Relation between impaired coronary microvascular circulation and plasma atherogenic index in patients with ankylosing spondylitis

Year 2023, , 1215 - 1222, 29.10.2023

Eyüp Özkan , Yücel Yılmaz , Fatma Betül Çelik , Şaban Keleşoğlu , Yasemin Doğan , Erkan Demirci , Esen Kasapoğlu , Ümmühan Zeynep Bilgili , Mustafa Calıskan

https://doi.org/10.32322/jhsm.1343245

Abstract

Aim: The coronary flow reserve (CFR) is a sign of endothelial dysfunction and early-stage coronary artery disease (CAD). Plasma atherogenic index (PAI) is related to subclinical CAD and may be used as a predictor of cardiovascular mortality. Our aim is to determine CFR and PAI in patients with AS and to investigate whether PAI can be used in the detection of early stage CAD.
Methods: The study population comprised 48 patients, who were diagnosed with AS based on modified New York criteria and 35 healthy volunteers. PAI values were calculated with the formula log 10 triglyceride (TG) / high-density lipoprotein (HDL).
Results: No difference was detected between the two groups for the demographic variables, including age, sex and BMI. The comparison of the groups for PAI and CFR demonstrated that PAI levels were observed to be significantly higher and CFR levels were observed to be significantly lower in the AS patients (p=0.01, p<0.001, respectively). Correlation analysis revealed that CFR and PAI were negatively correlated (PAI- p<0.0001 r=-0.661). When two groups were formed, one below CFR level 2 and the other above CFR level 2, only PAI was found to increase significantly from the new lipid indices (p=0.004).
Conclusion: There is an independent negative correlation between PAI and CFR values. PAI may be useful in identifying AS patients facing high risk of adverse cardiovascular events, and may also enable the early diagnosis of subclinical atherosclerosis.

Keywords

Ankylosing spondylitis, Plasma atherogenic index, Atherosclerosis, Coronary flow reserve

