Reproductive outcomes of testicular versus ejaculated sperm for intracytoplasmic sperm injection among men with high levels of DNA fragmentation in semen: systematic review and meta-analysis

Fertility and Sterility

Volumn 108, Issue 3, 2017, Pages 456-467.e1

  Esteves, Sandro C ^a   Roque, Matheus ^b   Bradley, Cara K ^c   Garrido, Nicolás ^d  

^a ANDROFERT   (Brazil)

^b ORIGEN   (Brazil)

^c Genea   (Australia)

^d IVI Foundation   (Spain)

Author keywords

intracytoplasmic sperm injection; male infertility; Semen; sperm DNA fragmentation; testicular sperm

Indexed keywords

DNA;

ARTICLE; BIRTH RATE; CLINICAL OUTCOME; DNA FRAGMENTATION; EJACULATION; EMBRYO TRANSFER; FERTILIZATION; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; LIVE BIRTH; MALE; META ANALYSIS; OLIGOSPERMIA; OOCYTE; PREGNANCY RATE; PRIORITY JOURNAL; REPRODUCTION; SPERM; SPONTANEOUS ABORTION; SYSTEMATIC REVIEW; TESTIS; ADULT; COMPARATIVE STUDY; FEMALE; INFERTILITY; PREGNANCY; PREGNANCY OUTCOME; PROCEDURES; SECRETION (PROCESS); SPERM RETRIEVAL; STATISTICS AND NUMERICAL DATA; TREATMENT OUTCOME; YOUNG ADULT;

ADULT; DNA FRAGMENTATION; EJACULATION; FEMALE; HUMANS; INFERTILITY; MALE; PREGNANCY; PREGNANCY OUTCOME; SPERM INJECTIONS, INTRACYTOPLASMIC; SPERM RETRIEVAL; TESTIS; TREATMENT OUTCOME; YOUNG ADULT;

EID: 85028730162     PISSN: 00150282     EISSN: 15565653     Source Type: Journal    
DOI: 10.1016/j.fertnstert.2017.06.018     Document Type: Article

References (71)

