Paper - A presomite human embryo (Shaw) - the implantation
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W J Hamilton, R J Gladstone A presomite human embryo (Shaw) - the implantation. J. Anat.: 1942, 76(Pt 2);187-203 PMID: 17104888
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A Presomite Human Embryo (Shaw): The Implantation
By W. J. Hamilton And R. J. Gladstone
Department Of Anatomy, St Bartholomew’s»Hospital Medical College, London
Introduction
IN a previous communication (Gladstone & Hamilton, 1941) we gave a short description of the chorionic vesicle, and a detailed account of the structure of the intrachorionic rudiment of the ‘ Shaw ’ embryo. The present communication provides a more detailed account of the chorionic villi and their method of attachment to the -implantation cavity. An accountis also given of the structure of the endometrium adjacent to the implantation cavity. The chorionic vesicle has the following diameters: Maximum external, including villi: 11 mm. Vertical external: 4-04 mm. Maximum internal: 8 mm. Vertical internal: 3 mm. . The wall consists of an inner mesodermal layer (a description of this tissue is given in our previous paper), a cytotrophoblastic or Langhan’s layer, and a syncytiotrophoblastic layer. Projecting from the surface of the vesicle throughout its extent are villi; these are more differentiated and longer at the
circumference than at the poles of the chorionic vesicle. The villi may be '
divided into three parts, a proximal part which has_ a mesodermal core, a short intermediate part which is densely cellular, some of the cells of which are continuous‘ with _ the cytotrophoblast, and a distal part composed of loose columns of cytotrophoblastic tissue. There is a layer of syncytiotrophoblast of varying thickness on the sides of the villi.
As there is some confusion in the literature on the nomenclature of the different parts of the trophoblastic tissue we give here an account of the terms which we use:
Plasmoditrophoblast we regard as the primary plasmodium seen at the early stages of implantation, e.g. Miller, T.B. 1, Peters, and other early embryos; it corresponds to the implantation syncytium of Grosser’s classification (1927) and to the plasmo- dium of Florian (1928). After implantation it undergoes retrogression and, in the present specimen, only remnants of it are present. -
Syncytiotrophoblast has been divided into villous syncytiotrophoblast, which covers the villi, and peripheral, which is found on the trophoblastic shell and lining the implantation cavity; it correspondsto the resorptive syncytium of Grosser (1927) and Florian (1928).
Cytotrophoblast, following the description of Ramsey (1938), has been subdivided into central cytotrophoblast, or Langhan’s layer, and peripheral, or cytotrophoblast of the cell columns and trophoblastic shell. This is regarded as a second generation of cytotrophoblast by Grosser (1927).
The trophoblastic shell is recognized as the layer of cytotrophoblastic tissue, of varying thickness, which lines the implantation cavity" including the decidua capsularis. .
Peripheral syncytium is regarded as the tissue which invades the maternal tissue and which is situated outside the trophoblastic shell. It corresponds to the syncytial sprouts of Hill (1932) and the proliferation plasmodium of Florian (1928). It is typically found outside the border, or penetration zone, or the foetal-maternal border, of Wislocki-& Streeter (1938).
The Implantation Cavity
A general view of the specimen shows that the walls of the implantation cavity have been torn, more especially on the superficial aspect and at the sides (Pl. 1, fig. 1). At one side the decidua capsularis has been torn away from the tips of the chorionic villi and has become folded and broken. A large fragment includes nearly the whole of the ‘operculum deciduae’ and the zone of the decidua capsularis surrounding the infiltrated fibrinous plug which has sealed the aperture of entry. On‘the deep aspect or placental side of the chorionic vesicle the wall of the implantation cavity is formed by an incomplete layer of cytotrophoblastic cells. Syncytiotrophoblast covers the foetal aspect of the cytotrophoblastic lamina, and scattered plasmoditrophoblast masses are found over and amongst these cells. A large cleft, the maternal sinus, separates the cytotrophoblastic lamina from the maternal decidua basalis. The maternal sinus, which is lined with endothelium in some areas and in others by flattened trophoblastic cells, opens into intervillous spaces.
