Imaging of a Large Collection of Human Embryo Using a Super-Parallel MR Microscope

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1 Magn Reson Med Sci, Vol. 6, No. 3, pp , 2007 MAJOR PAPER Imaging of a Large Collection of Human Embryo Using a Super-Parallel MR Microscope Yoshimasa MATSUDA 1,ShinyaONO 1, Yosuke OTAKE 1, Shinya HANDA 1, Katsumi KOSE 1 *, Tomoyuki HAISHI 2,ShigetoYAMADA 3, Chikako UWABE 3, and Kohei SHIOTA 3 1 Institute of Applied Physics, University of Tsukuba Tennodai, Tsukuba, Ibaraki , Japan 2 MR Technology Inc., Tsukuba, Japan 3 Center for Congenital Anatomy Research, Kyoto University, Kyoto, Japan (Received December 6, 2006; Accepted September 5, 2007) Using 4 and 8-channel super-parallel magnetic resonance (MR) microscopes with a horizontal bore 2.34T superconducting magnet developed for 3-dimensional MR microscopy of the large Kyoto Collection of Human Embryos, we acquired T 1 -weighted 3D images of 1204 embryos at a spatial resolution of (40 mm) 3 to (150 mm) 3 in about 2 years. Similarity of image contrast between the T 1 -weighted images and stained anatomical sections indicated that T 1 -weighted 3D images could be used for an anatomical 3D image database for human embryology. Keywords: embryo, ˆxed specimen, MR microscopy, multi-channel receiver, parallel MRI Introduction The 40,000 50,000 human embryos acquired by Kyoto University from 1961 to are famous andbelievedtobethelargestsuchcollectioninthe world. The uniqueness of such a large collection underlies the desire for the non-destructive 3D measurements of these specimens. Several methods for non-destructive 3D measurement may be applied to chemically ˆxed embryos. Although X-ray computed tomography (CT) is widely used, especially for skeletal systems, the poorly established skeletal systems of these human embryos made its use unsuitable in this case. Neither was ultrasound, used clinically for fetuses and embryos in vivo, useful for visualizing the internal ˆne structure of the chemically ˆxed embryos because of the limited wavelength of clinical ultrasound machines. However, MR microscopy is a very powerful tool for 3D measurement of human embryos because the chemically ˆxed human embryos contain large quantities of mobile or NMR visible protons, which are major components of the formalin preservation uid. Three-dimensional *Corresponding author, Phone: , Fax: , measurement of the human embryo structures at high spatial resolution replaces the time-consuming histological sectioning, staining, and 3D reconstruction tasks. Consequently, in 1999, Kyoto and Tsukuba Universities began a project to acquire 3D MR microscopic images of thousands of embryos. We report their methods and results. 4,5 Materials and Methods Humanembryospecimens Human embryo specimens were chemically ˆxed in Bouin's uid and stored in 10z formalin solution. 1 Twelve hundred and four undamaged and normal-appearing specimens, ranging from Carnegie stage (CS) 13 to 23 and corresponding to 28 to 56 days post conception, were selected from the collection (Table). The specimens were transferred from preservation tubes to nuclear magnetic resonance (NMR) sample tubes, the diameters of which were minimized to maximize the signal-to-noise ratio (SNR) of the NMR signal. The specimens were transported in NMR sample tubes ˆlled with formalin solution to avoid mechanical shock and biological contamination. 139

2 140 Y. Matsuda et al. Table. Human embryos selected for 3D magnetic resonance microscopy Carnegie Stage Number of Samples Tube inner diameter (mm) Voxel Size (mm) /7.0 40, /9.0 40, 45, 50, /9.0 45, 50, /9.0 50, 55, /18 120, /18 120, 150 Outer and inner diameters (OD/ID; mm) of the NMR test tubes used for the embryos were 5/4; 8/7; 10/9; 12/10.5; 15/13.5; and 20/18. The total number of embryos was Super-parallel MR microscope Four- and eight-channel super-parallel MR microscopes were developed Each consisted of a 2.34T horizontal bore superconducting magnet (40 cm room temperature bore, 16 cm diameter spherical volume [dsv] homogeneous region), 4- and 8- channel linear array gradient probes, 4- and 8- channel parallel NMR transceivers, an 8-channel radiofrequency (RF) transmitter, a 3-channel gradient driver, and industrial personal computers. Figure 1 shows the 8-channel linear-array gradient probe developed for NMR sample tubes measuring 8 mm in outer diameter. The 4-channel linear array gradient probe with replaceable radiofrequency (RF) coil units was used for measuring specimens stored in NMR sample tubes measuring 10-, 12-, 15-, and 20-mm in outer diameter. The RF coils were solenoids, and the numbers of turns were optimized for the diameters of the sample tubes. The 4-channel parallel NMR transceiver system was built in-house utilizing commercial quadrature detection modules. 9 The 8-channel parallel NMR transceiver was a commercial system (DTRX-Octet-array, MRTechnology-DS Technology, Japan). The detected parallel NMR signals were digitized using 4 or 8 ADC boards (PC-414G3, Datel, USA) installed in one or 2 industrial personal computers running on the Windows 98 operating system. Further details of the system were described previously. 9 Imaging pulse sequences Three-dimensional spin echo or gradient echo imaging pulse sequences were used throughout the experiment. Repetition time (TR) varied from 100 to 2400 ms, and echo time (TE) varied from 8 to 28 ms in the spin echo sequences. In the gradient echo Fig. 1. Eight-channel linear array gradient probe. Size: 14 cm (width) 14 cm (height) 18.5 cm (diameter). Outer diameters for the sample tubes were 8 mm. sequences, TR and TE were ˆxed at 100 ms and 6 ms, and ip angles (FA) were varied from 109to 909. The image matrix for most pulse sequences was ; for some sequences, it was Voxel size varied from (40 mm) 3 to (150 mm) 3. Imaging experiments Embryo specimens were imaged in NMR sample tubes ˆlled with formalin solution, which protected the embryos from desiccation and magnetic susceptibility artifacts. To improve the SNR, NMR sig- Magnetic Resonance in Medical Sciences

