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Significance of Subclinical Varicocele Detected by Scrotal Sonography in Male Infertility: A Preliminary Report
0022-534 7/93/1504-1158$03.00/0 THE JOURNAL OF UROLOGY Copyright © 1993 by AMERICAN UROLOGICAL ASSOCIATION, INC.
Vol. 150, 1158-1160, October 1993
Printed in U. S.A.
SIGNIFICANCE OF SUBCLINICAL VARICOCELE DETECTED BY SCROTAL SONOGRAPHY IN MALE INFERTILITY: A PRELIMINARY REPORT NOBUYUKI KONDOH, NORIO MEGURO, KIYOMI MATSUMIYA, MIKIO NAMIKI,* HISAKAZU KIYOHARA AND AKIHIKO OKUYAMA From the Department of Urology, Osaka-Central Hospital and Osaka University Medical Sclwol, Osaka, Japan
ABSTRACT
To assess the clinical significance of subclinical right varicocele, · we used scrotal sonography for a prospective study of 68 infertile patients with a clinical left varicocele. A significant difference was found in the improvement in postoperative semen characteristics between sonographically diagnosed bilateral and unilateral groups. We conclude that a subclinical right varicocele is · also detrimental for spermatogenesis in patients with a clinical left varicocele. KEY WORDS: scrotum; ultrasonography; varicocele; infertility, male
Since the report by Tulloch of an azoospermic patient who achieved successful impregnation after bilateral varicocelec tomy, 1 scrotal varicocele has become widely recognized as a cause of male infertility. Recent progress in diagnostic methods has revealed a higher incidence of subclinical varicocele, the clinical significance of which is controversial in the field of male infertility. In 1970 Dubin and Amelar reported that the size of the varicocele is not related to improvement in postop erative semen characteristics. 2 Therefore, even a subclinical varicocele may be pathologically significant, although Dubin and Amelar did not subscribe to the possibility of the existence of a subclinical varicocele that could not be detected by careful palpation with Valsalva's maneuver. 3 Another point of interest in their report is a dramatic increase in the incidence of bilateral varicocele in infertile patients compared to that previously reported. 4 This increase is largely due to cases of previously overlooked right varicocele. As a result, the relationship be tween overlooked right varicocele and limited improvement in postoperative semen characteristics has become controversial. For this reason, a prospective study was done to assess the clinical significance of right subclinical varicocele. Scrotal so nography was used as the diagnostic technique to detect sub clinical varicocele because it is noninvasive and easy to perform.
Procedure of scrotal sonography. The patients were examined in the supine and upright positions during normal respiration and while performing Valsalva's maneuver. Imaging was ob tained by a balloon filled with water that was interposed between the transducer and scrotal skin, because it is fairly difficult to bring the transducer into direct contact with the scrotal skin. A longitudinal scan at the neck of the scrotum is the most convenient for good visualization of the venous chan nels in the case of a left clinical varicocele (fig. 1). For this reason imaging of a right subclinical varicocele was done at a point corresponding to that on the left side (figs. 2 and 3). Regarding the criteria for diagnosis of a varicocele, we adopted Rubin's classification, that is dilatation of the main diameter of the dominant vein during Valsalva's maneuver of more than 1.0 mm. compared to that in the relaxed upright position. 7 Several patients were also examined with Doppler ultrasonic sonography at the inguinal level. RESULTS
MATERIALS AND METHODS
Of our 64 infertile patients 8 were not evaluable. Of the remaining 56 patients 30 had a subclinical right varicocele as diagnosed by sonography and bilateral varicocele observed son ographically (group 1), while 26 showed no subclinical right varicocele but only a left varicocele was observed clinically and sonographically (group 2). We compared various parameters of
Accepted for publication March 26, 1993. * Requests for reprints: Department of Urology, Osaka University Medical School, 2-2 Yamada-Oka, Suita City, Osaka 565, Japan.
Fm. 1. Scrotal sonography of left clinical varicocele reveals obvious dilatation of main diameter of dominant vein (arrows). A, normal respiration. B, Valsalva's maneuver.
