Журналов:     Статей:        

Андрология и генитальная хирургия. 2023; 24: 49-57

Клиническое значение варикоцелэктомии: обзор литературы

Олефир Ю. В., Ефремов Е. А., Родионов М. А., Живулько А. Р., Попов Д. М., Монаков Д. М., Фаниев М. В.

https://doi.org/10.17650/2070-9781-2023-24-2-49-57

Аннотация

Оперативное лечение клинически значимого варикоцеле у бесплодных мужчин с патоспермией является общепринятой практикой. Однако уже длительное время не решенными остаются вопросы о роли этого заболевания в патогенезе таких состояний, как гипогонадизм и орхалгия, а также о роли варикоцелэктомии в устранении болевой симптоматики в мошонке и повышении уровня тестостерона. Предметом дискуссии остается и целесообразность оперативного лечения варикоцеле у пациентов с азооспермией.

Список литературы

1. Jensen C.F.S., Østergren P., Dupree J.M. et al. Varicocele and male infertility. Nat Rev Urol 2017;14(9):523–33. DOI: 10.1038/nrurol.2017.98

2. Peterson A.C., Lance R.S., Ruiz H.E. Outcomes of varicocele ligation done for pain. J Urol 1998;159(5):1565–7. DOI: 10.1097/00005392-199805000-00043

3. Shridharani A., Lockwood G., Sandlow J. Varicocelectomy in the treatment of testicular pain: a review. Curr Opin Urol 2012;22(6):499–506. DOI: 10.1097/MOU.0b013e328358f69f

4. Котов С.В., Корочкин Н.Д., Клименко А.А. Рецидивное варикоцеле. Вестник урологии 2021;9(2):132–41. DOI: 10.21886/2308-6424-2021-9-2-132-141

5. Жуков О.Б., Капто А.А., Михайленко Д.С., Евдокимов В.В. Варикозная болезнь органов таза мужчины. Андрология и генитальная хирургия 2016;17(4):72–7. DOI: 10.17650/2070-9781-2016-17-4-72-77

6. Yaman O., Ozdiler E., Anafarta K., Göğüş O. Effect of microsurgical subinguinal varicocele ligation to treat pain. Urology 2000;55(1):107–8. DOI: 10.1016/S0090-4295(99)00374-X

7. Schlegel P.N., Goldstein M. Alternate indications for varicocele repair: non-obstructive azoospermia, pain, androgen deficiency and progressive testicular dysfunction. Fertil Steril 2011;96(6):1288–93. DOI: 10.1016/j.fertnstert.2011.10.033

8. Muthuveloe D.W., During V., Ashdown D. et al. The effectiveness of varicocele embolisation for the treatment of varicocele related orchalgia. Springer Plus 2015;4(1):392. DOI: 10.1186/s40064-015-1177-2

9. Elzanaty S., Johansen C.E. Microsurgical varicocele repair on men with grade III lesions and chronic dull scrotal pain: a pilot study. Curr Urol 2015;8(1):29–31. DOI: 10.1159/000365685

10. Han D.Y., Yang Q.Y., Chen X. et al. Who will benefit from surgical repair for painful varicocele: a meta-analysis. Int Urol Nephrol 2016;48(7):1071–8. DOI: 10.1007/s11255-016-1246-7

11. Karademir K., Senkul T., Baykal K. et al. Evaluation of the role of varicocelectomy including external spermatic vein ligation in patients with scrotal pain. Int J Urol 2005;12(5):484–8. DOI: 10.1111/j.1442-2042.2005.01063.x

12. Maghraby H.A. Laparoscopic varicocelectomy for painful varicoceles: merits and outcomes. J Endourol 2002;16(2):107–10. DOI: 10.1089/089277902753619627

13. Parekattil S.J., Brahmbhatt J.V. Robotic approaches for male infertility and chronic orchialgia microsurgery. Curr Opin Urol 2011;21(6):493–9. DOI: 10.1097/MOU.0b013e32834bb783

14. Chawla A., Kulkarni G., Kamal K., Zini A. Microsurgical varicocelectomy for recurrent or persistent varicoceles associated with orchalgia. Urology 2005;66(5):1072–4. DOI: 10.1016/j.urology.2005.05.052

15. Reşorlu B., Kara C., Sahin E., Unsal A. et al. The significance of age on success of surgery for patients with varicocele. Int Urol Nephrol 2010;42(2):351–6. DOI: 10.1007/s11255-009-9589-y

16. Park H.J., Lee S.S., Park N.C. Predictors of pain resolution after varicocelectomy for painful varicocele. Asian J Androl 2011;13(5):754–8. DOI: 10.1038/aja.2010.87

17. Kim S.O., Jung H., Park K. Outcomes of microsurgical subinguinal varicocelectomy for painful varicoceles. J Androl 2012;33(5):872–5. DOI: 10.2164/jandrol.111.014993

18. Chen L.K., Chen S.S. Risk factors for developing pain in normospermic patients with varicocoele. Int J Androl 2012;35:176–80. DOI: 10.1111/j.1365-2605.2011.01215.x

19. Handel L.N., Shetty R., Sigman M. The relationship between varicoceles and obesity. J Urol 2006;176(5):2138–40; discussion 2140. DOI: 10.1016/j.juro.2006.07.023

20. Soylemez H., Atar M., Ali Sancaktutar A. et al. Varicocele among healthy young men in Turkey; prevalence and relationship with body mass index. Int Braz J Urol 2012;38(1):116–21. DOI: 10.1590/S1677-55382012000100016

21. Bungum M., Humaidan P., Axmon A. et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod 2007;22(1):174–9. DOI: 10.1093/humrep/del326

22. Collins J.A., Barnhart K.T., Schlegel P.N. Do sperm DNA integrity tests predict pregnancy with in vitro fertilization? Fertil Steril 2008;89(4):823–31. DOI: 10.1016/j.fertnstert.2007.04.055

