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Renal Manifestations in Lupus Pregnancy

  • Nina KelloEmail author
  • Jeanie Lee
  • Donandre Jackson
  • Galina Marder
  • Sonali Narain
Chapter

Abstract

The management of pregnancy in patients with SLE, lupus nephritis, and APS is complex and should start well before conception by evaluating maternal and fetal risks and medication adjustment. Interdisciplinary collaboration between the rheumatologist, nephrologist, and high-risk obstetrician is very important, and a careful treatment plan has to be drafted with close monitoring by involved specialties throughout the course of pregnancy.

Keywords

Renal manifestations in lupus pregnancy Pregnancy and lupus Pregnancy and renal manifestations of lupus Lupus pregnancy Pregnancy and renal manifestations Antiphospholipid syndrome in pregnant women Lupus nephritis in pregnancy 

References

  1. 1.
    Clark CA, Spitzer KA, Laskin CA. Decrease in pregnancy loss rates in patients with systemic lupus erythematosus over a 40-year period. J Rheumatol. 2005;32(9):1709–12.PubMedPubMedCentralGoogle Scholar
  2. 2.
    Clowse ME, Magder LS, Petri M. The clinical utility of measuring complement and anti-dsDNA antibodies during pregnancy in patients with systemic lupus erythematosus. J Rheumatol. 2011;38(6):1012–6.PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Buyon JP, Kim MY, Guerra MM, Laskin CA, Petri M, Lockshin MD, et al. Predictors of pregnancy outcomes in patients with lupus: a cohort study. Ann Intern Med. 2015;163(3):153–63.PubMedPubMedCentralCrossRefGoogle Scholar
  4. 4.
    Lockshin MD, Kim M, Laskin CA, Guerra M, Branch DW, 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. 2012;64(7):2311–8.PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Yan Yuen S, Krizova A, Ouimet JM, Pope JE. Pregnancy outcome in systemic lupus erythematosus (SLE) is improving: results from a case control study and literature review. Open Rheumatol J. 2008;2:89–98.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Clowse ME, Magder LS, Witter F, Petri M. The impact of increased lupus activity on obstetric outcomes. Arthritis Rheum. 2005;52(2):514–21.PubMedCrossRefPubMedCentralGoogle Scholar
  7. 7.
    Gregory EC, MacDorman MF, Martin JA. Trends in fetal and perinatal mortality in the United States, 2006–2012. NCHS Data Brief. 2014;(169):1–8.Google Scholar
  8. 8.
    Arkema EV, Palmsten K, Sjöwall C, Svenungsson E, Salmon JE, Simard JF. 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;68(7):988–94.CrossRefGoogle Scholar
  9. 9.
    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. 1986;13(4):732–9.PubMedGoogle Scholar
  10. 10.
    Yang H, Liu H, Xu D, Zhao L, Wang Q, Leng X, et al. Pregnancy-related systemic lupus erythematosus: clinical features, outcome and risk factors of disease flares – a case control study. PLoS One. 2014;9(8):e104375.PubMedPubMedCentralCrossRefGoogle Scholar
  11. 11.
    Chakravarty EF, Colon I, Langen ES, Nix DA, El-Sayed YY, Genovese MC, et al. Factors that predict prematurity and preeclampsia in pregnancies that are complicated by systemic lupus erythematosus. Am J Obstet Gynecol. 2005;192(6):1897–904.PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Moroni G, Ponticelli C. Pregnancy after lupus nephritis. Lupus. 2005;14(1):89–94.PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Clowse ME. Lupus activity in pregnancy. Rheum Dis Clin N Am. 2007;33(2):237–52.. vCrossRefGoogle Scholar
  14. 14.
    Ko HS, Ahn HY, Jang DG, Choi SK, Park YG, Park IY, et al. Pregnancy outcomes and appropriate timing of pregnancy in 183 pregnancies in Korean patients with SLE. Int J Med Sci. 2011;8(7):577–83.PubMedPubMedCentralCrossRefGoogle Scholar
  15. 15.