We studied 64 men 26 to 4 1 years old with normal function of the thyroid, adrenal and pituitary glands, and no evidence of sexual dysfunction but who had been infertile for at least 24 months. At least 3 semen specimens were examined at the initial visit, all of which showed a decreased sperm count (less than 40 X 106/ml.) and/or decreased sperm motility (less than 60% ). All patients had an idiopathic left varicocele clinically palpable with or without Valsalva's maneuver but no clinical right varicocele. Scrotal sonography was performed with B-mode gray scale ultrasound with a linear probe of 3.5 MHz. Regardless of the existence of right subclinical varicocele, high ligation of the left internal spermatic vein with a modified Palomo procedure5 was performed the next day. Changes in the semen characteristics, defined as sperm count and sperm motility, were assessed 3 months after surgical repair. A postoperative value was consid ered improved from the preoperative value if it was more than 2 standard deviations above the preoperative mean. 6 Statistical analysis was done with Wilcoxon's test and chi-square analysis.
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S UBCLINICAL VARICOCELE D ETECTED BY S O N O GRAPHY
deterioration in 20 (66.7%) in group 1, compared to 17 (65.4%) and 9 (34.6%), respectively, in group 2. These results also show a statistically significant difference between groups 1 and 2 (p <0.05, table 2). DISCUSSION
Fm. 2. Group 1 patient. Scrotal sonography of right side reveals dilatation of diameter of veins by more than 1.0 mm. (arrows) . Subclin ical varicocele was diagnosed according to our criteria. A, normal respiration . B, Valsalva's maneuver.
Fm. 3. Group 2. Dilatation of diameter of veins is not detected in scrotal sonography of right side. Arrows show dominant veins. A, normal respiration. B, Valsalva's maneuver.
the 2 groups (table 1). No significant differences were found in patient age, height, weight or Johnsen's score. The right testic ular volume was significantly smaller in group 1 than in group 2 (p <0.05). In regard to semen characteristics, no significant difference was found in preoperative values but the postopera tive sperm count was significantly lower in group 1 than in group 2 (p <0.05). Postoperative changes in the sperm count in group 1 showed improvement in 8 patients (26.7%). Group 2 showed improvement in 16 patients (61.5%), while in 10 the sperm count remained unchanged or worsened (38.5%). There fore, these results show a statistically significant difference between groups 1 and 2 (p <0.01). Similarly, sperm motility showed improvement in 10 patients (33.3%) and no change or
Group
No. Pts.
Although the pathophysiology of varicocele in male infertility remains unclear, varicocelectomy is the most widely used ther apeutic modality. Initial reports on clinical varicocele occurring mostly on the left side documented an average postoperative improvement in semen quality of almost 65 % .4• 8 Nevertheless, this figure showed room for improvement. Recent investigators have observed a higher incidence of bilateral varicocele9• 1 0 than the previously reported 15%. Dubin and Amelar found 50 to 60% of the varicoceles on palpation.3 McClure and Hricak, using scrotal sonography, found that 70% of the patients had bilateral varicocele.11 These increases in incidence are related to the progress made in diagnostic techniques, including Doppler sonography, scrotal ultrasound, scrotal thermography, radionuclide scanning and gonadal venography. These new diagnostic methods have given rise to the concept of an over looked right varicocele, whether subclinical or not, as a cause of the limited effectiveness of left varicocelectomy. We previously indicated the possibility that bilateral varico cele affected spermatogenesis more seriously than a unilateral varicocele, and mentioned the need for a prospective control study that would include subclinical varicoceles12 to investigate more precisely the 'relationship between varicoceles and im paired spermatogenesis. Consequently, we undertook this study using scrotal ultrasound, which is especially effective for screen ing, although reliability may be somewhat inferior to that of the Doppler method. 