Paper - Notes on irregularities of ovogenesis and abnormal development of the embryo in cavia (1933)

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Nicol T. Notes on irregularities of ovogenesis and abnormal development of the embryo in cavia. (1933) J Anat. 68: 75-84.5. PMID 17104465

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This historic 1933 paper by Nicol describes abnormal guinea pig development.


Modern Notes: guinea pig | ovary

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Notes on Irregularities of Ovogenesis and Abnormal Development of the Embryo in Cavia

By Thomas Nicol, M.B., Cu.B., F.R.C.S.E.

Senior Lecturer in Anatomy, University of Glasgow

Introduction

The purpose of this paper is to put upon record instances of irregularities in ovogenesis and of deviations from the normal in the early stages in the development of the embryo of Cavia. These specimens were obtained during a series of investigations on the development of Cavia with particular reference to the appearances in the ovaries and the changes undergone by the uterusin pregnant and non-pregnant animals.


A. Pluriovular Follicles

The widespread distribution of the pluriovular follicle in Mammalia is well known, but, as Mainland (1928) points out, the frequency with which ovaries containing pluriovular follicles are met in a series of ovaries has been worked out in some animals only, such as cat, dog, Dasyurus viverrinus, Texas armadillo, opossum, pig, mouse and by himself in the ferret!. In the mouse, Engle (1927) records polyovular follicles in twelve ovaries in a series of one hundred taken from sixty-four animals,


In the course of a study of serial sections of both ovaries of fifty-two guinea-pigs, with special reference to the corpus luteum and ovogenesis, pluriovular follicles were observed by me in only three animals. This fact seemed worthy of record as giving some indication of the comparative rarity of the condition in Cavia, and from the circumstance that one of these animals was pregnant and its history known.


The pregnant animal previously littered two. It was then placed with the male and killed 19 days afterwards. One normal embryo was found in each uterine horn. Both ovaries cut serially showed pluriovular follicles. In ovary A ten pluriovular follicles were observed of which one was relatively large, three medium-sized and six small, and all were at the surface of the ovary?. One of the small follicles contained three ova, but all the others only two. These follicles were so orientated in the ovary that in nine of them one ovum was placed peripherally and the other at the central pole of the follicle. In some, one ovum was the smaller and usually that nearer the surface. In the smaller follicles there was no follicular cavity, and the ova lay surrounded by granulosa cells, though in the medium-sized follicles, and single large follicle, a follicular cavity with liquor folliculi was present. Some of the smaller ova appeared normal, and in the medium-sized follicles one ovum usually showed degenerative changes. The large follicle was atretic with the two ova lying free in its cavity and surrounded by a few follicular cells.


1 Reference may be made to Mainland’s paper (1928) for the literature on this subject. 2 Normal mature follicles according to Evans and Swezy (1931) vary in size between 900 and 1260 microns. The relatively large follicles of the above description measure from 650 to 750 microns in diameter, the medium-sized from 450 to 550 microns, and the small from 170 to 250 microns.


Six pluriovular follicles were observed in ovary B of the pregnant animal, and all at the surface of the ovary. One of these was relatively large, measuring 678 microns in diameter, and contained two ova each ina separate cumulus and widely separated by a large follicular cavity containing liquor folliculi. The ovum nearest the surface was smaller, showed evidence of degenerative changes and was covered with a single layer of granulosa cells. The larger ovum was apparently healthy and situated at the central pole of the follicle, being covered by several rows of granulosa cells. Deep to the larger ovum in the most central part of this large follicle was a second smaller cavity containing liquor folliculi. The entire follicle was surrounded by a well-marked tunica externa and interna. The other five pluriovular follicles in ovary B were small; four of these were biovular, but the fifth had four ova of which two showed degeneration. Some showed a small follicular cavity, others did not, and the ova in the smallest follicles appeared healthy. From the history of this animal the presence of pluriovular follicles would seem to bear no relation to fertility. In this connection it may be noted that Hartman (1926) recorded the presence of numerous pluriovular follicles in two pregnant macaques, and neither had twin embryos.

In one non-pregnant animal two largish biovular follicles and several smaller ones were found in each ovary, and the former as well as some of the latter showed degenerative changes. The ovaries of the other non-pregnant animal showed much the same appearances.

