Determinants of Embryo Implantation: Roles of the Endometrium and Embryo in Implantation Success.
Advanced extrauterine pregnancy
Ectopic pregnancy
Embryo
Endometrium
Livebirth
Journal
Reproductive sciences (Thousand Oaks, Calif.)
ISSN: 1933-7205
Titre abrégé: Reprod Sci
Pays: United States
ID NLM: 101291249
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
received:
28
09
2022
accepted:
15
03
2023
medline:
21
7
2023
pubmed:
30
3
2023
entrez:
29
3
2023
Statut:
ppublish
Résumé
Both uterine endometrium and embryo contribute to implantation success. However, their relative role in the implantation success is still a matter for debate, as are the roles of endometrial receptivity analysis (ERA), endometrial scratch (ES), endometrial microbiome, and intrauterine or intravenous measures that are currently advocated to improve the implantation success. There is insufficient evidence to suggest that the endometrium is more important than the embryo in determining the implantation success and the utility of these measures, especially when euploid embryos are transferred is limited. Although embryo implantation on epithelium other than the endometrium is a very rare event, evidence suggests that embryo implantation and growth is not limited to the endometrium alone. Embryos can implant and develop to result in livebirths on epithelium that lacks the typical endometrial development present at implantation. Currently, the role of embryo euploidy in implantation success is underappreciated. At a minimum, it is the author's opinion that until robust, definitive studies are conducted that demonstrate benefit, reproductive endocrinologists and infertility specialist should be prudent in the way they counsel patients about the utility of ERA, ES, and other measures in improving implantation success.
Identifiants
pubmed: 36988904
doi: 10.1007/s43032-023-01224-w
pii: 10.1007/s43032-023-01224-w
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
2339-2348Informations de copyright
© 2023. The Author(s), under exclusive licence to Society for Reproductive Investigation.
Références
Mascarenhas MN, et al. National, regional, and global trends in infertility prevalence since 1990: a systematic analysis of 277 health surveys. PLoS Med. 2012;9(12): e1001356.
pubmed: 23271957
pmcid: 3525527
Khan SN, et al. Diffused intra-oocyte hydrogen peroxide activates myeloperoxidase and deteriorates oocyte quality. PLoS One. 2015;10(7): e0132388.
pubmed: 26197395
pmcid: 4511228
Xie Y, et al. Transient stress and stress enzyme responses have practical impacts on parameters of embryo development, from IVF to directed differentiation of stem cells. Mol Reprod Dev. 2008;75(4):689–97.
pubmed: 17654540
Liu H, et al. Epigenetic modifications working in the decidualization and endometrial receptivity. Cell Mol Life Sci. 2020;77(11):2091–101.
pubmed: 31813015
Liu KE, Hartman M, Hartman A. Management of thin endometrium in assisted reproduction: a clinical practice guideline from the Canadian Fertility and Andrology Society. Reprod Biomed Online. 2019;39(1):49–62.
pubmed: 31029557
Nikas G, Aghajanova L. Endometrial pinopodes: some more understanding on human implantation? Reprod Biomed Online. 2002;4(Suppl 3):18–23.
pubmed: 12470560
Boomsma CM, et al. Endometrial secretion analysis identifies a cytokine profile predictive of pregnancy in IVF. Hum Reprod. 2009;24(6):1427–35.
pubmed: 19228761
Klimczak AM, et al. B-cell lymphoma 6 expression is not associated with live birth in a normal responder in vitro fertilization population. Fertil Steril. 2022;117(2):351–8.
pubmed: 34809978
Mansouri-Attia N, et al. Endometrium as an early sensor of in vitro embryo manipulation technologies. Proc Natl Acad Sci USA. 2009;106(14):5687–92.
pubmed: 19297625
pmcid: 2667091
Brosens JJ, et al. Uterine selection of human embryos at implantation. Sci Rep. 2014;4:3894.
pubmed: 24503642
pmcid: 3915549
Young SL, et al. Effect of randomized serum progesterone concentration on secretory endometrial histologic development and gene expression. Hum Reprod. 2017;32(9):1903–14.
