Paper - A young human ovum in situ
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- 1 A Young Human Ovum In Situ
- 1.1 History
- 1.2 Gross Specimen
- 1.3 Technical Preparation
- 1.4 Abbreviations for all Figures
- 1.5 Decidua
- 1.6 Chorionic Vesicle, Villi, and Implantation Cavity
- 1.7 Trophoblast and Penetration Zone
- 1.8 Operculum Deciduae or Verschluss
- 1.9 Embryo
- 1.10 Summary
- 1.11 Bibliography
A Young Human Ovum In Situ
J. P. Greenhill
Hull Laboratory of Anatomy, The University of Chicago
(1927) Twenty-Two Figures
The series of young human ova is still far from complete and the inadequacy of our understanding of the early stages justifies a detailed description of all young ova. The ovum here described presents certain peculiarities which have not previously been emphasized. It was obtained by Dr. D. W. Day, of Rockford, Illinois, from a decidual cast expelled on October 31, 1918. ‘There is some question as to whether the last normal menstrual period began August 18, 1918, or September 16, 1918. The matter of age has already been discussed (Greenhill, ’27). The development of the ovum indicates that it belongs to a group of ova about nineteen days old. The cast was placed in 10 per cent formalin, three and one-half hours after it had been expelled. It is designated as H 518 in the Embryological Collection of the Department of Anatomy, The University of Chicago.
The cast, which was pear-shaped and measured 46 X 33 X 7 mm., was opened and the implantation site was photographed (fig. 1). The cervical end of the cast was readily distinguishable from the part which had been in the fundus of the uterus. Near the junction of these two distinct portions was an intact oval elevation which protruded into the uterine lumen. This elevation measured about 9.4 mm. in length, 7.3 mm. in width, and 3 mm. in height, and the entire decidua at this site was 6.3 mm. high; but since this specimen was aborted, not all of the decidua was obtained. This elevation contained the ovum. One spot in the elevation appeared more translucent than the surrounding tissue. As will be described later, this represented the point of entrance of the fertilized ovum. The surface of the decidua Vera was furrowed.
After remaining in formalin for five months, the implantation cavity was gradually run into 80 per cent alcohol. After hardening, it was cut through the middle of its ‘longest axis.
Abbreviations for all Figures
|Ad.bl.c., adherent blood cells fi.bd._._ fibrinoid
All., allantois fibd. in plas., fibrinoid in plasmodium
Am.V., amniotic vesicle Int.sp. and Im3v.sp., intervillous space
Bd..st., body stalk
Br.m'll., branched villus
Br.bd., brush border
Bl.p1'.gm., blood pigment
B1. in PL, blood in plasmodium
Bl.v., blood vessel
Bl..sin., blood sinus
Cell. l., cellular layer
Chor.laev., chorion leave
Dec.bas., decidua basalis
Dec.caps., decidua capsularis
Dec.gl., decidual gland
Mat.bl., maternal blood
Mat.end., maternal endothelium
Pen.an.., penetration zone
Plus. and Plasm., plasmodium
Plus. in sin., pla.smorlium in sinus
Sp.art., spiral artery
Trophy. in gl., trophoblast in gland
Trans. and Tr.c., transition cell
Ut._gl., uterine gland
Van.s'in., venous sinus
Fig. 1 Photograph of the decidual cast opened. Natural size. The dark spot 2 mm. to the left of the guide line marks the position of the operculum deciduae.
Fig. 2 Photograph of the gross specimen in 80 per cent alcohol, showing relations of ovum and decidua from the right half of the implantation site. X 13.9.
One—half (block A) was dehydrated, cleared in bergamot oil, embedded in paraffin, and cut 10 u thick in series, except for a few sections which were cut 6 p thick. These were originally stained with phosphotungstic acid hematoxylin (Mallory). The other half (block B), which contained the body stalk, was photographed (fig. 2) to show the general relations of the ovum to the decidua and was cut into two longitudinal parts. Both were run into paraffin and cut serially, but the lateral half was first mordanted for five days in 1 per cent aqueous osmic acid. Some of these sections were stained with Mallory’s connective-tissue stain and others with iron hematoxylin.
The portion of the decidua basalis which borders on the implantation cavity differs from the remainder of the basalis. -It is separated from the implantation cavity by an almost continuous layer of fibrinoid and is known by a variety of names, such as Umlagerungszone (Strahl, ’90, and Peters, ’99), Durchdringungszone (Grosser, ’25), Zwischenzone (Strahl und Beneke, ’l0), transition zone (Bryce—Teacher, ’O8), border zone (Herzog, ’09), detritus zone (Bonnet, ’12), la zone périovulaire (Delporte, ’12), etc. We shall call it the penetration zone (after Grosser) and describe it with the trophoblast.
Aside from the penetration zone, the decidual change found in early ova is very variable. In the very young Sch. ovum of v. Mtillendorff (’21 a) and that of Bryce-Teacher no. 1 (’08), there is an outspoken decidual change, whereas in the older ova of Peters (’99), Jung (’08), and Linzenmeier (’14) there is only a slight decidual change, and this is limited to the vicinity of the ovum. Still more remarkable is the Kleinhans ovum (Grosser, ’22), where the endometrium resembles the premenstrual mucosa as figured by Schroeder (’13) for the twenty—sixth day of the menstrual cycle. This extreme variability in decidual reaction supports Grosser’s contention that ovulation does not necessarily occur at a definite time in the menstrual cycle, but it must not be forgotten that we do not yet know the nature of the variability in the cyclic changes of the endometrium.
