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Review Article| Volume 49, ISSUE 1, P45-66, February 2023

Myocardial Involvement in Systemic Autoimmune Rheumatic Diseases

  • Alexia A. Zagouras
    Affiliations
    Cleveland Clinic Lerner College of Medicine at Case Western Reserve University, , EC-10 Cleveland Clinic, 9501 Euclid Avenue, Cleveland, OH 44195, USA
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  • W.H. Wilson Tang
    Correspondence
    Corresponding author. 9500 Euclid Avenue, Desk J3-4, Cleveland, OH 44195.
    Affiliations
    Cleveland Clinic Lerner College of Medicine at Case Western Reserve University, , EC-10 Cleveland Clinic, 9501 Euclid Avenue, Cleveland, OH 44195, USA

    Kaufman Center for Heart Failure Treatment and Recovery, Heart Vascular and Thoracic Institute, Cleveland Clinic, Cleveland, OH, USA
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      References

        • Mitratza M.
        • Klijs B.
        • Hak A.E.
        • et al.
        Systemic autoimmune disease as a cause of death: mortality burden and comorbidities.
        Rheumatology. 2021; 60: 1321-1330
        • Lee K.S.
        • Kronbichler A.
        • Eisenhut M.
        • et al.
        Cardiovascular involvement in systemic rheumatic diseases: an integrated view for the treating physicians.
        Autoimmun Rev. 2018; 17: 201-214
        • De Lorenzis E.
        • Gremese E.
        • Bosello S.
        • et al.
        Microvascular heart involvement in systemic autoimmune diseases: The purinergic pathway and therapeutic insights from the biology of the diseases.
        Autoimmun Rev. 2019; 18: 317-324
        • Caforio A.L.P.
        • Marcolongo R.
        • Baritussio A.
        • et al.
        Myocarditis in systemic immune-mediated diseases.
        in: Caforio A.L.P. Myocarditis: pathogenesis, diagnosis and treatment. Springer International Publishing, 2020: 195-221https://doi.org/10.1007/978-3-030-35276-9_11
        • Bartoloni E.
        • Shoenfeld Y.
        • Gerli R.
        Inflammatory and autoimmune mechanisms in the induction of atherosclerotic damage in systemic rheumatic diseases: two faces of the same coin.
        Arthritis Care Res (Hoboken). 2011; 63: 178-183
        • Full L.E.
        • Ruisanchez C.
        • Monaco C.
        The inextricable link between atherosclerosis and prototypical inflammatory diseases rheumatoid arthritis and systemic lupus erythematosus.
        Arthritis Res Ther. 2009; 11: 217
        • Ku I.A.
        • Imboden J.B.
        • Hsue P.Y.
        • et al.
        Rheumatoid arthritis: model of systemic inflammation driving atherosclerosis.
        Circ J. 2009; 73: 977-985
        • Prasad M.
        • Hermann J.
        • Gabriel S.E.
        • et al.
        Cardiorheumatology: cardiac involvement in systemic rheumatic disease.
        Nat Rev Cardiol. 2015; 12: 168-176
        • Montecucco F.
        • Mach F.
        Common inflammatory mediators orchestrate pathophysiological processes in rheumatoid arthritis and atherosclerosis.
        Rheumatology (Oxford). 2009; 48: 11-22
        • Breland U.M.
        • Hollan I.
        • Saatvedt K.
        • et al.
        Inflammatory markers in patients with coronary artery disease with and without inflammatory rheumatic disease.
        Rheumatology (Oxford). 2010; 49: 1118-1127
        • Faccini A.
        • Kaski J.C.
        • Camici P.G.
        Coronary microvascular dysfunction in chronic inflammatory rheumatoid diseases.
        Eur Heart J. 2016; 37: 1799-1806
        • Camici P.G.
        • d’Amati G.
        • Rimoldi O.
        Coronary microvascular dysfunction: mechanisms and functional assessment.
        Nat Rev Cardiol. 2015; 12: 48-62
        • Mohammed S.F.
        • Hussain S.
        • Mirzoyev S.A.
        • et al.
        Coronary microvascular rarefaction and myocardial fibrosis in heart failure with preserved ejection fraction.
        Circulation. 2015; 131: 550-559
        • Sorop O.
        • Heinonen I.
        • van Kranenburg M.
        • et al.
        Multiple common comorbidities produce left ventricular diastolic dysfunction associated with coronary microvascular dysfunction, oxidative stress, and myocardial stiffening.
        Cardiovasc Res. 2018; 114: 954-964
        • Zanatta E.
        • Colombo C.
        • D’Amico G.
        • et al.
        Inflammation and coronary microvascular dysfunction in autoimmune rheumatic diseases.
        Int J Mol Sci. 2019; 20: 5563
        • Vaccarino V.
        • Khan D.