13 Similar to results in some recent reports, the incidence of bilateral varicocele established in our study is also surprisingly high (54 % ), although our criteria for subclinical varicocele may be too lenient. Nevertheless, it appears that the significant difference in right testicular volume between the 2 groups suggests the clinical significance of subclinical varicocele. How ever, at the same time no significant differences were found between the 2 groups in Johnsen's score for the right testis. Although a clear explanation of this discrepancy is difficult, the damaging effect to the right testis of left clinical varicocele may interfere with accurate information about the condition of the right testis. Therefore, the postoperative changes in various parameters, especially semen characteristics, should be examined for a comparison between the 2 groups. The significantly lower value of the postoperative sperm count for the subclinical group in our study may indicate the potential for improvement after ligation of the right subclinical varicocele. It should be noted in this connection that Yarborough et al demonstrated a small but significant increase in sperm count after occlusion of the subclinical varicocele. 14 Others have also reported improvement in semen quality resulting from corrected subclinical varico celes, although diagnostic techniques did not include sonogra phy.15, 16 With regard to the diagnostic techniques used, the reliability of scrotal sonography is controversial. The reliability of Doppler sonography is reported to be almost 90% that of
TABLE 1 . Age, testicular volume, Johnsen's score count and semen characteristics in 2 groups of patients Johnsen's Score Preop. Values Postop. Values Testicular Vol. (cc) Count Age (yrs.) Sperm Count Sperm Count* Sperm Sperm Rt. Lt. Rt.• Lt. (106/ml.) Motility ( % ) (106/ml.) Motility ( % ) 14.4 ± 13.2 8.4 ± 0.9 27.1 ± 20.8 8.6 ± 1.0 13.7 ± 1.4 25.2 ± 16.2 42.1 ± 17.9 13.9 ± 1.2 33.6 ± 3.6 20.5 ± 26.4 19.7 ± 18.8 8.4 ± 1.5 8.6 ± 1.2 43.8 ± 35.8 33.9 ± 3.7 14.6 ± 0.9 43.3 ± 25.8 14.1 ± 1.0
30 1 2 26 Values are means ± standard deviation. • p <0.05 (Wilcoxon test).
1 160 TABLE 2.
SUBCLINICAL VARICOCELE DETECTED BY SONOGRAPHY Effectiveness of varicocelectomy in 2 groups of patients Sperm Count (No. cases)*
Group
Improved
Sperm Motility (No. cases)t
Unchanged or Worse
22 8 1 10 16 2 * p <0.01 (chi-square analysis). t p <0.05 (chi-square analysis).
Improved 10 17
Unchanged or Worse 20 9
venography, 17 while scrotal sonography is not recommended for postoperative followup. We also used Doppler sonography in some cases and soon realized the need for a more skilled operator than in the case of scrotal sonography. We believe that the combined use of scrotal and Doppler sonography is the best choice. Although high resonance sonography, for example with a 7.5 to 10 MHz. transducer, is preferable, 3.5 MHz. proved to be sufficient for diagnosis of subclinical varicoceles according to the criteria used in our study. We conclude that subclinical varicoceles have a detrimental effect on spermatogenesis and may offer some explanation for the failure to obtain optimal results with a unilateral surgical approach during the last 30 years. In the future, we will ligate the right subclinical varicoceles of the patients in group 1 on the basis of the results of this study to obtain better semen characteristics. REFERENCES
1. Tulloch, W. S.: A consideration of sterility factors in the light of subsequent pregnancies. II. Subfertility in the male. Edinburgh Med. J., 59: 29, 1952. 2. Dubin, L. and Amelar, R. D.: Varicocele size and results of vari cocelectomy in selected subfertile men with varicocele. Fertil. Steril., 2 1: 606, 1970. 3. Amelar, R. D. and Dubin, L.: Therapeutic implications of left, right, and bilateral varicocelectomy. Urology, 30: 53, 1987.
