Publications by authors named "Shigehito Yamada"

106 Publications

Early development of the cortical layers in the human brain.

J Anat 2021 Jun 17. Epub 2021 Jun 17.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

The cortical plate (CP) first appears at seven postconceptional weeks (pcw), when it splits the preexisting preplate into two layers, the marginal zone and the presubplate (pSP). Although three-dimensional (3D) analysis using fetal magnetic resonance imaging and two-dimensional tissue observations have been reported, there have been no studies analyzing the early development of the layer structure corresponding to the pSP stage in 3D. Here, we reconstructed 3-D models of the brain with a focus on the cortical layers in pSP stage. To achieve this, we digitized serial tissue sections of embryos between CS20 and CS23 from the Kyoto Collection (n = 7, approximately 7-8.5 pcw), and specimens at early fetal phase from the Blechschmidt Collection (n = 2, approximately 9.5-12 pcw, crown rump length [CRL] 39 and 64 mm). We observed tissue sections and 3D images and performed quantitative analysis of the thickness, surface area, and volume. Because the boundary between pSP and the intermediate zone (IZ) could not be distinguished in hematoxylin and eosin-stained sections, the two layers were analyzed together as a single layer in this study. The histology of the layers was observed from CS21 and became distinct at CS22. Subsequently, we observed the 3-D models; pSP-IZ was present in a midlateral region of the cerebral wall at CS21, and an expansion centered around this region was observed after CS22. We observed it over the entire cerebral hemisphere at early fetal phase (CRL 39 mm). The thickness of pSP-IZ was visible in 3D and was greater in the midlateral region. At the end of the pSP stage (CRL 64 mm), the thick region expanded to lateral, superior, and posterior regions around the primordium of the insula. While, the region near the basal ganglia was not included in the thickest 10% of the pSP-IZ area. Middle cerebral artery was found in the midlateral region of the cerebral wall, near the area where pSP-IZ was observed. Feature of layer structure growth was revealed by quantitative assessment as thickness, surface area, and volume. The maximum thickness value of pSP-IZ and CP increased significantly according to CRL, whereas the median value increased slightly. The layer structure appeared to grow and spread thin, rather than thickening during early development, which is characteristic during pSP stages. The surface area of the cerebral total tissue, CP, and pSP-IZ increased in proportion to the square of CRL. The surface area of CP and pSP-IZ approached that of the total tissue at the end of the pSP stage. Volume of each layer increased in proportion to the cube of CRL. pSP-IZ and CP constituted over 50% of the total tissue in volume at the end of the pSP stages. We could visualize the growth of pSP-IZ in 3D and quantify it during pSP stage. Our approach allowed us to observe the process of rapid expansion of pSP-IZ from the midlateral regions of the cerebral wall, which subsequently becomes the insula.
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http://dx.doi.org/10.1111/joa.13488DOI Listing
June 2021

The development of the tensor vastus intermedius during the human embryonic period and its clinical implications.

J Anat 2021 May 24. Epub 2021 May 24.

Congenital Anomaly Research Center, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

The tensor vastus intermedius (TVI) is a newly discovered muscle located in the anterolateral thigh area and is considered the fifth component of the quadriceps femoris muscle. There have been several papers describing its anatomical and morphological features in detail; however, many features of this muscle, such as its ontology or kinetic functions, remain unknown. The purpose of this study was to determine the initial appearance of the TVI muscle in human embryonic development and to investigate its growth and development. Histological observations were performed on 30 lower limbs of 15 human embryos from Carnegie stage (CS) 21, 22, and 23 (with crown-rump length ranging from 18.7 to 28.7 mm). Myocyte clusters of the TVI were observed between the vastus lateralis and intermedius muscles in 7 out of 10 limbs in CS 22, indicating that the TVI arises during this stage. In CS 23, the TVI was clearly present in all specimens except one. However, neither the aponeurosis nor the tendonous structure of the TVI were observed in these embryonic stages. Formation of the conventional four components of the quadriceps muscle is completed within CS 21; therefore, our results suggest that the TVI is the last element to develop in the quadriceps femoris complex. It is posited that after the embryonic period, the TVI continues to grow, while forming the tendinous structure toward the patella and receiving vascular supply from certain vascular branches. The clinical significance of these findings is that orthopedists and plastic surgeons who perform surgical procedures within the anterolateral thigh (ALT) area should be aware of the anatomy and development of the TVI in order to reduce surgical complications. Our present research aims to contribute to a deeper understanding of the morphogenesis of the TVI and the other femoral extensor muscles.
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http://dx.doi.org/10.1111/joa.13453DOI Listing
May 2021

A 3D analysis of growth trajectory and integration during early human prenatal facial growth.

Sci Rep 2021 Mar 25;11(1):6867. Epub 2021 Mar 25.

Department of Plastic and Reconstructive Surgery, Kyoto University Graduate School of Medicine, 54 Kawahara-cho, Shogoin, Sakyo-ku, Kyoto, 606-8507, Japan.

Significant shape changes in the human facial skeleton occur in the early prenatal period, and understanding this process is critical for studying a myriad of congenital facial anomalies. However, quantifying and visualizing human fetal facial growth has been challenging. Here, we applied quantitative geometric morphometrics (GM) to high-resolution magnetic resonance images of human embryo and fetuses, to comprehensively analyze facial growth. We utilized non-linear growth estimation and GM methods to assess integrated epigenetic growth between masticatory muscles and associated bones. Our results show that the growth trajectory of the human face in the early prenatal period follows a curved line with three flexion points. Significant antero-posterior development occurs early, resulting in a shift from a mandibular prognathic to relatively orthognathic appearance, followed by expansion in the lateral direction. Furthermore, during this time, the development of the zygoma and the mandibular ramus is closely integrated with the masseter muscle.
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http://dx.doi.org/10.1038/s41598-021-85543-5DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7994314PMC
March 2021

Morphology and morphometry of the human early foetal brain: A three-dimensional analysis.