Loeb (1901) occasionally found follicles with two ova in the guinea-pig, and in some of these the ova were unequal in size. Disparity in size of the ova in a pluriovular follicle is apparently fairly common in other animals. Hartman (1926) states that the explanation probably lies in the differential growth potentialities of the eggs and different thresholds of response to growth stimuli, and points out that since normally many primordial ova remain quiescent, whereas others enter the growth period, it is to be expected that if a number of ova are fortuitously united into a single follicle, they will nevertheless exhibit their individual properties and either grow or remain retarded, as the case may be. On the other hand, Loeb (1917) has described pluriovular follicles of the guinea-pig in which primordial follicles “push their way into larger follicles, perhaps into such follicles which are already in the process of degeneration,” and in favour of this interpretation he mentioned that in the majority of cases the more undeveloped egg is situated toward the outer pole of the follicle. Mainland (1928) states that degeneration seems to be the usual fate of these follicles, and in this connection it may be noted that most of those recorded here showed some evidence of degeneration.


Various theories have also been suggested to explain the occurrence of such follicles. There does not appear to be much evidence to support their origin from polynuclear ova, and no example of the latter was encountered by me. Loeb (1917) found numerous pluriovular follicles in what he calls the “ hypotypical” ovaries of a guinea-pig which had been used in “under-feeding”’ experiments, and had its thyroid removed and the lobe of another thyroid engrafted subcutaneously. He claims that in this animal there was manifested a relative decrease in the amount of the connective tissue surrounding the follicles, and suggests that pluriovular follicles may be formed by a concrescence of previously separate follicles.

A lack of balance in development between the follicular tissue and the connective tissue, at the stage in the embryonic ovary when the small follicles normally become separated from each other, is the explanation favoured by O’Donoghue, Hartman, Mainland and others. In support of this I have observed several examples in which the connective tissue formed a definite layer around two small ova, yet there was at this stage little if any attempt to penetrate between them. What would normally have resulted in these instances cannot be foretold, but it seems reasonable that if the connective tissue failed to separate the ova that a biovular follicle would result. Evans and Swezy (1931) maintain that in the Mammalia all the ova of adult life are new formations, and state that the common method of formation of new ova in the guinea-pig is for a group of cells to be pushed inward from the germinal epithelium, usually as a solid cord which soon becomes cut off from the epithelium and comes to lie along the inner border of the tunica albuginea. One or more cells in each group then become enlarged to form the ova, and the remaining cells form the follicle cells; occasionally most of the cells in a group change into ova forming polyovular follicles, but these soon disappear, as large follicles containing more than one ovum are relatively rare in the guinea-pig.

The occurrence of pluriovular follicles in Cavia is apparently uncommon. It may be, however, that the condition is not quite as rare as would appear from the present series of ovaries, since the examination of the latter was carried out chiefly with reference to the corpus luteum and the appearances of medium-sized and large follicles, and perhaps occasional small pluriovular follicles may have been overlooked.

B. Abnormal Early Development of the Embryo

There are few records of abnormalities in the early stages of Rodents, and so far as I am aware, none such as are here described have been recorded in Cavia. Abnormal ova in different groups of Mammals have been recorded by various writers, including Huber (1915) in the rat, Hill (1910) in Dasyurus, Hartman (1919) in the opossum, Corner (1921) in the pig, Robinson (1921) in the ferret, Sobotta (1924) in the mouse, and Hammond (1914) in the sow and rabbit. Meyer (1917) has recorded several examples of degenerate guinea-pig embryos in pregnant animals from 19 to 87 days after coitus, and Squier (19382), dealing with the living guinea-pig egg and its early development, has described pathological morulae, four-celled stages, and blastocysts. My specimens are described not so much in the interest of comparative or experimental teratology, but as giving some interesting sidelights on the peculiar and specialised early stages seen in Cavia.

