A plea for a more physiological ICSI
Corresponding Author
T. Ebner
Landes- Frauen- und Kinderklinik, Kinderwunsch Zentrum, Linz, Upper Austria, Austria
Correspondence
Assoc. Prof. Dr. Thomas Ebner, Kinderwunsch Zentrum, Landes- Frauen- und Kinderklinik, Krankenhausstr. 26-30, A-4020 Linz, Austria.
Tel.: 0043-732-6923-24605;
Fax: 0043-732-6923-24604;
E-mail:[email protected]
Search for more papers by this authorM. Filicori
GynePro Medical Centers, Reproductive Medicine Unit, Bologna, Italy
Search for more papers by this authorG. Tews
Landes- Frauen- und Kinderklinik, Kinderwunsch Zentrum, Linz, Upper Austria, Austria
Search for more papers by this authorL. Parmegiani
GynePro Medical Centers, Reproductive Medicine Unit, Bologna, Italy
Search for more papers by this authorCorresponding Author
T. Ebner
Landes- Frauen- und Kinderklinik, Kinderwunsch Zentrum, Linz, Upper Austria, Austria
Correspondence
Assoc. Prof. Dr. Thomas Ebner, Kinderwunsch Zentrum, Landes- Frauen- und Kinderklinik, Krankenhausstr. 26-30, A-4020 Linz, Austria.
Tel.: 0043-732-6923-24605;
Fax: 0043-732-6923-24604;
E-mail:[email protected]
Search for more papers by this authorM. Filicori
GynePro Medical Centers, Reproductive Medicine Unit, Bologna, Italy
Search for more papers by this authorG. Tews
Landes- Frauen- und Kinderklinik, Kinderwunsch Zentrum, Linz, Upper Austria, Austria
Search for more papers by this authorL. Parmegiani
GynePro Medical Centers, Reproductive Medicine Unit, Bologna, Italy
Search for more papers by this authorSummary
Intracytoplasmic sperm injection (ICSI) can be considered the most ‘revolutionary’ in vitro insemination technique because it has efficiently allowed the treatment of male factor infertility. Although ICSI has been successfully and safely applied worldwide for almost 20 years, currently, we have no real knowledge regarding the hypothetical long-term side effects on ICSI adults, given the increased likelihood of spermatozoa with defective nuclear content fertilising the oocytes. The aim of this review article is to investigate the most recent advances of performing ICSI in the safest possible manner, thus, minimising the theoretical hazards of this procedure. To allow for substantiated recommendation which male gametes to choose for physiological ICSI an updated search was performed in Medline and Embase, from 1996 to June 2011. Recent technical advances allow operators to more or less simulate physiological conditions in the laboratory, reducing potential damage to the gametes. It seems possible to prevent fertilisation by DNA-damaged and chromosomal-unbalanced spermatozoa by selecting ICSI sperm by motility and/or maturation markers such as hyaluronic acid or other zona pellucida receptors. Furthermore, novel non-invasive imaging techniques can be valid tools for helping in the morphological selection of ICSI spermatozoa.
References
- Ahmad L, Jalali S, Shami SA, Akram Z (2007) Sperm preparation: DNA damage by comet assay in normo- and teratozoospermics. Arch Androl 53: 325–338.
-
Ahmadi A, Ng SC (1999a) Fertilizing ability of DNA-damaged spermatozoa. J Exp Zool 284: 696–704.
10.1002/(SICI)1097-010X(19991101)284:6<696::AID-JEZ11>3.0.CO;2-E CAS PubMed Web of Science® Google Scholar
- Ahmadi A, Ng SC (1999b) Developmental capacity of damaged spermatozoa. Hum Reprod 14: 2279–2284.
- Alvarez JG (2005) The predictive value of sperm chromatin structure assay. Hum Reprod 20: 2365–2367.
- Antinori M, Licata E, Dani G, Cerusico F, Versaci C, D'angelo D, Antinori S (2008) Intracytoplasmic morphologically selected sperm injection: a prospective randomized trial. Reprod Biomed Online 16: 835–841.
- Avendaño C, Oehninger S (2011) DNA fragmentation in morphologically normal spermatozoa: how much should we be concerned in the ICSI era? J Androl 32: 356–363.
- Avendaño C, Franchi A, Duran H, Oehninger S (2010) DNA fragmentation of normal spermatozoa negatively impacts embryo quality and intracytoplasmic sperm injection outcome. Fertil Steril 94: 549–557.
- Baccetti B (2004) Microscopical advances in assisted reproduction. J Submicrosc Cytol Pathol 36: 333–339.
- Balaban B, Lundin K, Morrell JM, Tjellström H, Urman B, Holmes PV (2003) An alternative to PVP for slowing sperm prior to ICSI. Hum Reprod 18: 1887–1889.
- Balaban B, Yakin K, Alatas C, Oktem O, Isiklar A, Urman B (2011) Clinical outcome of intracytoplasmic injection of spermatozoa morphologically selected under high magnification: a prospective randomized study. Reprod Biomed Online 22: 472–476
- Barak Y, Menezo Y, Veiga A, Elder K (2001) A physiological replacement for polyvinylpyrrolidone (PVP) in assisted reproductive technology. Hum Fertil (Camb) 4: 99–103.
- Bartoov B, Eltes F, Pansky M, Langzam J, Reichart M, Soffer Y (1994) Improved diagnosis of male fertility potential via a combination of quantitative ultramorphology and routine semen analyses. Hum Reprod 9: 2069–2075.
- Bartoov B, Berkovitz A, Eltes F (2001) Selection of spermatozoa with normal nuclei to improve the pregnancy rate with intracytoplasmic sperm injection. N Engl J Med 345: 1067–1068.
- Bartoov B, Berkovitz A, Eltes F, Kogosowski A, Menezo Y, Barak Y (2002) Real-time fine morphology of motile human sperm cells is associated with IVF-ICSI outcome. J Androl 23: 1–8.
