Abstract
Purpose
Fertility preservation in women with cancer represents a major medical challenge at the intersection of oncological and reproductive concerns. With therapeutic advancements, the survival rates of cancer patients have significantly improved, offering the possibility of motherhood. Currently, there is a lack of data on the return of cryopreserved oocytes/embryos and pregnancy outcomes following cancer treatment.
Methods
We conducted a retrospective, single-center, descriptive cohort study, including women who underwent fertility preservation through oocyte or embryo cryopreservation before a medium risk of gonadotoxicity chemotherapy for cancer at our Department of Reproductive Medicine and Oncofertility between January 2012 and May 2024.
Results
A total of 327 women were included, with 318 cases of oocyte cryopreservation and nine embryo cryopreservation. The average follow-up duration was 5.1 ± 2.7 years. Among the 49 women who expressed a desire for pregnancy post-cancer treatment, 65.3% of them (n = 32/49) reported at least one live birth. Of the 35 live births recorded, 80% (n = 28/35) resulted from spontaneous pregnancies, five were achieved after thawing vitrified oocytes (11.4%), and three after oocyte donation (8.6%). The return rate of cryopreserved oocytes was 6.92% (22/318), with a live birth rate per woman of 22.7% (5/22) following oocyte warming.
Conclusion
Although fertility preservation (FP) must be proposed systematically in age-reproductive women facing cancer with a medium risk of gonadotoxicity chemotherapy, physicians must be aware of the low rate of oocyte return and the potential for spontaneous pregnancies despite a post-cancer diminished ovarian reserve. Fertility consultations should also be better integrated into oncologic post-treatment care.
Keywords: Cancer, Fertility preservation, Oocyte vitrification, Follow-up, Live birth rate
Introduction
Fertility preservation (FP) in children and age-reproductive women with cancer represents a major medical challenge. With therapeutic advancements, the survival rate of women with cancer has significantly improved, and the possibility of motherhood is an important factor for long-term quality of life. All women of childbearing age have to be informed about the risk level of gonadotoxicity and/or premature ovarian insufficiency related to the chemotherapy protocol, prior to the start of treatment, in order to discuss potential FP techniques [1, 21, 26]. Since 2011, French law has authorized oocyte vitrification, which is now the reference technique for fertility preservation in the context of cancer [4, 25]. Oocyte vitrification is a viable option across all levels of gonadotoxic risk, including high-risk treatments, while ovarian tissue cryopreservation may be offered either as a complement to oocyte vitrification in high gonadotoxic risk chemotherapy or as an alternative when oocyte vitrification is not feasible. Additionally, ovarian tissue cryopreservation is suitable for prepubertal girls or premenarchal adolescents diagnosed with malignancy, as well as for patients unable to undergo controlled ovarian stimulation due to an urgent need for cancer therapy (Rives et al. 2022). Oocyte vitrification, as opposed to embryo preservation, allows women autonomy in their future reproductive decisions, independently of a partner’s presence at the time of fertility preservation. In 2016, Perrin et al. reported the first French live birth following FP in a woman whose oocytes had been vitrified before treatment for stage IV Hodgkin’s lymphoma [23]. Long-term data on the use of cryopreserved oocytes/embryos in the context of cancer are limited and often grouped with other FP indications, as endometriosis and/or elective fertility preservation. The utilization rate of cryopreserved oocytes is estimated to be between 7 and 13%, with a live birth rate (LBR) per woman from the use of vitrified oocytes ranging between 18 and 33% [2, 16]. Additionally, although follow-up for ovarian function after cancer treatment is recommended, it appears that few women pursue consultations for this purpose during their follow-up [18, 19]. The objective of our study was to study the follow-up of reproductive data on women who underwent oocyte or embryo vitrification at our assisted reproduction center before starting cancer treatment.
