Pregnancies through oocyte donation. A mini review of pathways involved in placental dysfunction
Javier Caradeux1*† 
Benjamín Fernández1 Francisco Ávila1 Andrés Valenzuela1 Mauricio Mondión2 Francesc Figueras3†- 1Department of Obstetrics and Gynecology, Clínica Santa María, Santiago, Chile
- 2Shady Groove Fertility, Santiago, Chile
- 3Fetal Medicine Research Center, BCNatal, Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Deu), Institut Clínic de Ginecologia, Obstetrícia i Neonatologia, Universitat de Barcelona, Barcelona, Spain
Pregnancies resulting from assisted reproductive techniques (ART) are increasingly prevalent worldwide. While most pregnancies conceived through in-vitro fertilization (IVF) progress without complications, mounting evidence suggests that these pregnancies are at a heightened risk of adverse perinatal outcomes. Specifically, IVF pregnancies involving oocyte donation have garnered attention due to numerous reports indicating an elevated risk profile for pregnancy-related complications within this subgroup of patients. The precise mechanisms contributing to this increased risk of complications remain incompletely understood. Nonetheless, it is likely that they are mediated by an abnormal immune response at the fetal–maternal interface. Additionally, these outcomes may be influenced by baseline patient characteristics, such as the etiology of infertility, absence of corpus luteum, and variations in endometrial preparation protocols, among other factors. This review aims to succinctly summarize the most widely accepted mechanisms that potentially contribute to the onset of placental dysfunction in pregnancies conceived through oocyte donation.
Introduction
Pregnancies through assisted reproductive techniques (ART) are on the rise worldwide; current estimates report nearly 3.2 million cycles per year, with Asia, Europe, and North America as the major contributors (1). The increasing numbers can be partially explained by lower cost and easier access to ART facilities (2, 3), a progressive delay in maternal age at first pregnancy (4, 5), and policymaking and social acceptance of non-traditional families (6, 7).
Even though most pregnancies through in-vitro fertilization (IVF) evolve without pregnancy-related complications (8, 9), there is growing evidence that these pregnancies are at higher risk of adverse perinatal outcomes such as preterm birth, preeclampsia, fetal growth restriction and stillbirth (10–15). Recently, the Society of Maternal & Fetal Medicine (SMFM) released a series of recommendations highlighting the need for proper study and management (16).
The exact mechanisms that lead to the increased risk of pregnancy complications are not fully understood, they are probably mediated by baseline characteristics such as maternal age and comorbidities, intrinsic factors of infertility and the interventions carried out during the fertilization process. This is reflected in how perinatal risks vary according to the fertilization method used, the endometrial preparation protocols, the presence of corpus luteum, the selected transfer method (frozen vs. fresh embryo transfer), and the origin of the selected oocyte (12, 14, 17–22).
Donated oocytes, perinatal outcomes, and placental dysfunction
Among ART, IVF pregnancies through oocyte donation (OD) represent roughly 5 to 7% of all embryo transfers (4, 23), also with an increasing trend over time. In the last few years, these pregnancies have gained attention as several reports have demonstrated a higher risk profile of pregnancy-related complications (24–26).
When compared against IVF conceived with autologous oocytes, pregnancies from OD have shown lower placental volumes at the first trimester (27), a different uterine perfusion profile across gestation (28, 29), higher rates of villitis of unknown etiology (VUE) (30) and also an increased risk of preeclampsia (14, 26) and placental related disease in the third trimester (14, 17, 31–33).
More recently a retrospective study conducted by our group (34), compared antenatal indicators of placental dysfunction between donated and autologous oocytes in the third trimester, demonstrating an abnormal growth velocity from the second trimester to delivery among ART gestations, especially in those conceived with donated oocytes. These findings support mechanisms related to progressive placental dysfunction, rather than abnormal placentation.
Mechanisms involved in placental dysfunction in OD
Placental dysfunction can manifest in different ways, such as preterm birth, fetal growth restriction, preeclampsia and stillbirth, among others (35–38). In line with the above, several mechanisms have been involved in the onset of placental dysfunction and preeclampsia (39) among pregnancies conceived through OD. In the following sections, these pathways are addressed.
Baseline characteristics and infertility etiology
Among infertile couples, several baseline characteristics could be related to a higher risk of placental dysfunction and preeclampsia. Among them maternal age is still one of the main factors related with IVF success (40, 41). While this is true for IVF with autologous oocytes, some studies have shown that pregnancy outcomes (i.e., cumulative live rate) among gestations conceived through OD depend mainly on donor age (42, 43). However, the former seems to not apply when it comes to the risk of placental related disease (44). In fact, several factors may interact as mediators for placental dysfunction; first, there is consistent evidence that women with advanced maternal age have more comorbidities, a higher risk of preeclampsia and present more complicated patterns of multimorbidity during pregnancy (45–47). Second, endometrial receptivity has been proposed to be negatively affected by age, potentially influencing implantation, placental function and pregnancy outcome (48, 49), yet further studies are needed. Finally, infertility etiology could also influence pregnancy outcomes; A diminished ovarian reserve, which is a common indication of ART with OD, has been proposed as an indicator of a reduced vascular capacity and has been independently associated with a higher risk of preeclampsia and placental malperfusion lesions (50, 51). Also, premature ovarian failure, recurrent pregnancy loss and idiopathic infertility have been related with several underlying autoimmune diseases (i.e., systemic lupus erythematosus and antiphospholipid syndrome) (52–54), all conditions highly related with placental dysfunction, preeclampsia and adverse pregnancy outcome (55, 56). Other conditions such as endometriosis have been related with a reduced oocyte yield and a dysregulated decidualization leading to a reduced fertilization rate and a higher risk of preeclampsia (57–61). Also, polycystic ovarian syndrome has been related with an increased oxidative stress and chronic inflammation leading to a higher risk of VUE and hypertensive disorder of pregnancy (62–67). Moreover, altered pathways in lipids and glucose metabolism have been proposed to lead to altered placental structure, villous overcrowding, and finally abnormal placental function (68–70). Although by themselves they do not constitute a frequent indication for OD, they may coexist and act as contributing factors to placental dysfunction.
Embryo transfer method, endometrial preparation protocols, and role of corpus luteum
Several publications demonstrate a different risk profile according to the selected ART protocol (71, 72). Overall, most evidence supports that frozen embryo transfer (FET) presents (among others) a lower risk of small for gestational age and perinatal mortality, but a higher-risk of preeclampsia and placental disease when compared with fresh embryo transfer (14, 71, 73). Regardless, in the last few years the use of FET has presented a progressive increase (23), in part due to a reduced risk of ovarian hyperstimulation syndrome and the expansion of the “freeze all” strategy (which facilitates single embryo transfer and allows time for preimplantation genetic testing).
Although the above refers to studies carried out mainly in IVF with autologous oocytes, when it comes to pregnancies through OD, pooled data report that nearly 40% of them come from FET (23). The former is relevant as it has been argued that the increased risk of preeclampsia found in FET could be linked with the selected protocol for embryo transfer, rather than the cryopreservation and freezing-thawing process itself (74, 75).
Briefly, commonly used protocols for embryo transfer could be summarized in, natural cycles, stimulated cycles, and programmed cycles. In the latter, there is no ovulation associated, therefore no corpus luteum (CL). This becomes relevant as programmed cycles are employed in OD and there is consistent evidence that CL produces not only progesterone and estrogen, but also Relaxin and VEGF. The last two have been found to be implicated in maternal renal and circulatory pregnancy-adaptation and are not replaced during programmed cycles (20, 21, 76). Also, impaired endometrial receptivity has been linked with placental dysfunction among IVF (77). Therefore, it is plausible that the absence of these factors could contribute to an abnormal uterine environment, a suboptimal endometrium support with impaired decidualization, and an insufficient maternal-pregnancy adaptation (78). Thus, leading to the higher risk of placental dysfunction found in pregnancies through OD.
