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Atherosclerosis in the Rheumatic Diseases: Compounding the Age Risk

  • Naoto Yokogawa
  • Joan M. Von FeldtEmail author
Chapter
  • 1k Downloads

Abstract

In geriatrics, atherosclerosis is a common ­comorbidity, since aging is the strongest risk factor for its development. Patients with autoimmune rheumatic disease have an increased risk of atherosclerotic cardiovascular ­disease (ASCVD) morbidity and mortality. Systemic lupus erythematosus (SLE) and rheumatoid arthritis (RA) have been studied the most, but other autoimmune diseases may confer the risk of ASCVD as well. In addition to traditional risk factors, systemic inflammation likely contributes to ASCVD risk. Atherosclerosis is considered an inflammatory process, and may be accelerated by systemic inflammation. ASCVD risk reduction can be targeted by aggressive management of ASCVD risk factors and the primary rheumatic disease.

Keywords

Atherosclerosis Atherosclerotic cardiovascular disease Endothelial dysfunction Inflammation Intimal-medial thickness Morbidity Mortality Rheumatic ­diseases Rheumatoid arthritis Systemic lupus erythematosus 

References

  1. 1.
    Ross R. Atherosclerosis – an inflammatory disease. N Engl J Med. 1999;340:115–26.PubMedGoogle Scholar
  2. 2.
    Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868–74.PubMedGoogle Scholar
  3. 3.
    Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685–95.PubMedGoogle Scholar
  4. 4.
    Aubry MC, Maradit-Kremers H, Reinalda MS, Crowson CS, Edwards WD, Gabriel SE. Differences in atherosclerotic coronary heart disease between subjects with and without rheumatoid arthritis. J Rheumatol. 2007;34:937–42.PubMedGoogle Scholar
  5. 5.
    Hollan I, Scott H, Saatvedt K, et al. Inflammatory rheumatic ­disease and smoking are predictors of aortic inflammation: a controlled study of biopsy specimens obtained at coronary artery surgery. Arthritis Rheum. 2007;56:2072–9.PubMedGoogle Scholar
  6. 6.
    van Leuven SI, Franssen R, Kastelein JJ, Levi M, Stroes ES, Tak PP. Systemic inflammation as a risk factor for atherothrombosis. Rheumatology. 2008;47:3–7.PubMedGoogle Scholar
  7. 7.
    Levi M, van der Poll T, Büller HR. Bidirectional relation between inflammation and coagulation. Circulation. 2004;109:2698–704.PubMedGoogle Scholar
  8. 8.
    Khovidhunkit W, Memon RA, Feingold KR, Grunfeldt C. Infection and inflammation-induced proatherogenic changes of lipoproteins. J Infect Dis. 2000;181:S462–72.PubMedGoogle Scholar
  9. 9.
    Hahn BH, Grossman J, Ansell BJ, Skaggs BJ, McMahon M. Altered lipoprotein metabolism in chronic inflammatory states: pro-inflammatory high-density lipoprotein and accelerated atherosclerosis in systemic lupus erythematosus and rheumatic disease. Arthritis Res Ther. 2008;10:213.PubMedGoogle Scholar
  10. 10.
    Crosby JR, Kaminski WE, Schatteman G, et al. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res. 2000;87:728–30.PubMedGoogle Scholar
  11. 11.
    Werner N, Kosiol S, Schiegl T, et al. Circulating endothelial ­progenitor cells and cardiovascular outcomes. N Engl J Med. 2005;353:999–1007.PubMedGoogle Scholar
  12. 12.
    Hill JM, Zalos G, Halcox JP, et al. Circulating endothelial progenitor cells, vascular function, and cardiovascular risk. N Engl J Med. 2003;348:593–600.PubMedGoogle Scholar
  13. 13.
    Vasa M, Fichtlscherer S, Aicher A, et al. Number and migratory activity of circulating endothelial progenitor cells inversely correlate with risk factors for coronary artery disease. Circ Res. 2001;89:E1–7.PubMedGoogle Scholar
  14. 14.
    Verma S, Kuliszewski MA, Li SH, et al. C-reactive protein attenuates endothelial progenitor cell survival, differentiation, and function: further evidence of a mechanistic link between C-reactive protein and cardiovascular disease. Circulation. 2004;109:2058–67.PubMedGoogle Scholar
  15. 15.
