Reproductive Biology and Endocrinology | |
Utility of antioxidants during assisted reproductive techniques: an evidence based review | |
Stefan S du Plessis1  Damayanthi Durairajanayagam3  Ashok Agarwal2  | |
[1] Division of Medical Physiology, Faculty of Medicine and Health Sciences, Stellenbosch University, Tygerberg 7505, South Africa;Center for Reproductive Medicine, Glickman Urological & Kidney Institute, Cleveland Clinic, Cleveland, OH 44195, USA;Discipline of Physiology, Faculty of Medicine, MARA University of Technology, Sungai Buloh, Selangor, 47000, Malaysia | |
关键词: ART outcome; Intracytoplasmic sperm injection; In vitro fertilization; Assisted reproductive technology; Antioxidants; Oxidative stress; Reactive oxygen species; | |
Others : 1139726 DOI : 10.1186/1477-7827-12-112 |
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received in 2014-08-12, accepted in 2014-11-06, 发布年份 2014 | |
【 摘 要 】
Assisted reproductive technology (ART) is a common treatment of choice for many couples facing infertility issues, be it due to male or female factor, or idiopathic. Employment of ART techniques, however, come with its own challenges as the in vitro environment is not nearly as ideal as the in vivo environment, where reactive oxygen species (ROS) build-up leading to oxidative stress is kept in check by the endogenous antioxidants system. While physiological amounts of ROS are necessary for normal reproductive function in vivo, in vitro manipulation of gametes and embryos exposes these cells to excessive ROS production either by endogenous or exogenous environmental factors. In this review, we discuss the sources of ROS in an in vitro clinical setting and the influence of oxidative stress on gamete/embryo quality and the outcome of IVF/ICSI. Sources of ROS and different strategies of overcoming the excessive generation of ROS in vitro are also highlighted. Endogenously, the gametes and the developing embryo become sources of ROS. Multiple exogenous factors act as potential sources of ROS, including exposure to visible light, composition of culture media, pH and temperature, oxygen concentration, centrifugation during spermatozoa preparation, ART technique involving handling of gamete/embryo and cryopreservation technique (freeze/thawing process). Finally, the use of antioxidants as agents to minimize ROS generation in the in vitro environment and as oral therapy is highlighted. Both enzymatic and non-enzymatic antioxidants are discussed and the outcome of studies using these antioxidants as oral therapy in the male or female or its use in vitro in media is presented. While results of studies using certain antioxidant agents are promising, the current body of evidence as a whole suggests the need for further well-designed and larger scale randomized controlled studies, as well as research to minimize oxidative stress conditions in the clinical ART setting.
【 授权许可】
2014 Agarwal et al.; licensee BioMed Central Ltd.
【 预 览 】
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20150322094818146.pdf | 1317KB | download | |
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Figure 1. | 170KB | Image | download |
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【 参考文献 】
- [1]Zegers-Hochschild F, Adamson GD, de Mouzon J, Ishihara O, Mansour R, Nygren K, Sullivan E, van der Poel S, International Committee for Monitoring Assisted Reproductive T, World Health O: The International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) Revised Glossary on ART Terminology, 2009. Hum Reprod 2009, 24:2683-2687.
- [2]Sharlip ID, Jarow JP, Belker AM, Lipshultz LI, Sigman M, Thomas AJ, Schlegel PN, Howards SS, Nehra A, Damewood MD, Overstreet JW, Sadovsky R: Best practice policies for male infertility. Fertil Steril 2002, 77:873-882.
- [3]Gupta S, Sekhon L, Kim Y, Agarwal A: The role of oxidative stress and antioxidants in assisted reproduction. Curr Women’s Health Rev 2010, 6:227-238.
- [4]Lampiao F: Free radicals generation in an in vitro fertilization setting and how to minimize them. World J Obstet Gynecol 2012, 1:29-34.
- [5]du Plessis SS, Makker K, Desai NR, Agarwal A: Impact of oxidative stress on IVF. Expet Rev Obstet Gynecol 2008, 3:539-554.
- [6]Rakhit M, Gokul SR, Agarwal A, du Plessis SS: Antioxidant strategies to overcome OS in IVF-Embryo transfer. In Studies on Women’s Health. Humana Press; 2013:237-262.
- [7]Agarwal A, Allamaneni SS: Role of free radicals in female reproductive diseases and assisted reproduction. Reprod Biomed Online 2004, 9:338-347.
- [8]Sharma RK, Agarwal A: Role of reactive oxygen species in male infertility. Urology 1996, 48:835-850.
- [9]Hammadeh ME, Al Hasani S, Rosenbaum P, Schmidt W, Fischer Hammadeh C: 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, 277:515-526.
- [10]Aitken RJ: Free radicals, lipid peroxidation and sperm function. Reprod Fertil Dev 1995, 7:659-668.
- [11]Agarwal A, Said TM, Bedaiwy MA, Banerjee J, Alvarez JG: Oxidative stress in an assisted reproductive techniques setting. Fertil Steril 2006, 86:503-512.
- [12]Saalu LC: The incriminating role of reactive oxygen species in idiopathic male infertility: an evidence based evaluation. Pakistan J Biol Sci 2010, 13:413-422.
