Paper - The chorion and endometrium of the embryo H.R.1.

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Johnston TB. The chorion and endometrium of the embryo H.R.1. (1941) Amer. J Anat. 75: 153-163.

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See also by the same author Johnston TB. An early human embryo, with 0.55 mm. long embryonic shield. (1940) J. Anat., 75:1-49.

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The Chorion and Endometrium of the Embryo H.R.1

By T. B. Johnston

Guy’s Hospital Medical School

In the preceding number of this Journal a detailed description was given of the [[|Paper - An Early Human Embryo, with 0.55 mm long Embryonic Shield|Embryo H.R. 1]]; the present paper deals with the chorion and the endometrium of this embryo.

The Chorion

The fixation and preservation of the constituent parts of the chorion were, not unnaturally, still better than the fixation and preservation of the embryo itself.

The primary mesenchyme which lines the chorion, and extends into the chorionic villi and their branches, is everywhere closely applied to the cytotrophoblast. As will be seen from the figures already published no shrinkage has occurred, and in this respect the tissues are as well preserved as they were in the Strahl-Beneke (1910) and the Hugo (Stieve, 1926) embryos.

The constituent cells of the mesenchyme exhibit many variations in form, but the majority are elongated and lie with their long axes parallel to the cytotrophoblast both in the chorionic wall and in the interior of the villi. (1) Fusiform cells with branching processes at each end are very numerous (Text-fig. 1). They tend to occur in short strings of two or three, especially in the villi. Their nuclear structure is distinct; the nucleolus is prominent and the chromatin network is clearly shown, although it is not darkly stained. (2) Elongated, rod-like forms also are numerous. Their nuclei stain so darkly that their structure cannot be made out. These cells also tend to occur in short strings which suggest the angioblastic strands described by Maclntyre. (3) Smaller, rounded, cells with deeply staining nuclei and scanty cytoplasm form a less numerous group. (4) In addition, short rod-like forms occur with deeply stained nuclei. They may be the earlier stages of group (2), or they may be cells of group (2) which have been cut obliquely to their long axes. (5) Within the villi, and in places in the chorionic wall, large mesoblasts with oval nuclei and branching protoplasmic processes are common. Their nuclear structure is clearly shown and they appear to represent early stages of the cells in group (1).

No indubitably vascular spaces and no blood-islands are present in any part of the chorion, although angioblastic strands, of rather doubtful identity, were recognized in the apical region of the chorion. Hertig (1935) has recently put forward the view that both mesoblasts and angioblasts are direct derivatives of the cells of the cytotrophoblast and claims to have recognized angioblastic strands in the mesenchyme of the Miller ovum. If his interpretation is correct, it is strange that no obvious angioblastic tissue can be identified in the chorionic mesenchyme of H.R. 1 and that such as is present has not developed in the interval between the. two stages, for the H.R. 1 is certainly at least two and not improbably three or even four days older than the Miller ovum. At the same time it must be remembered that H.R. 1 required to be reblocked after the chorionic-cavity had been opened and it is possible that in the process the superficial parts of the chorionic mesenchyme might have suffered injury or loss. In this way the absence of the mesothelial layer, which Maclntyre (1926) has described as present in embryo T.B. 2, may be accounted for, because it is only in a few places that cells are present which are worthy of the name “mesothelial”.

File:Johnston1941 text-fig01.jpg

Text-fig. 1. Primary mesenchyme of a chorionic villus, showing numerous fusiform and branching cells. x 950.

The chorionic villi cover the whole of the outer surface of the chorion. They are longest and most crowded together in the region of the decidua basalis, where they average 0-6 mm. in length. In this situation they show fewer branches than in the lateral walls of the chorion, where they tend to be both broader and shorter. Being more widely spaced they are able to branch freely and as many as 10-12 branches may arise from one villus. In the region of the decidua capsularis the villi are shortest and measure on the average 0-2 mm. They are narrower than the villi in the lateral walls and show fewer branches.

The cells of the mesodermal cores of the villi are specially well preserved and show numerous branching and anastomosing processes. Fusiform cells predominate and arrange themselves in the long axis of the villus or its branches.

The Cytotrophoblast forms an easily recognizable layer over the whole surface of the chorion and the chorionic The cells are regularly arranged The chorion and endometrium of the embryo H .R. 1 155 and show little variation in size. It is a curious fact that although most of them possess nuclei with a clearly defined chromatin network, many of them exhibit darkly staining pycnotic nuclei in which no trace of structure can be discerned.