pubmed: 28854727
pmcid: 5850604
Maclean A, et al. Fallopian tube epithelial cells express androgen receptor and have a distinct hormonal responsiveness when compared with endometrial epithelium. Hum Reprod. 2020;35(9):2097–106.
pubmed: 32876325
Papacleovoulou G, et al. Regulation of 3beta-hydroxysteroid dehydrogenase type 1 and type 2 gene expression and function in the human ovarian surface epithelium by cytokines. Mol Hum Reprod. 2009;15(6):379–92.
pubmed: 19414525
Ikechebelu JI, Onwusulu DN, Chukwugbo CN. Term abdominal pregnancy misdiagnosed as abruptio placenta. Niger J Clin Pract. 2005;8(1):43–5.
pubmed: 16392455
Nassali MN, et al. A case report of an asymptomatic late term abdominal pregnancy with a live birth at 41 weeks of gestation. BMC Res Notes. 2016;9:31.
pubmed: 26785887
pmcid: 4717624
Siati A, et al. Abdominal pregnancy with a healthy newborn: a new case. Pan Afr Med J. 2019;34:35.
pubmed: 31762903
pmcid: 6859041
Puscheck EE, et al. Molecular biology of the stress response in the early embryo and its stem cells. Adv Exp Med Biol. 2015;843:77–128.
pubmed: 25956296
Xie Y, et al. Hypoxic stress induces, but cannot sustain trophoblast stem cell differentiation to labyrinthine placenta due to mitochondrial insufficiency. Stem Cell Res. 2014;13(3 Pt A):478–91.
pubmed: 25239494
pmcid: 4253717
Yang Y, et al. Hypoxic stress forces adaptive and maladaptive placental stress responses in early pregnancy. Birth Defects Res. 2017;109(17):1330–44.
pubmed: 29105384
Yang Y, et al. Blastocyst-derived stem cell populations under stress: impact of nutrition and metabolism on stem cell potency loss and miscarriage. Stem Cell Rev Rep. 2017;13(4):454–64.
pubmed: 28425063
Scott R 3rd, Zhang M, Seli E. Metabolism of the oocyte and the preimplantation embryo: implications for assisted reproduction. Curr Opin Obstet Gynecol. 2018;30(3):163–170.
Gurner KH, et al. A microenvironment of high lactate and low pH created by the blastocyst promotes endometrial receptivity and implantation. Reprod Biomed Online. 2022;44(1):14–26.
pubmed: 34810095
Lucas ES, Salker MS, Brosens JJ. Uterine plasticity and reproductive fitness. Reprod Biomed Online. 2013;27(5):506–14.
pubmed: 23948451
Almquist LD, et al. Endometrial BCL6 testing for the prediction of in vitro fertilization outcomes: a cohort study. Fertil Steril. 2017;108(6):1063–9.
pubmed: 29126613
pmcid: 5726554
Likes CE, et al. Medical or surgical treatment before embryo transfer improves outcomes in women with abnormal endometrial BCL6 expression. J Assist Reprod Genet. 2019;36(3):483–90.
pubmed: 30610661
pmcid: 6439015
Starks G. Tubal conservation with ectopic gestations. A reappraisal. Am Surg. 1984;50(4):222–4.
pubmed: 6231872
Pavlova GA. Tubal muscles determine embryo implantation site; prognosis of ectopic pregnancy at chronic functional disorders. Med Hypotheses. 2019;132: 109332.
pubmed: 31421418
Jiang H, Li JX. Interaction networks between the fallopian tubes and the embryo in human tubal pregnancy: current knowledge and perspectives. J Obstet Gynaecol Res. 2021;47(12):4139–47.
pubmed: 34558156
Elito J Jr, Han KK, Camano L. Tubal patency after clinical treatment of unruptured ectopic pregnancy. Int J Gynaecol Obstet. 2005;88(3):309–13.
