Atherogenic index of plasma: a useful marker for subclinical atherosclerosis in ankylosing spondylitis

AIP associate with cIMT in AS
  • Erkan Cure
  • Abdullah Icli
  • Ali Ugur Uslu
  • Davut Sakiz
  • Medine Cumhur Cure
  • Rabia Aydogan Baykara
  • Fatma Yavuz
  • Sevket Arslan
  • Adem Kucuk
Original Article
  • 19 Downloads

Abstract

Ankylosing spondylitis (AS) is associated with an increased risk of atherosclerotic cardiovascular disease (ACD). The atherogenic index of plasma (AIP), which is the logarithmic transformation of the plasma triglyceride (TG) level to the high-density lipoprotein level (HDL) ratio, has been suggested to be a novel marker in the identification of atherosclerosis risk. Therefore, this study aims to determine if the AIP can act as an accurate marker for the detection of subclinical atherosclerosis. Fifty-two male patients with AS and 52 age-, gender-, and body mass index (BMI)-matched healthy control subjects were included in the study. For each patient, AIP and total cholesterol (TC)/HDL values were calculated and carotid artery intima-media thickness (cIMT) was measured. The mean (SD) cIMT and median (range) AIP values for AS patients were higher than that of the healthy control subjects (0.60 ± 0.18 vs. 0.51 ± 0.10, p = 0.003 and 0.23 [− 0.32 to 0.85] vs. 0.09 [− 0.53 to 0.49], p = 0.007, respectively). A positive correlation was found between the patients’ cIMT and AIP values (r = 0.307, p = 0.002) and TC/HDL values (r = 0.241, p = 0.014). Regression analysis revealed an independent association between the subclinical atherosclerosis and AIP (beta [β] = 0.309, p = 0.002). There were no independent correlations between subclinical atherosclerosis and TC (β = 0.245, p = 0.065), TG (β = 0.185, p = 0.515), HDL (β = 0.198, p = 0.231), TC/HDL (β = 0.032, p = 0.862), and low-density lipoprotein (LDL) (β = 0.151, p = 0.246). A strong and independent correlation exists between AIP and cIMT values. Therefore, the AIP could serve as a better marker than the TC/HDL ratio for the detection of subclinical atherosclerosis in AS patients.

Keywords

Ankylosing spondylitis Atherogenic index of plasma Carotid intima-media thickness Subclinical atherosclerosis 

Notes

Compliance with ethical standards

Ethics approval for the study was obtained from the Institutional Review Board at the Necmettin Erbakan University School of Medicine. Signed approval forms were taken from the subjects who participated in the study. This study was conducted in accordance with the updated Declaration of Helsinki.

