Skip to main content

Advertisement

Log in

Fertility and infertility implications in rheumatoid arthritis; state of the art

  • Review
  • Published:
Inflammation Research Aims and scope Submit manuscript

Abstract

Background

A bulk of investigations imply that women with rheumatoid arthritis (RA) deliver fewer children in comparison to healthy women.

Purpose

This review article attempts to clarify the involvement of infertility-related issues in both RA men and women. Moreover, the effect of RA disease on the fertility quality and quantity will be discussed.

Results

Declined fertility rate in RA women seems to stem from modified inflammatory settings, advanced maternal age, limited sexual activity, and adverse effects of drugs on ovarian function. Women with RA may have smaller families and seem to be slower to conceive relative to their peer women. The chance of gestation in RA women may drop due to suppressed sexual function through pain and fatigue. In addition, treatment of RA women with non-steroidal anti-inflammatory drugs (NSAIDs) may prevent ovulation and therefore hinder the conception.

Conclusions

A complex interaction between RA disease and fertility related issues is present. Despite an increase rate of infertility in RA females or males, the mechanisms involved in this outcome is still unknown. Plausible causes of the decreased fertility rate in RA patients might be due to inflammatory cytokines, suppressed sexual activity, drug treatments, mother age, personal choice, or a combination of these elements.

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.

Fig. 1

Similar content being viewed by others

References

  1. Wallenius M, Skomsvoll JF, Irgens LM, Salvesen KÅ, Nordvåg B-Y, Koldingsnes W, et al. Fertility in women with chronic inflammatory arthritides. Rheumatology. 2011;50:1162–7.

    PubMed  Google Scholar 

  2. Wallenius M, Skomsvoll J, Irgens L, Salvesen K, Nordvåg B, Koldingsnes W, et al. Parity in patients with chronic inflammatory arthritides childless at time of diagnosis. Scand J Rheumatol. 2012;41:202–7.

    CAS  PubMed  Google Scholar 

  3. Skomsvoll JF, Ostensen M, Baste V, Irgens LM. Number of births, interpregnancy interval, and subsequent pregnancy rate after a diagnosis of inflammatory rheumatic disease in Norwegian women. J Rheumatol. 2001;28:2310–4.

    CAS  PubMed  Google Scholar 

  4. Förger F, Vallbracht I, Helmke K, Villiger PM, Ostensen M. Pregnancy mediated improvement of rheumatoid arthritis. Swiss Med Wkly. 2012;142:w13644.

    PubMed  Google Scholar 

  5. Østensen M, Villiger PM, Förger F. Interaction of pregnancy and autoimmune rheumatic disease. Autoimmun Rev. 2012;11:A437–A446446.

    PubMed  Google Scholar 

  6. Østensen M, Villiger PM. The remission of rheumatoid arthritis during pregnancy. Semin Immunopathol. 2007;29:185–91. https://doi.org/10.1007/s00281-007-0072-5.

    Article  PubMed  Google Scholar 

  7. Förger F, Villiger PM. Immunological adaptations in pregnancy that modulate rheumatoid arthritis disease activity. Nat Rev Rheumatol. 2020;16:113–22. https://doi.org/10.1038/s41584-019-0351-2.

    Article  PubMed  Google Scholar 

  8. Del Junco D, Annegers J, Coulam C, Luthra HS. The relationship between rheumatoid arthritis and reproductive function. Br J Rheumatol. 1989;28:33.

    PubMed  Google Scholar 

  9. Tsepelidis S, Devreker F, Demeestere I, Flahaut A, Gervy C, Englert Y. Stable serum levels of anti-Müllerian hormone during the menstrual cycle: a prospective study in normo-ovulatory women. Hum Reprod. 2007;22:1837–40.

    CAS  PubMed  Google Scholar 

  10. Leverenz DL, Eudy AM, Jayasundara M, Haroun T, McDaniel G, Nowell WB, et al. Contraception methods used by women with rheumatoid arthritis and psoriatic arthritis. Clin Rheumatol. 2019;38:1207–12.

