A systematic review and meta-analysis to determine the effect of sperm DNA damage on in vitro fertilization and intracytoplasmic sperm injection outcome

Asian Journal of Andrology

Volumn 19, Issue 1, 2017, Pages 80-90

  Simon, Luke ^a   Zini, Armand ^b   Dyachenko, Alina ^b   Ciampi, Antonio ^b   Carrell, Douglas ^a  

^a UNIVERSITY OF UTAH SCHOOL OF MEDICINE   (United States)

^b ST MARY S HOSPITAL   (Canada)

Author keywords

assisted reproductive technology outcomes; clinical pregnancy; meta analysis; sperm DNA damage; systematic review

Indexed keywords

COMET ASSAY; DNA DAMAGE; EMBASE; FEMALE; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; MEDLINE; META ANALYSIS; PREGNANCY; SYSTEMATIC REVIEW; TUNEL ASSAY; DNA FRAGMENTATION; IN VITRO FERTILIZATION; INFERTILITY, MALE; MALE; METABOLISM; PREGNANCY RATE; SPERMATOZOON;

COMET ASSAY; DNA DAMAGE; DNA FRAGMENTATION; FEMALE; FERTILIZATION IN VITRO; HUMANS; IN SITU NICK-END LABELING; INFERTILITY, MALE; MALE; PREGNANCY; PREGNANCY RATE; SPERM INJECTIONS, INTRACYTOPLASMIC; SPERMATOZOA;

EID: 85008622761     PISSN: 1008682X     EISSN: 17457262     Source Type: Journal    
DOI: 10.4103/1008-682X.182822     Document Type: Review

References (137)

1. Aitken RJ. Sperm function tests and fertility. Int J Androl 2006; 29: 69-75
2. Kovac JR, Pastuszak AW, Lamb DJ. The use of genomics, proteomics, and metabolomics in identifying biomarkers of male infertility. Fertil Steril 2013; 99: 998-1007
3. Pregl Breznik B, Kovacic B, Vlaisavljevic V. Are sperm DNA fragmentation, hyperactivation and hyaluronan-binding ability predictive for fertilization and embryo development in in vitro fertilization and intracytoplasmic sperm injection Fertil Steril 2013; 99: 1233-41
4. Ruvolo G, Fattouh RR, Bosco L, Brucculeri AM, Cittadini E. New molecular markers for the evaluation of gamete quality. J Assist Reprod Genet 2013; 30: 207-12
5. Pacey AA. Assessment of male factor. Best Pract Res Clin Obstet Gynaecol 2012; 26: 739-46
6. Aitken RJ, de Iuliis GN. Origins and consequences of DNA damage in male germ cells. Reprod Biomed Online 2007; 14: 727-33
7. Zini A, Sigman M. Are tests of sperm DNA damage clinically useful Pros and cons. J Androl 2009; 30: 219-29
8. Barratt CL, Aitken RJ, Bjorndahl L, Carrell DT, de Boer P, et al. Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications - A position report. Hum Reprod 2010; 25: 824-38
9. Evenson DP, Jost LK, Marshall D, Zinaman MJ, Clegg E, et al. Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod 1999; 14: 1039-49
10. O'Brien J, Zini A. Sperm DNA integrity and male infertility. Urology 2005; 65: 16-22
11. Fernandez JL, Velez de la Calle JF, Tamayo M, Cajigal D, Agarwal A, et al. Sperm DNA integrity and male infertility: current perspectives. Arch Med Sci 2009; 5: S55-62
12. Simon L, Lutton D, McManus J, Lewis SE. Sperm DNA damage measured by the alkaline Comet assay as an independent predictor of male infertility and IVF success. Fertil Steril 2011a; 95: 652-7
13. Li L, Wang L, Cai J, Huang H. Correlation of sperm DNA damage with IVF and ICSI outcomes: a systematic review and meta-analysis. J Assist Reprod Genet 2006; 23: 367-76
14. Collins JA, Barnhart KT, Schlegel PN. Do sperm DNA integrity tests predict pregnancy with in vitro fertilization Fertil Steril 2008; 89: 823-31