J Anat 2021 08 23;239(2):498-516. Epub 2021 Mar 23.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Morphometric analyses in the early foetal phase (9-13 postconceptional week) are critical for evaluating normal brain growth. In this study, we assessed sequential morphological and morphometric changes in the foetal brain during this period using high-resolution T1-weighted magnetic resonance imaging (MRI) scans from 21 samples preserved at Kyoto University. MRI sectional views (coronal, mid-sagittal, and horizontal sections) and 3D reconstructions of the whole brain revealed sequential changes in its external morphology and internal structures. The cerebrum's gross external view, lateral ventricle and choroid plexus, cerebral wall, basal ganglia and thalamus, and corpus callosum were assessed. The development of the cerebral cortex, white matter microstructure, and basal ganglia can be well-characterized using MRI scans. The insula became apparent and deeply impressed as brain growth progressed. A thick, densely packed cellular ventricular/subventricular zone and ganglionic eminence became apparent at high signal intensity. We detected the emergence of important landmarks which may be candidates in the subdivision processes during the early foetal period; the corpus callosum was first detected in the sample with crown-rump length (CRL) 62 mm. A primary sulcus on the medial part of the cortex (cingulate sulcus) was observed in the sample with CRL 114 mm. In the cerebellum, the hemispheres, posterolateral fissure, union of the cerebellar halves, and definition of the vermis were observed in the sample with CRL 43.5 mm, alongside the appearance of a primary fissure in the sample with CRL 56 mm and the prepyramidal fissure in the sample with CRL 75 mm. The volumetric, linear, and angle measurements revealed the comprehensive and regional development, growth, and differentiation of brain structures during the early foetal phase. The early foetal period was neither morphologically nor morphometrically uniform. The cerebral proportion (length/height) and the angle of cerebrum to the standard line at the lateral view of the cerebrum, which may reflect the growth and C-shape formation of the cerebrum, may be a candidate for subdividing the early foetal period. Future precise analyses must establish a staging system for the brain during the early foetal period. This study provides insights into brain structure, allowing for a correlation with functional maturation and facilitating the early detection of brain damage and abnormal development.
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http://dx.doi.org/10.1111/joa.13433DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC8273585PMC
August 2021

Bronchial tree of the human embryo: Categorization of the branching mode as monopodial and dipodial.

PLoS One 2021 15;16(1):e0245558. Epub 2021 Jan 15.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Some human organs are composed of bifurcated structures. Two simple branching modes-monopodial and dipodial-have been proposed. With monopodial branching, child branches extend from the sidewall of the parent branch. With dipodial branching, the tip of the bronchus bifurcates. However, the branching modes of the human bronchial tree have not been elucidated precisely. A total of 48 samples between Carnegie stage (CS) 15 and CS23 belonging to the Kyoto Collection were used to acquire imaging data with phase-contrast X-ray computed tomography. Bronchial trees of all samples were three-dimensionally reconstructed from the image data. We analyzed the lobar bronchus, segmental bronchus, and subsegmental bronchus. After calculating each bronchus length, we categorized the branching mode of the analyzed bronchi based on whether the parent bronchus was divided after generation of the analyzed bronchi. All lobar bronchi were formed with monopodial branching. Twenty-five bifurcations were analyzed to categorize the branching mode of the segmental and subsegmental bronchi; 22 bifurcations were categorized as monopodial branching, two bifurcations were not categorized as any branching pattern, and the only lingular bronchus that bifurcated from the left superior lobar bronchus was categorized as dipodial branching. The left superior lobar bronchus did not shorten during the period from CS17 or CS18, when the child branch was generated, to CS23. All analyzed bronchi that could be categorized, except for one, were categorized as monopodial branching. The branching modes of the lobar bronchus and segmental bronchus were similar in the mouse lung and human lung; however, the modes of the subsegmental bronchi were different. Furthermore, remodeling, such as shrinkage of the bronchus, was not observed during the analysis period. Our three-dimensional reconstructions allowed precise calculation of the bronchus length, thereby improving the knowledge of branching morphogenesis in the human embryonic lung.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0245558PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7810312PMC
June 2021

Development of Helical Myofiber Tracts in the Human Fetal Heart: Analysis of Myocardial Fiber Formation in the Left Ventricle From the Late Human Embryonic Period Using Diffusion Tensor Magnetic Resonance Imaging.

J Am Heart Assoc 2020 10 30;9(19):e016422. Epub 2020 Sep 30.

Human Health Science Graduate School of Medicine Kyoto University Kyoto Japan.

Background Detection of the fiber orientation pattern of the myocardium using diffusion tensor magnetic resonance imaging lags ≈12 weeks of gestational age (WGA) behind fetal myocardial remodeling with invasion by the developing coronary vasculature (8 WGA). We aimed to use diffusion tensor magnetic resonance imaging tractography to characterize the evolution of fiber architecture in the developing human heart from the later embryonic period. Methods and Results Twenty human specimens (8-24 WGA) from the Kyoto Collection of Human Embryos and Fetuses, including specimens from the embryonic period (Carnegie stages 20-23), were used. Diffusion tensor magnetic resonance imaging data were acquired with a 7T magnetic resonance system. Fractional anisotropy and helix angle were calculated using standard definitions. In all samples, the fibers ran helically in an organized pattern in both the left and right ventricles. A smooth transmural change in helix angle values (from positive to negative) was detected in all 16 directions of the ventricles. This feature was observed in almost all small (Carnegie stage 23) and large samples. A higher fractional anisotropy value was detected at the outer side of the anterior wall and septum at Carnegie stage 20 to 22, which spread around the ventricular wall at Carnegie stage 23 and in the early fetal samples (11-12 WGA). The fractional anisotropy value of the left ventricular walls decreased in samples with ≥13 WGA, which remained low (≈0.09) in larger samples. Conclusions From the human late embryonic period (from 8 WGA), the helix angle arrangement of the myocardium is comparable to that of the adult, indicating that the myocardial structure blueprint, organization, and integrity are already formed.
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http://dx.doi.org/10.1161/JAHA.120.016422DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7792405PMC
October 2020

Shoulder girdle formation and positioning during embryonic and early fetal human development.

