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Current Vascular Pharmacology


ISSN (Print): 1570-1611
ISSN (Online): 1875-6212

Review Article

Primary Sjögren’s Syndrome and Cardiovascular Disease

Author(s): Konstantinos Melissaropoulos*, Dimitrios Bogdanos, Theodoros Dimitroulas, Lazaros I. Sakkas, George D. Kitas and Dimitrios Daoussis

Volume 18, Issue 5, 2020

Page: [447 - 454] Pages: 8

DOI: 10.2174/1570161118666200129125320

Price: $65


Sjögren’s syndrome is a rheumatic autoimmune disease that primarily affects middle-aged women and runs a slowly progressing course with sicca symptoms being the prevalent manifestation. Premature atherosclerosis and increased cardiovascular (CV) morbidity and mortality are frequently encountered in rheumatic diseases characterized by significant systemic inflammation, such as the inflammatory arthritides, systemic vasculitides and systemic lupus erythematosus. In the same context, chronic inflammation and immune aberrations underlying Sjögren’s syndrome are also reported to be associated with augmented risk of atherosclerosis. Increased CV disease (CVD) frequency has been found in recent meta-analyses. The involvement of the CV system is not a common feature of Sjögren’s syndrome; however, specific manifestations, such as autoantibody-mediated heart block, pericarditis, pulmonary arterial hypertension and dysautonomia, have been described. This review focuses on studies addressing CV morbidity in Sjögren’s syndrome and presents current data regarding distinct CV features of the disease.

Keywords: Sjögren's syndrome, cardiovascular morbidity, atherosclerosis, echocardiography, anti-Ro antibodies, heart block, dysautonomia.

Graphical Abstract
Brito-Zerón P, Baldini C, Bootsma H, et al. Sjögren syndrome. Nat Rev Dis Primers 2016; 2: 16047.
[] [PMID: 27383445]
Ioannidis JPA, Vassiliou VA, Moutsopoulos HM. Long-term risk of mortality and lymphoproliferative disease and predictive classifica-tion of primary Sjögren’s syndrome. Arthritis Rheum 2002; 46(3): 741-7.
[] [PMID: 11920410]
Voulgarelis M, Tzioufas AG, Moutsopoulos HM. Mortality in Sjögren’s syndrome. Clin Exp Rheumatol 2008; 26(5)(Suppl. 51): S66-71.
[PMID: 19026146]
Liang Y, Yang Z, Qin B, Zhong R. Primary Sjogren’s syndrome and malignancy risk: a systematic review and meta-analysis. Ann Rheum Dis 2014; 73(6): 1151-6.
[] [PMID: 23687261]
Moutsopoulos HM. Sjögren’s syndrome: autoimmune epithelitis. Clin Immunol Immunopathol 1994; 72(2): 162-5.
[] [PMID: 8050187]
Goules AV, Kapsogeorgou EK, Tzioufas AG. Insight into pathogenesis of Sjögren’s syndrome: Dissection on autoimmune infiltrates and epithelial cells. Clin Immunol 2017; 182: 30-40.
[] [PMID: 28330683]
Tzioufas AG, Tatouli IP, Moutsopoulos HM. Autoantibodies in Sjögren’s syndrome: clinical presentation and regulatory mechanisms. Presse Med 2012; 41(9 Pt 2): e451-60.
[] [PMID: 22840991]
Mavragani CP, Moutsopoulos HM. The geoepidemiology of Sjögren’s syndrome. Autoimmun Rev 2010; 9(5): A305-10.
[] [PMID: 19903539]
Shiboski CH, Shiboski SC, Seror R, et al. 2016 American college of rheumatology/european league against rheumatism classification criteria for primary sjögren’s syndrome: a consensus and data-driven methodology involving three international patient cohorts. Arthritis Rheumatol 2017; 69(1): 35-45.
[] [PMID: 27785888]
Vitali C, Bombardieri S, Jonsson R, et al. Classification criteria for Sjögren’s syndrome: a revised version of the European criteria pro-posed by the American-European consensus group. Ann Rheum Dis 2002; 61(6): 554-8.
