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Yamaguchi Y & Yamada S. (2018). The Kyoto Collection of Human Embryos and Fetuses: History and Recent Advancements in Modern Methods. Cells Tissues Organs (Print) , 205, 314-319. PMID: 30064127 DOI.

The Kyoto Collection of Human Embryos and Fetuses: History and Recent Advancements in Modern Methods

The Kyoto Collection of Human Embryos and Fetuses, the largest collection of human embryos worldwide, was initiated in the 1960s, and the Congenital Anomaly Research Center of Kyoto University was established in 1975 for long-term storage of the collection and for the promotion of research into human embryonic and fetal development. Currently, the Kyoto Collection comprises approximately 45,000 specimens of human embryonic or fetal development and is renowned for the following unique characteristics: (1) the collection is considered to represent the total population of fetal specimens nationwide in Japan, (2) it comprises a large number of specimens with a variety of external malformations, and (3) for most specimens there are clinical and epidemiological data from the mothers and the pregnancies concerned. Therefore, the specimens have been used extensively for morphological studies and could potentially be used for epidemiological analysis. Recently, several new approaches such as DNA extraction from formalin-fixed specimens or geometric morphometrics have been adopted and it is to be expected that further technological advances will facilitate new studies on the specimens of the Kyoto Collection as well as of other human embryo collections worldwide. Permanent preservation of the Kyoto Collection is, therefore, of paramount importance so that it will continue to contribute to human embryological studies in the future. © 2018 S. Karger AG, Basel. KEYWORDS: Anatomy; Embryo/fetus; Embryology human; Histology human; Image analysis; Image analysis medical; Magnetic resonance imaging PMID: 30064127 DOI: 10.1159/000490672

Eugenics and Maternal Protection Law in Japan.

Human cardiac development in the first trimester: a high-resolution magnetic resonance imaging and episcopic fluorescence image capture atlas. Dhanantwari P, Lee E, Krishnan A, Samtani R, Yamada S, Anderson S, Lockett E, Donofrio M, Shiota K, Leatherbury L, Lo CW. Circulation. 2009 Jul 28;120(4):343-51. doi: 10.1161/CIRCULATIONAHA.108.796698. No abstract available. PMID 19635979

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  • Embryology - 発生学 (Hassei-gaku)
  • Kyoto embryology collection - 京都発生学コレクション (Kyōto hassei-gaku korekushon)
  • Digital embryology collection - デジタル発生学コレクション (Dejitaru hassei-gaku korekushon)
  • Digital embryology consortium - デジタル発生学コンソーシアム (Dejitaru hassei-gaku konsōshiamu)

Collection Overview

(Last Updated - April 7, 2014) Specimens 23,813

Stage 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 Embryonic Fetal
Normal 14 16 5 25 44 298 745 2133 1569 2653 2621 2697 2417 2393 1620 1101 909 21260 920
Abnormal 0 0 1 2 4 9 42 69 40 167 236 186 131 265 260 114 50 1576 54
Total 14 16 6 27 48 307 787 2202 1609 2820 2857 2883 2548 2658 1880 1215 959 22836 974
Kyoto Specimens
Stage 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 Embryonic Fetal
Normal 14 16 5 25 44 298 745 2133 1569 2653 2621 2697 2417 2393 1620 1101 909 21260 920
Abnormal 0 0 1 2 4 9 42 69 40 167 236 186 131 265 260 114 50 1576 54
Total 14 16 6 27 48 307 787 2202 1609 2820 2857 2883 2548 2658 1880 1215 959 22836 974
Stage 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 Embryonic Fetal
Normal 14 16 5 25 44 298 745 2133 1569 2653 2621 2697 2417 2393 1620 1101 909 21260 920
Abnormal 0 0 1 2 4 9 42 69 40 167 236 186 131 265 260 114 50 1576 54
Total 14 16 6 27 48 307 787 2202 1609 2820 2857 2883 2548 2658 1880 1215 959 22836 974


Branching morphogenesis of the urinary collecting system in the human embryonic metanephros

Ishiyama H, Ishikawa A, Kitazawa H, Fujii S, Matsubayashi J, Yamada S & Takakuwa T. (2018). Branching morphogenesis of the urinary collecting system in the human embryonic metanephros. PLoS ONE , 13, e0203623. PMID: 30192900 DOI.

