Generic placeholder image

Current Rheumatology Reviews


ISSN (Print): 1573-3971
ISSN (Online): 1875-6360

Review Article

Reinterpreting Evidence of Rheumatoid Arthritis-Associated Interstitial Lung Disease to Understand Etiology

Author(s): Emily K. Wu, Robert D. Ambrosini, R. Matthew Kottmann, Christopher T. Ritchlin, Edward M. Schwarz and Homaira Rahimi*

Volume 15 , Issue 4 , 2019

Page: [277 - 289] Pages: 13

DOI: 10.2174/1573397115666190116102451

Price: $65


Interstitial Lung Disease (ILD) is a well-known complication of rheumatoid arthritis (RA) which often results in significant morbidity and mortality. It is often diagnosed late in the disease process via descriptive criteria. Multiple subtypes of RA-ILD exist as defined by chest CT and histopathology. In the absence of formal natural history studies and definitive diagnostics, a conventional dogma has emerged that there are two major subtypes of RA-ILD (nonspecific interstitial pneumonia (NSIP) and Usual Interstitial Pneumonia (UIP)). These subtypes are based on clinical experience and correlation studies. However, recent animal model data are incongruous with established paradigms of RA-ILD and beg reassessment of the clinical evidence in order to better understand etiology, pathogenesis, prognosis, and response to therapy. To this end, here we: 1) review the literature on epidemiology, radiology, histopathology and clinical outcomes of the various RAILD subtypes, existing animal models, and current theories on RA-ILD pathogenesis; 2) highlight the major gaps in our knowledge; and 3) propose future research to test an emerging theory of RAILD that posits initial rheumatic lung inflammation in the form of NSIP-like pathology transforms mesenchymal cells to derive chimeric disease, and subsequently develops into frank UIP-like fibrosis in some RA patients. Elucidation of the pathogenesis of RA-ILD is critical for the development of effective interventions for RA-ILD.

Keywords: Rheumatoid Arthritis-Associated Interstitial Lung Disease (RA-ILD), Nonspecific Interstitial Pneumonia (NSIP), Usual Interstitial Pneumonia (UIP), Computed Tomography (CT), Histology, inflammation, fibrosis, animal models.

Graphical Abstract
Kim EJ, Collard HR, King TE Jr. Rheumatoid arthritis-associated interstitial lung disease: the relevance of histopathologic and radiographic pattern. Chest 2009; 136(5): 1397-405.
[] [PMID: 19892679]
O’Dwyer DN, Armstrong ME, Cooke G, Dodd JD, Veale DJ, Donnelly SC. Rheumatoid Arthritis (RA) associated interstitial lung disease (ILD). Eur J Intern Med 2013; 24(7): 597-603.
[] [PMID: 23916467]
Aubart F, Crestani B, Nicaise-Roland P, et al. High levels of anti-cyclic citrullinated peptide autoantibodies are associated with co-occurrence of pulmonary diseases with rheumatoid arthritis. J Rheumatol 2011; 38(6): 979-82.
[] [PMID: 21362759]
Luukkainen R, Saltyshev M, Pakkasela R, Nordqvist E, Huhtala H, Hakala M. Relationship of rheumatoid factor to lung diffusion capacity in smoking and non-smoking patients with rheumatoid arthritis. Scand J Rheumatol 1995; 24(2): 119-20.
[] [PMID: 7747143]
Gibofsky A. Overview of epidemiology, pathophysiology, and diagnosis of rheumatoid arthritis. Am J Manag Care 2012; 18(13)(Suppl.): S295-302.
[PMID: 23327517]
Helmick CG, Felson DT, Lawrence RC, et al. National Arthritis Data Workgroup. Estimates of the prevalence of arthritis and other rheumatic conditions in the United States. Part I. Arthritis Rheum 2008; 58(1): 15-25.
[] [PMID: 18163481]
Haringman JJ, Gerlag DM, Zwinderman AH, et al. Synovial tissue macrophages: A sensitive biomarker for response to treatment in patients with rheumatoid arthritis. Ann Rheum Dis 2005; 64(6): 834-8.
[] [PMID: 15576415]
McInnes IB, Schett G. The pathogenesis of rheumatoid arthritis. N Engl J Med 2011; 365(23): 2205-19.
[] [PMID: 22150039]
Firestein GS. Evolving concepts of rheumatoid arthritis. Nature 2003; 423(6937): 356-61.
[] [PMID: 12748655]
Lajas C, Abasolo L, Bellajdel B, et al. Costs and predictors of costs in rheumatoid arthritis: a prevalence-based study. Arthritis Rheum 2003; 49(1): 64-70.
[] [PMID: 12579595]
Gabriel SE, Crowson CS, Kremers HM, et al. Survival in rheumatoid arthritis: a population-based analysis of trends over 40 years. Arthritis Rheum 2003; 48(1): 54-8.
