10 1109@10 923789 PDF
10 1109@10 923789 PDF
10 1109@10 923789 PDF
6, JUNE 2001
Abstract—In order to automate routine fecal examination for aged more overseas travel and international food fads, allows
parasitic diseases, we propose in this study a computer processing parasitic diseases to migrate from one country to other distant
algorithm using digital image processing techniques and an countries. And despite high levels of sanitation, food inspec-
artificial neural network (ANN) classifier. The morphometric
characteristics of eggs of human parasites in fecal specimens tion, and vector control in developed countries, individuals who
were extracted from microscopic images through digital image may have acquired parasitic infections elsewhere require med-
processing. An ANN then identified the parasite species based on ical treatment. In addition, the role of zoonotic parasite is be-
those characteristics. We selected four morphometric features coming more important as agents of human diseases.
based on three morphological characteristics representing shape, Human parasitic infections are recognized through the iden-
shell smoothness, and size. A total of 82 microscopic images con-
taining seven common human helminth eggs were used. The first tification of parasitic organizms in the feces, urine, blood, and
stage (ANN-1) of the proposed ANN classification system isolated tissues by using the proper diagnostic methods [1]. Fecal exam-
eggs from confusing artifacts. The second stage (ANN-2) classified ination is the most common diagnostic method. Trained experts
eggs by species. The performance of ANN was evaluated by the examine the fecal specimens, searching for parasitic organizms,
tenfold cross-validation method to obviate the dependency on usually the eggs of helminths and cysts of protozoa. If the orga-
the selection of training samples. Cross-validation results showed
86.1% average correct classification ratio for ANN-1 and 90.3% nizms are present, they examine the sizes, shapes, and numbers
for ANN-2 with small variances of 46.0 and 39.0, respectively. to identify the species of parasites, the degree of infection, and
The algorithm developed will be an essential part of a completely appropriate therapeutic modalities. But diagnosticians are reluc-
automated fecal examination system. tant to perform fecal examinations; with decreasing importance
Index Terms—Artificial neural network, automatic identifica- of most parasites, less material is submitted for examination,
tion, helminth egg, pattern classification. which results in an insufficiency of training material. Thus, it
is difficult to maintain enough people with expertise in diag-
I. INTRODUCTION nostic parasitology. Worst of all, diagnostic parasitologists are
expected to maintain high standards of proficiency in the iden-
tion of morphological characteristics, isolation of parasitic formalin-preserved specimens containing eggs of seven human
organizms from unwanted dreg materials, and identification helminths. There were about 12 images/parasite species. The
of parasite species. To develop a totally automated system, seven typical species of human helminth were chosen as
image segmentation, the algorithm for morphometric feature follows [1]: ascaris lumbricoides, trichuris trichiura, capillaria
extraction, and classification should be automated. In addition, philippinensis, clonorchis sinensis, paragonimus westermani,
dedicated hardware equipment is necessary to scan complete diphyllobothrium latum, and taenia. Representatives of each of
images of each specimen under microscope. the egg types are shown in Fig. 1 to help the reader understand
We propose in this paper an automated method to detect the classification problem visually.
common helminth eggs in microscopic fecal specimen images To localize and classify helminth eggs in a given image, we
and to identify their correct species using digital image pro- first found meaningful objects in the image and extracted their
cessing techniques [7] and an artificial neural network (ANN) features using digital image processing methods. Then a two-
system [8]. The ANN classifier is widely used in pattern stage ANN classified them based on their numeric features.
recognition problems owing to its good performance and easy All processing routines were written in MATLAB (Mathworks,
application [8]–[10]. Natick, MA) and overall processing steps are outlined in Fig. 2.
Fig. 3. One of the typical microscopic images of fecal specimen under 200-fold magnification.
Fig. 4. Comparative sizes of typical helminth eggs. Dark bars denote ranges of length.
