Journal of Pathology and Translational Medicine

Original Article

Tongue Growth during Prenatal Development in Korean Fetuses and Embryos: Soo Jeong Hong, Bong Geun Cha, Yeon Sook Kim, Suk Keun Lee, Je Geun Chi; J Pathol Transl Med. 2015;49(6):497-510. Published online October 16, 2015; DOI: https://doi.org/10.4132/jptm.2015.09.17

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Background
Prenatal tongue development may affect oral-craniofacial structures, but this muscular organ has rarely been investigated. Methods: In order to document the physiology of prenatal tongue growth, we histologically examined the facial and cranial base structures of 56 embryos and 106 fetuses. Results: In Streeter’s stages 13–14 (fertilization age [FA], 28 to 32 days), the tongue protruded into the stomodeal cavity from the retrohyoid space to the cartilaginous mesenchyme of the primitive cranial base, and in Streeter’s stage 15 (FA, 33 to 36 days), the tongue rapidly swelled and compressed the cranial base to initiate spheno-occipital synchondrosis and continued to swell laterally to occupy most of the stomodeal cavity in Streeter’s stage 16–17 (FA, 37 to 43 days). In Streeter’s stage 18–20 (FA, 44 to 51 days), the tongue was vertically positioned and filled the posterior nasopharyngeal space. As the growth of the mandible and maxilla advanced, the tongue was pulled down and protruded anteriorly to form the linguomandibular complex. Angulation between the anterior cranial base (ACB) and the posterior cranial base (PCB) was formed by the emerging tongue at FA 4 weeks and became constant at approximately 124°–126° from FA 6 weeks until birth, which was consistent with angulations measured on adult cephalograms. Conclusions: The early clockwise growth of the ACB to the maxillary plane became harmonious with the counter-clockwise growth of the PCB to the tongue axis during the early prenatal period. These observations suggest that human embryonic tongue growth affects ACB and PCB angulation, stimulates maxillary growth, and induces mandibular movement to achieve the essential functions of oral and maxillofacial structures.

Citations

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Case Reports

VATER Association: Three autopsy case reports with imusual defects.: Mi Ja Lee, Myeong Cherl Kook, Je G Chi; Korean J Pathol. 1995;29(5):678-683.

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Abstract: VATER association represents vertebral defects, anal atresia, tracheo-esophageal fistula with without esophageal atresia, renal defects and radial limb dysplasia. The probability of the simultaneous occurrence of any three of these defects is so unlikely that it suggests a sporadic non-random association. This non-random association appears to be related to some chromosomal anomalies, the caudal regression syndrome, mesodermal defects in early developmental period or the matemal use of sex hormones during embryogenesis. We report three autopsy cases of the VATER association that showed most of the known major and minor defects as well as an unusual concurrence of other defects, i.e., scoliosis, talipes varus, absent penis, urethral agenesis and stenosis, rectourethral fistula, rib anomaly, single umbilical artery, Meckel's diverticulum, diaphragmatic hemia, absent rectum, short neck, simian crease, low set ear, and hypoplastic lung.

Intraabdominal Heterotopic Thymus: Report of an autopsy case.: Hye Seung Han, Je Geun Chi; Korean J Pathol. 1996;30(11):1057-1059.

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Abstract PDF: Ectopic thymus results from the aberrant migration of thymic tissue and is mostly present in the mediastinum, the base of the skull, the tracheal bifurcation and the cervical region. We report the first case of intraabdominal heterotopic thymus incidentally detected and attached to the liver without associated anomalies. This fetus was sent to the Department without any clinical information. The fetus was small for gestational age, but had no external abnormalities. Each organ showed normal development except for the liver. The liver weighed 6 gm(normal 17.064+/-4.143 gm). Gray white heterotopic thymus was attached to the superior surface of the liver in the subdiaphragmatic area. It measured 1.1x0.6x0.5 cm. There was no diaphragmatic defect. The cervical thymic tissue near the thyroid was small and measured 0.2 gm(normal 0.927+/-0.485 gm). There was no thymic tissue in the anterior superior mediastinum. The histologic features of the heterotopic thymus were identical to the orthotopic thymus showing features appropriate for the gestational age. The origin of this subdiaphragmatic heterotopic thymus is speculated.