23. Giwercman A., Lindstedt L., Larsson M. et al. Sperm chromatin structure assay as an independent predictor of fertility in vivo: a case-control study. Int J Androl 2010;33(1):e221–7. DOI: 10.1111/j.1365-2605.2009.00995.x

24. Henkel R., Hajimohammad M., Stalf T. et al. Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril 2004;81(4):965–72. DOI: 10.1016/j.fertnstert.2003.09.044

25. Virro M.R., Larson-Cook K.L., Evenson D.P. Sperm chromatin structure assay (SCSA) parameters are related to fertilization, blastocyst development, and ongoing pregnancy in in vitro fertilization and intracytoplasmic sperm injection cycles. Fertil Steril 2004;81(5):1289–95. DOI: 10.1016/j.fertnstert.2003.09.063

26. Lopes S., Sun J.G., Jurisicova A. et al. Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril 1998;69(3):528–32. DOI: 10.1016/S0015-0282(97)00536-0

27. De Iuliis G.N., Thomson L.K., Mitchell L.A. et al. DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2’- deoxyguanosine, a marker of oxidative stress. Biol Reprod 2009;81(3):517–24. DOI: 10.1095/biolreprod.109.076836

28. Sakkas D., Seli E., Bizzaro D. et al. Abnormal spermatozoa in the ejaculate: abortive apoptosis and faulty nuclear remodelling during spermatogenesis. Reprod Biomed Online 2003;7(4):428–32. DOI: 10.1016/S1472-6483(10)61886-X

29. Tremellen K. Oxidative stress and male infertility – a clinical perspective. Hum Reprod Update 2008;14(3):243–58. DOI: 10.1093/humupd/dmn004

30. Sun J.G., Jurisicova A., Casper R.F. Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 1997;56(3):602–7. DOI: 10.1095/biolreprod56.3.602

31. Allamaneni S.S., Naughton C.K., Sharma R.K. et al. Increased seminal reactive oxygen species levels in patients with varicoceles correlate with varicocele grade but not with testis size. Fertil Steril 2004;82(6):1684–6. DOI: 10.1016/j.fertnstert.2004.04.071

32. Mancini A., Meucci E., Milardi D. et al. Seminal antioxidant capacity in pre- and postoperative varicocele. J Androl 2004;25(1):44–9. DOI: 10.1002/j.1939-4640.2004.tb02757.x

33. Saleh R.A., Agarwal A., Sharma R.K. et al. Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertil Steril 2003;80(6):1431–6. DOI: 10.1016/S0015-0282(03)02211-8

34. Schoor R.A., Elhanbly S.M., Niederberger C. The pathophysiology of varicocele-associated male infertility. Curr Urol Rep 2001;2(6):432–6. DOI: 10.1007/s11934-001-0035-7

35. Naughton C.K., Nangia A.K., Agarwal A. Pathophysiology of varicoceles in male infertility. Hum Reprod Update 2001;7(5):473–81. DOI: 10.1093/humupd/7.5.473

36. Nallella K.P., Allamaneni S.S., Pasqualotto F.F. et al. Relationship of interleukin-6 with semen characteristics and oxidative stress in patients with varicocele. Urology 2004;64(5):1010–3. DOI: 10.1016/j.urology.2004.05.045

37. Гамидов С.И., Овчинников Р.И., Попова А.Ю. и др. Адъювантная антиоксидантная терапия у больных бесплодием при варикоцеле. Урология 2017;2(suppl):64–72. DOI: 10.18565/urol.2017.2-supplement.64-72

38. Köksal I.T., Tefekli A., Usta M. et al. The role of reactive oxygen species in testicular dysfunction associated with varicocele. BJU Int 2000;86(4):549–52. DOI: 10.1046/j.1464-410X.2000.00755.x

39. Blumer C.G., Restelli A.E., Giudice P.T. et al. Effect of varicocele on sperm function and semen oxidative stress. BJU Int 2012;109(2):259–65. DOI: 10.1111/j.1464-410X.2011.10240.x

40. Romeo C., Ientile R., Santoro G. et al. Nitric oxide production is increased in the spermatic veins of adolescents with left idiophatic varicocele. J Pediatr Surg 2001;36(2):389–93. DOI: 10.1053/jpsu.2001.20724

41. Pasqualotto F.F., Sundaram A., Sharma R.K. et al. Semen quality and oxidative stress scores in fertile and infertile patients with varicocele. Fertil Steril 2008;89(3):602–7. DOI: 10.1016/j.fertnstert.2007.03.057

42. Mostafa T., Anis T.H., El-Nashar A. et al. Varicocelectomy reduces reactive oxygen species levels and increases antioxidant activity of seminal plasma from infertile men with varicocele. Int J Androl 2001;24(5):261–5. DOI: 10.1046/j.1365-2605.2001.00296.x

43. Cervellione R.M., Cervato G., Zampieri N. et al. Effect of varicocelectomy on the plasma oxidative stress parameters. J Pediatr Surg 2006;41(2):403–6. DOI: 10.1016/j.jpedsurg.2005.11.018

44. Hurtado de Catalfo G.E., Ranieri-Casilla A., Marra F.A. et al. Oxidative stress biomarkers and hormonal profile in human patients undergoing varicocelectomy. Int J Androl 2007;30(6):519–30. DOI: 10.1111/j.1365-2605.2007.00753.x

45. Chen S.S., Huang W.J., Chang L.S., Wei Y.H. Attenuation of oxidative stress after varicocelectomy in subfertile patients with varicocele. J Urol 2008;179(2):639–42. DOI: 10.1016/j.juro.2007.09.039

46. Sakamoto Y., Ishikawa T., Kondo Y. et al. The assessment of oxidative stress in infertile patients with varicocele. BJU Int 2008;101(12):1547–52. DOI: 10.1111/j.1464-410X.2008.07517.x

47. Dada R., Shamsi M.B., Venkatesh S. et al. Attenuation of oxidative stress & DNA damage in varicocelectomy: implications in infertility management. Indian J Med Res 2010;132(6):728–30.

