Pulmonary Involvement in Sjögren Syndrome

Abstract

Sjögren syndrome (SS) is a chronic autoimmune disease characterized by lymphocytic inflammation of exocrine glands and a variety of extraglandular sites. Lung involvement as defined by symptoms and either pulmonary function testing or radiographic abnormalities occurs in approximately 10 to 20% of patients. Subclinical lung disease is even more frequent and often includes evidence of small airways disease and airway inflammation. In general, patients will have evidence of both airway and interstitial lung disease by radiographs and pathology. Bronchiolitis and bronchiectasis are the most common airway manifestations while the interstitial pathologies associated with SS include nonspecific interstitial pneumonitis, usual interstitial pneumonitis, and lymphocytic interstitial pneumonitis. Patients with SS are also at an increased risk of lymphoma. A protean of other lung abnormalities including amyloidosis, granulomatous lung disease, pseudolymphoma, pulmonary hypertension, and pleural disease have been described.

Keywords

Sjögren syndrome - airways disease - interstitial lung disease - lymphoma - prevalence - treatment

• References

• 1 Shiboski SC, Shiboski CH, Criswell L , et al; Sjögren's International Collaborative Clinical Alliance (SICCA) Research Groups. American College of Rheumatology classification criteria for Sjögren's syndrome: a data-driven, expert consensus approach in the Sjögren's International Collaborative Clinical Alliance cohort. Arthritis Care Res (Hoboken) 2012; 64 (4) 475-487
• 2 Peri Y, Agmon-Levin N, Theodor E, Shoenfeld Y. Sjögren's syndrome, the old and the new. Best Pract Res Clin Rheumatol 2012; 26 (1) 105-117
• 3 Vitali C, Bombardieri S, Jonsson R , et al; European Study Group on Classification Criteria for Sjögren's Syndrome. Classification criteria for Sjögren's syndrome: a revised version of the European criteria proposed by the American-European Consensus Group. Ann Rheum Dis 2002; 61 (6) 554-558
• 4 Mavragani CP, Moutsopoulos HM. The geoepidemiology of Sjögren's syndrome. Autoimmun Rev 2010; 9 (5) A305-A310
• 5 Yazisiz V, Arslan G, Ozbudak IH , et al. Lung involvement in patients with primary Sjögren's syndrome: what are the predictors?. Rheumatol Int 2010; 30 (10) 1317-1324
• 6 Pertovaara M, Korpela M, Saarelainen S , et al. Long-term follow-up study of pulmonary findings in patients with primary Sjögren's syndrome. Scand J Rheumatol 2004; 33 (5) 343-348
• 7 Strimlan CV, Rosenow III EC, Divertie MB, Harrison Jr EG. Pulmonary manifestations of Sjögren's syndrome. Chest 1976; 70 (03) 354-361
• 8 Uffmann M, Kiener HP, Bankier AA, Baldt MM, Zontsich T, Herold CJ. Lung manifestation in asymptomatic patients with primary Sjögren syndrome: assessment with high resolution CT and pulmonary function tests. J Thorac Imaging 2001; 16 (4) 282-289
• 9 Constantopoulos SH, Papadimitriou CS, Moutsopoulos HM. Respiratory manifestations in primary Sjögren's syndrome. A clinical, functional, and histologic study. Chest 1985; 88 (2) 226-229
• 10 García-Carrasco M, Ramos-Casals M, Rosas J , et al. Primary Sjögren syndrome: clinical and immunologic disease patterns in a cohort of 400 patients. Medicine (Baltimore) 2002; 81 (4) 270-280
• 11 Ramos-Casals M, Solans R, Rosas J , et al; GEMESS Study Group. Primary Sjögren syndrome in Spain: clinical and immunologic expression in 1010 patients. Medicine (Baltimore) 2008; 87 (4) 210-219
• 12 Palm O, Garen T, Berge Enger T , et al. Clinical pulmonary involvement in primary Sjogren's syndrome: prevalence, quality of life and mortality—a retrospective study based on registry data. Rheumatology (Oxford) 2013; 52 (1) 173-179
