Zona-free embryo culture: Is it a viable option to improve pregnancy rates?

Reproductive BioMedicine Online

Volumn 21, Issue 1, 2010, Pages 17-25

  Vajta, Gábor ^a   Rienzi, Laura ^b   Bavister, Barry D ^c  

^a JAMES COOK UNIVERSITY   (Australia)

^b GENERA Centre for Reproductive Medicine   (Italy)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

assisted hatching; hatching; microwell; pronase; zona functions; zona hardening

Indexed keywords

GONADOTROPIN; PRONASE;

BLASTOCYST; CELL DAMAGE; CELL STRUCTURE; CELL VIABILITY; CLINICAL TRIAL; CRYOPRESERVATION; DRUG MEGADOSE; EMBRYO CULTURE; EMBRYO DEVELOPMENT; EMBRYO TRANSFER; FEMALE INFERTILITY; FERTILIZATION; FERTILIZATION IN VITRO; HATCHING; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INTRACYTOPLASMIC SPERM INJECTION; MICROFLUIDICS; NONHUMAN; OOCYTE; PREGNANCY; PROGNOSIS; PROSPECTIVE STUDY; REVIEW; TREATMENT FAILURE; ZONA FREE EMBRYO CULTURE; ZONA PELLUCIDA; ZYGOTE;

ANIMALS; BLASTOCYST; EMBRYO CULTURE TECHNIQUES; EMBRYO TRANSFER; EMBRYO, MAMMALIAN; FEMALE; FERTILIZATION IN VITRO; HUMANS; PREGNANCY; PREGNANCY RATE; ZONA PELLUCIDA;

EID: 78650176772     PISSN: 14726483     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.rbmo.2010.03.014     Document Type: Review

References (123)