48. Rodriguez Peña M, Alescio L, Russell A, et al. Predictors of improved seminal parameters and fertility after varicocele repair in young adults. Andrologia 2009;41(5):277–81. DOI: 10.1111/j.1439-0272.2009.00919.x

49. Lacerda J.I., Del Giudice P.T., da Silva B.F. et al. Adolescent varicocele: improved sperm function after varicocelectomy. Fertil Steril 2011;95(3):994–9. DOI: 10.1016/j.fertnstert.2010.10.031

50. Smith R., Kaune H., Parodi D. et al. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod 2006;21(4):986–93. DOI: 10.1093/humrep/dei429

51. Blumer C.G., Fariello R.M., Restelli A.E. et al. Sperm nuclear DNA fragmentation and mitochondrial activity in men with varicocele. Fertil Steril 2008;90(5):171–22. DOI: 10.1016/j.fertnstert.2007.09.007

52. Chen C.H., Lee S.S., Chen D.C. et al. Apoptosis and kinematics of ejaculated spermatozoa in patients with varicocele. J Androl 2004;25(3):348–53. DOI: 10.1002/j.1939-4640.2004.tb02799.x

53. Bertolla R.P., Cedenho A.P., Hassun Filho P.A. et al. Sperm nuclear DNA fragmentation in adolescents with varicocele. Fertil Steril 2006;85(3):625–8. DOI: 10.1016/j.fertnstert.2005.08.032

54. Zini A, Dohle G. Are varicoceles associated with increased deoxyribonucleic acid fragmentation? Fertil Steril 2011;96(6):1283–7. DOI: 10.1016/j.fertnstert.2011.10.016

55. Zini A., Azhar R., Baazeem A., Gabriel M.S. Effect of microsurgical varicocelectomy on human sperm chromatin and DNA integrity: a prospective trial. Int J Androl 2011;34(1):14–9. DOI: 10.1111/j.1365-2605.2009.01048.x

56. Werthman P., Wixon R., Kasperson K., Evenson D.P. Significant decrease in sperm deoxyribonucleic acid fragmentation after varicocelectomy. Fertil Steril 2008;90(5):1800–4. DOI: 10.1016/j.fertnstert.2006.09.019

57. Marmar J.L., Agarwal A., Prabakaran S. et al. Reassessing the value of varicocelectomy as a treatment for male subfertility with a new meta-analysis. Fertil Steril 2007;88(3):639–48. DOI: 10.1016/j.fertnstert.2006.12.008

58. Smit M., Romijn J.C., Wildhagen M.F. et al. Decreased sperm DNA fragmentation after surgical varicocelectomy is associated with increased pregnancy rate. J Urol 2010;183(1):270–4. DOI: 10.1016/j.juro.2009.08.161

59. Baker K., McGill J., Sharma R. et al. Pregnancy after varicocelectomy: impact of postoperative motility and DFI. Urology 2013;81(4):760–6. DOI: 10.1016/j.urology.2012.12.005

60. Leung L., Ho K.L., Tam P.C., Yiu M.K. Subinguinal microsurgical varicocelectomy for male factor subfertility: ten-year experience. Hong Kong Med J 2013;19(4):334–40. DOI: 10.12809/hkmj133884

61. Practice Committee of American Society for Reproductive Medicine. Report on varicocele and infertility. Fertil Steril 2008;90(5 Suppl):S247–9. DOI: 10.1016/j.fertnstert.2008.08.050

62. Agarwal A., Deepinder F., Cocuzza M. et al. Efficacy of varicocelectomy in improving semen parameters: new metaanalytical approach. Urology 2007;70(3):532–8. DOI: 10.1016/j.urology.2007.04.011

63. French D.B., Desai N.R., Agarwal A. Varicocele repair: does it still have a role in infertility treatment? Curr Opin Obstet Gynecol 2008;20(3):269–74. DOI: 10.1097/GCO.0b013e3282fcc00c

64. Acar H., Kilinc M., Guven S. et al. Comparison of semen profile and frequency of chromosome aneuploidies in sperm nuclei of patients with varicocele before and after varicocelectomy. Andrologia 2009;41(3):157–62. DOI: 10.1111/j.1439-0272.2008.00907.x

65. Mansour Ghanaie M., Asgari S.A., Dadrass N. et al. Effects of varicocele repair on spontaneous first trimester miscarriage: a randomized clinical trial. Urol J 2012;9(2):505–13.

66. Nasr-Esfahani M.H., Abasi H., Razavi S. et al. Varicocelectomy: semen parameters and protamine deficiency. Int J Androl 2009;32(2):115–22. DOI: 10.1111/j.1365-2605.2007.00822.x

67. Pirke K.M., Vogt H.J., Sintermann R., Spyra B. Testosterone in peripheral plasma, spermatic vein and in testicular tissue under basal conditions and after HCG-stimulation in patients with varicocele. Andrologia 1983;15(6):637–41. DOI: 10.1111/j.1439-0272.1983.tb00179.x

68. Abdel-Meguid T.A., Farsi H.M., Al-Sayyad A. et al. Effects of varicocele on serum testosterone and changes of testosterone after varicocelectomy: a prospective controlled study. Urology 2014;84(5):1081–7. DOI: 10.1016/j.urology.2014.05.029

69. Tanrikut C., Goldstein M., Rosoff J.S. et al. Varicocele as a risk factor for androgen deficiency and effect of repair. BJU Int 2011;108(9):1480–4. DOI: 10.1111/j.1464-410X.2010.10030.x

70. Goldstein M., Eid J.F. Elevation of intratesticular and scrotal skin surface temperature in men with varicocele. J Urol 1989;142(3):743–5. DOI: 10.1016/S0022-5347(17)38874-2