15. The Practice Committee of the American Society for Reproductive Medicine. The clinical utility of sperm DNA integrity testing: a guideline. Fertil Steril 2013; 99: 673-7
16. Zini A, Boman JM, 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. Hum Reprod 2008; 23: 2663-8
17. Zhao J, Zhang Q, Wang Y, Li Y. Whether sperm deoxyribonucleic acid fragmentation has an effect on pregnancy and miscarriage after in vitro fertilization/intracytoplasmic sperm injection: a systematic review and meta-analysis. Fertil Steril 2014; 102: 998-1005
18. Barratt CL, De Jonge CJ. Clinical relevance of sperm DNA assessment: an update. Fertil Steril 2010; 94: 1958-9
19. Gorczyca W, Gong J, Drazynkiewicz Z. Detection of DNA strand breaks in individual apoptotic cells by the in situ terminal deoxynucleotidyl transferase and nick translation assay. Cancer Res 1993a; 53: 1945-51
20. Hughes CM, Lewis SE, McKelvey-Martin VJ, Thompson W. A comparison of baseline and induced DNA damage in human spermatozoa from fertile and infertile men, using a modified comet assay. Mol Hum Reprod 1996; 2: 613-9
21. Fernandez JL, Muriel L, Goyanes V, Segrelles E, Gosalvez J, et al. Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion test. Fertil Steril 2005; 84: 833-42
22. Henkel R, Hoogendijk CF, Bouic PJ, Kruger TF. TUNEL assay and SCSA determine different aspects of sperm DNA damage. Andrologia 2010; 42: 305-13
23. Schulte RT, Ohl DA, Sigman M, Smith GD. Sperm DNA damage in male infertility: etiologies, assays, and outcomes. J Assist Reprod Genet 2010; 27: 3-12
24. Tavukcuoglu IS, Al-Azawi T, Khaki AA, Khaki A, Khalil A, et al. Clinical value of DNA fragmentation evaluation tests under ART treatments. J Turk Ger Gynecol Assoc 2012; 13: 270-4
25. Ostling O, Johanson KJ. Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem Biophy Res Commun 1984; 123: 291-8
26. Gorczyca W, Traganos F, Jesionowska H, Darzynkiewicz Z. Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells. Exp Cell Res 1993b; 207: 202-5
27. Fernandez JL, Mouriel L, Rivero MT, Goyanes V, Vasquez R, et al. The sperm chromatin dispersion test: a simple method for the determination of sperm DNA fragmentation. J Androl 2003; 24: 59-66
28. Drazynkiewicz Z, Kapuscinski J. Acridine orange: A versatile probe of nucleic acids and other cell constituents. In: Melamed MR, Lindmo T, Mendelsohn ML, editors. Flow Cytometry and Sorting. 2nd ed. New York: Wiley-Liss; 1976. p. 291-314
29. Chohan KR, Griffin JT, Lafromboise M, DeJonge CJ, Carrell DT. Comparison of chromatin assays for DNA fragmentation evaluation in human sperm. J Androl 2006; 27: 53-9
30. Nallella KP, Sharma RK, Aziz N, Agarwal A. Significance of sperm characteristics in the evaluation of male infertility. Fertil Steril 2006; 85: 629-34
31. Natali A, Turek PJ. An assessment of new sperm tests for male infertility. Urology 2011; 77: 1027-34
32. Ribas-Maynou J, Garcra-Peiro A, Fernandez-Encinas A, Abad C, Amengual MJ, et al. Comprehensive analysis of sperm DNA fragmentation by five different assays: TUNEL assay, SCSA, SCD test and alkaline and neutral comet assay. Andrology 2013; 1: 715-22
33. Simon L, Liu L, Murphy K, Ge S, Hotaling J, et al. Comparative analysis of three sperm DNA damage assays and sperm nuclear protein content in couples undergoing assisted reproduction treatment. Hum Reprod 2014a; 29: 904-17