- Bartoov B, Berkovitz A, Eltes F, Kogosovsky A, Yagoda A, Lederman H, Artzi S, Gross M, Barak Y (2003) Pregnancy rates are higher with intracytoplasmic morphologically selected sperm injection than with conventional intracytoplasmic injection. Fertil Steril 80: 1413–1419.
- Bellver J, Meseguer M, Muriel L, García-Herrero S, Barreto MA, Garda AL, Remohí J, Pellicer A, Garrido N (2010) Chromosome microdeletions, sperm DNA fragmentation and sperm oxidative stress as causes of recurrent spontaneous abortion of unknown etiology. Hum Reprod 25: 1713–1721.
- Belva F, De Schrijver F, Tournaye H, Liebaers I, Devroey P, Haentjens P, Bonduelle M (2011) Neonatal outcome of 724 children born after ICSI using non-ejaculated sperm. Hum Reprod 7: 1752–1758.
- Benchaib M, Braun V, Lornage J, Hadj S, Salle B, Lejeune H, Guérin JF (2003) Sperm DNA fragmentation decreases the pregnancy rate in an assisted reproductive technique. Hum Reprod 18: 1023–1028.
- Berkovitz A, Eltes F, Yaari S, Katz N, Barr I, Fishman A, Bartoov B (2005) The morphological normalcy of the sperm nucleus and pregnancy rate of intracytoplasmic injection with morphologically selected sperm. Hum Reprod 20: 185–190.
- Berkovitz A, Eltes F, Ellenbogen A, Peer S, Feldberg D, Bartoov B (2006a) Does the presence of nuclear vacuoles in human sperm selected for ICSI affect pregnancy outcome? Hum Reprod 21: 1787–1790.
- Berkovitz A, Eltes F, Lederman H, Peer S, Ellenbogen A, Feldberg B, Bartoov B (2006b) How to improve IVF-ICSI outcome by sperm selection. Reprod Biomed Online 12: 634–638.
- Billig H, Chun SY, Eisenhauer K, Hsueh AJ (1996) Gonadal cell apoptosis: hormone-regulated cell demise. Hum Reprod Update 2: 103–117.
- Black M, Liu de Y, Bourne H, Baker HW (2010) Comparison of outcomes of conventional intracytoplasmic sperm injection and intracytoplasmic sperm injection using sperm bound to the zona pellucida of immature oocytes. Fertil Steril 93: 672–674.
- Boe-Hansen GB, Ersboll AK, Christensen P (2005) Variability and laboratory factors affecting the sperm chromatin structure assay in human semen. J Androl 26: 360–368.
- Boitrelle F, Ferfouri F, Petit JM, Segretain D, Tourain C, Bergere M, Bailly M, Vialard F, Albert M, Selva J (2011) Large human sperm vacuoles observed in motile spermatozoa under high magnification: nuclear thumbprints linked to failure of chromatin condensation. Hum Reprod 7: 1650–1658.
- Bonduelle M, Van Assche E, Joris H, Keymolen K, Devroey P, Van Steriteghem A, Liebaers I (2002) Prenatal testing in ICSI pregnancies: incidence of chromosomal anomalies in 1586 karyotypes and relation to sperm parameters. Hum Reprod 17: 2600–2614.
- Borini A, Tarozzi N, Bizzaro D, Bonu MA, Fava L, Flamigni C, Coticchio G (2006) Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART. Hum Reprod 21: 2876–2881.
- Bungum M, Humaidan P, Spano M, Jepson K, Bungum L, Giwercman A (2004) The predictive value of sperm chromatin structure assay (SCSA) parameters for the outcome of intrauterine insemination, IVF and ICSI. Hum Reprod 19: 1401–1408.
- Bungum M, Humaidan P, Axmon A, Spanò M, Bungum L, Erenpreiss J, Giwercman A (2007) Sperm DNA integrity assessment in prediction of assisted reproduction technology outcome. Hum Reprod 22: 174–179.
- Bungum M, Spanò M, Humaidan P, Eleuteri P, Rescia M, Giwercman A (2008) Sperm chromatin structure assay parameters measured after density gradient centrifugation are not predictive for the outcome of ART. Hum Reprod 23: 4–10.
- Burrello N, Arcidiacono G, Vicari E, Asero P, Di Benedetto D, De Palma A, Romeo R, D'Agata R, Calogero AE (2004) Morphologically normal spermatozoa of patients with secretory oligo-astheno-teratozoospermia have an increased aneuploidy rate. Hum Reprod 19: 2298–2302.
- Carrell DT, Liu L, Peterson CM, Jones KP, Hatasaka HH, Erickson L, Campbell B (2003) Sperm DNA fragmentation is increased in couples with unexplained recurrent pregnancy loss. Arch Androl 49: 49–55.
- Cassuto NG, Bouret D, Plouchart JM, Jellad S, Vanderzwalmen P, Balet R, Larue L, Barak Y (2009) A new real-time morphology classification for human spermatozoa: a link for fertilization and improved embryo quality. Fertil Steril 92: 1616–1625.
- Castillo J, Simon L, de Mateo S, Lewis S, Oliva R (2011) Protamine/DNA ratios and DNA damage in native and density gradient centrifugated sperm from infertile patients. J Androl 32: 324–332.
- Cayli S, Jakab A, Ovari L, Delpiano E, Celik-Ozenci C, Sakkas D, Ward D, Huszar G (2003) Biochemical markers of sperm function: male fertility and sperm selection for ICSI. Reprod Biomed Online 7: 462–468.
- Celik-Ozenci C, Jakab A, Kovacs T, Catalanotti J, Demir R, Bray-Ward P, Ward D, Huszar G (2004) Sperm selection for ICSI: shape properties do not predict the absence or presence of numerical chromosomal aberrations. Hum Reprod 19: 2052–2059.
- Chan PJ, Jacobson JD, Corselli JU, Patton WC (2006) A simple zeta method for sperm selection based on membrane charge. Fertil Steril 85: 481–486.