[] [PMID: 12528103]
Minaur NJ, Jacoby RK, Cosh JA, Taylor G, Rasker JJ. Outcome after 40 years with rheumatoid arthritis: a prospective study of function, disease activity, and mortality. J Rheumatol Suppl 2004; 69: 3-8.
[PMID: 15053445]
Kuo CF, Luo SF, See LC, Chou IJ, Chang HC, Yu KH. Rheumatoid arthritis prevalence, incidence, and mortality rates: a nationwide population study in Taiwan. Rheumatol Int 2013; 33(2): 355-60.
[] [PMID: 22451027]
Sparks JA, Chang SC, Liao KP, et al. Rheumatoid Arthritis and Mortality Among Women During 36 Years of Prospective Follow-Up: Results From the Nurses’ Health Study. Arthritis Care Res (Hoboken) 2016; 68(6): 753-62.
[] [PMID: 26473946]
Bongartz T, Nannini C, Medina-Velasquez YF, et al. Incidence and mortality of interstitial lung disease in rheumatoid arthritis: a population-based study. Arthritis Rheum 2010; 62(6): 1583-91.
[] [PMID: 20155830]
Olson AL, Swigris JJ, Sprunger DB, et al. Rheumatoid arthritis-interstitial lung disease-associated mortality. Am J Respir Crit Care Med 2011; 183(3): 372-8.
[] [PMID: 20851924]
Schmidt SL, Sundaram B, Flaherty KR. Diagnosing fibrotic lung disease: when is high-resolution computed tomography sufficient to make a diagnosis of idiopathic pulmonary fibrosis? Respirology 2009; 14(7): 934-9.
[] [PMID: 19740255]
Aaløkken TM, Naalsund A, Mynarek G, et al. Diagnostic accuracy of computed tomography and histopathology in the diagnosis of usual interstitial pneumonia. Acta Radiol 2012; 53(3): 296-302.
[] [PMID: 22334869]
Doyle JJ, Eliasson AH, Argyros GJ, et al. Prevalence of pulmonary disorders in patients with newly diagnosed rheumatoid arthritis. Clin Rheumatol 2000; 19(3): 217-21.
[] [PMID: 10870658]
Richman NC, Yazdany J, Graf J, Chernitskiy V, Imboden JB. Extraarticular manifestations of rheumatoid arthritis in a multiethnic cohort of predominantly Hispanic and Asian patients. Medicine (Baltimore) 2013; 92(2): 92-7.
[] [PMID: 23429352]
Carmona L, González-Alvaro I, Balsa A, Angel Belmonte M, Tena X, Sanmartí R. Rheumatoid arthritis in Spain: occurrence of extra-articular manifestations and estimates of disease severity. Ann Rheum Dis 2003; 62(9): 897-900.
[] [PMID: 12922967]
Gabbay E, Tarala R, Will R, et al. Interstitial lung disease in recent onset rheumatoid arthritis. Am J Respir Crit Care Med 1997; 156(2 Pt 1): 528-35.
[] [PMID: 9279235]
Mori S, Cho I, Koga Y, Sugimoto M. Comparison of pulmonary abnormalities on high-resolution computed tomography in patients with early versus longstanding rheumatoid arthritis. J Rheumatol 2008; 35(8): 1513-21.
[PMID: 18597412]
Hyldgaard C, Hilberg O, Pedersen AB, et al. A population-based cohort study of rheumatoid arthritis-associated interstitial lung disease: comorbidity and mortality. Ann Rheum Dis 2017; 76(10): 1700-6.
[] [PMID: 28611082]
Kim D, Cho SK, Choi CB, et al. Impact of interstitial lung disease on mortality of patients with rheumatoid arthritis. Rheumatol Int 2017; 37(10): 1735-45.
[] [PMID: 28748423]
Solomon JJ, Ryu JH, Tazelaar HD, et al. Fibrosing interstitial pneumonia predicts survival in patients with rheumatoid arthritis-associated interstitial lung disease (RA-ILD). Respir Med 2013; 107(8): 1247-52.
[] [PMID: 23791462]
Koduri G, Norton S, Young A, et al. Interstitial lung disease has a poor prognosis in rheumatoid arthritis: results from an inception cohort. Rheumatology (Oxford) 2010; 49(8): 1483-9.
[] [PMID: 20223814]
Yunt ZX, Chung JH, Hobbs S, et al. High resolution computed tomography pattern of usual interstitial pneumonia in rheumatoid arthritis-associated interstitial lung disease: Relationship to survival. Respir Med 2017; 126: 100-4.
[] [PMID: 28427540]
Zamora-Legoff JA, Krause ML, Crowson CS, Ryu JH, Matteson EL. Patterns of interstitial lung disease and mortality in rheumatoid arthritis. Rheumatology (Oxford) 2017; 56(3): 344-50.
[] [PMID: 27940586]
Lee HK, Kim DS, Yoo B, et al. Histopathologic pattern and clinical features of rheumatoid arthritis-associated interstitial lung disease. Chest 2005; 127(6): 2019-27.
