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Investigation of subclinical atherosclerosis in psoriatic arthritis patients with minimal disease activity

  • Original Article - Observational Research
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Abstract

The aim of this study was to investigate the presence of subclinical atherosclerosis among psoriatic arthritis (PsA) patients without any cardiovascular disease (CVD) or traditional cardiovascular risk factors through measurement of endothelial function and carotid intima-media thickness (IMT) and correlated with disease-related risk factors. Twenty patients with PsA according to classification criteria for psoriatic arthritis and 20 age- and sex-matched controls were included. Patients with risk factors for cardiovascular disease were excluded. Carotid IMT was measured using two-dimensional carotid ultrasonography (USG). Endothelial function was determined by measuring flow-mediated endothelial-dependent vasodilatation (FMD %) and nitrate-induced dilatation (NID %) using brachial artery USG. Additionally, serum asymmetric dimethylarginine (ADMA) level was obtained using ELISA methodology. In this cross-sectional study, FMD % was significantly more decreased among PsA patients versus control group [mean 11 % (median (range) %10.5 (8–15 %)] and mean 13.2 % [median (range) 12, 8 % (8.1–17.6 %), respectively; p = 0.01]. There was no significant difference in NID %, ADMA level and mean IMT or maximum IMT results. FMD % did not show a significant correlation with clinical and laboratory data of PsA patients. This study showed that endothelial dysfunction may be present in PsA patients with no CVD and traditional cardiovascular risk factors. The study findings lend support to the previous reports that suggested a potential relationship between PsA and atherosclerotic disorders.

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References

  1. Gladman DD (2004) Psoriatic arthritis. In: Maddison PJ, Isenberg DA, Woo P, Glass DN, Breedveld F (eds) Oxford textbook of rheumatology, 3rd edn. Oxford University Press, Oxford, pp 766–778

    Google Scholar 

  2. Wong D, Gladman DD, Husted J, Long JA, Farewell VT (1997) Mortality studies in psoriatic arthritis: results from a single outpatient clinic. I. Causes and risk of death. Arthritis Rheum 40:1868–1872

    Article  CAS  PubMed  Google Scholar 

  3. Di Minno MN, Iervolino S, Peluso R, Scarpa R, Di Minno G (2011) Carotid intima-media thickness in psoriatic arthritis: differences between tumor necrosis factor-α blockers and traditional disease-modifying antirheumatic drugs. Arterioscler Thromb Vasc Biol 31(3):705–712 CaRRDs study group

    Article  PubMed  Google Scholar 

  4. Sattar N, McCarey DW, Capell H, McInnes IB (2003) Explaining how “high-grade” systemic inflammation accelerates vascular risk in rheumatoid arthritis. Circulation 108(24):2957–2963

    Article  PubMed  Google Scholar 

  5. Tam LS, Shang Q, Li EK, Tomlinson B, Chu TT, Li M, Leung YY, Kwok LW, Wong KC, Li TK, Yu T, Zhu TY, Kun EW, Yip GW, Yu CM (2008) Subclinical carotid atherosclerosis in patients with psoriatic arthritis. Arthritis Rheum 59(9):1322–1331

    Article  PubMed  Google Scholar 

  6. Eder L, Jayakar J, Shanmugarajah S, Thavaneswaran A, Pereira D, Chandran V, Rosen CF, Gladman DD (2013) The burden of carotid artery plaques is higher in patients with psoriatic arthritis compared with those with psoriasis alone. Ann Rheum Dis 72(5):715–720

    Article  PubMed  Google Scholar 

  7. Turiel M, Atzeni F, Tomasoni L, de Portu S, Delfino L, Bodini BD, Longhi M, Sitia S, Bianchi M, Ferrario P, Doria A, De Gennaro CV, Sarzi-Puttini P (2009) Non-invasive assessment of coronary flow reserve and ADMA levels: a case-control study of early rheumatoid arthritis patients. Rheumatology (Oxford) 48(7):834–839

    Article  CAS  Google Scholar 

  8. Miyazaki H, Matsuoka H, Cooke JP, Usui M, Ueda S, Okuda S, Imaizumi T (1999) Endogenous nitric oxide synthase inhibitor: a novel marker of atherosclerosis. Circulation 99(9):1141–1146

