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Published in: Reproductive Biology and Endocrinology 1/2018

Open Access 01-12-2018 | Short communication

In vitro maturation of oocytes from excised ovarian tissue in a patient with autoimmune ovarian insufficiency possibly associated with Epstein-Barr virus infection

Authors: Irma Virant-Klun, Andrej Vogler

Published in: Reproductive Biology and Endocrinology | Issue 1/2018

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Abstract

Background

Some reports show that it is possible to isolate immature oocytes from human ovarian tissue retrieved by a cortex biopsy or ovariectomy of non-stimulated ovaries and mature them in vitro. The mature oocytes can be vitrified and stored for in vitro fertilization, which, along with ovarian tissue cryopreservation, is mostly practiced in young cancer patients to preserve their fertility. There is much less data on this new approach in women with a natural ovarian insufficiency, which can be caused by different factors, including viral infection. In this case report this advanced methodology was used in a young patient suffering from ovarian insufficiency which was possibly associated with Epstein-Barr virus and infectious mononucleosis (glandular fever).

Methods

This case report included a 27-year-old patient who attended our infertility clinic because of ovarian failure as a part of autoimmune polyendocrinopathy that occurred after Epstein-Barr virus infection, which has rarely been reported until now. Although antral follicles were observed in her ovaries by ultrasound monitoring, she was amenorrhoeic with menopausal concentrations of follicle-stimulating hormone (FSH) and without mature follicles. Therefore, a small biopsy of ovarian cortex tissue was performed using laparoscopy to retrieve immature oocytes. The retrieved oocytes were matured in vitro, cryopreserved, and stored for in vitro fertilization and potential pregnancy.

Results

Four immature, germinal vesicle (GV) oocytes were found and removed from tissue, denuded mechanically by a pipette, and matured in vitro in a maturation medium with added FSH and hCG as well as in co-culture with cumulus cells, which were retrieved by their denudation. Three oocytes matured in vitro to the metaphase II (MII) stage and were vitrified for in vitro fertilization along with ovarian tissue cryopreservation.

