Stesura Seveso 227Archivio Italiano di Urologia e Andrologia 2021; 93, 2 ORIGINAL PAPER No conflict of interest declared. After the physical exam, varicocele can be confirmed by CDUS (1) and CDUS may be required in the presence of factors interfering with physical examination. The aim of the current treatment is the ligation of inter- nal and external spermatic vein branches while preserv- ing all arterial structures, lymphatics and the vas defer- ens. In general, varicocelectomy is performed in patients with poor semen quality, providing improvement in semen parameters in 50-80% of the patients and, in addition, varicocele repair may result in improvements in natural pregnancy rates (2-6). There are studies on the optimal number of veins to be ligated, which varies upon the varicocelectomy technique, while there are not many studies on the parameters effectively predicting this number and on the correlation of surgical success with the number of ligated spermatic veins. In our study, we aimed to evaluate the correlation of pre-varicocelectomy physical examination findings and of CDUS measurement results with the number of inter- nal/external spermatic veins ligated during surgery and to analyze whether CDUS findings correlate with semen parameters. MATERIALS AND METHODS Patient population A total of 84 patients diagnosed with grade 3 left varico- cele in our clinic between November 15, 2016 and November 15, 2018 were evaluated. Patients over 18 years of age who had infertility or abnormal semen parameters or scrotal pain (resistant to medical treatment) with grade 3 left varicocele (visible and palpable spermat- ic veins without Valsalva maneuver at rest) were included in the study. Patients who were found to have missing data during data recording, evaluation or analysis, recur- rent cases with a history of varicocelectomy, patients with endovascular treatment history for varicose veins and patients under 18 years were excluded from the study. Study sesign The study was designed as a retrospective study. No patients underwent any additional tests or assessments Background: This study aimed to determine the contribution of color Doppler ultrasonog- raphy (CDUS) performed before varicocelectomy to the success of surgical treatment and to evaluate the correlation between CDUS findings and semen parameters. Methods: A total of 84 patients diagnosed with grade 3 left varicocele in our clinic between 2016 and 2018 were evaluated. The patients in whom the decision for varicocelectomy was based on only physical examination (PE) findings and abnormal semen analysis (SA) were defined as Group 1, while the patients under- going varicocelectomy based on PE, CDUS and SA findings were defined as Group 2. The patients diagnosed with varicocele based on PE and CDUS findings who were included in a follow- up protocol due to normal semen parameters were defined as Group 3. Results: In Group 1, there was a total of 28 patients and the mean number of ligated internal spermatic veins was 4.53 (range, 2-10). In Group 2, there was a total of 30 patients and the number of ligated internal spermatic veins was 3.76 (range, 1-8). No statistically significant difference was found between Group 1 and 2 in terms of the number of internal spermatic veins ligated during varicocelectomy. No statistically significant correlation was found between semen parameters and the num- ber of veins ligated during varicocelectomy in Group 1 and 2 and between semen parameters and CDUS findings group 2 and 3. Conclusions: In patients with primary grade 3 varicocele, diag- nosed by physical examination there is no need for additional imaging in primary cases. KEY WORDS: Varicocele; Varicocelectomy; Color Doppler ultra- sonography; Semen parameters; Number of vein ligated. Submitted 25 December 2020; Accepted 3 February 2021 INTRODUCTION Varicocele is defined as the dilatation of the veins of the pampiniform plexus. Diagnostic methods, including physical examination, Doppler stethoscope examination, thermography, color Doppler ultrasonography (CDUS), scintigraphy, and venography are used for the diagnosis of varicocele, although the current view is that physical examination is sufficient and additional imaging methods are not always required for the diagnosis of varicocele. Contribution of pre-varicocelectomy color Doppler ultrasonography finding to surgery and its correlation with semen parameters Caner Ediz 1, Muhammed Cihan Temel 1, Suna Şahin Ediz 2, Serkan Akan 1, Serkan Yenigürbüz 1, Mehmet Pehlivanoğlu 1, Ömer Yılmaz 1 1 Department of Urology, Sultan Abdulhamid Han Education and Research Hospital, Istanbul, Turkey; 2 Department of Radiology, Kartal Dr. Lutfi Kirdar City Hospital, Istanbul, Turkey. DOI: 10.4081/aiua.2021.2.227 Summary Archivio Italiano di Urologia e Andrologia 2021; 93, 2 C. Ediz, M. Cihan Temel, S. Şahin Ediz, S. Akan, S. Yenigürbüz, M. Pehlivanoğlu, Ö. Yılmaz 228 other than the evaluations performed for the diagnosis of varicocele in routine urologic practice (physical exami- nation, semen analysis and, if required, CDUS). All pro- cedures performed in this study were in accordance with the ethical standards of the institutional