Predictors of SLE relapse in pregnancy and post-partum among multi-ethnic patients in Malaysia


Autoři: Syahrul Sazliyana Shaharir aff001;  Mohd Shahrir Mohamed Said aff001;  Rozita Mohd aff002;  Rizna Abdul Cader aff002;  Ruslinda Mustafar aff002;  Rahana Abdul Rahman aff003
Působiště autorů: Rheumatology Unit, Department of Internal Medicine, Universiti Kebangsaan Malaysia Medical Centre (UKMMC), Jalan Yaacob Latiff, Kuala Lumpur, Malaysia aff001;  Nephrology Unit, Department of Internal Medicine, Universiti Kebangsaan Malaysia Medical Centre (UKMMC), Jalan Yaacob Latiff, Kuala Lumpur, Malaysia aff002;  Department of Obstetrics and Gynaecology, Universiti Kebangsaan Malaysia Medical Centre (UKMMC), Jalan Yaacob Latiff, Kuala Lumpur, Malaysia aff003
Vyšlo v časopise: PLoS ONE 14(9)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0222343

Souhrn

Flare of Systemic Lupus Erythematosus (SLE) may occur during pregnancy and puerperium. We studied the prevalence and factors associated with SLE relapse during pregnancy and post-partum period in a multi-ethnic SLE cohort. Consecutive SLE patients who attended the outpatient clinic were reviewed for previous history of pregnancies in our institution. Patients who had a complete antenatal, delivery, and post-partum follow up were included. Their medical records were retrospectively analysed to assess the disease activity at pre-pregnancy/conception, during antenatal, and post-partum period. Presence of flare episodes during pregnancy and puerperium were recorded. The pregnancy outcomes recorded include live birth, foetal loss, prematurity and intra-uterine growth restrictions (IUGR). Univariate and multivariable logistic regression with generalized estimating equations (GEE) analyses were performed to determine the factors associated with disease relapse and the pregnancy outcomes. A total of 120 patients with 196 pregnancies were included, with a live birth rate of 78.6%. Four (2.0%) were diagnosed to have SLE during pregnancy. The flare rate in pregnancy was 40.1% while post-partum 17.4%. Majority of the relapse in pregnancy occurred in haematological system (62.3%) followed by renal (53.2%), musculoskeletal (22.1%), and mucocutaneous (14.3%). In GEE analyses, active disease at conception was the independent predictor of SLE relapse during and after pregnancy, whereas older maternal age and Malay ethnicity were associated with higher flare during post-partum. HCQ use was significantly associated with reduced risk of flare in univariate analysis but it was no longer significant in the GEE analyses. Presence of disease flare in pregnancy was significantly associated with prematurity. In conclusion, pregnancy in SLE need to be planned during quiescent state as pre-pregnant active disease was associated with disease relapse in both during and after pregnancy. Malay patients had an increased risk of post-partum flare but further larger prospective studies are needed to confirm the association between pregnancies in the different ancestral background.

Klíčová slova:

Medicine and health sciences – Clinical medicine – Clinical immunology – Autoimmune diseases – Lupus erythematosus – Systemic lupus erythematosus – Immunology – Rheumatology – Women's health – Maternal health – Pregnancy – Pregnancy complications – Miscarriage – Obstetrics and gynecology – Hematology – Diagnostic medicine – Signs and symptoms – Proteinuria – Pathology and laboratory medicine – Biology and life sciences – Lupus nephritis – People and places – Population groupings – Ethnicities – Malay people – Chinese people


Zdroje

1. Uramoto KM, Michet CJ Jr, Thumboo J, Sunku J, O'Fallon WM, Gabriel SE. Trends in the incidence and mortality of systemic lupus erythematosus, 1950–1992. Arthritis Rheum. 1999;42(1):46–50. Epub 1999/01/27. doi: 10.1002/1529-0131(199901)42:1<46::AID-ANR6>3.0.CO;2-2 9920013.

2. Tsokos GC. Systemic lupus erythematosus. N Engl J Med. 2011;365(22):2110–21. Epub 2011/12/02. doi: 10.1056/NEJMra1100359 22129255.

