Intratesticular Arterial Pulsatility and Resistance Index in Males with Scrotal Varicocele

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1 DOI / Original Research Article Intratesticular Arterial Pulsatility and Resistance Index in Males with Scrotal Varicocele Shih-Feng Wang 1,2,4 I-Jen Chiang 1,* Wah-On Lo 2 Kuo-Chiang Chen 2,3,4 Teh-Sheng Hsieh 2,4 Chih-Ming Lin 2 Background: To investigate difference in intratesticular arterial pulsatility index (PI) and resistance index (RI) between varicocele and healthy testes using power Doppler ultrasonography. Materials and Methods: Patients undergoing scrotal ultrasonography were recruited. PI and RI of the intratesticular artery were measured using a 12-MHz power Doppler ultrasound, and varicocele grades were obtained by physical examination. Results: Forty-four males with left scrotal varicocele and 12 healthy males were included. PI and RI were similar in the right testis between groups (p = 0.31 and 0.404, respectively), but significantly higher RI in the left varicocele testis (p = 0.013). The left testes of varicocele patients had a higher RI and smaller size than their right testes (p= and 0.001, respectively). No significant differences in PI, RI, and testicular size between different varicocele grades were observed. Conclusions: The study findings reveal that RI was higher in the varicocele testis. Thus, varicocele may have influence in the vascularity and circulation within the testis. Key words: Doppler ultrasonography, Pulsatility index, Resistance index, Varicocele Introduction Scrotal varicocele is an abnormal dilation and tortuosity of the internal spermatic veins within the pampiniform plexus of the spermatic cord. Idiopathic varicoceles are more common on the left side, where the left spermatic vein enters perpendicular to the left renal vein. The underlying pathological process is unknown, but is considered related to increased hydrostatic pressure and valvular incompetence. Retrograde flow into the internal spermatic vein results in dilatation and tortuosity of the pampiniform plexus. Doppler ultrasonography has been used for assessing diseases of testis and scrotum [1]. Additionally, some studies reported different results of potential alterations in the microcirculation of capsular branch of testicular artery in the presence of varicocele [2, 3]. Clinical varicocele can lead to Impaired testicular circulation This clinical study aimed to compare intratesticular arterial blood flow using power Doppler ultrasonography (PDUS) in scrotal varicocele patients and healthy males. Graduate Institute of Biomedical Informatics, Taipei Medical University, Taipei, Taiwan 1 Department of Urology, Cathay General Hospital, Taipei, Taiwan 2 Graduate Institute of Basic Medicine, Fu Jen Catholic University, New Taipei, Taiwan 3 School of Medicine, Fu-Jen Catholic University, New Taipei, Taiwan 4 Submitted September, 22, 2014; final version accepted February, 02, *Correspondence author: I-Jen Chiang ( @gmail.com) 輔仁醫學期刊第 14 卷第 1 期

2 Shih-Feng Wang I-Jen Chiang Wah-On Lo Kuo-Chiang Chen Teh-Sheng Hsieh Chih-Ming Lin Methods This was an observational clinical study of patients from our outpatient clinic with a request of scrotal ultrasonography. Exclusion criteria included a history of inguinal or scrotal surgery, testicular trauma, genital infectious diseases, congenital scrotal anomalies such as undescending testis, hydrocele, and inguinal hernia, or other clinically detectable diseases. The varicocele grades were determined during physical examination (Table 1) [4]. All patients were assessed using scrotal gray-scale ultrasonography and PDUS with a 12-MHz lineararray transducer of a BK medical ultrasound scanner. Ultrasonography was performed in a warm room with the patients in the supine position, and their penis resting on the lower abdomen. Table 1. Varicocele grading Grade 1 Grade 2 Grade 3 Varicocele only palpable during or after Valsalva maneuver on physical exam Varicocele palpable on routine physical exam without the need for Valsalva maneuver Varicocele visible to the eye and palpable on physical exam The pulsatility index (PI) and resistance index (RI) were assessed from the intratesticular branch of the testicular arteries from both the left and right testes in the patient and control groups using PDUS. PI and RI were calculated automatically using the scans from at least five continuous identical waveforms (Fig. 1). The same operator made all measurements. A p-value of 0.05 was considered statistically significant. Fig. 1. Power Doppler ultrasonography of the left intratesticular arterial branch. The machine calculates PI and RI automatically. At least five continuous identical Doppler waveforms were obtained. Results From October 2010 to January 2013, 46 males with scrotal varicocele were enrolled in the study, and 12 healthy males were recruited to the control group. Two patients with clinical right scrotal varicocele were excluded; the remaining 44 patients had left-sided clinical varicocele. The mean age of the two groups was similar (30.02 ± and ± 10.82, respectively, p = 0.106). A comparison of the testicular length, PI, and RI values between the two groups are shown in Table 2. There was no statistically significant difference between the size of the left and right testis in each group. PI and RI of the intratesticular arterial branch were similar in the right testis between groups, but were significantly higher in left varicocele testis (p = 0.05 and 0.013, respectively). We also compared these parameters between the left and right testis within each group, and the data are shown in Table 3. In the patient group, the testis was smaller and RI was higher on the left side. There was a similar trend in PI, but the 2 Fu-Jen Journal of Medicine Vol.14 No