- [13]Gupta S, Malhotra N, Sharma D, Chandra A, Agarwal A: Oxidative stress and its role in female infertility and assisted reproduction: clinical implications. Int J Fertil Steril 2009, 2:147-164.
- [14]de Lamirande E, Gagnon C: A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa. Int J Androl 1993, 16:21-25.
- [15]Agarwal A, Virk G, Ong C, du Plessis SS: Effect of oxidative stress on male reproduction. World J Men’s Health 2014, 32:1-17.
- [16]Kothari S, Thompson A, Agarwal A, du Plessis SS: Free radicals: their beneficial and detrimental effects on sperm function. Indian J Exp Biol 2010, 48:425-435.
- [17]Tremellen K: Oxidative stress and male infertility–a clinical perspective. Hum Reprod Update 2008, 14:243-258.
- [18]Aitken RJ, Fisher HM, Fulton N, Gomez E, Knox W, Lewis B, Irvine S: Reactive oxygen species generation by human spermatozoa is induced by exogenous NADPH and inhibited by the flavoprotein inhibitors diphenylene iodonium and quinacrine. Mol Reprod Dev 1997, 47:468-482.
- [19]Rengan AK, Agarwal A, van der Linde M, du Plessis SS: An investigation of excess residual cytoplasm in human spermatozoa and its distinction from the cytoplasmic droplet. Reprod Biol Endocrinol 2012, 10:92.
- [20]Whittington K, Ford WC: Relative contribution of leukocytes and of spermatozoa to reactive oxygen species production in human sperm suspensions. Int J Androl 1999, 22:229-235.
- [21]Kessopoulou E, Tomlinson MJ, Barratt CL, Bolton AE, Cooke ID: Origin of reactive oxygen species in human semen: spermatozoa or leucocytes? J Reprod Fertil 1992, 94:463-470.
- [22]Saleh RA, Agarwal A, Nada EA, El-Tonsy MH, Sharma RK, Meyer A, Nelson DR, Thomas AJ: 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(Suppl 3):1597-1605.
- [23]Kroese AC, de Lange NM, Collins J, Evers JL: Surgery or embolization for varicoceles in subfertile men. Cochrane Database Syst Rev 2012., 10CD000479
- [24]Shiraishi K, Matsuyama H, Takihara H: Pathophysiology of varicocele in male infertility in the era of assisted reproductive technology. Int J Urol: Offic J Jpn Urol Assoc 2012, 19:538-550.
- [25]Agarwal A, Prabakaran S, Allamaneni SS: Relationship between oxidative stress, varicocele and infertility: a meta-analysis. Reprod Biomed Online 2006, 12:630-633.
- [26]Agarwal A, Gupta S, Abdel-Razek H, Krajcir N, Athayde K: Impact of oxidative stress on gametes and embryos in an ART Laboratory. Clin Embryologist 2006, 9:5-22.
- [27]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, 105:653-660.
- [28]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, 77:1184-1190.
- [29]Zhuo L, Kimata K: Cumulus oophorus extracellular matrix: its construction and regulation. Cell Struct Funct 2001, 26:189-196.
- [30]Huang Z, Wells D: The human oocyte and cumulus cells relationship: new insights from the cumulus cell transcriptome. Mol Hum Reprod 2010, 16:715-725.
- [31]Matos L, Stevenson D, Gomes F, Silva-Carvalho JL, Almeida H: Superoxide dismutase expression in human cumulus oophorus cells. Mol Hum Reprod 2009, 15:411-419.
- [32]Attaran M, Pasqualotto E, Falcone T, Goldberg JM, Miller KF, Agarwal A, Sharma RK: The effect of follicular fluid reactive oxygen species on the outcome of in vitro fertilization. Int J Fertil Womens Med 2000, 45:314-320.
- [33]Pasqualotto EB, Agarwal A, Sharma RK, Izzo VM, Pinotti JA, Joshi NJ, Rose BI: Effect of oxidative stress in follicular fluid on the outcome of assisted reproductive procedures. Fertil Steril 2004, 81:973-976.
- [34]Bedaiwy MA, Elnashar SA, Goldberg JM, Sharma R, Mascha EJ, Arrigain S, Agarwal A, Falcone T: Effect of follicular fluid oxidative stress parameters on intracytoplasmic sperm injection outcome. Gynecol Endocrinol 2012, 28:51-55.
- [35]Jana SK KNB, Chattopadhyay R, Chakravarty B, Chaudhury K: Upper control limit of reactive oxygen species in follicular fluid beyond which viable embryo formation is not favorable. Reprod Toxicol 2010, 29:447-451.
- [36]Das S, Chattopadhyay R, Ghosh S, Ghosh S, Goswami SK, Chakravarty BN, Chaudhury K: Reactive oxygen species level in follicular fluid–embryo quality marker in IVF? Hum Reprod 2006, 21:2403-2407.
- [37]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, 7:175-189.
- [38]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, 5:104-108.
- [39]Agarwal A, Saleh RA, Bedaiwy MA: Role of reactive oxygen species in the pathophysiology of human reproduction. Fertil Steril 2003, 79:829-843.
- [40]Goto Y, Noda Y, Mori T, Nakano M: Increased generation of reactive oxygen species in embryos cultured in vitro. Free Radic Biol Med 1993, 15(1):69-75.