    PubMed  Google Scholar 

  11. Provost M, Eaton JL, Clowse ME. Fertility and infertility in rheumatoid arthritis. Curr Opin Rheumatol. 2014;26:308–14.

    PubMed  Google Scholar 

  12. Katz PP. Childbearing decisions and family size among women with rheumatoid arthritis. Arthritis Care Res. 2006;55:217–23.

    Google Scholar 

  13. Clowse ME, Chakravarty E, Costenbader KH, 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. 2012;64:668–74.

    Google Scholar 

  14. Eudy AM, McDaniel G, Hurd WW, Clowse ME. Fertility and ovarian reserve among women with rheumatoid arthritis. J Rheumatol. 2019;46:455–9.

    CAS  PubMed  Google Scholar 

  15. Brouwer J, Laven JS, Hazes JM, Schipper I, Dolhain RJ. Levels of Serum anti-müllerian hormone, a marker for ovarian reserve, in women with rheumatoid arthritis. Arthritis Care Res. 2013;65:1534–8.

    CAS  Google Scholar 

  16. Silman A, Roman E, Beral V, Brown A. Adverse reproductive outcomes in women who subsequently develop rheumatoid arthritis. Ann Rheum Dis. 1988;47:979.

    CAS  PubMed  PubMed Central  Google Scholar 

  17. Spector TD, Silman A. Is poor pregnancy outcome a risk factor in rheumatoid arthritis? Ann Rheum Dis. 1990;49:12.

    CAS  PubMed  PubMed Central  Google Scholar 

  18. Nørgård BM, Larsen MD, Friedman S, Knudsen T, Fedder J. Decreased chance of a live born child in women with rheumatoid arthritis after assisted reproduction treatment: a nationwide cohort study. Ann Rheum Dis. 2019;78:328–34.

    PubMed  Google Scholar 

  19. Chakravarty EF, Nelson L, Krishnan E. Obstetric hospitalizations in the United States for women with systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheumatol. 2006;54:899–907.

    Google Scholar 

  20. Lin H, Chen S, Lin H, et al. Increased risk of adverse pregnancy outcomes in women with rheumatoid arthritis: a nationwide population-based study. Ann Rheum Dis. 2010;69:715–7.

    PubMed  Google Scholar 

  21. Bowden AP, Barrett JH, Fallow W, Silman AJ. Women with inflammatory polyarthritis have babies of lower birth weight. J Rheumatol. 2001;28:355–9.

    CAS  PubMed  Google Scholar 

  22. Kishore S, Mittal V, Majithia V. Obstetric outcomes in women with rheumatoid arthritis: results from nationwide inpatient sample database 2003–2011✰. Semin Arthritis Rheum. 2019;49(2):236–40.

    PubMed  Google Scholar 

  23. Aljary H, Czuzoj-Shulman N, Spence AR, Abenhaim HA. Pregnancy outcomes in women with rheumatoid arthritis: a retrospective population-based cohort study. J Maternal-Fetal Neonatal Med. 2020;33(4):618–24. https://doi.org/10.1080/14767058.2018.1498835.

    Article  Google Scholar 

  24. Jethwa H, Lam S, Smith C, Giles I. Does rheumatoid arthritis really improve during pregnancy? A systematic review and metaanalysis. J Rheumatol. 2019;46:245–50.

    PubMed  Google Scholar 

  25. Jabbour H, Sales K. Prostaglandin receptor signalling and function in human endometrial pathology. Trends Endocrinol Metab. 2004;15:398–404.

    CAS  PubMed  Google Scholar 

  26. Rashid NA, Lalitkumar S, Lalitkumar PG, Gemzell-Danielsson K. Endometrial receptivity and human embryo implantation. Am J Reprod Immunol. 2011;66:23–30.

    PubMed  Google Scholar 

  27. Gemzell-Danielsson K, Hamberg M. Endocrinology: the effect of antiprogestin (RU 486) and prostaglandin biosynthesis inhibitor (naproxen) on uterine fluid prostaglandin F2α concentrations. Hum Reprod. 1994;9:1626–30.

