Reproductive BioMedicine Online
Volume 20, Issue 2 , Pages 209-222 , February 2010

Slow freezing, vitrification and ultra-rapid freezing of human embryos: a systematic review and meta-analysis

  • Faten F. AbdelHafez

      Affiliations

    • Department of Obstetrics and Gynecology, Cleveland Clinic Foundation, Cleveland, OH, USA
    • ,
  • Nina Desai

      Affiliations

    • Department of Obstetrics and Gynecology, Cleveland Clinic Foundation, Cleveland, OH, USA
    • Corresponding Author InformationCorresponding author.
    • ,
  • Ahmed M. Abou-Setta

      Affiliations

    • Private Clinic, Pyramids, Giza, Egypt
    • Present address: Alberta Research Centre for Health Evidence, University of Alberta, Edmonton, Canada.
    • ,
  • Tommaso Falcone

      Affiliations

    • Department of Obstetrics and Gynecology, Cleveland Clinic Foundation, Cleveland, OH, USA
    • ,
  • James Goldfarb

      Affiliations

    • Department of Obstetrics and Gynecology, Cleveland Clinic Foundation, Cleveland, OH, USA

Received 5 March 2009 ,Revised 16 April 2009 ,Accepted 21 September 2009.

References 

  1. Al-Hasani S, Ozmen B, Koutlaki N, et al. Three years of routine vitrification of human vzygotes: is it still fair to advocate slow-rate freezing?. Reprod. Biomed. Online. 2007;14:288–293
  2. Barg PE, Barad DH, Feichtinger W. Ultrarapid freezing (URF) of mouse and human preembryos: a modified approach. J. In vitro Fertil. Embryo Transfer IVF. 1990;7:355–357
  3. Bernal DPCC, Colturato LF, Leef DM, Kort HI, Nagy ZP. Evaluation of blastocyst recuperation, implantation and pregnancy rates after vitrification/warming or slow freezing/thawing cycles. Fertil. Steril. 2008;90(Suppl. 1):277–278
  4. Bucher HC, Guyatt GH, Griffith LE, Walter SD. The results of direct and indirect treatment comparisons in meta-analysis of randomized controlled trials. J. Clin. Epidemiol. 1997;50:683–691
  5. Chi HJ, Koo JJ, Kim MY, et al. Cryopreservation of human embryos using ethylene glycol in controlled slow freezing. Hum. Reprod. 2002;17:2146–2151
  6. Clifford AL, Jilbert PM, Gentry WL, et al. Better ongoing pregnancy rates from frozen embryo transfers when vitrified blastocysts are used. Fertil. Steril. 2007;88(Suppl. 1):S349–S350
  7. Desai N, Blackmon H, Szeptycki J, Goldfarb J. Cryoloop vitrification of human day 3 cleavage-stage embryos: post-vitrification development, pregnancy outcomes and live births. Reprod. Biomed. Online. 2007;14:208–213
  8. DerSimonian R, Laird N. Meta-analysis in clinical trials. Control. Clin. Trials. 1986;7:177–188
  9. Edgar DH, Archer J, McBain J, Bourne H. Embryonic factors affecting outcome from single cryopreserved embryo transfer. Reprod. Biomed. Online. 2007;14:718–723
  10. Feichtinger W, Hochfellner C, Ferstl U. Clinical experience with ultra-rapid freezing of embryos. Hum. Reprod. 1991;6:735–736
  11. Gardner DK, Pool TB, Lane M. Embryo nutrition and energy metabolism and its relationship to embryo growth, differentiation, and viability. Semin. Reprod. Med. 2000;18:205–218
  12. Gordts S, Roziers P, Campo R, Noto V. Survival and pregnancy outcome after ultrarapid freezing of human embryos. Fertil. Steril. 1990;53:469–472
  13. Higgins, J., Green, S., 2008. In: Collaboration TC (Ed.), Cochrane Handbook for Systematic Reviews of Interventions, Version 5.0.1 (updated September 2008).
  14. Higgins JP, Thompson SG, Deeks JJ, Altman DG. Measuring inconsistency in meta-analyses. Br. Med. J. 2003;327:557–560
  15. Hiraoka K, Hiraoka K, Kinutani M, Kinutani K. Blastocoele collapse by micropipetting prior to vitrification gives excellent survival and pregnancy outcomes for human day 5 and 6 expanded blastocysts. Hum. Reprod. 2004;19:2884–2888