- [41]Li R, Liu Y, Pedersen HS, Callesen H: Effect of ambient light exposure of media and embryos on development and quality of porcine parthenogenetically activated embryos. Zygote 2014, 1-6. [Epub ahead of print]
- [42]Ottosen LD, Hindkjaer J, Ingerslev J: Light exposure of the ovum and preimplantation embryo during ART procedures. J Assist Reprod Genet 2007, 24:99-103.
- [43]Squirrell JM, Wokosin DL, White JG, Bavister BD: Long-term two-photon fluorescence imaging of mammalian embryos without compromising viability. Nat Biotechnol 1999, 17:763-767.
- [44]Hockberger PE, Skimina TA, Centonze VE, Lavin C, Chu S, Dadras S, Reddy JK, White JG: Activation of flavin-containing oxidases underlies light-induced production of H2O2 in mammalian cells. Proc Natl Acad Sci U S A 1999, 96:6255-6260.
- [45]Oh SJ, Gong SP, Lee ST, Lee EJ, Lim JM: Light intensity and wavelength during embryo manipulation are important factors for maintaining viability of preimplantation embryos in vitro. Fertil Steril 2007, 88:1150-1157.
- [46]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, 62:1022-1027.
- [47]Takenaka M, Horiuchi T, Yanagimachi R: Effects of light on development of mammalian zygotes. Proc Natl Acad Sci U S A 2007, 104:14289-14293.
- [48]Moshkdanian G, Nematollahi-Mahani SN, Pouya F, Nematollahi-Mahani A: Antioxidants rescue stressed embryos at a rate comparable with co-culturing of embryos with human umbilical cord mesenchymal cells. J Assist Reprod Genet 2011, 28:343-349.
- [49]Umaoka Y, Noda Y, Nakayama T, Narimoto K, Mori T, Iritani A: Effect of visual light on in vitro embryonic development in the hamster. Theriogenology 1992, 38:1043-1054.
- [50]Takahashi M, Saka N, Takahashi H, Kanai Y, Schultz RM, Okano A: Assessment of DNA damage in individual hamster embryos by comet assay. Mol Reprod Dev 1999, 54:1-7.
- [51]Shahar S, Wiser A, Ickowicz D, Lubart R, Shulman A, Breitbart H: Light-mediated activation reveals a key role for protein kinase A and sarcoma protein kinase in the development of sperm hyper-activated motility. Hum Reprod 2011, 26:2274-2282.
- [52]Jin J, Jin N, Zheng H, Ro S, Tafolla D, Sanders KM, Yan W: Catsper3 and Catsper4 are essential for sperm hyperactivated motility and male fertility in the mouse. Biol Reprod 2007, 77:37-44.
- [53]Ho HC, Suarez SS: Hyperactivation of mammalian spermatozoa: function and regulation. Reproduction 2001, 122:519-526.
- [54]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 2001, 59:44-53.
- [55]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 1992, 96:219-231.
- [56]Sikka SC: Role of oxidative stress and antioxidants in andrology and assisted reproductive technology. J Androl 2004, 25:5-18.
- [57]Kalthur G, Raj S, Thiyagarajan A, Kumar S, Kumar P, Adiga SK: Vitamin E supplementation in semen-freezing medium improves the motility and protects sperm from freeze-thaw-induced DNA damage. Fertil Steril 2011, 95:1149-1151.
- [58]Taylor K, Roberts P, Sanders K, Burton P: Effect of antioxidant supplementation of cryopreservation medium on post-thaw integrity of human spermatozoa. Reprod Biomed Online 2009, 18:184-189.
- [59]Keshtgar S, Fanaei H, Bahmanpour S, Azad F, Ghannadi A, Kazeroni M: In vitro effects of alpha-tocopherol on teratozoospermic semen samples. Andrologia 2012, 44(Suppl 1):721-727.
- [60]Fanaei H, Khayat S, Halvaei I, Ramezani V, Azizi Y, Kasaeian A, Mardaneh J, Parvizi MR, Akrami M: Effects of ascorbic acid on sperm motility, viability, acrosome reaction and DNA integrity in teratozoospermic samples. Iranian J Reprod Med 2014, 12:103-110.
- [61]Branco CS, Garcez ME, Pasqualotto FF, Erdtman B, Salvador M: Resveratrol and ascorbic acid prevent DNA damage induced by cryopreservation in human semen. Cryobiology 2010, 60:235-237.
- [62]Jenkins TG, Aston KI, Carrell DT: Supplementation of cryomedium with ascorbic acid-2-glucoside (AA2G) improves human sperm post-thaw motility. Fertil Steril 2011, 95:2001-2004.
- [63]Lewin A, Lavon H: The effect of coenzyme Q10 on sperm motility and function. Mol Aspects Med 1997, 18(Suppl):S213-S219.
- [64]Ortiz A, Espino J, Bejarano I, Lozano GM, Monllor F, Garcia JF, Pariente JA, Rodriguez AB: High endogenous melatonin concentrations enhance sperm quality and short-term in vitro exposure to melatonin improves aspects of sperm motility. J Pineal Res 2011, 50:132-139.
- [65]du Plessis SS, Hagenaar K, Lampiao F: The in vitro effects of melatonin on human sperm function and its scavenging activities on NO and ROS. Andrologia 2010, 42:112-116.
