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In Vitro Maturation: a Committee Opinion

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In Vitro Maturation: a Committee Opinion ASRM PAGES In vitro maturation: a committee opinion Practice Committees of the American Society for Reproductive Medicine, the Society of Reproductive Biologists and Technologists, and the Society for Assisted Reproductive Technology American Society for Reproductive Medicine, Birmingham, Alabama The results of in vitro maturation (IVM) investigations suggest the potential for wider clinical application. This document discusses the efficacy of IVM as reported in the published literature to date. This document replaces the document of the same name, last published in 2013. (Fertil SterilÒ 2021;115:298-304. Ó2020 by American Society for Reproductive Medicine.) El resumen está disponible en Español al final del artículo. Discuss: You can discuss this article with its authors and other readers at https://www.fertstertdialog.com/posts/31765 n vitro fertilization (IVF) typically Table 1 provides some definitions of (3). Cytoplasmic maturation refers to involves ovarian stimulation with IVM currently in use. an accumulation of factors that prepare I the use of exogenous gonadotro- The human oocyte reaches its full the cytoplasm for fertilization and em- pins to induce the maturation of size (100–120 mm in diameter) at the bryonic development (17, 18). Epige- gonadotropin-sensitive follicles and small antral stage, during which time netic processes are a component of inhibit the atresia of nondominant fol- the follicular diameter is only a fraction nuclear and cytoplasmic oocyte matu- licles (1, 2). The classic use of the term of its final ovulatory diameter. ration, influencing development after in vitro maturation (IVM) refers to the The ability of an oocyte to resume and fertilization (19, 20). For this reason, maturation of immature cumulus- complete meiosis is closely linked the potential for epigenetic disruption, oocyte complexes (COCs) in culture to follicular diameter (12–15). In such as abnormal methylation of from prophase I (i.e., from the humans, the kinetics of oocyte maternally expressed genes, warrants germinal vesicle [GV] stage) through maturation have been studied with careful evaluation in oocytes matured meiosis I to reach metaphase II (MII) the use of oocytes obtained from in vitro (21). after their recovery from follicles that oophorectomy specimens from non- have not been exposed to the preovu- malignant gynecologic disorders and POTENTIAL APPLICATIONS latory trigger (3). This was defined then cultured to undergo IVM, OF IVM largely in nonhuman animal studies. reaching MII after 36–48 hours (3). The clinical application of IVM may be In clinical human IVF, however, the It should be noted that even if an limited by alternative evidence-based term IVM is often used to refer to immature oocyte progresses to the MII strategies to successfully mitigate the in vitro maturation of oocytes stage with the use of IVM (i.e., com- risk of ovarian hyperstimulation syn- retrieved at the GV or metaphase I pletes nuclear maturation), it may not drome (OHSS) in high-risk populations. (MI) stage from follicles after exposure necessarily have undergone cyto- Historically, candidates for IVM have to exogenous FSH and/or hCG (‘‘folli- plasmic maturation and achieved full included those at risk for OHSS, cle priming’’) to increase the likelihood developmental competence. For a including women with polycystic ovary of obtaining some mature oocytes mature oocyte to undergo successful syndrome (PCOS) or polycystic ovary (4, 5). Interpretation of studies re- fertilization and subsequent develop- (PCO)–like ovaries and women with ported in the literature could be ment, synchronization of nuclear and estrogen-sensitive cancers. Because clarified if specific terminology was cytoplasmic maturation must occur significantly less medication is used used to delineate between IVM with (16). Nuclear maturation consists of for stimulation with the use of IVM, and without short gonadotropin GV breakdown induced by the LH surge and the stimulation is of shorter dura- stimulation, and with and without followed by resumption of meiosis and tion requiring fewer injections and hCG exposure before retrieval (6, 7). extrusion of the first polar body (MII) less monitoring, the financial and emotional burden is reduced compared Received November 3, 2020; accepted November 9, 2020; published online December 24, 2020. with traditional IVF cycles. In addition, Reprint requests: Practice Committee, American Society for Reproductive Medicine, 1209 Montgom- ery Highway, Birmingham, Alabama 35216-2809 (E-mail: [email protected]). patients with limited time before poten- tially gonadotoxic cancer treatments Fertility and Sterility® Vol. 115, No. 2, February 2021 0015-0282/$36.00 Copyright ©2020 American Society for Reproductive Medicine, Published by Elsevier Inc. may be candidates to use IVM for https://doi.org/10.1016/j.fertnstert.2020.11.018 fertility preservation (22, 23). Finally, 298 VOL. 