Persistent and Recurrent Postsurgical Varicoceles: Venographic Anatomy and Treatment with N-butyl Cyanoacrylate Embolization

Transcription

1 Persistent and Recurrent Postsurgical Varicoceles: Venographic Anatomy and Treatment with N-butyl Cyanoacrylate Embolization Daniel Y. Sze, MD, PhD, Jeffrey S. Kao, Joan K. Frisoli, MD, PhD, Stuart W. McCallum, MD, William A. Kennedy II, MD, and Mahmood K. Razavi, MD PURPOSE: To elucidate the mechanism of persistence or recurrence of varicoceles after surgical repair by examining the venographic anatomy, and to review the efficacy of treatment of these patients with n-butyl cyanoacrylate (NBCA) embolization. MATERIALS AND METHODS: From 2001 to 2007, 17 patients with persistent or recurrent varicoceles were studied by retrograde venography 4 months to 18 years after open surgical repair. All patients were then treated with NBCA glue embolization of the entire gonadal vein and the venographically identified duplications and collateral vessels, with three patients undergoing bilateral procedures. Venographic anatomy and clinical success were retrospectively analyzed. RESULTS: The majority of patients (65%) exhibited duplications draining into a single left gonadal vein. Duplications were most frequently found to be confined to the pelvis and inguinal canal. Communication with other retroperitoneal veins, including the renal hilar, lumbar, iliac, and circumaortic renal vein, was relatively uncommon. NBCA embolization effectively treated the main gonadal vein as well as the duplications and communications, with only one patient developing thrombophlebitic complications. CONCLUSIONS: Duplication of the gonadal vein in the pelvic or inguinal region with apparent incomplete ligation or resection is a common finding in patients with persistence or recurrence of varicocele after surgery. NBCA embolization effectively treats these duplicated vessels, resulting in a high rate of clinical success on short-term follow-up. J Vasc Interv Radiol 2008; 19: Abbreviation: NBCA n-butyl cyanoacrylate VARICOCELES have been recognized symptomatic, and are detectable in ap-anproximately adrenal metabolites from the left 40% of subfertile adult renal vein (7,8). as a major etiology of male infertility, testicular atrophy, and pain for moremale subjects and 15% of all adolescent Ablation was first promoted in the than a century 1 3). ( They are exceptionally male subjects. Left-sided involve- 1880s as an effective treatment for the common but not always ment is approximately 10 times morepain and subfertility associated with common than right-sided involvement, varicoceles (9). Current surgical tech- and isolated right-sided inniques include conventional open var- From the Division of Interventional Radiology volvement is rare. Unlike varicosities icocelectomy (retroperitoneal, inguinal, or subinguinal mass ligation or (D.Y.S., J.S.K., J.K.F., M.K.R.) and Department of of the lower extremities, varicoceles Urology (S.W.M., W.A.K.), Stanford University usually result from venous reflux artery-sparing ligation) and microsur- or laparoscopic varicocelectomy Medical Center, H-3646, 300 Pasteur Drive, Stanford, CA Received July 12, 2007; final revision caused by congenital absence of valvesgical received October 30, 2007; accepted November 7, rather than postthrombotic and postphlebitic complications. Resultant imtion rates continue to improve with (10). Although success and complica Address correspondence to D.Y.S.; dansze@stanford.edu paired fertility and testicular growth technical modifications, each of these From the SIR 2007 Annual Meeting. failure are usually blamed on in-approachecreased carries the risk of clinical intrascrotal temperature 4), ( failure or recurrence. Endovascular None of the authors have identified a conflict of interest. but the average increase is only 1 Ctreatment was reported in the late (5). Other proposed mechanisms of 1970s by several groups, and since SIR, 2008 DOI: /j.jvir damage include hypoxia from venous then, series as large as 5,500 patients hypertension (6) and reflux of renal have been reported (11). Clinical fail- 539

