Pentraxin 3 and epicardial fat thickness are independently associated with diabetic retinopathy in diabetic patients

  • Elif TuranEmail author
  • Kadir Kırboğa
  • Yaşar Turan
  • Ayşe Yeşim Göçmen
Original Article


Previous studies have shown that diabetic retinopathy and inflammation are closely related. Pentraxin 3 (PTX3), high-sensitive C-reactive protein (HsCRP), and epicardial fat thickness (EFT) are parameters associated with inflammation. The aim of this cross-sectional study, was to determine if the levels of HsCRP, PTX3, and EFT were predictors or markers for diabetic retinopathy (DR). Cross-sectional study, 40 normal, nondiabetic subjects (group1), 50 type 2 diabetic patients without DR (group2), and 110 type 2 diabetic patients with DR (group3) were included. PTX3 and HsCRP concentrations were measured and transthoracic echocardiography was used to measure EFT. ANOVA and the post hoc multiple comparisons showed that differences among group 1 and group 2 and also among group 2 and group 3 for PTX3 (p < 0.01 and p = 0.018, respectively), for HsCRP (p < 0.01 and p = 0.042, respectively), and for EFT (p < 0.01 and p = 0.021, respectively) were statistically significant. The difference in serum creatinine was statistically significant only among group 2 and group 3 (p < 0.01). Diabetes duration (OR = 1.116, p < 0.01), PTX3 (OR = 8.516, p = 0.039), EFT (OR = 1.444, p = 0.02), and serum creatinine level (OR = 15.45, p = 0.015) have independent association with DR. Besides, the well-known factors such as diabetes duration and serum creatinine, PTX3, as a marker of inflammation, and EFT, as a marker of inflammation and vascular damage, were independently associated with DR in diabetic patients. Clinical trial number: 20.03.2015/30


Diabetic retinopathy Pentraxin 3 HsCRP Epicardial fat tissue 



This study was funded by the Scientific Research Projects of the University of Bozok.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the Bozok University Clinical Research Ethics Committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

This article does not contain any studies with animals performed by any of the authors.

Informed consent

Informed consent was obtained from all individual participants included in the study.


