Book - Contributions to Embryology Carnegie Institution No.54
A Case of True Lateral Hermaphroditism in a Pig with Functional Ovary
By George W. Corner,
Of the Anatomical Laboratory, Johns Hopkins Medical School.
With one plate.
That variety of true hermaphroditism which is characterized by the presence of an ovary on one side and a testis on the opposite side is one of the rarest forms of structural abnormality of the genitalia. No undoubted cases have yet been reported in man, and but two instances have been observed in swine. Some idea of the rarity of the condition may be gained from the results of a systematic examination of 500,000 swine made in the Berlin municipal abattoir, under the direction of Ludwig Pick (1914). In this series of animals five cases of hermaphroditism were observed, but none of them was of the lateral variety, a mixed gland (ovotestis) on one or both sides being present in each.
Reuter (1885) described the case of a two months' old pig, discovered among a litter which also contained two pseudohermaphrodites. This animal possessed a right testis and a left ovary. The ovary was very small but contained ova in primordial follicles; the testis contained numerous interstitial cells, but apparently there were no germ-cells in the tubules. On the side on which the testis was located the uterus ended in a rudimentary Fallopian tube.
Kingsbury (1909) recorded the examination of a young adult pig with male external genitalia. There was a normal-looking uterus with a rudimentary left ovary and a large right testis with a typical epididymis. On the right side the Fallopian tube ended in a diminutive blind sac. The ovary contained a few ova in follicles; the testis had the typical structure of a crytorchid testis, with numerous interstitial cells but without germ-cells in the tubules.
Description of Specimen
The author's specimen, consisting of the uterus, tubes, and ovaries of an adult pig, was found among a number of uteri which had been brought in from a neighboring slaughter-house for study; therefore no information is at hand concerning the history or appearance of the animal from which it came.
The uterus was normally formed (fig. 1), presenting two cornua as usual. Its size corresponded to that of the uterus of a young, sexually mature sow. On the right side the uterine cornu ended in a normal Fallopian tube in connection with a normal ovary; the latter contained four recent corpora lutea, one of them cystically dilated. On washing out the contents of the tube with saline solution, one ovum was found, normal in all respects except that the cytoplasm was slightly shrunken; one polar body had been extruded. The left uterine horn, normal in size and form, ended in a very slender tube about 1 mm. in external diameter near the uterus, which gradually thinned down to an almost linear dimension, losing its lumen, and finally ending in the connective tissue over the epididymis (fig. 1).
On the left side, in place of an ovary there was a mass 30 by 25 by 20 mm. in diameter, of dull flesh-color, exactly resembling a testis in form, texture, and color. It was covered by a thick capsule in which large and somewhat tortuous vessels coursed; when this tunic was incised the contents bulged over the cut edges. The exposed surface was dry and granular in appearance.
On this side of the uterus there was a well-defined Wolffian duct, such as is occasionally present in sows, beginning in the vagina and running parallel to the uterine horn between the layers of the broad ligament. However, instead of ending in a cul-de-sac or in a series of minute cysts in the region of the ovarian pedicle, as this duct usually does when present in the sow, it became greatly convoluted as it approached the tip of the cornu and finally so closely coiled as to form the body indicated in figure 1. This structure presented the appearance of an epididymis by reason of its texture, its close apposition to the testis-like body, and also because of a slight constriction at the middle portion, suggesting a division into globus major and minor.
Microscopic examination fully confirmed the foregoing interpretation and proved that the specimen was indeed one of true lateral hermaphroditism. Sections of the testis (figs. 2 and 3) showed a typical tunica albuginea, within which the gland substance consisted of tubules separated by relatively wide groups of interstitial cells of normal appearance, in whose nuclei mitotic figures were occasionally found. The tubules were lined by a layer of high cells, nowhere more than one cell deep, except that here and there a nucleus lay farther from the basal margin than the others. The nuclei were of medium size and contained relatively less chromatin than those of the interstitial cells. No mitoses could be found. The cytoplasm toward the free border was frayed out into long irregular strands which were so interlaced that the lumina of the tubules seemed in most places to be filled by this vague network of protoplasmic material. Within the cell-bodies of this epithelial lining there were numerous large vacuoles. Germ-cells were totally lacking; no tubule contained any cells other than those already described, which were presumably partially degenerated Sertoli cells. The connective tissue of the testis was normal in appearance, showing no sign of the hyaline degeneration which has sometimes been seen in hermaphrodite glands. The epididymis (fig. 4) was similar in all respects to that of a normal male animal except that it contained no spermatozoa.