[] [PMID: 12006334]
Bartoloni E, Alunno A, Valentini V, et al. Targeting inflammation to prevent cardiovascular disease in chronic rheumatic diseases: myth or reality? Front Cardiovasc Med 2018; 5: 177.
[] [PMID: 30619884]
Ramos-Casals M, Brito-Zerón P, Sisó-Almirall A, Bosch X, Tzioufas AG. Topical and systemic medications for the treatment of primary Sjögren’s syndrome. Nat Rev Rheumatol 2012; 8(7): 399-411.
[] [PMID: 22549247]
Giannelou M, Mavragani CP. Cardiovascular disease in systemic lupus erythematosus: a comprehensive update. J Autoimmun 2017; 82: 1-12.
[] [PMID: 28606749]
Nurmohamed MT, Heslinga M, Kitas GD. Cardiovascular comorbidity in rheumatic diseases. Nat Rev Rheumatol 2015; 11(12): 693-704.
[] [PMID: 26282082]
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(2): 178-83.
[] [PMID: 20740611]
Crowson CS, Gabriel SE, Semb AG, et al. Trans-atlantic cardiovascular consortium for rheumatoid arthritis. Rheumatoid arthritis-specific cardiovascular risk scores are not superior to general risk scores: a validation analysis of patients from seven countries. Rheumatology (Oxford) 2017; 56(7): 1102-10.
[] [PMID: 28339992]
Edwards N, Langford-Smith AWW, Parker BJ, et al. QRISK3 improves detection of cardiovascular disease risk in patients with systemic lupus erythematosus. Lupus Sci Med 2018; 5(1)e000272
[] [PMID: 30167314]
Khanna NN, Jamthikar AD, Gupta D, et al. Rheumatoid arthritis: atherosclerosis imaging and cardiovascular risk assessment using machine and deep learning-based tissue characterization. Curr Atheroscler Rep 2019; 21(2): 7.
[] [PMID: 30684090]
Pego-Reigosa JM, Restrepo Vélez J, Baldini C, et al. Comorbidities (excluding lymphoma) in Sjögren’s syndrome. Rheumatol Oxf Engl 2019.
[] [PMID: 30770715]
Valim V, Gerdts E, Jonsson R, et al. Atherosclerosis in Sjögren’s syndrome: evidence, possible mechanisms and knowledge gaps. Clin Exp Rheumatol 2016; 34(1): 133-42.
[PMID: 26812164]
Yong WC, Sanguankeo A, Upala S. Association between primary Sjogren’s syndrome, arterial stiffness, and subclinical atherosclerosis: a systematic review and meta-analysis. Clin Rheumatol 2019; 38(2): 447-55.
[] [PMID: 30178172]
Garcia ABA, Dardin LP, Minali PA, Czapkowsky A, Ajzen SA, Trevisani VF. Asymptomatic atherosclerosis in primary sjögren syndrome: correlation between low ankle brachial index and autoantibodies positivity. J Clin Rheumatol 2016; 22(6): 295-8.
[] [PMID: 27556236]
Karageorgas T, Ioakeimidis D, Mavragani CP. Psychological comorbidities associated with subclinical atherosclerosis in Greek patients with primary Sjögren’s syndrome: a potential contribution of sleep impairment. Clin Exp Rheumatol 2018; 36(3)(Suppl. 112): 68-72.
[PMID: 29148412]
Pérez-De-Lis M, Akasbi M, Sisó A, et al. Cardiovascular risk factors in primary Sjögren’s syndrome: a case-control study in 624 patients. Lupus 2010; 19(8): 941-8.
[] [PMID: 20581017]
Juarez M, Toms TE, de Pablo P, et al. Cardiovascular risk factors in women with primary Sjögren’s syndrome: United Kingdom primary Sjögren’s syndrome registry results. Arthritis Care Res (Hoboken) 2014; 66(5): 757-64.
[] [PMID: 24877201]
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(2): 185-92.
