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Cryopreservation of Intact Human Ovary with Its Vascular Pedicle

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Cryopreservation of Intact Human Ovary with Its Vascular Pedicle del227.fm Page 1 Tuesday, May 30, 2006 12:23 PM ARTICLE IN PRESS Human Reproduction Page 1 of 12 doi:10.1093/humrep/del227 Cryopreservation of intact human ovary with its vascular pedicle Mohamed A.Bedaiwy1,2, Mahmoud R.Hussein3, Charles Biscotti4 and Tommaso Falcone1,5 1Department of Obstetrics and Gynecology, Minimally Invasive Surgery Center, The Cleveland Clinic Foundation, Cleveland, OH, USA, 5 2Department of Obstetrics and Gynecology, 3Department of Pathology, Assiut University Hospitals and School of Medicine, Assiut, Egypt and 4Anatomic Pathology Department, Minimally Invasive Surgery Center, The Cleveland Clinic Foundation, Cleveland, OH, USA 5To whom correspondence should be addressed at: Department of Obstetrics and Gynecology, A81, The Cleveland Clinic Foundation, 9500 Euclid Avenue, Cleveland, OH 44195, USA. E-mail: [email protected] 10 BACKGROUND: The aim of this study was to assess the immediate post-thawing injury to the human ovary that was cryopreserved either as a whole with its vascular pedicle or as ovarian cortical strips. MATERIALS AND METHODS: Bilateral oophorectomy was performed in two women (46 and 44 years old) undergoing vaginal hysterectomy and laparoscopic hysterectomy, respectively. Both women agreed to donate their ovaries for experimental research. In both patients, one of the harvested ovaries was sectioned and cryopreserved (by slow freezing) as ovarian cortical 15 strips of 1.0 ´ 1.0 ´ 5.0 mm3 each. The other ovary was cryopreserved intact with its vascular pedicle. After thawing 7 days later, follicular viability, histology, terminal deoxynucleotidyl transferase (TdT)-mediated dUTP-digoxigenin nick-end labelling (TUNEL) assay (to detect apoptosis) and immunoperoxidase staining (to define Bcl-2 and p53 pro- tein expression profiles) of the ovarian tissue were performed. Tissues from non-cryopreserved ovaries served as con- trol specimens (two cases). RESULTS: The overall viability of the primordial follicles was 75 and 78% in intact 20 cryopreserved–thawed (C–T) ovaries and 81 and 83% in ovarian cortical strips in the 46- and 44-year-old patients, respectively. Comparable primordial follicle counts, absence of features of necrosis, mean values of apoptosis and weak Bcl-2 and p53 protein expressions were observed both in the intact C–T ovary and in the C–T ovarian cortical strips. CONCLUSIONS: Cryoperfusion and cryopreservation of entire human ovary can be achieved with the main- tenance of excellent viability of the superficial and the deeper tissues using a slow-freezing protocol. Cryopreserva- 25 tion injury is associated neither with significant alteration in the expression pattern of Bcl-2 and p53 proteins in the ovarian tissues nor with significant follicular damage. Key words: apoptosis/Bcl-2/cryopreservation/follicular viability/intact human ovary Introduction can be implanted after cancer treatment as an autograft to an 45 Although many reproductive-age patients can survive their orthotopic or a heterotopic site. Immature oocytes derived from 30 cancers and lead normal lives, they are at increased risk of thawed tissue can be matured in vitro if appropriate protocols impaired reproductive functions. Consequently, fertility pres- are developed in the future. Also, the maturation process of the ervation is an important quality-of-life issue for them. Fertility immature oocytes could be achieved by xenografting in immu- preservation strategies were introduced to protect and/or regain nodeficient mice (Gook et al., 2003). 50 reproductive function in patients exposed to cancer chemother- To date, ovulation and creation of a human embryo from 35 apy and/or radiotherapy. Advances in assisted reproductive heterotopic ovarian transplant have been reported (Oktay et al., technologies (ART), such as ovarian tissue cryopreservation 2004). Moreover, two live births from orthotopic ovarian trans- and transplantation, oocyte cryopreservation and novel ovula- plants following spontaneous (Donnez et al., 2004) and IVF tion induction regimens, have renewed interest in fertility pres- (Meirow et al., 2005) cycles were reported, following modified 55 ervation in women scheduled to receive gonadotoxic cryopreservation and surgical protocols pioneered, in sheep, by 40 chemotherapy and/or radiotherapy (Falcone et al., 2004). Of Gosden and associates (Gosden et al., 1994; Baird et al., these technologies, ovarian tissue cryopreservation may be a 1999). Despite these advances, ischaemic damage to the tissue viable option for women who cannot delay treatment to undergo and revascularization injury and the theoretical possibility of ovarian stimulation to create embryos or obtain oocytes for reintroducing malignant tumour cells remain as the main 60 freezing. In this entirely experimental process, thawed tissue limitations for this option (Bedaiwy and Falcone, 2004). © The Author 2006. Published by Oxford University Press on behalf of the European Society of Human Reproduction and Embryology. All rights reserved. 