Advertisement

Prevention of Stroke in Rheumatoid Arthritis

  • Alicia M. Zha
  • Mario Di Napoli
  • Réza Behrouz
Stroke (HP Adams, Section Editor)
Part of the following topical collections:
  1. Topical Collection on Stroke

Abstract

The risk of cerebrovascular disease is increased among rheumatoid arthritis (RA) patients and remains an underserved area of medical need. Only a minor proportion of RA patients achieve suitable stroke prevention. Classical cardiovascular risk factors appear to be under-diagnosed and undertreated among patients with RA. Reducing the inflammatory burden is also necessary to lower the cardiovascular risk. An adequate control of disease activity and cerebrovascular risk assessment using national guidelines should be recommended for all patients with RA. For patients with a documented history of cerebrovascular or cardiovascular risk factors, smoking cessation and corticosteroids and non-steroidal anti-inflammatory drugs at the lowest dose possible are crucial. Risk score models should be adapted for patients with RA by introducing a 1.5 multiplication factor, and their results interpreted to appropriately direct clinical care. Statins, angiotensin-converting enzyme inhibitors, and angiotensin-II receptor blockers are preferred treatment options. Biologic and non-biologic disease-modifying anti-rheumatic drugs should be initiated early to mitigate the necessity of symptom control drugs and to achieve early alleviation of the inflammatory state. Early control can improve vascular compliance, decrease atherosclerosis, improve overall lipid and metabolic profiles, and reduce the incidence of heart disease that may lead to atrial fibrillation. In patients with significant cervical spine involvement, early intervention and improved disease control are necessary and may prevent further mechanical vascular injury.

Keywords

Rheumatoid arthritis Stroke Cerebrovascular disease Risk factors Autoimmune disease Inflammation 

Notes

Compliance with Ethical Standards

Conflict of Interest

Alicia M. Zha, Mario Di Napoli, and Réza Behrouz declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. 1.•
    Behrouz R. The risk of ischemic stroke in major rheumatic disorders. J Neuroimmunol. 2014;277:1–5. A general review of the risk and epidemiology of ischemic stroke in major rheumatic disorders including RA. PubMedCrossRefGoogle Scholar
  2. 2.••
    Liou TH, Huang SW, Lin JW, et al. Risk of stroke in patients with rheumatism: a nationwide longitudinal population-based study. Sci Rep. 2014;4:5110. A large population based study or RA and lupus patients suggesting a strong association of stroke with RA. PubMedCentralPubMedCrossRefGoogle Scholar
  3. 3.
    Minaur NJ, Jacoby RK, Cosh JA, et al. Outcome after 40 years with rheumatoid arthritis: a prospective study of function, disease activity, and mortality. J Rheumatol Suppl. 2004;69:3–8.PubMedGoogle Scholar
  4. 4.
    Avina-Zubieta JA, Choi HK, Sadatsafavi M, et al. Risk of cardiovascular mortality in patients with rheumatoid arthritis: a meta-analysis of observational studies. Arthritis Rheum. 2008;59:1690–7.PubMedCrossRefGoogle Scholar
  5. 5.••
    Sodergren A, Stegmayr B, Ohman ML, Wallberg-Jonsson S. Increased incidence of stroke and impaired prognosis after stroke among patients with seropositive rheumatoid arthritis. Clin Exp Rheumatol. 2009;27:641–4. A study based on a large Swedish registry reporting an increased risk of stoke and subsequent mortality in RA patients, compared to the general population. PubMedGoogle Scholar
  6. 6.
    Bacani AK, Gabriel SE, Crowson CS, et al. Noncardiac vascular disease in rheumatoid arthritis: increase in venous thromboembolic events? Arthritis Rheum. 2012;64:53–61.PubMedCentralPubMedCrossRefGoogle Scholar
  7. 7.
    Solomon DH, Goodson NJ, Katz JN, et al. Patterns of cardiovascular risk in rheumatoid arthritis. Ann Rheum Dis. 2006;65:1608–12.PubMedCentralPubMedCrossRefGoogle Scholar
  8. 8.
    Solomon DH, Karlson EW, Rimm EB, et al. Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation. 2003;107:1303–7.PubMedCrossRefGoogle Scholar
  9. 9.
    Solomon DH, Kremer J, Curtis JR, et al. Explaining the cardiovascular risk associated with rheumatoid arthritis: traditional risk factors versus markers of rheumatoid arthritis severity. Ann Rheum Dis. 2010;69:1920–5.PubMedCentralPubMedCrossRefGoogle Scholar
  10. 10.•
    Boyer JF, Gourraud PA, Cantagrel A, et al. Traditional cardiovascular risk factors in rheumatoid arthritis: a meta-analysis. Joint Bone Spine. 2011;78:179–83.PubMedCrossRefGoogle Scholar
  11. 11.
    van Halm VP, Peters MJ, Voskuyl AE, et al. Rheumatoid arthritis versus diabetes as a risk factor for cardiovascular disease: a cross-sectional study, the CARRE Investigation. Ann Rheum Dis. 2009;68:1395–400.PubMedCrossRefGoogle Scholar
  12. 12.
