Correlation Between Epicardial Fat Thickness and Cardiovascular Risk in Hemodialysis Patients
American Journal of Internal Medicine
Volume 3, Issue 3, May 2015, Pages: 86-94
Received: Mar. 6, 2015; Accepted: Mar. 19, 2015; Published: Mar. 26, 2015
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Ashraf Abd El-Khalik Barakat, Intensive Care Department, Theodor Bilharz Research Institute, Cairo, Egypt
Fatma Mohammed Nasr, Intensive Care Department, Theodor Bilharz Research Institute, Cairo, Egypt
Amna Ahmed Metwaly, Intensive Care Department, Theodor Bilharz Research Institute, Cairo, Egypt
Manar Abd El-Rouf Raafat Ameen, Nephrology Department, Theodor Bilharz Research Institute, Cairo, Egypt
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Background: Cardiovascular diseases are common in hemodialysis (HD) patients and cardiovascular mortality is responsible for 50% of overall deaths in these patients. Epicardial fat thickness (EpFT) may be an effective marker for the prediction of cardiovascular diseases in hemodialysis patients. The thickness of EpF can be measured by echocardiography that can accurately estimate the actual amount of EpF. The aim of the current study is to assess the association between EpFT and carotid intima-media thickness (CIMT), left ventricular systolic and diastolic function and left ventricular mass index in patients with chronic kidney disease (CKD) undergoing hemodialysis to clarify the relationships between EpF and cardiovascular disease risk in these patients. Materials and Methods: Forty adult uremic patients from dialysis unit and twenty (age and sex matched) healthy control subjects were included in this study. Clinical evaluation, routine laboratory investigations, echocardiographic study including measurement of EpFT and carotid Duplex to estimate CIMT were done to all subjects. Results: we found highly significant increase in serum C-reactive protein and significant increase in serum phosphorus and triglyceride with significant decrease in serum calcium and high-density lipoprotein cholesterol in hemodialysis patients compared to the controls. Also, there were significant increases in left ventricular mass index, left atrium diameter, carotid intima-media thickness, epicardial fat thickness, peak velocity of the late filling wave due to atrial contraction (A wave) and deceleration time of E wave in hemodialysis patients compared to the controls. There were also highly significant decrease in E/A ratio in hemodialysis patients compared to healthy control subjects. EpFT measured by echocardiography in hemodialysis patients was positively correlated with body mass index, CRP, left atrium diameter, left ventricular mass index, deceleration time and CIMT and negatively correlated with high-density lipoprotein cholesterol and E/A ratio. Conclusion: Hemodialysis patients can be evaluated routinely by echocardiography for early detection of cardiovascular structural and functional changes which are common in these patients and epicardial fat thickness is an effective marker for the prediction of cardiovascular risk in hemodialysis patients.
Hemodialysis Patients, Cardiovascular Diseases, Carotid Intima-Media Thickness, Epicardial Fat Thickness
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Ashraf Abd El-Khalik Barakat, Fatma Mohammed Nasr, Amna Ahmed Metwaly, Manar Abd El-Rouf Raafat Ameen, Correlation Between Epicardial Fat Thickness and Cardiovascular Risk in Hemodialysis Patients, American Journal of Internal Medicine. Vol. 3, No. 3, 2015, pp. 86-94. doi: 10.11648/j.ajim.20150303.12
Zhang QL and Rothenbacher D (2008): Prevalence of chronic kidney disease in population-based studies: systematic review. BMC Public Health 8:117.
Foley RN, Parfrey PS and Sarnak MJ (1998): Epidemiology of cardiovascular disease in chronic renal disease. J Am. Soc. Nephro.l 9 (12 Suppl) S16–23.
Block GA, Raggi P, Bellasi A, et al., (2007): Mortality effect of coronary calcification and phosphate binder choice in incident hemodialysis patients. Kid. Int. 71:438–441.
