Review of Endometrial Receptivity Array: A Personalized Approach to Embryo Transfer and Its Clinical Applications
Abstract
1. Introduction
2. A Description of Endometrial Receptivity Array
3. ERA in the Context of Natural Frozen Embryo Transfer
4. ERA in the Context of Hormone Replacement Therapy Frozen Embryo Transfer
5. Clinical Outcomes Using ERA in Infertile Women
6. Clinical Outcomes Using ERA in Specific Populations
Study Type | Implantation Rate (RIF) | Implantation Rate (Non-RIF) | Pregnancy Rate (RIF) | Pregnancy Rate (Non-RIF) | Pregnancy Rate (Adenomyosis) | Pregnancy Rate (No Adenomyosis) |
---|---|---|---|---|---|---|
Retrospective cohort study [78] | 33% | 39% | 42.4% ongoing | 56% | N/A | N/A |
Retrospective cohort study [84] | 50% | N/A | 58.5% ongoing, 76.5% clinical | N/A | N/A | N/A |
Retrospective cohort study [38] | N/A | N/A | 58.8% receptive patients, 50% nonreceptive patients | N/A | N/A | N/A |
Prospective case–control study [23] | 33.9% | N/A | 51.7% | N/A | N/A | N/A |
Retrospective cohort study [88] | N/A | N/A | N/A | N/A | 62.5% with ERA, 63.1% without ERA | 63.9% |
7. Summary and Discussion
8. Conclusions
Author Contributions
Funding
Conflicts of Interest
References
- Scott, R.T., Jr.; Ferry, K.; Su, J.; Tao, X.; Scott, K.; Treff, N.R. Comprehensive chromosome screening is highly predictive of the reproductive potential of human embryos: A prospective, blinded, nonselection study. Fertil. Steril. 2012, 97, 870–875. [Google Scholar] [CrossRef] [PubMed]
- Heger, A.; Sator, M.; Pietrowski, D. Endometrial Receptivity and its Predictive Value for IVF/ICSI-Outcome. Geburtshilfe Und Frauenheilkd. 2012, 72, 710–715. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Penzias, A.; Bendikson, K.; Butts, S.; Coutifaris, C.; Falcone, T.; Fossum, G.; Gitlin, S.; Gracia, C.; Hansen, K.; La Barbera, A.; et al. The use of preimplantation genetic testing for aneuploidy (PGT-A): A committee opinion. Fertil. Steril. 2018, 109, 429–436. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Simopoulou, M.; Sfakianoudis, K.; Maziotis, E.; Tsioulou, P.; Grigoriadis, S.; Rapani, A.; Giannelou, P.; Asimakopoulou, M.; Kokkali, G.; Pantou, A.; et al. PGT-A: Who and when? A systematic review and network meta-analysis of RCTs. J. Assist. Reprod. Genet. 2021, 38, 1939–1957. [Google Scholar] [CrossRef] [PubMed]
- Twisk, M.; Mastenbroek, S.; van Wely, M.; Heineman, M.J.; Van Der Veen, F.; Repping, S. Preimplantation genetic screening for abnormal number of chromosomes (aneuploidies) in in vitro fertilisation or intracytoplasmic sperm injection. Cochrane Database Syst. Rev. 2006, CD005291. [Google Scholar] [CrossRef]
- Kliman, H.J.; Frankfurter, D. Clinical approach to recurrent implantation failure: Evidence-based evaluation of the endometrium. Fertil. Steril. 2019, 111, 618–628. [Google Scholar] [CrossRef]
- Achache, H.; Revel, A. Endometrial receptivity markers, the journey to successful embryo implantation. Hum. Reprod. Update 2006, 12, 731–746. [Google Scholar] [CrossRef][Green Version]
- Lessey, B.A.; Young, S.L. What exactly is endometrial receptivity? Fertil. Steril. 2019, 111, 611–617. [Google Scholar] [CrossRef]
- Moustafa, S.; Young, S. Diagnostic and therapeutic options in recurrent implantation failure. F1000Research 2020, 9, 208. [Google Scholar] [CrossRef][Green Version]
- Dorostghoal, M.; Ghaffari, H.-O.; Moramezi, F.; Keikhah, N. Overexpression of Endometrial Estrogen Receptor-Alpha in The Window of Implantation in Women with Unexplained Infertility. Int. J. Fertil. Steril. 2018, 12, 37–42. [Google Scholar] [CrossRef]
- Noyes, R.W.; Hertig, A.T.; Rock, J. Dating the endometrial biopsy. Am. J. Obstet. Gynecol. 1975, 122, 262–263. [Google Scholar] [CrossRef] [PubMed]
