15Oct 2019

ULTRASOUND HISTOGRAM ANALYSES OF EPICARDIAL ADIPOSE TISSUE.

  • 1st Department of Cardiology, East Slovak Institute of Cardiovascular Diseases, Kosice, Slovakia.
  • Department of Paediatrics and Adolescent Medicine, Faculty of Medicine, P.J. Safarik University in Kosice, Slovakia .
  • Institute of Mathematics, P. J. Safarik University in Kosice, Slovakia.
  • Department of Stomatology and Maxillofacial Surgery, Faculty of Medicine, P.J. Safarik University in Kosice, Slovakia.
  • Institute of Parasitology of the Slovak Academy of Sciences, Kosice, Slovakia.
  • Institute of Theoretical Health Sciences, Faculty of Health Care, University of Miskolc, Hungary.
  • Abstract
  • Keywords
  • References
  • Cite This Article as
  • Corresponding Author

Objective: Adipose tissue is a major endocrine organ and plays a key role in energy homeostasis. Two types of adipose tissue such as white and brown adipose tissue exist having essentially different physiological function. The epicardial adipose tissue (EAT) is considered as reliable marker of visceral adiposity, however its composition is not entirely clear. The aim of our study was to examine the qualitative features of EAT by ultrasound histograms in obese and normal-weight adolescents. Methods: 70 (mean age of 17.72 ? 1.20) randomly selected adolescents were involved in this study. Ultrasonographic histogram was used to assess the EAT structure by the contrast between the epicardial adipose tissue and left atrium (EAT/LA-value). Furthermore, anthropometric and biochemical parameters of cardiovascular risk were also obtained. Results: The EAT/LA-value differed significantly between normal weight and obese youngsters (14.76?0.83 vs. 26.22?0.95; p0.001) and was associated with clinical parameters of obesity (body mass index (BMI): r=0.57; p0.0001 and BMI percentile: r=0.72; p0.0001), laboratory parameters of cardiovascular risk factors (ALT: r=0.38; p<0.001, adiponectin: r= -0.33; p<0.01, hsCRP: r=0.24; p<0.05) and EAT thickness (EAT at end-systole: r=0.46; p<0.0001 and EAT at end-diastole: r=0.43; p<0.0001). Multiple regression analysis showed that the EAT/LA-value was associated with EAT at end-systole [B (95%CI) = 2.52 (0.94, 4.11); p≤0.01] and alanine aminotransferase (ALT) [9.23 (0.20, 18.26); p≤0.05 however, BMI proved to be the strongest independent predictor [0.16 (0.10, 0.21); p≤0.001 Conclusion: The ultrasound histogram of epicardial adipose tissue seems to be non-invasive, low-cost and easy imaging approach that can qualitatively distinguish between different types and characteristics of adipose tissue.