1. S. Abdelmassih, J. Cardoso, V. Abdelmassih, J.A. Dias, R. Abdelmassih, and Z.P. Nagy Laser-assisted ICSI: a novel approach to obtain higher oocyte survival and embryo quality rates Hum. Reprod. 17 2002 2694 2699 (Pubitemid 35174124)
2. C.R. Austin, and M.W. Bishop Role of the rodent acrosome and perforatorium in fertilization Proc. R. Soc. B Biol. Sci. 149 1958 241 248
3. C.R. Austin, and A.W.H. Braden Early reactions of the rodent egg to spermatozoon penetration J. Exp. Biol. 33 1956 358 366
4. B.D. Bavister Culture of preimplantation embryos: facts and artifacts Hum. Reprod. Update 1 1995 91 148
5. J.M. Bedford Puzzles of mammalian fertilization-and beyond Int. J. Dev. Biol. 52 2008 415 426
6. E. Bertrand, M. Van den Bergh, and J. Englert Does zona pellucida thickness influence the fertilization rate? Hum. Reprod. 10 1995 1189 1193
7. J.D. Bleil, and P.M. Wassarman PM Mammalian sperm-egg interaction: identification of a glycoprotein in mouse egg zonae pellucidae possessing receptor activity for sperm Cell 20 1980 873 882 (Pubitemid 10078567)
8. D.E. Boatman In vitro growth of non-human primate pre- and peri-implantation embryos B.D. Bavister, The Mammalian Preimplantation Embryo. Regulation of Growth and Differentiation 1987 Plenum Press New York 273 308
9. P.J. Booth, S.J. Tan, and R. Reipurth Simplification of bovine somatic cell nuclear transfer by application of a zona-free manipulation technique Cloning Stem Cells 3 2001 139 150 (Pubitemid 34123572)
10. R.A. Bronson, and A. McLaren Transfer to the mouse oviduct of eggs with and without the zona pellucida J. Reprod. Fertil. 22 1970 129 137
11. C.R. Brown, N. Clarke, and J.M. Aiken Changes in the composition of the hamster zona pellucida after fertilization in vivo but not in vitro J. Reprod. Fertil. 90 1990 447 454 (Pubitemid 20386480)
12. G. Calongos, A. Hasegawa, and S. Komori Harmful effects of anti-zona pellucida antibodies in folliculogenesis, oogenesis, and fertilization J. Reprod. Immunol. 79 2009 148 155
13. I. Checiu, and M. Checiu There are no in vivo pulsations of mouse blastocysts Rom. J. Morphol. Embryol. 42 1996 147 154
14. J. Cohen, K.L. Inge, and M. Suzman Videocinematoraphy of fresh and cryopreserved embryos: a retrospective analysis of embryonic morphology and implantation Fertil. Steril. 51 1989 820 827 (Pubitemid 19127855)
15. J. Cohen, C. Elsner, and K. Kort Impairment of the hatching process following in vitro fertilization in the human and improvement of implantation by assisted hatching using micromanipulation Hum. Reprod. 5 1990 7 13 (Pubitemid 20111624)
16. J. Cohen Assisted hatching of human embryos J. In Vitro Fertil. Embryo Transfer 8 1991 179 190
17. G. Coticchio, M.A. Bonu, and R. Sciajno Truths and myths of oocyte sensitivity to controlled rate freezing Reprod. Biomed. Online 15 2007 24 30 (Pubitemid 47162091)
18. H.B. Croxatto Physiology of gamete and embryo transport through the fallopian tube Reprod. Biomed. Online 4 2002 160 169
19. Das, S., Blake, D., Farquhar, C., et al., 2009. Assisted Hatching on Assisted Conception (IVF and ICSI). Cochrane Database Systematic Reviews 15, CD001894.
20. J. Ding, N. Rana, and W.P. Dmowski Intracytoplasmic sperm injection into zona-free human oocytes results in normal fertilization and blastocyst development Hum. Reprod. 14 1999 476 478 (Pubitemid 29097405)
21. I. Donnay, and H.J. Leese Embryo metabolism during the expansion of the bovine blastocyst Mol. Reprod. Dev. 53 1999 171 178 (Pubitemid 29214780)
22. Ebner, T., Balaban, B., Moser, M., et al., 2009 Automatic user-independent zona pellucida imaging at the oocyte stage allows for the prediction of preimplantation development. Fertility and Sterility (advance publ). doi: 10.1016/j.fertnstert.2009.03.106.
