Neuroendocrine, immunologic, and microvascular systems interactions in rheumatoid arthritis: Physiopathogenetic and therapeutic perspectives

Seminars in Arthritis and Rheumatism

Volumn 29, Issue 2, 1999, Pages 65-81

  Masi, A T ^a   Bijlsma, J W J ^a   Chikanza, I C ^a   Pitzalis, C ^a   Cutolo, M ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

Hormones; Mediators of inflammation; Microvasculature; Rheumatoid arthritis; Risk factors; Therapy

Indexed keywords

CORTICOSTEROID; ESTRADIOL; GLUCOCORTICOID; PRASTERONE; PRASTERONE SULFATE; PROLACTIN;

CARDIOVASCULAR SYSTEM; CIGARETTE SMOKING; DISEASE CONTROL; FEMALE; HEALTH CARE PLANNING; HOMEOSTASIS; HORMONE BLOOD LEVEL; HUMAN; IMMUNE SYSTEM; INFLAMMATION; MALE; NEUROENDOCRINE SYSTEM; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; RISK FACTOR; VASCULAR ENDOTHELIUM;

EID: 0032746863     PISSN: 00490172     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0049-0172(99)80039-0     Document Type: Article

References (115)

1. Chrousos G.P. The hypothalamic-pituitary-adrenal axis and immune-mediated inflammation N Engl J Med 332 1995 1351 1362
2. Chikanza I.C. Grossman A.B. Neuroendocrine immune responses to inflammation: the concept of the neuroendocrine immune loop Ballières Clin Rheumatol 10 1996 199 225
3. Besedovsky H.O. del Rey A. Immune-neuro-endocrine interactions: facts and hypotheses Endocr Rev 17 1996 64 102
4. Pietrini P. Guazzelli M. Life events in the course of chronic diseases: a psychological myth or a psycho-neurobiochemical loop? Clin Exp Rheumatol 15 1997 125 128
5. Sternberg E.M. Neural-immune interactions in health and disease J Clin Invest 100 1997 2641 2647
6. Masi A.T. Feigenbaum S.L. Chatterton R.T. Hormonal and pregnancy relationships to rheumatoid arthritis: convergent effects with immunologic and microvascular systems Semin Arthritis Rheum 25 1995 1 27
7. Masi A.T. Feigenbaum S.L. Chatterton R.T. Cutolo M. Integrated hormonal-immunological-vascular (“H-I-V” triad) systems interactions in rheumatic diseases Clin Exp Rheumatol 13 1995 203 216
8. Masi A.T. Incidence of rheumatoid arthritis: do the observed age-sex interaction patterns support a role of androgenicanabolic steroid deficiency in its pathogenesis? Br J Rheumatol 33 1994 697 699
9. Masi A.T. Chang H.T. Cigarette smoking and other acquired risk factors for rheumatoid arthritis Kaufman L.D. Varga I. Rheumatic diseases and the environment 1999 Chapman & Hall New York 111 127
10. Springer T.A. Traffic signals for lymphocyte recirculation and leukocyte emigration: the multistep paradigm Cell 76 1994 301 314
11. Pitzalis C. The Michael Mason Prize Essay 1996: role of adhesion mechanisms in the pathogenesis of chronic synovitis Br J Rheumatol 35 1996 1198 1215
12. Templ E. Koeller M. Riedl M. Wagner O. Graninger W. Luger A. Anterior pituitary function in patients with newly diagnosed rheumatoid arthritis Br J Rheumatol 35 1996 350 356
13. (Suppl) Wilder R.L. Corticotropin releasing hormone and the hypothalamic-pituitary-adrenal axis in the regulation of inflammatory arthritis Agents Actions 41 1993 3 9
14. Masi A.T. DaSilva J.A.P. Cutolo M. Perturbations of hypothalamic-pituitary-gonadal (HPG) axis and adrenal androgen (AA) functions in rheumatoid arthritis Ballières Clin Rheum 10 1996 295 332
