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Use of subinguinal incision for microsurgical testicular biopsy during varicocelectomy in men with nonobstructive azoospermia
TECHNIQUES AND INSTRUMENTATION Use of subinguinal incision for microsurgical testicular biopsy during varicocelectomy in men with nonobstructive azoospermia Marcello Cocuzza, M.D.,a Rodrigo Pagani, M.D.,a Roberto Iglesias Lopes, M.D.,a Kelly S. Athayde, M.T., M.S.,a,b Antonio M. Lucon, M.D., Ph.D.,a Miguel Srougi, M.D., PhD.,a and Jorge Hallak, M.D., Ph.D.a a
Department of Urology, University of S~ao Paulo, S~ao Paulo, Brazil; and b Reproductive Research Center, Glickman Urological Institute and Department of Obstetrics and Gynecology, Cleveland Clinic, Cleveland, Ohio
Objective: To describe a subinguinal technique of microsurgical testicular biopsy performed during subinguinal varicocelectomy in men with nonobstructive azoospermia. Design: Prospective clinical study. Setting: Andrology laboratory at tertiary care hospital. Male infertility section, department of urology, at tertiary care hospital. Patient(s): Ten azoospermic men with clinical varicocele. Intervention(s): Subinguinal microsurgical testicular biopsy and microsurgical varicocele repair. Main Outcome Measure(s): Safety, feasibility, and effectiveness of subinguinal testicular biopsy during varicocele repair. Result(s): All testes were easily delivered through the subinguinal incision, and testicular biopsies were successfully performed under microscopic view. After a median follow-up of 9 months, none of the patients had any discomfort, pain, or presented with testicular atrophy. No intraoperative or postoperative complications were observed. There was no incidence of wound infection or scrotal hematoma. Conclusion(s): The subinguinal approach is a safe and effective option for testicular biopsy during varicocele repair in men with nonobstructive azoospermia. This technique may be an attractive alternative to traditional biopsy because it obviates scrotal violation. (Fertil Steril 2009;91:925–8. 2009 by American Society for Reproductive Medicine.) Key Words: Varicocele, testicular biopsy, male infertility, nonobstructive azoospermia, microsurgery
The estimated incidence of nonobstructive azoospermia in association with varicocele is 5%–10% (1). Although motile sperm are found in the ejaculate of 21%–55% of azoospermic men after varicocele repair, spontaneous pregnancies are rare (1, 2). Varicocelectomy in this population may avoid the need for more invasive procedures such as testicular sperm extraction (TESE) by providing sperm by ejaculation for intracytoplasmic sperm injection (ICSI) (3). Fertilizing ability and ICSI success rates have been suggested to be superior when fresh motile ejaculated sperm are used compared with sperm provided by testicular biopsy or microsurgical TESE (4). Testicular biopsy during varicocele repair in azoospermic men provides histologic data that can be used as a predictor of sperm appearance in ejaculate after surgery as well as of Received September 5, 2007; revised December 13, 2007; accepted December 19, 2007. Reprint requests: Marcello Cocuzza, M.D., Department of Urology, Uni~o Paulo, Rua Adma Jafet, 50 151/152, Sa ~o Paulo versity of Sa 01308-050, Brazil (FAX: 55-11-3256-9511; E-mail: mcocuzza@uol. com.br).
0015-0282/09/$36.00 doi:10.1016/j.fertnstert.2007.12.065
success in sperm retrieval (2, 5). Previous studies reported the efficacy and safety of open transscrotal testicular biopsy performed at the same time as varicocele repair (2, 6). To our knowledge, the use of a subinguinal incision for microsurgical testicular biopsy performed during varicocelectomy has not been described in the literature. To evaluate the feasibility of this procedure we describe herein our technique of microsurgical biopsy of the testes during subinguinal varicocelectomy in men with nonobstructive azoospermia.
