Paper - Circulation of the maternal blood through the placenta

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Ninian F. Circulation of the maternal blood through the placenta. (1939) Irish J. Med. Sci. 14(2): 59-65.

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Note this historic paper was published in 1939 and our understanding of early placental development has improved since this historic human study.

See also by this author - Ninian F. A study of the structure and vascular conditions of the human corpus luteum in the menstrual cycle and in pregnancy. (1933) Irish J. Med. Sci. 8(1): 1-16.

Modern Notes: placenta

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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)

Circulation of the Maternal Blood through the Placenta

By Ninian Falkiner.


This work has been carried out in the Zoological Laboratory, Trinity College, Dublin, under a grant from the Medical Research Council of Ireland, to Whom the author makes his grateful acknowledgment.


The circulation of the maternal blood through the human placenta has hitherto been the subject of many investigations, and the main difficulty in solving the problem has been the scarcity of material suitable for injection experiments.

For many years the same illustrations of placental circulation have graced our textbooks of midwifery until this year when De Lee‘, in the latest edition of his textbook, reproduced illustrations from the work of Rudolf Spanner’.

My interest in the subject was aroused by the study of the vascular arrangements in an early ovum described in 19323. A laborious reconstruction was then carried out which showed the arrangement of the venous and arterial channels in the decidua and their -connections with the implantation cavity. This work substantiated the descriptions of the arteries and venous channels which Bartelmesz‘ had worked out for the endometrium in its premenstrual condition, and was itself substantiated by recent work describing an early ovum of about the same stage of development (Yale)5.

For some years I have been carrying out experiments with regard to the injection technique of the uterine circulation in specimens obtained by hysterectomy, and last year, stimulated by the opportunities for research which have been put at the disposal of the profession by the Irish Medical Research Council, I determined to carry out injections of placentae, uteri, and, if possible, of a pregnant uterus if such material could be obtained at an operation for carcinoma cervicis, and of a uterus obtained at Caesarean hysterectomy. This work has been carried out in the Zoological Laboratory of Trinity College, Dublin, under Professor Bronte Gatenby’s direction and with the assistance of his staff, to whom I acknowledge my thanks.

As there has not been, to my knowledge, a detailed account of Spanner ’s work published in this country, I feel that it is necessary to recount briefly his painstaking investigations and brilliant interpretations. His work includes :-- Survey and description of vessels in the gravid uterus.

The utero-placental arteries.

The foetal vessels.

The placental septa.

The venous return flow.

The formation of the intervillous space.

The circulation in the intervillous space and the theories which have been put forward to explain it, viz. :

(1) the blood circulation directed by the energy of the heart as such;

(2) the influence of the difference of tone in the -uterine muscle on the circulation in the intervillous space; and

(3) the influence of the so-called villous pulsation on the circulation in the intervillous space.

Spanner’s experimental investigation included the injection of gravid uteri which shows the arrangement of the arteries and veins in the uterus. He describes the venous system as consisting of two networks: the first situated just beneath the decidua and of such a fine mesh that the arteries have just room to reach the decidua. This venous network drains into the second more superficial network, which in turn drains into the main tributaries of the ovarian and uterine veins.

Corrosion preparations show that the communications between the placental circulation and the deep venous network are limited to the margin of the placenta. Also by corrosion preparations Spanner succeeded in showing the arterial connections with the intervillous spaces. In contradistinction to the older descriptions the arteries are distributed irregularly in the base of the cotyledon, not as previously described by EBumm' in the placental septa. Spanner gives the total number of arterial openings into the intervillous space as 488.

The foetal vessels of the placenta as described by Spanner give a very difierent conception of the anatomy of the placenta to the accepted description. Instead of the villous tree being comparable to a tree with its branches arranged like a conifer, the villous trunk is described as being like the trunk of an inverted drooping ash or like an old-fashioned chandelier. It runs down from the chorial limits of the placenta to the decidual plate, its vessels, passing into the decidual plate and then passing again into the placenta, run parallel but in the opposite direction to the main vessels in the villous trunk.