71. Li F., Yue H., Yamaguchi K. et al. Effect of surgical repair on testosterone production in infertile men with varicocele: a metaanalysis. Int J Urol 2012;19(2):149–54. DOI: 10.1111/j.1442-2042.2011.02890.x

72. Hsiao W., Rosoff J.S., Pale J.R. et al. Older age is associated with similar improvements in semen parameters and testosterone after subinguinal microsurgical varicocelectomy. J Urol 2011;185(2):620–5. DOI: 10.1016/j.juro.2010.09.114

73. Zohdy W., Ghazi S., Arafa M. Impact of varicocelectomy on gonadal and erectile functions in men with hypogonadism and infertility. J Sex Med 2011;8(3):885–93. DOI: 10.1111/j.1743-6109.2010.01974.x

74. Sathya Srini V., Belur Veerachari S. Does varicocelectomy improve gonadal function in men with hypogonadism and infertility? Analysis of a prospective study. Int J Endocrinol 2011;2011:916380. DOI: 10.1155/2011/916380

75. Hsiao W., Rosoff J.S., Pale J.R. et al. Varicocelectomy is associated with increases in serum testosterone independent of clinical grade. Urology 2013;81(6):1213–7. DOI: 10.1016/j.urology.2013.01.060

76. Esteves S.C. Clinical management of infertile men with nonobstructive azoospermia. Asian J Androl 2015;17(3):459–70. DOI: 10.4103/1008-682X.148719

77. Попова А.Ю., Гамидов С.И., Овчинников Р.И. и др. Варикоцеле и необструктивная азооспермия – с чего начать? Андрология и генитальная хирургия 2017;18(4):77–80. DOI: 10.17650/2070-9781-2017-18-4-77-80

78. Gat Y., Bachar G.N., Everaert K. et al. Induction of spermatogenesis in azoospermic men after internal spermatic vein embolization for the treatment of varicocele. Hum Reprod 2005;20(4):1013–7. DOI: 10.1093/humrep/deh706

79. Esteves S.C., Miyaoka R., Agarwal A. Sperm retrieval techniques for assisted reproduction. Int Braz J Urol 2011;37(5):570–83. DOI: 10.1590/S1677-55382011000500002

80. Matthews G.J., Matthews E.D., Goldstein M. Induction of spermatogenesis and achievement of pregnancy after microsurgical varicocelectomy in men with azoospermia and severe oligoasthenospermia. Fertil Steril 1998;70(1):71–5. DOI: 10.1016/S0015-0282(98)00108-3

81. Poulakis V., Ferakis N., de Vries R. et al. Induction of spermatogenesis in men with azoospermia or severe oligoteratoasthenospermia after antegrade internal spermatic vein sclerotherapy for the treatment of varicocele. Asian J Androl 2006;8(5):613–9. DOI: 10.1111/j.1745-7262.2006.00157.x

82. Abdel-Meguid T.A., Al-Sayyad A., Tayib A., Farsi H.M. Does varicocele repair improve male infertility? An evidence-based perspective from a randomized, controlled trial. Eur Urol 2011;59(3):455–61. DOI: 10.1016/j.eururo.2010.12.008

83. Kiraç M., Deniz N., Biri H. The effect of microsurgical varicocelectomy on semen parameters in men with non-obstructive azoospermia. Curr Urol 2013;6(3):136–40. DOI: 10.1159/000343527

84. Schlegel P.N., Kaufmann J. Role of varicocelectomy in men with nonobstructive azoospermia. Fertil Steril 2004;81(6):1585–8. DOI: 10.1016/j.fertnstert.2003.10.036

85. Tung M.C., Huang W.J., Chen K.K. Modified subinguinal varicocelectomy for painful varicocele and varicocele-associated infertility. J Chin Med Assoc 2004;67(6):296–300.

86. Pasqualotto F.F., Sobreiro B.P., Hallak J. et al. Induction of spermatogenesis in azoospermic men after varicocelectomy repair: an update. Fertil Steril 2006;85(3):635–9. DOI: 10.1016/j.fertnstert.2005.08.043

87. Esteves S.C., Glina S. Recovery of spermatogenesis after microsurgical subinguinal varicocele repair in azoospermic men based on testicular histology. Int Braz J Urol 2005;31(6):541–8. DOI: 10.1590/S1677-55382005000600005

88. Esteves S.C., Miyaoka R., Roque M., Agarwal A. Outcome of varicocele repair in men with nonobstructive azoospermia: systematic review and meta-analysis. Asian J Androl 2016;18(2):246–53. DOI: 10.4103/1008-682X.169562

89. Ustuner M., Yilmaz H., Yavuz U. et al. Varicocele repair improves testicular histology in men with nonobstructive azoospermia. Biomed Res Int 2015;2015:709452. DOI: 10.1155/2015/709452

90. Yamamoto M., Hibi H., Hirata Y. et al. Effect of varicocelectomy on sperm parameters and pregnancy rate in patients with subclinical varicocele: a randomized prospective controlled study. J Urol 1996;155(5):1636–8.

91. Kroese A.C., de Lange N.M., Collins J., Evers J.L. Surgery or embolization for varicoceles in subfertile men. Cochrane Database Syst Rev 2012;10:CD000479. DOI: 10.1002/14651858.CD000479.pub5

92. Kim K.H., Lee J.Y., Kang D.H. et al. 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 2013;54(10):703–9. DOI: 10.4111/kju.2013.54.10.703

93. Kirby E.W., Wiener L.E., Rajanahally S. et al. Undergoing varicocele repair before assisted reproduction improves pregnancy rate and live birth rate in azoospermic and oligospermic men with a varicocele: a systematic review and meta-analysis. Fertil Steril 2016;106(6):1338–43. DOI: 10.1016/j.fertnstert.2016.07.1093

Andrology and Genital Surgery. 2023; 24: 49-57

Clinical significance of varicocelectomy: literature review

Olefir Yu. V., Efremov E. A., Rodionov M. A., Zhivulko A. R., Popov D. M., Monakov D. M., Faniev M. V.

https://doi.org/10.17650/2070-9781-2023-24-2-49-57

Abstract

Surgical treatment of clinically significant varicocele in infertile men with pathospermia is a common practice. However, the question of the role of this disease in the pathogenesis of such conditions as hypogonadism and orchalgia, as well as the role of varicocelectomy in eliminating pain symptoms in the scrotum and increasing testosterone levels, has remained ambiguous for a long time. The expediency of surgical treatment of varicocele in patients with azoospermia also remains a subject of discussion.

