2017, Number 03
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Ginecol Obstet Mex 2017; 85 (03)
Sperm DNA fragmentation: Current research
Saucedo-de la Llata E, López-Reyes JJ, Moraga-Sánchez MR, Romeu-Sarrió A, Carmona-Ruiz IO
Language: Spanish
References: 174
Page: 164-189
PDF size: 387.66 Kb.
ABSTRACT
Objetive: To review the mechanisms responsible for sperm DNA fragmentation and its methods of analysis. This includes a briefly review about the definition of DNA fragmentation; what characteristics make the sperm unique and different from other cells. We also give a discussion about the impact of the current techniques to evaluate sperm DNA fragmentation and its utility and clinical application. Lastly, there are practice recommendations regarding what our group considers to be the best approach for this subject.
Methodology: Bibliographic search in the databases: Medline, Pubmed, Pubmed Central and Google Scholar with the keywords: DNA fragmentation, sperm DNA fragmentation, fragmentation of human sperm DNA and DNA fragmentation tests.
Conclusion: The integrity of the paternal genome is of crucial importance to reach our goal of a healthy newborn. Current techniques are far from perfect in terms of predictability, selection and results. New technologies may give us the information missing in order to elucidate the role of sperm DNA fragmentation tests in the assisted reproduction lab.
REFERENCES
Hull MG, Glazener CM, Kelly NJ, Conway DI, Foster PA, Hinton RA, Coulson C, Lambert PA, Watt EM, Desai KM: Population study of causes, treatment, and outcome of infertility. Br Med J (Clin Res Ed) 1985, 291(6510):1693- 1697.
Chung CC, Fleming R, Jamieson ME, Yates RW, Coutts JR: Randomized comparison of ovulation induction with and without intrauterine insemination in the treatment of unexplained infertility. Human reproduction 1995, 10(12):3139-3141.
Santiso R, Tamayo M, Gosalvez J, Meseguer M, Garrido N, Fernandez JL: Simultaneous determination in situ of DNA fragmentation and 8-oxoguanine in human sperm. Fertility and sterility 2010, 93(1):314-318.
Velez de la Calle JF, Muller A, Walschaerts M, Clavere JL, Jimenez C, Wittemer C, Thonneau P: Sperm deoxyribonucleic acid fragmentation as assessed by the sperm chromatin dispersion test in assisted reproductive technology programs: results of a large prospective multicenter study. Fertility and sterility 2008, 90(5):1792-1799.
Bungum M, Humaidan P, Axmon A, Spano M, Bungum L, Erenpreiss J, Giwercman A: Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Human reproduction 2007, 22(1):174-179.
Zhao J, Zhang Q, Wang Y, Li Y: Whether sperm deoxyribonucleic acid fragmentation has an effect on pregnancy and miscarriage after in vitro fertilization/intracytoplasmic sperm injection: a systematic review and meta-analysis. Fertility and sterility 2014, 102(4):998-1005 e1008.
Simon L, Lutton D, McManus J, Lewis SE: Sperm DNA damage measured by the alkaline Comet assay as an independent predictor of male infertility and in vitro fertilization success. Fertility and sterility 2011, 95(2):652-657.
Simon L, Lewis SE: Sperm DNA damage or progressive motility: which one is the better predictor of fertilization in vitro? Syst Biol Reprod Med 2011, 57(3):133-138.
Giwercman A, Richthoff J, Hjollund H, Bonde JP, Jepson K, Frohm B, Spano M: Correlation between sperm motility and sperm chromatin structure assay parameters. Fertility and sterility 2003, 80(6):1404-1412.
Lewis SE: Is sperm evaluation useful in predicting human fertility? Reproduction 2007, 134(1):31-40.
Lopes S, Sun JG, Jurisicova A, Meriano J, Casper RF: Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertility and sterility 1998, 69(3):528-532.
Gandini L, Lombardo F, Paoli D, Caruso F, Eleuteri P, Leter G, Ciriminna R, Culasso F, Dondero F, Lenzi A et al: Fullterm pregnancies achieved with ICSI despite high levels of sperm chromatin damage. Human reproduction 2004, 19(6):1409-1417.
Ris H, Mirsky AE: The state of the chromosomes in the interphase nucleus. The Journal of general physiology 1949, 32(4):489-502.
Williamson R: Properties of rapidly labelled deoxyribonucleic acid fragments isolated from the cytoplasm of primary cultures of embryonic mouse liver cells. Journal of molecular biology 1970, 51(1):157-168.
Kitazumi I, Tsukahara M: Regulation of DNA fragmentation: the role of caspases and phosphorylation. FEBS J 2011, 278(3):427-441.
Taatjes DJ, Sobel BE, Budd RC: Morphological and cytochemical determination of cell death by apoptosis. Histochem Cell Biol 2008, 129(1):33-43.
