Abstract
Cardiac coronary Ca score (CCS), and extra coronary Ca score (ECCS) estimation in asymptomatic systemic sclerosis (SSc) patients and their relation to different disease and patients’ variables. The CCS and ECCS were estimated in asymptomatic 20 SSc patients compared to 20 age and sex-matched healthy control using non-contrast cardiac computed tomography. All were applied for cardiac history taking, examination, echocardiography, body mass index (BMI), complete blood picture, erythrocyte sedimentation rate, and lipid profile estimation. The SSc patients were 11 females and 9 males with a mean age of (42.55 ± 9.145) and mean disease duration (12.9 ± 6.774). CCS was reported in 9 (45%) SSc cases and 2 (10%) of the control; (p = 0.013) and was significantly greater in SSc patients (58.4 ± 175.443) than in the control group (0.7 ± 2.25); (p = 0.01). The ECCS was significantly higher in SSc cases (194.45 ± 586.511) than control group (2.8 ± 7.8); (p = 0.001) and reported in 16 (80%) SSc cases and 3 (15%) of controls; (p = 0.000). Limited scleroderma cases had higher scores than diffuse type. Patients with total ca score (> 100) were older (p = 0.016), had longer disease duration (p = 0.001) and greater BMI (p = 0.002). Significant correlation was found between the log-transformed CCS and disease duration, age, BMI, left ventricular mass, and mass index. Systemic sclerosis patients are at increased risk of subclinical cardiovascular disease determined by cardiac Ca scoring as a noninvasive and reliable method. Extra coronary calcification may be an earlier indicator for this. Disease duration is a determinant risk factor for cardiac calcification in SSc.
Key Points • Although the association between interleukin-6 (IL-6) promoter polymorphism and rheumatic arthritis (RA) has been discussed in the previous meta-analysis, their conclusions are inconsistent. • Systemic sclerosis patients are at high risk of accelerated atherosclerosis and cardiovascular diseases. Coronary atherosclerosis was previously estimated in SSc patients through coronary angiography. A novel method of assessing coronary artery disease is the coronary calcium score, as determined by multidetector computed tomography, it measures coronary artery calcification that occurs in atherosclerotic plaque. In this study, the cardiac coronary and extra coronary Ca score were evaluated in relation to disease characteristics in asymptomatic SSC patients for early detection of coronary artery disease. |
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Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Fernández-Codina A, Simeón-Aznar CP, Pinal-Fernandez I, Rodríguez-Palomares J, Pizzi MN, Hidalgo CE, Del Castillo AG et al (2017) Cardiac involvement in systemic sclerosis: differences between clinical subsets and influence on survival. Rheumatol Int 37(1):75–84
Ngian GS, Sahhar J, Wicks IP, Van Doornum S (2011) Cardiovascular disease in systemic sclerosis-an emerging association? Arthritis Res Ther 13(4):1–10
Magda SL, Mincu RI, Mihai CM, Cinteza M, Vinereanu D (2015) Atherosclerosis in systemic sclerosis: a Modern Controversy. Maedica 10(3):248
Man A, Zhu Y, Zhang Y, Dubreuil M, Rho YH, Peloquin C et al (2013) The risk of cardiovascular disease in systemic sclerosis: a population-based cohort study. Ann Rheum Dis 72(7):1188–93
van Kempen BJ, Spronk S, Koller MT, Elias-Smale SE, Fleischmann KE, Ikram MA et al (2011) Comparative effectiveness and cost-effectiveness of computed tomography screening for coronary artery calcium in asymptomatic individuals. J Am Coll Cardiol 58(16):1690–701
