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Correlation of ultrasound-measured venous size and reversal of flow with Valsalva with improvement in semen-analysis parameters after varicocelectomy
Correlation of ultrasound-measured venous size and reversal of flow with Valsalva with improvement in semen-analysis parameters after varicocelectomy We studied 68 men with varicoceles to determine preoperative parameters that are associated with improvements in semen analysis after varicocelectomy. Ultrasound-measured venous diameter and reversal of flow were found to correlate with successful outcome. (Fertil Steril威 2006;86:250 –2. ©2006 by American Society for Reproductive Medicine.)
Varicoceles are found in 35%– 40% of men with primary and 75%– 80% of men with secondary infertility, but in only 15% of the general population (1, 2). Venous dilation is thought to impair the countercurrent heat-exchange mechanism in the scrotum (3). Pooling of venous blood is likely to cause the increased intratesticular temperature and the progressive, duration-dependent decline in testis function that is observed in patients with varicocele (4, 5). Surgical ligation of varicoceles reduces intratesticular temperature to the normal range (6). This is accompanied by an improvement in semen parameters and Leydig cell function of the testis. Clinical size of varicoceles has been associated with the degree of response to varicocelectomy. Patients with larger varicoceles were found to have greater improvements in semen analysis parameters than men with smaller varicoceles (7). Jarow and coworkers found that semen analysis parameters improved in men with ultrasound-detected but clinically nonpalpable varicoceles and suggested a cutoff of a venous diameter of 3 mm (8). Other studies have found similar results, namely, that repair of ultrasound-detected but not clinically palpable varicoceles improves semen analysis parameters (9, 10). No objective preoperative measures correlate with improvement in semen parameters (7, 11, 12). Our study sought to determine whether preoperative venous diameter measured by high-resolution ultrasound with color-flow Doppler and/or reversal of flow with Valsalva predicted response to varicocelectomy.
tection of patient confidentiality. Specific Institutional Review Board approval was not obtained pursuant to institutional policies for a study of this type. Physical examination was performed in a warm room after the scrotum was treated with a heating pad. Varicoceles were graded clinically: grade 1—palpable impulse with Valsalva; grade 2— dilated and tortuous veins palpable; grade 3—veins visible through scrotal skin. Ultrasound was performed on men in whom a contralateral varicocele was suspected but unable to be adequately evaluated or to evaluate any other suspected pathologic finding. Serum FSH, LH, T, E2, and PRL levels were measured. Semen analysis was performed using 1992 World Health Organization criteria manually. Ultrasound was performed by designated radiology technicians, in the supine position as well as during the Valsalva maneuver. The largest vein identified during the supine, relaxed portion of the examination was measured. Reversal of venous flow with the Valsalva maneuver in the supine and upright positions was also noted. The criteria used by the Department of Radiology for a diagnosis of varicocele by ultrasound criteria alone included a venous diameter ⬎2.5 mm and/or reversal of flow.
Sixty-eight men with palpable varicoceles who underwent a high-resolution ultrasound with color-flow Doppler examination of the scrotum before microsurgical varicocelectomy were studied. We performed this study in accordance with institutional policies concerning the pro-
Microsurgical subinguinal varicocelectomy was performed in all patients as described elsewhere (13–15). Briefly, a subinguinal incision was made and the testis was delivered. Under microscopic magnification (15–24 power), all spermatic vein tributaries were doubly ligated with 3-0 silk ties after the testicular arteries were identified based on visible pulsation or pulsatile flow under the microscope. The vasal veins were preserved unless they were dilated and were larger than the spermatic veins.
Received May 20, 2005; revised and accepted December 14, 2005. Presented at the 2003 Annual Meeting of the American Urological Association, April 26 –30, 2003, Chicago, Illinois. Reprint requests: Jonathan D. Schiff, M.D., 1120 Park Avenue, New York, New York 10128 (FAX: 212-996-2506; E-mail: jonathandschiff@ hotmail.com).