Since considerable variations exist in the structure of different parts of the wall of the‘ implantation cavity, it is desirable to consider these parts under separate headings, namely: (1) A basal or placental area. (2) A marginal zone or circumferential part of the decidua capsularis, forming the lateral walls of the implantation cavity. (3) The central part of the decidua capsularis or superficial wall next the lumen of the uterus, comprising the ‘ operculum deciduae’, the infiltrated fibrinous plug, and the circular zone of the decidua capsularis surrounding the ‘aperture of entry’.
(1) The basal or placental area. A wide space, the basal sinus, separates
the outer wall of the implantation cavity from an incomplete lamina which is
formed by fused plates of cytotrophoblastic tissue uniting the tips of the villi.
These plates arise from, and are continuous with, proliferating cells constituting
the cell columns which grow outward from the tips of the villi. The cells at the
base of the cell columns are continuous with the central cytotrophoblastic layer
of the villi (Pl. 1, fig. 2). The central cytotrophoblastic cells lining the bases
of the villi are cuboidal and are continuous with the similar cells in the chorionic
wall. They have a large, round nucleus, with a distinct nucleolus, and a small
amount of pale cytoplasm; mitoses are frequently found in these cells (Pl. 2,
fig. 3). The cells of the peripheral cytotrophoblast which form the cell columns
and the cytotrophoblastic lamina vary in size, those close to the tips of the
villi being smaller than the more peripherally situated cells. The cell boundaries are less clearly defined, the nuclei are paler and often irregular and are sur-
rounded by ‘a dark band‘ of cytoplasm outside of which there is a clear space
(Pl. 2, fig. 5). Mitoses are not frequently observed in these cells.
The central cells are covered by a complete layer of syncytiotrophoblast, patches of which are occasionally included in the cytotrophoblast. Remnants of degenerating maternal tissue are rarely to be found among the cytotropho- blastic cells and occasional leucocytes are also present. The syncytiotrophoblast of the villi and chorionic wall varies in thickness in different villi; in some areas the outer border contains small vacuoles giving it a foamy appearance; in other areas large vacuoles are found (Pl. 2, figs. 3, 4). The syncytiotrophoblastic layer stains more darkly than the cytotrophoblast cells. A typical‘ brush border ’ was observed in many parts (Pl. 2, fig. 4); in others it is indistinct or absent.
Text-fig. 1. Remnants of the plasmoditrophoblast, or primary plasmodium of the implantation. Note large and small vacuoles and pycnotic nuclei in process of disintegration. x c. 550.
The nuclei vary in size and are irregular in shape; where the layer is thin they
are flattened. Only very rarely are mitotic figures seen. A distinct nucleolus
is present. In some situations the syncytiotrophoblastic layer shows indefinite
cell boundaries (Pl. 2, fig. 3). The isolated masses of plasmoditrophoblast stain a deep pink colour with eosin, often with a lavender tint. Many small vacuoles and well-formed nuclei are present in certain of these masses, while other pieces contain large vacuoles and degenerating nuclei (Text-fig. 1). Large, apparently
anuclear, masses are also present. Occasionally engulfed maternal blood cells
and other maternal tissue are found within the masses. No transitional stages between the syncytiotrophoblast and the plasmoditrophoblast can be demon-
strated.
The greater part of the uterine wall of the sinus is lined by a single layer
of epithelioid cells continuous with the endothelium lining maternal vessels
which open into the sinus (Pl. 1, fig. 2). Areas, however, are present which are covered by laminated masses of fibrin. In some places the epithelioid layer
lies beneath a laminated fibrinous deposit, and in others the fibrinous deposit
is infiltrated with nuclei indicating commencing organization of a_. clot which
had been deposited during life. Where anchoring villi are seen directly attached
to the decidua, near the circumference of the placental zone, there is no large
continuous space or sinus, the intervals between the attachments of the villi
being simply radiating clefts, lined by syncytiotrophoblast, which extend a
short distance into the maternal tissue in the 'z5he of penetration. It is probable,
therefore, that, in the living state, the space existed as a cleft which was
capable of opening up into a sinus containing a variable amount of maternal
blood which was in direct contact with the syncytiotrophoblast lining the
uterine wall of the sinus as well as with that covering the villi and the outer
wall of the chorionic vesicle.
The outer boundary of the sinus shows a number of rounded swellings separated by grooves or depressions into the bottom of which capillary vessels, and spaces lined by endothelium, are seen to open (Pl. 1, fig. 1; Pl. 4-, fig. 10).