Developmental stage at embryo transfer (i.e., blastocyst-vs. cleavage-stage) has been proposed to influence perinatal outcomes (79, 80). To date, exploring the independent effect of developmental stage at the time of transfer and the impact of cryopreservation on the outcome of interest has been challenging. A recent network meta-analysis (81) demonstrates (with a very-low certainty of evidence) that frozen-blastocyst transfer was associated with a reduction in the risk for LBW compared with both fresh-transfer modalities, and fresh-cleavage transfer may be associated with a reduction in the risk for perinatal death compared with frozen-blastocyst transfer. However, high-quality RCTs and individual participant data meta-analyses are still lacking.
Preimplantation genetic testing
Similar to the reported increase of pregnancies conceived through ART (1), the use of preimplantation genetic testing (PGT) has demonstrated a progressive increase over time (82, 83). In part due a higher risk of pregnancies with chromosomal abnormalities among patients with advanced maternal age and the possibility of testing for several inherited disorders among patients with recurrent pregnancy loss and recurrent implantation failure, among others (83). Most of PGT are conducted through trophectoderm biopsy, in which 5 to 10 trophectoderm cells are extracted as study samples (83–85). As placenta develops from the trophectoderm (86), there is some concern that the use of PGT could be related to defective placentation and the development of placental dysfunction (87, 88), thus increasing the risk of pregnancy complications such as hypertensive disorder of pregnancy and preeclampsia among others (89, 90). While initial meta-analyses showed that PGT pregnancies were associated with a higher risk of hypertensive disorder of pregnancy, their results were limited by a high sample heterogeneity (91, 92). A most recent systematic review and meta-analysis, restricted only to singletons from FET cycles, including 11.469 live births after PGT and 20.438 live births after IVF/ICSI (no-PGT), concludes that trophectoderm biopsy does not alter the risk of developing hypertensive disorders in subsequent pregnancies (84). Nonetheless, larger cohort studies and well-designed RCTs are still lacking.
Regardless of the above, the use of PGT could be considered at least as non-routine among pregnancies through OD. Since, it has been shown to report no benefit among fresh oocyte donation cycles recipients (93–95), and conflicting results have been reported for frozen oocyte donation cycles recipients (95, 96). Therefore, it seems reasonable not to consider PGT as a major contributing factor for placental dysfunction among OD pregnancies.
Immune tolerance breakdown
Normal placentation and pregnancy evolution requires the development of maternal immune tolerance to a semi-allogeneic fetus. To date, most accepted mechanisms involved in pregnancy immunomodulation and crosstalk between mother and fetus include; (i) a trophoblast with an overall poor antigenicity, mainly due to a lack of classic HLA-I and II antigens, with the exception of HLA-C, and the expression of nonclassical HLA molecules of class E and G (97, 98); (ii) a shift in the functional balance of T helper (Th) cells towards type-2 cells with a decline in cell-mediated Th1-type immunity (99); (iii) a change in the activity of uterine natural killer (uNK) cells from cytotoxic to regulatory, mainly producing chemokines, growth factors, cytokines and angiogenic factors, of relevance for the development of maternal–fetal interface (100); and (iv) a major proportion of macrophages with an anti-inflammatory, M2-like phenotype, involved in the dampening of immune reactions (98).
Several findings support the role of immunological dysfunction in the development of preeclampsia among spontaneous conception (39, 100). Pregnancy after OD is considered as a unique model to assess the immunologic pathways involved in placental dysfunction, as the fetus is an absolute allograft in contrast to semi-allograft fetus in natural conception.
In line with the above, it has been shown that among OD pregnancies, the degree of HLA mismatch between mother and fetus is correlated with a higher number of maternal decidual-activated CD4+ Treg cells (101–104), a reduced number of tissue macrophages (105, 106), and the development of gestational hypertension and preeclampsia (107, 108). Furthermore, the risk of preeclampsia has been reported to be even higher among pregnancies conceived with double gamete donation (oocyte and sperm donation) (109), which could be attributed to an additive effect from the lack of paternal antigen-specific tolerance (97).
Also, genome-wide mRNA analysis in placentas from OD pregnancies have shown a reduced expression of thrombomodulin (110), several complement regulatory proteins (111), and altered immunoregulation by co-inhibitory pathways (112).
Moreover, several placental lesions are observed at different histologic levels in women with pregnancies conceived through OD, supporting an abnormal immune response. Of remark, (i) severe chronic deciduitis with dense fibrinoid deposition is a characteristic finding in OD pregnancy. Suggesting an important maternal alloimmune reaction resembling host versus graft disease at the human fetal–maternal interface (113). (ii) Also, a significantly increased prevalence of VUE is reported among pregnancies conceived through OD (30) which represent a manifestation of maternal anti-fetal rejection. (iii) Of remark, Schonkeren et al. (114) described a specific histologic lesion among uncomplicated OD pregnancies consistent on a diffuse inflammatory infiltrate involving the entire chorionic plate. In their study, preeclampsia occurs only in the group without the immunological lesion. Therefore, this lesion could reflect a protective immune mechanism towards the completely allogeneic fetus.
Other mechanisms
It is known that there are social determinants for placental insufficiency, being more prevalent among women from disfavoured socioeconomic status (115). The pathways operating these relationships are not fully understood, and epigenetic mechanisms may explain intergenerational transmission (116). A fraction of egg donations is non-altruistically motivated, making donors more likely to come from a more disadvantaged socioeconomic background, which could result in higher rates of perinatal complications in recipients.
Discussion
The development of ART and specifically the progress achieved in conceiving pregnancies through OD represent a significant opportunity for couples which under other conditions would not be able to achieve pregnancy. However, it should be acknowledged that there is consistent evidence of a higher risk profile among this subgroup of patients.
In this mini review, we intended to succinctly summarize the most widely accepted pathways linked with placental dysfunction. Overall, it could be stated that several non-exclusive physio pathological mechanisms are involved, rendering to these patients a cumulative higher risk of progressive placental dysfunction and preeclampsia.
It is our belief that the subgroup of OD pregnant patients requires further attention. First, already among infertile populations there are reports of higher morbidity & mortality (117, 118). Second, at the population level, there is a progressive and consistent trend of increasing numbers. Theoretically, this could lead to a worldwide higher frequency of preeclampsia. Third, at the individual level, the patient baseline characteristics plus the combination of the physio pathological mechanisms involved could potentially lead to more severe cases (119–121).
Regarding management of ART pregnancies, current recommendation from the Society of Maternal–Fetal Medicine (16) and the UK National Institute of Clinical Excellence (122), consider IVF as a moderate risk factor for preeclampsia and recommends low-dose aspirin and serial scanning only if an additional risk factor is found. However, these guidelines lump together all ART techniques as an overall category, without establishing differences between the mode of conception. Moreover, there are no clear recommendations regarding other surveillance tools, such as maternal and fetal Doppler assessment or angiogenic markers assessment, which arguably have shown moderate-to-good performance for the prediction of adverse perinatal outcomes among high-risk pregnancies (123, 124), and has been proposed as a tool to capture placental dysfunction secondary to pathophysiologic mechanisms other than early defective trophoblast invasion (125, 126).