In our specimen the cells below the penetration zone show the typical decidual change. They are essentially large polygonal, pale cells with large ovoid nuclei (figs. 12, 13), but some cells are round or spindle-shaped. In the lower third of the basalis there is a coagulum between the stroma cells. The latter stand out beautifully in the sections mordanted with osmic acid. Scattered throughout the basalis are leucocytes. Frassi (’07), Jung (’08), and P. Meyer (’24) maintain that leucocytes are found only in maternal tissue, and hence present a means of differentiating between fetal and maternal tissue. However, Grosser in his Sch. ovum (’22) found leucocytes two and three rows in depth in the trophoblast. Todyo ( ’12) likewise found leucocytes in fetal tissue. But might not the presence of these leucocytes signify degeneration of the trophoblast”!
The glands in the decidua basalis of our specimen are narrow and run obliquely. Near the ovum they are almost parallel with the long axis of the implantation cavity (figs. 5, 22). Most of the glands resemble those seen in the early premenstrual phase. Only an occasional gland shows the typical ‘saw-toothed’ change of pregnancy (the so-called pregnancy gland of Opitz). Nearly all the glands appear empty, and but few of them show marked secretory activity. Some contain free masses of epithelium which have separated from the basal membrane, and an occasional one contains a little coagulable material. A few glands contain red and white blood cells. In most places the epithelial cells of the glands are cuboidal, they have granular protoplasm and they contain large pale nuclei. The total number of glands is strikingly small (fig. 2).
The decidua marginalis is similar to the decidua basalis, but the decidual changes, except very near the implantation cavity, are not so pronounced. There is in the marginalis, as in the basalis, a distinct penetration zone.
The blood vessels in the decidua beneath and to the sides of the implantation cavity are numerous a.nd consist chieﬂy of veins (figs. 2, 3, 17). Almost all the veins are dilated and contain free blood or fibrin or both. Most of the arteries are narrow, spiral-shaped, and contain very little blood (fig. 3). The walls of most of the veins consist of a layer of endothelium and an outer thin layer of connective tissue (fig. 7). The arteries, on the other hand, have not only an endothelial, but also a well-defined circular musculofibrous layer. Just beneath the implantation cavity and to one side is a large angulated sinus, the shape of which is probably the result of pressure of the ovum (fig. 2). This angulated vein in many sections seems to have only an endothelial layer. It contains free blood and fibrin just as most of the veins do and communicates with the implantation cavity. At the site of the communication is a mass of plasmodium which extends far into_the vein (fig. 7 ). The blood surrounding the mass of plasmodium is not coagulated. Below the implantation cavity this large venous sinus is found to join other veins. Hence there are interlacing connections between veins and the implantation cavity. This shows that the growth of the ovum is not due to simple pushing apart of tissue. Teacher (’24) regards this large vessel, which is found in many young ova, as the main drain which leads from the implantation cavity into the maternal veins. Grosser (’25), however, believes that this sinus does not participate in the circulation because in his ovum Sch. and in other ova the blood in the sinus is largely coagulated. Teacher (’24, ’25) asserts that the abortion of the Bryce-Teacher ovum no. 1 was due to rupture of, and thrombosis in, the large underlying venous sinus.
Fig. 3 Photograph of a median section of the ovum. 48 mm. B. & L. Tessar X 14 reduced to 11.2 diameters. Mallory connective-tissue stain.
Fig. 4 Photograph, showing body stalk with allantois. Z-Obj. AA X 38 reduced to 30.4 diameters. Mallory connective-tissue stain.
Fig. 5 Photograph, showing body stalk with portion of amniotic vesicle. Z-Obj. AA X 38 reduced to 30.4 diameters. Mallory connective-tissue stain.
In the decidua of our specimen the endothelium in most of the veins is normal, but occasionally it is separated from the vein wall, and in one large vein which runs diagonally across the decidua it is missing. This is observed in many successive sections. The decidua forms the boundary of the vein in this area, and yet there is no coagulation of blood here. This disappearance of endothelium is most likely due to the action of the plasmodial masses in the lumen of this vein. This peculiar relationship between vein and decidua is hardly an artefact. In the Bryce-Teacher ovum no. 1, Teacher (’08) describes the absence of some endothelium in a blood vessel which is being invaded by a mass of syncytium. The gap, however, is filled by a thrombus.
There are many communications between the implantation cavity and maternal veins, and, in addition, there is _a blood vessel on one side of the implantation cavity which has not only been invaded by plasmodium, but in which one wall has been replaced by a mass of plasmodium (fig. 17).
A very careful study was made to find arterioles which open into the implantation cavity. While some arterioles were found coming close to the implantation cavity, none were found to actually communicate with it. The arterioles break up into capillaries before reaching the implantation cavity. We can, therefore, say definitely that large arterioles do not enter the intervillous space even at this early stage. From a study of the Bryce-Teacher ovum no. 1, Teacher (’24, ’25) is inclined to believe that blood ﬂows “into the implantation cavity in jets from many little vessels situated at various points on the roof" and sides of the cavity and ﬂows out by the large sinus at the base. As these vessels are all very small, it is impossible to be sure from the microscopic characters whether they are .arterial or venous capillaries, but the direction of the blood ﬂow from them is clear.”
