Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub. 2014, 158(3):404-411 | DOI: 10.5507/bp.2013.054

Intima media thickness measurement as a marker of subclinical atherosclerosis in SLE patient

Andrea Smrzovaa, Pavel Horaka, Martina Skacelovaa, Zuzana Hermanovab, Katerina Langovac, Josef Zadrazila, Dalibor Novotnyd
a Department of Internal Medicine III - Nephrology, Rheumatology, Endocrinology, Faculty of Medicine and Dentistry, Palacky University Olomouc, Czech Republic
b Department of Immunology, Faculty of Medicine and Dentistry, Palacky University Olomouc
c Department of Medical Biophysics, Faculty of Medicine and Dentistry, Palacky University Olomouc
d Department of Cinical Biochemistry, University Hospital Olomouc

Aim: Accelerated atherosclerosis in systemic lupus erythematosus (SLE) is an important cause of morbidity and mortality. The pathophysiology of accelerated atherosclerosis in SLE is mediated by factors such as inflammatory processes in the vascular wall, specific antibodies, dyslipoproteinemia, endothelial dysfunction and the high prevalence of traditional risk factors for cardiovascular diseases. In this context, we evaluated the clinical significance of ultrasound examination of the carotic arteries in the early diagnosis of atherosclerosis.

Methods: The study included 63 patients with SLE (female: male 53:10, mean age 38.4±12.7 years, mean disease duration 143.0 ±82.6 months), 24 patients had lupus nephritis. The control group consisted of 24 volunteers (female: male 20:4 mean age 31.04±8.59). Intima media thickness (IMT) was measured by ultrasound on both sides. The results were correlated with markers of lipid spectrum, anti-dsDNA, antinucleosomal and anticardiolipin antibodies, lupus anticoagulant and complement components. Clinical disease activity and damage were evaluated by SLEDAI and SLICC indices. Lifestyle and other important factors were examined per protocol and by questionnaire.

Results: A significant difference of IMT (P≤0.03) was found between the lupus patients and sex-age adjusted healthy controls with an in mean IMT in SLE patients of 0.569±0.11 mm, in control group 0.495±0.05 mm. A significant correlation between IMT and disease duration, age, positivity of lupus anticoagulant, use of ACE inhibitors, glomerular filtration and serum creatinine were found. No difference in IMT was found between patients with or without lupus nephritis.

Conclusion: IMT measurement could be used as a clinical predictor of risk of accelerated atherosclerosis in lupus patients.

Keywords: systemic lupus erythematodes, atherosclerosis, intima media thickness

Received: December 11, 2012; Accepted: July 8, 2013; Prepublished online: July 29, 2013; Published: September 30, 2014  Show citation

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Smrzova, A., Horak, P., Skacelova, M., Hermanova, Z., Langova, K., Zadrazil, J., & Novotny, D. (2014). Intima media thickness measurement as a marker of subclinical atherosclerosis in SLE patient. Biomedical papers158(3), 404-411. doi: 10.5507/bp.2013.054
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References