    Moroni G, Doria A, Giglio E, Tani C, Zen M, Strigini F, et al. Fetal outcome and recommendations of pregnancies in lupus nephritis in the 21st century. A prospective multicenter study. J Autoimmun. 2016;74:6–12.PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Doria A, Iaccarino L, Sarzi-Puttini P, Ghirardello A, Zampieri S, Arienti S, et al. Estrogens in pregnancy and systemic lupus erythematosus. Ann N Y Acad Sci. 2006;1069:247–56.PubMedCrossRefPubMedCentralGoogle Scholar
  17. 17.
    Doria A, Iaccarino L, Arienti S, Ghirardello A, Zampieri S, Rampudda ME, et al. Th2 immune deviation induced by pregnancy: the two faces of autoimmune rheumatic diseases. Reprod Toxicol. 2006;22(2):234–41.PubMedCrossRefPubMedCentralGoogle Scholar
  18. 18.
    Cutolo M, Sulli A, Capellino S, Villaggio B, Montagna P, Seriolo B, et al. Sex hormones influence on the immune system: basic and clinical aspects in autoimmunity. Lupus. 2004;13(9):635–8.PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    de Jesus GR, Mendoza-Pinto C, de Jesus NR, Dos Santos FC, Klumb EM, Carrasco MG, et al. Understanding and managing pregnancy in patients with lupus. Autoimmune Dis. 2015;2015:943490.PubMedPubMedCentralGoogle Scholar
  20. 20.
    Kim MY, Buyon JP, Guerra MM, Rana S, Zhang D, Laskin CA, et al. Angiogenic factor imbalance early in pregnancy predicts adverse outcomes in patients with lupus and antiphospholipid antibodies: results of the PROMISSE study. Am J Obstet Gynecol. 2016;214(1):108 e1–e14.CrossRefGoogle Scholar
  21. 21.
    Leaños-Miranda A, et al. Circulating angiogenic factors and the risk of preeclampsia in systemic lupus erythematosus pregnancies. J Rheumatol. 2015;42(7):1141–9.PubMedCrossRefPubMedCentralGoogle Scholar
  22. 22.
    Miyakis S, Lockshin MD, Atsumi T, Branch DW, Brey RL, Cervera R, 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.PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Chighizola CB, Gerosa M, Trespidi L, Di Giacomo A, Rossi F, Acaia B, et al. Update on the current recommendations and outcomes in pregnant women with antiphospholipid syndrome. Expert Rev Clin Immunol. 2014;10(11):1505–17.PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Meroni PL, Borghi MO, Raschi E, Tedesco F. Pathogenesis of antiphospholipid syndrome: understanding the antibodies. Nat Rev Rheumatol. 2011;7(6):330–9.PubMedCrossRefPubMedCentralGoogle Scholar
  25. 25.
    Salmon JE, Girardi G, Lockshin MD. The antiphospholipid syndrome as a disorder initiated by inflammation: implications for the therapy of pregnant patients. Nat Clin Pract Rheumatol. 2007;3(3):140–7; quiz 1 p following 87.PubMedCrossRefPubMedCentralGoogle Scholar
  26. 26.
    Bertolaccini ML, Sanna G. Recent advances in understanding antiphospholipid syndrome. F1000Res. 2016;5:2908.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Proulle V, Furie RA, Merrill-Skoloff G, Furie BC, Furie B. Platelets are required for enhanced activation of the endothelium and fibrinogen in a mouse thrombosis model of APS. Blood. 2014;124(4):611–22.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    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. 2014;60(2–3):170–6.PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Saavedra MA. Impact of previous lupus nephritis on maternal and fetal outcomes during pregnancy. Clin Rheumatol. 2012;31(5 SRC - GoogleScholar):813–9.PubMedCrossRefPubMedCentralGoogle Scholar
  30. 30.
    Smyth A, Oliveira GH, Lahr BD, Bailey KR, Norby SM, Garovic VD. 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):2060–8.PubMedPubMedCentralCrossRefGoogle Scholar
  31. 31.
