Paper - Some observations on the development of the vagina in the pig (1934)
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Baxter JS. Some observations on the development of the vagina in the pig. (1934) J Anat. 68: 239-250.1. PMID 17104471
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Some Observations on the Development of the Vagina in the Pig
By James S. Baxter, M.Sc., M.B., F.R.C.S.I. T
he Department of Anatomy, Queen’s University, Belfast
A considerable amount of evidence has now been brought forward to show that developmentally the vagina is a compound organ, in at least several mammalian forms. Further, this evidence indicates that the mode of development of the vagina differs very considerably in different orders and even among the members of one order of Mammalia, and it appears certain that the descriptions which seek to establish a uniform developmental process, differing only in details, for the vagina in the mammals above the marsupials can now no longer be accepted.
In a recent paper(1) I have brought forward evidence to show that the variations in the developmental process are closely correlated in the rodents with the anatomical differences of the lower part of the female genito-urinary tract. A study of the development of the vagina in the rabbit showed that the upper portion was derived from the Miillerian ducts, while the lower and lesser portion arose from the fusion of two Wolffian bulbs with one another. In the rabbit the vagina communicates with the exterior through a fairly long urogenital sinus. In the rat (Mijsberg (2)) the same structures, Millerian ducts and Wolffian ducts, are concerned in the formation of the vagina, and, in addition, the urogenital sinus divides into two canals and the dorsal canal forms the lowest part of the vagina. In the rat the vagina opens directly to the exterior, the genital tract being thus more completely emancipated from the urinary tract than in the rabbit; and this emancipation is to be associated with the additional developmental process at the lower end.
The developmental processes of the rabbit and the rat suggest the nature of the compound formation of the vagina, but before a complete understanding of the morphology of the vagina becomes possible, descriptions of the developmental processes in other mammalian orders are required and their correlation with the varying anatomical forms must be established. The Ungulata have not yet been extensively studied. The descriptions of the development of the vagina in this order are not very complete and in several points they are contradictory. I have studied the developmental processes in the pig as part of the wider investigation of the development and morphology of the vagina in the Mammalia on which I am at present engaged. In this paper I present the description of the development of one form as a necessary preliminary to the consideration of the vagina in the Ungulata generally.
Felix and Buhler (8) give the same description for ungulates as they do for other mammals, namely, that in all the vagina is formed solely from the fused Miillerian ducts. Henneberg(4) has described the formation of the external genitals in the female pig, and he notes in his account that the urogenital sinus is split into two parts (dorsal and ventral) from above downwards by a frontal division. The anterior channel becomes the urethra, the posterior one aids in the building of the vagina. In a female foetal pig of 12 em. c.R. length WoodJones (5) has described the fusion of the lower ends of the Miillerian ducts with the Wolffian ducts and the entry of the latter ducts into the urogenital sinus. He has interpreted this as a stage in development where there exists a median Wolffian chamber into which the Millerian ducts will open later in foetal life. Tourneux (6) gives an account of the vaginal anlage in a foetal horse, and shows that in its lower part the Miillerian and Wolffian ducts blend to form a common canal. On the other hand, Retterer (7) found that the lower part of the vagina in the horse and the calf was split off from the upper part of the urogenital sinus by the formation of a frontal septum. Bergschicker (quoted by Mijsberg) studied the Millerian and Wolffian ducts in the cow and found that the Miillerian ducts fused with the urogenital sinus for some distance at their lower ends. The Wolffian ducts thus obtained a definitive opening into the lower part of the vagina.
The Mullerian ducts in the pig fuse with one another in the genital cord to form the utero-vaginal canal in the same manner as in other mammals. According to Tourneux and Legay (8) the fusion occurs when the foetus measures about 60 mm. from vertex to rump and commences towards the middle of the genital cord. My material does not show the place of first fusion of the Miillerian ducts, but it does indicate clearly that the lower ends of the Miillerian ducts remain separate until quite late in foetal life (see text-fig. 2).
Shortly after its formation (8-2 cm. stage) the vaginal anlage consists of an epithelial tube, oval in transverse section, which bifurcates at its lower end; and each limb of the tube comes into separate contact with the dorsal wall of the urogenital sinus. The wall of this tube and of the limbs consists of a single layer of columnar epithelial cells, but the extreme lower ends of the separated extremities are solid, each end being filled up with a mass of polyhedral cells. This solid portion of each duct corresponds with the part in contact with the urogenital sinus}.