[] [PMID: 25582881]
Wu X-F, Huang J-Y, Chiou J-Y, Chen HH, Wei JC, Dong LL. Increased risk of coronary heart disease among patients with primary Sjögren’s syndrome: a nationwide population-based cohort study. Sci Rep 2018; 8(1): 2209.
[] [PMID: 29396489]
Bartoloni E, Alunno A, Valentini V, et al. The prevalence and relevance of traditional cardiovascular risk factors in primary Sjögren’s syndrome. Clin Exp Rheumatol 2018; 36(3)(Suppl. 112): 113-20.
[PMID: 29998823]
Gasparyan AY, Ayvazyan L, Cocco G, Kitas GD. Adverse cardiovascular effects of antirheumatic drugs: implications for clinical practice and research. Curr Pharm Des 2012; 18(11): 1543-55.
[] [PMID: 22364138]
Rempenault C, Combe B, Barnetche T, et al. Metabolic and cardiovascular benefits of hydroxychloroquine in patients with rheumatoid arthritis: a systematic review and meta-analysis. Ann Rheum Dis 2018; 77(1): 98-103.
[] [PMID: 28970215]
Costedoat-Chalumeau N, Dunogué B, Morel N, Le Guern V, Guettrot-Imbert G. Hydroxychloroquine: a multifaceted treatment in lupus. Presse Med 2014; 43(6 Pt 2): e167-80.
[] [PMID: 24855048]
Sumpter MD, Tatro LS, Stoecker WV, Rader RK. Evidence for risk of cardiomyopathy with hydroxychloroquine. Lupus 2012; 21(14): 1594-6.
[] [PMID: 23036986]
Yogasundaram H, Putko BN, Tien J, et al. Hydroxychloroquine-induced cardiomyopathy: case report, pathophysiology, diagnosis, and treatment. Can J Cardiol 2014; 30(12): 1706-15.
[] [PMID: 25475472]
Aviña-Zubieta JA, Abrahamowicz M, De Vera MA, et al. Immediate and past cumulative effects of oral glucocorticoids on the risk of acute myocardial infarction in rheumatoid arthritis: a population-based study. Rheumatology (Oxford) 2013; 52(1): 68-75.
[] [PMID: 23192907]
Davis JM III, Maradit Kremers H, Crowson CS, et al. Glucocorticoids and cardiovascular events in rheumatoid arthritis: a population-based cohort study. Arthritis Rheum 2007; 56(3): 820-30.
[] [PMID: 17330254]
Souverein PC, Berard A, Van Staa TP, et al. Use of oral glucocorticoids and risk of cardiovascular and cerebrovascular disease in a population based case-control study. Heart 2004; 90(8): 859-65.
[] [PMID: 15253953]
Salles G, Barrett M, Foà R, et al. Rituximab in B-cell hematologic malignancies: a review of 20 years of clinical experience. Adv Ther 2017; 34(10): 2232-73.
[] [PMID: 28983798]
Beltai A, Barnetche T, Daien C, et al. Cardiovascular morbidity and mortality in primary Sjögren syndrome: a systematic review and meta-analysis. Arthritis Care Res (Hoboken) 2020; 72(1): 131-9.
[] [PMID: 30570824]
Yong WC, Sanguankeo A, Upala S. Association between primary Sjögren’s syndrome, cardiovascular and cerebrovascular disease: a systematic review and meta-analysis. Clin Exp Rheumatol 2018; 36(3)(Suppl. 112): 190-7.
[PMID: 29600936]
Agca R, Heslinga SC, Rollefstad S, et al. EULAR recommendations for cardiovascular disease risk management in patients with rheumatoid arthritis and other forms of inflammatory joint disorders: 2015/2016 update. Ann Rheum Dis 2017; 76(1): 17-28.
[] [PMID: 27697765]
Wigley FM, Flavahan NA. Raynaud’s phenomenon. N Engl J Med 2016; 375(6): 556-65.
[] [PMID: 27509103]
García-Carrasco M, Sisó A, Ramos-Casals M, et al. Raynaud’s phenomenon in primary Sjögren’s syndrome. Prevalence and clinical characteristics in a series of 320 patients. J Rheumatol 2002; 29(4): 726-30.