Samejima K, Tone S, Earnshaw WC: CAD/DFF40 nuclease is dispensable for high molecular weight DNA cleavage and stage I chromatin condensation in apoptosis. J Biol Chem 2001, 276(48):45427-45432.
Duncan JS, Turowec JP, Vilk G, Li SS, Gloor GB, Litchfield DW: Regulation of cell proliferation and survival: convergence of protein kinases and caspases. Biochim Biophys Acta 2010, 1804(3):505-510.
Kitazumi I, Maseki Y, Nomura Y, Shimanuki A, Sugita Y, Tsukahara M: Okadaic acid induces DNA fragmentation via caspase-3-dependent and caspase-3-independent pathways in Chinese hamster ovary (CHO)-K1 cells. FEBS J 2010, 277(2):404-412.
Jayaraj R, Gupta N, Rao PV: Multiple signal transduction pathways in okadaic acid induced apoptosis in HeLa cells. Toxicology 2009, 256(1-2):118-127.
Li LY, Luo X, Wang X: Endonuclease G is an apoptotic DNase when released from mitochondria. Nature 2001, 412(6842):95-99.
Chen D, Stetler RA, Cao G, Pei W, O'Horo C, Yin XM, Chen J: Characterization of the rat DNA fragmentation factor 35/Inhibitor of caspase-activated DNase (Short form). The endogenous inhibitor of caspase-dependent DNA fragmentation in neuronal apoptosis. J Biol Chem 2000, 275(49):38508-38517.
Biddie SC, John S: Minireview: Conversing with chromatin: the language of nuclear receptors. Mol Endocrinol 2014, 28(1):3-15.
Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ: Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389(6648):251-260.
Lee DY, Hayes JJ, Pruss D, Wolffe AP: A positive role for histone acetylation in transcription factor access to nucleosomal DNA. Cell 1993, 72(1):73-84.
Miller KM, Tjeertes JV, Coates J, Legube G, Polo SE, Britton S, Jackson SP: Human HDAC1 and HDAC2 function in the DNA-damage response to promote DNA nonhomologous end-joining. Nat Struct Mol Biol 2010, 17(9):1144-1151.
Tachiwana H, Kagawa W, Shiga T, Osakabe A, Miya Y, Saito K, Hayashi-Takanaka Y, Oda T, Sato M, Park SY et al: Crystal structure of the human centromeric nucleosome containing CENP-A. Nature 2011, 476(7359):232-235.
Gonzalez-Marin C, Gosalvez J, Roy R: Types, causes, detection and repair of DNA fragmentation in animal and human sperm cells. Int J Mol Sci 2012, 13(11):14026-14052.
Conwell CC, Vilfan ID, Hud NV: Controlling the size of nanoscale toroidal DNA condensates with static curvature and ionic strength. Proc Natl Acad Sci U S A 2003, 100(16):9296-9301.
Balhorn R: A model for the structure of chromatin in mammalian sperm. The Journal of cell biology 1982, 93(2):298-305.
Barratt CL, Aitken RJ, Bjorndahl L, Carrell DT, de Boer P, Kvist U, Lewis SE, Perreault SD, Perry MJ, Ramos L et al: Sperm DNA: organization, protection and vulnerability: from basic science to clinical applications--a position report. Human reproduction 2010, 25(4):824-838.
Lin MH, Kuo-Kuang Lee R, Li SH, Lu CH, Sun FJ, Hwu YM: Sperm chromatin structure assay parameters are not related to fertilization rates, embryo quality, and pregnancy rates in in vitro fertilization and intracytoplasmic sperm injection, but might be related to spontaneous abortion rates. Fertility and sterility 2008, 90(2):352-359.
Fraser L: Structural damage to nuclear DNA in mammalian spermatozoa: its evaluation techniques and relationship with male infertility. Polish journal of veterinary sciences 2004, 7(4):311-321.
Sakkas D, Alvarez JG: Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertility and sterility 2010, 93(4):1027-1036.
Gosalvez J, Lopez-Fernandez C, Fernandez JL, Gouraud A, Holt WV: Relationships between the dynamics of iatrogenic DNA damage and genomic design in mammalian spermatozoa from eleven species. Mol Reprod Dev 2011, 78(12):951-961.
Robinson L, Gallos ID, Conner SJ, Rajkhowa M, Miller D, Lewis S, Kirkman-Brown J, Coomarasamy A: The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis. Human reproduction 2012, 27(10):2908-2917.
Smith A, Haaf T: DNA nicks and increased sensitivity of DNA to fluorescence in situ end labeling during functional spermiogenesis. Biotechniques 1998, 25(3):496-502.
Balhorn R, Reed S, Tanphaichitr N: Aberrant protamine 1/protamine 2 ratios in sperm of infertile human males. Experientia 1988, 44(1):52-55.
Belokopytova IA, Kostyleva EI, Tomilin AN, Vorob'ev VI: Human male infertility may be due to a decrease of the protamine P2 content in sperm chromatin. Molecular reproduction and development 1993, 34(1):53-57.
