Reproductive function in women with immune-mediated inflammatory rheumatic diseases

Vlasova G.A., Perminova S.G., Kosheleva N.M., Nazarenko T.A.

1) Academician V. I. Kulakov National Medical Research Center of Obstetrics, Gynecology, and Perinatology, Ministry of Health of Russia, Moscow; 2) V.A. Nasonova Research Institute of Rheumatology, Moscow, Russia
The paper presents a systematic analysis of the data available in the literature on immune-mediated inflammatory rheumatic diseases (IIRDs) and their therapy on the female reproductive system, as well as on the use of procedures for maintaining and implementing the reproductive function in this patient population receiving ART programs. The review includes Russian and foreign publications of Pubmed on this topic during 2010–2018. The authors conclude that there is a need for further investigations of the impact of IIRDs and their therapy on female reproductive function and for elaboration and clinical introduction of individual approaches to maintaining and implementing reproductive function in patients with IIRDs in the ART programs.

Keywords

immune-mediated inflammatory rheumatic diseases
infertility
systemic lupus erythematosus
rheumatoid arthritis
cytostatic therapy
diminished ovarian reserve
premature ovarian failure
GnRH analogues
oocyte/embryo cryopreservation
ART programs

References

  1. Насонов Е.Л., ред. Ревматология. Российские клинические рекомендации. М.: ГЭОТАР-Медиа; 2017. 456 с. [Nasonov EL, ed. Revmatologiya. Rossiyskie klinicheskie rekomendatsii/Rheumatology. Russian Clinical Recommendations. M.: GEOTAR-Media; 2017. 456 p.(In Russian)]
  2. Oktem O., Hande Y., Hale B., Bulent U. Reproductive aspects of systemic lupus erythematosus. J. Reprod. Immunol. 2016; 117: 57-65.https://doi.org/10.1016/j.jri.2016.07.001.
  3. Straub R.H., Bijlsma J.W., Masi A., Cutolo M. Role of neuroendocrine and neuroimmune mechanisms in chronic inflammatory rheumatic diseases - the 10-year update. Semin. Arthritis Rheum. 2013; 43(3): 392-404. https://doi.org/10.1016/j.semarthrit.2013.04.008.
  4. Colasanti T., Maselli A., Conti F. Autoantibodies to estrogen receptor α interfere with T lymphocyte homeostasis and are associated with disease activity in systemic lupus erythematosus (SLE). Arthritis Rheum. 2012; 64(3): 778-87. https://doi.org/10.1002/art.33400.
  5. Capellino S., Straub R.H., Cutolo M. Aromatase and regulation of the estrogen-to-androgen ratio in synovial tissue inflammation: common pathway in both sexes. Ann. N.Y. Acad. Sci. 2014; 1317: 24-31. https://doi.org/10.1111/nyas.12398.
  6. Cutolo M., Brizzolara R., Atzeni F., Capellino S., Straub R.H., Puttini P.C. The immunomodulatory effects of estrogens: clinical relevance in immune-mediated rheumatic diseases. Ann. N.Y. Acad. Sci. 2010; 1193: 36-42. https://doi.org/10.1111/j.1749-6632.2009.05383.x.
  7. Østensen M., Andreoli L., Brucato A., Cetin I., Chambers C., Clowse M. et al. State of the art: reproduction and pregnancy in rheumatic diseases. Autoimmun. Rev. 2015; 14(5): 376-86. https://doi.org/10.1016/j.autrev.2014.12.011.
  8. Østensen M. Sexual and reproductive health in rheumatic disease. Nat. Rev. Rheumatol. 2017; 13(8): 485-93. https://doi.org/10.1038/nrrheum.2017.102.
  9. Clowse M.E., Chakravarty E., Costenbader K.H., Chambers C., Michaud K. Effects of infertility, pregnancy loss, and patient concerns on family size of women with rheumatoid arthritis and systemic lupus erythematosus. Arthritis Care Res. (Hoboken). 2012; 64(5): 668-74. https://doi.org/10.1002/acr.21593.
  10. Andreoli L., Bertsias G.K., Agmon-Levin N., Brown S., Cervera R., Costedoat-Chalumeau N. et al. EULAR recommendations for women’s health and the management of family planning, assisted reproduction, pregnancy and menopause in patients with systemic lupus erythematosus and/or antiphospholipid syndrome. Ann. Rheum. Dis. 2017; 76(3): 476-85. https://doi.org/10.1136/annrheumdis-2016-209770.