• 13 Gardiner P, Ward C, Allison A , et al. Pleuropulmonary abnormalities in primary Sjögren's syndrome. J Rheumatol 1993; 20 (5) 831-837
• 14 Kelly C, Gardiner P, Pal B, Griffiths I. Lung function in primary Sjögren's syndrome: a cross sectional and longitudinal study. Thorax 1991; 46 (3) 180-183
• 15 Bellido-Casado J, Plaza V, Díaz C , et al. Bronchial inflammation, respiratory symptoms and lung function in Primary Sjögren's syndrome. Arch Bronconeumol 2011; 47 (7) 330-334
• 16 Davidson BK, Kelly CA, Griffiths ID. Ten year follow up of pulmonary function in patients with primary Sjögren's syndrome. Ann Rheum Dis 2000; 59 (9) 709-712
• 17 Aerni MR, Vassallo R, Myers JL, Lindell RM, Ryu JH. Follicular bronchiolitis in surgical lung biopsies: clinical implications in 12 patients. Respir Med 2008; 102 (2) 307-312
• 18 Oxholm P, Bundgaard A, Birk Madsen E, Manthorpe R, Vejlø Rasmussen F. Pulmonary function in patients with primary Sjögren's syndrome. Rheumatol Int 1982; 2 (4) 179-181
• 19 Papathanasiou MP, Constantopoulos SH, Tsampoulas C, Drosos AA, Moutsopoulos HM. Reappraisal of respiratory abnormalities in primary and secondary Sjögren's syndrome. A controlled study. Chest 1986; 90 (3) 370-374
• 20 Papiris SA, Maniati M, Constantopoulos SH, Roussos C, Moutsopoulos HM, Skopouli FN. Lung involvement in primary Sjögren's syndrome is mainly related to the small airway disease. Ann Rheum Dis 1999; 58 (1) 61-64
• 21 Linstow M, Kriegbaum NJ, Backer V, Ulrik C, Oxholm P. A follow-up study of pulmonary function in patients with primary Sjögren's syndrome. Rheumatol Int 1990; 10 (2) 47-49
• 22 Ito I, Nagai S, Kitaichi M , et al. Pulmonary manifestations of primary Sjogren's syndrome: a clinical, radiologic, and pathologic study. Am J Respir Crit Care Med 2005; 171 (6) 632-638
• 23 Dalavanga YA, Voulgari PV, Georgiadis AN , et al. Lymphocytic alveolitis: a surprising index of poor prognosis in patients with primary Sjogren's syndrome. Rheumatol Int 2006; 26 (9) 799-804
• 24 Belenguer R, Ramos-Casals M, Brito-Zerón P , et al. Influence of clinical and immunological parameters on the health-related quality of life of patients with primary Sjögren's syndrome. Clin Exp Rheumatol 2005; 23 (3) 351-356
• 25 Papiris SA, Saetta M, Turato G , et al. CD4-positive T-lymphocytes infiltrate the bronchial mucosa of patients with Sjögren's syndrome. Am J Respir Crit Care Med 1997; 156 (2 Pt 1) 637-641
• 26 Andoh Y, Shimura S, Sawai T, Sasaki H, Takishima T, Shirato K. Morphometric analysis of airways in Sjögren's syndrome. Am Rev Respir Dis 1993; 148 (5) 1358-1362
• 27 Shi JH, Liu HR, Xu WB , et al. Pulmonary manifestations of Sjögren's syndrome. Respiration 2009; 78 (4) 377-386
• 28 Nakanishi M, Fukuoka J, Tanaka T , et al. Small airway disease associated with Sjögren's syndrome: clinico-pathological correlations. Respir Med 2011; 105 (12) 1931-1938
• 29 Ryu JH, Myers JL, Swensen SJ. Bronchiolar disorders. Am J Respir Crit Care Med 2003; 168 (11) 1277-1292
• 30 Yousem SA, Colby TV, Carrington CB. Follicular bronchitis/bronchiolitis. Hum Pathol 1985; 16 (7) 700-706
• 31 Borie R, Schneider S, Debray MP , et al. Severe chronic bronchiolitis as the presenting feature of primary Sjögren's syndrome. Respir Med 2011; 105 (1) 130-136
• 32 Gottenberg JE, Cinquetti G, Larroche C , et al; Club Rhumatismes et Inflammations and the French Society of Rheumatology. Efficacy of rituximab in systemic manifestations of primary Sjogren's syndrome: results in 78 patients of the AutoImmune and Rituximab registry. Ann Rheum Dis 2013; 72 (6) 1026-1031
• 33 Lohrmann C, Uhl M, Warnatz K , et al. High-resolution CT imaging of the lung for patients with primary Sjogren's syndrome. Eur J Radiol 2004; 52 (2) 137-143
