Treatment of male idiopathic infertility with recombinant human follicle-stimulating hormone: a prospective, controlled, randomized clinical study
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1 Treatment of male idiopathic infertility with recombinant human follicle-stimulating hormone: a prospective, controlled, randomized clinical study Carlo Foresta, M.D., Ph.D., a Andrea Bettella, M.D., Ph.D., a Andrea Garolla, M.D., Ph.D., a Guido Ambrosini, M.D., Ph.D., b and Alberto Ferlin, M.D., Ph.D. a a Centre for Male Gamete Cryopreservation, Department of Histology, Microbiology, and Medical Biotechnologies, and b Department of Gynecological and Human Reproduction Sciences, University of Padova, Padova, Italy Objective: To evaluate the effects of treatment with FSH on seminal parameters and spontaneous pregnancy in male infertility. Design: Prospective, controlled, randomized clinical study. Setting: Infertility center at a university hospital. Patient(s): One hundred twelve men affected by idiopathic oligozoospermia. Intervention(s): Patients were randomized into two groups: 62 subjects were treated with 100 IU of recombinant human FSH on alternate days for 3 months, and 50 patients did not receive any treatment. Semen analysis was performed in all subjects at the end of this period of treatment and after the following 3 months. Subjects who had not reached spontaneous pregnancy underwent assisted reproductive techniques. Main Outcome Measure(s): Seminal parameters, testicular cytologic analysis, FSH, LH, T, and inhibin B concentrations. Result(s): The treatment group considered as a whole did not show modifications in sperm parameters. However, a subgroup of these (30, 48.4%) had a significant increase of sperm count (responder group). In the period including 3 months after the withdrawal of FSH therapy, we observed a significantly higher spontaneous pregnancy rate in the responder group (5 of 30 [16.7%]) with respect to nonresponder and nontreated groups (1 of 32 [3.1%] and 2 of 50 [4.0%], respectively). Furthermore, the improvement of seminal parameters in the responder group allowed these patients to undergo less frequent IVF-ET/intracytoplasmic sperm injection. Conclusion(s): Results from this controlled, randomized clinical trial show that FSH therapy does not improve sperm concentration or pregnancy rate when infertile male patients are chosen solely by the clinical criteria of idiopathic oligospermia and normal FSH concentration. Subgroup analysis, however, does indicate that patients without maturation arrest in addition to the clinical scenario do benefit from medical therapy. (Fertil Steril 2005; 84: by American Society for Reproductive Medicine.) Key Words: Male infertility, FSH therapy, idiopathic oligozoospermia Follicle-stimulating hormone plays a crucial role in spermatogenesis (1, 2), and several experimental and clinical studies have demonstrated the importance of this hormone in regulating a normal quantitative spermatogenic process in animals and humans (3 7). Because of this physiologic role of FSH in spermatogenesis, various attempts have been made to treat idiopathic oligozoospermic subjects with this hormone. However, the results obtained so far are still controversial. In particular, several uncontrolled studies have shown an improvement of seminal parameters and/or an increase of pregnancy rates in infertile men treated with different doses of FSH (8 12). Nevertheless, these results have not been confirmed in randomized controlled studies. Only two randomized controlled clinical studies have been performed using both highly purified FSH and recombinant human FSH Received September 28, 2004; revised and accepted March 15, Reprint requests: Carlo Foresta, University of Padova, Department of Histology, Microbiology, and Medical Biotechnologies, Centre for Male Gamete Cryopreservation, Via Gabelli, 63, Padova 35121, Italy (FAX: ; carlo.foresta@unipd.it). (hfsh), and they did not show any improvement of seminal parameters or a significant increase in pregnancy rates in infertile men receiving the treatment compared with those receiving no treatment or placebo (13, 14). Controlled trials are crucial to evaluate the effectiveness of a novel therapeutic protocol, but this evaluation is extremely difficult in the setting of male infertility. In fact, fertility of a man should actually be considered in the setting of the fertility of the couple, and it is not always evident only from the man s semen analysis, with the exception of azoospermia or severe oligozoospermia. Furthermore, a reduction of sperm number in the ejaculate might be caused by different etiologies and might be related to different kinds of tubular disease, such as hypospermatogenesis or maturation arrest at different levels of spermatogenesis. These considerations should be kept in mind when recruiting infertile or oligozoospermic men as a whole to study the effectiveness of a therapeutic protocol. Recently, we demonstrated that FSH (highly purified FSH and recombinant hfsh) could be an appropriate and valid 654 Fertility and Sterility Vol. 84, No. 3, September /05/$30.00 Copyright 2005 American Society for Reproductive Medicine, Published by Elsevier Inc. doi: /j.fertnstert