There are still several research gaps and potential future developments in the field; for one side, there is a need for better characterization and a more complete risk-profile assessment of candidates for OD. In line with the above, identifying novel predictive factors to assess the risk for maternal serious complications may be of value (127). Also, evaluation for signs of immune tolerance breakdown, through the assessment of cellular subpopulations imbalance or its product (such as cytokines or chemokines) (128) and its correlation with known clinical signs of placental dysfunction (i.e., angiogenic markers or fetal & maternal Doppler), could also be explored. Moreover, HLA screening and matching could also be considered as a suitable tool attempting to decrease the reported immune tolerance disbalance (129).
Therapeutic interventions such as the use of some immunosuppressive agents have already shown some encouraging results enhancing outcomes among patients with recurrent pregnancy loss. Among them, hydroxychloroquine is a known anti-inflammatory and immune regulator drug commonly used in patients with autoantibodies disease. Its use during pregnancy has shown to improve the live birth rate in patients with persistent positive antiphospholipid antibodies and to reduce the risk of preeclampsia and fetal loss in mid and late pregnancy among patients with systemic lupus erythematosus (130–132). Also, when combined with prednisone, it has shown to improve outcomes of frozen embryo transfer in antinuclear antibody-positive patients undergoing IVF/ICSI treatment (133). Moreover, its use has been reported as an effective therapeutic strategy in women with repeated implantation failure due cellular immune abnormalities, through a shift in Th2 responses (134). Therefore, hydroxychloroquine could be proposed as a potential treatment for immune tolerance imbalance among pregnancies through OD. However, there is still scarcity of high-quality data that precludes further recommendations (135, 136). Finally, up to date and evidence based counselling about the related short and long-term risk should be offered to OD candidates, as in some cases the risk may be significant, and even overcome the benefits (137–141).
In conclusion, compelling evidence suggests the convergence of various additive factors associated with placental dysfunction in pregnancies conceived through oocyte donation. These factors encompass patient baseline characteristics, absence of corpus luteum, and dysfunction in pregnancy immune tolerance. Further research is imperative as this demographic constitutes a subgroup exhibiting the highest susceptibility to placental dysfunction, potentially necessitating a more vigilant follow-up – a practice not presently endorsed by existing guidelines.
Author contributions
JC: Writing – original draft, Writing – review & editing. BF: Writing – original draft. FÁ: Writing – original draft. AV: Writing – original draft. MM: Writing – review & editing. FF: Writing – review & editing.
Funding
The author(s) declare that no financial support was received for the research, authorship, and/or publication of this article.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.
Publisher’s note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
References
1. Adamson, GD, Zegers-Hochschild, F, and Dyer, S. Global fertility care with assisted reproductive technology. Fertil Steril. (2023) 120:473–82. doi: 10.1016/j.fertnstert.2023.01.013
2. Chiware, TM, Vermeulen, N, Blondeel, K, Farquharson, R, Kiarie, J, and Lundin, K. IVF and other ART in low-and middle-income countries: a systematic landscape analysis. Hum Reprod Update. (2021) 27:213–28. doi: 10.1093/humupd/dmaa047
3. Imrie, R, Ghosh, S, Narvekar, N, Vigneswaran, K, Wang, Y, and Savvas, M. Socioeconomic status and fertility treatment outcomes in high-income countries: a review of the current literature. Hum Fertil. (2023) 26:27–37. doi: 10.1080/14647273.2021.1957503
4. Adamson, GD, Zegers-Hochschild, F, Dyer, S, Chambers, G, de Mouzon, J, and Ishihara, O, International Committee for Monitoring Assisted Reproductive Technology: World report on assisted reproductive technology, (2018). Available at:https://www.icmartivf.org/reports-publications/ (Accessed December 14, 2022)
5. OECD Family Database – OECD. Available at:https://www.oecd.org/els/family/database.htm, (Accessed September 17, 2023)
6. Inhorn, MC, and Patrizio, P. Infertility around the globe: new thinking on gender, reproductive technologies and global movements in the 21st century. Hum Reprod Update. (2015) 21:411–26. doi: 10.1093/humupd/dmv016
7. Fertility treatment: trends and figures|HFEA. (2019), Available at:https://www.hfea.gov.uk/about-us/publications/research-and-data/fertility-treatment-2019-trends-and-figures/#Section7 (Accessed October 17, 2023)
8. Cutting, R. Single embryo transfer for all. Best Pract Res Clin Obstet Gynaecol. (2018) 53:30–7. doi: 10.1016/j.bpobgyn.2018.07.001
9. Shah, JS, Vaughan, DA, Leung, A, Korkidakis, A, Figueras, F, and Garcia, D. Perinatal outcomes in singleton pregnancies after in vitro fertilization cycles over 24 years. Fertil Steril. (2021) 116:27–35. doi: 10.1016/j.fertnstert.2021.01.043
10. Qin, J-B, Sheng, X-Q, Wu, D, Gao, S-Y, You, Y-P, and Yang, T-B. Worldwide prevalence of adverse pregnancy outcomes among singleton pregnancies after in vitro fertilization/intracytoplasmic sperm injection: a systematic review and meta-analysis. Arch Gynecol Obstet. (2017) 295:285–301. doi: 10.1007/s00404-016-4250-3
11. Cavoretto, P, Candiani, M, Giorgione, V, Inversetti, A, Abu-Saba, MM, and Tiberio, F. Risk of spontaneous preterm birth in singleton pregnancies conceived after IVF/ICSI treatment: meta-analysis of cohort studies. Ultrasound Obstet Gynecol. (2018) 51:43–53. doi: 10.1002/uog.18930
12. Bay, B, Boie, S, and Kesmodel, US. Risk of stillbirth in low-risk singleton term pregnancies following fertility treatment: a national cohort study. BJOG. (2019) 126:253–60. doi: 10.1111/1471-0528.15509
13. Cavoretto, PI, Giorgione, V, Sotiriadis, A, Viganò, P, Papaleo, E, and Galdini, A. IVF/ICSI treatment and the risk of iatrogenic preterm birth in singleton pregnancies: systematic review and meta-analysis of cohort studies. J Matern Fetal Neonatal Med. (2020) 35:1987–96. doi: 10.1080/14767058.2020.1771690