From the apices of the villi typical cell columns are continued into the trophoblast shell which forms the outer boundary of the intervillous space. The cells in these columns vary considerably in size. The smaller cells are found at the apices of the villi, where they are closely crowded together. The larger cells are found in the trophoblast shell and show large intracellular shrinkage spaces (Pl. 1, fig. 1). In addition the chromatin network of the nuclei is irregularly disposed and appears to have undergone shrinkage in many places, leaving clear areas which are unstained. The appearance indicates that many of these cells are undergoing degenerative changes. It is certain that at the apices of the villi the cell columns are actively growing and it is a curious fact that in nearly 400 sections only a few, very doubtful, mitotic figures were seen. Florian (1928) has suggested that the nuclei in the plasmodium increase by amitosis, and the absence of mitotic figures strongly suggests that the same process is the normal method of cell division in the cytotrophoblast.

The plasmodial trophoblast. The cytotrophoblast of the chorionic membrane and of the chorionic villi is everywhere covered with a thin layer of resorption plasmodium (Florian, 1928). It is this layer which is bathed with the maternal blood in the intervillous space and through which all the nutritive substances must pass before they can reach the embryo. It has the appearance of a very fine foam, and its free surface shows the well-recognized “brush border”. The contained nuclei are irregularly spaced, and tend to be flattened against the cytotrophoblast. For the most part they are darkly staining and their structure is diflicult to discern. No mitotic figures were seen, but, on the other hand, no dumb-bell forms, such as Florian has described, were encountered.

The cytotrophoblast of the cell columns is covered for the most part with plasmodium, but there are many patches where no covering plasmodium is visible and the chorionic surface of the cytotrophoblast shell is in direct contact with the maternal blood of the intervillous space.

Islands of free plasmodium are found in the intervillous space. They are usually pale in colour; the fine foam is coarser in character and contains numerous vacuoles; and the contained nuclei show obvious retrogressive changes. In many of these islands the nuclei are dark and pycnotic and have lost their regular outline; in others the nuclei are swollen and hydropic, are pale in colour, and contain only a nucleolus and some shrunken shreds of chromatin. They areobviously in process of dissolution. Although they occur generally throughout the intervillous space, they are few in number under the decidua basalis and numerous under the decidua capsularis.

Areas of healthy looking plasmodium occur in the midst of the trophoblast shell and around the periphery of the shell in contact with the endometrium. Many of these areas line slit-like spaces in the shell (Pl. 1, fig. 3), but others appear to be surrounded completely by the cytotrophoblast. Where a free surface presents itself for examination, the “brush border”, which is so characteristic of the “resorption plasmodium”, is absent or inconspicuous. Florian (1928) has termed this the “proliferative plasmodium”, as he believes that it differs materially in its function from the “resorptive plasmodium”.

Both in the trophoblast shell and in the peripheral zone the strands of proliferative plasmodium are easily recognized on account of their distinctive staining reactions. The nuclei stain so darkly with haematoxylin that their structure can be made out only with difliculty, while the surrounding plasmodium stains reddish pink with eosin. In the peripheral zone, particularly, the nuclei are elongated, being fusiform or rod-like, and the associated plasmodium is drawn out into strands in the long axis of the-nucleus. Some of these strands contain three or four nuclei end to end and _appear to be actively streaming into the endometrium (Pl. 1, fig. 1). In the maternal tissues they are found at considerable distances from the trophoblast shell. In these situations it is exceedingly difficult to convince oneself that they form part of an open-meshed plasmodial network and are not independent units. They can be seen in contact with the walls of the maternal blood Vessels and uterine glands, and the adjoining maternal cells present the appearances of incipient degenerative changes. Occasionally the nuclei of these plasmodial strands are V- orY-shaped, and in places they lose their elongated shape and become irregularly quadrangular. In the latter case the surrounding plasmodium adapts itself to the altered shape of the nucleus. In many situations one strip of plasmodium contains two elongated nuclei lying side by side, and these forms, together with the V- and Y-shaped nuclei, give support to Florian’s view that in the plasmodial trophoblast amitotic nuclear division is the rule. The Y-shaped nuclei represent the first stage, the V-shaped nuclei the second, and the side-by-side nuclei the third and completed phase of the process.

The proliferative plasmodium can be seen in close relationship with the uterine vessels, which it is presumably attacking. The walls of the arterioles concerned are thickened and their lining endothelial cells are swollen. In many places the proliferative plasmodium has replaced the endothelium lining the wide venous sinuses which surround the ovum, and in these situations its margin is always clear cut and no “brush borders” are apparent.