34. Egger M, Smith GD, Altman DG. Systematic Reviews in Health Care: Meta-analysis in Context. London: BMJ Publishing; 2001. p. 506
35. Deville WL, Buntinx F, Bouter LM, Montori VM, de Vet HC, et al. Conducting systematic reviews of diagnostic studies: didactic guidelines. BMC Med Res Methodol 2002; 2: 9
36. Evenson D, Wixon R. Meta-analysis of sperm DNA fragmentation using the sperm chromatin structure assay. Reprod Biomed Online 2006; 12: 466-72
37. Sharma RK, Sabanegh E, Mahfouz R, Gupta S, Thiyagarajan A, et al. TUNEL as a test for sperm DNA damage in the evaluation of male infertility. Urology 2010; 76: 1380-6
38. Larson KL, de Jonge CJ, Barnes AM, Jost LK, Evenson DP. Sperm chromatin structure assay parameters as predicted of failed pregnancy following assisted reproductive techniques. Hum Reprod 2000; 15: 1717-22
39. Bungum M, Humaidan P, Spano M, Jepson K, Bungum L, et al. The predictive value of sperm chromatin structure assay (SCSA) parameters for the outcome of intrauterine insemination, IVF and ICSI. Hum Reprod 2004; 19: 1401-8
40. Henkel R, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C, et al. Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril 2004; 81: 965-72
41. Simon L, Proutski I, Stevenson M, Jennings D, McManus J, et al. Sperm DNA damage has negative association with live birth rates after IVF. Reprod Biomed Online 2012; 26: 68-78
42. Chi HJ, Chung DY, Choi SY, Kim JH, Kim GY, et al. Integrity of human sperm DNA assessed by the neutral comet assay and its relationship to semen parameters and clinical outcomes for the IVF-ET program. Clin Exp Reprod Med 2011; 38: 10-7
43. Abu-Hassan D, Koester F, Shoepper B, Schultze-Mosgau A, Asimakopoulos B, et al. Comet assay of cumulus cells and spermatozoa DNA status, and the relationship to oocyte fertilization and embryo quality following ICSI. Reprod Biomed Online 2006; 12: 447-52
44. Sakkas D, Urner F, Bianchi P, Bizzaro D, Wagner I, et al. Sperm chromatin anomalies can influence decondensation after intracytoplasmic sperm injection. Hum Reprod 1996; 11: 837-43
45. Tomlinson MJ, Moffatt O, Manicardi GC, Bizzaro D, Afnan M, et al. Interrelationships between seminal parameters and sperm nuclear DNA damage before and after density gradient centrifugation: implications for assisted conception. Hum Reprod 2001; 16: 2160-5
46. Oehninger S, Franken DR, Ombelet W. Sperm functional tests. Fertil Steril 2014; 102: 1528-33
47. Wang C, Swerdloff RS. Limitations of semen analysis as a test of male fertility and anticipated needs from newer tests. Fertil Steril 2014; 102: 1502-7
48. Sigman M. Refining the measurement of sperm DNA fragmentation. Fertil Steril 2012; 98: 1123
49. Bungum M. Sperm DNA integrity assessment: a new tool in diagnosis and treatment of fertility. Obstet Gynecol Int 2012; 2012: 531042
50. Palermo GD, Neri QV, Cozzubbo T, Rosenwaks Z. Perspectives on the assessment of human sperm chromatin integrity. Fertil Steril 2014; 102: 1508-17
51. Tarlatzis BC, Goulis DG. Sperm DNA fragmentation assessment: is it really helpful Gynecol Endocrinol 2010; 26: 315-6
52. Beshay VE, Bukulmez O. Sperm DNA damage: how relevant is it clinically Curr Opin Obstet Gynecol 2012; 24: 172-9
53. Ramalho-Santos J. Sins of the fathers: sperm DNA damage in the context of assisted reproduction. Hum Reprod 2014; 29: 2356-8