[] [PMID: 15947315]
Solomon JJ, Chung JH, Cosgrove GP, et al. Predictors of mortality in rheumatoid arthritis-associated interstitial lung disease. Eur Respir J 2016; 47(2): 588-96.
[] [PMID: 26585429]
Nurmi HM, Purokivi MK, Kärkkäinen MS, Kettunen HP, Selander TA, Kaarteenaho RL. Variable course of disease of rheumatoid arthritis-associated usual interstitial pneumonia compared to other subtypes. BMC Pulm Med 2016; 16(1): 107.
[] [PMID: 27461264]
Zamora-Legoff JA, Krause ML, Crowson CS, Ryu JH, Matteson EL. Progressive decline of lung function in rheumatoid arthritis-associated interstitial lung disease. Arthritis Rheumatol 2017; 69(3): 542-9.
[] [PMID: 27788297]
Kelly CA, Saravanan V, Nisar M, et al. Rheumatoid arthritis-related interstitial lung disease: associations, prognostic factors and physiological and radiological characteristics--a large multicentre UK study. Rheumatology (Oxford) 2014; 53(9): 1676-82.
[] [PMID: 24758887]
Kim EJ, Elicker BM, Maldonado F, et al. Usual interstitial pneumonia in rheumatoid arthritis-associated interstitial lung disease. Eur Respir J 2010; 35(6): 1322-8.
[] [PMID: 19996193]
Wang JX, Du CG. A retrospective study of clinical characteristics of interstitial lung disease associated with rheumatoid arthritis in Chinese patients. Med Sci Monit 2015; 21: 708-15.
[] [PMID: 25746669]
Fujii M, Adachi S, Shimizu T, Hirota S, Sako M, Kono M. Interstitial lung disease in rheumatoid arthritis: assessment with high-resolution computed tomography. J Thorac Imaging 1993; 8(1): 54-62.
[] [PMID: 8418318]
Cortet B, Flipo RM, Rémy-Jardin M, et al. Use of high resolution computed tomography of the lungs in patients with rheumatoid arthritis. Ann Rheum Dis 1995; 54(10): 815-9.
[] [PMID: 7492220]
Franquet T. High-resolution CT of lung disease related to collagen vascular disease. Radiol Clin North Am 2001; 39(6): 1171-87.
[] [PMID: 11699667]
du Bois R, King TE Jr. Challenges in pulmonary fibrosis x 5: the NSIP/UIP debate. Thorax 2007; 62(11): 1008-12.
[] [PMID: 17965079]
Flaherty KR, Thwaite EL, Kazerooni EA, et al. Radiological versus histological diagnosis in UIP and NSIP: survival implications. Thorax 2003; 58(2): 143-8.
[] [PMID: 12554898]
Flaherty KR, Travis WD, Colby TV, et al. Histopathologic variability in usual and nonspecific interstitial pneumonias. Am J Respir Crit Care Med 2001; 164(9): 1722-7.
[] [PMID: 11719316]
Li XR, Peng SC, Wei LQ. Nonspecific interstitial pneumonia overlaps organizing pneumonia in lung-dominant connective tissue disease. Int J Clin Exp Pathol 2015; 8(9): 11230-5.
[PMID: 26617847]
Mäkelä K, Hodgson U, Piilonen A, et al. Analysis of the histologic features associated with interobserver variation in idiopathic pulmonary fibrosis. Am J Surg Pathol 2018; 42(5): 672-8.
[] [PMID: 29438171]
Katzenstein AL, Zisman DA, Litzky LA, Nguyen BT, Kotloff RM. Usual interstitial pneumonia: histologic study of biopsy and explant specimens. Am J Surg Pathol 2002; 26(12): 1567-77.
[] [PMID: 12459623]
Doyle TJ, Dellaripa PF. Lung manifestations in the rheumatic diseases. Chest 2017; 152(6): 1283-95.
[] [PMID: 28552544]
Bouros D, Wells AU, Nicholson AG, et al. Histopathologic subsets of fibrosing alveolitis in patients with systemic sclerosis and their relationship to outcome. Am J Respir Crit Care Med 2002; 165(12): 1581-6.
[] [PMID: 12070056]
Douglas WW, Tazelaar HD, Hartman TE, et al. Polymyositis-dermatomyositis-associated interstitial lung disease. Am J Respir Crit Care Med 2001; 164(7): 1182-5.
[] [PMID: 11673206]
Kim DS, Yoo B, Lee JS, et al. The major histopathologic pattern of pulmonary fibrosis in scleroderma is nonspecific interstitial pneumonia. Sarcoidosis Vasc Diffuse Lung Dis 2002; 19(2): 121-7.
[PMID: 12108451]
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): 632-8.
[] [PMID: 15579729]
Assayag D, Elicker BM, Urbania TH, et al. Rheumatoid arthritis-associated interstitial lung disease: radiologic identification of usual interstitial pneumonia pattern. Radiology 2014; 270(2): 583-8.