PLoS One 2020 11;15(9):e0238225. Epub 2020 Sep 11.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Positional information on the shoulder girdle (the clavicle and scapula) is important for a better understanding of the function of the upper limb in the locomotive system as well as its associated disease pathogenesis. However, such data are limited except for information on the axial position of the scapula. Here, we describe a three-dimensional reconstruction of the shoulder girdle including the clavicle and scapula, and its relationship to different landmarks in the body. Thirty-six human fetal specimens (crown-rump length range: 7.6-225 mm) from the Kyoto Collection were used for this study. The morphogenesis and three-dimensional position of the shoulder girdle were analyzed with phase-contrast X-ray computed tomography and magnetic resonance imaging. We first detected the scapula body along with the coracoid and humeral head at Carnegie stage 18; however, the connection between the body and coracoid was not confirmed at this stage. During development, all landmarks on the shoulder girdle remained at the same axial position except for the inferior angle, which implies that the scapula enlarged in the caudal direction and reached the adult axial position in the fetal period. The scapula body was rotated internally and in the upward direction at the initiation of morphogenesis, but in the fetal period the scapula body was different than that in the adult position. The shoulder girdle was located at the ventral side of the vertebrae at the time of initial morphogenesis, but changed its position to the lateral side of the vertebrae in the late embryonic and fetal periods. Such a unique position of the shoulder girdle may contribute to the stage-specific posture of the upper limb. Adequate internal and upward rotation of the scapula could help in reducing the shoulder width, thereby facilitating childbirth. The data presented in this study can be used as normal morphometric references for shoulder girdle evaluations in the embryonic and fetal periods.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0238225PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7485900PMC
October 2020

Nascent nephrons during human embryonic development: Spatial distribution and relationship with urinary collecting system.

J Anat 2021 02 5;238(2):455-466. Epub 2020 Sep 5.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

The two major components of the metanephros, the urinary collecting system (UCS) and nephron, have different developmental courses. Nephron numbers vary widely between species and individuals and are determined during fetal development. Furthermore, the development of nascent nephrons may contribute to the expansion of the proximal part of the UCS. This study investigated the distribution of nascent nephrons and their interrelationship with UCS branches during human embryogenesis. We obtained samples from 31 human embryos between Carnegie stages (CSs) 19 and 23 from the Kyoto Collection at the Congenital Anomaly Research Center of Kyoto University in Japan. Serial histological sections of the metanephros with the UCS were digitalized and computationally reconstructed for morphological and quantitative analyses. The three-dimensional (3D) coordinates for the positions of all UCS branch points, end points, attachment points to nascent nephrons (APs), and renal corpuscles (RCs) were recorded and related to the developmental phase. Phases were categorized from phase 1 to phase 5 according to the histological analysis. The UCS branching continued until RCs first appeared (at CS19). End branches with attached nascent nephrons (EB-AP[+]) were observed after CS19 during the fifth generation or higher during the embryonic period. The range of end branch and EB-AP(+) generation numbers was broad, and the number of RCs increased with the embryonic stage, reaching 273.8 ± 104.2 at CS23. The number of RCs connected to the UCS exceeded the number not connected to the UCS by CS23. The 3D reconstructions revealed RCs to be distributed around end branches, close to the surface of the metanephros. The RCs connected to the UCS were located away from the surface. The APs remained near the end point, whereas connecting ducts that become renal tubules were found to elongate with maturation of the RCs. Nascent nephrons in RC phases 3-5 were preferentially attached to the end branches at CS22 and CS23. The mean generation number of EB-AP(-) was higher than that of EB-AP(+) in 19 of 22 metanephros and was statistically significant for eight metanephros at CS22 and CS23. The ratio of the deviated branching pattern was almost constant (29%). The ratio of the even branching pattern with EB-AP(+) and EB-AP(+) to the total even branching pattern increased with CS (9.2% at CS21, 19.2% at CS22, and 45.4% at CS23). Our data suggest the following: EB-AP(+) may not branch further at the tip (i.e., by tip splitting), but branching beneath the AP (lateral branching) continues throughout the embryonic stages. Our study provides valuable data that can further the understanding of the interactions between the UCS and nascent nephrons during human embryogenesis.
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http://dx.doi.org/10.1111/joa.13308DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7812128PMC
February 2021

Gait-combined transcranial alternating current stimulation modulates cortical control of muscle activities during gait.

Eur J Neurosci 2020 12 9;52(12):4791-4802. Epub 2020 Aug 9.

Department of Physical Therapy, Human Health Sciences, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Non-invasive brain stimulation has been of interest as a therapeutic tool to modulate cortical excitability. However, there is little evidence that oscillatory brain stimulation can modulate the cortical control of muscle activities during gait, which can be assessed using coherence analysis of paired surface electromyographic (EMG) recordings. This study aimed to investigate the effects of gait-combined transcranial alternating current stimulation (tACS) at the gait cycle frequency on the cortical control of muscle activities during gait using EMG-EMG coherence analysis. Fourteen healthy young adults participated in this study. All participants underwent 2 test conditions (real tACS and sham stimulation over the leg area of the primary motor cortex during 10-min treadmill walking). The average peak-to-peak amplitudes of the motor evoked potentials (MEPs) from the tibialis anterior (TA) and lateral gastrocnemius muscles in the sitting position and EMG-EMG coherences in the TA muscle, triceps surae muscles, quadriceps muscles, and hamstring muscles during gait were measured before and after stimulation. Entrainment effect was significantly higher during real tACS than during sham stimulation. After real tACS, the MEP amplitude and beta band (13-33 Hz) coherence area increased in the TA muscle. The change in MEP amplitude from the TA muscle was positively correlated with the change in beta band coherence area in the TA muscle. Gait-combined tACS can modulate the strength of descending neural drive to TA motoneurons during gait. This suggests that oscillatory brain stimulation is a useful therapeutic tool to modulate the cortical control of muscle activities during gait.
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http://dx.doi.org/10.1111/ejn.14919DOI Listing
December 2020

Gait improvements by assisting hip movements with the robot in children with cerebral palsy: a pilot randomized controlled trial.

J Neuroeng Rehabil 2020 07 3;17(1):87. Epub 2020 Jul 3.

