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64 - The Impact of Oxidative Stress on Female Reproduction and ART: An Evidence-Based Review

from PART III - ASSISTED REPRODUCTION

Published online by Cambridge University Press:  04 August 2010

By
Sajal Gupta ,
Lucky Sekhon ,
Nabil Aziz  and
Ashok Agarwal
Edited by
Botros R. M. B. Rizk ,
Juan A. Garcia-Velasco ,
Hassan N. Sallam  and
Antonis Makrigiannakis
Botros R. M. B. Rizk
Affiliation:
University of South Alabama
Juan A. Garcia-Velasco
Affiliation:
Rey Juan Carlos University School of Medicine,
Hassan N. Sallam
Affiliation:
University of Alexandria School of Medicine
Antonis Makrigiannakis
Affiliation:
University of Crete
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Summary

INTRODUCTION

Aerobic metabolism is associated with the generation of pro-oxidant molecules called free radicals or reactive oxygen species (ROS) that include the hydroxyl radicals, superoxide anion, hydrogen peroxide, and nitric oxide. There is a complex interaction of the pro-oxidants and antioxidants, resulting in the maintenance of the intracellular homeostasis. Whenever there is an imbalance between the pro-oxidants and antioxidants, a state of oxidative stress (OS) is initiated.

OVERVIEW OF OS AND ROS

Under normal conditions, paired electrons create stable bonds in biomolecules. However, if the bond is weak, it might break, leading to the formation of free radicals. Free radicals are defined as any species with one or more unpaired electrons in the outer orbit that include ROS such as superoxide, hydrogen peroxide, hydroxyl, and singlet oxygen radicals. They are generally very small molecules and are highly reactive due to the presence of unpaired valence shell electrons, initiating a cascade of reactions of more free radicals leading to uncontrolled chain reactions (1). Free radicals such as the superoxide radical are formed when high-energy electrons leak from the electron transport chain. The dismutation of superoxide results in the formation of hydrogen peroxide. The hydroxyl ion is a major type of ROS that is highly reactive, having the ability to modify purine and pyrimidines and cause damaging DNA strand breaks (2,3).

ROS are formed endogenously as a natural byproduct of aerobic metabolism and through the activity of various metabolic pathways and enzymes of oocytes and embryos.

Keywords

assisted reproductive technologyfemale infertilityfolliculogenesisin vitro fertilizationovarian steroidogenesisoocyte maturationoxidative stressluteolysispregnancyreactive oxygen species
Type
Chapter
Information
Infertility and Assisted Reproduction , pp. 629 - 642
Publisher: Cambridge University Press
Print publication year: 2008

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References

Gupta, S, Agarwal, A, Krajcir, N, Alvarez, JG. Role of oxidative stress in endometriosis. Reprod Biomed Online 2006;13(1):126–34.CrossRefGoogle ScholarPubMed
Agarwal, A, Gupta, S, Sharma, R. Oxidative stress and its implications in female infertility — a clinician's perspective. Reprod Biomed Online 2005;11(5):641–50.CrossRefGoogle ScholarPubMed
Agarwal, A, Gupta, S, Sharma, RK. Role of oxidative stress in female reproduction. Reprod Biol Endocrinol 2005;3:28.CrossRefGoogle ScholarPubMed
Wang, X, Falcone, T, Attaran, M, Goldberg, JM, Agarwal, A, Sharma, RK. Vitamin C and vitamin E supplementation reduce oxidative stress-induced embryo toxicity and improve the blastocyst development rate. Fertil Steril 2002;78(6):1272–7.CrossRefGoogle ScholarPubMed
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 2000;45(5):314–20.Google ScholarPubMed
Agarwal, A, Saleh, RA, Bedaiwy, MA. Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 2003;79(4):829–43.CrossRefGoogle ScholarPubMed
Sharma, A. Role of reactive oxygen species in gynecologic diseases. Reprod Med Biol 2004;3:177–99.CrossRefGoogle ScholarPubMed