23. O. Epifano, L.F. Liang, and M. Familari Coordinate expression of the three zona pellucida genes during mouse oogenesis Development 121 1995 1947 1956
24. G. Familiari, R. Heyn, and M. Relucenti Structural changes of the zona pellucida during fertilization and embryo development Front. Biosci. 13 2008 6730 6751
25. H.L. Feng, A.H. Hershlag, and G.M. Scholl A retrospective study comparing three different assisted hatching techniques Fertil. Steril. 91 2009 1323 1325
26. C.Y. Fong, A. Bongso, and S.C. Ng Ongoing normal pregnancy after transfer of zona-free blastocysts: implications for embryo transfer in the human Hum. Reprod. 12 1997 557 560 (Pubitemid 27156455)
27. C.Y. Fong, A. Bongso, and S.C. Ng Blastocyst pregnancy after enzymatic treatment of the zona pellucida: improving in vitro fertilization and understanding implantation Hum. Reprod. 13 1998 2926 2932 (Pubitemid 28482753)
28. C.Y. Fong, A. Bongso, and H. Sathananthan Ultrastructural observations of enzymatically treated human blastocysts: zona-free blastocyst transfer and rescue of blastocysts with hatching difficulties Hum. Reprod. 16 2001 540 546 (Pubitemid 32218807)
29. P. Freistedt, P. Stojkovic, and E. Wolf Energy status of nonmatured and in vitro-matured domestic cat oocytes and of different stages of in vitro-produced embryos: enzymatic removal of the zona pellucida increases adenosine triphosphate content and total cell number of blastocysts Biol. Reprod. 65 2001 793 798 (Pubitemid 32777365)
30. A. Gabrielsen, S. Lindenberg, and K. Petersen The impact of the zona pellucida thickness variation of human embryos on pregnancy outcome in relation to suboptimal embryo development. A prospective randomized controlled study Hum. Reprod. 16 2001 2166 2170 (Pubitemid 32951912)
31. D.S. Gonzales, and B.D. Bavister Zona pellucida escape by hamster blastocysts in vitro is delayed and morphologically different compared with zona escape in vivo Biol. Reprod. 52 1995 470 480
32. D.S. Gonzales, B.D. Bavister, and S.A. Mese In utero and in vitro proteinase activity during the Mesocricetus auratus zona escape time window Biol. Reprod. 64 2000 222 230 (Pubitemid 32044631)
33. D.A. Gook, and D.H. Edgar Human oocyte cryopreservation Hum. Reprod. Update 13 2007 591 605 (Pubitemid 350018527)
34. Gook, D.A., Edgar, D.H., Borg, J., Martic, M., et al., 2008. Detection of zona pellucida proteins during human folliculogenesis. Hum. Reprod. 23, 394-402.
35. J.M. Greve, and P.M. Wassarman Mouse egg extracellular coat is a matrix of interconnected filaments possessing a structural repeat J. Mol. Biol. 181 1985 253 264
36. T. Hardarson, K. Lundin, and L. Hamberger The position of the metaphase II spindle cannot be predicted by the location of the first polar body in the human oocyte Hum. Reprod. 15 2000 1372 1376 (Pubitemid 30335967)
37. A. Hershlag, and H.L. Feng The effect of pre-freeze assisted hatching onpost-thaw survival of mouse embryos Fertil. Steril. 84 2005 1752 1754 (Pubitemid 41785682)
38. K. Hiraoka, K. Hiraoka, and M. Kinutani Case report: successful pregnancy after vitrification of a human blastocyst that had completely escaped from the zona pellucida on day 6 Hum. Reprod. 19 2004 988 990 (Pubitemid 38456067)
39. K. Hiraoka, K. Hiraoka, and M. Kinutani Vitrification of human hatched blastocysts: a report of 4 cases J. Reprod. Med. 55 2007 413 415 (Pubitemid 46799295)
40. Y.Y. Hsieh, C.C. Chang, and H.D. Tsai Zona-free oocyte fertilized with intracytoplasmic sperm injection and underwent further division: case report and literature review Chang Gung Med. J. 24 2001 599 602
