Improving ICSI: A review from the spermatozoon perspective

Systems Biology in Reproductive Medicine

Volumn 62, Issue 6, 2016, Pages 359-371

  Simopoulou, Mara ^a,b   Gkoles, Laertis ^b   Bakas, Panagiotis ^b   Giannelou, Polina ^b   Kalampokas, Theodoros ^b   Pantos, Konstantinos ^c   Koutsilieris, Michael ^a  

^a UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^b UNIVERSITY OF ATHENS   (Greece)

^c Genesis Athens Hospital   (Greece)

Author keywords

ART; fertilization; ICSI; infertility; spermatozoon

Indexed keywords

HYALURONIC ACID; LIPOCORTIN 5; CHROMATIN; CULTURE MEDIUM;

DENSITY GRADIENT CENTRIFUGATION; DNA FRAGMENTATION; HUMAN; IN VITRO FERTILIZATION; INTRACYTOPLASMIC SPERM INJECTION; MALE; MICROSCOPY; OOCYTE; PRIORITY JOURNAL; REVIEW; SPERM; SPERMATOZOON; ZONA PELLUCIDA; CHROMATIN; CULTURE MEDIUM; FEMALE; FERTILITY; METABOLISM; PHYSIOLOGY; STANDARDS;

ANNEXIN A5; CHROMATIN; CULTURE MEDIA; FEMALE; HUMANS; HYALURONIC ACID; MALE; SPERM INJECTIONS, INTRACYTOPLASMIC; SPERM-OVUM INTERACTIONS; SPERMATOZOA;

EID: 84988412569     PISSN: 19396368     EISSN: 19396376     Source Type: Journal    
DOI: 10.1080/19396368.2016.1229365     Document Type: Review

References (122)

1. Aitken, R.J., Mattei, A., and Irvine, S., (1986) Paradoxical stimulation of human sperm motility by 2-deoxyadenosine. J Reprod Fertil 78:515-27.
2. Aktan, T.M., Montag, M., Duman, S., Gorkemli, H., Rink, K., and Yurdakul, T., (2004) Use of a laser to detect viable but immotile spermatozoa. Andrologia 36:366-9.
3. Alvarez, J.G., Lasso, J.L., Blasco, L., Nunez, R.C., Heyner, S., Caballero, P.P., et al. (1993) Centrifugation of human spermatozoa induces sublethal damage; separation of human spermatozoa from seminal plasma by a dextran swim-up procedure without centrifugation extends their motile lifetime. Hum Reprod 8:1087-92.
4. Antinori, M., Licata, E., Dani, G., Cerusico, F., Versaci, C., d’Angelo, D., et al. (2008) Intracytoplasmic morphologically selected sperm injection:a prospective randomized trial. Reprod Biomed Online 16:835-41.
5. Arends, M.J., and Wyllie, A.H., (1991) Apoptosis:mechanisms and roles in pathology. Int Rev Exp Pathol 32:223-54.
6. Avendano, C., Franchi, A., Jones, E., and Oehninger, S., (2009) Pregnancy-specific β-1-glycoprotein 1 and human leukocyte antigen-E mRNA in human sperm:differential expression in fertile and infertile men and evidence of a possible functional role during early development. Hum Reprod 24:270-7.
7. Avendano, C., and Oehninger, S., (2011) DNA fragmentation in morphologically normal spermatozoa:how much should we be concerned in the ICSI era? J Androl 32:356-63.
8. Baccetti, B., (2004) Microscopical advances in assisted reproduction. J Submicrosc Cytol Pathol 36:333-9.
9. Balaban, B., Lundin, K., Morrell, J.M., Tjellstrom, H., Urman, B., and Holmes, P.V., (2003) An alternative to PVP for slowing sperm prior to ICSI. Hum Reprod 18:1887-9.
10. Bartoov, B., Berkovitz, A., and Eltes, F., (2001) Selection of spermatozoa with normal nuclei to improve the pregnancy rate with intracytoplasmic sperm injection. N Engl J Med 345:1067-8.