Agarwal, A, Allamaneni, SS. Role of free radicals in female reproductive diseases and assisted reproduction. Reprod Biomed Online 2004;9(3):338–47.CrossRefGoogle ScholarPubMed
Agarwal, A, Gupta, S, Sikka, S. The role of free radicals and antioxidants in reproduction. Curr Opin Obstet Gynecol 2006;18(3):325–32.CrossRefGoogle ScholarPubMed
Wang, Y, Sharma, RK, Falcone, T, Goldberg, J, Agarwal, A. Importance of reactive oxygen species in the peritoneal fluid of women with endometriosis or idiopathic infertility. Fertil Steril 1997; 68(5):826–30.CrossRefGoogle ScholarPubMed
Du, B, Takahashi, K, Ishida, GM, Nakahara, K, Saito, H, Kurachi, H. Usefulness of intraovarian artery pulsatility and resistance indices measurement on the day of follicle aspiration for the assessment of oocyte quality. Fertil Steril 2006;85(2):366–70.CrossRefGoogle ScholarPubMed
Rosselli, M, Keller, PJ, Dubey, RK. Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. Hum Reprod Update 1998;4(1):3–24.CrossRefGoogle ScholarPubMed
Lee, TH, Wu, MY, Chen, MJ, Chao, KH, Ho, HN, Yang, YS. Nitric oxide is associated with poor embryo quality and pregnancy outcome in in vitro fertilization cycles. Fertil Steril 2004;82(1):126–31.CrossRefGoogle ScholarPubMed
Manau, D, Balasch, J, Jimenez, W, et al. Follicular fluid concentrations of adrenomedullin, vascular endothelial growth factor and nitric oxide in IVF cycles: relationship to ovarian response. Hum Reprod 2000;15(6):1295–9.CrossRefGoogle ScholarPubMed
Suzuki, T, Sugino, N, Fukaya, T, et al. Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization. Fertil Steril 1999;72(4):720–6.CrossRefGoogle ScholarPubMed
Tamate, K, Sengoku, K, Ishikawa, M. The role of superoxide dismutase in the human ovary and fallopian tube. J Obstet Gynaecol 1995;21(4):401–9.CrossRefGoogle ScholarPubMed
Jozwik, M, Wolczynski, S, Szamatowicz, M. Oxidative stress markers in preovulatory follicular fluid in humans. Mol Hum Reprod 1999;5(5):409–13.CrossRefGoogle ScholarPubMed
Sugino, N, Takiguchi, S, Kashida, S, Karube, A, Nakamura, Y, Kato, H. Superoxide dismutase expression in the human corpus luteum during the menstrual cycle and in early pregnancy. Mol Hum Reprod 2000;6(1):19–25.CrossRefGoogle ScholarPubMed
Aten, RF, Duarte, KM, Behrman, HR. Regulation of ovarian antioxidant vitamins, reduced glutathione, and lipid peroxidation by luteinizing hormone and prostaglandin F2 alpha. Biol Reprod 1992;46(3):401–7.CrossRefGoogle ScholarPubMed
Briggs, DA, Sharp, DJ, Miller, D, Gosden, RG. Transferrin in the developing ovarian follicle: evidence for de-novo expression by granulosa cells. Mol Hum Reprod 1999;5(12):1107–14.CrossRefGoogle ScholarPubMed
Sugino, N, Karube-Harada, A, Taketani, T, Sakata, A, Nakamura, Y. Withdrawal of ovarian steroids stimulates prostaglandin F2alpha production through nuclear factor-kappaB activation via oxygen radicals in human endometrial stromal cells: potential relevance to menstruation. J Reprod Dev 2004;50(2):215–25.CrossRefGoogle ScholarPubMed
Ota, H, Igarashi, S, Hatazawa, J, Tanaka, T. Endothelial nitric oxide synthase in the endometrium during the menstrual cycle in patients with endometriosis and adenomyosis. Fertil Steril 1998;69(2):303–8.CrossRefGoogle ScholarPubMed
Tseng, L, Zhang, J, Peresleni, T, Goligorsky, MS. Cyclic expression of endothelial nitric oxide synthase mRNA in the epithelial glands of human endometrium. J Soc Gynecol Investig 1996;3(1):33–8.CrossRefGoogle ScholarPubMed
Park, JK, Song, M, Dominguez, CE, et al. Glycodelin mediates the increase in vascular endothelial growth factor in response to oxidative stress in the endometrium. Am J Obstet Gynecol 2006;195(6):1772–7.CrossRefGoogle ScholarPubMed
Hickey, M, Krikun, G, Kodaman, P, Schatz, F, Carati, C, Lockwood, CJ. Long-term progestin-only contraceptives result in reduced endometrial blood flow and oxidative stress. J Clin Endocrinol Metab 2006;91(9):3633–8.CrossRefGoogle ScholarPubMed