The endothelium lining these vessels is continuous with a single layer of
syncytiotrophoblast which in most places covers the summits of the swellings.
The character of this epithelial lining is, in general, that of an attenuated layer,
the nuclei and cytoplasm both being stained a deep purple colour and with
no visible cell outlines; the nuclei of the tissue covering the summits of the
swellings are as a rule larger and more rounded than the nuclei of the endo-
thelium lining the capillary vessels and vascular spaces. Further, there is
direct continuity of the thick layer of syncytiotrophoblast, which covers the
sides of adherent ‘anchoring’ villi, with the thin stratum of epithelium lining
A the outer wall of the sinus. These anchoring villi are most numerous at the circumference of the sinus where the villi are firmly adherent to the decidua,
whereas, in the central region, they are united together at their surfaces by
expansions from the cell columns to form cytotrophoblastic laminae.
In some places the syncytiotrophoblast lining the uterine wall of the sinus is seen to be continuous with the epithelium of distended and degenerating uterine glands which have been opened up by the formation of the implantation cavity (Pl. 4-, fig. 8). Many of these glands are greatly elongated and displaced, so that their long axes lie parallel to the outer wall of the sinus. Since their much enlarged lumina often contain blood as well as secretion, it is probable that when, in the earlier stages of the embedding process, the inter glandular tissue in the ‘necrotic zone’ breaks down, the opening up of their lumina contributes to the formation of the cavity of the sinus. In many places groups of chorionic villi are attached to a thin plate of cytotrophoblastic tissue, covered by syncytiotrophoblast, which intervenes between the cavity of the sinus externally and the intervillous space internally, that is, on the side turned towards the wall of the chorionic vesicle. This clearly_ indicates, in our opinion, that a cleft has been formed by the breaking down of the spongytissue composing the ‘necrotic zone’ described by Bryce & Teacher (1908) in the earlier stage of development which follows the initial entry of the blastocyst. At the stage reached by the specimen we are describing, the necrotic tissue which formed the solid part of the sponge-work has broken down and has been‘ supplanted by thin plates of cytotrophoblast covered by syncytiotrophoblast, which join the tips of small groups of chorionic villi and which contribute to the formation of the trophoblastic shell. Also at this stage both walls of the sinus are covered by syncytiotrophoblast which is thicker and more typical in structure where it covers the outer surface of the thin plates attached to the tips of the villi than externally where it is attenuated and in some places defective.
In the region of the sinus, and in relation with the outer or parietal wall of
the implantation cavity in the future placental area, we can distinguish three
surfaces which are disposed in concentric planes relative to the outer wall of
the chorionic vesicle. These surfaces are: (1) The outer wall of the intervillous
space. The thin plates to which the tips of groups of anchoring villi are attached
are, in the vicinity of the villi, lined by syncytiotrophoblast. (2) The outer
surfaces of the thin plates of cytotrophoblast are also partly covered by
syncytiotrophoblast, more particularly where this has apparently grown round
the edges of the gaps between the plates; elsewhere it is bare or covered by
a single layer of endothelium-like cells, suggesting the formation of the sinus
by the opening up of vascular spaces as well as by the inclusion of dilated
uterine glands and breaking down of necrotic tissue. Bare areas are also
present which are sometimes covered by blood clot or a fibrinous coagulum
tinged with eosin and containing disintegrated red blood corpuscles and leuco-
cytes. The third surface is the outer wall of the sinus. The syncytiotrophoblast
lining_the latter also varies in different places. In the clefts between the
rounded swellings, where capillary vessels open into the sinus, the latter is
lined by endothelium; where uterine glands have been opened up the epithelium
lining the sinus is continuous with, and resembles, the glandular epithelium.
In other places there are definite patches of plasmoditrophoblast giving origin
to plasmodial strands which radiate outwards into the uterine tissue beyond
the sinus where it may be seen opening up distended and degenerating glands,
and extending into congested capillary vessels and vascular spaces.
_ (2) The marginal zone or circumferential part of the decidua capsularis
forming the lateral walls of the implantation cavity. The marginal or circum-
ferential part of the decidua covering the sides of the chorionic vesicle differs
from the decidua basalis in being more dense and uniform in general appearance.