The indication for repair was infertility with a varicocele in the setting of normal hormonal profile. All clinically palpable varicoceles were repaired. Subclinical right-sided varicoceles detected on ultrasound were repaired in cases of severe oligospermia (⬍5 ⫻ 106 sperm/mL) or with a grade 1 left varicocele and ⬍20 ⫻ 106 sperm/mL.
250
Fertility and Sterility姞 Vol. 86, No. 1, July 2006 Copyright ©2006 American Society for Reproductive Medicine, Published by Elsevier Inc.
0015-0282/06/$32.00 doi:10.1016/j.fertnstert.2005.12.038
Semen analysis was performed at a mean of 5 months postoperatively, and at least two specimens were available for each patient pre- and postoperatively. Statistical analysis used the Mann-Whitney U-test and 2 analysis for proportional data. Pre- and postoperative comparisons was performed using the Microsoft Excel spreadsheet program (Microsoft Corp., Redmond, WA). P⬍.05 was considered statistically significant. Mean age was 36.5 years (23–53 years), and mean testis size was 17.6 cm3 on the right and 16.1 cm3 on the left measured by orchidometer. On physical examination, 27 unilateral left, three unilateral right, and 38 bilateral varicoceles were detected. Serum hormone levels for the group were FSH ⫽ 9.9 IU/dL, LH ⫽ 5.9 IU/dL, T ⫽ 377.2 ng/dL, and estrogen ⫽ 29.2 ng/dL. Preoperative hormone levels were not significantly different between men whose semen parameters improved and those whose parameters did not. Mean preoperative sperm count was 21.3 ⫻ 106/mL, with a median of 16 ⫻ 106/mL and with 31.3% motile sperm (median, 40%) and 13.3% normal forms (median, 13.5%). Intragroup differences were not significant. Ultrasound detected 48 bilateral, 16 unilateral left, and two unilateral right varicoceles according to the radiologists’ criteria from the 68 men examined. Two men with clinical varicoceles had no reversal of flow and venous diameter ⬍2.5 mm. Forty-two men underwent bilateral and 26 underwent unilateral varicocelectomies, with one of the unilateral repairs for a right-sided varicocele only. Semen analysis parameters improved regardless of varicocele size; however, not all improvements reached statistical significance. For the cohort of 68 men there was a 75% (P ⫽ .005) increase in the median sperm count to 29 ⫻ 106/mL and a 40% (P ⫽ .01) improvement in median motility to 56% motility. Men who underwent varicocelectomy with the largest vein measuring ⬎3 mm had a significant improvement in
sperm count and motility (Table 1). However, those with varicoceles ⬍3 mm did not demonstrate a significant improvement. Preoperative ultrasound-measured reversal of flow with Valsalva also predicted success of varicocelectomy (Table 1). Fifty-three men had reversal of flow on preoperative ultrasound in one or both testicular veins, while only 15 men had no reversal of flow found. Significant improvements occurred in median sperm count (200%) and motility (55%) postoperatively in men with reversal of flow on ultrasound (Table 1). Men without reversal of flow had a modest improvement in motility that was not significant. The association of varicocele with infertility has been recognized for more than 50 years (16). Varicocele causes a duration-dependent decline in semen analysis parameters and in T production (17, 18). Several investigators evaluated preoperative varicocele parameters to try to predict response to varicocelectomy (11, 12). Repairing large, clinically palpable varicoceles results in a greater improvement in semen analysis parameters than repairing smaller varicoceles (7). Jarow et al. found that repairing subclinical, ultrasound-detected varicoceles also results in statistically significant improvements in semen analysis parameters but that repairing these varicoceles was less beneficial than repairing clinically detected varicoceles (7, 8). Other than clinical exam grade, objective preoperative predictors of successful varicocelecotomy are still lacking. The goal of our study was to determine whether the venous diameter of the largest testicular vein identified on ultrasound and reversal of flow with Valsalva were associated with response to varicocele ligation. We tested a cutoff of 3 mm based on the prior work of Jarow and others (8 –11) Our cohort of men was analyzed according to ultrasound-measured venous size and reversal of flow (Table 1). Reversal of flow with Valsalva was strongly associated with an improvement in postoperative semen analysis pa-
TABLE 1 Median pre- and postoperative semen analysis parameters for men with varicocele repairs stratified by largest venous diameter or reversal of flow measured on preoperative ultrasound. Count (ⴛ106)
Motility (%)
Morphology (% normal)
Vein size (mm)
n
Pre
Post
Pre
Post
Pre
Post
⬍3 ⱖ3 Reversal of flow Present Absent
27 41
15.5 9.5
27.5 29.5 (P ⫽ .008)
36 42.5
58 (P ⫽ .08) 65 (P ⫽ .05)
4 10.5
12 13
53 15
10 4
40 33
62 (P ⫽ .004) 45
10 0
14 7.5
30 (P ⫽ .003) 4
Note: Post ⫽ postoperative; Pre ⫽ preoperative. Schiff. Predictors of varicocelectomy outcome. Fertil Steril 2006.
