Paper - Early human twins with peculiar relations to each other and the chorion

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Gruenwald P. Early human twins with peculiar relations to each other and the chorion. (1942) Anat. Rec, 83: 267-279.

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Note this paper was published in 1942 and our understanding of early twin development has improved since this historic human study.

Also by this author:

Gruenwald P. The mechanism of kidney development in human embryos as revealed by an early stage in the agenesis of the ureteric buds. (1939) Anat. Rec. 75(2) 240-247.

Gruenwald P. The development of the sex cords in the gonads of man and mammals. (1942) Amer. J Anat. 359-396.


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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)

Early Human Twins with peculiar relations to each Other and the Chorion

Peter Gruenwald

Department of Anatomy, The Chicago Medical School, Illinois

Two text-figures and two plates (Six Figures)

In accordance with the comparatively small number of early human embryos on record, only very few instances of twins in human ova of the first month have been described. Apart from the interest commanded by this scarcity of related findings, the twins to be described here are of importance because they exhibit a type of mutual relationship which, to the best of the author’s knowledge, has never been described before. These peculiar relations are probably the cause of a malformation of one of the partners, ourentery (Rabaud, ’00), which has never been seen in man. Furthermore, these twins represent, as will be pointed out in the course of the present discussion, an early stage of acardius formation.

Description of the Specimen

The twins were found in an ovum which had been fixed in Bouin’s fluid, sectioned serially at 10 u, and stained with hemalum and eosin. The embryos proved to be cut transversely, and a sagittal reconstruction was made in which the inner surface of the chorion nearest the dorsal sides of the embryos was arbitrarily taken as a straight line (fig. 1). The principal features will be described with the help of this reconstruction. The embryo directly attached to the chorion will be referred to as twin A, the other one as twin B. It will be noticed that twin A is incompletely preserved. Its cranial half is torn off and missing; it must have escaped through a small tear in the chorion. Normally developed organs of both twins will not be described unless such description is necessary for the following discussion.

  • A brief description of these twins was presented at the Fifty-seventh Annual Meeting of the American Association of Anatomists (see Anat. Rec., vol. 79, suppl., pp. 27-28, 1941).

The incompletely preserved embryo A will be considered first. Figure 1 shows the extent of the artificial defect. The missing portion comprised the cranial part of the embryo and extended to a point just beyond the level of the vitelline duct. The persisting portion in the series is normally developed (figs. 7, 8). It is attached to the chorion by a normal body stalk containing the narrow allantois and the umbilical vessels, and covered on its dorsal side by amniotic epithelium (fig. 8). A tapering extension of the amniotic sac follows the body stalk almost to the chorion; the allantois ends at a slightly shorter distance from the embryo (fig. 1). In the body itself, only the neural primordium must be mentioned. It does not form a closed tube in the preserved portion, in contrast to that of the other twin which is almost completely closed. It will be shown later that the condition found in twin A is probably the normal one. The umbilical veins of embryo A as shown in figure 7, are of interest because they lead not only to that embryo but, through large anastomoses, also to the umbilical veins of twin B as will be pointed out soon in more detail.

It can be assumed that the missing part of embryo A had escaped through an opening of the amniotic cavity on its ventral side, between twin B and the preserved part of twin A. A small defect (not shown i11 fig. 1) in the wall of the yolk sac of embryo B probably indicates the former insertion of the vitelline duct of twin A, although the possibility cannot be definitely excluded that both twins had separate yolk sacs (see below).

Twin B is normally developed in its cranial parts, approximately to the level of the liver primordium (figs. 1, 3, 4). No vitelline duct has been formed in this embryo, due to the absence of a detached hind-gut. Instead, the part of the body normally containing the hind-gut is invaginated into the yolk sac and covered with entoderm in such a manner that its ventral surface is lined by what would normally be the dorsal wall of the gut (fig. 5). The structures dorsal to the gut, ineluding neural tube, notochord and somites, show normal mutual relations. There is, however, no normal transition of the neural tube into an open groove and then a trunk-tail-node, as characteristic of this stage. The neural primordium forms a tube almost to the caudal tip of the body, with only a small opening near its end. No normal trunk—tail—node is present. The epidermal covering of this part of the body forms, together with the adjacent amnion, an ectodermal tube appearing sickle—shaped on cross section (fig. 5). The mesodermal surfaces of amnion and yolk sac are closely applied to each other in this area. This condition represents typical ourentery as described first by Rabaud ( ’00) in chick embryos. In the cases presented by Rabaud, only a shorter caudal part of the body was affected, and consequently the cranial part of the hind—gut was present as well as the allantois; the structures normally composing the tail were invaginated into the proximal part of the allantois. No cases of this malformation were ever described as such in other groups of amniotes; however, as pointed out previously (Gruenwald, ’41), a case of “Dottersackbruch” found in a lizard embryo by Peter (’34) actually exhibits this anomaly. In man, the present case is the first on record, apart from small protrusions of axial organs into the l1ind—gut in otherwise severely maldeveloped embryos, which might be regarded as very low degrees of the malformation in question. Body stalk, allantois, and cloacal membrane are absent in the present case (twin B).

