ORIGINAL ARTICLE. V. Mitchell,* G. Robin, à F. Boitrelle, P. Massart, C. Marchetti, F. Marcelli and J.-M. Rigot. Summary

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1 international journal of andrology ISSN ORIGINAL ARTICLE Correlation between testicular sperm extraction outcomes and clinical, endocrine and testicular histology parameters in 120 azoospermic men with normal serum FSH levels V. Mitchell,* G. Robin, à F. Boitrelle, P. Massart, C. Marchetti, F. Marcelli and J.-M. Rigot *Laboratoire de Spermiologie, Service d Andrologie, Hôpital A. Calmette, EA 4308 Spermatogenesis and Male Gamete Quality, àservice de Médecine de la Reproduction, Hôpital Jeanne-de-Flandre, and Biologie de la Reproduction, Hôpital Jeanne-de-Flandre, CHRU Lille, France Summary Keywords: azoospermia, follicle-stimulating hormone, inhibin B, testicular sperm extraction Correspondence: Valérie Mitchell, Laboratoire de Spermiologie, Hôpital A. Calmette, CHRU Lille, Cedex F-59037, France. valerie-mitchell@chru-lille.fr Received 11 February 2010; revised 4 May and 3 June 2010; accepted 7 June 2010 doi: /j x We retrospectively evaluated the clinical and hormonal profiles, sperm extraction outcomes and testicular histology parameters in 120 azoospermic men with normal serum follicle-stimulating hormone (FSH) level. Microsurgical epididymal sperm aspiration (MESA) and testicular sperm extraction (TESE) were performed in 33 and 87 cases, respectively. Sperm were successfully retrieved in all the MESA procedures and in 65 of the TESE procedures. The mean serum FSH and inhibin B levels and the testicular volume differed significantly according to whether or not sperm were retrieved. The threshold serum inhibin B value for predicting successful TESE was pg ml (sensitivity: 69.7%; specificity: 66.7%). The 13 patients with Sertoli cell only syndrome (SCOS) had a higher mean serum FSH level and a lower mean serum inhibin B level than the other phenotypes. TESE was negative for 11 of the 13 SCOS men. The mean ± SD inhibin B level was significantly lower in patients with 5 10 IU L of FSH than those with 2 5 IU L of FSH ( ± vs ± pg ml, respectively). The sperm retrieval rates were 71.42% for the group with 5 10 IU L of FSH and 87.32% for the group with 2 5 IU Lof FSH. Ten of the 13 SCOS men had a FSH level between 5 and 10 IU L. The clinical pregnancy rate was significantly lower (p = 0.04) in the group with 5 10 IU L (50%) of FSH than in the group with 2 5 IU L (77.5%) of FSH. In conclusion, there is no FSH value below which spermatogenesis is always found. Inhibin B assays and clinical assessments are thus of particular value in men with normal serum FSH levels. Introduction In the workup of azoospermia, thorough physical examinations, ultrasound investigations, semen analysis and plasma hormone measurements are essential. The serum level of follicle-stimulating hormone (FSH) is an important endocrine parameter in the evaluation of male infertility (Nieschlag, 1993; Bergmann et al., 1994; Bourcigaux & Christin-Maître, 2008); it serves as a useful index of the state of the seminiferous epithelium (de Kretser, 1979) and discriminates between testicular impairment of spermatogenesis (i.e. secretory azoospermia) and obstructive disorders (Behre et al., 1997). Azoospermic men with normal-sized testes and normal serum FSH concentrations are typically classified as suffering from obstructive azoospermia. In such cases, one can expect to retrieve adequate numbers of sperm by either microsurgical epididymal sperm aspiration (MESA) or testicular sperm extraction (TESE; Bromage et al., 2007). To date, most evaluations of azoospermia have been performed in non-obstructive men with elevated FSH levels (Chen et al., 1996; Ezeh et al., 1998; Jezek et al., 1998; Foresta et al., 1999) or in men with a primary obstruction (Nistal et al., 1999; Bromage et al., 2007; Smit et al., 2007). Given that azoospermic men with normal FSH levels have generally been pooled with men displaying elevated FSH levels (Bergmann et al., 1994; Bohring & Krause, 1999; von Eckardstein et al., 1999; Zitzmann et al., 2006; Bromage et al., 2007; Goulis et al., 2008, 2009), we thought that it would be of value to evaluate International Journal of Andrology ª 2010 European Academy of Andrology, 34,

