Antiphospholipid antibodies and the risk of adverse pregnancy outcomes in patients with systemic lupus erythematosus: a systematic review and meta-analysis

References

• Kiriakidou M, Ching CL. Systemic lupus erythematosus. Ann Intern Med. 2020;172(11):ITC81–ITC96. doi: 10.7326/AITC202006020
   PubMed Web of Science ®Google Scholar
• Buyon JP, Kim MY, Guerra MM, et al. Predictors of pregnancy outcomes in patients with lupus: a cohort study. Ann Intern Med. 2015;163(3):153–163. doi: 10.7326/m14-2235
   PubMed Web of Science ®Google Scholar
• Sammaritano LR, Bermas BL, Chakravarty EE, et al. 2020 American college of rheumatology guideline for the management of reproductive health in rheumatic and musculoskeletal diseases. Arthritis & Rheumat. 2020;72(4):529–556. doi: 10.1002/art.41191
   PubMed Web of Science ®Google Scholar
• Andreoli L, Bertsias GK, Agmon-Levin 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):476–485. doi: 10.1136/annrheumdis-2016-209770
   PubMed Web of Science ®Google Scholar
• Pericleous C, D’Souza A, McDonnell T, et al. Antiphospholipid antibody levels in early systemic lupus erythematosus: are they associated with subsequent mortality and vascular events? Rheumatology. 2020;59(1):146–152. doi: 10.1093/rheumatology/kez239
   PubMed Web of Science ®Google Scholar
• Zhan Z, Yang Y, Zhan Y, et al. Fetal outcomes and associated factors of adverse outcomes of pregnancy in southern Chinese women with systemic lupus erythematosus. PloS One. 2017;12(4):e0176457. doi: 10.1371/journal.pone.0176457
   PubMed Web of Science ®Google Scholar
• Saleh M, Sjowall C, Strevens H, et al. Adverse pregnancy outcomes after multi-professional follow-up of women with systemic lupus erythematosus: an observational study from a single centre in Sweden. J Clin Med. 2020;9(8):2598. doi: 10.3390/jcm9082598
   PubMed Web of Science ®Google Scholar
• Chen D, Lao M, Zhang J, et al. Fetal and maternal outcomes of planned pregnancy in patients with systemic lupus erythematosus: a retrospective multicenter study. J Immunol Res. 2018;2018:1–7. doi: 10.1155/2018/2413637
   Web of Science ®Google Scholar
• Larosa M, Le Guern V, Guettrot-Imbert G, et al. Evaluation of lupus anticoagulant, damage, and remission as predictors of pregnancy complications in lupus women: the French GR2 study. Rheumatology (Oxford). 2022;61(9):3657–3666. doi: 10.1093/rheumatology/keab943
   PubMed Web of Science ®Google Scholar
• Yelnik CM, Laskin CA, Porter TF, et al. Lupus anticoagulant is the main predictor of adverse pregnancy outcomes in aPL-positive patients: validation of PROMISSE study results. Lupus Sci Med. 2016;3(1):e000131–e000131. doi: 10.1136/lupus-2015-000131
   PubMed Web of Science ®Google Scholar
• Mankee A, Petri M, Magder LS. Lupus anticoagulant, disease activity and low complement in the first trimester are predictive of pregnancy loss. Lupus Sci Med. 2015;2(1):e000095–e000095. doi: 10.1136/lupus-2015-000095
   PubMedGoogle Scholar
• Angel Saavedra M, Miranda-Hernandez D, Sanchez A, et al. Pregnancy outcomes in women with childhood-onset and adult-onset systemic lupus erythematosus: a comparative study. Rheumatol Int. 2016;36(10):1431–1437. doi: 10.1007/s00296-016-3525-0
   PubMed Web of Science ®Google Scholar
• Tian X, Li M, Ye Z, et al. Related factors of fetal loss in Chinese women with systemic lupus erythematosus: data from Chinese SLE treatment and research group registry IV. Int J Rheum Dis. 2015;18(6):654–660. doi: 10.1111/1756-185X.12542
   PubMed Web of Science ®Google Scholar
• Deguchi M, Maesawa Y, Kubota S, et al. Factors associated with adverse pregnancy outcomes in women with systematic lupus erythematosus. J Reprod Immunol. 2018;125:39–44. doi: 10.1016/j.jri.2017.11.005
