Journal of Computer Assisted Tomography 26(6):927–932 © 2002 Lippincott Williams & Wilkins, Inc., Philadelphia Automatic Brain Tissue Extraction Method Using Erosion–Dilation Treatment (BREED) From Three-Dimensional Magnetic Resonance Imaging T1-Weighted Data Naoki Miura, Akito Taneda, Kazuhito Shida, Ryuta Kawashima, Yoshiyuki Kawazoe, Hiroshi Fukuda, and Toshio Shimizu Abstract: To improve the efficiency of brain image analysis, we propose a fullautomatic method for extracting brain tissue from three-dimensional magnetic resonance imaging of T1-weighted data on the human head (brain tissue extraction method using erosion-dilation treatment [BREED]). The extraction processing is realized by combining signal intensity thresholding by means of the discriminant analysis method and an erosion-dilation treatment of the image. The accuracy of BREED is evaluated using both simulated and subject data. BREED can extract brain tissues with high accuracy (approximately 97%) for either simulated or subject data. Index Terms: MRI—Segmentation—Brain tissue extraction—Discriminant analysis method— Erosion-dilation treatment. Segmentation of the brain images obtained by magnetic resonance imaging (MRI) is important because it is needed as a pretreatment for brain image analysis such as quantitative analysis of brain and cerebrospinal fluid (CSF) structures (1), gyral volumes and variances (2), and intersubject variability of ethnical and gender differences (3). So far, the segmentation of brain images has usually been a manual operation performed by welltrained experts. Obviously, however, this approach has several problems to overcome when we analyze many brain images, including 1) the need for well-trained experts, 2) the processing time for one brain image (in the case of our laboratory, typically 8 hours for one brain image by one expert), and 3) human error and operator dependency of the results (i.e., obtained results differ in accordance with who performed the operation). To overcome these difficulties, computational tools (4–7) and full-automatic segmentation techniques have been proposed (8–16). Full-automatic segmentation methods have been developed on the basis of various ideas: a priori knowledge [e.g., anatomic brain atlas (8–11) and signal intensity properties (12)], image processing approaches such as surface detection techniques (e.g., snakes) (9,13,14), automatic foreground thresholding (15), and morphologic operations with a region-growing method, morphology-based brain segmentation (MBRASE) (16). In the present article, we propose a fast full-automatic method for extracting brain tissue from threedimensional MRI T1-weighted (3D-MRI-T1) data on the human head that uses discriminant analysis to determine the threshold of signal intensity and erosion-dilation treatment of the brain image to remove nonbrain parts. We call this method BREED (brain tissue extraction method using erosion-dilation treatment). MATERIALS AND METHODS In the 3D-MRI-T1 data, CSF has lower signal intensity than white matter and gray matter; hence, CSF and brain tissue can easily be separated on the basis of signal intensity difference. The brain tissue is connected with its surrounding tissues through cranial nerves, blood vessels, and signal noise. Because the signal intensity difference between the brain tissue and these connecting parts is not significant, another technique is needed to separate them. Conversely, these connecting parts are thin or small tissues (typically, the largest connecting From the Department of Electronic and Information System Engineering, Faculty of Science and Technology, Hirosaki University, Hirosaki (N. Miura, A. Taneda, and T. Shimizu), and Center for Interdisciplinary Research (K. Shida), New Industry Creation Hatchery Center (R. Kawashima), Institute for Materials Research (Y. Kawazoe), and Institute of Development, Aging, and Cancer (H. Fukuda), Tohoku University, Sendai, Japan. Address correspondence and reprint requests to Dr. T. Shimizu, Department of Electronic and Information System Engineering, Faculty of Science and Technology, Hirosaki University, 3, Bunkyo-cho, Hirosaki, Aomori, 036–8561, Japan. E-mail: [email protected] 927 928 N. MIURA ET AL. part, the optic nerve, has a diameter of 3 mm). Therefore, to remove the connecting parts from the brain tissue, we use erosion-dilation treatment because it is useful to delete thin or small parts from the original image. Brain Tissue Extraction Procedure BREED comprises the following five steps: (i) Threshold determination and binarization: to separate brain tissue and CSF, the threshold of signal intensity is determined using the discriminant analysis method. The details of this calculation are described below. After determining the threshold, “0” and “1” are assigned to the voxels in accordance with whether the voxel has lower or