97.2 %) 3 (3.4 %)
Predicted as pathological 0 (0 %) 88 (100 %) 23 (2.8 %) 85 (96.6 %)
ANN-based scheme Predicted as normal 819 (98.9 %) 2 (2.3 %) 794 (96.0 %) 5 (5.7 %)
Predicted as pathological 9 (1.1 %) 86 (97.7 %) 33 (4.0 %) 83 (94.3 %)

results of the ANN-based scheme along with the proposed of delivery that would not put the mother and the baby in
ANFIS-based method are presented in Table 3. The correct extra danger and can be tolerable. On the other hand, when
prediction rates of the normal and pathological data in the a pathological CTG is mistakenly evaluated as normal, a
test data set were 98.9 and 97.7 %, respectively, for the decision of natural delivery might put both the baby’s and
ANN-based scheme as compared to 100 % for the pro- the mother’s lives in danger. Therefore, misclassification of
posed ANFIS-based scheme. The correct prediction rates pathological CTG as normal should be avoided as much as
of the normal and pathological data in the training data set possible, which can be accomplished through the feature
were 96.0 and 94.3 %, respectively, for the ANN-based selection method.
scheme as compared to 97.2 and 96.6 % for the proposed
ANFIS-based scheme. Consequently, the proposed scheme
outperforms the ANN-based scheme for an average of 2 % 5 Conclusions
for both the training and the test data sets in terms of
classification accuracies. CTG recordings carry very valuable information if inter-
The proposed scheme can further be improved in several preted correctly. The information extracted from these
ways. First, a feature reduction method, such as the genetic recordings allows for the early identification of a patho-
algorithm, can be utilized to select the features that carry logical state and assists the obstetrician to predict future
the most useful information while eliminating the irrele- complications and take necessary actions. In this study, an
vant ones. This will not only speed up the scheme but also ANFIS-based scheme was presented for predicting the fetal
improve the classification rates. In addition, the scheme can state (as normal or pathological) from CTG data. Twenty-
be modified to give more significance to reducing the one diagnostic features extracted from the CTG recordings
misclassification rate for the pathological CTG. When an by an automated CTG analysis program SisPorto 2.0 were
obstetrician incorrectly interprets a normal CTG as patho- used to train an ANFIS model. The model was trained to
logical, he/she would most likely proceed with cesarean output 0 for the normal and 1 for the pathological data. The
delivery. This would just be a wrong decision on the type trained model was then used to predict the fetal state given

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Neural Comput & Applic (2013) 23:1583–1589 1589

the features extracted from a CTG recording. Test results classification using support vector machines. IEEE Trans Biomed
based on extensive clinical data proved the proposed Eng 53(5):875–884
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11. Georgoulas G, Stylios CD, Groumpos PP (2005) Feature
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