15. Jacob C.O. Cytokines and anti-cytokines Curr Op Immunol 2 1989 249 257
16. Akira S. Hirano T. Taga T. Kishimoto T. Biology of multifunctional cytokines: IL 6 and related molecules (IL 1 and TNF) FASEB J 4 1990 2860 2867
17. Hanamaijer R. Koolwijk P. Le Clercq L. de Vree W.J. van Hinsbergh V.W. Regulation of metalloproteinase expression in human vein and microvascular endothelial cells: effects of tumor necrosis factor alpha, interleukin 1and phorbol ester Biochem J 296 1993 803 809
18. Mackay C.R. Imhof B.A. Cell adhesion in the immune system Immunol Today 14 1993 99 102
19. Friedl H.P. Till G.O. Ryan U.S. Ward P.A. Mediatorinduced activation of xanthine oxidase in endothelial cells FASEB J 3 1989 2512 2518
20. Beckman J.S. Crow J.P. Pathological implications of nitric oxide, superoxide and peroxynitrite formation Biochem Soc Trans 21 1993 330 334
21. Baeurle P.A. Baltimore T. The physiology of the NFkB transcription factor Cohen P. Foulkes J.G. The hormonal control regulation of gene transcription 1991 Elsevier Science Amsterdam 423 446
22. Amstad P.A. Krupitza G. Cerutti P.A. Mechanisms of c-fos induction by active oxygen Cancer Res 52 1992 3952 3960
23. Wehling M. Specific, nongenomic actions of steroid hormones Annu Rev Physiol 59 1997 365 393
24. Catania A. Lipton J.M. Alpha-melanocyte stimulating hormone in the modulation of host reactions Endocr Rev 14 1993 564 576
25. Chikanza I.C. Panayi G.S. Hypothalamic-pituitary mediated modulation of immune function: prolactin as a neuroimmune peptide Br J Rheumatol 30 1991 203 207
26. Chikanza I.C. Grossman A.G. Hypothalamic-pituitarymediated immunomodulation: arginine vasopressin is a neuroendocrine immune mediator Br J Rheumatol 37 1998 131 136
27. Lotz M. Carson D.A. Vaughan J.H. Substance P activation of rheumatoid synoviocytes: neural pathway in pathogenesis of arthritis Science 235 1987 893 895
28. Karalis K. Sano H. Redwine J. Listwak S. Wilder R.L. Chrousos G.P. Autocrine or paracrine inflammatory actions of corticotropin-releasing hormone in vivo Science 254 1991 421 423
29. Chikanza I.C. The neuroendocrine immunology of rheumatoid arthritis Ballières Clin Rheumatol 10 1996 273 293
30. Arvidson N.G. Gudbjørnsson B. Elfman L. Ryddn A.C. Totterman T.H. Hällgren R. Circadian rhythm of serum interleukin-6 in rheumatoid arthritis Ann Rheum Dis 53 1994 521 524
31. Crofford L.J. Kalogeras K.T. Mastorakos G Majiakou M.A. Wells J. Kanik K.S. Circadian relationships between interleukin (IL)-6 and hypothalamic-pituitary-adrenal axis hormones: failure of IL-6 to cause sustainedhypercortisolism in patients with early untreated rheumatoid arthritis J Clin Endocrinol Metab 82 1997 1279 1283
32. Cutolo M. Foppiam L. Prete C. Hypothalamicpituitary-adrenocortical axis function in premenopausal women with rheumatoid arthritis not treated with glucocorticoids: controlled results indicating decreased plasma DHEA at baseline and following low dose ACTH J Rheumatol 26 1999 282 286
33. Masi A.T. Chrousos C.P. Bornstein S.R. Enigmas of adrenal androgen and glucocorticoid dissociation in premenopausal onset rheumatoid arthritis J Rheumatol 26 1999 247 250
