Abstract
Chronic inflammation from autoimmune diseases has shown to be a risk factor for atherosclerosis, subsequently leading to cardiovascular disease. Endothelial dysfunction is the early pathogenesis of atherosclerosis in chronic inflammation, but the risk of atherosclerosis in sarcoidosis is less well defined. This meta-analysis aimed to explore the association of subclinical atherosclerosis and arterial stiffness in sarcoidosis. A comprehensive search of the MEDLINE and EMBASE databases was performed from date of inception through August 2017. The inclusion criterion was observational studies evaluating the association between sarcoidosis, subclinical atherosclerosis, and arterial stiffness by measuring pulse wave velocity (PWV). Definitions of sarcoidosis and methods to assess PWV were recorded for each study. The pooled standardized mean difference (SMD) of PWV and 95% confidence interval (CI) was calculated using a random-effects meta-analysis. The between-study heterogeneity of effect size was quantified using the Q statistic and I 2. Data were extracted from five observational studies involving 499 subjects. Pooled result demonstrated a significant increase in PWV in patients who have sarcoidosis compared with controls (SMD = 0.57 m/s; 95% CI 0.21–0.92, p value = 0.002, I 2 = 75%, P heterogeneity < 0.01). After excluding studies with low or moderate quality, there was an increase in PWV in sarcoidosis compared with controls (SMD = 0.29 m/s; 95% CI 0.00–0.57, p value = 0.05, I 2 = 55%, P heterogeneity = 0.08). Our study suggests that sarcoidosis is associated with increased arterial stiffness and therefore at risk of subclinical atherosclerosis. Prospective study is required to investigate the association of subclinical atherosclerosis causing overt cardiovascular disease in patients with sarcoidosis.
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References
Mason JC, Libby P (2015) Cardiovascular disease in patients with chronic inflammation: mechanisms underlying premature cardiovascular events in rheumatologic conditions. Eur Heart J 36(8):482–49c
Thomas KW, Hunninghake GW (2003) Sarcoidosis. Sarcoidosis JAMA 289(24):3300–3303. https://doi.org/10.1001/jama.289.24.3300
Dumas O, Abramovitz L, Wiley AS, Cozier YC, Camargo CA Jr (2016) Epidemiology of sarcoidosis in a prospective cohort study of U.S. women. Ann Am Thorac Soc 13(1):67–71. https://doi.org/10.1513/AnnalsATS.201508-568BC
Rybicki BA, Major M, Popovich J Jr, Maliarik MJ, Iannuzzi MC (1997) Racial differences in sarcoidosis incidence: a 5-year study in a health maintenance organization. Am J Epidemiol 145(3):234–241. https://doi.org/10.1093/oxfordjournals.aje.a009096
Libby P, Ridker PM, Maseri A (2002) Inflammation and atherosclerosis. Circulation 105(9):1135–1143. https://doi.org/10.1161/hc0902.104353
Asmar R, Benetos A, Topouchian J, Laurent P, Pannier B, Brisac AM, Target R, Levy BI (1995) Assessment of arterial distensibility by automatic pulse wave velocity measurement. Validation and clinical application studies. Hypertension 26(3):485–490. https://doi.org/10.1161/01.HYP.26.3.485
Takemura T, Shishiba T, Akiyama O, Oritsu M, Matsui Y, Eishi Y (1997) Vascular involvement in cutaneous sarcoidosis. Pathol Int 47(2–3):84–89. https://doi.org/10.1111/j.1440-1827.1997.tb03725.x
Sekiguchi M, Yazaki Y, Isobe M, Hiroe M (1996) Cardiac sarcoidosis: diagnostic, prognostic, and therapeutic considerations. Cardiovasc Drugs Ther 10(5):495–510. https://doi.org/10.1007/BF00050989
Ungprasert P, Crowson CS, Matteson EL (2017) Risk of cardiovascular disease among patients with sarcoidosis: a population-based retrospective cohort study, 1976–2013. Eur Respir J 49(2)
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, Moher D, Becker BJ, Sipe TA, Thacker SB (2000) Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA 283(15):2008–2012. https://doi.org/10.1001/jama.283.15.2008
listed Na. Statement on sarcoidosis. Joint statement of the American Thoracic Society (ATS), the European Respiratory Society (ERS) and the World Association of Sarcoidosis and Other Granulomatous Disorders (WASOG) adopted by the ATS Board of Directors and by the ERS Executive Committee (1999) Am J Respir Crit Care Med 160(2):736–55
Stang A (2010) Critical evaluation of the Newcastle-Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses. Eur J Epidemiol 25(9):603–605. https://doi.org/10.1007/s10654-010-9491-z
Hozo SP, Djulbegovic B, Hozo I (2005) Estimating the mean and variance from the median, range, and the size of a sample. BMC Med Res Methodol 5(1):13. https://doi.org/10.1186/1471-2288-5-13
Wan X, Wang W, Liu J, Tong T (2014) Estimating the sample mean and standard deviation from the sample size, median, range and/or interquartile range. BMC Med Res Methodol 14(1):135. https://doi.org/10.1186/1471-2288-14-135
Higgins JPT GS (2011) Cochrane handbook for systematic reviews of interventions. The Cochrane Collaboration