Abnormal or retarded segmentation

The first preparation (Plate I, fig. 1) shows the appearance of an abnormal segmented ovum. The specimen was found at the midpoint of uterine horn A of Cavia No. 64 at the anti-mesometric side of the lumen. Another abnormal segmented ovum was found in horn B of the same animal and almost identically placed. The ovum (Plate I, fig. 1) appears to consist of eight cells, maximum possible age 138 hours, and measures, including zona, 0-07 x 0-039 x 0-07 mm. The zona has partially degenerated and the normal development of the ovum seems to have been arrested. The nuclei are still apparently healthy and the cell protoplasm finely and fairly evenly granular. Plate I, fig. 2, represents a normal eight-cell stage. The ovum, including zona, measures 0-066 x 0-043 x 0-08 mm., maximum possible age 72 hours, and is still in the tube. The welldeveloped zona and the appearance of the cytoplasm in the normal specimen, due to the distribution of the lipoid globules represented in the figure by rounded spaces, distinguish it from the abnormal ovum (Plate I, fig. 1).


It will be noted that the normal eight-cell stage and this abnormal eight-cell stage compare closely in measurement, and that while the former is still in the oviduct the latter is half-way along the uterine horn. A normal sixteen-cell stage, maximum possible age 106 hours, and measuring about 0-119 mm. in diameter, is still in the tube near the tubo-uterine junction. Such abnormal ova may occur with normal ova in the same uterus. The possibility is, however, always to be guarded against that such structures may not be of ovarian origin, but belong to the category of “false embryos,”’ i.e. decidual remains. The uterine epithelium and the endometrium in both horns of Cavia No. 64 appeared healthy.


Young abnormal segmenting eggs such as the one figured, or the fragments of them, and ova which have either not been fertilised or have failed to develop, were not of infrequent occurrence, but a numerical record of them has not been kept. Such abnormal ova have also been found in the rat (Huber, 1915) and in the mouse (Sobotta, 1924).

Abnormal blastocyst formation

The example of this type shown (Plate I, fig. 3) is one of two “‘ blastocysts,” both abnormal, which were observed at the tubo-uterine junction of horn B of Cavia No. 33. No ova were found in the other tube or horn. Each presents very similar appearances, measuring 0-06 x 0-038 x 0-06 mm. including zona, and maximum possible age is 4 days. Plate I, fig. 3, represents a median section through one of these abnormal ova and shows a well-marked zona enclosing a degenerated cellular mass, the nuclei of the cells having practically all disappeared. Plate I, fig. 4, shows for comparison a normal blastocyst of maximum possible age 5 days, measuring, including zona, 0-072 x 0-045 x 0-05 mm., and nestling against the wall of a pocket on the anti-mesometric side of the uterine horn. This blastocyst is cut in approximately the same plane as the abnormal one. In contrast to the abnormal example which is about the same size as this normal blastocyst, the cells of the latter are fewer and the nuclei large and prominent. Abnormal ova such as is shown (Plate I, fig. 3) have frequently been found by workers in this Department, some along with normal blastocysts in the same uterus, and in all examples it was noted that the tubes and uterine horns appeared healthy and normal. Huber (1915) has described abnormal segmentation cavity formation in ova obtained from the uterus of the rat, and Corner (1921) has recorded degenerate blastocysts in the pig.

Suppression of the trophoblast

The third specimen to which attention is drawn was obtained from the uterus of Cavia No. 77. In horn A was found a normal embryo (text-fig. 1), of maximum possible age 18 days, and at the stage when the amnion cavity is well developed and its roof double-layered, the mesoderm having appeared in a normal manner. In horn B the rudiment shown in Plate II, fig. 6, was encountered and is probably about the same age. It was found ina swelling almost similar in size to that which contained the normal embryo in the other uterine horn, and occupied a very small decidual cavity (Plate I, fig. 5) confined to the extreme mesometric side of the uterus. The structure is very small, measures 0-1 x 0-1 x 0-1 mm., and consists (Plate II, fig. 6) of a small cavity with a thin single-layered roof and elsewhere a double-layered wall; the latter is better appreciated in the stained sections of the actual specimen as owing to a slight obliquity only some of the nuclei are showing in both rows in the same section. The thin roof in the fixed specimen is directed towards the mesometric side of the uterus, and thoughit must be admitted that the rudiment may have rotated in the process of preparation this seems unlikely. The interpretation of the specimen is difficult and must be only conjectural, yet the appearances are perhaps sufficiently interesting to warrant some suggestion as to what they might represent. I regard the cavity as that of the amnion roofed mesometrically by thin amniotic ectoderm and lined elsewhere by embryonic ectoderm, the outer layer of cells adhering to the latter being probably formative endoderm, the remainder of the embryo having been suppressed or failed to develop. There is no evidence of traiger or mesoderm or any embryonic fragments. It will be noted that the specimen occupies a very small decidual cavity at the extreme mesometric side of the uterine lumen, and the view might be advanced that it had become embedded here instead of as normally at the anti-mesometric side of the lumen, and that this faulty implanation may in some measure have contributed to its failure to develop normally. In this connection it may be noted that “implantations”’ on the mesometric side of the uterine lumen in the guinea-pig, as illustrated by Emrys-Roberts (1910), appear to belong to the class of “false embryos” described by Maclaren (1926). The endometrium of the uterus was healthy and normal. In the pig Corner has recorded a very interesting abnormality consisting of total absence of an embryonic area.