115 NO. 2 / FEBRUARY 2021 Fertility and Sterility® TABLE 1 Definitions of IVM. Term in literature Oocyte maturation Exposure to hormones Reference Biological definition of IVM GV to MII No exposure to hCG or LH Edwards 1965 (3) Variations on definition of IVM Truncated IVF without FSH GV or MI to MII hCG primes intermediate Chian 1999 (8) follicles, no FSH Follicle priming with FSH GV or MI to MII Minimal FSH stimulation, no Wynn 1998 (9) HCG Mild-stimulation IVF/ GV or MI to MII Minimal FSH stimulation and Fadini 2009 (10) truncated IVF early hCG administration to prime intermediate follicles Rescue IVM Any immature oocytes at Controlled ovarian Sacha 2018 (11) retrieval to MII hyperstimulation cycle resulting in GV or MI oocytes denuded of cumulus cells Note: GV ¼ germinal vesicle; IVF ¼ in vitro fertilization; IVM ¼ in vitro maturation; MI ¼ metaphase I; MII ¼ metaphase II. ASRM. IVM: committee opinion. Fertil Steril 2020. a study has shown the effectiveness of IVM in patients with oocytes was improved, although 20% of recovered oocytes repeated assisted reproduction failure due to resistant ovary were matured in vivo in this treatment group. Clinical preg- syndrome (24). nancy rates after fresh embryo transfer were highest when both FSH and hCG were used, 26.5%, compared with 11.8%, 5.4%, and 13.7% in the nonprimed, hCG-primed, and FSH- IVM IN CLINICAL PRACTICE primed groups, respectively (10). However, embryos in this Follicular Priming group likely arose from a combination of both in vivo and There have been several clinical studies comparing IVM with in vitro matured oocytes, complicating interpretation of these conventional IVF using in vitro matured human oocytes in results. PCO-like and PCOS patients (25–29) and in ovulatory In several studies from Belgium in which IVM was con- women (26, 30, 31). Several trials have also evaluated the ducted after a short (3-day) FSH stimulation with no hCG, utility of follicular priming versus the retrieval of oocytes clinical pregnancy rates have been reported. In a small study from unstimulated antral follicles (10, 25). Three methods of of 39 PCO/PCOS patients and 73 IVM cycles, after vitrified- follicular priming have been reported. One method is to warmed embryo transfer, the ongoing clinical pregnancy minimally stimulate ovaries with low doses of FSH for 3–6 rate per transfer was 7/22 (31.8%) (33). A larger study of days, followed by retrieval on cycle day 7–10 in the absence 121 patients and 239 IVM cycles in which 3 days of FSH of hCG administration. Other approaches use only hCG and no hCG was administered and oocytes were retrieved (single 10,000 IU injection) to ‘‘prime’’ intermediate-sized fol- from follicles no larger than 6 mm, an ongoing clinical preg- licles 36 hours before oocyte retrieval, as well as the addition nancy rate of 9/24 (37.5%) after vitrified-warmed embryo of minimal FSH stimulation before this hCG priming. This transfer was reported (34). Pregnancy rate after fresh embryo form of priming with hCG is physiologically different than transfer was significantly lower in both of these studies. late follicular administration of hCG in a traditional IVF cycle. Subsequently, a ‘‘freeze-all’’ IVM strategy was used in a Priming with FSH and a single priming injection of hCG study of 79 PCOS patients, resulting in a cumulative live birth on cycle day 6, followed by IVM, in 921 PCOS women resulted rate per patient of 17/78 (21.8%) (35). Further supporting the in a cumulative live birth rate per cycle of 33.7% (32). A retro- notion that freeze-all strategies are better for FSH priming of spective cohort study comparing IVM with the use of FSH and IVM cycles, a recent study showed a very high miscarriage an hCG priming injection versus conventional IVF in 919 rate after IVM when fresh transfers were compared with women with high antral follicle count (AFC) reported that frozen-thawed embryo transfers (36.8% vs. 4.5%) (28). One although the number of mature oocytes and good-quality em- thing to bear in mind with all of these studies is that there bryos was lower in the IVM group, the cumulative live birth is a high level of attrition from retrieved immature COCs to rate after one cycle of IVM was 239/608 (39.3%) versus good-quality blastocysts, owing in part to low maturation 155/311 (49.8%) for IVF (29). success after IVM. The chance of a single immature oocyte re- The combination of gonadotropin and hCG priming sulting in a live birth was only 1.1% (35). In addition, inter- compared with single-agent follicular priming has been stud- pretation of these studies is complicated not only by ied with disparate results. A large randomized trial in 400 significant variation in the stimulation protocols used, but women with normal ovaries showed that when both FSH also by inconsistent reporting of the stage of meiotic matura- and hCG were used for priming, the percentage of oocytes tion of the oocytes at retrieval (GV vs. MI, as well as any that matured in vitro and the total number of available mature mature MII oocytes recovered).
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