14. Chih, HJ, Elias, FTS, Gaudet, L, and Velez, MP. Assisted reproductive technology and hypertensive disorders of pregnancy: systematic review and meta-analyses. BMC Pregnancy Childbirth. (2021) 21:449. doi: 10.1186/s12884-021-03938-8
15. Sarmon, KG, Eliasen, T, Knudsen, UB, and Bay, B. Assisted reproductive technologies and the risk of stillbirth in singleton pregnancies: a systematic review and meta-analysis. Fertil Steril. (2021) 116:784–92. doi: 10.1016/j.fertnstert.2021.04.007
16. Society for Maternal-Fetal Medicine (SMFM)Ghidini, A, Gandhi, M, Mccoy, J, and Kuller, JA. Publications Committee. Society for Maternal-Fetal Medicine Consult Series #60: management of pregnancies resulting from in vitro fertilization. Am J Obstet Gynecol. (2022) 226:B2–B12. doi: 10.1016/j.ajog.2021.11.001,
17. Johnson, KM, Hacker, MR, Resetkova, N, O’Brien, B, and Modest, AM. Risk of ischemic placental disease in fresh and frozen embryo transfer cycles. Fertil Steril. (2019) 111:714–21. doi: 10.1016/j.fertnstert.2018.11.043
18. Bosdou, JK, Anagnostis, P, Goulis, DG, Lainas, GT, Tarlatzis, BC, and Grimbizis, GF. Risk of gestational diabetes mellitus in women achieving singleton pregnancy spontaneously or after ART: a systematic review and meta-analysis. Hum Reprod Update. (2020) 26:514–44. doi: 10.1093/humupd/dmaa011
19. Matsuzaki, S, Nagase, Y, Takiuchi, T, Kakigano, A, Mimura, K, and Lee, M. Antenatal diagnosis of placenta accreta spectrum after in vitro fertilization-embryo transfer: a systematic review and meta-analysis. Sci Rep. (2021) 11:9205. doi: 10.1038/s41598-021-88551-7
20. Singh, B, Reschke, L, Segars, J, and Baker, VL. Frozen-thawed embryo transfer: the potential importance of the corpus luteum in preventing obstetrical complications. Fertil Steril. (2020) 113:252–7. doi: 10.1016/j.fertnstert.2019.12.007
21. Conrad, KP, von Versen-Höynck, F, and Baker, VL. Potential role of the corpus luteum in maternal cardiovascular adaptation to pregnancy and preeclampsia risk. Am J Obstet Gynecol. (2022) 226:683–99. doi: 10.1016/j.ajog.2021.08.018
22. Niu, Y, Suo, L, Zhao, D, Wang, Y, Miao, R, and Zou, J. Is artificial endometrial preparation more associated with early-onset or late-onset preeclampsia after frozen embryo transfer? J Assist Reprod Genet. (2023) 40:1045–54. doi: 10.1007/s10815-023-02785-0
23. Chambers, GM, Dyer, S, Zegers-Hochschild, F, de Mouzon, J, and Ishihara, O. International Committee for Monitoring Assisted Reproductive Technologies world report: assisted reproductive technology, 2014†. Hum Reprod. (2021) 36:2921–34. doi: 10.1093/humrep/deab198
24. Savasi, VM, Mandia, L, Laoreti, A, and Cetin, I. Maternal and fetal outcomes in oocyte donation pregnancies. Hum Reprod Update. (2016) 22:620–33. doi: 10.1093/humupd/dmw012
25. Moreno Sepulveda, J, and Checa, MA. Risk of adverse perinatal outcomes after oocyte donation: a systematic review and meta-analysis. J Assist Reprod Genet. (2019) 36:2017–37. doi: 10.1007/s10815-019-01552-4
26. Keukens, A, Van Wely, M, Van Der Meulen, C, and Mochtar, MH. Pre-eclampsia in pregnancies resulting from oocyte donation, natural conception or IVF: a systematic review and meta-analysis. Hum Reprod. (2022) 37:586–99. doi: 10.1093/humrep/deab267
27. Rizzo, G, Aiello, E, Pietrolucci, ME, and Arduini, D. Placental volume and uterine artery Doppler evaluation at 11 + 0 to 13 + 6 weeks’ gestation in pregnancies conceived with in-vitro fertilization: comparison between autologous and donor oocyte recipients: placental volume in IVF pregnancies. Ultrasound Obstet Gynecol. (2016) 47:726–31. doi: 10.1002/uog.14918
28. Inversetti, A, Mandia, L, Candiani, M, Cetin, I, Larcher, A, and Savasi, V. Uterine artery Doppler pulsatility index at 11–38 weeks in ICSI pregnancies with egg donation. J Perinat Med. (2018) 46:21–7. doi: 10.1515/jpm-2016-0180
29. Cavoretto, PI, Farina, A, Miglio, R, Zamagni, G, Girardelli, S, and Vanni, VS. Prospective longitudinal cohort study of uterine arteries Doppler in singleton pregnancies obtained by IVF/ICSI with oocyte donation or natural conception. Hum Reprod. (2020) 35:2428–38. doi: 10.1093/humrep/deaa235
30. Dancey, S, Mery, E, Esteves, A, Oltean, I, Hayawi, L, and Tang, K. Placenta pathology in recipient versus donor oocyte derivation for in vitro fertilization in a setting of hypertensive disorders of pregnancy and IUGR. Placenta. (2021) 108:114–21. doi: 10.1016/j.placenta.2021.03.012
31. Modest, AM, Johnson, KM, Karumanchi, SA, Resetkova, N, Young, BC, and Fox, MP. Risk of ischemic placental disease is increased following in vitro fertilization with oocyte donation: a retrospective cohort study. J Assist Reprod Genet. (2019) 36:1917–26. doi: 10.1007/s10815-019-01545-3
32. Johnson, KM, Hacker, MR, Thornton, K, Young, BC, and Modest, AM. Association between in vitro fertilization and ischemic placental disease by gestational age. Fertil Steril. (2020) 114:579–86. doi: 10.1016/j.fertnstert.2020.04.029
33. Modest, AM, Smith, LH, Toth, TL, Collier, A-RY, and Hacker, MR. Multifoetal gestations mediate the effect of in vitro fertilisation (IVF) on ischaemic placental disease in autologous oocyte IVF more than donor oocyte IVF. Paediatr Perinat Epidemiol. (2022) 36:181–9. doi: 10.1111/ppe.12857
34. Caradeux, J, Ávila, F, Vargas, F, Fernández, B, Winkler, C, and Mondión, M. Fetal growth velocity according to the mode of assisted conception. Fetal Diagn Ther. (2023) 50:299–308. doi: 10.1159/000531451
35. Messerlian, C, Maclagan, L, and Basso, O. Infertility and the risk of adverse pregnancy outcomes: a systematic review and meta-analysis. Hum Reprod. (2013) 28:125–37. doi: 10.1093/humrep/des347
36. Bastek, JA, Brown, AG, Anton, L, Srinivas, SK, and D’addio, A. Biomarkers of inflammation and placental dysfunction are associated with subsequent preterm birth. J Matern Fetal Neonatal Med. (2011) 24:600–5. doi: 10.3109/14767058.2010.511340
37. Burton, GJ, and Jauniaux, E. Pathophysiology of placental-derived fetal growth restriction. Am J Obstet Gynecol. (2018) 218:S745–61. doi: 10.1016/j.ajog.2017.11.577
38. Morgan, TK. Role of the placenta in preterm birth: a review. Am J Perinatol. (2016) 33:258–66. doi: 10.1055/s-0035-1570379
39. Jung, E, Romero, R, Yeo, L, Gomez-Lopez, N, Chaemsaithong, P, and Jaovisidha, A. The etiology of preeclampsia. Am J Obstet Gynecol. (2022) 226:S844–66. doi: 10.1016/j.ajog.2021.11.1356
