Ultrasound evaluation of varicoceles: guidelines and recommendations of the European Society of Urogenital Radiology Scrotal and Penile Imaging Working Group (ESUR-SPIWG) for detection, classification, and grading

Abstract

Varicoceles are relatively common particularly in asymptomatic men and are even more prevalent in subfertile men, representing the most common potentially correctable cause of male infertility. Ultrasound (US) is the imaging modality of choice for varicocele evaluation, but there is no widely accepted consensus on examination technique, diagnostic criteria, or classification. In view of this uncertainty, the guideline writing group (WG) of the European Society of Urogenital Radiology (ESUR) Scrotal and Penile Imaging Working Group (ESUR-SPIWG) undertook a literature review and assessment of the quality of relevant evidence. The group then produced evidence-based recommendations for varicocele US examination, interpretation, and classification by consensus agreement. The results are presented in the form of 15 clinical questions with a brief summary of the relevant evidence and the authorised recommendations from the SPIWG. This paper provides a short summary of the evidence evaluation and the complete recommendations.

Key Points

• Varicocele is a common clinical problem; it is highly prevalent amongst subfertile men and the most common potentially correctable cause of male infertility.

• Ultrasound is the imaging modality of choice for varicocele assessment, but there is no generally agreed consensus on the US examination technique or the criteria that should be used for diagnosis, grading, and classification.

• This paper summarises the recommendations of the ESUR-SPIWG for standardising the US assessment of varicoceles. This includes examination technique, image interpretation, classification, and reporting.

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Abbreviations

AGREE:

Appraisal of Guidelines for Research and Evaluation

AVMs:

Arteriovenous malformations

ESUR:

European Society of Urogenital Radiology

GRADE:

Grading of Recommendations Assessment, Development and Evaluation

H:

Height

L:

Length

OCEBM:

Oxford Centre for Evidence Based Medicine

PICO:

Patient Problem (or Population), Intervention, Comparison or Control, Outcome

Sec:

Seconds

SPIWG:

Scrotal and Penile Imaging Working Group

V:

Volume

W:

Width

WG:

Guideline writing group

References

  1. 1.

    Paick S, Choi WS (2019) Varicocele and testicular pain: a review. World J Mens Health 37(1):4–11

    Article  PubMed  PubMed Central  Google Scholar 

  2. 2.

    Dubin L, Amelar RD (1970) Varicocele size and results of varicocelectomy in selected subfertile men with varicocele. Fertil Steril 21(8):606–609

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. 3.

    Practice Committee of the American Society for Reproductive Medicine; Society for Male Reproduction and Urology (2014) Report on varicocele and infertility: a committee opinion. Fertil Steril 102(6):1556–1560

    Article  Google Scholar 

  4. 4.

    Khera M, Lipshultz LI (2008) Evolving approach to the varicocele. Urol Clin North Am 35(2):183–189

    Article  PubMed  PubMed Central  Google Scholar 

  5. 5.

    Zini A, Dohle G (2011) Are varicoceles associated with increased deoxyribonucleic acid fragmentation? Fertil Steril 96(6):1283–1287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. 6.

    Jungwirth A, Giwercman A, Tournaye H et al (2012) European Association of Urology guidelines on male infertility: the 2012 update. Eur Urol 62(2):324–332

    Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Agarwal A, Deepinder F, Cocuzza M et al (2007) Efficacy of varicocelectomy in improving semen parameters: new meta-analytical approach. Urology. 70(3):532–538

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Brouwers MC, Kho ME, Browman GP et al (2010) AGREE II: advancing guideline development, reporting and evaluation in health care. CMAJ. 182(18):E839–E842

    Article  PubMed  PubMed Central  Google Scholar 

  9. 9.

    van der Molen AJ, Reimer P, Dekkers IA et al (2018) Post-contrast acute kidney injury - Part 1: definition, clinical features, incidence, role of contrast medium and risk factors : recommendations for updated ESUR Contrast Medium Safety Committee guidelines. Eur Radiol 28(7):2845–2855

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Guyatt GH, Oxman AD, Kunz R et al (2011) GRADE guidelines: 2. Framing the question and deciding on important outcomes. J Clin Epidemiol 64(4):395–400

    Article  PubMed  PubMed Central  Google Scholar 

  11. 11.

    Medicine OCfE-B. The Oxford 2011 Levels of Evidence 2011 Available from: https://www.cebm.net/2016/05/ocebm-levels-of-evidence/. Accessed April 2019

  12. 12.

