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Rheumatology International

, Volume 39, Issue 7, pp 1191–1200 | Cite as

Epicardial adipose tissue thickness in systemic sclerosis patients without overt cardiac disease

  • Duygu Temiz KaradagEmail author
  • Tayfun Sahin
  • Senem Tekeoglu
  • Ozlem Ozdemir Isik
  • Ayten Yazici
  • Ayse Cefle
Observational Research
  • 25 Downloads

Abstract

Systemic sclerosis is associated with an increased prevalence/incidence of coronary artery disease. The aim of this study was to investigate epicardial adipose tissue (EAT) thickness which may contribute to cardio-metabolic risk in systemic sclerosis (SSc) patients without overt cardiac disease. EAT thickness was measured by transthoracic conventional Doppler echocardiography and compared in SSc patients (n = 47) and age- and sex-matched healthy controls (n = 36). The relationships between EAT thickness and markers of cardio-metabolic risk in SSc were examined. EAT thickness was significantly greater in patients with SSc compared to healthy controls (6 [7–5] vs 5 [6.75–3.25], p = 0.041). Compared to controls, erythrocyte sedimentation rate (ESR), C-reactive protein (CRP), leukocyte, neutrophil, B-type natriuretic protein (BNP), fasting plasma insulin and HOMA-IR were elevated (18 [31–10] vs 8.5 [18–4], p < 0.001; 0.4 [0.67–0.18] vs 0.21 [0.48–0.09], p = 0.012; 7510 [8731–5990] vs 6435 [7360–5195], p = 0.002; 4350 [5440–3570] vs 3390 [4168–2903], p < 0.001; 111 [185–74] vs 70 [127–70], p = 0.010; 6.7 [10.5–4.7] vs 4.7 [6.8–4.1], p = 0.008; 1.7 [2.6–1] vs 1.1 [1.7–0.9], p = 0.015, respectively). The total and low-density lipoprotein (LDL)-cholesterol were decreased in SSc patients (197 ± 45 vs 284 ± 36, p = 0.005; 118 [148–84] vs 140 [180–115], p = 0.003, respectively). In patients with SSc, the EAT thickness correlated positively with age, ESR, CRP, insulin, hemoglobin A1c and total and LDL-cholesterol (r = 0.574, p < 0.001; r = 0.352, p = 0.015; r = 0.334, p = 0.022; r = 0.290, p = 0.048; r = 0.317, p = 0.030; r = 0.396, p = 0.006 and r = 0.349, p = 0.016, respectively). Our study confirms that EAT thickness is greater in SSc patients compared to healthy controls using echocardiographic measurements. The results of our study suggest that EAT thickness is a candidate for atherosclerotic risk assessment in SSc.

Keywords

Cardiovascular disease Echocardiography Epicardial adipose tissue thickness Systemic sclerosis 

Notes

Acknowledgements

The authors are grateful to Mr. Jeremy Jones of the Academic Writing Department of Kocaeli University, Izmit, Turkey, for his assistance in editing the English used and for his help and advice concerning the contents of this manuscript.

Author contributions

The authors certify that they take responsibility for the entire work, and they agree that any questions related to the work in the future are appropriately and fully investigated. DTK acquired the clinical data, contributed to the design of the work, performed all the statistical analysis and drafted the manuscript. TS acquired the echocardiography data, data interpretation and revised the work for important intellectual content. ST, OOI, and AY contributed to data interpretation and critical revision of the data and the manuscript AC coordinated the study, data interpretation and contributed to the revision of the data and the drafting of the manuscript.

Funding

This study had no financial support.

Compliance with ethical standards

Conflict of interest

None of the authors has financial or non-financial conflicts of interest to disclose.

Ethical approval

This article does not contain any studies with animals performed by any of the authors. All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study was approved by Kocaeli University School of Medicine Ethics Committee for noninvasive clinical trials with protocol number 178 in 16th June 2015 (KOU KAEK 2015/178). The data of this study were derived during a previous study entitled “Evaluation of the ventricular dysfunction by two-dimensional speckle tracking echocardiography in SSc patients without pulmonary hypertension”.