Iborra, A, Palacio, JR, Martinez, P. Oxidative stress and autoimmune response in the infertile woman. Chem Immunol Allergy 2005;88:150–62.Google ScholarPubMed
Agarwal, A, Said, TM, Bedaiwy, MA, Banerjee, J, Alvarez, JG. Oxidative stress in an assisted reproductive techniques setting. Fertil Steril 2006;86(3):503–12.CrossRefGoogle Scholar
Zeller, JM, Henig, I, Radwanska, E, Dmowski, WP. Enhancement of human monocyte and peritoneal macrophage chemiluminescence activities in women with endometriosis. Am J Reprod Immunol Microbiol 1987;13(3):78–82.CrossRefGoogle ScholarPubMed
Alpay, Z, Saed, GM, Diamond, MP. Female infertility and free radicals: potential role in adhesions and endometriosis. J Soc Gynecol Investig 2006;13(6):390–8.CrossRefGoogle ScholarPubMed
Reubinoff, BE, Har-El, R, Kitrossky, N, et al. Increased levels of redox-active iron in follicular fluid: a possible cause of free radical-mediated infertility in beta-thalassemia major. Am J Obstet Gynecol 1996;174(3):914–18.CrossRefGoogle ScholarPubMed
Arumugam, K, Yip, YC. De novo formation of adhesions in endometriosis: the role of iron and free radical reactions. Fertil Steril 1995;64(1):62–4.Google ScholarPubMed
Murphy, AA, Palinski, W, Rankin, S, Morales, AJ, Parthasarathy, S. Evidence for oxidatively modified lipid-protein complexes in endometrium and endometriosis. Fertil Steril 1998;69(6):1092–4.CrossRefGoogle ScholarPubMed
Donnez, J, Langendonckt, A, Casanas-Roux, F, et al. Current thinking on the pathogenesis of endometriosis. Gynecol Obstet Invest 2002;54 (Suppl. 1):52–8; discussion 9–62.CrossRefGoogle ScholarPubMed
Murphy, AA, Palinski, W, Rankin, S, Morales, AJ, Parthasarathy, S. Macrophage scavenger receptor(s) and oxidatively modified proteins in endometriosis. Fertil Steril 1998;69(6):1085–91.CrossRefGoogle ScholarPubMed
Jackson, LW, Schisterman, EF, Dey-Rao, R, Browne, R, Armstrong, D. Oxidative stress and endometriosis. Hum Reprod 2005;20(7): 2014–20.CrossRefGoogle ScholarPubMed
Polak, G, Koziol-Montewka, M, Gogacz, M, Blaszkowska, I, Kotarski, J. Total antioxidant status of peritoneal fluid in infertile women. Eur J Obstet Gynecol Reprod Biol 2001;94(2):261–3.CrossRefGoogle ScholarPubMed
Szczepanska, M, Kozlik, J, Skrzypczak, J, Mikolajczyk, M. Oxidative stress may be a piece in the endometriosis puzzle. Fertil Steril 2003;79(6):1288–93.CrossRefGoogle ScholarPubMed
Ho, HN, Wu, MY, Chen, SU, Chao, KH, Chen, CD, Yang, YS. Total antioxidant status and nitric oxide do not increase in peritoneal fluids from women with endometriosis. Hum Reprod 1997;12(12):2810–15.CrossRefGoogle Scholar
Wu, Y, Kajdacsy-Balla, A, Strawn, E, et al. Transcriptional characterizations of differences between eutopic and ectopic endometrium. Endocrinology 2006;147(1):232–46.CrossRefGoogle ScholarPubMed
Bedaiwy, MA, Falcone, T, Sharma, RK, et al. Prediction of endometriosis with serum and peritoneal fluid markers: a prospective controlled trial. Hum Reprod 2002;17(2):426–31.CrossRefGoogle ScholarPubMed
Bedaiwy, MA, Falcone, T. Peritoneal fluid environment in endometriosis. Clinicopathological implications. Minerva Ginecol 2003;55(4):333–45.Google ScholarPubMed
Said, TM, Agarwal, A, Falcone, T, Sharma, RK, Bedaiwy, MA, Li, L. Infliximab may reverse the toxic effects induced by tumor necrosis factor alpha in human spermatozoa: an in vitro model. Fertil Steril 2005;83(6):1665–73.CrossRefGoogle ScholarPubMed
Zhang, X, Sharma, RK, Agarwal, A, Falcone, T. Effect of pentoxifylline in reducing oxidative stress-induced embryotoxicity. J Assist Reprod Genet 2005;22(11–12):415–17.CrossRefGoogle ScholarPubMed
Strandell, A, Lindhard, A, Waldenstrom, U, Thorburn, J. Hydrosalpinx and IVF outcome: cumulative results after salpingectomy in a randomized controlled trial. Hum Reprod 2001;16(11):2403–10.CrossRefGoogle Scholar
