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01.07.2022 | Original Article

Increased epicardial adipose tissue thickness correlates with endothelial dysfunction in spondyloarthritis

verfasst von: Aicha Ben Tekaya, Takwa Mehmli, Imtinene Ben Mrad, Ahmed Fendri, Seif Boukriba, Selma Bouden, Leila Rouached, Rawdha Tekaya, Olfa Saidane, Ines Mahmoud, Leila Abdelmoula

Erschienen in: Clinical Rheumatology | Ausgabe 10/2022

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Abstract

Introduction

We aimed to investigate the relationship between epicardial adipose tissue (EAT) thickness, flow-mediated dilation (FMD), and carotid intima-media thickness (cIMT) in spondyloarthritis (SpA) patients compared to healthy controls.

Methods

We performed a cross-sectional study including SpA patients aged ≤ 50 years without traditional cardiovascular risk factors and healthy controls matched for age and gender. Baseline characteristics, laboratory data, and SpA-related parameters were recorded. All participants underwent ultrasound examination with measurement of EAT thickness, FMD, and cIMT by both an experienced cardiologist and radiologist blinded to clinical data. The relationships between the ultrasound measurements were analyzed using Spearman’s correlation coefficient and Person correlation.

Results

The study included 94 subjects (47 SpA and 47 healthy controls). The sex-ratio was 2.35; the median age of patients was 36 years (IQR: 28–46), and the median disease duration was 11 years (IQR: 5–16). Compared to the control group, SpA patients had significantly higher values of EAT thickness (p = 0.001) and cIMT (p < 0.0001). FMD values were significantly lower in SpA patients compared to controls (p = 0.008). The univariate analysis detected a significant negative association between EAT thickness and FMD (p = 0.026; r = − 0.325), and between left cIMT and FMD (p = 0.027; r = − 0.322). No association was found between EAT thickness and cIMT.

Conclusion

EAT thickness, FMD, and cIMT were significantly impaired in SpA patients compared with healthy controls supporting evidence of accelerated atherosclerosis in SpA. EAT thickness was correlated to endothelial dysfunction suggesting the role of EAT in predicting the early reversible stages of atherosclerosis.

Key Points

• Spondyloarthritis is associated with impaired subclinical atherosclerosis markers accurately increased epicardial fat and carotid intima-media thickness and endothelial dysfunction.

• Increased epicardial fat thickness is correlated with impaired endothelial function in spondyloarthritis patients.

Peters MJ, van der Horst-Bruinsma IE, Dijkmans BA, Nurmohamed MT (2004) Cardiovascular risk profile of patients with spondylarthropathies, particularly ankylosing spondylitis and psoriatic arthritis. Semin Arthritis Rheum 34:585–592. https://doi.org/10.1016/j.semarthrit.2004.07.010CrossRefPubMed

Łosińska K, Korkosz M, Kwaśny-Krochin B (2019) Endothelial dysfunction in patients with ankylosing spondylitis. Reumatologia/Rheumatology 57:100–105. https://doi.org/10.5114/reum.2019.84815CrossRefPubMed

Kerekes G, Soltész P, Nurmohamed MT, Gonzalez-Gay MA, Turiel M, Végh E, Shoenfeld Y, McInnes I, Szekanecz Z (2012) Validated methods for assessment of subclinical atherosclerosis in rheumatology. Nat Rev Rheumatol 8:224–234. https://doi.org/10.1038/nrrheum.2012.16CrossRefPubMed

Moroni L, Selmi C, Angelini C, Meroni PL (2017) Evaluation of endothelial function by flow-mediated dilation: a comprehensive review in rheumatic disease. Arch Immunol Ther Exp (Warsz) 65:463–475. https://doi.org/10.1007/s00005-017-0465-7CrossRef

Shimabukuro M, Hirata Y, Tabata M, Dagvasumberel M, Sato H, Kurobe H, Fukuda D, Soeki T, Kitagawa T, Takanashi S, Sata M (2013) Epicardial adipose tissue volume and adipocytokine imbalance are strongly linked to human coronary atherosclerosis. Arterioscler Thromb Vasc Biol 33:1077–1084. https://doi.org/10.1161/ATVBAHA.112.300829CrossRefPubMed

Marchington JM, Mattacks CA, Pond CM (1989) Adipose tissue in the mammalian heart and pericardium: structure, foetal development and biochemical properties. Comp Biochem Physiol B 94:225–232. https://doi.org/10.1016/0305-0491(89)90337-4CrossRefPubMed

Ansari MA, Mohebati M, Poursadegh F, Foroughian M, Shamloo AS (2018) Is echocardiographic epicardial fat thickness increased in patients with coronary artery disease? A systematic review and meta-analysis. Electron Physician 10:7249–7258. https://doi.org/10.19082/7249CrossRefPubMedPubMedCentral