- Chohan KR, Griffin JT, Lafromboise M, De Jonge CJ, Carrell DT (2006) Comparison of chromatin assays for DNA fragmentation evaluation in human sperm. J Androl 27: 53–59.
- Collins JA, Barnhart KT, Schlegel PN (2008) Do sperm DNA integrity tests predict pregnancy with in vitro fertilization. Fertil Steril 89: 823–831.
- De Vos A, Van De Velde H, Joris H, Verheyen G, Devroey P, Van Steirteghem A (2003) Influence of individual sperm morphology on fertilization, embryo morphology, and pregnancy outcome of intracytoplasmic sperm injection. Fertil Steril 79: 42–48.
- Donnelly ET, O'Connell M, McClure N, Lewis SE (2000) Differences in nuclear DNA fragmentation and mitochondrial integrity of semen and prepared human spermatozoa. Hum Reprod 15: 1552–1561.
- Dozortsev D, Rybouchkin A, De Sutter P, Dhont M (1995) Sperm plasma membrane damage prior to intracytoplasmic sperm injection: a necessary condition for sperm nucleus decondensation. Hum Reprod 10: 2960–2964.
- Duran EH, Morshedi M, Taylor S, Oehninger S (2002) Sperm DNA quality predicts intrauterine insemination outcome: a prospective cohort study. Hum Reprod 17: 3122–3128.
- Ebner T, Shebl O, Moser M, Mayer RB, Arzt W, Tews G (2011) Easy sperm processing technique allowing exclusive accumulation and later usage of DNA-strand break-free spermatozoa. Reprod Biomed Online 22: 37–43.
- Enciso M, Sarasa J, Agarwal A, Fernández JL, Gosálvez J (2009) A two-tailed Comet assay for assessing DNA damage in spermatozoa. Reprod Biomed Online 18: 609–616.
- Evenson DP, Jost LK, Marshall D, Zinaman MJ, Clegg E, Purvis K, de Angelis P, Claussen OP (1999) Utility of the sperm chromatin structure assay as a diagnostic and prognostic tool in the human fertility clinic. Hum Reprod 14: 1039–1049.
- Evenson DP, Larson KL, Jost LK (2002) Sperm chromatin structure assay: its clinical use for detecting sperm DNA fragmentation in male infertility and comparisons with other techniques. J Androl 23: 25–43.
- Fernandez JL, Muriel L, Rivero MT, Goyanes Y, Vazques R, Alvarez JG (2003) The sperm chromatin dispersion test: a simple method for the determination of sperm DNA fragmentation. J Androl 24: 59–66.
- Fernandez-Gonzalez R, Moreira PN, Perez-Crespo M, Sanchez-Martin M, Ramirez MA, Pericuesta E, Bilbao A, Bermejo-Alvarez P, de Dios HJ, De Fonseca FR, Gutiérrez-Adán A (2008) Long-term effects of mouse intracytoplasmic sperm injection with DNA-fragmented sperm on health and behavior of adult offspring. Biol Reprod 78: 761–772.
- Figueira R de C, Braga DP, Setti AS, Iaconelli A Jr, Borges E Jr (2011) Morphological nuclear integrity of sperm cells is associated with preimplantation genetic aneuploidy screening cycle outcomes. Fertil Steril 95: 990–993.
- Fleming SD, Ilad RS, Griffin AM, Wu Y, Ong KJ, Smith HC, Aitken RJ (2008) Prospective controlled trial of an electrophoretic method of sperm preparation for assisted reproduction: comparison with density gradient centrifugation. Hum Reprod 23: 2646–2651.
- Franco JG Jr, Baruffi RL, Mauri AL, Petersen CG, Oliveira JB, Vagnini L (2008) Significance of large nuclear vacuoles in human spermatozoa: implications for ICSI. Reprod Biomed Online 17: 42–45.
- French DB, Sabanegh ES Jr, Goldfarb J, Desai N (2010) Does severe teratozoospermia affect blastocyst formation, live birth rate, and other clinical outcome parameters in ICSI cycles? Fertil Steril 93: 1097–1103.
- Frydman N, Prisant N, Hesters L, Frydman R, Tachdjian G, Cohen-Bacrie P, Fanchin R (2008) Adequate ovarian follicular status does not prevent the decrease in pregnancy rates associated with high sperm DNA fragmentation. Fertil Steril 89: 92–97.
- Gandini L, Lombardo F, Paoli D, Caruso F, Eleuteri P, Leter G, Ciriminna R, Culasso F, Dondero F, Lenzi A, Spanò M (2004) Full-term pregnancies achieved with ICSI despite high levels of sperm chromatin damage. Hum Reprod 19: 1409–1417.
- Garolla A, Fortini D, Menegazzo M, De Toni L, Nicoletti V, Moretti A, Selice R, Engl B, Foresta C (2008) High-power microscopy for selecting spermatozoa for ICSI by physiological status. Reprod Biomed Online 17: 610–616.
- Gianaroli L, Magli MC, Collodel G, Moretti E, Ferraretti AP, Baccetti B (2008) Sperm head's birefringence: a new criterion for sperm selection. Fertil Steril 90: 104–112.
- Gianaroli L, Magli MC, Ferraretti AP, Crippa A, Lappi M, Capitani S, Baccetti B (2010) Birefringence characteristics in sperm heads allow for the selection of reacted spermatozoa for intracytoplasmic sperm injection. Fertil Steril 93: 807–813.
- Giritharan G, Li MW, De Sebastiano F, Esteban FJ, Horcajadas JA, Lloyd KC, Donjacour A, Maltepe E, Rinaudo PF (2010) Effect of ICSI on gene expression and development of mouse preimplantation embryos. Hum Reprod 25: 3012–3024.
- Giwercman A, Richthoff J, Hjøllund H, Bonde JP, Jepson K, Frohm B, Spano M (2003) Correlation between sperm motility and sperm chromatin structure assay parameters. Fertil Steril 80: 1404–1412.