Materials and methods
We conducted a retrospective, single-center, descriptive epidemiological study at the Department of Reproductive Medicine and Oncofertility in a Universitary Teaching Hospital on a cohort of women who underwent FP through oocyte or embryo cryopreservation before starting chemotherapy, between January 2012 and May 2024. In the strategy of our oncofertility department, we propose oocyte vitrification as the first-line option before chemotherapy with medium gonadotoxic risk [10]. In high gonadotoxic risk chemotherapy, or when chemotherapy has started before FP, we first recommend ovarian tissue cryopreservation, either as a complement to oocyte vitrification or as an alternative when oocyte vitrification is not feasible. Usually, in low risk gonadotoxic chemotherapy, we propose an ovarian reserve assay before and after cancer, and oocyte vitrification is proposed only if diminished ovarian reserve before starting treatment or if patient is about 35 years with a risk of postponing a pregnancy for several years. Cases of ovarian tissue cryopreservation were not included in this study. All women included in the study were followed up until May 2024. Data were extracted from medical records.
All women underwent at least one cycle of controlled ovarian stimulation (COS), using an antagonist random start protocol (daily administration of GnRH antagonist starting on the first day of ovarian stimulation). Recombinant follicle-stimulating hormone (FSH) or FSH combined with luteinizing hormone (LH) gonadotropins were administered at doses ranging from 150 to 450 IU/day, depending on BMI, age, anti-Müllerian hormone (AMH) levels, and antral follicle count. Follicular growth was monitored by several pelvic ultrasounds, combined with serum levels of estradiol, progesterone, and LH during ovarian stimulation. Ovulation was triggered by administering recombinant human chorionic gonadotropin (hCG) and/or GnRH analogs when at least three follicles measured more than 17 mm. Oocyte retrieval was performed 36 h after ovulation trigger, under general or local anesthesia. Oocytes were vitrified on the same day or underwent in vitro fertilization in cases of embryo vitrification.
Oocytes were incubated for 1 h at 37 °C, 6% CO2 in culture medium (FertiCult® IVF medium, Fertipro, Beernem, Belgium), then denudated and metaphase II oocytes were vitrified. Alternatively, oocytes were fertilized either by ICSI or IVF depending on semen parameters, according to ESHRE protocols, cultured in Sage 1-Step ® culture medium (Cooper Surgical, Ballerup, Denmark) at 37 °C, 6% CO2, 5% O2, then vitrified. Vitrification of oocytes and embryos was performed according to manufacturer’s protocol (Vit Kit-Freeze®, Fujifilm Irvine Scientific, Tilburg, The Netherlands) in High Security Vitrification straws (Cryo Bio System®) [11]. They were subsequently stored in liquid nitrogen.
In the follow-up post-cancer, AMH was systematically studied in women who came back for a pregnancy project. Following the data of Decanter et al., AMH was always assessed at least 1 year after the end of chemotherapy [6].
For oocyte and embryo warming, the manufacturer’s protocols were used (Vit Kit-Thaw®, Fujifilm Irvine Scientific, Tilburg, The Netherlands). Thawed oocytes and embryos were cultured for 2 h in 20% HSA culture medium (FertiCult® IVF medium, Fertipro, Beernem, Belgium); oocytes were then fertilized by ICSI according to ESHRE protocol, as described above [11]. Thawed and fresh embryos were transferred under echoguidance (Guardia ® transfer catheter, COOK Medical, Limerick, Ireland).
The primary objective of the study was to evaluate the live birth rate and the return rate of vitrified oocytes/embryos following cancer treatment. Secondary objectives were the oocyte survival rate after thawing, the fertilization rate, and the live birth rate after oocyte warming.
Statistical analysis
Categorical variables were presented as numbers and percentages. Quantitative variables were presented as means ± standard deviation for continuous variables.
Results
A total of 327 women were included; 318 underwent oocyte cryopreservation before starting cancer treatment, and nine underwent embryo cryopreservation. The characteristics of the women are described in Table 1. The average age at the time of oocyte retrieval was 28.7 ± 5.9 years, with a BMI of 22.9 ± 4.6 kg/m2 and an AMH level of 2.8 ± 2.3 ng/mL. The majority of the women (71.3%, n = 233/327) were nulliparous before fertility preservation. At the time of the study, the women’s average age was 33.8 ± 6.5 years, corresponding to an average follow-up duration of 5.1 ± 2.7 years.
Table 1.