- Kliman, H.J.; McSweet, J.C.; Grunert, G.M.; Cardone, V.R.; Cadesky, K.; Keefe, D.L. The endometrial function test (EFT) directs care and predicts ART outcome. Fertil. Steril. 2002, 78, S17. [Google Scholar] [CrossRef]
- Kliman, H.J.; Honig, S.; Walls, D.; Luna, M.; McSweet, J.C.; Copperman, A.B. Optimization of endometrial preparation results in a normal endometrial function test® (EFT®) and good reproductive outcome in donor ovum recipients. J. Assist. Reprod. Genet. 2006, 23, 299–303. [Google Scholar] [CrossRef] [PubMed]
- Soriano, D.; Adler, I.; Bouaziz, J.; Zolti, M.; Eisenberg, V.H.; Goldenberg, M.; Seidman, D.S.; Elizur, S.E. Fertility outcome of laparoscopic treatment in patients with severe endometriosis and repeated in vitro fertilization failures. Fertil. Steril. 2016, 106, 1264–1269. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Littman, E.; Giudice, L.; Lathi, R.; Berker, B.; Milki, A.; Nezhat, C. Role of laparoscopic treatment of endometriosis in patients with failed in vitro fertilization cycles. Fertil. Steril. 2005, 84, 1574–1578. [Google Scholar] [CrossRef] [PubMed]
- Macer, M.L.; Taylor, H.S. Endometriosis and Infertility: A Review of the Pathogenesis and Treatment of Endometriosis-associated Infertility. Obstet. Gynecol. Clin. N. Am. 2012, 39, 535–549. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Díaz-Gimeno, P.; Horcajadas, J.A.; Martinez-Conejero, J.A.; Esteban, F.J.; Alama, P.; Pellicer, A.; Simon, C. A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil. Steril. 2011, 95, 50–60.e15. [Google Scholar] [CrossRef]
- Venter, J.C.; Adams, M.D.; Myers, E.W.; Li, P.W.; Mural, R.J.; Sutton, G.G.; Smith, H.O.; Yandell, M.; Evans, C.A.; Holt, R.A.; et al. The Sequence of the Human Genome. Science 2001, 291, 1304–1351. [Google Scholar] [CrossRef][Green Version]
- Gómez, E.; Ruíz-Alonso, M.; Miravet, J.; Simón, C. Human Endometrial Transcriptomics: Implications for Embryonic Implantation. Cold Spring Harb. Perspect. Med. 2015, 5, a022996. [Google Scholar] [CrossRef]
- Altmäe, S.; Esteban, F.J.; Stavreus-Evers, A.; Simón, C.; Giudice, L.; Lessey, B.A.; Horcajadas, J.A.; Macklon, N.S.; D’Hooghe, T.; Campoy, C.; et al. Guidelines for the design, analysis and interpretation of ‘omics’ data: Focus on human endometrium. Hum. Reprod. Update 2014, 20, 12–28. [Google Scholar] [CrossRef]
- Ruiz-Alonso, M.; Blesa, D.; Simón, C. The genomics of the human endometrium. Biochim. Biophys. Acta BBA-Mol. Basis Dis. 2012, 1822, 1931–1942. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Díaz-Gimeno, P.; Ruiz-Alonso, M.; Blesa, D.; Bosch, N.; Martínez-Conejero, J.A.; Alamá, P.; Garrido, N.; Pellicer, A.; Simón, C. The accuracy and reproducibility of the endometrial receptivity array is superior to histology as a diagnostic method for endometrial receptivity. Fertil. Steril. 2013, 99, 508–517. [Google Scholar] [CrossRef] [PubMed]
- Garrido-Gómez, T.; Ruiz-Alonso, M.; Blesa, D.; Diaz-Gimeno, P.; Vilella, F.; Simón, C. The endometrial receptivity array for diagnosis and personalized embryo transfer as a treatment for patients with repeated implantation failure. Fertil. Steril. 2013, 100, 818–824. [Google Scholar] [CrossRef]
- Wong, K.M.; Mastenbroek, S.; Repping, S. Cryopreservation of human embryos and its contribution to in vitro fertilization success rates. Fertil. Steril. 2014, 102, 19–26. [Google Scholar] [CrossRef]
- Zhang, J.; Du, M.; Li, Z.; Wang, L.; Hu, J.; Zhao, B.; Feng, Y.; Chen, X.; Sun, L. Fresh versus frozen embryo transfer for full-term singleton birth: A retrospective cohort study. J. Ovarian Res. 2018, 11, 59. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Shapiro, B.S.; Daneshmand, S.T.; Garner, F.C.; Aguirre, M.; Hudson, C.; Thomas, S. Evidence of impaired endometrial receptivity after ovarian stimulation for in vitro fertilization: A prospective randomized trial comparing fresh and frozen–thawed embryo transfer in normal responders. Fertil. Steril. 2011, 96, 344–348. [Google Scholar] [CrossRef]