Within the trophoblastic shell there are numerous straight channels which are parallel to the veins in the adjoining part of the stratum spongiosum. They are lined for the most part with the proliferative plasmodium (Pl. 1, fig. 3), but here and there small patches retain a lining of endothelium. These spaces and the presence of proliferative plasmodium in the walls of the venous sinuses immediately outside the trophoblastic shell suggest that, after the implantation of the ovum, the implantation cavity is enlarged, in part at least, by the incorporation of the adjoining venous sinuses. The mechanism of the process appears to be as follows. Strands of proliferative plasmodium attack the walls of the vessel, destroy and replace the lining endothelium. The trophoblastic shell enlarges at the expense of the intervening maternal tissues until the sinus becomes separated from the intervillous space only by the proliferative plasmodium "and the trophoblastic shell. Degenerative changes occur in the trophoblast so that new spaces areformed which enable the sinus to communicate with the intervillous space. A new trophoblastic shell is then formed on the opposite side of the sinus, which gradually loses its identity, becoming merged eventually in the intervillous space.

File:Johnston1941 text-fig02.jpg

Text-fig. 2. The apical part of the triangular chorionic cavity and the adjoining part of the stratum spongioeum, showing the absence of the “saw-teeth" appearance in the uterine glands in the immediate vicinity of the ovum. x 30.

The Endometrium

The uterine mucosa presents the typical appearances associated with an early pregnancy. The compact and spongy layers are quite characteristic.

The glands of the stratum spongiosum are enormously dilated and full of secretion, and in the vicinity of the ovum some contain extravasated blood. The lining epithelium displays the “saw-teeth” appearance, except in the immediate neighbourhood of the ovum, where the walls of the glands are much less irregular than they are elsewhere (Text-fig. 2). Presumably these glands have been subjected to considerable internal pressure, for their lining epithelium is flattened in many places and in some situations has disappeared.

The functional significance of this excessive glandular enlargement has been discussed recently by F alkiner (1932). Like many other writers he accepts the view that the secretion of the uterine glands provides nourishment for the ovum after it reaches the uterine cavity and prior to implantation. It is, however, a commonplace that in tubal and ovarian gestations the ovum may develop and form a normal embryo, although it is then unable to benefit by the secretion of the uterine glands. Again, the degree of dilation and the amount of the secretion are out of all proportion to the amount of nourishment required by the ovum. It is clear therefore that the production of “ embryotrophe” is not only not the principal function of the glandular activity but that it is very doubtful indeed whether the ovum derives any nourishment from this source. In addition to the function of producing “embryotrophe”, Falkiner ascribes to the glandular enlargement certain mechanical functions. He believes that it exerts “a definite efi'ect on the blood supply at the commencement of pregnancy, favouring the formation of a venous sinus”. With this view the appearances in the stratum spongiosum of H.R. 1 are in complete agreement. The compression exerted by the enlarged glands in the immediate vicinity of the ovum on the venous return from the area is seen in a large number of the sections, and undoubtedly helps to determine the character of the circulation in the intervillous space, which will be considered later in this section. In addition, Falkiner ascribes to the glandular enlargement the function (1) of forming a layer impervious to the action of the trophoblast, (2) of providing a natural line of cleavage, and (3) of providing a layer from which the mucous membrane may be regenerated post partum. That the glandular epithelium is very resistant to the destructive action of the proliferative trophoblast can be inferred from the appearances in numerous sections of H.R. 1. In many situations, ducts, surrounded by a small amount of stroma, are almost isolated by the trophoblast from the rest of the endometrium. Where “ peninsulas ” of the mucosa occur, they almost invariably contain ducts.

The stratum compactum is infiltrated with a large number of small round cells which are obviously lymphocytes. No typical decidual cells are present. Small areas of localized oedema, which tend to spread into ‘the more superficial parts of the stratum spongiosum, are a prominent feature. In many situations these areas are traversed by small veins which contain a disproportionately large number of white blood corpuscles (Text-fig. 3). A similar condition has been noted in the endometrium by Stieve, Falkiner and many other observers. Sandison (1932) has shown that white blood corpuscles may occur in unusually large numbers in “ any uncontracted blood vessel in which the circulation has temporarily ceased, but which remains connected with other circulating vessels”. This phenomenon is therefore associated with extremely sluggish circulation, and attention must be drawn to the evidence of such a type of circulation in the immediate neighbourhood of the ovum.