Strandell, A, Lindhard, A. Why does hydrosalpinx reduce fertility? The importance of hydrosalpinx fluid. Hum Reprod 2002;17(5):1141–5.CrossRefGoogle ScholarPubMed
Bedaiwy, MA, Falcone, T, Mohamed, MS, et al. Differential growth of human embryos in vitro: role of reactive oxygen species. Fertil Steril 2004;82(3):593–600.CrossRefGoogle ScholarPubMed
Okatani, Y, Morioka, N, Wakatsuki, A, Nakano, Y, Sagara, Y. Role of the free radical-scavenger system in aromatase activity of the human ovary. Horm Res 1993;39 (Suppl. 1):22–7.CrossRefGoogle ScholarPubMed
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 2004;82 (Suppl. 3):1171–6.CrossRefGoogle ScholarPubMed
Tarin, JJ. Potential effects of age-associated oxidative stress on mammalian oocytes/embryos. Mol Hum Reprod 1996;2(10):717–24.CrossRefGoogle ScholarPubMed
Takahashi, T, Takahashi, E, Igarashi, H, Tezuka, N, Kurachi, H. Impact of oxidative stress in aged mouse oocytes on calcium oscillations at fertilization. Mol Reprod Dev 2003;66(2):143–52.CrossRefGoogle ScholarPubMed
Tatone, C, Carbone, MC, Falone, S, et al. Age-dependent changes in the expression of superoxide dismutases and catalase are associated with ultrastructural modifications in human granulosa cells. Mol Hum Reprod 2006;12(11):655–60.CrossRefGoogle ScholarPubMed
Steele, EK, McClure, N, Maxwell, RJ, Lewis, SE. A comparison of DNA damage in testicular and proximal epididymal spermatozoa in obstructive azoospermia. Mol Hum Reprod 1999;5(9):831–5.CrossRefGoogle ScholarPubMed
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 2001;16(9):1912–21.CrossRefGoogle ScholarPubMed
Dalzell, LH, McVicar, CM, McClure, N, Lutton, D, Lewis, SE. Effects of short and long incubations on DNA fragmentation of testicular sperm. Fertil Steril 2004;82(5):1443–5.CrossRefGoogle Scholar
Alvarez, JG. Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular sperm. Hum Reprod 2005;20(7):2031–2; author reply 2–3.CrossRefGoogle Scholar
Alvarez, JG. The predictive value of sperm chromatin structure assay. Hum Reprod 2005;20(8):2365–7.CrossRefGoogle ScholarPubMed
Suganuma, R, Yanagimachi, R, Meistrich, ML. Decline in fertility of mouse sperm with abnormal chromatin during epididymal passage as revealed by ICSI. Hum Reprod 2005;20(11):3101–8.CrossRefGoogle ScholarPubMed
Fraga, CG, Motchnik, PA, Shigenaga, MK, Helbock, HJ, Jacob, RA, Ames, BN. Ascorbic acid protects against endogenous oxidative DNA damage in human sperm. Proc Natl Acad Sci USA 1991;88(24):11003–6.CrossRefGoogle ScholarPubMed
Carrell, DT, Liu, L, Peterson, CM, et al. Sperm DNA fragmentation is increased in couples with unexplained recurrent pregnancy loss. Arch Androl 2003;49(1):49–55.CrossRefGoogle ScholarPubMed
Alvarez, JG. DNA fragmentation in human spermatozoa: significance in the diagnosis and treatment of infertility. Minerva Ginecol 2003;55(3):233–9.Google ScholarPubMed
Rubes, J, Selevan, SG, Evenson, DP, et al. Episodic air pollution is associated with increased DNA fragmentation in human sperm without other changes in semen quality. Hum Reprod 2005;20(10):2776–83.CrossRefGoogle ScholarPubMed
Young, TW, Mei, FC, Yang, G, Thompson-Lanza, JA, Liu, J, Cheng, X. Activation of antioxidant pathways in ras-mediated oncogenic transformation of human surface ovarian epithelial cells revealed by functional proteomics and mass spectrometry. Cancer Res 2004;64(13):4577–84.CrossRefGoogle ScholarPubMed
Egozcue, J, Sarrate, Z, Codina-Pascual, M, et al. Meiotic abnormalities in infertile males. Cytogenet Genome Res 2005;111(3–4):337–42.CrossRefGoogle ScholarPubMed
Oyawoye, O, Abdel Gadir, A, Garner, A, Constantinovici, N, Perrett, C, Hardiman, P. Antioxidants and reactive oxygen species in follicular fluid of women undergoing IVF: relationship to outcome. Hum Reprod 2003;18(11):2270–4.CrossRefGoogle Scholar
