Clinical Radiology (2005) 60, 12481255

REVIEW

Testicular varicoceles
P. Beddy, T. Geoghegan, R.F. Browne, W.C. Torreggiani*
Department of Radiology, The Adelaide and Meath Hospital, Tallaght, Dublin 24, Ireland
Received 23 December 2004; received in revised form 23 May 2005; accepted 29 June 2005

KEYWORDS
Testicle; Testes; Varicocele; Doppler ultrasound; Magnetic resonance imaging; Therapeutic embolisation

A testicular varicocele represents an abnormal degree of venous dilatation of the pampiniform plexus. It is a relatively common condition and may present at scrotal pain and swelling. An association with male subfertility is an area of debate. This article describes the present day radiological criteria and imaging techniques to aid accurate diagnosis of varicoceles. In addition, the role of the interventional radiologist in treating this condition is discussed. Q 2005 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved.

Introduction
A varicocele is an abnormal degree of venous dilatation in the pampiniform plexus.1 It affects approximately 15% of men. It can present with scrotal pain and swelling, or during the investigation of male sub-fertility. Nowadays most are detected incidentally in patients undergoing scrotal ultrasound for other reasons and remain clinically silent. The aetiology of varicoceles is unclear. Idiopathic varicoceles are more common on the left side where the left spermatic vein enters perpendicular to the left renal vein. The right spermatic vein enters obliquely into the inferior vena cava and this appears to have some protective effect on the right side. Retrograde ow into the internal spermatic vein results in dilatation and tortuosity of the pampiniform plexus. Less frequent causes of varicoceles include compression of the renal vein sometimes by tumour, an aberrant renal vein or an obstructed renal vein. Because varicoceles are much less common on the right side, the nding of a right-sided varicocele necessitates evaluation of the abdomen to exclude an associated abdominal mass causing compressive symptoms
* Guarantor and correspondent: W.C. Torreggiani, Department of Radiology, Adelaide and Meath Hospital, Tallaght, Dublin 24, Ireland. Tel.: C353 141 437 00; fax: C353 141 438 05. E-mail address: william.torreggiani@amnch.ie (W.C. Torreggiani).

(Fig. 1), this is also true in older patients who present with a recent onset varicocele. The association of varicoceles with sub-fertility is controversial. In some patients sperm motility improves after varicocele ablation, but in others it remains the same. In this article we will describe the criteria for diagnosis, particularly emphasizing the present ultrasound guidelines. Methods and manoeuvres to aid visualization are discussed, as well as variations in appearance. In addition the role of the interventional radiologist in treating this disorder is described.

Diagnosis
Clinical
Varicoceles may be symptomatic with pain and swelling. The clinical suspicion of a varicocele depends on the expertise of the evaluating physician. A senior urologist, for example, is far more likely to make the correct diagnosis. A Valsalva manoeuvre (expiration against a closed glottis) is an important part of the clinical examination as this causes distension of the pampiniform plexus allowing greater visualization. Varicoceles greater than 34 mm in diameter are usually clinically apparent.1 A large varicocele is often described as a bag of worms surrounding the testis. Dubin and

0009-9260/$ - see front matter Q 2005 The Royal College of Radiologists. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.crad.2005.06.010

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positive rate for clinical examination makes it imperative that a practising radiologist be familiar with the radiological features and variations of testicular varicoceles.

Imaging
In the past, thermography was a widely used technique but has largely been superseded by ultrasound5 and will not be discussed further (Table 1). Ultrasound is now the most frequently used method and a high-frequency transducer of at least 7 MHz should be used. The features on grey scale ultrasound include a prominence of at least two to three veins of the pampiniform plexus, of which one should have a diameter greater than 23 mm in a supine position.6,7 In a study by Rifkin et al. in 21 patients with clinically palpable varicoceles, good correlation was found when 3 mm was used as the minimum size for diagnosis of a varicocele.6 Other studies have suggested 2 mm is sufcient to diagnose a varicocele. 5 However, the exact size of the vessel is variable. A Valsalva manoeuvre is an important component of the examination and should be performed routinely as it causes an increase in vessel size and conspicuousness (Fig. 2). In 1986, MacClure and Hricak assessed 50 subfertile and 25 control patients. In the subfertile group 50% had clinically detectable varicoceles while 68% had ultrasound evidence of a spermatic vein exceeding 3 mm in size. In the control group 16% had clinically detectable varicoceles while 32% had a spermatic vein exceeding 3 mm on ultrasound.8 This again suggested the additive importance of ultrasound over clinical evaluation alone. Unfortunately this study did not incorporate a group who underwent venography, which is considered to be the gold standard. Hamm et al.5 compared scrotal ultrasound with venography in 118 patients. In this study ultrasound was shown to have a sensitivity of 98% and specicity of 100% compared with venography, but 2 mm was used as the lower limit for venous dilatation.4 While the majority of varicoceles are extra-testicular in location, they may rarely traverse the testicle itself (Fig. 3). During the examination, conditions should allow for maximum visualization while maintaining patient comfort. The room should be darkened and a chaperone should be made available if possible. The procedure should be fully explained to the patient and also how to perform the Valsalva manoeuvre. In our institution, it is routine for the patient to hold the penis in the anatomical position