    Article  CAS  PubMed  Google Scholar 

  9. Vallance P (2001) Importance of asymmetrical dimethylarginine in cardiovascular risk. Lancet 358(9299):2096–2097

    Article  CAS  PubMed  Google Scholar 

  10. Atzeni F, Sarzi-Puttini P, Sitia S, Tomasoni L, Gianturco L, Battellino M, Boccassini L, De Gennaro CV, Marchesoni A, Turiel M (2011) Coronary flow reserve and asymmetric dimethylarginine levels: new measurements for identifying subclinical atherosclerosis in patients with psoriatic arthritis. J Rheumatol 38(8):1661–1664

    Article  CAS  PubMed  Google Scholar 

  11. Brunner H, Cockcroft JR, Deanfield J, Donald A, Ferrannini E, Halcox J et al (2005) Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. Endothelial function and dysfunction. Part II: association with cardiovascular risk factors and diseases. A statement by the Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension. J Hypertens 23(2):233–246

    Article  CAS  PubMed  Google Scholar 

  12. Deanfield J, Donald A, Ferri C, Giannattasio C, Halcox J, Halligan S et al (2005) Working Group on Endothelin and Endothelial Factors of the European Society of Hypertension. Endothelial function and dysfunction. Part I: 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 23(1):7–17

    Article  CAS  PubMed  Google Scholar 

  13. Nadar S, Blann AD, Lip GY (2004) Endothelial dysfunction: methods of assessment and application to hypertension. Curr Pharm Des 10(29):3591–3605

    Article  CAS  PubMed  Google Scholar 

  14. Lorenz MW, Markus HS, Bots ML, Rosvall M, Sitzer M (2007) Prediction of clinical cardiovascular events with carotid intima-media thickness: a systematic review and meta-analysis. Circulation 115(4):459–467

    Article  PubMed  Google Scholar 

  15. Gonzalez-Juanatey C, Llorca J, Miranda-Filloy JA, Amigo-Diaz E, Testa A, Garcia-Porrua C, Martin J, Gonzalez-Gay MA (2007) Endothelial dysfunction in psoriatic arthritis patients without clinically evident cardiovascular disease or classic atherosclerosis risk factors. Arthritis Rheum 57(2):287–293

    Article  CAS  PubMed  Google Scholar 

  16. Gonzalez-Juanatey C, Llorca J, Amigo-Diaz E, Dierssen T, Martin J, Gonzalez-Gay MA (2007) High prevalence of subclinical atherosclerosis in psoriatic arthritis patients without clinically evident cardiovascular disease or classic atherosclerosis risk factors. Arthritis Rheum 57:1074–1080

    Article  PubMed  Google Scholar 

  17. Coates LC, Fransen J, Helliwell PS (2010) Defining minimal disease activity in psoriatic arthritis: a proposed objective target for treatment. Ann Rheum Dis 69(1):48–53

    Article  CAS  PubMed  Google Scholar 

  18. Taylor W, Gladman D, Helliwell P, Marchesoni A, Mease P, Mielants H (2006) Classification criteria for psoriatic arthritis: development of new criteria from a large international study. Arthritis Rheum 54(8):2665–2673 CASPAR study group

    Article  PubMed  Google Scholar 

  19. van der Heijde DM, van’t Hof MA, van Riel PL, van Leeuwen MA, van Rijswijk MH, van de Putte LB (1992) Validity of single variables and composite indices for measuring disease activity in rheumatoid arthritis. Ann Rheum Dis 51(2):177–181

    Article  PubMed Central  PubMed  Google Scholar 

  20. Berth-Jones J, Grotzinger K, Rainville C, Pham B, Huang J, Daly S, Herdman M, Firth P, Hotchkiss K (2006) A study examining inter- and intrarater reliability of three scales for measuring severity of psoriasis: psoriasis area and severity index, Physician’s Global Assessment and Lattice System Physician’s Global Assessment. Br J Dermatol 155:707–713

    Article  CAS  PubMed  Google Scholar 

  21. Fries JF, Spitz P, Kraines RG, Holman HR (1980) Measurement of patient outcome in arthritis. Arthritis Rheum 23(2):137–145

    Article  CAS  PubMed  Google Scholar 

  22. Committee Guidelines (2003) European society of Hypertension-European society of cardiology guidelines for the management of arterial hypertension. J Hypertens 21:1011–1013