11. Bassiri, F., Tavalaee, M., and Nasr Esfahani, M.H., (2013) Correlation between Different Patterns of Hypo-Osmotic Swelling and Sperm Functional Tests. Int J Fertil Steril 7:193-8.
12. Bassiri, F., Tavalaee, M., Shiravi, A.H., Mansouri, S., and Nasr-Esfahani, M.H., (2012) Is there an association between HOST grades and sperm quality? Hum Reprod 27:2277-84.
13. Berkovitz, A., Eltes, F., Lederman, H., Peer, S., Ellenbogen, A., Feldberg, B., et al. (2006) How to improve IVF-ICSI outcome by sperm selection. Reprod Biomed Online 12:634-8.
14. Black, M., Liu de, Y., Bourne, H., and Baker, H.W., (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 93:672-4.
15. Boitrelle, F., Guthauser, B., Alter, L., Bailly, M., Bergere, M., Wainer, R., et al. (2014) High-magnification selection of spermatozoa prior to oocyte injection:confirmed and potential indications. Reprod Biomed Online 28:6-13.
16. Borges, E., Jr., Setti, A.S., Vingris, L., Figueira Rde, C., Braga, D.P., and Iaconelli, A., Jr. (2013) Intracytoplasmic morphologically selected sperm injection outcomes:the role of sperm preparation techniques. J Assist Reprod Genet 30:849-54.
17. Carlomagno, G., Nordio, M., Chiu, T.T., and Unfer, V., (2011) Contribution of myo-inositol and melatonin to human reproduction. Eur J Obstet Gynecol Reprod Biol 159:267-72.
18. Casciani, V., Minasi, M.G., Fabozzi, G., Scarselli, F., Colasante, A., Lobascio, A.M., et al. (2014) Traditional intracytoplasmic sperm injection provides equivalent outcomes compared with human zona pellucida-bound selected sperm injection. Zygote 22:565-70.
19. Casper, R.F., Meriano, J.S., Jarvi, K.A., Cowan, L., and Lucato, M.L., (1996) The hypo-osmotic swelling test for selection of viable sperm for intracytoplasmic sperm injection in men with complete asthenozoospermia. Fertil Steril 65:972-6.
20. Chan, P.J., Jacobson, J.D., Corselli, J.U., and Patton, W.C., (2006) A simple zeta method for sperm selection based on membrane charge. Fertil Steril 85:481-6.
21. Charehjooy, N., Najafi, M.H., Tavalaee, M., Deemeh, M.R., Azadi, L., Shiravi, A.H., et al. (2014) Selection of Sperm Based on Hypo-Osmotic Swelling May Improve ICSI Outcome:A Preliminary Prospective Clinical Trial. Int J Fertil Steril 8:21-8.
22. Check, J.H., Katsoff, B., Yuan, W., Summers-Chase, D., Hourani, W., and Horwath, D., (2012) Intracytoplasmic sperm injection completely negates the implantation problem associated with conventional fertilization with sperm with low hypo-osmotic swelling test scores as evidenced by evaluating donor-recipient pairs. Clin Exp Obstet Gynecol 39:21-2.
23. Chemes, E.H., and Rawe, Y.V., (2003) Sperm pathology:a step beyond descriptive morphology. Origin, characterization and fertility potential of abnormal sperm phenotypes in infertile men. Hum Reprod Update 9:405-28.
24. Chiu, T.T., Rogers, M.S., Law, E.L., Briton-Jones, C.M., Cheung, L.P., and Haines, C.J., (2002) Follicular fluid and serum concentrations of myo-inositol in patients undergoing IVF:relationship with oocyte quality. Hum Reprod 17:1591-6.
25. Condorelli, R.A., La Vignera, S., Bellanca, S., Vicari, E., and Calogero, A.E., (2012) Myoinositol:does it improve sperm mitochondrial function and sperm motility? Urology 79:1290-5.
26. De Vos, A., Van de Velde, H., Bocken, G., Eylenbosch, G., Franceus, N., Meersdom, G., et al. (2013) Does intracytoplasmic morphologically selected sperm injection improve embryo development? A randomized sibling-oocyte study. Hum Reprod 28:617-26.
