Top

Published in:

Open Access 01-12-2014 | Research

Predictors of epicardial adipose tissue in patients with type 2 diabetes mellitus

Authors: Emin M Akbas, Hikmet Hamur, Levent Demirtas, Eftal M Bakirci, Adalet Ozcicek, Fatih Ozcicek, Ufuk Kuyrukluyildiz, Kultigin Turkmen

Published in: Diabetology & Metabolic Syndrome | Issue 1/2014

Abstract

Background

Epicardial adipose tissue (EAT), visceral fat depot of the heart, was found to be associated with coronary artery disease in cardiac and non-cardiac patients. Platelet-to-lymphocyte ratio (PLR) and neutrophil-to-lymphocyte ratio (NLR) were introduced as potential markers to determine inflammation in various disorders. Recently, atherogenic index of plasma (AIP) was found to be closely associated with atherosclerosis in general population. Waist circumference is commonly used to assess the risk factors in various metabolic disorders. There has been a well known relation between inflammation and peripheral adipose tissue in diabetes mellitus. However, the data regarding EAT and inflammation is scant in this population. Hence, we aimed to determine the relationship between PLR, NLR, AIP, waist circumference and EAT in diabetic patients.

Methods

This was a cross-sectional study involving 156 patients with type 2 diabetes mellitus (87 females, 69 males; mean age, 53.62 ± 9.33 years) and 50 control subjects (35 females, 15 males; mean age, 51.06 ± 8.74 years). EAT was measured by using a trans-thoracic echocardiogram. Atherogenic index of plasma was calculated as the logarithmically transformed ratio of the serum triglyceride to high density lipoprotein (HDL)cholesterol. NLR and PLR were calculated as the ratio of the neutrophils and platelets to lymphocytes, respectively.

Results

Waist circumference, PLR, NLR, AIP and EAT measurements were significantly higher in diabetic patients when compared to control subjects. When diabetic patients were separated into two groups according to their median value of EAT (Group 1, EAT < 4.53 (n = 78) and group 2, EAT ≥4.53 (n = 78)), group 2 patients had significantly higher Body mass index (BMI), waist circumference, AIP, NLR and PLR levels. In the bivariate correlation analysis, EAT was positively correlated with PLR, NLR, AIP, BMI and waist circumference (r = 0.197, p = 0.014; r = 0.229, p = 0.004; r = 0.161, p = 0.044; r = 0.248, p = 0.002; r = 0.306, p < 0.001, respectively). Waist circumference was found to be independent variables of EAT.

Conclusions

Simple calculation of PLR and measurement of waist circumference were found to be associated with increased EAT in diabetic patients.

Coutinho M, Gerstein HC, Wang Y, Yusuf S: The relationship between glucose and incident cardiovascular events. A metaregression analysis of published data from 20 studies of 95,783 individuals followed for 12.4 years. Diabetes Care. 1999, 22 (2): 233-240. 10.2337/diacare.22.2.233.CrossRefPubMed

DeFronzo RA, Ferrannini E: Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care. 1991, 14 (3): 173-194. 10.2337/diacare.14.3.173.CrossRefPubMed

Paneni F, Beckman JA, Creager MA, Cosentino F: Diabetes and vascular disease: pathophysiology, clinical consequences, and medical therapy: part I. Eur Heart J. 2013, 34 (31): 2436-2443. 10.1093/eurheartj/eht149. PubMed PMID: 23641007. Pubmed Central PMCID: 3743069. Epub 2013/05/04. engPubMedCentralCrossRefPubMed

Baker AR, Silva NF, Quinn DW, Harte AL, Pagano D, Bonser RS, Kumar S, McTernan PG: Human epicardial adipose tissue expresses a pathogenic profile of adipocytokines in patients with cardiovascular disease. Cardiovasc Diabetol. 2006, 5: 1-10.1186/1475-2840-5-1. PubMed PMID: 16412224. Pubmed Central PMCID: 1352345. Epub 2006/01/18. engPubMedCentralCrossRefPubMed