higher signal intensity than the threshold, respectively. “1” corresponds to the brain tissue voxels. (ii) Erosion: the resultant image is eroded to delete thin or small connecting parts from the image. After this treatment, the image is divided into the brain tissue and nonbrain tissue if the number of erosions is appropriate. (iii) The largest-region-selection: a value of “0” is assigned to the voxels not belonging to the largest region in the image (because the largest region corresponds to the brain tissue). (iv) Dilation: the binary image obtained at step (iii) is dilated to recover the eroded brain tissue. The details of the erosion-dilation treatment (steps ii–iv) are explained below. (v) Recovering the original signal intensity: to the voxels with a value of “1” in the resultant binary image, the corresponding signal intensity values of the original 3D-MRI-T1 data are assigned. After this treatment, we can obtain extracted 3D-MRI-T1 brain data. Threshold Determination by the Discriminant Analysis Method A typical signal intensity histogram of the 3D-MRI-T1 data has two peaks: the peak at lower signal intensity comes from CSF, skull, and background noise, and the peak at higher signal intensity corresponds to white matter, gray matter, skin, and fat. By setting the threshold between these two peaks, we can approximately divide the 3D-MRI-T1 data into two parts, that is, higher (including white matter and gray matter) and lower (including CSF) signal regions. To determine the threshold, we adopt the discriminant analysis method. The discriminant analysis method determines the optimum threshold for dividing the histogram into a given number of classes. The discriminant function D for division into two classes (class 1 and class 2) is given by: D= 2b 2 w 1共M1 − MT兲 + 2共M2 − MT兲 2 = 121 + 222 J Comput Assist Tomogr, Vol. 26, No. 6, 2002 2 . (1) where b and w correspond to the variance of interclass and intraclass, respectively, and 1, 2, 1, 2, M1, M2, and MT are the number of voxels for class 1 and 2, the variance of class 1 and 2, the average signal intensity of class 1 and 2, and the average signal intensity for all voxels involved in the 3D-MRI-T1 data, respectively. By maximizing D with respect to the threshold between class 1 and 2, we can obtain the optimal threshold we need. Erosion-Dilation Treatment As depicted in Figure 1B, the binary image obtained by the threshold still keeps the thin or small parts connected between the brain tissue and outer tissues. These connecting parts can be removed by erosion treatment (17). If we define f(x, y, z) as the input value for the voxel at position x, y, z and g(x, y, z) as containing an output value for the voxel at position x, y, z, the algorithm of the erosion treatment we used is written as follows: • (a) Initial values for x, y, z are set. • (b) If at least one of f(x, y, z), f(x ± 1, y, z), f(x, y ± 1, z), or f(x, y, z ± 1) has “0”, “0” is set to g(x, y, z). • (c) When the condition of step (b) is not satisfied, “1” is set to g(x, y, z). • (d) Values for x, y, and z are updated, and we return to step (b). If all voxels have been checked, the loop is finished. It is noted that steps (a) through (d) correspond to one erosion treatment. As can be seen from Figure 1D, in the eroded image, the brain tissue is not connected with other tissues, and it is obvious that the brain tissue region is the largest region. By deleting the region with a small number of voxels in the image, the eroded brain tissue can be extracted. The erosion treatment is effective for deleting connecting parts; however, the erosion treatment also erodes the surface of brain tissue at the same time. To recover the brain tissue voxels lost during the erosion treatment, it is necessary to perform a dilation treatment. If we define g(x, y, z) as an input value for the voxel at position x, y, z, and h(x, y, z) as containing an output value for the voxel at position x, y, z, the dilation treatment is written as follows: • (a’) Initial values for x, y, and z are set. • (b’) If at least one of g(x, y, z), g(x ± 1, y, z), g(x, y ± 1, z), or g(x, y, z ± 1)’s has “1”, “1” is set to h(x, y, z). • (c’) When the condition of step (b’) is not satisfied, “0” is set to h(x, y, z). • (d’) Values for x, y, and z are updated, and we return to step (b’). If all voxels have been checked, the loop is finished. In the dilation treatment, the original binary image (corresponds to Fig. 1B) is used as a mask pattern to avoid “overdilation.” This masking is done by inhibiting the voxels with “0” in the mask pattern from being BRAIN TISSUE EXTRACTION METHOD FROM MRI DATA (a) input image (b) binary image (e) largest region (f) dilated once (c) eroded once 929 (d) eroded twice (g) dilated twice (h) resultant image FIG. 1. A through H: An example of the brain tissue extraction method using erosion-dilation