The next part of Spanner’s work deals with the placental septa. He prefaces this section with these words: “ Position, form, construction and importance of the placental septa have up to now not been sufficiently investigated as regards their relationships to the whole pla.centa as a circulation organ.” By various methods of injection technique Spanner shows that the septa form intact boundaries to the cotyledon at the base of the placenta, but do not reach the chorionic limits of the placenta. He also finds that branches of the foetal vessels do not transgress the septa and thus the cotyledon forms a placental circulation unit. The significance of the septa not reaching from the chorionic to the basal surface of the placenta is that the maternal blood after flowing up through the adjoining cotyledons in distinct streams merges in the subchoria.l space to form the lake of blood which drains to the margins of the placenta into the circular sinus and thence to the uterine veins. Cotyledon a.—B_v leaving out all villi a big villous trunk (A) is shown. The openings of the 11t.ero-placental arteries into the intcrvillous space are seen.

Ninian1939 plate01.jpg

PLATE 1. Illustration of Placental Circulation copied from Spanner’s Monograph “ .\Ii1tterlicher und kimllir-her Ixreislauf der invnstelilirlieii 1’lu.ccnta und seine Strombahncn.”

(Some details lIl('lll(l(Y'(l in his illustration are omitted).

l. Amnion epithelium. :3-4. .\Ien1bi-ana ehorii (Chorion plate). :2. Chorion (:0nI1ective tissm.-. 3. Foetal a1't.e1'y and vein. 4. Chorial tmphublast (or its (le1'i\-'atiV(-5}. Sul)~ cliurial blood space. 6. i\'itabm-h’s fibrinoid layer. 7. Der-i<lua basalis with many sections of utcro-placental whirl artvr_v. 8. .\Iat.crnal artery. 9. .\Iat.ernal vein. 10. Muscularis uteri. ll. Peritoneum. 12. \\'|iite infarct. (fibrinoixl knot). 13. Cell island (trophoblast). l-1. Chorion laeve. A. B. 0. Three big anchoring villous trunks to which the Cotyledons a. and (1., limited by septs (4 lower arrows), correspond as well as Marginal Cotyledon c. .\I.Z. Marginal Zone.

Cotyledon b,

cotyledon b. — Shows Spanner’s conception of the branching of the villous tree. The outstanding characteristic of the branching of t.he villous tree is that the smaller villous trunks run in the form of recurrent loops parallel to each other, running vertically from the basal limits of the placenta towards the chorion. This arrangement of t.he villous tree brings to mind the picture of an antique chandelier and its candles. Note that the main vessels of the villous trunk (B) run at first into the trophoblast of the basal plate, turn there and enter {in the form of three smaller recurrent trunks) the intervillous space. In addition from the centre of villous trunk (B) comes a minor villous trunk which also runs basalwards and is connected by small anchoring villi with the basal plate but finally turns towards the chorion.

Grateful Acknowledgement is made to Professor Spanner for permission to rrprorlzrrc this coloured plate.

Experiments carried out in the separated placenta confirmed this interpretation of the direction of flow. The number of cotyledons varies from 14-30 in individual placentee.

The Venous Drainage of the Placenta

The characteristic of the central zone of the placenta is that all venous channels lie close to the placental plate and never communicate with the intervillous space. The venous drainage is, therefore, situated only in the marginal zone and consists of about 100 channels of varying diameter (1-9 mm.), with an averaget-of 2.4 mm. Proof of this is adduced from the fact that in injection experiments of the venous circulation by a» partial method these marginal zone vessels are the first to fill.

The marginal sinus is of constant occurrence and is of fundamental importance in the placental circulation. By removing the upper chorial wall the communications of the marginal sinus with the intervillous space are seen. These take different forms, either port-hole-like openings or the medial partition may be lacking so that it merges into the intervillous space without a border. Spanner interprets this medial wall as the altered septa of the marginal; cotyledons but which, contrary to the other septa, reaches as far as the chorionic membrane.

The marginal sinus is often divided by an incomplete division wall. Drainage openings into the uterine veins are numerous. These divisions in the sinus are more rigid than vein walls and interpreted as holding the vein open under altering pressure conditions.

The marginal sinus measures 2 cm. by 3 cm. in places, but may be much smaller, with a diameter as little as 0.5 cm. in places;

The sub-chorial blood space is situated in that region of the placenta immediately subjacent to the chorionic membrane and is traversed by the villous trunks, but is itself free from villi. It measures 0.5 cm. or more in depth, but it is not shown in sections of separated placenta owing to the blood draining out immediately through the large openings in the marginal sinus, as can be observed in any placenta after delivery. Its existence is proved by injection experiments and its connections with the marginal sinus are easily demonstrated by Spanner.

Spanner’s description of the placenta is well illustrated in Plate I, which is taken from his monograph.

