Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 10/2023

Open Access 11-08-2023 | Turner's Syndrome | Fertility Preservation

Clinical pregnancy in Turner syndrome following re-implantation of cryopreserved ovarian cortex

Authors: CE Dunlop, SA Jack, EE Telfer, S. Zahra, RA Anderson

Published in: Journal of Assisted Reproduction and Genetics | Issue 10/2023

Login to get access

Abstract

Turner syndrome (TS) leads to a characteristic phenotype, including premature ovarian insufficiency and infertility. Ovarian tissue cryopreservation (OTC) is becoming an established fertility preservation strategy for both pre- and post-pubertal females and may offer the chance of having a biological family to selected patients with TS. To date, women with TS have had ovarian tissue cryopreserved but there are few reports of autologous re-implantation and none of pregnancy. We herein report, to our knowledge, the first clinical pregnancy in a patient with TS, conceived naturally following re-implantation of cryopreserved ovarian tissue which had been removed soon after spontaneous puberty. This provides proof of concept for OTC as a means of fertility preservation in TS.
Literature
1.
go back to reference Gravholt CH, Viuff M, Just J, Sandahl K, Brun S, van der Velden J, et al. The changing face of Turner Syndrome. Endocr Rev. 2023;44:33–69.CrossRefPubMed Gravholt CH, Viuff M, Just J, Sandahl K, Brun S, van der Velden J, et al. The changing face of Turner Syndrome. Endocr Rev. 2023;44:33–69.CrossRefPubMed
2.
go back to reference Gravholt CH, Andersen NH, Conway GS, Dekkers OM, Geffner ME, Klein KO, et al. Clinical practice guidelines for the care of girls and women with Turner syndrome: proceedings from the 2016 Cincinnati International Turner Syndrome Meeting. Eur J Endocrinol. 2017;177:G1–G70.CrossRefPubMed Gravholt CH, Andersen NH, Conway GS, Dekkers OM, Geffner ME, Klein KO, et al. Clinical practice guidelines for the care of girls and women with Turner syndrome: proceedings from the 2016 Cincinnati International Turner Syndrome Meeting. Eur J Endocrinol. 2017;177:G1–G70.CrossRefPubMed
3.
go back to reference Mercer CL, Lachlan K, Karcanias A, Affara N, Huang S, Jacobs PA, et al. Detailed clinical and molecular study of 20 females with Xq deletions with special reference to menstruation and fertility. Eur J Med Genet. 2013;56:1–6.CrossRefPubMed Mercer CL, Lachlan K, Karcanias A, Affara N, Huang S, Jacobs PA, et al. Detailed clinical and molecular study of 20 females with Xq deletions with special reference to menstruation and fertility. Eur J Med Genet. 2013;56:1–6.CrossRefPubMed
4.
go back to reference Modi DN, Sane S, Bhartiya D. Accelerated germ cell apoptosis in sex chromosome aneuploid fetal human gonads. Mol Hum Reprod. 2003;9:219–25.CrossRefPubMed Modi DN, Sane S, Bhartiya D. Accelerated germ cell apoptosis in sex chromosome aneuploid fetal human gonads. Mol Hum Reprod. 2003;9:219–25.CrossRefPubMed
5.
go back to reference Reynaud K, Cortvrindt R, Verlinde F, De Schepper J, Bourgain C, Smitz J. Number of ovarian follicles in human fetuses with the 45 X karyotype. Fertil Steril. 2004;81:1112–9.CrossRefPubMed Reynaud K, Cortvrindt R, Verlinde F, De Schepper J, Bourgain C, Smitz J. Number of ovarian follicles in human fetuses with the 45 X karyotype. Fertil Steril. 2004;81:1112–9.CrossRefPubMed
6.
