Book - Contributions to Embryology Carnegie Institution No.56-15

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Chapter 15. The Villi in Abortuses

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Mall FP. and Meyer AW. Studies on abortuses: a survey of pathologic ova in the Carnegie Embryological Collection. (1921) Contrib. Embryol., Carnegie Inst. Wash. Publ. 275, 12: 1-364.

In this historic 1921 pathology paper, figures and plates of abnormal embryos are not suitable for young students.

1921 Carnegie Collection - Abnormal: Preface | 1 Collection origin | 2 Care and utilization | 3 Classification | 4 Pathologic analysis | 5 Size | 6 Sex incidence | 7 Localized anomalies | 8 Hydatiform uterine | 9 Hydatiform tubal | Chapter 10 Alleged superfetation | 11 Ovarian Pregnancy | 12 Lysis and resorption | 13 Postmortem intrauterine | 14 Hofbauer cells | 15 Villi | 16 Villous nodules | 17 Syphilitic changes | 18 Aspects | Bibliography | Figures | Contribution No.56 | Contributions Series | Embryology History

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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)

As long ago as 1832 Seiler stated that, although he could not be certain from a magnification of 40 diameters, he did not think that chorionic villi were hollow. Although Seiler concluded even at this time that villi are filled with cellular tissue, the idea that they are hollow nevertheless persisted up to 1889. Seiler thought that the first vessels invaded the villi as late as the third month. He represented individual villi from chorionic vesicles from the fourth, fifth, and twelfth week as clubbed in form, and also pictured several good villous trees. It is of particular interest that he also represented a branching villus ending in a spherical termination, which suggests the "Zellknoten" of Kastschenko.

Muller (1847) claimed that villi may grow until they are 2 inches long by the fifth month, at which time he thought they still might cover two-thirds of the entire surface of the chorionic vesicle. However, Muller's statement that the villi are often cystic indicates quite clearly that he was not dealing with wholly normal material, and that he probably saw degenerate or even hydatiform specimens.

Robin (1854) apparently assumed that normal villi are hollow, for he stated that fibrous, fibrinous, scirrhous, tubercular, fatty, and calcareous changes of the placenta are made possible by fibrous obliteration of the cavities present in normal villi. Robin believed that such changes as these normally occur in the non-placental portion of the chorionic vesicle, and stated that unbranched and degenerate villi are found in placenta? of all ages. From his descriptions one may conclude that Robin noticed both the fibrinoid and the decidual layers of the placenta and possibly also the presence of so-called infarcts.

According to Winckler (1872), Bidder, Jr., showed that the villi are especially densely set and particularly thick in caliber at the margin of the placenta. Winckler himself distinguished three kinds of villi. He stated that atrophic villi are found everywhere, and that they never penetrate the maternal tissues beyond the closing plate (Schlussplatte) described by him. These villi, which were said to reach the cavernous spaces of the decidua, he declared to be uncovered by epithelium. Indeed, Winckler believed this to be true also of all other villi as long as they had not penetrated the closing plate of maternal tissue, into which his second class of villi were said to continue considerable distances without branching. He believed that the villi obtain a covering of epithelium only after they reach the cavernous spaces or blood-sinuses. His third class of villi, which also were said to be devoid of epithelium as long as they lay in the maternal tissue, differed from the second class only through their greater development.

Langhans (1877) emphasized the irregularities in the villi which had been mentioned by Muller, and concluded that villi always are vascularized.

Kolliker (1884) was especially impressed by the fact that the form of the villi varies so greatly that one can hardly make any generalizations. He found that branching might occur even at right angles, and that terminal branches which do not reach the placenta remain free. These free endings were said to be present in placentae of all ages, and to be filiform, cylindrical, pear-shaped, or club-shaped. Branching was said to be so frequent and the interlacing of these branches so common that only narrow intervillous spaces could be preserved in the placental area. Kolliker particularly distinguished branches which he called fastening rootlets (Haftwurzeln), which, according to him, were described by Ercolani and also by Langhans. These were said to always enter the placenta and to become attached to it so firmly that only considerable tension can separate the chorionic vesicle from the placenta. Kolliker stated that these fastening rootlets are commonest near the septa of the maternal tissues which separate the cotyledons, but that they nevertheless are found also in the center of the latter.

Kastschenko (1885), in a careful study of the epithelial covering of the villi, stated that they become more numerous in the region of the serotina by the end of the second month, and believed that villi grow only by means of terminal and never by lateral buds.