Original Articles

Prenatal Development of Eccrine Sweat Gland: Morphologic and Morphometric Analysis.: Nam Bok Cho, Tae Jin Lee, Je G Chi, Kye Yong Song; Korean J Pathol. 1997;31(2):121-134.

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Abstract PDF: To elucidate the developmental sequence of the eccrine sweat gland, a morphologic and a morphometric observation were done using developing human embryos and fetuses. Five embryos and sixty four fetuses from the 9th to the 38th week of the gestational age were studied. The skin was sampled in eight different areas, i.e., scalp, forehead, face, chest, abdomen, back, palm and sole. Routine histological sections were made for histological evaluation and morphometric analysis. The results obtained were as follows : The primordia of the eccrine sweat glands appeared first as regular undulation of the basal cells in the palm and the sole in the 13th week of getation. Subsequently, elongation and coiling of the cell cords were noted from the 16th to the 18th weeks. Intraductal lumen formation was first noted in the 20th week. Secretory segment of the eccrine sweat glands were noted from the distal part of the coiling intradermal sweat duct in the 22nd week of the gestational age. The eccrine sweat glands became fully developed by the 28th week of gestation and this included the clear cell, the dark cell and the myoepithelial cell. In the morphometric analysis, the number of eccrine epithelial buddings were decreased with aging and the highest were in the palm and the sole. The diameter of the eccrine sweat duct showed no significant change by gestational age or in the different sites observed. Straight and coiled eccrine sweat ducts or glands were lengthened into the deep reticular dermis and upper portion of the subcutaneous adipose tissue with an increase of the gestational age. The above results suggest that developmental stage and the number of eccrine glands of the skin in the fetal stage is different from other areas of the body, especially in the palm and the sole.

Expression of Cytokeratin 1, 10 and 14 in Fetal Skin.: Kye Yong Song, Sun Lee, Dong Hye Suh, Mi Kyung Kim, Hye Jung Min, Je G Chi; Korean J Pathol. 2001;35(3):226-231.

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Abstract PDF: BACKGROUND
During the fetal stage, the epidermis and adnexal epithelium might express different types of cytokeratin (CK) by developmental stages. The objective of this study is to observe the expressions of CK1, CK10 and CK14 in the skin of human fetuses.
METHODS
Immunohistochemical stains were applied to the skin of 42 fetuses ranging from 10 to 36 gestation weeks. Three different portions of the body (i.e., scalp, chest and sole) were sampled. Immunohistochemical staining with monoclonal antibodies against CK1, 10, 14 were done.
RESULTS
We found that CK14 was expressed in the basal layer of the epidermis and adnexae of fetuses beween 10 to 36 gestation weeks. However, stronger expression in the middle than the basal layer was noted in the soles of 15-week fetuses followed by exclusive basal expression. The sebaceous gland, the outer root sheath of the hair follicle and the eccrine duct epithelium also showed CK14 expressions, while CK14 was negative in hair germ and acini. Both CK1 and CK10 were expressed in the epidermis of fetuses ranging between 10 to 36 gestation weeks at the suprabasal layer of the scalp, chest and sole; while they were negative in the basal layer and skin adnexae including sebaceous, hair and eccrine gland.
CONCLUSIONS
Expression of cytokeratins in the fetal skin were noted at 10 weeks throughout the entire gestation period and were similar in the three different sites, except in the early stage of the sole. The main expression sites of K14 were the basal layer of the epidermis, the eccrine ducts and the outer root sheath cells of hair, suggesting the same origin, while those of K1 and K10 were in the suprabasal layer of epidermis.