Text-fig. 1. Diagrammatic drawing of normal embryo No. 77 of maximum possible age 13 days. x circa 18. A. amnion, showing ectodermic and mesodermic layers; A.C. amniotic cavity; #.C. extraembryonic coelom; Hct. ectoderm; E.M. endoderm plus mesoderm; 7. trager.


Abnormal uterine swellings and arrest of development of the embryo

It is well known that in the mouse, rat, ferret and other Mammals, there are fairly commonly found uterine swellings which, when sectioned, contain only fragments of an embryo. These swellings may be almost as large as those containing a normal embryo of the same age, but are usually somewhat smaller. Such abnormal swellings are also encountered in Cavia, though compared with the number of uteri examined in this Department they appear relatively uncommon. In some cases the swelling is practically uniformly solid and only by most careful serial examination can embryonic fragments be discovered; in other cases the decidual cavity or parts of it can be recognised.


Sometimes the swelling contains an embryo arrested in its development. This does not appear to be common. The uterus of Cavia No. 18 contained four embryos of maximum possible age 14 days, all in the same uterine horn. The embryonic swellings were about equal in size. Two of the embryos were normal, the other two showed what appeared to be arrested development, and all four were sectioned in approximately the same axis. The normal embryos are at the stage of development of that shown in text-fig. 1, and each measures by sections 0-96 mm. Plate II, fig. 7, illustrates the first of these abnormal embryos. It measures 0-55 x 0-23 x 0-4 mm., and is therefore much smaller than the normal of this age. The specimen shows an abnormal trager, continuous with which is a degenerating amnio-embryonal cell mass covered by degenerating endoderm. The proexocoelomic cavity is absent and the apparent central opening is proved by serial examination to be a crack. The specimen is attached by its trager end to the extreme mesometric side of the uterus and occupies 4 fairly extensive decidual cavity. This seems to have been a normal implantation at the anti-mesometric side of the lumen, but development of the embryo has been early arrested and the specimen has reached its present position by differential growth. The endometrium appeared to be normal and healthy.


The second abnormal embryo found in the uterus of Cavia No. 18 measures by sections 0-79 mm. and the formative end 0-28 x 0-195 x 0-24 mm. It is therefore much smaller than the normal embryo found in this uterus though its decidual cavity is as large, and implantation seems to have been normal. Embryos from the same female may differ slightly in their stage of development but not so markedly as in this case (cf. text-fig. 1 of normal embryo). Plate II, fig. 8, is a somewhat diagrammatic drawing of a median section of the formative end of this abnormal embryo. There is considerable development of mesoderm, but the amnio-embryonal ectodermal cells show appearances which seem to deviate from the normal. The amnion cavity has appeared, but the cells surrounding it are very numerous and appear to be breaking up into numerous smaller cells showing evidence of degeneration. The specimen would not permit of a photograph good enough for reproduction, but the drawing (Plate II, fig. 8) gives some impression of the great number of amnio-embryonal ectodermic cells. The decidua seems healthy and the triger normal, though smaller than that of the normal embryo found in this uterus (text-fig. 1). The abnormal appearances of this formative end are better appreciated when compared with the formative end of a normal embryo which has reached approximately the same stage of development (Plate ITI, fig. 9), and is of maximum possible age 15 days. The developing amnion cavity in this normal embryo is seen as a slit in the median line of the formative knob with the cells of the formative ectoderm arranged more or less radially to the axis of the slit. No such arrangement can be seen in the abnormal specimen (Plate II, fig. 8), and moreover in the latter case neither the cells nor their nuclei are so large and healthy as in the normal specimen. The general appearance of the specimen suggests that the amnio-embryonal ectoderm was in incipient disintegration some time before the specimen was fixed, i.e. normal development had been arrested.