Figure 1 (a) Grey scale ultrasound demonstrates large varicocele surrounding the right testes. (b) Coronal gadolinium-enhanced coronal fast low angle shot (FLASH) MRI image demonstrates large right renal mass with ipsilateral varices.

Amelar2 devised a useful clinical grading system for palpable varicoceles. Grade 1 varicoceles are considered to be those palpable only during a Valsalva manoeuvre. Grade 2 varicoceles are palpable without the Valsalva manoeuvre. Grade 3 varicoceles are visible on examination before palpation. Although clinical evaluation with Valsalva manoeuvre is a simple and non-invasive test, clinical examination is not without limitation. A study by Orda et al. of 38 males suggests that clinical assessment is highly subjective.3 In a World Health Organisation multicentre study on 141 men with sub-fertility the sensitivity of clinical examination was approximately 50% for the detection of a varicocele when compared with venography and it had a false-positive rate of 23%.4 This high false-

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Table 1

Imaging techniques used in evaluating testicular varicoceles. Diagnostic criteria Tortuous anechoic tubular structures adjacent to the testis. R2 prominent veins in pampiniform plexus. Expand with Valsalva manoeuvre and upright position with at least one O 23 mm in diameter Reux in the spermatic vein, which increases with Valsalva manoeuvre, may be identied. Doppler sonography can be used to grade venous reux as static (grade I), intermittent (grade II), or continuous (grade III) Enlargement of internal spermatic vein with reux into the abdominal, inguinal, scrotal or pelvic portions of the spermatic vein. Venous collateralization present. Incompetent spermatic vein Gadolinium-enhanced imaging useful. Delayed imaging in venous phase identies mass of dilated vessels and prominence of the pampiniform plexus Static images show intra-scrotal accumulation of the labelled red cells. Supine and erect imaging is obtained. Reux may be shown on dynamic images

Imaging method Ultrasound

Colour Doppler

Venography

MRI Scintigraphy (technetium-99mlabelled red blood cells)

with one hand. This allows easier evaluation of the exposed testes, as well as allowing the second hand to be free to pinch the nostrils in order to perform the Valsalva manoeuvre. We typically perform the evaluation initially in a supine position followed by a similar examination with the patient standing. It is often useful to wait a few minutes before evaluating the patient in the standing position to allow the varicoceles to ll. Some varicoceles only become apparent in this position. We routinely use colour Doppler as part of the examination (Fig. 2). It has been shown to improve diagnostic ability by the detection of reverse ow in the incompetent vein. The reux is quantied as permanent, which is signicant for a varicocele; intermittent; or brief, which is physiological. Intermittent reux is an area of debate and is usually insignicant if there is no palpable varicocele. Petros et al.9 evaluated 17 sub-fertile men with colour Doppler ultrasound versus clinical examination. Venography was performed as the gold standard. Venography revealed 14 varicoceles, 93% of which were detected by

Figure 2 (a) There is a varicocele on the left side of the pampiniform plexus. (b) After Valsalva manoeuvre there is marked engorgement and prominence of the varicocele. Initially the patient is in the supine position and then erect. Valsalva is attempted in both.

Figure 3 Sagittal ultrasound of the left testes shows a serpentigenous hypoechoic structures transcending the testes.