Immediately adjacent to the side of the implantation cavity are glands and veins curved like arcs which correspond to the curve of the implantation cavity (fig. 2). These curves are undoubtedly due to pressure of the growing ovum. One vein has been invaded by plasmodium (fig. 17). This is one of the places which shows how Well most glands resist invasion of the plasmodium in contrast to the veins which are very susceptible to invasion by plasmodium. Teacher (’24) observed the same resistance of the glands and susceptibility of the blood vessels in the Bryce—Teacher ovum no. 1. He says that invasion. of blood vessels and the blood liberated into the implantation cavity are essential to the life of the ovum. However, one gland in the marginal decidua of our specimen was found which was invaded by plasmodium and this gland was curved also. Frassi (’07) proved that glands could be opened laterally, and he and Fetzer (’10) found glands which opened into the intervillous space. These authors, as Well as Leopold (’06), Debeyre (’12), and S. van Heukelom (’98), found blood in gland lumina. So did We. Johnstone (’14) points out that gland invasion may be due to ‘the eroding action’ of trophodermic buds or to the diges~ tive action of proteolytic ferments of the trophoderm, while that tissue itself is at some little distance.
Above, the decidua capsularis varies from 0.09 mm. to 0.22 mm., Whereas laterally, where it bulges out over the decidua Vera, it measures 0.23 mm. on one side and 0.42 mm. on the other. The plasmodium is more abundant Where the capsularis measures 0.23 mm. The structure of the capsularis is hard to distinguish in most areas; but, in general, the tissue consists of degenerated decidual cells with fibrinoid, blood vessels, a moderate number of red blood cells, many leucocytes, pigment, and vacuoles scattered throughout. The degenerated decidual cells, most of Which lie free, are polygonal, club—, spindle—, and sausage—shaped, and have dark staining protoplasm and still darker nuclei. The latter vary in size, position, and shape. Some cells contain vacuoles. Beside these degenerated cells, there are a few normal decidual cells. As in the penetration zone, many phagocytes are present. Nearly all sections show leucocytes and pigment scattered about. In a few places free red blood cells are seen. There are few blood vessels. Some of them contain red and white blood cells, while others contain fibrin. A few of the larger vessels contain both free blood and fibrin. In some blood vessels the endothelium has separated from the basement membrane. fibrinoid is seen nearly everywhere within and on the inner surface of the decidua capsularis and in a few areas there is marked edema of the tissue.
The nearer the implantation cavity, the more necrotic is the tissue of the decidua capsularis, the more deeply it stains, and the more fibrinoid it contains. Just outside the implantation cavity the decidua capsularis, marginalis, and basalis merge into one layer which stains deeply because of the presence of fibrinoid. This area, like the capsularis, is elevated somewhat above the surrounding mucosa, and the uterine epithelium which covers this elevation is ﬂattened. Most of the capsularis itself has no epithelial covering. In one area of the capsularis the tissue is strikingly different, and this is described under the heading of ‘operculum deciduae.’
In a few areas the capsularis is invaded for a short distance by plasmodial masses coming from the implantation cavity. In one place a thin strand of plasmodium is contiguous with the free end of the endothelium of a blood capillary (figs. 18, 19). With the Mallory connective-tissue stain the plasmodium and endothelium look identical, and it is only with difficulty that a break in continuity of the two types of tissue can be seen. In another area a mass of cytoblast is in contact with the inner surface of the capsularis. No glands were seen anywhere in the capsularis. Johnstone, however, found disconnected portions of glandular tissue in the capsularis of his ovum.
The thickest part of the decidua Vera or parietalis (Bonnet, ’03) measures 3.9 mm. It contains numerous glands resembling those of the premenstrual phase and the epithelium "is intact everywhere. Many white blood cells are seen throughout the vera and there are abundant arteries and veins. The veins contain free blood and fibrin, but nearly all the arteries, which are spiral in shape, are empty.
At some distance from the ovum is a small abscess. The decidua around the abscess is very edematous and nearly all the blood vessels in this area contain a great deal of fibrin. The epithelium covering the decidua above and near the abscess is indistinct. In the Vicinity of the abscess are many dark—staining elliptical, spindle—shaped, and polyhedral cells, most of which are degenerated decidual cells. Some of these cells are multinucleated, and these may be phagocytes.
Chorionic Vesicle, Villi, and Implantation Cavity
The following is a list of the measurements of our ovum. All the measurements given are maximum ones, and they are written in the following order:
a. The measurement parallel with the long axis of the uterus.
b. The measurement perpendicular to the long axis of the uterus.
c. The measurement perpendicular to the mucous membrane.
1. The ovum including theidecidua capsularis as a gross specimen in formalin measured 9.4 Xv7.3 X 3.0 mm. and in the stained sections, 8.37 X 6.44 X 2.67 mm.
2. The implantation cavity in the stained sections measured 6.23 X 5.79 X 2.5 mm.
3. The ovum with the definitive villi in the stained sections measured 4.72 X 5.41 X 2.-23 mm.
4. The ovum "exclusive of villi in the stained sections meas
6. The yolk sac in the stained sections measured 0.64 )< 0.53 X 0.43 mm.
The amount of shrinkage in our ovum was only 11 per cent—an unusually small amount—~and because of this the ovum appears to be relatively large in comparison to the stage of development it represents. Although the longest axis of the implantation cavity is parallel with the long or sagittal axis of the uterus, the greatest diameter of the chorion is perpendicular to these two.
From the surface of the blastocyst, directed toward the decidua basalis, numerous well—developed villi arise, whereas on the opposite surface there are comparatively few villi. There is, therefore, a definite differentiation into a chorion frondosum and a chorion laeve (figs. 2, 3). Perhaps this is correlated with a superficial implantation. On the sides of the chorionic vesicle a fair number of villi take origin. Some of the villi show budding, but the buds themselves do not subdivide. Grosser (’26) believes that ova less than 4 cm. in diameter in which the outer wall of the chorionic vesicle is smooth (lacks villi) are abnormal. Normal embryos may, however, be found in such ova.