27. Dutch Society of Obstetrics and Gynaecology (NVOG). (2010) Guideline:Male Subfertility. Ubrecht, The Netherlands.
28. Ebner, T., Moser, M., and Tews, G., (2005) Possible applications of a non-contact 1.48 microm wavelength diode laser in assisted reproduction technologies. Hum Reprod Update 11:425-35.
29. Ebner, T., Shebl, O., Oppelt, P., and Mayer, R.B., (2014) Some reflections on intracytoplasmic morphologically selected sperm injection. Int J Fertil Steril 8:105-12.
30. Ebner, T., Tews, G., Mayer, R.B., Ziehr, S., Arzt, W., Costamoling, W., et al. (2011) Pharmacological stimulation of sperm motility in frozen and thawed testicular sperm using the dimethylxanthine theophylline. Fertil Steril 96:1331-6.
31. Eisenberg, F., Jr. and Parthasarathy, R., (1987) Measurement of biosynthesis of myo-inositol from glucose 6-phosphate. Methods Enzymol 141:127-43.
32. Essig, M., Schoenfeld, C., Amelar, R.D., Dubin, L., and Weiss, G., (1982) Stimulation of human sperm motility by relaxin. Fertil Steril 38:339-43.
33. Evenson, D.P., (2016) The Sperm Chromatin Structure Assay (SCSA(®)) and other sperm DNA fragmentation tests for evaluation of sperm nuclear DNA integrity as related to fertility. Anim Reprod Sci 169:56-75.
34. Ezeh, U.I., Moore, H.D., and Cooke, I.D., (1998) A prospective study of multiple needle biopsies versus a single open biopsy for testicular sperm extraction in men with non-obstructive azoospermia. Hum Reprod 13:3075-80.
35. Feichtinger, W., Obruca, A., and Brunner, M., (1995) Sex chromosomal abnormalities and intracytoplasmic sperm injection. Lancet 346:1566.
36. Foskett, J.K., (2010) Inositol trisphosphate receptor Ca2+ release channels in neurological diseases. Pflugers Arch 460:481-94.
37. Fraser, J.R., Laurent, T.C., and Laurent, U.B., (1997) Hyaluronan:its nature, distribution, functions and turnover. J Intern Med 242:27-33.
38. Gerber, P.A., Kruse, R., Hirchenhain, J., Krussel, J.S., and Neumann, N.J., (2008) Pregnancy after laser-assisted selection of viable spermatozoa before intracytoplasmatic sperm injection in a couple with male primary cilia dyskinesia. Fertil Steril 89:1826 e9–12.
39. Ghumman, S., Adiga, S.K., Upadhya, D., Kalthur, G., Jayaraman, V., Rao, S.B., et al. (2011) Combination of swim-up and density gradient separation methods effectively eliminate DNA damaged sperm. J Turk Ger Gynecol Assoc 12:148-52.
40. Gianaroli, L., Magli, M.C., Collodel, G., Moretti, E., Ferraretti, A.P., and Baccetti, B., (2008) Sperm head’s birefringence:a new criterion for sperm selection. Fertil Steril 90:104-12.
41. Gianaroli, L., Magli, M.C., Ferraretti, A.P., Crippa, A., Lappi, M., Capitani, S., et al. (2010) Birefringence characteristics in sperm heads allow for the selection of reacted spermatozoa for intracytoplasmic sperm injection. Fertil Steril 93:807-13.
42. Goksan Pabuccu, E., Sinem Caglar, G., Dogus Demirkiran, O., and Pabuccu, R., (2015) Uncommon but devastating event:total fertilisation failure following intracytoplasmic sperm injection. Andrologia (2016) 48:164-70. Epub 2015 May 1.
43. Grunewald, S., and Paasch, U., (2013) Sperm selection for ICSI using annexin V. Methods Mol Biol 927:257-62.
44. Hammitt, D.G., Bedia, E., Rogers, P.R., Syrop, C.H., Donovan, J.F., and Williamson, R.A., (1989) Comparison of motility stimulants for cryopreserved human semen. Fertil Steril 52:495-502.