MATERIALS AND METHODS The University of S~ao Paulo Institutional Review Board approved this study. Between August 2005 and November 2006, in a prospective study, 10 azoospermic patients underwent microsurgical testicular biopsy through the same subinguinal incision used during varicocele repair. During scrotal examination performed with the patient in the standing position, bilateral palpable varicocele was identified in 4 men, whereas only left varicocele was identified in 6. Doppler ultrasonography demonstrated subclinical right varicocele
Fertility and Sterility Vol. 91, No. 3, March 2009 Copyright ª2009 American Society for Reproductive Medicine, Published by Elsevier Inc.
925
in 3 patients. Subclinical right varicoceles were considered present if veins >3.0 mm in diameter were identified on Doppler ultrasound examination performed in a standing position. Testicular size was evaluated with testicular Prader orchidometry or by scrotal ultrasound (7). At least two preoperative semen analyses were evaluated according to World Healthy Organization guidelines (8). Azoospermia was confirmed after centrifugation for detection of sperm in the pellet. Hormone profile was assessed in all subjects according to FSH, LH, and T. All patients underwent preoperative genetic testing that revealed no Y chromosome microdeletions or karyotype abnormalities. The biopsy findings were classified as normal spermatogenesis, hypospermatogenesis, maturation arrest, and Sertoli cell–only (germ cell aplasia) using the standard hematoxylin-eosin sections.
lar region in the anterior surface of the testes at the middle portion was chosen for the tunical incision, approximately 5 mm long. Small bleeders were controlled with bipolar cautery, and testicular parenchyma was excised with iris scissors (Fig. 2). The tunica albuginea and vaginalis were closed with 4-0 polyglactin sutures. At the completion of biopsy the testis was returned to the normal scrotal position, and the spermatic cord was placed over a Penrose drain. Microsurgical varicocele repair was performed with the artery- and lymphaticsparing technique as previously described (9). The Scarpa’s fascia was closed with an interrupted absorbable suture, and the skin was closed with a running subcuticular 5-0 absorbable monofilament suture. All patients were observed at regular intervals and evaluated by physical examination and seminal analysis.
All procedures were performed bilaterally and under regional anesthesia. After giving antibiotics, a 2-cm subinguinal incision was made 1 cm below the external inguinal ring. The Camper’s fascia and Scarpa’s fascia were incised to expose the spermatic cord, which was then surrounded by a Penrose drain. The spermatic cord was mobilized out of the incision to permit identification of the external spermatic veins that penetrated the floor of the inguinal canal. These identified external spermatic veins were ligated with 4-0 silk ties and divided. The testis was delivered into the incision after a soft digital dissection exposing the tunica vaginalis (Fig. 1). The tunica vaginalis was entered and held open with clamps. Dissection was performed under a Zeiss operating microscope (model S8; Carl Zeiss, Jena, Germany) with 6 to 8 magnification. The outer surface of the tunica albuginea was examined to avoid subtunical arteries. An avascu-
RESULTS The mean (SD) age of the patients was 29.4 5.2 years. The varicocele was grade 3 in 6 patients (60%) and grade 2 in 4 (40%). Of the 10 patients, 4 had bilateral clinical varicocele, and 3 had left clinical varicocele with subclinical right varicocele and underwent bilateral varicocele repair as well as simultaneous bilateral testicular biopsy. Three patients had only left varicocele and underwent unilateral repair and biopsy of the ipsilateral testis. All testes were easily delivered into the subinguinal incision after digital dissection, and testicular biopsies were successfully performed under microscopic view. The mean testicular volume was 12.6 4.5 mL for left testes and 13.1 3.7 mL for right
FIGURE 2
(A) Digital dissection of the testis. (B) Testis delivered into the wound, exposing the tunica vaginalis.
(A) Tunica vaginalis entered and held open with clamps. (B) Microscopic view showing a tunica albuginea incision in an avascular region and testis biopsy.