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rameters. Reversal of flow predicted a statistically significant improvement in sperm count (200%) and motility (55%) on postoperative semen analysis. Absence of reversal of flow was associated with small, nonsignificant improvements in semen analysis. The pathophysiology of varicoceles is postulated to either be temperature elevation of the testes or exposure of the testes to toxic metabolites (4 – 6). Reversal of flow contributes to both of these mechanisms of testicular damage by impairing the countercurrent heat-exchange mechanism and by exposing the testis to retrograde blood flow, which could contain metabolites from the adrenal. We found that testicular venous size was associated with an improvement in semen analysis parameters after varicocele repair. Median sperm count (210%) and motility (53%) improved significantly for men with venous size ⬎3 mm who underwent varicocelectomy. Men with veins smaller than 3 mm did show improvements in parameters, but these did not reach significance. However, given the limited number of men with veins ⬍3 mm, the lack of significance is likely due to a lack of power to detect such a difference. Furthermore, given the large number of men with reversal of flow and the obvious importance of this parameter in determining outcome, this factor may have overwhelmed the venous size in terms of predicting outcome. Repairing varicoceles improves sperm count and motility. We believe that fixing varicoceles that are palpable or are greater than 3 mm or have reversal of flow with Valsalva on ultrasound maximizes the patient’s chance of improving after repair. Fixing ultrasound-detected veins without reversal of flow may not improve outcomes. Jonathan D. Schiff, M.D. Philip S. Li, M.D. Marc Goldstein, M.D. Center for Male Reproductive Medicine and Microsurgery, Cornell Institute for Reproductive Medicine and James Buchanan Brady Foundation Department of Urology, New York-Weill Cornell Medical Center, New York, New York
252
Schiff et al.