Turkmen K, Erdur FM, Ozcicek F, Ozcicek A, Akbas EM, Ozbicer A, Demirtas L, Turk S, Tonbul HZ: Platelet-to-lymphocyte ratio better predicts inflammation than neutrophil-to-lymphocyte ratio in end-stage renal disease patients. Hemodial Int. 2013, 17 (3): 391-396. 10.1111/hdi.12040. PubMed PMID: 23522328CrossRefPubMed

He W, Yin C, Guo G, Jiang C, Wang F, Qiu H, Chen X, Rong R, Zhang B, Xia L: Initial neutrophil lymphocyte ratio is superior to platelet lymphocyte ratio as an adverse prognostic and predictive factor in metastatic colorectal cancer. Med Oncol. 2013, 30 (1): 439-PubMed PMID: 23307251. Epub 2013/01/12. engCrossRefPubMed

Seidell JC, Perusse L, Despres JP, Bouchard C: Waist and hip circumferences have independent and opposite effects on cardiovascular disease risk factors: the Quebec Family Study. Am J Clin Nutr. 2001, 74 (3): 315-321. PubMed PMID: 11522554. Epub 2001/08/28. engPubMed

Stevens J, Couper D, Pankow J, Folsom AR, Duncan BB, Nieto FJ, Jones D, Tyroler HA: Sensitivity and specificity of anthropometrics for the prediction of diabetes in a biracial cohort. Obes Res. 2001, 9 (11): 696-705. 10.1038/oby.2001.94. PubMed PMID: 11707536. Epub 2001/11/15. engCrossRefPubMed

Sargeant LA, Bennett FI, Forrester TE, Cooper RS, Wilks RJ: Predicting incident diabetes in Jamaica: the role of anthropometry. Obes Res. 2002, 10 (8): 792-798. 10.1038/oby.2002.107. PubMed PMID: 12181388. Epub 2002/08/16. engCrossRefPubMed

10.

Frohlich J, Dobiasova M: Fractional esterification rate of cholesterol and ratio of triglycerides to HDL-cholesterol are powerful predictors of positive findings on coronary angiography. Clin Chem. 2003, 49 (11): 1873-1880. 10.1373/clinchem.2003.022558. PubMed PMID: 14578319CrossRefPubMed

11.

Grundy SM, Cleeman JI, Merz CN, Brewer HB, Clark LT, Hunninghake DB, Pasternak RC, Smith SC, Stone NJ, Coordinating Committee of the National Cholesterol Education Program: Implications of recent clinical trials for the National cholesterol education program adult treatment panel III guidelines. J Am Coll Cardiol. 2004, 44 (3): 720-732. 10.1016/j.jacc.2004.07.001. PubMed PMID: 15358046CrossRefPubMed

12.

Cockcroft DW, Gault MH: Prediction of creatinine clearance from serum creatinine. Nephron. 1976, 16 (1): 31-41. 10.1159/000180580. PubMed PMID: 1244564. Epub 1976/01/01. engCrossRefPubMed

13.

Dobiasova M, Frohlich J, Sedova M, Cheung MC, Brown BG: Cholesterol esterification and atherogenic index of plasma correlate with lipoprotein size and findings on coronary angiography. J Lipid Res. 2011, 52 (3): 566-571. 10.1194/jlr.P011668. PubMed PMID: 21224290. Pubmed Central PMCID: 3035693PubMedCentralCrossRefPubMed

14.

Yosefy C: Hyperglycaemia and its relation to cardiovascular morbidity and mortality: has it been resolved?. Acta Diabetol. 2003, 40 (Suppl 2): S380-S388. PubMed PMID: 14704873. Epub 2004/01/06. engCrossRefPubMed

15.