There is very little magma, the chorionic mesoderm being largely confined to the wall of the blastocyst where it consists of scattered spindle cells, some of which have long fibrils. In a few places there are small blood-vessel anlagen in the mesoderm. Blood-vessel anlagen are also seen in the mesoderm of a. few of the larger villi (fig. 6). These anlagen consist of short tubules, the walls of which are formed by a single layer of thick endothelial cells. The lumen of most of these tubules appears empty, but in one near the body stalk are a few nucleated red blood cells.
The body stalk (figs. 2, 4, 5) is situated in the chorionic vesicle basally, but eccentrically, and its cells are more compact than they are elsewhere in the blastocyst. The allantoic duct (fig. 4), which consists of simple, cubical epithelium, extends but a short distance into the body stalk. It is seen in fifteen consecutive sections, and its lumen seems to contain ﬂuid. The yolk sac is discussed in the description of the embryo.
ured 4.08 X 4.21 X 1.58 mm.
5. The embryonicidisc (estimated) in the stained sections measured 0.15 X 0.13 mm.
In most places the chorionic ectoderm consists of two layers, an inner cytotrophoblast or pre—Langhans layer and an outer syncytial layer (fig. 6). The protoplasm of the former is well differentiated into individual cells and the nuclei are large, pale, and distributed with some degree of regularity. The outer layer varies considerably in thickness and has elongated and dark—staining nuclei which lie parallel to the surface. Sometimes the outer layer is barely visible because it is so thin. Many villi are covered with only one layer of ectoderm, and this is usually the syncytial layer. On the tips of some villi the ectoderm is heaped up into a large mass of cytotrophoblast (fig. 22), by means of which the villi are occasionally attached to the decidua basalis. There is much trophoblast between the villi and the walls of the implantation chamber. A few villi have a very fine brush border on the syncytium. Two villi are seen where part of the ectodermal covering is missing in some sections. They probably represent an early stage of degeneration.
A small piece of ectoderm was torn loose from the chorion during the preparation of the specimen and is attached to the inner surface of the decidua capsularis at the site of the operculum deciduae which represents the point of entrance of the ovum (p. 316 and fig. 20).
The implantation cavity, which is ovoid in shape, is confined to the decidua compacta. Nearly all the maternal blood cells in the cavity are in astate of good preservation. While there is considerable blood in some parts of the implantation cavity (fig. 3), the latter is by no means filled with formed blood elements. In the two ova of Teacher and Bryce (’08, ’24) and those of Johnstone (’14), Herzog (’09), and others, the implantation cavity is entirely filled with blood. In the ova of Marchand (’03) and Frassi (’07) there was no blood in the intervillous space.
Nearly all along the border of the implantation cavity, but mostly at the basalis, is an abundant homogeneous or striped hyaline—like layer of fibrinoid (figs. 7, 12, 13, 14). It is essentially a rough boundary line between normal fetal and fairly normal maternal tissue, but in a number of places fibrinoid is seen not only within plasmodium, but also on the fetal side of some plasmodial masses (figs. 7, 12). There is abundant fibrinoid also within the penetration zone (fig. 13) and in the decidua capsularis (figs. 18, 19). Like fibrin, it has a conspicuous bright red color when stained with eosin. With the Mallory connective—tissue stain it has a deep red color.
Many writers use the term fibrin to designate both fibrin and fibrinoid. However, as Grosser (’09) points out, the term fibrin should be used only for the coagulum which arises from blood or lymph. On the other hand, there are essentially two sources of fibrinoid, the chief one of which is the trophoblast, and the syncytium forms fibrinoid earlier than the cytoblast. The second source of fibrinoid is degenerated maternal tissue.
In the very young Sch. ovum of _v. Mollendorff (’21 a) and the Bryce-Teacher ovum no. 1 (’08) the fibrinoid is of maternal origin, while in the older ova of Jung (’08), P. Meyer (’24), van Heukelom (’98), and Frassi (’07) it is of mixed origin. The fibrinoid derived from maternal tissue is due to contact with trophoblast, but on rare occasions fibrinoid may result from a distant action of the trophoblast. Grosser (’25 b) discusses the qliestion of fibrin and fibrinoid in the placenta.
Trophoblast and Penetration Zone
The trophoblast (Hubrecht, ’89). is most abundant at the sides of the implantation cavity, especially on the side directed toward the cervix uteri (fig. 3, on the left); but there is also much of it basally. It lies free for the most part, but some masses project from the distal ends of villi. The most striking feature of this ovum is the very widespread invasion of maternal tissue by the plasmoditrophoblast. This invasion is most evident in the decidua which immediately surrounds the ovum, but masses of plasmodium are also found within blood vessels at some distance from the ovum.
Fig. 6 Photograph, showing vascular anlage in a villus. Z-Obj. 8 mm. apo. immers. obj. 0c. 8 X 300 reduced to 240 diameters. Phosphotungstic acid hematoxylin stain.
Fig. 7 Photograph, showing margin of implantation cavity with a plasmodial mass within a blood sinus. Z-Obj. C. X 80 reduced to 64 diameter. Mallory connective-tissue stain.
Fig. 8 Photograph, showing plasmodium and penetration zone. Z-Obj. 4.0 mm. apo. immers. obj. 0c. 4 X 450 reduced to 360 diameters. Phosphotungstic acid hematoxylin stain.
There are two distinct types of trophoblast, namely, cytotrophoblast (cytoblast) and plasmoditrophoblast (plasmodium, syncytium). The cells of the cytoblast (figs. 9, 10) are large, pale, finely granular, polygonal or irregularly elliptical, and contain vacuoles. The nuclei, which are large and pale, are essentially ovoid in shape, but many are irregular in outline. The nuclei in the trophoblast are better preserved after osmie—acid mordanting. This probably means that the wrinkling of the nuclei seen in some of the other sections is an artefaet. Most cells have only one nucleus. In some groups the cells are closely packed, while in others the cells are more or less free.