2 Normal serum FSH level and sperm extraction V. Mitchell et al. the former group in isolation. Hence, we examined the clinical profiles, hormonal parameters, MESA and TESE success rates and testicular histology phenotypes in a large, well-characterized group of azoospermic patients with normal serum FSH seen in our andrology centre between 2003 and Materials and methods Subjects We retrospectively analysed the medical records of 120 men with azoospermia (regardless of the aetiology) and serum FSH levels defined as 2 10 IU L. All the subjects had been thoroughly evaluated in our andrology clinic between 2003 and 2008 [with an investigation of the patient s medical history, a physical examination, three semen analyses and serum FSH, inhibin B, testosterone and luteinizing hormone (LH) assays]. The testicular volume (defined here as sum of the two testis volumes) was calculated following ultrasound examination of the genital tract. Surgical sperm extraction MESA was performed only in men whose epididymis was distended (n = 33), whereas TESE was preferred in the other 87 cases. The MESA procedure was performed under general anaesthesia with a 25-gauge needle and a syringe containing 0.5 ml of sperm preparation medium (Medicult, Limonest, France). The needle was inserted (up to four times per side) into the head of the epididymis. The aspirate was drawn through the needle into a sterile plastic tube and examined immediately for the presence of spermatozoa. Straws were frozen in Sperm- Freeze medium (Fertipro NV, Beernem, Belgium). For TESE, a single, large biopsy was taken in a transverse scrototomy procedure. Testicular biopsies were immersed in Ferticult culture medium (FertiPro NV) in a Petri dish (BD Biosciences, Erembodegem-Aalst, Belgium) and sent to the reproductive biology laboratory for TESE. Sperm were extracted after mincing and shredding the testicular tissue in culture medium with two scalpels. An aliquot was examined under an inverted microscope (DM IRB Microscope; Hoffman Optics, Leica, Germany) at 400 magnification. The TESE outcome was interpreted as positive or negative, according to the presence or absence of spermatozoa, respectively. Testicular biopsies for histological evaluation In addition to the biopsy for TESE, a second testicular sample for histological examination was immediately immersed in Bouin s solution and fixed for 48 h. Serial sections were prepared from paraffin blocks and stained with haematoxylin-eosin-green FCF. At least one section showing the most seminiferous tubules was used for histological evaluation. The sample was qualitatively classified as having one of the following spermatogenic phenotypes: Sertoli cell only syndrome (SCOS, i.e. all tubules lacked germ cells and were lined with Sertoli cells), normal spermatogenesis (i.e. cells from all stages of spermatogenesis and an adequate number of elongated spermatids spermatozoa), hypospermatogenesis (i.e. a uniform reduction in spermatid number) or germ cell arrest (i.e. no progression past the spermatocyte or round spermatid stage). Thus, spermatogenesis cells are present in three of the phenotypes (normal spermatogenesis, hypospermatogenesis and germ cell arrest) and absent in one (SCOS). Hormone analysis Serum FSH and LH levels were determined in an immunoassay with a limit of detection of 0.05 IU L and intraand interassay coefficients of variation of <3% and <5%, respectively. The reference range was 2 10 IU L for serum FSH and 2 12 IU L for serum LH. Serum testosterone was measured by radioimmunoassay. The normal range