        • Votaw J.
        • et al.
        Inflammation is related to coronary flow reserve detected by positron emission tomography in asymptomatic male twins.
        J Am Coll Cardiol. 2011; 57: 1271-1279
        • Yılmaz S.
        • Caliskan M.
        • Kulaksızoglu S.
        • et al.
        Association between serum total antioxidant status and coronary microvascular functions in patients with SLE.
        Echocardiography. 2012; 29: 1218-1223
        • Dinesh P.
        • Rasool M.
        uPA/uPAR signaling in rheumatoid arthritis: Shedding light on its mechanism of action.
        Pharmacol Res. 2018; 134: 31-39
        • Toldi G.
        • Szalay B.
        • Bekő G.
        • et al.
        Plasma soluble urokinase plasminogen activator receptor (suPAR) levels in systemic lupus erythematosus.
        Biomarkers. 2012; 17: 758-763
        • Mekonnen G.
        • Corban M.T.
        • Hung O.Y.
        • et al.
        Plasma soluble urokinase-type plasminogen activator receptor level is independently associated with coronary microvascular function in patients with non-obstructive coronary artery disease.
        Atherosclerosis. 2015; 239: 55-60
        • Cutolo M.
        • Soldano S.
        • Smith V.
        Pathophysiology of systemic sclerosis: current understanding and new insights.
        Expert Rev Clin Immunol. 2019; 15: 753-764
        • Maurer B.
        • Distler J.H.W.
        • Distler O.
        The Fra-2 transgenic mouse model of systemic sclerosis.
        Vasc Pharmacol. 2013; 58: 194-201
        • Venalis P.
        • Kumánovics G.
        • Schulze-Koops H.
        • et al.
        Cardiomyopathy in murine models of systemic sclerosis.
        Arthritis Rheumatol. 2015; 67: 508-516
        • Maurer B.
        • Busch N.
        • Jüngel A.
        • et al.
        Transcription factor fos-related antigen-2 induces progressive peripheral vasculopathy in mice closely resembling human systemic sclerosis.
        Circulation. 2009; 120: 2367-2376
        • Giacomo R.
        • Sheon M.
        • Christine M.
        • et al.
        Reduced lymphatic reserve in heart failure with preserved ejection fraction.
        J Am Coll Cardiol. 2020; 76: 2817-2829
        • Schwartz N.
        • Chalasani M.L.S.
        • Li T.M.
        • et al.
        Lymphatic function in autoimmune diseases.
        Front Immunol. 2019; 10: 519
        • Rossi A.
        • Sozio F.
        • Sestini P.
        • et al.
        Lymphatic and blood vessels in scleroderma skin, a morphometric analysis.
        Hum Pathol. 2010; 41: 366-374
        • Bouta E.M.
        • Bell R.D.
        • Rahimi H.
        • et al.
        Targeting lymphatic function as a novel therapeutic intervention for rheumatoid arthritis.
        Nat Rev Rheumatol. 2018; 14: 94-106
        • Bracamonte-Baran W.
        • Čiháková D.
        Cardiac autoimmunity: myocarditis.
        Adv Exp Med Biol. 2017; 1003: 187-221
        • Ryabkova V.A.
        • Shubik Y.V.
        • Erman M.V.
        • et al.
        Lethal immunoglobulins: autoantibodies and sudden cardiac death.
        Autoimmun Rev. 2019; 18: 415-425
        • Myers J.M.
        • Fairweather D.
        • Huber S.A.
        • et al.
        Autoimmune myocarditis, valvulitis, and cardiomyopathy.
        Curr Protoc Immunol. 2013; (Chapter 15:Unit 15.14): 1-51
        • Nagatomo Y.
        • Tang W.H.W.
        Autoantibodies and cardiovascular dysfunction: cause or consequence?.
        Curr Heart Fail Rep. 2014; 11: 500-508
        • Li Y.
        • Heuser J.S.
        • Kosanke S.D.
        • et al.
        Cryptic epitope identified in rat and human cardiac myosin S2 region induces myocarditis in the Lewis rat.
        J Immunol. 2004; 172: 3225-3234
        • Mascaro-Blanco A.
        • Alvarez K.
        • Yu X.
        • et al.
        Consequences of unlocking the cardiac myosin molecule in human myocarditis and cardiomyopathies.
        Autoimmunity. 2008; 41: 442-453
        • Myers J.M.
        • Cooper L.T.
        • Kem D.C.
        • et al.
        Cardiac myosin-Th17 responses promote heart failure in human myocarditis.
        JCI Insight. 2016; 1: 85851
        • Düngen H.-D.
        • Dordevic A.
        • Felix S.B.
        • et al.
        β1-adrenoreceptor autoantibodies in heart failure: physiology and therapeutic implications.