The cross validation took up the leave-one-out method [5] axis. The smoothness may be rephrased as the trajectory of its
with the alteration of tenfold crossover to avoid excessive time- radial distance, , which has smaller high frequency compo-
consuming repetitions. It generally provides network perfor- nents than those of the artifacts. The input layer has four input
mance evaluations independent of the choice of training and test nodes to receive the morphological feature values. It has one
set. output node which indicates whether the input morphologies are
1) Artifacts Removal with ANN-1: Significant morpholog- those of eggs or artifacts. The desired output values were de-
ical differences exist between parasite eggs and artifacts, even rived from the ground truth obtained from diagnostic experts. A
though they are similar in size, as mentioned earlier. The egg standard sigmoid activation function was used at the input and
cell has a shell membrane which makes its boundary look more hidden nodes, while a linear activation function was used at the
circular and smoother than those of the artifacts. The circularity output node [8]. 187 samples (87 eggs and 100 artifacts in total)
of shell may be expressed by the ratio of its short axis and long were randomly divided into ten subsets of approximately equal
722 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. 48, NO. 6, JUNE 2001
TABLE III
SUMMARY OF FEATURES USED IN ANN-1 AND ANN-2
B. ANN Classification
III. RESULTS In all, the finally trained ANN-1 showed 100% correct clas-
sification in the training phase and 84% correct classification in
A. Segmentation and Feature Extraction
the test phase. In terms of detection accuracy, it showed 83%
Typical digital processing results with the original image of TP ratio and 10% FP ratio on the test samples with the cutoff at
Fig. 3 are shown in Figs. 7 and 8. In this case, the original the half of output scale. The results are summarized in Table IV.
724 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. 48, NO. 6, JUNE 2001
(a)
(b)
Fig. 7. Typical results of digital image processing: (a) median filtered image, (b) black and white image obtained from binary thresholding. A total of 11 objects
marked by rectangular boxes are detected as meaningful objects. The rectangles represent the segmented objects.
And the ROC curve in Fig. 6 shows the efficiency in TP/FP re- neighbor classifier are compared with ANN-1 and ANN-2,
lationship. The normalized area under the curve is 0.87. respectively. The number of three and eight were chosen
The finally trained ANN-2 showed 100% correct classifica- since they showed better performances than other values
tion in learning stage and 83% correct classification at test stage. in each application. The results show the superiority of
For more details, identification results for individual species are the proposed ANN classifiers over the -nearest neighbor
presented in a confusion matrix form in Table V. classifiers.
In Table VI, the comparison between performance evalua- Fig. 9 shows the typical results of final classification for the
tions of these two ANNs and -nearest neighbor classifiers C. sinensis and C. philippinensis. The white boxes in Fig. 9(a)
are summarized. The three-nearest neighbor and eight-nearest and (c) denotes the detected parasite eggs by ANN-1. Then the
YANG et al.: AUTOMATIC IDENTIFICATION OF HUMAN HELMINTH EGGS ON MICROSCOPIC FECAL SPECIMENS 725
(a)
(b)
(c)
(d)
Fig. 8. Comparison of meaningful objects, segmented from Fig. 7. The leftmost images show objects and their obtained boundary lines. The plots in the middle
column represent their normalized radial trajectories, r (). The plots in the last column show the logarithms of amplitude spectra against discrete frequencies
ranging from zero to 2 . (a), (b), and (c) Artifacts. (d) Egg cell.
IV. DISCUSSIONS
TABLE V
DETAILS OF ANN-2 CLASSIFICATION RESULTS IN A CONFUSION MATRIX FORM
TABLE VI
COMPARISONS OF ANN-1 AND ANN-2 WITH SIMPLE k -NEAREST NEIGHBOR CLASSIFIERS
ANN-based classifier. The results showed acceptable perfor- produced erroneous results in minor cases especially when
mances with an 84% detection ratio and an 83% identification there is any nearby material around the object of concerns.
ratio and proved the applicability of the developed algorithms More complicated and accurate segmentation techniques
to full automatic examination system. such as [12]–[17] are expected to improve the results and
The visual recognition results used as ground truths in this being investigated for possible simpler form.