Pitsavos C, Tampourlou M, Panagiotakos DB, Skoumas Y, Chrysohoou C, Nomikos T, Stefanadis C: Association between low-grade systemic inflammation and type 2 diabetes mellitus among men and women from the ATTICA study. Rev Diabet Stud. 2007, Summer; 4 (2): 98-104. PubMed PMID: 17823694. Pubmed Central PMCID: 2036265. Epub 2007/09/08. engCrossRefPubMed

16.

Sena CM, Pereira AM, Seica R: Endothelial dysfunction - a major mediator of diabetic vascular disease. Biochim Biophys Acta. 2013, 1832 (12): 2216-2231. 10.1016/j.bbadis.2013.08.006. PubMed PMID: 23994612. Epub 2013/09/03. EngCrossRefPubMed

17.

Rajala MW, Scherer PE: Minireview: the adipocyte–at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology. 2003, 144 (9): 3765-3773. 10.1210/en.2003-0580. PubMed PMID: 12933646. Epub 2003/08/23. engCrossRefPubMed

18.

Nguyen DV, Shaw LC, Grant MB: Inflammation in the pathogenesis of microvascular complications in diabetes. Front Endocrinol (Lausanne). 2012, 3: 170-PubMed PMID: 23267348. Pubmed Central PMCID: 3527746. Epub 2012/12/26. eng

19.

Koyama H, Maeno T, Fukumoto S, Shoji T, Yamane T, Yokoyama H, Emoto M, Tahara H, Inaba M, Hino M, Shioi A, Miki T, Nishizawa Y: Platelet P-selectin expression is associated with atherosclerotic wall thickness in carotid artery in humans. Circulation. 2003, 108 (5): 524-529. 10.1161/01.CIR.0000081765.88440.51. PubMed PMID: 12860908. Epub 2003/07/16. engCrossRefPubMed

20.

Shoji T, Koyama H, Fukumoto S, Maeno T, Yokoyama H, Shinohara K, Emoto M, Yamane T, Hino M, Shioi A, Nishizawa Y: Platelet activation is associated with hypoadiponectinemia and carotid atherosclerosis. Atherosclerosis. 2006, 188 (1): 190-195. 10.1016/j.atherosclerosis.2005.10.034. PubMed PMID: 16313909. Epub 2005/11/30. engCrossRefPubMed

21.

Imtiaz F, Shafique K, Mirza SS, Ayoob Z, Vart P, Rao S: Neutrophil lymphocyte ratio as a measure of systemic inflammation in prevalent chronic diseases in Asian population. Int Arch Med. 2012, 5 (1): 2-10.1186/1755-7682-5-2. PubMed PMID: 22281066. Pubmed Central PMCID: 3277482PubMedCentralCrossRefPubMed

22.

Borissoff JI, Spronk HM, ten Cate H: The hemostatic system as a modulator of atherosclerosis. N Engl J Med. 2011, 364 (18): 1746-1760. 10.1056/NEJMra1011670. PubMed PMID: 21542745. Epub 2011/05/06. engCrossRefPubMed

23.

Langer HF, Gawaz M: Platelet-vessel wall interactions in atherosclerotic disease. Thromb Haemost. 2008, 99 (3): 480-486. PubMed PMID: 18327395. Epub 2008/03/11. engPubMed

24.

Tamhane UU, Aneja S, Montgomery D, Rogers EK, Eagle KA, Gurm HS: Association between admission neutrophil to lymphocyte ratio and outcomes in patients with acute coronary syndrome. Am J Cardiol. 2008, 102 (6): 653-657. 10.1016/j.amjcard.2008.05.006. PubMed PMID: 18773982CrossRefPubMed

25.

Walsh SR, Cook EJ, Goulder F, Justin TA, Keeling NJ: Neutrophil-lymphocyte ratio as a prognostic factor in colorectal cancer. J Surg Oncol. 2005, 91 (3): 181-184. 10.1002/jso.20329. PubMed PMID: 16118772CrossRefPubMed

26.