was taken as ng ml. Serum inhibin B levels were measured using the two-site OBI Inhibin B enzyme immunoassay manufactured by Oxford Bio-Innovation Ltd (Oxford, UK) and distributed by Diagnostic Systems Laboratories Beckman Coulter (Villepinte, France). To improve the measurement range, an additional reference point (7.8 pg ml) was added to the standard curve. The mean normal serum inhibin B concentration was considered to be 238 ± 32 pg ml. Statistical analysis All statistical analyses were carried out with sas software, version 9.1 (SAS Institute Inc., Cary, NC, USA). Descriptive data were recorded at baseline for the 120 included patients. The data were presented using descriptive statistics [number, mean, standard deviation (SD), minimum and maximum]. Differences between mean values were assessed in a Kruskal Wallis test and a Student s t-test. Comparison of intracytoplasmic sperm injection (ICSI) outcome variables was performed with a Chi-squared test. Each parameter s value for predicting the presence of testicular spermatozoa was analysed in a logistic regression model. In all analyses, the threshold for statistical significance was set at p < The area under the receiver operating characteristic (ROC) curve was used to assess the predictive accuracy of selected parameters for the likelihood of retrieving sperm (with a value of International Journal of Andrology ª 2010 European Academy of Andrology, 34,

3 V. Mitchell et al. Normal serum FSH level and sperm extraction indicating no predictive power and 1.0 indicating perfect prediction). Results The mean age of the study population was 34.3 years (range: years). Various aetiologies of male infertility were presented: 10 men had congenital, bilateral absence of the vas deferens (CBAVD), 5 had a history of inguinal hernia, 19 had a history of maldescended testes and 8 had a history of varicocele or chemotherapy. The aetiology could not be unambiguously determined for 78 of the 120 men. The latter were therefore classified as having idiopathic azoospermia. All the 33 MESA procedures (100%) retrieved adequate sperm for ICSI. Sixtyfive of the 87 TESE procedures (74.7%) were successful (Table 1). Overall, 98 (81.66%) patients had adequate sperm retrieval for ICSI. The mean serum FSH level was 4.99 IU L. Patients with successful sperm retrieval differed significantly from the group with no sperm retrieval in terms of the mean serum FSH, inhibin B levels and total testicular volume (4.97 ± 2.10 IU ml vs ± 2.05 IU ml; ± pg ml vs ± pg ml; ± 8.38 ml vs ± 5.52 ml, respectively). Testosterone and LH values did not differ significantly between the two groups. After construction of an ROC curve, we found that the area under the curve (AUC) for inhibin B was The best inhibin B threshold value for predicting the success or failure of TESE was pg ml (sensitivity: 69.7%; specificity: 66.7%). The area under the ROC curve for the serum inhibin B FSH ratio was (sensitivity: 79.8%; specificity: 61.7%). Of the 120 patients, 45 (37.5%) had a total testicular volume below the 30 ml threshold and were considered to be partly non-obstructive. The mean FSH level in this group was not significantly different from that in the group of men with a normal testicular volume (5.09 ± 2.07 vs ± 2.09 IU L, respectively). The mean inhibin B level in men with a testicular volume below 30 ml was significantly lower ( ± pg ml) than in the group with a normal testicular volume ( ± pg ml). Germ cell development was observed in 74 of the 87 men having undergone open testicular biopsies (Table 2): 13 patients (14.9%) showed characteristics of SCOS, 43 men showed normal spermatogenesis (49.5%), 20 had hypospermatogenesis (23%) and germ cell arrest was recorded in 11 cases (12.6%). The mean serum FSH level was significantly higher in SCOS patients (6.81 ± 1.59 IU L) than in patients with other histological phenotypes. Furthermore, the mean serum inhibin B level