Skip to main content
Log in

The international transportation of frozen embryos does not affect IVF outcomes

  • Gynecologic Endocrinology and Reproductive Medicine
  • Published:
Archives of Gynecology and Obstetrics Aims and scope Submit manuscript

Abstract

Purpose

The regulated transportation of cryopreserved human embryos resulting from assisted reproduction treatments offers opportunities for patients undergoing embryo transfer in other regions/countries. However, the principal concern for fertility clinics is maintaining unaltered embryo quality to ensure satisfactory clinical outcomes. The aim of the study was to evaluate the efficacy of the transportation process comparing the survival rate and competence of transported embryos to embryos produced and transferred on-site, in frozen embryo transfer cycles.

Methods

This retrospective study assessed the outcomes of 621 blastocysts thawed at IVI Roma (Italy) between March 2021 and March 2022. Autologous or donated oocytes fertilized in vitro, cultured to the blastocyst stage, and cryopreserved in IVI Roma clinic (Group A, n = 450), were compared to embryos generated in IVI Spain clinics and transported to IVI Roma (Group B, n = 171).

Results

Groups A and B respectively showed no significant difference in embryo survival rates after thawing (N = 440/450, 97.8% vs. N = 168/171, 98.2%, p = 0.71), pregnancy rates (N = 221/440, 50.23% vs. N = 77/168, 45.83%, p = 0.33), clinical pregnancy rates (N = 200/440, 45.45% vs. N = 62/168, 36.90%, p = 0.06), and miscarriage rates (N = 42/221, 19,00% vs. 21/77, 28.57%, p = 0.13), even after stratification for the source of the oocyte. Logistic binomial regression considering donor oocytes, preimplantation genetic testing, and patients’ age, did not show any significant results on embryo survival and IVF outcomes.

Conclusion

The regulated transport of cryopreserved blastocysts did not affect embryo survival rate or IVF outcomes. Our data support the safety of embryo cryopreservation and medical transportation services, allowing clinics and patients to transport embryos with no significant risk to embryo competence.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author, M.C., upon reasonable request.

References

  1. Cohen J, Grudzinskas G, Johnson M (2012) Welcome to the ’100% Club’! Reprod Biomed Online. https://doi.org/10.1016/j.rbmo.2012.03.001

    Article  PubMed  Google Scholar 

  2. Coates A et al (2017) Optimal euploid embryo transfer strategy, fresh versus frozen, after preimplantation genetic screening with next generation sequencing: a randomized controlled trial. Fertil Steril. https://doi.org/10.1016/j.fertnstert.2016.12.022

    Article  PubMed  Google Scholar 

  3. Chen Z-J et al (2016) Fresh versus frozen embryos for infertility in the polycystic ovary syndrome. N Engl J Med. https://doi.org/10.1056/nejmoa1513873

    Article  PubMed  PubMed Central  Google Scholar 

  4. Wang A et al (2017) Freeze-only versus fresh embryo transfer in a multicenter matched cohort study: contribution of progesterone and maternal age to success rates. Fertil Steril. https://doi.org/10.1016/j.fertnstert.2017.05.007

    Article  PubMed  PubMed Central  Google Scholar 

  5. Mohamed AMF, Chouliaras S, Jones CJP, Nardo LG (2011) Live birth rate in fresh and frozen embryo transfer cycles in women with endometriosis. Eur J Obstet Gynecol Reprod Biol. https://doi.org/10.1016/j.ejogrb.2011.01.020

    Article  PubMed  Google Scholar 

  6. Cobo A, De Los Santos MJ, Castellò D, Gámiz P, Campos P, Remohí J (2012) Outcomes of vitrified early cleavage-stage and blastocyst-stage embryos in a cryopreservation program: evaluation of 3150 warming cycles. Fertil Steril. https://doi.org/10.1016/j.fertnstert.2012.07.1107

    Article  PubMed  Google Scholar 

  7. Nahman MR (2016) Reproductive tourism: through the anthropological ‘reproscope.’ Annu Rev Anthropol. https://doi.org/10.1146/annurev-anthro-102313-030459

