Skip to main content
SpringerLink
Log in

Ovarian functions and polycystic ovary syndrome in adult women with type 1 diabetes mellitus in a Turkish population

  • Original Article
  • Published:
Journal of Endocrinological Investigation Aims and scope Submit manuscript

Abstract

Purpose

The effect of gonadotropin-releasing hormone agonist (GnRHa) stimulation has not been studied in adult women with type 1 diabetes mellitus (DM). We investigated the baseline and stimulated hormone levels after GnRHa and the frequency and relationship between polycystic ovary syndrome (PCOS) and type 1 DM in adult women with type 1 DM.

Methods

We included 55 adult women (age, 17–35 years) with type 1 DM and 15 healthy women (age, 20–29 years). Hormones including total testosterone, androstenedione, dehydroepiandrosterone sulphate (DHEAS), follicle-stimulating hormone (FSH), luteinising hormone (LH), estradiol, prolactin, and thyroid-stimulating hormone were measured in the early follicular phase of the menstrual cycle. All participants underwent GnRHa stimulation test, and FSH, LH, estradiol and 17-OHP response levels were measured every 6 h for 24 h. PCOS was diagnosed according to ESHRE/ASRM (Rotterdam) criteria.

Results

Between patients with type 1 DM and healthy controls, no significant differences were noted in mean age and body mass index (BMI) as well as baseline and stimulated hormone levels after buserelin stimulation, except for baseline serum 17-OHP levels, which was higher in patients with type 1 DM. Polycystic ovary morphology (PCOM) was detected in 14 (25%) patients, clinical hyperandrogenism in 16 (29%), hyperandrogenemia in 25 (45%), anovulatory cycle in 72%, and PCOS in 20 (36%).

Conclusion

All parameters representing androgen excess disorders, except 17-OHP level, of both groups were similar, and frequencies of PCOS and anovulatory cycle in adult women with type 1 DM were 36% and 72%, respectively.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Codner E, Merino PM, Tena-Sempere M (2012) Female reproduction and type 1 diabetes: from mechanisms to clinical findings. Hum Reprod Update 18:568–585. https://doi.org/10.1093/humupd/dms024

    Article  CAS  PubMed  Google Scholar 

  2. Codner E, Soto N, Lopez P, Trejo L, Avila A, Eyzaguirre FC, Iniguez G, Cassorla F (2006) Diagnostic criteria for polycystic ovary syndrome and ovarian morphology in women with type 1 diabetes mellitus. J Clin Endocrinol Metab 91:2250–2256. https://doi.org/10.1210/jc.2006-0108

    Article  CAS  PubMed  Google Scholar 

  3. Conway G, Dewailly D, Diamanti-Kandarakis E, Escobar-Morreale HF, Franks S, Gambineri A, Kelestimur F, Macut D, Micic D, Pasquali R, Pfeifer M, Pignatelli D, Pugeat M, Yildiz BO, ESE PCOS Special Interest Group (2014) The polycystic ovary syndrome: a position statement from the European Society of Endocrinology. Eur J Endocrinol 171:1–29. https://doi.org/10.1530/EJE-14-0253

    Article  CAS  Google Scholar 

  4. Codner E, Mook-Kanamori D, Bazaes RA, Unanue N, Sovino H, Ugarte F, Avila A, Iniguez G, Cassorla F (2005) Ovarian function during puberty in girls with type 1 diabetes mellitus: response to leuprolide. J Clin Endocrinol Metab 90:3939–3945. https://doi.org/10.1210/jc.2005-0142

    Article  CAS  PubMed  Google Scholar 

  5. Unluhizarci K, Karaca Z, Kelestimur F (2021) Role of insulin and insulin resistance in androgen excess disorders. World J Diabetes 12:616–629. https://doi.org/10.4239/wjd.v12.i5.616

    Article  PubMed  PubMed Central  Google Scholar 

  6. Codner E, Cassorla F (2009) Puberty and ovarian function in girls with type 1 diabetes mellitus. Horm Res 71:12–21. https://doi.org/10.1159/000173737

    Article  CAS  PubMed  Google Scholar 

  7. Escobar-Morreale HF, Roldan B, Barrio R, Alonso M, Sancho J, de la Calle H, Garcia-Robles R (2000) High prevalence of the polycystic ovary syndrome and hirsutism in women with type 1 diabetes mellitus. J Clin Endocrinol Metab 85:4182–4187. https://doi.org/10.1210/jcem.85.11.6931

    Article  CAS  PubMed  Google Scholar 

  8. Bolli GB (2001) Physiological insulin replacement in type 1 diabetes mellitus. Exp Clin Endocrinol Diabetes 109:317–332. https://doi.org/10.1055/s-2001-18591

    Article  Google Scholar 

  9. Cara JF, Rosenfield RL (1988) Insulin-like growth factor I and insulin potentiate luteinizing hormone-induced androgen synthesis by rat ovarian thecal-interstitial cells. Endocrinology 123:733–739. https://doi.org/10.1210/endo-123-2-733