  1. Bulkley BH, Roberts WC. The heart in systemic lupus erythematosus and the changes induced in it by corticosteroid therapy. A study of 36 necropsies patients. Am J Med 1975;58:243-64. Go to original source... Go to PubMed...
  2. 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. Go to original source... Go to PubMed...
  3. Borchers AT, Keen CL, Shoenfeld Y, Gershwin ME. Surviving the butterfly and the wolf: mortality trends in systemic lupus erythematosus. Autoimmun Rev 2004;3:423-53. Go to original source... Go to PubMed...
  4. Manzi S, Meilahn EN, Rairie JE, Conte CG, Medsger TA Jr, Jansen-McWilliams L, D'Agostino RB, Kuller LH. Age-specific incidence rates of myocardial infarction and angina in women with systemic lupus erythematosus: comparison with the Framingham Study. Am J Epidemiol 1997;145:408-15. Go to original source... Go to PubMed...
  5. Asanuma Y, Oeser A, Shintani AK, Turner E, Olsen N, Fazio S, Linton MF, Raggi P, Stein CM. Premature coronary-artery atherosclerosis in systemic lupus erythematosus. N Engl J Med 2004;350:1571-5. Go to original source...
  6. Esdaile JM, Abrahamowicz M, Grodzicky T, Li Y, Panaritis C, du Berger R, Côte R, Grover SA, Fortin PR, Clarke AE, Senécal JL. Traditional Framingham risk factors fail to fully account for accelerated atherosclerosis in systemic lupus erythematosus. Arthritis Rheum 2001;44:2331-7. Go to original source... Go to PubMed...
  7. Fischer LM, Schlienger RG, Matter C, Jick H, Meier CR. Effect of rheumatoid arthritis or systemic lupus erythematosus on the risk of first-time acute myocardial infarction. Am J Cardiol 2004;93:198-200. Go to original source... Go to PubMed...
  8. Bruce IN, Gladman DD, Urowitz MB. Premature atherosclerosis in systemic lupus erythematosus. Rheum Dis Clin North Ann 2000;26:257-78. Go to original source... Go to PubMed...
  9. Manzi S, Wasko MC. Inflammation-mediated rheumatic diseases and atherosclerosis. Ann Rheum Dis 2000;59:321-5. Go to original source... Go to PubMed...
  10. Tan EM, Cohen AS, Fries JF, Masi AT, McShane DJ, Rothfield NF, Schaller JG, Talal N, Winchester RJ. The 1982 revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 1982;25:1271-7. Go to original source... Go to PubMed...
  11. Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH. Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 1992;35:630-40. Go to original source... Go to PubMed...
  12. Gladman DD, Urowitz MB. The SLICC/ACR damage index: progress report and experience in the field. Lupus 1999;8:632-7. Go to original source... Go to PubMed...
  13. Touboul PJ, Hennerici MG, Meairs S, Adams H, Amarenco P, Desvarieux M, Ebrahim S, Fatar M, Hernandez Hernandez R, Kownator S, Prati P, Rundek T, Taylor A, Bornstein N, Csiba L, Vicaut E, Woo KS, Zannad F. Mannheim intima - media thickness consensus. Cerebrovasc Dis 2004;18:246-9. Go to original source... Go to PubMed...
  14. Vaverková H, Soska V, Rosolová H, Ceska R, Cífková R, Freiberger T, Pit'ha J, Poledne R, Stulc T, Urbanová Z, Vráblík M. Czech atherosclerosis society guidelines for the diagnosis and treatment of dyslipidemia in adults. Cas Lek Cesk 2007;146:2-15.
  15. Weening JJ, D'Agati VD, Schwartz MM, Seshan SV, Alpers CE, Appel GB, Balow JE, Bruijn JA, Cook T, Ferrario F, Fogo AB, Ginzler EM, Hebert L, Hill G, Hill P, Jennette JC, Kong NC, Lesavre P, Lockshin M, Looi LM, Makino H, Moura LA, Nagata M. International Society of Nephrology Working Group on the Classification of Lupus Nephritis, Renal Pathology Society Working Group on the Classification of Lupus Nephritis The classification of glomerulonephritis in systemic lupus erythematosus revisited. Kidney Int 2004;65:521-30. Go to original source... Go to PubMed...
