Volume 5, Issue 5 (7-2007)                   IJRM 2007, 5(5): 137-150 | Back to browse issues page

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Youssry M, Ozmen B, Orief Y, Zohni K, Al-Hasani S. Human sperm DNA damage in the context of assisted reproductive techniques. IJRM 2007; 5 (5) :137-150
URL: http://ijrm.ir/article-1-93-en.html
1- Department of Obstetrics and Gynecology, University of Alexandria, Alexandria, Egypt
2- Department of Obstetrics and Gynecology, University of Ankara, Ankara, Turkey
3- Medical Sciences Division, Reproduction Unit, National Research Center, Egypt
4- Department of Obstetrics and Gynecology, University of Schleswig – Holstein, Luebeck, Germany , sf_alhasani@hotmail.com
Abstract:   (3357 Views)
Fertilization involves direct interaction of the sperm and oocyte, fusion of the cell membranes and :::::union::::: of male and female gamete genomes. The completion of this process and subsequent embryo development depend in part on the inherent integrity of the sperm DNA. Sperm genome quality has been emphasized for several years as playing a major role in early embryogenesis. There is clinical evidence showing that human sperm DNA damage may adversely affect reproductive outcomes and that spermatozoa of infertile men possess substantially more DNA damage than do spermatozoa of fertile men. Testing DNA integrity may help selecting spermatozoa with intact DNA or with the least amount of DNA damage for use in assisted reproductive techniques (ARTs). This review will focus on how sperm DNA is organized, what causes sperm DNA damage and what impact this damage may have on reproductive outcome.
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Type of Study: Original Article |

References
1. Agarwal A, Said T. Role of sperm chromatin abnormalities and DNA damage in male infertility. Human Reprod Update 2003; 9:331-345. [DOI:10.1093/humupd/dmg027]
2. Sakkas D, Mariethoz E, Manicardi G, Bizari D, Bianchi P, Bianchi U. Origin of DNA damage in ejaculated human spermatozoa. Reviews of Reproduction 1999; 4:31-37. [DOI:10.1530/ror.0.0040031]
3. Alvarez J G. DNA fragmentation in human spermatozoa: significance in the diagnosis and treatment of infertility. Minerva Ginecol 2003; 55:233-239.
4. Potts RJ, Newbury CJ, Smith G, Notarianni LJ, Jefferies TM. Sperm chromatin damage associated with male smoking. Mutat Res 1999; 423:103-111. [DOI:10.1016/S0027-5107(98)00242-5]
5. Saleh R, Agarwal A, Sharma R, Nelson D, Tomas AJ. Effect of cigarette smoking on levels of seminal oxidative stress in infertile men: a prospective study. Fertil Steril 2002; 78:491-499. [DOI:10.1016/S0015-0282(02)03294-6]
6. Sun JG, Jurusucova A, Casper RF. Deletion of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 1997; 56: 602-607. [DOI:10.1095/biolreprod56.3.602]
7. Aitken R, Buckingham D, Brindle J, Gomez E, Baker G, Irvine S. Analysis of sperm movement in relation to the oxidative stress created by leucocytes in washed sperm preparations and seminal plasma. Hum Reprod1995; 10: 2061-2071. [DOI:10.1093/oxfordjournals.humrep.a136237]
8. Fraga CG, Motchnik PA, Wyrobek AJ, Rempel DM, Ames BN. Smoking and low antioxidant levels increase oxidative damage to sperm DNA. Mutat Res1996; 351: 199-209. [DOI:10.1016/0027-5107(95)00251-0]
9. Tomilson, MJ, White A, Barratt CL, Bolton AE, Cooke ID. The removal of morphologically abnormal sperm forms by phagocytes: a positive role for seminal leucocytes. Hum Reprod 1992; 7:517-522. [DOI:10.1093/oxfordjournals.humrep.a137682]
10. Sigman M, Lopes L. Correlation between round cells and white cells in the semen. J Urol 1993; 388: 573-574. [DOI:10.1016/S0022-5347(17)36386-3]
11. Alvarez JG, Sharma RK, Ollero M, Saleh R, Lopez M, Thomas AJ, Evnson, DP, Agarwal A. Increased DNA damage in sperm from leukocytospermic semen samples as determined by the sperm chromatin structure assay. Fertil Steril 2002; 78: 319-329. [DOI:10.1016/S0015-0282(02)03201-6]
12. Siciliano L, Tarantino P, Longobardi F, Rago V, De Stefano C, Caprino A. Impaired seminal antioxidant capacity in the human semen with hyperviscosity or oligoasthenozoospermia. J Androl 2001; 22:798-803.
