Paper - Some notes on recent primate embryology

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Gatenby JB. Some notes on recent primate embryology. (1945) Irish J. Med. Sci. 177-187.

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This 1945 paper by Gatenby is a review of "current" research circa 1919 in primate embryology. Describes embryo Hertig-Rock No. 1 8004

See also - Hertig AT. and Rock J. Two human ova of the pre-villous stage, having a developmental age of about seven and nine days respectively. (1945) Contrib. Embryol., Carnegie Inst. Wash. Publ. 557, 31: 65-84.

Modern Notes: Embryonic Development | monkey | implantation

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Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

Some Notes on Recent Primate Embryology

By J. Bronte Gatenby.

From a lecture delivered at the Rotunda Hospital, March 1st, 1945.


Within the last ten years great advances in our knowledge not only of the oestrus cycle, but in primate embryology, have been made, chiefly by American workers, of whom may be mentioned George L. Streeter, Carl G. Hartman, Arthur T. Hertig, Chester H. Heuser, George W. Corner and George B. Wislocki. These investigators ,have chiefly worked on an unrivalled collection of macaque ova. In America a number of young human ova have recently been described - that of Hertig and Rock (about 11 days old) being the most perfect known to science. Ramsey (Yale ovum), Brewer (Edwards Jones Brewer), Krafka (Torpin ovum) and Scipiades have also contributed papers on human embedding stages.[1] Almost all of this material is fixed with Bouin’s fluid, a good general histological agent, but quite unsuitable for the necessary cytological work.

Early Macaque Development

It appears that the zona pellucida, which is a thick non-cellular membrane around the mammalian egg, persists for a part of the 5 days the blastocyst is free in the uterine cavity. This zona pellucida has special physical properties, not being prone to adhere to cilia or cell surfaces. Whereas, once it is removed or dissolved, the surface cells of the blastocyst are sticky. Thusthe ovum with zona pellucida can be easily manipulated with a glass pipette, while the blastocyst has the faculty of adhering to various objects such as glass and steel needles.

The ovum, blastocyst, or early embryo of the monkey is still free in the uterine cavity on -the 8th and 9th days and can be washed out of the uterine cavity. Roughly, such eggs are 1/5 mm. in diameter, e.g., exact measurement of one is 0-23 x0*22 mm. In the 8th or 9th day blastocyst four types of cell can be seen: (1) trophoblast cells of the blastocyst wall ; (2) trophoblast cells of the embryonic pole; (3) large primitive formative cells, destined to form the germ disc from which the embryo proper arises; (4) primitive endoderm cells, which form a membrane beneath other cells of the embryonic pole.

At this stage the zona pellucida may still be adherent to the trophoblast. The total number of cells is 140, two-thirds of which are at the embryonic pole. The free -blastocyst on the 9th day may be 0-267 mm., whereas the egg before segmentati-on is about 0110 mm. The increase in size does not mean that the egg has grown, but rather that its substance has become redistributed. During cleavage the egg actually becomes smaller, and real growth of the blastocyst does not occur until it has been embedded. The blastocyst is actually a film of cells over a droplet of water. It should be mentioned that during its journey down the tube, the blastocyst is turgid, and that it subsequently givcs off liquid, and its walls tend to collapse at the time of its embedding and first attack on the maternal endometrial plaque. But once again it begins to become spherical and turgid, its abembryonic wall thickening, and attacking the endometrial surface opposite to the endometrial plaque already established. Thus two opposed placental sites occur in the macaque monkey, but only one embedding region in man. The blastocyst of the monkey closely resembles that of other placental mammals, and it may safely be assumed that when the early human st-ages are known, they will be like those of the macaque.


In the macaque, of 44 implantations, 41 occurred centrally either on the anterior or posterior wall of the uterus, half each. Three specimens were exceptional, two near the lateral border of the uterus, one near the entrance to the cervical canal.