  16. Almdal T, Scharling H, Jensen JS, Vestergaard H. The independent effect of type 2 diabetes mellitus on ischemic heart disease, stroke, and death. Arch Intern Med 2004;164:1422-6. Go to original source... Go to PubMed...
  17. Chanson P, Salenave S. Metabolic syndrome in Cushing's syndrome. Neuroendocrinology 2010;92, Suppl 1:96-101. Go to original source... Go to PubMed...
  18. Horcicka V, Zadrazil J, Karasek D, Al Jabry S, Krejci K, Strebl P, Halenka M, Elfmark M. Significance of HLA nondependent risk factors of chronic transplant nephropathy for the development of endothelial dysfunction after kidney transplantation. Transplant Proc 2009;41:1599-603. Go to original source... Go to PubMed...
  19. Dobmeyer J, Lohrmann J, Feussner G. Prevalence and association of atherosclerosis at three different arterial sites in patients with type III hyperlipoproteinemia. Atherosclerosis 1996;119:89-98. Go to original source... Go to PubMed...
  20. Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, Mejía JC, Aydintug AO, Chwalinska-Sadowska H, de Ramón E, Fernández-Nebro A, Galeazzi M, Valen M, Mathieu A, Houssiau F, Caro N, Alba P, Ramos-Casals M, Ingelmo M, Hughes GR. Morbidity and mortality in systemic lupus erythematosus during a 10-year period: a comparison of early and late manifestations in a cohort of 1,000 patients. Medicine (Baltimore) 2003;82:299-308. Go to original source... Go to PubMed...
  21. Maksimowcz-McKinnon K, Manzi S. Cardiovascular Manifestations of Lupus. In: Wallace JD, Hahn BH. Dubois' Lupus erythematosus: Philadelphia; 2007. p. 670-1.
  22. 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. Go to original source... Go to PubMed...
  23. Heeneman S, Daemen MJ. Cardiovascular risks in spondyloarthritides. Curr Opin Rheumatol 2007;19:358-62. Go to original source... Go to PubMed...
  24. Kimhi O, Caspi D, Bornstein NM, Maharshak N, Gur A, Arbel Y, Comaneshter D, Paran D, Wigler I, Levartovsky D, Berliner S, Elkayam O. Prevalence and risk factors of atherosclerosis in patients with psoriatic arthritis. Semin Arthritis Rheum 2007;36:203-9. Go to original source... Go to PubMed...
  25. Cerinic MM, Valentini G, Sorano GG. Blood coagulation, fibrinolysis, and markers of endothelial dysfunction in systemic sclerosis. Semin Arthritis Rheum 2003;32:285-95. Go to original source... Go to PubMed...
  26. Gerli R, Bartoloni Bocci E, Vaudo G, Marchesi S, Vitali C, Shoenfeld Y. Traditional cardiovascular risk factors in primary Sjögren's syndrome - role of dyslipidaemia. Rheumatology (Oxford) 2006;45:1580-1. Go to original source... Go to PubMed...
  27. 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. Go to original source... Go to PubMed...
  28. Alberti KG, Zimmet P, Shaw J. IDF Epidemiology Task Force Consensus Group The metabolic syndrome - a new worldwide definition. Lancet 2005;366:1059-62. Go to original source... Go to PubMed...
  29. Tailor AM, Peeters PH, Norat T, Vineis P, Romaguera D. An update on the prevalence of the metabolic syndrome in children and adolescents. Int J Pediatr Obes 2010;5:202-13. Go to original source... Go to PubMed...
  30. Nascimento IS, Quaio CR, Sinicato NA, Appenzeller S, de Carvalho JF. Aspects of atherosclerosis and metabolic syndrome in lupus erythematosus. Acta Reumatol Port 2010;35:294-300. Go to PubMed...
  31. Mok CC, Poon WL, Lai JP, Wong CK, Chiu SM, Wong CK, Lun SW, Ko GT, Lam CW, Lam CS. Metabolic syndrome, endothelial injury, and subclinical atherosclerosis in patients with systemic lupus erythematosus. Scand J Rheumatol 2010;39:42-9. Go to original source... Go to PubMed...
  32. Telles R, Lanna C, Ferreira G, Rebeiro A. Metabolic syndrome in patients with systemic lupus erythematosus: association with traditional risk factors for coronary heart disease and lupus characteristics. Lupus 2010;19:803-9. Go to original source... Go to PubMed...