Characteristics of the age-reproductive women undergoing oocyte or embryo vitrification prior to oncological treatment
| N = 327 | |
|---|---|
| Mean age at time of oocyte retrieval (years) | 28.7 ± 5.9 |
| Current age (years) | 33.8 ± 6.5 |
| Mean follow-up duration (years) | 5.1 ± 2.7 |
| Number of women who underwent oocyte vitrification | 318 |
| Number of women who underwent embryo vitrification | 9 |
| Gravidity before FP | |
| 0 | 233 (71.3) |
| 1 | 45 (13.8) |
| 2 | 30 (9.2) |
| 3 or more | 10 (3.1) |
| Parity before FP | |
| 0 | 268 (82) |
| 1 | 41 (12.5) |
| 2 | 18 (5.5) |
| BMI (kg/m2) | 22.9 ± 4.6 |
| AMH (ng/ml) | |
| Before chemotherapy1 | 2.8 ± 2.3 |
| After chemotherapy (> 1 year)2 | 0.8 ± 1.7 |
| AFC | |
| Before chemotherapy3 | 19.3 ± 11.5 |
| After chemotherapy (> 1 year)4 | 6.8 ± 7.4 |
| Mean number of vitrified oocytes per woman | 10.4 ± 7.5 |
| Mean number of vitrified embryos per woman | 5.7 ± 3.7 |
Note: Data are expressed as mean ± standard deviation or n (%)
AMH=anti-Mullerian hormone; BMI= body
Mass index; AFC= antral follicle count
Missing data:1Analysis on n=252; 2Analysis on n=76; 3Analysis on n=262;4Analysis on n=49
The indications for FP in our cohort are presented in Table 2. Among the 327 patients, 170 patients (52%) underwent a FP technique due to a hematologic malignancy, and 92 patients (28.1%) due to gynecological cancer, of which 86 (93.5%) were for breast cancer (86/92). It is important to note that the three women with acute myeloid leukemia underwent oocyte retrieval just after receiving their first course of chemotherapy. This procedure only concerns these three women who at the time refused cryopreservation of ovarian tissue and is not recommended [20].
Table 2.
Fertility preservation with oocyte or embryo vitrification before cancer treatment: characteristics of oncological indications
| N = 327 (%) | |
|---|---|
| Hematologic | 170 (52) |
| Hodgkin’s lymphoma | 124 |
| Non-Hodgkin’s lymphoma | 36 |
| Acute myeloid leukemia | 3 |
| Chronic myeloid leukemia | 2 |
| Other | 5 |
| Gynecologic | 92 (28.1) |
| Breast cancer | 86 |
| Ovarian cancer | 6 |
| Sarcoma | 18 (5.5) |
| Gastrointestinal cancer | 15 (4.6) |
| Glioma | 12 (37) |
| Melanoma | 10 (3.1) |
| Other | 10 (3.1) |
Note: Data are presented as n (%)
The follow-up is resumed by the flowchart in Fig. 1. Among the 327 patients who cryopreserved their oocytes or embryos, 15% of women (n = 49) expressed a desire for pregnancy after cancer treatment, and 65.3% of them (n = 32/49) reported at least one live birth after cancer. A total of 35 live births were recorded for 32 women, of which 80% (n = 28/35) occurred after spontaneous pregnancies. Four births were achieved with frozen-thawed oocytes, and three births resulted from oocyte donation, representing respectively 11.4% and 8.6% of the post-cancer pregnancies.
Fig. 1.
Follow-up after oncological treatment
Characteristics of the frozen-thawed cycles after oocyte vitrification are presented in Table 3. The majority of women who returned to use their oocytes had breast cancer or Hodgkin’s lymphoma with more than 2 courses of BEACOPP (bleomycin, etoposide, doxorubicin, cyclophosphamide, vincristine, procarbazine, and prednisolone). The return rate of vitrified oocytes was 6.9% (22/318), with a live birth rate per woman of 22.7% (5/22) after oocyte warming. The average age of patients at the time of vitrification was 32.7 ± 5.8 years. The average duration between vitrification and the return was 4.3 ± 2.4 years. The average number of oocytes warmed per woman was 8.8 ± 5.2. The oocyte survival rate after warming was 61.3%, and the fertilization rate was 42%.
Table 3.