    Article  CAS  PubMed  Google Scholar 

  10. Corner E, Iniguez G, Hernandez IM, Lopez P, Rhumie HK, Villarroel C, Reira A (2011) Elevated anti-Mullerian hormone (ADH) and inhibin B levels in prepubertal girls with type 1 diabetes mellitus. Clin Endocrinol (Oxf) 74:73–78. https://doi.org/10.1111/j.1365-2265.2010.03887.x

    Article  CAS  Google Scholar 

  11. Sahin Y, Kelestimur F (1993) 17-Hydroxyprogesterone response to buserelin testing in the polycystic ovary syndrome. Clin Endocrinol (Oxf) 39:151–155. https://doi.org/10.1111/j.1365-2265.1993.tb01767.x

    Article  CAS  PubMed  Google Scholar 

  12. Rosenfield RL (2013) Clinical review: adolescent anovulation: maturational mechanisms and implications. J Clin Endocrinol Metab 98:3572–3583. https://doi.org/10.1210/jc.2013-1770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Rotterdam ESHRE/ASRM-Sponsored PCOS Consensus Workshop Group (2004) Consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil Steril 81:19–25. https://doi.org/10.1016/j.fertnstert.2003.10.004

    Article  Google Scholar 

  14. Miyoshi A, Nagai S, Takeda M, Kondo T, Nomoto H, Kameda H, Hirai A, Cho K, Kimachi K, Shimizu C, Atsumi T, Miyoshi H (2013) Ovarian morphology and prevalence of polycystic ovary syndrome in Japanese women with type 1 diabetes mellitus. J Diabetes Investig 4:326–329. https://doi.org/10.1111/jdi.12040

    Article  PubMed  PubMed Central  Google Scholar 

  15. Asuncion M, Calvo RM, San Millan JL, Sancho J, Aviles E-M (2000) A prospective study of the prevalence of the polycystic ovary syndrome in unselected Caucasian women from Spain. J Clin Endocrinol Metab 85:2434–2438. https://doi.org/10.1210/jcem.85.7.6682

    Article  CAS  PubMed  Google Scholar 

  16. Kelestimur F, Unluhizarci K, Baybuga H, Atmaca H, Bayram F, Sahin Y (2006) Prevalence of polycystic ovarian changes and polycystic ovary syndrome in premenopausal women with treated type 2 diabetes mellitus. Fertil Steril 86:405–410. https://doi.org/10.1016/j.fertnstert.2006.01.019

    Article  PubMed  Google Scholar 

  17. Palomba S, Falbo A, Zullo F, Orio FJR (2009) Evidence-based and potential benefits of metformin in the polycystic ovary syndrome: a comprehensive review. Endocr Rev 30:1–50. https://doi.org/10.1210/er.2008-0030

    Article  CAS  PubMed  Google Scholar 

  18. Codner E, Escobar-Morreale HF (2007) Clinical review: Hyperandrogenism and polycystic ovary syndrome in women with type 1 diabetes mellitus. J Clin Endocrinol Metab 92:1209–1216. https://doi.org/10.1210/jc.2006-2641

    Article  CAS  PubMed  Google Scholar 

  19. Diamanti-Kandarakis E, Dunaif A (2012) Insulin resistance and the polycystic ovary syndrome revisited: an update on mechanisms and implications. Endocr Rev 33:981–1030. https://doi.org/10.1210/er.2011-1034

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Poretsky L, Cataldo NA, Rosenwaks Z, Giudice LC (1999) The insulin-related ovarian regulatory system in health and disease. Endocr Rev 20:535–582. https://doi.org/10.1210/edrv.20.4.0374

    Article  CAS  PubMed  Google Scholar 

  21. Adashi EY, Hsueh AJ, Yen SS (1981) Insulin enhancement of luteinizing hormone and follicle-stimulating hormone release by cultured pituitary cells. Endocrinology 108:1441–1449. https://doi.org/10.1210/endo-108-4-1441

    Article  CAS  PubMed  Google Scholar 

  22. Roldan B, Escobar-Morreale HF, Barrio R, de La Calle H, Alonso M, Garcia-Robles R, Sancho J (2001) Identification of the source of androgen excess in hyperandrogenic type 1 diabetic patients. Diabetes Care 24:1297–1299. https://doi.org/10.2337/diacare.24.7.1297

    Article  CAS  PubMed  Google Scholar 

  23. Yildiz BO, Bozdag G, Yapici Z, Esinler I, Yarali H (2012) Prevalence, phenotype and cardiometabolic risk of polycystic ovary syndrome under different diagnostic criteria. Hum Reprod 27:3067–3073. https://doi.org/10.1093/humrep/des232

    Article  PubMed  Google Scholar 

  24. Bizzarri C, Benevento D, Rava L, Patera IP, Schiaffini R, Ciampalini P, Giannone G, Cappa M (2011) Ovarian hyperandrogenism in adolescents and young women with type I diabetes is primarily related to birth weight and body mass index. Fertil Steril 96:1497-1502.e1. https://doi.org/10.1016/j.fertnstert.2011.09.023