Paszkowski, T, Clarke, RN, Hornstein, MD. Smoking induces oxidative stress inside the Graafian follicle. Hum Reprod 2002;17(4):921–5.CrossRefGoogle ScholarPubMed
Pasqualotto, EB, Agarwal, A, Sharma, RK, et al. Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril 2004;81(4):973–6.CrossRefGoogle ScholarPubMed
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 1997;12(5):1047–55.CrossRefGoogle ScholarPubMed
Yang, HW, Hwang, KJ, Kwon, HC, Kim, HS, Choi, KW, Oh, KS. Detection of reactive oxygen species (ROS) and apoptosis in human fragmented embryos. Hum Reprod 1998;13(4):998–1002.CrossRefGoogle ScholarPubMed
Kurzawa, R, Glabowski, W, Baczkowski, T, Wiszniewska, B, Marchlewicz, M. Growth factors protect in vitro cultured embryos from the consequences of oxidative stress. Zygote 2004;12(3):231–40.CrossRefGoogle ScholarPubMed
Ebisch, IM, Peters, WH, Thomas, CM, Wetzels, AM, Peer, PG, Steegers-Theunissen, RP. Homocysteine, glutathione and related thiols affect fertility parameters in the (sub)fertile couple. Hum Reprod 2006;21(7):1725–33.CrossRefGoogle ScholarPubMed
Das, S, Chattopadhyay, R, Ghosh, S, et al. Reactive oxygen species level in follicular fluid — embryo quality marker in IVF?Hum Reprod 2006;21(9):2403–7.CrossRefGoogle ScholarPubMed
Seino, T, Saito, H, Kaneko, T, Takahashi, T, Kawachiya, S, Kurachi, H. 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 2002;77(6):1184–90.CrossRefGoogle Scholar
Paszkowski, T, Traub, AI, Robinson, SY, McMaster, D. Selenium dependent glutathione peroxidase activity in human follicular fluid. Clin Chim Acta 1995;236(2):173–80.CrossRefGoogle ScholarPubMed
Bedaiwy, M, Agarwal, A, Said, TM, et al. Role of total antioxidant capacity in the differential growth of human embryos in vitro. Fertil Steril 2006;86(2):304–9.CrossRefGoogle ScholarPubMed
Ferda Verit, F, Erel, O, Kocyigit, A. Association of increased total antioxidant capacity and anovulation in nonobese infertile patients with clomiphene citrate-resistant polycystic ovary syndrome. Fertil Steril 2007.Google Scholar
Sabatini, L, Wilson, C, Lower, A, Al-Shawaf, T, Grudzinskas, JG. Superoxide dismutase activity in human follicular fluid after controlled ovarian hyperstimulation in women undergoing in vitro fertilization. Fertil Steril 1999;72(6):1027–34.CrossRefGoogle ScholarPubMed
Shiverick, KT, Salafia, C. Cigarette smoking and pregnancy I: ovarian, uterine and placental effects. Placenta 1999;20(4):265–72.CrossRefGoogle ScholarPubMed
Guerin, P, El Mouatassim, S, Menezo, Y. Oxidative stress and protection against reactive oxygen species in the pre-implantation embryo and its surroundings. Hum Reprod Update 2001;7(2):175–89.CrossRefGoogle ScholarPubMed
Harvey, AJ, Kind, KL, Thompson, JG. REDOX regulation of early embryo development. Reproduction 2002;123(4):479–86.CrossRefGoogle ScholarPubMed
Matsui, M, Oshima, M, Oshima, H, et al. Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Dev Biol 1996;178(1):179–85.CrossRefGoogle ScholarPubMed
Knott, L, Hartridge, T, Brown, NL, Mansell, JP, Sandy, JR. Homocysteine oxidation and apoptosis: a potential cause of cleft palate. In Vitro Cell Dev Biol Anim 2003;39(1–2):98–105.2.0.CO;2>CrossRefGoogle ScholarPubMed
Parman, T, Wiley, MJ, Wells, PG. Free radical-mediated oxidative DNA damage in the mechanism of thalidomide teratogenicity. Nat Med 1999;5(5):582–5.CrossRefGoogle ScholarPubMed
Burton, GJ, Hempstock, J, Jauniaux, E. Oxygen, early embryonic metabolism and free radical-mediated embryopathies. Reprod Biomed Online 2003;6(1):84–96.CrossRefGoogle ScholarPubMed
Wentzel, P, Welsh, N, Eriksson, UJ. Developmental damage, increased lipid peroxidation, diminished cyclooxygenase-2 gene expression, and lowered prostaglandin E2 levels in rat embryos exposed to a diabetic environment. Diabetes 1999;48(4):813–20.CrossRefGoogle ScholarPubMed
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 1990;5(1):104–8.CrossRefGoogle ScholarPubMed