Cocuzza. Subinguinal testis biopsy during varicocelectomy. Fertil Steril 2009.
Cocuzza. Subinguinal testis biopsy during varicocelectomy. Fertil Steril 2009.
FIGURE 1
926
Cocuzza et al.
Subinguinal testis biopsy during varicocelectomy
Vol. 91, No. 3, March 2009
testes. The mean preoperative hormone levels were 21.0 15.2 mIU/mL for FSH, 7.4 4.3 mIU/mL for LH, and for 553.4 186.7 ng/dL for T. The mean (range) operative time for bilateral repair was 95 minutes (80–110 minutes) and for unilateral repair was 66 minutes (60–70 minutes). Postoperative semen analyses were collected 3 and 6 months after surgery. Of the 10 patients, 3 (30%) had motile sperm in the ejaculate during postoperative seminal analysis. All biopsies showed pathological changes. The histologic pattern of testis, varicocele grade, and postoperative seminal concentration and motility are summarized in Table 1. Although we did not apply any pain score or evaluate necessity of analgesic intake, no intraoperative or postoperative complications were observed. After a median (range) follow-up of 9 months (6–20 months), none of the patients had any discomfort, pain, or presented with testicular atrophy. There was no incidence of wound infection or scrotal hematoma. DISCUSSION Azoospermic men with varicocele must decide whether to undergo varicocelectomy or TESE/ICSI. Many of them will ultimately require ICSI, especially those with Sertoli cell– only or maturation arrest at the spermatocyte stage (1, 2, 6). However, more than half of these men with maturation arrest at the spermatid stage or hypospermatogenesis can provide postoperative motile sperm by ejaculation. Hence, testicular histology may be considered in deciding how long a couple should wait after varicocelectomy before proceeding with assisted reproductive technology. Currently, we recommend that patients with maturation arrest or hypospermatogenesis pattern wait 12–18 months before proceeding to testicular sperm extraction and ICSI; for those with Sertoli cell–only pattern we do not encourage waiting more than 12 months.
Although clinical information may preclude the necessity of diagnostic testis biopsy, in some cases histologic analysis can be important to differentiate between normal and impaired spermatogenesis. Varicocele can result in infertility through the sloughing of immature cells or through an arrest of spermatogenesis at the spermatid or primary spermatocyte stages. Posinovec et al. (10) showed that although varicocele has a bilateral effect, the greater the degree of damage, the greater the differences in histologic findings in both testicles. In addition, approximately 20% of focal spermatogenesis is missed when unilateral biopsy was performed. We found one patient who presented discordant histology pattern between the testes. Currently, because the most advanced pattern of testicular histology on biopsy is recognized as the predictive factor for sperm recovery after varicocele repair, we perform biopsy in both testes when the surgery is also performed bilaterally. An increase in the incidence of testicular cancer has been reported during the past 30 years (11). Recently an increased prevalence of testicular nodules and cancer was reported in infertile men, especially those presenting with azoospermia (12, 13). Radical inguinal orchiectomy is the gold standard procedure to initially approach testicular cancer. Previous scrotal violation has been associated with an increased risk for local recurrence (14). Although the lifetime risk of testicular cancer is still low, avoiding transscrotal testicular biopsy in young infertile men could prevent consequences of scrotal violation (15). The use of a subinguinal incision for testicular biopsy during varicocele repair was feasible and effective in all cases. Although there were a limited number of patients in this series, we believe that the reduced mean testicular volume usually found in patients with nonobstructive azoospermia allowed the complete exposure of the testis in such a small
TABLE 1 Histologic pattern of testis and seminal parameters in 10 azoospermic men after microsurgical subinguinal varicocele repair.
