Varicocele management in the era of in vitro fertilization/intracytoplasmic sperm injection

Asian Journal of Andrology

Volumn 18, Issue 3, 2016, Pages 343-348

  Pathak, Piyush ^a   Chandrashekar, Aravind ^b   Hakky, Tariq S ^c   Pastuszak, Alexander W ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b KAISER PERMANENTE   (United States)

^c Advanced Urology   (United States)

Author keywords

hypogonadism; Leydig cell; male fertility; Sertoli cell; varicocele

Indexed keywords

REACTIVE OXYGEN METABOLITE;

AZOOSPERMIA; COST EFFECTIVENESS ANALYSIS; DNA DAMAGE; FERTILIZATION IN VITRO; HUMAN; INFERTILITY THERAPY; INTRACYTOPLASMIC SPERM INJECTION; MALE INFERTILITY; PREGNANCY; REVIEW; SPERM; VARICOCELE; VARICOCELECTOMY; COMPLICATION; DISEASE MANAGEMENT; IN VITRO FERTILIZATION; INFERTILITY, MALE; MALE; SPERMATOZOON COUNT; SPERMATOZOON MOTILITY;

DISEASE MANAGEMENT; FERTILIZATION IN VITRO; HUMANS; INFERTILITY, MALE; MALE; SPERM COUNT; SPERM INJECTIONS, INTRACYTOPLASMIC; SPERM MOTILITY; VARICOCELE;

EID: 84969752741     PISSN: 1008682X     EISSN: 17457262     Source Type: Journal    
DOI: 10.4103/1008-682X.178482     Document Type: Review

References (100)