Fertility preservation with oocyte vitrification before cancer treatment: characteristics of the frozen-thawed cycles
| N = 22 | |
|---|---|
| Age at oocyte retrieval | 32.7 ± 5.8 |
| Age at oocyte return | 37.4 ± 4.9 |
| Type of cancer (%) | |
| Breast cancer | 50 (11/22) |
| Hodgkin’s lymphoma | 31.8 (7/22) |
| Non-Hodgkin’s lymphoma | 4.6 (1/22) |
| Ovarian cancer | 9 (2/22) |
| Medulloblastoma | 4.6 (1/22) |
| Total number of cycles | 29 |
| Number of cycles per woman | 1.3 ± 0.7 |
| Number of oocytes vitrified per woman | 8.8 ± 5.2 |
| Number of oocytes injected per woman | 4.1 ± 3.2 |
| Total number of warmed thawed oocytes | 194 |
| Total number of mature oocytes injected | 119 |
| Survival rate post-thawing (%) | 61.3 |
| Total number of embryos | 57 |
| Total number of diploid embryos | 50 |
| Fertilization rate (%) | 42 |
| Number of usable embryos per woman | 1.4 ± 1.3 |
| Number of fresh embryos transferred | 31 |
| Number of frozen embryos | 11 |
| Number of FET | 5 |
| Total number of embryos transferred | 36 |
| Number of pregnancies | 8 |
| Number of women | 7 |
| Outcomes | |
| Live birth | 5 |
| Early miscarriage | 3 |
| Pregnancy rate per transfer (%) | 22.2 (8/36) |
| Live birth rate per woman (%) | 22.7 (5/22) |
Note: Data are expressed as mean ± standard deviation or % (n)
FET=frozen and thawed embryo transfer
Among the nine women who underwent embryo vitrification, four had a child following a spontaneous pregnancy. Two couples returned for a frozen embryo transfer without achieving pregnancy. Nevertheless, one of these two couples subsequently achieved a live birth following a spontaneous pregnancy.
Among our cohort, 73.1% of them (n = 239) did not return for specialized oncofertility follow-up after cancer treatment, and 3.4% of them passed away (n = 11). The outcomes of the vitrified oocytes and embryos are detailed in Table 4.
Table 4.
Fertility preservation with oocyte vitrification before cancer treatment: outcome of vitrified oocytes and embryos
| Oocytes | Embryos | |
|---|---|---|
| Cryostorage without return | 284 | 5 |
| Partial return | 2 | |
| Complete return | 20 | 2 |
| Donation to research | 0 | |
| Destruction asked by patient/couple | 11 | 2 |
| Transfer for return to another center | 1 |
Among the women who experienced unsuccessful outcome after oocyte return, one woman underwent IVF-ICSI with her own fresh oocytes, six received oocyte donations, and one received a double gametes donation. Only three women achieved pregnancy through oocyte donation.
Discussion
Although FP must be proposed systematically in age-reproductive women facing cancer with treatment having a medium risk of gonadotoxicity, physicians must be aware of the low rate of oocyte return and the high rate of spontaneous pregnancies despite a post-cancer diminished ovarian reserve. In fertility preservation, the counseling must take into account the risk of premature ovarian failure related to the pre-treatment ovarian reserve, the age, and the gonadotoxicity of the chemotherapy regimen, by estimating the Cyclophosphamide Equivalent Dose (CED) [3]. In our cohort, we propose oocyte vitrification in case of chemotherapy with a medium risk of gonadotoxicity, and we did not include in our study the patients who underwent OTC, indicated before high risk of gonadotoxicity. So, in women who underwent a medium risk gonadotoxicity chemotherapy, the majority of live births after cancer were achieved spontaneously, with only 6.9% of women who asked for returning their oocytes. These findings are consistent with the literature. In the cohort of 508 patients studied by Porcu et al., with a mean follow-up of 9.3 ± 6.8 years, most pregnancies were spontaneous, and the oocyte return rate was 8.7% (44/508) for oncological patients [24]. Similarly, Cobo et al. reported an oocyte usage rate of 7.2% (80/1073) for oncological indications [5]. In the study of Peigné et al., out of the 793 women who had cryopreserved oocytes and embryos before breast cancer treatment, 68 (8.5% [6.7–10.7]) used them, resulting in eight live births. The majority of live births in this cohort were spontaneous pregnancies (81%, n = 89/110) [22].