2 540 NBCA Embolization of Recurrent Postsurgical Varicoceles April 2008 JVIR ure or recurrence rates for surgery and endovascular treatment have been reported to be 1% 10% after 1 2 years, and the mechanism of failure is frequently ascribed to formation or preexistence of collateral pathways (8,12,13). We retrospectively evaluated the venous anatomy of patients referred for endovascular embolization after surgical failure or recurrence of varicocele. In addition, we reviewed the efficacy of n-butyl cyanoacrylate (NBCA) glue embolization in the treatment of these redundant vessels. Table 1 Type of Previous Surgical Varicocelectomy in Patients with Persistence or Recurrence of Varicocele Type Subinguinal Inguinal Retroperitoneal Mass ligation Artery sparing Microscopic artery sparing Laparoscopic Note. Surgical records were unavailable for two additional patients who each underwent two surgeries. MATERIALS AND METHODS Exemption from obtaining patient consent was obtained from our institutional review board for this retrospective analysis. Patient data were handled in compliance with the Health Insurance Portability and Accountability Act. Patient Demographics Diagnosis and grading of varicoceles was performed by one of three referring urologists and all patients underwent pre- and postsurgical ultrasound (US) examination. Varicoceles were graded on the standard scale on which a grade of 0 indicates that the varicocele is detectable by US only, a grade of 1 indicates that it is palpable with the Valsalva maneuver, a grade of 2 indicates that it is palpable without the Valsalva maneuver, and a grade of 3 indicates that it is visible through the scrotum (14). In the event of postsurgical persistence or later recurrence of varicocele, the patient was referred for venography and embolization. Seventeen patients were referred over a 66-month period from 2001 to 2007, nine for persistence and eight for recurrence. Four patients were referred for subfertility and 13 for pain. The embolization procedure was performed as soon as 4 months and as long as 18 years after surgical repair, with a mean of 29 months and a median of 14 months. In the group with recurrence after initial surgical success, the mean time elapsed between surgery and embolization was 48 months and the median time was 24 months. The patients ranged in age from 13 to 54 years, with a mean of 25 years and a median of 21 years. Two patients had each undergone two previous surgical varicocelectomies at Figure 1. Bahren et al (16) and Murray et al (12) classifications of varicocele anatomy. (a) According to the system of Bahren et al (16), type 0 anatomy shows no evidence of venous reflux on venography; type 1 anatomy shows reflux into a single gonadal vein without duplication; type 2 anatomy shows reflux into a single gonadal vein that communicates with accessory gonadal, lumbar, and/or iliac veins, or the vena cava; and type 3 anatomy shows reflux into a gonadal vein duplicated caudally, coalescing into a single trunk at the renal vein junction. Type 4 anatomy shows a competent valve at the renal/gonadal junction, but reflux into a renal hilar or capsular collateral vessel that communicates with the gonadal vein. Type 5 shows reflux into a gonadal vein that drains into a circumaortic renal vein. (b) According to the system of Murray et al (12), type R is renal, encompassing types 2 and 4 in the report of Bahren et al (16). Type S is scrotal, showing cross-scrotal collateral vessels. Type P is parallel, and subtype A shows duplication superior to the iliac crest, subtype B shows midretroperitoneal duplication between the iliac crest and pubic ramus, and subtype C shows duplication at or below the inguinal canal. other hospitals, but operative notes describing surgical technique were not available for them. The surgical histories of the other 15 patients are listed in Table 1. None underwent laparoscopic or retroperitoneal procedures, and all surgeries were artery-sparing. All surgeries were performed on the left side only for left-sided varicoceles. Eleven patients had grade 1 persistence or recurrence, two had grade 2 persistence or recurrence, and four had grade 3 persistence or recurrence. One patient had a concomitant grade 0 rightsided varicocele as well, but was referred for treatment of only the symptomatic left-sided recurrent varicocele. Embolization Procedure Different routes of venous access were employed by different practitioners. Most

3 Volume 19 Number 4 Sze et al 541 Figure 2. Variations of Bahren type 3 anatomy of the left gonadal vein. (a) Duplicated vein in the upper and lower retroperitoneal segments and inguinal segment, coalescing into a single vein draining into the left renal vein (not shown; type 3 by the classification of Bahren et al [16], type A by the classification of Murray et al [12]; overall type 3A). Note communication with collateral veins extending laterally over the ilium (arrows). (b) Glue cast after NBCA embolization in the patient in a shows occlusion of single trunk (arrowhead) and duplications. Note extension of NBCA into lateral branches identified by venography (arrows). (c) Duplication of the pelvic and inguinal segments (arrows) is seen coalescing into a single trunk draining into the renal vein (arrowhead; type 3 on Bahren et al [16] classification, type B on Murray et al [12] classification; overall type 3B). (d) Glue cast after NBCA embolization in the patient in c shows filling of pelvic vessels. patients treated earlier in the study period underwent right femoral puncture, but patients treated later