research com- mittee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. All participating patients gave written informed consent. In all patients, presence and localization of scrotal pain, presence of scrotal swelling, presence of infertility, varic- ocele grade, semen parameters (total sperm volume, total sperm count, sperm count per milliliter, ratio of forward moving sperms/motile sperms without progressive movement/immotile sperms, ratio of sperms with normal morphology, mean sperm velocity, ejaculate pH, pres- ence of pyospermia) and the number of internal/external spermatic veins ligated during varicocelectomy were recorded. Additionally, in accordance with the guideline recommendation, the width of the pampiniform venous plexus was evaluated with CDUS and the diameter of the varicose spermatic vein measured during the Valsalva maneuver was recorded in required patients. All semen analysis results were evaluated using the reference values defined by World Health Organization (WHO) in 2010. The time interval of two semen analysis for each patient was 15 days. The average of two semen analyzes for each patient was taken. SonoScape S40 CDUS system (Australia) was used in all patients undergoing CDUS. A 7.5 Mhz-linear probe was used during measurements. First, the testicular structure was examined using grayscale ultrasonography during normal respiration by elevating the chest and head region by 15° while the patients were in supine position. Testicular volume was measured by using the “prolate ellipse” formula (W x H x D x 0.52). Plexus pampini- formis veins were evaluated by identifying the most dilated vein and then measuring the increase in its diam- eter during the Valsalva maneuver. The presence of reflux was assessed using the color mode during normal respiration and the Valsalva maneuver. The patients in whom the decision for varicocelectomy was based on only physical examination (PE) findings and semen analysis (SA) were defined as Group 1, while the patients undergoing varicocelectomy based on PE, CDUS and SA findings were defined as Group 2. The patients diagnosed with varicocele based on PE and CDUS findings who were included in the follow-up pro- tocol due to normal semen parameters were defined as Group 3. Thus, it was planned to compare the contribu- tion of CDUS to varicocelectomy (between Group 1 and 2) and its correlation in patients with normal or abnor- mal semen parameters (between Group 2 and 3). There were 28, 30 and 26 patients in Group 1, 2, and 3, respectively. The patients in Group 1 and 2 underwent left subin- guinal varicocelectomy (the routine procedure in our clinic) for the diagnosis of grade 3 left varicocele. The patients undergoing varicocelectomy had at least two sperm parameter lower than the SA reference values defined by WHO or infertility. Varicocelectomy was not performed in patients with only scrotal pain and normal SA results. Subinguinal varicocelectomy was performed under spinal or general anesthesia. The testis was not routinely delivered from the scrotum and the visible external spermatic vein(s) and internal spermatic veins were ligated by preserving testicular arterial and lym- phatic vessels. The patients in Group 3 were enrolled into follow-up to control the changes in semen parameters at 6-month intervals. Study aim The study had two primary objectives. Firstly, we aimed to evaluate the adequacy of physical examination by investigating whether there was a statistically significant difference between Group 1 and 2 in terms of the num- ber of internal and external spermatic veins ligated dur- ing varicocelectomy and to assess the contribution of radiological imaging to the determination of the optimal number of spermatic veins to be ligated. In addition, we analyzed whether each of the recorded parameters of the patients were in correlation with the number of ligated external and internal spermatic veins. The second aim was to investigate the presence of a correlation between the maximum spermatic vein diameter measured using CDUS during the Valsalva maneuver and semen param- eters in Group 2 and 3 patients. We thereby aimed to evaluate the correlation between semen parameters and additional radiological imaging findings in patients with Grade 3 varicocele. Statistical analysis Statistical analyses were performed using SPSS Statistics 22.0 software (SPSS Inc., Chicago, IL, USA). The normal- ity hypothesis was tested using the Kolmogorov-Smirnov test during data analysis. Descriptive statistics for con- tinuous variables were presented as median and mini- mum-maximum values. The independent-samples t-test and Mann-Whitney U-test were used to analyze data not conforming to a normal distribution. Pearson and Spearman tests were used for correlation analyses. Statistical significance was defined as p < 0.05. RESULTS The median ages of the patients were 27.5 years (range, 22-39 years) in Group 1, 24.5 years (range, 19-39 years) in Group 2 and 26 years (range, 18-35 years) in Group 3. Regarding primary presenting complaints, testicular pain and scrotal swelling were present in 39.28% (11/28) and 39.28% (11/28) of the patients in Group 1, respectively; in 