54. Simon L, Murphy K, Shamsi MB, Liu L, Emery B, et al. Paternal influence of sperm DNA integrity on early embryonic development. Hum Reprod 2014b; 29: 2402-12
55. Saleh RA, Agarwal A, Nada EA, El-Tonsy MH, Sharma RK, et al. Negative effects of increased sperm DNA damage in relation to seminal oxidative stress in men with idiopathic and male factor infertility. Fertil Steril 2003; 79: 1597-605
56. Gandini L, Lombardo F, Paoli D, Caruso F, Eleuteri P, et al. Full-term pregnancies achieved with ICSI despite high levels of sperm chromatin damage. Hum Reprod 2004; 19: 1409-17
57. 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 2010; 183: 270-4
58. Greco E, Scarselli F, Iacobelli M, Rienzi L, Ubaldi F, et al. Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Hum Reprod 2005; 20: 226-30
59. Bungum M, Spano M, Humaidan P, Eleuteri P, Rescia M, et al. Sperm chromatin structure assay parameters measured after density gradient centrifugation are not predictive for the outcome of ART. Hum Reprod 2008; 23: 4-10
60. Claassens OE, Menkveld R, Franken V, Pretorius E, Swart Y, et al. The acridine orange test: determining the relationship between sperm morphology and fertilization in vitro. Hum Reprod 1992; 7: 242-7
61. Hoshi K, Katayose H, Yanagida K, Kimura Y, Sato A. The relationship between acridine orange fluorescence of sperm nuclei and the fertilizing ability of human sperm. Fertil Steril 1996; 66: 634-9
62. Angelopoulos T, Moshel YA, Lu L, Macanas E, Grifo JA, et al. Simultaneous assessment of sperm chromatin condensation and morphology before and after separation procedures: effect on the clinical outcome after in vitro fertilization. Fertil Steril 1998; 69: 740-7
63. Hammadeh ME, Al-Hassani S, Gaub C, Rosenbaum P, Georg T, et al. Prediction value of chromatin decondensation in vitro on fertilization rate after intracytoplasmic sperm injection (ICSI). Int J Androl 2001; 24: 311-6
64. Hammadeh ME, Al Hasani S, Rosenbaum P, Schmidt W, Hammadeh CF. Reactive oxygen species, total antioxidant concentration of seminal plasma and their effect on sperm parameters and outcome of IVF/ICSI patients. Arch Gynecol Obstet 2008; 277: 515-26
65. Virant-Klun I, Tomazevic T, Meden-Vrtovec H. Sperm single-stranded DNA, detected by acridine orange staining, reduces fertilization and quality of ICSI-derived embryos. J Assist Reprod Genet 2002; 19: 319-28
66. Duran EH, Gurgan T, Gunalp S, Enginsu ME, Yarali H, et al. A logistic regression model including DNA status and morphology of spermatozoa for prediction of fertilization in vitro. Hum Reprod 1998; 13: 1235-9
67. Duran EH, Morshedi M, Taylor S, Oehninger S. Sperm DNA quality predicts intrauterine insemination outcome: a prospective cohort study. Hum Reprod 2002; 17: 3122-8
68. Katayose H, Yanagida K, Hashimoto S, Yamada H, Sato A. Use of diamide-acridine orange fluorescence staining to detect aberrant protamination of human-ejaculated sperm nuclei. Fertil Steril 2003; 79: 670-6
69. Cebesoy FB, Aydos K, Unlu C. Effect of sperm chromatin damage on fertilization ratio and embryo quality post-ICSI. Arch Androl 2006; 52: 397-402
70. Zhang Y, Wang H, Wang L, Zhou Z, Sha J, et al. The clinical significance of sperm DNA damage detection combined with routine semen testing in assisted reproduction. Mol Med Report 2008; 1: 617-24