The Wolffian ducts appear to open into the urogenital sinus cephalad to the level of contact of the Millerian ducts with the sinus. At first sight this relationship between the ducts seems distinctly unusual, but closer examination
1 The presence of a distinct basement membrane on the dorsal wall of the sinus, between it and the tips of the Miillerian ducts, would make it seem very unlikely that an upward proliferation of sinus epithelium into the lower ends of the ducts (“‘ conus vaginalis” of Spuler) had occurred. These cells are almost certainly Miillerian in origin and have been formed in situ by proliferation from the growing tip of the duct. , Development of the Vagina in the Pig 241
suggests, I think, the interpretation. Inspection of the dorsal wall of the urogenital sinus in a wax-plate reconstruction of this stage (text-fig. 1) indicates that the terminal part of the Wolffian duct has the form of an elongated funnel. (This is confirmed by the study of a graphically reconstructed paramedian section through the ducts and sinus (text-fig. 5 A).) There is an inwardly projecting ridge on each side on the inner wall of the sinus. When traced upwards this ridge is found to be continuous with the upper margin of the apparent opening of the Wolffian duct; followed downwards it runs upon the lateral wall of the sinus to the level of the termination of the Millerian duct, and there it turns fairly sharply medialwards and disappears. A transverse section of this part of the sinus (Plate I, fig. 1) shows that the two ridges are the anterior boundaries of dorso-lateral bays, each bay being perfectly continuous in an upward direction with the lumen of the corresponding Wolffian duct. The epithelium lining the sinus and the bays is stratified, the cells being polymorphous. It is lower in the bays (about three cells thick) than elsewhere on the sinus walls, where it averages five to six cells in thickness, but there are no definite cytological differences to be detected between the epithelia of the dorsal and ventral walls of the sinus.
Text-tig. 1. Drawing of a wax-plate reconstruction of the lower end of the genital cord of an 8-2 cm. female foetal pig. The reconstruction is viewed from in front and slightly from above. The left half of the anterior wall of the urogenital sinus has been removed: (1) fused Miillerian ducts; (2) Wolffian duct; (3) opening of left Wolffian duct into sinus recess; (4) overhanging edge of this opening continuous with fold on lateral wall of sinus; (5) point of contact of Miillerian duct with sinus.
Text-fig. 2. Drawing of a wax-plate reconstruction of the lower end of the genital cord in a female foetal pig of 12-4 cm. c.R. length. Only the epithelial structures are represented, and the reconstruction is viewed from in front and from the left side: (1) fused Miillerian ducts; (2) Wolffian duct; (3) Miillerian vaginal cord; (4) upgrowth of Wolffian epithelium on anterior aspect of left vaginal cord; (5) median canal; (6) urogenital sinus.
The tubular vaginal anlage now grows and enlarges both in length and breadth. Longitudinal ridges begin to be evident upon the inner surface of the hollow portion, especially towards the lower end (12-4 cm. stage). The lining epithelium of this part is still seen, in sections perpendicular to the free surface, to consist of a single layer of columnar cells. Traced downwards the vaginal anlage bifurcates, each separate part being formed by a solid cord of epithelial cells and representing the terminal non-fused part of a Millerian duct (Plate I, fig. 2). The corresponding Wolffian duct lies anterior, and somewhat lateral, to the Miillerian cord. As these structures are traced caudally Wolffian cells are found on the anterior aspect of each Miillerian cord (Plate I, fig. 3). These cells are in the form of a solid mass which, when traced caudally, becomes patent and soon establishes an open connection with the Wolffian duct proper, the duct itself being now definitely enlarged (see text-fig. 5 B for the relations of Wolffian and Miillerian epithelium at this stage). Ata lower level the Wolffian ducts fuse with one another in the middle line, the lumina however remaining separate for a short distance (Plate I, fig. 4). The Miillerian epithelium has almost disappeared at this level, being represented only by a few cells on the dorsal aspect of the left duct. A short distance further caudally the Millerian epithelium has completely disappeared and the Wolffian ducts form a single median canal. The wall of this canal consists of a stratified epithelium, the constituent cells of which are characterised by the clearness of the cytoplasm. The canal continues for some distance further caudally and then opens into the dorsal part of the urogenital sinus (Plate I, fig. 5). In the sections at this . level the cells of the Wolffian canal quite markedly differ from the cells of the sinus in the better staining of the cytoplasm of the sinus cells with Orange G.