13. Holmes RP, Goodman HO, Shihabi Z, Jarow JP. The taurine and hypotaurine content of human semen. J Androl 1992; 13: 289-292.
14. Potts RJ, Jefferies TM, Notarianni LJ. Atioxidant capacity of the epidedymis. Hum Reprod 1999; 14:2513-2516. [DOI:10.1093/humrep/14.10.2513]
15. Donnelly ET, Steele EK, Mcclure N, Lewis SE. Assessment of DNA integrity and morphology of ejaculated spermatozoa from fertile and infertile men before and after cryopreservation. Hum Reprod 2001; 16: 1191-1199. [DOI:10.1093/humrep/16.6.1191]
16. Sailer BL, Sarkar LJ, Bjordahl JA. Effects of heat stress on mouse testicular cells and sperm chromatin structure. J Androl 1997; 18:294-301.
17. Saleh RA, Agarwal A, Sharma RK. Evaluation of nuclear DNA damage in spermatozoa from infertile men with varicocele. Fertil Steril 2003; 80:1431-1436. [DOI:10.1016/S0015-0282(03)02211-8]
18. Fischer MA, Willis J, Zini A. Human sperm DNA integrity: correlation with sperm cytoplasmic droplets. Urology 2003; 61:207-211. [DOI:10.1016/S0090-4295(02)02098-8]
19. Zini A, Blumenfeld A, Libman J. Beneficial effect of microsurgical varicocelectomy on human sperm DNA integrity. Hum Reprod 2005; 20:1018-1021. [DOI:10.1093/humrep/deh701]
20. Chatterjee R, Haines GA, Perera DM, Goldstone A, Morris ID. Testicular and sperm DNA damage after treatment with fludarabine for chronic lymphocytic leukaemia. Hum Reprod 2000; 15:762-766. [DOI:10.1093/humrep/15.4.762]
21. Bucci LR, Meistrich ML. Effects of busulfan on murine spermatogenesis: cytotoxicity, sterility, sperm abnormalities, and dominant lethal mutations. Mutat Res 1987; 176:259-268. [DOI:10.1016/0027-5107(87)90057-1]
22. Armon J, Meirow D, Lewis-Roness H, Ornoy A. Genetic and teratogenic effects of cancer treatments on gametes and embryos. Hum Reprod Update 2001; 7:394-403. [DOI:10.1093/humupd/7.4.394]
23. Erenpreiss J, Spano M, Erenpreisa J. Sperm chromatin structure and male infertility: biological and clinical aspects. Asian Journal of Andrology 2006; 8:11-29. [DOI:10.1111/j.1745-7262.2006.00112.x]
24. Agarwal A, Said T. Oxidative stress, DNA damage and apoptosis in male infertility: a clinical approach. BJU International 2005; 95:503-507. [DOI:10.1111/j.1464-410X.2005.05328.x]
25. Aitken RJ, Krausz C. Oxidative stress, DNA damage and the Y chromosome. Reproduction 2001; 122: 497-506. [DOI:10.1530/rep.0.1220497]
26. Fuentes-Mascorro G, Serrano H, Rosado A. Sperm chromatin. Arch Androl 2000; 45: 215-225. [DOI:10.1080/01485010050193995]
27. Pienta KJ, Coffey DS. Structural analysis of the role of the nuclear matrix and DNA loops in the organization of the nucleus and chromosome. J Cell Suppl 1984; 1: 123-135. [DOI:10.1242/jcs.1984.Supplement_1.9]
28. Finch, JT, Klug A. Solenoid model superstructure in chromatin. Proc Natl Aca Sci USA 1976; 73: 1897-1901. [DOI:10.1073/pnas.73.6.1897]
29. Ward WS, Coffey DS. DNA packaging and organization in mammalian spermatozoa: Comparision with somatic cells. Biol Reprod, 19991; 44: 569-574. [DOI:10.1095/biolreprod44.4.569]
30. Loir M, Lanneau M. Structural function of the basic nuclear proteins in rat spermatids. J Ultrastruct Res 1984; 86:262-272. [DOI:10.1016/S0022-5320(84)90106-0]
31. Corzett M, Mazrimas J, Balhorn R. Protamine 1: protamine 2 stoichiometry in the sperm of eutherian mammals. Mol Reprod Dev 2002; 61:519-527. [DOI:10.1002/mrd.10105]
32. Ward WS, Coffey DS. Specific organization of genes in relation to the sperm nuclear matrix. Biochem Biophy Res Commun 1990; 173:20-25. [DOI:10.1016/S0006-291X(05)81015-0]
33. Carrell DT, Liu L. Altered protamine 2 expression is uncommon in donors of known fertility, but common among men with poor fertilizing capacity, and may reflect other abnormalities of spermiogenesis. Journal of Andrology 2001; 22:604-610.