Resorlu H, Akbal A, Resorlu M, Gokmen F, Ates C, Uysal F, Adam G, Aylanc N, Arslan M, İnceer BS (2015) Epicardial adipose tissue thickness in patients with ankylosing spondylitis. Clin Rheumatol 34:295–299. https://doi.org/10.1007/s10067-014-2568-4CrossRefPubMed

Surucu GD, Yildirim A, Yetisgin A, Akturk E (2019) Epicardial adipose tissue thickness as a new risk factor for atherosclerosis in patients with ankylosing spondylitis. J Back Musculoskelet Rehabil 32:237–243. https://doi.org/10.3233/BMR-160650CrossRefPubMed

10.

Iacobellis G, Willens HJ (2009) Echocardiographic epicardial fat: a review of research and clinical applications. J Am Soc Echocardiogr 22:1311–1319; quiz 1417–8. https://doi.org/10.1016/j.echo.2009.10.013CrossRefPubMed

11.

Thijssen DHJ, Bruno RM, van Mil ACCM, Holder SM, Faita F, Greyling A, Zock PL, Taddei S, Deanfield JE, Luscher T, Green DJ, Ghiadoni L (2019) Expert consensus and evidence-based recommendations for the assessment of flow-mediated dilation in humans. Eur Heart J 40:2534–2547. https://doi.org/10.1093/eurheartj/ehz350CrossRefPubMed

12.

Choi H, Uceda DE, Dey AK, Mehta NN (2019) Application of Non-invasive Imaging in Inflammatory Disease Conditions to Evaluate Subclinical Coronary Artery Disease. Curr Rheumatol Rep 22:1. https://doi.org/10.1007/s11926-019-0875-0CrossRefPubMed

13.

Demir K, Avcı A, Ergulu Esmen S, Tuncez A, Yalcın MU, Yılmaz A, Altunkeser BB (2021) Assessment of arterial stiffness and epicardial adipose tissue thickness in predicting the subclinical atherosclerosis in patients with ankylosing spondylitis. Clin Exp Hypertens 43:169–174. https://doi.org/10.1080/10641963.2020.1833025CrossRefPubMed

14.

Çağlar SO, Boyraz İ, Erdem F, Yazici S, Çağlar H, Koç B, Çağlar E, Yazici M (2016) Evaluation of Atrial Conduction Times, Epicardial Fat Thickness and Carotid Intima-Media Thickness in Patients With Ankylosing Spondylitis. Arch Rheumatol 31:353–358. https://doi.org/10.5606/ArchRheumatol.2016.5867CrossRefPubMedPubMedCentral

15.

Büyükterzi Z, Alpaydin MS, Akkurt HE, Yilmaz H (2019) Epicardial adipose tissue thickness is associated with disease severity in patients with newly- diagnosed ankylosing spondylitis. Kocaeli Med J 8:97–103. https://doi.org/10.5505/ktd.2019.80037CrossRef

16.

Üstün N, Kurt M, Atci N, Yağiz E, Güler H, Turhanoğlu A (2014) Increased epicardial fat tissue is a marker of subclinic atherosclerosis in ankylosing spondylitis. Arch Rheumatol 29:267–272. https://doi.org/10.5606/ArchRheumatol.2014.4606CrossRef

17.

Boyraz I, Caglar S, Erdem F, Yazici M, Yazici S, Koc B, Gunduz R, Karakoyun A (2016) Assessment of relation between neutrophil lympocyte, platelet lympocyte ratios and epicardial fat thickness in patients with ankylosing spondylitis. Med Glas (Zenica) 13:14–17. https://doi.org/10.17392/832-16CrossRef

18.

Öz A, Coşkun H, Çınar T, Efe SÇ, Öz N, Ayça B, Karabağ T, Aytekin E (2020) Evaluation of atrial conduction times and epicardial adipose Ttssue thickness in patients with ankylosing spondylitis. Istanb Med J 21:430–435. https://doi.org/10.4274/imj.galenos.2020.35002CrossRef

19.

Bai R, Zhang Y, Liu W, Ma C, Chen X, Yang J, Sun D (2019) The relationship of ankylosing spondylitis and subclinical atherosclerosis: a systemic review and meta-analysis. Angiology 70:492–500. https://doi.org/10.1177/0003319718814309CrossRefPubMed

20.

Cure E, Icli A, Uslu AU, Sakiz D, Cure MC, Baykara RA, Yavuz F, Arslan S, Kucuk A (2018) Atherogenic index of plasma: a useful marker for subclinical atherosclerosis in ankylosing spondylitis: AIP associate with cIMT in AS. Clin Rheumatol 37:1273–1280. https://doi.org/10.1007/s10067-018-4027-0CrossRefPubMed

21.