    Bramham K, Hunt BJ, Bewley S, Germain S, Calatayud I, Khamashta MA, et al. Pregnancy outcomes in systemic lupus erythematosus with and without previous nephritis. J Rheumatol. 2011;38(9):1906–13.PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    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. 2016;74:194–200.PubMedCrossRefPubMedCentralGoogle Scholar
  33. 33.
    Wagner SJ, Craici I, Reed D, Norby S, Bailey K, Wiste HJ, et al. Maternal and foetal outcomes in pregnant patients with active lupus nephritis. Lupus. 2009;18(4):342–7.PubMedPubMedCentralCrossRefGoogle Scholar
  34. 34.
    Smyth A, et al. A systematic review and meta-analysis of pregnancy outcomes in patients with systemic lupus erythematosus and lupus nephritis. Clin Soc Nephrol p. 2010;5(11 SRC – GoogleScholar):2060–8.CrossRefGoogle Scholar
  35. 35.
    Moroni G. Fetal outcome and recommendations of pregnancies in lupus nephritis in the 21st century. A prospective multicenter study. 2016;74SRC – GoogleScholar:6–12.Google Scholar
  36. 36.
    Andrade R, Sanchez ML, Alarcon GS, Fessler BJ, Fernandez M, Bertoli AM, et al. Adverse pregnancy outcomes in women with systemic lupus erythematosus from a multiethnic US cohort: LUMINA (LVI) [corrected]. Clin Exp Rheumatol. 2008;26(2):268–74.PubMedPubMedCentralGoogle Scholar
  37. 37.
    Moroni G, Ponticelli C. The risk of pregnancy in patients with lupus nephritis. J Nephrol. 2003;16(2):161–7.PubMedPubMedCentralGoogle Scholar
  38. 38.
    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(4):182–8.PubMedCrossRefPubMedCentralGoogle Scholar
  39. 39.
    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(5):534–41.PubMedCrossRefPubMedCentralGoogle Scholar
  40. 40.
    Cervera R, Piette JC, Font J, Khamashta MA, Shoenfeld Y, Camps MT, et al. Antiphospholipid syndrome: clinical and immunologic manifestations and patterns of disease expression in a cohort of 1,000 patients. Arthritis Rheum. 2002;46(4):1019–27.PubMedCrossRefPubMedCentralGoogle Scholar
  41. 41.
    Opatrny L, David M, Kahn SR, Shrier I, Rey E. Association between antiphospholipid antibodies and recurrent fetal loss in women without autoimmune disease: a metaanalysis. J Rheumatol. 2006;33(11):2214–21.PubMedPubMedCentralGoogle Scholar
  42. 42.
    Sinico RA, Cavazzana I, Nuzzo M, Vianelli M, Napodano P, Scaini P, et al. Renal involvement in primary antiphospholipid syndrome: retrospective analysis of 160 patients. Clin J Am Soc Nephrol. 2010;5(7):1211–7.PubMedPubMedCentralCrossRefGoogle Scholar
  43. 43.
    Nochy D, Daugas E, Droz D, Beaufils H, Grunfeld JP, Piette JC, et al. The intrarenal vascular lesions associated with primary antiphospholipid syndrome. J Am Soc Nephrol. 1999;10(3):507–18.PubMedPubMedCentralGoogle Scholar
  44. 44.
    Tektonidou MG. Renal involvement in the antiphospholipid syndrome (APS)-APS nephropathy. Clin Rev Allergy Immunol. 2009;36(2–3):131–40.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Fakhouri F. Pregnancy-related thrombotic microangiopathies: clues from complement biology. Transfus Apher Sci. 2016;54(2):199–202.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    George JN, Nester CM, McIntosh JJ. Syndromes of thrombotic microangiopathy associated with pregnancy. Hematology Am Soc Hematol Educ Program. 2015;2015:644–8.PubMedCrossRefPubMedCentralGoogle Scholar
  47. 47.