more likely underwent right basilic or brachial vein puncture (15). Inferior vena cavograms and left renal venograms were obtained with use of pigtail catheters with patients in a 30 reverse Trendelenburg position with mild Valsalva maneuver breath-hold. Ten patients were treated through arm vein access, in which selection of the left gonadal vein was performed with a 5-F JB3 catheter (Cook, Bloomington, Indiana), and through it, a microcatheter (Rapid Transit; Cordis, Miami, Florida) was advanced to the inguinal canal. In seven patients, femoral access was obtained and Cobra 2 catheters (Cook) with coaxial microcatheters were used. Contrast medium was injected throughout the course of the gonadal vein to delineate duplications, collateral vessels, and connecting branches. The vessels within the inguinal canal were then occluded with embolization coils (Tornado; Cook) or by external manual compression by the patient himself. The most anxious patients required sedation and were unable to perform manual compression and therefore received coils. Nine patients were treated with NBCA only and eight patients were treated with NBCA and coils. NBCA glue (Trufill; Cordis) was mixed at a ratio of 1:3 by volume with Ethiodol (Savage Labs, Melville, New York) and then slowly injected through the microcatheter along the entire length of the gonadal vein starting just cephalad to the inguinal canal, with extra administration at venographically identified branch points to force NBCA into collateral vessels. When treating largervolume veins, the NBCA was cleared from the microcatheter with 5% dextrose solution. A maximum of 1 g of NBCA and 3 ml of Ethiodol were used for each vein. Underlying slow flow in the veins allowed polymerization of the

4 542 NBCA Embolization of Recurrent Postsurgical Varicoceles April 2008 JVIR Figure 3. Radiographic depiction of surgical sites and failure. (a) Retrograde venogram of the inguinal region of a patient with type 3B anatomy shows the site of ligation of the main gonadal vein (arrowhead) with persistent filling from two duplicated vessels (white arrows). Duplications started in the lower pelvic region (black arrow) and extended through the inguinal canal. (b) Retrograde venogram in a patient with type 3C anatomy shows a single collateral vessel (arrow) above the ligation site (arrowhead) in the inguinal canal. NBCA without substantial flow or reflux into the renal vein and pulmonary circulation. In three patients, including the one with a concomitant grade 0 right varicocele, reflux into the right gonadal vein was identified during cavography, and bilateral gonadal veins were treated with a 5-F MPA catheter (Cook) to engage the right gonadal vein from arm access or a Simmons 1 catheter from femoral access, in conjunction with a coaxial microcatheter. All patients with arm vein access were discharged within 1 hour and those with femoral access were discharged within 4 hours after completion of the procedure. All were prescribed a week-long course of nonsteroidal antiinflammatory medications. Follow-up with the referring urologists was performed by physical examination at a mean of 2.3 months and with supplemental US examination in equivocal cases. For those patients who were referred with subfertility issues, seminal parameters were obtained before and approximately 3 months after the embolization procedure, at the discretion of the urologist. Venographic anatomy was retrospectively classified according to the system of Bahren et al (16,17) and the system of Murray et al (12) as reviewed by a single reader (Fig 1). RESULTS The large majority of patients (11 of 17) exhibited Bahren type 3 left-sided venographic anatomy, with caudal duplications and collateral channels draining into a single gonadal vein at the left renal vein (Fig 2). Duplications were found most frequently in the pelvis and in the inguinal canal. In only four patients were the actual ligated veins identifiable; the other 13 veins were venographically indistinguishable from uninstrumented veins (Fig 3). Two patients exhibited type 1 anatomy (ie, single vessel without duplication), two exhibited type 2 anatomy (ie, communication with accessory gonadal, lumbar, iliac vein, or vena cava), one exhibited type 4 anatomy (ie, communication with renal hilar collateral vessel), and one exhibited type 5 anatomy (ie, circumaortic renal vein). The patients who had type 4 and type 5 anatomy also exhibited duplications in the retroperitoneum and pelvis similar to type 3 anatomy (Fig 4). None had type 0 anatomy (ie, no identified reflux). Two patients also showed venographic evidence of nutcracker compression of the left renal vein (one with type 2 anatomy, one with type 3 anatomy), but both denied symptoms of flank pain and hematuria and neither renal vein was treated. Of the three right gonadal veins that were also