Informed consent

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

References

  1. 1.
    Chizzolini C, Brembilla NC, Montanari E, Truchetet ME (2011) Fibrosis and immune dysregulation in systemic sclerosis. Autoimmun Rev 10:276–281.  https://doi.org/10.1002/art.30380 CrossRefGoogle Scholar
  2. 2.
    Kahan A, Allanore Y (2006) Primary myocardial involvement in systemic sclerosis. Rheumatol (Oxf) 45(Suppl. 4):7Google Scholar
  3. 3.
    Mavrogeni S, Koutsogeorgopoulou L, Karabela G, Stavropoulos E, Katsifis G, Raftakis J, Plastiras S, Noutsias M, Markousis-Mavrogenis G, Kolovou G (2017) Silent myocarditis in systemic sclerosis detected by cardiovascular magnetic resonance using Lake Louise criteria. BMC Cardiovasc Disord 17(1):187.  https://doi.org/10.1186/s12872-017-0619-x CrossRefGoogle Scholar
  4. 4.
    Au K, Singh MK, Bodukam V, Bae S, Maranian P, Ogawa R, Spiegel B, McMahon M, Hahn B, Khanna D (2011) Atherosclerosis in systemic sclerosis: a systematic review and meta-analysis. Arthritis Rheum 63:2078–2090.  https://doi.org/10.1002/art.30380 CrossRefGoogle Scholar
  5. 5.
    Ungprasert P, Charoenpong P, Ratanasrimetha P, Thongprayoon C, Cheungpasitporn W, Suksaranjit P (2014) Risk of coronary artery disease in patients with systemic sclerosis: a systematic review and meta-analysis. Clin Rheumatol 33:1099–1104.  https://doi.org/10.1007/s10067-014-2681-4 CrossRefGoogle Scholar
  6. 6.
    Szucs G, Tímár O, Szekanecz Z, Dér H, Kerekes G, Szamosi S, Shoenfeld Y, Szegedi G, Soltész P (2007) Endothelial dysfunction precedes atherosclerosis in systemic sclerosis—relevance for prevention of vascular complications. Rheumatol (Oxf) 46:759–762CrossRefGoogle Scholar
  7. 7.
    Blagojevic J, Matucci Cerinic M (2007) Macrovascular involvement in systemic sclerosis: comorbidity or accelerated atherosclerosis? Curr Rheumatol 9:181–182CrossRefGoogle Scholar
  8. 8.
    Montecucco F, Mach F (2009) Common inflammatory mediators orchestrate pathophysiological processes in rheumatoid arthritis and atherosclerosis. Rheumatol (Oxf) 48:11–22.  https://doi.org/10.1093/rheumatology/ken395 CrossRefGoogle Scholar
  9. 9.
    Avina-Zubieta JA, Thomas J, Sadatsafavi M, Lehman AJ, Lacaille D (2012) Risk of incident cardiovascular events in patients with rheumatoid arthritis: a meta-analysis of observational studies. Ann Rheum Dis 71:1524–1529.  https://doi.org/10.1136/annrheumdis-2011-200726 CrossRefGoogle Scholar
  10. 10.
    Szentpetery A, Healy GM, Brady D, Haroon M, Gallagher P, Redmond CE, Fleming H, Duignan J, Dodd JD, FitzGerald O (2018) Higher coronary plaque burden in psoriatic arthritis is independent of metabolic syndrome and associated with underlying disease severity. Arthritis Rheumatol 70:396–407.  https://doi.org/10.1002/art.40389 CrossRefGoogle Scholar
  11. 11.
    Matloch Z, Kotulak T, Haluzık M (2016) The role of epicardial adipose tissue in heart disease. Physiol Res 65:23–32Google Scholar
  12. 12.
    Parisi V, Rengo G, Pagano G, D’Esposito V, Passaretti F, Caruso A, Grimaldi MG, Lonobile T, Baldascino F, De Bellis A, Formisano P, Ferrara N, Leosco D (2015) Epicardial adipose tissue has an increased thickness and is a source of inflammatory mediators in patients with calcific aortic stenosis. Int J Cardiol 186:167–169.  https://doi.org/10.1016/j.ijcard.2015.03.201 CrossRefGoogle Scholar
  13. 13.
    Lima-Martínez MM, Colmenares L, Campanelli Y, Paoli M, Rodney M, Santos RD, Iacobellis G (2018) Epicardial adipose tissue thickness and type 2 diabetes risk according to the FINDRISC modified for Latin America. Clin Investig Arterioscler 18:30077–30079.  https://doi.org/10.1016/j.arteri.2018.06.002 Google Scholar
  14. 14.
    Dey D, Wong ND, Tamarappoo B, Nakazato R, Gransar H, Cheng VY, Ramesh A, Kakadiaris I, Germano G, Slomka PJ, Berman DS (2010) Computer-aided non-contrast CT-based quantification of pericardial and thoracic fat and their associations with coronary calcium and metabolic syndrome. Atherosclerosis 209:136–141.  https://doi.org/10.1016/j.atherosclerosis.2009.08.032 CrossRefGoogle Scholar