  11. Van Sinderen M., Menkhorst E., Winship A., Cuman C., Dimitriadis E. Preimplantation human blastocyst-endometrial interactions: the role of inflammatory mediators. Am. J. Reprod. Immunol. 2013; 69(5): 427-40. https://doi.org/10.1111/aji.12038.
  12. Sowers M. Anti-Müllerian hormone and inhibin B variability during normal menstrual cycles. Fertil. Steril. 2010; 94(4): 1482-6. https://doi.org/10.1016/j.fertnstert.2009.07.1674.
  13. Henes M. Ovarian reserve alterations in premenopausal women with chronic inflammatory rheumatic diseases: impact of rheumatoid arthritis, Behcet’s disease and spondyloarthritis on anti Mullerian hormone levels. Rheumatology. 2015; 54(9): 1709-12. https://doi.org/10.1093/rheumatology/kev124.
  14. Brouwer J., Laven J.S., Hazes JM., Schipper I., Dolhain R.J. Levels of serum anti- Müllerian hormone, a marker for ovarian reserve, in women with rheumatoid arthritis. Arthritis Care Res. (Hoboken). 2013; 65(9): 1534-8. https://doi.org/10.1002/acr.22013.
  15. Somers E.C., Marder W. Infertility - prevention and management. Rheum. Dis. Clin. North Am. 2017; 43(2): 75-85. https://doi.org/10.1016/j.rdc.2016.12.007.
  16. Кошелева Н.М. Терапия генно-инженерными биологическими препаратами и беременность. В кн.: Насонов Е.Л., ред. Генно-инженерные биологические препараты в лечении ревматоидного артрита. М.: ИМА-ПРЕСС; 2013: 467-75. [Kosheleva N.M. Therapy by genetically engineered biological preparations and pregnancy. In: Genno-inzhenernye biologicheskie preparaty v lechenii revmatoidnogo artrita/Genetically engineered biological preparations in treatment of rheumatoid arthritis. Nasonov E.L., ed. М.: IМА-PRESS; 2013: 467-75.(In Russian)].
  17. Leroy C., Rigot J.M., Leroy M., Decanter C., Le Mapihan K., Parent A.S. et al. Immunosuppressive drugs and fertility. Orphanet J. Rare Dis. 2015; 10: 136. https://doi.org/10.1186/s13023-015-0332-8.
  18. Boumpas D.T., Austin H.A., Vaughan E.M., Yarboro C.H., Klippel J.H., Balow J.E. Risk for sustained amenorrhea in patients with systemic lupus erythematosus receiving intermittent pulse cyclophosphamide therapy. Ann. Intern. Med. 1993; 119(5): 366-9.
  19. Park M.C., Park Y.B., Jung S.Y., Chung I.H., Choi K.H., Lee S.K. Risk of ovarian failure and pregnancy outcome in patients with lupus nephritis treated with intravenous cyclophosphamide pulse therapy. Lupus. 2004; 13: 69-74. https://doi.org/0.1191/0961203304lu1063oa.
  20. Mok C.C., Chan P.T., To C.H. Anti-Müllerian hormone and ovarian reserve in systemic lupus erythematosus. Arthritis Rheum. 2013; 65(1): 206-10. https://doi.org/10.1002/art.37719.
  21. Clowse M.E., Copland S.C., Hsieh T.C., Chow S.C., Hoffman G.S., Merkel P.A. et al. Ovarian reserve diminished by oral cyclophosphamide therapy for granulomatosis with polyangiitis (Wegener’s). Arthritis Care Res. (Hoboken). 2011; 63(12): 1777-81. https://doi.org/10.1002/acr.20605.
  22. Akawatcharangura P., Taechakraichana N., Osiri M. Prevalence of premature ovarian failure in systemic lupus erythematosus patients treated with immunosuppressive agents in Thailand. Lupus. 2016; 25(4): 436-44. https://doi.org/10.1177/0961203315617539.
  23. Brunner H.I., Silva C.A., Reiff A., Higgins G.C., Imundo L., Williams C.B. et al. Randomized, double-blind, dose-escalation trial of triptorelin for ovary protection in childhood-onset systemic lupus erythematosus. Arthritis Rheumatol. 2015; 67(5): 1377-85. https://doi.org/10.1002/art.39024.37719.
  24. Kim M., Rostas S., Gabardi S. Mycophenolate fetal toxicity and risk evaluation and mitigation strategies. Am. J. Transplant. 2013; 13(6): 1383-9. https://doi.org/10.1111/ajt.12238.
  25. Hill M.J., Cooper J.C., Levy G., Alford C., Richter K.S., DeCherney A.H. et al. Ovarian reserve and subsequent assisted reproduction outcomes after methotrexate therapy for ectopic pregnancy or pregnancy of unknown location. Fertil. Steril. 2014; 101(2): 413-9. https://doi.org/10.1016/j.fertnstert.2013.10.027.