1. Palermo, G., Joris, H., Derde, M.P., Camus, M., Devroey, P., van Steirteghem, A., Sperm characteristics and outcome of human assisted fertilization by subzonal insemination and intracytoplasmic sperm injection. Fertil Steril 59 (1993), 826–835.
2. Strassburger, D., Friedler, S., Raziel, A., Schachter, M., Kasterstein, E., Ron-el, R., Very low sperm count affects the result of intracytoplasmic sperm injection. J Assist Reprod Genet 17 (2000), 431–436.
3. Mitchell, V., Rives, N., Albert, M., Peers, M.C., Selva, J., Clavier, B., et al. Outcome of ICSI with ejaculated spermatozoa in a series of men with distinct ultrastructural flagellar abnormalities. Hum Reprod 21 (2006), 2065–2074.
4. Esteves, S.C., Agarwal, A., Reproductive outcomes, including neonatal data, following sperm injection in men with obstructive and nonobstructive azoospermia: case series and systematic review. Clinics (Sao Paulo) 68:Suppl 1 (2013), 141–150.
5. Esteves, S.C., Prudencio, C., Seol, B., Verza, S., Knoedler, C., Agarwal, A., Comparison of sperm retrieval and reproductive outcome in azoospermic men with testicular failure and obstructive azoospermia treated for infertility. Asian J Androl 16 (2014), 602–606.
6. Lewis, S.E., John Aitken, R., Conner, S.J., Iuliis, G.D., Evenson, D.P., Henkel, R., et al. The impact of sperm DNA damage in assisted conception and beyond: recent advances in diagnosis and treatment. Reprod Biomed Online 27 (2013), 325–337.
7. Gosálvez, J., Lopez-Fernandez, C., Fernandez, J.L., Esteves, S.C., Johnston, S.D., Unpacking the mysteries of sperm DNA fragmentation: ten frequently asked questions. J Reprod Biotechnol Fertil 4 (2015), 1–16.
8. Esteves, S.C., Gosálvez, J., López-Fernández, C., Núñez-Calonge, R., Caballero, P., Agarwal, A., et al. Diagnostic accuracy of sperm DNA degradation index (DDSi) as a potential noninvasive biomarker to identify men with varicocele-associated infertility. Int Urol Nephrol 47 (2015), 1471–1477.
9. Lewis, S.E., Should sperm DNA fragmentation testing be included in the male infertility work-up?. Reprod Biomed Online 31 (2015), 134–137.
10. Aitken, R.J., Krausz, C., Oxidative stress, DNA damage and the Y chromosome. Reproduction 122 (2001), 497–506.
11. Hamada, A., Esteves, S.C., Nizza, M., Agarwal, A., Unexplained male infertility: diagnosis and management. Int Braz J Urol 38 (2012), 576–594.
12. Hamada, A., Esteves, S.C., Agarwal, A., Insight into oxidative stress in varicocele-associated male infertility: part 2. Nat Rev Urol 10 (2013), 26–37.
13. Esteves, S.C., Sharma, R.K., Gosálvez, J., Agarwal, A., A translational medicine appraisal of specialized andrology testing in unexplained male infertility. Int Urol Nephrol 46 (2014), 1037–1052.
14. Majzoub, A., Esteves, S.C., Gosálvez, J., Agarwal, A., Specialized sperm function tests in varicocele and the future of andrology laboratory. Asian J Androl 18 (2016), 205–212.
15. Spano, M., Bonde, J.P., Hjollund, H.I., Kolstad, H.A., Cordelli, E., Leter, G., Danish First Pregnancy Planner Study Team. Sperm chromatin damage impairs human fertility. Fertil Steril 73 (2000), 43–50.
16. Feijo, C.M., Esteves, S.C., Diagnostic accuracy of sperm chromatin dispersion test to evaluate sperm deoxyribonucleic acid damage in men with unexplained infertility. Fertil Steril 101 (2014), 58–63.
17. Esteves, S.C., Novel concepts in male factor infertility: clinical and laboratory perspectives. J Assist Reprod Genet 33 (2016), 1319–1335.
18. Bungum, M., Humaidan, P., Axmon, A., Spano, M., Bungum, L., Erenpreiss, J., et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod 22 (2007), 174–179.
19. Evgeni, E., Lymberopoulos, G., Gazouli, M., Asimakopoulos, B., Conventional semen parameters and DNA fragmentation in relation to fertility status in a Greek population. Eur J Obstet Gynecol Reprod Biol 188 (2015), 17–23.
20. Samplaski, M.K., Dimitromanolakis, A., Lo, K.C., Grober, E.D., Mullen, B., Garbens, A., et al. The relationship between sperm viability and DNA fragmentation rates. Reprod Biol Endocrinol, 13, 2015, 42.
21. Saleh, R.A., Agarwal, A., Nelson, D.R., Nada, E.A., El-Tonsy, M.H., Alvarez, J.G., et al. Increased sperm nuclear DNA damage in normozoospermic infertile men: a prospective study. Fertil Steril 78 (2002), 313–318.
22. Giwercman, A., Lindstedt, L., Larsson, M., Bungum, M., Spano, M., Levine, R.J., et al. Sperm chromatin structure assay as an independent predictor of fertility in vivo: a case-control study. Int J Androl 33 (2010), e221–e227.
23. Practice Committee of the American Society for Reproductive Medicine. Diagnostic evaluation of the infertile male: a committee opinion. Fertil Steril 103 (2015), 18–25.
24. Agarwal, A., Cho, C.L., Esteves, S.C., Should we evaluate and treat sperm DNA fragmentation?. Curr Opin Obstet Gynecol 28 (2016), 164–171.