3 Imaging of a Large Collection of Human Embryo nals were usually accumulated 16 or 24 times. Several spin echo and gradient echo imaging sequences were used to determine an optimum pulse sequence for visualization of embryo anatomy. The optimum pulse sequence described in the results was used for 3D imaging of the 1204 human embryos. Post processing of the image dataset Acquired 3D image datasets were interpolated from to voxels using a zero-ˆlled Fourier transform technique. Midsagittal cross-sectional images of the embryos were selected after 3D rotation of the interpolated 3D image datasets. Results and Discussion 141 Optimum pulse sequence for visualization of embryo anatomy Figure 2 shows mid-sagittal planes selected from 3D spin echo images of a CS22 human embryo, of which maximum intensity projection (MIP) images are shown in Fig. 3. TE was ˆxed to 8 ms, and TR was varied from 100 to 2400 ms (Fig. 2a-e). To keep the total imaging time constant (11.5 hours), the number of accumulated signals was varied from 24 to one (Fig. 2a-e). In Fig. 2f-h, TR was ˆxed to 800 ms, and TE was varied from 8 to 28 ms. T 1-weighted (T 1W) images are shown in Fig. 2a-b, and T 2-weighted (T 2W) images are shown in Fig. 2g-h. The proton density weighted (PDW) image (Fig. 2e) shows that the density of mobile protons is nearly uniform throughout the embryo Fig. 2. Mid-sagittal planes selected from 3D spin echo images of a CS22 human embryo. Repetition time/echo time were: a: 100/8 ms. b: 200/8 ms. c: 800/8 ms. d: 1200/8 ms. e: 2400/8 ms. f: 1200/8 ms. g: 1200/18 ms. h: 1200/28 ms. Field of view, mm mm mm; image matrix, ; voxel size, (120 mm) 3. Image acquisition times (about 11.5 hours) were identical for all images. Vol. 6 No. 3, 2007

4 142 Y. Matsuda et al. Fig. 3. Maximum intensity projection images of the CS22 human embryo used to image the crosssections shown in Fig. 2. These images were made by the VOLUME-ONE software provided by the VOLUME-ONE developer group and available on the Internet ( specimen, except in the liver. The low intensity of the liver results from its short T 2 ( 10 ms). The results described above demonstrate that the image contrast in the T 1WandT 2Wimagesisdetermined predominantly by T 1 and T 2, respectively. Because the development of the neural system is most important in human embryology, 11 image contrast of the neural system should be optimized. Figure 2 shows that T1W imagesmeetthisrequirement. The contrast-to-noise ratio (CNR) for the vertebrae shown in Fig. 2a was better than that shown in Fig. 2b, so we concluded that Fig. 2a was the best spin echo image for visualization of embryo anatomy. Figure 4 shows mid-sagittal planes selected from 3D gradient echo images of the CS22 human embryo used for the 3D spin echo sequences. The contrastofimageswithsmall ipangles(fig.4a-b)is similartothatofthepdwimageinfig.2e,and the contrast of images with large ip angles (Fig. 4e-f)issimilartothatoftheT1W imageshownin Fig. 2a. To compare the T 1W images obtained by spin echo and gradient echo sequences, the CNR for the vertebrae was calculated by dividing the signal intensity dišerence between the bright and dark regions of the vertebrae by the background noise. The CNR for the gradient echo image (Fig. 4f) was 80z higher than that for the spin echo image (Fig. 2a). However, as shown in Figs. 4 and 5, gradient echo images were quite sensitive to the magnetic susceptibility ešect produced by air bubbles on the surface of the embryo. Air bubbles were inevitable because all the embryo specimens were Fig. 4. Mid-sagittal planes selected from 3D gradient echo images of a CS22 human embryo. Repetition time/echo time: 100 ms/6 ms; ip angles: a: 159. b: 209. c: 309. d: 459. e: 609. f: 909; ˆeldof vision: mm mm mm; image matrix: ; voxel size: (120 mm) 3 ; and number of excitations: 16 for a-f. transferred from the preservation sample tubes to the NMR sample tubes for MR microscopy measurements. We therefore concluded that the 3D spin echo sequence with a TR/TE=100 ms/8 ms should be used to acquire images of the 1204 embryos. MR microscopy of the 1204 embryos Figure 6 shows typical mid-sagittal images selected from 3D image datasets of CS13 to CS23 embryosacquiredwitht 1W sequences. To accelerate the imaging speed, 4 (CS17 23) or 8 (CS13 16) embryos were imaged simultaneously. For the T 1Wsequences, TR was kept at 100 ms and TE was minimized: TE was varied from 8 ms to 12 ms according to the voxel size, which was determined by the achievable gradient ˆeld strength. While the image matrix was ˆxed to , voxel size was varied from (40 mm) 3 to (120 mm) 3 in Fig. 6. The 3D images of the 1204 embryos were acquired from 2003 to Magnetic Resonance in Medical Sciences