study are considered very reliable since they had been derived The practical fecal examination is based not only on the exis-
from well-trained human experts and also cross checked by tence of helminth eggs but also on the number of their findings.
other diagnostic methods, for example, DNA analysis. Since the helminth normally produces a large number of eggs,
The ANN errors revealed in the detection and identifica- there must be many of them in a fecal specimen. Therefore, any
tion results are thought to be caused mainly by incomplete few positive findings, whether True or False, need further ex-
segmentation results rather than by the ANN performance aminations such as blood and tissue analysis.
itself. The errors involved in poorly segmented objects There is no general rule for selection of proper network
affect ANN at the training phase as well as the test (ap- topology and proper data sample size for the best performance.
plication) phase by providing inaccurate numeric features. We studied the dependency of the optimal network topology
Despite its advantages over the common edge detection on the available data size by comparing the results with
methods specifically for microscopic images, the binary available data of 52 and 82. The numbers of neurons (input–1st
thresholding method used in this study results in tradeoff hidden–2nd hidden–output layer) in ANN-1 and ANN-2 for
between accuracy and complexity. In majority of images, the best results were changed from 4-6-6-1 to 4-8-8-1 and from
this method showed good segregation result. However, it 3-6-6-7 to 3-8-8-7, respectively. This indicates that there exists
YANG et al.: AUTOMATIC IDENTIFICATION OF HUMAN HELMINTH EGGS ON MICROSCOPIC FECAL SPECIMENS 727
(a)
(b)
Fig. 9. Typical results of ANN-1 and ANN-2: (a) detection result of C. sinensis. (b) Identification result of (a).
a relationship between the optimal network topology and the In this study, ANN classification was performed by two
available sample size in our specific application. The adequacy sub classifiers. This separation made the training easier and
of the sample size of 82 still has not been verified. The proper reduced total processing time in real application to images.
size of data sample is highly related to the distributional Most ANNs classify given patterns according to their geo-
characteristics of the given data samples. For example, in a metric clustering in the pattern space [8]. In the case of
case where the given data samples represent the classification fecal images, however, the artifacts are too dispersed in the
problem well, relatively small number of data would provide feature space to be treated as one or few couples of classes.
satisfactory result. This would increase the complexity of ANN, that is, the
728 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. 48, NO. 6, JUNE 2001
(c)
(d)
Fig. 9. (Continued.) Typical results of ANN-1 and ANN-2. (c) Detection result of C. philippinensis and (d) identification result of (c).
number of nodes and connections. Therefore, egg finding in The computed time for the overall procedure, including digital
the segmented objects was implemented separately from the image processing and ANN classifiers was approximately 15
identification of parasite species. The resultant two ANNs s/image. By discarding objects smaller than the minimum egg
have much simpler architectures than they would have in size at the segmentation, which eliminated unnecessary feature
one incorporated network. Moreover, this separation reduced extraction, the computational load was alleviated. By the way, one
the number of computations by skipping the application of specimen slide usually consists of 60 view fields under 200-fold
ANN-2 to the artifacts preremoved by ANN-1. magnified views. Therefore, if the developed algorithm is applied
YANG et al.: AUTOMATIC IDENTIFICATION OF HUMAN HELMINTH EGGS ON MICROSCOPIC FECAL SPECIMENS 729
to the entire section of slide plate, it will take about 15 min to [16] N. Shareef, D. L. Wang, and R. Yagel, “Segmentation of medical images
process. This length of time, which appear rather lengthy, can be using LEGION,” IEEE Trans. Med. Imag., vol. 18, pp. 74–91, Jan. 1999.
[17] M. D. Srinath, P. K. Rajasekaran, and R. Viswanathan, Introduction to
easilyreducedbyhalformorebyimplementingroutinesoptimally Statistical Signal Processing with Applications. Englewood Cliffs, NJ:
with professionalprogramming languages and compilation. Prentice-Hall, 1996.
