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Association of embryo transfer type with infertility in endometriosis: a systematic review and meta-analysis

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Abstract

Purpose

The study aims to evaluate whether frozen embryo transfer can restore optimal receptivity leading to better assisted reproductive technology outcomes in women with endometriosis.

Methods

This systematic review and meta-analysis, conducted from January 10, 2021 to July 1, 2021, searched the Cochrane Library, PubMed, Embase, Web of Science, OVID, and Clinicaltrials.gov databases from inception to January 10, 2021. The search strategy combined search terms as follows: (“endometriosis” OR “deep endometriosis” OR “endometrioma”) AND (“frozen-thawed embryo transfer” OR “frozen embryo transfer” OR “freeze-all strategy”) AND (“pregnancy outcome” OR “live birth rate” OR “clinical pregnancy rate” OR “miscarriage rate”). No publication time or language limits were set during the searches. In addition, references of the related articles were searched by hand. Patients were included if they had a history of endometriosis and had received fresh or frozen embryo transfer. Only the first transfer cycle was included. Odds ratios (ORs) and 95% confidence intervals (CIs) were used to express outcomes, and data synthesis was conducted using RevMan, version 5.4 software.

Results

A total of six studies with moderate methodologic quality were retrieved in the meta-analysis. The studies included 3010 women with endometriosis who wanted to conceive; 1777 (59.0%) had frozen embryo transfer, and 1233 (41.0%) had fresh embryo transfer. There was a significantly higher frequency of live births in the frozen embryo group than in the fresh embryo group (OR, 1.53; 95% CI, 1.13–2.08; P = .007). Despite a similar clinical pregnancy rate in the two groups (OR, 1.26; 95% CI, 0.95–1.69; P = .11), the difference in miscarriage rate was significant (OR, 0.70; 95% CI, 0.50–0.97; P = .03). Evidence quality was considered moderate.

Conclusion

Cryopreserved embryo transfer has resulted in preferable reproduction outcomes when compared with fresh embryo transfer in patients with endometriosis, but the evidence is not yet abundant. More strictly designed research is needed to evaluate whether frozen embryo transfer leads to better reproductive outcomes in women with endometriosis compared with those receiving fresh embryo transfer.

Registration number

PROSPERO CRD42021248313.

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References

  1. Saunders P, Horne AW. Endometriosis: etiology, pathobiology, and therapeutic prospects. Cell. 2021;184(11):2807–24.

    Article  CAS  Google Scholar 

  2. Cimadomo D, et al. Definition, diagnostic and therapeutic options in recurrent implantation failure: an international survey of clinicians and embryologists. Hum Reprod. 2021;36(2):305–17.

    Article  CAS  Google Scholar 

  3. Kong H, et al. A multi-center, randomized controlled clinical trial of the application of a shortened protocol of long-acting Triptorelin down-regulated prior to IVF/ICSI among patients with endometriosis: a protocol. Reprod Health. 2018; 15(1).

  4. de Ziegler D, Borghese B, Chapron C. Endometriosis and infertility: pathophysiology and management. Lancet. 2010;376(9742):730–8.

    Article  Google Scholar 

  5. Donnez J, et al. Oxidative stress in the pelvic cavity and its role in the pathogenesis of endometriosis. Fertil Steril. 2016;106(5):1011–7.

    Article  CAS  Google Scholar 

  6. Máté G, Bernstein LR, Török AL. Endometriosis is a cause of infertility. does reactive oxygen damage to gametes and embryos play a key role in the pathogenesis of infertility caused by endometriosis? Front Endocrinol. 2018; 9.

  7. Chapron C, et al. Rethinking mechanisms, diagnosis and management of endometriosis. Nat Rev Endocrinol. 2019;15(11):666–82.

    Article  Google Scholar 

  8. Gonzalez-Comadran M, et al. The impact of endometriosis on the outcome of Assisted Reproductive Technology. Reprod Biol Endocrinol. 2017;15(1):8.

    Article  Google Scholar 

  9. Barnhart K, Dunsmoor-Su R, Coutifaris C. Effect of endometriosis on in vitro fertilization. Fertil Steril. 2002;77(6):1148–55.

    Article  Google Scholar 

  10. Corachan A, et al. Novel therapeutic targets to improve IVF outcomes in endometriosis patients: a review and future prospects. Hum Reprod Update. 2021;27(5):923–72.

    Article  Google Scholar 

  11. Leone RMU, et al. A systematic review on endometriosis during pregnancy: diagnosis, misdiagnosis, complications and outcomes. Hum Reprod Update. 2016;22(1):70–103.

    Article  Google Scholar 

  12. Andersen CY. Grand challenges in reproductive endocrinology. Front Endocrinol. 2017; 7.

  13. Valbuena D, Martin J, de Pablo JL, Remohí J, Pellicer A, Simón C. Increasing levels of estradiol are deleterious to embryonic implantation because they directly affect the embryo. Fertil Steril. 2001;76(5):962–8.

    Article  CAS  Google Scholar 

  14. Lee JH, et al. Machine learning approach to find the relation between endometriosis, benign breast disease, cystitis and non-toxic goiter. Sci Reports. 2019. 9(1).

  15. Wu J, et al. Fertility and neonatal outcomes of freeze-all vs. fresh embryo transfer in women with advanced endometriosis. Front Endocrinol. 2019. 10.

  16. Erşahin AA, et al. Frozen embryo transfer prevents the detrimental effect of high estrogen on endometrium receptivity. J Turk. 2017;18(1):38–42.