Despite our center’s 12 years of experience in fertility preservation through oocyte vitrification, only 22 survivor cancer women returned to use their oocytes, and two women returned to use their embryos. In our study, the LBR per woman after oocyte warming was 22.7%, lower than the 32% LBR rate reported in a meta-analysis by Fraison et al., which included eight studies and 177 patients [13]. This difference may be explained by the relatively low number of women in our cohort who return their oocytes, as well as a post-warming oocyte survival rate of 61.3% and a fertilization rate of 42%, which are below the rates usually reported in the literature in the context of cancer. Porcu et al. reported a post-warming oocyte survival rate of 80.9% (n = 157/194) and a fertilization rate of 73.2% (n = 101/138) in the oncological group [24]. In the cohort of Cobo et al., the oocyte survival rate was 81.8% (n = 495/609) [5].
However, half of our cohort consisted of hematological indications for FP. In Hodgkin’s lymphomas, some authors have shown that the pro-inflammatory peri-oocyte follicular environment could impact ovarian reserve, ovarian stimulation response, and oocyte quality [27]. In women with Hodgkin’s lymphoma, fertility preservation prior to ABVD (doxorubicin, bleomycin, vinblastine, and dacarbazine) chemotherapy should be discussed depending on age, but also in cases where there is a high probability of therapeutic intensification [6]. In women who are to undergo chemotherapy with alkylating agents, it is crucial to perform fertility preservation. The choice between oocyte and/or ovarian tissue cryopreservation should be based on the patient’s condition, age, cumulative dose of alkylating agent, the emergency of starting treatment, and the existence of recent exposure to chemotherapy [7, 9].
Since 2011, in our ART center, oocyte vitrification is counseled in first intention over embryo vitrification, and we were unable to compare these two techniques due to the limited number of cases involving embryo vitrification in our cohort. The cohort study of ter Welle-Butalid et al. also found a minority of FP cases involving embryo preservation, but reported comparable LBR between the two techniques [28]. In the meta-analysis of Fraison et al., the LBR after embryo and oocyte cryopreservation for cancer were 41% (95% CI: 34–48, I2: 0%) and 32% (95% CI: 26–39, I2: 0%), respectively. Survival rate after thawing, fertilization rate, and LBR after oocyte vitrification are laboratory dependent and probably embryologist dependent. In a SWOT analysis, Gil-Arribas et al. underlined that there is a lack of control of ART laboratories with a risk of non-optimal results after oocyte vitrification [14]. Embryo cryopreservation is probably better mastered because it has been used for over 40 years, with maybe less interlaboratory variability after embryo freezing [29]. Therefore, each laboratory should be able to present its own laboratory results in order to provide the best possible counseling to women requiring fertility preservation. There is also the possibility of altered oocyte quality at the time of FP in the context of cancer, although this argument is debated [12]. Therefore, when it is possible, women with a partner should be offered the option to cryopreserve unfertilized oocytes or to split the oocytes, allowing for both embryo and oocyte cryopreservation [1]. Current mean age of the women in our study was 33.8 ± 6.5 years, suggesting that many women may not yet have considered pregnancy. Additionally, our study may underestimate the number of spontaneous pregnancies, as 73.1% of women did not return for follow-up at our center after their treatments. This high rate of patients lost to follow-up, which is a major limitation of our study, highlights the need for better integration of fertility consultations into the post-treatment care provided by oncologists.
Despite established guidelines, not all women with cancer receive an oncofertility counseling before treatment [1],Rives et al. 2022). Several studies reported a positive psychological impact from fertility preservation, though the decision to pursue fertility preservation techniques is often challenging [8, 17]. Greenwood et al. also highlighted the importance of clear information, emotional support, and providing accurate success rates to reduce the risk of regret [15]. Over time, as more long-term data on cancer survivors and assisted reproduction outcomes with vitrified oocytes become available, we will be able to offer more personalized counseling per type of cancer regarding fertility preservation decisions.
