The present study aimed to analyse the frequency of premature rupture of membranes (PROMs) among 190 women with systemic lupus erythematosus (SLE) followed up at the Hospital Universitário Pedro Ernesto from 2011 to 2018 and to review the literature on PROM in patients with SLE.
Methods
A cohort study of SLE patients was conducted by analysing the following variables: sociodemographic characteristics, clinical manifestations of lupus, modified disease activity index for pregnancy, drugs used during pregnancy, intercurrent maternal infections and obstetric outcomes. Additionally, seven electronic databases (PubMed, Embase, Cochrane, Scielo, Scielo Brazil, Virtual Health Library Regional Portal and Google Scholar) were systematically searched. The search was updated on 3 February 2020.
Results
Infections (relative risk (RR): 3.26, 95% confidence interval (CI): 1.5–6.7, p = .001), history of serositis (RR: 2.59, 95% CI: 1.31–5.11, p = .006) and anti-RNP positivity (RR: 3.08, 95% CI: 1.39–6.78, p = .005) were associated risk factors for PROM, while anti-RNP positivity (RR: 3.37, 95% CI: 1.35–8.40; p = .009) were associated with premature PROM (PPROM). The prevalence of PROM and PPROM was 28.7% and 12.9%, respectively. In the systematic review, the prevalence of PROM and PPROM was 2.7%–35% (I2 = 87.62%) and 2.8%–20% (I2 = 79.56%), respectively.
Conclusions
PROM, both at term and preterm, occurs more frequently in women with lupus than in the general population. A history of serositis, anti-RN, infections and immunosuppression during pregnancy may increase the susceptibility to PROM. The systematic review did not find any study with the main objective of evaluating PROM/PPROM in women with lupus.
ReesFDohertyMGraingeM, et al.Burden of Comorbidity in systemic lupus erythematosus in the UK, 1999-2012. Arthritis Care Res2016; 68(6): 819–827. DOI: 10.1002/acr.22751.
2.
MichetCJMcKennaCHElvebackLR, et al.Epidemiology of systemic lupus erythematosus and other connective tissue diseases in Rochester, Minnesota, 1950 through 1979. Mayo Clinic Proc1985; 60(2): 105–113. DOI: 10.1016/s0025-6196(12)60294-8.
3.
DelignyCThomasLDubreuilF, et al.Lupus systémique en Martinique: enquête épidémiologique. La Revue de Médecine Interne2002; 23(1): 21–29. DOI: 10.1016/s0248-8663(01)00511-2.
4.
BorellaELojaconoAGattoM, et al.Predictors of maternal and fetal complications in SLE patients: a prospective study. Immunologic Res2014; 60(2–3): 170–176. DOI: 10.1007/s12026-014-8572-6.
5.
LateefAPetriM. Managing lupus patients during pregnancy. Best Pract Res Clin Rheumatol2013; 27(3): 435–447. DOI: 10.1016/j.berh.2013.07.005.
6.
ClowseMEB. Lupus activity in pregnancy. Rheum Dis Clin North America2007; 33(2): 237–252. DOI: 10.1016/j.rdc.2007.01.002.
7.
ClarkCASpitzerKALaskinCA. Decrease in pregnancy loss rates in patients with systemic lupus erythematosus over a 40-year period. The J rheumatology2005; 32(9): 1709–1712.
8.
TincaniABazzaniCZingarelliS, et al.Lupus and the antiphospholipid syndrome in pregnancy and obstetrics: clinical characteristics, diagnosis, pathogenesis, and treatment. Semin Thromb Hemost2008; 34(03): 267–273. DOI: 10.1055/s-0028-1082270.
9.
BertsiasGIoannidisJPABoletisJ, et al.EULAR recommendations for the management of systemic lupus erythematosus. Report of a task force of the EULAR standing committee for international clinical studies including therapeutics. Ann Rheum Dis2008; 67(2): 195–205. DOI: 10.1136/ard.2007.070367.
10.
ArkemaEVPalmstenKSjöwallC, et al.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 Res2016; 68(7): 988–994. DOI: 10.1002/acr.22791.
11.
Ateka-BarrutiaOKhamashtaM. The challenge of pregnancy for patients with SLE. Lupus2013; 22(12): 1295–1308. DOI: 10.1177/0961203313504637.
12.
