Paper - The chimpanzee ovum in the early stages of implantation (about 10.5 days)

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Heuser CH. The chimpanzee ovum in the early stages of implantation (about 10.5 days). (1940) J Morphol. : 155- .

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This historic 1940 paper by Heuser is a description of the early developing chimpanzee at the time of implantation.

Modern Notes: Implantation

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The Chimpanzee Ovum In The Early Stages Of Implantation (About 10.5 Days)

Chester H. Heuser

Department of EmbryologyThe Carnegie Institution Of Washington, Baltimore, Maryland

One Text Mount: And Four Plates (Menr Figures)

Studies of the later stages of the anthropoid apes have shown that their placentation is very similar to that of man. Thus VVislocki examined placentae of chimpanzees during the last half of gestation and came to the conclusion that “placentation in man and the anthropoid apes is so Very similar that i11 the later stages the pl-acentae are practically indistinguishable from one another.” It seemed reasonable to believe that the early stages of these forms would also be found much alike. VVitl1 the hope of securing some of this material an attempt was made to recover a specimen comparable to the youngest known human embryo.

The venture was made possible through the cooperation of the Yale Laboratories of Primate Biology and the Department of Embryology, Carnegie Institution of Washingtoli. The time of ovulation in the chimpanzee is fairly well known from the work of Elder and Yerkes (’36) and Elder (’38). This information is a first requisite in obtaining an embryo of a desired age. Elder found that the menstrual cycle in the chimpanzee is about 35 days and that ovulation occurred a few days before the mid-interval swelling of the sex skin began to regress, which is about 14 days before the beginning of the next cycle.

With this information an estimate can be made of the probable day of conception. Advantage can then be taken of the operative procedure of enucleating the uterine mucosa as worked out for the recovery of embryos of the rhesus monkey. Operations were performed by Dr. C. Gr. llartman on two animals i11 Mai-eli, 1938, and on the same animals again in May, 1939. ()ne individual gave negative results but the other, Mame, fnrnislied a normal ovum, ‘Yerkes A’ ((7arn.egie no. 0. 620), on the thirt_V—second day of the menstrual cycle, l\Ilareh 26, 1938, and an atypical blast:.ocyst, ‘Yerkes B’ (Carne_e;ie no. t‘. (342) on ;\Ta_V 20, 1939. The esti— mated conception age of no. (3.('20 is 10:} days. 0.642 was removed on the twenty-ninth day of the cycle, about 12 days after the estimated time of fertilization. A brief report was made (Elder, Hartman and Heuser, ’39), of the successful out-come of the experiment.

At the time of the first operation Doctor Hartnian obserx-‘ed a small pink spot on tl1e surface of the endometrium wliieh he suspected as the site of an implanted ovum. The translucency of the fresh tissue disappeared in the tixiiig‘ fluid and the spot was no longer plainly visible. The B0uin’s solution was replaced with 35% alcohol and from this point on all changes of fluid were made \'er_\f gradua.l1_v. Under the binocular microscope with suitable illumination——especially by manipulating a concentrated horizontal beam of light-—the site of implantation was again found. A. small block of mucosa containing the ovum was cut out and carried up gradually to 8% ‘celloidin. 'l‘he eelloidin block was then embedded in 52° parattin and cut in sections 6 ii in tliiclmess, using‘ the wate1'—on—the—l<nife method. The sections were stained in hematoxylin and eosin.

in the middle of the sheet of endometrium an oval sliglitly raised area, 2 X 8 min., was marked off from the surrounding surface by a deep slit—1ike groove. The ovum was implanted just lateral to the c11rVing' edge of the groove (fig. 4) and there was no noticeable protuberance into the uterine lumen. The sections reveal the ovum entirely buried in the uterine mucosa; with the exception of a small area marking‘ the point of entrance, it is covered by maternal epithelium.

The diameter of the ovum is about 0.72 mm. and the bare area represents about 2% of its surface. The trophoblast has made a luxuriant growthiand is differentiated into an inner layer of closely packed cells, the cytotrophoblast, and a surrounding syncytial zone, the plasmoditrophoblast. The external surface of the trophoblast is relatively smooth and lies in close conta.ct with the uterine stroma. Occasional loops or streamers from the plasmoditrophoblast extend to blood vessels and others end blindly in the stroma. In a few places the endothelium is destroyed at the points of contact allowing the entrance of a small amount of blood into the laeunar spaces. Blood vessels lying near the ovum are also tapped -as shown in figure 2. Large fluid-filled spaces have appeared in the plasmoditrophoblast. These laeunar spaces are found by plate reconstruction to be joined together forming a temporary labyrinthine arrangement.

