Skip to main content

Advertisement

Log in

Oocyte retrieval outcomes among adolescent transgender males

  • Fertility Preservation
  • Published:
Journal of Assisted Reproduction and Genetics Aims and scope Submit manuscript

Abstract

Purpose

To compare fertility preservation (FP) outcomes among adolescent transgender males with those of cisgender females.

Methods

This retrospective cohort study included nine adolescent transgender males and 39 adolescent cisgender females who underwent FP between January 2017–April 2019 and September 2013–April 2019, respectively. The transgender males were referred before initiating testosterone, and the cisgender females were referred due to cancer diagnosis before starting anticancer treatment. Statistical analyses compared assisted reproductive technology (ART) data and FP outcomes between two groups.

Results

Basal FSH levels (5.4 ± 1.7 mIU/mL) and AFC (19.8 ± 5.6) of all transgender males were normal compared with standard references. The mean age of transgender males and cisgender females was similar (16.4 ± 1.1 vs 15.5 ± 1.3 years, respectively, P = 0.064). The amount of FSH used for stimulation was significantly lower among the former compared with the latter (2416 ± 1041 IU vs 4372 ± 1877 IU, P < 0.001), but the duration of stimulation was similar (12.6 ± 4.0 and 10.1 ± 2.8 days, P = 0.086). Peak estradiol level was significantly higher among transgender males compared with cisgender females (3073 ± 2637 pg/mL vs 1269 ± 975 pg/mL, respectively, P = 0.018), but there were no significant differences in number of retrieved oocytes between the two groups (30.6 ± 12.8 vs 22 ± 13.2, P = 0.091), number of MII oocytes (25.6 ± 12.9 vs 18.8 ± 11.2, P = 0.134), or maturity rates (81.5 ± 10.0% vs 85.4 ± 14.6%, P = 0.261).

Conclusions

Adolescent transgender males have an excellent response to ovulation stimulation before initiating testosterone treatment. Oocyte cryopreservation is, therefore, a feasible and effective way for them to preserve their fertility for future biological parenting.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. 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.

    Google Scholar 

  2. Murad MH, Elamin MB, Garcia MZ, Mullan RJ, Murad A, Erwin PJ, et al. Hormonal therapy and sex reassignment: a systematic review and meta-analysis of quality of life and psychosocial outcomes. Clin Endocrinol. 2010;72:214–31.

    Google Scholar 

  3. Edwards-Leeper L, Spack NP. Psychological evaluation and medical treatment of transgender youth in an interdisciplinary "Gender Management Service" (GeMS) in a major pediatric center. J Homosex. 2012;59:321–36.

    PubMed  Google Scholar 

  4. Olson J, Schrager SM, Belzer M, Simons LK, Clark LF. Baseline physiologic and psychosocial characteristics of transgender youth seeking care for gender dysphoria. J Adolesc Health. 2015;57:374–80.

    PubMed  PubMed Central  Google Scholar 

  5. 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.

    PubMed  CAS  Google Scholar 

  6. 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.

    PubMed  Google Scholar 

  7. Futterweit W, Deligdisch L. Histopathological effects of exogenously administered testosterone in 19 female to male transsexuals. J Clin Endocrinol Metab. 1986;62:16–21.

    PubMed  CAS  Google Scholar 

  8. 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.

    PubMed  CAS  Google Scholar 

  9. 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.

    PubMed  CAS  Google Scholar 

  10. Caanen MR, Soleman RS, Kuijper EA, Kreukels BP, De Roo C, Tilleman K, et al. Antimüllerian hormone levels decrease in female-to-male transsexuals using testosterone as cross-sex therapy. Fertil Steril. 2015;103:1340–5.

    PubMed  CAS  Google Scholar 

  11. 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;16:145–7.

    Google Scholar 

  12. 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.

    PubMed  CAS  Google Scholar 

  13. 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  Google Scholar 

  14. 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.

    Google Scholar 

  15. Harada M, Osuga Y. Fertility preservation for female cancer patients. Int J Clin Oncol. 2019;24:28–33.

    PubMed  Google Scholar 

  16. De Roo C, Tilleman K, T'Sjoen G, De Sutter P. Fertility options in transgender people. Int Rev Psychiatry. 2016;28:112–9.

