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Classification of Tumors of the Ovary: Developmental and Ultrastructural Considerations

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Classification of Tumors of the Ovary: Developmental and Ultrastructural Considerations ANNALS OF CLINICAL AND LABORATORY SCIENCE, Vol. 9, No. 3 Copyright © 1979, Institute for Clinical Science, Inc. Classification of Tumors of the Ovary: Developmental and Ultrastructural Considerations BERNARD GONDOS, M.D. Department o f Pathology, University of Connecticut, Farmington, CT 06032 ABSTRACT The classification of ovarian tumors presents a difficult problem because of the great variety of tumor types that can occur. The complex structure of the normal ovary and the diversity of cell types present at different stages of development contribute to this difficulty. Developmental and ultrastructu­ ral studies have helped to clarify the problem by indicating specific cell types that correspond directly with the major tumor categories. Tumors may thus be grouped as being of epithelial, germ cell or sex cord stromal origin. The ultrastructural features of tumors in the different categories indicate common characteristics shared with corresponding cell types in the developing ovary. The findings clearly support a histogenetic approach in the classification of ovarian tumors. Introduction they also behave in entirely different ways in their clinical presentation, laboratory The diversity in histologic appearance findings, response to various forms of and clinical behavior of tumors of the treatment and eventual outcome. It is ovary presents a particularly difficult therefore critical that the pathologist be problem to pathologist and clinician able to convey to the clinician an appro­ alike. For the pathologist, the number of priate and accurate diagnosis in cases of different categories of ovarian tumors is ovarian neoplasia. in itself an imposing challenge. In addi­ The complexity of the problem is un­ tion, there are so many sub-types in the derscored by the multiplicity of ap­ various categories that only a thorough proaches to the analysis of ovarian tumors understanding of the classification of that have existed over the years. The tumors of the ovary will enable a correct most successful of these have been based interpretation and proper designation in on histogenetic considerations. Utilizing evaluating such cases. For the clinician such an analysis, the World Health Or­ involved in the management of patients ganization has proposed a standardized with ovarian tumors, the problem is classification and nomenclature of ova­ further complicated. Not only do the rian tumors.26 This classification is re­ tumors have different appearances, but viewed in a recent paper51 to which the 179 0091-7370/79/0500-0179 $01.50 © Institute for Clinical Science, Inc. 180 GONDOS reader is referred. Since the present au­ germ cells, oogonia, oocytes), granulosa thor is in essential agreement with the cells and stromal cells. WHO classification, the purpose of this The surface epithelium of the fetal report is not to present a new classifica­ ovary represents an extension of the tion, but rather to add support to the his- coelomic epithelium (mesothelium) over togenetic approach, using data derived the developing gonad. The gonads ini­ from developmental and ultrastructural tially develop as outpouchings into the studies. coelomic cavity in the region of the geni­ tal ridge. Immediately adjacent to the forming gonads, the coelomic epithelium Development of the Ovary invaginates and extends caudally to give Implicit in a histogenetic approach to rise to the Mullerian ducts, the source of tumor classification is an understanding the major part of the female genital tract. of the different normal cell types in­ A special feature of the epithelium over- volved. The ovary is a complex structure lying the fetal ovary is that it undergoes participating in two major functions extensive proliferation during the second which are interrelated but distinct: re­ trimester,20 then reverts to a single layer production and hormone secretion. as is present in the adult.43 The prolifera­ These functions require several cell tion occurs during the formation of corti­ types, i.e., germ cells, supporting cells, cal sex cords which contain germ cells hormone secreting cells.19 and granulosa cells. The surface The development of these different epithelium contributes to the formation cell types within a single organ requires of the granulosa cells,16 some of which are intricate coordination and interaction. also derived from the rete ovarii.8 Much of this complex developmental The germ cells originate extragonad- process takes place in the fetal ovary.56 ally in the yolk sac endoderm, then mi­ Consequently, understanding of ovarian grate to the developing gonad during the histogenesis entails special consideration second month of gestation.58 