    Plus EE. GRADE: Grading of Recommendations Assessment, Development and Evaluation (A, B, C, D): John Wiley & Sons, Inc; 2018. Available from: http://www.essentialevidenceplus.com/product/concept_infomastery.cfm. Accessed April 2019

  13. 13.

    Dalkey N, Helmer O (1963) An experimental application of the DELPHI method to the use of experts. Manag Sci 9(3):458–467

    Article  Google Scholar 

  14. 14.

    Jungwirth A, Diemer T, Kopa Z, Krausz C, Minhas S, Tournaye H (2018) Guidelines on male infertility, European Association of Urology. EAU Guidelines Office, Arnhem. Available from: https://uroweb.org/wp-content/uploads/EAU-Guidelines-on-Male-Infertility-2018-large-text.pdf. Accessed April 2019

  15. 15.

    Saypol DC (1981) Varicocele. J Androl 2(2):61–71

    Article  Google Scholar 

  16. 16.

    Alsaikhan B, Alrabeeah K, Delouya G, Zini A (2016) Epidemiology of varicocele. Asian J Androl 18(2):179–181

    Article  PubMed  PubMed Central  Google Scholar 

  17. 17.

    Dubin L, Amelar RD (1971) Etiologic factors in 1294 consecutive cases of male infertility. Fertil Steril 22(8):469–474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. 18.

    Kibar Y, Seckin B, Erduran D (2002) The effects of subinguinal varicocelectomy on Kruger morphology and semen parameters. J Urol 168(3):1071–1074

    Article  PubMed  PubMed Central  Google Scholar 

  19. 19.

    Zini A, Boman JM (2009) Varicocele: red flag or red herring? Semin Reprod Med 27(2):171–178

    Article  PubMed  PubMed Central  Google Scholar 

  20. 20.

    Liguori G, Trombetta C, Garaffa G et al (2004) Color Doppler ultrasound investigation of varicocele. World J Urol 22(5):378–381

    Article  PubMed  PubMed Central  Google Scholar 

  21. 21.

    Marmar JL (2001) Varicocele and male infertility: Part II: the pathophysiology of varicoceles in the light of current molecular and genetic information. Hum Reprod Update 7(5):461–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. 22.

    Will MA, Swain J, Fode M, Sonksen J, Christman GM, Ohl D (2011) The great debate: varicocele treatment and impact on fertility. Fertil Steril 95(3):841–852

    Article  PubMed  PubMed Central  Google Scholar 

  23. 23.

    Naughton CK, Nangia AK, Agarwal A (2001) Varicocele and male infertility: Part II: pathophysiology of varicoceles in male infertility. Hum Reprod Update 7(5):473–481

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. 24.

    Papanikolaou F, Chow V, Jarvi K, Fong B, Ho M, Zini A (2000) Effect of adult microsurgical varicocelectomy on testicular volume. Urology. 56(1):136–139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Jung A, Schuppe HC (2007) Influence of genital heat stress on semen quality in humans. Andrologia. 39(6):203–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. 26.

    Evers JH, Collins J, Clarke J (2008) Surgery or embolisation for varicoceles in subfertile men. Cochrane Database Syst Rev 2008(3):CD000479. https://doi.org/10.1002/14651858.CD000479.pub3

    Article  Google Scholar 

  27. 27.

    Kroese AC, De Lange NM, Collins JA, Evers JL (2013) Varicocele surgery, new evidence. Hum Reprod Update 19(4):317

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. 28.

    Kroese ACJ, de Lange NM, Collins J, Evers JL (2012) Surgery or embolization for varicoceles in subfertile men. Cochrane Database Syst Rev (10):CD000479. https://doi.org/10.1002/14651858.CD000479.pub5

  29. 29.

    Smit M, Romijn JC, Wildhagen MF, Veldhoven JL, Weber RF, Dohle GR (2010) Decreased sperm DNA fragmentation after surgical varicocelectomy is associated with increased pregnancy rate. J Urol 183(1):270–274

    Article  PubMed  PubMed Central  Google Scholar 

  30. 30.

    Baazeem A, Belzile E, Ciampi A et al (2011) Varicocele and male factor infertility treatment: a new meta-analysis and review of the role of varicocele repair. Eur Urol 60(4):796–808

    Article  PubMed  PubMed Central  Google Scholar 

  31. 31.