   PubMed Web of Science ®Google Scholar
• Li Y, Zhang L, Xu K, et al. A systematic review and meta-analysis of pregnancy outcomes in systemic lupus erythematosus patients. Int J Rheum Dis. 2016;19:266. doi: 10.1111/1756-185X.12962
   Google Scholar
• Moher D, Shamseer L, Clarke M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4(1):1. doi: 10.1186/2046-4053-4-1
   PubMed Web of Science ®Google Scholar
• Aringer M, Costenbader K, Daikh D, et al. 2019 European league against rheumatism/American college of rheumatology classification criteria for systemic lupus erythematosus. Ann Rheum Dis. 2019;78(9):1151–1159. doi: 10.1136/annrheumdis-2018-214819
   PubMed Web of Science ®Google Scholar
• Black SM, Walocko F, Li X, et al. Development of systemic lupus in patients with cutaneous lupus using the 2012 systemic lupus international collaborating clinics (SLICC) classification criteria for systemic lupus erythematosus. J Am Acad Dermatol. 2021;85(1):200–202. doi: 10.1016/j.jaad.2020.12.061
   PubMed Web of Science ®Google Scholar
• Raghupathy R, Szekeres-Bartho J. Progesterone: a unique hormone with immunomodulatory roles in pregnancy. Int J Mol Sci. 2022;23(3):1333. doi: 10.3390/ijms23031333
   PubMed Web of Science ®Google Scholar
• Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in meta-analyses. BMJ. 2003;327(7414):557–560. doi: 10.1136/bmj.327.7414.557
   PubMed Web of Science ®Google Scholar
• Hayashino Y, Noguchi Y, Fukui T. Systematic evaluation and comparison of statistical tests for publication bias. J Epidemiol. 2005;15(6):235–243. doi: 10.2188/jea.15.235
   PubMed Web of Science ®Google Scholar
• Jiang D, Wang L, Bai C, et al. Association between abdominal obesity and asthma: a meta-analysis. Allergy Asthma Clin Immunol. 2019;15(1):16. doi: 10.1186/s13223-019-0333-6
   PubMed Web of Science ®Google Scholar
• De-Xuan K, Zhi-Kun Z, Hui-Dong L. Correlation between systemic lupus erythematosus and adverse pregnancy outcomes in pregnant women. Matern Child Health Care China. 2022;37:1865–1868. doi: 10.19829/j.zgfybj.issn.1001-4411.2022.10.035
   Google Scholar
• Xiaoyun L, Jinfeng S. Premature birth outcomes in pregnant women with systemic lupus erythematosus. Zhejiang Clin med. 2021;23:1473–1475.
   Google Scholar
• Xiujuan T, Juan H, Peng H, et al. Outcome analysis of patients with systemic lupus erythematosus complicated with pregnancy. J Clin Intern Med. 2021;38:399–402. doi: 10.3969/j.issn.1001-9057.2021.06.012
   Google Scholar
• Al Arfaj AS, Khalil N. Pregnancy outcome in 396 pregnancies in patients with SLE in Saudi Arabia. Lupus. 2010;19(14):1665–1673. doi: 10.1177/0961203310378669
   PubMed Web of Science ®Google Scholar
• Chen D, Lao M, Zhang J, et al. Fetal and maternal outcomes of planned pregnancy in patients with systemic lupus erythematosus: a retrospective multicenter study. J Immunol Res. 2018;2018:2413637. doi: 10.1155/2018/2413637
   PubMed Web of Science ®Google Scholar
• Hamed HO, Ahmed SR, Alzolibani A, et al. Does cutaneous lupus erythematosus have more favorable pregnancy outcomes than systemic disease? A two-center study. Acta Obstet Gynecol Scand. 2013;92(8):934–942. doi: 10.1111/aogs.12158
   PubMed Web of Science ®Google Scholar
• Jiang M, Chang Y, Wang Y, et al. High-risk factors for adverse pregnancy outcomes in systemic lupus erythaematosus: a retrospective study of a Chinese population. BMJ Open. 2021;11(11):e049807. doi: 10.1136/bmjopen-2021-049807
   PubMed Web of Science ®Google Scholar
• Ko HS, Ahn HY, Jang DG, et al. Pregnancy outcomes and appropriate timing of pregnancy in 183 pregnancies in Korean patients with SLE. Int J Med Sci. 2011;8(7):577–583. doi: 10.7150/ijms.8.577
   PubMed Web of Science ®Google Scholar