In a foetus of 17-5 cm. c.R. length the solid Miillerian epithelial cords have commenced to fuse in the middle line and they have become relatively shorter. There is as yet no communication between the upper tubular (Miillerian) part of the vagina and the median (Wolffian) canal below (Plate I, fig. 6). The Wolffian ducts open into the Wolffian canal a short distance below the junction of the solid Miillerian cords with it. Above its solid ends the Miillerian vaginal anlage is lined with a single layer of columnar cells; and with the further-growth the longitudinal folds of the epithelium in its upper part have become more numerous.
At a slightly later stage (18-2 cm. c.R. length) the upper part of the vagina is still lined with a single layer of columnar epithelial cells. The Wolffian ducts lie anterior to this part of the vagina, one on each side of the middle line, and are clothed with a cubical epithelium. As the sections are followed caudally small isolated areas which show the first appearances of stratification of the epithelium are found in the vaginal mucosa. Further caudally these areas become larger and more numerous, and they are finally continuous, so that for some distance above the terminal solid epithelial cord the vagina possesses a. stratified epithelial lining, two or three cells thick. This part of the vagina terminates in a very short epithelial cord, evidently the result of fusion of the Development of the Vagina in the Pig 243
paired cords of earlier stages. The lower end of this Miillerian cord shows a sudden transition in cell type to the form which was previously recognised as Wolffian in the mass of cells which connected the Miillerian epithelial cords with the sinus at the 12-4.cm. stage. This Wolffian cord divides into two when traced further caudally, each part becomes progressively larger, acquires a lumen and finally re-unites with its fellow and with the corresponding Wolffian duct. The united structure passes on as the median Wolffian canal and terminates in the sinus.
Text-fig. 3. Photograph of the vagina and urogenital sinus of a 35 cm. sow laid open from the ventral aspect, x3. (1) Miillerian vagina; (2) “hymen”; (3) opening of Gartner’s duct; (4) opening of urethra into urogenital sinus.
A young sow (6 weeks old) measuring 35 cm. from vertex to rump afforded me an opportunity to study the vagina with particular reference to the presence or absence of ‘“‘hymeneal”’ structures. According to Weber(9) there is a circular constriction where the vagina joins the urogenital canal in many ungulates, and this constriction may be supplemented by transverse folds of the mucous membrane. On laying open the vagina and urogenital sinus of this specimen from the ventral aspect, the appearance figured in text-fig. 3 was found. There is clearly seen to be a circular fold of mucous membrane constricting the vagina and separating off an upper part from the remainder. This upper portion shows numerous delicate longitudinal ridges and furrows, and quite definitely corresponds with the upper tubular part of the vaginal anlage of early stages. A short distance below the circular fold there is seen on each side the opening of Gartner’s duct, and below this level is the opening of the urethra into the urogenital sinus. A few longitudinal ridges of mucous membrane run downwards from the openings of Gartner’s ducts, but this part of the vagina is relatively smooth walled. The “hymeneal” fold lies therefore between the Millerian vagina above and the median Wolffian canal below, and in this position it does not guard the opening of the vagina into the sinus. A vertical section through the “‘hymeneal”’ fold is shown in text-fig. 4. It has the form of a transverse shelf in the vagina, more apparent from the upper aspect. Both surfaces of this shelf are clothed with stratified squamous epithelium. The vaginal wall a short distance above the level of the fold is lined with a single layer of columnar cells. Probably this part of the vagina does not become stratified until the time of sexual maturity. ‘Wilson (10) describes it to be three or four cells thick in the -adult pig at the resting stage of the sexual cycle. The muscular coat of the upper part of the vagina consists mainly of bundles of smooth muscle circularly arranged. External to this layer are a few longitudinal bundles. At the level of the hymen a new layer of circularly disposed smooth muscle is found which replaces the other. It lies outside the circular stratum of the upper part of the vagina and is separated from it by a definite connective tissue septum. Both layers are, however, internal to the stratum vasculare. At the region of the opening of the urethra into the urogenital sinus, striated muscle fibres from the pelvic floor are found to blend with this second layer of smooth muscle.