71. Jiang H, He RB, Wang CL, Zhu J. The relationship of sperm DNA fragmentation index with the outcomes of in-vitro fertilisation-embryo transfer and intracytoplasmic sperm injection. J Obstet Gynaecol 2011b; 31: 636-9
72. Wang WB, Zhao LW, Xiang ZQ, Zhou XZ, Gui YL, et al. Correlation analysis of the results of double fluorescence (AO/PI) staining and clinical outcomes. J Reprod Contracept 2012; 23: 111-8
73. Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, et al. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod 2007; 22: 174-9
74. Boe-Hansen GB, Fedder J, Ersboll AK, Christensen P. The sperm chromatin structure assay as a diagnostic tool in the human fertility clinic. Hum Reprod 2006; 21: 1576-82
75. Muriel L, Meseguer M, Fernandez JL, Alvarez J, Remohi J, et al. Value of the sperm chromatin dispersion test in predicting pregnancy outcome in intrauterine insemination: a blind prospective study. Hum Reprod 2006b; 21: 738-44
76. Thomson LK, Zieschang JA, Clark AM. Oxidative deoxyribonucleic acid damage in sperm has a negative impact on clinical pregnancy rate in intrauterine insemination but not intracytoplasmic sperm injection cycles. Fertil Steril 2011; 96: 843-7
77. Yang XY, Zhang Y, Sun XP, Cui YQ, Qian XQ, et al. Sperm chromatin structure assay predicts the outcome of intrauterine insemination. Natl J Androl 2011; 17: 977-83
78. Alkhayal A, San Gabriel M, Zeidan K, Alrabeeah K, Noel D, et al. Sperm DNA and chromatin integrity in semen samples used for intrauterine insemination. J Assist Reprod Genet 2013; 30: 1519-24
79. Sun JG, Jurisicova A, Casper RF. Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 1997; 56: 602-7
80. Lopes S, Sun JG, Jurisicova A, Meriano J, Casper RF. Sperm deoxyribonucleic acid fragmentation is increased in poor quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril 1998; 69: 528-32
81. Marchetti C, Obert G, Deffosez A, Formstecher P, Marchetti P. Study of mitochondrial membrane potential, reactive oxygen species, DNA fragmentation and cell viability by flow cytometry in human sperm. Hum Reprod 2002; 17: 1257-65
82. Tomsu M, Sharma V, Miller D. Embryo quality and IVF treatment outcome may correlate with different sperm comet parameters. Hum Reprod 2002; 17: 1856-62
83. Lewis SEM, O'Connell M, Stevenson M, Thompson-Cree L, McClure N. An algorithm to predict pregnancy in assisted reproduction. Hum Reprod 2004; 19: 1385-94
84. Nasr-Esfahani MH, Salehi M, Razavi S, Anjlmshoa M, Rozahani S, et al. Effect of sperm DNA damage and sperm protamine deficiency on fertilization and embryo development post-ICSI. Reprod Biomed Online 2005; 11: 198-205
85. Hammadeh ME, Radwan M, Al-Hasani S, Micu R, Rosenbaum P, et al. Comparison of reactive oxygen species concentration in seminal plasma and semen parameters in partners of pregnant and nonpregnant patients after IVF/ICSI. Reprod Biomed Online 2006; 13: 696-706
86. Caglar GS, Koster F, Schopper B, Asimakopoulos B, Nehls B, et al. Semen DNA fragmentation index, evaluated with both TUNEL and comet assay, and the ICSI outcome. In Vivo 2007; 21: 1075-80
87. Stevanato J, Bertolla RP, Barradas V, Spaine DM, Cedenho AP, et al. Semen processing by density gradient centrifugation does not improve sperm apoptotic deoxyribonucleic acid fragmentation rates. Fertil Steril 2008; 90: 889-90