Correspondence
REFERENCES 1. Gorelick J, Goldstein M. Loss of fertility in men with varicocele. Fertil Steril 1993;59:613– 6. 2. Kim ED, Leibman BB, Brinblat DI, Lipshultz LI. Varicocele repair improves semen parameters in azoospermic men with spermatogenic failure. J Urol 1999;162:737– 40. 3. Dubin L, Amelar RD. Etiologic factors in 1294 consecutive cases of male infertility. Fertil Steril 1971;22:469 –74. 4. Zorgniotti AW, MacLeod J. Studies in temperature human sperm quality and varicocele. Fertil Steril 1973;24:854 – 63. 5. Goldstein M, Eid JF. Elevation of intratesticular and scrotal skin surface temperature in men with varicocele. J Urol 1989;142:743–7. 6. Wright EJ, Young GPH, Goldstein M. Reduction in testicular temperature after varicocelectomy in infertile men. Urology 1997;50: 257– 60. 7. Steckel J, Dicker A, Goldstein M. Relationship between varicocele size and response to varicocelectomy. J Urol 1993;149:769 –71. 8. Jarow J, Ogle S, Eskew LA. Seminal improvement following repair of ultrasound detected subclinical varicoceles. J Urol 1996;155:1287–90. 9. McClure RD, Hricak H. Scrotal ultrasound in the infertile man: detection of subclinical unilateral and bilateral varicoceles. J Urol 1986;135:711–5. 10. Pierik FH, Vreeburg JT, Stijnen T, van Roijen JH, Dohle GR, Lameris JS, et al. Improvement of sperm count and motility after ligation of varicoceles detected with colour Doppler ultrasonography. Int J Androl 1998;21:256 – 60. 11. Eskew LA, Bechtold R, Watson NE, Scharling E, Wolfman N, Jarow JP. Ultrasonographic diagnosis of varicoceles. Fertil Steril 1993;60: 693–7. 12. Takihara M, Ichikawa T, Shiseki Y, Nakamura T, Shimazaki J. Relationship between grade of varicocele and the response to varicocelectomy. Int J Urol 1996;3:282–5. 13. Goldstein M, Gilbert BR, Dicker AP, Dwosh J, Gnecco C. Microsurgical inguinal varicocelectomy with delivery of the testis: an artery and lymphatic sparing technique. J Urol 1992;148:1808 –11. 14. Marmar JL, Kim Y. Subinguinal microsurgical varicocelectomy: a technical critique and statistical analysis of semen and pregnancy data. J Urol 1994;152:1127–32. 15. Goldstein M. Surgical management of male infertility and other scrotal disorders. In: Walsh PC, Retik AB, Vaughan ED, Wein AJ, eds. Campbell’s urology. 8th ed. New York: Saunders, 2002:1532– 87. 16. Russell JK. Varicocele, age, and fertility. Lancet 1957;2:222–30. 17. Cheval MJ, Purcell MH. Deterioration of semen parameters over time in men with untreated varicocele: evidence of progressive testicular damage. Fertil Steril 1992;57:174 –7. 18. Su LM, Goldstein M, Schlegel P. The effect of varicocelectomy on serum testosterone levels in infertile men with varicoceles. J Urol 1995;154:1752– 6.
Vol. 86, No. 1, July 2006
Varicoceles are found in 35%– 40% of men with primary and 75%– 80% of men with secondary infertility, but in only 15% of the general population (1, 2). Venous dilation is thought to impair the countercurrent heat-exchange mechanism in the scrotum (3). Pooling of venous blood is likely to cause the increased intratesticular temperature and the progressive, duration-dependent decline in testis function that is observed in patients with varicocele (4, 5). Surgical ligation of varicoceles reduces intratesticular temperature to the normal range (6). This is accompanied by an improvement in semen parameters and Leydig cell function of the testis. Clinical size of varicoceles has been associated with the degree of response to varicocelectomy. Patients with larger varicoceles were found to have greater improvements in semen analysis parameters than men with smaller varicoceles (7). Jarow and coworkers found that semen analysis parameters improved in men with ultrasound-detected but clinically nonpalpable varicoceles and suggested a cutoff of a venous diameter of 3 mm (8). Other studies have found similar results, namely, that repair of ultrasound-detected but not clinically palpable varicoceles improves semen analysis parameters (9, 10). No objective preoperative measures correlate with improvement in semen parameters (7, 11, 12). Our study sought to determine whether preoperative venous diameter measured by high-resolution ultrasound with color-flow Doppler and/or reversal of flow with Valsalva predicted response to varicocelectomy.