Griveau JF, Charbonneau M, Blanchard Y, Lescoat D, Le Lannou D: Decondensation of human sperm nuclei and HP1 protamine degradation from normospermia and asthenospermia in Xenopus egg extracts. Archives of andrology 1992, 29(2):127-136.
Billig H, Chun SY, Eisenhauer K, Hsueh AJ: Gonadal cell apoptosis: hormone-regulated cell demise. Hum Reprod Update 1996, 2(2):103-117.
Pentikainen V, Erkkila K, Dunkel L: Fas regulates germ cell apoptosis in the human testis in vitro. Am J Physiol 1999, 276(2 Pt 1):E310-316.
Sakkas D, Mariethoz E, Manicardi G, Bizzaro D, Bianchi PG, Bianchi U: Origin of DNA damage in ejaculated human spermatozoa. Rev Reprod 1999, 4(1):31-37.
Burrello N, Arcidiacono G, Vicari E, Asero P, Di Benedetto D, De Palma A, Romeo R, D'Agata R, Calogero AE: Morphologically normal spermatozoa of patients with secretory oligo-astheno-teratozoospermia have an increased aneuploidy rate. Human reproduction 2004, 19(10):2298-2302.
McPherson S, Longo FJ: Chromatin structure-function alterations during mammalian spermatogenesis: DNA nicking and repair in elongating spermatids. Eur J Histochem 1993, 37(2):109-128.
McPherson SM, Longo FJ: Nicking of rat spermatid and spermatozoa DNA: possible involvement of DNA topoisomerase II. Dev Biol 1993, 158(1):122-130.
Marcon L, Boissonneault G: Transient DNA strand breaks during mouse and human spermiogenesis new insights in stage specificity and link to chromatin remodeling. Biol Reprod 2004, 70(4):910-918.
Ollero M, Gil-Guzman E, Lopez MC, Sharma RK, Agarwal A, Larson K, Evenson D, Thomas AJ, Jr., Alvarez JG: Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Human reproduction 2001, 16(9):1912-1921.
Greco E, Scarselli F, Iacobelli M, Rienzi L, Ubaldi F, Ferrero S, Franco G, Anniballo N, Mendoza C, Tesarik J: Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Human reproduction 2005, 20(1):226-230.
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):831-835.
Suganuma R, Yanagimachi R, Meistrich ML: Decline in fertility of mouse sperm with abnormal chromatin during epididymal passage as revealed by ICSI. Human reproduction 2005, 20(11):3101-3108.
Banks S, King SA, Irvine DS, Saunders PT: Impact of a mild scrotal heat stress on DNA integrity in murine spermatozoa. Reproduction 2005, 129(4):505-514.
Sailer BL, Sarkar LJ, Bjordahl JA, Jost LK, Evenson DP: Effects of heat stress on mouse testicular cells and sperm chromatin structure. J Androl 1997, 18(3):294-301.
Bianchi PG, Manicardi GC, Bizzaro D, Bianchi U, Sakkas D: Effect of deoxyribonucleic acid protamination on fluorochrome staining and in situ nick-translation of murine and human mature spermatozoa. Biol Reprod 1993, 49(5):1083-1088.
Morris ID: Sperm DNA damage and cancer treatment. Int J Androl 2002, 25(5):255-261.
O'Flaherty C, Vaisheva F, Hales BF, Chan P, Robaire B: Characterization of sperm chromatin quality in testicular cancer and Hodgkin's lymphoma patients prior to chemotherapy. Human reproduction 2008, 23(5):1044-1052.
Rubes J, Selevan SG, Sram RJ, Evenson DP, Perreault SD: GSTM1 genotype influences the susceptibility of men to sperm DNA damage associated with exposure to air pollution. Mutat Res 2007, 625(1-2):20-28.
de Paula T, Bertolla R, Spaine D, Cunha M, Schor N, Cedenho A: Effect of cryopreservation on sperm apoptotic deoxyribonucleic acid fragmentation in patients with oligozoospermia. Fertil Steril 2006, 86:597 - 600.
Thomson L, Fleming S, Aitken R, De Iuliis G, Zieschang J, Clark A: Cryopreservation-induced human sperm DNA damage is predominantly mediated by oxidative stress rather than apoptosis. Hum Reprod 2009, 24:2061 - 2070.
Frainais C, Vialard F, Rougier N, Aegerther P, Damond F, Ayel J, Yazbeck C, Hazout A, Selva J: Impact of freezing/thawing technique on sperm DNA integrity in HIV-1 patients. J Assist Reprod Genet 2010, 27:415 - 421.
Kimmins S, Sassone-Corsi P: Chromatin remodelling and epigenetic features of germ cells. Nature 2005, 434(7033):583-589.
Meyer-Ficca ML, Scherthan H, Burkle A, Meyer RG: Poly(ADP-ribosyl)ation during chromatin remodeling steps in rat spermiogenesis. Chromosoma 2005, 114(1):67-74.