88. Velez de la Calle JF, Muller A, Walschaerts M, Clavere JL, Jimenez C, et al. Sperm deoxyribonucleic acid fragmentation as assessed by the sperm chromatin dispersion test in assisted reproductive technology programs: results of a large prospective multicenter study. Fertil Steril 2008; 90: 1792-9
89. Gu LJ, Chen ZW, Chen ZJ, Xu JF, Li M. Sperm chromatin anomalies have an adverse effect on the outcome of conventional in vitro fertilization: a study with strictly controlled external factors. Fertil Steril 2009; 92: 1344-6
90. Gu LJ, Lu WH, Chen ZW. Effects of fertilization and pregnancy after embryo transfer-Sperm DNA damage in vitro fertilization. Chin J Birth Health Hered 2011; 19: 111-2. [In Chinese]
91. Nijs M, Creemers E, Cox A, Franssen K, Janssen M, et al. Chromomycin A3 staining, sperm chromatin structure assay and hyaluronic acid binding assay as predictors for assisted reproductive outcome. Reprod Biomed Online 2009; 19: 671-84
92. Nijs M, De Jonge C, Cox A, Janssen M, Bosmans E, et al. Correlation between male age, WHO sperm parameters, DNA fragmentation, chromatin packaging and outcome in assisted reproduction technology. Andrologia 2011; 43: 174-9
93. Tarozzi N, Nadalini M, Stronati A, Prato LD, Coticchio G, et al. Anomalies in sperm chromatin packing: impactions for assisted reproductive treatment. Reprod Biomed Online 2009; 18: 486-95
94. Tavalaee M, Razavi S, Nasr-Esfahani MH. Influence of sperm chromatin anomalies on assisted reproductive technology outcome. Fertil Steril 2009; 91: 1119-26
95. Daris B, Goropevnek A, Hojnik N, Vlaisavljevi V. Sperm morphological abnormalities as indicators of DNA fragmentation and fertilization in ICSI. Arch Gynecol Obstet 2010; 281: 363-7
96. Kennedy C, Ahlering P, Rodriguez H, Levy S, Sutovsky P. Sperm chromatin structure correlates with spontaneous abortion and multiple pregnancy rates in assisted reproduction. Reprod Biomed Online 2011; 22: 272-6
97. Na L, Li L. Effect of sperm DNA damage on the outcome of in vitro fertilization-embryo transfer. Guangxi Med J 2011; 33: 257-60
98. Rama Raju GA, Prakash GJ, Krishna KM, Madan K, Narayana TS, et al. Noninsulin-dependent diabetes mellitus: effects on sperm morphological and functional characteristics, nuclear DNA integrity and outcome of assisted reproductive technique. Andrologia 2012; 44: 490-8
99. Sharbatoghli M, Valojerdi MR, Amanlou M, Khosravi F, Jafar-Abadi MA. 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 2012; 286: 1315-22
100. Lazaros L, Vartholomatos G, Pamporaki C, Kosmas I, Takenaka A, et al. Sperm flow cytometric parameters are associated with ICSI outcome. Reprod Biomed Online 2013; 26: 611-8
101. Sanchez-Martin P, Sanchez-Martin F, Gonzalez-Martinez M, Gosalvez J. Increased pregnancy after reduced male abstinence. Syst Biol Reprod Med 2013; 59: 256-60
102. Benchaib M, Lornage J, Mazoyer C, Lejeune H, Salle B, et al. Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertil Steril 2007; 87: 93-101
103. Borini A, Tarozzi N, Bizzaro D, Bonu MA, Fava L, et al. Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART. Hum Reprod 2006; 21: 2876-81
104. Frydman N, Prisant N, Hesters L, Frydman R, Tachdjian G, et al. Adequate ovarian follicular status does not prevent the decrease in pregnancy rates associated with high sperm DNA fragmentation. Fertil Steril 2008; 89: 93-8
