Pathogenesis of atherosclerosis in rheumatoid arthritis

Main Article Content

Joko Rilo Pambudi
Harry Isbagio

Abstract

Increased morbidity and mortality in patients with rheumatoid arthritis (RA) is largely associated with cardiovascular disease. In this case, the factors that play a role is chronic inflammation. A chronic inflammatory associated with condition which accelerate atherosclerosis and increased cardiovascular morbidity and mortality. Inflammatory and atherogenic mediators have a role in pathogenesis of RA and atherosclerosis. Atherogenesis in RA start when cytokines from the inflamed synovial tissue are released into the systemic circulation. Circulating cytokines affects the function of other tissues such as adipose tissue, skeletal muscle, liver and vascular endothelium that would lead to proatherogenic transformation process such as insulin resistance, prothrombotic effects, pro-oxidative stress and endothelial dysfunction. Size, weight and durationof systemic inflammatory response in RA are the most important factor causing damage. IMT (Intima Media Thickness) measurement on common carotid arteries byB-mode ultrasound is a rapid non-invasive examination of the structural anatomy, reproducible and relatively low risks that are advantageous for assessing therisk of cardiovascular disease and monitoring disease progression.

Article Details

How to Cite
Pambudi, J., & Isbagio, H. (2018). Pathogenesis of atherosclerosis in rheumatoid arthritis. Indonesian Journal of Rheumatology, 5(1). https://doi.org/10.37275/ijr.v5i1.46
Section
Review Article

References

1. Sattar N, McInnes IB. Atherosclerosis in rheumatoid arthritis. In: Firestein GS, Budd RC, Jr. EDH, editors. Kellys’Textbook of Rheumatology. 8 ed. Philadelphia: Saunders Elsevier; 2008, p421-31.
2. Gabriel SE, Crowson CS, Kremers HM, Doran MF, Turesson C, O’Fallon WM, et al. Survival in rheumatoid arthritis: a population-based analysis of trends over 40 years. Arthritis & Rheumatism. 2003;48(1):54-8.
3. Solomon DH, Karlson EW, Rimm EB, al. e. Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis. Circulation. 2003;107:1303-07.
4. Maradit-Kremers H, Nicola PJ, Crowson CS, Ballman KV, Gabriel SE. Cardiovascular death in rheumatoid arthritis: a population-based study. Arthritis & Rheumatism. 2005;52(3):722-32.
5. del Rincon I, 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 & Rheumatism.2001;44:9.
6. Wallberg-Jonsson S, Ohman ML, Rantapaa-Dahlqvist S. Cardiovascular morbidity and mortality in patient with seropositive rheumatoid arthritis in Northern Sweden. J Rheumatol. 1997;24:445-51.
7. Turesson C, Jarenros A, Jacobsson LT. Increase incidence of cardiovascular diseases in patient with rheumatoid arthritis. Annals of the rheumatic diseases. 2004;63:952-55.
8. Watson DJ, Rhodes T, HA. G. 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- 02.
9. Goodson NJ, Wiles NJ, Lunt M, Barrett EM, Silman AJ, Symmons DP. Mortality in early inflammatory polyarthritis: cardiovascular mortality is increased in seropositive patients. Arthritis & Rheumatism. 2002;46(8):2010-9.
10. van Halm VP, Peters MJ, Voskuyl AE, Boers M, Lems WF, Visser M, et al. Rheumatoid arthritis versus diabetes as a risk factor for cardiovascular disease: a cross-sectional study, the CARRE Investigation. Annals of the rheumatic diseases. 2009;68(9):1395-400.
11. Van Doornum S, Jennings GLR, Wicks IP. Reducing the cardiovascular disease burden in rheumatoid arthritis. MJA 2006;184(6):287-90.
12. Solomon DH, Goodson NJ, Katz JN, Weinblatt ME, Avorn J, Setoguchi S, et al. Patterns of cardiovascular risk in rheumatoid arthritis. Annals of the rheumatic diseases. 2006;65(12):1608-12.
13. Fischer LM, Schlienger RG, Matter C, Jick H, Meier CR. Effect of rheumatoid arthritis or systemic lupus erythematosus on the risk of firsttime acute myocardial infarction. The American Journal of Cardiology. 2004;93:198-200.
14. Turesson C, McClelland RL, Christianson TJ, Matteson EL. Severe extraarticular disease manifestations are associated with an increased risk of first ever cardiovascular events in patients with rheumatoid arthritis.Annals of the rheumatic diseases. 2007;66(1):70-5.