    Article  Google Scholar 

  8. Rinehart LA (2021) Storage, transport, and disposition of gametes and embryos: legal issues and practical considerations. Fertil Steril. https://doi.org/10.1016/j.fertnstert.2020.11.025

    Article  PubMed  Google Scholar 

  9. Fineschi V, Neri M, Turillazzi E (2005) The new Italian law on assisted reproduction technology (Law 40–2004). J Med Ethics. https://doi.org/10.1136/jme.2004.010231

    Article  PubMed  PubMed Central  Google Scholar 

  10. European Parliament (2004) DIRECTIVE 2004/23/EC. Official Journal of European Union

    Google Scholar 

  11. Balaban B et al (2011) The Istanbul consensus workshop on embryo assessment: proceedings of an expert meeting. Hum Reprod. https://doi.org/10.1093/humrep/der037

    Article  Google Scholar 

  12. Gatimel N, Moreau J, Bettiol C, Parinaud J, Léandri RD (2021) Semi-automated versus manual embryo vitrification: inter-operator variability, time-saving, and clinical outcomes. J Assist Reprod Genet. https://doi.org/10.1007/s10815-021-02346-3

    Article  PubMed  PubMed Central  Google Scholar 

  13. Nagy ZP, Shapiro D, Chang CC (2020) Vitrification of the human embryo: a more efficient and safer in vitro fertilization treatment. Fertil Steril. https://doi.org/10.1016/j.fertnstert.2019.12.009

    Article  PubMed  Google Scholar 

  14. Vajta G, Rienzi L, Ubaldi FM (2015) Open versus closed systems for vitrification of human oocytes and embryos. Reprod Biomed Online. https://doi.org/10.1016/j.rbmo.2014.12.012

    Article  PubMed  Google Scholar 

  15. Fernández-Shaw S, Cercas R, Braña C, Villas C, Pons I (2015) Ongoing and cumulative pregnancy rate after cleavage-stage versus blastocyst-stage embryo transfer using vitrification for cryopreservation: Impact of age on the results. J Assist Reprod Genet. https://doi.org/10.1007/s10815-014-0387-9

    Article  PubMed  Google Scholar 

  16. Paoli D et al (2021) Cryopreserved gamete and embryo transport: proposed protocol and form templates-SIERR (Italian Society of Embryology, Reproduction, and Research). Biopreserv Biobank. https://doi.org/10.1089/bio.2020.0080

    Article  PubMed  Google Scholar 

  17. Alikani M, Parmegiani L (2018) Human reproductive cell cryopreservation, storage, handling, and transport: risks and risk management. Semin Reprod Med. https://doi.org/10.1055/s-0038-1676849

    Article  PubMed  Google Scholar 

  18. Alikani M (2018) Cryostorage of human gametes and embryos: a reckoning. Reprod Biomed Online. https://doi.org/10.1016/j.rbmo.2018.05.004

    Article  PubMed  Google Scholar 

  19. La Marca A et al (2019) A novel transnational fresh oocyte donation (TOD) program based on transport of frozen sperm and embryos. Hum Reprod. https://doi.org/10.1093/humrep/dey331

    Article  PubMed  Google Scholar 

  20. Takanashi Y (2004) Clinical evaluation of frozen/thawed embryo transfer following transport of oocytes and embryos. Reprod Med Biol. https://doi.org/10.1111/j.1447-0578.2004.00045.x

    Article  PubMed  PubMed Central  Google Scholar 

  21. Gardner D, Schoolcraft W (1999) In-vitro culture of human blastocysts.

  22. Bosch E, De Vos M, Humaidan P (2020) The future of cryopreservation in assisted reproductive technologies. Front Endocrinol. https://doi.org/10.3389/fendo.2020.00067

    Article  Google Scholar 

  23. Ku PY, Lee RKK, Lin SY, Lin MH, Hwu YM (2012) Comparison of the clinical outcomes between fresh blastocyst and vitrified-thawed blastocyst transfer. J Assist Reprod Genet. https://doi.org/10.1007/s10815-012-9874-z