    Aubry MC, Maradit-Kremers H, Reinalda MS, et al. Differences in atherosclerotic coronary heart disease between subjects with and without rheumatoid arthritis. J Rheumatol. 2007;34:937–42.PubMedGoogle Scholar
  13. 13.•
    del Rincon ID, Williams K, Stern MP, et al. High incidence of cardiovascular events in a rheumatoid arthritis cohort not explained by traditional cardiac risk factors. Arthritis Rheum. 2001;44:2737–45. A study suggesting RA could be an independent risk factor for stroke. PubMedCrossRefGoogle Scholar
  14. 14.
    Dessein PH, Joffe BI, Stanwix AE. Inflammation, insulin resistance, and aberrant lipid metabolism as cardiovascular risk factors in rheumatoid arthritis. J Rheumatol. 2003;30:1403–5.PubMedGoogle Scholar
  15. 15.
    Choi HK, Seeger JD. Lipid profiles among US elderly with untreated rheumatoid arthritis—the Third National Health and Nutrition Examination Survey. J Rheumatol. 2005;32:2311–6.PubMedGoogle Scholar
  16. 16.•
    Del Rincon I, Williams K, Stern MP, et al. Association between carotid atherosclerosis and markers of inflammation in rheumatoid arthritis patients and healthy subjects. Arthritis Rheum. 2003;48:1833–40. One of the earliest reports of linking RA to early atherosclerosis. PubMedCrossRefGoogle Scholar
  17. 17.
    Gonzalez-Gay MA, Gonzalez-Juanatey C, Lopez-Diaz MJ, et al. HLA-DRB1 and persistent chronic inflammation contribute to cardiovascular events and cardiovascular mortality in patients with rheumatoid arthritis. Arthritis Rheum. 2007;57:125–32.PubMedCrossRefGoogle Scholar
  18. 18.
    Goodson NJ, Symmons DP, Scott DG, et al. Baseline levels of C-reactive protein and prediction of death from cardiovascular disease in patients with inflammatory polyarthritis: a ten-year follow up study of a primary care-based inception cohort. Arthritis Rheum. 2005;52:2293–9.PubMedCrossRefGoogle Scholar
  19. 19.
    Wallberg-Jonsson S, Johansson H, Ohman ML, Rantapaa-Dahlqvist S. Extent of inflammation predicts cardiovascular disease and overall mortality in seropositive rheumatoid arthritis. A retrospective cohort study from disease onset. J Rheumatol. 1999;26:2562–71.PubMedGoogle Scholar
  20. 20.
    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.PubMedCrossRefGoogle Scholar
  21. 21.
    Hallenbeck JM. Inflammatory reactions at the blood-endothelial interface in acute stroke. Adv Neurol. 1996;71:281–97. discussion 297-300.PubMedGoogle Scholar
  22. 22.
    Becker KJ. Targeting the central nervous system inflammatory response in ischemic stroke. Curr Opin Neurol. 2001;14:349–53.PubMedCrossRefGoogle Scholar
  23. 23.
    Sattar N, McCarey DW, Capell H, McInnes IB. Explaining how “high-grade” systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation. 2003;108:2957–63.PubMedCrossRefGoogle Scholar
  24. 24.
    Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685–95.PubMedCrossRefGoogle Scholar
  25. 25.
    Farragher TM, Goodson NJ, Naseem H, et al. Association of the HLA-DRB1 gene with premature death, particularly from cardiovascular disease, in patients with rheumatoid arthritis and inflammatory polyarthritis. Arthritis Rheum. 2008;58:359–69.PubMedCentralPubMedCrossRefGoogle Scholar
  26. 26.••
    van den Oever IA, van Sijl AM, Nurmohamed MT. Management of cardiovascular risk in patients with rheumatoid arthritis: evidence and expert opinion. Ther Adv Musculoskelet Dis. 2013;5:166–81. Closet body of literature to a guideline for manamgnent of cardiovascular risk specifically in RA patients. PubMedCentralPubMedCrossRefGoogle Scholar
  27. 27.
    Toussirot E, Michel F, Binda D, Dumoulin G. The role of leptin in the pathophysiology of rheumatoid arthritis. Life Sci. 2015.Google Scholar
  28. 28.
    Curb JD, Abbott RD, Rodriguez BL, et al. C-reactive protein and the future risk of thromboembolic stroke in healthy men. Circulation. 2003;107:2016–20.PubMedCrossRefGoogle Scholar
  29. 29.