Minot (1889) accepted the opinion that villi are hollow during the earliest stages of development only, and stated that the villous nodules are especially common in older placentae. In speaking of the collaginous tissue (Gallertschicht) composing the inner portion of the villi, Minot stated that it usually contains a considerable number of large, uninucleated, granular wandering cells, now frequently spoken of as Hofbauer cells and discussed more fully in the previous chapter.

Giacomini (1892), in describing a young tubal conceptus, the villi of which were not evident macroscopically, apparently regarded some of the syncytial buds as representing young villi, and later (Giacomini, 1893), when considering chorionic vesicles devoid of an embryo, which had evidently undergone hydatiform degeneration, again spoke of the presence of many syncytial buds, some of which he again interpreted as being young villi.

De Loos (1897), who had no material from the first 6 months, believed that all early conceptuses are covered completely by villi which are solid epithelial buds in the earliest stages. He further believed that "they become hollow later and are invaded by mesenchyme after vacuolation of the syncytial buds has prepared the way for this invasion. According to de Loos, all villi in contact with the decidua basalis become vascularized, and he distinguished between stem, or original, and fastening or nutritional villi. From a study of cross-sections of villi, he concluded that the number of villi with small caliber increases from the third to the fifth month, and that the caliber is greatest at the fourth month. De Loos also thought that the caliber of the villi decreases with the branching, and that there are relatively more villi of small caliber in full-term placenta?, which he regarded as evidence that new villi are constantly arising. Since Wiskott (1882) had found only syncytium present on villi at the sixth month, de Loos concluded that villi in older placentas which still are uncovered by epithelium necessarily are hollow.

J. Kollmann (1898) found villi 1 mm. long and well developed in a chorionic vesicle of 6 mm. and stated that they might either be universally distributed or merely equatorial. This writer, who limited the term ectoderm to the Langhans layer, apparently referred the syncytium to a maternal origin. He also spoke of nonvascular villous branches about 1 mm. thick, which played the role of fastening villi, and distinguished two kinds, viz, ectodermic villi without a stroma and mesodermic villi with it. In 1907 Kollmann used the term villi terminales for villi which had traversed trophoblastic nodules, and villi adherentes for those the terminations of which ended in or were joined to each other by the trophoblast or a decidual plate.

Paladino (1899), although studying mainly the epithelium, stated that one of the vesicles, the age of which he estimated as 13 or 14 days, was covered completely by villi. Webster (1901), who devoted considerable attention to villi, recognized the presence of floating villi and found that villi, as a rule, are much more numerous and are branched by the sixth week. According to Webster, the mesoblast in the youngest villi is finely granular, vacuolated, and stains but faintly. He also found villi which were attached to the chorionic vesicle by syncytial stalks only, an occurrence which he attributed to failure of the mesoblast to penetrate the early plasmodial bud. He found many more small villi present by the fourth month, and stated that the mesenchyme around the vessels is usually condensed at this time. By the sixth month the villi were said to be slender and more branched, and lateral budding was said to be much less frequent. Aside from changes in the epithelium, Webster found the connective tissue of the small villi to be loose or mucoid as term was approached, and stated that the villi are more simple, possess fewer buds and branches, and are in part nonvascular in the region of the chorion lave by the sixth week.

Marchand (1903) found that villi 1 mm. long uniformly covered a chorionic vesicle 14 to 15 mm. in size, except at its mid-portion, in which a fold was located. None of the villi were said to reach the capsularis at this time and all were nonvascular. Marchand stated, however, that the mesenchyme cells frequently were arranged in rows so as to simulate young capillaries. In a second specimen, 14 mm. in size, the villi, on the contrary, were largely restricted to the region of the decidua basalis. Only isolated villi were found at the opposite poles, and but very few on the lateral surfaces. These were branched but slightly, but some of them were vascularized.

Bonnet (1903) described early lymphatics in the villi and represented a ciliated border and also a membrana limitans. It seems that Kupffer (1888) was the first to describe the ciliated border, reported later also by Marchand (1903), and even more recently by Friolet (1905), Stoffel (1905), Daels (1908 a ) and Herzog (1909), in all thin sections of the villi. Rossi Doria (1905) explained the so-called ciliated border by the manner in which the erythrocytes become embedded in the margin of the syncytium; and although a reticulum also has been described in the stroma of the villus, later histologic studies do not confirm the presence of it, of a membrana limitans, or of a ciliated border. These things, however, do not deny the fact, confirmed also by Fossati (1906), that a network can be revealed in the stroma by the use of the Apathy, Golgi, Van Gieson, Mallory, and Cajal methods of staining. This, however, does not necessarily demonstrate the existence of a true reticulum.