References

1. Jensen C.F.S., Østergren P., Dupree J.M. et al. Varicocele and male infertility. Nat Rev Urol 2017;14(9):523–33. DOI: 10.1038/nrurol.2017.98

2. Peterson A.C., Lance R.S., Ruiz H.E. Outcomes of varicocele ligation done for pain. J Urol 1998;159(5):1565–7. DOI: 10.1097/00005392-199805000-00043

3. Shridharani A., Lockwood G., Sandlow J. Varicocelectomy in the treatment of testicular pain: a review. Curr Opin Urol 2012;22(6):499–506. DOI: 10.1097/MOU.0b013e328358f69f

4. Kotov S.V., Korochkin N.D., Klimenko A.A. Retsidivnoe varikotsele. Vestnik urologii 2021;9(2):132–41. DOI: 10.21886/2308-6424-2021-9-2-132-141

5. Zhukov O.B., Kapto A.A., Mikhailenko D.S., Evdokimov V.V. Varikoznaya bolezn' organov taza muzhchiny. Andrologiya i genital'naya khirurgiya 2016;17(4):72–7. DOI: 10.17650/2070-9781-2016-17-4-72-77

6. Yaman O., Ozdiler E., Anafarta K., Göğüş O. Effect of microsurgical subinguinal varicocele ligation to treat pain. Urology 2000;55(1):107–8. DOI: 10.1016/S0090-4295(99)00374-X

7. Schlegel P.N., Goldstein M. Alternate indications for varicocele repair: non-obstructive azoospermia, pain, androgen deficiency and progressive testicular dysfunction. Fertil Steril 2011;96(6):1288–93. DOI: 10.1016/j.fertnstert.2011.10.033

8. Muthuveloe D.W., During V., Ashdown D. et al. The effectiveness of varicocele embolisation for the treatment of varicocele related orchalgia. Springer Plus 2015;4(1):392. DOI: 10.1186/s40064-015-1177-2

9. Elzanaty S., Johansen C.E. Microsurgical varicocele repair on men with grade III lesions and chronic dull scrotal pain: a pilot study. Curr Urol 2015;8(1):29–31. DOI: 10.1159/000365685

10. Han D.Y., Yang Q.Y., Chen X. et al. Who will benefit from surgical repair for painful varicocele: a meta-analysis. Int Urol Nephrol 2016;48(7):1071–8. DOI: 10.1007/s11255-016-1246-7

11. Karademir K., Senkul T., Baykal K. et al. Evaluation of the role of varicocelectomy including external spermatic vein ligation in patients with scrotal pain. Int J Urol 2005;12(5):484–8. DOI: 10.1111/j.1442-2042.2005.01063.x

12. Maghraby H.A. Laparoscopic varicocelectomy for painful varicoceles: merits and outcomes. J Endourol 2002;16(2):107–10. DOI: 10.1089/089277902753619627

13. Parekattil S.J., Brahmbhatt J.V. Robotic approaches for male infertility and chronic orchialgia microsurgery. Curr Opin Urol 2011;21(6):493–9. DOI: 10.1097/MOU.0b013e32834bb783

14. Chawla A., Kulkarni G., Kamal K., Zini A. Microsurgical varicocelectomy for recurrent or persistent varicoceles associated with orchalgia. Urology 2005;66(5):1072–4. DOI: 10.1016/j.urology.2005.05.052

15. Reşorlu B., Kara C., Sahin E., Unsal A. et al. The significance of age on success of surgery for patients with varicocele. Int Urol Nephrol 2010;42(2):351–6. DOI: 10.1007/s11255-009-9589-y

16. Park H.J., Lee S.S., Park N.C. Predictors of pain resolution after varicocelectomy for painful varicocele. Asian J Androl 2011;13(5):754–8. DOI: 10.1038/aja.2010.87

17. Kim S.O., Jung H., Park K. Outcomes of microsurgical subinguinal varicocelectomy for painful varicoceles. J Androl 2012;33(5):872–5. DOI: 10.2164/jandrol.111.014993

18. Chen L.K., Chen S.S. Risk factors for developing pain in normospermic patients with varicocoele. Int J Androl 2012;35:176–80. DOI: 10.1111/j.1365-2605.2011.01215.x

19. Handel L.N., Shetty R., Sigman M. The relationship between varicoceles and obesity. J Urol 2006;176(5):2138–40; discussion 2140. DOI: 10.1016/j.juro.2006.07.023

20. Soylemez H., Atar M., Ali Sancaktutar A. et al. Varicocele among healthy young men in Turkey; prevalence and relationship with body mass index. Int Braz J Urol 2012;38(1):116–21. DOI: 10.1590/S1677-55382012000100016

21. Bungum M., Humaidan P., Axmon A. et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod 2007;22(1):174–9. DOI: 10.1093/humrep/del326

22. Collins J.A., Barnhart K.T., Schlegel P.N. Do sperm DNA integrity tests predict pregnancy with in vitro fertilization? Fertil Steril 2008;89(4):823–31. DOI: 10.1016/j.fertnstert.2007.04.055

23. Giwercman A., Lindstedt L., Larsson M. et al. Sperm chromatin structure assay as an independent predictor of fertility in vivo: a case-control study. Int J Androl 2010;33(1):e221–7. DOI: 10.1111/j.1365-2605.2009.00995.x