Dotsenko O, Chaturvedi N, Thom SA, Wright AR, Mayet J, Shore A, Schalkwijk C, Hughes AD: Platelet and leukocyte activation, atherosclerosis and inflammation in European and South Asian men. J Thromb Haemost. 2007, 5 (10): 2036-2042. 10.1111/j.1538-7836.2007.02711.x. PubMed PMID: 17883700. Pubmed Central PMCID: 2650817. Epub 2007/09/22. engPubMedCentralCrossRefPubMed

27.

Turkmen K, Ozcicek F, Ozcicek A, Akbas EM, Erdur FM, Tonbul HZ: The relationship between neutrophil-to-lymphocyte ratio and vascular calcification in end-stage renal disease patients. Hemodial Int. 2013, 18 (1): 47-53. PubMed PMID: 23819627CrossRefPubMed

28.

Turkmen K, Tufan F, Selcuk E, Akpinar T, Oflaz H, Ecder T: Neutrophil-to-lymphocyte ratio, insulin resistance, and endothelial dysfunction in patients with autosomal dominant polycystic kidney disease. Indian J Nephrol. 2013, 23 (1): 34-40. 10.4103/0971-4065.107195. PubMed PMID: 23580803. Pubmed Central PMCID: 3621236. Epub 2013/04/13. engPubMedCentralCrossRefPubMed

29.

Turkmen K: Platelet-to-lymphocyte ratio: one of the novel and valuable platelet indices in hemodialysis patients. Hemodial Int. 2013, 17 (4): 670-PubMed PMID: 24015774. Epub 2013/09/11. EngPubMed

30.

Turkmen K, Guney I, Yerlikaya FH, Tonbul HZ: The relationship between neutrophil-to-lymphocyte ratio and inflammation in end-stage renal disease patients. Ren Fail. 2012, 34 (2): 155-159. PubMed PMID: 22172001PubMed

31.

Azab B, Chainani V, Shah N, McGinn JT: Neutrophil-lymphocyte ratio as a predictor of major adverse cardiac events among diabetic population: a 4-year follow-up study. Angiology. 2013, 64 (6): 456-465. 10.1177/0003319712455216. PubMed PMID: 22904109. Epub 2012/08/21. engCrossRefPubMed

32.

Bhat T, Teli S, Rijal J, Bhat H, Raza M, Khoueiry G, Meghani M, Akhtar M, Costantino T: Neutrophil to lymphocyte ratio and cardiovascular diseases: a review. Expert Rev Cardiovasc Ther. 2013, 11 (1): 55-59. 10.1586/erc.12.159. PubMed PMID: 23259445CrossRefPubMed

33.

Ho E, Shimada Y: Formation of the epicardium studied with the scanning electron microscope. Dev Biol. 1978, 66 (2): 579-585. 10.1016/0012-1606(78)90263-4. PubMed PMID: 700255. Epub 1978/10/01. engCrossRefPubMed

34.

Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, Sarov-Blat L, O'Brien S, Keiper EA, Johnson AG, Martin J, Goldstein BJ, Shi Y: Human epicardial adipose tissue is a source of inflammatory mediators. Circulation. 2003, 108 (20): 2460-2466. 10.1161/01.CIR.0000099542.57313.C5. PubMed PMID: 14581396CrossRefPubMed

35.

Kremen J, Dolinkova M, Krajickova J, Blaha J, Anderlova K, Lacinova Z, Haluzikova D, Bosanska L, Vokurka M, Svacina S, Haluzik M: Increased subcutaneous and epicardial adipose tissue production of proinflammatory cytokines in cardiac surgery patients: possible role in postoperative insulin resistance. J Clin Endocrinol Metab. 2006, 91 (11): 4620-4627. 10.1210/jc.2006-1044. PubMed PMID: 16895955CrossRefPubMed

36.