3. Manson JJ, Rahman A. Systemic lupus erythematosus. Orphanet journal of rare diseases. 2006;1:6–. doi: 10.1186/1750-1172-1-6 16722594.

4. Østensen M. New insights into sexual functioning and fertility in rheumatic diseases. Best Practice & Research Clinical Rheumatology. 2004;18(2):219–32. https://doi.org/10.1016/j.berh.2004.01.002.

5. Cervera R, Font J, Carmona F, Balasch J. Pregnancy outcome in systemic lupus erythematosus: good news for the new millennium. Autoimmun Rev. 2002;1(6):354–9. Epub 2003/07/10. 12848991.

6. Wong KL, Chan FY, Lee CP. Outcome of pregnancy in patients with systemic lupus erythematosus. A prospective study. Arch Intern Med. 1991;151(2):269–73. Epub 1991/02/01. 1992954.

7. Petri M, Howard D, Repke J. Frequency of lupus flare in pregnancy. The Hopkins Lupus Pregnancy Center experience. Arthritis Rheum. 1991;34(12):1538–45. Epub 1991/12/01. doi: 10.1002/art.1780341210 1670196.

8. Ruiz-Irastorza G, Lima F, Alves J, Khamashta MA, Simpson J, Hughes GR, et al. Increased rate of lupus flare during pregnancy and the puerperium: a prospective study of 78 pregnancies. Br J Rheumatol. 1996;35(2):133–8. Epub 1996/02/01. doi: 10.1093/rheumatology/35.2.133 8612024.

9. Clowse ME, Magder LS, Witter F, Petri M. The impact of increased lupus activity on obstetric outcomes. Arthritis Rheum. 2005;52(2):514–21. Epub 2005/02/05. doi: 10.1002/art.20864 15692988.

10. Nossent HC, Swaak TJ. Systemic lupus erythematosus. VI. Analysis of the interrelationship with pregnancy. J Rheumatol. 1990;17(6):771–6. Epub 1990/06/01. 2388198.

11. Tincani A, Faden D, Tarantini M, Lojacono A, Tanzi P, Gastaldi A, et al. Systemic lupus erythematosus and pregnancy: a prospective study. Clin Exp Rheumatol. 1992;10(5):439–46. Epub 1992/09/01. 1458696.

12. Lockshin MD. Pregnancy does not cause systemic lupus erythematosus to worsen. Arthritis Rheum. 1989;32(6):665–70. Epub 1989/06/01. doi: 10.1002/anr.1780320602 2638570.

13. Georgiou PE, Politi EN, Katsimbri P, Sakka V, Drosos AA. Outcome of lupus pregnancy: a controlled study. Rheumatology (Oxford). 2000;39(9):1014–9. Epub 2000/09/15. doi: 10.1093/rheumatology/39.9.1014 10986308.

14. Lima F, Buchanan NM, Khamashta MA, Kerslake S, Hughes GR. Obstetric outcome in systemic lupus erythematosus. Semin Arthritis Rheum. 1995;25(3):184–92. Epub 1995/12/01. 8650588.

15. Carmona F, Font J, Cervera R, Munoz F, Cararach V, Balasch J. Obstetrical outcome of pregnancy in patients with systemic Lupus erythematosus. A study of 60 cases. Eur J Obstet Gynecol Reprod Biol. 1999;83(2):137–42. Epub 1999/07/03. doi: 10.1016/s0301-2115(98)00312-1 10391522.

16. 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. Epub 1986/08/01. 3772921.

17. Baer AN, Witter FR, Petri M. Lupus and pregnancy. Obstet Gynecol Surv. 2011;66(10):639–53. Epub 2011/11/25. doi: 10.1097/OGX.0b013e318239e1ee 22112525.

18. Andrade RM, McGwin G Jr., Alarcon GS, Sanchez ML, Bertoli AM, Fernandez M, et al. Predictors of post-partum damage accrual in systemic lupus erythematosus: data from LUMINA, a multiethnic US cohort (XXXVIII). Rheumatology (Oxford). 2006;45(11):1380–4. Epub 2006/08/02. doi: 10.1093/rheumatology/kel222 16880189.

