Impact of oxidative stress on IVF

Expert Review of Obstetrics and Gynecology

Volumn 3, Issue 4, 2008, Pages 539-554

  Du Plessis, Stefan S ^a   Makker, Kartikeya ^b   Desai, Nisarg R ^b   Agarwal, Ashok ^b  

^a UNIVERSITY OF STELLENBOSCH   (South Africa)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

Antioxidant; Assisted reproductive technology; Embryo; Free radical; IVF; Oocyte; Oxidative stress; Reactive oxygen species; Spermatozoa

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALPHA TOCOPHEROL; AMINO ACID; ANTIOXIDANT; ASCORBIC ACID; CHELATING AGENT; COPPER ZINC SUPEROXIDE DISMUTASE; EXCITATORY AMINO ACID TRANSPORTER 3; FREE RADICAL; HYDROGEN PEROXIDE; HYDROXYL RADICAL; MANGANESE SUPEROXIDE DISMUTASE; MELATONIN; MITOCHONDRIAL DNA; REACTIVE OXYGEN METABOLITE; RETINOL; SCAVENGER; SUPEROXIDE; SUPEROXIDE DISMUTASE;

ACROSOME REACTION; ANTIOXIDANT ACTIVITY; BIRTH DEFECT; CONGENITAL MALFORMATION; CRYOPRESERVATION; CULTURE MEDIUM; DEFENSE MECHANISM; DNA DAMAGE; DNA FRAGMENTATION; EMBRYO CULTURE; EMBRYO DEVELOPMENT; FERTILIZATION IN VITRO; FREEZE THAWING; HUMAN; INTRACYTOPLASMIC SPERM INJECTION; LIGHT; LIPID PEROXIDATION; MALE INFERTILITY; MITOCHONDRIAL MEMBRANE POTENTIAL; NONHUMAN; OVARY FOLLICLE FLUID; OVARY HYPERSTIMULATION; OXIDATIVE PHOSPHORYLATION; OXIDATIVE STRESS; OXYGEN CONCENTRATION; PATHOPHYSIOLOGY; PREGNANCY OUTCOME; PREGNANCY RATE; PRENATAL DIAGNOSIS; REVIEW; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPONTANEOUS ABORTION;

EID: 49149087856     PISSN: 17474108     EISSN: None     Source Type: Journal    
DOI: 10.1586/17474108.3.4.539     Document Type: Review

References (160)

1. Sies H. Strategies of antioxidant defense. Eur. J. Biochem. 215, 213-219 (1993).
2. Spiteller G. Review: on the chemistry of oxidative sttess. J. Lipid Mediat. 7, 199-221 (1993).
3. Aitken RJ, Buckingham DW, West KM. Reactive oxygen species and human spermatozoa:. analysis of the cellular mechanisms involved in luminol- and lucigenin-dependent chemiluminescence. J. Cell. Physiol. 151, 466-477 (1992).
4. Janssen YM, Van Houten B, Borm PJ, Mossman BT. Cell and tissue responses to oxidative damage. Lab. Invest. 69, 261-274 (1993).
5. Agarwal A, Saleh RA, Bedaiwy MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil. Steril. 79, 829-843 (2003).
6. Schafer FQ, Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic. Biol. Med. 30, 1191-1212 (2001).
7. Lennon SV, Martin SJ, Cotter TG. Dose-dependent induction of apoptosis in human tumour cell lines by widely diverging stimuli. Cell Prolif. 24, 203-214 (1991).
8. Valko M, Morris H, Cronin MT. Metals, toxicity and oxidative stress. Curr. Med. Chem. 12, 1161-1208 (2005).
9. Agarwal A, Nallella KP, Allamaneni SS, Said TM. Role of antioxidants in treatment of male infertility: an overview of the literature. Reprod. Biomed. Online 8, 616-627 (2004).
10. 2, a necessary evil for cell signaling. Science 312, 1882-1883 (2006).