was significantly lower in SCOS patients (93.92 ± pg ml) than in other histological phenotypes. Testicular volume did not appear to be correlated with the histology results. In SCOS, the probability of a negative TESE outcome was very high (11 of 13 cases: 84.62%). For predicting the success or failure of TESE, the best sensitivity (61%) and specificity (64%) were observed Table 1 Patient characteristics as a function of the success or failure of testicular sperm extraction (TESE) Patients (n = 120) Successful TESE (n = 65) Unsuccessful TESE (n = 22) Kruskal Wallis test (p) Follicle-stimulating hormone (IU L) 4.99 ± ± ± Serum inhibin B (pg ml) ± ± ± Serum testosterone (ng ml) 4.41 ± ± ± Serum LH (IU L) 3.40 ± ± ± Total testicular volume (ml) ± ± ± Table 2 Patient characteristics as a function of the histological phenotype Patients (n = 87) Sertoli cell only syndrome (n = 13) Normal spermatogenesis (n = 43) Hypospermatogenesis (n = 20) Germ cell arrest (n = 11) Kruskal Wallis test (p) Follicle-stimulating hormone (IU L) 6.81 ± ± ± ± Serum inhibin B (pg ml) ± ± ± ± Serum testosterone (ng ml) 4.4 ± ± ± ± Luteinizing hormone (IU L) 4.12 ± ± ± ± Total testicular volume (ml) ± ± ± ± Successful testicular sperm extraction, n =65 2 (15.38%) 43 (100%) 20 (100%) 0 (0%) International Journal of Andrology ª 2010 European Academy of Andrology, 34,

4 Normal serum FSH level and sperm extraction V. Mitchell et al. Table 3 Endocrine status, testicular volume and sperm retrieval as a function of follicle-stimulating hormone (FSH) levels FSH (IU L) Student s t-test (p) Patients, n = (59.1%) 49 (40.9%) FSH (IU L) 3.71 ± ± 1.31 Serum inhibin B (pg ml) ± ± < Serum testosterone (ng ml) 4.45 ± ± Serum luteinizing hormone (IU L) 3.78 ± ± 1.37 Total testicular volume (ml) ± ± Successful sperm retrieval 62 (87.32%) 35 (71.42%) Successful testicular sperm extraction 39 (84.78%) 26 (63.41%) with an FSH threshold value of 5 IU L (AUC: 0.650). We then grouped the patients according to whether their serum FSH concentration was above or below this cut-off (Table 3). In patients with 5 10 IU L of FSH, the serum inhibin B level ( ± pg ml) was significantly lower than in patients with 2 5 IU L ( ± pg ml) of FSH. The area under the ROC curve for inhibin B in men with serum FSH of 2 5 IU L was (sensitivity: 54.4%; specificity: 66.7%), whereas that in men with FSH of 5 10 IU L was (sensitivity: 71.9%; specificity: 66.7%). The best inhibin B threshold values for predicting the success or failure of TESE in each of the two groups were and 101 pg ml, respectively. The FSH-stratified groups differed significantly in terms of sperm retrieval rates, with 87.32% for 2 5 IU L and 71.42% for 5 10 IU L (Table 4). Ten of the 13 SCOS men had serum FSH levels of 5 10 IU L. Eight of the 11 men with germ cell arrest had serum FSH levels of 2 5 IU L. The outcomes of ICSI treatment cycles are shown in Table 4. The couples in the FSH 2 5 and 5 10 groups underwent a total of 41 and 26 ICSI treatment cycles, respectively, with corresponding mean fertilization rates Table 4 Comparison of intracytoplasmic sperm injection outcome variables according to the follicle-stimulating hormone (FSH) level FSH (IU L) Chi-squared test (p) Couples n =41 n =26 Cycles n =91 n =67 Injected oocytes (mean number) Fertilization rate (%) Embryo transfers n = 79 n = 61 Implantation rate (%) Biochemical pregnancy (%) Abortion rate (%) Clinical pregnancy (%) Live birth rate (%) of 56.1 and 54.4%. The FSH groups did not differ significantly in terms of the mean implantation rate (20.6 and 14.8, respectively). The clinical pregnancy rate was significantly higher (p = 0.04) in the group of men with 2 5 IU L FSH (77.5%) than in the group with 5 10 IU L FSH (50%). Although the live birth rate was higher in the 2 5 IU L group than in the 5 10 IU L group (60% vs. 46.1%, respectively), this difference was not statistically significant (p = 0.394). In each