Serdaroğlu Beyazal M, Erdoğan T, Türkyılmaz AK, Devrimsel G, Cüre MC, Beyazal M, Sahin I (2016) Relationship of serum osteoprotegerin with arterial stiffness, preclinical atherosclerosis, and disease activity in patients with ankylosing spondylitis. Clin Rheumatol 35:2235–2241. https://doi.org/10.1007/s10067-016-3198-9CrossRefPubMed

22.

Hamdi W, Chelli BM, Zouch I, Ghannouchi MM, Haouel M, Ladeb MF, Kchir MM (2012) Assessment of preclinical atherosclerosis in patients with ankylosing spondylitis. J Rheumatol 39:322–326. https://doi.org/10.3899/jrheum.110792CrossRefPubMed

23.

Bodnár N, Kerekes G, Seres I, Paragh G, Kappelmayer J, Némethné ZG, Szegedi G, Shoenfeld Y, Sipka S, Soltész P, Szekanecz Z, Szántó S (2011) Assessment of subclinical vascular disease associated with ankylosing spondylitis. J Rheumatol 38:723–729. https://doi.org/10.3899/jrheum.100668CrossRefPubMed

24.

Verma I, Syngle A, Krishan P, Garg N (2017) Endothelial progenitor cells as a marker of endothelial dysfunction and atherosclerosis in ankylosing spondylitis: a cross-sectional study. Int J Angiol 26:36–42. https://doi.org/10.1055/s-0036-1593445CrossRefPubMed

25.

Sari I, Okan T, Akar S, Cece H, Altay C, Secil M, Birlik M, Onen F, Akkoc N (2006) Impaired endothelial function in patients with ankylosing spondylitis. Rheumatology 45:283–286. https://doi.org/10.1093/rheumatology/kei145CrossRefPubMed

26.

Aydın H, Toprak A, Deyneli O, Yazıcı D, Tarçın Ö, Sancak S, Yavuz D, Akalin S (2010) Epicardial fat tissue thickness correlates with endothelial dysfunction and other cardiovascular risk factors in patients with metabolic syndrome. Metab Syndr Relat Disord 8:229–234. https://doi.org/10.1089/met.2009.0080CrossRefPubMed

27.

Aslan AN, Keleş T, Ayhan H, Kasapkara HA, Akçay M, Durmaz T, Sarı C, Baştuğ S, Çakır B, Bozkurt E (2015) The relationship between epicardial fat thickness and endothelial dysfunction in type I diabetes mellitus. Echocardiography 32:1745–1753. https://doi.org/10.1111/echo.12960CrossRefPubMed

28.

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-zCrossRefPubMed

29.

Mazurek T, Zhang L, Zalewski A, Mannion JD, Diehl JT, Arafat H, Blat LS, Brien SO, Keiper EA, Johnson AG, Martin J, Goldstein BJ, Shi Y (2003) Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108:2460–2466. https://doi.org/10.1161/01.CIR.0000099542.57313.C5CrossRefPubMed

30.

Ahn SG, Lim HS, Joe DY, Kang SJ, Choi BJ, Choi SY, Yoon MH, Hwang GS, Tahk SJ, Shin JH (2008) Relationship of epicardial adipose tissue by echocardiography to coronary artery disease. Heart 94:e7. https://doi.org/10.1136/hrt.2007.118471CrossRefPubMed

31.

Tachibana M, Miyoshi T, Osawa K, Toh N, Oe H, Nakamura K, Naito T, Sato S, Kanazawa S, Ito H (2016) Measurement of epicardial fat thickness by transthoracic echocardiography for predicting high-risk coronary artery plaques. Heart Vessels 31:1758–1766. https://doi.org/10.1007/s00380-016-0802-5CrossRefPubMed

32.

Celermajer DS, Sorensen KE, Bull C, Robinson J, Deanfield JE (1994) Endothelium-dependent dilation in the systemic arteries of asymptomatic subjects relates to coronary risk factors and their interaction. J Am Coll Cardiol 24:1468–1474. https://doi.org/10.1016/0735-1097(94)90141-4CrossRefPubMed

33.

Lakshmanan S, Shekar C, Kinninger A, Birudaraju D, Dahal S, Onuegbu A, Cherukuri L, Hamal S, Flores F, Dailing C, Roy SK, Budoff M (2020) Association of flow mediated vasodilation and burden of subclinical atherosclerosis by coronary CTA. Atherosclerosis 302:15–19. https://doi.org/10.1016/j.atherosclerosis.2020.04.009CrossRefPubMed

34.

