Association between ultrasonographically measured visceral fat tissue thickness and proinflammatory adipokines in obesity

  • Veljko Crnobrnja Clinical Center of Vojvodina, Center for Laboratory Medicine, Novi Sad
  • Branislava Ilinčić Clinical Center of Vojvodina, Center for Laboratory Medicine, Novi Sad
  • Edita Stokić Faculty of Medicine, Novi Sad
  • Marijana Basta Nikolić Univerzitet u Novom Sadu, Medicinski fakultet, Katedra za radiologiju. Klinički centar Vojvodine, Centar za radiologiju.
  • Sonja Slankamenac Klinički centar Vojvodine, Klinika za endokrinologiju, dijabetes i bolesti metabolizma.
  • Anastazija Stojšić- Milosavljević Univerzitet u Novom Sadu, Medicinski fakultet, Katedra za internu medicinu. Institut za kardiovaskularne bolesti, Sremska Kamenica.
  • Radmila Žeravica Univerzitet u Novom Sadu, Medicinski fakultet, Zavod za patološku fiziologiju. Klinički centar Vojvodine, Centar za laboratorijsku medicinu
  • Velibor Čabarkapa Univerzitet u Novom Sadu, Medicinski fakultet, Zavod za patološku fiziologiju. Klinički centar Vojvodine, Centar za laboratorijsku medicinu
Keywords: adipokines;, adipose tissue;, anthropometry;, metabolic diseases;, obesity;, resistin;, severity of illness index;, ultrasonography

Abstract


Background/Aim. Obesity status can be assessed with numerous anthropometric, morphological and functional indices and this study was designed to assess relationship among them. The aim of this study was to investigate associations between anthropometric indices, ultrasonography measurement of visceral and subcutaneous fat tissue thickness and certain proinflammatory adipokines level. Methods. This cross-sectional study comprised a consecutive sample of 60 obese respondents without obesity-related comorbidities, and 20 age-matched healthy normal-weight controls. Anthropometric [body mass index (BMI), waist circumference (WC), neck circumference (NC), body fat, a body shape index (ABSI)], and ultrasonographic indices [thickness of intraabdominal fatt tissue (IAFT), visceral fat (VF), maximum subcutaneous fat (Max SFT), minimal subcutaneous fat (Min SFT)], and serum levels of chemerin and resistin were assessed in all subjects. Results. All anthropometric indices showed statistically significant differences between study groups. The mean IAFT, Max SFT, Min SFT and VF were significantly higher in the obese group compared to controls (p < 0.01, for all). Serum levels of chemerin and resistin correlated positively with BMI, percentage of fat adipose tissue (FAT, %), total FAT (kg), and VF (p < 0.05, for all). Also, we observed significant correlation between resistin and NC (r = 0.23, p = 0.03) and ABSI (r = 0.22, p = 0.04). In multivariable linear regression analysis, chemerin (β = 0.23; p = 0.008) and resistin (β = 0.43; p =0.002) were independently and significantly associated only with VF. Conclusion. Obesity indices, both classical and newer ones, are in positive, statistically significant correlation with the level of proinflammatory cytokines. Ultrasonographically measured VF thickness, independently associated with adipokine levels, may improve assessment of proinflammatory fat tissue characteristics. Further studies are needed to precisely define the use of ultrasonographic fat tissue measurements into clinical practice.

Author Biographies

Marijana Basta Nikolić, Univerzitet u Novom Sadu, Medicinski fakultet, Katedra za radiologiju. Klinički centar Vojvodine, Centar za radiologiju.
Sonja Slankamenac, Klinički centar Vojvodine, Klinika za endokrinologiju, dijabetes i bolesti metabolizma.
Anastazija Stojšić- Milosavljević, Univerzitet u Novom Sadu, Medicinski fakultet, Katedra za internu medicinu. Institut za kardiovaskularne bolesti, Sremska Kamenica.
Radmila Žeravica, Univerzitet u Novom Sadu, Medicinski fakultet, Zavod za patološku fiziologiju. Klinički centar Vojvodine, Centar za laboratorijsku medicinu
Velibor Čabarkapa, Univerzitet u Novom Sadu, Medicinski fakultet, Zavod za patološku fiziologiju. Klinički centar Vojvodine, Centar za laboratorijsku medicinu

References

Ross R, Bradshaw AJ. The future of obesity reduction: be-yond weight loss. Nat Rev Endocrinol. 2009; 5(6): 319‒25.

Stevens GA, Singh GM, Lu Y, Danaei G, Lin JK, Finucane MM et al. National, regional and global trends in adult over-weight and obesity prevalences. Popul Health Metr 2012; 10(1): 22.

Lim SL, Bruce AS. Prospect theory and body mass: charac-terizing psychological parameters for weight-related risk at-titudes and weight-gain aversion. Front Psychol 2015; 6: 330.

Qin X, Zhang Y, Cai Y, He M, Sun L, Fu J, et al. Prevalence of obesity, abdominal obesity and associated factors in hyper-tensive adults aged 45–75 years. Clin Nutr 2013; 32(3): 361‒7.