11. Ford WC. Reactive oxygen species and sperm. Hum. Fertil. (Camb.) 4, 77-78 (2001).
12. Gagnon C, Iwasaki A, De Lamirande E, Kovalski N. Reactive oxygen species and human spermatozoa. Ann. NY Acad. Sci. 637, 436-444 (1991).
13. Aitken RJ. Molecular mechanisms regulating human sperm function. Mol. Hum. Reprod. 3, 169-173 (1997).
14. Attaran M, Pasqualotto E, Falcone T et al. The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int. J. Fertil. Womens Med. 45, 314-320 (2000).
15. de Lamirande E, Leclerc P, Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol. Hum. Reprod. 3, 175-194 (1997).
16. Sakkas D, Urner F, Bizzaro D et al. Sperm nuclear DNA damage and altered chromatin structure: effect on fertilization and embryo development. Hum. Reprod. 13(Suppl. 4), 11-19 (1998).
17. Agarwal A, Said TM, Bedaiwy MA, Banerjee J, Alvarez JG. Oxidative stress in an assisted reproductive techniques setting. Fertil. Steril. 86, 503-512 (2006).
18. Guerin P, El Mouatassim S, Menezo Y. Oxidative stress and protection against reactive oxygen species in the preimplantation embryo and its surroundings. Hum. Reprod. Update. 7, 175-189 (2001).
19. Goto Y, Noda Y, Mori T, Nakano M. Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic. Biol. Med. 15, 69-75 (1993).
20. Steptoe PC, Edwards RG, Purdy JM. Clinical aspects of pregnancies established with cleaving embryos grown in vitro. Br. J. Obstet. Gynaecol. 87, 757-768 (1980).
21. Taylor C. Antioxidants and reactive oxygen species in human fertility. Environ. Toxicol. Pharmacol. 10, 189-198 (2001).
22. Agarwal A, Allamaneni SS. Role of free radicals in female reproductive diseases and assisted reproduction. Reprod. Biomed. Online 9, 338-347 (2004).
23. Pasqualotto EB, Agarwal A, Sharma RK et al. Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil. Steril. 81, 973-976 (2004).
24. Wiener-Megnazi Z, Vardi L, Lissak A et al. Oxidative stress indices in follicular fluid as measured by the thermochemiluminescence assay correlate with outcome parameters in in vitro fertilization. Fertil. Steril. 82(Suppl. 3), 1171-1176 (2004).
25. Agarwal A, Gupta S, Abdel-Razek H, Krajcir N, Athayde K. Impact of oxidative stress on gametes and embryos in an ART Laboratory. Clin. Embryol. 9, 5-22 (2006).
26. Portz DM, Elkins TE, White R et al. Oxygen free radicals and pelvic adhesion formation: I. Blocking oxygen free radical toxicity to prevent adhesion formation in an endometriosis model. Int. J. Fertil. 36, 39-42 (1991).
27. O'Bryan MK, Zini A, Cheng CY, Schlegel PN. Human sperm endothelial nitric oxide synthase expression: correlation with sperm motility. Fertil. Steril. 70, 1143-1147 (1998).
28. de Lamirande E, Gagnon C. Impact of reactive oxygen species on spermatozoa: a balancing act between beneficial and detrimental effects. Hum. Reprod. 10(Suppl. 1), 15-21 (1995).
29. Agarwal A, Gupta S, Sharma RK. Role of oxidative stress in female reproduction. Reprod. Biol. Endocrinol. 3, 28 (2905).
30. Sikka SC. Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. J. Androl. 25, 5-18 (2004).
31. de Lamirande E, Gagnon C. A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa. Int. J. Androl. 16, 21-25 (1993).
32. Gavella M, Lipovac V. NADH-dependent oxidoreductase (diaphorase) activity and isozyme pattern of sperm in infertile men. Arch. Androl. 28, 135-141 (1992).
33. Plante M, de Lamirande E, Gagnon C. Reactive oxygen species released by activated neutrophils, but not by deficient spermatozoa, are sufficient to affect normal sperm motility. fertil. Steril. 62, 387-393 (1994).