The uterine epithelium on the surface is a simple layer of cubical and flattened cells beneath which are aconsiderable number of lymphocytes. The stroma
dilfers from that of the decidua basalis in the sparseness of the glands, only
remnants of which are present. The epithelium _of the glands shows varying
stages of disintegration and in some cases has completely disappeared. In
other places the walls consist merely of flattened cells of mesothelial type-
On reaching the angle between the marginal and the parietal deciduae the lateral blood sinus divides into two branches of which one extends into the
adjacent part of the decidua parietalis and the other is prolonged into the
decidua marginalis and, by further extension and subdivision, into the peripheral part of the decidua capsularis. The sinuses are lined by flattened endothelial cells and contain blood coagulum, palely stained with eosin, in which
are embedded scattered leucocytes and degenerated erythrocytes. The stroma
contains a large number of round, oval and branched decidual cells which
extend throughout the whole thickness of the stroma and are characterized
by their large size, the pink colour of their cytoplasm, and their large, round
nuclei (Pl. 3, fig. 7). The nucleus is palely stained by haematoxylin, the nuclear
membrane is delicate and there is a fine nuclear reticulum showing usually a
nucleolus and slight nodal thickenings. Numerous lymphocytes and leucocytes
are present in the stroma and are "most numerous beneath the uterine epithelium
and around the blood sinuses. The stroma nearer the chorionic vesicle is denser
and more uniform in appearance than it is nearer the surface and beneath the
uterine epithelium, where it appears to be oedematous. The decidua marginalis
is limited on its inner or chorionic surface by an incomplete layer of cytotrophoblast and some plasmodial remains. The tips of the elongated circumferential villi have become detached in many places, the points of attachment
being merely indicated by bare areas or a few cytotrophoblast cells adhering to the inner surface of the decidua (Pl. 3,_ fig. 6). Syncytial processes extending into the marginal decidua are frequent and are best seen near the junction of the marginal with the central part of the decidua capsularis (Pl. 3, ‘fig. 7). These syncytial processes vary in shape andlare darkly stained in contrast to the more lightly stained decidual cells.
(3) The central part of the decidua capsularis, including the ‘ operculum ’ and
the region surrounding the aperture of entry. The epithelium on the surface of
the decidua capsularis consists of a single layer of low cubical or polygonal
cells which are continuous with similar cells of the marginal zone; the cell bodies
are stained pink with eosin, the cytoplasm being coarsely granular and fre-
quently showing vacuoles which are most frequent in the vicinity of the nucleus
and near the free border of the cell. The outlines of the cells are ill-defined and
there is no definite basement membrane. The nuclei are stained a deep purple
and are round or oval in outline. Mitotic figures are rarely seen, but lympho-
cytes lying in pairs close together are common immediately beneath the
epithelial cells or, in some places, between the cells.
In the compact tissue beneath the epithelium are numerous decidual cells;
these appear either as isolated cells or in groups and columns. The existence
of the decidual cells is in most places associated with the presence of numerous
lymphocytes and leucocytes in the supporting connective tissue. The inter-
glandular connective tissue appears to have broken down in places, and in
others to have been replaced by decidual cells. The presence of decidual cells
at this stage of development is not limited to the zone immediately surrounding
the implantation cavity, these cells being found also in the decidua parietalis, a small portion of which, in our specimen, is in continuity with the decidua
capsularis. ‘
On approaching the region of the closed aperture‘of entry the uterine epithelium tends to become flattened. Transitional stages occur between a single layer of evenly disposed cubical cells and one of irregularly shaped flattened cells which is spread out over the stratum compactum. The cells here show signs of degeneration and appear to be stretched over the underlying compact layer. In some places the epithelium is absent, leaving bare areas limited by a stratum of condensed connective tissue, or ‘ basement membrane ’.
Beneath the surface layer of uterine epithelium apparently isolated cells
or small multinucleated masses of syncytium are occasionally visible and.also
a considerable number of lymphocytes and polymorphonuclear leucocytes;
the stroma contains numerous decidual cells (Pl. 3, fig. 7). The latter, however,
diminish in number as the aperture of entry is approached. Further, in this
region all traces of the uterine glands have disappeared and the stroma becomes
denser and less vascular. It is infiltrated with extravasations of blood and
fibrinoid material and‘ contains a large number of lymphocytes. The deep
surface of the decidua capsularis is covered by cytotrophoblastic cells which
are several layers thick in places, while in other areas they only appear as
scattered cells. They line part of the trophoblastic shell.
