Skip to main content
Top
Published in: Journal of Assisted Reproduction and Genetics 10/2020

01-10-2020 | Fertility | Fertility Preservation

Ovarian stimulation outcomes among transgender men compared with fertile cisgender women

Authors: Hadar Amir, Iris Yaish, Nivin Samara, Joseph Hasson, Asnat Groutz, Foad Azem

Published in: Journal of Assisted Reproduction and Genetics | Issue 10/2020

Login to get access

Abstract

Purpose

To compare assisted reproductive technology (ART) outcomes among transgender men with those of fertile cisgender women.

Methods

This retrospective cohort study included 12 transgender men, six with no testosterone exposure and six after testosterone treatment, and 12 cisgender women (oocyte donors) who underwent ART in our institution between June 2017 and December 2019. Statistical analyses compared ART data and outcomes between three groups: cisgender women, transgender men without testosterone exposure, and transgender men after testosterone exposure. Comparisons were also made between transgender men with and without testosterone exposure.

Results

The transgender men with no testosterone exposure (23.3 ± 4 years) were significantly younger than the transgender men who had undergone testosterone treatment (30.3 ± 3.8 years; P = 0.012) and the cisgender women (29.1 ± 3.1 years; P = 0.004). The amount of FSH used for ovulation induction (1999 ± 683 mIU/mL) was significantly lower among transgender men without prior testosterone exposure compared with that among cisgender women (3150 ± 487 mIU/mL; P = 0.007). There were no differences in the peak estradiol levels, the number of oocytes retrieved, the number of MII oocytes, and the oocyte maturity rates between the three groups. Five out of six testosterone-treated transgender men underwent embryo cryopreservation, and they all achieved good-quality embryos.