Initially re­ of fetal stages of development. Table I ferred to as primitive germ cells, these indicates the principal cell types present cells become closely associated with ad­ in the fetal ovary. These are the surface jacent granulosa cells on arrival in the epithelial cells, germ cells (primitive gonad and undergo active proliferation, TABLE I Cell Types in Developing Ovary Cell Type Specific Name Origin Characteristics Epithelial cells Surface epithelium Coelomic epithelium Columnar cells on surface; multiple layers early, then single layer after second trimester. Germ cells Primitive germ cells Yolk sac Large round to oval ameboid cells. Oogonia Round cells in active mitosis, in clusters. Oocytes Round cells in meiosis, become incorporated in follicles. Supporting cells Granulosa cells Surface epithelium/ Oval to elongated cells associated Rete ovarii/ with germ cells in cortical sex Mesenchyme (?) cords. Stromal cells Theca interna Mesenchyme Elongated cells at edge of follicle. Theca externa Undifferentiated stromal cells. Interstitial cells Large oval cells with abundant cytoplasm. CLASSIFICATION OF TUMORS OF THE OVARY 181 at which time they are called oogonia. Another cell type of apparent mesen­ This mitotic phase is followed by a mei- chymal origin is that associated with an­ otic phase which begins at the end of the drogen production. Interstitial cells, hilar third month.22 The cells in meiosis are cells, Leydig cells are names given to the then referred to as oocytes. ovarian stromal cells which are homolo­ Until mid-gestation, the germ cells and gous to the Leydig cells of the testis. The granulosa cells are arranged in cortical latter are clearly derived from mesen­ aggregates without evident organization. chyme.21,25 Interstitial cells appear in the Toward the end of the fifth month the fetal ovary as early as the end of the third first follicles begin to appear, starting in month of gestation.23 Their capacity for the innermost region of the cortex. The and involvement in endocrine activity at process of folliculogenesis, involving the this time are unclear. In the mature ov­ surrounding of individual oocytes by a ary, it appears that such cells are involved unilaminar envelope of flattened, elon­ in androgen production. gated granulosa cells, continues over the next several months. By the early Tumors of the Ovary neonatal period, all of the oocytes present The developmental analysis described have become incorporated in follicles. previously indicates the following prin­ Many of the original population of oocytes cipal cell types: epithelial cells, germ in the fetal ovary degenerate prior to cells, granulosa cells and mesenchymal becoming incorporated in follicles, with (stromal) cells. As indicated in table II, only a limited number surviving the ear­ ovarian tumors can be grouped in a corre­ lier prefollicular stages. sponding manner, i.e., epithelial tumors, The final major tissue component of germ cell tumors and sex cord stromal the developing ovary, the mesenchyme, tumors. The last category represents a remains largely undifferentiated during combination of tumors derived from the fetal period. With the beginning of granulosa cells and stromal cells. The follicle growth in the latter part of gesta­ tion, mesenchymal or stromal cells be­ TABLE II come associated with the follicles. These Major Categories of Ovarian Tumors cells, located outside the basement membrane enlosing the granulosa cells C e l l T y p e Tumor Type Sub-Types and oocyte, constitute the theca interna. The stromal elements adjacent to but not Epithelium Epithelial Serous Mucinous associated with the follicle are referred to Endometrioid as the theca externa. The theca interna Clear cell Brenner tumor and granulosa cells are the cellular ele­ Mixed ments principally responsible for produc­ Undifferentiated tion of sex hormones. This activity be­ Germ cell Germ cell Dysgerminoma comes most evident in the reproductive Endodermal sinus tumor years when, following ovulation, the two Embryonal carcinoma cell types undergo luteinization, a proc­ Polyembryoma Choriocarcinoma ess whereby accumulation of organelles Teratoma associated with steroid hormone produc­ Mixed tion results in great cellular enlargement. Granulosa cell Sex cord Granulosa cell tumor Stromal cell stromal The coma-fibroma The hormones produced are of estrogenic Sertoli-Leydig cell and progestational type. Hormone secre­ tumor Gyn androb1astoma tion also takes place prior to luteinization Lipid cell tumors and in the immature ovary. 182 GONDOS frequent combination of these cell types common occurrence in the young age within a single tumor and their common group and as a rule are not associated involvement in hormone production with endocrine abnormalities. Almost support such a grouping. identical tumor types are found in the Epithelial tumors are the most frequent
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