2 treatment of oligozoospermic patients only when FSH and inhibin B plasma levels are in the normal range and the testicular tubular structure is characterized by hypospermatogenesis without germ cell maturation disturbances (15 18). No efficacy of FSH treatment is seen either when FSH plasma concentrations are higher than normal or when spermatogenic arrest is present. These preliminary studies were conducted primarily to verify the effectiveness of this therapy in male infertility and with particular attention to the criteria able to select appropriate clinical conditions predicting a seminal response to this specific hormonal treatment. Here, we better clarified the effectiveness of FSH therapy on sperm count and pregnancy rate by means of a prospective, controlled, randomized clinical study in a selected group of patients affected by idiopathic oligozoospermia. MATERIALS AND METHODS Our study was approved by the ethics committee of the University of Padova, and informed consent was obtained from each subject. All phases of the study were performed at the Infertility Centre of the University of Padova. All men were informed about the protocol of treatment and in particular about the different phases of the design of the study and about the possibility of undergoing assisted reproductive techniques (ARTs) during this period. Inclusion criteria were [1] a history of infertility for at least 2 years, [2] sperm count /ml on at least three separate occasions, according to World Health Organization guidelines (19), [3] idiopathic infertility with exclusion of common conditions, such as history of cryptorchidism, postmumps orchitis, testicular torsion or trauma, varicocele, seminal tract infections, antisperm antibodies and Y chromosome microdeletions, karyotypic abnormalities, and CFTR gene mutations, [4] normal plasma levels of FSH (range, 1 7 IU/L), LH (range, 2 6 IU/L), PRL (range, ng/ml), T (range 3 9 ng/ml), and inhibin B ( 150 pg/ml), and [5] exclusion of clear female factors, such as ovulatory disorders, tubal factor, and endocrine abnormalities as evaluated by endocrine evaluation, pelvic ultrasound examination, and hysterosalpingography. A total of 128 patients fulfilled the inclusion criteria and were enrolled in the study. Patients were randomly allocated to treatment or nontreatment groups in a blinded fashion by third-party true randomization in a 1:1 ratio with a random number generator. Sixty-five men were allocated to the treatment group and 63 to the nontreatment group. Of these, 6 couples (2 from the treatment group and 4 from the nontreatment group) were subsequently excluded from the study because of concurrent illnesses. Ten subjects (1 from the treatment group and 9 from the nontreatment group) dropped out before completing the study: 2 in the nontreatment group were lost, 7 in the nontreatment group dropped out by the patient s request, and 1 in the treatment group discontinued intervention. Therefore, 112 men affected by idiopathic oligozoospermia completed the study (62 in the treatment group and 50 in the nontreatment group), were analyzed, and are described here. There were no significant differences between the groups in the clinical characteristics that we assessed. The testicular structure was analyzed in all patients by means of bilateral fine needle aspiration cytology (FNAC) (20 22), to evaluate the tubular status related to the oligozoospermia. The methods of aspiration and cytologic analysis have been described previously in detail (20 22). Briefly, testicular aspiration is a simple procedure performed with a 23-gauge (0.6-mm) butterfly needle attached to a 20-mL syringe. The retrieved material is placed on two or more microscope slides for each testis, stained with May- Grünwald and Giemsa stains, and examined under a light microscope at magnifications of 125, 400, and 1,250, counting at least 200 spermatogenic cells (spermatogonia, primary and secondary spermatocytes, early and late spermatids, and spermatozoa) per smear and the interposed Sertoli cells. The cell number is expressed as a percentage. All patients underwent ultrasound scanning of the testis to evaluate testicular size and morphology before undergoing testicular