  1. Bornfeldt KE, Tabas I (2011) Insulin resistance, hyperglycemia, and atherosclerosis. Cell Metab 14:575?585. https://doi.org/1016/j.cmet.2011.07.015
  2. Lloyd-Jones D,Adams R,?Carnethon M,?De Simone G,?Ferguson TB,?Flegal K,?Ford E,?Furie K,?Go A,?Greenlund K,?Haase N,?Hailpern S,?Ho M,?Howard V,?Kissela B,?Kittner S,?Lackland D,?Lisabeth L,?Marelli A,?McDermott M,?Meigs J,?Mozaffarian D,?Nichol G,?O'Donnell C,?Roger V,?Rosamond W,?Sacco R,?Sorlie P,?Stafford R,?Steinberger J,?Thom T,?Wasserthiel-Smoller S,?Wong N,?Wylie-Rosett J,?Hong Y (2009) Heart disease and stroke statistics?2009 update: a report? from the American Heart Association Statistics Committee and Stroke Statistics? Circulation 119:21?181. http://doi.org/10.1161/CIRCULATIONAHA.108.191261
  3. Saely CHH, Geiger V, Saely HD (2012) Brown versus White Adipose Tissue: A Mini-Review. Gerontology 58:15?23. http://doi.org/10.1159/000321319
  4. Nedergaard J, Bengtsson T, Cannon B (2007) Unexpected evidence for active brown adipose tissue in adult humans. American Journal of Physiology. Endocrinology and Metabolism. 293:444?52. https://doi.org/10.1152/ajpendo.00691.2006
  5. Feldmann HM, Golozoubova V, Cannon B, Nedergaard J (2009) UCP1 ablation induces obesity and abolishes diet-induced thermogenesis in mice exempt from thermal stress by living at thermoneutrality. Cell Metab. 9:203?209.? https://doi.org/10.1016/j.cmet.2008.12.014
  6. Gilsanz V, Hu HH, Kajimura S (2013) Relevance of brown adipose tissue in infancy and adolescence. Pediatr Res. 73:3?9. http://doi.org/1038/pr.2012.141
  7. Hamann A, Flier JS, Lowell BB (1996) Decreased brown fat markedly enhances susceptibility to diet-induced obesity, diabetes, and hyperlipidaemia. Endocrinology 137:21?29. https://doi.org/10.1210/endo.137.1.8536614
  8. Cypess AM,Lehman S,?Williams G,?Tal I,?Rodman D,?Goldfine AB,?Kuo FC,?Palmer EL,?Tseng YH,?Doria A,?Kolodny GM,?Kahn CR (2009) Identification and importance of brown adipose tissue in adult humans. N Engl. J.Med. 360:1509?1517. http://doi.org/1056/NEJMoa0810780
  9. van Marken Lichtenbelt WD,Vanhommerig JW,?Smulders NM,?Drossaerts JM,?Kemerink GJ,?Bouvy ND,?Schrauwen P,?Teule GJ (2009) Cold-activated brown adipose tissue in healthy men. N Engl. J. Med. 360:1500?1508. http://doi.org/1056/NEJMoa0808718
  10. Zingaretti MC,Crosta F,?Vitali A,?Guerrieri M,?Frontini A,?Cannon B,?Nedergaard J,?Cinti S (2009) The presence of UCP1 demonstrates that metabolically active adipose tissue in the neck of adult humans truly represents brown adipose tissue. FASEB J. 23:3113?3120.? http://dio.org/1096/fj.09-133546
  11. Harms M, Seale P (2013) Brown and beige fat: development, function and therapeutic potential. Nature medicine. 19:1252-1263. http://doi.org/1038/nm.3361
  12. Talman AH,?Psaltis PJ,?Cameron JD,?Meredith IT,?Seneviratne SK,?Wong DT(2014) Epicardial adipose tissue: far more than a fat depot. Cardiovasc. Diagn. Ther. 4:416?429.? https://doi.org/10.3978/j.issn.2223-3652.2014.11.05
  13. Iacobellis G, Assael F, Ribaudo MC, Zappaterreno A, Alessi G, Di Mario U, Leonetti F (2003) Epicardial fat from echocardiography: a new method for visceral adipose tissue prediction. Obes. Res. 11: 304?310. https://doi.org/10.1038/oby.2003.45
  14. Iacobellis G, Leonetti F, Di Mario U (2003) Images in cardiology: Massive epicardial adipose tissue indicating severe visceral obesity. Clin. Cardiol. 26:237. https://doi.org/10.1002/clc.4960260508
  15. Iacobellis G, Pellicelli AM, Grisorio B, Barbarini G, Leonetti F, Sharma AM, Barbaro G (2008) Relation of epicardial fat and alanine aminotransferase in subjects with increased visceral fat. Obesity 16:179-183. https://doi.org/10.1038/oby.2007.50
  16. Iacobellis G, Willens HJ, Barbaro G, Sharma AM (2008) Threshold values of high risk echocardiographic epicardial fat thickness. Obesity 16:887?892. https://doi.org/10.1038/oby.2008.6
