REAPPRAISAL OF THE VALUE OF TESTICULAR BIOPSY IN THE INVESTIGATION OF INFERTILITY

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1 FERTWTY AND STEIuLlTY Copyright <> 1980 The American Fertility Society Vol., No.1 January 1980 Prinwl in U.S.A. REAPPRAISAL OF THE VALUE OF TESTICULAR BIOPSY IN THE INVESTIGATION OF INFERTILITY TERENCE J. COLGAN, M.D.. YV AN C. BEDARD, M.D., PH.D., F.R.C.P.(C)* HARRY T. G. STRAWBRIDGE, M.D., F.R.C.P.(C) MARTIN B. BUCKSPAN, M.D., F.R.C.P.(C) PInLIP G. KLOTZ, M.D., F.R.C.P.(C) Divisions of Pathology and Urology, Mount S ~nai Hospital, University of Toronto, Toronto, Ontario, Canada One hundred and forty-two biopsies were reviewed to reappraise the value and indications for testicular biopsy in the investigation of infertility. These biopsies were categorized within the following morphologic patterns: normal, hypospermatogenesis, maturation arrest, Sertoli cell-only, and Klinefelter's. The morphology of the biopsies was correlated with the available sperm count, and the contribution of the biopsy to the patient's treatment was assessed. Testicular biopsy has proved most useful in azoospermia for the identification of obstruction. In oligospermia, biopsy appears to be of little use. Fertil Steril:56, 1980 Male infertility is a common problem, since male etiologic factors are important in one-half of barren marriages. l - The armamentarium for investigation of male infertility includes history, physical examination, biochemical investigations, semen analysis, and testicular biopsy. Although testicular biopsy has been performed for more than 0 years, its role remains controversial. 4-7 The purpose of this paper is to present our experience with testicular biopsies in an attempt to assess indications for this procedure. Testicular biopsies were reviewed with emphasis on informa" tion yielded by biopsy beyond that obtained from seminal fluid analysis. The contribution of biopsy to therapeutic decisions is considered. MATERIALS AND METHODS During the period January 1971 to February 1979, 142 patients underwent testicular biopsy at Mount Sinai Hospital, Toronto, during investigation of infertility. Unilateral biopsies were usually performed under general anesthesia on an outpatient basis. A small incision through skin, dartos, Received July 9, 1979; accepted August 16, *Reprint requests: Dr. Y. C. Bedard, 600 University Avenue, Toronto, Onto M5G lx5, Canada. 56 and tunica albuginea exposed' the testicular parenchyma for biopsy. The biopsy specimen was immediately immersed in Bouin's fixative for better histologic preservation. Bilateral testicular biopsy was performed when a significant discrepancy in size or consistency between the testes was detected clinically. 8 Occasionally, biopsy was performed incidentally to varicocelectomy. Each biopsy specimen was processed using routine histologic techniques and hematoxylin and eosin staining. The authors reviewed and classified each biopsy without prior knowledge of clinical history or semen analysis. Semen was analyzed using a specimen obtained by masturbation after 2 to 5 days of sexual abstinence. Sperm counts were determined using a hemocytometer and a 1:10 or 1:20 dilution of semen by normal saline-chloroform diluent, and expressed as number of sperm per milliliter of semen. These semen samples were grouped according to sperm count into one of three categories: total absence of sperm (azoospermia), <1 to 20 million/ml (oligospermia), and >20 million/ml The latter category could not be considered truly oligospermic, yet it did not represent a normal sperm count since the semen of most patients contained fewer than 50 to 60 million sperm/ml.