treated at the time of left-sided treatment, all three exhibited type 3 anatomy. Only one of these patients had documented grade 0 right-sided varicocele, but all three were treated because of the possibility of communication with and contribution to the left-sided varicocele, even though communications were not identified on venography (15). All 17 patients were available for follow-up at 6 months. Embolization was successful in reducing signs and symptoms in all patients. Only one patient had a clinically detectable but asymptomatic grade 1 persistent varicocele, which had decreased from a grade of 2. This patient developed a delayed pampiniform plexus thrombophlebitis 6 days after embolization after lifting heavy luggage on his way back to college. Symptoms resolved with cold packs, additional nonsteroidal antiinflammatory medications, and a 1-week course of oral cephalexin. He declined further imaging until 6 months later, did not exhibit a change in seminal parameters, and has not sought additional treatment. In the five patients who underwent serial seminal examinations, the preembolization motile sperm count was (mean SD), which in-

5 Volume 19 Number 4 Sze et al 543 Figure 4. Types 4 and 5 anatomy with concomitant type 3 duplication. (a) Tortuous collateral vessel from the renal hilum is shown feeding the gonadal vein with competent valve at the renal vein (arrowhead; Bahren et al [16] type 4 anatomy) with extensive upper and lower retroperitoneal duplication (type 4A). A 150-cm microcatheter was hubbed from the right brachial access without reaching the actual gonadal vein. (b) Glue cast after NBCA embolization shows multiple collateral branches filled with NBCA. (c) Composite image from venograms of upper and lower left renal veins in a patient with circumaortic left renal vein shows reflux into the gonadal vein from the lower vein (arrow; Bahren et al [16] type 5 anatomy). (d) Glue cast after NBCA embolization shows upper retroperitoneal duplication (type 5A). Table 2 Incidence of Bahren Anatomic Classes (16) in Patients Undergoing de novo Venography and in Our Cohort of Postsurgical Patients (%) Bahren Anatomic Type Sigmund et al (17), N 717 Wunsch and Efinger (11), N 2,047 creased to a postembolization count of DISCUSSION Branching and duplication of the gonadal veins have long been suspected as Lenz et al (21), N 386 Current Series, N * * Actual incidence of Bahren type 3 anatomy was not specified in the publication, but was calculated as the remainder after accounting for the other types, the incidences of which were specified. common anatomic factors contributing to the failure of surgical treatment of varicoceles (8,12,18). The presence and the actual number of duplicate veins are very difficult to assess at the time of surgery. Techniques to improve assessment at the time of surgery include direct injection venography (19), reverse Trendelenburg positioning, and temporary clamp occlusion of the main gonadal vein to cause increased turgor and flow through redundant or collateral channels (20). The possibility of preoperative venography is attractive but unrealistic. Catheter venography is routinely performed only at the time of embolization, and US, computed tomography, and magnetic resonance imaging lack the spatial resolution and sensitivity to detect these small and complex structures. In the early description of venographic classification of 717 varicoceles evaluated for sclerotherapy by Bahren et al (16) and Sigmund et al (17), the majority of patients (69%) had simple, single-vessel, duplication-free type 1 anatomy (Table 2). Of the types with duplications (types 2 5), each accounted for only about 2% 9% in their series,

6 544 NBCA Embolization of Recurrent Postsurgical Varicoceles April 2008 JVIR Table 3 Venographic Anatomy of Postsurgical Varicocele Recurrence (%) Anatomic Type (Bahren classification) (16) Punekar et al (24), N 33 Kattan (23), N 9 Feneley et al (27), N 18 Tefekli et al (22), N 36 Murray et al (12), N 26 Current Series, N NS Total, 85; A, 4; Total, 22; Total, 96; A, 12; 3 B, 57; C, 39* Total, 89; A, 100; Total, 100; individual B, 28; C, 60* Total, 65; A, 29; B, 0; C, 0* individual B, 57; C, 14* types, NS types, NS NS Previous surgery NS Laparoscopic High ligation Technical success of embolization Embolic material used Conventional repair Ligation Open inguinal or subinguinal 85 NP 78 NP Coils NP STS NP Detachable balloon Note. NS not specified, NP not performed; STS sodium tetradecyl sulfate. The classification of Bahren et al (16) was not universally used, so anatomic patterns were not differentiated in several reports. * When described in the original report, the Murray classification is also specified here as follows: A, high retroperitoneal; B, low retroperitoneal; C, inguinal. NBCA with 2.4% having type 3 anatomy. Similarly, in the large series