• 34 Watanabe M, Naniwa T, Hara M, Arakawa T, Maeda T. Pulmonary manifestations in Sjogren's syndrome: correlation analysis between chest computed tomographic findings and clinical subsets with poor prognosis in 80 patients. J Rheumatol 2010; 37 (2) 365-373
• 35 Mandl T, Diaz S, Ekberg O , et al. Frequent development of chronic obstructive pulmonary disease in primary SS—results of a longitudinal follow-up. Rheumatology (Oxford) 2012; 51 (5) 941-946
• 36 Soto-Cardenas MJ, Perez-De-Lis M, Bove A , et al. Bronchiectasis in primary Sjögren's syndrome: prevalence and clinical significance. Clin Exp Rheumatol 2010; 28 (5) 647-653
• 37 Deheinzelin D, Capelozzi VL, Kairalla RA, Barbas Filho JV, Saldiva PH, de Carvalho CR. Interstitial lung disease in primary Sjögren's syndrome. Clinical-pathological evaluation and response to treatment. Am J Respir Crit Care Med 1996; 154 (3 Pt 1) 794-799
• 38 Franquet T, Giménez A, Monill JM, Díaz C, Geli C. Primary Sjögren's syndrome and associated lung disease: CT findings in 50 patients. AJR Am J Roentgenol 1997; 169 (3) 655-658
• 39 Taouli B, Brauner MW, Mourey I, Lemouchi D, Grenier PA. Thin-section chest CT findings of primary Sjögren's syndrome: correlation with pulmonary function. Eur Radiol 2002; 12 (6) 1504-1511
• 40 Matsuyama N, Ashizawa K, Okimoto T, Kadota J, Amano H, Hayashi K. Pulmonary lesions associated with Sjögren's syndrome: radiographic and CT findings. Br J Radiol 2003; 76 (912) 880-884
• 41 Liebow AA, Carrington CB. Diffuse pulmonary lymphoreticular infiltrations associated with dysproteinemia. Med Clin North Am 1973; 57 (3) 809-843
• 42 Parambil JG, Myers JL, Lindell RM, Matteson EL, Ryu JH. Interstitial lung disease in primary Sjögren syndrome. Chest 2006; 130 (5) 1489-1495
• 43 Suda T, Kaida Y, Nakamura Y , et al. Acute exacerbation of interstitial pneumonia associated with collagen vascular diseases. Respir Med 2009; 103 (6) 846-853
• 44 Isaksen K, Jonsson R, Omdal R. Anti-CD20 treatment in primary Sjögren's syndrome. Scand J Immunol 2008; 68 (6) 554-564
• 45 Cha SI, Fessler MB, Cool CD, Schwarz MI, Brown KK. Lymphoid interstitial pneumonia: clinical features, associations and prognosis. Eur Respir J 2006; 28 (2) 364-369
• 46 Johkoh T, Müller NL, Pickford HA , et al. Lymphocytic interstitial pneumonia: thin-section CT findings in 22 patients. Radiology 1999; 212 (2) 567-572
• 47 Johkoh T, Ichikado K, Akira M , et al. Lymphocytic interstitial pneumonia: follow-up CT findings in 14 patients. J Thorac Imaging 2000; 15 (3) 162-167
• 48 Watanabe Y, Koyama S, Miwa C , et al. Pulmonary mucosa-associated lymphoid tissue (MALT) lymphoma in Sjögren's syndrome showing only the LIP pattern radiologically. Intern Med 2012; 51 (5) 491-495
• 49 Swartz MA, Vivino FB. Dramatic reversal of lymphocytic interstitial pneumonitis in Sjögren's syndrome with rituximab. J Clin Rheumatol 2011; 17 (8) 454
• 50 Seror R, Sordet C, Guillevin L , et al. Tolerance and efficacy of rituximab and changes in serum B cell biomarkers in patients with systemic complications of primary Sjögren's syndrome. Ann Rheum Dis 2007; 66 (3) 351-357
• 51 Fauchais AL, Lambert M, Launay D , et al. Antiphospholipid antibodies in primary Sjögren's syndrome: prevalence and clinical significance in a series of 74 patients. Lupus 2004; 13 (4) 245-248
• 52 Ramagopalan SV, Wotton CJ, Handel AE, Yeates D, Goldacre MJ. Risk of venous thromboembolism in people admitted to hospital with selected immune-mediated diseases: record-linkage study. BMC Med 2011; 9: 1
• 53 Rajagopala S, Singh N, Gupta K, Gupta D. Pulmonary amyloidosis in Sjogren's syndrome: a case report and systematic review of the literature. Respirology 2010; 15 (5) 860-866