2 Vol., No.1 REAPPRAISAL OF TESTICULAR BIOPSY 57 Testicular biopsies could be categorized within the following morphologic classifications: normal, hypospermatogenesis, maturation arrest, Sertoli cell-only, and Klinefelter's. Normal. The normal testicular parenchyma is composed of seminiferous tubules and interstitium (Fig. 1). The seminiferous tubules contain Sertoli and germ cells confined within their limiting basement membrane. The Sertoli cells rest on the basement membrane, have pale nuclei, and a large amount of cytoplasm. Normal spermatogenesis proceeds through six steps to completion: primary and secondary spermatogonia, primary and secondary spermatocytes, spermatids, and sperm. A single seminiferous tubule usually does not exhibit all of these stages since spermatogenesis occurs in waves along the tubules, 9 and a particular field may reveal only one or a few of these maturation stages. Therefore, spermatogenesis can be adequately assessed only after viewing numerous fields and tubules. Hypospermatogenesis. Hypospermatogenesis is characterized by reduced spermatogenesis affecting all stages of germinal cells in a uniform manner (Fig. 2). This reduction can be mild, moderate, or severe in degree. The Leydig cells in hypospermatogenesis are unaffected, although peritubular fibrosis may occur. Maturation Arrest. In maturation arrest spermatogenesis is halted at either a late (spermatid) or early (spermatocyte) stage in the majority of tubules (Fig. ). In any particular patient, the level of the arrest is constant. Maturation arrest usually demonstrates sloughing of immature forms into the tubular lumina. Sertoli Cell-Only Syndrome. In the Sertoli cellonly the tubules demonstrate a total absence of germ cells, a decrease in size, and the presence of Sertoli cells only (Fig. 4). A variable degree of tubular fibrosis is present. Klinefelter's Syndrome. In Klinefelter's there is a progressive loss of germ cells, fibrous obliteration of tubules, and Leydig cell hyp~rplasia (Fig. 5). In the final stage, the tubules have diffusely hyalinized basement membranes, and germinal and Sertoli cells are absent. This condition is also known as sclerosing tubular degeneration and is seen in 47,XXY chromosome karyotypes and occasionally in karyotypically normal males. The relative frequencies of these morphologic classifications are listed in Table 1. Hypospermatogenesis was noted in approximately in one-half, of all biopsies, followed by normal, Sertoli cell-only, maturation arrest, and Klinefelter's. Eight biopsies were considered'unsatis- FIG'. 2. Hypospermatogenesis. There is an over-all proportional reduction of the germinal epithelium ( x 200), FIG.. Maturation arrest. There is a halt of spermatogenesis at the spermatocyte stage (x 250), FIG. 1. Normal testicular biopsy (x 200). For the purpose of this study, the postbiopsy course of azoospermic or oligospermic patients was followed. RESULTS

3 January 1980 COLGAN ET AL. 58 TABLE 1. Relative Frequencies of Morphologic Patterns in Testicular Biopsies of 142 Patients Morphologic pattern Normal Hypospennatogenesis Sertoli cell-only Maturation arrest Klinefelter's Inadequate sample No. of cases % of total factory because of crushed or insufficient tissue_ Sperm counts were available for 91 of the 142 patients. Azoospermia was found in more than half of the 91 patients (Table 2). In these azoospermic patients all morphologic classifications were represented. In contrast, none ofthe oligospermic patients showed Sertoli cell-only or Klinefelter's on biopsy. In the oligospermic group, hypospermatogenesis predominated. Eleven patients had sperm counts between 20 and 60 million/ml. The morphologic patterns of these 11 patients were distributed among hypospermatogenesis, normal, and maturation arrest. Clinical follow-up of the azoospermic patients revealed that biopsy had provided essential information in the consideration of surgical intervention. A diagnosis of Sertoli cell-only or Klinefelter's on biopsy precluded further treatment. Fifteen of the twenty-nine azoospermic patients with normal or hypospermatogenic morphologic patterns refused further treatment or were not available for follow-up. The remaining 14 azoospermic patients with these morphologic patterns subsequently agreed to vasography. The vasograms demonstrated absence of the vas deferens in 4 patients, and 9 of the 10 remaining patients had epididymovasostomies following epididymal head smears showing the presence of spermatozoa. In contrast, biopsies of oligospermic patients FIG. 4. Sertoli cell-only. The tubules show complete absence of germinal epithelium ( x assisted therapeutic decisions infrequently. Although eight of these patients underwent varicocelectomy, the indications for this operation were clinical and were not based on biopsy results. On follow-up, only 4 of the 27 oligospermic patients had been placed on hormone therapy, but morphology did not influence the choice of drug used. DISCUSSION The same or a similar classification system of testicular morphology has been reported previously by others. 1O- 12 Classification of biopsies is both useful and usually facile. However, the distinction between the various degrees of hypospermatogenesis and between normal and mild hypospermatogenesis can be subjective. A mixed morphologic picture of normal, hypospermatogenesis, maturation arrest, and/or Sertoli cell-only is occasionally seen in a testicular biopsy (Fig. 6). It is conceivable that some biopsies diagnosed as Sertoli cell-only represent the end stage of progressive germinal atrophy through hypospermatogenesis and/or maturation arrest stages rather than a congenital lesion. Serial biopsies (for example, in hypospermatogenic patients) to support this speculation are lacking, although this possibility has been mentioned previously. 6 Series of testicular biopsies have been reported FIG. 5. Klinefelter's. The tubules show a thickened basement membrane which is lined by Sertoli cells only. The interstitial cells are markedly hyperplastic (x 200),