    Macleod R, Biyani CS, Cartledge J, Eardley I (2015) Varicocele. BMJ Clin Evid 2015

  32. 32.

    Kim KH, Lee JY, Kang DH, Lee H, Seo JT, Cho KS (2013) Impact of surgical varicocele repair on pregnancy rate in subfertile men with clinical varicocele and impaired semen quality: a meta-analysis of randomized clinical trials. Korean J Urol 54(10):703–709

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Fertility: assessment and treatment for people with fertility problems. National Institute for Health and Clinical Excellence: Guidance [CG11]. London (UK) 2004. www.nice.org.uk/guidance/cg11. Accessed April 2019

  34. 34.

    Lotti F, Maggi M (2014) Ultrasound of the male genital tract in relation to male reproductive health. Hum Reprod Update 21(1):56–83

    Article  PubMed  PubMed Central  Google Scholar 

  35. 35.

    Hirsh AV, Cameron KM, Tyler JP, Simpson J, Pryor JP (1980) The Doppler assessment of varicoceles and internal spermatic vein reflux in infertile men. Br J Urol 52(1):50–56

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 36.

    Dhabuwala CB, Kumar AB, Kerkar PD, Bhutawala A, Pierce J (1989) Patterns of Doppler recordings and its relationship to varicocele in infertile men. Int J Androl 12(6):430–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. 37.

    Sarteschi LM, Paoli R, Bianchini M, Menchini Fabris GF (1993) Lo studio del varicocele con eco-color-Doppler. G Ital Ultrasonologia 4(2):43–49

    Google Scholar 

  38. 38.

    Hoekstra T, Witt MA (1995) The correlation of internal spermatic vein palpability with ultrasonographic diameter and reversal of venous flow. J Urol 153(1):82–84

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. 39.

    Chiou RK, Anderson JC, Wobig RK et al (1997) Color Doppler ultrasound criteria to diagnose varicoceles: correlation of a new scoring system with physical examination. Urology. 50(6):953–956

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. 40.

    Cornud F, Belin X, Amar E, Delafontaine D, Helenon O, Moreau JF (1999) Varicocele: strategies in diagnosis and treatment. Eur Radiol 9(3):536–545

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Oyen RH (2002) Scrotal ultrasound. Eur Radiol 12(1):19–34

    Article  PubMed  PubMed Central  Google Scholar 

  42. 42.

    Pauroso S, Di Leo N, Fulle I, Di Segni M, Alessi S, Maggini E (2011) Varicocele: ultrasonographic assessment in daily clinical practice. J Ultrasound 14(4):199–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. 43.

    Iosa G, Lazzarini D (2013) Hemodynamic classification of varicoceles in men: our experience. J Ultrasound 16(2):57–63

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Patil V, Shetty SC, Das SK (2016) Redefining the criteria for grading varicoceles based on reflux times: a clinicoradiological correlation. Ultrasound Q 32(1):82–85

    Article  PubMed  PubMed Central  Google Scholar 

  45. 45.

    Wolverson MK, Houttuin E, Heiberg E, Sundaram M, Gregory J (1983) High-resolution real-time sonography of scrotal varicocele. AJR Am J Roentgenol 141(4):775–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. 46.

    Gonda RL Jr, Karo JJ, Forte RA, O'Donnell KT (1987) Diagnosis of subclinical varicocele in infertility. AJR Am J Roentgenol 148(1):71–75

    Article  PubMed  PubMed Central  Google Scholar 

  47. 47.

    Orda R, Sayfan J, Manor H, Witz E, Sofer Y (1987) Diagnosis of varicocele and postoperative evaluation using inguinal ultrasonography. Ann Surg 206(1):99–101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. 48.

    McClure RD, Khoo D, Jarvi K, Hricak H (1991) Subclinical varicocele: the effectiveness of varicocelectomy. J Urol 145(4):789–791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. 49.

    Eskew LA, Watson NE, Wolfman N, Bechtold R, Scharling E, Jarow JP (1993) Ultrasonographic diagnosis of varicoceles. Fertil Steril 60(4):693–697

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. 50.

    Pilatz A, Altinkilic B, Kohler E, Marconi M, Weidner W (2011) Color Doppler ultrasound imaging in varicoceles: is the venous diameter sufficient for predicting clinical and subclinical varicocele? World J Urol 29(5):645–650

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Jarow JP, Ogle SR, Eskew LA (1996) Seminal improvement following repair of ultrasound detected subclinical varicoceles. J Urol 155(4):1287–1290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. 52.