- Gorczyca W, Traganos F, Jesionowska H, Darzynkiewicz Z (1993) Presence of DNA strand breaks and increased sensitivity of DNA in situ to denaturation in abnormal human sperm cells: analogy to apoptosis of somatic cells. Exp Cell Res 207: 202–205.
- Greco E, Scarselli F, Iacobelli M, Rienzi L, Ubaldi F, Ferrero S, Franco G, Anniballo N, Mendoza C, Tesarik J (2005) Efficient treatment of infertility due to sperm DNA damage by ICSI with testicular spermatozoa. Hum Reprod 20: 226–230.
- Hazout A, Dumont-Hassan M, Junca AM, Cohen BP, Tesarik J (2006) High-magnification ICSI overcomes paternal effect resistant to conventional ICSI. Reprod Biomed Online 12: 19–25.
- Henkel R, Hajimohammad M, Stalf T, Hoogendijk C, Mehnert C, Menkveld R, Gips H, Schill WB, Kruger TF (2004) Influence of deoxyribonucleic acid damage on fertilization and pregnancy. Fertil Steril 81: 965–972.
- Heytens E, Parrington J, Coward K, Young C, Lambrecht S, Yoon SY, Fissore RA, Hamer R, Deane CM, Ruas M, Grasa P, Soleimani R, Cuvelier CA, Gerris J, Dhont M, Deforce D, Leybaert L, De Sutter P (2009) Reduced amounts and abnormal forms of phospholipase C zeta (PLCζ) in spermatozoa from infertile men. Hum Reprod 24: 2417–2428.
- Høst E, Lindenberg S, Kahn JA, Christensen F (1999) DNA strand breaks in human sperm cells: a comparison between men with normal and oligozoospermic sperm samples. Acta Obstet Gynecol Scand 78: 336–339.
- Høst E, Lindenberg S, Smidt-Jensen S (2000a) DNA strand breaks in human spermatozoa: correlation with fertilization in vitro in oligozoospermic men and in men with unexplained infertility. Acta Obstet Gynecol Scand 79: 189–193.
- Høst E, Lindenberg S, Smidt-Jensen S (2000b) The role of DNA strand breaks in human spermatozoa used for IVF and ICSI. Acta Obstet Gynecol Scand 79: 559–563.
- Huang CC, Lin DP, Tsao HM, Cheng TC, Liu CH, Lee MS (2005) Sperm DNA fragmentation negatively correlates with velocity and fertilization rates but might not affect pregnancy rates. Fertil Steril 84: 130–140.
- Hughes CM, Lewis SE, McKelvey-Martin VJ, Thompson W (1996) A comparison of baseline and induced DNA damage in human spermatozoa from fertile and infertile men, using a modified comet assay. Mol Hum Reprod 2: 613–619.
- Hunnicutt GR, Primakoff P, Myles DG (1996) Sperm surface protein PH-20 is bifunctional: one activity is a hyaluronidase and a second, distinct activity is required in secondary sperm-zona binding. Biol Reprod 55: 80–86.
- Huszar G, Vigue L (1993) Incomplete development of human spermatozoa is associated with increased creatine phosphokinase concentration and abnormal head morphology. Mol Reprod Dev 34: 292–298.
- Huszar G, Stone K, Dix D, Vigue L (2000) Putative creatine kinase M-isoform in human sperm is identified as the 70-kilodalton heat shock protein HspA2. Biol Reprod 63: 925–932.
- Huszar G, Ozenci CC, Cayli S, Zavaczki Z, Hansch E, Vigue L (2003) Hyaluronic acid binding by human sperm indicates cellular maturity, viability, and unreacted acrosomal status. Fertil Steril 79(Suppl. 3): 1616–1624.
- Huszar G, Jakab A, Sakkas D, Ozenci CC, Cayli S, Delpiano E, Ozkavukcu S (2007) Fertility testing and ICSI sperm selection by hyaluronic acid binding: clinical and genetic aspects. Reprod Biomed Online 14: 650–663.
- Irvine DS, Twigg JP, Gordon EL, Fulton N, Milne PA, Aitken RJ (2000) DNA integrity in human spermatozoa: relationships with semen quality. J Androl 21: 33–44.
- Jackson RE, Bormann CL, Hassun PA, Rocha AM, Motta EL, Serafini PC, Smith GD (2010) Effects of semen storage and separation techniques on sperm DNA fragmentation. Fertil Steril 94: 2626–2630.
- Jakab A, Sakkas D, Delpiano E, Cayli S, Kovanci E, Ward D, Revelli A, Huszar G (2005) Intracytoplasmic sperm injection: a novel selection method for sperm with normal frequency of chromosomal aneuploidies. Fertil Steril 84: 1665–1673.
- Joly- Helas G, de La Rochebrochard C, Mousset-Siméon N, Moirot H, Tiercin C, Romana SP, Le Caignec C, Clavier B, Macé B, Rives N (2007) Complex chromosomal rearrangement and intracytoplasmic sperm injection: a case report. Hum Reprod 22: 1292–1297.
- Kasai T, Ogawa K, Mizuno K, Nahai S, Uchida Y, Ohta S, Fujie M, Suzuki K, Hirata S, Hoshi K (2002) Relationship between sperm mitochondrial membrane potential, sperm motility, and fertility potential. Asian J Androl 4: 97–103.
- Kennedy C, Ahlering P, Rodriguez H, Levy S, Sutovsky P (2011) Sperm chromatin structure correlates with spontaneous abortion and multiple pregnancy rates in assisted reproduction. Reprod Biomed Online 22: 272–276.
- Kim JW, Chang EM, Song SH, Park SH, Yoon TK, Shim SH (2011) Complex chromosomal rearrangements in infertile males: complexity of rearrangement affects spermatogenesis. Fertil Steril 95: 349–352.
- Kovacs P, Kovats T, Sajgo A, Szollosi J, Matyas S, Kaali SG (2011) The role of hyaluronic acid binding assay in choosing the fertilization method for patients undergoing IVF for unexplained infertility. J Assist Reprod Genet 28: 49–54.