TincaniADanieliENuzzoM, et al. Impact of in utero environment on the offspring of lupus patients. Lupus2006; 15(11): 801–807. DOI: 10.1177/0961203306071005.
13.
UrowitzMGladmanDMacKinnonA, et al. Neurocognitive abnormalities in offspring of mothers with systemic lupus erythematosus. Lupus2008; 17(6): 555–560. DOI: 10.1177/0961203308089326.
14.
NalliCIodiceAAndreoliL, et al.Children born to SLE and APS mothers. Lupus2014; 23(12): 1246–1248. DOI: 10.1177/0961203314538109.
15.
VinetÉPineauCClarkeA, et al.Neurodevelopmental disorders in children born to mothers with systemic lupus erythematosus. Lupus2014; 23(11): 1099–1104. DOI: 10.1177/0961203314541691.
16.
WalleniusMSalvesenKÅDaltveitAK, et al. Systemic lupus erythematosus and outcomes in first and subsequent births based on data from a national birth registry. Arthritis Care Res2014; 66(11): 1718–1724. DOI: 10.1002/acr.22373.
17.
ClowseMEJamisonMMyersE, et al. A national study of the complications of lupus in pregnancy. Am J Obstet Gynecol2008; 199(2): 127–136. DOI: 10.1016/j.ajog.2008.03.012.
18.
SmythAOliveiraGHMLahrBD, et al.A systematic review and meta-analysis of pregnancy outcomes in patients with systemic lupus erythematosus and lupus nephritis. Clin J Am Soc Nephrol2010; 5(11): 2060–2068. DOI: 10.2215/CJN.00240110.
19.
VinetEClarkeAEGordonC, et al.Decreased live births in women with systemic lupus erythematosus. Arthritis Care Res2011; 63(7): 1068–1072. DOI: 10.1002/acr.20466.
20.
ChakravartyEFColónILangenES, et al.Factors that predict prematurity and preeclampsia in pregnancies that are complicated by systemic lupus erythematosus. Am J Obstet Gynecol2005; 192(6): 1897–1904. DOI: 10.1016/j.ajog.2005.02.063.
21.
JohnsonMPetriMWitterF, et al.Evaluation of preterm delivery in a systemic lupus erythematosus pregnancy clinic. Obstet Gynecol1995; 86(3): 396–399. DOI: 10.1016/0029-7844(95)00186-U.
22.
GunnGCMishellDRMortonDG. Premature rupture of the fetal membranes. Am J Obstet Gynecol1970; 106(3): 469–483. DOI: 10.1016/0002-9378(70)90378-9.
23.
GoldenbergRLCulhaneJFIamsJD, et al.Epidemiology and causes of preterm birth. The Lancet2008; 371(9606): 75–84. DOI: 10.1016/S0140-6736(08)60074-4.
LealMdCEsteves-PereiraAPNakamura-PereiraM, et al.Prevalence and risk factors related to preterm birth in Brazil. Reprod Health2016; 13(Suppl 3): 127. DOI: 10.1186/s12978-016-0230-0.
26.
MenonR. Oxidative stress damage as a detrimental factor in preterm birth pathology. Front Immunol2014; 5: 567. DOI: 10.3389/fimmu.2014.00567.
27.
HochbergMC. Updating the American College of rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum1997; 40(9): 1725. DOI: 10.1002/art.1780400928.
28.
BuyonJPKalunianKCRamsey-GoldmanR, et al.Assessing disease activity in SLE patients during pregnancy. Lupus1999; 8(8): 677–684. DOI: 10.1191/096120399680411272.
29.
MoherDLiberatiATetzlaffJThe PRISMA Group, et al.Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med2009; 6(7): e1000097. DOI: 10.1371/journal.pmed1000097.
30.
SheaBJReevesBCWellsG, et al. AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ2017; 358: j4008. DOI: 10.1136/bmj.j4008.
31.
StroupD. F.BerlinJ AMortonSC, et al.Meta-analysis of observational studies in epidemiology: a proposal for reporting. JAMA2000 Apr 19; 283(15): 2008–2012. DOI: 10.1001/jama.283.15.2008.
32.
MoolaSMunnZSearsK, et al.Conducting systematic reviews of association (etiology). Int J Evidence-Based Healthc2015; 13(3): 163–169. DOI: 10.1097/XEB.0000000000000064.
33.