    Thomas MR, Robinson S, Scully MA. How we manage thrombotic microangiopathies in pregnancy. Br J Haematol. 2016;173(6):821–30.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Abalos E, Cuesta C, Grosso AL, Chou D, Say L. Global and regional estimates of preeclampsia and eclampsia: a systematic review. Eur J Obstet Gynecol Reprod Biol. 2013;170(1):1–7.PubMedCrossRefGoogle Scholar
  49. 49.
    Ananth CV, Keyes KM, Wapner RJ. Pre-eclampsia rates in the United States, 1980–2010: age-period-cohort analysis. BMJ. 2013;347:f6564.PubMedPubMedCentralCrossRefGoogle Scholar
  50. 50.
    Marchetti T, de Moerloose P, Gris JC. Antiphospholipid antibodies and the risk of severe and non-severe pre-eclampsia: the NOHA case-control study. J Thromb Haemost. 2016;14(4):675–84.PubMedCrossRefPubMedCentralGoogle Scholar
  51. 51.
    Yelnik CM, Laskin CA, Porter TF, Branch DW, Buyon JP, Guerra MM, 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.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    do Prado AD, Piovesan DM, Staub HL, Horta BL. Association of anticardiolipin antibodies with preeclampsia. Obstet Gynecol. 2010;116(6):1433–43.PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Cnossen JS, Morris RK, ter Riet G, Mol BW, van der Post JA, 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(6):701–11.PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Tedeschi SK, Guan H, Fine A, Costenbader KH, Bermas B. Organ-specific systemic lupus erythematosus activity during pregnancy is associated with adverse pregnancy outcomes. Clin Rheumatol. 2016;35(7):1725–32.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Yee CS, Akil M, Khamashta M, Bessant R, Kilding R, Giles I, et al. The BILAG2004-Pregnancy index is reliable for assessment of disease activity in pregnant SLE patients. Rheumatology (Oxford). 2012;51(10):1877–80.CrossRefGoogle Scholar
  56. 56.
    Clowse ME, Wallace DJ, Weisman M, James A, Criscione-Schreiber LG, Pisetsky DS. Predictors of preterm birth in patients with mild systemic lupus erythematosus. Ann Rheum Dis. 2013;72(9):1536–9.PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Ruiz-Irastorza G, Khamashta MA, Gordon C, Lockshin MD, Johns KR, Sammaritano L, et al. Measuring systemic lupus erythematosus activity during pregnancy: validation of the lupus activity index in pregnancy scale. Arthritis Rheum. 2004;51(1):78–82.PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    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(6):643–50.CrossRefGoogle Scholar
  59. 59.
    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(2):519–25.PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Shibata S, Sasaki T, Hirabayashi Y, Seino J, Okamura K, Yoshinaga K, et al. Risk factors in the pregnancy of patients with systemic lupus erythematosus: association of hypocomplementaemia with poor prognosis. Ann Rheum Dis. 1992;51(5):619–23.PubMedPubMedCentralCrossRefGoogle Scholar
  61. 61.
    Moroni G, Quaglini S, Banfi G, Caloni M, Finazzi S, Ambroso G, et al. Pregnancy in lupus nephritis. Am J Kidney Dis. 2002;40(4):713–20.PubMedCrossRefPubMedCentralGoogle Scholar
  62. 62.
    Clowse ME, Magder LS, Witter F, Petri M. Early risk factors for pregnancy loss in lupus. Obstet Gynecol. 2006;107(2 Pt 1):293–9.PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Andreoli L, Bertsias GK, Agmon-Levin N, Brown S, Cervera R, Costedoat-Chalumeau 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):476–85.PubMedPubMedCentralCrossRefGoogle Scholar
  64. 64.
    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(6):1070–6.CrossRefGoogle Scholar
  65. 65.
    Gordon C. Pregnancy and autoimmune diseases. Best Pract Res Clin Rheumatol. 2004;18(3):359–79.PubMedCrossRefPubMedCentralGoogle Scholar
  66. 66.
    Espinosa G, Cervera R. Current treatment of antiphospholipid syndrome: lights and shadows. Nat Rev Rheumatol. 2015;11(10):586–96.PubMedCrossRefPubMedCentralGoogle Scholar
  67. 67.