41. R.H. Hunter Sperm-egg interactions in the pig: monospermy, extensive polyspermy, and the formation of chromatin aggregates J. Anat. 122 1976 43 59
42. R.H. Hunter Ovarian control of very low sperm/egg ratios at the commencement of mammalian fertilisation to avoid polyspermy Mol. Reprod. Dev. 44 1996 417 422 (Pubitemid 26262064)
43. K.A. Ivani, and G.E. Seidel At least half of capacitated, motile mouse sperm can fertilize zona-free mouse oocytes J. Exp. Zool. 260 1991 406 412
44. M.J. Izquierdo-Rico, M. Jimenez-Movilla, and E. Llop Hamster zona pellucida is formed by four glycoproteins: ZP1, ZP2, ZP3, and ZP4 J. Proteome Res. 8 2009 926 941
45. L. Jelínková, J. Pavelková, and K. Rezábek Treatment of infertility using oocytes without the zona pellucida Ceská Gynekol. 65 2000 456 459 (in Czech)
46. L. Jelínková, J. Pavelková, and E. Strehler Improved implantation rate after chemical removal of the zona pellucida Fertil. Steril. 79 2003 1299 1303 (Pubitemid 36687875)
47. R.P. Kapur, and L.V. Johnson Selective sequestration of an oviductal fluid glycoprotein in the perivitelline space of mouse oocytes and embryos J. Exp. Zool. 238 1986 249 260 (Pubitemid 16071822)
48. S.S. Kilani, S. Cooke, and A.K. Kan Do age and extended culture affect the architecture of the zona pellucida of human oocytes and embryos? Zygote 14 2006 39 44
49. K. Kinget, M. Nijs, and A.M. Cox A novel approach for patients at risk for ovarian hyperstimulation syndrome: elective transfer of a single zona-free blastocyst on day 5 Reprod. Biomed. Online 4 2002 51 55
50. O. Khorram, S.S. Shapiro, and M.M. Jones Transfer of nonassisted hatched and hatching human blastocysts after in vitro fertilization Fertil. Steril. 74 2000 163 165 (Pubitemid 30427291)
51. C.S. Ko, D.C. Ding, and T.W. Chu Changes to the meiotic spindle and zona pellucida of mature mouse oocytes following different cryopreservation methods Anim. Reprod. Sci. 105 2008 272 282
52. I. Lagutina, G. Lazzari, and R. Duchi Comparative aspects of somatic cell nuclear transfer with conventional and zona-free method in cattle, horse, pig and sheep Theriogenology 67 2007 90 98 (Pubitemid 44854141)
53. M.G. Larman, C.B. Sheehan, and D.K. Gardner Calcium-free vitrification reduces cryoprotectant-induced zona pellucida hardening and increases fertilization rates in mouse oocytes Reproduction 131 2006 53 61 (Pubitemid 43230703)
54. K.C. Lan, F.J. Huang, and Y.C. Lin Zona-free versus laser zona-assisted hatching blastocyst transfer: a comparison of outcomes Fertil. Steril. 91 2008 1959 1962
55. J. Li, G. Vajta, and H. Callesen Comparison of cell numbers of zona-intact and zona-free parthenogenetically activated porcine embryos cultured in vitro Reprod. Fertil. Dev. 22 2009 234
56. C. Liu, E.S. Litscher, and S. Mortillo Targeted disruption of the mZP3 gene results in production of eggs lacking a zona pellucida and infertility in female mice Proc. Natl. Acad. Sci. USA 93 1996 5431 5436 (Pubitemid 26159467)
57. A. Lopata, and D.L. Hay The potential of early human embryos to form blastocysts, hatch from their zona and secrete HCG in culture Hum. Reprod. 4 1989 87 94 (Pubitemid 20072582)
58. J.R. Loret De Mola, and W.T. Garside Analysis of the human zona pellucida during culture: correlation with diagnosis and the preovulatory hormonal environment J. Assist. Reprod. Genet. 14 1997 332 336 (Pubitemid 27287818)
59. C. Manna, L. Rienzi, and E. Greco Zona pellucida solubility and cortical granule complements in human oocytes following assisted reproductive techniques Zygote 9 2001 201 210 (Pubitemid 33691991)
