Fetal outcome and recommendations of pregnancies in lupus nephritis in the 21st century. A prospective multicenter study

Journal of Autoimmunity

Volumn 74, Issue , 2016, Pages 6-12

  Moroni, Gabriella ^a   Doria, Andrea ^b   Giglio, Elisa ^a   Tani, Chiara ^c   Zen, Margherita ^b   Strigini, Francesca ^c   Zaina, Barbara ^a   Tincani, Angela ^d   de Liso, Federica ^a   Matinato, Caterina ^a   Grossi, Claudia ^e   Gatto, Mariele ^b   Castellana, Paola ^f   Limardo, Monica ^g   Meroni, Pier Luigi ^e,h   Messa, Piergiorgio ^a   Ravani, Pietro ⁱ   Mosca, Marta ^c  

^a FONDAZIONE IRCCS CA GRANDA OSPEDALE MAGGIORE POLICLINICO   (Italy)

^b UNIVERSITY OF PADOVA   (Italy)

^c UNIVERSITY OF PISA   (Italy)

^d Rheumatology and Clinical Immunology Unit   (Italy)

^e IRCCS   (Italy)

^f SAN PAOLO HOSPITAL   (Italy)

^g Azienda Ospedaliera della Provincia di Lecco   (Italy)

^h UNIVERSITY OF MILAN   (Italy)

ⁱ UNIVERSITY OF CALGARY   (Canada)

Author keywords

Fetal outcome; Lupus nephritis; Pregnancy; Preterm delivery; Small for gestational age; Systemic lupus erythematosus

Indexed keywords

ACETYLSALICYLIC ACID; AZATHIOPRINE; CARDIOLIPIN ANTIBODY; CREATININE; CYCLOSPORIN; HEPARIN; HYDROXYCHLOROQUINE; IMMUNOGLOBULIN G ANTIBODY; LUPUS ANTICOAGULANT; PHOSPHOLIPID ANTIBODY; PREDNISONE; AUTOANTIBODY; BIOLOGICAL MARKER; COMPLEMENT COMPONENT C1Q;

ADULT; ARTICLE; ASIAN; CAUCASIAN; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CREATININE BLOOD LEVEL; FEMALE; FETUS OUTCOME; FETUS RISK; FETUS WASTAGE; FOLLOW UP; GLOMERULUS FILTRATION RATE; HISTORY; HUMAN; HYPERTENSION; IMMUNOSUPPRESSIVE TREATMENT; INHERITANCE; LUPUS ERYTHEMATOSUS NEPHRITIS; MAJOR CLINICAL STUDY; MULTICENTER STUDY; OBSERVATIONAL STUDY; PATIENT COUNSELING; PREGNANCY; PREGNANT WOMAN; PREMATURE LABOR; PREMATURITY; PRIORITY JOURNAL; PROSPECTIVE STUDY; PROTEINURIA; RISK FACTOR; SLEDAI; SMALL FOR DATE INFANT; BLOOD; CLINICAL TRIAL; IMMUNOLOGY; ODDS RATIO; PREGNANCY COMPLICATION; PREGNANCY OUTCOME; PROGNOSIS;

ADULT; AUTOANTIBODIES; BIOMARKERS; COMPLEMENT C1Q; FEMALE; HUMANS; LUPUS NEPHRITIS; ODDS RATIO; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY OUTCOME; PREMATURE BIRTH; PROGNOSIS; PROSPECTIVE STUDIES;

EID: 84992612588     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2016.07.010     Document Type: Article

References (69)