Large, thin-walled, venous sinuses are found in all young human ova closely adjoining the implantation cavity. They communicate freely with the intervillous space; they communicate with one another; and they are drained by a number of very large veins. One of these sinuses is shown in P1. 1, fig. 2. It is placed deep to the decidua basalis and three veins are shown leading from it into the deeper layers of the stratum spongiosum. Falkiner (1932) has suggested that these sinuses owe their origin to the pressure of the dilated glands on the neighbouring veins, and the appearances in the embryo H.R. 1 certainly support his view.

File:Johnston1941 text-fig03.jpg

Text-fig. 3. The deepest part of , the stratum compactum in the neighbourhood of the ovum. In the lefi half of the figure a vein is shown cut obliquely as it lies between two uterine glands. Note the patch of oedema which surrounds its upper and lower ends. In~the right half of the figure one of the tortuous arterioles has been cut in several places. The stroma by which it is surrounded is non-oedematous. x 100.

If we now turn to a consideration of the arteries in the stratum compactuln, we find a very diiferent picture. Barthelmez (1931) and Daron (1936) have shown that, apart from some minute branches which are restricted to the deepest part of the stratum spongiosum, all the arteries follow a very tortuous course, so that the same vessel is cut in many places in the same section. This character makes the arteries easy to identify but diflicult and tedious to trace. They run in the interglandular tissue surrounded with a sheath of stroma, whereas the veins run in close relationship to the walls of the glands and have little or no surrounding stroma in the stratum spongiosum. In the vicinity of the trophoblast shell in H.R. 1 the tissue around the smaller arteries shows no signs of oedema (Text-fig. 3) as compared with the tissue around the smaller veins. The arterioles themselves are the subject of attack from the proliferative trophoblast and show resulting changes. Their walls are noticeably thickened and the thickening involves both the endothelial lining and the outer walls. Despite a very prolonged search I was unable to trace any of these arterioles into the intervillous space or into any of the venous sinuses. In many situations small branches of the arteries almost succeeded in reaching the intervillous space but their ends were always occluded and usually sealed 011‘ by fibrin. A similar fibrinous change was found in several of the larger arteriolesiin the stratum compactum in the immediate neighbourhood of the ovum (Textfigs. 4, 5).

File:Johnston1941 text-fig04.jpg

Text-fig. 4. A small arteriole in the stratum compactum close to the trophoblast shell, which lies to the right in the figure. The lumen of the vessel is partially occluded by clotted blood and the walls of the patent portion show extensive fibrinous changes. x 960.

Although no arterioles were found opening into the intervillous space or the adjoining venous sinuses, a number of dilated capillaries were found in the decidua capsularis which undoubtedly established communications either directly or indirectly with the intervillous space. These capillaries contain the normal proportion of white to red cells and their _walls are not conspicuously thickened.

Falkiner succeeded in tracing one arteriole into one of the sinuses, and Stieve (1926) has figured a vessel, which he identifies as a small artery, opening indirectly into intervillous space. He states further “Die Einmiindung der Arterien in die weiteren Blutraume lasst sich an mehreren Stellen gut beobachten”. Nevertheless, he concludes that the circulation in the intervillous space and in the sinuses is exceedingly slow.

File:Johnston1941 text-fig05.jpg

Text-fig. 5. The same arteriole as in Text-fig. 4, five sections (25 u.) later. It is now’ completely occluded and sealed off with fibrin. x 960.

In H.R. 1 the blood in the intervillous space and the sinuses must have been almost stagnant. Only a relatively small number of capillaries could be traced into the space so that the inlet must have been negligible. The sealing ofi‘ of the small branches of the arteries seems to be a precaution to prevent a rapid circulation at this stage. Indeed, the areas of patchy oedema, the disproportionate number of Ieucocytes in the superficial and many of the deeper veins, the size of the venous sinuses, the sealing of of the arteries, and the capillary type of inlet, all point in the same direction. They indicate that, prior to the formation of blood vessels in the chorionic villi, and the establishment of the chorionic circulation, efficient nutrition of the embryo can only be ensured provided that the circulation in the intervillous space is so slow that the contained blood is practically stagnant.

One must not, however, overlook the fact that far more than adequate provision is made for the venous drainage of the sinuses and the intervillous space. The presence of so many large and intercommunicating veins leading away from the immediate neighbourhood of the ovum suggests that the establishment of free circulation in the intervillous space at a later stage is not a gradual but rather a comparatively sudden process and ensures that increased entry of blood into the space, no matter how extensive, will not overtax the carrying capacity of the outlets.