aspiration. Semen evaluations were performed in a blinded fashion with regard to treatment and by the same operator. Plasma concentrations of FSH, LH, and T were measured by RIA with standard methods. Inhibin B plasma concentrations were measured by a solid-phase sandwich ELISA specific for the dimeric inhibin-b form (Serotec, Oxford, United Kingdom), as previously described (23, 24). Forty age-matched fertile and normozoospermic subjects were considered as controls for seminal and hormonal parameters. Design of the Study Improvement of seminal parameters is not always associated with an improvement in pregnancy rates. Therefore, to clarify the effectiveness of FSH therapy, subjects were studied in three consecutive phases, with primary outcomes being represented by both sperm parameters and pregnancy rate: [1] a period of treatment with recombinant hfsh for 3 months (therapy period), [2] the following 3-month period after the withdrawal of therapy, during which all subjects were monitored for semen parameters and spontaneous pregnancies (follow-up period), and [3] the following 3-month period, during which all subjects who had not reached pregnancy during the two previous periods underwent ART (ART period) (Fig. 1). Therapy Period After the initial assessment (basal hormonal parameters, three semen analyses, history and physical examination, ultrasound scanning of the testes, and FNAC), the patients were prospectively randomized into two groups: 62 subjects Fertility and Sterility 655
3 FIGURE 1 Study description. FIVET in vitro fertilization embryo transfer. PATIENTS STUDIED (112) Treated group (62) (r-hfsh 100 IU on alternate days) Infertile-control group (50) (no therapy) THERAPY PERIOD 3 months Responder group (30) Non-responder group (32) (50) FOLLOW UP PERIOD 3 months 16.7% 5/30 3.1% 1/32 4.0% 2/50 Spontaneous No (25) No (31) No (48) ART PERIOD 3 months IUI 20.0% 3/15 IUI n.s. IUI n.s. after ART IVF FIVET 30.0% 3/10 ICSI - IVF FIVET 18.2% 2/11 ICSI 20.0% 4/20 IVF FIVET 22.2% 4/18 ICSI 20.0% 6/30 n.s.: not suitable Foresta. FSH therapy in male idiopathic infertility. Fertil Steril received recombinant hfsh (100 IU IM on alternate days for 3 months) (treated group), and 50 patients did not receive any treatment (infertile control group). The two groups were comparable in terms of age ( years vs years), duration of infertility ( years vs years), and semen, hormonal, and cytologic parameters, as discussed below. At the end of this 3-month period, semen analysis was performed in all subjects (treated and controls) by the same operator. Pretreatment and posttreatment semen evaluations were performed in a blinded fashion with regard to treatment. All spontaneous pregnancies occurring during this period were recorded and eventually confirmed by measurement of hcg plasma levels. Follow-Up Period To evaluate the effectiveness of FSH treatment, we continued to study these 112 male-factor infertile couples during an additional 3-month period. All subjects were encouraged to have a special coitus frequency, at least two to three times per week, particularly at midcycle. All spontaneous pregnancies occurring during these 3 months were recorded and confirmed by measurement of hcg plasma levels. 656 Foresta et al. FSH therapy in male idiopathic infertility Vol. 84, No. 3, September 2005
4 TABLE 1 Clinical and hormonal features of oligozoospermic patients compared with controls (fertile subjects). Treated group (n 62) Infertile control group (n 50) Control group (n 40) Demographic data Age of patients (y) Age of partner (y) Infertility duration (y) Seminal parameters Sperm concentrations ( 10 6 /ml) a a Total no. of spermatozoa ( 10 6 ) a a Forward motility (%) b b Normal morphology (%) Hormone levels FSH (IU/L) LH (IU/L) T (ng/ml) Inhibin B (pg/ml) Testicular volume (ml) b b Note: Data are presented as mean SD. The treatment group received recombinant hfsh (100 IU on alternate days); the infertile control group received no treatment. a P.001 vs. control group. b P.05 vs. control group. Foresta. FSH therapy in male idiopathic infertility. Fertil Steril At the end of the follow-up period, all patients were reevaluated for semen analysis. ART Period Within 3 months after the follow-up period, all patients who had not reached spontaneous pregnancy underwent ARTs. Patients with a total number of motile postwash spermatozoa were randomly enrolled either to IUI for three cycles or IVF for 1 cycle (25, 26). If the number of total motile spermatozoa was not suitable for IUI ( ), couples were enrolled only in IVF programs, either IVF-ET or intracytoplasmic sperm injection (ICSI) (1 cycle), considering the specific indications. After this period, the new pregnancies were recorded. For