Patient
Histopathologic pattern of the left testis
Histopathologic pattern of the right testis
Varicocele grade
Varicocele repair
Sperm concentration (3106/mL)
Sperm motility (%)
1 2 3 4 5 6 7 8 9 10
MA SCO HYPO MA MA MA SCO SCO HYPO SCO
— SCO HYPO MA — MA SCO — HYPO HYPO
3 3 2 2 3 2 2 3 3 3
Left Bilateral Bilateral Bilateral Left Bilateral Bilateral Left Bilateral Bilateral
12.2 0 0.6 0 0 0 0 0 3.9 0
40 0 50 0 0 0 0 0 20 0
Note: MA ¼ maturation arrest; SCO ¼ Sertoli cell–only syndrome (germ cell aplasia); HYPO ¼ hypospermatogenesis. Cocuzza. Subinguinal testis biopsy during varicocelectomy. Fertil Steril 2009.
Fertility and Sterility
927
incision without any complication. Microsurgical techniques during testicular biopsy have been used to identify testicular vessels on the surface of the tunica albuginea, reducing the incidence of complications compared with non-microscopic open biopsies (16). Our technique included the use of magnification, obviating scrotal violation. This procedure should be validated in a larger series and may be an attractive alternative to the traditional scrotal approach for testicular biopsy in azoospermic patients presenting with varicocele.
1. Kadioglu A, Tefekli A, Cayan S, Kandirali E, Erdemir F, Tellaloglu S. Microsurgical inguinal varicocele repair in azoospermic men. Urology 2001;57:328–33. 2. Matthews GJ, Matthews ED, Goldstein M. Induction of spermatogenesis and achievement of pregnancy after microsurgical varicocelectomy in men with azoospermia and severe oligoasthenospermia. Fertil Steril 1998;70:71–5. 3. Pasqualotto FF, Sobreiro BP, Hallak J, Pasqualotto EB, Lucon AM. Induction of spermatogenesis in azoospermic men after varicocelectomy repair: an update. Fertil Steril 2006;85:635–9. 4. Aboulghar MA, Mansour RT, Serour GI, Fahmy I, Kamal A, Tawab NA, et al. Fertilization and pregnancy rates after intracytoplasmic sperm injection using ejaculate semen and surgically retrieved sperm. Fertil Steril 1997;68:108–11. 5. Su LM, Palermo GD, Goldstein M, Veeck LL, Rosenwaks Z, Schlegel PN. Testicular sperm extraction with intracytoplasmic sperm
Cocuzza et al.
7. 8.
9.
10.
REFERENCES
928
6.
11. 12.
13.
14.
15. 16.
injection for nonobstructive azoospermia: testicular histology can predict success of sperm retrieval. J Urol 1999;161:112–6. Lee JS, Park HJ, Seo JT. What is the indication of varicocelectomy in men with nonobstructive azoospermia? Urology 2007;69:352–5. Prader A. Testicular size: assessment and clinical importance. Triangle 1966;7:240–3. World Health Organization. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. New York: Cambridge University Press, 1999. Marmar JL, Kim Y. Subinguinal microsurgical varicocelectomy: a technical critique and statistical analysis of semen and pregnancy data. J Urol 1994;152:1127–32. Posinovec J. The necessity for bilateral biopsy in oligo- and azoospermia. Int J Fertil 1976;21:189–91. Huyghe E, Matsuda T, Thonneau P. Increasing incidence of testicular cancer worldwide: a review. J Urol 2003;170:5–11. Nobert C, Goldstein M. Increased incidence of testicular cancer in men with infertility and abnormal semen analysis. Fertil Steril 2001; 76(Suppl 1):S50. Mancini M, Carmignani L, Gazzano G, Sagone P, Gadda F, Bosari S, et al. High prevalence of testicular cancer in azoospermic men without spermatogenesis. Hum Reprod 2007;22:1042–6. Leibovitch I, Baniel J, Foster RS, Donohue JP. The clinical implications of procedural deviations during orchiectomy for nonseminomatous testis cancer. J Urol 1995;154:935–9. Aitken RJ, Koopman P, Lewis SE. Seeds of concern. Nature 2004;432: 48–52. Dardashti K, Williams RH, Goldstein M. Microsurgical testis biopsy: a novel technique for retrieval of testicular tissue. J Urol 2000;163: 1206–7.