4. Dubin, L. and Amelar, R. D.: Varicocelectomy as therapy in male infertility: a study of 504 cases. J. Urol. , 1 13: 640, 1975. 5. Palomo, A.: Radical cure of varicocele by a new technique: prelim inary report. J. Urol., 61: 604, 1949. 6. Tinga, D. J., Jager, S., Bruijnen, C. L. A. H., Kremer, J. and Mensink, H. J.: Factors related to semen improvement and fertility after varicocele operation. Fertil. Steril., 41: 404, 1984. 7. Orda, R., Sayfan, J., Manor, H., Witz, E. and Sofer, Y.: D iagnosis of varicocele and postoperative evaluation using inguinal ultra sonography. Ann. Surg., 206: 99, 1987. 8. Brown, J. S.: Varicocelectomy in the subfertile male: a ten-year experience with 295 cases. Fertil. Steril. , 27: 1046, 1976. 9. Narayan, P., Amplatz, K. and Gonzalez, R.: Varicocele and male subfertility. Fertil. Steril., 36: 92, 1981. 10. Cockett, A. T. K., Takihara, H. and Consentino, M. J.: The varicocele. Fertil. Steril., 4 1: 5, 1984. 11. McClure, R. D. and Hricak, H.: Scrotal ultrasound in the infertile man: detection of subclinical unilateral and bilateral varicoceles. J. Urol., 135: 711, 1986. 12. Kondoh, N., Koh, E., Matsui, T., Takeyama, M., Nakamura, M., Namiki, M., Fujioka, H., Kiyohara, H. and Okuyama, A.: Im provement of semen characteristics after surgical repair of bilat eral testicular varicocele as compared to unilateral varicocele patients. Arch. Androl., 24: 61, 1990. 13. Bock, E., Solivetti, F. M., D'Ascenzo, R., Rossi, P., Nero, G. F., Montagna, G. and Giovenco, P.: Echography in the study of varicocele: evaluation of reliability versus Doppler method. Rays, 13: 97, 1988. 14. Yarborough, M. A., Burns, J. R. and Keller, F. S.: Incidence and clinical significance of subclinical scrotal varicoceles. J. Urol., 141: 1372, 1989. 15. Bsat, F. A. and Masabni, R.: Effectiveness of varicocelectomy in varicoceles diagnosed by physical examination versus Doppler studies. Fertil. Steril., 50: 321, 1988. 16. Dhabuwala, C. B., Hamid, S. and Moghissi, K. S.: Clinical versus subclinical varicocele: improvement in fertility after varicocelec tomy. Fertil. Steril., 57: 854, 1992. 17. Basile-Fasolo, C., Izzo, P. L., Canale, D. and Menchini Fabris, G. F.: Doppler sonography, contact scrotal thermography and ve nography: a comparative study in evaluation of subclinical vari cocele. Int. J. Fertil., 30: 62, 1986.
Vol. 150, 1158-1160, October 1993
Printed in U. S.A.
SIGNIFICANCE OF SUBCLINICAL VARICOCELE DETECTED BY SCROTAL SONOGRAPHY IN MALE INFERTILITY: A PRELIMINARY REPORT NOBUYUKI KONDOH, NORIO MEGURO, KIYOMI MATSUMIYA, MIKIO NAMIKI,* HISAKAZU KIYOHARA AND AKIHIKO OKUYAMA From the Department of Urology, Osaka-Central Hospital and Osaka University Medical Sclwol, Osaka, Japan
ABSTRACT
To assess the clinical significance of subclinical right varicocele, · we used scrotal sonography for a prospective study of 68 infertile patients with a clinical left varicocele. A significant difference was found in the improvement in postoperative semen characteristics between sonographically diagnosed bilateral and unilateral groups. We conclude that a subclinical right varicocele is · also detrimental for spermatogenesis in patients with a clinical left varicocele. KEY WORDS: scrotum; ultrasonography; varicocele; infertility, male
Since the report by Tulloch of an azoospermic patient who achieved successful impregnation after bilateral varicocelec tomy, 1 scrotal varicocele has become widely recognized as a cause of male infertility. Recent progress in diagnostic methods has revealed a higher incidence of subclinical varicocele, the clinical significance of which is controversial in the field of male infertility. In 1970 Dubin and Amelar reported that the size of the varicocele is not related to improvement in postop erative semen characteristics. 2 Therefore, even a subclinical varicocele may be pathologically significant, although Dubin and Amelar did not subscribe to the possibility of the existence of a subclinical varicocele that could not be detected by careful palpation with Valsalva's maneuver. 3 Another point of interest in their report is a dramatic increase in the incidence of bilateral varicocele in infertile patients compared to that previously reported. 4 This increase is largely due to cases of previously overlooked right varicocele. As a result, the relationship be tween overlooked right varicocele and limited improvement in postoperative semen characteristics has become controversial. For this reason, a prospective study was done to assess the clinical significance of right subclinical varicocele. Scrotal so nography was used as the diagnostic technique to detect sub clinical varicocele because it is noninvasive and easy to perform.