The ‘operculum deciduae’, or closing plate. This is a flattened disc-like
structure the margins of which spread out from the site of the original aperture
of entry over the uterine epithelium which covers the stratum compactum of
the decidua capsularis. The exact size of the operculum is diflicult to determine
as, in the sections, the edge of the disc on one side is seen to be adherent to the
surface of the decidua capsularis and to thin out gradually into an indeterminate
border, whereas on the other side, where it is still separate from the decidua,
the border is folded. Further, the lengths of the diameters at right angles to
the planes of the sections cannot be estimated with certainty since the edge
of the operculum extends on both sides beyond the area contained within the
block. The number of serial sections (which were cut at a thickness of 10p.)
is 263. This gives a minimum diameter in a plane at right angles to that of the
sections of 2-63 mm. The greatest horizontal diameter of the disc, obtained by
measurements from sections on the slides, is approximately 3 mm. Thus,
assuming that the disc was roughly circular in outline, and allowing 0-37 mm.
for the missing edges of the disc which were not included in the block, the
average length of the diameters passing through the centre of the disc would
be approximately 3 mm., or about one-third of the maximum diameter of the
chorionic vesicle.
The operculum is seen in all the sections to rest on the surface of an accidentally detached fragment of the decidua capsularis. One edge of this fragment appears to have been torn from the circumferential part of the
decidua capsularis a short distance from its junction with the decidua parietalis;
here the torn edges of the two parts of the decidua capsularis which are slightly
194 ‘ W. J. Hamilton and R. J. Gladstone
separated are seen to correspond. The other end of the fragment-gradually tapers to a free border which is at a considerable distance from the free border of the torn decidua on the corresponding side (Pl. 1, fig. 1). The wide gap between these two edges is occupied by a part of the wall of the chorionic vesicle, and from the latter project the elongated branched villi which characterize the circumferential zone of the vesicle. The tips of these villi are joined by thin plates of syncytiotrophoblast forming the trophoblastic shell, which are similar to the plates which have been previously described in the region of the decidua basalis. The superficial surface of these plates, however, although covered in some places by a syncytial layer, is in the greater part of its extent bare; it appears to have been torn away from the superficial layer of a missing part of the decidua capsularis which would have covered the exposed part of the chorionic vesicle. ‘ ’
The operculum consists of a hyaline fibrinoid material stained a yellowish pink colour with eosin and containing irregularly disposed, deeply stained, pycnotic nuclei (Pl. 4.-, fig. 9). These are round, oval, or rod-shaped, and vary in size, some being comparable to the nucleus of a small lymphocyte, though a cytoplasmic zone around the nucleus is seldom recognizable. Other nuclei are flattened and are seen mostly on the free surface; these resemble the nuclei of a mesothelium, while others which are larger in size appear to be the nuclei of degenerating plasmoditrophoblast. N_o vessels are visible, although where the operculum has become adherent to the decidua, ingrowths are present on its deep surface which resemble angioblastic strands and indicate a commencing organization of the fibrinoid material. Degenerating red blood corpuscles are visible in some places, and in some places also the ground substance or matrix is laminated, suggesting that the structure has originated as a blood coagulum which has become infiltrated with leucocytes and is undergoing degeneration and absorption. It is probable that the adherent portions of the operculum would have been replaced by scar tissue, while the outlying and circumferential free parts which do not receive any blood supply would have disintegrated and been cast off into the lumen of the uterus.
Comments and Comparisons
It is not our intention to enter into a detailed discussion of different phases of implantation, but only“ to deal with the more recent relevant literature. A statement on the age of the embryo was given in our previous communication. The assumed fertilization age of the embryo, from the patient’s history, was estimated to be between 20 and 23 days. The embryo was found, however, to be much younger than its supposed fertilization age and was estimated to be at about the 17th or 18th day of development, i.e. at approximately the same stage of development as the Wa 17 (Grosser, 1931) and younger than the Jones & Brewer (1935). The chorionic villi show a stage of development and difi"erentia- tion comparable to embryos of the Group E of Bryce’s classification (1924), and this group would also include the additional embryos, Hugo (Stieve, 1926),
Cite this page: Hill, M.A. (2024, April 16) Embryology Paper - A presomite human embryo (Shaw) - the implantation. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Paper_-_A_presomite_human_embryo_(Shaw)_-_the_implantation
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