[] [PMID: 24126367]
Yoshinouchi T, Ohtsuki Y, Fujita J, et al. Nonspecific interstitial pneumonia pattern as pulmonary involvement of rheumatoid arthritis. Rheumatol Int 2005; 26(2): 121-5.
[] [PMID: 15580351]
Travis WD, Costabel U, Hansell DM, et al. An official American Thoracic Society/European Respiratory Society statement: Update of the international multidisciplinary classification of the idiopathic interstitial pneumonias. Am J Respir Crit Care Med 2013; 188(6): 733-48.
[] [PMID: 24032382]
Katzenstein AL, Mukhopadhyay S, Myers JL. Diagnosis of usual interstitial pneumonia and distinction from other fibrosing interstitial lung diseases. Hum Pathol 2008; 39(9): 1275-94.
[] [PMID: 18706349]
Veeraraghavan S, Latsi PI, Wells AU, et al. BAL findings in idiopathic nonspecific interstitial pneumonia and usual interstitial pneumonia. Eur Respir J 2003; 22(2): 239-44.
[] [PMID: 12952254]
MacDonald SL, Rubens MB, Hansell DM, et al. Nonspecific interstitial pneumonia and usual interstitial pneumonia: comparative appearances at and diagnostic accuracy of thin-section CT. Radiology 2001; 221(3): 600-5.
[] [PMID: 11719652]
Kligerman SJ, Groshong S, Brown KK, Lynch DA. Nonspecific interstitial pneumonia: radiologic, clinical, and pathologic considerations. Radiographics 2009; 29(1): 73-87.
[] [PMID: 19168837]
Travis WD, Matsui K, Moss J, Ferrans VJ. Idiopathic nonspecific interstitial pneumonia: prognostic significance of cellular and fibrosing patterns: survival comparison with usual interstitial pneumonia and desquamative interstitial pneumonia. Am J Surg Pathol 2000; 24(1): 19-33.
[] [PMID: 10632484]
Johnson C. Recent advances in the pathogenesis, prediction, and management of rheumatoid arthritis-associated interstitial lung disease. Curr Opin Rheumatol 2017; 29(3): 254-9.
[] [PMID: 28207496]
Nicholson AG, Colby TV, du Bois RM, Hansell DM, Wells AU. The prognostic significance of the histologic pattern of interstitial pneumonia in patients presenting with the clinical entity of cryptogenic fibrosing alveolitis. Am J Respir Crit Care Med 2000; 162(6): 2213-7.
[] [PMID: 11112140]
Akira M, Sakatani M, Hara H. Thin-section CT findings in rheumatoid arthritis-associated lung disease: CT patterns and their courses. J Comput Assist Tomogr 1999; 23(6): 941-8.
[] [PMID: 10589572]
Assayag D, Lubin M, Lee JS, King TE, Collard HR, Ryerson CJ. Predictors of mortality in rheumatoid arthritis-related interstitial lung disease. Respirology 2014; 19(4): 493-500.
[] [PMID: 24372981]
Remy-Jardin M, Remy J, Cortet B, Mauri F, Delcambre B. Lung changes in rheumatoid arthritis: CT findings. Radiology 1994; 193(2): 375-82.
[] [PMID: 7972746]
Tanaka N, Kim JS, Newell JD, et al. Rheumatoid arthritis-related lung diseases: CT findings. Radiology 2004; 232(1): 81-91.
[] [PMID: 15166329]
Mori S. Management of rheumatoid arthritis patients with interstitial lung disease: Safety of biological antirheumatic drugs and assessment of pulmonary fibrosis. Clin Med Insights Circ Respir Pulm Med 2015; 9(Suppl. 1): 41-9.
[] [PMID: 26401101]
Roubille C, Haraoui B. Interstitial lung diseases induced or exacerbated by DMARDS and biologic agents in rheumatoid arthritis: a systematic literature review. Semin Arthritis Rheum 2014; 43(5): 613-26.
[] [PMID: 24231065]
Perez-Alvarez R, Perez-de-Lis M, Diaz-Lagares C, et al. Interstitial lung disease induced or exacerbated by TNF-targeted therapies: analysis of 122 cases. Semin Arthritis Rheum 2011; 41(2): 256-64.
[] [PMID: 21277618]
Koo BS, Hong S, Kim YJ, Kim YG, Lee CK, Yoo B. Mortality in patients with rheumatoid arthritis-associated interstitial lung disease treated with an anti-tumor necrosis factor agent. Korean J Intern Med (Korean Assoc Intern Med) 2015; 30(1): 104-9.
[] [PMID: 25589842]
Conway R, et al. Methotrexate and interstitial lung disease in rheumatoid arthritis-a systematic literature review and meta-analysis. Ir J Med Sci 2013; 182: S94-4.
Dawson JK, Graham DR, Desmond J, Fewins HE, Lynch MP. Investigation of the chronic pulmonary effects of low-dose oral methotrexate in patients with rheumatoid arthritis: a prospective study incorporating HRCT scanning and pulmonary function tests. Rheumatology (Oxford) 2002; 41(3): 262-7.