Conclusion
In women who have undergone oocyte vitrification prior to cancer treatment with chemotherapy at moderate risk of gonadotoxicity, physicians should be mindful of both the challenges posed by the low rate of oocyte return and the potential for spontaneous pregnancies, despite the diminished ovarian reserve often observed after cancer treatment. It is also essential to recognize that many women seeking to conceive after cancer treatment may face difficulties in achieving a pregnancy. This highlights the critical need for comprehensive counseling and individualized fertility preservation strategies to support cancer patients in their reproductive choices. Fertility preservation should be viewed as an important option for future conception post-cancer and must be systematically offered prior to any gonadotoxic anticancer treatment. Furthermore, the high rate of patients lost to follow-up, which is a major limitation of our study, highlights the need for better integration of fertility consultations into the post-treatment care provided by oncologists.
Author contribution
All authors contributed to the study conception and design. Material preparation, data collection, and analysis were performed by Appoline Zimmermann. The first draft of the manuscript was written by Appoline Zimmermann, and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Funding
No funding was received for conducting this study.
Data availability
The datasets generated during the current study are available from the corresponding author on reasonable request.
Declarations
Ethical approval
This study was approved by the local ethics committee of our university.
Conflict of interest
The authors declare no competing interests.
Footnotes
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
References
- 1.Anderson RA, Amant F, Braat D, D’Angelo A, Chuva de Sousa Lopes SM, Demeestere I, Dwek S, Frith L, Lambertini M, Maslin C, Moura-Ramos M, Nogueira D, Rodriguez-Wallberg K, Vermeulen N. ESHRE guideline: female fertility preservation†. Hum Reprod Open 2020(4):hoaa052. 10.1093/hropen/hoaa052. [DOI] [PMC free article] [PubMed]
- 2.Balkenende EM, Dahhan T, van der Veen F, Repping S, Goddijn M. Reproductive outcomes after oocyte banking for fertility preservation. Reprod Biomed Online. 2018;37(4):425–33. 10.1016/j.rbmo.2018.07.005. [DOI] [PubMed] [Google Scholar]
- 3.Close A, Burns K, Bjornard K, Webb M, Chavez J, Chow EJ, Meacham L. Fertility preservation in pediatric leukemia and lymphoma: a report from the Children’s Oncology Group. Pediatr Blood Cancer. 2023;70(8): e30407. 10.1002/pbc.30407. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Cobo A, Diaz C. Clinical application of oocyte vitrification: a systematic review and meta-analysis of randomized controlled trials. Fertil Steril. 2011;96(2):277–85. 10.1016/j.fertnstert.2011.06.030. [DOI] [PubMed] [Google Scholar]
- 5.Cobo A, García-Velasco J, Domingo J, Pellicer A, Remohí J. Elective and onco-fertility preservation: factors related to IVF outcomes. Hum Reprod Oxf Engl. 2018;33(12):2222–31. 10.1093/humrep/dey321. [DOI] [PubMed] [Google Scholar]
- 6.Decanter C, Delepine J, Behal H, Manier S, Bruno B, Barbatti M, Robin C, Labreuche J, Morschhauser F, Pigny P. Longitudinal study of AMH variations in 122 adolescents and young adults (AYA) and non-AYA lymphoma patients to evaluate the chemo-induced ovarian toxicity to further personalise fertility preservation counselling. Hum Reprod. 2021;36(10):2743–52. 10.1093/humrep/deab189. [DOI] [PubMed] [Google Scholar]
- 7.Delattre S, Segers I, Van Moer E, Drakopoulos P, Mateizel I, Enghels L, Tournaye H, De Vos M. Combining fertility preservation procedures to spread the eggs across different baskets: a feasibility study. Hum Reprod Oxf Engl. 2020;35(11):2524–36. 10.1093/humrep/deaa193. [DOI] [PubMed] [Google Scholar]