Subinguinal testis biopsy during varicocelectomy
Vol. 91, No. 3, March 2009
Department of Urology, University of S~ao Paulo, S~ao Paulo, Brazil; and b Reproductive Research Center, Glickman Urological Institute and Department of Obstetrics and Gynecology, Cleveland Clinic, Cleveland, Ohio
Objective: To describe a subinguinal technique of microsurgical testicular biopsy performed during subinguinal varicocelectomy in men with nonobstructive azoospermia. Design: Prospective clinical study. Setting: Andrology laboratory at tertiary care hospital. Male infertility section, department of urology, at tertiary care hospital. Patient(s): Ten azoospermic men with clinical varicocele. Intervention(s): Subinguinal microsurgical testicular biopsy and microsurgical varicocele repair. Main Outcome Measure(s): Safety, feasibility, and effectiveness of subinguinal testicular biopsy during varicocele repair. Result(s): All testes were easily delivered through the subinguinal incision, and testicular biopsies were successfully performed under microscopic view. After a median follow-up of 9 months, none of the patients had any discomfort, pain, or presented with testicular atrophy. No intraoperative or postoperative complications were observed. There was no incidence of wound infection or scrotal hematoma. Conclusion(s): The subinguinal approach is a safe and effective option for testicular biopsy during varicocele repair in men with nonobstructive azoospermia. This technique may be an attractive alternative to traditional biopsy because it obviates scrotal violation. (Fertil Steril 2009;91:925–8. 2009 by American Society for Reproductive Medicine.) Key Words: Varicocele, testicular biopsy, male infertility, nonobstructive azoospermia, microsurgery
The estimated incidence of nonobstructive azoospermia in association with varicocele is 5%–10% (1). Although motile sperm are found in the ejaculate of 21%–55% of azoospermic men after varicocele repair, spontaneous pregnancies are rare (1, 2). Varicocelectomy in this population may avoid the need for more invasive procedures such as testicular sperm extraction (TESE) by providing sperm by ejaculation for intracytoplasmic sperm injection (ICSI) (3). Fertilizing ability and ICSI success rates have been suggested to be superior when fresh motile ejaculated sperm are used compared with sperm provided by testicular biopsy or microsurgical TESE (4). Testicular biopsy during varicocele repair in azoospermic men provides histologic data that can be used as a predictor of sperm appearance in ejaculate after surgery as well as of Received September 5, 2007; revised December 13, 2007; accepted December 19, 2007. Reprint requests: Marcello Cocuzza, M.D., Department of Urology, Uni~o Paulo, Rua Adma Jafet, 50 151/152, Sa ~o Paulo versity of Sa 01308-050, Brazil (FAX: 55-11-3256-9511; E-mail: mcocuzza@uol. com.br).
0015-0282/09/$36.00 doi:10.1016/j.fertnstert.2007.12.065
success in sperm retrieval (2, 5). Previous studies reported the efficacy and safety of open transscrotal testicular biopsy performed at the same time as varicocele repair (2, 6). To our knowledge, the use of a subinguinal incision for microsurgical testicular biopsy performed during varicocelectomy has not been described in the literature. To evaluate the feasibility of this procedure we describe herein our technique of microsurgical biopsy of the testes during subinguinal varicocelectomy in men with nonobstructive azoospermia.
MATERIALS AND METHODS The University of S~ao Paulo Institutional Review Board approved this study. Between August 2005 and November 2006, in a prospective study, 10 azoospermic patients underwent microsurgical testicular biopsy through the same subinguinal incision used during varicocele repair. During scrotal examination performed with the patient in the standing position, bilateral palpable varicocele was identified in 4 men, whereas only left varicocele was identified in 6. Doppler ultrasonography demonstrated subclinical right varicocele
Fertility and Sterility Vol. 91, No. 3, March 2009 Copyright ª2009 American Society for Reproductive Medicine, Published by Elsevier Inc.
