Th2 immune deviation induced by pregnancy: The two faces of autoimmune rheumatic diseases

Reproductive Toxicology

Volumn 22, Issue 2, 2006, Pages 234-241

  Doria, Andrea ^a   Iaccarino, Luca ^a   Arienti, Silvia ^a   Ghirardello, Anna ^a   Zampieri, Sandra ^a   Rampudda, Maria Elisa ^a   Cutolo, Maurizio ^b   Tincani, Angela ^c   Todesco, Silvano ^a  

^a UNIVERSITY OF PADOVA   (Italy)

^b UNIVERSITY OF GENOA   (Italy)

^c Brescia Hospital and University   (Italy)

Author keywords

Congenital heart block; Estrogens; IL 6; Neonatal lupus; Pregnancy; Rheumatoid arthritis; SLE activity; Systemic lupus erythematosus; Th1 and Th2 cytokines

Indexed keywords

ANTIMALARIAL AGENT; AZATHIOPRINE; CHLOROQUINE; CYCLOPHOSPHAMIDE; CYCLOSPORIN A; HYDROXYCHLOROQUINE; IMMUNOGLOBULIN; IMMUNOSUPPRESSIVE AGENT; LEFLUNOMIDE; METHOTREXATE; METHYLPREDNISOLONE; ORAL CONTRACEPTIVE AGENT; PREDNISONE; SALAZOSULFAPYRIDINE; TUMOR NECROSIS FACTOR ALPHA ANTIBODY;

ARTICLE; AUTOIMMUNE DISEASE; CARDIOMYOPATHY; CONGENITAL DEAFNESS; FETUS DISEASE; GESTATION PERIOD; HEART BLOCK; HEMATOLOGIC MALIGNANCY; HUMAN; IMMUNE RESPONSE; NONHUMAN; OTOTOXICITY; PREGNANCY OUTCOME; RASH; RHEUMATIC DISEASE; SYSTEMIC LUPUS ERYTHEMATOSUS; TH1 CELL; TH2 CELL; THIRD TRIMESTER PREGNANCY;

ADRENAL CORTEX HORMONES; ANTIRHEUMATIC AGENTS; ARTHRITIS, RHEUMATOID; FEMALE; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; PREGNANCY; PREGNANCY OUTCOME; TH1 CELLS; TH2 CELLS;

EID: 33745597352     PISSN: 08906238     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.reprotox.2006.04.001     Document Type: Article

References (96)