15. Libby P. Inflammation in atherosclerosis. NATURE. 2002;420(19):868-74.
16. Gabriel SE. Why do people with rheumatoid arthritis still die prematurely? Annals of the rheumatic diseases. 2008;67 Suppl 3:iii30-4.
17. Choi HK, Hernán MA, Seeger JD, Robins JM, Wolfe F. Methotrexate and mortality in patients with rheumatoid arthritis: a prospective study. The Lancet. 2002;359 (9313): 1173-7.
18. Krishnan E, Lingala VB, Singh G. Declines in mortality from acute myocardial infarction in successive incidence and birth cohorts of patients with rheumatoid arthritis. Circulation. 2004;110:1774-79.
19. Maradit-Kremers H. Safety, efficacy, and mortality in a long-term cohort of patients with rheumatoid arthritis taking methotrexate: followup after a mean of 13.3 years. Arthritis & Rheumatism. 1997;40(5):984-85.
20. Sherer Y, Shoenfeld Y. Mechanisms of disease: atherosclerosis in autoimmune diseases. Nature clinical practice Rheumatology. 2006;2(2):99-106.
21. Doria A, Sherer Y, Meroni PL, Shoenfeld Y. Inflammation and accelerated atherosclerosis: Basic mechanisms. Rheum Dis Clin N Am. 2005;31:355-62.
22. Ross R. Atherosclerosis — an inflammatory disease. The New England Journal of Medicine. 1999;340(2):115-26.
23. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-95.
24. Hollan I, Scott H, Saatvedt K, Prayson R, Mikkelsen K, Nossent HC, et al. Inflammatory rheumatic disease and smoking are predictors of aortic inflammation: a controlled study of biopsy specimens obtained at coronary artery surgery. Arthritis and rheumatism. 2007;56(6):2072-9.Epub 2007/05/29.
25. Szekanecz Z, Kerekes G, Der H, Sandor Z, Szabo Z, Vegvari A, et al. Accelerated atherosclerosis in rheumatoid arthritis. Annals of the New York Academy of Sciences. 2007;1108(1):349-58.
26. Shoenfeld Y, Gerli R, Doria A, Matsuura E, Cerinic MM, Ronda N, et al. Accelerated atherosclerosis in autoimmune rheumatic diseases. Circulation. 2005;112(21):3337-47.
27. Van Doornum S, McColl G, Wicks IP. Accelerated atherosclerosis: an extraarticular feature of rheumatoid arthritis? Arthritis & Rheumatism.2002;46(4):862-73.
28. Pearson TA, Mensah GA, Alexander RW, al. e. Markers of inflammation and cardiovascular disease: application to clinical and public healthpractice: a statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation. 2003;107:499-511.
29. Pasceri V, Yeh ETH. A Tale of two diseases: atherosclerosis and rheumatoid arthritis. Circulation. 1999;100(21):2124-6.
30. Sattar N, McCarey DW, Capell H, McInnes IB. Explaining how “highgrade” systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation. 2003;108 (24):2957-63.
31. McEntegart A, Capell HA, Creran D, Rumley A, Woodward M, Lowe GDO. Cardiovascular risk factors, including thrombotic variables, in a population with rheumatoid arthritis. Rheumatology. 2001;40:640-44.
32. Turesson C, Jarenros A, Jacobsson LT. Endothelial expression of MHC class II molecules in autoimmune disease. Curr Pharm Dis. 2004;10:129-43.
33. Vallbracht KB, Schwimmbeck PL, Seeberg B, al. e. Endothelial dysfunction of peripheral arteries in patients with immunohistologically confirmed myocardial inflammation correlates with endothelial expression of human leukocyte antigens and adhesion molecules in myocardial biopsies. Journal of the American College of Cardiology. 2002;40:515-20.
34. Turesson C, Jacobsson LTH, Matteson EL. Cardiovascular co-morbidity in rheumatic diseases. Vascular Health and Risk Management.2008;4(3):605-14.
35. Michel JJ, Turesson C, Lemster B, al. e. CD57-expressing T cells that have senescent features are expanded in rheumatoid arthritis. Arthritis &Rheumatism. 2007(56):43-57.
36. Liuzzo G, Kopecky SL, Frye RL, al. e. Pertubation of the T-cell repertoire in patients with unstable angina. Circulation. 1999;100:2135-39.