It is well known that in polytocous animals like the pig or rat, the eggs become quite evenly spaced along the uterus before embedding. This phenomenon is at present unexplained. In the macaque there is no evidence that any embedding plaque forms previously to the arrival of the blastocyst. On the contrary, Streeter describes a case where the blastocyst in contact with the endometrium made a plaque of implantation, then changed its mind and shifted on further, and made another and definite implantation. It should be remembered that deciduomata or plaques can be produced by administration of hormones and local trauma even in the absence of an ovum. Further reference to this will be made below. It is interesting to note that the blastocyst does not fix just opposite the inner cell mass, but slightly peripherally, but always the embryonic knob or inner cell mass is turned towards the endometrial epithelium.

Actual Process of Embedding

It has, of course, been known for years that some mammalian blastocysts embed by producing at the pole a strong proteolytic enzyme, which dissolves a passage through the endometrium into the embedding site. The American school has worked out the details for the macaque very fully. Where the blastocyst and uterine epithelium touch, there is a disturbance in the arrangement of the endometrial epithelial nuclei, and the maternal cell cytoplasm here becomes paler, indicating beginning of cyt-olysis. In the blastocyst at the touching point there is an increase of nuclei in what Heuser and Streeter now call the syncytial layer. It appears that at this moment the trophoblast nuclei at this point have multiplied without similar provision of new cell walls—the peculiar character of the syncytiotrophoblast or plasmodotrophoblasts has now been established. It has been claimed that in time stages the macaque and the human develop» -alike up to the 30th day. No free blastocyst or early embedding stages are yet known in man. The 10 or 11-day-old human ovum is deeply and interstitially embedded, whereas the macaque of the same age is still on the surface and attacking an epithelial plaque which has been formed under stimulus by the blastocyst. It seems to be assumed by mammalian embryologists that in man the epithelial plaque is not formed at all, and the human ovum has much stronger penetrative powers than those of the macaque. I11 the gibbon and orang-utan the ovum implants intcrstitially, and has a decidua capsularis as in man.

Significant Dates of Macaque Stages of Embedding

Online Editor - see Macaque Placental Timeline table from this data.

  • 9th Day. Ovuln beginning contact. Endometrial proliferation to form epithelial plaque.
  • 10th Day. Invasion. Erosion of strorna, gland and vessels. Lacunae beginning. Transition of cytotrophoblast to syncytium.
  • 12th Day. Trabeculae and cascades of trophoblast cells. Mesoblast, yolk sac. Ovum walls collapsed, no sinusoids.
  • 13th Day. Sinusoids comniunicate with lacunae. Villi begin. Ovum walls dilated, abembryonic wall hypertrophies preparatory to formation of second implantation site.
  • 15th Day. Maternal epithelium reaches end of proliferative period.
  • 17th Day. Necrotic border zone. Blood in glands. Primitive body mesoderm.
  • 19th Day. Villi with three zones established, and branching. Pinocytosis (imbibing of liquid substances}.
  • 22.5 Day. Villi vascular. Oedema at junction zone.

As regards decidua, what is in the macaque? Wislocki and Streeter mention oedema, but nowhere discuss deciduze in their account of the embedding of the macaque monkey up to the 30th day, and they make the point that outside the plaque area the epithelium of the uterus and the stroma are quite normal for the period. Much the same applies to the Hertig-Rock human ovum, to be mentioned below. According to Streeter, the function of the epithelial plaque is not certain. It is clear at least that the plaque cells form a pabulum for the ovum. In this connection it has been shown by Hisaw in non—pregnant macaque monkeys that, following traumatisation during biopsies on the presecretory corporin phase of experimental cycles, epithelial plaques appear. Streeter has noted the same whorls or nests of epithelium in Hisaw’s material as in the normal pregnant uterus. In time, the pregnancy plaques last 7-10 days, whereas Hisavv’s experimental plaques are prolonged. It is still not certain that transitory plaques do not occur in the human and disappear quickly. In the gibbon, Selenka observed epithelial cell nests in the endometrium similar to those of macaques, and in the gibbon embedding of the ovum is interstitial as in man. I made a special point of this in view of the controversy over borderline cells. Nevertheless, on the evidence now available it seems likely that the early embedding stages in man will be found different from those of the macaque, and much more like the well-known stages in the guinea pig. The embedding of the human ovum would appear to be accomplished more quickly than in the monkey, and is probably well advanced on the 8th or 9th day.