Conclusion

Our results show that Epstein-Barr infection is possibly associated with autoimmune ovarian failure. The devastating impact on fertility in such disorder can be successfully avoided by in vitro maturation of oocytes from excised ovarian tissue.
Literature
1.
go back to reference Revel A, Koler M, Simon A, Lewin A, Laufer N, Safran A. Oocyte collection during cryopreservation of the ovarian cortex. Fertil Steril. 2003;79:1237–9.CrossRefPubMed Revel A, Koler M, Simon A, Lewin A, Laufer N, Safran A. Oocyte collection during cryopreservation of the ovarian cortex. Fertil Steril. 2003;79:1237–9.CrossRefPubMed
2.
go back to reference Revel A, Revel-Vilk S, Aizenman E, Porat-Katz A, Safran A, Ben-Meir A, et al. At what age can human oocytes be obtained? Fertil Steril. 2009;92:458–63.CrossRefPubMed Revel A, Revel-Vilk S, Aizenman E, Porat-Katz A, Safran A, Ben-Meir A, et al. At what age can human oocytes be obtained? Fertil Steril. 2009;92:458–63.CrossRefPubMed
3.
go back to reference Isachenko E, Rahimi G, Isachenko V, Nawroth F. In-vitro maturation of germinal-vesicle oocytes and cryopreservation in metaphase I/II: a possible additional option to preserve fertility during ovarian tissue cryopreservation. Reprod BioMed Online. 2004;8:553–7.CrossRefPubMed Isachenko E, Rahimi G, Isachenko V, Nawroth F. In-vitro maturation of germinal-vesicle oocytes and cryopreservation in metaphase I/II: a possible additional option to preserve fertility during ovarian tissue cryopreservation. Reprod BioMed Online. 2004;8:553–7.CrossRefPubMed
4.
go back to reference Huang JY, Buckett WM, Gilbert L, Tan SL, Chian RC. Retrieval of immature oocytes followed by in vitro maturation and vitrification: a case report on a new strategy of fertility preservation in women with borderline ovarian malignancy. Gynecol Oncol. 2007;105:542–4.CrossRefPubMed Huang JY, Buckett WM, Gilbert L, Tan SL, Chian RC. Retrieval of immature oocytes followed by in vitro maturation and vitrification: a case report on a new strategy of fertility preservation in women with borderline ovarian malignancy. Gynecol Oncol. 2007;105:542–4.CrossRefPubMed
5.
go back to reference Huang JY, Tulandi T, Holzer H, Lau NM, Macdonald S, Tan SL, et al. Cryopreservation of ovarian tissue and in vitro matured oocytes in a female with mosaic Turner syndrome: case report. Hum Reprod. 2008;23:336–9. Huang JY, Tulandi T, Holzer H, Lau NM, Macdonald S, Tan SL, et al. Cryopreservation of ovarian tissue and in vitro matured oocytes in a female with mosaic Turner syndrome: case report. Hum Reprod. 2008;23:336–9.
6.
go back to reference Huang JY, Tulandi T, Holzer H, Tan SL, Chian RC. Combining ovarian tissue cryobanking with retrieval of immature oocytes followed by in vitro maturation and vitrification: an additional strategy of fertility preservation. Fertil Steril. 2008;89:567–72.CrossRefPubMed Huang JY, Tulandi T, Holzer H, Tan SL, Chian RC. Combining ovarian tissue cryobanking with retrieval of immature oocytes followed by in vitro maturation and vitrification: an additional strategy of fertility preservation. Fertil Steril. 2008;89:567–72.CrossRefPubMed
7.
go back to reference Gonzalez C, Devesa M, Boada M, Coroleu B, Veiga A, Barri PN. Combined strategy for fertility preservation in an oncologic patient: vitrification of in vitro matured oocytes and ovarian tissue freezing. J Assist Reprod Genet. 2011;28:1147–9.CrossRefPubMedPubMedCentral Gonzalez C, Devesa M, Boada M, Coroleu B, Veiga A, Barri PN. Combined strategy for fertility preservation in an oncologic patient: vitrification of in vitro matured oocytes and ovarian tissue freezing. J Assist Reprod Genet. 2011;28:1147–9.CrossRefPubMedPubMedCentral
8.
