Pregnancy and Lupus Nephritis

Seminars in Nephrology

Volumn 35, Issue 5, 2015, Pages 487-499

  Kattah, Andrea G ^a   Garovic, Vesna D ^a  

^a MAYO CLINIC   (United States)

Author keywords

Anti inflammatory agents therapeutic use; Lupus nephritis; Preeclampsia; Pregnancy; Pregnancy complications; Systemic lupus erythematosus

Indexed keywords

ACETYLSALICYLIC ACID; ANTICOAGULANT AGENT; BIOLOGICAL PRODUCT; CALCINEURIN INHIBITOR; CYTOTOXIC AGENT; HYDROXYCHLOROQUINE; STEROID; ANTIHYPERTENSIVE AGENT; FIBRINOLYTIC AGENT; IMMUNOSUPPRESSIVE AGENT;

ANTIPHOSPHOLIPID SYNDROME; ARTICLE; BLOOD PRESSURE REGULATION; CONGENITAL HEART BLOCK; FEMALE FERTILITY; FETUS OUTCOME; HUMAN; IMMUNE SYSTEM; IMMUNOSUPPRESSIVE TREATMENT; KIDNEY FUNCTION; LUPUS ERYTHEMATOSUS NEPHRITIS; MATERNAL CARE; NONHUMAN; PHARMACEUTICAL CARE; PREECLAMPSIA; PREGNANCY; PREGNANCY OUTCOME; PRENATAL CARE; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS; ABORTION, SPONTANEOUS; DISEASE COURSE; FEMALE; HYPERTENSION; IMMUNOLOGY; KIDNEY; LUPUS ERYTHEMATOSUS, SYSTEMIC; LUPUS NEPHRITIS; PHYSIOLOGY; PRE-ECLAMPSIA; PREGNANCY COMPLICATIONS; PREMATURE BIRTH; RISK FACTOR;

ABORTION, SPONTANEOUS; ANTICOAGULANTS; ANTIHYPERTENSIVE AGENTS; ANTIPHOSPHOLIPID SYNDROME; ASPIRIN; DISEASE PROGRESSION; FEMALE; FIBRINOLYTIC AGENTS; HUMANS; HYPERTENSION; IMMUNOSUPPRESSIVE AGENTS; KIDNEY; LUPUS ERYTHEMATOSUS, SYSTEMIC; LUPUS NEPHRITIS; PRE-ECLAMPSIA; PREGNANCY; PREGNANCY COMPLICATIONS; PREGNANCY OUTCOME; PREMATURE BIRTH; RISK FACTORS;

EID: 84961579302     PISSN: 02709295     EISSN: 15584488     Source Type: Journal    
DOI: 10.1016/j.semnephrol.2015.08.010     Document Type: Review

References (98)