19. 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 Care Res (Hoboken). 2004;51(1):78–82. doi: 10.1002/art.20081 14872459

20. Buyon JP, Kalunian KC, Ramsey-Goldman R, Petri MA, Lockshin MD, Ruiz-Irastorza G, et al. Assessing disease activity in SLE patients during pregnancy. Lupus. 1999;8(8):677–84. Epub 1999/11/24. doi: 10.1191/096120399680411272 10568906.

21. Lateef A, Petri M. Managing lupus patients during pregnancy. Best Pract Res Clin Rheumatol. 2013;27(3):435–47. Epub 2013/11/19. doi: 10.1016/j.berh.2013.07.005 24238698; PubMed Central PMCID: PMC3834352.

22. Carvalheiras G, Vita P, Marta S, Trovão R, Farinha F, Braga J, et al. Pregnancy and Systemic Lupus Erythematosus: Review of Clinical Features and Outcome of 51 Pregnancies at a Single Institution. Clin Rev Allergy Immunol. 2010;38(2):302–6. doi: 10.1007/s12016-009-8161-y 19603147

23. Shaharir SS, Hussein H, Rajalingham S, Mohamed Said MS, Abdul Gafor AH, Mohd R, et al. Damage in the Multiethnic Malaysian Systemic Lupus Erythematosus (SLE) Cohort: Comparison with Other Cohorts Worldwide. PLoS One. 2016;11(11):e0166270. doi: 10.1371/journal.pone.0166270 27846298

24. Yap DYH, Chan TM. Lupus Nephritis in Asia: Clinical Features and Management. Kidney diseases (Basel, Switzerland). 2015;1(2):100–9. Epub 2015/08/05. doi: 10.1159/000430458 27536670.

25. Chen D, Lao M, Zhang J, Zhan Y, Li W, Cai X, et al. Fetal and Maternal Outcomes of Planned Pregnancy in Patients with Systemic Lupus Erythematosus: A Retrospective Multicenter Study. J Immunol Res. 2018;2018:7. doi: 10.1155/2018/2413637 30255104

26. Zhan Z, Yang Y, Zhan Y, Chen D, Liang L, Yang X. Fetal outcomes and associated factors of adverse outcomes of pregnancy in southern Chinese women with systemic lupus erythematosus. PLoS One. 2017;12(4):e0176457–e. doi: 10.1371/journal.pone.0176457 28441446.

27. Ku M, Guo S, Shang W, Li Q, Zeng R, Han M, et al. Pregnancy Outcomes in Chinese Patients with Systemic Lupus Erythematosus (SLE): A Retrospective Study of 109 Pregnancies. PLoS One. 2016;11(7):e0159364. Epub 2016/07/22. doi: 10.1371/journal.pone.0159364 27442513; PubMed Central PMCID: PMC4956200.

28. Wu J, Ma J, Bao C, Di W, Zhang W-H. Pregnancy outcomes among Chinese women with and without systemic lupus erythematosus: a retrospective cohort study. BMJ Open. 2018;8(4):e020909. doi: 10.1136/bmjopen-2017-020909 29654043

29. Yang MJ, Chen CY, Chang WH, Tseng JY, Yeh CC. Pregnancy outcome of systemic lupus erythematosus in relation to lupus activity before and during pregnancy. J Chin Med Assoc. 2015;78(4):235–40. Epub 2015/03/10. doi: 10.1016/j.jcma.2014.11.008 25747013.

30. 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. Epub 2014/08/15. doi: 10.1371/journal.pone.0104375 25118692; PubMed Central PMCID: PMC4131906.

31. Ko HS, Ahn HY, Jang DG, Choi S-K, Park Y-G, Park IY, et al. Pregnancy outcomes and appropriate timing of pregnancy in 183 pregnancies in Korean patients with SLE. International journal of medical sciences. 2011;8(7):577–83. doi: 10.7150/ijms.8.577 22022210.

32. Hochberg MC. Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1997;40(9):1725. Epub 1997/10/27. doi: 10.1002/1529-0131(199709)40:9&lt;1725::AID-ART29&gt;3.0.CO;2-Y 9324032.