Krakauer NY, Krakauer JC. A new body shape index predicts mortality hazard independently of body mass index. PLoS One 2012; 7(7): e39504.

Ji M, Zhang S, An R. Effectiveness of A Body Shape Index (ABSI) in predicting chronic diseases and mortality: a sys-tematic review and meta-analysis. Obes Rev 2018; 19(5): 737‒59.

Stolk RP, Meijer R, Mali WP, Grobbee DE, van der Graaf Y. Secondary Manifestations of Arterial Disease Study Group. Ultrasound measurements of intraabdominal fat estimate the metabolic syndrome better than do measurements of waist circumference. Am J Clin Nutr 2003; 77(4): 857‒60.

Farcas AD, Vonica CL, Golea A. Non-alcoholic fatty liver disease, bulb carotid intima-media thickness and obesity phenotypes: results of a prospective observational study. Med Ultrason 2017; 19(3): 265‒71.

Bazzocchi A, Filonzi G, Ponti F, Sassi C, Salizzoni E, Battista G, et al. Accuracy, reproducibility and repeatability of ultraso-nography in the assessment of abdominal adiposity. Acad Radiol 2011; 18(9): 1133‒43.

Kawanami D, Maemura K, Takeda N, Harada T, Nojiri T, Imai Y, et al. Direct reciprocal effects of resistin and adiponectin on vascular endothelial cells: a new insight into adipocyto-kine-endothelial cell interactions. Biochem Biophys Res Commun 2004; 314(2): 415‒9.

Bozaoglu K, Bolton K, McMillan J, Zimmet P, Jowett J, Collier G, et al. Chemerin is a novel adipokine associated with obesity and metabolic syndrome. Endocrinology 2007; 148(10): 4687‒94.

Goralski KB, McCarthy TC, Hanniman EA, Zabel BA, Butcher EC, Parlee SD, et al. Chemerin, a novel adipokine that regu-lates adipogenesis and adipocyte metabolism. J Biol Chem 2007; 282(38): 28175‒8813.

Kaur J, Adya R, Tan BK, Chen J, Randeva HS. Identification of chemerin receptor (ChemR23) in human endothelial cells: chemerin-induced endothelial angiogenesis. Biochem Bio-phys Res Commun 2010; 391(4): 1762‒8.

Muruganandan S, Roman AA, Sinal CJ. Role of chemer-in/CMKLR1 signaling in adipogenesis and osteoblastogene-sis of bone marrow stem cells. J Bone Miner Res 2010; 25(2): 222‒34.

Djurić-Stefanović A, Vasin D, Jovanović S, Lazić Lj, Kovac J, Popović I, et al. Ultrasonographic evaluation of visceral and subcu-taneous abdominal fat tissue before and after bariatric sur-gery. Acta Chir Iugosl 2013; 60(3): 25‒30.

Rothman KJ. BMI-related errors in the measurement of obe-sity. Int J Obes (Lond) 2008; 32 Suppl 3: S56‒9.

Völgyi E, Tylavsky FA, Lyytikäinen A, Suominen H, Alén M, Cheng S. Assessing body composition with DXA and bioim-pedance: effects of obesity, physical activity, and age. Obesi-ty (Silver Spring) 2008; 16(3): 700‒5.

Neeland IJ, Turer AT, Ayers CR, Berry JD, Rohatgi A, Das SR, et al. Body fat distribution and incident cardiovascular dis-ease in obese adults. J Am Coll Cardiol 2015; 65(19): 2150‒1.

Yang GR, Yuan SY, Fu HJ, Wan G, Zhu LX, Bu XL, et al.Neck circumference positively related with central obesi-ty, overweight, and metabolic syndrome in Chinese sub-jects with type 2 diabetes: Beijing Community Diabetes Study 4. Diabetes Care 2010; 33(11): 2465‒7.

Cherneva RV, Georgiev OB, Petrova DS, Manov EI, Petrova JI. Resistin and oxidative stress in non-diabetic sleep apnea pa-tients with nocturnal hypertension. Curr Resp Med Rev 2014; 10(2): 124‒30.

Vonbank A, Saely C, Lins C, Zanolin D, Lieherer A, Muendlein A, et al. The A body shape index and type 2 diabetes are mutually independent predictor of cardiovascular events risk in angiographied coronary patients. JAAC 2018; 71(Suppl 11): DOI: 10.1016/S0735-1097(18)32622-6

Gomez-Peralta F, Abreu C, Cruz-Bravo M, Alcarria E, Gutierrez-Buey G, Krakauer NY, et al. Relationship between "a body shape index (ABSI)" and body composition in obese patients with type 2 diabetes. Diabetol Metab Syndr 2018; 10: 21.

Grant JF, Chittleborough CR, Shi Z, Taylor AW. The association between A Body Shape Index and mortality: Results from an Australian cohort. PLoS One 2017; 12(7): 0181244.

