Leydig cell hypofunction resulting in male pseudohermaphroditism*

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1 FERmlTY AND STERILlTY Copyright" 1982 The American Fertility Society Vol. 37, No.6, May 1982 Printed in U.S.A. Leydig cell hypofunction resulting in male pseudohermaphroditism* Peter A. Lee, M.D., Ph.D.t+1I John A. Rock, M.D. Terry R. Brown, Ph.D.+ Kaye M. Fichman, M.D.+ Claude J. Migeon, M.D.+ Howard W. Jones, Jr., M.D. The Johns Hopkins University School of Medicine, Baltimore, Maryland, and University of Pittsburgh School of Medicine, Children's Hospital of Pittsburgh, Pittsburgh, Pennsylvania An 11-year-old patient with male pseudohermaphroditism presented with essentially normal-appearing female external genitalia. When examined, inguinal gonads, redundant foreskin, and some posterior labial fusion were found. Evaluation revealed basal testosterone (T) levels ranging from 65 to 107 ng/dl with slightly elevated serum gonadotropin levels (luteinizing hormone [LH): 76 ng/ml, and folliclestimulating hormone [FSH}: 568 ng/ml). Neither T nor its precursors increased with human chorionic gonadotropin (hcg) stimulation. However, progesterone (P), 17-hydroxyprogesterone (17-0HP), and cortisol (F) responses to adrenocorticotropic hormone (ACTH) were normal. Androgen binding and 5a-reductase activity in cultured genital skin fibroblasts were normal. These data, plus the microscopic finding of a markedly reduced number of Leydig cells, strongly suggest that. the male pseudohermaphroditism in this patient was due to inadequate Leydig cell function unrelated to LHreceptors. Fertil Steril37:675, 1982 An absence of Leydig cells has been reported to be the cause of male pseudohermaphroditism in three cases recently reported in the literature.!-3 The first patient! presented at age 35 with no pubertal development except pubic hair. Exami- Received September 8, 1981; revised and accepted January 27,1982. *Supported in part by USPHS grants AM and RR treprint requests: Peter A. Lee, M.D., Ph.D., Children's Hospital of Pittsburgh, 125 DeSoto Street, Pittsburgh, Pennsylvania *Division of Pediatric Endocrinology, Department of Pediatrics, The Johns Hopkins University School of Medicine. Division of Reproductive Endocrinology, Department of Obstetrics and Gynecology, The Johns Hopkins University School of Medicine. IIDepartment of Pediatrics, University of Pittsburgh School of Medicine, Children's Hospital of Pittsburgh. nation revealed some posterior labial fusion, bilateral inguinal masses, and a shallow vagina but otherwise normal female external genitalia with a normal clitoris and separate urethral and vaginal openings. The second patient 2 also presented as a prepubertal phenotypic female at age 15 who had bilateral masses in the inguinal areas. Both patients showed no change in steroidal levels after chorionic gonadotropin stimulation but a normal response to adrenocorticotropic hormone (ACTH) stimulation. Both had a marked reduction or absence of Leydig cells, and spermatogonia were present in the tubules. In the older patient, there was also extensive hyalinization of the seminiferous tubules. The third patient3 was evaluated at the age of 2.5 years. This patient had no Leydig cells identified after 14 days of human chorionic gonadotropin (hcg) stimulation and no Lee et ai. Genital ambiguity in Leydig cell failure 675

2 When the patient was standing, the external genitalia were asymmetrical, the left labium being larger than the right. Each labium contained a 2 x 2-cm mass. The clitoris was 2 cm long with redundant foreskin. The urethral meatus was in the normal female position, and there was some posterior labial fusion. When the labia were retracted, a vaginal opening and vaginal pouch could be visualized (Fig. 1). No uterine, adnexal structures, or prostate could be palpated on rectal examination. The patient had a bone age of 7 years 10 months and a 46,XY karyotype. After hormonal evaluation (see Results), genital reconstructive surgery was performed. The gonads were removed through incisions in the labia, the posterior fusion was incised, the vaginal introitus was exteriorized, and a portion of the redundant foreskin was excised (Fig. 2). SPECIAL STUDIES The patient had a 5-day hcg stimulation test (3000 U/M 2 of body surface area per day) and an Figure 1 External genitalia showing (A) labia majora containing testes, redundant foreskin, and posterior labial fusion and (B) urethral and vaginal openings. binding of luteinizing hormone (LH)-hCG to membrane preparations of testicular tissue. CASE REPORT This 11-year-old white phenotypic female presented with a 6-month history of intermittent abdominal discomfort and the intermittent appearance of bilateral inguinal masses. She was the 2860-gm product of a term pregnancy complicated by first-trimester bleeding and gestational diabetes controlled by diet. Five older siblings, three males and two females, are normal, and all have reproduced. Two younger siblings, one male and one female, are also normal. The patient was normotensive, weighed 23.6 kg, and was cm tall. She had no breast development, no acne, and no axillary hair, but a few coarse hairs were present on the labia. Her physical examination was entirely normal except for the genitalia (Fig. 1). There was mild tenderness at palpation over the internal inguinal rings. 676 Lee et al. Genital ambiguity in Leydig cell failure Figure 2 Postoperative appearance of external genitalia demonstrating the medial labial incisions made for gonad resection, circumcision incision, and incision for resection of posterior labial fusion. Fertility and Sterility