    Grisar J, Aletaha D, Steiner CW, et al. Depletion of endothelial progenitor cells in the peripheral blood of patients with rheumatoid arthritis. Circulation. 2005;111:204–11.PubMedGoogle Scholar
  16. 16.
    Denny MF, Thacker S, Mehta H, et al. Interferon-alpha induces abnormal vascular repair in systemic lupus erythematosus: a potential link to premature atherosclerosis. Blood. 2007;110:2907–15.PubMedGoogle Scholar
  17. 17.
    Lee PY, Li Y, Richards HB, et al. Type I interferon as a novel risk factor for endothelial progenitor cell depletion and endothelial dysfunction in systemic lupus erythematosus. Arthritis Rheum. 2007;56:3759–69.PubMedGoogle Scholar
  18. 18.
    Westerweel PE, Luijten RK, Hoefer IE, Koomans HA, Derksen RH, Verhaar MC. Haematopoietic and endothelial progenitor cells are deficient in quiescent systemic lupus erythematosus. Ann Rheum Dis. 2007;66:865–70.PubMedGoogle Scholar
  19. 19.
    Baechler EC, Batliwalla FM, Karypis G, et al. Interferon-inducible gene expression signature in peripheral blood cells of patients with severe lupus. Proc Natl Acad Sci USA. 2003;100:2610–5.PubMedGoogle Scholar
  20. 20.
    Bennett L, Palucka AK, Arce E, et al. Interferon and granulopoiesis signatures in systemic lupus erythematosus blood. J Exp Med. 2003;197:711–23.PubMedGoogle Scholar
  21. 21.
    Vaarala O, Alfthan G, Jauhiainen M, Leirisalo-Repo M, Aho K, Palosuo T. Crossreaction between antibodies to oxidised low-density lipoprotein and to cardiolipin in systemic lupus erythematosus. Lancet. 1993;341:923–5.PubMedGoogle Scholar
  22. 22.
    Delgado Alves J, Kumar S, Isenberg DA. Cross-reactivity between anti-cardiolipin, anti-high-density lipoprotein and anti-apolipoprotein A-I IgG antibodies in patients with systemic lupus erythematosus and primary antiphospholipid syndrome. Rheumatology. 2003;42:893–9.PubMedGoogle Scholar
  23. 23.
    Matsuura E, Koike T. Accelerated atheroma and anti-beta2-glycoprotein I antibodies. Lupus. 2000;9:210–6.PubMedGoogle Scholar
  24. 24.
    Navarro M, Cervera R, Font J, et al. Anti-endothelial cell antibodies in systemic autoimmune diseases: prevalence and clinical significance. Lupus. 1997;6:521–6.PubMedGoogle Scholar
  25. 25.
    Øhlenschlaeger T, Garred P, Madsen HO, Jacobsen S. Mannose-binding lectin variant alleles and the risk of arterial thrombosis in systemic lupus erythematosus. N Engl J Med. 2004;351:260–7.PubMedGoogle Scholar
  26. 26.
    Sjöholm AG, Jönsson G, Braconier JH, Sturfelt G, Truedsson L. Complement deficiency and disease: an update. Mol Immunol. 2006;43:78–85.PubMedGoogle Scholar
  27. 27.
    Liuzzo G, Goronzy JJ, Yang H, et al. Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes. Circulation. 2000;101:2883–8.PubMedGoogle Scholar
  28. 28.
    Kim WJ, Kim H, Suk K, Lee WH. Macrophages express granzyme B in the lesion areas of atherosclerosis and rheumatoid arthritis. Immunol Lett. 2007;111:57–65.PubMedGoogle Scholar
  29. 29.
    Swanberg M, Lidman O, Padyukov L, et al. MHC2TA is associated with differential MHC molecule expression and susceptibility to rheumatoid arthritis, multiple sclerosis and myocardial infarction. Nat Genet. 2005;37:486–94.PubMedGoogle Scholar
  30. 30.