Morrison JL. Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clin Exp Pharmacol Physiol. 2008;35(7):730–43.
pubmed: 18498533
Chen W, Itoyama T, Chaganti RS. Splicing factor SRP20 is a novel partner of BCL6 in a t(3;6)(q27;p21) translocation in transformed follicular lymphoma. Genes Chromosomes Cancer. 2001;32(3):281–4.
pubmed: 11579468
Evans-Hoeker E, et al. Endometrial BCL6 overexpression in eutopic endometrium of women with endometriosis. Reprod Sci. 2016;23(9):1234–41.
pubmed: 27222232
pmcid: 5933165
Yoo JY, et al. KRAS Activation and over-expression of SIRT1/BCL6 contributes to the pathogenesis of endometriosis and progesterone resistance. Sci Rep. 2017;7(1):6765.
pubmed: 28754906
pmcid: 5533722
Díaz-Gimeno P, et al. A genomic diagnostic tool for human endometrial receptivity based on the transcriptomic signature. Fertil Steril. 2011;95(1):50–60, 60.e1–15.
Navot D, et al. The window of embryo transfer and the efficiency of human conception in vitro. Fertil Steril. 1991;55(1):114–8.
pubmed: 1986951
Wilcox AJ, Baird DD, Weinberg CR. Time of implantation of the conceptus and loss of pregnancy. N Engl J Med. 1999;340(23):1796–9.
pubmed: 10362823
Genbacev OD, et al. Trophoblast L-selectin-mediated adhesion at the maternal-fetal interface. Science. 2003;299(5605):405–8.
pubmed: 12532021
Ruiz-Alonso M, et al. The endometrial receptivity array for diagnosis and personalized embryo transfer as a treatment for patients with repeated implantation failure. Fertil Steril. 2013;100(3):818–24.
pubmed: 23756099
Arian SE, et al. Endometrial receptivity array before frozen embryo transfer cycles: a systematic review and meta-analysis. Fertil Steril. 2023;119(2):229–38.
Ding J, et al. Trophoblast-derived IL-6 serves as an important factor for normal pregnancy by activating Stat3-mediated M2 macrophages polarization. Int Immunopharmacol. 2021;90: 106788.
pubmed: 32718866
Rőszer T. Understanding the mysterious M2 macrophage through activation markers and effector mechanisms. Mediators Inflamm. 2015;2015: 816460.
pubmed: 26089604
pmcid: 4452191
Ding J, et al. M2 macrophage-derived G-CSF promotes trophoblasts EMT, invasion and migration via activating PI3K/Akt/Erk1/2 pathway to mediate normal pregnancy. J Cell Mol Med. 2021;25(4):2136–47.
pubmed: 33393205
pmcid: 7882967
Nilsson LL, Hviid TVF. HLA Class Ib-receptor interactions during embryo implantation and early pregnancy. Hum Reprod Update. 2022;28(3):435–54.
pubmed: 35234898
Plaks V, et al. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J Clin Invest. 2008;118(12):3954–65.
pubmed: 19033665
pmcid: 2582932
Camargo-Díaz F, et al. Colony stimulating factor-1 and leukemia inhibitor factor expression from current-cycle cannula isolated endometrial cells are associated with increased endometrial receptivity and pregnancy. BMC Womens Health. 2017;17(1):63.
pubmed: 28830391
pmcid: 5567912
Mor G, Aldo P, Alvero AB. The unique immunological and microbial aspects of pregnancy. Nat Rev Immunol. 2017;17(8):469–82.
pubmed: 28627518
Dekel N, et al. The role of inflammation for a successful implantation. Am J Reprod Immunol. 2014;72(2):141–7.
pubmed: 24809430
pmcid: 6800188
Gnainsky Y, et al. Biopsy-induced inflammatory conditions improve endometrial receptivity: the mechanism of action. Reproduction. 2015;149(1):75–85.
pubmed: 25349438
Gnainsky Y, et al. Local injury of the endometrium induces an inflammatory response that promotes successful implantation. Fertil Steril. 2010;94(6):2030–6.
pubmed: 20338560
pmcid: 3025806
Barash A, et al. Local injury to the endometrium doubles the incidence of successful pregnancies in patients undergoing in vitro fertilization. Fertil Steril. 2003;79(6):1317–22.