45. Hammitt, D.G., Ferrigni, R.G., Sattler, C.A., Rebert, J.A., and Singh, A.P., (2002) Development of a new and efficient laboratory method for processing testicular sperm. J Assist Reprod Genet 19:335-42.
46. Hoogendijk, C.F., Kruger, T.F., Bouic, P.J., and Henkel, R.R., (2009) A novel approach for the selection of human sperm using annexin V-binding and flow cytometry. Fertil Steril 91:1285-92.
47. Huang, H.Y., Huang, Y.H., Kao, W.L., and Yao, D.J., (2015a) Embryo formation from low sperm concentration by using dielectrophoretic force. Biomicrofluidics 9:022404.
48. Huang, J., Ju, Y., Wang, X., Zhang, Q., and Sodmergen (2015b) A one-step rectification of sperm cell targeting ensures the success of double fertilization. J Integr Plant Biol 57:496-503.
49. Huang, M.T., Kuo-Kuang Lee, R., Lu, C.H., Chen, Y.J., Li, S.H., and Hwu, Y.M., (2015c) The efficiency of conventional microscopic selection is comparable to the hyaluronic acid binding method in selecting spermatozoa for male infertility patients. Taiwan J Obstet Gynecol 54:48-53.
50. Huang, Y.M., Zheng, S.J., Yan, J., Yang, H.Q., Wu, D., Wang, Q., et al. (2016) Investigation on the interaction of letrozole with herring sperm DNA through spectroscopic and modeling methods. Luminescence 31:1077-84.
51. Huszar, G., Jakab, A., Sakkas, D., Ozenci, C.C., Cayli, S., Delpiano, E., et al. (2007) Fertility testing and ICSI sperm selection by hyaluronic acid binding:clinical and genetic aspects. Reprod Biomed Online 14:650-63.
52. Ioannou, D., Miller, D., Griffin, D.K., and Tempest, H.G., (2016) Impact of sperm DNA chromatin in the clinic. J Assist Reprod Genet 33:157-66.
53. Jakab, A., Sakkas, D., Delpiano, E., Cayli, S., Kovanci, E., Ward, D., et al. (2005) Intracytoplasmic sperm injection:a novel selection method for sperm with normal frequency of chromosomal aneuploidies. Fertil Steril 84:1665-73.
54. Jayaraman, V., Upadhya, D., Narayan, P.K., and Adiga, S.K., (2012) Sperm processing by swim-up and density gradient is effective in elimination of sperm with DNA damage. J Assist Reprod Genet 29:557-63.
55. Jeyendran, R. S., Van der Ven, H. H., Perez-Pelaez, M., Crabo, B. G., and Zaneveld, L. J., (1984). Development of an assay to assess the functional integrity of the human sperm membrane and its relationship to other semen characteristics. J Reprod Fertil 70:219-228.
56. Kang, H.J., Lee, S.H., Park, Y.S., Lim, C.K., Ko, D.S., Yang, K.M., et al. (2015) Artificial oocyte activation in intracytoplasmic sperm injection cycles using testicular sperm in human in vitro fertilization. Clin Exp Reprod Med 42:45-50.
57. Kato, Y., and Nagao, Y., (2009) Effect of PVP on sperm capacitation status and embryonic development in cattle. Theriogenology 72:624-35.
58. Kato, Y., and Nagao, Y., (2012) Effect of polyvinylpyrrolidone on sperm function and early embryonic development following intracytoplasmic sperm injection in human assisted reproduction. Reprod Med Biol 11:165-76.
59. Kheirollahi-Kouhestani, M., Razavi, S., Tavalaee, M., Deemeh, M.R., Mardani, M., Moshtaghian, J., et al. (2009) Selection of sperm based on combined density gradient and Zeta method may improve ICSI outcome. Hum Reprod 24:2409-16.