- 8.Deshpande NA, Braun IM, Meyer FL. Impact of fertility preservation counseling and treatment on psychological outcomes among women with cancer: a systematic review. Cancer. 2015;121(22):3938–47. 10.1002/cncr.29637. [DOI] [PubMed] [Google Scholar]
- 9.Dolmans M-M, von Wolff M, Poirot C, Diaz-Garcia C, Cacciottola L, Boissel N, Liebenthron J, Pellicer A, Donnez J, Andersen CY. Transplantation of cryopreserved ovarian tissue in a series of 285 women: a review of five leading European centers. Fertil Steril. 2021;115(5):1102–15. 10.1016/j.fertnstert.2021.03.008. [DOI] [PubMed] [Google Scholar]
- 10.Donnez J, Dolmans M-M. Fertility preservation in women. N Engl J Med. 2017;377(17):1657–65. 10.1056/NEJMra1614676. [DOI] [PubMed] [Google Scholar]
- 11.ESHRE Guideline Group on Good Practice in IVF Labs, De los Santos MJ, Apter S, Coticchio G, Debrock S, Lundin K, Plancha CE, Prados F, Rienzi L, Verheyen G, Woodward B, Vermeulen N. Revised guidelines for good practice in IVF laboratories (2015)†. Hum Reprod. 2016;31(4):685–6. 10.1093/humrep/dew016. [DOI] [PubMed]
- 12.Fabiani C, Ferrante MG, Meneghini C, Licata E, Paciotti G, Gallo M, Schiavi M, Spina V, Guarino A, Caserta D, Rago R. Female fertility preservation: impact of cancer on ovarian function and oocyte quality. Int J Gynecol Obstet. 2022;156(1):166–71. 10.1002/ijgo.13702. [DOI] [PubMed] [Google Scholar]
- 13.Fraison E, Huberlant S, Labrune E, Cavalieri M, Montagut M, Brugnon F, Courbiere B. Live birth rate after female fertility preservation for cancer or haematopoietic stem cell transplantation: a systematic review and meta-analysis of the three main techniques; embryo, oocyte and ovarian tissue cryopreservation. Hum Reprod. 2023;38(3):489–502. 10.1093/humrep/deac249. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14.Gil-Arribas E, Blockeel C, Pennings G, Nekkebroeck J, Velasco JAG, Serna J, De Vos M. Oocyte vitrification for elective fertility preservation: a SWOT analysis. Reprod Biomed Online. 2022;44(6):1005–14. 10.1016/j.rbmo.2022.02.001. [DOI] [PubMed] [Google Scholar]
- 15.Greenwood EA, Pasch LA, Hastie J, Cedars MI, Huddleston HG. To freeze or not to freeze: decision regret and satisfaction following elective oocyte cryopreservation. Fertil Steril. 2018;109(6):1097-1104.e1. 10.1016/j.fertnstert.2018.02.127. [DOI] [PubMed] [Google Scholar]
- 16.Hammarberg K, Kirkman M, Stern C, McLachlan RI, Clarke G, Agresta F, Gook D, Rombauts L, Vollenhoven B, Fisher JRW. Survey of reproductive experiences and outcomes of cancer survivors who stored reproductive material before treatment. Hum Reprod. 2017;32(12):2423–30. 10.1093/humrep/dex314. [DOI] [PubMed] [Google Scholar]
- 17.Logan S, Anazodo A. The psychological importance of fertility preservation counseling and support for cancer patients. Acta Obstet Gynecol Scand. 2019;98(5):583–97. 10.1111/aogs.13562. [DOI] [PubMed] [Google Scholar]
- 18.Marklund A, Eloranta S, Wikander I, Kitlinski ML, Lood M, Nedstrand E, Thurin-Kjellberg A, Zhang P, Bergh J, Rodriguez-Wallberg KA. Efficacy and safety of controlled ovarian stimulation using GnRH antagonist protocols for emergency fertility preservation in young women with breast cancer—a prospective nationwide Swedish multicenter study. Hum Reprod. 2020;35(4):929–38. 10.1093/humrep/deaa029. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19.Massarotti C, Scaruffi P, Lambertini M, Sozzi F, Remorgida V, Anserini P. Beyond fertility preservation: role of the oncofertility unit in the reproductive and gynecological follow-up of young cancer patients. Hum Reprod Oxf Engl. 2019;34(8):1462–9. 10.1093/humrep/dez108. [DOI] [PubMed] [Google Scholar]
