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Arterial stiffness and peripheral arterial disease in patients with systemic lupus erythematosus

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Abstract

Systemic lupus erythematosus (SLE) is associated with increased cardiovascular risk. We aimed to evaluate arterial stiffness and the ankle brachial index (ABI), two markers of subclinical cardiovascular disease, in SLE. We studied 55 patients with SLE (12.7% males, age 53.3 ± 15.3 years) and 61 age- and gender-matched controls. Arterial stiffness was evaluated by measuring pulse wave velocity (PWV), augmentation index (AIx) and central systolic, diastolic, pulse and mean blood pressure (BP). Peripheral arterial disease was defined as ABI ≤ 0.90. Regarding markers of arterial stiffness, patients with SLE had lower PWV and AIx than controls (p < 0.01 and p < 0.05, respectively). However, after adjusting for differences in cardiovascular risk factors between patients with SLE and controls, PWV and AIx did not differ between the two groups. Central systolic, diastolic, pulse and mean BP also did not differ between the two groups. In patients with SLE, PWV correlated independently with systolic BP (B = 0.05, p < 0.001) and waist/hip ratio (B = 6.72, p < 0.05). Regarding ABI, the lowest ABI was lower in patients with SLE than in controls (p < 0.005). However, after adjusting for differences in cardiovascular risk factors between patients with SLE and controls, the lowest ABI did not differ between the two groups. The prevalence of PAD also did not differ between patients with SLE and controls (10.0 and 5.4%, respectively; p = NS). Markers of arterial stiffness and the ABI do not appear to differ between patients with SLE and age- and gender-matched controls. However, given the small sample size, larger studies are needed to clarify whether SLE promotes arterial stiffness and PAD.

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References

  1. D’Cruz DP, Khamashta MA, Hughes GR (2007) Systemic lupus erythematosus. Lancet 369:587–596

    Article  PubMed  Google Scholar 

  2. Danchenko N, Satia JA, Anthony MS (2006) Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus 15:308–318

    Article  CAS  PubMed  Google Scholar 

  3. Nossent J, Cikes N, Kiss E, Marchesoni A, Nassonova V, Mosca M, Olesinska M, Pokorny G, Rozman B, Schneider M, Vlachoyiannopoulos PG, Swaak A (2007) Current causes of death in systemic lupus erythematosus in Europe, 2000–2004: relation to disease activity and damage accrual. Lupus 16:309–317

    Article  CAS  PubMed  Google Scholar 

  4. Ward MM (1999) Premature morbidity from cardiovascular and cerebrovascular diseases in women with systemic lupus erythematosus. Arthritis Rheum 42:338–346

    Article  CAS  PubMed  Google Scholar 

  5. Fischer LM, Schlienger RG, Matter C, Jick H, Meier CR (2004) Effect of rheumatoid arthritis or systemic lupus erythematosus on the risk of first-time acute myocardial infarction. Am J Cardiol 93:198–200

    Article  PubMed  Google Scholar 

  6. Tziomalos K, Sivanadarajah N, Mikhailidis DP, Boumpas DT, Seifalian AM (2008) Increased risk of vascular events in systemic lupus erythematosus: is arterial stiffness a predictor of vascular risk? Clin Exp Rheumatol 26:1134–1145

    CAS  PubMed  Google Scholar 

  7. Asanuma Y, Oeser A, Shintani AK, Turner E, Olsen N, Fazio S, Linton MF, Raggi P, Stein CM (2003) Premature coronary-artery atherosclerosis in systemic lupus erythematosus. N Engl J Med 349:2407–2415

    Article  CAS  PubMed  Google Scholar 

  8. Nuttall SL, Heaton S, Piper MK, Martin U, Gordon C (2003) Cardiovascular risk in systemic lupus erythematosus—evidence of increased oxidative stress and dyslipidaemia. Rheumatology (Oxford) 42:758–762

    Article  CAS  Google Scholar 

  9. El Magadmi M, Ahmad Y, Turkie W, Yates AP, Sheikh N, Bernstein RM, Durrington PN, Laing I, Bruce IN (2006) Hyperinsulinemia, insulin resistance, and circulating oxidized low density lipoprotein in women with systemic lupus erythematosus. J Rheumatol 33:50–56

    PubMed  Google Scholar 

  10. De Leeuw K, Freire B, Smit AJ, Bootsma H, Kallenberg CG, Bijl M (2006) Traditional and non-traditional risk factors contribute to the development of accelerated atherosclerosis in patients with systemic lupus erythematosus. Lupus 15:675–682

    Article  PubMed  Google Scholar 

  11. Vlachopoulos C, Aznaouridis K, O’Rourke MF, Safar ME, Baou K, Stefanadis C (2010) Prediction of cardiovascular events and all-cause mortality with central haemodynamics: a systematic review and meta-analysis. Eur Heart J 31:1865–1871

    Article  PubMed  Google Scholar 

  12. Vlachopoulos C, Aznaouridis K, Stefanadis C (2010) Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J Am Coll Cardiol 55:1318–1327