tection of patient confidentiality. Specific Institutional Review Board approval was not obtained pursuant to institutional policies for a study of this type. Physical examination was performed in a warm room after the scrotum was treated with a heating pad. Varicoceles were graded clinically: grade 1—palpable impulse with Valsalva; grade 2— dilated and tortuous veins palpable; grade 3—veins visible through scrotal skin. Ultrasound was performed on men in whom a contralateral varicocele was suspected but unable to be adequately evaluated or to evaluate any other suspected pathologic finding. Serum FSH, LH, T, E2, and PRL levels were measured. Semen analysis was performed using 1992 World Health Organization criteria manually. Ultrasound was performed by designated radiology technicians, in the supine position as well as during the Valsalva maneuver. The largest vein identified during the supine, relaxed portion of the examination was measured. Reversal of venous flow with the Valsalva maneuver in the supine and upright positions was also noted. The criteria used by the Department of Radiology for a diagnosis of varicocele by ultrasound criteria alone included a venous diameter ⬎2.5 mm and/or reversal of flow.
Sixty-eight men with palpable varicoceles who underwent a high-resolution ultrasound with color-flow Doppler examination of the scrotum before microsurgical varicocelectomy were studied. We performed this study in accordance with institutional policies concerning the pro-
Microsurgical subinguinal varicocelectomy was performed in all patients as described elsewhere (13–15). Briefly, a subinguinal incision was made and the testis was delivered. Under microscopic magnification (15–24 power), all spermatic vein tributaries were doubly ligated with 3-0 silk ties after the testicular arteries were identified based on visible pulsation or pulsatile flow under the microscope. The vasal veins were preserved unless they were dilated and were larger than the spermatic veins.
Received May 20, 2005; revised and accepted December 14, 2005. Presented at the 2003 Annual Meeting of the American Urological Association, April 26 –30, 2003, Chicago, Illinois. Reprint requests: Jonathan D. Schiff, M.D., 1120 Park Avenue, New York, New York 10128 (FAX: 212-996-2506; E-mail: jonathandschiff@ hotmail.com).
The indication for repair was infertility with a varicocele in the setting of normal hormonal profile. All clinically palpable varicoceles were repaired. Subclinical right-sided varicoceles detected on ultrasound were repaired in cases of severe oligospermia (⬍5 ⫻ 106 sperm/mL) or with a grade 1 left varicocele and ⬍20 ⫻ 106 sperm/mL.
250
Fertility and Sterility姞 Vol. 86, No. 1, July 2006 Copyright ©2006 American Society for Reproductive Medicine, Published by Elsevier Inc.
0015-0282/06/$32.00 doi:10.1016/j.fertnstert.2005.12.038
Semen analysis was performed at a mean of 5 months postoperatively, and at least two specimens were available for each patient pre- and postoperatively. Statistical analysis used the Mann-Whitney U-test and 2 analysis for proportional data. Pre- and postoperative comparisons was performed using the Microsoft Excel spreadsheet program (Microsoft Corp., Redmond, WA). P⬍.05 was considered statistically significant. Mean age was 36.5 years (23–53 years), and mean testis size was 17.6 cm3 on the right and 16.1 cm3 on the left measured by orchidometer. On physical examination, 27 unilateral left, three unilateral right, and 38 bilateral varicoceles were detected. Serum hormone levels for the group were FSH ⫽ 9.9 IU/dL, LH ⫽ 5.9 IU/dL, T ⫽ 377.2 ng/dL, and estrogen ⫽ 29.2 ng/dL. Preoperative hormone levels were not significantly different between men whose semen parameters improved and those whose parameters did not. Mean preoperative sperm count was 21.3 ⫻ 106/mL, with a median of 16 ⫻ 106/mL and with 31.3% motile sperm (median, 40%) and 13.3% normal forms (median, 13.5%). Intragroup differences were not significant. Ultrasound detected 48 bilateral, 16 unilateral left, and two unilateral right varicoceles according to the radiologists’ criteria from the 68 men examined. Two men with clinical varicoceles had no reversal of flow and venous diameter ⬍2.5 mm. Forty-two men underwent bilateral and 26 underwent unilateral varicocelectomies, with one of the unilateral repairs for a right-sided varicocele only. Semen analysis parameters improved regardless of varicocele size; however, not all improvements reached statistical significance. For the cohort of 68 men there was a 75% (P ⫽ .005) increase in the median sperm count to 29 ⫻ 106/mL and a 40% (P ⫽ .01) improvement in median motility to 56% motility. Men who underwent varicocelectomy with the largest vein measuring ⬎3 mm had a significant improvement in