IUI, ovarian stimulation started on day 3 of a spontaneous menstrual cycle with 100 mg of clomiphene citrate for 5 days. Ovarian monitoring was carried out by vaginal ultrasound, starting on day 10 of the menstrual cycle. Ovulation was induced with hcg (5,000 IU IM) when at least one follicle with a diameter 18 mm was observed. Two inseminations per cycle were performed, 24 hours and 48 hours after the administration of hcg. For IVF, the ovulation induction protocol used was the same for all the female partners and included down-regulation with a GnRH agonist and ovarian stimulation with recombinant hfsh. Follicular growth was monitored according to E 2 plasma levels and ultrasound measurements. Follicular aspiration was performed under transvaginal ultrasound guidance hours after hcg administration. The following steps, as regarding sperm preparation, insemination of oocytes, fertilization, embryo culture, and ET were performed according to European Society of Human Reproduction and Embryology indications (27). Statistical Analysis The results are expressed as mean SD. Comparisons between groups were performed with unpaired Student s t-tests. Comparisons of pretreatment and posttreatment data were performed with paired Student s t-tests. Comparisons of proportion were performed with a one-sided nonparametric resampling test. Probability (P) values of.05 were considered statistically significant. RESULTS Therapy Period The baseline clinical and hormonal data of the treated, infertile control, and normal control (fertile subjects) groups are summarized in Table 1. The treatment was well tolerated in all subjects, and no significant side effects were reported. In the treatment group considered as a whole, no modifications in sperm parameters were observed during the 3 Fertility and Sterility 657
5 TABLE 2 Sperm parameters observed during the different periods of the study in responder and nonresponder groups (treated subjects) and in the infertile control group (no treatment). Responder group (n 30) Non-responder group (n 32) Infertile control group (n 50) Sperm count ( 10 6 /ml) Total spermatozoa ( 10 6 ) Sperm count ( 10 6 /ml) Total spermatozoa ( 10 6 ) Sperm count ( 10 6 /ml) Total spermatozoa ( 10 6 ) Basal End of therapy period a a End of follow-up period b b End of ART period Note: Data are presented as mean SD. Therapy period: treatment with recombinant hfsh (100 IU IM) on alternate days for 3 months; follow-up period: an observation period of 3 months after the withdrawal of therapy; ART period: 3 months of ART. a P.01 vs. pretreatment. b P.05 vs. pretreatment. Foresta. FSH therapy in male idiopathic infertility. Fertil Steril months of therapy (sperm concentration /ml basal and /ml at the end of therapy). However, individual analysis of sperm parameters allowed us to identify two subgroups after the 3-month period of recombinant hfsh treatment: the responder group (30 of 62 subjects, 48.4%), who increased their sperm count after therapy, with a doubling of sperm concentration with respect to baseline; and the nonresponder group (32 of 62 subjects, 51.6%), who showed no increase in seminal parameters after FSH treatment. No significant variations were observed in other seminal parameters, such as forward motility and normal morphology, at the end of treatment in both groups (data not shown). In the infertile control group, no significant variations of sperm parameters were observed during this first period of observation. Table 2 summarizes the seminal parameters observed before and after recombinant hfsh therapy in the responder and nonresponder groups and in the infertile control group. Confirming previous studies, pretreatment testicular cytologic analysis of the patients in the responder group was characterized by isolated hypospermatogenesis (reduction in the number of germ cells without maturative disturbances); nonresponder patients had a cytologic picture of hypospermatogenesis, with maturative disturbances at different levels of the spermatogenetic process (spermatogonial spermatocytes or spermatidic arrest). During this first period, we did not observe spontaneous pregnancies in either the treated or the infertile control groups. Follow-Up Period Three months after the withdrawal of recombinant hfsh therapy, another sperm analysis was performed in all subjects. We did not observe any significant differences in seminal parameters in the treated group considered as a whole or in the nonresponder and infertile control groups. The responder group showed a significantly higher sperm concentration with respect to pretreatment sperm count. The mean sperm concentration in this group was not different from that observed after the 3-month period of FSH