of Wunsch and Efinger (11) in which 2,047 of 5,500 patients had anatomy classified, only 12.4% of patients exhibited type 3 anatomy, and in a series of 386 patients reported by Lenz et al (21), only 5.4% had type 3 anatomy. Our series differs from theirs in that all our patients have previously undergone surgical ligation. It is not surprising, then, that a larger proportion of our patients exhibited duplications. However, duplications of types 2, 4, and 5 were not common in our small series, but type 3 anatomy was pervasive (Table 2). Even the patients with type 4 and 5 anatomy exhibited concurrent type 3 duplication. Additionally, recognition and reporting of duplications may have been low in their series (11,21) because of limitations of imaging quality. Digital subtraction venography, which is more sensitive to small or superimposed duplications, was performed in all our patients, whereas all venographic examples shown in the reports of Bahren et al (16,17), Lenz et al (21), and Wunsch and Efinger (11) were unsubtracted images. The anatomic pattern of recurrence may reflect the surgical technique prevalent in a series (Table 3). The anatomic distribution of our series is in sharp contrast to that of Tefekli et al (22), who reported a 78% incidence of type 0 (ie, nonrefluxing) anatomy in their series of recurrent varicoceles. The series of Kattan (23) and Punekar et al (24) appear to show similar distributions of anatomic variants as our series, but the findings of Kattan et al (23) differ in that the duplications were found primarily more cranial in the retroperitoneum. This could reflect a higher site of ligation associated with laparoscopic surgery being prevalent in that series. Our pattern of distribution is more similar to the distribution reported by Murray et al (12), who also reported that 85% of their recognized duplications were found in the middle or lower segments of the gonadal vein. The original descriptions by Bahren et al (16) and Sigmund et al (17) emphasized duplications and communications in the retroperitoneum and diagrammed only single gonadal vessels in the inguinal region. Our findings suggest that duplications extending into or solely involving the sites of surgical ligation in or near the inguinal canal are a variation of the type 3 anatomy that forms the major population of our surgical failures. In fact, published venographic images from the early report of Sigmund et al (17) include images that clearly show duplication above and within the inguinal canal in a patient they classified as having type 1 (ie, nonduplicated) anatomy. Because the majority of surgical varicocele treatments are confined to the inguinal region, duplications here would have the greatest impact on immediate and delayed failure. Murray et al (12) addressed this issue by classifying parallel duplications as A high (ie, above the iliac crest), B middle (ie, between iliac crest and pubic ramus) and C low (ie, at or below the inguinal canal). With our hybridization of the systems of Bahren et al (16,17) and Murray et al (12), our patients with type 3 duplication had type 3A (28%), type 3B (57%), and 3C (14%) anatomy, with all type A duplications extending into the pelvis and almost all type B duplications extending into the inguinal region. Only six of the 14 veins with type 3 duplication had single veins within the inguinal canal. Numerous catheter-based technical methods to eliminate retrograde flow into the gonadal vein have been reported and adopted (25). Solid embolic

7 Volume 19 Number 4 Sze et al 545 materials such as metallic coils, detachable balloons, and gelatin sponge share the theoretical risk with surgery of missing duplicated and collateral vessels. Liquid embolic or sclerosing agents, such as NBCA, detergents (eg, ethanolamine oleate), alcohols (eg, polidocanol, ethanol), and boiling contrast media, have the theoretical advantage of distributing into branches and duplications if injected in sufficient quantity and at sufficient pressure. NBCA glue avoids some of the risks associated with lowviscosity liquids by solidifying quickly (26). This characteristic could reduce the likelihood of nontarget embolization in the presence of patient motion, respiration, change in position, or change of intraabdominal pressure. Some of the patients deemed not to be candidates for embolization in other reports because of complex anatomy (27,28) could probably be safely treated with NBCA. Nevertheless, one of our patients developed symptoms of delayed pampiniform thrombophlebitis 6 days after the embolization after lifting luggage, suggesting possible migration of the NBCA embolus or associated thrombus. Unfortunately, the patient refused additional imaging at the time, an issue that might be better addressed in a future prospective protocol. This article also has other limitations, including