1. [1] Mintz, G., Niz, J., Gutierrez, G., Garcia-Alonso, A., Karchmer, S., Prospective study of pregnancy in systemic lupus erythematosus. Results of a multidisciplinary approach. J. Rheumatol. 13 (1986), 732–739.
2. [2] Oviasu, E., Hicks, J., Cameron, J.S., The outcome of pregnancy in women with lupus nephritis. Lupus 1 (1991), 19–25.
3. [3] Packham, D.K., Lam, S.S., Nicholls, K., Fairley, K.F., Kincaid-Smith, P.S., Lupus nephritis and pregnancy. Q. J. Med. 83 (1992), 315–324.
4. [4] Imbasciati, E., Surian, M., Bottino, S., Cosci, P., Colussi, G., Ambroso, G.C., et al. Lupus nephropathy and pregnancy. A study of 26 pregnanciesin patients with systemic lupus erythematosus and nephritis. Nephron 36 (1984), 46–51.
5. [5] Moroni, G., Quaglini, S., Banfi, G., Caloni, M., Finazzi, S., Ambroso, G., et al. Pregnancy in lupus nephritis. Am. J. Kidney Dis. 40 (2002), 713–720.
6. [6] Huong, D.L., Papo, T., Beaufils, H., Wechsler, B., Blétry, O., Baumelou, A., Godeau, P., Piette, J.C., Renal involvement in systemic lupus erythematosus. A study of 180 patients from a single center. Med. Baltim. 78 (1999), 148–166.
7. [7] Abu-Shakra, M., Urowitz, M.B., Gladman, D.D., Gough, J., Mortality studies in systemic lupus erythematosus. Results from a single center. I. Causes of death. J. Rheumatol. 22 (1995), 1259–1264.
8. [8] Clark, C.A., Spitzer, K.A., Laskin, C.A., Decrease in pregnancy loss rates in patients with systemic lupus erythematosus over a 40-year period. J. Rheumatol. 32 (2005), 1709–1712.
9. [9] Huong, D.L., Wechsler, B., Vauthier-Brouzes, D., Beaufils, H., Lefebvre, G., Piette, J.C., Pregnancy in past or present lupus nephritis: a study of 32 pregnancies from a single centre. Ann. Rheum. Dis. 60 (2001), 599–604.
10. [10] Imbasciati, E., Tincani, A., Gregorini, G., Doria, A., Moroni, G., Cabiddu, G., et al. Pregnancy in women with pre-existing lupus nephritis: predictors of fetal and maternal outcome. Nephrol. Dial. Transpl. 24 (2009), 519–525.
11. [11] Smyth, A., Oliveira, G.H., Lahr, B.D., Bailey, K.R., Norby, S.M., Garovic, V.D., A systematic review and meta-analysis of pregnancy outcomes in patients with systemic lupus erythematosus and lupus nephritis. Clin. J. Am. Soc. Nephrol. 5 (2010), 2060–2068.
12. [12] Liu, J., Zhao, Y., Song, Y., Zhang, W., Bian, X., Yang, J., et al. Pregnancy in women with systemic lupus erythematosus: a retrospective study of 111 pregnancies in Chinese women. J. Matern. Fetal Neonatal. Med. 25 (2012), 261–266.
13. [13] Saavedra, M.A., Cruz-Reyes, C., Vera-Lastra, O., Romero, G.T., Cruz-Cruz, P., Arias-Flores, R., et al. Impact of previous lupus nephritis on maternal and fetal outcomes during pregnancy. Clin. Rheumatol. 31 (2012), 813–819.
14. [14] Wagner, S.J., Craici, I., Reed, D., Norby, S., Bailey, K., Wiste, H.J., et al. Maternal and foetal outcomes in pregnant patients with active lupus nephritis. Lupus 18 (2009), 342–347.
15. [15] Clowse, M.E., Magder, L.S., Witter, F., Petri, M., Early risk factors for pregnancy loss in lupus. Obstet. Gynecol. 107:2 Pt 1 (2006), 293–299.
16. [16] Clowse, M.E., Magder, L.S., Petri, M., The clinical utility of measuring complement and anti-dsDNA antibodies during pregnancy in patients with systemic lupus erythematosus. J. Rheumatol. 38 (2011), 1012–1016.
17. [17] Clowse, M.E., Wallace, D.J., Weisman, M., James, A., Criscione-Schreiber, L.G., Pisetsky, D.S., Predictors of preterm birth in patients with mild systemic lupus erythematosus. Ann. Rheum. Dis. 72 (2013), 1536–1539.