Shantouf RS, Budoff MJ, Ahmadi N, et al., (2010): Total and individual coronary artery calcium scores as independent predictors of mortality in hemodialysis patients. Am J Nephrol 31:419–425.
Watanabe R, Lemos MM, Manfredi SR, et al., (2010) : Impact of cardiovascular calcification in nondialyzed patients after 24 months of follow-up. Clin J Am Soc Nephrol 5:189–194.
Russo D, Corrao S, Battaglia Y, et al. (2011): Progression of coronary artery calcification and cardiac events in patients with chronic renal disease not receiving dialysis. Kid. Int. 80:112–118.
Sarnak M. J., LeveyA. S., Schoolwerth A. C. et al., ( 2003) : “Kidney disease as a risk factor for development of Cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention,” Circulation, 108(17): 2154–2169.
Muntner P., He J., Hamm L., et al., (2002): “Renal insufficiency and subsequent death resulting from cardiovascular disease in the United States,” Journal of the American Society of Nephrology, 13( 3): 745–753.
Foley R. N., Murray A. M., Li S., Herzog C. A., et al., (2005): “Chronic kidney disease and the risk for cardiovascular disease, renal replacement, and death in the United States medicare population, 1998 to 1999,” Journal of the American Society of Nephrology, 16 (2):489–495.
Rahman M., Pressel S., Davis B. R. et al., (2006): “Cardiovascular outcomes in high-risk hypertensive patients stratified by baseline glomerular filtration rate,” Annals of InternalMedicine, 144(3): 172–180.
Van Der Velde M., Matsushita k., Coresh J. et al., ( 2011): “Lower estimated glomerular filtration rate and higher albuminuria are associated with all-cause and cardiovascular mortality. A collaborative meta-analysis of high-risk population cohorts,” Kid. Int., 79 (12): 1341–1352.
Segura J., Campo C., Gil P. et al., (2004): “Development of chronic kidney disease and cardiovascular prognosis in essential hypertensive patients,” Journal of the American Society of Nephrology, 15(6): 1616–1622.
Knobler H, Zornitzki T, Vered S. et al., (2004): “Reduced glomerular filtration rate in asymptomatic diabetic patients: predictor of increased risk for cardiac events independent of albuminuria,” Journal of the American College of Cardiology, 44, (11): 2142–2148.
Antman E.M., Anbe D.T., Armstrong P.W. et al., (2004): “ACC/AHA guidelines for the management of patients with ST-elevation myocardial infarction. A report of the American College of cardiology/ American Heart Association Task Force on Practice Guidelines (Committee to Revise the 1999 Guidelines for the Management of patients with acute myocardial infarction),” Journal of the American College of Cardiology, 44(3): 1–211, 2004.
Kalantar-Zadeh K., Block G., Humphreys M. H., et al., (2003): “Reverse epidemiology of cardiovascular risk factors in maintenance dialysis patients,” Kid. 63(3): 793–808, 2003.
Parfrey P.S., Foley R. N., Harnett J.D., et al., (1996): “Outcome and risk factors for left ventricular disorders in chronic uraemia,” Nephrology Dialysis Transplantation, 11(7): 1277–1285.
Cheung A.K., Sarnak M. J., Yan G. et al., (2000):“Atherosclerotic cardiovascular disease risks in chronic hemodialysis patients,” Kid. Int. 58 (1): 353–362.
Muntner P., He J., Astor B.C., et al., (2005): “Traditional and nontraditional risk factors predict coronary heart disease in chronic kidney disease: results from the atherosclerosis risk in communities study,” Journal of the American Society of Nephrology, 16(2): 529–538, 2005.
Himmelfarb J., Stenvinkel P., Ikizler T.A., et al., (2002): “Perspectives in renal medicine: the elephant in uremia: oxidant stress as a unifying concept of cardiovascular disease in uremia,” Kid. Int. 62(5): 1524–1538.