105. Henkel R, Kierspel E, Hajimohammad M, Stalf T, Hoogendijk C, et al. DNA fragmentation of spermatozoa and assisted reproduction technology. Reprod Biomed Online 2003; 7: 477-84
106. Host E, Lindenberg S, Smidt-Jensen S. The role of DNA strand breaks in human spermatozoa used for IVF and ICSI. Acta Obstet Gynecol Scand 2000; 79: 559-63
107. Huang CC, Lin DP, Tsao HM, Cheng TC, Liu CH, et al. Sperm DNA fragmentation negatively correlates with velocity and fertilization rates but might not affect pregnancy rates. Fertil Steril 2005; 84: 130-40
108. Lin HH, Lee RK, Li SH, Lu CH, Sun FJ, et al. Sperm chromatin structure assay parameters are not related to fertilization rates, embryo quality, and pregnancy rates in in vitro fertilization and intracytoplasmic sperm injection, but might be related to spontaneous abortion rates. Fertil Steril 2008; 90: 352-9
109. Speyer BE, Pizzey AR, Ranieri M, Joshi R, Delhanty JD, et al. Fall in implantation rates following ICSI with sperm with high DNA fragmentation. Hum Reprod 2010; 25: 1609-18
110. Jiang HH, He XJ, Song B, Cao YX. Sperm chromatin integrity test for predicting the outcomes of IVF and ICSI. Natl J Androl 2011a; 17: 1083-6
111. Fang L, Lou LJ, Ye YH, Jin F, Zhou J. A study on correlation between sperm DNA fragmentation index and age of male various parameters of sperm and in vitro fertilization outcome. Chin J Med Genet 2011; 28: 432-5
112. Ni W, Xiao S, Qiu X, Jin J, Pan C, et al. Effect of sperm DNA fragmentation on clinical outcome of frozen-thawed embryo transfer and on blastocyst formation. PLoS One 2014; 9: e94956
113. Simon L, Brunborg G, Stevenson M, Lutton D, McManus J, et al. Clinical significance of sperm DNA damage in assisted reproductive outcome. Hum Reprod 2010; 25: 1594-608
114. Simon L, Castillo J, Oliva R, Lewis S. The relationship between human sperm protamines, DNA damage and assisted reproductive outcomes. Reprod Biomed Online 2011b; 23: 724-34
115. Avendano C, Franchi A, Duran H, Oehninger S. DNA fragmentation of normal spermatozoa negatively impacts embryo quality and intracytoplasmic sperm injection outcome. Fertil Steril 2010; 94: 549-57
116. Check JH, Graziano V, Cohen R, Krotec J, Check ML. Effect of an abnormal sperm chromatin structural assay (SCSA) on pregnancy outcome following (IVF) with ICSI in previous IVF failures. Arch Androl 2005; 51: 121-4
117. Zini A, Meriano J, Kader K, Jarvi K, Laskin CA, et al. Potential adverse effect of sperm DNA damage on embryo quality after ICSI. Hum Reprod 2005; 20: 3476-80
118. Micinski P, Pawlicki K, Wielgus E, Bochenek M, TworkowskaI I. The sperm chromatin structure assay (SCSA) as prognostic factor in IVF/ICSI program. Reprod Biol 2009; 9: 65-70
119. Dar S, Grover SA, Moskovtsev SI, Swanson S, Baratz A, et al. In vitro fertilization-intracytoplasmic sperm injection outcome in patients with a markedly high DNA fragmentation index (>50%). Fertil Steril 2013; 100: 75-80
120. Yang XY, Wang LL, Chen P, Zhang Y, Zhang W, et al. Impact of sperm DNA fragmentation index and sperm malformation rate on the clinical outcome of ICSI. Natl J Androl 2013; 19: 1082-7
