Pregnancy in systemic lupus erythematosus: A literature review
DOI:
https://doi.org/10.37800/RM.1.2023.116-125Keywords:
systemic lupus erythematosus, immune response during pregnancy, pregnancy outcomes, risk, benefit, in vitro fertilization, therapyAbstract
Relevance: Systemic lupus erythematosus (SLE) is a multifaceted chronic relapsing autoimmune disease of unknown etiology. SLE has always been a serious diagnosis in women, being a multi-system pathology classically occurring in childbearing age, causing serious systemic comorbidities with potential impact on functional performance, psychosocial status, and survival.
The study aimed to establish safe recommendations for counseling women of reproductive age with SLE who have reproductive plans.
Materials and methods: The scientific literature search was performed in EMBASE, MEDLINE, and Google scholar databases from January 2013 to December 2022. We used combinations of the following keywords: “systemic lupus erythematosus,” “immune response in pregnancy,” “pregnancy outcomes,” “risk, benefit, in vitro fertilization,” and “therapy.” Titles and abstracts were analyzed for relevance to the research topic. This literature review included five meta-analyses, four study cohorts, and seven systematic reviews comparing maternal and fetal pregnancy outcomes in women with and without SLE. This article addresses issues related to the decision to conceive in a woman with SLE, focusing on the impact of diagnosis and disease activity status on the mother and fetus to make a safe decision to conceive with SLE.
Results: The pleomorphic unregulated immune nature of lupus in the presence of uncontrolled disease carries a higher risk of complicated pregnancy. Therefore, SLE pregnancy must be well planned and is usually encouraged if the disease is inactive (at least six months before conception) to provide immune rest for a safer outcome. Conclusion: Pregnancy and gestation with SLE in women of reproductive age are safe with an appropriate preconception counseling strategy, close monitoring of SLE exacerbations, and multidisciplinary management according to best practice.
References
Dalal D.S., Patel K.A., Patel M.A. Systemic lupus erythematosus and pregnancy: a brief review // J. Obstetr. Gynecol. India. – 2019. – Vol. 69(2). – P. 104-109. https://doi.org/10.1007/s13224-019-01212-8
Nahal S.K., Selmi C., Gershwin M.E. Safety issues and recommendations for successful pregnancy outcome in systemic lupus erythematosus // J. Autoimmun. – 2018. – Vol. 93. – P. 16-23. https://doi.org/10.1016/j.jaut.2018.07.016
Orefice R. Immunology and the immunological response in pregnancy // Best Pract. Res. Clin. Obstetr. Gynaecol. – 2021. – Vol. 76. – P. 3-12. https://doi.org/10.1016/j.bpobgyn.2020.07.013
Abu-Raya B., Michalski C., Sadarangani M., Lavoie P.M. Maternal immunological adaptation during normal pregnancy // Front. Immunol. – 2020. – Vol. 11. – Art. no. 575197. https://doi.org/10.3389/fimmu.2020.575197
Zhang S., Han X., Liu W., Wen Q., Wang J. Pregnancy in patients with systemic lupus erythematosus: a systematic review // Arch. Gynecol. Obstet. – 2022. https://doi.org/10.1007/s00404-022-06718-7
Gluhovschi C., Gluhovschi G., Petrica L., Velciov S., Gluhovschi A. Pregnancy associated with systemic lupus erythematosus: immune tolerance in pregnancy and its deficiency in systemic lupus erythematosus an immunological dilemma // J. Immunol. Res. – 2015. – Art. no. 241547. https://doi.org/10.1155/2015/241547
Braga A., Neves E., Guimarães J., Braga J., Vasconcelos C. The dynamics of Th17 / Treg ratio in SLE patients during pregnancy // J. Reprod. Immunol. – 2022. – Vol. 151. – Art. No. 103622. https://doi.org/10.1016/j.jri.2022.103622