In order to gain a general view of the ovary it was cut into six blocks and sections were taken from each of these portions; these presented everywhere the histological structure of a normally functioning organ (fig. 5) . The corpora lutea were recently formed, with the membrana propria broken down and the elements of the theca interna just beginning to invade the granulosa, indicating that ovulation had taken place about three days before. (For grounds for this estimate, see Corner, 1919.) This finding is, of course, in accord with the presence of an ovum in the tube. No special significance is attached to the fact that one of the corpora lutea was slightly cystic, since this is a common occurrence in normal swine. The cortex of the ovary contained primordial ova and there were numerous follicles of normal type. Due consideration was given to the possibility that small masses of testicular tissue might be present in the ovary; that is, that the organ might be an ovotestis (as in one of Pick's cases, winch macroscopically closely resembles ours), but no foreign tissue was found.
The uterine mucosa was normal and similar in both horns. From the results of studies on the cyclic changes in the uterine mucosa, now in preparation, the author feels justified in stating that the uterus of this animal presented the microscopic features characteristic of the period of oestrus.
Owing to the fortunate circumstance that this pig passed into the butcher's hands as a sexually mature animal just after an ovulation had occurred, we have had a unique opportunity to study the physiological state of the ovary; indeed, this is apparently the first sure case of glandular hermaphroditism in which there is direct evidence of the discharge into the deferent duct of germ-cells from either gonad.
In the presence of a normal ovary containing very early corpora lutea, an ovum in passage through the Fallopian tube, and a full-sized uterus histologically normal, it seems more simple to consider this animal as functionally a female (at least as far as the internal genitalia are concerned) in which a local malformation had substituted a functionless testis and an epididymis for one ovary and the corresponding oviduct. In this respect the conditions are much like those of the previously described examples of true hermaphroditism in swine (now numbering about fifteen), in each of which the internal genitalia have been feminine as to gross morphology, with a more or less well-developed uterus and a testis or ovotestis in the anatomical position of the ovary. The opposite type of hermaphroditism — the presence of an ovary or ovotestis at the usual site of the testis, with the genital duct system resembling the male type — should it occur, is far less likely to be observed by the anatomist because of the general custom of castration of boars intended for the butcher. In three of the four cases in man, however, which were summarized in the comprehensive review of L. Pick (1914), the hermaphrodite gland was found in the inguinal canal. The male gland of our specimen was not dissimilar to those of other cases. The close resemblance to the testes of ridglings, the absence of germ-cells, the relatively numerous interstitial cells, the remarkably complete epididymis, the persistent Wolffian duct, have all been commented upon in previous reports. So fully elaborated and indubitable a male apparatus as this must at once dispose of contentions such as that of Kermauner (1912), that the germ-lacking organs of supposed hermaphrodites are merely examples of nondifferentiation from a neutral state of the gonadal primordium. In view of the current debate as to the early history of the germ-cells in mammals, great interest attaches to the question as to whether these gamete-free testes of hermaphrodites at any time in their development contained spermatogonia ; and upon the answer to this depend the further questions as to why the ova seem always to survive at the expense of the spermatozoa, and in what manner the male germ-cells are inhibited; but these questions must await experimental attack or the chance discovery of embryonic stages of glandular hermaphroditism.
Corner, G. \Y., 1919. On the origin of the corpus luteum of the sow from both granulosa and theca interna. Am. Jour. Anat. 26, 117-183.
Kermatjnbr, F., 1912. Sexus anceps oder Hermaphroditismus. Frankf. Zeitschr. f. Pathol. 11.
Kincsuurt, B. F., 1909. Report of a case of hermaphroditism (H. verus lateralis) in Sus scrofa. Anatomical Record, 3, 27S-282.
Pick, L., 1914. Ueber den vvahren Hcrmaphroditismus des Menschen und der Saugetiere. Arch, f . mikr. Anat. 84, 2 Abt. 119-242.
Retjtek, J., 1885. Ein Beitrag zur Lehre von Hcrmaphroditismus. Verh. d. phys. med. Gesellsch. zu Wurzburg, N. F. xix.
(1) General view of specimen; X 0.75. (2) Section of testis showing relative proportions of tubular and interstitial cells; X 28; hematoxylin and eosin. (3) Section of testis showing details of structure; X 1300; iron hematoxylin. (4) Section of epididymis showing normal character of tissue; X 80; hematoxylin and eosin. (5) Section of ovary showing several small Graafian follicles and part of an early corpus luteum ; X 15; hematoxylin and eosin. These figures were drawn directly on stone from the gross specimen and from the sections.