    PubMed  Google Scholar 

  17. Johnson EK, Finlayson C. Preservation of fertility potential for gender and sex diverse individuals. Transgend Health. 2016;1:41–4.

    PubMed  PubMed Central  Google Scholar 

  18. 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.

    PubMed  Google Scholar 

  19. Jones CA, Reiter L, Greenblatt E. Fertility preservation in transgender patients. Int J Transgend. 2016;17:76–82.

    CAS  Google Scholar 

  20. Nahata L, Tishelman AC, Caltabellotta NM, Quinn GP. Low fertility preservation utilization among transgender youth. J Adolesc Health. 2017;61:40–4.

    PubMed  Google Scholar 

  21. Chen D, Simons L, Johnson EK, Lockart BA, Finlayson C. Fertility preservation for transgender adolescents. J Adolesc Health. 2017;61:120–3.

    PubMed  PubMed Central  Google Scholar 

  22. Riggs DW, Bartholomaeus C. Fertility preservation decision making among Australian transgender and non-binary adults. Reprod Health. 2018;25(15):181.

    Google Scholar 

  23. Brik T, Vrouenraets LJJJ, Schagen SEE, Meissner A, de Vries MC, Hannema SE. Use of fertility preservation among a cohort of transgirls in the Netherlands. J Adolesc Health. 2019;64:589–93.

    PubMed  Google Scholar 

  24. James-Abra S, Tarasoff LA, Green D, Epstein R, Anderson S, Marvel S, et al. Trans people's experiences with assisted reproduction services: a qualitative study. Hum Reprod. 2015;30:1365–74.

    PubMed  CAS  Google Scholar 

  25. Chen D, Matson M, Macapagal K, Johnson EK, Rosoklija I, Finlayson C, et al. Attitudes toward fertility and reproductive health among transgender and gender-nonconforming adolescents. J Adolesc Health. 2018;63:62–8.

    PubMed  PubMed Central  Google Scholar 

  26. Chen D, Kyweluk MA, Sajwani A, Gordon EJ, Johnson EK, Finlayson CA, et al. Factors affecting fertility decision-making among transgender adolescents and young adults. LGBT Health. 2019;6:107–15.

    PubMed  PubMed Central  Google Scholar 

  27. Segev-Becker A, Israeli G, Elkon-Tamir E, Perl L, Sekler O, Amir H, et al. Children and adolescent with gender dysphoria in Israel: increasing referral and fertility preservation rates. Endocr Pract. 2020;26:423–8. https://doi.org/10.4158/EP-2019-0418.Onlineaheadofprint.

    Article  PubMed  Google Scholar 

  28. Fernández R, Esteva I, Gómez-Gil E, Rumbo T, Almaraz MC, Roda E, et al. The CA(n) polymorphism of ERβ is associated with FtM transsexualism. J Sex Med. 2014;11:720–8.

    PubMed  Google Scholar 

  29. Fernández R, Guillamon A, Cortés-Cortés J, Gómez-Gil E, Jácome A, Esteva I, et al. Molecular basis of gender dysphoria: androgen and estrogen receptor interaction. Psychoneuroendocrinology. 2018;98:161–7.

    PubMed  Google Scholar 

  30. Zulli K, Bianco B, Mafra FA, Teles JS, Christofolini DM, Barbosa CP. Polymorphism of the estrogen receptor β gene is related to infertility and infertility-associated endometriosis. Arq Bras Endocrinol Metabol. 2010;54:567–71.

    PubMed  Google Scholar 

  31. Ayvaz OU, Ekmekçi A, Baltaci V, Onen HI, Unsal E. Evaluation of in vivo fertilization parameters and estrogen receptor alfa gene polymorphism for women with unexplained infertility. J Assist Reprod Genet. 2009;26:503–10.

    PubMed  PubMed Central  Google Scholar 

  32. Anagnostou E, Mavrogianni D, Theofanakis C, Drakakis P, Bletsa R, Demirol A, et al. ESR1, ESR2 and FSH receptor gene polymorphism in combination: a useful genetic tool for the prediction of poor responders. Curr Pharm Biotechnol. 2012;13:426–34.

    PubMed  CAS  Google Scholar 

  33. de Mattos CS, Trevisan CM, Peluso C, Adami F, Cordts EB, Christofolini DM, et al. ESR1 and ESR2 gene polymorphisms are associated with human reproduction outcomes in Brazilian women. J Ovarian Res. 2014;20(7):114.