    Hahn BH, McMahon MA, Wilkinson A, Wallace WD, Daikh DI, Fitzgerald JD, et al. American College of Rheumatology guidelines for screening, treatment, and management of lupus nephritis. Arthritis Care Res (Hoboken). 2012;64(6):797–808.CrossRefGoogle Scholar
  68. 68.
    Clowse ME, Magder L, Witter F, Petri M. Hydroxychloroquine in lupus pregnancy. Arthritis Rheum. 2006;54(11):3640–7.PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Izmirly PM, Costedoat-Chalumeau N, Pisoni CN, Khamashta MA, Kim MY, 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. 2012;126(1):76–82.PubMedPubMedCentralCrossRefGoogle Scholar
  70. 70.
    Doria A, Tincani A, Lockshin M. Challenges of lupus pregnancies. Rheumatology (Oxford). 2008;47(Suppl 3):iii9–12.Google Scholar
  71. 71.
    Armenti VT, Daller JA, Constantinescu S, Silva P, Radomski JS, Moritz MJ, et al. Report from the National Transplantation Pregnancy Registry: outcomes of pregnancy after transplantation. Clin Transpl. 2006;20:57–70.Google Scholar
  72. 72.
    Bar Oz B, Hackman R, Einarson T, Koren G. Pregnancy outcome after cyclosporine therapy during pregnancy: a meta-analysis. Transplantation. 2001;71(8):1051–5.PubMedCrossRefPubMedCentralGoogle Scholar
  73. 73.
    Paziana K, Del Monaco M, Cardonick E, Moritz M, Keller M, Smith B, et al. Ciclosporin use during pregnancy. Drug Saf. 2013;36(5):279–94.PubMedCrossRefPubMedCentralGoogle Scholar
  74. 74.
    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(11):1192–6.PubMedCrossRefPubMedCentralGoogle Scholar
  75. 75.
    Sifontis NM, Coscia LA, Constantinescu S, Lavelanet AF, Moritz MJ, Armenti VT. Pregnancy outcomes in solid organ transplant recipients with exposure to mycophenolate mofetil or sirolimus. Transplantation. 2006;82(12):1698–702.PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Clowse ME, Magder L, Petri M. Cyclophosphamide for lupus during pregnancy. Lupus. 2005;14(8):593–7.PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Kart Köseoglu H, Yücel AE, Künefeci G, Ozdemir FN, Duran H. Cyclophosphamide therapy in a serious case of lupus nephritis during pregnancy. Lupus. 2001;10(11):818–20.PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Perricone R, De Carolis C, Kröegler B, Greco E, Giacomelli R, Cipriani P, et al. Intravenous immunoglobulin therapy in pregnant patients affected with systemic lupus erythematosus and recurrent spontaneous abortion. Rheumatology (Oxford). 2008;47(5):646–51.CrossRefGoogle Scholar
  79. 79.
    Bates SM, Greer IA, Middeldorp S, Veenstra DL, Prabulos AM, Vandvik PO, et al. VTE, thrombophilia, antithrombotic therapy, and pregnancy: Antithrombotic Therapy and Prevention of Thrombosis, 9th ed: American College of Chest Physicians Evidence-Based Clinical Practice Guidelines. Chest. 2012;141(2 Suppl):e691S–736S.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Erkan D, Yazici Y, Peterson MG, Sammaritano L, Lockshin MD. A cross-sectional study of clinical thrombotic risk factors and preventive treatments in antiphospholipid syndrome. Rheumatology (Oxford). 2002;41(8):924–9.CrossRefGoogle Scholar
  81. 81.
    Petri M. Detection of coronary artery disease and the role of traditional risk factors in the Hopkins Lupus Cohort. Lupus. 2000;9(3):170–5.PubMedCrossRefPubMedCentralGoogle Scholar
  82. 82.