Leduc F, Maquennehan V, Nkoma GB, Boissonneault G: DNA damage response during chromatin remodeling in elongating spermatids of mice. Biol Reprod 2008, 78(2):324-332.
Brugmans L, Kanaar R, Essers J: Analysis of DNA doublestrand break repair pathways in mice. Mutat Res 2007, 614(1-2):95-108.
Neal JA, Meek K: Choosing the right path: does DNA-PK help make the decision? Mutat Res 2011, 711(1-2):73-86.
Audebert M, Salles B, Calsou P: Involvement of poly(ADPribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J Biol Chem 2004, 279(53):55117-55126.
Ahmed EA, de Boer P, Philippens ME, Kal HB, de Rooij DG: Parp1-XRCC1 and the repair of DNA double strand breaks in mouse round spermatids. Mutat Res 2010, 683(1-2):84-90.
Pandita TK, Richardson C: Chromatin remodeling finds its place in the DNA double-strand break response. Nucleic Acids Res 2009, 37(5):1363-1377.
Kinner A, Wu W, Staudt C, Iliakis G: Gamma-H2AX in recognition and signaling of DNA double-strand breaks in the context of chromatin. Nucleic Acids Res 2008, 36(17):5678-5694.
Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Lobrich M, Jeggo PA: ATM signaling facilitates repair of DNA doublestrand breaks associated with heterochromatin. Mol Cell 2008, 31(2):167-177.
Gavrieli Y, Sherman Y, Ben-Sasson SA: Identification of programmed cell death in situ via specific labeling of nuclear DNA fragmentation. The Journal of cell biology 1992, 119(3):493-501.
Sergerie M, Laforest G, Bujan L, Bissonnette F, Bleau G: Sperm DNA fragmentation: threshold value in male fertility. Human reproduction 2005, 20(12):3446-3451.
Sergerie M, Laforest G, Boulanger K, Bissonnette F, Bleau G: Longitudinal study of sperm DNA fragmentation as measured by terminal uridine nick end-labelling assay. Human reproduction 2005, 20(7):1921-1927.
Ostling O, Johanson KJ: Microelectrophoretic study of radiation-induced DNA damages in individual mammalian cells. Biochemical and biophysical research communications 1984, 123(1):291-298.
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. Molecular human reproduction 1996, 2(8):613-619.
Simon L, Carrell DT: Sperm DNA damage measured by comet assay. Methods Mol Biol 2013, 927:137-146.
Lewis SE, John Aitken R, Conner SJ, Iuliis GD, Evenson DP, Henkel R, Giwercman A, Gharagozloo P: The impact of sperm DNA damage in assisted conception and beyond: recent advances in diagnosis and treatment. Reproductive biomedicine online 2013, 27(4):325-337.
Simon L, Proutski I, Stevenson M, Jennings D, McManus J, Lutton D, Lewis SE: Sperm DNA damage has a negative association with live-birth rates after IVF. Reproductive biomedicine online 2013, 26(1):68-78.
Evenson DP, Jost LK, Baer RK, Turner TW, Schrader SM: Individuality of DNA denaturation patterns in human sperm as measured by the sperm chromatin structure assay. Reproductive toxicology 1991, 5(2):115-125.
Darzynkiewicz Z, Traganos F, Sharpless T, Melamed MR: Thermal denaturation of DNA in situ as studied by acridine orange staining and automated cytofluorometry. Exp Cell Res 1975, 90(2):411-428.
Evenson DP, Jost LK, Marshall D, Zinaman MJ, Clegg E, Purvis K, de Angelis P, Claussen OP: Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Human reproduction 1999, 14(4):1039-1049.
Osman A, Alsomait H, Seshadri S, El-Toukhy T, Khalaf Y: The effect of sperm DNA fragmentation on live birth rate after IVF or ICSI: a systematic review and meta-analysis. Reproductive biomedicine online 2014.
Benchaib M, Lornage J, Mazoyer C, Lejeune H, Salle B, Francois Guerin J: Sperm deoxyribonucleic acid fragmentation as a prognostic indicator of assisted reproductive technology outcome. Fertility and sterility 2007, 87(1):93-100.
Boe-Hansen GB, Fedder J, Ersboll AK, Christensen P: The sperm chromatin structure assay as a diagnostic tool in the human fertility clinic. Human reproduction 2006, 21(6):1576-1582.
Borini A, Tarozzi N, Bizzaro D, Bonu MA, Fava L, Flamigni C, Coticchio G: Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART. Human reproduction 2006, 21(11):2876-2881.
Frydman N, Prisant N, Hesters L, Frydman R, Tachdjian G, Cohen-Bacrie P, Fanchin R: Adequate ovarian follicular status does not prevent the decrease in pregnancy rates associated with high sperm DNA fragmentation. Fertility and sterility 2008, 89(1):92-97.