• Palma Dos Reis CR, Cardoso G, Carvalho C, et al. Prediction of adverse pregnancy outcomes in women with systemic lupus erythematosus. Clin Rev Allergy Immunol. 2020;59(3):287–294. doi: 10.1007/s12016-019-08762-9
   PubMed Web of Science ®Google Scholar
• Zhang LL, Shu H, Zhang S, et al. Pregnancy outcomes and risk factors in pregnant women with systemic lupus erythematosus. Clin Exp Obstet Gynecol. 2020;47:189–193. doi: 10.31083/j.ceog.2020.02.5043
   Web of Science ®Google Scholar
• Al-Riyami N, Salman B, Al-Rashdi A, et al. Pregnancy outcomes in systemic lupus erythematosus women: a single tertiary centre experience. Sultan Qaboos Univ Med J. 2021;21(2):e244–e252. doi: 10.18295/squmj.2021.21.02.013
   PubMedGoogle Scholar
• Ramsey-Goldman R, Kutzer JE, Kuller LH, et al. Pregnancy outcome and anti-cardiolipin antibody in women with systemic lupus erythematosus. American J Epidemiology. 1993;138(12):1057–1069. doi: 10.1093/oxfordjournals.aje.a116824
   PubMed Web of Science ®Google Scholar
• Feld J, Kibari A, Rozenbaum M, et al. The fetal outcomes of pregnancies of systemic lupus erythematosus patients in northern Israel. J Matern Fetal Neonatal Med. 2015;28(5):564–567. doi: 10.3109/14767058.2014.926327
   PubMed Web of Science ®Google Scholar
• Hwang JK, Park HK, Sung YK, et al. Maternal outcomes and follow-up of preterm and term neonates born to mothers with systemic lupus erythematosus. J Matern Fetal Neonatal Med. 2018;31(1):7–13. doi: 10.1080/14767058.2016.1205027
   PubMed Web of Science ®Google Scholar
• Liu E, Zhou Y. Prognosis in pregnant females with systemic lupus erythematosus. Arch Rheumatol. 2017;32(4):298–302. doi: 10.5606/ArchRheumatol.2017.6304
   PubMed Web of Science ®Google Scholar
• Nojima J, Motoki Y, Aoki N, et al. A novel ELISA system for simultaneous detection of six subclasses of anti-phospholipid antibodies for prediction of thrombotic complications among SLE patients. Thromb Res. 2014;133(6):1135–1140. doi: 10.1016/j.thromres.2014.03.032
   PubMed Web of Science ®Google Scholar
• Ong SG, Ding HJ. Predictors of adverse pregnancy outcome in a cohort of women with systemic lupus erythematosus in Malaysia. Med J Malaysia. 2021;76:466–473.
   PubMedGoogle Scholar
• Poh YJ, Yii IYL, Goh LH, et al. Maternal and fetal outcomes in systemic lupus erythematosus pregnancies. Ann Acad Med Singap. 2020;49(12):963–970. doi: 10.47102/annals-acadmedsg.2020373
   PubMed Web of Science ®Google Scholar
• Kalok A, Abdul Cader R, Indirayani I, et al. Pregnancy outcomes in systemic lupus erythematosus (SLE) women. Horm Mol Biol Clin Investig. 2019;40(3). doi: 10.1515/hmbci-2019-0007
   PubMed Web of Science ®Google Scholar
• Petri M, Howard D, Repke J, et al. The Hopkins lupus pregnancy center: 1987–1991 update. Am J Reprod Immunol. 1992;28(3–4):188–191. doi: 10.1111/j.1600-0897.1992.tb00788.x
   PubMed Web of Science ®Google Scholar
• Weinian L, Xiaoyan C, Xiaojun L, et al. Risk factors of disease progression and adverse pregnancy outcome in patients with systemic lupus erythematosus during pregnancy. Chin J Gen Pract. 2017;16:214–218. doi: 10.3760/cma.j.issn.1671-7368.2017.03.010
   Google Scholar
• Yu-Zhu Y, Shui-Sheng Z, Jian-Lin H, et al. The impact of lupus flares on maternal and fetal outcomes in pregnant patients with systemic lupus erythematosus. Chin J Rheumatol. 2012;16:53–56. doi: 10.3760/cma.j.issn.1007-7480.2012.01.013
   Google Scholar
• Miyakis S, Lockshin MD, Atsumi T, et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost. 2006;4(2):295–306. doi: 10.1111/j.1538-7836.2006.01753.x
   PubMed Web of Science ®Google Scholar
• Gordon C, Amissah-Arthur MB, Gayed M, et al. The British society for rheumatology guideline for the management of systemic lupus erythematosus in adults. Rheumatology (Oxford). 2018;57(1):e1–e45. doi: 10.1093/rheumatology/kex286