Afsar B, Turkmen K, Covic A, et al., (2014): An Update on Coronary Artery Disease and Chronic Kidney Disease. International J Nephr, 9.
Bajraktari G, Berbatovci-Ukimeraj M, Hajdari A, et al., (2009): Predictors of increased left ventricular filling pressure in dialysis patients with preserved left ventricular ejection fraction. Croat Med J 50: 543–549.
Hirota H, Yoshida K, Kishimoto T, et al.,(1995): Continuous activation of gp130, a signal-transducing receptor component for interleukin 6-related cytokines, causes myocardial hypertrophy in mice. Proc Natl Acad Sci U S A, 92:4862–4866.
Wu CK, Yang CY, Lin JW, et al., (2012): The relationship among central obesity, systemic inflammation, and left ventricular diastolic dysfunction as determined by structural equation modeling. Obesity (Silver Spring) 2012, 20:730–737.
Marchington JM, Mattacks CA and Pond CM (1989): Adipose tissue in the mammalian heart and pericardium: structure, foetal development and biochemical properties. Comp Biochem Physiol B 94: 225–232.
Iacobellis G, Corradi D and Sharma AM (2005): Epicardial adipose tissue: anatomic, biomolecular and clinical relationships with the heart. Nat. Clin. Pract. Cardiovasc. Med. 2:536–543.
Kadowaki T, Yamauchi T, Kubota N, et al., (2006): Adiponectin and adiponectin receptors in insulin resistance, diabetes, and the metabolic syndrome.J Clin Invest 116: 1784-1792.
Kern PA, Ranganathan S, Li C, et al., (2001): Adipose tissue tumor necrosis factor and interleukin-6 expression in human obesity and insulin resistance. Am J Physiol Endocrinol Metab, 745-751.
Mazurek T, Zhang L, Zalewski A, et al., (2003): Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108:2460-2466.
Tonbul HZ, Kultigin T, Kayikcioglu H, et al., (2011): Epicardial adipose tissue and coronary artery calcification in diabetic and nondiabetic end-stage renal disease patients. Ren Fail 33: 770-775.
Turkmen K, Kayikcioglu H, Ozbek O, et al.,(2011): The relationship between epicardial adipose tissue and malnutrition, inflammation, atherosclerosis / calcification syndrome in ESRD patients. Clin J Am Soc Nephrol 6 (8):1920-1925.
Alvarez Tamargo JA, Barriales Alvarez V, Sanmartin Pena JC, et al., (2001) :Angiographic correlates of the high-risk criteria for conventional exercise testing and the Duke treadmill score. Rev Esp Cardiol; 54: 860-7.
Corradi D, Maestri R, Callegari S, et al., (2004): The ventricular epicardial fat is related to the myocardial mass in normal, ischemic and hypertrophic hearts. Cardiovasc Pathol; 13: 313-6.
Iacobellis G, Ribaudo MC, Zappaterreno A, et al., (2004): Relation between epicardial adipose tissue and left ventricular mass. Am J Cardiol; 94: 1084-7.
Iacobellis G, Assael F, Ribaudo MC, et al., (2003): Epicardial fat from echocardiography: a new method for visceral adipose tissue prediction. Obes Res. 11(2):304-10.
Aribas A, Akilli H, Kayrak M, et al., (2014): Echocardiographic Epicardial Fat Thickness in Patients with Paroxysmal Atrial Fibrillation. Exp Clin Cardiol 20(6) 3574-3586.
Cobble M and Bale B., (2010): Carotid intima-media thickness: Knowledge and application to every day practice. Postgrad Med. 2010; 122 (1):10-18
Ossareh S, Alaei A and Saedi D., (2011): Carotid intima-media thickness in maintenance hemodialysis patients: role of cardiovascular risk factor. Iran J Kidney; 5(3):169-174
Francesco A B, Francesco M, Giovanni T et al.,(2001): Prognostic Value of Ultrasonographic Measurement of Carotid Intima Media Thickness in Dialysis Patients. J Am Soc Nephrol ; 12: 242-464.