34. Rook G.A.W. Hernandez-Pando R. Lightman S.L. Hormones, peripherally activated prohormones and regulation of the Th1/Th2 balance Immunol Today 15 1994 301 303
35. [abstract] Masi A.T. Chatterton R.T. Aldag J.C. Comstock G.W. Helzlsouer K.J. Hoffman S.C. Decreased serum dehydroepiandrosterone sulfate levels in menstruating women prior to onset of RA before age 50: independent reference laboratory assays validate previous significant results Arthritis Rheum 41 1998 S126
36. [abstract] Masi A.T. Chatterton R.T. Fecbt T. Aldag J.C. Comstock G.W. Helzlsouer K.J. Dissociation of serum dehydroepiandrosterone sulfate and cortisol levels in younger premenopausal women prior to onset of rheumatoid arthritis before age 50: results of a prospective, controlled study Arthritis Rheum 41 1998 S126
37. Levick J.R. Hypoxia and acidosis in chronic inflammatory arthritis: relation to vascular supply and dynamic effusion pressure J Rheumatol 17 1990 579 582
38. Stevens C.R. Blake D.R. Merry P. Revell P.A. Levick J.R. A comparative study by morpbometry of the microvasculature in normal and rheumatoid synovium Arthritis Rheum 34 1991 1508 1513
39. Colville-Nash P.R. Scott D.L. Angiogenesis and rheumatoid arthritis: pathogenic and therapeutic implications Ann Rheum Dis 51 1992 919 925
40. Edmonds S.E. Blake D.R. Morris C.J. Winyard P.G. An imaginative approach to synovitis: the role of hypoxic reperfusion damage in arthritis J Rheumatol 20 suppl 37 1993 26 31
41. [Review] Quyyumi A.A. Endothelial function in health and disease: new insights into the genesis of cardiovascular disease Am J Med 105 1998 325 395
42. Masi A.T. Chatterton R.T. Comstock G.W. Helzlsouer K.J. Hoffman S.C. Malamet R.L. A positive history of rheumatoid arthritis (RA) in a first degree relative (FDR) or a positive serological predictor for RA prior to disease onset before age 50 were uniformly present in a sample of younger, premenopausal incident cases: results of a prospective, controlled study Arthritis Rheum 41 1998 S126
43. Hasstedt S.J. Clegg D.O. Ingles L. Ward R.H. HLA-linked rheumatoid arthritis Am J Hum Genet 55 1994 738 746
44. Chap 41 Masi A.T. Feigenbaum S.L. Lockshin M.D. Rheumatological and antiphospholipid syndrome disorders (in press) Winn H.N. Hobbins J.C. Clinical maternal-fetal medicine 1999 Pathenon Publishing London
45. Morales D.E. McGowan K.A. Grant D.S. Maheswari S. Bhartiya D. Cid M.C. Estrogen promotes angiogenic activity in human umbilical vein endothelial cells in vitro and in a murine model Circulation 91 1995 755 763
46. Miller M.E. Dores G.M. Thorpe S.L. Akerly W.L. Paradoxical influence of estrogenic hormones on platelet-endothelial cell interactions Thromb Res 74 1994 577 594
47. Cutolo M. Sulli A. Seriolo B. Accardo S. Masi A.T. Estrogens, the immune response and autoimmunity Clin Exp Rheumatol 13 1995 217 226
48. Banerjee S.K. Campbell D.R. Weston A.P. Banerjee D.K. Biphasic estrogen response on bovine adrenal medulla capillary endothelial cell adhesion, proliferation and tube formation Mol Cell Biochem 177 1997 97 105