1. Pastuszak AW, Wang R. Varicocele and testicular function. Asian J Androl 2015; 17: 659-67.
2. Sheehan MM, Ramasamy R, Lamb DJ. Molecular mechanisms involved in varicocele-Associated infertility. J Assist Reprod Genet 2014; 31: 521-6.
3. Eisenberg ML, Lipshultz LI. Varicocele-induced infertility: newer insights into its pathophysiology. Indian J Urol 2011; 27: 58-64.
4. Naughton CK, Nangia AK, Agarwal A. Pathophysiology of varicoceles in male infertility. Hum Reprod Update 2001; 7: 473-81.
5. Goldstein M, Eid JF. Elevation of intratesticular and scrotal skin surface temperature in men with varicocele. J Urol 1989; 142: 743-5.
6. Ozbek E, Yurekli M, Soylu A, Davarci M, Balbay MD. The role of adrenomedullin in varicocele and impotence. BJU Int 2000; 86: 694-8.
7. Hendin BN, Kolettis PN, Sharma RK, Thomas AJ, Agarwal A. Varicocele is associated with elevated spermatozoal reactive oxygen species production and diminished seminal plasma antioxidant capacity. J Urol 1999; 161: 1831-4.
8. Gilbert BR, Witkin SS, Goldstein M. Correlation of sperm-bound immunoglobulins with impaired semen analysis in infertile men with varicoceles. Fertil Steril 1989; 52: 469-73.
9. Fujisawa M, Yoshida S, Matsumoto O, Kojima K, Kamidono S. Deoxyribonucleic acid polymerase activity in the testes of infertile men with varicocele. Fertil Steril 1988; 50: 795-800.
10. Mieusset R, Bujan L. Testicular heating and its possible contributions to male infertility: a review. Int J Androl 1995; 18: 169-84.
11. Simşek F, Türkeri L, Cevik I, Bircan K, Akdaş A. Role of apoptosis in testicular tissue damage caused by varicocele. Arch Esp Urol 1998; 51: 947-50.
12. Tulloch WS. Varicocele in subfertility; results of treatment. Br Med J 1955; 2: 356-8.
13. Evers JL, Collins JA, Vandekerckhove P. Surgery or embolisation for varicocele in subfertile men. Cochrane Database Syst Rev 2001; 1: CD000479.
14. Abdel-Meguid TA, Al-Sayyad A, Tayib A, Farsi HM. Does varicocele repair improve male infertility?. An evidence-based perspective from a randomized, controlled trial. Eur Urol 2011; 59: 455-61.
15. Kroese AC, de Lange NM, Collins J, Evers JL. Surgery or embolization for varicoceles in subfertile men. Cochrane Database Syst Rev 2012; 10: CD000479.
16. Baazeem A, Belzile E, Ciampi A, Dohle G, Jarvi K, et al. Varicocele and male factor infertility treatment: a new meta-Analysis and review of the role of varicocele repair. Eur Urol 2011; 60: 796-808.
17. Boulet SL, Mehta A, Kissin DM, Warner L, Kawwass JF, et al. Trends in use of and reproductive outcomes associated with intracytoplasmic sperm injection. JAMA 2015; 313: 255-63.
18. Bonduelle M, Van Assche E, Joris H, Keymolen K, Devroey P, et al. Prenatal testing in ICSI pregnancies: incidence of chromosomal anomalies in 1586 karyotypes and relation to sperm parameters. Hum Reprod 2002; 17: 2600-14.
19. Gjerris AC, Loft A, Pinborg A, Christiansen M, Tabor A. Prenatal testing among women pregnant after assisted reproductive techniques in Denmark 1995-2000: a national cohort study. Hum Reprod 2008; 23: 1545-52.
20. Amor DJ, Halliday J. A review of known imprinting syndromes and their association with assisted reproduction technologies. Hum Reprod 2008; 23: 2826-34.
21. Sandin S, Nygren KG, Iliadou A, Hultman CM, Reichenberg A. Autism and mental retardation among offspring born after in vitro fertilization. JAMA 2013; 310: 75-84.
22. Davies MJ, Moore VM, Willson KJ, Van Essen P, Priest K, et al. Reproductive technologies and the risk of birth defects. N Engl J Med 2012; 366: 1803-13.
23. Zhu JL, Basso O, Obel C, Bille C, Olsen J. Infertility, infertility treatment, and congenital malformations: Danish national birth cohort. BMJ 2006; 333: 679.
24. Kolettis PN, Sabanegh ES. Significant medical pathology discovered during a male infertility evaluation. J Urol 2001; 166: 178-80.
25. Walsh TJ, Croughan MS, Schembri M, Chan JM, Turek PJ. Increased risk of testicular germ cell cancer among infertile men. Arch Intern Med 2009; 169: 351-6.
26. Walsh TJ, Schembri M, Turek PJ, Chan JM, Carroll PR, et al. Increased risk of high-grade prostate cancer among infertile men. Cancer 2010; 116: 2140-7.