- [66]Mansour G, Abdelrazik H, Sharma RK, Radwan E, Falcone T, Agarwal A: L-carnitine supplementation reduces oocyte cytoskeleton damage and embryo apoptosis induced by incubation in peritoneal fluid from patients with endometriosis. Fertil Steril 2009, 91:2079-2086.
- [67]Abdelrazik H, Sharma R, Mahfouz R, Agarwal A: L-carnitine decreases DNA damage and improves the in vitro blastocyst development rate in mouse embryos. Fertil Steril 2009, 91:589-596.
- [68]Will MA, Clark NA, Swain JE: Biological pH buffers in IVF: help or hindrance to success. J Assist Reprod Genet 2011, 28:711-724.
- [69]Bagger PV, Byskov AG, Christiansen MD: Maturation of mouse oocytes in vitro is influenced by alkalization during their isolation. J Reprod Fertil 1987, 80:251-255.
- [70]Suzuki N, Mittler R: Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 2006, 126:45-51.
- [71]Ferguson WJ, Braunschweiger KI, Braunschweiger WR, Smith JR, McCormick JJ, Wasmann CC, Jarvis NP, Bell DH, Good NE: Hydrogen ion buffers for biological research. Anal Biochem 1980, 104:300-310.
- [72]Larkindale J, Knight MR: Protection against heat stress-induced oxidative damage in Arabidopsis involves calcium, abscisic acid, ethylene, and salicylic acid. Plant Physiol 2002, 128:682-695.
- [73]Calzi F, Papaleo E, Rabellotti E, Ottolina J, Vailati S, Vigano P, Candiani M: Exposure of embryos to oxygen at low concentration in a cleavage stage transfer program: reproductive outcomes in a time-series analysis. Clin Lab 2012, 58:997-1003.
- [74]Cohen J, Gilligan A, Esposito W, Schimmel T, Dale B: Ambient air and its potential effects on conception in vitro. Hum Reprod 1997, 12:1742-1749.
- [75]Bontekoe S, Mantikou E, van Wely M, Seshadri S, Repping S, Mastenbroek S: Low oxygen concentrations for embryo culture in assisted reproductive technologies. Cochrane Database Syst Rev 2012., 7CD008950
- [76]Kovacic B, Sajko MC, Vlaisavljevic V: A prospective, randomized trial on the effect of atmospheric versus reduced oxygen concentration on the outcome of intracytoplasmic sperm injection cycles. Fertil Steril 2010, 94:511-519.
- [77]Kovacic B, Vlaisavljevic V: Influence of atmospheric versus reduced oxygen concentration on development of human blastocysts in vitro: a prospective study on sibling oocytes. Reprod Biomed Online 2008, 17:229-236.
- [78]Gomes Sobrinho DB, Oliveira JB, Petersen CG, Mauri AL, Silva LF, Massaro FC, Baruffi RL, Cavagna M, Franco JG Jr: IVF/ICSI outcomes after culture of human embryos at low oxygen tension: a meta-analysis. Reprod Biol Endocrinol 2011, 9:143.
- [79]Shekarriz M, DeWire DM, Thomas AJ Jr, Agarwal A: A method of human semen centrifugation to minimize the iatrogenic sperm injuries caused by reactive oxygen species. Eur Urol 1995, 28:31-35.
- [80]Henkel RR, Schill WB: Sperm preparation for ART. Reprod Biol Endocrinol 2003, 1:108.
- [81]McKinney KA, Lewis SE, Thompson W: The effects of pentoxifylline on the generation of reactive oxygen species and lipid peroxidation in human spermatozoa. Andrologia 1996, 28:15-20.
- [82]Lampiao F, Strijdom H, Du Plessis SS: Effects of sperm processing techniques involving centrifugation on nitric oxide, reactive oxygen species generation and sperm function. Open Androl J 2010, 2:1-5.
- [83]Agarwal A, Said TM: Role of sperm chromatin abnormalities and DNA damage in male infertility. Hum Reprod Update 2003, 9:331-345.
- [84]Gandini L, Lombardo F, Paoli D, Caponecchia L, Familiari G, Verlengia C, Dondero F, Lenzi A: Study of apoptotic DNA fragmentation in human spermatozoa. Hum Reprod 2000, 15:830-839.
- [85]Pegg DE: Principles of cryopreservation. Methods Mol Biol 2007, 368:39-57.
- [86]Di Santo M, Tarozzi N, Nadalini M, Borini A: Human sperm cryopreservation: update on techniques, effect on DNA integrity, and implications for ART. Adv Urol 2012, 2012:854837.
- [87]Thomson LK, Fleming SD, Aitken RJ, De Iuliis GN, Zieschang JA, Clark AM: Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Hum Reprod 2009, 24:2061-2070.
- [88]Zribi N, Feki Chakroun N, El Euch H, Gargouri J, Bahloul A, Ammar Keskes L: Effects of cryopreservation on human sperm deoxyribonucleic acid integrity. Fertil Steril 2010, 93:159-166.
- [89]Zini A, Al-Hathal N: Antioxidant therapy in male infertility: fact or fiction? Asian J Androl 2011, 13:374-381.