  26. Garritsen F.M., van den Broek M.P.H., van Zuilen A.D., Fidder H.H., de Bruin-Weller M.S., Spuls P.I. Pregnancy and fetal outcomes after paternal exposure to azathioprine, methotrexate or mycophenolic acid: a critically appraised topic. Br. J. Dermatol. 2017; 176(4): 866-77.1 https://doi.org/0.1111/bjd.15320.
  27. Flint J., Panchal S., Hurrell A., van de Venne M., Gayed M., Schreiber K.et al. BSR and BHPR guideline on prescribing drugs in pregnancy and breastfeedingPart I: standard and biologic disease modifying anti-rheumatic drugs and corticosteroids. Rheumatology (Oxford). 2016; 55(9): 1693-7. https://doi.org/10.1093/rheumatology/kev404.
  28. Riley S.A., Lecarpentier J., Mani V., Goodman M.J., Mandal B.K., Turnberg LA. Sulphasalazine induced seminal abnormalities in ulcerative colitis: results of mesalazine substitution. Gut. 1987; 28(8): 1008-12.
  29. Imseis H.M., Zimmerman P.D., Samuels P., Kniss D.A. Tumor necrosis factor-alfa induces cyclo-oxygenase-2 gene expression in first trimester trophoblasts: suppression by glucocorticoids and NSAIDs. Pancenta. 1997; 18(7): 521-6.
  30. Daher S., Fonseca F., Ribero O., Musatti C., Gerbase de Lima M. Tumor necrosis factor during pregnancy. Eur. J. Obstet. Gynecol. Reprod. Biol. 1999; 83(1): 77-9.
  31. Yu X.W., Yan C.F., Jin H.L., Li X. Tumor necrosis factor receptor 1 expression and early spontaneous abortion. Int. J. Gynaecol. Obstet. 2005; 88(1): 44-8.
  32. Treacy G. Using an analogous monoclonal antibody to evaluate the reproductive and chronic toxicity potential for a humanized anti-TNF-α monoclonal antibody. Hum. Exp. Toxicol. 2000; 19(4): 226-8.
  33. Levy R.A., de Jesus G.R., de Jesus N.R., Klumb E.M. Critical review of the current recommendations for the treatment of systemic inflammatory rheumatic diseases during pregnancy and lactation. Autoimmun. Rev. 2016; 15(10): 955-63. https://doi.org/10.1016/j.autrev.2016.07.014.
  34. Whirledge S., Cidlowski J.A. Glucocorticoids, stress and fertility. Minerva Endocrinol. 2010; 35(2): 109-25.
  35. Brouwer J., Hazes J.M., Laven J.S., Dolhain R.J. Fertility in women with rheumatoid arthritis: influence of disease activity and medication. Ann. Rheum. Dis. 2015; 74(10): 1836-41. https://doi.org/10.1136/annrheumdis-2014-205383.
  36. Micu M.C., Micu R., Ostensen M. Luteinized unruptured follicle syndrome increased by inactive disease and selective cyclooxygenase 2 inhibitors in women with inflammatory arthropathies. Arthritis Care Res. (Hoboken). 2011; 63(9): 1334-8. https://doi.org/10.1002/acr.20510.
  37. Kailasam C., Hunt L.P., Ryder I., Bhakri I., Gordon U.D. Safety and effectiveness of diclofenac sodium in assisted reproduction treatment: a randomized prospective double-blind study. Reprod. Biomed. Online. 2008; 16(5): 724-9.
  38. Loren A.W., Mangu P.B., Nohr Beck L., Brennan L., Magdalinski A.J., Partridge A.H. et al. Fertility preservation for patients with cancer: American Society of Clinical Oncology Clinical Practice Guideline Update. J. Clin. Oncol. 2013; 31(19): 2500-10. https://doi.org/10.1200/JCO.2013.49.2678.
  39. Smith B.M., Duncan F.E., Ataman L., Smith K., Quinn G.P., Chang R.J. et al. The National Physicians Cooperative: transforming fertility management in the cancer setting and beyond. Future Oncol. 2018; 14(29): 3059-72. https://doi.org/10.2217/fon-2018-0278.
  40. Blumenfeld Z., Zur H., Dann E.J. Gonadotropin-releasing hormone agonist cotreatment during chemotherapy may increase pregnancy rate in survivors. Oncologist. 2015; 20(11): 1283-9. https://doi.org/10.1634/theoncologist.2015-0223.
  41. Marder W., Fisseha S., Ganser M.A., Somers E.C. Ovarian damage during chemotherapy in autoimmune diseases: broad health implications beyond fertility. Clin. Med. Insights Reprod. Health. 2012; 6: 9-18.