- 20.Meirow D, Epstein M, Lewis H, Nugent D, Gosden RG. Administration of cyclophosphamide at different stages of follicular maturation in mice: effects on reproductive performance and fetal malformations. Hum Reprod. 2001;16(4):632–7. 10.1093/humrep/16.4.632. [DOI] [PubMed] [Google Scholar]
- 21.Oktay K, Harvey BE, Partridge AH, Quinn GP, Reinecke J, Taylor HS, Wallace WH, Wang ET, Loren AW. Fertility preservation in patients with cancer: ASCO clinical practice guideline update. J Clin Oncol Off J Am Soc Clin Oncol. 2018;36(19):1994–2001. 10.1200/JCO.2018.78.1914. [DOI] [PubMed] [Google Scholar]
- 22.Peigné M, Mur P, Laup L, Hamy A-S, Sifer C, Mayeur A, Eustache F, Sarandi S, Vinolas C, Rakrouki S, Benoit A, Grynberg M, Sonigo C. Fertility outcomes several years after urgent fertility preservation for patients with breast cancer. Fertil Steril. 2024;122(3):504–13. 10.1016/j.fertnstert.2024.04.031. [DOI] [PubMed] [Google Scholar]
- 23.Perrin J, Saïas-Magnan J, Broussais F, Bouabdallah R, D’Ercole C, Courbiere B. First French live-birth after oocyte vitrification performed before chemotherapy for fertility preservation. J Assist Reprod Genet. 2016;33(5):663–6. 10.1007/s10815-016-0674-8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Porcu E, Cipriani L, Dirodi M, De Iaco P, Perrone AM, Zinzani PL, Taffurelli M, Zamagni C, Ciotti PM, Notarangelo L, Calza N, Damiano G. Successful pregnancies, births, and children development following oocyte cryostorage in female cancer patients during 25 years of fertility preservation. Cancers. 2022;14(6): 1429. 10.3390/cancers14061429. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Rienzi L, Gracia C, Maggiulli R, LaBarbera AR, Kaser DJ, Ubaldi FM, Vanderpoel S, Racowsky C. Oocyte, embryo and blastocyst cryopreservation in ART: systematic review and meta-analysis comparing slow-freezing versus vitrification to produce evidence for the development of global guidance. Hum Reprod Update. 2017;23(2):139–55. 10.1093/humupd/dmw038. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 26.Rives N, Courbière B, Almont T, Kassab D, Berger C, Grynberg M, Papaxanthos A, Decanter C, Elefant E, Dhedin N, Barraud-Lange V, Béranger M-C, Demoor-Goldschmidt C, Frédérique N, Bergère M, Gabrel L, Duperray M, Vermel C, Hoog-Labouret N, Pibarot M, Provansal M, Quéro L, Lejeune H, Methorst C, Saias J, Véronique-Baudin J, Giscard d’Estaing S, Farsi F, Poirot C. Huyghe É (2022) What should be done in terms of fertility preservation for patients with cancer? The French 2021 guidelines. Eur J Cancer Oxf Engl. 1990;173:146–66. 10.1016/j.ejca.2022.05.013. [DOI] [PubMed] [Google Scholar]
- 27.Sonigo C, Comtet M, Duros S, Sifer C, Sermondade N, Grynberg M. Antral follicle responsiveness to FSH, assessed by the follicular output rate (FORT), is altered in Hodgkin’s lymphoma when compared with breast cancer candidates for fertility preservation. J Assist Reprod Genet. 2018;35(1):91–7. 10.1007/s10815-017-1059-3. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 28.ter Welle-Butalid ME, Derhaag JG, van Bree BE, Vriens IJH, Goddijn M, Balkenende EME, Beerendonk CCM, Bos AME, Homminga I, Benneheij SH, van Os HC, Smeenk JMJ, Verhoeven MO, van Bavel CCAW, Tjan-Heijnen VCG, van Golde RJT. Outcomes of female fertility preservation with cryopreservation of oocytes or embryos in the Netherlands: a population-based study. Hum Reprod. 2024;deae243. 10.1093/humrep/deae243. [DOI] [PMC free article] [PubMed]
- 29.Tucker M, Morton P, Liebermann J. Human oocyte cryopreservation: a valid alternative to embryo cryopreservation? Eur J Obstet Gynecol Reprod Biol. 2004;113(Suppl 1):S24-27. 10.1016/j.ejogrb.2003.11.006. [DOI] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
The datasets generated during the current study are available from the corresponding author on reasonable request.