60. R.T. Mansour, C.A. Rhodes, and M.A. Aboulghar Transfer of zona-free embryos improves outcome in poor prognosis patients: a prospective randomized controlled study Hum. Reprod. 15 2000 1061 1064 (Pubitemid 30251300)
61. A. Massip, and J. Mulnard Time-lapse cinematographic analysis of hatching of normal and frozen-thawed cow blastocysts J. Reprod. Fertil. 58 1980 475 478
62. P.L. Matson, J. Graefling, and S.M. Junk Cryopreservation of oocytes and embryos: use of a mouse model to investigate effects upon zona hardness and formulate treatment strategies in an in vitro fertilization programme Hum. Reprod. 12 1997 1550 1553 (Pubitemid 27373214)
63. A. McLaren The fate of the zona pellucida in mice J. Embryol. Exp. Morphol. 23 1970 1 19
64. H.W. Michelmann, D. Rath, and E. Töpfer-Petersen Structural and functional events on the porcine zona pellucida during maturation, fertilization and embryonic development: a scanning electron microscopy analysis Reprod. Domest. Anim. 42 2007 594 602 (Pubitemid 350043857)
65. B. Mintz Experimental study of the developing mammalian egg: removal of zona pellucida Science 138 1962 594 595
66. B. Mintz Control of embryo implantation and survival Adv. Biosci. 6 1971 317 341
67. J.A. Modlinski The role of the zona pellucida in the development of mouse eggs in vivo J. Embryol. Exp. Morphol. 23 1970 539 547
68. M. Montag, and H. van der Ven Oocyte assessment and embryo viability prediction: birefringence imaging Reprod. Biomed. Online 17 2008 454 460
69. M. Montag, B. Koll, and Holmes P. van der Ven Significance of the number of embryonic cells and the state of the zona pellucida for hatching of mouse blastocysts in vitro versus in vivo Biol. Reprod. 62 2000 1738 1744 (Pubitemid 30333758)
70. R.M. Moor, and R.G. Cragle The sheep egg: enzymatic removal of the zona pellucida and culture of eggs in vitro J. Reprod. Fertil. 27 1971 401 409
71. N.W. Moore, C.E. Adams, and L.E.A. Rowson Development potential of single blastomeres of the rabbit egg J. Reprod. Fertil. 17 1968 527 533
72. Y. Murayama, J. Mizuno, and H. Kamakura Mouse zona pellucida dynamically changes its elasticity during oocyte maturation, fertilization and early embryo development Hum. Cell 19 2006 119 125
73. F. Nawroth, P. Müller, and C. Wolf Is the zona pellucida thickness of metaphase-II oocytes in an IVF/ICSI program influenced by the patient's age? Gynecol. Obstet. Invest. 52 2001 55 59 (Pubitemid 32830581)
74. B. Oback, A.T. Wiersema, and P. Gaynor Cloned cattle derived from a novel zona-free embryo reconstruction system Cloning Stem Cells 5 2003 3 12 (Pubitemid 36418421)
75. A. Obruca, D. Sakkas, and Y. Menezo Use of lasers in assisted fertilization and hatching Hum. Reprod. 9 1994 1723 1726 (Pubitemid 24291091)
76. C. O'Neill The potential roles for embryotrophic ligands in preimplantation embryo development Hum. Reprod. Update 14 2008 275 288 (Pubitemid 351575092)
77. M.W. Orsini Morphological evidence on the intrauterine career of the ovum A.C. Enders, Delayed Implantation 1963 University of Chicago Press Chicago, IL, USA 155 166
78. M.W. Orsini, and A. McLaren Loss of the zona pellucida in mice, and the effect of tubal ligation and ovariectomy J. Reprod. Fertil. 13 1967 485 499
79. M. Palmstierna, D. Murkes, and G. Csemiczky Zona pellucida thickness variation and occurrence of visible mononucleated blastomers in preembryos are associated with a high pregnancy rate in IVF treatment J. Assist. Reprod. Genet. 15 1998 70 75 (Pubitemid 28114763)
80. Papi, M., Brunelli, R., Sylla, L., et al., 2010. Mechanical properties of zona pellucida hardening. European Biophysical Journal 27 (Epub ahead of print). 39,6,987-992