Rossi Doria (1905) found young villi which had not yet been invaded by mesenchyme and emphasized that the two layers of chorionic epithelium had not yet differentiated in Peters's ovum. Nevertheless, a reference to the illustration accompanying Peters's monograph shows very clearly the presence of short villi containing stroma, even in this specimen. According to Rossi Doria, the mesenchjane begins to appear first in the villi during the second week, at which time they also begin to branch and become vascular.

Friolet (1905), who examined a chorionic vesicle 11 by 12 by 9 mm., the age of which he estimated as 3 to 4 weeks, concluded that villi arise by the extension of the fetal mesoblast into the trabeculae of trophoblast, and regarded a. brush border as a natural attribute of the syncytium. Friolet found the villi developed better in the region of the basalis and especially around the whole periphery of the mid-zone of the chorion. They were sparser in the capsularis, though without degenerative changes.

Kworostansky (1903) discussed the mesodermic structure of the villi, including the Hofbauer cells, finding the stroma much as we know it now; but Michaelis (1903) claimed to have found a granular line between the stroma of the villus and the Langhans layer, which he regarded as indicating the existence of a definite limiting membrane. Michaelis concluded that the existence of this membrane finally disposed of the idea that the Langhans layer may arise from the stroma, but anyone familiar with the appearances produced by Bielchowsky's stains between the epithelium and the stroma of the villi will question Michaelis' conclusions.

Von Lenhossek (1902) also recognized the existence of a basement membrane, and Frassi (1906), upon the basis of material stained with silver nitrate, stated that the villi in the greater number of moles have a limiting membrane, fibrous in nature, which he regarded as "identical in form and structure with that demonstrated and described in the villi of young placentae." However, Daels (1908 3 ), from the use of Weigert preparations, concluded that a la}^er of fibrin, the product of degenerative changes, forms between the exochorion and endochorion, and Friolet, who at first could not find a membrana limitans, said to have been described first by Langhans, found a definite hyaline zone in an abortus from the third month.

Happe (1906) found the villi of chorionic vesicles of the fourth to the sixth week branched and about 2 to 7 mm. long, but nevertheless nonvascular. The form of the youngest villi, which were about 2 mm. long, was said to be polyplike, the ends being swollen. Most of the villi of the three conceptuses from the fourth to the sixth week showed an increase in caliber at the point of branching, the swellings being especially marked at the origin of the terminal branches of some of the villi. Happe stated that Hofbauer cells were not present in the youngest villi, and that those of the older conceptuses contained only a few.

Eternod (1909) divided the development of the villi into five phases: (1) a primordial, avillous syncytial phase; (2) an avillous trophodermic phase; (3) a trophodermic, transitory, zonal villous phase; (4) a diffuse, placental villous phase; and (5) a diffuse, chorionic, and chorion-frondosum phase. Eternod placed the conceptuses of Peters and Leopold in the second or avillous phase, in spite of the fact that both these vesicles had short villi containing mesenchyme. His third phase was illustrated by the specimens of Reichert and Ahlfeld and one of his own in which the villi had an annular or equatorial distribution. According to Eternod, the portions of the chorionic vesicle which later are in contact with the basalis and capsularis are devoid of villi during this phase, which he regarded as a transitory, but nevertheless necessary, phase. He believed that the bare areas upon the chorionic vesicles resulted from inequalities in the expansion of the chorion, and stated that in the specimen of Reichert and in one of his own, the ventral or capsular bare area is less evident than the basal or dorsal, as he called it. He believed that the ventral bare area disappeared earlier than the dorsal, only to reappear again, however, when the chorion laeve developed. Although he was not absolutely decided in this matter, Eternod believed it improbable that young villi are interpolated between the older, concluding that the chorion frondosum is enlarged through the addition of villi at its periphery with far greater regularity than heretofore suspected.

The fourth phase in the development of the villi, according to Eternod, occurs in vesicles with a length of approximately 9 to 16 mm. In such the villi are branched and their terminations fused by trophoderm. The fifth phase follows the fourth very quickly, for it is said to be present in chorionic vesicles 17 mm. in size, and to be characterized by great inequalities of growth- and by far greater complexity in the basal area than in that of the capsularis.