pubmed: 12798877
Han X, Hu L. The effect of endometrial scratch on pregnancy outcomes of frozen-thawed embryo transfer: a propensity score-matched study. Gynecol Endocrinol. 2022;38(1):39–44.
pubmed: 34279161
Mak JSM, et al. The effect of endometrial scratch on natural-cycle cryopreserved embryo transfer outcomes: a randomized controlled study. Reprod Biomed Online. 2017;35(1):28–36.
pubmed: 28476486
Metwally M, et al. Endometrial scratch to increase live birth rates in women undergoing first-time in vitro fertilisation: RCT and systematic review. Health Technol Assess. 2022;26(10):1–212.
pubmed: 35129113
pmcid: 8859770
Metwally M, et al. A randomised controlled trial to assess the clinical effectiveness and safety of the endometrial scratch procedure prior to first-time IVF, with or without ICSI. Hum Reprod. 2021;36(7):1841–53.
pubmed: 34050362
pmcid: 8213451
Frantz S, et al. Decrease in pregnancy rate after endometrial scratch in women undergoing a first or second in vitro fertilization. A multicenter randomized controlled trial. Hum Reprod. 2019;34(1):92–9.
pubmed: 30496529
Li W, et al. Randomised controlled trials evaluating endometrial scratching: assessment of methodological issues. Hum Reprod. 2019;34(12):2372–80.
pubmed: 31825478
Lensen S, et al. A randomized trial of endometrial scratching before in vitro fertilization. N Engl J Med. 2019;380(4):325–34.
pubmed: 30673547
van Hoogenhuijze NE, et al. Economic evaluation of endometrial scratching before the second IVF/ICSI treatment: a cost-effectiveness analysis of a randomized controlled trial (SCRaTCH trial). Hum Reprod. 2022;37(2):254–63.
pubmed: 34864993
Paulson RJ. Cognitive dissonance in infertility treatment: why is it so difficult to discard disproven therapies, like the endometrial scratch? F S Rep. 2022;3(2):85.
pubmed: 35789722
pmcid: 9250139
Craciunas L, et al. Intrauterine administration of human chorionic gonadotropin (hCG) for subfertile women undergoing assisted reproduction. Cochrane Database Syst Rev. 2016;5:Cd011537.
Kamath MS, Kirubakaran R, Sunkara SK. Granulocyte-colony stimulating factor administration for subfertile women undergoing assisted reproduction. Cochrane Database Syst Rev. 2020;1(1):Cd013226.
pubmed: 31978254
Siristatidis CS, et al. Endometrial injection of embryo culture supernatant for subfertile women in assisted reproduction. Cochrane Database Syst Rev. 2020;8(8):Cd013063.
pubmed: 32797689
Makrigiannakis A, et al. Intrauterine CRH-treated PBMC in repeated implantation failure. Eur J Clin Invest. 2019;49(5): e13084.
pubmed: 30739317
Makrigiannakis A, et al. Repeated implantation failure: a new potential treatment option. Eur J Clin Invest. 2015;45(4):380–4.
pubmed: 25652716
Zhou P, et al. The effect of intralipid on pregnancy outcomes in women with previous implantation failure in in vitro fertilization/intracytoplasmic sperm injection cycles: a systematic review and meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2020;252:187–92.
pubmed: 32622103
Kumar P, Marron K, Harrity C. Intralipid therapy and adverse reproductive outcome: is there any evidence? Reprod Fertil. 2021;2(3):173–86.
pubmed: 35118388
pmcid: 8788620
Pirtea P, et al. Rate of true recurrent implantation failure is low: results of three successive frozen euploid single embryo transfers. Fertil Steril. 2021;115(1):45–53.
pubmed: 33077239
Casper RF. It’s time to pay attention to the endometrium. Fertil Steril. 2011;96(3):519–21.
pubmed: 21880272
Catt JW, Henman M. Toxic effects of oxygen on human embryo development. Hum Reprod. 2000;15(Suppl 2):199–206.