40. Fertility treatment: preliminary trends and figures | HFEA. (2021), Available at:https://www.hfea.gov.uk/about-us/publications/research-and-data/fertility-treatment-2021-preliminary-trends-and-figures/ (Accessed October 17, 2023)
41. Seshadri, S, Morris, G, Serhal, P, and Saab, W. Assisted conception in women of advanced maternal age. Best Pract Res Clin Obstet Gynaecol. (2021) 70:10–20. doi: 10.1016/j.bpobgyn.2020.06.012
42. Wang, YA, Farquhar, C, and Sullivan, EA. Donor age is a major determinant of success of oocyte donation/recipient programme. Hum Reprod. (2012) 27:118–25. doi: 10.1093/humrep/der359
43. Hogan, RG, Wang, AY, Li, Z, Hammarberg, K, Johnson, L, and Mol, BW. Oocyte donor age has a significant impact on oocyte recipients’ cumulative live-birth rate: a population-based cohort study. Fertil Steril. (2019) 112:724–30. doi: 10.1016/j.fertnstert.2019.05.012
44. Soares, SR, Troncoso, C, Bosch, E, Serra, V, Simón, C, and Remohí, J. Age and uterine receptiveness: predicting the outcome of oocyte donation cycles. J Clin Endocrinol Metab. (2005) 90:4399–404. doi: 10.1210/jc.2004-2252
45. Li, J, Li, Y, Duan, Y, Xiao, X, Luo, J, and Luo, M. Dose-response associations of maternal age with pregnancy complications and multimorbidity among nulliparas and multiparas: a multicentric retrospective cohort study in southern China. J Glob Health. (2023) 13:4117. doi: 10.7189/jogh.13.04117
46. Lean, SC, Derricott, H, Jones, RL, and Heazell, AEP. Advanced maternal age and adverse pregnancy outcomes: a systematic review and meta-analysis. PLoS One. (2017) 12:e0186287. doi: 10.1371/journal.pone.0186287
47. Sheen, J-J, Wright, JD, Goffman, D, Kern-Goldberger, AR, Booker, W, and Siddiq, Z. Maternal age and risk for adverse outcomes. Am J Obstet Gynecol. (2018) 219:390.e1–390.e15. doi: 10.1016/j.ajog.2018.08.034
48. Pathare, ADS, Loid, M, Saare, M, Gidlöf, SB, Zamani Esteki, M, and Acharya, G. Endometrial receptivity in women of advanced age: an underrated factor in infertility. Hum Reprod. (2023) 29:773–93. doi: 10.1093/humupd/dmad019
49. Neykova, K, Tosto, V, Giardina, I, Tsibizova, V, and Vakrilov, G. Endometrial receptivity and pregnancy outcome. J Matern Fetal Neonatal Med. (2022) 35:2591–605. doi: 10.1080/14767058.2020.1787977
50. Ganer Herman, H, Volodarsky-Perel, A, Ton Nu, TN, Machado-Gedeon, A, Cui, Y, and Shaul, J. Diminished ovarian reserve is a risk factor for preeclampsia and placental malperfusion lesions. Fertil Steril. (2023) 119:794–801. doi: 10.1016/j.fertnstert.2023.01.029
51. Woldringh, GH, Frunt, MHA, and Kremer, J. Decreased ovarian reserve relates to pre-eclampsia in IVF/ICSI pregnancies. Hum Reprod. (2006) 21:2948–54. doi: 10.1093/humrep/del155
52. Grossmann, B, Saur, S, Rall, K, Pecher, A-C, Hübner, S, and Henes, J. Prevalence of autoimmune disease in women with premature ovarian failure. Eur J Contracept Reprod Health Care. (2020) 25:72–5. doi: 10.1080/13625187.2019.1702638
53. Deroux, A, Dumestre-Perard, C, Dunand-Faure, C, Bouillet, L, and Hoffmann, P. Female infertility and serum auto-antibodies: a systematic review. Clin Rev Allergy Immunol. (2017) 53:78–86. doi: 10.1007/s12016-016-8586-z
54. Del Porto, F, Ferrero, S, Cifani, N, Sesti, G, and Proietta, M. Antiphospholipid antibodies and idiopathic infertility. Lupus. (2022) 31:347–53. doi: 10.1177/09612033221076735
55. Society for Maternal-Fetal Medicine (SMFM)Silver, R, Craigo, S, Porter, F, Osmundson, SS, Kuller, JA, et al. Society for maternal-fetal medicine consult series #64: systemic lupus erythematosus in pregnancy. Am J Obstet Gynecol. (2023) 228:B41–60. doi: 10.1016/j.ajog.2022.09.001,
56. Sammaritano, LR. Antiphospholipid syndrome. Best Pract Res Clin Rheumatol. (2020) 34:101463. doi: 10.1016/j.berh.2019.101463
57. Drummond, K, Danesh, NM, Arseneault, S, Rodrigues, J, Tulandi, T, and Raina, J. Association between endometriosis and risk of preeclampsia in women who conceived spontaneously: a systematic review and meta-analysis. J Minim Invasive Gynecol. (2023) 30:91–9. doi: 10.1016/j.jmig.2022.11.008
58. Farland, LV, Prescott, J, Sasamoto, N, Tobias, DK, Gaskins, AJ, and Stuart, JJ. Endometriosis and risk of adverse pregnancy outcomes. Obstet Gynecol. (2019) 134:527–36. doi: 10.1097/AOG.0000000000003410
59. Vercellini, P, Viganò, P, Bandini, V, Buggio, L, Berlanda, N, and Somigliana, E. Association of endometriosis and adenomyosis with pregnancy and infertility. Fertil Steril. (2023) 119:727–40. doi: 10.1016/j.fertnstert.2023.03.018
60. Rabaglino, MB, and Conrad, KP. Evidence for shared molecular pathways of dysregulated decidualization in preeclampsia and endometrial disorders revealed by microarray data integration. FASEB J. (2019) 33:11682–95. doi: 10.1096/fj.201900662R
61. Conrad, KP, Rabaglino, MB, and Post Uiterweer, ED. Emerging role for dysregulated decidualization in the genesis of preeclampsia. Placenta. (2017) 60:119–29. doi: 10.1016/j.placenta.2017.06.005
62. Pan, H, Xian, P, Yang, D, Zhang, C, Tang, H, and He, X. Polycystic ovary syndrome is an independent risk factor for hypertensive disorders of pregnancy: a systematic review, meta-analysis, and meta-regression. Endocrine. (2021) 74:518–29. doi: 10.1007/s12020-021-02886-9
63. Sha, T, Wang, X, Cheng, W, and Yan, Y. A meta-analysis of pregnancy-related outcomes and complications in women with polycystic ovary syndrome undergoing IVF. Reprod Biomed Online. (2019) 39:281–93. doi: 10.1016/j.rbmo.2019.03.203
64. Roos, N, Kieler, H, Sahlin, L, Ekman-Ordeberg, G, and Falconer, H. Risk of adverse pregnancy outcomes in women with polycystic ovary syndrome: population based cohort study. BMJ. (2011) 343:d6309. doi: 10.1136/bmj.d6309
65. Hochberg, A, Mills, G, Volodarsky-Perel, A, Nu, TNT, Machado-Gedeon, A, and Cui, Y. The impact of polycystic ovary syndrome on placental histopathology patterns in in-vitro fertilization singleton live births. Placenta. (2023) 139:12–8. doi: 10.1016/j.placenta.2023.05.015
66. Schoots, MH, Bourgonje, MF, Bourgonje, AR, Prins, JR, van Hoorn, EGM, and Abdulle, AE. Oxidative stress biomarkers in fetal growth restriction with and without preeclampsia. Placenta. (2021) 115:87–96. doi: 10.1016/j.placenta.2021.09.013