Conclusions

Transgender men have an excellent response to ovulation stimulation even after long-term exposure to testosterone. Oocyte/embryo cryopreservation is, therefore, a feasible and effective way for them to preserve their fertility for future biological parenting.
Literature
1.
go back to reference Condorelli M, Demeestere I. Challenges of fertility preservation in non-oncological disease. Acta Obstet Gynecol Scand. 2019;98:638–46.CrossRef Condorelli M, Demeestere I. Challenges of fertility preservation in non-oncological disease. Acta Obstet Gynecol Scand. 2019;98:638–46.CrossRef
2.
go back to reference Del-Pozo-Lérida S, Salvador C, Martínez-Soler F, Tortosa A, Perucho M, Giménez-Bonafé P. Preservation of fertility in patients with cancer (Review). Oncol Rep. 2019;41:2607–14.PubMed Del-Pozo-Lérida S, Salvador C, Martínez-Soler F, Tortosa A, Perucho M, Giménez-Bonafé P. Preservation of fertility in patients with cancer (Review). Oncol Rep. 2019;41:2607–14.PubMed
3.
go back to reference Alteri A, Pisaturo V, Nogueira D, D’Angelo A. Elective egg freezing without medical indications. Acta Obstet Gynecol Scand. 2019;98:647–52.CrossRef Alteri A, Pisaturo V, Nogueira D, D’Angelo A. Elective egg freezing without medical indications. Acta Obstet Gynecol Scand. 2019;98:647–52.CrossRef
4.
go back to reference Jones CA, Reiter L, Greenblatt E. Fertility preservation in transgender patients. Int J Transgend. 2016;17:76–82.CrossRef Jones CA, Reiter L, Greenblatt E. Fertility preservation in transgender patients. Int J Transgend. 2016;17:76–82.CrossRef
5.
go back to reference Chen D, Simons L, Johnson EK, Lockart BA, Finlayson C. Fertility preservation for transgender adolescents. J Adolesc Health. 2017;61:120–3.CrossRef Chen D, Simons L, Johnson EK, Lockart BA, Finlayson C. Fertility preservation for transgender adolescents. J Adolesc Health. 2017;61:120–3.CrossRef
6.
go back to reference Nahata L, Tishelman AC, Caltabellotta NM, Quinn GP. Low fertility preservation utilization among transgender youth. J Adolesc Health. 2017;61:40–4.CrossRef Nahata L, Tishelman AC, Caltabellotta NM, Quinn GP. Low fertility preservation utilization among transgender youth. J Adolesc Health. 2017;61:40–4.CrossRef
7.
go back to reference Coleman E, Bockting W, Botzer M, Cohen-Kettenis P, DeCuypere G, Feldman J, et al. Standards of care for the health of transsexual, transgender, and gender-nonconforming people, version 7. Int J Transgend. 2012;13:165–232.CrossRef Coleman E, Bockting W, Botzer M, Cohen-Kettenis P, DeCuypere G, Feldman J, et al. Standards of care for the health of transsexual, transgender, and gender-nonconforming people, version 7. Int J Transgend. 2012;13:165–232.CrossRef
8.
go back to reference Van Den Broecke R, Van Der Elst J, Liu J, Hovatta O, Dhont M. The female-to-male transsexual patient: a source of human ovarian cortical tissue for experimental use. Hum Reprod. 2001 Jan;16:145–7.CrossRef Van Den Broecke R, Van Der Elst J, Liu J, Hovatta O, Dhont M. The female-to-male transsexual patient: a source of human ovarian cortical tissue for experimental use. Hum Reprod. 2001 Jan;16:145–7.CrossRef
9.
go back to reference De Roo C, Lierman S, Tilleman K, Peynshaert K, Braeckmans K, Caanen M, et al. Ovarian tissue cryopreservation in female-to-male transgender people: insights into ovarian histology and physiology after prolonged androgen treatment. Reprod BioMed Online. 2017;34:557–66.CrossRef De Roo C, Lierman S, Tilleman K, Peynshaert K, Braeckmans K, Caanen M, et al. Ovarian tissue cryopreservation in female-to-male transgender people: insights into ovarian histology and physiology after prolonged androgen treatment. Reprod BioMed Online. 2017;34:557–66.CrossRef
10.
go back to reference Lierman S, Tilleman K, Braeckmans K, Peynshaert K, Weyers S, T’Sjoen G, et al. Fertility preservation for trans men: frozen-thawed in vitro matured oocytes collected at the time of ovarian tissue processing exhibit normal meiotic spindles. J Assist Reprod Genet. 2017;34:1449–56.CrossRef Lierman S, Tilleman K, Braeckmans K, Peynshaert K, Weyers S, T’Sjoen G, et al. Fertility preservation for trans men: frozen-thawed in vitro matured oocytes collected at the time of ovarian tissue processing exhibit normal meiotic spindles. J Assist Reprod Genet. 2017;34:1449–56.CrossRef