pubmed: 11041525
Kasius A, et al. Endometrial thickness and pregnancy rates after IVF: a systematic review and meta-analysis. Hum Reprod Update. 2014;20(4):530–41.
pubmed: 24664156
Simeonov M, et al. The entire range of trigger-day endometrial thickness in fresh IVF cycles is independently correlated with live birth rate. Reprod Biomed Online. 2020;41(2):239–47.
pubmed: 32532669
Yuan X, et al. Endometrial thickness as a predictor of pregnancy outcomes in 10787 fresh IVF-ICSI cycles. Reprod Biomed Online. 2016;33(2):197–205.
pubmed: 27238372
Lv H, et al. Effect of endometrial thickness and embryo quality on live-birth rate of fresh IVF/ICSI cycles: a retrospective cohort study. Reprod Biol Endocrinol. 2020;18(1):89.
pubmed: 32825835
pmcid: 7441697
Gingold JA, et al. Endometrial pattern, but not endometrial thickness, affects implantation rates in euploid embryo transfers. Fertil Steril. 2015;104(3):620-8.e5.
pubmed: 26079695
pmcid: 4561002
Qiao L, et al. A fetal fraction enrichment method reduces false negatives and increases test success rate of fetal chromosome aneuploidy detection in early pregnancy loss. J Transl Med. 2022;20(1):345.
pubmed: 35918754
pmcid: 9344718
Toikkanen S, Joensuu H, Erkkola R. DNA aneuploidy in ectopic pregnancy and spontaneous abortions. Eur J Obstet Gynecol Reprod Biol. 1993;51(1):9–13.
pubmed: 8282147
Liu J, et al. DNA microarray reveals that high proportions of human blastocysts from women of advanced maternal age are aneuploid and mosaic. Biol Reprod. 2012;87(6):148.
pubmed: 23136294
Huang L, et al. Noninvasive preimplantation genetic testing for aneuploidy in spent medium may be more reliable than trophectoderm biopsy. Proc Natl Acad Sci USA. 2019;116(28):14105–12.
pubmed: 31235575
pmcid: 6628824
Gleicher N, Orvieto R. Is the hypothesis of preimplantation genetic screening (PGS) still supportable? A review. J Ovarian Res. 2017;10(1):21.
pubmed: 28347334
pmcid: 5368937
Capalbo A, et al. FISH reanalysis of inner cell mass and trophectoderm samples of previously array-CGH screened blastocysts shows high accuracy of diagnosis and no major diagnostic impact of mosaicism at the blastocyst stage. Hum Reprod. 2013;28(8):2298–307.
pubmed: 23739221
Johnson DS, et al. Comprehensive analysis of karyotypic mosaicism between trophectoderm and inner cell mass. Mol Hum Reprod. 2010;16(12):944–9.
pubmed: 20643877
pmcid: 2989828
Rubio C, et al. Multicenter prospective study of concordance between embryonic cell-free DNA and trophectoderm biopsies from 1301 human blastocysts. Am J Obstet Gynecol. 2020;223(5):751.e1-751.e13.
pubmed: 32470458
Rubio C, et al. Embryonic cell-free DNA versus trophectoderm biopsy for aneuploidy testing: concordance rate and clinical implications. Fertil Steril. 2019;112(3):510–9.
pubmed: 31200971
Kaye L, et al. Pregnancy rates for single embryo transfer (SET) of day 5 and day 6 blastocysts after cryopreservation by vitrification and slow freeze. J Assist Reprod Genet. 2017;34(7):913–9.
pubmed: 28500451
pmcid: 5476550
Tiegs AW, et al. Worth the wait? Day 7 blastocysts have lower euploidy rates but similar sustained implantation rates as day 5 and day 6 blastocysts. Hum Reprod. 2019;34(9):1632–9.
pubmed: 31402381
Bourdon M, et al. Day 5 versus day 6 blastocyst transfers: a systematic review and meta-analysis of clinical outcomes. Hum Reprod. 2019;34(10):1948–64.
pubmed: 31644803
pmcid: 7967799
Yin X, et al. Increased activation of the PI3K/AKT pathway compromises decidualization of stromal cells from endometriosis. J Clin Endocrinol Metab. 2012;97(1):E35-43.
