OJRad  Vol.1 No.2 , December 2011
Synchrotron Refraction Enhanced Tomography of an Intact Common Marmoset (Callithrix jacchus)
ABSTRACT
The common marmoset (Callithrix jacchus), a small new world monkey species, has been widely used in various scientific fields. It is necessary to understand connections between specific genotypes, their structure, and function; however, an anatomical atlas of the entire body of the common marmoset has not yet been reported. In addition to conventional absorption, refraction enhanced computed tomography (CT) based on synchrotron radiation can increase the contrast of boundaries between small absorption differences. In this study, to examine the potential of creating an anatomical atlas of the whole body of the common marmoset non-invasively, we visualized an intact marmoset using synchrotron refraction enhanced CT. The cryogenic marmoset was scanned using the medical imaging beamline at the SPring-8 synchrotron radiation research facility in JAPAN. The trabecular structure, articular cartilage, cruciate ligament in the knee joint, and small airways (diameter: > 400 μm) was clearly identified with 50 μm voxel size and 37 keV x-ray energy. The structure of the heart and branching vessels in the kidneys and liver were also identified without contrast agents, and the anatomical structure of the brain was slightly visible. These results show that synchrotron refraction enhanced CT is useful for creating an anatomical atlas non-invasively, and further studies are planned that will combine refraction enhanced CT and other imaging techniques to analyse the morphology and create a complete atlas of the whole body of the common marmoset.

Cite this paper
nullSera, T. , Yokota, H. , Nakamura, S. , Uesugi, K. , Hoshino, M. , Yagi, N. , Ito, T. , Hikishima, K. and Okano, H. (2011) Synchrotron Refraction Enhanced Tomography of an Intact Common Marmoset (Callithrix jacchus). Open Journal of Radiology, 1, 28-37. doi: 10.4236/ojrad.2011.12005.
References
[1]   P. Cagni, I. Gon?alves Jr., F. Ziller, N. Emile and M. Barros, “Humans and Natural Predators Induce Different Fear/Anxiety Reactions and Response Pattern to Diaze- pam in Marmoset Monkeys,” Pharmacology Biochemis- try and Behavior, Vol. 93, No. 2, 2009, pp. 134-140. doi:10.1016/j.pbb.2009.04.020

[2]   A. Iwanami, J. Yamane, H. Katoh, M. Nakamura, S. Mo- moshima, H. Ishii, Y. Tanioka, N. Tamaoki, T. Nomura, Y. Toyama and H. Okano, “Establishment of Graded Spinal Cord Injury Model in a Nonhuman Primate: The Common Marmoset,” Journal of Neuroscience Research, Vol. 80, No. 2, 2005, pp. 172-181. doi:10.1002/jnr.20435

[3]   E. Sasaki, K. Hanazawa, R. Kurita, A. Akatsuka, T. Yo- shizaki, H. Ishii, Y. Tanioka, Y. Ohnishi, H. Suemizu, A. Sugawara, N. Tamaoki, K. Izawa, Y. Nakazaki, H. Ha- mada, H. Suemori, S. Asano, N. Nakatsuji, H. Okano and K. Tani, “Establishment of Novel Embryonic Stem Cell Lines Derived from the Common Marmoset (Callithrix jacchus),” Stem Cells, Vol. 23, No. 9, 2005, pp. 1304- 1313. doi:10.1634/stemcells.2004-0366

[4]   M. Raveendran, S. Tardif, C. N. Ross, S. N. Austad, R. A. Harris, A. Milosavljevic and J. Rogers, “Polymorphic Mi- crosatellite Loci for the Common Marmoset (Callithrix jacchus) Designed Using a Cost- and Time-Efficient Me- thod,” American Journal of Primatology, Vol. 70, No. 9, 2008, pp. 906-910. doi:10.1002/ajp.20581

[5]   E. Sasaki, H. Suemizu, A. Shimada, K. Hanazawa, R. Oiwa, M. Kamioka, I. Tomioka, Y. Sotomaru, R. Hira- kawa, T. Eto, S. Shiozawa, T. Maeda, M. Ito, R. Ito, C. Kito, C. Yagihashi, K. Kawai, H. Miyoshi, Y. Tanioka, N. Tamaoki, S. Habu, H. Okano and T. Nomura, “Genera- tion of Transgenic Non-Human Primates with Germline Transmission,” Nature, Vol. 459, No. 7246, 2009, pp. 523- 527. doi:10.1038/nature08090