In the macaque, the actual breaking through to the uterine stroma and the creation of a gap in the surface is not effected until the 10th day. The endometrial cells immediately exposed to attack tend »to slip towards the. blastocyst wall, and their nuclei resist digestion for some time, becoming heaped together into pyknotic masses, of which more than one can be seen in some sections of the embedding site. Resistance to digestion by cell nuclei has long been known by entomologists who have observed digesting material of other organisms in insect intestines. It is interesting to note that destruction of maternal cells is the first fruit of the embedding process. How far such destruction is the normal course of events in the later human ova is a moot question. It is claimed by Hertig and Rock that where noticeable necrosis of maternal cells is present the ova are abnormal. Yet in this connection it is very interesting to notice that Streeter's school has shown that in the macaque, necrosis is present, not only on the outer embedding edge of the early trophoblast, but in later stages in the deeper maternal tissues. In the macaque ovum at 17 days, Streeter and Wislocki speak of a “ necrotic zone ”, formed by conversion of the disrupted maternal plaque cells.

Trophoblast after the 10th Day

Between the 10th and 11th days, as the macaque trophoblast thickens, there occurs widespread conversion of trophoblast cells into syncytial areas. Once contact between syncytium and maternal stroma becomes intimate, the student of this stage will find it difficult to distinguish between maternal and embryonic tissue.

The following types of cells have been described :—

  1. Ordinary trophoblast cells
  2. trophoblast cells differentiating into the next category
  3. synctium
  4. epithelial plaque cells of the endometrium (in Macaque)
  5. epithelial proliferation cells of the uterine glands
  6. endothelial cells of the maternal vascular system
  7. maternal stroma in various stages of differentiating into decidua (human)
  8. angioblasts budding from the cytotrophoblast
  9. categories of leucocytes
  10. pleomorphic border zone cells (in man)

Of these types, the syncytial cells are quite obvious. At this early stage these cells are seen to be engulfing red blood corpuscles. Clefts soon appear between the developing syncytial cells, and these clefts later connect with eroded venous sinusoids and fill with blood and other fluids. Near the embedding ovum, the arterial supply is in the form of spiral vessels. The spiral and kinked nature of the artery can be used to reduce, or even block, arterial pressure. The spiral arteries usually penetrate up near the endometrium, though their capillary connections further than that are not at present understood in the embedding site of the monkey. According to Heuser and Streeter, there is no evidence of arterial capillaries emptying into the venous lacunm or sinuso-ids, and these authors indicate that in these early periods, the blood supply around the ovum is essentially stagnant. Other American authors have also pointed out that in the lacunae of human ova the hacmatids stain badly, indicating their hastening dissolution and supporting the view that at this period no true circulation has been established.

An important aspect of pregnancy is the physiological control of the maternal blood vessels supplying the placenta. According to Streeter these problems naturally fall into four sections:

A. The blood supply of the normal uterus during the different phases of the menstrual cycle;
B. Changes in the blood vessels during the formation of the placenta;
C. The character of the definitive placental circulation;
D. The vascular changes related to parturition.