    Article  CAS  PubMed  Google Scholar 

  25. Braham R, RobertA A, Musallam MA, Alanazi A, Sweden NB, Al Dawish MA (2017) Reproductive disturbances among Saudi adolescent girls and young women with type 1 diabetes mellitus. World J Diabet 8:475–483. https://doi.org/10.4239/wjd.v8.i11.475

    Article  Google Scholar 

  26. Amato MC, Guarnotta V, Ciresi A, Modica R, Panto F, Giordano C (2014) No phenotypic differences for polycystic ovary syndrome (PCOS) between women with and without type 1 diabetes mellitus. J Clin Endocrinol Metab 99:203–211. https://doi.org/10.1210/jc.2013-2669

    Article  CAS  PubMed  Google Scholar 

  27. Gunness A, Pazderska A, Ahmed M, McGowan A, Phelan N, Boran G, Taylor AE, O’Reilly MW, Arlt W, Moore K, Behan LA, Sherlock M, Gibney J (2018) Measurement of selected androgens using liquid chromatography-tandem mass spectrometry in reproductive-age women with Type 1 diabetes. Hum Reprod 33:1727–1734. https://doi.org/10.1093/humrep/dey243

    Article  CAS  PubMed  Google Scholar 

  28. Lebkowska A, Adamska A, Krentowska A, Uruska A, Rogowicz-Frontczak A, Araszkiewicz A, Ozegowska K, Hryniewicka J, Lesniewska M, Wender-Ozegowska E, Zozulinska-Ziolkiewicz D, Kowalska I (2021) The influence of prepubertal onset of type 1 diabetes and age of menarche on polycystic ovary syndrome diagnosis. J Clin Endocrinol Metab 106:1811–1820. https://doi.org/10.1210/cinema/dgab062 (PMID: 33537700)

    Article  PubMed  Google Scholar 

  29. Bayona A, Martinez-Vaello V, Zamora J, Nattero-Chavez L, Luque-Ramirez M, Escobar-Morreale HF (2022) Prevalence of PCOS and related hyperandrogenic traits in premenopausal women with type 1 diabetes: a systematic review and meta-analysis. Hum Reprod Update 28:501–517. https://doi.org/10.1093/humupd/dmac011 (PMID: 35237802)

    Article  PubMed  Google Scholar 

  30. Escobar-Morreale HF, Roldan-Martin MB (2016) Type 1 diabetes and polycystic ovary syndrome: systematic review and meta-analysis. Diabetes Care 39:639–648. https://doi.org/10.2337/dc15-2577

    Article  CAS  PubMed  Google Scholar 

  31. Ehrmann DA, Rosenfield RL, Barnes RB, Brigell DF, Sheikh Z (1992) Detection of functional ovarian hyperandrogenism in women with androgen excess. N Engl J Med 327:157–162. https://doi.org/10.1056/NEJM199207163270304

    Article  CAS  PubMed  Google Scholar 

  32. Kadiroğulları P, Demir E, Bahat PY, Kıyak H, Seckin KD (2020) Evaluation of relationship between HbA1c levels and ovarian reserve in patients with type 1 diabetes mellitus. Gynecol Endocrinol 36:426–430. https://doi.org/10.1080/09513590.2019.1708893

    Article  CAS  PubMed  Google Scholar 

  33. Teede HJ, Misso ML, Costello MF, Dokras A, Laven J, Moran L, Piltonen T, Norman RJ, International PCOS Network (2018) Recommendations from the international evidence-based guideline for the assessment and management of polycystic ovary syndrome. Hum Reprod 33:1602–1618. https://doi.org/10.1093/humrep/dey256

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

Preparation for publication of this article is supported by the Society of Endocrinology and Metabolism of Turkey.

Funding

None.

Author information

Authors and Affiliations

  1. Department of Endocrinology, Erciyes University Medical School, Kayseri, Turkey

    E. Urhan, A. Hacioglu, Z. Karaca & K. Unluhizarci

  2. Department of Endocrinology, Tekirdağ Namik Kemal University Medical School, Tekirdaǧ, Turkey

    G. Elbuken

  3. Department of Endocrinology, Yeditepe University Medical School, Istanbul, Turkey

    F. Kelestimur

Authors
  1. E. Urhan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. G. Elbuken
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. A. Hacioglu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Z. Karaca
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. K. Unluhizarci
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. F. Kelestimur
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Z. Karaca.

Ethics declarations

Conflict of interest

All authors declare no conflict of interest in the reported research.

Ethical approval

All procedures which were performed in studies with human participants followed the 1964 Helsinki Declaration the ethical standards of the national or institutional research committee and its later amendments or comparable ethical standards.

Informed consent

Informed consent in this study was taken from all participants.

Additional information

Publisher's Note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Urhan, E., Elbuken, G., Hacioglu, A. et al. Ovarian functions and polycystic ovary syndrome in adult women with type 1 diabetes mellitus in a Turkish population. J Endocrinol Invest 46, 609–616 (2023). https://doi.org/10.1007/s40618-022-01946-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40618-022-01946-9

Keywords

Search

Navigation