53.33% (16/30) and 30% (9/30) of the patients in Group 2, respectively; and in 69.23% (18/26) and 30.77% (8/26) of the patients in Group 3, respec- tively. Infertility was the presenting complaint in 25% (7/28) and 16.66% (5/30) of the patients in Group 1 and 2, respectively. In Group 1, there was a total of 28 patients and the total number of ligated internal spermatic veins was 127. The median number of ligated internal spermatic veins was 4 (range, 2-10) in Group 1. In Group 2, there were a total of 30 patients and the total number of ligated internal spermatic veins was 113. The median number of ligated internal spermatic veins was 4 (range, 1-8) in Group 2. No statistically significant difference was found between Group 1 and 2 in the number of internal spermatic veins ligated during varicocelectomy (p = 0.114) (Table 1). The total number of ligated external veins was 17 and the median number was 0 (range, 0-2) in Group 1. A total of 16 external spermatic veins were ligated and the median number of ligated external spermatic veins was 0 (range, 0-2) in Group 2. No statistically significant dif- ference was found between Group 1 and 2 in terms of the number of external spermatic veins ligated during varicocelectomy (p = 0.845) (Table 1). A statistically significant positive correlation was found between the number of internal spermatic veins and the number of external spermatic veins ligated during varic- ocelectomy in Group 1 and 2 (p = 0.023 and p = 0.049). However, a correlation analysis between the numbers of ligated internal and external spermatic veins and semen parameters found no statistically significant correlation in either groups (p > 0.05) (p and r values) (Table 2). In Group 2, a correlation analysis was conducted to examine the correlation of the maximum spermatic vein diameter measured by CDUS during the Valsalva maneu- ver with semen parameters and the number of ligated external and internal spermatic veins. In conclusion, the maximum spermatic vein diameter measured during the Valsalva maneuver was not significantly correlated with any of the semen parameters or the numbers of ligated external and internal spermatic veins (p > 0.05) (p and r values) (Table 3). In Group 3, there was also no statistically significant cor- relation between semen parameters and the maximum spermatic vein diameter measured during the Valsalva maneuver (p > 0.05). DISCUSSION Varicocele is the most common correctable cause of male infertility (7). Approximately 19-41% of the patients pre- senting with primary infertility are diagnosed with varic- ocele (8, 9), while this rate ranges from 45% to 81% in patients presenting with secondary infertility (9). The most likely cause of impaired spermatogenesis is testicu- lar hyperthermia associated with varicocele, while increased reactive oxygen products and apoptosis are closely related to the pathophysiology of varicocele (7). Varicocele is usually asymptomatic but testicular pain may be the first presenting symptom in 10% of the patients. It is usually unilateral. Surgical treatment is extremely successful and relieves pain in 90% of the patients in cases where chronic testicular pain etiologi- cally determined to be caused by varicocele is not relieved by conservative treatment (10). CDUS may have a role in the possible differential diagnoses particularly in cases of unexplained scrotal pain. Raghavendran et al. (11) reported that severe testicular pain in a patient diag- 229Archivio Italiano di Urologia e Andrologia 2021; 93, 2 Varicocele and color Doppler ultrasonography Table 1. No statistically significant difference was found between Group 1 and 2 in the number of internal and external spermatic veins ligated during varicocelectomy (p > 0.05). Group 1 (n = 28) Group 2 (n = 30) p value Median (min-max) Median (min-max) Internal spermatic vein 4 (2-10) 4 (1-8) 0.114 External spermatic vein 0 (0-2) 0 (0-2) 0.845 Table 2. Correlation Analysis between semen parameter results and the numbers of ligated internal and external spermatic veins in Group 1 and 2. No positive correlation was found between any of the parameters evaluated in semen analysis and the number of ligated veins (p > 0.05). Semen analysis results P-values for the correlation analysis between semen analysis and the number of ligated internal and external spermatic veins in Group 1 and 2 Group 1 (n = 28) Group 2 (n = 30) Group 1 Group 1 Group 2 Group 2 Median (min-max) Median (min-max) Internal spermatic vein External spermatic vein Internal spermatic vein External spermatic vein Semen volume (ml) 2.3 (1-5) 3 (1-5) 0.59 0.08 0.25 0.54 Sperm count (106/ml) 27.45 (0-127) 13.2 (0-89.6) 0.28 0.42 0.98 0.32 Total sperm count (x106) 75 (0-345) 46 (0-224) 0.46 0.42 0.78 0.24 Forward moving (%) 23 (0-75.4) 23 (0-60) 0.23 0.78 0.85 0.31 Motile without progressive movement (%) 17.81 (0-62.3) 21.1 (0-39) 0.74 0.42 0.16 0.66 Immotile (%) 49.5 (0-78) 50 (0-95) 0.75 0.5 0.98 0.34 Morphology (%) 8 (0-34) 4 (0-20) 0.45 0.181 0.57 0.21 Table 3. Correlation analysis between semen parameters and spermatic vein diameters measured by CDUS in Group 2 and 3. No positive correlation was found between any of the