    Hallenbeck JM. The many faces of tumor necrosis factor in stroke. Nat Med. 2002;8:1363–8.PubMedCrossRefGoogle Scholar
  30. 30.
    Zhang J, Fu L, Shi J, et al. The risk of metabolic syndrome in patients with rheumatoid arthritis: a meta-analysis of observational studies. PLoS One. 2013;8:e78151.PubMedCentralPubMedCrossRefGoogle Scholar
  31. 31.
    da Cunha VR, Brenol CV, Brenol JC, et al. Metabolic syndrome prevalence is increased in rheumatoid arthritis patients and is associated with disease activity. Scand J Rheumatol. 2012;41:186–91.PubMedCrossRefGoogle Scholar
  32. 32.
    Chung CP, Oeser A, Solus JF, et al. Prevalence of the metabolic syndrome is increased in rheumatoid arthritis and is associated with coronary atherosclerosis. Atherosclerosis. 2008;196:756–63.PubMedCrossRefGoogle Scholar
  33. 33.
    Han C, Robinson Jr DW, Hackett MV, et al. Cardiovascular disease and risk factors in patients with rheumatoid arthritis, psoriatic arthritis, and ankylosing spondylitis. J Rheumatol. 2006;33:2167–72.PubMedGoogle Scholar
  34. 34.
    Tam LS, Tomlinson B, Chu TT, et al. Cardiovascular risk profile of patients with psoriatic arthritis compared to controls—the role of inflammation. Rheumatology (Oxford). 2008;47:718–23.CrossRefGoogle Scholar
  35. 35.
    Suissa S, Bernatsky S, Hudson M. Antirheumatic drug use and the risk of acute myocardial infarction. Arthritis Rheum. 2006;55:531–6.PubMedCrossRefGoogle Scholar
  36. 36.
    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.PubMedCentralPubMedCrossRefGoogle Scholar
  37. 37.
    Edwards CJ, Arden NK, Fisher D, et al. The changing use of disease-modifying anti-rheumatic drugs in individuals with rheumatoid arthritis from the United Kingdom General Practice Research Database. Rheumatology (Oxford). 2005;44:1394–8.CrossRefGoogle Scholar
  38. 38.
    Choi HK, Hernan MA, Seeger JD, et al. Methotrexate and mortality in patients with rheumatoid arthritis: a prospective study. Lancet. 2002;359:1173–7.PubMedCrossRefGoogle Scholar
  39. 39.
    Naranjo A, Sokka T, Descalzo MA, et al. Cardiovascular disease in patients with rheumatoid arthritis: results from the QUEST-RA study. Arthritis Res Ther. 2008;10:R30.PubMedCentralPubMedCrossRefGoogle Scholar
  40. 40.
    Prodanovich S, Ma F, Taylor JR, et al. Methotrexate reduces incidence of vascular diseases in veterans with psoriasis or rheumatoid arthritis. J Am Acad Dermatol. 2005;52:262–7.PubMedCrossRefGoogle Scholar
  41. 41.
    Park YB, Choi HK, Kim MY, et al. Effects of antirheumatic therapy on serum lipid levels in patients with rheumatoid arthritis: a prospective study. Am J Med. 2002;113:188–93.PubMedCrossRefGoogle Scholar
  42. 42.
    Georgiadis AN, Papavasiliou EC, Lourida ES, et al. Atherogenic lipid profile is a feature characteristic of patients with early rheumatoid arthritis: effect of early treatment—a prospective, controlled study. Arthritis Res Ther. 2006;8:R82.PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Dessein PH, Joffe BI, Stanwix AE. Effects of disease modifying agents and dietary intervention on insulin resistance and dyslipidemia in inflammatory arthritis: a pilot study. Arthritis Res. 2002;4:R12.PubMedCentralPubMedCrossRefGoogle Scholar
  44. 44.
    Panoulas VF, Metsios GS, Pace AV, et al. Hypertension in rheumatoid arthritis. Rheumatology (Oxford). 2008;47:1286–98.CrossRefGoogle Scholar
  45. 45.
    Kumeda Y, Inaba M, Goto H, et al. Increased thickness of the arterial intima-media detected by ultrasonography in patients with rheumatoid arthritis. Arthritis Rheum. 2002;46:1489–97.PubMedCrossRefGoogle Scholar
  46. 46.
    Wallberg-Jonsson S, Ohman M, Rantapaa-Dahlqvist S. Which factors are related to the presence of atherosclerosis in rheumatoid arthritis? Scand J Rheumatol. 2004;33:373–9.PubMedCrossRefGoogle Scholar
  47. 47.
    Kisiel B, Kruszewski R, Juszkiewicz A et al. Methotrexate, cyclosporine A, and biologics protect against atherosclerosis in rheumatoid arthritis. J Immunol Res. 2015; 2015:759610.Google Scholar
  48. 48.