Apart from the older investigations by Bartelmetz and Falkiner on the human, recent work has been done on the macaque in Section A by Daron and Herberg. Apparently here there are two distinct types of arteries in the endometrium — (1) large tortuous coiled or spiral arteries, closely wound to form radial columns through the mucosa. Each consists of a single artery surrounded by dense stroma and which has few branches till it divides peripherally into numerous pre-capillary arterioles, (2) small arteries only slightly coiled, and only extending to the basal zone of the mucous membrane, in which they soon break up into capillaries. During menstruation the terminal branches of the spiral arteries are lost.

Under Section B, some recent information relative to changes in the blood vessels during formation of the placenta is mentioned elsewhere. On Sections C and D, Spanner and Falkiner have published iteresting papers, and I do not propose to enter into this question. Nevertheless some remarks on recent reactions to Dr. Falkiner’s work in Section B will be in order. The question of the relationship of the sinuses to the vascular pattern of the endometrium, and to the changes which it undergoes in the course of the (estrous cycle, is fundamental. Falkiner claimed to have been able, in his specimen, to trace in full the connection of the sinuses with the rest of the vascular tree, and to have demonstrated that they represent localised dilations of immediately precapillary venules. According to E. M. Ramsey, who’ has recently studied the “ Yale ovum ”, the indirect evidence which is available in this specimen is in support of Falkiner’s view. The distance of the sinuses of the Yale from the spiral arteries, taken into conjunction with the structure of their walls, indicates that they are either capillaries or venules.

Ramsey believes that either as a result of hormonal conditioning prior to, or during, implantation, or as a result of direct action by the growing trophoblast, the distension of venules is affected.

The Decidua

Decidual reaction is the appearance of large clear epithelioid vesiculated cells 40-50 um, in diameter, ovoid or polyhedral in form, and usually tightly compressed owing to the imbibition of oedema fluid, or to the storage of glycogen. These decidual cells arise from the typical fusiform stroma cells, mainly of the stratum compactum of the uterine wall. Decidual cells occur where implantation takes place, even if in the tube or the ovary.

Group I. (Younger than primitive streak)

  • Stage 1. no villi.
  • Stage 2. villi.
  • Stage 3. branched villi

Group II. Priiitive streak.

Group III. Neural groove and associated structures.

Decidual reaction is generally supposed to be invoked in order to block the rapid extension of the syncytium. In Group 1 ova[2] the reaction is local, in older ova it is said to be found in other parts of the compacta, though this is denied by Falkiner for his specimen. Falkiner states: “ That decidual reaction in the human has nothing or little to do with immediate contact with the growing ovum is borne out by the occurrence of typical decidua in the uterus in ectopic pregnancy and also by the occurrence in normal pregnancy of ectopic decidual cells. It is also to be noted that the occurrence of large cells in the immediately surrounding zone of early human ova has. been usually attributed to decidual reaction. Such a conclusion, in my opinion, is erroneous, as I have shown in this specimen that the cells are trophoblastic in origin.”

If, however, it could be shown that in the human, epithelial plaques formed during early stages of embedding as in the macaque, it might be that the wandering border line cells were really swollen epithelial cells, and not foetal in origin as Falkiner assumes. The properly prepared new material at present being studied by me may assist in this problem.

According to Krafka, in the border zone of the “ Torpin ovum ” two distinct cell types prevail, one which is definitely syncytium in varying degrees of degeneration, the other, a large clear pale cell which grades perfectly into the developmental series in the trophoblast column. This may be said to support Falkiner’s view. It is certainly true that in the Hertig-Rock No. 1, peri-ovular disturbance of stroma is practically non-existent. In Krafka’s “ Torpin ovum” the border line cells are shown wandering an astonishing distance from the ovum wall.