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Figure 4 Spot lm demonstrating selective catheter and guide-wire in the left renal vein and testicular vein.

colour Doppler ultrasound, but only 71% by clinical examination alone.9 We do not routinely use duplex ultrasound as the technique is time-consuming and there is much confusion about its signicance. Scrotal scintigraphy was met with enthusiasm in the early 1980s, however, the sensitivity was low and the technique was time-consuming. More recent studies using dynamic varicocele scintigraphy have been more promising especially in the group with a small or subclinical varicocele.10 Although venography is still considered to be the gold standard, it is time consuming and invasive. A normal venogram is one in which is a single testicular vein is seen up to the inguinal ligament and into the spermatic cord, there may be a few divisions as part of the pampiniform plexus. If a varicocele is present, the internal spermatic vein will be enlarged and there will be reux into the abdominal, inguinal, scrotal or pelvic portions of the spermatic vein. There will also be venous collateralization and anastomotic channels. Marsmann et al.11 classied the degree of reux on

Figure 5 Selective venography of left testicular vein demonstrates dilatation of pampiniform plexus around the left testes in keeping with a varicocele.

venography from 0 to 5. Grade 0 was no reux, grade 1 to 5 represented reux into the upper lumbar, lower lumbar, upper pelvic, lower pelvic or inguinal portions of the spermatic veins, respectively.11 In our institution, venography is performed either in the assessment of difcult or uncertain cases or more commonly before denitive treatment by venous embolization. It is important to shield the gonads during venography and treatment procedures. Pulsed uoroscopy and image

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Figure 6 Coronal T1-weighted MRI image post-gadolinium shows left-sided varicocele.

capturing should be used during all venographic and therapeutic procedures. We typically perform the procedure under local anaesthetic. Conscious sedation is sometimes used in very anxious patients but is not essential. We typically puncture the right common femoral vein under ultrasound guidance, the jugular vein offers an alternative approach site. Using a co-axial system, a 5 F sheath is placed into the common femoral vein. We use a 5 F standard Cobra catheter and a hydrophilic guide-wire. The catheter and guide-wire are then advanced into the inferior vena cava (IVC) and the renal vein on the left or occasionally directly into the testicular vein on the right as it enters the IVC. Access to the right renal vein may be difcult in some cases. The use of a guide catheter helps cannulation of this vessel by stabilizing the catheter and guide-wire. After a failed trial with a Cobra catheter we try a more angled catheter such as a 5 F Omni Selective catheter. If we still fail then we directly proceed to attempt access via the internal jugular vein. Occasionally we use the basilic vein as an access point. The catheter is advanced into the testicular vein over the guide-wire (Fig. 4). Contrast medium is then injected by hand and images obtained (Fig. 5). Limited images should be obtained over the testes due to their sensitivity to ionizing radiation. Imaging with other techniques, such as magnetic

Figure 7 Spot view of the testicular vein showing coil embolization extending through the length of the testicular vein.

resonance imaging (MRI) or computed tomography (CT), is only occasionally required, for example, to evaluate the presence of obstructing masses particularly on the right side. When conventional venography is contraindicated (history of anaphylaxis, etc), magnetic resonance venography (MRV) is a suitable alternative (Fig. 6). Magnetic resonance angiography has been used for the assessment of recurrent varicoceles.12,13

Treatment
The decision to treat should be based primarily on whether it is symptomatic or associated with

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subfertility, and the choice is between surgical treatment and radiological treatment. Where there is a trained radiologist, percutaneous embolization should be the rst-line therapy,14 with surgery reserved for the small proportion of patients who have failed catheterization. However, the decision is often based on local bias and availability of local expertise. With surgery, three common techniques are employed. These are sub-inguinal ligation, inguinal ligation and retroperitoneal ligation, with the latter being the most frequently practiced. Laparoscopic varicocele ligation has not been shown to be superior to open surgery and may be associated with serious complications.15 Barbalias et al.16 compared the three surgical approaches with percutaneous embolization in a randomised, prospective study. There were similar recurrence rates with all four techniques. In addition, there was signicant improvement in sperm motility in all groups, with open inguinal ligation having marginally the best results.16 Post-procedure the return to normal activities is, however, signicantly faster after embolization compared with surgery. These results have been seen in other studies.17,18 Percutaneous embolization involves selective catheterization of the spermatic vein and subsequent occlusion with a sclerosing agent or a solid embolization coil.19 The procedure is usually carried out on a day-case basis. Embolization or sclerotherapy is preceded in all cases by venography to both access the size and distribution of the varicocele, as well as to conrm correct position of the catheter before embolization. We use coils,
Table 2 Difculties Difculty puncturing femoral vein Procedural difculties and their management.