Host E, Lindenberg S, Smidt-Jensen S: The role of DNA strand breaks in human spermatozoa used for IVF and ICSI. Acta obstetricia et gynecologica Scandinavica 2000, 79(7):559-563.
Larson KL, DeJonge CJ, Barnes AM, Jost LK, Evenson DP: Sperm chromatin structure assay parameters as predictors of failed pregnancy following assisted reproductive techniques. Human reproduction 2000, 15(8):1717-1722.
Simon L, Brunborg G, Stevenson M, Lutton D, McManus J, Lewis SE: Clinical significance of sperm DNA damage in assisted reproduction outcome. Human reproduction 2010, 25(7):1594-1608.
Fernandez JL, Muriel L, Rivero MT, Goyanes V, Vazquez R, Alvarez JG: The sperm chromatin dispersion test: a simple method for the determination of sperm DNA fragmentation. J Androl 2003, 24(1):59-66.
Fernandez JL, Muriel L, Goyanes V, Segrelles E, Gosalvez J, Enciso M, LaFromboise M, De Jonge C: Simple determination of human sperm DNA fragmentation with an improved sperm chromatin dispersion test. Fertility and sterility 2005, 84(4):833-842.
Enciso M, Muriel L, Fernandez JL, Goyanes V, Segrelles E, Marcos M, Montejo JM, Ardoy M, Pacheco A, Gosalvez J: Infertile men with varicocele show a high relative proportion of sperm cells with intense nuclear damage level, evidenced by the sperm chromatin dispersion test. Journal of andrology 2006, 27(1):106-111.
Fernandez JL, Cajigal D, Lopez-Fernandez C, Gosalvez J: Assessing sperm DNA fragmentation with the sperm chromatin dispersion test. Methods in molecular biology 2011, 682:291-301.
Pregl Breznik B, Kovacic B, Vlaisavljevic V: Are sperm DNA fragmentation, hyperactivation, and hyaluronan-binding ability predictive for fertilization and embryo development in in vitro fertilization and intracytoplasmic sperm injection? Fertility and sterility 2013, 99(5):1233-1241.
Sun JG, Jurisicova A, Casper RF: Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro. Biol Reprod 1997, 56(3):602-607.
Lopes S, Jurisicova A, Casper RF: Gamete-specific DNA fragmentation in unfertilized human oocytes after intracytoplasmic sperm injection. Human reproduction 1998, 13(3):703-708.
Henkel R, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C, Menkveld R, Gips H, Schill W, Kruger T: Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril 2004, 81:965 - 972.
Tesarik J, Greco E, Mendoza C: Late, but not early, paternal effect on human embryo development is related to sperm DNA fragmentation. Hum Reprod 2004, 19:611 - 615.
Nasr-Esfahani M, Salehi M, Razavi S, Anjomshoa M, Rozbahani S, Moulavi F, Mardani M: Effect of sperm DNA damage and sperm protamine deficiency on fertilization and embryo development post-ICSI. Reprod Biomed Online 2005, 11:198 - 205.
Aitken R, Baker M: Oxidative stress, sperm survival and fertility control. Mol Cell Endocrinol 2006, 250:66 - 69.
Evgeni E, Charalabopoulos K, Asimakopoulos B: Human Sperm DNA Fragmentation and its Correlation with Conventional Semen Parameters. Journal of reproduction & infertility 2014, 15(1):2-14.
Nallella KP, Sharma RK, Aziz N, Agarwal A: Significance of sperm characteristics in the evaluation of male infertility. Fertility and sterility 2006, 85(3):629-634.
Haidl G, Allam JP, Schuppe HC: Chronic epididymitis: impact on semen parameters and therapeutic options. Andrologia 2008, 40(2):92-96.
Jequier AM: Semen analysis: a new manual and its application to the understanding of semen and its pathology. Asian journal of andrology 2010, 12(1):11-13.
Aitken RJ: Whither must spermatozoa wander? The future of laboratory seminology. Asian J Androl 2010, 12(1):99-103.
Andrade-Rocha FT: Semen analysis in laboratory practice: an overview of routine tests. Journal of clinical laboratory analysis 2003, 17(6):247-258.
Spano M, Seli E, Bizzaro D, Manicardi GC, Sakkas D: The significance of sperm nuclear DNA strand breaks on reproductive outcome. Current opinion in obstetrics & gynecology 2005, 17(3):255-260.
Acharyya S, Kanjilal S, Bhattacharyya AK: Does human sperm nuclear DNA integrity affect embryo quality? Indian journal of experimental biology 2005, 43(11):1016-1022.
Wyrobek AJ, Eskenazi B, Young S, Arnheim N, Tiemann- Boege I, Jabs EW, Glaser RL, Pearson FS, Evenson D: Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(25):9601-9606.
Younglai EV, Holt D, Brown P, Jurisicova A, Casper RF: Sperm swim-up techniques and DNA fragmentation. Human reproduction 2001, 16(9):1950-1953.