11.
go back to reference Futterweit W, Deligdisch L. Histopathological effects of exogenously administered testosterone in 19 female to male transsexuals. J Clin Endocrinol Metab. 1986;62:16–21.CrossRef Futterweit W, Deligdisch L. Histopathological effects of exogenously administered testosterone in 19 female to male transsexuals. J Clin Endocrinol Metab. 1986;62:16–21.CrossRef
12.
go back to reference Spinder T, Spijkstra JJ, van den Tweel JG, Burger CW, van Kessel H, Hompes PG, et al. The effects of long term testosterone administration on pulsatile luteinizing hormone secretion and on ovarian histology in eugonadal female to male transsexual subjects. J Clin Endocrinol Metab. 1989;69:151–7.CrossRef Spinder T, Spijkstra JJ, van den Tweel JG, Burger CW, van Kessel H, Hompes PG, et al. The effects of long term testosterone administration on pulsatile luteinizing hormone secretion and on ovarian histology in eugonadal female to male transsexual subjects. J Clin Endocrinol Metab. 1989;69:151–7.CrossRef
13.
go back to reference Pache TD, Chadha S, Gooren LJ, Hop WC, Jaarsma KW, Dommerholt HB, et al. Ovarian morphology in long-term androgen-treated female to male transsexuals. A human model for the study of polycystic ovarian syndrome? Histopathology. 1991;19:445–52.CrossRef Pache TD, Chadha S, Gooren LJ, Hop WC, Jaarsma KW, Dommerholt HB, et al. Ovarian morphology in long-term androgen-treated female to male transsexuals. A human model for the study of polycystic ovarian syndrome? Histopathology. 1991;19:445–52.CrossRef
14.
go back to reference Loverro G, Resta L, Dellino M, Edoardo DN, Cascarano MA, Loverro M, et al. Uterine and ovarian changes during testosterone administration in young female-to-male transsexuals. Taiwan J Obstet Gynecol. 2016;55:686–91.CrossRef Loverro G, Resta L, Dellino M, Edoardo DN, Cascarano MA, Loverro M, et al. Uterine and ovarian changes during testosterone administration in young female-to-male transsexuals. Taiwan J Obstet Gynecol. 2016;55:686–91.CrossRef
15.
go back to reference Ikeda K, Baba T, Noguchi H, Nagasawa K, Endo T, Kiya T, et al. Excessive androgen exposure in female-to-male transsexual persons of reproductive age induces hyperplasia of the ovarian cortex and stroma but not polycystic ovary morphology. Hum Reprod. 2013;28:453–61.CrossRef Ikeda K, Baba T, Noguchi H, Nagasawa K, Endo T, Kiya T, et al. Excessive androgen exposure in female-to-male transsexual persons of reproductive age induces hyperplasia of the ovarian cortex and stroma but not polycystic ovary morphology. Hum Reprod. 2013;28:453–61.CrossRef
16.
go back to reference Iwase A, Osuka S, Goto M, Murase T, Nakamura T, Takikawa S, et al. Clinical application of serum anti-Müllerian hormone as an ovarian reserve marker: a review of recent studies. J Obstet Gynaecol Res. 2018;44:998–1006.CrossRef Iwase A, Osuka S, Goto M, Murase T, Nakamura T, Takikawa S, et al. Clinical application of serum anti-Müllerian hormone as an ovarian reserve marker: a review of recent studies. J Obstet Gynaecol Res. 2018;44:998–1006.CrossRef
17.
go back to reference Caanen MR, Soleman RS, Kuijper EA, Kreukels BP, De Roo C, Tilleman K, et al. Anti-Müllerian hormone levels decrease in female-to-male transsexuals using testosterone as cross-sex therapy. Fertil Steril. 2015;103:1340–5.CrossRef Caanen MR, Soleman RS, Kuijper EA, Kreukels BP, De Roo C, Tilleman K, et al. Anti-Müllerian hormone levels decrease in female-to-male transsexuals using testosterone as cross-sex therapy. Fertil Steril. 2015;103:1340–5.CrossRef
18.
go back to reference Deutsch MB, Feldman JL. Updated recommendations from the world professional association for transgender health standards of care. Am Fam Physician. 2013;87:89–93.PubMed Deutsch MB, Feldman JL. Updated recommendations from the world professional association for transgender health standards of care. Am Fam Physician. 2013;87:89–93.PubMed
19.
go back to reference Hembree WC, Cohen-Kettenis PT, Gooren L, Hannema SE, Meyer WJ, Murad MH, et al. Endocrine treatment of gender-dysphoric/gender-incongruent persons: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2017;102:3869–903.CrossRef Hembree WC, Cohen-Kettenis PT, Gooren L, Hannema SE, Meyer WJ, Murad MH, et al. Endocrine treatment of gender-dysphoric/gender-incongruent persons: an Endocrine Society clinical practice guideline. J Clin Endocrinol Metab. 2017;102:3869–903.CrossRef