Causes of Hydrops Fetalis: Analysis of 149 Autopsy Cases.: Ho chang Lee, Je G Chi, Sung Hye Park; Korean J Pathol. 2007;41(2):103-108.

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Abstract PDF: BACKGROUND
Hydrops fetalis is defined as abnormal accumulation of serous fluid in two or more fetal compartments, and this malady is known to be associated with various pathologic conditions.
METHODS
We collected 149 cases of hydrops fetalis out of 2,312 autopsies, and we tried to elaborate the underlying causes of hydrops fetalis. The diagnosis was based on the material from either antenatal termination or intrauterine death.
RESULTS
The relative incidence of hydrops fetalis was 6.44% of all the pediatric autopsies we performed. The gestational age was evenly distributed from 18 to 33 weeks, except for 30 to 31 weeks. There was no sex difference in the incidence of hydrops fetalis. The main causes were cardiovascular diseases (30.9%), cystic hygroma (13.4%), chromosomal anomaly (8.05%), thoracic conditions (7.38%), followed by urinary tract malformation (4.03%), infection (4.03%) and anemia (3.36%). The most common chromosomal anomaly was Turner syndrome and the second one was Down syndrome.
CONCLUSION
Since various conditions can be the cause of hydrops fetalis, pathologists should pay attention to elaborate the underlying causes in every single autopsy.

Significance of CD99 Immunoreactive Cells in relation to Gastrin-producing Cells in Human Gastric Mucosa.: Eun Young Kim, Jong Im Lee, Jung Ran Kim; Korean J Pathol. 2003;37(4):263-269.

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Abstract PDF: BACKGROUND
CD99 is characteristically expressed in Ewing's sarcoma/primitive neuroendocrine tumors and its immunoreactivity has also been reported in gastrointestinal neuroendocrine tumors. However, the normal distribution of CD99 reactive cells in gastrointestinal mucosa and their function are not fully understood.
METHODS
We performed an immunohistochemical study using antibodies to CD99 and gastrin on formalin fixed and paraffin embedded tissue of the stomach.
RESULTS
CD99 were strongly expressed in the gastric glands of neonate (3/3) and infant (1/1) cases but not detected in the fetal period (0/30). In adults, CD99 was observed in 36.8% (7/19). The number of CD99 positive cells were fewer in adult (3.48+/-6.43) than in neonate (5.66+/-0.58) and infant (11.33+/-2.21). CD99 was mostly located along the cytoplasmic membrane of glandular cells but cytoplasmic expression was also evident in neonate and infant cases. The G cells and CD99 expressed cells were reduced in the area showing intestinal metaplasia and atrophic change. As a result of the double stain, some of the G cells coexpress CD99 antigen, which were more in neonate (29%) than in adult (2.6%).
CONCLUSIONS
The CD99 positive cells were found in the gastric pyloric antrum during the postnatal period and progressively reduced with age. This suggests the participation of CD99 protein in the differentiation and secretory process of neuroendocrine cells.

A Study of Umbilical Cord Length According to the Gestational Age.: Eun Kyung Kim, Je Geun Chi; Korean J Pathol. 1994;28(5):511-513.

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Abstract PDF: The umbilical cord length may be a reliable indicator of fetal activity during gestation because it grows in response to tensile forces related to fetal movement. But there has been little attention to normal range of the umbilical cord length. We analyzed the umbilical cord length of 2342 cases de1ivered in Seoul National University Hospital to determine mean values according to the gestational age. The umbilical cord length increased linearly from 15.5cm of 13 week to 50.6 cm of 44 week. After 42 week, the growth was nearly stopped. There was no difference by fetal sex. The length of umbilical cord was variable even within same gestational age.

Ultrastructural Observation on Maturation Process of Cytomegalovirus in Human Cells.: Chul Jong Yoon, Je Geun Chi; Korean J Pathol. 1994;28(5):478-484.