18. [18] de Jesus, G.R., Agmon-Levin, N., Andrade, C.A., Andreoli, L., Chighizola, C.B., Porter, T.F., 14th international congress on antiphospholipid antibodies task force report on obstetric antiphospholipid syndrome. Autoimmun. Rev. 13 (2014), 795–813.
19. [19] Levy, R.A., Dos Santos, F.C., de Jesús, G.R., de Jesús, N.R., Antiphospholipid antibodies and antiphospholipid syndrome during pregnancy: diagnostic concepts. Front. Immunol., 6, 2015, 205.
20. [20] Lockshin, M.D., Kim, M., Laskin, C.A., Guerra, M., Branch, D.W., Merrill, J., et al. Prediction of adverse pregnancy outcome by the presence of lupus anticoagulant, but not anticardiolipin antibody, in patients with antiphospholipid antibodies. Arthritis Rheum. 64 (2012), 2311–2318.
21. [21] Carvalheiras, G., Faria, R., Braga, J., Vasconcelos, C., Fetal outcome in autoimmune diseases. Autoimmun. Rev. 11 (2012), A520–A530.
22. [22] Abou-Nassar, K., Carrier, M., Ramsay, T., Rodger, M.A., The association between antiphospholipid antibodies and placenta mediated complications: a systematic review and meta-analysis. Thromb. Res. 128 (2011), 77–85.
23. [23] De Carolis, S., Botta, A., Santucci, S., Salvi, S., Moresi, S., Di Pasquo, E., et al. Complementemia and obstetric outcome in pregnancy with antiphospholipid syndrome. Lupus 21 (2012), 776–778.
24. [24] Carmona, F., Font, J., Moga, I., Làzaro, I., Cervera, R., Pac, V., et al. Class III-IV proliferative lupus nephritis and pregnancy: a study of 42 cases. Am. J. Reprod. Immunol. 53 (2005), 182–188.
25. [25] Koh, J.H., Ko, H.S., Lee, J., Jung, S.M., Kwok, S.K., Ju, J.H., et al. Pregnancy and patients with preexisting lupus nephritis: 15 years of experience at a single center in Korea. Lupus 24 (2015), 764–772.
26. [26] Moroni, G., Doria, A., Giglio, E., Imbasciati, E., Tani, C., Zen, M., et al. Maternal outcome in pregnant women with lupus nephritis. A prospective multicenter study. J. Autoimmun., 30, 2016, 10.1016/j.jaut.2016.06.012.
27. [27] Hochberg, M.C., Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis. Rheum., 40, 1997, 1725.
28. [28] Finster, M., Wood, M., The Apgar score has survived the test of times. Anesthesiology 102 (2005), 855–885.
29. [29] Brown, M.A., Lindheimer, M.D., de Swiet, M., Van Assche, A., Moutquin, J.M., The classification and diagnosis of the hypertensive disorders of pregnancy: statement from the International Society for the Study of Hypertension in Pregnancy (ISSHP). Hypertens. Pregnancy, 20, 2001 (IX-XIV).
30. [30] Audibert, F., Friedman, S.A., Frangieh, A.Y., Sibai, B.M., Clinical utility of strict diagnostic criteria for the HELLP (hemolysis, elevated liver enzymes, and low platelets) syndrome. Am. J. Obstet. Gynecol. 175 (1996), 460–464.
31. [31] Petri, M., Genovese, M., Engle, E., Hochberg, M., Definition, incidence, and clinical description of flare in systemic lupus erythematosus. A prospective cohort study. Arthritis Rheum. 34 (1991), 937–944.
32. [32] de Liso, F., Matinato, C., Novembrino, C., Radice, A., Raffiotta, F., Ronchi, M., et al. Value of a commercial Kit for detecting anti-C1q antibodies and correlation with immunological and clincial activity of lupus nephritis. Clin. Chem. Lab. Med. 53 (2015), 1771–1777.
33. [33] Meroni, P.L., Macor, P., Durigutto, P., De Maso, L., Gerosa, M., Ferraresso, M., et al. Complement activation in antiphospholipid syndrome and its inhibition to prevent rethrombosis after arterial surgery. Blood 127 (2016), 365–367.