Department of Physical Therapy, Human Health Sciences, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Background: Recently, rehabilitation robots are expected to improve the gait of cerebral palsy (CP) children. However, only few previous studies have reported the kinematic and kinetic changes by using wearable exoskeleton robots. The aim of this study was to investigate the change in gait parameters in CP children by training with the wearable robot-assisted gait training.

Methods: 10 spastic CP children with Gross Motor Function Classification Scale levels I-III completed a sham-controlled crossover randomized trial. Robot-assisted gait training (RAGT) and non-assisted gait training (NAGT) were performed on the treadmill with the Honda Walking Assist (HWA) in two different days. To examine the carry-over effect from treadmill walking to overground walking, participants also performed 5.5 m overground-walks without the HWA before and after treadmill training (pre- and post-trial). During treadmill walking, peak of both hip and knee angles were measured. Also, we calculated the limb symmetry of hip range of motion. In addition, gait speed and ground reaction force were measured in overground trials.

Results: The maximum hip angle on the limb with fewer hip movements, which was defined as the affected limb, showed a significant interaction between ASSIST (RAGT and NAGT) and TIME (pre- and post-trial) (p < 0.05). Limb symmetry significantly improved after RAGT (p < 0.05), but not in NAGT. Furthermore, the affected limb showed a significant increase in the positive peak of the anterior-posterior ground reaction force during 70-100% of the gait cycle (p < 0.05). However, there was no change in gait speed.

Conclusion: By assisting the both hip movements with the HWA, maximum hip flexion and extension angle of the affected limb improved. Also, limb symmetry and propulsion force of the affected limb improved. Our results suggest that assisting both hip movements with the HWA might be an effective method for improving gait in CP children.

Trial Registration: UMIN-CTR, UMIN000030667. Registered 3 January 2018, https://upload.umin.ac.jp/cgi-open-bin/ctr_e/ctr_view.cgi?recptno=R000033737.
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http://dx.doi.org/10.1186/s12984-020-00712-3DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7333257PMC
July 2020

Immediate Effect on Ground Reaction Forces Induced by Step Training Based on Discrete Skill during Gait in Poststroke Individuals: A Pilot Study.

Rehabil Res Pract 2020 19;2020:2397374. Epub 2020 May 19.

Department of Physical Therapy, Human Health Sciences, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Methods: Twenty-two community-dwelling patients with chronic hemiplegia participated in this study. Eight participants performed only discrete-skill step training during the loading response phase, focusing on paretic hip extension movement (LR group). Another eight performed only discrete-skill step training during the preswing phase, focusing on paretic swing movement (PSw group). The remaining six were trained using both training methods, with at least 6 months in each group to washout the influence of previous training. Therefore, the final number of participants in each group was 14. The braking and propulsive forces of GRFs were measured during gait before and after 30 repetitions of the discrete-skill step training.

Results: Although both groups showed a significant increase in stride length, walking speed was increased only in the LR group. The PSw group showed an increase in braking forces of both sides without any change in propulsion. In the LR group, paretic braking impulse did not change, while nonparetic propulsion increased.

Conclusion: The discrete-skill step training during loading response phase induced an increase in nonparetic propulsion, resulting in increased walking speed. This study provides a clear understanding of immediate effects of the discrete-skill step training in patients with chronic stroke and helps improve interventions in long-term rehabilitation.
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http://dx.doi.org/10.1155/2020/2397374DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7254076PMC
May 2020

Perinatal benign hypophosphatasia antenatally diagnosed through measurements of parental serum alkaline phosphatase and ultrasonography.

Congenit Anom (Kyoto) 2020 Nov 16;60(6):199-200. Epub 2020 Jun 16.

Clinical Genetics Unit, Kyoto University Hospital, Kyoto, Japan.

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http://dx.doi.org/10.1111/cga.12374DOI Listing
November 2020

Classification of the "human tail": Correlation between position, associated anomalies, and causes.

Clin Anat 2020 Sep 4;33(6):929-942. Epub 2020 Jun 4.

Congenital Anomaly Research Center, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Introduction: Numerous case reports have indicated that the "human tail" is not always a harmless protrusion but can be associated with anomalies such as occult dysraphic malformations. However, the definition and classification of this anomaly have not been discussed. A prevailing hypothesis is that the "human tail" is a residual embryonic tail. Herein, we attempted to classify and define the human tail and investigate the frequency of this anomaly.

Materials And Methods: We first defined the human tail as a protrusion on the dorsal side of the lumbar, sacrococcygeal, and para-anal regions identified after birth. We collected case reports written in English, Japanese, French, German, and Italian that were published from the 1880s to the present.

Results: We discovered two important findings: (a) the cause of this anomaly may differ even though the "tails" resemble each other closely in appearance and (b) its position tends to be correlated with the type of anomaly and its associated cause. We propose a new classification of the human tail based on these findings.

Conclusion: Our classification may facilitate more accurate treatment and precise case descriptions of the human tail.
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http://dx.doi.org/10.1002/ca.23609DOI Listing
September 2020

The bronchial tree of the human embryo: an analysis of variations in the bronchial segments.

J Anat 2020 08 13;237(2):311-322. Epub 2020 Apr 13.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

A classical study has revealed the general growth of the bronchial tree and its variations up to Carnegie stage (CS) 19. In the present study, we extended the morphological analysis CS by CS until the end of the embryonic period (CS23). A total of 48 samples between CS15 and CS23 belonging to the Kyoto Collection were used to acquire imaging data by performing phase-contrast X-ray computed tomography. Three-dimensionally reconstructed bronchial trees revealed the timeline of morphogenesis during the embryonic period. Structures of the trachea and lobar bronchus showed no individual difference during the analyzed stages. The right superior lobar bronchus was formed after the generation of both the right middle lobar bronchus and the left superior lobar bronchus. The speed of formation of the segmental bronchi, sub-segmental bronchi, and further generation seemed to vary among individual samples. The distribution of the end-branch generation among five lobes was significantly different. The median branching generation value in the right middle lobe was significantly low compared with that of the other four lobes, whereas that of the right inferior lobe was significantly larger than that of both the right and left superior lobes. Variations found between CS20 and CS23 were all described in the human adult lung, indicating that variation in the bronchial tree may well arise during the embryonic period and continue throughout life. The data provided may contribute to a better understanding of bronchial tree formation during the human embryonic period.
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http://dx.doi.org/10.1111/joa.13199DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7369191PMC
August 2020

Three-dimensional morphogenesis of the omental bursa from four recesses in staged human embryos.