1. Doria A, Iaccarino L, Sarzi-Puttini P, et al. Estrogens in pregnancy and systemic lupus erythematosus. Ann N Y Acad Sci, in press.
2. Munoz-Valle J.F., Vazquez-Del Mercado M., Garcia-Iglesias T., 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 131 (2003) 377-384
3. Salem M.L. Estrogen, a double-edged sword: modulation of TH1- and TH2-mediated inflammations by differential regulation of TH1/TH2 cytokine production. Curr Drug Targets Inflamm Allergy 3 (2004) 97-104
4. Greig P.C., Herbert W.N., Robinette B.L., and Teot L.A. Amniotic fluid interleukin-10 concentrations increase trough pregnancy and are elevate in patients with preterm labor associated with intrauterine infection. Am J Obstet Gynecol 173 (1995) 1223-1227
5. Branch D.W. Physiologic adaptation of pregnancy. Am J Reprod Immunol 28 (1992) 120-212
6. Kupfermine M.J., Peaceman A.M., Aderka D., et al. Soluble tumor necrosis factor receptors in maternal plasma and second-trimester amniotic fluid. Am J Obstet Gynecol 173 (1995) 900-905
7. Ramirez F., Fowell D.J., Puklavec M., Simmonds S., and Mason D. Glucocorticoids promote a Th2 cytokine response by CD4+ T cells in vitro. J Immunol 156 (1996) 2406-2412
8. Cutolo M., Sulli A., Seriolo B., Accardo S., and Masi A.T. Estrogens, the immune response and autoimmunity. Clin Exp Rheumatol 13 (1995) 217-226
9. Doria A., Cutolo M., Ghirardello A., et al. Steroid hormones and disease activity during pregnancy in systemic lupus eythematosus. Arthritis Rheum 47 (2002) 202-209
10. Doria A., Ghirardello A., Iaccarino L., et al. Pregnancy, cytokines and disease activity in systemic lupus erythematosus. Arthritis Rheum 51 (2004) 989-995
11. Østensen M., Forger F., Nelson J.L., Schumacher A., Hebisch G., and Villiger P.M. Pregnancy in patients with rheumatic disease: anti-inflammatory cytokines increase in pregnancy and decrease post partum. Ann Rheum Dis 64 (2005) 801-803
12. Doria A., Iaccarino L., Ghirardello A., et al. Pregnancy in rare autoimmune rheumatic diseases: UCTD, MCTD, myositis, systemic vasculitis and Behçet disease. Lupus 13 (2004) 690-695
13. Doria A, Iaccarino L, Ghirardello A, et al. Pregnancy in rare autoimmune rheumatic diseases: systemic sclerosis, dermato-polymyositis and vasculitides. Z Rheumatol, in press.
14. Nossent H.C., and Swaak T.J.G. Systemic lupus erythematosus. VI. Analysis of the interrelationship with pregnancy. J Rheumatol 17 (1990) 771-776
15. Fine L.G., Barnett E.V., Danovitch G.M., et al. Systemic lupus erythematosus in pregnancy. Ann Intern Med 94 (1981) 667-677
16. Ramsey Goldman R. Pregnancy in systemic lupus erythematosus. Rheum Dis Clin North Am 14 (1988) 169-185
17. Park M.C., Park Y.B., Jung S.Y., Chung I.H., Choi K.H., and Lee S.K. Risk of ovarian failure and pregnancy outcome in patients with lupus nephritis treated with intravenous cyclophosphamide pulse therapy. Lupus 13 (2004) 569-574
18. Petri M. Prospective study of systemic lupus erythematosus pregnancy. Lupus 13 (2004) 688-689
19. Mintz G., Nitz J., Gutierrez G., et al. Prospective study of pregnancy in systemic lupus erythematosus: results of a multi-disciplinary approach. J Rheumatol 13 (1986) 732-739
20. Lockshin M.D., Reinitz E., Druzin M.L., Murrman M., and Estes D. Lupus pregnancy: case-control prospective study demonstrating absence of lupus exacerbation during or after pregnancy. Am J Med 77 (1984) 893-898
21. Urowitz M.B., Gladman D.D., Farewell V.T., Stewart J., and McDonald J. Lupus and pregnancy studies. Arthritis Rheum 36 (1993) 1392-1397
22. Petri M., Howard D., and Repke J. Frequency of lupus flare in pregnancy: the Hopkins lupus pregnancy center experience. Arthritis Rheum 34 (1991) 1538-1545
23. Ruitz-Irastorza G., Lima F., Alves J., et al. Increased rate of lupus flare during pregnancy and the puerperium. Br J Rheumatol 35 (1996) 133-138
24. Wong K.L., Chan F.Y., and Lee X.P. Outcome of pregnancy in patients with systemic lupus erythematosus. A prospective study. Arch Intern Med 151 (1991) 269-273