37. Liuzzo G, Goronzy JJ, Yang H, al. e. Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes. Circulation.2000;101:2883-88.
38. Gerli R, Schillaci G, Giordano A, Bocci EB, Bistoni O, Vaudo G, et al.CD4+CD28- T lymphocytes contribute to early atherosclerotic damage in rheumatoid arthritis patients. Circulation. 2004;109(22):2744-8.
39. Wolfe F, Michaud K, Gefeller O, Choi HK. Predicting mortality in patients with rheumatoid arthritis. Arthritis & Rheumatism. 2003;48(6):1530-42.
40. Young A, Koduri G, Batley M, Kulinskaya E, Gough A, Norton S, et al. Mortality in rheumatoid arthritis. Increased in the early course of disease, in ischaemic heart disease and in pulmonary fibrosis. Rheumatology. 2007;46(2):350-7.
41. Kumeda Y, Inaba M, Goto H, Nagata M, Henmi Y, Furumitsu Y, et al. Increased thickness of the arterial intima-media detected by ultrasonography in patients with rheumatoid arthritis. Arthritis & Rheumatism. 2002;46(6):1489-97.
42. Thomson W, Harrison Be, Ollier B, Wiles N, Payton T, Barrett J, et al. Quantifying the exact role of hla–drb1 alleles in susceptibility to inflammatory polyarthritis. Arthritis & Rheumatism. 1999;42(4):757-62.
43. Hinks A, Barton A, John S, Bruce I, Hawkins C, Griffiths CE, et al. Association between the PTPN22 gene and rheumatoid arthritis and juvenile idiopathic arthritis in a UK population: further support that PTPN22 is an autoimmunity gene. Arthritis and rheumatism. 2005;52(6):1694-9.
44. Gorman JD, Lum RF, Chen JJ, Suarez-Almazor ME, Thomson G, Criswell LA. Impact of shared epitope genotype and ethnicity on erosive disease: a meta-analysis of 3,240 rheumatoid arthritis patients. Arthritis & Rheumatism. 2004;50(2):400-12.
45. Harrison B, Thomson W, Symmons D, Ollier B, Wiles N, Payton T, et al. The influence of HLA–DRB1 alleles and rheumatoid factor on disease outcome in an inception cohort of patients with early inflammatory arthritis. Arthritis & Rheumatism. 1999;42(10) :2174-83.
46. Farragher TM, Goodson NJ, Naseem H, Silman AJ, Thomson W, Symmons D, et al. Association of the HLA-DRB1 gene with premature death, particularly from cardiovascular disease, in patients with rheumatoid arthritis and inflammatory polyarthritis. Arthritis & Rheumatism. 2008;58(2):359-69.
47. Silman AJ, Newman J, MacGregor AJ. Cigarette smoking increases the risk of rheumatoid arthritis. Result from a nationwide study of diseasediscordant twins. Arthritis & Rheumatism. 1996;39:732-5.
48. Goodson NJ, Silman AJ, Pattison DJ, Lunt M, Bunn D, Luben R, et al. Traditional cardiovascular risk factors measured prior to the onset of inflammatory polyarthritis. Rheumatology. 2004;43(6):731-6.
49. Hutchinson D. Heavy cigarette smoking is strongly associated with rheumatoid arthritis (RA), particularly in patients without a family history of RA. Annals of the rheumatic diseases. 2001;60(3):223-7.
50. Klareskog L, Padyukov L, Lorentzen J, Alfredsson L. Mechanism of disease: Genetic susceptibility and environmental triggers in the development of rheumatoid arthritis Nature clinical practice Rheumatology. 2006;2:425- 33.
51. Homma S, Hirose N, Ishida H, Ishii T, Araki G, Halsey JH. Carotid plaque and intima-media thickness assessed by B-mode ultrasonography in subjects ranging From young adults to centenarians editorial comment.Stroke. 2001;32(4):830-5.
52. del Rincon I, O’Leary DH, Freeman GL, Escalante A. Acceleration of atherosclerosis during the course of rheumatoid arthritis. Atherosclerosis. 2007;195(2):354-60.
53. Liang KP, Liang KV, Matteson EL, McClelland RL, Christianson TJ, Turesson C. Incidence of noncardiac vascular disease in rheumatoid arthritis and relationship to extraarticular disease manifestations. Arthritis and rheumatism. 2006;54(2):642-8.