go back to reference Bernard V, Donadille B, Zenaty D, Courtillot C, Salenave S, Brac de la Perriere A, et al. Spontaneous fertility and pregnancy outcomes amongst 480 women with Turner syndrome. Hum Reprod. 2016;31:782–8.CrossRefPubMed Bernard V, Donadille B, Zenaty D, Courtillot C, Salenave S, Brac de la Perriere A, et al. Spontaneous fertility and pregnancy outcomes amongst 480 women with Turner syndrome. Hum Reprod. 2016;31:782–8.CrossRefPubMed
7.
go back to reference Pasquino AM, Passeri F, Pucarelli I, Segni M, Municchi G. Spontaneous pubertal development in Turner's syndrome. Italian Study Group for Turner's Syndrome. J Clin Endocrinol Metab. 1997;82:1810–3.PubMed Pasquino AM, Passeri F, Pucarelli I, Segni M, Municchi G. Spontaneous pubertal development in Turner's syndrome. Italian Study Group for Turner's Syndrome. J Clin Endocrinol Metab. 1997;82:1810–3.PubMed
8.
go back to reference Tanaka T, Igarashi Y, Ozono K, Ohyama K, Ogawa M, Osada H, et al. Frequencies of spontaneous breast development and spontaneous menarche in Turner syndrome in Japan. Clin Pediatr Endocrinol. 2015;24:167–73.CrossRefPubMedPubMedCentral Tanaka T, Igarashi Y, Ozono K, Ohyama K, Ogawa M, Osada H, et al. Frequencies of spontaneous breast development and spontaneous menarche in Turner syndrome in Japan. Clin Pediatr Endocrinol. 2015;24:167–73.CrossRefPubMedPubMedCentral
9.
go back to reference Schleedoorn MJ, Mulder BH, Braat DDM, Beerendonk CCM, Peek R, Nelen W, et al. International consensus: ovarian tissue cryopreservation in young Turner syndrome patients: outcomes of an ethical Delphi study including 55 experts from 16 different countries. Hum Reprod. 2020;35:1061–72.CrossRefPubMedPubMedCentral Schleedoorn MJ, Mulder BH, Braat DDM, Beerendonk CCM, Peek R, Nelen W, et al. International consensus: ovarian tissue cryopreservation in young Turner syndrome patients: outcomes of an ethical Delphi study including 55 experts from 16 different countries. Hum Reprod. 2020;35:1061–72.CrossRefPubMedPubMedCentral
10.
go back to reference ESHRE Guideline Group on Female Fertility Preservation, Anderson RA, Amant F, Braat D, D'Angelo A, de Sousa C, Lopes SM, et al. ESHRE guideline: female fertility preservation. Hum Reprod Open. 2020;2020:hoaa052.CrossRef ESHRE Guideline Group on Female Fertility Preservation, Anderson RA, Amant F, Braat D, D'Angelo A, de Sousa C, Lopes SM, et al. ESHRE guideline: female fertility preservation. Hum Reprod Open. 2020;2020:hoaa052.CrossRef
11.
go back to reference Oktay K, Bedoschi G, Berkowitz K, Bronson R, Kashani B, McGovern P, et al. Fertility Preservation in Women with Turner Syndrome: A Comprehensive Review and Practical Guidelines. J Pediatr Adolesc Gynecol. 2016;29:409–16.CrossRefPubMed Oktay K, Bedoschi G, Berkowitz K, Bronson R, Kashani B, McGovern P, et al. Fertility Preservation in Women with Turner Syndrome: A Comprehensive Review and Practical Guidelines. J Pediatr Adolesc Gynecol. 2016;29:409–16.CrossRefPubMed
12.
go back to reference Talaulikar VS, Conway GS, Pimblett A, Davies MC. Outcome of ovarian stimulation for oocyte cryopreservation in women with Turner syndrome. Fertil Steril. 2019;111:505–9.CrossRefPubMed Talaulikar VS, Conway GS, Pimblett A, Davies MC. Outcome of ovarian stimulation for oocyte cryopreservation in women with Turner syndrome. Fertil Steril. 2019;111:505–9.CrossRefPubMed
13.