5 Imaging of a Large Collection of Human Embryo 143 Fig. 5. Enlarged mid-sagittal head images acquired with a: the spin echo sequence (repetition time/echo time [TR/TE]: 100 ms/8 ms) and b: gradient echo sequence (TR/TE/ ip angle: 100 ms/6 ms/909). Signal loss areas caused by air bubbles in the gradient echo image are indicated by arrows. Fig. 6. Typical mid-sagittal cross sections acquired with T 1 -weighted spin echo sequences and selected from 3D image datasets of CS13 23 embryos. Repetition time was set at 100 ms for all sequences. Echo time was minimized depending on the voxel size. Image matrix was Carnegie stage and voxel size (mm) 3 were: a:13and40;b:14and45;c:15and50;d:16and55;e:17 and 70; f: 18and80;g: 19 and 100; h: 20 and 100; i: 21 and 120; j: 22 and 120; and k: 23 and 120. Figure 7 shows typical mid-sagittal images of CS17 embryos. Although the embryos have various dimensions, the internal structure seems identical. Comparison of image contrast with anatomical sections Figure 8 shows sagittal cross sections of CS23 embryos: Fig. 8a-c depict a T 1-weighted SE image (TR/TE=100 ms/8 ms), a Nissl-stained anatomi- Vol. 6 No. 3, 2007

6 144 Y. Matsuda et al. Fig. 7. Mid-sagittal cross sections selected from 3D image datasets of CS17 embryos acquired with T 1 -weighted spin echo sequences. Repetition time/echo time: 100 ms/12 ms; ˆeld of view: 8.96 mm 8.96 mm mm; image matrix, ; voxel size, (70 mm) 3 ; an number of excitations: 16. Fig. 8. Mid-sagittal cross sections of CS23 embryos. a: T 1 -weighted spin echo image (repetition time/echo time:100 ms/8 ms); b: anatomical section with Nissl staining; 11 c: inverted contrast image of b. cal section as presented in a textbook, 11 andaninverted contrast image of Fig. 8b, respectively. The ˆgure shows that the image contrast of the T 1Wimage is quite similar to that of the stained anatomical section. The image intensities of several organs of the embryos shown in Fig. 8a and 8c are plotted in Fig. 9. The organs selected were tongue, liver, neural tube, Magnetic Resonance in Medical Sciences