Hecht HS, Cronin P, Blaha MJ, Budoff MJ, Kazerooni EA, Narula J et al (2017) 2016 SCCT/STR guidelines for coronary artery calcium scoring of noncontrast noncardiac chest CT scans: a report of the Society of Cardiovascular Computed Tomography and Society of Thoracic Radiology. J Cardio Computed Tomogr 11(1):74–84
Grundy SM, Stone NJ, Bailey AL, Beam C, Birtcher KK, Blumenthal RS et al (2019) 2018 AHA/ACC/AACVPR/AAPA/ABC/ACPM/ADA/AGS/APhA/ASPC/NLA/PCNA guideline on the management of blood cholesterol: executive summary: a report of the American College of Cardiology/American Heart Association Task Force on Clinical Practice Guidelines. J Am Coll Cardiol 73(24):3168–3209
Kianoush S, Al Rifai M, Cainzos-Achirica M, Al-Mallah MH, Tison GH, Yeboah J et al (2017) Thoracic extra-coronary calcification for the prediction of stroke: the multi-ethnic study of atherosclerosis. Atherosclerosis 1(267):61–67
Tison GH, Guo M, Blaha MJ, McClelland RL, Allison MA, Szklo M et al (2015) Multisite extracoronary calcification indicates increased risk of coronary heart disease and all-cause mortality: the multi-ethnic study of atherosclerosis. J Cardio Computed Tomogr 9(5):406–14
Van Den Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A et al (2013) 2013 classification criteria for systemic sclerosis: an American College of Rheumatology/European League against Rheumatism collaborative initiative. Arthritis Rheum 65(11):2737–2747
Clements PJ, Lachenbruch PA, Seibold JR, Zee B, Steen VD, Brennan P et al (1993) Skin thickness score in systemic sclerosis: an assessment of interobserver variability in 3 independent studies. J Rheumatol 20(11):1892–6
Cappelli S, Randone SB, Camiciottoli G, De Paulis A, Guiducci S, Matucci-Cerinic M (2015) Interstitial lung disease in systemic sclerosis: where do we stand? Eur Respir Rev 24(137):411–9
Cutolo M, Pizzorni C, Sulli A (2004) Nailfold video-capillaroscopy in systemic sclerosis. Zeitschrift fur Rheumatol 63:457–462
LeRoy EC, Black CM, Fleischmajer R, Jablonska S, Krieg T, Medsger TA Jr et al (1988) Scleroderma (systemic sclerosis): classification, subsets and pathogenesis. J Rheumatol 15(2):202–5
Mitchell C, Rahko PS, Blauwet LA, Canaday B, Finstuen JA, Foster MC et al (2019) Guidelines for performing a comprehensive transthoracic echocardiographic examination in adults: recommendations from the American Society of Echocardiography. J Am Soc Echocardiogr 32(1):1–64
Lang RM, Bierig M, Devereux RB, Flachskampf FA, Foster E, Pellikka PA et al (2006) Recommendations for chamber quantification. Eur J Echocardiogr 7(2):79–108
Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M, Detrano R (1990) Quantification of coronary artery calcium using ultrafast computed tomography. J Am Coll Cardiol 15(4):827–32
Gargiulo P, Marsico F, Parente A, Paolillo S, Cecere M, Casaretti L et al (2014) Ischemic heart disease in systemic inflammatory diseases An appraisal. Int J Cardiol 170(3):286–90
Bartoloni E, Shoenfeld Y, Gerli R (2011) Inflammatory and autoimmune mechanisms in the induction of atherosclerotic damage in systemic rheumatic diseases: two faces of the same coin. Arthritis Care Res 63(2):178
Tyndall AJ, Bannert B, Vonk M, Airò P, Cozzi F, Carreira PE et al (2010) Causes and risk factors for death in systemic sclerosis: a study from the EULAR Scleroderma Trials and Research (EUSTAR) database. Ann Rheum Dis 69(10):1809–15
Dave AJ, Fiorentino D, Lingala B, Krishnan E, Chung L (2014) Atherosclerotic cardiovascular disease in hospitalized patients with systemic sclerosis: higher mortality than patients with lupus and rheumatoid arthritis. Arthritis Care Res 66(2):323–327
Panh L, Lairez O, Ruidavets JB, Galinier M, Carrié D, Ferrières J (2017) Coronary artery calcification: From crystal to plaque rupture. Arch Cardiovasc Dis 110(10):550–61