- Kovanci E, Kovacs T, Moretti E, Vigue L, Bray-Ward P, Ward DC, Huszar G (2001) FISH assessment of aneuploidy frequencies in mature and immature human spermatozoa classified by the absence or presence of cytoplasmic retention. Hum Reprod 16: 1209–1217.
- Kruger TF, Menkveld R, Stander FS, Lombard CJ, Van der Merwe JP, van Zyl JA, Smith K (1986) Sperm morphologic features as a prognostic factor in in vitro fertilization. Fertil Steril 46: 1118–1123.
- Kruger TF, Acosta AA, Simmons KF, Swanson RJ, Matta JF, Oehninger S (1988) Predictive value of abnormal sperm morphology in in vitro fertilization. Fertil Steril 49: 112–117.
- Kurokawa M, Fissore RA (2003) ICSI-generated mouse zygotes exhibit altered calcium oscillations, inositol 1,4,5-trisphosphate receptor-1 down-regulation, and embryo development. Mol Hum Reprod 9: 523–533.
- Larson-Cook KL, Brannian JD, Hansen KA, Kasperson KM, Aamold ET, Evenson DP (2003) Relationship between the outcomes of assisted reproductive techniques and sperm DNA fragmentation as measured by the sperm chromatin structure assay. Fertil Steril 80: 895–902.
- Lee TH, Liu CH, Shih YT, Tsao HM, Huang CC, Chen HH, Lee MS (2010) Magnetic-activated cell sorting for sperm preparation reduces spermatozoa with apoptotic markers and improves the acrosome reaction in couples with unexplained infertility. Hum Reprod 25: 839–846.
- Leese HJ, Sturmey RG, Baumann CG, McEvoy TG (2007) Embryo viability and metabolism: obeying the quite rules. Hum Reprod 22: 3047–3055.
- Leunens L, Celestin-Westreich S, Bonduelle M, Liebaers I, Ponjaert-Kristoffersen I (2008) Follow-up of cognitive and motor development of 10-year-old singleton children born after ICSI compared with spontaneously conceived children. Hum Reprod 23: 105–111.
- Li Z, Wang L, Cai J, Huang H (2006) Correlation of sperm DNA damage with IVF and ICSI outcomes: a systematic review and meta-analysis. J Assist Reprod Genet 23: 367–376.
- Lin MH, Kuo-Kuang Lee R, Li SH, Lu CH, Sun FJ, Hwu YM (2008) 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. Fertil Steril 90: 352–359.
- Liu F, Qiu Y, Zou Y, Deng ZH, Yang H, Liu DY (2011) Use of zona pellucida-bound sperm for intracytoplasmic sperm injection produces higher embryo quality and implantation than conventional intracytoplasmic sperm injection. Fertil Steril 95: 815–818.
- Loft S, Kold-Jensen T, Hjollund NH, Giwercman A, Gyllemborg J, Ernst E, Olsen J, Scheike T, Poulsen HE, Bonde JP (2003) Oxidative DNA damage in human sperm influences time to pregnancy. Hum Reprod 18: 1265–1272.
- Lopes S, Sun JG, Jurisicova A, Meriano J, Casper RF (1998) Sperm deoxyribonucleic acid fragmentation is increased in poor-quality semen samples and correlates with failed fertilization in intracytoplasmic sperm injection. Fertil Steril 69: 528–532.
- Mahfouz R, Sharma R, Thiyagarajan A, Kale V, Gupta S, Sabanegh E, Agarwal A (2010) Semen characteristics and sperm DNA fragmentation in infertile men with low and high levels of seminal reactive oxygen species. Fertil Steril 94: 2141–2146.
- Marchesi DE, Feng HL (2007) Sperm DNA integrity from sperm to egg. J Androl 28: 481–489.
- Marchesi DE, Biederman H, Ferrara S, Hershlag A, Feng HL (2010) The effect of semen processing on sperm DNA integrity: comparison of two techniques using the novel Toluidine Blue Assay. Eur J Obstet Gynecol Reprod Biol 151: 176–180.
- Markoulaki S, Kurokawa M, Yoon SY, Matson S, Ducibella T, Fissore R (2007) Comparison of Ca2 + and CaMKII responses in IVF and ICSI in the mouse. Mol Hum Reprod 13: 265–272.
- Mauri AL, Petersen CG, Oliveire JB, Massaro FC, Baruffi LR, Franco JG Jr (2010) Comparison of day 2 embryo quality after conventional ICSI versus intracytoplasmic morphologically selected sperm injection (IMSI) using sibling oocytes. Eur J Obstet Gynecol Reprod Biol 150: 42–46.
- McPherson S, Longo FJ (1993) Chromatin structure-function alterations during mammalian spermatogenesis: DNA nicking and repair in elongating spermatids. Eur J Histochem 37: 109–128.
- Menezo Y, Nicollet B (2004) Replacement of PVP by Hyaluronate (SpermSlowTM) in ICSI - Impact on outcome. Abstract of 18th World Congress on Fertility and Sterility IFFS.
-
Menezo Y, Junca AM, Dumont-Hassan M, De Mouzon J, Cohen-Bacrie P, Ben Khalifa M (2010) ‘Physiologic‘ (hyaluronic acid-carried) icsi results in the same embryo quality and pregnancy rates as with the use of potentially toxic polyvinylpyrrolidone (PVP). Fertil Steril 94(Suppl. 1): 232.
10.1016/j.fertnstert.2010.07.900 Google Scholar
- Meseguer M, Santiso R, Garrido N, García-Herrero S, Remohí J, Fernandez JL (2011) Effect of sperm DNA fragmentation on pregnancy outcome depends on oocyte quality. Fertil Steril 95: 124–128.
- Morozumi K, Yanagimachi R (2005) Incorporation of the acrosome into the oocyte during intracytoplasmic sperm injection could be potentially hazardous to embryo development. Proc Natl Acad Sci USA 102: 14209–14214.