of the two groups, one pregnancy turned out to be biochemical. Four women in the FSH 2 5 IU L group and two women in the FSH 5 10 IU L group suffered a spontaneous abortion during the first trimester. Discussion To the best of our knowledge, this is the first study to have solely analysed a large sample of azoospermic patients with normal serum FSH levels. Surprisingly, an obstructive cause of azoospermia was confirmed in only 35% of the men. The definition of obstructive azoospermia is clear-cut in clinical terms: normal FSH levels and a normal testicular volume. For most of the men of our series, these criteria were not fulfilled. The frequently observed testicular hypotrophy suggested testicular failure in a population of azoospermic men in whom normal spermatogenesis was expected. Hence, not all azoospermic patients with normal FSH levels should be classified as having an obstructive disorder. It is generally acknowledged that plasma FSH values below 10 IU L are associated with a good likelihood of finding sperm. When an obstructive aetiology is obvious (such as in CBAVD or following a vasectomy), sperm retrieval rates of close to 100% are typically reported. However, when there are no clinical findings to suggest obstruction, the sperm retrieval rate remains variable. Even after thorough clinical and endocrine screening, some cases cannot be accurately categorized. Accordingly, these patients should receive counselling on testicular biopsies. 302 International Journal of Andrology ª 2010 European Academy of Andrology, 34,

5 V. Mitchell et al. Normal serum FSH level and sperm extraction In the event of an obstructive defect, sperm is generally retrievable from the epididymis. However, MESA has a limited success rate (about 13%; Berardinucci et al., 1998; Smit et al., 2007). In our series of patients with normal FSH levels and in line with our physicians experience and preferences, MESA was only offered to men presenting a well-defined cause of obstruction, a distended epididymis and a normal testicular volume. In TESE, a single, large biopsy was preferred to multiple, small samples. The mean sperm retrieval rate was 81.66%. This finding demonstrates that sperm retrieval can be unsuccessful in nearly 20% of men with normal preoperative FSH levels, even when large and bilateral testicular biopsies are performed. In our study, successful testicular sperm retrieval was less likely in men with 5 10 IU L FSH levels than in men with FSH levels below 5 IU L. Our results did not corroborate those reported by Jezek et al. (1998), who found that TESE was successful in 96.2% of azoospermic patients with normal FSH levels. However, most of Jezek et al. s patients were suffering from well-defined obstructive azoospermia (unlike those in our series). Our results raise the question of (i) Why spermatozoa may not always be found in samples from men with normal FSH concentration? and (ii) Why sometimes severe abnormalities in spermatogenesis can be observed in these patients? In the 87 men having undergone TESE, we found 13 cases with SCOS and no evidence of spermatogenesis. This suggests that FSH may not be a perfect marker for spermatogenesis. Inhibin B levels in these 13 men were significantly lower than in histological phenotypes with spermatogenic cells suggesting that inhibin B might be a good marker for spermatogenesis. It is probable that certain aetiologies accounted for the observed defects in spermatogenesis. These notably include chronic obstruction and testicular causes (varicocele, etc.). The absence of sperm may result from intratesticular blockade or non-functional seminiferous tubules and thus an absence of sperm in the epididymis. Spermatogenesis was defective for 50.6% of the men in our series and no spermatogenesis was detected in 14.9% of the testicular biopsies. Hendry et al. (1990) reported the presence of defective spermatogenesis in 9.5% of patients with