Fu B., Tian Z., Wei H. TH17 cells in human recurrent pregnancy loss and pre-eclampsia // Cell Mol. Immunol. – 2014. – Vol. 11(6). – P. 564-570. https://doi.org/10.1038/cmi.2014.54
Lasarte S., Elsner D., Guía-González M., Ramos-Medina R., Sánchez-Ramón S., Esponda P. Female sex hormones regulate the Th17 immune response to sperm and Candida albicans // Hum. Reprod. – 2013. – Vol. 28(12). – P. 3283-3291. https://doi.org/10.1093/humrep/det348
Tsuda S., Nakashima A., Morita K., Shima T., Yoneda S., Kishi H. The role of decidual regulatory T cells in the induction and maintenance of fetal antigen-specific tolerance: imbalance between regulatory and cytotoxic T cells in pregnancy complications // Hum. Immunol. – 2021. – Vol. 82(5). – P. 346-352. https://doi.org/10.1016/j.humimm.2021.01.019
Pastore D.E.A., Costa M.L., Parpinelli M.A., Surita F.G. A critical review on obstetric follow-up of women affected by systemic lupus erythematosus // Rev Bras Ginecol Obstet. – 2018. – Vol. 40(4). – P. 209-224. https://doi.org/10.1055/s-0038-1625951
Maynard S., Guerrier G., Duffy M. Pregnancy in women with systemic lupus and lupus nephritis // Adv. Chronic Kidney Dis. – 2019. – Vol. 26(5). – P. 330-337. https://doi.org/10.1053/j.ackd.2019.08.013
Buyon J.P., Kim M.Y., Guerra M.M., Laskin C.A., Petri M., Lockshin M.D., Sammaritano L., Branch D.W., Porter T.F., Sawitzke A., Merrill J.T., Stephenson M.D., Cohn E., Garabet L., Salmon J.E. Predictors of Pregnancy Outcomes in Patients With Lupus: A Cohort Study // Ann. Inter. Med. – 2015. - Vol. 163(3). – P. 153-163. https://doi.org/10.7326/M14-2235
Braga A., Barros T., Faria R., Marinho A., Carvalheira G., Rocha G., Farinha F., Neves E., Vasconcelos C., Braga J. Systemic lupus erythematosus and pregnancy: A retrospective single-center study of 215 pregnancies from Portugal // Lupus. – 2021. – Vol. 30(13). – P. 2165-2175. https://doi.org/10.1177/09612033211050340
Andreoli L., Bertsias G.K., Agmon-Levin N., Brown S., Cervera R., Costedoat-Chalumeau N., Doria A., Fischer-Betz R., Forger F., Moraes-Fontes M.F., Khamashta M., King J., Lojacono A., Marchiori F., Meroni P.L., Mosca M., Motta M., Ostensen M., Pamfil C., Raio L., Tincani, A. 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. – Vol. 76(3). – P. 476-485. https://doi.org/10.1136/annrheumdis-2016-209770
Tincani A, Bompane D, Danieli E, Doria A. Pregnancy, lupus and antiphospholipid syndrome (Hughes syndrome). Lupus. – 2006. – 15(3). – P.156-160. https://doi.org/10.1191/0961203306lu2279rr.
Phuti A., Hodkinson B., Tikly M., Schneider M. ‘The feeling of not being entitled to something’: fertility, pregnancy, and sexuality among women with systemic lupus erythematosus in South Africa // Scand. J. Rheumatol. – 2020. – Vol. 49(3). – P. 214-220. https://doi.org/10.1080/03009742.2019.1657492
Lian XJ., Fan L., Xia X. Fetal and maternal outcome in patients with active lupus nephritis: comparison between new-onset and pre-existing lupus nephritis // BMC Nephrol. – 2021. – Vol. 22. – Art. no. 419. https://doi.org/10.1186/s12882-021-02633-2
Liu Y., Zhang Y., Wei Y., Yang H. Effect of hydroxychloroquine on preeclampsia in lupus pregnancies: a propensity score-matched analysis and meta-analysis // Arch. Gynecol. Obstet. – 2021. – Vol. 303(2). – P. 435-441. https://doi.org/10.1007/s00404-020-05762-5
Arkema E.V., Palmsten K., Sjöwall C., Svenungsson E., Salmon J.E., Simard J.F. What to Expect When Expecting With Systemic Lupus Erythematosus (SLE): A Population-Based Study of Maternal and Fetal Outcomes in SLE and Pre-SLE // Arthritis Care Res (Hoboken). – 2016. – Vol. 68(7). – P. 988-994. https://doi.org/10.1002/acr.22791