60. Kim, E.K., Kim, E.H., Kim, E.A., Lee, K.A., Shin, J.E., and Kwon, H., (2015) Comparison of the effect of different media on the clinical outcomes of the density-gradient centrifugation/swim-up and swim-up methods. Clin Exp Reprod Med 42:22-9.
61. Klement, A.H., Koren-Morag, N., Itsykson, P., and Berkovitz, A., (2013) Intracytoplasmic morphologically selected sperm injection versus intracytoplasmic sperm injection:a step toward a clinical algorithm. Fertil Steril 99:1290-3.
62. Knez, K., Zorn, B., Tomazevic, T., Vrtacnik-Bokal, E., and Virant-Klun, I., (2011) The IMSI procedure improves poor embryo development in the same infertile couples with poor semen quality:a comparative prospective randomized study. Reprod Biol Endocrinol 9:123.
63. Kovacic, B., Vlaisavljevic, V., and Reljic, M., (2006) Clinical use of pentoxifylline for activation of immotile testicular sperm before ICSI in patients with azoospermia. J Androl 27:45-52.
64. Leach, M., Aitken, R.J., and Sacks, G., (2015) Sperm DNA fragmentation abnormalities in men from couples with a history of recurrent miscarriage. Aust N Z J Obstet Gynaecol 55:379-83.
65. Lee, T. H., Liu, C. H., Shih, Y. T., Tsao, H. M., Huang, C. C., Chen, H. H., and Lee, M. S., (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.
66. Liu, D.Y., (2011) Could using the zona pellucida bound sperm for intracytoplasmic sperm injection (ICSI) enhance the outcome of ICSI? Asian J Androl 13:197-8.
67. Lukaszuk, K., Wcislo, M., Liss, J., Stachowicz, A., Jakiel, G., Lukaszuk, M., et al. (2015) First Pregnancy, Somatic and Psychological Status of a 4-Year-Old Child Born following Annexin V TESA Sperm Separation. AJP Rep 5:e105–8.
68. Luppi, S., Martinelli, M., Giacomini, E., Giolo, E., Zito, G., Garcia, R.C., et al. (2015) Comparative proteomic analysis of spermatozoa isolated by swim-up or density gradient centrifugation. Reprod Biol Endocrinol 13:36.
69. Marchetti, C., Obert, G., Deffosez, A., Formstecher, P., and Marchetti, P., (2002) Study of mitochondrial membrane potential, reactive oxygen species, DNA fragmentation and cell viability by flow cytometry in human sperm. Hum Reprod 17:1257-65.
70. Mizuno, K., Hoshi, K., and Huang, T., (2002) Fertilization and embryo development in a mouse ICSI model using human and mouse sperm after immobilization in polyvinylpyrrolidone. Hum Reprod 17:2350-5.
71. Montag, M., Rink, K., Delacretaz, G., and van der Ven, H., (2000) Laser-induced immobilization and plasma membrane permeabilization in human spermatozoa. Hum Reprod 15:846-52.
72. Morales, P., Llanos, M., Yovich, J.L., Cummins, J.M., and Vigil, P., (1993) Pentoxifylline increases sperm penetration into zona-free hamster oocytes without increasing the acrosome reaction. Andrologia 25:359-62.
73. Nadalini, M., Tarozzi, N., Di Santo, M., and Borini, A., (2014) Annexin V magnetic-activated cell sorting versus swim-up for the selection of human sperm in ART:is the new approach better then the traditional one? J Assist Reprod Genet 31:1045-51.
74. Nasr-Esfahani, M.H., Aboutorabi, R., Esfandiari, E., and Mardani, M., (2002) Sperm MTT viability assay:a new method for evaluation of human sperm viability. J Assist Reprod Genet 19:477-82.
75. Neri, Q.V., Lee, B., Rosenwaks, Z., Machaca, K., and Palermo, G.D., (2014) Understanding fertilization through intracytoplasmic sperm injection (ICSI). Cell Calcium 55:24-37.
76. Nomikos, M., Yu, Y., Elgmati, K., Theodoridou, M., Campbell, K., Vassilakopoulou, V., et al. (2013) Phospholipase Czeta rescues failed oocyte activation in a prototype of male factor infertility. Fertil Steril 99:76-85.