    Schiff JD, Li PS, Goldstein M (2006) Correlation of ultrasound-measured venous size and reversal of flow with Valsalva with improvement in semen-analysis parameters after varicocelectomy. Fertil Steril 86(1):250–252

    Article  PubMed  PubMed Central  Google Scholar 

  53. 53.

    Karami M, Mazdak H, Khanbabapour S, Adibi A, Nasr N (2014) Determination of the best position and site for color Doppler ultrasonographic evaluation of the testicular vein to define the clinical grades of varicocele ultrasonographically. Adv Biomed Res 3:17

    Article  PubMed  PubMed Central  Google Scholar 

  54. 54.

    Kim YS, Kim SK, Cho IC, Min SK (2015) Efficacy of scrotal Doppler ultrasonography with the Valsalva maneuver, standing position, and resting-Valsalva ratio for varicocele diagnosis. Korean J Urol 56(2):144–149

    Article  PubMed  PubMed Central  Google Scholar 

  55. 55.

    Cina A, Minnetti M, Pirronti T et al (2006) Sonographic quantitative evaluation of scrotal veins in healthy subjects: normative values and implications for the diagnosis of varicocele. Eur Urol 50(2):345–350

    Article  PubMed  PubMed Central  Google Scholar 

  56. 56.

    Metin A, Bulut O, Temizkan M (1991) Relationship between the left spermatic vein diameter measured by ultrasound and palpated varicocele and Doppler ultrasound findings. Int Urol Nephrol 23(1):65–68

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. 57.

    Zampieri N, Cervellione RM (2008) Varicocele in adolescents: a 6-year longitudinal and followup observational study. J Urol 180(4):1653–1656

    Article  PubMed  PubMed Central  Google Scholar 

  58. 58.

    Zhou T, Zhang W, Chen Q et al (2015) Effect of varicocelectomy on testis volume and semen parameters in adolescents: a meta-analysis. Asian J Androl 17(6):1012–1016

    Article  PubMed  PubMed Central  Google Scholar 

  59. 59.

    Sakamoto H, Saito K, Ogawa Y, Yoshida H (2008) Effects of varicocele repair in adults on ultrasonographically determined testicular volume and on semen profile. Urology. 71(3):485–489

    Article  PubMed  PubMed Central  Google Scholar 

  60. 60.

    Cornud F, Amar E, Hamida K, Thiounn N, Helenon O, Moreau JF (2000) Imaging in male hypofertility and impotence. BJU Int 86:153–163

    Article  PubMed  PubMed Central  Google Scholar 

  61. 61.

    Goede J, Hack WW, Sijstermans K et al (2011) Normative values for testicular volume measured by ultrasonography in a normal population from infancy to adolescence. Horm Res Paediatr 76(1):56–64

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. 62.

    Kim ED, Lipshultz LI (1996) Role of ultrasound in the assessment of male infertility. J Clin Ultrasound 24(8):437–453

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. 63.

    Condorelli R, Calogero AE, La Vignera S (2013) Relationship between testicular volume and conventional or nonconventional sperm parameters. Int J Endocrinol 2013:6

    Article  Google Scholar 

  64. 64.

    Tijani KH, Oyende BO, Awosanya GO, Ojewola RW, Yusuf AO (2014) Assessment of testicular volume: a comparison of fertile and sub-fertile West African men. Afr J Urol 20(3):136–140

    Article  Google Scholar 

  65. 65.

    Sakamoto H, Ogawa Y, Yoshida H (2008) Relationship between testicular volume and testicular function: comparison of the Prader orchidometric and ultrasonographic measurements in patients with infertility. Asian J Androl 10(2):319–324

    Article  PubMed  PubMed Central  Google Scholar 

  66. 66.

    Sakamoto H, Yajima T, Nagata M, Okumura T, Suzuki K, Ogawa Y (2008) Relationship between testicular size by ultrasonography and testicular function: measurement of testicular length, width, and depth in patients with infertility. Int J Urol 15(6):529–533

    Article  PubMed  PubMed Central  Google Scholar 

  67. 67.

    Lambert B (1951) The frequency of mumps and of mumps orchitis and the consequences for sexuality and fertility. Acta Genet Stat Med 2(Suppl. 1:1–166

    CAS  PubMed  PubMed Central  Google Scholar 

  68. 68.