Bundhun P.K., Soogund M.Z.S., Huang F. Arterial/venous thrombosis, fetal loss and stillbirth in pregnant women with systemic lupus erythematosus versus primary and secondary antiphospholipid syndrome: a systematic review and meta-analysis // BMC Pregn. Childbirth. – 2018. – Vol. 18(1). – Art. no. 212. https://doi.org/10.1186/s12884-018-1850-x
Mehta B., Luo Y., Xu J. Trends in Maternal and Fetal Outcomes Among Pregnant Women With Systemic Lupus Erythematosus in the United States: A Cross-sectional Analysis // Ann Intern Med. – 2019. – Vol. 171(3). – P. 164-171. https://doi.org/10.7326/M19-0120
Ananth C.V., Keyes K.M., Wapner R.J. Pre-eclampsia rates in the United States, 1980-2010: age-period-cohort analysis // BMJ. – 2013. – Vol. 347. – Art. no. f6564. https://doi.org/10.1136/bmj.f6564
Cervera R., Serrano R., Pons-Estel G.J. Morbidity and mortality in the antiphospholipid syndrome during a 10-year period: a multicentre prospective study of 1000 patients // Ann. Rheum. Dis. – 2015. – Vol. 74(6). – P. 1011-1018. https://doi.org/10.1136/annrheumdis-2013-204838
Lateef A., Petri M. Systemic lupus erythematosus and pregnancy // Rheum. Dis. Clin. – 2017. – Vol. 43(2) – P. 215-226. https://doi.org/10.1016/j.rdc.2016.12.009
Jakobsen I., Helmig R., Stengaard-Pedersen K. Maternal and fetal outcomes in pregnant systemic lupus erythematosus patients: an incident cohort from a stable referral population followed during 1990–2010 // Scand. J. Rheumatol. – 2015. – Vol. 44(5). – P. 377-384. https://doi.org/10.3109/03009742.2015.1013982
Bălănescu A., Donisan T., Bălănescu D. An ever-challenging relationship: lupus and pregnancy // Reumatologia. – 2017. – Vol. 55(1). – P. 29-37. https://doi.org/10.5114/reum.2017.66685
Kramer M.S., Lydon J., Goulet L., Kahn S., Dahhou M., Platt R.W. Maternal stress/distress, hormonal pathways and spontaneous preterm birth // Paediatr. Perinat. Epidemiol. – 2013. – Vol. 27(3) – P. 237-246. https://doi.org/10.1111/ppe.12042
Petri M. Pregnancy and systemic lupus erythematosus // Best Pract. Res. Clin. Obstet. Gynaecol. – 2020. – Vol. 64. – P. 24-30. https://doi.org/10.1016/j.bpobgyn.2019.09.002
Voltolini C., Torricelli M., Conti N., Vellucci F.L., Severi F.M., Petraglia F. Understanding spontaneous preterm birth: from underlying mechanisms to predictive and preventive interventions // Reprod. Sci. – 2013. – Vol. 20(11). – P. 1274-1292. https://doi.org/10.1177/1933719113477496
Namazy J.A., Murphy V.E., Powell H., Gibson P.G., Chambers C., Schatz M. Effects of asthma severity, exacerbations, and oral corticosteroids on perinatal outcomes // Eur. Respir. J. – 2013. – Vol. 41(5). – P. 1082-1090. https://doi.org/10.1183/09031936.00195111
Wei S., Lai K., Yang Z., Zeng K. Systemic lupus erythematosus and risk of preterm birth: a systematic review and meta-analysis of observational studies // Lupus. – 2017. – Vol. 26(6). – P. 563-571. https://doi.org/10.1177/0961203316686704
Wei S., Lai K., Yang Z., Zeng K. Systemic lupus erythematosus and 88. risk of preterm birth: a systematic review and meta-analysis of observational studies // Lupus. – 2017. – Vol. 26(6). – P. 563-571. https://doi.org/10.1111/aji.12329
Toijonen A.E., Heinonen S.T., Gissler M.V., Macharey G. A comparison of risk factors for breech presentation in preterm and term labor: a nationwide, population-based case-control study // Arch. Gynecol. Obstet. – 2020. – Vol. 301. – P. 393-403. https://doi.org/10.1007/s00404-019-05385-5
Nguyen C.T., Mestman J.H. Postpartum thyroiditis // Clin. Obstet. Gynecol. – 2019. – Vol. 62(2). – P. 359-364. https://doi.org/10.1097/GRF.0000000000000430
Maleki N., Tavosi Z. Evaluation of thyroid dysfunction and autoimmunity in gestational diabetes mellitus and its relationship with postpartum thyroiditis // Diabet. Med. – 2015. – Vol. 32(2). – P. 206-212. https://doi.org/10.1111/dme.12580