Procedure of scrotal sonography. The patients were examined in the supine and upright positions during normal respiration and while performing Valsalva's maneuver. Imaging was ob tained by a balloon filled with water that was interposed between the transducer and scrotal skin, because it is fairly difficult to bring the transducer into direct contact with the scrotal skin. A longitudinal scan at the neck of the scrotum is the most convenient for good visualization of the venous chan nels in the case of a left clinical varicocele (fig. 1). For this reason imaging of a right subclinical varicocele was done at a point corresponding to that on the left side (figs. 2 and 3). Regarding the criteria for diagnosis of a varicocele, we adopted Rubin's classification, that is dilatation of the main diameter of the dominant vein during Valsalva's maneuver of more than 1.0 mm. compared to that in the relaxed upright position. 7 Several patients were also examined with Doppler ultrasonic sonography at the inguinal level. RESULTS
MATERIALS AND METHODS
Of our 64 infertile patients 8 were not evaluable. Of the remaining 56 patients 30 had a subclinical right varicocele as diagnosed by sonography and bilateral varicocele observed son ographically (group 1), while 26 showed no subclinical right varicocele but only a left varicocele was observed clinically and sonographically (group 2). We compared various parameters of
Accepted for publication March 26, 1993. * Requests for reprints: Department of Urology, Osaka University Medical School, 2-2 Yamada-Oka, Suita City, Osaka 565, Japan.
Fm. 1. Scrotal sonography of left clinical varicocele reveals obvious dilatation of main diameter of dominant vein (arrows). A, normal respiration. B, Valsalva's maneuver.
We studied 64 men 26 to 4 1 years old with normal function of the thyroid, adrenal and pituitary glands, and no evidence of sexual dysfunction but who had been infertile for at least 24 months. At least 3 semen specimens were examined at the initial visit, all of which showed a decreased sperm count (less than 40 X 106/ml.) and/or decreased sperm motility (less than 60% ). All patients had an idiopathic left varicocele clinically palpable with or without Valsalva's maneuver but no clinical right varicocele. Scrotal sonography was performed with B-mode gray scale ultrasound with a linear probe of 3.5 MHz. Regardless of the existence of right subclinical varicocele, high ligation of the left internal spermatic vein with a modified Palomo procedure5 was performed the next day. Changes in the semen characteristics, defined as sperm count and sperm motility, were assessed 3 months after surgical repair. A postoperative value was consid ered improved from the preoperative value if it was more than 2 standard deviations above the preoperative mean. 6 Statistical analysis was done with Wilcoxon's test and chi-square analysis.
1158
S UBCLINICAL VARICOCELE D ETECTED BY S O N O GRAPHY
deterioration in 20 (66.7%) in group 1, compared to 17 (65.4%) and 9 (34.6%), respectively, in group 2. These results also show a statistically significant difference between groups 1 and 2 (p <0.05, table 2). DISCUSSION
Fm. 2. Group 1 patient. Scrotal sonography of right side reveals dilatation of diameter of veins by more than 1.0 mm. (arrows) . Subclin ical varicocele was diagnosed according to our criteria. A, normal respiration . B, Valsalva's maneuver.
Fm. 3. Group 2. Dilatation of diameter of veins is not detected in scrotal sonography of right side. Arrows show dominant veins. A, normal respiration. B, Valsalva's maneuver.
the 2 groups (table 1). No significant differences were found in patient age, height, weight or Johnsen's score. The right testic ular volume was significantly smaller in group 1 than in group 2 (p <0.05). In regard to semen characteristics, no significant difference was found in preoperative values but the postopera tive sperm count was significantly lower in group 1 than in group 2 (p <0.05). Postoperative changes in the sperm count in group 1 showed improvement in 8 patients (26.7%). Group 2 showed improvement in 16 patients (61.5%), while in 10 the sperm count remained unchanged or worsened (38.5%). There fore, these results show a statistically significant difference between groups 1 and 2 (p <0.01). Similarly, sperm motility showed improvement in 10 patients (33.3%) and no change or
Group
No. Pts.