The plasmodium (figs. 8 to 15) stains more deeply and seems to be made up of myriads of small, closely packed granules. J ohnstone (’14) speaks of the plasmodial protoplasm as foam—like, but the actual appearance is a matter of fixation. There are no cell membranes as in the eytoblast, but throughout the plasmodium are scattered large oval or irregularly quadrangular nuclei which show bright red nucleoli in the sections stained with Mallory’s connective—tissue stain (fig. 14). The nucleoli are small, elliptical, and irregular, and not infrequently two or more are seen within one nucleus. Usually, the nucleoli are centrally placed, but oecasionally they are eccentric. The surface of the plasmodium may be very irregular, so that small pockets of the implantation cavity appear to extend into the plasmodium. Some of these pockets, which appear as vacuoles within the plas—V modium, contain maternal blood cells (fig. 8). The cytoblast has long been regarded as an earlier stage in development than the plasmodium, but not much evidence has been produced to demonstrate the relationship. figures 9 and 10 show several transitional stages between the two types. The cells of the cytoblast swell, their protoplasm acquires a denser granulation and stains more deeply. The nuclei enlarge and the cell borders disappear. This change is attributed to contact with the maternal blood. Delporte (’12) illustrates a number of these transitional stages.
Fig. 9 Camera-lucida drawing, howing cytoblast, plasmodium, and transition stages. Z-2 mm. apo. immers. obj. oc. 4 X 770 reduced to 513 diameters. Mallory connective-tissue stain.
Fig. 10 Camera-lucida drawing, showing cytoblast, plasmodium, and transition stages. Z-apo. X. 0c. 8 X 600 reduced to 500 diameters. Mallory connective-tissue stain.
Fig. 11 Camera.-lucida drawing, showing plasmoﬂium in ‘penetration zone. Z-2 mm. apo. immers. obj. 0c. 6 X 790 reduced to 592.5 diameters. Mallory connective-tissue stain.
Fig. 12 Camera-lucida drawing of the basal portion of the implantation cavity, showing penetration zone, fibrinoid, and plasmodium. Z-2 mm. apo. immers. obj. 0c. 4 X 768 reduced to 384 diameters. Mallory connective-tissue stain.
With the Mallory connective-tissue stain plasmodium presents a beautiful picture (figs. 14, 15). The protoplasm typically stains a striking purple, and spread all over this are the bright red nucleoli.
Fig. 13 Camera-lucida drawing, showing active invasion by plasmodium through an opening in fibrinoid layer. Z-2 mm. apo. immers. obj. oc. 6 X 790 reduced to 395 diameters. Mallory connective-tissue stain.
In many areas plasmodium is found alone, but in nearly every place where cytoblast is found plasmodium is likewise seen, and both are in very intimate contact. All the invasion of maternal tissue is by the plasmodium, none by the cytoblast. While most of the invading plasmodium is free from the chorionic plate or villi, one large mass of it is seen extending from the end of a villus across the intervillous space, down to and invading the decidua basalis (fig. 14).
Nearly all of the invasion by the plasmodium takes place in the penetration zone. In the very early ova of v. M6llendorff (Sch.) (’21 a) and Bryce—Teacher no. 1 (’08), there is no penetration zone, but instead, there is a zone of necrotic decidua containing many leucocytes, but no fetal elements. In the Miller ovum (’13), Which, according to Streeter (’26), is younger than these two, there are syncytial strands in the decidua. In later stages this invasion increases until the second generation of trophoblast (Grosser, ’25) is reached, when the penetration zone forms a distinct layer [Peters (’99) and other ova]. However, the zone is missing in the young ovum of Schlagenhaufer and Verocay (’16).
In our specimen the penetration zone is found not only in the decidua basalis, but also in the marginalis (figs. 2, 8, 11, 12, 13, 14). It is the dividing line between the fetal and maternal tissue and consists essentially of decidual cells which are in various stages of degeneration and of invading trophoblast. Nearly all the decidua that is adjacent to plasmodial masses is necrotic. A few decidual cells, not in contact with plasmodium, have pyknotic nuclei, and this may be due to the distant action of the plasmodium. This decidua is more deeply stained than the remainder. Some of the plasmodium is also degenerated. In the penetration zone the decidual cells are more edematous and their structure is less distinct than it is elsewhere in the basalis and marginalis. In some places the cell outlines cannot be distinguished. Some of the cells are pale and contain very granular protoplasm. This layer also contains fairly large isolated masses of protoplasm which stain very deeply, contain dark nuclei, and resemble plasmodium. Most of these large dark masses are degenerated decidual cells, some of which form symplasmata of Bonnet. In addition, there are many phagocytic cells. P. Meyer (’24) speaks of these cell masses as ‘syncytial wandering cells’ and maintains they are of trophoblastic origin. Scattered throughout the penetration layer are masses of fibrinoid and in some places there are vacuoles between decidual cells. Likewise, there are clumps of maternal red blood cells, leucocytes, and pigment granules. There are, furthermore, in the penetration zone, the terminal portions of Veins which communicate with the implantation cavity.
fig. 14 Cameraiucida drawing, showing plasmodium extending from tip of villus into penetration zone. Z~3 mm. apo. immers. obj. 0c. 6 X 500 reduced to 333 diameters. Mallory connective-tissue stain.
fig. 15 Camera—1ucida drawing, showing plasmodium with psendopods within penetration zone. Z-2 mm. apo. immers. obj. 0c. 18 X 1840 reduced to 1226 diameters. Mallory connective tissue stain.