    Watson DJ, Rhodes T, Guess HA. All-cause mortality and vascular events among patients with rheumatoid arthritis, osteoarthritis, or no arthritis in the UK General Practice Research Database. J Rheumatol. 2003;30:1196–202.PubMedGoogle Scholar
  31. 31.
    Urowitz MB, Ibañez D, Gladman DD. Atherosclerotic vascular events in a single large lupus cohort: prevalence and risk factors. J Rheumatol. 2007;34:70–5.PubMedGoogle Scholar
  32. 32.
    Ahmad Y, Shelmerdine J, Bodill H, et al. Subclinical atherosclerosis in systemic lupus erythematosus (SLE): the relative contribution of classic risk factors and the lupus phenotype. Rheumatology. 2007;46:983–8.PubMedGoogle Scholar
  33. 33.
    Roman MJ, Crow MK, Lockshin MD, et al. Rate and determinants of progression of atherosclerosis in systemic lupus erythematosus. Arthritis Rheum. 2007;56:3412–9.PubMedGoogle Scholar
  34. 34.
    Esdaile JM, Abrahamowicz M, Grodzicky T, et al. Traditional Framingham risk factors fail to fully account for accelerated ­atherosclerosis in systemic lupus erythematosus. Arthritis Rheum. 2001;44:2331–7.PubMedGoogle Scholar
  35. 35.
    Solomon DH, Curhan GC, Rimm EB, Cannuscio CC, Karlson EW. Cardiovascular risk factors in women with and without rheumatoid arthritis. Arthritis Rheum. 2004;50:3444–9.PubMedGoogle Scholar
  36. 36.
    Dessein PH, Norton GR, Woodiwiss AJ, Joffe BI, Wolfe F. Influence of nonclassical cardiovascular risk factors on the ­accuracy of predicting subclinical atherosclerosis in rheumatoid arthritis. J Rheumatol. 2007;34:943–51.PubMedGoogle Scholar
  37. 37.
    Gonzalez A, Maradit Kremers H, Crowson CS, et al. Do cardiovascular risk factors confer the same risk for cardiovascular outcomes in rheumatoid arthritis patients as in non-rheumatoid arthritis patients? Ann Rheum Dis. 2008;67:64–9.PubMedGoogle Scholar
  38. 38.
    Roman MJ, Shanker BA, Davis A, et al. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003;349:2399–406.PubMedGoogle Scholar
  39. 39.
    Von Feldt JM, Scalzi LV, Cucchiara AJ, et al. Homocysteine levels and disease duration independently correlate with coronary artery calcification in patients with systemic lupus erythematosus. Arthritis Rheum. 2006;54:2220–7.Google Scholar
  40. 40.
    Park YB, Lee SK, Lee WK, et al. Lipid profiles in untreated patients with rheumatoid arthritis. J Rheumatol. 1999;26:1701–4.PubMedGoogle Scholar
  41. 41.
    Choi HK, Seeger JD. Lipid profiles among US elderly with untreated rheumatoid arthritis – the Third National Health and Nutrition Examination Survey. J Rheumatol. 2005;32:2311–16.PubMedGoogle Scholar
  42. 42.
    Haskard DO. Accelerated atherosclerosis in inflammatory rheumatic diseases. Scand J Rheumatol. 2004;33:281–92.PubMedGoogle Scholar
  43. 43.
    Kroot EJ, van Leeuwen MA, van Rijswijk MH, et al. No increased mortality in patients with rheumatoid arthritis: up to 10 years of follow up from disease onset. Ann Rheum Dis. 2000;59:954–8.PubMedGoogle Scholar
  44. 44.
    Peltomaa R, Paimela L, Kautiainen H, Leirisalo-Repo M. Mortality in patients with rheumatoid arthritis treated actively from the time of diagnosis. Ann Rheum Dis. 2002;61:889–94.PubMedGoogle Scholar
  45. 45.
    Goodson N, Marks J, Lunt M, Symmons D. Cardiovascular admissions and mortality in an inception cohort of patients with rheumatoid arthritis with onset in the 1980s and 1990s. Ann Rheum Dis. 2005;64:1595–601.PubMedGoogle Scholar
  46. 46.
    Gabriel SE, Crowson CS, Kremers HM, et al. Survival in rheumatoid arthritis: a population-based analysis of trends over 40 years. Arthritis Rheum. 2003;48:54–8.PubMedGoogle Scholar
  47. 47.