3 Intratesticular PI and RI in scrotal varicocele data were not statistically significant (p = 0.06). In contrast, there were no differences in the testicular size, PI, and RI in the control group. The mean peak systolic velocity was / centimeter per second (cm/s). Patients were then divided into three subgroups according to varicocele grade and the results are shown in Table 4. We analyzed the ultrasonographic data of the varicocele testes using the Kruskal Wallis test. There was no significant difference in testis size, PI, and RI among subgroups. Table 2. Testicular length, pulsatility index (PI), and resistance index (RI) in the control and patient groups Patient Control p-value length of left testis (cm) 3.59 ± ± length of right testis (cm) 3.72 ± ± Left PI 1.19 ± ± Left RI 0.63 ± ± 0.11 *0.01 Right PI 1.05 ± ± Right RI 0.54 ± ± Independent t-test *statistically significant Table 3. Testicular length, pulsatility index (PI), and resistance index (RI) between the left and right testis of each group Patient group Left Right p-value Length of testis (cm) 3.59 ± ± 0.31 *0.04 PI 1.19 ± ± RI 0.63 ± ± 0.13 *0.001 Control group Length of testis (cm) 3.78 ± ± PI 0.93 ± ± RI 0.53 ± ± Paired t-test *statistically significant Table 4. Subgroups according to varicocele grade Grade 1 Grade 2 Grade 3 p-value Number Age (years) ± ± ± length of 3.66 ± ± ± testis (cm) PI 1.09 ± ± ± RI 0.62 ± ± ± Discussion Kruskal-Wallis Test Scrotal varicocele is common in healthy males, and contributes to the risk of infertility [4]. Although it is considered to be a congenital lesion, varicocele is rarely diagnosed before school age, and the frequency and severity vary with age and method of diagnosis. The prevalence of clinically diagnosed varicocele is approximately 8% 16% [5], and some studies have shown that infertile males have a much higher incidence of bilateral varicoceles [6]. Ultrasonography is the primary imaging modality to evaluate scrotal diseases. We can obtain valuable information by assessing the acute scrotum, scrotal mass, and male infertility using B-mode and Doppler ultrasonography. Ultrasonography is used to evaluate testicular size and location as well as detect varicoceles [7]. Color Doppler ultrasonography (CDUS) has a sensitivity of 83% 95% for assessing subclinical varicocele [8, 9]. Several studies have proposed a venous diameter ranging from 2 to 3 mm as the diagnostic criteria for varicocele [10, 11]. Changed diameter during Valsalva maneuver [12, 13], the sum of venous diameter [14], and flow volume [15] are also used for ultrasonographic diagnosis. 輔仁醫學期刊第 14 卷第 1 期