Text-fig. 4. Vertical section through “hymeneal” fold in a 35 cm. pig, x 25. (1) Circular muscle of Miillerian vagina; (2) circular muscle surrounding Wolffian vagina and separated from the first layer by a connective tissue septum. Mallory triple connective tissue stain.
It has been shown in the foregoing description that, developmentally considered, there are three regions in the vagina of the pig: (1) an upper portion which is formed from the lower part of the tubular utero-vaginal canal; (2) below this, there is a region, quite short and narrow, derived from the solid tips of the Millerian ducts; and (8) next the sinus is a median canal into which open the Wolffian ducts (ducts of Gartner in the adult). I propose now to consider each of these parts and I shall designate them, for convenience, the upper, the middle, and the lower vaginal segments.
Upper segment. This part is formed from the fused Miillerian ducts in the lower portion of the genital cord. It has for long the form of a simple epithelial tube lined by a single layer of columnar cells. During development numerous vertical ridges are formed on its inner surface. The transformation of the columnar epithelial lining into a stratified one commences very late in foetal life and is first to be observed at the lower end. From this part it spreads slowly and irregularly upwards, and probably does not reach the cervix until the time of sexual maturity. It is noteworthy that this segment of the vagina never becomes solid during development; and in this, as also in the slow transformation undergone by its epithelium, it is in strong contrast with the upper part of the vagina in the human female. The retention of the primitive tubular condition in the upper region of the vagina seems to be the rule in lower mammals (it is found at least in several rodents, in some bats, and in the mole); but to what extent this segment of the vagina is represented in higher forms, if at all, can be determined only by the study of vaginal development in the primates.
Middle segment. The lower ends of the Miillerian ducts are separate from one another in the early stages of development, and union between them does not occur until the foetus has attained a considerable size (17-5 cm.). When first observed the separated parts are solid at their tips, being formed there of polyhedral epithelial cells. According to Nagel (11) this solid condition is to be expected, since these structures represent the growing parts of the Millerian ducts. At first these cell masses are in contact with the dorsal sinus recesses or bays which, as I have already mentioned, I believe to be the expanded funnel openings of the Wolffian ducts; later, the lower end of each duct is fused with a small diverticulum from the median (Wolffian) canal of the lower segment (12-4 cm. stage). This diverticulum is later drawn out on each side into an epithelial cord, the cells of which are different in appearance from those of the middle'segment proper. (These diverticula are further referred to below.) The lower separated rudiments of the middle segment remain short, become flattened antero-posteriorly and may be termed Miillerian vaginal cords (Plate I, fig. 6). Union of these cords in the middle line occurs about the 17:5 cm. stage, and subsequent canalisation gives rise to the constricted part of the vagina which is the “hymen.” My preparations do not show canalisation to have occurred at, or before, the 18-2 cm. stage. This does not agree with the observations of MacCallum (12), who studied the Wolffian body and ducts by the injection of colouring masses into the allantois. He noted that the Millerian ducts could be injected by this means in female foetuses of the pig measuring 120 mm. c.R. length or more. The pressure employed in this procedure might force a passage between the two parts of the vagina before the histological appearances of canalisation are to be appreciated. It seems certain to me, however, that no functional communication exists between the two parts up to the 18-2 cm. stage.
The situation of the “hymen,” marking out as it does the lower limit of the Miillerian element in the vagina and delimiting this from the Wolffian contribution below, is precisely what I have previously described for the “hymen” in the rabbit. Here, in the pig, the “hymen” is again seen to be placed at the boundary zone between the actively growing Mullerian segment above and the Wolffian duct segment below. The hymen in the human female (in which form it has been most closely studied) would seem to be formed between the urogenital sinus below and whatever structures form the vagina above. What these vaginal component parts are seems to me to be still undetermined in spite of the large amount of work upon the subject. It is therefore not yet possible to say if the hymeneal structures in these lower forms (pig and rabbit) have the same developmental relationships as in the human subject. These would be truly homologous only if the human vagina were a simple structure wholly derived from the Mullerian ducts.