24. Henkel R., Hajimohammad M., Stalf T. et al. Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril 2004;81(4):965–72. DOI: 10.1016/j.fertnstert.2003.09.044

25. Virro M.R., Larson-Cook K.L., Evenson D.P. Sperm chromatin structure assay (SCSA) parameters are related to fertilization, blastocyst development, and ongoing pregnancy in in vitro fertilization and intracytoplasmic sperm injection cycles. Fertil Steril 2004;81(5):1289–95. DOI: 10.1016/j.fertnstert.2003.09.063

26. Lopes S., Sun J.G., Jurisicova A. et al. Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril 1998;69(3):528–32. DOI: 10.1016/S0015-0282(97)00536-0

27. De Iuliis G.N., Thomson L.K., Mitchell L.A. et al. DNA damage in human spermatozoa is highly correlated with the efficiency of chromatin remodeling and the formation of 8-hydroxy-2’- deoxyguanosine, a marker of oxidative stress. Biol Reprod 2009;81(3):517–24. DOI: 10.1095/biolreprod.109.076836

28. Sakkas D., Seli E., Bizzaro D. et al. Abnormal spermatozoa in the ejaculate: abortive apoptosis and faulty nuclear remodelling during spermatogenesis. Reprod Biomed Online 2003;7(4):428–32. DOI: 10.1016/S1472-6483(10)61886-X

29. Tremellen K. Oxidative stress and male infertility – a clinical perspective. Hum Reprod Update 2008;14(3):243–58. DOI: 10.1093/humupd/dmn004

30. Sun J.G., Jurisicova A., Casper R.F. Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 1997;56(3):602–7. DOI: 10.1095/biolreprod56.3.602

31. Allamaneni S.S., Naughton C.K., Sharma R.K. et al. Increased seminal reactive oxygen species levels in patients with varicoceles correlate with varicocele grade but not with testis size. Fertil Steril 2004;82(6):1684–6. DOI: 10.1016/j.fertnstert.2004.04.071

32. Mancini A., Meucci E., Milardi D. et al. Seminal antioxidant capacity in pre- and postoperative varicocele. J Androl 2004;25(1):44–9. DOI: 10.1002/j.1939-4640.2004.tb02757.x

33. Saleh R.A., Agarwal A., Sharma R.K. et al. Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertil Steril 2003;80(6):1431–6. DOI: 10.1016/S0015-0282(03)02211-8

34. Schoor R.A., Elhanbly S.M., Niederberger C. The pathophysiology of varicocele-associated male infertility. Curr Urol Rep 2001;2(6):432–6. DOI: 10.1007/s11934-001-0035-7

35. Naughton C.K., Nangia A.K., Agarwal A. Pathophysiology of varicoceles in male infertility. Hum Reprod Update 2001;7(5):473–81. DOI: 10.1093/humupd/7.5.473

36. Nallella K.P., Allamaneni S.S., Pasqualotto F.F. et al. Relationship of interleukin-6 with semen characteristics and oxidative stress in patients with varicocele. Urology 2004;64(5):1010–3. DOI: 10.1016/j.urology.2004.05.045

37. Gamidov S.I., Ovchinnikov R.I., Popova A.Yu. i dr. Ad\"yuvantnaya antioksidantnaya terapiya u bol'nykh besplodiem pri varikotsele. Urologiya 2017;2(suppl):64–72. DOI: 10.18565/urol.2017.2-supplement.64-72

38. Köksal I.T., Tefekli A., Usta M. et al. The role of reactive oxygen species in testicular dysfunction associated with varicocele. BJU Int 2000;86(4):549–52. DOI: 10.1046/j.1464-410X.2000.00755.x

39. Blumer C.G., Restelli A.E., Giudice P.T. et al. Effect of varicocele on sperm function and semen oxidative stress. BJU Int 2012;109(2):259–65. DOI: 10.1111/j.1464-410X.2011.10240.x

40. Romeo C., Ientile R., Santoro G. et al. Nitric oxide production is increased in the spermatic veins of adolescents with left idiophatic varicocele. J Pediatr Surg 2001;36(2):389–93. DOI: 10.1053/jpsu.2001.20724

41. Pasqualotto F.F., Sundaram A., Sharma R.K. et al. Semen quality and oxidative stress scores in fertile and infertile patients with varicocele. Fertil Steril 2008;89(3):602–7. DOI: 10.1016/j.fertnstert.2007.03.057

42. Mostafa T., Anis T.H., El-Nashar A. et al. Varicocelectomy reduces reactive oxygen species levels and increases antioxidant activity of seminal plasma from infertile men with varicocele. Int J Androl 2001;24(5):261–5. DOI: 10.1046/j.1365-2605.2001.00296.x

43. Cervellione R.M., Cervato G., Zampieri N. et al. Effect of varicocelectomy on the plasma oxidative stress parameters. J Pediatr Surg 2006;41(2):403–6. DOI: 10.1016/j.jpedsurg.2005.11.018

44. Hurtado de Catalfo G.E., Ranieri-Casilla A., Marra F.A. et al. Oxidative stress biomarkers and hormonal profile in human patients undergoing varicocelectomy. Int J Androl 2007;30(6):519–30. DOI: 10.1111/j.1365-2605.2007.00753.x

45. Chen S.S., Huang W.J., Chang L.S., Wei Y.H. Attenuation of oxidative stress after varicocelectomy in subfertile patients with varicocele. J Urol 2008;179(2):639–42. DOI: 10.1016/j.juro.2007.09.039

46. Sakamoto Y., Ishikawa T., Kondo Y. et al. The assessment of oxidative stress in infertile patients with varicocele. BJU Int 2008;101(12):1547–52. DOI: 10.1111/j.1464-410X.2008.07517.x

47. Dada R., Shamsi M.B., Venkatesh S. et al. Attenuation of oxidative stress & DNA damage in varicocelectomy: implications in infertility management. Indian J Med Res 2010;132(6):728–30.