Higgins JP, Thompson SG, Deeks JJ, Altman DG (2003) Measuring inconsistency in meta-analyses. BMJ 327(7414):557–560. https://doi.org/10.1136/bmj.327.7414.557
Sterne JA, Egger M (2001) Funnel plots for detecting bias in meta-analysis: guidelines on choice of axis. J Clin Epidemiol 54(10):1046–1055. https://doi.org/10.1016/S0895-4356(01)00377-8
Tuleta I, Skowasch D, Biener L, Pizarro C, Schueler R, Nickenig G et al (2017) Impaired vascular function in sarcoidosis patients. Adv Exp Med Biol 980:1–9. https://doi.org/10.1007/5584_2016_203
Moyssakis I, Gialafos E, Tentolouris N, Floudas CS, Papaioannou TG, Kostopoulos C, Latsi P, Vaiopoulos G, Votteas V, Rapti A (2008) Impaired aortic elastic properties in patients with systemic sarcoidosis. Eur J Clin Investig 38(2):82–89. https://doi.org/10.1111/j.1365-2362.2007.01906.x
Ardic I, Yarlioglues M, Dogdu O, Buyukoglan H, Kanbay A, Akpek M, Bol C, Yuksel M, Akkaya E, Vuruskan E, Kaya MG (2012) Assessment of aortic elastic properties in patients with sarcoidosis. Blood Press 21(5):286–292. https://doi.org/10.3109/08037051.2012.656397
Samanci NS, Poturoglu S, Samanci C, Alis D, Emre HO, Koldas M, Ozcelik HK, Durmus T, Kantarci F, Ozturk S (2017) Evaluation of carotid intima-media thickness with vascular endothelial growth factor and malondialdehyde levels in patients with sarcoidosis. Diagn Interv Imaging 98(7–8):557–561. https://doi.org/10.1016/j.diii.2017.04.004
Balci H, Sipahi Demirkok S, Yildiz M, Metin G, Hacibekiroglu M, Simsek G (2010) The relationship between the inflammatory markers and arterial distensibility in patients with sarcoidosis. Trakya Univ Tip Fak Derg 27(1):44–50
Hellmann M, Dudziak M, Dubaniewicz A (2015) Increased pulse wave velocity in pulmonary sarcoidosis: a preliminary study. Pol Arch Med Wewn 125(6):475–477
Siasos G, Tousoulis D, Gialafos E, Oikonomou E, Zaromitidou M, Aggeli C, Korompelis P, Kallianos A, Rapti A, Zisimos K, Marinos G, Stefanadis C, Papavassiliou AG (2011) Association of sarcoidosis with endothelial function, arterial wall properties, and biomarkers of inflammation. Am J Hypertens 24(6):647–653. https://doi.org/10.1038/ajh.2011.30
Siasos G, Paraskevopoulos T, Gialafos E, Rapti A, Oikonomou E, Zaromitidou M, Mourouzis K, Siasou G, Gouliopoulos N, Tsalamandris S, Vlasis K, Stefanadis C, Papavassiliou AG, Tousoulis D (2015) Vascular function and ocular involvement in sarcoidosis. Microvasc Res 100:54–58. https://doi.org/10.1016/j.mvr.2015.03.008
Tuleta I, Pingel S, Biener L, Pizarro C, Hammerstingl C, Ozturk C et al (2016) Atherosclerotic vessel changes in sarcoidosis. Adv Exp Med Biol 910:23–30. https://doi.org/10.1007/5584_2015_205
Maksimowicz-McKinnon K, Hoffman GS (2004) Large-vessel vasculitis. Semin Respir Crit Care Med 25(5):569–579. https://doi.org/10.1055/s-2004-836148
Chapelon-Abric C, de Zuttere D, Duhaut P, Veyssier P, Wechsler B, Huong DL et al (2004) Cardiac sarcoidosis: a retrospective study of 41 cases. Medicine (Baltimore) 83(6):315–334. https://doi.org/10.1097/01.md.0000145367.17934.75
Fernandes SR, Singsen BH, Hoffman GS (2000) Sarcoidosis and systemic vasculitis. Semin Arthritis Rheum 30(1):33–46. https://doi.org/10.1053/sarh.2000.8364
Stefanadis C, Vlachopoulos C, Karayannacos P, Boudoulas H, Stratos C, Filippides T, Agapitos M, Toutouzas P (1995) Effect of vasa vasorum flow on structure and function of the aorta in experimental animals. Circulation 91(10):2669–2678. https://doi.org/10.1161/01.CIR.91.10.2669
Hunninghake GW, Costabel U, Ando M, Baughman R, Cordier JF, du Bois R, Eklund A, Kitaichi M, Lynch J, Rizzato G, Rose C, Selroos O, Semenzato G, Sharma OP (1999) ATS/ERS/WASOG statement on sarcoidosis. American Thoracic Society/European Respiratory Society/World Association of Sarcoidosis and other Granulomatous Disorders. Sarcoidosis Vasc Diffuse Lung Dis 16(2):149–173
Kul S, Kutlu GA, Guvenc TS, Kavas M, Demircioglu K, Yilmaz Y, Yakar HI, Kanbay A, Boga S, Caliskan M (2017) Coronary flow reserve is reduced in sarcoidosis. Atherosclerosis 264:115–121. https://doi.org/10.1016/j.atherosclerosis.2017.05.005
Santos-Gallego CG, Weiss AJ, Sanz J (2017) Non-cardiac sarcoid actually affects the heart by reducing coronary flow reserve. Atherosclerosis 264:74–76. https://doi.org/10.1016/j.atherosclerosis.2017.07.006
Davies JI, Struthers AD (2003) Pulse wave analysis and pulse wave velocity: a critical review of their strengths and weaknesses. J Hypertens 21(3):463–472. https://doi.org/10.1097/00004872-200303000-00004
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Yong, W.C., Sanguankeo, A. & Upala, S. Association between sarcoidosis, pulse wave velocity, and other measures of subclinical atherosclerosis: a systematic review and meta-analysis. Clin Rheumatol 37, 2825–2832 (2018). https://doi.org/10.1007/s10067-017-3926-9
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DOI: https://doi.org/10.1007/s10067-017-3926-9