    Article  PubMed  Google Scholar 

  13. Yip GW, Shang Q, Tam LS, Zhang Q, Li EK, Fung JW, Yu CM (2009) Disease chronicity and activity predict subclinical left ventricular systolic dysfunction in patients with systemic lupus erythematosus. Heart 95:980–987

    Article  PubMed  Google Scholar 

  14. Roldan CA, Alomari IB, Awad K, Boyer NM, Qualls CR, Greene ER, Sibbitt WL Jr (2014) Aortic stiffness is associated with left ventricular diastolic dysfunction in systemic lupus erythematosus: a controlled transesophageal echocardiographic study. Clin Cardiol 37:83–90

    Article  PubMed  Google Scholar 

  15. Pieretti J, Roman MJ, Devereux RB, Lockshin MD, Crow MK, Paget SA, Schwartz JE, Sammaritano L, Levine DM, Salmon JE (2007) Systemic lupus erythematosus predicts increased left ventricular mass. Circulation 116:419–426

    Article  PubMed  Google Scholar 

  16. Selzer F, Sutton-Tyrrell K, Fitzgerald S, Tracy R, Kuller L, Manzi S (2001) Vascular stiffness in women with systemic lupus erythematosus. Hypertension 37:1075–1082

    Article  CAS  PubMed  Google Scholar 

  17. Bjarnegråd N, Bengtsson C, Brodszki J, Sturfelt G, Nived O, Länne T (2006) Increased aortic pulse wave velocity in middle aged women with systemic lupus erythematosus. Lupus 15:644–650

    Article  PubMed  Google Scholar 

  18. Morreale M, Mulè G, Ferrante A, D’ignoto F, Cottone S (2016) Early vascular aging in normotensive patients with systemic lupus erythematosus: comparison with young patients having hypertension. Angiology 67:676–682

    Article  CAS  PubMed  Google Scholar 

  19. Sabio JM, Vargas-Hitos JA, Martinez-Bordonado J, Navarrete-Navarrete N, Díaz-Chamorro A, Olvera-Porcel C, Zamora M, Jiménez-Alonso J (2015) Association between low 25-hydroxyvitamin D, insulin resistance and arterial stiffness in nondiabetic women with systemic lupus erythematosus. Lupus 24:155–163

    Article  CAS  PubMed  Google Scholar 

  20. Sacre K, Escoubet B, Pasquet B, Chauveheid MP, Zennaro MC, Tubach F, Papo T (2014) Increased arterial stiffness in systemic lupus erythematosus (SLE) patients at low risk for cardiovascular disease: a cross-sectional controlled study. PLoS ONE 9:e94511

    Article  PubMed  PubMed Central  Google Scholar 

  21. Cypiene A, Kovaite M, Venalis A, Dadoniene J, Rugiene R, Petrulioniene Z, Ryliskyte L, Laucevicius A (2009) Arterial wall dysfunction in systemic lupus erythematosus. Lupus 18:522–529

    Article  CAS  PubMed  Google Scholar 

  22. Aboyans V, Criqui MH, Abraham P, Allison MA, Creager MA, Diehm C, Fowkes FG, Hiatt WR, Jönsson B, Lacroix P, Marin B, McDermott MM, Norgren L, Pande RL, Preux PM, Stoffers HE, Treat-Jacobson D, American Heart Association Council on Peripheral Vascular Disease, Council on Epidemiology and Prevention, Council on Clinical Cardiology, Council on Cardiovascular Nursing, Council on Cardiovascular Radiology and Intervention, and Council on Cardiovascular Surgery and Anesthesia (2012) Measurement and interpretation of the ankle-brachial index: a scientific statement from the American Heart Association. Circulation 126:2890–2909

    Article  PubMed  Google Scholar 

  23. Collaboration Ankle Brachial Index, Fowkes FG, Murray GD, Butcher I, Heald CL, Lee RJ, Chambless LE, Folsom AR, Hirsch AT, Dramaix M, deBacker G, Wautrecht JC, Kornitzer M, Newman AB, Cushman M, SuttonTyrrell K, Fowkes FG, Lee AJ, Price JF, d’Agostino RB, Murabito JM, Norman PE, Jamrozik K, Curb JD, Masaki KH, Rodríguez BL, Dekker JM, Bouter LM, Heine RJ, Nijpels G, Stehouwer CD, Ferrucci L, McDermott MM, Stoffers HE, Hooi JD, Knottnerus JA, Ogren M, Hedblad B, Witteman JC, Breteler MM, Hunink MG, Hofman A, Criqui MH, Langer RD, Fronek A, Hiatt WR, Hamman R, Resnick HE, Guralnik J, McDermott MM (2008) Ankle brachial index combined with Framingham Risk Score to predict cardiovascular events and mortality: a meta-analysis. JAMA 300:197–208