  15. 15.
    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 11:304–310CrossRefGoogle Scholar
  16. 16.
    Van den Hoogen F, Khanna D, Fransen J et al (2013) Classification criteria for systemic sclerosis: an American College of Rheumatology/European League Against Rheumatism collaborative initiative. Ann Rheum Dis 72:1747–1755.  https://doi.org/10.1136/annrheumdis-2013-204424 CrossRefGoogle Scholar
  17. 17.
    LeRoy EC, Black C, Fleischmajer R, Jablonska S, Krieg T, Medsger TA Jr, Rowell N, Wollheim F (1988) Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 15:202–205Google Scholar
  18. 18.
    Clements P, Lachenbruch P, Siebold J et al (1995) Inter and intraobserver variability of total skin thickness score (modified Rodnan TSS) in systemic sclerosis. J Rheumatol. 22:1281–1285Google Scholar
  19. 19.
    Medsger TA Jr, Bombardieri S, Czirjak L, Scorza R, Della Rossa A, Bencivelli W (2003) Assessment of disease severity and prognosis. Clin Exp Rheumatol 21:42–46Google Scholar
  20. 20.
    Valentini G, Iudici M, Walker UA, Jaeger VK, Baron M, Carreira P (2017) The European Scleroderma Trials and Research group (EUSTAR) task force for the development of revised activity criteria for systemic sclerosis: derivation and validation of a preliminarily revised EUSTAR activity index. Ann Rheum Dis. 76:270–276CrossRefGoogle Scholar
  21. 21.
    Chobanian AV, Bakris GL, Black HR, Cushman WC, Green LA, Izzo JL Jr, Jones DW, Materson BJ, Oparil S, Wright JT Jr, Roccella EJ, National Heart, Lung, and Blood Institute Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure, National High Blood Pressure Education Program Coordinating Committee (2003) The Seventh Report of the Joint National Committee on Prevention, Detection, Evaluation, and Treatment of High Blood Pressure: the JNC 7 report. JAMA 289:2560–272CrossRefGoogle Scholar
  22. 22.
    Hsu VM, Moreyra AE, Wilson AC, Shinnar M, Shindler DM, Wilson JE, Desai A, Seibold JR (2008) Assessment of pulmonary arterial hypertension in patients with systemic sclerosis: comparison of noninvasive tests with results of right-heart catheterization. J Rheumatol 35:458–465Google Scholar
  23. 23.
    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 28:412–419CrossRefGoogle Scholar
  24. 24.
    WHO (1995) Physical status: the use and interpretation of anthropometry. Report of a WHO Expert Committee. World Health Organ Tech Rep Ser 854:1–452Google Scholar
  25. 25.
    Expert Panel on Detection, Evaluation, and Treatment of High Blood Cholesterol in Adults (2001) Executive summary of the third report of the national cholesterol education program (NCEP) expert panel on detection, evaluation, and treatment of high blood cholesterol in adults (Adult Treatment Panel III). JAMA 285:2486–2497.  https://doi.org/10.1001/jama.285.19.2486 CrossRefGoogle Scholar
  26. 26.
    Lang RM, Bierig M, Devereux RB et al (2005) Chamber Quantification Writing Group; American Society of Echocardiography’s Guidelines and Standards Committee; European Association of Echocardiography. Recommendations for chamber quantification: a report from the American Society of Echocardiography’s Guidelines and Standards Committee and the Chamber Quantification Writing Group, developed in conjunction with the European Association of Echocardiography, a branch of the European Society of Cardiology. J Am Soc Echocardiogr 18:1440–1463CrossRefGoogle Scholar
  27. 27.
    Porter TR, Shillcutt SK, Adams MS, Desjardins G, Glas KE, Olson JJ, Troughton RW (2015) Guidelines for the use of echocardiography as a monitor for therapeutic intervention in adults: a report from the American Society of echocardiography. J Am Soc Echocardiogr 28:40–56.  https://doi.org/10.1016/j.echo.2014.09.009 CrossRefGoogle Scholar
  28. 28.
    Chu SY, Chen YJ, Liu CJ, Tseng WC, Lin MW, Hwang CY, Chen CC, Lee DD, Chen TJ, Chang YT, Wang WJ, Liu HN (2013) Increased risk of acute myocardial infarction in systemic sclerosis: a nationwide population-based study. Am J Med 126:982–988.  https://doi.org/10.1016/j.amjmed.2013.06.025 CrossRefGoogle Scholar