27. Eisenberg ML, Li S, Brooks JD, Cullen MR, Baker LC. Increased risk of cancer in infertile men: analysis of U.S. claims data. J Urol 2015; 193: 1596-601.
28. Eisenberg ML, Li S, Behr B, Pera RR, Cullen MR. Relationship between semen production and medical comorbidity. Fertil Steril 2015; 103: 66-71.
29. Lipshultz LI, Corriere JN. Progressive testicular atrophy in the varicocele patient. J Urol 1977; 117: 175-6.
30. Witt MA, Lipshultz LI. Varicocele: a progressive or static lesion?. Urology 1993; 42: 541-3.
31. Gorelick JI, Goldstein M. Loss of fertility in men with varicocele. Fertil Steril 1993; 59: 613-6.
32. Diamond DA, Zurakowski D, Atala A, Bauer SB, Borer JG, et al. Is adolescent varicocele a progressive disease process?. J Urol 2004; 172: 1746-8.
33. Chen SS, Chen LK. Risk factors for progressive deterioration of semen quality in patients with varicocele. Urology 2012; 79: 128-32.
34. Kim ED, Leibman BB, Grinblat DM, Lipshultz LI. Varicocele repair improves semen parameters in azoospermic men with spermatogenic failure. J Urol 1999; 162: 737-40.
35. MacLeod J. Seminal cytology in the presence of varicocele. Fertil Steril 1965; 16: 735-57.
36. Ayodeji O, Baker HW. Is there a specific abnormality of sperm morphology in men with varicoceles?. Fertil Steril 1986; 45: 839-42.
37. Zümrütbaş AE, Gülpinar Ö, Mermerkaya M, Süer E, Yaman Ö. The effect of varicocele on sperm morphology and DNA maturity: does acridine orange staining facilitate diagnosis?. Turk J Urol 2013; 39: 165-9.
38. Vigil P, Wöhler C, Bustos-Obregón E, Comhaire F, Morales P. Assessment of sperm function in fertile and infertile men. Andrologia 1994; 26: 55-60.
39. Blumer CG, Fariello RM, Restelli AE, Spaine DM, Bertolla RP, et al. Sperm nuclear DNA fragmentation and mitochondrial activity in men with varicocele. Fertil Steril 2008; 90: 1716-22.
40. Vazquez-Levin MH, Friedmann P, Goldberg SI, Medley NE, Nagler HM. Response of routine semen analysis and critical assessment of sperm morphology by Kruger classification to therapeutic varicocelectomy. J Urol 1997; 158: 1804-7.
41. Schatte EC, Hirshberg SJ, Fallick ML, Lipschultz LI, Kim ED. Varicocelectomy improves sperm strict morphology and motility. J Urol 1998; 160: 1338-40.
42. Cho C, Esteves SC, Agarwal A. Novel insights into the pathophysiology of varicocele and its association with reactive oxygen species and sperm DNA fragmentation. Asian J Androl 2016; 18: 186-93.
43. Tremellen K. Oxidative stress and male infertility - A clinical perspective. Hum Reprod Update 2008; 14: 243-58.
44. Agarwal A, Said TM, Bedaiwy MA, Banerjee J, Alvarez JG. Oxidative stress in an assisted reproductive techniques setting. Fertil Steril 2006; 86: 503-12.
45. Lysiak JJ, Turner SD, Nguyen QA, Singbartl K, Ley K, et al. Essential role of neutrophils in germ cell-specific apoptosis following ischemia/reperfusion injury of the mouse testis. Biol Reprod 2001; 65: 718-25.
46. Ahotupa M, Huhtaniemi I. Impaired detoxification of reactive oxygen and consequent oxidative stress in experimentally cryptorchid rat testis. Biol Reprod 1992; 46: 1114-8.
47. Reddy MM, Mahipal SV, Subhashini J, Reddy MC, Roy KR, et al. Bacterial lipopolysaccharide-induced oxidative stress in the impairment of steroidogenesis and spermatogenesis in rats. Reprod Toxicol 2006; 22: 493-500.
48. de Lamirande E, Gagnon C. Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Hum Reprod 1995; 10 Suppl 1: 15-21.
49. de Lamirande E, Jiang H, Zini A, Kodama H, Gagnon C. Reactive oxygen species and sperm physiology. Rev Reprod 1997; 2: 48-54.
50. Aitken RJ, Clarkson JS, Fishel S. Generation of reactive oxygen species, lipid peroxidation, and human sperm function. Biol Reprod 1989; 41: 183-97.
51. Ochsendorf FR. Infections in the male genital tract and reactive oxygen species. Hum Reprod Update 1999; 5: 399-420.
52. Gil-Guzman E, Ollero M, Lopez MC, Sharma RK, Alvarez JG, et al. Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Hum Reprod 2001; 16: 1922-30.