J Anat 2020 07 16;237(1):166-175. Epub 2020 Feb 16.

Department of Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

The omental bursa (OB) is a complex upper abdominal structure in adults. Its morphological complexity stems from embryonic development. Approximately 200 years ago, the first theory regarding OB development was reported, describing that the OB developed from changes in the position of the stomach and its dorsal mesentery. Thereafter, the second theory reported that the OB originated from three recesses: the right pneumato-enteric recess (rPER), hepato-enteric recess (HER), and pancreatico-enteric recess (PaER). However, the first theory, focusing on the rotation of the stomach, is still described in certain modern embryology textbooks. These two coexisting embryological theories deter the understanding of the anatomical complexity of the OB. This study aimed to unify these two theories into realistic illustrations. Approximately 10 samples per stage among Carnegie stage (CS) 13 and CS21 were microscopically observed and histological serial sections of the representative samples were aligned using the new automatic alignment method. The aligned images were segmented computationally and reconstructed into 3D models. The rPER and the HER encompassed the right half circumference of the esophagus and the stomach at CS13 and CS14, the PaER spread dorsal to the stomach and formed a discoid shape at CS15 and CS16, the infracardiac bursa (ICB) was separated by the diaphragm at CS17 and CS18, and the fourth recess, which we called the greater omental recess (GOR), extended caudally from the PaER among CS19 and CS21. The present results indicate that the fourth recess is also the origin of the OB. These two theories over 200 years can be generally unified into one embryological description indicating a new recess as the origin of the OB.
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http://dx.doi.org/10.1111/joa.13174DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7309287PMC
July 2020

Relationship between rectal abdominis muscle position and physiological umbilical herniation and return: A morphological and morphometric study.

Anat Rec (Hoboken) 2020 12 15;303(12):3044-3051. Epub 2020 Jan 15.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

The herniation of the intestinal loop (IL) in the extraembryonic coelom and its return to abdominal cavity is in parallel with the formation of the rectal abdominis muscle (RAM). Using high-resolution magnetic resonance imaging data of human fetuses (n = 19, CRL22-69 mm; stored at Kyoto Collection), this study aimed to analyze the relationship between the development of RAM and phase of IL herniation. The RAM runs at the lateral part of the abdominal wall in the small samples in the herniation phase. The position was shifted to the midline area in the larger samples in the herniation phase. According to fetal growth, the caudal ends of the muscles extended along the umbilical ring towards the pubis, though the caudal part of the RAMs were thin and faint in most of the samples. Length measurements related with the growth of the abdominal wall including RAM and abdominal circumference showed positive correlation with fetal growth. On the contrary, diastasis of RAMs and the width and area of the umbilical ring were almost constant according to fetal growth. Such morphometric value showed no obvious changes regardless of the phases of herniation. The ratio of the width and diastasis of the RAMs to the circumference was decreased, indicating that the closure of the ventral body wall was influenced by growth differences. The present data indicate that the formation of the abdominal wall including RAM is independent of the phase of IL herniation, whether in the extraembryonic coelom or in the abdominal cavity.
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http://dx.doi.org/10.1002/ar.24358DOI Listing
December 2020

Gait-synchronized oscillatory brain stimulation modulates common neural drives to ankle muscles in patients after stroke: A pilot study.

Neurosci Res 2020 Jul 11;156:256-264. Epub 2019 Nov 11.

Department of Physical Therapy, Human Health Sciences, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

The present study aimed to investigate the long-term effects of gait intervention with transcranial alternating current stimulation (tACS) synchronized with gait cycle frequency on the cortical control of muscle activity during gait, using coherence analyses, in patients after stroke. Eight chronic post-stroke patients participated in a single-blinded crossover study, and 7 patients completed the long-term intervention. Each patient received tACS over the primary motor cortex foot area on the affected side, which was synchronized with individual gait cycle frequency, and sham stimulation during treadmill gait in a random order. Electrical neuromuscular stimulation was used to assist the paretic ankle movement in both conditions. After gait intervention with tACS, beta band (15-35 Hz) coherence, which is considered to have a cortical origin, significantly increased in the paretic tibialis anterior (TA) muscle during 6-min of over-ground gait. The change in beta band coherence in the paretic TA muscle was positively correlated with the change in gait distance. These results indicate that gait intervention with tACS synchronized with gait cycle frequency may induce gait-specific plasticity that modulates the common neural drive to the TA motoneurons on the paretic side during gait and leads to changes in gait function in patients after stroke.
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http://dx.doi.org/10.1016/j.neures.2019.11.001DOI Listing
July 2020

Human embryonic ribs all progress through common morphological forms irrespective of their position on the axis.

Dev Dyn 2019 12 6;248(12):1257-1263. Epub 2019 Sep 6.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Background: We aimed to analyze the morphogenesis of all ribs from 1st to 12th rib pairs plus vertebrae to compare their differences and features according to the position along the cranial-caudal axis during the human embryonic period.

Results: Rib pair formation was analyzed using high-resolution digitalized imaging data (n = 29) between Carnegie stage (CS) 18 and CS23 (corresponding to ED13-14 in mouse; HH29-35 in chick). A total of 348 rib pairs, from 1st to 12th rib pairs of each sample were subjected to Procrustes and principal component (PC) analyses. PC1 and PC2 accounted for 76.3% and 16.4% (total 92.7%) of the total variance, respectively, indicating that two components mainly accounted for the change in shape. The distribution of PC1 and PC2 values for each rib showed a "fishhook-like shape" upon fitting to a quartic equation. PC1 and PC2 value position for each rib pair moved along the fitted curve according to the development. Thus, the change in PC1 and PC2 could be expressed by a single parameter using a fitted curve as a linear scale for shape.

Conclusion: Human embryonic ribs all progress through common morphological forms irrespective of their position on the axis.
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http://dx.doi.org/10.1002/dvdy.107DOI Listing
December 2019

Morphogenesis of the femur at different stages of normal human development.