  29. 29.
    Ali H, Ng KR, Low AH (2015) A qualitative systematic review of the prevalence of coronary artery disease in systemic sclerosis. Int J Rheum Dis 18:276–286.  https://doi.org/10.1111/1756-185X.12566 CrossRefGoogle Scholar
  30. 30.
    Long BD, Stojanovska J, Brown RKJ, Attili AK, Jackson EA, Ognenovski V (2017) Increased epicardial fat volume is independently associated with the presence and severity of systemic sclerosis. Acad Radiol 24:1473–1481.  https://doi.org/10.1016/j.acra.2017.07.003 CrossRefGoogle Scholar
  31. 31.
    Rabkin SW (2014) The relationship between epicardial fat and indices of obesity and the metabolic syndrome: a systematic review and meta-analysis. Metab Syndr Relat Disord 12:31–42.  https://doi.org/10.1089/met.2013.0107 CrossRefGoogle Scholar
  32. 32.
    Singh N, Singh H, Khanijoun HK, Iacobellis G (2007) Echocardiographic assessment of epicardial adipose tissue–a marker of visceral adiposity. McGill Med J 10:26–30Google Scholar
  33. 33.
    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 (2003) Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108(20):2460–2466CrossRefGoogle Scholar
  34. 34.
    Medsger TA Jr, Silman AJ, Steen VD et al (1999) A disease severity scale for systemic sclerosis: development and testing. J Rheumatol 26:2159–2167Google Scholar
  35. 35.
    Temiz A, Gökmen F, Gazi E, Akbal A, Barutçu A, Bekler A, Altun B, Tan YZ, Güneş F, Şen H (2015) Epicardial adipose tissue thickness, flow-mediated dilatation of the brachial artery, and carotid intima-media thickness, Associations in rheumatoid arthritis patients. Herz 40:217–224.  https://doi.org/10.1007/s00059-014-4140-z CrossRefGoogle Scholar
  36. 36.
    Iacobellis G, Ribaudo MC, Assael F, Vecci E, Tiberti C, Zappaterreno A, Di Mario U, Leonetti F (2003) Echocardiographic epicardial adipose tissue is related to anthropometric and clinical parameters of metabolic syndrome: a new indicator of cardiovascular risk. J Clin Endocrinol Metab 88:5163–5168CrossRefGoogle Scholar
  37. 37.
    Kim BJ, Kim HS, Kang JG, Kim BS, Kang JH (2016) Association of epicardial fat volume and nonalcoholic fatty liver disease with metabolic syndrome: From the CAESAR study. J Clin Lipidol 10:1423–1430.  https://doi.org/10.1016/j.jacl.2016.09.007 CrossRefGoogle Scholar
  38. 38.
    Iudici M, Fasano S, Iacono D, Russo B, Cuomo G, Valentini G (2014) Prevalence and factors associated with glucocorticoids (GC) use in systemic sclerosis (SSc): a systematic review and metaanalysis of cohort studies and registries. Clin Rheumatol 33:153–164.  https://doi.org/10.1007/s10067-013-2422-0 CrossRefGoogle Scholar
  39. 39.
    Flüchter S, Haghi D, Dinter D, Heberlein W, Kühl HP, Neff W, Sueselbeck T, Borggrefe M, Papavassiliu T (2007) Volumetric assessment of epicardial adipose tissue with cardiovascular magnetic resonance imaging. Obesity 15:870–878CrossRefGoogle Scholar
  40. 40.
    Abbara S, Desai JC, Cury RC, Butler J, Nieman K, Reddy V (2005) Mapping epicardial fat with multi-detector computed tomography to facilitate percutaneous transepicardial arrhythmia ablation. Eur J Radiol 57:417–422CrossRefGoogle Scholar
  41. 41.
    Yiu KH, Schouffoer AA, Marsan NA, Ninaber MK, Stolk J, Vlieland TV, Scherptong RW, Delgado V, Holman ER, Tse HF, Huizinga TW, Bax JJ, Schuerwegh AJ (2011) Left ventricular dysfunction assessed by speckle tracking strain analysis in patients with systemic sclerosis: relationship to functional capacity and ventricular arrhythmias. Arthrit Rheumat 63:3969–3978.  https://doi.org/10.1002/art.30614 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Division of Rheumatology, Department of Internal MedicineKocaeli University School of MedicineUmuttepe-İzmitTurkey
  2. 2.Division of CardiologyKocaeli University School of MedicineUmuttepe-İzmitTurkey

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