    Article  PubMed  PubMed Central  Google Scholar 

  24. Kuleshova LL, Lopata A (2002) Vitrification can be more favorable than slow cooling. Fertil Steril. https://doi.org/10.1016/S0015-0282(02)03305-8

    Article  PubMed  Google Scholar 

  25. Daar J et al (2016) Cross-border reproductive care: an ethics committee opinion. Fertil Steril. https://doi.org/10.1016/j.fertnstert.2016.08.038

    Article  Google Scholar 

  26. Gordy D, Tashjian RS, Lee H, Movassaghi M, Yong WH (2019) Domestic and international shipping of biospecimens. Methods in molecular biology. Springer

    Google Scholar 

  27. Requena A, Cruz M, Pellicer A (2019) Is the transport of frozen embryos a good option to improve results in a transnational oocyte donation program? Hum Reprod. https://doi.org/10.1093/humrep/dez093

    Article  PubMed  Google Scholar 

  28. La Marca A, De Canto MB, Mignini Renzini M, Rodriguez A, Vassena R (2019) Reply: Is the transport of frozen embryos a good option to improve results in a transnational oocyte donation program? Hum Reprod. https://doi.org/10.1093/humrep/dez084

    Article  PubMed  Google Scholar 

  29. Tabks C (2020) Cryostorage of reproductive tissues in the in vitro fertilization laboratory: a committee opinion. Fertil Steril. https://doi.org/10.1016/j.fertnstert.2020.06.019

    Article  Google Scholar 

  30. Movimentazione Materiale Crioconservato (2022). https://www.sierr.it/risorse/utility/movimentazione-materiale-crioconservato. Accessed 14 Aug 2022

  31. Canosa S et al (2022) Are commercial warming kits interchangeable for vitrified human blastocysts? Further evidence for the adoption of a Universal Warming protocol. J Assist Reprod Genet. https://doi.org/10.1007/s10815-021-02364-1

    Article  PubMed  PubMed Central  Google Scholar 

  32. Parmegiani L et al (2020) ‘Universal Warming’ protocol for vitrified oocytes to streamline cell exchange for transnational donation programs: a multi-center study. J Assist Reprod Genet 37(6):1379–1385. https://doi.org/10.1007/s10815-020-01798-3

    Article  PubMed  PubMed Central  Google Scholar 

  33. Patrizio P, Albertini DF, Gleicher N, Caplan A (2022) The changing world of IVF: the pros and cons of new business models offering assisted reproductive technologies. J Assist Reprod Genet. https://doi.org/10.1007/s10815-022-02399-y

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all the biologists involved in sample transport services at IVIRMA clinics in Italy and Spain, and all the participants for making this work possible. We would like to thank Judith Mifsud (MD) for reviewing the manuscript.

Funding

The authors declare that no funds, grants, or other support were received during the preparation of this manuscript.

Author information

Authors and Affiliations

Authors

Contributions

LP: Data analysis, manuscript writing. FDeA: Data collection. ST: Manuscript writing, statistical analysis. MT: Data management. DG: project development. AP: Critically review the final draft. MC: Project development, manuscript editing.

Corresponding author

Correspondence to Mauro Cozzolino.

Ethics declarations

Conflict of interest

The authors have no relevant financial or non-financial interests to disclose.

Ethical approval

This research study was conducted retrospectively from data obtained for clinical purposes and was approved by the Ethical Committee “Lazio 2” (protocol number 0116965/2022).

Consent to participate and publish

All participants included in the study gave written consent to sensible data utilization prior to data extraction from their electronic medical records.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pellegrini, L., De Angelis, F., Tartaglia, S. et al. The international transportation of frozen embryos does not affect IVF outcomes. Arch Gynecol Obstet 308, 989–995 (2023). https://doi.org/10.1007/s00404-023-07092-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00404-023-07092-8

Keywords

Navigation