PLoS One 2019 23;14(8):e0221569. Epub 2019 Aug 23.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

The present study aimed to better characterize the morphogenesis of the femur from the embryonic to the early fetal periods. Sixty-two human fetal specimens (crown-rump length [CRL] range: 11.4-185 mm) from the Kyoto Collection were used for this study. The morphogenesis and internal differentiation process of the femur were analyzed in 3D using phase-contrast X-ray computed tomography and magnetic resonance imaging. The cartilaginous femur was first observed at Carnegie stage 18. Major anatomical landmarks were formed prior to the initiation of ossification at the center of the diaphysis (CRL, 40 mm), as described by Bardeen. The region with very high signal intensity (phase 5 according to Streeter's classification; i.e., area described as cartilage disintegration) emerged at the center of the diaphysis, which split the region with slightly low signal intensity (phase 4; i.e., cartilage cells of maximum size) in fetuses with a CRL of 40.0 mm. The phase 4 and phase 5 regions became confined to the metaphysis, which might become the epiphyseal cartilage plate. Femur length and ossified shaft length (OSL) showed a strong positive correlation with CRL. The OSL-to-femur length ratio rapidly increased in fetuses with CRL between 40 and 75 mm, which became moderately increased in fetuses with a CRL of ≥75 mm. Cartilage canal invasion occurred earlier at the proximal epiphysis (CRL, 62 mm) than at the distal epiphysis (CRL, 75 mm). Morphometry and Procrustes analysis indicated that changes in the femur shape after ossification were limited, which were mainly detected at the time of initial ossification and shortly after that. In contrast, femoral neck anteversion and torsion of the femoral head continuously changed during the fetal period. Our data could aid in understanding the morphogenesis of the femur and in differentiating normal and abnormal development during the early fetal period.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0221569PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6707600PMC
March 2020

Rib Cage Morphogenesis in the Human Embryo: A Detailed Three-Dimensional Analysis.

Anat Rec (Hoboken) 2019 12 25;302(12):2211-2223. Epub 2019 Jul 25.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Formation of the skeletal structure in the human embryo has important consequences in terms of support, protection, and function of organs and other systems. We aimed to describe the formation of the rib cage during the embryonic period, in order to detect prominent features and identify the possible factors affecting rib cage morphology. We employed high-resolution digitized imaging data (n = 34) obtained in human embryos with Carnegie stage (CS) between 17 and 23. The rib cage became detectable as cartilage formation at CS17, expanding outward from the dorsal side of the chest-abdominal region. Ribs elongated progressively to surround the chest, differentiating into the upper and lower rib cage regions by CS20. The ends of corresponding ribs in the upper region elongated toward each other, leading to their joining and sternum formation between CS21 and CS23, while the lower region of the rib cage remained widely open. The rib cage area with the largest width shifted from the 5th rib pair at CS17 to the 9th pair at CS23. The depth of the rib cage was similar across the upper region at CS17, with the major portion remaining in the middle part after CS20. The heart was located beneath the rib pairs providing the largest depth, while the liver was located beneath the rib pairs providing the largest width. Formation of the sternum, development of spinal kyphosis, and organization of larger internal organs within the thoracic and abdominal cavity are possible factors affecting rib cage morphology. Anat Rec, 302:2211-2223, 2019. © 2019 American Association for Anatomy.
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http://dx.doi.org/10.1002/ar.24226DOI Listing
December 2019

Position of the cecum in the extraembryonic and abdominal coelom in the early fetal period.

Congenit Anom (Kyoto) 2020 May 23;60(3):87-88. Epub 2019 Jul 23.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

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http://dx.doi.org/10.1111/cga.12348DOI Listing
May 2020

Level set distribution model of nested structures using logarithmic transformation.

Med Image Anal 2019 08 10;56:1-10. Epub 2019 May 10.

Tokyo University of Agriculture and Technology, 2-24-16 Nakacho, Koganei, Tokyo 184-8588, Japan.

In this study, we propose a method for constructing a multishape statistical shape model (SSM) for nested structures such that each is a subset or superset of another. The proposed method has potential application to any pair of shapes with an inclusive relationship. These types of shapes are often found in anatomy, such as the brain surface and ventricles. The main contribution of this paper is to introduce a new shape representation called log-transformed level set function (LT-LSF), which has a vector space structure that preserves the correct inclusive relationship of the nested shape. In addition, our method is applicable to an arbitrary number of nested shapes. We demonstrate the effectiveness of the proposed shape representation by modeling the anatomy of human embryos, including the brain, ventricles, and choroid plexus volumes. The performance of the SSM was evaluated in terms of generalization and specificity ability. Additionally, we measured leakage criteria to assess the ability to preserve inclusive relationships. A quantitative comparison of our SSM with conventional multishape SSMs demonstrates the superiority of the proposed method.
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http://dx.doi.org/10.1016/j.media.2019.05.003DOI Listing
August 2019

Vesicular swelling in the cervical region with lymph sac formation in human embryos.

Congenit Anom (Kyoto) 2019 May 18. Epub 2019 May 18.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

Vesicular swelling in the cervical region (VSC) is occasionally observed among human embryos around Carnegie stage (CS) 21. However, its mechanism and significance in fetal development are unclear. The present study aimed to analyze the relation of development of VSC with jugular lymph sac (JLS) formation. Serial histological sections that were digitalized from 14 embryos at CS20 and CS21 stored at the Kyoto Collection were used for the analysis. Subcutaneous edema and enlargement of the subarachnoid space were found to cause VSC. No obvious abnormalities in cranial regions that may be related to the VSC were detected on histological sections. Three-dimensional reconstructions revealed the following: (a) the JLS was located bilaterally at the levels between the first and fourth cervical vertebrae; (b) the JLS was pyramidal in shape; and (c) no severe deformity and/or malformation was found in all samples. The JLS was not connected to the subcutaneous tissue and subarachnoid space in all samples. The mean volume of the JLS increased nine-times from CS20 (0.02 mm in VSC [-] group) to CS21 (0.18 mm in VSC [-] group). The mean volume of the JLS was comparable between the VSC [-] and VSC (+) groups at both CS20 and CS21. A moderate correlation was observed between VSCd and the mean volume of the JLS in both groups at CS20 (R = 0.75) and CS21 (R = 0.56). In conclusion, the dynamics of the lymphatic system at the cervical region may contribute to VSC observed around CS21. © 2019 Japanese Teratology Society.
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http://dx.doi.org/10.1111/cga.12339DOI Listing
May 2019

Relationship Between Physiological Umbilical Herniation and Liver Morphogenesis During the Human Embryonic Period: A Morphological and Morphometric Study.