    Article  Google Scholar 

  23. Persson J, Stavenow L, Wikstrand J, Israelsson B, Formgren J, Berglund G (1992) Noninvasive quantification of atherosclerotic lesions. Reproducibility of ultrasonographic measurement of arterial wall thickness and plaque size. Arterioscler Thromb 12(2):261–266

    Article  CAS  PubMed  Google Scholar 

  24. Roman MJ, Saba PS, Pini R, Spitzer M, Pickering TG, Rosen S, Alderman MH, Devereux RB (1992) Parallel cardiac and vascular adaptation in hypertension. Circulation 86(6):1909–1918

    Article  CAS  PubMed  Google Scholar 

  25. Joakimsen O, Bønaa KH, Stensland-Bugge E (1997) Reproducibility of ultrasound assessment of carotid plaque occurrence, thickness, and morphology the Tromsø study. Stroke 28(11):2201–2207

    Article  CAS  PubMed  Google Scholar 

  26. Celermajer DS, Sorensen KE, Gooch VM et al (1992) Non-invasive detection of endothelial dysfunction in children and adults at risk of atherosclerosis. Lancet 340:1111–1115

    Article  CAS  PubMed  Google Scholar 

  27. Glagov S, Weisenberg E, Zarins CK, Stankunavicius R, Kolettis GJ (1987) Compensatory enlargement of human atherosclerotic coronary arteries. N Engl J Med 316:1371–1375

    Article  CAS  PubMed  Google Scholar 

  28. Gladman DD, Farewell VT, Wong K, Husted J (1998) Mortality studies in psoriatic arthritis: results from a single outpatient center. II. Prognostic indicators for death. Arthritis Rheum 41(6):1103–1110

    Article  CAS  PubMed  Google Scholar 

  29. Mallbris L, Akre O, Granath F, Yin L, Lindelöf B, Ekbom A, Ståhle-Bäckdahl M (2004) Increased risk for cardiovascular mortality in psoriasis inpatients but not in outpatients. Eur J Epidemiol 19(3):225–230

    Article  PubMed  Google Scholar 

  30. Tam LS, Tomlinson B, Chu TT, Li M, Leung YY et al (2008) Cardiovascular risk profile of patients with psoriatic arthritis compared to controls–the role of inflammation. Rheumatology (Oxford) 47(5):718–723

    Article  Google Scholar 

  31. Kimhi O, Caspi D, Bornstein NM, Maharshak N, Gur A, Arbel Y, Comaneshter D, Paran D, Wigler I, Levartovsky D, Berliner S, Elkayam O (2007) Prevalence and risk factors of atherosclerosis in patients with psoriatic arthritis. Semin Arthritis Rheum 36(4):203–209

    Article  PubMed  Google Scholar 

  32. Syngle A, Vohra K, Sharma A, Kaur L (2010) Endothelial dysfunction in ankylosing spondylitis improves after tumor necrosis factor-alpha blockade. Clin Rheumatol 29(7):763–770

    Article  PubMed  Google Scholar 

  33. Gonzalez-Juanatey C, Testa A, Garcia-Castelo A, Garcia-Porrua C, Llorca J, Gonzalez-Gay MA (2004) Active but transient improvement of endothelial function in rheumatoid arthritis patients undergoing long-term treatment with anti-tumor necrosis factor alpha antibody. Arthritis Rheum 51(3):447–450

    Article  CAS  PubMed  Google Scholar 

  34. Bosello S, Santoliquido A, Zoli A, Di Campli C, Flore R, Tondi P, Ferraccioli G (2007) TNF-alpha blockade induces a reversible but transient effect on endothelial dysfunction in patients with long-standing severe rheumatoid arthritis. Clin Rheumatol 27(7):833–839

    Article  PubMed  Google Scholar 

  35. Spinelli FR, Metere A, Barbati C, Pierdominici M, Iannuccelli C et al (2013) Effect of therapeutic inhibition of TNF on circulating endothelial progenitor cells in patients with rheumatoid arthritis. Mediators Inflamm. doi:10.1155/2013/537539