HigginsJPTAltmanDGGotzschePC, et al. The cochrane collaboration’s tool for assessing risk of bias in randomised trials. BMJ2011; 343: d5928. DOI: 10.1136/bmj.d5928.
34.
JaraLJCruz-CruzPSaavedraMA, et al.Bromocriptine during pregnancy in systemic lupus erythematosus: a pilot clinical trial. Ann New York Acad Sci2007; 1110: 297–304. DOI: 10.1196/annals.1423.031.
35.
SaavedraMACruz-ReyesCVera-LastraO, et al.Impact of previous lupus nephritis on maternal and fetal outcomes during pregnancy. Clin Rheumatol2012; 31(5): 813–819. DOI: 10.1007/s10067-012-1941-4.
36.
ZhanZYangYZhanY, et al.Fetal outcomes and associated factors of adverse outcomes of pregnancy in southern Chinese women with systemic lupus erythematosus. PLoS One2017; 12(4): e0176457. DOI: 10.1371/journal.pone.0176457.
37.
LimaFBuchananNMMKhamashtaMA, et al.Obstetric outcome in systemic lupus erythematosus. Semin Arthritis Rheum1995; 25(3): 184–192. DOI: 10.1016/s0049-0172(95)80030-1.
38.
Leaños-MirandaACárdenas-MondragónGUlloa-AguirreA, et al.Anti-prolactin autoantibodies in pregnant women with systemic lupus erythematosus: maternal and fetal outcome. Lupus2007; 16(5): 342–349. DOI: 10.1177/0961203307078197.
39.
RahmanFZRahmanJAl-SuleimanSA, et al.Pregnancy outcome in lupus nephropathy. Arch Gynecol Obstet2005; 271(3): 222–226. DOI: 10.1007/s00404-003-0574-x.
40.
KobayashiNYamadaHKishidaT, et al.Hypocomplementemia correlates with intrauterine growth retardation in systemic lupus erythematosus. Am J Reprod Immunol1999; 42(3): 153–159. DOI: 10.1111/j.1600-0897.1999.tb00479.x.
41.
MoroniGDoriaAGiglioE, et al.Fetal outcome and recommendations of pregnancies in lupus nephritis in the 21st century. A prospective multicenter study. J Autoimmun2016; 74: 6–12. DOI: 10.1016/j.jaut.2016.07.010.
42.
KohJHKoHSLeeJ, et al.Pregnancy and patients with preexisting lupus nephritis: 15 years of experience at a single center in Korea. Lupus2015; 24(7): 764–772. DOI: 10.1177/0961203315572715.
43.
KlumbEMBarrosLMSRomeiroL, et al.Impacto da nefrite sobre os resultados gestacionais de mulheres com lúpus eritematoso sistêmico. Revista Brasileira de Reumatologia2005; 45(3): 107–113.
44.
BerceanuCBratilaECirstoiuM, et al.Clinical and paraclinical approach in antiphospholipid syndrome-systemic lupus erythematosus-pregnancy interrelationship. Eur J Clin Invest2016; 46: 8–9.
45.
AraRRoyJSAhmedS, et al.Pregnancy outcomes in women with systemic lupus erythematosus in a tertiary care hospital of Dhaka, Bangladesh. Int J Rheum Dis2019; 22: 48.
46.
FoocharoenCNanagaraRSalangL, et al.Pregnancy and disease outcome in patients with systemic lupus erythematosus (SLE): a study at Srinagarind Hospital. J Med Assoc Thailand Chotmaihet thangphaet2009; 92(2): 167–174.
47.
TrongkamolthumTWongthaneeAKasitanonN, et al.Pregnancy outcomes in pregnant patients with systemic lupus erythematosus: 23-year experience from Chiang Mai University. Int J Rheum Dis2016; 19: 267.
48.
Farfan-LabonneBLuis-VásquezIÁvila-CarrascoA, et al.Resultados perinatales en mujeres mexicanas con lupus eritematoso sistémico. Perinatología y Reproducción Humana2017; 31(1): 3–9.
49.
AlbaPBOtaduyCGobbiCA, et al.Lupus nehritis and pregnancy: maternal and fetal outcome. Ann Rheum Dis2017; 76: 1220.
50.
RosselloPMariniANadalM, et al. Evolution of pregnant patients with systemic lupus erythematosus (SLE). Lupus2013; 22(1): 166–167.
51.