34. [34] Weening, J.J., D'Agati, V.D., Schwartz, M.M., Seshan, S.V., Alpers, C.E., Appel, G.B., et al. The classification of glomerulonephritis in systemic lupus erythematosus revisited. J. Am. Soc. Nephrol. 15 (2004), 241–250.
35. [35] Alshohaib, S., Outcome of pregnancy in patients with inactive systemic lupus erythromatosus and minimal proteinuria. Saudi. J. Kidney Dis. Transpl. 20 (2009), 802–805.
36. [36] Kwok, L.W., Tam, L.S., Zhu, T., Leung, Y.Y., Li, E., Predictors of maternal and fetal outcomes in pregnancies of patients with systemic lupus erythematosus. Lupus 20 (2011), 829–836.
37. [37] Tandon, A., Ibañez, D., Gladman, D.D., Urowitz, M.B., The effect of pregnancy on lupus nephritis. Arthritis Rheum. 50 (2004), 3941–3946.
38. [38] Gladman, D.D., Tandon, A., Ibañez, D., Urowitz, M.B., The effect of lupus nephritis on pregnancy outcome and fetal and maternal complications. J. Rheumatol. 37 (2010), 754–758.
39. [39] Al Arfaj, A.S., Khalil, N., Pregnancy outcome in 396 pregnancies in patients with SLE in Saudi Arabia. Lupus 19 (2010), 1665–1673.
40. [40] Fischer-Betz, R., Specker, C., Brinks, R., Aringer, M., Schneider, M., Low risk of renal flares and negative outcomes in women with lupus nephritis conceiving after switching from mycophenolate mofetil to azathioprine. Rheumatology 52 (2013), 1070–1076.
41. [41] Buyon, J.P., Kim, M.Y., Guerra, M.M., Laskin, C.A., Petri, M., Lockshin, M.D., et al. Predictors of pregnancy outcomes in patients with lupus: a cohort study. Ann. Intern. Med. 163 (2015), 153–163.
42. [42] Clowse, M.E., Magder, L.S., Witter, F., Petri, M., The impact of increased lupus activity on obstetric outcomes. Arthritis Rheum. 52 (2005), 514–521.
43. [43] Gilbert, J.S., Ryan, M.J., LaMarca, B.B., Sedeek, M., Murphy, S.R., Granger, J.P., Pathophysiology of hypertension during preeclampsia: linking placental ischemia with endothelial dysfunction. Am. J. Physiol. Heart. Circ. Physiol. 294 (2008), H541–H550.
44. [44] American College of Obstetricians and Gynecologists, Task force on hypertension in pregnancy, hypertension in pregnancy. Report of the American college of obstetricians and Gynecologists’ task force on hypertension in pregnancy. Obstet. Gynecol. 122 (2013), 1122–1131.
45. [45] Cavallasca, J.A., Laborde, H.A., Ruda-Vega, H., Nasswetter, G.G., Maternal and fetal outcomes of 72 pregnancies in Argentine patients with systemic lupus erythematosus (SLE). Clin. Rheumatol. 27 (2008), 41–46.
46. [46] Chakravarty, E.F., Colón, I., Langen, E.S., Nix, D.A., El-Sayed, Y.Y., Genovese, M.C., et al. Factors that predict prematurity and preeclampsia in pregnancies that are complicated by systemic lupus erythematosus. Am. J. Obstet. Gynecol. 192 (2005), 1897–1904.
47. [47] Borella, E., Lojacono, A., Gatto, M., Andreoli, L., Taglietti, M., Iaccarino, L., et al. Predictors of maternal and fetal complications in SLE patients: a prospective study. Immunol. Res. 60 (2014), 170–176.
48. [48] Petri, M., Howard, D., Repke, J., Goldman, D.W., The Hopkins lupus pregnancy center: 1987-1991 update. Am. J. Reprod. Immunol. 28 (1992), 188–191.
49. [49] de Jong, F., Monuteaux, M.C., van Elburg, R.M., Gillman, M.W., Belfort, M.B., Systematic review and meta-analysis of preterm birth and later systolic blood pressure. Hypertension 59 (2012), 226–234.
50. [50] Mu, M., Wang, S.F., Sheng, J., Zhao, Y., Li, H.Z., Hu, C.L., et al. Birth weight and subsequent blood pressure: a meta-analysis. Arch. Cardiovasc. Dis. 105 (2012), 99–113.
51. [51] Report of the national high blood pressure education program working Group on high blood pressure in pregnancy. Am. J. Obstet. Gynecol. 183 (2000), S1–S22.