go back to reference Fasano G, Moffa F, Dechène J, Englert Y, Demeestere I. Vitrification of in vitro matured oocytes collected from antral follicles at the time of ovarian tissue cryopreservation. Reprod Biol Endocrin. 2011;9:150.CrossRef Fasano G, Moffa F, Dechène J, Englert Y, Demeestere I. Vitrification of in vitro matured oocytes collected from antral follicles at the time of ovarian tissue cryopreservation. Reprod Biol Endocrin. 2011;9:150.CrossRef
9.
go back to reference Escriba MJ, Grau N, Escrich L, Novella-Maestre E, Sanchez-Serrano M. Spontaneous in vitro maturation of oocytes prior to ovarian tissue cryopreservation in natural cycles of oncologic patients. J Assist Reprod Genet. 2012;29:1261–5.CrossRefPubMedPubMedCentral Escriba MJ, Grau N, Escrich L, Novella-Maestre E, Sanchez-Serrano M. Spontaneous in vitro maturation of oocytes prior to ovarian tissue cryopreservation in natural cycles of oncologic patients. J Assist Reprod Genet. 2012;29:1261–5.CrossRefPubMedPubMedCentral
10.
go back to reference Imesch P, Scheiner D, Xie M, Fink D, Macas E, Dubey R, et al. Developmental potential of human oocytes matured in vitro followed by vitrification and activation. J Ovarian Res. 2013;6:30.CrossRefPubMedPubMedCentral Imesch P, Scheiner D, Xie M, Fink D, Macas E, Dubey R, et al. Developmental potential of human oocytes matured in vitro followed by vitrification and activation. J Ovarian Res. 2013;6:30.CrossRefPubMedPubMedCentral
11.
go back to reference Shirasawa H, Kumagai J, Sato W, Kumazawa Y, Sato N, Terada Y. Retrieval and in vitro maturation of human oocytes from ovaries removed during surgery for endometrial carcinoma: a novel strategy for human oocyte research. J Assist Reprod Genet. 2013;30:1227–30.CrossRefPubMedPubMedCentral Shirasawa H, Kumagai J, Sato W, Kumazawa Y, Sato N, Terada Y. Retrieval and in vitro maturation of human oocytes from ovaries removed during surgery for endometrial carcinoma: a novel strategy for human oocyte research. J Assist Reprod Genet. 2013;30:1227–30.CrossRefPubMedPubMedCentral
12.
go back to reference Prasath EB, Chan ML, Wong WH, Lim CJ, Tharmalingam MD, Hendricks M, et al. First pregnancy and live birth resulting from cryopreserved embryos obtained from in vitro matured oocytes after oophorectomy in an ovarian cancer patient. Hum Reprod. 2014;29:276–8.CrossRefPubMed Prasath EB, Chan ML, Wong WH, Lim CJ, Tharmalingam MD, Hendricks M, et al. First pregnancy and live birth resulting from cryopreserved embryos obtained from in vitro matured oocytes after oophorectomy in an ovarian cancer patient. Hum Reprod. 2014;29:276–8.CrossRefPubMed
13.
go back to reference Segers I, Mateizel I, Van Moer E, Smitz J, Tournaye H, Verheyem G, et al. In vitro maturation (IVM) of oocytes recovered from ovariectomy specimens in the laboratory: a promising “ex vivo” method of oocyte cryopreservation resulting in the first report of an ongoing pregnancy in Europe. J Assist Reprod Genet. 2015;32:1221–31.CrossRefPubMedPubMedCentral Segers I, Mateizel I, Van Moer E, Smitz J, Tournaye H, Verheyem G, et al. In vitro maturation (IVM) of oocytes recovered from ovariectomy specimens in the laboratory: a promising “ex vivo” method of oocyte cryopreservation resulting in the first report of an ongoing pregnancy in Europe. J Assist Reprod Genet. 2015;32:1221–31.CrossRefPubMedPubMedCentral
14.
go back to reference Uzelac PS, Delaney AA, Christensen GL, Bohler HC, Nakajima ST. Live birth following in vitro maturation of oocytes retrieved from extracorporeal ovarian tissue aspiration and embryo cryopreservation for 5 years. Fertil Steril. 2015;104:1258–60.CrossRefPubMed Uzelac PS, Delaney AA, Christensen GL, Bohler HC, Nakajima ST. Live birth following in vitro maturation of oocytes retrieved from extracorporeal ovarian tissue aspiration and embryo cryopreservation for 5 years. Fertil Steril. 2015;104:1258–60.CrossRefPubMed
15.