starting distally at the level of the inguinal ligament and progressing proximally to within 23 mm of renal vein (Fig. 7). Care is taken when placing coils proximally to ensure that they do not dislodge into the renal vein. We use 8 mm coils for a standard varicocele and 10 mm coils for a larger varicocele. It is important that all collateral and parallel veins that are visualized are individually cannulated and occluded. Sclerosing agents such as sodium tetradecyl sulphate may also be used. It is imperative that reux into the pampiniform plexus is prevented by external pressure at the inguinal crease before injecting the sclerosant. The immediate technical success rate is upwards of 90%.20 Failure of the procedure is usually due to unsuccessful catheterization or anatomical variants.21 We have summarized common difculties and suggested solutions in Table 2. Patients are discharged within 2 h of the procedure, most require simple analgesia post-procedure. Antibiotics are not given as standard. We advise patients to avoid sexual activity until they have resumed their usual functional levels. Long-term follow-up data have principally been accrued in studies carried out in sub-fertile men. The marker of successful therapy in this group is the improvement in semen quality and pregnancy rates postvaricocele ablation. Kuroiwa et al.22 treated 28 subfertile men with clinically detected varicoceles with percutaneous embolization, 82% had an improvement in the grade of varicocele and a signicant improvement in sperm count.22 A recent large series by Trombetta et al.23 in 560 sub-fertile men showed improvement in sperm count in 87% at

Management options (a) Use of micro puncture set for initial femoral puncture (b) Direct ultrasound guidance puncture of vein (recommended) (c) Get patient to perform Valsalva manoeuvre to enlarge size of femoral vein (a) A guide catheter or long sheath may aid in stabilising Cobra catheter (b) Use of a tracker (micro) catheter to enter testicular vein (c) Repeat procedure through alternative route such as jugular vein or basilic approach (a) Use of hydrophilic catheter and guide wire (b) Use of micro coils through a tracker catheter (c) Use of 4 French Cobra catheter instead of 5 French catheter (a) Treatment of vasospasm with vasodilators rarely helpful in venous system (b) Reattempt after interval (15 minutes) may allow spasm to abate (c) Spasm often induced by excessive manipulation. Smooth technique and experience may reduce frequency

Difculty accessing proximal testicular vein

Difculty accessing distal testicular vein for distal embolisation

Vessel spasm

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3 months post-procedure. Improved pregnancy rates are seen in a number of studies, however, a Cochrane review of ve randomized studies of varicocele repair revealed no overall improvement in pregnancy rates.2327 Whether improvements in sperm quality directly result in increased pregnancy rates is unclear but many clinicians favour repair of varicoceles in infertile couples.28 In terms of symptomatic varicoceles, Alqahtani et al.29 reported 41 patients who underwent percutaneous embolization for symptomatic disease. They found that 89.1% of patients reported a signicant improvement at mean follow-up of 22 months.29 Complications are uncommon. Coil migration is rare and is usually related to release too near to the renal vein.30 Tungsten coils should be avoided as there is some resorption of the coil and the longterm side effects of raised serum tungsten levels are unknown.31 If a sclerosing agent is used, thrombosis of the pampiniform plexus is possible, it occurs in less than 5% of patients, but is troublesome and requires treatment with antiinammatory agents and antibiotics.32 The indications for varicocele treatment differ in children as it may prevent future testicular atrophy and subfertility.33

Conclusion
Testicular varicoceles are an important disorder leading to signicant symptoms in some patients and associated with sub-fertility in others. Accurate diagnosis is important as correct treatment may lead to resolution of symptoms and improvement in sperm count in sub-fertile patients. As clinical diagnosis is inaccurate, imaging is usually required to conrm the diagnosis. Although ultrasound, including colour Doppler techniques, is the commonest method used in diagnosing varicoceles, venography remains the gold standard. Treatment may be surgical or radiological, with radiological treatment resulting in a quicker recovery.

References
1. Demas BE, Hricak H, McClure RD. Varicoceles. Radiologic diagnosis and treatment. Radiol Clin North Am 1991;29: 61927. 2. Dubin L, Amelar RD. Varicocele size and results of varicocelectomy in selected subfertile men with varicocele. Fertil Steril 1970;21:6069. 3. Orda R, Sayfan J, Manor H, Witz E, Sofer Y. Diagnosis of varicocele and postoperative evaluation using inguinal ultrasonography. Ann Surg 1987;206:99101.