LerouxMDesveauxCParcevauxM, et al. Impact of hydroxychloroquine on preterm delivery and intrauterine growth restriction in pregnant women with systemic lupus erythematosus: a descriptive cohort study. Lupus2015; 24(13): 1384–1391. DOI: 10.1177/0961203315591027.
52.
SaavedraMÁSánchezAMoralesS, et al.Azathioprine during pregnancy in systemic lupus erythematosus patients is not associated with poor fetal outcome. Clin Rheumatol2015; 34(7): 1211–1216. DOI: 10.1007/s10067-015-2987-x.
53.
KoHSAhnHYJangDG, et al.Pregnancy outcomes and appropriate timing of pregnancy in 183 pregnancies in Korean patients with SLE. Int J Med Sci2011; 8(7): 577–583. DOI: 10.7150/ijms.8.577.
54.
ClowseMEBGrotegutC. Racial and ethnic disparities in the pregnancies of women with systemic lupus erythematosus. Arthritis Care Res2016; 68(10): 1567–1572. DOI: 10.1002/acr.22847.
55.
ChakravartyEFNelsonLKrishnanE. Obstetric hospitalizations in the United States for women with systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum2006; 54(3): 899–907. DOI: 10.1002/art.21663.
56.
WuJMaJBaoC, et al.Pregnancy outcomes among Chinese women with and without systemic lupus erythematosus: a retrospective cohort study. BMJ Open2018; 8(4): e020909. DOI: 10.1136/bmjopen-2017-020909.
57.
EudyAMJayasundaraMHarounT, et al.Reasons for cesarean and medically indicated deliveries in pregnancies in women with systemic lupus erythematosus. Lupus2018; 27(3): 351–356. DOI: 10.1177/0961203317720525.
58.
ClarkCASpitzerKANadlerJN, et al.Preterm deliveries in women with systemic lupus erythematosus. The J rheumatology2003; 30(10): 2127–2132.
59.
CarmonaFFontJCerveraR, et al.Obstetrical outcome of pregnancy in patients with systemic Lupus Erythematosus. A study of 60 cases. Eur J Obstet Gynecol Reprod Biol1999; 83(2): 137–142. DOI: 10.1016/s0301-2115(98)00312-1.
60.
SimardJFChaichianYRossidesM, et al. Preterm delivery phenotypes in systemic lupus erythematosus pregnancies. Am J Perinatology2019; 36(9): 964–968. DOI: 10.1055/s-0038-1675648.
61.
ChenDLaoMZhangJ, et al.Fetal and maternal outcomes of planned pregnancy in patients with systemic lupus erythematosus: a retrospective multicenter study. J Immunol Res2018; 2018: 1–7. DOI: 10.1155/2018/2413637.
62.
PastoreDEACostaMLSuritaFG. Systemic lupus erythematosus and pregnancy: the challenge of improving antenatal care and outcomes. Lupus2019; 28(12): 1417–1426. DOI: 10.1177/0961203319877247.
63.
de JesusGRMendoza-PintoCde JesusNR, et al.Understanding and managing pregnancy in patients with lupus. Autoimmune Dis2015; 2015: 1–18. DOI: 10.1155/2015/943490.
64.
MercerBMGoldenbergRLDasAF, et al.What we have learned regarding antibiotic therapy for the reduction of infant morbidity after preterm premature rupture of the membranes. Semin Perinatology2003; 27(3): 217–230. DOI: 10.1016/s0146-0005(03)00016-8.
65.
PassiniRCecattiJGLajosGJ, et al.Brazilian multicentre study on preterm birth (EMIP): prevalence and factors associated with spontaneous preterm birth. PLoS One2014; 9(10): e109069. DOI: 10.1371/journal.pone.0109069.
66.
Fischer-BetzRSpeckerCBrinksR, et al.Low risk of renal flares and negative outcomes in women with lupus nephritis conceiving after switching from mycophenolate mofetil to azathioprine. Rheumatology2013; 52(6): 1070–1076. DOI: 10.1093/rheumatology/kes425.
67.
BalbiGGMDominguesVBalbiGGM, et al.Use of synthetic and biologic DMARDs during pregnancy. Expert Rev Clin Immunol2019; 15(1): 27–39. DOI: 10.1080/1744666X.2019.1541739.
68.
Götestam SkorpenCHoeltzenbeinMTincaniA, et al.The EULAR points to consider for use of antirheumatic drugs before pregnancy, and during pregnancy and lactation. Ann Rheum Dis2016; 75(5): 795–810. DOI: 10.1136/annrheumdis-2015-208840.