References

  1. 1.
    McCarey D, Sturrock RD (2009) Comparison of cardiovascular risk in ankylosing spondylitis and rheumatoid arthritis. Clin Exp Rheumatol 27:124–126Google Scholar
  2. 2.
    Klingberg E, Svealv BG, Tang MS, Bech-Hanssen O, Forsblad-d'Elia H, Bergfeldt L (2015) Aortic regurgitation is common in ankylosing spondylitis: time for routine echocardiography evaluation? Am J Med 128:1244–1250CrossRefPubMedGoogle Scholar
  3. 3.
    Peters MJ, van der Horst-Bruinsma IE, Dijkmans BA, Nurmohamed MT (2004) Cardiovascular risk profile of patients with spondylarthropathies, particularly ankylosing spondylitis and psoriatic arthritis. Semin Arthritis Rheum 34:585–592CrossRefPubMedGoogle Scholar
  4. 4.
    Rueda-Gotor J, Llorca J, Corrales A, Blanco R, Fuentevilla P, Portilla V, Exposito R, Mata C, Pina T, Gonzalez-Juanatey C, Gonzalez-Gay MA (2016) Carotid ultrasound in the cardiovascular risk stratification of patients with ankylosing spondylitis: results of a population-based study. Clin Exp Rheumatol 34:885–892PubMedGoogle Scholar
  5. 5.
    Nissen CB, Horslev-Petersen K, Primdahl J (2017) Cardiovascular risk profiles in a hospital-based population of patients with psoriatic arthritis and ankylosing spondylitis: a cross-sectional study. Rheumatol Int 37:113–120CrossRefPubMedGoogle Scholar
  6. 6.
    Heslinga SC, Peters MJ, Ter Wee MM, van der Horst-Bruinsma IE, van Sijl AM, Smulders YM, Nurmohamed MT (2015) Reduction of inflammation drives lipid changes in ankylosing spondylitis. J Rheumatol 42:1842–1845CrossRefPubMedGoogle Scholar
  7. 7.
    Garg N, Krishan P, Syngle A (2015) Rosuvastatin improves endothelial dysfunction in ankylosing spondylitis. Clin Rheumatol 34:1065–1071CrossRefPubMedGoogle Scholar
  8. 8.
    Papagoras C, Voulgari PV, Drosos AA (2013) Atherosclerosis and cardiovascular disease in the spondyloarthritides, particularly ankylosing spondylitis and psoriatic arthritis. Clin Exp Rheumatol 31:612–620PubMedGoogle Scholar
  9. 9.
    Serdaroğlu Beyazal M, Erdoğan T, Türkyılmaz AK, Devrimsel G, Cüre MC, Beyazal M, Sahin I (2016) Relationship of serum osteoprotegerin with arterial stiffness, preclinical atherosclerosis, and disease activity in patients with ankylosing spondylitis. Clin Rheumatol 35:2235–2241CrossRefPubMedGoogle Scholar
  10. 10.
    Ivanova EA, Myasoedova VA, Melnichenko AA, Grechko AV, Orekhov AN (2017) Small dense low-density lipoprotein as biomarker for atherosclerotic diseases. Oxidative Med Cell Longev 2017:1273042CrossRefGoogle Scholar
  11. 11.
    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 (2010) EULAR evidence-based recommendations for cardiovascular risk management in patients with rheumatoid arthritis and other forms of inflammatory arthritis. Ann Rheum Dis 69:325–331CrossRefPubMedGoogle Scholar
  12. 12.
    Tada H, Kawashiri MA, Konno T, Nohara A, Inazu A, Mabuchi H, Yamagishi M, Hayashi K (2016) Prevalence, clinical features, and prognosis of patients with extremely low high-density lipoprotein cholesterol. J Clin Lipidol 10:1311–1317CrossRefPubMedGoogle Scholar
  13. 13.
    Nordestgaard BG (2016) Triglyceride-rich lipoproteins and atherosclerotic cardiovascular disease: new insights from epidemiology, genetics, and biology. Circ Res 118:547–563CrossRefPubMedGoogle Scholar
  14. 14.
    Dobiasova M (2006) AIP—atherogenic index of plasma as a significant predictor of cardiovascular risk: from research to practice. Vnitr Lek 52:64–71PubMedGoogle Scholar
  15. 15.
    Cure E, Icli A, Ugur Uslu A, Aydoğan Baykara R, Sakiz D, Ozucan M, Yavuz F, Arslan S, Cumhur Cure M, Kucuk A (2017) Atherogenic index of plasma may be strong predictor of subclinical atherosclerosis in patients with Behçet disease. Z Rheumatol 76:259–266CrossRefPubMedGoogle Scholar
  16. 16.
    Icli A, Cure E, Uslu AU, Sakiz D, Cure MC, Ozucan M, Baykara RA, Karakoyun A, Balta S, Ozturk C, Arslan S, Kucuk A (2017) The relationship between Atherogenic index and carotid artery atherosclerosis in familial Mediterranean fever. Angiology 68:315–321CrossRefPubMedGoogle Scholar
  17. 17.
    Uslu AU, Kucuk A, Icli A, Cure E, Sakiz D, Arslan S, Baykara RA (2017) Plasma atherogenic index is an independent indicator of subclinical atherosclerosis in systemic lupus erythematosus. Eurasian J Med 49:193–197CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Parveen S, Jacob R, Rajasekhar L, Srinivasa C, Mohan IK (2017) Serum lipid alterations in early rheumatoid arthritis patients on disease modifying anti rheumatoid therapy. Indian J Clin Biochem 32:26–32CrossRefPubMedGoogle Scholar