[6]   G. Schatten and S. Mitalipov, “Developmental Biology: Transgenic Primate Offspring,” Nature, Vol. 459, No. 7246, 2009, pp. 515-516. doi:10.1038/459515a

[7]   G. J. Chellman, J. L. Bussiere, N. Makori, P. L. Martin, Y. Ooshima and G. F. Weinbauer, “Developmental and Re- productive Toxicology Studies in Nonhuman Primates,” Birth Defects Research Part B: Developmental and Re- productive Toxicology, Vol. 86, No. 6, 2009, pp. 446-462. doi:10.1002/bdrb.20216

[8]   D. Haig, “What Is a Marmoset?” American Journal of Primatology, Vol. 49, No. 4, 1999, pp. 285-296. doi:10.1002/(SICI)1098-2345(199912)49:4<285::AID-AJP1>3.3.CO;2-O

[9]   W. Saltzman and D. H. Abbott, “Effects of Elevated Circulating Cortisol Concentrations on Maternal Behavior in Common Marmoset Monkeys (Callithrix jacchus),” Psy- choneuroendocrinology, Vol. 34, No. 8, 2009, pp. 1222- 1234. doi:10.1016/j.psyneuen.2009.03.012

[10]   M. A. Hook and L. J. Rogers, “Visuospatial Reaching Pre- ferences of Common Marmosets (Callithrix jacchus): An Assessment of Individual Biases across a Variety of Tasks,” Journal of Comparative Psychology, Vol. 22, No. 1, 2008, pp. 41-51. doi:10.1037/0735-7036.122.1.41

[11]   E. Clara, L. Tommasi and L. J. Rogers, “Social Mobbing Calls in Common Marmosets (Callithrix jacchus): Effects of Experience and Associated Cortisol Levels,” Animal Cognition, Vol. 11, No. 2, 2008, pp. 349-358. doi:10.1007/s10071-007-0125-0

[12]   S. R. Zahed, S. L. Prudom, C. T. Snowdon and T. E. Ziegler, “Male Parenting and Response to Infant Stimuli in the Common Marmoset (Callithrix jacchus),” American Journal of Primatology, Vol. 70, No. 1, 2008, pp. 84- 92. doi:10.1002/ajp.20460

[13]   G. Epple, “Comparative Studies on Vocalization in Marmoset Monkeys (Haplidae),” Folia Primatologica (Basel), Vol. 8, No. 1, 1968, pp. 1-40.

[14]   J. D. Newman, W. M. Kenkel, E. C. Aronoff, N. A. Bock, M. R. Zametkin and A. C. Silva, “A Combined Histo- logical and MRI Brain Atlas of the Common Marmoset Monkey, Callithrix jacchus,” Brain Research Reviews, Vol. 62, No. 1, 2009, pp. 1-18. doi:10.1016/j.brainresrev.2009.09.001

[15]   K. Hikishima, M. M. Quallo, Y. Komaki, M. Yamada, K. Kawai, S. Momoshima, H. J. Okano, E. Sasaki, N. Ta- maoki, R. N. Lemon, A. Iriki and H. Okano, “Population- Averaged Standard Template Brain Atlas for the Com- mon Marmoset (Callithrix jacchus),” Neuroimage, Vol. 54, No. 4, 2011, pp. 2741-2749. doi:10.1016/j.neuroimage.2010.10.061

[16]   T. D. Nishimura, M. Takai, T. Tsubamoto, N. Egi and N. Shigehara, “Variation in Maxillary Sinus Anatomy among Platyrrhine Monkeys,” Journal of Human Evolution, Vol. 49, No. 3, 2005, pp. 370-389. doi:10.1016/j.jhevol.2005.05.001

[17]   W. M. Wagner and R. M. Kirberger, “Radiographic Ana- tomy of the Thorax and Abdomen of the Common Mar- moset (Callithrix jacchus),” Veterinary Radiology & Ul- trasound, Vol. 46, No. 3, 2005, pp. 217-224. doi:10.1111/j.1740-8261.2005.00044.x