4 Vol., No.1 REAPPRAISAL OF TESTICULAR BIOPSY 59 TABLE 2. Sperm Counts versus Morphology in Ninety-One Cases Morphologic pattern Azoospermia Oligospermiaa Nonnal Hypospennatogenesis Maturation arrest Sertoli cellonly Klinefelter's Inadequate sample Total athis category included men with a sperm count of <1 to 20 millionlml. Eleven men had sperm counts of >20 million/ml. previously. The morphologic patterns of testicular biopsies in azoospermic and oligospermic patients were described by Wong et al.,l0 Sniffen et al.,ll and Nelson l2 and essentially agree with the findings presented here. Wong et al. lo proposed a clinicopathologic classification for testicular biopsiespretesticular, testicular, and post-testicular. Drawing from a patient population like our own, Meinhard et al. 6 surprisingly found no difference between the morphologic patterns of azoospermic and oligospermic patients. Specimens indicating Sertoli cell-only and Klinefelter's were found only in the azoospermic group in our series. In our series, testicular biopsy of the azoospermic patient has proven essential in distinguishing obstruction from primary testicular failure. A normal or mildly hypospermatogenic biopsy finding was followed by vasography. Identification of obstructive azoospermia was one of the initial indications for the procedure. 4 Recently, testicular size and follicle-stimulating hormone (FSH) levels have been recommended to screen azoospermic patients for biopsy.7 Elevated FSH levels occur as a result of stimulation of the pituitary by spermatogenic failure, although the exact mechanism of this feedback has not yet been determinedy Consequently, high FSH levels usually reflect severe spermatogenic impairment and obviate the need for testicular biopsy. However, since an occasional patient with a normal biopsy may have an elevated FSH levev testicular biopsy cannot be entirely replaced by FSH estimation. Testicular biopsy of the hypogonadotropic hypogonadic patient with azoospermia may be performed prior to embarking on a lengthy and expensive course of hormone therapy for infertility. In these patients, the impact of absent pituitary stimulation and any previous exogenous testosterone suppression of the germinal epithelium can be assessed. In contrast to azoospermia, testicular biopsy in oligospermia was not essential in its diagnosis or treatment in our series. Since gonadotropin and testosterone assays can diagnose pretesticular causes of infertility, biopsy plays no role in diagnosis ofthese disorders. The morphologic appearance of a biopsy does not influence the selection of hormone treatment of idiopathic oligospermia. During the 8-year period of this study our indications for biopsy have become more limited, and the number of oligospermic patients coming to biopsy has diminished progressively. Nevertheless, biopsy of oligospermic patients is still advocated to establish the prognosis and treatment regimens. 4-6, 14 Indeed, a testicular biopsy rating for prognosis and prediction of hormone treatment response has been proposed. 15 However, others have found testicular biopsy to have no predictive value in patients treated with human menopausal gonadotropins. 16 In our hospital, serial semen analyses alone are used to assess the therapeutic efficacy of hormone treatment programs. REFERENCES FIG. 6. Mixed morphology. While the tubules in the upper part of the field show active spermatogenesis, the remaining tubules contain largely Sertoli cells only (x 200), 1. Simmons FA: Human infertility. N Engl J Med 255:1140, MacLeod J: Human male infertility. Obstet Gynecol Survey 26:5, Reame NE, Hafez ESE: Hereditary defects affecting fertility. N Engl J Med 292:675, Charny CW: Testicular biopsy. JAMA 115:1429, Charny CW: Reflections on testicular biopsy. Fertil Steril 14:610, 196

5 60 COLGAN ET AL. 6. Meinhard E, McRae CU, Chisholm GD: Testicular biopsy in evaluation of male infertility. Br Med J :577, Hargreave TB, Jequier AM: Can follicle stimulating hormone estimation replace testicular biopsy in the diagnosis of obstructive azoospermia? Br J Urol 50:415, Posinovec J: The necessity for bilateral biopsy in oligo- and azoospermia. Int J Fertil 21:189, Skakkebaek NE: Seminiferous tubules in the adult human testis. In Pathology of the Testis, Edited by RCB Pugh. London, Blackwell Scientific Publications, 1976, p Wong T, Straus FH, Warner NE: Testicular biopsy in the study of male infertility. Arch Pathol Lab Med 95:151, Sniffen RC, Howard RP, Simmons FA: The testis. II. Abnormalities of spermatogenesis: atresia of the excretory ducts. Arch Pathol Lab Med 50:285, 1950 January Nelson WO: Interpretation of testicular biopsy. JAMA 151:449, Franchimont P, Millet D, Vendrely E, Letawe J, Legros JJ, Netter A: Relationship between spermatogenesis and serum gonadotropin levels in azoospermia and oligospermia. J Clin Endocrinol Metab 4:100, Cunningham GR: Medical treatment of the subfertile male. Urol Clin North Am 5:56, Aatjes JH, van der Vijver JCM, Schenck PE: Value of testicular biopsy rating for prognosis in oligozoospermia. Br Med J 1:289, Paulsen CA, Plymate SR, Leonard JM: Current concepts in the management of male infertility. In The Testis in Normal and Infertile Men. Edited by P Troen, HR Nankin. New York, Raven Press, 1977, p 49

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