    Roubille C, Richer V, Starnino T, et al. The effects of tumour necrosis factor inhibitors, methotrexate, non-steroidal anti-inflammatory drugs and corticosteroids on cardiovascular events in rheumatoid arthritis, psoriasis and psoriatic arthritis: a systematic review and meta-analysis. Ann Rheum Dis. 2015;74:480–9.PubMedCentralPubMedCrossRefGoogle Scholar
  49. 49.
    Avina-Zubieta JA, Abrahamowicz M, De Vera MA, et al. Immediate and past cumulative effects of oral glucocorticoids on the risk of acute myocardial infarction in rheumatoid arthritis: a population-based study. Rheumatology (Oxford). 2013;52:68–75.CrossRefGoogle Scholar
  50. 50.
    del Rincon I, Battafarano DF, Restrepo JF, et al. Glucocorticoid dose thresholds associated with all-cause and cardiovascular mortality in rheumatoid arthritis. Arthritis Rheumatol. 2014;66:264–72.PubMedCrossRefGoogle Scholar
  51. 51.
    Hashizume M, Mihara M. Blockade of IL-6 and TNF-alpha inhibited oxLDL-induced production of MCP-1 via scavenger receptor induction. Eur J Pharmacol. 2012;689:249–54.PubMedCrossRefGoogle Scholar
  52. 52.
    Heathfield SK, Parker B, Zeef LA, et al. Certolizumab pegol attenuates the pro-inflammatory state in endothelial cells in a manner that is atheroprotective. Clin Exp Rheumatol. 2013;31:225–33.PubMedGoogle Scholar
  53. 53.
    Branen L, Hovgaard L, Nitulescu M, et al. Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol. 2004;24:2137–42.PubMedCrossRefGoogle Scholar
  54. 54.
    Greenberg JD, Kremer JM, Curtis JR, et al. Tumour necrosis factor antagonist use and associated risk reduction of cardiovascular events among patients with rheumatoid arthritis. Ann Rheum Dis. 2011;70:576–82.PubMedCrossRefGoogle Scholar
  55. 55.
    Robertson J, Peters MJ, McInnes IB, Sattar N. Changes in lipid levels with inflammation and therapy in RA: a maturing paradigm. Nat Rev Rheumatol. 2013;9:513–23.PubMedCrossRefGoogle Scholar
  56. 56.
    Spanakis E, Sidiropoulos P, Papadakis J, et al. Modest but sustained increase of serum high density lipoprotein cholesterol levels in patients with inflammatory arthritides treated with infliximab. J Rheumatol. 2006;33:2440–6.PubMedGoogle Scholar
  57. 57.
    Popa C, Netea MG, Radstake T, et al. Influence of anti-tumour necrosis factor therapy on cardiovascular risk factors in patients with active rheumatoid arthritis. Ann Rheum Dis. 2005;64:303–5.PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Daien CI, Duny Y, Barnetche T, et al. Effect of TNF inhibitors on lipid profile in rheumatoid arthritis: a systematic review with meta-analysis. Ann Rheum Dis. 2012;71:862–8.PubMedCrossRefGoogle Scholar
  59. 59.
    Kerekes G, Soltesz P, Der H, et al. Effects of rituximab treatment on endothelial dysfunction, carotid atherosclerosis, and lipid profile in rheumatoid arthritis. Clin Rheumatol. 2009;28:705–10.PubMedCrossRefGoogle Scholar
  60. 60.
    Souto A, Salgado E, Maneiro JR, et al. Lipid profile changes in patients with chronic inflammatory arthritis treated with biologic agents and tofacitinib in randomized clinical trials: a systematic review and meta-analysis. Arthritis Rheumatol. 2015;67:117–27.PubMedCrossRefGoogle Scholar
  61. 61.
    Rao VU, Pavlov A, Klearman M, et al. An evaluation of risk factors for major adverse cardiovascular events during tocilizumab therapy. Arthritis Rheumatol. 2015;67:372–80.PubMedCrossRefGoogle Scholar
  62. 62.
    Kume K, Amano K, Yamada S, et al. Tocilizumab monotherapy reduces arterial stiffness as effectively as etanercept or adalimumab monotherapy in rheumatoid arthritis: an open-label randomized controlled trial. J Rheumatol. 2011;38:2169–71.PubMedCrossRefGoogle Scholar
  63. 63.
    Tam LS, Shang Q, Li EK, et al. Infliximab is associated with improvement in arterial stiffness in patients with early rheumatoid arthritis—a randomized trial. J Rheumatol. 2012;39:2267–75.PubMedCrossRefGoogle Scholar
  64. 64.
    Sidiropoulos PI, Siakka P, Pagonidis K, et al. Sustained improvement of vascular endothelial function during anti-TNFalpha treatment in rheumatoid arthritis patients. Scand J Rheumatol. 2009;38:6–10.PubMedCrossRefGoogle Scholar
  65. 65.