The sections, e.g., figures 3 and 4 indicate that the pink color of the implantation site was produced by the blood in the laeunar spaces, intensified by blood—tinged coagulum lying above it on the uterine surface as well as by blood in the distended thin—walleCl vessels below the ehorion. These enlarged vessels are comparable to the subchorial sinuses which are consistently found associated with young human embryos. The large vessels sl1ow11 in the lower left corner of figure 3 unite and pass through fift.y—two sections to join a sinus 0.15 X 0.4 mm. which lies about 0.6 mm. below the ehorion. A second arm of the sinus bends toward the ehorion and becomes confluent with the trophoblastic lacuna -as shown on the left side of figure 2.

A large uterine gland with several branches is entangled in the trophoblast. The gross form of the gland is still discernible as shown in figures 1 and 3, and the epitl1elium shows various nhases of disintegration. The end of one branch lies near the edge of the chorionie cavity in close proximity to the embryo itself. One small segment of gland with dark pyknotic nuclei has been entirely out off and is free within the ehorion.

The embryo

As determined by count and measurement of the sections and further aided by reconstruction the embryo is found to be oval when viewed from above. The inference that the cephalic and caudal ends are identifiable an.d that the cephalocaudal axis passes through tl1e longer dimension of the plate is supported by the structure of the embryo, especially as regards the shape of the amniotic cavity and the greater accumulation of mesenchymal cells anticipating the position of the body stalk at the narrower end. These features are brought out in the drawing shown in figure 1 which was made from a graphic reconstruction of the serial photographs. It represents a section of the ovum passing through the midsagittal plane of the embryo. The sections were cut in a plane dorsoventrally oblique to the longitudinal axis of the embryo. This accounts for the exaggerated thickness of the disk as seen in the sections illustrated on plates 2 and 3. In reality the disk is a pseudostratified layer, one or two cells in thickness, measuring 0.124 )< 0.110 X 0.058 mm.


The amnion consists of a band of large cells which blend with the cytotrophoblast. This relation is shown in figures 5 and 6. The large, spherical, closely—packed nuclei of the amnion are very similar in appearance to those of the tr0phoblast. The amniotic cavity appears in the 10-day macaque embryo as a space between the germ disk and the covering trophoblast. Cells from the latter segregate and become transformed into the thin characteristic amniotic membrane. The amnion probably develops in a similar manner in the chimpanzee.

Primary entoderm

In comparison with a more rapid growth of other parts of the ovum the entoderm still remains in a quiescent state. In the caudal region of the embryo, as seen in figures 1, 4 to 6, it is a thin layer only one cell in thickness. The cytoplasm is scant in amount and the rounded nuclei protrude into the -chorionic cavity. Toward the front end of the embryo the entoderm cells are more closely packed and the layer is slightly thicker. The first two sections of the embryo proper pass beyond the germ disk and the entoderm is cut tangentially so that it appears as patches of cells without any part of the germ disk showing. At the edges of the embryonic plate the entoderm and extra-embryonic mesoderm blend and the two structures make contacts in many other places. In general, liowever, there .is a narrow ill-defined space between them which contains pink stained material. Some of this stained substance is probably cytoplasm and some of it is coagulum. The meshes enlarge and the space extends around the tangentially cut patches of entoderm. The layer of cells, composing the external wall of the space, overlays a11d blends with the mesencliymal tissue beyond the embryo, indicating that tl1c formation has been produced by the inward spread of mesoblast. Primary mesoblast

Heuser-1940 text-fig01.jpg

Fig.1 Drawing of a graphic reconstruction from serial photographs representing a section of the ovum passing through the mid—sagittal plane of the embryo proper. The positions of the sections shown in plates 1, 2 and 3 are indicated by arrows. Since the embryo lies eccentrically in the chorion, as shown in figure 4, the reconstruction does not cut through the maximum width of the ovum. A few streamers of plasmoditrophoblast are cut beyond their connection with the ovum and appear detached in the drawing. A part of the ovum is not covered with uterine epithelium. The exposed area, is about 0.0375 or about 2% of the total surface of the chorion. The trophoblast is enveloping a large uterine gland. Some of the glandular epithelium has been cytolyzed and other parts show stages of disintegration. The amniotic cavity is a. narrow space between the embryo and the amniogenic cells, diiferentiating from the cytotrophoblast. A small diverticulum near the caudal end of the embryo probably is the beginning of an amniotic duct.