34. Saleh RA, Agarwal A, Nada EA 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. 79(Suppl. 3), 1597-1605 (2003).
35. Gil-Guzman E, Ollero M, Lopez MC et al. Differential production of reactive oxygen species by subsets of human spermatozoa at different stages of maturation. Hum. Reprod. 16, 1922-1930 (2001).
36. Ollero M, Gil-Guzman E, Lopez MC et al. Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum. Reprod. 16, 1912-1921 (2001).
37. Twigg JP, Irvine DS, Aitken RJ. Oxidative damage to DNA in human spermatozoa does not preclude pronucleus formation at intracytoplasmic sperm injection. Hum. Reprod. 13, 1864-1871 (1998).
38. Kemal Duru N, Morshedi M, Oehninger S. Effects of hydrogen peroxide on DNA and plasma membrane integrity of human spermatozoa. Fertil. Steril. 74, 1200-1207 (2000).
39. Aitken RJ, Krausz C. Oxidative stress, DNA damage and the Y chromosome. Reproduction 122, 497-506 (2001).
40. Baker MA, Aitken RJ. Reactive oxygen species in spermatozoa: methods for monitoring and significance for the origins of genetic disease and infertility. Reprod. Biol. Endocrinol. 3, 67 (2005).
41. Wang X, Sharma RK, Gupta A et al. Alterations in mitochondria membrane potential and oxidative stress in infertile men: a prospective observational study. Fertil. Steril. 80(Suppl. 2), 844-850 (2003).
42. Aitken RJ. The Amoroso Lecture. The human spermatozoon - a cell in crisis? J. Reprod. fertil. 115, 1-7 (1999).
43. Esfandiari N, Falcone T, Agarwal A et al. Protein supplementation and the incidence of apoptosis and oxidative stress in mouse embryos. Obstet. Gynecol. 105, 653-660 (2005).
44. Sugino N, Takiguchi S, Kashida S et al. Superoxide dismutase expression in the human corpus luteum during the menstrual cycle and in early pregnancy. Mol. Hum. Reprod. 6, 19-25 (2000).
45. Suzuki T, Sugino N, Fukaya T et al. Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization. Fertil. Steril. 72, 720-726 (1999).
46. Bedaiwy M, Agarwal A, Falcone T et al. Relationship of follicular fluid oxidative stress parameters and outcome of intracytoplasmic sperm injection Fertil. Steril. 84, S250 (2005).
47. Lonergan P, Gutierrez-Adan A, Rizos D et al. Relative messenger RNA abundance in bovine oocytes collected in vitro or in vivo before and 20 hr after the preovulatory luteinizing hormone surge. Mol. Reprod. Dev. 66, 297-305 (2003).
48. Du B, Takahashi K, Ishida GM et al. Usefulness of intraovarian artery pulsatility and resistance indices measurement on the day of follicle aspiration for the assessment of oocyte quality. Fertil. Steril. 85, 366-370 (2006).
49. Chui DK, Pugh ND, Walker SM, Gregory L, Shaw RW. Follicular vascularity - the predictive value of transvaginal power Doppler ultrasonography in an in-vitro fertilization programme: a preliminary study. Hum. Reprod. 12, 191-196 (1997).
50. Van Blerkom J, Antczak M, Schrader R. The developmental potential of the human oocyte is related to the dissolved oxygen content of follicular fluid: association with vascular endothelial growth factor levels and perifollicular blood flow characteristics. Hum. Reprod. 12, 1047-1055 (1997).
51. Choi WJ, Banerjee J, Falcone T et al. Oxidative stress and tumor necrosis factor-α-induced alterations in metaphase II modse oocyte spindle structure. Fertil. Steril. 88, 1220-1231 (2007).
52. Eroglu A, Toth TL, Toner M. Alterations of the cytoskeleton and polyploidy induced by cryopreservation of metaphase II mouse oocytes. Fertil. Steril. 69, 944-957 (1998).
53. Schatten G, Simerly C, Schatten H. Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc. Natl. Acad. Sci. USA 82, 4152-4156 (1985).
54. Seino T, Saito H, Kaneko T et al. Eight-hydroxy-2′-deoxyguanosine in granulosa cells is correlated with the quality of oocytes and embryos in an in vitro fertilization-embryo transfer program. Fertil. Steril. 77, 1184-1190 (2002).