48. Rodriguez Peña M, Alescio L, Russell A, et al. Predictors of improved seminal parameters and fertility after varicocele repair in young adults. Andrologia 2009;41(5):277–81. DOI: 10.1111/j.1439-0272.2009.00919.x

49. Lacerda J.I., Del Giudice P.T., da Silva B.F. et al. Adolescent varicocele: improved sperm function after varicocelectomy. Fertil Steril 2011;95(3):994–9. DOI: 10.1016/j.fertnstert.2010.10.031

50. Smith R., Kaune H., Parodi D. et al. Increased sperm DNA damage in patients with varicocele: relationship with seminal oxidative stress. Hum Reprod 2006;21(4):986–93. DOI: 10.1093/humrep/dei429

51. Blumer C.G., Fariello R.M., Restelli A.E. et al. Sperm nuclear DNA fragmentation and mitochondrial activity in men with varicocele. Fertil Steril 2008;90(5):171–22. DOI: 10.1016/j.fertnstert.2007.09.007

52. Chen C.H., Lee S.S., Chen D.C. et al. Apoptosis and kinematics of ejaculated spermatozoa in patients with varicocele. J Androl 2004;25(3):348–53. DOI: 10.1002/j.1939-4640.2004.tb02799.x

53. Bertolla R.P., Cedenho A.P., Hassun Filho P.A. et al. Sperm nuclear DNA fragmentation in adolescents with varicocele. Fertil Steril 2006;85(3):625–8. DOI: 10.1016/j.fertnstert.2005.08.032

54. Zini A, Dohle G. Are varicoceles associated with increased deoxyribonucleic acid fragmentation? Fertil Steril 2011;96(6):1283–7. DOI: 10.1016/j.fertnstert.2011.10.016

55. Zini A., Azhar R., Baazeem A., Gabriel M.S. Effect of microsurgical varicocelectomy on human sperm chromatin and DNA integrity: a prospective trial. Int J Androl 2011;34(1):14–9. DOI: 10.1111/j.1365-2605.2009.01048.x

56. Werthman P., Wixon R., Kasperson K., Evenson D.P. Significant decrease in sperm deoxyribonucleic acid fragmentation after varicocelectomy. Fertil Steril 2008;90(5):1800–4. DOI: 10.1016/j.fertnstert.2006.09.019

57. Marmar J.L., Agarwal A., Prabakaran S. et al. Reassessing the value of varicocelectomy as a treatment for male subfertility with a new meta-analysis. Fertil Steril 2007;88(3):639–48. DOI: 10.1016/j.fertnstert.2006.12.008

58. Smit M., Romijn J.C., Wildhagen M.F. et al. Decreased sperm DNA fragmentation after surgical varicocelectomy is associated with increased pregnancy rate. J Urol 2010;183(1):270–4. DOI: 10.1016/j.juro.2009.08.161

59. Baker K., McGill J., Sharma R. et al. Pregnancy after varicocelectomy: impact of postoperative motility and DFI. Urology 2013;81(4):760–6. DOI: 10.1016/j.urology.2012.12.005

60. Leung L., Ho K.L., Tam P.C., Yiu M.K. Subinguinal microsurgical varicocelectomy for male factor subfertility: ten-year experience. Hong Kong Med J 2013;19(4):334–40. DOI: 10.12809/hkmj133884

61. Practice Committee of American Society for Reproductive Medicine. Report on varicocele and infertility. Fertil Steril 2008;90(5 Suppl):S247–9. DOI: 10.1016/j.fertnstert.2008.08.050

62. Agarwal A., Deepinder F., Cocuzza M. et al. Efficacy of varicocelectomy in improving semen parameters: new metaanalytical approach. Urology 2007;70(3):532–8. DOI: 10.1016/j.urology.2007.04.011

63. French D.B., Desai N.R., Agarwal A. Varicocele repair: does it still have a role in infertility treatment? Curr Opin Obstet Gynecol 2008;20(3):269–74. DOI: 10.1097/GCO.0b013e3282fcc00c

64. Acar H., Kilinc M., Guven S. et al. Comparison of semen profile and frequency of chromosome aneuploidies in sperm nuclei of patients with varicocele before and after varicocelectomy. Andrologia 2009;41(3):157–62. DOI: 10.1111/j.1439-0272.2008.00907.x

65. Mansour Ghanaie M., Asgari S.A., Dadrass N. et al. Effects of varicocele repair on spontaneous first trimester miscarriage: a randomized clinical trial. Urol J 2012;9(2):505–13.

66. Nasr-Esfahani M.H., Abasi H., Razavi S. et al. Varicocelectomy: semen parameters and protamine deficiency. Int J Androl 2009;32(2):115–22. DOI: 10.1111/j.1365-2605.2007.00822.x

67. Pirke K.M., Vogt H.J., Sintermann R., Spyra B. Testosterone in peripheral plasma, spermatic vein and in testicular tissue under basal conditions and after HCG-stimulation in patients with varicocele. Andrologia 1983;15(6):637–41. DOI: 10.1111/j.1439-0272.1983.tb00179.x

68. Abdel-Meguid T.A., Farsi H.M., Al-Sayyad A. et al. Effects of varicocele on serum testosterone and changes of testosterone after varicocelectomy: a prospective controlled study. Urology 2014;84(5):1081–7. DOI: 10.1016/j.urology.2014.05.029

69. Tanrikut C., Goldstein M., Rosoff J.S. et al. Varicocele as a risk factor for androgen deficiency and effect of repair. BJU Int 2011;108(9):1480–4. DOI: 10.1111/j.1464-410X.2010.10030.x

70. Goldstein M., Eid J.F. Elevation of intratesticular and scrotal skin surface temperature in men with varicocele. J Urol 1989;142(3):743–5. DOI: 10.1016/S0022-5347(17)38874-2