[18]   M. I. Hofmann, C. Schradin and T. Geissmann, “Radio- graphic Evaluation of Neonatal Skeletal Development in Callimico Goeldii Reveals Closer Similarity to Callithrix jacchus than to Saguinus oedipus,” American Journal of Primatology, Vol. 69, No. 4, 2007, pp. 420-433. doi:10.1002/ajp.20361

[19]   N. Yagi, Y. Suzuki, K. Umetani, Y. Kohmura and K. Ya- masaki, “Refraction-Enhanced X-Ray Imaging of Mouse Lung Using Synchrotron Radiation Source,” Medical Phy- sics, Vol. 26, No. 10, 1999, pp. 2190-2193. doi:10.1118/1.598735

[20]   Y. Suzuki, N. Yagi and K. Uesugi, “X-Ray Refraction- Enhanced Imaging and a Method for Phase Retrieval for a Simple Object,” Journal of Synchrotron Radiation, Vol. 9, No. 3, 2002, pp. 160-165. doi:10.1118/1.598735

[21]   A. Snigirev, I. Snigireva, V. Kohn, S. Kuznetsov and I. Schelokov, “On the Possibilities of X-Ray Phase Contrast Microimaging by Coherent High-Energy Synchrotron Ra- diation,” Review of Scientific Instruments, Vol. 66, No. 12, 1999, pp. 5486-5492. doi:10.1063/1.1146073

[22]   P. Cloetens, R. Barrett, J. Baruchel, J. Guigay and M. Schlenker, “Phase Objects in Synchrotron Radiation Hard X-Ray Imaging,” Journal of Physics D: Applied Physics, Vol. 29, No. 1, 1997, pp. 133-146. doi:10.1088/0022-3727/29/1/023

[23]   S. W. Wilkins, T. E. Gureyev, D. Gao, A. Pogany and A. W. Stevenson, “Phase-Contrast Imaging Using Polychro- matic HARD X-Rays,” Nature, Vol. 384, No. 6607, 1996, pp. 335-338. doi:10.1038/384335a0

[24]   R. A. Lewis, C. J. Hall, A. P. Hufton, S. Evans, R. H. Menk, F. Arfelli, L. Rigon, G. Tromba, D. R. Dance, I. O. Ellis, A. Evans, E. Jacobs, S. E. Pinder and K. D. Rogers, “X-Ray Refraction Effects: Application to the Imaging of Biological Tissues,” The British Journal of Radiology, Vol. 76, No. 905, 2003, pp. 301-308. doi:10.1259/bjr/32889803

[25]   M. J. Kitchen, R. A. Lewis, N. Yagi, K. Uesugi, D. Pa- ganin, S. B. Hooper, G. Adams, S. Jureczek, J. Singh, C. R. Christensen, A. P. Hufton, C. J. Hall, K. C. Cheung and K. M. Pavlov, “Phase Contrast X-Ray Imaging of Mice and Rabbit Lungs: A Comparative Study,” The British Journal of Radiology, Vol. 78, No. 935, 2005, pp. 1018- 1027. doi:10.1259/bjr/13024611

[26]   D. W. Parsons, K. Morgan, M. Donnelley, A. Fouras, J. Crosbie, I. Williams, R. C. Boucher, K. Uesugi, N. Yagi and K. K. Siu, “High-Resolution Visualization of Air- space Structures in Intact Mice via Synchrotron Phase- Contrast X-Ray Imaging (PCXI),” Journal of Anatomy, Vol. 213, No. 2, 2008, pp. 217-227. doi:10.1111/j.1469-7580.2008.00950.x

[27]   M. Donnelley, K. S. Morgan, A. Fouras, W. Skinner, K. Uesugi, N. Yagi, K. K. Siu and D. W. Parsons, “Real- Time Non-Invasive Detection of Inhalable Particulates De- livered into Live Mouse Airways,” Journal of Synchro- tron Radiation, Vol. 16, Part 4, 2009, pp. 553-561. doi:10.1107/S0909049509012618

[28]   T. Sera, K. Uesugi, N. Yagi, “Refraction-Enhanced To- mography of Mouse and Rabbit Lungs,” Medical Physics, Vol. 32, No. 9, 2005, pp. 2787-2792. doi:10.1118/1.2008429

[29]   K. Uesugi, A. Tsuchiyama, T. Nakano, Y. Suzuki, N. Yagi, K. Umetani and Y. Kohmura, “Development of Mi- cro-Tomography Imaging System for Rock and Mineral Samples,” Proceedings of SPIE 3772, Denver, 22 July 1999, pp 214-221.