    Google Scholar 

  17. Tan J, Cerrillo M, Cruz M, Cecchino GN, Garcia-Velasco JA. Early pregnancy outcomes in fresh versus deferred embryo transfer cycles for endometriosis-associated infertility: a retrospective cohort study. J Clin Med. 2021;10(2):1–9.

    Google Scholar 

  18. Tan Q, et al. MicroRNAs in small extracellular vesicles indicate successful embryo implantation during early pregnancy. Cells. 2020;9(3):645.

    Article  CAS  Google Scholar 

  19. Bourdon M, et al. The deferred embryo transfer strategy improves cumulative pregnancy rates in endometriosis-related infertility: a retrospective matched cohort study. PLOS ONE. 2018;13(4):e0194800.

    Article  Google Scholar 

  20. Fang Wang, X.K.M.L., Clinical outcome of first frozen-thawed embryo transfer cycle after whole embryo cryopreservation in patients with mild endometriosis. Journal of Reproductive Medicine, 2018. 27(3): p. 248–253.

  21. Asoglu MR, Celik C, Bahceci M. Frozen blastocyst transfer improves the chance of live birth in women with endometrioma. Gynecol Endocrinol. 2020;36(10):902–6.

    Article  Google Scholar 

  22. Mohamed AMF, et al. Live birth rate in fresh and frozen embryo transfer cycles in women with endometriosis. Eur J Obstet Gynecol Reprod Biol. 2011;156(2):177–80.

    Article  Google Scholar 

  23. R. Silva Martins, A.H.O.D., Subendometrial resistence and pulsatility index assessment of endometrial receptivity in assisted reproductive technology cycles. Reproductive Biology and Endocrinology, 2019(17): p. 1–7.

  24. Weinerman R, Mainigi M. Why we should transfer frozen instead of fresh embryos: the translational rationale. Fertil Steril. 2014;102(1):10–8.

    Article  Google Scholar 

  25. Ng EH, et al. Comparison of endometrial and subendometrial blood flow measured by three-dimensional power Doppler ultrasound between stimulated and natural cycles in the same patients. Hum Reprod. 2004;19(10):2385–90.

    Article  Google Scholar 

  26. Horcajadas JA, et al. Effect of controlled ovarian hyperstimulation in IVF on endometrial gene expression profiles. MHR Basic Sci Reprod Med. 2005;11(3):195–205.

    Article  CAS  Google Scholar 

  27. Haouzi D, et al. Gene expression profile of human endometrial receptivity: comparison between natural and stimulated cycles for the same patients. Human Reprod (Oxford). 2009;24(6):1436–45.

    Article  CAS  Google Scholar 

  28. Zhu X, et al. Endometrium cytokine profiles are altered following ovarian stimulation but almost not in subsequent hormone replacement cycles. Cytokine. 2019;114:6–10.

    Article  CAS  Google Scholar 

  29. Mirkin S, et al. Gene expression profiles and structural/functional features of the peri-implantation endometrium in natural and gonadotropin-stimulated cycles. J Clin Endocrinol Metab. 2004;89(11):5742–52.

    Article  CAS  Google Scholar 

  30. Du Y, et al. Effect of human chorionic gonadotropin injection before frozen embryo transfer on pregnancy outcomes in endometriosis-associated infertility. Front Med. 2020 7.

  31. Lessey BA, Young SL. What exactly is endometrial receptivity? Fertil Steril. 2019;111(4):611–7.

    Article  Google Scholar 

  32. Wang X, Yu Q. Endometriosis-related ceRNA network to identify predictive biomarkers of endometrial receptivity. Epigenomics. 2019;11(2):147–67.

    Article  CAS  Google Scholar 

  33. Wei D, et al. Frozen versus fresh single blastocyst transfer in ovulatory women: a multicentre, randomised controlled trial. Lancet. 2019;393(10178):1310–8.

    Article  Google Scholar 

Download references

Acknowledgements

We thank the authors of the retrieved studies for their research contributions to the field of reproductive fertility in the setting of endometriosis. We thank BioMed Proofreading® LLC for their copyediting services.

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Authors and Affiliations

  1. Department of Minimally Invasive Gynecology, Beijing Obstetrics and Gynecology Hospital, Capital Medical University, Beijing Maternal and Child Health Care Hospital, No. 17 Qihelou Street, Dong Cheng District, Beijing, 100006, China

    Yanan Chang, Minghong Shen, Sha Wang, Xiao Li & Hua Duan

  2. Department of Gynecology, Shengli Clinical Medical College of Fujian Medical University, Fujian Provincial Hospital, Fuzhou, 350001, Fujian Province, China

    Minghong Shen

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  1. Yanan Chang
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  3. Sha Wang
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  5. Hua Duan
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Contributions

H.D.: conception and design, data collection, analytic strategy, manuscript revision, and final article approval. Y.C.: conception and design, search and collection of data, analysis and synthesis, writing, and final article approval. M.S.: search and collection of data, analysis, manuscript revision, and final article approval. S.W.: collection of data, manuscript revision, and final article approval. X.L.: conception and design, manuscript revision, and final approval.

Corresponding author

Correspondence to Hua Duan.

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The authors declare no competing interests.

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Chang, Y., Shen, M., Wang, S. et al. Association of embryo transfer type with infertility in endometriosis: a systematic review and meta-analysis. J Assist Reprod Genet 39, 1033–1043 (2022). https://doi.org/10.1007/s10815-022-02460-w

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  • DOI: https://doi.org/10.1007/s10815-022-02460-w

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