    Gonzalez A, Maradit Kremers H, Crowson CS, et al. The widening mortality gap between rheumatoid arthritis patients and the general population. Arthritis Rheum. 2007;56:3583–7.PubMedGoogle Scholar
  48. 48.
    Kumar N, Marshall NJ, Hammal DM, et al. Causes of death in patients with rheumatoid arthritis: comparison with siblings and matched osteoarthritis controls. J Rheumatol. 2007;34:1695–8.PubMedGoogle Scholar
  49. 49.
    Solomon DH, Karlson EW, Rimm EB, et al. Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation. 2003;107:1303–7.PubMedGoogle Scholar
  50. 50.
    del Rincón ID, Williams K, Stern MP, Freeman GL, Escalante A. High incidence of cardiovascular events in a rheumatoid arthritis cohort not explained by traditional cardiac risk factors. Arthritis Rheum. 2001;44:2737–45.PubMedGoogle Scholar
  51. 51.
    Turesson C, Jarenros A, Jacobsson L. Increased incidence of cardiovascular disease in patients with rheumatoid arthritis: results from a community based study. Ann Rheum Dis. 2004;63:952–5.PubMedGoogle Scholar
  52. 52.
    Maradit-Kremers H, Crowson CS, Nicola PJ, et al. Increased unrecognized coronary heart disease and sudden deaths in rheumatoid arthritis: a population-based cohort study. Arthritis Rheum. 2005;52:402–11.PubMedGoogle Scholar
  53. 53.
    Kaplan MJ. Cardiovascular disease in rheumatoid arthritis. Curr Opin Rheumatol. 2006;18:289–97.PubMedGoogle Scholar
  54. 54.
    Turesson C, McClelland RL, Christianson TJ, Matteson EL. Severe extra-articular disease manifestations are associated with an increased risk of first ever cardiovascular events in patients with rheumatoid arthritis. Ann Rheum Dis. 2007;66:70–5.PubMedGoogle Scholar
  55. 55.
    Young A, Koduri G, Batley M, et al. Mortality in rheumatoid arthritis. Increased in the early course of disease, in ischaemic heart disease and in pulmonary fibrosis. Rheumatology. 2007;46:350–7.PubMedGoogle Scholar
  56. 56.
    Maradit-Kremers H, Nicola PJ, Crowson CS, Ballman KV, Gabriel SE. Cardiovascular death in rheumatoid arthritis: a population-based study. Arthritis Rheum. 2005;52:722–32.PubMedGoogle Scholar
  57. 57.
    Gerli R, Bartoloni Bocci E, Sherer Y, Vaudo G, Moscatelli S, Shoenfeld Y. Association of anti-cyclic citrullinated peptide antibodies with subclinical atherosclerosis in patients with rheumatoid arthritis. Ann Rheum Dis. 2008;67:724–5.PubMedGoogle Scholar
  58. 58.
    Urowitz MB, Bookman AA, Koehler BE, Gordon DA, Smythe HA, Ogryzlo MA. The bimodal mortality pattern of systemic lupus erythematosus. Am J Med. 1976;60:221–5.PubMedGoogle Scholar
  59. 59.
    Toloza SM, Uribe AG, McGwin Jr G, et al. Systemic lupus erythematosus in a multiethnic US cohort (LUMINA). XXIII. Baseline predictors of vascular events. Arthritis Rheum. 2004;50:3947–57.PubMedGoogle Scholar
  60. 60.
    Mancia G, De Backer G, Dominiczak A, et al. Management of Arterial Hypertension of the European Society of Hypertension; European Society of Cardiology. 2007 Guidelines for the Management of Arterial Hypertension: the Task Force for the Management of Arterial Hypertension of the European Society of Hypertension (ESH) and of the European Society of Cardiology (ESC). J Hypertens. 2007;25:1105–87.PubMedGoogle Scholar
  61. 61.
    Brohall G, Odén A, Fagerberg B. Carotid artery intima-media thickness in patients with Type 2 diabetes mellitus and impaired glucose tolerance: a systematic review. Diabet Med. 2006;23:609–16.PubMedGoogle Scholar
  62. 62.