        Circ Heart Fail. 2020; 13: e006155
        • Nagatomo Y.
        • Li D.
        • Kirsop J.
        • et al.
        Autoantibodies specifically against β1 adrenergic receptors and adverse clinical outcome in patients with chronic systolic heart failure in the β-blocker era: the importance of immunoglobulin G3 subclass.
        J Card Fail. 2016; 22: 417-422
        • Kill A.
        • Tabeling C.
        • Undeutsch R.
        • et al.
        Autoantibodies to angiotensin and endothelin receptors in systemic sclerosis induce cellular and systemic events associated with disease pathogenesis.
        Arthritis Res Ther. 2014; 16: R29
        • Kiriakidou M.
        • Ching C.L.
        Systemic lupus erythematosus.
        Ann Intern Med. 2020; 172: ITC81-ITC96
        • Durcan L.
        • O’Dwyer T.
        • Petri M.
        Management strategies and future directions for systemic lupus erythematosus in adults.
        Lancet. 2019; 393: 2332-2343
        • Miner J.J.
        • Kim A.H.J.
        Cardiac manifestations of systemic lupus erythematosus.
        Rheum Dis Clin North Am. 2014; 40: 51-60
        • Thomas G.
        • Cohen Aubart F.
        • Chiche L.
        • et al.
        Lupus Myocarditis: Initial Presentation and Longterm Outcomes in a Multicentric Series of 29 Patients.
        J Rheumatol. 2017; 44: 24-32
        • Bulkley B.H.
        • Roberts W.C.
        The heart in systemic lupus erythematosus and the changes induced in it by corticosteroid therapy. A study of 36 necropsy patients.
        Am J Med. 1975; 58: 243-264
        • Mavrogeni S.
        • Bratis K.
        • Markussis V.
        • et al.
        The diagnostic role of cardiac magnetic resonance imaging in detecting myocardial inflammation in systemic lupus erythematosus. Differentiation from viral myocarditis.
        Lupus. 2013; 22: 34-43
        • Jain D.
        • Halushka M.K.
        Cardiac pathology of systemic lupus erythematosus.
        J Clin Pathol. 2009; 62: 584-592
        • Prasada S.
        • Rivera A.
        • Nishtala A.
        • et al.
        Differential associations of chronic inflammatory diseases with incident heart failure.
        JACC: Heart Fail. 2020; 8: 489-498
        • Chen J.
        • Tang Y.
        • Zhu M.
        • et al.
        Heart involvement in systemic lupus erythematosus: a systemic review and meta-analysis.
        Clin Rheumatol. 2016; 35: 2437-2448
        • Leone P.
        • Cicco S.
        • Prete M.
        • et al.
        Early echocardiographic detection of left ventricular diastolic dysfunction in patients with systemic lupus erythematosus asymptomatic for cardiovascular disease.
        Clin Exp Med. 2020; 20: 11-19
        • Roldan C.A.
        • Alomari I.B.
        • Awad K.
        • et al.
        Aortic stiffness is associated with left ventricular diastolic dysfunction in systemic lupus erythematosus: a controlled transesophageal echocardiographic study.
        Clin Cardiol. 2014; 37: 83-90
        • Seneviratne M.G.
        • Grieve S.M.
        • Figtree G.A.
        • et al.
        Prevalence, distribution and clinical correlates of myocardial fibrosis in systemic lupus erythematosus: a cardiac magnetic resonance study.
        Lupus. 2016; 25: 573-581
        • Shang Q.
        • Yip G.W.K.
        • Tam L.S.
        • et al.
        SLICC/ACR damage index independently associated with left ventricular diastolic dysfunction in patients with systemic lupus erythematosus.
        Lupus. 2012; 21: 1057-1062
        • Chorin E.
        • Hochstadt A.
        • Arad U.
        • et al.
        Soluble ST2 and CXCL-10 may serve as biomarkers of subclinical diastolic dysfunction in SLE and correlate with disease activity and damage.
        Lupus. 2020; 29: 1430-1437
        • Dhakal B.P.
        • Kim C.H.
        • Al-Kindi S.G.
        • et al.
        Heart failure in systemic lupus erythematosus.
        Trends Cardiovasc Med. 2018; 28: 187-197
        • Wainwright B.
        • Bhan R.
        • Trad C.
        • et al.
        Autoimmune-mediated congenital heart block.
        Best Pract Res Clin Obstet Gynaecol. 2020; 64: 41-51
        • Scott J.S.
        • Maddison P.J.
        • Taylor P.V.
        • et al.
        Connective-tissue disease, antibodies to ribonucleoprotein, and congenital heart block.
        N Engl J Med. 1983; 309: 209-212
        • Jayaprasad N.
        • Johnson F.
        • Venugopal K.
        Congenital complete heart block and maternal connective tissue disease.