77. Nyboe Andersen, A., Carlsen, E., and Loft, A., (2008) Trends in the use of intracytoplasmatic sperm injection marked variability between countries. Hum Reprod Update 14:593-604.
78. Paes Almeida Ferreira de Braga, D., Iaconelli, A., Jr., Cassia Savio de Figueira, R., Madaschi, C., Semiao-Francisco, L. and Borges, E., Jr. (2009) Outcome of ICSI using zona pellucida-bound spermatozoa and conventionally selected spermatozoa. Reprod Biomed Online 19:802-7.
79. Palermo, G., Joris, H., Devroey, P., and Van Steirteghem, A.C., (1992) Pregnancies after intracytoplasmic injection of single spermatozoon into an oocyte. Lancet 340:17-8.
80. Palermo, G.D., Neri, Q.V., and Rosenwaks, Z., (2015) To ICSI or Not to ICSI. Semin Reprod Med 33:92-102.
81. Palermo, G.D., Neri, Q.V., Takeuchi, T., and Rosenwaks, Z., (2009) ICSI:where we have been and where we are going. Semin Reprod Med 27:191-201.
82. Parmegiani, L., Cognigni, G.E., Bernardi, S., Troilo, E., Taraborrelli, S., Arnone, A., et al. (2012) Comparison of two ready-to-use systems designed for sperm-hyaluronic acid binding selection before intracytoplasmic sperm injection:PICSI vs. Sperm Slow:a prospective, randomized trial. Fertil Steril 98:632-7.
83. Parmegiani, L., Cognigni, G.E., Ciampaglia, W., Pocognoli, P., Marchi, F., and Filicori, M., (2010) Efficiency of hyaluronic acid (HA) sperm selection. J Assist Reprod Genet 27:13-6.
84. Peer, S., Eltes, F., Berkovitz, A., Yehuda, R., Itsykson, P., and Bartoov, B., (2007) Is fine morphology of the human sperm nuclei affected by in vitro incubation at 37 degrees C? Fertil Steril 88:1589-94.
85. Petersen, C.G., Vagnini, L.D., Mauri, A.L., Massaro, F.C., Cavagna, M., Baruffi, R.L., et al. (2011) Relationship between DNA damage and sperm head birefringence. Reprod Biomed Online 22:583-9.
86. Platts, A.E., Dix, D.J., Chemes, H.E., Thompson, K.E., Goodrich, R., Rockett, J.C., et al. (2007) Success and failure in human spermatogenesis as revealed by teratozoospermic RNAs. Hum Mol Genet 16:763-73.
87. Pousette, A., Akerlof, E., Rosenborg, L., and Fredricsson, B., (1986) Increase in progressive motility and improved morphology of human spermatozoa following their migration through Percoll gradients. Int J Androl 9:1-13.
88. Pregl Breznik, B., Kovacic, B., and Vlaisavljevic, V., (2013) Are sperm DNA fragmentation, hyperactivation, and hyaluronan-binding ability predictive for fertilization and embryo development in in vitro fertilization and intracytoplasmic sperm injection? Fertil Steril 99:1233-41.
89. Rawe, V.Y., Diaz, E.S., Abdelmassih, R., Wojcik, C., Morales, P., Sutovsky, P., et al. (2008) The role of sperm proteasomes during sperm aster formation and early zygote development:implications for fertilization failure in humans. Hum Reprod 23:573-80.
90. Rawe, V.Y., Terada, Y., Nakamura, S., Chillik, C.F., Olmedo, S.B., and Chemes, H.E., (2002) A pathology of the sperm centriole responsible for defective sperm aster formation, syngamy and cleavage. Hum Reprod 17:2344-9.
91. Ricci, G., Perticarari, S., Boscolo, R., Montico, M., Guaschino, S., and Presani, G., (2009) Semen preparation methods and sperm apoptosis:swim-up versus gradient-density centrifugation technique. Fertil Steril 91:632-8.
