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Anti-Müllerian hormone serum levels in systemic lupus erythematosus patients: Influence of the disease severity and therapy on the ovarian reserve

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Abstract

Purpose

Systemic lupus erythematosus (SLE) mainly affects childbearing age women and pharmacological treatments may negatively influence the ovarian reserve. Anti-Müllerian hormone (AMH) could be a good biomarker for ovarian reserve.

Methods

AMH serum levels were assessed in 86 consecutive SLE female patients with regular menstrual cycle compared with 44 aged matched healthy controls. Clinical and demographic characteristics, disease duration, pattern of organ involvement, and previous and current therapies were recorded.

Results

AMH levels were comparable between patients and controls (4.2 ± 3.1 ng/ml vs. 5.0 ± 3.1 ng/ml, p = 0.21). According to disease severity, AMH levels were lower in SLE patients with major organ involvement than in controls (3.8 ± 2.7 ng/ml vs. 5.0 ± 3.1 ng/ml, p = 0.08); no difference was found between SLE patients with mild organ involvement (4.5 ± 3.4 ng/ml) and controls (p = 0.43). Grouping patients based on the pharmacological treatments, AMH serum levels did not differ among SLE patients treated with antimalarials only (4.7 ± 3.3 ng/ml), conventional disease-modifying antirheumatic drugs (cDMARDs) only (4.8 ± 3.2 ng/ml), cDMARDs and antimalarials (3.9 ± 2.9 ng/ml) or cyclophosphamide (CYC) only (4.9 ± 3.9 ng/ml), compared to controls, but patients sequentially treated with cDMARDs and CYC, had significantly lower AMH serum levels than controls (p = 0.01).

Conclusions

SLE patients showed comparable AMH levels than controls, however, a reduction of the ovarian reserve was associated with sequentially therapy with CYC and cDMARDs and with the disease severity. AMH could be a sensitive and specific biomarker of ovarian reserve in SLE and it could be useful for therapeutic strategy and family planning.

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References

  1. M.E. Clowse, E. Chakravarty, K.H. Costenbader, C. Chambers, K. Michaud, Effects of infertility, pregnancy loss, and patient concerns on family size of women with rheumatoid arthritis and systemic lupus erythematosus. Arthritis Care Res (Hoboken) 64(5), 668–674 (2012)

    Article  Google Scholar 

  2. R.A. Hickman, C. Gordon, Causes and management of infertility in systemic lupus erithematosus. Rheumatol. (Oxf.) 50, 1551–1558 (2011)

    Article  Google Scholar 

  3. J. Boivin, L. Bunting, J.A. Collins, K.G. Nygren, International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Hum. Reprod. 22, 4506–4512 (2007)

    Article  Google Scholar 

  4. M. Costa, D. Colia, Treating infertility in autoimmune patients. Rheumatology 47, 38–41 (2008)

    Article  Google Scholar 

  5. C. Leroy, J.M. Rigot, M. Leroy, C. Decanter, K.Le Mapihan, A.S. Parent, A.C.Le Guillou, I. Yakoub-Agha, S. Dharacy, C. Noel, M.C. Vantyghem, Immunosuppressive drugs and fertility. Orphanet. J. Rare. Dis. 10, 136 (2015)

    Article  PubMed  PubMed Central  Google Scholar 

  6. S. Appenzeller, P.F. Blatyta, L.T. Costallat, Ovarian failure in SLE patients using pulse cyclophosphamide: Comparison of different regimes. Rheumatol. Int. 28, 567–571 (2008)

    Article  CAS  PubMed  Google Scholar 

  7. J. Boivin, L. Bunting, J.A. Collins, K.G. Nygren, International estimates of infertility prevalence and treatment-seeking: potential need and demand for infertility medical care. Hum. Reprod. 22, 1506–1512 (2007)

    Article  PubMed  Google Scholar 

  8. A. Hoek, J. Schoemaker, H.A. Drexhage, Premature ovarian failure and ovarian autoimmuity. Endocr. Rev. 18, 107–134 (1997)

    CAS  PubMed  Google Scholar 

  9. VandanaJha Aysha, Deepti Goswami, Premature ovarian failure: An association with autoimmune diseases. J. Clin. Diagn. Res. 10(10), QC10–QC10 (2016)

    Google Scholar 

  10. G.B. Nacak, E. Ozkaya, C.Y. Abide, B.E. Bilgic, B. Devranoglu, R.G. Iscan, The impact of autoimmunity-related early ovarian aging on ICSI cycle outcome. Gynecol. Endocrinol. 4, 1–4 (2018)