References

• Gran JT, Husby G. Epidemiology of ankylosing spondylitis. In:Hochberg MC, Silman AJ, Smolen JS, Weinblatt ME, Weisman MH, eds. Rheumatology. 3 rd ed. London: Mosby. 2003:1153-1159.
• Salmon JE, Roman MJ. Subclinical atherosclerosis in rheumatoid arthritis and systemic lupus erythematosus. Am J Med. 2008;121(10 Suppl 1):S3-S8.
• Pereira IA, Borba EF. The role of inflammation, humoral and cell mediated autoimmunity in the pathogenesis of atherosclerosis. Swiss Med Wkly. 2008;138(37-38):534-539.
• Caiati C, Zedda N, Montaldo C, Montisci R, Iliceto S. Contrast enhanced transthoracic second harmonic echo Doppler with adenosine:a noninvasive, rapid and effective method for coronary flow reserve assessment. J Am Coll Cardiol. 1999;34(1):122-130.
• Britten MB, Zeiher AM, Schachinger V. Microvascular dysfunction in angiographically normal or mildly diseased coronary arteries predicts adverse cardiovascular long-term outcome. Coron Artery Dis. 2004;15(5):259-264.
• Montisci R, Marchetti MF, Ruscazio M, et al. Non-invasive coronary flow velocity reserve assessment predicts adverse outcome in women with unstable angina without obstructive coronary artery stenosis. J Public Health Res. 2023;12(2):22799036231181716
• Picano E. Stress echocardiography: a historical perspective. Am J Med. 2003;114(2):126-130.
• Won KB, Heo R, Park HB, et al. Atherogenic index of plasma and the risk of rapid progression of coronary atherosclerosis beyond traditional risk factors. Atherosclerosis. 2021;324:46-51.
• Hong SP, Kim CY, Jung HW. The comparison of the associations of Lipoprotein(a) and the atherogenic index of plasma with coronary artery calcification in patients without high LDL-C: a comparative analysis. J Lipid Atheroscler. 2023;12(2):152-163.
• Zheng Y, Li C, Yang J, et al. Atherogenic index of plasma for non-diabetic, coronary artery disease patients after percutaneous coronary intervention: a prospective study of the long-term outcomes in China. Cardiovasc Diabetol. 2022;21(1):29.
• Onat A, Can G, Kaya H, Hergenç G. "Atherogenic index of plasma" (log10 triglyceride/high-density lipoprotein-cholesterol) predicts high blood pressure, diabetes, and vascular events. J Clin Lipidol. 2010;4(2):89-98.
• Edwards MK, Blaha MJ, Loprinzi PD. Atherogenic index of plasma and triglyceride/high-density lipoprotein cholesterol ratio predict mortality risk better than individual cholesterol risk factors, among an older adult population. Mayo Clin Proc. 2017;92(4):680-681.
• Caliskan M, Erdogan D, Gullu H, et al. Effects of atorvastatin on coronary flow reserve in patients with slow coronary flow. Clin Cardiol. 2007;30(9):475-479.
• Lehtinen K. Mortality and causes of death in 398 patients admitted to hospital with ankylosing spondylitis. Ann Rheum Dis. 1993;52(3):174-176.
• Divecha H, Sattar N, Rumley A, Cherry L, Lowe GD, Sturrock R. Cardiovascular risk parameters in men with ankylosing spondylitis in comparison with non-inflammatory control subjects:relevance of systemic inflammation. Clin Sci (Lond). 2005;109(2):171-176.
• Sari I, Okan T, Akar S, et al. Impaired endothelial function in patients with ankylosing spondylitis. Rheumatology (Oxford). 2006;45(3):283-286.
• Gimbrone MA Jr, García-Cardeña G. Endothelial cell dysfunction and the pathobiology of atherosclerosis. Circ Res. 2016;118(4):620-636.
• Kume N, Cybulsky MI, Gimbrone MA Jr. Lysophosphatidylcholine, a component of atherogenic lipoproteins, induces mononuclear leukocyte adhesion molecules in cultured human and rabbit arterial endothelial cells. J Clin Invest. 1992;90(3):1138-1144.
• Gaydukova IZ, Khondkaryan EV, Aparkina AV, Rebrov AP. Changes in the serum concentrations of adhesion molecules and vascular endothelial growth factor in active ankylosing spondylitis patients taking amtolmetin guacil: results of a 56-week prospective ореn-label controlled observational study]. Ter Arkh. 2017;89(5):38-45.
• Pober JS, Sessa WC. Evolving functions of endothelial cells in inflammation. Nature Rev Immunol. 2007;7(10):803-815.
• Neumann P, Gertzberg N, Johnson A. TNF-alpha induces a decrease in eNOS promoter activity. Am J Physiol Lung Cell Mol Physiol. 2004;286(2):L452-L459.
• Caliskan M, Erdogan D, Gullu H, et al. Impaired coronary microvascular and left ventricular diastolic functions in patients with ankylosing spondylitis. Atherosclerosis. 2008;196(1):306-312.
• Kundu S, Ghosh P, Datta S, Ghosh A, Chattopadhyay S, Chatterjee M. Oxidative stress as a potential biomarker for determining disease activity in patients with rheumatoid arthritis. Free Radic Res. 2012;46(12):1482-1489.
• Steyers CM 3rd, Miller FJ Jr. Endothelial dysfunction in chronic inflammatory diseases. Int J Mol Sci. 2014;15(7):11324-11349.
• Feijoo M, Tunez I, Tasset I, Montilla P, Ruiz A, Collantes E. Infliximab reduces oxidative stress in ankylosing spondylitis. Clin Exp Rheumatol. 2009;27(1):167-168.