925
in 3 patients. Subclinical right varicoceles were considered present if veins >3.0 mm in diameter were identified on Doppler ultrasound examination performed in a standing position. Testicular size was evaluated with testicular Prader orchidometry or by scrotal ultrasound (7). At least two preoperative semen analyses were evaluated according to World Healthy Organization guidelines (8). Azoospermia was confirmed after centrifugation for detection of sperm in the pellet. Hormone profile was assessed in all subjects according to FSH, LH, and T. All patients underwent preoperative genetic testing that revealed no Y chromosome microdeletions or karyotype abnormalities. The biopsy findings were classified as normal spermatogenesis, hypospermatogenesis, maturation arrest, and Sertoli cell–only (germ cell aplasia) using the standard hematoxylin-eosin sections.
lar region in the anterior surface of the testes at the middle portion was chosen for the tunical incision, approximately 5 mm long. Small bleeders were controlled with bipolar cautery, and testicular parenchyma was excised with iris scissors (Fig. 2). The tunica albuginea and vaginalis were closed with 4-0 polyglactin sutures. At the completion of biopsy the testis was returned to the normal scrotal position, and the spermatic cord was placed over a Penrose drain. Microsurgical varicocele repair was performed with the artery- and lymphaticsparing technique as previously described (9). The Scarpa’s fascia was closed with an interrupted absorbable suture, and the skin was closed with a running subcuticular 5-0 absorbable monofilament suture. All patients were observed at regular intervals and evaluated by physical examination and seminal analysis.
All procedures were performed bilaterally and under regional anesthesia. After giving antibiotics, a 2-cm subinguinal incision was made 1 cm below the external inguinal ring. The Camper’s fascia and Scarpa’s fascia were incised to expose the spermatic cord, which was then surrounded by a Penrose drain. The spermatic cord was mobilized out of the incision to permit identification of the external spermatic veins that penetrated the floor of the inguinal canal. These identified external spermatic veins were ligated with 4-0 silk ties and divided. The testis was delivered into the incision after a soft digital dissection exposing the tunica vaginalis (Fig. 1). The tunica vaginalis was entered and held open with clamps. Dissection was performed under a Zeiss operating microscope (model S8; Carl Zeiss, Jena, Germany) with 6 to 8 magnification. The outer surface of the tunica albuginea was examined to avoid subtunical arteries. An avascu-
RESULTS The mean (SD) age of the patients was 29.4 5.2 years. The varicocele was grade 3 in 6 patients (60%) and grade 2 in 4 (40%). Of the 10 patients, 4 had bilateral clinical varicocele, and 3 had left clinical varicocele with subclinical right varicocele and underwent bilateral varicocele repair as well as simultaneous bilateral testicular biopsy. Three patients had only left varicocele and underwent unilateral repair and biopsy of the ipsilateral testis. All testes were easily delivered into the subinguinal incision after digital dissection, and testicular biopsies were successfully performed under microscopic view. The mean testicular volume was 12.6 4.5 mL for left testes and 13.1 3.7 mL for right
FIGURE 2
(A) Digital dissection of the testis. (B) Testis delivered into the wound, exposing the tunica vaginalis.
(A) Tunica vaginalis entered and held open with clamps. (B) Microscopic view showing a tunica albuginea incision in an avascular region and testis biopsy.
Cocuzza. Subinguinal testis biopsy during varicocelectomy. Fertil Steril 2009.
Cocuzza. Subinguinal testis biopsy during varicocelectomy. Fertil Steril 2009.
FIGURE 1
926
Cocuzza et al.
