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Three-dimensional microanatomical dynamics of the ovary in postreproductive aged women
Pietro M Motta, M.D., Rosemarie Heyn, Ph.D., Sayoko Makabe, M.D. Fertility and Sterility Volume 78, Issue 2, Pages (August 2002) DOI: /S (02)
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FIGURE 1 Menopausal ovary shows a conspicuous papilla (P) protruding from the ovarian surface along with its subjacent cortical stroma. A crypt (C) is recognized at the base of the papilla. SE = surface epithelial cells. SEM, original magnification, ×600. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 2 Higher magnification of a surface epithelial cell covering a papilla similar to that shown in Figure 1 corresponding to a menopausal ovary. Note its high metabolic activity related to the presence of numerous blebs (arrows) among microvilli. SEM, original magnification, ×7,000. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 3 High magnification of the microvilli covering the surface epithelial cells belonging to a menopausal ovary. Some of these microvilli are short and bent with a knob-like appearance (arrow). Nevertheless, some small holes and/or pits (empty arrows), corresponding to still active endocytic processes, are recognized among them. SEM, original magnification, ×25,000. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 4 General overview of a section corresponding to a menopausal ovary. Follicles are absent. Note the presence of a corpus hemorrhagicum (H) and two follicular cysts (C). The stroma appears dense with abundant scar tissue (S) and leukocyte infiltration (L). LM, hematoxylin-eosin, original magnification, ×25. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 5 Ultrathin section of a menopausal ovary showing the surface epithelium (SE), which consists of cubic cells irregularly covered by microvilli (arrow). Note the absence of follicles. The ovarian stroma (ST) is composed of dense connective tissue. In particular, fibrocytes (F) and collagen fibers (C) predominate. TEM, bar = 10 μm. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 6 Higher magnification of a rather flattened ovarian surface epithelium (SE) in menopause. Microvilli are clearly scarce and short. Cytoplasmic organelles, such as mitochondria (arrow), are recognized. Note a migratory leukocyte (L) crossing the epithelium. The stroma (ST) is dense. The empty arrow indicates a plasma cell. TEM, bar = 2 μm. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 7 Surface epithelial cells of the ovary in menopause. Note the irregular distribution of microvilli. Absence of microvilli in some regions (“bald cells,” asterisks) may indicate later stages of ovarian aging and cells likely to be eliminated (by apoptosis and/or necrosis). SEM, original magnification, ×2,000. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 8 Ovary in early postmenopause that still contains a corpus hemorrhagicum (H), a follicular cyst (C), and a corpus albicans (A). In addition, scar tissue (S) and leukocyte infiltration (L) are also observed as clear homogeneous and basophilic areas, respectively. The bottom of the picture shows the hilum of the ovary containing blood vessels (V). LM, hematoxylin-eosin, original magnification, ×25. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 9 Ovary in late postmenopause (senescence) showing a very smooth surface. Two big old corpora albicantia (A) are observed. The stroma appears much infiltrated by leukocytes (L) and scar tissue. LM, hematoxylin-eosin, original magnification, ×25. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 10 Ultrathin section of a late postmenopausal (senescent) ovary. The ovarian surface epithelium (SE), although very thin, is always present. Epithelial cells show few or no microvilli and are somewhat apart from each other, well defining the cellular limits (asterisk in B). These cells are characterized by perinuclear and perinucleolar chromatin condensation. Note the stroma (ST), mostly containing fibrocytes (F), dense aggregates of collagen fibers (C), colloid-like material (asterisk in A), and an engulfed thrombotic vessel (arrow in A). Dotted arrows in A indicate apoptotic cells destined to be sloughed off. The dotted encircled area in A is shown in a higher magnification in B. The encircled area in B indicates lysosomes and lipid deposits. TEM, bars = 10 μm (A), 1 μm (B). Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 11 Panoramic view of ovarian surface epithelial cells (A, B, C) in postmenopause. Note the irregular and decreasing distribution as well as low height of microvilli (from left to right, A to C) and the increasing definition of cellular limits. Cell “A” evidences a central concave area. Cell “C” is almost devoid of microvilli (similar to the cells shown in Fig. 10B). These latter likely correspond to apoptotic cells destined to be sloughed off. SEM, original magnification, ×3,500. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 12 Ovarian surface epithelial cells (SE) in late postmenopause (senescense). The cell on the left is normal. The two cells on the right are apoptotic. These are characterized by dark cytoplasm along with hyperchromatic and irregular nuclei and the presence of some lysosomes (arrows) in the cytoplasm. Wide fluid-filled intracellular vacuoles (V) are seen, likely corresponding to apoptotic cell detachment. TEM, bar = 2 μm. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 13 With advancing age, the ovarian stroma appears much denser. Collagen fibers are evident and arranged in irregular but thick bundles. SEM, original magnification, ×5,000. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 14 Menopausal and postmenopausal ovaries show a marked thickening of the vascular walls, particularly the arteries. The wide presence of smooth muscle cells (SMC) as well as abundant extracellular matrix deposits (asterisks), especially collagen fibers, are evident. Endothelial cells (E) appear often widely protruding into the vascular lumen (A, B), as contracted, thus decreasing the vascular caliber in which erythrocytes may be entrapped (“L” in B). In other instances, some endothelial cells show degenerative aspects (“E” in C). Note an unmyelinated nerve termination (dotted circle in A) within the tunica adventitia. TEM, original magnification for all the pictures, ×3,000. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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FIGURE 15 This diagram synthesizes the main morphological changes that the human ovary undergoes throughout the phases of reproductive aging (ovary life cycle): reproductive age, perimenopause, (early) postmenopause, and senescence (late postmenopause). The main features are the gradual reduction in the ovarian volume, gradual reduction in number and height of microvilli, increased number of apoptotic cells in the ovarian surface epithelium (darker cells), disappearance of follicles, thickening of the vascular walls, increase of scar tissue, and fibrosis in the ovarian stroma. Motta. Ovary ultrastructure after menopause. Fertil Steril 2002. Fertility and Sterility , DOI: ( /S (02) )
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