81. R.M. Perona, and P.M. Wassarman Mouse blastocysts hatch in vitro by using a trypsin-like pmteinase associated with cells of mud trophectoderm Dev. Biol. 1l4 1986 42 52 (Pubitemid 16078385)
82. T.T. Peura, and G. Vajta A comparison of established and new approaches in ovine and bovine nuclear transfer Cloning Stem Cells 5 2003 257 277 (Pubitemid 38031851)
83. T.T. Peura, I.M. Lewis, and A.O. Trounson The effect of recipient oocyte volume on nuclear transfer in cattle Mol. Reprod. Dev. 50 1999 185 191
84. S.V. Prasad, S.M. Skinner, and C. Carion Structure and function of the mammalian zona pellucida Cells Tissues Organs 166 1999 148 164
85. C.J. Quintans, M.J. Donaldson, and M.V. Bertolino Birth resulting from transfer of blastocysts cryopreserved with propanediol after spontaneous hatching Reprod. Biomed. Online 6 2003 66 68 (Pubitemid 36857122)
86. G.A. Rama Raju, and G.J. Prakash Meiotic spindle and zona pellucida characteristics as predictors of embryonic development: a preliminary study using PolScope imaging Reprod. Biomed. Online 14 2007 166 174 (Pubitemid 46296499)
87. T. Rankin, and J. Dean The molecular genetics of the zona pellucida: mouse mutations and infertility Mol. Hum. Reprod. 11 1996 889 894 (Pubitemid 126715948)
88. T. Rankin, M. Familari, and E. Lee Mice homozygous for an insertional mutation in the Zp3 gene lack a zona pellucida and are infertile Development 122 1996 2903 2910 (Pubitemid 26326521)
89. W.A. Ritchie, J.E. Taylor, and J.O. Gardner Live lambs born from zona-pellucida deduced embryos Cloning Stem Cells 7 2005 178 182 (Pubitemid 43150273)
90. T.L. Roth, W.F. Swanson, and D.E. Wildt Developmental competence of domestic cat embryos fertilized in vivo versus in vitro Biol. Reprod. 51 1994 441 451 (Pubitemid 24297616)
91. M.A. Sampaío, and S. Geber Births after transfer of zona-free blastocysts in oocyte donation cycles J. Assist. Reprod. Genet. 18 2001 156 159 (Pubitemid 32520028)
92. H. Sawada, K. Yamazaki, and M. Hoshi Trypsin-like hatching protease from mouse embryos: evidence for the presence in culture medium and its enzymatic properties J. Exp. Zool. 25 1990 83 87 (Pubitemid 20167586)
93. M.C. Schiewe, J.R. Araujo, and R.H. Asch Enzymatic characterization of zona pellucida hardening in human eggs and embryos J. Assist. Reprod. Genet. 12 1995 2 7
94. M.C. Schiewe, N.L. Hazeleger, and G. Sclimenti Physiological characterization of blastocyst hatching mechanisms by use of a mouse antihatching model Fertil. Steril. 63 1995 288 294
95. P.B. Seshagiri, and S. Sen Roy Cellular and molecular regulation of mammalian blastocyst hatching J. Reprod. Immunol. 83 2009 79 84
96. H. Shiloh, S. Lahav-Baratz, and M. Koifman The impact of cigarette smoking on zona pellucida thickness of oocytes and embryos prior to transfer into the uterine cavity Hum. Reprod. 19 2004 157 159 (Pubitemid 38072025)
97. E.L. Singh The disease control potential of embryos Theriogenology 27 1987 9 20
98. G.D. Smith, and S. Takayama Gamete and embryo isolation and culture with microfluidics Theriogenology 68S 2007 S190 S195
99. P. Soupart, and P.A. Strong Ultrastructural observations on polyspermic penetration of zona-pellucida-free human oocytes inseminated in vitro Fertil. Steril. 26 1975 523 537
100. J.D. Stanger, K. Stevenson, and A. Lakmaker Pregnancy following fertilization of zona-free, coronal cell intact human ova Hum. Reprod. 16 2001 164 167 (Pubitemid 32058599)
101. N.R. Stoddart, and S.D. Fleming Orientation of the first polar body of the oocyte at 6 or 12 o'clock during ICSI does not affect clinical outcome Hum. Reprod. 15 2000 1580 1585