    CAS  PubMed  Google Scholar 

  28. King AE, Critchley HO. Oestrogen and progesterone regulation of inflammatory processes in the human endometrium. J Steroid Biochem Mol Biol. 2010;120:116–26.

    CAS  PubMed  Google Scholar 

  29. Dawood MY. Nonsteroidal anti-inflammatory drugs and reproduction. Am J Obstet Gynecol. 1993;169:1255–65.

    CAS  PubMed  Google Scholar 

  30. Eppig JJ. Prostaglandin E2 stimulates cumulus expansion and hyaluronic acid synthesis by cumuli oophori isolated from mice. Biol Reprod. 1981;25:191–5.

    CAS  PubMed  Google Scholar 

  31. Hizaki H, Segi E, Sugimoto Y, Hirose M, Saji T, Ushikubi F, et al. Abortive expansion of the cumulus and impaired fertility in mice lacking the prostaglandin E receptor subtype EP2. Proc Natl Acad Sci. 1999;96:10501–6.

    CAS  PubMed  PubMed Central  Google Scholar 

  32. Reich R, Daphna-Iken D, Chun S, Popliker M, Slager R, Adelmann-Grill B, et al. Preovulatory changes in ovarian expression of collagenases and tissue metalloproteinase inhibitor messenger ribonucleic acid: role of eicosanoids. Endocrinology. 1991;129:1869–75.

    CAS  PubMed  Google Scholar 

  33. Markosyan N, Duffy DM. Prostaglandin E2 acts via multiple receptors to regulate plasminogen-dependent proteolysis in the primate periovulatory follicle. Endocrinology. 2008;150:435–44.

    PubMed  PubMed Central  Google Scholar 

  34. Hester KE, Harper MJ, Duffy DM. Oral administration of the cyclooxygenase-2 (COX-2) inhibitor meloxicam blocks ovulation in non-human primates when administered to simulate emergency contraception. Hum Reprod. 2009;25:360–7.

    PubMed  Google Scholar 

  35. Duffy DM, Stouffer RL. Follicular administration of a cyclooxygenase inhibitor can prevent oocyte release without alteration of normal luteal function in rhesus monkeys. Hum Reprod. 2002;17:2825–31.

    CAS  PubMed  Google Scholar 

  36. Duffy DM, Stouffer RL. The ovulatory gonadotrophin surge stimulates cyclooxygenase expression and prostaglandin production by the monkey follicle. MHR Basic Sci Reprod Med. 2001;7:731–9.

    CAS  Google Scholar 

  37. McCann NC, Lynch TJ, Kim SO, Duffy DM. The COX-2 inhibitor meloxicam prevents pregnancy when administered as an emergency contraceptive to nonhuman primates. Contraception. 2013;88:744–8.

    CAS  PubMed  Google Scholar 

  38. Yoshinaga K. Uterine receptivity for blastocyst implantation. Ann N Y Acad Sci. 1988;541:424–31.

    CAS  PubMed  Google Scholar 

  39. Dimitriadis E, White C, Jones R, Salamonsen L. Cytokines, chemokines and growth factors in endometrium related to implantation. Human Reprod Update. 2005;11:613–30.

    CAS  Google Scholar 

  40. Brouwer J, Hazes JMW, Laven JSE, et al. Fertility in women with rheumatoid arthritis: influence of disease activity and medication. Ann Rheum Dis. 2015;74:1836–41.

    CAS  PubMed  Google Scholar 

  41. Akintayo RO, Aworinde OO, Ojo O, Akintayo FC, Akinlade OM, Awodun RO, et al. Is rheumatoid arthritis an innocent bystander in female reproductive problems? A comparative study of fertility in Nigerian women with and without rheumatoid arthritis. European J Rheumatol. 2018;5:179.

    Google Scholar 

  42. Ince-Askan H, Dolhain RJ. Pregnancy and rheumatoid arthritis. Best Pract Res Clin Rheumatol. 2015;29:580–96.

    PubMed  Google Scholar 

  43. Saketos M, Sharma N, Santoro NF. Suppression of the hypothalamic–pituitary–ovarian axis in normal women by glucocorticoids. Biol Reprod. 1993;49:1270–6.