55. Gott AL, Hardy K, Winston RM, Leese HJ. Non-invasive measurement of pyruvate and glucose uptake and lactate production by single human preimplantation embryos. Hum. Reprod. 5, 104-108 (1990).
56. Bedaiwy MA, Falcone T, Mohamed MS et al. Differential growth of human embryos in vitro: role of reactive oxygen species. Fertil. Steril. 82, 593-600 (2004).
57. Jauniaux E, Gulbis B, Burton GJ. Physiological implications of the materno-fetal oxygen gradient in human early pregnancy. Reprod. Biomed. Online 7, 250-253 (2003).
58. Noda Y, Goto Y, Umaoka Y et al. Culture of human embryos in α modification of Eagle's medium under low oxygen tension and low illumination. Fertil. Steril. 62, 1022-1027 (1994).
59. Nasr-Esfahani MH, Winston NJ, Johnson MH. Effects of glucose, glutamine, ethylenediaminetetraacetic acid and oxygen tension on the concentration of reactive oxygen species and on development of the mouse preimplantation embryo in vitro. J. Reprod. Fertil. 96, 219-231 (1992).
60. Orsi NM, Leese HJ. Protection against reactive oxygen species during mouse preimplantation embryo development: role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Mol. Reprod. Dev. 59, 44-53 (2001).
61. Ozawa M, Nagai T. Fahrudin M et al. Addition of glutathione or thioredoxin to culture medium reduces intracellular redox status of porcine IVM/IVF embryos, resulting in improved development to the blastocyst stage. Mol. Reprod. Dev. 73, 998-1007 (2006).
62. Jones D. The role of oxygen concentration in oxidative stress: hypoxic and hyperoxic models. In: Oxidative Stress. Sies H (Ed.). Academic Press, London, UK 151-155 (1985).
63. Maas DH, Storey BT, Mastroianni L Jr. Oxygen tension in the oviduct of the rhesus monkey (Macaca. mulatta). Fertil. Steril. 27, 1312-1317 (1976).
64. Booth PJ, Holm P, Callesen H. The effect of oxygen tension on porcine embryonic development is dependent on embryo type. Theriogenology 63, 2040-2052 (2005).
65. Leoni GG, Rosati I, Succu S et al. A low oxygen atmosphere during IVF accelerates the kinetic of formation of in vitro produced ovine blastocysts. Reprod. Domest. Anim. 42, 299-304 (2007).
66. Morimoto Y, Oku Y, Sonoda M et al. High oxygen atmosphere improves human follicle development in organ cultures of ovarian cortical tissues in vitro. Hum. Reprod. 22, 3170-3177 (2007).
67. Girotti AW. Photosensitized oxidation of membrane lipids: reaction pathways, cytotoxic effects, and cytoprotective mechanisms. J. Photochem. Photobiol. B Biol. 63, 103-113 (2001).
68. Beehler BC, Przybyszewski J, Box HB, Kulesz-Martin MF. Formation of 8-hydroxydeoxyguanosine within DNA of mouse keratinocytes exposed in culture to UVB and H202. Carcinogenesis 13, 2003-2007 (1992).
69. Nakayama T, Noda Y, Goto Y, Mori T. Effects of visible light and other environmental factors on the production of oxygen radicals by hamster embryos. Theriogenology 41, 499-510 (1994).
70. Lampaio F, Strijdom H, Du Plessis S. Reactive oxygen species measurement in human spermatozoa by flow cytometry using the fluorescent probe, 2′,7_m-dichlorofluorescein-diacetate (DCFH-DA). Med. Tech. 20, 7-8 (2006).
71. Rahimi G, Isachenko E, Sauer H et al. Effect of different vitrification protocols for human ovarian tissue on reactive oxygen species and apoprosis. Reprod. Fertil. Dev. 15, 343-349 (2003).
72. Bilodeau JF, Chatterjee S, Sirard MA, Gagnon C. Levels of antioxidant defenses are decreased in bovine spermatozoa after a cycle of freezing and thawing. Mol. Reprod. Dev. 55, 282-288 (2000).