        Int J Cardiol. 2006; 112: 153-158
        • Moak J.P.
        • Barron K.S.
        • Hougen T.J.
        • et al.
        Congenital heart block: development of late-onset cardiomyopathy, a previously underappreciated sequela.
        J Am Coll Cardiol. 2001; 37: 238-242
        • Izmirly P.
        • Kim M.
        • Friedman D.M.
        • et al.
        Hydroxychloroquine to prevent recurrent congenital heart block in fetuses of Anti-SSA/Ro-positive mothers.
        J Am Coll Cardiol. 2020; 76: 292-302
        • McInnes I.B.
        • Schett G.
        The pathogenesis of rheumatoid arthritis.
        N Engl J Med. 2011; 365: 2205-2219
        • Solomon D.H.
        • Karlson E.W.
        • Rimm E.B.
        • et al.
        Cardiovascular morbidity and mortality in women diagnosed with rheumatoid arthritis.
        Circulation. 2003; 107: 1303-1307
        • Gabriel S.E.
        Cardiovascular morbidity and mortality in rheumatoid arthritis.
        Am J Med. 2008; 121: S9-S14
        • Elbadawi A.
        • Ahmed H.M.A.
        • Elgendy I.Y.
        • et al.
        Outcomes of acute myocardial infarction in patients with rheumatoid arthritis.
        Am J Med. 2020; 133: 1168-1179.e4
        • Nicola P.J.
        • Maradit-Kremers H.
        • Roger V.L.
        • et al.
        The risk of congestive heart failure in rheumatoid arthritis: a population-based study over 46 years.
        Arthritis Rheum. 2005; 52: 412-420
        • Lebowitz W.B.
        The heart in rheumatoid arthritis (rheumatoid disease). A clinical and pathological study of sixty-two cases.
        Ann Intern Med. 1963; 58: 102-123
        • Pappas D.A.
        • Taube J.M.
        • Bathon J.M.
        • et al.
        A 73-year-old woman with rheumatoid arthritis and shortness of breath.
        Arthritis Rheum. 2008; 59: 892-899
        • Ntusi N.A.B.
        • Piechnik S.K.
        • Francis J.M.
        • et al.
        Diffuse myocardial fibrosis and inflammation in rheumatoid arthritis: insights from CMR T1 mapping.
        JACC Cardiovasc Imaging. 2015; 8: 526-536
        • Greulich S.
        • Mayr A.
        • Kitterer D.
        • et al.
        Advanced myocardial tissue characterisation by a multi-component CMR protocol in patients with rheumatoid arthritis.
        Eur Radiol. 2017; 27: 4639-4649
        • Denton C.P.
        • Khanna D.
        Systemic sclerosis.
        The Lancet. 2017; 390: 1685-1699
        • Bissell L.-A.
        • Md Yusof MY
        • Buch M.H.
        Primary myocardial disease in scleroderma-a comprehensive review of the literature to inform the UK Systemic Sclerosis Study Group cardiac working group.
        Rheumatology (Oxford). 2017; 56: 882-895
        • Chatterjee S.
        Pulmonary hypertension in systemic sclerosis.
        Semin Arthritis Rheum. 2011; 41: 19-37
        • Launay D.
        • Sobanski V.
        • Hachulla E.
        • et al.
        Pulmonary hypertension in systemic sclerosis: different phenotypes.
        Eur Respir Rev. 2017; 26https://doi.org/10.1183/16000617.0056-2017
        • Fox B.D.
        • Shimony A.
        • Langleben D.
        • et al.
        High prevalence of occult left heart disease in scleroderma-pulmonary hypertension.
        Eur Respir J. 2013; 42: 1083-1091
        • Bourji K.I.
        • Kelemen B.W.
        • Mathai S.C.
        • et al.
        Poor survival in patients with scleroderma and pulmonary hypertension due to heart failure with preserved ejection fraction.
        Pulm Circ. 2017; 7: 409-420
        • Rubio-Rivas M.
        • Corbella X.
        • Guillén-Del-Castillo A.
        • et al.
        Spanish scleroderma risk score (RESCLESCORE) to predict 15-year all-cause mortality in scleroderma patients at the time of diagnosis based on the RESCLE cohort: derivation and internal validation.
        Autoimmun Rev. 2020; 19: 102507
        • Ciurzyński M.
        • Bienias P.
        • Lichodziejewska B.
        • et al.
        Assessment of left and right ventricular diastolic function in patients with systemic sclerosis.
        Kardiol Pol. 2008; 66 ([discussion: 277-278]): 269-276
        • Tennøe A.H.
        • Murbræch K.
        • Andreassen J.C.
        • et al.
        Left ventricular diastolic dysfunction predicts mortality in patients with systemic sclerosis.
        J Am Coll Cardiol. 2018; 72: 1804-1813
        • Sulli A.