Dandy (1910), in describing a chorionic vesicle 16 by 14 by 12 mm., found the villi branched and about 0.1 mm. thick and 1.25 mm. long. He stated that they "are more numerous at the point of attachment of the Bauchstiel and gradually fade away on all sides until, finally, a clear zone results from their absence on the opposite pole. . . . From the epithelial layer of the chorionic membrane and villi numerous buds develop, some from the syncytial layer alone, others from both layers of the epithelium. These represent proliferating and new forms of villi."

Miller (1913), in describing a conceptus 0.83 mm. in greatest diameter, stated that the mesodermic villi were as yet absent, and that the Langhans and syncytial layers were structurally identical, although already distinct. Lazitch (1913) called attention to the fact that the conceptuses described by Peters, Leopold, Strahl and Beneke, and Fetzer showed the earliest villi to be mesodermal buds, and that the specimen reported by Jung already showed the presence of dichotomy. Lazitch stated that the villi are less irregular and more cylindrical in form in the fifth month, and that curious forms, such as "little-horns," are rare. She stated further that the villi became long at term and possessed fewer buds, some of which looked as though they were branches arrested in development. Lazitch also found many ectodermic nodules or proliferating islands. In a conceptus measuring 26.5 by 22.0 by 14.5 mm., she found the villi 3 or 4 mm. long, with branches and trunks so oblique that they were almost parallel to the chorionic surface. According to her, the villi converge towards the poles of the chorionic vesicle, as stated by Eternod, but possess so variable a form that it is difficult to describe them, the caliber changing from thick to thin, from wide to narrow, from cylindrical to folded so quickly that a single branch sometimes possesses all these characteristics. She found anastomoses fairly numerous, but free villi ending in epithelial prolongations were rare. Most of the anastomoses seen resulted from ectodermic fusion, but villi separated by some distance and united by true villous bridges containing mesoderm were also seen. According to Lazitch, dichotomy occurred in 65 to 70 per cent of the villi, trichotomy in 20 to 25 per cent, and a more complex form in 10 per cent. The branching usually was at an acute angle, but branches which diverged 180 also were found. Since buds were present on the chorionic membrane, Lazitch concluded that a moderate amount of interpolation of new villi among the old undoubtedly occurs.

Johnson (1917) found the villi on a chorionic vesicle, containing an embryo with 24 somites, variable in size and 1.1 to 1.3 mm. long in the region of the chorion frondosum. Johnson stated that the villi were usually smaller at the bases, and that smaller villi, although few in number, were found among the larger.

Ingalls (1918) also found the villi on a chorionic vesicle 9.1 by 8.2 by 6 mm. to vary greatly in size and shape, but stated that the chorionic vesicle seemed to be covered by them over all of its surface. This finding of Ingalls seems to be in accord with observations upon the best-preserved and youngest specimens in the Carnegie Collection. Small chorionic vesicles, with one or two opposite bare areas, and others with sparsely set villi, are not rare, but at present we possess no evidence establishing the strictly normal nature of these specimens. Among these specimens is the vesicle represented in figure 7 (plate 1, Chap. IV). Isolated and sectioned villi from this specimen show the presence of but slight branching and rather cylindrical villi. The absence of some of the villi in this specimen is due to the mechanical means used in the removal of the blood-clot before the specimen was received.

A vesicle which, though macerated, deviates only very slightly from the normal, is No. 1878, the exterior of which is represented in figure 232 (plate 19, Chapter XIII), and the portion bearing the embryo in figure 233. As seen in the latter figure, these young villi look unusually matted and bulbous, though it must be remembered that young villi necessarily are united and covered by trophoblast in which they are implanted. Some isolated specimens of these villi are represented in figure 242, and what especially strikes one's attention is the presence of an exceedingly fine basal portion in the villus to the left. Although the caliber of normal young villi varies considerably, I do not believe that such forms as this can be regarded as strictly normal, and this belief is confirmed by an examination of sections of the villi, shown in figures 243 and 244. It is possible that maceration alone is responsible for some deviation from the normal form of these villi, but it is not improbable that one of the specimens, shown in figure 244, illustrates incipient hydatiform changes.