20.
go back to reference Ethics Committee of the American Society for Reproductive Medicine. Access to fertility services by transgender persons: an Ethics Committee opinion. Fertil Steril. 2015;104:1111–5.CrossRef Ethics Committee of the American Society for Reproductive Medicine. Access to fertility services by transgender persons: an Ethics Committee opinion. Fertil Steril. 2015;104:1111–5.CrossRef
21.
go back to reference De Wert G, Dondorp W, Shenfield F, Barri DP, Diedrich K, et al. ESHRE Task Force on Ethics and Law 23: medically assisted reproduction in singles, lesbian and gay couples, and transsexual people. Hum Reprod. 2014;29:1859–65.CrossRef De Wert G, Dondorp W, Shenfield F, Barri DP, Diedrich K, et al. ESHRE Task Force on Ethics and Law 23: medically assisted reproduction in singles, lesbian and gay couples, and transsexual people. Hum Reprod. 2014;29:1859–65.CrossRef
22.
go back to reference Kreukels BP, Haraldsen IR, De Cuypere G, Richter-Appelt H, Gijs L, Cohen-Kettenis PT. A European network for the investigation of gender incongruence: the ENIGI initiative. Eur Psychiatry. 2012;27:445–50.CrossRef Kreukels BP, Haraldsen IR, De Cuypere G, Richter-Appelt H, Gijs L, Cohen-Kettenis PT. A European network for the investigation of gender incongruence: the ENIGI initiative. Eur Psychiatry. 2012;27:445–50.CrossRef
24.
go back to reference Wierckx K, Van Caenegem E, Pennings G, Elaut E, Dedecker D, Van de Peer F, et al. Reproductive wish in transsexual men. Hum Reprod. 2012;27:483–7.CrossRef Wierckx K, Van Caenegem E, Pennings G, Elaut E, Dedecker D, Van de Peer F, et al. Reproductive wish in transsexual men. Hum Reprod. 2012;27:483–7.CrossRef
25.
go back to reference Auer MK, Fuss J, Nieder TO, Briken P, Biedermann SV, Stalla GK, et al. Desire to have children among transgender people in Germany: a cross-sectional multi-center study. J Sex Med. 2018;15:757–67.CrossRef Auer MK, Fuss J, Nieder TO, Briken P, Biedermann SV, Stalla GK, et al. Desire to have children among transgender people in Germany: a cross-sectional multi-center study. J Sex Med. 2018;15:757–67.CrossRef
26.
go back to reference De Roo C, Tilleman K, T’Sjoen G, De Sutter P. Fertility options in transgender people. Int Rev Psychiatry. 2016;28:112–9.CrossRef De Roo C, Tilleman K, T’Sjoen G, De Sutter P. Fertility options in transgender people. Int Rev Psychiatry. 2016;28:112–9.CrossRef
27.
go back to reference Johnson EK, Finlayson C. Preservation of fertility potential for gender and sex diverse individuals. Transgend Health. 2016;1:41–4.CrossRef Johnson EK, Finlayson C. Preservation of fertility potential for gender and sex diverse individuals. Transgend Health. 2016;1:41–4.CrossRef
28.
go back to reference Maxwell S, Noyes N, Keefe D, Berkeley AS, Goldman KN. Pregnancy outcomes after fertility preservation in transgender men. Obstet Gynecol. 2017;129:1031–4.CrossRef Maxwell S, Noyes N, Keefe D, Berkeley AS, Goldman KN. Pregnancy outcomes after fertility preservation in transgender men. Obstet Gynecol. 2017;129:1031–4.CrossRef
29.
go back to reference Chen D, Bernardi LA, Pavone ME, Feinberg EC, Moravek MB. Oocyte cryopreservation among transmasculine youth: a cases series. J Assist Reprod Genet. 2018;35:2057–61.CrossRef Chen D, Bernardi LA, Pavone ME, Feinberg EC, Moravek MB. Oocyte cryopreservation among transmasculine youth: a cases series. J Assist Reprod Genet. 2018;35:2057–61.CrossRef
31.
go back to reference Leung A, Sakkas D, Pang S, Thornton K, Resetkova N. Assisted reproductive technology outcomes in female-to-male transgender patients compared with cisgender patients: a new frontier in reproductive medicine. Fertil Steril. 2019;112:858–65.CrossRef Leung A, Sakkas D, Pang S, Thornton K, Resetkova N. Assisted reproductive technology outcomes in female-to-male transgender patients compared with cisgender patients: a new frontier in reproductive medicine. Fertil Steril. 2019;112:858–65.CrossRef
32.
go back to reference Adeleye AJ, Cedars MI, Smith J, Mok-Lin E. Ovarian stimulation for fertility preservation or family building in a cohort of transgender men. J Assist Reprod Genet. 2019;36:2155–61.CrossRef Adeleye AJ, Cedars MI, Smith J, Mok-Lin E. Ovarian stimulation for fertility preservation or family building in a cohort of transgender men. J Assist Reprod Genet. 2019;36:2155–61.CrossRef