• 54 Subcutaneous masses and adenopathy in a 77-year-old man with Sjögren's syndrome and amyloidosis. Am J Med 1989; 86 (5) 585-590
• 55 Anderson LG, Talal N. The spectrum of benign to malignant lymphoproliferation in Sjögren's syndrome. Clin Exp Immunol 1972; 10 (2) 199-221
• 56 Bonner Jr H, Ennis RS, Geelhoed GW, Tarpley Jr TM. Lymphoid infiltration and amyloidosis of lung in Sjögren's syndrome. Arch Pathol 1973; 95 (1) 42-44
• 57 Strimlan CV. Pulmonary involvement in Sjögren's syndrome. Chest 1986; 89 (6) 901-902
• 58 Desai SR, Nicholson AG, Stewart S, Twentyman OM, Flower CD, Hansell DM. Benign pulmonary lymphocytic infiltration and amyloidosis: computed tomographic and pathologic features in three cases. J Thorac Imaging 1997; 12 (3) 215-220
• 59 Jeong YJ, Lee KS, Chung MP , et al. Amyloidosis and lymphoproliferative disease in Sjögren syndrome: thin-section computed tomography findings and histopathologic comparisons. J Comput Assist Tomogr 2004; 28 (6) 776-781
• 60 Lantuejoul S, Moulai N, Quetant S , et al. Unusual cystic presentation of pulmonary nodular amyloidosis associated with MALT-type lymphoma. Eur Respir J 2007; 30 (3) 589-592
• 61 Naniwa T, Takeda Y. Long-term remission of pulmonary veno-occlusive disease associated with primary Sjögren's syndrome following immunosuppressive therapy. Mod Rheumatol 2011; 21 (6) 637-640
• 62 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) 109-112
• 63 Launay D, Hachulla E, Hatron PY, 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
• 64 Sato T, Matsubara O, Tanaka Y, Kasuga T. Association of Sjögren's syndrome with pulmonary hypertension: report of two cases and review of the literature. Hum Pathol 1993; 24 (2) 199-205
• 65 Bertoni M, Niccoli L, Porciello G , et al. Pulmonary hypertension in primary Sjögren's syndrome: report of a case and review of the literature. Clin Rheumatol 2005; 24 (4) 431-434
• 66 Hedgpeth MT, Boulware DW. Pulmonary hypertension in primary Sjögren's syndrome. Ann Rheum Dis 1988; 47 (3) 251-253
• 67 Teshigawara K, Kakizaki S, Horiya M , et al. Primary Sjogren's syndrome complicated by bilateral pleural effusion. Respirology 2008; 13 (1) 155-158
• 68 Kawamata K, Haraoka H, Hirohata S, Hashimoto T, Jenkins RN, Lipsky PE. Pleurisy in primary Sjögren's syndrome: T cell receptor beta-chain variable region gene bias and local autoantibody production in the pleural effusion. Clin Exp Rheumatol 1997; 15 (2) 193-196
• 69 Langenskiöld E, Bonetti A, Fitting JW , et al. Shrinking lung syndrome successfully treated with rituximab and cyclophosphamide. Respiration 2012; 84 (2) 144-149
• 70 Carmier D, Diot E, Diot P. Shrinking lung syndrome: recognition, pathophysiology and therapeutic strategy. Expert Rev Respir Med 2011; 5 (1) 33-39
• 71 Reddy KS, Jha V, Nada R , et al. Respiratory paralysis in Sjogren syndrome with normal renal function. Natl Med J India 2003; 16 (5) 253-254
• 72 Ohtani H, Imai H, Kodama T , et al. Severe hypokalaemia and respiratory arrest due to renal tubular acidosis in a patient with Sjögren syndrome. Nephrol Dial Transplant 1999; 14 (9) 2201-2203
• 73 Poux JM, Peyronnet P, Le Meur Y, Favereau JP, Charmes JP, Leroux-Robert C. Hypokalemic quadriplegia and respiratory arrest revealing primary Sjögren's syndrome. Clin Nephrol 1992; 37 (4) 189-191
• 74 Koga T, Kouhisa Y, Nakamura H , et al. A case of primary Sjögren's syndrome complicated with inflammatory myopathy and interstitial lung disease. Rheumatol Int 2012; 32 (11) 3647-3649
• 75 Sorajja P, Poirier MK, Bundrick JB, Matteson EL. Autonomic failure and proximal skeletal myopathy in a patient with primary Sjögren syndrome. Mayo Clin Proc 1999; 74 (7) 695-697