54. Chae CU, Lee RT, Rifai N, Ridker PM. Blood pressure and inflammation in apparently healthy men. Hypertension. 2001;38(3):399-403.
55. Panoulas VF, Douglas KM, Smith JP, Stavropoulos-Kalinoglou A, Metsios GS, Nightingale P, et al. Transforming growth factor-beta1 869T/C, but not interleukin-6 -174G/C, polymorphism associates with hypertension in rheumatoid arthritis. Rheumatology. 2009;48(2):113-8.
56. van Halm VP, Nielen MM, Nurmohamed MT, van Schaardenburg D, Reesink HW, Voskuyl AE, et al. Lipids and inflammation: serial measurements of the lipid profile of blood donors who later developed rheumatoid arthritis. Annals of the rheumatic diseases. 2007;66(2):184-8.
57. Chung CP, Oeser A, Solus JF, Gebretsadik T, Shintani A, Avalos I, et al. Inflammation-associated insulin resistance: differential effects in rheumatoid arthritis and systemic lupus erythematosus define potential mechanisms. Arthritis & Rheumatism. 2008;58(7):2105-12.
58. Rizzo M, Spinas GA, Cesur M, Ozbalkan Z, Rini GB, Berneis K. Atherogenic lipoprotein phenotype and LDL size and subclasses in drug-naive patients with early rheumatoid arthritis. Atherosclerosis. 2009;207(2):502-6.
59. Gonzalez-Gay MA, Gonzalez-Juanatey C, Martin J. Rheumatoid arthritis: a disease associated with accelerated atherogenesis. Seminars in arthritis and rheumatism. 2005;35(1):8-17.
60. Fukuzawa M, Satoh J, Qiang X, Miyaguchi S, Sakata Y, Nakazawa T, et al. Inhibition of tumor necrosis factor-a with anti-diabetic agents. Diabetes Research and Clinical Practice. 1999;43:147-54.
61. Hotamisligil GS, Peraldi P, Budavari A, Ellis R, White MF, Spielgelman BM. IRS-1-mediated inhibition of insulin receptor tyrosine kinase activity in TNF-$\alpha$-and obesity-induced insulin resistance. Science. 1996;271(5249):665-68.
62. Zwaka TP, Hombach V, Torzewski J. C-reactive protein-mediated low density lipoprotein uptake by macrophages: implications for atherosclerosis. Circulation. 2001;103(9):1194-7.
63. Blake GJ, Ridker PM. Novel clinical markers of vascular wall inflammation. Circulation research. 2001;89(9):763-71.
64. Danesh J, Wheeler JG, Hirschfield GM, Eda S, Eiriksdottir G, Rumley AnPD, et al. C-reactive protein and other circulating markers of inflammation in the prediction of coronary heart disease. N Engl J Med. 2004;350:1387- 97.
65. Goodson NJ, Symmons DP, Scott DG, Bunn D, Lunt M, Silman AJ. Baselinelevels of C-reactive protein and prediction of death from cardiovascular disease in patients with inflammatory polyarthritis: a ten-year followup study of a primary care-based inception cohort. Arthritis & Rheumatism.2005;52(8):2293-9.
66. Maradit-Kremers H, Nicola PJ, Crowson CS, Ballman KV, Gabriel SE. Prognostic importance of low body mass index in relation to cardiovascular mortality in rheumatoid arthritis. Arthritis & Rheumatism. 2004;50(11):3450-7.
67. Escalante A, Haas RW, del Rincón I. Paradoxical effect of body mass index on survival in rheumatoid arthritis. Arch Intern Med. 2005;165:6.
68. Mewar D, Coote A, Moore DJ, Marinou I, Keyworth J, Dickson MC, et al. Independent associations of anti-cyclic citrullinated peptide antibodies and rheumatoid factor with radiographic severity of rheumatoid arthritis.
Arthritis research & therapy. 2006;8(4):R128.
69. Del Val Del Amo N, Bosch RI, Manteca CF, Polo RG, Cortina EL. Anticyclic citrullinated peptide antibody in rheumatoid arthritis- relation with disease aggressiveness. Clinical and Experimental Rheumatology. 2006;24:281-6.
70. Lopez-Longo FJ, Oliver-Minarro D, de la Torre I, Gonzalez-Diaz de Rabago E, Sanchez-Ramon S, Rodriguez-Mahou M, et al. Association between anti-cyclic citrullinated peptide antibodies and ischemic heart disease in patients with rheumatoid arthritis. Arthritis and rheumatism.2009;61(4):419-24.