- Morrell JM, Moffatt O, Sakkas D, Manicardi GC, Bizzaro D, Tomlinson M, Nilsson H, Holmes PV (2004) Reduced senescence and retained nuclear DNA integrity in human spermatozoa prepared by density gradient centrifugation. J Assist Reprod Genetics 21: 217–222.
- Morris ID, Ilott S, Dixon L, Brison DR (2002) The spectrum of DNA damage in human sperm assessed by single cell gel electrophoresis (Comet assay) and its relationship to fertilization and embryo development. Hum Reprod 17: 990–998.
- Muratori M, Maggi M, Spinelli S, Filimberti E, Forti G, Baldi E (2003) Spontaneous DNA fragmentation in swim-up selected human spermatozoa during long term incubation. J Androl 24: 253–262.
- Muratori M, Tamburrino L, Tocci V, Costantino A, Marchiani S, Giachini C, Laface I, Krausz C, Meriggiola MC, Forti G, Baldi E (2010) Small variations in crucial steps of TUNEL assay coupled to flow cytometry greatly affect measures of sperm DNA fragmentation. J Androl 31: 336–345.
- Muriel L, Garrido N, Fernández JL, Remohí J, Pellicer A, de los Santos MJ, Meseguer M (2006) Value of the sperm deoxyribonucleic acid fragmentation level, as measured by the sperm chromatin dispersion test, in the outcome of in vitro fertilization and intracytoplasmic sperm injection. Fertil Steril 85: 371–383.
- Nadalini M, Tarozzi N, Distratis V, Scaravelli G, Borini A (2009) Impact of intracytoplasmic morphologically selected sperm injection on assisted reproduction outcome: a review. Reprod Biomed Online 19(Suppl. l3): 45–55.
- Nasr-Esfahani MH, Razavi S, Vahdati AA, Fathi F, Tavalaee M (2008) Evaluation of sperm selection procedure based on hyaluronic acid binding ability on ICSI outcome. J Assist Reprod Genet 25: 197–203.
- Navarro-Costa P, Nogueira P, Carvalho M, Leal F, Cordeiro I, Calhaz-Jorge C, Gonçalves J, Plancha CE (2010) Incorrect DNA methylation of the DAZL promoter CpG island associates with defective human sperm. Hum Reprod 25: 2647–2654.
- Nijs M, Creemers E, Cox A, Franssen K, Janssen M, Vanheusden E, De Jonge C, Ombelet W (2009) Chromomycin A3 staining, sperm chromatin structure assay and hyaluronic acid binding assay as predictors for assisted reproductive outcome. Reprod Biomed Online 19: 671–684.
- Nijs M, Creemers E, Cox A, Janssen M, Vanheusden E, Van der Elst J, Ombelet W (2010) Relationship between hyaluronic acid binding assay and outcome in ART: a pilot study. Andrologia 42: 291–296.
- Oehninger S (2011) Clinical management of male infertility in assisted reproduction: ICSI and beyond. Int J Androl 34: e319–e329.
- Oliveira JB, Massaro FC, Mauri AL, Petersen CG, Nicoletti AP, Baruffi RL, Franco JG Jr (2009) Motile sperm organelle morphology examination is stricter than Tygerberg criteria. Reprod Biomed Online 18: 320–326.
- Ollero M, Gil-Guzman E, Lopez MC, Sharma RK, Agarwal A, Larson K, Evenson D, Thomas AJ Jr, Alvarez JG (2001) Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum Reprod 16: 1912–1921.
- Ozmen B, Caglar GS, Koster F, Schopper B, Diedrich K, Al-Hasani S (2007) Relationship between sperm DNA damage, induced acrosome reaction and viability in ICSI patients. Reprod Biomed Online 15: 208–214.
- Paes Almeida Ferreira de Braga D, Iaconelli A Jr, Cassia Savio de FR, Madaschi C, Semiao-Francisco L, Borges E Jr (2009) Outcome of ICSI using zona pellucida-bound spermatozoa and conventionally selected spermatozoa. Reprod Biomed Online 19: 802–807.
- Palermo G, Joris H, Devroey P, Van Steirteghem AC (1992) Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340: 17–18.
- Parmegiani L, Cognigni GE, Bernardi S, Troilo E, Ciampaglia W, Filicori M (2010a) ‘Physiologic ICSI’: hyaluronic acid (HA) favors selection of spermatozoa without DNA fragmentation and with normal nucleus, resulting in improvement of embryo quality. Fertil Steril 93: 598–604.
- Parmegiani L, Cognigni GE, Ciampaglia W, Pocognoli P, Marchi F, Filicori M (2010b) Efficiency of hyaluronic acid (HA) sperm selection. J Assist Reprod Genet 27: 13–16.
- Parmegiani L, Cognigni GE, Filicori M (2010c) Risks in injecting hyaluronic acid non-bound spermatozoa. Reprod Biomed Online 20: 437–438.
- Payne JF, Raburn DJ, Couchman GM, Price TM, Jamison MG, Walmer DK (2005) Redefining the relationship between sperm deoxyribonucleic acid fragmentation as measured by the sperm chromatin structure assay and outcomes of assisted reproductive techniques. Fertil Steril 84: 356–364.
- Peer S, Eltes F, Berkovitz A, Yehuda R, Itsykson P, Bartoov B (2007) Is fine morphology of the human sperm nuclei affected by in vitro incubation at 37 degrees C? Fertil Steril 88: 1589–1594.
- Perdrix A, Travers A, Chelli MH, Escalier D, Do Rego JL, Milazzo JP, Mousset-Simeon N, Mace B, Rives N (2011) Assessment of acrosome and nuclear abnormalities in human spermatozoa with large vacuoles. Hum Reprod 26: 47–58.
- Polak de Fried E, Denaday F (2010) Single and twin ongoing pregnancies in two cases of previous ART failure after ICSI performed with sperm sorted using annexin V microbeads. Fertil Steril 94: 351.e16.