   PubMed Web of Science ®Google Scholar
• Nahal SK, Selmi C, Gershwin ME. Safety issues and recommendations for successful pregnancy outcome in systemic lupus erythematosus. J Autoimmun. 2018;93:16–23. doi: 10.1016/j.jaut.2018.07.016
   PubMed Web of Science ®Google Scholar
• Fischer-Betz R, Specker C. Pregnancy in systemic lupus erythematosus and antiphospholipid syndrome. Best Pract Res Clin Rheumatol. 2017;31(3):397–414. doi: 10.1016/j.berh.2017.09.011
   PubMed Web of Science ®Google Scholar
• Moroni G, Ponticelli C. Pregnancy in women with systemic lupus erythematosus (SLE). Eur J Intern Med. 2016;32:7–12. doi: 10.1016/j.ejim.2016.04.005
   PubMed Web of Science ®Google Scholar
• Petri M. Pregnancy and systemic lupus erythematosus. Best Pract Res Cl Ob. 2020;64:24–30. doi: 10.1016/j.bpobgyn.2019.09.002
   Web of Science ®Google Scholar
• Opatrny L, David M, Kahn SR, et al. Association between antiphospholipid antibodies and recurrent fetal loss in women without autoimmune disease: a metaanalysis. J Rheumatol. 2006;33:2214–2221.
   PubMed Web of Science ®Google Scholar
• Xu J, Chen D, Duan X, et al. The association between antiphospholipid antibodies and late fetal loss: a systematic review and meta-analysis. Acta Obstet Gynecol Scand. 2019;98(12):1523–1533. doi: 10.1111/aogs.13665
   PubMed Web of Science ®Google Scholar
• Marchetti T, Ribi C, Perneger T, et al. Prevalence, persistence and clinical correlations of classic and novel antiphospholipid antibodies in systemic lupus erythematosus. Rheumatology (Oxford). 2018;57(8):1350–1357. doi: 10.1093/rheumatology/key095
   PubMed Web of Science ®Google Scholar
• Smyth A, Oliveira GHM, Lahr BD, et al. A systematic review and meta-analysis of pregnancy outcomes in patients with systemic lupus erythematosus and lupus nephritis. Clin J Am Soc Nephrol. 2010;5(11):2060–2068. doi: 10.2215/CJN.00240110
   PubMed Web of Science ®Google Scholar
• Schreiber K, Sciascia S, de Groot PG, et al. Antiphospholipid syndrome. Nat Rev Dis Primers. 2018;4(1). doi: 10.1038/nrdp.2017.103
   Google Scholar
• Meroni PL, Borghi MO, Grossi C, et al. Obstetric and vascular antiphospholipid syndrome: same antibodies but different diseases? Nat Rev Rheumatol. 2018;14(7):433–440. doi: 10.1038/s41584-018-0032-6
   PubMed Web of Science ®Google Scholar
• Matrai CE, Rand JH, Baergen RN. Absence of distinct immunohistochemical distribution of annexin A5, C3b, C4d, and C5b-9 in placentas from patients with antiphospholipid antibodies, preeclampsia, and systemic lupus erythematosus. Pediatr Dev Pathol. 2019;22(5):431–439. doi: 10.1177/1093526619836025
   PubMed Web of Science ®Google Scholar
• Castellanos Gutierrez AS, Figueras F, Morales-Prieto DM, et al. Placental damage in pregnancies with systemic lupus erythematosus: a narrative review. Front Immunol. 2022;13:941586. doi: 10.3389/fimmu.2022.941586
   PubMed Web of Science ®Google Scholar
• Kim MY, Guerra MM, Kaplowitz E, et al. Complement activation predicts adverse pregnancy outcome in patients with systemic lupus erythematosus and/or antiphospholipid antibodies. Ann Rheum Dis. 2018;77(4):549–555. doi: 10.1136/annrheumdis-2017-212224
   PubMed Web of Science ®Google Scholar
• Deshmukh H, Way SS. Immunological basis for recurrent fetal loss and pregnancy complications. Annu Rev Pathol. 2019;14(1):185–210. doi: 10.1146/annurev-pathmechdis-012418-012743
   PubMedGoogle Scholar
• Li J, Xu D, Li HL. Evaluation of failed immunotherapy among patients with negative APLA recurrent spontaneous abortion by serum anticardiolipin antibodies and mononuclear cell of tim-1. Eur Rev Med Pharmacol Sci. 2017;21:908–912.