  17. Sacks HS, Fain JN, Bahouth SW, Ojha S, Frontini A, Budge H, Cinti S, Symonds ME (2013) Adult epicardial fat exhibits beige features. J Clin Endocrinol Metab. 98:1448-1455. https://doi.org/10.1210/jc.2013-1265
  18. Moreno-Santos I, P?rez-Belmonte LM, Mac?as-Gonz?lez M, Matar? MJ, Castellano D, L?pez-Garrido M, Porras-Mart?n C, S?nchez-Fern?ndez PL, G?mez-Doblas JJ, Cardona F, de Teresa-Galv?n E, Jim?nez-Navarro M (2016) Type 2 diabetes is associated with decreased PGC1α expression in epicardial adipose tissue of patients with coronary artery disease. Transl. Med. 14:243. https://doi.org/10.1186/s12967-016-0999-1
  19. Sacks HS, Fain JN, Holman B, Cheema P, Chary A, Parks F, Karas J, Optican R, Bahouth SW, Garrett E, Wolf RY, Carter RA, Robbins T, Wolford D, Samaha J (2009) Uncoupling protein-1 and related messenger ribonucleic acids in human epicardial and other adipose tissues: epicardial fat functioning as brown fat. J Clin Endocrinol Metab. 94:3611-3615. https://doi.org/10.1210/jc.2009-0571
  20. Dinas PC, Nikaki A, Jamurtas AZ, Prassopoulos V, Efthymiadou R, Koutedakis Y, Georgoulias P, and Flouris AD (2015) Association between habitual physical activity and brown adipose tissue activity in individuals undergoing PET-CT scan. Clinical Endocrinology 82:147-154. https://doi.org/10.1111/cen.12620
  21. Hao R, Yuan L, Zhang N, Li C, Yang J (2012) Brown adipose tissue: distribution and influencing factors on FDG PET/CT scan. J Pediatr Endocrinol Metab. 25:233-237.
  22. Prodhomme H, Ognard J, Robin P, Alavi Z, Salaun PY, Ben Salem D (2018) Imaging and identification of brown adipose tissue on CT scan. Clin Physiol Funct Imaging. 38:186-191. https://doi.org/10.1111/cpf.12373
  23. Mailloux GE, Bertrand M,Stampfler R (1985) Local histogram information content of ultrasound B-mode echographic texture. Ultrasound in Medicine & Biology 11:743-750.
  24. Masuo K, Funagi H, Kawai K (2012) The detection and grading of the fatty liver based on histogram analysis of ultrasonographic image and considering body measurements and laboratory data. Showa Univ J Med Sci. 24:209-218. https://doi.org/10.15369/sujms.24.209
  25. Syakalima M, Takiguchi M, Yasuda J, Mortal Y and Hashimoto A (1998) Comparison of attenuation and liver‐kidney contrast of liver ultrasonographs with histology and biochemistry in dogs with experimentally induced steroid hepatopathy, Veterinary Quarterly 20:18-22. https://doi.org/10.1080/01652176.1998.9694829
  26. Yamajima Y, Uhta K, Narui T, Abe R, Suzuki H, Ohtsuki, M (1983) Ultrasonographical Diagnosis of Fatty Liver: Significance of the Liver-Kidney Contrast. Tohoku J exp.Med. 139:43-50.
  27. Matthews DR, Hosker JP, Rudenski AS, Naylor BA, Treacher DF, Turner RC (1985) Homeostasis model assessment: insulin resistance and beta-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28:412-419.
  28. Ibrahim MM, Vague J (1956) The degree of masculine differentiation of obesities: a factor determining predisposition to diabetes, atherosclerosis, gout and uri-calculus disease. Am J Clin Nutr 4:20?29.
  29. Ibrahim MM, Bruun JM, Lihn AS, Pedersen SB, Richelsen B (2005) Monocyte chemoattractant Protein-1 release is higher in visceral than subcutaneous human adipose tissue (AT): implication of macrophages resident in the AT. J Clin Endocrinol Metab 90:2282?2289. https://doi.org/10.1210/jc.2004-1696
  30. Ibrahim MM, Curat CA, Wegner V, Sengen?s C, Miranville A, Tonus C, Busse, R, Bouloumi? A (2006) Macrophages in human visceral adipose tissue: increased accumulation in obesity and a source of resistin and visfatin. Diabetologia 49:744?747. https://doi.org/10.1007/s00125-006-0173-z
  31. Ibrahim MM (2010) Subcutaneous and visceral adipose tissue: structural and functional differences. Obesity reviews 11:11?18. https://doi.org/10.1111/j.1467-789X.2009.00623.x
  32. Park A, Kim WK, Bae KH (2014) Distinction of white, beige and brown adipocytes derived from mesenchymal stem cells. World J Stem cells 26:33-42. https://dx.doi.org/10.4252%2Fwjsc.v6.i1.33
