The Genital Anomaly Associated with Prenatal Exposure to Progestogens
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1 The Genital Anomaly Associated with Prenatal Exposure to Progestogens Howard W. Jones, Jr., M.D., and Lawson Wilkins, M.D. THE GREAT MAJORITY of individuals with positive (female) sex chromatin and masculinized external genitalia are examples of female hermaphroditism due to congenital adrenal hyperplasia. A few such individuals will be found to be true hermaphrodites. Except for a small, special group with multiple genitourinary anomalies and a few "spontaneous" cases, the remainder have no evident intrinsic androgenic source, but were born of mothers who had received, while pregnant, a steroid with androgenic properties. The small, special group with multiple genitourinary anomalies is characterized by a penile urethra with a urethrovaginal fistula, a capacious vagina and bladder, anomalies of the upper urinary tract, and often by a history of urinary retention. As there is no evidence of virilization in these cases and no endocrinologic explanation for their occurrence, they will not be considered here. Our principal concern is with female hermaphrodites whose mothers had received a compound with androgenic properties, although these compounds had been utilized in the first instance for their progestogenic characteristics. In all such cases the sex chromatin is positive (female) and the miillerian and wolffian ducts have developed entirely according to the normal female pattern. The only abnormality is confined to the external genitalia, where the genital tubercle and the scrotolabial folds have developed into genitalia with striking masculine characteristics. From the Departments of Gynecology and Pediatrics, Johns Hopkins University School of Medicine, Baltimore, Md. This paper was presented at the Fifteenth Annual Meeting of the American Society for the Study of Sterility, Atlantic City, N. J., April 3-5,
2 Vol. 11, No. 2, 1960 GENITAL ANOMALY 149 Exclusive of the patients previously reported by the present authors18 and included in the present material for completeness, there were 21 female patients with masculinization of the external genitalia reported in the literature through In 6 of these there was no history of maternal medication Two patients were observed whose mothers had arrhenoblastomas.1 5 Nine patients were observed whose mothers had received various forms of androgen for one reason or another, usually not related to a problem of pregnancy This leaves but 4 patients described whose mothers had received 17 -ethinyltestosterone for various complications related to pregnancy.7 10, 15, n MATERIAL The present material consists of 27 female patients with nonvirilizing masculinization of the external genitalia. Seventeen of these were previously reported. 18 All patients had positive (female) nuclear chromatin arrangement and normal levels of 17-ketosteroid excretion. The possibility of true hermaphroditism was excluded in 6 patients by exploratory laparotomy. \Vhen there is a clear history of maternal progestogen treatment, laparotomy is no longer considered necessary, so the possibility, although remote, that true hermaphroditism occurred in some of the 21 unexplored patients cannot be completely excluded. Seventeen mothers had received 17-ethinyltestosterone during their pregnancies. The doses varied from 20 to 200 mg. per day. There was a rough eorrelation between the size of the dose and the degree of abnormality. Large doses ( 100 to 200 mg. per day) and early administration (fourth to sixth week) were associated with scrotolabial fusion. However, in 1 case considerable fusion occurred with but 20 mg. per day beginning in the seventh week. In addition to the 17-ethinyltestosterone, 3 mothers had received intramuscular progesterone for short periods, 2 mothers had received 17-hydroxyprogesterone in oil, 7 mothers had received stilbestrol in large doses, and 1, ethinyl estradiol, 0.1 mg. per day, for a short period of time. Four mothers had received 17-ethinyl-19-nor-testosterone. The dosage varied from 3 to 30 mg. a day and had been started from the sixth to the fifteenth week. There was no fusion in the patient whose mother had started on the treatment in the :fifteenth week. In the other patients, whose mothers had started in the sixth, seventh, and tenth week, there was fusion of various degrees and it was very marked in the 2 patients whose mothers had started in the sixth and tenth week.