    Legendre CM, Licht C, Muus P, Greenbaum LA, Babu S, Bedrosian C, et al. Terminal complement inhibitor eculizumab in atypical hemolytic-uremic syndrome. N Engl J Med. 2013;368(23):2169–81.PubMedCrossRefPubMedCentralGoogle Scholar
  83. 83.
    Licht C, Greenbaum LA, Muus P, Babu S, Bedrosian CL, Cohen DJ, et al. Efficacy and safety of eculizumab in atypical hemolytic uremic syndrome from 2-year extensions of phase 2 studies. Kidney Int. 2015;87(5):1061–73.PubMedPubMedCentralCrossRefGoogle Scholar
  84. 84.
    Zuber J, Le Quintrec M, Krid S, Bertoye C, Gueutin V, Lahoche A, et al. Eculizumab for atypical hemolytic uremic syndrome recurrence in renal transplantation. Am J Transplant. 2012;12(12):3337–54.PubMedCrossRefPubMedCentralGoogle Scholar
  85. 85.
    Zuber J, Fakhouri F, Roumenina LT, Loirat C, Frémeaux-Bacchi V, aHUS/C3G FSGf. Use of eculizumab for atypical haemolytic uraemic syndrome and C3 glomerulopathies. Nat Rev Nephrol. 2012;8(11):643–57.CrossRefGoogle Scholar
  86. 86.
    Kello N, El Khoury L, Marder G, Furie R, Zapantis E, Horowitz DL. Secondary thrombotic microangiopathy in systemic lupus erythematosus and antiphospholipid syndrome, the role of complement and use of eculizumab: case series and review of literature. In Seminars in arthritis and rheumatism: WB Saunders; 2018.Google Scholar
  87. 87.
    Sarno L, Tufano A, Maruotti GM, et al. J Nephrol. 2019;32:17.  https://doi.org/10.1007/s40620-018-0517-z.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Bagon JA, Vernaeve H, De Muylder X, Lafontaine JJ, Martens J, Van Roost G. Pregnancy and dialysis. Am J Kidney Dis. 1998;31(5):756–65.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Mattos P, Santiago MB. Disease activity in systemic lupus erythematosus patients with end-stage renal disease: systematic review of the literature. Clin Rheumatol. 2012;31(6):897–905.PubMedCrossRefPubMedCentralGoogle Scholar
  90. 90.
    Campise M. Pregnancies in women receiving renal transplant for lupus nephritis: description of nine pregnancies and review of the literature. Lupus. 2015;24. SRC – GoogleScholar:1210–3.PubMedCrossRefPubMedCentralGoogle Scholar
  91. 91.
    Group KDIGOKTW. KDIGO clinical practice guideline for the care of kidney transplant recipients. Am J Transplant. 2009;9(Suppl 3):S1–155.Google Scholar
  92. 92.
    Lateef A, Petri M. Managing lupus patients during pregnancy. Best Pract Res Clin Rheumatol. 2013;27(3):435–47.PubMedCrossRefPubMedCentralGoogle Scholar
  93. 93.
    Campise M. Pregnancies in women receiving renal transplant for lupus nephritis: description of nine pregnancies and review of the literature. Lupus. 2015;24:1210–3.PubMedCrossRefPubMedCentralGoogle Scholar
  94. 94.
    McGrory CH. Pregnancy outcomes in female renal recipients: a comparison of systemic lupus erythematosus with other diagnoses. Am J Transplant. 2003;3:35–42.PubMedCrossRefPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2020

Authors and Affiliations

  • Nina Kello
    • 1
    Email author
  • Jeanie Lee
    • 2
  • Donandre Jackson
    • 3
  • Galina Marder
    • 4
  • Sonali Narain
    • 4
  1. 1.Division of RheumatologyDonald and Barbara Zucker School of Medicine at Hofstra/NorthwellGreat NeckUSA
  2. 2.Department of Internal MedicineDonald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell HealthGreat NeckUSA
  3. 3.Donald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell HealthGreat NeckUSA
  4. 4.Division of RheumatologyDonald and Barbara Zucker School of Medicine at Hofstra/Northwell, Northwell HealthGreat NeckUSA

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