In contrast with this specimen stands the vesicle, No. 2053, shown in figure 245. This is a somewhat older, but perfectly normal, chorionic vesicle, some of the villi from which are shown in section in figure 246. All of the villi of this specimen are of approximately the same development, and although trichotomy is present and simpler forms of branching are common, no marked diminution of the parent stem seems to occur at the point of branching. Moreover, the branches are approximately as large in caliber and sometimes even larger than the main trunk.

Somewhat older vesicles are Nos. 866, 2108, and 1892, represented in figures 247, 248, and 249. The first of these possesses decidedly fibrous, filiform villi, partly covered by decidua, such as are not uncommon in cases of retention. No. 2108 shows the characteristic towsled appearance of the villi in many chorionic vesicles with early hydatiform changes. The villi in these vesicles are usually longer than they ordinarily should be, and this fact alone shows that the stroma must have grown, unless one assumes, as did Daels (1908 a ), that it is mere y pulled along by the proliferating exochorion. In view of this belief, it is especially interesting that Daels thought that the stroma nevertheless might be increased instead of rarefied.

The villi in No. 1892 show early maceration changes, and that growth of this vesicle ceased some time before abortion is indicated also by a menstrual age of 54 days, although the size of the vesicle suggests an age of only 42 days. Some villi from this specimen, represented in figure 250, show the presence of maceration and also establish the fact that the villous trees have reached considerable complexity at this time. When maceration changes are more prolonged and lysis of the villi advances so far that they are structureless or almost so, one gets such shadow forms as those represented in No. 2197 (fig. 251). In these villi nothing remains but a mere gossamer, and the exterior of the entire chorion often has an eiderdown appearance, as suggested in a minor degree by this specimen (fig. 252) and to a far greater degree by No. 993, shown in figure 259. The villi of the former vesicle, the exterior of which measured 23 by 20 by 16 mm. and the interior 16 by 13 by 10 mm., although only 2 to 4 mm. long, nevertheless have reached considerable complexity in form, for a dozen or more branches sometimes leave the main stem at about the same place. Villi from other vesicles of approximately the same age may, however, be much longer, as illustrated by No. 1287, represented in figure 253, a specimen which also shows early hydatiform degeneration. In this case the relatively small size of the chorionic vesicle is evident at once upon inspection of the cross-section of the entire vesicle. The presence of matting and maceration is equally evident, and anyone at all familiar with these vesicles would not expect to find many traces of an embryo.

The presence of hydatiform degeneration is very common in abortuses of the fifth to sixth week. This is well illustrated by the villi shown in figure 255. A fairly normal villus and, for a specimen of this age, the largest found, is represented in figure 254. Many small knobs are seen along the branches of this villous tree, to the right of which there also are some macerated villi and to the left others fused by trophoblast. The contrast in form, surface, and appearance between the hydatiform and the normal villous tree is very striking indeed, and it would seem that the hydatiform villus largely loses its power of branching, and, except for local increases in caliber, grows mainly in length.

A somewhat older, apparently normal chorionic vesicle with normal villi is No. 2361, shown in figure 256. In this vesicle, which measures 35 by 35 mm. and which has an age of about 4J^ weeks, some of the villi in the basal area are very plainly hydatiform, although also macerated. Both of these changes are noticeable also in some degenerated villi shown in figure 257, but inspection of the capsular area of this chorion shows that no hydatiform change is evident here, nor is it evident on the external surface of the abortus represented in figure 258. This is due to the fact that the process is in its early stages, and because the conceptus is surrounded by decidua. Although the specimen has a menstrual age. of 124 days, the abnormal embryo (shown in figure 206, plate 18, Chap. XIII) is but 3 mm. long and the chorionic vesicle only 35 mm. in diameter, measurements which indicate anatomic ages of 4^ and 6J/2 weeks, respectively. Hence, if the menstrual age can be relied upon, this specimen must have been retained 80 days. This does not imply, however, that the chorionic vesicle necessarily had been dead during all this time. Judged by the menstrual age, the fetus should be 150 mm. long, and as judged by the chorionic diameter it should be 13 to 14 mm. long instead of 3 mm., its actual length.

A second good example of the development of hydatiform degeneration, especially in the area of the basalis, in vesicles of this size is found in No. 2077 (represented in fig. 101, plate 8, Chap. IX). This vesicle, which measured 40.5 by 28.5 by 18.5 mm., was reflected from the underlying decidua, but was nevertheless left attached to it so as to expose a large field of exquisite hydatids, a portion of which is shown in focus in the center of the figure.