The features shown are the blood entering the basal part of the placenta by means of the utero-placental arteries. The blood is delivered into the various cotyledons which are units in the basal part of the placenta where the villi are numerous. The branches of the villous trunk are illustrated in the same formation as the branches of a drooping ash. This arrangement is suited to the direction of the blood stream. The many blood streams on filling up the cotyledon overflow the upper margins of the septa and the whole placental blood stream merges into a single stream in the sub-chorial space. This stream is directed towards the margin of the placenta and makes its way into the circular sinus and marginal part of the placenta where it drains directly into the uterine veins.

This conception of placental circulation is quite new and appears more rational than the explanations hitherto accepted.

The first injection experiments to be described in this paper were carried out on uteri which had been removed for functional haemorrhage in women nearing the menopause. The technique adopted was that the uterus immediately after removal was placed in a 3.8 per cent. citrate solution at body temperature. Both uterine arteries were then dissected so as to enable the tying in of small glass cannulae. Clamps were placed on the infundibular pelvic vessels and the uterine circulation Washed out with citrate solution until the return flow was clear or almost clear. This washing out was done by hand, as previous experiments with a gravity feed had proved unsuccessful. The injection material (carmine gelatin) was then injected until the whole surface of the uterus indicated a filling of the small vessels. Then all arterial and venous trunks were carefully tied and the specimen fixed in Carnoy solution.

Sections of these specimens were taken across the whole depth of the uterus. These sections showed the distribution of the arterioles and small venous channels in the entirety of the uterine structure. Beautiful illustrations of the circulation could be seen not only in the sub-peritoneal tissues but also throughout the muscle and in the endometrium. fig. 1 shows a section across the uterus about the level of the insertion of the round ligaments. This illustration is reproduced. as it shows the extraordinary vascularity of the mucous membrane compared with other parts of the uterus. Careful study of sections such as the one illustrated, in various specimens, revealed that the injection material had in some places filled the small arterioles of the uterine mucosa.

Fig. 2 shows a very markedly spiral arteriole running in the spongy layer of the mucosa.

Other parts of the mucosa showed the venous channels and the complicated, possibly capillary, channels which occupy the area immediately beneath the uterine cavity, i.e., the compact layer of the endometrium. These intercommunicating small venous channels are drained by larger but again intercommunicating channels and cross down towards the muscularis. fig. 3 shows the venous circulation in the endometrium. fig. 4 is a reconstruction from serial sections. The value of this reconstruction is to show the frequency of the small arterioles and the extraordinarily complicated network of venous channels. These illustrations of circulation in the endometrium confirm the work of Bartehnez and in a. sense were only incidental findings in the course of developing the technique of injecting specimens. They have special interest, however, in showing the exact type of vascular conditions preceding implantation of the ovum.

The next specimen which I wish to describe is a uterus obtained at an operation for carcinoma of the cervix in a woman who was six to eight weeks pregnant. The injection of this specimen through the uterine arteries was attempted after a preliminary washing out with citrate solution, but the injection mass did not reach the intervillous space. However, certain interesting points are shown, and fig. 5 is a cross section of this uterus which shows the Young placenta in the process of formation, partially separated by thromboses, but with the central part of the placenta still in situ. The utero-placental arteries can be traced right up to the intervillous space and a small amount of the injection mass had made its way between the villi. fig. 6 shows a high magnification. The basal part of this placenta and a utero-placental artery (coil artery) are shown. The lumen of the artery is partially filled with the injection mass.