34. Aoki VW, Liu L, Coarrell DT. Identification and evaluation of a novel sperm protamine abnormality in a population of infertile males. Hum Reprod 2005; 20:1298-1306. [DOI:10.1093/humrep/deh798]
35. Schultz RM, Williams CJ. The science of ART. Science 2002; 296: 2188-2190. [DOI:10.1126/science.1071741]
36. Danan C, Sternberg D, Van Steirteghem A, Cazeneuve C, Duquesnoy P, Besmond C. Evaluation of parental mitochondrial inheritance in neonates born after intracytoplasmic sperm injection. Am J Hum Genet1999; 65:463-473. [DOI:10.1086/302484]
37. Donnelly ET, O'Connell M, McClure N, Lewis S. Differences in nuclear DNA fragmentation and mitochondrial integrity of semen and prepared human spermatozoa.HumReprod2000;15:1552-1561. [DOI:10.1093/humrep/15.7.1552]
38. May-Panloup P, Chretien MF, Savagner F, Vasseur C, Jean M, Malthiery Y. Increased sperm mitochondrial DNA content in male infertility. Hum Reprod 2003; 18: 550-556. [DOI:10.1093/humrep/deg096]
39. Tomsu M, Sharma V, Miller D. Embryo quality and IVF treatment outcomes may correlate with different sperm comet assay parameters. Hum Reprod 2002; 17:1856-1862. [DOI:10.1093/humrep/17.7.1856]
40. Evenson DP, Larson KL, Jost LK. Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Aandrol 2002; 23:25-43. [DOI:10.1002/j.1939-4640.2002.tb02599.x]
41. Bungum M, Humaidan P, Spano M, Jepson k, Bungum l, Giwercman A. The predictive value of sperm chromatin structure assay (SCSA) parameters for the outcome of intrauterine insemination, IVF and ICSI. Hum Reprod 2004; 19:1401-1408. [DOI:10.1093/humrep/deh280]
42. Nagata S. Apoptosis by death factor. Cell 1997; 88:355-365. [DOI:10.1016/S0092-8674(00)81874-7]
43. Vaux, DL, Korsmeyer SJ. Cell death in development. Cell 1999; 96; 245-254. [DOI:10.1016/S0092-8674(00)80564-4]
44. Sinha Hikim AP, Swerdloff RS. Hormonal and genetic control of germ cell apoptosis in the testis. Rev Reprod 1999; 4: 38-47. [DOI:10.1530/ror.0.0040038]
45. Kaufmann SH, Hengartner MO. Programmed cell death: alive and well in the new millennium. Trends in Cellular Biology 2001; 11: 526-534. [DOI:10.1016/S0962-8924(01)02173-0]
46. Høst E, Lindenberg S, Smidt-Jensen S. The role of DNA strand breaks in human spermatozoa used for IVF and ICSI. Acta Obstetricia et Gynecologica Scandinavica 2000; 79: 559-563. [DOI:10.1080/j.1600-0412.2000.079007559.x]
47. Nagata S. Apoptotic DNA fragmentation. Experimental Cell Research 2000; 256: 12-18. [DOI:10.1006/excr.2000.4834]
48. Suda, T, Takahashi T, Goldstein P, Nagata S. Molecular cloning and expression of Fas ligand, a novel member of tumor necrosis factor family.Cell 1993; 75:1169-1178. [DOI:10.1016/0092-8674(93)90326-L]
49. Huszar G, Sbracia M, Vigue L,Miller DJ, Shur BD. Sperm plasma membrane remodelling during spermiogenic maturation in men: relationship among plasma membrane beat 1,4 galactosyltransferase, cytoplasmic creatine phophokinase and creatine phosphokinase isoform ratios. Bio Reprod1997; 56: 1020-1024. [DOI:10.1095/biolreprod56.4.1020]
50. Francavilla S, D'abrizio P, Rucci N, Silvano G, Properzi G, Starface E, et al. Fas and Fas ligand expression in fetal and adult human testis with normal or deranged spermatogenesis. J Clin Endocrinal Metab 2000; 85: 2692-2700. [DOI:10.1210/jcem.85.8.6723]