Lower segment. This portion of the vagina develops rather later than the other parts. The rudiment of it can be recognised at the 8-2 em. stage, and it is well developed in a foetus of 12-4 cm. c.R. length, where it forms a median canal interposed between the Miillerian ducts and the urogenital sinus. The formation of this canal appears to me to have been the result of the union from above downwards of the two ridges found on the lateral wall of the sinus in the 8-2 cm. stage. The lower ununited ends of these folds are to be seen in Plate I, fig. 5.
Text-fig. 5 shows that there has been a “descent” of the Wolffian ducts relative to the Miillerian ducts during the formation of the lower segment, but the original contact area between the Millerian ducts and the dorsal (Wolffian) wall of the sinus remains the same. The Miillerian ducts consequently appear to fuse with two projections from the dorsal wall of the median canal, and further growth causes these projections to be drawn out into cords each continuous above with a Miillerian epithelial cord. When these cords fuse the fusion process is continued and involves the Wolffian cords of the lower segment as well.
Two structures may enter into the formation of the lower vaginal segment, namely, the Wolffian ducts and the urogenital sinus. My preparations would indicate that the Wolffian ducts form this part of the genital canal. Harris (13) has drawn attention to the fact that the dorsal wall of the urogenital sinus as far down as Miiller’s tubercle is mesodermic in origin, being derived from the Wolffian ducts in the series of changes which result in the formation of the base of the bladder. If this is so for the pig (and my specimens indicate it), the Miillerian ducts come in contact at their lower ends not with the urogenital sinus but with the Wolffian contribution to this structure. When the median canal is formed by union of the two sinus folds at least the dorsal wall of this canal is Wolffian, and the Wolffian element is certainly increased by the changing relationship of the Wolffian ducts to the Millerian ducts. The cords of the lower segment result from the drawing out of the Wolffian epithelium at the original contact point, and at the same time more and more of the lower end of the Wolffian ducts must be unrolled into the roof and anterior wall of the median canal. The histological difference between the epithelium of the median canal and the epithelium of the sinus in foetal life would also suggest that they are of different derivation. The apparently anomalous relationship of the Wolffian ducts to the lower ends of the Miillerian ducts requires further investigation, and I hope to make this the subject of a subsequent communication. At present it may be noted that all the growth processes involving the lower ends of the Wolffian ducts in the pig seem to be delayed. Examination and reconstruction of earlier stages in my possession show that the base of the bladder is late in formation, the ureters in a 35 mm. embryo still opening into the Wolffian ducts.
Text-fig. 5. Paramedian sections through the vaginal anlagen and related structures in A an 8-2 cm. foetus, and B a 12-4 cm. foetus. The drawings have been made from graphic reconstructions at the same magnification and represent. comparable parts in the two stages. For convenience the Wolffian duct is represented as lying entirely in the plane of section in B; actually its upper part is further lateral. (1) Wolffian duct; (2) fused Miillerian ducts; (3) uro genital sinus; (4) Wolffian epithelium with which tips of Millerian ducts lie in contact; (5) median canal formed by Wolffian ducts.
The conditions I have found at the 12-4 em. stage confirm Wood-Jones’ observations, namely, that at this time a canal is interposed between the lower ends of the Miillerian ducts and the urogenital sinus, and my specimens support his hypothesis that this canal is probably derived from the Wolffian ducts.
It may be thought that the formation of the lower vaginal segment by a frontal septum in the sinus is the process observed by Henneberg. It does not seem from Henneberg’s description, however, that he actually observed anything more than a descent of the point of union between the urethra and the vagina from the level of the upper border of the symphysis pubis to below the level of the lower border of that structure. Such a descent undoubtedly takes place, but the conditions I have found do not warrant the assumption that it is entirely due to septum formation in the urogenital sinus. On the contrary, the septum formed in the sinus is relatively small, and the real process that Henneberg observed is, I would suggest, a descent of the bladder and urethra towards the pelvis.
This investigation has not lent any support to the view of Felix and Bihler that the vagina in ungulates is derived wholly from the Miillerian ducts. The “hymen” limits the Millerian contribution, and this structure is found some distance from the opening of the vagina into the urogenital sinus.
- The development of the vagina has been investigated in the pig (Sus scrofa). Three distinct regions have been recognised which differ in their development. For convenience these have been called the upper, the middle, and the lower vaginal segments.
