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Age-Dependent in Vitro Maturation Efficacy of Human Oocytes

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Age-Dependent in Vitro Maturation Efficacy of Human Oocytes fcell-09-667682 June 15, 2021 Time: 15:47 # 1 ORIGINAL RESEARCH published: 18 June 2021 doi: 10.3389/fcell.2021.667682 Age-Dependent in vitro Maturation Efficacy of Human Oocytes – Is There an Optimal Age? Gilad Karavani1†, Peera Wasserzug-Pash2†, Talya Mordechai-Daniel1, Dvora Bauman1, Michael Klutstein2‡ and Tal Imbar1*‡ 1 Fertility Preservation Service, Department of Obstetrics and Gynecology, Hadassah Ein Kerem Medical Center and Faculty of Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel, 2 Institute of Biomedical and Oral Research, Faculty of Dental Medicine, The Hebrew University of Jerusalem, Jerusalem, Israel In vitro maturation of oocytes from antral follicles seen during tissue harvesting is a fertility Edited by: preservation technique with potential advantages over ovarian tissue cryopreservation Eleonora Napoli, University of California, Davis, (OTC), as mature frozen and later thawed oocyte used for fertilization poses decreased United States risk of malignant cells re-seeding, as compared to ovarian tissue implantation. We Reviewed by: previously demonstrated that in vitro maturation (IVM) performed following OTC in Raquel L. Bernardino, University of Porto, Portugal fertility preservation patients, even in pre-menarche girls, yields a fair amount of oocytes Volker Doetsch, available for IVM and freezing for future use. We conducted a retrospective cohort Goethe Business School, Germany study, evaluating IVM outcomes in chemotherapy naïve patients referred for fertility *Correspondence: preservation by OTC that had oocyte collected from the medium with attempted IVM. Tal Imbar [email protected] A total of 133 chemotherapy naïve patients aged 1–35 years were included in the study. †These authors share first authorship The primary outcome was IVM rate in the different age groups – pre-menarche (1–5 ‡These authors share last authorship and ≥6 years), post-menarche (menarche-17 years), young adults (18–24 years) and adults (25–29 and 30–35 years). We demonstrate a gradual increase in mean IVM rate Specialty section: in the age groups from 1 to 25 years [4.6% (1–5 years), 23.8% (6 years to menarche), This article was submitted to Cellular Biochemistry, and 28.4% (menarche to 17 years)], with a peak of 38.3% in the 18–24 years group, a section of the journal followed by a decrease in the 25–29 years group (19.3%), down to a very low IVM rate Frontiers in Cell and Developmental Biology (8.9%) in the 30–35 years group. A significant difference in IVM rates was noted between Received: 14 February 2021 the age extremes – the very young (1–5 years) and the oldest (30–35 years) groups, Accepted: 31 May 2021 as compared with the 18–24-year group (p < 0.001). Importantly, number of oocytes Published: 18 June 2021 matured, percent of patients with matured oocytes, and overall maturation rate differed Citation: significantly (p 0.001). Our finding of extremely low success rates in those very young Karavani G, Wasserzug-Pash P, < Mordechai-Daniel T, Bauman D, (under 6 years) and older (≥30 years) patients suggests that oocytes retrieved during Klutstein M and Imbar T (2021) OTC prior to chemotherapy have an optimal window of age that shows higher success Age-Dependent in vitro Maturation Efficacy of Human Oocytes – Is There rates, suggesting that oocytes may have an inherent tendency toward better maturation an Optimal Age? in those age groups. Front. Cell Dev. Biol. 9:667682. doi: 10.3389/fcell.2021.667682 Keywords: in vitro maturation, ovarian tissue cryopreservation, fertility preservation, women age, oocyte Frontiers in Cell and Developmental Biology| www.frontiersin.org 1 June 2021| Volume 9| Article 667682 fcell-09-667682 June 15, 2021 Time: 15:47 # 2 Karavani et al. IVM Rates Across the Age Groups INTRODUCTION in the study. While those chemotherapy and radiotherapy exposed patients, and patients for which oocytes were not Cryopreservation of ovarian cortical tissue followed by auto- found in the medium following OTC (and therefore IVM was transplantation has emerged as a promising fertility preservation not performed) were excluded. Counseling regarding fertility option (Feigin et al., 2007). Immature oocytes, usually in the preservation was done in a multidisciplinary consultation that germinal vesicle (GV) stage can be found during ovarian tissue included an oncologist, pediatric hematologist and reproductive handling (Revel et al., 2009; Gruhn et al., 2018) and the specialist, as well as a coordinating nurse and social worker. ability for maturation in vitro and cryopreservation as mature Female patients under 18 years of age were consulted with oocytes, provides an additional option for fertility preservation parental presence. After obtaining informed consent, patients (Chian et al., 2013). who decided to freeze ovarian tissue underwent partial/complete In vitro maturation (IVM) of oocytes from antral follicles seen laparoscopic oophorectomy. In our country, OTC is reimbursed during tissue harvesting is a fertility preservation technique with by the