7 Imaging of a Large Collection of Human Embryo heart, foot, vertebra (high and low intensity areas), and midbrain. The graph shows that there was a positive correlation (R 2 =0.61) between the set of images, which we interpreted as follows. It is well-known that the image intensity of the stained sections correlates positively with cell density and that longitudinal relaxation rate (1/T 1)correlates positively with intensity of the T1W image. This, and the graph in Fig. 9, suggests that cell density correlates positively with longitudinal relaxation rate. This is reasonable because when cell density increases, motion of the mobile protons among Fig. 9. Correlation between the intensity of the T 1 - weighted image and intensity of the Nissl stain. The correlation is statistically signiˆcant in Pº or in the cells tends to be slow, the spectral components of proton motion at the Larmor frequency (100 MHz) tends to increase, and longitudinal relaxation is prompted if the Larmor frequency is smaller than the inverse of the correlation time of the mobile protons. 12 The last assumption will be valid for most ˆxed specimens because the T 1 of chemically ˆxed specimens is shorter than that of fresh tissues in usual NMR frequencies In summary, the T1-weighted 3D images can be used for the 3D anatomical database of human embryos. Achievable spatial resolution The major purpose of this study was to acquire 3D microscopic images of a large number of human embryos within a limited timeframe. Thus, spatial resolution was not optimized for each embryo. Figure 10 shows a high-resolution mid-sagittal section of a CS22 embryo acquired with a gradient echo sequence (TR/TE=100 ms/6 ms; ip angle [FA]=909; number of excitations [NEX]=12) in 24 hours. The image matrix was , and the voxel size was 50 mm 3. Such a high-resolution image could be acquired for late-stage (CS21 23) embryos if measurement time was considerably extended. As shown by the gradient echo images in Fig. 4, T 2 * for most organs seems longer than 10 ms. This suggests that the spatial resolution is limited only by the SNR of the NMR signal per voxel. Higher magnetic ˆelds or improved RF coils will thus yield higher spatial resolution of the embryo specimens. Conclusions A super-parallel MR microscope with a horizontal bore 2.34T superconducting magnet developed for 3D MR microscopy of a large number of human embryos permitted acquisition of T 1-weighted 3D images of 1204 embryos at the spatial resolution of (40 mm) 3 (150 mm) 3 in about 2 years. The T 1 W image contrast was similar to that of stained anatomical sections, indicating that the T 1 W3Dimages can be used for an anatomical 3D image database for human embryology. In the future, higher spatial resolution will be attained using a higher magnetic ˆeld and improved RF coils. Fig. 10. Mid-sagittal cross-section of a CS22 embryo acquired with a gradient echo sequence (repetition time/echo time: 100 ms/6 ms; ip angle: 909; number of excitations: 8). The image matrix was and the voxel size was (50 mm) 3. Acknowledgments We gratefully acknowledge Professor Yoshiteru Seo at Dokkyo University School of Medicine and Dr. Masae Yaguchi at Keio University for their valuable advice throughout this project. Vol. 6 No. 3, 2007

8 146 Y. Matsuda et al. References 1. Nishimura H, Takano K, Tanimura T, Yasuda M. Normal and abnormal development of human embryos: ˆrst report of the analysis of 1,213 intact embryos. Teratology 1968; 1: Matsunaga E, Shiota K. Holoprosencephaly in human embryos: epidemiologic studies of 150 cases. Teratology 1977; 16: Shiota K. Neural tube defects and maternal hyperthermia in early pregnancy: epidemiology in a human embryo population. Am J Med Genet 1982; 12: Matsuda Y, Ono S, Handa S, Haishi T, Kose K. 3D MR microscopy of a large human embryo collection (Kyoto Collection) to create a 3D image database for human embryology, In: Proceedings of the 12th Annual Meeting of ISMRM, Kyoto, 2004; Matsuda Y, Ono S, Handa S, et al. 3D MR microscopy of a large human embryo collection: ˆnal report for 1,200 human embryos, In: Proceedings of the 13th Annual Meeting of ISMRM, Miami, 2005; Kose K, Haishi T, Matsuda Y, Anno I. Superparallel MR microscope, In: Proceedings of the 9th Annual Meeting of ISMRM, Glasgow, 2001; Matsuda Y, Haishi T, Yamazaki Y, Kose K, Anno I. Development of multi-channel gradient probe for super-parallel MR microscope, In: Proceedings of the 9th Annual Meeting of ISMRM, Glasgow, 2001; Matsuda Y, Utsuzawa S, Kurimoto T, et al. Development of a compact 8-channel parallel MRI console for super-parallel MR microscope, In: Proceedings of the 10th Annual Meeting of ISMRM, Hawaii, 2002; Matsuda Y, Utsuzawa S, Kurimoto T, et al. Superparallel MR microscope. Magn Reson Med 2003; 50: Otake Y, Matsuda Y, Kose K. 8-channel linear array gradient probe for the super-parallel MR microscope, In: Proceedings of the 13th Annual Meeting of ISMRM, Miami, 2005; Drews U. Taschenatlas der embryologie. 1st ed. Stuttgart: Georg Thieme Verlag, Bloembergen N, Purcell EN, Pound RV. Relaxation ešects in nuclear magnetic resonance absorption. Phys Rev 1948; 73: Thickman DI, Kundel HL, Wolf G. Nuclear magnetic resonance characteristics of fresh and ˆxed tissue: the ešect of elapsed time. Radiology 1983; 148: Kamman RL, Go KG, Stomp GP, Hulstaert CE, Berendsen HJ. Changes of relaxation times T 1 and T 2 in rat tissues after biopsy and ˆxation. Magn Reson Imaging 1985; 3: Johnson GA, Benveniste H, Black RD, Hedlund LW, Maronpot RR, Smith BR. Histology by magnetic resonance microscopy. Magn Reson Q 1993; 9:1 30. Magnetic Resonance in Medical Sciences

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