In the macaque (and perhaps human), amniogenesis does not clearly begin till the 10th day, when the future amnion cells can be seen in process of delamination from the trophoblastic wall. Accompanying this delamination, an accumulation of fluid begins in an intercellular space, at the junction between the delaminated amnion cells and the cells of the germ disc. This is the future amniotic cavity. This is to say that the original trophoblast cells overlying the pluripotential germ disc become difierentiated into three separate tissues — syncytium above, cytotrophoblast in the middle, and amnion below. Presumably the cells of the germ disc are primarily responsible for this local effect, and it has been suggested that at this early period they also produce the amniotic fluid. It is interesting to note that in many specimens of the macaque, the first amniotic cavity, while still uncovered by continuous amniotic cells, is seen to contain red blood corpuscles and often a group of pyknotic nuclei belonging to the original partly digested endometrium. Similarly the early blastocyst cavity often contains pieces of ‘broken down blastomeres, whose presence does not appear to indicate that the ovum is abnormal.

Extra-Embryonic Mesoderm in the Primate Blastocyst

That the cavity of the earliest human ova contained a network of stellate cells has been known since the time of Leopold and Peters, Bryce and Teacher. Recent work has thrown light on the origin of this mesenchyme so called, and consists of evidence obtained by the study of macaque blastocysts, and of the 11-day old human ovum of Rock and Hertig.

According to Heuser and Streeter, the early macaque blastocyst is a single layered vesicle, whose cells are much stretched. So much so, that Heuser and Streeter do not believe that delamination from them at this period is possible. However, there is a layer beneath the germ disc region formed of what they call primary endoderm. In the macaque, it seems certain that at the edges, these cells creep down and ultimately form an inner layer beneath the blastocyst wall. By the 11th or 12th day the entire trophoblast is lined with such cells and can now be regarded as a chorion. Heuser and Streeter say: “As to the origin of the cells composing the layer, either they are descendants of the first endodermal cells, or they arise by delamination.” Later in their account they accept fully that this lining is endodermal, and point out that by a similar process, the yolk sac of other mammals, such as the rabbit, dog, cat and sheep, arises. According to Heuser and Streeter, a large part of the primary yolk sac degenerates before an appreciable amount of mesoblast is added, and it gives no indication of attaining a functional state. The early membrane lining the chorion may be termed the “ primary yolk sac ”, and the structure present in later stages the “ definitive yolk sac ”. True mesoblast, according to them, is first seen in the chorion of the monkey on the 10th day in the angular spaces produced by the bulging of the germ disc into the chorionic cavity. It is stated that most, if not all, of these cells are spreading from the trophoblast, though, to quote the American authors: “It is possible that the primary endoderm contributes a few of these cells, just as the wall of the yolk sac differentiates mesoblast in later stages of man and other animals.”

From this account it is difficult to understand whether Streeter believes that the primitive endoderm lining breaks down and forms inesoderm, or whether the latter is formed in the active region above and to each side of the embryonic disc. It should be noted that the turgidity of the early blastocyst rapidly loosens about the 9th day, and the trophoblast cells are sufficiently collapsed to allow cell budding inwards. Active mitosis is taking place in the trophoblast at this period.

The Hertig-Rock Ovum No. 1

The Hertig-Rock Ovum No. 1 is 11 days old, and it is claimed to be the youngest known. However, the Miller is perhaps a day younger (10 days), though the Hertig-Rock No. 1 is the youngest complete ovum known. This ovum was got from a hysterectomy. There was a completely known clinical history. If ovulation[3] occurred on the 14th, i 2 days before the onset of the next menstrual period the Hertig-Rock No. 1 would be not more than 15 and not less than 8 days old. Spermatozoa in the female genital tract are not supposed to survive more than 3 or 4 days, whereas the egg lives about 24 hours without fertilisation. The successful coitus is supposed to have been that on the 12th day. Gonadotropic hormone was found in the urine of this case, that is, only 11 days after conception. The ovary had a recent corpus luteum 1-5x1x1-0 cm.: the lutein zone was 2-3 mm. in thickness; its central cavity with gelatinous coagulum was slightly haemorrhagic.