The eiderdown appearance due to maceration changes, which was referred to above and which is produced especially by post-partum maceration, is shown particularly well in No. 993, a portion of which is represented in figure 259. The only possibility of confusion of these changes with other conditions is that one might take an instance like this for intrauterine lysis, but usually other criteria will enable one to differentiate the two conditions. However, when the two conditions are associated such differentiation may become impossible. How very complicated the branching of the villi has already become in these vesicles of the sixth week, of a measurement of about 48 by 41 by 15 mm., is shown by the bush-like villus represented in figure 260. The thick main stem of this villus stands out in marked contrast to some of the branches, many of which are exceedingly fine and others matted and fused. Fine, thread-like villi are common, especially in the area of the chorion laeve, as early as the sixth to seventh week. This is exemplified well by the specimens shown in figure 261. However, these fine villi, which usually have a fibrous, non-vascular stroma, occur also in long retention and elsewhere on the vesicle than in the area of the chorion laeve. They are present in the macerated but otherwise normal villous tree in figure 262, the branches of which bear decidual masses and trophoblastic nodules. Nothing could stand in more marked contrast to this and other normal villous trees than the excellent hydatiform villi in figure 263, which were taken from a vesicle 40 by 36 by 18 mm., of approximately the seventh week. This contrast is emphasized further by such normal specimens as the villi from No. 837, shown in figure 264, transition forms between which and the former are typified in the villi represented in figures 265 and 266, taken from vesicles 45 by 35 by 30 mm. and 80 by 60 by 50 mm., respectively, the former of which also shows maceration changes.

Other types of normal villi from vesicles of the eighth week are shown in figure 267. In these villi from a vesicle 54 by 50 by 43 mm., as in some older specimens to be referred to later, the most striking thing is the presence of many small knobs on all sides of the branches. This is illustrated splendidly by the villous tree shown in figure 268, which was taken from a placenta of the thirty-sixth week. There seems to be a great variation in the occurrence of this knobbing which probably does not signify beginning branching. The knobs are too numerous for this when they are at all well developed, and, since they are so uniform in size, one would have to think of a perfect shower of branches arising at the same time. Since the placentse in which knobbing of the villi was especially evident look absolutely normal, I have come to regard its presence as tj^pical for villi beyond a certain age, without, however, regarding those in which it is present only in a minor degree as necessarily pathologic. A villous tree in which sparse knobbing is evident only upon magnification is that shown in figure 269, in which rather miscellaneous branching is present. Other filiform villi, and a group of them from this placenta of the eighth to ninth week, are shown in figure 270.

What a contrast in external appearance villi from different placentse may show is illustrated in figures 271 to 278, villi of the eleventh, twelfth, fourteenth, fifteenth, thirteenth, nineteenth, twenty-fourth, and twenty-fifth week, respectively. Nor are these variations in the 'external appearance of the villi to be attributed to age alone or necessarily to pathologic changes. The villi shown in figures 271, 272, and 274 look hydropic because of maceration, and those in figure 272 are decidedly fibrous and largely non-vascular. The chorionic membrane of this vesicle was decidedly infiltrated. The villus shown in figure 277 is also macerated, and the chorion likewise was infected, but the stroma in this case was edematous and had disappeared completely in places. Not infrequently the blood-vessels can be seen as fine white lines on the exterior of these macerated specimens. The villi shown in figure 273 came from a vesicle which had also been retained a considerable period of time, and those shown in figure 275, though filiform and fibrous, with nodules at the extremities, are also macerated.

Villi of small caliber are encountered quite frequently in apparently normal older placentae, but are especially common in the capsular region, at a time when retrogression of the chorion laeve is taking place. The contrast in form of the villi shown here is remarkable. Those in figure 278 appear like the leafless branches of an oak hung with streamers of lichen. These strange appearances are due to the presence of many exceedingly fine branches and perhaps even of early villi, almost alfof which, nevertheless, are highly vascular. Those in figure 276 are practically unmacerated, for they came from a fresh, normal abortus, and in spite of their extreme delicacy and curliness, I know of no reason to regard them as pathologic. That shown in figure 277 came from a retained infected conceptus, but to extent its form can be attributed to these facts is difficult to decide. It scarcely seems to me that such a marked diversity in form could exist in strictly normal villi, and it is possible that local conditions may to a large extent influence, even if they do not determine, the type of a particular villus.