Cheng KH, Chu CS, Lee KT, Lin TH, Hsieh CC, Chiu CC, Voon WC, Sheu SH, Lai WT: Adipocytokines and proinflammatory mediators from abdominal and epicardial adipose tissue in patients with coronary artery disease. Int J Obes. 2008, 32 (2): 268-274. 10.1038/sj.ijo.0803726. PubMed PMID: 17878891CrossRef

37.

Fain JN, Sacks HS, Buehrer B, Bahouth SW, Garrett E, Wolf RY, Carter RA, Tichansky DS, Madan AK: Identification of omentin mRNA in human epicardial adipose tissue: comparison to omentin in subcutaneous, internal mammary artery periadventitial and visceral abdominal depots. Int J Obes. 2008, 32 (5): 810-815. 10.1038/sj.ijo.0803790. PubMed PMID: 18180782CrossRef

38.

Tonbul HZ, Turkmen K, Kayikcioglu H, Ozbek O, Kayrak M, Biyik Z: Epicardial adipose tissue and coronary artery calcification in diabetic and nondiabetic end-stage renal disease patients. Ren Fail. 2011, 33 (8): 770-775. 10.3109/0886022X.2011.599913. PubMed PMID: 21770856. Epub 2011/07/21. engCrossRefPubMed

39.

Turkmen K, Kayikcioglu H, Ozbek O, Solak Y, Kayrak M, Samur C, Anil M, Zeki Tonbul H: The relationship between epicardial adipose tissue and malnutrition, inflammation, atherosclerosis/calcification syndrome in ESRD patients. Clin J Am Soc Nephrol. 2011, 6 (8): 1920-1925. 10.2215/CJN.00890111. PubMed PMID: 21757644. Pubmed Central PMCID: 3359546. Epub 2011/07/16. engPubMedCentralCrossRefPubMed

40.

Schwandt P: Can we slow down the global increase of adiposity?. Int J Prev Med. 2011, 2 (3): 115-116. PubMed PMID: 21811650. Pubmed Central PMCID: 3143521. Epub 2011/08/04. engPubMedCentralPubMed

41.

Rexrode KM, Carey VJ, Hennekens CH, Walters EE, Colditz GA, Stampfer MJ, Willett WC, Manson JE: Abdominal adiposity and coronary heart disease in women. JAMA. 1998, 280 (21): 1843-1848. 10.1001/jama.280.21.1843. PubMed PMID: 9846779CrossRefPubMed

42.

Rexrode KM, Buring JE, Manson JE: Abdominal and total adiposity and risk of coronary heart disease in men. Int J Obes Relat Metab Disord. 2001, 25 (7): 1047-1056. 10.1038/sj.ijo.0801615. PubMed PMID: 11443505CrossRefPubMed

43.

Visscher TL, Seidell JC, Molarius A, van der Kuip D, Hofman A, Witteman JC: A comparison of body mass index, waist-hip ratio and waist circumference as predictors of all-cause mortality among the elderly: the Rotterdam study. Int J Obes Relat Metab Disord. 2001, 25 (11): 1730-1735. 10.1038/sj.ijo.0801787. PubMed PMID: 11753597CrossRefPubMed

44.

Shetty R, Vivek G, Naha K, Nayak K, Goyal A, Dias LS: Correlation of epicardial fat and anthropometric measurements in Asian-Indians: a community based study. Avicenna J Med. 2012, 2 (4): 89-93. 10.4103/2231-0770.110739. PubMed PMID: 23826555. Pubmed Central PMCID: 3696206PubMedCentralCrossRefPubMed

45.

Kim SJ, Kim HS, Jung JW, Kim NS, Noh CI, Hong YM: Correlation between epicardial fat thickness by echocardiography and other parameters in obese adolescents. Korean Circ J. 2012, 42 (7): 471-478. 10.4070/kcj.2012.42.7.471. PubMed PMID: 22870081. Pubmed Central PMCID: 3409396PubMedCentralCrossRefPubMed

46.

