Shunt-type and stop-type varicocele in adolescents: prognostic value of these two different hemodynamic patterns Mohammad Javad Mohseni, M.D., Hamid Nazari, M.D., Erfan Amini, M.D., Niloufar Javan-Farazmand, M.D., Arash Baghayee, M.D., Hossein Farzi, and Abdol-Mohammad Kajbafzadeh, M.D. Pediatric Urology Research Center, Children s Hospital Medical Center, Tehran University of Medical Sciences, Tehran, Iran Objective: To investigate different varicocele hemodynamic patterns (shunt type vs. stop type) as predictors of new-onset testicular hypotrophy or recurrence after varicocelectomy. Design: Prospective clinical study. Setting: Department of pediatric urology, children s hospital medical center. Patient(s): Seventy-four children and adolescents with varicocele. Intervention(s): Based on ultrasound findings, patients were classified into shunt-type or stop-type varicocele groups. All patients with stop-type varicocele and testicular volume discrepancy of R20% underwent retroperitoneal varicocelectomy and internal spermatic vein ligation. Patients with shunt-type varicocele and R20% testicular asymmetry were randomly divided to undergo either retroperitoneal varicocelectomy (ligation of internal spermatic vein) or inguinal varicocelectomy with ligation of both internal and external spermatic veins. Patients with testicular volume discrepancy of <20% were put on conservative management. Main Outcome Measure(s): Occurrence of new-onset asymmetry among untreated patients and recurrence rate among operated patients. Result(s): Patients with shunt-type varicocele who did not undergo surgery revealed a higher risk of developing asymmetry during follow-up (odds ratio 10.5). Ligation of both internal and external spermatic veins in shunttype patients was associated with significantly decreased rate of recurrence (6.3%) compared with retroperitoneal approach (30.8%). Conclusion(s): Shunt-type varicocele is associated with a higher risk of testicular hypotrophy among untreated patients. In addition, recurrence rate in shunt-type patients who underwent inguinal varicocelectomy was lower compared with retroperitoneal approach. (Fertil Steril Ò 2011;96:1091 6. Ó2011 by American Society for Reproductive Medicine.) Key Words: Adolescent, disease progression, recurrence, varicocele, ultrasonography Received April 24, 2011; revised July 15, 2011; accepted August 16, 2011; published online September 15, 2011. M.J.M. has nothing to disclose. H.N. has nothing to disclose. E.A. has nothing to disclose. N.J.-F. has nothing to disclose. A.B. has nothing to disclose. H.F. has nothing to disclose. A.-M.K. has nothing to disclose. Reprint requests: Abdol-Mohammad Kajbafzadeh, M.D., Professor of Urology, Pediatric Urology Research Center, Department of Pediatric Urology, Children s Hospital Medical Center, Tehran University of Medical Sciences, No. 32, Second Floor, 7th Street, Saadat-Abad Ave., Tehran 1998714616, Iran (E-mail: kajbafzd@sina.tums.ac.ir). Varicocele is a rare condition in the pediatric population; however, the prevalence of varicocele increases with age and reaches 15% in adolescent boys (1). Varicocele has been shown to be associated with a progressive decline in testicular function (2) and to impair rapid testicular growth at puberty (3, 4). Therefore, adolescents who are at greatest risk for infertility in adulthood should be offered early surgical varicocele repair. A variety of clinical and radiologic findings are available to predict which adolescents will experience damage of testicular growth and function; however, a consensus has yet to be reached. Presence of R10% testicular asymmetry has been reported to correlate with decreased sperm motility and concentration, and these findings were more dramatic when asymmetry was R20% (5). Testicular size discrepancy is reported to occur two times more frequently in infertile men with varicocele (6). Therefore, the presence of testicular asymmetry may serve as a marker to identify adolescents who are at greatest risk for future infertility. Although the treatment of varicocele in children and adolescents remains controversial, the most recent data consider testicular volume discrepancy of >20% to be the major indication for varicocelectomy (7). For older adolescents, semen analysis can be performed, and patients with abnormal semen analysis should be considered for surgical treatment regardless of testicular hypotrophy. Some radiologic findings can also predict adolescents who are at risk for testicular hypotrophy. Ultrasonography is a noninvasive diagnostic tool for evaluating varicoceles and has been recommended for evaluating infertile men with varicoceles when physical examination is inconclusive (8). In addition to the varicocele diagnosis, testicular size, maximal vein diameter (MVD) and different hemodynamic patterns can be recorded using Doppler ultrasound. In a recent study, peak retrograde flow (PRF) has been shown to be a valuable tool in predicting persistent, progressive, and new-onset testicular asymmetry (9). Hemodynamic patterns in varicoceles may also predict the occurrence of testicular hypotrophy and the possibility of recurrence after surgical repair. Two different hemodynamic patterns in varicoceles have been described on the basis of venographic and Doppler flow studies (10). These include stop-type and shunt-type varicoceles. Incompetence of venous valves at different levels in relation to the communicating veins causes these two subtypes of varicocele. 0015-0282/$36.00 Fertility and Sterility â Vol. 96, No. 5, November 2011 1091 doi:10.1016/j.fertnstert.2011.08.024 Copyright ª2011 American Society for Reproductive Medicine, Published by Elsevier Inc.