Saritas T, Tascilar E, Abaci A, et al.,(2010): Importance of plasma N-terminal pro B-type natriuretic peptide, epicardial adipose tissue, and carotid intima-media thicknesses in asymptomatic obese children. Pediatr Cardiol.; 31(6):79.
Sengul C, Cevik C, Ozveren O, et al., (2011): Echocardiographic epicardial fat thickness is associated with carotid intima-media thickness in patients with metabolic syndrome. Echocardiography. 28 (8):853-8
Atakan A, Macunluoglu B, Kaya Y, et al., (2014): Epicardial fat thickness is associated with impaired coronary flow reserve in hemodialysis patients. Hemodial Int. 18 (1): 62-9.
Turan MN, Gungar O, Asci G et al., (2013): Epicardial adipose tissue volume and cardiovascular disease in hemodialysis patients. Atherosclerosis 226: 129-133.
Turkmen K, Ozbek O, Kayikcioglu H et al,. (2012): The relationship between epicardial adipose tissue and coronary artery calcification in peritoneal dialysis patients. Cardiorenal Med. 2:43-51.
Gottdiener J.S., Bendnarz I. and Devereaux R., (2004): American Society of Echocardiography recommendations for use of echocardiography inclinical trials. Journal of American Society of Echocardiography; 17: 1086: 1119
Devereux RB, Alonso DR, Lutas EM, et al.,(1986): Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am. J Cardiol. 57: 450-458.
Malavazos AE, Di Leo G, Secchi F, et al., (2010): Relation of echocardiographic epicardial fat thickness and myocardial fat. Am J Cardiol 105:1831-1835
Berglund GL, Riley WA, Barnes RW et al., (1994): Quality control in ultrasound studies on atherosclerosis. J. Int. Med. 236: 581-586.
Longenecker JC, Coresh J, Powe NR, et al., (2002): Traditional cardiovascular disease risk factors in dialysis patients compared with the general population: the CHOICE Study. J Am Soc Nephrol.; 13: 1918–1927.
Agarwal R. (2005): Hypertension in chronic kidney disease and dialysis: pathophysiology and management. Cardiol Clin. 23: 237–248.
Agarwal R, Andersen MJ, Bishu K, et al. (2006): Home blood pressure monitoring improves the diagnosis of hypertension in hemodialysis patients. Kidney Int. 69: 900–906.
Salifu MO, Abbott KC, Aytug S, et al., (2010): New-onset diabetes after hemodialysis initiation: impact on survival. Am J Nephrol 31(3):239-46.
Tien KJ, Lin ZZ, Chio CC, et al., (2013): Epidemiology and mortality of new-onset diabetes mellitus after dialysis: Taiwan national cohort study. Diabetes Care. 30. [Epub ahead of print].
Woodward RS, Schnitzler MA, Baty J, et al., (2003): Incidence and cost of new onset diabetes mellitus among U.S. wait-listed and transplanted renal allograft recipients. Am J Transplant 3(5):590-8.
Attman P-O, Samuelsson O and Alaupovic P(1993): Lipoprotein metabolism and renal failure. Am J Kidney Dis 21: 573–591. 55. Alaupovic P. ( 1991): Apolipoprotein composition as the basis for classify- ing plasma lipoproteins. Characterization of apoA- and apoB-con-taining lipoprotein families. Prog Lipid Res 30:105–138.
Foley RN, Parfrey PS and Sarnak MJ (1998): Clinical epidemiology of cardiovascular disease in chronic renal disease. Am J Kidney Dis 32: 112-119.
Attman P-O, Alaupovic P, Tavella M, et al., (1996): Abnor-mal lipid and apolipoprotein composition of major lipoprotein density classes in patients with chronic renal failure. Nephrol Dial Transplant 11: 63–69.