The point of entry of the ovum was not identified. A large part of the decidua capsularis is covered with a substantial and comparatively recent blood-clot. Where it is exposed on the surface it is covered with cubical epithelium, which, however, is not in a very good state of preservation. In its central part, where the point of entry probably was situated, a sheet of fibrinoid substance, staining well with eosin, forms nearly the whole thickness of the decidua. Its deep surface is covered, for the most part, with plasmodial trophoblast, but some shrinkage has apparently occurred in this region and has resulted in the separation of the trophoblast from the decidua. This sheet of fibrinoid substance is penetrated by strands of proliferative trophoblast and here and there contains broken-down cells which are apparently duct epithelium and stroma cells. In the peripheral part of the decidua capsularis the stroma cells become more numerous but are still intermingled with strands of proliferative trophoblast. The remains of ducts are easily recognizable and numerous dilated capillaries are present. The endothelial cells of these small vessels are slightly swollen and they are replaced in many situations by single units of the trophoblast. They contain a normal proportion of red blood corpuscles and many of them open into the venous sinuses or the intervillous space. In this part of the decidua capsularis small groups of lymphocytes are frequently to be observed.

In the peripheral zone it is not, as a rule, difficult to differentiate the foetal from the maternal tissues, although there is nowhere any necrotic zone such as is present in earlier stages, e.g. T.B. 1 (Bryce, 1908) and von Mo1lendorff’s Sch. (1921). Here and there fibrinoid patches are encountered and the maternal cells for the most part show signs of degenerative changes. The ducts appear to be least affected by the destructive process that is going on all around them and in many places are almost isolated by the trophoblast.


  1. Evidence is advanced in support of the view that the implantation cavity is enlarged by the incorporation within it of some of the large venous sinuses which are found in close proximity to the ovum.
  2. Proliferative plasmodial trophoblast can be distinguished from the resorptive plasmodium by the absence of a “ brush-border ” where it presents a free surface or edge.
  3. It is suggested that there is practically no circulation in the intervillous space at this stage. Evidence is advanced to show that as the walls of the arterioles in the endometrium are destroyed, the vessels are obliterated and do not open into the intervillous space, which is dependent for its inflow on capillaries in the decidua capsularis.
  4. The presence of a great number of large calibre veins leading away from the venous sinuses, and so from the intervillous space, is-regarded as a provision to ensure a ready outflow from the space when free circulation is established through it.

I wish to express my indebtedness to the University of Edinburgh for permission to publish this paper, the substance of which formed part of a thesis submitted for the degree of M.D. I am also indebted to Mr G. A. Walker, Senior Technical Assistant in the Anatomy Department, Guy’s Hospital Medical School, who was responsible for the microphotographic work.


BAETHELMEZ, G. W. (1931). Amer. J. Obetet. Gynaec. 21, 5.

Baron, T. H. (1908). Early Development and Imbedding of the Human Ovam. Glasgow.

DABON, G. H. (1936). Amer. J. Amt. 58, 349.

Fuxmna, N. M. (1932). Obet. Gymec. 39, 441.

FLORIAN, J. (1928). Amt. Anz. Erganzungsheft zum 66 211.

Hmrrro, A. T. (1935). Oontr. Embryol. Carney. Insm, 25, 39.

MAOINTYBE, D. (1926). Trans. Roy. Soc. Edinb. 55, pt. 1, 77.

v. Mfinnnnnonrr, W. (1921). Z. gee. Amt. 1. Z. Amt. Entwcksch. 62, 352.

Snzmsox, J. C. (1932). Amt. Rec. 54-, 105.

Srmvn, H. (1926). Z. Mikr. Amt. 7, 295.

S-rn.ua1., H. & BENEKE, R. (1910). Ein junger menechlicher Embryo. Wiesbaden.

Explanation of Plate 1

File:Johnston1941 plate01.jpg

Fig. 1. The trophoblast shell adjoining the apex of the triangular chorionic cavity is shown in the lower part of the figure. It includes the larger cells from the apiees of the cell columns and amongst them some patches of proliferative plasmodium can be seen. Strands of proliferative plasmodium are streaming into the adjoining endometrium and can be recognized by the elongated shape and dark staining of their apparently isolated units. In the upper right-hand part of the figure apparently discrete units have penetrated deeply into the endometrium. x 158.

Fig. 2. A dilated venous sinus, lying deep to the decidua basalis. Three large veins leave its upper (in the figure) border. x 52.

Fig. 3. One of the slit-like spaces in the trophoblast shell, partially lined by proliferative plasmadium. One of the large basal villi is shown in the lower left quadrant of the figure, cut obliquely in its long axis. x 80.

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