    Lavrencic A, Kosmina B, Keber I, Videcnik V, Keber D. Carotid intima-media thickness in young patients with familial hypercholesterolaemia. Heart. 1996;76:321–5.PubMedGoogle Scholar
  63. 63.
    Pujia A, Gnasso A, Irace C, et al. Intimal plus media thickness of common carotid arterial wall in subjects with hypertension. Artery. 1994;21:222–33.PubMedGoogle Scholar
  64. 64.
    Salmon JE, Roman MJ. Subclinical atherosclerosis in rheumatoid arthritis and systemic lupus erythematosus. Am J Med. 2008;121:S3–8.PubMedGoogle Scholar
  65. 65.
    Sangiorgi G, Rumberger JA, Severson A, et al. Arterial calcification and not lumen stenosis is highly correlated with atherosclerotic plaque burden in humans: a histologic study of 723 coronary artery segments using nondecalcifying methodology. J Am Coll Cardiol. 1998;31:126–33.PubMedGoogle Scholar
  66. 66.
    Asanuma Y, Oeser A, Shintani AK, et al. Premature coronary-artery atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003;349:2407–15.PubMedGoogle Scholar
  67. 67.
    Celermajer DS, Sorensen KE, Gooch VM, et al. Invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet. 1992;340:1111–5.PubMedGoogle Scholar
  68. 68.
    Deanfield J, Donald A, Ferri C, et al. Endothelial function and dysfunction. Methodological issues for assessment in the different vascular beds: a statement by the Working Group on Endothelin and Endothelial Factors of the European Society of Hypertension. J Hypertens. 2005;23(7–17):233–46.PubMedGoogle Scholar
  69. 69.
    Gonzalez-Gay MA, Gonzalez-Juanatey C, Vazquez-Rodriguez TR, Martin J, Llorca J. Endothelial dysfunction, carotid intima-media thickness, and accelerated atherosclerosis in rheumatoid arthritis. Semin Arthritis Rheum. 2008;38:67–70.PubMedGoogle Scholar
  70. 70.
    Ames PR, Margarita A, Sokoll KB, Weston M, Brancaccio V. Premature atherosclerosis in primary antiphospholipid syndrome: preliminary data. Ann Rheum Dis. 2005;64:315–7.PubMedGoogle Scholar
  71. 71.
    Kimball AB, Robinson Jr D, Wu Y, et al. Cardiovascular disease and risk factors among psoriasis patients in two US healthcare databases, 2001–2002. Dermatology. 2008;217:27–37.PubMedGoogle Scholar
  72. 72.
    Gonzalez-Juanatey C, Llorca J, Amigo-Diaz E, Dierssen T, Martin J, Gonzalez-Gay MA. High prevalence of subclinical atherosclerosis in psoriatic arthritis patients without clinically evident cardiovascular disease or classic atherosclerosis risk factors. Arthritis Rheum. 2007;57:1074–80.PubMedGoogle Scholar
  73. 73.
    Mathieu S, Joly H, Baron G, et al. Trend towards increased arterial stiffness or intima-media thickness in ankylosing spondylitis patients without clinically evident cardiovascular disease. Rheumatology. 2008;47:1203–7.PubMedGoogle Scholar
  74. 74.
    Sari I, Okan T, Akar S, et al. Impaired endothelial function in patients with ankylosing spondylitis. Rheumatology. 2006;45:283–6.PubMedGoogle Scholar
  75. 75.
    de Leeuw K, Sanders JS, Stegeman C, Smit A, Kallenberg CG, Bijl M. Accelerated atherosclerosis in patients with Wegener’s granulomatosis. Ann Rheum Dis. 2005;64:753–9.PubMedGoogle Scholar
  76. 76.
    Gonzalez-Juanatey C, Lopez-Diaz MJ, Martin J, Llorca J, Gonzalez-Gay MA. Atherosclerosis in patients with biopsy-proven giant cell arteritis. Arthritis Rheum. 2007;57:1481–6.PubMedGoogle Scholar
  77. 77.
    Hettema ME, Bootsma H, Kallenberg CG. Macrovascular disease and atherosclerosis in SSc. Rheumatology. 2008;47:578–83.PubMedGoogle Scholar
  78. 78.