It may be of interest to note that Huber (1915) has recorded two examples of rat egg-cylinders in which the only abnormality observed is in the region of the ectodermal node. These cases he interprets as showing a retardation of the development of the ectodermal node and differentiation of the primary embryonic ectoderm.

Two embryos in a single decidual cavity

This interesting specimen (Plate ITI, fig. 10) must represent an exceedingly rare condition. It shows two embryos of maximum possible age 14 days enclosed within a single decidual cavity. The upper embryo is the smaller, its mesoderm has not yet appeared, and it represents a younger stage of development than the lower older and larger embryo which shows considerable development of mesoderm. Serial examination proves each embryo to be complete, there being no connection between the trager ends which are normally directed towards the mesometrial side of the uterus. The condition described above bears a close resemblance to the very rare case of two egg-cylinders in one decidual crypt described by Huber in the rat. In Huber’s fig. 10, p. 187, the two egg-cylinders have in part a common ectoplacental cone, but he states that the ectoplacental cones are for a short distance distinct before partial fusion occurs, showing that each egg-cylinder developed from a separate ovum. As in the present case the upper egg-cylinder represents a younger stage of development in which no mesoderm is present, while the lower and larger one is at a later stage and shows considerable mesodermic development. Huber believed that both ova were seminated at about the same time, became lodged in close proximity in the same uterine mucosal fold, and with further development of the decidual crypts both became enclosed within the same crypt at perhaps slightly different levels. In further development one blastodermic vesicle developing more rapidly dominated the other. The appearances he believes are not to be explained on the supposition of superfecundation or superfoetation. He also gives evidence to support the view that when two morula masses are lodged in close proximity in the same mucosal fold one or the other degenerates, and that the normal development of both is of very rare occurrence. In the oviducts in Cavia several examples have been observed where two apparently normal segmenting ova are adherent to one another, and it may be suggested that this case of twin embryos resulted from two such ova which had remained adherent and become implanted together, one later growing more rapidly at the expense of the other.


These examples of abnormal early development in Cavia may be grouped into Huber’s two main classes, first, those in which all the ova of a given animal show abnormal development, and second, those in which an abnormal ovum is found in the same uterus along with an average number of normally developed ova, As I have already said I do not propose to discuss these cases from the point of view of comparative or experimental teratology. Nor shall I deal with the theories respecting the underlying cause of the departures from normality which have been classified and discussed by Corner (1928), but it may be noted that in each case the maternal structures were examined with care and seemed to be anatomically and functionally normal. I am unable to report on the ovaries since they were unfortunately not preserved.


It seems, however, that in this series the abnormalities were not due to local maternal conditions, but represent some embryonic imperfection. Stockard, from experimental results, maintains that changes in the condition of moisture, temperature and oxygen supply are the most frequent causes of embryonic death as well as monstrous development, but careful consideration of this in relation to the animal stock in this Department lends no support to the view that such conditions have been active in the production of such abnormalities as are described. Professor Robinson in his Struthers Lecture showed that a considerable amount of prenatal death is normal in Mammals. From the tables given by Stockard and Papanicolaou (1918), in the record of their experiments on the modification of the germ cells in Mammals, Robinson states that in guinea-pigs it appears that the prenatal death-rate of normal non-inbred lines is 13-30 per cent., but he regards this as rather low for Cavia. The ultimate fate of these abnormal embryos is merely a matter of conjecture. Meyer, describing degenerate guinea-pig embryos belonging to later phases than are dealt with in this paper, states that intra-uterine absorption is not a rare occurrence.


References

Corner GW. (1921). ‘Abnormalities of the mammalian embryo occurring before implantation.” Carnegie Inst. Wash. Pub. No. 276, p. 61.

Corner GW. Physiology of the corpus luteum. I. The effect of very early ablation of the corpus luteum upon embryos and uterus. (1928) Am. J. Physiol. 86: 74.