33. Petri M, Orbai AM, Alarcon GS, Gordon C, Merrill JT, Fortin PR, et al. Derivation and validation of the Systemic Lupus International Collaborating Clinics classification criteria for systemic lupus erythematosus. Arthritis Rheum. 2012;64(8):2677–86. Epub 2012/05/04. doi: 10.1002/art.34473 22553077; PubMed Central PMCID: PMC3409311.

34. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, et al. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. 1982;25(11):1271–7. Epub 1982/11/01. doi: 10.1002/art.1780251101 7138600.

35. 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. Epub 2006/01/20. doi: 10.1111/j.1538-7836.2006.01753.x 16420554.

36. 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. 1991;34(8):937–44. Epub 1991/08/01. doi: 10.1002/art.1780340802 1859487.

37. Medina-Quiñones CV, Ramos-Merino L, Ruiz-Sada P, Isenberg D. Analysis of Complete Remission in Systemic Lupus Erythematosus Patients Over a 32-Year Period. Arthritis Care Res (Hoboken). 2016;68(7):981–7. doi: 10.1002/acr.22774 26554745

38. Chen YE, Korbet SM, Katz RS, Schwartz MM, Lewis EJ. Value of a complete or partial remission in severe lupus nephritis. Clin J Am Soc Nephrol. 2008;3(1):46–53. Epub 2007/11/16. doi: 10.2215/CJN.03280807 18003764; PubMed Central PMCID: PMC2390978.

39. Ruperto N, Hanrahan LM, Alarcon GS, Belmont HM, Brey RL, Brunetta P, et al. International consensus for a definition of disease flare in lupus. Lupus. 2011;20(5):453–62. Epub 2010/12/15. doi: 10.1177/0961203310388445 21148601.

40. Clowse ME, Magder L, Witter F, Petri M. Hydroxychloroquine in lupus pregnancy. Arthritis Rheum. 2006;54(11):3640–7. Epub 2006/11/01. doi: 10.1002/art.22159 17075810.

41. Eudy A, Siega-Riz AM, Engel S, Franceschini N, Howard AG, Clowse M, et al. 139. Disease flares during pregnancy and postpartum in patients with systemic lupus erythematosus. Pregnancy Hypertension. 2018;13:S26–S7. https://doi.org/10.1016/j.preghy.2018.08.080.

42. 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. Epub 2011/03/17. doi: 10.3899/jrheum.100746 21406496.

43. Clowse MEB. Lupus activity in pregnancy. Rheum Dis Clin North Am. 2007;33(2):237–v. doi: 10.1016/j.rdc.2007.01.002 17499705.

44. Ateka-Barrutia O, Nelson-Piercy C. Connective tissue disease in pregnancy. Clinical Medicine. 2013;13(6):580–4. doi: 10.7861/clinmedicine.13-6-580 24298106

45. 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. Epub 2002/09/27. doi: 10.1053/ajkd.2002.35678 12324905.

46. Carvalheiras G, Vita P, Marta S, Trovao R, Farinha F, Braga J, et al. Pregnancy and systemic lupus erythematosus: review of clinical features and outcome of 51 pregnancies at a single institution. Clin Rev Allergy Immunol. 2010;38(2–3):302–6. Epub 2009/07/16. doi: 10.1007/s12016-009-8161-y 19603147.

47. 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. doi: 10.7326/M14-2235 26098843.

48. Teh CL, Wan SA, Cheong YK, Ling GR. Systemic lupus erythematosus pregnancies: ten-year data from a single centre in Malaysia. Lupus. 2017;26(2):218–23. Epub 2016/08/16. doi: 10.1177/0961203316664996 27522092.

49. De Bandt M, Palazzo E, Belmatoug N, M'Bappe P, Hayem G, Kahn MF, et al. [Outcome of pregnancies in lupus: experience at one center]. Ann Med Interne (Paris). 2000;151(2):87–92. Epub 2000/06/16. 10855360.