Although the pathophysiology of varicocele in male infertility remains unclear, varicocelectomy is the most widely used ther apeutic modality. Initial reports on clinical varicocele occurring mostly on the left side documented an average postoperative improvement in semen quality of almost 65 % .4• 8 Nevertheless, this figure showed room for improvement. Recent investigators have observed a higher incidence of bilateral varicocele9• 1 0 than the previously reported 15%. Dubin and Amelar found 50 to 60% of the varicoceles on palpation.3 McClure and Hricak, using scrotal sonography, found that 70% of the patients had bilateral varicocele.11 These increases in incidence are related to the progress made in diagnostic techniques, including Doppler sonography, scrotal ultrasound, scrotal thermography, radionuclide scanning and gonadal venography. These new diagnostic methods have given rise to the concept of an over looked right varicocele, whether subclinical or not, as a cause of the limited effectiveness of left varicocelectomy. We previously indicated the possibility that bilateral varico cele affected spermatogenesis more seriously than a unilateral varicocele, and mentioned the need for a prospective control study that would include subclinical varicoceles12 to investigate more precisely the 'relationship between varicoceles and im paired spermatogenesis. Consequently, we undertook this study using scrotal ultrasound, which is especially effective for screen ing, although reliability may be somewhat inferior to that of the Doppler method. 13 Similar to results in some recent reports, the incidence of bilateral varicocele established in our study is also surprisingly high (54 % ), although our criteria for subclinical varicocele may be too lenient. Nevertheless, it appears that the significant difference in right testicular volume between the 2 groups suggests the clinical significance of subclinical varicocele. How ever, at the same time no significant differences were found between the 2 groups in Johnsen's score for the right testis. Although a clear explanation of this discrepancy is difficult, the damaging effect to the right testis of left clinical varicocele may interfere with accurate information about the condition of the right testis. Therefore, the postoperative changes in various parameters, especially semen characteristics, should be examined for a comparison between the 2 groups. The significantly lower value of the postoperative sperm count for the subclinical group in our study may indicate the potential for improvement after ligation of the right subclinical varicocele. It should be noted in this connection that Yarborough et al demonstrated a small but significant increase in sperm count after occlusion of the subclinical varicocele. 14 Others have also reported improvement in semen quality resulting from corrected subclinical varico celes, although diagnostic techniques did not include sonogra phy.15, 16 With regard to the diagnostic techniques used, the reliability of scrotal sonography is controversial. The reliability of Doppler sonography is reported to be almost 90% that of
TABLE 1 . Age, testicular volume, Johnsen's score count and semen characteristics in 2 groups of patients Johnsen's Score Preop. Values Postop. Values Testicular Vol. (cc) Count Age (yrs.) Sperm Count Sperm Count* Sperm Sperm Rt. Lt. Rt.• Lt. (106/ml.) Motility ( % ) (106/ml.) Motility ( % ) 14.4 ± 13.2 8.4 ± 0.9 27.1 ± 20.8 8.6 ± 1.0 13.7 ± 1.4 25.2 ± 16.2 42.1 ± 17.9 13.9 ± 1.2 33.6 ± 3.6 20.5 ± 26.4 19.7 ± 18.8 8.4 ± 1.5 8.6 ± 1.2 43.8 ± 35.8 33.9 ± 3.7 14.6 ± 0.9 43.3 ± 25.8 14.1 ± 1.0
30 1 2 26 Values are means ± standard deviation. • p <0.05 (Wilcoxon test).
1 160 TABLE 2.
SUBCLINICAL VARICOCELE DETECTED BY SONOGRAPHY Effectiveness of varicocelectomy in 2 groups of patients Sperm Count (No. cases)*
Group
Improved
Sperm Motility (No. cases)t
Unchanged or Worse
22 8 1 10 16 2 * p <0.01 (chi-square analysis). t p <0.05 (chi-square analysis).