92. Romany, L., Garrido, N., Motato, Y., Aparicio, B., Remohi, J., and Meseguer, M., (2014) Removal of annexin V-positive sperm cells for intracytoplasmic sperm injection in ovum donation cycles does not improve reproductive outcome:a controlled and randomized trial in unselected males. Fertil Steril 102:1567-75 e1.
93. Rossato, M., Di Virgilio, F., and Foresta, C., (1996) Involvement of osmo-sensitive calcium influx in human sperm activation. Mol Hum Reprod 2:903-9.
94. Rubino, P., Palini, S., Chigioni, S., Carlomagno, G., Quagliariello, A., De Stefani, S., et al. (2015) Improving fertilization rate in ICSI cycles by adding myoinositol to the semen preparation procedures:a prospective, bicentric, randomized trial on sibling oocytes. J Assist Reprod Genet 32:387-94.
95. Said, T.M., Agarwal, A., Zborowski, M., Grunewald, S., Glander, H.J., and Paasch, U., (2008) Utility of magnetic cell separation as a molecular sperm preparation technique. J Androl 29:134-42.
96. Sakkas, D., Manicardi, G.C., Tomlinson, M., Mandrioli, M., Bizzaro, D., Bianchi, P.G., et al. (2000) The use of two density gradient centrifugation techniques and the swim-up method to separate spermatozoa with chromatin and nuclear DNA anomalies. Hum Reprod 15:1112-6.
97. Sallam, H.N., Farrag, A., Agameya, A.F., El-Garem, Y., and Ezzeldin, F., (2005) The use of the modified hypo-osmotic swelling test for the selection of immotile testicular spermatozoa in patients treated with ICSI:a randomized controlled study. Hum Reprod 20:3435-40.
98. Schatten, H., and Sun, Q.Y., (2009) The functional significance of centrosomes in mammalian meiosis, fertilization, development, nuclear transfer, and stem cell differentiation. Environ Mol Mutagen 50:620-36.
99. Semprini, A.E., Levi-Setti, P., Bozzo, M., Ravizza, M., Taglioretti, A., Sulpizio, P., et al. (1992) Insemination of HIV-negative women with processed semen of HIV-positive partners. Lancet 340:1317-9.
100. Setti, A.S., Figueira, R.C., Braga, D.P., Aoki, T., Iaconelli, A., Jr. and Borges, E., Jr. (2013a) Intracytoplasmic morphologically selected sperm injection is beneficial in cases of advanced maternal age:a prospective randomized study. Eur J Obstet Gynecol Reprod Biol 171:286-90.
101. Setti, A.S., Paes de Almeida Ferreira Braga, D., Iaconelli, A., Jr., Aoki, T., and Borges, E., Jr. (2013b) Twelve years of MSOME and IMSI:a review. Reprod Biomed Online 27:338-52.
102. Sharma, R.K., and Agarwal, A., (1997) Influence of artificial stimulation on unprocessed and Percoll-washed cryopreserved sperm. Arch Androl 38:173-9.
103. Stanger, J.D., Vo, L., Yovich, J.L., and Almahbobi, G., (2010) Hypo-osmotic swelling test identifies individual spermatozoa with minimal DNA fragmentation. Reprod Biomed Online 21:474-84.
104. Stanic, P., Sonicki, Z., and Suchanek, E., (2002) Effect of pentoxifylline on motility and membrane integrity of cryopreserved human spermatozoa. Int J Androl 25:186-90.
105. Stegen, C., van Rumste, M.M., Mol, B.W., and Koks, C.A., (2012) The value of chromosomal analysis in oligozoospermic men. Fertil Steril 98:1438-42.
106. Strehler, E., Baccetti, B., Sterzik, K., Capitani, S., Collodel, G., De Santo, M., et al. (1998) Detrimental effects of polyvinylpyrrolidone on the ultrastructure of spermatozoa (Notulae seminologicae 13). Hum Reprod 13:120-3.