go back to reference Nadesapillai S, van der Coelen S, Goebel L, Peek R, Braat DD, van der Velden JA, et al. Deciding on future fertility: considerations of girls with Turner syndrome and their parents to opt for or against ovarian tissue cryopreservation. Reprod Biomed Online. 2023. Nadesapillai S, van der Coelen S, Goebel L, Peek R, Braat DD, van der Velden JA, et al. Deciding on future fertility: considerations of girls with Turner syndrome and their parents to opt for or against ovarian tissue cryopreservation. Reprod Biomed Online. 2023.
14.
go back to reference Donnez J, Dolmans MM, Squifflet J, Kerbrat G, Jadoul P. Live birth after allografting of ovarian cortex between monozygotic twins with Turner syndrome (45,XO/46,XX mosaicism) and discordant ovarian function. Fertil Steril. 2011;96:1407–11.CrossRefPubMed Donnez J, Dolmans MM, Squifflet J, Kerbrat G, Jadoul P. Live birth after allografting of ovarian cortex between monozygotic twins with Turner syndrome (45,XO/46,XX mosaicism) and discordant ovarian function. Fertil Steril. 2011;96:1407–11.CrossRefPubMed
15.
go back to reference Gosden RG, Baird DT, Wade JC, Webb R. Restoration of fertility to oophorectomized sheep by ovarian autografts stored at -196oC. Human Reprod. 1994;9:597–603.CrossRef Gosden RG, Baird DT, Wade JC, Webb R. Restoration of fertility to oophorectomized sheep by ovarian autografts stored at -196oC. Human Reprod. 1994;9:597–603.CrossRef
16.
go back to reference Mamsen LS, Charkiewicz K, Anderson RA, Telfer EE, McLaughlin M, Kelsey TW, et al. Characterization of follicles in girls and young women with Turner syndrome who underwent ovarian tissue cryopreservation. Fertil Steril. 2019;111(1217-25):e3. Mamsen LS, Charkiewicz K, Anderson RA, Telfer EE, McLaughlin M, Kelsey TW, et al. Characterization of follicles in girls and young women with Turner syndrome who underwent ovarian tissue cryopreservation. Fertil Steril. 2019;111(1217-25):e3.
17.
go back to reference Rodriguez-Wallberg KA, Sergouniotis F, Nilsson HP, Lundberg FE. Trends and outcomes of fertility preservation for girls, adolescents and young adults with Turner syndrome: A prospective cohort study. Front Endocrinol (Lausanne). 2023;14:1135249.CrossRefPubMedPubMedCentral Rodriguez-Wallberg KA, Sergouniotis F, Nilsson HP, Lundberg FE. Trends and outcomes of fertility preservation for girls, adolescents and young adults with Turner syndrome: A prospective cohort study. Front Endocrinol (Lausanne). 2023;14:1135249.CrossRefPubMedPubMedCentral
18.
go back to reference Schleedoorn M, van der Velden J, Braat D, Beerendonk I, van Golde R, Peek R, et al. TurnerFertility trial: PROTOCOL for an observational cohort study to describe the efficacy of ovarian tissue cryopreservation for fertility preservation in females with Turner syndrome. BMJ Open. 2019;9:e030855.CrossRefPubMedPubMedCentral Schleedoorn M, van der Velden J, Braat D, Beerendonk I, van Golde R, Peek R, et al. TurnerFertility trial: PROTOCOL for an observational cohort study to describe the efficacy of ovarian tissue cryopreservation for fertility preservation in females with Turner syndrome. BMJ Open. 2019;9:e030855.CrossRefPubMedPubMedCentral
19.
go back to reference Borgstrom B, Hreinsson J, Rasmussen C, Sheikhi M, Fried G, Keros V, et al. Fertility preservation in girls with turner syndrome: prognostic signs of the presence of ovarian follicles. J Clin Endocrinol Metab. 2009;94:74–80.CrossRefPubMed Borgstrom B, Hreinsson J, Rasmussen C, Sheikhi M, Fried G, Keros V, et al. Fertility preservation in girls with turner syndrome: prognostic signs of the presence of ovarian follicles. J Clin Endocrinol Metab. 2009;94:74–80.CrossRefPubMed