67. Chiarello, DI, Abad, C, Rojas, D, Toledo, F, Vázquez, CM, and Mate, A. Oxidative stress: Normal pregnancy versus preeclampsia. Biochim Biophys Acta Mol basis Dis. (2020) 1866:165354. doi: 10.1016/j.bbadis.2018.12.005
68. Riesche, L, and Bartolomei, MS. Assisted reproductive technologies and the placenta: clinical, morphological, and molecular outcomes. Semin Reprod Med. (2018) 36:240–8. doi: 10.1055/s-0038-1676640
69. Chen, M, Wu, L, Zhao, J, Wu, F, Davies, MJ, and Wittert, GA. Altered glucose metabolism in mouse and humans conceived by IVF. Diabetes. (2014) 63:3189–98. doi: 10.2337/db14-0103
70. Vambergue, A, and Fajardy, I. Consequences of gestational and pregestational diabetes on placental function and birth weight. World J Diabetes. (2011) 2:196–203. doi: 10.4239/wjd.v2.i11.196
71. Roque, M, Haahr, T, Geber, S, Esteves, SC, and Humaidan, P. Fresh versus elective frozen embryo transfer in IVF/ICSI cycles: a systematic review and meta-analysis of reproductive outcomes. Hum Reprod. (2019) 25:2–14. doi: 10.1093/humupd/dmy033
72. Sha, T, Yin, X, Cheng, W, and Massey, IY. Pregnancy-related complications and perinatal outcomes resulting from transfer of cryopreserved versus fresh embryos in vitro fertilization: a meta-analysis. Fertil Steril. (2018) 109:330–342.e9. doi: 10.1016/j.fertnstert.2017.10.019
73. Sacha, CR, Harris, AL, James, K, Basnet, K, Freret, TS, and Yeh, J. Placental pathology in live births conceived with in vitro fertilization after fresh and frozen embryo transfer. Am J Obstet Gynecol. (2020) 222:360.e1–360.e16. doi: 10.1016/j.ajog.2019.09.047
74. Blazquez, A, García, D, Vassena, R, Figueras, F, and Rodriguez, A. Risk of pre-eclampsia after fresh or frozen embryo transfer in patients undergoing oocyte donation. Eur J Obstet Gynecol Reprod Biol. (2018) 227:27–31. doi: 10.1016/j.ejogrb.2018.05.030
75. Ginström Ernstad, E, Wennerholm, U-B, Khatibi, A, Petzold, M, and Bergh, C. Neonatal and maternal outcome after frozen embryo transfer: increased risks in programmed cycles. Am J Obstet Gynecol. (2019) 221:126.e1–126.e18. doi: 10.1016/j.ajog.2019.03.010
76. Guo, X, Yi, H, Li, TC, Wang, Y, Wang, H, and Chen, X. Role of vascular endothelial growth factor (VEGF) in human embryo implantation: clinical implications. Biomol Ther. (2021) 11:253. doi: 10.3390/biom11020253
77. Cottrell, HN, Deepak, V, Spencer, JB, Sidell, N, and Rajakumar, A. Effects of Supraphysiologic levels of estradiol on endometrial decidualization, sFlt1, and HOXA10 expression. Reprod Sci. (2019) 26:1626–32. doi: 10.1177/1933719119833485
78. Conrad, KP. Evidence for corpus luteal and endometrial origins of adverse pregnancy outcomes in women conceiving with or without assisted reproduction. Obstet Gynecol Clin N Am. (2020) 47:163–81. doi: 10.1016/j.ogc.2019.10.011
79. Marconi, N, Allen, CP, Bhattacharya, S, and Maheshwari, A. Obstetric and perinatal outcomes of singleton pregnancies after blastocyst-stage embryo transfer compared with those after cleavage-stage embryo transfer: a systematic review and cumulative meta-analysis. Hum Reprod. (2022) 28:255–81. doi: 10.1093/humupd/dmab042
80. Glujovsky, D, Quinteiro Retamar, AM, Alvarez Sedo, CR, Ciapponi, A, and Cornelisse, S. Cleavage-stage versus blastocyst-stage embryo transfer in assisted reproductive technology. Cochrane Database Syst Rev. (2022) 2022:CD002118. doi: 10.1002/14651858.CD002118.pub6
81. Siristatidis, C, Papapanou, M, Karageorgiou, V, Martins, WP, Bellos, I, and Teixeira, DM. Congenital anomaly and perinatal outcome following blastocyst-vs cleavage-stage embryo transfer: systematic review and network meta-analysis. Ultrasound Obstet Gynecol. (2023) 61:12–25. doi: 10.1002/uog.26019
82. Theobald, R, SenGupta, S, and Harper, J. The status of preimplantation genetic testing in the UK and USA. Hum Reprod. (2020) 35:986–98. doi: 10.1093/humrep/deaa034
83. Spinella, F, Bronet, F, Carvalho, F, Coonen, E, De Rycke, M, and Rubio, C. ESHRE PGT consortium data collection XXI: PGT analyses in 2018. Hum Reprod Open. (2023) 2023:hoad010. doi: 10.1093/hropen/hoad010
84. Mao, D, Xu, J, and Sun, L. Impact of trophectoderm biopsy for preimplantation genetic testing on obstetric and neonatal outcomes: a meta-analysis. Am J Obstet Gynecol. (2023) S0002-9378:544–6. doi: 10.1016/j.ajog.2023.08.010
85. Kokkali, G, Traeger-Synodinos, J, Vrettou, C, Stavrou, D, Jones, GM, and Cram, DS. Blastocyst biopsy versus cleavage stage biopsy and blastocyst transfer for preimplantation genetic diagnosis of beta-thalassaemia: a pilot study. Hum Reprod. (2007) 22:1443–9. doi: 10.1093/humrep/del506
86. Turco, MY, and Moffett, A. Development of the human placenta. Development. (2019) 146:dev163428. doi: 10.1242/dev.163428
87. Yao, Q, Chen, L, Liang, Y, Sui, L, Guo, L, and Zhou, J. Blastomere removal from cleavage-stage mouse embryos alters placental function, which is associated with placental oxidative stress and inflammation. Sci Rep. (2016) 6:25023. doi: 10.1038/srep25023
88. Sugawara, A, Sato, B, Bal, E, Collier, AC, and Ward, MA. Blastomere removal from cleavage-stage mouse embryos alters steroid metabolism during pregnancy. Biol Reprod. (2012) 87:1–9. doi: 10.1095/biolreprod.111.097444
89. Zhang, WY, von Versen-Höynck, F, Kapphahn, KI, Fleischmann, RR, Zhao, Q, and Baker, VL. Maternal and neonatal outcomes associated with trophectoderm biopsy. Fertil Steril. (2019) 112:283–290.e2. doi: 10.1016/j.fertnstert.2019.03.033
90. Zheng, W, Yang, SH, Yang, C, Ren, BN, Sun, SM, and Liu, YL. Perinatal outcomes of singleton live births after preimplantation genetic testing during single frozen-thawed blastocyst transfer cycles: a propensity score-matched study. Fertil Steril. (2022) 117:562–70. doi: 10.1016/j.fertnstert.2021.12.020
91. Hou, W, Shi, G, Ma, Y, Liu, Y, Lu, M, and Fan, X. Impact of preimplantation genetic testing on obstetric and neonatal outcomes: a systematic review and meta-analysis. Fertil Steril. (2021) 116:990–1000. doi: 10.1016/j.fertnstert.2021.06.040
92. Zheng, W, Yang, C, Yang, S, Sun, S, Mu, M, and Rao, M. Obstetric and neonatal outcomes of pregnancies resulting from preimplantation genetic testing: a systematic review and meta-analysis. Hum Reprod Update. (2021) 27:989–1012. doi: 10.1093/humupd/dmab027