parameters evaluated in semen analysis and spermatic vein diameter (p > 0.05). P-values for the correlation analysis between semen analysis results and spermatic vein diameters measured by CDUS in Group 2 and 3 Spermatic vein diameter Semen volume Sperm count Total Forward Motile without Immotile Morphology measured by CDUS sperm count moving progressive Median (mm) (min-max) movement Group 2 (n = 30) 3.8 (2.8-7) 0.99 0.96 0.78 0.57 0.055 0.98 0.37 Group 3 (n = 26) 2.9 (2.3-4) 0.54 0.56 0.85 0.9 0.4 0.68 0.9 Archivio Italiano di Urologia e Andrologia 2021; 93, 2 C. Ediz, M. Cihan Temel, S. Şahin Ediz, S. Akan, S. Yenigürbüz, M. Pehlivanoğlu, Ö. Yılmaz 230 nosed with varicocele was due to a thrombus in a vari- cose vein. Presenting complaints may include promi- nence of testicular vessels and feeling of unilateral scro- tal swelling in addition to testicular pain. The dilatation of spermatic veins causes an increase in the temperature in the testicles and scrotum. This increase in temperature may cause a progressive dysfunction in the testicles and epididymis, leading to infertility (12, 13). In our clinical practice, patients with the diagnosis of varicocele with- out any pathology in semen parameters are offered con- servative treatments (use of analgesics or palliative treat- ment recommendations for pain relief) and follow up at 3-6-month intervals. We perform surgery in cases with- out relief of testicular pain with conservative treatment. The diagnosis of varicocele is based on physical exami- nation without any need for additional tests. In a study by WHO, it was demonstrated that 70% of patients were diagnosed with varicocele using venography, while in the same patients this rate was 30-40% with physical examination and physical examination had a false posi- tive rate of 23%. However, the sensitivity and specificity of physical examination in the diagnosis of varicocele were reported to be 71% and 69%, respectively (14-16). We aimed to eliminate this false negativity effect by including patients with Grade 3 varicocele in our study group. Urology guidelines try to minimize this margin of error by recommending the confirmation by CDUS of the diagnosis of varicocele made by physical examina- tion. The benefit of additional diagnostic imaging methods usually does not go beyond supporting the diagnosis, while these methods are still used in the clinical practice of urologists. Unfortunately, the contribution of these methods in the evaluation of testicular volume and determination of venous reflux in adult patients is not substantial as in pediatric patients (17). Moreover, it contributes to the determination of surgical technique in adolescent varicocelectomy but not in adult varicocelec- tomy (18). We use CDUS in our practice particularly in patients with pathologies interfering with varicocele evaluation (e.g., scrotal edema, cellulitis or prior scrotal surgery), patients with recurrent varicocele and morbid obese patients. However, additional imaging methods revealed no additional result other than supporting the diagnosis and/or establishing differential diagnosis. It should be kept in mind that CDUS used in the diagnosis of varicocele is affected by many factors. Poor quality of the measuring device causes false-negative diagnoses and excessive mobility of the spermatic cord vessels leads to false-positive diagnoses (19). The employed technique is another influential factor. Measurements taken in the standing position are diagnostically more successful compared to the measurements taken in the lying or backward-leaning position (20). The caput of the epi- didymis is the most suitable region for optimal success of ultrasonographic measurements in varicocele evaluation (21). In analyses evaluating the success of ultrasonogra- phy, the sensitivity and specificity of color Doppler ultra- sonography in the diagnosis of varicocele were 97% and 94%, respectively (22). Color Doppler examination has a higher sensitivity and specificity and a lower cost com- pared to thermography and angiography and is a non- invasive evaluation method and the procedure of choice in the diagnosis of venous reflux in varicocele (23). Physical examination remains the most valuable method (24, 25), in fact our study found no statistically signifi- cant difference between the patients who were diagnosed via physical examination and the patients whose diag- noses were supported by CDUS in terms of the numbers of internal and external spermatic veins ligated during varicocelectomy and we concluded that additional imag- ing had no additional predictive value compared to physical examination in the determination of the number of spermatic veins to be ligated during varicocelectomy in patients with Grade 3 varicocele. We therefore do not think that CDUS should be used as a routine method. In contrast to the failure in predicting the number of vessels ligated during varicocelectomy, there are studies in the literature reporting that there is a correlation between CDUS findings and semen parameters and/or infertility. Mahdavi et al. reported that semen volume, sperm count and sperm motility and morphology correlated with CDUS