49. Cid M.C. Kleinman H.K. Grant D.S. Schnaper H.W. Fauci A.S. Hoffman G.S. Estradiol enhances leukocyte binding to tumor necrosis factor (TNF)-stimulated endothelial cells via an increase in TNF-induced adhesion molecules E-selectin, intercellular adhesion molecule type 1, and vascular cell adhesion molecule type 1 J Clin Invest 93 1994 17 25
50. Nakai K. Itoh C. Hotta K. Itoh T. Yoshizumi M. Hiramori K. Estradiol-17 beta regulates the induction of VCAM-1 mRNA expression by interleukin-1 beta in human umbilical vein endothelial cells Life Sci 54 1994 PL221 PL227
51. Hishikawa K. Nakaki T. Marumo T. Suzuki H. Kato R. Saruta T. Up-regulation of nitric oxide synthase by estradiol in human aortic endothelial cells FEBS Lett 360 1995 291 293
52. discussion, 67–69 Moncada S. Nitric oxide in the vasculature: physiology and pathophysiology Ann NY Acad Sci 811 1997 60 67
53. Clancy R.M. Amin A.R. Abramson S.B. The role of nitric oxide in inflammation and immunity Arthritis Rheum 41 1998 1141 1151
54. Rosselli M. Imthurn B. Macas E. Keller P.J. Dubey R.K. Endogenous nitric oxide modulates endothelin-1 induced contraction of bovine oviduct Biochem Biophys Res Commun 201 1994 143 148
55. Yallampalli C. Byam-Smith M. Nelson S.O. Garfield R.E. Steroid hormones modulate the production of nitric oxide and cGMP in the rat uterus Endocrinology 134 1994 1971 1974
56. Miyahara K. Kawamoto T. Sase K. Yui Y. Toda K. Yang L.X. Cloning and structural characterization of the human endothelial nitric-oxide-synthase gene Eur J Biochem 223 1994 719 726
57. Das S.K. Taylor J.A. Korach K.S. Paria B.C. Dey S.K. Lubahn D.B. Estrogenic responses in estrogen receptor-alpha deficient mice reveal a distinct estrogen signaling pathway Proc Natl Acad Sci U S A 94 1997 12786 12791
58. Hutchison S.J. Sudhir K. Chou T.M. Sievers R.E. Zhu B.Q. Sun Y.P. Testosterone worsens endothelial dysfunction associated with hypercholesterolemia and environmental tobacco smoke exposure in male rabbit aorta J Am Coll Cardiol 29 1997 800 807
59. Fujimoto R. Morimoto I. Morita E. Sugimoto H. Ito Y. Eto S. Androgen receptors, 5 alpha-reductase activity and androgen-dependent proliferation of vascular smooth muscle cells J Steroid Biochem Mol Biol 50 1994 169 174
60. Lansink M. Koolwijk P. van Hinsbergh V. Kooistra T. Effect of steroid hormones and retinoids on the formation of capillary-like tubular structures of human microvascular endothelial cells in fibrinmatrices is related to urokinase expression Blood 92 1998 927 938
61. Orth D.N. Kovacs W.J. The adrenal cortex Wilson J.D. Foster D.W. Kronenberg H.M. Larsen P.R. 9th ed. Williams Textbook of Endocrinology 1998 W.B. Saunders Philadelphia 517 664
62. Cronstein B.N. Kimmel S.C. Levin R.I. Martiniuk F. Weissmann G. A mechanism for the antiinflammatory effects of corticosteroids: the glucocorticoid receptor regulates leukocyte adhesion to endothelial cells and expression of endothelialleukocyte adhesion molecule 1 and intercellular adhesion molecule 1 Proc Natl Acad Sci U S A 89 1992 9991 9995
63. Pitzalis C. Pipitone N. Bajocchi G. Hall M. Goulding N. Lee A. Corticosteroids inhibit lymphocyte binding to endothelium and intercellular adhesion: an additional mechanism for their anti-inflammatory andimmunosuppressive effect J Immunol 10 1997 5007 5016