Corner GW. (1928). “The problem of embryonic pathology in Mammals, with observations upon intrauterine mortality in the pig.” Amer. J. Anat. vol. xxxI, p. 523.

Emrys-Roserts, E. (1910). “The embedding of the embryo guinea-pig in the uterine wall and its nutrition at that stage of development.” J. Anaé. vol. xLIv, p. 192.

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—— (1926). “Polynuclear ova and polyovular follicles in the opossum and other Mammals, with special reference to the problem of fecundity.” Amer. J. Anat. vol. xxXvH, p. 1.

Hu, J. P. (1910). “The early development of the Marsupialia, with special reference to the native cat (Dasyurus viverrinus).” Quart. J. Micr. Sct. vol. tvt, N.S. p. 1.

Huser, G. Carn (1915). “The development of the albino rat, Mus Norvegicus Albinus. II. Abnormal ova, end of the first to the end of the ninth day.” J. Morph. vol. xxvi, p. 359.

Lozs, L. (1901). “On progressive changes in the ova in mammalian ovaries.” J. Med. Research, vol. vi, p. 39.

—— (1917). “The concrescence of follicles in the hypotypical ovary.” Biol. Bull. vol. xxxiu1, p. 187.

Macrazen, N. H. W. (1926). “The early development of Cavia: note on associated remains of previous placentation.” Proc. Roy. Soc. B, vol. xcrx, p. 230.

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Marntanp, D. (1928). “The pluriovular follicle, with reference to its occurrence in the ferret.” J. Anat. vol. uxt, p. 139. .

Meyer, A. W. (1917). “Intra-uterine absorption of ova.” Anat. Rec. vol. XII, p. 293.

Nicot, T. (1932). “The uterus of Cavia after intravitam staining with trypan blue: Preliminary note.” J. Anat. vol. LxvI, pt. II, p. 181.

(1933). ‘‘Studies on the reproductive system in the guinea-pig: Variations in the cestrous cycle in the virgin animal, after parturition, and during pregnancy.” Proc. Roy. Soc. Edin. vol. tim, pt. IIT (No. 16), p. 220.

—— (1933). “Studies on the reproductive system in the guivea-pig: II. Post partum repair of the uterus, and the associated appearances in the ovaries.” Trans. Roy. Soc. Edin. (in press).

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Plates

EXPLANATION OF PLATES

Plate I

Fig. 1. Section of abnormal segmented egg or egg that has failed to develop (64 A)? lying in the uterus. Fixed Zenker. Stained iron-haematoxylin. Photomicrograph. x circa 500. Compare fig. 2.

Fig. 2. Section of normal eight-cell stage (34 A) in the oviduct. Fixed Zenker. Stained ironhaematoxylin. Photomicrograph. x circa 500.

Fig. 3. Section of abnormal blastocyst (33 B). Fixed Zenker. Stained haemalum and eosin. Photomicrograph. x circa 660. Compare fig. 4.

Fig. 4. Section of normal blastocyst (24 A) lying in the uterus. x circa 570. From Maclaren (1926).

Plate II

Fig. 5. Section of embryonic rudiment (77 B) in small decidual cavity. Fixed Zenker. Stained iron-haematoxylin. Photomicrograph. x circa 120.

Fig. 6. Same as fig. 5. x circa 425.

Fig. 7. Section of embryonic rudiment (18 B). Fixed Zenker. Stained haemalum and eosin. Photomicrograph. x circa 108.

Fig. 8. Diagrammatical drawing of formative knob of embryo (18 C), of maximum possible age 14 days, arrested in its development. x circa 150. Am. amniotic cavity, HZ. ectoderm, H.C. extraembryonic coelom, Hn. endoderm, M. Mesoderm. The stippling of the ectoderm of the knob gives a good impression of the breaking down of the cells into numerous nucleated masses. Compare fig. 9.

Plate III

Fig. 9. Drawing of section of formative knob of a normal embryo (16 C) of maximum age 15 days. x circa 219. Explanations as in fig. 8. (From an unpublished figure—Maclaren.)

Fig. 10. Section showing two embryos (82 A) in a single decidual crypt. Maximum possible age 14 days. Fixation formalin and corrosive sublimate. Stained iron-haematoxylin. Photomicrograph, x circa 30.


1 Catalogue number of parent animal.


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