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Abstract PDF: Cytomegalovirus(CMV) infection can be diagnosed by finding characteristic intranuclear inclusion body and enlargement of the cell size congenital CMV infection can be associated with various types of anomalies seen in different gestational age. These anomalies are probable due to direct virus infection of the parenchymal cell m early gestation. Based on four autopsy cases of congenital CMV infection we have studied maturation process of virus particles in parenchymal cells, with special reference to me mode of replication and transmission. Virus particles in CMV-infected cells in brain and kidney showed nucleocapsids with characteristic concentric core, that were enclosed around fibrillar network in nucleus. During replication process virions showed various morphogenic mutation that was rather consistent in different tissues and individuals. There were virions without core or with eccentric core. Occasional cores were divided into 2~5 fragments. The virus particles reached the cytoplasm through the nuclear membrane, and here the virions increased twice in size. After virions were fully matured in the cytop1asm. they showed exocytosis phenomenon through the cellular membrane to reach extracellular portion.

Congenital Cystic Adenomatoid Malformation of the Lung: Clinicopathologic analysis of 22 cases.: Young Lyun Oh, Yeon Lim Suh, Je G Chi; Korean J Pathol. 1994;28(3):219-227.

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Abstract: Congenital cystic adenomatoid malformation of the lung(CCAML) is a rare developmental anomaly characterized by an "adenomatoid" hyperplasia of terminal respiratory structures with formation of the cysts of varying sizes. CCAML is separated into three major types based on the gross and microscopic findings. We have analyzed 22 cases of CCAML, those consisted of 6 autopsy cases and 16 surgical specimens. Out of 22 cases, 5 cases were composed of large cysts(type I) and 9 cases had multiple small cysts(type II). Remaining one case revealed features of solid type(type III), and 7 cases were mixed form. There were 16 boys and 6 girls. All cases were below the age of 14 years. There was no clear-cut age difference between different types of CCAML. However, inflammation, fibrosis and pseudostratification of epithelium were often found in older age. All fetal autopsy cases of CCAML had hydrops fetalis and were associated with maternal hydramnios. One case of type III showed definite mucinogenic cells in the cysts unexpectedly, and one case of the mixed form(typeI+II+III) was found in a fetus of 22 weeks of gestational age. Above findings contradicted the classical description of the CCAML, and suggested that arbitrary classification into three types may not be the best way in understanding this condition.

Hydatidiform Mole with a Coexisting Fetus: Report of three cases with nuclear DNA ploidy analysis by flow cytometry or chromosomal analysis.: Kyu Rae Kim, Dong Hee Choi, Woo Hee Jung, Yong Hyun Park, Myong Ock Ahn, Seon Hee Cha; Korean J Pathol. 1992;26(4):348-354.

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Abstract PDF: Three cases of hydatidiform mole with a coexisting fetus are described. In two cases, flow cytometric analysis of nuclear DNA content from paraffin-embedded, molar tissues and normal-appearing placental tissues showed diploid pattern. One case had karyotypes of 46, XX both in fetal skin fibroblasts and in molar tissues. Microscopically, the villi showed diffuse hydropic swelling with circumferential trophoblastic proliferations and consistent with the diagnosis of complete mole. Two patient had persistent gestational trophoblastic neoplasia on the follow-up. Therefore, in cases of hydatidiform mole with a coexisting fetus, dizygotic twin pregnancies composed of a normal pregnancy from one ovum and a complete mole pregnancy from the other ovum must be considered and the patients should be followed with serum beta-hCG measurements.

Development and Growth of Tongue in Korean Fetuses.: Suk Keun Lee, Chang Yun Lim, Je G Chi; Korean J Pathol. 1990;24(4):358-374.