The chorionic cavity contains a relatively large amount of inesoblastic tissue. The inner surface of the cytotrophohlast is lined by closely adherent cells and from them strands or vesicular groups of cells grow out into the chorionic space. The tissue is rather dense in pa1'ts of the cavity and in other regions there are wide meshes which occupy approximately one—third of the cavity. The segmentation cavity in younger blastocysts is presumably very small and soon becomes occupied by the extra-embryonic mesoblast. In the present specimen it appears that the tissue has spread up to the embryo proper, the line of cells below the primary entoderm being the fringe of the advancing mesoblast.

With the hope of finding a critical stage in the formation of the yolk sac a second operation was planned to yield an embryo slightly older than the previous one. About 12 days after the estimated time of conception hysterotomy was again erformed on Mamo. A site of implantation was not detected on the fresh endometrium but a small protruding vesicle was found after fixation in Bouin’s fluid. It proved to be an abnormal blastocyst only partially embedded in the uterine mucosa. At one side of the ovum a foot—like process is covered by uterine epithelium but the larger spherical portion of the egg as shown in the figures on plate 4 is exposed to the uterine lumen. The maximum diameter is about 0.27 mm.

The specimen consists of a wall of trophoblast from which partitions extend across the interior dividing it up into vesicular spaces of variable size. A few cells show large distended nuclei with fragmented or clumped masses of chromatin within. Two nuclei of this type are shown in figure 9. Similar nuclei in the process of disintegration are present in the plasmoditrophoblast of the normal chimpanzee and human embryos. The condition suggests an intracellular origin of at least some of the lacunar spaces in the trophoblast.

Several isolated syncytial masses, the largest containing as many as nineteen nuclei, rest in the uterine stroma. The structure of these masses appears the same as that of normal plasmoditrophoblast. They probably are detached ends of processes which grew out from the surface of the ovum. The stroma immediately beneath the ovum is condensed but surrounding this zone there is a large edematous area. The nuclei of the cells in the more compact region are enlarged, indicating that stroma cells are in the process of becoming transformed into decidual cells.

An embryo failed to develop. No group of cells was found which could be regarded as an embryonic mass. The formative cells were possibly more defective than the remainder of the ovum and perished whereas the extra—embryonic part survived for a longer time.

Discussion And Summary

Until quite recently the specimen reported by Miller (’13) has remained the youngest known normal human embryo.

It was restudied and fully described some years later by Streeter (’36). Although only a few sections of the curetted endometrium were saved, the material has been of great value in providing information on early implantation. VVithin the year two human embryos—one slightly younger and the other perhaps a little older th-an the Miller ovum—l1ave been secured under the most favorable circumstances by Hertig and Rock ( ’39). The specimens are catalogued in the Carnegie Collection under the numbers 7699 (younger one) and 7700 (older one). It has been my privilege to study these excellently preserved embryos. As Hertig and Rock are preparing a description of the specimens I shall refer to them only briefly.


The picture of implantation at this stage of development is almost identical in the chimpanzee and in man. In each the ovum is buried in the uterine mucosa immediately beneath the epithelium.

The chimpanzee chorion has not as yet produced a bulge of the endometrium above it into the uterine cavity. The ovum entered the mucosa at the curving edge of a slit-like groove and it is possible that if implantation had occurred on the flat part of the endometrium a slight elevation would be seen. This surmise is based on the condition in the slightly older human specimens i11 each of which there is a swelling about 1 mm. in diameter and 0.14 to 0.21 high.

The trophoblast is differentiated into an inner cellular layer and a broad vacuolated covering zone of plasmoditrophoblast which is closely applied to the uterine stroma. The external surface of the chorion, especially in the deeper region, is made slightly irregular by a few outgrowing processes but chorionic. villi have not yet appeared. The trophoblast has destroyed vascular endothelium in a. few places establishing communications between lacunae and blood vessels. It is evident, however, from the small number of corpuscles found within the vessels that circulation is sluggish near the implanted ovum at this stage of development.