[] [PMID: 11934961]
Khanna D, et al. Mycophenolate mofetil versus oral cyclophosphamide in scleroderma-related interstitial lung disease: scleroderma lung study II. Ann Rheum Dis 2016; 75: 531-1.
Hayashi M, Kikuchi T, Takada T. Mycophenolate mofetil for the patients with interstitial lung diseases in amyopathic dermatomyositis with anti-MDA-5 antibodies. Clin Rheumatol 2017; 36(1): 239-40.
[] [PMID: 27718019]
Tashkin DP, Elashoff R, Clements PJ, et al. Cyclophosphamide versus placebo in scleroderma lung disease. N Engl J Med 2006; 354(25): 2655-66.
[] [PMID: 16790698]
Suda T. Up-to-Date Information on Rheumatoid Arthritis-Associated Interstitial Lung Disease. Clin Med Insights Circ Respir Pulm Med 2016; 9(Suppl. 1): 155-62.
[] [PMID: 27279757]
Picchianti Diamanti A, Markovic M, Argento G, et al. Therapeutic management of patients with rheumatoid arthritis and associated interstitial lung disease: case report and literature review. Ther Adv Respir Dis 2017; 11(1): 64-72.
[] [PMID: 27733490]
Wolfe F, Caplan L, Michaud K. Treatment for rheumatoid arthritis and the risk of hospitalization for pneumonia: associations with prednisone, disease-modifying antirheumatic drugs, and anti-tumor necrosis factor therapy. Arthritis Rheum 2006; 54(2): 628-34.
[] [PMID: 16447241]
Gómez-Reino JJ, Carmona L, Valverde VR, Mola EM, Montero MD. Treatment of rheumatoid arthritis with tumor necrosis factor inhibitors may predispose to significant increase in tuberculosis risk: a multicenter active-surveillance report. Arthritis Rheum 2003; 48(8): 2122-7.
[] [PMID: 12905464]
BTS recommendations for assessing risk and for managing Mycobacterium tuberculosis infection and disease in patients due to start anti-TNF-alpha treatment. Thorax 2005; 60(10): 800-5.
[] [PMID: 16055611]
Kremer JM, Alarcón GS, Weinblatt ME, et al. Clinical, laboratory, radiographic, and histopathologic features of methotrexate-associated lung injury in patients with rheumatoid arthritis: a multicenter study with literature review. Arthritis Rheum 1997; 40(10): 1829-37.
[] [PMID: 9336418]
Conway R, Low C, Coughlan RJ, O’Donnell MJ, Carey JJ. Methotrexate and lung disease in rheumatoid arthritis: a meta-analysis of randomized controlled trials. Arthritis Rheumatol 2014; 66(4): 803-12.
[] [PMID: 24757133]
Md Yusof MY, Kabia A, Darby M, et al. Effect of rituximab on the progression of rheumatoid arthritis-related interstitial lung disease: 10 years’ experience at a single centre. Rheumatology (Oxford) 2017; 56(8): 1348-57.
[] [PMID: 28444364]
Md Yusof MY, Kabia A, Darby M, et al. Effect of rituximab on the progression of rheumatoid arthritis-related interstitial lung disease: 10 years’ experience at a single centre. Rheumatology (Oxford) 2017; 56(8): 1348-57.
[] [PMID: 28444364]
Mera-Varela A, Pérez-Pampín E. Abatacept therapy in rheumatoid arthritis with interstitial lung disease. J Clin Rheumatol 2014; 20(8): 445-6.
[] [PMID: 25417684]
Fernández-Díaz C, Loricera J, Castañeda S, et al. Abatacept in patients with rheumatoid arthritis and interstitial lung disease: A national multicenter study of 63 patients. Semin Arthritis Rheum 2018; 48(1): 22-7.
[] [PMID: 29422324]
Kimura Y, Weiss JE, Haroldson KL, et al. Childhood arthritis rheumatology research alliance carra net investigators. Pulmonary hypertension and other potentially fatal pulmonary complications in systemic juvenile idiopathic arthritis. Arthritis Care Res (Hoboken) 2013; 65(5): 745-52.
[] [PMID: 23139240]
Asquith DL, Miller AM, McInnes IB, Liew FY. Animal models of rheumatoid arthritis. Eur J Immunol 2009; 39(8): 2040-4.
[] [PMID: 19672892]
Sakaguchi N, Takahashi T, Hata H, et al. Altered thymic T-cell selection due to a mutation of the ZAP-70 gene causes autoimmune arthritis in mice. Nature 2003; 426(6965): 454-60.
[] [PMID: 14647385]
Sakaguchi S, et al. SKG mice, a new genetic model of rheumatoid arthritis. Arthritis Res Ther 2003; 5(Suppl. 3): S4.
Keith RC, Powers JL, Redente EF, et al. A novel model of rheumatoid arthritis-associated interstitial lung disease in SKG mice. Exp Lung Res 2012; 38(2): 55-66.