Subinguinal testis biopsy during varicocelectomy
Vol. 91, No. 3, March 2009
testes. The mean preoperative hormone levels were 21.0 15.2 mIU/mL for FSH, 7.4 4.3 mIU/mL for LH, and for 553.4 186.7 ng/dL for T. The mean (range) operative time for bilateral repair was 95 minutes (80–110 minutes) and for unilateral repair was 66 minutes (60–70 minutes). Postoperative semen analyses were collected 3 and 6 months after surgery. Of the 10 patients, 3 (30%) had motile sperm in the ejaculate during postoperative seminal analysis. All biopsies showed pathological changes. The histologic pattern of testis, varicocele grade, and postoperative seminal concentration and motility are summarized in Table 1. Although we did not apply any pain score or evaluate necessity of analgesic intake, no intraoperative or postoperative complications were observed. After a median (range) follow-up of 9 months (6–20 months), none of the patients had any discomfort, pain, or presented with testicular atrophy. There was no incidence of wound infection or scrotal hematoma. DISCUSSION Azoospermic men with varicocele must decide whether to undergo varicocelectomy or TESE/ICSI. Many of them will ultimately require ICSI, especially those with Sertoli cell– only or maturation arrest at the spermatocyte stage (1, 2, 6). However, more than half of these men with maturation arrest at the spermatid stage or hypospermatogenesis can provide postoperative motile sperm by ejaculation. Hence, testicular histology may be considered in deciding how long a couple should wait after varicocelectomy before proceeding with assisted reproductive technology. Currently, we recommend that patients with maturation arrest or hypospermatogenesis pattern wait 12–18 months before proceeding to testicular sperm extraction and ICSI; for those with Sertoli cell–only pattern we do not encourage waiting more than 12 months.
Although clinical information may preclude the necessity of diagnostic testis biopsy, in some cases histologic analysis can be important to differentiate between normal and impaired spermatogenesis. Varicocele can result in infertility through the sloughing of immature cells or through an arrest of spermatogenesis at the spermatid or primary spermatocyte stages. Posinovec et al. (10) showed that although varicocele has a bilateral effect, the greater the degree of damage, the greater the differences in histologic findings in both testicles. In addition, approximately 20% of focal spermatogenesis is missed when unilateral biopsy was performed. We found one patient who presented discordant histology pattern between the testes. Currently, because the most advanced pattern of testicular histology on biopsy is recognized as the predictive factor for sperm recovery after varicocele repair, we perform biopsy in both testes when the surgery is also performed bilaterally. An increase in the incidence of testicular cancer has been reported during the past 30 years (11). Recently an increased prevalence of testicular nodules and cancer was reported in infertile men, especially those presenting with azoospermia (12, 13). Radical inguinal orchiectomy is the gold standard procedure to initially approach testicular cancer. Previous scrotal violation has been associated with an increased risk for local recurrence (14). Although the lifetime risk of testicular cancer is still low, avoiding transscrotal testicular biopsy in young infertile men could prevent consequences of scrotal violation (15). The use of a subinguinal incision for testicular biopsy during varicocele repair was feasible and effective in all cases. Although there were a limited number of patients in this series, we believe that the reduced mean testicular volume usually found in patients with nonobstructive azoospermia allowed the complete exposure of the testis in such a small
TABLE 1 Histologic pattern of testis and seminal parameters in 10 azoospermic men after microsurgical subinguinal varicocele repair.
Patient
Histopathologic pattern of the left testis
Histopathologic pattern of the right testis
Varicocele grade
Varicocele repair
Sperm concentration (3106/mL)
Sperm motility (%)
1 2 3 4 5 6 7 8 9 10
MA SCO HYPO MA MA MA SCO SCO HYPO SCO
— SCO HYPO MA — MA SCO — HYPO HYPO
3 3 2 2 3 2 2 3 3 3
Left Bilateral Bilateral Bilateral Left Bilateral Bilateral Left Bilateral Bilateral
12.2 0 0.6 0 0 0 0 0 3.9 0
40 0 50 0 0 0 0 0 20 0
Note: MA ¼ maturation arrest; SCO ¼ Sertoli cell–only syndrome (germ cell aplasia); HYPO ¼ hypospermatogenesis. Cocuzza. Subinguinal testis biopsy during varicocelectomy. Fertil Steril 2009.