Khurma V, Meyer C, Park GS, Mcmahon M, Lin J, Singh RR et al (2008) A pilot study of subclinical coronary atherosclerosis in systemic sclerosis: coronary artery calcification in cases and controls. Arthritis Care Res 59(4):591–7
Mok MY, Lau CS, Chiu SS, Tso AW, Lo Y, Law LS et al (2011) Systemic sclerosis is an independent risk factor for increased coronary artery calcium deposition. Arthritis Rheum 63(5):1387–1395
Au K, Singh MK, Bodukam V, Bae S, Maranian P, Ogawa R et al (2011) Atherosclerosis in systemic sclerosis: a systematic review and meta-analysis. Arthritis Rheum 63(7):2078–2090
Pagkopoulou E, Poutakidou M, Garyfallos A, Kitas G, Dimitroulas T (2017) Cardiovascular risk in systemic sclerosis: micro-and macro-vascular involvement. Indian J Rheumatol 12(6):211
Iribarren C, Sidney S, Sternfeld B, Browner WS (2000) Calcification of the aortic arch: risk factors and association with coronary heart disease, stroke, and peripheral vascular disease. Jama 283(21):2810–5
Iijima K, Hashimoto H, Hashimoto M, Son BK, Ota H, Ogawa S et al (2010) Aortic arch calcification detectable on chest X-ray is a strong independent predictor of cardiovascular events beyond traditional risk factors. Atherosclerosis 210(1):137–44
Woo JS, Kim W, Kwon SH, Youn HC, Kim HS, Kim JB et al (2016) Aortic arch calcification on chest X-ray combined with coronary calcium score show additional benefit for diagnosis and outcome in patients with angina. J Geriatr Cardiol JGC 13(3):218
Roberts WC (1986) The senile cardiac calcification syndrome. Am J Cardiol 58(6):572–4
Kamenský G, Lisy L, Polak E, Piknova E, Plevova N (2001) Mitral annular calcifications and aortic plaques as predictors of increased cardiovascular mortality. J Cardiol 37:21
Koonce J, Schoepf JU, Nguyen SA, Northam MC, Ravenel JG (2009) Extra-cardiac findings at cardiac CT: experience with 1,764 patients. Eur Radiol 19(3):570–6
Grossman C, Levin M, Koren-Morag N, Bornstein G, Leibowitz A, Ben-Zvi I et al (2018) Left ventricular hypertrophy predicts cardiovascular events in hypertensive patients with coronary artery calcifications. Am J Hypertens 31(3):313–20
Hortells L, Sur S, St HC (2018) Cell phenotype transitions in cardiovascular calcification. Frontiers in cardiovascular medicine 26(5):27
Hortells L, Sosa C, Guillén N, Lucea S, Millán Á, Sorribas V (2017) Identifying early pathogenic events during vascular calcification in uremic rats. Kidney Int 92(6):1384–94
Yehudina Y, Golovach IY (2019) Calcinosis in systemic sclerosis: prevalence, clinical picture, management, complications. PAIN, JOINTS, SPINE. 9(2):108–19
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Naglaa Afifi: conceived the idea and planned the research work, data analysis, and manuscript writing. Maha Khalifa: contributing the design, performed part of investigations, and supervised the finding. Alaa Alah Mohamed verified the analytic methods and reviewed the manuscript. Hend Galal participated in writing the research, performed part of investigations, and supervised the work. All authors discussed the result and contributed to the final manuscript.
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The study conforms to the 1995 Helsinki declaration and is approved by the research ethical committee, Faculty of Medicine, Ain Shams University FWA000017585 (No: FMASU R 13/2020).
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Afifi, N., Khalifa, M.M.M., Al Anany, A.A.M.M.M. et al. Cardiac calcium score in systemic sclerosis. Clin Rheumatol 41, 105–114 (2022). https://doi.org/10.1007/s10067-021-05887-1
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DOI: https://doi.org/10.1007/s10067-021-05887-1