- Bhattacharya, S. Maternal and perinatal outcomes after fresh versus frozen embryo transfer—What is the risk-benefit ratio? Fertil. Steril. 2016, 106, 241–243. [Google Scholar] [CrossRef][Green Version]
- Zhao, J.; Xu, B.; Zhang, Q.; Li, Y.P. Which one has a better obstetric and perinatal outcome in singleton pregnancy, IVF/ICSI or FET?: A systematic review and meta-analysis. Reprod. Biol. Endocrinol. 2016, 14, 51. [Google Scholar] [CrossRef][Green Version]
- Evans, J.; Hannan, N.J.; Edgell, T.A.; Vollenhoven, B.J.; Lutjen, P.J.; Osianlis, T.; Salamonsen, L.A.; Rombauts, L.J.F. Fresh versus frozen embryo transfer: Backing clinical decisions with scientific and clinical evidence. Hum. Reprod. Update 2014, 20, 808–821. [Google Scholar] [CrossRef][Green Version]
- Blanco-Breindel, M.F.; Singh, M.; Kahn, J. Endometrial Receptivity. In StatPearls [Internet]; StatPearls Publishing: Treasure Island, FL, USA, 2023. Available online: http://www.ncbi.nlm.nih.gov/books/NBK587449/ (accessed on 27 March 2023).
- Groenewoud, E.; Cohlen, B.; Al-Oraiby, A.; Brinkhuis, E.; Broekmans, F.; de Bruin, J.; Dool, G.V.D.; Fleisher, K.; Friederich, J.; Goddijn, M.; et al. A randomized controlled, non-inferiority trial of modified natural versus artificial cycle for cryo-thawed embryo transfer. Hum. Reprod. 2016, 31, 1483–1492. [Google Scholar] [CrossRef][Green Version]
- Agha-Hosseini, M.; Hashemi, L.; Aleyasin, A.; Ghasemi, M.; Sarvi, F.; Nashtaei, M.S.; Khodarahmian, M. Natural cycle versus artificial cycle in frozen-thawed embryo transfer: A randomized prospective trial. J. Turk. Soc. Obstet. Gynecol. 2018, 15, 12–17. [Google Scholar] [CrossRef] [PubMed]
- Mumusoglu, S.; Polat, M.; Ozbek, I.Y.; Bozdag, G.; Papanikolaou, E.G.; Esteves, S.C.; Humaidan, P.; Yarali, H. Preparation of the Endometrium for Frozen Embryo Transfer: A Systematic Review. Front. Endocrinol. 2021, 12, 688237. [Google Scholar] [CrossRef] [PubMed]
- Eleftheriadou, A.; Francis, A.; Wilcox, M.; Jayaprakasan, K. Frozen Blastocyst Embryo Transfer: Comparison of Protocols and Factors Influencing Outcome. J. Clin. Med. 2022, 11, 737. [Google Scholar] [CrossRef] [PubMed]
- Greenbaum, S.; Athavale, A.; Klement, A.H.; Bentov, Y. Luteal phase support in fresh and frozen embryo transfers. Front. Reprod. Health 2022, 4, 919948. [Google Scholar] [CrossRef] [PubMed]
- Jia, Y.; Sha, Y.; Qiu, Z.; Guo, Y.; Tan, A.; Huang, Y.; Zhong, Y.; Dong, Y.; Ye, H. Comparison of the Effectiveness of Endometrial Receptivity Analysis (ERA) to Guide Personalized Embryo Transfer with Conventional Frozen Embryo Transfer in 281 Chinese Women with Recurrent Implantation Failure. Med. Sci. Monit. Int. Med. J. Exp. Clin. Res. 2022, 28, e935634. [Google Scholar] [CrossRef]
- Hashimoto, T.; Koizumi, M.; Doshida, M.; Toya, M.; Sagara, E.; Oka, N.; Nakajo, Y.; Aono, N.; Igarashi, H.; Kyono, K. Efficacy of the endometrial receptivity array for repeated implantation failure in Japan: A retrospective, two-centers study. Reprod. Med. Biol. 2017, 16, 290–296. [Google Scholar] [CrossRef]
- Patel, J.A.; Patel, A.J.; Banker, J.M.; Shah, S.I.; Banker, M.R. Personalized embryo transfer helps in improving In vitro fertilization/ICSI outcomes in patients with recurrent implantation failure. J. Hum. Reprod. Sci. 2019, 12, 59–66. [Google Scholar] [CrossRef]
- ERA-EMMA-ALICE-Manual-EndomeTRIO-Manual-USA-2021.pdf [Internet]. Available online: https://www.igenomix.ca/wp-content/uploads/sites/14/2021/10/ERA-EMMA-ALICE-Manual-EndomeTRIO-Manual-USA-2021.pdf (accessed on 27 March 2023).