    CAS  PubMed  Google Scholar 

  44. Whirledge S, Cidlowski JA. A role for glucocorticoids in stress-impaired reproduction: beyond the hypothalamus and pituitary. Endocrinology. 2013;154:4450–68.

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Gordon D, Beastall G, Thomson J, Sturrock R. Androgenic status and sexual function in males with rheumatoid arthritis and ankylosing spondylitis. QJM Int J Med. 1986;60:671–9.

    CAS  Google Scholar 

  46. O'moráin C, Smethurst P, Doré CJ, Levi A. Reversible male infertility due to sulphasalazine: studies in man and rat. Gut. 1984;25:1078–84.

    PubMed  PubMed Central  Google Scholar 

  47. Visser K, Katchamart W, Loza E, Martinez-Lopez J, Salliot C, Trudeau J, et al. Multinational evidence-based recommendations for the use of methotrexate in rheumatic disorders with a focus on rheumatoid arthritis: integrating systematic literature research and expert opinion of a broad international panel of rheumatologists in the 3E Initiative. Ann Rheum Dis. 2009;68:1086–93.

    CAS  PubMed  Google Scholar 

  48. Wallenius M, Lie E, Daltveit AK, Salvesen KÅ, Skomsvoll JF, Kalstad S, et al. Brief report: no excess risks in offspring with paternal preconception exposure to disease-modifying antirheumatic drugs. Arthritis Rheumatol. 2015;67:296–301.

    CAS  PubMed  Google Scholar 

  49. Weber-Schoendorfer C, Hoeltzenbein M, Wacker E, Meister R, Schaefer C. No evidence for an increased risk of adverse pregnancy outcome after paternal low-dose methotrexate: an observational cohort study. Rheumatology. 2013;53:757–63.

    PubMed  Google Scholar 

  50. Millsop JW, Heller MM, Eliason MJ, Murase JE. Dermatological medication effects on male fertility. Dermatol Ther. 2013;26:337–46.

    PubMed  Google Scholar 

  51. Puchner R, Danninger K, Puchner A, Pieringer H. Impact of TNF-blocking agents on male sperm characteristics and pregnancy outcomes in fathers exposed to TNF-blocking agents at time of conception. Clin Exp Rheumatol. 2012;30:765–7.

    PubMed  Google Scholar 

  52. Ramonda R, Foresta C, Ortolan A, Bertoldo A, Oliviero F, Lorenzin M, et al. Influence of tumor necrosis factor α inhibitors on testicular function and semen in spondyloarthritis patients. Fertil Steril. 2014;101:359–65.

    CAS  PubMed  Google Scholar 

  53. Micu MC, Micu R, Surd S, Gîrlovanu M, Bolboacă SD, Ostensen M. TNF-α inhibitors do not impair sperm quality in males with ankylosing spondylitis after short-term or long-term treatment. Rheumatology. 2014;53:1250–5.

    CAS  PubMed  Google Scholar 

  54. Whirledge S, Cidlowski JA. Glucocorticoids, stress, and fertility. Minerva Endocrinol. 2010;35:109.

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Martini AC, Molina RI, Tissera AD, Ruiz RD, De Cuneo MF. Analysis of semen from patients chronically treated with low or moderate doses of aspirin-like drugs. Fertil Steril. 2003;80:221–2.

    PubMed  Google Scholar 

  56. Reed SD, Vollan TA, Svec MA. Pregnancy outcomes in women with rheumatoid arthritis in Washington State. Matern Child Health J. 2006;10:361–6.

    PubMed  Google Scholar 

  57. Wolfberg AJ, Lee-Parritz A, Peller AJ, Lieberman ES. Association of rheumatologic disease with preeclampsia. Obstet Gynecol. 2004;103:1190–3.

    PubMed  Google Scholar 

  58. Nørgaard M, Larsson H, Pedersen L, Granath F, Askling J, Kieler H, et al. Rheumatoid arthritis and birth outcomes: a Danish and Swedish nationwide prevalence study. J Intern Med. 2010;268:329–37.