3 Table 1. Hormone Levels in a Patient with Leydig Cell Hypoplasia Hormone Unit Patient Plasma Testosterone ng/dl 103; 107 Androstenedione ng/dl 28;29 Progesterone ng/dl hydroxyprogesterone ng/dl 10 Dehydroepiandrosterone ng/dl 214 Serum Follicle-stimulating hormone ng/ml 568 Luteinizing hormone ng/ml 76 Normal levels (mean ± SD) Prepubertal Adult male Follicular adult female 12 ± ± ± ± ± ± ± 5 21 ± 8 37 ± 6 35 ± ± ± ± ± ± ± ± ± ± 3 48 ± ± 21 intravenous ACTH stimulation test (100 U synthetic ACTH given over a I-minute period). Previously described methods were used for the determination of progesterone (p),4 17-hydroxyprogesterone (17-0HP),4 LH,5 follicle-stimulating hormone (FSH),6 and cortisol (F).7 Dehydroepiandrosterone (DHEA) was measured after extraction and chromatography procedure similar to those used for 17-0HP. Plasma testosterone (T) and androstenedione (d4a) were measured by a modification of the method of Furuyama et al. 8 after extraction of 1 ml of plasma with carbon tetrachloride and chromatography using LH-20 Sephadex columns and isooctane:benzene:methanol (85:19:5) as solvent. Dihydrotestosterone (DHT) levels were measured in a commercial laboratory. Fibroblasts grown in culture from a foreskin biopsy were used for DHT receptor assay and 5a-reductase activity. Conditions for the culture skin fibroblasts9 and the assay of whole cell DHT binding lo were as previously described, except that the unbound steroid was removed by absorption on dextran-gelatin-coated charcoal (0.05% dextran T70, 0.1% calfskin gelatin, 0.5% activated charcoal). 11, 12 Specifically bound DHT was Table 2. Hormone Responses to hcg and ACTH Stimulation T ngldl a'a ngldl hcg stimulation test (3000 units daily) Baseline Day Day Day Day ACTH stimulation test (100 units synthetic ACTH intravenous push) Baseline minutes minutes minutes minutes calculated by subtracting nonspecific binding from the total bound radioactivity. The kinetics of the saturation of the receptors by increasing amounts of DHT (0.2 to 2.5 nm) were studied. A Scatchard plot13 of the data and linear regression analysis14 permitted the determination of the binding capacity (Bmax) and affinity (apparent dissociation constant or K d) of the receptor for DHT. Deoxyribonucleic acid (DNA) was measured by the method of Burton. 15 The quantitation of 5a-reduced products formed from T was accomplished as previously described,9 except that the initial concentration oft added to each culture plate was 200 nm (4 nm 3H-testosterone plus 196 nm nonradiolabeled T). RESULTS Basal levels of androgens and intermediate metabolites of adrenal and testicular source are listed in Table 1. Plasma T levels were those of a pubertal male and and those of d 4A, P, and 17-0HP were in a prepubertal range. Plasma DHEA levels were at the lower limit of the adult male range. Urinary 17 -ketosteroids were in the 17-0HP P DHT F ngldl ngldl ngldl mgldl Lee et ai. Genital ambiguity in Leydig cell failure 677

4 products, mainly DHT. The 5a-reduced products/ J.Lg DNA/60 minutes (n = 3). The normal value from our laboratory for genital skin fibroblasts is 2492 ± 644 (mean ± SD). It was concluded that the androgen binding and metabolic studies in cultured genital skin fibroblasts were within the normal range. DISCUSSION ~ Figure 3 Resected testes, epididymides, and spermatic cords. Testes have been bisected. pubertal range (4.6 mg/24 hour). FSH levels were above the adult male range, and LH levels were elevated for age and at the upper limit of the adult male range. There was no detectable response of P, 17-0HP, Jl 4 A, T, and DHT to 5 days of hcg stimulation (Table 2). The hormonal response to ACTH stimulation was normal (Table 2). The testes, epididymides, and spermatic cord are shown in Figure 3. The testes contained a markedly reduced number of Leydig cells, considering that the patient had somewhat elevated levels of endogenous LH. The basement membrane of the seminiferous tubules was normal. In the tubules, the Sertoli cells appeared normal, and various types of spermatogonia were present, but spermatocytes were absent (Fig. 4). Skin fibroblast cultures propagated from explants of the patient's foreskin specimens were assayed for androgen receptor binding and 5a-reductase enzyme activity. The specific DHT binding (Bmax) was 541 fmol/mg DNA (normal, 619 ± 165 fmol/mg [mean ± standard deviation (SD)]) and Kd ofdht for the steroid receptor was 0.82 x 10-9 M (normal, 0.78 ± 0.25 [mean ± SD]). The metabolism of T by the patient's foreskin fibroblasts resulted in a predominance of 5a-reduced 678 Lee et a1. Genital ambiguity in Leydig cell failure This prepubertal male pseudohermaphrodite presented with essentially normal female external genitalia. Inguinal gonads could be palpated, and a redundant foreskin and posterior labia fusion were present. Evaluation of the patient indicated that she was unable to increase circulating levels of T when stimulated with gonadotropin. The measurement of precursors during hcg stimulation, the normal blood pressure, and lack of any evidence of adrenal cortical insufficiency indicated that there was no steroid enzyme deficiency. The F, P, and 17-0HP responses to acute ACTH administration were also normal. It is clear that our patient did not have a complete absence of Leydig cells; well-defined cells were seen on the testicular biopsy, and the levels of plasma T reaching 107 ng/dl were indicative of some degree of secretion of androgens by the gonads. However, the low basal levels of T despite high normal LH concentrations, along with the absence of response to hcg, demonstrate a definite hypofunction of the Leydig cells..this correlated with an apparent decreased number of Figure 4 Microscopic section of testis showing paucity of Leydig cells and seminiferous tubules demonstrating limited germ cell maturation. Fertility and Sterility