  19. 19.
    van der Linden S, Valkenburg HA, Cats A (1984) Evaluation of diagnostic criteria for ankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 27:361–368CrossRefPubMedGoogle Scholar
  20. 20.
    Garrett S, Jenkinson T, Kennedy LG (1994) A new approach to defining disease status in ankylosing spondylitis: the bath ankylosing spondylitis disease activity index. J Rheumatol 21:2286–2291PubMedGoogle Scholar
  21. 21.
    Calin A, Garrett S, Whitelock H (1994) A new approach to defining functional ability in ankylosing spondylitis: the development of the bath ankylosing spondylitis functional index. J Rheumatol 21:2281–2285PubMedGoogle Scholar
  22. 22.
    Icli A, Cure E, Cure MC, Uslu AU, Balta S, Mikhailidis DP, Ozturk C, Arslan S, Sakız D, Sahin M, Kucuk A (2016) Endocan levels and subclinical atherosclerosis in patients with systemic lupus erythematosus. Angiology 2016 67:749–755Google Scholar
  23. 23.
    Geçene M, Tuncay F, Borman P, Yücel D, Senes M, Yılmaz BK (2013) Atherosclerosis in male patients with ankylosing spondylitis: the relation with methylenetetrahydrofolate reductase (C677T) gene polymorphism and plasma homocysteine levels. Rheumatol Int 33:1519–1524CrossRefPubMedGoogle Scholar
  24. 24.
    Gupta N, Saigal R, Goyal L, Agrawal A, Bhargava R, Agrawal A (2014) Carotid intima media thickness as a marker of atherosclerosis in ankylosing spondylitis. Int J Rheumatol 2014:839135CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Malesci D, Niglio A, Mennillo GA, Buono R, Valentini G, La Montagna G (2007) High prevalence of metabolic syndrome in patients with ankylosing spondylitis. Clin Rheumatol 26:710–714CrossRefPubMedGoogle Scholar
  26. 26.
    Szabo SM, Levy AR, Rao SR, Kirbach SE, Lacaille D, Cifaldi M, Maksymowych WP (2011) Increased risk of cardiovascular and cerebrovascular diseases in individuals with ankylosing spondylitis: a population-based study. Arthritis Rheum 63:3294–3304CrossRefPubMedGoogle Scholar
  27. 27.
    Divecha H, Sattar N, Rumley A, Cherry L, Lowe GD, Sturrock R (2005) Cardiovascular risk parameters in men with ankylosing spondylitis in comparison with non-inflammatory control subjects: relevance of systemic inflammation. Clin Sci (Lond) 109:171–176CrossRefGoogle Scholar
  28. 28.
    Hung YM, Chang WP, Wei JC, Chou P, Wang PY (2016) Midlife ankylosing spondylitis increases the risk of cardiovascular diseases in males 5 years later: a national population-based study. Medicine (Baltimore) 295:3596CrossRefGoogle Scholar
  29. 29.
    Qian Q, Xu X, He H, Ji H, Zhang H, Ding Y, Dai SM, Zou Y, Zhu Q, Yang C, Ye S, Jiang L, Tang JP, Tong Q, He D, Zhao D, Li Y, Ma Y, Zhou J, Yuan Z, Zhang J, Jin L, Zhou X, Reveille JD, Zou H, Wang J (2017) Clinical patterns and characteristics of ankylosing spondylitis in China. Clin Rheumatol 36:1561–1568CrossRefPubMedGoogle Scholar
  30. 30.
    Han C, Robinson DW Jr, Hackett MV, Paramore LC, Fraeman KH, Bala MV (2006) Cardiovascular disease and risk factors in patients with rheumatoid arthritis, psoriatic arthritis, and ankylosing spondylitis. J Rheumatol 33:2167–2172PubMedGoogle Scholar
  31. 31.
    Keles N, Aksu F, Aciksari G, Yilmaz Y, Demircioglu K, Kostek O, Cekin ME, Kalcik M, Caliskan M (2016) Is triglyceride/HDL ratio a reliable screening test for assessment of atherosclerotic risk in patients with chronic inflammatory disease? North Clin Istanb 3:39–45PubMedPubMedCentralGoogle Scholar
  32. 32.
    Mathieu S, Gossec L, Dougados M, Soubrier M (2011) Cardiovascular profile in ankylosing spondylitis: a systematic review and meta-analysis. Arthritis Care Res (Hoboken) 63:557–563CrossRefGoogle Scholar
  33. 33.
    Halle M, Berg A, Baumstark MW, König D, Huonker M, Keul J (1999) Influence of mild to moderately elevated triglycerides on low density lipoprotein subfraction concentration and composition in healthy men with low high density lipoprotein cholesterol levels. Atherosclerosis 143:185–192CrossRefPubMedGoogle Scholar
  34. 34.
    Pitha J, Kovar J, Skodova Z, Cifkova R, Stavek P, Cervenka L, Sejda T, Lanska V, Poledne R (2015) Association of intima-media thickness of carotid arteries with remnant lipoproteins in men and women. Physiol Res 64:377–384Google Scholar