[PMID: 11950013]
Ramos-Casals M, Solans R, Rosas J, et al. Primary Sjögren syndrome in Spain: clinical and immunologic expression in 1010 patients. Medicine (Baltimore) 2008; 87(4): 210-9.
[] [PMID: 18626304]
Kraus A, Caballero-Uribe C, Jakez J, Villa AR, Alarcón-Segovia D. Raynaud’s phenomenon in primary Sjögren’s syndrome. Association with other extraglandular manifestations. J Rheumatol 1992; 19(10): 1572-4.
[PMID: 1464870]
Skopouli FN, Talal A, Galanopoulou V, Tsampoulas CG, Drosos AA, Moutsopoulos HM. Raynaud’s phenomenon in primary Sjögren’s syndrome. J Rheumatol 1990; 17(5): 618-20.
[PMID: 2359071]
Horvath IF, Szanto A, Papp G, Zeher M. Clinical course, prognosis, and cause of death in primary Sjögren’s syndrome. J Immunol Res 2014; 2014647507
[] [PMID: 24963499]
Fragkioudaki S, Mavragani CP, Moutsopoulos HM. Predicting the risk for lymphoma development in Sjogren syndrome: An easy tool for clinical use. Medicine (Baltimore) 2016; 95(25): 3766.
[] [PMID: 27336863]
Levy P-Y, Corey R, Berger P, et al. Etiologic diagnosis of 204 pericardial effusions. Medicine (Baltimore) 2003; 82(6): 385-91.
[] [PMID: 14663288]
Brucato A, Shinar Y, Brambilla G, et al. Idiopathic recurrent acute pericarditis: familial Mediterranean fever mutations and disease evolution in a large cohort of Caucasian patients. Lupus 2005; 14(9): 670-4.
[] [PMID: 16218464]
Gyöngyösi M, Pokorny G, Jambrik Z, et al. Cardiac manifestations in primary Sjögren’s syndrome. Ann Rheum Dis 1996; 55(7): 450-4.
[] [PMID: 8774163]
Rantapää-Dahlqvist S, Backman C, Sandgren H, Ostberg Y. Echocardiographic findings in patients with primary Sjögren’s syndrome. Clin Rheumatol 1993; 12(2): 214-8.
[] [PMID: 8358981]
Vassiliou VA, Moyssakis I, Boki KA, Moutsopoulos HM. Is the heart affected in primary Sjögren’s syndrome? An echocardiographic study. Clin Exp Rheumatol 2008; 26(1): 109-12.
[PMID: 18328155]
Kobak S, Kalkan S, Kirilmaz B, Orman M, Ercan E. Pulmonary arterial hypertension in patients with primary Sjögren’s syndrome. Autoimmune Dis 2014; 2014710401
[] [PMID: 24511390]
Manganelli P, Bernardi P, Taliani U, Caminiti C. Echocardiographic findings in primary Sjögren’s syndrome. Ann Rheum Dis 1997; 56(9): 568.
[] [PMID: 9370886]
Yan S, Li M, Wang H, et al. Characteristics and risk factors of pulmonary arterial hypertension in patients with primary Sjögren’s syndrome. Int J Rheum Dis 2018; 21(5): 1068-75.
[] [PMID: 29624870]
Bridge K, Farivar RS. A case of Sjögren’s syndrome leading to mitral and aortic valve replacement. J Thorac Cardiovasc Surg 2010; 139(6): e139-40.
[] [PMID: 20176373]
Kono M, Aoyagi S, Okazaki T, Tayama K. Aortic stenosis in a patient with Sjogren’s syndrome. Int Heart J 2016; 57(2): 251-3.
[] [PMID: 26973276]
Golan TD, Keren D, Elias N, et al. Severe reversible cardiomyopathy associated with systemic vasculitis in primary Sjögren’s syndrome. Lupus 1997; 6(6): 505-8.
[] [PMID: 9256307]
Levin MD, Zoet-Nugteren SK, Markusse HM. Myocarditis and primary Sjögren’s syndrome. Lancet 1999; 354(9173): 128-9.