The third specimen was a uterus obtained at Caesarean hysterectomy and as this specimen yielded rather remarkable results I will describe the technique applied in detail. At operation—a classical Oaasarean section-———the placental site was involved in the incision, that is, the lower part of the placenta became separated during the incision and delivery of the infant. A subtotal hysterectomy was then rapidly carried out and the uterus was placed in warm citrate solution. Immediately the process of dissecting out the uterine arteries and introducing cannulae was undertaken. The whole uterus was washed out with citrate solution. It was noted that the citrate solution was coming out through the severed vessels in the incision in the uterine wall. The incision was rapidly stitched up in such a way as to occlude these vessels. Then the citrate was kept running through the uterine arteries until the return flow through the infundibular pelvic and uterine veins was completely clear. This took some little time and the citrate solution surrounding the uterus was constantly changed not only to maintain the temperature but to keep it comparatively clear. The carmine gelatin solution was then run in until it could be seen clearly coming back through the uterine veins and it could also be seen seeping out through the incision to some extent. It also made its appearance in the cavity of the uterus. The whole uterus was then placed in Carnoy solution and when it was fixed to some extent, 48 hours later, it was carefully cut across so as to show the placenta in situ. The placenta had remained in situ except where it had been separated during the operation. The injection mass had run up in the utero-placental arteries into the intervillous space, up to the sub-chorial blood space and thence to the circular sinus and back to the uterine veins. fig. 7 is a photograph of the specimen after it was cut across. This photograph is reproduced to show the specimen as it appeared. fig. 8 is a drawing of this photograph which shows diagramatically the utero-placental arteries, the sparse distribution of the injection mass amongst the villi, the complete filling of the sub-chorial blood space and the marginal sinus. A point worth noting in these two plates is the shape of the whole placenta. It is not the flattened deflated organ that we are accustomed to see after delivery, but is much more rotund. We must remember that the maternal and fmtal blood is always completely or partially drained from the separated placenta. It is this fact which makes the recognition of the sub-chorial blood space diflicult in the separated placenta. A further study of various sections demonstrated the placental septa and reconstruction of the maternal artery ascending in the placental septa was possible. In fig. 9 a placental septum is shown and can be readily distinguished from the villous trunks which are also well demonstrated. A reconstruction of the vessels in the placental septum was made, as there seems to be a certain amount of doubt as to the significance of these vessels. This reconstruction is reproduced in fig. 10 and shows its convoluted course and openings into the intervillous space. fig. 11 is a photograph of the placental septum shown in fig. 9 at a higher magnification. In fig 12 the relationships of the marginal sinus of the placenta and uterine veins are well demonstrated, also the relationships of the chorion, amnion and decidua at the margin of the placenta. The marginal sinus is divided by a partition wall at this point. Such partition walls are constant findings in the marginal sinus but do not extend throughout the whole circumference of the sinus.


The distribution of the injection material in the last described specimen supports Spanner’s contentions with regard to placental circulation. first of all, the utero-placental arteriescan be demonstrated and their communication with the intervillous space is clearly shown. Next, in that part of the placenta -lying near the basal or decidual plate, the injection material is rather sparsely distributed amongst the numerous villi, but as one traces the intervillous space towards the chorion the injected material becomes greater in amount while the villi become less numerous, while immediately under the chorion a solid mass of injection material is present. At the periphery of this sub-chorial mass of ."'jection material one can trace a communication leading into the marginal sinus which itself communicates with the uterine veins. Such a distribution of the injected material would fit in with Spanner’s interpretation for, if the blood is altogether delivered to the intervillous spaces by the utero-placental arteries situated irregularly at the base of the placenta, but limited to the central zone, it will spread upwards in the intervillous space, its lateral flow being limited by the placental septa. The placental septa do not reach the chorial limits of the placenta and thus the blood in each cotyledon merges into the c-ommon stream in that part of the intervillous space above the level of the septa. This blood having traversed the intervillous space now forms" a large lake or pool immediately subjacent to the chorion which drains out to the periphery, into the marginal sinus and thence to the uterine veins.

Fig. 1. Micro photograph of transverse section of the uterus which had been injected through the uterine arteries with gelatin Carmine mass. The dark area beneath the surface of the endometrium shows the distribution of the injection mass in the arterioles and capillaries.

Fig. 2. Microphotograph of endometrium in injected specimen showing arterioles and their spiral st-ruot-11re.

Fig. 3. Microphotograph of the endometrium in injected specimen showing the capillary channels in the compact layer with the small veins which come down from the compact layer towards the muscularis.

Fig. 4. A reconstruction prepared from the sections of an injected uterus showing the complicated anastomoses of the venous channels (black) and the large number of arterioles (white) in comparison with the number of glands (stippled).

Fig. 5. Microphotograph of section of pregnant uterus (6-8 week 8) showing the young placenta in situ. This specimen was injected through the uterine arteries, but the injection mass did not fill the intervillous space.

Fig. 6. Microphotograph of the basal portion of the placenta from the specimen shown in fig. 5. The section shows the injection mass which has filled the utero placental arteries almost as far as their openings into the intervillous space.

Fig. 7. Photograph of uterus removed at Cz13sa1'ea,1'1 hysterectomy. The uterus was Injected w1th gelat-111 eat-mine mass through the uterine art-eries. The entrance of a. utero plaeental artery into the intervillous space is clearly shown (arrow).