25. Tandon A., Ibanez D., Gladman D.D., and Urowitz M.B. The effect of pregnancy on lupus nephritis. Arthritis Rheum 50 (2004) 3941-3946
26. Gimovsky M.L., and Montoro M. Systemic lupus erythematosus and other connective tissue diseases in pregnancy. Clin Obstet Gynecol 34 (1991) 35-50
27. Moroni G., and Ponticelli C. Pregnancy after lupus nephritis. Lupus 14 (2005) 89-94
28. Khamashta M.A., and Hughes G.R.V. Pregnancy in systemic lupus erythematosus. Curr Opin Rheumatol 8 (1996) 424-429
29. Molad Y., Borokowki T., Monselise A., et al. Maternal and fetal outcome of lupus pregnancy: a prospective study of 29 pregnancy. Lupus 14 (2005) 145-151
30. Cortès-Hernàndez J., Ordi-Ros J., Paredes F., Casellas M., Castillo F., and Vilardell-Tarres M. Clinical predictors of fetal and maternal outcome in systemic lupus erythematosus: a prospective study of 103 pregnancies. Rheumatology 41 (2002) 643-650
31. Soubassi L., Haidopoulos D., Sindos M., et al. Pregnancy outcome in women with pre-existing lupus nephritis. J Obstet Gynaecol 24 (2004) 630-634
32. Ruiz-Irastorza G., and Khamashta M.A. Evaluation of systemic lupus erythematosus activity durino pregnancy. Lupus 13 (2004) 679-682
33. Buyon J.P., Kalunian K.C., Ramsey-Goldman R., et al. Assessing disease activity in SLE patients during pregnancy. Lupus 8 (1999) 677-684
34. Ruiz-Irastorza G., Khamashta M.A., Gordon C., et al. Measuring systemic lupus erythematosus activity during pregnancy: validation of the lupus activity index in pregnancy scale. Arthritis Rheum 51 (2004) 78-82
35. Houssiau F.A., Lafebvre C., Vanden Berghe M., et al. Serum interleukin 10 titers in systemic lupus erythematosus reflect disease activity. Lupus 4 (1995) 393-395
36. Kovacs E.J., Messingham K.A., and Gregory M.S. Estrogens regulation of immune responses after injury. Mol Cell Endocrinol 193 (2002) 5098-5104
37. Clowse M.E., Magder L.S., Witter F., and Petri M. The impact of increased lupus activity on obstetric outcomes. Arthritis Rheum 52 (2005) 514-521
38. Kitridou R.C. The mother in systemic lupus erythematosus. In: Wallace D.J., and Hahn B.H. (Eds). Dubois' lupus erythematosus. 5th ed. (1997), Williams & Wilkins, Baltimore 967-1002
39. Packham D.K., Lam S.S., Nicholls K., et al. Lupus nephritis and pregnancy. Q J Med 83 (1992) 315-324
40. Julkunen H., Kaaja R., Palosuo T., et al. Pregnancy in lupus nephropaty. Acta Obstet Gynecol Scand 72 (1993) 258-263
41. Carmona F., Font J., Moga I., et al. Class III-IV proliferative lupus nephiritis and pregnancy: a study of 42 cases. Am J Reprod Immunol 53 (2005) 182-188
42. Nossent H.C., and Swaak T.J. Systemic lupus erythematosus. VI. Analysis of the interrelationship with pregnancy. J Rheumatol 17 (1990) 771-776
43. Petri M., and Allbritton J. Fetal outcome of lupus pregnancy: a retrospective case-control study of the Hopkins lupus cohort. J Rheumatol 20 (1993) 650-656
44. Clark C.A., Spitzer K.A., and 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
45. Clark C.A., Spitzer K.A., Nadler J.N., and Laskin C.A. Preterm deliveries in women with systemic lupus erythematosus. J Rheumatol 30 (2003) 2127-2132
46. Martinez-Rueda J.O., Arce-Salinas C.A., Kraus A., et al. Factors associated with fetal losses in severe systemic lupus erythematosus. Lupus 5 (1996) 113-119
47. Rahman F.Z., Rahman J., and Al-Suleiman S.A. Rahman MS Pregnancy outcome in lupus nephropathy. Arch Gynecol Obstet 271 (2005) 222-226
48. Chakravarty E.F., Colon I., Langen E.S., 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
49. Buyon J.P., Cronstein B.N., Morris M., et al. Serum complement values (C3 and C4) to differentiate between systemic lupus activity and pre-eclampsia. Am J Med 21 (1986) 194-200
50. Derksen R.H.W.M., Bruinse H.W., Groot P.G., et al. Pregnancy in systemic lupus erythematosus: a prospective study. Lupus 3 (1994) 149-155