[] [PMID: 10408493]
Watanabe T, Takahashi Y, Hirabayashi K, Tomaru U, Machida M. Acute fulminant myocarditis in a patient with primary Sjögren’s syndrome. Scand J Rheumatol 2019; 48(2): 164-5.
[] [PMID: 30516409]
Yoshioka K, Tegoshi H, Yoshida T, Uoshima N, Kasamatsu Y. Myocarditis and primary Sjögren’s syndrome. Lancet 1999; 354(9194): 1996.
[] [PMID: 10622319]
Farber HW, Loscalzo J. Pulmonary arterial hypertension. N Engl J Med 2004; 351(16): 1655-65.
[] [PMID: 15483284]
Badesch DB, Raskob GE, Elliott CG, et al. Pulmonary arterial hypertension: baseline characteristics from the REVEAL Registry. Chest 2010; 137(2): 376-87.
[] [PMID: 19837821]
Condliffe R, Kiely DG, Peacock AJ, et al. Connective tissue disease-associated pulmonary arterial hypertension in the modern treatment era. Am J Respir Crit Care Med 2009; 179(2): 151-7.
[] [PMID: 18931333]
Humbert M, Sitbon O, Chaouat A, et al. Pulmonary arterial hypertension in France: results from a national registry. Am J Respir Crit Care Med 2006; 173(9): 1023-30.
[] [PMID: 16456139]
Lim Y, Low TT, Chan SP, et al. Pulmonary arterial hypertension in a multi-ethnic Asian population: characteristics, survival and mortality predictors from a 14-year follow-up study. Respirology 2019; 24(2): 162-70.
[] [PMID: 30180305]
Zhao J, Wang Q, Liu Y, et al. Clinical characteristics and survival of pulmonary arterial hypertension associated with three major con-nective tissue diseases: A cohort study in China. Int J Cardiol 2017; 236: 432-7.
[] [PMID: 28159359]
Sato T, Hatano M, Iwasaki Y, et al. Prevalence of primary Sjögren’s syndrome in patients undergoing evaluation for pulmonary arterial hypertension. PLoS One 2018; 13(5)e0197297
[] [PMID: 29763424]
Launay D, Hachulla E, Hatron P-Y, Jais X, Simonneau G, Humbert M. Pulmonary arterial hypertension: a rare complication of primary Sjögren syndrome: report of 9 new cases and review of the literature. Medicine (Baltimore) 2007; 86(5): 299-315.
[] [PMID: 17873760]
Liu Z, Yang X, Tian Z, et al. The prognosis of pulmonary arterial hypertension associated with primary Sjögren’s syndrome: a cohort study. Lupus 2018; 27(7): 1072-80.
[] [PMID: 29419347]
Liu Z, Wang J, Lai J, et al. Is it possible to apply the treat-to-target strategy in primary Sjögren’s syndrome-associated pulmonary arterial hypertension? Clin Rheumatol 2018; 37(11): 2989-98.
[] [PMID: 30039269]
Vanoni F, Lava SAG, Fossali EF, et al. Neonatal systemic lupus erythematosus syndrome: a comprehensive review. Clin Rev Allergy Immunol 2017; 53(3): 469-76.
[] [PMID: 29116459]
Brito-Zerón P, Izmirly PM, Ramos-Casals M, Buyon JP, Khamashta MA. The clinical spectrum of autoimmune congenital heart block. Nat Rev Rheumatol 2015; 11(5): 301-12.
[] [PMID: 25800217]
Brucato A. Prevention of congenital heart block in children of SSA-positive mothers. Rheumatology (Oxford) 2008; 47(Suppl. 3): iii35-7.
[] [PMID: 18504284]
Gleicher N, Elkayam U. Preventing congenital neonatal heart block in offspring of mothers with anti-SSA/Ro and SSB/La antibodies: a review of published literature and registered clinical trials. Autoimmun Rev 2013; 12(11): 1039-45.
[] [PMID: 23684701]
Chandler SF, Fynn-Thompson F, Mah DY. Role of cardiac pacing in congenital complete heart block. Expert Rev Cardiovasc Ther 2017; 15(11): 853-61.