1. Ortega L.M., Schultz D.R., Lenz O., Pardo V., Contreras G.N. Review: lupus nephritis: pathologic features, epidemiology and a guide to therapeutic decisions. Lupus 2010, 19:557-574.
2. Domsic R.T., Manzi S. Epidemiology and classification of systemic lupus erythematosus 2008, Mosby Elsevier, Philadelphia. 4th ed. M.C. Hochberg, J.S. Smolen (Eds.).
3. Clowse M.E., Jamison M., Myers E., James A.H. A national study of the complications of lupus in pregnancy. Am J Obstet Gynecol 2008, 199(127):e1-e6.
4. Chakravarty E.F., Nelson L., Krishnan E. Obstetric hospitalizations in the United States for women with systemic lupus erythematosus and rheumatoid arthritis. Arthritis Rheum 2006, 54:899-907.
5. To C.H., Petri M. Is antibody clustering predictive of clinical subsets and damage in systemic lupus erythematosus?. Arthritis Rheum 2005, 52:4003-4010.
6. Zen M., Ghirardello A., Iaccarino L., Tonon M., Campana C., Arienti S., et al. Hormones, immune response, and pregnancy in healthy women and SLE patients. Swiss Med Wkly 2010, 140:187-201.
7. 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 2010, 5:2060-2068.
8. Lockshin M.D., Reinitz E., Druzin M.L., Murrman M., Estes D. Lupus pregnancy. Case-control prospective study demonstrating absence of lupus exacerbation during or after pregnancy. Am J Med 1984, 77:893-898.
9. Urowitz M.B., Gladman D.D., Farewell V.T., Stewart J., McDonald J. Lupus and pregnancy studies. Arthritis Rheum 1993, 36:1392-1397.
10. Petri M., Howard D., Repke J. Frequency of lupus flare in pregnancy. The Hopkins Lupus Pregnancy Center experience. Arthritis Rheum 1991, 34:1538-1545.
11. Ruiz-Irastorza G., Lima F., Alves J., Khamashta M.A., Simpson J., Hughes G.R., et al. Increased rate of lupus flare during pregnancy and the puerperium: a prospective study of 78 pregnancies. Br J Rheumatol 1996, 35:133-138.
12. Smyth A., Radovic M., Garovic V.D. Women, kidney disease, and pregnancy. Adv Chronic Kidney Dis 2013, 20:402-410.
13. Bramham K., Lightstone L. Pre-pregnancy counseling for women with chronic kidney disease. J Nephrol 2012, 25:450-459.
14. Bramham K., Hunt B.J., Bewley S., Germain S., Calatayud I., Khamashta M.A., et al. Pregnancy outcomes in systemic lupus erythematosus with and without previous nephritis. J Rheumatol 2011, 38:1906-1913.
15. Chen H.H., Lin H.C., Yeh J.C., Chen C.P. Renal biopsy in pregnancies complicated by undetermined renal disease. Acta Obstet Gynecol Scand 2001, 80:888-893.
16. Germain S., Nelson-Piercy C. Lupus nephritis and renal disease in pregnancy. Lupus 2006, 15:148-155.
17. 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 Transplant 2009, 24:519-525.
18. 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 2011, 20:829-836.
19. Moroni G., Quaglini S., Banfi G., Caloni M., Finazzi S., Ambroso G., et al. Pregnancy in lupus nephritis. Am J Kidney Dis 2002, 40:713-720.
20. Bertsias G.K., Tektonidou M., Amoura Z., Aringer M., Bajema I., Berden J.H., et al. Joint European League Against Rheumatism and European Renal Association-European Dialysis and Transplant Association (EULAR/ERA-EDTA) recommendations for the management of adult and paediatric lupus nephritis. Ann Rheum Dis 2012, 71:1771-1782.
21. Shames R.S. Gender differences in the development and function of the immune system. J Adolesc Health 2002, 30(Suppl):59-70.
22. Lin H., Mosmann T.R., Guilbert L., Tuntipopipat S., Wegmann T.G. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 1993, 151:4562-4573.
23. Shabanova S.S., Ananieva L.P., Alekberova Z.S., Guzov I.I. Ovarian function and disease activity in patients with systemic lupus erythematosus. Clin Exp Rheumatol 2008, 26:436-441.
24. Doria A., Cutolo M., Ghirardello A., Zampieri S., Vescovi F., Sulli A., et al. Steroid hormones and disease activity during pregnancy in systemic lupus erythematosus. Arthritis Rheum 2002, 47:202-209.
25. Jara-Quezada L., Graef A., Lavalle C. Prolactin and gonadal hormones during pregnancy in systemic lupus erythematosus. J Rheumatol 1991, 18:349-353.