- [90]Zribi N, Chakroun NF, Ben Abdallah F, Elleuch H, Sellami A, Gargouri J, Rebai T, Fakhfakh F, Keskes LA: Effect of freezing-thawing process and quercetin on human sperm survival and DNA integrity. Cryobiology 2012, 65:326-331.
- [91]Moubasher AE, El Din AM, Ali ME, El-sherif WT, Gaber HD: Catalase improves motility, vitality and DNA integrity of cryopreserved human spermatozoa. Andrologia 2013, 45(2):135-139.
- [92]Esteves SC, Sharma RK, Thomas AJ Jr, Agarwal A: Cryopreservation of human spermatozoa with pentoxifylline improves the post-thaw agonist-induced acrosome reaction rate. Hum Reprod 1998, 13:3384-3389.
- [93]Brennan AP, Holden CA: Pentoxifylline-supplemented cryoprotectant improves human sperm motility after cryopreservation. Hum Reprod 1995, 10:2308-2312.
- [94]Bell M, Wang R, Hellstrom WJ, Sikka SC: Effect of cryoprotective additives and cryopreservation protocol on sperm membrane lipid peroxidation and recovery of motile human sperm. J Androl 1993, 14:472-478.
- [95]Wang R, Sikka SC, Veeraragavan K, Bell M, Hellstrom WJ: Platelet activating factor and pentoxifylline as human sperm cryoprotectants. Fertil Steril 1993, 60:711-715.
- [96]Kalthur G, Salian SR, Keyvanifard F, Sreedharan S, Thomas JS, Kumar P, Adiga SK: Supplementation of biotin to sperm preparation medium increases the motility and longevity in cryopreserved human spermatozoa. J Assist Reprod Genet 2012, 29:631-635.
- [97]Nallella KP, Sharma RK, Allamaneni SS, Aziz N, Agarwal A: Cryopreservation of human spermatozoa: comparison of two cryopreservation methods and three cryoprotectants. Fertil Steril 2004, 82:913-918.
- [98]Sole M, Santalo J, Boada M, Clua E, Rodriguez I, Martinez F, Coroleu B, Barri PN, Veiga A: How does vitrification affect oocyte viability in oocyte donation cycles? A prospective study to compare outcomes achieved with fresh versus vitrified sibling oocytes. Hum Reprod 2013, 28:2087-2092.
- [99]Cobo A, Meseguer M, Remohi J, Pellicer A: Use of cryo-banked oocytes in an ovum donation programme: a prospective, randomized, controlled, clinical trial. Hum Reprod 2010, 25:2239-2246.
- [100]Bansal AK, Bilaspuri GS: Impacts of oxidative stress and antioxidants on semen functions. Vet Med Int 2010., 2010
- [101]Kessopoulou E, Powers HJ, Sharma KK, Pearson MJ, Russell JM, Cooke ID, Barratt CL: A double-blind randomized placebo cross-over controlled trial using the antioxidant vitamin E to treat reactive oxygen species associated male infertility. Fertil Steril 1995, 64:825-831.
- [102]Suleiman SA, Ali ME, Zaki ZM, El-Malik EM, Nasr MA: Lipid peroxidation and human sperm motility: protective role of vitamin E. J Androl 1996, 17:530-537.
- [103]Ghanem H, Shaeer O, El-Segini A: Combination clomiphene citrate and antioxidant therapy for idiopathic male infertility: a randomized controlled trial. Fertil Steril 2010, 93:2232-2235.
- [104]Keskes-Ammar L, Feki-Chakroun N, Rebai T, Sahnoun Z, Ghozzi H, Hammami S, Zghal K, Fki H, Damak J, Bahloul A: Sperm oxidative stress and the effect of an oral vitamin E and selenium supplement on semen quality in infertile men. Arch Androl 2003, 49:83-94.
- [105]Moslemi MK, Tavanbakhsh S: Selenium-vitamin E supplementation in infertile men: effects on semen parameters and pregnancy rate. Int J Gen Med 2011, 4:99-104.
- [106]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 1999, 14:1028-1033.
- [107]Greco E, Iacobelli M, Rienzi L, Ubaldi F, Ferrero S, Tesarik J: Reduction of the incidence of sperm DNA fragmentation by oral antioxidant treatment. J Androl 2005, 26:349-353.
- [108]Greco E, Romano S, Iacobelli M, Ferrero S, Baroni E, Minasi MG, Ubaldi F, Rienzi L, Tesarik J: ICSI in cases of sperm DNA damage: beneficial effect of oral antioxidant treatment. Hum Reprod 2005, 20:2590-2594.
- [109]Dawson EB, Harris WA, Rankin WE, Charpentier LA, McGanity WJ: Effect of ascorbic acid on male fertility. Ann N Y Acad Sci 1987, 498:312-323.
- [110]Dawson EB, Harris WA, Teter MC, Powell LC: Effect of ascorbic acid supplementation on the sperm quality of smokers. Fertil Steril 1992, 58:1034-1039.
- [111]Wong WY, Merkus HM, Thomas CM, Menkveld R, Zielhuis GA, Steegers-Theunissen RP: Effects of folic acid and zinc sulfate on male factor subfertility: a double-blind, randomized, placebo-controlled trial. Fertil Steril 2002, 77:491-498.