64. Schule R. Rangarajan P. Kliewer S. Ransone L.J. Bolado J. Yang N. Functional antagonism between oncoprotein c-Jun and the glucocorticoid receptor Cell 62 1990 1217 1226
65. Paliogianni F. Raptis A. Ahuja S.S. Najjar S.M. Boumpas D.T. Negative transcriptional regulation of human interleukin 2 (IL-2) gene by glucocorticoids through interference with nuclear transcription factorsAP-1 and NF-AT J Clin Invest 91 1993 1481 1489
66. Scheinman R.I. Gualberto A. Jewell C.M. Cidlowski J.A. Baldwin A.S. Jr Characterization of mechanisms involved in transrepression of NF-kappa B by activated glucocorticoid receptors Mol Cell Biol 15 1995 943 953
67. [see comments] Scheinman R.I. Cogswell P.C. Lofquist A.K. Baldwin A.S. Jr Role of transcriptional activation of I kappa B alpha in mediation of inununosuppression by glucocorticoids Science 270 1995 283 286
68. Boumpas D.T. Paliogianni F. Anastassiou E.D. Balow J.E. Glucocorticosteroid action on the immune system: molecular and cellular aspects Clin Exp Rheum 9 1991 413 423
69. Buttgereit F. Krauss S. Brand M.D. Methylprednisolone inhibits uptake of Cat+ and NA+ ions into concanavalin A-stimulated thymocytes Biochem J 326 1997 329 332
70. Masi A.T. Chrousos G.P. Dilemmas of low dosage glucocorticoid treatment in rheumatoid arthritis: considerations of timing Ann Rheum Dis 56 1997 1 4
71. Bellido T. Jilka R.L. Boyce B.F. Girasole G. Broxmeyer H. Dalrymple S.A. Regulation of interleukin-6, osteoclastogenesis and bone mass by androgens: the role of the androgen receptor J Clin Invest 95 1995 2886 2895
72. Keller E.T. Chang C. Ershler W.B. Inhibition of NFκB activity through maintenance of IκBα levels contributes to dihydrotestosterone-mediated repression of interleukin-6 promoter J Biol Chem 271 1996 26267 26275
73. Cutolo M. Do sex hormones modulate synovial macrophages in rheumatoid arthritis? Ann Rheum Dis 56 1997 281 284
74. Nelson J.L. Hughes K.A. Smith A.G. Nisperos B.B. Branchaud A.M. Hansen J.A. Maternal-fetal disparity in HLA class II alloantigens and the pregnancy-induced amelorization of rheumatoid arthritis N Engl J Med 329 1993 466 471
75. Rovensky J. Jurankova E. Rauova L. Biazickova S. Lukac J. Veselkova Z. Relationship between endocrine, immune and clinical variables in patients with systemic lupus erythematosus J Rheumatol 24 1997 2330 2334
76. Morita Y. Yamamura M. Harada S. Okamoto H. Inoue H. Makino H. A role of interleukin-12 in perpetuating Thl cellmediated immune responses in rheumatoid arthritis Arthritis Rheum 39 1996 S128
77. Suzuki T. Suzuki N. Daynes R.A. Ershlergrowth W.B. Dehydroepiandrosterone enhances IL-2 production and cytotoxic effector function of human T cells Clin Immunol Immunopathol 61 1993 202 211
78. Rincon M. Anguita J. Nakamura T. Fikrig E. Flavell R.A. Interleukin (IL)-6 directs the differentiation of IL-4-producing CD4+ T cells J Exp Med 185 1997 461 469
79. Araneo B.A. Dowell T. Diegel M. Daynes R.A. Dihydrotestosterone exerts a depressive influence on the production of interleukin-4 (IL-4), IL-5, and gamma interferon, but not IL-2 by activated routine T cells Blood 78 1991 688 699
80. Cutolo M. Accardo S. Villaggio B. Barone A. Sulli A. Balleari E. Androgen metabolism and inhibition of interleukin-1 synthesis in primary cultured human synovial macrophages Mediators Inflamm 4 1995 138 143