  33. Petri M. Detection of coronary artery disease and the role of traditional risk factors in the Hopkins Lupus Cohort. Lupus 2000;9:170-5. Go to original source... Go to PubMed...
  34. Burt VL, Cutler JA, Higgins M, Horan MJ, Labarthe D, Whelton P, Brown C, Roccella EJ. Trends in the prevalence, awareness, treatment, and control of hypertension in the adult US population. Data from the health examination surveys, 1960 to 1991. Hypertension 1995;26:60-9. Go to original source... Go to PubMed...
  35. Volkmann ER, Grossman JM, Sahakian LJ, Skaggs BJ, FitzGerald J, Ragavendra N, Charles-Schoeman C, Chen W, Gorn A, Karpouzas G, Weisman M, Wallace DJ, Hahn BH, McMahon M. Low physical activity is associated with proinflammatory high-density lipoprotein and increased subclinical atherosclerosis in women with systemic lupus erythematosus. Arthritis Care Res 2010;62:258-65. Go to original source...
  36. Hirsch AT, Haskal ZJ, Hertzer NR, Bakal CW, Creager MA, Halperin JL, Hiratzka LF, Murphy WR, Olin JW, Puschett JB, Rosenfield KA, Sacks D, Stanley JC, Taylor LM Jr, White CJ, White J, White RA, Antman EM, Smith SC Jr, Adams CD, Anderson JL, Faxon DP, Fuster V, Gibbons RJ, Hunt SA, Jacobs AK, Nishimura R, Ornato JP, Page RL, Riegel B. ACC/AHA 2005 Practice Guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic). Circulation 2006;113:463-558. Go to original source... Go to PubMed...
  37. Tyrrell PN, Beyene J, Feldman BM, McCrindle BW, Silverman ED, Bradley TJ. Rheumatic disease and carotid intima-media thickness: a systematic review and meta-analysis. Arterioscler Thromb Vasc Biol 2010;30:1014-26. Go to original source... Go to PubMed...
  38. Kiani AN, Post WS, Magder LS, Petri M. Predictors of progression in atherosclerosis over 2 years in systemic lupus erythematosus. Rheumatology (Oxford). 2011;50(11): 2071-9. Go to original source... Go to PubMed...
  39. Belibou C, Ancuþa C, Ancuþa E, Filoº C, Chirieac R. Carotid intima-media thickness and plaque as surrogate biomarkers of atherosclerosis among consecutive women with systemic lupus erythematosus. Rom J Morphol Embryol. 2012;53(1):29-34.
  40. Karp I, Abrahamowicz M, Fortin PR, Pilote L, Neville C, Pineau CA, Esdaile JM. Recent corticosteroid use and recent disease activity: independent determinants of coronary heart disease risk factors in systemic lupus erythematosus? Arthritis Rheum 2008;59:169-75. Go to original source... Go to PubMed...
  41. Rahman P, Gladman DD, Urowitz MB. The cholesterol lowering effect of antimalarial drugs is enhanced in patients with lupus taking corticosteroid drugs. Rheumatol 1999;26:325-30.
  42. Toms TE, Panoulas VF, Douglas KM, Griffiths HR, Kitas GD. Lack of association between glucocorticoid use and presence of the metabolic syndrome in patients with rheumatoid arthritis: a cross-sectional study. Arthritis Res Ther 2008;10:145-53. Go to original source...
  43. Thompson T, Sutton-Tyrrell K, Wildman RP, Kao A, Fitzgerald SG, Shook B, Tracy RP, Kuller LH, Brockwell S, Manzi S. Progression of carotid intima-media thickness and plaque in women with systemic lupus erythematosus. Arthritis Rheum 2008;58:835-42. Go to original source... Go to PubMed...
  44. Urbanus RT, Siegerink B, Roest M, Rosendaal FR, de Groot PG, Algra A. Antiphospholipid antibodies and risk of myocardial infarction and ischemic stroke in young women in the RATIO study: a case-control study. Lancet Neurol 2009;8: 971-3. Go to original source... Go to PubMed...
  45. Peters MJ, Symmons DP, McCarey D, Dijkmans BA, Nicola P, Kvien TK, McInnes IB, Haentzschel H, Gonzalez-Gay MA, Provan S, Semb A, Sidiropoulos P, Kitas G, Smulders YM, Soubrier M, Szekanecz Z, Sattar N, Nurmohamed MT. 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. Go to original source... Go to PubMed...