• Karakoc M, Altindag O, Keles H, Soran N, Selek S. Serum oxidative-antioxidative status in patients with ankylosing spondilitis. Rheumatol Int. 2007;27(12):1131-1134.
• Ku IA, Imboden JB, Hsue PY, Ganz P. Rheumatoid arthritis: model of systemic inflammation driving atherosclerosis. Circ J. 2009;73(6):977-985.
• Hurt-Camejo E, Paredes S, Masana L, et al. Elevated levels of small, low-density lipoprotein with high affinity for arterial matrix components in patients with rheumatoid arthritis: possible contribution of phospholipase A2 to this atherogenic profile. Arthritis Rheum. 2001;44(12):2761-2767.
• Cure E, Icli A, Uslu AU, et al. Atherogenic index of plasma:a useful marker for subclinical atherosclerosis in ankylosing spondylitis: AIP associate with cIMT in AS. Clin Rheumatol. 2018;37(5):1273-1280.
• Masi AT, Fessler SL, Brezka ML, Wang Y, Donohue SE. Systematic review and meta-analysis of individual serum lipids and analysis of lipid ratios in ankylosing spondylitis and healthy control cohorts: significantly lower mean HDL-cholesterol level in ankylosing spondylitis cohorts. Clin Exp Rheumatol. 2023;41(9):1862-1874.
• Malesci D, Niglio A, Mennillo GA, Buono R, Valentini G, La Montagna G. High prevalence of metabolic syndrome in patients with ankylosing spondylitis. Clin Rheumatol. 2007;26(5):710-714.
• Gullu H, Erdogan D, Caliskan M, et al. Interrelationship between noninvasive predictors of atherosclerosis:transthoracic coronary flow reserve, flow-mediated dilation, carotid intima-media thickness, aortic stiffness, aortic distensibility, elastic modulus, and brachial artery diameter. Echocardiography. 2006;23(10):835-842.
• Haude M, Baumgart D, Verna E, et al. Intracoronary Doppler- and quantitative coronary angiography-derived predictors of major adverse cardiac events after stent implantation. Circulation. 2001;103(9):1212-1217.
• Serruys PW, di Mario C, Piek J, et al. Prognostic value of intracoronary flow velocity and diameter stenosis in assessing the short- and long-term outcomes of coronary balloon angioplasty:the DEBATE Study (Doppler Endpoints Balloon Angioplasty Trial Europe). Circulation. 1997;96(10):3369-3377.
• Kelshiker MA, Seligman H, Howard JP, et al. Coronary Flow Outcomes Reviewing Committee. Coronary flow reserve and cardiovascular outcomes:a systematic review and meta-analysis. Eur Heart J. 2022;43(16):1582-1593.
• Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation. 2000;101(16):1899-1906.
• Civieri G, Montisci R, Kerkhof PLM, Iliceto S, Tona F. Coronary flow velocity reserve by echocardiography: beyond atherosclerotic disease. Diagnostics (Basel). 2023;13(2):193.
• Kul S, Kutlu GA, Guvenc TS, et al. Coronary flow reserve is reduced in sarcoidosis. Atherosclerosis. 2017;264:115-121.
• Çalışkan M, Baycan ÖF, Çelik FB, et al. Coronary microvascular dysfunction is common in patients hospitalized with COVID-19 infection. Microcirculation. 2022;29(4-5):e12757.
• Poddubnyĭ DA, Rebrov AP. [Endothelial dysfunction in patients with Bechterew's disease (ankylosing spondylitis)]. Klin Med (Mosk). 2007;85(7):66-9.
• Yılmaz S, Caliskan M, Kulaksızoglu S, et al. Association between serum total antioxidant status and coronary microvascular functions in patients with SLE. Echocardiography. 2012;29(10):1218-1223.
• Fernández-Macías JC, Ochoa-Martínez AC, Varela-Silva JA, Pérez-Maldonado IN. Atherogenic index of plasma: novel predictive biomarker for cardiovascular illnesses. Arch Med Res. 2019;50(5):285-294.
• National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III). Third Report of the National Cholesterol Education Program (NCEP) Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (Adult Treatment Panel III) final report. Circulation. 2002;106(25):3143-3421.
• Park YB, Lee SK, Lee WK, et al. Lipid profiles in untreated patients with rheumatoid arthritis. J Rheumatol. 1999;26(8):1701-1704.
• Dobiásová M. AIP--atherogenic index of plasma as a significant predictor of cardiovascular risk: from research to practice. Vnitr Lek. 2006;52(1):64-71.
• Kul Ş, Çalışkan Z, Güvenç TS, Güvenç RÇ, Çalışkan M. Plasma lipids in patients with inflammatory bowel disease: observations on the associations between lipid indices and coronary flow reserve. Wien Klin Wochenschr. 2020;132(11-12):283-294.
• Cure E, Icli A, Ugur Uslu A, et al. Atherogenic index of plasma may be strong predictor of subclinical atherosclerosis in patients with Behçet disease. Z Rheumatol. 2017;76(3):259-256.
• Uslu AU, Kucuk A, Icli A, et al. Plasma Atherogenic Index is an Independent Indicator of Subclinical Atherosclerosis in Systemic Lupus Erythematosus. Eurasian J Med. 2017;49(3):193-197.
• Laclaustra M, Casasnovas JA, Fernández-Ortiz A, et al. Femoral and carotid subclinical atherosclerosis association with risk factors and coronary calcium: the AWHS study. J Am Coll Cardiol. 2016;67(11):1263-1274.