26. Doria A., Ghirardello A., Iaccarino L., Zampieri S., Punzi L., Tarricone E., et al. Pregnancy, cytokines, and disease activity in systemic lupus erythematosus. Arthritis Rheum 2004, 51:989-995.
27. Munoz-Valle J.F., Vazquez-Del Mercado M., Garcia-Iglesias T., Orozco-Barocio G., Bernard-Medina G., Martinez-Bonilla G., et al. T(H)1/T(H)2 cytokine profile, metalloprotease-9 activity and hormonal status in pregnant rheumatoid arthritis and systemic lupus erythematosus patients. Clin Exp Immunol 2003, 131:377-384.
28. Aluvihare V.R., Kallikourdis M., Betz A.G. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004, 5:266-271.
29. Valencia X., Yarboro C., Illei G., Lipsky P.E. Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus. J Immunol 2007, 178:2579-2588.
30. Lyssuk E.Y., Torgashina A.V., Soloviev S.K., Nassonov E.L., Bykovskaia S.N. Reduced number and function of CD4+CD25highFoxP3+ regulatory T cells in patients with systemic lupus erythematosus. Adv Exp Med Biol 2007, 601:113-119.
31. Tower C., Crocker I., Chirico D., Baker P., Bruce I. SLE and pregnancy: the potential role for regulatory T cells. Nat Rev Rheumatol 2011, 7:124-128.
32. Smith M.C., Moran P., Ward M.K., Davison J.M. Assessment of glomerular filtration rate during pregnancy using the MDRD formula. Bjog 2008, 115:109-112.
33. Cunningham F., Leveno K., Bloom S., Hauth J., Rouse D., Spong C. Maternal physiology 2010, McGraw-Hill, New York. 23rd ed.
34. Higby K., Suiter C.R., Phelps J.Y., Siler-Khodr T., Langer O. Normal values of urinary albumin and total protein excretion during pregnancy. Am J Obstet Gynecol 1994, 171:984-989.
35. Report of the American College of Obstetricians and Gynecologists' Task Force on Hypertension in Pregnancy. Obstet Gynecol 2013, 122:1122-1131. Hypertension in pregnancy.
36. Schwarz E.B., Manzi S. Risk of unintended pregnancy among women with systemic lupus erythematosus. Arthritis Rheum 2008, 59:863-866.
37. Park M.C., Park Y.B., Jung S.Y., Chung I.H., Choi K.H., Lee S.K. Risk of ovarian failure and pregnancy outcome in patients with lupus nephritis treated with intravenous cyclophosphamide pulse therapy. Lupus 2004, 13:569-574.
38. Dooley M.A., Nair R. Therapy Insight: preserving fertility in cyclophosphamide-treated patients with rheumatic disease. Nat Clin Pract Rheumatol 2008, 4:250-257.
39. Ruiz-Irastorza G., Khamashta M.A. Lupus and pregnancy: ten questions and some answers. Lupus 2008, 17:416-420.
40. Gladman D.D., Tandon A., Ibanez D., Urowitz M.B. The effect of lupus nephritis on pregnancy outcome and fetal and maternal complications. J Rheumatol 2010, 37:754-758.
41. Clowse M.E. Lupus activity in pregnancy. Rheum Dis Clin North Am 2007, 33:237-252. v.
42. 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 2008, 27:41-46.
43. Chakravarty E.F., Colon 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 2005, 192:1897-1904.
44. Clowse M.E., Magder L.S., Witter F., Petri M. The impact of increased lupus activity on obstetric outcomes. Arthritis Rheum 2005, 52:514-521.
45. Smyth A., Garovic V.D. Systemic lupus erythematosus and pregnancy. Minerva Urol Nefrol 2009, 61:457-474.
46. Ko H.S., Ahn H.Y., Jang D.G., Choi S.K., Park Y.G., Park I.Y., et al. Pregnancy outcomes and appropriate timing of pregnancy in 183 pregnancies in Korean patients with SLE. Int J Med Sci 2011, 8:577-583.
47. Ritchie J., Smyth A., Tower C., Helbert M., Venning M., Garovic V. Maternal deaths in women with lupus nephritis: a review of published evidence. Lupus 2012, 21:534-541.
48. 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 2012, 31:813-819.
49. Petri M. Hopkins Lupus Pregnancy Center: 1987 to 1996. Rheum Dis Clin North Am 1997, 23:1-13.
50. Clowse M.E., Magder L.S., Witter F., Petri M. Early risk factors for pregnancy loss in lupus. Obstet Gynecol 2006, 107:293-299.
51. 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 2009, 18:342-347.