        • Ghio M.
        • Bezante G.P.
        • et al.
        Blunted coronary flow reserve in systemic sclerosis.
        Rheumatology (Oxford). 2004; 43: 505-509
        • Valentini G.
        • Vitale D.F.
        • Giunta A.
        • et al.
        Diastolic abnormalities in systemic sclerosis: evidence for associated defective cardiac functional reserve.
        Ann Rheum Dis. 1996; 55: 455-460
        • Zanatta E.
        • Famoso G.
        • Boscain F.
        • et al.
        Nailfold avascular score and coronary microvascular dysfunction in systemic sclerosis: a newsworthy association.
        Autoimmun Rev. 2019; 18: 177-183
        • Mukherjee M.
        • Chung S.-E.
        • Ton V.K.
        • et al.
        Unique Abnormalities in right ventricular longitudinal strain in systemic sclerosis patients.
        Circ Cardiovasc Imaging. 2016; 9https://doi.org/10.1161/CIRCIMAGING.115.003792
        • Yiu K.H.
        • Schouffoer A.A.
        • Marsan N.A.
        • et al.
        Left ventricular dysfunction assessed by speckle-tracking strain analysis in patients with systemic sclerosis: relationship to functional capacity and ventricular arrhythmias.
        Arthritis Rheum. 2011; 63: 3969-3978
        • Rodríguez-Reyna T.S.
        • Morelos-Guzman M.
        • Hernández-Reyes P.
        • et al.
        Assessment of myocardial fibrosis and microvascular damage in systemic sclerosis by magnetic resonance imaging and coronary angiotomography.
        Rheumatology (Oxford). 2015; 54: 647-654
        • Mavrogeni S.
        • Koutsogeorgopoulou L.
        • Karabela G.
        • et al.
        Silent myocarditis in systemic sclerosis detected by cardiovascular magnetic resonance using Lake Louise criteria.
        BMC Cardiovasc Disord. 2017; 17: 187
        • Mohameden M.
        • Vashisht P.
        • Sharman T.
        Scleroderma and primary myocardial disease.
        in: StatPearls. StatPearls Publishing, 2020 (Available at:) (Accessed July 22, 2020)
        • Allanore Y.
        • Meune C.
        Primary myocardial involvement in systemic sclerosis: evidence for a microvascular origin.
        Clin Exp Rheumatol. 2010; 28: S48-S53
        • West S.G.
        • Killian P.J.
        • Lawless O.J.
        Association of myositis and myocarditis in progressive systemic sclerosis.
        Arthritis Rheum. 1981; 24: 662-668
        • De Luca G.
        • Campochiaro C.
        • De Santis M.
        • et al.
        Systemic sclerosis myocarditis has unique clinical, histological and prognostic features: a comparative histological analysis.
        Rheumatology (Oxford). 2020; https://doi.org/10.1093/rheumatology/kez658
        • Hesselstrand R.
        • Scheja A.
        • Shen G.Q.
        • et al.
        The association of antinuclear antibodies with organ involvement and survival in systemic sclerosis.
        Rheumatology (Oxford). 2003; 42: 534-540
        • Machado C.
        • Sunkel C.E.
        • Andrew D.J.
        Human autoantibodies reveal titin as a chromosomal protein.
        J Cell Biol. 1998; 141: 321-333
        • Riemekasten G.
        • Philippe A.
        • Näther M.
        • et al.
        Involvement of functional autoantibodies against vascular receptors in systemic sclerosis.
        Ann Rheum Dis. 2011; 70: 530-536
        • Manetti M.
        • Milia A.F.
        • Guiducci S.
        • et al.
        Progressive loss of lymphatic vessels in skin of patients with systemic sclerosis.
        J Rheumatol. 2011; 38: 297-301
        • Furuta S.
        • Iwamoto T.
        • Nakajima H.
        Update on eosinophilic granulomatosis with polyangiitis.
        Allergol Int. 2019; 68: 430-436
        • Miloslavsky E.
        • Unizony S.
        The heart in vasculitis.
        Rheum Dis Clin North Am. 2014; 40: 11-26
        • Chang H.-C.
        • Chou P.-C.
        • Lai C.-Y.
        • et al.
        Antineutrophil cytoplasmic antibodies and organ-specific manifestations in eosinophilic granulomatosis with polyangiitis: a systematic review and meta-analysis.
        J Allergy Clin Immunol Pract. 2021; 9: 445-452.e6
        • Dalia T.
        • Parashar S.
        • Patel N.V.
        • et al.
        Eosinophilic myocarditis demonstrated using cardiac magnetic resonance imaging in a patient with eosinophilic granulomatosis with polyangiitis (churg-strauss disease).
        Cureus. 2018; 10: e2792
        • Comarmond C.
        • Pagnoux C.
        • Khellaf M.