51. Sakkas D, Moffatt O, Manicardi GC, Mariethoz E, Tarozzi N, Bizzaro D. Nature of DNA damage in ejaculated human spermatozoa and the possible involved of apoptosis. Bi Reprod 2002; 66: 1061-1067. [DOI:10.1095/biolreprod66.4.1061]
52. Paasch U, Grunewald S, Agarwal A, Glandera HJ. Activation pattern of caspases in human spermatozoa. Fertil Steril 2004; 81 (Suppl1 ):802-809. [DOI:10.1016/j.fertnstert.2003.09.030]
53. Kim JM, Ghosh SR, Weil A, Zirkin BR. Caspase-3 and caspase-activated deoxyribonuclease are associated with testicular germ cell apoptosis resulting from reduced intratesticular testosterone. Endocrinilogy 2001; 142: 3809-3816. [DOI:10.1210/endo.142.9.8375]
54. Barkett M, Gilmore T D. Control of apoptosis by Rel/NF-kB transcription factors. Oncogene 1999; 18: 6910-6924. [DOI:10.1038/sj.onc.1203238]
55. Barroso G, Morshedi M, Oehninger S. Analysis of DNA fragmentation, plasma membrane translocation of phosphatidylserine and oxidative stress in human spermatozoa. Human Reproduction 2000; 15: 1338-1344. [DOI:10.1093/humrep/15.6.1338]
56. MacLeod J. The role of oxygen in the metabolism and motility of human spermatozoa. Am J Physiol 1943; 138:512-518. [DOI:10.1152/ajplegacy.1943.138.3.512]
57. Aitken R J. The human spermatozoon - a cell in crisis? The Amoroso Lecture. J Reprod Fertil 1999; 115:1-7. [DOI:10.1530/jrf.0.1150001]
58. Saleh R, Agarwal A. Oxidative stress and male infertility: from research bench to clinical practice. J Androl 2002; 23: 737-752.
59. Pardon OF, Brackett NL, Sharma RK, Kohn S, Lynn CM, Thomas A J, Jrand argawal A. Seminal reactive oxygen species, sperm motility and morphology in men with spinal cord injury. Fertil Ssteril 1997; 67: 115-1120. [DOI:10.1016/S0015-0282(97)81448-3]
60. Duru NK, Morshedi M, Schuffner A, Oehninger S. Semen treatment with progesterone and/or acetyl-L-carnitine does not improve sperm motility or membrane damage after cryopreservation-thawing. Fertil Steril 2000; 74:715-720. [DOI:10.1016/S0015-0282(00)01494-1]
61. Sikka SC. Relative impact of oxidative stress on male reproductive function. Curr Med Chem. 2001; 8:851-862. [DOI:10.2174/0929867013373039]
62. Aitken RJ, Buckingham D, West K. Differential Contribution of leucocytes and spermatozoa to the generation of reactive oxygen species in the ejaculates of oligozoospermic patients and fertile donors. Journal of Reproductive Fertility 1992; 94: 451-62. [DOI:10.1530/jrf.0.0940451]
63. Zini A, de Lamirande E, Gagnon C. Reactive oxygen species in semen of infertile patients: levels of superoxide dismutase- and catalase-like activities in seminal plasma and spermatozoa. International Journal of Andrology 1993; 16:183-188. [DOI:10.1111/j.1365-2605.1993.tb01177.x]
64. Plante M, de Lamirande E, Gagnon C. Reactive oxygen species released by activated neutrophils, but not by deficient spermatozoa are suffieceint to affect normal sperm motility. Fertility and Sterility 1994; 62: 387-393. [DOI:10.1016/S0015-0282(16)56895-2]
65. McKelvey-Martin VJ, Melia N, Walsh IK, Johnston SR, Hughes CM, Lewis SE, Thompson W. Two potential clinical applications of the alkaline single-cell gel electrophoresis assay: (1) human bladder washings and transitional cell carcinoma of the bladder: and (2) human sperm and male infertility. Mutat Res 1997; 375: 93-104. [DOI:10.1016/S0027-5107(97)00005-5]