  1. 1.
    Klein BE. Overview of epidemiologic studies of diabetic retinopathy. Ophthalmic Epidemiol. 2007;14(4):179–83. Scholar
  2. 2.
    Mallika P, Lee P, Cheah W, Wong J, Syed Alwi S, Nor Hayati H, et al. Risk factors for diabetic retinopathy in diabetics screened using fundus photography at a primary health care setting in East Malaysia. Malaysian family physician : the official journal of the Academy of Family Physicians of Malaysia. 2011;6(2–3):60–5.Google Scholar
  3. 3.
    Ando T, Henmi T, Haruta D, Haraguchi A, Ueki I, Horie I, et al. Graves’ disease complicated by ventricular fibrillation in three men who were smokers. Thyroid : official journal of the American Thyroid Association. 2011;21(9):1021–5. Scholar
  4. 4.
    Pradhan AD, Manson JE, Rifai N, Buring JE, Ridker PM. C-reactive protein, interleukin 6, and risk of developing type 2 diabetes mellitus. Jama. 2001;286(3):327–34.CrossRefPubMedCentralGoogle Scholar
  5. 5.
    Mugabo Y, Li L, Renier G. The connection between C-reactive protein (CRP) and diabetic vasculopathy. Focus on preclinical findings. Curr Diabetes Rev. 2010;6(1):27–34.CrossRefPubMedCentralGoogle Scholar
  6. 6.
    Wang X, Dai Y, Chen X. Changes of the concentration of serum adiponectin and high sensitivity C-reactive protein in type 2 diabetes mellitus patients with retinopathy. International Journal of Ophthalmology. 2010;10:1699–701.Google Scholar
  7. 7.
    Du J-H, Li X, Li R, Xu L, Ma R-R, Liu S-F, et al. Elevation of serum apelin-13 associated with proliferative diabetic retinopathy in type 2 diabetic patients. International journal of ophthalmology. 2014;7(6):968–73.PubMedPubMedCentralGoogle Scholar
  8. 8.
    Brown DW, Giles WH, Croft JB. White blood cell count: an independent predictor of coronary heart disease mortality among a national cohort. J Clin Epidemiol. 2001;54(3):316–22.CrossRefPubMedCentralGoogle Scholar
  9. 9.
    Fazzini F, Peri G, Doni A, Dell'Antonio G, Dal Cin E, Bozzolo E, et al. PTX3 in small-vessel vasculitides: an independent indicator of disease activity produced at sites of inflammation. Arthritis Rheum. 2001;44(12):2841–50.CrossRefPubMedCentralGoogle Scholar
  10. 10.
    Saygi S, Kirilmaz B, Tengiz I, Turk UO, Yildiz H, Tuzun N, et al. Long pentraxin-3 measured at late phase associated with GRACE risk scores in patients with non-ST elevation acute coronary syndrome and coronary stenting. Turk Kardiyoloji Dernegi arsivi : Turk Kardiyoloji Derneginin yayin organidir. 2012;40(3):205–12. Scholar
  11. 11.
    Peri G, Introna M, Corradi D, Iacuitti G, Signorini S, Avanzini F, et al. PTX3, a prototypical long pentraxin, is an early indicator of acute myocardial infarction in humans. Circulation. 2000;102(6):636–41.CrossRefPubMedCentralGoogle Scholar
  12. 12.
    Latini R, Maggioni AP, Peri G, Gonzini L, Lucci D, Mocarelli P, et al. Prognostic significance of the long pentraxin PTX3 in acute myocardial infarction. Circulation. 2004;110(16):2349–54. Scholar
  13. 13.
    Bevelacqua V, Libra M, Mazzarino MC, Gangemi P, Nicotra G, Curatolo S, Massimino D, Plumari A, Merito P, Valente G, Stivala F, La Greca S, Malaponte G (2006) Long pentraxin 3: a marker of inflammation in untreated psoriatic patients. Int J Mol Med 18 (3):415–423.Google Scholar
  14. 14.
    Inoue K, Sugiyama A, Reid PC, Ito Y, Miyauchi K, Mukai S, et al. Establishment of a high sensitivity plasma assay for human pentraxin3 as a marker for unstable angina pectoris. Arterioscler Thromb Vasc Biol. 2007;27(1):161–7. Scholar
  15. 15.
    Suzuki S, Takeishi Y, Niizeki T, Koyama Y, Kitahara T, Sasaki T, et al. Pentraxin 3, a new marker for vascular inflammation, predicts adverse clinical outcomes in patients with heart failure. Am Heart J. 2008;155(1):75–81. Scholar
  16. 16.
    Matsubara J, Sugiyama S, Nozaki T, Sugamura K, Konishi M, Ohba K, et al. Pentraxin 3 is a new inflammatory marker correlated with left ventricular diastolic dysfunction and heart failure with normal ejection fraction. J Am Coll Cardiol. 2011;57(7):861–9. Scholar
  17. 17.
    Balta S, Demirkol S, Kurt O, Sarlak H, Akhan M. Epicardial adipose tissue measurement: inexpensive, easy accessible and rapid practical method. Anadolu kardiyoloji dergisi : AKD = the Anatolian journal of cardiology. 2013;13(6):611. Scholar
  18. 18.
    Katsiki N, Mikhailidis DP, Wierzbicki AS. Epicardial fat and vascular risk: a narrative review. Curr Opin Cardiol. 2013;28(4):458–63. Scholar
  19. 19.
    Iacobellis G, Malavazos AE, Corsi MM. Epicardial fat: from the biomolecular aspects to the clinical practice. Int J Biochem Cell Biol. 2011;43(12):1651–4. Scholar
  20. 20.
    Iacobellis G, Ribaudo MC, Assael F, Vecci E, Tiberti C, Zappaterreno A, et al. Echocardiographic epicardial adipose tissue is related to anthropometric and clinical parameters of metabolic syndrome: a new indicator of cardiovascular risk. J Clin Endocrinol Metab. 2003;88(11):5163–8. Scholar
  21. 21.
    Dubin R, Li Y, Ix JH, Shlipak MG, Whooley M, Peralta CA. Associations of pentraxin-3 with cardiovascular events, incident heart failure, and mortality among persons with coronary heart disease: data from the heart and soul study. Am Heart J. 2012;163(2):274–9.CrossRefPubMedCentralGoogle Scholar
  22. 22.
    Manfredi AA, Rovere-Querini P, Bottazzi B, Garlanda C, Mantovani A. Pentraxins, humoral innate immunity and tissue injury. Curr Opin Immunol. 2008;20(5):538–44.CrossRefPubMedCentralGoogle Scholar
  23. 23.
    Kocyigit I, Eroglu E, Orscelik O, Unal A, Gungor O, Ozturk F, et al. Pentraxin 3 as a novel bio-marker of inflammation and endothelial dysfunction in autosomal dominant polycystic kidney disease. Journal of nephrology. 2014;27(2):181–6.CrossRefPubMedCentralGoogle Scholar
  24. 24.
    Kume N, Mitsuoka H, Hayashida K, Tanaka M. Pentraxin 3 as a biomarker for acute coronary syndrome: comparison with biomarkers for cardiac damage. J Cardiol. 2011;58(1):38–45.CrossRefPubMedCentralGoogle Scholar
  25. 25.
    Yu HI, Sheu W, Song YM, Liu HC, Lee WJ, Chen YT. C-reactive protein and risk factors for peripheral vascular disease in subjects with type 2 diabetes mellitus. Diabet Med. 2004;21(4):336–41.CrossRefPubMedCentralGoogle Scholar
  26. 26.
    Yang HS, Woo JE, Lee SJ, Park SH, Woo JM. Elevated plasma pentraxin 3 levels are associated with development and progression of diabetic retinopathy in Korean patients with type 2 diabetes mellitus. Invest Ophthalmol Vis Sci. 2014;55(9):5989–97.CrossRefPubMedCentralGoogle Scholar
  27. 27.
    Zhou W, Hu W. Serum and vitreous pentraxin 3 concentrations in patients with diabetic retinopathy. Genetic testing and molecular biomarkers. 2016;20(3):149–53.CrossRefPubMedCentralGoogle Scholar
  28. 28.
    Yamasaki K, Kurimura M, Kasai T, Sagara M, Kodama T, Inoue K. Determination of physiological plasma pentraxin 3 (PTX3) levels in healthy populations. Clin Chem Lab Med. 2009;47(4):471–7. Scholar
  29. 29.
    Talman AH, Psaltis PJ, Cameron JD, Meredith IT, Seneviratne SK, Wong DT. Epicardial adipose tissue: far more than a fat depot. Cardiovascular diagnosis and therapy. 2014;4(6):416–29.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Verhagen SN, Visseren FL. Perivascular adipose tissue as a cause of atherosclerosis. Atherosclerosis. 2011;214(1):3–10. Scholar
  31. 31.
    Akbas EM, Hamur H, Demirtas L, Bakirci EM, Ozcicek A, Ozcicek F, et al. Predictors of epicardial adipose tissue in patients with type 2 diabetes mellitus. Diabetology & metabolic syndrome. 2014;6(1):55.CrossRefGoogle Scholar
  32. 32.
    Wang CP, Hsu HL, Hung WC, Yu TH, Chen YH, Chiu CA, et al. Increased epicardial adipose tissue (EAT) volume in type 2 diabetes mellitus and association with metabolic syndrome and severity of coronary atherosclerosis. Clin Endocrinol. 2009;70(6):876–82.CrossRefGoogle Scholar
  33. 33.
    Chatterjee TK, Stoll LL, Denning GM, Harrelson A, Blomkalns AL, Idelman G, et al. Proinflammatory phenotype of perivascular adipocytes: influence of high-fat feeding. Circ Res. 2009;104(4):541–9. Scholar
  34. 34.
    Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, et al. Human epicardial adipose tissue is a source of inflammatory mediators. Circulation. 2003;108(20):2460–6. Scholar
  35. 35.
    Stram DA, Jiang X, Varma R, Torres M, Burkemper BS, Choudhury F, et al. Factors associated with prevalent diabetic retinopathy in Chinese Americans: the Chinese American Eye Study. Ophthalmology retina. 2018;2(2):96–105. Scholar
  36. 36.
    Zhang G, Chen H, Chen W, Zhang M. Prevalence and risk factors for diabetic retinopathy in China: a multi-hospital-based cross-sectional study. Br J Ophthalmol. 2017;101(12):1591–5. Scholar
  37. 37.
    Tokgözoğlu L. Ateroskleroz ve enflamasyonun rolü. Türk Kardiyol Dern Arş. 2009;4:1–6.Google Scholar

Copyright information

© Research Society for Study of Diabetes in India 2018

Authors and Affiliations

  1. 1.School of Medicine, Division of Endocrinology and MetabolismBozok UniversityYozgatTurkey
  2. 2.School of Medicine, Division of OphthalmologyBozok UniversityYozgatTurkey
  3. 3.School of Medicine, Division of CardiologyBozok UniversityYozgatTurkey
  4. 4.School of Medicine, Division BiochemistryBozok UniversityYozgatTurkey

Personalised recommendations