treatment (Table 2). During the follow-up period, the responder group showed significantly higher pregnancy rates. In fact, 5 patients achieved spontaneous pregnancies in the responder group (5 of 30, 16.7%), whereas one patient in the nonresponder group (1 of 32, 3.1%) and 2 in the infertile control group (2 of 50, 4.0%) achieved pregnancy (Fig. 1, Table 3). ART Period Six months after the withdrawal of recombinant hfsh therapy, another sperm analysis was performed in all subjects. No significant differences in seminal parameters were observed in the treated group considered as a whole or in the nonresponder and infertile control groups with respect to previous examinations. In the responder group, we observed a reduction of sperm concentration that was not, however, statistically different with respect to previous analyses. During this period, the patients who did not achieve pregnancy in the previous periods underwent ARTs. Because all patients in the responder group had a number of total motile postwash spermatozoa , they were randomly en- 658 Foresta et al. FSH therapy in male idiopathic infertility Vol. 84, No. 3, September 2005
6 TABLE 3 Pregnancy rates during the follow-up and ART periods in responder and nonresponder groups (treated subjects) and in infertile control group (no treatment). Follow-up period (spontaneous) ART period IUI IVF-ET ICSI Cumulative Treated subjects (n 62) 9.7 (6/62) 20.0 (3/15) 23.8 (5/21) 20.0 (4/20) 29.0 (18/62) Responder group (n 30) 16.7 (5/30) a 20.0 (3/15) 30.0 (3/10) 36.7 (11/30) Nonresponder group (n 32) 3.1 (1/32) Nonsuitable 18.2 (2/11) 20.0 (4/20) 21.9 (7/32) Infertile control group (n 50) 4.0 (2/50) Nonsuitable 22.2 (4/18) 20.0 (6/30) 24.0 (12/50) Note: Data are expressed as percentage (number). a P.05 vs. nonresponder and infertile control groups. Foresta. FSH therapy in male idiopathic infertility. Fertil Steril rolled in two ART programs: 15 subjects to IUI (three cycles) and 10 subjects to IVF-ET (one cycle). There were three pregnancies achieved in the patients assigned to IUI (3 of 15, 20.0%) and three pregnancies in the patients assigned to IVF-ET (3 of 10, 30.0%). The cumulative pregnancy rate in this group after ART was therefore 24.0% (6 of 25). In the other two groups, the number of total motile spermatozoa was not sufficient for an IUI program, so they were enrolled only for IVF (one cycle). Cumulative pregnancy rates in these groups after ART were 19.3% (6 of 31) and 20.8% (10 of 48) in the nonresponder and infertile control groups, respectively (Fig. 1, Table 3). In summary, during the follow-up and ART periods (i.e., during the 6-month period after the withdrawal of recombinant hfsh therapy), the cumulative pregnancy rate was 29.0% (18 of 62) in treated subjects. For the treatment subgroups, the pregnancy rates were 36.7% (11 of 30) in the responder group and 21.9% (7 of 32) in the nonresponder group. In the infertile control group, the pregnancy rate was 24.0% (12 of 50) (Table 3). DISCUSSION A male factor is the cause of infertility in approximately 25% 30% of infertile couples, and in an additional 30%, detectable abnormalities can be found in both partners (28, 29). Many aspects of male infertility are poorly understood, and medical therapy for these patients is mainly empiric and largely unsuccessful. Therefore, the management of male infertility often does not consider a pharmacologic treatment, and couples are directly treated with assisted reproduction. However, we think that medical therapy with FSH might be a valid method for improving spermatogenesis, although this treatment is effective only in selected cases. This is the first prospective, controlled, randomized clinical study showing that treatment with recombinant hfsh can improve seminal parameters and also spontaneous pregnancies in a selected group of idiopathic oligozoospermic patients. To evaluate the effectiveness of FSH therapy, we randomized infertile patients into two groups, treated or untreated. We did not observe any significant variation in seminal parameters in infertile control subjects and in the treatment group considered as a whole. However, in treated patients, a significant increase of sperm concentration was observed in approximately half the subjects (responder group). These subjects were affected by isolated hypospermatogenesis without spermatogenic arrest, as evaluated by FNAC before treatment. These data expand and confirm previous preliminary studies and strengthen the evidence that FSH treatment could be effective only in oligozoospermic subjects with normal FSH and inhibin B plasma concentrations and a testicular structure of moderate hypospermatogenesis without maturation defect. In such cases the spermatogenetic