its retrospective nature with only short-term follow-up, small sample size, and heterogeneity of patient population, indications, and technical details of embolization procedures. In conclusion, redundancies of the gonadal veins confined to the region in or near the inguinal canal appear to be responsible for the majority of postsurgical persistent or recurrent varicoceles. NBCA is effective at embolizing these collateral and redundant vessels and may have certain advantages over other solid and liquid agents. References 1. World Health Organization. The influence of varicocele on parameters of fertility in a large group of men presenting to infertility clinics. Fertil Steril 1992; 57: Beddy P, Geoghegan T, Browne RF, Torreggiani WC. Testicular varicoceles. Clin Radiol 2005; 60: Ficarra V, Cerruto MA, Liguori G, et al. Treatment of varicocele in subfertile men: the Cochrane review a contrary opinion. Eur Urol 2006; 49: Ali JI, Weaver DJ, Weinstein SH, Grimes EM. Scrotal temperature and semen quality in men with and without varicocele. Arch Androl 1990; 24: Yamaguchi M, Sakatoku J, Takihara H. The application of intrascrotal deep body temperature measurement for the noninvasive diagnosis of varicoceles. Fertil Steril 1989; 52: Chakraborty J, Hikim AP, Jhunjhunwala JS: Stagnation of blood in the microcirculatory vessels in the testes of men with varicocele. J Androl 1985; 6: Peng BC, Tomashefsky P, Nagler HM. The cofactor effect: varicocele and infertility. Fertil Steril 1990; 54: Comhaire F, Kunnen M, Nahoum C. Radiological anatomy of the internal spermatic vein(s) in 200 retrograde venograms. Int J Androl 1981; 4: Barwell R. One hundred cases of varicocele treated by subcutaneous wire loop. Lancet 1885; 1: Turek PJ. Treatment of male infertility. In: Tanagho EA, McAninch JW, eds. Smith s general urology, 16th edition. New York: McGraw-Hill, Chapter Wunsch R, Efinger K. The interventional therapy of varicoceles amongst children, adolescents and young men. Eur J Radiol 2005; 53: Murray RR Jr, Mitchell SE, Kadir S. Comparison of varicocele anatomy following surgery and percutaneous balloon occlusion. J Urol 1986; 135: Kaufman SL, Kadir S, Barth KH, Smyth JW, Walsh PC, White RI Jr. Mechanisms of recurrent varicocele after balloon occlusion or surgical ligation of the internal spermatic vein. Radiology 1983; 147: Dubin L, Amelar RD. Varicocele size and results of varicocelectomy in selected subfertile men with varicocele. Fertil Steril 1970; 21: Pieri S, Agresti P, Fiocca G, Regine G. Phlebographic classification of anatomic variants in the right internal spermatic vein confluence. Radiol Med (Torino) 2006; 111: Bahren W, Lenz M, Porst H, Wierschin W. Side-effects, complications and contra-indications of percutaneous sclerotherapy of the internal spermatic vein for the treatment of idiopathic varicoceles. Fortschr Rontgenstr 1983; 138: Sigmund G, Bähren W, Gall H, Lenz M, Thon W. Idiopathic varicoceles: feasibility of percutaneous sclerotherapy. Radiology 1987; 164: Sofikitis N, Dritsas K, Miyagawa I, Koutselinis A. Anatomical characteristics of the left testicular venous system in man. Arch Androl 1993; 30: Gill B, Kogan SJ, Maldonado J, Reda E, Levitt SB. Significance of intraoperative venographic patterns on the postoperative recurrence and surgical incision placement of pediatric varicoceles. J Urol 1990; 144: Nyirady P, Kiss A, Pirot L, et al. Evaluation of 100 laparoscopic varicocele operations with preservation of testicular artery and ligation of collateral vein in children and adolescents. Eur Urol 2002; 42: Lenz M, Hof N, Kersting-Sommerhoff B, Bautz W. Anatomic variants of the spermatic vein: importance for percutaneous sclerotherapy of idiopathic varicocele. Radiology 1996; 198: Tefekli A, Cayan S, Uluocak N, Poyanli A, Alp T, Kadioglu A. Is selective internal spermatic venography necessary in detecting recurrent varicocele after surgical repair? Eur Urol 2001; 40: Kattan S. Incidence and pattern of varicocele recurrence after laparoscopic ligation of the internal spermatic vein with preservation of the testicular artery. Scan J Urol Nephrol 1998; 32: Punekar SV, Prem AR, Richorkar VR, Deshmukh HL, Kelkar AR. Post-surgical recurrent varicocele: efficacy of internal spermatic venography and steel-coil embolization. Br J Urol 1996; 77: Cornud F, Belin X, Amar E, Delafontaine D, Helenon O, Moreau JF. Varicocele: strategies in diagnosis and treatment. Eur Radiol 1999; 9: Pollak JS, White RI Jr. The use of cyanoacrylate adhesives in peripheral embolization. J Vasc Interv Radiol 2001; 12: Feneley MR, Pal MK, Nockler IB, Hendry WF. Retrograde embolization and causes of failure in the primary treatment of varicocele. Br J Urol 1997; 80: Marsman WP. The aberrantly fed varicocele: frequency, venographic appearance, and results of transcatheter embolization. AJR Am J Roentgenol 1995; 164: