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The LDL/HDL ratio and atherosclerosis in ankylosing spondylitis

Das Verhältnis von LDL zu HDL und Atherosklerose bei ankylosierender Spondylitis

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Abstract

Objectives

In ankylosing spondylitis (AS) patients, cardiac and vascular involvement may manifest as atherosclerosis and coronary artery disease. Systemic inflammation, oxidative stress, increased low-density lipoprotein (LDL) cholesterol and decreased high-density lipoprotein (HDL) cholesterol constitute a significant risk for atherosclerosis. This study investigated the relationship between carotid intima–media thickness (CIMT), LDL/HDL ratio, total oxidant status (TOS; an indicator of oxidative stress) and ischemic modified albumin (IMA; an ischemic marker in AS patients).

Patients and methods

Sixty AS patients were diagnosed using the Modified New York Criteria; 54 age- and gender-matched participants were included as controls. CIMT, LDL/HDL ratio, TOS and IMA were measured using the most appropriate methods.

Results

IMA was higher in AS patients compared to controls (p < 0.0001). TOS was also increased in AS patients (p = 0.005); as was CIMT (p < 0.0001). The LDL/HDL ratio was also greater in AS patients compared to controls (p = 0.047). A positive correlation was found between CIMT and LDL/HDL ratio among AS patients.

Conclusion

Elevated CIMT, IMA and TOS levels suggest an increased risk of atherosclerotic heart disease in AS patients. The LDL/HDL ratio was higher in AS patients compared to controls, and there was a correlation between LDL/HDL ratio and CIMT, albeit statistically weak. Therefore, the LDL/HDL ratio is not a reliable marker to predict atherosclerotic heart disease in AS patients.

Zusammenfassung

Ziel

Bei Patienten mit Spondylitis ankylosans (AS) kann sich eine kardiale und vaskuläre Beteiligung als Atherosklerose und koronare Herzkrankheit (KHK) manifestieren. Systemische Entzündung, oxidativer Stress, erhöhtes Low-Density-Lipoprotein(LDL)-Cholesterin und vermindertes High-Density-Lipoprotein(HDL)-Cholesterin stellen ein signifikantes Risiko für Atherosklerose dar. In der vorliegenden Studie wird die Beziehung zwischen Karotis-Intima-Media-Dicke (CIMT), LDL-HDL-Quotient, totalem oxidativem Status (TOS, Indikator für oxidativen Stress) und ischämiemodifiziertem Albumin (IMA, Ischämiemarker bei AS-Patienten) untersucht.

Patienten und Methoden

Anhand der Modified New York Criteria erfolgte die Diagnosestellung bei 60 AS-Patienten; Kontrollen waren 54 in Alter und Geschlecht entsprechende Personen. CIMT, LDL/HDL-Quotient, TOS und IMA wurden mit den am besten geeigneten Methoden ermittelt.

Ergebnisse

IMA war bei AS-Patienten höher als bei den Kontrollen (p < 0,0001). Auch TOS war bei AS-Patienten erhöht (p = 0,005) sowie CIMT (p < 0,0001). Der LDL/HDL-Quotient war bei AS-Patienten ebenfalls größer als bei den Kontrollen (p = 0,047). Es fand sich eine positive Korrelation zwischen CIMT und LDL/HDL-Quotient bei AS-Patienten.

Schlussfolgerung

Erhöhte Werte für CIMT, IMA und TOS sprechen für ein erhöhtes Risiko einer KHK bei AS-Patienten. Der LDL/HDL-Quotient war bei AS-Patienten höher als bei den Kontrollen, und es bestand eine – allerdings schwache – Korrelation zwischen dem LDL/HDL-Quotienten und CIMT. Folglich ist der LDL/HDL-Quotient kein reliabler Marker zur Vorhersage einer KHK bei AS-Patienten.

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References

  1. Daikh DI, Chen PP (2014) Advances in managing ankylosing spondylitis. F1000PrimeRep 6:78

    Google Scholar 

  2. Maghraoui A El (2011) Extra-articular manifestations of ankylosing spondylitis: prevalence, characteristics and therapeutic implications. Eur J Intern Med 22:554–560

    Article  PubMed  Google Scholar 

  3. Essers I, Stolwijk C, Boonen A et al (2016) Ankylosing spondylitis and risk of ischaemic heart disease: apopulation-based cohort study. Ann Rheum Dis 75:203–209

    Article  PubMed  Google Scholar 

  4. Katakami N, Kaneto H, Shimomura I (2014) Carotid ultrasonography: A potent tool for better clinical practice in diagnosis of atherosclerosis in diabetic patients. J Diabetes Investig 5:3–13

    Article  PubMed  Google Scholar 

  5. Yang C, Sun Z, Li Y et al (2014) The correlation between serum lipid profile with carotid intima-media thickness and plaque. Bmc Cardiovasc 14:181

    Article  CAS  Google Scholar 

  6. Garcia-Gomez C, Bianchi M, Fuente D de la et al (2014) Inflammation, lipid metabolism and cardiovascular risk in rheumatoidarthritis: A qualitative relationship? World J Orthop 5:304–311

    Article  PubMed  PubMed Central  Google Scholar 

  7. Halm VP van, Denderen JC van, Peters MJet al (2006) Increased disease activity is associated with a deteriorated lipid profile inpatients with ankylosing spondylitis. Ann Rheum Dis 65:1473–1477

    Article  PubMed  PubMed Central  Google Scholar 

  8. Wan AWN, Sakri F, MokhsinAet al (2015) Low serum high density lipoproteincholesterol concentration is an independent predictor for enhanced inflammationand endothelial activation. PLOS ONE 10:0116867

    Google Scholar 

  9. Zhong Y, Wang N, Xu H et al (2012) Ischemia-modified albumin instable coronary atherosclerotic heart disease: clinical diagnosis and riskstratification. Coron Artery Dis 23:538–541

    Article  PubMed  Google Scholar 

  10. Linden S van der, Valkenburg HA, Cats A (1984) Evaluation of diagnostic criteria forankylosing spondylitis. A proposal for modification of the New York criteria. Arthritis Rheum 27:361–368

    Article  PubMed  Google Scholar 

  11. Bar-Or D, Lau E, Winkler JV (2000) A novel assay for cobalt-albumin binding and its potential as a marker for myocardial ischemia – a preliminary report. J Emerg Med 19:311–315

    Article  CAS  PubMed  Google Scholar 

  12. Erel O (2005) A new automated colorimetric method for measuring total oxidantstatus. Clin Biochem 38:1103–1111

    Article  CAS  PubMed  Google Scholar 

  13. Gianturco L, Bodini BD, Atzeni Fet al (2015) Cardiovascular and autoimmune diseases in females: The role of microvasculature and dysfunctional endothelium. Atherosclerosis 241:259–263

    Article  CAS  PubMed  Google Scholar 

  14. Nimkuntod P, Tongdee P (2015) Plasma low-density lipoprotein cholesterol/high-density lipoprotein cholesterol concentration ratio and early marker of carotid artery atherosclerosis. J Med Assoc Thai 98:58–63

    Google Scholar 

  15. Limbu YR, Rajbhandari R, Sharma R et al (2015) Carotid intima-media thickness (CIMT) and carotid plaques in young Nepalesepatients with angiographically documented coronary artery disease. Cardiovasc Diagn Ther 5:1–7

    PubMed  PubMed Central  Google Scholar 

  16. Gupta N, Saigal R, Goyal L et al (2014) Carotid intimamedia thickness as a marker of atherosclerosis in ankylosing spondylitis. Int Jrheumatol 2014:839135

    Google Scholar 

  17. Gonzalez-Juanatey C, Vazquez-Rodriguez TR, Miranda-Filloy JA et al (2009) The high prevalence ofsubclinical atherosclerosis in patients with ankylosing spondylitis withoutclinically evident cardiovascular disease. Medicine (Baltimore) 88:358–365

    Article  Google Scholar 

  18. Mathieu S, Joly H, Baron Get al (2008) Trend towards increased arterial stiffness or intima-media thickness in ankylosing spondylitis patients without clinically evident cardiovasculardisease. Rheumatology (Oxford) 47:1203–1207

    Article  CAS  Google Scholar 

  19. Takata K, Imaizumi S, Kawachi Eet al (2014) Impact of cigarette smoking cessation on high-density lipoprotein functionality. Circ J 78:2955–2962

    Article  PubMed  Google Scholar 

  20. Divecha H, Sattar N, Rumley A et al (2005) Cardiovascular risk parameters in men with ankylosing spondylitis in comparison with non-inflammatory control subjects: relevance of systemic inflammation. Clin Sci (Lond) 109:171–176

    Article  CAS  Google Scholar 

  21. Mathieu S, Gossec L, Dougados M et al (2014) Cardiovascular profile inankylosing spondylitis: a systematic review and meta-analysis. Arthritis Care Res 63:557–563

    Article  Google Scholar 

  22. Sathiya R, Velu VK, Niranjan Get al (2014) A comparative study of serum uric acid levels and lipid ratios incoronary artery disease patients. Int J Biomed Sci 10:124–128

    CAS  PubMed  PubMed Central  Google Scholar 

  23. Karkucak M, Capkin E, Alver A et al (2010) The effect of anti-TNF agent on oxidation status in patients with ankylosingspondylitis. ClinRheumatol 29:303–307

    Google Scholar 

  24. Stanek A, Cieslar G, Romuk E et al (2010) Decrease in antioxidant status of plasma and erythrocytes from patientswith ankylosing spondylitis. Clin Biochem 43:566–570

    Article  CAS  PubMed  Google Scholar 

  25. Karakoc M, Altindag O, Keles H et al (2007) Serumoxidative-antioxidative status in patients with ankylosing spondilitis. Rheumatol Int 27:1131–1134