pubmed: 22072736
Klemmt PA, et al. Stromal cells from endometriotic lesions and endometrium from women with endometriosis have reduced decidualization capacity. Fertil Steril. 2006;85(3):564–72.
pubmed: 16500320
pmcid: 1626574
Aghajanova L, et al. Steroidogenic enzyme and key decidualization marker dysregulation in endometrial stromal cells from women with versus without endometriosis. Biol Reprod. 2009;80(1):105–14.
pubmed: 18815356
pmcid: 2704986
Lessey BA, Kim JJ. Endometrial receptivity in the eutopic endometrium of women with endometriosis: it is affected, and let me show you why. Fertil Steril. 2017;108(1):19–27.
pubmed: 28602477
pmcid: 5629018
Dubernard G, et al. Immunohistochemistry of adhesion molecules, metalloproteinases and NO-synthases in extravillous trophoblast of tubal pregnancy. Cell Mol Biol (Noisy-le-grand). 2005;51 Suppl:Ol829–37.
Lessey BA, Young SL. What exactly is endometrial receptivity? Fertil Steril. 2019;111(4):611–7.
pubmed: 30929718
Xu L, et al. Outcomes of embryo vitrification at different developmental stages: evaluation of 2412 warming cycles. Medicine (Baltimore). 2022;101(19): e29233.
pubmed: 35583531
Zhang B, et al. Reduced ectopic pregnancy rate on day 5 embryo transfer compared with day 3: a meta-analysis. PLoS One. 2017;12(1): e0169837.
pubmed: 28121989
pmcid: 5266274
Fylstra DL. Ovarian ectopic pregnancy 6 years after supracervical cesarean hysterectomy: a case report. J Reprod Med. 2009;54(10):649–51.
pubmed: 20677487
Sadłecki P, Grabiec M, Walentowicz-Sadłecka M. Broad ligament pregnancy - a rare and challenging diagnosis. Clin Case Rep. 2021;9(9): e04823.
pubmed: 34552742
pmcid: 8443409
Son SY, et al. Mesenteric ectopic pregnancy with tubo-ovarian abscess. Radiol Case Rep. 2021;16(5):1165–8.
pubmed: 33777281
pmcid: 7985701
Ganeshselvi P, et al. Primary abdominal pregnancy implanted on the sigmoid colon. J Obstet Gynaecol. 2003;23(6):667.
pubmed: 14617477
Martingano D, et al. Ruptured primary omental pregnancy mimicking adnexal implantation. J Am Osteopath Assoc. 2017;117(2):128–32.
pubmed: 28134955
Garzon S, et al. Primary hepatic pregnancy: report of a case treated with laparoscopic approach and review of the literature. Fertil Steril. 2018;110(5):925-931.e1.
pubmed: 30316439
Chen L, et al. Successful laparoscopic management of diaphragmatic pregnancy:a rare case report and brief review of literature. BMC Pregnancy Childbirth. 2019;19(1):99.
pubmed: 30922250
pmcid: 6438013
Dabiri T, et al. Advanced extrauterine pregnancy at 33 weeks with a healthy newborn. Biomed Res Int. 2014;2014: 102479.
pubmed: 25544940
pmcid: 4273539
Jackson P, et al. A successful pregnancy following total hysterectomy. Br J Obstet Gynaecol. 1980;87(5):353–5.
pubmed: 7387933
Kim MJ, et al. Sonographic diagnosis of a viable abdominal pregnancy with planned delivery after fetal lung maturation. J Clin Ultrasound. 2013;41(9):563–5.
pubmed: 23124825
Gure T, et al. Term abdominal pregnancy with live baby: case report from Hiwot Fana Specialized University Hospital, Eastern Ethiopia. Int Med Case Rep J. 2021;14:689–95.
pubmed: 34616185
pmcid: 8488043
Quaas AM, Paulson RJ. Is the endometrial receptivity analysis batting high enough to warrant widespread-or at least selective-use? Fertil Steril. 2021;116(2):341–2.
pubmed: 34176587