    Google Scholar 

  11. H.J.A. Carp, C. Selmi, Y. Shoenfeld, The autoimmune bases of infertility and pregnancy loss. J. Autoimmun. 38, 266–274 (2012)

    Article  CAS  Google Scholar 

  12. E.R. te Velde, G.J. Scheffer, M. Dorland, F.J. Broekmans, B.C. Fauser, Developmental and endocrine aspects of a normal ovarian aging. Mol. Cell. Endocrinol. 145, 67–73 (1998)

    Article  Google Scholar 

  13. E.R. te Velde, M. Dorland, F.J. Broekmans, Age at menopause as a marker of reproductive ageing. Maturitas 30, 119–125 (1998)

    Article  Google Scholar 

  14. Practice Committee of the American Society for Reproductive Medicine, Testing and interpreting measures of ovarian reserve: a committee opinion. Fertil. Steril. 103, e9–e17 (2015)

    Google Scholar 

  15. J.A. Visser, F.H. de Jong, J.S.E. Laven, A.P. Themmen, Anti-Mullerian hormone: a new marker for ovarian function. Soc. Reprod. Fertil. 131, 1–9 (2006)

    Article  CAS  Google Scholar 

  16. B. Wiweko, D.M.P. Prawesti, A. Hestiantoro, K. Sumapraja, M. Natadisastra, A. Baziad, Chronological age vs biological age: an age related normogram for antral follicl count; FSH and anti- Mullerian hormone. J. Assist. Reprod. Genet. 30, 1563–1567 (2013)

    Article  PubMed  PubMed Central  Google Scholar 

  17. C. Fiçicioglu, T. Kutlu, E. Baglam, Z. Bakacak, Early follicular antimüllerian hormone as an indicator of ovarian reserve. Fertil. Steril. 85, 592–596 (2006)

    Article  CAS  PubMed  Google Scholar 

  18. B. Vigier, J.Y. Picard, D. Tran, L. Legeai, N. Josso, Production of anti-Müllerian hormone: another homology between Sertoli and granulosa cells. Endocrinology 114, 1315–1320 (1984)

    Article  CAS  PubMed  Google Scholar 

  19. A. La Marca, A. Volpe, Anti-Mullerian hormone (AMH) in female reproduction: is measurement of circulating AMH a useful tool? Clin. Endocrinol. (Oxf.). 64, 603–610 (2006)

    Article  CAS  PubMed  Google Scholar 

  20. C.L. Cook, Y. Siow, S. Taylor, M.E. Fallat, Serum müllerian-inhibiting substance levels during normal mestrual cycles. Fertil. Steril. 73, 859–861 (2000)

    Article  CAS  PubMed  Google Scholar 

  21. D. Dewailly, C.Y. Andersen, A. Balen, F. Broekmans, N. Dilaver, R. Fanchin, G. Griesinger, T.W. Kelsey, A. La Marca, C. Lambalk, H. Mason, S.M. Nelson, J.A. Visser, W.H. Wallace, R.A. Anderson, The physiology and clinical utility of anti-Mullerian hormone in women. Hum. Reprod. Update 20, 370–385 (2014)

    Article  PubMed  Google Scholar 

  22. M.F. Brougham, P.M. Crofton, E.J. Johnson, N. Evans, R.A. Anderson, W.H. Wallace, Anti Müllerian Hormone is a marker of gonadotoxicity in pre- and postpuberal girls treated for cancer: a prospective study. J. Clin. Endocrinol. Metab. 97, 2059–2067 (2012)

    Article  CAS  PubMed  Google Scholar 

  23. J. Bala, S. Seth, R. Dhankhar, V.S. Ghalaut, Chemotherapy: Impact on Anti-Müllerian hormone levels in breast carcinoma. J. Clin. Diagn. Res. 10, BC19–21 (2016)

    CAS  PubMed  PubMed Central  Google Scholar 

  24. H. Browne, A. Armstrong, A. Decherney, R. Babb, G. Illei, J. Segars, S. Pavletic, Assessment of ovarian function with anti-Mullerian hormone in systemic lupus erythematosus patients undergoing hematopoietic stem cell transplant. Fertil. Steril. 91, 1529–1532 (2009)

    Article  CAS  PubMed  Google Scholar 

  25. B. Lawrenz, J. Henes, M. Henes, E. Neunhoeeffer, M. Schmalzing, T. Fehm, I. Kitter, Impact of systemic lupus erythematosus on ovarian reserve in premenopausal women: evaluation by using anti-Mullerian hormone. Lupus 20, 1193–1197 (2011)