- Madero, S.; Rodriguez, A.; Vassena, R.; Vernaeve, V. Endometrial preparation: Effect of estrogen dose and administration route on reproductive outcomes in oocyte donation cycles with fresh embryo transfer. Hum. Reprod. 2016, 31, 1755–1764. [Google Scholar] [CrossRef][Green Version]
- Glujovsky, D.; Pesce, R.; Fiszbajn, G.; Sueldo, C.; Hart, R.J.; Ciapponi, A. Endometrial preparation for women undergoing embryo transfer with frozen embryos or embryos derived from donor oocytes. Cochrane Database Syst. Rev. 2020, 2020, CD006359. [Google Scholar] [CrossRef]
- Devroey, P.; Pados, G. Preparation of endometrium for egg donation. Hum. Reprod. Update 1998, 4, 856–861. [Google Scholar] [CrossRef][Green Version]
- Navot, D.; Laufer, N.; Kopolovic, J.; Rabinowitz, R.; Birkenfeld, A.; Lewin, A.; Granat, M.; Margalioth, E.J.; Schenker, J.G. Artificially Induced Endometrial Cycles and Establishment of Pregnancies in the Absence of Ovaries. N. Engl. J. Med. 1986, 314, 806–811. [Google Scholar] [CrossRef] [PubMed]
- Borini, A.; Prato, L.D.; Bianchi, L.; Violini, F.; Cattoli, M.; Flamigni, C. CLINICAL ASSISTED REPRODUCTION: Effect of Duration of Estradiol Replacement on the Outcome of Oocyte Donation. J. Assist. Reprod. Genet. 2001, 18, 187–192. [Google Scholar] [CrossRef] [PubMed]
- Bourdon, M.; Santulli, P.; Maignien, C.; Gayet, V.; Pocate-Cheriet, K.; Marcellin, L.; Chapron, C. The deferred embryo transfer strategy improves cumulative pregnancy rates in endometriosis-related infertility: A retrospective matched cohort study. PLoS ONE 2018, 13, e0194800. [Google Scholar] [CrossRef] [PubMed]
- Sekhon, L.; Feuerstein, J.; Pan, S.; Overbey, J.; Lee, J.A.; Briton-Jones, C.; Flisser, E.; Stein, D.E.; Mukherjee, T.; Grunfeld, L.; et al. Endometrial preparation before the transfer of single, vitrified-warmed, euploid blastocysts: Does the duration of estradiol treatment influence clinical outcome? Fertil. Steril. 2019, 111, 1177–1185.e3. [Google Scholar] [CrossRef]
- Zarei, A.; Sohail, P.; Parsanezhad, M.E.; Alborzi, S.; Samsami, A.; Azizi, M. Comparison of four protocols for luteal phase support in frozen-thawed Embryo transfer cycles: A randomized clinical trial. Arch. Gynecol. Obstet. 2016, 295, 239–246. [Google Scholar] [CrossRef]
- Tabibzadeh, S. Molecular control of the implantation window. Hum. Reprod. Update 1998, 4, 465–471. [Google Scholar] [CrossRef][Green Version]
- Franasiak, J.M.; Ruiz-Alonso, M.; Scott, R.T.; Simón, C. Both slowly developing embryos and a variable pace of luteal endometrial progression may conspire to prevent normal birth in spite of a capable embryo. Fertil. Steril. 2016, 105, 861–866. [Google Scholar] [CrossRef][Green Version]
- Weissman, A. RESULTS—Frozen-Thawed Embryo Transfer—IVF-Worldwide [Internet]. 2017. Available online: https://ivf-worldwide.com/survey/frozen-thawed-embryo-transfer/results-frozen-thawed-embryo-transfer.html (accessed on 25 March 2023).