    PubMed  Google Scholar 

  59. Bharti B, Lee SJ, Lindsay SP, Wingard DL, Jones KL, Lemus H, et al. Disease severity and pregnancy outcomes in women with rheumatoid arthritis: results from the organization of teratology information specialists autoimmune diseases in pregnancy project. J Rheumatol. 2015;42:1376–82.

    PubMed  Google Scholar 

  60. Ince-Askan H, Mandaviya PR, Felix JF, Duijts L, van Meurs JB, Hazes JM, et al. Altered DNA methylation in children born to mothers with rheumatoid arthritis during pregnancy. Ann Rheum Dis. 2019;78:1198–204.

    CAS  PubMed  Google Scholar 

  61. de Man YA, Hazes JM, van der Heide H, Willemsen SP, de Groot CJ, Steegers EA, et al. Association of higher rheumatoid arthritis disease activity during pregnancy with lower birth weight: results of a national prospective study. Arthritis Rheumatol. 2009;60:3196–206.

    Google Scholar 

  62. Ong KK, Dunger DB. Perinatal growth failure: the road to obesity, insulin resistance and cardiovascular disease in adults. Best Pract Res Clin Endocrinol Metab. 2002;16:191–207.

    CAS  PubMed  Google Scholar 

  63. Leunissen RW, Kerkhof GF, Stijnen T, Hokken-Koelega A. Timing and tempo of first-year rapid growth in relation to cardiovascular and metabolic risk profile in early adulthood. JAMA. 2009;301:2234–42.

    CAS  PubMed  Google Scholar 

  64. Steenwinkel F, Hokken-Koelega A, Ridder MA, Hazes JM, Dolhain RJ. Rheumatoid arthritis during pregnancy and postnatal catch-up growth in the offspring. Arthritis Rheumatol. 2014;66:1705–11.

    PubMed  Google Scholar 

  65. de Steenwinkel FD, Hokken-koelega AC, Hazes J, Dolhain RJ. Does elevated disease activity or medication use influence the bone density of the prepubertal offspring in pregnant women with rheumatoid arthritis? Arthritis Rheum. 2013;65:S172.

    Google Scholar 

  66. Ince-Askan H, Hazes JMW, Dolhain R. Breastfeeding among women with rheumatoid arthritis compared with the general population: results from a nationwide prospective cohort study. J Rheumatol. 2019;46(9):1067–74. https://doi.org/10.3899/jrheum.180805.

    Article  CAS  PubMed  Google Scholar 

  67. Murray KE, Moore L, O’Brien C, Clohessy A, Brophy C, Minnock P, et al. Updated pharmacological management of rheumatoid arthritis for women before, during, and after pregnancy, reflecting recent guidelines. Ir J Med Sci. 2019;188:169–72 (1971-).

    CAS  PubMed  Google Scholar 

  68. Østensen M, Andreoli L, Brucato A, Cetin I, Chambers C, Clowse ME, et al. State of the art: reproduction and pregnancy in rheumatic diseases. Autoimmun Rev. 2015;14:376–86.

    PubMed  Google Scholar 

  69. Østensen M, Khamashta M, Lockshin M, Parke A, Brucato A, Carp H, et al. Anti-inflammatory and immunosuppressive drugs and reproduction. Arthritis Res Ther. 2006;8:209.

    PubMed  PubMed Central  Google Scholar 

  70. Bermas BL. Non-steroidal anti inflammatory drugs, glucocorticoids and disease modifying anti-rheumatic drugs for the management of rheumatoid arthritis before and during pregnancy. Curr Opin Rheumatol. 2014;26:334–40.

    CAS  PubMed  Google Scholar 

  71. Skorpen CG, Hoeltzenbein M, Tincani A, Fischer-Betz R, Elefant E, Chambers C, et al. The EULAR points to consider for use of antirheumatic drugs before pregnancy, and during pregnancy and lactation. Ann Rheum Dis. 2016;75:795–810.