- [112]Ebisch IM, Pierik FH, FH DEJ, Thomas CM, Steegers-Theunissen RP: Does folic acid and zinc sulphate intervention affect endocrine parameters and sperm characteristics in men? Int J Androl 2006, 29:339-345.
- [113]Raigani M, Yaghmaei B, Amirjannti N, Lakpour N, Akhondi MM, Zeraati H, Hajihosseinal M, Sadeghi MR: The micronutrient supplements, zinc sulphate and folic acid, did not ameliorate sperm functional parameters in oligoasthenoteratozoospermic men. Andrologia 2013, 46:956-962.
- [114]Azizollahi G, Azizollahi S, Babaei H, Kianinejad M, Baneshi MR, Nematollahi-mahani SN: Effects of supplement therapy on sperm parameters, protamine content and acrosomal integrity of varicocelectomized subjects. J Assist Reprod Genet 2013, 30:593-599.
- [115]Lafuente R, Gonzalez-Comadran M, Sola I, Lopez G, Brassesco M, Carreras R, Checa MA: Coenzyme Q10 and male infertility: a meta-analysis. J Assist Reprod Genet 2013, 30:1147-1156.
- [116]Nadjarzadeh A, Shidfar F, Amirjannati N, Vafa MR, Motevalian SA, Gohari MR, Nazeri Kakhki SA, Akhondi MM, Sadeghi MR: Effect of Coenzyme Q10 supplementation on antioxidant enzymes activity and oxidative stress of seminal plasma: a double-blind randomised clinical trial. Andrologia 2014, 46:177-183.
- [117]Nadjarzadeh A, Sadeghi MR, Amirjannati N, Vafa MR, Motevalian SA, Gohari MR, Akhondi MA, Yavari P, Shidfar F: Coenzyme Q10 improves seminal oxidative defense but does not affect on semen parameters in idiopathic oligoasthenoteratozoospermia: a randomized double-blind, placebo controlled trial. J Endocrinol Invest 2011, 34:e224-e228.
- [118]Safarinejad MR, Safarinejad S, Shafiei N, Safarinejad S: Effects of the reduced form of coenzyme Q10 (ubiquinol) on semen parameters in men with idiopathic infertility: a double-blind, placebo controlled, randomized study. J Urol 2012, 188:526-531.
- [119]Balercia G, Buldreghini E, Vignini A, Tiano L, Paggi F, Amoroso S, Ricciardo-Lamonica G, Boscaro M, Lenzi A, Littarru G: Coenzyme Q10 treatment in infertile men with idiopathic asthenozoospermia: a placebo-controlled, double-blind randomized trial. Fertil Steril 2009, 91:1785-1792.
- [120]Safarinejad MR: Efficacy of coenzyme Q10 on semen parameters, sperm function and reproductive hormones in infertile men. J Urol 2009, 182:237-248.
- [121]Safarinejad MR: The effect of coenzyme Q(1)(0) supplementation on partner pregnancy rate in infertile men with idiopathic oligoasthenoteratozoospermia: an open-label prospective study. Int Urol Nephrol 2012, 44:689-700.
- [122]Cicek N, Eryilmaz OG, Sarikaya E, Gulerman C, Genc Y: Vitamin E effect on controlled ovarian stimulation of unexplained infertile women. J Assist Reprod Genet 2012, 29:325-328.
- [123]Crha I, Hruba D, Ventruba P, Fiala J, Totusek J, Visnova H: Ascorbic acid and infertility treatment. Cent Eur J Public Health 2003, 11:63-67.
- [124]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, 80:459-461.
- [125]Griesinger G, Franke K, Kinast C, Kutzelnigg A, Riedinger S, Kulin S, Kaali SG, Feichtinger W: Ascorbic acid supplement during luteal phase in IVF. J Assist Reprod Genet 2002, 19:164-168.
- [126]Papaleo E, Unfer V, Baillargeon JP, Chiu TT: Contribution of myo-inositol to reproduction. Eur J Obstet Gynecol Reprod Biol 2009, 147:120-123.
- [127]Ciotta L, Stracquadanio M, Pagano I, Carbonaro A, Palumbo M, Gulino F: Effects of myo-inositol supplementation on oocyte’s quality in PCOS patients: a double blind trial. Eur Rev Med Pharmacol Sci 2011, 15:509-514.
- [128]Tamura H, Nakamura Y, Terron MP, Flores LJ, Manchester LC, Tan DX, Sugino N, Reiter RJ: Melatonin and pregnancy in the human. Reprod Toxicol 2008, 25:291-303.
- [129]Batioglu AS, Sahin U, Gurlek B, Ozturk N, Unsal E: The efficacy of melatonin administration on oocyte quality. Gynecol Endocrinol 2012, 28:91-93.
- [130]Eryilmaz OG, Devran A, Sarikaya E, Aksakal FN, Mollamahmutoglu L, Cicek N: Melatonin improves the oocyte and the embryo in IVF patients with sleep disturbances, but does not improve the sleeping problems. J Assist Reprod Genet 2011, 28:815-820.
- [131]Rizzo P, Raffone E, Benedetto V: Effect of the treatment with myo-inositol plus folic acid plus melatonin in comparison with a treatment with myo-inositol plus folic acid on oocyte quality and pregnancy outcome in IVF cycles. A prospective, clinical trial. Eur Rev Med Pharmacol Sci 2010, 14:555-561.