- Escribá, M.-J.; Bellver, J.; Bosch, E.; Sánchez, M.; Pellicer, A.; Remohí, J. Delaying the initiation of progesterone supplementation until the day of fertilization does not compromise cycle outcome in patients receiving donated oocytes: A randomized study. Fertil. Steril. 2006, 86, 92–97. [Google Scholar] [CrossRef]
- Bergin, K.; Eliner, Y.; Duvall, D.W.; Roger, S.; Elguero, S.; Penzias, A.S.; Sakkas, D.; Vaughan, D.A. The use of propensity score matching to assess the benefit of the endometrial receptivity analysis in frozen embryo transfers. Fertil. Steril. 2021, 116, 396–403. [Google Scholar] [CrossRef]
- Riestenberg, C.; Kroener, L.; Quinn, M.; Ching, K.; Ambartsumyan, G. Routine endometrial receptivity array in first embryo transfer cycles does not improve live birth rate. Fertil. Steril. 2021, 115, 1001–1006. [Google Scholar] [CrossRef]
- Personalized Embryo Transfer (PET) Calculator. Igenomix. (n.d.). Available online: https://clinics.myigenomix.com/pet/calculator (accessed on 24 March 2023).
- Steptoe, P.C.; Edwards, R.G. Reimplantation of a Human Embryo with Subsequent Tubal Pregnancy. Lancet 1976, 307, 880–882. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.; Liu, J.; Collins, G.S.; Salem, S.A.; Liu, X.; Lyle, S.S.; Peck, A.C.; Sills, E.S.; Salem, R.D. Selection of single blastocysts for fresh transfer via standard morphology assessment alone and with array CGH for good prognosis IVF patients: Results from a randomized pilot study. Mol. Cytogenet. 2012, 5, 24. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Kort, J.D.; McCoy, R.C.; Demko, Z.; Lathi, R.B. Are blastocyst aneuploidy rates different between fertile and infertile populations? J. Assist. Reprod. Genet. 2018, 35, 403–408. [Google Scholar] [CrossRef] [PubMed]
- A 5-Year Multicentre Randomized Controlled Trial Comparing Personalized, Frozen and Fresh Blastocyst Transfer in IVF-Reproductive BioMedicine Online [Internet]. Available online: https://www.rbmojournal.com/article/S1472-6483(20)30319-9/fulltext (accessed on 20 April 2023).
- Bassil, R.; Casper, R.; Samara, N.; Hsieh, T.B.; Barzilay, E.; Orvieto, R.; Haas, J. Does the endometrial receptivity array really provide personalized embryo transfer? J. Assist. Reprod. Genet. 2018, 35, 1301–1305. [Google Scholar] [CrossRef]
- Mahajan, N.; Kaur, S.; Alonso, M.R. Window of implantation is significantly displaced in patients with adenomyosis with previous implantation failure as determined by endometrial receptivity assay. J. Hum. Reprod. Sci. 2018, 11, 353–358. [Google Scholar] [CrossRef] [PubMed]
- Hombalegowda, R.; Ziegler, W. Evaluating the role of endometrial receptivity array (era) in patients with first Frozen Embryo Transfers (FET). Fertil. Steril. 2020, 113, e39–e40. [Google Scholar] [CrossRef]
- Neves, A.R.; Devesa, M.; Martínez, F.; Garcia-Martinez, S.; Rodriguez, I.; Polyzos, N.P.; Coroleu, B. What is the clinical impact of the endometrial receptivity array in PGT-A and oocyte donation cycles? J. Assist. Reprod. Genet. 2019, 36, 1901–1908. [Google Scholar] [CrossRef]
- Brosens, J.J.; Salker, M.S.; Teklenburg, G.; Nautiyal, J.; Salter, S.; Lucas, E.S.; Steel, J.H.; Christian, M.; Chan, Y.-W.; Boomsma, C.M.; et al. Uterine Selection of Human Embryos at Implantation. Sci. Rep. 2014, 4, 3894. [Google Scholar] [CrossRef][Green Version]
- Maheshwari, A.; Bari, V.; Bell, J.L.; Bhattacharya, S.; Bhide, P.; Bowler, U.; Brison, D.; Child, T.; Chong, H.Y.; Cheong, Y.; et al. Transfer of thawed frozen embryo versus fresh embryo to improve the healthy baby rate in women undergoing IVF: The E-Freeze RCT. Health Technol. Assess. 2022, 26, 1–142. [Google Scholar] [CrossRef]
- Atkinson, M.; Crittenden, J.; Smith, H.; Sjoblom, C. Retrospective cohort study on preparation regimens for frozen embryo transfer. Reprod. Fertil. 2021, 2, 308–316. [Google Scholar] [CrossRef]
- Lessey, B.A.; Kim, J.J. Endometrial Receptivity in Eutopic Endometrium of Women with Endometriosis It is affected, let me show you why. Fertil. Steril. 2017, 108, 19–27. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Fox, C.; Morin, S.; Jeong, J.W.; Scott, R.T.; Lessey, B.A. Local and systemic factors and implantation: What is the evidence? Fertil. Steril. 2016, 105, 873–884. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Brosens, J.; Verhoeven, H.; Campo, R.; Gianaroli, L.; Gordts, S.; Hazekamp, J.; Hägglund, L.; Mardesic, T.; Varila, E.; Zech, J.; et al. High endometrial aromatase P450 mRNA expression is associated with poor IVF outcome. Hum. Reprod. 2004, 19, 352–356. [Google Scholar] [CrossRef]
- Repeated Implantation Failure: Clinical Approach-Fertility and Sterility [Internet]. Available online: https://www.fertstert.org/article/S0015-0282(12)00324-X/fulltext (accessed on 25 March 2023).