51. Costedoat-Chalumenau N., Amoura Z., Lupoglazoff J.M., et al. Outcome of pregnancies in patients with anti-SSA/Ro antibodies. Arthritis Rheum 50 (2004) 3187-3194
52. Brucato A., Buyon J.P., Horsfall A.C., et al. Fourth international workshop on neonatal lupus syndromes and the Ro/SSA-La/SSB System. Clin Exp Rheumatol 17 (1999) 130-136
53. Costedoat-Chalumeau N., Georgin-Lavialle S., Amoura Z., and Piette J.C. Anti-SSA/Ro and anti-SSB/La antibody-mediated congenital heart block. Lupus 14 (2005) 660-664
54. Brucato A., Doria A., Frassi M., et al. Pregnancy outcome in 100 women with autoimmune diseases and anti-Ro/SSA antibodies: a prospective controlled study. Lupus 11 (2002) 716-721
55. Buyon J.P., Heibert R., Copel J., et al. Autoimmune-associated confùgenital heart block: demographics, mortality, mobidity and recurrence obtained from a national neonatal lupus registry. J Am Coll Cardiol 31 (1998) 1658-1666
56. Costedoat-Chalumeau N., Amoura Z., Villain E., Cohen L., and Piette J.C. Anti-SSA/Ro antibodies and the heart: more than complete congenital heart block? A review of electrocardiographic and myocardial abnormalities and of treatment options. Arthritis Res Ther 7 (2005) 69-73
57. Udink ten Cate F.E., Breur J.M., Cohen M.I., et al. Dilated cardiomyopathy in isolated congenital complete atrioventricular block: early and long-term risk in children. J Am Coll Cardiol 37 (2001) 1129-1134
58. Neiman A.R., Lee L.A., Weston W.L., et al. Cutaneous manifestations of neonatal lupus without heart block: characteristics of mothers and children enrolled in a national registry. J Pediatr 137 (2000) 674-680
59. Brooks P.M., and Needs C.J. Antirheumatic drugs in pregnancy and lactation. Baillière's Clin Rheumatol 4 (1990) 157-171
60. Østensen M. Disease specific problems related to drug therapy in pregnancy. Lupus 13 (2004) 746-750
61. Hart C.W., and Naunton R.F. The ototoxicity of chloroquine phosphate. Arch Otolaryngol 80 (1964) 407-412
62. Costedoat-Chalumenau N., Amoura Z., Huong du L.T., Lechat P., and Piette J.C. Safety of hydroxychloroquine in pregnant patients with connective tissue disease. Review of the literature. Autoimmun Rev 4 (2005) 111-115
63. Borba E.F., Turrini-Filho J.R., Kuruma K.A., et al. Chloroquine gestational use in systemic lupus erythematosus: assessing the risk of child ototoxicity by pure tone audiometry. Lupus 13 (2004) 223-227
64. Costedoat-Chalumeau N., Amoura Z., Duhaut P., et al. Safety of hydroxychloroquine in pregnant patients with connective tissue diseases: a study of one hundred thirty-three cases compared with a control group. Arthritis Rheum 48 (2003) 3207-3211
65. Plaquenil (1997), Sanofi Winthrop Pharmaceuticals, New York, NY [package insert]
66. Tincani A., Rebaioli C.B., Frassi M., et al. Pregnancy and autoimmunity: maternal treatment and maternal disease influence on pregnancy outcome. Autoimmun Rev 4 (2005) 423-428
67. Jansen N.M., and Genta M.S. The effects of Immunosoppressive and anti-inflammatory medications on fertility, pregnancy, and lactation. Arch Intern Med 160 (2000) 610-619
68. Clowse M.E., Magder L., and Petri M. Cyclophosphamide for lupus during pregnancy. Lupus 14 (2005) 593-597
69. Anon. Reduction in incidence of rheumatoid arthritis associated with oral contraceptive. Royal College of General Practoiners' oral contraceptive study. Lancet 1 (1978) 569
70. Brennan P., Bankhead C., Silman A.J., and Symmons D. Oral contraceptive and rheumatoid arthritis: results from primary care-based incident case control study. Semin Arthritis Rheum 26 (1997) 817-823
71. Silman A.J., and Hochberg M.C. Rheumatoid arthritis. In: Silman A.J., and Hochberg M.C. (Eds). Epidemiology of the rheumatic disease (2001), Oxford University Press, Oxford 31
72. Gordon C. Pregnancy and autoimmune diseases. Best Pract Res Clin Rheumatol 18 (2004) 359
73. Silman A.J. Epidemiology of rheumatoid arthritis. APMIS 102 (1994) 721-728