Insufficient distal valves allow spontaneous and continuous reflux from the internal spermatic vein into the orthograde draining (cremasteric and deferential) veins via collateral vessels. This hemodynamic pattern produces steady flow, both retrograde and orthograde, in Doppler ultrasound. The stop type of flow occurs in patients with competent valves above the level of communicating veins. This type allows only a brief period of reflux from the spermatic vein into the pampiniform plexus, and the reflux is stopped by a competent valve above the level of communicating veins (Fig. 1). In the present study, we investigated whether different varicocele hemodynamic patterns could be used as predictors of new-onset hypotrophy. Furthermore, we evaluated the effect of different surgical methods (ligation of internal spermatic vein vs. ligation of both internal and external spermatic veins) on recurrence rates in adolescent patients with shunt-type varicocele. MATERIALS AND METHODS Patients From March 2006 to December 2009, 42 consecutive adolescents with leftside shunt-type varicocele and 32 with stop-type varicocele were evaluated for varicocele repair. Physical examination and Doppler ultrasonography was performed in all patients. Varicocele was graded I to III according to the Dubin and Amelar clinical classification (11). Testicular dimensions were obtained by ultrasonography, and testicular volumes in ml were calculated using the formula length (cm) width height 0.71. MVD and PRF during valsalva maneuver were also calculated. All measurements were performed by a single radiologist. Based on ultrasound findings, patients were classified into shunt or stop-type varicocele subgroups. The varicocele was considered to be stop type when a decrescendo bruit appeared at the beginning of a valsalva maneuver, representing a short retrograde venous blood flow, and to be shunt-type when a continuous sound (steady flow) caused by both retrograde and orthograde flow was detected. If testicular volume measurements differed by R20%, patients were considered to have testicular asymmetry and deemed to be candidates of varicocelectomy. All patients with stop-type varicocele and testicular volume discrepancy of R20% (n ¼ 15) underwent internal spermatic vein ligation using retroperitoneal approach (group 1). Applying block randomization, patients with shunt-type varicocele and R20% testicular asymmetry (n ¼ 29) were divided into two groups. Retroperitoneal internal spermatic vein ligation was performed in 13 of 29 patients with shunt-type varicocele (group 2a), and both internal and external spermatic veins were ligated through an inguinal incision in the remaining 16 patients (group 2b). All surgeries were performed by a single pediatric urologist (A.K.) with the aid of magnification loupe to preserve the testicular artery and lymphatics. Patients were followed for R6 months, assessing for testicular size by ultrasonography and recurrence of varicocele. Patients who did not attend outpatient appointments were excluded from the study. Figure 2 shows a summary of the numbers of patients allocated to each ultimate treatment. Written informed consents were obtained from all parents. The study was conducted in accordance with the declaration of Helsinki, and our Institutional Review Board approved the study. Statistical Analysis Statistical analysis was performed using SPSS version 16 software. Comparison of quantitative data between study groups was performed using the t test, and when the data were not normally distributed according to the Kolmogorov-Smirnov test we applied the Mann-Whitney U test. Qualitative data were also compared using chi-square or Fisher exact test with two-tailed P<.05 considered to be statistically significant. RESULTS A total of 74 patients ages between 8 and 18 years (median 13; interquartile range 12 15) were enrolled in the study. Clinical examination revealed left-side grade I, II, and III varicoceles in 9 (12.2%), 35 (47.3%) and 30 (40.5%) patients, respectively. Shunt-type and stop-type varicoceles were evident in 42 and 32 patients, respectively. PRF, MVD, and varicocele grade was significantly higher in patients with shunt-type varicocele. Testicular volume asymmetry was also more frequent and severe in this subgroup of patients (Table 1). Median duration of follow up for patients in groups 1, 2a, and 2b were 15 (range 10 36), 