93. Doyle, N, Gainty, M, Eubanks, A, Doyle, J, Hayes, H, and Tucker, M. Donor oocyte recipients do not benefit from preimplantation genetic testing for aneuploidy to improve pregnancy outcomes. Hum Reprod. (2020) 35:2548–55. doi: 10.1093/humrep/deaa219
94. Martello, CL, Kulmann, MIR, Donatti, LM, Bos-Mikich, A, and Frantz, N. Preimplantation genetic testing for aneuploidies does not increase success rates in fresh oocyte donation cycles: a paired cohort study. J Assist Reprod Genet. (2021) 38:2909–14. doi: 10.1007/s10815-021-02339-2
95. Roeca, C, Johnson, R, Carlson, N, and Polotsky, AJ. Preimplantation genetic testing and chances of a healthy live birth amongst recipients of fresh donor oocytes in the United States. J Assist Reprod Genet. (2020) 37:2283–92. doi: 10.1007/s10815-020-01874-8
96. Peyser, A, Brownridge, S, Rausch, M, and Noyes, N. The evolving landscape of donor egg treatment: success, women’s choice, and anonymity. J Assist Reprod Genet. (2021) 38:2327–32. doi: 10.1007/s10815-021-02262-6
97. Saito, S, Nakabayashi, Y, Nakashima, A, Shima, T, and Yoshino, O. A new era in reproductive medicine: consequences of third-party oocyte donation for maternal and fetal health. Semin Immunopathol. (2016) 38:687–97. doi: 10.1007/s00281-016-0577-x
98. Krop, J, Tian, X, van der Hoorn, M-L, and Eikmans, M. The mac is back: the role of macrophages in human healthy and complicated pregnancies. Int J Mol Sci. (2023) 24:5300. doi: 10.3390/ijms24065300
99. Scherjon, S, Lashley, L, van der Hoorn, M-L, and Claas, F. Fetus specific T cell modulation during fertilization, implantation and pregnancy. Placenta. (2011) 32:S291–7. doi: 10.1016/j.placenta.2011.03.014
100. Yagel, S, Cohen, SM, and Goldman-Wohl, D. An integrated model of preeclampsia: a multifaceted syndrome of the maternal cardiovascular-placental-fetal array. Am J Obstet Gynecol. (2022) 226:S963–72. doi: 10.1016/j.ajog.2020.10.023
101. Nakabayashi, Y, Nakashima, A, Yoshino, O, Shima, T, Shiozaki, A, and Adachi, T. Impairment of the accumulation of decidual T cells, NK cells, and monocytes, and the poor vascular remodeling of spiral arteries, were observed in oocyte donation cases, regardless of the presence or absence of preeclampsia. J Reprod Immunol. (2016) 114:65–74. doi: 10.1016/j.jri.2015.07.005
102. Tilburgs, T, Scherjon, SA, van der Mast, BJ, Haasnoot, GW, and Voort-Maarschalk, V-VD. Fetal-maternal HLA-C mismatch is associated with decidual T cell activation and induction of functional T regulatory cells. J Reprod Immunol. (2009) 82:148–57. doi: 10.1016/j.jri.2009.05.003
103. Chernyshov, VP, Tumanova, LE, Sudoma, IA, and Bannikov, VI. Th1 and Th2 in human IVF pregnancy with allogenic fetus. Am J Reprod Immunol. (2008) 59:352–8. doi: 10.1111/j.1600-0897.2007.00578.x
104. Tian, X, Goemaere, NNT, van der Meeren, L, Yang, J, Kapsenberg, JM, and Lashley, LEELO. Inflammatory placental lesions are specifically observed in healthy oocyte donation pregnancies with extreme fetal-maternal incompatibility. Placenta. (2023) 143:100–9. doi: 10.1016/j.placenta.2023.10.005
105. Bürk, MR, Troeger, C, Brinkhaus, R, Holzgreve, W, and Hahn, S. Severely reduced presence of tissue macrophages in the basal plate of pre-eclamptic placentae. Placenta. (2001) 22:309–16. doi: 10.1053/plac.2001.0624
106. van der Hoorn, M-LP, van Egmond, A, Swings, GMJS, van Beelen, E, van der Keur, C, and Tirado-González, I. Differential immunoregulation in successful oocyte donation pregnancies compared with naturally conceived pregnancies. J Reprod Immunol. (2014) 101–102:96–103. doi: 10.1016/j.jri.2013.08.002
107. van Bentem, K, Bos, M, van der Keur, C, Brand-Schaaf, SH, Haasnoot, GW, and Roelen, DL. The development of preeclampsia in oocyte donation pregnancies is related to the number of fetal-maternal HLA class II mismatches. J Reprod Immunol. (2020) 137:103074. doi: 10.1016/j.jri.2019.103074
108. Lashley, L, Haasnoot, GW, Spruyt-Gerritse, M, and Claas, FHJ. Selective advantage of HLA matching in successful uncomplicated oocyte donation pregnancies. J Reprod Immunol. (2015) 112:29–33. doi: 10.1016/j.jri.2015.05.006
109. Blazquez, A, García, D, Vassena, R, Figueras, F, and Rodriguez, A. Risk of preeclampsia in pregnancies resulting from double gamete donation and from oocyte donation alone. Pregnancy Hypertens. (2018) 13:133–7. doi: 10.1016/j.preghy.2018.06.010
110. Bos, M, Baelde, HJ, Bruijn, JA, Bloemenkamp, KWM, van der Hoorn, M-LP, and Turner, RJ. Loss of placental thrombomodulin in oocyte donation pregnancies. Fertil Steril. (2017) 107:119–129.e5. doi: 10.1016/j.fertnstert.2016.10.005
111. Lashley, L, Buurma, A, Swings, GMJS, Eikmans, M, Anholts, JDH, and Bakker, JA. Preeclampsia in autologous and oocyte donation pregnancy: is there a different pathophysiology? J Reprod Immunol. (2015) 109:17–23. doi: 10.1016/j.jri.2015.03.004
112. van Hof, LJ, Dijkstra, KL, van der Keur, C, Eikmans, M, Baelde, HJ, and Bos, M. Decreased expression of ligands of placental immune checkpoint inhibitors in uncomplicated and preeclamptic oocyte donation pregnancies. J Reprod Immunol. (2020) 142:103194. doi: 10.1016/j.jri.2020.103194
113. Gundogan, F, Bianchi, DW, Scherjon, SA, and Roberts, DJ. Placental pathology in egg donor pregnancies. Fertil Steril. (2010) 93:397–404. doi: 10.1016/j.fertnstert.2008.12.144
114. Schonkeren, D, Swings, G, Roberts, D, Claas, F, de Heer, E, and Scherjon, S. Pregnancy close to the edge: an immunosuppressive infiltrate in the chorionic plate of placentas from uncomplicated egg cell donation. PLoS One. (2012) 7:e32347. doi: 10.1371/journal.pone.0032347
115. Hirst, JE, Villar, J, Victora, CG, Papageorghiou, AT, Finkton, D, and Barros, FC. The antepartum stillbirth syndrome: risk factors and pregnancy conditions identified from the INTERGROWTH-21st project. BJOG. (2018) 125:1145–53. doi: 10.1111/1471-0528.14463
116. McDade, TW, Ryan, CP, Jones, MJ, Hoke, MK, Borja, J, and Miller, GE. Genome-wide analysis of DNA methylation in relation to socioeconomic status during development and early adulthood. Am J Phys Anthropol. (2019) 169:3–11. doi: 10.1002/ajpa.23800
117. Murugappan, G, Li, S, Lathi, RB, Baker, VL, Luke, B, and Eisenberg, ML. Increased risk of severe maternal morbidity among infertile women: analysis of US claims data. Am J Obstet Gynecol. (2020) 223:404.e1–404.e20. doi: 10.1016/j.ajog.2020.02.027