74. Brennan P., Barrett J., Fiddler M., Thomson W., Payton T., and Silman A. Maternal-fetal HLA incompatibility and the course of inflammatory arthritis during pregnancy. J Rheumatol 27 (2000) 2843-2848
75. Østensen M., and Villiger M. Immunology of pregnancy as a remission inducing agent in rheumatoid arthritis. Transpl Immunol 9 (2002) 155-160
76. Hench P.S. The ameliorating effect of pregnancy on chronic atrophic (infectious rheumatoid) arthritis, fibrosistis, and intermittent hydrartrosis. Mayo Clinic Proc 13 (1938) 161
77. Neely N.T., and Persellin R.H. Activity of rheumatoid arthritis during pregnancy. Tex Med 73 (1977) 59-63
78. Østensen M., and Husby G. A prospective clinical study of the effect of pregnancy on rheumatoid arthritis and ankylosing spondylitis. Arthritis Rheum 26 (1983) 1155-1159
79. Unger A., Kay A., Griffin A.J., et al. Disease activity and pregnancy associated alpha2-glycoprotein in rheumatoid arthritis during pregnancy. BMJ 286 (1983) 750-752
80. Nelson J.L., Hughes K.A., Smith A.G., Nisperos B.B., Branchaud A.M., and Hansen J.A. Maternal-fetal disparity in HLA class II alloantigenes and the pregnancy-induced amelioration of rheumatoid arthritis. N Engl J Med 329 (1993) 466-471
81. Quinn C., Mulpeter K., Casey E.B., and Freighery C.F. Changes in levels of IgM RF and alpha2 PAG correlate with increased disease activity in rheumatoid during puerperium. Scand J Rheumatol 22 (1993) 273-279
82. Barrett J.H., Brennan P., Fiddler M.A., et al. Does Rheumatoid arthritis remit during pregnancy and relapse postpartum?. Arthritis Rheum 42 (1999) 1219-1227
83. Østensen M., Fuher L., Mathieu R., et al. A prospective study of pregnant patients with rheumatoid arthritis and ankylosing spondylits using validated clinical instruments. Ann Rheum Dis 63 (2004) 1212-1217
84. Fiddler M.A. Rheumatoid arthritis and pregnancy: issues for consideration in clinical management. Arthritis Care Res 10 (1997) 264-272
85. Nelson J.L., and Østensen M. Pregnancy and rheumatoid arthritis. Rheum Dis Clin North Am 23 (1997) 195-212
86. Silman A.J., Kay A., and Brennan P. Timing of pregnancy in relation to the onset of rheumatoid arthritis. Arthritis Rheum 35 (1992) 152-155
87. Brennan P., and Silman A.J. Breast-feeding and the onset of rheumatoid arthritis. Arthritis Rheum 37 (1994) 808-813
88. Barrett J.H., Brennan P., Fiddler M., et al. Breast-feeding and post partum relapse in women with rheumatoid and inflammatory arthritis. Arthritis Rheum 43 (2000) 1010-1015
89. Lloyd M.E., Carr M., McElhatton P., et al. The effects of methotrexate on pregnancy, fertility and lactation. Q J Med 92 (1999) 551-563
90. Janssen N.M., and Genta M.S. The effects of immunosoppressive and anti-inflammatory medications on fertility, pregnancy, and lactation. Arch Intern Med 160 (2000) 610-619
91. Brent R.L. Teratogen update: reproductive risks of leflunomide (Arava), a pyrimidine synthesis inhibitor: counseling women taking leflunomide before or during pregnancy and men taking leflunomide who are contemplating fathering a child. Teratology 63 (2001) 106-112
92. Giroir B.P., Peppel K., Silva M., et al. The biosynthesis of tumor necrosis factor during pregnancy: studies with CAT reporter transgene and TNF inhibitors. Eur Cytokine Netw 3 (1992) 533-538
93. Antoni C.E., Furst D., Manger B., et al. Outcome of pregnancy in women receiving remicade (Infliximab) for the tretment of Chron's disease or rheumatois arthritis. Arthritis Rheum 44 (2001) S84
94. Khanna D., McMahon M., and Furst D.E. Safety of tumour necrosis factor-alpha antagonists. Drug Saf 27 (2004) 307-324
95. Shrim A., and Koren G. Tumour necrosis factor alpha and use of infliximab. Safety during pregnancy. Can Fam Physician 51 (2005) 667-668
96. Katz J.A., Antoni C., Keenan G.F., Smth D.E., Jacobs S.J., and Lichtenstein G.R. Outcome of pregnancy in women receiving infliximab fort he treatment of Crohn's disease and rheumatoid arthritis. Am J Gastroenterol 99 (2004) 2385-2392