  33. Chechi K, Blanchard PG, Mathieu P, Deshaies Y, Richard D (2013) Brown fat like gene expression in the epicardial fat depot correlates with circulating HDL-cholesterol and triglycerides in patients with coronary artery disease. Int J Cardiol. 167: 2264-2270. https://doi.org/10.1016/j.ijcard.2012.06.008
  34. Reddy NL, Jones TA, Wayte SC, Adesanya O, Sankar S, Yeo YC, Tripathi G, McTernan PG, Randeva HS, Kumar S, Hutchinson CE, Barber TM (2014) Identification of brown adipose tissue using MR imaging in a human adult with histological and immunohistochemical confirmation. Clin Endocrinol Metab. 99:117-121. https://doi.org/10.1210/jc.2013-2036
  35. Chalfant JS, Smith ML, Hu HH, Dorey FJ, Goodarzian F, Fu CH, Gilsanz V (2012) Inverse association between brown adipose tissue activation and white adipose tissue accumulation in successfully treated pediatric malignancy. Am J Clin Nutr. 95: 1144?1149. https://dx.doi.org/10.3945%2Fajcn.111.030650
  36. Gifford A, Towse TF, Walker RC, Avison MJ, Welch EB (2016) Characterizing active and inactive brown adipose tissue in adult humans using PET-CT and MR Am J Physiol Endocrinol Metab. 311:95-104. https://doi.org/10.1152/ajpendo.00482.2015
  37. Holstila M, Virtanen KA, Gr?nroos TJ, Laine J, Lepom?ki V, Saunavaara J, Lisinen I, Komu M, Hannukainen JC, Nuutila P, Parkkola R, Borra RJ (2013) Measurement of brown adipose tissue mass using a novel dual-echo magnetic resonance imaging approach: a validation study. Metabolism. 62: 1189-1198. https://doi.org/10.1016/j.metabol.2013.03.002
  38. Lowitz GE (1983) Can a local histogram really map texture information? Pattern Recognition 16:141-147. https://doi.org/10.1016/0031-3203(83)90017-1
  39. Fierbinteanu-Braticevici C, Dina I, Petrisor A, Tribus L, Negreanu L, Carstoiu C (2010) Noninvasive investigations for non alcoholic fatty liver disease and liver fibrosis. World J Gastroenterol. 16:4784-4791. https://dx.doi.org/10.3748%2Fwjg.v16.i38.4784
  40. Osawa H, Mori Y (1996) Sonographic diagnosis of fatty liver using a histogram technique that compares liver and renal cortical echo amplitudes. J Clin Ultrasound. 24:25?29. https://doi.org/10.1002/(SICI)1097-0096(199601)24:1%3C25::AID-JCU4%3E3.0.CO;2-N
  41. Lee P, Greenfield JR, Ho KK, Fulham MJ (2010) A critical appraisal of the prevalence and metabolic significance of brown adipose tissue in adult humans. Am J Physiol Endocrinol Metab. 299:601?606. https://doi.org/10.1152/ajpendo.00298.2010
  42. Saito M, Okamatsu-Ogura Y, Matsushita M, Watanabe K, Yoneshiro T, Nio-Kobayashi J, Iwanaga T, Miyagawa M, Kameya T, Nakada K, Kawai Y, Tsujisaki M (2009) High incidence of metabolically active brown adipose tissue in healthy adult humans: effects of cold exposure and adiposity. Diabetes 58:1526?1531. https://doi.org/10.2337/db09-0530
  43. Shimizu I, Aprahamian T, Kikuchi R, Shimizu A, Papanicolaou KN, MacLauchlan S, Maruyama S, Walsh K (2014) Vascular rarefaction mediates whitening of brown fat in obesity J Clin Invest. 124:2099?2112. https://dx.doi.org/10.1172%2FJCI71643
  44. Hu HH, Yin L, Aggabao PC, Perkins TG, Chia JM, Gilsanz V (2013) Comparison of brown and white adipose tissues in infants and children with chemical-shift-encoded water-fat MRI. J Magn Reson Imaging 38:885-896. https://dx.doi.org/10.1002%2Fjmri.24053
  45. Schusterova I, Leenen FH, Jurko A, Sabol F, Takacova J (2014) Epicardial adipose tissue and cardiometabolic risk factors in overweight and obese children and adolescents. Pediatr Obes. 9:63-70. https://doi.org/10.1111/j.2047-6310.2012.00134.x.

[Ingrid Schusterova, Alzbeta Banovcinova, Daniel Klein, Juraj Banovcin, Jindrich Soltys, Ingrid Papajova and Laszlo Barkai. (2019); ULTRASOUND HISTOGRAM ANALYSES OF EPICARDIAL ADIPOSE TISSUE. Int. J. of Adv. Res. 7 (Oct). 682-690] (ISSN 2320-5407). www.journalijar.com


Alzbeta Banovcinova
Department of Paediatrics and Adolescent, Faculty of Medicine, P. J. Šafárik University in Košice, Slovakia

DOI:


Article DOI: 10.21474/IJAR01/9880      
DOI URL: https://dx.doi.org/10.21474/IJAR01/9880