[] [PMID: 22185348]
Shiomi A, Usui T, Ishikawa Y, Shimizu M, Murakami K, Mimori T. GM-CSF but not IL-17 is critical for the development of severe interstitial lung disease in SKG mice. J Immunol 2014; 193(2): 849-59.
[] [PMID: 24951817]
Sendo S, Saegusa J, Okano T, Takahashi S, Akashi K, Morinobu A. CD11b+Gr-1dim Tolerogenic dendritic cell-like cells are expanded in interstitial lung disease in SKG mice. Arthritis Rheumatol 2017; 69(12): 2314-27.
[] [PMID: 28805019]
van Eden W, Wagenaar-Hilbers JP, Wauben MH. Adjuvant arthritis in the rat. In: Curr Protoc Immunol. 2001. 15: p. 15 4.
[] [PMID: 18432736]
Bendele A. Animal models of rheumatoid arthritis. J Musculoskelet Neuronal Interact 2001; 1(4): 377-85.
[PMID: 15758488]
Kim EY, Moudgil KD. The determinants of susceptibility/resistance to adjuvant arthritis in rats. Arthritis Res Ther 2009; 11(4): 239.
[] [PMID: 19678912]
Song LN, Kong XD, Wang HJ, Zhan LB. establishment of a rat adjuvant arthritis-interstitial lung disease model. BioMed Res Int 2016.20162970783
[] [PMID: 26881215]
Liu J, Wan L, Sheng CJ, Xie XL. [The correlative study on pulmonary function changes and Th1/Th2 cells & regulatory T cells in adjuvant arthritis rats]. . Xibao Yu Fenzi Mianyixue Zazhi 2011; 27(1): 56-60. [The correlative study on pulmonary function changes and Th1/Th2 cells & regulatory T cells in adjuvant arthritis rats].
[PMID: 21208566]
Wan L, Liu J, Huang C, et al. The reduced pulmonary function is related to the decreased expression of Treg and Foxp3 in adjuvant-induced arthritis rats. Xibao Yu Fenzi Mianyixue Zazhi 2013; 29(3): 251-5.
[PMID: 23643080]
Schurgers E, Mertens F, Vanoirbeek JA, et al. Pulmonary inflammation in mice with collagen-induced arthritis is conditioned by complete Freund’s adjuvant and regulated by endogenous IFN-γ. Eur J Immunol 2012; 42(12): 3223-34.
[] [PMID: 22930199]
Keffer J, Probert L, Cazlaris H, et al. Transgenic mice expressing human tumour necrosis factor: a predictive genetic model of arthritis. EMBO J 1991; 10(13): 4025-31.
[] [PMID: 1721867]
Bawadekar M, Gendron-Fitzpatrick A, Rebernick R, et al. Tumor necrosis factor alpha, citrullination, and peptidylarginine deiminase 4 in lung and joint inflammation. Arthritis Res Ther 2016; 18(1): 173.
[] [PMID: 27450561]
Douni E, Akassoglou K, Alexopoulou L, et al. Transgenic and knockout analyses of the role of TNF in immune regulation and disease pathogenesis. J Inflamm 1995-1996; 47(1-2): 27-38.
[PMID: 8913927]
Li P, Schwarz EM. The TNF-alpha transgenic mouse model of inflammatory arthritis. Springer Semin Immunopathol 2003; 25(1): 19-33.
[] [PMID: 12904889]
Shelef MA, Sokolove J, Lahey LJ, et al. Peptidylarginine deiminase 4 contributes to tumor necrosis factor α-induced inflammatory arthritis. Arthritis Rheumatol 2014; 66(6): 1482-91.
[] [PMID: 24497204]
Miyazaki Y, Araki K, Vesin C, et al. Expression of a tumor necrosis factor-alpha transgene in murine lung causes lymphocytic and fibrosing alveolitis. A mouse model of progressive pulmonary fibrosis. J Clin Invest 1995; 96(1): 250-9.
[] [PMID: 7542280]
Lundblad LK, Thompson-Figueroa J, Leclair T, et al. Tumor necrosis factor-alpha overexpression in lung disease: a single cause behind a complex phenotype. Am J Respir Crit Care Med 2005; 171(12): 1363-70.
[] [PMID: 15805183]
Klareskog L, Padyukov L, Rönnelid J, Alfredsson L. Genes, environment and immunity in the development of rheumatoid arthritis. Curr Opin Immunol 2006; 18(6): 650-5.
[] [PMID: 17010589]
Klareskog L, Padyukov L, Lorentzen J, Alfredsson L. Mechanisms of disease: Genetic susceptibility and environmental triggers in the development of rheumatoid arthritis. Nat Clin Pract Rheumatol 2006; 2(8): 425-33.
[] [PMID: 16932734]
Juge PA, Lee JS, Ebstein E, et al. MUC5B Promoter Variant and Rheumatoid Arthritis with Interstitial Lung Disease. N Engl J Med 2018; 379(23): 2209-19.