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Abstract PDF: We examined sixty-three human embryos ranged from three weeks to eight weeks of fertilization age and 117 human fetuses from eleven weeks to fourty weeks of gestational age. Anatomical structure of developing tongue could be classified into eight developmental stages. The first is the sgage of mesial swelling of tongue primordium in the fertilization age of 28~40 days (Streeter stage 13~16), the second is the stage of lateral swelling of tongue primordium in the fertilization age of 41~46 days (Streeter stage 17~18), the third is the sgage of vertical positioning of tongue in the fertilization age of 47~53 days (Streeter stage 19~21), the fourth is the transitional stage of tongue from vertical position to horizontal position in the fertilization age of 54~56 days (Streeter stage 22~23), the fifth is the stage horizontal positioning of tongue in the gestational age of 11 weeks, the sixth is the stage of protrusion of tongue in the gestational age of 12 weeks, the seventh is the stage of maturation of tongue muscle in the gestational age of 7-10 months. The development of tongue papilla characteristically progresses into three stages. The first stage is the epithelial ingrowth for the crypt formation, the second stage is the anatomical formation of vallate, fungiform and filiform papillae, and the third stage is the differentiation of taste buds in the vallate and fungiform papillae or the formation of thick spike-like keratinization at the tip of filiform papilla. We observed that the tongue primordium mainly derived from occipital myotome developed more repidly than other oro-facial structures, so it transitionally occuied the spaces of the pharynx and the posterior nasal cavity, and directly affected the formation of palate and the growth of maxilla and mandible. Whereas the tongue papilla development showed continuous developmental sequences during the fetal period.

Morphological Observation on the Prenatal Development of the Human Gastrointestinal Tract.: Yeon Lim Suh, Je G Chi; Korean J Pathol. 1990;24(2):103-119.

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Abstract PDF: A total of 322 fetuses and 29 embryos were examined light microscopically to evaluate the morphological development of the human gastrointestinal tract with increasing gestational age. The human embryos were analysed by reconstruction of serial section slides. One hundred and forty fetuses ranging from 15 to 41 weeks of gestation were used for correlating the gestational age and the body weight with the measurement of the small and large intestines. 1) The esophagus develps from the distal part of the foregut through a partition of the tracheoesophageal septum. Initially the esophagus is short, but it elongates rapidly and reaches its final relative length and position by the seventh week. The epithelium of the esophagus proliferates and completely obliterates the lumen by the seventh week, but recanalization occurs by the ninth week. The esophageal epithelia consist of three different groups of cells; stratified squamoid cells, ciliated columnar cells and tall columnar cells by the 21th week. 2) The stomach appears as a fusiform enlargement of the caudal part of the esophagus at the fourth week. During next two weeks the stomach acquires its adult shape and final position. The primordial gastric pits and the parietal cells appear at the eighth and eleventh weeks, respectively. 3) As the midgut elongates, it forms a ventral U-shaped loop, called primitive intestinal loop by the fifth week. At this stage the cecum appears as a swelling from the caudal limb of the intestinal loop. By the seventh week the bulks of the caudal limb of the intestine herniate into the umbilical cord, in which the loop rotates 90 degrees counterclockwise around the axis of the superior mesenteric artery. During the tenth week, the intestine returns to the abdomen and undergoes a further 180 degrees counterclockwise rotatation. 4) The cloaca is divided into two parts by a urorectal septum at the fifth week. By the seventh week the urorectal septum has fused with the cloacal membrane, dividing it into a dorsal anal membrane and ventral urogenital membrane. The anal membrane ruptures at the eighth week. 5) During the sixth week the duodenal lumen becomes completely filled with proliferating epithelium. The villi project from the mucosa of the small and large intestines at the eighth and eleventh weeks, respectively. The villi of large intestine become resorbed again after the 21th week. At the fifth week Paneth cells appear through the entire length of the intestine including the rectum, but disappear in the colon and the rectum after the 36th week. 6) The developing Auerbach's plexuses are well recognized along the outside of muscle coat throughout the gastrointestinal tract, but demonstrate no immunoreactivity for the anti-neuron specific enolase antibody. The neuroblasts in the myenteric plexus reveal strong positivity for the anti-neuron specific enolase antibody at the eleventh week, but the ganglion cells differentiate by the fourteenth week. 7) Differentiation of the gastrointestinal wall and development of the myenteric plexus begin form the esophagus and progress caudally down to the colon. But the anorectal wall is differentiated from the cloaca more earlier than the esophagus, stomach and colon are. 8) The small and the large intestines elongate progressively with the increasing gestational age and body weight and increase approximately 5.6 and 5.4 folds, respectively during the 25 weeks from the 15th to 41th week of gestation. At the 40th gestational week the small intestine is 5.68 times the length of the colon. 9) The correlation between the body weight (BW), crown-rump length (CR) and intestianl length (small intestine (SI), large itestine (LI) is presented as: SI (cm)= -33.67 + 4.14CR + 11.62 (BW)(1/3), LI (cm)= 5.56 + 0.76CR + 0.007BW (gm), CR (cm)= 7.82 + 0.015 SI + 0.41 (BW)(1/2).