Fig. 1 Graphic mid-sagittal reconstruction of the twins, X 20. Twin B to the left, the preserved part of twin A to the right. The arrow: indicate the levels of the figures with corresponding numbers.

Fig. 2 Diagram of a probable early stage of the same twins, also showing their principal blood vessels. Only part of the yolk sac is shown. No ectodermal or mesodermal intraembryonic organs are shown in these figures.

The lack of any direct attachment of twin B to the chorion raises the question where this embryo had the connections with extraembryonic parts necessary for its metabolism. Figure 1 shows that the only structure connecting twin B with other parts of the ovum, is the amnion which is common to both twins. Since twin B is completely preserved, it can be assumed with certainty that its body had no direct connection with that of twin A. There is, however, a strong possibility that a common yolk sac had provided for another communication, more important even than that through the amnion. Due to the damaged condition of twin A, the relations of the yolk sac cannot be established with certainty. Blood vessels leading out of twin B or into it, were found in two areas only. One of these was mentioned above when it was stated that the vessels occupying the position of normal umbilical veins in twin A, continued to twin B. They can be traced from their normal position in twin A, in the body wall near the attachment of the amnion to a similar location in the lateral body wall of twin B (fig. 5). No details of their course from one twin to the other can be given because the respective area is damaged by the artificial defect of twin A. However, the continuity can be traced beyond doubt through the amnion. No corresponding arteries were found. The second area in which blood vessels enter or leave embryo B, is its attachment to the yolk sac. No exact survey of these vessels could be made because of the abnormally extensive and close relations of the embryo to the yolk sac; it must be emphasized, however, that this is the only area where arteries lead out of twin B. This fact makes the assumption of a yolk sac common to both twins highly probable. The circulation in the wall of this common sac would then have provided for the arterial limb of the circulation, the venous part of which consisted of the above mentioned umbilical veins, and also veins of the yolk sac. An attempt was made at determining the age of the twins. Thirteen pairs of somites were counted in the completely preserved twin B. This, however, may not indicate the correct stage of general development because of the malformations present in the caudal part of twin B. The absence of a typical posterior neuropore and, caudal to it, a neural plate passing over into a trunk-tail-node, points to an anomaly in the differentiation of the early embryonic organs in that region. The corresponding portion of twin A appears to be normally developed (figs. 7, 8). This region, as well as the apparently normal cranial part of twin B, were compared with Politzer’s (’28) detailed description of a normal 18-somite human embryo. Particularly the nervous system of that normal embryo as also described by Sternberg (’27), was used for comparison. The corresponding parts of the twins show slightly earlier stages of development. The anterior neuropore of twin B, for instance, is 0.23 mm. long against 0.1 mm. in the 18-somite embryo. The condition of the ventral body wall and its reflection into the amnion likewise presents a slightly earlier condition in the twins. It can therefore be concluded that the twins were fixed in a stage of between 13 and 18 pairs of somites.

Discussion and Conclusions

In view of the damaged condition of twin A an attempt must be made at reconstructing the relations of this embryo to twin B, as well as the probable condition of its cranial part. It was pointed out in the preceding section of this report that both twins probably had a common yolk sac. Conclusive evidence of the existence of twins with one common yolk sac has been shown by Arey (’22) in an ovum containing two normal embryos attached by individual vitelline ducts to one yolk sac. Another more complicated case briefly described by Heaney and Bartelmez (’31), will be referred to later in this discussion. The diagram given in figure 2, showing a probable early stage of the twins described in the present report, is therefore based on the assumption of a yolk sac common to both embryos. This same diagram, as well as the reconstruction (fig. 1), shows both twins with their midplanes coinciding, and both embryos facing in the same direction. Direct evidence of this is shown, in spite of the damage to twin A, by the condition of the amnion and the umbilical veins running from each side of twin B to the same side of twin A. As was mentioned in the introduction, this peculiar relation of twins is so far unique. To the best of the author’s knowledge the two partners face in opposite directions in all cases of twins or double monsters with coinciding midplanes described up to the present time.