73. Bilodeau J, Chatterjee S, Sirad M et al. Cryopreservation of bovine semen decreases antioxidant defenses in spermatozoa. Biol. Reprod. 60, 102 (1999).
74. Alvarez JG, Storey BT. Evidence for increased lipid peroxidative damage and loss of superoxide dismutase activity as a mode of sublethal cryodamage to human sperm during cryopreservation. J. Androl. 13, 232-241 (1992).
75. Alvarez JG, Storey BT. Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility. Biol. Reprod. 29, 548-555 (1983).
76. Agarwal A, Prabakaran SA. Mechanism, measurement, and prevention of oxidative stress in male reproductive physiology. Indian J. Exp. Biol. 43, 963-974 (2005).
77. Guyader-Joly C, Guerin P, Renard JP et al. Precursors of taurine in female genital tract: effects on developmental capacity of bovine embryo produced in vitro. Amino Acids 15, 27-42 (1998).
78. Gardiner CS, Salmen JJ, Brandt CJ, Stover SK. Glutathione is present in reproductive tract secretions and improves development of mouse embryos after chemically induced glutathione depletion. Biol. Reprod. 59, 431-436 (1998).
79. Takahashi M, Nagai T, Hamano S et al. Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos. Biol. Reprod. 49, 228-232 (1993).
80. Zuelke KA, Jones DP, Perreault SD. Glutathione oxidation is associated with altered microtubule function and disrupted fertilization in mature hamster oocytes. Biol. Reprod. 57, 1413-1419 (1997).
81. Shiotani M, Noda Y, Narimoto K et al. Immunohistochemical localization of superoxide dismutase in the human ovary. Hum. Reprod. 6, 1349-1353 (1991).
82. Li J, Foote RH, Simkin M. Development of rabbit zygotes cultured in protein-free medium with catalase, taurine, or superoxide dismutase. Biol. Reprod. 49, 33-37 (1993).
83. El Mouatassim S, Guerin P, Menezo Y. Expression of genes encoding antioxidant enzymes in human and mouse oocytes during the final stages of maturation. Mol. Hum. Reprod. 5, 720-725 (1999).
84. Cetica PD, Pintos LN, Dalvit GC, Beconi MT. Antioxidant enzyme activity and oxidative stress in bovine oocyte in vitro maturation. IUBMB Life 51, 57-64 (2001).
85. Lee KF, Yeung WS. Gamete/embryo - oviduct interactions: implications on in vitro culture. Hum. Fertil. (Camb.) 9, 137-143 (2006)
86. Yang HW, Hwang KJ, Kwon HC et al. Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum. Reprod. 13, 998-1002 (1998).
87. Agarwal A, Said TM. Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum. Reprod. Update 9, 331-345 (2003).
88. Kowaltowski AJ, Vercesi AE. Mitochondrial damage induced by conditions of oxidative stress. Free Radic. Biol. Med. 26, 463-471 (1999).
89. Braude P, Bolton V, Moore S. Human gene expression first occurs between the four- and eight-cell stages of preimplantation development. Nature 332, 459-461 (1988).
90. 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, 611-615 (2004).
91. Blondin P, Coenen K, Sirard MA. The impact of reactive oxygen species on bovine sperm fertilizing ability and oocyte maturation. J. Androl. 18, 454-460 (1997).
92. Harvey AJ, Kind KL, Thompson JG. REDOX regulation of early embryo development. Reproduction 123, 479-486 (2002).
93. Kwon HC, Yang HW, Hwang KJ et al. Effects of low oxygen condition on the generation of reactive oxygen species and the development in mouse embryos cultured in vitro. J. Obstet. Gynaecol. Res. 25, 359-366 (1999).
94. Pierce GB, Parchment RE, Lewellyn AL. Hydrogen peroxide as a mediator of programmed cell death in the blastocyst. Differentiation 46, 181-186 (1991).
95. Kitagawa Y, Suzuki K, Yoneda A, Watanabe T. Effects of oxygen concentration and antioxidants on the in vitro developmental ability, production of reactive oxygen species (ROS), and DNA fragmentation in porcine embryos. Theriogenology 62, 1186-1197 (2004).