  42. Moore H.C., Unger J.M., Phillips K.A., Boyle F., Hitre E., Porter D. et al. Goserelin for ovarian protection during breast-cancer adjuvant chemotherapy. N. Engl. J. Med. 2015; 372(10): 923-32. https://doi.org/10.1056/NEJMoa1413204.
  43. Somers E.C., Marder W., Christman G.M., Ognenovski V., McCune W.J. Use of a gonadotropin-releasing hormone analog for protection against premature ovarian failure during cyclophosphamide therapy in women with severe lupus. Arthritis Rheum. 2005; 52(9): 2761-7. https://doi.org/10.1002/art.21263.
  44. Blumenfeld Z., Evron A. Preserving fertility when choosing chemotherapy regimens – the role of gonadotropin-releasing hormone agonists. Expert Opin. Pharmacother. 2015; 16(7): 1009-20. https://doi.org/10.1517/14656566.2015.1031654.
  45. Ladanyi C., Mor A., Christianson M.S., Dhillon N., Segars J.H. Recent advances in the field of ovarian tissue cryopreservation and opportunities for research. J. Assist. Reprod. Genet. 2017; 34(6): 709-22. https://doi.org/10.1007/s10815-017-0899-1.
  46. Youssef M.A., Van der Veen F., Al-Inany H.G., Mochtar M.H., Griesinger G., Nagi Mohesen M. et al. Gonadotropin-releasing hormone agonist versus HCG for oocyte triggering in antagonist-assisted reproductive technology. Cochrane Database Syst. Rev. 2014; 31(10): CD008046. https://doi.org/10.1002/14651858
  47. Краснопольская К.В., Назаренко Т.А., Сесина Н.И., Александрова В.Р. Программы экстракорпорального оплодотворения с эмбрионами, полученными из витрифицированных и нативных ооцитов донора. Акушерство и гинекология. 2017; 3: 75-80. [Krasnopol’skaya K.V., Nazarenko T.A., Sesina N.I., Aleksandrova V.R. Programmy ekstrakorporal’nogo oplodotvoreniya s embrionami, poluchennymi iz vitrifitsirovannykh i nativnykh ootsitov donora. Akusherstvo i ginekologiya. 2017; 3:75-80. (In Russian)]. doi: https://dx.doi.org/10.18565/aig.2017.3.75-80.
  48. Cobo A., Garcia-Velasco J.A., Coello A., Domingo J., Pellicer A., Remohi J. Oocyte vitrification as an efficient option for elective fertility preservation. Fertil. Steril. 2016; 105(3): 755-64. https://doi.org/10.1016/j.fertnstert.2015.11.027.
  49. Goldman R.H., Racowsky C., Farland L.V., Munne S., Ribustello L., Fox J.H. Predicting the likelihood of live birth for elective oocyte cryopreservation: a counseling tool for physicians and patients. Hum. Reprod. 2017; 32(4): 853-9. https://doi.org/10.1093/humrep/dex008.
  50. Donnez J., Godin P.A., Qu J., Nisolle M. Gonadal cryopreservation in the young patient with gynaecological malignancy. Curr. Opin. Obstet. Gynecol. 2000; 12(1): 1-9.
  51. Di Nisio M., Rutjes A.W., Ferrante N., Tiboni G.M., Cuccurullo F., Porreca E. Thrombophilia and outcomes of assisted reproduction technologies: a systematic review and meta-analysis. Blood. 2011; 118(10): 2670-8. https://doi.org/10.1182/blood-2011-03-340216.
  52. Orquevaux P., Masseau A., Le Guern V., Gayet V., Vauthier D., Guettrot-Imbert G. et al. In vitro fertilization in 37 women with systemic lupus erythematosus or antiphospholipid syndrome: a series of 97 procedures. J. Rheumatol. 2017; 44(5): 613-8.https://doi.org/10.3899/jrheum.160462.
  53. Henriksson P., Westerlund E., Wallén H., Brandt L., Hovatta O., Ekbom A. Incidence of pulmonary and venous thromboembolism in pregnancies after in vitro fertilisation: cross sectional study. BMJ. 2015; 346: e8632. https://doi.org/10.1136/bmj.e8632.
  54. Humaidan P., Polyzos N.P., Alsbjerg B., Erb K., Mikkelsen A.L., Elbaek H.O. et al. GnRHa trigger and individualized luteal phase hCG support according to ovarian response to stimulation: two prospective randomized controlled multi-centre studies in IVF patients. Hum. Reprod. 2013; 28(9): 2511-21. https://doi.org/10.1093/humrep/det249.
  55. Henes M., Henes J.C., Neunhoeffer E., Von Wolff M., Schmalzing M., Kötter I. et al. Fertility preservation methods in young women with systemic lupus erythematosus prior to cytotoxic therapy: experiences from the FertiPROTEKT network. Lupus. 2012; 21(9): 953-8. https://doi.org/10.1177/0961203312442753.