53. Moustafa MH, Sharma RK, Thornton J, Mascha E, Abdel-Hafez MA, et al. Relationship between ROS production, apoptosis and DNA denaturation in spermatozoa from patients examined for infertility. Hum Reprod 2004; 19: 129-38.
54. Zini A, Dohle G. Are varicoceles associated with increased deoxyribonucleic acid fragmentation?. Fertil Steril 2011; 96: 1283-7.
55. Griveau JF, Dumont E, Renard P, Callegari JP, Le Lannou D. Reactive oxygen species, lipid peroxidation and enzymatic defence systems in human spermatozoa. J Reprod Fertil 1995; 103: 17-26.
56. Aitken RJ, Koppers AJ. Apoptosis and DNA damage in human spermatozoa. Asian J Androl 2011; 13: 36-42.
57. Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 2003; 79: 829-43.
58. de Lamirande E, Gagnon C. Reactive oxygen species and human spermatozoa. II. Depletion of adenosine triphosphate plays an important role in the inhibition of sperm motility. J Androl 1992; 13: 379-86.
59. Agarwal A, Hamada A, Esteves SC. Insight into oxidative stress in varicocele-Associated male infertility: part 1. Nat Rev Urol 2012; 9: 678-90.
60. Aitken RJ, Krausz C. Oxidative stress, DNA damage and the Y chromosome. Reproduction 2001; 122: 497-506.
61. Vydra G. Multinuclear spermatides observed in varicocele. Morphol Igazsagugyi Orv Sz 1978; 18: 161-5.
62. Cameron DF, Snydle FE, Ross MH, Drylie DM. Ultrastructural alterations in the adluminal testicular compartment in men with varicocele. Fertil Steril 1980; 33: 526-33.
63. Zini A, Defreitas G, Freeman M, Hechter S, Jarvi K. Varicocele is associated with abnormal retention of cytoplasmic droplets by human spermatozoa. Fertil Steril 2000; 74: 461-4.
64. Gomez E, Buckingham DW, Brindle J, Lanzafame F, Irvine DS, et al. Development of an image analysis system to monitor the retention of residual cytoplasm by human spermatozoa: correlation with biochemical markers of the cytoplasmic space, oxidative stress, and sperm function. J Androl 1996; 17: 276-87.
65. Keating J, Grundy CE, Fivey PS, Elliott M, Robinson J. Investigation of the association between the presence of cytoplasmic residues on the human sperm midpiece and defective sperm function. J Reprod Fertil 1997; 110: 71-7.
66. Fischer MA, Willis J, Zini A. Human sperm DNA integrity: correlation with sperm cytoplasmic droplets. Urology 2003; 61: 207-11.
67. Schlesinger MH, Wilets IF, Nagler HM. Treatment outcome after varicocelectomy. A critical analysis. Urol Clin North Am 1994; 21: 517-29.
68. Parikh FR, Kamat SA, Kodwaney GG, Balaiah D. Computer-Assisted semen analysis parameters in men with varicocele: is surgery helpful?. Fertil Steril 1996; 66: 440-5.
69. Chen SS, Huang WJ, Chang LS, Wei YH. Attenuation of oxidative stress after varicocelectomy in subfertile patients with varicocele. J Urol 2008; 179: 639-42.
70. Zini A, Azhar R, Baazeem A, Gabriel MS. Effect of microsurgical varicocelectomy on human sperm chromatin and DNA integrity: a prospective trial. Int J Androl 2011; 34: 14-9.
71. Smit M, Romijn JC, Wildhagen MF, Veldhoven JL, Weber RF, et al. Decreased sperm DNA fragmentation after surgical varicocelectomy is associated with increased pregnancy rate. J Urol 2013; 189: S146-50.
72. Li F, Yamaguchi K, Okada K, Matsushita K, Ando M, et al. Significant improvement of sperm DNA quality after microsurgical repair of varicocele. Syst Biol Reprod Med 2012; 58: 274-7.
73. Wang YJ, Zhang RQ, Lin YJ, Zhang RG, Zhang WL. Relationship between varicocele and sperm DNA damage and the effect of varicocele repair: a meta-Analysis. Reprod Biomed Online 2012; 25: 307-14.
74. Reichart M, Eltes F, Soffer Y, Zigenreich E, Yogev L, et al. Sperm ultramorphology as a pathophysiological indicator of spermatogenesis in males suffering from varicocele. Andrologia 2000; 32: 139-45.
75. Oliva A, Dotta A, Multigner L. Pentoxifylline and antioxidants improve sperm quality in male patients with varicocele. Fertil Steril 2009; 91: 1536-9.
76. Zini A, Al-Hathal N. Antioxidant therapy in male infertility: fact or fiction?. Asian J Androl 2011; 13: 374-81.
77. Kobori Y, Ota S, Sato R, Yagi H, Soh S, et al. Antioxidant cosupplementation therapy with Vitamin C, Vitamin E, and coenzyme Q10 in patients with oligoasthenozoospermia. Arch Ital Urol Androl 2014; 86: 1-4.