The mutual relations of the twins have a direct bearing on the question of the probable condition of twin A’s head. The inversion of the caudal part of twin B was probably brought about by mechanical interference with the head of twin A (fig. 2), and the possibility must be considered that similar pressure may have been exerted in the opposite direction as well, causing inversion of the head of twin A. In bird embryos where inversion of one end of the body is by far more frequent than in mammals, omphalocephaly (inversion of the head) occurs more often than ourentery. Its causation in single embryos is not purely mechanical (Grruenwald, ’41); in double monsters, however, omphalocephaly is very probably due to mutual interference of the partners (Gruenwald, ’37, ’41). This experience is in favor of the possibility that the head of twin A was affected with omphalocephaly. On the other hand, an omphalocephalic head torn away from the yolk sac by force, could hardly have caused so little damage to the yolk sac as was actually found. For this reason the alternative of a normally developed head is considered more probable and was followed in preparing the diagram of figure 2.

According to the present findings and considerations, the following appears to be the most probable formal genesis of the malformation in question. Two embryos developed in one embryoblast in such a manner that they had common amnion and yolk sac. Their primitive streaks were situated approximately in one straight line and both oriented in the same direction. Consequently, the caudal end of only one of them (twin A) could establish normal relations to the chorion by means of a body stalk, whereas the caudal end of the other twin (B) was situated near the cranial end of A but nowhere near the chorion. Whether the absence of structures corresponding to body stalk and allantois in twin B is a sequel of these abnormal relations, or a primary defect of the region near the caudal end of the primitive streak, cannot be established. The absence of a cloacal membrane and a trunk-tailnode of normal dimensions points toward the latter alternative, but both causes may well be jointly responsible for the development of the defect. Figure 2 shows diagrammatically how mechanical interference of the two twins probably caused ourentery in twin B, in a similar manner as pointed out previously (’37) in a discussion of omphalocephalic twins in birds. This depression of the caudal end of the body into the yolk sac must have occurred at an early stage, before the appearance of a distinct tail fold could assure normal detachment of the trunk-tail-node region from the blastoderm.

As far as could be ascertained, twin A has a normal vascular system (fig. 2). The cranial part of twin B’s vascular apparatus including the Vitelline vessels, is also normally developed. There is, however, a serious disturbance in the development of its umbilical vessels, as is to be expected in accordance with the defect of body stalk and allantois. Whether or not any arteries found in the location indicated by Au’ in figure 2, are to be considered as modified umbilical arteries, will not be discussed. For the circulation itself this question is unimportant since these vessels, just as the vitelline arteries, branch in the wall of the yolk sac. Umbilical veins were found to be present, connected indirectly with the circulation of the chorion by their anastomoses with the corresponding veins of twin A. Due to these peculiarities, blood leaving the body of twin B could go only through the vascular network of the yolk sac and then either back to twin B or, through anastomoses in the wall of the yolk sac, to twin A and thus indirectly to the chorion. Blood returning to twin B could flow either through the umbilical veins, or again through anastomoses in the yolk sac circulation (fig. 2). This shows that twin B essentially depended in its circulation on twin A; its blood had to pass through the other twin’s heart at least once on its way to the chorion and back. Somewhat similar conditions were found in a pair of human twins by Heaney and Bartelmez ( ’31). In that case, one normal embryo was found occupying the chorion together with a smaller, apparently underdeveloped twin. The embryos had separate amnions, but the smaller one had no umbilical cord. Its only connection with its surroundings consisted of a group of blood vessels leading to a yolk sac which was otherwise in normal topographic relations to the larger twin. In that case the entire circulation of the smaller embryo must have gone to the chorion via yolk sac and body of the other twin.