  35. 35.
    Miller M, Stone NJ, Ballantyne C (2011) Triglycerides and cardiovascular disease: a scientific statement from the American Heart Association. Circulation 123:2292–2333CrossRefPubMedGoogle Scholar
  36. 36.
    Maia DG, Augusto KL, Bezerra MC, Rodrigues CEM (2017) Metabolic syndrome in patients with ankylosing spondylitis receiving anti-TNFα therapy: association with predictors of cardiovascular risk. Clin Rheumatol 36:2371–2376CrossRefPubMedGoogle Scholar
  37. 37.
    Talavera-Garcia E, Delgado-Lista J, Garcia-Rios A, Delgado-Casado N, Gomez-Luna P, Gomez-Garduno A, Gomez-Delgado F, Alcala-Diaz JF, Yubero-Serrano E, Marin C, Perez-Caballero AI, Fuentes-Jimenez FJ, Camargo A, Rodriguez-Cantalejo F, Tinahones FJ, Ordovas JM, Perez-Jimenez F, Perez-Martinez P, Lopez-Miranda J (2016) Influence of obesity and metabolic disease on carotid atherosclerosis in patients with coronary artery disease (CordioPrev study). PLoS One 11:e0153096CrossRefPubMedPubMedCentralGoogle Scholar
  38. 38.
    Annema W, Willemsen HM, de Boer JF, Dikkers A, van der Giet M, Nieuwland W, Muller Kobold AC, van Pelt LJ, Slart RH, van der Horst IC, Dullaart RP, Tio RA, Tietge UJ (2016) HDL function is impaired in acute myocardial infarction independent of plasma HDL cholesterol levels. J Clin Lipidol 10:1318–1328CrossRefPubMedGoogle Scholar
  39. 39.
    Chistiakov DA, Melnichenko AA, Orekhov AN, Bobryshev YV (2017) Paraoxonase and atherosclerosis-related cardiovascular diseases. Biochimie 132:19–27CrossRefPubMedGoogle Scholar
  40. 40.
    Xu H, Qu Y (2017) Correlation of PON1 polymorphisms with ankylosing spondylitis susceptibility: a case-control study in Chinese Han population. Medicine (Baltimore) 96:e7416CrossRefGoogle Scholar
  41. 41.
    Ceccon FT, Azevedo VF, Engelhorn CA, Abdalla DS, Faulin TE, Guarita-Souza LC, Pecoits-Filho R, Faria-Neto JR (2013) Evaluation of sub-clinical atherosclerosis and plasma levels of minimally modified LDL in patients with ankylosing spondylitis and its correlation with disease activity. Rev Bras Reumatol 53:470–475CrossRefPubMedGoogle Scholar
  42. 42.
    Kucuk A, Uğur Uslu A, Icli A, Cure E, Arslan S, Turkmen K, Toker A, Kayrak M (2017) The LDL/HDL ratio and atherosclerosis in ankylosing spondylitis. Z Rheumatol 76:58–63CrossRefPubMedGoogle Scholar
  43. 43.
    Cure MC, Tufekci A, Cure E, Kirbas S, Ogullar S, Kirbas A, Unal H, Yuce S, Cakmak S (2013) Low-density lipoprotein subfraction, carotid artery intima-media thickness, nitric oxide, and tumor necrosis factor alpha are associated with newly diagnosed ischemic stroke. Ann Indian Acad Neurol 16:498–503CrossRefPubMedPubMedCentralGoogle Scholar
  44. 44.
    Tsunoda F, Koba S, Hirano T, Ban Y, Iso Y, Suzuki H, Geshi E, Katagiri T (2004) Association between small dense low-density lipoprotein and postprandial accumulation of triglyceride-rich remnant-like particles in normotriglyceridemic patients with myocardial infarction. Circ J 68:1165–1172CrossRefPubMedGoogle Scholar
  45. 45.
    Arida A, Protogerou AD, Konstantonis G, Konsta M, Delicha EM, Kitas GD, Sfikakis PP (2015) Subclinical atherosclerosis is not accelerated in patients with ankylosing spondylitis with low disease activity: new data and metaanalysis of published studies. J Rheumatol 42:2098–2105CrossRefPubMedGoogle Scholar

Copyright information

© International League of Associations for Rheumatology (ILAR) 2018

Authors and Affiliations

  1. 1.Department of Internal MedicineCamlica Erdem HospitalIstanbulTurkey
  2. 2.Department of CardiologyNecmettin Erbakan UniversityKonyaTurkey
  3. 3.Department of Internal MedicineYunus Emre State HospitalEskisehirTurkey
  4. 4.Department of Endocrinology and Metabolism, Diskapi Training and Research HospitalUniversity of Health SciencesAnkaraTurkey
  5. 5.Department of BiochemistryIstanbul LaboratoryIstanbulTurkey
  6. 6.Department of Physical Medicine and RehabilitationMalatya Training and Research HospitalMalatyaTurkey
  7. 7.Department of Internal MedicineDogubeyazit Doc. Dr. Yasar Eryilmaz State HospitalAgriTurkey
  8. 8.Division of Allergy and Clinical ImmunologyKonya Training and Research HospitalKonyaTurkey
  9. 9.Division of Rheumatology, Department of Internal MedicineNecmettin Erbakan UniversityKonyaTurkey

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