        • et al.
        Eosinophilic granulomatosis with polyangiitis (Churg-Strauss): clinical characteristics and long-term followup of the 383 patients enrolled in the French Vasculitis Study Group cohort.
        Arthritis Rheum. 2013; 65: 270-281
        • Szczeklik W.
        • Miszalski-Jamka T.
        Cardiac involvement in eosinophilic granulomatosis with polyangitis (Churg Strauss) (RCD code: I-3A.7a).
        J Rare Cardiovasc Dis. 2014; 1: 91-95
        • Dennert R.M.
        • van Paassen P.
        • Schalla S.
        • et al.
        Cardiac involvement in Churg-Strauss syndrome.
        Arthritis Rheum. 2010; 62: 627-634
        • Brucato A.
        • Maestroni S.
        • Masciocco G.
        • et al.
        [Cardiac involvement in Churg-Strauss syndrome].
        G Ital Cardiol (Rome). 2015; 16: 493-500
        • Moosig F.
        • Bremer J.P.
        • Hellmich B.
        • et al.
        A vasculitis centre based management strategy leads to improved outcome in eosinophilic granulomatosis and polyangiitis (Churg-Strauss, EGPA): monocentric experiences in 150 patients.
        Ann Rheum Dis. 2013; 72: 1011-1017
        • Steinfeld J.
        • Bradford E.S.
        • Brown J.
        • et al.
        Evaluation of clinical benefit from treatment with mepolizumab for patients with eosinophilic granulomatosis with polyangiitis.
        J Allergy Clin Immunol. 2019; 143: 2170-2177
        • Jennette J.C.
        • Falk R.J.
        • Bacon P.A.
        • et al.
        2012 Revised international chapel hill consensus conference nomenclature of vasculitides.
        Arthritis Rheum. 2013; 65: 1-11
        • McGeoch L.
        • Carette S.
        • Cuthbertson D.
        • et al.
        Cardiac involvement in granulomatosis with polyangiitis.
        J Rheumatol. 2015; 42: 1209-1212
        • Guillevin L.
        • Pagnoux C.
        • Seror R.
        • et al.
        The Five-Factor Score revisited: assessment of prognoses of systemic necrotizing vasculitides based on the French Vasculitis Study Group (FVSG) cohort.
        Medicine (Baltimore). 2011; 90: 19-27
        • Walsh M.
        • Flossmann O.
        • Berden A.
        • et al.
        Risk factors for relapse of antineutrophil cytoplasmic antibody-associated vasculitis.
        Arthritis Rheum. 2012; 64: 542-548
        • Hanna R.M.
        • Lopez E.
        • Wilson J.
        Granulomatosis with polyangiitis with myocarditis and ventricular tachycardia.
        Case Rep Med. 2017; 2017: 6501738
        • Munch A.
        • Sundbøll J.
        • Høyer S.
        • et al.
        Acute myocarditis in a patient with newly diagnosed granulomatosis with polyangiitis.
        Case Rep Cardiol. 2015; 2015: 134529
        • Guillevin L.
        • Pagnoux C.
        • Karras A.
        • et al.
        Rituximab versus azathioprine for maintenance in ANCA-associated vasculitis.
        N Engl J Med. 2014; 371: 1771-1780
        • Oliveira G.H.M.
        • Seward J.B.
        • Tsang T.S.M.
        • et al.
        Echocardiographic findings in patients with wegener granulomatosis.
        Mayo Clinic Proc. 2005; 80: 1435-1440
        • Luciano N.
        • Valentini V.
        • Calabrò A.
        • et al.
        One year in review 2015: Sjögren’s syndrome.
        Clin Exp Rheumatol. 2015; 33: 259-271
        • Chiang C.-H.
        • Liu C.-J.
        • Chen P.-J.
        • et al.
        Primary sjögren’s syndrome and the risk of acute myocardial infarction: a nationwide study.
        Acta Cardiol Sin. 2013; 29: 124-131
        • Bartoloni E.
        • Baldini C.
        • Schillaci G.
        • et al.
        Cardiovascular disease risk burden in primary Sjögren’s syndrome: results of a population-based multicentre cohort study.
        J Intern Med. 2015; 278: 185-192
        • Gyöngyösi M.
        • Pokorny G.
        • Jambrik Z.
        • et al.
        Cardiac manifestations in primary Sjögren’s syndrome.
        Ann Rheum Dis. 1996; 55: 450-454
        • Vassiliou V.A.
        • Moyssakis I.
        • Boki K.A.
        • et al.
        Is the heart affected in primary Sjögren’s syndrome? An echocardiographic study.
        Clin Exp Rheumatol. 2008; 26: 109-112
        • Bayram N.A.
        • Cicek O.F.
        • Erten S.
        • et al.