treatment (2-erosion, 2-dilation). assigned “1” during the dilation. By adopting this masking, our program guarantees that a meaningless dilation is not performed. If the thickness of optic nerve is taken into consideration, the binary image must be eroded inward by 1.5 mm. Therefore, when the case of the voxel size of the input image is 1 × 1 × 1 mm, it is reasonable to suppose that the optimum erosion frequency is twice that value. An example of the brain tissue extraction process is shown in Figure 1A through H. This is a case in which both the erosion treatment and the dilation treatment were performed twice. From Figure 1H, it can be seen that only the brain tissue is successfully left in the resultant image. Although SBD gives us useful simulated images, SBD cannot simulate the influence of individual difference in brain shape. To study the influence of individual difference, we used three normal subjects’ brain data obtained from Telecommunication Advancement Organization of Japan, Aoba Brain Imaging Center. The subjects’ ages were 33 years old (Subject I), 44 years old (Subject II), and 70 years old (Subject III). The number of voxels and the voxel size for these data are 256 × 256 × 124 voxels and 1 × 1 × 1.5 mm, respectively. For these subject data, well-trained experts have manually extracted the brain tissue to obtain reference images. Validation Assessment of the Accuracy of Extracted Brain Tissue Simulated Data Extraction accuracy can be evaluated by comparing the resultant image and reference image, where the reference image is defined as the correctly extracted brain image. In SBD, the brain tissue is determined exactly. In the case of the subject data, the brain data manually segmented by specialists are used as the reference image. As four quantities to assess the accuracy of BREED, we introduce true-positive (TP), false-positive (FP), false-negative (FN), and true-negative (TN) quantities. True-positive (TP) is the number of correctly extracted brain tissue voxels that overlap the corresponding brain tissue voxels of the reference image when the resultant and reference images are superposed. False-positive (FP) is the number of voxels incorrectly extracted as “brain tissue” that overlap the nonbrain tissue in the reference image. False-negative (FN) is the number of brain tissue We used a simulated brain database (SBD) currently published by the McConnell Brain Imaging Center at the Montreal Neurologic Institute (18–21) to evaluate BREED. The SBD is a database of the 3D digital phantom generated by an MRI simulator in which various imaging parameters such as slice thickness, noise, and intensity nonuniformity (INU) can be changed. We used the digital phantoms with a slice thickness of 1 mm and with all combinations of the noise levels (0%, 1%, 3%, 5%, 7%, and 9%) and INU levels (0%, 20%, and 40%). In total, 18 combinations are used for noise and INU levels. The number of voxels in these data is 181 × 217 × 181 voxels, and the voxel size of these data is 1 × 1 × 1 mm. Subject Brain Data J Comput Assist Tomogr, Vol. 26, No. 6, 2002 930 N. MIURA ET AL. voxels incorrectly deleted in the resultant image. Truenegative (TN) is the number of nonbrain tissue voxels deleted by this method in the resultant image. By using TP, FP, FN, and TN, sensitivity (SE), positive predictive value (PPV), and extraction accuracy (EA) can be defined. Sensitivity (SE) is the ratio of the correctly extracted brain tissue of the resultant image (TP) to the brain tissue of the reference image (TP + FN): SE = TP . TP + FN (2) Positive predictive value (PPV) is the ratio of the correctly extracted brain tissue of the resultant image (TP) to the brain tissue of the resultant image (TP + FP): . PPV = TP . TP + FP (3) Extraction accuracy (EA) is the geometric mean of SE and PPV: EA = 公TP ⳯ PPV. (4) In the next section, we assess BREED through these parameters and show the performance of BREED. A 1-erosion and 1-dilation B RESULTS After the binarization of the images, more than 99% of the brain tissue remains in most of the binary images. Even in the image in the worst condition (noise level ⳱ 9%, INU level ⳱ 40%), 97.1% of the brain tissue remains. Therefore, brain tissue voxels are deleted only a little by the binarization of the images. In the case of 1-erosion and 1-dilation, 2-erosion and 2-dilation, and 3-erosion and 3-dilation, the average EAs for the simulated data are 80.1%, 97.4%, and 96.8%, respectively. Because 2-erosion and 2-dilation give the highest EAs, we adopt these values as the optimum numbers of erosion-dilation treatment. The resultant image with typical imaging parameters (noise level ⳱ 3%, INU level ⳱ 20%) is shown in Figure 2. Also, in the case of subject data, the highest accuracy is obtained by 2-erosion and 2-dilation (about 96.9%). To evaluate the processing speed, the