Whcn a mass of plasmodium invades maternal tissue, it encounters first a layer of fibrinoid. We find all stages in the invasion of the decidua, from a mere contact of plasmodium with the fibrinoid to the stages shown in figures 13 and 14, where the fibrinoid has been eroded and ingested and the trophoblast is destroying maternal tissue. In one area where a vein has been invaded, one wall of the vein is replaced by plasmodium (fig. 17). In other veins which have been invaded, masses of excellently preserved plasmodium are seen, some of them at quite a distance from the implantation cavity I (figs. 6, 16, 22). Hence, at this early period we have deportation of fetal elements into the maternal circulation.
Some of the fibrinoid found in the plasmodial masses may represent degeneration of the plasmodium itself (figs. 7, 12). In general, the latter appears to be enlarging the implantation cavity and making room for the later arrival of the growing chorionic vesicle and villi. The cytoblast which is found distally has larger cells than the cytoblast of the definitive villi. The reason for this, according to Grosser ( ’25) is that the distal cytoblast is older.
fig. 16 Photograph, showing eroded bloocl sinus in deaidua basalis. Z-obj. AA X 38. Phosphotungstic acid hematoxylin stain.
fig. 17 Photograph, showing erosion of blood sinus in decidua marginalis. Z-obj. O X 80. Phosphotungstic acid hematoxylin stain.
In many plasmodial masses and in some of the syncytium which covers the villi, opaque and yellow pigment granules are seen (figs. 12, 13). These probably represent the end products of broken—down red blood cells due to the phagocytic action of plasmodium. In a few places red blood cells are adherent to the surface of the plasmodium, but there is no direct evidence of the destruction of these blood cells by the plasmodium. The pigment is highly insoluble. The constant presence of these pigment granules in the syncytium and their absence in other tissues led Johnstone (’14) to regard the granules as a means of recognizing syncytium. Prof. Lorrain Smith, who studied these granules with Johnstone, suggested that they are composed of molecules of blood pigment adherent to droplets of fat or lipoid.
The amount of invasion in our specimen is astonishing. At least twelve different sites are found where the plasmodium has broken through the layer of fibrinoid and invaded the decidua or has broken through the walls of veins. In some areas of sections stained with phosphotungstic acid hematoxylin, the union between the decidua and plasmodium is so intimate that only Very careful study reveals the boundaries between the fetal and maternal ‘tissues (figs. 11, 13). The amount of invasion shown in our ovum is unusual, especially when We consider the stage of development it represents (pp. 343, 344).
Most of the plasmodium which is free in the implantation cavity and is in contact with blood has a brush border (striated border, Biirstenbesatz) (figs. 9, 18, 19,), but the latter is not present everywhere. The plasmodium which invades does not seem to have the brush border (except in one place. Brush borders have been described by Herzog (’09), Jung (’08), V. Miillendorff (’21), Bonnet (’03), Marchand (’03), Johnstone (’14), and others. Lenhossék (quoted by Johnstone, ’14), who studied this border in a fresh specimen, saw no evidence of motile processes. Teacher (’24), in speaking of the Bryce—Teacher ovum no. 1, says “the striated border could notxbee made out on the syncytium. It is certainly absent from the masses which are invading the decidua in search of .v'es‘sels—-these have clean-cut margins.” Does this represent a difference between resorbing and invading plasmodium? In some areas of our specimen there are projections of invading plasmodium which look like pseudopods (fig. 15).
fig. 18 Photograph, showing plasmodinl pseudoporl in contact with vascular endothelium in decidua capsularis. Z-apo. 2 mm. obj. 0c. 2 X 450. Osmic-acid mordant. Iron-hematoxylin stain. V
fig. 19 Key figure to figure 18. fibrinoid is solid black. Maternal tissue is white. Plasmodium is stippled. Pseudopod in contact with endothelial cell at point indicated as Mamend.
As previously mentioned, in one area of the decidua capsularis a strand of plasmodium coming from the intervillous space is definitely contiguous to the endothelium of a maternal capillary. Both plasmodium and endothelium stain similarly, and only with an apochromatic immersion lens could the contact surface be found between the fetal and the maternal elements (figs. 18, 19). In the Teacher-Bryce ovum no. 2 an area was found and drawn [Teacher, ’24, ’25; (fig. 13)] which shows an open blood vessel communicating with the intervillous space. On both sides of the communicating area the syncytium seems to be continuous with the endothelium which is practically perfect. Teacher adds “. . . . it is nevertheless clear that the syncytium does not originate from the maternal endothelium.” Jung (’08) also shows syncytial masses continuous with the endothelium of maternal blood vessels. It should be borne in mind that very thin sections are usually necessary to bring out the difference between the two cell types. Jung’s sections were between 10 u and 15 u thick.
In the sections mordanted with osmic acid there is absolute contact between plasmodium and decidua, whereas in most of the other sections there is a space between the two, probably due to shrinkage. As far as we know, the only other author who used osmic acid is J ohnstone (’14), but he does not mention the phenomena just described.
While in most places the two distinct layers of the trophoblast are seen, there are numerous areas where only one layer, usually the plasmodial or syncytial, is found} This may be because the cytoblast has not proliferated as rapidly as it has been transformed into syncytium, and this is especially true where there has been very active growth. We know that by the fifth month there is very little of the cellular layer left on the villi, and the explanation is that the growth phase of the trophoblast is in abeyance. However, even at term one may find an occasional Langhans cell.