20.
go back to reference Peek R, Schleedoorn M, Smeets D, van de Zande G, Groenman F, Braat D, et al. Ovarian follicles of young patients with Turner's syndrome contain normal oocytes but monosomic 45. X granulosa cells. Hum Reprod. 2019;34:1686–96.PubMed Peek R, Schleedoorn M, Smeets D, van de Zande G, Groenman F, Braat D, et al. Ovarian follicles of young patients with Turner's syndrome contain normal oocytes but monosomic 45. X granulosa cells. Hum Reprod. 2019;34:1686–96.PubMed
21.
go back to reference Balen AH, Harris SE, Chambers EL, Picton HM. Conservation of fertility and oocyte genetics in a young woman with mosaic Turner syndrome. BJOG. 2010;117:238–42.CrossRefPubMed Balen AH, Harris SE, Chambers EL, Picton HM. Conservation of fertility and oocyte genetics in a young woman with mosaic Turner syndrome. BJOG. 2010;117:238–42.CrossRefPubMed
22.
go back to reference Schleedoorn MJ, Fleischer K, Braat D, Oerlemans A, van der Velden A, Peek R. Why Turner patients with 45, X monosomy should not be excluded from fertility preservation services. Reprod Biol Endocrinol. 2022;20:143.CrossRefPubMedPubMedCentral Schleedoorn MJ, Fleischer K, Braat D, Oerlemans A, van der Velden A, Peek R. Why Turner patients with 45, X monosomy should not be excluded from fertility preservation services. Reprod Biol Endocrinol. 2022;20:143.CrossRefPubMedPubMedCentral
23.
go back to reference Dolmans MM, von Wolff M, Poirot C, Diaz-Garcia C, Cacciottola L, Boissel N, et al. Transplantation of cryopreserved ovarian tissue in a series of 285 women: a review of five leading European centers. Fertil Steril. 2021;115:1102–15.CrossRefPubMed Dolmans MM, von Wolff M, Poirot C, Diaz-Garcia C, Cacciottola L, Boissel N, et al. Transplantation of cryopreserved ovarian tissue in a series of 285 women: a review of five leading European centers. Fertil Steril. 2021;115:1102–15.CrossRefPubMed
24.
go back to reference Dunlop CE, Brady BM, McLaughlin M, Telfer EE, White J, Cowie F, et al. Re-implantation of cryopreserved ovarian cortex resulting in restoration of ovarian function, natural conception and successful pregnancy after haematopoietic stem cell transplantation for Wilms tumour. J Assist Reprod Genet. 2016;33:1615–20.CrossRefPubMedPubMedCentral Dunlop CE, Brady BM, McLaughlin M, Telfer EE, White J, Cowie F, et al. Re-implantation of cryopreserved ovarian cortex resulting in restoration of ovarian function, natural conception and successful pregnancy after haematopoietic stem cell transplantation for Wilms tumour. J Assist Reprod Genet. 2016;33:1615–20.CrossRefPubMedPubMedCentral
25.
go back to reference Demeestere I, Simon P, Dedeken L, Moffa F, Tsepelidis S, Brachet C, et al. Live birth after autograft of ovarian tissue cryopreserved during childhood. Hum Reprod. 2015;30:2107–9.CrossRefPubMed Demeestere I, Simon P, Dedeken L, Moffa F, Tsepelidis S, Brachet C, et al. Live birth after autograft of ovarian tissue cryopreserved during childhood. Hum Reprod. 2015;30:2107–9.CrossRefPubMed
26.
go back to reference Bryman I, Sylven L, Berntorp K, Innala E, Bergstrom I, Hanson C, et al. Pregnancy rate and outcome in Swedish women with Turner syndrome. Fertil Steril. 2011;95:2507–10.CrossRefPubMed Bryman I, Sylven L, Berntorp K, Innala E, Bergstrom I, Hanson C, et al. Pregnancy rate and outcome in Swedish women with Turner syndrome. Fertil Steril. 2011;95:2507–10.CrossRefPubMed