81. Daynes R.A. Dudley D.J. Araneo B.A. Regulation of murine lymphokine production in vivo. II. Dehydroepiandrosterone is a natural enhancer of interleukin 2 synthesis by helper T cells Eur J Immunol 20 1990 793 802
82. Daynes R.A. Araneo B.A. Ershler W.B. Maloney C. Li G.Z. Ryu S.Y. Altered regulation of IL-6 production with normal aging: possible linkage to the age-associated decline in dehydroepiandrosterone and its sulfated derivative J Immunol 150 1993 5219 5230
83. Daynes R.A. Araneo B.A. Contrasting effects of glucocorticoids on the capacity of T cells to produce the growth factors interleukin 2 and interleukin 4 Eur J Immunol 19 1989 2319 2325
84. Westacott C.I. Whicher J.T. Barnes I.C. Thompson D. Swan A.J. Dieppe P.A. Synovial fluid concentration of five different cytokines in rheumatic diseases Ann Rheum Dis 49 1990 676 681
85. Firestein G.S. Xu W.D. Townsend K. Broide D. AlvaroGracia J. Glasebrook A. Cytokines in chronic inflammatory arthritis. I. Failure to detect T cell lymphokines (interleukin 2 and interleukin 3) and presence of macrophagecolony-stimulating factor (CSF-1) and a novel mast cell growth factor in rheumatoid synovitis J Exp Med 168 1988 1573 1586
86. Ahmed S.A. Penhale W.J. Talal N. Sex hormones, immune response and autoimmune diseases: mechanisms of sex hormone action Am J Pathol 121 1985 531 555
87. Meulenberg P.M.M. Hofman J.A. Maternal testosterone and fetal sex J Steroid Biochem Mol Biol 39 1991 51 54
88. Elenkov L.J. Hoffman J. Wilder R.L. Does differential neuroendocrine control of cytokine production govern the expression of autoimmune diseases in pregnancy and the postpartum period? Mol Med Today 3 1997 379 383
89. Bijlsma J.W.J. Van Everdingen A.A. Jacobs J.W.G. Corticosteroids in rheumatoid arthritis: how best to use them Clin Immunother 3 1995 271 286
90. Verhoef C.M. van Roon J.A.G. Vianen M.E. Lafeber F.P.J.G. Bijlsma J.W.J. The immune suppressive effect of dexamethasone in rheumatoid arthritis is accompanied by upregulation of interleukin 10 and by differential changesin interferon y and interleukin 4 production Ann Rheum Dis 58 1999 49 54
91. Oka M. Effect of pregnancy on the onset and course of rheumatoid arthritis Ann Rheum Dis 12 1953 227 229
92. Nelson J.L. Østensen M. Pregnancy and rheumatoid arthritis Rheum Dis Clin North Am 23 1997 195 212
93. Cutolo M. Masi A.T. Do androgens influence the pathophysiology of rheumatoid arthritis? Facts and hypotheses J Rheumatol 25 1998 1041 1047
94. Cutolo M. Sulli A. Villaggio B. Seriolo B. Accardo S. Relationships between steroid hormones and cytokines in rheumatoid arthritis and systemic lupus erythematosus Ann Rheum Dis 57 1998 573 577
95. Cutolo M. The roles of steroid hormones in arthritis Br J Rheumatol 37 1998 597 601
96. Neuroendocrine immune basis of the rheumatic diseases Cutolo M. Masi A.T. Bijlsma J.W.J. Chikanza I.C. Bradlow L.W. Castagnetta L. Proceedings of The First International Conference Genoa, Italy, September 18–20, 1998 Ann NYAcad Sci 876 1999
97. Saag K.G. Criswell L.A. Sems K.M. Nettleman M.D. Kolluri S. Low-dose corticosteroids in rheumatoid arthritis: a meta-analysis of their moderate-term effectiveness Arthritis Rheum 39 1996 1818 1825