  16. Kaufman RA, Menezo Y, Hazout A, et al. Cocultured blastocyst cryopreservation: experience of more than 500 transfer cycles. Fertil. Steril. 1995;64:1125–1129
  17. Kim S, Lee S, Lee J, et al. Study on the vitrification of human blastocysts. II: Effect of vitrification on the implantation and the pregnancy of human blastocysts. Korean J. Fertil. Steril. 2000;27:67–74
  18. Kuwayama M, Vajta G, Ieda S, Kato O. Comparison of open and closed methods for vitrification of human embryos and the elimination of potential contamination. Reprod. Biomed. Online. 2005;11:608–614
  19. Lai AC, Lin BP, Chang CC, et al. Pregnancies after transfer of ultrarapidly frozen human embryos. J. Assist. Reprod. Genet. 1996;13:625–628
  20. Lee SY, Son WY, Yoon SH, Lim JH. Clinical-pregnancy outcome after vitrification of blastocysts produced from in vitro maturation cycles. Fertil. Steril. 2007;88:1449–1451
  21. Li Y, Chen ZJ, Yang HJ, et al. Comparison of vitrification and slow-freezing of human day 3 cleavage stage embryos: post-vitrification development and pregnancy outcomes. Zhonghua Fu Chan Ke Za Zhi. 2007;42:753–755
  22. Liebermann J, Dietl J, Vanderzwalmen P, Tucker MJ. Recent developments in human oocyte, embryo and blastocyst vitrification: where are we now?. Reprod. Biomed. Online. 2003;7:623–633
  23. Liebermann J, Nawroth F, Isachenko V, et al. Potential importance of vitrification in reproductive medicine. Biol. Reprod. 2002;67:1671–1680
  24. Liebermann J, Tucker MJ. Comparison of vitrification and conventional cryopreservation of day 5 and day 6 blastocysts during clinical application. Fertil. Steril. 2006;86:20–26
  25. Loutradi KE, Kolibianakis EM, Venetis CA, et al. Cryopreservation of human embryos by vitrification or slow freezing: a systematic review and meta-analysis. Fertil. Steril. 2008;90:186–193
  26. Marek D, Langley M, Doody KM, Doody KJ. Frozen embryo transfer (FET) of day 5 blastocyst embryos compared with transfer of day 6 or day 7 blastocyst embryos. Fertil. Steril. 2001;76(Suppl. 1):S121
  27. Mauri AL, Petersen CG, Baruffi RL, et al. Comparison of the cryopreservation of human embryos obtained after intracytoplasmic sperm injection with a slow cooling or an ultrarapid cooling procedure. J. Assist. Reprod. Genet. 2001;18:257–261
  28. McAlister FA, Laupacis A, Wells GA, Sackett DL. Users’ Guides to the Medical Literature: XIX. Applying clinical trial results B. Guidelines for determining whether a drug is exerting (more than) a class effect. J. Am. Med. Assoc. 1999;282:1371–1377
  29. Medved R, Virant-Klun I, Meden-Vrtovec H, Tomazevic T. Outcome of frozen–thawed blastocysts derived from gonadotrophin releasing hormone agonist or antagonist cycles. J. Assist. Reprod. Genet. 2006;23:275–279
  30. Menezo Y. Cryopreservation of IVF embryos: which stage?. Eur. J. Obstet. Gynecol. Reprod. Biol. 2004;113(Suppl. 1):S28–S32
  31. Mukaida T, Oka C, Goto T, Takahashi K. Artificial shrinkage of blastocoeles using either a micro-needle or a laser pulse prior to the cooling steps of vitrification improves survival rate and pregnancy outcome of vitrified human blastocysts. Hum. Reprod. 2006;21:3246–3252
  32. Nagy ZP, Taylor T, Elliott T, et al. Removal of lysed blastomeres from frozen–thawed embryos improves implantation and pregnancy rates in frozen embryo transfer cycles. Fertil. Steril. 2005;84:1606–1612
  33. Pegg DE. The role of vitrification techniques of cryopreservation in reproductive medicine. Hum. Fertil. (Camb.). 2005;8:231–239