The American workers use the following technique for opening a uterus suspected of containing an ovum. The specimen is immersed in normal saline and the uterine cavity entered by cutting both lateral endometrial Walls with fine straight scissors. The uterine lining is then exposed by gentle retraction of the anterior from the posterior wall, with the fundus serving as a hinge. The embedded ovum is almost invariably on the anterior or posterior wall. The uterine cavity contained only a small quantity of thin mucus. The uterine glands were very tortuous with saw-tooth contour.

The ovum showed as a tiny slightly elevated translucent area surrounded by congestion and haemorrhage, on the posterior surface. On the anterior surface just opposite there was another area’ of haemorrhage and congestion, apparently showing that the trophoblast elaborates a substance capable of dilating blood vessels and allowing red blood corpuscles to escape into the surrounding tissue. This is the first evidence of a possible secondary site in the human, such as is well known in the macaque. The measurements of the Hertig—Rock No. 1 are :— Chorion (external) 0.713 x 0.515 x 1.026 mm. Other human ova known are as follows, based on the size of the chorionic cavity.

Miller 04 as against 0.336 x 0276 x 0480 of the Hertig-Rock No. 1. The West and Dible 0.48 x 028. It will be remembered that the BryceTeacher I[4] outside measurement is 1-95 x -95 x 1-10. Hertig and Rock also describe another equally well preserved human ovum said to be 12 days old (Hertig-Bock No. II). Both ova were fixed for 24 hours in Bouin’s picro-formol-acetic fluid. The Hertig-Rock No. 1 is barely beneath the repairing endometrial epithelium, on the uterine surface of which is a fibrinous coagulum. In the‘ oedematous endometrial stroma there is a prominent arteriole, showing a surrounding slight predecidual reaction, such as also occurs in the endometrium adjacent to the ovum. Secretory uterine glands with cell blems, and now partially surrounded by trophoblast, and an enlarged thin-walled arteriovenous sinusoids for supplying the trophoblastic lacunm can be seen. The uterine glands are not occluded, and ascend to the endometrial surface. The ovum consists of outer syncytiotrophoblast containing blood-filled intercommunicating lacunae, which are the precursors of the intervillous spaces, and inner cytotrophoblast, giving rise to syncytiotrophoblast outwards, amnion at the embryonic pole, and extra-embryonic mesoderm inwards. The latter has invaded the blastocyst cavity and formed Heuser’s or the exoccelomic membrane (see below). The embryo consists of a thick disc-of orderly arranged cylindrical epithelial cells, lying beneath which is an irregularly arranged layer of endoderm cells, clearly marked off from the mesoderm of Heuser ’s membrane. In this respect the human embryo is easier to study than the macaque at comparable age.

In the Hertig-Rock No. 1 the intercommunicating syncytial vacuoles, future intervillousspaces, are beginning to contain small quantities of maternal blood, mainly, however, leucocytes. The syncytiotrophoblast contains small quantities of phagocytosed blood.

In both Hertig-Rock ova, the endometria are cedematous, congested and haemorrhagic. The maternal blood in the trophoblastic lacunm is almost entirely venous in origin, there being only one direct tiny arteriolar connection in the younger specimen and only a few in the older. Hertig and Rock claim that the origin of the well-known sinusoids or peritrophoblastic blood spaces appears to be from the terminal branches of the spiral arterioles, since transitions between the two types of vessel are seen especially in the younger Hertig-Rock ovum. The arterioles in the latter are said to be segmentally constructed, whereas in the older Hertig-Rock (No. II, 12 days) a large part of at least one arteriole is widely dilated. The interstitial hemorrhage in the younger Hertig-Rock (No. I, 11 days) is said to be due to diapedesis, in the older to definite defects in the walls of the venous sinusoids.