    Mbaeri TU, Orakwe JC, Nwofor AME, Oranusi CK, Mbonu OO (2013) Ultrasound measurements of testicular volume: comparing the three common formulas with the true testicular volume determined by water displacement. Afr J Urol 19(2):69–73

    Article  Google Scholar 

  69. 69.

    Sakamoto H, Saito K, Oohta M, Inoue K, Ogawa Y, Yoshida H (2007) Testicular volume measurement: comparison of ultrasonography, orchidometry, and water displacement. Urology. 69(1):152–157

    Article  PubMed  PubMed Central  Google Scholar 

  70. 70.

    Liguori G, Trombetta C, Ollandini G et al (2009) Predictive factors of better improvement in semen quality after sclerotization of varicocele: preliminary report. J Androl Sci 16:47–53

    Google Scholar 

  71. 71.

    Abdel-Meguid TA, Al-Sayyad A, Tayib A, Farsi HM (2011) Does varicocele repair improve male infertility? An evidence-based perspective from a randomized, controlled trial. Eur Urol 59(3):455–461

    Article  PubMed  PubMed Central  Google Scholar 

  72. 72.

    Liguori G, Ollandini G, Pomara G et al (2010) Role of renospermatic basal reflow and age on semen quality improvement after sclerotization of varicocele. Urology. 75(5):1074–1078

    Article  PubMed  PubMed Central  Google Scholar 

  73. 73.

    Cornud F, Amar E, Hamida K, Helenon O, Moreau JF (2001) Ultrasound findings in male hypofertility and impotence. Eur Radiol 11(11):2126–2136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. 74.

    Kocakoc E, Serhatlioglu S, Kiris A, Bozgeyik Z, Ozdemir H, Bodakci MN (2003) Color Doppler sonographic evaluation of inter-relations between diameter, reflux and flow volume of testicular veins in varicocele. Eur Radiol 47(3):251–256

    Article  Google Scholar 

  75. 75.

    Kozakowski KA, Gjertson CK, Decastro GJ, Poon S, Gasalberti A, Glassberg KI (2009) Peak retrograde flow: a novel predictor of persistent, progressive and new onset asymmetry in adolescent varicocele. J Urol 181(6):2717–2722

    Article  PubMed  PubMed Central  Google Scholar 

  76. 76.

    Tasci AI, Resim S, Caskurlu T, Dincel C, Bayraktar Z, Gurbuz G (2001) Color Doppler ultrasonography and spectral analysis of venous flow in diagnosis of varicocele. Eur Urol 39(3):316–321

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. 77.

    Mohseni MJ, Nazari H, Amini E et al (2011) Shunt-type and stop-type varicocele in adolescents: prognostic value of these two different hemodynamic patterns. Fertil Steril 96(5):1091–1096

    Article  PubMed  PubMed Central  Google Scholar 

  78. 78.

    Glassberg KI (2014) My indications for treatment of the adolescent varicocele (and why?). Trans Androl Urol 3(4):402–412

    Google Scholar 

  79. 79.

    Paduch DA, Niedzielski J (1997) Repair versus observation in adolescent varicocele: a prospective study. J Urol 158(3):1128–1132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. 80.

    Poon SA, Gjertson CK, Mercado MA, Raimondi PM, Kozakowski KA, Glassberg KI (2010) Testicular asymmetry and adolescent varicoceles managed expectantly. J Urol 183(2):731–734

    Article  PubMed  PubMed Central  Google Scholar 

  81. 81.

    Morteza T, Ehsan A (2016) Quantitative Doppler assessment of flow characteristics in pampiniform venous plexus, in patients with varicocele: is there any relationship with semen analysis? PJR. 20(3):121–124

    Google Scholar 

  82. 82.

    Van Batavia JP, Badalato G, Fast A, Glassberg KI (2013) Adolescent varicocele-is the 20/38 harbinger a durable predictor of testicular asymmetry? J Urol 189(5):1897–1902

    Article  PubMed  PubMed Central  Google Scholar 

  83. 83.

    Hsu HS, Chang LS, Cheng MT, Wei YH (1994) Decreased blood flow and defective energy metabolism in the varicocele-bearing testicles of rats. Eur Urol 25:71–75

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. 84.