25. Agarwal, A., Majzoub, A., Esteves, S.C., Ko, E., Ramasamy, R., Zini, A., Clinical utility of sperm DNA fragmentation testing: practice recommendations based on clinical scenarios. Transl Androl Urol 5 (2016), 935–950.
26. Seli, E., Gardner, D.K., Schoolcraft, W.B., Moffatt, O., Sakkas, D., Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertil Steril 82 (2004), 378–383.
27. Lewis, S.E., Aitken, R.J., DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res 322 (2005), 33–41.
28. Tesarik, J., Greco, E., Mendoza, C., Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum Reprod 19 (2004), 611–615.
29. Avendaño, C., Franchi, A., Duran, H., Oehninger, S., DNA fragmentation of normal spermatozoa negatively affects embryo quality and intracytoplasmic sperm injection outcome. Fertil Steril 94 (2010), 549–557.
30. Robinson, L., Gallos, I.D., Conner, S.J., Rajkhowa, M., Miller, D., Lewis, S., et al. The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis. Hum Reprod 27 (2012), 2908–2917.
31. Zini, A., Boman, J.M., Belzile, E., Ciampi, A., Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Human Reprod 23 (2008), 2663–2668.
32. Greco, E., Scarselli, F., Iacobelli, M., Rienzi, L., Ubaldi, F., Ferrero, S., et al. Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Hum Reprod 20 (2005), 226–230.
33. Sakkas, D., Alvarez, J.G., Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril 93 (2010), 1027–1036.
34. Esteves, S.C., Sánchez-Martín, F., Sánchez-Martín, P., Schneider, D.T., Gosálvez, J., Comparison of reproductive outcome in oligozoospermic men with high sperm DNA fragmentation undergoing intracytoplasmic sperm injection with ejaculated and testicular sperm. Fertil Steril 104 (2015), 1398–1405.
35. Mehta, A., Bolyakov, A., Schlegel, P.N., Paduch, D.A., Higher pregnancy rates using testicular sperm in men with severe oligospermia. Fertil Steril 104 (2015), 1382–1387.
36. Bradley, C.K., McArthur, S.J., Gee, A.J., Weiss, K.A., Schmidt, U., Toogood, L., Intervention improves assisted conception intracytoplasmic sperm injection outcomes for patients with high levels of sperm DNA fragmentation: a retrospective analysis. Andrology 4 (2016), 903–910.
37. Moskovtsev, S.I., Jarvi, K., Mullen, J.B., Cadesky, K.I., Hannam, T., Lo, K.C., Testicular spermatozoa have statistically significantly lower DNA damage compared with ejaculated spermatozoa in patients with unsuccessful oral antioxidant treatment. Fertil Steril 93 (2010), 1142–1146.
38. Muratori, M., Tamburrino, L., Marchiani, S., Cambi, M., Olivito, B., Azzari, C., et al. Investigation on the origin of sperm DNA fragmentation: role of apoptosis, immaturity and oxidative stress. Mol Med 21 (2015), 109–122.
39. Moher, D., Liberati, A., Tetzlaff, J., Altman, D.G., Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. BMJ 339 (2009), 332–339.
40. Sterne, J.A.C., Hernán, M.A., Reeves, B.C., Savovic, J., Berkman, N.D., Viswanathan, M., et al. ROBINS-I: a tool for assessing risk of bias in nonrandomized studies of interventions. BMJ, 355, 2016, i4919.
41. Higgins JPT, Green S, eds. Cochrane handbook for systematic reviews of interventions version 5.1.0 [updated March 2011]. Cochrane Collaboration, 2011. Available at: http://handbook.cochrane.org. Accessed Dec 10th, 2016.
42. Steger, K., Wilhelm, J., Konrad, L., Stalf, T., Greb, R., Diemer, T., et al. Both protamine-1 to protamine-2 mRNA ratio and Bcl2 mRNA content in testicular spermatids and ejaculated spermatozoa discriminate between fertile and infertile men. Hum Reprod 23 (2008), 11–16.
43. Sharbatoghli, M., Valojerdi, M.R., Amanlou, M., Khosravi, F., Jafar-abadi, M.A., Relationship of sperm DNA fragmentation, apoptosis and dysfunction of mitochondrial membrane potential with semen parameters and ART outcome after intracytoplasmic sperm injection. Arch Gynecol Obstet 286 (2012), 1315–1322.
44. Moskovtsev, S.I., Alladin, N., Lo, K.C., Jarvi, K., Mullen, J.B.M., Librach, C.L., A comparison of ejaculated and testicular spermatozoa aneuploidy rates in patients with high sperm DNA damage. Syst Biol Reprod Med 58 (2012), 142–148.
45. Pabuccu, E.G., Caglar, G.S., Tangal, S., Haliloglu, A.H., Pabuccu, R., Testicular versus ejaculated spermatozoa in ICSI cycles of normozoospermic men with high sperm DNA fragmentation and previous ART failures. Andrologia, 49, 2017, e12609.
46. Abhyankar, N., Kathrins, M., Niederberger, C., Use of testicular sperm for intracytoplasmic sperm injection among men with cryptozoospermia: a meta-analysis. Fertil Steril 105 (2016), 1469–1475.
47. Cho, C.L., Esteves, S.C., Agarwal, A., Novel insights into the pathophysiology of varicocele and its association with reactive oxygen species and sperm DNA fragmentation. Asian J Androl 18 (2016), 186–193.