Rajman I, Harper L, McPake D, et al. (1998): Low-density lipoprotein subfraction profiles in chronic renal failure. Nephrol Dial Trans plant 13: 2281–2287.
Reddy E, Suchitra M, Reddy Vet al., (2008): Dyslipidemia: End Stage Renal Disease and Hemodialysis. Int. J. Neph. 5 (1).
Lee CT, Tsai YC, Ng HY, et al., (2009): Association between C-reactive protein and biomarkers of bone and mineral metabolism in chronic hemodialysis patients: A cross-sectional study. J Ren Nutr; 19: 2227.
Wang AY, Lam CW, Wang M, et al., (2008): Increased circulating inflammatory proteins predict a worse prognosis with valvular calcification inendstage renal disease: A prospective cohort study. Am J Nephrol; 28: 6653.
Spasovski G. (2007): New aspects of treatment of renal bone disease in dialysis patients. Prilozi. 28(1):205-13.
Jeznach-Steinhagen A, Słotwiński R and Szczygieł B. (2007): Malnutrition, inflammation, atherosclerosis in hemodialysis patients.Rocz Panstw Zakl Hig. 58(1):83-8.
Resic H; Ajanovic S and Kukavica N (2009): Plasma levels of brain natriuretic peptides and cardiac troponin in hemodialysis patients. Bosn J. Basic Med Sci. 9(2):137-141.
Abd El-khalik A A , Ameen M A R, Metwaly A A, et al., (2014):. Cardiovascular Calcification in Chronic Hemodialysis Patients: Contributors Interplay. Am J Life Sci 2(5): 251-259.
Waked E, El Shanawani F, Raafat M, et al., (2011): Bone Specific Alkaline Phosphatase and Cardiovascular Morbidity among Patients on Maintenance Hemodialysis. Life Science Journal, 8(4):1078- 1087.
Rampersaud E; Bielak LF; Persa A (2008): The association of coronary artery calcification and carotid artery intima-media thickness with distinct traditional coronary artery disease risk factors in asymptomatic adults. Am. J. of Epidemiology 168(9):1016-1023.
Gagliardi GM, Rossi S, Manes MT, et al.(2004): Impact of left ventricular patterns and diastolic dysfunction on hemodialysis patients. G Ital Nefrol ; 21(1):45-50.
Fathi, R., N. Isbel, B. Haluska, C. et al.,(2003): Correlates of subclinical left ventricular dysfunction in ESRD. Am. J. Kidney. Dis. 41: 1016- 1025.
Manes MT, Gagliardi M, Misuraca G, et al.,(2005): Left ventricular geometric patterns and cardiac function in patients with chronic renal failure undergoing hemodialysis. Monaldi Arch Chest Dis: 64(1):27-32.
Kocyigit I, Gungor O, Unal A, et al., (2014): A low serum triiodo-thyroxine level is association with epicardial adipose tissue in peritoneal dialysis patients. J. Atheroscler. Thromb. 21(10), 1066- 1074
Yañez-RiveraT G, Baños-Gonzalez M A, Ble-Castillo J L, et al., (2014): Relationship between epicardial adipose tissue, coronary artery disease and adiponectin in a Mexican population. Cardiovascular Ultrasound, 12-35.
Kerr J D, Holden R M, Morton AR, et al., (2013): Associations of epicardial fat with coronary calcification, insulin resistance, inflammation, and fibroblast growth factor-23 in stage 3-5 chronic kidney disease. BMC Nephrology 14:26.
Iacobellis G, Leonetti F, Singh N, et al., (2007): Relationship of epicardial adipose tissue with atrial dimensions and diastolic function in morbidly obese subjects. Int J Cardiol 115 :272-273.