    Zhang M, Du L, Liu Z, Qi H, Chu Q (2014) The effects of varicocelectomy on testicular arterial blood flow: laparoscopic surgery versus microsurgery. Urol J 11(5):1900–1906

    PubMed  PubMed Central  Google Scholar 

  85. 85.

    Grasso FL, Pepe P, Panella P, Pepe F (1997) Volocimetric evaluation of spermatic vessels with echo color Doppler in patients with idiopathic varicocele. Minerva Urol Nefrol 49(4):179–182

    Google Scholar 

  86. 86.

    Ross JA, Watson JN Jr, Jarow JP (1994) The effect of varicoceles on testicular blood flow in man. Urology. 44(4):535–539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. 87.

    Akcar N, Turgut M, Adapinar B, Ozkan IR (2004) Intratesticular arterial resistance and testicular volume in infertile men with subclinical varicocele. J Clin Ultrasound 32(8):389–393

    Article  PubMed  PubMed Central  Google Scholar 

  88. 88.

    Tarhan S, Gumus B, Gunduz I, Ayyildiz V, Goktan C (2003) Effect of varicocele on testicular artery blood flow in men color Doppler investigation. Scand J Urol Nephrol 37(1):38–42

    Article  PubMed  PubMed Central  Google Scholar 

  89. 89.

    Biagiotti G, Cavallini G, Modenini F, Vitali G, Gianaroli L (2002) Spermatogenesis and spectral echo-colour Doppler traces from the main testicular artery. BJU Int 90(9):903–908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. 90.

    Unsal A, Turgut AT, Taskin F, Kosar U, Karaman CZ (2007) Resistance and pulsatility index increase in capsular branches of testicular artery: indicator of impaired testicular microcirculation in varicocele? J Clin Ultrasound 35(4):191–195

    Article  PubMed  PubMed Central  Google Scholar 

  91. 91.

    Baigorri BF, Dixon RG (2016) Varicocele: a review. Semin Intervent Radiol 33(3):170–176

    Article  PubMed  PubMed Central  Google Scholar 

  92. 92.

    (1985) Comparison among different methods for the diagnosis of varicocele. World Health Organisation.. Fertil Steril 43(4):575–582

  93. 93.

    Cariati M, Pieri S, Agresti P et al (2012) Diagnosis of right-sided varicocele: a retrospective comparative study between clinical examination, Doppler findings, US imaging and vascular anatomy at phlebography. Eur J Radiol 81(9):1998–2006

    Article  PubMed  PubMed Central  Google Scholar 

  94. 94.

    DeCastro GJ, Shabsigh A, Poon SA, Laor L, Glassberg KI (2009) Adolescent varicocelectomy - is the potential for catch-up growth related to age and/or Tanner stage? J Urol 181(1):322–327

    Article  PubMed  PubMed Central  Google Scholar 

  95. 95.

    Gat Y, Bachar GN, Zukerman Z, Belenky A, Gorenish M (2004) Physical examination may miss the diagnosis of bilateral varicocele: a comparative study of 4 diagnostic modalities. J Urol 172(4):1414–1417

    Article  PubMed  PubMed Central  Google Scholar 

  96. 96.

    Pfeiffer D, Berger J, Schoop C, Tauber R (2006) A Doppler-based study on the prevalence of varicocele in German children and adolescents. Andrologia. 38(1):13–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. 97.

    Preziosi P, Miano R, Bitelli M, Ciolfi MG, Micali S, Micali F (2001) Right varicocele associated with inferior vena cava malformation in situs inversus: percutaneous treatment with retrograde sclerotherapy. J Endourol 15(10):1001–1003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. 98.

    Ding H, Tian J, Du W, Zhang L, Wang H, Wang Z (2012) Open non-microsurgical, laparoscopic or open microsurgical varicocelectomy for male infertility: a meta-analysis of randomized controlled trials. BJU Int 110(10):1536–1542

    Article  PubMed  PubMed Central  Google Scholar 

  99. 99.

    Cervellione RM, Corroppolo M, Bianchi A (2008) Subclinical varicocele in the pediatric age group. J Urol 179(2):717–719

    Article  PubMed  PubMed Central  Google Scholar 

  100. 100.

    Zampieri N, Dall’Agnola A (2011) Subclinical varicocele and sports: a longitudinal study. Urology. 77(5):1199–1202

    Article  PubMed  PubMed Central  Google Scholar 

  101. 101.