findings in patients with varicocele (26). In our study, the maximum spermatic vein diameter measured during the Valsalva maneuver by CDUS was not signifi- cantly correlated with any of the sperm parameters or the numbers of ligated external and internal spermatic veins in Group 2. Based on the results of our study, CDUS per- formed in addition to physical examination for the diag- nosis of varicocele has no contribution to the interpreta- tion of sperm parameters or to the prediction of the number of spermatic veins that should be ligated during the operation. Retroperitoneal, laparoscopic, inguinal and subinguinal methods have been described for the treatment of varico- cele. In recent years, studies showed that robot-assisted microscopic varicocelectomy is as successful as the con- ventional methods (27). However, microscopic subin- guinal varicocelectomy is the golden standard for the treatment of varicocele (28, 29). This method includes the treatment of venous system by preserving testicular arteri- al and lymphatic vessels. In conventional varicocelectomy performed without using a microscope or optic magnifier, the most important cause of recurrence after the treatment of varicocele is the inability to ligate the small internal spermatic vein branches due to their invisibility to the naked eye (30). In the literature, it is reported that intra- operative indocyanine green administration is one of the ways of increasing the success of this technique and min- imizing testicular artery injuries (29). Another method is the use of intraoperative microvascular Doppler ultra- sonography (10). In a study evaluating 65 patients under- going microsurgical subinguinal varicocelectomy at vari- ance analysis, only the number of ligated veins 4 mm or more in diameter was higher in grade 3 varicoceles than in grade 1 and 2 varicoceles and the increase in varicocele grade was not related to the total number of ligated veins (31). In a new study, Babai et al. was reported that the presence of testicular reflux has no effect on semen analy- sis parameters, but also does not predict the consequences of varicocelectomy and therefore is not a suitable progno- sis factor in varicocele patients (32). Also in our study, there was no statistically significant correlation between varicocele grade on physical examination or CDUS find- 231Archivio Italiano di Urologia e Andrologia 2021; 93, 2 Varicocele and color Doppler ultrasonography ings (diameter of the vein or presence of reflux) and the total number of ligated spermatic veins. Outcomes of this study are different from those of previous studies of Belani et al. (31) and Mahdavi et al. (26), but similar to the results of Babai et al. (32). Based on statistical results, we have not found any radi- ological data that predict sperm parameters or the num- ber of internal and external spermatic veins ligated dur- ing varicocelectomy. Therefore, it was demonstrated that inclusion of CDUS in the preoperative evaluation in patients with Grade 3 varicocele has no effect on surgical decision making or the number of ligated spermatic veins which determines the surgical success index. The present study has several limitations. Our study is limited by the small number of patients due to a single- center trial. In our operations, we do not use microscop- ic magnification routinely during surgery and not all the patients were operated on by a single surgeon experi- enced in the field of andrology. The last limitation of our study was its retrospective evaluation limited to findings of patients with Grade 3 varicocele. Doppler ultrasound could be useful when varicocele is not visible or palpable. For these reasons, we believe that larger case series will be more effective in the interpretation of our study findings. CONCLUSIONS The best diagnostic method for grade 3 varicocele is physical examination and there is no need for additional imaging in primary cases. It is obvious that every imaging study will have an additional cost and will cause time and labor loss. Imaging studies do not contribute to surgical decision making or the prediction of surgical success. However, it should be kept in mind that physical exami- nation is not sufficient in all cases, yet it can provide use- ful information particularly for the evaluation of second- ary/tertiary varicocele cases and for the diagnosis of addi- tional testicular pathologies. 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Urology. 2004; 64:137-139. 32. Babai M, Gharibvand MM, Momeni M, et al. Comparison of pre- operative and post-operative (varicocelectomy) sperm parameters in patients suffering varicocle with and without reflux in Doppler ultra- sonography. J Family Med Prim Care. 2019; 8:1730-1734. Correspondence Caner Ediz, Assoc. Prof. (Corresponding Author) drcanerediz@gmail.com Muhammed Temel Cihan, MD Serkan Akan, MD Serkan Yenigürbüz, MD Mehmet Pehlivanoğlu, MD Ömer Yılmaz, MD Department of Urology, Sultan Abdulhamid Han Education and Research Hospital Tibbiye Street. Selimiye neighborhood, 34668 Uskudar/Istanbul (Turkey) Suna Şahin Ediz, MD Department of Radiology, Kartal Dr. Lutfi Kirdar City Hospital, Istanbul (Turkey)