4 Shih-Feng Wang I-Jen Chiang Wah-On Lo Kuo-Chiang Chen Teh-Sheng Hsieh Chih-Ming Lin Varicoceles might contribute to testicular atrophy, which has been suggested as an indication for prophylactic varicocelectomy [16]. In males with varicocele, the decreased testicular volume is related to the loss of seminiferous tubule elements and decreased tubular diameter [17]. However, subclinical varicocele is not associated with ipsilateral testicular atrophy and does not affect the intratesticular circulation [18]. In our patient group, the diameter of the varicocele testis was less than that of the contralateral site. In contrast, there was no significant difference in testicular size in the healthy control group. Doppler ultrasonography has been used to assess organ perfusion and the microcirculation in many organs, and it can help with the evaluation of scrotal diseases [19, 20]. The testicular microcirculation has been evaluated using CDUS, but its relationship with scrotal varicocele is controversial. In early studies, there was no effect of the testicular microcirculation on testicular RI or volume changes in patients with subclinical varicocele [2, 18]. Testicular arterial blood flow was significantly decreased in males with varicocele [21]. A study evaluated the testicular arteries of azoospermic patients with CDUS [22]. The authors concluded that RI and peak systolic velocity were reliable indicators for routine clinical use to identify infertile or dyspermic men. More recently, varicocele was reported to affect testicular arterial blood flow. For example, increased capsular branches of the testicular arterial PI and RI were reported by Ünsal et al. [3], which might be an indicator of impaired testicular microcirculation. Another study investigated RI of intratesticular arteries and assessed its relationship with spermatogenesis [23]. The authors suggested that RI of >0.6 might be suggestive of a pathological sperm count in andrological patients, and is likely to be a reliable indicator for routine clinical use to identify subfertile males. Some studies have discussed the relationship between varicocele grade and CDUS findings. PI and RI were similar among the three subgroups. Although the data were not statistically significant, there seemed to be a trend that higher grade varicocele led to smaller testis. However, a larger-scale clinical study is necessary to confirm any potential relationship. The limitations of this study are the small number of patients and the absence of semen analysis. In addition, the cut-off values for PI and RI in varicocele are not well-established. A future study should be performed with more patients and younger healthy males as the control group. In conclusion, our preliminary data show that clinical varicocele results in ipsilateral testicular atrophy and impaired microcirculation. Intratesticular PI and RI measured using PDUS seem to be valuable for urologists during the analysis of patients with scrotal varicocele. Acknowledgements We thank Professor Jian-An Sun from Department of Public Health Fu-Jen Catholic University for statistics instruction. Conflicts of interest The authors declare no financial or nonfinancial conflicts of interest related to the subject matter or materials discussed in this manuscript. 4 Fu-Jen Journal of Medicine Vol.14 No

5 Intratesticular PI and RI in scrotal varicocele References 1. Dudea SM, Ciurea A, Chiorean A, et al. Doppler applications in testicular and scrotal disease. Med Ultrason 2010; 12: Ross JA, Watson NE, Jr., Jarow JP. The effect of varicoceles on testicular blood flow in man. Urology 1994; 44: Ünsal A, Turgut AT, Taşkin F, et al. Resistance and pulsatility index increase in capsular branches of testicular artery: Indicator of impaired testicular microcirculation in varicocele? J Clin Ultrasound 2007; 35: Wein AJ, Kavoussi LR, Novick AC, et al. Abnormalities of the testis and scrotum and their surgical management; in: Wein AJ (ed): Campbell-Walsh Urology: Elsevier Health Sciences. 2011, pp Barthold Spencer J. Abnormalities of the Testis and Scrotum and Their Surgical Management; in: Wein AJ (ed): Campbell-Walsh Urology. Elsevier Health Sciences. 10 ed., 2012, pp Trussell JC, Haas GP, Wojtowycz A, et al. High prevalence of bilateral varicoceles confirmed with ultrasonography. Int Urol Nephrol 2003; 35: Kim ED, Lipshultz LI. Role of ultrasound in the assessment of male infertility. J Clin Ultrasound 1996; 24: Hoekstra T, Witt MA. The correlation of internal spermatic vein palpability with ultrasonographic diameter and reversal of venous flow. J Urol 1995; 153: Petros JA, Andriole GL, Middleton WD, et al. Correlation of testicular color Doppler ultrasonography, physical examination and venography in the detection of left varicoceles in men with infertility. J Urol 1991; 145: Atasoy C, Fitoz S. Gray-scale and color Doppler sonographic findings in intratesticular varicocele. J Clin Ultrasound 2001; 29: Jarow JP, Ogle SR, Eskew LA. Seminal improvement following repair of ultrasound detected subclinical varicoceles. J Urol 1996; 155: Tasci AI, Resim S, Caskurlu T, et al. Color doppler ultrasonography and spectral analysis of venous flow in diagnosis of varicocele. Eur Urol 2001; 39: Pierik FH, Dohle GR, van Muiswinkel JM, et al. Is routine scrotal ultrasound advantageous in infertile men? J Urol 1999; 162: Chiou RK, Anderson JC, Wobig RK, et al. Color Doppler ultrasound criteria to diagnose varicoceles: correlation of a new scoring system with physical examination. Urology 1997; 50: Kocakoc E, Serhatlioglu S, Kiris A, et al. Color Doppler sonographic evaluation of interrelations between diameter, reflux and flow volume of testicular veins in varicocele. Eur J Radiol 2003; 47: Pinto KJ, Kroovand RL, Jarow JP. Varicocele related testicular atrophy and its predictive effect upon fertility. J Urol 1994; 152: Yamamoto M, Katsuno S, Yokoi K, et al. The effect of varicocelectomy on testicular volume in infertile patients with varicoceles. Nagoya J Med Sci 1995; 58: Akcar N, Turgut M, Adapinar B, et al. Intratesticular arterial resistance and testicular volume 輔仁醫學期刊第 14 卷第 1 期