    Diamond DA (2007) Adolescent varicocele. Curr Opin Urol 17(4):263–267

    Article  PubMed  PubMed Central  Google Scholar 

  102. 102.

    Cvitanic OA, Cronan JJ, Sigman M, Landau ST (1993) Varicoceles: postoperative prevalence-a prospective study with color Doppler US. Radiology. 187(3):711–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. 103.

    Rotker K, Sigman M (2016) Recurrent varicocele. Asian J Androl 18(2):229–233

    Article  PubMed  PubMed Central  Google Scholar 

  104. 104.

    Glassberg KI, Badalato GM, Poon SA, Mercado MA, Raimondi PM, Gasalberti A (2011) Evaluation and management of the persistent/recurrent varicocele. Urology. 77(5):1194–1198

    Article  PubMed  PubMed Central  Google Scholar 

  105. 105.

    Kwak N, Siegel D (2014) Imaging and interventional therapy for varicoceles. Curr Urol Rep 15(4):399

  106. 106.

    El-Haggar S, Nassef S, Gadalla A, Latif A, Mostafa T (2012) Ultrasonographic parameters of the spermatic veins at the inguinal and scrotal levels in varicocele diagnosis and post-operative repair. Andrologia. 44(3):210–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. 107.

    Winkelbauer FW, Ammann ME, Karnel F, Lammer J (1994) Doppler sonography of varicocele: long-term follow-up after venography and transcatheter sclerotherapy. J Ultrasound Med 13(12):953–958

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. 108.

    Palazzo S, Boezio F, Mancini V et al (2002) Significance of scrotal Doppler color ultrasonography in the postoperative control of patients treated with varicocelectomy. Arch Ital Urol Androl 74(4):247–249

    PubMed  PubMed Central  Google Scholar 

  109. 109.

    Hauser R, Yogev L, Greif M et al (1997) Sperm binding and ultrasound changes after operative repair of varicocele: correlation with fecundity. Andrologia. 29(3):145–147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. 110.

    Zucchi A, Mearini L, Mearini E, Fioretti F, Bini V, Porena M (2006) Varicocele and fertility: relationship between testicular volume and seminal parameters before and after treatment. J Androl 27(4):548–551

    Article  PubMed  PubMed Central  Google Scholar 

  111. 111.

    Trombetta C, Salisci E, Deriu M et al (1993) Echo-flowmetric control 6 years after percutaneous treatment of varicocele. Arch Ital Urol Androl 65(4):363–367

    CAS  PubMed  PubMed Central  Google Scholar 

  112. 112.

    Haller J, Gritzmann N, Czembirek H et al (1986) Pulsed duplex sonographic follow-up of varicoceles following sclerotherapy. Rofo. 145(5):547–550

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. 113.

    Hamm B, Sorensen R, Berger T (1986) Non-invasive imaging procedures in the diagnosis and control of therapy of varicoceles. 2. Importance of thermography and sonography for therapy control following sclerotherapy of varicoceles. Rofo. 144(6):665–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. 114.

    Mastrojeni C, Pagano G, Scalisi M, Leonello G, Manfré A, Versaci A (2001) Idiopathic varicocele. Diagnosis and follow-up with CW-Doppler and echo-color-Doppler: our experience. G Chir. 22(1-2):41–44

  115. 115.

    Cil AS, Bozkurt M, Bozkurt DK, Gok M (2015) Investigating the relationship between persistent reflux flow on the first postoperative day and recurrent varicocele in varicocelectomy patients. J Clin Med Res 7(1):29–32

    Article  PubMed  PubMed Central  Google Scholar 

  116. 116.

    El-Saeity NS, Sidhu PS (2006) “Scrotal varicocele, exclude a renal tumour”. Is this evidence based? Clin Radiol 61(7):593–599

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. 117.

    Spittel JA Jr, DeWeerd JH, Shick RM (1959) Acute varicocele: a vascular clue to renal tumor. Proc Staff Meet Mayo Clin 34(5):134–137

    PubMed  PubMed Central  Google Scholar 

  118. 118.

    Gibbons RP, Monte JE, Correa RJ Jr, Mason JT (1976) Manifestations of renal cell carcinoma. Urology. 8(3):201–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. 119.

    Skinner DG, Colvin RB, Vermillion CD, Pfister RC, Leadbetter WF (1971) Diagnosis and management of renal cell carcinoma. A clinical and pathologic study of 309 cases. Cancer. 28(5):1165–1177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. 120.