sperm count and motility (Table 1). However, those with varicoceles ⬍3 mm did not demonstrate a significant improvement. Preoperative ultrasound-measured reversal of flow with Valsalva also predicted success of varicocelectomy (Table 1). Fifty-three men had reversal of flow on preoperative ultrasound in one or both testicular veins, while only 15 men had no reversal of flow found. Significant improvements occurred in median sperm count (200%) and motility (55%) postoperatively in men with reversal of flow on ultrasound (Table 1). Men without reversal of flow had a modest improvement in motility that was not significant. The association of varicocele with infertility has been recognized for more than 50 years (16). Varicocele causes a duration-dependent decline in semen analysis parameters and in T production (17, 18). Several investigators evaluated preoperative varicocele parameters to try to predict response to varicocelectomy (11, 12). Repairing large, clinically palpable varicoceles results in a greater improvement in semen analysis parameters than repairing smaller varicoceles (7). Jarow et al. found that repairing subclinical, ultrasound-detected varicoceles also results in statistically significant improvements in semen analysis parameters but that repairing these varicoceles was less beneficial than repairing clinically detected varicoceles (7, 8). Other than clinical exam grade, objective preoperative predictors of successful varicocelecotomy are still lacking. The goal of our study was to determine whether the venous diameter of the largest testicular vein identified on ultrasound and reversal of flow with Valsalva were associated with response to varicocele ligation. We tested a cutoff of 3 mm based on the prior work of Jarow and others (8 –11) Our cohort of men was analyzed according to ultrasound-measured venous size and reversal of flow (Table 1). Reversal of flow with Valsalva was strongly associated with an improvement in postoperative semen analysis pa-
TABLE 1 Median pre- and postoperative semen analysis parameters for men with varicocele repairs stratified by largest venous diameter or reversal of flow measured on preoperative ultrasound. Count (ⴛ106)
Motility (%)
Morphology (% normal)
Vein size (mm)
n
Pre
Post
Pre
Post
Pre
Post
⬍3 ⱖ3 Reversal of flow Present Absent
27 41
15.5 9.5
27.5 29.5 (P ⫽ .008)
36 42.5
58 (P ⫽ .08) 65 (P ⫽ .05)
4 10.5
12 13
53 15
10 4
40 33
62 (P ⫽ .004) 45
10 0
14 7.5
30 (P ⫽ .003) 4
Note: Post ⫽ postoperative; Pre ⫽ preoperative. Schiff. Predictors of varicocelectomy outcome. Fertil Steril 2006.
Fertility and Sterility姞
251
rameters. Reversal of flow predicted a statistically significant improvement in sperm count (200%) and motility (55%) on postoperative semen analysis. Absence of reversal of flow was associated with small, nonsignificant improvements in semen analysis. The pathophysiology of varicoceles is postulated to either be temperature elevation of the testes or exposure of the testes to toxic metabolites (4 – 6). Reversal of flow contributes to both of these mechanisms of testicular damage by impairing the countercurrent heat-exchange mechanism and by exposing the testis to retrograde blood flow, which could contain metabolites from the adrenal. We found that testicular venous size was associated with an improvement in semen analysis parameters after varicocele repair. Median sperm count (210%) and motility (53%) improved significantly for men with venous size ⬎3 mm who underwent varicocelectomy. Men with veins smaller than 3 mm did show improvements in parameters, but these did not reach significance. However, given the limited number of men with veins ⬍3 mm, the lack of significance is likely due to a lack of power to detect such a difference. Furthermore, given the large number of men with reversal of flow and the obvious importance of this parameter in determining outcome, this factor may have overwhelmed the venous size in terms of predicting outcome. Repairing varicoceles improves sperm count and motility. We believe that fixing varicoceles that are palpable or are greater than 3 mm or have reversal of flow with Valsalva on ultrasound maximizes the patient’s chance of improving after repair. Fixing ultrasound-detected veins without reversal of flow may not improve outcomes. Jonathan D. Schiff, M.D. Philip S. Li, M.D. Marc Goldstein, M.D. Center for Male Reproductive Medicine and Microsurgery, Cornell Institute for Reproductive Medicine and James Buchanan Brady Foundation Department of Urology, New York-Weill Cornell Medical Center, New York, New York
252
Schiff et al.