- Stephenson, M.D.; Fluker, M.R. Treatment of repeated unexplained in vitro fertilization failure with intravenous immunoglobulin: A randomized, placebo-controlled Canadian trial. Fertil. Steril. 2000, 74, 1108–1113. [Google Scholar] [CrossRef] [PubMed]
- Meyer, W.R.; Castelbaum, A.J.; Somkuti, S.; Sagoskin, A.W.; Doyle, M.; Harris, J.E.; Lessey, B.A. Hydrosalpinges adversely affect markers of endometrial receptivity. Hum. Reprod. 1997, 12, 1393–1398. [Google Scholar] [CrossRef][Green Version]
- Li, T.C.; Klentzeris, L.; Barratt, C.; Warren, M.A.; Cooke, S.; Cooke, I.D. A study of endometrial morphology in women who failed to conceive in a donor insemination programme. BJOG Int. J. Obstet. Gynaecol. 1993, 100, 935–938. [Google Scholar] [CrossRef]
- Koot, Y.E.M.; van Hooff, S.R.; Boomsma, C.M.; van Leenen, D.; Groot Koerkamp, M.J.A.; Goddijn, M.; Eijkemans, M.J.C.; Fauser, B.C.J.M.; Holstege, F.C.P.; Macklon, N.S. An endometrial gene expression signature accurately predicts recurrent implantation failure after IVF. Sci. Rep. 2016, 6, 19411. [Google Scholar] [CrossRef][Green Version]
- Tapia, A.; Gangi, L.M.; Zegers-Hochschild, F.; Balmaceda, J.; Pommer, R.; Trejo, L.; Pacheco, I.M.; Salvatierra, A.M.; Henríquez, S.; Quezada, M.; et al. Differences in the endometrial transcript profile during the receptive period between women who were refractory to implantation and those who achieved pregnancy. Hum. Reprod. 2007, 23, 340–351. [Google Scholar] [CrossRef][Green Version]
- Mahajan, N. Endometrial receptivity array: Clinical application. J. Hum. Reprod. Sci. 2015, 8, 121–129. [Google Scholar] [CrossRef]
- Tan, J.; Kan, A.; Hitkari, J.; Taylor, B.; Tallon, N.; Warraich, G.; Yuzpe, A.; Nakhuda, G. The role of the endometrial receptivity array (ERA) in patients who have failed euploid embryo transfers. J. Assist. Reprod. Genet. 2018, 35, 683–692. [Google Scholar] [CrossRef]
- Ota, T.; Funabiki, M.; Tada, Y.; Karita, M.; Hayashi, T.; Maeda, K.; Matsubara, T.; Iwaki, Y.; Sugiyama, N.; Henmi, T.; et al. The Reproductive Outcomes for the Infertile Patients with Recurrent Implantation Failures May Be Improved by Endometrial Receptivity Array Test. J. Med. Cases 2019, 10, 138–140. [Google Scholar] [CrossRef][Green Version]
- Kaur, S.; Naidu, P. Why results of endometrial receptivity assay testing should not be discounted in recurrent implantation failure? Onco Fertil. J. 2019, 2, 46. [Google Scholar] [CrossRef]
- Kasahara, Y.; Hashimoto, T.; Yokomizo, R.; Takeshige, Y.; Yoshinaga, K.; Toya, M.; Igarashi, H.; Kishi, H.; Kyono, K. Evaluation of Pregnancy Outcomes of Vitrified-Warmed Blastocyst Transfer before and after Endometrial Receptivity Analysis in Identical Patients with Recurrent Implantation Failure. Fertil. Reprod. 2021, 03, 35–41. [Google Scholar] [CrossRef]
- Ocal, P.; Cift, T.; Bulut, B.; Balcan, E.; Cepni, I.; Aydogan, B.; Irez, T. Recurrent Implantation Failure Is More Frequently Seen in Female Patients with Poor Prognosis. Int. J. Fertil. Steril. 2012, 6, 71–78. [Google Scholar] [PubMed]
- Rose, B.I.; Cover, L.; Brown, S. On the utility of the endometrial receptivity assay (era) to correct recurrent implantation failure (rif): Not as simple as it seems. Fertil. Steril. 2020, 114, e168. [Google Scholar] [CrossRef]