    El Abiad Y, Qarro A (2016) Acute varicocele revealing renal cancer. N Engl J Med 374(21):2075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. 121.

    Bate J (1927) Symptomatic varicocele. J Urol 18(6):649–662

    Article  Google Scholar 

  122. 122.

    Ding GX, Song NH, Feng CC et al (2012) Is there an association between advanced stage of renal cell carcinoma and paraneoplastic syndrome? Med Princ Pract 21(4):370–374

    Article  PubMed  PubMed Central  Google Scholar 

  123. 123.

    Ates N, Yuksel M, Ylmaz S, Habibi M, Ipekci T (2016) Retroperitoneal paraganglioma presenting as right-sided varicocele: case report. Ann Saudi Med 36(2):148–151

    Article  PubMed  PubMed Central  Google Scholar 

  124. 124.

    Arrabal-Polo MA, Merino-Salas S (2013) Acute left varicocele in an adult. CMAJ. 185(4):323

    Article  PubMed  PubMed Central  Google Scholar 

  125. 125.

    Chandramohan S, Chakravertry S (2007) Re: “Scrotal varicocoele, exclude a renal tumour”. Is this evidence based? Clin Radiol 62(2):192–193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. 126.

    Espinosa Bravo R, Lemourt Oliva M, Pérez Monzón AF et al (2003) Carcinoma de células renales y varicocele izquierdo de forma simultánea. Arch Esp Urol 56(5):533–535

    PubMed  PubMed Central  Google Scholar 

  127. 127.

    Robson J, Wolstenhulme S, Knapp P (2012) Is there a co-association between renal or retroperitoneal tumours and scrotal varicoceles? A systematic review. Ultrasound. 20(4):182–191

    Article  Google Scholar 

  128. 128.

    Oster J (1971) Varicocele in children and adolescents: an investigation of the incidence among Danish school children. Scand J Urol Nephrol 5(1):27–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. 129.

    Akbay E, Cayan S, Doruk E, Duce MN, Bozlu M (2000) The prevalence of varicocele and varicocele-related testicular atrophy in Turkish children and adolescents. BJU Int 86(4):490–493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  130. 130.

    Erginel B, Vural S, Akin M et al (2014) Wilms’ tumor: a 24-year retrospective study from a single center. Pediatr Hematol Oncol 31(5):409–414

    Article  PubMed  PubMed Central  Google Scholar 

  131. 131.

    Pavan N, Bucci S, Mazzon G, Bertolotto M, Trombetta C, Liguori G (2015) It’s not always varicocele: a strange case of Zinner syndrome. Can Urol Assoc J 9(7-8):E535–E538

    Article  PubMed  PubMed Central  Google Scholar 

  132. 132.

    Conzi R, Damasio MB, Bertolotto M et al (2017) Sonography of scrotal wall lesions and correlation with other modalities. J Ultrasound Med 36(10):2149–2163

    Article  PubMed  PubMed Central  Google Scholar 

  133. 133.

    Secil M, Bertolotto M, Rocher L et al (2017) Imaging features of paratesticular masses. J Ultrasound Med 36(7):1487–1509

    Article  PubMed  PubMed Central  Google Scholar 

  134. 134.

    Yilmaz C, Arslan M, Arslan M (2009) Intrascrotal arteriovenous malformation simulating varicocele. AJR Am J Roentgenol 192(6):W351

    Article  PubMed  PubMed Central  Google Scholar 

  135. 135.

    Bhatt S, Jafri SZ, Wasserman N, Dogra VS (2011) Imaging of non-neoplastic intratesticular masses. Diagn Interv Radiol 17(1):52–63

    PubMed  PubMed Central  Google Scholar 

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The scientific guarantor of this publication is Dr. Simon Freeman on behalf of the Scrotal and Penile Imaging Working Group of the European Society of Urogenital Radiology (ESUR-SPIWG).

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Freeman, S., Bertolotto, M., Richenberg, J. et al. Ultrasound evaluation of varicoceles: guidelines and recommendations of the European Society of Urogenital Radiology Scrotal and Penile Imaging Working Group (ESUR-SPIWG) for detection, classification, and grading. Eur Radiol 30, 11–25 (2020). https://doi.org/10.1007/s00330-019-06280-y

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Keywords

  • Varicocele
  • Scrotum
  • Infertility, male
  • Ultrasonography
  • Ultrasonography, Doppler