Warren, JS, Johnson, KJ, Ward, PA. Oxygen radicals in cell injury and cell death. Pathol Immunopathol Res 1987;6(5–6):301–15.CrossRefGoogle ScholarPubMed
Buhimschi, IA, Kramer, WB, Buhimschi, CS, Thompson, LP, Weiner, CP. Reduction-oxidation (redox) state regulation of matrix metalloproteinase activity in human fetal membranes. Am J Obstet Gynecol 2000;182(2):458–64.CrossRefGoogle ScholarPubMed
Machaty, Z, Thompson, JG, Abeydeera, LR, Day, BN, Prather, RS. Inhibitors of mitochondrial ATP production at the time of compaction improve development of in vitro produced porcine embryos. Mol Reprod Dev 2001;58(1):39–44.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Lane, M, Maybach, JM, Gardner, DK. Addition of ascorbate during cryopreservation stimulates subsequent embryo development. Hum Reprod 2002;17(10):2686–93.CrossRefGoogle ScholarPubMed
Lighten, AD, Moore, GE, Winston, RM, Hardy, K. Routine addition of human insulin-like growth factor-I ligand could benefit clinical in-vitro fertilization culture. Hum Reprod 1998;13(11):3144–50.CrossRefGoogle ScholarPubMed
Racowsky, C, Jackson, KV, Cekleniak, NA, Fox, JH, Hornstein, MD, Ginsburg, ES. The number of eight-cell embryos is a key determinant for selecting day 3 or day 5 transfer. Fertil Steril 2000;73(3):558–64.CrossRefGoogle ScholarPubMed
Jauniaux, E, Gulbis, B, Burton, GJ. Physiological implications of the materno-fetal oxygen gradient in human early pregnancy. Reprod Biomed Online 2003;7(2):250–3.CrossRefGoogle ScholarPubMed
Noda, Y, Goto, Y, Umaoka, Y, Shiotani, M, Nakayama, T, Mori, T. Culture of human embryos in alpha modification of Eagle's medium under low oxygen tension and low illumination. Fertil Steril 1994;62(5):1022–7.CrossRefGoogle ScholarPubMed
Nicol, CJ, Zielenski, J, Tsui, LC, Wells, PG. An embryoprotective role for glucose-6-phosphate dehydrogenase in developmental oxidative stress and chemical teratogenesis. FASEB J 2000;14(1):111–27.CrossRefGoogle ScholarPubMed
Dumoulin, JC, Meijers, CJ, Bras, M, Coonen, E, Geraedts, JP, Evers, JL. Effect of oxygen concentration on human in-vitro fertilization and embryo culture. Hum Reprod 1999;14(2):465–9.CrossRefGoogle ScholarPubMed
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 2004;62(7):1186–97.CrossRefGoogle Scholar
Wang, AW, Zhang, H, Ikemoto, I, Anderson, DJ, Loughlin, KR. Reactive oxygen species generation by seminal cells during cryopreservation. Urology 1997;49(6):921–5.CrossRefGoogle ScholarPubMed
Gadea, J, Gumbao, D, Matas, C, Romar, R. Supplementation of the thawing media with reduced glutathione improves function and the in vitro fertilizing ability of boar spermatozoa after cryopreservation. J Androl 2005;26(6):749–56.CrossRefGoogle ScholarPubMed
Chan, PJ, Calinisan, JH, Corselli, JU, Patton, WC, King, A. Updating quality control assays in the assisted reproductive technologies laboratory with a cryopreserved hamster oocyte DNA cytogenotoxic assay. J Assist Reprod Genet 2001;18(3):129–34.CrossRefGoogle ScholarPubMed
Kim, SS, Yang, HW, Kang, HG, et al. Quantitative assessment of ischemic tissue damage in ovarian cortical tissue with or without antioxidant (ascorbic acid) treatment. Fertil Steril 2004;82(3):679–85.CrossRefGoogle ScholarPubMed
Speroff, L GR, Kase, NG. Assisted Reproduction Clinical Gynecologic Endocrinology and Infertility, 6th edn. Philadelphia: Lippincott Williams & Wilkins, 1999:643–724.Google Scholar
Esfandiari, N, Falcone, T, Agarwal, A, Attaran, M, Nelson, DR, Sharma, RK. Protein supplementation and the incidence of apoptosis and oxidative stress in mouse embryos. Obstet Gynecol 2005;105(3):653–60.CrossRefGoogle ScholarPubMed
Catt, JW, Henman, M. Toxic effects of oxygen on human embryo development. Hum Reprod 2000;15 (Suppl. 2):199–206.CrossRefGoogle ScholarPubMed