    Gonzalez-Juanatey C, Vazquez-Rodriguez TR, Miranda-Filloy JA, et al. Anti-TNF-alpha-adalimumab therapy is associated with persistent improvement of endothelial function without progression of carotid intima-media wall thickness in patients with rheumatoid arthritis refractory to conventional therapy. Mediat Inflamm. 2012;2012:674265.CrossRefGoogle Scholar
  66. 66.
    Del Porto F, Lagana B, Lai S, et al. Response to anti-tumour necrosis factor alpha blockade is associated with reduction of carotid intima-media thickness in patients with active rheumatoid arthritis. Rheumatology (Oxford). 2007;46:1111–5.CrossRefGoogle Scholar
  67. 67.
    Ferrante A, Giardina AR, Ciccia F, et al. Long-term anti-tumour necrosis factor therapy reverses the progression of carotid intima-media thickness in female patients with active rheumatoid arthritis. Rheumatol Int. 2009;30:193–8.PubMedCrossRefGoogle Scholar
  68. 68.
    Tam LS, Li EK, Shang Q, et al. Tumour necrosis factor alpha blockade is associated with sustained regression of carotid intima-media thickness for patients with active psoriatic arthritis: a 2-year pilot study. Ann Rheum Dis. 2011;70:705–6.PubMedCrossRefGoogle Scholar
  69. 69.
    Angel K, Provan SA, Fagerhol MK, et al. Effect of 1-year anti-TNF-alpha therapy on aortic stiffness, carotid atherosclerosis, and calprotectin in inflammatory arthropathies: a controlled study. Am J Hypertens. 2012;25:644–50.PubMedCentralPubMedCrossRefGoogle Scholar
  70. 70.
    Wong M, Oakley SP, Young L, et al. Infliximab improves vascular stiffness in patients with rheumatoid arthritis. Ann Rheum Dis. 2009;68:1277–84.PubMedCentralPubMedCrossRefGoogle Scholar
  71. 71.
    Kerekes G, Soltesz P, Szucs G, et al. Effects of adalimumab treatment on vascular disease associated with early rheumatoid arthritis. Isr Med Assoc J. 2011;13:147–52.PubMedGoogle Scholar
  72. 72.
    Kirkham BW, Wasko MC, Hsia EC, et al. Effects of golimumab, an anti-tumour necrosis factor-alpha human monoclonal antibody, on lipids and markers of inflammation. Ann Rheum Dis. 2014;73:161–9.PubMedCentralPubMedCrossRefGoogle Scholar
  73. 73.
    Benucci M, Saviola G, Manfredi M, et al. Factors correlated with improvement of endothelial dysfunction during rituximab therapy in patients with rheumatoid arthritis. Biologics. 2013;7:69–75.PubMedCentralPubMedGoogle Scholar
  74. 74.
    Peters MJ, van Halm VP, Voskuyl AE, et al. Does rheumatoid arthritis equal diabetes mellitus as an independent risk factor for cardiovascular disease? A prospective study. Arthritis Rheum. 2009;61:1571–9.PubMedCrossRefGoogle Scholar
  75. 75.
    Myasoedova E, Crowson CS, Kremers HM, et al. Lipid paradox in rheumatoid arthritis: the impact of serum lipid measures and systemic inflammation on the risk of cardiovascular disease. Ann Rheum Dis. 2011;70:482–7.PubMedCentralPubMedCrossRefGoogle Scholar
  76. 76.
    Kinosian B, Glick H, Garland G. Cholesterol and coronary heart disease: predicting risks by levels and ratios. Ann Intern Med. 1994;121:641–7.PubMedCrossRefGoogle Scholar
  77. 77.
    Yoo WH. Dyslipoproteinemia in patients with active rheumatoid arthritis: effects of disease activity, sex, and menopausal status on lipid profiles. J Rheumatol. 2004;31:1746–53.PubMedGoogle Scholar
  78. 78.
    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.PubMedCrossRefGoogle Scholar
  79. 79.
    Rollefstad S, Ikdahl E, Hisdal J, et al. Rosuvastatin-induced carotid plaque regression in patients with inflammatory joint diseases: the rosuvastatin in rheumatoid arthritis, ankylosing spondylitis and other inflammatory joint diseases study. Arthritis Rheumatol. 2015;67:1718–28.PubMedCrossRefGoogle Scholar
  80. 80.
    Dhillon N, Liang K. Prevention of stroke in rheumatoid arthritis. Curr Treat Options Neurol. 2015;17:356.PubMedCrossRefGoogle Scholar
  81. 81.
    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.PubMedCrossRefGoogle Scholar
  82. 82.