- [132]Unfer V, Raffone E, Rizzo P, Buffo S: Effect of a supplementation with myo-inositol plus melatonin on oocyte quality in women who failed to conceive in previous in vitro fertilization cycles for poor oocyte quality: a prospective, longitudinal, cohort study. Gynecol Endocrinol 2011, 27:857-861.
- [133]Tavilani H, Goodarzi MT, Vaisi-raygani A, Salimi S, Hassanzadeh T: Activity of antioxidant enzymes in seminal plasma and their relationship with lipid peroxidation of spermatozoa. Int Braz J 2008, 34:485-491.
- [134]Atig F, Raffa M, Ali HB, Abdelhamid K, Saad A, Ajina M: Altered antioxidant status and increased lipid per-oxidation in seminal plasma of tunisian infertile men. Int J Biol Sci 2012, 8:139-149.
- [135]Mahanta R, Gogoi A, Chaudhury PN, Roy S, Bhattacharyya IK, Sharma P: Association of oxidative stress biomarkers and antioxidant enzymatic activity in male infertility of north-East India. J Obstet Gynaecol India 2012, 62:546-550.
- [136]Alscher RG, Erturk N, Heath LS: Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot 2002, 53:1331-1341.
- [137]Marzec-Wroblewska U, Kaminski P, Lakota P, Szymanski M, Wasilow K, Ludwikowski G, Kuligowska-Prusinska M, Odrowaz-Sypniewska G, Stuczynski T, Michalkiewicz J: Zinc and iron concentration and SOD activity in human semen and seminal plasma. Biol Trace Elem Res 2011, 143:167-177.
- [138]Yan L, Liu J, Wu S, Zhang S, Ji G, Gu A: Seminal superoxide dismutase activity and its relationship with semen quality and SOD gene polymorphism. J Assist Reprod Genet 2014, 31:549-554.
- [139]Suzuki T, Sugino N, Fukaya T, Sugiyama S, Uda T, Takaya R, Yajima A, Sasano H: Superoxide dismutase in normal cycling human ovaries: immunohistochemical localization and characterization. Fertil Steril 1999, 72:720-726.
- [140]Liu J, Li Y: [Effect of oxidative stress and apoptosis in granulosa cells on the outcome of IVF-ET]. Zhong nan da xue xue bao Yi xue ban = J Cent South Univ Med Sci 2010, 35:990-994.
- [141]Noblanc A, Kocer A, Chabory E, Vernet P, Saez F, Cadet R, Conrad M, Drevet JR: Glutathione peroxidases at work on epididymal spermatozoa: an example of the dual effect of reactive oxygen species on mammalian male fertilizing ability. J Androl 2011, 32(6):641-650.
- [142]Jeulin C, Soufir JC, Weber P, Laval-Martin D, Calvayrac R: Catalase activity in human spermatozoa and seminal plasma. Gamete Res 1989, 24:185-196.
- [143]Alrabeeah K, Alhathal N, San Gabriel M, Zini A: Influence of seminal catalase activity on IVF pregnancy. J Urol 2011, 185:e805.
- [144]Chi HJ, Kim JH, Ryu CS, Lee JY, Park JS, Chung DY, Choi SY, Kim MH, Chun EK, Roh SI: Protective effect of antioxidant supplementation in sperm-preparation medium against oxidative stress in human spermatozoa. Hum Reprod 2008, 23:1023-1028.
- [145]Li Z, Lin Q, Liu R, Xiao W, Liu W: Protective effects of ascorbate and catalase on human spermatozoa during cryopreservation. J Androl 2010, 31:437-444.
- [146]Rossi T, Mazzilli F, Delfino M, Dondero F: Improved human sperm recovery using superoxide dismutase and catalase supplementation in semen cryopreservation procedure. Cell Tissue Bank 2001, 2:9-13.
- [147]Perkins AV: Endogenous anti-oxidants in pregnancy and preeclampsia. Aust N Z J Obstet Gynaecol 2006, 46:77-83.
- [148]Imai H, Nakagawa Y: Biological significance of phospholipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic Biol Med 2003, 34:145-169.
- [149]Crisol L, Matorras R, Aspichueta F, Exposito A, Hernandez ML, Ruiz-Larrea MB, Mendoza R, Ruiz-Sanz JI: Glutathione peroxidase activity in seminal plasma and its relationship to classical sperm parameters and in vitro fertilization-intracytoplasmic sperm injection outcome. Fertil Steril 2012, 97:852-857.
- [150]Geva E, Bartoov B, Zabludovsky N, Lessing JB, Lerner-Geva L, Amit A: The effect of antioxidant treatment on human spermatozoa and fertilization rate in an in vitro fertilization program. Fertil Steril 1996, 66:430-434.
- [151]Mistry HD, Broughton Pipkin F, Redman CW, Poston L: Selenium in reproductive health. Am J Obstet Gynecol 2012, 206:21-30.
- [152]Flohe L: Selenium in mammalian spermiogenesis. Biol Chem 2007, 388:987-995.
- [153]Iqbal K, Khan A, Khattak MMAK: Biological significance of ascorbic acid (Vitamin C) in human health – a review. Pak J Nutr 2004, 3:5-13.