Fertility and Sterility
927
incision without any complication. Microsurgical techniques during testicular biopsy have been used to identify testicular vessels on the surface of the tunica albuginea, reducing the incidence of complications compared with non-microscopic open biopsies (16). Our technique included the use of magnification, obviating scrotal violation. This procedure should be validated in a larger series and may be an attractive alternative to the traditional scrotal approach for testicular biopsy in azoospermic patients presenting with varicocele.
1. Kadioglu A, Tefekli A, Cayan S, Kandirali E, Erdemir F, Tellaloglu S. Microsurgical inguinal varicocele repair in azoospermic men. Urology 2001;57:328–33. 2. Matthews GJ, Matthews ED, Goldstein M. Induction of spermatogenesis and achievement of pregnancy after microsurgical varicocelectomy in men with azoospermia and severe oligoasthenospermia. Fertil Steril 1998;70:71–5. 3. Pasqualotto FF, Sobreiro BP, Hallak J, Pasqualotto EB, Lucon AM. Induction of spermatogenesis in azoospermic men after varicocelectomy repair: an update. Fertil Steril 2006;85:635–9. 4. Aboulghar MA, Mansour RT, Serour GI, Fahmy I, Kamal A, Tawab NA, et al. Fertilization and pregnancy rates after intracytoplasmic sperm injection using ejaculate semen and surgically retrieved sperm. Fertil Steril 1997;68:108–11. 5. Su LM, Palermo GD, Goldstein M, Veeck LL, Rosenwaks Z, Schlegel PN. Testicular sperm extraction with intracytoplasmic sperm
Cocuzza et al.
7. 8.
9.
10.
REFERENCES
928
6.
11. 12.
13.
14.
15. 16.
injection for nonobstructive azoospermia: testicular histology can predict success of sperm retrieval. J Urol 1999;161:112–6. Lee JS, Park HJ, Seo JT. What is the indication of varicocelectomy in men with nonobstructive azoospermia? Urology 2007;69:352–5. Prader A. Testicular size: assessment and clinical importance. Triangle 1966;7:240–3. World Health Organization. WHO laboratory manual for the examination of human semen and sperm-cervical mucus interaction. New York: Cambridge University Press, 1999. Marmar JL, Kim Y. Subinguinal microsurgical varicocelectomy: a technical critique and statistical analysis of semen and pregnancy data. J Urol 1994;152:1127–32. Posinovec J. The necessity for bilateral biopsy in oligo- and azoospermia. Int J Fertil 1976;21:189–91. Huyghe E, Matsuda T, Thonneau P. Increasing incidence of testicular cancer worldwide: a review. J Urol 2003;170:5–11. Nobert C, Goldstein M. Increased incidence of testicular cancer in men with infertility and abnormal semen analysis. Fertil Steril 2001; 76(Suppl 1):S50. Mancini M, Carmignani L, Gazzano G, Sagone P, Gadda F, Bosari S, et al. High prevalence of testicular cancer in azoospermic men without spermatogenesis. Hum Reprod 2007;22:1042–6. Leibovitch I, Baniel J, Foster RS, Donohue JP. The clinical implications of procedural deviations during orchiectomy for nonseminomatous testis cancer. J Urol 1995;154:935–9. Aitken RJ, Koopman P, Lewis SE. Seeds of concern. Nature 2004;432: 48–52. Dardashti K, Williams RH, Goldstein M. Microsurgical testis biopsy: a novel technique for retrieval of testicular tissue. J Urol 2000;163: 1206–7.
Subinguinal testis biopsy during varicocelectomy
Vol. 91, No. 3, March 2009