    Kernan WN, Ovbiagele B, Black HR, et al. Guidelines for the prevention of stroke in patients with stroke and transient ischemic attack: a guideline for healthcare professionals from the American Heart Association/American Stroke Association. Stroke. 2014;45:2160–236.PubMedCrossRefGoogle Scholar
  83. 83.
    Tikiz C, Utuk O, Pirildar T, et al. Effects of Angiotensin-converting enzyme inhibition and statin treatment on inflammatory markers and endothelial functions in patients with longterm rheumatoid arthritis. J Rheumatol. 2005;32:2095–101.PubMedGoogle Scholar
  84. 84.
    Flammer AJ, Sudano I, Hermann F, et al. Angiotensin-converting enzyme inhibition improves vascular function in rheumatoid arthritis. Circulation. 2008;117:2262–9.PubMedCrossRefGoogle Scholar
  85. 85.
    Dagenais NJ, Jamali F. Protective effects of angiotensin II interruption: evidence for antiinflammatory actions. Pharmacotherapy. 2005;25:1213–29.PubMedCrossRefGoogle Scholar
  86. 86.
    Peters MJ, Symmons DP, McCarey D, et al. EULAR evidence-based recommendations for cardiovascular risk management in patients with rheumatoid arthritis and other forms of inflammatory arthritis. Ann Rheum Dis. 2010;69:325–31.PubMedCrossRefGoogle Scholar
  87. 87.
    Goodson NJ, Brookhart AM, Symmons DP, et al. Non-steroidal anti-inflammatory drug use does not appear to be associated with increased cardiovascular mortality in patients with inflammatory polyarthritis: results from a primary care based inception cohort of patients. Ann Rheum Dis. 2009;68:367–72.PubMedCentralPubMedCrossRefGoogle Scholar
  88. 88.
    Crofford LJ, Breyer MD, Strand CV, et al. Cardiovascular effects of selective COX-2 inhibition: is there a class effect? The International COX-2 Study Group. J Rheumatol. 2006;33:1403–8.PubMedGoogle Scholar
  89. 89.
    Greenberg JD, Bingham 3rd CO, Abramson SB, et al. Effect of cardiovascular comorbidities and concomitant aspirin use on selection of cyclooxygenase inhibitor among rheumatologists. Arthritis Rheum. 2005;53:12–7.PubMedCrossRefGoogle Scholar
  90. 90.
    Chung WS, Peng CL, Lin CL, et al. Rheumatoid arthritis increases the risk of deep vein thrombosis and pulmonary thromboembolism: a nationwide cohort study. Ann Rheum Dis. 2014;73:1774–80.PubMedCrossRefGoogle Scholar
  91. 91.
    de Laat B, Mertens K, de Groot PG. Mechanisms of disease: antiphospholipid antibodies-from clinical association to pathologic mechanism. Nat Clin Pract Rheumatol. 2008;4:192–9.PubMedCrossRefGoogle Scholar
  92. 92.
    Mukubo Y, Kawamata M. Perioperative hypercoagulability in patients with rheumatoid arthritis: Sonoclot study. J Anesth. 2004;18:62–4.PubMedCrossRefGoogle Scholar
  93. 93.
    Olech E, Merrill JT. The prevalence and clinical significance of antiphospholipid antibodies in rheumatoid arthritis. Curr Rheumatol Rep. 2006;8:100–8.PubMedCrossRefGoogle Scholar
  94. 94.
    Gladd DA, Olech E. Antiphospholipid antibodies in rheumatoid arthritis: identifying the dominoes. Curr Rheumatol Rep. 2009;11:43–51.PubMedCrossRefGoogle Scholar
  95. 95.
    Erkan D, Lockshin MD. Antiphospholipid syndrome. Curr Opin Rheumatol. 2006;18:242–8.PubMedGoogle Scholar
  96. 96.
    Levine SR, Brey RL, Tilley BC, et al. Antiphospholipid antibodies and subsequent thrombo-occlusive events in patients with ischemic stroke. JAMA. 2004;291:576–84.PubMedCrossRefGoogle Scholar
  97. 97.
    Hoekstra M, Haagsma CJ, Doelman CJ, van de Laar MA. Intermittent rises in plasma homocysteine in patients with rheumatoid arthritis treated with higher dose methotrexate. Ann Rheum Dis. 2005;64:141–3.PubMedCentralPubMedCrossRefGoogle Scholar
  98. 98.
    Engelmann MD, Svendsen JH. Inflammation in the genesis and perpetuation of atrial fibrillation. Eur Heart J. 2005;26:2083–92.PubMedCrossRefGoogle Scholar
  99. 99.
    Liu T, Li G, Li L, Korantzopoulos P. Association between C-reactive protein and recurrence of atrial fibrillation after successful electrical cardioversion: a meta-analysis. J Am Coll Cardiol. 2007;49:1642–8.PubMedCrossRefGoogle Scholar
  100. 100.