    Article  CAS  PubMed  Google Scholar 

  26. C.C. Mok, P.T. Chan, C.H. To, Anti-müllerian hormone and ovarian reserve in systemic lupus erythematosus. Arthritis Rheum. 65, 206–210 (2013)

    Article  CAS  PubMed  Google Scholar 

  27. A.A. Gasparin, L. Souza, M. Siebert, R.M. Xavier, R.M. Chakr, P.E. Palominos, J.C. Brenol, O.A. Monticielo, Assessment of anti-Müllerian hormone levels in premenopausal patients with systemic lupus erythematosus. Lupus 25, 227–232 (2016)

    Article  CAS  PubMed  Google Scholar 

  28. M.C. Hochberg, Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 40, 1725 (1997)

    Article  CAS  PubMed  Google Scholar 

  29. Rotterdam ESHRE/ASRM- Sponsored PCOS Consensus Workshop Group, Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome. Fertil. Steril. 81(1), 19–25 (2004)

    Article  Google Scholar 

  30. C. Bombardier, D.D. Gladman, M.B. Urowitz, D. Caron, C.H. Chang, Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum. 35(6), 630–640 (1992)

    Article  CAS  PubMed  Google Scholar 

  31. MHRA. Urgent field safety notice—FSN 20434–3 AMH Gen II ELISA (REF A79765), 2013 (Accessed March 15, 2014)

  32. N. Morel, A. Bachelot, Z. Chakhtoura, P. Ghillani-Dalbin, Z. Amoura, L. Galicier, O. Aumaitre, J.C. Piette, J. Pourrat, D. Boutin, K. Sacre, J.E. Kahn, P. Duhaut, D. Farge, C. Francès, G. Guettrot-Imbert, J.R. Harlé, O. Lambotte, V. Le Guern, D. Sène, S. Trad, E. Vidal, F. Sarrot-Reynauld, A. Gompel, M.L. Tanguy, P. Touraine, J.M. Lacorte, N. Costedoat-Chalumeau; PLUS group, Study of Anti-Müllerian hormone and its relation to the subsequent probability of pregnancy in 112 patients with systemic lupus erythematosus, exposed or not cyclophosphamide. J. Clin. Endocrinol. Metab. 98, 3785–3792 (2013)

    Article  CAS  PubMed  Google Scholar 

  33. M. Gol, U. Saygili, M. Koyuncuoglu., T. Uslu, Influence of hight-dose methotrexate therapy on the primordial follicle of the mouse ovary. J. Obstet. Gynaecol. Res. 35(3), 429–433 (2009)

    Article  CAS  PubMed  Google Scholar 

  34. D.B. de Araujo, L.Y.S. Yamakami, N.E. Aikawa, E. Bonfà., V.S. Viana, S.G. Pasoto, R.M. Pereira, P.C. Serafin, E.F. Borba, C.A. Silva, Ovarian reserve in adult patients with childhood-onset lupus: a possible deleterious effect of methotrexate? Scand. J. Rheumatol. 43, 503–511 (2014)

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Rheumatology, Università Cattolica del Sacro Cuore, Rome, Italy

    Clara Di Mario, Valentina Varriano, Annamaria Paglionico, Gianfranco Ferraccioli & Elisa Gremese

  2. Division of Rheumatology, Fondazione Policlinico Universitario “A. Gemelli”—I.R.C.C.S., Rome, Italy

    Luca Petricca, Maria Rita Gigante, Gianfranco Ferraccioli, Barbara Tolusso & Elisa Gremese

  3. Institute of Biochemistry and Clinical Biochemistry, Università Cattolica del Sacro Cuore, Rome, Italy

    Angelina Barini

  4. Institute of Biochemistry and Clinical Biochemistry, Fondazione Policlinico Universitario “A. Gemelli”—I.R.C.C.S., Rome, Italy

    Angelina Barini & Antonella Barini

  5. Institute of Microbiology, Università Cattolica del Sacro Cuore, Rome, Italy

    Paola Cattani

  6. Institute of Microbiology, Fondazione Policlinico Universitario “A. Gemelli”—I.R.C.C.S., Rome, Italy

    Paola Cattani

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  1. Clara Di Mario
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Correspondence to Elisa Gremese.

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Di Mario, C., Petricca, L., Gigante, M.R. et al. Anti-Müllerian hormone serum levels in systemic lupus erythematosus patients: Influence of the disease severity and therapy on the ovarian reserve. Endocrine 63, 369–375 (2019). https://doi.org/10.1007/s12020-018-1783-1

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  • DOI: https://doi.org/10.1007/s12020-018-1783-1

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