    Article  CAS  PubMed  Google Scholar 

  26. Sloten TT van, Henry RM, Dekker JM et al (2014) Endothelial dysfunction plays a key role in increasing cardiovascular risk intype 2 diabetes: the Hoorn study. Hypertension 64:1299–1305

    Article  PubMed  Google Scholar 

  27. Jerkic M, Letarte M (2015) Contribution of oxidative stress to endothelialdysfunction in hereditary hemorrhagic telangiectasia. Front Genet 6:34

    Article  PubMed  PubMed Central  Google Scholar 

  28. Ali OS, Abdelgawad HM, Mohammed MS et al (2014) Ischemic heart diseases in Egypt: role of xanthine oxidase system and ischemia-modified albumin. Heart Vessels 29:629–637

    Article  PubMed  Google Scholar 

  29. Leitemperguer MR, Tatsch E, Kober H et al (2014) Assessment of ischemia-modified albumin levels in patients with rheumatoidarthritis. Clin Lab 60:1065–1070

    CAS  PubMed  Google Scholar 

  30. Montagnana M, Lippi G, Volpe Aet al (2014) Evaluation of cardiac laboratory markers in patients with systemicsclerosis. Clin Biochem 39:913–917

    Article  Google Scholar 

  31. Szabo SM, Levy AR, Rao SRet al (2011) Increased risk of cardiovascular and cerebrovascular diseases in individuals withankylosing spondylitis: a population-based study. Arthritis Rheum 63:3294–3304

    Article  PubMed  Google Scholar 

  32. Valente RL, Valente JM, Castro GR de et al (2013) Subclinical atherosclerosis in ankylosing spondylitis: is there a role forinflammation? Rev Bras Reumatol 53:377–381

    Article  PubMed  Google Scholar 

  33. Şerban C, Dragan S (2014) The relationship between inflammatory and oxidative stressbiomarkers, atherosclerosis and rheumatic diseases. Curr Pharm Des 20:585–600

    Article  PubMed  Google Scholar 

  34. Cure MC, Tufekci A, Cure E et al (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 16:498–503

    Article  PubMed  PubMed Central  Google Scholar 

  35. Toth PP, Patti AM, Nikolic D et al (2016) Bergamot reduces plasma lipids, atherogenic small dense LDL, and subclinical atherosclerosis in subjects with moderate hypercholesterolemia: a 6 months prospective study. Front Pharmacol 6:299

    Article  PubMed  PubMed Central  Google Scholar 

  36. Saleheen D, Scott R, Javad S et al (2015) Association of HDL cholesterol efflux capacity with incident coronary heart disease events: a prospective case-control study. Lancet Diabetes Endocrinol 3:507–513

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Icli A, Cure E, Cure MC et al (2015) Endocan levels and subclinical atherosclerosis in patients with systemic lupus erythematosus. Angiology. doi:10.1177/0003319715616240

    Google Scholar 

  38. Marsillach J, Becker JO, Vaisar T et al (2015) Paraoxonase-3 is depleted from the high-density lipoproteins of autoimmune disease patients with subclinical atherosclerosis. J Proteome Res 14:2046–2054

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Ronda N, Favari E, Borghi MO et al (2014) Impaired serum cholesterol efflux capacity in rheumatoid arthritis and systemic lupus erythematosus. Ann Rheum Dis 73:609–615

    Article  PubMed  Google Scholar 

  40. Shah AS, Urbina EM, Khoury PR et al (2013) Lipids and lipoprotein ratios: contribution to carotid intima media thickness in adolescents and young adults with type 2 diabetes mellitus. J Clin Lipidol 7:441–445

    Article  PubMed  PubMed Central  Google Scholar 

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Author information

Authors and Affiliations

  1. Division of Rheumatology, Department of Internal Medicine, Meram School of Medicine, Necmettin Erbakan University, Konya, Turkey

    A. Kucuk

  2. Eskişehir Military Hospital, Eskisehir, Rize, Turkey

    A. Uğur Uslu

  3. Necmettin Erbakan University, Konya, Turkey

    A. Icli, S. Arslan, K. Turkmen, A. Toker & M. Kayrak

  4. Recep Tayyip Erdogan University, Rize, Turkey

    E. Cure

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  1. A. Kucuk
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Correspondence to A. Kucuk.

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Conflict of interest

A. Kucuk, A. Ugur Uslu, A. Icli, E. Cure, S. Arslan, K. Turkmen, A. Toker and M. Kayrak state that there are no conflicts of interest.

The Ethics Committee for Clinical Research of Necmettin Erbakan University Faculty of Medicine approved the present study.

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U. Müller-Ladner, Bad Nauheim

U. Lange, Bad Nauheim

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Kucuk, A., Uğur Uslu, A., Icli, A. et al. The LDL/HDL ratio and atherosclerosis in ankylosing spondylitis. Z Rheumatol 76, 58–63 (2017). https://doi.org/10.1007/s00393-016-0092-4

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