[30]   S. Goto, K. Takeshita, Y. Suzuki, H. Ohashi, Y. Asano, H. Kimura, T. Matsushita, N. Yagi, M. Isshiki, H. Yama- zaki, Y. Yoneda, K. Umetani and T. Ishikawa, “Constru- ction and Commissioning of a 215-m-Long Beamline at SPring-8,” Nuclear Instruments and Methods in Physics Research Section A, Vol. 467-468, Part. 1, 2001, pp. 682- 685. doi:10.1016/S0168-9002(01)00445-4

[31]   N. Yagi, M. Yamamoto, K. Uesugi and K. Inoue, “A Large-Area CMOS Imager as an X-Ray Detector for Syn- chrotron Radiation Experiments,” Journal of Synchrotron Radiation, Vol. 11, Part 4, 2004, pp. 347-352. doi:10.1107/S0909049504008519

[32]   A. C. Kak and M. Slaney, “Principles of Computerized Tomographic Imaging,” IEEE Press, New York, 1988.

[33]   C. M. Bagi, M. Volberg, M. Moalli, V. Shen, E. Olson, N. Hanson, E. Berryman and C. J. Andresen, “Age-Related Changes in Marmoset Trabecular and Cortical Bone and Response to Alendronate Therapy Resemble Human Bone Physiology and Architecture,” Anatomical Record (Ho- boken), Vol. 290, No. 8, 2007, pp. 1005-1016. doi:10.1002/ar.20561

[34]   D. Chapman, W. Thomlinson, R. E. Johnston, D. Wa- shburn, E. Pisano, N. Gmür, Z. Zhong, R. Menk, F. Arfelli and D. Sayers, “Diffraction Enhanced X-Ray Imaging,” Physics in Medicine and Biology, Vol. 42, No. 11, 1997, pp. 2015-2025. doi:10.1088/0031-9155/42/11/001

[35]   S. Fiedler, A. Bravin, J. Keyril?inen, M. Fernández, P. Suortti, W. Thomlinson, M. Tenhunen, P. Virkkunen and M. Karjalainen-Lindsberg, “Imaging Lobular Breast Carcinoma: Comparison of Synchrotron Radiation DEI-CT Technique with Clinical CT, Mammography and Histology,” Physics in Medicine and Biology, Vol. 49, No. 2, 2004, pp. 175-188. doi:10.1088/0031-9155/49/2/001

[36]   A. Bravin, J. Keyril?inen, M. Fernández, S. Fiedler, C. Nemoz, M. L. Karjalainen-Lindsberg, M. Tenhunen, P. Virkkunen, M. Leidenius, K. von Smitten, P. Sipil? and P. Suortti, “High-Resolution CT by Diffraction-Enhanced X-Ray Imaging: Mapping of Breast Tissue Samples and Comparison with Their Histo-Pathology,” Physics in Me- dicine and Biology, Vol. 52, No. 8, 2007, pp. 2197- 2211. doi:10.1088/0031-9155/52/8/011

[37]   J. Keyril?inen, M. Fernández, M. L. Karjalainen-Lind- sberg, P. Virkkunen, M. Leidenius, K. von Smitten, P. Si- pil?, S. Fiedler, H. Suhonen, P. Suortti and A. Bravin, “Toward High-Contrast Breast CT at Low Radiation Dose.” Radiology, Vol. 249, No. 1, 2008, pp. 321-327. doi:10.1148/radiol.2491072129

[38]   J. Li, Z. Zhong, D. Connor, J. Mollenhauer, C. Muehle- man, “Phase-Sensitive X-Ray Imaging of Synovial joints,” Osteoarthritis and Cartilage, Vol. 17, No. 9, 2009, pp. 1193-1196. doi:10.1016/j.joca.2009.03.005