Anat Rec (Hoboken) 2019 11 29;302(11):1968-1976. Epub 2019 May 29.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

It is widely hypothesized that physiological umbilical herniation (PUH) in humans occurs, because the liver occupies a large space in the abdominal cavity, which pushes the intestine into the extraembryonic coelom during the embryonic period. We have recently shown the presence of the intestinal loop in the extraembryonic coelom in embryos with liver malformation. Here, we analyzed the relationship between the liver and the PUH at Carnegie stage 21 of four embryos with liver malformation, including two with hypogenesis (HY1, HY2) and two with agenesis (AG1, AG2), using phase-contrast X-ray computed tomography and compared them with two control embryos. The intestinal loop morphology in the malformed embryos differed from that in the control embryos, except in HY1. The length of the digestive tract in the extraembryonic coelom of the embryos with liver malformation was similar to or longer than that of the controls. The rate of intestinal loop lengthening in the extraembryonic coelom compared with that of the total digestive tract in all embryos with liver malformation was similar to or higher than that of the controls. The estimated total abdominal cavity volume in the embryos with liver malformation was considerably smaller than that of the controls, while the intestinal volume was similar. The cardia and proximal portion of the pancreas connecting to the duodenum were located at almost identical positions in all the embryos, whereas other parts of the upper digestive tract deviated in the embryos with abnormal livers. Thus, our results provided evidence that PUH occurred independently of liver volume. Anat Rec, 302:1968-1976, 2019. © 2019 American Association for Anatomy.
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http://dx.doi.org/10.1002/ar.24149DOI Listing
November 2019

Analysis of facial skeletal asymmetry during foetal development using μCT imaging.

Orthod Craniofac Res 2019 May;22 Suppl 1:199-206

Oral Health Sciences, University of British Columbia, Vancouver, British Columbia, Canada.

Objectives: Asymmetry has been noted in the human craniofacial region in several pathological conditional and growth abnormalities, often with a directional predilection. Physiological asymmetry has also been reported in normal adults and adolescents, with certain regions of the cranioskeleton, such as the mandible, displaying prevalent asymmetry. However, the timing at which such asymmetries arise has not been evaluated. The objectives of this study were to assess the degree of asymmetry in facial bones during the foetal stages of human development.

Material And Methods: Twenty-one preserved conceptuses from the Congenital Anomaly Research Center at Kyoto University, between ages 15 and 20 weeks of gestation, were studied using high-resolution μCT imaging. Asymmetry analysis was performed on digitally segmented facial bone pairs, using geometric morphometric (GM) approaches as well as adapted deformation-based asymmetry (DBA) methods.

Results: GM analysis revealed that the developing facial bones display statistically significant fluctuating and directional asymmetry. DBA methods suggest that the magnitude of asymmetry in facial bones is low and does not appear to be correlated to the estimate of overall size of conceptus. Additionally, the patterns of asymmetry are highly variable between individual specimens.

Conclusions: The developing foetal facial skeleton displays variable patterns of low magnitude asymmetry. GM and DBA methods offer unique advantages to assess facial asymmetry quantitatively and qualitatively.
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http://dx.doi.org/10.1111/ocr.12304DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6512839PMC
May 2019

Revisiting the infracardiac bursa using multimodal methods: topographic anatomy for surgery of the esophagogastric junction.

J Anat 2019 07 12;235(1):88-95. Epub 2019 Apr 12.

Department of Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

In embryology, the infracardiac bursa (ICB) is a well-known derivative separated from the omental bursa. During surgeries around the esophagogastric junction (EGJ), surgeons often encounter a closed space considered to be equivalent to the ICB, but the macroscopic anatomy in adults is hardly known. This study aimed to revisit the ICB using multimodal methods to show its development from the embryonic to adult stage and clarify its persistence and topographic anatomy. Histological sections of 79 embryos from Carnegie stage (CS) 16 to 23 and magnetic resonance (MR) images of 39 fetuses were examined to study the embryological development of the ICB. Horizontal sections around the EGJ obtained from three adult cadavers were examined to determine the topographic anatomy and histology of the ICB. Further, 32 laparoscopic surgical videos before (n = 16) and after (n = 16) the start of this study were reviewed to confirm its remaining rate and topographic anatomy in surgery. The ICB was formed in 1 out of 10 CS17 samples, and in 8 out of 10 CS18 samples. Further, it was observed in all CS19-23 except one CS23 sample and in 25 (64%) out of 39 fetus samples. Three-dimensional reconstructed MR images of fetuses revealed that the ICB was located at the right alongside the esophagus and the cranial side of the diaphragmatic crus. In one adult cadaver, the caudal end of the ICB arose from the level of the esophageal hiatus and the cranial end reached up to the level of the pericardium. The inner surface cells of the space consisted of the mesothelium. In laparoscopic surgery, the ICB was identified in only 11 (69%) out of 16 surgeries before. However, subsequently we were able to identify the ICB reproducibly in 15 (94%) out of 16 surgeries. Thus, the ICB is the structure commonly remaining in almost all adults as a closed space located at the right alongside the esophagus and the cranial side of the diaphragmatic crus. It may be available as a useful landmark in surgery of the EGJ.
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http://dx.doi.org/10.1111/joa.12989DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6580070PMC
July 2019

Spatial Relationship Between the Metanephros and Adjacent Organs According to the Carnegie Stage of Development.

Anat Rec (Hoboken) 2019 11 18;302(11):1901-1915. Epub 2019 Mar 18.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, 606-8501, Japan.