    Google Scholar 

  34. Hines M, Brook C, Conway GS. Androgen and psychosexual development: core gender identity, sexual orientation and recalled childhood gender role behavior in women and men with congenital adrenal hyperplasia (CAH). J Sex Res. 2004;41:75–81.

    PubMed  Google Scholar 

  35. Sadr M, Khorashad BS, Talaei A, Fazeli N, Hönekopp J. 2D:4D suggests a role of prenatal testosterone in gender dysphoria. Arch Sex Behav. 2020;49:421–32.

    PubMed  PubMed Central  Google Scholar 

  36. Bütikofer A, Figlio DN, Karbownik K, Kuzawa CW, Salvanes KG. Evidence that prenatal testosterone transfer from male twines reduces the fertility and socioeconomic success of their female co-twin. Proc Natl Acad Sci U S A. 2019;116:6749–53.

    PubMed  PubMed Central  Google Scholar 

  37. Filippou P, Homburg R. Is foetal hyperexposure to androgens a cause of PCOS? Hum Reprod Update. 2017;23:421–32.

    PubMed  CAS  Google Scholar 

  38. Abbott DH, Kraynak M, Dumesic DA, Levine JE. In utero androgen excess: a developmental commonality preceding polycystic ovary syndrome? Front Horm Res. 2019;53:1–17.

    PubMed  PubMed Central  Google Scholar 

  39. Balen AH, Morley LC, Misso M, Franks S, Legro RS, Wijeyaratne CN, et al. The management of anovulatory infertility in women with polycystic ovary syndrome: an analysis of the evidence to support the development of global WHO guidance. Hum Reprod Update. 2016;22:687–708.

    PubMed  Google Scholar 

  40. 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.

    CAS  Google Scholar 

  41. 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.

    PubMed  Google Scholar 

  42. 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.

    PubMed  Google Scholar 

  43. 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.

    PubMed  Google Scholar 

  44. Domingo J, Guillen V, Ayllon Y, MartinezM ME, Pellicer A, et al. Ovarian response to controlled ovarian hyperstimulation in cancer patients is diminished even before oncological treatment. Fertil Steril. 2012;97:930–4.

    PubMed  Google Scholar 

  45. Pal L, Leykin L, Schifren JL, Isaacson KB, Chang YC, Nikruil N, et al. Malignancy may adversely influence the quality and behavior of oocytes. Hum Reprod. 1998;13:1837–40.

    PubMed  CAS  Google Scholar 

  46. Klock SC, Zhang JX, Kazer RR. Fertility preservation for female cancer patients: early clinical experience. Fertil Steril. 2010;94:149–55.

    PubMed  Google Scholar 

  47. Oktay K, Hourvitz A, Sahin G, Oktem O, Safro B, Cil A, et al. Letrozole reduces estrogen and gonadotropin exposure in women with breast cancer undergoing ovarian stimulation before chemotherapy. J Clin Endocrinol Metab. 2006;91:3885–90.

    PubMed  CAS  Google Scholar 

  48. Quintero RB, Helmer A, Huang JQ, Westphal LM. Ovarian stimulation for fertility preservation in patients with cancer. Fertil Steril. 2010;93:865–8.

    PubMed  CAS  Google Scholar 

  49. Almog B, Azem F, Gordon D, Pauzner D, Amit A, Barkan G, et al. Effects of cancer on ovarian response in controlled ovarian stimulation for fertility preservation. Fertil Steril. 2012;98:957–60.

    PubMed  Google Scholar 

  50. Robertson AD, Missmer SA, Ginsbug ES. Embryo yield after in vitro fertilization in women undergoing embryo banking for fertility preservation before chemotherapy. Fertil Steril. 2011;95:588–91.

    PubMed  Google Scholar 

  51. Quinn MM, Cakmak H, Letourneau JM, Cedars MI, Rosen MP. Response to ovarian stimulation is not impacted by a breast cancer diagnosis. Hum Reprod. 2017;32:568–74.