52. Rahman P., Gladman D.D., Urowitz M.B. Clinical predictors of fetal outcome in systemic lupus erythematosus. J Rheumatol 1998, 25:1526-1530.
53. Carmona F., Font J., Moga I., Lazaro I., Cervera R., Pac V., et al. Class III-IV proliferative lupus nephritis and pregnancy: a study of 42 cases. Am J Reprod Immunol 2005, 53:182-188.
54. 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 2005, 32:1709-1712.
55. Askanase A.D., Friedman D.M., Copel J., Dische M.R., Dubin A., Starc T.J., et al. Spectrum and progression of conduction abnormalities in infants born to mothers with anti-SSA/Ro-SSB/La antibodies. Lupus 2002, 11:145-151.
56. Baer A.N., Witter F.R., Petri M. Lupus and pregnancy. Obstet Gynecol Surv 2011, 66:639-653.
57. Stanhope T.J., White W.M., Moder K.G., Smyth A., Garovic V.D. Obstetric nephrology: lupus and lupus nephritis in pregnancy. Clin J Am Soc Nephrol 2012, 7:2089-2099.
58. Cnossen J.S., Morris R.K., ter Riet G., Mol B.W., van der Post J.A., Coomarasamy A., et al. Use of uterine artery Doppler ultrasonography to predict pre-eclampsia and intrauterine growth restriction: a systematic review and bivariable meta-analysis. Cmaj 2008, 178:701-711.
59. Madazli R., Yuksel M.A., Oncul M., Imamoglu M., Yilmaz H. Obstetric outcomes and prognostic factors of lupus pregnancies. Arch Gynecol Obstetrics 2014, 289:49-53.
60. Buyon J.P., Tamerius J., Ordorica S., Young B., Abramson S.B. Activation of the alternative complement pathway accompanies disease flares in systemic lupus erythematosus during pregnancy. Arthritis Rheum 1992, 35:55-61.
61. Cortes-Hernandez J., Ordi-Ros J., Paredes F., Casellas M., Castillo F., Vilardell-Tarres M. Clinical predictors of fetal and maternal outcome in systemic lupus erythematosus: a prospective study of 103 pregnancies. Rheumatology (Oxford) 2002, 41:643-650.
62. 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 2011, 38:1012-1016.
63. Day C., Hewins P., Hildebrand S., Sheikh L., Taylor G., Kilby M., et al. The role of renal biopsy in women with kidney disease identified in pregnancy. Nephrol Dial Transplant 2008, 23:201-206.
64. Daugas E., Nochy D., Huong D.L., Duhaut P., Beaufils H., Caudwell V., et al. Antiphospholipid syndrome nephropathy in systemic lupus erythematosus. J Am Soc Nephrol 2002, 13:42-52.
65. Moroni G., Ventura D., Riva P., Panzeri P., Quaglini S., Banfi G., et al. Antiphospholipid antibodies are associated with an increased risk for chronic renal insufficiency in patients with lupus nephritis. Am J Kidney Dis 2004, 43:28-36.
66. do Prado A.D., Piovesan D.M., Staub H.L., Horta B.L. Association of anticardiolipin antibodies with preeclampsia: a systematic review and meta-analysis. Obstet Gynecol 2010, 116:1433-1443.
67. Bates S.M., Greer I.A., Pabinger I., Sofaer S., Hirsh J. Venous thromboembolism, thrombophilia, antithrombotic therapy, and pregnancy: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines (8th edition). Chest 2008, 133(Suppl):844S-886S.
68. Miyakis S., Lockshin M.D., Atsumi T., Branch D.W., Brey R.L., Cervera R., et al. International consensus statement on an update of the classification criteria for definite antiphospholipid syndrome (APS). J Thromb Haemost 2006, 4:295-306.
69. von Dadelszen P., Ornstein M.P., Bull S.B., Logan A.G., Koren G., Magee L.A. Fall in mean arterial pressure and fetal growth restriction in pregnancy hypertension: a meta-analysis. Lancet 2000, 355:87-92.
70. Cooper W.O., Hernandez-Diaz S., Arbogast P.G., Dudley J.A., Dyer S., Gideon P.S., et al. Major congenital malformations after first-trimester exposure to ACE inhibitors. N Engl J Med 2006, 354:2443-2451.
71. Butters L., Kennedy S., Rubin P.C. Atenolol in essential hypertension during pregnancy. BMJ 1990, 301:587-589.
72. Kattah A.G., Garovic V.D. The management of hypertension in pregnancy. Adv Chronic Kidney Dis 2013, 20:229-239.
73. Mariotti V., Marconi A.M., Pardi G. Undesired effects of steroids during pregnancy. J Matern Fetal Neonatal Med 2004, 16(Suppl 2):5-7.