- Prinosilova P, Kruger T, Sati L, Ozkavukcu S, Vigue L, Kovanci E, Huszar G (2009) Selectivity of hyaluronic acid binding for spermatozoa with normal Tygerberg strict morphology. Reprod Biomed Online 18: 177–183.
- Ramos L, Wetzels AM (2001) Low rates of DNA fragmentation in selected motile human spermatozoa assessed by the TUNEL assay. Hum Reprod 16: 1703–1707.
- Rawe VY, Boudri HU, Alvarez Sedó C, Carro M, Papier S, Nodar F (2010) Healthy baby born after reduction of sperm DNA fragmentation using cell sorting before ICSI. Reprod Biomed Online 20: 320–323.
- Razavi SH, Nasr-Esfahani MH, Deemeh MR, Shayesteh M, Tavalaee M (2010) Evaluation of zeta and HA-binding methods for selection of spermatozoa with normal morphology, protamine content and DNA integrity. Andrologia 42: 13–19.
- Richardson C, Jasin M (2000) Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 405: 697–700.
- Roldan ER (2006) Better intracytoplasmic sperm injection without sperm membranes and acrosome. Proc Natl Acad Sci USA 103: 17585–17586.
- Said T, Agarwal A, Grunewald S, Rasch M, Baumann T, Kriegel C, Li L, Glander HJ, Thomas AJ Jr, Paasch U (2006) Selection of nonapoptotic spermatozoa as a new tool for enhancing assisted reproduction outcomes: an in vitro model. Biol Reprod 74: 530–537.
- Sakkas D, Alvarez JG (2010) Sperm DNA fragmentation: mechanisms of origin, impact on reproductive outcome, and analysis. Fertil Steril 93: 1027–1036.
- Sakkas D, Bianchi PG, Manicardi GC (1997). Chromatin packaging anomalies and DNA damage in human sperm: their possible implications in the treatment of male factor infertility. In: Genetics of Human Male Infertility. C Barratt, C De Jonge, D Mortimer, J Parinaud (eds). Editions EDK, Paris, UK, pp 205–221.
- Sanchez M, Aran B, Blanco J, Vidal F, Veiga A, Barri PN, Huszar G (2005) Preliminary clinical and FISH results on hyaluronic acid sperm selection to improve ICSI. Hum Reprod 20(Suppl. 1): i200.
- Schatten H, Sun QY (2009) The role of centrosomes in mammalian fertilization and its significance for ICSI. Mol Hum Reprod 15: 531–538.
- Seli E, Gardner DK, Schoolcraft WB, Moffatt O, Sakkas D (2004) Extent of nuclear DNA damage in ejaculated spermatozoa impacts on blastocyst development after in vitro fertilization. Fertil Steril 82: 378–383.
- Sharma RK, Said T, Agarwal A (2004) Sperm DNA damage and its clinical relevance in assessing reproductive outcome. Asian J Androl 6: 139–148.
- Siffroi JP, Benzacken B, Straub B, Le Bourhis C, North MO, Curotti G, Bellec V, Alvarez S, Dadoune JP (1997) Assisted reproductive technology and complex chromosomal rearrangements: the limits of ICSI. Mol Hum Reprod 3: 847–851.
- Simon L, Brunborg G, Stevenson M, Lutton D, McManus J, Lewis SE (2010) Clinical significance of sperm DNA damage in assisted reproduction outcome. Hum Reprod 25: 1594–1608.
- Sousa Setti A, Figueira RD, Paes de Almeida Ferreira Braga D, Iaconelli A Jr, Borges E Jr (2011) Intracytoplasmic morphologically selected sperm injection benefits for patients with oligoasthenozoospermia according to the 2010 World Health Organization reference values. Fertil Steril 95: 2711–2714.
- Souza Setti A, Ferreira RC, Paes de Almeida Ferreira Braga D, de Cássia Sávio Figueira R, Iaconelli A Jr, Borges EJ (2010) Intracytoplasmic sperm injection outcome versus intracytoplasmic morphologically selected sperm injection outcome: a meta-analysis. Reprod Biomed Online 21: 450–455.
- Spanò M, Bonde JP, Hjøllund HI, Kolstad HA, Cordelli E, Leter G (2000) Sperm chromatin damage impairs human fertility. The Danish First Pregnancy Planner Study Team. Fertil Steril 73: 43–50.
- Speyer BE, Pizzey AR, Ranieri M, Joshi R, Delhanty JD, Serhal P (2010) Fall in implantation rates following ICSI with sperm with high DNA fragmentation. Hum Reprod 25: 1609–1618.
- Stanger JD (2010) Hypo-osmotic swelling test identifies individual spermatozoa with minimal DNA fragmentation. Reprod Biomed Online 21: 474–484.
- Stevanato J, Bertolla RP, Barradas V, Spaine DM, Cedenho AP, Ortiz V (2008) Semen processing by density gradient centrifugation does not improve sperm apoptotic deoxyribonucleic acid fragmentation rates. Fertil Steril 90: 889–890.
- Sun JG, Jurisicova A, Casper RF (1997) Detection of deoxyribonucleic acid fragmentation in human sperm: correlation with fertilization in vitro . Biol Reprod 56: 602–607.
- Svalander P, Jakobsson AH, Forsberg AS, Bengtsson AC, Wikland M (1996) The outcome of intracytoplasmic sperm injection is unrelated to ‘strict criteria’ sperm morphology. Hum Reprod 11: 1019–1022.
- Tarozzi N, Nadalini M, Bizzaro D, Serrao L, Fava L, Scaravelli G, Borini A (2009) Sperm-hyaluronan-binding assay: clinical value in conventional IVF under Italian law. Reprod Biomed Online 19(Suppl. 3): 35–43.
- Tomlinson MJ, Moffatt O, Manicardi GC, Bizzaro D, Afnan M, Sakkas D (2001) Interrelationships between seminal parameters and sperm nuclear DNA damage before and after density gradient centrifugation: implications for assisted conception. Hum Reprod 16: 2160–2165.