71. Li F., Yue H., Yamaguchi K. et al. Effect of surgical repair on testosterone production in infertile men with varicocele: a metaanalysis. Int J Urol 2012;19(2):149–54. DOI: 10.1111/j.1442-2042.2011.02890.x

72. Hsiao W., Rosoff J.S., Pale J.R. et al. Older age is associated with similar improvements in semen parameters and testosterone after subinguinal microsurgical varicocelectomy. J Urol 2011;185(2):620–5. DOI: 10.1016/j.juro.2010.09.114

73. Zohdy W., Ghazi S., Arafa M. Impact of varicocelectomy on gonadal and erectile functions in men with hypogonadism and infertility. J Sex Med 2011;8(3):885–93. DOI: 10.1111/j.1743-6109.2010.01974.x

74. Sathya Srini V., Belur Veerachari S. Does varicocelectomy improve gonadal function in men with hypogonadism and infertility? Analysis of a prospective study. Int J Endocrinol 2011;2011:916380. DOI: 10.1155/2011/916380

75. Hsiao W., Rosoff J.S., Pale J.R. et al. Varicocelectomy is associated with increases in serum testosterone independent of clinical grade. Urology 2013;81(6):1213–7. DOI: 10.1016/j.urology.2013.01.060

76. Esteves S.C. Clinical management of infertile men with nonobstructive azoospermia. Asian J Androl 2015;17(3):459–70. DOI: 10.4103/1008-682X.148719

77. Popova A.Yu., Gamidov S.I., Ovchinnikov R.I. i dr. Varikotsele i neobstruktivnaya azoospermiya – s chego nachat'? Andrologiya i genital'naya khirurgiya 2017;18(4):77–80. DOI: 10.17650/2070-9781-2017-18-4-77-80

78. Gat Y., Bachar G.N., Everaert K. et al. Induction of spermatogenesis in azoospermic men after internal spermatic vein embolization for the treatment of varicocele. Hum Reprod 2005;20(4):1013–7. DOI: 10.1093/humrep/deh706

79. Esteves S.C., Miyaoka R., Agarwal A. Sperm retrieval techniques for assisted reproduction. Int Braz J Urol 2011;37(5):570–83. DOI: 10.1590/S1677-55382011000500002

80. Matthews G.J., Matthews E.D., Goldstein M. Induction of spermatogenesis and achievement of pregnancy after microsurgical varicocelectomy in men with azoospermia and severe oligoasthenospermia. Fertil Steril 1998;70(1):71–5. DOI: 10.1016/S0015-0282(98)00108-3

81. Poulakis V., Ferakis N., de Vries R. et al. Induction of spermatogenesis in men with azoospermia or severe oligoteratoasthenospermia after antegrade internal spermatic vein sclerotherapy for the treatment of varicocele. Asian J Androl 2006;8(5):613–9. DOI: 10.1111/j.1745-7262.2006.00157.x

82. Abdel-Meguid T.A., Al-Sayyad A., Tayib A., Farsi H.M. Does varicocele repair improve male infertility? An evidence-based perspective from a randomized, controlled trial. Eur Urol 2011;59(3):455–61. DOI: 10.1016/j.eururo.2010.12.008

83. Kiraç M., Deniz N., Biri H. The effect of microsurgical varicocelectomy on semen parameters in men with non-obstructive azoospermia. Curr Urol 2013;6(3):136–40. DOI: 10.1159/000343527

84. Schlegel P.N., Kaufmann J. Role of varicocelectomy in men with nonobstructive azoospermia. Fertil Steril 2004;81(6):1585–8. DOI: 10.1016/j.fertnstert.2003.10.036

85. Tung M.C., Huang W.J., Chen K.K. Modified subinguinal varicocelectomy for painful varicocele and varicocele-associated infertility. J Chin Med Assoc 2004;67(6):296–300.

86. Pasqualotto F.F., Sobreiro B.P., Hallak J. et al. Induction of spermatogenesis in azoospermic men after varicocelectomy repair: an update. Fertil Steril 2006;85(3):635–9. DOI: 10.1016/j.fertnstert.2005.08.043

87. Esteves S.C., Glina S. Recovery of spermatogenesis after microsurgical subinguinal varicocele repair in azoospermic men based on testicular histology. Int Braz J Urol 2005;31(6):541–8. DOI: 10.1590/S1677-55382005000600005

88. Esteves S.C., Miyaoka R., Roque M., Agarwal A. Outcome of varicocele repair in men with nonobstructive azoospermia: systematic review and meta-analysis. Asian J Androl 2016;18(2):246–53. DOI: 10.4103/1008-682X.169562

89. Ustuner M., Yilmaz H., Yavuz U. et al. Varicocele repair improves testicular histology in men with nonobstructive azoospermia. Biomed Res Int 2015;2015:709452. DOI: 10.1155/2015/709452

90. Yamamoto M., Hibi H., Hirata Y. et al. Effect of varicocelectomy on sperm parameters and pregnancy rate in patients with subclinical varicocele: a randomized prospective controlled study. J Urol 1996;155(5):1636–8.

91. Kroese A.C., de Lange N.M., Collins J., Evers J.L. Surgery or embolization for varicoceles in subfertile men. Cochrane Database Syst Rev 2012;10:CD000479. DOI: 10.1002/14651858.CD000479.pub5

92. Kim K.H., Lee J.Y., Kang D.H. et al. 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 2013;54(10):703–9. DOI: 10.4111/kju.2013.54.10.703

93. Kirby E.W., Wiener L.E., Rajanahally S. et al. Undergoing varicocele repair before assisted reproduction improves pregnancy rate and live birth rate in azoospermic and oligospermic men with a varicocele: a systematic review and meta-analysis. Fertil Steril 2016;106(6):1338–43. DOI: 10.1016/j.fertnstert.2016.07.1093