[] [PMID: 30345907]
Jawaheer D, Li W, Graham RR, et al. Dissecting the genetic complexity of the association between human leukocyte antigens and rheumatoid arthritis. Am J Hum Genet 2002; 71(3): 585-94.
[] [PMID: 12181776]
Migita K, Nakamura T, Koga T, Eguchi K. HLA-DRB1 alleles and rheumatoid arthritis-related pulmonary fibrosis. J Rheumatol 2010; 37(1): 205-7.
[] [PMID: 20040645]
Ennis H, Gupta A, Dawson J, Lunt M, Thomson W, Herrick A. HLA-DRB1 associations with rheumatoid arthritis-related pulmonary fibrosis. Scand J Rheumatol 2014; 43(1): 75-6.
[] [PMID: 24295149]
Klareskog L, Stolt P, Lundberg K, et al. A new model for an etiology of rheumatoid arthritis: smoking may trigger HLA-DR (shared epitope)-restricted immune reactions to autoantigens modified by citrullination. Arthritis Rheum 2006; 54(1): 38-46.
[] [PMID: 16385494]
Seibold MA, Wise AL, Speer MC, et al. A common MUC5B promoter polymorphism and pulmonary fibrosis. N Engl J Med 2011; 364(16): 1503-12.
[] [PMID: 21506741]
Zhang GY, Liao T, Gao WY. MUC5B promoter polymorphism and pulmonary fibrosis. N Engl J Med 2011; 365(2): 178.
[] [PMID: 21751917]
Zhang Y, Noth I, Garcia JG, Kaminski N. A variant in the promoter of MUC5B and idiopathic pulmonary fibrosis. N Engl J Med 2011; 364(16): 1576-7.
[] [PMID: 21506748]
Fingerlin TE, Murphy E, Zhang W, et al. Genome-wide association study identifies multiple susceptibility loci for pulmonary fibrosis. Nat Genet 2013; 45(6): 613-20.
[] [PMID: 23583980]
Noth I, Zhang Y, Ma SF, et al. Genetic variants associated with idiopathic pulmonary fibrosis susceptibility and mortality: a genome-wide association study. Lancet Respir Med 2013; 1(4): 309-17.
[] [PMID: 24429156]
Borie R, Crestani B, Dieude P, et al. The MUC5B variant is associated with idiopathic pulmonary fibrosis but not with systemic sclerosis interstitial lung disease in the European Caucasian population. PLoS One 2013; 8(8)e70621
[] [PMID: 23940607]
Horimasu Y, Ohshimo S, Bonella F, et al. MUC5B promoter polymorphism in Japanese patients with idiopathic pulmonary fibrosis. Respirology 2015; 20(3): 439-44.
[] [PMID: 25581455]
Lee MG, Lee YH. A meta-analysis examining the association between the MUC5B rs35705950 T/G polymorphism and susceptibility to idiopathic pulmonary fibrosis. Inflamm Res 2015; 64(6): 463-70.
[] [PMID: 25926289]
van der Vis JJ, Snetselaar R, Kazemier KM, ten Klooster L, Grutters JC, van Moorsel CH. Effect of Muc5b promoter polymorphism on disease predisposition and survival in idiopathic interstitial pneumonias. Respirology 2016; 21(4): 712-7.
[] [PMID: 26699835]
Juge PA, Borie R, Kannengiesser C, et al. Shared genetic predisposition in rheumatoid arthritis-interstitial lung disease and familial pulmonary fibrosis. Eur Respir J 2017; 49(5)1602314
[] [PMID: 28495692]
Shaw M, Collins BF, Ho LA, Raghu G. Rheumatoid arthritis-associated lung disease. Eur Respir Rev 2015; 24(135): 1-16.
[] [PMID: 25726549]
Kilsgård O, Andersson P, Malmsten M, et al. Peptidylarginine deiminases present in the airways during tobacco smoking and inflammation can citrullinate the host defense peptide LL-37, resulting in altered activities. Am J Respir Cell Mol Biol 2012; 46(2): 240-8.
[] [PMID: 21960546]
Makrygiannakis D, Hermansson M, Ulfgren AK, et al. Smoking increases peptidylarginine deiminase 2 enzyme expression in human lungs and increases citrullination in BAL cells. Ann Rheum Dis 2008; 67(10): 1488-92.
[] [PMID: 18413445]
Perry E, Kelly C, Eggleton P, De Soyza A, Hutchinson D. The lung in ACPA-positive rheumatoid arthritis: an initiating site of injury? Rheumatology (Oxford) 2014; 53(11): 1940-50.
[] [PMID: 24831057]
Nishimura K, Sugiyama D, Kogata Y, et al. Meta-analysis: diagnostic accuracy of anti-cyclic citrullinated peptide antibody and rheumatoid factor for rheumatoid arthritis. Ann Intern Med 2007; 146(11): 797-808.
[] [PMID: 17548411]
Bongartz T, Cantaert T, Atkins SR, et al. Citrullination in extra-articular manifestations of rheumatoid arthritis. Rheumatology (Oxford) 2007; 46(1): 70-5.