69.
KlumbEPintoAJesusG, et al.Are women with lupus at higher risk of HPV infection?. Lupus2010; 19(13): 1485–1491. DOI: 10.1177/0961203310372952.
70.
Al MaimouniHGladmanDDIbañezD, et al.Switching treatment between mycophenolate mofetil and azathioprine in lupus patients: indications and outcomes. Arthritis Care Res2014; 66(12): 1905–1909. DOI: 10.1002/acr.22364.
71.
FeldmanCHMartyFMWinkelmayerWC, et al.Comparative rates of serious infections among patients with systemic lupus erythematosus receiving immunosuppressive medications. Arthritis Rheumatol2017; 69(2): 387–397. DOI: 10.1002/art.39849.
72.
VinickiJPelletSCPappalardoC, et al.Invasive fungal infections in Argentine patients with systemic lupus erythematosus. Lupus2013; 22(9): 892–898. DOI: 10.1177/0961203313496342.
73.
MenonRBoldoghIHawkinsHK, et al.Histological evidence of oxidative stress and premature senescence in preterm premature rupture of the human fetal membranes recapitulated in vitro. The Am J Pathol2014; 184(6): 1740–1751. DOI: 10.1016/j.ajpath.2014.02.011.
74.
MenonRRichardsonLS. Preterm prelabor rupture of the membranes: A disease of the fetal membranes. Semin Perinatology2017; 41(7): 409–419. DOI: 10.1053/j.semperi.2017.07.012.
75.
LaskinCABombardierCHannahME, et al.Prednisone and aspirin in women with autoantibodies and unexplained recurrent fetal loss. New Engl J Med1997; 337(3): 148–154. DOI: 10.1056/NEJM199707173370302.
76.
DixonCLRichardsonLSheller-MillerS, et al.A distinct mechanism of senescence activation in amnion epithelial cells by infection, inflammation, and oxidative stress. Am J Reprod Immunol2018; 79(3): e12790. DOI: 10.1111/aji.12790.
77.
FortunatoSJMenonRLombardiSJ. Support for an infection-induced apoptotic pathway in human fetal membranes. Am J Obstet Gynecol2001; 184(7): 1392–1398; discussion 1397-1398. DOI: 10.1067/mob.2001.115434.
78.
MooreRMMansourJMRedlineRW, et al.The physiology of fetal membrane rupture: insight gained from the determination of physical properties. Placenta2006; 27(11–12): 1037–1051. DOI: 10.1016/j.placenta.2006.01.002.
79.
WingDAFassettMJGetahunD. Acute pyelonephritis in pregnancy: an 18-year retrospective analysis. Am J Obstet Gynecol2014; 210(3): e1–e6219. DOI: 10.1016/j.ajog.2013.10.006.
BernatskySBoivinJ-FJosephL, et al.Mortality in systemic lupus erythematosus. Arthritis Rheum2006; 54(8): 2550–2557. DOI: 10.1002/art.21955.
82.
DanzaARuiz-IrastorzaG. Infection risk in systemic lupus erythematosus patients: susceptibility factors and preventive strategies. Lupus2013; 22(12): 1286–1294. DOI: 10.1177/0961203313493032.
83.
TedeschiSKGuanHFineA, et al.Organ-specific systemic lupus erythematosus activity during pregnancy is associated with adverse pregnancy outcomes. Clin Rheumatol2016; 35(7): 1725–1732. DOI: 10.1007/s10067-016-3270-5.
84.
DimaAJurcutCBaicusCThe impact of anti-U1-RNP positivity: systemic lupus erythematosus versus mixed connective tissue disease. Rheumatol Int2018; 38(7): 1169–1178. DOI: 10.1007/s00296-018-4059-4.
85.
CarpinteroMFMartinezLFernandezI, et al.Diagnosis and risk stratification in patients with anti-RNP autoimmunity. Lupus2015; 24(10): 1057–1066. DOI: 10.1177/0961203315575586.
86.
MatsuedaYArinumaYNagaiT, et al.Synergistic enhancement of production of proinflammatory cytokines of human peripheral blood monocytes by anti-Sm and anti-RNP antibodies. PLoS One, 2018; 13(12): e0209282. DOI: 10.1371/journal.pone.0209282.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