go back to reference Hourvitz A, Yerushalmi GM, Maman E, Raanani H, Elizur S, Brengauz M, et al. Combination of ovarian tissue harvesting and immature oocyte collection for fertility preservation increases preservation yield. Reprod BioMed Online. 2015;31:497–505.CrossRefPubMed Hourvitz A, Yerushalmi GM, Maman E, Raanani H, Elizur S, Brengauz M, et al. Combination of ovarian tissue harvesting and immature oocyte collection for fertility preservation increases preservation yield. Reprod BioMed Online. 2015;31:497–505.CrossRefPubMed
16.
go back to reference Donnez J, Dolmans MM. Ovarian cortex transplantation: 60 reported live births brings the success and worldwide expansion of the technique towards routine clinical practice. J Assist Reprod Genet. 2015;32(8):1167–70.CrossRefPubMedPubMedCentral Donnez J, Dolmans MM. Ovarian cortex transplantation: 60 reported live births brings the success and worldwide expansion of the technique towards routine clinical practice. J Assist Reprod Genet. 2015;32(8):1167–70.CrossRefPubMedPubMedCentral
17.
go back to reference Dolmans MM, Marinescu C, Saussoy P, Van Langendonckt A, Amorim C, Donnez J. Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood. 2010;116:2908–14.CrossRefPubMed Dolmans MM, Marinescu C, Saussoy P, Van Langendonckt A, Amorim C, Donnez J. Reimplantation of cryopreserved ovarian tissue from patients with acute lymphoblastic leukemia is potentially unsafe. Blood. 2010;116:2908–14.CrossRefPubMed
18.
go back to reference Rosendahl M, Greve T, Andersen CY. The safety of transplanting cryopreserved ovarian tissue in cancer patients: a review of the literature. J Assist Reprod Genet. 2013;30:11–24.CrossRefPubMed Rosendahl M, Greve T, Andersen CY. The safety of transplanting cryopreserved ovarian tissue in cancer patients: a review of the literature. J Assist Reprod Genet. 2013;30:11–24.CrossRefPubMed
19.
go back to reference Bastings L, Beerendonk CC, Westphal JR, Massuger LF, Kaal SE, van Leeuwen FE, et al. Autotransplantation of cryopreserved ovarian tissue in cancer survivors and the risk of reintroducing malignancy: a systematic review. Hum Reprod Update. 2013;19:483–506.CrossRefPubMed Bastings L, Beerendonk CC, Westphal JR, Massuger LF, Kaal SE, van Leeuwen FE, et al. Autotransplantation of cryopreserved ovarian tissue in cancer survivors and the risk of reintroducing malignancy: a systematic review. Hum Reprod Update. 2013;19:483–506.CrossRefPubMed
20.
go back to reference Shirasawa H, Kumazawa Y, Sato W, Ono N, Terada Y. In vitro maturation and cryopreservation of oocytes retrieved from intra-operative aspiration during second enucleation for ovarian tumor: a case report. Gynecol Oncol Rep. 2016;19:1–4.PubMedPubMedCentral Shirasawa H, Kumazawa Y, Sato W, Ono N, Terada Y. In vitro maturation and cryopreservation of oocytes retrieved from intra-operative aspiration during second enucleation for ovarian tumor: a case report. Gynecol Oncol Rep. 2016;19:1–4.PubMedPubMedCentral
21.
go back to reference Wilken-Jensen HN, Kristensen SG, Jeppesen JV, Yding AC. Developmental competence of oocytes isolated from surplus medulla tissue in connection with cryopreservation of ovarian tissue for fertility preservation. Acta Obstet Gynecol Scand. 2014;93:32–7.CrossRefPubMed Wilken-Jensen HN, Kristensen SG, Jeppesen JV, Yding AC. Developmental competence of oocytes isolated from surplus medulla tissue in connection with cryopreservation of ovarian tissue for fertility preservation. Acta Obstet Gynecol Scand. 2014;93:32–7.CrossRefPubMed
22.
go back to reference Yin H, Jiang H, Kristensen SG, Andersen CY. Vitrification of in vitro matured oocytes collected from surplus ovarian medulla tissue resulting from fertility preservation of ovarian cortex tissue. J Assist Reprod Genet. 2016;33:741–6.CrossRefPubMedPubMedCentral Yin H, Jiang H, Kristensen SG, Andersen CY. Vitrification of in vitro matured oocytes collected from surplus ovarian medulla tissue resulting from fertility preservation of ovarian cortex tissue. J Assist Reprod Genet. 2016;33:741–6.CrossRefPubMedPubMedCentral
23.