66. Ostling O, Johanson KJ. Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochem Biophys Res Commun 1984; 123: 291-298. [DOI:10.1016/0006-291X(84)90411-X]
67. Singh NP, McCoy MT, Tice RR, Schneider EL. A simple technique for quantification of low levels of DNA damage in individual cells. Exp Cell Res 1998; 175: 184-191. [DOI:10.1016/0014-4827(88)90265-0]
68. Duty SM, Singh NP, Ryan L. Reliability of the comet assay in cryopreserved human sperm. Human Reproduction 2002; 17:1274-1280. [DOI:10.1093/humrep/17.5.1274]
69. Morris ID, Ilott S, Dixon L, Brison DR. The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) and its relationshipto fertilization and embryo development. Human Reproduction 2002; 17:990-998. [DOI:10.1093/humrep/17.4.990]
70. Abu-Hassan D, Koester F, Schoepper B, Schultze-mosgau, Asimakopoulos B, Diedrich K, Al-hassani S. COMET assay of cumulus cells and spermatozoa DNA status, and the relationship to oocyte fertilization and embryo quality following ICSI. Reproductive BioMedicine Online 2005; 12:447-442. [DOI:10.1016/S1472-6483(10)61997-9]
71. Gorczyca W, Traganos F, Jesionowska H, Darzynkievicz Z. Presence of DNA strand breaks and increased sensitivity of DNA in situ to degeneration in abnormal human sperm cells: analogy to apoptosis of somatic cells. Experimental Cell Research 1993; 207:202-205. [DOI:10.1006/excr.1993.1182]
72. Muratori M, Piomboni P, Baldi E. Functional and ultrastructural features of DNA-fragmented sperm. Journal of Andrology 2000; 21:903-912.
73. 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. Fertility and Sterility1998; 69:529-532. [DOI:10.1016/S0015-0282(97)00536-0]
74. Benchaib M, Braun V, Lornage J, Hadj S, Salle B, Lejeune H, Guerin JF. Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique. Human Reproduction 2003; 18:1023-1028. [DOI:10.1093/humrep/deg228]
75. Sharma RK, Said T, Agarwal A. Sperm DNA damage and its clinical relevance in assessing reproductive outcome. Asian Journal of Andrology 2004; 6:139-148.
76. Drazynkiewicz Z, Traganos F, Sharpless T, Melamed MR. Thermal denaturation of DNA in situ as studied by acridine orange staining and automated cytofluorometry. Exp Cell Res 1975; 90: 411-428. [DOI:10.1016/0014-4827(75)90331-6]
77. Evenson DP, Jost LK, Marshall D, Zinaman MJ, Clegg E, Purvis K, 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 -1049. [DOI:10.1093/humrep/14.4.1039]
78. Spano M, Bonde JP, Hijollund HI, Kolstad HA, Cordelli E, Leter G. Sperm chromatin damage impairs human fertility. Fertility and Sterility 2000; 73:43-50. [DOI:10.1016/S0015-0282(99)00462-8]
79. Duran EH, Gurgan T, Gunalp S, Einginsu ME, YaraliH, Ayhan A. A logistic regression model including DNA status and morphology of spermatozoa for prediction of fertilization in vitro. Hum Reprod 1998; 13; 1235-1239. [DOI:10.1093/humrep/13.5.1235]
80. Fernandez JL, Mouriel L, Rivero MT, Goyanes V, Vasquez R, Alvarez JL. The sperm chromatin dispersion test: a simple method for determination of sperm DNA fragmentation. J Androl 2003; 24: 59-66.