[] [PMID: 16782731]
Samara KD, Trachalaki A, Tsitoura E, et al. Upregulation of citrullination pathway: From autoimmune to idiopathic lung fibrosis. Respir Res 2017; 18(1): 218.
[] [PMID: 29287593]
Chang X, Yamada R, Suzuki A, et al. Localization of peptidylarginine deiminase 4 (PADI4) and citrullinated protein in synovial tissue of rheumatoid arthritis. Rheumatology (Oxford) 2005; 44(1): 40-50.
[] [PMID: 15466895]
Baeten D, Peene I, Union A, et al. Specific presence of intracellular citrullinated proteins in rheumatoid arthritis synovium: relevance to antifilaggrin autoantibodies. Arthritis Rheum 2001; 44(10): 2255-62.
[<2255:AID-ART388>3.0.CO;2-#] [PMID: 11665966]
Zhang Y, Li H, Wu N, Dong X, Zheng Y. Retrospective study of the clinical characteristics and risk factors of rheumatoid arthritis-associated interstitial lung disease. Clin Rheumatol 2017; 36(4): 817-23.
[] [PMID: 28191607]
Vassallo R, Luckey D, Behrens M, et al. Cellular and humoral immunity in arthritis are profoundly influenced by the interaction between cigarette smoke effects and host HLA-DR and DQ genes. Clin Immunol 2014; 152(1-2): 25-35.
[] [PMID: 24631425]
Svärd A, Skogh T, Alfredsson L, et al. Associations with smoking and shared epitope differ between IgA- and IgG-class antibodies to cyclic citrullinated peptides in early rheumatoid arthritis. Arthritis Rheumatol 2015; 67(8): 2032-7.
[] [PMID: 25916813]
Kokkonen H, Brink M, Hansson M, et al. Associations of antibodies against citrullinated peptides with human leukocyte antigen-shared epitope and smoking prior to the development of rheumatoid arthritis. Arthritis Res Ther 2015; 17: 125.
[] [PMID: 25990747]
Lee YH, Bae SC, Song GG. Gene-environmental interaction between smoking and shared epitope on the development of anti-cyclic citrullinated peptide antibodies in rheumatoid arthritis: a meta-analysis. Int J Rheum Dis 2014; 17(5): 528-35.
[] [PMID: 24618101]
Lugli EB, Correia RE, Fischer R, et al. Expression of citrulline and homocitrulline residues in the lungs of non-smokers and smokers: implications for autoimmunity in rheumatoid arthritis. Arthritis Res Ther 2015; 17: 9.
[] [PMID: 25600626]
Terao C, Ohmura K, Ikari K, et al. Effects of smoking and shared epitope on the production of anti-citrullinated peptide antibody in a Japanese adult population. Arthritis Care Res (Hoboken) 2014; 66(12): 1818-27.
[] [PMID: 24942650]
Terao C, Suzuki A, Ikari K, et al. An association between amino acid position 74 of HLA-DRB1 and anti-citrullinated protein antibody levels in Japanese patients with anti-citrullinated protein antibody-positive rheumatoid arthritis. Arthritis Rheumatol 2015; 67(8): 2038-45.
[] [PMID: 25832994]
Chang K, Yang SM, Kim SH, Han KH, Park SJ, Shin JI. Smoking and rheumatoid arthritis. Int J Mol Sci 2014; 15(12): 22279-95.
[] [PMID: 25479074]
Sparks JA, Chang SC, Nguyen UDT, et al. Smoking behavior changes in the early rheumatoid arthritis period and risk of mortality during thirty-six years of prospective followup. Arthritis Care Res (Hoboken) 2018; 70(1): 19-29.
[] [PMID: 28464477]
Sparks JA, Chang SC, Deane KD, et al. Associations of Smoking and Age With Inflammatory Joint Signs Among Unaffected First-Degree Relatives of Rheumatoid Arthritis Patients: Results From Studies of the Etiology of Rheumatoid Arthritis. Arthritis Rheumatol 2016; 68(8): 1828-38.
[] [PMID: 26866831]
Källberg H, Ding B, Padyukov L, et al. Smoking is a major preventable risk factor for rheumatoid arthritis: estimations of risks after various exposures to cigarette smoke. Ann Rheum Dis 2011; 70(3): 508-11.
[] [PMID: 21149499]
Reynisdottir G, Karimi R, Joshua V, et al. Structural changes and antibody enrichment in the lungs are early features of anti-citrullinated protein antibody-positive rheumatoid arthritis. Arthritis Rheumatol 2014; 66(1): 31-9.
[] [PMID: 24449573]
Pereira DA, Kawassaki Ade M, Baldi BG. Interpretation of autoantibody positivity in interstitial lung disease and lung-dominant connective tissue disease. J Bras Pneumol 2013; 39(6): 728-41.
[] [PMID: 24473767]

Rights & Permissions Print Export Cite as
© 2022 Bentham Science Publishers | Privacy Policy