- Eisman, L.E.; Pisarska, M.D.; Wertheimer, S.; Chan, J.L.; Akopians, A.L.; Surrey, M.W.; Danzer, H.C.; Ghadir, S.; Chang, W.Y.; Alexander, C.J.; et al. Clinical utility of the endometrial receptivity analysis in women with prior failed transfers. J. Assist. Reprod. Genet. 2021, 38, 645–650. [Google Scholar] [CrossRef]
- Cozzolino, M.; Diaz-Gimeno, P.; Pellicer, A.; Garrido, N. Evaluation of the endometrial receptivity assay and the preimplantation genetic test for aneuploidy in overcoming recurrent implantation failure. J. Assist. Reprod. Genet. 2020, 37, 2989–2997. [Google Scholar] [CrossRef]
- Hiraoka, T.; Hirota, Y.; Osuga, Y. How does adenomyosis impact endometrial receptivity? An updated systematic review of clinical and molecular insights. F&S Rev. 2022, 4, 15–25. [Google Scholar] [CrossRef]
- Vercellini, P.; Consonni, D.; Dridi, D.; Bracco, B.; Frattaruolo, M.P.; Somigliana, E. Uterine adenomyosis and in vitro fertilization outcome: A systematic review and meta-analysis. Hum. Reprod. 2014, 29, 964–977. [Google Scholar] [CrossRef][Green Version]
- Squillace, A.L.; Simonian, D.S.; Allegro, M.C.; Júnior, E.B.; Bianchi, P.H.D.M.; Bibancos, M. Adenomyosis and in vitro fertilization impacts—A literature review. JBRA Assist. Reprod. 2021, 25, 303–309. [Google Scholar] [CrossRef]
- Garcia-Velasco, J.A.; Fassbender, A.; Ruiz-Alonso, M.; Blesa, D.; D‘hooghe, T.; Simon, C. Is endometrial receptivity transcriptomics affected in women with endometriosis? A pilot study. Reprod. Biomed. Online 2015, 31, 647–654. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Cousineau, T.M.; Domar, A.D. Psychological impact of infertility. Best Practice Res. Clin. Obstet. Gynaecol. 2007, 21, 293–308. [Google Scholar] [CrossRef] [PubMed]
- Coughlan, C. What to do when good-quality embryos repeatedly fail to implant. Best Practice Res. Clin. Obstet. Gynaecol. 2018, 53, 48–59. [Google Scholar] [CrossRef] [PubMed]
- Santos-Ribeiro, S.; Siffain, J.; Polyzos, N.P.; van de Vijver, A.; van Landuyt, L.; Stoop, D.; Tournaye, H.; Blockeel, C. To delay or not to delay a frozen embryo transfer after a failed fresh embryo transfer attempt? Fertil. Steril. 2016, 105, 1202–1207.e1. [Google Scholar] [CrossRef] [PubMed][Green Version]
- Brogaard, K. What Is an Endometrial Receptivity Array (ERA)? [Internet]. Path Fertility. 2018. Available online: https://pathfertility.com/what-is-an-endometrial-receptivity-array-era/ (accessed on 27 March 2023).
- What Is ERA? Do I Need an ERA Test for Successful IVF? [Internet]. RMA Network-Fertility Clinic. 2021. Available online: https://rmanetwork.com/blog/era-test-for-ivf-endometrial-receptivity-analysis/ (accessed on 27 March 2023).
- ColoCRM. How Much Does IVF Cost?|IVF Costs [Internet]. CCRM Fertility. Available online: https://www.ccrmivf.com/ivf-cost/ (accessed on 27 March 2023).
- How Much Does IVF Cost In 2023?—Forbes Health [Internet]. Available online: https://www.forbes.com/health/family/how-much-does-ivf-cost/ (accessed on 29 March 2023).
- The Cost of IVF in 2022 [Internet]. Available online: https://fertilityspace.io/blog/the-cost-of-ivf-in-2022 (accessed on 27 March 2023).