process can be efficaciously stimulated, thereby obtaining an increased sperm number in the ejaculate. The second aim of the present study was to evaluate the effectiveness of FSH therapy in terms of pregnancy rate. This is an important issue when evaluating the effect of a treatment for male infertility, because the improvement of seminal parameters often is not associated with an improvement of pregnancy rate, and conversely, spontaneous pregnancies can be achieved in infertile couples outside the treatment period. An improved pregnancy rate is also the primary endpoint for infertile couples, thus this parameter should be evaluated as a main outcome measurement of the effectiveness of a pharmacologic treatment in male infertility. Only two randomized, controlled clinical studies of FSH therapy in male infertility have been performed, and neither showed a significant increase in sperm concentrations or in pregnancy rates (13, 14). However, the selection criteria for infertile men recruited in these studies were not strict enough to derive conclusive information. Matorras et al. (13) evaluated 148 consecutive men undergoing IUI because of infertility, but they included men with a wide variation of sperm parameters. In fact, the mean sperm concentration in the FSH-treated group was /ml, with only Fertility and Sterility 659
7 18.2% of men presenting oligozoospermia. Kamischke et al. (14) studied a group of patients with different degrees of testicular alteration; in fact, selection criteria for treatment were limited to abnormal semen parameters and basal FSH concentrations 12 IU/L. In contrast to these studies, we detected a significant increase in spontaneous pregnancies in the responder group compared with both nonresponder and infertile control groups during the 3-month period after the withdrawal of recombinant hfsh therapy (16.7% vs. 3.1% and 4.0%, respectively, P.05). If we also add the pregnancies obtained with IUI during the following 3 months, pregnancy rates were 26.7% (8 of 30) in responder subjects, 3.1% (1 of 32) in nonresponder subjects, and 4.0% (2 of 50) in infertile control subjects. These data are very important because they highlight that FSH therapy, when performed in appropriate subjects, allows infertile couples to conceive spontaneously or by IUI in approximately one fourth of cases. In other words, these subjects benefitted from FSH therapy mainly because they could avoid more complex ART, such as IVF-ET or ICSI. Although the cumulative pregnancy rate, including with IVF-ET and ICSI cycles, seemed to be higher at the end of the study in responder subjects, it does not statistically differ with respect to the nonresponder and infertile control groups (36.7% vs. 21.9% and 24.0%, respectively), but a statistical analysis is difficult because of the dispersion of data. However, it is important to stress that the improvement of seminal parameters in the responder group after recombinant hfsh therapy and during the 6 months of follow-up allowed these patients to perform a less invasive method, whereas this was not possible for the other two patient groups. Intrauterine insemination is considered the most cost-effective and least-invasive treatment for male factor infertility when at least motile postwash spermatozoa are present in the ejaculate (25, 26, 30). Conversely, ICSI involves several risks in the female partners (multiple pregnancies, hyperstimulation syndrome, increase in abortion rate) and in the offspring (premature birth, low birthweight, chromosome abnormalities). In conclusion, this controlled, randomized clinical trial shows that FSH treatment is not effective in unselected oligozoospermic men. However, this is the first demonstration that such treatment can induce a significance increase in sperm count and an improvement in pregnancy rate in a subgroup of oligozoospermic patients (those with normal FSH plasma levels and absence of maturation arrest). These results underline the importance of strict criteria for the selection of patients to be treated with FSH. In our opinion, a deep understanding of the pathophysiologic conditions in male infertility has an important impact on the choice of medical treatment and on the perspectives of success. Indeed, the age of the female partner is an important aspect in decisions to treat the male for a long period. The results of this study suggest that a rational treatment of male infertility is possible. Therefore, in male infertility initial efforts should be directed to the study of infertile male patients and to improve sperm quality, whenever possible. Intracytoplasmic sperm injection should be applied only in the presence of severe male factor infertility or in the absence of a significant improvement of semen parameters after medical treatment. REFERENCES 1. Matsumoto AM. Hormonal control of human spermatogenesis. In: Burger H, de Kretser D, eds. The testis. New York: Raven Press, 1989: Sharpe RM. Follicle-stimulating hormone and spermatogenesis in adult male. 