107. Tachawiwat, K., Getpook, C., and Geater, A., (2015) Comparison of hyaluronan binding assay scores of spermatozoa using swim-up techniques and density gradient centrifugation. J Med Assoc Thai 98 Suppl 2:S84–91.
108. Tandara, M., Balić, A., Tandara, L., Bilić-Zulle, L., Sunj, M., Kozina, V., Goluža, T., and Jukić, M., (2014) Sperm DNA integrity testing:big halo is a good predictor of embryo quality and pregnancy after conventional IVF. Andrology 2:678-686.
109. Tarlatzis, B.C., Kolibianakis, E.M., Bontis, J., Tousiou, M., Lagos, S., and Mantalenakis, S., (1995) Effect of pentoxifylline on human sperm motility and fertilizing capacity. Arch Androl 34:33-42.
110. Tournaye, H., Van der Linden, M., Van den Abbeel, E., Devroey, P., and Van Steirteghem, A., (1993) Effects of pentoxifylline on in-vitro development of preimplantation mouse embryos. Hum Reprod 8:1475-80.
111. Van Steirteghem, A., Liu, J., Nagy, Z., Joris, H., Tournaye, H., Liebaers, I., et al. (1993) Use of assisted fertilization. Hum Reprod 8:1784-5.
112. Vanderzwalmen, P., Hiemer, A., Rubner, P., Bach, M., Neyer, A., Stecher, A., et al. (2008) Blastocyst development after sperm selection at high magnification is associated with size and number of nuclear vacuoles. Reprod Biomed Online 17:617-27.
113. Vermey, B.G., Chapman, M.G., Cooke, S., and Kilani, S., (2015) The relationship between sperm head retardance using polarized light microscopy and clinical outcomes. Reprod Biomed Online 30:67-73.
114. Vicari, E., de Palma, A., Burrello, N., Longo, G., Grazioso, C., Barone, N., et al. (2003) Absolute polymorphic teratozoospermia in patients with oligo-asthenozoospermia is associated with an elevated sperm aneuploidy rate. J Androl 24:598-603.
115. Wober, M., Ebner, T., Steiner, S.L., Strohmer, H., Oppelt, P., Plas, E., et al. (2015) A new method to process testicular sperm:combining enzymatic digestion, accumulation of spermatozoa, and stimulation of motility. Arch Gynecol Obstet 291:689-94.
116. World Health Organization (WHO). (2010) Laboratory Manual for the Examination and Processing of Human Semen. WHO Press, Geneva.
117. Xue, X., Wang, W.S., Shi, J.Z., Zhang, S.L., Zhao, W.Q., Shi, W.H., et al. (2014) Efficacy of swim-up versus density gradient centrifugation in improving sperm deformity rate and DNA fragmentation index in semen samples from teratozoospermic patients. J Assist Reprod Genet 31:1161-6.
118. Yuzpe, A.A., Liu, Z., and Fluker, M.R., (2000) Rescue intracytoplasmic sperm injection (ICSI)-salvaging in vitro fertilization (IVF) cycles after total or near-total fertilization failure. Fertil Steril 73:1115-9.
119. Zhang, Z., Zhu, L., Jiang, H., Chen, H., Chen, Y., and Dai, Y., (2015) Sperm DNA fragmentation index and pregnancy outcome after IVF or ICSI:A meta-analysis. J Assist Reprod Genet. 32:17-26.
120. Zhang, H., Dornadula, G., Beumont, M., Livornese, L., Jr., Van Uitert, B., Henning, K., et al. (1998) Human immunodeficiency virus type 1 in the semen of men receiving highly active antiretroviral therapy. N Engl J Med 339:1803-9.
121. Zini, A., Finelli, A., Phang, D., and Jarvi, K., (2000) Influence of semen processing technique on human sperm DNA integrity. Urology 56:1081-4.
122. Zini, A., Phillips, S., Courchesne, A., Boman, J. M., Baazeem, A., Bissonnette, F., Kadoch, I. J., and San Gabriel, M., (2009) Sperm head morphology is related to high deoxyribonucleic acid stainability assessed by sperm chromatin structure assay. Fertil. Steril. 91:2495-2500.