  34. Rama Raju GA, Haranath GB, Krishna KM, et al. Vitrification of human 8-cell embryos, a modified protocol for better pregnancy rates. Reprod. Biomed. Online. 2005;11:434–437
  35. Review Manager (RevMan) [Computer program], 2006. Version 4.3 for Windows. The Nordic Cochrane Centre, Copenhagen, The Cochrane Collaboration.
  36. Rienzi L, Ubaldi F, Iacobelli M, et al. Developmental potential of fully intact and partially damaged cryopreserved embryos after laser-assisted removal of necrotic blastomeres and post-thaw culture selection. Fertil. Steril. 2005;84:888–894
  37. Saito H, Ishida GM, Kaneko T, et al. Application of vitrification to human embryo freezing. Gynecol. Obstet. Invest. 2000;49:145–149
  38. Salumets A, Suikkari AM, Makinen S, et al. Frozen embryo transfers: implications of clinical and embryological factors on the pregnancy outcome. Hum. Reprod. 2006;21:2368–2374
  39. Salumets A, Tuuri T, Makinen S, et al. Effect of developmental stage of embryo at freezing on pregnancy outcome of frozen–thawed embryo transfer. Hum. Reprod. 2003;18:1890–1895
  40. Schroder AK, Banz C, Katalinic A, et al. Counselling on cryopreservation of pronucleated oocytes. Reprod. Biomed. Online. 2003;6:69–74
  41. Seelig AS, Al-Hasani S, Katalinic A, et al. Comparison of cryopreservation outcome with gonadotrophin-releasing hormone agonists or antagonists in the collecting cycle. Fertil. Steril. 2002;77:472–475
  42. Senn A, Vozzi C, Chanson A, et al. Prospective randomized study of two cryopreservation policies avoiding embryo selection: the pronucleate stage leads to a higher cumulative delivery rate than the early cleavage stage. Fertil. Steril. 2000;74:946–952
  43. Shamonki MI, Oktay K. Oocyte and ovarian tissue cryopreservation: indications, techniques, and applications. Semin. Reprod. Med. 2005;23:266–276
  44. Shapiro BS, Daneshmand ST, Garner FC, et al. Contrasting patterns in in vitro fertilization pregnancy rates among fresh autologous, fresh oocyte donor, and cryopreserved cycles with the use of day 5 or day 6 blastocysts may reflect differences in embryo-endometrium synchrony. Fertil. Steril. 2008;89:20–26
  45. Shaw JM, Jones GM. Terminology associated with vitrification and other cryopreservation procedures for oocytes and embryos. Hum. Reprod. Update. 2003;9:583–605
  46. Song F, Altman DG, Glenny AM, Deeks JJ. Validity of indirect comparison for estimating efficacy of competing interventions: empirical evidence from published meta-analyses. Br. Med. J. 2003;326:472
  47. Tao J, Tamis R, Fink K. Pregnancies achieved after transferring frozen morula/compact stage embryos. Fertil. Steril. 2001;75:629–631
  48. Trounson A, Sathananthan AH. Ultrarapid freezing. In:  Mashiach S, et al. editor. Advances Assisted Reproductive Technologies. New York: Plenum Press; 1990;p. 589–599
  49. Trounson A, Peura A, Freemann L, Kirby C. Ultrarapid freezing of early cleavage stage human embryos and eight-cell mouse embryos. Fertil. Steril. 1988;49:822–826
  50. Trounson A, Peura A, Kirby C. Ultrarapid freezing: a new low-cost and effective method of embryo cryopreservation. Fertil. Steril. 1987;48:843–850
  51. Trounson A, Sjoblom P. Cleavage and development of human embryos in vitro after ultrarapid freezing and thawing. Fertil. Steril. 1988;50:373–376
  52. Tummon IS, Wentworth MA, Thornhill AR. Frozen–thawed embryo transfer and live birth: long-term follow-up after one oocyte retrieval. Fertil. Steril. 2006;86:239–242
  53. Vajta G, Kuwayama M. Improving cryopreservation systems. Theriogenology. 2006;65:236–244