Ishiyama H1, Ishikawa A1, Kitazawa H1, Fujii S1, Matsubayashi J1, Yamada S1,2, Takakuwa T1.


An elaborate system of ducts collects urine from all nephrons, and this structure is known as the urinary collecting system (UCS). This study focused on how the UCS is formed during human embryogenesis. Fifty human embryos between the Carnegie stage (CS) 14 and CS23 were selected from the Kyoto Collection at the Congenital Anomaly Research Center of Kyoto University, Japan. Metanephroses, including the UCS, were segmented on serial digital virtual histological sections. Three-dimensional images were computationally reconstructed for morphological and quantitative analyses. A CS timeline was plotted. It consisted of the 3-D structural morphogenesis of UCS and quantification of the total amount of end-branching, average and maximum numbers of generations, deviation in the metanephros, differentiation of the urothelial epithelium in the renal pelvis, and timing of the rapid expansion of the renal pelvis. The first UCS branching generation occurred by CS16. The average branching generation reached a maximum of 8.74 ± 1.60 and was already the twelfth in CS23. The total end-branching number squared between the start and the end of the embryonic period. UCS would reach the fifteenth branching generation soon after CS23. The number of nephrons per UCS end-branch was low (0.21 ± 0.14 at CS19, 1.34 ± 0.49 at CS23), indicating that the bifid branching occurred rapidly and that the formation of nephrons followed after. The renal pelvis expanded mainly in CS23, which was earlier than that reported in a previous study. The number of nephrons connected to the UCS in the expanded group (246.0 ± 13.2) was significantly larger than that of the pre-expanded group (130.8 ± 80.1) (P < 0.05). The urothelial epithelium differentiated from the zeroth to the third generations at CS23. Differentiation may have continued up until the tenth generation to allow for renal pelvis expansion. The branching speed was not uniform. There were significantly more branching generations in the polar- than in the interpolar regions (P < 0.05). Branching speed reflects the growth orientation required to form the metanephros. Further study will be necessary to understand the renal pelvis expansion mechanism in CS23. Our CS-based timeline enabled us to map UCS formation and predict functional renal capacity after differentiation and growth.

Anat Rec (Hoboken). 2018 Apr 16. doi: 10.1002/ar.23783. [Epub ahead of print] Developing the Digital Kyoto Collection in Education and Research. Hill MA1. Author information Abstract The Kyoto embryo collection was begun in 1961 by Dr. Hideo Nishimura. The collection has been continuously developed and currently contains over 44,000 human normal and abnormal specimens. Beginning online in 1997, the internet provided an opportunity to make embryos from the collection widely available for research and educational purposes ( These embryonic development resources have been continuously published and available from that time until today. Published in Japanese as an Atlas of Embryonic Development. Published online as the Kyoto Human Embryo Visualization Project ( and also as the Human Embryo Atlas ( Published now electronically as a digital eBook ( This new digital format allows incorporation of whole embryo and histology manipulable images, labels, and a linked glossary. New imaging modalities of magnetic resonance imaging (MRI) and episcopic fluorescence image capture (EFIC) can also be easily displayed as animations. For research, the collection specimens and histological sections have been extensively studied and published in several hundred papers, discussed here and elsewhere in this special edition. I will also describe how the Kyoto collection will now form a major partner of a new international embryology research group, the Digital Embryology Consortium ( The digital Kyoto collection will be made available for remote researcher access, analysis, and comparison with other collections allowing new research and educational applications. This work was presented at the 40th Anniversary Commemoration Symposium of the Congenital Anomaly Research Center, Graduate School of Medicine, Kyoto University, Japan, November, 2015. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. KEYWORDS: Kyoto collection; development; digital technology; embryology; human PMID: 29663673 DOI: 10.1002/ar.23783


Cartilage formation in the pelvic skeleton during the embryonic and early-fetal period

PLoS One. 2017 Apr 6;12(4):e0173852. doi: 10.1371/journal.pone.0173852. eCollection 2017.