- [154]Mendiola J, Torres-Cantero AM, Moreno-Grau JM, Ten J, Roca M, Moreno-Grau S, Bernabeu R: Food intake and its relationship with semen quality: a case–control study. Fertil Steril 2009, 91:812-818.
- [155]Mendiola J, Torres-Cantero AM, Vioque J, Moreno-Grau JM, Ten J, Roca M, Moreno-Grau S, Bernabeu R: A low intake of antioxidant nutrients is associated with poor semen quality in patients attending fertility clinics. Fertil Steril 2010, 93:1128-1133.
- [156]Wallock LM, Tamura T, Mayr CA, Johnston KE, Ames BN, Jacob RA: Low seminal plasma folate concentrations are associated with low sperm density and count in male smokers and nonsmokers. Fertil Steril 2001, 75:252-259.
- [157]Murphy LE, Mills JL, Molloy AM, Qian C, Carter TC, Strevens H, Wide-Swensson D, Giwercman A, Levine RJ: Folate and vitamin B12 in idiopathic male infertility. Asian J Androl 2011, 13:856-861.
- [158]Colagar AH, Marzony ET, Chaichi MJ: Zinc levels in seminal plasma are associated with sperm quality in fertile and infertile men. Nutr Res 2009, 29:82-88.
- [159]Yamaguchi S, Miura C, Kikuchi K, Celino FT, Agusa T, Tanabe S, Miura T: Zinc is an essential trace element for spermatogenesis. Proc Natl Acad Sci U S A 2009, 106:10859-10864.
- [160]Omu AE, Dashti H, Al-Othman S: Treatment of asthenozoospermia with zinc sulphate: andrological, immunological and obstetric outcome. Eur J Obstet Gynecol Reprod Biol 1998, 79:179-184.
- [161]Lanzafame FM, La Vignera S, Vicari E, Calogero AE: Oxidative stress and medical antioxidant treatment in male infertility. Reprod Biomed Online 2009, 19:638-659.
- [162]Mayo JC, Sainz RM, Antoli I, Herrera F, Martin V, Rodriguez C: Melatonin regulation of antioxidant enzyme gene expression. Cell Mol Life Sci 2002, 59:1706-1713.
- [163]Nakamura Y, Tamura H, Takayama H, Kato H: Increased endogenous level of melatonin in preovulatory human follicles does not directly influence progesterone production. Fertil Steril 2003, 80:1012-1016.
- [164]Tamura H, Takasaki A, Miwa I, Taniguchi K, Maekawa R, Asada H, Taketani T, Matsuoka A, Yamagata Y, Shimamura K, Morioka H, Ishikawa H, Reiter RJ, Sugino N: Oxidative stress impairs oocyte quality and melatonin protects oocytes from free radical damage and improves fertilization rate. J Pineal Res 2008, 44:280-287.
- [165]Seko LM, Moroni RM, Leitao VM, Teixeira DM, Nastri CO, Martins WP: Melatonin supplementation during controlled ovarian stimulation for women undergoing assisted reproductive technology: systematic review and meta-analysis of randomized controlled trials. Fertil Steril 2014, 101:154-161. e154
- [166]Omu AE, Al-Azemi MK, Kehinde EO, Anim JT, Oriowo MA, Mathew TC: Indications of the mechanisms involved in improved sperm parameters by zinc therapy. Med Princ Pract 2008, 17:108-116.
- [167]Talevi R, Barbato V, Fiorentino I, Braun S, Longobardi S, Gualtieri R: Protective effects of in vitro treatment with zinc, d-aspartate and coenzyme q10 on human sperm motility, lipid peroxidation and DNA fragmentation. Reprod Biol Endocrinol 2013, 11:81.
- [168]Kotdawala AP, Kumar S, Salian SR, Thankachan P, Govindraj K, Kumar P, Kalthur G, Adiga SK: Addition of zinc to human ejaculate prior to cryopreservation prevents freeze-thaw-induced DNA damage and preserves sperm function. J Assist Reprod Genet 2012, 29:1447-1453.
- [169]Safarinejad MR, Safarinejad S: Efficacy of selenium and/or N-acetyl-cysteine for improving semen parameters in infertile men: a double-blind, placebo controlled, randomized study. J Urol 2009, 181:741-751.
- [170]Banihani S, Sharma R, Bayachou M, Sabanegh E, Agarwal A: Human sperm DNA oxidation, motility and viability in the presence of L-carnitine during in vitro incubation and centrifugation. Andrologia 2012, 44(Suppl 1):505-512.
- [171]Zhou X, Liu F, Zhai S: Effect of L-carnitine and/or L-acetyl-carnitine in nutrition treatment for male infertility: a systematic review. Asia Pac J Clin Nutr 2007, 16(Suppl 1):383-390.
- [172]Showell MG, Brown J, Yazdani A, Stankiewicz MT, Hart RJ: Antioxidants for male subfertility. Cochrane Database Syst Rev 2011, (1):CD007411. doi: 10.1002/14651858.CD007411.pub2.
- [173]Showell MG, Brown J, Clarke J, Hart RJ: Antioxidants for female subfertility. Cochrane Database Syst Rev 2013., 8CD007807