74. Fraser F.C., Sajoo A. Teratogenic potential of corticosteroids in humans. Teratology 1995, 51:45-46.
75. Hviid A., Molgaard-Nielsen D. Corticosteroid use during pregnancy and risk of orofacial clefts. Cmaj 2011, 183:796-804.
76. 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, 23:1192-1196.
77. Costedoat-Chalumeau N., Amoura Z., Huong D.L., Lechat P., Piette J.C. Safety of hydroxychloroquine in pregnant patients with connective tissue diseases. Review of the literature. Autoimmun Rev 2005, 4:111-115.
78. Clowse M.E., Magder L., Witter F., Petri M. Hydroxychloroquine in lupus pregnancy. Arthritis Rheum 2006, 54:3640-3647.
79. Ostensen 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.
80. Anderka M.T., Lin A.E., Abuelo D.N., Mitchell A.A., Rasmussen S.A. Reviewing the evidence for mycophenolate mofetil as a new teratogen: case report and review of the literature. Am J Med Genet A 2009, 149A:1241-1248.
81. Section IV: long-term management of the transplant recipient. IV.10. Pregnancy in renal transplant recipients. Nephrol Dial Transplant 2002, 17(Suppl 4):50-55. European best practice guidelines for renal transplantation.
82. 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 (Oxford) 2013, 52:1070-1076.
83. Coscia L.A., Armenti V.T. Transplantation: pregnancy outcomes in kidney recipients: more data are needed. Nat Rev Nephrol 2010, 6:131-132.
84. Chen W., Tang X., Liu Q., Fu P., Liu F., Liao Y., et al. Short-term outcomes of induction therapy with tacrolimus versus cyclophosphamide for active lupus nephritis: a multicenter randomized clinical trial. Am J Kidney Dis 2011, 57:235-244.
85. Alsuwaida A. Successful management of systemic lupus erythematosus nephritis flare-up during pregnancy with tacrolimus. Mod Rheumatol 2011, 21:73-75.
86. Hou S. Pregnancy in renal transplant recipients. Adv Chronic Kidney Dis 2013, 20:253-259.
87. Jain A., Venkataramanan R., Lever J., Warty V., Fung J., Todo S., et al. FK506 and pregnancy in liver transplant patients. Transplantation 1993, 56:1588-1589.
88. Clowse M.E., Magder L., Petri M. Cyclophosphamide for lupus during pregnancy. Lupus 2005, 14:593-597.
89. Hahn K.M., Johnson P.H., Gordon N., Kuerer H., Middleton L., Ramirez M., et al. Treatment of pregnant breast cancer patients and outcomes of children exposed to chemotherapy in utero. Cancer 2006, 107:1219-1226.
90. Gupta R., Deepanjali S., Thabah M.M., Kaur P., Gupta S. Successful twin pregnancy while on cyclophosphamide therapy in a patient with lupus nephritis. Rheumatol Int 2009, 29:1503-1505.
91. Fernandez M., Andrade R., Alarcon G.S. Cyclophosphamide use and pregnancy in lupus. Lupus 2006, 15:59.
92. Moroni G., Ponticelli C. Pregnancy after lupus nephritis. Lupus 2005, 14:89-94.
93. Cassina M., Johnson D.L., Robinson L.K., Braddock S.R., Xu R., Jimenez J.L., et al. Pregnancy outcome in women exposed to leflunomide before or during pregnancy. Arthritis Rheum 2012, 64:2085-2094.
94. Zandman-Goddard G., Levy Y., Shoenfeld Y. Intravenous immunoglobulin therapy and systemic lupus erythematosus. Clin Rev Allergy Immunol 2005, 29:219-228.
95. Micheloud D., Nuno L., Rodriguez-Mahou M., Sanchez-Ramon S., Ortega M.C., Aguaron A., et al. Efficacy and safety of etanercept, high-dose intravenous gammaglobulin and plasmapheresis combined therapy for lupus diffuse proliferative nephritis complicating pregnancy. Lupus 2006, 15:881-885.
96. Sangle S.R., Lutalo P.M., Davies R.J., Khamashta M.A., D'Cruz D.P. B-cell depletion therapy and pregnancy outcome in severe, refractory systemic autoimmune diseases. J Autoimmun 2013, 43:55-59.
97. Ginzler E.M., Wallace D.J., Merrill J.T., Furie R.A., Stohl W., Chatham W.W., et al. Disease control and safety of belimumab plus standard therapy over 7 years in patients with systemic lupus erythematosus. J Rheumatol 2014, 41:300-309.
98. Danve A., Perry L., Deodhar A. Use of belimumab throughout pregnancy to treat active systemic lupus erythematosus-a case report. Semin Arthritis Rheum 2014, 44:195-197.