An intersex bovine animal
Keywords: intersex, hermaphrodite, pseudohermaphrodite
A bovine animal with ambiguous genitalia was a examined by a rDVM (Image acknowledgement & copyright Mr Max Winkler):
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Although raised as a heifer, the animal did not have a vulva but possessed a rudimentary scrotum and urinated from a vulva-like orifice between the cranial set of four teats.
The animal was sent to slaughter and its tracts sent to the AVC for investigation. Dissection showed the following:
Although raised as a heifer, the animal did not have a vulva but possessed a rudimentary scrotum and urinated from a vulva-like orifice between the cranial set of four teats.
The animal was sent to slaughter and its tracts sent to the AVC for investigation. Dissection showed the following:
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The ventral aspect of the reproductive tract of an intersex bovine (case pending histology data). Note that this is a high resolution image that can be examined in detail.
The ventral aspect of the reproductive tract of an intersex bovine (case pending histology data). Note that this is a high resolution image that can be examined in detail.
This tract was submitted for examination by an interested owner who submitted the animal for slaughter. The animal was ostensibly a fully grown beef heifer close to two years of age. It was seen to urinate from an orifice between the halves of its udder. However, there was no vulva, no scrotum, testes, vulva or vagina. The RDVM was unable to palpate a reproductive tract.
Dissection showed the presence of a long urethra (U) terminating (ExU) between the halves of the udder. There was no hypospadia. Two, well developed seminal vesicles (SeV, histology pending) were present just cranial to the anus and two equally well developed ampullae (Am) arose between the seminal vesicles, terminating cranially in blind ends in the meso-genital fold. The ampullae entered the colliculus seminus (CS) in conjunction with openings to the seminal vesicles, approximately where they would be located in a normal male. Attempts to locate a prostate gland (body or disseminate part) were fruitless but small indentation in the lumen of the urethra in the area of the colliculus seminus suggested an abortive attempt at gland formation in that area.
Ureters (Ur) entered the bladder in their normal position.
Cranial to the termination of the ampullae, the mesogenital fold continued and although a uterus (Ut) was present, no cervix or uterine body could be identified. The uterus contained a small volume of opaque fluid and the left and right halves of the uterus communicated with one another. The right gonad (G1) resembled an ovary containing a single large follicle/cyst (histology pending). The left gonad (G2) resembled a testis (histology pending) with dense, brown parenchyma.
A close-up view of the ovary-like and testes-like gonads:
A close-up view of the ovary-like and testes-like gonads:
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Close examination of the terminal part of the reproductive tract (below) ending between the halves of the udder, showed a vulva-like structure with the corpus cavernosum penis, ending in a clitoris-like structure. The vulva lips are the homolog of the prepuce in females.
Close examination of the terminal part of the reproductive tract (below) ending between the halves of the udder, showed a vulva-like structure with the corpus cavernosum penis, ending in a clitoris-like structure. The vulva lips are the homolog of the prepuce in females.
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As seen below, the penis in this animal contained a corpus cavernousus, and a urethra that was surrounded (at least partially) by corpus spongiosum urethra. Two small muscle groups present caudally on the penis were presumed to be the retractor penis muscles:
Interestingly, this animal also had a small scrotum (ringed below) just caudal to the four teats. Not surprisingly, apart from a fat pad, it was devoid of contents.
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Apart from the presence of the large cyst, the right gonad was very similar to the left gonad on histologic examination. The cyst was lined with a single layer of epithelium, not resembling granulosa cells (consistent with a follicle) at all. The nature and origin of the cyst remains unknown; possibly an undeveloped segment of the mesonephric (wolffian) system. Both gonads showed diffuse masses and cords of cells which resembled interstitial cells in testes (leydig cells). The wall of the cyst and these cells are shown in the main image below. Within these cords and masses of cells, were small islands of cells circumscribed by thin layers of fibrous tissue. These are shown in the inset. These structures resembled aborted formation of seminiferous tubules. There was no evidence of any zona pellucidae; convenient markers for the presence of primordial (primary) follicles.
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In summary, this animal had gonads that were more testis-like than ovary-like. Therefore it was assumed to be a male pseudohermaphrodite; a partially developed female with male-like gonads.
In rare cases, freemartinism may cause such severe masculinization of the female tract, that it is almost completely male, so there is remote possibility that this animal's phenotype could have been an extreme manifestation of freemartinism.
We were not able to perform karyotyping in this case because live cells are required for karyotyping. Neither unfortunately, were we able to perform FISH (floursencent in-situ hybridization) for the Y chromosome or male gene sequences such as the SRY gene. The latter was merely due to lack of financial resources. Immunohistochemical staining of the stromal cells in the gonads of this animal would probably have revealed the presence of androgens.
Notes: Male pseudohermaphrodites are far more common that true hermaphrodites. Male pseudohermaphrodites such as this animal, are essentially incompletely masculinized females. One should recall that the default gender for all embryos is female and in the absence of any gonads, a female reproductive tract will develop. In the presence of testes however, sertoli cells produce inhibin and anti-müllerian hormone, suppressing the female tract (the müllerian/paramesonephric system). Also, androgens from the testes stimulate the formation of the male system (penis, accessory glands etc). The result is a male animal. Any defect that interferes with this process will result in the development of an incompletely converted female-to-male i.e. a pseudohermaphrodite. Because these animals have testes, they are termed male pseudohermaphrodites, named for the type of gonads they possess. They do not possess gonadal tissue from both sexes therefore they are not true hermaphrodites.
Interestingly, the gonadal sex is not always determined by the karyotype in these animals i.e. almost any karyoype can be associated with almost any form of intersex. Also although male pseudohermaphrodites commonly have XX karyotypes with variable SR-y characteristics, any combination of these is possible. Therefore neither FISH nor karyotyping may have revealed what would have been "diagnostically convenient" i.e. An SrY male with an XY karyotype.
True hermaphroditism can be bilateral (an ovotestes on both sides), unilateral (one ovotestis and one gonad of either sex) or lateral (an ovary on one side and a testis on the other). Initially therefore (prior to histological examination) the tentative diagnosis on this case was lateral hermaphroditism. This turned out to be an incorrect assumption.
Apart from freemartins, which can be regarded are true hermaphrodites, other true hermaphrodites are rare (In some extremely rare cases, separate male and female gonads can be found on both side (two testes and two ovaries ~ 4 gonads); a hermaphrodite beluga whale with four such gonads has been reported. De Guise, D. 1994. True Hermaphroditism in a St. Lawrence Beluga Whale (Deiphinapterus leucas) J. Wildlife Diseases. 30:287-290
Finally, it has been shown that feminization of the male tract is possible in mice (Behringer, 1995) when the dam expresses a gene for high concentrations of anti-müllerian hormone. Such a syndrome would not be detected by the diagnostic tools that we would have used. However, the bovine placenta is less intimate that the murine placenta, so it is unlikely that a large peptide molecule such as AMH could cross the placenta and feminize the tract.