1 For Permissions, please email: [email protected] del227.fm Page 2 Tuesday, May 30, 2006 12:23 PM ARTICLE IN PRESS M.A.Bedaiwy et al. The ischaemic damage to ovarian tissues can induce a high Materials and methods 120 rate of follicular loss (Baird et al., 1999; Demirci et al., 2002). The study group included both control (non-cryopreserved) and cryo- Therefore, eliminating this ischaemic damage could maintain preserved human ovaries. Also tissue sections from lymph nodes, 65 both the viability and the functional integrity of the transplant. squamous cell carcinoma, leukaemia cell lines, normal skin and liver Ideally, this could be achieved by transplantation of an intact were used as tissue-specific positive controls for Bcl-2, p53, apoptotic ovary with vascular anastomosis. Transplantation of an intact cells, PAS and Masson’s trichrome staining. 125 ovary with its vascular pedicle using microvascular anastomo- sis was achieved both in murine species (Yin et al., 2003) and Patients in the cryopreservation group 70 in mammals (Jeremias et al., 2002; Bedaiwy et al., 2003). The Institutional Review Board of The Cleveland Clinic Foundation Partial restoration of hormonal functions (Bedaiwy et al., approved this study. The first patient, aged 46 years, presented with 2003) and pregnancy (Wang et al., 2002) after transplantation menorrhagia and symptomatic fibroid uterus, who underwent total vaginal hysterectomy with bilateral salpingo-oophorectomy, McCall 130 of intact cryopreserved–thawed (C–T) ovaries were also culdoplasty and cystoscopy. Intraoperative findings included an 8–10 reported. Recently, cryopreservation of intact human ovary week-sized uterus and normal-appearing ovaries. The second patient, 75 with its vascular pedicle resulting in high post-thaw survival rates aged 44 years, presented with severe premenstrual dysphoric disor- of follicles, small vessels and stromal cells as well as a normal ders, who underwent laparoscopic bilateral salpingo-oophorectomy. histological structure in all the ovarian components was Normal-appearing uterus, tubes and ovaries were detected. Both ova- 135 reported using a slow-freezing protocol. Slow freezing was ries and their pedicles, from both patients, were processed immedi- achieved using a cryofreezing one-degree container (Martinez- ately as detailed below. 80 Madrid et al., 2004). The structural homeostasis of tissues is regulated by a delicate Patients in the control group balance between cell survival and apoptotic cell death. In tis- In the control group, formalin-fixed paraffin-embedded ovarian sues, several molecules are involved in the survival (survival tissue was obtained from the Archives of the Department of 140 molecules such as Bcl-2) or cell death (apoptotic molecules Pathology, Assiut University Hospitals. Four ovarian tissue speci- mens were obtained from two women, 44 and 47 years old. The first 85 such as p53) processes. Bcl-2 is a membrane-associated protein was diagnosed with irregular uterine bleeding due to uterine that resides in the nuclear envelope and mitochondria. It exerts fibroids and was treated by total abdominal hysterectomy with its survival functions by modulating the mitochondrial release bilateral salpingo-oophorectomy. The second underwent total vag- 145 of cytochrome c and antagonizing the effects of Bax gene (Bcl-2- inal hysterectomy with bilateral salpingo-oophorectomy due to associated X). Bcl-2 is expressed in granulosa cells of both pelvic organ prolapse. The ovaries obtained from both patients 90 fetal and adult ovaries. p53 gene encodes a 53-kDa oncosup- appeared normal with a smooth white convoluted surface and firm pressive nuclear protein that functions to antagonize Bcl-2 consistency. effects. In the ovary, p53 protein is expressed in the apoptotic granulosa cells of atretic follicles. In several organs such as the Cryopreservation 150 heart, ischaemia is associated with the induction of Bcl-2 and Cryopreservation of the intact ovary 95 p53 protein expressions. Similarly, the induction of these mol- We adopted our previous protocol described in 2003 (Bedaiwy ecules following ovarian ischaemia may have far-reaching et al., 2003). Briefly, immediately after oophorectomy, one ovary effects on the outcome of the subsequent ovarian transplantation (from each patient) was perfused with heparinized Ringer’s solu- (Hussein, 2005). tion followed by perfusion and immersion in a bath containing the 155 Although previous studies examined the long-term effects cryoprotective mixture which was
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