The Exocoelomic Membrane (Heuser’s membrane)

Reference has been made to the formation of a layer of cells inside the blastocyst cavity and under the trophoblast in the macaque. In the 8-9 day ovum there are only about 7 primitive endoderm cells beneath the germ disc, but in more advanced 9-day specimens, these primitive endodermic cells are continuous with cells underlying the whole trophoblast. As has been stated, Heuser and Streeter do not feel quite sure as to the origin of the new cells. If they are budded off from the primitive endoderm, they are endoderm; if they have originated from the wall of the deflating ovum, they are primitive mesoderm. It is interesting to note that Hertig and Rock unequivocally believe that a continuous stream of mesoblast cells are being budded off from the trophoblast in the human ovum before, at and after this period. Without entering into the difficult question of the nature and identification of these lining cells, we can safely trace their fate.

At first a mere lining, these cells begin to wander into the chorionic cavity and soon obliterate all the space in the cavity except for a spherical area beneath the primitive endoderm. The walls of this subendodermal space are formed very distinctly and constitute what is called nowadays the exoecelomic membrane. This membrane is similarly present also in the Miller and Werner (Stieve) ova and its subsequent fate is easily followed out. The stellate mesoblast connectives between the exocoelomic membrane and the chorionic wall break down, and the vesicular membrane drifts aside as a small sphere and is known in this free state in the Hertig-Rock No. II, the Linzenmeier, the Yale, the Peters and the Edwards-Jones-Brewer ova. Falkiner found the remains of a similar structure in his ovum in 1932, but on advice (not the present writer’s) left the description out of his published paper.

Now why not call this spherical area below the primitive endoderm “the yolk sac ”? Actually Stieve, and West and Dible did call this space the yolk sac. However, the space or vesicle does come away from the primitive endoderm, and another and definitive yolk sac is formed later. Also the network and the vesicle are formed of stellate cells of a fibroblastic appearance. It is interesting that the American authors have thus satisfactorily cleared up the nature of what many of us thought in the past were artefacts. Reference has been made above to Streeter and Heuser’s description both of degenerating cells inside otherwise quite healthy monkey blastocysts, and the very extensive necrotic zone in late monkey placentation.

Yolk Sac in Macaque

Heuser and Streeter are not clear as to how the definitive yolk sac is formed, i.e., partly from mesenchyme elements or endoderm alone. That the part of the yolk sac which abuts against the germ disc is primitive endoderm may be accepted, though the American authors seem to believe that some endoderm cells are derived from slipped down germ disc (ectomesoderm) cells. In the region of the formation of what Heuser and Streeter call the secondary yolk sac, various mesenchyme cells of the exocoelomic membrane abut against the forming secondary yolk sac, and it must be nearly if not quite impossible to identify with certainty the place of origin of the various elements concerned.

Origin of Lacunae Around Early Embedded Trophoblast

Teacher (1925)[5]believes they arise as spaces between the extending syncytial strands, while Streeter (1926) in the earlier Miller ovum considers that they arise from intra- and intercellular vacuoles. According to Krafka in the “ Torpin ovum ” there is a definite gradation from vacuoles to intercellular spaces and massive lacunae. This gradation is smaller at the luminal or abembryonic pole, and larger at the basal or embryonic pole.

So far as the presence of blood in the lacunae is concerned, it is apparently absent in the Miller, -but present in the Hertig-Rock No. 1. Reference has been made to the interesting fact that blood may occur even in the early amniotic cavity of the monkey, and too much stress cannot in future be laid on the effects of blood on the syncytium of early human ova.

Brush Border, Prickle Surface or Cuticula

These names have been applied to certain fine processes on the lacunar edges of human syncytial cells which, according to Brewer, never have brush borders in Group 1 ova. The presence of brush borders is nowadays supposed to provide useful evidence as to the age of the villi. No brush borders have been described in the macaque.