[39]   P. Coan, A. Wagner, A. Bravin, P. C. Diemoz, J. Key- ril?inen and J. Mollenhauer, “In Vivo X-Ray Phase Con- trast Analyzer-Based Imaging for Longitudinal Osteo- arthritis Studies in Guinea Pigs,” Physics in Medicine and Biology, Vol. 55, No. 24, 2010, pp. 7649-7662. doi:10.1088/0031-9155/55/24/017

[40]   D. M. Connor, H. D. Hallen, D. S. Lalush, D. R. Sumner and Z. Zhong, “Comparison of Diffraction-Enhanced Com- puted Tomography and Monochromatic Synchrotron Radiation Computed Tomography of Human Trabecular Bone,” Physics in Medicine and Biology, Vol. 54, No. 20, 2009, pp. 6123-6133. doi:10.1088/0031-9155/54/20/006

[41]   D. M. Connor, H. Benveniste, F. A. Dilmanian, M. F. Krit- zer, L. M Miller and Zhong Z, “Computed Tomography of Amyloid Plaques in a mouse Model of Alzheimer’s Disease Using Diffraction Enhanced Imaging,” Neuroimage, Vol. 46, No. 4, 2009, pp. 908-914. doi:10.1016/j.neuroimage.2009.03.019

[42]   A. Momose, S. Kawamoto, I. Koyama, Y. Hamaishi, K. Takai, K. Uesughi and Y. Suzuki, “Demonstration of X- Ray Talbot Interferometry,” Japanese Journal of Applied Physics, Vol. 42, Part 2, 2003, pp. L866-L868. doi:10.1143/JJAP.42.L866

[43]   A. Momose, W. Yashiro, Y. Takeda, Y. Suzuki and T. Hattori, “Phase Tomography by X-Ray Talbot Interfer- ometry for Biological Imaging,” Japanese Journal of Ap- plied Physics, Vol. 45, No. 6A, 2006, pp. 5254-5262. doi:10.1143/JJAP.45.5254

[44]   J. Wu, T. Takeda, T. T. Lwin, A. Momose, N. Sunaguchi, T. Fukami, T. Yuasa and T. Akatsukaka, “Imaging Renal Structures by X-Ray Phase-Contrast Microtomography,” Kidney International, Vol. 75, No. 9, 2009, pp. 945-951. doi:10.1038/ki.2009.42

[45]   M. Shinohara, T. Yamashita, H. Tawa, M. Takeda, N. Sa- saki, T. Takaya, R. Toh, A. Takeuchi, T. Ohigashi, K. Shi- nohara, S. Kawashima, M. Yokoyama, K. Hirata and A. Momose, “Atherosclerotic Plaque Imaging Using Phase- Contrast X-Ray Computed Tomography,” American Jour- nal of Physiology Heart and Circulatory Physiology, Vol. 294, No. 2, 2008, pp. H1094-H1100. doi:10.1152/ajpheart.01149.2007

[46]   E. Pagot, S. Fiedler, P. Cloetens, A. Bravin, P. Coan, K. Fezzaa, J. Baruchel, J. H?rtwig, K. von Smitten, M. Lei- denius, M. L. Karjalainen-Lindsberg and J. Keyril?inen, “Quantitative Comparison between Two Phase Contrast Techniques: Diffraction Enhanced Imaging and Phase Propagation Imaging,” Physics in Medicine and Biology, Vol. 50, No. 4, 2005, pp. 709-724. doi:10.1088/0031-9155/50/4/010

[47]   Y. Ma, P. R. Hof, S. C. Grant, S. J. Blackband, R. Ben- nett, L. Slatest, M. D. McGuigan and H. Benveniste, “A Three-Dimensional Digital Atlas Database of the Adult C57BL/6J Mouse Brain by Magnetic Resonance Microscopy,” Neuroscience, Vol. 135, No. 4, 2005, pp. 1203- 1215. doi:10.1016/j.neuroscience.2005.07.014

[48]   T. Sera, H. Yokota, K. Fujisaki, K. Fukasaku, H. Tachi- bana, K. Uesugi, N. Yagi and R. Himeno, “Development of High-Resolution 4D in Vivo-CT for Visualization of Cardiac and Respiratory Deformations of Small Animals,” Physics in Medicine and Biology, Vol. 53, No. 16, 2008, pp. 4285-4301. doi:10.1088/0031-9155/53/16/005