52. [52] Ryan, M.J., The pathophysiology of hypertension in systemic lupus erythematosus. Am. J. Physiol. Regul. Integr. Comp. Physiol. 296 (2009), R1258–R1267.
53. [53] Lindheimer, M.D., Taler, S.J., Cunningham, F.G., Hypertension in pregnancy. J. Am. Soc. Hypertens., 4, 2010 68–67.
54. [54] Zetterstrom, K., Lindeberg, S.N., Haglund, B., Hanson, U., Chronic hypertension as a risk factor for offspring to be born small for gestational age. Acta Obstet. Gynecol. Scand. 85 (2006), 1046–1050.
55. [55] Allen, V.M., Joseph, K., Murphy, K.E., Magee, L.A., Ohlsson, A., The effect of hypertensive disorders in pregnancy on small for gestational age and stillbirth: a population based study. BMC Pregnancy Childbirth, 4, 2004, 17.
56. [56] Magee, L.A., von Dadelszen, P., Bohun, C.M., Rey, E., El-Zibdeh, M., Stalker, S., et al. Serious perinatal complications of non-proteinuric hypertension: an international, multicentre, retrospective cohort study. J. Obstet. Gynaecol. Can. 25 (2003), 372–382.
57. [57] Magee, L.A., Pels, A., Helewa, M., Rey, E., von Dadelszen, P., Diagnosis, evaluation, and management of the hypertensive disorders of pregnancy. J. Obstet. Gynaecol. Can. 36 (2014), 575–576.
58. [58] Clowse, M.E., Magder, L., Witter, F., Petri, M., Hydroxychloroquine in lupus pregnancy. Arthritis Rheum. 54 (2006), 3640–3647.
59. [59] Leroux, M., Desveaux, C., Parcevaux, M., Julliac, B., Gouyon, J.B., Dallay, D., et al. Impact of hydroxychloroquine on preterm delivery and intrauterine growth restriction in pregnant women with systemic lupus erythematosus: a descriptive cohort study. Lupus 24 (2015), 1384–1391.
60. [60] Ponticelli, C., Moroni, G., Immunosuppression in pregnant women with systemic lupus erythematosus. Expert Rev. Clin. Immunol. 11 (2015), 549–552.
61. [61] Hayslett, J.P., Lynn, R.I., Effect of pregnancy in patients with lupus nephropathy. Kidney Int. 18 (1980), 207–220.
62. [62] Leroux, M., Desveaux, C., Parcevaux, M., Lazaro, E., Impact of hydroxychloroquine on preterm delivery and intrauterine growth restriction in pregnant women with systemic lupus erythematosus: a descriptive cohort study. Lupus 24 (2015), 1384–1391.
63. [63] Izmirly, P.M., Costedoat-Chalumeau, N., Pisoni, C.N., Khamashta, M.A., Kim, M.Y., Saxena, A., et al. Maternal use of Hydroxychloroquine is associated with a reduced risk of recurrent anti-SSA/Ro-antibody–associated cardiac manifestations of neonatal lupus. Circulation 126 (2012), 76–82.
64. [64] Coomarasamy, A., Honest, H., Papaioannou, S., Gee, H., Khan, K.S., Aspirin for prevention of preeclampsia in women with historical risk factors: a systematic review. Obstet. Gynecol. 101 (2003), 1319–1332.
65. [65] Duley, L., Henderson-Smart, D.J., Knight, M., King, J.F., Antiplatelet agents for preventing pre-eclampsia and its complications. Cochrane Database Syst. Rev., 2004, CD004659.
66. [66] Abadi, S., Einarson, A., Koren, G., Use of warfarin during pregnancy. Can. Fam. Physician 48 (2002), 695–697.
67. [67] Ruffatti, A., Salvan, E., Del Ross, T., Gerosa, M., Andreoli, L., Maina, A., et al. Treatment strategies and pregnancy outcomes in antiphospholipid syndrome patients with thrombosis and triple antiphospholipid positivity. A European multicenter retrospective study. Thromb. Haemost. 112 (2014), 727–735.
68. [68] Petri, M., Immunosuppressive drug use in pregnancy. Autoimmunity 36 (2003), 51–56.
69. [69] Chen, C.W., Jaffe, I.Z., Karumanchi, S.A., Pre-eclampsia and cardiovascular disease. Cardiovasc. Res. 101 (2014), 579–586.