102. R.G. Sturmey, and H.J. Leese Energy metabolism in pig oocytes and early embryos Reproduction 126 2003 197 204 (Pubitemid 36987165)
103. Q.Y. Sun Cellular and molecular mechanisms leading to cortical reaction and polyspermy block in mammalian eggs Microsc. Res. Tech. 61 2003 342 348
104. Y.P. Sun, Y. Xu, and T. Cao Zona pellucida thickness and clinical pregnancy outcome following in vitro fertilization Int. J. Gynaecol. Obstet. 89 2005 258 262 (Pubitemid 40779296)
105. H. Suzuki, M. Togashi, and J. Adachi Developmental ability of zona-free mouse embryos is influenced by cell association at the 4-cell stage Biol. Reprod. 53 1995 78 83
106. K. Takahashi, Y. Araki, and M. Motoyama Normal development of a zona-free oocyte to the blastocyst stage following ICSI Hum. Reprod. 14 1999 2677 2679
107. R.T. Tecirlioglu, A.J. French, and I.M. Lewis Birth of a cloned calf derived from vitrified hand-made cloned (HMC) embryo: a technical report Reprod. Fertil. Dev. 15 2003 361 366 (Pubitemid 38528973)
108. G.A. Thouas, G.M. Jones, and A.O. Trounson The 'GO' system - a novel method of microculture for in vitro development of mouse zygotes to the blastocyst stage Reproduction 126 2003 161 169 (Pubitemid 36987162)
109. A.O. Trounson, and N.W. Moore The survival and development of sheep eggs following complete or partial removal of the zona pellucida J. Reprod. Fertil. 41 1974 97 105
110. G. Vajta Handmade cloning; the future way of nuclear transfer? Trends Biotechnol. 25 2007 250 253 (Pubitemid 46755411)
111. G. Vajta, T. Krösi, and Y. Du The well-of-the-well system: an efficient approach to improve embryo development Reprod. BioMed. Online 17 2008 73 81
112. G. Vajta, I.M. Lewis, and P. Hyttel Somatic cell cloning without micromanipulators Cloning 3 2001 89 95 (Pubitemid 32735032)
113. G. Vajta, I.M. Lewis, and T.R. Tecirlioglu Handmade somatic cell cloning in cattle Methods Mol. Biol. 348 2006 183 195
114. G. Vajta, T.T. Peura, and P. Holm A new method for the culture of zona-included or zon-free embryos: the Well of the Well (WOW) system Mol. Reprod. Dev. 55 2000 256 264 (Pubitemid 30082886)
115. A. Van Soom, A.E. Wrathall, and A. Herrler Is the zona pellucida an efficient barrier to viral infection? Reprod. Fertil. Dev. 22 2010 21 31
116. P.M. Wassarman Zona pellucida glycoproteins Annu. Rev. Biochem. 57 1988 415 442
117. P.M. Wassarman, and D.F. Albertini Cellular and molecular biology of the mammalian ovum E. Knobil, J.D. Neill, The Physiology of Reproduction 1994 Raven Press New York, NY 79 122
118. P.M. Wassarman, and E.S. Litscher Mammalian fertilization: the egg's multifunctional zona pellucida Int. J. Dev. Biol. 52 2008 665 676
119. S. Wołczyński, J. Domitrz, and M. Syrewicz Pregnancy and delivery after the transfer of one blastocyst with enzymatically removed zona pellucida Ginekol. Pol. 70 1999 835 839 (in Polish)
120. B.J. Woodward, S.J. Montgomery, and G.M. Hartshorne Spindle position assessment prior to ICSI does not benefit fertilization or early embryo quality Reprod. Biomed. Online 16 2008 232 238 (Pubitemid 351291970)
121. R.W. Wright Jr., G.B. Anderson, and P.T. Cupps Blastocyst expansion and hatching of bovine ova cultured in vitro J. Anim. Sci. 43 1976 170 174
122. G.M. Wu, L. Lai, and J. Mao Birth of piglets by in vitro fertilization of zona-free porcine oocytes Theriogenology 62 2004 1544 1556 (Pubitemid 39282935)
123. K.P. Xu, N.M. Loskutoff, and K.J. Betteridge Immature zona-free bovine oocytes can be matured, fertilized and cultured to the blastocyst stage in vitro J. Reprod. Fertil. 5 1990 57