        Assessment of left ventricular functions in patients with Sjögren’s syndrome using tissue Doppler echocardiography.
        Int J Rheum Dis. 2013; 16: 425-429
        • Levin M.D.
        • Zoet-Nugteren S.K.
        • Markusse H.M.
        Myocarditis and primary Sjögren’s syndrome.
        Lancet. 1999; 354: 128-129
        • Kau C.-K.
        • Hu J.-C.
        • Lu L.-Y.
        • et al.
        Primary Sjögren’s syndrome complicated with cryoglobulinemic glomerulonephritis, myocarditis, and multi-organ involvement.
        J Formos Med Assoc. 2004; 103: 707-710
        • Brito-Zerón P.
        • Pasoto S.G.
        • Robles-Marhuenda A.
        • et al.
        Autoimmune congenital heart block and primary Sjögren’s syndrome: characterisation and outcomes of 49 cases.
        Clin Exp Rheumatol. 2020; 38 (4): 95-102
        • Caforio A.L.P.
        • Adler Y.
        • Agostini C.
        • et al.
        Diagnosis and management of myocardial involvement in systemic immune-mediated diseases: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Disease.
        Eur Heart J. 2017; 38: 2649-2662
        • Hamzeh N.
        • Steckman D.A.
        • Sauer W.H.
        • et al.
        Pathophysiology and clinical management of cardiac sarcoidosis.
        Nat Rev Cardiol. 2015; 12: 278-288
        • Iwai K.
        • Takemura T.
        • Kitaichi M.
        • et al.
        Pathological studies on sarcoidosis autopsy. II. Early change, mode of progression and death pattern.
        Acta Pathol Jpn. 1993; 43: 377-385
        • Perry A.
        • Vuitch F.
        Causes of death in patients with sarcoidosis. A morphologic study of 38 autopsies with clinicopathologic correlations.
        Arch Pathol Lab Med. 1995; 119: 167-172
        • Baughman R.P.
        • Teirstein A.S.
        • Judson M.A.
        • et al.
        Clinical characteristics of patients in a case control study of sarcoidosis.
        Am J Respir Crit Care Med. 2001; 164: 1885-1889
        • Iwai K.
        • Sekiguti M.
        • Hosoda Y.
        • et al.
        Racial difference in cardiac sarcoidosis incidence observed at autopsy.
        Sarcoidosis. 1994; 11: 26-31
        • Kusano K.F.
        • Satomi K.
        Diagnosis and treatment of cardiac sarcoidosis.
        Heart. 2016; 102: 184-190
        • Uusimaa P.
        • Ylitalo K.
        • Anttonen O.
        • et al.
        Ventricular tachyarrhythmia as a primary presentation of sarcoidosis.
        Europace. 2008; 10: 760-766
        • Koplan B.A.
        • Soejima K.
        • Baughman K.
        • et al.
        Refractory ventricular tachycardia secondary to cardiac sarcoid: Electrophysiologic characteristics, mapping, and ablation.
        Heart Rhythm. 2006; 3: 924-929
        • Zhu T.Y.
        • Li E.K.
        • Tam L.-S.
        Cardiovascular risk in patients with psoriatic arthritis.
        Int J Rheumatol. 2012; 2012
        • Wong K.
        • Gladman D.D.
        • Husted J.
        • et al.
        Mortality studies in psoriatic arthritis: results from a single outpatient clinic. I. Causes and risk of death.
        Arthritis Rheum. 1997; 40: 1868-1872
        • Buckley C.
        • Cavill C.
        • Taylor G.
        • et al.
        Mortality in psoriatic arthritis – a single-center study from the UK.
        J Rheumatol. 2010; 37: 2141-2144
        • Liew J.W.
        • Ramiro S.
        • Gensler L.S.
        Cardiovascular morbidity and mortality in ankylosing spondylitis and psoriatic arthritis.
        Best Pract Res Clin Rheumatol. 2018; 32: 369-389
        • Haroon N.N.
        • Paterson J.M.
        • Li P.
        • et al.
        Patients with ankylosing spondylitis have increased cardiovascular and cerebrovascular mortality.
        Ann Intern Med. 2015; 163: 409-416
        • Husted J.A.
        • Thavaneswaran A.
        • Chandran V.
        • et al.
        Cardiovascular and other comorbidities in patients with psoriatic arthritis: a comparison with patients with psoriasis.
        Arthritis Care Res (Hoboken). 2011; 63: 1729-1735
        • Atluri R.B.
        Inflammatory myopathies.
        Mo Med. 2016; 113: 127-130
        • Zhang L.
        • Wang G.
        • Ma L.
        • et al.
        Cardiac involvement in adult polymyositis or dermatomyositis: a systematic review.
        Clin Cardiol. 2012; 35: 686-691
        • Gonzalez-Lopez L.
        • Gamez-Nava J.I.