I regret that it has not been possible to compare villi from placentae of the same age, but from different pregnancies, in the same women, in order to determine the possible occurrence of variations in the type of villi in succeeding pregnancies. There seems to be no doubt that the diversity in form of villi increases rather than decreases with advancing age of the conceptus, and that the differentiation -extends even to the last months of pregnancy. At this time, however, the more prevailing type of normal villus appears to be such as that from the thirty-first week, shown in figure 279.

Normal villi apparently vary greatly, not only in length and caliber, but also in complexity and manner of branching, and in the appearance of their surfaces, which change from smooth to extremely knobbed. It is not uncommon to find that exclusion of the villi reduces the measurement of a chorionic vesicle from onethird to one-half. This is illustrated by the specimens in figures 231 (plate 19, Chap. XIII) and 253, both of which are relatively small vesicles. Nor are these long villi always slender and unbranched, for frequently, as illustrated in figure 281, in which a more branched, bushy villus from a vesicle 70 by 50 by 40 mm. is represented, they are decidedly umbelliferous. However, as is usually the case, the villi of this specimen were somewhat unequally developed.

Extreme grades of fibrosis, as represented in figure 283 (plate 24, Chap. XVI), with vessels in varying degrees of disappearance, have been found to occur in cases of long retention in lues and also under conditions of infection. These particular villi were taken from a vesicle measuring only 55 by 35 by 20 mm. Rather unusually formed, clubbed, decidedly macerated villi from an ovarian pregnancy are shown in figure 168 (plate 16, Chap. XI). Anomalous development of villi seems to be more common in tubal, and perhaps also in ovarian, than in uterine pregnancy. In tubal specimens the villi not infrequently are but sparsely developed and bare areas seem to be much more frequent. Moreover, the chorionic vesicles are often too small in proportion to the contained fetus. This is illustrated well by No. 1151, shown in figure 280. To what extent this disproportion is the result of reduction in the size of the vesicles after death of the fetus or to retardation in growth because of an abnormal location, or to both, I am unable to say. Some of the villi of this small vesicle also show hydatiform degeneration, while others merely are macerated, as shown in figure 282.

Careful examination of young chorionic vesicles has failed to reveal villi which are purely epithelial or ectodermic, nor have I seen any formed by the extension of mesoderm into the trophodermic trabeculse. As soon as an area of the syncytium and the Langhans layer becomes elevated at a given point, the mesoderm accompanies them if this elevation represents a beginning villus. No matter how marked the syncytial development, I have never noticed the presence of a normal structure in the distal portion of a villus and a purely syncytial structure in the basilar portion. No matter how long or how complicated the syncytial buds became, they never were invaded by mesenchyme or became vascularized. However, this fact does not preclude the inclusion of blood within syncytial skeins or trophoblastic nodules, or within invaginations of epithelium in the mesoderm of the villi. All these appearances not infrequently are seen in specimens in which there has been considerable growth of syncytium or of the Langhans layer, but I have never seen evagination of these two layers without a mesodermal core. No matter how long vascularization of a villus is delayed, and in some cases this seems never to occur, such villi otherwise have the same structure as the rest, just as trophoblastic development on the early villi seems to be universal and not visibly influenced in its first stages by the location of the embryonic disk or the shape of the early conceptus. These facts undoubtedly are not without significance for the nutrition of the early conceptus. The universal presence of villi establishes conditions much more favorable to circulation of the surrounding fluids, besides very materially increasing the area of absorption. Hence I do not believe that bare areas in the basal and capsular regions of a young conceptus can be regarded as normal.

Branching of the villi occurs exceedingly early and does not seem to develop any special plan or be limited to any particular plane. The angle generally is an acute one, probably because of the fact that the branches aim to reach the trophoderm or the decidua. It is not at all uncommon to find several branches arising at the same level, or they may leave the parent trunk in quick succession.

Although considerable variation in size and complexity of the villi seems to exist even in normal chorionic vesicles, these differences are not necessarily so pronounced in the same as in different specimens. However, one not infrequently meets with simple, unbranched villi among others of great complexity, but I did not get the impression that, except in the first few months, much interpolation of villi occurs later in development. It is quite surprising how large a placental area can be formed by a single villous tree, and placental differentiation occasionally seems to be present in chorionic vesicles with embryos of a length of only 17 mm., which implies an age of only about 7 weeks. Indeed, it does not seem improbable to me that close observation will show that some placental diffentiation exists as early as the sixth week.