96. Jurisicova A, Varmuza S, Casper RF. Programmed cell death and human embryo fragmentation. Mol. Hum. Reprod. 2, 93-98 (1996).
97. Nasr-Esfahani MH, Aitken JR, Johnson MH. Hydrogen peroxide levels in mouse oocytes and early cleavage stage embryos developed in vitro or in vivo. Development 109, 501-507 (1990).
98. Goto Y, Noda Y, Narimoto K, Umaoka Y, Mori T. Oxidative stress on mouse embryo development in vitro. Free Radir. Biol. Med. 13, 47-53 (1992).
99. Harvey AJ, Kind KL, Thompson JG. Effect of the oxidative phosphorylation uncoupler 2,4-dinitrophenol on hypoxia-inducible factor-regulated gene expression in bovine blastocysts. Reprod. Fertil. Dev. 16, 665-673 (2004).
100. Nasr-Esfahani MM, Johnson MH. The origin of reactive oxygen species in mouse embryos cultured in vitro. Development 113, 551-560 (1991).
101. Goyanes VJ, Ron-Corzo A, Costas E, Maneiro E. Morphometric categorization of the human oocyte and early conceptus. Hum. Reprod. 5, 613-618 (1990).
102. Plachot M, Mandelbaum J. Oocyte maturation, fertilization and embryonic growth in vitro. Br. Med. Bull. 46, 675-694 (1990).
103. Erenus M, Zouves C, Rajamahendran P et al. The effect of embryo quality on subsequent pregnancy rates after in vitro fertilization. Fertil. Steril. 56, 707-710 (1991).
104. Hyslop PA, Hinshaw DB, Halsey WA Jr et al. Mechanisms of oxidant-mediated cell injury. The glycolytic and mitochondrial pathways of ADP phosphorylation are major intracellular targets inactivated by hydrogen peroxide. J. Biol. Chem. 263, 1665-1675 (1988).
105. Duran EH, Morshedi M, Taylor S, Oehninger S. Sperm DNA quality predicts intrauterine insemination outcome: a prospective cohort study. Hum. Reprod. 17, 3122-3128 (2002).
106. Simpson JL, Lamb DJ. Genetic effects of intracytoplasmic sperm injection. Semin. Reprod. Med. 19, 239-249 (2001).
107. Bedaiwy MA, Goldberg JM, Falcone T et al. Relationship between oxidative stress and embryotoxicity of hydrosalpingeal fluid. Hum. Reprod. 17, 601-604 (2002).
108. Turner TT. De Graaf's thread: the human epididymis. J. Androl. 29, 237-250 (2008).
109. Greco E, Scarselli F, Iacobelli M et al. Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Hum. Reprod. 20, 226-230 (2005).
110. Greco E, Iacobelli M, Rienzi L et al. Reduction of the incidence of sperm DNA fragmentation by oral antioxidant treatment. J. Androl. 26, 349-353 (2005).
111. Sharma RK, Said T, Agarwal A. Sperm DNA damage and its clinical relevance in assessing reproductive outcome. Asian J. Androl. 6, 139-148 (2004).
112. Agarwal A, Allamaneni SS, Nallella KP, George AT, Mascha E. Correlation of reactive oxygen species levels with the fertilization rate after in vitro fertilization: a qualified meta-analysis. Fertil. Steril. 84, 228-231 (2005).
113. Sakkas D, Percival G, D'Arcy Y, Sharif K, Afnan M. Assessment of early cleaving in vitro fertilized human embryos at the 2-cell stage before transfer improves embryo selection. Fertil. Steril. 76, 1150-1156 (2001).
114. Sun JG, Jurisicova A, Casper RF. Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol. Reprod. 56, 602-607 (1997).
115. +7 by microarray technology. Mol. Hum. Reprod. 9, 253-264 (2003).
116. Aitken RJ, Baker MA. Oxidative stress and male reproductive biology. Reprod. Fertil. Dev. 16, 581-588 (2004).
117. 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. 2, 613-619 (1996).