4. Comparison among different methods for the diagnosis of varicocele. World Health Organization. Fertil Steril 1985; 43:57582. 5. Hamm B, Fobbe F, Sorensen R, Felsenberg D. Varicoceles: Combined sonography and thermography in diagnosis and post therapeutic evaluation. Radiology 1986;160:41924. 6. Rifkin MD, Foy PM, Kurtz AB, Pasto ME, Goldberg BB. The role of diagnostic ultrasonography in varicocele evaluation. J Ultrasound Med 1983;2:2715. 7. Wolverson M, Houttuin E, Heiberg E, Sundaram M, Gregory J. High-resolution real-time sonography of scrotal varicocele. AJR Am J Roentgenol 1983;141:7759. 8. MacClure RD, Hricak H. Scrotal ultrasound in the infertile man: Detection of subclinical unilateral and bilateral varicoceles. J Urol 1986;135:7115. 9. Petros JA, Andriole GL, Middleton WD, Picus DA. Correlation of testicular color Doppler ultrasonography, physical examination and venography in the detection of left varicoceles in men with infertility. J Urol 1991;145:7858. 10. Prenen J, Van Dis P, Feijen H. Varicocele scintigraphy: A simplied method for the detection of spermatic vein reux. Clin Nucl Med 1996;21:9217. 11. Marsmann JWP. Clinical versus subclinical varicoceles: Venographic ndings and improvement of fertility after embolisation. Radiology 1985;155:63542. 12. Von Heijne A. Recurrent varicocele. Demonstration by 3D phase-contrast MR angiography. Acta Radiol 1997;38: 10202. 13. Varma MK, Ho VB, Haggerty M, Bates DG, Moore DC. MR venography as a diagnostic tool in the assessment of recurrent varicocele in an adolescent. Pediatr Radiol 1998; 28:6367. 14. Hargreave TB. Varicocelea clinical enigma. Br J Urol 1993; 72:4018. 15. Soulie M, Seguin P, Richeux L, et al. Urological complications of laparoscopic surgery: Experience with 350 procedures at a single center. J Urol 2001;165:19603. 16. Barbalias GA, Liatsikos EN, Nikiforidis G, Siablis D. Treatment of varicocele for male infertility: A comparative study evaluating currently used approaches. Eur Urol 1998;34: 3938. 17. Sautter T, Sulser T, Suter S, Gretener H, Hauri D. Treatment of varicocele: A prospective randomized comparison of laparoscopy versus antegrade sclerotherapy. Eur Urol 2002; 41:398400. 18. Fretz PC, Sandlow JI. Varicocele: Current concepts in pathophysiology, diagnosis and treatment. Urol Clin North Am 2002;29:92137. 19. Iaccarino V. A nonsurgical treatment of varicocele: Transcatheter sclerotherapy of gonadal veins. Ann Radiol (Paris) 1980;23:36970. 20. Nabi G, Asterlings S, Greene DR, Marsh RL. Percutaneous embolization of varicoceles: Outcomes and correlation of semen improvement with pregnancy. Urology 2004;63: 35963. 21. Keoghane SR, Jones L, Wright MP, Kabala J. Percutaneous retrograde varicocele embolisation using tungsten embolisation coils: A ve year audit. Int Urol Nephrol 2001;33: 51720. 22. Kuroiwa T, Hasuo K, Yasumori K, et al. Trans-catheter embolization of testicular vein for varicocele testis. Acta Radiol 1991;32:3114. 23. Schlesinger MH, Wilets IF, Nagler HM. Treatment outcome after varicocelectomy. A critical analysis. Urol Clin North Am 1994;21:51729.

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24. Trombetta C, Liguori G, Bucci S, Ciciliato S, Belgrano E. Percutaneous treatment of varicocele. Urol Int 2003;70: 1138. 25. Zuckerman AM, Mitchell SE, Venbrux AC, et al. Percutaneous varicocele occlusion: Long-term follow-up. J Vasc Interv Radiol 1994;5:3159. 26. Evers JL, Collins JA, Vandekerckhove P. Surgery or embolization for varicocele in subfertile men. Cochrane Database Syst Rev 2001;1:CD000479. 27. Evers JL, Collins JA. Assessment of efcacy of varicocele repair for male subfertility: A systematic review. Lancet 2003;361:184952. 28. Sandlow J. Pathogenesis and treatment of varicoceles. BMJ 2004;328:9678.

29. Alqahtani A, Yazbeck S, Dubois J, Garel L. Percutaneous embolization of varicocele in children: A Canadian experience. J Pediatr Surg 2002;37:7835. 30. Cornud F, Belin X, Amar E, Delafontaine D, Helenon O, Moreau JF. Varicocele: Strategies in diagnosis and treatment. Eur Radiol 1999;9:53645. 31. Barrett J, Wells I, Riordan R, Roobottom C. Endovascular embolization of varicoceles: Resorption of tungsten coils in the spermatic vein. Cardiovasc Intervent Radiol 2000;23: 4579. 32. Thomas Jr AJ, Geisinger MA. Current management of varicoceles. Urol Clin North Am 1990;17:893907. 33. Kass EJ, Belman AB. Reversal of testicular growth failure by varicocele ligation. J Urol 1987;137:4756.