Okumura M1, Ishikawa A1, Aoyama T1, Yamada S1,2, Uwabe C2, Imai H3, Matsuda T3, Yoneyama A4, Takeda T4, Takakuwa T1.


The pelvic skeleton is formed via endochondral ossification. However, it is not known how the normal cartilage is formed before ossification occurs. Furthermore, the overall timeline of cartilage formation and the morphology of the cartilage in the pelvis are unclear. In this study, cartilage formation in the pelvic skeletons of 25 human fetuses (crown-rump length [CRL] = 11.9-75.0 mm) was observed using phase-contrast computed tomography and 7T magnetic resonance imaging. The chondrification center of the ilium, ischium, and pubis first appeared simultaneously at Carnegie stage (CS) 18, was located around the acetabulum, and grew radially in the later stage. The iliac crest formed at CS20 while the iliac body's central part remained chondrified. The iliac body formed a discoid at CS22. The growth rate was greater in the ilium than in the sacrum-coccyx, pubis, and ischium. Connection and articulation formed in a limited period, while the sacroiliac joint formed at CS21. The articulation of the pubic symphysis, connection of the articular column in the sacrum, and Y-shape connection of the three parts of the hip bones to the acetabulum were observed at CS23; the connection of the ischium and pubic ramus was observed at the early-fetal stage. Furthermore, the degree of connection at the center of the sacrum varied among samples. Most of the pelvimetry data showed a high correlation with CRL. The transverse and antero-posterior lengths of the pelvic inlet of the lesser pelvis varied among samples (R2 = 0.11). The subpubic angle also varied (65-90°) and was not correlated with CRL (R2 = 0.22). Moreover, cartilaginous structure formation appeared to influence bone structure. This study provides valuable information regarding the morphogenesis of the pelvic structure.

Shigehito Yamada

Search term: Yamada S

<pubmed limit=5>Yamada Shigehito</pubmed>


A detailed comparison of mouse and human cardiac development

Pediatr Res. 2014 Dec;76(6):500-7. doi: 10.1038/pr.2014.128. Epub 2014 Aug 28.

Krishnan A1, Samtani R2, Dhanantwari P3, Lee E4, Yamada S5, Shiota K5, Donofrio MT6, Leatherbury L1, Lo CW7.


BACKGROUND: Mouse mutants are used to model human congenital cardiovascular disease. Few studies exist comparing normal cardiovascular development in mice vs. humans. We carried out a systematic comparative analysis of mouse and human fetal cardiovascular development. METHODS: Episcopic fluorescence image capture (EFIC) was performed on 66 wild-type mouse embryos from embryonic day (E) 9.5 to birth; 2-dimensional and 3-dimensional datasets were compared with EFIC and magnetic resonance images from a study of 52 human fetuses (Carnegie stage 13-23). RESULTS: Time course of atrial, ventricular, and outflow septation were outlined and followed a similar sequence in both species. Bilateral venae cavae and prominent atrial appendages were seen in the mouse fetus; in human fetuses, atrial appendages were small, and a single right superior vena cava was present. In contrast to humans with separate pulmonary vein orifices, a pulmonary venous confluence with one orifice enters the left atrium in mice. CONCLUSION: The cardiac developmental sequences observed in mouse and human fetuses are comparable, with minor differences in atrial and venous morphology. These comparisons of mouse and human cardiac development strongly support that mouse morphogenesis is a good model for human development. PMID 25167202

Morphogenesis of the spleen during the human embryonic period

Anat Rec (Hoboken). 2014 Nov 18. doi: 10.1002/ar.23099. [Epub ahead of print]

Endo A1, Ueno S, Yamada S, Uwabe C, Takakuwa T.