Saijo Y, Kiyota N, Kawasaki Y, Miyazaki Y, Kashimura J, Fukuda M, Kishi R: Relationship between C-reactive protein and visceral adipose tissue in healthy Japanese subjects. Diabetes Obes Metab. 2004, 6 (4): 249-258. 10.1111/j.1462-8902.2003.0342.x. PubMed PMID: 15171748CrossRefPubMed

47.

Park HS, Park JY, Yu R: Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-alpha and IL-6. Diabetes Res Clin Pract. 2005, 69 (1): 29-35. 10.1016/j.diabres.2004.11.007. PubMed PMID: 15955385CrossRefPubMed

48.

Lichtash CT, Cui J, Guo X, Chen YD, Hsueh WA, Rotter JI, Goodarzi MO: Body adiposity index versus body mass index and other anthropometric traits as correlates of cardiometabolic risk factors. PLoS One. 2013, 8 (6): e65954-10.1371/journal.pone.0065954. PubMed PMID: 23776578. Pubmed Central PMCID: 3679008PubMedCentralCrossRefPubMed

49.

Engeli S, Feldpausch M, Gorzelniak K, Hartwig F, Heintze U, Janke J, Mohlig M, Pfeiffer AF, Luft FC, Sharma AM: Association between adiponectin and mediators of inflammation in obese women. Diabetes. 2003, 52 (4): 942-947. 10.2337/diabetes.52.4.942. PubMed PMID: 12663465CrossRefPubMed

50.

Plourde G, Karelis AD: Current issues in the identification and treatment of metabolically healthy but obese individuals. Nutr Metab Cardiovasc Dis. 2014, 24 (5): 455-459. 10.1016/j.numecd.2013.12.002. PubMed PMID: 24529490CrossRefPubMed

51.

Iacobellis G, Willens HJ: Echocardiographic epicardial fat: a review of research and clinical applications. J Am Soc Echocardiogr. 2009, 22 (12): 1311-1319. 10.1016/j.echo.2009.10.013. quiz 417–8. PubMed PMID: 19944955CrossRefPubMed

Title: Predictors of epicardial adipose tissue in patients with type 2 diabetes mellitus
Authors: Emin M Akbas
Hikmet Hamur
Levent Demirtas
Eftal M Bakirci
Adalet Ozcicek
Fatih Ozcicek
Ufuk Kuyrukluyildiz
Kultigin Turkmen
Publication date: 01-12-2014
Publisher: BioMed Central
Published in: Diabetology & Metabolic Syndrome / Issue 1/2014
Electronic ISSN: 1758-5996
DOI: https://doi.org/10.1186/1758-5996-6-55

ACC 2024 Congress Coverage

Heart Failure Video

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Predictors of epicardial adipose tissue in patients with type 2 diabetes mellitus

Abstract

Background

Methods

Results

Conclusions

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page

Keynote webinar | Spotlight on sleep in brain health

Springer Medicine

Abstract

Background

Methods

Results

Conclusions

Please log in to get access to this content

Other articles of this Issue 1/2014

Health literacy skills in type 2 diabetes mellitus outpatients from an university-affiliated hospital in Rio de Janeiro, Brazil

Multivariate epidemiologic analysis of type 2 diabetes mellitus risks in the Lebanese population

Alpha-lipoic acid as a pleiotropic compound with potential therapeutic use in diabetes and other chronic diseases

Assessment of college students’ awareness and knowledge about conditions relevant to metabolic syndrome

Link between insulin resistance and hypertension: What is the evidence from evolutionary biology?

Plasma and urine metabolic profiles are reflective of altered beta-oxidation in non-diabetic obese subjects and patients with type 2 diabetes mellitus

ACC 2024 Congress Coverage

Year in Review: Heart failure and cardiomyopathies

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

Incentivised to exercise

New intervention for STEMI-related cardiogenic shock

» View more highlights on the ACC 2024 congress hub page