Supernumerary Tooth Germs in the Incistive Canal of Five Fetal Maxillas.: Suk Keun Lee, Chang Yun Lim, Je G Chi; Korean J Pathol. 1989;23(2):235-239.

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Abstract PDF: Five fetal maxillas were obtained from the autopsy file of fetal postmortem examination, and were examined by serial micro-sections of frontal plane and horizontal plane. Especially the area around the incisive canal of the maxilla was carefully observed. The results are as follows. 1) In 5 fetal maxillas extra-dental laminas and supernumerary tooth germs which are severely malformed in shape are found in the dilated incisive canal, where prominent vessels and nerves are distributed. 2) The supernumerary tooth germs disclose almost normal histo-differentiation of odontoblast and ameloblast, and there shows relatively abundant perifollicular fibrosis in the place of perifollicular bone. 3) It is observed that the over-growth of the extradental lamina from the dental ridge of deciduous central incisor frequently tends to direct toward the incisive canal that includes prominent vessels and nerves.

Weekly Development and Growth of Tooth Germ in Korean Fetuses.: Suk Keun Lee, Chang Yun Lim, Je G Chi; Korean J Pathol. 1989;23(1):1-19.

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Abstract PDF: In order to elucidate the developmental stages of human tooth germ during prenatal period, we examined 254 normal fetuses ranging in gestational age from six weeks to fourty weeks old histologically. Lim's developmental pattern of prenatal tooth germ was divided into three groups, the first group consisting of five grades (I, II, III, IV, V) was for the development of enamel epithelium the second group of three grades was for the deposition of dentin matrix and enamel matrix, and the third group of three grades (A, B, C) was for the growth of perifollicular bone. Some developmental progress between enamel epithelium and dental papilla could be identified by observation of the sequential development of deciduous and permanent tooth germs histologically. The following results were made. 1) The prenatal development of tooth germ showed similar weekly stages in both the maxilla and the mandible. The initial deposition of dentin matrix and enamel matrix (III-1 stage) started at 12-14 weeks of gestational age in the deciduous incisor and canine, and at 16-20 weeks of gestational age in the deciduous molars. And the initial deposition of dentin matrix and enamel matrix in the permanent first molar was at 20-22 weeks of gestational age, and that of the permanent incisor was at 34-36 weeks, and that of the permanent canine was 36-38 weeks, and of the permanent premolar was at 38-40 weeks. 2) The S-shaped curvature was characteristically found where the reciprocal induction of odontoblast and amelobast occurred actively in the developing tooth germ. Primarily pre-ameloblasts which abutted on the dental papilla differentiate the condensed mesenchymal cells into odontoblasts, and secondarily matured odontoblasts which bulged into enamel epithelium produced dentin matrix and differentiated the shrunken pre-ameloblasts into ameloblasts. 3) The mandible grew more rapidly than the maxilla during the early prenatal period. The trabecular bone from both jaws proliferated initially into labial side of developing tooth follicle and gradually circumscribed the tooth follicle lingually and mesio-distally, to form perifollicular bone resultantly.

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