  54. Vajta G, Nagy ZP. Are programmable freezers still needed in the embryo laboratory? Review on vitrification. Reprod. Biomed. Online. 2006;12:779–796
  55. Van den Abbeel E, Camus M, Van Waesberghe L, et al. A randomized comparison of the cryopreservation of one-cell human embryos with a slow controlled-rate cooling procedure or a rapid cooling procedure by direct plunging into liquid nitrogen. Hum. Reprod. 1997;12:1554–1560
  56. Van den Abbeel E, Camus M, Verheyen G, et al. Slow controlled-rate freezing of sequentially cultured human blastocysts: an evaluation of two freezing strategies. Hum. Reprod. 2005;20:2939–2945
  57. Van den Abbeel E, Van der Elst J, van der Linden M, van Steirteghem AC. High survival rate of one-cell mouse embryos cooled rapidly to −196 degrees C after exposure to a propylene glycol–dimethylsulfoxide–sucrose solution. Cryobiology. 1997;34:1–12
  58. Van der Elst J, Van den Abbeel E, Vitrier S, et al. Selective transfer of cryopreserved human embryos with further cleavage after thawing increases delivery and implantation rates. Hum. Reprod. 1997;12:1513–1521
  59. Vanderzwalmen P, Bertin G, Debauche C, et al. Births after vitrification at morula and blastocyst stages: effect of artificial reduction of the blastocoelic cavity before vitrification. Hum. Reprod. 2002;17:744–751
  60. Veeck LL. Does the developmental stage at freeze impact on clinical results post-thaw?. Reprod. Biomed. Online. 2003;6:367–374
  61. Veeck LL, Bodine R, Clarke RN, et al. High pregnancy rates can be achieved after freezing and thawing human blastocysts. Fertil. Steril. 2004;82:1418–1427
  62. Virant-Klun I, Tomazevic T, Bacer-Kermavner L, et al. Successful freezing and thawing of blastocysts cultured in sequential media using a modified method. Fertil. Steril. 2003;79:1428–1433
  63. Vyjayanthi S, Tang T, Fattah A, et al. Elective cryopreservation of embryos at the pronucleate stage in women at risk of ovarian hyperstimulation syndrome may affect the overall pregnancy rate. Fertil. Steril. 2006;86:1773–1775
  64. Wang JX, Yap YY, Matthews CD. Frozen–thawed embryo transfer: Influence of clinical factors on implantation rate and risk of multiple conception. Hum. Reprod. 2001;16:2316–2319
  65. Warnes GM, Payne D, Jeffrey R, et al. Reduced pregnancy rates following the transfer of human embryos frozen or thawed in culture media supplemented with normal serum albumin. Hum. Reprod. 1997;12:1525–1530
  66. Zhu GJ, Jin L, Zhang HW, et al. Vitrification of human cleaved embryos in vitro fertilization-embryo transfer. Zhonghua Fu Chan Ke Za Zhi. 2005;40:682–684
  67. Ziebe S, Bech B, Petersen K, et al. Resumption of mitosis during post-thaw culture: a key parameter in selecting the right embryos for transfer. Hum. Reprod. 1998;13:178–181

 Dr Nina Desai received her doctorate in cell biology from the University of Medicine and Dentistry of New Jersey (1984). She served as IVF Laboratory Director at Ohio State and later at University Hospital, Case Western Reserve, Cleveland, Ohio. Dr Desai was invited to join the Cleveland Clinic Foundation in 2000 as Director of IVF and Clinical Research. She is also an Assistant Professor at the Lerner College of Medicine, Case Western Reserve. Her research interests include non-invasive markers of embryonic potential, growth factor modulation of embryonic differentiation, apoptosis, stem cell derivation and vitrification of embryo, oocytes and isolated follicles.

PII: S1472-6483(09)00226-0

doi: 10.1016/j.rbmo.2009.11.013

Reproductive BioMedicine Online
Volume 20, Issue 2 , Pages 209-222 , February 2010

Article Tools

* Image Usage & Resolution