35.
go back to reference Almog B, Shehata F, Shalom-Paz E, Tan SL, Tulandi T. Age-related normogram for antral follicle count: McGill reference guide. Fertil Steril. 2011;95:663–6.CrossRef Almog B, Shehata F, Shalom-Paz E, Tan SL, Tulandi T. Age-related normogram for antral follicle count: McGill reference guide. Fertil Steril. 2011;95:663–6.CrossRef
36.
go back to reference Ng EH, Yeung WS, Fong DY, Ho PC. Effects of age on hormonal and ultrasound markers of ovarian reserve in Chinese women with proven fertility. Hum Reprod. 2003;18:2169–74.CrossRef Ng EH, Yeung WS, Fong DY, Ho PC. Effects of age on hormonal and ultrasound markers of ovarian reserve in Chinese women with proven fertility. Hum Reprod. 2003;18:2169–74.CrossRef
37.
go back to reference Balen AH, Schachter ME, Montgomery D, Reid RW, Jacobs HS. Polycystic ovaries are a common finding in untreated female to male transsexuals. Clin Endocrinol. 1993;38:325–9.CrossRef Balen AH, Schachter ME, Montgomery D, Reid RW, Jacobs HS. Polycystic ovaries are a common finding in untreated female to male transsexuals. Clin Endocrinol. 1993;38:325–9.CrossRef
38.
go back to reference Baba T, Endo T, Honnma H, Kitajima Y, Hayashi T, Ikeda H, et al. Association between polycystic ovary syndrome and female-to-male transsexuality. Hum Reprod. 2007;22:1011–6.CrossRef Baba T, Endo T, Honnma H, Kitajima Y, Hayashi T, Ikeda H, et al. Association between polycystic ovary syndrome and female-to-male transsexuality. Hum Reprod. 2007;22:1011–6.CrossRef
39.
go back to reference Vujovic S, Popovic S, Sbutega-Milosevic G, Djordjevic M, Gooren L. Transsexualism in Serbia: a twenty-year follow-up study. J Sex Med. 2009;6:1018–23.CrossRef Vujovic S, Popovic S, Sbutega-Milosevic G, Djordjevic M, Gooren L. Transsexualism in Serbia: a twenty-year follow-up study. J Sex Med. 2009;6:1018–23.CrossRef
40.
go back to reference Baba T, Endo T, Ikeda K, Shimizu A, Honnma H, Ikeda H, et al. Distinctive features of female-to-male transsexualism and prevalence of gender identity disorder in Japan. J Sex Med. 2011;8:1686–93.CrossRef Baba T, Endo T, Ikeda K, Shimizu A, Honnma H, Ikeda H, et al. Distinctive features of female-to-male transsexualism and prevalence of gender identity disorder in Japan. J Sex Med. 2011;8:1686–93.CrossRef
41.
go back to reference Thakre N, Homburg R. A review of IVF in PCOS patients at risk of ovarian hyperstimulation syndrome. Expert Rev Endocrinol Metab. 2019;14:315–9.CrossRef Thakre N, Homburg R. A review of IVF in PCOS patients at risk of ovarian hyperstimulation syndrome. Expert Rev Endocrinol Metab. 2019;14:315–9.CrossRef
42.
go back to reference Rotterdam ESHRE/ASRM-Sponsored PCOS consensus workshop group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod. 2004;19:41–7.CrossRef Rotterdam ESHRE/ASRM-Sponsored PCOS consensus workshop group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod. 2004;19:41–7.CrossRef
43.
go back to reference Lai TC, McDougall R, Feldman D, Elder CV, Pang KC. Fertility counseling for transgender adolescents: a review. J Adolesc Health. 2020;66:658–65.CrossRef Lai TC, McDougall R, Feldman D, Elder CV, Pang KC. Fertility counseling for transgender adolescents: a review. J Adolesc Health. 2020;66:658–65.CrossRef
44.
go back to reference Armuand G, Dhejne C, Olofsson JI, Rodriguez-Wallberg KA. Transgender men’s experiences of fertility preservation: a qualitative study. Hum Reprod. 2017;32:383–90.CrossRef Armuand G, Dhejne C, Olofsson JI, Rodriguez-Wallberg KA. Transgender men’s experiences of fertility preservation: a qualitative study. Hum Reprod. 2017;32:383–90.CrossRef
Metadata
Title
Ovarian stimulation outcomes among transgender men compared with fertile cisgender women
Authors
Hadar Amir
Iris Yaish
Nivin Samara
Joseph Hasson
Asnat Groutz
Foad Azem
Publication date
01-10-2020
Publisher
Springer US
Published in
Journal of Assisted Reproduction and Genetics / Issue 10/2020
Print ISSN: 1058-0468
Electronic ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-020-01902-7

Other articles of this Issue 10/2020

Journal of Assisted Reproduction and Genetics 10/2020 Go to the issue