Tan KCB, Xu A, Chow WS, Lam MCW, Ai VHG, Tam SCF, Lam KSL (2004) Hypoadiponectinemia is associated with impaired endothelium-dependent vasodilation. J Clin Endocrinol Metab 89:765–769. https://doi.org/10.1210/jc.2003-031012CrossRefPubMed

35.

Dick GM, Katz PS, Farias M, Morris M, James J, Knudson JD, Tune JD (2006) Resistin impairs endothelium-dependent dilation to bradykinin, but not acetylcholine, in the coronary circulation. Am J Physiol Heart Circ Physiol 291:H2997-3002. https://doi.org/10.1152/ajpheart.01035.2005CrossRefPubMed

36.

Karastergiou K, Evans I, Ogston N, Miheisi N, Nair D, Kaski JC, Jahangiri M, Vidya MA (2010) Epicardial adipokines in obesity and coronary artery disease induce atherogenic changes in monocytes and endothelial cells. Arterioscler Thromb Vasc Biol 30:1340–1346. https://doi.org/10.1161/ATVBAHA.110.204719CrossRefPubMed

37.

Zhang C (2008) The role of inflammatory cytokines in endothelial dysfunction. Basic Res Cardiol 103:398–406. https://doi.org/10.1007/s00395-008-0733-0CrossRefPubMedPubMedCentral

38.

Picchi A, Gao X, Belmadani S, Potter BJ, Focardi M, Chilian WM, Zhang C (2006) Tumor necrosis factor-α induces endothelial dysfunction in the prediabetic metabolic syndrome. Circ Res 99:69–77. https://doi.org/10.1161/01.RES.0000229685.37402.80CrossRefPubMed

39.

Wassmann S, Stumpf M, Strehlow K, Schmid A, Schieffer B, Böhm M, Nickenig G (2004) Interleukin-6 induces oxidative stress and endothelial dysfunction by overexpression of the angiotensin II type 1 receptor. Circ Res 94:534–541. https://doi.org/10.1161/01.RES.0000115557.25127.8DCrossRefPubMed

40.

Sengul C, Cevik C, Ozveren O, Oduncu V, Sunbul A, Akgun T, Can MM, Semiz E, Dindar I (2011) Echocardiographic epicardial fat thickness is associated with carotid intima-media thickness in patients with metabolic syndrome. Echocardiography 28:853–858. https://doi.org/10.1111/j.1540-8175.2011.01471.xCrossRefPubMed

41.

Erdoğan T, Durakoğlugil ME, Çetin M, Altan Kocaman S, Duman H, Çiçek Y, Şatıroğlu Ö (2019) Epicardial adipose tissue predicts carotid intima-media thickness independently of body mass index and waist circumference. Acta Cardiol Sin 35:32–41. https://doi.org/10.6515/ACS.201901_35(1).20180628ACrossRefPubMedPubMedCentral

42.

Nelson MR, Mookadam F, Thota V, Emani U, Al Harthi M, Lester SJ, Cha S, Stepanek J, Hurst RT (2011) Epicardial fat: an additional measurement for subclinical atherosclerosis and cardiovascular risk stratification? J Am Soc Echocardiogr 24:339–345. https://doi.org/10.1016/j.echo.2010.11.008CrossRefPubMed

43.

Iacobellis G (2015) Local and systemic effects of the multifaceted epicardial adipose tissue depot. Nat Rev Endocrinol 11:363–371. https://doi.org/10.1038/nrendo.2015.58CrossRefPubMed

44.

Reiss AB, Siegart NM, De Leon J (2017) Interleukin-6 in atherosclerosis: atherogenic or atheroprotective? Clin Lipidol 12:14–23. https://doi.org/10.1080/17584299.2017.1319787CrossRef

Titel: Increased epicardial adipose tissue thickness correlates with endothelial dysfunction in spondyloarthritis
verfasst von: Aicha Ben Tekaya
Takwa Mehmli
Imtinene Ben Mrad
Ahmed Fendri
Seif Boukriba
Selma Bouden
Leila Rouached
Rawdha Tekaya
Olfa Saidane
Ines Mahmoud
Leila Abdelmoula
Publikationsdatum: 01.07.2022
Verlag: Springer International Publishing
Erschienen in: Clinical Rheumatology / Ausgabe 10/2022
Print ISSN: 0770-3198
Elektronische ISSN: 1434-9949
DOI: https://doi.org/10.1007/s10067-022-06261-5

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Increased epicardial adipose tissue thickness correlates with endothelial dysfunction in spondyloarthritis

Abstract

Introduction

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Results

Conclusion

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