78. Showell MG, Mackenzie-Proctor R, Brown J, Yazdani A, Stankiewicz MT, et al. Antioxidants for male subfertility. Cochrane database Syst Rev 2014; 12: CD007411.
79. Agarwal A, Sekhon LH. The role of antioxidant therapy in the treatment of male infertility. Hum Fertil (Camb) 2010; 13: 217-25.
80. Daitch JA, Bedaiwy MA, Pasqualotto EB, Hendin BN, Hallak J, et al. Varicocelectomy improves intrauterine insemination success rates in men with varicocele. J Urol 2001; 165: 1510-3.
81. Cayan S, Erdemir F, Ozbey I, Turek PJ, Kadiolu A, et al. Can varicocelectomy significantly change the way couples use assisted reproductive technologies?. J Urol 2002; 167: 1749-52.
82. Esteves SC, Oliveira F, Bertolla RP. Clinical outcome of intracytoplasmic sperm injection in infertile men with treated and untreated clinical varicocele. J Urol 2010; 184: 1442-6.
83. Pasqualotto FF, Braga DP, Figueira RC, Setti AS, Iaconelli A, et al. Varicocelectomy does not impact pregnancy outcomes following intracytoplasmic sperm injection procedures. J Androl 2012; 33: 239-43.
84. Esteves SC, Roque M, Agarwal A. Outcome of assisted reproductive technology in men with treated and untreated varicocele: systematic review and meta-Analysis. Asian J Androl 2016; 18: 254-8.
85. Shiraishi K, Matsuyama H, Takihara H. Pathophysiology of varicocele in male infertility in the era of assisted reproductive technology of ART. Int J Urol 2012; 19: 538-50.
86. Zini A, Boman J, Baazeem A, Jarvi K, Libman J. Natural history of varicocele management in the era of intracytoplasmic sperm injection. Fertil Steril 2008; 90: 2251-6.
87. Weedin JW, Khera M, Lipshultz LI. Varicocele repair in patients with nonobstructive azoospermia: a meta-Analysis. J Urol 2010; 183: 2309-15.
88. Cocuzza M, Cocuzza MA, Bragais FM, Agarwal A. The role of varicocele repair in the new era of assisted reproductive technology. Clinics (Sao Paulo) 2008; 63: 395-404.
89. Schlegel PN, Kaufmann J. Role of varicocelectomy in men with nonobstructive azoospermia. Fertil Steril 2004; 81: 1585-8.
90. Inci K, Hascicek M, Kara O, Dikmen AV, Gürgan T, et al. Sperm retrieval and intracytoplasmic sperm injection in men with nonobstructive azoospermia, and treated and untreated varicocele. J Urol 2009; 182: 1500-5.
91. Haydardedeoglu B, Turunc T, Kilicdag EB, Gul U, Bagis T. The effect of prior varicocelectomy in patients with nonobstructive azoospermia on intracytoplasmic sperm injection outcomes: a retrospective pilot study. Urology 2010; 75: 83-6.
92. Pasqualotto FF, Sobreiro BP, Hallak J, Pasqualotto EB, Lucon AM. Induction of spermatogenesis in azoospermic men after varicocelectomy repair: an update. Fertil Steril 2006; 85: 635-9.
93. Gat Y, Bachar GN, Everaert K, Levinger U, Gornish M. Induction of spermatogenesis in azoospermic men after internal spermatic vein embolization for the treatment of varicocele. Hum Reprod 2005; 20: 1013-7.
94. Abdel-Meguid TA. Predictors of sperm recovery and azoospermia relapse in men with nonobstructive azoospermia after varicocele repair. J Urol 2012; 187: 222-6.
95. Ron-El R, Strassburger D, Friedler S, Komarovski D, Bern O, et al. Extended sperm preparation: an alternative to testicular sperm extraction in non-obstructive azoospermia. Hum Reprod 1997; 12: 1222-6.
96. Schlegel PN. Is assisted reproduction the optimal treatment for varicocele-Associated male infertility?. A cost-effectiveness analysis. Urology 1997; 49: 83-90.
97. Kim J. Surgical managements versus artificial reproductive technology in male infertility: cost effectiveness in Korea. Clin Exp Reprod Med 2013; 40: 30-5.
98. Meng MV, Greene KL, Turek PJ. Surgery or assisted reproduction?. A decision analysis of treatment costs in male infertility. J Urol 2005; 174: 1926-31.
99. Lee R, Li PS, Goldstein M, Schattman G, Schlegel PN. A decision analysis of treatments for nonobstructive azoospermia associated with varicocele. Fertil Steril 2009; 92: 188-96.
100. Penson DF, Paltiel DA, Krumholz HM, Palter S. The cost-effectiveness of treatment for varicocele related infertility. J Urol 2002; 168: 2490-4.