50. Kobayashi N, Yamada H, Kishida T, Kato EH, Ebina Y, Sakuragi N, et al. Hypocomplementemia correlates with intrauterine growth retardation in systemic lupus erythematosus. Am J Reprod Immunol. 1999;42(3):153–9. Epub 1999/10/12. 10517175.

51. Mokbel AMG A., AboElgheit S. Could women with systemic lupus erythematosus (SLE) have successful pregnancy outcomes? Prospective observational study. The Egyptian Rheumatologist. 2013;35:133–9.

52. Urowitz MB, Gladman DD, Farewell VT, Stewart J, McDonald J. Lupus and pregnancy studies. Arthritis Rheum. 1993;36(10):1392–7. Epub 1993/10/01. doi: 10.1002/art.1780361011 8216399.

53. Chakravarty EF, Colón 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. American Journal of Obstetrics & Gynecology. 2005;192(6):1897–904. doi: 10.1016/j.ajog.2005.02.063 15970846

54. Moroni G, Quaglini S, Banfi G, Caloni M, Finazzi S, Ambroso G, et al. Pregnancy in lupus nephritis. American Journal of Kidney Diseases. 2002;40(4):713–20. doi: 10.1053/ajkd.2002.35678 12324905

55. Saavedra MA, Sánchez A, Morales S, Navarro-Zarza JE, Ángeles U, Jara LJ. Primigravida is associated with flare in women with systemic lupus erythematosus. Lupus. 2015;24(2):180–5. doi: 10.1177/0961203314552116 25253570.

56. Ku M, Guo S, Shang W, Li Q, Zeng R, Han M, et al. Pregnancy Outcomes in Chinese Patients with Systemic Lupus Erythematosus (SLE): A Retrospective Study of 109 Pregnancies. PLoS One. 2016;11(7):e0159364–e. doi: 10.1371/journal.pone.0159364 27442513.

57. Hussein Aly EA, Mohamed Riyad R, Nabil Mokbel A. Pregnancy outcome in patients with systemic lupus erythematosus: A single center study in the High Risk Pregnancy unit. Middle East Fertility Society Journal. 2016;21(3):168–74. http://dx.doi.org/10.1016/j.mefs.2015.12.003.

58. Tandon A, Ibanez D, Gladman DD, Urowitz MB. The effect of pregnancy on lupus nephritis. Arthritis Rheum. 2004;50(12):3941–6. Epub 2004/12/14. doi: 10.1002/art.20638 15593212.

59. Petri M. The Hopkins Lupus Pregnancy Center: ten key issues in management. Rheum Dis Clin North Am. 2007;33(2):227–v. doi: 10.1016/j.rdc.2007.01.003 17499704.

60. Carmona F, Font J, Cervera R, Muñoz F, Cararach V, Balasch J. Obstetrical outcome of pregnancy in patients with systemic Lupus Erythematosus. A study of 60 cases. European Journal of Obstetrics and Gynecology and Reproductive Biology. 1999;83(2):137–42. doi: 10.1016/s0301-2115(98)00312-1 10391522

61. Levy RA, Vilela VS, Cataldo MJ, Ramos RC, Duarte JL, Tura BR, et al. Hydroxychloroquine (HCQ) in lupus pregnancy: double-blind and placebo-controlled study. Lupus. 2001;10(6):401–4. Epub 2001/07/04. doi: 10.1191/096120301678646137 11434574.

62. 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. Epub 2002/06/06. doi: 10.1093/rheumatology/41.6.643 12048290.

63. Mohd Yusoff Z, Amat A, Naim D, Othman S. Postnatal Care Practices among the Malays, Chinese and Indians: A Comparison. SHS Web Conf. 2018;45:05002.

64. Jamal J.A. GZA, Husain K. Medicinal plants used for postnatal care in Malay traditional medicine in the Peninsular Malaysia. Pharmacognosy Journal. 2011; 3 (24):15–24.

65. Lewis MJ, Jawad AS. The effect of ethnicity and genetic ancestry on the epidemiology, clinical features and outcome of systemic lupus erythematosus. Rheumatology (Oxford). 2017;56(suppl_1):i67–i77. Epub 2016/12/13. doi: 10.1093/rheumatology/kew399 27940583.