        • Sanchez L.
        • et al.
        Cardiac manifestations in dermato-polymyositis.
        Clin Exp Rheumatol. 1996; 14: 373-379
        • Allanore Y.
        • Vignaux O.
        • Arnaud L.
        • et al.
        Effects of corticosteroids and immunosuppressors on idiopathic inflammatory myopathy related myocarditis evaluated by magnetic resonance imaging.
        Ann Rheum Dis. 2006; 65: 249-252
        • Garg V.
        • Tan W.
        • Ardehali R.
        • et al.
        Giant cell myocarditis masquerading as orbital myositis with a rapid, fulminant course necessitating mechanical support and heart transplantation.
        ESC Heart Fail. 2017; 4: 371-375
        • Dalakas M.C.
        Inflammatory muscle diseases.
        N Engl J Med. 2015; 372: 1734-1747
        • Dankó K.
        • Ponyi A.
        • Constantin T.
        • et al.
        Long-term survival of patients with idiopathic inflammatory myopathies according to clinical features: a longitudinal study of 162 cases.
        Medicine (Baltimore). 2004; 83: 35-42
        • Schrezenmeier E.
        • Dörner T.
        Mechanisms of action of hydroxychloroquine and chloroquine: implications for rheumatology.
        Nat Rev Rheumatol. 2020; 16: 155-166
        • Chatre C.
        • Roubille F.
        • Vernhet H.
        • et al.
        Cardiac complications attributed to chloroquine and hydroxychloroquine: a systematic review of the literature.
        Drug Saf. 2018; 41: 919-931
        • Nadeem U.
        • Raafey M.
        • Kim G.
        • et al.
        Chloroquine- and hydroxychloroquine-induced cardiomyopathy: a case report and brief literature review.
        Am J Clin Pathol. 2021; 155: 793-801
        • Jang D.-I.
        • Lee A.-H.
        • Shin H.-Y.
        • et al.
        The role of tumor necrosis factor alpha (TNF-α) in autoimmune disease and current TNF-α inhibitors in therapeutics.
        Int J Mol Sci. 2021; 22: 2719
        • Chung E.S.
        • Packer M.
        • Lo K.H.
        • et al.
        Anti-TNF Therapy Against Congestive Heart Failure Investigators. Randomized, double-blind, placebo-controlled, pilot trial of infliximab, a chimeric monoclonal antibody to tumor necrosis factor-alpha, in patients with moderate-to-severe heart failure: results of the anti-TNF Therapy Against Congestive Heart Failure (ATTACH) trial.
        Circulation. 2003; 107: 3133-3140
        • Sinagra E.
        • Perricone G.
        • Romano C.
        • et al.
        Heart failure and anti tumor necrosis factor-alpha in systemic chronic inflammatory diseases.
        Eur J Intern Med. 2013; 24: 385-392
        • Coletta A.P.
        • Clark A.L.
        • Banarjee P.
        • et al.
        Clinical trials update: RENEWAL (RENAISSANCE and RECOVER) and ATTACH.
        Eur J Heart Fail. 2002; 4: 559-561
        • Iqubal A.
        • Iqubal M.K.
        • Sharma S.
        • et al.
        Molecular mechanism involved in cyclophosphamide-induced cardiotoxicity: Old drug with a new vision.
        Life Sci. 2019; 218: 112-131
        • Kurauchi K.
        • Nishikawa T.
        • Miyahara E.
        • et al.
        Role of metabolites of cyclophosphamide in cardiotoxicity.
        BMC Res Notes. 2017; 10: 406
        • Higgins A.Y.
        • O’Halloran T.D.
        • Chang J.D.
        Chemotherapy-induced cardiomyopathy.
        Heart Fail Rev. 2015; 20: 721-730
        • Caforio A.L.P.
        • Pankuweit S.
        • Arbustini E.
        • et al.
        Current state of knowledge on aetiology, diagnosis, management, and therapy of myocarditis: a position statement of the European Society of Cardiology Working Group on Myocardial and Pericardial Diseases.
        Eur Heart J. 2013; 34 (2648a-2648d): 2636-2648
        • Bissell L.-A.
        • Anderson M.
        • Burgess M.
        • et al.
        Consensus best practice pathway of the UK Systemic Sclerosis Study group: management of cardiac disease in systemic sclerosis.
        Rheumatology (Oxford). 2017; 56: 912-921
        • Hamzeh N.Y.
        • Wamboldt F.S.
        • Weinberger H.D.
        Management of cardiac sarcoidosis in the United States: a Delphi study.
        Chest. 2012; 141: 154-162
        • Baker M.C.
        • Sheth K.
        • Witteles R.
        • et al.
        TNF-alpha inhibition for the treatment of cardiac sarcoidosis.
        Semin Arthritis Rheum. 2020; 50: 546-552