Chorion and uterine gland

In the chimpanzee specimen a uterine gland lies in the path of the invading trophoblast which has partially surrounded a few of its branches. Parts of the gland show progressive stages of disinteg1'ation but the form of much of it is still retained. A branch of the gland extends as far as the edge of the chorionic cavity. One small segment has been cut off and is free Within the chorion. This detached fragment is located near the surface epithelium of the uterus and may represent. a part near the former mouth of the gland. Glandular involvement is also present in the new human embryos mentioned above. A broad branch in no. 7699, slide 5, for example rests upon the cytotrophoblast and the plasmodi— trophoblast is closely applied to the gland. And a similar case is seen in slide 8 of the same specimen Where the syncytial layer is moulded around a part of another gland near its mouth. The gland passes through the Wall of the ovum and is separated from the chorionic cavity by a layer of cytotrophoblast one cell in thickness. In the slightly older specimen, no. 7700, a similar but less extensive glandular involvement is seen in slides 5 and 6. The chorion-gland relationships are apparently temporary and chance conditions soon to be eliminated.


The embryo proper is located at the deeper or internal edge of the chorionic cavity which is small in comparison with the size of the ovum as a Whole. A glance at the section shown in figure 4 might give the impression that the embryo lies near the uterine surface and not deep within the ovum. Examining the structure of the ovum more carefully, it is seen that the deeper half of the trophoblast, expecially the plasmoditrophoblast with its included la-cunae has increased greatly in thickness Whereas the opposite half is still quite thin and it is obvious that the embryo is placed at the bottom of the chorionic cavity (top in the figure) and lies as far as possible from the uterine l.umen. The specimen is in accord 164 cnnsrnn H. nnnsnr.

therefore with the normal condition of the primate blastecyst, the embryonic pole of which first makes contact with the uterine mucosa.

I’m'»2m'ti'L‘c mesoblast

A striking feature of the chimpanzee embryo is the precocity and abundant. growth of tlie primitive mesoblast. Instead of a large and definite cavity Within the chorion the territory is occupied by the mesoblast distributed in the form of irregular strands and 1nesh—like groupings of cells. The tissue is intimately connected to the eytoti-oplioblast from which it apparently arises from all sides.


It may be assumed that the first entodermal cells appear early in the chimpanzee just as they do in the ova of monkeys and other mammals. But the formation of a yolk sac is long deferred. At least in the 10§»—day specimen the endoderm is a thin layer only one cell in thickness in the caudal region and about two cells in thickness toward the front end of the embryo. Presumably the layer by multiplication of its cells will increase in thickness and differentiate into yolk sac and gut entoderm.

The smaller specimen, although definitely abnormal, gives a clue as to the probable size of the blastocyst at the time of entrance into the uterine mucosa. The maximum diameter of the ovum is only 0.27 mm. and it is already more than half implanted. The size of the blastocyst at the initial step of penetration is problematieal but it may be assumed that it is smaller than the measurement given, perhaps not more than 0.2 mm.

As a further contribution. this ovum indicates a very early segregation of formative (embryonic) and eXtra—embryonic cells of the ovum. Localized defects are encoinitered at various steps in development and the blastocyst at the beginning of its existence is evidently no exception. The presence of a vacuolated spherical mass of trophoblast without any indication of an emb1:y011.'1c area points to a greater sensitivity or \'u111erabi1'1ty of the formative cells.

Literature Cited

ELDER, J. H. 1938 The time of ovu1at.ion in c11impan7.oos. Yale J. Biol. 8: Med., V01. 10, pp. 347-364.

ELDER-, J. H., (J. G. IIAR'l‘MAN' .-\:\*1> (7. II. I-IEUSE1: 1938 A ten and one-h:11f day ( e111h1-yo. ‘Yerkes A.’ J. A111. Med. Ass11., V01. 3, pp. 1156-1159.

ELDER, J. I.-[., AND B. M. YERKES 1936 The sexual cycle of the chimpanzee. Anat. Reta, V01. 67, pp. 119-143.

Hn:1t.T1G, A. 'l‘., AND J. C. ROCK 1938 On a con1p1ete normal 12-day human ovum of the p1'c~vil10us stage. Aunt. Rec, vol. 73, suppl. 110. 2, pp. 26-27.

HISUSER, (3. II. 1938 E31-1y dc-ve1opme11t of the primitive mesoblast in e1nb1'yos of the rhesus monkey. Coiip. 1-?os._, C:11'11egie Inst. W'as11., Pub. no. 501, pp. 383—388.

M1I.L.1«:R, J. W. 1913 Corpus Luteum uud St-,11\v:111ge1-sc,]1aft. Das ji‘111gste operativ e1-11a1te1m menschlichc Ei. Ber]. klin. W0el1nscl1r., vol. 50, pp. 865-869.