81. Floyd RA, Watson JJ, Harris J, West M, Wong PK. Formation of 8-hydroxy-2-deoxyguanosine, hydroxyl free radical adduct of DNA in granulocytes exposed to the tumor promoter. Biochem Biophys Res Commun1986; 137:841-846. [DOI:10.1016/0006-291X(86)91156-3]
82. Carrell DT, Wilcox AL,Lowy L, Peterson CM, Jones KP, Erickson L, et al. Elevated sperm chromosome aneuploidy and apoptosis in patients with unexplained recurrent pregnancy loss. Obstetrics and Gynecology, 2003; 101:1229-1235. [DOI:10.1016/S0029-7844(03)00339-9]
83. Larson - Cook K, Brannian J, Hansen K, Kasperson K, Aamold E, Evenson D. Relationship between the outcomes of assisted reproductive techniques and sperm DNA fragmentation as measured by the sperm chromatin structure assay. Fertility and Sterility 2003; 80: 895-902. [DOI:10.1016/S0015-0282(03)01116-6]
84. Hǿst E, Lindenberg S, Smidt-Jensen S. The role of DNA strand breaks in human spermatozoa used for IVF and ICSI. Acta Obstetricia et Gynecologica Scandinavica 2000; 79: 559-563. [DOI:10.1080/j.1600-0412.2000.079007559.x]
85. Hǿst E, Lindenberg S, Kahn JA, Christensen F. DNA strand breaks in human sperm cells: A comparison between men with normal and oligozoospermic sperm samples. Acta Obstetricia et Gynecologica Scandinavica 1999; 78: 336-339. [DOI:10.1080/j.1600-0412.1999.780412.x]
86. Huang CC, Lin DP, Tsao HM, Cheng TC, Liu CH, Lee MS. Sperm DNA fragmentation negatively correlates with velocity and fertilization rates, but might not affect pregnancy rates. Fertility and Sterility 2005; 84: 130-140. [DOI:10.1016/j.fertnstert.2004.08.042]
87. Muriel L, Garrido N, Fernandez J L, Alvarez J, Remohi J, Pellicer A, Garrido N. Value of the sperm deoxyribonucleic acid fragmentation level, as measured by the sperm chromatin dispersion test, in the outcome of in vitro fertilization and intracytoplasmic sperm injection. Fertility and Sterility 2006; 85:371-383. [DOI:10.1016/j.fertnstert.2005.07.1327]
88. Payne JF, Raburn DJ, Couchman GM, Price TM, Jamison MG, Walmer DK. Redefining the relationship between sperm deoxyribonucleic acid fragmentation as measured by the sperm chromatin structure assay and outcomes of assisted reproductive techniques. Fertility and Sterility 2005; 84:356-364. [DOI:10.1016/j.fertnstert.2005.02.032]
89. Larson KL, DeJonge CJ, Barnes AM, Jost LK, Evenson DP. Sperm chromatin structure assay parameters as predictors of failed pregnancy following assisted reproductive techniques. Human Reproduction 2000; 15: 1717-1722. [DOI:10.1093/humrep/15.8.1717]
90. Borini A, Tarozzi N, Bizzaro D, Bonu MA, Fava L, Flamigni C, Coticchio G. Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART. Human Reproduction 2006; 21:2876-2881. [DOI:10.1093/humrep/del251]
91. Gandini L, Lombardo F, Paoli D , Caruso F, Eleuteri P, Leter G, et al. Full term pregnancies achieved with ICSI despite high levels of sperm chromatin damage. Human reproduction 2004; 19:1409-1417. [DOI:10.1093/humrep/deh233]
92. Benchaib M, Lornage J, Mazoyer C,Lejeune H, Salle B, Francois Guerin J. Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertility and Sterility 2006; 87:93-100. [DOI:10.1016/j.fertnstert.2006.05.057]
93. 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. Human Reproduction 2005; 20:2032-2033. [DOI:10.1093/humrep/deh815]
94. Li Z, 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; 23:367-376. [DOI:10.1007/s10815-006-9066-9]
95. Tomlinson MJ, Moffatt O, Manicardi GC, Bizzaro D, Afnan M, Sakkas D. Interrelationships between seminal parameters and sperm nuclear DNA damage before and after density gradient centrifugation: implications for assisted conception. Human Reproduction 2001; 16: 2160-2165. [DOI:10.1093/humrep/16.10.2160]