- By the fusion of the Millerian ducts in the genital cord there is formed a simple epithelial tube which is the utero-vaginal canal. The lower part of this tube is the anlage of the upper segment of the vagina. The wall of this tube becomes folded during development so that a number of vertical ridges are formed in this part. The epithelial lining commences to become stratified at the lower part of this segment late in foetal life, and this change spreads very gradually upwards. Even in a young sow, 35 em. in length, the major portion of the upper vaginal segment is lined with a single layer of columnar cells.
- The lower ends of the Miillerian ducts do not fuse with each other until the foetus is about 17-5 cm. in length. Each duct tip is in contact with the dorsal wall of the sinus, and each is solid through the proliferation of the constituent epithelium. In this way two short Millerian vaginal cords are formed. These fuse with each other in the middle line and the resulting structure becomes canalised shortly before or at birth. This part of the vagina remains narrow and forms a hymen in the vaginal canal. It has been termed the middle vaginal segment.
- The lower end of each Wolffian duct has a funnel-shaped opening into the urogenital sinus. The posterior wall of this funnel (with that of the opposite side) forms the dorsal wall of the urogenital sinus down to, and including, the area where the Miillerian ducts are in contact with the sinus. The funnel openings of the two Wolffian ducts are narrowed by the union of two sidewall sinus folds. The result is the formation of a median Wolffian canal interposed between the Miillerian ducts and the sinus. Disproportionate growth between the Miillerian ducts on the one hand and the Wolffian ducts and urogenital sinus on the other hand causes the tips of the Millerian ducts to draw out two Wolffian cords from the dorsal aspect of the median canal. These cords fuse with one another in the middle line just later than the Miillerian vaginal cords, and the resulting structure is canalised before or at birth. The median canal and the two cords derived from it form the lower vaginal segment into which open the persisting Wolffian ducts.
- It is pointed out that the upper vaginal segment of the pig and other lower mammals may not correspond at all with the upper part of the vagina in higher forms. The late persistence of a columnar epithelial lining to this part is also indicated.
- The hymen in this form is situated in the vagina. It marks off the Miillerian element in the vagina from the Wolffian element lying below, and thus has a similar situation to the hymen in the rabbit. Whether these hymeneal structures in lower mammals have the same developmental relationships as the hymen in the human female is uncertain in the light of recent work ' on the development of the human vagina. The hymen in the human would seem to differ in that it is developed between the sinus below and whatever structure or structures form the vagina above.
It is with pleasure that I acknowledge the kindness of Prof. Walmsley in providing facilities for, and supervising, this investigation. I have also to thank Miss M. E. Rea for text-figs. 1, 2 and 5.
(1) Baxter, J. 8. (1933). J. Anat. vol. Lxvul, p. 555.
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(11) Naaet, W. (1891). Arch. mikr. Anat. Bd. xxxvit.
(12) MacCatuum, J. B. (1902). Amer. J. Anat. vol. 1, p. 255.
(13) Harris, H. A. (1926). J. Anat. vol. Lx, p. 329. 250 James S. Baxter
Explanation of Plate I
Fig. 1. Transverse section of the lower part of the genital cord in an 8-2 cm. female pig foetus, x 86. (1) Dorso-lateral sinus bay; (2) fused Miillerian ducts.
Fig. 2. Transverse section of the lower part of the genital cord in a female foetus of 12-4 cm. c.R. length, x86. (1) Wolffian duct; (2) Wolffian epithelium on anterior aspect of the right Miillerian vaginal cord; (3) Miillerian vaginal cord.
Fig. 3. A section 75 microns caudal to the preceding one at the same magnification. Lettering as in fig. 2.
Fig. 4. A section 75 microns further caudal in the same foetus showing the union of the Wolffian ducts to form the upper part of the median canal. A few Miillerian cells are to be seen on the dorsal aspect of the fused ducts.
Fig. 5. Transverse section of the genital cord in the same foetus showing the opening of the fused Wolffian ducts into the urogenital sinus. (1) Urogenital sinus; (2) fused Wolffian ducts.
Fig. 6. Coronal section of the lower part of the genital cord in a female foetal pig of 17-5 em. c.R. length, x 25. (1) Miillerian vagina; (2) Miillerian vaginal cord; (3) median canal formed by fusion of Wolffian ducts; (4) Wolffian duct. Owing to spiral twisting of the vagina around the urethra this section does not appear as if truly coronal.
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