These two cases can safely be regarded as early stages of acardius formation although it cannot be asserted that in any of them the “dependent” twin would have developed into a typical acardius as far as its body is concerned. In a summarizing review of the subject Schwalbe (’07) cites two contrasting views of the origin of acardiac twins, and there has been no change in the status of the problem since his report. One of these views holds that the acardius is a primarily maldeveloped twin whereas, according to the other opinion, an anatomically normal embryo becomes an acardius if the propelling power of its heart is inferior to that of the other twin. The present observation, as well as that of Heaney and Bartelmez, suggests a third possibility, namely, abnormal topographic relations of a twin with a normally developed body. (The additional malformation in the present case is only incidental to the vascular condition.) The present author believes, however, that no decision is to be made among these possibilities. Any anomaly, anatomical or functional, intraembryonic or extraembryonic, may turn one twin into an acardius if its circulation becomes dependent on that of the other embryo. There is no reason to assume that all acardii must owe their development to one and the same of the above mentioned three possibilities.


1. A serially sectioned human ovum is described, containing twins with unusual malformations and mutual relations. The embryos are in a stage of between 13 and 18 pairs of somites.

2. The original longitudinal axes of both embryos are in one line, with both twins facing in the same direction. In all other known twins or double monsters with coinciding axes in vertebrates, the partners face in opposite directions.

3. Only twin A shows a normal attachment to the chorion. Body stalk and allantois are absent in twin B. This embryo is not directly attached to the chorion; it is connected only with twin A by the common amnion and probably a common yolk sac. Its umbilical veins lead through the amnion into those of twin A; umbilical arteries are absent.

4. Blood of twin B must have passed through twin A in order to reach the chorion. This shows that an early stage of acardius formation exists in the present twins. With regard to the general question of the origin. of that malformation, it is suggested that different anatomical or functional anomalies may lead to the type of circulation characteristic of an acardius.

5. Twin B is the first known case of typical ourentery in a mammalian embryo. This malformation, more common in birds, consists of an inversion of detachment of the caudal part of the body, so that it protrudes into the yolk sac and is covered by entoderm of the prospective hid-gut. In the present case the malformation was probably caused by pressure exerted by the other twin.

Literature Cited

AREY, L. B. 1922 Direct proof of monozygotic origin of human identical twins. Anat. Rec., vol. 23, pp. 245-252.

GRUENWALD, P. 1937 Ein Fall von omphalocephalen Syncephalis bei der Ente. Zeitschr. f. Anat. u. Entw., vol. 107, pp. 782-787.

1941 Normal and abnormal detachment of body and gut from the blastoderm in the chick embryo, with remarks on the early development of the allantois. J. M01-ph., vol. 69, pp. 83-125.

HEANEY, N. S., AND G. W. BARTELMEZ 1931 A case of monochorial twins with a single yolk sac. Anat. Rec., vol. 48, suppl., p. 47.

PETER, K. 1934 Ein Dottersackbruch bei einem Eidechsenembryo, entstanden im Bereich der sekundéiren Kiirperbildung. Zeitschr. f. mikr.-anat. Forsch., vol. 35, pp. 457-479.

Ponmznn, G. 1928 Ueber einen menschlichen Embryo mit 18 Ursegmentpaaren. Zeitschr. f. Anat. u. Entw., vol. 87, pp. 674-727.

RABAUD, E. 1900 Etude embryologique de l’ourentérie et de la cordentérie. J. dc l’Anat. et de la Physiol., vol. 36, pp. 619-634.

SCHWALBE, E. 1907 Die Morphologie dcr Missbildungen des Menschen und der Tiere, vol. 2. Fischer, Jena.

STERNBERG, T. 1927 Beitrage zur Kenntnis de vorderen Neuroporus beim Menschen. Zeitschr. 1". Anat. u. Entw., vol. 82, pp. 747-780.


Plate 1

3 Section of the normal head of twin B and the yolk sac.

4 Section of twin B at the level of the heart, and the yolk sac. The latter contains the ourenteric caudal end of the body.

5 Section of twin B, a short distance caudal of the anterior intestinal portal. The yolk sac, connected with the gut, contains the ourenteric part of the body. An arrow points to the right umbilical vein.

The levels of these sections are indicated in the graphic reconstruction (fig. 1). x amniotic cavity surrounding the ourenteric caudal portion of the body. X 62.

Plate 2

6 Section of twin B at the level of the transition from the normal to the ourenteric part of tl1e body. A, amniotic cavity; Y, yolk sac.

7 and 8 Sections of the normally developed caudal portion of twin A. The levels of these sections are indicated in the graphic reconstruction (fig. 1). X 62.

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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)


Gruenwald P. Early human twins with peculiar relations to each other and the chorion. (1942) Anat. Rec, 83: 267-279.

Cite this page: Hill, M.A. (2019, January 19) Embryology Paper - Early human twins with peculiar relations to each other and the chorion. Retrieved from

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