Blood-in-Glands Phase

In early pregnancy the uterine glands are usually described as being in the active secretory phase corresponding to the premenstrual phase of the menstrual cycle. Menstruation following suspected pregnancy has been recorded in the human. The so-called placental sign is a menstruation during a period of demonstrated pregnancy. Krafka has drawn attention to- the fact that no blood in the glands has been recorded in the Miller, Miiller, Stieve (Huge) and Torpin. It is usual in all Group II ova, e.g., Linzenmeier, Yale, Peters, Bryce-Teacher, and Falkiner. It would seem that the blood-in-glands reaction occurs in man and the monkey at a time corresponding with the expected succeeding menstruation, which is partially held up by pregnancy. Thus it is now claimed that blood in the glands can be an important sign of the age of the ovum. It definitely occurs in the monkey on the 17th day. Krafka suggests that during embedding two separate processes are simultaneously going on : (1) invasion of the vascular bed of the implantation site; (2) a general extravasation accompanying the oedema of an impending menstruation.

Urinary Gonadotropic Hormone in Primates

The so-called urinary prolan appears in the human throughout pregnancy from the embedding. In the chimpanzee positive Z. A. tests have been obtained up to the 4th month of pregnancy. The macaque monkey was always supposed to be negative for these tests until Hamlett showed that the Friedman (rabbit) pregnancy test gave positive results for urine of the macaque between the 19th and 25th day. It is interesting to note on the question of the place of origin of this hormone, that its appearance for a few days in the macaque, for some months in one of the great apes, and for all gestation in man, cannot be correlated with periods of placenta formation in the three groups of animals.


  1. In the human ova, hasmatids first pass into the lacunae by diapedesis, only later by rupture of maternal sinusoids.
  2. A possible function of the zone pellucida is to prevent sticking of the egg in the tubes.
  3. The human trophoblast buds inwardly mesenchyme, which aggregates to form an exocmlomic vesicle known now as Heuser’s membrane. This vesicle is apparently not endodermal, but might possibly be called a “primary endodermal sac”, but is more likely mesoblast. Subsequently a definitive yolk sac vesicle is formed later, the primary becoming detached as a free vesicle in the chorionic cavity.
  4. The human trophoblast at the embryonic end buds amniogenic cells. All around its outer surface it forms syncytium. This budding goes on for a long time.
  5. Recent work has correlated the presence of the unique spiral arteries of the uterus with the process of menstruation, and the embedding of the ovum.
  6. The monkey ovum embeds on a button or plaque of hypertrophic endometrial epithelium which is formed after fixation of the blastocyst. It seems probable that no such button is formed by the human ovum which, like that of the guinea pig, quickly corrodes its way into the maternal compacta without causing noticeable hyperplasia or decidua formation. This deep or interstitial embedding is quite different from what occurs in the macaque.
  7. The recently discovered Hertig-Rock ovum No. I is very like the well-known Miller ovum, and is 11 days old.
  8. In trying to arrive at the age of early human ova, brush borders on the syncytium, and blood in the uterine glands have definite value as evidence.
  9. Maternal cell necrosis occurs around the early embedding macaque blastocyst, and is quite extensive in the 30 days placental border.
  10. The age of ova described in recent American embryological publications has been computed by assuming that there is only one monthly ovulation, about the 13th or 14th day, that the spermatozoa live 3 or 4 days, and the ripe oiicyte only 24 hours.


  1. Contributions to Embryology. Carneg. Inst. Wash. mainly Nos. 160-169 and 179-186.
  2. Streeter’s classification.
  3. Nowhere do these American authors consider that there is more than one ovulation in the intermenstrual period.
  4. Bryce TH. and Teacher JH. Contributions To The Study Of The Early Development And Imbedding Of The Human Ovum 1. An Early Ovum Imbedded In The Decidua. (1908) James Maclehose and Sons. Glasgow.
  5. Teacher JH. On the implantation of the human ovum and the early development of the trophoblast. (1925) J Obst. Gynaecol. 31(2); 166-217.

Cite this page: Hill, M.A. (2019, June 19) Embryology Paper - Some notes on recent primate embryology. Retrieved from

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