national health insurance and therefore does not require potential advantages over ovarian tissue cryopreservation (OTC). out of pocket coverage. The primary outcome were the overall Although not well established, IVM is believed to be feasible even and mean IVM rates in each age group. in the pediatric age group. A mature frozen and later thawed oocyte used for fertilization might serve as a safer option than re-implantation of ovarian cortex tissue, posing decreased risk Data Collection of malignant cells re-seeding. In our previously published work, Data was collected from patients’ electronic medical records we demonstrated that IVM performed following OTC in fertility and from the IVF laboratory database. Parameters retrieved preservation patients, even in pre-menarche girls, yields a fair included: demographic and clinical data; cancer diagnosis; age amount of oocytes available for IVM and freezing for future use. at diagnosis; treatment with chemotherapy and its timing with However, in the very young age group (under 6 years) there are regard to OTC; OTC procedure related information (partial or substantially decreased maturation rates, making this procedure complete oophorectomy) and IVF laboratory data – including invaluable in this age group (Karavani et al., 2019). OTC (number of ovarian tissue ampules cryopreserved); oocytes The human age-specific fertility rate follows an inverted u retrieval and the IVM process and outcomes with emphasis shape curve: beginning to rise with puberty (usually marked by given to the assessment of number of matured oocytes following the occurrence of menarche), reaching a peak around the age of IVM, overall and per patient IVM rate according to age 30 years, followed by a decline, beginning around the age of 35 groups and percent of patient with at least one matured toward significant low maturity and fertility rate in the early 40s oocyte following IVM. and later (Hawkes and Smith, 2010). A similar trend was observed for euploid oocyte rate across reproductive lifespan with a peak of euploid oocyte rate around the age of 25 (Gruhn et al., 2019). However, the rate of oocyte maturation capability as related to age Ovarian Tissue Cryopreservation has yet to be analyzed. Of important note is the fact that oocyte Procedure maturation capability is not necessarily linked to aneuploidy, and The OTC procedure done in our center includes the removal aneuploid oocytes can still mature. of the entire (complete oophorectomy) or most of the ovary As resources are limited and patients and their families (partial oophorectomy) in a laparoscopic procedure. The tissue are often required to fund the fertility preservation process, is then placed on ice in Leibovitz L-15 medium (GIBCO-BRL, it is of need to optimize and personalize consultation Paisley, United Kingdom) and transferred immediately to the regarding the success rate of IVM attempt in oocytes retrieved adjacent IVF laboratory for tissue examination and processing. during OTC, especially considering the fact that an ovarian In some cases, predominantly younger patients, insertion of a tissue with potential future use has already been preserved venous access device (port-a-cath) or bone-marrow aspiration during the process. is performed following the oophorectomy. In the case of Herein, we aimed to study the human age-specific oocytes normal post-operative course, discharge is customarily 24 h maturation ability in naïve human oocytes collected from media post procedure. Freezing of ovarian tissue has previously been of ovarian cortex pieces during fertility preservation procedures described in the literature (Meirow et al., 1999) and performed in order to define the age groups in which IVM should be in a similar fashion in our medical center. Briefly, ovarian attempted following OTC. cortex is carefully separated from the medulla in a specific media using sterile scissors. The tissue is then cut into 5- mm3 stripes, that are transferred to pre-cooled freezing medium MATERIALS AND METHODS containing 1.5 M dimethyl sulfoxide (DMSO) and 0.1 M sucrose. Each fragment is then placed in a 2 ml cryovial containing Study Population a cryoprotectant medium (sucrose, ethylene glycol, and serum Our study cohort consisted of female patients aged 1–35 years, substitute supplement) and processed using a slow freezing referred to our fertility preservation clinic between 2003 and protocol in a programmable freezing machine (Kryo 360, Planer, 2020. Patients for whom data regarding cancer diagnosis, United Kingdom). The frozen vials, each containing five cortex chemotherapy, and OTC related data was available were included slices, are then stored in liquid nitrogen. Frontiers in Cell and Developmental Biology| www.frontiersin.org 2 June 2021| Volume 9| Article 667682 fcell-09-667682 June 15, 2021 Time: 15:47 # 3 Karavani et al. IVM Rates Across the Age Groups Cumulus Oocyte Complexes Collection (HSD) test. Association of the patients’ age and the in vitro From the Media and Cortex maturation rate was tested using the Pearson correlation coefficient (“ ”) for the 1–17 years and the 18–35 years age Following the cortex dissection and cryopreservation, the r groups separately.
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