    CAS  Google Scholar 

  72. Weber-Schoendorfer C, Chambers C, Wacker E, Beghin D, Bernard N, NoFP C, et al. Pregnancy outcome after methotrexate treatment for rheumatic disease prior to or during early pregnancy: a prospective multicenter cohort study. Arthritis Rheumatol. 2014;66:1101–10.

    CAS  PubMed  Google Scholar 

  73. Brent RL. Utilization of animal studies to determine the effects and human risks of environmental toxicants (drugs, chemicals, and physical agents). Pediatrics. 2004;113:984–95.

    PubMed  Google Scholar 

  74. Cassina M, Johnson D, Robinson L, Braddock S, Xu R, Jimenez J, et al. Pregnancy outcome in women exposed to leflunomide before or during pregnancy. Arthritis Rheum. 2012;64:2085–94.

    CAS  PubMed  Google Scholar 

  75. Chambers CD, Johnson DL, Robinson LK, Braddock SR, Xu R, Lopez-Jimenez J, et al. Birth outcomes in women who have taken leflunomide during pregnancy. Arthritis Rheum. 2010;62:1494–503.

    PubMed  PubMed Central  Google Scholar 

  76. Weber-Schoendorfer C, Oppermann M, Wacker E, Bernard N, centres noFp, Beghin D, et al. Pregnancy outcome after TNF-α inhibitor therapy during the first trimester: a prospective multicentre cohort study. Br J Clin Pharmacol. 2015;80:727–39.

    CAS  PubMed  PubMed Central  Google Scholar 

  77. Chaudrey KH, Kane SV. Safety of immunomodulators and anti-TNF therapy in pregnancy. Curr Treat Options Gastroenterol. 2015;13:77–89.

    PubMed  Google Scholar 

  78. Eworuke E, Panucci G, Goulding M, Neuner R, Toh S. Use of tumor necrosis factor-alpha inhibitors during pregnancy among women who delivered live born infants. Pharmacoepidemiol Drug Saf. 2019;28:296–304.

    CAS  PubMed  Google Scholar 

  79. Kawai Y, Tsuchiya T, Aoki S. Pregnancy outcomes of patients exposed to adalimumab in Japan. Dig Dis. 2019;37:123–30.

    PubMed  Google Scholar 

  80. Malek A, Sager R, Kuhn P, Nicolaides KH, Schneider H. Evolution of maternofetal transport of immunoglobulins during human pregnancy. Am J Reprod Immunol. 1996;36:248–55.

    CAS  PubMed  Google Scholar 

  81. Mahadevan U, Wolf DC, Dubinsky M, Cortot A, Lee SD, Siegel CA, et al. Placental transfer of anti–tumor necrosis factor agents in pregnant patients with inflammatory bowel disease. Clin Gastroenterol Hepatol. 2013;11:286–92.

    CAS  PubMed  Google Scholar 

  82. Berthelsen BG, Fjeldsøe-Nielsen H, Nielsen CT, Hellmuth E. Etanercept concentrations in maternal serum, umbilical cord serum, breast milk and child serum during breastfeeding. Rheumatology. 2010;49:2225–7.

    CAS  PubMed  Google Scholar 

  83. Hyrich KL, Verstappen SM. Biologic therapies and pregnancy: the story so far. Rheumatology. 2013;53:1377–85.

    PubMed  Google Scholar 

  84. Brooks P. Use and benefits of nonsteroidal anti-inflammatory drugs. Am J Med. 1998;104:9S–13S.

    CAS  PubMed  Google Scholar 

  85. Wood SF. Women’s health and the FDA. N Engl J Med. 2005;353:1650–1.

    CAS  PubMed  Google Scholar 

  86. Østensen ME, Skomsvoll JF. Anti-inflammatory pharmacotherapy during pregnancy. Expert Opin Pharmacother. 2004;5:571–80.

    PubMed  Google Scholar 

  87. Østensen M. Nonsteroidal anti-inflammatory drugs during pregnancy. Scand J Rheumatol. 1998;27:128–32.