    Guo Y, Lip GY, Apostolakis S. Inflammation in atrial fibrillation. J Am Coll Cardiol. 2012;60:2263–70.PubMedCrossRefGoogle Scholar
  101. 101.
    Corrao S, Messina S, Pistone G, et al. Heart involvement in rheumatoid arthritis: systematic review and meta-analysis. Int J Cardiol. 2013;167:2031–8.PubMedCrossRefGoogle Scholar
  102. 102.
    Kim SC, Liu J, Solomon DH. The risk of atrial fibrillation in patients with rheumatoid arthritis. Ann Rheum Dis. 2014;73:1091–5.PubMedCentralPubMedCrossRefGoogle Scholar
  103. 103.
    Lindhardsen J, Ahlehoff O, Gislason GH, et al. Risk of atrial fibrillation and stroke in rheumatoid arthritis: Danish nationwide cohort study. BMJ. 2012;344:e1257.PubMedCentralPubMedCrossRefGoogle Scholar
  104. 104.
    Bacani AK, Crowson CS, Roger VL et al. Increased incidence of atrial fibrillation in patients with rheumatoid arthritis. Biomed Res Int 2015; 2015:809514.Google Scholar
  105. 105.
    Ando Y, Kai S, Uyama E, et al. Involvement of the central nervous system in rheumatoid arthritis: its clinical manifestations and analysis by magnetic resonance imaging. Intern Med. 1995;34:188–91.PubMedCrossRefGoogle Scholar
  106. 106.
    Watts RA, Mooney J, Lane SE, Scott DG. Rheumatoid vasculitis: becoming extinct? Rheumatology (Oxford). 2004;43:920–3.CrossRefGoogle Scholar
  107. 107.
    Caballol Pons N, Montala N, Valverde J, et al. Isolated cerebral vasculitis associated with rheumatoid arthritis. Joint Bone Spine. 2010;77:361–3.PubMedCrossRefGoogle Scholar
  108. 108.
    Solomon DH, Curtis JR, Saag KG, et al. Cardiovascular risk in rheumatoid arthritis: comparing TNF-alpha blockade with nonbiologic DMARDs. Am J Med. 2013;126(730):e739–17.Google Scholar
  109. 109.
    Scott DG, Bacon PA. Intravenous cyclophosphamide plus methylprednisolone in treatment of systemic rheumatoid vasculitis. Am J Med. 1984;76:377–84.PubMedCrossRefGoogle Scholar
  110. 110.
    Makol A, Matteson EL, Warrington KJ. Rheumatoid vasculitis: an update. Curr Opin Rheumatol. 2015;27:63–70.PubMedCrossRefGoogle Scholar
  111. 111.
    Stone JH, Merkel PA, Spiera R, et al. Rituximab versus cyclophosphamide for ANCA-associated vasculitis. N Engl J Med. 2010;363:221–32.PubMedCentralPubMedCrossRefGoogle Scholar
  112. 112.
    Jarrett SJ, Cunnane G, Conaghan PG, et al. Anti-tumor necrosis factor-alpha therapy-induced vasculitis: case series. J Rheumatol. 2003;30:2287–91.PubMedGoogle Scholar
  113. 113.
    Sokumbi O, Wetter DA, Makol A, Warrington KJ. Vasculitis associated with tumor necrosis factor-alpha inhibitors. Mayo Clin Proc. 2012;87:739–45.PubMedCentralPubMedCrossRefGoogle Scholar
  114. 114.
    Agarwal AK, Peppelman Jr WC, Kraus DR, Eisenbeis Jr CH. The cervical spine in rheumatoid arthritis. BMJ. 1993;306:79–80.PubMedCentralPubMedCrossRefGoogle Scholar
  115. 115.
    Blom M, Creemers MC, Kievit W, et al. Long-term follow-up of the cervical spine with conventional radiographs in patients with rheumatoid arthritis. Scand J Rheumatol. 2013;42:281–8.PubMedCrossRefGoogle Scholar
  116. 116.
    Yurube T, Sumi M, Nishida K, et al. Incidence and aggravation of cervical spine instabilities in rheumatoid arthritis: a prospective minimum 5-year follow-up study of patients initially without cervical involvement. Spine (Phila Pa 1976). 2012;37:2136–44.CrossRefGoogle Scholar
  117. 117.
    Ahn JK, Hwang JW, Oh JM, et al. Risk factors for development and progression of atlantoaxial subluxation in Korean patients with rheumatoid arthritis. Rheumatol Int. 2011;31:1363–8.PubMedCrossRefGoogle Scholar
  118. 118.
    Garg A, Gaikwad SB, Kanodia A, et al. Positional occlusion/stasis of vertebral arteries in a case of cervical rheumatoid arthritis presenting with multiple posterior circulation infarcts: a case report with angiographic demonstration. Spine (Phila Pa 1976). 2004;29:E321–325.CrossRefGoogle Scholar
  119. 119.