S'L'1cEET*1£R, G. L. 1926 The ‘Miller’ ov11n1a—The y01111gest 1101-11131 human C111bl'_V0 thus far known. Car11egie Inst. V\-'ash., pub. 110. 363. Contrib. to Embryoh, V01. 18, pp. 32-48.

WISLOCKI, G, B. 1933 Gravid reproductio11 t1-act and pl:1ce11t.a of the chi1npa11zee. A111. J. Phys. A11t111'op., vol. 18, pp. 81-92.

W1sLo<:*1:1, G. B., AND G. L. STREETER 1.938 On the plac-e11t.atiou of the nlacaqlle ( 1nu1att:L), from the time of '1111p1a11tat.io11 until the f0rmatio11 of the definitive placenta. (7a.1'11ogie Inst. W:1sh., Pub. 110. 496. C011t1'i‘n. to Embryo], vol. 27 , pp. 1—66.


The figures on plates 1, 2 and 3 are photographs of six sections of the chimpanzee ovum ‘Yerkes A.’

Heuser1940 plate01.jpg

The locations of the sections in the specimen as :1. whole are indicated by arrows in figure 1. Lilies p1'ojecte(l through the arrows and dashes on the photographs coincide with the plane of tl1e reeoiistriictioii shown in figure 1.

2 The section is located near the edge of the ovum. One laoima is in (10111lllllllltttfloll with 21. large blood vessel. 111 21.11 :1<l_ioi11ii1g section t11e three parts of tl1e blood vessel unite in :1. eom111oi1 t1-unk wl1iel1 issues from a subclmrial sinus. C. 63.0, seetioii 3-1-5. X 150. B1. \'., blood vessels; Lac-., l:1(-un;1; P1,, plas111o(litr0phoblast; Vt. 011., uterine epithelium.

File:Heuser1940 plate02.jpg

3 B1-unches of 21. large uterine gland are p~.u'ti:1Jly surrounded by the plas1n0dit-roplioblast. One piece of gland has been detached and is free i11 the chorionic cavity. At the hez1.(l oi’ the a1'1'o\\-' a. mass of cougulliin lies over a small gap in the eliorionic w:.1ll. The 1)l‘G£lk, pi-<>l):1bly due to iI1j111'_\', extends through five sections. (3.620, section 4-3 9. X 154). B1. v., lrlood vessels; (Th. 0., cho1'ionie e,:1vity; Ut. g'l., uterine gland.

4 The section passes through the middle region of the ovum. The embryo lies eccentrically in the ovum but at the deep edge of the chorionic cavity. As the germ disk is cut obliquely the thickness of the germ disk is exaggerated. Parts of two large mitotic figures are seen in the germ disk. 0. 620, section 4-1-5. X 150. Amn., amnion; Cyt., cytotrophoblast; Emb., germ disk of embryo.

5 The amniotic cavity is cut across at the caudal end of the embryo. Primary entodermal cells are applied to the ventral surface of the germ disk. 0. 620, section 4-1-1. X 400. Am. c., amniotic cavity; Ent., primary entoderm.


File:Heuser1940 plate03.jpg

6 This section joins the one shown in figure 4. The remainder of the lower cell in mitosis of figure 4 is seen in this photograph. The primitive mesoblast in the chorionic cavity blends with the cytotrophoblast. C. 620, section 4-1-4. X 400. A1nn., amnion; Mes., primitive mesoderm.

7 A branch of uterine gland extends to the edge of the chorionic cavity. The germ disk is cut ventral to the amniotic cavity. The entoderm is slightly thicker than in the caudal region of the embryo. C. 620, section 4-2-2. X 400. Emb., gerin disk of embryo; Ent., primary entoderm.

File:Heuser1940 plate04.jpg

Photographs of chimpanzee ovum ‘Yerkes B.’

8 Section showing the ovum and a detached fragment of trophoblast. The uterine stroma is slightly condensed in a small region above the embryo. In the large edematous area are numerous blood vessels. 0. 642, section 4 2-6. X 100. Ut. -ep., uterine epithelium.

9 The stroma cells are enlarged, indicating that they are being transformed into decidual cells. The ovum only partially implanted protrudes into the uterine lumen and is not covered with endornetrium. Two large degenerate nuclei with clumped masses of chromatin are seen in the trophoblast. An embryo proper is not present in the specimen. 0. 642, section 4-2-3. X 500. Troph., trophoblast; Ut. ep., uterine epithelium.

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