- Tomsu M, Sharma V, Miller D (2002) Embryo quality and IVF treatment outcomes may correlate with different sperm comet assay parameters. Hum Reprod 17: 1856–1862.
-
Upadhya D, Kalthur G, Kumar P, Rao BS, Adiga SK (2010) Association between the extent of DNA damage in the spermatozoa, fertilization and developmental competence in preimplantation stage embryos. J Turkish-German Gynecol Assoc 11: 182–186.
10.5152/jtgga.2010.34 Google Scholar
- Van den Bergh M, Emiliani S, Biramane J, Vannin AS, Englert Y (1998) A first prospective study of the individual straight line velocity of the spermatozoon and its influences on the fertilization rate after intracytoplasmic sperm injection. Hum Reprod 13: 3103–3107.
- Van den Bergh M, Fahy-Deshe M, Hohl MK (2009) Pronuclear zygote score following intracytoplasmic injection of hyaluronan-bound spermatozoa: a prospective randomized study. Reprod Biomed Online 19: 796–801.
- Van Steirteghem AC, Nagy Z, Joris H, Liu J, Staessen C, Smitz J, Wisanto A, Devroey P (1993) High fertilization and implantation rates after intracytoplasmic sperm injection. Hum Reprod 8: 1061–1066.
- Vanderzwalmen P, Hiemer A, Rubner P, Bach M, Neyer A, Stecher A, Uher P, Zintz M, Lejeune B, Vanderzwalmen S, Cassuto C, Zech NH (2008) Blastocyst development after sperm selection at high magnification is associated with size and number of nuclear vacuoles. Reprod Biomed Online 17: 617–627.
- Varghese AC, Bragais FM, Mukhopadhyay D, Kundu S, Pal M, Bhattacharyya AK, Agarwal A (2009) Human sperm DNA integrity in normal and abnormal semen samples and its correlation with sperm characteristics. Andrologia 41: 207–215.
- Velez de la Calle JF, Muller A, Walschaerts M, Clavere JL, Jimenez C, Wittemer C, Thonneau P (2008) Sperm deoxyribonucleic acid fragmentation as assessed by the sperm chromatin dispersion test in assisted reproductive technology programs: results of a large prospective multicenter study. Fertil Steril 90: 1792–1799.
- Virant-Klun I, Tomazevic T, Meden-Vrtovec H (2002) Sperm single-stranded DNA, detected by acridine orange staining, reduces fertilization and quality of ICSI-derived embryos. J Assist Reprod Genet 19: 319–328.
- Virro MR, Larson-Cook KL, Evenson DP (2004) Sperm chromatin structure assay (SCSA) parameters are related to fertilization, blastocyst development, and ongoing pregnancy in in vitro fertilization and intracytoplasmic sperm injection cycles. Fertil Steril 81: 1289–1295.
- Wilding M, Coppola G, di Matteo L, Palagiano A, Fusco E, Dale B (2011) Intracytoplasmic injection of morphologically selected spermatozoa (IMSI) improves outcome after assisted reproduction by deselecting physiologically poor quality spermatozoa. J Assist Reprod Genet 28: 253–262.
- Woldringh GH, Horvers M, Janssen AJ, Reuser JJ, de Groot SA, Steiner K, D'Hauwers KW, Wetzels AM, Kremer JA (2011) Follow-up of children born after ICSI with epididymal spermatozoa. Hum Reprod 7: 1759–1767.
- Worrilow KC, Huynh HT, Bower JB, Anderson AR, Schillings W, Crain JL (2007) PICSI vs. ICSI: statistically significant improvement in clinical outcomes in 240 in vitro fertilization (IVF) patients. Fertil Steril 88(Suppl. 1): s37.
- Worrilow KC, Eid S, Matthews J, Pelts E, Khoury C, Liebermann J (2010) Multi-site clinical trial evaluating PICSI, a method for selection of hyaluronan bound sperm (HBS) for use in ICSI: improved clinical outcomes. Hum Reprod 25(Suppl. 1): i7.
- Yagci A, Murk W, Stronk J, Huszar G (2010) Spermatozoa bound to solid state hyaluronic acid show chromatin structure with high DNA chain integrity: an acridine orange fluorescence study. J Androl 31: 566–572.
- Yanagimachi R (1994) Mammalian fertilization. In: The Physiology of Reproduction. E Knobil, JD Neill (eds). Raven Press Ltd, New York, pp 189–317.
- Ye H, Huang GN, Gao Y, Liu de Y (2006) Relationship between human sperm-hyaluronan binding assay and fertilization rate in conventional in vitro fertilization. Hum Reprod 21: 1545–1550.
- Younglai EV, Holt D, Brown P, Jurisicova A, Casper RF (2001) Sperm swim-up techniques and DNA fragmentation. Hum Reprod 16: 1950–1953.
- Zhang LH, Qiu Y, Wang KH, Wang Q, Tao G, Wang LG (2010) Measurement of sperm DNA fragmentation using bright-field microscopy: comparison between sperm chromatin dispersion test and terminal uridine nick-end labeling assay. Fertil Steril 94: 1027–1032.
- Zini A, Libman J (2006) Sperm DNA damage: importance in the era of assisted reproduction. Curr Opin Urol 16: 428–434.
- Zini A, Sigman M (2009) Are tests of sperm DNA damage clinically useful? Pros and cons. J Androl 20: 219–229.
- Zini A, Finelli A, Phang D, Jarvi K (2000a) Influence of semen processing technique on human sperm DNA integrity. Urology 56: 1081–1084.
- Zini A, Nam RK, Mak V, Phang D, Jarvi K (2000b) Influence of initial semen quality on the integrity of human sperm DNA following semen processing. Fertil Steril 74: 824–827.
- Zini A, Bielecki R, Phang D, Zenzes MT (2001) Correlations between two markers of sperm DNA integrity, DNA denaturation and DNA fragmentation, in fertile and infertile men. Fertil Steril 75: 674–677.
- Zini A, Boman JM, Belzile E, Ciampi A (2008) Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum Reprod 23: 2663–2668.