12 (range 6 36), and 14 (range 6 36) months, respectively, and among 30 patients who did not require varicocele repair at presentation, 17 were followed for a median period of 12 months (range 9 24) to see if new asymmetry in testicular volume occurred. Among untreated patients, testicular volume asymmetry occurred in six patients with shunt-type (three patients with clinical grade II and three with clinical grade III varicocele) and two patients with stop-type varicocele (both with clinical grade II) during the follow-up period, whereas in the remaining nine (seven stop-type and two shunt-type patients) no asymmetry was noted. Thus, patients with shunt-type varicocele who did not undergo surgery revealed a higher risk of developing asymmetry during follow-up (odds ratio 10.5, 95% confidence interval 1.11 98.91; P¼.03). Although the baseline PRF in patients who showed testicular asymmetry was higher compared with patients who did not show asymmetry, this difference was not statistically significant. In addition, we could not find a prognostic role for baseline MVD, because this parameter did not differ significantly between patients with and without newonset asymmetry (Table 2). PRF increased from 14.8 13.1 to 23.4 11.9 cm/s (P¼.025 [paired t test]) in patients with shunttype varicoceles who were on conservative management, and it increased from 4.0 2.8 to 5.4 4.7 cm/s (P¼.515 [paired t test]) in patients with stop-type varicocele. All patients who underwent varicocelectomy were followed and evaluated for the recurrence of varicocele and resolution of testicular asymmetry. None of the patients with stop-type varicocele who underwent varicocelectomy showed recurrence during follow-up. Recurrence was noted in 4 of 13 patients (30.8%) in group 2a and 1 of 16 (6.3%) in group 2b (P¼.027). Baseline PRF, MVD, and age did not differ significantly between the patients with and without recurrence. In addition, resolution of testicular asymmetry was noted in 10 (66.7%), 9 (69.2%), and 13 (81.3%) patients of groups 1, 2a, and 2b, respectively (P¼.624). DISCUSSION Despite extensive study, the optimal treatment of varicocele in male adolescents remains controversial. Semen analysis cannot be performed in adolescents until they have progressed to the point in pubertal development necessary for adequate ejaculation. Sample procurement for semen analysis may also raise ethical questions. In addition, norms for adolescent semen parameters have not been established. Therefore, the testicular volume discrepancy has been considered to be the best criterion for testicular growth failure and future infertility, and based on guidelines, testicular hypotrophy is the major indication for varicocelectomy in adolescents. The presence of ipsilateral testicular hypotrophy may increase the risk of abnormal semen analysis and infertility in future. Diamond et al. reported abnormal sperm count in 11% and 59% of patients with testicular volume discrepancy of 10% 20% and >20%, respectively (5). Surgical repair of varicocele improves semen parameters in infertile men (12) and the prevalence of testicular catch-up growth has been reported to be as high as 80% after varicocelectomy (13 15). Patients with varicocele and no evidence of testicular hypotrophy may be eligible for a conservative nonsurgical 1092 Mohseni et al. Shunt-type vs. stop-type varicocele Vol. 96, No. 5, November 2011
FIGURE 1 (A) Schematic anatomy of the shunt-type varicocele shows incompetent valves and shunting through communicating veins, whereas in (B) stop-type varicocele the reflux in the spermatic vein is stopped by a competent valve. (C) Doppler ultrasound reveals reflux and increased venous diameter in a patient with shunt-type varicocele. (D) Stop-type varicocele is associated with slightly increased venous diameter. (E) Continuous and steady flow on bidirectional Doppler ultrasound is evident in shunt-type varicocele. (F) Stop-type varicocele is associated with a brief period of reflux on bidirectional Doppler ultrasound. Fertility and Sterility â 1093