[49]   K. Uesugi, T. Sera and N. Yagi, “Fast Tomography Using Quasi-Monochromatic Undulator Radiation,” Journal of Synchrotron Radiation, Vol. 13, part 5, 2006, pp. 403- 407.doi:10.1107/S0909049506023466

[50]   H. Tokuno, I. Tanaka, Y. Umitsu, T. Akazawa and Y. Na- kamura, “Web-Accessible Digital Brain Atlas of the Com- mon Marmoset (Callithrix jacchus),” Neuroscience Re- search, Vol. 64, No. 1, 2009, pp. 128-131. doi:10.1016/j.neures.2009.02.003

[51]   M. Dhenain, S. W. Ruffins and R. E. Jacobs, “Three- Dimensional Digital Mouse Atlas Using High-Resolution MRI,” Developmental Biology, Vol. 232, No. 2, 2001, pp. 458-470. doi:10.1006/dbio.2001.0189

[52]   G. A. Johnson, G. P. Cofer, S. L. Gewalt and L. W. Hed- lund, “Morphologic Phenotyping with MR Microscopy: The Visible Mouse,” Radiology, Vol. 222, No. 3, 2002, pp. 789-793. doi:10.1148/radiol.2223010531

[53]   W. P. Segars, B. M. Tsui, E. C. Frey, G. A. Johnson and S. S. Berr, “Development of a 4-D Digital Mouse Phan- tom for Molecular Imaging Research,” Molecular Imag- ing and Biology, Vol. 6, No. 3, 2004, pp. 149-159. doi:10.1016/j.mibio.2004.03.002

[54]   B. Dogdas, D. Stout, A. F. Chatziioannou and R. M. Leahy, “Digimouse: A 3D Whole Body Mouse Atlas from CT and Cryosection Data,” Physics in Medicine and Biology, Vol. 52, No. 3, 2007, pp. 577-587. doi:10.1088/0031-9155/52/3/003

[55]   M. Baiker, J. Milles, J. Dijkstra, T. D. Henning, A. W. Weber, I. Que, E. L. Kaijzel, C. W. L?wik, J. H. Reiber and B. P. Lelieveldt, “Atlas-Based Whole-Body Segmen- tation of Mice from Low-Contrast Micro-CT Data,” Me- dical Image Analysis, Vol. 14, No. 6, 2010, pp. 723-737. doi:10.1016/j.media.2010.04.008

[56]   E. Bihel, P. Pro-Sistiaga, A. Letourneur, J. Toutain, R. Saulnier, R. Insausti, M. Bernaudin, S. Roussel and O. Touzani, “Permanent or Transient Chronic Ischemic Stroke in the Non-Human Primate: Behavioral, Neuroimaging, Histological, and Immunohistochemical Investigations,” Journal of Cerebral Blood Flow & Metabolism, Vol. 30, No. 2, 2009, pp. 273-285. doi:10.1038/jcbfm.2009.209

[57]   A. Iwanami, S. Kaneko, M. Nakamura, Y. Kanemura, H. Mori, S. Kobayashi, M. Yamasaki, S. Momoshima, H. Ishii, K. Ando, Y. Tanioka, N. Tamaoki, T. Nomura, Y. Toya- ma and H. Okano, “Transplantation of Human Neural Stem Cells for Spinal Cord Injury in Primates,” Journal of Neuroscience Research, Vol. 80, No. 2, 2005, pp. 182- 190. doi:10.1002/jnr.20436

[58]   H. Yokota, R. Kawaguchi, S. Nakamura, A. Makinouchi, T. Higuchi and H. Yabe, “3-Dimensional Digitizing for the Biological Sample Using a 3-Dimensional Internal Structure Microscope,” 2001 Proceedings of the Bioen- gineering Conference ASME, Snowbird, Utah, 27 June-1 July 2001, pp. 217-218.

[59]   H. Yokota, K. Kudoh, T. Higuchi, Y. Sagara and G. S, Do, “Observation and Measurement of Frozen Biological Sample by 3-Dimensional Internal Structure Microscope,” Cryobiology and Cryotechnology, Vol. 44, No. 1, 1998, pp. 1-9.

 
 
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