5 Leydig cells seen at histologic examination when compared with that observed in normal pubertal testes. An inability of the testes to produce adequate amounts of T in a pubertal subject can be due either to a decrease in the number of normal Leydig cells or to a decrease in LH receptors with a normal number of Leydig cells. A complete absence of LH receptors despite a normal number of Leydig cells would be expected to result in a microscopic appearance of the testes similar to that observed prior to puberty when Leydig cells are not visible. The appearance of Leydig cells in testes with a partial absence oflh receptors has not been verified. A partial absence of LH receptors with a normal number of Leydig cells could be expected to give a microscopic appearance of poorly developed Leydig cells, but in normal quantity. However, another possible situation would be a decrease in the total number of Leydig cells in the testes and a proportional decrease in the number oflh receptor sites with the number of receptors per cell being normal. Unfortunately, no receptor studies were carried out on our patient's gonadal tissue. Therefore, we cannot determine in our patient whether the LH binding activity was normal for the number of Leydig cells or not. It is of interest to note in the case of Schwartz et a1. 3 that the lack of LH receptor sites and the inability to distinguish Leydig cells on microscopic examination could be interpreted as either a normal number of Leydig cells with complete absence of receptors or a complete absence of Leydig cells with a resulting absence of receptors. REFERENCES 1. Berthezene F, Forest MG, Grimand JA, Claustrat B, Mor nex R: Leydig-cell agenesis. A course of male pseudohermaphroditism. N Engl J Med 295:969, Brown DM, Markland C, Dehner LP: Leydig cell hypoplasia: a cause of male pseudohermaphroditism. J Clin Endocrinol Metab 46:1, Schwartz M, Imperato-McGinley J, Peterson RE, Cooper G, Morris PL, MacGillivray M, Hensle T: Male pseudohe:rmaphroditism secondary to an abnormality in Leydig cell differentiation. J Clin Endocrinol Metab 53:123, Gutai JP, Kowarski AA, Migeon CJ: Twenty-four hour integrated concentration of progesterone, 17 -hydroxyprogesterone and cortisol in normal male subjects. J Clin Endocrinol Metab 44:116, Lee PA, Plotnick LP, Steele RE, Thompson RG, Blizzard RM: Integrated concentrations of luteinizing hormone and puberty. J Clin Endocrinol Metab 43:168, Lee PA, Plotnick LP, Migeon CJ, Kowarski AA: Integrated concentrations of follicle-stimulating hormone and puberty. J Clin Endocrinol Metab 46:488, Beitins IZ, Shaw MH, Kowarski A, Migeon CJ: Comparison of competitive protein binding radioassay of cortisol to double isotope dilution and Porter-Silber methods. Steroids 15:765, Furuyama SD, Mayes M, Nugent CA: A radioimmunoassay for plasma testosterone. Steroids 16:415, Amrhein JA, Klingensmith GJ, Walsh PC, McKusick VA, Migeon CJ: Partilil androgen insensitivity. The Reifenstein syndrome revisited. N Engl J Med 297:350, Brown TR, Migeon CJ: Cultured human skin fibroblasts: a model for the study of androgen action. Molec Cell Biochem 36:3, Korenman SG, Dukes BA: Specific estrogen binding by the cytoplasm of human breast carcinoma. J Clin Endocrinol Metab 30:639, McGuire WL, DeLaGarza M: Improved sensitivity in the measurement of estrogen receptor in human breast cancer. J Clin Endocrinol Metab 37:986, Scatchard G: The attraction of proteins for small molecules and ions. Ann NY Acad Sci 51:660, Rodbard D, Rayford PL, Cooper J: Statistical quality control of radioimmunoassays. J Clin Endocrinol Metab 28: 1412, Burton K: A study of the conditions and mechanism of the diphenylamine reaction for the colorimetric estimation of deoxyribonucleic acid. Biochem J 62:315, 1956 Lee et al. Genital ambiguity in Leydig cell failure 679

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