The targets for the developed algorithm were seven typical
human helminth eggs. For the identification of more parasitic
species than in this study, a detailed analysis of materials in- Yoon Seok Yang (S’00) received the B.S. degree in
side the shell membrane [4] under 400-fold or higher magnifi- control and instrumentation engineering from Seoul
cation is indispensable. Much more features than employed in National University, Seoul, Korea, in 1996 and M.S.
degree in interdisciplinary course (biomedical engi-
this study may be possible and even the best features, in terms neering major) from Yonsei University, Seoul, Korea,
of maximal variances and minimal redundancy, would be able in 1998. He is currently a Ph.D. degree candidate in
to derived from them using dimensionality reduction methods the Medical Electronics Laboratory (MELab) of the
Seoul National University.
like Karhunen–Loéve transformation [17]. Future work will ac- From 1996 to 1998, he worked as a Research
commodate this procedure. Member at the Department of Biomedical En-
The ultimate goal of this study is to develop an automatic exam- gineering of Yonsei University Medical Center.
His main research topic was an early detection of breast cancer in digital
ination system. Two different types of processing are possible. In mammogram. In 1998, he joined the Medical Electronics Laboratory (MELab)
an online processing system, the program performs the parasitic of the Seoul National University, where the major research activities are
egg identification on one digital image before the next scan. In development of portable electronics and intelligent algorithms for medical and
biological applications such as artificial pancreas, biosensors, telemedicine,
this case, total processing time should be reduced significantly. and man-machine interface. His interests include signal processing. From
UsingthelargestoragecapacityofamodernPC,anoff-linesystem 1999 to 2000, he worked on the ultrasonic biologic tissue characterization
scans the whole slide first and stores all digital images. Then, the project funded by MEDISON, Korea, that develops various ultrasonic medical
equipments.
program retrieves the stored images and carries out the identifica- Mr. Yang is a student member of Korea Society of Medical and Biological
tion. The developed algorithm will be an essential part of the main Engineering (KOSOMBE).
software of a completely automated system.
Min-Ho Choi received the Ph.D. degree in parasite Jong-Yil Chai received the M.D. and Ph.D. (medical
biochemistry (medical parasitology major) from parasitology) degrees from Seoul National University
Seoul National University, Seoul, Korea, in 1996. College of Medicine, Seoul, Korea, in 1976 and 1984,
From 1989 to 1993, he has worked as a Research respectively.
Assistant at the Department of Parasitology, Seoul He has been with the Department of Parasitology,
National University College of Medicine, Seoul Seoul National University College of Medicine since
Korea. He was a Public Health Doctor of National 1976. He is now Professor and Chairperson of the De-
Institute of Health, Korea, from 1993 to 1996, where partment. For abroad studies, he worked on mucosal
he counseled HIV-infected persons in Korea. He immunity to protozoan parasites, from 1986 to 1987,
joined the faculty of the Department of Parasitology, in Animal Parasitology Institute, US Department of
Seoul National University College of Medicine in Agriculture, Beltsville, MD, as a Visiting Scientist.
1996, where he is currently an Assistant Professor. He is now a Visiting Scholar He also studied on immunity to intestinal parasites, in 1993, in the Department
at the Department of Pathology, Division of Infectious Diseases, University of of Parasitology, Institute of Medical Science, The University of Tokyo, Japan, as
California, San Diego Medical Center, San Diego, CA, and he is studying the a Visiting Professor. He has published over 300 peer-reviewed academic papers
pathogenesis of amebiasis and transgenic amebae. in the field of medical parasitology and one textbook on clinical parasitology,
Dr. Choi is a member of Korea Society for Parasitology and the American and contributed many chapters of textbooks on clinical medicine. His research
Society of Parasitology. area includes a wide range of parasites of human beings including protozoa
and helminths, but he has been mostly interested in the researches on intestinal
flukes.
Dr. Chai is currently the President of Korean Society for Parasitology, and
member of American Society of Tropical Medicine and Hygiene, American
Society of Parasitologists, Society of Protozoologists, Society for Mucosal Im-
munology, and Helminthological Society of Washington, Royal Society of Trop-
ical Medicine and Hygiene, and Japanese Society of Parasitology.