Liu CH, Tsao HM, Cheng TC, Wu HM, Huang CC, Chen CI, Lin DP, Lee MS: DNA fragmentation, mitochondrial dysfunction and chromosomal aneuploidy in the spermatozoa of oligoasthenoteratozoospermic males. Journal of assisted reproduction and genetics 2004, 21(4):119-126.
Perrin A, Caer E, Oliver-Bonet M, Navarro J, Benet J, Amice V, De Braekeleer M, Morel F: DNA fragmentation and meiotic segregation in sperm of carriers of a chromosomal structural abnormality. Fertility and sterility 2009, 92(2):583-589.
Tang SS, Gao H, Zhao Y, Ma S: Aneuploidy and DNA fragmentation in morphologically abnormal sperm. International journal of andrology 2010, 33(1):e163-179.
Menkveld R, Holleboom CA, Rhemrev JP: Measurement and significance of sperm morphology. Asian journal of andrology 2011, 13(1):59-68.
Ombelet W, Wouters E, Boels L, Cox A, Janssen M, Spiessens C, Vereecken A, Bosmans E, Steeno O: Sperm morphology assessment: diagnostic potential and comparative analysis of strict or WHO criteria in a fertile and a subfertile population. Int J Androl 1997, 20(6):367-372.
Xia Y, Cheng S, Bian Q, Xu L, Collins MD, Chang HC, Song L, Liu J, Wang S, Wang X: Genotoxic effects on spermatozoa of carbaryl-exposed workers. Toxicological sciences : an official journal of the Society of Toxicology 2005, 85(1):615-623.
Karydis S, Asimakopoulos B, Papadopoulos N, Vakalopoulos I, Al-Hasani S, Nikolettos N: ICSI outcome is not associated with the incidence of spermatozoa with abnormal chromatin condensation. In vivo 2005, 19(5):921-925.
Sun F, Ko E, Martin RH: Is there a relationship between sperm chromosome abnormalities and sperm morphology? Reproductive biology and endocrinology : RB&E 2006, 4:1.
Barratt CL, Mansell S, Beaton C, Tardif S, Oxenham SK: Diagnostic tools in male infertility-the question of sperm dysfunction. Asian J Androl 2011, 13(1):53-58.
Huszar G, Jakab A, Sakkas D, Ozenci CC, Cayli S, Delpiano E, Ozkavukcu S: Fertility testing and ICSI sperm selection by hyaluronic acid binding: clinical and genetic aspects. Reproductive biomedicine online 2007, 14(5):650-663.
Dam AH, Feenstra I, Westphal JR, Ramos L, van Golde RJ, Kremer JA: Globozoospermia revisited. Human reproduction update 2007, 13(1):63-75.
Bungum M, Bungum L, Giwercman A: Sperm chromatin structure assay (SCSA): a tool in diagnosis and treatment of infertility. Asian journal of andrology 2011, 13(1):69-75.
Zenzes MT: Smoking and reproduction: gene damage to human gametes and embryos. Hum Reprod Update 2000, 6(2):122-131.
Perrin J, Tassistro V, Mandon M, Grillo JM, Botta A, Sari- Minodier I: Tobacco consumption and benzo(a)pyrenediol- epoxide-DNA adducts in spermatozoa: in smokers, swim-up procedure selects spermatozoa with decreased DNA damage. Fertility and sterility 2011, 95(6):2013-2017.
Hughes EG, Brennan BG: Does cigarette smoking impair natural or assisted fecundity? Fertility and sterility 1996, 66(5):679-689.
Bolumar F, Olsen J, Boldsen J: Smoking reduces fecundity: a European multicenter study on infertility and subfecundity. The European Study Group on Infertility and Subfecundity. American journal of epidemiology 1996, 143(6):578-587.
Midgette AS, Baron JA: Cigarette smoking and the risk of natural menopause. Epidemiology 1990, 1(6):474-480.
Sims P, Grover PL, Swaisland A, Pal K, Hewer A: Metabolic activation of benzo(a)pyrene proceeds by a diol-epoxide. Nature 1974, 252(5481):326-328.
Denissenko MF, Pao A, Tang M, Pfeifer GP: Preferential formation of benzo[a]pyrene adducts at lung cancer mutational hotspots in P53. Science 1996, 274(5286):430-432.
Benowitz NL, Kuyt F, Jacob P, 3rd, Jones RT, Osman AL: Cotinine disposition and effects. Clin Pharmacol Ther 1983, 34(5):604-611.
Rosa M, Pacifici R, Altieri I, Pichini S, Ottaviani G, Zuccaro P: How the steady-state cotinine concentration in cigarette smokers is directly related to nicotine intake. Clin Pharmacol Ther 1992, 52(3):324-329.