118. Murugappan, G, Li, S, Alvero, RJ, Luke, B, and Eisenberg, ML. Association between infertility and all-cause mortality: analysis of US claims data. Am J Obstet Gynecol. (2021) 225:57.e1–57.e11. doi: 10.1016/j.ajog.2021.02.010
119. Masturzo, B, Di Martino, D, Prefumo, F, Cavoretto, P, Germano, C, and Gennarelli, G. Higher rate of early-onset preeclampsia in pregnancies following oocyte donation according to increasing maternal age. Arch Gynecol Obstet. (2019) 300:861–7. doi: 10.1007/s00404-019-05291-w
120. Ervaala, A, Laivuori, H, Gissler, M, Kere, J, Kivinen, K, and Pouta, A. Characteristics of preeclampsia in donor cell gestations. Pregnancy Hypertens. (2022) 27:59–61. doi: 10.1016/j.preghy.2021.12.005
121. Dai, F, Lan, Y, Pan, S, Wang, Y, Hua, Y, and Xiao, W. Pregnancy outcomes and disease phenotype of hypertensive disorders of pregnancy in singleton pregnancies after in vitro fertilization: a retrospective analysis of 1130 cases. BMC Pregnancy Childbirth. (2023) 23:523. doi: 10.1186/s12884-023-05838-5
122. RCOG. The investigation and management of the small-for-gestational-age fetus. Green-top Guideline 31 (2013), Available at:https://www.rcog.org.uk/globalassets/documents/guidelines/gtg_31.pdf
123. Martinez-Portilla, RJ, Caradeux, J, Meler, E, Lip-Sosa, DL, Sotiriadis, A, and Figueras, F. Third-trimester uterine artery Doppler for prediction of adverse outcome in late small-for-gestational-age fetuses: systematic review and meta-analysis. Ultrasound Obstet Gynecol. (2020) 55:575–85. doi: 10.1002/uog.21940
124. Conde-Agudelo, A, Villar, J, Kennedy, SH, and Papageorghiou, AT. Predictive accuracy of cerebroplacental ratio for adverse perinatal and neurodevelopmental outcomes in suspected fetal growth restriction: systematic review and meta-analysis. Ultrasound Obstet Gynecol. (2018) 52:430–41. doi: 10.1002/uog.19117
125. Llurba, E, Turan, O, Kasdaglis, T, Harman, CR, and Baschat, AA. Emergence of late-onset placental dysfunction: relationship to the change in uterine artery blood flow resistance between the first and third trimesters. Am J Perinatol. (2013) 30:505–12. doi: 10.1055/s-0032-1329181
126. Binder, J, Monaghan, C, Thilaganathan, B, Carta, S, and Khalil, A. De-novo abnormal Uteroplacental circulation in the third trimester: pregnancy outcome and pathological implications. Ultrasound Obstetr Gynecol. (2017) 52:60–5. doi: 10.1002/uog.17564
127. Pimentel, C, Solene, D, Frédérique, J, Guillaume, B, Jean, L, and Maëla, LL. What are the predictive factors for preeclampsia in oocyte recipients? J Hum Reprod Sci. (2019) 12:327–33. doi: 10.4103/jhrs.JHRS_43_19
128. Behnam Sani, K, and Sawitzki, B. Immune monitoring as prerequisite for transplantation tolerance trials. Clin Exp Immunol. (2017) 189:158–70. doi: 10.1111/cei.12988
129. Mangum, DS, and Caywood, E. A clinician’s guide to HLA matching in allogeneic hematopoietic stem cell transplant. Hum Immunol. (2022) 83:687–94. doi: 10.1016/j.humimm.2022.03.002
130. Ye, S, Liu, Y, Zhao, X, Ma, Y, and Wang, Y. Hydroxychloroquine improves pregnancy outcomes of women with positive antinuclear antibody spectrum test results. Front Med. (2023) 10:1113127. doi: 10.3389/fmed.2023.1113127
131. Duan, J, Ma, D, Wen, X, Guo, Q, Gao, J, and Zhang, G. Hydroxychloroquine prophylaxis for preeclampsia, hypertension and prematurity in pregnant patients with systemic lupus erythematosus: a meta-analysis. Lupus. (2021) 30:1163–74. doi: 10.1177/09612033211007199
132. Tian, Y, Xu, J, Chen, D, Yang, C, and Peng, B. The additional use of hydroxychloroquine can improve the live birth rate in pregnant women with persistent positive antiphospholipid antibodies: a systematic review and meta-analysis. J Gynecol Obstet Hum Reprod. (2021) 50:102121. doi: 10.1016/j.jogoh.2021.102121
133. Gao, R, Deng, W, Meng, C, Cheng, K, Zeng, X, and Qin, L. Combined treatment of prednisone and hydroxychloroquine may improve outcomes of frozen embryo transfer in antinuclear antibody-positive patients undergoing IVF/ICSI treatment. Lupus. (2021) 30:2213–20. doi: 10.1177/09612033211055816
134. Ghasemnejad-Berenji, H, Ghaffari Novin, M, Hajshafiha, M, Nazarian, H, Hashemi, SM, and Ilkhanizadeh, B. Immunomodulatory effects of hydroxychloroquine on Th1/Th2 balance in women with repeated implantation failure. Biomed Pharmacother. (2018) 107:1277–85. doi: 10.1016/j.biopha.2018.08.027
135. Andreescu, M. The impact of the use of immunosuppressive treatment after an embryo transfer in increasing the rate of live birth. Front Med. (2023) 10:67876. doi: 10.3389/fmed.2023.1167876
136. Mirzaei, M, Amirajam, S, Moghimi, ES, Behzadi, S, Rohani, A, and Zerangian, N. The effects of hydroxychloroquine on pregnancy outcomes in infertile women: a systematic review and meta-analysis. J Med Life. (2023) 16:189–94. doi: 10.25122/jml-2022-0095
137. Schutte, JM, Schuitemaker, NWE, Steegers, EAP, and van Roosmalen, J. Maternal death after oocyte donation at high maternal age: case report. Reprod Health. (2008) 5:12. doi: 10.1186/1742-4755-5-12
138. Korb, D, Schmitz, T, Seco, A, Le Ray, C, Santulli, P, and Goffinet, F. Increased risk of severe maternal morbidity in women with twin pregnancies resulting from oocyte donation. Hum Reprod. (2020) 35:1922–32. doi: 10.1093/humrep/deaa108
139. Garcia Castro, J, Rodríguez-Pardo, J, and Díaz de Terán, J. Eclampsia-induced posterior reversible encephalopathy syndrome in a donor oocyte recipient. J Family Reprod Health. (2020) 14:269–72. doi: 10.18502/jfrh.v14i4.5211
140. Sadeghi, MR. Do we have the right to challenge the rules of nature using science and technology tools? J Reprod Infertil. (2019) 20:199–200.
Keywords: in-vitro, infertility, preeclampsia, perinatal outcome, immune tolerance
Citation: Caradeux J, Fernández B, Ávila F, Valenzuela A, Mondión M and Figueras F (2024) Pregnancies through oocyte donation. A mini review of pathways involved in placental dysfunction. Front. Med. 11:1338516. doi: 10.3389/fmed.2024.1338516
Edited by:
Simcha Yagel, Hadassah Medical Center, IsraelReviewed by:
Raigam Jafet Martinez-Portilla, Instituto Nacional de Perinatología (INPER), MexicoCopyright © 2024 Caradeux, Fernández, Ávila, Valenzuela, Mondión and Figueras. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Javier Caradeux, javier.caradeux@clinicasantamaria.cl
†ORCID: Javier Caradeux, https://orcid.org/0000-0002-9504-4596
Francesc Figueras, https://orcid.org/0000-0003-4403-1274