66. Ruiz-Irastorza G, Khamashta MA. Lupus and pregnancy: integrating clues from the bench and bedside. Eur J Clin Invest. 2011;41(6):672–8. Epub 2010/12/17. doi: 10.1111/j.1365-2362.2010.02443.x 21158850.

67. Lima F, Buchanan NMM, Khamashta MA, Kerslake S, Hughes GRV. Obstetric outcome in systemic lupus erythematosus. Semin Arthritis Rheum. 1995;25(3):184–92. https://doi.org/10.1016/S0049-0172(95)80030-1. 8650588

68. Chakravarty EF, Colón 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. doi: 10.1016/j.ajog.2005.02.063 15970846

69. 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. Epub 2015/06/23. doi: 10.7326/M14-2235 26098843.

70. Eudy AM, Siega-Riz AM, Engel SM, Franceschini N, Howard AG, Clowse MEB, et al. Effect of pregnancy on disease flares in patients with systemic lupus erythematosus. Ann Rheum Dis. 2018;77(6):855–60. doi: 10.1136/annrheumdis-2017-212535 29463519

71. Surita FGdC, Parpinelli MÂ, Yonehara E, Krupa F, Cecatti JG. Systemic lupus erythematosus and pregnancy: clinical evolution, maternal and perinatal outcomes and placental findings. Sao Paulo Medical Journal. 2007;125:91–5. 17625706

72. Wong K-L, Chan F-Y, Lee C-P. Outcome of Pregnancy in Patients With Systemic Lupus Erythematosus: A Prospective Study. Arch Intern Med. 1991;151(2):269–73. doi: 10.1001/archinte.1991.00400020043010 1992954

73. 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. Epub 2011/10/25. doi: 10.7150/ijms.8.577 22022210; PubMed Central PMCID: PMC3198253.

74. Yang M-J, Chen C-Y, Chang W-H, Tseng J-Y, Yeh C-C. Pregnancy outcome of systemic lupus erythematosus in relation to lupus activity before and during pregnancy. Journal of the Chinese Medical Association. 2015;78(4):235–40. doi: 10.1016/j.jcma.2014.11.008 25747013

75. Wu J, Ma J, Bao C, Di W, Zhang W-H. Pregnancy outcomes among Chinese women with and without systemic lupus erythematosus: a retrospective cohort study. BMJ Open. 2018;8(4):e020909–e. doi: 10.1136/bmjopen-2017-020909 29654043.

76. Chen D, Lao M, Zhang J, Zhan Y, Li W, Cai X, et al. Fetal and Maternal Outcomes of Planned Pregnancy in Patients with Systemic Lupus Erythematosus: A Retrospective Multicenter Study. Journal of Immunology Research. 2018;2018:2413637–. doi: 10.1155/2018/2413637 30255104.

77. Gilda Parastandechehr STF, Pedram Paragomi, Maassoumeh Akhlaghi and Mahmood Akbarian Can pregnancy induce relapse in systemic lupus erythematosus (SLE)? Can pregnancy induce relapse in systemic lupus erythematosus. 2016;1(1):27–32.

78. Lockshin MD, Reinitz E, Druzin ML, Murrman M, Estes D. Lupus pregnancy: Case-control prospective study demonstrating absence of lupus exacerbation during or after pregnancy. Am J Med. 1984;77(5):893–8. doi: 10.1016/0002-9343(84)90538-2 6496544

79. Meehan RT, Dorsey JK. Pregnancy among patients with systemic lupus erythematosus receiving immunosuppressive therapy. J Rheumatol. 1987;14(2):252–8. 3598995.

80. Petri M, Howard D, Repke J, Goldman DW. The Hopkins Lupus Pregnancy Center: 1987–1991 update. Am J Reprod Immunol. 1992;28(3–4):188–91. Epub 1992/10/01. 1283682.

81. Rubbert A, Pirner K, Wildt L, Kalden JR, Manger B. Pregnancy course and complications in patients with systemic lupus erythematosus. Am J Reprod Immunol. 1992;28(3–4):205–7. Epub 1992/10/01. 1285879.


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