Pacifici R, Altieri I, Gandini L, Lenzi A, Pichini S, Rosa M, Zuccaro P, Dondero F: Nicotine, cotinine, and trans-3-hydroxycotinine levels in seminal plasma of smokers: effects on sperm parameters. Ther Drug Monit 1993, 15(5):358-363.
Pacifici R, Altieri I, Gandini L, Lenzi A, Passa AR, Pichini S, Rosa M, Zuccaro P, Dondero F: Environmental tobacco smoke: nicotine and cotinine concentration in semen. Environ Res 1995, 68(1):69-72.
Vine MF, Hulka BS, Margolin BH, Truong YK, Hu PC, Schramm MM, Griffith JD, McCann M, Everson RB: Cotinine concentrations in semen, urine, and blood of smokers and nonsmokers. Am J Public Health 1993, 83(9):1335-1338.
Bentley KS, Working PK: Use of seminiferous tubule segments to study stage specificity of unscheduled DNA synthesis in rat spermatogenic cells. Environmental and molecular mutagenesis 1988, 12(3):285-297.
Zenzes MT, Puy LA, Bielecki R, Reed TE: Detection of benzo[a]pyrene diol epoxide-DNA adducts in embryos from smoking couples: evidence for transmission by spermatozoa. Molecular human reproduction 1999, 5(2):125-131.
Sepaniak S, Forges T, Gerard H, Foliguet B, Bene MC, Monnier-Barbarino P: The influence of cigarette smoking on human sperm quality and DNA fragmentation. Toxicology 2006, 223(1-2):54-60.
Niu ZH, Liu JB, Shi TY, Yuan Y, Shi HJ: [Impact of cigarette smoking on human sperm DNA integrity]. Zhonghua nan ke xue = National journal of andrology 2010, 16(4):300-304.
Morris ID, Ilott S, Dixon L, Brison DR: The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) and its relationship to fertilization and embryo development. Human reproduction 2002, 17(4):990-998.
Evenson D, Wixon R: Meta-analysis of sperm DNA fragmentation using the sperm chromatin structure assay. Reproductive biomedicine online 2006, 12(4):466-472.
Collins JA, Barnhart KT, Schlegel PN: Do sperm DNA integrity tests predict pregnancy with in vitro fertilization? Fertility and sterility 2008, 89(4):823-831.
Ozmen B, Koutlaki N, Youssry M, Diedrich K, Al-Hasani S: DNA damage of human spermatozoa in assisted reproduction: origins, diagnosis, impacts and safety. Reproductive biomedicine online 2007, 14(3):384-395.
Li Z, Wang L, Cai J, Huang H: Correlation of sperm DNA damage with IVF and ICSI outcomes: a systematic review and meta-analysis. Journal of assisted reproduction and genetics 2006, 23(9-10):367-376.
Zini A, Jamal W, Cowan L, Al-Hathal N: Is sperm DNA damage associated with IVF embryo quality? A systematic review. Journal of assisted reproduction and genetics 2011, 28(5):391-397.
Zini A, Boman JM, Belzile E, Ciampi A: Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Human reproduction 2008, 23(12):2663-2668.
Seli E, Gardner DK, Schoolcraft WB, Moffatt O, Sakkas D: Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertility and sterility 2004, 82(2):378-383.
Genesca A, Caballin MR, Miro R, Benet J, Germa JR, Egozcue J: Repair of human sperm chromosome aberrations in the hamster egg. Hum Genet 1992, 89(2):181-186.
Parinaud J, Mieusset R, Vieitez G, Labal B, Richoilley G: Influence of sperm parameters on embryo quality. Fertility and sterility 1993, 60(5):888-892.
Twigg JP, Irvine DS, Aitken RJ: Oxidative damage to DNA in human spermatozoa does not preclude pronucleus formation at intracytoplasmic sperm injection. Human reproduction 1998, 13(7):1864-1871.
Carrell DT, Liu L, Peterson CM, Jones KP, Hatasaka HH, Erickson L, Campbell B: Sperm DNA fragmentation is increased in couples with unexplained recurrent pregnancy loss. Arch Androl 2003, 49(1):49-55.
Pryor WA, Stone K, Zang LY, Bermudez E: Fractionation of aqueous cigarette tar extracts: fractions that contain the tar radical cause DNA damage. Chemical research in toxicology 1998, 11(5):441-448.
Zang LY, Stone K, Pryor WA: Detection of free radicals in aqueous extracts of cigarette tar by electron spin resonance. Free radical biology & medicine 1995, 19(2):161-167.
Santos EP, Lopez-Costa S, Chenlo P, Pugliese MN, Curi S, Ariagno J, Repetto H, Sardi M, Palaoro L, Mendeluk G: Impact of spontaneous smoking cessation on sperm quality: case report. Andrologia 2011, 43(6):431-435.
Ma E, Chan T, Zhang O, Yang JS, Wang YY, Li YC, Ho R, Lai C, Lam PY: Effectiveness of acupuncture for smoking cessation in a Chinese population. Asia Pac J Public Health 2015, 27(2):NP2610-2622.