Grosser (’10) suggested that the variability in the relative proportions of cyto— and plasmoditrophoblast in very young ova may be explained on the assumption that there are two phases of trophoblastic activity. A period of invasion of the maternal tissue by plasmodium is followed by extensive degeneration of the latter. Then there is a great proliferation of trophoblastic cells with distinct boundaries (cytoblast) which fills the implantation cavity. This is what we see in the Sch. ovum of V. Mollendorff (’21 a). The massive cytoblastic shell then begins to go over into plasmodium, and a new phase of active enlargement of the implantation cavity begins. Eventually, says Grosser, we have the picture presented by the Bryce—Teacher ovum no. 1 (’08) with its ‘primary villi’ of plasmodium. The implantation plasmodium then degenerates and a ‘second generation’ of cytoblast takes its place, as in the ovum of Peters (’99). This proliferation reaches its height as the Trophoblastschale of Merttens’ (’94) ovum. From this cytoblast comes the syncytium of the early definitive villi which have appeared in the interim. While Grosser believes that the Trophoblastschale plays a part in the further enlargement of the implantation cavity, he does not appear to regard this particularly significant.
The conditions in our ovum suggest that there is a phase of active erosion following the stage represented by the Peters ovum, quite comparable in magnitude to that which
‘Bonnet (’03) suggested and Grosser (’25 a) agreed to make a distinction between syncytium and plasmodium. They consider syncytium to be a brightly stained, multinucleated mass of granular protoplasm formed by the union of a number of degenerating cells, whereas plasmodium denotes a tissue in which division of nuclei has occurred without division into cells.
precedes it. On this basis, we should regard the peripheral actively eroding plasmodium of H518 as derived from the proliferating cytoblast of the Peters stage. There is then a phase of active erosion of which the ovum of Jung represents the beginning and H518 the end. Various specimens of this period, viz., the ova of Jung (’08), Teacher-Bryce no. 2 (’08, ’24), Heine-Hofbauer (’11), Kiss (’21), P. Meyer (’24), and Stolper (’O6), all show more or less erosion by plasmodium. The conditions in these ova cannot be explained, however, unless we assume some variability in the trophoblastic development in different cases. In some, as in ours, the erosion would be followed by a. phase of proliferation, whereas in others it proceeds pari passu with a proliferation from the young definitive villi. An accurate seriation of early ova is out of the question at the present time, not only because we lack adequate criteria, but because the published data concerning most specimens are all too meager. As a matter of fact, Grosser ’s most suggestive hypothesis of trophoblastic phases will have to be substantiated and developed by a vastly larger series of normal ova than we have available at present.
Operculum Deciduae or Verschluss
There is a region where the continuity of the decidua capsularis is interrupted by tissue which differs from the decidua, but which resembles plasmodium (figs. 20, 21). In most of the sections this tissue, which was called ‘Verschluss’ by Schlagenhaufer and Verocay and to which Teacher recently (’25) gave the name ‘operculum deciduae,’ extends through the entire thickness of the capsularis. It is situated eccentrically in the capsularis (fig. 1), and its outer surface is slightly depressed. To its inner surface are attached a small mass of plasmodium with a shred of chorionic membrane torn loose from the ovum.
The structure of the operculum is hard to describe. Most of it resembles plasmodium, but some areas appear to be granular and ill-defined, especially at the periphery. In some places there are pale, irregularly shaped cells with nuclei which Vary considerably in size and shape. The adjoining capsularis stains Very deeply. It consists almost entirely of a fenestrated fibrinoid which is exactly like the fibrinoid seen in other parts where plasmodium is invading the decidua. In many sections the fibrinoid is found not only on the sides of the operculum, but also on its inner surface, thereby forming a support on which the operculum rests. Teacher speaks of the fibrinoid situated below the operculum as “the internal shield of fibrin.” A similar shield is found in Johnstone’s ovum.
fig. 20 Camera—lucida drawing, showing operculum deciduae and its relations to the chorion. B. & L. obj. 1. 0c. 6 X 145. Mallory connective-tissue stain.
With an apochromatic-immersion lens it is definitely seen that the opercular mass is continuous with the chorionic ectoderm and the plasmodial mass attached to its inner surface (fig. 21). The operculum would, therefore, seem to be fetal in origin and was originally attached to the chorionic Vesicle, but subsequently tore away. This indicates how firm is the union between ectoderm and operculum. In the TeacherBryce ovum no. 2 (’24, ’25), the blastocyst is adherent to the decidua capsularis at the operculum, and the continuity of the blastocyst ectoderm with the operculum is Very clearly seen.
Linzenmeier, in 1914, and Herzog, as early as 1909, described a structure similar to the operculum without attaching much significance to it; but in 1916, Schlagenhaufer and Verocay pointed out that this area, which represented the last part of the ovum to enter the implantation site, also closed the opening made by the ovum. Teacher ,(’24, ’25) agrees with Schlagenhaufer and Verocay that the Verschluss or operculum is an invariable constituent of the human ovum and that it is a temporary structure which begins to disappear at a very early period. In most of the ova described there is no adhesion between the blastocyst and the capsularis. Under the remains of the operculum a shield of fibrin is formed which seals the inner mouth of the aperture of entrance (Teacher, ’24, ’25). This shield, like the operculum itself, disappears in the degenerated capsularis. Likewise, no mark is left on the blastocyst of the union between it and the operculum. In the Sch. ovum of v. Miillendorff (’21a) there is a mass of large cells in the decidua capsularis which v. M61lendorff regards as a degenerated embryonic rudiment, but which Teacher (’24, ’25), Grosser (’25), and P. Meyer (’24) interpret as the operculum.