Description of Plates


FIG. 242. Isolated villi from No. 1878, shown in figures 232 and 233, plate 19, Chapter XIII. X4.5.

FIGS. 243-244. Appearance of villi in section, same specimen. X7.5.

FIG. 245. Cross-section view of an entire normal vesicle with cyema and adnexa. No. 2053. X3.

FIG. 246. Section of villi from same. X36.

FIG. 247. External appearance of conceptus, showing filiform villi. No. 866. XI. 5.

Fig. 248. External appearance of conceptus, showing presence of hydatiform villi. No. 2108. X2.25.

FIG. 249. Sparsely villous area from No. 1892. Xl.5.

FIG. 250. Isolated villi from same specimen, showing maceration changes. X3.

FIG. 251. Isolated shadow or gossamer villi. No. 2197. X9.

FIG. 252. External appearance of same specimen. Xl.5.

FIG. 253. Cross section of No. 1287. Xl.5.

FIG. 254. Villi from No. 1466. X2.25.

FIG. 255. Hydatiform villi from No. 2233. X4.

FIG. 256. Section of chorionic vesicle with hydatiform villi in basal area. No. 2361. Xl.5.


FIG. 257. Isolated villi from No. 2361, showing both maceration and hydatiform degeneration. X6.75. .

FIG. 258. External appearance of abortus, same case. X0.75.

FIG. 259. Changes in external appearance of villi, due to maceration alone. No. 993. X3.

FIG. 260. Isolated villous tree from same vesicle. X3.

FIG. 261. Isolated filiform villi. No. 1639. X3.

FIG. 262. Isolated villous tree. No. 2336. X6.75.

FIG. 263. Fine hydatiform villi. No. 1797. X3.

Fig. 264. Normal villi. No. 837. X2.25.

FIG. 265. Transitional villi between normal and hydatid. No. 432. X2.25.

FIG. 266. Transitional hydatiform villi. No. 437. X2.25.

FIG. 267. Normal, knobbed or budded villi. No. 1063. X2.25.

FIG. 268. Villous tree from a normal specimen, illustrating many small knobs. No. 2335. X6.75.

FIG. 269. Villous tree showing few buds or knobs. No. 1840a. X2.25.

FIG. 270. Filiform villi and a portion of the vesicle from the same specimen. X3.

FIG. 271. Villi showing maceration changes. No. 2348. X6.75.


FIG. 272. Villi showing maceration changes. No. 2339. X6.75.

FIG. 273. Villous tree with smooth villi. No. 2253. X6.75.

FIG. 274. Villous tree with knobbed villi. No. 2372. X6.75.

FIG. 275. Filiform villus. No. 2326. X6.75.

FIG. 2V 6. Fine, frowsy villus. No. 2414. X6.75.

FIG. 277. Massive villous tree. No. 2283. X6.75.

FIG. 278. Knobbed, curly villi. No. 2384. X6.75.

FIG. 279. Mossy villi. No. 2249. X4.5.

FIG. 280. Tubal conceptus (No. 1151), showing disproportion between the chorionic vesicle and the fetus, sparse development of the villi, and some hydatiform degeneration. Xl.5. FIG. 281. Villous tree from No. 651ft. X2.25. FIG. 282. Villi from No. 1151, shown in figure 280. X3.


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Mall FP. and Meyer AW. Studies on abortuses: a survey of pathologic ova in the Carnegie Embryological Collection. (1921) Contrib. Embryol., Carnegie Inst. Wash. Publ. 275, 12: 1-364.

In this historic 1921 pathology paper, figures and plates of abnormal embryos are not suitable for young students.

1921 Carnegie Collection - Abnormal: Preface | 1 Collection origin | 2 Care and utilization | 3 Classification | 4 Pathologic analysis | 5 Size | 6 Sex incidence | 7 Localized anomalies | 8 Hydatiform uterine | 9 Hydatiform tubal | Chapter 10 Alleged superfetation | 11 Ovarian Pregnancy | 12 Lysis and resorption | 13 Postmortem intrauterine | 14 Hofbauer cells | 15 Villi | 16 Villous nodules | 17 Syphilitic changes | 18 Aspects | Bibliography | Figures | Contribution No.56 | Contributions Series | Embryology History

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