The morphological changes in the metanephros and its spatial relationship to the adjacent organs was evaluated based on the Carnegie stages (CSs) from 14 through 23. The imaging modalities used included magnetic resonance imaging (N = 4), phase-contrast X-ray computed tomography (N = 11), and serial histological sections (N = 40), supplemented by three-dimensional image reconstruction. The orientation of the hilus of the metanephros changed significantly between CS17 (34.4 ± 13.7 degrees) and 18 (122.3 ± 38.1 degrees), with an increase in the number of branches of the urinary collecting system, from 1.61 ± 0.42 at CS17 to 3.20 ± 0.35 at CS18. This increase in the number of branches influenced the growth of the metanephros and the orientation of its hilus. The right and left metanephroses were in proximity throughout the embryonic period. The local maximum interpole distances were observed at CS18 (0.87 ± 0.11 mm for the upper and 0.50 ± 0.25 mm for the lower pole). Mesenchymal tissue was observed between the metanephros and iliac arteries, as well as between the right and left metanephros. Throughout development, the position of the lower pole of the metanephros remained adjacent to the aortic bifurcation. The position of the upper pole, referenced with respect to the aortic bifurcation, increased by >2.0 mm, reflecting the longitudinal growth of the metanephros. Our findings provide a detailed description of the morphogenesis of the metanephros and of its hilus, which might contribute to our understanding of congenital malformations and malpositions of the kidneys. Anat Rec, 302:1901-1915, 2019. © 2019 American Association for Anatomy.
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http://dx.doi.org/10.1002/ar.24103DOI Listing
November 2019

Critical Growth Processes for the Midfacial Morphogenesis in the Early Prenatal Period.

Cleft Palate Craniofac J 2019 09 17;56(8):1026-1037. Epub 2019 Feb 17.

1 Department of Plastic and Reconstructive Surgery, Kyoto University Graduate School of Medicine, Kyoto, Japan.

Background: Congenital midfacial hypoplasia often requires intensive treatments and is a typical condition for the Binder phenotype and syndromic craniosynostosis. The growth trait of the midfacial skeleton during the early fetal period has been assumed to be critical for such an anomaly. However, previous embryological studies using 2-dimensional analyses and specimens during the late fetal period have not been sufficient to reveal it.

Objective: To understand the morphogenesis of the midfacial skeleton in the early fetal period via 3-dimensional quantification of the growth trait and investigation of the developmental association between the growth centers and midface.

Methods: Magnetic resonance images were obtained from 60 human fetuses during the early fetal period. Three-dimensional shape changes in the craniofacial skeleton along growth were quantified and visualized using geometric morphometrics. Subsequently, the degree of development was computed. Furthermore, the developmental association between the growth centers and the midfacial skeleton was statistically investigated and visualized.

Results: The zygoma expanded drastically in the anterolateral dimension, and the lateral part of the maxilla developed forward until approximately 13 weeks of gestation. The growth centers such as the nasal septum and anterior portion of the sphenoid were highly associated with the forward growth of the midfacial skeleton (RV = 0.589; < .001).

Conclusions: The development of the midface, especially of the zygoma, before 13 weeks of gestation played an essential role in the midfacial development. Moreover, the growth centers had a strong association with midfacial forward growth before birth.
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http://dx.doi.org/10.1177/1055665619827189DOI Listing
September 2019

Return of the intestinal loop to the abdominal coelom after physiological umbilical herniation in the early fetal period.

J Anat 2019 04 25;234(4):456-464. Epub 2019 Jan 25.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

The intestine elongates during the early fetal period, herniates into the extraembryonic coelom, and subsequently returns to the abdominal coelom. The manner of herniation is well-known; however, the process by which the intestinal loop returns to the abdomen is not clear. Thus, the present study was designed to document and measure intestinal movements in the early fetal period in three dimensions to elucidate the intestinal loop return process. Magnetic resonance images from human fetuses whose intestinal loops herniated (herniated phase; n = 5) while returning to the abdominal coelom [transition phase; n = 3, crown-rump length (CRL)] 37, 41, and 43 mm] and those whose intestinal loops returned to the abdominal coelom normally (return phase; n = 12) were selected from the Kyoto Collection. Intestinal return began from proximal to distal in samples with CRL of 37 mm. Only the ileum ends were observed in the extraembryonic coelom in samples with CRLs of 41 and 43 mm, whereas the ceca were already located in the abdominal coeloms. The entire intestinal tract had returned to the abdominal coelom in samples with CRL > 43 mm. The intestinal length increased almost linearly with fetal growth irrespective of the phase (R  = 0.90). The ratio of the intestinal length in the extraembryonic coelom to the entire intestinal length was maximal in samples with CRLs of 32 mm (77%). This ratio rapidly decreased in three of the samples that were in the transition phase. The abdominal volumes increased exponentially (to the third power) during development. The intestinal volumes accounted for 33-41% of the abdominal volumes among samples in the herniated phase. The proportion of the intestine in the abdominal cavity increased, whereas that in the liver decreased, both without any break or plateau. The amount of space available for the intestine by the end of the transition phase was approximately 200 mm . The amount of space available for the intestine in the abdominal coelom appeared to be sufficient at the beginning of the return phase in samples with CRLs of approximately 43 mm compared with the maximum intestinal volume available for the extraembryonic coelom in the herniated phase, which was 25.8 mm in samples with CRLs of 32 mm. A rapid increase in the space available for the intestine in the abdominal coelom that exceeded the intestinal volume in the extraembryonic coelom generated an inward force, leading to a 'sucked back' mechanism acting as the driving force. The height of the hernia tip increased to 8.9 mm at a maximum fetal CRL of 37 mm. The height of the umbilical ring increased in a stepwise manner between the transition and return phases and its height in the return phase was comparable to or higher than that of the hernia tip during the herniation phase. We surmised that the space was generated in the aforementioned manner to accommodate the herniated portion of the intestine, much like the intestine wrapping into the abdominal coelom as the height of the umbilical ring increased.
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http://dx.doi.org/10.1111/joa.12940DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6422813PMC
April 2019

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

PLoS One 2018 7;13(9):e0203623. Epub 2018 Sep 7.

Human Health Science, Graduate School of Medicine, Kyoto University, Kyoto, Japan.

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.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0203623PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6128595PMC
February 2019
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