• 76 Alexander EL. Neurologic disease in Sjögren's syndrome: mononuclear inflammatory vasculopathy affecting central/peripheral nervous system and muscle. A clinical review and update of immunopathogenesis. Rheum Dis Clin North Am 1993; 19 (4) 869-908
• 77 Johnston SL, Dudley CR, Unsworth DJ, Lock RJ. Life-threatening acute pulmonary haemorrhage in primary Sjögren's syndrome with cryoglobulinaemia. Scand J Rheumatol 2005; 34 (5) 404-407
• 78 Tomita Y, Mori S, Arima N, Fukuda K, Kohrogi H. Rapidly progressive pulmonary fibrosis following the onset of diffuse alveolar hemorrhage in Sjögren's syndrome: an autopsy case report. Intern Med 2012; 51 (3) 295-299
• 79 Gal I, Kovacs J, Zeher M. Case series: coexistence of Sjögren's syndrome and sarcoidosis. J Rheumatol 2000; 27 (10) 2507-2510
• 80 Ramos-Casals M, Font J, Garcia-Carrasco M , et al. Primary Sjögren syndrome: hematologic patterns of disease expression. Medicine (Baltimore) 2002; 81 (4) 281-292
• 81 Ramos-Casals M, Brito-Zerón P, García-Carrasco M, Font J. Sarcoidosis or Sjögren syndrome? Clues to defining mimicry or coexistence in 59 cases. Medicine (Baltimore) 2004; 83 (2) 85-95
• 82 Kauppi M, Pukkala E, Isomäki H. Elevated incidence of hematologic malignancies in patients with Sjögren's syndrome compared with patients with rheumatoid arthritis (Finland). Cancer Causes Control 1997; 8 (2) 201-204
• 83 Theander E, Henriksson G, Ljungberg O, Mandl T, Manthorpe R, Jacobsson LT. Lymphoma and other malignancies in primary Sjögren's syndrome: a cohort study on cancer incidence and lymphoma predictors. Ann Rheum Dis 2006; 65 (6) 796-803
• 84 Ioannidis JP, Vassiliou VA, Moutsopoulos HM. Long-term risk of mortality and lymphoproliferative disease and predictive classification of primary Sjögren's syndrome. Arthritis Rheum 2002; 46 (3) 741-747
• 85 Ramos-Casals M, Brito-Zerón P, Yagüe J , et al. Hypocomplementaemia as an immunological marker of morbidity and mortality in patients with primary Sjogren's syndrome. Rheumatology (Oxford) 2005; 44 (1) 89-94
• 86 Voulgarelis M, Dafni UG, Isenberg DA, Moutsopoulos HM. Malignant lymphoma in primary Sjögren's syndrome: a multicenter, retrospective, clinical study by the European Concerted Action on Sjögren's Syndrome. Arthritis Rheum 1999; 42 (8) 1765-1772
• 87 Kokosi M, Riemer EC, Highland KB. Pulmonary involvement in Sjögren syndrome. Clin Chest Med 2010; 31 (3) 489-500
• 88 Leandro MJ, Isenberg DA. Rheumatic diseases and malignancy—is there an association?. Scand J Rheumatol 2001; 30 (4) 185-188
• 89 Franquet T, Díaz C, Domingo P, Giménez A, Geli C. Air trapping in primary Sjögren syndrome: correlation of expiratory CT with pulmonary function tests. J Comput Assist Tomogr 1999; 23 (2) 169-173
• 90 Pisa EK, Pisa P, Kang HI, Fox RI. High frequency of t(14;18) translocation in salivary gland lymphomas from Sjögren's syndrome patients. J Exp Med 1991; 174 (5) 1245-1250
• 91 Tonami H, Matoba M, Kuginuki Y , et al. Clinical and imaging findings of lymphoma in patients with Sjögren syndrome. J Comput Assist Tomogr 2003; 27 (4) 517-524
• 92 Papiris SA, Kalomenidis I, Malagari K , et al. Extranodal marginal zone B-cell lymphoma of the lung in Sjögren's syndrome patients: reappraisal of clinical, radiological, and pathology findings. Respir Med 2007; 101 (1) 84-92
• 93 Sunada K, Hasegawa Y, Kodama T , et al. Thymic and pulmonary mucosa-associated lymphoid tissue lymphomas in a patient with Sjögren's syndrome and literature review. Respirology 2007; 12 (1) 144-147
• 94 Song MK, Seol YM, Park YE , et al. Pulmonary nodular lymphoid hyperplasia associated with Sjögren's syndrome. Korean J Intern Med 2007; 22 (3) 192-196