Fig. 8, Diagrammatic drawing of specimen shown in Fig. 7. 1st aI'1‘Ic)>W—-—Uf-61‘0placent-3.1 artery.0peI1_1ng mt-0 t-}_1e 1nterv111eus space. 2nd 8.I‘I'0j.>s: e§[se (LoniglomeI'a.tio11 of mject-1on mass 111 sub-chomal .r<I=g10n. 3rd a,110w~—— ax-gma sinus. 4t-h arrow — Umbilical cord.

Fig. 9. Micro photograph of section of full term placenta in situ. The distribution of the injection mass in the intervillous space is well shown. The sub-chorial blood space and marginal sinus are filled with injection mass. The section also shows the villous trunks (arrow) and the placental septa; (arrow).

Fig. 10. This figure is a reconstruction of a maternal artery running in a placental sept. An opening into the intervillous space is shown.

Fig. 11. Photograph of a placental sept which clearly shows the presence of the gelatin carmine mass in the maternal vessel coursing upwards in the placental sept. =This photograph is of one of the sections used in the reconstruction shown in fig. 10.

Fig. 12. Microphotograph of the margin of a full—term placenta in situ, the specimen having been injected through the uterine -arteries with carmine gelatin mass. This photograph demonstrates the relationships of the marginal sinus to the sub-chorial blood space, the intervillous space and the uterine veins. The sinus is divided by a partition wall (arrow) and the lower part of the sinus can be seen communicating with t-he uterine veins. The injection mass can be traced directly into the uterine sinus (arrow). A feature in this Photograph is the demonstration of the relationships of the chorion, amnion and decidua at the margin of the placenta.

Spanner concludes that the chief motive force in the placental circulation is derived from the vis a tergo of arterial blood pressure. Itis very diflicult to determine What eflect the contractions of the uterine muscle have on the placental circulation.

Obviously the contraction of the uterine muscle may aflect the circulation in three different ways. One, by altering the inflow of blood; two, by pressure on the blood lake in the placenta itself and, three, by altering the pressure in the venous outflow. Probably the greatest effect is the increased pressure on the blood in the sub-chorial blood space in which case the effect of painless contractions of the uterus would be to squeeze the blood out of the placental circulation into the maternal veins. The difficulty of accepting such an effect of uterine contractions is that the effect of the contraction on the uterine veins Would be one of diminishing the calibre of the vessels draining the placenta. This would tend to hinder the flow of blood from the placenta to the maternal veins. Another suggested factor in the circulation of the blood through the placenta is the so-called villous pulsation. It would be difficult to imagine that the rhythmic pulsations present in the foetal vessels both of the trunks and of the finer branches can have effect on the direction or force of the flow of the maternal blood. I therefore agree with Spanner that the main factor in the flow of blood through the placenta is the maternal arterial pressure, but that the influence of the contraction of the uterine muscle has not yet been measured.

In conclusion it may be pointed out that the findings which Spanner has published provide a satisfactory illustration not only of the circulation of the blood through the placenta but also a very clear conception of the anatomy of the organ. In my opinion such complete knowledge of the placenta is an essential if the significance of pathological lesions in the placenta is to be understood.


1. De Lee, J. B.: Principles and Practice of Obstetrics. 7th Edition. Pp. 41-44.

2. Spanner, Rudolf: “ Miitterlicher und kindlicher Kreislauf der menschlichen Placenta und seine Strombahnen.” Zeitschrift fiir Anatomic and Entwicklurngsgeschichte, 1935, cv. 2, pp. 163-242.

3. Falkiner, Ninian McI.: “ A description of a Human Ovum fifteen Days old with special reference to the Vascular Arrangements and to the Morphology of the Trophoblast.” J o. Obst. and Ggzm. Brit. E-mp” Vol. 39, pp. 471-509. .

4. Bartelmez, G. W.: “ The Human Uterine Mucous -Membrane during Menstruation.” .Ame'r. Jo. Obst. and Gym, 1931, xxi, 5.

5. Ramsey, Elizabeth M.: “ The Yale Embryo.” Contributions to Embryology, No. 161, from Publication 496 of Carnegie Institution of Washington, 1938, pp. 6784.

6. Bumm, E.: Arch. f. Gymik., 43 (1893), 37 (1890).

Cite this page: Hill, M.A. (2019, August 21) Embryology Paper - Circulation of the maternal blood through the placenta. Retrieved from

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