71. Maggi E, Chiesa R, Melissano G, Castellano R, Astore D, Grossi A, et al. LDL oxidation in patients with severe carotid atherosclerosis. A study of in vitro and in vivo oxidation markers. Arteriosclerosis, thrombosis, and vascular biology. 1994;14(12):1892-9.
72. Lehtimaki T, Lehtinen S, Solakivi T, Nikkila M, Jaakkola O, Jokela H, et al. Autoantibodies against oxidized low density lipoprotein in patients with angiographically verified coronary artery disease. Arteriosclerosis, thrombosis, and vascular biology. 1999;19(1):23-7.
73. Sherer Y, Gerli R, Vaudo G, Schillaci G, Gilburd B, Giordano A, et al. Prevalence of antiphospholipid and antioxidized low-density lipoprotein antibodies in rheumatoid arthritis. Ann N Y Acad Sci. 2005;1051:299-303.
74. Grignani G, Maiolo A. Cytokines and hemostasis. Haematologica. 2000;85:967-72.
75. Gonzalez-Gay MA, Gonzalez-Juanatey C, Vazquez-Rodriguez TR, Martin J, Llorca J. Endothelial dysfunction, carotid intima-media thickness, andaccelerated atherosclerosis in rheumatoid arthritis. Seminars in arthritis and rheumatism. 2008;38(2):67-70.
76. O’Leary DH, Bots ML. Imaging of atherosclerosis: carotid intima-media thickness. Eur Heart J. 2010;31(14):1682-9.
77. Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M. Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation. 2007;115(4):459-67.
78. Pignoli P, Tremoli E, Poli A, Oreste P, Paoletti R. Intimal plus medial thickness of the arterial wall: a direct measurement with ultrasound imaging. Circulation. 1986;74(6):1399-406.
79. Salonen JT, Salonen R. Ultrasonographically assessed carotid morphology and the risk of coronary heart disease. Arteriosclerosis, thrombosis, and vascular biology. 1991;11(5):1245-9.
80. Nair SB, Malik R, Khattar RS. Carotid intima-media thickness: ultrasound measurement, prognostic value and role in clinical practice. Postgraduate medical journal. 2012;88(1046):694-9.
81. Veller MG, Fisher CM, Nicolaides AN, Renton SN, Geroulakos GN, Stafford NJ, et al. Measurement of the ultrasonic intima-media complex thickness in normal subjects. Journal of Vascular Surgery. 1993;17(4):719-25.
82. Belcaro G, A.N. N, Ramaswami G, Cesarone MR, De Sanctis M, Incandela L, et al. Carotid and femoral ultrasound morphology screening and cardiovascular events in low risk subjects: a 10-year follow-up study (the CAFES-CAVE study). Atherosclerosis. 2001;156:9.
83. Mancia G, Fagard R, Narkiewicz K, Redon J, Zanchetti A, Bohm M, et al. 2013 ESH”ESC Guideline for the mangement of arterial hypertension. European Heart Journal 2013.
84. Park YB, Ahn CW, Choi HK, Lee SH, In BH, Lee HC, et al. Atherosclerosis in rheumatoid arthritis: morphologic evidence obtained by carotid ultrasound. Arthritis & Rheumatism. 2002;46(7):1714-9.
85. Roman MJ, Moeller E, Davis A, Paget SA, Crow MK, Lockshin MD, et al. Preclinical carotid atherosclerosis in patients with rheumatoid arthritis. Annal s of Internal Medicine. 2006;144(4):249-56.
86. Gonzalez-Juanatey C, Llorca J, Martin J, Gonzalez-Gay MA. Carotid intima-media thickness predicts the development of cardiovascular events in patients with rheumatoid arthritis. Seminars in ar thritis and rheumatism. 2009;38(5):366-71.
87. Gonzalez-Juanatey C, Llorca J, Testa A, Revuelta J, Garcia-Porrua C, Gonzalez-Gay MA. Increased prevalence of severe subclinical atherosclerotic findings in long-term treated rheumatoid arthritis patients without clinically evident atheroscler otic disease. Medicine. 2003;82(6):407-13.
88. Evans MR, Escalante A, Battafarano DF, Freeman GL, O’Leary DH, del Rincon I. Carotid atherosclerosis predicts incident acute coronary syndromes in rheumatoid arthritis. Arthritis & Rheumatism. 2011;63(5):1211-20.