118. Kodama H, Yamaguchi R, Fukuda J, Kasai H, Tanaka T. Increased oxidative deoxyribonucleic acid damage in the spermatozoa of infertile male patients. fertil. Steril. 68, 519-524 (1997).
119. Aitken RJ, Baker MA, Sawyer D. Oxidative stress in the male germ line and its role in the aetiology of male infertility and genetic disease. Reprod. Biomed. Online 7, 65-70 (2003).
120. Olsen AK, Lindeman B, Wiger R, Duale N, Brunborg G. How do male germ cells handle DNA damage? Toxicol. Appl. Pharmacol. 207, 521-531 (2005).
121. Lewis SE, Aitken RJ. DNA damage to spermatozoa has impacts on fertilization and pregnancy. Cell Tissue Res. 322, 33-41 (2005).
122. Erenpreiss J, Spano M, Erenpreisa J, Bungum M, Giwercman A. Sperm chromatin structure and male fertility: biological and clinical aspects. Asian J. Androl. 8, 11-29 (2006).
123. 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. 346, 725-730 (2002).
124. Van Steirteghem A, Bonduelle M, Liebaers I, Devroey P. Children born after assisted reproductive technology. Am. J. Perinatol. 19, 59-65 (2002).
125. Van Steirteghem A. Bonduelle M, Devroey P, Liebaers I. Follow-up of children born after ICSI. Hum. Reprod. Update 8, 111-116 (2002).
126. Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol. Reprod. 62, 1526-1535 (2000).
127. Young LE, Fernandes K, McEvoy TG et al. Epigenetic change in IGF2R is associated with fetal overgrowth after sheep embryo culture. Nat. Genet. 27, 153-154 (2001).
128. DeBaun MR, Niemitz EL, Feinberg AP. Association of in vitro fertilization with Beckwith-Wiedemann syndrome and epigenetic alterations of LIT1 and H19. Am. J. Hum. Genet. 72, 156-160 (2003).
129. Gicquel C, Gaston V, Mandelbaum J et al. In vitro fertilization may increase the risk of Beckwith-Wiedemann syndrome related to the abnormal imprinting of the KCN1OT gene. Am. J. Hum. Genet. 72, 1338-1341 (2003).
130. Halliday J, Oke K, Breheny S, Algar E, Armor D. Beckwith-Wedemann syndrome and IVF: a case-control study. Am. J. Hum. Genet. 75, 526-528 (2004).
131. Orstavik KH. Intracytoplasmic sperm injection and congenital syndromes because of imprinting defects. Tidsskr. Nor. Laegeforen 123, 177 (2003).
132. Cox GF, Burger J, Lip V et al. Intracytoplasmic sperm injection may increase the risk of imprinting defects. Am. J. Hum. Genet. 71, 162-164 (2002).
133. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308, 1466-1469 (2005).
134. Aitken RJ, Sawyer D. The human spermatozoon - not waving but drowning. Adv. Exp. Med. Biol. 518, 85-98 (2003).
135. Henkel RR, Schill WB. Sperm preparation for ART. Reprod. Biol. Endocrinol. 1, 108 (2003).
136. Grunewald S, Miska W, Miska G et al. Molecular glass wool filtration as a new tool for sperm preparation. Hum. Reprod. 22, 1405-1412 (2007).
137. Paasch U, Grunewald S, Glander HJ. Sperm selection in assisted reproductive techniques. Soc. Reprod. Fertil. Suppl. 65, 515-525 (2007).
138. Miltenyi S, Muller W, Weichel W, Radbruch A. High gradient magnetic cell separation with MACS. Cytometry 11, 231-238 (1990).
139. Hipler UC, Schreiber G, Wollina U. Reactive oxygen species in human semen: investigations and measurements. Arch. Androl. 40, 67-78 (1998).
140. Said T, Agarwal A, Zborowski M et al. Utility of magnetic cell separation as a molecular sperm preparation technique. J. Androl. 29, 134-142 (2008).