- Bergh, P.A.; Navot, D. The impact of embryonic development and endometrial maturity on the timing of implantation. Fertil. Steril. 1992, 58, 537–542. [Google Scholar] [CrossRef]
- Cohen, A.M.; Ye, X.Y.; Colgan, T.J.; Greenblatt, E.M.; Chan, C. Comparing endometrial receptivity array to histologic dating of the endometrium in women with a history of implantation failure. Syst. Biol. Reprod. Med. 2020, 66, 347–354. [Google Scholar] [CrossRef]
- Endometrial Receptivity Revisited: Endometrial Transcriptome Adjusted for Tissue Cellular Heterogeneity|Human Reproduction|Oxford Academic [Internet]. Available online: https://academic.oup.com/humrep/article/33/11/2074/5123535?login=false (accessed on 27 March 2023).
- Coutifaris, C.; Myers, E.R.; Guzick, D.S.; Diamond, M.P.; Carson, S.A.; Legro, R.S.; McGovern, P.G.; Schlaff, W.D.; Carr, B.R.; Steinkampf, M.P.; et al. Histological dating of timed endometrial biopsy tissue is not related to fertility status. Fertil. Steril. 2004, 82, 1264–1272. [Google Scholar] [CrossRef]
Retrospective Cohort Study: No Prior Genetic Screening [57] | |||
---|---|---|---|
Variable | Non-ERA Group | ERA Group | |
Live birth rate | 39.7% | 50% | |
Miscarriage rate | 10.7% | 5.6% | |
Retrospective Cohort Studies: With Prior Genetic Screening | |||
Study 1 [58] | |||
Variable | Non-ERA Group | ERA Group (Receptive Only) | ERA Group (With Adjustment) |
Pregnancy rate | 35.2% | 39% | 33.3% |
Study 2 [59] | |||
Variable | Non-ERA Group | ERA Group | |
Implantation rate | 65% | 55.6% | |
Pregnancy rate | 70% | 58.3% | |
Study 3 [54]: | |||
Variable | Non-ERA Group | ERA Group | |
Live birth rate | 54.96% | 49.62% | |
Positive pregnancy test rate | 74.50% | 69.17% | |
Clinical pregnancy rate | 61.76% | 61.65% | |
Miscarriage rate | 6.52% | 8.27% | |
Prospective Cohort Study: With Prior Genetic Screening [55] | |||
Variable | Non-ERA Group | ERA Group | |
Live birth rate | 56.6% | 56.5% | |
Randomized Controlled Trial: With Prior Genetic Screening [60] | |||
Variable | Non-ERA Group (Fresh Embryo Transfer) | Non-ERA Group (FET) | ERA Group (pET) |
Pregnancy rate (first embryo transfer) | 58.5% | 54.3% | 72.5% |
Pregnancy rate (cumulative) | 80.7% | 79.7% | 93.6% |
Live birth rate (first embryo transfer) | 45.7% | 42.4% | 56.2% |
Live birth rate (cumulative) | 48.9% | 55.4% | 71.2% |
Implantation rate | 38.6% | 43.2% | 57.3% |
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content. |
© 2023 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Rubin, S.C.; Abdulkadir, M.; Lewis, J.; Harutyunyan, A.; Hirani, R.; Grimes, C.L. Review of Endometrial Receptivity Array: A Personalized Approach to Embryo Transfer and Its Clinical Applications. J. Pers. Med. 2023, 13, 749. https://doi.org/10.3390/jpm13050749
Rubin SC, Abdulkadir M, Lewis J, Harutyunyan A, Hirani R, Grimes CL. Review of Endometrial Receptivity Array: A Personalized Approach to Embryo Transfer and Its Clinical Applications. Journal of Personalized Medicine. 2023; 13(5):749. https://doi.org/10.3390/jpm13050749
Chicago/Turabian StyleRubin, Sarah C., Mawerdi Abdulkadir, Joshua Lewis, Aleksandr Harutyunyan, Rahim Hirani, and Cara L. Grimes. 2023. "Review of Endometrial Receptivity Array: A Personalized Approach to Embryo Transfer and Its Clinical Applications" Journal of Personalized Medicine 13, no. 5: 749. https://doi.org/10.3390/jpm13050749
APA StyleRubin, S. C., Abdulkadir, M., Lewis, J., Harutyunyan, A., Hirani, R., & Grimes, C. L. (2023). Review of Endometrial Receptivity Array: A Personalized Approach to Embryo Transfer and Its Clinical Applications. Journal of Personalized Medicine, 13(5), 749. https://doi.org/10.3390/jpm13050749