    Urowitz MB, Gladman DD, Ibanez D, Berliner Y. Modification of hypertension and hypercholesterolaemia in patients with systemic lupus erythematosus: a quality improvement study. Ann Rheum Dis. 2006;65:115–7.PubMedGoogle Scholar
  79. 79.
    Grosser T, Fries S, FitzGerald GA. Biological basis for the cardiovascular consequences of COX-2 inhibition: therapeutic challenges and opportunities. J Clin Invest. 2006;116:4–15.PubMedGoogle Scholar
  80. 80.
    Nussmeier NA, Whelton AA, Brown MT, et al. Complications of the COX-2 inhibitors parecoxib and valdecoxib after cardiac surgery. N Engl J Med. 2005;352:1081–91.PubMedGoogle Scholar
  81. 81.
    Bresalier RS, Sandler RS, Quan H, et al. Cardiovascular events associated with rofecoxib in a colorectal adenoma chemoprevention trial. N Engl J Med. 2005;352:1092–102.PubMedGoogle Scholar
  82. 82.
    Solomon DH, Avorn J, Stürmer T, Glynn RJ, Mogun H, Schneeweiss S. Cardiovascular outcomes in new users of coxibs and nonsteroidal antiinflammatory drugs: high-risk subgroups and time course of risk. Arthritis Rheum. 2006;54:1378–89.PubMedGoogle Scholar
  83. 83.
    Solomon DH, Glynn RJ, Rothman KJ, et al. Subgroup analyses to determine cardiovascular risk associated with nonsteroidal antiinflammatory drugs and coxibs in specific patient groups. Arthritis Rheum. 2008;59:1097–104.PubMedGoogle Scholar
  84. 84.
    Nashel DJ. Is atherosclerosis a complication of long-term corticosteroid treatment? Am J Med. 1986;80:925–9.PubMedGoogle Scholar
  85. 85.
    Da Silva JA, Jacobs JW, Kirwan JR, et al. Safety of low dose glucocorticoid treatment in rheumatoid arthritis: published evidence and prospective trial data. Ann Rheum Dis. 2006;65:285–93.PubMedGoogle Scholar
  86. 86.
    Davis III JM, Maradit Kremers H, Crowson CS, et al. Glucocorticoids and cardiovascular events in rheumatoid arthritis: a population-based cohort study. Arthritis Rheum. 2007;56:820–30.PubMedGoogle Scholar
  87. 87.
    Ridker PM, Cannon CP, Morrow D, et al. C-reactive protein ­levels and outcomes after statin therapy. N Engl J Med. 2005;352:20–8.PubMedGoogle Scholar
  88. 88.
    Ridker PM, Danielson E, Fonseca FA, et al. Rosuvastatin to prevent vascular events in men and women with elevated C-reactive protein. N Engl J Med. 2008;359:2195–207.PubMedGoogle Scholar
  89. 89.
    McCarey DW, McInnes IB, Madhok R, et al. Trial of atorvastatin in rheumatoid arthritis (TARA): double-blind, randomised ­placebo-controlled trial. Lancet. 2004;363:2015–21.PubMedGoogle Scholar
  90. 90.
    Costenbader KH, Karlson EW, Gall V, et al. Barriers to a trial of atherosclerosis prevention in systemic lupus erythematosus. Arthritis Rheum. 2005;53:718–23.PubMedGoogle Scholar
  91. 91.
    Choi HK, Hernán MA, Seeger JD, Robins JM, Wolfe F. Methotrexate and mortality in patients with rheumatoid arthritis: a prospective study. Lancet. 2002;359:1173–7.PubMedGoogle Scholar
  92. 92.
    Lafyatis R, York M, Marshak-Rothstein A. Antimalarial agents: closing the gate on Toll-like receptors? Arthritis Rheum. 2006;54:3068–70.PubMedGoogle Scholar
  93. 93.
    Wallace DJ, Metzger AL, Stecher VJ, Turnbull BA, Kern PA. Cholesterol-lowering effect of hydroxychloroquine in patients with rheumatic disease: reversal of deleterious effects of steroids on lipids. Am J Med. 1990;89:322–6.PubMedGoogle Scholar
  94. 94.