   PubMed Web of Science ®Google Scholar
• Sharabi A, Tsokos GC. T cell metabolism: new insights in systemic lupus erythematosus pathogenesis and therapy. Nat Rev Rheumatol. 2020;16(2):100–112. doi: 10.1038/s41584-019-0356-x
   PubMed Web of Science ®Google Scholar
• Chayoua W, Kelchtermans H, Gris JC, et al. The (non-)sense of detecting anti-cardiolipin and anti-β2glycoprotein I IgM antibodies in the antiphospholipid syndrome. J Thromb Haemost. 2020;18(1):169–179. doi: 10.1111/jth.14633
   PubMed Web of Science ®Google Scholar
• Chighizola CB, Lonati PA, Trespidi L, et al. The complement system in the pathophysiology of pregnancy and in systemic autoimmune rheumatic diseases during pregnancy. Front Immunol. 2020;11:2084. doi: 10.3389/fimmu.2020.02084
   PubMed Web of Science ®Google Scholar
• Green ES, Arck PC. Pathogenesis of preterm birth: bidirectional inflammation in mother and fetus. Semin Immunopathol. 2020;42(4):413–429. doi: 10.1007/s00281-020-00807-y
   PubMed Web of Science ®Google Scholar
• Abrahams VM. Mechanisms of antiphospholipid antibody-associated pregnancy complications. Thromb Res. 2009;124(5):521–525. doi: 10.1016/j.thromres.2009.07.011
   PubMed Web of Science ®Google Scholar
• Chappell LC, Cluver CA, Kingdom J, et al. Pre-eclampsia. Lancet. 2021;398(10297):341–354. doi: 10.1016/S0140-6736(20)32335-7
   PubMed Web of Science ®Google Scholar
• Kesavan K, Devaskar SU. Intrauterine growth restriction: postnatal monitoring and outcomes. Pediatr Clin North Am. 2019;66(2):403–423. doi: 10.1016/j.pcl.2018.12.009
   PubMed Web of Science ®Google Scholar
• Fazzari MJ, Guerra MM, Salmon J, et al. Adverse pregnancy outcomes in women with systemic lupus erythematosus: can we improve predictions with machine learning? Lupus Sci Med. 2022;9(1):e000769. doi: 10.1136/lupus-2022-000769
   PubMed Web of Science ®Google Scholar
• Shimada K, Koike T, Ichikawa K, et al. IgG class anti-cardiolipin antibody as a possible marker for evaluating fetal risk in patients with systemic lupus erythematosus. J Autoimmun. 1989;2(6):843–849. doi: 10.1016/0896-8411(89)90010-3
   PubMed Web of Science ®Google Scholar
• Cucurull E, Espinoza LR, Mendez E, et al. Anticardiolipin and anti-β2glycoprotein-I antibodies in patients with systemic lupus erythematosus: comparison between Colombians and spaniards. Lupus. 1999;8(2):134–141. doi: 10.1191/096120399678847533
   PubMed Web of Science ®Google Scholar
• Qamar T, Levy RA, Sammaritano L, et al. Characteristics of high-titer IgG antiphospholipid antibody in systemic lupus erythematosus patients with and without fetal death. Arthritis Rheum. 1990;33(4):501–504. doi: 10.1002/art.1780330406
   PubMedGoogle Scholar
• Sebastiani GD, Passiu G, Galeazzi M, et al. Prevalence and clinical associations of anticardiolipin antibodies in systemic lupus erythematosus: a prospective study. Clin Rheumatol. 1991;10(3):289–293. doi: 10.1007/BF02208692
   PubMed Web of Science ®Google Scholar
• Wang Z, Wang Y, Zhu R, et al. Long-term survival and death causes of systemic lupus erythematosus in China: a systemic review of observational studies. Medicine (Baltimore). 2015;94(17):e794. doi: 10.1097/MD.0000000000000794
   PubMed Web of Science ®Google Scholar
• Ferucci ED, Johnston JM, Gaddy JR, et al. Prevalence and incidence of systemic lupus erythematosus in a population-based registry of American Indian and Alaska native people, 2007–2009. Arthritis & Rheumat. 2014;66(9):2494–2502. doi: 10.1002/art.38720
   PubMed Web of Science ®Google Scholar