96. Benchaib M, Braun V, Lornage J, Hadj S, Salle B, Lejeune H, Guerin JF. Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique. Human Reproduction 2003; 18(5): 1023-1028. [DOI:10.1093/humrep/deg228]
97. Nasr-Esfahani MH, Salehi M, Razavi S, Anjomshoa M, Rozbahani S, Moulavi F, Mardani M. Effect of sperm DNA damage and sperm protamine deficiency on fertilization and embryo development post-ICSI. Reproductive Biomedicine Online 2005; 11:198-205. [DOI:10.1016/S1472-6483(10)60959-5]
98. Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, Giwercman A. Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Human Reproduction 2007; 22: 174-179. [DOI:10.1093/humrep/del326]
99. Cox GF, Burger J, Lip V, Mau UA, Sperling K, Wu BL, Horsthemke B. Intracytoplasmic sperm injection may increase the risk of imprinting defects. American Journal of Human Genetics 2002; 71:162-164. [DOI:10.1086/341096]
100. Bonduelle M, Legein J, Buysse A , Van Assche E, Wisanto A, Devroey P, et al. Prospective follow up study of 423 children born after intracytoplasmic sperm injection. Human Reproduction 1996; 11:1558-1564. [DOI:10.1093/oxfordjournals.humrep.a019437]
101. Van Steirteghem A. Outcome of assisted reproductive technology. N Engl J Med 1998; 338:194-195. [DOI:10.1056/NEJM199801153380312]
102. Kurinczuk JJ, Bower C. Birth defects in infants conceived by intracytoplasmic sperm injection: an alternative interpretation. British Medical Journal 1997; 315:1260-1265. [DOI:10.1136/bmj.315.7118.1260]
103. Hansen M, Kurinczuk JJ, Bower C, Webb S. The risk of major birth defects after intracytoplasmic sperm injection and in vitro fertilization. N Engl J Med 2002:7; 346:725-730. [DOI:10.1056/NEJMoa010035]
104. Yoshida H. Fertilizability of fresh and frozen human spermatozoa. Nippon Sanka Fujinka Gakkai Zasshi 1991; 43:1233-1240.
105. Watson PF. Recent developments and concepts in cryopreservation of spermatozoa and the assessment of their post-thaw function. Reprod Fertil Dev1995; 7: 871-891. [DOI:10.1071/RD9950871]
106. Brotherton J. Cryopreservation of human semen. Arch Androl 1990; 25:181-195. [DOI:10.3109/01485019008987609]
107. Royere D, Hamamah S, Nicolle JC, Lansac J. Chromatin alterations induced by freeze-thawing influence the fertilizing ability of human sperm. Int J Androl1991;14: 328-332. [DOI:10.1111/j.1365-2605.1991.tb01100.x]
108. Duru NK, Morshedi MS, Schuffner A, Oehninger S. Cryopreservation-Thawing of fractionated human spermatozoa is associated with membrane phosphatidylserine externalization and not DNA fragmentation. Journal of Andrology 2001; 22:646-51.
109. de Paula TS, Bertolla RP, Spaine DM, Cunha MA, Schor N, Cedenho AP. Effect of cryopreservation on sperm apoptotic deoxyribonucleic acid fragmentation in patients with oligozoospermia. Fertility and Sterility 2006; 86:597-600. [DOI:10.1016/j.fertnstert.2006.01.047]
110. Isachenko E, Isachenko V, Katkov II, Rahimi G, Schondorf T, Mallmann P, et al. DNA integrity and motility of human spermatozoa after standard slow freezing versus cryoprotectant-free vitrification. Human Reproduction2004; 19:932-939. [DOI:10.1093/humrep/deh194]
111. Isachenko V, Isachenko E, Katkov II, Montag M, Dessole S, Nawroth F, et al. Cryoprotectant-free cryopreservation of human spermatozoa by vitrification and freezing in vapor: effect on motility, DNA integrity, and fertilization ability. Biol Reprod 2004; 71:1167-1173. [DOI:10.1095/biolreprod.104.028811]

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