3 150 JONES & WILKINS Fertility & Sterility One patient's mother had received a tablet containing 3 mg. of methyltestosterone and 0.01 mg. of ethinyl estradiol daily from the eighth week to term. In this patient there was phallic enlargement but no labial fusion. Two mothers had received intramuscular progesterone. One had received 100 mg. three times a week for six injections during the ninth and tenth week and had taken 10 mg. of stilbestrol from the fifth month to term. The dosage in the other mother is unknown. There was slight fusion in 1 patient, but there was clitoral enlargement in both. There was no history of maternal medication in 3 patients. Interestingly enough, one such mother described generalized acne and another, deepening of the voice, edema, and hirsutism during the gestation. External Genitalia THE CONGENITAL ANOMALY It is of considerable practical importance in the surgical correction of anomalies of the external genitalia to know if the maldevelopment is the same in all patients, regardless of the steroid involved. The principal structure involved-the urogenital sinus-gives rise in the female to a portion of the bladder, urethra, paraurethral glands, bartholian glands, vaginal vestibule, the lower vagina, the inner surface of the labia majora, and the minor vestibular glands; in the male it yields part of the bladder, prostatic urethra, prostate, Cowper's glands, the membranous urethra, the cavernous urethra, and the periurethral glands. The genital tubercle, which is also concerned in the anomalies under consideration, yields the clitoris and prepuce in the female and the homologous structures in the male. As these structures are concerned not only with external appearance and with providing an entrance to the genital and urinary tracts but also with urinary control, it is of utmost impmtance that the gynecologic surgeon know if the anomaly is unifonn in detail, regardless of steroid, and if the generative and urologic structures can be surgically separated without damage to either. The problem is underlined by the exquisite end-organ specificity possessed by various compounds used by experimental embryologists (review by Jost 14 ). This anatomic problem was studied in detail on a relatively large number of patients with anomalies due to congenital adrenal hyperplasia. 13 It was concluded that in no case did the vagina communicate with that portion of the urogenital sinus that gives rise in the female to the entire urethra or in
4 Vol. 11, No.2, 1960 GENITAL ANOMALY 151 the male to the prostatic urethra. The communication was always with the caudal urogenital sinus derivatives, which in the female yield the vaginal vestibule and in the male the membranous urethra. The urinary sphincter mechanism was therefore fortunately not involved. Additional studies of many patients with congenital adrenal hyperplasia have confirmed the validity of these findings. It will be recognized that the embryonic significance of the prostatic utricle as the homologue of the vagina may be inconsistent with the findings just related. In the present series there was a well-developed urogenital sinus in 6 patients whose mothers had received 17 -ethiny!testosterone, in 2 patients whose mothers had received 17-ethinyl-19-nor-testosterone, and in the 3 patients whose mothers had received no medication. A careful study of these anomalies by endoscopic examination and by roentgen visualization indicated that the anatomic arrangements resulting from the adrenal androgen of congenital adrenal hyperplasia as outlined in the preceding paragraph was the same in detail as those in the present series of patients whose mothers had received 17 -ethinyltestosterone or 17 -ethinyl- 19-nor-testosterone. The surgical potentiality was therefore essentially the same as with the cases of congenital adrenal hyperplasia. Urinary continence was not threatened by surgical separation of the generative and urinary orifices. The practical surgical results bear out these anatomic considerations. Internal Genitalia All 3 patients whose mothers had received no steroid therapy were subjected to laparotomy to rule out true hermaphroditism. On 1 patient, reared as a boy, a total hysterectomy and bilateral salpingo-oophorectomy were performed, and on the other patients, who were reared as girls, ovarian biopsy was carried out. The uterus, tubes, and ovaries in all instances were entirely normal and there was no gross evidence of wolffian duct structures. Three other patients, 2 whose mothers had received 17 -ethinyltestosterone and 1 whose mother had received progesterone alone, were subject to laparotomy. In each instance the tubes and ovaries were entirely normal. Biopsy of the ovaries was carried out in all 3 patients and revealed no abnormality. DIAGNOSIS AND TREATMENT Any newborn infant with ambiguous external genitalia must be suspected of having nonvirilizing female hermaphroditism. If the nuclear chromatin