processing time is measured. We use a standard personal computer with an AMD Athron 700-MHz central processing unit (Advanced Micro Devices, Sunnyvale, CA, U.S.A.) and 512 Mbytes of main memory, where it is working under the FreeBSD operating system (FreeBSD Project, available at http://www.freebsd.org). BREED was implemented using C language. The average processing time for one 2-erosion and 2-dilation C 3-erosion and 3-dilation FIG. 2. Resultant images of the brain tissue extraction method using erosion-dilation treatment in 1-erosion and 1-dilation (A), 2-erosion and 2-dilation (B), and 3-erosion and 3-dilation (C) for simulated data (noise level = 3%, intensity nonuniformity level = 20%). The top row shows representative slices of the input image. The images in the middle row are resultant images. The bottom row shows a comparison between resultant and reference images, where true-positive, false-positive, and false-negative values are shown by dark gray, light gray, and white regions, respectively. J Comput Assist Tomogr, Vol. 26, No. 6, 2002 BRAIN TISSUE EXTRACTION METHOD FROM MRI DATA brain image in the case of 2-erosion and 2-dilation is 8.6 seconds for simulated data and 14.2 seconds for subject data. DISCUSSION Evaluation of the Threshold Decided by the Discriminant Analysis Method Brain tissue voxels are deleted only a little by the binarization of the images. Conversely, about 10% of the CSF voxels remained in the binary images. The signal intensity of the remaining CSF voxels is higher than the obtained threshold, because signal intensity distributions of gray matter and CSF usually overlap to some extent as a result of the partial volume effect. For accurate extraction of the brain tissue, it is desirable that the brain tissue not be deleted in the binarization of the image, even if the other tissues remain to some extent. From this point of view, the obtained threshold is appropriate. Effect of the Erosion Frequency on the Extraction Accuracy In the case of 1-erosion and 1-dilation, the EAs have a low value (approximately 80%). This indicates that the ratio of the brain tissue is small. From Figure 2A, we can see that many other tissues remain. In the case of 1-erosion, any part of the image is eroded inward by 1 mm (because the voxel size of simulated data is 1 × 1 × 1 mm). Hence, regions with a width of 2 mm or less are deleted. The thickest of the connecting parts is the optic nerve, whose thickness is about 3 mm. Therefore, 1-erosion treatment cannot delete optic nerves. In the case of 2-erosion and 2-dilation and 3-erosion and 3-dilation, the EAs have high values. From Figure 2B and C, we can see that the brain tissue is correctly extracted. The EA for Subject III is slightly lower than those of the other two subjects. One of the possible reasons is the effect of aging, because Subject III is aged and his brain was atrophied. Additionally, imaging artifact and individual difference could cause a similar effect. Fortunately, the influence of such effects on EA is small; hence, we can say that BREED can give sufficiently high performance to aged data. Although it is confirmed that BREED can extract brain tissue with high accuracy, some limitations exist. The upper part of the cerebellum and the fornix are good examples. These are thin tissues on the surface of the brain tissue, and many parts of these regions are completely deleted by the erosion treatment. As a result, they could not recover by means of the dilation treatment. Blood vessels on the brain surface such as the superior sagittal vessel are another example. These can adhere to the brain surface, and their signal intensities are similar to that of the brain tissue. Therefore, it is difficult to delete these regions by BREED. 931 Processing Speed The average processing time for one brain image is 8.6 seconds for simulated data and 14.2 seconds for subject data. Although direct comparison of various computational methods is not easy because the evaluation environment of each method is different and the porting of these methods to the same environment is difficult, the processing speed of BREED is faster than that of other methods [e.g., MBRASE requires 30 minutes of central processing unit time on a processor of an SGI Power Challenge R10K (Silicon Graphics, Mountain View, CA, U.S.A.) (16)]. It is a great advantage of BREED that the brain tissue can be extracted correctly within quite a short time; this feature should be especially useful when a number of brain images are processed at once. CONCLUSION In the current study, we propose BREED for automatically extracting brain tissue from 3D-MRI-T1 data. The BREED method can accurately extract the brain tissue for both simulated and subject brain data. The most significant feature of BREED is its fast processing speed. 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