[] [PMID: 28875729]
Mofors J, Eliasson H, Ambrosi A, et al. Comorbidity and long-term outcome in patients with congenital heart block and their siblings exposed to Ro/SSA autoantibodies in utero. Ann Rheum Dis 2019; 78(5): 696-703.
[] [PMID: 30808622]
Karnabi E, Boutjdir M. Role of calcium channels in congenital heart block. Scand J Immunol 2010; 72(3): 226-34.
[] [PMID: 20696020]
Lazzerini PE, Capecchi PL, Laghi-Pasini F. The “invulnerability” of the adult conduction system to anti-Ro/SSA antibodies? A matter of calcium channel expression on the cardiomyocyte. J Cardiovasc Electrophysiol 2011; 22(8)E88
[] [PMID: 21692891]
Stea EA, Routsias JG, Clancy RM, Buyon JP, Moutsopoulos HM, Tzioufas AG. Anti-La/SSB antiidiotypic antibodies in maternal serum: a marker of low risk for neonatal lupus in an offspring. Arthritis Rheum 2006; 54(7): 2228-34.
[] [PMID: 16802359]
Routsias JG, Kyriakidis NC, Friedman DM, et al. Association of the idiotype:antiidiotype antibody ratio with the efficacy of intravenous immunoglobulin treatment for the prevention of recurrent autoimmune-associated congenital heart block. Arthritis Rheum 2011; 63(9): 2783-9.
[] [PMID: 21618202]
Jobling K, Rajabally H, Ng W-F. Anti-Ro antibodies and complete heart block in adults with Sjögren’s syndrome. Eur J Rheumatol 2018; 5(3): 194-6.
[] [PMID: 30071943]
Baumgart DC, Gerl H, Dörner T. Complete heart block caused by primary Sjögren’s syndrome and hypopituitarism. Ann Rheum Dis 1998; 57(10): 635.
[] [PMID: 9893579]
Lee LA, Pickrell MB, Reichlin M. Development of complete heart block in an adult patient with Sjögren’s syndrome and anti-Ro/SSA autoantibodies. Arthritis Rheum 1996; 39(8): 1427-9.
[] [PMID: 8702455]
Liang M, Bao L, Xiong N, et al. Cardiac arrhythmias as the initial manifestation of adult primary Sjögren’s syndrome: a case report and literature review. Int J Rheum Dis 2015; 18(7): 800-6.
[] [PMID: 26171561]
Santos-Pardo I, Martínez-Morillo M, Villuendas R, Bayes-Genis A. Anti-Ro antibodies and reversible atrioventricular block. N Engl J Med 2013; 368(24): 2335-7.
[] [PMID: 23758256]
Sung MJ, Park S-H, Kim S-K, Lee YS, Park CY, Choe JY. Complete atrioventricular block in adult Sjögren’s syndrome with anti-Ro autoantibody. Korean J Intern Med (Korean Assoc Intern Med) 2011; 26(2): 213-5.
[] [PMID: 21716914]
Tam WK, Hsu HC, Hsieh MH, Yeh JS, Tam WC. Association of anti-Ro/Sjögren’s syndrome type A antibodies and complete atrio-ventricular block in an adult with Sjögren’s syndrome. Arch Rheumatol 2017; 33(2): 225-9.
[] [PMID: 30207577]
Lazzerini PE, Brucato A, Capecchi PL, et al. Isolated atrioventricular block of unknown origin in the adult and autoimmunity: diagnostic and therapeutic considerations exemplified by 3 anti-Ro/SSA-associated cases. HeartRhythm Case Rep 2015; 1(5): 293-9.
[] [PMID: 28491571]
Lazzerini PE, Acampa M, Guideri F, et al. Prolongation of the corrected QT interval in adult patients with anti-Ro/SSA-positive connective tissue diseases. Arthritis Rheum 2004; 50(4): 1248-52.
[] [PMID: 15077308]
Lodde BM, Sankar V, Kok MR, Leakan RA, Tak PP, Pillemer SR. Adult heart block is associated with disease activity in primary Sjögren’s syndrome. Scand J Rheumatol 2005; 34(5): 383-6.