Arbib N., Hadar E., Sneh-Arbib O., Chen R., Wiznitzer A., Gabbay-Benziv R. First trimester thyroid stimulating hormone as an independent risk factor for adverse pregnancy outcome // J. Matern. Fetal. Neonatal. Med. – 2017. – Vol. 30(18). – P. 2174-2178. https://doi.org/10.1080/14767058.2016.1242123
Ateka-Barrutia O., Nelson-Piercy C. Management of rheumatologic diseases in pregnancy // Int. J. Clin. Rheumatol. – 2020. – Vol. 7(5). – P. 541-558. https://doi.org/10.3109/03009740903449313
Gómez-Guzmán M., Jiménez R., Romero M., Sánchez M., Zarzuelo M.J., Gómez-Morales M. Chronic hydroxychloroquine improves endothelial dysfunction and protects kidney in a mouse model of systemic lupus erythematosus // Hypertension. – 2014. – Vol. 64(2). – P. 330-337. https://doi.org/10.1161/HYPERTENSIONAHA.114.03587
Clowse M.E.B., Eudy A.M., Balevic S., Sanders-Schmidler G., Kosinski A., Fischer-Betz R., Gladman D.D., Molad Y., Nalli C., Mokbel A., Tincani A., Urowitz M., Bay C., van Noord M., Petri M. Hydroxychloroquine in the pregnancies of women with lupus: a meta-analysis of individual participant data // Lupus Sci. Med. – 2022. – Vol. 9(1). – Art. no. e000651. https://doi.org/10.1136/lupus-2021-000651
Saavedra M., Sánchez A., Morales S., Ángeles U., Jara L.J. Azathioprine during pregnancy in systemic lupus erythematosus patients is not associated with poor fetal outcome // Clin. Rheumatol. – 2014. – Vol. 34(7). – P. 1211-1216. https://doi.org/10.1007/s10067-015-2987-x
Webster P., Wardle A., Bramham K., Webster L., Nelson-Piercy C., Lightstone L. Tacrolimus is an effective treatment for lupus nephritis in pregnancy // Lupus. – 2014. – Vol. 23(11). – P. 1192-1196. https://doi.org/10.1177/0961203314540353
Ostensen M., Cetin I. Autoimmune connective tissue diseases // Best Pract. Res. Clin. Obstet. Gynaecol. – 2016. – Vol. 29(5). – P. 658-670. https://doi.org/10.1016/j.bpobgyn.2015.03.003
Leroux M., Desveaux C., Parcevaux M., Julliac B., Gouyon J-B., Dallay D. Impact of hydroxychloroquine on preterm delivery and intrauterine growth restriction in pregnant women with systemic lupus erythematosus: a descriptive cohort study // Lupus. – 2015. – Vol. 24(13). – P. 1384-1391. https://doi.org/10.1177/0961203315591027
Seo M., Chae J., Kim Y., Cha H., Choi S., Oh S. Hydroxychloroquine treatment during pregnancy in lupus patients is associated with lower risk of preeclampsia // Lupus. – 2019. – Vol. 28(6). – P. 722-730. https://doi.org/10.1177/0961203319843343
Do S.C., Rizk N.M., Druzin M.L., Simard J.F. Does hydroxychloroquine protect against preeclampsia and preterm delivery in systemic lupus erythematosus pregnancies? // Am. J. Perinatal. – 2020. – Vol. 37(09). – P. 873-880. https://doi.org/10.1055/s-0039-3402752
Ghalandari N., Crijns H.J., Dolhain R.J., Hazes J.M., van Puijenbroek E.P. Dilemma of belimumab therapy (dis) continuation during pregnancy: Results of a retrospective study in eudravigilance // Lupus. – 2022. – Vol. 0(0). https://doi.org/10.1177/09612033221143
Lazzaroni M.G., Dall’Ara F., Fredi M., Nalli C., Reggia R., Lojacono A. A comprehensive review of the clinical approach to pregnancy and systemic lupus erythematosus // J. Autoimmun. – 2016. – Vol. 74. – P. 106-117. https://doi.org/10.1016/j.jaut.2016.06.016
Downloads
Published
How to Cite
Issue
Section
License
The articles published in this Journal are licensed under the CC BY-NC-ND 4.0 (Creative Commons Attribution – Non-Commercial – No Derivatives 4.0 International) license, which provides for their non-commercial use only. Under this license, users have the right to copy and distribute the material in copyright but are not permitted to modify or use it for commercial purposes. Full details on the licensing are available at https://creativecommons.org/licenses/by-nc-nd/4.0/.