    Jones MW, Kaufmann JC. Vertebrobasilar artery insufficiency in rheumatoid atlantoaxial subluxation. J Neurol Neurosurg Psychiatry. 1976;39:122–8.PubMedCentralPubMedCrossRefGoogle Scholar
  120. 120.
    Webb FW, Hickman JA, Brew DS. Death from vertebral artery thrombosis in rheumatoid arthritis. Br Med J. 1968;2:537–8.PubMedCentralPubMedCrossRefGoogle Scholar
  121. 121.
    Kuether TA, Nesbit GM, Clark WM, Barnwell SL. Rotational vertebral artery occlusion: a mechanism of vertebrobasilar insufficiency. Neurosurgery. 1997;41:427–32. discussion 432-423.PubMedCrossRefGoogle Scholar
  122. 122.
    Takeshima Y, Matsuda R, Hironaka Y, et al. Rheumatoid arthritis-induced lateral atlantoaxial subluxation with multiple vertebrobasilar infarctions. Spine (Phila Pa 1976). 2015;40:E186–189.CrossRefGoogle Scholar
  123. 123.
    Kauppi MJ, Neva MH, Laiho K, et al. Rheumatoid atlantoaxial subluxation can be prevented by intensive use of traditional disease modifying antirheumatic drugs. J Rheumatol. 2009;36:273–8.PubMedCrossRefGoogle Scholar
  124. 124.
    Casey AT, Crockard HA, Bland JM, et al. Predictors of outcome in the quadriparetic nonambulatory myelopathic patient with rheumatoid arthritis: a prospective study of 55 surgically treated Ranawat class IIIb patients. J Neurosurg. 1996;85:574–81.PubMedCrossRefGoogle Scholar
  125. 125.
    Pellicci PM, Ranawat CS, Tsairis P, Bryan WJ. A prospective study of the progression of rheumatoid arthritis of the cervical spine. J Bone Joint Surg Am. 1981;63:342–50.PubMedGoogle Scholar
  126. 126.
    Miyamoto H, Sumi M, Uno K. Outcome of surgery for rheumatoid cervical spine at one institute over three decades. Spine J. 2013;13:1477–84.PubMedCrossRefGoogle Scholar
  127. 127.
    Alghasham A, Rasheed Z. Therapeutic targets for rheumatoid arthritis: progress and promises. Autoimmunity. 2014;47:77–94.PubMedCrossRefGoogle Scholar
  128. 128.
    Pyne D, Ehrenstein M, Morris V. The therapeutic uses of intravenous immunoglobulins in autoimmune rheumatic diseases. Rheumatology (Oxford). 2002;41:367–74.CrossRefGoogle Scholar
  129. 129.
    Katz U, Shoenfeld Y, Zandman-Goddard G. Update on intravenous immunoglobulins (IVIg) mechanisms of action and off-label use in autoimmune diseases. Curr Pharm Des. 2011;17:3166–75.PubMedCrossRefGoogle Scholar
  130. 130.
    Katz-Agranov N, Khattri S, Zandman-Goddard G. The role of intravenous immunoglobulins in the treatment of rheumatoid arthritis. Autoimmun Rev. 2015;14:651–8.PubMedCrossRefGoogle Scholar
  131. 131.
    Tani C, D'Aniello D, Delle Sedie A, et al. Rhupus syndrome: assessment of its prevalence and its clinical and instrumental characteristics in a prospective cohort of 103 SLE patients. Autoimmun Rev. 2013;12:537–41.PubMedCrossRefGoogle Scholar
  132. 132.
    Eriksson C, Engstrand S, Sundqvist KG, Rantapaa-Dahlqvist S. Autoantibody formation in patients with rheumatoid arthritis treated with anti-TNF alpha. Ann Rheum Dis. 2005;64:403–7.PubMedCentralPubMedCrossRefGoogle Scholar
  133. 133.
    Costa MF, Said NR, Zimmermann B. Drug-induced lupus due to anti-tumor necrosis factor alpha agents. Semin Arthritis Rheum. 2008;37:381–7.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Alicia M. Zha
    • 1
  • Mario Di Napoli
    • 2
    • 3
  • Réza Behrouz
    • 4
  1. 1.Department of NeurologyThe Ohio State University College of MedicineColumbusUSA
  2. 2.Neurological ServiceSan Camillo de’ Lellis General HospitalRietiItaly
  3. 3.SMDN-Neurological SectionCentre for Cardiovascular Medicine and Cerebrovascular Disease PreventionSulmonaItaly
  4. 4.Department of Neurology, School of MedicineUniversity of Texas Health Science Center San Antonio, Medical Arts and Research CenterSan AntonioUSA

Personalised recommendations