    PubMed  CAS  Google Scholar 

  52. Michaan N, Ben-David G, Ben-Yosef D, Almog B, Many A, Pauzner D, et al. Ovarian stimulation and emergency in vitro fertilization for fertility preservation in cancer patients. Eur J Obstet Gynecol Reprod Biol. 2010;149:175–7.

    PubMed  Google Scholar 

  53. Knopman JM, Noyes N, Talebian S, Krey LC, Grifo JA, Licciardi F. Women with cancer undergoing ART for fertility preservation: a cohort study of their response to exogenous gonadotropins. Fertil Steril. 2009;91:1476–8.

    PubMed  Google Scholar 

  54. Turan V, Quinn MM, Dayioglu N, Rosen MP, Oktay K. The impact of malignancy onresponse to ovarian stimulation for fertility preservation: a meta-analysis. Fertil Steril. 2018;110:1347–55.

    PubMed  Google Scholar 

  55. 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.

    PubMed  Google Scholar 

  56. De Roo C, Tilleman K, Vercruysse C, Declercq H, T'Sjoen G, Weyers S, et al. Texture profile analysis reveals a stiffer ovarian cortex after testosterone therapy: a pilot study. J Assist Reprod Genet. 2019;36:1837–43.

    PubMed  PubMed Central  Google Scholar 

  57. Maxwell S, Noyes N, Keefe D, Berkeley AS, Goldman KN. Pregnancy outcomes after fertility preservation in transgender men. Obstet Gynecol. 2017;129:1031–4.

    PubMed  Google Scholar 

  58. Insogna IG, Ginsburg E, Srouji S. Fertility preservation for adolescent transgender male patients: a case series. J Adolesc Health. 2020. https://doi.org/10.1016/j.jadohealth.2019.12.004.

  59. 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.

    PubMed  CAS  Google Scholar 

  60. 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.

    PubMed  Google Scholar 

  61. Cooper AR, Parker A, Lambert-Messerlian G, French A, White A, Odem RR, et al. Should we be utilizing transabdominal antral follicle count (AFC) ovarian reserve screens in prepubertal and pubertal girls. J Pediatr Adolesc Gynecol. 2011;24:e51.

    Google Scholar 

  62. LabCorp. Expected values and S.I. unit conversion tables. 2019 https://www.esoterix.com/sites/default/files/Endocrine%20Sciences%20Expected%20Values%20%281%29.pdf

  63. Deutsch MB, Bhakri V, Kubicek K. Effects of cross-sex hormone treatment on transgender women and men. Obstet Gynecol. 2015;125:605–10.

    PubMed  PubMed Central  CAS  Google Scholar 

  64. Vita R, Settineri S, Liotta M, Benvenga S, Trimarchi F. Changes in hormonal and metabolic parameters in transgender subjects on cross-sex hormone therapy: a cohort study. Maturitas. 2018;107:92–6.

    PubMed  CAS  Google Scholar 

  65. Gessler M, Poustka A, Cavenee W, Neve RL, Orkin SH, Bruns GA. Homozygous deletion in Wilms tumours of a zinc-finger gene identified by chromosome jumping. Nature. 1990;343:774–8.

    PubMed  CAS  Google Scholar 

  66. Gao F, Zhang J, Wang X, Yang J, Chen D, Huff V, et al. Wt1 functions in ovarian follicle development by regulating granulosa cell differentiation. Hum Mol Genet. 2014;23:333–41.

    PubMed  CAS  Google Scholar 

  67. Wang H, Li G, Zhang J, Gao F, Li W, Qin Y, et al. Novel WT1 missense mutations in Han Chinese women with premature ovarian failure. Sci Rep. 2015;11(5):13983.

    Google Scholar 

  68. Rotterdam ESHRE/ASRM-Sponsored PCOS consensus workshop group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Hum Reprod. 2004;19:41–7.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Hadar Amir.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was approved by the ethics committee (Helsinki) of the Tel Aviv Medical Center (#0647-19-TLV) and the institutional and review board of the Rabin Medical Center (#0757-19-RMC).

Statement of informed consent

Informed consent was obtained from all individual participants included in the study.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Amir, H., Oren, A., Klochendler Frishman, E. et al. Oocyte retrieval outcomes among adolescent transgender males. J Assist Reprod Genet 37, 1737–1744 (2020). https://doi.org/10.1007/s10815-020-01815-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10815-020-01815-5

Keywords

Navigation