Feugang, JM, Roover, R, Moens, A, Leonard, S, Dessy, F, Donnay, I. Addition of beta-mercaptoethanol or Trolox at the morula/blastocyst stage improves the quality of bovine blastocysts and prevents induction of apoptosis and degeneration by prooxidant agents. Theriogenology 2004;61(1):71–90.CrossRefGoogle ScholarPubMed
Tatemoto, H, Ootaki, K, Shigeta, K, Muto, N. Enhancement of developmental competence after in vitro fertilization of porcine oocytes by treatment with ascorbic acid 2-O-alpha-glucoside during in vitro maturation. Biol Reprod 2001;65(6):1800–6.CrossRefGoogle ScholarPubMed
Dalvit, G, Llanes, SP, Descalzo, A, Insani, M, Beconi, M, Cetica, P. Effect of alpha-tocopherol and ascorbic acid on bovine oocyte in vitro maturation. Reprod Domest Anim 2005;40(2):93–7.CrossRefGoogle ScholarPubMed
Oyamada, T, Fukui, Y. Oxygen tension and medium supplements for in vitro maturation of bovine oocytes cultured individually in a chemically defined medium. J Reprod Dev 2004;50(1):107–17.CrossRefGoogle Scholar
Matos, DG, Furnus, CC, Moses, DF. Glutathione synthesis during in vitro maturation of bovine oocytes: role of cumulus cells. Biol Reprod 1997;57(6):1420–5.CrossRefGoogle ScholarPubMed
Ali, AA, Bilodeau, JF, Sirard, MA. Antioxidant requirements for bovine oocytes varies during in vitro maturation, fertilization and development. Theriogenology 2003;59(3–4):939–49.CrossRefGoogle ScholarPubMed
Guerin, P, Guillaud, J, Menezo, Y. Hypotaurine in spermatozoa and genital secretions and its production by oviduct epithelial cells in vitro. Hum Reprod 1995;10(4):866–72.CrossRefGoogle ScholarPubMed
Takahashi, M, Nagai, T, Hamano, S, Kuwayama, M, Okamura, N, Okano, A. Effect of thiol compounds on in vitro development and intracellular glutathione content of bovine embryos. Biol Reprod 1993;49(2):228–32.CrossRefGoogle ScholarPubMed
Nonogaki, T, Noda, Y, Narimoto, K, Umaoka, Y, Mori, T. Effects of superoxide dismutase on mouse in vitro fertilization and embryo culture system. J Assist Reprod Genet 1992;9(3):274–80.CrossRefGoogle ScholarPubMed
Lornage, J. [Biological aspects of endometriosis in vitro fertilization]. J Gynecol Obstet Biol Reprod (Paris) 2003;32(8 Pt. 2):S48–50.Google ScholarPubMed
Saleh, RA, Agarwal, A. Oxidative stress and male infertility: from research bench to clinical practice. J Androl 2002;23(6):737–52.Google ScholarPubMed
Potts, RJ, Notarianni, LJ, Jefferies, TM. Seminal plasma reduces exogenous oxidative damage to human sperm, determined by the measurement of DNA strand breaks and lipid peroxidation. Mutat Res 2000;447(2):249–56.CrossRefGoogle ScholarPubMed
Bidri, M, Choay, P. [Taurine: a particular aminoacid with multiple functions]. Ann Pharm Fr 2003;61(6):385–91.Google ScholarPubMed
Henkel, RR, Schill, WB. Sperm preparation for ART. Reprod Biol Endocrinol 2003;1:108.CrossRefGoogle ScholarPubMed
Paul, M, Sumpter, JP, Lindsay, KS. Factors affecting pentoxifylline stimulation of sperm kinematics in suspensions. Hum Reprod 1996;11(9):1929–35.CrossRefGoogle ScholarPubMed
Lamond, S, Watkinson, M, Rutherford, T, et al. Gene-specific chromatin damage in human spermatozoa can be blocked by antioxidants that target mitochondria. Reprod Biomed Online 2003;7(4):407–18.CrossRefGoogle ScholarPubMed
Ermilov, A, Diamond, MP, Sacco, AG, Dozortsev, DD. Culture media and their components differ in their ability to scavenge reactive oxygen species in the plasmid relaxation assay. Fertil Steril 1999;72(1):154–7.CrossRefGoogle ScholarPubMed
Kattera, S, Chen, C. Short coincubation of gametes in in vitro fertilization improves implantation and pregnancy rates: a prospective, randomized, controlled study. Fertil Steril 2003;80(4):1017–21.CrossRefGoogle ScholarPubMed
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 1996;11(11):2507–11.CrossRefGoogle ScholarPubMed
Dirnfeld, M, Shiloh, H, Bider, D, et al. A prospective randomized controlled study of the effect of short coincubation of gametes during insemination on zona pellucida thickness. Gynecol Endocrinol 2003;17(5):397–403.CrossRefGoogle ScholarPubMed