5 Fig. I. Saggital view showing the relations of the urogenital sinus to the vagina and female urethra of an 18-month-old patient with female hermaphroditism. Fig. 2. A, external genitalia. B, beginning of the operation. Incision into the urogenital sinus. (Reprinted by permission of the Williams & Wilkins Co., Baltimore, Md.l4)
6 Vol. 11, No. 2, 1960 GENITAL ANOMALY 153 arrangement is positive, the diagnosis lies between the adrenogenital syndrome, true hermaphroditism, and nonvirilizing female hermaphroditism. A normal excretion of urinary 17 -ketosteroids eliminates adrenal hyperplasia. True hermaphroditism can be excluded only by laparotomy, but if there is a history of maternal progestogen therapy we no longer consider laparotomy justified. With steroid-induced hermaphroditism, progressive virilization will not occur. Although no patients with iatrogenic masculinized external genitalia have yet reached puberty, there is no reason to believe that any abnormality in menstruation will ensue. For these reasons the rearing should be feminine. Surgical reconstruction of the external genitalia is the only indicated therapy. This, of course, is reserved for the more serious deformities. Of the 26 patients reared as girls in this series, 9 had reconstructive procedures according to the technic outlined in the accompanying figures (Figs. 1-6). Two additional patients had a simple amputation of the phallus. The remainder Fig. 3. A, the situation after the incision of the urogenital sinus. B, freeing of the posterior and lateral edges of the vagina in order to bring them to the edges of the skin without undue traction. (Reprinted by permission of the Williams & Wilkins Co., Baltimore, Md.14 )
7 154 JONES & WILKINS Fertility & Sterility 4 Fig. 4. The operative situation after the edges of the vagina and urogenital sinus are sutured to the skin. (Reprinted by permission of the Williams & Wilkins Co., Baltimore, Md.l4 ) Fig. 5. A, the skin incision to excise the phallus. B, drawing to show the shape of the incision to preserve the flap of mucous membrane along the ventral surface of the phallus to be used in fashioning a cosmetic clitoris. (Reprinted by permission of the Williams & Wilkins Co., Baltimore, Md.14 ) had phallic enlargements that were not considered sufficient to require removal. THE USE OF PROGESTOGENS FOR THE TREATMENT OF PREGNANCY WAST AGE Although it seems inescapable that the masculinization of the external genitalia of the reported children was associated with the maternal medication as described, the association is obviously not a simple one. The progestogens concerned are widely used, and only a very small proportion of babies born of treated mothers are affected. Differences in hormone deficiency, placental permeability, hormone metabolism, and end-organ sensitivity are probably concerned in the effect. The question naturally arises as to the propriety of the use of progestogens for the therapy of pregnancy wastage. Although a sufficient number of cases
8 Vol. 11, No.2, 1960 GENITAL ANOMALY 155 Fig. 6. The concluding steps of the operation. (Reprinted by- permission of the Williams & Wilkins Co., Baltimore, Md.14 ) has not accumulated to be valid in a statistical sense, it is known that some progestogens are less androgenic than others with respect to the fetal female external genitalia. Progesterone, the nature hormone, seems to give less trouble than 17-ethinyltestosterone and considerably less trouble than 17- ethiny 1-19-nor-testosterone. We are convinced that the danger of this undesirable side effect is not great enough to interdict the use of these compounds for the treatment of pregnancy wastage, but common sem:e suggests the use of those that have given the least trouble. Perhaps the most important single point of this entire problem is that the use of a progestogen should be reserved only for those cases where a progestogenic deficiency can be shown to exist. In any event, the defect is not serious and can be easily corrected. The practical point is awareness of the problem. SUMMARY Masculinization of the external genitalia without progressive virilization was observed in 27 children. The mothers of 17 of these had received 17- ethinyltestosterone, of 4, 17-ethinyl-19-nor-testosterone, of 2, progesterone, and of 1, methyltestosterone. Three mothers had received no medication. The anatomic arrangement of the deformity was similar to that observed in congenital adrenal hyperplasia. Surgical correction was quite satisfactory, without damage to either the generative or urologic structures.