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Hum Reprod 1997;12: Tapanainen JS, Aittomaki K, Min J, Vaskivuo T, Huhtaniemi IT. Men homozygous for an inactivating mutation of the follicle-stimulating hormone (FSH) receptor gene present variable suppression of spermatogenesis and fertility. Nat Genet 1997;15: Acosta AA, Khalifa E, Oehninger S. Pure human follicle stimulating hormone has a role in the treatment of severe male infertility by assisted reproduction: Norfolk s total experience. Hum Reprod 1992;7: Bartoov B, Eltes F, Lunenfeld E. Sperm quality of subfertile males before and after treatment with human follicle-stimulating hormone. Fertil Steril 1994;61: Strehler E, Sterzik K, De Santo M, Abt M, Wiedemann R, Bellati U, et al. The effect of follicle-stimulating hormone therapy on sperm quality: an ultrastructural mathematical evaluation. J Androl 1997;18: Ashkenazi J, Bar-Hava I, Farhi J, Levy T, Feldberg D, Orvieto R, et al. The role of purified follicle stimulating hormone therapy in the male partner before intracytoplasmic sperm injection. Fertil Steril 1999;72: Ben-Rafael Z, Farhi J, Feldberg D, Bartoov B, Kovo M, Eltes F, et al. Follicle-stimulating hormone treatment for men with idiopathic oligoteratoasthenozoospermia before in vitro fertilization: the impact on sperm microstructure and fertilization potential. Fertil Steril 2000;73: Matorras R, Perez C, Corcostegui B, Pijoan JI, Ramon O, Delgado P, et al. Treatment of the male with follicle-stimulating hormone in intrauterine insemination with husband s spermatozoa: a randomized study. Hum Reprod 1997;12: Kamischke A, Behre HM, Bergmann M, Simoni M, Schafer T, Nieschlag E. Recombinant human follicle stimulating hormone for treatment of male idiopathic infertility: a randomized, double-blind, placebo-controlled, clinical trial. Hum Reprod 1998;13: Foresta C, Bettella A, Ferlin A, Garolla A, Rossato M. 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8 and after therapy with follicle stimulating hormone. Hum Reprod 1999;14: Foresta C, Bettella A, Merico M, Garolla A, Plebani M, Ferlin A, et al. FSH in the treatment of oligozoospermia. Mol Cell Endocrinol 2000; 161: Foresta C, Bettella A, Merico M, Garolla A, Ferlin A, Rossato M. Use of recombinant human follicle-stimulating hormone in the treatment of male factor infertility. Fertil Steril 2002;77: World Health Organization. Laboratory manual for the examination of human semen and sperm-cervical mucus interaction. 4th ed. Cambridge, United Kingdom: Cambridge University Press, Foresta C, Varotto A, Scandellari C. Assessment of testicular cytology by fine needle aspiration as a diagnostic parameter in the evaluation of the azoospermic subject. Fertil Steril 1992;57: Foresta C, Varotto A. Assessment of testicular cytology by fine needle aspiration as a diagnostic parameter in the evaluation of the oligospermic subject. Fertil Steril 1992;58: Foresta C, Ferlin A, Bettella A, Rossato M, Varotto A. Diagnostic and clinical features in azoospermia. Clin Endocrinol 1995;43: Groome NP, Illingworth PJ, O Brien M, Pai R, Rodger FE, Mather JP, et al. Measurement of dimeric inhibin B throughout the human menstrual cycle. J Clin Endocrinol Metab 1996;81: Illingworth PJ, Groome NP, Byrd W, Rainey WE, Mcneilly AS, Mather JP, et al. Inhibin-B: a likely candidate for the physiologically important form of inhibin in men. J Clin Endocrinol Metab 1996; 81: Oehninger S. Clinical and laboratory management of male infertility: an opinion on its current status. J Androl 2000;6: Khalil MR, Rasmussen PE, Erb K, Laursen SB, Rex S, Westergaard LG. Homologous intrauterine insemination. An evaluation of prognostic factors based on a review of 2473 cycles. Acta Obstet Gynecol Scand 2001;80: Gianaroli L, Plachot M, van Kooij R, Al-Hasani S, Dawson K, DeVos A, et al. ESHRE guidelines for good practice in IVF laboratories. Hum Reprod 2000;15: World Health Organization. Towards more objectivity in diagnosis and management of male infertility. Results of a World Health Organization multicenter study. Int J Androl 1987;10(Suppl 7): Bhasin S, de Krestser DM, Baker HWG. Pathophysiology and natural history of male infertility. J Clin Endocrinol Metab 1994;79: Comhaire F, Zalata A, Mahmoud A. Critical evaluation of the effectiveness of different modes of treatment of male infertility. Andrologia 1996;28(Suppl 1):31 5. Fertility and Sterility 661
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