    Petri M, Lakatta C, Magder L, Goldman D. Effect of prednisone and hydroxychloroquine on coronary artery disease risk factors in systemic lupus erythematosus: a longitudinal data analysis. Am J Med. 1994;96:254–9.PubMedGoogle Scholar
  95. 95.
    Petri M. Hydroxychloroquine use in the Baltimore Lupus Cohort: effects on lipids, glucose and thrombosis. Lupus. 1996;5:S16–22.PubMedGoogle Scholar
  96. 96.
    Tam LS, Gladman DD, Hallett DC, Rahman P, Urowitz MB. Effect of antimalarial agents on the fasting lipid profile in systemic lupus erythematosus. J Rheumatol. 2000;27:2142–5.PubMedGoogle Scholar
  97. 97.
    Wasko MC, Hubert HB, Lingala VB, et al. Hydroxychloroquine and risk of diabetes in patients with rheumatoid arthritis. JAMA. 2007;298:187–93.PubMedGoogle Scholar
  98. 98.
    Wallace DJ. Does hydroxychloroquine sulfate prevent clot formation in systemic lupus erythematosus? Arthritis Rheum. 1987;30:1435–6.PubMedGoogle Scholar
  99. 99.
    Petri M. Thrombosis and systemic lupus erythematosus: the Hopkins Lupus Cohort perspective. Scand J Rheumatol. 1996;25:191–3.PubMedGoogle Scholar
  100. 100.
    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. 2002;41:924–9.PubMedGoogle Scholar
  101. 101.
    Ruiz-Irastorza G, Egurbide MV, Pijoan JI, et al. Effect of antimalarials on thrombosis and survival in patients with systemic lupus erythematosus. Lupus. 2006;15:577–83.PubMedGoogle Scholar
  102. 102.
    Alarcón GS, McGwin G, Bertoli AM, et al. Effect of hydroxychloroquine on the survival of patients with systemic lupus erythematosus: data from LUMINA, a multiethnic US cohort (LUMINA L). Ann Rheum Dis. 2007;66:1168–72.PubMedGoogle Scholar
  103. 103.
    Jacobsson LT, Turesson C, Gülfe A, et al. Treatment with tumor necrosis factor blockers is associated with a lower incidence of first cardiovascular events in patients with rheumatoid arthritis. J Rheumatol. 2005;32:1213–8.PubMedGoogle Scholar
  104. 104.
    Jacobsson LT, Turesson C, Nilsson JA, et al. Treatment with TNF blockers and mortality risk in patients with rheumatoid arthritis. Ann Rheum Dis. 2007;66:670–5.PubMedGoogle Scholar
  105. 105.
    Carmona L, Descalzo MA, Perez-Pampin E, et al. All-cause and cause-specific mortality in rheumatoid arthritis are not greater than expected when treated with tumour necrosis factor antagonists. Ann Rheum Dis. 2007;66:880–5.PubMedGoogle Scholar
  106. 106.
    Dixon WG, Watson KD, Lunt M, et al. Reduction in the incidence of myocardial infarction in patients with rheumatoid arthritis who respond to anti-tumor necrosis factor alpha therapy: results from the British Society for Rheumatology Biologics Register. Arthritis Rheum. 2007;56:2905–12.PubMedGoogle Scholar
  107. 107.
    Anker SD, Coats AJ. How to RECOVER from RENAISSANCE? The significance of the results of RECOVER, RENAISSANCE, RENEWAL and ATTACH. Int J Cardiol. 2002;86:123–30.PubMedGoogle Scholar
  108. 108.
    Wolfe F, Michaud K. Heart failure in rheumatoid arthritis: rates, predictors, and the effect of anti-tumor necrosis factor therapy. Am J Med. 2004;116:305–11.PubMedGoogle Scholar
  109. 109.
    van Leuven SI, Kastelein JJ, Allison AC, Hayden MR, Stroes ES. Mycophenolate mofetil (MMF): firing at the atherosclerotic plaque from different angles? Cardiovasc Res. 2006;69:341–7.PubMedGoogle Scholar

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© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  1. 1.Education Veterans Administration Medical CenterUniversity of PennsylvaniaPhiladelphiaUSA

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