6 Shih-Feng Wang I-Jen Chiang Wah-On Lo Kuo-Chiang Chen Teh-Sheng Hsieh Chih-Ming Lin in infertile men with subclinical varicocele. J Clin Ultrasound 2004; 32: Jee WH, Choe BY, Byun JY, et al. Resistive index of the intrascrotal artery in scrotal inflammatory disease. Acta Radiol 1997; 38: Lefort C, Thoumas D, Badachi Y, et al. Ischemic orchiditis: review of 5 cases diagnosed by color Doppler ultrasonography. J Radiol 2001; 82: Tarhan S, Gumus B, Gunduz I, et al. Effect of varicocele on testicular artery blood flow in men--color Doppler investigation. Scand J Urol Nephrol 2003; 37: Biagiotti G, Cavallini G, Modenini F, et al. Spermatogenesis and spectral echo-colour Doppler traces from the main testicular artery. BJU Int 2002; 90: Pinggera GM, Mitterberger M, Bartsch G, et al. Assessment of the intratesticular resistive index by colour Doppler ultrasonography measurements as a predictor of spermatogenesis. BJU Int 2008; 101: Fu-Jen Journal of Medicine Vol.14 No

7 Intratesticular PI and RI in scrotal varicocele 精索靜脈曲張男性睪丸內部脈動與阻力指數分析 王世鋒 1,2,4 蔣以仁謝德生 1,* 2,4 羅華安林志明 2 2 陳國強 2,3,4 背景 : 以杜卜勒超音波, 分析精索靜脈曲張患者與健康人睪丸內部脈動指數與阻力指數之間的差異 材料及方法 : 我們將那些接受過睪丸超音波的患者納入研究分析, 利用 12-MHz 的強力杜卜勒超音波來測量睪丸內部動脈的脈動指數與阻力指數, 此外靜脈曲張的程度是依照身體檢查來判斷 結果 : 共有 44 名左側精索靜脈曲張患者以及 12 名健康男性納入本研究, 這兩組的右側睪丸的脈動指數及阻力指數是差不多的 (p=0.31 及 0.404), 然而病患的左側睪丸比健康者有較高的阻力指數 (p=0.013) 病患的左側睪丸比右側有較高的阻力指數, 也比較小 (p=0.036 及 0.001), 此外在於不同程度的靜脈曲張中尚未發現在脈動指數 阻力指數及睪丸大小上有顯著差異 結論 : 研究結果發現阻力指數在精索靜脈曲張患者較高, 因此我們認為精索靜脈曲張對於睪丸內部的血流狀況有顯著影響 關鍵字 : 杜卜勒超音波, 脈動指數, 阻力指數, 精索靜脈曲張 1 臺北市臺北醫學大學醫學資訊研究所 新北市輔仁大學醫學系 4 投稿日期 :2014 年 09 月 22 日接受日期 :2015 年 02 月 02 日 * 通訊作者 : 蔣以仁電子信箱 : @gmail.com 2 臺北市國泰綜合醫院泌尿科 3 新北市輔仁大學基礎醫學研究所 輔仁醫學期刊第 14 卷第 1 期

8 Shih-Feng Wang I-Jen Chiang Wah-On Lo Kuo-Chiang Chen Teh-Sheng Hsieh Chih-Ming Lin 8 Fu-Jen Journal of Medicine Vol.14 No