normal FSH levels and suspected obstructive azoospermia. Furthermore, normal FSH levels may not rule out complete SCOS. According to Bergmann et al. (1994), 13% of azoospermic patients with bilateral, complete SCOS have FSH levels below 7 IU L. Thus, FSH is an important but not perfectly discriminant indicator of testicular morphology and must therefore be interpreted with caution. Our results concord with other studies in which testicular histology was predictive of successful testicular biopsy and sperm extraction in infertile, azoospermic patients even when FSH levels were not elevated (Tournaye et al., 1997; Schoor et al., 2002). However, the testicular histology can only be determined after TESE and so should not really be considered as a predictive parameter. There was significant heterogeneity in FSH concentrations in an azoospermic group with a SCOS phenotype, irrespective of the presence or absence of spermatozoa in the wet preparation (Tournaye et al., 1997). This heterogeneity probably explains the FSH level s low predictive value for successful testicular sperm recovery. Moreover, it should not be assumed that patients with normal FSH levels and a histopathological SCOS phenotype will have a below-average testicular volume. Likewise, testicular volume is variable, with a significant distribution overlap between populations with and without spermatozoa in the wet preparation (Tournaye et al., 1997). Thus, high testicular volume and normal serum FSH levels do not guarantee successful testicular sperm recovery in patients with a histopathological SCOS phenotype. It is well accepted that all azoospermic men should undergo comprehensive endocrine and clinical testing. The initial check-up must include plasma FSH and total testosterone assays. The FSH assay is simple and reproducible. Depending on the study in question, serum FSH levels in fertile men vary from 1.3 to 7.6 or 8.4 IU L (Schoor et al., 2002; Sikaris et al., 2005). The FSH reference range in our andrology centre has long been set at between 2 and 10 IU L. It is generally admitted that a normal serum FSH concentration does not exclude mildto-severe impairment of spermatogenesis or even SCOS in individual cases (Bergmann et al., 1994). Thus, FSH is an important, but not absolutely discriminant, indicator of testicular morphology and should be interpreted with caution and in the light of other fertility parameters. Schematically, a normal FSH level in azoospermia generally suggests an obstructive profile for which a congenital or acquired obstructive cause has to be identified. In azoospermic men, an FSH level >7.6 IU L and testicular length <4.5 cm predict non-obstructive azoospermia with >89% probability (Schoor et al., 2002). Other literature reports (von Eckardstein et al., 1999; Foresta et al., 1999) suggest that both inhibin B and FSH can be within the normal range and inconsistent with testicular histology. In recent years, several studies have identified inhibin B (released by Sertoli cells) levels in serum as a diagnostic marker for the quality of spermatogenesis (von Eckardstein et al., 1999). It has been suggested that an inhibin B assay can augment the value of serum FSH concentrations when making a non-invasive diagnosis of spermatogenesis (Pierik et al., 1998; Bohring et al., 2002). A review of the reports published to date shows that the validity of serum inhibin B as a predictor of sperm recovery in azoospermia International Journal of Andrology ª 2010 European Academy of Andrology, 34,