Konishi M, Sugiyama S, Sugamura K et al ( 2012): Accumulation of pericardial fat correlates with left ventricular diastolic dysfunction in patients with normal ejection fraction Journal of Cardiology 59, (3): 344–351
Yusuf S, Hawken S, Ounpuu S, et al.(2005): Obesity and the risk of myocardial infarction in 27,000 participants from 52 countries: a case-control study. Lancet 366: 1640-9.
Guerra F, Mancinelli L, Buglioni A, et al. (2011): Microalbuminuria and left ventricular mass in overweight and obese hypertensive patients: role of the metabolic syndrome. High Blood Press. Cardiovasc. Prev. 18 : 195-201.
Apridonidze T, Shaqra H, Ktaich N, et al., (2011): Relation of components of the metabolic syndrome to left ventricular geometry in hispanic and non-hispanic black adults. Am J Cardiovasc Dis 1: 84-91.
Van der Meer RW, Rijzewijk LJ, Diamant M, et al., (2008): The ageing male heart: myocardial triglyceride content as independent predictor of diastolic function. Eur Heart J 29:1516-1522.
Iozzo P (2011): Myocardial, perivascular, and epicardial fat. Diabetes Care 34(Suppl 2):S371-S379.
Greenstein AS, Khavandi K, Withers SB, et al., (2009): Local inflammation and hypoxia abolish the protective anticontractile properties of perivascular fat in obese patients. Circulation 119: 1661–1670.
Pang C, Gao Z, Yin J, et al., (2008): Macrophage infiltration into adipose tissue may promote angiogenesis for adipose tissue remodeling in obesity. Am J Physiol Endocrinol Metab 295:E313-E322.
Henrichot E, Juge-Aubry CE, Pernin A, et al., (2005): Production of chemokines by perivascular adipose tissue: a role in the pathogenesis of atherosclerosis? Arterioscler Thromb Vasc Biol 25:2594–2599.
Xu Y, Cheng X, Hong K, et al., (2012): How to interpret epicardial adipose tissue as a cause of coronary artery disease: a meta-analysis. Coronary Artery Dis 23: 227-233.
Baker AR, Silva NF, Quinn DW et al., (2006): Human epicardial adipose tissue expresses a pathogenic profile of adipocytokines in patients with cardiovascular disease. Cardiovasc. Diabetol. 5: 1
Subbotin VM. (2012): Neovascularization of coronary tunica intima (DIT) is the cause of coronary atherosclerosis. Lipoproteins invade coronary intima via neovascularization from adventitial vasa vasorum, but not from the arterial lumen: a hypothesis. Theor. Biol. Med. Model. 9: 11
Alexopoulos N, McLean DS, Janik M et al.(2010): Epicardial adipose tissue and coronary artery plaque characteristics. Atherosclerosis 210: 150–154
Tavora F, Kutys R, Li L et al.(2010): Adventitial lymphocytic inflammation in human coronary arteries with intimal atherosclerosis. Cardiovasc Pathol 19: 61–68
Ding J, Hsu FC, Harris TB et al. (2009): The association of pericardial fat with incident coronary heart disease: the Multi-Ethnic Study of Atherosclerosis (MESA). Am J Clin Nutr 90: 499–504
Mahabadi AA, Berg MH, Lehmann N et al. (2013): Association of epicardial fat with cardiovascular risk factors and incident myocardial infarction in the general population: the Heinz Nixdorf Recall Study. J Am Coll Cardiol 61: 1388–1395.
Chaldakov GN, Stankulov IS and Aloe L (2001): Subepicardial adipose tissue in human coronary atherosclerosis: another neglected phenomenon. Atherosclerosis 154:237-238.
Maeda K, Okubo K, Shimomura I, et al., (1997): Analysis of an expression profile of genes in the human adipose tissue. Gene 190:227-235.
Chaldakov GN, Beltowsky J, Ghenev PI, et al.,(2012): Adipoparacrinology–vascular periadventitial adipose tissue (tunica adiposa) as an example. Cell Biol Int 36:327-330.
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