[] [PMID: 16234186]
Lazzerini PE, Capecchi PL, Laghi-Pasini F. Isolated atrioventricular block of unknown origin in adults and anti-Ro/SSA antibodies: clinical evidence, putative mechanisms, and therapeutic implications. Heart Rhythm 2015; 12(2): 449-54.
[] [PMID: 25444852]
Pavlakis PP, Alexopoulos H, Kosmidis ML, et al. Peripheral neuropathies in Sjögren’s syndrome: a critical update on clinical features and pathogenetic mechanisms. J Autoimmun 2012; 39(1-2): 27-33.
[] [PMID: 22318209]
Dineen J, Freeman R. Autonomic neuropathy. Semin Neurol 2015; 35(4): 458-68.
[] [PMID: 26502768]
Andonopoulos AP, Ballas C. Autonomic cardiovascular neuropathy in primary Sjögren’s syndrome. Rheumatol Int 1995; 15(3): 127-9.
[] [PMID: 8588124]
Adamec I, Žarković K, Sentić M, Habek M. Autonomic failure in Sjögren’s syndrome. Clin Auton Res 2016; 26(2): 165-6.
[] [PMID: 26815843]
Goodman BP. Immunoresponsive autonomic neuropathy in sjögren syndrome-case series and literature review. Am J Ther 2019; 26(1): e66-71.
[] [PMID: 28379880]
Sakakibara R, Hirano S, Asahina M, et al. Primary Sjogren’s syndrome presenting with generalized autonomic failure. Eur J Neurol 2004; 11(9): 635-8.
[] [PMID: 15379743]
Barendregt PJ, Markusse HM, Man In’t Veld AJ. Primary Sjögren’s syndrome presenting as autonomic neuropathy. Case report. Neth J Med 1998; 53(5): 196-200.
[] [PMID: 9852707]
Niemelä RK, Hakala M, Huikuri HV, Airaksinen KE. Comprehensive study of autonomic function in a population with primary Sjögren’s syndrome. No evidence of autonomic involvement. J Rheumatol 2003; 30(1): 74-9.
[PMID: 12508393]
Barendregt PJ, Tulen JH, van den Meiracker AH, Markusse HM. Spectral analysis of heart rate and blood pressure variability in primary Sjögren’s syndrome. Ann Rheum Dis 2002; 61(3): 232-6.
[] [PMID: 11830428]
Andonopoulos AP, Christodoulou J, Ballas C, Bounas A, Alexopoulos D. Autonomic cardiovascular neuropathy in Sjögren’s syndrome. A controlled study. J Rheumatol 1998; 25(12): 2385-8.
[PMID: 9858434]
Kovács L, Paprika D, Tákacs R, et al. Cardiovascular autonomic dysfunction in primary Sjögren’s syndrome. Rheumatology (Oxford) 2004; 43(1): 95-9.
[] [PMID: 12949253]
Koh JH, Kwok S-K, Lee J, Park SH. Autonomic dysfunction in primary Sjogren’s syndrome: a prospective cohort analysis of 154 Korean patients. Korean J Intern Med (Korean Assoc Intern Med) 2017; 32(1): 165-73.
[] [PMID: 27017389]
Mandl T, Hammar O, Theander E, Wollmer P, Ohlsson B. Autonomic nervous dysfunction development in patients with primary Sjogren’s syndrome: a follow-up study. Rheumatology (Oxford) 2010; 49(6): 1101-6.
[] [PMID: 20219783]
Newton JL, Frith J, Powell D, et al. UK primary Sjögren’s syndrome registry. Autonomic symptoms are common and are associated with overall symptom burden and disease activity in primary Sjogren’s syndrome. Ann Rheum Dis 2012; 71(12): 1973-9.
[] [PMID: 22562982]
Cai FZ, Lester S, Lu T, et al. Mild autonomic dysfunction in primary Sjögren’s syndrome: a controlled study. Arthritis Res Ther 2008; 10(2): R31.
[] [PMID: 18328102]

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