FIGURE 2 Summary of the numbers of patients allocated to each ultimate treatment. approach. However, it should be considered that varicocele is a progressive disease and that the incidence of testicular hypotrophy increases with puberty (1). Among patients with no asymmetry at initial visit, Kozakowski et al. reported >50% progression to R10% asymmetry during a mean follow-up of 13.2 months (9). Therefore, conservative approach does not guarantee preservation of fertility, and patients who are selected for this approach should be monitored closely. TABLE 1 Comparison of baseline clinical and radiologic characteristics between shunt-type and stop-type varicocele. Stop-type Shunt-type P value PRF (cm/s), median (range) 2.0 (1 18) 8.1 (2.5 47) <.001 a MVD (mm), (mean SD) 2.64 2.00 3.71 1.25.006 b Grade I 7 (21.9%) 2 (4.8%) <.001 c II 25 (78.1%) 10 (23.8%) III 0 (0%) 30 (71.4%) Asymmetry R20% 15 (46.9%) 29 (69%).046 d <20% 17 (53.1%) 13 (31%) Size discrepancy (%) 14.6 29.3 28.0 35.8.090 b Note: MVD ¼ maximal vein diameter; PRF ¼ peak retrograde flow. a Mann-Whitney U test. b t test. c Pearson chi-square test. d Fisher exact test. 1094 Mohseni et al. Shunt-type vs. stop-type varicocele Vol. 96, No. 5, November 2011
TABLE 2 Comparison of different clinical and radiologic characteristics between patients with and without new-onset asymmetry during follow-up. Patients with new-onset asymmetry during follow-up Patients without new-onset asymmetry during follow-up P value Age 14.6 3.3 14 2.6.668 a Baseline PRF 12.4 14.0 6.1 5.3.230 a Final PRF 23.1 12.2 5.6 5.0.001 a MVD 2.75 0.91 2.07 1.31.238 a Grade I 0 3 (33.3%).048 b II 5 (62.5%) 6 (66.7%) III 3 (37.5%) 0 Type Shunt 6 (75%) 2 (22.2%).03 b Stop 2 (25%) 7 (77.8%) Note: MVD ¼ maximal vein diameter; PRF ¼ peak retrograde flow. a t test. b Pearson chi-square test. Several prognostic factors have been sought to predict progression of testicular asymmetry and occurrence of new asymmetry through time. Despite the limited role of color Doppler ultrasound in adults, it seems to be a useful tool for evaluation of varicocele in pediatric and adolescent patients. Color Doppler ultrasound not only can be used for accurate diagnosis and grading of adolescent varicocele, but also may be helpful in predicting occurrence of testicular hypotrophy, determining the type of treatment, and predicting the outcome of varicocelectomy (16 18). In the present study, we investigated the hemodynamic patterns of varicocele (shunt type vs. stop type), which are easily obtainable by Doppler ultrasound, and their ability to act as prognostic factors for occurrence of testicular asymmetry among patients on conservative management and recurrence after varicocele repair. To our knowledge there is no other study that evaluates the prognostic role of these hemodynamic patterns in varicocele patients. We noted that shunttype varicocele is associated with a high incidence of new-onset testicular hypotrophy. Given the high association between shunt-type varicocele and clinically high-grade disease, the importance of classification based on hemodynamic patterns may be questioned. Patients with clinical grade III varicocele present with shunt-type varicocele, and grade I varicocele is usually stop type. Nevertheless, a considerable number of stop-type patients presented with grade II varicocele, and among patients with grade II varicocele this classification may be of prognostic value. Two of nine patients (28.6%) with stop-type and grade II varicocele, showed new asymmetry during follow-up, whereas new asymmetry occurred in three of four (75%) grade II shunttype patients. Therefore clinical grade of varicocele does not seem to be a reliable prognostic factor to predict testicular growth arrest. Earlier authors have also shown that adolescent boys are at significant risk of testicular growth arrest and abnormal spermatogenesis regardless of varicocele grade (3, 19, 20). One shortcoming to the present study is the large drop-out rate among patients on the observation arm, which affects the power of study to compare prognostic value of shunt-type and stop-type grade II varicocele. However, loss to follow-up occurred with similar rates in shunt-type and stop-type patients, which may minimize the effect of the bias caused by high drop-out rate in comparing these two groups. In addition to the prognostic value of these hemodynamic patterns in predicting new asymmetry, we found a higher recurrence rate among shunt-type patients who underwent internal spermatic vein ligation compared with ligation of both internal and external spermatic veins, which supports the possible role of these hemodynamic patterns in planning surgery. The prognostic value of radiologic grading, MVD, and