White AR, Rampes H, Liu JP, Stead LF, Campbell J: Acupuncture and related interventions for smoking cessation. Cochrane Database Syst Rev 2014, 1:CD000009.
Jackson R, Bormann C, Hassun P, Rocha A, Motta E, Serafini P, Smith G: Effects of semen storage and separation techniques on sperm DNA fragmentation. Fertil Steril 2010, 94:2626 - 2630.
Brahem S, Mehdi M, Elghezal H, Saad A: Semen processing by density gradient centrifugation is useful in selecting sperm with higher double-strand DNA integrity. Andrologia 2011, 43:196 - 202.
Jayaraman V, Upadhya D, Narayan PK, Adiga SK: Sperm processing by swim-up and density gradient is effective in elimination of sperm with DNA damage. Journal of assisted reproduction and genetics 2012, 29(6):557-563.
Said T, Agarwal A, Grunewald S, Rasch M, Baumann T, Kriegel C, Li L, Glander H, Thomas AJ, Paasch U: Selection of nonapoptotic spermatozoa as a new tool for enhancing assisted reproduction outcomes: an in vitro model. Biol Reprod 2006, 74:530 - 537.
Hoogendijk C, Kruger T, Bouic P, Henkel R: A novel approach for the selection of human sperm using annexin V-binding and flow cytometry. Fertil Steril 2009, 91:1285 - 1292.
Rawe V, Boudri H, Alvarez Sedó C, Carro M, Papier S, Nodar F: Healthy baby born after reduction of sperm DNA fragmentation using cell sorting before ICSI. Reprod Biomed Online 2010, 20:320 - 323.
Polak de Fried E, Denaday F: Single and twin ongoing pregnancies in two cases of previous ART failure after ICSI performed with sperm sorted using annexin V microbeads. Fertility and sterility 2010, 94(1):351 e315-358.
Rawe VY, Boudri HU, Alvarez Sedo C, Carro M, Papier S, Nodar F: Healthy baby born after reduction of sperm DNA fragmentation using cell sorting before ICSI. Reproductive biomedicine online 2010, 20(3):320-323.
Jakab A, Sakkas D, Delpiano E, Cayli S, Kovanci E, Ward D, Revelli A, Huszar G: Intracytoplasmic sperm injection: a novel selection method for sperm with normal frequency of chromosomal aneuploidies. Fertility and sterility 2005, 84(6):1665-1673.
Parmegiani L, Cognigni GE, Ciampaglia W, Pocognoli P, Marchi F, Filicori M: Efficiency of hyaluronic acid (HA) sperm selection. Journal of assisted reproduction and genetics 2010, 27(1):13-16.
Tarozzi N, Nadalini M, Bizzaro D, Serrao L, Fava L, Scaravelli G, Borini A: Sperm-hyaluronan-binding assay: clinical value in conventional IVF under Italian law. Reproductive biomedicine online 2009, 19 Suppl 3:35-43.
Sakkas D: Novel technologies for selecting the best sperm for in vitro fertilization and intracytoplasmic sperm injection. Fertility and sterility 2013, 99(4):1023-1029.
Ahmadi A, Ng SC: Fertilizing ability of DNA-damaged spermatozoa. The Journal of experimental zoology 1999, 284(6):696-704.
Jaroudi S, Kakourou G, Cawood S, Doshi A, Ranieri DM, Serhal P, Harper JC, SenGupta SB: Expression profiling of DNA repair genes in human oocytes and blastocysts using microarrays. Human reproduction 2009, 24(10):2649-2655.
Hamatani T, Falco G, Carter MG, Akutsu H, Stagg CA, Sharov AA, Dudekula DB, VanBuren V, Ko MS: Age-associated alteration of gene expression patterns in mouse oocytes. Human molecular genetics 2004, 13(19):2263-2278.
Henkel R, Kierspel E, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C, Menkveld R, Schill WB, Kruger TF: DNA fragmentation of spermatozoa and assisted reproduction technology. Reproductive biomedicine online 2003, 7(4):477-484.
Ming L, Yuan C, Ping L, Jie Q: Higher abnormal fertilization, higher cleavage rate, and higher arrested embryos rate were found in conventional IVF than in intracytoplasmic sperm injection. Clin Exp Obstet Gynecol 2015, 42(3):372- 375.
European IVFMC, European Society of Human R, Embryology, Kupka MS, D'Hooghe T, Ferraretti AP, de Mouzon J, Erb K, Castilla JA, Calhaz-Jorge C et al: Assisted reproductive technology in Europe, 2011: results generated from European registers by ESHREdagger. Hum Reprod 2016, 31(2):233-248.
Sakkas D, Ramalingam M, Garrido N, Barratt CL: Sperm selection in natural conception: what can we learn from Mother Nature to improve assisted reproduction outcomes? Hum Reprod Update 2015, 21(6):711-726.
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