Halliwell, B, Gutteridge, JM. Free radicals and antioxidant protection: mechanisms and significance in toxicology and disease. Hum Toxicol 1988;7(1):7–13.CrossRefGoogle ScholarPubMed
Kowaltowski, AJ, Vercesi, AE. Mitochondrial damage induced by conditions of oxidative stress. Free Radic Biol Med 1999;26(3–4):463–71.CrossRefGoogle ScholarPubMed
Ronnenberg, AG, Goldman, MB, Chen, D, et al. Preconception folate and vitamin B(6) status and clinical spontaneous abortion in Chinese women. Obstet Gynecol 2002;100(1):107–13.Google ScholarPubMed
Pierce, JD, Cackler, AB, Arnett, MG. Why should you care about free radicals?RN 2004;67(1):38–42; quiz 3.Google ScholarPubMed
Jauniaux, E, Watson, A, Burton, G. Evaluation of respiratory gases and acid-base gradients in human fetal fluids and uteroplacental tissue between 7 and 16 weeks gestation. Am J Obstet Gynecol 2001;184(5):998–1003.CrossRefGoogle Scholar
Quinn, P, Harlow, GM. The effect of oxygen on the development of preimplantation mouse embryos in vitro. J Exp Zool 1978;206(1):73–80.CrossRefGoogle ScholarPubMed
Jauniaux, E, Watson, AL, Hempstock, J, Bao, YP, Skepper, JN, Burton, GJ. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol 2000;157(6):2111–22.CrossRefGoogle ScholarPubMed
Rodesch, F, Simon, P, Donner, C, Jauniaux, E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol 1992;80(2):283–5.Google ScholarPubMed
Barrionuevo, MJ, Schwandt, RA, Rao, PS, Graham, LB, Maisel, LP, Yeko, TR. Nitric oxide (NO) and interleukin-1beta (IL-1beta) in follicular fluid and their correlation with fertilization and embryo cleavage. Am J Reprod Immunol 2000;44(6):359–64.CrossRefGoogle ScholarPubMed
Caniggia, I, Mostachfi, H, Winter, J, et al. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest 2000;105(5):577–87.CrossRefGoogle Scholar
Myatt, L, Cui, X. Oxidative stress in the placenta. Histochem Cell Biol 2004;122(4):369–82.CrossRefGoogle ScholarPubMed
Jauniaux, E, Hempstock, J, Greenwold, N, Burton, GJ. Trophoblastic oxidative stress in relation to temporal and regional differences in maternal placental blood flow in normal and abnormal early pregnancies. Am J Pathol 2003;162(1):115–25.CrossRefGoogle ScholarPubMed
W. Choi, JB, Agarwal, A, Falcone, T, Sharma, RK. Can vitamin C supplementation reduce oxidative stress induced cytoskeleton damage of mouse oocyte. Fertil Steril 2005;84 (Suppl. 1):S452.Google Scholar
Henmi, H, Endo, T, Kitajima, Y, Manase, K, Hata, H, Kudo, R. Effects of ascorbic acid supplementation on serum progesterone levels in patients with a luteal phase defect. Fertil Steril 2003;80(2):459–61.CrossRefGoogle ScholarPubMed
Crha, I, Hruba, D, Ventruba, P, Fiala, J, Totusek, J, Visnova, H. Ascorbic acid and infertility treatment. Cent Eur J Public Health 2003;11(2):63–7.Google ScholarPubMed
Griesinger, G, Franke, K, Kinast, C, et al. Ascorbic acid supplement during luteal phase in IVF. J Assist Reprod Genet 2002;19(4):164–8.CrossRefGoogle ScholarPubMed
Rumbold, A, Crowther, CA. Vitamin C supplementation in pregnancy. Cochrane Database Syst Rev 2005(2):CD004072.Google ScholarPubMed
Rumbold, A, Middleton, P, Crowther, CA. Vitamin supplementation for preventing miscarriage. Cochrane Database Syst Rev 2005(2):CD004073.Google ScholarPubMed
Ledee-Bataille, N, Olivennes, F, Lefaix, JL, Chaouat, G, Frydman, R, Delanian, S. Combined treatment by pentoxifylline and tocopherol for recipient women with a thin endometrium enrolled in an oocyte donation programme. Hum Reprod 2002;17(5):1249–53.CrossRefGoogle Scholar
Ebisch, IM, Thomas, CM, Peters, WH, Braat, DD, Steegers- Theunissen, RP. The importance of folate, zinc and antioxidants in the pathogenesis and prevention of subfertility. Hum Reprod Update 2007;13(2):163–74.CrossRefGoogle ScholarPubMed

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