PRF, have been evaluated in several studies (9, 21, 22). An inverse relationship has been reported between MVD and different semen parameters. Studying 38 young men aged 17 19 years, Paduch and Niedzielski noted a significant linear negative relationship between sperm motility and pampiniform vein diameter (21).However, a study by Kozakowski et al. did not reveal MVD as a significant predictor of progression of testicular asymmetry in adolescent patients with varicocele (9). We also could not find a significant prognostic value for MVD to predict occurrence of asymmetry or recurrence after varicocele repair. Kozakowski et al. found that PRF was a potent tool for predicting persistent and progressive asymmetry and advocated surgical repair among patients with a left-side varicocele exhibiting PRF R38 cm/s (9). Similarly, Gitlin and McCullough found PRF >40 cm/s to be associated with abnormalities in semen analysis (22). Zampieri and Cervellione (16) used the Hirsch classification for grading varicocele (23) and suggested that grades II and III vein reflux (spontaneous venous reflux) are associated with the onset of testicular hypotrophy and abnormal semen analysis regardless of clinical grade of varicocele. They also recommended closer follow-up, i.e., every 6 months, for patients with spontaneous venous reflux. Retrograde flow may cause temperature increase in testes and exposure to toxic metabolites (24), and reversal of flow has been associated with significant improvement in sperm count and motility after varicocelectomy (25). High incidence of new onset testicular hypotrophy among shunt-type patients in the present study occurred regardless of baseline PRF values. Therefore, hemodynamic pattern (i.e., shunt-type vs. stop-type) may be a more potent prognostic factor than PRF. Fertility and Sterility â 1095
The mean baseline PRF in patients with new-onset asymmetry was 12.4 14.0 cm/s, which is quite lower compared with PRF values in Kozakowski et al. s study (9). This difference may be related to the patients position. A standing column of blood pooling in an upright patient may dampen the measured velocity. Although the prevalence of asymmetry was higher among patients with shunt-type varicocele in comparison with stop-type patients (69% vs. 46.9%, respectively), it is not expected for the stop-type patients to present with 46.9% asymmetry. Nevertheless it should be considered that our institution is a major referral center for pediatric urology, and many of these patients were referred to us by their primary care providers to determine if they required surgery. In addition testicular asymmetry is not necessarily associated with high grade or shunt-type varicocele and has been reported to occur in patients with subclinical varicocele (26) and up to 11% of adolescents without varicocele (20). At baseline, 15 of 32 patients with stop-type varicocele (46.9%) underwent varicocelectomy owing to testicular asymmetry, whereas during follow-up, asymmetry occurred in 2 of 9 patients with stop-type varicocele (22.2%). Reflux from the internal spermatic vein into the orthograde draining (cremasteric and deferential) veins occurs in shunt-type varicocele. The orthograde venous blood flow in this subtype of varicocele is similar to that of physiologic venous backflow from the testis and epididymis in the draining veins; however, the shunted blood volume exceeds the physiologic venous backflow. Therefore, over a period of time, draining deferential and cremasteric veins may become dilated and incompetent. This can explain the significant increase in PRF from 14.8 13.1 to 23.4 11.9 cm/s in our patients with shunt-type varicocele who were on conservative management. Preservation of these dilated and incompetent veins during varicocelectomy may be associated with recurrence of varicocele. Therefore, ligation of external spermatic veins in shunt-type varicocele through inguinal or subinguinal approach seems to be necessary to prevent persistence or recurrence of the disease. Schiff et al. reported the microsurgical subinguinal approach as a safe method with lower morbidity compared with retroperitoneal approach (27); however, microscopic dissection is more difficult in subinguinal approach compared with inguinal approach, because it is associated with a greater number of spermatic vessels (28). 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