go back to reference Kundsin RB, Falk L, Hertig AT, Horne HW Jr. Mycoplasma, chlamydia, Epstein-Barr, herpes I and II, and AIDS infections among 100 consecutive infertile female patients and husbands: diagnosis, treatment, and results. Int J Fertil. 1986;31:356–9.PubMed Kundsin RB, Falk L, Hertig AT, Horne HW Jr. Mycoplasma, chlamydia, Epstein-Barr, herpes I and II, and AIDS infections among 100 consecutive infertile female patients and husbands: diagnosis, treatment, and results. Int J Fertil. 1986;31:356–9.PubMed
24.
go back to reference Thomas D, Michou V, Moustakarias T, Aleporou V, Matzavinos T, Mitsakos-Barbagiannis K, et al. Altered immunophenotypic parameters in infertile women. Possible role of herpes viremia. Am J Reprod Immunol. 2005;54:101–11.CrossRefPubMed Thomas D, Michou V, Moustakarias T, Aleporou V, Matzavinos T, Mitsakos-Barbagiannis K, et al. Altered immunophenotypic parameters in infertile women. Possible role of herpes viremia. Am J Reprod Immunol. 2005;54:101–11.CrossRefPubMed
25.
go back to reference Zhai J, Yao G, Dong F, Bu Z, Cheng Y, Sato Y, et al. In vitro activation of follicles and fresh tissue auto-transplantation in primary ovarian insufficiency patients. J Clin Endocrinol Metab. 2016;101:4405–12.CrossRefPubMedPubMedCentral Zhai J, Yao G, Dong F, Bu Z, Cheng Y, Sato Y, et al. In vitro activation of follicles and fresh tissue auto-transplantation in primary ovarian insufficiency patients. J Clin Endocrinol Metab. 2016;101:4405–12.CrossRefPubMedPubMedCentral
26.
go back to reference Woad KJ, Watkins WJ, Prendergast D, Shelling AN. The genetic basis of premature ovarian failure. Aust N Z J Obstet Gynaecol. 2006;46:242–4.CrossRefPubMed Woad KJ, Watkins WJ, Prendergast D, Shelling AN. The genetic basis of premature ovarian failure. Aust N Z J Obstet Gynaecol. 2006;46:242–4.CrossRefPubMed
27.
go back to reference Van Kasteren Y, Schoemaker J. Premature ovarian failure: a systematic review on therapeutic interventions to restore ovarian function and achieve pregnancy. Hum Reprod Update. 1999;5:483–92.CrossRefPubMed Van Kasteren Y, Schoemaker J. Premature ovarian failure: a systematic review on therapeutic interventions to restore ovarian function and achieve pregnancy. Hum Reprod Update. 1999;5:483–92.CrossRefPubMed
28.
29.
go back to reference Dittfeld A, Gwizdek K, Michalski M, Wojnicz R. A possible link between the Epstein-Barr virus infection and autoimmune thyroid disorders. Cent Eur J Immunol. 2016;41:297–301.CrossRefPubMedPubMedCentral Dittfeld A, Gwizdek K, Michalski M, Wojnicz R. A possible link between the Epstein-Barr virus infection and autoimmune thyroid disorders. Cent Eur J Immunol. 2016;41:297–301.CrossRefPubMedPubMedCentral
30.
go back to reference Reato G, Morlin L, Chen S, Furmaniak J, Rees Smith B, Masiero S, et al. Premature ovarian failure in patients with autoimmune Addison's disease: clinical, genetic, and immunological evaluation. J Clin Endocrinol Metab. 2011;96:E1255–61.CrossRefPubMed Reato G, Morlin L, Chen S, Furmaniak J, Rees Smith B, Masiero S, et al. Premature ovarian failure in patients with autoimmune Addison's disease: clinical, genetic, and immunological evaluation. J Clin Endocrinol Metab. 2011;96:E1255–61.CrossRefPubMed
33.
go back to reference Hassan HA. 2001. Cumulus cell contribution to cytoplasmic maturation and oocyte developmental competence in vitro. J Assist Reprod Genet. 2001;18:539–43.CrossRefPubMedPubMedCentral Hassan HA. 2001. Cumulus cell contribution to cytoplasmic maturation and oocyte developmental competence in vitro. J Assist Reprod Genet. 2001;18:539–43.CrossRefPubMedPubMedCentral
Metadata
Title
In vitro maturation of oocytes from excised ovarian tissue in a patient with autoimmune ovarian insufficiency possibly associated with Epstein-Barr virus infection
Authors
Irma Virant-Klun
Andrej Vogler
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2018
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-018-0350-1

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