    Article  Google Scholar 

  24. Tziomalos K, Athyros VG, Karagiannis A, Mikhailidis DP (2010) The role of ankle brachial index and carotid intima-media thickness in vascular risk stratification. Curr Opin Cardiol 25:394–398

    Article  PubMed  Google Scholar 

  25. June RR, Scalzi LV (2013) Peripheral vascular disease in systemic lupus patients. J Clin Rheumatol 19:367–372

    Article  PubMed  Google Scholar 

  26. Kay SD, Poulsen MK, Diederichsen AC, Voss A (2016) Coronary, carotid, and lower-extremity atherosclerosis and their interrelationship in Danish patients with systemic lupus erythematosus. J Rheumatol 43:315–322

    Article  CAS  PubMed  Google Scholar 

  27. Erdozain JG, Villar I, Nieto J, Ruiz-Irastorza G (2014) Peripheral arterial disease in systemic lupus erythematosus: prevalence and risk factors. J Rheumatol 41:310–317

    Article  PubMed  Google Scholar 

  28. Theodoridou A, Bento L, D’Cruz DP, Khamashta MA, Hughes GR (2003) Prevalence and associations of an abnormal ankle-brachial index in systemic lupus erythematosus: a pilot study. Ann Rheum Dis 62:1199–1203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Friedewald WT, Levy RI, Fredrickson DS (1972) Estimation of the concentration of low-density lipoprotein cholesterol in plasma, without use of the preparative ultracentrifuge. Clin Chem 18:499–502

    CAS  PubMed  Google Scholar 

  30. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D (1999) A more accurate method to estimate glomerular filtration rate from serum creatinine: a new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med 130:461–470

    Article  CAS  PubMed  Google Scholar 

  31. Van Bortel LM, Laurent S, Boutouyrie P, Chowienczyk P, Cruickshank JK, De Backer T, Filipovsky J, Huybrechts S, Mattace-Raso FU, Protogerou AD, Schillaci G, Segers P, Vermeersch S, Weber T, Artery Society, European Society of Hypertension Working Group on Vascular Structure and Function, European Network for Noninvasive Investigation of Large Arteries (2012) Expert consensus document on the measurement of aortic stiffness in daily practice using carotid-femoral pulse wave velocity. J Hypertens 30:445–448

    Article  PubMed  Google Scholar 

  32. Selzer F, Sutton-Tyrrell K, Fitzgerald SG, Pratt JE, Tracy RP, Kuller LH, Manzi S (2004) Comparison of risk factors for vascular disease in the carotid artery and aorta in women with systemic lupus erythematosus. Arthritis Rheum 50:151–159

    Article  PubMed  Google Scholar 

  33. Cecelja M, Chowienczyk P (2009) Dissociation of aortic pulse wave velocity with risk factors for cardiovascular disease other than hypertension: a systematic review. Hypertension 54:1328–1336

    Article  CAS  PubMed  Google Scholar 

  34. Wohlfahrt P, Somers VK, Cifkova R, Filipovsky J, Seidlerova J, Krajcoviechova A, Sochor O, Kullo IJ, Lopez-Jimenez F (2014) Relationship between measures of central and general adiposity with aortic stiffness in the general population. Atherosclerosis 235:625–631

    Article  CAS  PubMed  Google Scholar 

  35. Yusuf S, Hawken S, Ounpuu S, Bautista L, Franzosi MG, Commerford P, Lang CC, Rumboldt Z, Onen CL, Lisheng L, Tanomsup S, Wangai P Jr, Razak F, Sharma AM, Anand SS, INTERHEART Study Investigators (2005) Obesity and the risk of myocardial infarction in 27,000 participants from 52 countries: a case-control study. Lancet 366:1640–1649

    Article  PubMed  Google Scholar 

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Authors and Affiliations

  1. First Propedeutic Department of Internal Medicine, Medical School, Aristotle University of Thessaloniki, AHEPA Hospital, 1 Stilponos Kyriakidi Street, 54636, Thessaloníki, Greece

    Konstantinos Tziomalos, Evangelia Makri, Nikolaos Raptis & Apostolos I. Hatzitolios

  2. Clinical Immunology Unit, Second Department of Internal Medicine, Medical School, Aristotle University of Thessaloniki, Hippokration Hospital, Thessaloníki, Greece

    Ioannis Gkougkourelas, Alexandros Sarantopoulos, Eleni Bekiari, Konstantinos Tselios, Marianna Pantoura & Panagiota Boura

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  1. Konstantinos Tziomalos
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  2. Ioannis Gkougkourelas
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  3. Alexandros Sarantopoulos
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  4. Eleni Bekiari
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  9. Apostolos I. Hatzitolios
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Correspondence to Konstantinos Tziomalos.

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All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

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Tziomalos, K., Gkougkourelas, I., Sarantopoulos, A. et al. Arterial stiffness and peripheral arterial disease in patients with systemic lupus erythematosus. Rheumatol Int 37, 293–298 (2017). https://doi.org/10.1007/s00296-016-3610-4

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