6 Normal serum FSH level and sperm extraction V. Mitchell et al. is subject to debate (von Eckardstein et al., 1999; Ballescá et al., 2000; Brugo-Olmedo et al., 2001; Vernaeve et al., 2002; Bailly et al., 2003). In our population, the area under the ROC curve for inhibin B (0.703) did not indicate perfect prediction. Nevertheless, the best inhibin B concentration for discriminating between successful and unsuccessful TESE in azoospermic men with normal plasma FSH was pg ml (sensitivity: 69.7%; specificity: 66.7%). In our population, the serum inhibin B level seems to be an indicator of spermatogenic function. It is also a predictor of sperm recovery in patients with normal FSH levels. Finally, the inhibin B FSH ratio did not yield higher sensitivity and specificity than inhibin B alone. Conclusion Of the 120 azoospermic patients with normal FSH levels evaluated in our centre, 50.6% had defective spermatogenesis, 9.1% had a total absence of germ cells and 35% had an obstructive profile. This study highlighted difficulties in classifying azoospermic men and a high proportion of the study subjects were classified as having idiopathic azoospermia (i.e. of unknown aetiology). Although azoospermia with normal FSH levels and a normal testicular volume suggests obstruction of the genital tract, normal FSH levels do not always rule out the presence of defects in spermatogenesis. In men with normal FSH levels, the serum inhibin B assay and a clinical evaluation might identify the outcome of sperm extraction and provision of associated counselling. Hence, one should not assume that azoospermic men with non-elevated FSH concentrations will have uniformly normal spermatogenesis and successful sperm extraction outcomes. There is no serum FSH level below which spermatogenesis can be reliably found, as shown by a patient in our series who had an SCOS phenotype and no viable spermatozoa after attempted TESE, despite an FSH concentration of 2.5 IU L. Acknowledgements The authors thank N. Sebbane at Lille 2 University for statistical analysis of the results. The study was funded by grants from the Interregional G4 Collaboration on Reproduction (Amiens, Caen, Rouen and Lille University Hospitals), Lille University Hospital (PHRC 2004 R-1908), the French Language Society for Andrology (SALF), the GRAL Andrology Research Group, the French Agency for Biomedicine (ABM) and the Fonds d Aide à la Recherche Organon (FARO, Laboratoires Organon, France). References Bailly M, Guthauser B, Bergere M, Wainer R, Lombroso R, Ville Y & Selva J. (2003) Effects of low concentrations of inhibin B on the outcomes of testicular sperm extraction and intracytoplasmic sperm injection. Fertil Steril 79, Ballescá JL, Balasch J, Calafell JM, Alvarez R, Fábregues F, de Osaba MJ, Ascaso C & Vanrell JA. (2000) Serum inhibin B determination is predictive of successful testicular sperm extraction in men with non-obstructive azoospermia. Hum Reprod 15, Behre HM, Yeung CH & Nieschlag E. (1997) Diagnosis of male infertility and hypogonadism. In: Andrology: Male Reproductive Health and Dysfunction (eds E Nieshlag & HM Behre), pp Springer, Heidelberg. Berardinucci D, Zini A & Jarvi K. (1998) Outcome of microsurgical reconstruction in men with suspected epididymal obstruction. J Urol 159, Bergmann M, Behre HM & Nieschlag E. (1994) Serum FSH and testicular morphology in male infertility. Clin Endocrinol 40, Bohring C & Krause W. (1999) Serum levels of inhibin B in men with different causes of spermatogenic failure. Andrologia 31, Bohring C, Schroeder-Printzen I, Weidner W & Krause W. (2002) Serum levels of inhibin B and follicle-stimulating hormone may predict successful sperm retrieval in men with azoospermia who are undergoing testicular sperm extraction. Fertil Steril 78, Bourcigaux N & Christin-Maître S. (2008) Hormonal evaluation in infertile men. Gyn Obst Fertil 36, Bromage SJ, Falconer DA, Lieberman BA, Sangar V & Payne SR. (2007) Sperm retrieval rates in subgroups of primary azoospermic males. Eur Urol 51, Brugo-Olmedo S, De Vincentiis S, Calamera JC, Urrutia F, Nodar F & Acosta AA. (2001) Serum inhibin B may be a reliable marker of the presence of testicular spermatozoa in patients with nonobstructive azoospermia. Fertil Steril 76, Chen CS, Chu SH, Lai YM, Wang ML & Chan PR. (1996) Reconsideration of testicular