    Google Scholar 

  88. Akil M, Amos R, Stewart P. Infertility may sometimes be associated with NSAID consumption. Rheumatology. 1996;35:76–8.

    CAS  Google Scholar 

  89. Smith G, Roberts R, Hall C, Nuki G. Reversible ovulatory failure associated with the development of luteinized unruptured follicles in women with inflammatory arthritis taking non-steroidal anti-inflammatory drugs. Rheumatology. 1996;35:458–62.

    CAS  Google Scholar 

  90. Van der Weiden R, Wouters J. Infertility may sometimes be associated with non-steroidal anti-inflammatory drug consumption. Br J Rheumatol. 1997;36:605.

    PubMed  Google Scholar 

  91. Nielsen GL, Sørensen HT, Larsen H, Pedersen L. Risk of adverse birth outcome and miscarriage in pregnant users of non-steroidal anti-inlammatory drugs: population based observational study and case-control study. BMJ Br Med J. 2001;322(7281):266–70.

    CAS  Google Scholar 

  92. Li D-K, Liu L, Odouli R. Exposure to non-steroidal anti-inflammatory drugs during pregnancy and risk of miscarriage: population based cohort study. BMJ. 2003;327:368.

    CAS  PubMed  PubMed Central  Google Scholar 

  93. Nakhai-Pour HR, Broy P, Sheehy O, Bérard A. Use of nonaspirin nonsteroidal anti-inflammatory drugs during pregnancy and the risk of spontaneous abortion. CMAJ. 2011;183:1713–20.

    PubMed  PubMed Central  Google Scholar 

  94. Edelman AB, Jensen JT, Doom C, Hennebold JD. Impact of the prostaglandin synthase-2 inhibitor celecoxib on ovulation and luteal events in women. Contraception. 2013;87:352–7.

    CAS  PubMed  Google Scholar 

  95. Bata M, Al-Ramahi M, Salhab A, Gharaibeh M, Schwartz J. Delay of ovulation by meloxicam in healthy cycling volunteers: a placebo-controlled, double-blind, crossover study. J Clin Pharmacol. 2006;46:925–32.

    CAS  PubMed  Google Scholar 

  96. Brouwer J, Hazes J, Laven J, Dolhain R. FRI0145 High disease activity and preconceptional use of prednisone and non-steroidal anti-inflammatory drugs impair fertility in women with rheumatoid arthritis. Ann Rheum Dis. 2013;72:A419–A419419.

    Google Scholar 

  97. Brubaker W, Li S, Baker L, Eisenberg M. Increased risk of autoimmune disorders in infertile men: analysis of US claims data. Andrology. 2018;6:94–8.

    CAS  PubMed  Google Scholar 

Download references

Funding

Not applicable.

Author information

Authors and Affiliations

Authors

Contributions

AF Participated in manuscript preparation and read the manuscript critically. SN Participated in manuscript preparation and read the manuscript critically. MRHS Participated in manuscript preparation and read the manuscript critically. FHH Participated in manuscript preparation and read the manuscript critically. SJ Participated in manuscript preparation and read the manuscript critically. MA Participated in manuscript preparation and read the manuscript critically. MJM Developed the main idea, participated in manuscript preparation and read the manuscript critically. SA Developed the main idea, participated in manuscript preparation, and read the manuscript critically.

Corresponding authors

Correspondence to Mohammad Javad Mousavi or Saeed Aslani.

Ethics declarations

Conflict of interest

Abolfazl Fattah, Soheila Nouraei, Mohammad Reza Hooshangi Shayesteh, Forough Hatefi Hesari, Sirous Jamalzehi, Mojtaba Abbasi, Mohammad Javad Mousavi, and Saeed Aslani declare that they have no conflict of interest.

Additional information

Responsible Editor: John Di Battista.

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

Fattah, A., Asadi, A., Shayesteh, M.R.H. et al. Fertility and infertility implications in rheumatoid arthritis; state of the art. Inflamm. Res. 69, 721–729 (2020). https://doi.org/10.1007/s00011-020-01362-w

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00011-020-01362-w

Keywords

Navigation