Improved 10 17
Unchanged or Worse 20 9
venography, 17 while scrotal sonography is not recommended for postoperative followup. We also used Doppler sonography in some cases and soon realized the need for a more skilled operator than in the case of scrotal sonography. We believe that the combined use of scrotal and Doppler sonography is the best choice. Although high resonance sonography, for example with a 7.5 to 10 MHz. transducer, is preferable, 3.5 MHz. proved to be sufficient for diagnosis of subclinical varicoceles according to the criteria used in our study. We conclude that subclinical varicoceles have a detrimental effect on spermatogenesis and may offer some explanation for the failure to obtain optimal results with a unilateral surgical approach during the last 30 years. In the future, we will ligate the right subclinical varicoceles of the patients in group 1 on the basis of the results of this study to obtain better semen characteristics. REFERENCES
1. Tulloch, W. S.: A consideration of sterility factors in the light of subsequent pregnancies. II. Subfertility in the male. Edinburgh Med. J., 59: 29, 1952. 2. Dubin, L. and Amelar, R. D.: Varicocele size and results of vari cocelectomy in selected subfertile men with varicocele. Fertil. Steril., 2 1: 606, 1970. 3. Amelar, R. D. and Dubin, L.: Therapeutic implications of left, right, and bilateral varicocelectomy. Urology, 30: 53, 1987.
4. Dubin, L. and Amelar, R. D.: Varicocelectomy as therapy in male infertility: a study of 504 cases. J. Urol. , 1 13: 640, 1975. 5. Palomo, A.: Radical cure of varicocele by a new technique: prelim inary report. J. Urol., 61: 604, 1949. 6. Tinga, D. J., Jager, S., Bruijnen, C. L. A. H., Kremer, J. and Mensink, H. J.: Factors related to semen improvement and fertility after varicocele operation. Fertil. Steril., 41: 404, 1984. 7. Orda, R., Sayfan, J., Manor, H., Witz, E. and Sofer, Y.: D iagnosis of varicocele and postoperative evaluation using inguinal ultra sonography. Ann. Surg., 206: 99, 1987. 8. Brown, J. S.: Varicocelectomy in the subfertile male: a ten-year experience with 295 cases. Fertil. Steril. , 27: 1046, 1976. 9. Narayan, P., Amplatz, K. and Gonzalez, R.: Varicocele and male subfertility. Fertil. Steril., 36: 92, 1981. 10. Cockett, A. T. K., Takihara, H. and Consentino, M. J.: The varicocele. Fertil. Steril., 4 1: 5, 1984. 11. McClure, R. D. and Hricak, H.: Scrotal ultrasound in the infertile man: detection of subclinical unilateral and bilateral varicoceles. J. Urol., 135: 711, 1986. 12. Kondoh, N., Koh, E., Matsui, T., Takeyama, M., Nakamura, M., Namiki, M., Fujioka, H., Kiyohara, H. and Okuyama, A.: Im provement of semen characteristics after surgical repair of bilat eral testicular varicocele as compared to unilateral varicocele patients. Arch. Androl., 24: 61, 1990. 13. Bock, E., Solivetti, F. M., D'Ascenzo, R., Rossi, P., Nero, G. F., Montagna, G. and Giovenco, P.: Echography in the study of varicocele: evaluation of reliability versus Doppler method. Rays, 13: 97, 1988. 14. Yarborough, M. A., Burns, J. R. and Keller, F. S.: Incidence and clinical significance of subclinical scrotal varicoceles. J. Urol., 141: 1372, 1989. 15. Bsat, F. A. and Masabni, R.: Effectiveness of varicocelectomy in varicoceles diagnosed by physical examination versus Doppler studies. Fertil. Steril., 50: 321, 1988. 16. Dhabuwala, C. B., Hamid, S. and Moghissi, K. S.: Clinical versus subclinical varicocele: improvement in fertility after varicocelec tomy. Fertil. Steril., 57: 854, 1992. 17. Basile-Fasolo, C., Izzo, P. L., Canale, D. and Menchini Fabris, G. F.: Doppler sonography, contact scrotal thermography and ve nography: a comparative study in evaluation of subclinical vari cocele. Int. J. Fertil., 30: 62, 1986.