141. Okada H, Tatsumi N, Kanzaki M et al. Formation of reactive oxygen species by spermatozoa from asthenospermic patients: response to treatment with pentoxifylline. J. Urol. 157, 2140-2146 (1997).
142. Lenzi A, Picardo M, Gandini L et al. Glutathione treatment of dyspermia: effect on the lipoperoxidation process. Hum. Reprod. 9, 2044-2050 (1994).
143. Zalata AA, Ahmed AH, Allamaneni SS, Comhaire FH, Agarwal A. Relationship between acrosin activity of human spermatozoa and oxidative stress. Asian J. Androl. 6, 313-318 (2004).
144. Zhang X, Sharma RK, Agarwal A, Falcone T. Effect of pentoxifylline in reducing oxidative stress-induced embryotoxicity. J. Assist. Reprod. Genet. 22, 415-417 (2005).
145. Parinaud J, Le Lannou D, Vieitez G et al. Enhancement of motility by treating spermatozoa with an antioxidant solution (Sperm-Fit) following ejaculation. Hum. Reprod. 12, 2434-036 (1997).
146. Lane M, Maybach JM, Gardner DK. Addition of ascorbate during cryopreservation stimulates subsequent embryo development. Hum. Reprod. 17, 2686-2693 (2002).
147. Luck MR, Jeyaseelan I, Scholes RA. Ascorbic acid and fertility. Biol. Reprod. 52, 262-266 (1995).
148. Ford W, Whittington K. Debate: is antioxidant therapy a promising strategy to improve human reproduction? Antioxidant therapy for male subfertility: a promise that remains unfulfilled. Hum. Reprod. Update 13, 1416 (1998).
149. Dawson EB, Harris WA, Teter MC, Powell LC. Effect of ascorbic acid supplementation on the sperm quality of smokers. Fertil. Steril. 58, 1034-1039 (1992).
150. Lenzi A, Culasso F, Gandini L, Lombardo F, Dondero F. Placebo-controlled, double-blind, cross-over trial of glutathione therapy in male infertility. Hum. Reprod. 8, 1657-1662 (1993).
151. Vicari E, Calogero AE. Effects of treatment with carnitines in infertile patients with prostato-vesiculo-epididymitis. Hum. Reprod. 16, 2338-2342 (2001).
152. Rolf C, Cooper TG, Yeung CH, Nieschlag E. Antioxidant treatment of patients with asthenozoospermia or moderate oligoasthenozoospermia with high-dose vitamin C and vitamin E: a randomized, placebo-controlled, double-blind study. Hum. Reprod. 14, 1028-1033 (1999).
153. Tamura H, Takasaki A, Miwa I et al. Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J. Pineal Res. 44, 280-287 (2008).
154. Cocuzza M, Agarwal A. Nonsurgical treatment of male infertility: specific and empiric therapy. Biol. Targets Ther. 1, 259-269 (2007).
155. Watson AJ, Watson PH, Warnes D et al. Preimplantation development of in vitro-matured and in vitro-fertilized ovine zygotes: comparison between coculture on oviduct epithelial cell monolayers and culture under low oxygen atmosphere. Biol. Reprod. 50, 715-724 (1994).
156. Gianaroli L, Fiorentino A, Magli MC, Ferraretti AP, Montanaro N. Prolonged sperm-oocyte exposure and high sperm concentration affect human embryo viability and pregnancy rate. Hum. Reprod. 11, 2507-2511 (1996).
157. Kattera S, Chen C. Short coincubation of gametes in in vitro fertilization improves implantation and pregnancy rates: a prospective, randomized, controlled study. Fertil. Steril. 80, 1017-1021 (2003).
158. Borini A, Lagalla C, Sciajno R et al. Artificial reproductive technology achievements for optimizing embryo quality. Ann. NY Acad. Sci. 1034, 252-261 (2004).
159. Gómez E, Rodríguez A, Muñoz M et al. Serum free embryo culture medium improves in vitro survival of bovine blastocysts to vitrification. Theriogenology 69, 1013-1021 (2008).
160. Mercader A, Valbuena D, Simón C. Human embryo culture. Methods Enzymol. 420, 3-18 (2006).