9 156 JONES & WILKINS Fertility & Sterility REFERENCES 1. BHETNALL, C. P. A case of arrhenoblastoma complicating pregnancy. ]. Obst. & Gynaec. Brit. Emp. 52:235, CARPENTIEH, P. J. Malformation genitale du foetus feminin apn':s administration d'un nouveau steroide de synthese pendant la grossesse. Bull. Soc. roy. belge gyntket obst. 28:137, CHAXIS, D., Jn. Some aspects of hermaphroditism: report of a case of female pseudohermaphroditism. ]. Ural. 42:508, CoTTE, G. Plastic operations for sexual ambiguity. ]. Mt. Sinai Hasp., New York 14:170, FELICISSIMO, P. X. J., and DE ABHEU, J. M. S. Sobre un caso de arrhenoblastoma do ovario e gravidez topic simultanea: virilisacao da gestante do feto feminino. Rev. gynec. e obst. 1 :356, GoLD, A. P., and MICHAEL, A.M. Testosterone-induced female pseudohermaphroditism. ]. Pediat. 52:279, GRoss, R. E., and MEEKER, I. A. Abnormalities of sexual development. Observations from 75 cases. Pediatrics 16:303, GRUNWALDT, E., and BATES, T. Nonadrenal female pseudohermaphroditism after administration of testosterone to mother during pregnancy. Pediatrics 20:503, HAYLES, A. B., and NoLAN, R. B. Female pseudohermaphroditism: report of case in an infant born of a mother receiving methyltestosterone during pregnancy. Proc. Staff Meet., Mayo Clin. 32:41, HAYLES, A. B., and NoLAN, R. B. Masculinization of female fetus, possibly related to administration of progesterone during pregnancy. Report of two cases. Proc. Staff Meet., Mayo Clinic 33:200, HAYNES, E., THOMAS, H., and WHEELER, N. S. Pseudohermaphroditism with psychosis. M. Rec. 154:307, HoFFMAN, F., OvERZIER, C., and UHDE, G. Zur Frage der hormonalen Erzeugung fotaler Zwitterbildung beim Mensch en. Geburtsh. u. Frauenh. 15:1061, Jmms, H. W., JR., and JoNES, G. E. S. The gynecological aspects of adrenal hyperplasia and allied disorders. Am.]. Obst. & Gynec. 68:1330, JoNES, H. W., JR., and ScoTT, W. W. Hermaphroditism, Genital Anomalies and Related Endocrine Disorders. Baltimore, Williams & Wilkins, MoNCRIEFF, A. Non-adrenal female pseudohermaphroditism associated with hormonal administration during pregnancy. Lancet 2:267, NELLHAUS, G. Artificially induced female pseudohermaphroditism. New England ]. Med. 258:935, REILLY, W. A., HINMAN, F., PicKERING, D. E., and CRANE, J. T. Phallic urethra in female pseudohermaphroditism. A.M.A. Am. ]. Dis. Child. 95:9, WILKINS, L., JoNES, H. W., JR., HoLMAN, G. H., and STEMPFEL, R. S., JR. Masculinization of the female fetus associated with administration of oral and intramuscular progestins during gestation: non-adrenal female pseudohermaphroditism. ]. Clin. Endocrinol. 18:559, ZAr-.'lJER, J., and MuLLER, H. A. Dber die Methylandrostenediolbehandlung wahrend einer Schwengerschaft. Geburtsh. u. Frauenh. 13:216, 1953.
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