Correspondence
REFERENCES 1. Gorelick J, Goldstein M. Loss of fertility in men with varicocele. Fertil Steril 1993;59:613– 6. 2. Kim ED, Leibman BB, Brinblat DI, Lipshultz LI. Varicocele repair improves semen parameters in azoospermic men with spermatogenic failure. J Urol 1999;162:737– 40. 3. Dubin L, Amelar RD. Etiologic factors in 1294 consecutive cases of male infertility. Fertil Steril 1971;22:469 –74. 4. Zorgniotti AW, MacLeod J. Studies in temperature human sperm quality and varicocele. Fertil Steril 1973;24:854 – 63. 5. Goldstein M, Eid JF. Elevation of intratesticular and scrotal skin surface temperature in men with varicocele. J Urol 1989;142:743–7. 6. Wright EJ, Young GPH, Goldstein M. Reduction in testicular temperature after varicocelectomy in infertile men. Urology 1997;50: 257– 60. 7. Steckel J, Dicker A, Goldstein M. Relationship between varicocele size and response to varicocelectomy. J Urol 1993;149:769 –71. 8. Jarow J, Ogle S, Eskew LA. Seminal improvement following repair of ultrasound detected subclinical varicoceles. J Urol 1996;155:1287–90. 9. McClure RD, Hricak H. Scrotal ultrasound in the infertile man: detection of subclinical unilateral and bilateral varicoceles. J Urol 1986;135:711–5. 10. Pierik FH, Vreeburg JT, Stijnen T, van Roijen JH, Dohle GR, Lameris JS, et al. Improvement of sperm count and motility after ligation of varicoceles detected with colour Doppler ultrasonography. Int J Androl 1998;21:256 – 60. 11. Eskew LA, Bechtold R, Watson NE, Scharling E, Wolfman N, Jarow JP. Ultrasonographic diagnosis of varicoceles. Fertil Steril 1993;60: 693–7. 12. Takihara M, Ichikawa T, Shiseki Y, Nakamura T, Shimazaki J. Relationship between grade of varicocele and the response to varicocelectomy. Int J Urol 1996;3:282–5. 13. Goldstein M, Gilbert BR, Dicker AP, Dwosh J, Gnecco C. Microsurgical inguinal varicocelectomy with delivery of the testis: an artery and lymphatic sparing technique. J Urol 1992;148:1808 –11. 14. Marmar JL, Kim Y. Subinguinal microsurgical varicocelectomy: a technical critique and statistical analysis of semen and pregnancy data. J Urol 1994;152:1127–32. 15. Goldstein M. Surgical management of male infertility and other scrotal disorders. In: Walsh PC, Retik AB, Vaughan ED, Wein AJ, eds. Campbell’s urology. 8th ed. New York: Saunders, 2002:1532– 87. 16. Russell JK. Varicocele, age, and fertility. Lancet 1957;2:222–30. 17. Cheval MJ, Purcell MH. Deterioration of semen parameters over time in men with untreated varicocele: evidence of progressive testicular damage. Fertil Steril 1992;57:174 –7. 18. Su LM, Goldstein M, Schlegel P. The effect of varicocelectomy on serum testosterone levels in infertile men with varicoceles. J Urol 1995;154:1752– 6.
Vol. 86, No. 1, July 2006