We aimed to observe morphological changes in the spleen from the emergence of the primordium to the end of the embryonic period by using histological serial sections of 228 samples. Between Carnegie stages (CSs) 14 and 17, the spleen was usually recognized as a bulge in the dorsal mesogastrium (DM), and after CS 20, the spleen became apparent. Intrasplenic folds were observed later. A high-density area was first recognized in 6 of the 58 cases at CS 16 and in all cases examined after CS 18. The spleen was recognized neither as a bulge nor as a high-density area at CS 13. The mesothelium was pseudostratified until CS 16 and was replaced with high columnar cells and then with low columnar cells. The basement membrane was obvious after CS 17. The mesenchymal cells differentiated from cells in the DM, and sinus formation started at CS 20. Hematopoietic cells were detected after CS 18. The vessels were observed at CS 14 in the DM. Hilus formation was observed after CS 20. The parallel entries of the arteries and veins were observed at CS 23. The rate of increase in spleen length in relation to that of stomach length along the cranial-caudal direction was 0.51 ± 0.11, which remained constant during CSs 19 and 23, indicating that their growths were similar. These data may help to better understand the development of normal human embryos and to detect abnormal embryos in the early stages of development. This article is protected by copyright. All rights reserved. Copyright © 2014 Wiley Periodicals, Inc. KEYWORDS: dorsal mesogastrium; human embryo; morphogenesis; spleen PMID 25403423

High-resolution histological 3D-imaging: Episcopic fluorescence image capture is widely applied for experimental animals

Congenit Anom (Kyoto). 2014 Nov;54(4):250-1. doi: 10.1111/cga.12057.

Tsuchiya M1, Yamada S.

PMID 24517239


Development of the human tail bud and splanchnic mesenchyme

Congenit Anom (Kyoto). 2013 Mar;53(1):27-33. doi: 10.1111/j.1741-4520.2012.00387.x.

Hashimoto R1.

Abstract The purpose of this paper was to shed some light on anorectal development from a viewpoint of the tail bud and splanchnic mesenchyme for better understanding of the morphogenesis of the human anorectum. Human embryos ranging from Carnegie stage 11 to 23 (CS 11 to 23) were adopted in this study. Seventeen embryos preserved at the Congenital Anomaly Research Center of Kyoto University Graduate School of Medicine were histologically examined. The cloaca, extending caudally to the hindgut, was dramatically enlarged, particularly both its dorsal portion and membrane, that is, the cloacal membrane resulting from the development of the tailgut derived from the tail bud. The splanchnic mesenchyme surrounding the hindgut was spread out in the direction of the urorectal septum ventrally, suggesting that it participated in the formation of the septum. No fusion of the urorectal septum and the cloacal membrane was found. The splanchnic mesenchyme proliferated and developed into smooth muscle (circular and longitudinal) layers from cranial to caudal along the hindgut. The tail bud seems to cause both the adequate dilation of the dorsal cloaca and the elongation of the cloacal membrane; its dorsal portion in particular will be necessary for normal anorectal development. The splanchnic mesenchyme developed and descended toward the pectinate line and formed the internal sphincter muscle at the terminal bowel. © 2012 The Author. Congenital Anomalies © 2012 Japanese Teratology Society.

PMID 23480355


Variabilities in prenatal development of orofacial system

Anat Anz. 1991;172(2):97-107.

Tanaka O.


Reliable information on embryonic and fetal development of the human oro-facial system is meager. Much of the data available at present is not entirely reliable, because it was derived from a small number of specimens. An embryological approach with human materials is important for establishing a normal standard of development including individual variabilities as well as clarifying the embryogenesis and etiology of defective development (Nishimura et al. 1977). It is important in human craniofacial embryology to know the variabilities, that is, individual differences in developmental phenomena of the oro-facial region during human prenatal life. In recent times the importance of morphologic investigations of human development has received less emphasis. Yet, without thorough knowledge of the basic facts of prenatal human development, erroneous assumptions can be made in more dynamic approaches and lead investigators astray. Knowledge of prenatal development of human orofacial structures and some of their deviations will therefore be welcomed by many basic scientists and clinicians in the field of facial clefts and other craniofacial malformations. The author was engaged in the collection and systematic study of human embryos and fetuses with Dr. Hideo Nishimura, Emeritus Professor of Kyoto University, Kyoto, Japan, and has been studying the normal and abnormal development during prenatal life. Several results obtained from the study of a large number of specimens are presented laying stress on the orofacial development.

PMID 2048747