27.
go back to reference Hagman A, Kallen K, Barrenas ML, Landin-Wilhelmsen K, Hanson C, Bryman I, et al. Obstetric outcomes in women with Turner karyotype. J Clin Endocrinol Metab. 2011;96:3475–82.CrossRefPubMed Hagman A, Kallen K, Barrenas ML, Landin-Wilhelmsen K, Hanson C, Bryman I, et al. Obstetric outcomes in women with Turner karyotype. J Clin Endocrinol Metab. 2011;96:3475–82.CrossRefPubMed
28.
go back to reference Chevalier N, Letur H, Lelannou D, Ohl J, Cornet D, Chalas-Boissonnas C, et al. Materno-fetal cardiovascular complications in Turner syndrome after oocyte donation: insufficient prepregnancy screening and pregnancy follow-up are associated with poor outcome. J Clin Endocrinol Metab. 2011;96:E260–7.CrossRefPubMed Chevalier N, Letur H, Lelannou D, Ohl J, Cornet D, Chalas-Boissonnas C, et al. Materno-fetal cardiovascular complications in Turner syndrome after oocyte donation: insufficient prepregnancy screening and pregnancy follow-up are associated with poor outcome. J Clin Endocrinol Metab. 2011;96:E260–7.CrossRefPubMed
29.
go back to reference Tarani L, Lampariello S, Raguso G, Colloridi F, Pucarelli I, Pasquino AM, et al. Pregnancy in patients with Turner's syndrome: six new cases and review of literature. Gynecol Endocrinol. 1998;12:83–7.CrossRefPubMed Tarani L, Lampariello S, Raguso G, Colloridi F, Pucarelli I, Pasquino AM, et al. Pregnancy in patients with Turner's syndrome: six new cases and review of literature. Gynecol Endocrinol. 1998;12:83–7.CrossRefPubMed
30.
go back to reference Hadnott TN, Gould HN, Gharib AM, Bondy CA. Outcomes of spontaneous and assisted pregnancies in Turner syndrome: the U.S. National Institutes of Health experience. Fertil Steril. 2011;95:2251–6.CrossRefPubMedPubMedCentral Hadnott TN, Gould HN, Gharib AM, Bondy CA. Outcomes of spontaneous and assisted pregnancies in Turner syndrome: the U.S. National Institutes of Health experience. Fertil Steril. 2011;95:2251–6.CrossRefPubMedPubMedCentral
31.
go back to reference Mamsen LS, Kelsey TW, Ernst E, Macklon KT, Lund AM, Andersen CY. Cryopreservation of ovarian tissue may be considered in young girls with galactosemia. J Assist Reprod Genet. 2018;35:1209–17.CrossRefPubMedPubMedCentral Mamsen LS, Kelsey TW, Ernst E, Macklon KT, Lund AM, Andersen CY. Cryopreservation of ovarian tissue may be considered in young girls with galactosemia. J Assist Reprod Genet. 2018;35:1209–17.CrossRefPubMedPubMedCentral
32.
go back to reference Grynberg M, Bidet M, Benard J, Poulain M, Sonigo C, Cedrin-Durnerin I, et al. Fertility preservation in Turner syndrome. Fertil Steril. 2016;105:13–9.CrossRefPubMed Grynberg M, Bidet M, Benard J, Poulain M, Sonigo C, Cedrin-Durnerin I, et al. Fertility preservation in Turner syndrome. Fertil Steril. 2016;105:13–9.CrossRefPubMed
Metadata
Title
Clinical pregnancy in Turner syndrome following re-implantation of cryopreserved ovarian cortex
Authors
CE Dunlop
SA Jack
EE Telfer
S. Zahra
RA Anderson
Publication date
11-08-2023
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 10/2023
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-023-02905-w

Other articles of this Issue 10/2023

Journal of Assisted Reproduction and Genetics 10/2023 Go to the issue