According to Teacher (’24, ’25), the operculum must be regarded as a special apparatus. It is not a part of the trophoblast, although it originates from the same tissue, because it does not have the same functions as the rest of the extra-embryonic ectoderm. Peters, in a recent article (’25), attacks Teacher’s claim that the operculum, or, as he calls it, Einbruchspforte, consists only of ‘syneytium (ectoderm)’ and that only secondarily does a layer of fibrin develop toward the ovum. Peters likewise disagrees with Schlagenhaufer (’16), who maintains that in all cases there is a purely trophoblastic Verschluss, and he also takes issue with v. Mollendorff (’24), who believes the Verschluss is purely decidual.
In his contribution of 1899, Peters pointed out that in the Verschluss (operculum of Teacher) syncytium and cytoblast were both present and were mixed with blood, ‘fibrin,’ and also degenerated (maternal) capsularis cells. The capsularis immediately around the Einbruchspforte shows an unclear histological picture containing blood and ‘fibrin.’ Peters (’25) points out that occasionally the Verschluss can consist only of trophoblast, while the other elements surround it. On the other hand, the trophoblast may be so scarce that the Verschluss will consist essentially of decidua. The Verschluss is very different in the Bryce-Teacher ovum no. 1 (’08) and the V. Mollendorff Sch. (’21 a) ovum, both of which are younger than Peters’ ovum. Likewise, the Verschluss varies considerably in the ova of Schlagenhaufer (’16), P. Meyer (’24), V. Mollendorff, W0. (’24), Linzenmeier (’14), and Peters (’99).
Peters’ final conclusions regarding the controversy of the operculum which was started by Teacher’s recent contribution (’24) is that more incontestable young ova must become available for study before the origin, nature, and history of the operculum can be written.
fig. 21 Camera-lucida drawing, showing inner one-third of cperculum and chorion more highly magnified. Z-apo. immers. X 0c. 6 X 600 reduced to 450 diameters. Mallory connective-tissue stain.
fig. 22 Photograph, showing decidua basalis with trophoblast masses within a gland and a blood vessel. Z-obj. AA X 38. Phosphotungstic acid hematoxylin stain.
As has been said, the ovum was opened before dehydration. This was done under ﬂuid with iridectomy scissors, using a binocular microscope at a magnification of 10 diameters. A nearly spherical vesicle, identified as a yolk sac, was found ﬂoating free in the eXtra—embryonic coelom which contained but few delicate strands of magma. The body stalk was also found in situ (fig. 2, Bd.st.). Obviously, a break had occurred at the junction of the amniotic vesicle and the body stalk, perhaps during the abortion. These parts were afterward found to be poorly preserved as compared to the chorion. The embryo presumably lay spread out on the yolk sac, but, despite a prolonged study under the most favorable lighting conditions, nothing could be found except an occasional blood island and a low, nearly circular blister. In embedding and cutting, the yolk sac was so oriented that the sections passed vertically through the blister. This proved to be the embryonic disc and its amnion. All of the sections from one side of the slide dropped off during the staining, but the beginning and end of both yolk sac and embryo were preserved, and, as they did not collapse during the technical procedures, their dimensions and some details of structure could be made out. The former extends through forty-three sections 10 u thick and has the typical structure of an early yolk sac soon after the appearance of blood islands. The largest section (the twenty-third in the series) measures 0.64 X 0.53 mm. In comparison, the embryonic disc is very small, for it is present in only fifteen sections and measures 0.13 mm. in the fourth section of the series. It is accordingly, a slightly elongated disc and concave when viewed from above. It would seem probable that the embryo’s development was retarded or ceased entirely shortly before the abortion, whereas the membranes continued to develop normally. This is frequently seen in abortive ova. As might be expected from its small size, the embryonic disc shows no sign of a primitive streak or of mesoderm, consisting simply of a pseudostratified columnar epithelium lying upon the yolk sac and passing over more or less abruptly into the amnion. In the region of the embryonic disc, the amniotic cavity is exceedingly small; caudally, it would appear that it expands into a rather large vesicle which lies in one side of the body stalk (fig. 5, Am.V.). This is prolonged as a narrow amniotic duct into the body stalk and ends blindly near its base. The beginning of the allantoic duct cannot be made out, owing to the distortion in the region where the yolk sac and amniotic vesicles were broken from the body stalk. There is, however, a small spherical vesicle of typical endodermal cells in the body stalk just lateral to the amniotic duct which is undoubtedly the dilated end of the allantois, already separated from the rest of the duct (fig. 4, All.) as has been found in other ova of this period. The general relations of the embryo and its surroundings are not unlike those of the Teacher-Bryce no. 2 embryo (Bryce, ’24), although the form of the amnio-embryonic and yolk—sac vesicles is very different.
A young human ovum which was obtained in an aborted decidual cast is described. The measurements are given on pages 325, 326. The outstanding feature of this ovum is the unusual amount of invasion of the decidua by plasmodium. There is very abundant trophoblast, especially plasmoditrophoblast in the intervillous space. There are numerous definitive villi, some of which have begun to branch. Blood vessel anlagen are found in the mesoderm of the chorionic vesicle, the villi, the body stalk, and the yolk sac. The few preserved sections of the embryo show‘ a small amniotic vesicle and an embryonic shield lying upon a large yolk sac. In the decidua capsularis is an operculum deciduae (Teacher, ’25) which appears to consist of fetal ectoderm and is attached to the‘ chorion laeve by a strand of plasmodium. The decidual reaction is more pronounced in the stroma cells than in the glands. Some of the large veins in the spongiosa beneath the ovum communicate with the intervillous space and contain free masses of plasmodium. The development of our ovum tallies with ova considered by Grosser to have a maximum age of nineteen days.
I should like to thank Dr. George W. Bartelmez, without whose most valuable assistance this study would not have been possible.
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