121. Nicopoullos JD, Gilling-Smith C, Almeida PA, Homa S, Norman-Taylor JQ, et al. Sperm DNA fragmentation in subfertile men: the effect on the outcome of intracytoplasmic sperm injection and correlation with sperm variables. Br J Urol Int 2008; 101: 1553-60
122. Nunez-Calonge R, Caballero P, Lopez-Fernandez C, Guijarro JA, Fernandez JL, et al. An improved experimental model for understanding the impact of sperm DNA fragmentation on human pregnancy following ICSI. Reprod Sci 2012; 19: 1163-8
123. Gosalvez J, Caballero P, Lopez-Fernandez C, Ortega L, Guijarro JA, et al. Can DNA fragmentation of neat or swim-up spermatozoa be used to predict pregnancy following ICSI of fertile oocyte donors Asian J Androl 2013; 15: 812-8
124. Seli E, Gardner DK, Schoolcraft WB, Moffatt O, Sakkas D. Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertil Steril 2004; 82: 378-83
125. Esbert M, Pacheco A, Vidal F, Florensa M, Riqueros M, et al. Impact of sperm DNA fragmentation on the outcome of IVF with own or donated oocytes. Reprod Biomed Online 2011; 23: 704-10
126. Benchaib M, Braun V, Lornage J, Hadj S, Salle B, et al. Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique. Hum Reprod 2003; 18: 1023-8
127. Bakos HW, Thompson JG, Feil D, Lane M. Sperm DNA damage is associated with assisted reproductive technology pregnancy. Int J Androl 2007; 31: 518-26
128. Larson-Cook KL, Brannian JD, Hansen KA, Kasperson KM, Aamold ET, et al. Relationship between the outcomes of assisted reproductive techniques and sperm DNA fragmentation as measured by the sperm chromatin structure assay. Fertil Steril 2003; 80: 895-902
129. Virro MR, Larson-Cook KL, Evenson DP. 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: 1289-95
130. Payne JF, Raburn DJ, Couchman GM, Price TM, Jamison MG, et al. Redefining the relationship between sperm deoxyribonucleic acid fragmentation as measured by the sperm chromatin structure assay and outcomes of assisted reproductive techniques. Fertil Steril 2005; 84: 356-64
131. Guerin P, Matillon C, Bleau G, Levy R, Menezo Y. Impact of sperm DNA fragmentation on ART outcome. Gynecol Obstet Fertil 2005; 33: 665-8
132. Muriel L, Garrido N, Fernandez JL, Remohi J, Pellicer A, et al. Value of the sperm DNA fragmentation level, measured by the sperm chromatin dispersion (SCD) test, in the IVF and ICSI outcome. Fertil Steril 2006a; 85: 371-83
133. Lopez G, Lafuente R, Checa MA, Carreras R, Brassesco M. Diagnostic value of sperm DNA fragmentation and sperm high-magnification for predicting outcome of assisted reproduction treatment. Asian J Androl 2013; 15: 790-4
134. Anifandis G, Bounartzi T, Messini CI, Dafopoulos K, Markandona R, et al. Sperm DNA fragmentation measured by Halosperm does not impact on embryo quality and ongoing pregnancy rates in IVF/ICSI treatments. Andrologia 2015; 47: 295-302
135. Meseguer M, Santiso R, Garrido N, Garcia-Herrero S, Remohi J, et al. Effect of sperm DNA fragmentation on pregnancy outcome depends on oocyte quality. Fertil Steril 2011; 95: 124-8
136. Morris ID, Iiott S, Dixon L, Brison DR. The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) and its relationship to fertilization and embryo development. Hum Reprod 2002; 17: 990-8
137. Ozmen B, Caglar GS, Koster F, Schopper B, Diedrich K, et al. Relationship between sperm DNA damage, induced acrosome reaction and viability in ICSI patients. Reprod Biomed Online 2007; 15: 208-14.