98. Kirwan J.R. The effect of glucocorticosteroids on joint destruction in rheumatoid arthritis. Arthritis and Rheumatism Council Low-dose Glucocorticoid StudyGroup N Eng J Med 333 1995 142 146
99. Boers M. Verhoeven A.C. Markusse H.M. van de Laar M.A.F.J. Westhovens R. van Denderen J.C. Randomised comparison of combined step-down prednisolone, methotrexate and sulphasalazine with sulphasalazine alone in early rheumatoid arthritis Lancet 350 1997 309 318
100. Weusten B.L. Jacobs J.W. Bijlsma J.W. Corticosteroid pulse therapy in active rheumatoid arthritis Semin Arthritis Rheum 23 1993 183 192
101. Schleimer R.P. Claman H.N. Dronsky A.L. Antiinflammatory steroid action: basic and clinical aspects 1989 Academic Press San Diego, CA
102. Saag K.G. Koehnke R. Caldwell J.R. Brasington R. Burmeister L.F. Zimmerman B. Low dose long-term corticosteroid therapy in rheumatoid arthritis: an analysis of serious adverse advents Am J Med 96 1994 115 123
103. Piper J.M. Ray W.A. Daugherty J.R. Griffin M.R. Corticosteroid use and peptic ulcer disease: role of non-steroidal anti-inflammatory drugs Ann Intern Med 114 1991 735 740
104. Spangler R.S. Cyclooxygenase 1 and 2 in rheumatic disease: implications for nonsteroidal anti-inflammatory drug therapy Semin Arthritis Rheum 26 1996 435 446
105. Bijlsma J.W.J. Prevention of glucocorticoid induced osteoporosis Ann Rheum Dis 56 1997 507 509
106. Recommendations for the prevention and treatment of glucocorticosteroid induced osteoporosis Arthritis Rheum 39 1996 American College of Rheumatology Task Force on Osteoporosis Guidelines 1791 1801
107. Ramos-Remus C. Russel A.S. Dangers of low dose corticosteroids in rheumatoid arthritis Bull Rheum Dis 46 1997 1 4
108. Cohen M.D. Conn D.L. Benefits of low-dose corticosteroids in rheumatoid arthritis Bull Rheum Dis 46 1997 4 7
109. Bijlsma J.W.J. van den Brink H.R. Estrogens and rheumatoid arthritis Am J Reprod Immunol 28 1992 231 234
110. van den Brink H.R. van Everdingen A.A. van Wijk M.J.G. Jacobs J.W.G. Bijlsma J.W.J. Adjuvant oestrogen therapy does not influence disease activity in postmenopausal female patients with rheumatoid arthritis Ann Rheum Dis 52 1993 862 865
111. Hall G.M. Daniels M. Huskisson E.C. Spector T.D. A randomized controlled trial of the effect of hormone replacement therapy on disease activity in postmenopausal rheumatoid arthritis Ann Rheum Dis 53 1994 112 116
112. van den Brink H.R. Lems W.F. van Everdingen A.A. Bijlsma J.W.J. Adjuvant oestrogen treatment increases bone mineral density in postmenopausal women with rheumatoid arthritis Ann Rheum Dis 52 1993 302 305
113. Bird H.A. Burkizshaw L. Pearson D. Atkinson P.J. Leathman P.A. Hill J. A controlled trial of nandrolone decanoate in the treatment of rheumatoid arthritis in postmenopausal women Ann Rheum Dis 46 1987 237 243
114. Booij A. Biewenga-Booij C.M. Huber-Bruning O. Cornelis C. Jacobs J.W.G. Bijlsma J.W.J. Androgens as adjuvant treatment in postmenopausal female patients with rheumatoid arthritis Ann Rheum Dis 55 1996 811 815
115. Cutolo M. Balleari E. Guisti M. Intra E. Accardo S. Androgen replacement therapy in male patients with rheumatoid arthritis Arthritis Rheum 34 1991 1 5