biopsy and follicle-stimulating hormone measurement in the era of intracytoplasmic sperm injection for nonobstructive azoospermia? Hum Reprod 11, von Eckardstein S, Simoni M, Bergmann M, Weinbauer GF, Gassner P, Schepers AG & Nieschlag E. (1999) Serum inhibin B in combination with serum follicle-stimulating hormone (FSH) is a more sensitive marker than serum FSH alone for impaired spermatogenesis in men, but cannot predict the presence of sperm in testicular tissue samples. J Clin Endocrinol Metab 84, Ezeh UI, Moore HD & Cooke ID. (1998) A prospective study of multiple needle biopsies versus a single open biopsy for testicular sperm extraction in men with non-obstructive azoospermia. Hum Reprod 13, Foresta C, Bettella A, Petraglia F, Pistorello M, Luisi S & Rossato M. (1999) Inhibin B levels in azoospermic subjects with cytologically characterized testicular pathology. Clin Endocrinol 50, Goulis DG, Polychronou P, Mikos T, Grimbizis G, Gerou S, Pavlidou V, Papanikolaou A, Tarlatzis BC, Bontis IN & Papadimas I. (2008) Serum inhibin-b and follicle stimulating hormone as predictors of the presence of sperm in testicular fine needle aspirate in men with azoospermia. Hormones 7, Goulis DG, Tsametis C, Iliadou PK, Polychronou P, Kantartzi PD, Tarlatzis BC, Bontis IN & Papadimas I. (2009) Serum inhibin B and anti-müllerian hormone are not superior to follicle-stimulating hormone as predictors of the presence of sperm in testicular fine-needle aspiration in men with azoospermia. Fertil Steril 91, Hendry WF, Levison DA, Parkinson JM, Parslow JM & Royle MG. (1990) Testicular obstruction: clinicopathological studies. Ann R Coll Surg Engl 72, International Journal of Andrology ª 2010 European Academy of Andrology, 34,

7 V. Mitchell et al. Normal serum FSH level and sperm extraction Jezek D, Knuth UA & Schulze W. (1998) Successful testicular sperm extraction (TESE) in spite of high serum follicle stimulating hormone and azoospermia: correlation between testicular morphology, TESE results, semen analysis and serum hormone values in 103 infertile men. Hum Reprod 13, de Kretser DM. (1979) Endocrinology of male infertility. Br Med Bull 35, Nieschlag E. (1993) Care for the infertile male. Clin Endocrinol 38, Nistal M, Riestra ML, Galmés-Belmonte I & Paniagua R. (1999) Testicular biopsy in patients with obstructive azoospermia. Am J Surg Pathol 23, Pierik FH, Vreeburg JT, Stijnen T, De Jong FH & Weber RF. (1998) Serum inhibin B as a marker of spermatogenesis. J Clin Endocrinol Metab 83, Schoor RA, Elhanbly S, Niederberger CS & Ross LS. (2002) The role of testicular biopsy in the modern management of male infertility. J Urol 67, Sikaris K, McLachlan RI, Kazlauskas R, de Kretser D, Holden CA & Handelsman DJ. (2005) Reproductive hormone reference intervals for healthy fertile young men: evaluation of automated platform assays. J Clin Endocrinol Metab 90, Smit M, Dohle GR, Wildhagen MF & Weber RF. (2007) Can inhibin-b predict the outcome of microsurgical epididymal sperm aspiration in patients with suspected primary obstructive azoospermia. Asian J Androl 9, Tournaye H, Verheyen G, Nagy P, Ubaldi F, Goossens A, Silber S, Van Steirteghem AC & Devroey P. (1997) Are there any predictive factors for successful testicular sperm recovery in azoospermic patients? Hum Reprod 12, Vernaeve V, Tournaye H, Schiettecatte J, Verheyen G, Van Steirteghem A & Devroey P. (2002) Serum inhibin B cannot predict testicular sperm retrieval in patients with non-obstructive azoospermia. Hum Reprod 17, Zitzmann M, Nordhoff V, von Schönfeld V, Nordsiek-Mengede A, Kliesch S, Schüring AN et al. (2006) Elevated follicle-stimulating hormone levels and the chances for azoospermic men to become fathers after retrieval of elongated spermatids from cryopreserved testicular tissue. Fertil Steril 86, International Journal of Andrology ª 2010 European Academy of Andrology, 34,

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