Received 16.04.2019

Accepted 19.04.2019

About the Authors

Galina A.Vlasova, graduate student of 1st gynecology department, Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia.
Tel.: +79153220879. E-mail: galinavlasova089@gmail.com
117997 Russia, Moscow, Ac. Oparina str. 4.
Svetlana G. Perminova, MD, PhD, leading researcher of 1st gynecology department, Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health of Russia. Tel.: +79153220879.E-mail: perisvet@list.ru
117997 Russia, Moscow, Ac. Oparina str. 4.
Nadezhda M. Kosheleva, MD, Rheumatologist, PhD, Senior scientific researcher of the Laboratory of Vascular Rheumatology, V.A. Nasonova Research Rheumatology Institute. Tel.: +74951092910. E-mail: nadkosheleva@yandex.ru
115522 Russia, Moscow, Kashirskoye Shosse 34A.
Tatiana A. Nazarenko, MD, PhD, Head of the Institute of Reproductive Technologies, Research Center of Obstetrics, Gynecology and Perinatology, Ministry of Health
of Russia. Tel.: +79153220879.E-mail: t.nazarenko@mail.ru
117997 Russia, Moscow, Ac. Oparina str. 4.

For citation: Vlasova G.A., Perminova S.G., Kosheleva N.M., Nazarenko T.A. Reproductive function in women with immune-mediated inflammatory rheumatic diseases.
Akusherstvo i Ginekologiya/ Obstetrics and gynecology. 2019; 10: 51-59. (In Russian).
https://dx.doi.org/10.18565/aig.2019.10.51-59

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