Shin HY, Lee DC, Chu SH, Jeon JY, Lee MK, Im JA, et al. Chemerin levels are positively correlated with abdominal visceral fat accumulation. Clin Endocrinol (Oxf) 2012; 77(1):

Andersson DP, Laurencikiene J, Acosta JR, Rydén M, Arner P. Circulating and Adipose Levels of Adipokines Associated With Insulin Sensitivity in Nonobese Subjects With Type 2 Diabetes. J Clin Endocrinol Metab 2016; 101(10): 3765‒771.

Schlecht I, Fischer B, Behrens G, Leitzmann MF. Relations of Visceral and Abdominal Subcutaneous Adipose Tissue, Body Mass Index, and Waist Circumference to Serum Concen-trations of Parameters of Chronic Inflammation. Obes Facts 2016; 9(3): 144‒57.

McTernan PG, McTernan CL, Chetty R, Jenner K, Fisher FM, Lauer MN, et al. Increased resistin gene and protein expres-sion in human abdominal adipose tissue. J Clin Endocrinol Metab 2002; 87(5): 2407.

Azuma K, Katsukawa F, Oguchi S, Murata M, Yamazaki H, Shi-mada A, et al. Correlation between serum resistin level and adiposity in obese individuals. Obes Res 2003; 11(8): 997‒1001.

Jain SH, Massaro JM, Hoffmann U, Rosito GA, Vasan RS, Raji A, et al. Cross-sectional associations between abdominal and thoracic adipose tissue compartments and adiponectin and resistin in the Framingham Heart Study. Diabetes Care 2009; 32(5): 903‒8.

Jialal I, Devaraj S, Kaur H, Adams-Huet B, Bremer AA. In-creased chemerin and decreased omentin-1 in both adipose tissue and plasma in nascent metabolic syndrome. J Clin Endocrinol Metab 2013; 98(3): E514‒7.

Ouwens DM, Bekaert M, Lapauw B, Van Nieuwenhove Y, Lehr S, Hartwig S, et al. Chemerin as biomarker for insulin sensitivi-ty in males without typical characteristics of metabolic syn-drome. Arch Physiol Biochem 2012; 118(3): 135‒8.

Fülöp P, Seres I, Lőrincz H, Harangi M, Somodi S, Paragh G. As-sociation of chemerin with oxidative stress, inflammation and classical adipokines in non-diabetic obese patients. J Cell Mol Med 2014; 18(7): 1313‒20.

Manduteanu I, Simionescu M. Inflammation in atherosclerosis: a cause or a result of vascular disorders? J Cell Mol Med 2012; 16(9): 1978‒90.

Li ZY, Wang P, Miao CY. Adipokines in inflammation, insu-lin resistance and cardiovascular disease. Clin Exp Pharma-col Physiol 2011; 38(12): 888‒96.

Malo E, Ukkola O, Jokela M, Moilanen L, Kähönen M, Nieminen MS, et al. Resistin is an indicator of the metabolic syndrome according to five different definitions in the Finnish Health 2000 survey. Metab Syndr Relat Disord 2011; 9(3): 203‒10.

Piestrzeniewicz K, Łuczak K, Komorowski J, Maciejewski M, Jankie-wicz Wika J, Goch JH. Resistin increases with obesity and ath-erosclerotic risk factors in patients with myocardial infarc-tion. Metabolism 2008; 57(4): 488‒93.

de Luis DA, Sagrado MG, Conde R, Aller R, Izaola O, de la Fuente B, et al. Relation of resistin levels with cardiovascular risk factors, insulin resistance and inflammation in naïve diabetes obese patients. Diabetes Res Clin Pract 2010; 89(2): 110‒4.

Uslu S, Kebapçi N, Kara M, Bal C. Relationship between adi-pocytokines and cardiovascular risk factors in patients with type 2 diabetes mellitus. Exp Ther Med 2012; 4(1): 113‒20.

Kushiyama A, Sakoda H, Oue N, Okubo M, Nakatsu Y, Ono H, et al. Resistin-like molecule β is abundantly expressed in foam cells and is involved in atherosclerosis development. Arteri-oscler Thromb Vasc Biol 2013; 33(8): 1986‒93.

Jové M, Planavila A, Cabrero A, Novell F, Ros E, Zambón D, et al. Reductions in plasma cholesterol levels after fenofibrate treatment are negatively correlated with resistin expression in human adipose tissue. Metabolism 2003; 52(3): 351‒5.

Osawa H, Tabara Y, Kawamoto R, Ohashi J, Ochi M, Onuma H, et al. Plasma resistin, associated with single nucleotide polymorphism -420, is correlat-ed with insulin resistance, lower HDL cholester-ol, and high-sensitivity C-reactive protein in the Japanese general population. Diabetes Care 2007; 30(6): 1501‒6.

Toan NL, Van Hoan N, Cuong DV, Dung NV, Dung PT, Hang NT, et al. Adipose tissue-derived cyto-kines and their correlations with clinical charac-teristics in Vietnamese patients with type 2 diabe-tes mellitus. Diabetol Metab Syndr 2018; 10: 41.

Published
2020/12/08
Section
Original Paper