48. Rubes, J., Selevan, S.G., Sram, R.J., Evenson, D.P., Perreault, S.D., GSTM1 genotype influences the susceptibility of men to sperm DNA damage associated with exposure to air pollution. Mut Res 625 (2007), 20–28.
49. Agarwal, A., Hamada, A., Esteves, S.C., Insight into oxidative stress in varicocele-associated male infertility: part 1. Nat Rev Urol 9 (2012), 678–690.
50. Sotolongo, B., Huang, T.T., Isenberger, E., Ward, W.S., An endogenous nuclease in hamster, mouse, and human spermatozoa cleaves DNA into loop-sized fragments. J Androl 26 (2005), 272–280.
51. Steele, E.K., McClure, N., Maxwell, R.J., Lewis, S.E., A comparison of DNA damage in testicular and proximal epididymal spermatozoa in obstructive azoospermia. Mol Hum Reprod 5 (1999), 831–835.
52. O'Connell, M., McClure, N., Lewis, S.E., Mitochondrial DNA deletions and nuclear DNA fragmentation in testicular and epididymal human sperm. Hum Reprod 17 (2002), 1565–1570.
53. Suganuma, R., Yanagimachi, R., Meistrich, M.L., Decline in fertility of mouse sperm with abnormal chromatin during epididymal passage as revealed by ICSI. Hum Reprod 20 (2005), 3101–3108.
54. Cissen, M., Wely, M.V., Scholten, I., Mansell, S., Bruin, J.P., Mol, B.W., et al. Measuring sperm DNA fragmentation and clinical outcomes of medically assisted reproduction: a systematic review and meta-analysis. PLoS One, 11, 2016, e0165125.
55. Zini, A., Bach, P.V., Al-Malki, A.H., Schlegel, P.N., Use of testicular sperm for ICSI in oligozoospermic couples: how far should we go?. Hum Reprod 32 (2017), 7–13.
56. Tiseo, B.C., Esteves, S.C., Cocuzza, M.S., Summary evidence on the effects of varicocele treatment to improve natural fertility in subfertile men. Asian J Androl 18 (2016), 239–245.
57. Zini, A., Dohle, G., Are varicoceles associated with increased deoxyribonucleic acid fragmentation?. Fertil Steril 96 (2011), 1283–1287.
58. Wang, Y.J., Zhang, R.Q., Lin, Y.J., Zhang, R.G., Zhang, W.L., Relationship between varicocele and sperm DNA damage and the effect of varicocele repair: a meta-analysis. Reprod Biomed Online 25 (2012), 307–314.
59. Smit, M., Romijn, J.C., Wildhagen, M.F., Veldhoven, J.L., Weber, R.F., Dohle, G.R., Decreased sperm DNA fragmentation after surgical varicocelectomy is associated with increased pregnancy rate. J Urol 189 (2013), S146–S150.
60. Ni, K., Steger, K., Yang, H., Wang, H., Hu, K., Chen, B., Sperm protamine mRNA ratio and DNA fragmentation index represent reliable clinical biomarkers for men with varicocele after microsurgical varicocele ligation. J Urol 192 (2014), 170–176.
61. Moskovtsev, S.I., Lecker, I., Mullen, J.B., Jarvi, K., Willis, J., White, J., et al. Cause specific treatment in patients with high sperm DNA damage resulted in significant DNA improvement. Syst Biol Reprod Med 55 (2009), 109–115.
62. Zini, A., San Gabriel, M., Baazeem, A., Antioxidants and sperm DNA damage: a clinical perspective. J Assist Reprod Genet 26 (2009), 427–432.
63. Talevi, R., Barbato, V., Fiorentino, I., Braun, S., Longobardi, S., Gualtieri, R., Protective effects of in vitro treatment with zinc, d-aspartate and coenzyme Q10 on human sperm motility, lipid peroxidation and DNA fragmentation. Reprod Biol Endocrinol, 11, 2013, 81.
64. Showell, M.G., Mackenzie-Proctor, R., Brown, J., Yazdani, A., Stankiewicz, M.T., Hart, R.J., Antioxidants for male subfertility. Cochrane Database Syst Rev, 2014, CD007411.
65. Kort, H.I., Massey, J.B., Elsner, C.W., Mitchell-Leef, D., Shapiro, D.B., Witt, M.A., et al. Impact of body mass index values on sperm quantity and quality. J Androl 27 (2006), 450–452.
66. Wijesekara, G.U., Fernando, D.M., Wijerathna, S., Bandara, N., Environmental and occupational exposures as a cause of male infertility. Ceylon Med J 60 (2015), 52–56.
67. Sánchez-Peña, L.C., Reyes, B.E., López-Carrillo, L., Organophosphorous pesticide exposure alters sperm chromatin structure in Mexican agricultural workers. Toxicol Appl Pharmacol 196 (2004), 108–113.
68. Esteves, S.C., Lee, W., Benjamin, D.J., Seol, B., Verza, S. Jr., Agarwal, A., Reproductive potential of men with obstructive azoospermia undergoing percutaneous sperm retrieval and intracytoplasmic sperm injection according to the cause of obstruction. J Urol 189 (2013), 232–237.
69. Esteves, S.C., Clinical management of infertile men with nonobstructive azoospermia. Asian J Androl 17 (2015), 459–470.
70. Esteves, S.C., Miyaoka, R., Agarwal, A., Sperm retrieval techniques for assisted reproduction. Int Braz J Urol 37 (2011), 570–583.
71. Esteves, S.C., Miyaoka, R., Orosz, J.E., Agarwal, A., An update on sperm retrieval techniques for azoospermic males. Clinics (Sao Paulo) 68:Suppl 1 (2013), 99–110.