    PubMed Central  PubMed  Google Scholar 

  36. Vallance P, Leone A, Calver A, Collier J (1992) Accumulation of an endogenous inhibitor of nitric oxide synthesis in chronic renal failure. Lancet 339(8793):572–575

    Article  CAS  PubMed  Google Scholar 

  37. Surdacki A, Martens-Lobenhoffer J, Wloch A et al (2007) Elevated plasma asymmetric dimethyl-l-arginine levels are linked to endothelial progenitor cell depletion and carotid atherosclerosis in rheumatoid arthritis. Arth Rheum 56(3):809–819

    Article  CAS  Google Scholar 

  38. Di Franco M, Spinelli FR, Metere A et al (2012) Serum levels of asymmetric dimethylarginine and apelin as potential markers of vascular endothelial dysfunction in early rheumatoid arthritis. Mediators Inflamm. doi:10.1155/2012/347268

    Google Scholar 

  39. Eder L, Zisman D, Barzilai M, Laor A, Rahat M, Rozenbaum M, Bitterman H, Feld J, Rimar D, Rosner I (2008) Subclinical atherosclerosis in psoriatic arthritis: a case-control study. J Rheumatol 35(5):877–882

    PubMed  Google Scholar 

  40. Tam LS, Li EK, Shang Q, Tomlinson B, Li M, Leung YY, Kuan WP, Kwok LW, Li TK, Zhu Y, Kun EW, Yip G, Yu CM (2011) 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 70(4):705–706

    Article  PubMed  Google Scholar 

  41. Van Doornum S, McColl G, Wicks IP (2002) Accelerated atherosclerosis: an extraarticular feature of rheumatoid arthritis? Arthritis Rheum 46(4):862–873

    Article  PubMed  Google Scholar 

  42. Gonzalez-Gay MA, Gonzalez-Juanatey C, Martin J (2005) Rheumatoid arthritis: a disease associated with accelerated atherogenesis. Semin Arthritis Rheum 35(1):8–17

    Article  PubMed  Google Scholar 

  43. Gonzalez-Gay MA, Gonzalez-Juanatey C, Lopez-Diaz MJ, Piñeiro A, Garcia-Porrua C et al (2007) HLA-DRB1 and persistent chronic inflammation contribute to cardiovascular events and cardiovascular mortality in patients with rheumatoid arthritis. Arthritis Rheum. 57(1):125–132

    Article  CAS  PubMed  Google Scholar 

  44. Vaudo G, Marchesi S, Gerli R, Allegrucci R, Giordano A, Siepi D et al (2004) Endothelial dysfunction in young patients with rheumatoid arthritis and low disease activity. Ann Rheum Dis 63(1):31–35

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Gonzalez-Juanatey C, Testa A, Garcia-Castelo A, Garcia-Porrua C, Llorca J et al (2003) HLA-DRB1 status affects endothelial function in treated patients with rheumatoid arthritis. Am J Med 114(8):647–652

    Article  CAS  PubMed  Google Scholar 

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Conflict of interest

The authors declare no conflict of interest. This study was funded by the Kocaeli University Coordinating Unit for Scientific Research Projects.

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Authors and Affiliations

  1. Department of Rheumatology, Bakırköy Dr. Sadi Konuk Training and Research Hospital, Istanbul, 34147, Turkey

    Baris Yilmazer

  2. Department of Cardiology, Medicine Faculty, Kocaeli University, Kocaeli, Turkey

    Tayfun Sahin

  3. Department of Biochemistry, Sisli Etfal Training and Research Hospital, Sisli-Istanbul, Turkey

    Berrin Öztaş Unlu

  4. Department of Biochemistry, Medicine Faculty, Kocaeli University, Kocaeli, Turkey

    Hale Maral Kir

  5. Department of Rheumatology, Medicine Faculty, Kocaeli University, Kocaeli, Turkey

    Ayse Cefle

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  1. Baris Yilmazer
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  2. Tayfun Sahin
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Correspondence to Baris Yilmazer.

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Yilmazer, B., Sahin, T., Unlu, B.Ö. et al. Investigation of subclinical atherosclerosis in psoriatic arthritis patients with minimal disease activity. Rheumatol Int 35, 1385–1392 (2015). https://doi.org/10.1007/s00296-015-3228-y

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  • DOI: https://doi.org/10.1007/s00296-015-3228-y

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